Nipah Virus C Protein Recruits Tsg101 to Promote the Efficient Release of Virus in an ESCRT-Dependent Pathway

PLoS Pathogens

Volumn 12, Issue 5, 2016, Pages

  Park, Arnold ^a,b   Yun, Tatyana ^c   Vigant, Frederic ^b   Pernet, Olivier ^a   Won, Sohui T ^b   Dawes, Brian E ^c   Bartkowski, Wojciech ^a   Freiberg, Alexander N ^c,d   Lee, Benhur ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c University of Texas Medical Branch School of Medicine   (United States)

^d UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESCRT PROTEIN; NIPAH VIRUS C PROTEIN; RECOMBINANT PROTEIN; TUMOR SUSCEPTIBILITY GENE 101 PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN; VPS28 PROTEIN; C PROTEIN, NIPAH VIRUS; DNA BINDING PROTEIN; PHOSPHOPROTEIN; TRANSCRIPTION FACTOR; VIRAL PROTEIN;

ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; INNATE IMMUNITY; NIPAH C VIRUS; NIPAH VIRUS; NIPAH VIRUS INFECTION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN INTERACTION; PROTEIN LOCALIZATION; SEQUENCE HOMOLOGY; TRANSMISSION ELECTRON MICROSCOPY; VIRUS CELL INTERACTION; VIRUS LIKE AGENT; VIRUS RELEASE; WESTERN BLOTTING; HEK293 CELL LINE; HENIPAVIRUS INFECTION; METABOLISM; PHYSIOLOGY;

BLOTTING, WESTERN; DNA-BINDING PROTEINS; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; HEK293 CELLS; HENIPAVIRUS INFECTIONS; HUMANS; IMMUNOPRECIPITATION; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; NIPAH VIRUS; PHOSPHOPROTEINS; TRANSCRIPTION FACTORS; VIRAL PROTEINS; VIRUS RELEASE;

EID: 84973300827     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005659     Document Type: Article

References (52)

1. Henne WM, Buchkovich NJ, Emr SD, (2011) The ESCRT pathway. Dev Cell21: 77–91. doi: 10.1016/j.devcel.2011.05.01521763610
2. Schmidt O, Teis D, (2012) The ESCRT machinery. Curr Biol22: R116–120. doi: 10.1016/j.cub.2012.01.02822361144
3. Votteler J, Sundquist WI, (2013) Virus budding and the ESCRT pathway. Cell Host Microbe14: 232–241. doi: 10.1016/j.chom.2013.08.01224034610
4. Bieniasz PD, (2009) The cell biology of HIV-1 virion genesis. Cell Host Microbe5: 550–558. doi: 10.1016/j.chom.2009.05.01519527882
5. Demirov DG, Freed EO, (2004) Retrovirus budding. Virus Res106: 87–102. 15567490
6. Morita E, Sundquist WI, (2004) Retrovirus budding. Annu Rev Cell Dev Biol20: 395–425. 15473846
7. Rossman JS, Jing X, Leser GP, Lamb RA, (2010) Influenza virus M2 protein mediates ESCRT-independent membrane scission. Cell142: 902–913. doi: 10.1016/j.cell.2010.08.02920850012
8. Harrison MS, Sakaguchi T, Schmitt AP, (2010) Paramyxovirus assembly and budding: building particles that transmit infections. Int J Biochem Cell Biol42: 1416–1429. doi: 10.1016/j.biocel.2010.04.00520398786
9. Patch JR, Crameri G, Wang LF, Eaton BT, Broder CC, (2007) Quantitative analysis of Nipah virus proteins released as virus-like particles reveals central role for the matrix protein. Virol J4: 1. 17204159
10. Patch JR, Han Z, McCarthy SE, Yan L, Wang LF, et al. (2008) The YPLGVG sequence of the Nipah virus matrix protein is required for budding. Virol J5: 137. doi: 10.1186/1743-422X-5-13719000317
11. Ciancanelli MJ, Basler CF, (2006) Mutation of YMYL in the Nipah virus matrix protein abrogates budding and alters subcellular localization. J Virol80: 12070–12078. 17005661
12. Irie T, Nagata N, Yoshida T, Sakaguchi T, (2008) Recruitment of Alix/AIP1 to the plasma membrane by Sendai virus C protein facilitates budding of virus-like particles. Virology371: 108–120. 18028977
13. Sakaguchi T, Kato A, Sugahara F, Shimazu Y, Inoue M, et al. (2005) AIP1/Alix is a binding partner of Sendai virus C protein and facilitates virus budding. J Virol79: 8933–8941. 15994787
14. Sugahara F, Uchiyama T, Watanabe H, Shimazu Y, Kuwayama M, et al. (2004) Paramyxovirus Sendai virus-like particle formation by expression of multiple viral proteins and acceleration of its release by C protein. Virology325: 1–10. 15231380
15. Gosselin-Grenet AS, Marq JB, Abrami L, Garcin D, Roux L, (2007) Sendai virus budding in the course of an infection does not require Alix and VPS4A host factors. Virology365: 101–112. 17467023
16. Garner OB, Yun T, Pernet O, Aguilar HC, Park A, et al. (2015) Timing of galectin-1 exposure differentially modulates Nipah virus entry and syncytium formation in endothelial cells. J Virol89: 2520–2529. doi: 10.1128/JVI.02435-1425505064
17. Pernet O, Schneider BS, Beaty SM, LeBreton M, Yun TE, et al. (2014) Evidence for henipavirus spillover into human populations in Africa. Nat Commun5: 5342. doi: 10.1038/ncomms634225405640
18. Yun T, Park A, Hill TE, Pernet O, Beaty SM, et al. (2015) Efficient reverse genetics reveals genetic determinants of budding and fusogenic differences between Nipah and Hendra viruses and enables real-time monitoring of viral spread in small animal models of henipavirus infection. J Virol89: 1242–1253. doi: 10.1128/JVI.02583-1425392218
19. Ciancanelli MJ, Volchkova VA, Shaw ML, Volchkov VE, Basler CF, (2009) Nipah virus sequesters inactive STAT1 in the nucleus via a P gene-encoded mechanism. J Virol83: 7828–7841. doi: 10.1128/JVI.02610-0819515782
20. Lo MK, Peeples ME, Bellini WJ, Nichol ST, Rota PA, et al. (2012) Distinct and overlapping roles of Nipah virus P gene products in modulating the human endothelial cell antiviral response. PLoS One7: e47790. doi: 10.1371/journal.pone.004779023094089
21. Mathieu C, Guillaume V, Volchkova VA, Pohl C, Jacquot F, et al. (2012) Nonstructural Nipah virus C protein regulates both the early host proinflammatory response and viral virulence. J Virol86: 10766–10775. doi: 10.1128/JVI.01203-1222837207
22. Yoneda M, Guillaume V, Sato H, Fujita K, Georges-Courbot MC, et al. (2010) The nonstructural proteins of Nipah virus play a key role in pathogenicity in experimentally infected animals. PLoS One5: e12709. doi: 10.1371/journal.pone.001270920856799
23. Park MS, Shaw ML, Munoz-Jordan J, Cros JF, Nakaya T, et al. (2003) Newcastle disease virus (NDV)-based assay demonstrates interferon-antagonist activity for the NDV V protein and the Nipah virus V, W, and C proteins. J Virol77: 1501–1511. 12502864
24. Lo MK, Harcourt BH, Mungall BA, Tamin A, Peeples ME, et al. (2009) Determination of the henipavirus phosphoprotein gene mRNA editing frequencies and detection of the C, V and W proteins of Nipah virus in virus-infected cells. J Gen Virol90: 398–404. doi: 10.1099/vir.0.007294-019141449
25. Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJ, (2015) The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc10: 845–858. doi: 10.1038/nprot.2015.05325950237
26. Gill DJ, Teo H, Sun J, Perisic O, Veprintsev DB, et al. (2007) Structural insight into the ESCRT-I/-II link and its role in MVB trafficking. EMBO J26: 600–612. 17215868
27. Peterson TA, Yu L, Piper RC, (2015) Backbone and side-chain NMR assignments for the C-terminal domain of mammalian Vps28. Biomol NMR Assign9: 21–24. doi: 10.1007/s12104-013-9537-824366722
28. Pineda-Molina E, Belrhali H, Piefer AJ, Akula I, Bates P, et al. (2006) The crystal structure of the C-terminal domain of Vps28 reveals a conserved surface required for Vps20 recruitment. Traffic7: 1007–1016. 16749904
29. McDonald B, Martin-Serrano J, (2009) No strings attached: the ESCRT machinery in viral budding and cytokinesis. J Cell Sci122: 2167–2177. doi: 10.1242/jcs.02830819535732
30. Im YJ, Hurley JH, (2008) Integrated structural model and membrane targeting mechanism of the human ESCRT-II complex. Dev Cell14: 902–913. doi: 10.1016/j.devcel.2008.04.00418539118
31. Martin-Serrano J, Zang T, Bieniasz PD, (2003) Role of ESCRT-I in retroviral budding. J Virol77: 4794–4804. 12663786
32. Bishop N, Woodman P, (2001) TSG101/mammalian VPS23 and mammalian VPS28 interact directly and are recruited to VPS4-induced endosomes. J Biol Chem276: 11735–11742. 11134028
33. Stuchell MD, Garrus JE, Muller B, Stray KM, Ghaffarian S, et al. (2004) The human endosomal sorting complex required for transport (ESCRT-I) and its role in HIV-1 budding. J Biol Chem279: 36059–36071. 15218037
34. Krempler A, Henry MD, Triplett AA, Wagner KU, (2002) Targeted deletion of the Tsg101 gene results in cell cycle arrest at G1/S and p53-independent cell death. J Biol Chem277: 43216–43223. 12205095
35. Wagner KU, Krempler A, Qi Y, Park K, Henry MD, et al. (2003) Tsg101 is essential for cell growth, proliferation, and cell survival of embryonic and adult tissues. Mol Cell Biol23: 150–162. 12482969
36. Park A, Won ST, Pentecost M, Bartkowski W, Lee B, (2014) CRISPR/Cas9 allows efficient and complete knock-in of a destabilization domain-tagged essential protein in a human cell line, allowing rapid knockdown of protein function. PLoS One9: e95101. doi: 10.1371/journal.pone.009510124743236
37. Strandin T, Hepojoki J, Vaheri A, (2013) Cytoplasmic tails of bunyavirus Gn glycoproteins-Could they act as matrix protein surrogates?Virology437: 73–80. doi: 10.1016/j.virol.2013.01.00123357734
38. Marsh GA, de Jong C, Barr JA, Tachedjian M, Smith C, et al. (2012) Cedar virus: a novel Henipavirus isolated from Australian bats. PLoS Pathog8: e1002836. doi: 10.1371/journal.ppat.100283622879820
39. Drexler JF, Corman VM, Muller MA, Maganga GD, Vallo P, et al. (2012) Bats host major mammalian paramyxoviruses. Nat Commun3: 796. doi: 10.1038/ncomms179622531181
40. Wu Z, Yang L, Yang F, Ren X, Jiang J, et al. (2014) Novel Henipa-like virus, Mojiang Paramyxovirus, in rats, China, 2012. Emerg Infect Dis20: 1064–1066. doi: 10.3201/eid2006.13102224865545
41. Chen BJ, Lamb RA, (2008) Mechanisms for enveloped virus budding: can some viruses do without an ESCRT?Virology372: 221–232. 18063004
42. Babst M, Odorizzi G, (2013) The balance of protein expression and degradation: an ESCRTs point of view. Curr Opin Cell Biol25: 489–494. doi: 10.1016/j.ceb.2013.05.00323773569
43. Siomi H, Siomi MC, (2009) RISC hitches onto endosome trafficking. Nat Cell Biol11: 1049–1051. doi: 10.1038/ncb0909-104919724258
44. Wegner CS, Rodahl LM, Stenmark H, (2011) ESCRT proteins and cell signalling. Traffic12: 1291–1297. doi: 10.1111/j.1600-0854.2011.01210.x21518165
45. Lo MK, Sogaard TM, Karlin DG, (2014) Evolution and structural organization of the C proteins of paramyxovirinae. PLoS One9: e90003. doi: 10.1371/journal.pone.009000324587180
46. Shnyrova AV, Ayllon J, Mikhalyov II, Villar E, Zimmerberg J, et al. (2007) Vesicle formation by self-assembly of membrane-bound matrix proteins into a fluidlike budding domain. J Cell Biol179: 627–633. 18025300
47. Lee B, Pernet O, Ahmed AA, Zeltina A, Beaty SM, et al. (2015) Molecular recognition of human ephrinB2 cell surface receptor by an emergent African henipavirus. Proc Natl Acad Sci U S A112: E2156–2165. doi: 10.1073/pnas.150169011225825759
48. Boonyaratanakornkit J, Schomacker H, Collins P, Schmidt A, (2013) Alix serves as an adaptor that allows human parainfluenza virus type 1 to interact with the host cell ESCRT system. PLoS One8: e59462. doi: 10.1371/journal.pone.005946223527201
49. Iwamoto M, Bjorklund T, Lundberg C, Kirik D, Wandless TJ, (2010) A general chemical method to regulate protein stability in the mammalian central nervous system. Chem Biol17: 981–988. doi: 10.1016/j.chembiol.2010.07.00920851347
50. Wang YE, Park A, Lake M, Pentecost M, Torres B, et al. (2010) Ubiquitin-regulated nuclear-cytoplasmic trafficking of the Nipah virus matrix protein is important for viral budding. PLoS Pathog6: e1001186. doi: 10.1371/journal.ppat.100118621085610
51. Levroney EL, Aguilar HC, Fulcher JA, Kohatsu L, Pace KE, et al. (2005) Novel innate immune functions for galectin-1: galectin-1 inhibits cell fusion by Nipah virus envelope glycoproteins and augments dendritic cell secretion of proinflammatory cytokines. J Immunol175: 413–420. 15972675
52. Halpin K, Bankamp B, Harcourt BH, Bellini WJ, Rota PA, (2004) Nipah virus conforms to the rule of six in a minigenome replication assay. J Gen Virol85: 701–707. 14993656