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Contribution of LCMV Towards Deciphering Biology of Quasispecies In Vivo

  • N. Sevilla
  • E. Domingo
  • J. C. de la Torre
Chapter
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 263)

Abstract

Arenaviruses have often been viewed as relatively stable genetically with amino acid sequence homologies of 90%–95% among different strains of lymphocytic choriomeningitis virus (LCMV) and of 44%–63% for homologous proteins of different arenaviruses: LCMV, Pichinde, Junin, Machupo and Lassa (Southern and Bishop 1987; Southern and Oldstone 1988). Yet considerable variation in biological properties among LCMV strains soon became apparent (reviewed in Dutko and Oldstone 1983; Southern and Oldstone 1988). Hotchin already recognized the importance of passage history in determining the biological properties of LCMV (Hotchin 1962). He showed that early mouse brain passages of LCMV-induced immunologic tolerance in newborn mice and mortality was low. In contrast, late mouse brain passages of LCMV lost the tolerance-inducing capacity, and mortality was high. Neonatal infection of certain mouse strains with LCMV strains Armstrong (ARM) and E-350-induced growth hormone deficiency and severe hypoglycemia, which frequently resulted in the death of the infected mice, while strains WE and Traub did not cause this syndrome. This difference was associated with the ability of LCMV ARM and E-350, but not WE and Traub, to replicate at high levels in the GH-producing cells in the anterior pituitary (Oldstone et al. 1985). Other biological differences among LCMV strains include the capacity of the virus to invade ß-cells in the islets of Langerhans, to cause alterations in glucose tolerance, or differences in the formation of immune complexes and lethality for adult guinea pigs (Southern and Oldstone 1988), as well as to induce generalized immunosuppression in adult mice. Selection of LCMV variants with distinguishable phenotypes occurs in different organs of infected mice persistently infected since birth with ARM tend to produce acute infection in adult mice, whereas isolates from the spleen of the same mice tend to persist (Ahmed and Oldstone 1988).

Keywords

Human Immunodeficiency Virus Type Peripheral Blood Lymphocyte Viral Persistence Single Amino Acid Change Lassa Fever 
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.

References

  1. Aebischer T, Moskophidis D, Rohrer UH, Zinkernagel RM, Hengartner H (1991) In vitro selection of lymphocytic choriomeningitis virus escape mutants by cytotoxic T lymphocytes. Proc Natl Acad Sci USA 88:11047–11051PubMedCrossRefGoogle Scholar
  2. Ahmed R, Hahn CS, Somasundaram T, Villarete L, Matloubian M, Strauss JH (1991) Molecular basis of organ-specific selection of viral variants during chronic infection. J Virol 65:4242–4247PubMedGoogle Scholar
  3. Ahmed R, Oldstone MB (1988) Organ-specific selection of viral variants during chronic infection [published erratum appears in J Exp Med 1988 Jul 1;168(1):457]. J Exp Med 167:1719–1724PubMedCrossRefGoogle Scholar
  4. Ahmed R, Salmi A, Butler LD, Chiller JM, Oldstone MB (1984) Selection of genetic variants of lymphocytic choriomeningitis virus in spleens of persistently infected mice. Role in suppression of cytotoxic T lymphocyte response and viral persistence. J Exp Med 160:521–540PubMedCrossRefGoogle Scholar
  5. Auperin DD, Romanowski V, Galinski M, Bishop DHL (1984) Sequencing studies of Pichinde arenavirus S RNA indicate a novel coding strategy, an ambisense viral S RNA. J Virol 52:897–904PubMedGoogle Scholar
  6. Baranowski E, Ruiz-Jarabo CM, Sevilla N, Andreu D, Beck E, Domingo E (2000) Cell recognition by foot-and-mouth disease virus that lacks the RGD integrin-binding motif: flexibility in aphthovirus receptor usage. J Virol 74:1641–1647PubMedCrossRefGoogle Scholar
  7. Batschelet E, Domingo E, Weissmann C (1976) The proportion of revertant and mutant phage in a growing population, as a function of mutation and growth rate. Gene 1:27–32PubMedCrossRefGoogle Scholar
  8. Borrow P, Evans C, Oldstone MBA (1995) Virus-induced immune suppression: immune system-mediated destruction of virus-infected dendritic cells results in generalized immune suppression. J Virol 69: 1059–1070PubMedGoogle Scholar
  9. Borrow P, Lewicki H, Wei X, Horwitz MS, Peffer N, Meyers H, Nelson JA, Gairin JE, Hahn BH, Oldstone MB, Shaw GM (1997) Antiviral pressure exerted by HTV-1-specific cytotoxic T lymphocytes (CTLs) during primary infection demonstrated by rapid selection of CTL-escape virus [see comments]. Nat Med 3: 205–211PubMedCrossRefGoogle Scholar
  10. Borrow P, Oldstone MB (1992) Characterization of lymphocytic choriomeningitis virus-binding protein(s): a candidate cellular receptor for the virus. J Virol 66:7270–7281PubMedGoogle Scholar
  11. Borrow P, Oldstone MBA (1997) Lymphocytic Choriomeningitis Virus. In: Nathanson N, et al. (eds) Viral Pathogenesis. Lippincott-Raven, PhiladelphiaGoogle Scholar
  12. Borrow P, Shaw GM (1998) Cytotoxic T-lymphocyte escape viral variants: how important are they in viral evasion of immune clearance in vivo? Immunol Rev 164:37–51PubMedCrossRefGoogle Scholar
  13. Buchmeier MJ, Southern PJ, Parekh BS, Wooddell MK, Oldstone MBA (1987) Site-specific antibodies define a cleavage site conserved among arenavirus GP-C glycoproteins. J Virol 61:982–985PubMedGoogle Scholar
  14. Buchmeier MJ, Welsh RM, Dutko FJ, Oldstone MBA (1980) The virology and immunobiology of lymphocytic choriomeningitis virus infection. Adv Immunol 30:275–331PubMedCrossRefGoogle Scholar
  15. Buesa-Gomez J, Teng MN, Oldstone CE, Oldstone MB, de la Torre JC (1996) Variants able to cause growth hormone deficiency syndrome are present within the disease-nil WE strain of lymphocytic choriomeningitis virus. J Virol 70:8988–8992PubMedGoogle Scholar
  16. Burns JW, Buchmeier MJ (1993) Glycoproteins of the arenaviruses. In: Salvato MS (ed) The arenaviridae. Plenum Press, New YorkGoogle Scholar
  17. Cao W, Henry MD, Borrow P, Yamada H, Eider JH, Ravkov EV, Niehol ST, Compans RW, Campbell KP, Oldstone MBA (1998) Identification of alpha-dystroglycan as a receptor for lymphocytic choriomeningitis virus and Lassa fever virus. Science 282:2079–2081PubMedCrossRefGoogle Scholar
  18. Carrillo C, Borea M, Moore DM, Morgan DO, Sobrino F (1998) In vivo analysis of the stability and fitness of variants recovered from foot-and-mouth disease virus quasispecies. J Gen Virol 79: 1699–1706PubMedGoogle Scholar
  19. Ciurea A, Klenerman P, Hunziker L, Horvath E, Senn BM, Ochsenbein AF, Hengartner H, Zinkernagel RM (2000) Viral persistence in vivo through selection of neutralizing antibody-escape variants. Proc Natl Acad Sci USA 97:2749–2754PubMedCrossRefGoogle Scholar
  20. de la Torre JC, Holland JJ (1990) RNA virus quasispecies populations can suppress vastly superior mutant progeny. J Virol 90:6278–6281Google Scholar
  21. de la Torre JC, Oldstone MB (1992) Selective disruption of growth hormone transcription machinery by viral infection. Proc Natl Acad Sci USA 92:9939–9943CrossRefGoogle Scholar
  22. de la Torre JC, Oldstone MBA (1996) The anatomy of viral persistence: Mechanisms of persistence and associated disease. Adv Virus Res 46:311–343PubMedCrossRefGoogle Scholar
  23. Dockter J, Evans CF, Tishon A, Oldstone MB (1996) Competitive selection in vivo by a cell for one variant over another: implications for RNA virus quasispecies in vivo. J Virol 70: 1799–1803PubMedGoogle Scholar
  24. Domingo E (1999) Quasispecies. In: Granoff A, Webster RG. (eds) Encyclopedia of Virology. Academic Press, LondonGoogle Scholar
  25. Domingo E, Holland JJ, Eigen M (2000) Quasispecies and RNA virus evolution: Principles and Consequences. Landes Bioscience, AustinGoogle Scholar
  26. Domingo E, Holland JJ (1997) RNA virus mutations and fitness for survival. Annu Rev Microbiol 51:151–178PubMedCrossRefGoogle Scholar
  27. Drake JW, Holland JJ (1999) Mutation rates among RNA viruses. Proc Natl Acad Sci USA 96: 13910–13913PubMedCrossRefGoogle Scholar
  28. Dutko FJ, Oldstone MBA (1983) Genomic and biological variation among commonly used lymphocytic choriomeningitis virus strains. J Gen Virol 64: 1689–1698PubMedCrossRefGoogle Scholar
  29. Eigen M (1971) Selforganization of matter and the evolution of biological macromolecules. Naturwissenschaften 58:465–523PubMedCrossRefGoogle Scholar
  30. Eigen M (1996) On the nature of virus quasispecies [letter; comment]. Trends Microbiol 4:216–218PubMedCrossRefGoogle Scholar
  31. Eigen M, Biebricher CK, (1988) Sequence space and quasispecies distribution. In: Domingo E, Ahlquist P, Holland JJ. (eds) RNA Geneties. CRC Press, Boca RatonGoogle Scholar
  32. Evans CF, Borrow P, de la Torre JC, Oldstone MB (1994) Virus-induced immunosuppression: kinetic analysis of the selection of a mutation associated with viral persistence. J Virol 94:7367–7373Google Scholar
  33. Evans DT, O’Connor DH, Jing P, Dzuris JL, Sidney J, da Silva J, Allen TM, Horton H, Venham JE, Rudersdorf RA, Vogel T, Pauza CD, Bontrop RE, DeMars R, Sette A, Hughes AL, Watkins DI (1999) Virus-specific cytotoxic T-lymphocyte responses select for amino-acid variation in simian immunodeficiency virus Env and Nef. Nat Med 5: 1270–1276PubMedCrossRefGoogle Scholar
  34. Farci P, Shimoda A, Coiana A, Diaz G, Peddis G, Melpolder JC, Strazzera A, Chien DY, Munoz SJ, Balestrieri A, Purcell RH, Alter HF (2000) The outcome of acute hepatitis C predicted by the evolution of the viral quasispecies. Science 288:339–344PubMedCrossRefGoogle Scholar
  35. Flint SJ, Enquist LW, Krug RM, Racaniello VR, Skalka AM (2000) Molecular biology, pathogenesis and control. In: Virology. ASM Press, Washington DCGoogle Scholar
  36. Forns X, Purcell RH, Bukh J (1999) Quasispecies in viral persistence and pathogenesis of hepatitis C virus. Trends Microbiol 7:402–410PubMedCrossRefGoogle Scholar
  37. Franze-Fernandez M-T, Zetina C, Iapalucci S, Lucero MA, Bouissou C, Lopez R, Rey O, Deheli M, Cohen GN, Zakin MM (1987) Molecular structure and early events in the replication of Tacaribe arenavirus S RNA. Virus Res 7:309–324PubMedCrossRefGoogle Scholar
  38. Friedberg EC, Walker GC, Siede W (1995) DNA repair and mutagenesis. In: American Society for Microbiology. Washington DCGoogle Scholar
  39. Garcin D, Rochat S, Kolakofsky D (1993) The Tacaribe arenavirus small zinc finger protein is required for both mRNA synthesis and genome replication. J Virol 67:807–812PubMedGoogle Scholar
  40. Goulder P, Price D, Nowak M, Rowland-Jones S, Phillips R, McMichael A (1997) Co-evolution of human immunodeficiency virus and cytotoxic T-lymphocyte responses. Immunol Rev 159:17–29PubMedCrossRefGoogle Scholar
  41. Gromeier M, Wimmer E, Gorbalenya AE (1999) Genetics, pathogenesis and evolution of picornaviruses. In: Domingo E, Webster RG. (eds) Origin and Evolution of Viruses. Academic Press, San DiegoGoogle Scholar
  42. Hansen JL, Long AM, Schultz SC (1997) Structure of the RNA-dependent RNA polymerase of poliovirus. Structure 5:1109–1122PubMedCrossRefGoogle Scholar
  43. Havlir DV, Eastman S, Gamst A, Richman DD (1996) Nevirapine-resistant human immunodeficiency virus: kinetics of replication and estimated prevalence in untreated patients. J Virol 70:7894–7899PubMedGoogle Scholar
  44. Holland JJ, de la Torre JC, Steinhauer DA (1992) RNA virus populations as quasispecies. [Review]. Curr Top Microbiol Immunol 176: 1–20PubMedCrossRefGoogle Scholar
  45. Hotchin J (1962) The biology of lymphocytic choriomeningitis infection: virus-induced immune disease. Cold Spring Harbor Symp Quant Biol 176: 1–20Google Scholar
  46. Iapalucci S, Lopez N, Rey O, Zakin MM, Cohen GN, Franze-Fernandez M-T (1989a) The 5’ region of Tacaribe virus L RNA encodes a protein with a potential metal binding domain. Virology 173: 357–361PubMedCrossRefGoogle Scholar
  47. Iapalucci S, Lopez R, Rey O, Lopez N, Franze-Fernandez M-T (1989b) Tacaribe virus L gene encodes a protein of 2210 amino acid residues. Virology 170:40–47PubMedCrossRefGoogle Scholar
  48. Karlsson AC, Gaines H, Sallberg M, Lindback S, Sonnerborg A (1999) Reappearance of founder virus sequence in human immunodeficiency virus type 1-infected patients. J Virol 73:6191–6196PubMedGoogle Scholar
  49. Kimata JT, Kuller L, Anderson DB, Dailey P, Overbaugh J (1999) Emerging cytopathic and antigenic simian immunodeficiency virus variants influence AIDS progression [see comments]. Nat Med 5: 535–541PubMedCrossRefGoogle Scholar
  50. King CC, Jamieson BD, Reddy K, Bali N, Concepcion RJ, Ahmed R (1992) Viral infection of the thymus. J Virol 66:3155–3160PubMedGoogle Scholar
  51. Klavinskis LS, Oldstone MBA (1989) Lymphocytic choriomeningitis virus selectively alters differentiated but not housekeeping functions: block in expression of growth hormone gene is at the level of transcription initiation. Virology 168:232–235PubMedCrossRefGoogle Scholar
  52. Lai MM (1992) Genetic recombination in RNA viruses. Curr Top Microbiol Immunol 176:21–32PubMedCrossRefGoogle Scholar
  53. Lech WJ, Wang G, Yang YL, Chee Y, Dorman K, McCrae D, Lazzeroni LC, Erickson JW, Sinsheimer JS, Kaplan AH (1996) In vivo sequence diversity of the protease of human immunodeficiency virus type 1: presence of protease inhibitor-resistant variants in untreated subjects. J Virol 70:2038–2043PubMedGoogle Scholar
  54. Lehmann-Grube F (1984) Portraits of viruses: arenaviruses. Inter-virology 22: 121–145Google Scholar
  55. Lewicki H, Tishon A, Borrow P, Evans C, Gairin JE, Hahn KM, Jewell DA, Wilson IA, Oldstone MBA (1995) CTL escape viral variants. I. Generation and molecular characterization. Virology 210:29–40PubMedCrossRefGoogle Scholar
  56. Martell M, Esteban JI, Quer J, Genesca J, Weiner A, Esteban R, Guardia J, Gomez J (1992) Hepatitis C virus (HCV) circulates as a population of different but closely related genomes: quasispecies nature of HCV genome distribution. J Virol 66:3225–3229PubMedGoogle Scholar
  57. Matloubian M, Kolhekar SR, Somasundaram T, Ahmed R (1993) Molecular determinants of macrophage tropism and viral persistence: importance of single amino acid changes in the polymerase and glycoprotein of lymphocytic choriomeningitis virus. J Virol 67:7340–7349PubMedGoogle Scholar
  58. Matloubian M, Somasundaram T, Kolhekar SR, Selvakumar R, Ahmed R (1990) Genetic basis of viral persistence: single amino acid change in the viral glycoprotein affects ability of lymphocytic choriomeningitis virus to persist in adult mice. J Exp Med 172:1043–1048PubMedCrossRefGoogle Scholar
  59. McMichael AI, Phillips RE, (1997) Escape of human immunodeficiency virus from immune control. Annu Rev Immunol 15:271–296PubMedCrossRefGoogle Scholar
  60. Meyer PR, Matsuura SE, Mian AM, So AG, Scott WA (1999) A mechanism of AZT resistance: an increase in nucleotide-dependent primer unblocking by mutant HIV-1 reverse transcriptase. Mol Cell 4:35–43PubMedCrossRefGoogle Scholar
  61. Meyer PR, Matsuura SE, So AG, Scott WA (1998) Unblocking of chain-terminated primer by HIV-1 reverse transcriptase through a nucleotide-dependent mechanism. Proc Natl Acad Sci USA 95: 13471–13476PubMedCrossRefGoogle Scholar
  62. Meyerhans A, Cheynier R, Albert J, Seth M, Kwok S, Sninsky J, Morfeldt-Manson L, Asjo B, Wain-Hobson S (1989) Temporal fluctuations in HIV quasispecies in vivo are not reflected by sequential HIV isolations. Cell 58:901–910PubMedCrossRefGoogle Scholar
  63. Meyerhans A, Vartanian JP (1999) The fidelity of cellular and viral polymerases and its manipulation for hypermutagenesis. In: Domingo E, Webster RG. Holland JJ. (eds) Origin and Evolution of Viruses. Academic Press, San DiegoGoogle Scholar
  64. Nagy PD, Simon AE (1987) New insights into the mechanisms of RNA recombination. Virology 235: 1–9CrossRefGoogle Scholar
  65. Najera I, Holguin A, Quinones-Mateu ME, Munoz-Fernandez MA, Najera R, Lopez-Galindez C, Domingo E (1995) Pol gene quasispecies of human immunodeficiency virus: mutations associated with drug resistance in virus from patients undergoing no drug therapy. J Virol 69:23–31PubMedGoogle Scholar
  66. Novella IS, Elena SF, Moya A, Domingo E, Holland JJ (1995) Size of genetic bottlenecks leading to virus fitness loss is determined by mean initial population fitness. J Virol 69:2869–2872PubMedGoogle Scholar
  67. Odermatt B, Eppler M, Leist TP, Hengartner H, Zinkernagel RM (1991) Virus-triggered acquired immunodeficiency by cytotoxic T-cell-dependent destruction of antigen-presenting cells and lymph follicle structure. Proc Natl Acad Sci USA 88:8252–8256PubMedCrossRefGoogle Scholar
  68. Oldstone MB, de la Torre JC, (1993) Viral diseases of the next century. [Review]. Transactions of the American Clinical & Climatological Association 93:62–68Google Scholar
  69. Oldstone MBA (1984) Virus can alter cell function without causing cell pathology: disordered function leads to imbalance of homeostasis and disease. In: Notkins AL., Oldstone MBA. (eds) Concepts in viral pathogenesis. Springer, Heidelberg Berlin New YorkGoogle Scholar
  70. Oldstone MBA (1989) Viral persistence. Cell 56:517–520PubMedCrossRefGoogle Scholar
  71. Oldstone MBA (1991) Molecular anatomy of viral persistence. J Virol 65:6381–6386PubMedGoogle Scholar
  72. Oldstone MBA (1998) Viral persistence: mechanisms and consequences. Curr Opin Microbiol 1:436–441PubMedCrossRefGoogle Scholar
  73. Oldstone MBA, Ahmed R, Buchmeier MJ., Blout P, Tishon A (1985) Perturbation of differentiated functions during viral infection in vivo. Virology 142:158–174PubMedCrossRefGoogle Scholar
  74. Oldstone MBA, Rodriguez M, Daughaday WH, Lampert PW (1984) Viral perturbation of endocrine function: disordered cell function leads to disturbed homeostasis and disease. Nature 307:278–281PubMedCrossRefGoogle Scholar
  75. Oldstone MBA, Sinha YN, Blout P, Tishon A, Rodriguez M, von Wedel R, Lampert PW (1982) Virus-induced alterations in homeostasis: alterations in differentiated functions of infected cells in vivo. Science 218:1125–1127PubMedCrossRefGoogle Scholar
  76. Parekh BS, Buchmeier MJ (1986) Proteins of lymphocytic choriomeningitis virus: antigenic topography of the viral glycoproteins. Virology 153: 168–178PubMedCrossRefGoogle Scholar
  77. Pawlotsky JM., Germanidis G, Neumann AU, Pellerin M, Frainais PO, Dhumeaux D (1998) Interferon resistance of hepatitis C virus genotype 1b: relationship to non-structural 5 A gene quasispecies mutations. J Virol 72:2795p–2805Google Scholar
  78. Pircher R, Burki K, Lang R, Hengartner H, Zinkernagel RM (1989) Tolerance induction in double specific T-cell receptor transgenic mice varies with antigen. Nature 342:559–561PubMedCrossRefGoogle Scholar
  79. Pircher H, Moskophidis D, Rohrer U, Burki K, Hengartner R, Zinkernagel RM 1990) Viral escape by selection of cytotoxic T cell-resistant virus variants in vivo. Nature 346:629–633PubMedCrossRefGoogle Scholar
  80. Planz O, Ehl S, Furrer E, Horvath E, Brundler MA, Hengartner H, Zinkernagel RM (1997) A critical role for neutralizing-antibody-producing B cells, CD4(+) T cells, and interferons in persistent and acute infections of mice with lymphocytic choriomeningitis virus: implications for adoptive immunotherapy of virus carriers. Proc Natl Acad Sci USA 94:6874–6879PubMedCrossRefGoogle Scholar
  81. Quinones-Mateu ME, Albright JL, Mas A, Soriano V, Arts EJ (1998) Analysis of pol gene heterogeneity, viral quasispecies, and drug resistance in individuals infected with group O strains of human immunodeficiency virus type 1. J Virol 72:9002–9015PubMedGoogle Scholar
  82. Ribeiro RM, Bonhoeffer S, Nowak MA (1998) The frequency of resistant mutant virus before antiviral therapy. Aids 12:461–465PubMedCrossRefGoogle Scholar
  83. Riviere Y, Ahmed R, Southern P, Oldstone MBA (1985) Perturbation of differentiated functions during viral infection in vivo. II. Viral reassortants map growth hormone defect to the S RNA of the lymphocytic choriomeningitis virus genome. Virology 142:175–182PubMedCrossRefGoogle Scholar
  84. Riviere Y, Oldstone MB (1986) Genetic reassortants of lymphocytic choriomeningitis virus: unexpected disease and mechanism of pathogenesis. J Virol 59:363–368PubMedGoogle Scholar
  85. Sala M, Wain-Hobson S (1999) Drift and conservation in RNA virus evolution: are they adapting or merely changing? In: Domingo E, Webster RG., Holland JJ. (eds) Origin and Evolution of Viruses. Academic Press, San DiegoGoogle Scholar
  86. Sala M, Zamhruno G, Vartanian JP, Marconi A, Bertazzoni U, Wain-Hohson S (1994) Spatial dis-continuities in human immunodeficiency virus type 1 quasispecies derived from epidermal Langerhans cells of a patient with AIDS and evidence for double infection. J Virol 68:5280,5283PubMedGoogle Scholar
  87. Salvato M, Borrow P, Shimomaye E, Oldstone MB (1991) Molecular basis of viral persistence: a single amino acid change in the glycoprotein of lymphocytic choriomeningitis virus is associated with suppression of the antiviral cytotoxic T-lymphocyte response and establishment of persistence. J Virol 65: 1863–1869PubMedGoogle Scholar
  88. Salvato M, Shimomaye EM, Oldstone MBA (1989) The primary structure of the lymphocytic choriomeningitis virus L gene encodes a putative RNA polymerase. Virology 169:377–384PubMedCrossRefGoogle Scholar
  89. Salvato M, Shimomaye EM, Southern P, Oldstone MBA (1988) Virus-lymphocyte interactions: IV. Molecular characterization of LCMV Armstrong (CTL+) small genomic segment and that of its variant, clone 13 (CTL-). Virology 164:517–522PubMedCrossRefGoogle Scholar
  90. Salvato MS (1993) Molecular biology of the prototype arenavirus, lymphocytic choriomeningitis virus. In: Salvato MS. (ed) The Arenaviridae. Plenum, New YorkCrossRefGoogle Scholar
  91. Salvato MS, Schweighofer KJ, Burns J, Shimomaye EM (1992) Biochemical and immunological evidence that the 11-kDa zinc-binding protein of lymphocytic choriomeningitis virus is a structural component of the virus. Virus Res 22: 185–198PubMedCrossRefGoogle Scholar
  92. Salvato MS, Shimomaye EM (1989) The completed sequence of lymphocytic choriomeningitis virus reveals a unique RNA structure and a gene for a zinc finger protein. Virology 173: 1–10PubMedCrossRefGoogle Scholar
  93. Sevilla N, Kunz S, Holz A, Lewicki H, Homann D, Yamada H, Campbell KP, de La Torre JC, Oldstone MB (2000) Immunosuppression and resultant viral persistence by specific viral targeting of dendritic cells. J Exp Med 192:1249–1260PubMedCrossRefGoogle Scholar
  94. Singh MK, Fuller-Pace FV, Buchmeier MJ, Southern PJ (1987) Analysis of genomic L RNA segment of lymphocytic choriomeningitis virus. Virology 161:448–456PubMedCrossRefGoogle Scholar
  95. Sousa R (1996) Structural and mechanistic relationships between nucleic acid polymerases. Trends Biochem Sci 21: 186–190PubMedGoogle Scholar
  96. Southern PJ, Bishop DH (1987) Sequence comparison among arena viruses. Curr Top Microbiol Immunol 133:19–39PubMedCrossRefGoogle Scholar
  97. Southern PJ, Singh MK, Riviere Y, Jacoby DR, Buchmeier MJ, Oldstone MBA (1987) Molecular characterization of the genomic S RNA segment from lymphocytic choriomeningitis virus. Virology 157:145–155PubMedCrossRefGoogle Scholar
  98. Steinhauer DA, Domingo E, Holland JJ (1992) Lack of evidence for proofreading mechanisms associated with an RNA virus polymerase. Gene 122:281–288PubMedCrossRefGoogle Scholar
  99. Teng MN, Borrow P, Oldstone MBA, de la Torre JC (1996a) A single amino acid change in the glycoprotein of lymphocytic choriomeningitis virus is associated with the ability to cause growth hormone deficiency syndrome. J Virol 70:8438–8443PubMedGoogle Scholar
  100. Teng MN, Oldstone MB, de la Torre JC (1996b) Suppression of lymphocytic choriomeningitis virus-induced growth hormone deficiency syndrome by disease-negative virus variants. Virology 223: 113–119PubMedCrossRefGoogle Scholar
  101. Tishon A, Borrow P, Evans C, Oldstone MB (1993) Virus-induced immunosuppression. 1. Age at infection relates to a selective or generalized defect. Virology 195:397–405PubMedCrossRefGoogle Scholar
  102. Tishon A, Oldstone MB (1990) Perturbation of differentiated functions during viral infection in vivo. In vivo relationship of host genes and lymphocytic choriomeningitis virus to growth hormone deficiency. Am J Pathol 137:965–969PubMedGoogle Scholar
  103. Valsamakis A, Riviere Y, Oldstone MBA (1987) Perturbation of differentiated functions in vivo during persistent viral infection. III. Decreased growth hormone mRNA. Virology 156:214–220PubMedCrossRefGoogle Scholar
  104. Wright KE, Spiro RC, Burns JW, Buchmeier MJ (1990) Post-translational processing of the glycoproteins of lymphocytic choriomeningitis virus. Virology 177: 175–183PubMedCrossRefGoogle Scholar
  105. Zinkernagel RM, Doherty PC (1979) MHC-restricted cytotoxic T cells: studies on the biological role of polymorphic major transplantation antigens determining T-cell restriction specificity, function, and responsiveness. Adv Immunol 27:51–177PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2002

Authors and Affiliations

  • N. Sevilla
    • 1
  • E. Domingo
    • 2
  • J. C. de la Torre
    • 1
  1. 1.Department of NeuropharmacologyThe Scripps Research InstituteLa JollaUSA
  2. 2.Centro de Biologia Molecular Severo OchoaUniversidad Autonoma de MadridCantoblanco, MadridSpain

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