Dual role of the arginine methyltransferase CARM1 in the regulation of c-Fos target genes

FASEB Journal

Volumn 22, Issue 9, 2008, Pages 3337-3347

  Fauquier, Lucas ^a   Duboé, Carine ^a   Joré, Cécile ^a   Trouche, Didier ^b   Vandel, Laurence ^a,c  

^a UNIVERSITÉ DE TOULOUSE   (France)

^b Université de Toulouse Paul Sabatier   (France)

^c Centre de Biologie du Developpement Toulouse   (France)

Author keywords

AP 1; MMPs; mRNA stability; p160 proteins; Post transcriptional regulation; Transcription

Indexed keywords

COACTIVATOR ASSOCIATED ARGININE METHYLTRANSFERASE 1; METHYLTRANSFERASE; PROTEIN P160; RNA; TRANSCRIPTION FACTOR AP 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GENE CONTROL; GENE EXPRESSION; GENE TARGETING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; ONCOGENE C FOS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RNA INTERFERENCE;

3T3 CELLS; ANIMALS; CELL LINE, TUMOR; GENES, FOS; HISTONE ACETYLTRANSFERASES; HUMANS; MATRIX METALLOPROTEINASE 1; MATRIX METALLOPROTEINASE 13; MATRIX METALLOPROTEINASE 3; MICE; PROMOTER REGIONS (GENETICS); PROTEIN-ARGININE N-METHYLTRANSFERASE; TRANSCRIPTION FACTOR AP-1; TRANSCRIPTION FACTORS;

EID: 51349157134     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.07-104604     Document Type: Article

References (52)

1. Chinenov, Y., and Kerppola, T. K. (2001) Close encounters of many kinds: Fos-Jun interactions that mediate transcription regulatory specificity. Oncogene 20, 2438-2452
2. Jochum, W., Passegue, E., and Wagner, E. F. (2001) AP-1 in mouse development and tumorigenesis. Oncogene 20, 2401-2412
3. Saez, E., Rutberg, S. E., Mueller, E., Oppenheim, H., Smoluk, J., Yuspa, S. H., and Spiegelman, B. M. (1995) c-fos is required for malignant progression of skin tumors. Cell 82, 721-732
4. Hu, E., Mueller, E., Oliviero, S., Papaioannou, V. E., Johnson, R., and Spiegelman, B. M. (1994) Targeted disruption of the c-fos gene demonstrates c-fos-dependent and -independent pathways for gene expression stimulated by growth factors or oncogenes. EMBO J. 13, 3094-3103
5. Yan, C., and Boyd, D. D. (2007) Regulation of matrix metalloproteinase gene expression. J. Cell. Physiol. 211, 19-26
6. Page-McCaw, A., Ewald, A. J., and Werb, Z. (2007) Matrix metalloproteinases and the regulation of tissue remodelling. Nat. Rev. Mol. Cell Biol. 8, 221-233
7. Hong, H., Kohli, K., Trivedi, A., Johnson, D. L., and Stallcup, M. R. (1996) GRIP1, a novel mouse protein that serves as a transcriptional coactivator in yeast for the hormone binding domains of steroid receptors. Proc. Natl. Acad. Sci. U. S. A. 93, 4948-4952
8. Li, H., Gomes, P. J., and Chen, J. D. (1997) RAC3, a steroid/ nuclear receptor-associated coactivator that is related to SRC-1 and TIF2. Proc. Natl. Acad. Sci. U. S. A. 94, 8479-8484
9. Onate, S. A., Boonyaratanakornkit, V., Spencer, T. E., Tsai, S. Y., Tsai, M. J., Edwards, D. P., and O'Malley, B. W. (1998) The steroid receptor coactivator-1 contains multiple receptor interacting and activation domains that cooperatively enhance the activation function 1 (AF1) and AF2 domains of steroid receptors. J. Biol. Chem. 273, 12101-12108
10. Voegel, J. J., Heine, M. J., Zechel, C., Chambon, P., and Gronemeyer, H. (1996) TIF2, a 160 kDa transcriptional mediator for the ligand-dependent activation function AF-2 of nuclear receptors. EMBO J. 15, 3667-3675
11. Anzick, S. L., Kononen, J., Walker, R. L., Azorsa, D. O., Tanner, M. M., Guan, X. Y., Sauter, G., Kallioniemi, O. P., Trent, J. M., and Meltzer, P. S. (1997) AIB1, a steroid receptor coactivator amplified in breast and ovarian cancer. Science 277, 965-968
12. Chen, H., Lin, R. J., Schiltz, R. L., Chakravarti, D., Nash, A., Nagy, L., Privalsky, M. L., Nakatani, Y., and Evans, R. M. (1997) Nuclear receptor coactivator ACTR is a novel histone acetyltransferase and forms a multimeric activation complex with P/CAF and CBP/p300. Cell 90, 569-580
13. Leo, C., and Chen, J. D. (2000) The SRC family of nuclear receptor coactivators. Gene 245, 1-11
14. Chen, D., Ma, H., Hong, H., Koh, S. S., Huang, S. M., Schurter, B. T., Aswad, D. W., and Stallcup, M. R. (1999) Regulation of transcription by a protein methyltransferase. Science 284, 2174-2177
15. Bauer, U. M., Daujat, S., Nielsen, S. J., Nightingale, K., and Kouzarides, T. (2002) Methylation at arginine 17 of histone H3 is linked to gene activation. EMBO Rep. 3, 39-44
16. Ma, H., Baumann, C. T., Li, H., Strahl, B. D., Rice, R., Jelinek, M. A., Aswad, D. W., Allis, C. D., Hager, G. L., and Stallcup, M. R. (2001) Hormone-dependent, CARM1-directed, arginine-specific methylation of histone H3 on a steroid-regulated promoter. Curr. Biol. 11, 1981-1985
17. An, W., Kim, J., and Roeder, R. G. (2004) Ordered cooperative functions of PRMT1, p300, and CARM1 in transcriptional activation by p53. Cell 117, 735-748
18. Covic, M., Hassa, P. O., Saccani, S., Buerki, C., Meier, N. I., Lombardi, C., Imhof, R., Bedford, M. T., Natoli, G., and Hottiger, M. O. (2005) Arginine methyltransferase CARM1 is a promoter-specific regulator of NF-κB- dependent gene expression. EMBO J. 24, 85-96
19. El Messaoudi, S., Fabbrizio, E., Rodriguez, C., Chuchana, P., Fauquier, L., Cheng, D., Theillet, C., Vandel, L., Bedford, M. T., and Sardet, C. (2006) Coactivator-associated arginine methyltransferase 1 (CARM1) is a positive regulator of the Cyclin E1 gene. Proc. Natl. Acad. Sci. U. S. A. 103, 13351-13356
20. Koh, S. S., Li, H., Lee, Y. H., Widelitz, R. B., Chuong, C. M., and Stallcup, M. R. (2002) Synergistic coactivator function by coactivator- associated arginine methyltransferase (CARM) 1 and β-catenin with two different classes of DNA-binding transcriptional activators. J. Biol. Chem. 277, 26031-26035
21. Fujiwara, T., Mori, Y., Chu, D. L., Koyama, Y., Miyata, S., Tanaka, H., Yachi, K., Kubo, T., Yoshikawa, H., and Tohyama, M. (2006) CARM1 regulates proliferation of PC12 cells by methylating HuD. Mol. Cell. Biol. 26, 2273-2285
22. Li, H., Park, S., Kilburn, B., Jelinek, M. A., Henschen-Edman, A., Aswad, D. W., Stallcup, M. R., and Laird-Offringa, I. A. (2002) Lipopolysaccharide- induced methylation of HuR, an mRNA-stabilizing protein, by CARM1: coactivator-associated arginine methyltransferase. J. Biol. Chem. 277, 44623-44630
23. Yadav, N., Lee, J., Kim, J., Shen, J., Hu, M. C., Aldaz, C. M., and Bedford, M. T. (2003) Specific protein methylation defects and gene expression perturbations in coactivator-associated arginine methyltransferase 1-deficient mice. Proc. Natl. Acad. Sci. U. S. A. 100, 6464-6468
24. Vandel, L., Nicolas, E., Vaute, O., Ferreira, R., Ait-Si-Ali, S., and Trouche, D. (2001) Transcriptional repression by the retinoblastoma protein through the recruitment of a histone methyltransferase. Mol. Cell. Biol. 21, 6484-6494
25. Zika, E., Fauquier, L., Vandel, L., and Ting, J. P. (2005) Interplay among coactivator-associated arginine methyltransferase 1, CBP, and CIITA in IFN-γ-inducible MHC-II gene expression. Proc. Natl. Acad. Sci. U. S. A. 102, 16321-16326
26. Lee, S. K., Kim, H. J., Na, S. Y., Kim, T. S., Choi, H. S., Im, S. Y., and Lee, J. W. (1998) Steroid receptor coactivator-1 coactivates activating protein-1-mediated transactivations through interaction with the c-Jun and c-Fos subunits. J. Biol. Chem. 273, 16651-16654
27. Koh, S. S., Chen, D., Lee, Y. H., and Stallcup, M. R. (2001) Synergistic enhancement of nuclear receptor function by p160 coactivators and two coactivators with protein methyltransferase activities. J. Biol. Chem. 276, 1089-1098
28. Eferl, R., and Wagner, E. F. (2003) AP-1: a double-edged sword in tumorigenesis. Nat. Rev. Cancer 3, 859-868
29. Gebhardt, C., Breitenbach, U., Richter, K. H., Furstenberger, G., Mauch, C., Angel, P., and Hess, J. (2005) c-Fos-dependent induction of the small ras-related GTPase Rab11a in skin carcinogenesis. Am. J. Pathol. 167, 243-253
30. Levy, N., Tatomer, D., Herber, C. B., Zhao, X., Tang, H., Sargeant, T., Ball, L. J., Summers, J., Speed, T. P., and Leitman, D. C. (2007) Differential regulation of native estrogen receptor regulatory elements by estradiol, tamoxifen, and raloxifene. Mol. Endocrinol. 22, 287-303
31. Xu, J., Qiu, Y., DeMayo, F. J., Tsai, S. Y., Tsai, M. J., and O'Malley, B. W. (1998) Partial hormone resistance in mice with disruption of the steroid receptor coactivator-1 (SRC-1) gene. Science 279, 1922-1925
32. Nishihara, E., Yoshida-Komiya, H., Chan, C. S., Liao, L., Davis, R. L., O'Malley, B. W., and Xu, J. (2003) SRC-1 null mice exhibit moderate motor dysfunction and delayed development of cerebellar Purkinje cells. J. Neurosci. 23, 213-222
33. Gehin, M., Mark, M., Dennefeld, C., Dierich, A., Gronemeyer, H., and Chambon, P. (2002) The function of TIF2/GRIP1 in mouse reproduction is distinct from those of SRC-1 and p/CIP. Mol. Cell. Biol. 22, 5923-5937
34. Xu, J., Liao, L., Ning, G., Yoshida-Komiya, H., Deng, C., and O'Malley, B. W. (2000) The steroid receptor coactivator SRC-3 (p/CIP/RAC3/AIB1/ACTR/TRAM- 1) is required for normal growth, puberty, female reproductive function, and mammary gland development. Proc. Natl. Acad. Sci. U. S. A. 97, 6379-6384
35. Chevillard-Briet, M., Trouche, D., and Vandel, L. (2002) Control of CBP co-activating activity by arginine methylation. EMBO J. 21, 5457-5466
36. Lee, Y. H., Coonrod, S. A., Kraus, W. L., Jelinek, M. A., and Stallcup, M. R. (2005) Regulation of coactivator complex assembly and function by protein arginine methylation and demethylimination. Proc. Natl. Acad. Sci. U. S. A. 102, 3611-3616
37. Xu, W., Chen, H., Du, K., Asahara, H., Tini, M., Emerson, B. M., Montminy, M., and Evans, R. M. (2001) A transcriptional switch mediated by cofactor methylation. Science 294, 2507-2511
38. Naeem, H., Cheng, D., Zhao, Q., Underhill, C., Tini, M., Bedford, M. T., and Torchia, J. (2007) The activity and stability of the transcriptional coactivator p/CIP/SRC-3 are regulated by CARM1-dependent methylation. Mol. Cell. Biol. 27, 120-134
39. Feng, Q., Yi, P., Wong, J., and O'Malley, B. W. (2006) Signaling within a coactivator complex: methylation of SRC-3/AIB1 is a molecular switch for complex disassembly. Mol. Cell. Biol. 26, 7846-7857
40. Bannister, A. J., and Kouzarides, T. (1995) CBP-induced stimulation of c-Fos activity is abrogated by E1A. EMBO J. 14, 4758-4762
41. Neininger, A., Kontoyiannis, D., Kotlyarov, A., Winzen, R., Eckert, R., Volk, H. D., Holtmann, H., Kollias, G., and Gaestel, M. (2002) MK2 targets AU-rich elements and regulates biosynthesis of tumor necrosis factor and interleukin-6 independently at different post-transcriptional levels. J. Biol. Chem. 277, 3065-3068
42. Rydziel, S., Delany, A. M., and Canalis, E. (2004) AU-rich elements in the collagenase 3 mRNA mediate stabilization of the transcript by cortisol in osteoblasts. J. Biol. Chem. 279, 5397-5404
43. Lopez de Silanes, I., Zhan, M., Lal, A., Yang, X., and Gorospe, M. (2004) Identification of a target RNA motif for RNA-binding protein HuR. Proc. Natl. Acad. Sci. U. S. A. 101, 2987-2992
44. Eberhardt, W., Doller, A., Akool el-S., and Pfeilschifter, J. (2007) Modulation of mRNA stability as a novel therapeutic approach. Pharmacol. Ther. 114, 56-73
45. Barreau, C., Paillard, L., and Osborne, H. B. (2005) AU-rich elements and associated factors: are there unifying principles? Nucleic Acids Res. 33, 7138-7150
46. Brook, M., Tchen, C. R., Santalucia, T., McIlrath, J., Arthur, J. S., Saklatvala, J., and Clark, A. R. (2006) Posttranslational regulation of tristetraprolin subcellular localization and protein stability by p38 mitogen-activated protein kinase and extracellular signal-regulated kinase pathways. Mol. Cell. Biol. 26, 2408-2418
47. Pullmann, R., Jr., Juhaszova, M., Lopez de Silanes, I., Kawai, T., Mazan-Mamczarz, K., Halushka, M. K., and Gorospe, M. (2005) Enhanced proliferation of cultured human vascular smooth muscle cells linked to increased function of RNA-binding protein HuR. J. Biol. Chem. 280, 22819-22826
48. Dixon, D. A., Kaplan, C. D., McIntyre, T. M., Zimmerman, G. A., and Prescott, S. M. (2000) Post-transcriptional control of cyclooxygenase-2 gene expression. The role of the 3′-untranslated region. J. Biol. Chem. 275, 11750-11757
49. Wang, Z. Q., Ovitt, C., Grigoriadis, A. E., Mohle-Steinlein, U., Ruther, U., and Wagner, E. F. (1992) Bone and haematopoietic defects in mice lacking c-fos. Nature 360, 741-745
50. Wagner, E. F., and Eferl, R. (2005) Fos/AP-1 proteins in bone and the immune system. Immunol. Rev. 208, 126-140
51. Grigoriadis, A. E., Schellander, K., Wang, Z. Q., and Wagner, E. F. (1993) Osteoblasts are target cells for transformation in c-fos transgenic mice. J. Cell Biol. 122, 685-701
52. Lemaitre, V., and D'Armiento, J. (2006) Matrix metalloproteinases in development and disease. Birth Defects Res. C Embryo Today 78, 1-10