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The Concept of Neurotropism and Selective Vulnerability (“Pathoclisis”) in Virus Infections of the Nervous System — A Historical Overview

  • G. Gosztonyi
  • H. Koprowski
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 253)

Abstract

Nervous diseases that we regard now to be of viral origin were known and described already in antiquity and in medieval times. Rabies, poliomyelitis and yellow fever belong to this category. The contagious nature of these diseases was suspected for centuries, and their symptomatology suggested that the brain is preferentially targeted by these infections. Not long after the advent of virology, the viral etiology of these diseases was proven. That such agents may have a special affinity to neural structures was first documented by experimental studies on rabies. Cantani (1888), Professor of Internal Medicine in Naples, laid down the concept of the neural spread of rabies: transection of limb nerves after peripheral inocu­lation prevented the evolution of the disease. One year later, two of his pupils, Di Vestea and Zagari (1889), published a more elaborate study on this subject in the Annales de l’Institut Pasteur; the recognition of the neural spread of rabies is attributed to these researchers in the literature. Schaffer (1890), in Budapest, provided evidence for the neural spread of rabies in humans based on histological studies: the most severe changes developed in spinal cord segments corresponding to the site of the animal bite. These early studies clearly established that the agent of rabies has such an elementary affinity to neural structures that it spreads exclusively along these pathways to the central nervous system (CNS).

Keywords

Rabies Virus Spinal Cord Segment Selective Vulnerability Acute Disseminate Encephalomyelitis Subacute Sclerosing Panencephalitis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Barbanti-Brodano G, Oyanagi S, Katz M, Koprowski H (1970) Presence of two different viral agents in brain cells of patients with subacute sclerosing panencephalitis. Proc Soc Exp Biol (NY) 134: 230–236Google Scholar
  2. Bauer HJ (1998) Heinrich Pette (1887–1964) In: Schliack H, Hippius H (eds) Nervenärzte — Biographien. Georg Thieme Verlag, Stuttgart, New York, pp 129–137Google Scholar
  3. Bouteille M, Fontaine C, Vedrenne CL, Delarue J (1965) Sur un cas d’encéphalite subaigue à inclusions. Etude anatomoclinique et ultrastructurelle. Rev Neurol 118: 454–458Google Scholar
  4. Callebaut C, Krust B, Jacotot E, Hovanessian AG (1993) T cell activation antigen, CD26, as a cofactor for entry of HIV in CD4+ cells. Science 262: 2045–2050PubMedCrossRefGoogle Scholar
  5. Cantani A (1888) Ueber die Verbreitung des Wuthgiftes längs der Nerven und Pasteur’s Schutzimpfungen. Wiener Med Wschr 38: 1061–1062Google Scholar
  6. Ciardi A, Sinclair E, Scaravilli F, Harcourt-Webster NJ, Lucas S (1990) The involvement of the cerebral cortex in human immunodeficiency virus encephalopathy: a morphological and immunohistochemical study. Acta Neuropathol 81: 51–59PubMedCrossRefGoogle Scholar
  7. Co MS, Gaulton GN, Fields BN, Greene MI (1985a) Isolation and biochemical characterization of the mammalian reovirus type 3 cell-surface receptor. PNAS USA 82: 1494–1498PubMedCrossRefGoogle Scholar
  8. Co MS, Gaulton GL, Tominaga A, Homcy CJ, Fields BN, Greene MI (1985b) Structural similarities between the mammalian ß-adrenergic and reovirus type 3 receptors. Proc Natl Acad Sci USA 82: 5315–5318PubMedCrossRefGoogle Scholar
  9. Conolly JH, Allen IV, Hurwitz Li, Millar JHD (1967) Measles virus antibody and antigen in subacute sclerosing panencephalitis. Lancet 1: 542–544CrossRefGoogle Scholar
  10. Davis LE, Johnson RT (1979) An explanation for the localization of herpes simplex encephalitis? Ann Neurol 5: 2–5PubMedCrossRefGoogle Scholar
  11. Dawson JR Jr (1933) Cellular inclusions in cerebral lesions of lethargic encephalitis. Am J Pathol 9:7–15 Dimmock NJ (1982) Initial stages of infection with animal viruses. J Gen Virol 59: 1–22Google Scholar
  12. Di Vestea A, Zagari G (1889) La transmission de la rage par voie nerveuse. Ann Inst Pasteur 3:237–248 Fields BN, Greene MI (1982) Genetic and molecular mechanism of viral pathogenesis: implications for prevention and treatment. Nature 300: 19–23Google Scholar
  13. Gaulton GN, Greene MI (1989) Inhibition of cellular DNA synthesis by reovirus occurs through a receptor-linked signaling pathway that is mimicked by antüdiotypic, antireceptor antibody. J Exp Med 169: 197–211PubMedCrossRefGoogle Scholar
  14. Gosztonyi G, Ludwig H (1984) Neurotransmitter receptors and viral neurotropism. Neuropsychiatr Clin 3: 107–114Google Scholar
  15. Gosztonyi G, Ludwig H (1995) Borna disease–neuropathology and pathogenesis. Curr Top Microbiol Immunol 190: 39–73PubMedCrossRefGoogle Scholar
  16. Gosztonyi G, Artigas J, Lamperth L, Webster H deF (1994) Human immunodeficiency virus (HIV) encephalitis: study of 19 cases with combined use of in situ hybridization and immunocytochemistry. J Neuropathol Exp Neurol 53: 521–534Google Scholar
  17. Gosztonyi G, Dietzschold B, Kao M, Rupprecht CE, Koprowski H (1993) Rabies and Borna disease: a comparative pathogenetic study of two neurovirulent agents. Lab Invest 68: 285–295PubMedGoogle Scholar
  18. Green H (1974) The gene for the poliovirus receptor. New Eng J Med 290: 1018–1019PubMedCrossRefGoogle Scholar
  19. Greenfield JG (1950) Encephalitis and encephalomyelitis in England and Wales during the last decade. Brain 73: 141–166PubMedCrossRefGoogle Scholar
  20. Haywood AM (1994) Virus receptors: binding, adhesion strengthening, and changes in viral structure. J Virol 68: 1–5PubMedGoogle Scholar
  21. Holland JJ (1961) Receptor affinities as major determinants of enterovirus tissue tropism in humans. Virology 15: 312–326PubMedCrossRefGoogle Scholar
  22. Holland JJ, McLaren LC, Syverton JT (1959) The mammalian cell virus relationship. IV. Infection of naturally insusceptible cells with enterovirus ribonucleic acid. J Exp Med 110: 65–79Google Scholar
  23. Joest E, Degen K (1909) Über eigentümliche Kerneinschlüsse der Ganglienzellen bei der enzootischen Gehirn-Rückenmarksentzündung der Pferde. Z Inf Krkh Haustiere 6: 348–356Google Scholar
  24. Johnson RT, Mims CA (1968) Pathogenesis of viral infections of the nervous system. New Eng J Medicine 278:23–30, 84–92Google Scholar
  25. Katz M, Koprowski H (1973) The significance of failure to isolate infectious viruses in cases of subacute sclerosing panencephalitis. Arch Ges Virusforschung 41: 390–393CrossRefGoogle Scholar
  26. Környey St (1933) Die Bedeutung der mesodermalen Reaktion und der Systemelektivität in der Pathologie der Poliomyelitis. Z Neur 146: 724–746Google Scholar
  27. Környey St (1939) Die primär neurotropen Viruskrankheiten des Menschen. Fortschr Neurol Psychiat 11:82–100 and 146–166Google Scholar
  28. Lentz TL, Burrage TG, Smith AL, Crick J, Tignor GH (1982) Is the acetylcholine receptor a rabies virus receptor? Science 215: 182–184PubMedCrossRefGoogle Scholar
  29. Levaditi C (1921) Comparaison entre les divers ultra-virus neurotropes (Ectodermoses neurotropes). C R Soc Biol 85: 425–429Google Scholar
  30. Levaditi C (1922) Ectodermoses neurotropes - poliomyélite, encéphalite, herpès. Etude clinique, histo-pathologique et expérimentale. Masson, ParisGoogle Scholar
  31. Levaditi C (1938) Les ultravirus des maladies humaines. Librairie Maloine, ParisGoogle Scholar
  32. Levaditi C, Voet J (1935) Nouvelle classification des ectodermoses neurotropes. C R Acad Sci 201: 743–745Google Scholar
  33. Ludwig H, Kraft W, Kao M, Gosztonyi G, Dahme E, Krey H (1985) Borna-Virus-Infection (Borna-Krankheit) bei natürlich und experimentell infizierten Tieren: ihre Bedeutung für Forschung und Praxis. Tierärztl Prax 13: 421–453PubMedGoogle Scholar
  34. Ludwig H, Bode L, Gosztonyi G (1988) Borna disease: a persistent virus infection of the central nervous system. Prog Med Virol 35: 107–151PubMedGoogle Scholar
  35. Marsh M, Helenius A (1989) Virus entry into animals cells. Adv Virus Res 36: 107–151PubMedCrossRefGoogle Scholar
  36. Mazlo M, Herndon M (1977) Progressive mulitifocal leukoencephalopathy: ultrastructural findings in two brain biopsies. Neuropathol Appl Neurobiol 3: 323–339CrossRefGoogle Scholar
  37. Mazlo M, Tariska I (1982) Are astrocytes infected in progressive multifocal leukoencephalopathy (PML)? Acta Neuropathol 56: 45–51PubMedCrossRefGoogle Scholar
  38. Mendelsohn CL, Wimmer E, Racaniello VR (1989) Cellular receptor for poliovirus: Molecular cloning, nucleotide sequence, and expression of a new member of the immunoglobulin superfamily. Cell 56: 855–865Google Scholar
  39. Negri A (1903) Beitrag zum Studium der Histologie der Tollwuth. Z Hyg Infektionskrankheiten 43: 507–528Google Scholar
  40. Nepom JT, Weiner HL, Dichter MA, Tardieu M, Spriggs DR, Gramm CF, Powers ML, Fields BN, Greene MI (1982) Identification of a hemagglutinin-specific idiotype associated with reovirus recognition shared by lymphoid and neural cells. J Exp Med 155: 155–167PubMedCrossRefGoogle Scholar
  41. Petito CK (1996) Neuropathology of human immunodeficiency virus: questions and answers. Editorial. Human Pathol 27: 623–624CrossRefGoogle Scholar
  42. Pette H (1929) Akute Infektion und Nervensystem. Munch Med Wochenschr 76: 225–230Google Scholar
  43. Pette H (1938) Die akut entzündlichen Erkrankungen des Zentralnervensystems. Verh Deutsch Ges Inn Med, Fünfzigster Kongress, 486–540Google Scholar
  44. Pette H (1942) Die akut entzündlichen Krankheiten des Nervensystems. Thieme, LeipzigGoogle Scholar
  45. Pette H, Döring G (1939) Über einheimische Panencephalitis vom Charakter der Encephalitis japonica. D Zeitschr Nervenheilk 149: 7–44CrossRefGoogle Scholar
  46. Radermecker J (1956) Systématique et électroencéphalographie des encéphalites et encéphalopathies. EEG Clin Neurophysiol Suppl No. 5. Masson, ParisGoogle Scholar
  47. Reagan KJ, Wunner WH (1985) Rabies virus interaction with various cell lines is independent of the acetylcholine receptor. Arch Virol 84: 277–282PubMedCrossRefGoogle Scholar
  48. Rivers TM, Sprunt DH, Berry GP (1933) Observations on attempts to produce acute disseminated encephalomyelitis in monkeys. J Exp Medicine 58: 39–53CrossRefGoogle Scholar
  49. Rivers TM, Schwentker FF (1935) Encephalomyelitis accompanied by myelin destruction experimentally produced in monkeys. J Exp Med 61: 689–702PubMedCrossRefGoogle Scholar
  50. Sabin AB, Olitsky PK (1938) Influence of host factors on neuroinvasiveness of vesicular stomatitis virus: III. Effect of age and pathway of infection on the character and localization of lesions in the central nervous system. J Exp Med 67: 201–228Google Scholar
  51. Sauvé GJ, Saragovi HU, Greeve MI (1993) Reovirus receptors. Adv Virus Res 42:325–341 Schaffer K (1890) Pathologie und pathologische Anatomie der Lyssa. Beitr Pathol Anat 7: 189–144Google Scholar
  52. Seifried O, Spatz H (1930) Die Ausbreitung der encephalitischen Reaktion bei der Bornaschen Krankheit der Pferde und deren Beziehungen zu der Encephalitis epidemica, der Heine-Medinschen Krankheit und der Lyssa des Menschen. Z Neurol Psychiat 124: 317–382CrossRefGoogle Scholar
  53. Spatz H (1930) Einteilung der echten Encephalitiden vom morphologischen Stand punkt aus. In: Handbuch der Geisteskrankheiten, Bd. 11, Spezieller Teil VII, Die Anatomie der Psychosen. Springer, Berlin, pp. 196–224Google Scholar
  54. Spatz H (1931) Über Encephalitis und Encephalitiden. Nervenarzt 4:466–472, 531–542Google Scholar
  55. Spriggs DR, Bronson RT, Fields BN (1983) Hemagglutinin variants of reovirus type 3 have altered central nervous system tropism. Science 220: 505–507PubMedCrossRefGoogle Scholar
  56. Meulen V, Katz M, Müller D (1972) Subacute sclerosing panencephalitis. A review. Curr Top Microbiol Immunol 57: 1–38Google Scholar
  57. Tyler KL, Bronson RT, Byers KB, Fields B (1985) Molecular basis of viral neurotropism: experimental reovirus infection. Neurology 35: 88–92PubMedCrossRefGoogle Scholar
  58. Bogaert L (1945) Une leucoencéphalite sclérosante subaiguë? J Neurol Neurosurg Psychiat 8: 101–120CrossRefGoogle Scholar
  59. Vogt C, Vogt O (1922) Erkrankungen der Grosshirnrinde im Lichte der Topistik, Pathoklise und Pathoarchitektonik. J Psychol Neurol 28: 1–171Google Scholar
  60. Vogt H (1912) Encephalitis nonpurulenta. In: Lewandowsky M (ed) Handbuch der Neurologie. Dritter Band, Spezielle Neurologie II. Berlin, Springer, pp 229–276Google Scholar
  61. Walters MNI, Leak PJ, Joske RA, Stanley NF, Perret DH (1965) Murine infection with reovirus. III. Pathology of infection with types 1 and 2. Br J Exp Pathol 46: 200–212PubMedGoogle Scholar
  62. Weiner HL, Drayna D, Averill DL Jr, Fields BN (1977) Molecular basis of reovirus virulence: role of the SI gene. PNAS USA 74: 5744–5748PubMedCrossRefGoogle Scholar
  63. Weiss RA, Tailor CS (1995) Retrovirus receptors. Cell 82: 531–533PubMedCrossRefGoogle Scholar
  64. ZuRhein GM, Chou SM (1965) Particles resembling papovaviruses in human cerebral demyelinating disease. Science 148: 1477–1479PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2001

Authors and Affiliations

  • G. Gosztonyi
    • 1
  • H. Koprowski
    • 2
  1. 1.Department of NeuropathologyUniversity Clinics Benjamin Franklin, Freie Universität BerlinBerlinGermany
  2. 2.Department of Microbiology and Immunology, Jefferson Alumni HallCenter for NeurovirologyPhiladelphiaUSA

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