Skip to main content
NCBI home page
Wiley - PMC COVID-19 Collection logoLink to Wiley - PMC COVID-19 Collection
. 2008 May 12;10(1):1–10. doi: 10.1111/j.1365-2990.1984.tb00335.x

CAN VIRAL ENVELOPE GLYCOLIPIDS PRODUCE AUTO‐IMMUNITY, WITH REFERENCE TO THE CNS AND MULTIPLE SCLEROSIS?

H E WEBB 1,✉, J K FAZAKERLEY 1
PMCID: PMC7168014  PMID: 6330601

Abstract

Many viruses, with lipid envelopes derived from the host cell membranes, have been implicated in the aetiology of multiple sclerosis (MS), and epidemiological studies support an infectious agent. Alternatively the disease is thought by other workers to be auto‐immune in nature, and recently much attention has been focused on immunological sensitivity to glycolipids in MS patients. In this paper it is proposed that CNS demyelination could arise in susceptible individuals (HLA type) from an immune response to glycolipids, triggered by the carrier effect of one or more enveloped neurotropic viruses.

References

  1. Adams J.M., Brooks M.B., Fisher E.D. & Tyler C.S. (1970) Measles antibodies in patients with multiple sclerosis and with other neurological and non‐neurological diseases. Neurology 20, 1039–42. [DOI] [PubMed] [Google Scholar]
  2. Allison A.C. (1971) Unresponsiveness to self antigens. Lancet ii, 1401. [DOI] [PubMed] [Google Scholar]
  3. Almeida J.D. & Waterson A.P. (1969) The morphology of virus antibody interaction. Advances in Virus Research 15, 307–338. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Arnon R., Crisp E., Kelly R., Ellison S.W., Myes L.W. & Tourtellotte W.W. (1980) Anti‐ganglioside antibodies in multiple sclerosis. Journal of the Neurological Science 26, 179–186. [DOI] [PubMed] [Google Scholar]
  5. Blough H.A. & Merlie J.P. (1970) The lipids of incomplete influenza virus. Virology 40, 68–92. [DOI] [PubMed] [Google Scholar]
  6. Burks J.S., Devald‐Macmillan B., Jankovsky L. & Gerdes J. (1979) Characterisation of coronaviruses isolated using multiple sclerosis autopsy brain material. Neurology 29, 547. [Google Scholar]
  7. Catalano L.W. Jr (1972) Herpes virus hominis antibody in multiple sclerosis and amyotropic lateral sclerosis. Neurology 22, 473–478. [DOI] [PubMed] [Google Scholar]
  8. Cook S.D., Dowling P.C. & Russell W.C. (1979) Neutralizing antibodies to canine distemper and measles virus in multiple sclerosis. Journal of the Neurological Sciences 41, 61–70. [DOI] [PubMed] [Google Scholar]
  9. Cox K.O. & Keast D. (1973) Rauscher virus infection, in virus erythrocyte clearance studies, and auto‐immune phenomena. Journal of the National Cancer Institute 50, 941–946. [DOI] [PubMed] [Google Scholar]
  10. Davison A.M. & Ilyas A.A. (1982) Cyclosporin A inhibits ganglioside‐stimulated lymphocyte rosette formation in multiple sclerosis. International Archives of Allergy and Applied Immunology 69, 393–396. [DOI] [PubMed] [Google Scholar]
  11. Dubois‐Dalcq M., Niedieck B. & Buyse M. (1970) Action of anticerebroside sera on myelinated tissue cultures. Pathologia Europea 5, 331–337. [PubMed] [Google Scholar]
  12. Erlandson R.A., Babcock V.I., Southam C.M., Bailey R.B. & Shipkey R.H. (1967) Semliki Forest virus in HEp‐2 cell cultures. Journal of Virology 1, 996–1009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Fazakerley J.K., Amor S. & Webb H.E. (1983) Reconstitution of Semliki Forest virus infected mice, induces immune mediated pathological changes in the CNS. Clinical and Experimental Immunology 52, 115–120. [PMC free article] [PubMed] [Google Scholar]
  14. Feinsod F.M., Spielman A. & Swaner J.L. (1975) Neutralisation of Sindbis virus by antisera to antigens of vector mosquitoes. American Journal of Tropical Medicine and Hygiene 24, 533–536. [DOI] [PubMed] [Google Scholar]
  15. Fry J.M., Weissbarth S., Lehrer G.M. & Bornstein M.B. (1974) Cerebroside antibody inhibits sulfatide synthesis in myelination and demyelination in cord tissue culture. Science 183, 540–542. [DOI] [PubMed] [Google Scholar]
  16. Gudnadottir M., Helgadottir H., Bjarnason O. & Jonsdottir K. (1964) Virus isolated from the brain of a patient with multiple sclerosis. Experimental Neurology 9, 85–95. [DOI] [PubMed] [Google Scholar]
  17. Harboe A., Schoyen R. & Bye‐Hansen A. (1966) Haemaglutination inhibition by antibody to host material of fowl plague virus grown in different tissues of chick chorioallantoic membranes. Acta Pathologica et Microbiologica Scandinavica 67, 573–578. [DOI] [PubMed] [Google Scholar]
  18. Herzberg L. (1976) Persistence of encephalitogenic arboviruses in brain cell cultures. Brain Research Association 1st Annual Conference Bath 68th April 1976.
  19. Heydrick F.P., Comer J.F. & Wachter R.F. (1971) Phospholipid composition of Venezuelan equine encephalomyelitis virus. Journal of Virology 7, 642–645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hirschberg C.B. & Robbins P.W. (1974) The glycolipids and phospholipids of Sindbis virus and their relation to the lipids of the host cell plasma membrane. Virology 61, 602–608. [DOI] [PubMed] [Google Scholar]
  21. Horikawa Y., Tsubaki T. & Nakajima M. (1973) Rubella antibody in multiple sclerosis. Lancet i, 996–997. [DOI] [PubMed] [Google Scholar]
  22. Illavia S.J. & Webb H.E. (1968) The maintenance of encephalitogenic viruses by non‐neuronal cerebral cells. British Medical Journal 1, 94–95. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Illavia S.J., Webb H.E. & Pathak S. (1982) Demyelination induced in mice by avirulent Semliki Forest virus. I. Virology and effects on optic nerve. Neuropathology and Applied Neurobiology 8, 35–42. [DOI] [PubMed] [Google Scholar]
  24. Ilyas A.A. & Davison A.N. (1983) Cellular hypersensitivity to gangliosides and myelin basic protein in multiple sclerosis. Journal of the Neurological Sciences 59, 85–95. [DOI] [PubMed] [Google Scholar]
  25. Jagelman S., Suckling A.J., Webb H.E. & Bowen E.T.W. (1978) The pathogenesis of avirulent Semliki Forest virus infections in athymic nude mice. Journal of General Virology 41, 599–607. [DOI] [PubMed] [Google Scholar]
  26. Kates M., Allison A.C., Tyrrell D.A.J. & James A.T. (1961) Lipids of influenza virus and their relation to those of the host cell. Biochimica et Biophysica Acta 52, 455–466. [Google Scholar]
  27. Kelly W.R., Blakemore W.F., Jagelman S. & Webb H.E. (1982) Demyelination induced in mice by avirulent Semliki Forest virus. II. An ultrastructural study of focal demyelination in the brain. Neuropathology and Applied Neurobiology 8, 43–53. [DOI] [PubMed] [Google Scholar]
  28. Klenk H.D. & Chopin P.W. (1969) Lipids of plasma membranes of monkey and hamster kidney cells and of parainfluenza virions grown in these cells. Virology 38, 255–268. [DOI] [PubMed] [Google Scholar]
  29. Klenk H.D. & Choppin P.W. (1970a) Plasma membrane lipids and parainfluenza virus assembly. Virology 66, 939–947. [DOI] [PubMed] [Google Scholar]
  30. Klenk H.D. & Choppin P.W. (1970b) Glycosphingolipids of plasma membrane of cultured cells and an enveloped virus (SV5) grown in these cells. Proceedings of the National Academy of Sciences (USA) 66, 57–64. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Konat G., Offner H., Lev‐Ram V., Cohen O., Schwartz M., Cohen I.R. & Sela B‐A (1982) Abnormalities in brain myelin of rabbits with experimental autoimmune multiple sclerosis‐like disease induced by immunization to gangliosides. Acta Neurologica Scandinauica 66, 568–574. [DOI] [PubMed] [Google Scholar]
  32. Laine R., Kettunen M., Gahmberg C.G., Kaarianinen L. & Renkonen O. (1972) Fatty chains of different lipid classes of SFV and host cell membranes. Journal of Virology 10, 433–438. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Leibowitz S. & Gregson N.A. (1979) Brain glycolipids as cell surface antigens Clinical Neuro‐immunology, ed. Clifford Rose F., pp. 29–41. Blackwell Scientific Publications, Oxford . [Google Scholar]
  34. Lumsden C.E. (1972) The clinical pathology of multiple sclerosis In Multiple Sclerosis ‐ A Reappraisal, 2nd edition, eds McAlpine D., Lumsden C.E. & Acheson E.D., pp. 317–319 Churchill Livingstone, Edinburgh . [Google Scholar]
  35. Luukkonen A., Kaariainen L. & Renkonen O. (1976) Phospholipids of SFV grown in cultured mosquito cells. Biochimica Biophysica Acta 450, 109–120. [DOI] [PubMed] [Google Scholar]
  36. Marcus D.M. & Schwarting G.A. (1976) Immunochemical properties to glycolipids and phospholipids. Advances in Immunology 23, 203–240. [PubMed] [Google Scholar]
  37. Ter Meulen V., Muller D., Kackell Y., Katz M. & Meyermann R. (1972) Isolation of infectious measles virus in measles encephalitis. Lancet ii, 1172–1175. [DOI] [PubMed] [Google Scholar]
  38. Ter Meulen V. & Stephenson J.R. (1983) The possible role of viral infections in multiple sclerosis and other related demyelinating diseases In Multiple Sclerosis, eds. Hallpike J.F., Adams C.W.M. & Tourtellotte W.W., pp. 241–274. Chapman and Hall, London . [Google Scholar]
  39. Miyamoto H., Walker J.E., Ginsburg A.H., Burks J., McIntosh K. & Kempe C.H. (1976) Antibodies to vaccinie and measles virus in multiple sclerosis patients. Archives of Neurology 33, 414–418. [DOI] [PubMed] [Google Scholar]
  40. Nagai Y., Momoi T., Saito M., Mitzuwawa E. & Ontani S. (1976) Ganglioside syndrome, a new autoimmune neurologic disorder, experimentally induced with brain ganglioside. Neuroscience Letters 2, 107–111. [DOI] [PubMed] [Google Scholar]
  41. Nakajima H. & Obara J. (1967) Physicochemical studies of Newcastle disease virus 3. The content of virus nucleic acid and its sedimentation pattern. Archiv für die gesamte virusforschung 20, 287–295. [DOI] [PubMed] [Google Scholar]
  42. Neighbour P.A. & Bloom P.N.A.S. (1979) Abscence of virus‐induced lymphocyte suppression and interferon production in MS. Proceeding of the National Academy of Science (USA) 76,476–480. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Nordal H.J., Vandvik B. & Norrby E. (1978) Multiple sclerosis: local synthesis of electrophoretically restricted measles, rubella, mumps, and herpes simplex virus antibodies in the central nervous system. Scandinavian Journal of Immunology 7, 473–479. [DOI] [PubMed] [Google Scholar]
  44. Oaten S.W., Bowen E.T.W. & Webb H.E. (1976) Enhanced resistance of mice to infection with Langat (TP21) virus following pre‐treatment with Sindbis or Semliki Forest virus. Journal of General Virology 33, 381–388. [DOI] [PubMed] [Google Scholar]
  45. Oaten S.W., Webb H.E. & Jagelman S. (1980) Resistance of mice to infection with West Nile virus following pretreatment with Sindbis, Semliki Forest and Chikungunya virus. Microbios Letters 13, 85–90. [Google Scholar]
  46. Offner H., Konat G. & Sela B‐A. (1981) Multi‐sialo brain gangliosides are powerful stimulators of active E‐rosetting lymphocytes from multiple sclerosis patients. Journal of the Neurological Sciences 52, 279–287. [DOI] [PubMed] [Google Scholar]
  47. Palacios R. & Moller G. (1981) Cyclosporin‐A blocks receptors for HLA‐DR antigens on T‐cells. Nature (London) 290,792–794. [DOI] [PubMed] [Google Scholar]
  48. Pathak S. & Webb H.E. (1974) Possible mechanisms for the transport of Semliki Forest virus into and within mouse brain. Journal of the Neurological Sciences 23, 175–184. [DOI] [PubMed] [Google Scholar]
  49. Pathak S. & Webb H.E. (1976) Paramyxovirus‐like inclusions in brain of patient with severe multiple sclerosis. Lancet ii, 311. [DOI] [PubMed] [Google Scholar]
  50. Pathak S., Illavia S.J. & Webb H.E. (1983) The identification and role of cells involved in C.N.S. demyelination in mice after Semliki Forest virus infection: an ultrastructural study. Immunology of nervous system. Progress in Brain Research 59, 237–254. [DOI] [PubMed] [Google Scholar]
  51. Precious S.W., Webb H.E. & Bowen E.T. (1976) Effect of two defined strains of Semliki Forest virus on cultures of suckling mouse brain cells. Microbios Letters 1, 23–36. [Google Scholar]
  52. Prineas J.W. (1972) Paramyxo‐like particles associated with acute demyelination in chronic relapsing multiple sclerosis. Science 178, 760–763. [DOI] [PubMed] [Google Scholar]
  53. Quigley J.P., Rifkin D.B. & Reich E. (1971) Phospholipid composition of Rous sarcoma virus, host cell membranes and other enveloped RNA viruses. Virology 46, 106–116. [DOI] [PubMed] [Google Scholar]
  54. Rapport M.M. & Graf L. (1969) Immunochemical reaction of lipids. Progress in Allergy, ed. Kallos P. et al, pp. 273–331. [PubMed]
  55. Raine C.S., Johnson A.B., Marcus D.M., Suzuki A. & Bornstein M.B. (1981) Demyelination in vitro. Journal of the Neurological Sciences 52, 117–131. [DOI] [PubMed] [Google Scholar]
  56. Reilly C.A. Jr & Schloss G.T. (1971) The erythrocyte as virus carrier in Friend and Rauscher virus leukemias. Cancer Research 31, 841–846. [PubMed] [Google Scholar]
  57. Renkonen O., Kaarainen L., Simons K. & Bahmbeg C.G. (1971) The lipid class composition of Semliki Forest virus and of plasma membranes of the host cells. Virology 46, 318–326. [DOI] [PubMed] [Google Scholar]
  58. Rogers N.G., Basnight M., Gibbs C.J. Jr & Gajdusek D.C. (1967) Latent viruses in chimpanzees with experimental Kuru. Nature (London) 216,445–449. [DOI] [PubMed] [Google Scholar]
  59. Roitt I. (1980) Essential Immunology, pp. 306–309. Blackwell Scientific Publications, Oxford . [Google Scholar]
  60. Rook G.A.W. & Webb H.E. (1970) Anti‐lymphocyte serum and tissue culture used to investigate the role of cell‐mediated response in viral encephalitis in mice. British Medical Jouranl 4, 210–212. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Rose N.R. & Witebsky E. (1968) Thyroid autoantibodies in thyroid disease. Advances in Metabolic Diseases 3, 231–277. [DOI] [PubMed] [Google Scholar]
  62. Saida T., Saida K., Dorfman S., Silberger D.H., Summer A.J., Manning M.C., Lisak R.P. & Brown M.N. (1979) Experimental allergic neuritis induced by sensitization with galactocerebrosides. Science 204, 1103–1106. [DOI] [PubMed] [Google Scholar]
  63. Sela B‐A., Konat A.B. & Offner H. (1982) Elevated ganglioside concentration in serum and peripheral blood lymphocytes from multiple sclerosis patients in remission. Journal of the Neurological Sciences 54, 143–148. [DOI] [PubMed] [Google Scholar]
  64. Salmi A., Gollmar Y., Norrby E. & Panelius M. (1973) Antibodies against three different structural components of measles virus in patients with multiple sclerosis, their sibling and matched controls. Acta Pathologica et Microbiologica Scandinauica 81B, 627–634. [DOI] [PubMed] [Google Scholar]
  65. Soule D.W., Marinetti G.V. & Morgan H.R. (1959) Studies of the haemolysis of red blood cells by mumps virus. IV. Quantitative study of changes in red blood cell lipids and of virus lipids. Journal of Experimental Medicine 110, 93–102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Steck A.J., Tschannen R. & Schaefer R. (1981) Induction of antimyelin and antioligodendrocyte antibodies by vaccinia virus ‐ an experimental study in the mouse. Journal of Neuroimmunology 1, 117–124. [DOI] [PubMed] [Google Scholar]
  67. Webb H.E., Mehta S., Leibowitz S. & Gregson N.A. (1984) Immunological reaction of the demyelinating Semliki Forest virus with immune serum to glycolipids and its possible importance to central nervous system viral autoimmune disease. Neuropathology and Applied Neurobiology 10, in press. [PubMed] [Google Scholar]
  68. Zlotnik I., Grant D.P. & Batter‐Hatton D. (1972) Encephalopathy in mice following inapparent Semliki Forest virus infection. British Journal of Experimental Pathology 53, 125–129. [PMC free article] [PubMed] [Google Scholar]

Articles from Neuropathology and Applied Neurobiology are provided here courtesy of Wiley

RESOURCES