Fatty Acid Synthase Expression Is Induced by the Epstein-Barr Virus Immediate-Early Protein BRLF1 and Is Required for Lytic Viral Gene Expression

Journal of Virology

Volumn 78, Issue 8, 2004, Pages 4197-4206

  Li, Yuling ^a   Webster Cyriaque, Jennifer ^b   Tomlinson, Christine C ^a   Yohe, Marielle ^a   Kenney, Shannon ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FATTY ACID SYNTHASE; IMMEDIATE EARLY PROTEIN; TRANSCRIPTION FACTOR;

ARTICLE; B LYMPHOCYTE ACTIVATION; ENZYME PHOSPHORYLATION; EPSTEIN BARR VIRUS; GENE INDUCTION; HUMAN; HUMAN CELL; IMMEDIATE EARLY GENE; PALMITOYLATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN MOTIF; REPORTER GENE; VIRUS EXPRESSION; VIRUS GENE; VIRUS GENOME; VIRUS REACTIVATION; VIRUS REPLICATION;

CELL LINE; DNA-BINDING PROTEINS; FATTY ACID SYNTHETASE COMPLEX; GENE EXPRESSION; GENES, REPORTER; GENES, VIRAL; HELA CELLS; HERPESVIRUS 4, HUMAN; HUMANS; IMMEDIATE-EARLY PROTEINS; LEUKOPLAKIA, HAIRY; MITOGEN-ACTIVATED PROTEIN KINASES; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RECEPTORS, ANTIGEN, B-CELL; TONGUE; TRANS-ACTIVATORS; VIRAL PROTEINS; VIRULENCE; VIRUS REPLICATION;

EID: 1842431670     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.78.8.4197-4206.2004     Document Type: Article

References (69)

1. Adamson, A. L., and S. C. Kenney. 1998. Rescue of the Epstein-Barr virus BZLF1 mutant, Z(S186A), early gene activation defect by the BRLF1 gene product. Virology 251:187-197.
2. Adamson, A. L., and S. Kenney. 1999. The Epstein-Barr virus BZLF1 protein interacts physically and functionally with the histone acetylase CREB-binding protein. J. Virol. 73:6551-6558.
3. Adamson, A. L., D. Darr, E. Holley-Guthrie, R. A. Johnson, A. Mauser, J. Swenson, and S. Kenney. 2000. Epstein-Barr virus immediate-early proteins BZLF1 and BRLF1 activate the ATF2 transcription factor by increasing the levels of phosphorylated p38 and c-Jun N-terminal kinases. J. Virol. 74:1224-1233.
4. Berthiaume, L. G. 2002. Insider information: how palmitoylation of Ras makes it a signaling double agent. Sci. STKE 2002:PE41.
5. Blazquez, C., I. Galve-Roperh, and M. Guzman. 2000. De novo-synthesized ceramide signals apoptosis in astrocytes via extracellular signal-regulated kinase. FASEB J. 14:2315-2322.
6. Cadwallader, K. A., H. Paterson, S. G. Macdonald, and J. F. Hancock. 1994. N-terminally myristoylated Ras proteins require palmitoylation or a polybasic domain for plasma membrane localization. Mol. Cell. Biol. 14:4722-4730.
7. Chang, L. K., T. T. Wei, Y. F. Chiu, C. P. Tung, J. Y. Chuang, S. K. Hung, C. Li, and S. T. Liu. 2003. Inhibition of Epstein-Barr virus lytic cycle by (-)-epigallocatechin gallate. Biochem. Biophys. Res. Commun. 301:1062-1068.
8. Chevallier-Greco, A., E. Manet, P. Chavrier, C. Mosnier, J. Daillie, and A. Sergeant. 1986. Both Epstein-Barr virus (EBV)-encoded trans-acting factors, EB1 and EB2, are required to activate transcription from an EBV early promoter. EMBO J. 5:3243-3249.
9. Conti, G., P. Portincasa, and C. Chezzi. 1995. Cerulenin inhibits production of mature virion particles in chick embryo fibroblasts infected by influenza A viruses. Res. Virol. 146:141-149.
10. Countryman, J., and G. Miller. 1985. Activation of expression of latent Epstein-Barr herpesvirus after gene transfer with a small cloned subfragment of heterogeneous viral DNA. Proc. Natl. Acad. Sci. USA 82:4085-4089.
11. Cox, M. A., J. Leahy, and J. M. Hardwick. 1990. An enhancer within the divergent promoter of Epstein-Barr virus responds synergistically to the R and Z transactivators. J. Virol. 64:313-321.
12. D'Agnolo, G., I. S. Rosenfeld, J. Awaya, S. Omura, and P. R. Vagelos. 1973. Inhibition of fatty acid synthesis by the antibiotic cerulenin. Specific inactivation of beta-ketoacyl-acyl carrier protein synthetase. Biochim. Biophys. Acta 326:155-156.
13. Darr, C. D., A. Mauser, and S. Kenney. 2001. Epstein-Barr virus immediate-early protein BRLF1 induces the lytic form of viral replication through a mechanism involving phosphatidylinositol 3-kinase activation. J. Virol. 75:6135-6142.
14. Dudler, T., and M. H. Gelb. 1996. Palmitoylation of Ha-Ras facilitates membrane binding, activation of downstream effectors, and meiotic maturation in Xenopus oocytes. J. Biol. Chem. 271:11541-11547.
15. Dunphy, J. T., and M. E. Linder. 1998. Signalling functions of protein palmitoylation. Biochim. Biophys. Acta 1436:245-261.
16. Farrell, P. J., D. T. Rowe, C. M. Rooney, and T. Kouzarides. 1989. Epstein-Barr virus BZLF1 trans-activator specifically binds to a consensus AP-1 site and is related to c-fos. EMBO J. 8:127-132.
17. Farwell, D. G., K. A. Shera, J. I. Koop, G. A. Bonnet, C. P. Matthews, G. W. Reuther, M. D. Coltrera, J. K. McDougall, and A. J. Klingelhutz. 2000. Genetic and epigenetic changes in human epithelial cells immortalized by telomerase. Am. J. Pathol. 156:1537-1547.
18. Feederle, R., M. Kost, M. Baumann, A. Janz, E. Drouet, W. Hammerschmidt, and H. J. Delecluse. 2000. The Epstein-Barr virus lytic program is controlled by the co-operative functions of two transactivators. EMBO J. 19:3080-3089.
19. Flemington, E., and S. H. Speck. 1990. Identification of phorbol ester response elements in the promoter of Epstein-Barr virus putative lyric switch gene BZLF1. J. Virol. 64:1217-1226.
20. Gorman, C. M., L. F. Moffat, and B. H. Howard. 1982. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol. Cell. Biol. 2:1044-1051.
21. Greenspan, J. S., D. Greenspan, E. T. Lennette, D. I. Abrams, M. A. Conant, V. Petersen, and U. K. Freese. 1985. Replication of Epstein-Barr virus within the epithelial cells of oral "hairy" leukoplakia, an AIDS-associated lesion. N. Engl. J. Med. 313:1564-1571.
22. Gruffat, H., E. Manet, A. Rigolet, and A. Sergeant. 1990. The enhancer factor R of Epstein-Barr virus (EBV) is a sequence-specific DNA binding protein. Nucleic Acids Res. 18:6835-6843.
23. Guinea, R., and L. Carrasco. 1990. Phospholipid biosynthesis and poliovirus genome replication, two coupled phenomena. EMBO J. 9:2011-2016.
24. Hardwick, J. M., P. M. Lieberman, and S. D. Hayward. 1988. A new Epstein-Barr virus transactivator, R, induces expression of a cytoplasmic early antigen. J. Virol. 62:2274-2284.
25. Hardwick, J. M., L. Tse, N. Applegren, J. Nicholas, and M. A. Veliuona. 1992. The Epstein-Barr virus R transactivator (Rta) contains a complex, potent activation domain with properties different from those of VP16. J. Virol. 66:5500-5508.
26. Horton, J. D. 2002. Sterol regulatory element-binding proteins: transcriptional activators of lipid synthesis. Biochem. Soc. Trans. 30:1091-1095.
27. Kenney, S., E. Holley-Guthrie, E. C. Mar, and M. Smith. 1989. The Epstein-Barr virus BMLF1 promoter contains an enhancer element that is responsive to the BZLF1 and BRLF1 transactivators. J. Virol. 63:3878-3883.
28. Kieff, E., and A. B. Rickinson. 2001. Epstein-Barr virus and its replication, p. 2511-2573. In B. Fields, D. Knipe, and P. Howley (ed.), Fields virology, 4rd ed. Lippincott-Raven Publishers, Philadelphia, Pa.
29. Kuhajda, F. P. 2000. Fatty-acid synthase and human cancer: new perspectives on its role in tumor biology. Nutrition 16:202-208.
30. Kuhajda, F. P., E. S. Pizer, J. N. Li, N. S. Mani, G. L. Frehywot, and C. A. Townsend. 2000. Synthesis and antitumor activity of an inhibitor of fatty acid synthase. Proc. Natl. Acad. Sci. USA 97:3450-3454.
31. Kumar, M. V., T. Shimokawa, T. R. Nagy, and M. D. Lane. 2002. Differential effects of a centrally acting fatty acid synthase inhibitor in lean and obese mice. Proc. Natl. Acad. Sci. USA 99:1921-1925.
32. Lieberman, P. M., J. M. Hardwick, and S. D. Hayward. 1989. Responsiveness of the Epstein-Barr virus NotI repeat promoter to the Z transactivator is mediated in a cell-type-specific manner by two independent signal regions. J. Virol. 63:3040-3050.
33. Liu, P., and S. H. Speck. 2003. Synergistic autoactivation of the Epstein-Barr virus immediate-early BRLF1 promoter by Rta and Zta. Virology 310:199-206.
34. Loftus, T. M., D. E. Jaworsky, G. L. Frehywot, C. A. Townsend, G. V. Ronnett, M. D. Lane, and F. P. Kuhajda. 2000. Reduced food intake and body weight in mice treated with fatty acid synthase inhibitors. Science 288:2379-2381.
35. Magana, M. M., and T. F. Osborne. 1996. Two tandem binding sites for sterol regulatory element binding proteins are required for sterol regulation of fatty-acid synthase promoter. J. Biol. Chem. 271:32689-32694.
36. Mauser, A., E. Holley-Guthrie, A. Zanation, W. Yarborough, W. Kaufmann, A. Klingelhutz, W. T. Seaman, and S. Kenney. 2002. The Epstein-Barr virus immediate-early protein BZLF1 induces expression of E2F-1 and other proteins involved in cell cycle progression in primary keratinocytes and gastric carcinoma cells. J. Virol. 76:12543-12552.
37. Moche, M., G. Schneider, P. Edwards, K. Dehesh, and Y. Lindqvist. 1999. Structure of the complex between the antibiotic cerulenin and its target, β-ketoacyl-acyl carrier protein synthase. J. Biol. Chem. 274:6031-6034.
38. Namazue, J., T. Kato, T. Okuno, K. Shiraki, and K. Yamanishi. 1989. Evidence for attachment of fatty acid to varicella-zoster virus glycoproteins and effect of cerulenin on the maturation of varicella-zoster virus glycoproteins. Intervirology 30:268-277.
39. Nemoto, T., S. Terashima, M. Kogure, Y. Hoshino, T. Kusakabe, T. Suzuki, and M. Gotoh. 2001. Overexpression of fatty acid synthase in oesophageal squamous cell dysplasia and carcinoma. Pathobiology 69:297-303.
40. Omura, S. 1976. The antibiotic cerulenin, a novel tool for biochemistry as an inhibitor of fatty acid synthesis. Bacteriol. Rev. 40:681-697.
41. Perry, D. K. 2002. Serine palmitoyltransferase: role in apoptotic de novo ceramide synthesis and other stress responses. Biochim. Biophys. Acta 1585:146-152.
42. Pizer, E. S., F. J. Chrest, J. A. DiGiuseppe, and W. F. Han. 1998. Pharmacological inhibitors of mammalian fatty acid synthase suppress DNA replication and induce apoptosis in tumor cell lines. Cancer Res. 58:4611-4615.
43. Quinlivan, E. B., E. Holley-Guthrie, M. Norris, D. Gutsch, S. L. Bachenheimer, and S. C. Kenney. 1993. Direct BRLF1 binding is required for cooperative BZLF1/BRLF1 activation of the Epstein-Barr virus early promoter, BMRF1. Nucleic Acids Res. 21:1999-2007.
44. Ragoczy, T., L. Heston, and G. Miller. 1998. The Epstein-Barr virus Rta protein activates lytic cycle genes and can disrupt latency in B lymphocytes. J. Virol. 72:7978-7984.
45. Riboni, L., P. Viani, R. Bassi, A. Prinetti, and G. Tettamanti. 1997. The role of sphingolipids in the process of signal transduction. Prog. Lipid Res. 36:153-195.
46. Rickinson, A. B., and E. Kieff. 2001. Epstein-Barr virus, p. 2575-2627. In B. Fields, D. Knipe, and P. Howley (ed.), Fields virology, 4rd ed. Lippincott-Raven Publishers, Philadelphia, Pa.
47. Rooney, C., N. Taylor, J. Countryman, H. Jenson, J. Kolman, and G. Miller. 1988. Genome rearrangements activate the Epstein-Barr virus gene whose product disrupts latency. Proc. Natl. Acad. Sci. USA 85:9801-9805.
48. Sarisky, R. T., Z. Gao, P. M. Lieberman, E. D. Fixman, G. S. Hayward, and S. D. Hayward. 1996. A replication function associated with the activation domain of the Epstein-Barr virus Zta transactivator. J. Virol. 70:8340-8347.
49. Schmitz-Peiffer, C., D. L. Craig, and T. J. Biden. 1999. Ceramide generation is sufficient to account for the inhibition of the insulin -stimulated PKB pathway in C2C12 skeletal muscle cells pretreated with palmitate. J. Biol. Chem. 274:24202-24210.
50. Semenkovich, C. F. 1997. Regulation of fatty acid synthase (FAS). Prog. Lipid Res. 36:43-53.
51. Sinclair, A. J., M. Brimmell, F. Shanahan, and P. J. Farrell. 1991. Pathways of activation of the Epstein-Barr virus productive cycle. J. Virol. 65:2237-2244.
52. Sixbey, J. W., J. G. Nedrud, N. Raab-Traub, R. A. Hanes, and J. S. Pagano. 1984. Epstein-Barr virus replication in oropharyngeal epithelial cells. N. Engl. J. Med. 310:1225-1230.
53. Slabas, A. R., A. Brown, B. S. Sinden, R. Swinhoe, J. W. Simon, A. R. Ashton, P. R. Whitfeld, and K. M. Elborough. 1994. Pivotal reactions in fatty acid synthesis. Prog. Lipid Res. 33:39-46.
54. Takada, K., N. Shimizu, S. Sakuma, and Y. Ono. 1986. trans activation of the latent Epstein-Barr virus (EBV) genome after transfection of the EBV DNA fragment. J. Virol. 57:1016-1022.
55. Takada, K., and Y. Ono. 1989. Synchronous and sequential activation of latently infected Epstein-Barr virus genomes. J. Virol. 63:445-449.
56. Urier, G., M. Buisson, P. Chambard, and A. Sergeant. 1989. The Epstein-Barr virus early protein EB1 activates transcription from different responsive elements including AP-1 binding sites. EMBO J. 8:1447-1453.
57. Van de Sande, T., E. De Schrijver, W. Heyns, G. Verhoeven, and J. V. Swinnen. 2002. Role of the phosphatidylinositol 3′-kinase/PTEN/Akt kinase pathway in the overexpression of fatty acid synthase in LNCaP prostate cancer cells. Cancer Res. 62:642-646.
58. 2-terminal myristoylation and palmitoylation at cysteine-3. J. Cell Biol. 136:1023-1035.
59. Fyn is required for association with the T cell receptor ζ chain through phosphotyrosine-Src homology domain-2 interactions. J. Cell Biol. 145:377-389.
60. Wakil, S. J. 1989. Fatty acid synthase, a proficient multifunctional enzyme. Biochemistry 28:4523-4530.
61. Wang, X., and W. Tian. 2001. Green tea epigallocatechin gallate: a natural inhibitor of fatty-acid synthase. Biochem. Biophys. Res. Commun. 288:1200-1206.
62. Webster-Cyriaque, J., and N. Raab-Traub. 1998. Transcription of Epstein-Barr virus latent cycle genes in oral hairy leukoplakia. Virology 248:53-65.
63. Webster-Cyriaque, J., J. Middeldorp, and N. Raab-Traub. 2000. Hairy leukoplakia: an unusual combination of transforming and permissive Epstein-Barr virus infections. J. Virol. 74:7610-7618.
64. Westphal, E. M., A. Mauser, J. Swenson, M. G. Davis, C. L. Talarico, and S. C. Kenney. 1999. Induction of lytic Epstein-Barr virus (EBV) infection in EBV-associated malignancies using adenovirus vectors in vitro and in vivo. Cancer Res. 59:1485-1491.
65. Willaime, S., P. Vanhoutte, J. Caboche, Y. Lemaigre-Dubreuil, J. Mariani, and B. Brugg. 2001. Ceramide-induced apoptosis in cortical neurons is mediated by an increase in p38 phosphorylation and not by the decrease in ERK phosphorylation. Eur. J. Neurosci. 13:2037-2046.
66. Wolven, A., H. Okamura, Y. Rosenblatt, and M. D. Resh. 1997. Palmitoylation of p59fyn is reversible and sufficient for plasma membrane association. Mol. Biol. Cell 8:1159-1173.
67. Yang, Y. A., W. F. Han, P. J. Morin, F. J. Chrest, and E. S. Pizer. 2002. Activation of fatty acid synthesis during neoplastic transformation: role of mitogen-activated protein kinase and phosphatidylinositol 3-kinase. Exp. Cell Res. 279:80-90.
68. Young, L. S., R. Lau, M. Rowe, G. Niedobitek, G. Packham, F. Shanahan, D. T. Rowe, D. Greenspan, J. S. Greenspan, and A. B. Rickinson. 1991. Differentiation-associated expression of the Epstein-Barr virus BZLF1 transactivator protein in oral hairy leukoplakia. J. Virol. 65:2868-2874.
69. Zalani, S., E. Holley-Guthrie, and S. Kenney. 1996. Epstein-Barr viral latency is disrupted by the IE BRLF1 protein through a cell-specific mechanism. Proc. Natl. Acad. Sci. USA 93:9194-9199.