Dynamics of ESCRT protein recruitment during retroviral assembly

Nature Cell Biology

Volumn 13, Issue 4, 2011, Pages 394-402

  Jouvenet, Nolwenn ^a,b   Zhadina, Maria ^a   Bieniasz, Paul D ^a   Simon, Sanford M ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b University of Montpellier I and II   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ESCRT PROTEIN; GAG PROTEIN; PROTEIN VPS4A; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; CYTOKINESIS; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; MULTIVESICULAR BODY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RETROVIRUS; VIRUS ASSEMBLY; VIRUS CELL INTERACTION;

CALCIUM-BINDING PROTEINS; CELL CYCLE PROTEINS; CELL MEMBRANE; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; GENE PRODUCTS, GAG; HELA CELLS; HIV-1; HUMANS; INFECTIOUS ANEMIA VIRUS, EQUINE; RECOMBINANT FUSION PROTEINS; RETROVIRIDAE; VACUOLAR PROTON-TRANSLOCATING ATPASES; VIRUS ASSEMBLY;

EID: 79953296191     PISSN: 14657392     EISSN: None     Source Type: Journal    
DOI: 10.1038/ncb2207     Document Type: Article

References (43)

1. McDonald, B. & Martin-Serrano, J. No strings attached: the ESCRT machinery in viral budding and cytokinesis. J. Cell Sci. 122, 2167-2177 (2009).
2. Wollert, T. et al. The ESCRT machinery at a glance. J. Cell Sci. 122, 2163-2166 (2009).
3. Bieniasz, P. D. Late budding domains and host proteins in enveloped virus release. Virology 344, 55-63 (2006). (Pubitemid 41814450)
4. Morita, E. & Sundquist, W. I. Retrovirus budding. Annu. Rev. Cell Dev. Biol. 20, 395-425 (2004). (Pubitemid 39488644)
5. Williams, R. L. & Urbe, S. The emerging shape of the ESCRT machinery. Nat. Rev. Mol. Cell Biol. 8, 355-368 (2007). (Pubitemid 46643239)
6. Babst, M., Katzmann, D. J., Snyder, W. B., Wendland, B. & Emr, S. D. Endosome-associated complex, ESCRT-II, recruits transport machinery for protein sorting at the multivesicular body. Dev. Cell 3, 283-289 (2002).
7. Babst, M., Katzmann, D. J., Estepa-Sabal, E. J., Meerloo, T. & Emr, S. D. Escrt-III: an endosome-associated heterooligomeric protein complex required for mvb sorting. Dev. Cell 3, 271-282 (2002).
8. Katzmann, D. J., Babst, M. & Emr, S. D. Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I. Cell 106, 145-155 (2001). (Pubitemid 32772626)
9. Saksena, S., Wahlman, J., Teis, D., Johnson, A. E. & Emr, S. D. Functional reconstitution of ESCRT-III assembly and disassembly. Cell 136, 97-109 (2009).
10. Wollert, T., Wunder, C., Lippincott-Schwartz, J. & Hurley, J. H. Membrane scission by the ESCRT-III complex. Nature 458, 172-177 (2009).
11. Wollert, T. & Hurley, J. H. Molecular mechanism of multivesicular body biogenesis by ESCRT complexes. Nature 464, 864-869 (2010).
12. Martin-Serrano, J., Zang, T. & Bieniasz, P. D. 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 (2001). (Pubitemid 34007935)
13. Garrus, J. E. et al. Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 107, 55-65 (2001). (Pubitemid 32972037)
14. Strack, B., Calistri, A., Craig, S., Popova, E. & Gottlinger, H. G. AIP1/ALIX is a binding partner for HIV-1 p6 and EIAV p9 functioning in virus budding. Cell 114, 689-699 (2003). (Pubitemid 37186765)
15. Fisher, R. D. et al. Structural and biochemical studies of ALIX/AIP1 and its role in retrovirus budding. Cell 128, 841-852 (2007). (Pubitemid 46341413)
16. Martin-Serrano, J., Eastman, S. W., Chung, W. & Bieniasz, P. D. HECT ubiquitin ligases link viral and cellular PPXY motifs to the vacuolar protein-sorting pathway. J. Cell Biol. 168, 89-101 (2005). (Pubitemid 40111060)
17. Martin-Serrano, J., Yarovoy, A., Perez-Caballero, D. & Bieniasz, P. D. Divergent retroviral late-budding domains recruit vacuolar protein sorting factors by using alternative adaptor proteins. Proc. Natl Acad. Sci. USA 100, 12414-12419 (2003). (Pubitemid 37271574)
18. Von Schwedler, U. K. et al. The protein network of HIV budding. Cell 114, 701-713 (2003). (Pubitemid 37203363)
19. Jouvenet, N. et al. Plasma membrane is the site of productive HIV-1 particle assembly. PLoS Biol. 4, e435 (2006).
20. Finzi, A., Orthwein, A., Mercier, J. & Cohen, E. A. Productive human immunode-ciency virus type 1 assembly takes place at the plasma membrane. J. Virol. 81, 7476-7490 (2007). (Pubitemid 47047835)
21. Welsch, S. et al. HIV-1 buds predominantly at the plasma membrane of primary human macrophages. PLoS Pathog. 3, e36 (2007).
22. Simon, S. M. Partial internal re-ections on total internal re-ectionfiuorescent microscopy. Trends Cell Biol. 19, 661-668 (2009).
23. Jouvenet, N., Bieniasz, P. D. & Simon, S. M. Imaging the biogenesis of individual HIV-1 virions in live cells. Nature 454, 236-240 (2008). (Pubitemid 351969887)
24. Jouvenet, N., Simon, S. M. & Bieniasz, P. D. Imaging the interaction of HIV-1 genomes and Gag during assembly of individual viral particles. Proc. Natl Acad. Sci. USA 106, 19114-19119 (2009).
25. Ivanchenko, S. et al. Dynamics of HIV-1 assembly and release. PLoS Pathog. 5, e1000652 (2009).
26. Lin, Y., Kimpler, L. A., Naismith, T. V., Lauer, J. M. & Hanson, P. I. Interaction of the mammalian endosomal sorting complex required for transport (ESCRT) III protein hSnf7-1 with itself, membranes, and the AAAC ATPase SKD1. J. Biol. Chem. 280, 12799-12809 (2005).
27. Howard, T. L., Stauffer, D. R., Degnin, C. R. & Hollenberg, S. M. CHMP1 functions as a member of a newly de-ned family of vesicle traficking proteins. J. Cell Sci. 114, 2395-2404 (2001). (Pubitemid 32684795)
28. Stuchell, M. D. et al. The human endosomal sorting complex required for transport (ESCRT-I) and its role in HIV-1 budding. J. Biol. Chem. 279, 36059-36071 (2004). (Pubitemid 39100614)
29. Zamborlini, A. et al. Release of autoinhibition converts ESCRT-III components into potent inhibitors of HIV-1 budding. Proc. Natl Acad. Sci. USA 103, 19140-19145 (2006). (Pubitemid 350002840)
30. Goila-Gaur, R., Demirov, D. G., Orenstein, J. M., Ono, A. & Freed, E. O. Defects in human immunode-ciency virus budding and endosomal sorting induced by TSG101 overexpression. J. Virol. 77, 6507-6519 (2003). (Pubitemid 36588420)
31. Morita, E. et al. Human ESCRT-III and VPS4 proteins are required for centrosome and spindle maintenance. Proc. Natl Acad. Sci. USA 107, 12889-12894 (2010).
32. Morita, E. et al. Human ESCRT and ALIX proteins interact with proteins of the midbody and function in cytokinesis. Embo J. 26, 4215-4227 (2007). (Pubitemid 47525161)
33. Carlton, J. G. & Martin-Serrano, J. Parallels between cytokinesis and retroviral budding: a role for the ESCRT machinery. Science 316, 1908-1912 (2007). (Pubitemid 47025792)
34. VerPlank, L. et al. 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 (2001).
35. Usami, Y., Popov, S. & Gottlinger, H. G. Potent rescue of human immunode-ciency virus type 1 late domain mutants by ALIX/AIP1 depends on its CHMP4 binding site. J. Virol. 81, 6614-6622 (2007). (Pubitemid 46878065)
36. Carlton, J. G., Agromayor, M. & Martin-Serrano, J. Differential requirements for Alix and ESCRT-III in cytokinesis and HIV-1 release. Proc. Natl Acad. Sci. USA 105, 10541-10546 (2008).
37. Zhai, Q. et al. 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 (2008).
38. Briggs, J. A. et al. The stoichiometry of Gag protein in HIV-1. Nat. Struct. Mol. Biol. 11, 672-675 (2004). (Pubitemid 38823535)
39. Popov, S., Popova, E., Inoue, M. & Gottlinger, H. G. Divergent Bro1 domains share the capacity to bind human immunode-ciency virus type 1 nucleocapsid and to enhance virus-like particle production. J. Virol. 83, 7185-7193 (2009).
40. Dussupt, V. et al. 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. 5, e1000339 (2009).
41. Neil, S. J., Eastman, S. W., Jouvenet, N. & Bieniasz, P. D. HIV-1 Vpu promotes release and prevents endocytosis of nascent retrovirus particles from the plasma membrane. PLoS Pathog. 2, e39 (2006).
42. Martin-Serrano, J., Zang, T. & Bieniasz, P. D. Role of ESCRT-I in retroviral budding. J. Virol. 77, 4794-4804 (2003). (Pubitemid 36402829)
43. Jouvenet, N. et al. Broad-spectrum inhibition of retroviral and loviral particle release by tetherin. J. Virol. 83, 1837-1844 (2009).