The p65 subunit of NF-κB inhibits COL1A1 gene transcription in human dermal and scleroderma fibroblasts through its recruitment on promoter by protein interaction with transcriptional activators (c-Krox, Sp1, and Sp3)

Journal of Biological Chemistry

Volumn 287, Issue 5, 2012, Pages 3462-3478

  Beauchef, Gallic ^a   Bigot, Nicolas ^a   Kypriotou, Magdalini ^a   Renard, Emmanuelle ^a   Porée, Benoît ^a   Widom, Russell ^b   Dompmartin Blanchere, Anne ^c   Oddos, Thierry ^d   Maquart, François Xavier ^e   Demoor, Magali ^a   Boumediene, Karim ^a   Galera, Philippe ^a  

^a Biology and Innovative Therapeutics for Ovarian Cancers group   (France)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Service de Dermatologie   (France)

^d JOHNSON AND JOHNSON   (United States)

^e UNIVERSITÉ DE REIMS CHAMPAGNE ARDENNE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMATIN IMMUNOPRECIPITATION ASSAY; CONSENSUS SEQUENCE; GENE TRANSCRIPTIONS; IMMUNE RESPONSE; IMMUNOPRECIPITATION ASSAYS; INHIBITORY EFFECT; NEW MECHANISMS; NUCLEAR FACTORS; PROTEIN INTERACTION; TRANSCRIPTIONAL ACTIVATORS; TRANSCRIPTIONAL CONTROL; TRANSCRIPTIONAL MECHANISMS; TRANSCRIPTIONAL REGULATION; TYPE I COLLAGEN; ZINC FINGER;

CELL CULTURE; COLLAGEN; FIBROBLASTS; GENE EXPRESSION REGULATION; TRANSCRIPTION FACTORS;

TRANSCRIPTION;

C KROX PROTEIN; COLLAGEN TYPE 1; INTERLEUKIN 1BETA; PARTHENOLIDE; PROTEIN P50; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTOR SP1; TRANSCRIPTION FACTOR SP3; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

ADULT; ARTICLE; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; COL1A1 GENE; COLLAGEN SYNTHESIS; CONSENSUS SEQUENCE; CONTROLLED STUDY; DOWN REGULATION; GENE; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PROTEIN INTERACTION; SCLERODERMA; SKIN FIBROBLAST; TRANSACTIVATION; TRANSCRIPTION REGULATION;

ADULT; CHILD; CHILD, PRESCHOOL; COLLAGEN TYPE I; DERMIS; DNA-BINDING PROTEINS; FIBROBLASTS; GENE EXPRESSION REGULATION; HUMANS; MALE; RESPONSE ELEMENTS; SCLERODERMA, LOCALIZED; SP1 TRANSCRIPTION FACTOR; SP3 TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84856304716     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.286443     Document Type: Article

References (73)

1. Vuorio, E., and de Crombrugghe, B. (1990) The family of collagen genes. Annu. Rev. Biochem. 59, 837-872
2. Ramirez, F., and Di Liberto, M. (1990) Complex and diversified regulatory programs control the expression of vertebrate collagen genes. FASEB J. 4, 1616-1623
3. Jimenez, S. A., Hitraya, E., and Varga, J. (1996) Pathogenesis of scleroderma. Collagen. Rheum. Dis. Clin. North Am. 22, 647-674 (Pubitemid 26396044)
4. Verrecchia, F., and Mauviel, A. (2004) TGF-β and TNF-α. Antagonistic cytokines controlling type I collagen gene expression. Cell. Signal. 16, 873-880 (Pubitemid 38638777)
5. Trojanowska, M., LeRoy, E. C., Eckes, B., and Krieg, T. (1998) Pathogenesis of fibrosis. Type 1 collagen and the skin. J. Mol. Med. 76, 266-274 (Pubitemid 28098712)
6. Jimenez, S. A., Varga, J., Olsen, A., Li, L., Diaz, A., Herhal, J., and Koch, J. (1994) Functional analysis of human α 1(I) procollagen gene promoter. Differential activity in collagen-producing and -nonproducing cells and response to transforming growth factor β1. J. Biol. Chem. 269, 12684-12691
7. Tamaki, T., Ohnishi, K., Hartl, C., LeRoy, E. C., and Trojanowska, M. (1995) Characterization of a GC-rich region containing Sp1 binding site(s) as a constitutive responsive element of the α 2(I) collagen gene in human fibroblasts. J. Biol. Chem. 270, 4299-42304
8. Ihn, H., and Trojanowska, M. (1997) Sp3 is a transcriptional activator of the human α2(I) collagen gene. Nucleic Acids Res. 25, 3712-3717 (Pubitemid 27390193)
9. Ihn, H., LeRoy, E. C., and Trojanowska, M. (1997) Oncostatin M stimulates transcription of the human α2(I) collagen gene via the Sp1/Sp3- binding site. J. Biol. Chem. 272, 24666-24672 (Pubitemid 27418684)
10. Kypriotou, M., Beauchef, G., Chadjichristos, C., Widom, R., Renard, E., Jimenez, S. A., Korn, J., Maquart, F. X., Oddos, T., Von Stetten, O., Pujol, J. P., and Galéra, P. (2007) Human collagen Krox up-regulates type I collagen expression in normal and scleroderma fibroblasts through interaction with Sp1 and Sp3 transcription factors. J. Biol. Chem. 282, 32000-32014 (Pubitemid 350106419)
11. Majello, B., De Luca, P., and Lania, L. (1997) Sp3 is a bifunctional transcription regulator with modular independent activation and repression domains. J. Biol. Chem. 272, 4021-4026 (Pubitemid 27078463)
12. He, S., Sun, J. M., Li, L., and Davie, J. R. (2005) Differential intranuclear organization of transcription factors Sp1 and Sp3. Mol. Biol. Cell 16, 4073-4083 (Pubitemid 41262879)
13. De Luca, P., Majello, B., and Lania, L. (1996) Sp3 represses transcription when tethered to promoter DNA or targeted to promoter proximal RNA. J. Biol. Chem. 271, 8533-8536 (Pubitemid 26125944)
14. Majello, B., De Luca, P., Suske, G., and Lania, L. (1995) Differential transcriptional regulation of c-myc promoter through the same DNA binding sites targeted by Sp1-like proteins. Oncogene 10, 1841-1848
15. Rippe, R. A., Schrum, L. W., Stefanovic, B., Solís-Herruzo, J. A., and Brenner, D. A. (1999) NF-κB inhibits expression of the α1(I) collagen gene. DNA Cell Biol. 18, 751-761 (Pubitemid 29504189)
16. Ghosh, S., May, M. J., and Kopp, E. B. (1998) NF-κB and Rel proteins. Evolutionarily conserved mediators of immune responses. Annu. Rev. Immunol.16, 225-260 (Pubitemid 28183365)
17. Karin, M. (2006) Nuclear factor-κB in cancer development and progression. Nature 441, 431-436
18. Karin, M., and Ben-Neriah, Y. (2000) Phosphorylation meets ubiquitination. The control of NF-κB activity. Annu. Rev. Immunol. 18, 621-663 (Pubitemid 30365393)
19. Baeuerle, P. A., and Baltimore, D. (1996) NF-κB. Ten years after. Cell 87, 13-20
20. Lu, Y., Fukuda, K., Li, Q., Kumagai, N., and Nishida, T. (2006) Role of nuclear factor-κB in interleukin-1-induced collagen degradation by corneal fibroblasts. Exp. Eye Res. 83, 560-568 (Pubitemid 43902777)
21. Baeuerle, P. A., and Baichwal, V. R. (1997) NF-κB as a frequent target for immunosuppressive and anti-inflammatory molecules. Adv. Immunol. 65, 111-137 (Pubitemid 27323247)
22. Okamoto, T., Sakurada, S., Yang, J. P., and Merin, J. P. (1997) Regulation of NFκB and disease control. Identification of a novel serine kinase and thioredoxin as effectors for signal transduction pathway for NF-κB activation. Curr. Top. Cell Regul. 35, 149-161
23. Pahl, H. L. (1999) Activators and target genes of Rel/NF-κB transcription factors. Oncogene 18, 6853-6866
24. Solis-Herruzo, J. A., Brenner, D. A., and Chojkier, M. (1988) Tumor necrosis factor α inhibits collagen gene transcription and collagen synthesis in cultured human fibroblasts. J. Biol. Chem. 263, 5841-5845
25. Mori, K., Hatamochi, A., Ueki, H., Olsen, A., and Jimenez, S. A. (1996) The transcription of human α 1(I) procollagen gene (COL1A1) is suppressed by tumour necrosis factor-α through proximal short promoter elements. Evidence for suppression mechanisms mediated by two nuclear factor binding sites. Biochem. J. 319, 811-816
26. Buss, H., Dörrie, A., Schmitz, M. L., Frank, R., Livingstone, M., Resch, K., and Kracht, M. (2004) Phosphorylation of serine 468 by GSK-3β negatively regulates basal p65 NF-κB activity. J. Biol. Chem. 279, 49571-49574 (Pubitemid 39577758)
27. Zhong, H., SuYang, H., Erdjument-Bromage, H., Tempst, P., and Ghosh, S. (1997) The transcriptional activity of NF-κB is regulated by the IκB-associated PKAc subunit through a cyclic AMP-independent mechanism. Cell 89, 413-424
28. Greene, W. C., and Chen, L. F. (2004) Regulation of NF-κB action by reversible acetylation. Novartis Found. Symp. 259, 208-217; discussion 218-225
29. Quivy, V., and Van Lint, C. (2004) Regulation at multiple levels of NF-κB-mediated transactivation by protein acetylation. Biochem. Pharmacol. 68, 1221-1229 (Pubitemid 39094288)
30. Ryo, A., Suizu, F., Yoshida, Y., Perrem, K., Liou, Y. C., Wulf, G., Rottapel, R., Yamaoka, S., and Lu, K. P. (2003) Regulation of NF-κB signaling by Pin1-dependent prolyl isomerization and ubiquitin-mediated proteolysis of p65/RelA. Mol. Cell 12, 1413-1426 (Pubitemid 38037011)
31. Desterro, J. M., Rodriguez, M. S., and Hay, R. T. (1998) SUMO-1 modification of IκBα inhibits NF-κB activation. Mol. Cell 2, 233-239 (Pubitemid 128373648)
32. Marshall, H. E., Merchant, K., and Stamler, J. S. (2000) Nitrosation and oxidation in the regulation of gene expression. FASEB J. 14, 1889-1900
33. Peterkofsky, B., and Diegelmann, R. (1971) Use of a mixture of proteinasefree collagenases for the specific assay of radioactive collagen in the presence of other proteins. Biochemistry 10, 988-994
34. Goldberg, H., Helaakoski, T., Garrett, L. A., Karsenty, G., Pellegrino, A., Lozano, G., Maity, S., and de Crombrugghe, B. (1992) Tissue-specific expression of the mouse α2(I) collagen promoter. Studies in transgenic mice and in tissue culture cells. J. Biol. Chem. 267, 19622-19630
35. Chomczynski, P., and Sacchi, N. (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159 (Pubitemid 17064313)
36. Livak, K. J., and Schmittgen, T. D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-ΔΔC(T)) method. Methods 25, 402-408 (Pubitemid 34164012)
37. Andrews, N. C., and Faller, D. V. (1991) A rapid micropreparation technique for extraction of DNA-binding proteins from limiting numbers of mammalian cells. Nucleic Acids Res. 19, 2499
38. Ghayor, C., Chadjichristos, C., Herrouin, J. F., Ala-Kokko, L., Suske, G., Pujol, J. P., and Galera, P. (2001)) Sp3 represses the Sp1-mediated transactivation of the human COL2A1 gene in primary and dedifferentiated chondrocytes. J. Biol. Chem. 276, 36881-36895
39. Reuter, U., Chiarugi, A., Bolay, H., and Moskowitz, M. A. (2002) Nuclear factor-κB as a molecular target for migraine therapy. Ann. Neurol. 51, 507-516 (Pubitemid 34260781)
40. Tassorelli, C., Greco, R., Morazzoni, P., Riva, A., Sandrini, G., and Nappi G. (2005) Parthenolide is the component of tanacetum parthenium that inhibits nitroglycerin-induced Fos activation. Studies in an animal model of migraine. Cephalalgia 25, 612-621 (Pubitemid 41026027)
41. Inagaki, Y., Truter, S., Tanaka, S., Di Liberto, M., and Ramirez, F. (1995) Overlapping pathways mediate the opposing actions of tumor necrosis factor-α and transforming growth factor-β on α 2(I) collagen gene transcription. J. Biol. Chem. 270, 3353-3358
42. Kouba, D. J., Chung, K. Y., Nishiyama, T., Vindevoghel, L., Kon, A., Klement, J. F., Uitto, J., and Mauviel, A. (1999) Nuclear factor-κB mediates TNF-alpha inhibitory effect on α 2(I) collagen (COL1A2) gene transcription in human dermal fibroblasts. J. Immunol. 162, 4226-4234 (Pubitemid 29314811)
43. Iraburu, M. J., Domínguez-Rosales, J. A., Fontana, L., Auster, A., García- Trevijano, E. R., Covarrubias-Pinedo, A., Rivas-Estilla, A. M., Greenwel, P., and Rojkind, M. (2000) Tumor necrosis factor α down-regulates expression of the α1(I) collagen gene in rat hepatic stellate cells through a p20C/ EBPβ- and C/EBPδ-dependent mechanism. Hepatology 31, 1086-1093 (Pubitemid 30233233)
44. García-Trevijano, E. R., Iraburu, M. J., Fontana, L., Domínguez-Rosales, J. A., Auster, A., Covarrubias-Pinedo, A., and Rojkind, M. (1999) Transforming growth factor β1 induces the expression of α1(I) procollagen mRNA by a hydrogen peroxide-C/EBPβ-dependent mechanism in rat hepatic stellate cells. Hepatology 29, 960-970 (Pubitemid 29109616)
45. Varela-Rey, M., Montiel-Duarte, C., Osés-Prieto, J. A., López-Zabalza, M. J., Jaffrèzou, J. P., Rojkind, M., and Iraburu, M. J. (2002) p38 MAPK mediates the regulation of α1(I) procollagen mRNA levels by TNF-α and TGF-β in a cell line of rat hepatic stellate cells. FEBS Lett. 528, 133-138 (Pubitemid 35258013)
46. Bitzer, M., von Gersdorff, G., Liang, D., Dominguez-Rosales, A., Beg, A. A., Rojkind, M., and Böttinger, E. P. (2000) A mechanism of suppression of TGF-β/SMAD signaling by NF-κB/RelA. Genes Dev. 14, 187-197 (Pubitemid 30070984)
47. Zhou, A., Scoggin, S., Gaynor, R. B., and Williams, N. S. (2003) Identification of NF-κB-regulated genes induced by TNFα utilizing expression profiling and RNA interference. Oncogene 22, 2054-2064 (Pubitemid 36523642)
48. Yamane, K., Ihn, H., Asano, Y., Jinnin, M., and Tamaki, K. (2003) Antagonistic effects of TNF-α on TGF-β signaling through down-regulation of TGF-beta receptor type II in human dermal fibroblasts. J. Immunol. 171, 3855-3862 (Pubitemid 37254591)
49. Vermes, C., Roebuck, K. A., Chandrasekaran, R., Dobai, J. G., Jacobs, J. J., and Glant, T. T. (2000) Particulate wear debris activates protein tyrosine kinases and nuclear factor κB, which down-regulates type I collagen synthesis in human osteoblasts. J. Bone Miner. Res. 15, 1756-1765 (Pubitemid 30666229)
50. Aoki, T., Kataoka, H., Ishibashi, R., Nozaki, K., Morishita, R., and Hashimoto, N. (2009) Reduced collagen biosynthesis is the hallmark of cerebral aneurysm. Contribution of interleukin-1β and nuclear factor-κB. Arterioscler. Thromb. Vasc. Biol. 29, 1080-1086
51. Schreiber, J., Efron, P. A., Park, J. E., Moldawer, L. L., and Barbul, A. (2005) Adenoviral gene transfer of an NF-κB super-repressor increases collagen deposition in rodent cutaneous wound healing. Surgery 138, 940-946 (Pubitemid 41608490)
52. Ashburner, B. P., Westerheide, S. D., and Baldwin, A. S. (2001) The p65 (RelA) subunit of NF-κB interacts with the histone deacetylase (HDAC) corepressors HDAC1 and HDAC2 to negatively regulate gene expression. Mol. Cell. Biol. 21, 7065-7077 (Pubitemid 32916079)
53. Gao, Z., Chiao, P., Zhang, X., Zhang, X., Lazar, M. A., Seto, E., Young, H. A., and Ye, J. (2005) Coactivators and corepressors of NF-κB in IκB αgene promoter. J. Biol. Chem. 280, 21091-21098 (Pubitemid 40805668)
54. Dechend, R., Hirano, F., Lehmann, K., Heissmeyer, V., Ansieau, S., Wulczyn, F. G., Scheidereit, C., and Leutz, A. (1999) The Bcl-3 oncoprotein acts as a bridging factor between NF-κB/Rel and nuclear co-regulators. Oncogene 18, 3316-3323 (Pubitemid 29286977)
55. Kim, J. M., Oh, Y. K., Kim, Y. J., Youn, J., and Ahn, M. J. (2004) Escherichiacoli up-regulates proinflammatory cytokine expression in granulocyte/macrophage lineages of CD34 stem cells via p50 homodimeric NF-κB. Clin. Exp. Immunol. 137, 341-350 (Pubitemid 39013080)
56. Kurland, J. F., Kodym, R., Story, M. D., Spurgers, K. B., McDonnell, T. J., and Meyn, R. E. (2001) NF-κB1 (p50) homodimers contribute to transcription of the bcl-2 oncogene. J. Biol. Chem. 276, 45380-45386
57. Franzoso, G., Bours, V., Park, S., Tomita-Yamaguchi, M., Kelly, K., and Siebenlist, U. (1992) The candidate oncoprotein Bcl-3 is an antagonist of p50/NF-κB-mediated inhibition. Nature 359, 339-342
58. Udalova, I. A., Richardson, A., Denys, A., Smith, C., Ackerman, H., Foxwell, B., and Kwiatkowski, D. (2000) Functional consequences of a polymorphism affecting NF-κB p50-p50 binding to the TNF promoter region. Mol. Cell. Biol. 20, 9113-9119 (Pubitemid 32246100)
59. Urban, M. B., and Baeuerle, P. A. (1991) The role of the p50 and p65 subunits of NF-κB in the recognition of cognate sequences. New Biol. 3, 279-288
60. Baeuerle, P. A. (1991) The inducible transcription activator NF-κB. Regulation by distinct protein subunits. Biochim. Biophys. Acta 1072, 63-80
61. Schmitz, M. L., Stelzer, G., Altmann, H., Meisterernst, M., and Baeuerle, P. A. (1995) Interaction of the COOH-terminal transactivation domain of p65 NF-κB with TATA-binding protein, transcription factor IIB, and coactivators. J. Biol. Chem. 270, 7219-7226
62. Zhu, N. L., Li, C., Huang, H. H., Sebald, M., Londhe, V. A., Heisterkamp, N., Warburton, D., Bellusci, S., and Minoo, P. (2007) TNF-α represses transcription of human bone morphogenetic protein-4 in lung epithelial cells. Gene 393, 70-80 (Pubitemid 46551526)
63. Artlett, C. M., Chen, S. J., Varga, J., and Jimenez, S. A. (1998) Modulation of basal expression of the human α1(I) procollagen gene (COL1A1) by tandem NF-1/Sp1 promoter elements in normal human dermal fibroblasts. Matrix Biol. 17, 425-434 (Pubitemid 28519875)
64. Chun, J. Y., Hu, Y., Pinder, E., Wu, J., Li, F., and Gao, A. C. (2007) Selenium inhibition of survivin expression by preventing Sp1 binding to its promoter. Mol. Cancer Ther. 6, 2572-2580 (Pubitemid 47480423)
65. Kum, Y. S., Kim, K. H., Park, T. I., Suh, I. S., Oh, H. K., Cho, C. H., Park, J. B., Chang, Y. C., Park, J. H., Lee, K. G., and Park, K. K. (2007) Antifibrotic effect via the regulation of transcription factor Sp1 in lung fibrosis. Biochem. Biophys. Res. Commun. 363, 368-374
66. Ihn, H., and Tamaki, K. (2000) Increased phosphorylation of transcription factor Sp1 in scleroderma fibroblasts. Association with increased expression of the type I collagen gene. Arthritis Rheum. 43, 2240-2247
67. Verrecchia, F., Rossert, J., and Mauviel, A. (2001) Blocking sp1 transcription factor broadly inhibits extracellular matrix gene expression in vitro and in vivo. Implications for the treatment of tissue fibrosis. J. Invest. Dermatol. 116, 755-763 (Pubitemid 32467656)
68. Azakie, A., Fineman, J. R., and He, Y. (2006) Sp3 inhibits Sp1-mediated activation of the cardiac troponin T promoter and is down-regulated during pathological cardiac hypertrophy in vivo. Am. J. Physiol. Heart Circ. Physiol. 291, H600-H611 (Pubitemid 44175065)
69. Teunissen, B. E., van Amersfoorth, S. C., Opthof, T., Jongsma, H. J., and Bierhuizen, M. F. (2002) Sp1 and Sp3 activate the rat connexin40 proximal promoter. Biochem. Biophys. Res. Commun. 292, 71-78 (Pubitemid 34687330)
70. Wang, J., and Bannon, M. J. (2005) Sp1 and Sp3 activate transcription of the human dopamine transporter gene. J. Neurochem. 93, 474-482 (Pubitemid 40547504)
71. Hitraya, E. G., Varga, J., Artlett, C. M., and Jiménez, S. A. (1998) Identification of elements in the promoter region of the α1(I) procollagen gene involved in its up-regulated expression in systemic sclerosis. Arthritis Rheum. 41, 2048-2058 (Pubitemid 28506696)
72. Chen, L. F., and Greene W. C. (2003) Regulation of distinct biological activities of the NF-κB transcription factor complex by acetylation. J. Mol. Med. 81, 549-557
73. Karin, M., Cao, Y., Greten, F. R., and Li, Z. W. (2002) NF-κB in cancer. From innocent bystander to major culprit. Nat. Rev. Cancer 2, 301-310 (Pubitemid 37328783)