Bone morphogenetic protein signaling in vascular disease: Anti-inflammatory action through myocardin-related transcription factor A

Journal of Biological Chemistry

Volumn 287, Issue 33, 2012, Pages 28067-28077

  Wang, Dahai ^a   Prakash, Jamunabai ^a   Nguyen, Peter ^a   Davis Dusenbery, Brandi N ^a   Hill, Nicholas S ^a   Layne, Matthew D ^b   Hata, Akiko ^a   Lagna, Giorgio ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BOSTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION DOMAIN; ANTI-INFLAMMATORY ACTION; ANTI-INFLAMMATORY EFFECTS; BONE MORPHOGENETIC PROTEINS; CYTOKINES; ELEVATED LEVEL; INFLAMMATORY CELLS; INFLAMMATORY CYTOKINES; INFLAMMATORY MEDIATORS; INFLAMMATORY RESPONSE; NUCLEAR LOCALIZATION; OVER-EXPRESSION; PULMONARY ARTERY; PULMONARY ARTERY SMOOTH MUSCLE CELLS; THERAPEUTIC INTERVENTION; TYPE II; VASCULAR DISEASE;

GENE ENCODING; TRANSCRIPTION; TRANSCRIPTION FACTORS; WELL STIMULATION;

SIGNALING;

ALPHA SMOOTH MUSCLE ACTIN; BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN RECEPTOR 2; CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; EOTAXIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 2; MYOCARDIN; MYOCARDIN RELATED TRANSCRIPTION FACTOR A; SMAD6 PROTEIN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL DEDIFFERENTIATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE EXPRESSION; HUMAN; HUMAN CELL; INFLAMMATION; MICROARRAY ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PULMONARY HYPERTENSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; TRANSCRIPTION INITIATION; TRANSCRIPTION INITIATION SITE; VASCULAR DISEASE;

BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE II; CELLS, CULTURED; DNA-BINDING PROTEINS; HUMANS; HYPERTENSION, PULMONARY; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; ONCOGENE PROTEINS, FUSION; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84864994800     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.379487     Document Type: Article

References (44)

1. Toshner, M., Tajsic, T., and Morrell, N. W. (2010) Pulmonary hypertension: advances in pathogenesis and treatment. Br. Med. Bullet. 94, 21-32
2. Machado, R. D., Eickelberg, O., Elliott, C. G., Geraci, M. W., Hanaoka, M., Loyd, J. E., Newman, J. H., Phillips, J. A., 3rd, Soubrier, F., Trembath, R. C., and Chung, W. K. (2009) Genetics and genomics of pulmonary arterial hypertension. J. Am. Coll. Cardiol. 54, S32-S42
3. Eickelberg, O., and Morty, R. E. (2007) Transforming growth factor β/bone morphogenic protein signaling in pulmonary arterial hypertension: remodeling revisited. Trends Cardiovasc. Med. 17, 263-269
4. Pullamsetti, S. S., Savai, R., Janssen, W., Dahal, B. K., Seeger, W., Grimminger, F., Ghofrani, H. A., Weissmann, N., and Schermuly, R. T. (2011) Inflammation, immunological reaction and role of infection in pulmonary hypertension. Clin. Microbiol. Infect 17, 7-14
5. Machado, R. D., Aldred, M. A., James, V., Harrison, R. E., Patel, B., Schwalbe, E. C., Gruenig, E., Janssen, B., Koehler, R., Seeger, W., Eickelberg, O., Olschewski, H., Elliott, C. G., Glissmeyer, E., Carlquist, J., Kim, M., Torbicki, A., Fijalkowska, A., Szewczyk, G., Parma, J., Abramowicz, M. J., Galie, N., Morisaki, H., Kyotani, S., Nakanishi, N., Morisaki, T., Humbert, M., Simonneau, G., Sitbon, O., Soubrier, F., Coulet, F., Morrell, N. W., and Trembath, R. C. (2006) Mutations of the TGF-β type II receptor BMPR2 in pulmonary arterial hypertension. Hum. Mutat. 27, 121-132
6. Thomson, J. R., Machado, R. D., Pauciulo, M. W., Morgan, N. V., Humbert, M., Elliott, G. C., Ward, K., Yacoub, M., Mikhail, G., Rogers, P., Newman, J., Wheeler, L., Higenbottam, T., Gibbs, J. S., Egan, J., Crozier, A., Peacock, A., Allcock, R., Corris, P., Loyd, J. E., Trembath, R. C., and Nichols, W. C. (2000) Sporadic primary pulmonary hypertension is associated with germline mutations of the gene encoding BMPR-II, a receptor member of the TGF-β family. J. Med. Genet. 37, 741-745
7. Atkinson, C., Stewart, S., Upton, P. D., Machado, R., Thomson, J. R., Trembath, R. C., and Morrell, N. W. (2002) Primary pulmonary hypertension is associated with reduced pulmonary vascular expression of type II bone morphogenetic protein receptor. Circulation 105, 1672-1678
8. Yang, X., Long, L., Southwood, M., Rudarakanchana, N., Upton, P. D., Jeffery, T. K., Atkinson, C., Chen, H., Trembath, R. C., and Morrell, N. W. (2005) Dysfunctional Smad signaling contributes to abnormal smooth muscle cell proliferation in familial pulmonary arterial hypertension. Circ. Res. 96, 1053-1063
9. Hruska, K. A., Mathew, S., and Saab, G. (2005) Bone morphogenetic proteins in vascular calcification. Circ. Res. 97, 105-114
10. Burton, D. G., Matsubara, H., and Ikeda, K. (2010) Pathophysiology of vascular calcification: Pivotal role of cellular senescence in vascular smooth muscle cells. Exp. Gerontol. 45, 819-824
11. Lagna, G., Ku, M. M., Nguyen, P. H., Neuman, N. A., Davis, B. N., and Hata, A. (2007) Control of phenotypic plasticity of smooth muscle cells by bone morphogenetic protein signaling through the myocardin-related transcription factors. J. Biol. Chem. 282, 37244-37255
12. Nicolls, M. R., Taraseviciene-Stewart, L., Rai, P. R., Badesch, D. B., and Voelkel, N. F. (2005) Autoimmunity and pulmonary hypertension: a perspective. Eur. Respir. J. 26, 1110-1118
13. Humbert, M., Monti, G., Brenot, F., Sitbon, O., Portier, A., Grangeot-Keros, L., Duroux, P., Galanaud, P., Simonneau, G., and Emilie, D. (1995) Increased interleukin-1 and interleukin-6 serum concentrations in severe primary pulmonary hypertension. Am. J. Respir. Crit. Care Med. 151, 1628-1631
14. Fartoukh, M., Emilie, D., Le Gall, C., Monti, G., Simonneau, G., and Humbert, M. (1998) Chemokine macrophage inflammatory protein-1alpha mRNA expression in lung biopsy specimens of primary pulmonary hypertension. Chest 114, 50S-51S
15. Sanchez, O., Marcos, E., Perros, F., Fadel, E., Tu, L., Humbert, M., Dartevelle, P., Simonneau, G., Adnot, S., and Eddahibi, S. (2007) Role of endothelium-derived CC chemokine ligand 2 in idiopathic pulmonary arterial hypertension. Am. J. Respir. Crit. Care Med. 176, 1041-1047
16. Soon, E., Holmes, A. M., Treacy, C. M., Doughty, N. J., Southgate, L., Machado, R. D., Trembath, R. C., Jennings, S., Barker, L., Nicklin, P., Walker, C., Budd, D. C., Pepke-Zaba, J., and Morrell, N. W. (2010) Elevated levels of inflammatory cytokines predict survival in idiopathic and familial pulmonary arterial hypertension. Circulation 122, 920-927
17. Taraseviciene-Stewart, L., Nicolls, M. R., Kraskauskas, D., Scerbavicius, R., Burns, N., Cool, C., Wood, K., Parr, J. E., Boackle, S. A., and Voelkel, N. F. (2007) Absence of T cells confers increased pulmonary arterial hypertension and vascular remodeling. Am. J. Respir. Crit. Care Med. 175, 1280-1289
18. Daley, E., Emson, C., Guignabert, C., de Waal Malefyt, R., Louten, J., Kurup, V. P., Hogaboam, C., Taraseviciene-Stewart, L., Voelkel, N. F., Rabinovitch, M., Grunig, E., and Grunig, G. (2008) Pulmonary arterial remodeling induced by a Th2 immune response. J. Exp. Med. 205, 361-372
19. Steiner, M. K., Syrkina, O. L., Kolliputi, N., Mark, E. J., Hales, C. A., and Waxman, A. B. (2009) Interleukin-6 overexpression induces pulmonary hypertension. Circ. Res. 104, 236-244
20. Fujita, M., Mason, R. J., Cool, C., Shannon, J. M., Hara, N., and Fagan, K. A. (2002) Pulmonary hypertension in TNF-α-overexpressing mice is associated with decreased VEGF gene expression. J. Appl. Physiol. 93, 2162-2170
21. Hagen, M., Fagan, K., Steudel, W., Carr, M., Lane, K., Rodman, D. M., and West, J. (2007) Interaction of interleukin-6 and the BMP pathway in pulmonary smooth muscle. Am. J. Physiol. Lung Cell Mol. Physiol. 292, L1473-L1479
22. West, J. (2010) Cross talk between Smad, MAPK, and actin in the etiology of pulmonary arterial hypertension. Adv. Exp. Med. Biol. 661, 265-278
23. Song, Y., Coleman, L., Shi, J., Beppu, H., Sato, K., Walsh, K., Loscalzo, J., and Zhang, Y. Y. (2008) Inflammation, endothelial injury, and persistent pulmonary hypertension in heterozygous BMPR2-mutant mice. Am. J. Physiol. 295, H677-H690
24. 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
25. Hata, A., Seoane, J., Lagna, G., Montalvo, E., Hemmati-Brivanlou, A., and Massagué, J. (2000) OAZ uses distinct DNA- and protein-binding zinc fingers in separate BMP-Smad and Olf signaling pathways. Cell 100, 229-240
26. Preston, I. R., Hill, N. S., Warburton, R. R., and Fanburg, B. L. (2006) Role of 12-lipoxygenase in hypoxia-induced rat pulmonary artery smooth muscle cell proliferation. Am. J. Physiol. Lung Cell Mol. Physiol. 290, L367-L374
27. Chan, M. C., Hilyard, A. C., Wu, C., Davis, B. N., Hill, N. S., Lal, A., Lieberman, J., Lagna, G., and Hata, A. (2010) Molecular basis for antagonism between PDGF and the TGFβ family of signaling pathways by control of miR-24 expression. EMBO J. 29, 559-573
28. Sprague, A. H., and Khalil, R. A. (2009) Inflammatory cytokines in vascular dysfunction and vascular disease. Biochem. Pharmacol. 78, 539-552
29. Gupta, V., Yeo, G., Kawakubo, H., Rangnekar, V., Ramaswamy, P., Hayashida, T., MacLaughlin, D. T., Donahoe, P. K., and Maheswaran, S. (2007) Mullerian-inhibiting substance induces Gro-β expression in breast cancer cells through a nuclear factor-κB-dependent and Smad1-dependent mechanism. Cancer Res. 67, 2747-2756
30. Karin, M. (1999) How NF-κB is activated: the role of the IκB kinase (IKK) complex. Oncogene 18, 6867-6874
31. Beg, A. A., Ruben, S. M., Scheinman, R. I., Haskill, S., Rosen, C. A., and Baldwin, A. S., Jr. (1992) IκB interacts with the nuclear localization sequences of the subunits of NF-κB: a mechanism for cytoplasmic retention. Genes Dev. 6, 1899-1913
32. Zabel, U., Henkel, T., Silva, M. S., and Baeuerle, P. A. (1993) Nuclear uptake control of NF-κB by MAD-3, an IκB protein present in the nucleus. EMBO J. 12, 201-211
33. Agrawal, A., Cha-Molstad, H., Samols, D., and Kushner, I. (2003) Overexpressed nuclear factor-κB can participate in endogenous C-reactive protein induction, and enhances the effects of C/EBPβ and signal transducer and activator of transcription-3. Immunology 108, 539-547
34. Zhang, Y., Saccani, S., Shin, H., and Nikolajczyk, B. S. (2008) Dynamic protein associations define two phases of IL-1β transcriptional activation. J. Immunol. 181, 503-512
35. 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. U.S.A. 99, 14855-14860
36. Simic, P., and Vukicevic, S. (2005) Bone morphogenetic proteins in development and homeostasis of kidney. Cytokine Growth Factor Rev. 16, 299-308
37. Dendooven, A., van Oostrom, O., van der Giezen, D. M., Leeuwis, J. W., Snijckers, C., Joles, J. A., Robertson, E. J., Verhaar, M. C., Nguyen, T. Q., and Goldschmeding, R. (2011) Loss of endogenous bone morphogenetic protein-6 aggravates renal fibrosis. Am. J. Pathol. 178, 1069-1079
38. Yao, Y., Bennett, B. J., Wang, X., Rosenfeld, M. E., Giachelli, C., Lusis, A. J., and Boström, K. I. (2010) Inhibition of bone morphogenetic proteins protects against atherosclerosis and vascular calcification. Circulation Research 107, 485-494
39. Tang, R. H., Zheng, X. L., Callis, T. E., Stansfield, W. E., He, J., Baldwin, A. S., Wang, D. Z., and Selzman, C. H. (2008) Myocardin inhibits cellular proliferation by inhibiting NF-κB(p65)-dependent cell cycle progression. Proc. Natl. Acad. Sci. U.S.A. 105, 3362-3367
40. Davis-Dusenbery, B. N., Chan, M. C., Reno, K. E., Weisman, A. S., Layne, M. D., Lagna, G., and Hata, A. (2011) Down-regulation of Kruppel-like factor-4 (KLF4) by microRNA-143/145 is critical for modulation of vascular smooth muscle cell phenotype by transforming growth factor-beta and bone morphogenetic protein 4. J. Biol. Chem. 286, 28097-28110
41. Yu, Y., Sweeney, M., Zhang, S., Platoshyn, O., Landsberg, J., Rothman, A., and Yuan, J. X. (2003) PDGF stimulates pulmonary vascular smooth muscle cell proliferation by upregulating TRPC6 expression. Am. J. Physiol. Cell Physiol. 284, C316-C330
42. Yu, Y., Keller, S. H., Remillard, C. V., Safrina, O., Nicholson, A., Zhang, S. L., Jiang, W., Vangala, N., Landsberg, J. W., Wang, J. Y., Thistlethwaite, P. A., Channick, R. N., Robbins, I. M., Loyd, J. E., Ghofrani, H. A., Grimminger, F., Schermuly, R. T., Cahalan, M. D., Rubin, L. J., and Yuan, J. X. (2009) A functional single-nucleotide polymorphism in the TRPC6 gene promoter associated with idiopathic pulmonary arterial hypertension. Circulation 119, 2313-2322
43. Sawada, H., Mitani, Y., Maruyama, J., Jiang, B. H., Ikeyama, Y., Dida, F. A., Yamamoto, H., Imanaka-Yoshida, K., Shimpo, H., Mizoguchi, A., Maruyama, K., and Komada, Y. (2007) A nuclear factor-κB inhibitor pyrrolidine dithiocarbamate ameliorates pulmonary hypertension in rats. Chest 132, 1265-1274
44. Yu, P. B., Beppu, H., Kawai, N., Li, E., and Bloch, K. D. (2005) Bone morphogenetic protein (BMP) type II receptor deletion reveals BMP ligand-specific gain of signaling in pulmonary artery smooth muscle cells. J. Biol. Chem. 280, 24443-24450