Advertisement

Replication of Hantaviruses

  • C. B. Jonsson
  • C. S. Schmaljohn
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 256)

Abstract

Hantaviruses have a genome consisting of three segments of negative-sense, single-strand RNA (reviewed in Schmaljohn 1996a). The large (L), medium (M), and small (S) genomic segments, or vRNAs, code for the viral RNA-dependent RNA polymerase (RdRp), envelope glycoproteins (Gl and G2), and nucleoprotein (N), respectively. Nonstructural proteins have not been described for hantaviruses. One of the first molecular features found to distinguish hantaviruses from other viruses in the family Bunyaviridae is the sequence of their conserved, complementary terminal nucleotides on the L, M, and S segments (Schmaljohn and Dalrymple 1983). This characteristic, and the absence of serological cross-reactivity among other members of the family, were the bases for the proposal to establish the Hantavirus genus in the family Bunyaviridae in 1986.

Keywords

Hemorrhagic Fever With Renal Syndrome Rift Valley Fever Virus Terminal Nucleotide Hantavirus Infection Reverse Genetic System 
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.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Arikawa J, Ito M, Yao JS, Kariwa H, Takashima I, Hashimoto N (1994) Epizootiological studies of hantavirus infection among urban rats in Hokkaido, Japan: evidences for the persistent infection from the sero-epizootiological surveys and antigenic characterizations of hantavirus isolates. J Vet Med Sci 56:27–32PubMedCrossRefGoogle Scholar
  2. Betenbaugh M, Yu M, Kuehl K, White J, Pennock D, Spik K, Schmaljohn C (1995) Nucleocapsid- and virus-like particles assemble in cells infected with recombinant baculoviruses or vaccinia viruses expressing the M and the S segments of Hantaan virus. Virus Res 38:111–124PubMedCrossRefGoogle Scholar
  3. Bogdanova S, Gavrilovskaya I, Boyko V, Prokhorova N, Linev M, Apekina N, Gorbachkova Y, Rymalov N, Bernshteyn A, Chumakov M (1987) Persistent infection caused by hemorrhagic fever with renal syndrome virus in bank voles (Clethrionomys glareolus) — the natural host of the virus. Mikrobiologicheskiy Zhurnal 49:99–106Google Scholar
  4. Bouloy M, Pardigon N, Vialat P, Gerbaud S, Girard M (1990) Characterization of the 5′ and 3′ ends of viral messenger RNAs Isolated from BHK21 cells infected with Germiston virus (Bunyavirus). Virology 175:50–58PubMedCrossRefGoogle Scholar
  5. Bouloy M, Vialat M, Girard M, Pardigon N (1984) A transcript from the S segment of the Germiston bunyavirus is uncapped and codes for the nucleoprotein and a nonstructural protein. J Virol 49: 717–723PubMedGoogle Scholar
  6. Bridgen A, Elliott RM (1996) Rescue of a segmented negative-strand RNA virus entirely from cloned complementary DNAs. Proc Natl Acad Sci USA 93:15400–15404PubMedCrossRefGoogle Scholar
  7. Collett MS (1986) Messenger RNA of the M segment RNA of Rift Valley fever virus. Virology 151: 151–156PubMedCrossRefGoogle Scholar
  8. Dohmae K, Nishimune Y (1995) Protection against hantavirus infection by dam’s immunity transferred vertically to neonates. Arch Virol 140:165–172PubMedCrossRefGoogle Scholar
  9. Dohmae K, Okabe M, Nishimune Y (1994) Experimental transmission of hantavirus infection in laboratory rats. J Infect Dis 170:1589–1592PubMedCrossRefGoogle Scholar
  10. Domingo E, Holland JJ (1994) Mutation rates and rapid evolution of viruses. In: Morse SS (ed) The Evolutionary Biology of Viruses. Raven Press, New YorkGoogle Scholar
  11. Draper DE (1995) Protein-RNA recognition. Annu Rev Biochem 64:593–620PubMedCrossRefGoogle Scholar
  12. Duijsings D, Kormelink R, Goldbach R (1999) Alfalfa mosaic virus RNAs serve as cap donors for tomato spotted wilt virus transcription during coinfection of Nicotiana benthamiana. J Virol 73: 5172–5175PubMedGoogle Scholar
  13. Dunn EF, Pritlove DC, Jin H, Elliott RM (1995) Transcription of a recombinant bunyavirus RNA template by transiently expressed bunyavirus proteins. Virology 211:133–143PubMedCrossRefGoogle Scholar
  14. Elliott R (1996) The Bunyaviridae: Concluding remarks and future prospects. In: Elliott RM (ed) The Bunyaviridae. Plenum Press, New YorkGoogle Scholar
  15. Elliott RM, Dunn E (1999) Analysis of bunyavirus promoter sequences. XI International Congress of Virology, Sydney, AustraliaGoogle Scholar
  16. Elton D, Metcalf L, Bishop K, Harrison D, Digard P (1999) Identification of amino acid residues of influenza virus nucleoprotein essential for RNA binding. J Virol 73:7357–7367PubMedGoogle Scholar
  17. Eshita Y, Bishop DH (1984) The complete sequence of the M RNA of snowshoe hare bunyavirus reveals the presence of internal hydrophobic domains in the viral glycoprotein. Virology 137:227–240PubMedCrossRefGoogle Scholar
  18. Eshita Y, Ericson B, Romanowski V, Bishop DH (1985) Analyses of the mRNA transcription processes of snowshoe hare bunyavirus S and M RNA species. J Virol 55:681–689PubMedGoogle Scholar
  19. Fodor E, Pritlove DC, Brownlee GG (1994) The influenza virus panhandle is involved in the initiation of transcription. J Virol 68:4092–4096PubMedGoogle Scholar
  20. Garcin D, Lezzi M, Dobbs M, Elliott RM, Schmaljohn C, Kang CY, Kolakofsky D (1995) The 5’ ends of Hantaan virus (Bunyaviridae) RNAs suggest a prime-and-realign mechanism for the initiation of RNA synthesis. J Virol 69:5754–5762PubMedGoogle Scholar
  21. Gott P, Stohwasser R, Schnitzler P, Darai G, Bautz EK (1993) RNA binding of recombinant nucleocapsid proteins of hantaviruses. Virology 194:332–337PubMedCrossRefGoogle Scholar
  22. Gupta KC, Kingsbury DW (1982) Conserved polyadenylation signals in two negative-strand RNA virus families. Virology 120:518–523PubMedCrossRefGoogle Scholar
  23. Hansen JL, Long AM, Schultz SC (1997) Structure of the RNA-dependent RNA polymerase of poliovirus. Structure 5:1109–1122PubMedCrossRefGoogle Scholar
  24. Henikoff S, Henikoff JG (1994) Protein family classification based on searching a database of blocks. Genomics 19:97–107PubMedCrossRefGoogle Scholar
  25. Hewlett MJ, Pettersson RF, Baltimore D (1977) Circular forms of Uukuniemi virion RNA: an electron microscopic study. J Virol 21:1085–1093PubMedGoogle Scholar
  26. Hofmann K, Bucher P, Falquet L, Bairoch A (1999) The PROSITE database, its status in 1999. Nucl Acids Res 27:215–219PubMedCrossRefGoogle Scholar
  27. Honda A, Ueda K, Nagata K, Ishihama A (1988) RNA polymerase of influenza virus: role of NP in RNA chain elongation. J Biochem 104:1021–1026PubMedGoogle Scholar
  28. Hughes SH, Stock AM (in press) Preparing recombinant proteins for X-ray crystallography. In: Rossmann MG, Arnold E (eds) International Tables for Macromolecular Crystallography, Volume F. Kluwer Academic Publisher, DordrechtGoogle Scholar
  29. Hutchinson KL, Peters CJ, Nichol ST (1996) Sin Nombre virus mRNA synthesis. Virology 224:139–149PubMedCrossRefGoogle Scholar
  30. Hutchinson KL, Rollin PE, Peters CJ (1998) Pathogenesis of a North American hantavirus, Black Creek Canal virus, in experimentally infected Sigmodon hispidus. Am J Trop Med Hyg 59:58–65PubMedGoogle Scholar
  31. Jin H, Elliott RM (1992) Mutagenesis of the L protein encoded by Bunyamwera virus and production of monospecific antibodies. J Gen Virol 73:2235–2244PubMedCrossRefGoogle Scholar
  32. Jin H, Elliott RM (1993a) Characterization of Bunyamwera virus S RNA that is transcribed and replicated by the L protein expressed from recombinant vaccinia virus. J Virol 67:1396–1404PubMedGoogle Scholar
  33. Jin H, Elliott RM (1993b) Non-viral sequences at the 5’ ends of Dugbe nairovirus S mRNAs. J Gen Virol 74:2293–2297PubMedCrossRefGoogle Scholar
  34. Kariwa H, Kimura M, Yoshizumi S, Arikawa J, Yoshimatsu K, Takashima I, Hashimoto N (1996) Modes of Seoul virus infections: persistency in newborn rats and transiency in adult rats. Arch Virol 141:2327–2338PubMedCrossRefGoogle Scholar
  35. Kim GR, McKee KT Jr (1985) Pathogenesis of Hantaan virus infection in suckling mice: clinical, virologic, and serologic observations. Am J Trop Med Hyg 34:388–395PubMedGoogle Scholar
  36. Kolakofsky D, Hacker D (1991) Bunyavirus RNA synthesis: genome transcription and replication. Curr Top Microbiol Immunol 169:143–159PubMedCrossRefGoogle Scholar
  37. Krug RM, Plotch SJ, Ulmanen I, Herz C, Bouloy M (1981) The mechanism of initiation of influenza viral RNA transcription by capped RNA primers. In: Bishop DHL, Compans RW (eds) The Replication of Negative Strand Viruses. Elsevier North Holland, New YorkGoogle Scholar
  38. Kukkonen SK, Vaheri A, Plyusnin A (1998) Completion of the Tula hantavirus genome sequence: properties of the L segment and heterogeneity found in the 3’ termini of S and L genome RNAs. J Gen Virol 79:2615–2622PubMedGoogle Scholar
  39. Lee H, Baek L, Johnson K (1982) Isolation of Hantaan virus, the etiologic agent of Korean hemorrhagic fever from wild urban rats. J Infect Dis 146:638–644PubMedCrossRefGoogle Scholar
  40. Lee H, Baek L, Joo Y, Ahn I, Park K (1985) Study of horizontal and vertical transmission of Hantaan and Seoul virus in Apodemus agrarius and in rats. J Korean Soc Virol 15:55–63Google Scholar
  41. Lee H, Lee P, Baek L, Song C, Seong I (1981) Intraspecific transmission of Hantaan virus, etiologic agent of Korean hemorrhagic fever, in the rodent Apodemus agrarius. Am Soc Trop Med Hyg 30:1106–1112Google Scholar
  42. Li M, Ramirez BC, Krug RM (1998) RNA-dependent activation of primer RNA production by influenza virus polymerase: different regions of the same protein subunit constitute the two required RNA-binding site. EMBO J 17:5844–5852PubMedCrossRefGoogle Scholar
  43. Lopez N, Muller R, Prehaud C, Bouloy M (1995) The L protein of Rift Valley fever virus can rescue viral ribonucleoproteins and transcribe synthetic genome-like RNA molecules. J Virol 69:3972–3979PubMedGoogle Scholar
  44. Luytes W, Krystal M, Enami M, Parvin J, Palese P (1989) Amplification, expression, and packaging of a foreign gene by influenza virus. Cell 59:1107–1113CrossRefGoogle Scholar
  45. Mathews DH, Sabina J, Zucker M, Turner DH (1999) Expanded sequence dependence of thermodynamic parameters provides robust prediction of RNA secondary structure. J Mol Biol 288:911–940PubMedCrossRefGoogle Scholar
  46. McKee K Jr, Kim G, Green D, Peters C (1985) Hantaan virus infection in suckling mice: virologic and pathologic correlates. J Med Virol 17:107–117PubMedCrossRefGoogle Scholar
  47. Meyer BJ, Schmaljohn C (2000a) Accumulation of terminally deleted RNAs may play a role in Seoul virus persistence. J Virol 74:1321–1331PubMedCrossRefGoogle Scholar
  48. Meyer BJ, Schmaljohn CS (2000b) Persistent hantavirus infections: characteristics and mechanisms. Trends Microbiol 8:61–67PubMedCrossRefGoogle Scholar
  49. Morita C, Morikawa S, Sugiyama K, Komatsu T, Ueno H, Kitamura T (1993) Inability of a strain of Seoul virus to transmit itself vertically in rats. Jpn J Med Sci Biol 46:215–219PubMedGoogle Scholar
  50. Muller R, Poch O, Delarue M, Bishop DH, Bouloy M (1994) Rift Valley fever virus L segment: correction of the sequence and possible functional role of newly identified regions conserved in RNA-dependent polymerases. J Gen Virol 75:1345–1352PubMedCrossRefGoogle Scholar
  51. O’Reilly EK, Kao CC (1998) Analysis of RNA-dependent RNA polymerase structure and function as guided by known polymerase structures and computer predictions of secondary structure. Virology 252:287–303CrossRefGoogle Scholar
  52. Patterson JL, Holloway B, Kolakofsky D (1984) La Crosse virions contain a primer-stimulated RNA polymerase and a methylated cap-dependent endonuclease. J Virol 52:215–222PubMedGoogle Scholar
  53. Pattnaik AK, Abraham G (1983) Identification of four complementary RNA species in Akabane virus-infected cells. J Virol 47:452–462PubMedGoogle Scholar
  54. Patton JT, Davis NL, Wertz GW (1984) Role of vesicular stomatitis virus proteins in RNA replication. In: Bishop D, Compans R (eds) Nonsegmented negative strand viruses. Paramyxoviruses and rhabdoviruses. Academic Press, OrlandoGoogle Scholar
  55. Pettersson RF, Kuismanen E, Rauonnholm R, Ulmanen I (1985) mRNAs of Uukuniemi virus, a bunyavirus. In: Becker Y (ed) Viral messenger RNA transcription, processing, splicing, and molecular structure. NijhofT Publishing, BostonGoogle Scholar
  56. Plyusnin A, Vapalahti O, Vaheri A (1996) Hantaviruses: genome structure, expression and evolution. J Gen Virol 77:2677–2687PubMedCrossRefGoogle Scholar
  57. Poch O, Sauvaget I, Delarue M, Tordo N (1989) Identification of four conserved motifs among the RNA-dependent polymerase encoding elements. EMBO Journal 8:3867–3875PubMedGoogle Scholar
  58. Prehaud C, Lopez N, Blok MJ, Obry V, Bouloy M (1997) Analysis of the 3’ terminal sequence recognized by the Rift Valley fever virus transcription complex in its ambisense S segment. Virology 227:189–197PubMedCrossRefGoogle Scholar
  59. Raju R, Kolakofsky D (1987) Translational requirement of La Crosse virus S-mRNA synthesis. J Virol 63:122–128Google Scholar
  60. Raju R, Kolakofsky D (1989) The ends of La Crosse virus genome and antigenome RNAs within nucleocapsids are base paired. J Virol 63:122–128PubMedGoogle Scholar
  61. Robertson JS, Schubert M, Lazzarini RA (1981) Polyadenylation sites for influenza virus mRNA. J Virol 38:157–163PubMedGoogle Scholar
  62. Rodriguez LL, Owens JH, Peters CJ, Nichol ST (1998) Genetic reassortment among viruses causing hantavirus pulmonary syndrome. Virology 242:99–106PubMedCrossRefGoogle Scholar
  63. Rossier C, Patterson J, Kolakofsky D (1986) La Crosse virus small genome mRNA is made in the cytoplasm. J Virol 58:647–650PubMedGoogle Scholar
  64. Sankar S, Porter AG (1992) Point mutations which drastically affect the polymerization activity of encephalomyocarditis virus RNA-dependent RNA polymerase correspond to the active site of Escherichia coli DNA polymerase I. J Biol Chem 267:10168–10176PubMedGoogle Scholar
  65. Schmaljohn CS (1996a) Bunyaviridae: The viruses and their replication. In: Fields BN, Knipe DM, Howley PM (eds) Fields Virology. Lippencott-Raven, PhiladelphiaGoogle Scholar
  66. Schmaljohn CS (1996b) Molecular Biology of Hantaviruses. In: Elliott RM (ed) The Bunyaviridae. Plenum Press, New YorkGoogle Scholar
  67. Schmaljohn CS (1998) Hantaviruses (Bunyaviridae). In: Webster RG, Granoff A (eds) Encyclopedia of Virology. W.B. Saunders, LondonGoogle Scholar
  68. Schmaljohn CS, Dalrymple JM (1983) Analysis of Hantaan virus RNA: evidence for a new genus of Bunyviridae. Virology 131:482–491PubMedCrossRefGoogle Scholar
  69. Schmaljohn CS, Hasty SE, Harrison SA, Dalrymple JM (1983) Characterization of Hantaan virions, the prototype virus of hemorrhagic fever with renal syndrome. J Infect Dis 148:1005–1012PubMedCrossRefGoogle Scholar
  70. Seong BL, Brownlee GG (1992) Nucleotides 9 to 11 of the influenza A virion RNA promoter are crucial for activity in vitro. J Gen Virol 73:3115–3124PubMedCrossRefGoogle Scholar
  71. Severson W, Partin L, Schmaljohn CS, Jonsson CB (1999) Characterization of the Hantaan nucleocapsid protein-ribonucleic acid interaction. J Biol Chem 274:33732–33739PubMedCrossRefGoogle Scholar
  72. Shapiro GI, Krug RM (1988) Influenza virus RNA replication in vitro: synthesis of viral template RNAs and virion RNAs in the absence of an added primer. J Virol 62:2285–2290PubMedGoogle Scholar
  73. Siomi H, Dreyfuss G (1997) RNA-binding proteins as regulators of gene expression. Curr Opin Gen Dev 7:345–353CrossRefGoogle Scholar
  74. Steitz TA (1999) DNA polymerases: structural diversity and common mechanisms. J Biol Chem 274:17395–17398PubMedCrossRefGoogle Scholar
  75. Tanishita O, Takahashi Y, Okuno Y, Tamura M, Asada H, Dantas J Jr, Yamanouchi T, Domae K, Kurata T, Yamanishi K (1986) Persistent infection of rats with haemorrhagic fever with renal syndrome virus and their antibody responses. J Gen Virol 67:2819–2824PubMedCrossRefGoogle Scholar
  76. Uhrig JF, Soellick TR, Minke CJ, Philipp C, Kellmann JW, Schreier PH (1999) Homotypic interaction and multimerization of nucleocapsid protein of tomato spotted wilt tospovirus: identification and characterization of two interacting domains. Proc Natl Acad Sci USA 96:55–60PubMedCrossRefGoogle Scholar
  77. Ulmanen I, Seppala P, Pettersson RF (1981) In vitro translation of Uukuniemi virus-specific RNAs: identification of a nonstructural protein and a precursor to the membrane glycoproteins. J Virol 37:72–79PubMedGoogle Scholar
  78. Urquidi V, Bishop DHL (1992) Non-random reassortment between the tripartite RNA genomes of La Crosse and snowshoe hare viruses. J Gen Virol 73:2255–2265PubMedCrossRefGoogle Scholar
  79. Vialat P, Bouloy M (1992) Germiston virus transcriptase requires active 40S ribosomal subunits and utilizes capped cellular RNAs. J Virol 66:685–693PubMedGoogle Scholar
  80. Wo wer IK, Wower J, Zimmermann RA (1998) Ribosomal protein L27 participates in both 50S subunit assembly and the peptidyl transferase reactions. J Biol Chem 273:19847–19852CrossRefGoogle Scholar
  81. Yoo YC, Yoshimatsu K, Yoshida R, Tamura M, Azuma I, Arikawa J (1993) Comparison of virulence between Seoul virus strain SR-11 and Hantaan virus strain 76–118 of hantaviruses in newborn mice. Microbiol Immunol 37:557–562PubMedGoogle Scholar
  82. Zhang F (1984) Seroepidemiological investigation on hemorrhagic fever with renal syndrome. III. Carrier state and familial aggregation. Chung Hua Liu Hsing Ping Hsueh Tsa Chih 5:5–8PubMedGoogle Scholar
  83. Zhang X, Takashima I, Hashimoto N (1988) Role of maternal antibody in protection from hemorrhagic fever with renal syndrome virus infection in rats. Arch Virol 103:253–265PubMedCrossRefGoogle Scholar
  84. Zhang X, Takashima I, Mori F, Hashimoto N (1989) Comparison of virulence between two strains of Rattus serotype hemorrhagic fever with renal syndrome HFRS virus in newborn rats. Microbiol Immunol 33:195–206PubMedGoogle Scholar
  85. Zucker M, Mathews DH, Turner DH (1999) Algorithms and thermodynamics for RNA secondary structure prediction: a practical guide. In: Barciszewski J, Clark BFC (eds) RNA Biochemistry and Biotechnology. Kluwer Academic PublishersGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2001

Authors and Affiliations

  • C. B. Jonsson
    • 1
  • C. S. Schmaljohn
    • 2
  1. 1.Department of Chemistry and BiochemistryNew Mexico State UniversityLas CrucesUSA
  2. 2.United States Army Medical Research Institute of Infectious DiseasesFort DetrickFrederickUSA

Personalised recommendations