Functional analysis of Kaposi's sarcoma-associated herpesvirus vFLIP expression reveals a new mode of IRES-mediated translation

RNA

Volumn 20, Issue 11, 2014, Pages 1803-1814

  Othman, Zulkefley ^a   Sulaiman, Mariam K ^a   Willcocks, Margaret M ^a   Ulryck, Nathalie ^b   Blackbourn, David J ^a   Sargueil, Bruno ^b   Roberts, Lisa O ^a   Locker, Nicolas ^a  

^a UNIVERSITY OF SURREY   (United Kingdom)

^b FACULTÉ DES SCIENCES PHARMACEUTIQUES ET BIOLOGIQUES   (France)

Author keywords

EIF4E; IRES; RNA structure; Translation; Viruses

Indexed keywords

INITIATION FACTOR; INITIATION FACTOR 3; INITIATION FACTOR 4A; INITIATION FACTOR 4E; INITIATION FACTOR 4F; INITIATION FACTOR 4G; UNCLASSIFIED DRUG; VFLIP PROTEIN; VIRUS PROTEIN; VIRAL FLIP PROTEIN, HUMAN HERPESVIRUS 8; VIRUS RNA;

ARTICLE; CARCINOGENESIS; CONTROLLED STUDY; HERPES VIRUS; HIGH THROUGHPUT SCREENING; IN VITRO STUDY; INTERNAL RIBOSOME ENTRY SITE; KAPOSI SARCOMA; NONHUMAN; OPEN READING FRAME; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RIBOSOME; RIBOSOME SUBUNIT; RNA STRUCTURE; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; HEK293 CELL LINE; HUMAN; HUMAN HERPESVIRUS 8; METABOLISM; TUMOR CELL LINE;

BINDING SITES; CELL LINE, TUMOR; GENE EXPRESSION REGULATION, VIRAL; HEK293 CELLS; HERPESVIRUS 8, HUMAN; HUMANS; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; RIBOSOMES; RNA, VIRAL; TRANSCRIPTION, GENETIC; VIRAL PROTEINS;

EID: 84908137952     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.045328.114     Document Type: Article

References (86)

1. Ali IK, McKendrick L, Morley SJ, Jackson RJ. 2001. Activity of the hepatitis A virus IRES requires association between the cap-binding translation initiation factor (eIF4E) and eIF4G. J Virol 75: 7854-7863.
2. Ambroziak JA, Blackbourn DJ, Herndier BG, Glogau RG, Gullett JH, McDonald AR, Lennette ET, Levy JA. 1995. Herpes-like sequences in HIV-infected and uninfected Kaposi's sarcoma patients. Science 268: 582-583.
3. Arias C, Weisburd B, Stern-Ginossar N, Mercier A, Madrid AS, Bellare P, Holdorf M, Weissman JS, Ganem D. 2014. KSHV 2.0: A comprehensive annotation of the Kaposi's sarcoma-associated herpesvirus genome using next-generation sequencing reveals novel genomic and functional features. PLoS Pathog 10: E1003847.
4. Aversa SM, Cattelan AM, Salvagno L, Crivellari G, Banna G, Trevenzoli M, Chiarion-Sileni V, Monfardini S. 2005. Treatments of AIDS-related Kaposi's sarcoma. Crit Rev Oncol Hematol 53: 253-265.
5. Bagneris C, Ageichik AV, Cronin N, Wallace B, Collins M, Boshoff C, Waksman G, Barrett T. 2008. Crystal structure of a vFlip-IKKγ complex: Insights into viral activation of the IKK signalosome. Mol Cell 30: 620-631.
6. Ballon G, Chen K, Perez R, Tam W, Cesarman E. 2011. Kaposi sarcoma herpesvirus (KSHV) vFLIP oncoprotein induces B cell transdifferentiation and tumorigenesis in mice. J Clin Invest 121: 1141-1153.
7. Balvay L, Lopez Lastra M, Sargueil B, Darlix JL, Ohlmann T. 2007. Translational control of retroviruses. Nat Rev Microbiol 5: 128-140.
8. Balvay L, Soto Rifo R, Ricci EP, Decimo D, Ohlmann T. 2009. Structural and functional diversity of viral IRESes. Biochim Biophys Acta 1789: 542-557.
9. Bellaousov S, Reuter JS, Seetin MG, Mathews DH. 2013. RNA structure: web servers for RNA secondary structure prediction and analysis. Nucleic Acids Res 41: W471-W474.
10. Bieleski L, Talbot SJ. 2001. Kaposi's sarcoma-associated herpesvirus vCyclin open reading frame contains an internal ribosome entry site. J Virol 75: 1864-1869.
11. Bieleski L, Hindley C, Talbot SJ. 2004. A polypyrimidine tract facilitates the expression of Kaposi's sarcoma-associated herpesvirus vFLIP through an internal ribosome entry site. J Gen Virol 85: 615-620.
12. Boehringer D, Thermann R, Ostareck-Lederer A, Lewis JD, Stark H. 2005. Structure of the hepatitis C virus IRES bound to the human 80S ribosome: remodeling of the HCV IRES. Structure 13: 1695-1706.
13. Bordeleau ME, Mori A, Oberer M, Lindqvist L, Chard LS, Higa T, Belsham GJ, Wagner G, Tanaka J, Pelletier J. 2006. Functional characterization of IRESes by an inhibitor of the RNA helicase eIF4A. Nat Chem Biol 2: 213-220.
14. Borman AM, Michel YM, Kean KM. 2001. Detailed analysis of the requirements of hepatitis A virus internal ribosome entry segment for the eukaryotic initiation factor complex eIF4F. J Virol 75: 7864-7871.
15. Bouvard V, Baan R, Straif K, Grosse Y, Secretan B, El Ghissassi F, Benbrahim-Tallaa L, Guha N, Freeman C, Galichet L, et al. 2009. A review of human carcinogens-part B: biological agents. Lancet Oncol 10: 321-322.
16. Bushell M, Stoneley M, Kong YW, Hamilton TL, Spriggs KA, Dobbyn HC, Qin X, Sarnow P, Willis AE. 2006. Polypyrimidine tract binding protein regulates IRES-mediated gene expression during apoptosis. Mol Cell 23: 401-412.
17. Cencic R, Hall DR, Robert F, Du Y, Min J, Li L, Qui M, Lewis I, Kurtkaya S, Dingledine R, et al. 2011. Reversing chemoresistance by small molecule inhibition of the translation initiation complex eIF4F. Proc Natl Acad Sci 108: 1046-1051.
18. Cesarman E, Chang Y, Moore PS, Said JW, Knowles DM. 1995. Kaposi's sarcoma-associated herpesvirus-like DNA sequences in AIDS-related body-cavity-based lymphomas. N Engl J Med 332: 1186-1191.
19. Chamond N, Locker N, Sargueil B. 2010. The different pathways of HIV genomic RNA translation. Biochem Soc Trans 38: 1548-1552.
20. Chang Y, Cesarman E, Pessin MS, Lee F, Culpepper J, Knowles DM, Moore PS. 1994. Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma. Science 266: 1865-1869.
21. Chaudhary PM, Jasmin A, Eby MT, Hood L. 1999. Modulation of the NF-κ B pathway by virally encoded death effector domains-containing proteins. Oncogene 18: 5738-5746.
22. Colman R, Blackbourn DJ. 2008. Risk factors in the development of Kaposi's sarcoma. AIDS 22: 1629-1632.
23. de Breyne S, Yu Y, Unbehaun A, Pestova TV, Hellen CU. 2009. Direct functional interaction of initiation factor eIF4G with type 1 internal ribosomal entry sites. Proc Natl Acad Sci 106: 9197-9202.
24. Deforges J, Chamond N, Sargueil B. 2012. Structural investigation of HIV-1 genomic RNA dimerization process reveals a role for the Major Splice-site Donor stem loop. Biochimie 94: 1481-1489.
25. Dibrov SM, Ding K, Brunn ND, Parker MA, Bergdahl BM, Wyles DL, Hermann T. 2012. Structure of a hepatitis C virus RNA domain in complex with a translation inhibitor reveals a binding mode reminiscent of riboswitches. Proc Natl Acad Sci 109: 5223-5228.
26. Dibrov SM, Parsons J, Carnevali M, Zhou S, Rynearson KD, Ding K, Garcia Sega E, Brunn ND, Boerneke MA, Castaldi MP, et al. 2014. Hepatitis C virus translation inhibitors targeting the internal ribosomal entry site. J Med Chem 57: 1694-1707.
27. Dittmer DP. 2003. Transcription profile of Kaposi's sarcoma-associated herpesvirus in primary Kaposi's sarcoma lesions as determined by real-time PCR arrays. Cancer Res 63: 2010-2015.
28. Dittmer D, Lagunoff M, Renne R, Staskus K, Haase A, Ganem D. 1998. A cluster of latently expressed genes in Kaposi's sarcoma-associated herpesvirus. J Virol 72: 8309-8315.
29. Dupin N, Fisher C, Kellam P, Ariad S, Tulliez M, Franck N, van Marck E, Salmon D, Gorin I, Escande JP, et al. 1999. Distribution of human herpesvirus-8 latently infected cells in Kaposi's sarcoma, multicentric Castleman's disease, and primary effusion lymphoma. Proc Natl Acad Sci 96: 4546-4551.
30. Easton LE, Locker N, Lukavsky PJ. 2009. Conserved functional domains and a novel tertiary interaction near the pseudoknot drive translational activity of hepatitis C virus and hepatitis C virus-like internal ribosome entry sites. Nucleic Acids Res 37: 5537-5549.
31. Efklidou S, Bailey R, Field N, Noursadeghi M, Collins MK. 2008. vFLIP from KSHV inhibits anoikis of primary endothelial cells. J Cell Sci 121: 450-457.
32. Feoktistova K, Tuvshintogs E, Do A, Fraser CS. 2013. Human eIF4E promotes mRNA restructuring by stimulating eIF4A helicase activity. Proc Natl Acad Sci 110: 13339-13344.
33. Field N, Low W, Daniels M, Howell S, Daviet L, Boshoff C, Collins M. 2003. KSHV vFLIP binds to IKK-γ to activate IKK. J Cell Sci 116: 3721-3728.
34. Ganem D. 2010. KSHV and the pathogenesis of Kaposi sarcoma: Listening to human biology and medicine. J Clin Invest 120: 939-949.
35. Gingras AC, Raught B, Sonenberg N. 1999. eIF4 initiation factors: Effectors of mRNA recruitment to ribosomes and regulators of translation. Annu Rev Biochem 68: 913-963.
36. Grundhoff A, Ganem D. 2001. Mechanisms governing expression of the v-FLIP gene of Kaposi's sarcoma-associated herpesvirus. J Virol 75: 1857-1863.
37. Guasparri I, Keller SA, Cesarman E. 2004. KSHV vFLIP is essential for the survival of infected lymphoma cells. J Exp Med 199: 993-1003.
38. Hajdin CE, Bellaousov S, Huggins W, Leonard CW, Mathews DH, Weeks KM. 2013. Accurate SHAPE-directed RNA secondary structure modeling, including pseudoknots. Proc Natl Acad Sci 110: 5498-5503.
39. Hartmuth K, Urlaub H, Vornlocher HP, Will CL, Gentzel M, Wilm M, Luhrmann R. 2002. Protein composition of human prespliceosomes isolated by a tobramycin affinity-selection method. Proc Natl Acad Sci 99: 16719-16724.
40. Herndier B, Ganem D. 2001. The biology of Kaposi's sarcoma. Cancer Treat Res 104: 89-126.
41. Hinnebusch AG. 2014. The scanning mechanism of eukaryotic translation initiation. Annu Rev Biochem 83: 779-812.
42. Jackson RJ, Hellen CU, Pestova TV. 2010. The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol 11: 113-127.
43. James L, Sargueil B. 2008. RNA secondary structure of the feline immunodeficiency virus 5′UTR and Gag coding region. Nucleic Acids Res 36: 4653-4666.
44. Jenner RG, Alba MM, Boshoff C, Kellam P. 2001. Kaposi's sarcoma-associated herpesvirus latent and lytic gene expression as revealed by DNA arrays. J Virol 75: 891-902.
45. Karabiber F, McGinnis JL, Favorov OV, Weeks KM. 2013. QuShape: rapid, accurate, and best-practices quantification of nucleic acid probing information, resolved by capillary electrophoresis. RNA 19: 63-73.
46. Kieft JS. 2008. Viral IRES RNA structures and ribosome interactions. Trends Biochem Sci 33: 274-283.
47. Kraft JJ, Treder K, Peterson MS, Miller WA. 2013. Cation-dependent folding of 3′ cap-independent translation elements facilitates interaction of a 17-nucleotide conserved sequence with eIF4G. Nucleic Acids Res 41: 3398-3413.
48. Leidal AM, Pringle ES, McCormick C. 2012. Evasion of oncogene-induced senescence by γ-herpesviruses. Curr Opin Virol 2: 748-754.
49. Locker N, Easton LE, Lukavsky PJ. 2006. Affinity purification of eukaryotic 48S initiation complexes. RNA 12: 683-690.
50. Locker N, Easton LE, Lukavsky PJ. 2007. HCV and CSFV IRES domain II mediate eIF2 release during 80S ribosome assembly. EMBO J 26: 795-805.
51. Locker N, Chamond N, Sargueil B. 2011. A conserved structure within the HIV gag open reading frame that controls translation initiation directly recruits the 40S subunit and eIF3. Nucleic Acids Res 39: 2367-2377.
52. LowW, Harries M, Ye H, Du MQ, Boshoff C, Collins M. 2001. Internal ribosome entry site regulates translation of Kaposi's sarcoma-associated herpesvirus FLICE inhibitory protein. J Virol 75: 2938-2945.
53. Lukavsky PJ. 2009. Structure and function of HCV IRES domains. Virus Res 139: 166-171.
54. Martin F, Barends S, Jaeger S, Schaeffer L, Prongidi-Fix L, Eriani G. 2011. Cap-assisted internal initiation of translation of histone H4. Mol Cell 41: 197-209.
55. Matta H, Chaudhary PM. 2004. Activation of alternative NF-κ B pathway by human herpes virus 8-encoded Fas-associated death domainlike IL-1 β-converting enzyme inhibitory protein (vFLIP). Proc Natl Acad Sci 101: 9399-9404.
56. Merrick WC. 2004. Cap-dependent and cap-independent translation in eukaryotic systems. Gene 332: 1-11.
57. Mesri EA, Cesarman E, Boshoff C. 2010. Kaposi's sarcoma and its associated herpesvirus. Nat Rev Cancer 10: 707-719.
58. Moerke NJ, Aktas H, Chen H, Cantel S, Reibarkh MY, Fahmy A, Gross JD, Degterev A, Yuan JY, Chorev M, et al. 2007. Small-molecule inhibition of the interaction between the translation initiation factors eIF4E and eIF4G. Cell 128: 257-267.
59. Mortimer SA, Weeks KM. 2007. A fast-acting reagent for accurate analysis of RNA secondary and tertiary structure by SHAPE chemistry. J Am Chem Soc 129: 4144-4145.
60. Nicholson BL, White KA. 2011. 3′ Cap-independent translation enhancers of positive-strand RNA plant viruses. Curr Opin Virol 1: 373-380.
61. Ohlmann T, Rau M, Pain VM, Morley SJ. 1996. The C-terminal domain of eukaryotic protein synthesis initiation factor (eIF) 4G is sufficient to support cap-independent translation in the absence of eIF4E. EMBO J 15: 1371-1382.
62. Parkin DM. 2006. The global health burden of infection-associated cancers in the year 2002. Int J Cancer 118: 3030-3044.
63. Pause A, Methot N, Svitkin Y, Merrick WC, Sonenberg N. 1994. Dominant negative mutants of mammalian translation initiation factor eIF-4A define a critical role for eIF-4F in cap-dependent and capindependent initiation of translation. EMBO J 13: 1205-1215.
64. Pearce M, Matsumura S, Wilson AC. 2005. Transcripts encoding K12, v- FLIP, v-cyclin, and the microRNA cluster of Kaposi's sarcoma-associated herpesvirus originate from a common promoter. J Virol 79: 14457-14464.
65. Pestova TV, Hellen CU, Shatsky IN. 1996. Canonical eukaryotic initiation factors determine initiation of translation by internal ribosomal entry. Mol Cell Biol 16: 6859-6869.
66. Pisarev AV, Unbehaun A, Hellen CU, Pestova TV. 2007. Assembly and analysis of eukaryotic translation initiation complexes. Methods Enzymol 430: 147-177.
67. Plank TD, Kieft JS. 2012. The structures of nonprotein-coding RNAs that drive internal ribosome entry site function. Wiley Interdiscip Rev RNA 3: 195-212.
68. Redondo N, Sanz MA, Steinberger J, Skern T, Kusov Y, Carrasco L. 2012. Translation directed by hepatitis A virus IRES in the absence of active eIF4F complex and eIF2. PLoS One 7: E52065.
69. Redondo N, Garcia-Moreno M, Sanz MA, Carrasco L. 2013. Translation of viral mRNAs that do not require eIF4E is blocked by the inhibitor 4EGI-1. Virology 444: 171-180.
70. Renne R, Lagunoff M, Zhong W, Ganem D. 1996. The size and conformation of Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) DNA in infected cells and virions. J Virol 70: 8151-8154.
71. Russo JJ, Bohenzky RA, Chien MC, Chen J, Yan M, Maddalena D, Parry JP, Peruzzi D, Edelman IS, Chang Y, et al. 1996. Nucleotide sequence of the Kaposi sarcoma-associated herpesvirus (HHV8). Proc Natl Acad Sci 93: 14862-14867.
72. Sargueil B, McKenna J, Burke JM. 2000. Analysis of the functional role of a G·A sheared base pair by in vitro genetics. J Biol Chem 275: 32157-32166.
73. Soulier J, Grollet L, Oksenhendler E, Cacoub P, Cazals-Hatem D, Babinet P, D'Agay MF, Clauvel JP, Raphael M, Degos L, et al. 1995. Kaposi's sarcoma-associated herpesvirus-like DNA sequences in multicentric Castleman's disease. Blood 86: 1276-1280.
74. Stassinopoulos IA, Belsham GJ. 2001. A novel protein-RNA binding assay: Functional interactions of the foot-and-mouth disease virus internal ribosome entry site with cellular proteins. RNA 7: 114-122.
75. Stoneley M, Chappell SA, Jopling CL, Dickens M, MacFarlane M, Willis AE. 2000. c-Myc protein synthesis is initiated from the internal ribosome entry segment during apoptosis. Mol Cell Biol 20: 1162-1169.
76. Sturzl M, Gaus D, Dirks WG, Ganem D, Jochmann R. 2013. Kaposi's sarcoma-derived cell line SLK is not of endothelial origin, but is a contaminant from a known renal carcinoma cell line. Int J Cancer 132: 1954-1958.
77. Sun Q, Matta H, Lu G, Chaudhary PM. 2006. Induction of IL-8 expression by human herpesvirus 8 encoded vFLIP K13 via NF-κB activation. Oncogene 25: 2717-2726.
78. Sweeney TR, Abaeva IS, Pestova TV, Hellen CU. 2014. The mechanism of translation initiation on Type 1 picornavirus IRESs. EMBO J 33: 76-92.
79. Talbot SJ, Weiss RA, Kellam P, Boshoff C. 1999. Transcriptional analysis of human herpesvirus-8 open reading frames 71, 72, 73, K14, and 74 in a primary effusion lymphoma cell line. Virology 257: 84-94.
80. Thome M, Schneider P, Hofmann K, Fickenscher H, Meinl E, Neipel F, Mattmann C, Burns K, Bodmer JL, Schroter M, et al. 1997. Viral FLICE-inhibitory proteins (FLIPs) prevent apoptosis induced by death receptors. Nature 386: 517-521.
81. Van Eden ME, Byrd MP, Sherrill KW, Lloyd RE. 2004. Demonstrating internal ribosome entry sites in eukaryotic mRNAs using stringent RNA test procedures. RNA 10: 720-730.
82. Wang Z, Treder K, Miller WA. 2009. Structure of a viral cap-independent translation element that functions via high affinity binding to the eIF4E subunit of eIF4F. J Biol Chem 284: 14189-14202.
83. Wang Z, Parisien M, Scheets K, Miller WA. 2011. The cap-binding translation initiation factor, eIF4E, binds a pseudoknot in a viral cap-independent translation element. Structure 19: 868-880.
84. Weill L, James L, Ulryck N, Chamond N, Herbreteau CH, Ohlmann T, Sargueil B. 2010. A new type of IRES within gag coding region recruits three initiation complexes on HIV-2 genomic RNA. Nucleic Acids Res 38: 1367-1381.
85. Willcocks MM, Locker N, Gomwalk Z, Royall E, Bakhshesh M, Belsham GJ, Idamakanti N, Burroughs KD, Reddy PS, Hallenbeck PL, et al. 2011. Structural features of the Seneca Valley virus internal ribosome entry site (IRES) element: A picornavirus with a pestivirus-like IRES. J Virol 85: 4452-4461.
86. Yu Y, Abaeva IS, Marintchev A, Pestova TV, Hellen CU. 2011. Common conformational changes induced in type 2 picornavirus IRESs by cognate trans-acting factors. Nucleic Acids Res 39: 4851-4865.