Role of scleraxis in mechanical stretch-mediated regulation of cardiac myofibroblast phenotype

American Journal of Physiology - Cell Physiology

Volumn 311, Issue 2, 2016, Pages C297-C307

  Roche, Patricia L ^a   Nagalingam, Raghu S ^a   Bagchi, Rushita A ^a   Aroutiounova, Nina ^a   Belisle, Breanna M J ^a   Wigle, Jeffrey T ^a   Czubryt, Michael P ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

Author keywords

Cardiac fibroblast; Migration; Proliferation; Stretch; Transcription factor

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; COLLAGEN TYPE 1; COLLAGEN TYPE 3; F ACTIN; FOCAL ADHESION KINASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SCLERAXIS; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; VINCULIN; ACTIN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL CYCLE PROGRESSION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; FOCAL ADHESION; GENE EXPRESSION; HEART FIBROBLAST; IN VITRO STUDY; MALE; MYOFIBROBLAST; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; RAT; STRESS FIBER; ANIMAL; CARDIAC MUSCLE; CELL CULTURE; CELL MOTION; EXTRACELLULAR MATRIX; FIBROBLAST; GENE EXPRESSION REGULATION; GENETICS; HEART; METABOLISM; MOUSE; NIH 3T3 CELL LINE; PHENOTYPE; PHYSIOLOGY; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT;

ACTINS; ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; COLLAGEN TYPE I; EXTRACELLULAR MATRIX; FIBROBLASTS; FOCAL ADHESIONS; GENE EXPRESSION REGULATION; HEART; MALE; MICE; MYOCARDIUM; MYOFIBROBLASTS; NIH 3T3 CELLS; PHENOTYPE; PROMOTER REGIONS, GENETIC; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA;

EID: 84983684781     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00333.2015     Document Type: Article

References (49)

1. Bagchi RA, Czubryt MP. Synergistic roles of scleraxis and Smads in the regulation of collagen 1alpha2 gene expression. Biochim Biophys Acta 1823: 1936–1944, 2012.
2. Bagchi RA, Lin J, Wang R, Czubryt MP. Regulation of fibronectin gene expression in cardiac fibroblasts by scleraxis. Cell Tissue Res 2016 Jun 21. [Epub ahead of print].
3. Bagchi RA, Roche P, Aroutiounova N, Espira L, Abrenica B, Schweitzer R, Czubryt MP. The transcription factor scleraxis is a critical regulator of cardiac fibroblast phenotype. BMC Biol 14: 21, 2016.
4. Barnette DN, Hulin A, Ahmed AS, Colige AC, Azhar M, Lincoln J. Tgfbeta-Smad and MAPK signaling mediate scleraxis and proteoglycan expression in heart valves. J Mol Cell Cardiol 65: 137–146, 2013.
5. Berthet E, Chen C, Butcher K, Schneider RA, Alliston T, Amirtharajah M. Smad3 binds scleraxis and mohawk and regulates tendon matrix organization. J Orthop Res 31: 1475–1483, 2013.
6. Butt RP, Bishop JE. Mechanical load enhances the stimulatory effect of serum growth factors on cardiac fibroblast procollagen synthesis. J Mol Cell Cardiol 29: 1141–1151, 1997.
7. Cai Y, Biais N, Giannone G, Tanase M, Jiang G, Hofman JM, Wiggins CH, Silberzan P, Buguin A, Ladoux B, Sheetz MP. Nonmuscle myosin IIA-dependent force inhibits cell spreading and drives F-actin flow. Biophys J 91: 3907–3920, 2006.
8. Carver W, Nagpal ML, Nachtigal M, Borg TK, Terracio L. Collagen expression in mechanically stimulated cardiac fibroblasts. Circ Res 69: 116–122, 1991.
9. Chen YJ, Huang CH, Lee IC, Lee YT, Chen MH, Young TH. Effects of cyclic mechanical stretching on the mRNA expression of tendon/ ligament-related and osteoblast-specific genes in human mesenchymal stem cells. Connect Tissue Res 49: 7–14, 2008.
10. Chiquet M, Gelman L, Lutz R, Maier S. From mechanotransduction to extracellular matrix gene expression in fibroblasts. Biochim Biophys Acta 1793: 911–920, 2009.
11. Czubryt MP. Common threads in cardiac fibrosis, infarct scar formation, and wound healing. Fibrogenesis Tissue Repair 5: 19, 2012.
12. Darby I, Skalli O, Gabbiani G. Alpha-smooth muscle actin is transiently expressed by myofibroblasts during experimental wound healing. Lab Invest 63: 21–29, 1990.
13. Desai LP, White SR, Waters CM. Mechanical stretch decreases FAK phosphorylation and reduces cell migration through loss of JIP3-induced JNK phosphorylation in airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 297: L520–L529, 2009.
14. Deten A, Holzl A, Leicht M, Barth W, Zimmer HG. Changes in extracellular matrix and in transforming growth factor beta isoforms after coronary artery ligation in rats. J Mol Cell Cardiol 33: 1191–1207, 2001.
15. Espira L, Czubryt MP. Emerging concepts in cardiac matrix biology. Can J Physiol Pharmacol 87: 996–1008, 2009.
16. Espira L, Lamoureux L, Jones SC, Gerard RD, Dixon IM, Czubryt MP. The basic helix-loop-helix transcription factor scleraxis regulates fibroblast collagen synthesis. J Mol Cell Cardiol 47: 188–195, 2009.
17. Fernandez IE, Eickelberg O. New cellular and molecular mechanisms of lung injury and fibrosis in idiopathic pulmonary fibrosis. Lancet 380: 680–688, 2012.
18. Freed DH, Cunnington RH, Dangerfield AL, Sutton JS, Dixon IM. Emerging evidence for the role of cardiotrophin-1 in cardiac repair in the infarcted heart. Cardiovasc Res 65: 782–792, 2005.
19. Gabbiani G. The cellular derivation and the life span of the myofibroblast. Pathol Res Pract 192: 708–711, 1996.
20. Garrison G, Huang SK, Okunishi K, Scott JP, Kumar Penke LR, Scruggs AM, Peters-Golden M. Reversal of myofibroblast differentiation by prostaglandin E(2). Am J Respir Cell Mol Biol 48: 550–558, 2013.
21. Hecker L, Jagirdar R, Jin T, Thannickal VJ. Reversible differentiation of myofibroblasts by MyoD. Exp Cell Res 317: 1914–1921, 2011.
22. Hinz B. Tissue stiffness, latent TGF-beta1 activation, and mechanical signal transduction: implications for the pathogenesis and treatment of fibrosis. Curr Rheumatol Rep 11: 120–126, 2009.
23. Hinz B, Gabbiani G, Chaponnier C. The NH2-terminal peptide of alpha-smooth muscle actin inhibits force generation by the myofibroblast in vitro and in vivo. J Cell Biol 157: 657–663, 2002.
24. Hinz B, Mastrangelo D, Iselin CE, Chaponnier C, Gabbiani G. Mechanical tension controls granulation tissue contractile activity and myofibroblast differentiation. Am J Pathol 159: 1009–1020, 2001.
25. Hinz B, Phan SH, Thannickal VJ, Galli A, Bochaton-Piallat ML, Gabbiani G. The myofibroblast: one function multiple origins. Am J Pathol 170: 1807–1816, 2007.
26. Hinz B, Phan SH, Thannickal VJ, Prunotto M, Desmouliere A, Varga J, De Wever O, Mareel M, Gabbiani G. Recent developments in myofibroblast biology: paradigms for connective tissue remodeling. Am J Pathol 180: 1340–1355, 2012.
27. Hoffman LM, Jensen CC, Chaturvedi A, Yoshigi M, Beckerle MC. Stretch-induced actin remodeling requires targeting of zyxin to stress fibers and recruitment of actin regulators. Mol Biol Cell 23: 1846–1859, 2012.
28. Husse B, Briest W, Homagk L, Isenberg G, Gekle M. Cyclical mechanical stretch modulates expression of collagen I and collagen III by PKC and tyrosine kinase in cardiac fibroblasts. Am J Physiol Regul Integr Comp Physiol 293: R1898–R1907, 2007.
29. Leask A. Getting to the heart of the matter: new insights into cardiac fibrosis. Circ Res 116: 1269–1276, 2015.
30. Lejard V, Brideau G, Blais F, Salingcarnboriboon R, Wagner G, Roehrl MH, Noda M, Duprez D, Houillier P, Rossert J. Scleraxis and NFATc regulate the expression of the pro-alpha1(I) collagen gene in tendon fibroblasts. J Biol Chem 282: 17665–17675, 2007.
31. Levay AK, Peacock JD, Lu Y, Koch M, Hinton RB Jr, Kadler KE, Lincoln J. Scleraxis is required for cell lineage differentiation and extracellular matrix remodeling during murine heart valve formation in vivo. Circ Res 103: 948–956, 2008.
32. Lijnen PJ, Petrov VV, Fagard RH. Induction of cardiac fibrosis by transforming growth factor-beta(1). Mol Genetics Metab 71: 418–435, 2000.
33. Ma Y, Halade GV, Lindsey ML. Extracellular matrix and fibroblast communication following myocardial infarction. J Cardiovasc Transl Res 5: 848–857, 2012.
34. Maltseva O, Folger P, Zekaria D, Petridou S, Masur SK. Fibroblast growth factor reversal of the corneal myofibroblast phenotype. Invest Ophthalmol Vis Sci 42: 2490–2495, 2001.
35. Mitra SK, Hanson DA, Schlaepfer DD. Focal adhesion kinase: in command and control of cell motility. Nat Rev Mol Cell Biol 6: 56–68, 2005.
36. Muchaneta-Kubara EC, el Nahas AM. Myofibroblast phenotypes expression in experimental renal scarring. Nephrol Dial Transplant 12: 904–915, 1997.
37. Popov Y, Schuppan D. Targeting liver fibrosis: strategies for development and validation of antifibrotic therapies. Hepatology 50: 1294–1306, 2009.
38. Roche PL, Filomeno KL, Bagchi RA, Czubryt MP. Intracellular signaling of cardiac fibroblasts. Compr Physiol 5: 721–760, 2015.
39. Santiago JJ, Dangerfield AL, Rattan SG, Bathe KL, Cunnington RH, Raizman JE, Bedosky KM, Freed DH, Kardami E, Dixon IM. Cardiac fibroblast to myofibroblast differentiation in vivo and in vitro: expression of focal adhesion components in neonatal and adult rat ventricular myofibroblasts. Dev Dyn 239: 1573–1584, 2010.
40. Scott A, Danielson P, Abraham T, Fong G, Sampaio AV, Underhill TM. Mechanical force modulates scleraxis expression in bioartificial tendons. J Musculoskelet Neuronal Interact 11: 124–132, 2011.
41. Song G, Luo Q, Xu B, Ju Y. Mechanical stretch-induced changes in cell morphology and mRNA expression of tendon/ligament-associated genes in rat bone-marrow mesenchymal stem cells. Mol Cell Biomech 7: 165–174, 2010.
42. Speca S, Giusti I, Rieder F, Latella G. Cellular and molecular mechanisms of intestinal fibrosis. World J Gastroenterol 18: 3635–3661, 2012.
43. Swynghedauw B. Molecular mechanisms of myocardial remodeling. Physiol Rev 79: 215–262, 1999.
44. Tomasek JJ, Gabbiani G, Hinz B, Chaponnier C, Brown RA. Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat Rev Mol Cell Biol 3: 349–363, 2002.
45. Tomasek JJ, Haaksma CJ, Eddy RJ, Vaughan MB. Fibroblast contraction occurs on release of tension in attached collagen lattices: dependency on an organized actin cytoskeleton and serum. Anat Record 232: 359–368, 1992.
46. Vaughan MB, Odejimi TD, Morris TL, Sawalha D, Spencer CL. A new bioassay identifies proliferation ratios of fibroblasts and myofibroblasts. Cell Biol Int 38: 981–986, 2014.
47. Yoshigi M, Hoffman LM, Jensen CC, Yost HJ, Beckerle MC. Mechanical force mobilizes zyxin from focal adhesions to actin filaments and regulates cytoskeletal reinforcement. J Cell Biol 171: 209–215, 2005.
48. Zhang L, Tran N, Chen HQ, Kahn CJ, Marchal S, Groubatch F, Wang X. Time-related changes in expression of collagen types I and III and of tenascin-C in rat bone mesenchymal stem cells under co-culture with ligament fibroblasts or uniaxial stretching. Cell Tissue Res 332: 101–109, 2008.
49. Zhou Y, Huang X, Hecker L, Kurundkar D, Kurundkar A, Liu H, Jin TH, Desai L, Bernard K, Thannickal VJ. Inhibition of mechanosensitive signaling in myofibroblasts ameliorates experimental pulmonary fibrosis. J Clin Invest 123: 1096–1108, 2013.