Complex alternative cytoplasmic protein isoforms of the Kaposi's sarcoma-associated herpesvirus latency-associated nuclear antigen 1 generated through noncanonical translation initiation

Journal of Virology

Volumn 87, Issue 5, 2013, Pages 2744-2755

  Toptan, Tuna ^a   Fonseca, Lidia ^b   Kwun, Hyun Jin ^a   Chang, Yuan ^a   Moore, Patrick S ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b RESEARCH INSTITUTE FOR MEDICINES IMED ULISBOA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOPLASM PROTEIN; ISOPROTEIN; LATENCY ASSOCIATED NUCLEAR ANTIGEN; ONCOPROTEIN;

ACTIVE TRANSPORT; AMINO TERMINAL SEQUENCE; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DISEASE ASSOCIATION; EMBRYO; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 8; INTERNAL RIBOSOME ENTRY SITE; MOLECULAR WEIGHT; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN MOTIF; TRANSLATION INITIATION;

ANTIGENS, VIRAL; CELL LINE; CYTOPLASM; DNA, VIRAL; HEK293 CELLS; HERPESVIRUS 8, HUMAN; HUMANS; NUCLEAR PROTEINS; PEPTIDE CHAIN INITIATION, TRANSLATIONAL; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY;

EID: 84874688106     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03061-12     Document Type: Article

References (58)

1. 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 265:1865-1869.
2. Ballestas ME, Chatis PA, Kaye KM. 1999. Efficient persistence of extrachromosomal KSHV DNA mediated by latency-associated nuclear antigen. Science 284:641- 644.
3. Ballestas ME, Kaye KM. 2001. Kaposi's sarcoma-associated herpesvirus latency-associated nuclear antigen 1 mediates episome persistence through cis-acting terminal repeat (TR) sequence and specifically binds TR DNA. J. Virol. 75:3250 -3258.
4. Radkov SA, Kellam P, Boshoff C. 2000. The latent nuclear antigen of Kaposi sarcoma-associated herpesvirus targets the retinoblastoma-E2F pathway and with the oncogene Hras transforms primary rat cells. Nat. Med. 6:1121-1127.
5. Friborg J, Jr, Kong W, Hottiger MO, Nabel GJ. 1999. p53 inhibition by the LANA protein of KSHV protects against cell death. Nature 402:889-894.
6. Sato-Matsumura KC, Matsumura T, Nabeshima M, Katano H, Sata T, Koizumi H. 2001. Serological and immunohistochemical detection of human herpesvirus 8 in Kaposi's sarcoma after immunosuppressive therapy for bullous pemphigoid. Br. J. Dermatol. 145:633-637.
7. Kaul R, Verma SC, Robertson ES. 2007. Protein complexes associated with the Kaposi's sarcoma-associated herpesvirus-encoded LANA. Virology 364:317-329.
8. Shamay M, Liu J, Li R, Liao G, Shen L, Greenway M, Hu S, Zhu J, Xie Z, Ambinder RF, Qian J, Zhu H, Hayward SD. 2012. A protein array screen for Kaposi's sarcoma-associated herpesvirus LANA interactors links LANA to TIP60, PP2A activity, and telomere shortening. J. Virol. 86:5179-5191.
9. Chen W, Dittmer DP. 2011. Ribosomal protein S6 interacts with the latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus. J. Virol. 85:9495-9505.
10. Moore PS, Gao SJ, Dominguez G, Cesarman E, Lungu O, Knowles DM, Garber R, Pellett PE, McGeoch DJ, Chang Y. 1996. Primary characterization of a herpesvirus agent associated with Kaposi's sarcoma. J. Virol.70:549-558.
11. Gao S-J, Kingsley L, Hoover DR, Spira TJ, Rinaldo CR, Saah A, Phair J, Detels R, Parry P, Chang Y, Moore PS. 1996. Seroconversion to antibodies against Kaposi's sarcoma-associated herpesvirus-related latent nuclear antigens before the development of Kaposi's sarcoma. N. Engl. J. Med. 335:233-241.
12. Kedes DH, Operskalski E, Busch M, Kohn R, Flood J, Ganem D. 1996. The seroepidemiology of human herpesvirus 8 (Kaposi's sarcomaassociated herpesvirus): distribution of infection in KS risk groups and evidence for sexual transmission. Nat. Med. 2:918-924.
13. Lieberman PM, Hu J, Renne R. 2007. Gammaherpesvirus maintenance and replication during latency, p 379-402. In Arvin A, Mocarski A, Moore PS, Roizman B, Whitley RJ (ed), Human herpesviruses: biology, therapy, and immunoprophylaxis. Cambridge University Press, Cambridge, United Kingdom
14. Moore PS, Chang Y. 2001. Molecular virology of Kaposi's sarcomaassociated herpesvirus. Philos. Trans. R. Soc. Lond. B Biol. Sci. 356:499-516.
15. Rainbow L, Platt GM, Simpson GR, Sarid R, Gao SJ, Stoiber H, Herrington CS, Moore PS, Schulz TF. 1997. The 222-to 234-kilodalton latent nuclear protein (LNA) of Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) is encoded by orf73 and is a component of the latency-associated nuclear antigen. J. Virol. 71:5915-5921.
16. Kedes DH, Lagunoff M, Renne R, Ganem D. 1997. Identification of the gene encoding the major latency-associated nuclear antigen of the Kaposi's sarcoma-associated herpesvirus. J. Clin. Invest. 100:2606-2610.
17. Alkharsah KR, Schulz TF. 2012. A role for the internal repeat of the Kaposi's sarcoma-associated herpesvirus latent nuclear antigen in the persistence of an episomal viral genome. J. Virol. 86:1883-1887.
18. Russo JJ, Bohenzky RA, Chien MC, Chen J, Yan M, Maddalena D, Parry JP, Peruzzi D, Edelman IS, Chang Y, Moore PS. 1996. Nucleotide sequence of the Kaposi sarcoma-associated herpesvirus (HHV8). Proc. Natl. Acad. Sci. U. S. A. 93:14862-14867.
19. Kwun HJ, da Silva SR, Shah IM, Blake N, Moore PS, Chang Y. 2007. Kaposi's sarcoma-associated herpesvirus latency-associated nuclear antigen 1 mimics Epstein-Barr virus EBNA1 immune evasion through central repeat domain effects on protein processing. J. Virol. 81:8225-8235.
20. Lu F, Day L, Gao SJ, Lieberman PM. 2006. Acetylation of the latencyassociated nuclear antigen regulates repression of Kaposi's sarcomaassociated herpesvirus lytic transcription. J. Virol. 80:5273-5282.
21. Gao SJ, Zhang YJ, Deng JH, Rabkin CS, Flore O, Jenson HB. 1999. Molecular polymorphism of Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) latent nuclear antigen: evidence for a large reper-toire of viral genotypes and dual infection with different viral genotypes. J. Infect. Dis. 180:1466-1476. (Erratum, 180:1756.)
22. Gasteiger EHC, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A. 2005. Protein identification and analysis tools on the ExPASy server, 571-607. In Walker JM (ed), The proteomics protocol handbook. Humana Press, Inc, Clifton, NJ.
23. Gao S-J, Boshoff C, Jayachandra S, Weiss RA, Chang Y, Moore PS. 1997. KSHV ORF K9 (vIRF) is an oncogene that inhibits the interferon signaling pathway. Oncogene 15:1979-1986.
24. Glenn M, Rainbow L, Aurad F, Davison A, Schulz TF. 1999. Identification of a spliced gene from Kaposi's sarcoma-associated herpesvirus encoding a protein with similarities to latent membrane proteins 1 and 2A of Epstein-Barr virus. J. Virol. 73:6953-6963.
25. Canham M, Talbot SJ. 2004. A naturally occurring C-terminal truncated isoform of the latent nuclear antigen of Kaposi's sarcoma-associated herpesvirus does not associate with viral episomal DNA. J. Gen. Virol. 85: 1363-1369.
26. Kellam P, Bourboulia D, Dupin N, Shotton C, Fisher C, Talbot S, Boshoff C, Weiss RA. 1999. Characterization of monoclonal antibodies raised against the latent nuclear antigen of human herpesvirus 8. J. Virol. 73:5149-5155.
27. Piolot T, Tramier M, Coppey M, Nicolas JC, Marechal V. 2001. Close but distinct regions of human herpesvirus 8 latency-associated nuclear antigen 1 are responsible for nuclear targeting and binding to human mitotic chromosomes. J. Virol. 75:3948-3959.
28. Shinohara H, Fukushi M, Higuchi M, Oie M, Hoshi O, Ushiki T, Hayashi J, Fujii M. 2002. Chromosome binding site of latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus is essential for persistent episome maintenance and is functionally replaced by histone H1. J. Virol. 76:12917-12924.
29. Schwam DR, Luciano RL, Mahajan SS, Wong L, Wilson AC. 2000. Carboxy terminus of human herpesvirus 8 latency-associated nuclear antigen mediates dimerization, transcriptional repression, and targeting to nuclear bodies. J. Virol. 74:8532-8540.
30. Garber AC, Shu MA, Hu J, Renne R. 2001. DNA binding and modulation of gene expression by the latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus. J. Virol. 75:7882-7892.
31. Cherezova L, Burnside KL, Rose TM. 2011. Conservation of complex nuclear localization signals utilizing classical and non-classical nuclear import pathways in LANA homologs of KSHV and RFHV. PLoS One 6:e18920. doi:10.1371/journal.pone.0018920.
32. Komatsu T, Ballestas ME, Barbera AJ, Kelley-Clarke B, Kaye KM. 2004. KSHV LANA1 binds DNA as an oligomer and residues N-terminal to the oligomerization domain are essential for DNA binding, replication, and episome persistence. Virology 319:225-236.
33. Barbera AJ, Chodaparambil JV, Kelley-Clarke B, Joukov V, Walter JC, Luger K, Kaye KM. 2006. The nucleosomal surface as a docking station for Kaposi's sarcoma herpesvirus LANA. Science 311:856-861.
34. Kozak M. 1999. Initiation of translation in prokaryotes and eukaryotes. Gene 234:187-208.
35. Kozak M. 1983. Comparison of initiation of protein synthesis in procaryotes, eucaryotes, and organelles. Microbiol. Rev. 47:1-45.
36. Gray NK, Wickens M. 1998. Control of translation initiation in animals. Annu. Rev. Cell Dev. Biol. 14:399-458.
37. Kozak M. 1989. The scanning model for translation: an update. J. Cell Biol. 108:229-241.
38. Lee S, Liu B, Huang SX, Shen B, Qian SB. 2012. Global mapping of translation initiation sites in mammalian cells at single-nucleotide resolution. Proc. Natl. Acad. Sci. U. S. A. 109:E2424-E2432.
39. Kozak M. 2002. Pushing the limits of the scanning mechanism for initiation of translation. Gene 299:1-34.
40. Jackson RJ, Kaminski A. 1995. Internal initiation of translation in eukaryotes: the picornavirus paradigm and beyond. RNA 1:985-1000.
41. Dominguez DI, Ryabova LA, Pooggin MM, Schmidt-Puchta W, Futterer J, Hohn T. 1998. Ribosome shunting in cauliflower mosaic virus. Identification of an essential and sufficient structural element. J. Biol. Chem. 273:3669-3678.
42. Ryabova LA, Pooggin MM, Hohn T. 2006. Translation reinitiation and leaky scanning in plant viruses. Virus Res. 119:52-62.
43. Curran J, Kolakofsky D. 1988. Ribosomal initiation from an ACG codon in the Sendai virus P/C mRNA. EMBO J. 7:245-251.
44. Prats H, Kaghad M, Prats AC, Klagsbrun M, Lelias JM, Liauzun P, Chalon P, Tauber JP, Amalric F, Smith JA, et al. 1989. High molecular mass forms of basic fibroblast growth factor are initiated by alternative CUG codons. Proc. Natl. Acad. Sci. U. S. A. 86:1836-1840.
45. Sadler R, Wu L, Forghani B, Renne R, Zhong W, Herndier B, Ganem D. 1999. A complex translational program generates multiple novel proteins from the latently expressed kaposin (K12) locus of Kaposi's sarcomaassociated herpesvirus. J. Virol. 73:5722-5730.
46. Fouillot N, Tlouzeau S, Rossignol JM, Jean-Jean O. 1993. Translation of the hepatitis B virus P gene by ribosomal scanning as an alternative to internal initiation. J. Virol. 67:4886-4895.
47. Farris KD, Pintel DJ. 2010. Adeno-associated virus type 5 utilizes alternative translation initiation to encode a small Rep40-like protein. J. Virol. 84:1193-1197.
48. Corte-Real S, Collins C, Aires da Silva F, Simas JP, Barbas CF, III, Chang Y, Moore P, Goncalves J. 2005. Intrabodies targeting the Kaposi sarcoma-associated herpesvirus latency antigen inhibit viral persistence in lymphoma cells. Blood 106:3797-3802.
49. Chalfie M, Tu Y, Euskirchen G, Ward WW, Prasher DC. 1994. Green fluorescent protein as a marker for gene expression. Science 263:802-805.
50. Kwun HJ, da Silva SR, Qin H, Ferris RL, Tan R, Chang Y, Moore PS. 2011. The central repeat domain 1 of Kaposi's sarcoma-associated herpesvirus (KSHV) latency associated-nuclear antigen 1 (LANA1) prevents cis MHC class I peptide presentation. Virology 412:357-365.
51. Zhang YJ, Deng JH, Rabkin C, Gao SJ. 2000. Hot-spot variations of Kaposi's sarcoma-associated herpesvirus latent nuclear antigen and application in genotyping by PCR-RFLP. J. Gen. Virol. 81:2049-2058.
52. Chen ZJ. 2005. Ubiquitin signaling in the NF-B pathway. Nat. Cell Biol. 7:758-765.
53. Gjoerup O, Chang Y. 2010. Update on human polyomaviruses and cancer. Adv. Cancer Res. 106:1-51.
54. Brierley I, Dos Ramos FJ. 2006. Programmed ribosomal frameshifting in HIV-1 and the SARS-CoV. Virus Res. 119:29-42.
55. Woodard C, Shamay M, Liao G, Zhu J, Ng AN, Li R, Newman R, Rho HS, Hu J, Wan J, Qian J, Zhu H, Hayward SD. 2012. Phosphorylation of the chromatin binding domain of KSHV LANA. PLoS Pathog. 8:e1002972. doi:10.1371/journal.ppat.1002972.
56. Dresang LR, Teuton JR, Feng H, Jacobs JM, Camp DG 2nd, Purvine SO, Gritsenko MA, Li Z, Smith RD, Sugden B, Moore PS, Chang Y. 2011. Coupled transcriptome and proteome analysis of human lymphotropic tumor viruses: insights on the detection and discovery of viral genes. BMC Genomics 12:625. doi:10.1186/1471-2164-12-625.
57. Sarid R, Flore O, Bohenzky RA, Chang Y, Moore PS. 1998. Transcription mapping of the Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) genome in a body cavity-based lymphoma cell line (BC-1). J. Virol. 72:1005-1012.
58. Gao SJ, Kingsley L, Li M, Zheng W, Parravicini C, Ziegler J, Newton R, Rinaldo CR, Saah A, Phair J, Detels R, Chang Y, Moore PS. 1996. KSHV antibodies among Americans, Italians, and Ugandans with or without Kaposi's sarcoma. Nat. Med. 2:925-928.