Determination of the protease cleavage site repertoire-The RNase H but not the RT domain is essential for foamy viral protease activity

Virology

Volumn 454-455, Issue 1, 2014, Pages 145-156

  Spannaus, Ralf ^a   Bodem, Jochen ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Cleavage sites; Foamy virus; Protease; RNase H

Indexed keywords

INTEGRASE; PROTEINASE; RIBONUCLEASE H; RNA DIRECTED DNA POLYMERASE; VIRUS ANTIGEN; VIRUS PROTEIN;

ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; CORRELATIONAL STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN IMMUNODEFICIENCY VIRUS 1; LENTIVIRINAE; MOLONEY LEUKEMIA ONCOVIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; RNA ANALYSIS; RNA SEQUENCE; SEQUENCE ANALYSIS; SITE DIRECTED MUTAGENESIS; SPUMA VIRUS; VIRUS INFECTIVITY;

CLEAVAGE SITES; FOAMY VIRUS; PROTEASE; RNASE H;

ASPARTIC ACID ENDOPEPTIDASES; PROTEIN STRUCTURE, TERTIARY; RIBONUCLEASE H; RNA-DIRECTED DNA POLYMERASE; SPUMAVIRUS;

EID: 84895189773     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2014.02.013     Document Type: Article

References (48)

1. Adachi A., Gendelman H.E., Koenig S., Folks T., Willey R., Rabson A., Martin M.A. Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J. Virol. 1986, 59:284-291.
2. Baldwin D.N., Linial M.L. Proteolytic activity, the carboxy terminus of Gag, and the primer binding site are not required for Pol incorporation into foamy virus particles. J Virol 1999, 73:6387-6393.
3. Bodem J. Regulation of foamy viral transcription and RNA export. Adv. Virus Res. 2011, 81:1-31.
4. Bodem J., Löchelt M., Winkler I., Flower R.P., Delius H., Flügel R.M. Characterization 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. 1996, 70:9024-9027.
5. Cartellieri M., Rudolph W., Herchenröder O., Lindemann D., Rethwilm A. Determination of the relative amounts of Gag and Pol proteins in foamy virus particles. Retrovirology 2005, 2:44.
6. Cígler P., Kozísek M., Rezácová P., Brynda J., Otwinowski Z., Pokorná J., Plesek J., Grüner B., Dolecková-Maresová L., Mása M., Sedlácek J., Bodem J., Kräusslich H., Král V., Konvalinka J. From nonpeptide toward noncarbon protease inhibitors: metallacarboranes as specific and potent inhibitors of HIV protease. Proc. Natl. Acad. Sci. USA 2005, 102:15394-15399.
7. Dettenhofer M., Yu X.F. Highly purified human immunodeficiency virus type 1 reveals a virtual absence of Vif in virions. J. Virol. 1999, 73:1460-1467.
8. Enssle J., Fischer N., Moebes A., Mauer B., Smola U., Rethwilm A. Carboxy-terminal cleavage of the human foamy virus Gag precursor molecule is an essential step in the viral life cycle. J. Virol. 1997, 71:7312-7317.
9. Fenyöfalvi G., Bagossi P., Copeland T.D., Oroszlan S., Boross P., Tozser J. Expression and characterization of human foamy virus proteinase. FEBS Lett. 1999, 462:397-401.
10. Hartl M.J., Bodem J., Jochheim F., Rethwilm A., Rösch P., Wöhrl B.M. Regulation of Foamy virus protease activity by viral RNA-a novel and unique mechanism among retroviruses. J. Virol. 2011, 85:4462-4469.
11. Hartl M.J., Schweimer K., Reger M.H., Schwarzinger S., Bodem J., Rösch P., Wöhrl B.M. Formation of transient dimers by a retroviral protease. Biochem. J. 2010, 427:197-203.
12. Hartl M.J., Wöhrl B.M., Rösch P., Schweimer K. The solution structure of the simian foamy virus protease reveals a monomeric protein. J. Mol. Biol. 2008, 381:141-149.
13. Heinkelein M., Dressler M., Jarmy G., Rammling M., Imrich H., Thurow J., Lindemann D., Rethwilm A. Improved primate foamy virus vectors and packaging constructs. J. Virol. 2002, 76:3774-3783.
14. Hütter S., Müllers E., Stanke N., Reh J., Lindemann D. Prototype foamy virus protease activity is essential for intraparticle reverse transcription initiation but not absolutely required for uncoating upon host cell entry. J. Virol. 2013, 87:3163-3176.
15. Hütter S., Zurnic I., Lindemann D. Foamy virus budding and release. Viruses 2013, 5:1075-1098.
16. Imrich H., Heinkelein M., Herchenröder O., Rethwilm A. Primate foamy virus Pol proteins are imported into the nucleus. J. Gen. Virol. 2000, 81:2941-2947.
17. Jacks T., Power M.D., Masiarz F.R., Luciw P.A., Barr P.J., Varmus H.E. Characterization of ribosomal frameshifting in HIV-1 gag-pol expression. Nature 1988, 331:280-283.
18. Konvalinka J., Löchelt M., Zentgraf H., Flügel R.M., Kräusslich H.G. Active foamy virus proteinase is essential for virus infectivity but not for formation of a Pol polyprotein. J. Virol. 1995, 69:7264-7268.
19. Kozisek M., Henke S., Saskova K.G., Jacobs G.B., Schuch A., Buchholz B., Müller V., Kräusslich H.G., Rezacova P., Konvalinka J., Bodem J. Mutations in HIV-1 gag and pol compensate for the loss of viral fitness caused by a highly mutated protease. Antimicrob. Agents Chemother. 2012, 56:4320-4330.
20. Lee E.G., Linial M.L. The C terminus of foamy retrovirus Gag contains determinants for encapsidation of Pol protein into virions. J. Virol. 2008, 82:10803-10810.
21. Lee E.G., Roy J., Jackson D., Clark P., Boyer P.L., Hughes S.H., Linial M.L. Foamy retrovirus integrase contains a Pol dimerization domain required for protease activation. J. Virol. 2010, 85:1655-1661.
22. Lee E.G., Stenbak C.R., Linial M.L. Foamy virus assembly with emphasis on pol encapsidation. Viruses 2013, 5:886-900.
23. Lehmann-Che J., Giron M.L., Delelis O., Löchelt M., Bittoun P., Tobaly-Tapiero J., de The H., Saib A. Protease-dependent uncoating of a complex retrovirus. J. Virol. 2005, 79:9244-9253.
24. Leo B., Hartl M.J., Schweimer K., Mayr F., Wöhrl B.M. Insights into the structure and activity of prototype foamy virus RNase H. Retrovirology 2012, 9:14.
25. Leo B., Schweimer K., Rosch P., Hartl M.J., Wöhrl B.M. The solution structure of the prototype foamy virus RNase H domain indicates an important role of the basic loop in substrate binding. Retrovirology 2012, 9:73.
26. Linial M.L. Foamy Viruses 2007, Lippincott Williams & Wilkins, Philadelphia.
27. Löchelt M. Foamy virus transactivation and gene expression. Curr. Top. Microbiol. Immunol. 2003, 277:27-61.
28. Löchelt M., Flügel R.M. The human foamy virus pol gene is expressed as a Pro-Pol polyprotein and not as a Gag-Pol fusion protein. J. Virol. 1996, 70:1033-1040.
29. Miller A.D., Buttimore C. Redesign of retrovirus packaging cell lines to avoid recombination leading to helper virus production. Mol. Cell Biol. 1986, 6:2895-2902.
30. Müller B., Anders M., Aklyama H., Welsch S., Glass B., Nikovics K., Clavel F., Tervo H.M., Keppler O.T., Kräusslich H. HIV-1 Gag processing intermediates trans-dominantly interfere with HIV-1 infectivity. J. Biol. Chem. 2009, 284:9.
31. Müllers E., Stirnnagel K., Kaulfuss S., Lindemann D. Prototype foamy virus gag nuclear localization: a novel pathway among retroviruses. J. Virol. 2011, 85:9276-9285.
32. Pahl A., Flügel R.M. Characterization of the human spuma retrovirus integrase by site-directed mutagenesis, by complementation analysis, and by swapping the zinc finger domain of HIV-1. J. Biol. Chem. 1995, 270:2957-2966.
33. Pettit S.C., Moody M.D., Wehbie R.S., Kaplan A.H., Nantermet P.V., Klein C.A., Swanstrom R. The p2 domain of human immunodeficiency virus type 1 Gag regulates sequential proteolytic processing and is required to produce fully infectious virions. J. Virol. 1994, 8017-8027.
34. Pfrepper K.I., Löchelt M., Rackwitz H.R., Schnölzer M., Heid H., Flügel R.M. Molecular characterization of proteolytic processing of the Gag proteins of human spumavirus. J. Virol. 1999, 73:7907-7911.
35. Pfrepper K.I., Rackwitz H.R., Schnölzer M., Heid H., Löchelt M., Flügel R.M. Molecular characterization of proteolytic processing of the Pol proteins of human foamy virus reveals novel features of the viral protease. J. Virol. 1998, 72:7648-7652.
36. Rethwilm A. The replication strategy of foamy viruses. Curr. Top. Microbiol. Immunol. 2003, 277:1-26.
37. Rethwilm, A., 2013. Specific RNA-protein interactions in the replication of foamy viruses (FVs). Current opinion in virology.
38. Rethwilm, A., Lindemann, D., 2013. Foamy viruses, in: Knipe, D.M., Howley, P. (Eds.), Fields Virology.
39. Roy J., Linial M.L. Role of the foamy virus Pol cleavage site in viral replication. J. Virol. 2007, 81:4956-4962.
40. Schneider, A., Peter, D., Schmitt, J., Leo, B., Richter, F., Rosch, P., Wohrl, B.M., Hartl, M.J., 2013. Structural requirements for enzymatic activities of foamy virus protease-reverse transcriptase. Proteins.
41. Spannaus R., Hartl M.J., Wöhrl B.M., Rethwilm A., Bodem J. The prototype foamy virus protease is active independently of the integrase domain. Retrovirology 2012, 9:41.
42. Spannaus R., Schneider A., Hartl M., Wöhrl B.M., Bodem J. Foamy viral Gag p71/p68 cleavage is required for template switch of the reverse transcriptase. J. Virol. 2013, 87:7774-7776.
43. Stenbak C., Linial M. Role of the C terminus of foamy virus Gag in RNA packaging and Pol expression. J. Virol. 2004, 78:9423-9430.
44. Stirnnagel K., Lüftenegger D., Stange A., Swiersy A., Müllers E., Reh J., Stanke N., Grosse A., Chiantia S., Keller H., Schwille P., Hanenberg H., Zentgraf H., Lindemann D. Analysis of prototype foamy virus particle-host cell interaction with autofluorescent retroviral particles. Retrovirology 2010, 7:45.
45. Sundquist W.I., Kräusslich H.G. HIV-1 assembly, budding, and maturation. Cold Spring Harbor Perspect. Med. 2012, 2:a006924.
46. Swiersy A., Wiek C., Reh J., Zentgraf H., Lindemann D. Orthoretroviral-like prototype foamy virus Gag-Pol expression is compatible with viral replication. Retrovirology 2011, 8:66.
47. Yu S.F., Baldwin D.N., Gwynn S.R., Yendapalli S., Linial M.L. Human foamy virus replication: a pathway distinct from that of retroviruses and hepadnaviruses. Science 1996, 271:1579-1582.
48. Zemba M., Wilk T., Rutten T., Wagner A., Flügel R.M., Löchelt M. The carboxy-terminal p3Gag domain of the human foamy virus Gag precursor is required for efficient virus infectivity. Virology 1998, 247:7-13.