Virus-induced neurologic diseases: Coronaviruses and multiple sclerosis in patients, neural cells and in an animal model of MS
Multiple sclerosis (MS) is the most widespread neurologic disease in young adults, with a frequency of as many as 1 in 500 to 1000, especially in high-risk areas such as Canada, the northern parts of the United States and of Europe. Disease etiology is not known but is suspected to involve both genetic susceptibility and environmental triggering factors, the latter most likely viruses. It is suspected that infection by one or several common pathogen(s) before adolescence triggers MS in genetically susceptible individuals, as manifested by autoimmune reactions against antigens of the myelin sheaths surrounding nerve fibers in the central nervous system. Among the several viral candidates for induction of MS are the coronaviruses, a family of common respiratory pathogens involved in as many as 30% of common colds.
Dr. Talbot’s research team has detected the presence of these viruses in the brains of some MS patients but not controls, determined the infectability of neuronal and glial cells in continuous and primary cultures by human coronaviruses, and identified a striking human coronavirus-myelin cross-reactive T cell response in MS patients but not controls. Studies in progress deal with the characterization of the neurotropism of human coronaviruses and the possibility that they can trigger autoimmune pathology, perhaps through the molecular mimicry of myelin antigens and neurodegeneration.
Current research uses two parallel scientific approaches to understand how a respiratory virus may cause a neurologic disease like MS and others. On one hand, cell cultures from the central nervous systems, such as neurons are used to study the consequence of infection of these cells, notably the neurons which are the main target cells. On the other hand, an animal model, the mouse is used to characterize the molecular and cellular determinants of the interactiom of the virus with the immune and nervous system leading to neuroinflammation and neurodegeneration underlying neurological diseases, such as MS.
Dr. Pierre Talbot obtained his B.Sc. in Biochemistry (1977) from the Faculty of Sciences and Engineering of Laval University and his Ph.D. in Biochemistry (1981) from the Department of Biochemistry, Faculty of Medicine, University of British Columbia in Vancouver.
After post-doctoral training in immunovirology with Drs. Michael Buchmeier and Michael Oldstone at the Scripps Research Institute in La Jolla (California), he joined (in 1984) the Armand-Frappier Institute as an NSERC University Research Fellow and then FRSQ Senior Scholar of Exceptional Merit until 1997.
Between 1998 and 2002, he was Director of the Human Health Research Centre of INRS-Institut Armand-Frappier, and was Director of INRS-Institut Armand-Frappier between 2002 and 2007 as well as between 2017 and 2019.
The research efforts of his team, funded by Canadian Institutes of Health Research (CIHR) and the National Sciences and Engineering Research Council of Canada (NSERC), are aimed at an understanding of the interactions between a neurotropic virus and the immune and nervous systems that leads to the triggering of some neurologic diseases. The immediate target is the coronavirus as a possible etiological agent of multiple sclerosis.
From 2003 to 2017, Dr. Talbot holds a Tier I (senior) Canada Research Chair in NeuroImmunoVirology, and participates in the CIHR NeuroinflammationTraining Program
- multiple sclerosis
Desforges, M., A. Le Coupanec, P. Dubeau, A. Bourgouin, L. Lajoie, M. Dubé, and P.J. Talbot (2019)
Human coronaviruses and other respiratory viruses: underestimated opportunistic pathogens of the central nervous system? (2019)
Viruses, Dec. 20
Zhije, L., A.C.A. Tomlinson, A.H.M. Wong, D. Zhou, M. Desforges, P.J. Talbot. S. Benlekbir, J.L. Rubinstein, and J.M. Rini (2019)
The human coronavirus HCoV S-protein structure and receptor binding.
eLife, Oct. 25
Anderson, D.E., K. Pfeffermann, S.Y. Kim, B. Sawatsky, J. Pearson, M. Kovtun, D.L. Corcoran, Y. Krebs, K. Sigmundsson, S.F. Jamieson, Z,Z,J, Yeo, L.J. Rennick, L.-F. Wang, P.J. Talbot, W.P. Duprex, M.A. Garcia-Blanco, and V. Von Messling (2019)
Comparative loss-of-function screens reveal ABCE1 as an essential cellular host factor for efficient translation of Paramyxoviridae and Pneumoviridae.
MBio, May 14
Dubé, M., A. Le Coupanec, A.H.M. Wong, J.M. Rini, M. Desforges, and P.J. Talbot (2018)
Axonal transport enables neuron-to-neuron propagation of HCoV-OC43.
J. Virol. June 20
Stodola, J.K., G. Dubois, A. Le Coupanec, M. Desforges, and P.J. Talbot (2018)
The OC43 human coronavirus envelope protein is critical for infectious virus production and propagation in neuronal cells and is a determinant of neurovirulence and CNS pathology.
Virology 515: 134-149
Wong, A.H.M., A.C.A. Tomlison, D. Zhou, M. Satkuranajah, K. Chen, C. Sharon, M. Desforges, P.J. Talbot, and J.M. Rini (2017)
Receptor-binding loops in alphacoronavirus adaptation and evolution.
Nature Communications November 23
Meessen-Pinard, M., A. Le Coupanec, M. Desforges, and P.J. Talbot (2017)
Pivotal role of Receptor-Interacting Protein Kinase 1 and Mixed Lineage Kinase Domain-Like in neuronal cell death induced by human neuroinvasive coronavirus OC43.
J. Virol. 91: 1-20
Talbot, P.J, M. Desforges, M. Dubé, and A. Le Coupanec (2016)
Coronavirus respiratoires humains neurotropes : une relation ambigue entre neurovirulence et clivage protéique.
Med Sci (Paris). 2016 8-9;32(8-9):696-9. doi: 10.1051/medsci/20163208012. Epub 2016 Sep 12.
Shen, L., Y. Yang, F. Ye, G. Liu, M. Desforges, P.J. Talbot, and W. Tan (2016)
Safe and sensitive antiviral screening platform based on recombinant human coronavirus OC43 expressing the luciferase reporter gene.
Antimicrob. Agents Chemother. 60: 5492-5503.
Morfopoulou, S., J.R. Brown, E.G.Davies, G. Anderson, A. Virasami, W. Qasim, W.K. Chong, M. Hubank, V. Plagnol, M. Desforges, T.S. Jacques, P.J. Talbot, and J. Breuer (2016)
Human coronavirus OC43 associated with fatal encephalitis.
New Engl. J. Med. 375: 497-498.
Desforges, M., M. Meessen-Pinard, and P.J. Talbot (2016)
Modulating regulated cell death : the virus way to influence cell fate, survive and persist.
In: Programmed cell death in plants and animals. Rice, J., ed., ISBN 978-1-63484-505-02, Nova Science Publishers, Inc., Hauppauge, New York, U.S.A., Chap. 2, pp. 35-73.
Le Coupanec, A., M. Desforges, M. Meessen-Pinard, M. Dubé, R. Day, N.G. Seidah, and P.J. Talbot (2015)
Cleavage of a neuroinvasive human respiratory virus spike glycoprotein by proprotein convertases modulates neurovirulence and virus spread within the central nervous system.
PLoS Pathogens November 6.
Desforges, M., A. Le Coupanec, J.K. Stodola, M. Meessen-Pinard, and P.J. Talbot (2014)
Human coronaviruses : viral and cellular factors involved in neuroinvasiveness and neuropathogenesis.
Virus Res. 194: 145-158.
Brison, É., H. Jacomy, M. Desforges, and P.J. Talbot (2014)
Novel treatment with neuroprotective and antiviral properties against a neuroinvasive human respiratory virus.
J. Virol. 88: 1548-15623.
Desforges, M., A. Le Coupanec, É. Brison, M. Meessen-Pinard, and P.J. Talbot (2014)
Neuroinvasive and neurotropic human respiratory coronaviruses : potential neurovirulent agents in humans.
Adv. Exp. Med. Biol. 807: 75-96.
Desforges, M., A. Le Coupanec, É. Brison, M. Meessen-Pinard, et P.J. Talbot (2014)
Coronavirus humains respiratoires neuroinvasifs et neurotropes : agents neurovirulents potentiels.
Virologie 18: 5-16.
Desforges, M., J. Desjardins, C. Zhang, and P.J. Talbot (2013)
The acetyl-esterase activity of the hemagglutinin-esterase (HE) protein of human coronavirus OC43 strongly enhances the production of infectious virus.
J. Virol. 87: 3097-3107
Favreau, D.J., M. Meessen-Pinard, M. Desforges, and P.J. Talbot (2012)
Human coronavirus – induced neuronal programmed cell death is cyclophilin D – dependent and potentially caspase-dispensable.
J. Virol. 86: 81-93
Desforges, M., D.F. Favreau, É. Brison, J. Desjardins, M. Meessen-Pinard, H. Jacomy, and P.J. Talbot (2012)
Human coronaviruses : respiratory pathogens revisited as infectious neuroinvasive, neurotropic and neurovirulent agents.
In: Neuroviral Infections. Singh, S.K. and Ruzek, D., eds., Taylor & Francis Group, LLC/CRC Press, Chap. 5, pp. 93-120.
de Groot, R.J., S.C. Baker, R. Baric, L. Enjuanes, A. Gorbalenya, K.V. Holmes, S. Perlman, L. Poon, P. J.M. Rottier, P.J. Talbot, P.C.Y. Woo and J. Ziebuhr (2012)
In: Virus Taxonomy, Classification and Nomenclature of Viruses, Ninth Report of the International Committee on Taxonomy of Viruses, International Union of Microbiological Societies, Virology Division, King, A.M.Q., Adams, M. J., Carstens, E.B., and Lefkowitz, E.J., eds., ISBN : 978-0-12-384684-6, Elsevier Academic Press, Waltham, Massachusetts, U.S.A., pp. 806-828.
Ifergan, I., H. Kebir, J.I. Alvarez, G. Marceau, M. Bernard, L. Bourbonnière, J. Poiirier, P. Duquette, P.J. Talbot, N. Arbour, and A. Prat (2011)
CNS recruitment of effector memory CD8+ T lymphocytes during neuroinflammation is dependent on a4 integrin.
Talbot, P.J., M. Desforges, É. Brison, and H. Jacomy (2011)
Coronaviruses as encephalitis-inducing infectious agents.
In: Non-Flavivirus Encephalitis. Tkachev, S., ed.,
InTech – Open Access Publisher. ISBN 978-953-307-720-8. Chap. 9, pp. 185-202.
Brison, É., H. Jacomy, M. Desforges, and P.J. Talbot (2011)
Glutamate excitotoxicity is involved in the induction of paralysis in mice after infection by a human coronavirus with a single point mutation in its spike protein.
J. Virol. 85: 12464-12473
Cencic, R., M. Desforges, D.R. Hall, D. Kozakov, Y. Du, J. Min, R. Dingledine, H. Fu, S. Vajda, P.J. Talbot, and J. Pelletier (2011)
Blocking eIF4E-eIF4G interaction as a strategy to impair coronavirus replication.
J. Virol. 85: 6381-6389
Jacomy, H., J.R. St-Jean, É. Brison, G. Marceau, M. Desforges, and P.J. Talbot (2010)
Mutations in the spike glycoprotein of human coronavirus OC43 modulate disease in BALB/c mice from encephalitis to flaccid paralysis and demyelination.
J. Neurovirol. 16: 279-293
Favreau, D.J., M. Desforges, J. R. St-Jean, and P. J. Talbot (2009)
A human coronavirus OC43 variant harboring persistence-associated mutations in the S glycoprotein differentially induces the unfolded protein response in human neurons as compared to wild-type virus.
Virology 395: 255-267
Gagneur, S., S. Vallet, P. J. Talbot, M.-C. Legrand-Quillen, B. Picard, C. Payan, and J. Sizun (2008)
Outbreaks of human coronavirus in a paediatric and neonatal intensive care unit.
Eur. J. Pediatr. 167 : 1427-1434
Do Carmo, S., H. Jacomy, P.J. Talbot, and E. Rassart (2008)
Neuroprotective effect of Apolipoprotein D against human coronavirus OC43-induced encephalitis in mice.
J. Neurosci. 28: 10330-10338
Talbot, P.J., H. Jacomy, and M. Desforges (2007)
Pathogenesis of human coronaviruses, other than Severe Acute Respiratory Syndrome coronavirus.
In: The Nidoviruses, Perlman, S., Gallagher, T. and Snijder, E.J, eds., ASM Press. ISBN 978-1-55581-455-7. pp. 313-324.
Desforges, M., T. Miletti, M. Gagnon, and P.J. Talbot (2007)
Activation of human monocytic cells following infection by human coronavirus 229E.
Virus Res. 130: 128-140
Boucher, A., M. Desforges, P. Duquette, and P.J. Talbot (2007)
Long-term human coronavirus-myelin cross-reactive T-cell clones derived from multiple sclerosis patients.
Clin. Immunol. 123: 258-267
Jacomy, H., G. Fragoso, G. Almazan, W. E. Mushynski, and P.J. Talbot (2006)
Human coronavirus OC43 infection induces chronic encephalitis leading to motor disabilities in BALB/c mice.
Virology 349: 335-346
St-Jean, J.R., M. Desforges, F. Almazan, H. Jacomy, L. Enjuanes, and P.J. Talbot (2006)
Recovery of a neurovirulent human coronavirus OC43 from an infectious cDNA clone.
J. Virol. 80: 3670-3674
St-Jean, J., M. Desforges, and P.J. Talbot (2006)
Genetic evolution of human coronavirus OC43 in neural cell culture.
Adv. Exp. Med. Biol. 581: 499-502
Desforges, M., T. Miletti, M. Gagnon, and P.J. Talbot (2006)
HCoV-229E infects and activates monocytes.
Adv. Exp. Med. Biol. 581: 511-514
Jacomy, H., and P.J. Talbot (2006)
HCoV-OC43 induced apoptosis of murine neuronal cells.
Adv. Exp. Med. Biol. 581: 473-478
Gruslin, E., S. Moisan, Y. St-Pierre, M. Desforges, and P.J. Talbot (2005)
Transcriptome profile within the mouse central nervous system and activation of myelin-reactive T cells following murine coronavirus infection.
J. Neuroimmunol. 162:60-70
St-Jean, J., H. Jacomy, M. Desforges, A. Vabret, F. Freymuth, and P.J. Talbot (2005)
Genetic variability of human respiratory coronavirus OC43 : Authors’s reply to Letter to the Editor.
J. Virol. 79:3224-3225
Talbot, P.J., H. Jacomy, and E. Gruslin (2005)
Principles of immune-virus interactions in the nervous system.
In : Clinical Neuroimmunology, 2nd edition, Antel, J., Birnbaum, G., Hartung H.-P., and Vincent, A., eds., Oxford University Press, pp. 103-114
Talbot, P.J., A. Boucher, P. Duquette, and E. Gruslin (2005)
Coronaviruses and neuroantigens : myelin proteins, myelin genes.
In : Experimental models of multiple sclerosis. » Lavi, E., Constantinescu, C.S., eds., Kluwar Academic Publishers
Skowronski, D.M., C. Astell, R.C. Brunham, D.E. Low, M. Petric, R. Roper, P.J. Talbot, T. Tam, and L. Babiuk (2005)
Severe acute respiratory syndrome (SARS) : a year in review.
Annu. Rev. Med., 56: 357-381
St-Jean, J., H. Jacomy, M. Desforges, A. Vabret, F. Freymuth, and P.J. Talbot (2004)
Human respiratory coronavirus OC43 : genetic stability and neuroinvasion.
J. Virol. 78: 8824-8834
Jacomy, H., D. Boche, N. janabi, G. Guillemin, N. Arbour, J. van Beek, C. Canova and P.J. Talbot (2004)
Cellules microgliales : pathologie.
Dans: Neuroanatomie fonctionnelle de la cellules aux comportements. Vol. 7, Guillemin, G., ed., pp. 99-148 & 188-206
Adachi, D., G. Johnson, R. Draker, M. Ayers, T. Mazzulli, P.J. Talbot, and R. Tellier (2004)
Comprehensive detection and identification of human coronaviruses, including the SARS-associated coronavirus, with a single RT-PCR assay.
J. Virol. Meths 122: 29-36
Vallet, S., A. Gagneur, P.J. Talbot, M.-C. Legrand, J. Sizun, and B. Picard (2004)
Detection of human coronavirus 229E in nasal specimens in large scale studies using an RT-PCR hybridization assay
Mol. Cell. Probes 18: 75-80
Jacomy, H., and P.J. Talbot (2003)
Vacuolating encephalitis in mice infected by human coronavirus OC43.
Virology 315: 20-33
Qin, Y., P. Duquette, Y. Zhang, M. Olek, R.-R. Da, J. Richardson, J. P. Antel, P. Talbot, N. R. Cashman, W. W. Tourtellotte, H. Wekerle, and S. Van Den Noort (2003)
Intrathecal B-cell clonal expansion, an early sign of humoral immunity, in the cerebrospinal fluid of patients with clinically isolated syndrome suggestive of multiple sclerosis.
Lab. Invest., 83: 1081-1088
Nilges, K., H. Höhn, H. Pilch, C. Neukirch, K. Freitag, P.J. Talbot, and M.J. Maeurer (2003)
Human papillomavirus type 16 E7 peptide-directed CD8(+) T cells from patients with cervical cancer are cross-reactive with the coronavirus ns2 protein.
J. Virol. 77: 5464-5474
Breslin, J.J., I. Mørk, M.K. Smith, L.K. Vogel, E.M. Hemmila, A. Bonavia, P.J. Talbot, H. Sjöström O. Norén, and K.V. Holmes (2003)
Human coronavirus 229E: receptor binding domain and neutralization by soluble receptor at 37°C.
J. Virol. 77: 4435-4438
Bonavia, A., B.D. Zelus, D.E. Wentworth, P.J. Talbot, and K.V. Holmes (2003)
Identification of the receptor binding domain of HCoV-229E spike glycoprotein.
J. Virol. 77: 2530-2538
Wolfson, C., and P. Talbot (2002)
Bacterial infections as a cause of multiple sclerosis.
Lancet 360: 352-353
Gagneur, A., M.C. Legrand, B. Picard, R. Baron, P.J. Talbot, L. de Parcsau, et J. Sizun (2002)
Infections nosocomiales à coronavirus humains chez le nouveau-né.
Arch. Pédiatr. 9: 61-69
Gagneur, A., J. Sizun, S. Vallet, M.C. Legrand, B. Picard, and P.J. Talbot (2002)
Coronavirus-related nosocomial viral respiratory infections in a neonatal and paediatric intensive care unit : a prospective study.
J. Hosp. Infect. 00: 1-6
Desforges, M., G. Despars, S. Bérard, M. Gosselin, M.O. McKenzie, D.S. Lyles, P.J. Talbot, and L. Poliquin (2002)
Matrix protein mutations participate to inefficient induction leading to persistent infection of human neural cells by vesicular stomatitis virus.
Virology 295: 63-73
Plumb, J., W. P. Duprex, C. S. Cameron, C. Richter-Landsberg, P.J. Talbot, and S. McQuaid (2002)
Infection of human oligodendroglioma cells by a recombinant measles virus expressing enhanced green-fluorescent protein.
J. Neurovirol. 8: 24-34
Talbot, P.J. (2001)
Coronaviruses and the development of multiple sclerosis.
In: Strange Bedfellows : Infection & Chronic Disease, Conference Report, Canadian Public Health Association (www.cpha.ca) , pp. 19-20.
Boucher, A., F. Denis, P. Duquette, and P.J. Talbot (2001)
Generation from multiple sclerosis patients of long-term T-cell clones that are activated by both human coronavirus and myelin antigens.
Adv. Exp. Med. Biol. 494: 355-362
Jacomy, H., and P.J. Talbot (2001)
Susceptibility of murine CNS to OC43 infection.
Adv. Exp. Med. Biol. 494: 101-107
Desforges, M., J. Charron, S. Bérard, S. Beausoleil, G. Despars, J. Bell, P.J. Talbot, C.P. Stanners, and L. Poliquin (2001)
Different host-cell shutoff strategies related to the matrix protein lead to persistence of vesicular stomatitis virus mutants on fibroblast cells.
Virus Res. 76: 87-102
Boucher, A., M. Tremblay, N. Arbour, J. Edwards, R. Day, J. Newcombe, P. Duquette, F. Denis, P.J. Talbot (2001)
The role of neuroinvasive human coronaviruses in autoimmune processes associated with multiple sclerosis.
In: Genes and Viruses in Muliple Sclerosis Hommes OR, Wekerle H, Clanet M, eds. Elsevier Science pp. 209-220.
Talbot, P.J., D. Arnold, and J.P. Antel (2001)
Virus-induced autoimmune reactions in the nervous system.
Curr. Top. Microbiol. Immunol. 253: 247-271
Arbour, N.,R. Day, J. Newcombe, and P.J. Talbot (2000)
Neuroinvasion by human respiratory coronaviruses.
J. Virol. 74: 8913-8921
Edwards, J., F. Denis, and P.J. Talbot (2000)
Activation of glial cells by human coronavirus OC43.
J. Neuroimmunol. 108: 73-81
Sizun, J., M.W.N. Yu, and P.J. Talbot (2000)
Survival of human coronaviruses 229E and OC43 in suspension and after drying on surfaces: a possible source of nosocomial infections.
J. Hosp. Infect. 46: 55-60
Yu, M.W.N., J.K. Scott, A. Fournier, and P.J. Talbot (2000)
Characterization of murine coronavirus neutralization epitopes with phage-displayed peptides.
Virology 271: 182-196
Yu, M.W.N., and P.J. Talbot (2000)
Characterization of protection against coronavirus infection by non-internal image anti-idiotypic antibody.
Viral Immunol. 13: 93-106
Enjuanes, L., D.A. Brian, D. Cavanagh, K.V. Holmes, M.C. Lai, H. Laude, P. Masters, P. Rottier, S.G. Siddell, W.J.M. Spaan, F. Taguchi, and P.J. Talbot (1999)
In: Virus Taxonomy, Seventh report of the International Committee on Taxonomy of Viruses, Murphy, F.A., Fauquet, C.M., Bishop, D.H.L., Ghabrial, S.A., Jarvis, A.W., Martelli, G.P., Mayo, M.A., and Summers, M.D., eds., Academic Press, New York, pp. 835-849
Talbot, P., D. Dalençon, F. Lambert, R. Alain, J.C. Artault, J. Borg, and L.L. Sarliève (1999)
Les oligodendrocytes en culture infectés par le coronavirus murin représentent-ils un modèle de démyélinisation virale.
Médecine Sciences 15: XII-XIV
Freedman, M.S., R. Ransohoff, P.J. Talbot, and S.S. Zamvil (1999)
Highlights from the Fifth International Congress of the International Society of Neuroimmunology.
J. Neuroimmunol. 97: 4-8
Arbour, N., G. Côté, C. Lachance, M. Tardieu, N.R. Cashman, and P.J. Talbot (1999)
Acute and persistent infection of human neural cell lines by human coronavirus OC43.
J. Virol. 73: 3338-3350
Arbour, N., S. Ekandé, G. Côté, C. Lachance, F. Chagnon, M. Tardieu, N.R. Cashman, and P.J. Talbot (1999)
Persistent infection of human oligodendrocytic and neuroglial cell lines by human coronavirus 229E.
J. Virol. 73: 3326-3337
Chagnon, F., A. Lamarre, C. Lachance, M. Krakowski, T. Owens, J.F. Laliberté, P.J. Talbot (1998)
Characterization of the expression and immunogenicity of the ns4b protein of human coronavirus 229E.
Can J. Microbiol. 44: 1012-1017
Talbot, P.J. (1998)
Triggering of autoimmune diseases by molecular mimicry of self-antigens by microbial pathogens: a possible link between coronaviruses and multiple sclerosis.
Med. Update Ther. Diagn. Prev. 1: 45-47
Qin, Y., P.. Duquette, Y. Zhang, P. Talbot, R. Poole, and J. Antel (1998)
Clonal Expansion and Somatic Hypermutation of VH Genes of B Cells from Cerebrospinal Fluid in Multiple Sclerosis.
J. Clin. Invest. 102 : 1045-1050
Lachance C, N. Arbour, N.R. Cashman, and P.J. Talbot (1998)
Involvement of aminopeptidase N (CD13) in infection of human neural cells by human coronavirus 229E.
J. Virol. 72: 6511-6519
Arbour, N., and P.J. Talbot (1998)
Persistent infection of neural cell lines by human coronaviruses.
Adv. Exp. Med. Biol. 440: 575-581
Sizun, J., N. Arbour, and P.J. Talbot (1998)
Comparison of immunofluorescence with monoclonal antibodies and RT-PCR for the detection of human coronaviruses 229E and OC43 in cell culture.
J. Virol. Methods 72: 145-152
Lamarre, A., M.W.N. Yu, F. Chagnon, P.J. Talbot (1997)
A recombinant single chain antibody neutralizes coronavirus infectivity but only slightly delays lethal infection of mice.
Eur. J. Immunol. 27: 3447-3455
Lamarre, A., and P.J. Talbot (1997)
Characterization of phage-displayed anti- idiotypic antibody fragments against coronavirus-neutralizing monoclonal antibodies.
Viral Immunol. 10: 175-182
Talbot, P.J. (1997)
Virus-induced autoimmunity in multiple sclerosis: the coronavirus paradigm.
Adv. Clin. Neurosci. 7: 215-233
Cavanagh, D., D.A. Brian, M. Brinton, L. Enjuanes, M.C. Horzinek, M.M.C. Lai, H. Laude, P.G.W. Plagemann, S. Siddell, W.J.M. Spaan, and P.J. Talbot (1997)
Nidovirales: a new order comprising Coronaviridae and Arteriviridae.
Arch. Virol. 142: 629-633
Bonavia, A., N. Arbour, V. Wee Yong, and P.J. Talbot (1997)
Infection of primary cultures of human neural cells by human coronaviruses 229E and OC43.
J. Virol. 71: 800-806
Yu, M.W.N., S. Lemieux, and P.J. Talbot (1996)
Genetic control of anti-idiotypic vaccination against coronavirus infection.
Eur. J. Immunol. 26: 3230-3233
Talbot,P.J., Jn-S. Paquette, C. Ciurli, J.P. Antel, and F. Ouellet (1996)
Myelin basic protein and human coronavirus 229E cross-reactive T cells in multiple sclerosis.
Ann. Neurol. 39: 233-240