ALIX Rescues Budding of a Double PTAP/PPEY L-Domain Deletion Mutant of Ebola VP40: A Role for ALIX in Ebola Virus Egress

Journal of Infectious Diseases

Volumn 212, Issue , 2015, Pages S138-S145

  Han, Ziying ^a   Madara, Jonathan J ^a   Liu, Yuliang ^a   Liu, Wenbo ^a   Ruthel, Gordon ^a   Freedman, Bruce D ^a   Harty, Ronald N ^a  

^a UNIVERSITY OF PENNSYLVANIA SCHOOL OF VETERINARY MEDICINE   (United States)

Author keywords

Alix; budding; Ebola; ESCRT; filovirus; L domain; virus host interaction; VLPs

Indexed keywords

ALIX PROTEIN; ESCRT PROTEIN; PROTEIN VP40; UNCLASSIFIED DRUG; CALCIUM BINDING PROTEIN; MATRIX PROTEIN; VP40 PROTEIN, VIRUS;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EBOLAVIRUS; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; VIRUS LIKE AGENT; VIRUS RELEASE; ANIMAL; CELL LINE; CHLOROCEBUS AETHIOPS; COS 1 CELL LINE; EBOLA HEMORRHAGIC FEVER; GENE DELETION; GENETICS; HEK293 CELL LINE; METABOLISM; PROTEIN TERTIARY STRUCTURE; VIROLOGY;

AMINO ACID MOTIFS; ANIMALS; CALCIUM-BINDING PROTEINS; CELL LINE; CERCOPITHECUS AETHIOPS; COS CELLS; EBOLAVIRUS; HEK293 CELLS; HEMORRHAGIC FEVER, EBOLA; HUMANS; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, TERTIARY; SEQUENCE DELETION; VIRAL MATRIX PROTEINS; VIRUS RELEASE;

EID: 84942852769     PISSN: 00221899     EISSN: 15376613     Source Type: Journal    
DOI: 10.1093/infdis/jiu838     Document Type: Article

References (59)

1. Feldmann H, Klenk HD. Filoviruses. In: Baron S, ed. Medical Microbiology. 4th ed. Galveston, TX: 1996.
2. Feldmann H, Slenczka W, Klenk HD. Emerging and reemerging of filoviruses. Arch Virol Suppl 1996; 11:77-100.
3. Hartlieb B, Weissenhorn W. Filovirus assembly and budding. Virology 2006; 344:64-70.
4. Jasenosky LD, Kawaoka Y. Filovirus budding. Virus Res 2004; 106:181-8.
5. Harty RN, Brown ME, Wang G, Huibregtse J, Hayes FP. A PPxY motif within the VP40 protein of Ebola virus interacts physically and functionally with a ubiquitin ligase: implications for filovirus budding. Proc Natl Acad Sci U S A 2000; 97:13871-6.
6. Liu Y, Harty RN. Viral and host proteins that modulate filovirus budding. Future Virol 2010; 5:481-91.
7. Johnson RF, Bell P, Harty RN. Effect of Ebola virus proteins GP, NP and VP35 on VP40 VLP morphology. Virol J 2006; 3:31.
8. Harty RN. No exit: targeting the budding process to inhibit filovirus replication. Antiviral Res 2009; 81:189-97.
9. Irie T, Licata JM, Harty RN. Functional characterization of Ebola virus L-domains using VSV recombinants. Virology 2005; 336:291-8.
10. Licata JM, Simpson-Holley M,Wright NT, Han Z, Paragas J, Harty RN. Overlapping motifs (PTAP and PPEY) within the Ebola virus VP40 protein function independently as late budding domains: involvement of host proteins TSG101 and VPS-4. J Virol 2003; 77:1812-9.
11. Neumann G, Ebihara H, Takada A, et al. Ebola virus VP40 late domains are not essential for viral replication in cell culture. J Virol 2005; 79:10300-7.
12. Noda T, Sagara H, Suzuki E, Takada A, Kida H, Kawaoka Y. Ebola virus VP40 drives the formation of virus-like filamentous particles along with GP. J Virol 2002; 76:4855-65.
13. Urata S, Noda T, Kawaoka Y, Morikawa S, Yokosawa H, Yasuda J. 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 2007; 81:4895-9.
14. Timmins J, Schoehn G, Ricard-Blum S, et al. Ebola virus matrix protein VP40 interaction with human cellular factors Tsg101 and Nedd4. J Mol Biol 2003; 326:493-502.
15. Timmins J, Scianimanico S, Schoehn G, Weissenhorn W. Vesicular release of ebola virus matrix protein VP40. Virology 2001; 283:1-6.
16. Bieniasz PD. Late budding domains and host proteins in enveloped virus release. Virology 2006; 344:55-63.
17. Martin-Serrano J, Zang T, Bieniasz PD. HIV-1 and Ebola virus encode small peptide motifs that recruit Tsg101 to sites of particle assembly to facilitate egress. Nat Med 2001; 7:1313-9.
18. 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; 84:7847-56.
19. Kolesnikova L, Bohil AB, Cheney RE, Becker S. Budding of Marburgvirus is associated with filopodia. Cell Microbiol 2007; 9:939-51.
20. Kolesnikova L, Strecker T, Morita E, et al. Vacuolar protein sorting pathway contributes to the release of Marburg virus. J Virol 2009; 83:2327-37.
21. Urata S, Yasuda J. Regulation of Marburg virus (MARV) budding by Nedd4-1: A different WW domain of Nedd4.1 is critical for binding to MARV and Ebola virus VP40. J Gen Virol 2010; 91: 228-34.
22. Chen BJ, Lamb RA. Mechanisms for enveloped virus budding: can some viruses do without an ESCRT? Virology 2008; 372:221-32.
23. Rossman JS, Lamb RA. Viral membrane scission. Annu Rev Cell Dev Biol 2013; 29:551-69.
24. Zhai Q, Fisher RD, Chung HY, Myszka DG, Sundquist WI, Hill CP. Structural and functional studies of ALIX interactions with YPX(n)L late domains of HIV-1 and EIAV. Nat Struct Mol Biol 2008; 15:43-9.
25. Zhai Q, Landesman MB, Chung HY, et al. Activation of the retroviral budding factor ALIX. J Virol 2011; 85:9222-6.
26. Dussupt V, Javid MP, Abou-Jaoude G, 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 2009; 5:e1000339.
27. Sette P, Dussupt V, Bouamr F. Identification of the HIV-1 NC binding interface in Alix Bro1 reveals a role for RNA. J Virol 2012; 86:11608-15.
28. Sette P, Jadwin JA, Dussupt V, Bello NF, Bouamr F. The ESCRTassociated protein Alix recruits the ubiquitin ligase Nedd4-1 to facilitate HIV-1 release through the LYPXnL L domain motif. J Virol 2010; 84: 8181-92.
29. Sette P, Mu R, Dussupt V, et al. The Phe105 loop of Alix Bro1 domain plays a key role in HIV-1 release. Structure 2011; 19:1485-95.
30. 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; 114:689-99.
31. 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; 128:841-52.
32. Fujii K, Hurley JH, Freed EO. Beyond Tsg101: The role of Alix in 'ESCRTing' HIV-1. Nat Rev Microbiol 2007; 5:912-6.
33. Lee S, Joshi A, Nagashima K, Freed EO, Hurley JH. Structural basis for viral late-domain binding to Alix. Nat Struct Mol Biol 2007; 14:194-9.
34. Martin-Serrano J, Marsh M. ALIX catches HIV. Cell Host Microbe 2007; 1:5-7.
35. 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; 81:6614-22.
36. Lazert C, Chazal N, Briant L, Gerlier D, Cortay JC. Refined study of the interaction between HIV-1 p6 late domain and ALIX. Retrovirology 2008; 5:39.
37. Zhou X, Pan S, Sun L, Corvera J, Lin SH, Kuang J. The HIV-1 p6/EIAV p9 docking site in Alix is autoinhibited as revealed by a conformationsensitive anti-Alix monoclonal antibody. Biochem J 2008; 414:215-20.
38. Fujii K, Munshi UM, Ablan SD, et al. Functional role of Alix in HIV-1 replication. Virology 2009; 391:284-92.
39. Usami Y, Popov S, Popova E, Inoue M,WeissenhornW, Göttlinger HG. The ESCRT pathway and HIV-1 budding. Biochem Soc Trans 2009; 37:181-4.
40. Jouvenet N, Zhadina M, Bieniasz PD, Simon SM. Dynamics of ESCRT protein recruitment during retroviral assembly. Nat Cell Biol 2011; 13:394-401.
41. Sandrin V, Sundquist WI. ESCRT requirements for EIAV budding. Retrovirology 2013; 10:104.
42. Sharma A, Bruns K, Roder R, et al. Solution structure of the equine infectious anemia virus p9 protein: A rationalization of its different ALIX binding requirements compared to the analogous HIV-p6 protein. BMC Struct Biol 2009; 9:74.
43. Bissig C, Gruenberg J. ALIX and the multivesicular endosome: ALIX in Wonderland. Trends Cell Biol 2014; 24:19-25.
44. Lu J, Qu Y, Liu Y, et al. Host IQGAP1 and Ebola virus VP40 interactions facilitate virus-like particle egress. J Virol 2013; 87:7777-80.
45. Han Z, Lu J, Liu Y, et al. Small-Molecule Probes Targeting the Viral PPxY-Host Nedd4 Interface Block Egress of a Broad Range of RNAViruses. J Virol 2014; 88:7294-306.
46. Lu J, Han Z, Liu Y, et al. A host-oriented inhibitor of Junin Argentine hemorrhagic fever virus egress. J Virol 2014; 88:4736-43.
47. Boonyaratanakornkit J, Schomacker H, Collins P, Schmidt A. Alix serves as an adaptor that allows human parainfluenza virus type 1 to interact with the host cell ESCRT system. PloS One 2013; 8:e59462.
48. Usami Y, Popov S, Weiss ER, Vriesema-Magnuson C, Calistri A, Gottlinger HG. Regulation of CHMP4/ESCRT-III Function in Human Immunodeficiency Virus Type 1 Budding by CC2D1A. J Virol 2012; 86:3746-56.
49. Fisher RD, Wang B, Alam SL, et al. Structure and ubiquitin binding of the ubiquitin-interacting motif. J Biol Chem 2003; 278:28976-84.
50. Gottlinger HG. How HIV-1 hijacks ALIX. Nat Struct Mol Biol 2007; 14:254-6.
51. Patch JR, Han Z, McCarthy SE, et al. The YPLGVG sequence of the Nipah virus matrix protein is required for budding. Virol J 2008; 5:137.
52. Dilley KA, Gregory D, Johnson MC, Vogt VM. An LYPSL late domain in the gag protein contributes to the efficient release and replication of Rous sarcoma virus. J Virol 2010; 84:6276-87.
53. Irie T, Inoue M, Sakaguchi T. Significance of the YLDL motif in the M protein and Alix/AIP1 for Sendai virus budding in the context of virus infection. Virology 2010; 405:334-41.
54. Irie T, Shimazu Y, Yoshida T, Sakaguchi T. The YLDL sequence within Sendai virus M protein is critical for budding of virus-like particles and interacts with Alix/AIP1 independently of C protein. J Virol 2007; 81:2263-73.
55. Zhai Q, Landesman MB, Robinson H, Sundquist WI, Hill CP. Identification and structural characterization of the ALIX-binding late domains of simian immunodeficiency virus SIVmac239 and SIVagmTan-1. J Virol 2011; 85:632-7.
56. Bello NF, Dussupt V, Sette P, et al. Budding of retroviruses utilizing divergent L domains requires nucleocapsid. J Virol 2012; 86: 4182-93.
57. Weissenhorn W, Gottlinger H. Essential ingredients for HIV-1 budding. Cell Host Microbe 2011; 9:172-4.
58. Zhai Q, Landesman MB, Robinson H, Sundquist WI, Hill CP. Structure of the Bro1 domain protein BROX and functional analyses of the ALIX Bro1 domain in HIV-1 budding. PloS One 2011; 6:e27466.
59. Zhou X, Si J, Corvera J, Gallick GE, Kuang J. Decoding the intrinsic mechanism that prohibits ALIX interaction with ESCRT and viral proteins. Biochem J 2010; 432:525-34.