NEDD4L overexpression rescues the release and infectivity of human immunodeficiency virus type 1 constructs lacking PTAP and YPXL late domains

Journal of Virology

Volumn 82, Issue 10, 2008, Pages 4884-4897

  Chung, Hyo Young ^a   Morita, Eiji ^a   Von Schwedler, Uta ^a   Müller, Barbara ^b   Kräusslich, Hans Georg ^b   Sundquist, Wesley I ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CIS ACTING ELEMENT; GAG PROTEIN; PROTEIN SUBUNIT; TUMOR SUSCEPTIBILITY GENE 101 PROTEIN; UBIQUITIN PROTEIN LIGASE NEDD4; DNA BINDING PROTEIN; NEDD4 UBIQUITIN PROTEIN LIGASES; P6 GAG PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1; TRANSCRIPTION FACTOR; UBIQUITIN; UBIQUITIN PROTEIN LIGASE;

ANTIBODY TITER; ARTICLE; CATALYSIS; CYTOKINESIS; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME BINDING; GENE CONSTRUCT; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; MASON PFIZER MONKEY VIRUS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN EXPRESSION; UBIQUITINATION; VIRUS INFECTIVITY; VIRUS REPLICATION; CELL LINE; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PROTEIN MOTIF;

HUMAN IMMUNODEFICIENCY VIRUS 1; MASON-PFIZER MONKEY VIRUS; RNA VIRUSES;

AMINO ACID MOTIFS; CELL LINE; DNA-BINDING PROTEINS; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HIV-1; HUMANS; MASON-PFIZER MONKEY VIRUS; TRANSCRIPTION FACTORS; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES;

EID: 43249121457     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02667-07     Document Type: Article

References (68)

1. Carlton, J. G., and J. Martin-Serrano. 2007. Parallels between cytokinesis and retroviral budding: a role for the ESCRT machinery. Science 316:1908-1912.
2. Chen, C., O. Vincent, J. Jin, O. A. Weisz, and R. C. Montelaro. 2005. Functions of early (AP-2) and late (AIP1/ALIX) endocytic proteins in equine infectious anemia virus budding. J. Biol. Chem. 280:40474-40480.
3. Chen, H., C. A. Ross, N. Wang, Y. Huo, D. F. MacKinnon, J. B. Potash, S. G. Simpson, F. J. McMahon, J. R. DePaulo, Jr., and M. G. Mclnnis. 2001. NEDD4L on human chromosome 18q21 has multiple forms of transcripts and is a homologue of the mouse Nedd4-2 gene. Eur. J. Hum. Genet. 9:922-930.
4. Debonneville, C., S. Y. Flores, E. Kamynina, P. J. Plant, C. Tauxe, M. A. Thomas, C. Munster, A. Chraibi, J. H. Pratt, J. D. Horisberger, D. Pearce, J. Loffing, and O. Staub. 2001. Phosphorylation of Nedd4-2 by Sgk1 regulates epithelial Na(+) channel cell surface expression. EMBO J. 20:7052-7059.
5. Demirov, D. G., and E. O. Freed. 2004. Retrovirus budding. Virus Res. 106:87-102.
6. Demirov, D. G., A. Ono, J. M. Orenstein, and E. O. Freed. 2002. Overexpression of the N-terminal domain of TSG101 inhibits HIV-1 budding by blocking late domain function. Proc. Natl. Acad. Sci. USA 99:955-960.
7. Dunn, D. M., T. Ishigami, J. Pankow, A. von Niederhausern, J. Alder, S. C. Hunt, M. F. Leppert, J. M. Lalouel, and R. B. Weiss. 2002. Common variant of human NEDD4L activates a cryptic splice site to form a frameshifted transcript. J. Hum. Genet. 47:665-676.
8. Dunn, R., and L. Hicke. 2001. Domains of the rsp5 ubiquitin-protein ligase required for receptor-mediated and fluid-phase endocytosis. Mol. Biol. Cell 12:421-435.
9. Durocher, Y., S. Perret, and A. Kamen. 2002. High-level and high-throughput recombinant protein production by transient transfection of suspension-growing human 293-EBNA1 cells. Nucleic Acids Res. 30:E9.
10. Fisher, R. D., H. Y. Chung, Q. Zhai, H. Robinson, W. I. Sundquist, and C. P. Hill. 2007. Structural and biochemical studies of ALIX/AIP1 and its role in retrovirus budding. Cell 128:841-852.
11. Galan, J. M., V. Moreau, B. Andre, C. Volland, and R. Haguenauer-Tsapis. 1996. Ubiquitination mediated by the Npi1p/Rsp5p ubiquitin-protein ligase is required for endocytosis of the yeast uracil permease. J. Biol. Chem. 271:10946-10952.
12. Garnis, J. E., U. K. von Schwedler, O. W. Pornillos, S. G. Morham, K. H. Zavitz, H. E. Wang, D. A. Wettstein, K. M. Stray, M. Cote, R. L. Rich, D. G. Myszka, and W. I. Sundquist. 2001. Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 107:55-65.
13. Gottlinger, H. G., T. Dorfman, J. G. Sodroski, and W. A. Haseltine. 1991. Effect of mutations affecting the p6 gag protein on human immunodeficiency virus particle release. Proc. Natl. Acad. Sci. USA 88:3195-3199.
14. Gottwein, E., J. Bodem, B. Muller, A. Schmechel, H. Zentgraf, and H. G. Krausslich. 2003. The Mason-Pfizer monkey virus PPPY and PSAP motifs both contribute to virus release. J. Virol. 77:9474-9485.
15. Gottwein, E., S. Jager, A. Habermann, and H. G. Krausslich. 2006. Cumulative mutations of ubiquitin acceptor sites in human immunodeficiency virus type 1 Gag cause a late budding defect. J. Virol. 80:6267-6275.
16. Goulet, C. C., K. A. Volk, C. M. Adams, L. S. Prince, J. B. Stokes, and P. M. Snyder. 1998. Inhibition of the epithelial Na+ channel by interaction of Nedd4 with a PY motif deleted in Liddle's syndrome. J. Biol. Chem. 273:30012-30017.
17. Harvey, K. F., A. Dinudom, D. I. Cook, and S. Kumar. 2001. The Nedd4-like protein K1AA0439 is a potential regulator of the epithelial sodium channel. J. Biol. Chem. 276:8597-8601.
18. Heidecker, G., P. A. Lloyd, F. Soheilian, K. Nagashima, and D. Derse. 2007. The role of WWP1-Gag interaction and Gag ubiquitination in assembly and release of human T-cell leukemia virus type 1. J. Virol. 81:9769-9777.
19. Hein, C., J. Y. Springael, C. Volland, R. Haguenauer-Tsapis, and B. Andre. 1995. NPI1, an essential yeast gene involved in induced degradation of Gap1 and Fur4 permeases, encodes the Rsp5 ubiquitin-protein ligase. Mol. Microbiol. 18:77-87.
20. Hermida-Matsumoto, L., and M. D. Resh. 2000. Localization of human immunodeficiency virus type 1 Gag and Env at the plasma membrane by confocal imaging. J. Virol. 74:8670-8679.
21. Hurley, J. H., and S. D. Emr. 2006. The ESCRT complexes: structure and mechanism of a membrane-trafficking network. Annu. Rev. Biophys. Biomol. Struct. 35:277-298.
22. Ingham, R. J., G. Gish, and T. Pawson. 2004. The Nedd4 family of E3 ubiquitin ligases: functional diversity within a common modular architecture. Oncogene 23:1972-1984.
23. Itani, O. A., J. B. Stokes, and C. P. Thomas. 2005. Nedd4-2 isoforms differentially associate with ENaC and regulate its activity. Am. J. Physiol. Renal Physiol. 289:F334-F346.
24. Kanelis, V., D. Rotin, and J. D. Forman-Kay. 2001. Solution structure of a Nedd4 WW domain-ENaC peptide complex. Nat. Struct. Biol. 8:407-412.
25. Katzmann, D. J., S. Sarkar, T. Chu, A. Audhya, and S. D. Emr. 2004. Multivesicular body sorting: ubiquitin ligase Rsp5 is required for the modification and sorting of carboxypeptidase S. Mol. Biol. Cell 15:468-480.
26. Kim, B. Y., J. A. Olzmann, G. S. Barsh, L. S. Chin, and L. Li. 2007. Spongiform neurodegeneration-assoeiated E3 ligase Mahogunin ubiquitylates TSG101 and regulates endosomal trafficking. Mol. Biol. Cell 18:1129-1142.
27. Loriaux, M. M., R. P. Rehfuss, R. G. Brennan, and R. H. Goodman. 1993. Engineered leucine zippers show that hemiphosphorylated CREB complexes arc transcriptionally active. Proc. Natl. Acad. Sci. USA 90:9046-9050.
28. Malbert-Colas, L., G. Nicolas, C. Galand, M. C. Lecomte, and D. Dhermy. 2003. Identification of new partners of the epithelial sodium channel alpha subunit. C. R. Biol. 326:615-624.
29. Martin-Serrano, J. 2007. The role of ubiquitin in retroviral egress. Traffic 8:1297-1303.
30. Martin-Serrano, J., S. W. Eastman, W. Chung, and P. D. Bieniasz. 2005. HECT ubiquitin ligases link viral and cellular PPXY motifs to the vacuolar protein-sorting pathway. J. Cell Biol. 168:89-101.
31. Martin-Serrano, J., T. Zang, and P. D. Bieniasz. 2001. HIV-1 and Ebola virus encode small peptide motifs that recruit Tsg101 to sites of particle assembly to facilitate egress. Nat. Med. 7:1313-1319.
32. Medina, G., Y. Zhang, Y. Tang, E. Gottwein, M. L. Vana, F. Bouamr, J. Leis, and C. A. Carter. 2005. The functionally exchangeable L domains in RSV and HIV-1 Gag direct particle release through pathways linked by Tsg101. Traffic 6:880-894.
33. Morita, E., V. Sandrin, S. Alam, D. Eckert, S. P. Gygi, and W. I. Sundquist. 2007. Identification of the human MVB12 proteins as ESCRT-I subunits that function in HIV budding. Cell Host Microbe 2:41-53.
34. Morita, E., V. Sandrin, H. Y. Chung, S. G. Morham, S. P. Gygi, C. K. Rodesch, and W. I. Sundquist. 2007. Human ESCRT and ALIX proteins interact with proteins of the midbody and function in cytokinesis. EMBO J. 26:4215-4227.
35. Morita, E., and W. I. Sundquist. 2004. Retrovirus budding. Annu. Rev. Cell Dev. Biol. 20:395-425.
36. Ott, D. E., L. V. Coren, E. N. Chertova, T. D. Gagliardi, and U. Schubert. 2000. Ubiquitination of HIV-1 and MuLV Gag. Virology 278:111-121.
37. Ott, D. E., L. V. Coren, T. D. Copeland, B. P. Kane, D. G. Johnson, R. C. Sowder II, Y. Yoshinaka, S. Oroszlan, L. O. Arthur, and L. E. Henderson. 1998. Ubiquitin is covalently attached to the p6Gag proteins of human immunodeficiency virus type 1 and simian immunodeficiency virus and to the p12Gag protein of Moloney murine leukemia virus. J. Virol. 72:2962-2968.
38. Perez, M., R. C. Craven, and J. C. de la Torre. 2003. The small RING finger protein Z drives arenavirus budding: implications for antiviral strategies. Proc. Natl. Acad. Sci. USA 100:12978-12983.
39. Piper, R. C., and D. J. Katzmann. 2007. Biogenesis and function of multivesicular bodies. Annu. Rev. Cell Dev. Biol. 23:519-547.
40. Popov, S., E. Popova, M. Inoue, and H. G. Gottlinger. 2008. Human immunodeficiency virus type 1 Gag engages the Bro1 domain of ALIX/AIP1 through the nucleocapsid. J. Virol. 82:1389-1398.
41. Pornillos, O., S. L. Alam, D. R. Davis, and W. I. Sundquist. 2002. Structure of the Tsg101 UEV domain in complex with the PTAP motif of the HIV-1 p6 protein. Nat. Struct. Biol. 9:812-817.
42. Pornillos, O., S. L. Alam, R. L. Rich, D. G. Myszka, D. R. Davis, and W. I. Sundquist. 2002. Structure and functional interactions of the Tsg101 UEV domain. EMBO J. 21:2397-2406.
43. Putterman, D., R. B. Pepinsky, and V. M. Vogt. 1990. Ubiquitin in avian leukosis virus particles. Virology 176:633-637.
44. Sakalian, M., S. D. Parker, R. A. Weldon, Jr., and E. Hunter. 1996. Synthesis and assembly of retrovirus Gag precursors into immature capsids in vitro. J. Virol. 70:3706-3715.
45. Schubert, U., D. E. Ott, E. N. Chertova, R. Welker, U. Tessmer, M. F. Princiotta, J. R. Bennink, H. G. Krausslich, and J. W. Yewdell. 2000. Proteasome inhibition interferes with Gag polyprotein processing, release, and maturation of HIV-1 and HIV-2. Proc. Natl. Acad. Sci. USA 97:13057-13062.
46. Segura-Morales, C., C. Pescia, C. Chatellard-Causse, R. Sadoul, E. Bertrand, and E. Basyuk. 2005. Tsg101 and Alix interact with murine leukemia virus Gag and cooperate with Nedd4 ubiquitin ligases during budding. J. Biol. Chem. 280:27004-27012.
47. Shearwin-Whyatt, L., H. E. Dalton, N. Foot, and S. Kumar. 2006. Regulation of functional diversity within the Nedd4 family by accessory and adaptor proteins. Bioessays 28:617-628.
48. Shehu-Xhilaga, M., S. Ablan, D. G. Demirov, C. Chen, R. C. Montelaro, and E. O. Freed. 2004. Late domain-dependent inhibition of equine infectious anemia virus budding. J. Virol. 78:724-732.
49. Springael, J. Y., J. O. De Craene, and B. Andre. 1999. The yeast Npi1/Rsp5 ubiquitin ligase lacking its N-terminal C2 domain is competent for ubiquitination but not for subsequent endocytosis of the gap1 permease. Biochem. Biophys. Res. Commun. 257:561-566.
50. Staub, O., S. Dho, P. Henry, J. Correa, T. Ishikawa, J. McGlade, and D. Rotin. 1996. WW domains of Nedd4 bind to the proline-rich PY motifs in the epithelial Na+ channel deleted in Liddle's syndrome. EMBO J. 15:2371-2380.
51. Strack, B., A. Calistri, M. A. Accola, G. Palu, and H. G. Gottlinger. 2000. A role for ubiquitin ligase recruitment in retrovirus release. Proc. Natl. Acad. Sci. USA 97:13063-13068.
52. Strack, B., A. Calistri, S. Craig, E. Popova, and H. G. Gottlinger. 2003. AIP1/ALIX is a binding partner for HIV-1 p6 and EIAV p9 functioning in virus budding. Cell 114:689-699.
53. Strack, B., A. Calistri, and H. G. Gottlinger. 2002. Late assembly domain function can exhibit context dependence and involves ubiquitin residues implicated in endocytosis. J. Virol. 76:5472-5479.
54. Strausberg, R. L., et al. 2002. Generation and initial analysis of more than 15,000 full-length human and mouse cDNA sequences. Proc. Natl. Acad. Sci. USA 99:16899-16903.
55. Sundquist, W. I., H. L. Schubert, B. N. Kelly, G. C. Hill, J. M. Holten, and C. P. Hill. 2004. Ubiquitin recognition by the human TSG101 protein. Mol. Cell 13:783-789.
56. Urata, S., T. Noda, Y. Kawaoka, S. Morikawa, H. Yokosawa, and J. Yasuda. 2007. Interaction of Tsg101 with Marburg virus VP40 depends on the PPPY motif, but not the PT/SAP motif as in the case of Ebola virus, and Tsg101 plays a critical role in the budding of Marburg virus-like particles induced by VP40, NP, and GP. J. Virol. 81:4895-4899.
57. Usami, Y., S. Popov, and H. G. Gottlinger. 2007. Potent rescue of human immunodeficiency virus type 1 late domain mutants by ALIX/AIP1 depends on its CHMP4 binding site. J. Virol. 81:6614-6622.
58. Usami, Y., S. Popov, E. Popova, and H. G. Göttlinger. 2008. Efficient and specific rescue of human immunodeficiency virus type 1 budding defects by a Nedd4-like ubiquitin ligase. J. Virol. 82:4898-4907.
59. Vana, M. L., Y. Tang, A. Chen, G. Medina, C. Carter, and J. Leis. 2004. Role of Nedd4 and ubiquitination of Rous sarcoma virus Gag in budding of virus-like particles from cells. J. Virol. 78:13943-13953.
60. VerPlank, L., F. Bouamr, T. J. LaGrassa, B. Agresta, A. Kikonyogo, J. Leis, and C. A. Carter. 2001. Tsg101, a homologue of ubiquitin-conjugating (E2) enzymes, binds the L domain in HIV type 1 Pr55Gag. Proc. Natl. Acad. Sci. USA 98:7724-7729.
61. Vogt, V. M. 2000. Ubiquitin in retrovirus assembly: actor or bystander? Proc. Natl. Acad. Sci. USA 97:12945-12947.
62. Welsch, S., B. Muller, and H. G. Krausslich. 2007. More than one door - budding of enveloped viruses through cellular membranes. FEBS Lett. 581:2089-2097.
63. Wiesner, S., A. A. Ogunjimi, H. R. Wang, D. Rotin, F. Sicheri, J. L. Wrana, and J. D. Forman-Kay. 2007. Autoinhibition of the HECT-type ubiquitin ligase Smurf2 through its C2 domain. Cell 130:651-662.
64. Williams, R. L., and S. Urbe. 2007. The emerging shape of the ESCRT machinery. Nat. Rev. Mol. Cell Biol. 8:355-368.
65. Yasuda, J., and E. Hunter. 1998. A proline-rich motif (PPPY) in the Gag polyprotein of Mason-Pfizer monkey virus plays a maturation-independent role in virion release. J. Virol. 72:4095-4103.
66. Zhadina, M., M. O. McClure, M. C. Johnson, and P. D. Bieniasz. 2007. Ubiquitin-dependent virus particle budding without viral protein ubiquitin-ation. Proc. Natl. Acad. Sci. USA 104:20031-20036.
67. Zhai, Q., R. D. Fisher, H. Y. Chung, D. G. Myszka, W. I. Sundquist, and C. P. Hill. 2008. Structural and functional studies of ALIX interactions with YPX(n) L late domains of HIV-1 and EIAV. Nat. Struct. Mol. Biol. 15:43-49.
68. Zhang, Y., H. Qian, Z. Love, and E. Barklis. 1998. Analysis of the assembly function of the human immunodeficiency virus type 1 Gag protein nucleocapsid domain. J. Virol. 72:1782-1789.