Human cytomegalovirus UL76 elicits novel aggresome formation via interaction with S5a of the ubiquitin proteasome system

Journal of Virology

Volumn 87, Issue 21, 2013, Pages 11562-11578

  Lin, Shin Rung ^a   Jiang, Meei Jyh ^b   Wang, Hung Hsueh ^a   Hu, Cheng Hui ^a   Hsu, Ming Shan ^a   Hsi, Edward ^c   Duh, Chang Yih ^d   Wang, Shang Kwei ^a  

^a KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^b NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^c KAOHSIUNG MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^d NATIONAL SUN YAT SEN UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEASOME; PROTEIN S5A; PROTEIN UL76; UBIQUITIN; UNCLASSIFIED DRUG; VIRUS PROTEIN; VON WILLEBRAND FACTOR; VON WILLEBRAND FACTOR TYPE A;

AGGRESOME; ARTICLE; CELL STRAIN HEK293; CONTROLLED STUDY; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; DNA TRANSFECTION; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; LUNG ALVEOLUS CELL; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE;

CELL LINE; CYTOMEGALOVIRUS; HOST-PATHOGEN INTERACTIONS; HUMANS; MACROMOLECULAR SUBSTANCES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; PROTEIN DENATURATION; PROTEIN MULTIMERIZATION; TRANS-ACTIVATORS; VIRUS ACTIVATION; VIRUS LATENCY; VIRUS REPLICATION;

EID: 84886928717     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01568-13     Document Type: Article

References (87)

1. Mocarski ES, Shenk T, Pass RF. 2007. Cytomegalovirus, p 2701-2772. In Knipe M, Howley PM (ed). Fields virology, 5th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
2. Hansen SG, Powers CJ, Richards R, Ventura AB, Ford JC, Siess D, Axthelm MK, Nelson JA, Jarvis MA, Picker LJ, Fruh K. 2010. Evasion of CD8+ T cells is critical for superinfection by cytomegalovirus. Science 328:102-106.
3. Michaelis M, Doerr HW, Cinatl J. 2009. The story of human cytomegalovirus and cancer: increasing evidence and open questions. Neoplasia 11:1-9.
4. Caposio P, OrloffSL, Streblow DN. 2011. The role of cytomegalovirus in angiogenesis. Virus Res. 157:204-211.
5. Carter CJ. 2009. Schizophrenia susceptibility genes directly implicated in the life cycles of pathogens: cytomegalovirus, influenza, herpes simplex, rubella, and Toxoplasma gondii. Schizophr. Bull. 35:1163-1182.
6. Weissman AM, Shabek N, Ciechanover A. 2011. The predator becomes the prey: regulating the ubiquitin system by ubiquitylation and degradation. Nat. Rev. Mol. Cell Biol. 12:605-620.
7. Ciechanover A. 2005. Proteolysis: from the lysosome to ubiquitin and the proteasome. Nat. Rev. Mol. Cell Biol. 6:79-87.
8. Husnjak K, Elsasser S, Zhang N, Chen X, Randles L, Shi Y, Hofmann K, Walters KJ, Finley D, Dikic I. 2008. Proteasome subunit Rpn13 is a novel ubiquitin receptor. Nature 453:481-488.
9. Verma R, Oania R, Graumann J, Deshaies RJ. 2004. Multiubiquitin chain receptors define a layer of substrate selectivity in the ubiquitinproteasome system. Cell 118:99-110.
10. Kang Y, Chen X, Lary JW, Cole JL, Walters KJ. 2007. Defining how ubiquitin receptors hHR23a and S5a bind polyubiquitin. J. Mol. Biol. 369:168-176.
11. Gardner RG, Nelson ZW, Gottschling DE. 2005. Degradation-mediated protein quality control in the nucleus. Cell 120:803-815.
12. Matsuo Y, Kishimoto H, Tanae K, Kitamura K, Katayama S, Kawamukai M. 2011. Nuclear protein quality is regulated by the ubiquitinproteasome system through the activity of Ubc4 and San1 in fission yeast. J. Biol. Chem. 286:13775-13790.
13. Rosenbaum JC, Fredrickson EK, Oeser ML, Garrett-Engele CM, Locke MN, Richardson LA, Nelson ZW, Hetrick ED, Milac TI, Gottschling DE, Gardner RG. 2011. Disorder targets misorder in nuclear quality control degradation: a disordered ubiquitin ligase directly recognizes its misfolded substrates. Mol. Cell 41:93-106.
14. Fredrickson EK, Rosenbaum JC, Locke MN, Milac TI, Gardner RG. Exposed hydrophobicity is a key determinant of nuclear quality control degradation. Mol. Biol. Cell 22:2384-2395.
15. Blanchette P, Branton PE. 2009. Manipulation of the ubiquitinproteasome pathway by small DNA tumor viruses. Virology 384:317-323.
16. Martin-Serrano J. 2007. The role of ubiquitin in retroviral egress. Traffic 8:1297-1303.
17. Hewitt EW. 2003. The MHC class I antigen presentation pathway: strategies for viral immune evasion. Immunology 110:163-169.
18. Wiebusch L, Bach M, Uecker R, Hagemeier C. 2005. Human cytomegalovirus inactivates the G0/G1-APC/C ubiquitin ligase by Cdh1 dissociation. Cell Cycle. 4:1435-1439.
19. Tran K, Mahr JA, Choi J, Teodoro JG, Green MR, Spector DH. 2008. Accumulation of substrates of the anaphase-promoting complex (APC) during human cytomegalovirus infection is associated with the phosphorylation of Cdh1 and the dissociation and relocalization of APC subunits. J. Virol. 82:529-537.
20. Tavalai N, Stamminger T. 2011. Intrinsic cellular defense mechanisms targeting human cytomegalovirus. Virus Res. 157:128-133.
21. Kalejta RF. 2008. Functions of human cytomegalovirus tegument proteins prior to immediate early gene expression. Curr. Top. Microbiol. Immunol. 325:101-115.
22. Tran K, Mahr JA, Spector DH. 2010. Proteasome subunits relocalize during human cytomegalovirus infection, and proteasome activity is necessary for efficient viral gene transcription. J. Virol. 84:3079-3093.
23. Bateman A, Coin L, Durbin R, Finn RD, Hollich V, Griffiths-Jones S, Khanna A, Marshall M, Moxon S, Sonnhammer EL, Studholme DJ, Yeats C, Eddy SR. 2004. The Pfam protein families database. Nucleic Acids Res. 32:D138-D141.
24. Wang SK, Duh CY, Wu CW. 2004. Human cytomegalovirus UL76 encodes a novel virion-associated protein that is able to inhibit viral replication. J. Virol. 78:9750-9762.
25. Wang SK, Duh CY, Chang TT. 2000. Cloning and identification of regulatory gene UL76 of human cytomegalovirus. J. Gen. Virol. 81:2407-2416.
26. Isomura H, Stinski MF, Murata T, Nakayama S, Chiba S, Akatsuka Y, Kanda T, Tsurumi T. 2010. The human cytomegalovirus UL76 gene regulates the level of expression of the UL77 gene. PLoS One 5:e11901.
27. Goodrum FD, Jordan CT, High K, Shenk T. 2002. Human cytomegalovirus gene expression during infection of primary hematopoietic progenitor cells: a model for latency. Proc. Natl. Acad. Sci. U. S. A. 99:16255-16260.
28. Goodrum F, Jordan CT, Terhune SS, High K, Shenk T. 2004. Differential outcomes of human cytomegalovirus infection in primitive hematopoietic cell subpopulations. Blood 104:687-695.
29. Cheung AK, Abendroth A, Cunningham AL, Slobedman B. 2006. Viral gene expression during the establishment of human cytomegalovirus latent infection in myeloid progenitor cells. Blood 108:3691-3699.
30. Siew VK, Duh CY, Wang SK. 2009. Human cytomegalovirus UL76 induces chromosome aberrations. J. Biomed. Sci. 16:107.
31. Salsman J, Zimmerman N, Chen T, Domagala M, Frappier L. 2008. Genome-wide screen of three herpesviruses for protein subcellular localization and alteration of PML nuclear bodies. PLoS Pathog. 4:e1000100.
32. Aronheim A, Zandi E, Hennemann H, Elledge SJ, Karin M. 1997. Isolation of an AP-1 repressor by a novel method for detecting proteinprotein interactions. Mol. Cell. Biol. 17:3094-3102.
33. Gus Y, Karni R, Levitzki A. 2007. Subunit S5a of the 26S proteasome is regulated by antiapoptotic signals. FEBS J. 274:2815-2831.
34. Axelrod D, Koppel DE, Schlessinger J, Elson E, Webb WW. 1976. Mobility measurement by analysis of fluorescence photobleaching recovery kinetics. Biophys. J. 16:1055-1069.
35. Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K. 2007. WoLF PSORT: protein localization predictor. Nucleic Acids Res. 35:W585-W587.
36. Conchillo-Sole O, de Groot NS, Aviles FX, Vendrell J, Daura X, Ventura S. 2007. AGGRESCAN: a server for the prediction and evaluation of "hot spots" of aggregation in polypeptides. BMC Bioinformatics 8:65-82.
37. Sanchez de Groot N, Pallares I, Aviles FX, Vendrell J, Ventura S. 2005. Prediction of "hot spots" of aggregation in disease-linked polypeptides. BMC Struct. Biol. 5:18-33.
38. Fernandez-Escamilla AM, Rousseau F, Schymkowitz J, Serrano L. 2004. Prediction of sequence-dependent and mutational effects on the aggregation of peptides and proteins. Nat. Biotechnol. 22:1302-1306.
39. Wang SK, Hu CH, Lu MC, Duh CY, Liao PC, Tyan YC. 2009. Novel virus-associated proteins encoded by UL112-113 of human cytomegalovirus. J. Gen. Virol. 90:2840-2848.
40. Patterson GH, Piston DW, Barisas BG. 2000. Föster distances between green fluorescent protein pairs. Anal. Biochem. 284:438-440.
41. Elangovan M, Wallrabe H, Chen Y, Day RN, Barroso M, Periasamy A. Characterization of one- and two-photon excitation fluorescence resonance energy transfer microscopy. Methods 29:58-73.
42. Woulfe JM. 2007. Abnormalities of the nucleus and nuclear inclusions in neurodegenerative disease: a work in progress. Neuropathol. Appl. Neurobiol. 33:2-42.
43. Chiti F. 2006. Relative importance of hydrophobicity, net charge, and secondary structure propensities in protein aggregation, p 43-59, In Uversky VN, Fink AL (ed), Protein misfolding, aggregation, and conformational diseases. Part A. Protein aggregation and conformational diseases. Protein reviews, vol 4. Springer, New York, NY.
44. Aronheim A, Engelberg D, Li N, al-Alawi N, Schlessinger J, Karin M. Membrane targeting of the nucleotide exchange factor Sos is sufficient for activating the Ras signaling pathway. Cell 78:949-961.
45. Kataoka K, Fujiwara KT, Noda M, Nishizawa M. 1994. MafB, a new Maf family transcription activator that can associate with Maf and Fos but not with Jun. Mol. Cell. Biol. 14:7581-7591.
46. Uchiki T, Kim HT, Zhai B, Gygi SP, Johnston JA, O'Bryan JP, Goldberg AL. 2009. The ubiquitin-interacting motif protein, S5a, is ubiquitinated by all types of ubiquitin ligases by a mechanism different from typical substrate recognition. J. Biol. Chem. 284:12622-12632.
47. Wang Q, Young P, Walters KJ. 2005. Structure of S5a bound to monoubiquitin provides a model for polyubiquitin recognition. J. Mol. Biol. 348: 727-739.
48. Chandra A, Chen L, Madura K. 2010. Synthetic lethality of rpn11-1 rpn10Delta is linked to altered proteasome assembly and activity. Curr. Genet. 56:543-557.
49. 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.
50. Kaspari M, Tavalai N, Stamminger T, Zimmermann A, Schilf R, Bogner E. 2008. Proteasome inhibitor MG132 blocks viral DNA replication and assembly of human cytomegalovirus. FEBS Lett. 582:666-672.
51. Sadanari H, Tanaka J, Li Z, Yamada R, Matsubara K, Murayama T. Proteasome inhibitor differentially regulates expression of the major immediate early genes of human cytomegalovirus in human central nervous system-derived cell lines. Virus Res. 142:68-77.
52. Clague MJ, Urbe S. 2010. Ubiquitin: same molecule, different degradation pathways. Cell 143:682-685.
53. Wong E, Bejarano E, Rakshit M, Lee K, Hanson HH, Zaarur N, Phillips GR, Sherman MY, Cuervo AM. 2012. Molecular determinants of selective clearance of protein inclusions by autophagy. Nat. Commun. 3:1240.
54. Mayor T, Graumann J, Bryan J, Maccoss MJ, Deshaies RJ. 2007. Quantitative profiling of ubiquitylated proteins reveals proteasome substrates and the substrate repertoire influenced by the rpn10 receptor pathway. Mol. Cell. Proteomics 6:1885-1895.
55. Bortz E, Whitelegge JP, Jia Q, Zhou ZH, Stewart JP, Wu TT, Sun R. Identification of proteins associated with murine gammaherpesvirus 68 virions. J. Virol. 77:13425-13432.
56. Kim YE, Ahn JH. 2010. Role of the specific interaction of UL112-113 p84 with UL44 DNA polymerase processivity factor in promoting DNA replication of human cytomegalovirus. J. Virol. 84:8409-8421.
57. Kagele D, Rossetto CC, Tarrant MT, Pari GS. 2012. Analysis of the interactions of viral and cellular factors with human cytomegalovirus lytic origin of replication, oriLyt. Virology 424:106-114.
58. Pegoraro G, Voss TC, Martin SE, Tuzmen P, Guha R, Misteli T. 2012. Identification of mammalian protein quality control factors by highthroughput cellular imaging. PLoS One 7:e31684.
59. Rosenbaum JC, Gardner RG. 2011. How a disordered ubiquitin ligase maintains order in nuclear protein homeostasis. Nucleus 2:264-270.
60. Bennett EJ, Bence NF, Jayakumar R, Kopito RR. 2005. Global impairment of the ubiquitin-proteasome system by nuclear or cytoplasmic protein aggregates precedes inclusion body formation. Mol. Cell 17:351-365.
61. Latonen L. 2011. Nucleolar aggresomes as counterparts of cytoplasmic aggresomes in proteotoxic stress. Proteasome inhibitors induce nuclear ribonucleoprotein inclusions that accumulate several key factors of neurodegenerative diseases and cancer. Bioessays 33:386-395.
62. Riedinger C, Boehringer J, Trempe JF, Lowe ED, Brown NR, Gehring K, Noble ME, Gordon C, Endicott JA. 2010. Structure of Rpn10 and its interactions with polyubiquitin chains and the proteasome subunit Rpn12. J. Biol. Chem. 285:33992-34003.
63. Sakata E, Bohn S, Mihalache O, Kiss P, Beck F, Nagy I, Nickell S, Tanaka K, Saeki Y, Forster F, Baumeister W. 2012. Localization of the proteasomal ubiquitin receptors Rpn10 and Rpn13 by electron cryomicroscopy. Proc. Natl. Acad. Sci. U. S. A. 109:1479-1484.
64. Bohn S, Beck F, Sakata E, Walzthoeni T, Beck M, Aebersold R, Forster F, Baumeister W, Nickell S. 2010. Structure of the 26S proteasome from Schizosaccharomyces pombe at subnanometer resolution. Proc. Natl. Acad. Sci. U. S. A. 107:20992-20997.
65. Rani N, Aichem A, Schmidtke G, Kreft SG, Groettrup M. 2012. FAT10 and NUB1L bind to the VWA domain of Rpn10 and Rpn1 to enable proteasome-mediated proteolysis. Nat. Commun. 3:749-769.
66. Nagashima Y, Kowa H, Tsuji S, Iwata A. 2011. FAT10 protein binds to polyglutamine proteins and modulates their solubility. J. Biol. Chem. 286: 29594-29600.
67. Jacquemont C, Taniguchi T. 2007. Proteasome function is required for DNA damage response and fanconi anemia pathway activation. Cancer Res. 67:7395-7405.
68. Lundgren J, Masson P, Mirzaei Z, Young P. 2005. Identification and characterization of a Drosophila proteasome regulatory network. Mol. Cell. Biol. 25:4662-4675.
69. Lundgren J, Masson P, Realini CA, Young P. 2003. Use of RNA interference and complementation to study the function of the Drosophila and human 26S proteasome subunit S13. Mol. Cell. Biol. 23:5320-5330.
70. Moshe A, Gorovits R. 2012. Virus-induced aggregates in infected cells. Viruses 4:2218-2232.
71. Wileman T. 2007. Aggresomes and pericentriolar sites of virus assembly: cellular defense or viral design? Annu. Rev. Microbiol. 61:149-167.
72. Salsman J, Jagannathan M, Paladino P, Chan PK, Dellaire G, Raught B, Frappier L. 2012. Proteomic profiling of the human cytomegalovirus UL35 gene products reveals a role for UL35 in the DNA repair response. J. Virol. 86:806-820.
73. Loveland AN, Nguyen NL, Brignole EJ, Gibson W. 2007. The aminoconserved domain of human cytomegalovirus UL80a proteins is required for key interactions during early stages of capsid formation and virus production. J. Virol. 81:620-628.
74. Livingston CM, Ifrim MF, Cowan AE, Weller SK. 2009. Virus-induced chaperone-enriched (VICE) domains function as nuclear protein quality control centers during HSV-1 infection. PLoS Pathog. 5:e1000619.
75. Yu D, Silva MC, Shenk T. 2003. Functional map of human cytomegalovirus AD169 defined by global mutational analysis. Proc. Natl. Acad. Sci. U. S. A. 100:12396-12401.
76. Dunn W, Chou C, Li H, Hai R, Patterson D, Stolc V, Zhu H, Liu F. Functional profiling of a human cytomegalovirus genome. Proc. Natl. Acad. Sci. U. S. A. 100:14223-14228.
77. Sander G, Konrad A, Thurau M, Wies E, Leubert R, Kremmer E, Dinkel H, Schulz T, Neipel F, Sturzl M. 2008. Intracellular localization map of human herpesvirus 8 proteins. J. Virol. 82:1908-1922.
78. Pearson A, Coen DM. 2002. Identification, localization, and regulation of expression of the UL24 protein of herpes simplex virus type 1. J. Virol. 76:10821-10828.
79. Lymberopoulos MH, Pearson A. 2007. Involvement of UL24 in herpessimplex- virus-1-induced dispersal of nucleolin. Virology 363:397-409.
80. Knizewski L, Kinch L, Grishin NV, Rychlewski L, Ginalski K. 2006. Human herpesvirus 1 UL24 gene encodes a potential PD-(D/E)XK endonuclease. J. Virol. 80:2575-2577.
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.
82. Kasem S, Yu MH, Yamada S, Kodaira A, Matsumura T, Tsujimura K, Madbouly H, Yamaguchi T, Ohya K, Fukushi H. 2010. The ORF37 (UL24) is a neuropathogenicity determinant of equine herpesvirus 1 (EHV-1) in the mouse encephalitis model. Virology 400:259-270.
83. Nascimento R, Costa H, Dias JD, Parkhouse RM. 2011. MHV-68 open reading frame 20 is a nonessential gene delaying lung viral clearance. Arch. Virol. 156:375-386.
84. Blakeney S, Kowalski J, Tummolo D, DeStefano J, Cooper D, Guo M, Gangolli S, Long D, Zamb T, Natuk RJ, Visalli RJ. 2005. Herpes simplex virus type 2 UL24 gene is a virulence determinant in murine and guinea pig disease models. J. Virol. 79:10498-10506.
85. Ito H, Sommer MH, Zerboni L, Baiker A, Sato B, Liang R, Hay J, Ruyechan W, Arvin AM. 2005. Role of the varicella-zoster virus gene product encoded by open reading frame 35 in viral replication in vitro and in differentiated human skin and T cells in vivo. J. Virol. 79:4819-4827.
86. Leiva-Torres GA, Rochette PA, Pearson A. 2010. Differential importance of highly conserved residues in UL24 for herpes simplex virus 1 replication in vivo and reactivation. J. Gen. Virol. 91:1109-1116.
87. Jacobson JG, Chen SH, Cook WJ, Kramer MF, Coen DM. 1998. Importance of the herpes simplex virus UL24 gene for productive ganglionic infection in mice. Virology 242:161-169.