Sporadic amyotrophic lateral sclerosis: A hypothesis of persistent (non-lytic) enteroviral infection

Amyotrophic Lateral Sclerosis and Other Motor Neuron Disorders

Volumn 6, Issue 2, 2005, Pages 77-87

  Ravits, John ^a  

^a BENAROYA RESEARCH INSTITUTE   (United States)

Author keywords

Amyotrophic lateral sclerosis; Apoptosis; Capsid binding compounds; Enterovirus; Persistent viral infection; Poliovirus receptor

Indexed keywords

[(OXAZOLYLPHENOXY)ALKYL]ISOXAZOLE DERIVATIVE; ALPHA INTERFERON; ANTIVIRUS AGENT; CELL SURFACE RECEPTOR; PLECONARIL; PROTEINASE INHIBITOR; RECOMBINANT INTERCELLULAR ADHESION MOLECULE; UNCLASSIFIED DRUG; VIRUS RECEPTOR; VIRUS VACCINE;

AMYOTROPHIC LATERAL SCLEROSIS; APOPTOSIS; BLOOD BRAIN BARRIER; CHRONICITY; CLINICAL FEATURE; CONFORMATIONAL TRANSITION; DISEASE MODEL; DRUG RECEPTOR BINDING; ENTEROVIRUS INFECTION; GENETIC SUSCEPTIBILITY; HUMAN; IMMUNE RESPONSE; INOCULATION; LASER MICRODISSECTION; MOTONEURON; MUSCLE WEAKNESS; NERVE CELL NECROSIS; NERVE FIBER; NONHUMAN; PERSISTENT INFECTION; POLIOMYELITIS VIRUS; PREDICTION; PRIORITY JOURNAL; PROTEIN POLYMORPHISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; SIDE EFFECT; SYNAPSE; TRANSGENIC ANIMAL; VIROGENESIS; VIRUS CAPSID; VIRUS DETECTION; VIRUS GENOME; VIRUS PATHOGENESIS;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; APOPTOSIS; CAPSID PROTEINS; ENTEROVIRUS; ENTEROVIRUS INFECTIONS; HUMANS; POLIOVIRUS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 21344470889     PISSN: 14660822     EISSN: None     Source Type: Journal    
DOI: 10.1080/14660820510027026     Document Type: Review

References (203)

1. de la Torre JC, Oldstone MBA. Anatomy of viral persistence: mechanisms of persistence and associated disease. Adv Virus Research. 1996;46:311-43.
2. Salazar-Gureso EF, Roos RP. Amyotrophic lateral sclerosis and viruses. Clin Neurosci. 1995;3:360-7.
3. Rowland LP, Shneider NA. Amyotrophic lateral sclerosis. NEJM. 2001;344:1688-700.
4. Viola M, Myers J, Gramm K, Gibbs JC Jr, Roos RP. Failure to detect poliovirus genetic information in amyotrophic lateral sclerosis. Ann Neurol. 1979;5:402-3.
5. Cremer N, Oshiro L, Norris F. Cultures of tissues from patients with amyotrophic lateral sclerosis. Arch Neurol. 1973;29:331-3.
6. Muller WK, Schaltenbrtand G. Attempts to reproduce amyotrophic lateral sclerosis in laboratory animals by inoculation of Schu virus isolated from patient with apparent amyotrophic lateral sclerosis. J Neurol. 1979;220:1-19.
7. Norris FJ Jr. Current status of the search for virus in amyotrophic lateral sclerosis. Neuro Neuro Psychiatr. 1977;18(Suppl. 2-3): 443-54.
8. Weiner LP, Stohlman SA, Davis R. Attempts to demonstrate virus in amyotrophic lateral sclerosis. Neurology. 1980;30: 1319-22.
9. Gibbs CJ, Gajdusek DC. An update on long-term in vivo and in vitro studies designed to identify a virus as the cause of amyotrophic lateral sclerosis, Parkinsonism dementia and Parkinson's disease. In: Rowland LP, editor. Human Motor Neuron Diseases. New York: Raven Press; 1982. pp 343-53.
10. Fallis RJ, Weiner LP. Further studies in search of a virus in amyotrophic lateral sclerosis. In: Rowland LP, editor. Human Motor Neuron Diseases. New York: Raven Press; 1982. pp 355-61.
11. Kennedy PGE. On the possible role of viruses in the eetiology of motor neuron disease: a review. J Royal Soc Med. 1990;83:784-7.
12. Jubelt B. Viruses and motor neuron diseases. Adv Neurol. 1991;56:463-72.
13. Fraser H, Behan W, Chree A, Crossland G, Behan P. Mouse inoculation studies reveal no transmissible agent in amyotrophic lateral sclerosis. Brain Pathology. 1996;6:89-100.
14. Miller J, Guntaka RM, Myers J. Amyotrophic lateral sclerosis. Search for poliovirus by nucleic acid hybridization. Neurology. 1980;30:884-6.
15. Kohne DE, Gibbs CJ, White L, Tracy SM, Meinke W, Smith RA. Virus detection by nucleic acid hybridization examination of normal and ALS tissues for the presence of poliovirus. J Gen Virol. 1981;56:223-33.
16. Brachic M, Smith RA, Gibbs CJ, Garruto RM, Tourtellotte WW, Cash E. Detection of picornavirus sequences in nervous tissue of amyotrophic lateral sclerosis and control patients. Ann Neurol. 1985;18:337-43.
17. Love S. The search for a transmissible agent in ALS. Brain Patrol. 1996;6:99-100.
18. Muir P, Nicholson F, Spencer GT, Ajetunmobi JF, Starkey WG, Khan M, et al. Enterovirus infection of the central nervous system of humans: lack of association with chronic neurological disease. J Gen Virol. 1996;77:1469-76.
19. Muir P, van Loon AM. Enterovirus infections of the central nervous system. Intervirology. 1997;40:153-66.
20. Harber J, Bernhardt G, Lu H, Sgro JY, Wimmer E. Canyon rim residues, including antigenic determinants, modulate serotype-specific binding of polioviruses to mutants of the poliovirus receptor. Virology. 1995;214:559-70.
21. Bodian D. Histopathologic basis of clinical findings in poliomyelitis. Am J Med. 1949;6:563-78.
22. Sabin AB, Ward R. The natural history of human poliomyelitis. I. Distribution of virus in nervous and non-nervous tissues. J Exp Med. 1941;73:771-93.
23. Johnson RT. Selective vulnerability of neural cells to viral infections. In: Rowland LP, editor. Human Motor Neuron Diseases. New York: Raven Press; 1982. pp 331-7.
24. Salazar-Grueso EF, Cashmann NR, Maselli R, Roos RP. Upper motor neuron findings in patients with antecedent poliomyelitis. Neurology. 1987;37(Suppl1): 215.
25. Melchers W, de Villser M, Jongen P, van Loon A, Nibbeling R, Oostvogel P, et al. The postpolio syndrome: no evidence for poliovirus persistence. Ann Neurol. 1992;32:728-32.
26. Dalakas MC, Illa I. Post-polio syndrome: concepts in clinical diagnosis, pathogenesis and etiology. Adv Neurol. 1991;56:495-511.
27. Giraud P, Kopp N, Lina B, Chazot G. La sclérose latérale amotrophique: implication des entérovirus? Rev Neurol. (Paris). 2000;156:352-6.
28. Harter DH. Viruses other than poliovirus in human amyotrophic lateral sclerosis. In: Rowland LP, editor. Human Motor Neuron Diseases. New York: Raven Press; 1982. pp 339-42.
29. Westarp ME, Foring B, Rasmussen H, Schraff S, Mertens T, Kornhuber HH. Human spuma retrovirus antibodies in amyotrophic lateral sclerosis. Neuro, Psych, Brain Res. 1992;1:1-4.
30. Westarp ME, Ferrante P, Perron H, Bartmann P, Kornhuber HH. Sporadic ALS/MND: a global neurodeneration with retroviral involvement? J Neurol Sci. 1995;129(Suppl): 145-7.
31. Rosener M, Hahn H, Kranz M, Heeney J, Rethwilm A. Absence of serological evidence for foamy virus infection in patients with amyotrophic lateral sclerosis. J Med Virol. 1996;48:222-6.
32. Andrews WD, Tuke PW, Al-Chalabi A, Gaudin P, Ijaz S, Parton MJ, Garson JA. Detection of reverse transcriptase activity in the serum of patients with motor neuron disease. J Med Virol. 2000;61:527-32.
33. Moulignier A, Moulonguet A, Pialoux G, Rozenbaum W. Reversible ALS-like disorder in HIV infection. Neurology. 2001;57:995-1001.
34. MacGowan DJ, Scelsa SN, Waldron M. An ALS-like syndrome with new HIV infection and complete response to antiretroviral therapy. Neurology. 2001;57:1094-7.
35. Jubelt B, Berger JR. Does viral disease underlie ALS? Lessons from the AIDS pandemic. Neurology. 2001;57:945-6.
36. Cermelli C, Vinceti M, Beretti F, Pietrini V, Nacci G, Pietrosemoli P, et al. Risk of sporadic amyotrophic lateral sclerosis associated with seropositivity for herpesviruses and echovirus-7. Eur J Epidemiol. 2003;18:123-7.
37. Andrews WE, Al-Chalabi A, Garson JA. Lack of evidence for HTLV tax-rex DNA in motor neuron disease. J Neurol Sci. 1997;153:86-90.
38. Sola P, Bedin R, Casoni F, Barozzi P, Mandrioli J, Merelli E. New insights into the viral theory of amyotrophic lateral sclerosis: study on the possible role of Kaposi's sarcoma-associated virus/human herpesvirus 8. Eur Neurol. 2002;47:108-12.
39. Mullis KB, Faloona FA. Specific synthesis of DNA in vitro via a polymerase-catalysed chain rection. Methods Enzymol. 1987;155:335-50.
40. Saiki R, Gelfand DH, Stoffel S, Scharf SJ, Higuchi R, Horn GT, et al. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 1988;239:487-91.
41. Hyypia T, Auvinen P, Maaronen M. Polymerase chain reaction for human picornaviruses. J Gen Virol. 1989;70: 3261-8.
42. Rotbart HA. Enzymatic RNA amplification of the enteroviruses. J Clin Microbiol. 1990;28:438-42.
43. Chapman NM, Tracy S, Gauntt CJ, Fortmueller U. Molecular detection and identification of enteroviruses using enzymatic amplification and nucleic acid hybridization. J Clin Microbiol. 1990;28:843-50.
44. Woodall CJ, Riding MH, Graham DI, Clements GB. Sequences specific for enterovirus detected in spinal cord from patients with motor neuron disease. Br Med J. 1994;308:1541-3.
45. Berger MM, Kopp N, Vital C, Redl B, Aymard M, Lina B. Detection and cellular localization of enterovirus RNA sequences in spinal cord of ALS patients. Neurology. 2000;54:20-25.
46. Giraud P, Beaulieux F, Ono S, Shimizu N, Chazot G, Lina B. Detection of enteroviral sequences from frozen spinal cord samples of Japanese ALS patients. Neurology. 2001;56:1777-8.
47. Swanson NR, Fox SA, Mastaglia FI. Search for persistent infection with poliovirus or other enteroviruses in amyotrophic lateral sclerosis. Neuromusc Disord. 1995;5:457-65.
48. Walker MP, Schlaberg R, Hays AP, Bowser R, Lipkin WI. Absence of echovirus sequences in brain and spinal cord of amyotrophic lateral sclerosis patients. Ann Neurol. 2001;49:249-53.
49. Nix WA, Berger MM, Oberste MS, Brooks BR, McKenna-Yasek DM, Brown RH Jr, et al. Failure to detect enterovirus in the spinal cord of ALS patients using a sensitive RT-PCR method. Neurology. 2004;62:1372-7.
50. Oldstone MBA. Viruses can cause disease in the absence of morphological evidence of cell injury: implication for uncovering new diseases in the future. J Inf Diseases. 1989;159:384-9.
51. Oldstone MB. Viral persistence: mechanisms and consequences. Current Opinion in Microbiolgy. 1998;1:436-41.
52. Ahmed R, Morrison LA, Knipe DM. Viral persistence. In: Nathanson N, et al., eds, Viral Pathogenesis. Philadelphia: Lippincott-Raven Publishers; 1997. Chapter 9.
53. Lipton HL, Gilden DH. Viral diseases of the nervous system: persistent infections. In: Nathanson N, et al., eds, Viral Pathogenesis. Philadelphia: Lippincott-Raven Publishers; 1997. Chapter 36, 1997.
54. Ter Meulen V, Carter MJ, Wege H, Watanabe R. Mechanisms and consequences of virus persistence in the human nervous system. Ann NY Acad Sci. 1984;436:86-97.
55. Ahmed R, Chen ISY, editors, Persistent Viral Infections. Chichester: John Wiley & Sons; 1999.
56. Alcami A, Koszinowski UH. Viral mechanisms of immune evasion. Trends Microbiol. 2000;8:410-8.
57. Mahalingam S, Meanger J, Foster P, Lidbury BA. The viral manipulation of the host cellular and immune environments to enhance propagation and survival: a focus on RNA viruses. J Leukocyte Biology. 2002;72:429-39.
58. Vossen MTM, Westerhout EM, Soöderbert-Nauclér C, Wiertz EJ. Viral immune evasion: a masterpiece of evolution. Immunogenetics. 2002;54:527-42.
59. Frisk G. Mechanisms of chronic enteroviral persistence in tissue. Current Opin Infect Dis. 2001;14:251-6.
60. McKinney RE, Katz SL, Wilfert CM. Chronic enteroviral meningoencephalitis in agammaglobulinemic patients. Rev Infects Dis. 1987;9:334-56.
61. Zhang S, Racaneillo VR. Peristent echovirus infection of mouse cells expressing the viral receptor VLA-2. Virology. 1997;235:293-301.
62. Pavio N, Buc-Caron MH, Colbere-Garpin F. Persistent poliovirus infection of human fetal brain cells. J Virol. 1996;70:6395-401.
63. Carp RI. Persistent infection of human lymphoid cells with poliovirus and development of temperature sensitive mutants. Intervirology. 1981;15:49-56.
64. Lloyd RE, Bovee M. Persistent infection of human erythroblastoid cells by poliovirus. Virology. 1993;194: 200-9.
65. Colbere-Garapin F, Christodoulou C, Crainic R, Pelletier I. Persistent poliovirus infection of human neuroblastoma cells. Proc Natl Acad Sci. USA. 1989;86:7590-4.
66. Borzakian S, Couderc T, Barbier Y, Attal G, Pelletier I, Colbere-Garapin F. Persistent poliovirus infection: establishment and maintenance involve distinct mechanisms. Virology. 1992,186:398-408.
67. Pelletier I, Duncan G, Pavio, et al. Molecular mechanisms of poliovirus persistence: key role of capsid determinants during the establishment phase. Cell Mol Life Sci. 1998;54:1385-1402.
68. Blondel B, Duncan G, Couderc T, et al. Molecular aspects of poliovirus biology with a special focus on the interactions with nerve cells. J NeuroVirol. 1998;4:1-26.
69. Morrison ME, He YJ, Wien MW, Hogle JM, Racaniello VR. Homolog-scanning mutagenesis reveals poliovirus receptor residues important for virus binding and replication. J Virol. 1994;68:2578-88.
70. Colbere-Garapin F, Jacques S, Drillet AS, Pavio N, Couderc T, Blondel B, et al. Poliovirus persistence in human cells in vitro. Dev Biol. (Basel). 2001;105:99-104.
71. Destombes J, Couderc T, Thiesson D, Girard S, Wilt SG, Blondel B. Persistent poliovirus infection in mouse motor neurons. J Virol. 1997;71:1621-8.
72. Leparc-Goffart I, Julien J, Fuchs F, Janatova I, Aymard M, Kopecka H. Evidence for the presence of poliovirus genomic sequences in the CSF of patients with post-polio syndrome. J Clin Microbiol. 1996;34:2023-6.
73. See DM, Kean KM, Kopecka H. Analysis of the sequence of a poliovirus type 2-like defective interfering virus from the cerebrospinal fluid of a patient with post-polio syndrome. Abstract 5th Congres de la Societe Franaise de Microbiologie, Lille, France, April 28 1998.
74. Julien J, Leparc-Goffart I, Lina B, Fuchs F, Foray S, Janatova I, et al. Post-polio syndrome: poliovirus persistence is involved in the pathogenesis. J Neurol. 1999;246:472-6.
75. Leon-Monzon ME, Dalakas MC. Detection of poliovirus antibodies and poliovirus genome in patients with the post-polio syndrome. Ann NY Acad Sci. 1995;753:208-18.
76. Sharief MK, Hentges R, Ciardi M. Intrathecal immune response in patients with the post-polio syndrome. N Engl J Med. 1991;325:749-55.
77. Galbraith DN, Nairn C, Clements GB. Evidence for enteoviral persistence in humans. J Gen Virology. 1997;78: 307-12.
78. Kristensson K, Norrby E. Persistence of RNA viruses in the central nervous system. Ann Rev Microbiol. 1986;40: 159-84.
79. Johnson RT. Chronic inflammatory and demyelinating diseases. In: Viral Infections of the Nervous System (2nd edn). Philadelphia: Lippincott-Raven Press; 1998. Chapter 10.
80. Coles A, Scolding N. Immune responses and the nervous system. In: Scolding N, editor. Immunological and Inflammatory Disorders of the Central Nervous System. Oxford: Butterworth Heinemannn; 1999. Chapter 1. pp 1-20.
81. Jolly E, Mucke L, Oldstone M. Viral persistence in neurons explained by lack of major histocompatibility class I expression. Science. 1991;253:1283-5.
82. Perlman S, Wu GF. Selection of and evasion from cytotoxic T-cell responses in the central nervous system. In: Buchmeier MJ, Campbell MJ, editors. Neurovirology: Viruses and the Brain. San Diego: Academic Press; 2001. pp 219-42.
83. McGeer PL, McGeer EG. Inflammatory processes in amytrophic lateral sclerosis. Muscle Nerve. 2002;26: 459-70.
84. McGreer PL, Itagaki S, McGreer EG. Expression of histocompatibility glycoprotein HLA-DR in neurological disease. Acta Neuropathol. 1988;76:550-7.
85. Troost D, van den Oord JJ, de Jong JM, Swaab DF. Lymphocytic infiltration in the spinal cord of patients with amyotrophic lateral sclerosis. Clin Neuropathology. 1989;8: 289-94.
86. Engelhardt JI, Appel SH. IgG reactivity in the spinal cord and motor neurons in amyotrophic lateral sclerosis. Arch Neurol. 1990;47:1210-6.
87. Lampson LA, Kushner PD, Sobel RA. Major histocompatibility complex antigen expression in the affected tissues in amyotrophic lateral sclerosis. Ann Neurol. 1990;28: 365-72.
88. Troost D, Van den Oord JJ, De Jong JMBV. Immunohistochemical characterization of the inflammatory infiltrate in amyotrophic lateral sclerosis. Neuropath Appl Neurobiol. 1990;16:401-10.
89. Kawamata T, Akiyama H, Yamada T, McGeer PL. Immunologic reactions in amyotrophic lateral sclerosis brain and spinal cord tissue. Am J Path. 1992;140:691-707.
90. Engelhardt JI, Tajti J, Appel SH. Lymphocytic infiltrate in the spinal cord in amyotrophic lateral sclerosis. Arch Neurol. 1993;50:30-6.
91. Roulston A, Marcellus RC, Brapton PE. Viruses and apoptosis. Annu Rev Microbiol. 1999;53:577-628.
92. O'Brien V. Viruses and apoptosis. J Gen Virol. 1998;79:1833-45.
93. Hardwick JM. Viral-induced apoptosis. Adv Pharmacol. 1997;41:295-336.
94. Young LS, Dawson C, Eliopsulos AG. Viruses and apoptosis. Br Med Bull. 1997;53:509-21.
95. Shen Y, Shenk TE. Viruses and apoptosis. Curr Opin Genet Dev. 1995;5:105-11.
96. Allsopp TE, Fazakerley JK. Altruistic cell suicide and the specialized case of the virus-infected nervous system. Trends Neurosci. 2000;23:284-90.
97. Thomson BJ. Viruses and apoptosis. Int J Exp Pathol. 2001;82:65-76.
98. Barber GN. Host defense, viruses and apoptosis. Cell Death Differ. 2001;8:113-26.
99. Fazakerley JK, Allsopp TE. Programmed cell death in virus infections of the nervous system. Curr Top Microbiol Immunol. 2001;253:95-119.
100. Ubol S, Tucker PC, Griffin DE, Hardwick JM. Neurovirulent strains of alphavirus induce apoptosis in bcl-2-expressing cells: role of a single amino acid change in the E2 glycoprotein. Proc Natl Acad Sci. USA. 1994;91:5202-6.
101. Levine B, Huang Q, Isaacs JT, Reed JC, Griffin DE, Hardwick JM. Conversion of lytic to persistent alphavirus infection by bcl-2 cellular oncogene. Nature. 1993;361:739-42.
102. Tolskaya EA, Romanova LI, Kolesnikova MS, Ivannikova TA, Smirnova EA, Raikhlin NT, et al. Apoptosis-inducing and apoptosis-preventing functions of poliovirus. J Virol. 1995;69:1181-9.
103. Agol VI, Belov GA, Bienz K, Egger D, Kolesnikova MS, Raikhlin NT, et al. Two types of death of poliovirus-infected cells: caspase involvement in the apoptosis but not cytopathic effect. Virology. 1998;252:343-53.
104. Girard S, Couderc T, Destombes J, Thiesson D, Delpeyroux F, Blondel B. Poliovirus induces apoptosis in the mouse central nervous system. J Virol. 1999;73:6066-72.
105. Barco A, Feduchi E, Carrssco L. Poliovirus protease 3Cpro kills cells by apoptosis. Virology. 2000;266:352-60.
106. Goldstaub D, Gradi A, Bercovitch Z, Grosmann Z, Nophar Y, Luria S, et al. Poliovirus 2A protease induces apoptotic cell death. Mol Cell Biol. 2000;20:1271-7.
107. Blaschke AJ, Weiner JA, Chun J. Programmed cell death is a universal feature of embryonic and postnatal neuroproliferative regions throughout the central nervous system. J Comp Neurol. 1998;396:39-50.
108. Johnson EM, Deckwerth TL. Molecular mechanisms of developmental neuronal death. Annu Rev Neurosci. 1993;16:31-46.
109. Yuan J, Yankner BA. Apoptosis in the nervous system. Nature. 2000;407:802-9.
110. Burek MJ, Oppenheim RW. Cellular interactions that regulate programmed cell death in the developing vertebrate nervous system. In: Koliatsos VE, Ratan RR, editors. Cell death and diseases of the nervous system. New Jersey: Humana Press Inc; 1999. pp 145-179.
111. Yoshiyama Y, Yamada T, Asanuma K, Asahi T. Apoptosis related antigen, Ley and nick-end labeling are positive in spinal motor neurons in amyotrophic lateral sclerosis. Acta Neuropathol. 1994;88:207-11.
112. Troost D, Aten J, Morsink F, de Jong JM. Apoptosis in amyotrophic lateral sclerosis in not restricted to motor neurons. Bcl-2 expression is increased in unaffected post-central gyrus. Neuropath Appl Neurobiol. 1995;21: 498-504.
113. Mu X, He J, Anderson DW, Trojanowski JQ, Springer JE. Altered expression of bcl-2 and bax mRNA in amyotrophic lateral sclerosis spinal cord motor neurons. Ann Neurol. 1996;40:379-86.
114. Martin LJ. Neuronal death in amyotrophic lateral sclerosis is apoptosis: possible contribution of a programmed cell death mechanism. J Neuropathol Exp Neurol. 1999;58:459-71.
115. Ekegren T, Grundstrom E, Lindholm D, Aquilonius SM. Up-regulation of Bax protein and increased DNA degradation in ALS spinal cord motor neurons. Acta Neurol Scand. 1999;1000:317-21.
116. Sathasivam S, Ince PG, Shaw PJ. Apoptosis in amyotrophic lateral sclerosis: a review of the evidence. Neuropathol Appl Neurobiol. 2001;27:257-74.
117. Guégan C, Przedborski S. Programmed cell death in amyotrophic lateral sclerosis. J Clin Invest. 2003;111:153-61.
118. Griffin DE, Hardwick JM. Perspective: virus infections and the death of neurons. Trends Microbiol. 1999;7:155-60.
119. Everett H, McFadden G. Apoptosis: an innate immune response to virus infection. Trends Microbiol. 1999;7: 160-5.
120. Friedlander RM. Apoptosis and caspases in neurodegenerative diseases. NEJM. 2003;348:1365-75.
121. Gosztonyi G, Koprowski H. The concept of neurotropism and selective vulnerability ('pathoclisis') in virus infections of the nervous system: a historical overview. Curr Top Microbiol Immunol. 2001;253:1-13.
122. Evans DJ, Almond JW. Cell receptors for picornaviruses as determinants of cell tropism and pathogenesis. Trends Microbiol. 1998;6:198-202.
123. Rossmann MG, Bella J, Kolatkar PR, He Y, Wimmer E, Kuhn RJ, et al. Cell recognition and entry by rhinoviruses and enteroviruses. Virology. 2000;269:239-47.
124. Rossmann MG, He Y, Kuhn RJ. Picornavirus-receptor interactions. Trends Microbiol. 2002;10:324-31.
125. Ohka S, Nomoto A. Recent insights into poliovirus pathogenesis. Trends Microbiology. 2001;9:501-6.
126. Nomoto A, Koike S, Aoki HJ. Tissue tropism and species specificity of poliovirus infection. Trends Microbiology. 1994;2:47-51.
127. Rossmann MG, Bella J, Kolatkar R, He Y, Wimmer E, Kuhn RJ, et al. Cell recognition and entry by rhinoviruses and enteroviruses. Virology. 2000;269:239-47.
128. Belnap DM, McDermott BM Jr, Filman DJ, Cheng N, Trus BL, Zuccola HJ, et al. Three-dimensional structure of poliovirus receptor bound to poliovirus. Proc Natl Acad Sci. 2000;97:73-8.
129. Gromeier M, Lu HH, Bernhardt G, Harber JJ, Bibb JA, Wimmer E. The human poliovirus receptor: receptor-virus interaction and parameters of disease specificity. Ann NY Acad Sci. 1995;753:19-36.
130. Bernhardt G, Bibb JA, Bradley J, Wimmer E. Molecular characterization of the cellular receptor for poliovirus. Virology. 1994;199:105-13.
131. Racaneillo VR. The poliovirus receptor: a hook or an unzipper? Structure. 1996;4:769-73.
132. Solecki D, Gromeier M, Harber J, Bernhardt G, Wimmer E. Poliovirus and its cellular receptor: a molecular genetic dissection of a virus/receptor affinity interaction. J Mol Recogn. 1998;11:2-9.
133. Racaniello VR. Early events in poliovirus infection: virus-receptor interactions. Poc Natl Acad Sci. USA. 1996;93:11378-81.
134. Mendelsohn C, Johnson B, Lionetti KA, Nobis P, Wimmer E, Racaniello VR. Transformation of a human poliovirus receptor gene into mouse cells. Proc Natl Acad Sci. USA. 1986;83:7845-9.
135. Rossman MG. The canyon hypothesis: hiding the host cell receptor attachment site on a viral surface from immune surveillance. J Biol Chem. 1989;264:14587-90.
136. Wien MW, Chow M, Hogle JM. Poliovirus: new insights from an old paradigm. Structure. 1996;4:763-7.
137. Belnap DM, McDermott BM, Filman DJ, Cheng N, Trus BL, Succola HJ, et al. Three-dimensional structure of poliovirus receptor bound to poliovirus. PNAS. 2000;97:73-8.
138. He Y, Bowman VD, Mueller S, Bator CM, Bella J, Peng X, et al. Interaction of the poliovirus receptor with poliovirus. PNAS. 2000;97:79-84.
139. Brown RH Jr, Johnson D, Ogonowski M, Weiner HL. Type 1 human poliovirus binds to human synaptosomes. Ann Neurol. 1987;21:64-70.
140. Freistadt MF, Kaplan G, Racaniello VR. Heterogeneous expression of poliovirus receptor-related proteins in human cells and tissues. Mol Cell Biol. 1990;10:5700-6.
141. Mendelsohn C, Wimmer E, Racaniello VR. Cellular receptor for poliovirus: molecular cloning, nucleotide sequence and expression of a new member of the immunoglobulin suerfamily. Cell. 1989;56:855-65.
142. Yang WX, Terasaki T, Shiroki K, Ohka S, Aoki J, Tanabe S, et al. Efficient delivery of circulating poliovirus to the central nervous system independently of poliovirus receptor. Virology. 1997;229:421-8.
143. Crotty S, Hix L, Sigal LJ, Andino R. Poliovirus pathogenesis in a new poliovirus receptor transgenic mouse model: age-dependent paralysis and a mucosal route of infection. J Gen Virol. 2002;83:1707-20.
144. Ida-Hosonuma M, Iwasaki T, Taya C, Sato Y, Li J, Nagata N. Comparison of neuropathogenicity of poliovirus in two transgenic mouse strains expressing human poliovirus receptor with different distribution patterns. J Gen Virol. 2002;83:1095-105.
145. Andino R, Boddeker N, Silvera D, Gamarnik AV. Intracellular determinants of picornavirus replication. Trends Microbiol. 1999;7:76-82.
146. Jubelt B, Narayan O, Johnson RT. Pathogenesis of human poliovirus infection in mice. II. Age-dependency of paralysis. J Neuropathol Exp Neurol. 1980;39:149-59.
147. Johnson RT. Pathogenesis of poliovirus infections. Ann NY Acad Sci. 1995;753:361-5.
148. Johnson RT. Pathogenesis of central nervous system infections. In: Johnson RT, editor. Viral Infections of the Nervous System (2nd edn). Philadelphia: Lippincott-Raven; 1998. Chapter 3.
149. Ren R, Racaniello VR. Poliovirus spreads from muscle to the central nervous system by neural pathways. J Infect Dis. 1992;166:747-52.
150. Illa I, Leon-Monzon M, Agboatwalla M, Dure-Samin A, Dalakas MC. Role of muscle in acute poliomyelitis infection. Ann NY Acad Sci. 1995;753:58-67.
151. Gromeier M, Wimmer E. Mechanism of injury-provoked poliomyelitis. J Virol. 1998;72:5056-60.
152. Bradford-Hill A, Knowelden J. Inoculation and poliomyelitis: a statistical investigation in England and Wales in 1949. Br Med J. 1950;2:1-6.
153. McCloskey BP. The relationship of prophylactic inoculations to the onset of poliomyelitis. Lancet. 1950;2:659-63.
154. Sutter RW, Patriarca PA, Suleiman AJ, Brogan S, Malankar PG, Cochi SL, et al. Attributable risk of DTP injection in provoking paralytic poliomyelitis during a large outbreak in Oman. J Infect Dis. 1992;165:444-9.
155. Strebel PM, Ion-Nedelcu N, Baughman AL, Sutter RW, Cochi SL. Intramuscular injections within 30 days of immunization with oral poliovirus vaccine: a risk for vaccine-associated paralytic poliomyelitis. NEJM. 1995;332:500-6.
156. Nathanson N, Langmuir AD. The Cutter incident: poliomyelitis following formaldehyde inactivated poliovirus vaccination in the United States during the spring of 1955. Am J Hyg. 1963;78:16-81.
157. Bodian D, Horstmann DH. Polioviruses. In: Horsfall FL, Tamm I, editors. Viral and rickettsial Infections of man. Philadelphia: Lippincott; 1965. pp 430-73.
158. Bodian D, Howe HA. The rate of progression of poliomyelitis virus in nerves. Bull Johns Hopkins Hosp. 1941;69: 79-85.
159. Samuel BU, Ponnuraj E, Rajasingh J, John TJ. Experimental poliomyelitis in bonnet monkey: clinical features, virology and pathology. In: Brown F, Lewis BP, eds. Poliovirus attenuation: molecular mechanisms and practical aspects. Dev Biol Stand. 1993;78:71-8.
160. Leon-Monzon ME, Illa I, Dalakas MC. Expression of poliovirus receptor in human spinal cord and muscle. Ann NY Acad Sci. 1995;753:48-57.
161. Ohka S, Yang WX, Terada E, Iwasaki K, Nomoto A. Retrograde transport of intact poliovirus through the axon via the fast transport system. Virol. 1998;250:67-75.
162. Ponnuraj EM, John TJ, Levin MJ, Simoes EA. Cell-to-cell spread of poliovirus in the spinal cord of bonnet monkeys. J Gen Virol. 1998;79:2393-403.
163. Chou SM, Norris FH. Amyotrophic lateral sclerosis: lower motor neuron disease spreading to upper motor neuron disease. Muscle & Nerve. 1993;16:864-9.
164. Sigurdsson B. Observations on three slow infections of sheep: maedi, paratuberculosis, rida, a slow encephalitis of sheep with general remarks on infections which develop slowly, and some of their special characteristics. Br Vet J. 1954;110:255-70.
165. O'Connell J, Albin R, Blum D, Grint P, Schwartz J. Development of antiviral agents for picornavirus infections. In: Rotbart HA, editor. Human Enteroviral Infections. Washington DC: American Society for Microbiology; 1995. Chapter 18.
166. Smith TJ, Kremer MJ, Luo M, Vriend G, Arnold E, Kamer G, et al. The site of attachment in human rhinovirus 14 for antiviral agents that inhibit uncoating. Science. 1986;233:1286-93.
167. Rossmann MG. The structure of antiviral agents that inhibit uncoating when complexed with viral capsids. Antiviral Res. 1989;11:3-14.
168. Zhang A, Nanni RG, Li T, Arnold GF, Oren DA, Jacobo-Molina A, et al. Structure determination of antiviral compound SCH 38057 complexed with human rhinovirus 14. J Mol Biol. 1993;230:857-67.
169. McKinley MA, Fever DC, Rosen MG. Treatment of the picornavirus common cold by inhibitors of viral uncoating and attachment. Annu Rev Microbiol. 1992;46:635-45.
170. Oliveira MA, Zhao R, Lee WM, Kremer MJ, Minor I, Rueckert RR, et al. The structure of human rhinovirus 16. Structure. 1993;1:51-68.
171. Lewis JK, Bothner B, Smith TJ, Siuzdak G. Antiviral agent blocks breathing of the common cold virus. Proc Natal Acad Sci. USA. 1998;95:6774-8.
172. Wang W, Lee WM, Mosser AG, Rueckert RR. WIN 52035-dependent human rhinovirus 16: assembly deficiency caused by mutations near the canyon surface. J Virol. 1998;72:1210-8.
173. Abdel-Rahman SM, Kearns GL. Single oral dose escalation pharmacokinetics of pleconaril (VP63843) capsules in adults. J of Clin Pharm. 1999;39:613-8.
174. Kearns GL, Abdel-Rahman SM, James LP, Blowey DL, Marshall JD, Wells TG, et al. Single-dose pharmacokinetics of a pleconaril (VP63843) oral solution in children and adolescents. Antimicrobial Anents and Chemotherapy. 1999;43:634-8.
175. Ansevin CF. Treatment of ALS with pleconaril. Neurology. 2001;56:691-2.
176. McKinlay MA. Recent advances in the treatment of rhinovirus infections. Current Opinion Pharmacol. 2001;1: 477-81.
177. Okada I, Matsumori A, Matoba Y, Tominaga M, Yamada T, Kawai C. Combination treatment with ribavirin and interferon for coxsackievirus B3 replication. J Lab Clin Med. 1992;120:569-73.
178. Waldmeier PC. Prospects for antiapoptotic drug thereapy of neurodegenerative diseases. Progress in Neuro-Psychopharmacology & Biological Psychiatry. j2003;27: 303-21.
179. Jacobson MD. Anti-apoptosis therapy: a way of treating neural degeneration? Curr Biol. 1998;8:R418-21.
180. Tatton WG, Chalmers-Redman RM, Ju WY, Wadia J, Tatton NA. Apoptosis in neural degenerative disorders: potential for therapy by modifying gene transcription. J Neural Transm. 1997;49(Suppl): 245-68.
181. Schulz JB, Weller M, Moskowitz MA. Caspases as treatment targets in stroke and neurodegenerative diseases. Ann Neurol. 1999;45:421-9.
182. Nicholson DW. From bench to clinic with apoptosis-based therapeutic agents. Nature. 2000;407:810-6.
183. Vandepapelièr P. Thereapeutic vaccination against chronic viral infections. Lancet Infectious Diseases. 2002;2:353-67.
184. Rotbart HA. Nucleic acid detection systems for enteroviruses. Clin Microbiol Rev. 1991;4:156-68.
185. Romero JR, Rotbart HA. PCR-based strategies for the detection of human enteroviruses. In: Ehrlich GD, Greenberg SJ, editors. PCR-Based Diagnostics in Infectious Disease. Cambridge, MA: Blackwell Scientific Publications; 1994. p 341.
186. Romero JR. Reverse transcription-polymerase chain reaction detection of the enteroviruses: overview and clinical utility in pediatric enteroviral infections. Archives of Pathology and Laboratory Medicine. 1999;123:1161-9.
187. Olive DM, Al-Mufti S, Al-Mulla W, Khan MA, Pasca A, Stanway G, Al-Nakib W. Detection and differentiation of picornaviruses in clinical samples following genomic amplification. J Gen Virol. 1990;71:2141-7.
188. Gruber AD, Moennig V, Hewicker-Trautwein M, Trautwein G. Effect of formalin fixation and long-term storage on the detectability of bovine viral-diarrhoea-virus (BVDV) RNA in archival brain tissue using polymerase chain reaction. J Vet Med. 1994;41:654-61.
189. Karlsen F, Kalantari M, Chitemerere M, Johansson B, Hagmar B. Modifications of human and viral deoxyribonucleic acid by formaldehyde fixation. Lab Investigation. 1994;71:604-11.
190. Jubelt B, Lipton HL. ALS: persistent scientists do not find persisting enteroviruses (editorial). Neurology. 2004;62: 1250-1.
191. Redline RW, Genest DR, Tycko B. Detection of enteroviral infection in paraffin-embedded tissue by the RNA polymerase chain reaction technique. Am J Clin Pathol. 1991;96:568-571.
192. Rupp GM, Locker J. Purification and analysis of RNA from paraffin-embedded tissues. BioTechniques. 1988;6:56-60.
193. Ben-Ezra J, Johnson DA, Rossi J, Cook N, Wu A. Effect of fixation on the amplification of nucleic acids from paraffin-embedded material by the polymerase chain reaction. J Histochem Cytochem. 1991;39:351-4.
194. Foss RD, Guha-Thakurta N, Conran RM, Gutman P. Effects of fixative and fixation time on the extraction and polymerase chain
195. Dakhama A, Macek V, Hogg JC, Hegele RG. Amplification of human β-actin gene by the reverse transciptase-polymerase chain reaction: implications for assessment of RNA from formalin-fixed, paraffin-embedded material. J Histochem Cytochem. 1996;44:1205-7.
196. Coombs NJ, Gough AC, Primrose JN. Optimization of DNA and RNA extraction from archival formalin-fixed tissue. Nucleic Acids Research. 1999;27: 1-3.
197. Masuda N, Ohnishi T, Kawamoto S, Monden M, Okubo K. Analysis of chemical modification of RNA from formalin-fixed samples and optimization of molecular biology applications for such samples. Nucleic Acids Research. 1999;27:4436-43.
198. Beaulieux F, Berger MM, Tcheng R, Giraud P, Lina B. RNA extaction and RT-PCR procedures adapted for the detection of enterovirus sequences from fozen and paraffin-embedded formalin-fixed spinal cord samples. J Virol Methods. 2003;107:115-20.
199. Wolk D, Mitchell S, Patel R. Principles of molecular microbiology testing methods. Infectious Disease Clinics of North America. 2001;15:1157-1204.
200. Reiss RA, Rutz B. Quality control PCR: a method for detecting inhibitors of Taq DNA polymerase. BioTechniques. 1999;27:920-6.
201. Konet DS, Mezencio JMS, Babcock G, et al. Inhibitors of RT-PCR in serum. J Virol Methods. 2000;84:95-8.
202. Simone NL, Bonner RF, Gillespie JW, Emmert-Buck MR, Liotta LA. Laser-capture microdissection: opening the microscopic frontier to molecular analysis. Trends Genet. 1998;14:272-6.
203. Eltoum IA, Siegal GP, Frost AR. Microdissection of histologic sections: past, present, and future. Adv Anat Path. 2002;9:316-22.