Identification of late assembly domains of the human endogenous retrovirus-K(HML-2)

Retrovirology

Volumn 10, Issue 1, 2013, Pages

  Chudak, Claudia ^a   Beimforde, Nadine ^a   George, Maja ^a   Zimmermann, Anja ^a   Lausch, Veronika ^a   Hanke, Kirsten ^a   Bannert, Norbert ^a  

^a ROBERT KOCH INSTITUTE   (Germany)

Author keywords

Alix; Budding; Endogenous retrovirus; Gag protein; HERV K(HML 2); Late assembly domain; Retrovirus; Tsg101

Indexed keywords

ALIX PROTEIN; CELL PROTEIN; ESCRT I PROTEIN; GAG PROTEIN; PROTEIN P15; TETRAPEPTIDE; TUMOR SUSCEPTIBILITY GENE 101 PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CONTROLLED STUDY; ELECTRON MICROSCOPY; EMBRYO; ENDOGENOUS RETROVIRUS; GENE INSERTION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; LATE ASSEMBLY DOMAIN; MOLECULAR CLONING; NONHUMAN; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; VIRUS INACTIVATION; VIRUS RELEASE;

HUMAN ENDOGENOUS RETROVIRUS; HUMAN ENDOGENOUS RETROVIRUS K;

AMINO ACID MOTIFS; CELL LINE; ENDOGENOUS RETROVIRUSES; GENE PRODUCTS, GAG; HUMANS; MICROSCOPY, ELECTRON; PROTEIN BINDING; VIRUS ASSEMBLY; VIRUS RELEASE;

EID: 84887743079     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-10-140     Document Type: Article

References (51)

1. Freed EO. HIV-1 gag proteins: diverse functions in the virus life cycle. Virology 1998, 251:1-15. 10.1006/viro.1998.9398, 9813197.
2. Swanstrom R, Wills JW. Synthesis, assembly, and processing of viral proteins. Retroviruses 1997, Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press, Coffin JM, Hughes SH, Varmus HE.
3. Gottlinger HG, Dorfman T, Sodroski JG, Haseltine WA. Effect of mutations affecting the p6 gag protein on human immunodeficiency virus particle release. Proc Natl Acad Sci USA 1991, 88:3195-3199. 10.1073/pnas.88.8.3195, 51412, 2014240.
4. Wills JW, Cameron CE, Wilson CB, Xiang Y, Bennett RP, Leis J. An assembly domain of the Rous sarcoma virus Gag protein required late in budding. J Virol 1994, 68:6605-6618. 237081, 8083996.
5. Raiborg C, Stenmark H. The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature 2009, 458:445-452. 10.1038/nature07961, 19325624.
6. Garrus JE, von Schwedler UK, Pornillos OW, Morham SG, Zavitz KH, Wang HE, Wettstein DA, Stray KM, Cote M, Rich RL, et al. Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 2001, 107:55-65. 10.1016/S0092-8674(01)00506-2, 11595185.
7. Kikonyogo A, Bouamr F, Vana ML, Xiang Y, Aiyar A, Carter C, Leis J. Proteins related to the Nedd4 family of ubiquitin protein ligases interact with the L domain of Rous sarcoma virus and are required for gag budding from cells. Proc Natl Acad Sci USA 2001, 98:11199-11204. 10.1073/pnas.201268998, 58707, 11562473.
8. Ott DE, Coren LV, Chertova EN, Gagliardi TD, Schubert U. Ubiquitination of HIV-1 and MuLV Gag. Virology 2000, 278:111-121. 10.1006/viro.2000.0648, 11112487.
9. Schubert U, Ott DE, Chertova EN, Welker R, Tessmer U, Princiotta MF, Bennink JR, Krausslich HG, Yewdell JW. Proteasome inhibition interferes with gag polyprotein processing, release, and maturation of HIV-1 and HIV-2. Proc Natl Acad Sci USA 2000, 97:13057-13062. 10.1073/pnas.97.24.13057, 27177, 11087859.
10. Zhadina M, Bieniasz PD. Functional interchangeability of late domains, late domain cofactors and ubiquitin in viral budding. PLoS Pathog 2010, 6:e1001153. 10.1371/journal.ppat.1001153, 2958808, 20975941.
11. Joshi A, Munshi U, Ablan SD, Nagashima K, Freed EO. Functional replacement of a retroviral late domain by ubiquitin fusion. Traffic 2008, 9:1972-1983. 10.1111/j.1600-0854.2008.00817.x, 2763539, 18817521.
12. Fisher RD, Chung HY, Zhai Q, Robinson H, Sundquist WI, Hill CP. Structural and biochemical studies of ALIX/AIP1 and its role in retrovirus budding. Cell 2007, 128:841-852. 10.1016/j.cell.2007.01.035, 17350572.
13. Strack B, Calistri A, Craig S, Popova E, Gottlinger HG. AIP1/ALIX is a binding partner for HIV-1 p6 and EIAV p9 functioning in virus budding. Cell 2003, 114:689-699. 10.1016/S0092-8674(03)00653-6, 14505569.
14. Gottwein E, Bodem J, Muller B, Schmechel A, Zentgraf H, Krausslich HG. The mason-pfizer monkey virus PPPY and PSAP motifs both contribute to virus release. J Virol 2003, 77:9474-9485. 10.1128/JVI.77.17.9474-9485.2003, 187385, 12915562.
15. Bouamr F, Melillo JA, Wang MQ, Nagashima K, de Los Santos M, Rein A, Goff SP. PPPYVEPTAP motif is the late domain of human T-cell leukemia virus type 1 Gag and mediates its functional interaction with cellular proteins Nedd4 and Tsg101 [corrected]. J Virol 2003, 77:11882-11895. 10.1128/JVI.77.22.11882-11895.2003, 253756, 14581525.
16. Dussupt V, Javid MP, Abou-Jaoude G, Jadwin JA, de La Cruz J, Nagashima K, Bouamr F. The nucleocapsid region of HIV-1 Gag cooperates with the PTAP and LYPXnL late domains to recruit the cellular machinery necessary for viral budding. PLoS Pathog 2009, 5:e1000339. 10.1371/journal.ppat.1000339, 2651531, 19282983.
17. George M, Schwecke T, Beimforde N, Hohn O, Chudak C, Zimmermann A, Kurth R, Naumann D, Bannert N. Identification of the protease cleavage sites in a reconstituted Gag polyprotein of an HERV-K(HML-2) element. Retrovirology 2011, 8:30. 10.1186/1742-4690-8-30, 3114732, 21554716.
18. Monde K, Contreras-Galindo R, Kaplan MH, Markovitz DM, Ono A. Human endogenous retrovirus K Gag coassembles with HIV-1 Gag and reduces the release efficiency and infectivity of HIV-1. J Virol 2012, 86:11194-11208. 10.1128/JVI.00301-12, 3457174, 22855497.
19. Fukuma A, Abe M, Urata S, Yoshikawa R, Morikawa Y, Miyazawa T, Yasuda J. Viral and cellular requirements for the budding of feline endogenous retrovirus RD-114. Virol J 2011, 8:540. 10.1186/1743-422X-8-540, 3287669, 22168342.
20. Stoye JP. Studies of endogenous retroviruses reveal a continuing evolutionary saga. Nat Rev Microbiol 2012, 10:395-406.
21. Urnovitz HB, Murphy WH. Human endogenous retroviruses: nature, occurrence, and clinical implications in human disease. Clin Microbiol Rev 1996, 9:72-99. 172883, 8665478.
22. Kurth R, Bannert N. Beneficial and detrimental effects of human endogenous retroviruses. Int J Cancer 2010, 126:306-314. 10.1002/ijc.24902, 19795446.
23. Lower J, Lower R, Stegmann J, Frank H, Kurth R. Retrovirus particle production in three of four human teratocarcinoma cell lines. Haematol Blood Transfus 1981, 26:541-544.
24. Hanke K, Chudak C, Kurth R, Bannert N. The Rec protein of HERV-K(HML-2) upregulates androgen receptor activity by binding to the human small glutamine-rich tetratricopeptide repeat protein (hSGT). J Virol 2013, 87:11019. 11030, 10.1128/JVI.03031-12, 23926355.
25. Diem O, Schaffner M, Seifarth W, Leib-Mosch C. Influence of antipsychotic drugs on human endogenous retrovirus (HERV) transcription in brain cells. PLoS One 2012, 7:e30054. 10.1371/journal.pone.0030054, 3256206, 22253875.
26. Lower R, Lower J, Frank H, Harzmann R, Kurth R. Human teratocarcinomas cultured in vitro produce unique retrovirus-like viruses. J Gen Virol 1984, 65(Pt 5):887-898.
27. Dewannieux M, Harper F, Richaud A, Letzelter C, Ribet D, Pierron G, Heidmann T. Identification of an infectious progenitor for the multiple-copy HERV-K human endogenous retroelements. Genome Res 2006, 16:1548-1556. 10.1101/gr.5565706, 1665638, 17077319.
28. Hanke K, Kramer P, Seeher S, Beimforde N, Kurth R, Bannert N. Reconstitution of the ancestral glycoprotein of human endogenous retrovirus k and modulation of its functional activity by truncation of the cytoplasmic domain. J Virol 2009, 83:12790-12800. 10.1128/JVI.01368-09, 2786854, 19812154.
29. Lee YN, Bieniasz PD. Reconstitution of an infectious human endogenous retrovirus. PLoS Pathog 2007, 3:e10. 10.1371/journal.ppat.0030010, 1781480, 17257061.
30. Turner G, Barbulescu M, Su M, Jensen-Seaman MI, Kidd KK, Lenz J. Insertional polymorphisms of full-length endogenous retroviruses in humans. Curr Biol 2001, 11:1531-1535. 10.1016/S0960-9822(01)00455-9, 11591322.
31. Beimforde N, Hanke K, Ammar I, Kurth R, Bannert N. Molecular cloning and functional characterization of the human endogenous retrovirus K113. Virology 2008, 371:216-225. 10.1016/j.virol.2007.09.036, 18076964.
32. Demirov DG, Freed EO. Retrovirus budding. Virus Res 2004, 106:87-102. 10.1016/j.virusres.2004.08.007, 15567490.
33. von Schwedler UK, Stuchell M, Muller B, Ward DM, Chung HY, Morita E, Wang HE, Davis T, He GP, Cimbora DM, et al. The protein network of HIV budding. Cell 2003, 114:701-713. 10.1016/S0092-8674(03)00714-1, 14505570.
34. VerPlank L, Bouamr F, LaGrassa TJ, Agresta B, Kikonyogo A, Leis J, Carter CA. Tsg101, a homologue of ubiquitin-conjugating (E2) enzymes, binds the L domain in HIV type 1 Pr55(Gag). Proc Natl Acad Sci USA 2001, 98:7724-7729. 10.1073/pnas.131059198, 35409, 11427703.
35. Dolnik O, Kolesnikova L, Stevermann L, Becker S. Tsg101 is recruited by a late domain of the nucleocapsid protein to support budding of Marburg virus-like particles. J Virol 2010, 84:7847-7856. 10.1128/JVI.00476-10, 2897605, 20504928.
36. Pornillos O, Alam SL, Rich RL, Myszka DG, Davis DR, Sundquist WI. Structure and functional interactions of the Tsg101 UEV domain. EMBO J 2002, 21:2397-2406. 10.1093/emboj/21.10.2397, 125378, 12006492.
37. Li F, Chen C, Puffer BA, Montelaro RC. Functional replacement and positional dependence of homologous and heterologous L domains in equine infectious anemia virus replication. J Virol 2002, 76:1569-1577. 10.1128/JVI.76.4.1569-1577.2002, 135910, 11799151.
38. Bishop N, Horman A, Woodman P. Mammalian class E vps proteins recognize ubiquitin and act in the removal of endosomal protein-ubiquitin conjugates. J Cell Biol 2002, 157:91-101. 10.1083/jcb.200112080, 2173266, 11916981.
39. Cabezas A, Bache KG, Brech A, Stenmark H. Alix regulates cortical actin and the spatial distribution of endosomes. J Cell Sci 2005, 118:2625-2635. 10.1242/jcs.02382, 15914539.
40. Pan S, Wang R, Zhou X, He G, Koomen J, Kobayashi R, Sun L, Corvera J, Gallick GE, Kuang J. Involvement of the conserved adaptor protein Alix in actin cytoskeleton assembly. J Biol Chem 2006, 281:34640-34650. 10.1074/jbc.M602263200, 16966331.
41. Goila-Gaur R, Demirov DG, Orenstein JM, Ono A, Freed EO. Defects in human immunodeficiency virus budding and endosomal sorting induced by TSG101 overexpression. J Virol 2003, 77:6507-6519. 10.1128/JVI.77.11.6507-6519.2003, 155030, 12743307.
42. Usami Y, Popov S, Gottlinger HG. Potent rescue of human immunodeficiency virus type 1 late domain mutants by ALIX/AIP1 depends on its CHMP4 binding site. J Virol 2007, 81:6614-6622. 10.1128/JVI.00314-07, 1900090, 17428861.
43. Ruprecht K, Ferreira H, Flockerzi A, Wahl S, Sauter M, Mayer J, Mueller-Lantzsch N. Human endogenous retrovirus family HERV-K(HML-2) RNA transcripts are selectively packaged into retroviral particles produced by the human germ cell tumor line Tera-1 and originate mainly from a provirus on chromosome 22q11.21. J Virol 2008, 82:10008-10016. 10.1128/JVI.01016-08, 2566279, 18684837.
44. Subramanian RP, Wildschutte JH, Russo C, Coffin JM. Identification, characterization, and comparative genomic distribution of the HERV-K (HML-2) group of human endogenous retroviruses. Retrovirology 2011, 8:90. 10.1186/1742-4690-8-90, 3228705, 22067224.
45. Bannert N, Kurth R. Retroelements and the human genome: new perspectives on an old relation. Proc Natl Acad Sci USA 2004, 101(Suppl 2):14572-14579. 521986, 15310846.
46. Kraus B, Boller K, Reuter A, Schnierle BS. Characterization of the human endogenous retrovirus K Gag protein: identification of protease cleavage sites. Retrovirology 2011, 8:21. 10.1186/1742-4690-8-21, 3073897, 21429186.
47. Bieniasz PD. Late budding domains and host proteins in enveloped virus release. Virology 2006, 344:55-63. 10.1016/j.virol.2005.09.044, 16364736.
48. Wang H, Machesky NJ, Mansky LM. Both the PPPY and PTAP motifs are involved in human T-cell leukemia virus type 1 particle release. J Virol 2004, 78:1503-1512. 10.1128/JVI.78.3.1503-1512.2004, 321366, 14722305.
49. Luttge BG, Shehu-Xhilaga M, Demirov DG, Adamson CS, Soheilian F, Nagashima K, Stephen AG, Fisher RJ, Freed EO. Molecular characterization of feline immunodeficiency virus budding. J Virol 2008, 82:2106-2119. 10.1128/JVI.02337-07, 2258934, 18094166.
50. Demirov DG, Orenstein JM, Freed EO. The late domain of human immunodeficiency virus type 1 p6 promotes virus release in a cell type-dependent manner. J Virol 2002, 76:105-117. 10.1128/JVI.76.1.105-117.2002, 135729, 11739676.
51. Katoh K, Shibata H, Hatta K, Maki M. CHMP4b is a major binding partner of the ALG-2-interacting protein Alix among the three CHMP4 isoforms. Arch Biochem Biophys 2004, 421:159-165. 10.1016/j.abb.2003.09.038, 14678797.