Cardiac fibroblasts in cell culture systems: Myofibroblasts all along?

Journal of Cardiovascular Pharmacology

Volumn 57, Issue 4, 2011, Pages 389-399

  Rohr, Stephan ^a  

^a UNIVERSITY OF BERN   (Switzerland)

Author keywords

cardiac arrhythmia; cell culture; electrotonic crosstalk; fibroblast; Fibrosis; myofibroblast; paracrine crosstalk

Indexed keywords

CARDIAC FIBROBLAST; CARDIOVASCULAR DISEASE; CELL CULTURE; CELL INTERACTION; COCULTURE; FIBROBLAST; GAP JUNCTION; HEART DEPOLARIZATION; HEART ELECTROPHYSIOLOGY; MYOFIBROBLAST; MYOFIBROBLAST GAP JUNCTION; NONHUMAN; PARACRINE SIGNALING; PHENOTYPE; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; STROMA CELL;

ANIMALS; CELL CULTURE TECHNIQUES; FIBROBLASTS; FIBROSIS; HUMANS; MYOCARDIUM; MYOCYTES, CARDIAC; MYOFIBROBLASTS; PARACRINE COMMUNICATION; PHENOTYPE; STROMAL CELLS;

EID: 79954999107     PISSN: 01602446     EISSN: 15334023     Source Type: Journal    
DOI: 10.1097/FJC.0b013e3182137e17     Document Type: Review

References (100)

1. Goldsmith EC, Hoffman A, Morales MO, et al. Organization of fibroblasts in the heart. Dev Dynamics. 2004;230:787-794. (Pubitemid 38993878)
2. Kalluri R, Zeisberg M. Fibroblasts in cancer. Nat Rev Cancer. 2006;6: 392-401.
3. Giaume C, Koulakoff A, Roux L, et al. Astroglial networks: a step further in neuroglial and gliovascular interactions. Nat Rev Neurosci. 2010;11:87-99.
4. Fischer R, Reinehr R, Lu TP, et al. Intercellular communication via gap junctions in activated rat hepatic stellate cells. Gastroenterology. 2005; 128:433-448. (Pubitemid 40431095)
5. Ueda A, Nishida T, Otori T, et al. Electron-microscopic studies on the presence of gap junctions between corneal fibroblasts in rabbits. Cell Tissue Res. 1987;249:473-475.
6. Langevin HM, Cornbrooks CJ, Taatjes DJ. Fibroblasts form a body-wide cellular network. Histochem Cell Biol. 2004;122:7-15. (Pubitemid 39070588)
7. McAnulty RJ, Laurent GJ. Collagen synthesis and degradation in vivo. Evidence for rapid rates of collagen turnover with extensive degradation of newly synthesized collagen in tissues of the adult rat Coll Relat Res. 1987;7:93-104.
8. Banerjee I, Fuseler JW, Price RL, et al. Determination ofcell types and numbers during cardiac development in the neonatal and adult rat and mouse. Am JPhysiol Heart Circ Physiol. 2007;293:H1883-H1891. (Pubitemid 47367239)
9. Maisch B. Extracellular-matrix and cardiac interstitium\restriction is not a restricted phenomenon. Herz. 1995;20:75-80.
10. Nag AC Study of non-muscle cells of the adult mammalian heart\a fine-structural analysis and distribution. Cytobios. 1980;28:41-61. (Pubitemid 11219342)
11. Zak R. Development and proliferative capacity of cardiac-muscle cells. CircRes. 1974;35:17-26.
12. Gabbiani G The myofibroblast in wound healing and fibrocontractive diseases. J Pathol. 2003;200:500-503. (Pubitemid 36818250)
13. Weber KT. Extracellular matrix remodeling in heart failure: a role for de novo angiotensin ii generation. Circulation. 1997;96:4065-4082.
14. Weber KT. Fibrosis in hypertensive heart disease: Focus on cardiac fibroblasts. J Hypertens. 2004;22:47-50. (Pubitemid 38293529)
15. Desmouliere A, Chaponnier C, Gabbiani G Tissue repair, contraction, and the myofibroblast. Wound Repair Regen. 2005;13:7-12. (Pubitemid 40250424)
16. Amerongen MV, Bou-Gharios G, Popa E, et al. Bone marrow-derived myofibroblasts contribute functionally to scar formation after myocardial infarction. J Pathol. 2008;214:377-386. (Pubitemid 351212393)
17. Zeisberg EM, Tarnavski O, Zeisberg M, et al. Endothelial-to-mesenchymal transition contributes to cardiac fibrosis. Nat Med. 2007;13:952-961. (Pubitemid 47222040)
18. Tomasek JJ, Gabbiani G, Hinz B, et al. Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat Rev Mol Cell Biol. 2002;3:349-363. (Pubitemid 34619269)
19. Gabbiani G, Ryan GB, Majno G Presence of modified myofibroblasts in granulation tissue and their possible role in wound contraction. Experientia. 1971;27:549-550.
20. Darby I, Skalli O, Gabbiani G Alpha-smooth muscle actin is transiently expressed by myofibroblasts during experimental wound-healing. Lab Invest. 1990;63:21-29. (Pubitemid 20234670)
21. Singer II, Kawka DW, Kazazis DM, et al. In vivo co-distribution of fibronectin and actin fibers in granulation-tissue\immunofluorescence and electron-microscope studies of the fibronexus at the myofibroblast surface. J Cell Biol. 1984;98:2091-2106. (Pubitemid 14121840)
22. Gabbiani G, Chaponnier C, Huttner I. Cytoplasmic filaments and gap junctions in epithelial cells and myofibroblasts during wound healing. J Cell Biol. 1978;76:561-568. (Pubitemid 8295898)
23. Jamieson S, Going JJ, DArcy R, et al. Expression of gap junction proteins connexin 26 and connexin 43 in normal human breast and in breast tumours. J Pathol. 1998;184:37-43. (Pubitemid 28086151)
24. Powell DW, Mifflin RC, Valentich JD, et al. Myofibroblasts II. Intestinal subepithelial myofibroblasts. Am J Physiol. 1999;277:C183-C201.
25. Sui GP, Rothery S, Dupont E, et al. Gap junctions and connexin expression in human suburothelial interstitial cells. BJU Int. 2002;90: 118-129.
26. Wang J, Chen H, Seth A, et al. Mechanical force regulation of myofibroblast differentiation in cardiac fibroblasts. Am J Physiol Heart Circ Physiol. 2003;285:H1871-H1881. (Pubitemid 37305927)
27. Desmouliere A, Geinoz A, Gabbiani F, et al. Transforming growth factor-beta 1 induces alpha-smooth muscle actin expression in granulation tissue myofibroblasts and in quiescent and growing cultured fibroblasts. J Cell Biol. 1993;122:103-111. (Pubitemid 23188802)
28. Rønnov-Jessen L, Petersen O. Induction of alpha-smooth muscle actin by transforming growth factor-beta 1 in quiescent human breast gland fibroblasts. Implications for myofibroblast generation in breast neoplasia. Lab Invest. 1993;68:696-707. (Pubitemid 23202798)
29. Sun Y, Kiani MF, Postlethwaite AE, et al. Infarct scar as living tissue. Basic Res Cardiol. 2002;97:343-347.
30. Weber KT, Sun Y, Diez J. Fibrosis: a living tissue and the infarcted heart. JAm Coll Cardiol. 2008;52:2029-2031.
31. Petrov VV, Fagard RH, Lijnen PJ. Stimulation of collagen production by transforming growth factor-b1 during differentiation of cardiac fibroblasts to myofibroblasts. Hypertension. 2002;39:258-263. (Pubitemid 34165225)
32. De Bakker JMT, Van Capelle FJL, Janse MJ, et al. Slow conduction in the infarcted human heart\zigzag course of activation. Circulation. 1993;88:915-926. (Pubitemid 23264006)
33. Spach MS, Dolber PC Relating extracellular potentials and their derivatives to anisotropic propagation at a microscopic level in human cardiac muscle. Evidence for electrical uncoupling of side-to-side fiber connections with increasing age. CircRes. 1986;58:356-371. (Pubitemid 16120759)
34. Kohl P, Kamkin AG, Kiseleva IS, et al. Mechanosensitive fibroblasts in the sino-atrial node region of rat heart: interaction with cardiomyocytes and possible role. Exp Physiol. 1994;79:943-956. (Pubitemid 2163414)
35. McSpadden LC, Kirkton RD, Bursac N. Electrotonic loading of anisotropic cardiac monolayers by unexcitable cells depends on connexin type and expression level. Am J Physiol Cell Physiol. 2009; 297:C339-C351.
36. Goffin JM, Pittet P, Csucs G, et al. Focal adhesion size controls tension-dependent recruitment of a-smooth muscle actin to stress fibers. J Cell Biol. 2006;172:259-268. (Pubitemid 43112972)
37. Masur SK, Dewal HS, Dinh TT, et al. Myofibroblasts differentiate from fibroblasts when plated at low density. Proc NatlAcadSci USA. 1996;93: 4219-4223. (Pubitemid 26144266)
38. Santiago JJ, Dangerfield AL, Rattan SG, et al. Cardiac fibroblast to myofibroblast differentiation in vivo and in vitro: expression of focal adhesion components in neonatal and adult rat ventricular myofibro-blasts. Dev Dynamics. 2010;239:1573-1584.
39. Roy S, Khanna S, Bickerstaff AA, et al. Oxygen sensing by primary cardiac fibroblasts: a key role of p21. Circ Res. 2003;92:264-271. (Pubitemid 36258547)
40. Short M, Nemenoff RA, Zawada WM, et al. Hypoxia induces differentiation of pulmonary artery adventitial fibroblasts into myofi-broblasts. Am J Physiol Cell Physiol. 2004;286:C416-C425. (Pubitemid 38146366)
41. Leslie KO, Taatjes DJ, Schwarz J, et al. Cardiac myofibroblasts express alpha smooth muscle actin during right ventricular pressure overload in the rabbit Am J Pathol. 1991;139:207-216.
42. Poobalarahi F, Baicu CF, Bradshaw AD. Cardiac myofibroblasts differentiated in 3d culture exhibit distinct changes in collagen-I production, processing, and matrix deposition. Am J Physiol Heart Circ Physiol. 2006;291:H2924-H2932. (Pubitemid 44904094)
43. Thampatty BP, Wang JHC A new approach to study fibroblast migration. Cell Motility and the Cytoskeleton. 2007;64:1-5. (Pubitemid 44927725)
44. Vozenin MC, Lefaix JL, Ridi R, et al. The myofibroblast markers alpha-SM actin and beta-actin are differentially expressed in 2 and 3-d culture models of fibrotic and normal skin. Cytotechnology. 1998;26: 29-38. (Pubitemid 28076986)
45. Grinnell F, Ho C-H, Tamariz E, et al. Dendritic fibroblasts in three-dimensional collagen matrices. Mol Biol Cell. 2003;14:384-395. (Pubitemid 36237003)
46. Beningo KA, Dembo M, Wang YL. Responses of fibroblasts to anchorage of dorsal extracellular matrix receptors. Proc Natl Acad Sci USA. 2004;101:18024-18029. (Pubitemid 40054068)
47. Greenberg RS, Bernstein AM, Benezra M, et al. Fak-dependent regulation of myofibroblast differentiation. FASEB J. 2006;20: 1006-1008.
48. Kurikawa N, Suga M, Kuroda S, et al. An angiotensin II type 1 receptor antagonist, olmesartan medoxomil, improves experimental liver fibrosis by suppression of proliferation and collagen synthesis in activated hepatic stellate cells. Br J Pharmacol. 2003;139:1085-1094. (Pubitemid 36920670)
49. Yamada T, Kuno A, Masuda K, et al. Candesartan, an angiotensin II receptor antagonist, suppresses pancreatic inflammation and fibrosis in rats. J Pharmacol Exp Ther. 2003;307:17-23. (Pubitemid 37151887)
50. Swaney JS, Roth DM, Olson ER, et al. Inhibition of cardiac myofibroblast formation and collagen synthesis by activation and overexpression ofadenylyl cyclase. PNAS. 2005;102:437-442. (Pubitemid 40116785)
51. Lekgabe ED, Kiriazis H, Zhao C, et al. Relaxin reverses cardiac and renal fibrosis in spontaneously hypertensive rats. Hypertension. 2005;46:412-418. (Pubitemid 41099178)
52. Samuel CS, Unemori EN, Mookerjee I, et al. Relaxin modulates cardiac fibroblast proliferation, differentiation, and collagen pro-duction and reverses cardiac fibrosis in vivo. Endocrinology. 2004; 145:4125-4133. (Pubitemid 39120561)
53. Kapoun AM, Liang F, O'Young G, et al. B-type natriuretic peptide exerts broad functional opposition to transforming growth factor-b in primary human cardiac fibroblasts: fibrosis, myofibroblast conversion, pro-liferation, and inflammation. Circ Res. 2004;94:453-461. (Pubitemid 38326280)
54. Olson ER, Naugle JE, Zhang X, et al. Inhibition of cardiac fibroblast proliferation and myofibroblast differentiation by resveratrol. Am J Physiol. 2005;288:H1131-H1138. (Pubitemid 40270016)
55. Kolodsick JE, Peters-Golden M, Larios J, et al. Prostaglandin e2 inhibits fibroblast to myofibroblast transition via prostanoid receptor 2 signaling and cyclic adenosine monophosphate elevation. Am J. Respir Cell Mol Biol. 2003;29:537-544. (Pubitemid 37357704)
56. Burgess HA, Daugherty LE, Thatcher TH, et al. PPARg agonists inhibit TGF-ß induced pulmonary myofibroblast differentiation and collagen production: implications for therapy of lung fibrosis. Am JPhysiol. 2005; 288:L1146-L1153. (Pubitemid 40695441)
57. Hinz B, Celetta G, Tomasek JJ, et al. Alpha-smooth muscle actin expression upregulates fibroblast contractile activity. Mol Biol Cell. 2001;12:2730-2741. (Pubitemid 33051938)
58. Chilton L, Ohya S, Freed D, et al. K+ currents regulate the resting membrane potential, proliferation, and contractile responses in ventric-ular fibroblasts and myofibroblasts. Am J Physiol Heart Circ Physiol. 2005;288:H2931-H2939. (Pubitemid 40720677)
59. Shibukawa Y, Chilton EL, MacCannell KA, et al. K+ currents activated by depolarization in cardiac fibroblasts. Biophys J. 2005;88:3924-3935. (Pubitemid 40991105)
60. Walsh KB, Zhang J. Neonatal rat cardiac fibroblasts express three types of voltage-gated k+ channels: regulation of a transient outward current by protein kinase C Am J Physiol Heart Circ Physiol. 2008;294: H1010-H1017. (Pubitemid 351253315)
61. Wang YJ, Sung R, Lin MW, et al. Contribution of BK(Ca)-channel activity in human cardiac fibroblasts to electrical coupling of cardiomyocytes- fibroblasts. JMemb Biol. 2006;213:175-185. (Pubitemid 46790733)
62. Yue L, Xie J, Nattel S. Molecular determinants of cardiac fibroblast electrical function and therapeutic implications for atrial fibrillation. Cardiovasc Res. 2010 November 19, [Epub ahead of print].
63. Miragoli M, Gaudesius G, Rohr S. Electrotonic modulation of cardiac impulse conduction by myofibroblasts. Circ Res. 2006;98:801-810.
64. Zhang Y Kanter EM, Yamada KA. Remodeling of cardiac fibroblasts following myocardial infarction results in increased gap junction intercellular communication. Cardiovasc Pathol. 2010;19: e233-e240.
65. Camelliti P, Devlin GP, Matthews KG, et al. Spatially and temporally distinct expression of fibroblast connexins after sheep ventricular infarction. Cardiovasc Res. 2004;62:415-425. (Pubitemid 38496554)
66. Doble BW, Kardami E. Basic fibroblast growth factor stimulates connexin-43 expression and intercellular communication of cardiac fibroblasts. Mol Cell Biochem. 1995;143:81-87.
67. Goshima K Synchronized beating of and electrotonic transmission between myocardial cells mediated by heterotypic strain cells in monolayer culture. Exp Cell Res. 1969;58:420-426.
68. Hyde A, Blondel B, Matter A, et al. Homo-and heterocellular junctions in cell cultures: an electrophysiological and morphological study Prog Brain Res. 1969;31:283-311.
69. Rohr S, Flückiger-Labrada R, Kucera JP. Photolithographically defined deposition of attachment factors as a versatile method for patterning the growth of different cell types in culture. Eur J Physiol. 2003;446: 125-132. (Pubitemid 36539541)
70. Rohr S, Kucera JP. Optical recording system based on a fiber optic image conduit: assessement of microscopic activation patterns in cardiac tissue. Biophys J. 1998;75:1062-1075. (Pubitemid 28357548)
71. Rook MB, van Ginneken AC, de Jonge B, et al. Differences in gap junction channels between cardiac myocytes, fibroblasts, and heterol-ogous pairs. Am J Physiol Cell Physiol. 1992;263:C959-C977.
72. Gaudesius G, Miragoli M, Thomas SP, et al. Coupling of cardiac electrical activity over extended distances by fibroblasts of cardiac origin. Circ Res. 2003;93:421-428. (Pubitemid 37100007)
73. Rohr S, Kucera JP, Kléber AG Slow conduction in cardiac tissue, I: effects of a reduction of excitability versus a reduction of electrical coupling on microconduction. Circ Res. 1998;83:781-794. (Pubitemid 28489075)
74. Janse M, van Capelle F, Morsink H, et al. Flow of 'injury' current and patterns of excitation during early ventricular arrhythmias in acute regional myocardial ischemia in isolated porcine and canine hearts. Evidence for two different arrhythmogenic mechanisms. Circ Res. 1980; 47:151-165. (Pubitemid 10056042)
75. Feld Y Melamed-Frank M, Kehat I, et al. Electrophysiological modulation of cardiomyocytic tissue by transfected fibroblasts express-ing potassium channels: a novel strategy to manipulate excitability. Circulation. 2002;105:522-529. (Pubitemid 34141712)
76. Yankelson L, Feld Y Bressler-Stramer T, et al. Cell therapy for modification of the myocardial electrophysiological substrate. Circulation. 2008;117:720-731. (Pubitemid 351640673)
77. Zlochiver S, Muñoz V, Vikstrom KL, et al. Electrotonic myofibroblast-to-myocyte coupling increases propensity to reentrant arrhythmias in two-dimensional cardiac monolayers. Biophys J. 2008;95:4469-4480.
78. Katzung B. Effects of extracellular calcium and sodium on de-polarization-induced automaticity in guinea pig papillary muscle. Circ Res. 1975;37:118-127.
79. Miragoli M, Salvarani N, Rohr S. Myofibroblasts induce ectopic activity in cardiac tissue. Circ Res. 2007;101:755-758. (Pubitemid 350287189)
80. Fahrenbach JP, Mejia-Alvarez R, Banach K The relevance of non-excitable cells for cardiac pacemaker function. J Physiol. 2007;585: 565-578. (Pubitemid 350193925)
81. Kizana E, Ginn SL, Smyth CM, et al. Fibroblasts modulate cardiomyocyte excitability: implications for cardiac gene therapy. Gene Ther. 2006;13:1611-1615. (Pubitemid 44688462)
82. Powell DW, Mifflin RC, Valentich JD, et al. Myofibroblasts I. Paracrine cells important in health and disease. Am J Physiol Cell Physiol. 1999; 277:C1-C19. (Pubitemid 29352620)
83. LaFramboise WA, Scalise D, Stoodley P, et al. Cardiac fibroblasts influence cardiomyocyte phenotype in vitro. Am J Physiol Cell Physiol. 2007;292:C1799-C1808. (Pubitemid 47080551)
84. Rossini A, Zacheo A, Mocini D, et al. HMGB 1-stimulated human primary cardiac fibroblasts exert a paracrine action on human and murine cardiac stem cells. J Mol Cell Cardiol. 2008;44:683-693.
85. Sano M, Fukuda K, Kodama H, et al. Interleukin-6 family of cytokines mediate angiotensin II-induced cardiac hypertrophy in rodent cardio-myocytes. J Biol Chem. 2000;275:29717-29723. (Pubitemid 32043853)
86. Briest W, Homagk L, Rassler B, et al. Norepinephrine-induced changes in cardiac transforming growth factor-ß isoform expression pattern of female and male rats. Hypertension. 2004;44:410-418. (Pubitemid 39281488)
87. Takahashi N, Calderone A, Izzo NJ, et al. Hypertrophic stimuli induce transforming growth factor-beta 1 expression in rat ventricular myocytes. J Clin Invest. 1994;94:1470-1476. (Pubitemid 24309866)
88. Verheule S, Sato T, Everett T IV, et al. Increased vulnerability to atrial fibrillation in transgenic mice with selective atrial fibrosis caused by overexpression of TGF-ß1. CircRes. 2004;94:1458-1465. (Pubitemid 38780318)
89. Guy JL, Lambert DW, Turner AJ, et al. Functional angiotensin-converting enzyme 2 is expressed in human cardiac myofibroblasts. Exp Physiol. 2008;93:579-588. (Pubitemid 351595051)
90. Katwa LC, Campbell SE, Tyagi SC, et al. Cultured myofibroblasts generate angiotensin peptides de novo. J Mol Cell Cardiol. 1997;29: 1375-1386. (Pubitemid 27259651)
91. Goette A, Lendeckel U. Electrophysiological effects of angiotensin II. Part I: signal transduction and basic electrophysiological mechanisms. Europace. 2008;10:238-241. (Pubitemid 351767699)
92. Manabe I, Shindo T, Nagai R. Gene expression in fibroblasts and fibrosis: involvement in cardiac hypertrophy Circ Res. 2002;91:1103-1113. (Pubitemid 36076358)
93. Pedram A, Razandi M, O'Mahony F, et al. Estrogen receptor-ß prevents cardiac fibrosis. Mol Endocrinol. 2010;24:2152-2165.
94. Creemers EE, Pinto YM. Molecular mechanisms that control interstitial fibrosis in the pressure overloaded heart. Cardiovasc Res. 2011;89: 265-272.
95. Doble BW, Chen Y, Bosc DG, et al. Fibroblast growth factor-2 decreases metabolic coupling and stimulates phosphorylation as well as masking of connexin43 epitopes in cardiac myocytes. Circ Res. 1996;79:647-658. (Pubitemid 26317812)
96. Merle P-L, Feige J-J, Verdetti J. Basic fibroblast growth factor activates calcium channels in neonatal rat cardiomyocytes. J Biol Chem. 1995; 270:17361-17367.
97. Zhuang J, Yamada KA, Saffitz JE, et al. Pulsatile stretch remodels cell-to-cell communication in cultured myocytes. Circ Res. 2000;87: 316-322. (Pubitemid 30655973)
98. Teos LY, Zhao A, Alvin Z, et al. Basal and IGF-I-dependent regulation of potassium channels by map kinases and pi3-kinase during eccentric cardiac hypertrophy. Am J Physiol Heart Circ Physiol. 2008;295: H1834-H1845.
99. Clement S, Chaponnier C, Gabbiani G A subpopulation of cardiomyo-cytes expressing a-skeletal actin is identified by a specific polyclonal antibody. Circ Res. 1999;85:e51-e58.
100. Rohr S. Myofibroblasts in diseased hearts: new players in cardiac arrhythmias? Heart Rhythm. 2009;6:848-856.