Articles | Volume 6, issue 1
https://doi.org/10.5194/pb-6-17-2019
© Author(s) 2019. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
https://doi.org/10.5194/pb-6-17-2019
© Author(s) 2019. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
Review article
| 
10 May 2019
Review article |
| 10 May 2019
| 10 May 2019
Experimental autoimmune encephalomyelitis in the common marmoset: a translationally relevant model for the cause and course of multiple sclerosis
Bert A. 't Hart
Department of Immunobiology, Biomedical Primate Research Centre,
Rijswijk, the Netherlands
Department of Biomedical Sciences of Cells and Systems, University Medical Center Groningen, the Netherlands
Related subject area
Immunology
Use of nonhuman primates in obstructive lung disease research – is it required?
The common marmoset (Callithrix jacchus): a relevant preclinical model of human (auto)immune-mediated inflammatory disease of the brain
Franziska Dahlmann and Katherina Sewald
Primate Biol., 4, 131–142, https://doi.org/10.5194/pb-4-131-2017, https://doi.org/10.5194/pb-4-131-2017, 2017
Bert A. 't Hart, Jordon Dunham, S. Anwar Jagessar, and Yolanda S. Kap
Primate Biol., 3, 9–22, https://doi.org/10.5194/pb-3-9-2016, https://doi.org/10.5194/pb-3-9-2016, 2016
Short summary
Short summary
The increasing prevalence of chronic autoimmune inflammatory disorders (AIMIDs) in aging human populations creates a high unmet need for safe and effective medications. However, thus far the translation of pathogenic concepts developed in animal models into effective treatments for the patient has been notoriously difficult. The main reason is that currently used mouse-based animal models for the pipeline selection of promising new treatments were insufficiently predictive for clinical success.
Cited articles
Absinta, M., Sati, P., and Reich, D. S.: Advanced MRI and staging of
multiple sclerosis lesions, Nat. Rev. Neurol., 12, 358–368,
https://doi.org/10.1038/nrneurol.2016.59, 2016.
Absinta, M., Ha, S. K., Nair, G., Sati, P., Luciano, N. J., Palisoc, M.,
Louveau, A., Zaghloul, K. A., Pittaluga, S., Kipnis, J., and Reich, D. S.:
Human and nonhuman primate meninges harbor lymphatic vessels that can be
visualized noninvasively by MRI, Elife, 6, e29738, https://doi.org/10.7554/eLife.29738, 2017.
Antunes, S. G., de Groot, N. G., Brok, H., Doxiadis, G., Menezes, A. A.,
Otting, N., and Bontrop, R. E.: The common marmoset: a new world primate
species with limited Mhc class II variability, P. Natl. Acad. Sci. USA, 95,
11745–11750, 1998.
Araman, C., van Gent, M., Meeuwenoord, N., Heijmans, N., Marqvorsen, H. S.,
Faber, B. W., 't Hart, B. A., and van Kasteren, S. I.: Amyloid-like behavior
of site-specific citrullinated myelin oligodendrocyte protein (MOG) peptide
fragments inside EBV infected B-cells influences their cytotoxicity and
autoimmunogenicty, Biochemistry, 58, 763–775, https://doi.org/10.1021/acs.biochem.8b00852, 2019.
Ascherio, A. and Munger, K. L.: Environmental risk factors for multiple
sclerosis. Part II: Noninfectious factors, Ann. Neurol., 61, 504–513, 2007.
Ascherio, A., Munger, K. L., and Lunemann, J. D.: The initiation and
prevention of multiple sclerosis, Nat. Rev. Neurol., 8, 602–612,
https://doi.org/10.1038/nrneurol.2012.198, 2012.
Aspelund, A., Antila, S., Proulx, S. T., Karlsen, T. V., Karaman, S.,
Detmar, M., Wiig, H., and Alitalo, K.: A dural lymphatic vascular system
that drains brain interstitial fluid and macromolecules, J. Exp. Med., 212,
991–999, https://doi.org/10.1084/jem.20142290, 2015.
Axtell, R. C., de Jong, B. A., Boniface, K., van der Voort, L. F., Bhat, R.,
De Sarno, P., Naves, R., Han, M., Zhong, F., Castellanos, J. G., Mair, R.,
Christakos, A., Kolkowitz, I., Katz, L., Killestein, J., Polman, C. H., de
Waal Malefyt, R., Steinman, L., and Raman, C.: T helper type 1 and 17 cells
determine efficacy of interferon-beta in multiple sclerosis and experimental
encephalomyelitis, Nat. Med., 16, 406–412,
https://doi.org/10.1038/nm.2110, 2010.
Axthelm, M. K., Bourdette, D. N., Marracci, G. H., Su, W., Mullaney, E. T.,
Manoharan, M., Kohama, S. G., Pollaro, J., Witkowski, E., Wang, P., Rooney,
W. D., Sherman, L. S., and Wong, S. W.: Japanese macaque encephalomyelitis:
a spontaneous multiple sclerosis-like disease in a nonhuman primate, Ann. Neurol., 70, 362–373, https://doi.org/10.1002/ana.22449, 2011.
Bacchetti, P., Wolf, L. E., Segal, M. R., and McCulloch, C. E.: Ethics and
sample size, Am. J. Epidemiol., 161, 105–110,
https://doi.org/10.1093/aje/kwi014, 2005.
Bacchetti, P., Deeks, S. G., and McCune, J. M.: Breaking free of sample size
dogma to perform innovative translational research, Sci. Transl. Med., 3,
87ps24, https://doi.org/10.1126/scitranslmed.3001628, 2011.
Bacchetti, P., McCulloch, C., and Segal, M. R.: Being “underpowered” does
not make a study unethical, Stat. Med., 31, 4138–4139,
https://doi.org/10.1002/sim.5451, 2012.
Barnett, M. H. and Prineas, J. W.: Relapsing and remitting multiple
sclerosis: pathology of the newly forming lesion, Ann. Neurol., 55, 458–468,
2004.
Bartzokis, G.: Age-related myelin breakdown: a developmental model of
cognitive decline and Alzheimer's disease, Neurobiol. Aging, 25, 5–18, 2004.
Barun, B. and Bar-Or, A.: Treatment of multiple sclerosis with Anti-CD20
antibodies, Clin. Immunol., 142, 31–37, https://doi.org/10.1016/j.clim.2011.04.005, 2012.
Berer, K., Mues, M., Koutrolos, M., Rasbi, Z. A., Boziki, M., Johner, C.,
Wekerle, H., and Krishnamoorthy, G.: Commensal microbiota and myelin
autoantigen cooperate to trigger autoimmune demyelination, Nature, 479,
538–541, https://doi.org/10.1038/nature10554, 2011.
Beura, L. K., Hamilton, S. E., Bi, K., Schenkel, J. M., Odumade, O. A.,
Casey, K. A., Thompson, E. A., Fraser, K. A., Rosato, P. C., Filali-Mouhim,
A., Sekaly, R. P., Jenkins, M. K., Vezys, V., Haining, W. N., Jameson, S.
C., and Masopust, D.: Normalizing the environment recapitulates adult human
immune traits in laboratory mice, Nature, 532, 512–516, https://doi.org/10.1038/nature17655,
2016.
Bielekova, B., Sung, M. H., Kadom, N., Simon, R., McFarland, H., and Martin,
R.: Expansion and functional relevance of high-avidity myelin-specific
CD4+ T cells in multiple sclerosis, J. Immunol., 172, 3893–3904, 2004.
Billiau, A. and Matthys, P.: Modes of action of Freund's adjuvants in
experimental models of autoimmune diseases, J. Leukocyte Biol., 70, 849–860,
2001.
Birgisdottir, A. B., Lamark, T., and Johansen, T.: The LIR motif – crucial
for selective autophagy, J. Cell Sci., 126, 3237–3247, https://doi.org/10.1242/jcs.126128,
2013.
Blair, T. C., Manoharan, M., Rawlings-Rhea, S. D., Tagge, I., Kohama, S. G.,
Hollister-Smith, J., Ferguson, B., Woltjer, R. L., Frederick, M. C.,
Pollaro, J., Rooney, W. D., Sherman, L. S., Bourdette, D. N., and Wong, S.
W.: Immunopathology of Japanese macaque encephalomyelitis is similar to
multiple sclerosis, J. Neuroimmunol., 291, 1–10,
https://doi.org/10.1016/j.jneuroim.2015.11.026, 2016.
Blezer, E. L., Bauer, J., Brok, H. P., Nicolay, K., and 't Hart, B. A.:
Quantitative MRI-pathology correlations of brain white matter lesions
developing in a non-human primate model of multiple sclerosis, NMR Biomed.,
20, 90–103, 2007.
Boon, L., Laman, J. D., Ortiz-Buijsse, A., den Hartog, M. T., Hoffenberg,
S., Liu, P., Shiau, F., and de Boer, M.: Preclinical assessment of anti-CD40
Mab 5D12 in cynomolgus monkeys, Toxicology, 174, 53–65, 2002.
Bradford, C. M., Ramos, I., Cross, A. K., Haddock, G., McQuaid, S.,
Nicholas, A. P., and Woodroofe, M. N.: Localisation of citrullinated
proteins in normal appearing white matter and lesions in the central nervous
system in multiple sclerosis, J. Neuroimmunol., 273, 85–95,
https://doi.org/10.1016/j.jneuroim.2014.05.007, 2014.
Breithaupt, C., Schubart, A., Zander, H., Skerra, A., Huber, R., Linington,
C., and Jacob, U.: Structural insights into the antigenicity of myelin
oligodendrocyte glycoprotein, P. Natl. Acad. Sci. USA, 100, 9446–9451,
https://doi.org/10.1073/pnas.1133443100, 2003.
Brodin, P. and Davis, M. M.: Human immune system variation, Nat. Rev. Immunol., 17, 21–29, https://doi.org/10.1038/nri.2016.125, 2017.
Brok, H. P., Uccelli, A., Kerlero De Rosbo, N., Bontrop, R. E.,
Roccatagliata, L., de Groot, N. G., Capello, E., Laman, J. D., Nicolay, K.,
Mancardi, G. L., Ben-Nun, A., and 't Hart, B. A.: Myelin/oligodendrocyte
glycoprotein-induced autoimmune encephalomyelitis in common marmosets: the
encephalitogenic T cell epitope pMOG24-36 is presented by a monomorphic MHC
class II molecule, J. Immunol., 165, 1093–1101, 2000.
Brok, H. P., Bauer, J., Jonker, M., Blezer, E., Amor, S., Bontrop, R. E.,
Laman, J. D., and 't Hart, B. A.: Non-human primate models of multiple
sclerosis, Immunol. Rev., 183, 173–185, 2001.
Brok, H. P., Van Meurs, M., Blezer, E., Schantz, A., Peritt, D., Treacy, G.,
Laman, J. D., Bauer, J., and 't Hart, B.: Prevention of experimental
autoimmune encephalomyelitis in common marmosets using an anti-IL-12p40
monoclonal antibody, J. Immunol., 169, 6554–6563, 2002.
Brok, H. P., Boven, L., van Meurs, M., Kerlero de Rosbo, N., Celebi-Paul,
L., Kap, Y. S., Jagessar, A., Hintzen, R. Q., Keir, G., Bajramovic, J.,
Ben-Nun, A., Bauer, J., Laman, J. D., Amor, S., and 't Hart, B. A.: The
human CMV-UL86 peptide 981-1003 shares a crossreactive T-cell epitope with
the encephalitogenic MOG peptide 34–56, but lacks the capacity to induce EAE
in rhesus monkeys, J. Neuroimmunol., 182, 135–152,
https://doi.org/10.1016/j.jneuroim.2006.10.010, 2007.
Burm, S. M., Peferoen, L. A., Zuiderwijk-Sick, E. A., Haanstra, K. G., 't
Hart, B. A., van der Valk, P., Amor, S., Bauer, J., and Bajramovic, J. J.:
Expression of IL-1beta in rhesus EAE and MS lesions is mainly induced in the
CNS itself, J. Neuroinflamm., 13, 138, https://doi.org/10.1186/s12974-016-0605-8, 2016.
Burster, T., Beck, A., Tolosa, E., Marin-Esteban, V., Rotzschke, O., Falk,
K., Lautwein, A., Reich, M., Brandenburg, J., Schwarz, G., Wiendl, H.,
Melms, A., Lehmann, R., Stevanovic, S., Kalbacher, H., and Driessen, C.:
Cathepsin G, and not the asparagine-specific endoprotease, controls the
processing of myelin basic protein in lysosomes from human B lymphocytes, J. Immunol., 172, 5495–5503, 2004.
Caldwell, R. G., Wilson, J. B., Anderson, S. J., and Longnecker, R.:
Epstein-Barr virus LMP2A drives B cell development and survival in the
absence of normal B cell receptor signals, Immunity, 9, 405–411, 1998.
Camilli, G., Cassotta, A., Battella, S., Palmieri, G., Santoni, A.,
Paladini, F., Fiorillo, M. T., and Sorrentino, R.: Regulation and
trafficking of the HLA-E molecules during monocyte-macrophage
differentiation, J. Leukocyte Biol., 99, 121–130, https://doi.org/10.1189/jlb.1A0415-172R, 2016.
Caprariello, A. V., Rogers, J. A., Morgan, M. L., Hoghooghi, V., Plemel, J.
R., Koebel, A., Tsutsui, S., Dunn, J. F., Kotra, L. P., Ousman, S. S., Wee
Yong, V., and Stys, P. K.: Biochemically altered myelin triggers autoimmune
demyelination, P. Natl. Acad. Sci. USA, 115, 5528–5533,
https://doi.org/10.1073/pnas.1721115115, 2018.
Carrillo-Vico, A., Leech, M. D., and Anderton, S. M.: Contribution of myelin
autoantigen citrullination to T cell autoaggression in the central nervous
system, J. Immunol., 184, 2839–2846, https://doi.org/10.4049/jimmunol.0903639, 2010.
Carville, A. and Mansfield, K. G.: Comparative pathobiology of macaque
lymphocryptoviruses, Comp. Med., 58, 57–67, 2008.
Chirivi, R. G. S., van Rosmalen, J. W. G., Jenniskens, G. J., Pruijn, G. J.,
and Raats, J. M. H.: Citrullination: a target for disease intervention in
multiple sclerosis and other inflammatory diseases?, J. Clin. Cell. Immunol., 4,
146–153, 2013.
Choi, S. R., Howell, O. W., Carassiti, D., Magliozzi, R., Gveric, D.,
Muraro, P. A., Nicholas, R., Roncaroli, F., and Reynolds, R.: Meningeal
inflammation plays a role in the pathology of primary progressive multiple
sclerosis, Brain, 135, 2925–2937, https://doi.org/10.1093/brain/aws189, 2012.
Collins, B. E., Yang, L. J., Mukhopadhyay, G., Filbin, M. T., Kiso, M.,
Hasegawa, A., and Schnaar, R. L.: Sialic acid specificity of
myelin-associated glycoprotein binding, J. Biol. Chem., 272, 1248–1255, 1997.
Collins, B. E., Fralich, T. J., Itonori, S., Ichikawa, Y., and Schnaar, R.
L.: Conversion of cellular sialic acid expression from N-acetyl- to
N-glycolylneuraminic acid using a synthetic precursor, N-glycolylmannosamine
pentaacetate: inhibition of myelin-associated glycoprotein binding to neural
cells, Glycobiology, 10, 11–20, 2000.
Compston, A. and Coles, A.: Multiple sclerosis, Lancet, 372, 1502–1517,
2008.
Damsker, J. M., Hansen, A. M., and Caspi, R. R.: Th1 and Th17 cells:
adversaries and collaborators, Ann. NY Acad. Sci., 1183, 211–221,
https://doi.org/10.1111/j.1749-6632.2009.05133.x, 2010.
Davis, M. M.: A prescription for human immunology, Immunity, 29, 835–838,
https://doi.org/10.1016/j.immuni.2008.12.003, 2008.
Delamarre, L., Couture, R., Mellman, I., and Trombetta, E. S.: Enhancing
immunogenicity by limiting susceptibility to lysosomal proteolysis, J. Exp. Med., 203, 2049–2055, https://doi.org/10.1084/jem.20052442, 2006.
Delarasse, C., Daubas, P., Mars, L. T., Vizler, C., Litzenburger, T.,
Iglesias, A., Bauer, J., Della Gaspera, B., Schubart, A., Decker, L.,
Dimitri, D., Roussel, G., Dierich, A., Amor, S., Dautigny, A., Liblau, R.,
and Pham-Dinh, D.: Myelin/oligodendrocyte glycoprotein-deficient
(MOG-deficient) mice reveal lack of immune tolerance to MOG in wild-type
mice, J. Clin. Invest., 112, 544–553, 2003.
de Vos, A. F., van Meurs, M., Brok, H. P., Boven, L. A., Hintzen, R. Q., van
der Valk, P., Ravid, R., Rensing, S., Boon, L., 't Hart, B. A., and Laman,
J. D.: Transfer of central nervous system autoantigens and presentation in
secondary lymphoid organs, J. Immunol., 169, 5415–5423, 2002.
Dillon, S. R., Gross, J. A., Ansell, S. M., and Novak, A. J.: An APRIL to
remember: novel TNF ligands as therapeutic targets, Nat. Rev. Drug Discov., 5,
235–246, https://doi.org/10.1038/nrd1982, 2006.
Di Ruscio, A., Patti, F., Welner, R. S., Tenen, D. G., and Amabile, G.:
Multiple sclerosis: getting personal with induced pluripotent stem cells,
Cell Death Dis., 6, e1806, https://doi.org/10.1038/cddis.2015.179, 2015.
Doxiadis, G. G., van der Wiel, M. K., Brok, H. P., de Groot, N. G., Otting,
N., 't Hart, B. A., van Rood, J. J., and Bontrop, R. E.: Reactivation by
exon shuffling of a conserved HLA-DR3-like pseudogene segment in a New World
primate species, P. Natl. Acad. Sci. USA, 103, 5864–5868, 2006.
Dunham, J., Lee, L. F., van Driel, N., Laman, J. D., Ni, I., Zhai, W., Tu,
G. H., Lin, J. C., Bauer, J., 't Hart, B. A., and Kap, Y. S.: Blockade of
CD127 Exerts a Dichotomous Clinical Effect in Marmoset Experimental
Autoimmune Encephalomyelitis, J. Neuroimmune Pharm., 11, 73–83,
https://doi.org/10.1007/s11481-015-9629-6, 2016.
Dunham, J., Bauer, J., Campbell, G. R., Mahad, D. J., van Driel, N., van der
Pol, S. M. A., 't Hart, B. A., Lassmann, H., Laman, J. D., van Horssen, J.,
and Kap, Y. S.: Oxidative Injury and Iron Redistribution Are Pathological
Hallmarks of Marmoset Experimental Autoimmune Encephalomyelitis, J. Neuropath. Exp. Neur., 76, 467–478, https://doi.org/10.1093/jnen/nlx034, 2017a.
Dunham, J., van de Vis, R., Bauer, J., Wubben, J., van Driel, N., Laman, J.
D., 't Hart, B. A., and Kap, Y. S.: Severe oxidative stress in an acute
inflammatory demyelinating model in the rhesus monkey, PLoS ONE, 12,
e0188013, https://doi.org/10.1371/journal.pone.0188013, 2017b.
Dunham, J., van Driel, N., Eggen, B. J., Paul, C., 't Hart, B. A., Laman, J.
D., and Kap, Y. S.: Analysis of the cross-talk of Epstein-Barr
virus-infected B cells with T cells in the marmoset, Clinical & translational immunology, 6, e127, https://doi.org/10.1038/cti.2017.1, 2017c.
Editorial: Editorial: A milestone in multiple sclerosis, Lancet, 1, 459–460,
1976.
Ehlers, B., Spiess, K., Leendertz, F., Peeters, M., Boesch, C., Gatherer,
D., and McGeoch, D. J.: Lymphocryptovirus phylogeny and the origins of
Epstein-Barr virus, J. Gen. Virol., 91, 630–642, https://doi.org/10.1099/vir.0.017251-0, 2010.
Frohman, E. M., Racke, M. K., and Raine, C. S.: Multiple sclerosis–the
plaque and its pathogenesis, N. Engl. J. Med., 354, 942–955, 2006.
Fujinami, R. S., von Herrath, M. G., Christen, U., and Whitton, J. L.:
Molecular mimicry, bystander activation, or viral persistence: infections
and autoimmune disease, Clin. Microbiol. Rev., 19, 80–94, https://doi.org/10.1128/CMR.19.1.80-94.2006, 2006.
Garcia-Vallejo, J. J., Ilarregui, J. M., Kalay, H., Chamorro, S., Koning,
N., Unger, W. W., Ambrosini, M., Montserrat, V., Fernandes, R. J., Bruijns,
S. C., van Weering, J. R., Paauw, N. J., O'Toole, T., van Horssen, J., van
der Valk, P., Nazmi, K., Bolscher, J. G., Bajramovic, J., Dijkstra, C. D.,
't Hart, B. A., and van Kooyk, Y.: CNS myelin induces regulatory functions
of DC-SIGN-expressing, antigen-presenting cells via cognate interaction with
MOG, J. Exp. Med., 211, 1465–1483, https://doi.org/10.1084/jem.20122192, 2014.
Gardner, C., Magliozzi, R., Durrenberger, P. F., Howell, O. W., Rundle, J.,
and Reynolds, R.: Cortical grey matter demyelination can be induced by
elevated pro-inflammatory cytokines in the subarachnoid space of
MOG-immunized rats, Brain, 136, 3596–3608, https://doi.org/10.1093/brain/awt279, 2013.
Geijtenbeek, T. B., Van Vliet, S. J., Engering, A., 't Hart, B. A., and Van
Kooyk, Y.: Self- and Nonself-Recognition by C-Type Lectins on Dendritic
Cells, Annu. Rev. Immunol., 22, 33–54, 2004.
Genain, C. P. and Hauser, S. L.: Experimental allergic encephalomyelitis in
the New World monkey Callithrix jacchus, Immunol. Rev., 183, 159–172, 2001.
Genain, C. P., Nguyen, M. H., Letvin, N. L., Pearl, R., Davis, R. L.,
Adelman, M., Lees, M. B., Linington, C., and Hauser, S. L.: Antibody
facilitation of multiple sclerosis-like lesions in a nonhuman primate, J. Clin. Invest., 96, 2966–2974, 1995.
Genain, C. P., Cannella, B., Hauser, S. L., and Raine, C. S.: Identification
of autoantibodies associated with myelin damage in multiple sclerosis, Nat. Med., 5, 170–175, 1999.
Geurts, J. J. and Barkhof, F.: Grey matter pathology in multiple sclerosis,
Lancet Neurol., 7, 841–851, 2008.
Gold, R., Linington, C., and Lassmann, H.: Understanding pathogenesis and
therapy of multiple sclerosis via animal models: 70 years of merits and
culprits in experimental autoimmune encephalomyelitis research, Brain, 129,
1953–1971, 2006.
Goronzy, J. J. and Weyand, C. M.: Understanding immunosenescence to improve
responses to vaccines, Nat. Immunol., 14, 428–436, https://doi.org/10.1038/ni.2588, 2013.
Gran, B., Zhang, G. X., and Rostami, A.: Role of the IL-12/IL-23 system in
the regulation of T-cell responses in central nervous system inflammatory
demyelination, Crit. Rev. Immunol., 24, 111–128, 2004.
Haanstra, K. G., Hofman, S. O., Lopes Estevao, D. M., Blezer, E. L., Bauer,
J., Yang, L. L., Wyant, T., Csizmadia, V., 't Hart, B. A., and Fedyk, E. R.:
Antagonizing the alpha4beta1 integrin, but not alpha4beta7, inhibits
leukocytic infiltration of the central nervous system in rhesus monkey
experimental autoimmune encephalomyelitis, J. Immunol., 190, 1961–1973,
https://doi.org/10.4049/jimmunol.1202490, 2013a.
Haanstra, K. G., Jagessar, S. A., Bauchet, A. L., Doussau, M., Fovet, C. M.,
Heijmans, N., Hofman, S. O., van Lubeek-Veth, J., Bajramovic, J. J., Kap, Y.
S., Laman, J. D., Touin, H., Watroba, L., Bauer, J., Lachapelle, F.,
Serguera, C., and 't Hart, B. A.: Induction of Experimental Autoimmune
Encephalomyelitis With Recombinant Human Myelin Oligodendrocyte Glycoprotein
in Incomplete Freund's Adjuvant in Three Non-human Primate Species, J. Neuroimmune Pharm., 8, 1251–1264, https://doi.org/10.1007/s11481-013-9487-z, 2013b.
Haanstra, K. G., Wubben, J. A., Jonker, M., and 't Hart, B. A.: Induction of
Encephalitis in Rhesus Monkeys Infused with Lymphocryptovirus-Infected
B-Cells Presenting MOG34-56 Peptide, PLoS ONE, 8, e71549,
https://doi.org/10.1371/journal.pone.0071549, 2013c.
Haanstra, K. G., Dijkman, K., Bashir, N., Bauer, J., Mary, C., Poirier, N.,
Baker, P., Scobie, L., 't Hart, B. A., and Vanhove, B.: Selective Blockade of
CD28-Mediated T Cell Costimulation Protects Rhesus Monkeys against Acute
Fatal Experimental Autoimmune Encephalomyelitis, J. Immunol., 194, 1454–1466,
https://doi.org/10.4049/jimmunol.1402563, 2015.
Haig, D.: What is a marmoset?, Am. J. Primatol., 49, 285–296, 1999.
Hauser, S. L., Waubant, E., Arnold, D. L., Vollmer, T., Antel, J., Fox, R.
J., Bar-Or, A., Panzara, M., Sarkar, N., Agarwal, S., Langer-Gould, A., and
Smith, C. H.: B-cell depletion with rituximab in relapsing-remitting
multiple sclerosis, N. Engl. J. Med., 358, 676–688, 2008.
Heneka, M. T., Kummer, M. P., Stutz, A., Delekate, A., Schwartz, S.,
Vieira-Saecker, A., Griep, A., Axt, D., Remus, A., Tzeng, T. C., Gelpi, E.,
Halle, A., Korte, M., Latz, E., and Golenbock, D. T.: NLRP3 is activated in
Alzheimer's disease and contributes to pathology in APP/PS1 mice, Nature,
493, 674–678, https://doi.org/10.1038/nature11729, 2013.
Hohlfeld, R. and Wekerle, H.: Autoimmune concepts of multiple sclerosis as
a basis for selective immunotherapy: from pipe dreams to (therapeutic)
pipelines, P. Natl. Acad. Sci. USA, 101, 14599–14606, 2004.
Hohlfeld, R., Dornmair, K., Meinl, E., and Wekerle, H.: The search for the
target antigens of multiple sclerosis, part 1: autoreactive CD4+ T
lymphocytes as pathogenic effectors and therapeutic targets, Lancet Neurol.,
15, 198–209, https://doi.org/10.1016/S1474-4422(15)00334-8, 2015.
Howell, O. W., Reeves, C. A., Nicholas, R., Carassiti, D., Radotra, B.,
Gentleman, S. M., Serafini, B., Aloisi, F., Roncaroli, F., Magliozzi, R.,
and Reynolds, R.: Meningeal inflammation is widespread and linked to
cortical pathology in multiple sclerosis, Brain, 134, 2755–2771,
https://doi.org/10.1093/brain/awr182, 2011.
Hunter, C. A.: New IL-12-family members: IL-23 and IL-27, cytokines with
divergent functions, Nat. Rev. Immunol., 5, 521–531, 2005.
Igci, M., Baysan, M., Yigiter, R., Ulasli, M., Geyik, S., Bayraktar, R.,
Bozgeyik, I., Bozgeyik, E., Bayram, A., and Cakmak, E. A.: Gene expression
profiles of autophagy-related genes in multiple sclerosis, Gene, 588, 38–46,
https://doi.org/10.1016/j.gene.2016.04.042, 2016.
Ireland, J. M. and Unanue, E. R.: Autophagy in antigen-presenting cells
results in presentation of citrullinated peptides to CD4 T cells, J. Exp. Med.,
208, 2625–2632, https://doi.org/10.1084/jem.20110640, 2011.
Ireland, J. M. and Unanue, E. R.: Processing of proteins in autophagy
vesicles of antigen-presenting cells generates citrullinated peptides
recognized by the immune system, Autophagy, 8, 429–430, https://doi.org/10.4161/auto.19261,
2012.
Jagessar, S. A., Smith, P. A., Blezer, E., Delarasse, C., Pham-Dinh, D.,
Laman, J. D., Bauer, J., Amor, S., and 't Hart, B.: Autoimmunity against
myelin oligodendrocyte glycoprotein is dispensable for the initiation
although essential for the progression of chronic encephalomyelitis in
common marmosets, J. Neuropath. Exp. Neur., 67, 326–340, 2008.
Jagessar, S. A., Kap, Y. S., Heijmans, N., van Driel, N., van Straalen, L.,
Bajramovic, J. J., Brok, H. P., Blezer, E. L., Bauer, J., Laman, J. D., and
't Hart, B. A.: Induction of progressive demyelinating autoimmune
encephalomyelitis in common marmoset monkeys using MOG34-56 peptide in
incomplete freund adjuvant, J. Neuropath. Exp. Neur., 69, 372–385,
https://doi.org/10.1097/NEN.0b013e3181d5d053, 2010.
Jagessar, S. A., Gran, B., Heijmans, N., Bauer, J., Laman, J. D., 't Hart,
B. A., and Constantinescu, C. S.: Discrepant effects of human
interferon-gamma on clinical and immunological disease parameters in a novel
marmoset model for multiple sclerosis, J. Neuroimmune Pharm., 7, 253–265,
https://doi.org/10.1007/s11481-011-9320-5, 2012a.
Jagessar, S. A., Heijmans, N., Bauer, J., Blezer, E. L., Laman, J. D.,
Hellings, N., and 't Hart, B. A.: B-cell depletion abrogates T cell-mediated
demyelination in an antibody-nondependent common marmoset experimental
autoimmune encephalomyelitis model, J. Neuropath. Exp. Neur., 71, 716–728,
https://doi.org/10.1097/NEN.0b013e3182622691, 2012b.
Jagessar, S. A., Heijmans, N., Bauer, J., Blezer, E. L., Laman, J. D.,
Migone, T. S., Devalaraja, M. N., and 't Hart, B. A.: Antibodies against
human BLyS and APRIL attenuate EAE development in marmoset monkeys, J. Neuroimmune Pharm., 7, 557–570, https://doi.org/10.1007/s11481-012-9384-x, 2012c.
Jagessar, S. A., Heijmans, N., Blezer, E. L., Bauer, J., Blokhuis, J. H.,
Wubben, J. A., Drijfhout, J. W., van den Elsen, P. J., Laman, J. D., and 't
Hart, B. A.: Unravelling the T-cell-mediated autoimmune attack on CNS myelin
in a new primate EAE model induced with MOG34-56 peptide in incomplete
adjuvant, Eur J. Immunol., 42, 217–227, https://doi.org/10.1002/eji.201141863, 2012d.
Jagessar, S. A., Heijmans, N., Oh, L., Bauer, J., Blezer, E. L., Laman, J.
D., Migone, T. S., Devalaraja, M. N., and 't Hart, B. A.: Antibodies against
human BLyS and APRIL attenuate EAE development in marmoset monkeys, J. Neuroimmune Pharm., 7, 557–570, https://doi.org/10.1007/s11481-012-9384-x, 2012e.
Jagessar, S. A., Fagrouch, Z., Heijmans, N., Bauer, J., Laman, J. D., Oh,
L., Migone, T., Verschoor, E. J., and 't Hart, B. A.: The different clinical
effects of anti-BLyS, anti-APRIL and anti-CD20 antibodies point at a
critical pathogenic role of gamma-herpesvirus infected B cells in the
marmoset EAE model, J. Neuroimmune Pharm., 8, 727–738,
https://doi.org/10.1007/s11481-013-9448-6, 2013a.
Jagessar, S. A., Vierboom, M., Blezer, E. L., Bauer, J., 't Hart, B. A., and
Kap, Y. S.: Overview of models, methods, and reagents developed for
translational autoimmunity research in the common marmoset (Callithrix
jacchus), Experimental animals/Japanese Association for Laboratory Animal
Science, 62, 159–171, 2013b.
Jagessar, S. A., Heijmans, N., Blezer, E. L., Bauer, J., Weissert, R., and 't
Hart, B. A.: Immune profile of an atypical EAE model in marmoset monkeys
immunized with recombinant human myelin oligodendrocyte glycoprotein in
incomplete Freund's adjuvant, J. Neuroinflamm., 12, 169,
https://doi.org/10.1186/s12974-015-0378-5, 2015.
Jagessar, S. A., Holtman, I. R., Hofman, S., Morandi, E., Heijmans, N.,
Laman, J. D., Gran, B., Faber, B. W., van Kasteren, S. I., Eggen, B. J., and
't Hart, B. A.: Lymphocryptovirus Infection of Nonhuman Primate B Cells
Converts Destructive into Productive Processing of the Pathogenic CD8 T Cell
Epitope in Myelin Oligodendrocyte Glycoprotein, J. Immunol., 197, 1074–1088,
https://doi.org/10.4049/jimmunol.1600124, 2016.
Jha, H. C., Mehta, D., Lu, J., El-Naccache, D., Shukla, S. K., Kovacsics,
C., Kolson, D., and Robertson, E. S.: Gammaherpesvirus Infection of Human
Neuronal Cells, MBio, 6, e01844-01815, https://doi.org/10.1128/mBio.01844-15, 2015.
Jonker, M., Bakker, K., Slierendregt, B., 't Hart, B., and Bontrop, R.:
Autoimmunity in non-human primates: the role of major histocompatibility
complex and T cells, and implications for therapy, Hum. Immunol., 32, 31–40,
1991.
Joscelyn, J. and Kasper, L. H.: Digesting the emerging role for the gut
microbiome in central nervous system demyelination, Mult. Scler., 20,
1553–1559, https://doi.org/10.1177/1352458514541579, 2014.
Kabat, E. A., Wolf, A., and Bezer, A. E.: The rapid production of acute
disseminated encephalomyelitiis in rhesus monkeys by injection of
heterologous and homologous brain tissue with adjuvants, J. Exp. Med., 85, 117–130, 1947.
Kakalacheva, K., Regenass, S., Wiesmayr, S., Azzi, T., Berger, C., Dale, R.
C., Brilot, F., Munz, C., Rostasy, K., Nadal, D., and Lunemann, J. D.:
Infectious Mononucleosis Triggers Generation of IgG Auto-Antibodies against
Native Myelin Oligodendrocyte Glycoprotein, Viruses, 8, 51–58, https://doi.org/10.3390/v8020051,
2016.
Kap, Y. S., Smith, P., Jagessar, S. A., Remarque, E., Blezer, E., Strijkers,
G. J., Laman, J. D., Hintzen, R. Q., Bauer, J., Brok, H. P., and 't Hart, B.
A.: Fast progression of recombinant human myelin/oligodendrocyte
glycoprotein (MOG)-induced experimental autoimmune encephalomyelitis in
marmosets is associated with the activation of MOG34-56-specific cytotoxic T
cells, J. Immunol., 180, 1326–1337, 2008.
Kap, Y. S., van Driel, N., Blezer, E., Parren, P. W., Bleeker, W. K., Laman,
J. D., Craigen, J. L., and 't Hart, B. A.: Late B cell depletion with a
human anti-human CD20 IgG1kappa monoclonal antibody halts the development of
experimental autoimmune encephalomyelitis in marmosets, J. Immunol., 185,
3990–4003, https://doi.org/10.4049/jimmunol.1001393, 2010.
Kap, Y. S., Bauer, J., Driel, N. V., Bleeker, W. K., Parren, P. W., Kooi, E.
J., Geurts, J. J., Laman, J. D., Craigen, J. L., Blezer, E., and 't Hart, B.
A.: B-Cell Depletion Attenuates White and Gray Matter Pathology in Marmoset
Experimental Autoimmune Encephalomyelitis, J. Neuropath. Exp. Neur., 70,
992–1005, https://doi.org/10.1097/NEN.0b013e318234d421, 2011a.
Kap, Y. S., Jagessar, S. A., van Driel, N., Blezer, E., Bauer, J., van
Meurs, M., Smith, P., Laman, J. D., and 't Hart, B. A.: Effects of early
IL-17A neutralization on disease induction in a primate model of
experimental autoimmune encephalomyelitis, J. Neuroimmune Pharm., 6,
341–353, https://doi.org/10.1007/s11481-010-9238-3, 2011b.
Kap, Y. S., van Driel, N., Laman, J. D., Tak, P. P., and 't Hart, B. A.:
CD20+ B Cell Depletion Alters T Cell Homing, J. Immunol., 192, 4242–4253,
https://doi.org/10.4049/jimmunol.1303125, 2014.
Kap, Y. S., Bus-Spoor, C., van Driel, N., Dubbelaar, M. L., Grit, C.,
Kooistra, S. M., Fagrouch, Z., Verschoor, E., Bauer, J., Eggen, B. J. L.,
Harmsen, H. J. M., Laman, J. D., and 't Hart, B. A.: Targeted diet
modification reduces multiple sclerosis-like disease in adult outbred
marmoset monkeys, J. Immunol., 201, 3229–3243, https://doi.org/10.4049/jimmunol.1800822, 2018a.
Kap, Y. S., Bus-Spoor, C., van Driel, N., Dubbelaar, M. L., Grit, C.,
Kooistra, S. M., Fagrouch, Z. C., Verschoor, E. J., Bauer, J., Eggen, B. J.
L., Harmsen, H. J. M., Laman, J. D., and 't Hart, B. A.: Targeted Diet
Modification Reduces Multiple Sclerosis-like Disease in Adult Marmoset
Monkeys from an Outbred Colony, J. Immunol., 201, 3229–3243,
https://doi.org/10.4049/jimmunol.1800822, 2018b.
Kappos, L., Hartung, H. P., Freedman, M. S., Boyko, A., Radu, E. W., Mikol,
D. D., Lamarine, M., Hyvert, Y., Freudensprung, U., Plitz, T., van Beek, J.,
and Group, A. S.: Atacicept in multiple sclerosis (ATAMS): a randomised,
placebo-controlled, double-blind, phase 2 trial, Lancet Neurol., 13, 353–363,
https://doi.org/10.1016/S1474-4422(14)70028-6, 2014.
Kerlero de Rosbo, N., Milo, R., Lees, M. B., Burger, D., Bernard, C. C., and
Ben-Nun, A.: Reactivity to myelin antigens in multiple sclerosis. Peripheral
blood lymphocytes respond predominantly to myelin oligodendrocyte
glycoprotein, J. Clin. Invest., 92, 2602–2608, 1993.
Khan, G., Miyashita, E. M., Yang, B., Babcock, G. J., and Thorley-Lawson, D.
A.: Is EBV persistence in vivo a model for B cell homeostasis?, Immunity, 5,
173–179, 1996.
Kola, I. and Landis, J.: Can the pharmaceutical industry reduce attrition
rates?, Nat. Rev. Drug Discov., 3, 711–715, 2004.
Koldovsky, U., Koldovsky, P., Henle, G., Henle, W., Ackermann, R., and
Haase, G.: Multiple sclerosis-associated agent: transmission to animals and
some properties of the agent, Infect. Immun., 12, 1355–1366, 1975.
Kono, H. and Rock, K. L.: How dying cells alert the immune system to
danger, Nat. Rev. Immunol., 8, 279–289, https://doi.org/10.1038/nri2215, 2008.
Kurtzke, J. F.: Rating neurologic impairment in multiple sclerosis: an
expanded disability status scale (EDSS), Neurology, 33, 1444–1452, 1983.
Laman, J. D., van Meurs, M., Schellekens, M. M., de Boer, M., Melchers, B.,
Massacesi, L., Lassmann, H., Claassen, E., and 't Hart, B. A.: Expression of
accessory molecules and cytokines in acute EAE in marmoset monkeys
(Callithrix jacchus), J. Neuroimmunol., 86, 30–45, 1998.
Laman, J. D., 't Hart, B. A., Brok, H., Meurs, M., Schellekens, M. M.,
Kasran, A., Boon, L., Bauer, J., Boer, M., and Ceuppens, J.: Protection of
marmoset monkeys against EAE by treatment with a murine antibody blocking
CD40 (mu5D12), Eur J. Immunol., 32, 2218–2228, 2002.
Laman, J. D., Kooistra, S. M., and Clausen, B. E.: Reproducibility Issues:
Avoiding Pitfalls in Animal Inflammation Models, Methods in molecular
biology Clifton, N.J., 1559, 1–17, https://doi.org/10.1007/978-1-4939-6786-5_1, 2017.
Lassmann, H. and Ransohoff, R. M.: The CD4-Th1 model for multiple
sclerosis: a critical [correction of crucial] re-appraisal, Trends Immunol.,
25, 132–137, https://doi.org/10.1016/j.it.2004.01.007, 2004.
Lassmann, H., Niedobitek, G., Aloisi, F., Middeldorp, J. M., and
NeuroproMiSe, E. B. V. W. G.: Epstein-Barr virus in the multiple sclerosis
brain: a controversial issue–report on a focused workshop held in the
Centre for Brain Research of the Medical University of Vienna, Austria,
Brain, 134, 2772–2786, https://doi.org/10.1093/brain/awr197, 2011.
Laurence, M. and Benito-Leon, J.: Epstein-Barr virus and multiple
sclerosis: Updating Pender's hypothesis, Mult. Scler. Relat. Dis., 16, 8–14,
https://doi.org/10.1016/j.msard.2017.05.009, 2017.
Li, X., Bhattacharya, S., J., Z., Phadnis-Moghe, A. S., Crawford, R. B., and
Kaminski, N. E.: Aryl Hydrocarbon Receptor Activation Suppresses EBF1 and
PAX5 and Impairs Human B Lymphopoiesis, J. Immunol., 199, 3504–3515, https://doi.org/10.4049/jimmunol.1700289,
2017.
Lisak, R. P., Benjamins, J. A., Nedelkoska, L., Barger, J. L., Ragheb, S.,
Fan, B., Ouamara, N., Johnson, T. A., Rajasekharan, S., and Bar-Or, A.:
Secretory products of multiple sclerosis B cells are cytotoxic to
oligodendroglia in vitro, J. Neuroimmunol., 246, 85–95,
https://doi.org/10.1016/j.jneuroim.2012.02.015, 2012.
Louveau, A., Smirnov, I., Keyes, T. J., Eccles, J. D., Rouhani, S. J.,
Peske, J. D., Derecki, N. C., Castle, D., Mandell, J. W., Lee, K. S.,
Harris, T. H., and Kipnis, J.: Structural and functional features of central
nervous system lymphatic vessels, Nature, 523, 337–341, https://doi.org/10.1038/nature14432,
2015.
Lublin, F. D., Reingold, S. C., Cohen, J. A., Cutter, G. R., Sorensen, P.
S., Thompson, A. J., Wolinsky, J. S., Balcer, L. J., Banwell, B., Barkhof,
F., Bebo Jr., B., Calabresi, P. A., Clanet, M., Comi, G., Fox, R. J.,
Freedman, M. S., Goodman, A. D., Inglese, M., Kappos, L., Kieseier, B. C.,
Lincoln, J. A., Lubetzki, C., Miller, A. E., Montalban, X., O'Connor, P. W.,
Petkau, J., Pozzilli, C., Rudick, R. A., Sormani, M. P., Stuve, O., Waubant,
E., and Polman, C. H.: Defining the clinical course of multiple sclerosis:
the 2013 revisions, Neurology, 83, 278–286, https://doi.org/10.1212/WNL.0000000000000560,
2014.
Lucchinetti, C. F., Popescu, B. F., Bunyan, R. F., Moll, N. M., Roemer, S.
F., Lassmann, H., Bruck, W., Parisi, J. E., Scheithauer, B. W., Giannini,
C., Weigand, S. D., Mandrekar, J., and Ransohoff, R. M.: Inflammatory
cortical demyelination in early multiple sclerosis, N. Engl. J. Med., 365,
2188–2197, https://doi.org/10.1056/NEJMoa1100648, 2011.
Ludlage, E. and Mansfield, K.: Clinical care and diseases of the common
marmoset (Callithrix jacchus), Comp. Med., 53, 369–382, 2003.
Mackowiak, P. A.: Recycling metchnikoff: probiotics, the intestinal
microbiome and the quest for long life, Front. Public Health, 1, 52,
https://doi.org/10.3389/fpubh.2013.00052, 2013.
MacPherson, G., Kushnir, N., and Wykes, M.: Dendritic cells, B cells and the
regulation of antibody synthesis, Immunol. Rev., 172, 325–334, 1999.
Maggi, P., Macri, S. M., Gaitan, M. I., Leibovitch, E., Wholer, J. E.,
Knight, H. L., Ellis, M., Wu, T., Silva, A. C., Massacesi, L., Jacobson, S.,
Westmoreland, S., and Reich, D. S.: The formation of inflammatory
demyelinated lesions in cerebral white matter, Ann. Neurol., 76, 594–608,
https://doi.org/10.1002/ana.24242, 2014.
Maggi, P., Sati, P., and Massacesi, L.: Magnetic resonance imaging of
experimental autoimmune encephalomyelitis in the common marmoset, J. Neuroimmunol., 304, 86–92, https://doi.org/10.1016/j.jneuroim.2016.09.016, 2017.
Manoury, B., Mazzeo, D., Fugger, L., Viner, N., Ponsford, M., Streeter, H.,
Mazza, G., Wraith, D. C., and Watts, C.: Destructive processing by
asparagine endopeptidase limits presentation of a dominant T cell epitope in
MBP, Nat. Immunol., 3, 169–174, https://doi.org/10.1038/ni754, 2002.
Mansfield, K.: Marmoset models commonly used in biomedical research, Comp. Med., 53, 383–392, 2003.
Marquez, A. C. and Horwitz, M. S.: The Role of Latently Infected B Cells in
CNS Autoimmunity, Front. Immunol., 6, 544, https://doi.org/10.3389/fimmu.2015.00544,
2015.
Martino, G., Franklin, R. J., Baron Van Evercooren, A., Kerr, D. A., and
Stem Cells in Multiple Sclerosis Consensus: Stem cell transplantation in
multiple sclerosis: current status and future prospects, Nat. Rev. Neurol., 6, 247–255, https://doi.org/10.1038/nrneurol.2010.35, 2010.
Massacesi, L., Genain, C. P., Lee-Parritz, D., Letvin, N. L., Canfield, D.,
and Hauser, S. L.: Active and passively induced experimental autoimmune
encephalomyelitis in common marmosets: a new model for multiple sclerosis,
Ann. Neurol., 37, 519–530, 1995.
Matzinger, P.: Tolerance, danger, and the extended family, Annu. Rev. Immunol.,
12, 991–1045, 1994.
Mazzarino, P., Pietra, G., Vacca, P., Falco, M., Colau, D., Coulie, P.,
Moretta, L., and Mingari, M. C.: Identification of effector-memory
CMV-specific T lymphocytes that kill CMV-infected target cells in an
HLA-E-restricted fashion, Eur J. Immunol., 35, 3240–3247, 2005.
McFarland, H. I., Lobito, A. A., Johnson, M. M., Nyswaner, J. T., Frank, J.
A., Palardy, G. R., Tresser, N., Genain, C. P., Mueller, J. P., Matis, L.
A., and Lenardo, M. J.: Determinant spreading associated with demyelination
in a nonhuman primate model of multiple sclerosis, J. Immunol., 162,
2384–2390, 1999.
Merchant, M. and Longnecker, R.: LMP2A survival and developmental signals
are transmitted through Btk-dependent and Btk-independent pathways,
Virology, 291, 46–54, https://doi.org/10.1006/viro.2001.1187, 2001.
Micu, I., Plemel, J. R., Caprariello, A. V., Nave, K. A., and Stys, P. K.:
Axo-myelinic neurotransmission: a novel mode of cell signalling in the
central nervous system, Nat. Rev. Neurosci., 19, 58, https://doi.org/10.1038/nrn.2017.128, 2017.
Miller, J. D., Weber, D. A., Ibegbu, C., Pohl, J., Altman, J. D., and
Jensen, P. E.: Analysis of HLA-E peptide-binding specificity and contact
residues in bound peptide required for recognition by CD94/NKG2, J. Immunol.,
171, 1369–1375, 2003.
Montalban, X., Hauser, S. L., Kappos, L., Arnold, D. L., Bar-Or, A., Comi,
G., de Seze, J., Giovannoni, G., Hartung, H. P., Hemmer, B., Lublin, F.,
Rammohan, K. W., Selmaj, K., Traboulsee, A., Sauter, A., Masterman, D.,
Fontoura, P., Belachew, S., Garren, H., Mairon, N., Chin, P., Wolinsky, J.
S., and Investigators, O. C.: Ocrelizumab versus Placebo in Primary
Progressive Multiple Sclerosis, N. Engl. J. Med., 376, 209–220,
https://doi.org/10.1056/NEJMoa1606468, 2017.
Morandi, E., Jagessar, S. A., 't Hart, B. A., and Gran, B.: EBV Infection
Empowers Human B Cells for Autoimmunity: Role of Autophagy and Relevance to
Multiple Sclerosis, J. Immunol., 199, 435–448, https://doi.org/10.4049/jimmunol.1700178,
2017a.
Morandi, E., Jagessar, S. A., 't Hart, B. A., and Gran, B.: EBV Infection
Empowers Human B Cells for Autoimmunity: Role of Autophagy and Relevance to
Multiple Sclerosis, J. Immunol., 199, 435–448, https://doi.org/10.4049/jimmunol.1700178, 2017b.
Moscarello, M. A., Wood, D. D., Ackerley, C., and Boulias, C.: Myelin in
multiple sclerosis is developmentally immature, J. Clin. Invest., 94, 146–154,
https://doi.org/10.1172/JCI117300, 1994.
Munz, C.: Enhancing immunity through autophagy, Annu. Rev. Immunol., 27,
423–449, https://doi.org/10.1146/annurev.immunol.021908.132537, 2009.
Nigida, S. M., Falk, L. A., Wolfe, L. G., and Deinhardt, F.: Isolation of a
cytomegalovirus from salivary glands of white-lipped marmosets (Saguinus
fuscicollis), Lab. Anim. Sci., 29, 53–60, 1979.
O'Mahony, S. M., Clarke, G., Borre, Y. E., Dinan, T. G., and Cryan, J. F.:
Serotonin, tryptophan metabolism and the brain-gut-microbiome axis, Behav. Brain Res., 277, 32–48, https://doi.org/10.1016/j.bbr.2014.07.027, 2015.
Pakpoor, J., Disanto, G., Gerber, J. E., Dobson, R., Meier, U. C.,
Giovannoni, G., and Ramagopalan, S. V.: The risk of developing multiple
sclerosis in individuals seronegative for Epstein-Barr virus: a
meta-analysis, Mult. Scler., 19, 162–166, https://doi.org/10.1177/1352458512449682, 2013.
Pan, B., Fromholt, S. E., Hess, E. J., Crawford, T. O., Griffin, J. W.,
Sheikh, K. A., and Schnaar, R. L.: Myelin-associated glycoprotein and
complementary axonal ligands, gangliosides, mediate axon stability in the
CNS and PNS: neuropathology and behavioral deficits in single- and
double-null mice, Exp. Neurol., 195, 208–217, 2005.
Pasteur, L.: Methode pour prevenir la rage apres morsure., Comptes rendus
des seances de l'Academie des sciences, 101, 765–774, 1885.
Pender, M. P.: Infection of autoreactive B lymphocytes with EBV, causing
chronic autoimmune diseases, Trends Immunol., 24, 584–588, 2003.
Pietra, G., Romagnani, C., Mazzarino, P., Falco, M., Millo, E., Moretta, A.,
Moretta, L., and Mingari, M. C.: HLA-E-restricted recognition of
cytomegalovirus-derived peptides by human CD8+ cytolytic T lymphocytes,
P. Natl. Acad. Sci. USA, 100, 10896–10901, 2003.
Pluchino, S., Gritti, A., Blezer, E., Amadio, S., Brambilla, E., Borsellino,
G., Cossetti, C., Del Carro, U., Comi, G., 't Hart, B., Vescovi, A., and
Martino, G.: Human neural stem cells ameliorate autoimmune encephalomyelitis
in non-human primates, Ann. Neurol., 66, 343–354, 2009.
Ransohoff, R. M.: EAE: pitfalls outweigh virtues of screening potential
treatments for multiple sclerosis, Trends Immunol., 27, 167–168, 2006.
Ransohoff, R. M., Hafler, D. A., and Lucchinetti, C. F.: Multiple
sclerosis-a quiet revolution, Nat. Rev. Neurol., 11, 134–142,
https://doi.org/10.1038/nrneurol.2015.14, 2015.
Raposo, G., Nijman, H. W., Stoorvogel, W., Liejendekker, R., Harding, C. V.,
Melief, C. J., and Geuze, H. J.: B lymphocytes secrete antigen-presenting
vesicles, J. Exp. Med., 183, 1161–1172, 1996.
Rath, M., Muller, I., Kropf, P., Closs, E. I., and Munder, M.: Metabolism
via Arginase or Nitric Oxide Synthase: Two Competing Arginine Pathways in
Macrophages, Front. Immunol., 5, 532, https://doi.org/10.3389/fimmu.2014.00532,
2014.
Ressing, M. E., Horst, D., Griffin, B. D., Tellam, J., Zuo, J., Khanna, R.,
Rowe, M., and Wiertz, E. J.: Epstein-Barr virus evasion of CD8(+) and
CD4(+) T cell immunity via concerted actions of multiple gene products,
Semin. Cancer Biol., 18, 397–408, https://doi.org/10.1016/j.semcancer.2008.10.008,
2008.
Rivailler, P., Cho, Y. G., and Wang, F.: Complete genomic sequence of an
Epstein-Barr virus-related herpesvirus naturally infecting a new world
primate: a defining point in the evolution of oncogenic lymphocryptoviruses,
J. Virol., 76, 12055–12068, 2002.
Rivers, T. M. and Schwenkter, F. F.: Encephalomyelitis accompanied by
myelin destruction experimentally produced in monkeys, J. Exp. Med., 61,
698–703, 1935.
Rivers, T. M., Sprunt, D. H., and Berry, G. P.: Observations on the attempts
to produce acute disseminated allergic encephalomyelitis in primates, J.
Exp. Med., 58, 39–53, 1933.
Rose, L. M., Richards, T., and Alvord Jr., E. C.: Experimental allergic
encephalomyelitis (EAE) in nonhuman primates: a model of multiple sclerosis,
Lab. Anim. Sci., 44, 508–512, 1994.
Russell, W. M. S. and Burch, R. L.: The Principles of Humane Experimental
Technique, Methuen, London, 1959.
Safaiyan, S., Kannaiyan, N., Snaidero, N., Brioschi, S., Biber, K., Yona,
S., Edinger, A. L., Jung, S., Rossner, M. J., and Simons, M.: Age-related
myelin degradation burdens the clearance function of microglia during aging,
Nat. Neurosci., 19, 995–998, https://doi.org/10.1038/nn.4325, 2016.
Sanvito, L., Constantinescu, C. S., Gran, B., and 't Hart, B. A.: The
multifaceted role of interferon-ã in central nervous system autoimmune
demyelination, The Open Autoimmunity Journal, 2, 151–159, 2010.
Sato, F., Martinez, N. E., Stewart, E. C., Omura, S., Alexander, J. S., and
Tsunoda, I.: “Microglial nodules” and “newly forming lesions” may be a Janus
face of early MS lesions; implications from virus-induced demyelination, the
Inside-Out model, BMC Neurol., 15, 219, https://doi.org/10.1186/s12883-015-0478-y, 2015.
Sawcer, S., Franklin, R. J., and Ban, M.: Multiple sclerosis genetics,
Lancet Neurol., 13, 700–709, https://doi.org/10.1016/S1474-4422(14)70041-9, 2014.
Segal, B. M., Constantinescu, C. S., Raychaudhuri, A., Kim, L.,
Fidelus-Gort, R., and Kasper, L. H.: Repeated subcutaneous injections of
IL12/23 p40 neutralising antibody, ustekinumab, in patients with
relapsing-remitting multiple sclerosis: a phase II, double-blind,
placebo-controlled, randomised, dose-ranging study, Lancet Neurol., 7,
796–804,
https://doi.org/10.1016/S1474-4422(08)70173-X, 2008.
Serre, L., Girard, M., Ramadan, A., Menut, P., Rouquie, N., Lucca, L. E.,
Mahiddine, K., Leobon, B., Mars, L. T., and Guerder, S.: Thymic-Specific
Serine Protease Limits Central Tolerance and Exacerbates Experimental
Autoimmune Encephalomyelitis, J. Immunol., 199, 3748–3756,
https://doi.org/10.4049/jimmunol.1700667, 2017.
Shahi, S. K., Freedman, S. N., and Mangalam, A. K.: Gut microbiome in
multiple sclerosis: The players involved and the roles they play, Gut Microbes, 8, 607–615, https://doi.org/10.1080/19490976.2017.1349041, 2017.
Shetty, A., Gupta, S. G., Varrin-Doyer, M., Weber, M. S., Prod'homme, T.,
Molnarfi, N., Ji, N., Nelson, P. A., Patarroyo, J. C., Schulze-Topphoff, U.,
Fogal, S. E., Forsthuber, T., Sobel, R. A., Bernard, C. C., Slavin, A. J.,
and Zamvil, S. S.: Immunodominant T-cell epitopes of MOG reside in its
transmembrane and cytoplasmic domains in EAE, Neurol. Neuroimmunol. Neuroinflamm., 1, e22,
https://doi.org/10.1212/NXI.0000000000000022, 2014.
Singh, S., Metz, I., Amor, S., van der Valk, P., Stadelmann, C., and Bruck,
W.: Microglial nodules in early multiple sclerosis white matter are
associated with degenerating axons, Acta Neuropathol., 125, 595–608,
https://doi.org/10.1007/s00401-013-1082-0, 2013.
Springer, S. A., Diaz, S. L., and Gagneux, P.: Parallel evolution of a
self-signal: humans and new world monkeys independently lost the cell
surface sugar Neu5Gc, Immunogenetics, 66, 671–674,
https://doi.org/10.1007/s00251-014-0795-0, 2014.
Sriram, S. and Steiner, I.: Experimental allergic encephalomyelitis: A
misleading model of multiple sclerosis, Ann. Neurol., 58, 939–945, 2005.
Steinman, L.: Blocking adhesion molecules as therapy for multiple sclerosis:
natalizumab, Nat. Rev. Drug Discov., 4, 510–518, 2005.
Steinman, L. and Zamvil, S. S.: Virtues and pitfalls of EAE for the
development of therapies for multiple sclerosis, Trends Immunol., 26,
565–571,
https://doi.org/10.1016/j.it.2005.08.014, 2005.
Stys, P. K., Zamponi, G. W., van Minnen, J., and Geurts, J. J.: Will the
real multiple sclerosis please stand up?, Nature reviews, Neuroscience, 13,
507–514, https://doi.org/10.1038/nrn3275, 2012.
Takahashi, K. and Yamanaka, S.: Induction of pluripotent stem cells from
mouse embryonic and adult fibroblast cultures by defined factors, Cell, 126,
663–676, https://doi.org/10.1016/j.cell.2006.07.024, 2006.
Takahama, M., Akira, S., and Saitoh, T.: Autophagy limits activation of the
inflammasomes, Immunol. Rev., 281, 62–73, https://doi.org/10.1111/imr.12613, 2018.
Tangvoranuntakul, P., Gagneux, P., Diaz, S., Bardor, M., Varki, N., Varki,
A., and Muchmore, E.: Human uptake and incorporation of an immunogenic
nonhuman dietary sialic acid, P. Natl. Acad. Sci. USA, 100, 12045–12050,
https://doi.org/10.1073/pnas.2131556100, 2003.
Tardif, S. D., Smucny, D. A., Abbott, D. H., Mansfield, K., Schultz-Darken,
N., and Yamamoto, M. E.: Reproduction in captive common marmosets
(Callithrix jacchus), Comp. Med., 53, 364–368, 2003.
Tardif, S. D., Mansfield, K. G., Ratnam, R., Ross, C. N., and Ziegler, T.
E.: The marmoset as a model of aging and age-related diseases, Ilar J., 52,
54–65, 2011.
Taylor, R. E., Gregg, C. J., Padler-Karavani, V., Ghaderi, D., Yu, H.,
Huang, S., Sorensen, R. U., Chen, X., Inostroza, J., Nizet, V., and Varki,
A.: Novel mechanism for the generation of human xeno-autoantibodies against
the nonhuman sialic acid N-glycolylneuraminic acid, J. Exp. Med., 207,
1637–1646, https://doi.org/10.1084/jem.20100575, 2010.
Tempera, I., De Leo, A., Kossenkov, A. V., Cesaroni, M., Song, H., Dawany,
N., Showe, L., Lu, F., Wikramasinghe, P., and Lieberman, P. M.:
Identification of MEF2B, EBF1, and IL6R as Direct Gene Targets of
Epstein-Barr Virus (EBV) Nuclear Antigen 1 Critical for EBV-Infected
B-Lymphocyte Survival, J. Virol., 90, 345–355, https://doi.org/10.1128/JVI.02318-15, 2015.
't Hart, B. A.: Reverse translation of failed treatments can help improving
the validity of preclinical animal models, Eur. J. Pharmacol., 759, 14–18,
https://doi.org/10.1016/j.ejphar.2015.03.030, 2015.
't Hart, B. A.: Primate autoimmune disease models; lost for translation?,
Clinical & translational immunology, 5, e122, https://doi.org/10.1038/cti.2016.82, 2016a.
't Hart, B. A.: Why does multiple sclerosis only affect human primates?,
Mult. Scler., 22, 559–563, https://doi.org/10.1177/1352458515591862, 2016b.
't Hart, B. A. and Massacesi, L.: Clinical, pathological, and immunologic
aspects of the multiple sclerosis model in common marmosets (Callithrix
jacchus), J. Neuropath. Exp. Neur., 68, 341–355, 2009.
't Hart, B. A. and van Kooyk, Y.: Yin-Yang regulation of autoimmunity by
DCs, Trends Immunol., 25, 353–359, 2004.
't Hart, B. A., Elferink, J. G., and Nibbering, P. H.: Effect of apocynin
on the induction of ulcerative lesions in rat skin injected with tubercle
bacteria, Int. J. Immunopharmaco., 14, 953–961, 1992.
't Hart, B. A., Bauer, J., Muller, H. J., Melchers, B., Nicolay, K., Brok,
H., Bontrop, R. E., Lassmann, H., and Massacesi, L.: Histopathological
characterization of magnetic resonance imaging- detectable brain white
matter lesions in a primate model of multiple sclerosis: a correlative study
in the experimental autoimmune encephalomyelitis model in common marmosets
(Callithrix jacchus), Am. J. Pathol., 153, 649–663, 1998.
't Hart, B. A., Vogels, J. T., Spijksma, G., Brok, H. P., Polman, C., and
van der Greef, J.: 1H-NMR spectroscopy combined with pattern recognition
analysis reveals characteristic chemical patterns in urines of MS patients
and non-human primates with MS-like disease, J. Neurol. Sci., 212, 21–30, 2003.
't Hart, B. A., Vogels, J. T., Bauer, J., Brok, H. P. M., and Blezer, E.:
Non-invasive measurement of brain damage in a primate model of multiple
sclerosis, Trends Mol. Med., 10, 85–91, 2004.
't Hart, B. A., Bauer, J., Brok, H. P., and Amor, S.: Non-human primate
models of experimental autoimmune encephalomyelitis: Variations on a theme,
J. Neuroimmunol., 168, 1–12, 2005a.
't Hart, B. A., Blezer, E. L., Brok, H. P., Boon, L., de Boer, M., Bauer,
J., and Laman, J. D.: Treatment with chimeric anti-human CD40 antibody
suppresses MRI-detectable inflammation and enlargement of pre-existing brain
lesions in common marmosets affected by MOG-induced EAE, J. Neuroimmunol.,
163, 31–39, 2005b.
't Hart, B. A., Brok, H. P., Remarque, E., Benson, J., Treacy, G., Amor, S.,
Hintzen, R. Q., Laman, J. D., Bauer, J., and Blezer, E. L.: Suppression of
ongoing disease in a nonhuman primate model of multiple sclerosis by a
human-anti-human IL-12p40 antibody, J. Immunol., 175, 4761–4768, 2005c.
't Hart, B. A., Losen, M., Brok, H. P. M., and de Baets, M. H.: Chronic
Diseases, in: The Laboratory Primate, edited by: Wolfe-Coote, S. P.,
Handbook of Experimental Animals, Elsevier Science, 417–433, 2005d.
't Hart, B. A., Smith, P., Amor, S., Strijkers, G. J., and Blezer, E. L.:
MRI-guided immunotherapy development for multiple sclerosis in a primate,
Drug. Discov. Today, 11, 58–66, 2006.
't Hart, B. A., Hintzen, R. Q., and Laman, J. D.: Multiple sclerosis – a
response-to-damage model, Trends Mol. Med., 15, 235–244, 2009.
't Hart, B. A., Gran, B., and Weissert, R.: EAE: imperfect but useful models
of multiple sclerosis, Trends Mol. Med., 17, 119–125, https://doi.org/10.1016/j.molmed.2010.11.006, 2011.
't Hart, B. A., Abbott, D. H., Nakamura, K., and Fuchs, E.: The marmoset
monkey: a multi-purpose preclinical and translational model of human biology
and disease, Drug. Discov. Today, 17, 1160–1165, https://doi.org/10.1016/j.drudis.2012.06.009,
2012.
't Hart, B. A., Chalan, P., Koopman, G., and Boots, A. M.: Chronic
autoimmune-mediated inflammation: a senescent immune response to injury,
Drug. Discov. Today, 18, 372–379, https://doi.org/10.1016/j.drudis.2012.11.010, 2013.
't Hart, B. A., Jagessar, S. A., Kap, Y. S., Haanstra, K. G., Philippens, I.
H., Serguera, C., Langermans, J., and Vierboom, M.: Improvement of
preclinical animal models for autoimmune-mediated disorders via reverse
translation of failed therapies, Drug. Discov. Today, 19, 1394–1401,
https://doi.org/10.1016/j.drudis.2014.03.023, 2014.
't Hart, B. A., van Kooyk, Y., Geurts, J. J., and Gran, B.: The primate
autoimmune encephalomyelitis model; a bridge between mouse and man, Ann Clin. Transl. Neur., 2, 581–593, https://doi.org/10.1002/acn3.194, 2015.
't Hart, B. A., Kap, Y. S., Morandi, E., Laman, J. D., and Gran, B.: EBV
Infection and Multiple Sclerosis: Lessons from a Marmoset Model, Trends Mol. Med., 22, 1012–1024, https://doi.org/10.1016/j.molmed.2016.10.007, 2016.
't Hart, B. A., Dunham, J., Faber, B. W., Laman, J. D., van Horssen, J.,
Bauer, J., and Kap, Y. S.: A B Cell-Driven Autoimmune Pathway Leading to
Pathological Hallmarks of Progressive Multiple Sclerosis in the Marmoset
Experimental Autoimmune Encephalomyelitis Model, Front. Immunol., 8,
804, https://doi.org/10.3389/fimmu.2017.00804, 2017a.
't Hart, B. A., Laman, J. D., and Kap, Y. S.: Reverse Translation for
Assessment of Confidence in Animal Models of Multiple Sclerosis for Drug
Discovery, Clin. Pharmacol. Ther., 103, 262–270, https://doi.org/10.1002/cpt.801, 2017b.
Thiruvalluvan, A., Czepiel, M., Kap, Y. A., Mantingh-Otter, I., Vainchtein,
I., Kuipers, J., Bijlard, M., Baron, W., Giepmans, B., Bruck, W., 't Hart, B.
A., Boddeke, E., and Copray, S.: Survival and Functionality of Human Induced
Pluripotent Stem Cell-Derived Oligodendrocytes in a Nonhuman Primate Model
for Multiple Sclerosis, Stem. Cell. Transl. Med., 5, 1550–1561,
https://doi.org/10.5966/sctm.2016-0024, 2016.
Uccelli, A., Oksenberg, J. R., Jeong, M. C., Genain, C. P., Rombos, T.,
Jaeger, E. E., Giunti, D., Lanchbury, J. S., and Hauser, S. L.:
Characterization of the TCRB chain repertoire in the New World monkey
Callithrix jacchus, J. Immunol., 158, 1201–1207, 1997.
Vales-Gomez, M., Reyburn, H. T., Erskine, R. A., Lopez-Botet, M., and
Strominger, J. L.: Kinetics and peptide dependency of the binding of the
inhibitory NK receptor CD94/NKG2-A and the activating receptor CD94/NKG2-C
to HLA-E, Embo J., 18, 4250–4260, 1999.
Vallejo, A. N., Weyand, C. M., and Goronzy, J. J.: T-cell senescence: a
culprit of immune abnormalities in chronic inflammation and persistent
infection, Trends Mol. Med., 10, 119–124, https://doi.org/10.1016/j.molmed.2004.01.002, 2004.
van der Valk, P. and Amor, S.: Preactive lesions in multiple sclerosis,
Curr. Opin. Neurol., 22, 207–213, https://doi.org/10.1097/WCO.0b013e32832b4c76, 2009.
van der Wiel, M. K., Otting, N., de Groot, N. G., Doxiadis, G. G., and
Bontrop, R. E.: The repertoire of MHC class I genes in the common marmoset:
evidence for functional plasticity, Immunogenetics, 65, 841–849,
https://doi.org/10.1007/s00251-013-0732-7, 2013.
Van Kooyk, Y. and Geijtenbeek, T. B.: DC-SIGN: escape mechanism for
pathogens, Nat. Rev. Immunol., 3, 697–709, 2003.
Van Lambalgen, R. and Jonker, M.: Experimental allergic encephalomyelitis
in rhesus monkeys: II. Treatment of EAE with anti-T lymphocyte subset
monoclonal antibodies, Clin. Exp. Immunol., 68, 305–312, 1987a.
van Lambalgen, R. and Jonker, M.: Experimental allergic encephalomyelitis
in rhesus monkeys: I. Immunological parameters in EAE resistant and
susceptible rhesus monkeys, Clin. Exp. Immunol., 68, 100–107, 1987b.
van Venrooij, W. J. and Pruijn, G. J.: Citrullination: a small change for a
protein with great consequences for rheumatoid arthritis, Arthritis Res., 2,
249–251, 2000.
van Zwam, M., Huizinga, R., Heijmans, N., van Meurs, M., Wierenga-Wolf, A.
F., Melief, M. J., Hintzen, R. Q., 't Hart, B. A., Amor, S., Boven, L. A.,
and Laman, J. D.: Surgical excision of CNS-draining lymph nodes reduces
relapse severity in chronic-relapsing experimental autoimmune
encephalomyelitis, J. Pathol., 217, 543–551, 2009.
Vanderlugt, C. L., Begolka, W. S., Neville, K. L., Katz-Levy, Y., Howard, L.
M., Eagar, T. N., Bluestone, J. A., and Miller, S. D.: The functional
significance of epitope spreading and its regulation by co-stimulatory
molecules, Immunol. Rev., 164, 63–72, 1998.
Vanheusden, M., Stinissen, P., 't Hart, B. A., and Hellings, N.:
Cytomegalovirus: a culprit or protector in multiple sclerosis?, Trends Mol. Med., 21, 16–23, https://doi.org/10.1016/j.molmed.2014.11.002, 2015.
Varki, A.: Loss of N-glycolylneuraminic acid in humans: Mechanisms,
consequences, and implications for hominid evolution, Am. J.
Phys. Anthropol., 33, 54–69, 2001.
Varki, A.: Are humans prone to autoimmunity? Implications from evolutionary
changes in hominin sialic acid biology, J. Autoimmun., 83, 134–142,
https://doi.org/10.1016/j.jaut.2017.07.011, 2017.
von Budingen, H. C., Hauser, S. L., Nabavi, C. B., and Genain, C. P.:
Characterization of the expressed immunoglobulin IGHV repertoire in the New
World marmoset Callithrix jacchus, Immunogenetics, 53, 557–563, 2001.
von Budingen, H. C., Palanichamy, A., Lehmann-Horn, K., Michel, B. A., and
Zamvil, S. S.: Update on the autoimmune pathology of multiple sclerosis:
B-cells as disease-drivers and therapeutic targets, Eur. Neurol., 73, 238–246,
https://doi.org/10.1159/000377675, 2015.
Vossenaar, E. R., Zendman, A. J., van Venrooij, W. J., and Pruijn, G. J.:
PAD, a growing family of citrullinating enzymes: genes, features and
involvement in disease, Bioessays, 25, 1106–1118, https://doi.org/10.1002/bies.10357, 2003.
Wang, B.: Sialic acid is an essential nutrient for brain development and
cognition, Annu. Rev. Nutr., 29, 177–222,
https://doi.org/10.1146/annurev.nutr.28.061807.155515, 2009.
Wang, F., Rivailler, P., Rao, P., and Cho, Y.: Simian homologues of
Epstein-Barr virus, Philos. T. R. Soc. B, 356, 489–497,
https://doi.org/10.1098/rstb.2000.0776, 2001.
Wekerle, H.: Brain Autoimmunity and Intestinal Microbiota: 100 Trillion Game
Changers, Trends Immunol., 38, 483–497, https://doi.org/10.1016/j.it.2017.03.008, 2017.
Wilkin, T. J.: The primary lesion theory of autoimmunity: a speculative
hypothesis, Autoimmunity, 7, 225–235, 1990.
Wood, D. D., Ackerley, C. A., Brand, B., Zhang, L., Raijmakers, R.,
Mastronardi, F. G., and Moscarello, M. A.: Myelin localization of
peptidylarginine deiminases 2 and 4: comparison of PAD2 and PAD4 activities,
Lab. Invest., 88, 354–364, https://doi.org/10.1038/labinvest.3700748, 2008.
Yang, L. J., Zeller, C. B., Shaper, N. L., Kiso, M., Hasegawa, A., Shapiro,
R. E., and Schnaar, R. L.: Gangliosides are neuronal ligands for
myelin-associated glycoprotein, P. Natl. Acad. Sci. USA, 93, 814–818, 1996.
Yu, L., Chen, Y., and Tooze, S. A.: Autophagy pathway: Cellular and
molecular mechanisms, Autophagy, 14, 207–215, https://doi.org/10.1080/15548627.2017.1378838,
2018.
Zaguia, F., Saikali, P., Ludwin, S., Newcombe, J., Beauseigle, D., McCrea,
E., Duquette, P., Prat, A., Antel, J. P., and Arbour, N.: Cytotoxic NKG2C+
CD4 T cells target oligodendrocytes in multiple sclerosis, J. Immunol., 190,
2510–2518, https://doi.org/10.4049/jimmunol.1202725, 2013.
Short summary
Aging Western societies are facing an increasing prevalence of chronic autoimmune-mediated inflammatory disorders (AIMIDs). Animal models have a crucial role in the preclinical research of disease mechanisms and therapy development. Multiple sclerosis is an AIMID specifically affecting the brain and spinal cord. We discuss here a unique MS model in common marmoset monkeys, which has provided novel insights into the disease process as well as into the mechanism of action of new therapies.
Aging Western societies are facing an increasing prevalence of chronic autoimmune-mediated...
