Myocardial fibroblast-matrix interactions and potential therapeutic targets

Journal of Molecular and Cellular Cardiology

Volumn 70, Issue , 2014, Pages 92-99

  Goldsmith, Edie C ^a   Bradshaw, Amy D ^b,c   Zile, Michael R ^b,c   Spinale, Francis G ^a,d  

^a UNIVERSITY OF SOUTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b RALPH H JOHNSON VA MEDICAL CENTER   (United States)

^c MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^d WJB Dorn VA Medical Center   (United States)

Author keywords

Discoidin Domain Receptor; Extracellular matrix; Fibroblast; Integrin; Myofibroblast; Transformation

Indexed keywords

CELL MARKER; COLLAGEN TYPE 1; DISCOIDIN DOMAIN RECEPTOR 2; FIBROBLAST ACTIVATION PROTEIN; FIBROBLAST SPECIFIC PROTEIN; INTEGRIN; UNCLASSIFIED DRUG; VIMENTIN; DISCOIDIN RECEPTOR; LECTIN RECEPTOR; PROTEIN TYROSINE KINASE;

BIOACCUMULATION; CELL ACTIVATION; CELL DIFFERENTIATION; CELL FUNCTION; CELL INTERACTION; CELL POPULATION; EXTRACELLULAR MATRIX; FIBROBLAST; HEART MUSCLE CELL; HUMAN; INTRACELLULAR SIGNALING; MOLECULAR DIAGNOSIS; MOLECULAR EVOLUTION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; REVIEW; UPREGULATION; ANIMAL; CHEMISTRY; FIBROSIS; GENE EXPRESSION REGULATION; GENETICS; HEART MUSCLE; METABOLISM; MOLECULARLY TARGETED THERAPY; MYOFIBROBLAST; PATHOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; CELL DIFFERENTIATION; COLLAGEN TYPE I; EXTRACELLULAR MATRIX; FIBROBLASTS; FIBROSIS; GENE EXPRESSION REGULATION; HUMANS; INTEGRINS; MOLECULAR TARGETED THERAPY; MYOCARDIUM; MYOFIBROBLASTS; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, MITOGEN; SIGNAL TRANSDUCTION;

EID: 84899120281     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2014.01.008     Document Type: Review

References (99)

1. Spinale F.G. Myocardial matrix remodeling and the matrix metalloproteinases: influence on cardiac form and function. Physiol Rev 2007, 87:1285-1342.
2. Caulfield J.B., Borg T.K. The collagen network of the heart. Lab Invest 1979, 40:364-372.
3. Souders C.A., Bowers S.L.K., Baudino T.A. Cardiac fibroblast: the renaissance cell. Circ Res 2009, 105:1164-1176.
4. Fan D., Takawale A., Lee J., Kassiri Z. Cardiac fibroblasts, fibrosis and extracellular matrix remodeling in heart disease. Fibrogenesis Tissue Repair 2012, 5:15.
5. Eghbali M., Weber K.T. Collagen and the myocardium: fibrillar structure, biosynthesis and degradation in relation to hypertrophy and its regression. Mol Cell Biochem 1990, 96:1-14.
6. Wenstrup R.J., Florer J.B., Brunskill E.W., Bell S.M., Chervoneva I., Birk D.E. Type V collagen controls the initiation of collagen fibril assembly. J Biol Chem 2004, 279:53331-53337.
7. Prockop D.J., Kivirikko K.I. Collagens: molecular biology, diseases, and potentials for therapy. Annu Rev Biochem 1995, 64:403-434.
8. Prockop D.J., Hulmes D.J.S. Assembly of collagen fibrils de novo from soluble precursors: polymerization and copolymerization of procollagen, pN-collagen, and mutated collagens. Collagen: primer in structure, processing and assembly 1994, 47-90. Academic Press, San Diego, CA.
9. Colige A., Vandenberghe I., Thiry M., Lambert C.A., Van Beeumen J., Li S.W., et al. Cloning and characterization of ADAMTS-14, a novel ADAMTS displaying high homology with ADAMTS-2 and ADAMTS-3. J Biol Chem 2002, 277:5756-5766.
10. Kessler E., Takahara K., Biniaminov L., Brusel M., Greenspan D.S. Bone morphogenetic protein-1: the type I procollagen C-proteinase. Science 1996, 271:360-362.
11. Steiglitz B.M., Keene D.R., Greenspan D.S. PCOLCE2 encodes a functional procollagen C-proteinase enhancer (PCPE2) that is a collagen-binding protein differing in distribution of expression and post-translational modification from the previously described PCPE1. J Biol Chem 2002, 277:49820-49830.
12. Takahara K., Kessler E., Biniaminov L., Brusel M., Eddy R.L., Jani-Sait S., et al. Type I procollagen COOH-terminal proteinase enhancer protein: identification, primary structure, and chromosomal localization of the cognate human gene (PCOLCE). J Biol Chem 1994, 269:26280-26285.
13. Baicu C.F., Zhang Y., Van Laer A.O., Renaud L., Zile M.R., Bradshaw A.D. Effects of the absence of procollagen C-endopeptidase enhancer-2 on myocardial collagen accumulation in chronic pressure overload. Am J Physiol Heart Circ Physiol 2012, 303:H234-H240.
14. Boluyt M.O., O'Neill L., Meredith A.L., Bing O.H., Brooks W.W., Conrad C.H., et al. Alterations in cardiac gene expression during the transition from stable hypertrophy to heart failure. Marked upregulation of genes encoding extracellular matrix components. Circ Res 1994, 75:23-32.
15. Borg T.K., Rubin K., Lundgren E., Borg K., Obrink B. Recognition of extracellular matrix components by neonatal and adult cardiac myocytes. Dev Biol 1984, 104:86-96.
16. Trombetta-Esilva J., Eadie E.P., Zhang Y., Norris R.A., Borg T.K., Bradshaw A.D. The effects of age and the expression of SPARC on extracellular matrix production by cardiac fibroblasts in 3-D cultures. PLoS One 2013, 8:e79715.
17. Konstandin M.H., Toko H., Gastelum G.M., Quijada P., De La Torre A., Quintana M., et al. Fibronectin is essential for reparative cardiac progenitor cell response after myocardial infarction. Circ Res 2013, 113:115-125.
18. Serini G., Bochaton-Piallat M.L., Ropraz P., Geinoz A., Borsi L., Zardi L., et al. The fibronectin domain ED-A is crucial for myofibroblastic phenotype induction by transforming growth factor-beta1. J Cell Biol 1998, 142:873-881.
19. Arslan F., Smeets M.B., Riem Vis P.W., Karper J.C., Quax P.H., Bongartz L.G., et al. Lack of fibronectin-EDA promotes survival and prevents adverse remodeling and heart function deterioration after myocardial infarction. Circ Res 2011, 108:582-592.
20. Frangogiannis N.G. Matricellular proteins in cardiac adaptation and disease. Physiol Rev 2012, 92:635-688.
21. Xia Y., Dobaczewski M., Gonzalez-Quesada C., Chen W., Biernacka A., Li N., et al. Endogenous thrombospondin 1 protects the pressure-overloaded myocardium by modulating fibroblast phenotype and matrix metabolism. Hypertension 2011, 58:902-911.
22. Bradshaw A.D., Baicu C.F., Rentz T.J., Van Laer A.O., Boggs J., Lacy J.M., et al. Pressure overload-induced alterations in fibrillar collagen content and myocardial diastolic function: role of secreted protein acidic and rich in cysteine (SPARC) in post-synthetic procollagen processing. Circulation 2009, 119:269-280.
23. Dobaczewski M., Gonzalez-Quesada C., Frangogiannis N.G. The extracellular matrix as a modulator of the inflammatory and reparative response following myocardial infarction. J Mol Cell Cardiol 2010, 48:504-511.
24. Tamaoki M., Imanaka-Yoshida K., Yokoyama K., Nishioka T., Inada H., Hiroe M., et al. Tenascin-C regulates recruitment of myofibroblasts during tissue repair after myocardial injury. Am J Pathol 2005, 167:71-80.
25. McCurdy S., Baicu C.F., Heymans S., Bradshaw A.D. Cardiac extracellular matrix remodeling: fibrillar collagens and Secreted Protein Acidic and Rich in Cysteine (SPARC). J Mol Cell Cardiol 2010, 48:544-549.
26. Dettman R.W., Denetclaw W., Ordahl C.P., Bristow J. Common epicardial origin of coronary vascular smooth muscle, perivascular fibroblasts and intermyocardial fibroblasts in the avian heart. Dev Biol 1998, 193:169-181.
27. Gittenberger-De Groot A.C., Vrancken Peeters M.P.F.M., Mentine M.M.T., Gourdie R.G., Poelmann R.E. Epicardium-derived cells contribute to a novel population to the myocardial wall and the atrioventricular cushions. Circ Res 1998, 82:1043-1052.
28. Snider P., Standley K.N., Wang J., Azhar M., Doetschman T., Conway S.J. Origin of cardiac fibroblasts and the role of periostin. Circ Res 2009, 105:934-947.
29. Morales M.O., Price R.L., Goldsmith E.C. Expression of Discoidin Domain Receptor 2 (DDR2) in the developing heart. Microsc Microanal 2005, 11:260-267.
30. Goldsmith E.C., Hoffman A., Morales M.O., Potts J.D., Price R.L., McFadden A., et al. Organization of fibroblasts in the heart. Dev Dyn 2004, 230:787-794.
31. Banerjee I., Fuseler J.W., Price R.L., Borg T.K., Baudino T.A. Determination of cell types and numbers during cardiac development in the neonatal and adult rat and mouse. Am J Physiol Heart Circ Physiol 2007, 293:H1883-H1891.
32. Nag A. Study of non-muscle cells of the adult mammalian heart: a fine structural analysis and distribution. Cytobios 1980, 28:41-61.
33. Zak R. Development and proliferative capacity of cardiac muscle cells. Circ Res 1974, 32:17-26.
34. Frangogiannis N.G. The mechanistic basis of infarct healing. Antioxid Redox Signal 2006, 8:1907-1939.
35. Balasubramanian S., Quinones L., Kasiganesan H., Zhang Y., Pleasant D.L., Sundararai K.P., et al. β3 integrin in cardiac fibroblast is critical for extracellular matrix accumulation during pressure overload hypertrophy in mouse. PLoS One 2012, 7:e45076.
36. Kuwahara F., Kai H., Tokuda K., Kai M., Takeshita A., Egashira K., et al. Transforming growth factor-beta function blocking prevents myocardial fibrosis and diastolic dysfunction in pressure-overload rats. Circulation 2002, 106:130-135.
37. Stewart J.A., Massey E.P., Fix C., Zhu J., Goldsmith E.C., Carver W. Temporal alterations in cardiac fibroblast function following induction of pressure overload. Cell Tissue Res 2010, 340:117-126.
38. Goldsmith E.C., Bradshaw A.D., Spinale F.G. Cellular mechanisms of tissue fibrosis. 2. Contributory pathways leading to myocardial fibrosis: moving beyond collagen expression. Am J Physiol Cell Physiol 2013, 304:C393-C402.
39. Crawford J.R., Haudek S.B., Cieslik K.A., Trial J., Entman M.L. Origin of developmental precursors dictates the pathophysiologic role of cardiac fibroblasts. J Cardiovasc Transl Res 2012, 5:749-759.
40. Von Gise A., Pu W.T. Endocardial and epicardial epithelial to mesenchymal transitions in heart development and disease. Circ Res 2012, 110:1628-1645.
41. Carlson S., Trial J., Soeller C., Entman M.L. Cardiac mesenchymal stem cells contribute to scar formation after myocardial infarction. Cardiovasc Res 2011, 91:99-107.
42. Haudek S.B., Xia Y., Huebener P., Lee J.M., Carlson S., Crawford J.R., et al. Bone marrow-derived fibroblast precursors mediate ischemic cardiomyopathy in mice. Proc Natl Acad Sci 2006, 103:18284-18289.
43. Strutz F., Okada H., Lo C.W., Danoff T., Carone R.L., Tomaszewski J.E., et al. Identification and characterization of fibroblast marker: FSP1. J Cell Biol 1995, 130(2):393-405.
44. Okada H., Danoff T.M., Kalluri R., Neilson E.G. Early role of FSP1 in epithelial-mesenchymal transformation. Am J Physiol Renal Physiol 1997, 273:F563-F574.
45. Schneider M., Kostin S., Strom C.C., Aplin M., Lyngbaek S., Theilade J., et al. S100A4 is upregulated in injured myocardium and promotes growth and survival of cardiac myocytes. Cardiovasc Res 2007, 75:40-50.
46. Inamoto S., Murao S., Yokoyama M., Kitazawa S., Maeda S. Isoproterenol-induced myocardial injury resulting altered S100A4 and S100A11 protein expression in the rat. Pathol Int 2000, 50:480-485.
47. Bhowmick N.A., Chytil A., Plieth D., Gorska A.E., Dumont N., Shappell S., et al. TGF-b signaling in fibroblasts modulates the oncogenic potential of adjacent epithelia. Science 2004, 303:848-851.
48. Song K., Nam Y.J., Luo X., Qi X., Tan W., Huang G.N., et al. Heart repair by reprogramming non-myocytes with cardiac transcription factors. Nature 2012, 485:599-604.
49. Kong P., Christia P., Saxena A., Su Y., Frangogiannis N.G. Lack of specificity of fibroblast-specific protein 1 in cardiac remodeling and fibrosis. Am J Physiol Heart Circ Physiol 2013, 305:H1363-H1372.
50. Osterreicher C.H., Penz-Osterreicher M., Grivennikov S.I., Guma M., Koltsova E.K., Datz C., et al. Fibroblast-specific protein 1 identifies an inflammatory subpopulation of macrophages in the liver. Proc Natl Acad Sci 2001, 108:308-313.
51. Shrivastava A., Radziejewski C., Campbell E., Kovac L., McGlynn M., Ryan T.E., et al. An orphan receptor tyrosine kinase family whose members serve as nonintegrin collagen receptors. Mol Cell 1997, 1:25-34.
52. Vogel W., Gish G.D., Alves F., Pawson T. The Discoidin domain receptor tyrosine kinases are activated by collagen. Mol Cell 1997, 1:13-23.
53. Lai C., Lemke G. Structure and expression of the Tyro 10 receptor tyrosine kinase. Oncogene 1994, 9:877-883.
54. Lai C., Lemke G. An extended family of protein-tyrosine kinase genes differentially expressed in the vertebrate nervous system. Neuron 1991, 6:691-704.
55. Alves F., Vogel W., Mossie K., Millauer B., Hofler H., Ullrich A. Distinct structural characteristics of discoidin I subfamily receptor tyrosine kinases and complementary expression in human cancer. Oncogene 1995, 10:609-618.
56. Johnson J.D., Edman J.C., Rutter W.J. A receptor tyrosine kinase found in breast carcinoma cells has an extracellular discoidin I-like domain. Proc Natl Acad Sci 1993, 90:5677-5681.
57. Goldsmith E.C., Zhang X., Watson J., Hastings J., Potts J.D. The collagen receptor DDR2 is expressed during early cardiac development. Anat Rec 2010, 293:762-769.
58. Bhadriraju K., Chung K.H., Spurlin T.A., Haynes R.J., Elliott J.T., Plant A.L. The relative roles of collagen adhesive receptor DDR2 activation and matrix stiffness on the down-regulation of focal adhesion kinase in vascular smooth muscle cells. Biomaterials 2009, 30:6687-6694.
59. Ferri N., Carragher N.O., Raines E.W. Role of Discoidin domain receptors 1 and 2 in human smooth muscle cell-mediated collagen remodeling: potential implications in atherosclerosis and lymphangioleiomyomatosis. Am J Pathol 2004, 164:1575-1585.
60. Talasila A., Germack R., Dickenson J.M. Characterization of P2Y receptor subtypes functionally expressed on neonatal rat cardiac myofibroblasts. Br J Pharmacol 2009, 158:339-353.
61. Sun J., Li S.H., Liu S.M., Wu J., Weisel R.D., Zhuo Y.F., et al. Improvement in cardiac function after bone marrow cell therapy is associated with an increase in myocardial inflammation. Am J Physiol Heart Circ Physiol 2009, 296:H43-H50.
62. Squires C.E., Escobar G.P., Payne J.F., Leonardi R.A., Goshorn D.K., Sheats N.J., et al. Altered fibroblast function following myocardial infarction. J Mol Cell Cardiol 2005, 39:699-707.
63. Rossert J., Terraz C., Dupont S. Regulation of type I collagen gene expression. Nephrol Dial Transplant 2000, 15:66-68.
64. Rossert J., Eberspaecher H., de Crombrugghe B. Separate cis-acting DNA elements of the mouse pro-α1(I) collagen promoter direct expression of reporter genes to different type I collagen-producing cells in transgenic mice. J Cell Biol 1995, 129:1421-1432.
65. Ford C.M., Li S., Pickering J.G. Angiotensin II stimulates collagen synthesis in human vascular smooth muscle cells: involvement of the AT1 receptor, transforming growth factor β and tyrosine phosphorylation. Arterioscler Thromb Vasc Biol 1999, 19:1843-1851.
66. Schlumberger W., Thie M., Rauterberg J., Robenek H. Collagen synthesis in cultured aortic smooth muscle cells: modulation by collagen lattice culture, transforming growth factor-beta1 and epidermal growth factor. Arterioscler Thromb 1991, 11:1660-1666.
67. Zheng B., Zhang Z., Black C.M., de Brombrugghe B., Denton C.P. Ligand-dependent genetic recombination in fibroblasts: a potentially powerful technique for investigating gene function in fibrosis. Am J Pathol 2002, 160:1609-1617.
68. Cai C.L., Martin J.C., Sun Y., Cui L., Want L., Ouyang K., et al. A myocardial lineage derives from Tbx18 epicardial cells. Nature 2008, 454:104-109.
69. Duan J., Lee Y., Jania C., Gong J., Rojas M., Burk L., et al. Rib fractures and death from deletion of osteoblast βcatenin in adult mice is rescued by corticosteroids. PLoS One 2013, 8(2):e55757.
70. Evans R.M. Vimentin: the conundrum of the intermediate filament gene family. Bioessays 1998, 20:79-86.
71. Grigore A., Arsene D., Filipoiu F., Cionca F., Enache S., Ceausu M., et al. Cellular immunophenotypes in human embryonic, fetal and adult heart. Rom J Morphol Embryol 2012, 53:299-311.
72. Boopathy A.V., Pendergrass K.D., Che P.L., Yoon Y.S., Davis M.E. Oxidative stress-induced notch1 signaling promotes cardiogenic gene expression in mesenchymal stem cells. Stem Cell Res Ther 2013, 4:43.
73. Waxman A.S., Kornreich B.G., Gould R.A., Noise N.S., Butcher J.T. Interactions between TGFβ1 and cyclic strain in modulation of myofibroblastic differentiation of canine mitral valve interstitial cells in 3D culture. J Vet Cardiol 2012, 14:211-221.
74. Endo J., Sano M., Fujita J., Hayashida K., Yuasa S., Aoyama N., et al. Bone marrow-derived cells are involved in the pathogenesis of cardiac hypertrophy in response to pressure overload. Circulation 2007, 116:1176-1184.
75. Garin-Chesa P., Old L.J., Rettig W.J. Cell surface glycoprotein of reactive stromal fibroblasts as a potential antibody target in human epithelial cancers. Proc Natl Acad Sci 1990, 87:7235-7239.
76. Park J.E., Lenter M.C., Zimmermann R.N., Garin-Chesa P., Old L.J., Rettig W.J. Fibroblast activation protein, a dual specificity serine protease expressed in reactive human tumor stromal fibroblasts. J Biol Chem 1999, 274:36505-36512.
77. Rettig W.J., Garin-Chesa P., Beresford H.R., Oettgen H.F., Melamed M.R., Old L.J. Cell-surface glycoproteins of human sarcomas: differential expression in normal and malignant tissues and cultured cells. Proc Natl Acad Sci 1988, 85:3110-3114.
78. Levy M.T., McCaughan G.W., Abbott C.A., Park J.E., Cunningham A.M., Muller E., et al. Fibroblast activation protein: A cell surface dipeptidyl peptidase and gelatinase expressed by stellate cells at the tissue remodeling interface in human cirrhosis. Hepatology 1999, 29:1768-1778.
79. Acharya P.S., Zukas A., Zukas A., Chandan V., Katzenstein A.L.A., Pure E. Fibroblast activation protein: a serine protease expressed at the remodeling interface in idiopathic pulmonary fibrosis. Hum Pathol 2006, 37:352-360.
80. Brokopp C.E., Schoenauer R., Richards P., Bauer S., Lohmann C., Emmert M.Y., et al. Fibroblast activation protein is induced by inflammation and degrades type I collagen in thin-cap fibroatheromata. Eur Heart J 2001, 32:2713-2722.
81. Baum J., Duffy H.S. Fibroblasts and myofibroblasts: what are we talking about?. J Cardiovasc Pharmacol 2011, 57(4):376-379.
82. Porter K.E., Turner N.A. Cardiac fibroblasts: at the heart of myocardial remodeling. Pharmacol Ther 2009, 123:255-278.
83. Hinz B., Phan S.H., Thannickai V.J., Prunotto M., Desmouliere A., Varga J., et al. Recent developments in myofibroblast biology. Am J Pathol 2012, 180:1340-1355.
84. Gabbiani G. The myofibroblast in wound healing and fibrocontractive diseases. J Pathol 2003, 200:500-503.
85. Hinz B. Masters and servants of the force: the role of matrix adhesion in myofibroblast force perception and transmission. Eur J Cell Biol 2006, 85:175-181.
86. Tomasek J.J., Gabbiani G., Hinz B., Chaponnier C., Brown R.A. Myofibroblasts and mechano-regulation of connective tissue remodeling. Nat Rev Mol Cell Biol 2002, 3:349-363.
87. Ross R.S., Borg T.K. Integrins and the myocardium. Circ Res 2001, 88:1112-1119.
88. Hudon-David F., Bouzeghrane F., Couture P., Thibault G. Thy-1 expression by cardiac fibroblasts: lack of associate with myofibroblast contractile markers. J Mol Cell Cardiol 2007, 42:991-1000.
89. Talior-Volodarsky I., Connelly K.A., Arora P.D., Gullberg D., McCulloch C.A. α11 integrin stimulates myofibroblast differentiation in diabetic cardiomyopathy. Cardiovasc Res 2012, 96:265-275.
90. Carver W., Molano I., Reaves T.A., Borg T.K., Terracio L. Role of the alpha 1 beta 1 integrin complex in collagen gel contraction in vitro by fibroblasts. J Cell Physiol 1995, 165:425-437.
91. Wilson C.G., Stone J.W., Fowlkes V., Morales M.O., Murphy C.J., Baxter S.C., et al. Age-dependent expression of collagen receptors and deformation of type I collagen substrates by rat cardiac fibroblasts. Microsc Microanal 2011, 17:555-562.
92. Wipff P.J., Rifkin D.B., Meister J.J., Hinz B. Myofibroblast contraction activates latent TGF-b1 from the extracellular matrix. J Cell Biol 2007, 179:1311-1323.
93. Xu H., Bihan D., Chang F., Huang P.H., Farndale R.W., Leitinger B. Discoidin domain receptors promote α1β1- and α2β1-integrin mediated cell adhesion to collagen by enhancing integrin activation. PLoS One 2012, 7:e52209.
94. Xu H., Raynal N., Stathopoulos S., Myllyharju J., Farndale R.W., Leitinger B. Collagen binding specificity of the discoidin domain receptors: binding sites on collagens II and III and molecular determinants for collagen IV recognition by DDR1. Matrix Biol 2011, 30:16-26.
95. Konitsiotis A.D., Raynal N., Bihan D., Hohenester E., Farndale R.W., Leitinger B. Characterization of high affinity binding motifs for the Discoidin domain receptor DDR2 in collagen. J Biol Chem 2008, 283:6861-6868.
96. Hou G., Vogel W.F., Bendeck M.P. Tyrosine kinase activity of Discoidin domain receptor 1 is necessary for smooth muscle cell migration and matrix metalloproteinase expression. Circ Res 2002, 90:1147-1149.
97. Hou G., Vogel W., Bendeck M.P. The Discoidin domain receptor tyrosine kinase DDR1 in arterial wound repair. J Clin Invest 2001, 107:727-735.
98. Zhang P., Wang W., Wang X., Wang X., Song Y., Han Y., et al. Protein analysis of atrial fibrosis via label-free proteomics in chronic atrial fibrillation patients with mitral valve disease. PLoS One 2013, 8:e60210.
99. Spinale F.G., Zile M.R. Integrating the myocardial matrix into heart failure recognition and management. Circ Res 2013, 113:725-738.