MRTF-A mediates LPS-induced pro-inflammatory transcription by interacting with the COMPASS complex

Journal of Cell Science

Volumn 127, Issue 21, 2014, Pages 4645-4657

  Yu, Liming ^a   Weng, Xinyu ^a   Liang, Peng ^a   Dai, Xin ^a   Wu, Xiaoyan ^a   Xu, Huihui ^a   Fang, Mingming ^a,b   Fang, Fei ^a   Xu, Yong ^a  

^a NANJING MEDICAL UNIVERSITY   (China)

^b Jiangsu Jiankang Vocational Institute   (China)

Author keywords

COMPASS; Epigenetics; MRTF A; NF B; Pro inflammatory transcription

Indexed keywords

COMMUNICATING WITH THE HISTONE H3K4 METHYLTRANSFERASE COMPLEX; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; MYOCARDIN RELATED TRANSCRIPTION FACTOR A; PROTEIN; SYNAPTOTAGMIN I; UNCLASSIFIED DRUG; HISTONE LYSINE METHYLTRANSFERASE; LIPOPOLYSACCHARIDE; MKL1 PROTEIN, HUMAN; MKL1 PROTEIN, MOUSE; TRANSACTIVATOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; COLITIS; CONTROLLED STUDY; DOWN REGULATION; GENE OVEREXPRESSION; GENE SILENCING; GENETIC TRANSCRIPTION; HISTONE MODIFICATION; HUMAN; HUMAN CELL; INFLAMMATION; MEDIATOR; MOUSE; NONHUMAN; PROMOTER REGION; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION INITIATION; ANIMAL; CELL LINE; CHEMICALLY INDUCED; EPIGENETICS; GENETICS; METABOLISM;

ANIMALS; CELL LINE; COLITIS; EPIGENOMICS; HISTONE-LYSINE N-METHYLTRANSFERASE; HUMANS; LIPOPOLYSACCHARIDES; MICE; NF-KAPPA B; TRANS-ACTIVATORS;

EID: 84913593969     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.152314     Document Type: Article

References (53)

1. Alexander, M. R. and Owens, G. K. (2012). Epigenetic control of smooth muscle cell differentiation and phenotypic switching in vascular development and disease. Annu. Rev. Physiol. 74, 13-40.
2. Arvey, A., van der Veeken, J., Samstein, R. M., Feng, Y., Stamatoyannopoulos, J. A. and Rudensky, A. Y. (2014). Inflammation-induced repression of chromatin bound by the transcription factor Foxp3 in regulatory T cells. Nat. Immunol. 15, 580-587.
3. Austenaa, L., Barozzi, I., Chronowska, A., Termanini, A., Ostuni, R., Prosperini, E., Stewart, A. F., Testa, G. and Natoli, G. (2012). The histone methyltransferase Wbp7 controls macrophage function through GPI glycolipid anchor synthesis. Immunity 36, 572-585.
4. Cen, B., Selvaraj, A., Burgess, R. C., Hitzler, J. K., Ma, Z., Morris, S. W. and Prywes, R. (2003). Megakaryoblastic leukemia 1, a potent transcriptional coactivator for serum response factor (SRF), is required for serum induction of SRF target genes. Mol. Cell. Biol. 23, 6597-6608.
5. Chen, D., Fang, F., Yang, Y., Chen, J., Xu, G., Xu, Y. and Gao, Y. (2013). Brahma-related gene 1 (Brg1) epigenetically regulates CAM activation during hypoxic pulmonary hypertension. Cardiovasc. Res. 100, 363-373.
6. Crider, B. J., Risinger, G. M., Jr, Haaksma, C. J., Howard, E. W. and Tomasek, J. J. (2011). Myocardin-related transcription factors A and B are key regulators of TGF-b1-induced fibroblast to myofibroblast differentiation. J. Invest. Dermatol. 131, 2378-2385.
7. Fang, F., Yang, Y., Yuan, Z., Gao, Y., Zhou, J., Chen, Q. and Xu, Y. (2011). Myocardin-related transcription factor A mediates OxLDL-induced endothelial injury. Circ. Res. 108, 797-807.
8. Fang, F., Chen, D., Yu, L., Dai, X., Yang, Y., Tian, W., Cheng, X., Xu, H., Weng, X., Fang, M. et al. (2013). Proinflammatory stimuli engage Brahma related gene 1 and Brahma in endothelial injury. Circ. Res. 113, 986-996.
9. Fuchs, O. (2013). Targeting of NF-kappaB signaling pathway, other signaling pathways and epigenetics in therapy of multiple myeloma. Cardiovasc. Hematol. Disord. Drug Targets 13, 16-34.
10. Ghisletti, S., Barozzi, I., Mietton, F., Polletti, S., De Santa, F., Venturini, E., Gregory, L., Lonie, L., Chew, A., Wei, C. L. et al. (2010). Identification and characterization of enhancers controlling the inflammatory gene expression program in macrophages. Immunity 32, 317-328.
11. Gilles, L., Bluteau, D., Boukour, S., Chang, Y., Zhang, Y., Robert, T., Dessen, P., Debili, N., Bernard, O. A., Vainchenker,W. et al. (2009). MAL/SRF complex is involved in platelet formation and megakaryocyte migration by regulating MYL9 (MLC2) and MMP9. Blood 114, 4221-4232.
12. Gown, A. M., Tsukada, T. and Ross, R. (1986). Human atherosclerosis. II. Immunocytochemical analysis of the cellular composition of human atherosclerotic lesions. Am. J. Pathol. 125, 191-207.
13. Hanna, M., Liu, H., Amir, J., Sun, Y., Morris, S. W., Siddiqui, M. A., Lau, L. F. and Chaqour, B. (2009). Mechanical regulation of the proangiogenic factor CCN1/CYR61 gene requires the combined activities of MRTF-A and CREBbinding protein histone acetyltransferase. J. Biol. Chem. 284, 23125-23136.
14. Helms, W. S., Jeffrey, J. L., Holmes, D. A., Townsend, M. B., Clipstone, N. A. and Su, L. (2007). Modulation of NFAT-dependent gene expression by the RhoA signaling pathway in T cells. J. Leukoc. Biol. 82, 361-369.
15. Hinson, J. S., Medlin, M. D., Lockman, K., Taylor, J. M. and Mack, C. P. (2007). Smooth muscle cell-specific transcription is regulated by nuclear localization of the myocardin-related transcription factors. Am. J. Physiol. 292, H1170-H1180.
16. Holbert, M. A., Sikorski, T., Carten, J., Snowflack, D., Hodawadekar, S. and Marmorstein, R. (2007). The human monocytic leukemia zinc finger histone acetyltransferase domain contains DNA-binding activity implicated in chromatin targeting. J. Biol. Chem. 282, 36603-36613.
17. Hotamisligil, G. S. (2006). Inflammation and metabolic disorders. Nature 444, 860-867.
18. Kim, Y. B., Yu, J., Lee, S. Y., Lee, M. S., Ko, S. G., Ye, S. K., Jong, H. S., Kim, T. Y., Bang, Y. J. and Lee, J. W. (2005). Cell adhesion status-dependent histone acetylation is regulated through intracellular contractility-related signaling activities. J. Biol. Chem. 280, 28357-28364.
19. Krajewski, W. A. and Reese, J. C. (2010). SET domains of histone methyltransferases recognize ISWI-remodeled nucleosomal species. Mol. Cell. Biol. 30, 552-564.
20. Li, P., Spann, N. J., Kaikkonen, M. U., Lu, M., Oh, Y., Fox, J. N., Bandyopadhyay, G., Talukdar, S., Xu, J., Lagakos, W. S. et al. (2013). NCoR repression of LXRs restricts macrophage biosynthesis of insulinsensitizing omega 3 fatty acids. Cell 155, 200-214.
21. Ling, L. and Lobie, P. E. (2004). RhoA/ROCK activation by growth hormone abrogates p300/histone deacetylase 6 repression of Stat5-mediated transcription. J. Biol. Chem. 279, 32737-32750.
22. Lockman, K., Taylor, J. M. and Mack, C. P. (2007). The histone demethylase, Jmjd1a, interacts with the myocardin factors to regulate SMC differentiation marker gene expression. Circ. Res. 101, e115-e123.
23. Luchsinger, L. L., Patenaude, C. A., Smith, B. D. and Layne, M. D. (2011). Myocardin related transcription factor-a complexes activate type I collagen expression in lung fibroblasts. J. Biol. Chem. 286, 44116-44125.
24. Morita, T., Mayanagi, T. and Sobue, K. (2007). Dual roles of myocardin-related transcription factors in epithelial mesenchymal transition via slug induction and actin remodeling. J. Cell Biol. 179, 1027-1042.
25. Natoli, G. (2009). Control of NF-kappaB-dependent transcriptional responses by chromatin organization. Cold Spring Harb. Perspect. Biol. 1, a000224.
26. Natoli, G. (2011). Specialized chromatin patterns in the control of inflammatory gene expression. Curr. Top. Microbiol. Immunol. 349, 61-72.
27. Olson, E. N. and Nordheim, A. (2010). Linking actin dynamics and gene transcription to drive cellular motile functions. Nat. Rev. Mol. Cell Biol. 11, 353-365.
28. Qian, B. Z. and Pollard, J. W. (2010). Macrophage diversity enhances tumor progression and metastasis. Cell 141, 39-51.
29. Ramirez-Carrozzi, V. R., Nazarian, A. A., Li, C. C., Gore, S. L., Sridharan, R., Imbalzano, A. N. and Smale, S. T. (2006). Selective and antagonistic functions of SWI/SNF and Mi-2beta nucleosome remodeling complexes during an inflammatory response. Genes Dev. 20, 282-296.
30. Rosette, C. and Karin, M. (1995). Cytoskeletal control of gene expression: depolymerization of microtubules activates NF-kappa B. J. Cell Biol. 128, 1111-1119.
31. Sans, M., Panés, J., Ardite, E., Elizalde, J. I., Arce, Y., Elena, M., Palacín, A., Fernández-Checa, J. C., Anderson, D. C., Lobb, R. et al. (1999). VCAM-1 and ICAM-1 mediate leukocyte-endothelial cell adhesion in rat experimental colitis. Gastroenterology 116, 874-883.
32. Selvaraj, A. and Prywes, R. (2003). Megakaryoblastic leukemia-1/2, a transcriptional co-activator of serum response factor, is required for skeletal myogenic differentiation. J. Biol. Chem. 278, 41977-41987.
33. Shilatifard, A. (2012). The COMPASS family of histone H3K4 methylases: mechanisms of regulation in development and disease pathogenesis. Annu. Rev. Biochem. 81, 65-95.
34. Smale, S. T. (2011). Hierarchies of NF-κB target-gene regulation. Nat. Immunol. 12, 689-694.
35. Small, E. M., Thatcher, J. E., Sutherland, L. B., Kinoshita, H., Gerard, R. D., Richardson, J. A., Dimaio, J. M., Sadek, H., Kuwahara, K. and Olson, E. N. (2010). Myocardin-related transcription factor-a controls myofibroblast activation and fibrosis in response to myocardial infarction. Circ. Res. 107, 294-304.
36. Stoneman, V., Braganza, D., Figg, N., Mercer, J., Lang, R., Goddard, M. and Bennett, M. (2007). Monocyte/macrophage suppression in CD11b diphtheria toxin receptor transgenic mice differentially affects atherogenesis and established plaques. Circ. Res. 100, 884-893.
37. Sun, Y., Boyd, K., Xu, W., Ma, J., Jackson, C. W., Fu, A., Shillingford, J. M., Robinson, G. W., Hennighausen, L., Hitzler, J. K. et al. (2006). Acute myeloid leukemia-associated Mkl1 (Mrtf-a) is a key regulator of mammary gland function. Mol. Cell. Biol. 26, 5809-5826.
38. Tam, W. L. and Weinberg, R. A. (2013). The epigenetics of epithelialmesenchymal plasticity in cancer. Nat. Med. 19, 1438-1449.
39. Tang, Z., Chen, W. Y., Shimada, M., Nguyen, U. T., Kim, J., Sun, X. J., Sengoku, T., McGinty, R. K., Fernandez, J. P., Muir, T. W. et al. (2013). SET1 and p300 act synergistically, through coupled histone modifications, in transcriptional activation by p53. Cell 154, 297-310.
40. Tian, W., Xu, H., Fang, F., Chen, Q., Xu, Y. and Shen, A. (2013). Brahma-related gene 1 bridges epigenetic regulation of proinflammatory cytokine production to steatohepatitis in mice. Hepatology 58, 576-588.
41. Tugal, D., Liao, X. and Jain, M. K. (2013). Transcriptional control of macrophage polarization. Arterioscler. Thromb. Vasc. Biol. 33, 1135-1144.
42. Wang, D. Z., Li, S., Hockemeyer, D., Sutherland, L., Wang, Z., Schratt, G., Richardson, J. A., Nordheim, A. and Olson, E. N. (2002). Potentiation of serum response factor activity by a family of myocardin-related transcription factors. Proc. Natl. Acad. Sci. USA 99, 14855-14860.
43. Wang, X., Zhu, K., Li, S., Liao, Y., Du, R., Zhang, X., Shu, H. B., Guo, A. Y., Li, L. and Wu, M. (2012). MLL1, a H3K4 methyltransferase, regulates the TNFastimulated activation of genes downstream of NF-κB. J. Cell Sci. 125, 4058-4066.
44. Weber, C., Zernecke, A. and Libby, P. (2008). The multifaceted contributions of leukocyte subsets to atherosclerosis: lessons from mouse models. Nat. Rev. Immunol. 8, 802-815.
45. Wu, M., Wang, P. F., Lee, J. S., Martin-Brown, S., Florens, L., Washburn, M. and Shilatifard, A. (2008). Molecular regulation of H3K4 trimethylation by Wdr82, a component of human Set1/COMPASS. Mol. Cell. Biol. 28, 7337-7344.
46. Wynn, T. A., Chawla, A. and Pollard, J. W. (2013). Macrophage biology in development, homeostasis and disease. Nature 496, 445-455.
47. Xu, Y., Luchsinger, L., Lucey, E. C. and Smith, B. D. (2011). The effect of class II transactivator mutations on bleomycin-induced lung inflammation and fibrosis. Am. J. Respir. Cell Mol. Biol. 44, 898-905.
48. Xu, Y., Qian, L., Zong, G., Ma, K., Zhu, X., Zhang, H., Li, N., Yang, Q., Bai, H., Ben, J. et al. (2012). Class A scavenger receptor promotes cerebral ischemic injury by pivoting microglia/macrophage polarization. Neuroscience 218, 35-48.
49. Yang, Y., Chen, D., Yuan, Z., Fang, F., Cheng, X., Xia, J., Fang, M., Xu, Y. and Gao, Y. (2013). Megakaryocytic leukemia 1 (MKL1) ties the epigenetic machinery to hypoxia-induced transactivation of endothelin-1. Nucleic Acids Res. 41, 6005-6017.
50. Zaki, M. H., Vogel, P., Malireddi, R. K., Body-Malapel, M., Anand, P. K., Bertin, J., Green, D. R., Lamkanfi, M. and Kanneganti, T. D. (2011). The NOD-like receptor NLRP12 attenuates colon inflammation and tumorigenesis. Cancer Cell 20, 649-660.
51. Zhang, M., Fang, H., Zhou, J. and Herring, B. P. (2007). A novel role of Brg1 in the regulation of SRF/MRTFA-dependent smooth muscle-specific gene expression. J. Biol. Chem. 282, 25708-25716.
52. Zhou, J., Zhang, M., Fang, H., El-Mounayri, O., Rodenberg, J. M., Imbalzano, A. N. and Herring, B. P. (2009). The SWI/SNF chromatin remodeling complex regulates myocardin-induced smooth muscle-specific gene expression. Arterioscler. Thromb. Vasc. Biol. 29, 921-928.
53. Zhou, Y., Huang, X., Hecker, L., Kurundkar, D., Kurundkar, A., Liu, H., Jin, T. H., Desai, L., Bernard, K. and Thannickal, V. J. (2013). Inhibition of mechanosensitive signaling in myofibroblasts ameliorates experimental pulmonary fibrosis. J. Clin. Invest. 123, 1096-1108.