Lymphocytes from SJL/J mice immunized with spinal cord respond selectively to a peptide of proteolipid protein and transfer relapsing demyelinating experimental autoimmune encephalomyelitis.

Whitham, R H; Bourdette, D N; Hashim, G A; Herndon, R M; Ilg, R C; Vandenbark, A A; Offner, H

doi:10.4049/jimmunol.146.1.101

Cited by 130Multiple Sclerosis Research StudiesT-cell and B-cell ImmunologySystemic Lupus Erythematosus Research

Lymphocytes from SJL/J mice immunized with spinal cord respond selectively to a peptide of proteolipid protein and transfer relapsing demyelinating experimental autoimmune encephalomyelitis.

Whitham, R H, Bourdette, D N, Hashim, G A, Herndon, R M, Ilg, R C, Vandenbark, A A, Offner, H·1991·The Journal of Immunology

DOI 10.4049/jimmunol.146.1.101

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Abstract

Relapsing experimental autoimmune encephalomyelitis (R-EAE) can be induced in SJL/J mice by immunization with spinal cord homogenate and adjuvant. The specific Ag(s) responsible for acute disease and subsequent relapses in this model is unknown. Myelin basic protein (BP), an encephalitogenic peptide of BP (BP 87-99), and proteolipid protein (PLP) can each induce R-EAE in SJL/J mice, and a peptide of PLP (PLP 139-151) has been reported to induce acute EAE. To determine the encephalitogens in cord-immunized mice with R-EAE, the in vitro proliferative responses of lymph node cells (LNC) and central nervous system mononuclear cells to BP, BP peptides, and PLP peptides were examined during acute EAE and during relapses. LNC responded only to PLP peptides 139-151 and 141-151 and did not respond to BP or its peptides during acute or chronic disease. Central nervous system mononuclear cells also preferentially responded to PLP 139-151 and 141-151 during acute and relapsing disease. A PLP 139-151 peptide-specific Th cell line was selected from LNC of cord-immunized donors. Five million peptide-specific line cells transferred severe relapsing demyelinating EAE to naive recipients. We conclude that PLP peptide 139-151 is the major encephalitogen for R-EAE in cord-immunized SJL/J mice. We demonstrate for the first time that Th cells specific for this peptide are sufficient to transfer relapsing demyelinating EAE. The predominance of a PLP immune response rather than a BP response in SJL/J mice suggests that genetic background may determine the predominant myelin Ag response in human demyelinating diseases such as multiple sclerosis.

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PLP-induced acute mouse EAE is a routinely used model for multiple sclerosis.
“We also studied therapeutic efficacy in the proteolipid protein (PLP)-induced acute mouse EAE, a routinely used model for the autoimmune inflammatory neurodegenerative disease multiple sclerosis [39], [40], in which the involvement of inflammation in the brain enhance the permeability of this difficult to reach organ.”
From Fabrication Principles and Their Contribution to the Superior In Vivo Therapeutic Efficacy of Nano-Liposomes Remote Loaded with Glucocorticoids (2011) · cites this paper as [40]

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Background
Therapy of chronic relapsing experimental allergic encephalomyelitis and the role of the blood-brain barrier: elucidation by the action of Brequinar sodium
O'Neill, J. K., Baker, D., DAVISON, A. N., Maggon, K. K., JAFFEE, B. D., & Turk, J. L. (1992) · Journal of Neuroimmunology · doi:10.1016/0165-5728(92)90090-8 · Cited by 34 · see citing works
Spreading of the immune response to different myelin basic protein peptides in chronic experimental autoimmune encephalomyelitis in B10.RIII mice
Jansson, L., Diener, P., Engström, Å., Olsson, T. P., & Holmdahl, R. (1995) · European Journal of Immunology · doi:10.1002/eji.1830250812 · Cited by 31 · see citing works
Epitope spreading occurs in active but not passive EAE induced by myelin basic protein
Voskuhl, R. R., Farris, R. W., Nagasato, K., McFarland, H. F., & Dubois-Dalcq, M. E. (1996) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(96)00054-9 · Cited by 30 · see citing works
Experimental Autoimmune Encephalomyelitis
Rao, P., & Segal, B. M. (2012) · Methods in molecular biology · doi:10.1007/978-1-60761-720-4_18 · Cited by 29 · see citing works
Enhancement of EAE and induction of autoantibodies to T-cell epitopes in mice infected with a recombinant vaccinia virus encoding myelin proteolipid protein
Wang, L.-Y., & Fujinami, R. S. (1997) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(96)00235-4 · Cited by 29 · see citing works
“PLP has been found to be the predominant encephalitogen in spinal cord homogenates as T-cells from spinal cord homogenate immunized SJLrJ mice proliferated selectively to p139–151 when compared to whole MBP or the encephalitogenic Ž .peptide MBP 87–99 Whitham et al., 1991 .”
Background
Immunoneutralization of chemokines for the prevention and treatment of central nervous system autoimmune disease
Karpus, W. J., Fife, B. T., & Kennedy, K. J. (2003) · Methods · doi:10.1016/s1046-2023(02)00360-2 · Cited by 28 · see citing works
Multiple sclerosis: immunological findings and possible implications for therapy
Hintzen, R. Q., Polman, C. H., Lucas, C. J., et al. (1992) · Journal of Neuroimmunology · doi:10.1016/0165-5728(92)90169-l · Cited by 27 · see citing works
Animal Models of Multiple Sclerosis
Smith, P. (2021) · Current Protocols · doi:10.1002/cpz1.185 · Cited by 28 · see citing works
Treatment of relapsing experimental autoimmune encephalomyelitis with T cell receptor peptides
Whitham, R. H., Kotzin, B. L., Buenafe, A. C., et al. (1993) · Journal of Neuroscience Research · doi:10.1002/jnr.490350202 · Cited by 26 · see citing works
Self-citation
Antisense oligonucleotide blockade of alpha 4 integrin prevents and reverses clinical symptoms in murine experimental autoimmune encephalomyelitis
Myers, K. J., Witchell, D. R., Graham, M. J., et al. (2004) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2004.10.029 · Cited by 24 · see citing works
“ISIS 17044 was evaluated in both prophylactic and therapeutic dosing regimes in a mouse model of EAE induced by direct immunization with PLP peptide (Whitham et al., 1991).”
Method
Fine specificity of CD4+ T cell responses to the dominant encephalitogenic PLP 139-151 peptide in SJL/J mice
McRae, B. L., & Miller, S. D. (1994) · Neurochemical Research · doi:10.1007/bf00968709 · Cited by 23 · see citing works
Anticoagulation with warfarin and rivaroxaban ameliorates experimental autoimmune encephalomyelitis
Stolz, L., Derouiche, A., Devraj, K., Weber, F., Brunkhorst, R., & Foerch, C. (2017) · Journal of Neuroinflammation · doi:10.1186/s12974-017-0926-2 · Cited by 22 · see citing works
“One hundred seventy female SJL/J mice that are specific pathogen free and aged 9–10 weeks at immunization were purchased from Charles River (Sulzfeld, Germany) or Janvier (Le Genest-Saint-Isle, France) to study relapsing-remitting (RR-)EAE [9].”
Gender differences in CNS autoimmunity induced by mimicry epitope for PLP 139–151 in SJL mice
Massilamany, C., Thulasingam, S., Steffen, D. J., & Reddy, J. (2010) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2010.09.011 · Cited by 22 · see citing works
“Viable lymphoblasts were harvested on day 4 postimulation by Ficoll-hypaque density gradient centrifugation, and groups of naive male and female SJL mice were injected i.p. with 10 × 106 cells per mouse (Whitham et al., 1991).”
Administration of PLP139–151 Primes T Cells Distinct from Those Spontaneously Responsive In Vitro to This Antigen
Penitente, R., Nicolò, C., van den Elzen, P., et al. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.180.10.6611 · Cited by 22 · see citing works
“within whole myelin (14, 15), suggesting that the same repertoire”
Background
Sjogrens Syndrome as Failed Local Immunohomeostasis: Prospects for Cell-Based Therapy
Mircheff, A. K. (2003) · The Ocular Surface · doi:10.1016/s1542-0124(12)70012-5 · Cited by 20 · see citing works
TCR Peptide Therapy in Autoimmune Diseases
Vandenbark, A. A., Hashim, G. A., & Offner, H. (1993) · International Reviews of Immunology · doi:10.3109/08830189309051210 · Cited by 20 · see citing works
Self-citation
Genetics of experimental autoimmune encephalomyelitis in the mouse.
Andersson, Å., & Karlsson, J. (2004) · PubMed · Cited by 19 · see citing works
Lipoic acid downmodulates CD4 from human T lymphocytes by dissociation of p56Lck
Marracci, G., Marquardt, W. E., Strehlow, A., McKeon, G. P., Gross, J., Buck, D. C., Kozell, L. B., & BOURDETTE, D. N. (2006) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2006.03.172 · Cited by 18 · see citing works
Self-citation
Transgenic mouse models of multiple sclerosis
Scheikl, T., Pignolet, B., Mars, L. T., & Liblau, R. (2010) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-010-0481-9 · Cited by 18 · see citing works
“In SJL mice (H-2), the immunization with whole CNS homogenate induces relapsing EAE during which the autoreactive CD4 T cell response is focused on the PLP139–151 peptide [47].”
Background
Ingested Type I Interferon: A Potential Treatment for Autoimmunity
Brod, S. A. (2002) · Journal of Interferon & Cytokine Research · doi:10.1089/10799900260475669 · Cited by 18 · see citing works
Complement System in Central Nervous System Disorders
Shin, M. L., Rus, H., & Niculescu, F. I. (1998) · CRC Press eBooks · doi:10.1201/b14212-24 · Cited by 18 · see citing works
T cell receptor Vβ gene usage in the recognition of myelin basic protein by cerebrospinal fluid‐ and blood‐derived T cells from patients with multiple sclerosis
Chou, Y. K., Burenafe, A. C., Dedrick, R. L., et al. (1994) · Journal of Neuroscience Research · doi:10.1002/jnr.490370203 · Cited by 18 · see citing works
Self-citation
Role of omega-3 endocannabinoids in the modulation of T-cell activity in a multiple sclerosis experimental autoimmune encephalomyelitis (EAE) model
Kim, J. S., Soto‐Díaz, K., Bingham, T. W., Steelman, A. J., & Das, A. (2023) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2023.102886 · Cited by 16 · see citing works
“Considering that RR-EAE is a CD4 T-cell-mediated process (71, 72), these in vivo data correspond with our findings that DHEA and DHEA-epoxide eCBs influence T-cell polarization, Th17 effector function, and antigen-specific activation in TCR splenocytes.”
Result
Inducible expression of antigens in plants: a study focused on peptides related to multiple sclerosis immunotherapy
Arévalo-Villalobos, J. I., Govea‐Alonso, D. O., Bañuelos-Hernández, B., González‐Ortega, O., Zarazúa, S., & Rosales‐Mendoza, S. (2020) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2020.03.013 · Cited by 15 · see citing works
Autoimmunity Is a Type I Interferon-Deficiency Syndrome Corrected by Ingested Type I IFN via the GALT System
Brod, S. A. (1999) · Journal of Interferon & Cytokine Research · doi:10.1089/107999099313343 · Cited by 14 · see citing works
Characteristics of initial and reinduced experimental autoimmune encephalomyelitis
Lindsey, J. W. (1996) · Immunogenetics · doi:10.1007/bf02602559 · Cited by 13 · see citing works
Nonmyelin-Specific T Cells Accelerate Development of Central Nervous System APC and Increase Susceptibility to Experimental Autoimmune Encephalomyelitis
Jones, R. E., Kay, T. W. H., Keller, T., et al. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.170.2.831 · Cited by 13 · see citing works
Self-citation
Epitope specificity and V gene expression of cerebrospinal fluid T cells specific for intact versus cryptic epitopes of myelin basic protein
Satyanarayana, K., Chou, Y. K., BOURDETTE, D. N., et al. (1993) · Journal of Neuroimmunology · doi:10.1016/0165-5728(93)90268-4 · Cited by 11 · see citing works
Self-citation
Immune tolerance mediated by recombinant proteolipid protein prevents experimental autoimmune encephalomyelitis
Elliott, E. A., Cofiell, R., Wilkins, J. A., et al. (1997) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(97)00093-3 · Cited by 11 · see citing works
The polysialic acid modification of the neural cell adhesion molecule is involved in spatial learning and hippocampal long-term potentiation
Becker, C. G., Artola, A., Gerardy‐Schahn, R., Becker, T., Welzl, H., & Schachner, M. (1996) · Journal of Neuroscience Research · doi:10.1002/(sici)1097-4547(19960715)45:2 · Cited by 304 · see citing works
Self-citation
Infection with a recombinant vaccinia virus encoding myelin proteolipid protein causes suppression of chronic relapsing–remitting experimental allergic encephalomyelitis
Wang, L.-Y., Theil, D. J., Whitton, J. L., & Fujinami, R. S. (1999) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(99)00020-x · Cited by 10 · see citing works
Life history of a brain autoreactive T cell: From thymus through intestine to blood-brain barrier and brain lesion
Kawakami, N., & Wekerle, H. (2024) · Neurotherapeutics · doi:10.1016/j.neurot.2024.e00442 · Cited by 10 · see citing works
How special is a pathogenic CNS autoantigen? Immunization to many CNS self-antigens does not induce autoimmune disease
Mor, F., & Cohen, I. R. (2006) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2005.12.003 · Cited by 9 · see citing works
“Thus, upon immunization with spinal cord homogenate containing several thousands of different proteins, the immune system reacts to a small number of ‘‘dominant’’ proteins such as PLP (Whitham et al., 1991), MBP and MOG.”
Background
T cells with encephalitogenic potential from multiple sclerosis patients and Lewis rats fail to induce disease in SCID mice following intracisternal injection
Jones, R. E., Chou, Y. K., Young, A., et al. (1995) · Journal of Neuroimmunology · doi:10.1016/0165-5728(94)00130-g · Cited by 8 · see citing works
“…EAE following immunization with myelin antigens, most notably myelin basic protein (BP) and proteolipid protein (PLP), and myelin antigen-specific T lymphocytes from immunized rodent donors induce EAE after systemic transfer into naive recipients (Bourdette et al., 1989; Whitham et al., 1991).”
BackgroundInfluentialSelf-citation
Immunity to T cell receptor peptides: theory and applications
Offner, H., Hashim, G. A., & Vandenbark, A. A. (1994) · Regulatory Peptides · doi:10.1016/0167-0115(94)90197-x · Cited by 8 · see citing works
Self-citation
3-Hydroxy-3-methylglutaryl coenzyme A reductase inhibitor Atorvastatin mediated effects depend on the activation status of target cells in PLP-EAE
Mix, E., Ibrahim, S. M., Pahnke, J., et al. (2006) · Journal of Autoimmunity · doi:10.1016/j.jaut.2006.09.006 · Cited by 8 · see citing works
Regulation of Lymphatic GM-CSF Expression by the E3 Ubiquitin Ligase Cbl-b
Peer, S., Cappellano, G., Hermann‐Kleiter, N., Albrecht-Schgoer, K., Hinterleitner, R., Baier, G., & Gruber, T. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02311 · Cited by 7 · see citing works
Modulation of CNS autoimmune responses by CD8+ T cells coincides with their oligoclonal expansion
Fischer, H. J., van den Brandt, J., Lingner, T., Odoardi, F., Flügel, A., Weishaupt, A., & Reichardt, H. M. (2015) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2015.10.020 · Cited by 6 · see citing works
“Considering that more than 80% of all MS patients suffer from a relapsingremitting disease type (Compston and Coles, 2002), rodent models closely mimicking this variant of MS, such as SJL mice or DA rats, are of particular value (Herrmann et al., 2005; Whitham et al., 1991).”
Background
Encephalitogenic T lymphocytes develop from SJL/J hematopoietic cells transplanted into severe combined immimodeficient ( SCID) mice
Jones, R. E., Whitham, R. H., Sullivan, T. J., et al. (1995) · Journal of Neuroimmunology · doi:10.1016/0165-5728(94)00179-r · Cited by 6 · see citing works
Self-citation
Expression of soma-restricted proteolipid/DM20 proteins in lymphoid cells
Feng, J., Fernandes, A. O., Bongarzone, E. R., et al. (2003) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2003.08.003 · Cited by 6 · see citing works
“Myelin proteolipid protein (PLP), as the main component of the myelin sheath in the central nervous system (CNS), is a potent autoencephalitogen (Whitham et al., 1991).”
Background
Evaluation of methods of modeling and formation of experimental allergic encephalomyelitis
Nefоdov, O. O., Belenichev, I. F., Fedchenko, M. P., Popazova, O., Ryzhenko, V. P., & Morozova, O. V. (2022) · Research Results in Pharmacology · doi:10.3897/rrpharmacology.8.77361 · Cited by 5 · see citing works

Inhibition of murine relapsing experimental autoimmune encephalomyelitis by immune tolerance to proteolipid protein and its encephalitogenic peptides.
Kennedy, M., Tan, L., Canto, M. C. D., Tuohy, V. K., Lu, Z. J., Trotter, J. L., & Miller, S. D. (1990) · The Journal of Immunology · doi:10.4049/jimmunol.144.3.909 · Cited by 140 · see citing works
Targeting myelin proteolipid protein to the MHC class I pathway by ubiquitination modulates the course of experimental autoimmune encephalomyelitis
Theil, D. J., Libbey, J. E., Rodrı́guez, F., Whitton, J. L., Tsunoda, I., Derfuss, T. J., & Fujinami, R. S. (2008) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2008.07.005 · Cited by 5 · see citing works
Treatment of experimental encephalomyelitis with a novel chimeric fusion protein of myelin basic protein and proteolipid protein.
Elliott, E. A., McFarland, H., Nye, S. H., et al. (1996) · Journal of Clinical Investigation · doi:10.1172/jci118954 · Cited by 84 · see citing works
Suppression of MOG- and PLP-induced experimental autoimmune encephalomyelitis using a novel multivalent bifunctional peptide inhibitor
Badawi, A. H., & Siahaan, T. J. (2013) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2013.07.009 · Cited by 25 · see citing works
Amelioration of Established Experimental Autoimmune Encephalomyelitis by an MHC Anchor-Substituted Variant of Proteolipid Protein 139–151
Margot, C. D., Ford, M. L., & Evavold, B. D. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.6.3352 · Cited by 27 · see citing works

Authors: Whitham, R. H., Bourdette, D. N., Hashim, G. A., Herndon, R. M., Ilg, R. C., Vandenbark, A. A., & Offner, H.
Affiliations: Veterans Health Administration (US)
ORCID: Bourdette, D N
Vandenbark, A A
Venue: The Journal of Immunology
Publisher: Oxford University Press (OUP)
Published: 1991-01-01
Volume: 146
Issue: 1
Pages: 101-107
ISSN: 0022-1767 (ISSN-L)
1550-6606
DOI: 10.4049/jimmunol.146.1.101
OpenAlex: W1562022567
Cited by: 130
References: 0
Citations by year: 2024: 3 · 2023: 3 · 2022: 1 · 2021: 2 · 2020: 3 · 2018: 2 · 2017: 2 · 2016: 2 · 2015: 3 · 2014: 3 · 2013: 2 · 2012: 3
FWCI: 7.30
Type: journal article
Language: en
Open access: closed
Licence: academic.oup.com/pages/standard-publication-reuse-rights (vor)
Locations: The Journal of Immunology (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (5r01ns021466-05)
National Institute of Neurological Disorders and Stroke (NS23444, NS23221, NS 21466, R01NS023444, R01NS023221)
Topics: Health Sciences › Medicine › Pathology and Forensic Medicine › Multiple Sclerosis Research Studies
Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Health Sciences › Medicine › Rheumatology › Systemic Lupus Erythematosus Research
Keywords: proteolipid protein, myelin basic protein, SJL/J mice, T cell transfer, multiple sclerosis, genetic background, demyelinating disease
MeSH terms: Animals, Brain, Cell Line, Encephalomyelitis, Autoimmune, Experimental, Female, T-Lymphocytes, Helper-Inducer, Immunization, Passive, Leukocytes, Mononuclear, Lymph Nodes, Lymphocyte Activation, Mice, Inbred Strains, Myelin Proteins, Peptide Fragments, Spinal Cord, Time Factors, Myelin Proteolipid Protein, Mice

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Lymphocytes from SJL/J mice immunized with spinal cord respond selectively to a peptide of proteolipid protein and transfer relapsing demyelinating experimental autoimmune encephalomyelitis.

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