Evidence for Ubiquitin-Regulated Nuclear and Subnuclear Trafficking among Paramyxovirinae Matrix Proteins

PLoS Pathogens

Volumn 11, Issue 3, 2015, Pages 1-33

  Pentecost, Mickey ^a   Vashisht, Ajay A ^a   Lester, Talia ^a   Voros, Tim ^a   Beaty, Shannon M ^b   Park, Arnold ^a   Wang, Yao E ^a   Yun, Tatyana E ^c   Freiberg, Alexander N ^c   Wohlschlegel, James A ^a   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)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; LYSINE; MOLECULAR SCAFFOLD; PARAMYXOVIRINAE MATRIX PROTEIN; UBIQUITIN; UNCLASSIFIED DRUG; MATRIX PROTEIN; NUCLEAR LOCALIZATION SIGNAL;

ARTICLE; CONFOCAL MICROSCOPY; GENE CONSTRUCT; GENE MUTATION; GENETIC TRANSFECTION; HENDRA VIRUS; HUMAN; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MUMPS VIRUS; NIPAH VIRUS INFECTION; NUCLEAR EXPORT SIGNAL; NUCLEAR LOCALIZATION SIGNAL; NUCLEAR PORE COMPLEX; NUCLEAR TRAFFICKING; NUCLEOCYTOPLASMIC TRANSPORT; PARAMYXOVIRINAE; PROTEIN ANALYSIS; PROTEIN INTERACTION; PROTEOMICS; REGULATORY MECHANISM; SENDAI VIRUS; SHOTGUN PROTEOMICS; SUBNUCLEAR TRAFFICKING; UBIQUITINATION; VIRUS MORPHOGENESIS; VIRUS RELEASE; VIRUS REPLICATION; AMINO ACID SEQUENCE; ANIMAL; CELL NUCLEUS; CHLOROCEBUS AETHIOPS; HELA CELL LINE; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT; THREE DIMENSIONAL IMAGING; VERO CELL LINE;

HENDRA VIRUS; MUMPS VIRUS; NIPAH VIRUS; PARAMYXOVIRIDAE; PARAMYXOVIRINAE; SENDAI VIRUS;

AMINO ACID SEQUENCE; ANIMALS; CELL NUCLEUS; CERCOPITHECUS AETHIOPS; HELA CELLS; HUMANS; IMAGING, THREE-DIMENSIONAL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MICROSCOPY, CONFOCAL; NUCLEAR LOCALIZATION SIGNALS; PARAMYXOVIRINAE; PROTEIN TRANSPORT; TRANSFECTION; UBIQUITIN; VERO CELLS; VIRAL MATRIX PROTEINS;

EID: 84926478775     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004739     Document Type: Article

References (130)

1. (2011) The Biology of paramyxoviruses. Norfolk, UK: Caister Academic Press.
2. Mariner JC, House JA, Mebus CA, Sollod AE, Chibeu D, et al. (2012) Rinderpest eradication: appropriate technology and social innovations. Science 337: 1309–1312. doi: 10.1126/science.1223805 22984063
3. Aguilar HC, Lee B, (2011) Emerging paramyxoviruses: molecular mechanisms and antiviral strategies. Expert Rev Mol Med 13: e6. doi: 10.1017/S1462399410001754 21345285
4. Eaton BT, Broder CC, Middleton D, Wang LF, (2006) Hendra and Nipah viruses: different and dangerous. Nat Rev Microbiol 4: 23–35. 16357858
5. Lamb RA, Parks GD, Fields BN, Knipe DM, Howley PM, (2013) Paramyxoviridae: The viruses and their replication. In: Fields virology. 6th ed. Philadelphia: Wolters Kluwer Health/Lippincott Williams & Wilkins. pp. 957–995.
6. Lo MK, Rota PA, (2008) The emergence of Nipah virus, a highly pathogenic paramyxovirus. J Clin Virol 43: 396–400. doi: 10.1016/j.jcv.2008.08.007 18835214
7. Harrison MS, Sakaguchi T, Schmitt AP, (2010) Paramyxovirus assembly and budding: building particles that transmit infections. Int J Biochem Cell Biol 42: 1416–1429. doi: 10.1016/j.biocel.2010.04.005 20398786
8. Jardetzky TS, Lamb RA, (2014) Activation of paramyxovirus membrane fusion and virus entry. Curr Opin Virol 5C: 24–33.
9. Lee B, Ataman ZA, (2011) Modes of paramyxovirus fusion: a Henipavirus perspective. Trends Microbiol 19: 389–399. doi: 10.1016/j.tim.2011.03.005 21511478
10. Lamb RA, Paterson RG, Jardetzky TS, (2006) Paramyxovirus membrane fusion: lessons from the F and HN atomic structures. Virology 344: 30–37. 16364733
11. Battisti AJ, Meng G, Winkler DC, McGinnes LW, Plevka P, et al. (2012) Structure and assembly of a paramyxovirus matrix protein. Proc Natl Acad Sci U S A 109: 13996–14000. doi: 10.1073/pnas.1210275109 22891297
12. Terrier O, Rolland JP, Rosa-Calatrava M, Lina B, Thomas D, et al. (2009) Parainfluenza virus type 5 (PIV-5) morphology revealed by cryo-electron microscopy. Virus Res 142: 200–203. doi: 10.1016/j.virusres.2008.12.017 19185600
13. Pohl C, Duprex WP, Krohne G, Rima BK, Schneider-Schaulies S, (2007) Measles virus M and F proteins associate with detergent-resistant membrane fractions and promote formation of virus-like particles. J Gen Virol 88: 1243–1250. 17374768
14. Russell PH, Almeida JD, (1984) A regular subunit pattern seen on non-infectious Newcastle disease virus particles. J Gen Virol 65 (Pt 6): 1023–1031.
15. Heggeness MH, Smith PR, Choppin PW, (1982) In vitro assembly of the nonglycosylated membrane protein (M) of Sendai virus. Proc Natl Acad Sci U S A 79: 6232–6236. 6292897
16. Hewitt JA, Nermut MV, (1977) A morphological study of the M-protein of Sendai virus. J Gen Virol 34: 127–136. 188976
17. Buechi M, Bachi T, (1982) Microscopy of internal structures of Sendai virus associated with the cytoplasmic surface of host membranes. Virology 120: 349–359. 6285608
18. Bachi T, (1980) Intramembrane structural differentiation in Sendai virus maturation. Virology 106: 41–49. 6251620
19. 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. 10590118
20. Vincent S, Gerlier D, Manie SN, (2000) Measles virus assembly within membrane rafts. J Virol 74: 9911–9915. 11024118
21. Riedl P, Moll M, Klenk HD, Maisner A, (2002) Measles virus matrix protein is not cotransported with the viral glycoproteins but requires virus infection for efficient surface targeting. Virus Res 83: 1–12. 11864737
22. Subhashri R, Shaila MS, (2007) Characterization of membrane association of Rinderpest virus matrix protein. Biochem Biophys Res Commun 355: 1096–1101. 17336269
23. Stricker R, Mottet G, Roux L, (1994) The Sendai virus matrix protein appears to be recruited in the cytoplasm by the viral nucleocapsid to function in viral assembly and budding. J Gen Virol 75 (Pt 5): 1031–1042.
24. Caldwell SE, Lyles DS, (1986) Dissociation of newly synthesized Sendai viral proteins from the cytoplasmic surface of isolated plasma membranes of infected cells. J Virol 57: 678–683. 3003398
25. Henderson G, Murray J, Yeo RP, (2002) Sorting of the respiratory syncytial virus matrix protein into detergent-resistant structures is dependent on cell-surface expression of the glycoproteins. Virology 300: 244–254. 12350355
26. Schmitt AP, He B, Lamb RA, (1999) Involvement of the cytoplasmic domain of the hemagglutinin-neuraminidase protein in assembly of the paramyxovirus simian virus 5. J Virol 73: 8703–8712. 10482624
27. Schmitt AP, Leser GP, Morita E, Sundquist WI, Lamb RA, (2005) Evidence for a new viral late-domain core sequence, FPIV, necessary for budding of a paramyxovirus. J Virol 79: 2988–2997. 15709019
28. Waning DL, Schmitt AP, Leser GP, Lamb RA, (2002) Roles for the cytoplasmic tails of the fusion and hemagglutinin-neuraminidase proteins in budding of the paramyxovirus simian virus 5. J Virol 76: 9284–9297. 12186912
29. Essaidi-Laziosi M, Shevtsova A, Gerlier D, Roux L, (2013) Mutation of the TYTLE Motif in the Cytoplasmic Tail of the Sendai Virus Fusion Protein Deeply Affects Viral Assembly and Particle Production. PLoS One 8: e78074. doi: 10.1371/journal.pone.0078074 24339863
30. 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. 11040121
31. Coronel EC, Takimoto T, Murti KG, Varich N, Portner A, (2001) Nucleocapsid incorporation into parainfluenza virus is regulated by specific interaction with matrix protein. J Virol 75: 1117–1123. 11152484
32. Iwasaki M, Takeda M, Shirogane Y, Nakatsu Y, Nakamura T, et al. (2009) The matrix protein of measles virus regulates viral RNA synthesis and assembly by interacting with the nucleocapsid protein. J Virol 83: 10374–10383. doi: 10.1128/JVI.01056-09 19656884
33. Cathomen T, Naim HY, Cattaneo R, (1998) Measles viruses with altered envelope protein cytoplasmic tails gain cell fusion competence. J Virol 72: 1224–1234. 9445022
34. Tahara M, Takeda M, Yanagi Y, (2007) Altered interaction of the matrix protein with the cytoplasmic tail of hemagglutinin modulates measles virus growth by affecting virus assembly and cell-cell fusion. J Virol 81: 6827–6836. 17442724
35. Ghildyal R, Li D, Peroulis I, Shields B, Bardin PG, et al. (2005) Interaction between the respiratory syncytial virus G glycoprotein cytoplasmic domain and the matrix protein. J Gen Virol 86: 1879–1884. 15958665
36. Runkler N, Pohl C, Schneider-Schaulies S, Klenk HD, Maisner A, (2007) Measles virus nucleocapsid transport to the plasma membrane requires stable expression and surface accumulation of the viral matrix protein. Cell Microbiol 9: 1203–1214. 17217427
37. 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. 17005661
38. 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. 17204159
39. 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 Pathog 6: e1001186. doi: 10.1371/journal.ppat.1001186 21085610
40. Pantua HD, McGinnes LW, Peeples ME, Morrison TG, (2006) Requirements for the assembly and release of Newcastle disease virus-like particles. J Virol 80: 11062–11073. 16971425
41. Takimoto T, Murti KG, Bousse T, Scroggs RA, Portner A, (2001) Role of matrix and fusion proteins in budding of Sendai virus. J Virol 75: 11384–11391. 11689619
42. 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. Virology 325: 1–10. 15231380
43. Li M, Schmitt PT, Li Z, McCrory TS, He B, et al. (2009) Mumps virus matrix, fusion, and nucleocapsid proteins cooperate for efficient production of virus-like particles. J Virol 83: 7261–7272. doi: 10.1128/JVI.00421-09 19439476
44. Schmitt AP, Leser GP, Waning DL, Lamb RA, (2002) Requirements for budding of paramyxovirus simian virus 5 virus-like particles. J Virol 76: 3952–3964. 11907235
45. Inoue M, Tokusumi Y, Ban H, Kanaya T, Shirakura M, et al. (2003) A new Sendai virus vector deficient in the matrix gene does not form virus particles and shows extensive cell-to-cell spreading. J Virol 77: 6419–6429. 12743299
46. Cathomen T, Mrkic B, Spehner D, Drillien R, Naef R, et al. (1998) A matrix-less measles virus is infectious and elicits extensive cell fusion: consequences for propagation in the brain. EMBO J 17: 3899–3908. 9670007
47. Irie T, Inoue M, Sakaguchi T, (2010) Significance of the YLDL motif in the M protein and Alix/AIP1 for Sendai virus budding in the context of virus infection. Virology 405: 334–341. doi: 10.1016/j.virol.2010.06.031 20605035
48. 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. 8337834
49. 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. doi: 10.1128/JVI.02374-08 19297465
50. 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. 16171404
51. Duan Z, Li Q, He L, Zhao G, Chen J, et al. (2013) Application of green fluorescent protein-labeled assay for the study of subcellular localization of Newcastle disease virus matrix protein. J Virol Methods 194: 118–122. doi: 10.1016/j.jviromet.2013.08.014 23994149
52. Duan Z, Song Q, Wang Y, He L, Chen J, et al. (2013) Characterization of signal sequences determining the nuclear export of Newcastle disease virus matrix protein. Arch Virol 158: 2589–2595. doi: 10.1007/s00705-013-1769-5 23807745
53. 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. 179199
54. Bauer A, Neumann S, Karger A, Henning AK, Maisner A, et al. (2014) ANP32B Is a Nuclear Target of Henipavirus M Proteins. PLoS One 9: e97233. doi: 10.1371/journal.pone.0097233 24823948
55. 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. 15728840
56. Komander D, Rape M, (2012) The ubiquitin code. Annu Rev Biochem 81: 203–229. doi: 10.1146/annurev-biochem-060310-170328 22524316
57. Bailey D, O’Hare P, (2005) Comparison of the SUMO1 and ubiquitin conjugation pathways during the inhibition of proteasome activity with evidence of SUMO1 recycling. Biochem J 392: 271–281. 16117725
58. Hjerpe R, Thomas Y, Chen J, Zemla A, Curran S, et al. (2012) Changes in the ratio of free NEDD8 to ubiquitin triggers NEDDylation by ubiquitin enzymes. Biochem J 441: 927–936. doi: 10.1042/BJ20111671 22004789
59. Mimnaugh EG, Chen HY, Davie JR, Celis JE, Neckers L, (1997) Rapid deubiquitination of nucleosomal histones in human tumor cells caused by proteasome inhibitors and stress response inducers: effects on replication, transcription, translation, and the cellular stress response. Biochemistry 36: 14418–14429. 9398160
60. 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. 11087859
61. 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. 11087861
62. Xu Q, Farah M, Webster JM, Wojcikiewicz RJ, (2004) Bortezomib rapidly suppresses ubiquitin thiolesterification to ubiquitin-conjugating enzymes and inhibits ubiquitination of histones and type I inositol 1,4,5-trisphosphate receptor. Mol Cancer Ther 3: 1263–1269. 15486193
63. Fang D, Kerppola TK, (2004) Ubiquitin-mediated fluorescence complementation reveals that Jun ubiquitinated by Itch/AIP4 is localized to lysosomes. Proc Natl Acad Sci U S A 101: 14782–14787. 15469925
64. Lee J, Lee Y, Lee MJ, Park E, Kang SH, et al. (2008) Dual modification of BMAL1 by SUMO2/3 and ubiquitin promotes circadian activation of the CLOCK/BMAL1 complex. Mol Cell Biol 28: 6056–6065. doi: 10.1128/MCB.00583-08 18644859
65. Kerppola TK, (2008) Bimolecular fluorescence complementation (BiFC) analysis as a probe of protein interactions in living cells. Annu Rev Biophys 37: 465–487. doi: 10.1146/annurev.biophys.37.032807.125842 18573091
66. Kerppola TK, (2006) Design and implementation of bimolecular fluorescence complementation (BiFC) assays for the visualization of protein interactions in living cells. Nat Protoc 1: 1278–1286. 17406412
67. Hou X, Suquilanda E, Zeledon A, Kacsinta A, Moore A, et al. (2005) Mutations in Sendai virus variant F1-R that correlate with plaque formation in the absence of trypsin. Med Microbiol Immunol 194: 129–136. 15834752
68. Rawling J, Cano O, Garcin D, Kolakofsky D, Melero JA, (2011) Recombinant Sendai viruses expressing fusion proteins with two furin cleavage sites mimic the syncytial and receptor-independent infection properties of respiratory syncytial virus. J Virol 85: 2771–2780. doi: 10.1128/JVI.02065-10 21228237
69. 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. 1560547
70. Mellacheruvu D, Wright Z, Couzens AL, Lambert JP, St-Denis NA, et al. (2013) The CRAPome: a contaminant repository for affinity purification-mass spectrometry data. Nat Methods 10: 730–736. doi: 10.1038/nmeth.2557 23921808
71. Sun W, McCrory TS, Khaw WY, Petzing S, Myers T, et al. (2014) Matrix Proteins of Nipah and Hendra Viruses Interact with Beta Subunits of AP-3 Complexes. J Virol 88: 13099–13110. doi: 10.1128/JVI.02103-14 25210190
72. Kimura M, Imamoto N (2014) Biological Significance of the Importin-beta Family-Dependent Nucleocytoplasmic Transport Pathways. Traffic.
73. Yarbrough ML, Mata MA, Sakthivel R, Fontoura BM, (2014) Viral subversion of nucleocytoplasmic trafficking. Traffic 15: 127–140. doi: 10.1111/tra.12137 24289861
74. Jeram SM, Srikumar T, Pedrioli PG, Raught B, (2009) Using mass spectrometry to identify ubiquitin and ubiquitin-like protein conjugation sites. Proteomics 9: 922–934. doi: 10.1002/pmic.200800666 19180541
75. McLane LM, Corbett AH, (2009) Nuclear localization signals and human disease. IUBMB Life 61: 697–706. doi: 10.1002/iub.194 19514019
76. Terry LJ, Shows EB, Wente SR, (2007) Crossing the nuclear envelope: hierarchical regulation of nucleocytoplasmic transport. Science 318: 1412–1416. 18048681
77. Marchenko ND, Hanel W, Li D, Becker K, Reich N, et al. (2010) Stress-mediated nuclear stabilization of p53 is regulated by ubiquitination and importin-alpha3 binding. Cell Death Differ 17: 255–267. doi: 10.1038/cdd.2009.173 19927155
78. Mashtalir N, Daou S, Barbour H, Sen NN, Gagnon J, et al. (2014) Autodeubiquitination Protects the Tumor Suppressor BAP1 from Cytoplasmic Sequestration Mediated by the Atypical Ubiquitin Ligase UBE2O. Mol Cell 54: 392–406. doi: 10.1016/j.molcel.2014.03.002 24703950
79. von Mikecz A, (2006) The nuclear ubiquitin-proteasome system. J Cell Sci 119: 1977–1984. 16687735
80. Banerjee R, Weidman MK, Navarro S, Comai L, Dasgupta A, (2005) Modifications of both selectivity factor and upstream binding factor contribute to poliovirus-mediated inhibition of RNA polymerase I transcription. J Gen Virol 86: 2315–2322. 16033979
81. Lymberopoulos MH, Pearson A, (2010) Relocalization of upstream binding factor to viral replication compartments is UL24 independent and follows the onset of herpes simplex virus 1 DNA synthesis. J Virol 84: 4810–4815. doi: 10.1128/JVI.02437-09 20147409
82. Stow ND, Evans VC, Matthews DA, (2009) Upstream-binding factor is sequestered into herpes simplex virus type 1 replication compartments. J Gen Virol 90: 69–73. doi: 10.1099/vir.0.006353-0 19088274
83. Lawrence FJ, McStay B, Matthews DA, (2006) Nucleolar protein upstream binding factor is sequestered into adenovirus DNA replication centres during infection without affecting RNA polymerase I location or ablating rRNA synthesis. J Cell Sci 119: 2621–2631. 16763197
84. Zhai W, Comai L, (1999) A kinase activity associated with simian virus 40 large T antigen phosphorylates upstream binding factor (UBF) and promotes formation of a stable initiation complex between UBF and SL1. Mol Cell Biol 19: 2791–2802. 10082545
85. Raychaudhuri S, Fontanes V, Barat B, Dasgupta A, (2009) Activation of ribosomal RNA transcription by hepatitis C virus involves upstream binding factor phosphorylation via induction of cyclin D1. Cancer Res 69: 2057–2064. doi: 10.1158/0008-5472.CAN-08-3468 19223538
86. Watanabe H, Tanaka Y, Shimazu Y, Sugahara F, Kuwayama M, et al. (2005) Cell-specific inhibition of paramyxovirus maturation by proteasome inhibitors. Microbiol Immunol 49: 835–844. 16172538
87. Shields SB, Piper RC, (2011) How ubiquitin functions with ESCRTs. Traffic 12: 1306–1317. doi: 10.1111/j.1600-0854.2011.01242.x 21722280
88. Votteler J, Sundquist WI, (2013) Virus budding and the ESCRT pathway. Cell Host Microbe 14: 232–241. doi: 10.1016/j.chom.2013.08.012 24034610
89. Irie T, Shimazu Y, Yoshida T, Sakaguchi T, (2007) 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 81: 2263–2273. 17166905
90. Moore HM, Bai B, Matilainen O, Colis L, Peltonen K, et al. (2013) Proteasome activity influences UV-mediated subnuclear localization changes of NPM. PLoS One 8: e59096. doi: 10.1371/journal.pone.0059096 23554979
91. Vilotti S, Biagioli M, Foti R, Dal Ferro M, Lavina ZS, et al. (2012) The PML nuclear bodies-associated protein TTRAP regulates ribosome biogenesis in nucleolar cavities upon proteasome inhibition. Cell Death Differ 19: 488–500. doi: 10.1038/cdd.2011.118 21921940
92. Leljak Levanic D, Horvat T, Martincic J, Bauer N, (2012) A novel bipartite nuclear localization signal guides BPM1 protein to nucleolus suggesting its Cullin3 independent function. PLoS One 7: e51184. doi: 10.1371/journal.pone.0051184 23251450
93. Latonen L, Moore HM, Bai B, Jaamaa S, Laiho M, (2011) Proteasome inhibitors induce nucleolar aggregation of proteasome target proteins and polyadenylated RNA by altering ubiquitin availability. Oncogene 30: 790–805. doi: 10.1038/onc.2010.469 20956947
94. Thoms HC, Loveridge CJ, Simpson J, Clipson A, Reinhardt K, et al. (2010) Nucleolar targeting of RelA(p65) is regulated by COMMD1-dependent ubiquitination. Cancer Res 70: 139–149. doi: 10.1158/0008-5472.CAN-09-1397 20048074
95. Kruger T, Scheer U, (2010) p53 localizes to intranucleolar regions distinct from the ribosome production compartments. J Cell Sci 123: 1203–1208. doi: 10.1242/jcs.062398 20332106
96. Andersen JS, Lam YW, Leung AK, Ong SE, Lyon CE, et al. (2005) Nucleolar proteome dynamics. Nature 433: 77–83. 15635413
97. Pokrovskaja K, Mattsson K, Kashuba E, Klein G, Szekely L, (2001) Proteasome inhibitor induces nucleolar translocation of Epstein-Barr virus-encoded EBNA-5. J Gen Virol 82: 345–358. 11161273
98. Mattsson K, Pokrovskaja K, Kiss C, Klein G, Szekely L, (2001) Proteins associated with the promyelocytic leukemia gene product (PML)-containing nuclear body move to the nucleolus upon inhibition of proteasome-dependent protein degradation. Proc Natl Acad Sci U S A 98: 1012–1017. 11158586
99. Matafora V, D'Amato A, Mori S, Blasi F, Bachi A, (2009) Proteomics analysis of nucleolar SUMO-1 target proteins upon proteasome inhibition. Mol Cell Proteomics 8: 2243–2255. doi: 10.1074/mcp.M900079-MCP200 19596686
100. Duan Z, Chen J, Xu H, Zhu J, Li Q, et al. (2014) The nucleolar phosphoprotein B23 targets Newcastle disease virus matrix protein to the nucleoli and facilitates viral replication. Virology 452–453: 212–222.
101. Scott MS, Troshin PV, Barton GJ, (2011) NoD: a Nucleolar localization sequence detector for eukaryotic and viral proteins. BMC Bioinformatics 12: 317. doi: 10.1186/1471-2105-12-317 21812952
102. Emmott E, Hiscox JA, (2009) Nucleolar targeting: the hub of the matter. EMBO Rep 10: 231–238. doi: 10.1038/embor.2009.14 19229283
103. Greco A, (2009) Involvement of the nucleolus in replication of human viruses. Rev Med Virol 19: 201–214. doi: 10.1002/rmv.614 19399920
104. Hiscox JA, (2007) RNA viruses: hijacking the dynamic nucleolus. Nat Rev Microbiol 5: 119–127. 17224921
105. Salvetti A, Greco A, (2013) Viruses and the nucleolus: The fatal attraction. Biochim Biophys Acta.
106. Satterly N, Tsai PL, van Deursen J, Nussenzveig DR, Wang Y, et al. (2007) Influenza virus targets the mRNA export machinery and the nuclear pore complex. Proc Natl Acad Sci U S A 104: 1853–1858. 17267598
107. von Kobbe C, van Deursen JM, Rodrigues JP, Sitterlin D, Bachi A, et al. (2000) Vesicular stomatitis virus matrix protein inhibits host cell gene expression by targeting the nucleoporin Nup98. Mol Cell 6: 1243–1252. 11106761
108. 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. 12827470
109. Bian T, Gibbs JD, Orvell C, Imani F, (2012) Respiratory syncytial virus matrix protein induces lung epithelial cell cycle arrest through a p53 dependent pathway. PLoS One 7: e38052. doi: 10.1371/journal.pone.0038052 22662266
110. Hu J, Zacharek S, He YJ, Lee H, Shumway S, et al. (2008) WD40 protein FBW5 promotes ubiquitination of tumor suppressor TSC2 by DDB1-CUL4-ROC1 ligase. Genes Dev 22: 866–871. doi: 10.1101/gad.1624008 18381890
111. Andrews P, He YJ, Xiong Y, (2006) Cytoplasmic localized ubiquitin ligase cullin 7 binds to p53 and promotes cell growth by antagonizing p53 function. Oncogene 25: 4534–4548. 16547496
112. Ohta T, Michel JJ, Schottelius AJ, Xiong Y, (1999) ROC1, a homolog of APC11, represents a family of cullin partners with an associated ubiquitin ligase activity. Mol Cell 3: 535–541. 10230407
113. Liu J, Furukawa M, Matsumoto T, Xiong Y, (2002) NEDD8 modification of CUL1 dissociates p120(CAND1), an inhibitor of CUL1-SKP1 binding and SCF ligases. Mol Cell 10: 1511–1518. 12504025
114. Dundr M, Hoffmann-Rohrer U, Hu Q, Grummt I, Rothblum LI, et al. (2002) A kinetic framework for a mammalian RNA polymerase in vivo. Science 298: 1623–1626. 12446911
115. Wang W, Budhu A, Forgues M, Wang XW, (2005) Temporal and spatial control of nucleophosmin by the Ran-Crm1 complex in centrosome duplication. Nat Cell Biol 7: 823–830. 16041368
116. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, et al. (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7: 539. doi: 10.1038/msb.2011.75 21988835
117. Shyu YJ, Liu H, Deng X, Hu CD, (2006) Identification of new fluorescent protein fragments for bimolecular fluorescence complementation analysis under physiological conditions. Biotechniques 40: 61–66. 16454041
118. Clarke DK, Sidhu MS, Johnson JE, Udem SA, (2000) Rescue of mumps virus from cDNA. J Virol 74: 4831–4838. 10775622
119. Kaiser P, Wohlschlegel J, (2005) Identification of ubiquitination sites and determination of ubiquitin-chain architectures by mass spectrometry. Methods Enzymol 399: 266–277. 16338362
120. Wohlschlegel JA, (2009) Identification of SUMO-conjugated proteins and their SUMO attachment sites using proteomic mass spectrometry. Methods Mol Biol 497: 33–49. doi: 10.1007/978-1-59745-566-4_3 19107409
121. Tabb DL, McDonald WH, Yates JR, 3rd, (2002) DTASelect and Contrast: tools for assembling and comparing protein identifications from shotgun proteomics. J Proteome Res 1: 21–26. 12643522
122. Xu T, Venable J, Park SK, Cociorva D, Lu B, et al. ProLuCID, a fast and sensitive tandem mass spectra-based protein identification program; 2006. AMER SOC BIOCHEMISTRY MOLECULAR BIOLOGY INC 9650 ROCKVILLE PIKE, BETHESDA, MD 20814–3996 USA. pp. S174-S174.
123. Elias JE, Gygi SP, (2007) Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat Methods 4: 207–214. 17327847
124. Florens L, Carozza MJ, Swanson SK, Fournier M, Coleman MK, et al. (2006) Analyzing chromatin remodeling complexes using shotgun proteomics and normalized spectral abundance factors. Methods 40: 303–311. 17101441
125. Bardou P, Mariette J, Escudie F, Djemiel C, Klopp C, (2014) jvenn: an interactive Venn diagram viewer. BMC Bioinformatics 15: 293. doi: 10.1186/1471-2105-15-293 25176396
126. Huang da W, Sherman BT, Lempicki RA, (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44–57. doi: 10.1038/nprot.2008.211 19131956
127. Huang da W, Sherman BT, Zheng X, Yang J, Imamichi T, et al. (2009) Extracting biological meaning from large gene lists with DAVID. Curr Protoc Bioinformatics Chapter 13: Unit 13 11.
128. Cline MS, Smoot M, Cerami E, Kuchinsky A, Landys N, et al. (2007) Integration of biological networks and gene expression data using Cytoscape. Nat Protoc 2: 2366–2382. 17947979
129. Montojo J, Zuberi K, Rodriguez H, Kazi F, Wright G, et al. (2010) GeneMANIA Cytoscape plugin: fast gene function predictions on the desktop. Bioinformatics 26: 2927–2928. doi: 10.1093/bioinformatics/btq562 20926419
130. Stone R, Takimoto T, (2013) Critical role of the fusion protein cytoplasmic tail sequence in parainfluenza virus assembly. PLoS One 8: e61281. doi: 10.1371/journal.pone.0061281 23593451