Mutational analysis of the latency-associated nuclear antigen DNA-binding domain of Kaposi's sarcoma-associated herpesvirus reveals structural conservation among gammaherpesvirus origin-binding proteins

Journal of General Virology

Volumn 91, Issue 9, 2010, Pages 2203-2215

  Han, Soo Jin ^a   Hu, Jianhong ^a   Pierce, Brian ^b   Weng, Zhiping ^b,c   Renne, Rolf ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b BOSTON UNIVERSITY   (United States)

^c Boston University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; EPSTEIN BARR VIRUS ANTIGEN 1; LATENCY ASSOCIATED NUCLEAR ANTIGEN; ORIGIN BINDING PROTEIN; PROLINE; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; BIOINFORMATICS; DNA BINDING; DNA DETERMINATION; DNA REPLICATION; EPSTEIN BARR VIRUS; GAMMAHERPESVIRINAE; GENE MUTATION; GENETIC TRANSCRIPTION; HUMAN HERPESVIRUS 8; IMMUNOPRECIPITATION; LONG TERMINAL REPEAT; MUTAGENESIS; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN MULTIMERIZATION; REGULATORY SEQUENCE; SEQUENCE ALIGNMENT; TRANSCRIPTION REGULATION;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; ANTIGENS, VIRAL; BINDING SITES; CELL LINE; CERCOPITHECUS AETHIOPS; CONSERVED SEQUENCE; DNA REPLICATION; DNA, VIRAL; ELECTROPHORETIC MOBILITY SHIFT ASSAY; EPSTEIN-BARR VIRUS NUCLEAR ANTIGENS; EVOLUTION, MOLECULAR; GAMMAHERPESVIRINAE; HERPESVIRUS 8, HUMAN; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; MUTATION; NUCLEAR PROTEINS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; STRUCTURAL HOMOLOGY, PROTEIN;

HUMAN HERPESVIRUS 4; HUMAN HERPESVIRUS 8;

EID: 77956283378     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.020958-0     Document Type: Article

References (47)

1. Ballestas, M. E. & Kaye, K. M. (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.
2. Ballestas, M. E., Chatis, P. A. & Kaye, K. M. (1999). Efficient persistence of extrachromosomal KSHV DNA mediated by latency-associated nuclear antigen. Science 284, 641-644.
3. Barbera, A. J., Chodaparambil, J. V., Kelley-Clarke, B., Joukov, V., Walter, J. C., Luger, K. & Kaye, K. M. (2006). The nucleosomal surface as a docking station for Kaposi's sarcoma herpesvirus LANA. Science 311, 856-861.
4. Bates, P. A., Kelley, L. A., MacCallum, R. M. & Sternberg, M. J. (2001). Enhancement of protein modeling by human intervention in applying the automatic programs 3D-JIGSAW and 3D-PSSM. Proteins (Suppl. 5), 39-46.
5. Bochkarev, A., Barwell, J. A., Pfuetzner, R. A., Furey, W., Jr, Edwards, A. M. & Frappier, L. (1995). Crystal structure of the DNA-binding domain of the Epstein-Barr virus origin-binding protein EBNA 1. Cell 83, 39-46.
6. Bochkarev, A., Barwell, J. A., Pfuetzner, R. A., Bochkareva, E., Frappier, L. & Edwards, A. M. (1996). Crystal structure of the DNA-binding domain of the Epstein-Barr virus origin-binding protein, EBNA1, bound to DNA. Cell 84, 791-800. (Pubitemid 26094208)
7. Burnside, K. L., Ryan, J. T., Bielefeldt-Ohmann, H., Bruce, A. G., Thouless, M. E., Tsai, C. & Rose, T. M. (2006). RFHVMn ORF73 is structurally related to the KSHV ORF73 latency-associated nuclear antigen (LANA) and is expressed in retroperitoneal fibromatosis (RF) tumor cells. Virology 354, 103-115.
8. Ceccarelli, D. F. & Frappier, L. (2000). Functional analyses of the EBNA1 origin DNA binding protein of Epstein-Barr virus. J Virol 74, 4939-4948.
9. Cesarman, E., Chang, Y., Moore, P. S., Said, J. W. & Knowles, D. M. (1995). Kaposi's sarcoma-associated herpesvirus-like DNA sequences in AIDS-related body-cavity-based lymphomas. N Engl J Med 332, 1186-1191.
10. Chang, Y., Cesarman, E., Pessin, M. S., Lee, F., Culpepper, J., Knowles, D. M. & Moore, P. S. (1994). Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma. Science 266, 1865-1869.
11. Cotter, M. A. & Robertson, E. S. (1999). The latency-associated nuclear antigen tethers the Kaposi's sarcoma-associated herpesvirus genome to host chromosomes in body cavity-based lymphoma cells. Virology 264, 254-264.
12. Cruickshank, J., Shire, K., Davidson, A. R., Edwards, A. M. & Frappier, L. (2000). Two domains of the Epstein-Barr virus origin DNA-binding protein, EBNA1, orchestrate sequence-specific DNA binding. J Biol Chem 275, 22273-22277.
13. de Prat-Gay, G., Gaston, K. & Cicero, D. O. (2008). The papillomavirus E2 DNA binding domain. Front Biosci 13, 6006-6021.
14. Fiser, A. & Sali, A. (2003). ModLoop: automated modeling of loops in protein structures. Bioinformatics 19, 2500-2501. (Pubitemid 38016660)
15. Fujita, T., Ikeda, M., Kusano, S., Yamazaki, M., Ito, S., Obayashi, M. & Yanagi, K. (2001). Amino acid substitution analyses of the DNA contact region, two amphipathic α-helices and a recognition-helix-like helix outside the dimeric β-barrel of Epstein-Barr virus nuclear antigen 1. Intervirology 44, 271-282.
16. Gao, S. J., Kingsley, L., Li, M., Zheng, W., Parravicini, C., Ziegler, J., Newton, R., Rinaldo, C. R., Saah, A. & other authors (1996). KSHV antibodies among Americans, Italians and Ugandans with and without Kaposi's sarcoma. Nat Med 2, 925-928.
17. Garber, A. C., Shu, M. A., 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.
18. Garber, A. C., Hu, J. & Renne, R. (2002). Latency-associated nuclear antigen (LANA) cooperatively binds to two sites within the terminal repeat, and both sites contribute to the ability of LANA to suppress transcription and to facilitate DNA replication. J Biol Chem 277, 27401-27411. (Pubitemid 34951761)
19. Grossman, S. R. & Laimins, L. A. (1996). EBNA1 and E2: a new paradigm for origin-binding proteins? Trends Microbiol 4, 87-89.
20. Grundhoff, A. & Ganem, D. (2003). The latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus permits replication of terminal repeat-containing plasmids. J Virol 77, 2779-2783.
21. Hantz, S., Couvreux, A., Champier, G., Trapes, L., Cotin, S., Denis, F., Bouaziz, S. & Alain, S. (2009). Conserved domains and structure prediction of human cytomegalovirus UL27 protein. Antivir Ther 14, 663-672.
22. Hass, M., Lelke, M., Busch, C., Becker-Ziaja, B. & Gunther, S. (2008). Mutational evidence for a structural model of the Lassa virus RNA polymerase domain and identification of two residues, Gly1394 and Asp1395, that are critical for transcription but not replication of the genome. J Virol 82, 10207-10217.
23. Havranek, J. J., Duarte, C. M. & Baker, D. (2004). A simple physical model for the prediction and design of protein-DNA interactions. J Mol Biol 344, 59-70.
24. Hegde, R. S., Grossman, S. R., Laimins, L. A. & Sigler, P. B. (1992). Crystal structure at 1.7 Å of the bovine papillomavirus-1 E2 DNA-binding domain bound to its DNA target. Nature 359, 505-512.
25. Hirt, B. (1967). Selective extraction of polyoma DNA from infected mouse cell cultures. J Mol Biol 26, 365-369.
26. Hu, J., Garber, A. C. & Renne, R. (2002). The latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus supports latent DNA replication in dividing cells. J Virol 76, 11677-11687.
27. Kedes, D. H., Operskalski, E., Busch, M., Kohn, R., Flood, J. & Ganem, D. (1996). The seroepidemiology of human herpesvirus 8 (Kaposi's sarcoma-associated herpesvirus): distribution of infection in KS risk groups and evidence for sexual transmission. Nat Med 2, 918-924 (erratum: Nat Med 1996 2, 1041).
28. Kelley-Clarke, B., Ballestas, M. E., Srinivasan, V., Barbera, A. J., Komatsu, T., Harris, T. A., Kazanjian, M. & Kaye, K. M. (2007). Determination of Kaposi's sarcoma-associated herpesvirus C-terminal latency-associated nuclear antigen residues mediating chromosome association and DNA binding. J Virol 81, 4348-4356.
29. Liang, H., Petros, A. M., Meadows, R. P., Yoon, H. S., Egan, D. A., Walter, K., Holzman, T. F., Robins, T. & Fesik, S. W. (1996). Solution structure of the DNA-binding domain of a human papillomavirus E2 protein: evidence for flexible DNA-binding regions. Biochemistry 35, 2095-2103.
30. Lieberman, P. M., Hu, J. & Renne, R. (2007). Gammaherpesvirus maintenance and replication during latency. In Human Herpesvirus: Biology. Therapy and Immunoprophylaxis, pp. 379-402. Edited by A. Arvin, G. Campadelli-Fiume, E. Mocarski, P. S. Moore, B. Roizman, R. Whitley and K. Yamanishi. New York: Cambridge University Press.
31. Lim, C., Sohn, H., Lee, D., Gwack, Y. & Choe, J. (2002). Functional dissection of latency-associated nuclear antigen 1 of Kaposi's sarcoma-associated herpesvirus involved in latent DNA replication and transcription of terminal repeats of the viral genome. J Virol 76, 10320-10331.
32. Moss, B., Elroy-Stein, O., Mizukami, T., Alexander, W. A. & Fuerst, T. R. (1990). Product review. New mammalian expression vectors. Nature 348, 91-92.
33. Notredame, C., Higgins, D. G. & Heringa, J. (2000). T-Coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 302, 205-217.
34. Pierce, B., Tong, W. & Weng, Z. (2005). M-ZDOCK: a grid-based approach for Cn symmetric multimer docking. Bioinformatics 21, 1472-1478. (Pubitemid 40542702)
35. Pierce, B., Tong, W. & Weng, Z. (2007). ZRANK: reranking protein docking predictions with an optimized energy function. Proteins 67, 1078-1086.
36. Pirovano, W. & Heringa, J. (2010). Protein secondary structure prediction. Methods Mol Biol 609, 327-348.
37. Purta, E., van Vliet, F., Tricot, C., De Bie, L. G., Feder, M., Skowronek, K., Droogmans, L. & Bujnicki, J. M. (2005). Sequence-structure- function relationships of a tRNA (m7G46) methyltransferase studied by homology modeling and site-directed mutagenesis. Proteins 59, 482-488.
38. Renne, R., Barry, C., Dittmer, D., Compitello, N., Brown, P. O. & Ganem, D. (2001). Modulation of cellular and viral gene expression by the latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus. J Virol 75, 458-468.
39. Sambrook, J. & Russell, D. W. (eds) (2001). Molecular Cloning: a Laboratory Manual, 3rd edn. New York: Cold Spring Harbor Laboratory Press.
40. Schepers, A., Ritzi, M., Bousset, K., Kremmer, E., Yates, J. L., Harwood, J., Diffley, J. F. & Hammerschmidt, W. (2001). Human origin recognition complex binds to the region of the latent origin of DNA replication of Epstein-Barr virus. EMBO J 20, 4588-4602.
41. Schwam, D. R., Luciano, R. L., Mahajan, S. S., Wong, L. & Wilson, A. C. (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. (Pubitemid 30666704)
42. Soulier, J., Grollet, L., Oksenhendler, E., Cacoub, P., Cazals-Hatem, D., Babinet, P., d'Agay, M. F., Clauvel, J. P., Raphael, M. & Degos, L. (1995). Kaposi's sarcoma-associated herpesvirus-like DNA sequences in multi-centric Castleman's disease. Blood 86, 1276-1280.
43. Stedman, W., Deng, Z., Lu, F. & Lieberman, P. M. (2004). ORC, MCM, and histone hyperacetylation at the Kaposi's sarcoma-associated herpesvirus latent replication origin. J Virol 78, 12566-12575.
44. Verma, S. C., Choudhuri, T., Kaul, R. & Robertson, E. S. (2006). Latency-associated nuclear antigen (LANA) of Kaposi's sarcoma-associated herpesvirus interacts with origin recognition complexes at the LANA binding sequence within the terminal repeats. J Virol 80, 2243-2256.
45. Verma, S. C., Lan, K. & Robertson, E. (2007). Structure and function of latency-associated nuclear antigen. Curr Top Microbiol Immunol 312, 101-136. (Pubitemid 47400345)
46. Wong, L. Y. & Wilson, A. C. (2005). Kaposi's sarcoma-associated herpesvirus latency-associated nuclear antigen induces a strong bend on binding to terminal repeat DNA. J Virol 79, 13829-13836.
47. You, J., Srinivasan, V., Denis, G. V., Harrington, W. J., Jr, Ballestas, M. E., Kaye, K. M. & Howley, P. M. (2006). Kaposi's sarcoma-associated herpesvirus latency-associated nuclear antigen interacts with bromodomain protein Brd4 on host mitotic chromosomes. J Virol 80, 8909-8919. (Pubitemid 44359965)