Ubiquitin-regulated nuclear-cytoplasmic trafficking of the Nipah virus matrix protein is important for viral budding

PLoS Pathogens

Volumn 6, Issue 11, 2010, Pages

  Wang, Yao E ^a   Park, Arnold ^a   Lake, Michael ^a   Pentecost, Mickey ^a   Torres, Betsabe ^a   Yun, Tatyana E ^b   Wolf, Mike C ^a   Holbrook, Michael R ^b,c   Freiberg, Alexander N ^b   Lee, Benhur ^a,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

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

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; BORTEZOMIB; LEUCINE; LYSINE; MATRIX PROTEIN; MUTANT PROTEIN; PROTEASOME INHIBITOR; UBIQUITIN; BORONIC ACID DERIVATIVE; MESSENGER RNA; PROTEINASE INHIBITOR; PYRAZINE DERIVATIVE;

ANTIVIRAL SUSCEPTIBILITY; ARTICLE; CELL MEMBRANE; CELL TRANSPORT; CONTROLLED STUDY; CYTOPLASM; FEMALE; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; NIPAH VIRUS; NIPAH VIRUS INFECTION; NONHUMAN; NUCLEAR IMPORT; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN TRANSPORT; UBIQUITINATION; VIRUS ASSEMBLY; VIRUS ENCEPHALITIS; VIRUS ENTRY; VIRUS RELEASE; AMINO ACID SEQUENCE; ANIMAL; CELL NUCLEUS; CERCOPITHECUS; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; HELA CELL; HENIPAVIRUS INFECTION; IMMUNOPRECIPITATION; KIDNEY; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEAR LOCALIZATION SIGNAL; PATHOGENICITY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY; VERO CELL; VIROLOGY; VIRUS SHEDDING; WESTERN BLOTTING;

NIPAH VIRUS; PARAMYXOVIRIDAE;

AMINO ACID SEQUENCE; ANIMALS; BLOTTING, WESTERN; BORONIC ACIDS; CELL NUCLEUS; CERCOPITHECUS AETHIOPS; CYTOPLASM; FLUORESCENT ANTIBODY TECHNIQUE; HELA CELLS; HENIPAVIRUS INFECTIONS; HUMANS; IMMUNOPRECIPITATION; KIDNEY; MOLECULAR SEQUENCE DATA; MUTATION; NIPAH VIRUS; NUCLEAR LOCALIZATION SIGNALS; PROTEASE INHIBITORS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; PYRAZINES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEQUENCE HOMOLOGY, AMINO ACID; UBIQUITIN; VERO CELLS; VIRAL MATRIX PROTEINS; VIRUS ASSEMBLY; VIRUS SHEDDING;

EID: 79251492016     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001186     Document Type: Article

References (71)

1. Eaton BT, Broder CC, Middleton D, Wang LF (2006) Hendra and Nipah viruses: different and dangerous. Nat Rev Microbiol 4: 23-35.
2. Field H, Young P, Yob JM, Mills J, Hall L, et al. (2001) The natural history of Hendra and Nipah viruses. Microbes Infect 3: 307-314.
3. Chua KB, Bellini WJ, Rota PA, Harcourt BH, Tamin A, et al. (2000) Nipah virus: a recently emergent deadly paramyxovirus. Science 288: 1432-1435.
4. Weingartl HM, Berhane Y, Czub M (2009) Animal models of henipavirus infection: a review. Vet J 181: 211-220.
5. Hsu VP, Hossain MJ, Parashar UD, Ali MM, Ksiazek TG, et al. (2004) Nipah virus encephalitis reemergence, Bangladesh. Emerg Infect Dis 10: 2082-2087.
6. (2009) ProMED-mail PRO/AH/EDR. Hendra virus, human, equine - Australia (04): (QL) fatal. 20090903.3098.
7. Lamb RA, Parks GD (2006) Paramyxoviridae: The Viruses and Their Replication. In: Knipe DM, Howley PM, eds. Fields Virology. Fifth ed. Philadelphia: Lippincott, Williams and Wilkins. pp 1449-1496.
8. Takimoto T, Portner A (2004) Molecular mechanism of paramyxovirus budding. Virus Res 106: 133-145.
9. Garoff H, Hewson R, Opstelten DJ (1998) Virus maturation by budding. Microbiol Mol Biol Rev 62: 1171-1190.
10. Ciancanelli MJ, Basler CF (2006) Mutation of YMYL in the Nipah virus matrix protein abrogates budding and alters subcellular localization. J Virol 80: 12070-12078.
11. 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 J 4: 1.
12. 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 J 5: 137.
13. Shaw ML, Cardenas WB, Zamarin D, Palese P, Basler CF (2005) Nuclear localization of the Nipah virus W protein allows for inhibition of both virus- and toll-like receptor 3-triggered signaling pathways. J Virol 79: 6078-6088.
14. Shaw ML, Garcia-Sastre A, Palese P, Basler CF (2004) Nipah virus V and W proteins have a common STAT1-binding domain yet inhibit STAT1 activation from the cytoplasmic and nuclear compartments, respectively. J Virol 78: 5633-5641.
15. 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 Virol 83: 7828-7841.
16. Watanabe N, Kawano M, Tsurudome M, Kusagawa S, Nishio M, et al. (1996) Identification of the sequences responsible for nuclear targeting of the V protein of human parainfluenza virus type 2. J Gen Virol 77(Pt 2): 327-338.
17. Yoshida T, Nagai Y'Yoshii S, Maeno K, Matsumoto T (1976) Membrane (M) protein of HVJ (Sendai virus): its role in virus assembly. Virology 71: 143-161.
18. Coleman NA, Peeples ME (1993) The matrix protein of Newcastle disease virus localizes to the nucleus via a bipartite nuclear localization signal. Virology 195: 596-607.
19. Peeples ME, Wang C, Gupta KC, Coleman N (1992) Nuclear entry and nucleolar localization of the Newcastle disease virus (NDV) matrix protein occur early in infection and do not require other NDV proteins. J Virol 66: 3263-3269.
20. Peeples ME (1988) Differential detergent treatment allows immunofluorescent localization of the Newcastle disease virus matrix protein within the nucleus of infected cells. Virology 162: 255-259.
21. Ghildyal R, Ho A, Dias M, Soegiyono L, Bardin PG, et al. (2009) The respiratory syncytial virus matrix protein possesses a Crm1-mediated nuclear export mechanism. J Virol 83: 5353-5362.
22. Ghildyal R, Ho A, Wagstaff KM, Dias MM, Barton CL, et al. (2005) Nuclear import of the respiratory syncytial virus matrix protein is mediated by importin beta1 independent of importin alpha. Biochemistry 44: 12887-12895.
23. Ghildyal R, Baulch-Brown C, Mills J, Meanger J (2003) The matrix protein of Human respiratory syncytial virus localises to the nucleus of infected cells and inhibits transcription. Arch Virol 148: 1419-1429.
24. Faaberg KS, Peeples ME (1988) Strain variation and nuclear association of Newcastle disease virus matrix protein. J Virol 62: 586-593.
25. Kanwal C, Li H, Lim CS (2002) Model system to study classical nuclear export signals. AAPS PharmSci 4: E18.
26. Terry LJ, Shows EB, Wente SR (2007) Crossing the nuclear envelope: hierarchical regulation of nucleocytoplasmic transport. Science 318: 1412-1416.
27. Dingwall C, Laskey RA (1991) Nuclear targeting sequences-a consensus? Trends Biochem Sci 16: 478-481.
28. Efthymiadis A, Shao H, Hubner S, Jans DA (1997) Kinetic characterization of the human retinoblastoma protein bipartite nuclear localization sequence (NLS) in vivo and in vitro. A comparison with the SV40 large T-antigen NLS. J Biol Chem 272: 22134-22139.
29. Schlenstedt G (1996) Protein import into the nucleus. FEBS Lett 389: 75-79.
30. Fukuda M, Asano S, Nakamura T, Adachi M, Yoshida M, et al. (1997) CRM1 is responsible for intracellular transport mediated by the nuclear export signal. Nature 390: 308-311.
31. Kau TR, Way JC, Silver PA (2004) Nuclear transport and cancer: from mechanism to intervention. Nat Rev Cancer 4: 106-117.
32. Lohrum MA, Woods DB, Ludwig RL, Balint E, Vousden KH (2001) C-terminal ubiquitination of p53 contributes to nuclear export. Mol Cell Biol 21: 8521-8532.
33. Li M, Brooks CL, Wu-Baer F, Chen D, Baer R, et al. (2003) Mono- versus polyubiquitination: differential control of p53 fate by Mdm2. Science 302: 1972-1975.
34. Trotman LC, Wang X, Alimonti A, Chen Z, Teruya-Feldstein J, et al. (2007) Ubiquitination regulates PTEN nuclear import and tumor suppression. Cell 128: 141-156.
35. Shcherbik N, Haines DS (2004) Ub on the move. J Cell Biochem 93: 11-19.
36. Huang TT, Wuerzberger-Davis SM, Wu ZH, Miyamoto S (2003) Sequential modification of NEMO/IKKgamma by SUMO-1 and ubiquitin mediates NFkappaB activation by genotoxic stress. Cell 115: 565-576.
37. Randow F, Lehner PJ (2009) Viral avoidance and exploitation of the ubiquitin system. Nat Cell Biol 11: 527-534.
38. Isaacson MK, Ploegh HL (2009) Ubiquitination, ubiquitin-like modifiers, and deubiquitination in viral infection. Cell Host Microbe 5: 559-570.
39. Henderson BR, Eleftheriou A (2000) A comparison of the activity, sequence specificity, and CRM1-dependence of different nuclear export signals. Exp Cell Res 256: 213-224.
40. Pankiv S, Lamark T, Bruun JA, Overvatn A, Bjorkoy G, et al. (2010) Nucleocytoplasmic shuttling of p62/SQSTM1 and its role in recruitment of nuclear polyubiquitinated proteins to promyelocytic leukemia bodies. J Biol Chem 285: 5941-5953.
41. Li SY, Davidson PJ, Lin NY, Patterson RJ, Wang JL, et al. (2006) Transport of galectin-3 between the nucleus and cytoplasm. II. Identification of the signal for nuclear export. Glycobiology 16: 612-622.
42. Rodriguez JJ, Cruz CD, Horvath CM (2004) Identification of the nuclear export signal and STAT-binding domains of the Nipah virus V protein reveals mechanisms underlying interferon evasion. J Virol 78: 5358-5367.
43. Patnaik A, Chau V, Wills JW (2000) Ubiquitin is part of the retrovirus budding machinery. Proc Natl Acad Sci U S A 97: 13069-13074.
44. Schubert U, Ott DE, Chertova EN, Welker R, Tessmer U, et al. (2000) Proteasome inhibition interferes with gag polyprotein processing, release, and maturation of HIV-1 and HIV-2. Proc Natl Acad Sci U S A 97: 13057-13062.
45. Vogt VM (2000) Ubiquitin in retrovirus assembly: actor or bystander? Proc Natl Acad Sci U S A 97: 12945-12947.
46. Morita E, Sundquist WI (2004) Retrovirus budding. Annu Rev Cell Dev Biol 20: 395-425.
47. Hoeller D, Crosetto N, Blagoev B, Raiborg C, Tikkanen R, et al. (2006) Regulation of ubiquitin-binding proteins by monoubiquitination. Nat Cell Biol 8: 163-169.
48. Qian SB, Ott DE, Schubert U, Bennink JR, Yewdell JW (2002) Fusion proteins with COOH-terminal ubiquitin are stable and maintain dual functionality in vivo. J Biol Chem 277: 38818-38826.
49. Carter S, Bischof O, Dejean A, Vousden KH (2007) C-terminal modifications regulate MDM2 dissociation and nuclear export of p53. Nat Cell Biol 9: 428-435.
50. Lee JC, Wang GX, Schickling O, Peter ME (2005) Fusing DEDD with ubiquitin changes its intracellular localization and apoptotic potential. Apoptosis 10: 1483-1495.
51. Spearman P, Wang JJ, Vander Heyden N, Ratner L (1994) Identification of human immunodeficiency virus type 1 Gag protein domains essential to membrane binding and particle assembly. J Virol 68: 3232-3242.
52. Hermida-Matsumoto L, Resh MD (2000) Localization of human immunodeficiency virus type 1 Gag and Env at the plasma membrane by confocal imaging. J Virol 74: 8670-8679.
53. Rodgers W (2002) Making membranes green: construction and characterization of GFP-fusion proteins targeted to discrete plasma membrane domains. Biotechniques 32: 1044-1046, 1048, 1050-1041.
54. Shenoy-Scaria AM, Gauen LK, Kwong J, Shaw AS, Lublin DM (1993) Palmitylation of an amino-terminal cysteine motif of protein tyrosine kinases p56lck and p59fyn mediates interaction with glycosyl-phosphatidylinositolanchored proteins. Mol Cell Biol 13: 6385-6392.
55. Elliott PJ, Zollner TM, Boehncke WH (2003) Proteasome inhibition: a new anti-inflammatory strategy. J Mol Med 81: 235-245.
56. Sanchez-Serrano I (2006) Success in translational research: lessons from the development of bortezomib. Nat Rev Drug Discov 5: 107-114.
57. Papandreou CN, Daliani DD, Nix D, Yang H, Madden T, et al. (2004) Phasefg I trial of the proteasome inhibitor bortezomib in patients with advanced solid tumors with observations in androgen-independent prostate cancer. J Clin Oncol 22: 2108-2121.
58. Ogawa Y, Tobinai K, Ogura M, Ando K, Tsuchiya T, et al. (2008) Phase I and II pharmacokinetic and pharmacodynamic study of the proteasome inhibitor bortezomib in Japanese patients with relapsed or refractory multiple myeloma. Cancer Sci 99: 140-144.
59. Hicke L (2001) Protein regulation by monoubiquitin. Nat Rev Mol Cell Biol 2: 195-201.
60. Johnson ES (2002) Ubiquitin branches out. Nat Cell Biol 4: E295-298.
61. Tanaka T, Soriano MA, Grusby MJ (2005) SLIM is a nuclear ubiquitin E3 ligase that negatively regulates STAT signaling. Immunity 22: 729-736.
62. Natoli G, Chiocca S (2008) Nuclear ubiquitin ligases, NF-kappaB degradation, and the control of inflammation. Sci Signal 1: pe1.
63. Martin-Serrano J (2007) The role of ubiquitin in retroviral egress. Traffic 8: 1297-1303.
64. Saad JS, Miller J, Tai J, Kim A, Ghanam RH, et al. (2006) Structural basis for targeting HIV-1 Gag proteins to the plasma membrane for virus assembly. Proc Natl Acad Sci U S A 103: 11364-11369.
65. Gonzalo S, Linder ME (1998) SNAP-25 palmitoylation and plasma membrane targeting require a functional secretory pathway. Mol Biol Cell 9: 585-597.
66. Manie SN, de Breyne S, Vincent S, Gerlier D (2000) Measles virus structural components are enriched into lipid raft microdomains: a potential cellular location for virus assembly. J Virol 74: 305-311.
67. Brown G, Rixon HW, Sugrue RJ (2002) Respiratory syncytial virus assembly occurs in GM1-rich regions of the host-cell membrane and alters the cellular distribution of tyrosine phosphorylated caveolin-1. J Gen Virol 83: 1841-1850.
68. Ali A, Nayak DP (2000) Assembly of Sendai virus: M protein interacts with F and HN proteins and with the cytoplasmic tail and transmembrane domain of F protein. Virology 276: 289-303.
69. Reed LJ, Muench H (1938) A simple method of estimating fifty percent endpoints. The American Journal of Hygiene. pp 493-397.
70. Lim KL, Chew KC, Tan JM, Wang C, Chung KK, et al. (2005) Parkin mediates nonclassical, proteasomal-independent ubiquitination of synphilin-1: implications for Lewy body formation. J Neurosci 25: 2002-2009.
71. Guo X, Roldan A, Hu J, Wainberg MA, Liang C (2005) Mutation of the SP1 sequence impairs both multimerization and membrane-binding activities of human immunodeficiency virus type 1 Gag. J Virol 79: 1803-1812.