LPA1-induced cytoskeleton reorganization drives fibrosis through CTGF-dependent fibroblast proliferation

FASEB Journal

Volumn 27, Issue 5, 2013, Pages 1830-1846

  Sakai, Norihiko ^a   Chun, Jerold ^b   Duffield, Jeremy S ^c,d   Wada, Takashi ^e   Luster, Andrew D ^a   Tager, Andrew M ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

^e KANAZAWA UNIVERSITY   (Japan)

Author keywords

Lysophosphatidic acid; Myocardin related transcription factor B; Myocardinrelated transcription factor A; Rho GTPases; Serum response factor

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; COLLAGEN TYPE 1; CONNECTIVE TISSUE GROWTH FACTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; LYSOPHOSPHATIDIC ACID; LYSOPHOSPHATIDIC ACID 1; MYOCARDIN; MYOCARDIN RELATED TRANSCRIPTION FACTOR A; MYOCARDIN RELATED TRANSCRIPTION FACTOR B; PROTEIN; RAC PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; ROCK PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ACTIN POLYMERIZATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOSKELETON; ENZYME ACTIVATION; FIBROBLAST; IN VIVO STUDY; MESOTHELIUM CELL; MOUSE; MYOFIBROBLAST; NONHUMAN; PARACRINE SIGNALING; PERITONEAL DIALYSIS; PERITONEAL FIBROSIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; STRESS FIBER;

ANILIDES; ANIMALS; BENZAMIDES; BIPHENYL COMPOUNDS; CELL PROLIFERATION; CHLORHEXIDINE; CONNECTIVE TISSUE GROWTH FACTOR; CYTOSKELETON; DISEASE MODELS, ANIMAL; EPITHELIAL CELLS; EPITHELIUM; ISOXAZOLES; LYSOPHOSPHOLIPIDS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOFIBROBLASTS; PERITONEAL FIBROSIS; RECEPTORS, LYSOPHOSPHATIDIC ACID; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS;

ANIMALIA; MUS;

EID: 84877102431     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-219378     Document Type: Article

References (53)

1. Selman, M., King, T. E., and Pardo, A. (2001) Idiopathic pulmonary fibrosis: prevailing and evolving hypotheses about its pathogenesis and implications for therapy. Ann. Intern. Med. 134, 136-151
2. Scotton, C. J., and Chambers, R. C. (2007) Molecular targets in pulmonary fibrosis: the myofibroblast in focus. Chest 132, 1311-1321
3. Choi, J. W., Herr, D. R., Noguchi, K., Yung, Y. C., Lee, C. W., Mutoh, T., Lin, M. E., Teo, S. T., Park, K. E., Mosley, A. N., and Chun, J. (2010) LPA receptors: subtypes and biological actions. Annu. Rev. Pharmacol. Toxicol. 50, 157-186
4. Tager, A. M., LaCamera, P., Shea, B. S., Campanella, G. S., Selman, M., Zhao, Z., Polosukhin, V., Wain, J., Karimi-Shah, B. A., Kim, N. D., Hart, W. K., Pardo, A., Blackwell, T. S., Xu, Y., Chun, J., and Luster, A. D. (2008) The lysophosphatidic acid receptor LPA1 links pulmonary fibrosis to lung injury by mediating fibroblast recruitment and vascular leak. Nat. Med. 14, 45-54
5. Castelino, F. V., Seiders, J., Bain, G., Brooks, S. F., King, C. D., Swaney, J. S., Lorrain, D. S., Chun, J., Luster, A. D., and Tager, A. M. (2011) Amelioration of dermal fibrosis by genetic deletion or pharmacologic antagonism of lysophosphatidic acid receptor 1 in a mouse model of scleroderma. Arthritis Rheum. 63, 1405-1415
6. Pradere, J. P., Klein, J., Gres, S., Guigne, C., Neau, E., Valet, P., Calise, D., Chun, J., Bascands, J. L., Saulnier-Blache, J. S., and Schanstra, J. P. (2007) LPA1 receptor activation promotes renal interstitial fibrosis. J. Am. Soc. Nephrol. 18, 3110-3118
7. Martin, P. (1997) Wound healing: aiming for perfect skin regeneration. Science 276, 75-81
8. Hoyles, R. K., Derrett-Smith, E. C., Khan, K., Shiwen, X., Howat, S. L., Wells, A. U., Abraham, D. J., and Denton, C. P. (2011) An essential role for resident fibroblasts in experimental lung fibrosis is defined by lineage-specific deletion of high-affinity type II transforming growth factor beta receptor. Am. J. Respir. Crit. Care Med. 183, 249-261
9. Yoshio, Y., Miyazaki, M., Abe, K., Nishino, T., Furusu, A., Mizuta, Y., Harada, T., Ozono, Y., Koji, T., and Kohno, S. (2004) TNP-470, an angiogenesis inhibitor, suppresses the progression of peritoneal fibrosis in mouse experimental model. Kidney Int. 66, 1677-1685
10. Contos, J. J., Ishii, I., Fukushima, N., Kingsbury, M. A., Ye, X., Kawamura, S., Brown, J. H., and Chun, J. (2002) Characterization of lpa(2) (Edg4) and lpa(1)/lpa(2) (Edg2/Edg4) lysophosphatidic acid receptor knockout mice: signaling deficits without obvious phenotypic abnormality attributable to lpa(2). Mol. Cell. Biol. 22, 6921-6929
11. Moolenaar, W. H., van Meeteren, L. A., and Giepmans, B. N. (2004) The ins and outs of lysophosphatidic acid signaling. Bioessays 26, 870-881
12. 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
13. 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
14. Miano, J. M. (2003) Serum response factor: toggling between disparate programs of gene expression. J. Mol. Cell. Cardiol. 35, 577-593
15. Muehlich, S., Cicha, I., Garlichs, C. D., Krueger, B., Posern, G., and Goppelt-Struebe, M. (2007) Actin-dependent regulation of connective tissue growth factor. Am. J. Physiol. Cell Physiol. 292, C1732-C1738
16. Leask, A., Parapuram, S. K., Shi-Wen, X., and Abraham, D. J. (2009) Connective tissue growth factor (CTGF, CCN2) gene regulation: a potent clinical bio-marker of fibroproliferative disease? J. Cell. Commun. Signal. 3, 89-94
17. Leask, A., and Abraham, D. J. (2003) The role of connective tissue growth factor, a multifunctional matricellular protein, in fibroblast biology. Biochem. Cell Biol. 81, 355-363
18. Liu, S., Shi-wen, X., Abraham, D. J., and Leask, A. (2011) CCN2 is required for bleomycin-induced skin fibrosis in mice. Arthritis Rheum. 63, 239-246
19. Van der Wal, J. B., and Jeekel, J. (2007) Biology of the peritoneum in normal homeostasis and after surgical trauma. Colorectal Dis. 9(Suppl. 2), 9-13
20. Kawaguchi, Y., Kawanishi, H., Mujais, S., Topley, N., and Oreopoulos, D. G. (2000) Encapsulating peritoneal sclerosis: definition, etiology, diagnosis, and treatment. International Society for Peritoneal Dialysis Ad Hoc Committee on Ultrafiltration Management in Peritoneal Dialysis. Perit. Dial. Int. 20(Suppl. 4), S43-55
21. Grassmann, A., Gioberge, S., Moeller, S., and Brown, G. (2005) ESRD patients in 2004: global overview of patient numbers, treatment modalities and associated trends. Nephrol. Dial. Transplant. 20, 2587-2593
22. Higuchi, C., Nishimura, H., and Sanaka, T. (2006) Biocompatibility of peritoneal dialysis fluid and influence of compositions on peritoneal fibrosis. Ther. Apher. Dial. 10, 372-379
23. Aroeira, L. S., Aguilera, A., Sanchez-Tomero, J. A., Bajo, M. A., del Peso, G., Jimenez-Heffernan, J. A., Selgas, R., and Lopez-Cabrera, M. (2007) Epithelial to mesenchymal transition and peritoneal membrane failure in peritoneal dialysis patients: pathologic significance and potential therapeutic interventions. J. Am. Soc. Nephrol. 18, 2004-2013
24. Rigby, R. J., and Hawley, C. M. (1998) Sclerosing peritonitis: the experience in Australia. Nephrol. Dial. Transplant. 13, 154-159
25. Bansal, S., Sheth, H., Siddiqui, N., Bender, F. H., Johnston, J. R., and Piraino, B. (2010) Incidence of encapsulating peritoneal sclerosis at a single U.S. university center. Adv. Perit. Dial. 26, 75-81
26. Contos, J. J., Fukushima, N., Weiner, J. A., Kaushal, D., and Chun, J. (2000) Requirement for the lpA1 lysophosphatidic acid receptor gene in normal suckling behavior. Proc. Natl. Acad. Sci. U. S. A. 97, 13384-13389
27. Lin, S. L., Kisseleva, T., Brenner, D. A., and Duffield, J. S. (2008) Pericytes and perivascular fibroblasts are the primary source of collagen-producing cells in obstructive fibrosis of the kidney. Am. J. Pathol. 173, 1617-1627
28. Tager, A. M., Kradin, R. L., LaCamera, P., Bercury, S. D., Campanella, G. S., Leary, C. P., Polosukhin, V., Zhao, L. H., Sakamoto, H., Blackwell, T. S., and Luster, A. D. (2004) Inhibition of pulmonary fibrosis by the chemokine IP-10/CXCL10. Am. J. Respir. Cell Mol. Biol. 31, 395-404
29. Vartiainen, M. K., Guettler, S., Larijani, B., and Treisman, R. (2007) Nuclear actin regulates dynamic subcellular localization and activity of the SRF cofactor MAL. Science 316, 1749-1752
30. Hjelle, J. T., Golinska, B. T., Waters, D. C., Steidley, K. R., McCarroll, D. R., and Dobbie, J. W. (1989) Isolation and propagation in vitro of peritoneal mesothelial cells. Perit. Dial. Int. 9, 341-347
31. Stylianou, E., Jenner, L. A., Davies, M., Coles, G. A., and Williams, J. D. (1990) Isolation, culture and characterization of human peritoneal mesothelial cells. Kidney Int. 37, 1563-1570
32. Sawada, T., Ishii, Y., Tojimbara, T., Nakajima, I., Fuchinoue, S., and Teraoka, S. (2002) The ACE inhibitor, quinapril, ameliorates peritoneal fibrosis in an encapsulating peritoneal sclerosis model in mice. Pharmacol. Res. 46, 505-510
33. Hinz, B., Phan, S. H., Thannickal, V. J., Prunotto, M., Desmouliere, A., Varga, J., De Wever, O., Mareel, M., and Gabbiani, G. (2012) Recent developments in myofibroblast biology: paradigms for connective tissue remodeling. Am. J. Pathol. 180, 1340-1355
34. Grotendorst, G. R. (1997) Connective tissue growth factor: a mediator of TGF-beta action on fibroblasts. Cytokine Growth Factor Rev. 8, 171-179
35. Mizutani, M., Ito, Y., Mizuno, M., Nishimura, H., Suzuki, Y., Hattori, R., Matsukawa, Y., Imai, M., Oliver, N., Goldschmeding, R., Aten, J., Krediet, R. T., Yuzawa, Y., and Matsuo, S. (2010) Connective tissue growth factor (CTGF/CCN2) is increased in peritoneal dialysis patients with high peritoneal solute transport rate. Am. J. Physiol. Renal Physiol. 298, F721-F733
36. Yung, S., Li, F. K., and Chan, T. M. (2006) Peritoneal mesothelial cell culture and biology. Perit. Dial. Int. 26, 162-173
37. Igarashi, A., Okochi, H., Bradham, D. M., and Grotendorst, G. R. (1993) Regulation of connective tissue growth factor gene expression in human skin fibroblasts and during wound repair. Mol. Biol. Cell 4, 637-645
38. Xu, M. Y., Porte, J., Knox, A. J., Weinreb, P. H., Maher, T. M., Violette, S. M., McAnulty, R. J., Sheppard, D., and Jenkins, G. (2009) Lysophosphatidic acid induces alphavbeta6 integrinmediated TGF-beta activation via the LPA2 receptor and the small G protein G alpha(q). Am. J. Pathol. 174, 1264-1279
39. Tatler, A. L., John, A. E., Jolly, L., Habgood, A., Porte, J., Brightling, C., Knox, A. J., Pang, L., Sheppard, D., Huang, X., and Jenkins, G. (2011) Integrin alphavbeta5-mediated TGF-beta activation by airway smooth muscle cells in asthma. J. Immunol. 187, 6094-6107
40. Lau, L. F., and Nathans, D. (1987) Expression of a set of growth-related immediate early genes in BALB/c 3T3 cells: coordinate regulation with c-fos or c-myc. Proc. Natl. Acad. Sci. U. S. A. 84, 1182-1186
41. Annes, J. P., Munger, J. S., and Rifkin, D. B. (2003) Making sense of latent TGF-beta activation. J. Cell Sci. 116, 217-224
42. Evelyn, C. R., Wade, S. M., Wang, Q., Wu, M., Iniguez-Lluhi, J. A., Merajver, S. D., and Neubig, R. R. (2007) CCG-1423: a small-molecule inhibitor of RhoA transcriptional signaling. Mol. Cancer Ther. 6, 2249-2260
43. Gan, L., Xue, J. X., Li, X., Liu, D. S., Ge, Y., Ni, P. Y., Deng, L., Lu, Y., and Jiang, W. (2011) Blockade of lysophosphatidic acid receptors LPAR1/3 ameliorates lung fibrosis induced by irradiation. Biochem. Biophys. Res. Commun. 409, 7-13
44. Cabello-Verrugio, C., Cordova, G., Vial, C., Zuniga, L. M., and Brandan, E. (2011) Connective tissue growth factor induction by lysophosphatidic acid requires transactivation of transforming growth factor type beta receptors and the JNK pathway. Cell. Signal. 23, 449-457
45. Price, M. A., Hill, C., and Treisman, R. (1996) Integration of growth factor signals at the c-fos serum response element. Philos. Trans. R. Soc. Lond. B Biol. Sci. 351, 551-559
46. 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
47. Yu, F. X., Zhao, B., Panupinthu, N., Jewell, J. L., Lian, I., Wang, L. H., Zhao, J., Yuan, H., Tumaneng, K., Li, H., Fu, X. D., Mills, G. B., and Guan, K. L. (2012) Regulation of the Hippo-YAP pathway by G-protein-coupled receptor signaling. Cell 150, 780-791
48. Deng, X., Mercer, P. F., Scotton, C. J., Gilchrist, A., and Chambers, R. C. (2008) Thrombin induces fibroblast CCL2/JE production and release via coupling of PAR1 to Galphaq and cooperation between ERK1/2 and Rho kinase signaling pathways. Mol. Biol. Cell 19, 2520-2533
49. Singh, I., Knezevic, N., Ahmmed, G. U., Kini, V., Malik, A. B., and Mehta, D. (2007) Galphaq-TRPC6-mediated Ca2 entry induces RhoA activation and resultant endothelial cell shape change in response to thrombin. J. Biol. Chem. 282, 7833-7843
50. Heusinger-Ribeiro, J., Eberlein, M., Wahab, N. A., and Goppelt-Struebe, M. (2001) Expression of connective tissue growth factor in human renal fibroblasts: regulatory roles of RhoA and cAMP. J. Am. Soc. Nephrol. 12, 1853-1861
51. Grotendorst, G. R., and Duncan, M. R. (2005) Individual domains of connective tissue growth factor regulate fibroblast proliferation and myofibroblast differentiation. FASEB J. 19, 729-738
52. Swaney, J. S., Chapman, C., Correa, L. D., Stebbins, K. J., Broadhead, A. R., Bain, G., Santini, A. M., Darlington, J., King, C. D., Baccei, C. S., Lee, C., Parr, T. A., Roppe, J. R., Seiders, T. J., Ziff, J., Prasit, P., Hutchinson, J. H., Evans, J. F., and Lorrain, D. S. (2011) Pharmacokinetic and pharmacodynamic characterization of an oral lysophosphatidic acid type 1 receptor-selective antagonist. J. Pharmacol. Exp. Ther. 336, 693-700
53. Watanabe, N., Ikeda, H., Nakamura, K., Ohkawa, R., Kume, Y., Tomiya, T., Tejima, K., Nishikawa, T., Arai, M., Yanase, M., Aoki, J., Arai, H., Omata, M., Fujiwara, K., and Yatomi, Y. (2007) Plasma lysophosphatidic acid level and serum autotaxin activity are increased in liver injury in rats in relation to its severity. Life Sci. 81, 1009-1015