Hantavirus Maturation

  • C. F. Spiropoulou
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 256)


During the process of virus maturation, all the viral structural components accumulate at the cell surface in order to interact and assemble into mature virions. The majority of the negative stranded RNA viruses have been shown to assemble and bud from the cell surface (Cadd et al. 1997; Garoff et al. 1998). In contrast, viruses of the family Bunyaviridae are characterized by an unusual pattern of intracellular maturation where the bilipid envelope of the virus particles is derived from the membranes of the endoplasmic reticulum-Golgi compartment (Murphy et al. 1973; Pettersson and Melin 1996). Due to this characteristic feature, Golgi maturation has been used as one of the criteria for classification of viruses as members of the family Bunyaviridae.


Cytoplasmic Tail Hemorrhagic Fever With Renal Syndrome Hantaan Virus Hantavirus Pulmonary Syndrome Virus Maturation 
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.


  1. Andersson AM, Melin L, Persson R, Raschperger E, Wikstrom L, Pettersson RF (1997a) Processing and membrane topology of the spike proteins Gl and G2 of Uukuniemi virus. J Virol 71:218–225PubMedGoogle Scholar
  2. Andersson AM, Melin L, Bean A, Pettersson RF (1997b) A retention signal necessary and sufficient for Golgi localization maps to the cytoplasmic tail of a Bunyaviridae (Uukuniemi virus) membrane glycoprotein. J Virol 71:4717–4727PubMedGoogle Scholar
  3. Anheier B, Lober C, Lindow S, Klenk H-D, Feldmann H (1999) Intracellular maturation of Hantaan virus glycoproteins. Abstract, XIth International Congress of Virology (VP11.03)Google Scholar
  4. Antic D, Wright KE, Kang CY (1992) Maturation of Hantaan virus glycoproteins Gl and G2. Virology 189:324–328PubMedCrossRefGoogle Scholar
  5. Arikawa J, Schmaljohn AL, Dalrymple JM, Schmaljohn CS (1989) Characterization of Hantaan virus envelope glycoprotein antigenic determinants defined by monoclonal antibodies. J Gen Virol 70:615–624PubMedCrossRefGoogle Scholar
  6. Betenbaugh M, Yu M, Kuehl K, White J, Pennock D, Spik K, Schmaljohn CS (1995) Nucleocapsid- and virus-like particles assemble in cells infected with recombinant baculoviruses or vaccinia viruses expressing the M and S segments of Hantaan virus. Virus Res 38:111–124PubMedCrossRefGoogle Scholar
  7. Bridgen A, Elliott RM (1996) Rescue of a segmented negative-strand RNA virus entirely from cloned complementary DNAs. Proc Natl Acad Sci USA 93:15400–15405PubMedCrossRefGoogle Scholar
  8. Cadd TL, Skoging U, Liljestrom P (1997) Budding of enveloped viruses from the plasma membrane. BioEssays 19:993–1000PubMedCrossRefGoogle Scholar
  9. Chen S-Y, Matsuoka Y, Compans RW (1992) Assembly of Gl and G2 glycoprotein oligomers in Punta Toro virus-infected cells. Virus Res 22:215–225PubMedCrossRefGoogle Scholar
  10. Choukhi A, Pillez A, Drobecq H, Sergheraert C, Wychowski C, Dubuisson J (1999) Characterization of aggregates of hepatitis C virus glycoproteins. J Gen Virol 80:3099–3107PubMedGoogle Scholar
  11. Colley KJ, Lee EU, Paulson JC (1992) The signal anchor and stem regions of the beta-galactoside alpha 2,6-sialyltransferase may each act to localize the enzyme to the Golgi apparatus. J Biol Chem 267:7784–7793PubMedGoogle Scholar
  12. Delamarre L, Pique C, Rosenberg AR, Blot V, Grange M-P, Le Blanc I, Dokhelar M-C (1999) The Y-S-L-I Tyrosine-based motif in the cytoplasmic domain of the human T-cell leukemia virus type 1 envelope is essential for cell-to-cell transmission. J Virol 73:9659–9663PubMedGoogle Scholar
  13. Durbin AP, Hall SL, Siew JW, Whitehead SS, Collins PL, Murphy BR (1997) Recovery of infectious human parainfluenza virus type 3 from cDNA clone. Virology 235:323–332PubMedCrossRefGoogle Scholar
  14. Garcia-Mata R, Bebok Z, Sorscher EJ, Sztul ES (1999) Characterization and dynamics of aggresome formation by a cytosolic GFP-chimera. J Cell Biol 146:1239–1254PubMedCrossRefGoogle Scholar
  15. Garcin D, Pelet T, Calain PLR, Curran J, Kolakofsky D (1995) A highly recombinogenic. system for the recovery of infectious Sendai paramyxovirus from cDNA: generation of a novel copy-back non-defective interfering virus. EMBO J 14:6087–6094PubMedGoogle Scholar
  16. Gamier L, Bowzard B, Wills JW (1998) Recent advances and remaining problems in HIV assembly. AIDS 12:S5–S16Google Scholar
  17. Garoff H, Hewson R, Opstelten D-JE (1998) Virus maturation by budding. Micr Mol Bio Rev 62:1171–1190Google Scholar
  18. Goldsmith CS, Elliott LH, Peters CJ, Zaki SR (1995) Ultrastructural characteristics of Sin Nombre virus, causative agent of hantavirus pulmonary syndrome. Arch Virol 140:2107–2122PubMedCrossRefGoogle Scholar
  19. Gupta S, De BP, Drazba JA, Banergee AK (1998) Involvement of actin microfilaments in the replication of human parainfluenza virus type 3. J Virol 72:2655–2662PubMedGoogle Scholar
  20. Hung TH, Zinyi C, Tungxin Z, Semao X, Changshou H (1985) Morphology and morphogenesis of viruses of hemorrhagic fever with renal syndrome (HFRS): I. Some peculiar aspects of the morphogenesis of various strains of HFRS virus. Intervirology 23:97–108PubMedCrossRefGoogle Scholar
  21. Hung TH (1988) Atlas of hemorrhagic fever with renal syndrome. Science Press, BeijingGoogle Scholar
  22. Hutchinson KL, Peters CJ, Nichol ST (1996) Sin Nombre virus mRNA synthesis.PubMedCrossRefGoogle Scholar
  23. Jackson MR, Nilsson T, Peterson PA (1993) Retrieval of transmembrane proteins to the endoplasmic reticulum. J Cell Biol 121:317–333PubMedCrossRefGoogle Scholar
  24. Jantti J, Hilden P, Ronka H, Makiranta V, Keranen S, Kuismanen E (1997) Immunocytochemical analysis of Uukuniemi virus budding compartments: role of the intermediate compartment and the Golgi stack in virus maturation. J Virol 71:1162–1172PubMedGoogle Scholar
  25. Kamrud KI, Schmaljohn CS (1994) Expression strategy of the M genome segment of Hantaan virus. Virus Res 31:109–121PubMedCrossRefGoogle Scholar
  26. Laakkonen P, Auvinen P, Kujala P, Kaariainen L (1998) Alphavirus replicase protein NSP1 induces filopodia and rearrangement of actin filaments. J Virol 72:10256–10269Google Scholar
  27. Liu B, Dai R, Tian C-J, Dawson L, Gorelick R, Yu X-F (1999) Interaction of the Human Immunodeficiency virus type 1 nucleocapsid with actin. J Virol 73:2901–2908PubMedGoogle Scholar
  28. Lopez S, Yao J-S, Kuhn RJ, Strauss EG, Strauss JH (1994) Nucleocapsid-glycoprotein interactions required for assembly of alphaviruses. J Virol 68:1316–1323PubMedGoogle Scholar
  29. Machamer C, Rose JK (1987) A specific transmembrane domain of a Coronavirus El glycoprotein is required for its retention in the Golgi region. J Cell Biol 105:1205–1214PubMedCrossRefGoogle Scholar
  30. Matsuoka Y, Ihara T, Bishop DHL, Compans RW (1988) Intracellular accumulation of Punta Toro virus glycoproteins expressed from cloned cDNA. Virology 167:251–260PubMedCrossRefGoogle Scholar
  31. Matsuoka Y, Chen S-Y, Compans RW (1994) A signal for Golgi retention in the bunyavirus Gl glycoprotein. J Biol Chem 269:22565–22573PubMedGoogle Scholar
  32. Matsuoka Y, Chen S-Y, Holland CE, Compans RW (1996) Molecular determinants of Golgi retention in the Punta Toro virus Gl protein. Arch Biochem Biophys 336:184–189PubMedCrossRefGoogle Scholar
  33. Mebatsion T, Konig M, Conzelmann K-K (1996) Budding of rabies virus particles in the absence of the spike glycoprotein. Cell 84:941–951PubMedCrossRefGoogle Scholar
  34. Murphy FA, Harrison AK, Whitfield SG (1973) Bunyaviridae: morphologic and morphogenetic similarities of Bunyamwera serologic supergroup viruses and several other arthropod-borne viruses. Intervirology 1:297–316PubMedCrossRefGoogle Scholar
  35. Nakitare GW, Elliott RM (1993) Expression of the Bunyamwera virus M genome segment and intracellular localization of NSM. Virology 195:511–520PubMedCrossRefGoogle Scholar
  36. Neumann G, Watanabe T, Ito H, Watanabe S, Goto H, Gao P, Hughes M, Perez DR, Donis R, Hoffmann E, Hobom G, Kawaoka Y (1999) Generation of influenza A viruses entirely from cloned cDNAs. Proc Natl Acad Sci USA 96:9345–9350PubMedCrossRefGoogle Scholar
  37. Nichol ST, Spiropoulou CF, Morzunov S, Rollin PE, Ksiazek TG, Feldmann H, Sanchez A, Childs J, Zaki S, Peters CJ (1993) Genetic identification of a hantavirus associated with an outbreak of acute respiratory illness. Science 262:914–917PubMedCrossRefGoogle Scholar
  38. Nilsson T, Lucocq JM, Mackay D, Warren G (1991) The membrane spanning domain of b-l,4-galac-tosyltransferase specifies trans Golgi localization. EMBO J 10:3567–3575PubMedGoogle Scholar
  39. Nilsson T, Warren G (1994) Retention and retrieval in the endoplasmic reticulum and the Golgi apparatus. Curr Opin Cell Biol 6:517–521PubMedCrossRefGoogle Scholar
  40. Ohno H, Stewart J, Fournier M-C, Bosshart H, Rhee I, Miyatake S, Saito T, Gallusser A, Kirchhausen T, Bonifacino JS (1995) Interaction of tyrosine-based sorting signals with clathrin associated proteins. Science 269:1872–1874PubMedCrossRefGoogle Scholar
  41. Pekosz A, He B, Lamb RA (1999) Reverse genetics of negative-strand RNA viruses: closing the circle. Proc Natl Acad Sci USA 96:8804–8806PubMedCrossRefGoogle Scholar
  42. Pensiero MN, Hay J (1992) The Hantaan virus M-segment glycoproteins Gl and G2 can be expressed independently. J Virol 66:1907–1914PubMedGoogle Scholar
  43. Persson R, Pettersson RF (1991) Formation and intracellular transport of a heterodimeric viral spike protein complex. J Cell Biol 112:257–266PubMedCrossRefGoogle Scholar
  44. Pettersson RF, Melin L (1996) Synthesis, assembly and intracellular transport of Bunyaviridae membrane proteins. In: Elliott RM (ed) The Bunyaviridae. Plenum Press, New York, pp 159–188Google Scholar
  45. Ravkov EV, Nichol ST, Compans RW (1997) Polarized entry and release in epithelial cells of Black Creek Canal Virus, a New World hantavirus. J Virol 71:1147–1154PubMedGoogle Scholar
  46. Ravkov EV, Compans RW (1998) Role of actin microfilaments in Black Creek Canal virus morphogenesis.J Virol 72:2865–2870PubMedGoogle Scholar
  47. Ravkov EV, Compans RW (2000) Association of a hantavirus nucleocapsid protein with the Golgi complex. Abstract: cell biology of virus entry, replication and pathogenesis. Keystone symposia (216)Google Scholar
  48. Rodriguez LL, Owens JH, Peters CJ, Nichol ST (1998) Genetic reassortment among viruses causing hantavirus pulmonary syndrome. Virology 242:99–106PubMedCrossRefGoogle Scholar
  49. Rottier PJM (1995) The Coronaviruses membrane glycoprotein. In: Siddell SG (ed) The Coronaviridae. Plenum Press, New York and London, pp 73–113Google Scholar
  50. Ruusala A, Persson R, Schmaljohn CS, Pettersson RF (1992) Coexpression of the membrane glycoproteins Gl and G2 of Hantaan virus is required for targeting to the Golgi complex. Virology 186:53–64PubMedCrossRefGoogle Scholar
  51. Schmaljohn CS (1996a) Molecular biology of hantaviruses. In: Elliott RM (ed) The Bunyaviridae. Plenum Press, New York, pp 63–90Google Scholar
  52. Schmaljohn CS (1996b) Bunyaviridae and their replication. In: Fields BN, Knipe DM, Howley PM (eds) Virology, Lippincott-Raven Pub, Philadelphia, pp 1447–1471Google Scholar
  53. Schmaljohn CS, Dalrymple JM (1983) Analysis of Hantaan virus RNA: Evidence for a new genus of Bunyaviridae. Virology 131:482–491PubMedCrossRefGoogle Scholar
  54. Schmaljohn CS, Hasty SE, Dalrymple JM, LeDuc JW, Lee HW, von Bonsdorff C-H, Brummer-Korvenkontio M, Vaheri A, Tsai TF, Regnery HL, Goldgaber D, Lee P-W (1985) Antigenic and genetic properties of viruses linked to hemorrhagic fever with renal syndrome. Science 227:1041–1044PubMedCrossRefGoogle Scholar
  55. Schmaljohn CS, Hasty SE, Rasmussen L, Dalrymple JM (1986) Hantaan virus replication: effects of monensin, tunicamycin and endoglycosidases on the structural glycoproteins. J Gen Virol 67:707–717PubMedCrossRefGoogle Scholar
  56. Schmaljohn CS, Schmaljohn AL, Dalrymple JM (1987) Hantaan virus M RNA: coding strategy, nucleotide sequence, and gene order. Virology 157:31–39PubMedCrossRefGoogle Scholar
  57. Schnell MJ, Mebatsion T, Conzelmann K-K (1994) Infectious rabies viruses from cloned cDNA. EMBO J 13:4195–4203PubMedGoogle Scholar
  58. Schnell MJ, Buonocore L, Boritz E, Ghosh HP, Chernish R, Rose JK (1998) Requirement of a nonspecific glycoprotein cytoplasmic domain sequence to drive efficient budding of vesicular stomatitis virus. EMBO J 17:1289–1296PubMedCrossRefGoogle Scholar
  59. Spiropoulou CF, Morzunov S, Feldmann H, Sanchez A, Peters CJ, Nichol ST (1994) Genome structure and variability of a virus causing hantavirus pulmonary syndrome. Virology 200:715–723PubMedCrossRefGoogle Scholar
  60. Tirabassi RS, Enquist LW (1998) Role of envelope protein gE endocytosis in the Pseudorabies virus life cycle. J Virol 72:4571–4579PubMedGoogle Scholar
  61. Tsukita S, Yonemura S, Tsukita S (1997) ERM proteins: head to tail regulation of actin-plasma membrane interaction. Trends Biochem Sci 22:53–58PubMedCrossRefGoogle Scholar
  62. Vincent M, Martin A, Compans RW (1998) Function of the KKXX motif in endoplasmic reticulum retrieval of a transmembrane protein depends on the length and structure of the cytoplasmic domain. J Biol Chem 273:950–956PubMedCrossRefGoogle Scholar
  63. Wang M, Pennock DG, Spik KW, Schmaljohn CS (1993) Epitope mapping studies with neutralizing and non-neutralizing monoclonal antibodies to the Gl and G2 envelope glycoproteins of Hantaan virus. Virology 197:757–766PubMedCrossRefGoogle Scholar
  64. Weisz OA, Swift AM, Machamer CE (1993) Oligomerization of a membrane protein correlates with its retention in the Golgi complex. J Cell Biol 122:1185–1196PubMedCrossRefGoogle Scholar
  65. Wong SH, Low SH, Hong W (1992) The 17-residue transmembrane domain of ß-galactoside α2,6-sialyltransferase is sufficient for Golgi retention. J Cell Biol 117:245–258PubMedCrossRefGoogle Scholar
  66. Ye Z, Liu T, Offringa DP, McInnis J, Levandowski RA (1999) Association of influenza virus matrix protein with ribonucleoproteins. J Virol 73:7467–7473PubMedGoogle Scholar
  67. Zaki SR, Greer PW, Coffield LM, Goldsmith CS, Notle KB, Foucar K, Feddersen RM, Zumwalt RE, Miller GL, Khan AS, Rollin PE, Ksiazek TG, Nichol ST, Mahy BWJ, Peters CJ (1995) Hantavirus pulmonary syndrome: pathogenesis of an emerging infectious disease. Am J Pathol 146:552–579PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2001

Authors and Affiliations

  • C. F. Spiropoulou
    • 1
  1. 1.Special Pathogens Branch, Division for Viral and Rickettsial DiseasesCenters for Disease Control and PreventionAtlantaUSA

Personalised recommendations