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Particle Assembly and Genome Packaging

  • Chapter
Foamy Viruses

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 277))

Abstract

Foamy virus (FV) replication is distinct from that of all other retroviruses in many respects, including viral assembly. In fact, the viral assembly pathway is rather similar to that of hepadnaviruses such as hepatitis B virus. Foamy virus Gag does not contain landmark retroviral assembly domains such as the major homology region, Cys-His boxes, or a defined M domain Like hepadnaviruses, the FV Gag protein is not cleaved and contains arginine-rich regions at the carboxyl terminus. In addition, egress of FV particles requires presence of the envelope glycoproteins Finally, the cis-acting sequences in the FV genome required for genome incorporation, although poorly defined, differ in location from other retroviruses.

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References

  • Baldwin DN, Linial ML (1998) The roles of Pol and Env in the assembly pathway of human foamy virus. J Virol 72:3658–3665

    PubMed  CAS  Google Scholar 

  • Baldwin DN, Linial ML (1999) Proteolytic activity, the carboxyl terminus of Gag, and the primer binding site are not required for Pol incorporation into foamy virus particles. J Virol 73:6387–6393

    PubMed  CAS  Google Scholar 

  • Banks JD, Beemon KL, Linial ML (1997) RNA regulatory elements in the genomes of simple retroviruses. Sem Virol 8:194–204

    CAS  Google Scholar 

  • Banks JD, Linial ML (2000) Secondary structure analysis of a minimal avian leukosis-sarcoma virus packaging signal. J Virol 74:464

    Article  Google Scholar 

  • Bennett RP, Nelle TD, Wills JW (1993) Functional chimeras of the Rous sarcoma vi-rus and human immunodeficiency virus Gag proteins. J Virol 67:6487–6498

    PubMed  CAS  Google Scholar 

  • Berkowitz R, Fisher J, Goff SP (1996) RNA packaging. Curr Top Microbiol Immunol 214:177–218

    Google Scholar 

  • Bodem J, Löchelt M, Winkler I, Flower RP, Delius H, Flügel RM (1996) Characteriza-tion of the spliced pol transcript of feline foamy virus—the splice acceptor site of the pol transcript is located in gag of foamy viruses. J Virol 70:9024–9027

    PubMed  CAS  Google Scholar 

  • Boucher B, Wynne SA, Crowther RA (1997) Determination of the fold of the core protein of hepatitis B virus by electron cryomicroscopy. Nature 386:88–91

    Article  Google Scholar 

  • Bowzard JB, Bennett RP, Krisina NK, Ernst SM, Rein A, Wills JW (1998) Importance of basic residues in the nucleocapsid sequence for retrovirus gag assembly and complementation rescue. J Virol 72:9034–9044

    PubMed  CAS  Google Scholar 

  • Campbell S, Vogt SM (1995) Self-assembly in vitro of purified CA-NC proteins from Rous sarcoma virus and human immunodeficiency virus type 1. J Virol 69:6487–6497

    Google Scholar 

  • Cimarelli A, Luban J (2000) Human immunodeficiency virus type 1 virion density is not determined by nucleocapsid basic residues. J Virol 74:6734–6740

    Article  PubMed  CAS  Google Scholar 

  • Craven RC, Leure-duPree RE, Weldon RA Jr, Wills JW (1995) Genetic analysis of the major homology region of the Rous sarcoma virus Gag protein. J Virol 69:4213–4227

    PubMed  CAS  Google Scholar 

  • De Guzman RN, Wu ZR, Stalling CC, Pappalardo L, Borer PN, Summers. FM (1998) Structure of the HIV-1 nucleocapsid protein bound to the SL3 psi-RNA recognition element. Science 279:384–388

    Article  PubMed  Google Scholar 

  • Dermott E, Clarke JK, Samuels J (1971) The morphogenesis and classification of bovine syncytial virus. J Gen Virol 12: 105–119

    Article  PubMed  CAS  Google Scholar 

  • Eastman SW, Linial ML (2001) Identification of a conserved residue of foamy virus Gag required for intracellular capsid assembly. J Virol 75:6857–6864

    Article  PubMed  CAS  Google Scholar 

  • Enssle J, Jordan I, Mauer B, Rethwilm A (1996) Foamy virus reverse transcriptase is expressed independently from the Gag protein. Proc Natl Acad Sci USA 93:4137–4141

    Google Scholar 

  • Erlwein O, Bieniasz PD, McClure MO (1998) Sequences in pol are required for transfer of human foamy virus-based vectors. J Virol 72:5510–5516

    PubMed  CAS  Google Scholar 

  • Fischer N, Heinkelein M, Lindemann D, Enssle J, Baum C, Werder E, Zentgraf H, Müller JG, Rethwilm A (1998) Foamy virus particle formation. J Virol 72:1610–1615

    Google Scholar 

  • Ganem D (1996) Hepadnaviridae and their replication. In: Fields BN, Knipe DM, Howley PM (eds) Fields Virology. Lippincott-Raven, Philadelphia

    Google Scholar 

  • Gamier L, Parent LJ, Rovinski B, Cao SX, Wills JW (1999) Identification of retroviral late domains as determinants of particle size. J Virol 73:2309–2320

    Google Scholar 

  • Garrus JE, von Schwedler UK, Pornillos OW, Morham SG, Zavitz KH, Wang HE, Wettstein DA,.Stray KM, Cote M, Rich RL, Myszka DG, Sundquist WI (2001) Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 107:55–65

    CAS  Google Scholar 

  • Goepfert PA, Shaw KE, Bansal A, Wang G, Edwards RH, Mulligan MJ (1999) An endoplasmic reticulum retrieval signal partitions human foamy virus maturation to intracytoplasmic membranes. J Virol 73:7210–7217

    PubMed  CAS  Google Scholar 

  • Goepfert PA, Shaw KL, Ritter GD, Mulligan MJ (1997) A sorting motif localizes the foamy virus glycoprotein to the endoplasmic reticulum. J Virol 71:778–784

    PubMed  CAS  Google Scholar 

  • Hatton T, Zhou S, Standring DN (1992) RNA- and DNA- binding activities in hepatitis B virus capsid protein: a model for their roles in virus replication. J Virol 66:5232–5241

    PubMed  CAS  Google Scholar 

  • Heinkelein M, Pietschmann T, Jarmy G, Dressler M, Imrich H, Thurow J, Lindemann D, Bock M, Moebes A, Roy J, Herchenröder O, Rethwilm A (2000a) Efficient intracellular retrotransposition of an exogenous primate retrovirus genome. EMBO J 19:3436–3445

    Article  PubMed  CAS  Google Scholar 

  • Heinkelein M, Leurs C, Rammling M, Peters K, Hanenberg H, Rethwilm A (2002) Pregenomic RNA is required for efficient incorporation of Pol polyprotein into foamy virus capsids. J Virol 76 (in press)

    Google Scholar 

  • Heinkelein M, Schmidt M, Fischer N, Moebes N, Lindemann D, Enssle J, Rethwilm A (1998) Characterization of a cis-acting sequence in the pol region required to transfer human foamy virus vectors. J Virol 72:6307–6314

    PubMed  CAS  Google Scholar 

  • Heinkelein M, Thurow J, Dressler M, Imrich H, Neumann-Haefelin D, McClure MO, Rethwilm A (2000b) Complex effects of deletions in the 5’ untranslated region of primate foamy virus on viral gene expression and RNA packaging. J Virol 74:3141–3148

    Article  PubMed  CAS  Google Scholar 

  • Holzschu DL, Delaney MA, Renshaw RW, Casey JW (1998) The nucleotide sequence and spliced pol mRNA levels of the nonprimate spumavirus bovine foamy virus. J Virol 72:2177–2182

    PubMed  CAS  Google Scholar 

  • Jacks T, (1990) Translational suppression in gene expression in retroviruses and retrotransposons. Curr Top Micrbiol Immunol 157:93–124

    Article  CAS  Google Scholar 

  • Jordan I, Enssle J, Güttler E, Mauer B, Rethwilm A (1996) Expression of human foamy virus reverse transcriptase involves a spliced pol mRNA. Virology 224:314319

    Google Scholar 

  • Karpel RL, Henderson LE, Oroszlan S (1987) Interactions of retroviral structural proteins with single-stranded nucleic acids. J Biol Chem 262:4961–4967

    PubMed  CAS  Google Scholar 

  • Khan R, Giedroc DP (1992) Recombinant human immunodeficiency virus type 1 nucleocapsid (NCp7) protein unwinds tRNA. J Biol Chem 267:6689–6695

    PubMed  CAS  Google Scholar 

  • Konvalinka J, Löchelt M, Zentgraf H, Flügel RM, Kräusslich H-G (1995) Active spumavirus proteinase is essential for virus infectivity but not for formation of the Pol polyprotein. J Virol 69:7264–7268

    PubMed  CAS  Google Scholar 

  • Lecellier CH, Neves M, Giron M-L, Tobaly-Tapiero J, Saib A (2002) Further characterization of equine foamy virus reveals unusual features among the foamy viruses. J Virol 76:7220–7227

    Article  PubMed  CAS  Google Scholar 

  • Lindemann D, Bock M, Schweizer M, Rethwilm A (1997) Efficient pseudotyping of murine leukemia virus particles with chimeric human foamy virus envelope proteins. J Virol 71:4815–4820

    PubMed  CAS  Google Scholar 

  • Lindemann D, Pietschmann T, Picard-Mareau M, Berg A, Heinkelein M, Thurow J, Knaus P, Zentgraf H, Rethwilm A (2001) A particle associated glycoprotein signal peptide essential for virus maturation and infectivity. J Virol 75:5762–5771

    Article  PubMed  CAS  Google Scholar 

  • Löchelt M, Flügel RM (1996) The human foamy virus pol gene is expressed as a Pro-Pol polyprotein and not as a Gag-Pol fusion protein. J Virol 70:1033–1040

    PubMed  Google Scholar 

  • Mammano F, Ohagen A, Hoglund S, Göttlinger HG (1994) Role of the major homology region of human immunodeficiency virus type 1 in virion morphogenesis. J Virol 68:4927–4936

    PubMed  CAS  Google Scholar 

  • Martin-Serrano J, Zang T, Bieniasz PD (2001) HIV-1 and Ebola virus encode small peptide motifs that recruit Tsg101 to sites of particle assembly to facilitate egress. Nature Med 7:1313–1319

    Article  PubMed  CAS  Google Scholar 

  • Meiering CD, Comstock KE, Linial ML (2000) Human foamy virus multiple integra-tions in persistently infected human erythroleukemia cells. J Virol 74:1718–1726

    Article  PubMed  CAS  Google Scholar 

  • Nassal M (1992) The arginine-rich domain of the hepatitis B virus core protein is required for pregenome encapsidation and productive viral positive-strand DNA synthesis but not for virus assembly. J Virol 66:4107–4116

    PubMed  CAS  Google Scholar 

  • Petit C, Giron M-L, Tobaly-Tapiero J, Bittoun P, Real E, Jacob Y, Tordo N, de Thé H, Saib A (2003) Targeting of incoming retroviral Gag to the centrosome involves a direct interaction with dynein LC8. J Virol (in press)

    Google Scholar 

  • Raux H, Flamand A, and Blondel D (2000) Interaction of the rabies virus P protein with the LC8 dynein light chain. J Virol 74:10212–10216

    Article  PubMed  CAS  Google Scholar 

  • Rein A. McClure MR, Rice NR, Luftig RB, Schultz AM (1986) Myristylation site in Pr65gag is essential for virus particle formation by Moloney murine leukemia virus. Proc Nail Acad Sci USA 83:7246–7250

    Article  Google Scholar 

  • Renshaw RW, Casey JW (1994) Transcriptional mapping of the 3’ end of the bovine syncytial virus genome. J Virol 68: 1021–1028

    PubMed  CAS  Google Scholar 

  • Rhee SS, Hunter E (1987) Myristylation is required for intracellular transport but not for assembly of D-type retrovirus capsids. J Virol 61:1045–1053

    PubMed  CAS  Google Scholar 

  • Rhee SS, Hunter E (1990) A single amino acid substitution within the matrix protein of a type D retrovirus converts its morphogenesis to that of a type C retrovirus. Cell 63:77–86

    Article  PubMed  CAS  Google Scholar 

  • Russell RA, Zeng Y, Erlwein O, Cullen BR, McClure MO (2001) The R region found in the human foamy virus long terminal repeat is critical for both gag and pol protein expression. J Virol 75:6817–6824

    Article  PubMed  CAS  Google Scholar 

  • Saib A, Puvion-Dutilleul F, Schmid M, Perks J, de Thé H (1997) Nuclear targeting of incoming human foamy virus gag proteins involves a centriolar step. J Virol 71:1155–1161

    PubMed  CAS  Google Scholar 

  • Sakalian M, Hunter E (1999) Separate assembly and transport domains within the Gag precursor of Mason-Pfizer monkey virus. J Virol 73:8073–8082

    PubMed  CAS  Google Scholar 

  • Sandefur S, Smith RM, Varthakavi V, Spearman P (2000) Mapping and characterization of the N-terminal I domain of human immunodeficiency virus Type 1 Pr55(Gag). J Virol 74:7238–7249

    Article  PubMed  CAS  Google Scholar 

  • Schliephake AW, Rethwilm A (1994) Nuclear localization of foamy virus Gag precursor protein. J Virol 68:4946–4954

    PubMed  CAS  Google Scholar 

  • Spearman P, Wang JJ, van der Heyden N, Ratner L (1994) Identification of human immunodeficiency virus type 1 Gag protein domains essential to membrane binding and particle assembly. J Virol 68:3232–3242

    PubMed  CAS  Google Scholar 

  • Swanstrom R, Wills JW (1997) Synthesis, assembly and processing of viral proteins. In: Coffin JM, Hughes SH, Varmus HE (eds) Retroviruses. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Tobaly-Tapiero J, Bittoun P, Neves M, Guillemin MC, Lecellier CH, Puvion-Dutilleul F, Gicquel B, Zientara S, Giron M-L, de Thé H, Saïb A (2000) Isolation and characterization of an equine foamy virus. J Virol 74:4064–4073

    Article  PubMed  CAS  Google Scholar 

  • VerPlank L, Bouamr F, LaGrassa TJ, Agresta B, Kikonyogo A, Leis J, Carter CA (2001) Tsg101, a homologue of ubiquitin-conjugating (E2) enzymes, binds the L domain in HIV type 1 Pr55(Gag). Proc Natl Acad Sci USA 98:7724–7729

    Article  PubMed  CAS  Google Scholar 

  • Wilk T, Geiselhart V, Frech M, SD, Flügel RM, Lö M (2001) Specific interaction of a novel foamy virus Env leader protein with the N-terminal Gag domain. J Virol 75:7995–8007

    Article  PubMed  CAS  Google Scholar 

  • Wynne SA, Crowther RA, Leslie AG (1999) The crystal structure of the human hepatitis B virus capsid. Mol Cell 3:771–780

    Article  PubMed  CAS  Google Scholar 

  • Yu SF, Baldwin DN, Gwynn SR, Yendapalli S, Linial ML (1996a) Human foamy virus replication—a pathway distinct from that of retroviruses and hepadnaviruses. Science 271:1579–1582

    Article  PubMed  CAS  Google Scholar 

  • Yu SF, Edelmann K, Strong RK, Moebes A, Rethwilm A, Linial ML (1996b) The carboxyl terminus of the human foamy virus gag protein contains separable nucleic acid binding and nuclear transport domains. J Virol 70:8255–8262

    PubMed  CAS  Google Scholar 

  • Yu SF, Linial ML (1993) Analysis of the role of the bel and bet open reading frames of human foamy virus by using a new quantitative assay. J Virol 67:6618–6624

    PubMed  CAS  Google Scholar 

  • Yuan B, Campbell S, Bacharach E, Rein A, Goff SP (2000) Infectivity of moloney murine leukemia virus defective in late assembly events is restored by late assembly domains of other retroviruses. J Virol 74:7250–7260

    Article  PubMed  CAS  Google Scholar 

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Linial, M.L., Eastman, S.W. (2003). Particle Assembly and Genome Packaging. In: Rethwilm, A. (eds) Foamy Viruses. Current Topics in Microbiology and Immunology, vol 277. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-55701-9_4

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  • DOI: https://doi.org/10.1007/978-3-642-55701-9_4

  • Publisher Name: Springer, Berlin, Heidelberg

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