Advertisement

Particle Assembly and Genome Packaging

Chapter
Part of the Current Topics in Microbiology and Immunology book series (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.

Keywords

Human Immunodeficiency Virus Type Rous Sarcoma Virus Foamy Virus Prototypic Foamy Virus Bovine Foamy Virus 
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. Baldwin DN, Linial ML (1998) The roles of Pol and Env in the assembly pathway of human foamy virus. J Virol 72:3658–3665PubMedGoogle Scholar
  2. 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 73:6387–6393PubMedGoogle Scholar
  3. Banks JD, Beemon KL, Linial ML (1997) RNA regulatory elements in the genomes of simple retroviruses. Sem Virol 8:194–204Google Scholar
  4. Banks JD, Linial ML (2000) Secondary structure analysis of a minimal avian leukosis-sarcoma virus packaging signal. J Virol 74:464CrossRefGoogle Scholar
  5. Bennett RP, Nelle TD, Wills JW (1993) Functional chimeras of the Rous sarcoma vi-rus and human immunodeficiency virus Gag proteins. J Virol 67:6487–6498PubMedGoogle Scholar
  6. Berkowitz R, Fisher J, Goff SP (1996) RNA packaging. Curr Top Microbiol Immunol 214:177–218Google Scholar
  7. 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 70:9024–9027PubMedGoogle Scholar
  8. Boucher B, Wynne SA, Crowther RA (1997) Determination of the fold of the core protein of hepatitis B virus by electron cryomicroscopy. Nature 386:88–91CrossRefGoogle Scholar
  9. 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 72:9034–9044PubMedGoogle Scholar
  10. 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 69:6487–6497Google Scholar
  11. Cimarelli A, Luban J (2000) Human immunodeficiency virus type 1 virion density is not determined by nucleocapsid basic residues. J Virol 74:6734–6740PubMedCrossRefGoogle Scholar
  12. 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 69:4213–4227PubMedGoogle Scholar
  13. 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 279:384–388PubMedCrossRefGoogle Scholar
  14. Dermott E, Clarke JK, Samuels J (1971) The morphogenesis and classification of bovine syncytial virus. J Gen Virol 12: 105–119PubMedCrossRefGoogle Scholar
  15. Eastman SW, Linial ML (2001) Identification of a conserved residue of foamy virus Gag required for intracellular capsid assembly. J Virol 75:6857–6864PubMedCrossRefGoogle Scholar
  16. 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 93:4137–4141Google Scholar
  17. Erlwein O, Bieniasz PD, McClure MO (1998) Sequences in pol are required for transfer of human foamy virus-based vectors. J Virol 72:5510–5516PubMedGoogle Scholar
  18. 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 72:1610–1615Google Scholar
  19. Ganem D (1996) Hepadnaviridae and their replication. In: Fields BN, Knipe DM, Howley PM (eds) Fields Virology. Lippincott-Raven, PhiladelphiaGoogle Scholar
  20. Gamier L, Parent LJ, Rovinski B, Cao SX, Wills JW (1999) Identification of retroviral late domains as determinants of particle size. J Virol 73:2309–2320Google Scholar
  21. 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 107:55–65Google Scholar
  22. 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 73:7210–7217PubMedGoogle Scholar
  23. Goepfert PA, Shaw KL, Ritter GD, Mulligan MJ (1997) A sorting motif localizes the foamy virus glycoprotein to the endoplasmic reticulum. J Virol 71:778–784PubMedGoogle Scholar
  24. 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 66:5232–5241PubMedGoogle Scholar
  25. 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 19:3436–3445PubMedCrossRefGoogle Scholar
  26. 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
  27. 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 72:6307–6314PubMedGoogle Scholar
  28. 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 74:3141–3148PubMedCrossRefGoogle Scholar
  29. 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 72:2177–2182PubMedGoogle Scholar
  30. Jacks T, (1990) Translational suppression in gene expression in retroviruses and retrotransposons. Curr Top Micrbiol Immunol 157:93–124CrossRefGoogle Scholar
  31. Jordan I, Enssle J, Güttler E, Mauer B, Rethwilm A (1996) Expression of human foamy virus reverse transcriptase involves a spliced pol mRNA. Virology 224:314319Google Scholar
  32. Karpel RL, Henderson LE, Oroszlan S (1987) Interactions of retroviral structural proteins with single-stranded nucleic acids. J Biol Chem 262:4961–4967PubMedGoogle Scholar
  33. Khan R, Giedroc DP (1992) Recombinant human immunodeficiency virus type 1 nucleocapsid (NCp7) protein unwinds tRNA. J Biol Chem 267:6689–6695PubMedGoogle Scholar
  34. 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 69:7264–7268PubMedGoogle Scholar
  35. 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 76:7220–7227PubMedCrossRefGoogle Scholar
  36. 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 71:4815–4820PubMedGoogle Scholar
  37. 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 75:5762–5771PubMedCrossRefGoogle Scholar
  38. 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 70:1033–1040PubMedGoogle Scholar
  39. 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 68:4927–4936PubMedGoogle Scholar
  40. 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 7:1313–1319PubMedCrossRefGoogle Scholar
  41. Meiering CD, Comstock KE, Linial ML (2000) Human foamy virus multiple integra-tions in persistently infected human erythroleukemia cells. J Virol 74:1718–1726PubMedCrossRefGoogle Scholar
  42. 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 66:4107–4116PubMedGoogle Scholar
  43. 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
  44. Raux H, Flamand A, and Blondel D (2000) Interaction of the rabies virus P protein with the LC8 dynein light chain. J Virol 74:10212–10216PubMedCrossRefGoogle Scholar
  45. 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 83:7246–7250CrossRefGoogle Scholar
  46. Renshaw RW, Casey JW (1994) Transcriptional mapping of the 3’ end of the bovine syncytial virus genome. J Virol 68: 1021–1028PubMedGoogle Scholar
  47. Rhee SS, Hunter E (1987) Myristylation is required for intracellular transport but not for assembly of D-type retrovirus capsids. J Virol 61:1045–1053PubMedGoogle Scholar
  48. 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 63:77–86PubMedCrossRefGoogle Scholar
  49. 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 75:6817–6824PubMedCrossRefGoogle Scholar
  50. 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 71:1155–1161PubMedGoogle Scholar
  51. Sakalian M, Hunter E (1999) Separate assembly and transport domains within the Gag precursor of Mason-Pfizer monkey virus. J Virol 73:8073–8082PubMedGoogle Scholar
  52. 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 74:7238–7249PubMedCrossRefGoogle Scholar
  53. Schliephake AW, Rethwilm A (1994) Nuclear localization of foamy virus Gag precursor protein. J Virol 68:4946–4954PubMedGoogle Scholar
  54. 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 68:3232–3242PubMedGoogle Scholar
  55. 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 YorkGoogle Scholar
  56. 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 74:4064–4073PubMedCrossRefGoogle Scholar
  57. 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 98:7724–7729PubMedCrossRefGoogle Scholar
  58. 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 75:7995–8007PubMedCrossRefGoogle Scholar
  59. Wynne SA, Crowther RA, Leslie AG (1999) The crystal structure of the human hepatitis B virus capsid. Mol Cell 3:771–780PubMedCrossRefGoogle Scholar
  60. 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 271:1579–1582PubMedCrossRefGoogle Scholar
  61. 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 70:8255–8262PubMedGoogle Scholar
  62. 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 67:6618–6624PubMedGoogle Scholar
  63. 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 74:7250–7260PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2003

Authors and Affiliations

  1. 1.Division of Basic Sciences A3–015Fred Hutchinson Cancer Research CenterSeattleUSA

Personalised recommendations