Skip to main content
SpringerLink
Log in

Bunyavirus: Structure and Replication

  • Chapter
  • First Online:
Viral Molecular Machines

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 726))

Abstract

The Bunyaviridae family is comprised of a large number of negative-sense, single-stranded RNA viruses that infect animals, insects, and plants. The tripartite genome of bunyaviruses, encapsidated in the form of individual ribonucleoprotein complexes, encodes four structural proteins, the glycoproteins Gc and Gn, the nucleoprotein N, and the viral polymerase L. Some bunyaviruses also use an ambi-sense strategy to encode the nonstructural proteins NSs and NSm. While some bunyaviruses have a T = 12 icosahedral symmetry, others only have locally ordered capsids, or capsids with no detectable symmetry. Bunyaviruses enter cells through clathrin-mediated endocytosis or phagocytosis. In endosome, viral glycoproteins facilitate membrane fusion at acidic pH, thus allowing bunyaviruses to uncoat and deliver their genomic RNA into host cytoplasm. Bunyaviruses replicate in cytoplasm where the viral polymerase L catalyzes both transcription and replication of the viral genome. While transcription requires a cap primer for initiation and ends at specific termination signals before the 3′ end of the template is reached, replication copies the entire template and does not depend on any primer for initiation. This review will discuss some of the most interesting aspects of bunyavirus replication, including L protein/N protein-mediated cap snatching, prime-and-realign for transcription and replication initiation, translation-coupled transcription, sequence/secondary structure-dependent transcription termination, ribonucleoprotein encapsidation, and N protein-mediated initiation of viral protein translation. Recent developments on the structure and functional characterization of the bunyavirus capsid and the RNA synthesis machineries (including both protein L and N) will also be discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

BDV:

Borna disease virus

BUNV:

Bunyamwera virus

CCHFV:

Crimean–Congo hemorrhagic fever virus

cRNA:

Complementary RNA or antigenomic RNA

EM:

Electron microscopy

FluA:

Influenza A virus

JCV:

Jamestown Canyon virus

LACV:

La Crosse virus

nt:

Nucleotide

NTR:

Nontranslated terminal region

OTU:

Ovarian tumor-like protease motif

PTV:

Punta Toro virus

RdRp:

RNA-dependent RNA polymerase

RNP:

Ribonucleoprotein complex

RSV:

Respiratory syncytial virus

RV:

Rabies virus

RVFV:

Rift Valley fever virus

SNV:

Sin Nombre virus

TSWV:

Tomato spotted wilt virus

UUKV:

Uukuniemi virus

vRNA:

Viral RNA or genomic RNA

VSV:

Vesicular stomatitis virus

References

  • Abraham G, Pattnaik AK (1983) Early RNA synthesis in Bunyamwera virus-infected cells. J Gen Virol 64(Pt 6):1277–1290

    Article  PubMed  CAS  Google Scholar 

  • Accardi L, Prehaud C, Di Bonito P, Mochi S, Bouloy M, Giorgi C (2001) Activity of Toscana and Rift Valley fever virus transcription complexes on heterologous templates. J Gen Virol 82:781–785

    PubMed  CAS  Google Scholar 

  • Albertini AA, Wernimont AK, Muziol T, Ravelli RB, Clapier CR, Schoehn G, Weissenhorn W, Ruigrok RW (2006) Crystal structure of the rabies virus nucleoprotein-RNA complex. Science 313:360–363

    Article  PubMed  CAS  Google Scholar 

  • Alfadhli A, Love Z, Arvidson B, Seeds J, Willey J, Barklis E (2001) Hantavirus nucleocapsid protein oligomerization. J Virol 75:2019–2023

    Article  PubMed  CAS  Google Scholar 

  • Barr JN (2007) Bunyavirus mRNA synthesis is coupled to translation to prevent premature transcription termination. RNA 13:731–736

    Article  PubMed  CAS  Google Scholar 

  • Barr JN, Wertz GW (2004) Bunyamwera bunyavirus RNA synthesis requires cooperation of 3′- and 5′-terminal sequences. J Virol 78:1129–1138

    Article  PubMed  CAS  Google Scholar 

  • Barr JN, Wertz GW (2005) Role of the conserved nucleotide mismatch within 3′- and 5′-terminal regions of Bunyamwera virus in signaling transcription. J Virol 79:3586–3594

    Article  PubMed  CAS  Google Scholar 

  • Barr JN, Elliott RM, Dunn EF, Wertz GW (2003) Segment-specific terminal sequences of Bunyamwera bunyavirus regulate genome replication. Virology 311:326–338

    Article  PubMed  CAS  Google Scholar 

  • Barr JN, Rodgers JW, Wertz GW (2006) Identification of the Bunyamwera bunyavirus transcription termination signal. J Gen Virol 87:189–198

    Article  PubMed  CAS  Google Scholar 

  • Battisti AJ, Chu YK, Chipman PR, Kaufmann B, Jonsson CB, Rossmann MG (2011) Structural studies of Hantaan virus. J Virol 85:835–841

    Article  PubMed  CAS  Google Scholar 

  • Bellocq C, Raju R, Patterson J, Kolakofsky D (1987) Translational requirement of La Crosse virus S-mRNA synthesis: in vitro studies. J Virol 61:87–95

    PubMed  CAS  Google Scholar 

  • Bergeron E, Albarino CG, Khristova ML, Nichol ST (2010) Crimean-Congo hemorrhagic fever virus-encoded ovarian tumor protease activity is dispensable for virus RNA polymerase function. J Virol 84:216–226

    Article  PubMed  CAS  Google Scholar 

  • Bishop DH, Gay ME, Matsuoko Y (1983) Nonviral heterogeneous sequences are present at the 5′ ends of one species of snowshoe hare bunyavirus S complementary RNA. Nucleic Acids Res 11:6409–6418

    Article  PubMed  CAS  Google Scholar 

  • Blakqori G, Kochs G, Haller O, Weber F (2003) Functional L polymerase of La Crosse virus allows in vivo reconstitution of recombinant nucleocapsids. J Gen Virol 84:1207–1214

    Article  PubMed  CAS  Google Scholar 

  • Blakqori G, van Knippenberg I, Elliott RM (2009) Bunyamwera orthobunyavirus S-segment untranslated regions mediate poly(A) tail-independent translation. J Virol 83:3637–3646

    Article  PubMed  CAS  Google Scholar 

  • Booth TF, Gould EA, Nuttall PA (1991) Structure and morphogenesis of Dugbe virus (Bunyaviridae, Nairovirus) studied by immunogold electron microscopy of ultrathin cryosections. Virus Res 21:199–212

    Article  PubMed  CAS  Google Scholar 

  • Boudko SP, Kuhn RJ, Rossmann MG (2007) The coiled-coil domain structure of the Sin Nombre virus nucleocapsid protein. J Mol Biol 366:1538–1544

    Article  PubMed  CAS  Google Scholar 

  • 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 175:50–58

    Article  PubMed  CAS  Google Scholar 

  • Collett MS (1986) Messenger RNA of the M segment RNA of Rift Valley fever virus. Virology 151:151–156

    Article  PubMed  CAS  Google Scholar 

  • de Haan P, Wagemakers L, Peters D, Goldbach R (1990) The S RNA segment of tomato spotted wilt virus has an ambisense character. J Gen Virol 71(Pt 5):1001–1007

    Article  PubMed  Google Scholar 

  • de Medeiros RB, Figueiredo J, Resende Rde O, De Avila AC (2005) Expression of a viral polymerase-bound host factor turns human cell lines permissive to a plant- and insect-infecting virus. Proc Natl Acad Sci USA 102:1175–1180

    Article  PubMed  CAS  Google Scholar 

  • Dias A, Bouvier D, Crepin T, McCarthy AA, Hart DJ, Baudin F, Cusack S, Ruigrok RW (2009) The cap-snatching endonuclease of influenza virus polymerase resides in the PA subunit. Nature 458:914–918

    Article  PubMed  CAS  Google Scholar 

  • Duijsings D, Kormelink R, Goldbach R (2001) In vivo analysis of the TSWV cap-snatching mechanism: single base complementarity and primer length requirements. EMBO J 20:2545–2552

    Article  PubMed  CAS  Google Scholar 

  • Dunn EF, Pritlove DC, Jin H, Elliott RM (1995) Transcription of a recombinant bunyavirus RNA template by transiently expressed bunyavirus proteins. Virology 211:133–143

    Article  PubMed  CAS  Google Scholar 

  • Egelman EH, Wu SS, Amrein M, Portner A, Murti G (1989) The Sendai virus nucleocapsid exists in at least four different helical states. J Virol 63:2233–2243

    PubMed  CAS  Google Scholar 

  • Eifan SA, Elliott RM (2009) Mutational analysis of the Bunyamwera orthobunyavirus nucleocapsid protein gene. J Virol 83:11307–11317

    Article  PubMed  CAS  Google Scholar 

  • Elliott RM (1990) Molecular biology of the Bunyaviridae. J Gen Virol 71(Pt 3):501–522

    Article  PubMed  CAS  Google Scholar 

  • Emery VC, Bishop DH (1987) Characterization of Punta Toro S mRNA species and identification of an inverted complementary sequence in the intergenic region of Punta Toro Phlebovirus ambisense S RNA that is involved in mRNA transcription termination. Virology 156:1–11

    Article  PubMed  CAS  Google Scholar 

  • 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 55:681–689

    PubMed  CAS  Google Scholar 

  • Flick R, Pettersson RF (2001) Reverse genetics system for Uukuniemi virus (Bunyaviridae): RNA polymerase I-catalyzed expression of chimeric viral RNAs. J Virol 75:1643–1655

    Article  PubMed  CAS  Google Scholar 

  • Flick R, Elgh F, Pettersson RF (2002) Mutational analysis of the Uukuniemi virus (Bunyaviridae family) promoter reveals two elements of functional importance. J Virol 76:10849–10860

    Article  PubMed  CAS  Google Scholar 

  • Fontana J, Lopez-Montero N, Elliott RM, Fernandez JJ, Risco C (2008) The unique architecture of Bunyamwera virus factories around the golgi complex. Cell Microbiol 10:2012–2028

    Article  PubMed  CAS  Google Scholar 

  • Freiberg AN, Sherman MB, Morais MC, Holbrook MR, Watowich SJ (2008) Three-dimensional organization of Rift Valley fever virus revealed by cryoelectron tomography. J Virol 82:10341–10348

    Article  PubMed  CAS  Google Scholar 

  • Garcin D, Kolakofsky D (1990) A novel mechanism for the initiation of Tacaribe arenavirus genome replication. J Virol 64:6196–6203

    PubMed  CAS  Google Scholar 

  • Garcin D, Kolakofsky D (1992) Tacaribe arenavirus RNA synthesis in vitro is primer dependent and suggests an unusual model for the initiation of genome replication. J Virol 66:1370–1376

    PubMed  CAS  Google Scholar 

  • 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 69:5754–5762

    PubMed  CAS  Google Scholar 

  • Garry CE, Garry RF (2004) Proteomics computational analyses suggest that the carboxyl terminal glycoproteins of Bunyaviruses are class II viral fusion protein (beta-penetrenes). Theor Biol Med Model 1:10

    Article  PubMed  CAS  Google Scholar 

  • Gavrilovskaya IN, Brown EJ, Ginsberg MH, Mackow ER (1999) Cellular entry of hantaviruses which cause hemorrhagic fever with renal syndrome is mediated by beta3 integrins. J Virol 73:3951–3959

    PubMed  CAS  Google Scholar 

  • Green TJ, Zhang X, Wertz GW, Luo M (2006) Structure of the vesicular stomatitis virus nucleoprotein-RNA complex. Science 313:357–360

    Article  PubMed  CAS  Google Scholar 

  • Habjan M, Penski N, Wagner V, Spiegel M, Overby AK, Kochs G, Huiskonen JT, Weber F (2009) Efficient production of Rift Valley fever virus-like particles: the antiviral protein MxA can inhibit primary transcription of bunyaviruses. Virology 385:400–408

    Article  PubMed  CAS  Google Scholar 

  • Haque A, Mir MA (2010) Interaction of hantavirus nucleocapsid protein with ribosomal protein S19. J Virol 84:12450–12453

    Article  PubMed  CAS  Google Scholar 

  • Honig JE, Osborne JC, Nichol ST (2004) Crimean-Congo hemorrhagic fever virus genome L RNA segment and encoded protein. Virology 321:29–35

    Article  PubMed  CAS  Google Scholar 

  • Huiskonen JT, Overby AK, Weber F, Grunewald K (2009) Electron cryo-microscopy and single-particle averaging of Rift Valley fever virus: evidence for GN-GC glycoprotein heterodimers. J Virol 83:3762–3769

    Article  PubMed  CAS  Google Scholar 

  • Huiskonen JT, Hepojoki J, Laurinmaki P, Vaheri A, Lankinen H, Butcher SJ, Grunewald K (2010) Electron cryotomography of Tula Hantavirus suggests a unique assembly paradigm for enveloped viruses. J Virol 84:4889–4897

    Article  PubMed  CAS  Google Scholar 

  • Hutchinson KL, Peters CJ, Nichol ST (1996) Sin Nombre virus mRNA synthesis. Virology 224:139–149

    Article  PubMed  CAS  Google Scholar 

  • Ihara T, Matsuura Y, Bishop DH (1985) Analyses of the mRNA transcription processes of Punta Toro Phlebovirus (Bunyaviridae). Virology 147:317–325

    Article  PubMed  CAS  Google Scholar 

  • Ikegami T, Peters CJ, Makino S (2005) Rift Valley fever virus nonstructural protein NSs promotes viral RNA replication and transcription in a minigenome system. J Virol 79:5606–5615

    Article  PubMed  CAS  Google Scholar 

  • 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 67:1396–1404

    PubMed  CAS  Google Scholar 

  • Jin H, Elliott RM (1993b) Non-viral sequences at the 5′ ends of Dugbe nairovirus S mRNAs. J Gen Virol 74(Pt 10):2293–2297

    Article  PubMed  CAS  Google Scholar 

  • Kainz M, Hilson P, Sweeney L, Derose E, German TL (2004) Interaction between tomato spotted wilt virus N protein monomers involves nonelectrostatic forces governed by multiple distinct regions in the primary structure. Phytopathology 94:759–765

    Article  PubMed  CAS  Google Scholar 

  • Kariwa H, Tanabe H, Mizutani T, Kon Y, Lokugamage K, Lokugamage N, Iwasa MA, Hagiya T, Araki K, Yoshimatsu K, Arikawa J, Takashima I (2003) Synthesis of Seoul virus RNA and structural proteins in cultured cells. Arch Virol 148:1671–1685

    Article  PubMed  CAS  Google Scholar 

  • Katz A, Freiberg AN, Backstrom V, Schulz AR, Mateos A, Holm L, Pettersson RF, Vaheri A, Flick R, Plyusnin A (2010) Oligomerization of Uukuniemi virus nucleocapsid protein. Virol J 7:187

    Article  PubMed  CAS  Google Scholar 

  • Kaukinen P, Koistinen V, Vapalahti O, Vaheri A, Plyusnin A (2001) Interaction between molecules of hantavirus nucleocapsid protein. J Gen Virol 82:1845–1853

    PubMed  CAS  Google Scholar 

  • Kaukinen P, Kumar V, Tulimaki K, Engelhardt P, Vaheri A, Plyusnin A (2004) Oligomerization of Hantavirus N protein: C-terminal alpha-helices interact to form a shared hydrophobic space. J Virol 78:13669–13677

    Article  PubMed  CAS  Google Scholar 

  • Kaukinen P, Vaheri A, Plyusnin A (2005) Hantavirus nucleocapsid protein: a multifunctional molecule with both housekeeping and ambassadorial duties. Arch Virol 150:1693–1713

    Article  PubMed  CAS  Google Scholar 

  • Kohl A, Dunn EF, Lowen AC, Elliott RM (2004) Complementarity, sequence and structural elements within the 3′ and 5′ non-coding regions of the Bunyamwera orthobunyavirus S segment determine promoter strength. J Gen Virol 85:3269–3278

    Article  PubMed  CAS  Google Scholar 

  • Kormelink R, van Poelwijk F, Peters D, Goldbach R (1992) Non-viral heterogeneous sequences at the 5′ ends of tomato spotted wilt virus mRNAs. J Gen Virol 73(Pt 8):2125–2128

    Article  PubMed  CAS  Google Scholar 

  • Kozak M, Shatkin AJ (1978) Migration of 40S ribosomal subunits on messenger RNA in the presence of edeine. J Biol Chem 253:6568–6577

    PubMed  CAS  Google Scholar 

  • 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(Pt 11):2615–2622

    PubMed  CAS  Google Scholar 

  • Kukkonen SK, Vaheri A, Plyusnin A (2005) L protein, the RNA-dependent RNA polymerase of Hantaviruses. Arch Virol 150:533–556

    Article  PubMed  CAS  Google Scholar 

  • Le May N, Dubaele S, Proietti De Santis L, Billecocq A, Bouloy M, Egly JM (2004) TFIIH transcription factor, a target for the Rift Valley hemorrhagic fever virus. Cell 116:541–550

    Article  PubMed  Google Scholar 

  • Le May N, Gauliard N, Billecocq A, Bouloy M (2005) The N terminus of Rift Valley fever virus nucleoprotein is essential for dimerization. J Virol 79:11974–11980

    Article  PubMed  CAS  Google Scholar 

  • Leonard VH, Kohl A, Osborne JC, McLees A, Elliott RM (2005) Homotypic interaction of Bunyamwera virus nucleocapsid protein. J Virol 79:13166–13172

    Article  PubMed  CAS  Google Scholar 

  • 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 69:3972–3979

    PubMed  CAS  Google Scholar 

  • Lowen AC, Boyd A, Fazakerley JK, Elliott RM (2005) Attenuation of bunyavirus replication by rearrangement of viral coding and noncoding sequences. J Virol 79:6940–6946

    Article  PubMed  CAS  Google Scholar 

  • Martin ML, Lindsey-Regnery H, Sasso DR, McCormick JB, Palmer E (1985) Distinction between Bunyaviridae genera by surface structure and comparison with Hantaan virus using negative stain electron microscopy. Arch Virol 86:17–28

    Article  PubMed  CAS  Google Scholar 

  • Mir MA, Panganiban AT (2004) Trimeric Hantavirus nucleocapsid protein binds specifically to the viral RNA panhandle. J Virol 78:8281–8288

    Article  PubMed  CAS  Google Scholar 

  • Mir MA, Panganiban AT (2005) The Hantavirus nucleocapsid protein recognizes specific features of the viral RNA panhandle and is altered in conformation upon RNA binding. J Virol 79:1824–1835

    Article  PubMed  CAS  Google Scholar 

  • Mir MA, Panganiban AT (2006a) The bunyavirus nucleocapsid protein is an RNA chaperone: possible roles in viral RNA panhandle formation and genome replication. RNA 12:272–282

    Article  PubMed  CAS  Google Scholar 

  • Mir MA, Panganiban AT (2006b) Characterization of the RNA chaperone activity of Hantavirus nucleocapsid protein. J Virol 80:6276–6285

    Article  PubMed  CAS  Google Scholar 

  • Mir MA, Panganiban AT (2008) A protein that replaces the entire cellular eIF4F complex. EMBO J 27:3129–3139

    Article  PubMed  CAS  Google Scholar 

  • Mir MA, Brown B, Hjelle B, Duran WA, Panganiban AT (2006) Hantavirus N protein exhibits genus-specific recognition of the viral RNA panhandle. J Virol 80:11283–11292

    Article  PubMed  CAS  Google Scholar 

  • Mir MA, Duran WA, Hjelle BL, Ye C, Panganiban AT (2008) Storage of cellular 5′ mRNA caps in P bodies for viral cap-snatching. Proc Natl Acad Sci USA 105:19294–19299

    Article  PubMed  CAS  Google Scholar 

  • Mir MA, Sheema S, Haseeb A, Haque A (2010) Hantavirus nucleocapsid protein has distinct m7G cap- and RNA-binding sites. J Biol Chem 285:11357–11368

    Article  PubMed  CAS  Google Scholar 

  • Mohamed NA (1981) Isolation and characterization of subviral structures from tomato spotted wilt virus. J Gen Virol 53:197–206

    Article  CAS  Google Scholar 

  • Mohl BP, Barr JN (2009) Investigating the specificity and stoichiometry of RNA binding by the nucleocapsid protein of Bunyamwera virus. RNA 15:391–399

    Article  PubMed  CAS  Google Scholar 

  • Obijeski JF, Bishop DH, Palmer EL, Murphy FA (1976) Segmented genome and nucleocapsid of La Crosse virus. J Virol 20:664–675

    PubMed  CAS  Google Scholar 

  • Obijeski JF, McCauley J, Skehel JJ (1980) Nucleotide sequences at the terminal of La Crosse virus RNAs. Nucleic Acids Res 8:2431–2438

    Article  PubMed  CAS  Google Scholar 

  • Ogg MM, Patterson JL (2007) RNA binding domain of Jamestown Canyon virus S segment RNAs. J Virol 81:13754–13760

    Article  PubMed  CAS  Google Scholar 

  • Ortega J, Martin-Benito J, Zurcher T, Valpuesta JM, Carrascosa JL, Ortin J (2000) Ultrastructural and functional analyses of recombinant influenza virus ribonucleoproteins suggest dimerization of nucleoprotein during virus amplification. J Virol 74:156–163

    Article  PubMed  CAS  Google Scholar 

  • Osborne JC, Elliott RM (2000) RNA binding properties of Bunyamwera virus nucleocapsid protein and selective binding to an element in the 5′ terminus of the negative-sense S segment. J Virol 74:9946–9952

    Article  PubMed  CAS  Google Scholar 

  • Overby AK, Popov V, Neve EP, Pettersson RF (2006) Generation and analysis of infectious virus-like particles of Uukuniemi virus (Bunyaviridae): a useful system for studying bunyaviral packaging and budding. J Virol 80:10428–10435

    Article  PubMed  CAS  Google Scholar 

  • Overby AK, Pettersson RF, Neve EP (2007) The glycoprotein cytoplasmic tail of Uukuniemi virus (Bunyaviridae) interacts with ribonucleoproteins and is critical for genome packaging. J Virol 81:3198–3205

    Article  PubMed  CAS  Google Scholar 

  • Overby AK, Pettersson RF, Grunewald K, Huiskonen JT (2008) Insights into bunyavirus architecture from electron cryotomography of Uukuniemi virus. Proc Natl Acad Sci USA 105:2375–2379

    Article  PubMed  CAS  Google Scholar 

  • Panganiban AT, Mir MA (2009) Bunyavirus N: eIF4F surrogate and cap-guardian. Cell Cycle 8:1332–1337

    Article  PubMed  CAS  Google Scholar 

  • Patterson JL, Kolakofsky D (1984) Characterization of La Crosse virus small-genome transcripts. J Virol 49:680–685

    PubMed  CAS  Google Scholar 

  • Patterson JL, Holloway B, Kolakofsky D (1984) La Crosse virions contain a primer-stimulated RNA polymerase and a methylated cap-dependent endonuclease. J Virol 52:215–222

    PubMed  CAS  Google Scholar 

  • Pettersson RF, von Bonsdorff CH (1975) Ribonucleoproteins of Uukuniemi virus are circular. J Virol 15:386–392

    PubMed  CAS  Google Scholar 

  • Plassmeyer ML, Soldan SS, Stachelek KM, Martin-Garcia J, Gonzalez-Scarano F (2005) California serogroup Gc (G1) glycoprotein is the principal determinant of pH-dependent cell fusion and entry. Virology 338:121–132

    Article  PubMed  CAS  Google Scholar 

  • Plassmeyer ML, Soldan SS, Stachelek KM, Roth SM, Martin-Garcia J, Gonzalez-Scarano F (2007) Mutagenesis of the La Crosse Virus glycoprotein supports a role for Gc (1066–1087) as the fusion peptide. Virology 358:273–282

    Article  PubMed  CAS  Google Scholar 

  • Raju R, Kolakofsky D (1989) The ends of La Crosse virus genome and antigenome RNAs within nucleocapsids are base paired. J Virol 63:122–128

    PubMed  CAS  Google Scholar 

  • Raymond DD, Piper ME, Gerrard SR, Smith JL (2010) Structure of the Rift Valley fever virus nucleocapsid protein reveals another architecture for RNA encapsidation. Proc Natl Acad Sci USA 107:11769–11774

    Article  PubMed  CAS  Google Scholar 

  • Reguera J, Weber F, Cusack S (2010) Bunyaviridae RNA polymerases (L-protein) have an N-terminal, influenza-like endonuclease domain, essential for viral cap-dependent transcription. PLoS Pathog 6:e1001101

    Article  PubMed  CAS  Google Scholar 

  • Rodgers JW, Zhou Q, Green TJ, Barr JN, Luo M (2006) Purification, crystallization and preliminary X-ray crystallographic analysis of the nucleocapsid protein of Bunyamwera virus. Acta Crystallogr Sect F Struct Biol Cryst Commun 62:361–364

    Article  PubMed  CAS  Google Scholar 

  • Roland KL, Liu CG, Turnbough CL Jr (1988) Role of the ribosome in suppressing transcriptional termination at the pyrBI attenuator of Escherichia coli K-12. Proc Natl Acad Sci USA 85:7149–7153

    Article  PubMed  CAS  Google Scholar 

  • Ronka H, Hilden P, Von Bonsdorff CH, Kuismanen E (1995) Homodimeric association of the spike glycoproteins G1 and G2 of Uukuniemi virus. Virology 211:241–250

    Article  PubMed  CAS  Google Scholar 

  • Rossier C, Patterson J, Kolakofsky D (1986) La Crosse virus small genome mRNA is made in the cytoplasm. J Virol 58:647–650

    PubMed  CAS  Google Scholar 

  • Rudolph MG, Kraus I, Dickmanns A, Eickmann M, Garten W, Ficner R (2003) Crystal structure of the Borna disease virus nucleoprotein. Structure 11:1219–1226

    Article  PubMed  CAS  Google Scholar 

  • Schmaljohn CS, Nichol ST (2007) Bunyaviridae. In: Knipe D, Howley P (eds) Fields virology, vol 2. Lippincott Williams & Wilkins, Philadelphia, PA, pp 1741–1790

    Google Scholar 

  • Severson WE, Xu X, Jonsson CB (2001) cis-Acting signals in encapsidation of Hantaan virus S-segment viral genomic RNA by its N protein. J Virol 75:2646–2652

    Article  PubMed  CAS  Google Scholar 

  • Severson W, Xu X, Kuhn M, Senutovitch N, Thokala M, Ferron F, Longhi S, Canard B, Jonsson CB (2005) Essential amino acids of the Hantaan virus N protein in its interaction with RNA. J Virol 79:10032–10039

    Article  PubMed  CAS  Google Scholar 

  • Sherman MB, Freiberg AN, Holbrook MR, Watowich SJ (2009) Single-particle cryo-electron microscopy of Rift Valley fever virus. Virology 387:11–15

    Article  PubMed  CAS  Google Scholar 

  • Shi X, Kohl A, Li P, Elliott RM (2007) Role of the cytoplasmic tail domains of Bunyamwera orthobunyavirus glycoproteins Gn and Gc in virus assembly and morphogenesis. J Virol 81:10151–10160

    Article  PubMed  CAS  Google Scholar 

  • Simons JF, Pettersson RF (1991) Host-derived 5′ ends and overlapping complementary 3′ ends of the two mRNAs transcribed from the ambisense S segment of Uukuniemi virus. J Virol 65:4741–4748

    PubMed  CAS  Google Scholar 

  • Snippe M, Borst JW, Goldbach R, Kormelink R (2005) The use of fluorescence microscopy to visualise homotypic interactions of tomato spotted wilt virus nucleocapsid protein in living cells. J Virol Methods 125:15–22

    Article  PubMed  CAS  Google Scholar 

  • Snippe M, Willem Borst J, Goldbach R, Kormelink R (2007) Tomato spotted wilt virus Gc and N proteins interact in vivo. Virology 357:115–123

    Article  PubMed  CAS  Google Scholar 

  • Tawar RG, Duquerroy S, Vonrhein C, Varela PF, Damier-Piolle L, Castagne N, MacLellan K, Bedouelle H, Bricogne G, Bhella D, Eleouet JF, Rey FA (2009) Crystal structure of a nucleocapsid-like nucleoprotein-RNA complex of respiratory syncytial virus. Science 326:1279–1283

    Article  PubMed  CAS  Google Scholar 

  • Tischler ND, Gonzalez A, Perez-Acle T, Rosemblatt M, Valenzuela PD (2005) Hantavirus Gc glycoprotein: evidence for a class II fusion protein. J Gen Virol 86:2937–2947

    Article  PubMed  CAS  Google Scholar 

  • 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 96:55–60

    Article  PubMed  CAS  Google Scholar 

  • Vialat P, Bouloy M (1992) Germiston virus transcriptase requires active 40 S ribosomal subunits and utilizes capped cellular RNAs. J Virol 66:685–693

    PubMed  CAS  Google Scholar 

  • Walter CT, Barr JN (2010) Bunyamwera virus can repair both insertions and deletions during RNA replication. RNA 16:1138–1145

    Article  PubMed  CAS  Google Scholar 

  • Walter CT, Bento DF, Alonso AG, Barr JN (2011) Amino acid changes within the Bunyamwera virus nucleocapsid protein differentially affect the mRNA transcription and RNA replication activities of assembled ribonucleoprotein templates. J Gen Virol 92:80–84

    Article  PubMed  CAS  Google Scholar 

  • Wang GJ, Hewlett M, Chiu W (1991) Structural variation of La Crosse virions under different chemical and physical conditions. Virology 184:455–459

    Article  PubMed  CAS  Google Scholar 

  • Weber F, Dunn EF, Bridgen A, Elliott RM (2001) The Bunyamwera virus nonstructural protein NSs inhibits viral RNA synthesis in a minireplicon system. Virology 281:67–74

    Article  PubMed  CAS  Google Scholar 

  • Xu X, Severson W, Villegas N, Schmaljohn CS, Jonsson CB (2002) The RNA binding domain of the Hantaan virus N protein maps to a central, conserved region. J Virol 76:3301–3308

    Article  PubMed  CAS  Google Scholar 

  • Ye Q, Krug RM, Tao YJ (2006) The mechanism by which influenza A virus nucleoprotein forms oligomers and binds RNA. Nature 444:1078–1082

    Article  PubMed  CAS  Google Scholar 

  • Yuan P, Bartlam M, Lou Z, Chen S, Zhou J, He X, Lv Z, Ge R, Li X, Deng T, Fodor E, Rao Z, Liu Y (2009) Crystal structure of an avian influenza polymerase PA(N) reveals an endonuclease active site. Nature 458:909–913

    Article  PubMed  CAS  Google Scholar 

  • Zamoto-Niikura A, Terasaki K, Ikegami T, Peters CJ, Makino S (2009) Rift Valley fever virus L protein forms a biologically active oligomer. J Virol 83:12779–12789

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Aaron Collier for critical reading of the manuscript. The authors are supported by grants C-1565 from the Welch Foundation and AI077785 from the National Institutes of Health.

Author information

Authors and Affiliations

  1. Department of Biochemistry and Cell Biology, Rice University, 6100 Main Street, MS140, Houston, TX, 77005, USA

    Tom S. Y. Guu, Wenjie Zheng & Yizhi J. Tao

Authors
  1. Tom S. Y. Guu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wenjie Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yizhi J. Tao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yizhi J. Tao .

Editor information

Editors and Affiliations

  1. Dept. Biological Sciences, Purdue University, W. State St. 915, West Lafayette, 47907-2054, Indiana, USA

    Michael G. Rossmann

  2. Dept. Biology, Catholic University of America, Washington, 20064, District of Columbia, USA

    Venigalla B. Rao

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Guu, T.S.Y., Zheng, W., Tao, Y.J. (2012). Bunyavirus: Structure and Replication. In: Rossmann, M., Rao, V. (eds) Viral Molecular Machines. Advances in Experimental Medicine and Biology, vol 726. Springer, Boston, MA. https://doi.org/10.1007/978-1-4614-0980-9_11

Download citation

Publish with us

Policies and ethics

Search

Navigation