Identification of conserved motifs in the Westnile virus envelope essential for particle secretion

BMC Microbiology

Volumn 13, Issue 1, 2013, Pages

  Garg, Himanshu ^a   Lee, Raphael T C ^b   Tek, Ng Oon ^c   Maurer Stroh, Sebastian ^b,d   Joshi, Anjali ^a  

^a Texas Tech University Health Sciences Center El Paso   (United States)

^b BIOINFORMATICS INSTITUTE   (Singapore)

^c TAN TOCK SENG HOSPITAL   (Singapore)

^d NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

Alix; Flavivirus; HIV; Late domains; Tsg101; Virus assembly; WNV

Indexed keywords

PROTEIN; SMALL INTERFERING RNA; VIRUS ENVELOPE PROTEIN;

ARTICLE; DISULFIDE BOND; MOLECULAR MODEL; MUTATION; NONHUMAN; PROTEIN ANALYSIS; PROTEIN STRUCTURE; SITE DIRECTED MUTAGENESIS; VIRUS ASSEMBLY; VIRUS ENVELOPE; WEST NILE FLAVIVIRUS; CELL LINE; CHEMICAL STRUCTURE; GENETICS; HUMAN; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PROTEIN CONFORMATION; PROTEIN MOTIF; VIRUS RELEASE;

FLAVIVIRUS; WEST NILE VIRUS;

AMINO ACID MOTIFS; CELL LINE; CONSERVED SEQUENCE; DNA MUTATIONAL ANALYSIS; HUMANS; MODELS, MOLECULAR; PROTEIN CONFORMATION; VIRAL ENVELOPE PROTEINS; VIRUS RELEASE; WEST NILE VIRUS;

EID: 84883276255     PISSN: None     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-13-197     Document Type: Article

References (72)

1. The molecular biology of West Nile Virus: a new invader of the western hemisphere. Brinton MA, Annu Rev Microbiol 2002 56 371 402 10.1146/annurev. micro.56.012302.160654 12142476 (Pubitemid 35217460)
2. Lindenbach BD, Thiel HJ, Rice CM, Flaviviridae: the viruses and their replication Philadelphia, PA: Fields virology Lippincott William & Wilkins 2007 1101 1152
3. Mutations in the West Nile prM protein affect VLP and virion secretion in vitro. Calvert AE, Huang CY, Blair CD, Roehrig JT, Virology 2012 433 35 44 10.1016/j.virol.2012.07.011 22858174
4. Identification of residues in West Nile virus pre-membrane protein that influence viral particle secretion and virulence. Setoh YX, Prow NA, Hobson-Peters J, Lobigs M, Young PR, Khromykh AA, Hall RA, J Gen Virol 2012 93 1965 1975 10.1099/vir.0.044453-0 22764317
5. Identifying the region influencing the cis-mode of maturation of West Nile (Sarafend) virus using chimeric infectious clones. Li J, Bhuvanakantham R, Howe J, Ng ML, Biochem Biophys Res Commun 2005 334 714 720 10.1016/j.bbrc.2005. 06.150 16018972 (Pubitemid 40982425)
6. Assembly and maturation of the flavivirus Kunjin virus appear to occur in the rough endoplasmic reticulum and along the secretory pathway, respectively. Mackenzie JM, Westaway EG, J Virol 2001 75 10787 10799 10.1128/JVI.75.22.10787- 10799.2001 11602720 (Pubitemid 33031548)
7. Maturation of Japanese encephalitis virus glycoproteins produced by infected mammalian and mosquito cells. Mason PW, Virology 1989 169 354 364 10.1016/0042-6822(89)90161-X 2523178 (Pubitemid 19105920)
8. Analyses of the terminal sequences of West Nile virus structural proteins and of the in vitro translation of these proteins allow the proposal of a complete scheme of the proteolytic cleavages involved in their synthesis. Nowak T, Farber PM, Wengler G, Virology 1989 169 365 376 10.1016/0042-6822(89)90162-1 2705302 (Pubitemid 19105921)
9. Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Garrus JE, von Schwedler UK, Pornillos OW, Morham SG, Zavitz KH, Wang HE, Wettstein DA, Stray KM, Cote M, Rich RL, et al. Cell 2001 107 55 65 10.1016/S0092-8674(01)00506-2 11595185 (Pubitemid 32972037)
10. Effect of mutations affecting the p6 gag protein on human immunodeficiency virus particle release. Gottlinger HG, Dorfman T, Sodroski JG, Haseltine WA, Proc Natl Acad Sci USA 1991 88 3195 3199 10.1073/pnas.88.8.3195 2014240 (Pubitemid 21916586)
11. Divergent retroviral late-budding domains recruit vacuolar protein sorting factors by using alternative adaptor proteins. Martin-Serrano J, Yarovoy A, Perez-Caballero D, Bieniasz PD, Proc Natl Acad Sci USA 2003 100 12414 12419 10.1073/pnas.2133846100 14519844 (Pubitemid 37271574)
12. AIP1/ALIX is a binding partner for HIV-1 p6 and EIAV p9 functioning in virus budding. Strack B, Calistri A, Craig S, Popova E, Gottlinger HG, Cell 2003 114 689 699 10.1016/S0092-8674(03)00653-6 14505569 (Pubitemid 37186765)
13. Fine mapping and characterization of the Rous sarcoma virus Pr76gag late assembly domain. Xiang Y, Cameron CE, Wills JW, Leis J, J Virol 1996 70 5695 5700 8764091 (Pubitemid 26240754)
14. Viral late domains. Freed EO, J Virol 2002 76 4679 4687 10.1128/JVI.76.10.4679-4687.2002 11967285 (Pubitemid 34441674)
15. Late domain function identified in the vesicular stomatitis virus M protein by use of rhabdovirus-retrovirus chimeras. Craven RC, Harty RN, Paragas J, Palese P, Wills JW, J Virol 1999 73 3359 3365 10074190 (Pubitemid 29135729)
16. A proline-rich motif within the matrix protein of vesicular stomatitis virus and rabies virus interacts with WW domains of cellular proteins: implications for viral budding. Harty RN, Paragas J, Sudol M, Palese P, J Virol 1999 73 2921 2929 10074141 (Pubitemid 29135680)
17. Mutations in the PPPY motif of vesicular stomatitis virus matrix protein reduce virus budding by inhibiting a late step in virion release. Jayakar HR, Murti KG, Whitt MA, J Virol 2000 74 9818 9827 10.1128/JVI.74.21.9818-9827.2000 11024108
18. A PPxY motif within the VP40 protein of Ebola virus interacts physically and functionally with a ubiquitin ligase: implications for filovirus budding. Harty RN, Brown ME, Wang G, Huibregtse J, Hayes FP, Proc Natl Acad Sci USA 2000 97 13871 13876 10.1073/pnas.250277297 11095724
19. The matrix protein of Marburg virus is transported to the plasma membrane along cellular membranes: exploiting the retrograde late endosomal pathway. Kolesnikova L, Bamberg S, Berghofer B, Becker S, J Virol 2004 78 2382 2393 10.1128/JVI.78.5.2382-2393.2004 14963134 (Pubitemid 38228931)
20. 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. Licata JM, Simpson-Holley M, Wright NT, Han Z, Paragas J, Harty RN, J Virol 2003 77 1812 1819 10.1128/JVI.77.3.1812-1819.2003 12525615 (Pubitemid 36109993)
21. HIV-1 and Ebola virus encode small peptide motifs that recruit Tsg101 to sites of particle assembly to facilitate egress. Martin-Serrano J, Zang T, Bieniasz PD, Nat Med 2001 7 1313 1319 10.1038/nm1201-1313 11726971 (Pubitemid 34007935)
22. 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. Urata S, Noda T, Kawaoka Y, Morikawa S, Yokosawa H, Yasuda J, J Virol 2007 81 4895 4899 10.1128/JVI.02829-06 17301151 (Pubitemid 46668689)
23. The small RING finger protein Z drives arenavirus budding: implications for antiviral strategies. Perez M, Craven RC, de la Torre JC, Proc Natl Acad Sci USA 2003 100 12978 12983 10.1073/pnas.2133782100 14563923 (Pubitemid 37340011)
24. Cellular factors required for Lassa virus budding. Urata S, Noda T, Kawaoka Y, Yokosawa H, Yasuda J, J Virol 2006 80 4191 4195 10.1128/JVI.80.8. 4191-4195.2006 16571837
25. Mutation of YMYL in the Nipah virus matrix protein abrogates budding and alters subcellular localization. Ciancanelli MJ, Basler CF, J Virol 2006 80 12070 12078 10.1128/JVI.01743-06 17005661 (Pubitemid 44904357)
26. AIP1/Alix is a binding partner of Sendai virus C protein and facilitates virus budding. Sakaguchi T, Kato A, Sugahara F, Shimazu Y, Inoue M, Kiyotani K, Nagai Y, Yoshida T, J Virol 2005 79 8933 8941 10.1128/JVI.79.14.8933-8941.2005 15994787 (Pubitemid 40934804)
27. Intracellular trafficking and maturation of herpes simplex virus type 1 gB and virus egress require functional biogenesis of multivesicular bodies. Calistri A, Sette P, Salata C, Cancellotti E, Forghieri C, Comin A, Gottlinger H, Campadelli-Fiume G, Palu G, Parolin C, J Virol 2007 81 11468 11478 10.1128/JVI.01364-07 17686835 (Pubitemid 47536117)
28. Role of the TSG101 gene in Epstein-Barr virus late gene transcription. Chua HH, Lee HH, Chang SS, Lu CC, Yeh TH, Hsu TY, Cheng TH, Cheng JT, Chen MR, Tsai CH, J Virol 2007 81 2459 2471 10.1128/JVI.02289-06 17182691
29. Herpes simplex virus type 1 cytoplasmic envelopment requires functional Vps4. Crump CM, Yates C, Minson T, J Virol 2007 81 7380 7387 10.1128/JVI.00222-07 17507493 (Pubitemid 47047827)
30. The vaccinia virus F13L YPPL motif is required for efficient release of extracellular enveloped virus. Honeychurch KM, Yang G, Jordan R, Hruby DE, J Virol 2007 81 7310 7315 10.1128/JVI.00034-07 17475658 (Pubitemid 46986670)
31. Potent inhibition of human Hepatitis B virus replication by a host factor Vps4. Kian Chua P, Lin MH, Shih C, Virology 2006 354 1 6 10.1016/j.virol.2006. 07.018 16920176 (Pubitemid 44441515)
32. Hepatitis B virus maturation is sensitive to functional inhibition of ESCRT-III, Vps4, and gamma 2-adaptin. Lambert C, Doring T, Prange R, J Virol 2007 81 9050 9060 10.1128/JVI.00479-07 17553870 (Pubitemid 47311448)
33. Involvement of host cellular multivesicular body functions in hepatitis B virus budding. Watanabe T, Sorensen EM, Naito A, Schott M, Kim S, Ahlquist P, Proc Natl Acad Sci USA 2007 104 10205 10210 10.1073/pnas.0704000104 17551004 (Pubitemid 47175287)
34. Association of Japanese encephalitis virus NS3 protein with microtubules and tumour susceptibility gene 101 (TSG101) protein. Chiou CT, Hu CC, Chen PH, Liao CL, Lin YL, Wang JJ, J Gen Virol 2003 84 2795 2805 10.1099/vir.0.19201-0 13679614 (Pubitemid 37220258)
35. Interaction between the yellow fever virus nonstructural protein NS3 and the host protein Alix contributes to the release of infectious particles. Carpp LN, Galler R, Bonaldo MC, Microbes Infect 2011 13 85 95 10.1016/j.micinf.2010. 10.010 21044891
36. Late budding domains and host proteins in enveloped virus release. Bieniasz PD, Virology 2006 344 55 63 10.1016/j.virol.2005.09.044 16364736 (Pubitemid 41814450)
37. Retrovirus budding. Demirov DG, Freed EO, Virus Res 2004 106 87 102 10.1016/j.virusres.2004.08.007 15567490 (Pubitemid 39582739)
38. N-linked glycosylation of west nile virus envelope proteins influences particle assembly and infectivity. Hanna SL, Pierson TC, Sanchez MD, Ahmed AA, Murtadha MM, Doms RW, J Virol 2005 79 13262 13274 10.1128/JVI.79.21.13262-13274. 2005 16227249 (Pubitemid 41508141)
39. Attributes of short linear motifs. Davey NE, Van Roey K, Weatheritt RJ, Toedt G, Uyar B, Altenberg B, Budd A, Diella F, Dinkel H, Gibson TJ, Molecular bioSystems 2012 8 268 281 10.1039/c1mb05231d 21909575
40. The conservation pattern of short linear motifs is highly correlated with the function of interacting protein domains. Ren S, Yang G, He Y, Wang Y, Li Y, Chen Z, BMC genomics 2008 9 452 10.1186/1471-2164-9-452 18828911
41. HIV Gag mimics the Tsg101-recruiting activity of the human Hrs protein. Pornillos O, Higginson DS, Stray KM, Fisher RD, Garrus JE, Payne M, He GP, Wang HE, Morham SG, Sundquist WI, J Cell Biol 2003 162 425 434 10.1083/jcb.200302138 12900394 (Pubitemid 36992201)
42. Database resources of the National Center for Biotechnology Information. Sayers EW, Barrett T, Benson DA, Bolton E, Bryant SH, Canese K, Chetvernin V, Church DM, Dicuccio M, Federhen S, et al. Nucleic Acids Res 2012 40 13 D25 10.1093/nar/gkr1184 22140104
43. Recent developments in the MAFFT multiple sequence alignment program. Katoh K, Toh H, Brief Bioinform 2008 9 286 298 10.1093/bib/bbn013 18372315 (Pubitemid 351890825)
44. Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ, Bioinformatics 2009 25 1189 1191 10.1093/bioinformatics/btp033 19151095
45. Domain enhanced lookup time accelerated BLAST. Boratyn GM, Schaffer AA, Agarwala R, Altschul SF, Lipman DJ, Madden TL, Biol Direct 2012 7 12 10.1186/1745-6150-7-12 22510480
46. A rapid and quantitative assay for measuring antibody-mediated neutralization of West Nile virus infection. Pierson TC, Sanchez MD, Puffer BA, Ahmed AA, Geiss BJ, Valentine LE, Altamura LA, Diamond MS, Doms RW, Virology 2006 346 53 65 10.1016/j.virol.2005.10.030 16325883 (Pubitemid 43254699)
47. Targeting the HIV entry, assembly and release pathways for anti-HIV gene therapy. Joshi A, Garg H, Ablan S, Freed EO, Nagashima K, Manjunath N, Shankar P, Virology 2011 415 95 106 10.1016/j.virol.2011.03.028 21529874
48. Overexpression of the N-terminal domain of TSG101 inhibits HIV-1 budding by blocking late domain function. Demirov DG, Ono A, Orenstein JM, Freed EO, Proc Natl Acad Sci USA 2002 99 955 960 10.1073/pnas.032511899 11805336 (Pubitemid 34106617)
49. Defects in human immunodeficiency virus budding and endosomal sorting induced by TSG101 overexpression. Goila-Gaur R, Demirov DG, Orenstein JM, Ono A, Freed EO, J Virol 2003 77 6507 6519 10.1128/JVI.77.11.6507-6519.2003 12743307 (Pubitemid 36588420)
50. TSG101/mammalian VPS23 and mammalian VPS28 interact directly and are recruited to VPS4-induced endosomes. Bishop N, Woodman P, J Biol Chem 2001 276 11735 11742 10.1074/jbc.M009863200 11134028
51. Functional replacement of a retroviral late domain by ubiquitin fusion. Joshi A, Munshi U, Ablan SD, Nagashima K, Freed EO, Traffic 2008 9 1972 1983 10.1111/j.1600-0854.2008.00817.x 18817521
52. Late domain-dependent inhibition of equine infectious anemia virus budding. Shehu-Xhilaga M, Ablan S, Demirov DG, Chen C, Montelaro RC, Freed EO, J Virol 2004 78 724 732 10.1128/JVI.78.2.724-732.2004 14694104 (Pubitemid 38067594)
53. Structural basis for viral late-domain binding to Alix. Lee S, Joshi A, Nagashima K, Freed EO, Hurley JH, Nat Struct Mol Biol 2007 14 194 199 10.1038/nsmb1203 17277784 (Pubitemid 46355573)
54. An Alix fragment potently inhibits HIV-1 budding: characterization of binding to retroviral YPXL late domains. Munshi UM, Kim J, Nagashima K, Hurley JH, Freed EO, J Biol Chem 2007 282 3847 3855 17158451 (Pubitemid 47084496)
55. Proline-rich sequence recognition: II. Proteomics analysis of Tsg101 ubiquitin-E2-like variant (UEV) interactions. Schlundt A, Sticht J, Piotukh K, Kosslick D, Jahnke N, Keller S, Schuemann M, Krause E, Freund C, Mol Cell Proteomics 2009 8 2474 2486 10.1074/mcp.M800337-MCP200 19542561
56. The late domain of human immunodeficiency virus type 1 p6 promotes virus release in a cell type-dependent manner. Demirov DG, Orenstein JM, Freed EO, J Virol 2002 76 105 117 10.1128/JVI.76.1.105-117.2002 11739676 (Pubitemid 33138996)
57. Increasing the precision of comparative models with YASARA NOVA-a self-parameterizing force field. Krieger E, Koraimann G, Vriend G, Proteins 2002 47 393 402 10.1002/prot.10104 11948792 (Pubitemid 34438688)
58. Crystal structure of the West Nile virus envelope glycoprotein. Nybakken GE, Nelson CA, Chen BR, Diamond MS, Fremont DH, J Virol 2006 80 11467 11474 10.1128/JVI.01125-06 16987985 (Pubitemid 44788862)
59. Neutralization of West Nile virus by cross-linking of its surface proteins with Fab fragments of the human monoclonal antibody CR4354. Kaufmann B, Vogt MR, Goudsmit J, Holdaway HA, Aksyuk AA, Chipman PR, Kuhn RJ, Diamond MS, Rossmann MG, Proc Natl Acad Sci USA 2010 107 18950 18955 10.1073/pnas.1011036107 20956322
60. Herpes simplex virus type 1 production requires a functional ESCRT-III complex but is independent of TSG101 and ALIX expression. Pawliczek T, Crump CM, J Virol 2009 83 11254 11264 10.1128/JVI.00574-09 19692479
61. L-domain flanking sequences are important for host interactions and efficient budding of vesicular stomatitis virus recombinants. Irie T, Harty RN, J Virol 2005 79 12617 12622 10.1128/JVI.79.20.12617-12622.2005 16188963 (Pubitemid 41433180)
62. Functional analysis of late-budding domain activity associated with the PSAP motif within the vesicular stomatitis virus M protein. Irie T, Licata JM, Jayakar HR, Whitt MA, Bell P, Harty RN, J Virol 2004 78 7823 7827 10.1128/JVI.78.14.7823-7827.2004 15220457 (Pubitemid 38915929)
63. ALIX is a Lys63-specific polyubiquitin binding protein that functions in retrovirus budding. Dowlatshahi DP, Sandrin V, Vivona S, Shaler TA, Kaiser SE, Melandri F, Sundquist WI, Kopito RR, Dev Cell 2012 23 1247 1254 10.1016/j.devcel.2012.10.023 23201121
64. Structure-based in silico identification of ubiquitin-binding domains provides insights into the ALIX-V:ubiquitin complex and retrovirus budding. Keren-Kaplan T, Attali I, Estrin M, Kuo LS, Farkash E, Jerabek-Willemsen M, Blutraich N, Artzi S, Peri A, Freed EO, et al. The EMBO journal 2013 32 538 551 10.1038/emboj.2013.4 23361315
65. MKRN1 induces degradation of West Nile virus capsid protein by functioning as an E3 ligase. Ko A, Lee EW, Yeh JY, Yang MR, Oh W, Moon JS, Song J, J Virol 2010 84 426 436 10.1128/JVI.00725-09 19846531
66. The role of ubiquitin in retroviral egress. Martin-Serrano J, Traffic 2007 8 1297 1303 10.1111/j.1600-0854.2007.00609.x 17645437 (Pubitemid 47394235)
67. Flavivirus West Nile (Sarafend) egress at the plasma membrane. Ng ML, Howe J, Sreenivasan V, Mulders JJ, Arch Virol 1994 137 303 313 10.1007/BF01309477 7944952 (Pubitemid 2133878)
68. The importance of being outer: consequences of the distinction between the outer and inner surfaces of flavivirus glycoprotein E. Seligman SJ, Bucher DJ, Trends Microbiol 2003 11 108 110 10.1016/S0966-842X(03)00005-2 12648938 (Pubitemid 36332127)
69. PCP consensus sequences of flaviviruses: correlating variance with vector competence and disease phenotype. Danecek P, Lu W, Schein CH, Journal of molecular biology 2010 396 550 563 10.1016/j.jmb.2009.11.070 19969003
70. Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. Adachi A, Gendelman HE, Koenig S, Folks T, Willey R, Rabson A, Martin MA, J Virol 1986 59 284 291 3016298 (Pubitemid 16013975)
71. Budding of equine infectious anemia virus is insensitive to proteasome inhibitors. Patnaik A, Chau V, Li F, Montelaro RC, Wills JW, J Virol 2002 76 2641 2647 10.1128/JVI.76.6.2641-2647.2002 11861830 (Pubitemid 34184849)
72. Single amino acid changes in the human immunodeficiency virus type 1 matrix protein block virus particle production. Freed EO, Orenstein JM, Buckler-White AJ, Martin MA, J Virol 1994 68 5311 5320 8035531 (Pubitemid 24226606)