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Archives of Virology

, Volume 150, Issue 9, pp 1693–1713 | Cite as

Hantavirus nucleocapsid protein: a multifunctional molecule with both housekeeping and ambassadorial duties

  • P. Kaukinen
  • A. Vaheri
  • A. Plyusnin
Brief Review

Summary.

In recent years important progress has been made studying the nucleocapsid (N) protein of hantaviruses. The N protein presents a good example of a multifunctional viral macromolecule. It is a major structural component of a virion that encapsidates viral RNA (vRNA). It also interacts with the virus polymerase (L protein) and one of the glycoproteins. On top of these “house keeping” duties, the N protein performs interactive “ambassadorial” functions interfering with important regulatory pathways in the infected cells.

Keywords

Infectious Disease Macromolecule Infected Cell Structural Component Regulatory Pathway 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Adamson, AL, Kenney, S 2001Epstein-Barr virus immediate-early protein BZLF1 is SUMO-1 modified and disrupts promyelocytic leukemia bodies.J Virol7523882399CrossRefPubMedGoogle Scholar
  2. Akhmatova, NK, Yusupova, RS, Khaiboullina, SF, Sibiryak, SV 2003Lymphocyte Apoptosis during Hemorragic Fever with Renal Syndrome.Russ J Immunol83746PubMedGoogle Scholar
  3. Alfadhli, A, Love, Z, Arvidson, B, Seeds, J, Willey, J, Barklis, E 2001Hantavirus nucleocapsid protein oligomerization.J Virol7520192023CrossRefPubMedGoogle Scholar
  4. Alfadhli, A, Steel, E, Finlay, L, Bachinger, HP, Barklis, E 2002Hantavirus nucleocapsid protein coiled-coil domains.J Biol Chem2772710327108CrossRefPubMedGoogle Scholar
  5. Andersson, AM, Melin, L, Bean, A, Pettersson, RF 1997A retention signal necessary and sufficient for Golgi localization maps to the cytoplasmic tail of a Bunyaviridae (Uukuniemi virus) membrane glycoprotein.J Virol7147174727PubMedGoogle Scholar
  6. Andersson, AM, Pettersson, RF 1998Targeting of a short peptide derived from the cytoplasmic tail of the G1 membrane glycoprotein of Uukuniemi virus (Bunyaviridae) to the Golgi complex.J Virol7295859596PubMedGoogle Scholar
  7. Andersson, I, Bladh, L, Mousavi-jazi, M, Magnusson, K, Lundkvist, Å, Haller, O, Mirazimi, A 2004Human MxA protein inhibits the replication of Crimean Congo hemorrhagic fever virus.J Virol7843234329CrossRefPubMedGoogle Scholar
  8. Andersson, I, Simon, M, Lundkvist, A, Nilsson, M, Holmstrom, A, Elgh, F, Mirazimi, A 2004Role of actin filaments in targeting of Crimean Congo hemorrhagic fever virus nucleocapsid protein to perinuclear regions of mammalian cells.J Med Virol728393CrossRefPubMedGoogle Scholar
  9. Avalos, RT, Yu, Z, Nayak, DP 1997Association of influenza virus NP and M1 proteins with cellular cytoskeletal elements in influenza virus-infected cells.J Virol7129472958PubMedGoogle Scholar
  10. Baudin, F, Bach, C, Cusack, S, Ruigrok, RW 1994Structure of influenza virus RNP. I. Influenza virus nucleoprotein melts secondary structure in panhandle RNA and exposes the bases to the solvent.EMBO J1331583165PubMedGoogle Scholar
  11. Betenbaugh, M, Yu, M, Kuehl, K, White, J, Pennock, D, Spik, K, Schmaljohn, C 1995Nucleocapsid- 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 Res38111124CrossRefPubMedGoogle Scholar
  12. Bouloy, M, Janzen, C, Vialat, P, Khun, H, Pavlovic, J, Huerre, M, Haller, O 2001Genetic evidence for an interferon-antagonistic function of rift valley fever virus nonstructural protein NSs.J Virol7513711377CrossRefPubMedGoogle Scholar
  13. Bridgen, A, Dalrymple, DA, Weber, F, Elliott, RM 2004Inhibition of Dugbe nairovirus replication by human MxA protein.Virus Res994750CrossRefPubMedGoogle Scholar
  14. Ceccaldi, PE, Valtorta, F, Braud, S, Hellio, R, Tsiang, H 1997Alteration of the actin-based cytoskeleton by rabies virus.J Gen Virol7828312835PubMedGoogle Scholar
  15. Cudmore, S, Reckmann, I, Way, M 1997Viral manipulations of the actin cytoskeleton.Trends Microbiol5142148CrossRefPubMedGoogle Scholar
  16. de Carvalho Nicacio, C, Gonzalez Della Valle, M, Padula, P, Bjorling, E, Plyusnin, A, Lundkvist, A 2002Cross-protection against challenge with Puumala virus after immunization with nucleocapsid proteins from different hantaviruses.J Virol7666696677CrossRefPubMedGoogle Scholar
  17. Digard, P, Elton, D, Bishop, K, Medcalf, E, Weeds, A, Pope, B 1999Modulation of nuclear localization of the influenza virus nucleoprotein through interaction with actin filaments.J Virol7322222231PubMedGoogle Scholar
  18. Elliott RM, Bouloy M, Calisher CH, Goldbach R, Moyer JT, Nichol ST, Petterson R, Plyusnin A, Schmaljohn C (2000) Bunyaviridae. In: van Regenmortel MHV, Fauquet CM, Bishop DHL, Carstens EB, Estes MK, Lemon SM, Maniloff J, Mayo MA, McGeoch DJ, Pringle CR, Wickner RB (eds) Virus Taxonomy: The Classification and Nomenclature of Viruses. The Seventh Report of the International Committee on Taxonomy of Viruses. Academic Press, San Diego, pp 599–621Google Scholar
  19. Ennis, FA, Cruz, J, Spiropoulou, CF, Waite, D, Peters, CJ, Nichol, ST, Kariwa, H, Koster, FT 1997Hantavirus pulmonary syndrome: CD8+ and CD4+ cytotoxic T lymphocytes to epitopes on Sin Nombre virus nucleocapsid protein isolated during acute illness.Virology238380390CrossRefPubMedGoogle Scholar
  20. Everett, RD, Freemont, P, Saitoh, H, Dasso, M, Orr, A, Kathoria, M, Parkinson, J 1998The disruption of ND10 during herpes simplex virus infection correlates with the Vmw110- and proteasome-dependent loss of several PML isoforms.J Virol7265816591PubMedGoogle Scholar
  21. Flick, K, Hooper, JW, Schmaljohn, CS, Pettersson, RF, Feldmann, H, Flick, R 2003Rescue of Hantaan virus minigenomes.Virology306219224CrossRefPubMedGoogle Scholar
  22. Fooks, AR, Stephenson, JR, Warnes, A, Dowsett, AB, Rima, BK, Wilkinson, GW 1993Measles virus nucleocapsid protein expressed in insect cells assembles into nucleocapsid-like structures.J Gen Virol7414391444PubMedGoogle Scholar
  23. Frese, M, Kochs, G, Feldmann, H, Hertkorn, C, Haller, O 1996Inhibition of bunyaviruses, phleboviruses, and hantaviruses by human MxA protein.J Virol70915923PubMedGoogle Scholar
  24. Garcin, D, Lezzi, M, Dobbs, M, Elliott, RM, Schmaljohn, C, Kang, CY, Kolakofsky, D 1995The 5′ ends of Hantaan virus (Bunyaviridae) RNAs suggest a prime-and-realign mechanism for the initiation of RNA synthesis.J Virol6957545762PubMedGoogle Scholar
  25. Gavrilovskaya, IN, Brown, EJ, Ginsberg, MH, Mackow, ER 1999Cellular entry of hantaviruses which cause hemorrhagic fever with renal syndrome is mediated by beta3 integrins.J Virol7339513959PubMedGoogle Scholar
  26. Gavrilovskaya, IN, Peresleni, T, Geimonen, E, Mackow, ER 2002Pathogenic hantaviruses selectively inhibit beta3 integrin directed endothelial cell migration.Arch Virol14719131931CrossRefPubMedGoogle Scholar
  27. Gavrilovskaya, IN, Shepley, M, Shaw, R, Ginsberg, MH, Mackow, ER 1998beta3 Integrins mediate the cellular entry of hantaviruses that cause respiratory failure.Proc Natl Acad Sci USA9570747079CrossRefPubMedGoogle Scholar
  28. Geimonen, E, Neff, S, Raymond, T, Kocer, SS, Gavrilovskaya, IN, Mackow, ER 2002Pathogenic and nonpathogenic hantaviruses differentially regulate endothelial cell responses.Proc Natl Acad Sci USA991383713842CrossRefPubMedGoogle Scholar
  29. Goldsmith, CS, Elliott, LH, Peters, CJ, Zaki, SR 1995Ultrastructural characteristics of Sin Nombre virus, causative agent of hantavirus pulmonary syndrome.Arch Virol14021072122CrossRefPubMedGoogle Scholar
  30. Gott, P, Zoller, L, Darai, G, Bautz, EK 1997A major antigenic domain of hantaviruses is located on the aminoproximal site of the viral nucleocapsid protein.Virus Genes143140CrossRefPubMedGoogle Scholar
  31. Guldner, HH, Szostecki, C, Grotzinger, T, Will, H 1992IFN enhance expression of Sp100, an autoantigen in primary biliary cirrhosis.J Immunol14940674073PubMedGoogle Scholar
  32. Gupta, S, De, BP, Drazba, JA, Banerjee, AK 1998Involvement of actin microfilaments in the replication of human parainfluenza virus type 3.J Virol7226552662PubMedGoogle Scholar
  33. Haller, O, Kochs, G 2002Interferon-induced mx proteins: dynamin-like GTPases with antiviral activity.Traffic3710717CrossRefPubMedGoogle Scholar
  34. Haynes, JI,2nd, Chang, D, Consigli, RA 1993Mutations in the putative calcium-binding domain of polyomavirus VP1 affect capsid assembly.J Virol6724862495PubMedGoogle Scholar
  35. Heggeness, MH, Smith, PR, Ulmanen, I, Krug, RM, Choppin, PW 1982Studies on the helical nucleocapsid of influenza virus.Virology118466470CrossRefPubMedGoogle Scholar
  36. Huang, YT, Romito, RR, De, BP, Banerjee, AK 1993Characterization of the in vitro system for the synthesis of mRNA from human respiratory syncytial virus.Virology193862867CrossRefPubMedGoogle Scholar
  37. Hutchinson, KL, Peters, CJ, Nichol, ST 1996Sin Nombre virus mRNA synthesis.Virology224139149CrossRefPubMedGoogle Scholar
  38. Iseni, F, Barge, A, Baudin, F, Blondel, D, Ruigrok, RW 1998Characterization of rabies virus nucleocapsids and recombinant nucleocapsid-like structures.J Gen Virol7929092919PubMedGoogle Scholar
  39. Iseni, F, Baudin, F, Blondel, D, Ruigrok, RW 2000Structure of the RNA inside the vesicular stomatitis virus nucleocapsid.RNA6270281CrossRefPubMedGoogle Scholar
  40. Jang, MS, Ryu, SW, Kim, E 2002Modification of Daxx by small ubiquitin-related modifier-1.Biochem Biophys Res Commun295495500CrossRefPubMedGoogle Scholar
  41. Jin, M, Park, J, Lee, S, Park, B, Shin, J, Song, KJ, Ahn, TI, Hwang, SY, Ahn, BY, Ahn, K 2002Hantaan virus enters cells by clathrin-dependent receptor-mediated endocytosis.Virology2946069CrossRefPubMedGoogle Scholar
  42. Johnson KM (2001) Hantaviruses: history and overview. In: Schmaljohn CS, Nichol ST (eds) Hantaviruses. Springer, Berlin Heidelberg New York Tokyo, pp 1–14Google Scholar
  43. Jonsson CB, Schmaljohn CS (2001) Replication of Hantaviruses. In: Schmaljohn CS, Nichol ST (eds) Hantaviruses. Springer, Berlin Heidelberg New York Tokyo, pp 15–32Google Scholar
  44. Kanerva, M, Melen, K, Vaheri, A, Julkunen, I 1996Inhibition of Puumala and Tula hantaviruses in Vero cells by MxA protein.Virology2245562CrossRefPubMedGoogle Scholar
  45. Kang, JI, Park, SH, Lee, PW, Ahn, BY 1999Apoptosis is induced by hantaviruses in cultured cells.Virology26499105CrossRefPubMedGoogle Scholar
  46. Kariwa, H, Tanabe, H, Mizutani, T, Kon, Y, Lokugamage, K, Lokugamage, N, Iwasa, MA, Hagiya, T, Araki, K, Yoshimatsu, K, Arikawa, J, Takashima, I 2003Synthesis of Seoul virus RNA and structural proteins in cultured cells.Arch Virol14816711685CrossRefPubMedGoogle Scholar
  47. Kaukinen, P, Koistinen, V, Vapalahti, O, Vaheri, A, Plyusnin, A 2001Interaction between molecules of hantavirus nucleocapsid protein.J Gen Virol8218451853PubMedGoogle Scholar
  48. Kaukinen, P, Kumar, V, Tulimaki, K, Engelhardt, P, Vaheri, A, Plyusnin, A 2004Oligomerization of Hantavirus N protein: C-terminal alpha-helices interact to form a shared hydrophobic space.J Virol781366913677CrossRefPubMedGoogle Scholar
  49. Kaukinen, P, Vaheri, A, Plyusnin, A 2003Mapping of the regions involved in homotypic interactions of Tula hantavirus N protein.J Virol771091010916CrossRefPubMedGoogle Scholar
  50. Kaukinen, P, Vaheri, A, Plyusnin, A 2003Non-covalent interaction between nucleocapsid protein of Tula hantavirus and small ubiquitin-related modifier-1, SUMO-1.Virus Res923745CrossRefPubMedGoogle Scholar
  51. Kim, TY, Choi, Y, Cheong, HS, Choe, J 2002Identification of a cell surface 30 kDa protein as a candidate receptor for Hantaan virus.J Gen Virol83767773PubMedGoogle Scholar
  52. Klumpp, K, Ruigrok, RW, Baudin, F 1997Roles of the influenza virus polymerase and nucleoprotein in forming a functional RNP structure.EMBO J1612481257CrossRefPubMedGoogle Scholar
  53. Kochs, G, Janzen, C, Hohenberg, H, Haller, O 2002Antivirally active MxA protein sequesters La Crosse virus nucleocapsid protein into perinuclear complexes.Proc Natl Acad Sci USA9931533158CrossRefPubMedGoogle Scholar
  54. Kolesnikova, L, Muhlberger, E, Ryabchikova, E, Becker, S 2000Ultrastructural organization of recombinant Marburg virus nucleoprotein: comparison with Marburg virus inclusions.J Virol7438993904CrossRefPubMedGoogle Scholar
  55. Kukkonen, SK, Vaheri, A, Plyusnin, A 2005L protein, the RNA-dependent RNA polymerase of hantaviruses.Arch Virol150533556CrossRefPubMedGoogle Scholar
  56. Kukkonen, SK, Vaheri, A, Plyusnin, A 2004Tula hantavirus L protein is a 250 kDa perinuclear membrane-associated protein.J Gen Virol8511811189CrossRefPubMedGoogle Scholar
  57. Kumar, V, Heikkonen, J, Engelhardt, P, Kaski, K 2004Robust filtering and particle picking in micrograph images towards 3D reconstruction of purified proteins with cryo-electron microscopy.J Struct Biol1454151CrossRefPubMedGoogle Scholar
  58. Le May, N, Dubaele, S, Proietti De Santis, L, Billecocq, A, Bouloy, M, Egly, JM 2004TFIIH transcription factor, a target for the Rift Valley hemorrhagic fever virus.Cell116541550CrossRefPubMedGoogle Scholar
  59. Lee, BH, Yoshimatsu, K, Maeda, A, Ochiai, K, Morimatsu, M, Araki, K, Ogino, M, Morikawa, S, Arikawa, J 2003Association of the nucleocapsid protein of the Seoul and Hantaan hantaviruses with small ubiquitin-like modifier-1-related molecules.Virus Res988391CrossRefPubMedGoogle Scholar
  60. Leonard VHJ, Kohl A, Weber F, Osborne JC, Bridgen A, Elliott RM Interactions of bunyamwera bunyavirus nucleoprotein. 2nd European Meeting on Viral Zoonoses St. Raphael, France 2003Google Scholar
  61. Li, XD, Kukkonen, S, Vapalahti, O, Plyusnin, A, Lankinen, H, Vaheri, A 2004Tula hantavirus infection of Vero E6 cells induces apoptosis involving caspase 8 activation.J Gen Virol8532613268CrossRefPubMedGoogle Scholar
  62. Li, XD, Makela, TP, Guo, D, Soliymani, R, Koistinen, V, Vapalahti, O, Vaheri, A, Lankinen, H 2002Hantavirus nucleocapsid protein interacts with the Fas-mediated apoptosis enhancer Daxx.J Gen Virol83759766PubMedGoogle Scholar
  63. Lundkvist, A, Kallio-Kokko, H, Sjolander, KB, Lankinen, H, Niklasson, B, Vaheri, A, Vapalahti, O 1996Characterization of Puumala virus nucleocapsid protein: identification of B-cell epitopes and domains involved in protective immunity.Virology216397406CrossRefPubMedGoogle Scholar
  64. Mackow, ER, Gavrilovskaya, IN 2001Cellular receptors and hantavirus pathogenesis.Curr Top Microbiol Immunol25691115PubMedGoogle Scholar
  65. Maeda, A, Lee, BH, Yoshimatsu, K, Saijo, M, Kurane, I, Arikawa, J, Morikawa, S 2003The intracellular association of the nucleocapsid protein (NP) of hantaan virus (HTNV) with small ubiquitin-like modifier-1 (SUMO-1) conjugating enzyme 9 (Ubc9).Virology305288297CrossRefPubMedGoogle Scholar
  66. Markotic, A, Hensley, L, Geisbert, T, Spik, K, Schmaljohn, C 2003Hantaviruses induce cytopathic effects and apoptosis in continuous human embryonic kidney cells.J Gen Virol8421972202CrossRefPubMedGoogle Scholar
  67. Martin-Benito, J, Area, E, Ortega, J, Llorca, O, Valpuesta, JM, Carrascosa, JL, Ortin, J 2001Three-dimensional reconstruction of a recombinant influenza virus ribonucleoprotein particle.EMBO Rep2313317CrossRefPubMedGoogle Scholar
  68. Matunis, MJ, Coutavas, E, Blobel, G 1996A novel ubiquitin-like modification modulates the partitioning of the Ran-GTPase-activating protein RanGAP1 between the cytosol and the nuclear pore complex.J Cell Biol13514571470CrossRefPubMedGoogle Scholar
  69. Maul, GG 1998Nuclear domain 10, the site of DNA virus transcription and replication.Bioessays20660667CrossRefPubMedGoogle Scholar
  70. Mavrakis, M, Kolesnikova, L, Schoehn, G, Becker, S, Ruigrok, RW 2002Morphology of Marburg virus NP-RNA.Virology296300307CrossRefPubMedGoogle Scholar
  71. Melchior, F 2000SUMO-nonclassical ubiquitin.Annu Rev Cell Dev Biol16591626CrossRefPubMedGoogle Scholar
  72. Michaelson, JS, Bader, D, Kuo, F, Kozak, C, Leder, P 1999Loss of Daxx, a promiscuously interacting protein, results in extensive apoptosis in early mouse development.Genes Dev1319181923PubMedGoogle Scholar
  73. Mir, MA, Panganiban, AT 2004Trimeric hantavirus nucleocapsid protein binds specifically to the viral RNA panhandle.J Virol7882818288CrossRefPubMedGoogle Scholar
  74. Moyer, SA, Baker, SC, Horikami, SM 1990Host cell proteins required for measles virus reproduction.J Gen Virol71775783PubMedGoogle Scholar
  75. Muller, S, Dejean, A 1999Viral immediate-early proteins abrogate the modification by SUMO-1 of PML and Sp100 proteins, correlating with nuclear body disruption.J Virol7351375143PubMedGoogle Scholar
  76. Ortega, J, Martin-Benito, J, Zurcher, T, Valpuesta, JM, Carrascosa, JL, Ortin, J 2000Ultrastructural and functional analyses of recombinant influenza virus ribonucleoproteins suggest dimerization of nucleoprotein during virus amplification.J Virol74156163PubMedGoogle Scholar
  77. Osborne, JC, Elliott, RM 2000RNA binding properties of bunyamwera virus nucleocapsid protein and selective binding to an element in the 5′ terminus of the negative-sense S segment.J Virol7499469952CrossRefPubMedGoogle Scholar
  78. Paintsil, J, Muller, M, Picken, M, Gissmann, L, Zhou, J 1998Calcium is required in reassembly of bovine papillomavirus in vitro.J Gen Virol7911331141PubMedGoogle Scholar
  79. Parkinson, J, Everett, RD 2000Alphaherpesvirus proteins related to herpes simplex virus type 1 ICP0 affect cellular structures and proteins.J Virol741000610017CrossRefPubMedGoogle Scholar
  80. Pensiero, MN, Sharefkin, JB, Dieffenbach, CW, Hay, J 1992Hantaan virus infection of human endothelial cells.J Virol6659295936PubMedGoogle Scholar
  81. Petri, T, Dimmock, NJ 1981Phosphorylation of influenza virus nucleoprotein in vivo.J Gen Virol57185190PubMedGoogle Scholar
  82. Pettersson RF, Melin L (1996) Synthesis, assembly and intracellular transport of Bunyaviridae membrane proteins. In: Elliott RM (eds) The Bunyaviridae. Plenum Press, New York, pp 159–188Google Scholar
  83. Plyusnin, A 2002Genetics of hantaviruses: implications to taxonomy.Arch Virol147665682CrossRefPubMedGoogle Scholar
  84. Portela, A, Digard, P 2002The influenza virus nucleoprotein: a multifunctional RNA-binding protein pivotal to virus replication.J Gen Virol83723734PubMedGoogle Scholar
  85. Raftery, MJ, Kraus, AA, Ulrich, R, Kruger, DH, Schonrich, G 2002Hantavirus infection of dendritic cells.J Virol761072410733CrossRefPubMedGoogle Scholar
  86. Ravkov, EV, Compans, RW 2001Hantavirus nucleocapsid protein is expressed as a membrane-associated protein in the perinuclear region.J Virol7518081815CrossRefPubMedGoogle Scholar
  87. Ravkov, EV, Nichol, ST, Compans, RW 1997Polarized entry and release in epithelial cells of Black Creek Canal virus, a New World hantavirus.J Virol7111471154PubMedGoogle Scholar
  88. Ravkov, EV, Nichol, ST, Peters, CJ, Compans, RW 1998Role of actin microfilaments in Black Creek Canal virus morphogenesis.J Virol7228652870PubMedGoogle Scholar
  89. Rossier, C, Patterson, J, Kolakofsky, D 1986La Crosse virus small genome mRNA is made in the cytoplasm.J Virol58647650PubMedGoogle Scholar
  90. Rudolph, MG, Kraus, I, Dickmanns, A, Eickmann, M, Garten, W, Ficner, R 2003Crystal structure of the borna disease virus nucleoprotein.Structure1112191226CrossRefPubMedGoogle Scholar
  91. Ruusala, A, Persson, R, Schmaljohn, CS, Pettersson, RF 1992Coexpression of the membrane glycoproteins G1 and G2 of Hantaan virus is required for targeting to the Golgi complex.Virology1865364CrossRefPubMedGoogle Scholar
  92. Salonen, A, Ahola, T, Kaariainen, L 2005Viral RNA replication in association with cellular membranes.Curr Top Microbiol Immunol285139173PubMedGoogle Scholar
  93. Sandalon, Z, Oppenheim, A 1997Self-assembly and protein–protein interactions between the SV40 capsid proteins produced in insect cells.Virology237414421CrossRefPubMedGoogle Scholar
  94. Schmaljohn, CS, Dalrymple, JM 1983Analysis of Hantaan virus RNA: evidence for a new genus of bunyaviridae.Virology131482491CrossRefPubMedGoogle Scholar
  95. Schoehn, G, Iseni, F, Mavrakis, M, Blondel, D, Ruigrok, RW 2001Structure of recombinant rabies virus nucleoprotein-RNA complex and identification of the phosphoprotein binding site.J Virol75490498CrossRefPubMedGoogle Scholar
  96. Seeler, JS, Dejean, A 2003Nuclear and unclear functions of SUMO.Nat Rev Mol Cell Biol4690699CrossRefPubMedGoogle Scholar
  97. Sen, GC, Ransohoff, RM 1993Interferon-induced antiviral actions and their regulation.Adv Virus Res4257102PubMedGoogle Scholar
  98. Severson, W, Partin, L, Schmaljohn, CS, Jonsson, CB 1999Characterization of the Hantaan nucleocapsid protein-ribonucleic acid interaction.J Biol Chem2743373233739CrossRefPubMedGoogle Scholar
  99. Severson, WE, Xu, X, Jonsson, CB 2001cis-Acting signals in encapsidation of Hantaan virus S-segment viral genomic RNA by its N protein.J Virol7526462652CrossRefPubMedGoogle Scholar
  100. Shi, X, Elliott, RM 2002Golgi localization of Hantaan virus glycoproteins requires coexpression of G1 and G2.Virology3003138CrossRefPubMedGoogle Scholar
  101. Sironen, T, Vaheri, A, Plyusnin, A 2001Molecular evolution of Puumala hantavirus.J Virol751180311810CrossRefPubMedGoogle Scholar
  102. Smith, GA, Enquist, LW 2002Break ins and break outs: viral interactions with the cytoskeleton of Mammalian cells.Annu Rev Cell Dev Biol18135161CrossRefPubMedGoogle Scholar
  103. Spehner, D, Kirn, A, Drillien, R 1991Assembly of nucleocapsidlike structures in animal cells infected with a vaccinia virus recombinant encoding the measles virus nucleoprotein.J Virol6562966300PubMedGoogle Scholar
  104. Spiropoulou, CF, Goldsmith, CS, Shoemaker, TR, Peters, CJ, Compans, RW 2003Sin Nombre virus glycoprotein trafficking.Virology3084863CrossRefPubMedGoogle Scholar
  105. Temonen, M, Vapalahti, O, Holthofer, H, Brummer-Korvenkontio, M, Vaheri, A, Lankinen, H 1993Susceptibility of human cells to Puumala virus infection.J Gen Virol74515518PubMedGoogle Scholar
  106. Thomas, D, Blakqori, G, Wagner, V, Banholzer, M, Kessler, N, Elliott, RM, Haller, O, Weber, F 2004Inhibition of RNA polymerase II phosphorylation by a viral interferon antagonist.J Biol Chem2793147131477CrossRefPubMedGoogle Scholar
  107. Thomas, D, Newcomb, WW, Brown, JC, Wall, JS, Hainfeld, JF, Trus, BL, Steven, AC 1985Mass and molecular composition of vesicular stomatitis virus: a scanning transmission electron microscopy analysis.J Virol54598607PubMedGoogle Scholar
  108. Torii, S, Egan, DA, Evans, RA, Reed, JC 1999Human Daxx regulates Fas-induced apoptosis from nuclear PML oncogenic domains (PODs).EMBO J1860376049CrossRefPubMedGoogle Scholar
  109. Tuffereau, C, Fischer, S, Flamand, A 1985Phosphorylation of the N and M1 proteins of rabies virus.J Gen Virol6622852289PubMedGoogle Scholar
  110. Uhrig, JF, Soellick, TR, Minke, CJ, Philipp, C, Kellmann, JW, Schreier, PH 1999Homotypic interaction and multimerization of nucleocapsid protein of tomato spotted wilt tospovirus: identification and characterization of two interacting domains.Proc Natl Acad Sci USA965560CrossRefPubMedGoogle Scholar
  111. Van Epps, HL, Terajima, M, Mustonen, J, Arstila, TP, Corey, EA, Vaheri, A, Ennis, FA 2002Long-lived memory T lymphocyte responses after hantavirus infection.J Exp Med196579588CrossRefPubMedGoogle Scholar
  112. Vapalahti, O, Kallio-Kokko, H, Narvanen, A, Julkunen, I, Lundkvist, A, Plyusnin, A, Lehvaslaiho, H, Brummer-Korvenkontio, M, Vaheri, A, Lankinen, H 1995Human B-cell epitopes of Puumala virus nucleocapsid protein, the major antigen in early serological response.J Med Virol46293303PubMedGoogle Scholar
  113. Vulliemoz, D, Roux, L 2001“Rule of six”: how does the Sendai virus RNA polymerase keep count?J Virol7545064518CrossRefPubMedGoogle Scholar
  114. Weber, F, Bridgen, A, Fazakerley, JK, Streitenfeld, H, Kessler, N, Randall, RE, Elliott, RM 2002Bunyamwera bunyavirus nonstructural protein NSs counteracts the induction of alpha/beta interferon.J Virol7679497955CrossRefPubMedGoogle Scholar
  115. Wilson, VG, Rangasamy, D 2001Viral interaction with the host cell sumoylation system.Virus Res811727CrossRefPubMedGoogle Scholar
  116. Wolf, E, Kim, PS, Berger, B 1997MultiCoil: a program for predicting two- and three-stranded coiled coils.Protein Sci611791189PubMedGoogle Scholar
  117. Wootton, SK, Yoo, D 2003Homo-oligomerization of the porcine reproductive and respiratory syndrome virus nucleocapsid protein and the role of disulfide linkages.J Virol7745464557CrossRefPubMedGoogle Scholar
  118. Xu, X, Severson, W, Villegas, N, Schmaljohn, CS, Jonsson, CB 2002The RNA binding domain of the hantaan virus N protein maps to a central, conserved region.J Virol7633013308CrossRefPubMedGoogle Scholar
  119. Yoshimatsu, K, Lee, BH, Araki, K, Morimatsu, M, Ogino, M, Ebihara, H, Arikawa, J 2003The multimerization of hantavirus nucleocapsid protein depends on type-specific epitopes.J Virol77943952CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag/Wien 2005

Authors and Affiliations

  • P. Kaukinen
    • 1
  • A. Vaheri
    • 1
  • A. Plyusnin
    • 1
  1. 1.Department of VirologyHaartman Institute, University of HelsinkiFinland

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