Latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus up-regulates transcription of human telomerase reverse transcriptase promoter through interaction with transcription factor Sp1

Journal of Virology

Volumn 78, Issue 19, 2004, Pages 10348-10359

  Verma, Subhash C ^a   Borah, Sumit ^a   Robertson, Erle S ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYBRID PROTEIN; LATENCY ASSOCIATED NUCLEAR ANTIGEN; TELOMERASE; TELOMERASE REVERSE TRANSCRIPTASE; TRANSCRIPTION FACTOR GAL4; TRANSCRIPTION FACTOR SP1;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL IMMORTALIZATION; CELL NUCLEUS; CONTROLLED STUDY; GENE CONTROL; GENE MAPPING; GENETIC TRANSCRIPTION; HERPES VIRUS INFECTION; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 8; IMMUNOPRECIPITATION; MOLECULE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REPORTER GENE; TRANSCRIPTION INITIATION; UPREGULATION;

ANTIGENS, VIRAL; ARTIFICIAL GENE FUSION; CELL LINE; CELL NUCLEUS; DNA-BINDING PROTEINS; GENES, REPORTER; HERPESVIRUS 8, HUMAN; HUMANS; LUCIFERASES; NUCLEAR PROTEINS; PRECIPITIN TESTS; PROMOTER REGIONS (GENETICS); PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE PROTEINS; SP1 TRANSCRIPTION FACTOR; TELOMERASE; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; UP-REGULATION;

EID: 4544290097     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.78.19.10348-10359.2004     Document Type: Article

References (82)

1. An, J., A. K. Lichtenstein, G. Brent, and M. B. Rettig. 2002. The Kaposi sarcoma-associated herpesvirus (KSHV) induces cellular interleukin 6 expression: role of the KSHV latency-associated nuclear antigen and the AP1 response element. Blood 99:649-654.
2. Aster, J. C., E. S. Robertson, R. P. Hasserjian, J. R. Turner, E. Kieff, and J. Sklar. 1997. Oncogenic forms of NOTCH1 lacking either the primary binding site for RBP-Jkappa or nuclear localization sequences retain the ability to associate with RBP-Jkappa and activate transcription. J. Biol. Chem. 272:11336-11343.
3. Ballestas, M. E., P. A. Chatis, and K. M. Kaye. 1999. Efficient persistence of extrachromosomal KSHV DNA mediated by latency-associated nuclear antigen. Science 284:641-644.
4. Ballestas, M. E., and K. M. Kaye. 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.
5. Berg, J. M. 1992. Sp1 and the subfamily of zinc finger proteins with guaninerich binding sites. Proc. Natl. Acad. Sci. USA 89:11109-11110.
6. Cesarman, E., Y. Chang, P. S. Moore, J. W. Said, and D. M. Knowles. 1995. Kaposi's sarcoma-associated herpesvirus-like DNA sequences in AIDS-related body-cavity-based lymphomas. N. Engl. J. Med. 332:1186-1191.
7. Cesarman, E., P. S. Moore, P. H. Rao, G. Inghirami, D. M. Knowles, and Y. Chang. 1995. In vitro establishment and characterization of two acquired immunodeficiency syndrome-related lymphoma cell lines (BC-1 and BC-2) containing Kaposi's sarcoma-associated herpesvirus-like (KSHV) DNA sequences. Blood 86:2708-2714.
8. Chang, Y., E. Cesarman, M. S. Pessin, F. Lee, J. Culpepper, D. M. Knowles, and P. S. Moore. 1994. Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma. Science 266:1865-1869.
9. Chen, L. I., T. Nishinaka, K. Kwan, I. Kitabayashi, K. Yokoyama, Y. H. Fu, S. Crunwald, and R. Chiu. 1994. The retinoblastoma gene product RB stimulates Sp1-mediated transcription by liberating Sp1 from a negative regulator. Mol. Cell. Biol. 14:4380-4389.
10. Cole, E. G., and K. Gaston. 1997. A functional YY1 binding site is necessary and sufficient to activate Surf-1 promoter activity in response to serum growth factors. Nucleic Acids Res. 25:3705-3711.
11. Cotter, M. A., II, and E. S. Robertson. 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. Cotter, M. A., II, C. Subramanian, and E. S. Robertson. 2001. The Kaposi's sarcoma-associated herpesvirus latency-associated nuclear antigen binds to specific sequences at the left end of the viral genome through its carboxyterminus. Virology 291:241-259.
13. Courey, A. J., D. A. Holtzman, S. P. Jackson, and R. Tjian. 1989. Synergistic activation by the glutamine-rich domains of human transcription factor Sp1. Cell 59:827-836.
14. Datta, P. K., P. Raychaudhuri, and S. Bagchi. 1995. Association of p107 with Sp1: genetically separable regions of p107 are involved in regulation of E2F-and Sp1-dependent transcription. Mol. Cell. Biol. 15:5444-5452.
15. Datto, M. B., Y. Li, J. F. Panus, D. J. Howe, Y. Xiong, and X. F. Wang. 1995. Transforming growth factor beta induces the cyclin-dependent kinase inhibitor p21 through a p53-independent mechanism. Proc. Natl. Acad. Sci. USA 92:5545-5549.
16. Datto, M. B., Y. Yu, and X. F. Wang. 1995. Functional analysis of the transforming growth factor beta responsive elements in the WAF1/Cip1/p21 promoter. J. Biol. Chem. 270:28623-28628.
17. Dupin, N., C. Fisher, P. Kellam, S. Ariad, M. Tulliez, N. Franck, E. van Marck, D. Salmon, I. Gorin, J. P. Escande, R. A. Weiss, K. Alitalo, and C. Boshoff. 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. USA 96:4546-4551.
18. Emili, A., J. Greenblatt, and C. J. Ingles. 1994. Species-specific interaction of the glutamine-rich activation domains of Sp1 with the TATA box-binding protein. Mol. Cell. Biol. 14:1582-1593.
19. Flore, O., S. Rafii, S. Ely, J. J. O'Leary, E. M. Hyjek, and E. Cesarman. 1998. Transformation of primary human endothelial cells by Kaposi's sarcoma-associated herpesvirus. Nature 394:588-592.
20. Friborg, J., Jr, W. Kong, M. O. Hottiger, and G. J. Nabel. 1999. p53 inhibition by the LANA protein of KSHV protects against cell death. Nature 402:889-894.
21. Fujimuro, M, and S. D. Hayward. 2003. The latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus manipulates the activity of glycogen synthase kinase-3beta. J. Virol. 77:8019-8030.
22. Fujimuro, M., F. Y. Wu, C. ApRhys, H. Kajumbula, D. B. Young, G. S. Hayward, and S. D. Hayward. 2003. A novel viral mechanism for dysregulation of beta-catenin in Kaposi's sarcoma-associated herpesvirus latency. Nat. Med. 9:300-306.
23. Gallimore, P. H., and A. S. Turnell. 2001. Adenovirus E1A: remodelling the host cell, a life or death experience. Oncogene 20:7824-7835.
24. Gao, S. J., L. Kingsley, M. Li, W. Zheng, C. Parravicini, J. Ziegler, R. Newton, C. R. Rinaldo, A. Saah, J. Phair, R. Detels, Y. Chang, and P. S. Moore. 1996. KSHV antibodies among Americans, Italians and Ugandans with and without Kaposi's sarcoma. Nat. Med. 2:925-928.
25. Gao, S. J., Y. J. Zhang, J. H. Deng, C. S. Rabkin, O. Flore, and H. B. Jenson. 1999. Molecular polymorphism of Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) latent nuclear antigen: evidence for a large repertoire of viral genotypes and dual infection with different viral genotypes. J. Infect. Dis. 180:1466-1476.
26. Garber, A. C., M. A. Shu, J. Hu, and R. Renne. 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.
27. Garcia, A., S. Cereghini, and E. Sontag. 2000. Protein phosphatase 2A and phosphatidylinositol 3-kinase regulate the activity of Sp1-responsive promoters. J. Biol. Chem. 275:9385-9389.
28. Gill, G., E. Pascal, Z. H. Tseng, and R. Tjian. 1994. A glutamine-rich hydrophobic patch in transcription factor Sp1 contacts the dTAFII110 component of the Drosophila TFIID complex and mediates transcriptional activation. Proc. Natl. Acad. Sci. USA 91:192-196.
29. Greider, C. W. 1991. Chromosome first aid. Cell 67:645-647.
30. Greider, C. W. 1996. Telomere length regulation. Annu. Rev. Biochem. 65:337-365.
31. Groves, A. K., M. A. Cotter, C. Subramanian, and E. S. Robert son. 2001. The latency-associated nuclear antigen encoded by Kaposi's sarcoma-associated herpesvirus activates two major essential Epstein-Barr virus latent promoters. J. Virol. 75:9446-9457.
32. Grundhoff, A., and D. Ganem. 2003. The latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus permits replication of terminal repeat-containing plasmids. J. Virol. 77:2779-2783.
33. Hirano, F., M. Chung, H. Tanaka, N. Maruyama, I. Makino, D. D. Moore, and C. Scheidereit. 1998. Alternative splicing variants of IkappaB beta establish differential NF-kappaB signal responsiveness in human cells. Mol. Cell. Biol. 18:2596-2607.
34. Hirano, F., H. Tanaka, Y. Hirano, M. Hiramoto, H. Handa, I. Makino, and C. Scheidereit 1998. Functional interference of Sp1 and NF-kappaB through the same DNA binding site. Mol. Cell. Biol. 18:1266-1274.
35. Hirano, F., H. Tanaka, T. Miura, Y. Hirano, K. Okamoto, Y. Makino, and I. Makino. 1998. Inhibition of NF-kappaB-dependent transcription of human immunodeficiency virus 1 promoter by a phosphodiester compound of vitamin C and vitamin E, EPC-K1. Immunopharmacology 39:31-38.
36. Horikawa, I., P. L. Cable, C. Afshari, and J. C. Barrett. 1999. Cloning and characterization of the promoter region of human telomerase reverse transcriptase gene. Cancer Res. 59:826-830.
37. Hyun, T. S., C. Subramanian, M. A. Cotter II, R. A. Thomas, and E. S. Robertson. 2001. Latency-associated nuclear antigen encoded by Kaposi's sarcoma-associated herpesvirus interacts with Tat and activates the long terminal repeat of human immunodeficiency virus type 1 in human cells. J. Virol. 75:8761-8771.
38. Johannessen, M., P. A. Olsen, R. Sorensen, B. Johansen, O. M. Seternes, and U. Moens. 2003. A role of the TATA box and the general co-activator hTAF(II)130/135 in promoter-specific trans-activation by simian virus 40 small t antigen. J. Gen. Virol. 84:1887-1897.
39. Kao, W. Y., J. A. Briggs, M. C. Kinney, R. A. Jensen, and R. C. Briggs. 1997. Structure and function analysis of the human myeloid cell nuclear differentiation antigen promoter: evidence for the role of Sp1 and not of c-Myb or PU.1 in myelomonocytic lineage-specific expression. J. Cell Biochem. 65:231-244.
40. Kardassis, D., P. Papakosta, K. Pardali, and A. Moustakas. 1999. c-Jun transactivates the promoter of the human p21 (WAF1/Cip1) gene by acting as a superactivator of the ubiquitous transcription factor Sp1. J. Biol. Chem. 274:29572-29581.
41. Karlseder, J., H. Rotheneder, and E. Wintersberger. 1996. Interaction of Sp1 with the growth and cell cycle-regulated transcription factor E2F. Mol. Cell. Biol. 16:1659-1667.
42. Kedes, D. H., E. Operskalski, M. Busch, R. Kohn, J. Flood, and D. Ganem. 1996. The seroepidemiology of human herpesvirus 8 (Kaposi's sarcoma-associated herpesvirus): distribution of infection in KS risk groups and evidence for sexual transmission. Natl Med: 2:918-924.
43. Kellam, P., C. Boshoff, D. Whitby, S. Matthews, R. A. Weiss, and S. J. Talbot 1997. Identification of a major latent nuclear antigen, LNA-1, in the human herpesvirus 8 genome. J. Hum. Virol. 1:19-29.
44. Kim, N. W., M. A. Piatyszek, K. R. Prowse, C. B. Harley, M. D. West, P. L. Ho, G. M. Coviello, W. E. Wright, S. L. Weinrich, and J. W. Shay. 1994. Specific association of human telomerase activity with immortal cells and cancer. Science 266:2011-2015.
45. Kirch, H. C., S. Ruschen, D. Brockmann, H. Esche, I. Horikawa, J. C. Barrett, B. Opalka, and U. R. Hengge. 2002. Tumor-specific activation of hTERT-derived promoters by tumor suppressive E1A-mutants involves re-cruitment of p300/CBP/HAT and suppression of HDAC-1 and defines a combined tumor targeting and suppression system. Oncogene 21:7991-8000.
46. Knight, J. S., M. A. Cotter II, and E. S. Robertson. 2001 The latency associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus trans-activates the telomerase reverse transcriptase promoter, J. Biol. Chem. 276:22971-22978.
47. Krithivas, A., M. Fujimuro, M. Weidner, D. B. Young and S. D. Hayward. 2002. Protein interactions targeting the latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus to cell chromosomes. J. Virol. 76:11596-11604.
48. Kyo, S., T. Kanaya, M. Takakura, M. Tanaka, and M. Inoue. 1999. Human telomerase reverse transcriptase as a critical determinant of telomerase activity in normal and malignant endometrial tissues. Int. J. Cancer 80:60-63.
49. Kyo, S., M. Takakura, T. Taira, T. Kanaya, H. Itoh, M. Yutsudo, H. Ariga, and M. Inoue. 2000. Sp1 cooperates with c-Myc to activate transcription of the human telomerase reverse transcriptase gene (hTERT). Nucleic Acids Res. 28:669-677.
50. Lania, L., B. Majello, and P. De Luca. 1997. Transcriptional regulation by the Sp family proteins. Int. J. Biochem. Cell Biol. 29:1313-1323.
51. Lee, D., H. Z. Kim, K. W. Jeong, Y. S. Shim, I. Horikawa, J. C. Barrett, and J. Choe. 2002. Human papillomavirus E2 down-regulates the human telomerase reverse transcriptase promoter. J. Biol. Chem. 277:27748-27756.
52. Lee, J. S., K. M. Calvin, and Y. Shi. 1993. Evidence for physical interaction between the zinc-finger transcription factors YY1 and Sp1. Proc. Natl. Acad. Sci. USA 90:6145-6149.
53. Lee, J. S., H. Ngo, D. Kim, and J. H. Chung. 2000. Erythroid Kruppel-like factor is recruited to the CACCC box in the beta-globin promoter but not to the CACCC box in the gamma-globin promoter: the role of the neighboring promoter elements. Proc. Natl. Acad. Sci. USA 97:2468-2473.
54. Liao, W., Y. Tang, S. F. Lin, H. J. Kung, and C. Z. Giam. 2003. K-bZIP of Kaposi's sarcoma-associated herpesvirus/human herpesvirus 8 (KSHV/HHV-8) binds KSHV/HHV-8 Rta and represses Rta-mediated transactivation. J. Virol. 77:3809-3815.
55. Lim, C., Y. Gwack, S. Hwang, S. Kim, and J. Choe. 2001. The transcriptional activity of cAMP response element-binding protein-binding protein is modulated by the latency associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus. J. Biol. Chem. 276:31016-31022.
56. Lim, C., D. Lee, T. Seo, C. Choi, and J. Choe. 2003. Latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus functionally interacts with heterochromatin protein 1. J. Biol. Chem. 278:7397-7405.
57. Lim, C., H. Sohn, Y. Gwack, and J. Choe. 2000. Latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus (human herpesvirus-8) binds ATF4/CREB2 and inhibits its transcriptional activation activity. J. Gen. Virol. 81:2645-2652.
58. Lim, C., H. Sohn, D. Lee, Y. Gwack, and J. Choe. 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.
59. Lin, S. Y., A. R. Black, D. Kostic, S. Pajovic, C. N. Hoover, and J. C. Azizkhan. 1996. Cell cycle-regulated association of E2F1 and Sp1 is related to their functional interaction. Mol. Cell. Biol. 16:1668-1675.
60. Marin, M., A. Karis, P. Visser, F. Grosveld, and S. Philipsen. 1997. Transcription factor Sp1 is essential for early embryonic development but dispensable for cell growth and differentiation. Cell 89:619-628.
61. Meyerson, M., C. M. Counter, E. N. Eaton, L. W. Ellisen, P. Steiner, S. D. Caddie, L. Ziaugra, R. L. Berjersbergen, M. J. Davidoff, Q. Liu, S. Bacchetti, D. A. Haber, and R. A. Weinberg. 1997. hEST2, the putative human telomerase catalytic subunit gene, is up-regulated in tumor cells and during immortalization. Cell 90:785-795.
62. Moore, P. S., and Y. Chang. 1995. Detection of herpesvirus-like DNA sequences in Kaposi's sarcoma in patients with and without HIV infection. N. Engl. J. Med. 332:1181-1185.
63. Moustakas, A., and D. Kardassis. 1998. Regulation of the human p21/WAF1/Cip1 promoter in hepatic cells by functional interactions between Sp1 and Smad family members. Proc. Natl. Acad. Sci. USA 95:6733-6738.
64. Najafl, S. M., Z. Li, K. Makino, R. Shao, and M. C. Hung. 2003. The adenoviral E1A induces p21WAF1/CIP1 expression in cancer cells, Biochem. Biophys. Res. Commun. 305:1099-1104.
65. Piolot, T., M. Tramier, M. Coppey, J. C. Nicolas, and V. Marechal. 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.
66. Platt, G. M., G. R. Simpson, S. Mittnacht, and T. F. Schulz. 1999. Latent nuclear antigen of Kaposi's sarcoma-associated herpesvirus interacts with RINGS, a homolog of the Drosophila female sterile homeotic (fsh) gene. J. Virol. 73:9789-9795.
67. Radkov, S. A., P. Kellam, and C. Boshoff. 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.
68. Rainbow, L., G. M. Platt, G. R. Simpson, R. Sand, S. J. Gao, H. Stoiber, C. S. Herrington, P. S. Moore, and T. F. Schulz. 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.
69. Renne, R., C. Barry, D. Dittmer, N. Compitello, P. O. Brown, and D. Ganem. 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.
70. Robertson, E. S., J. Lin, and E. Kieff. 1996. The amino-terminal domains of Epstein-Barr virus nuclear proteins 3A, 3B, and 3C interact with RB-PJ(kappa). J. Virol. 70:3068-3074.
71. Schwam, D. R., R. L. Luciano, S. S. Mahajan, L. Wong, and A. C. Wilson. 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.
72. Shay, J. W., and S. Bacchetti. 1997. A survey of telomerase activity in human cancer. Eur. J. Cancer 33:787-791.
73. Shinohara, H., M. Fukushi, M. Higuchi, M. Oie, O. Hoshi, T. Ushiki, J. Hayashi, and M. Fujii. 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.
74. Sontag, E., J. M. Sontag, and A. Garcia. 1997. Protein phosphatase 2A is a critical regulator of protein kinase C zeta signaling targeted by SV40 small t to promote cell growth and NF-kappaB activation. EMBO J. 16:5662-5671.
75. Soulier, J., L. Grollet, E. Oksenhendler, P. Cacouh, D. Cazals-Hatem, P. Babinet, M. F. d'Agay, J. P. Clauvel, M. Raphael, L. Degos, et al. 1995. Kaposi's sarcoma-associated herpesvirus-like DNA sequences in multicentric Castleman's disease. Blood 86:1276-1280.
76. Steger, G., C. Schnabel, and H. M. Schmidt. 2002. The hinge region of the human papillomavirus type 8 E2 protein activates the human p21 (WAF1/CIP1) promoter via interaction with Sp1. J. Gen. Virol. 83:503-510.
77. Subramanian, C., and E. S. Robertson. 2002. The metastatic suppressor Nm23-H1 interacts with EBNA3C at sequences located between the glutamine- and proline-rich domains and can cooperate in activation of transcription. J. Virol. 76:8702-8709.
78. Takakura, M., S. Kyo, T. Kanaya, H. Hirano, J. Takeda, M. Yutsudo, and M. Inoue. 1999. Cloning of human telomerase catalytic subunit (hTERT) gene promoter and identification of proximal core promoter sequences essential for transcriptional activation in immortalized and cancer cells. Cancer Res. 59:551-557.
79. Takakura, M., S. Kyo, T. Kanaya, M. Tanaka, and M. Inoue. 1998. Expression of human telomerase subunits and correlation with telomerase activity in cervical cancer. Cancer Res. 58:1558-1561.
80. Udvadia, A. J., D. J. Templeton, and J. M. Horowitz. 1995. Functional interactions between the retinoblastoma (Rb) protein and Sp-family members: superactivation by Rb requires amino acids necessary for growth suppression. Proc. Natl. Acad. Sci. USA 92:3953-3957.
81. Yieh, L., H. B. Sanchez, and T. F. Osborne. 1995. Domains of transcription factor Sp1 required for synergistic activation with sterol regulatory element binding protein 1 of low density lipoprotein receptor promoter. Proc. Natl. Acad. Sci. USA 92:6102-6106.
82. Zhang, Y., X. H. Feng, and R. Derynck. 1998. Smad3 and Smad4 cooperate with c-Jun/c-Fos to mediate TGF-beta-induced transcription. Nature 394:909-913.