Prostaglandin e2 inhibits α-smooth muscle actin transcription during myofibroblast differentiation via distinct mechanisms of modulation of serum response factor and myocardin-related transcription factor-A

Journal of Biological Chemistry

Volumn 289, Issue 24, 2014, Pages 17151-17162

  Penke, Loka R K ^a   Huang, Steven K ^a   White, Eric S ^a   Peters Golden, Marc ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL ORGANS; BODY FLUIDS; CELL CULTURE; CHEMICAL ACTIVATION; FIBROBLASTS; LIPIDS; MUSCLE; TRANSCRIPTION;

IDIOPATHIC PULMONARY FIBROSIS; LUNG FIBROBLASTS; NUCLEAR ACCUMULATION; PULMONARY FIBROSIS; SERUM-RESPONSE FACTORS; SMOOTH MUSCLE ACTINS; TRANSFORMING GROWTH FACTORS; VASODILATOR-STIMULATED PHOSPHOPROTEINS;

TRANSCRIPTION FACTORS;

ALPHA SMOOTH MUSCLE ACTIN; COFILIN 1; MITOGEN ACTIVATED PROTEIN KINASE P38; MYOCARDIN RELATED TRANSCRIPTION FACTOR A; PROSTAGLANDIN E2; SERUM RESPONSE FACTOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; VASODILATOR STIMULATED PHOSPHOPROTEIN; ACTA2 PROTEIN, HUMAN; ACTIN; ACTIN BINDING PROTEIN; CELL ADHESION MOLECULE; DNA BINDING PROTEIN; MKL1 PROTEIN, HUMAN; ONCOPROTEIN; PHOSPHOPROTEIN; PROSTAGLANDIN; TRANSFORMING GROWTH FACTOR BETA;

ADULT; ARTICLE; CELL DIFFERENTIATION; CELL NUCLEUS; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME INHIBITION; FIBROSING ALVEOLITIS; GENE ACTIVATION; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; INHIBITION KINETICS; LUNG FIBROBLAST; MITOSIS INHIBITION; MYOFIBROBLAST; NUCLEAR IMPORT; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TRANSCRIPTION TERMINATION; CELL LINE; CYTOLOGY; DIFFERENTIATION; DRUG EFFECT; GENETIC TRANSCRIPTION; GENETICS; LUNG; METABOLISM; TRANSCRIPTION REGULATION; TRANSFORMING GROWTH FACTOR-{BETA} (TGF-{BETA}); VASODILATOR-STIMULATED PHOSPHOPROTEIN;

DIFFERENTIATION; MYOFIBROBLAST; PROSTAGLANDIN; TRANSCRIPTION REGULATION; TRANSFORMING GROWTH FACTOR-{BETA} (TGF-{BETA});

ACTINS; CELL ADHESION MOLECULES; CELL DIFFERENTIATION; CELL LINE; COFILIN 1; DINOPROSTONE; DNA-BINDING PROTEINS; HUMANS; LUNG; MICROFILAMENT PROTEINS; MYOFIBROBLASTS; ONCOGENE PROTEINS, FUSION; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHOPROTEINS; SERUM RESPONSE FACTOR; TRANSCRIPTION, GENETIC; TRANSFORMING GROWTH FACTOR BETA;

EID: 84902455478     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.558130     Document Type: Article

References (51)

1. American Thoracic Society and European Respiratory Society (2002) American Thoracic Society/European Respiratory Society International Multidisciplinary Consensus Classification of the Idiopathic Interstitial Pneumonias. This joint statement of the American Thoracic Society (ATS), and the European Respiratory Society (ERS) was adopted by the ATS board of directors, June 2001 and by the ERS Executive Committee, June 2001. Am. J. Respir. Crit. Care Med. 165, 277-304
2. Fernandez, I. E., and Eickelberg, O. (2012) New cellular and molecular mechanisms of lung injury and fibrosis in idiopathic pulmonary fibrosis. Lancet 380, 680-688
3. Todd, N. W., Luzina, I. G., and Atamas, S. P. (2012) Molecular and cellular mechanisms of pulmonary fibrosis. Fibrogenesis Tissue Repair 5, 11
4. Tomasek, J. J., Gabbiani, G., Hinz, B., Chaponnier, C., and Brown, R. A. (2002) Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat. Rev. Mol. Cell Biol. 3, 349-363 (Pubitemid 34619269)
5. Desmoulière, A., Badid, C., Bochaton-Piallat, M. L., and Gabbiani, G. (1997) Apoptosis during wound healing, fibrocontractive diseases, and vascular wall injury. Int. J. Biochem. Cell Biol. 29, 19-30 (Pubitemid 27096416)
6. 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
7. Klingberg, F., Hinz, B., and White, E. S. (2013) The myofibroblast matrix: implications for tissue repair and fibrosis. J. Pathol. 229, 298-309
8. Marinković, A., Liu, F., and Tschumperlin, D. J. (2013) Matrices of physiologic stiffness potently inactivate idiopathic pulmonary fibrosis fibroblasts. Am. J. Respir. Cell Mol. Biol. 48, 422-430
9. Wipff, P. J., Rifkin, D. B., Meister, J. J., and Hinz, B. (2007) Myofibroblast contraction activates latent TGF-β1 from the extracellular matrix. J. Cell Biol. 179, 1311-1323 (Pubitemid 350277747)
10. Leask, A., and Abraham, D. J. (2004) TGF-β signaling and the fibrotic response. FASEB J. 18, 816-827
11. Kim, S., Ip, H. S., Lu, M. M., Clendenin, C., and Parmacek, M. S. (1997) A serum response factor-dependent transcriptional regulatory program identifies distinct smooth muscle cell sublineages. Mol. Cell. Biol. 17, 2266-2278 (Pubitemid 27133314)
12. Du, K. L., Chen, M., Li, J., Lepore, J. J., Mericko, P., and Parmacek, M. S. (2004) Megakaryoblastic leukemia factor-1 transduces cytoskeletal signals and induces smooth muscle cell differentiation from undifferentiated embryonic stem cells. J. Biol. Chem. 279, 17578-17586 (Pubitemid 38560522)
13. Mack, C. P., and Owens, G. K. (1999) Regulation of smooth muscle α-actin expression in vivo is dependent on CArG elements within the 5′ and first intron promoter regions. Circ. Res. 84, 852-861 (Pubitemid 29181493)
14. Miralles, F., Posern, G., Zaromytidou, A. I., and Treisman, R. (2003) Actin dynamics control SRF activity by regulation of its coactivator MAL. Cell 113, 329-342 (Pubitemid 36556115)
15. Posern, G., and Treisman, R. (2006) Actin' together: serum response factor, its cofactors and the link to signal transduction. Trends Cell Biol. 16, 588-596 (Pubitemid 44636222)
16. Parmacek, M. S. (2007) Myocardin-related transcription factors: critical coactivators regulating cardiovascular development and adaptation. Circ. Res. 100, 633-644
17. Huang, S. K., and Peters-Golden, M. (2008) Eicosanoid lipid mediators in fibrotic lung diseases: ready for prime time? Chest 133, 1442-1450 (Pubitemid 351899641)
18. Thomas, P. E., Peters-Golden, M., White, E. S., Thannickal, V. J., and Moore, B. B. (2007) PGE(2) inhibition of TGF-β1-induced myofibroblast differentiation is Smad-independent but involves cell shape and adhesion-dependent signaling. Am. J. Physiol. Lung Cell. Mol. Physiol. 293, L417-428 (Pubitemid 47205022)
19. 2-mediated fibroblast responses via regulation of E prostanoid 2 receptor expression. J. Biol. Chem. 284, 32264-32271
20. Garrison, G., Huang, S. K., Okunishi, K., Scott, J. P., Kumar Penke, L. R., Scruggs, A. M., and Peters-Golden, M. (2013) Reversal of myofibroblast differentiation by prostaglandin E(2). Am. J. Respir. Cell Mol. Biol. 48, 550-558
21. Huang, S. K., Wettlaufer, S. H., Hogaboam, C. M., Flaherty, K. R., Martinez, F. J., Myers, J. L., Colby, T. V., Travis, W. D., Toews, G. B., and Peters-Golden, M. (2008) Variable prostaglandin E2 resistance in fibroblasts from patients with usual interstitial pneumonia. Am. J. Respir. Crit. Care Med. 177, 66-74
22. Okunishi, K., Sisson, T. H., Huang, S. K., Hogaboam, C. M., Simon, R. H., and Peters-Golden, M. (2011) Plasmin overcomes resistance to prostaglandin E2 in fibrotic lung fibroblasts by reorganizing protein kinase A signaling. J. Biol. Chem. 286, 32231-32243
23. Fernau, N. S., Fugmann, D., Leyendecker, M., Reimann, K., Grether-Beck, S., Galban, S., Ale-Agha, N., Krutmann, J., and Klotz, L. O. (2010) Role of HuR and p38MAPK in ultraviolet B-induced post-transcriptional regulation of COX-2 expression in the human keratinocyte cell line HaCaT. J. Biol. Chem. 285, 3896-3904
24. Hutter, D., Chen, P., Barnes, J., and Liu, Y. (2000) Catalytic activation of mitogen-activated protein (MAP) kinase phosphatase-1 by binding to p38 MAPK: critical role of the p38 C-terminal domain in its negative regulation. Biochem. J. 352, 155-163
25. Meyer-Ter-Vehn, T., Gebhardt, S., Sebald, W., Buttmann, M., Grehn, F., Schlunck, G., and Knaus, P. (2006) p38 inhibitors prevent TGF-β-induced myofibroblast transdifferentiation in human tenon fibroblasts. Invest. Ophthalmol. Vis. Sci. 47, 1500-1509 (Pubitemid 46780758)
26. Hautmann, M. B., Adam, P. J., and Owens, G. K. (1999) Similarities and differences in smooth muscle α-actin induction by TGF-β in smooth muscle versus non-smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 19, 2049-2058 (Pubitemid 29422235)
27. Elberg, G., Chen, L., Elberg, D., Chan, M. D., Logan, C. J., and Turman, M. A. (2008) MKL1 mediates TGF-β1-induced α-smooth muscle actin expression in human renal epithelial cells. Am. J. Physiol. Renal Physiol. 294, F1116-F1128
28. Sandbo, N., Kregel, S., Taurin, S., Bhorade, S., and Dulin, N. O. (2009) Critical role of serum response factor in pulmonary myofibroblast differentiation induced by TGF-β. Am. J. Respir. Cell Mol. Biol. 41, 332-338
29. Kolodsick, J. E., Peters-Golden, M., Larios, J., Toews, G. B., Thannickal, V. J., and Moore, B. B. (2003) Prostaglandin E2 inhibits fibroblast to myofibroblast transition via E. prostanoid receptor 2 signaling and cyclic adenosine monophosphate elevation. Am. J. Respir. Cell Mol. Biol. 29, 537-544 (Pubitemid 37357704)
30. Meyer-ter-Vehn, T., Sieprath, S., Katzenberger, B., Gebhardt, S., Grehn, F., and Schlunck, G. (2006) Contractility as a prerequisite for TGF-β-induced myofibroblast transdifferentiation in human tenon fibroblasts. Invest. Ophthalmol. Vis. Sci. 47, 4895-4904 (Pubitemid 46586390)
31. Deaton, R. A., Su, C., Valencia, T. G., and Grant, S. R. (2005) Transforming growth factor-β1-induced expression of smooth muscle marker genes involves activation of PKN and p38 MAPK. J. Biol. Chem. 280, 31172-31181 (Pubitemid 41291854)
32. 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-β1-induced fibroblast to myofibroblast differentiation. J. Invest. Dermatol. 131, 2378-2385
33. Sotiropoulos, A., Gineitis, D., Copeland, J., and Treisman, R. (1999) Signal-regulated activation of serum response factor is mediated by changes in actin dynamics. Cell 98, 159-169 (Pubitemid 29344904)
34. Sandbo, N., Lau, A., Kach, J., Ngam, C., Yau, D., and Dulin, N. O. (2011) Delayed stress fiber formation mediates pulmonary myofibroblast differentiation in response to TGF-β. Am. J. Physiol. Lung Cell. Mol. Physiol. 301, L656-666
35. Cao, W., Daniel, K. W., Robidoux, J., Puigserver, P., Medvedev, A. V., Bai, X., Floering, L. M., Spiegelman, B. M., and Collins, S. (2004) p38 mitogen-activated protein kinase is the central regulator of cyclic AMP-dependent transcription of the brown fat uncoupling protein 1 gene. Mol. Cell. Biol. 24, 3057-3067 (Pubitemid 38381292)
36. Choi, S. C., Kim, B. S., Song, M. Y., Choi, E. Y., Oh, H. M., Lyou, J. H., Han, W. C., Moon, H. B., Kim, T. H., Oh, J. M., Chung, H. T., and Jun, C. D. (2003) Downregulation of p38 kinase pathway by cAMP response element-binding protein protects HL-60 cells from iron chelator-induced apoptosis. Free Radic. Biol. Med. 35, 1171-1184
37. Robidoux, J., Cao, W., Quan, H., Daniel, K. W., Moukdar, F., Bai, X., Floering, L. M., and Collins, S. (2005) Selective activation of mitogen-activated protein (MAP) kinase kinase 3 and p38α MAPKis essential for cyclic AMP-dependent UCP1 expression in adipocytes. Mol. Cell. Biol. 25, 5466-5479 (Pubitemid 40853582)
38. Zhang, J., Bui, T. N., Xiang, J., and Lin, A. (2006) Cyclic AMP inhibits p38 activation via CREB-induced dynein light chain. Mol. Cell. Biol. 26, 1223-1234 (Pubitemid 43202551)
39. Yang, Y., Zhe, X., Phan, S. H., Ullenbruch, M., and Schuger, L. (2003) Involvement of serum response factor isoforms in myofibroblast differentiation during bleomycin-induced lung injury. Am. J. Respir. Cell Mol. Biol. 29, 583-590 (Pubitemid 37357709)
40. Huang, S. K., Fisher, A. S., Scruggs, A. M., White, E. S., Hogaboam, C. M., Richardson, B. C., and Peters-Golden, M. (2010) Hypermethylation of PTGER2 confers prostaglandin E2 resistance in fibrotic fibroblasts from humans and mice. Am. J. Pathol. 177, 2245-2255
41. Thannickal, V. J., Lee, D. Y., White, E. S., Cui, Z., Larios, J. M., Chacon, R., Horowitz, J. C., Day, R. M., and Thomas, P. E. (2003) Myofibroblast differentiation by transforming growth factor-β1 is dependent on cell adhesion and integrin signaling via focal adhesion kinase. J. Biol. Chem. 278, 12384-12389 (Pubitemid 36800223)
42. Serezani, C. H., Kane, S., Medeiros, A. I., Cornett, A. M., Kim, S. H., Marques, M. M., Lee, S. P., Lewis, C., Bourdonnay, E., Ballinger, M. N., White, E. S., and Peters-Golden, M. (2012) PTEN directly activates the actin depolymerization factor cofilin-1 during PGE2-mediated inhibition of phagocytosis of fungi. Sci. Signal. 5, ra12
43. White, E. S., Atrasz, R. G., Dickie, E. G., Aronoff, D. M., Stambolic, V., Mak, T. W., Moore, B. B., and Peters-Golden, M. (2005) Prostaglandin E(2) inhibits fibroblast migration by E-prostanoid 2 receptor-mediated increase in PTEN activity. Am. J. Respir. Cell Mol. Biol. 32, 135-141 (Pubitemid 40189695)
44. Maher, T. M., Evans, I. C., Bottoms, S. E., Mercer, P. F., Thorley, A. J., Nicholson, A. G., Laurent, G. J., Tetley, T. D., Chambers, R. C., and McAnulty, R. J. (2010) Diminished prostaglandin E2 contributes to the apoptosis paradox in idiopathic pulmonary fibrosis. Am. J. Respir. Crit. Care Med. 182, 73-82
45. Wilborn, J., Crofford, L. J., Burdick, M. D., Kunkel, S. L., Strieter, R. M., and Peters-Golden, M. (1995) Cultured lung fibroblasts isolated from patients with idiopathic pulmonary fibrosis have a diminished capacity to synthesize prostaglandin E2 and to express cyclooxygenase-2. J. Clin. Invest. 95, 1861-1868
46. Stumm, C. L., Wettlaufer, S. H., Jancar, S., and Peters-Golden, M. (2011) Airway remodeling in murine asthma correlates with a defect in PGE2 synthesis by lung fibroblasts. Am. J. Physiol. Lung Cell. Mol. Physiol. 301, L636-644
47. Walker, N. M., Badri, L. N., Wadhwa, A., Wettlaufer, S., Peters-Golden, M., and Lama, V. N. (2012) Prostaglandin E2 as an inhibitory modulator of fibrogenesis in human lung allografts. Am. J. Respir. Crit. Care Med. 185, 77-84
48. Liu, F., Mih, J. D., Shea, B. S., Kho, A. T., Sharif, A. S., Tager, A. M., and Tschumperlin, D. J. (2010) Feedback amplification of fibrosis through matrix stiffening and COX-2 suppression. J. Cell Biol. 190, 693-706
49. Moore, B. B., Coffey, M. J., Christensen, P., Sitterding, S., Ngan, R., Wilke, C. A., McDonald, R., Phare, S. M., Peters-Golden, M., Paine, R., 3rd, and Toews, G. B. (2000) GM-CSF regulates bleomycin-induced pulmonary fibrosis via a prostaglandin-dependent mechanism. J. Immunol. 165, 4032-4039 (Pubitemid 32057315)
50. Moore, B. B., Ballinger, M. N., White, E. S., Green, M. E., Herrygers, A. B., Wilke, C. A., Toews, G. B., and Peters-Golden, M. (2005) Bleomycin-induced E prostanoid receptor changes alter fibroblast responses to prostaglandin E2. J. Immunol. 174, 5644-5649 (Pubitemid 40593205)
51. Nakagawa, N., Yuhki, K., Kawabe, J., Fujino, T., Takahata, O., Kabara, M., Abe, K., Kojima, F., Kashiwagi, H., Hasebe, N., Kikuchi, K., Sugimoto, Y., Narumiya, S., and Ushikubi, F. (2012) The intrinsic prostaglandin E2-EP4 system of the renal tubular epithelium limits the development of tubulointerstitial fibrosis in mice. Kidney Int. 82, 158-171