The relationship between myocardial extracellular matrix remodeling and ventricular function

European Journal of Cardio-thoracic Surgery

Volumn 30, Issue 4, 2006, Pages 604-610

  Brower, Gregory L ^a   Gardner, Jason D ^a   Forman, Mary F ^a   Murray, David B ^a   Voloshenyuk, Tetyana ^a   Levick, Scott P ^a   Janicki, Joseph S ^a  

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

Author keywords

Collagen; Collagen types; Cross linking; Fibrosis; Hypertrophy; Myocardial remodeling

Indexed keywords

COLLAGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; COLLAGEN METABOLISM; CONTROLLED STUDY; CROSS LINKING; EXTRACELLULAR MATRIX; FIBROSIS; HEART HYPERTROPHY; HEART LEFT VENTRICLE MASS; HEART MUSCLE CELL; HEART MUSCLE FIBROSIS; HEART VENTRICLE FUNCTION; HEART VENTRICLE REMODELING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVIEW; SARCOMERE;

CARDIOMEGALY; EXTRACELLULAR MATRIX; FIBRILLAR COLLAGENS; FIBROSIS; HUMANS; MYOCARDIUM; VENTRICULAR DYSFUNCTION; VENTRICULAR FUNCTION; VENTRICULAR REMODELING;

EID: 33748292887     PISSN: 10107940     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejcts.2006.07.006     Document Type: Review

References (77)

1. Baicu C.F., Stroud J.D., Livesay V.A., Hapke E., Holder J., Spinale F.G., and Zile M.R. Changes in extracellular collagen matrix alter myocardial systolic performance. Am J Physiol Heart Circ Physiol 284 (2003) H122-H132
2. Janicki J.S., and Matsubara B.B. Myocardial collagen and left ventricular diastolic dysfunction. In: Gaasch W.H., and LeWinter M.M. (Eds). Left ventricular diastolic dysfunction (1993), Lea Febiger, Philadelphia 125-140
3. Bishop J.E., and Laurent G.J. Collagen turnover and its regulation in the normal and hypertrophying heart. Eur Heart J 16 Suppl. C (1995) 38-44
4. Mays P.K., Bishop J.E., and Laurent G.J. Age-related changes in the proportion of types I and III collagen. Mech Ageing Dev 45 (1988) 203-212
5. Medugorac I. Characterization of intramuscular collagen in the mammalian left ventricle. Basic Res Cardiol 77 (1982) 589-598
6. Mukherjee D., and Sen S. Collagen phenotypes during development and regression of myocardial hypertrophy in spontaneously hypertensive rats. Circ Res 67 (1990) 1474-1480
7. Mukherjee D., and Sen S. Alteration of collagen phenotypes in ischemic cardiomyopathy. J Clin Invest 88 (1991) 1141-1146
8. Mukherjee D., and Sen S. Alteration of cardiac collagen phenotypes in hypertensive hypertrophy: role of blood pressure. J Mol Cell Cardiol 25 (1993) 185-196
9. Weber K.T., Janicki J.S., Shroff S.G., Pick R., Chen R.M., and Bashey R.I. Collagen remodeling of the pressure-overloaded, hypertrophied nonhuman primate myocardium. Circ Res 62 (1988) 757-765
10. Borg T.K., and Caulfield J.B. The collagen matrix of the heart. Fed Proc 40 (1981) 2037-2041
11. Robinson T.F., Cohen-Gould L., and Factor S.M. Skeletal framework of mammalian heart muscle. Arrangement of inter- and pericellular connective tissue structures. Lab Invest 49 (1983) 482-498
12. Robinson T.F., Factor S.M., and Sonnenblick E.H. The heart as a suction pump. Sci Am 254 (1986) 84-91
13. Robinson T.F., Geraci M.A., Sonnenblick E.H., and Factor S.M. Coiled perimysial fibers of papillary muscle in rat heart: morphology, distribution, and changes in configuration. Circ Res 63 (1988) 577-592
14. Pearlman E.S., Weber K., Janicki J.S., Pietra G.G., and Fishman A.P. Muscle fiber orientation and connective tissue content in the hypertrophied human heart. Lab Invest 46 (1982) 158-164
15. MacKenna D.A., Omens J.H., and Covell J.W. Left ventricular perimysial collagen fibers uncoil rather than stretch during diastolic filling. Basic Res Cardiol 91 (1996) 111-122
16. Bing O.H.L., Matsushita S., Fanburg B.L., and Levine H.J. Mechanical properties of rat cardiac muscle during experimental hypertrophy. Circ Res 28 (1971) 234-245
17. Caulfield J.B., and Borg T.K. The collagen network of the heart. Lab Invest 40 (1979) 364-372
18. Jugdutt B.I. Extracellular matrix and cardiac remodeling. In: Villarreal F.J. (Ed). Interstitial fibrosis in heart failure (2005), Springer, New York 23-55
19. Narayan S., Janicki J.S., Shroff S.G., Pick R., and Weber K.T. Myocardial collagen and mechanics after preventing hypertrophy in hypertensive rats. Am J Hypertens 2 (1989) 675-682
20. Gelpi R.J., Pasipoularides A., Lader A.S., Patrick T.A., Chase N., Hittinger L., Shannon R.P., Bishop S.P., and Vatner S.F. Changes in diastolic cardiac function in developing and stable perinephritic hypertension in conscious dogs. Circ Res 68 (1991) 555-567
21. Douglas P.S., and Tallant B. Hypertrophy, fibrosis and diastolic dysfunction in early canine experimental hypertension. J Am Coll Cardiol 17 (1991) 530-536
22. MacFarlane N., Northridge D.B., Wright A.R., Grant S., and Dargie H.J. A comparative study of left ventricular structure and function in elite athletes. Br J Sports Med 25 (1991) 45-48
23. Nixon J.V., Wright A.R., Porter T.R., Roy V., and Arrowood J.A. Effects of exercise on left ventricular diastolic performance in trained athletes. Am J Cardiol 68 (1991) 945-949
24. Shapiro L.M., and McKenna W.J. Left ventricular hypertrophy. Relation of structure to diastolic function in hypertension. Br Heart J 51 (1984) 637-642
25. Szlachcic J., Tubau J.F., O'Kelly B., and Massie B.M. Correlates of diastolic filling abnormalities in hypertension: a doppler echocardiographic study. Am Heart J 120 (1991) 386-391
26. Woolley D.E. Mammalian collagenases. In: Piez K., and Reddi A.H. (Eds). Extracellular matrix biochemistry (1984), Elsevier, New York 119-158
27. Montfort I., and Pérez-Tamayo R. The distribution of collagenase in normal rat tissues. J Histochem Cytochem 23 (1975) 910-920
28. Tyagi S.C., Matsubara L., and Weber K.T. Direct extraction and estimation of collagenase(s) activity by zymography in microquantities of rat myocardium and uterus. Clin Biochem 26 (1993) 191-198
29. Woolley D.E., Tetlow L.C., and Evanson J.M. Collagenase immunolocalization studies of rheumatoid and malignant tissues. In: Woolley D.E., and Evanson J.M. (Eds). Collagenase in normal and pathological tissues (1978), John Wiley & Sons, New York 105-125
30. Takahashi S., Barry A.C., and Factor S.M. Collagen degradation in ischaemic rat hearts. Biochem J 265 (1990) 233-241
31. Charney R.H., Takahashi S., Zhao M., Sonnenblick E.H., and Eng C. Collagen loss in the stunned myocardium. Circulation 85 (1992) 1483-1490
32. Takahashi S., Geenen D., Nieves E., and Iwazumi T. Collagenase degrades collagen in vivo in the ischemic heart. Biochim Biophys Acta 1428 (1999) 251-259
33. Gunja-Smith Z., Morales A.R., Romanelli R., and Woessner Jr. J.F. Remodeling of human myocardial collagen in idiopathic dilated cardiomyopathy-role of metalloproteinases and pyridinoline cross-links. Am J Pathol 148 (1996) 1639-1648
34. Li Y.Y., Feldman A.M., Sun Y., and McTiernan C.F. Differential expression of tissue inhibitors of metalloproteinases in the failing human heart. Circulation 98 (1998) 1728-1734
35. Reddy H.K., Tjahja I.E., Campbell S.E., Janicki J.S., Hayden M.R., and Tyagi S.C. Expression of matrix metalloproteinase activity in idiopathic dilated cardiomyopathy: a marker of cardiac dilatation. Mol Cell Biochem 264 (2004) 183-191
36. Thomas C.V., Coker M.L., Zellner J.L., Handy J.R., Crumbley A.J., and Spinale F.G. Increased matrix metalloproteinase activity and selective upregulation in LV myocardium from patients with end-stage dilated cardiomyopathy. Circulation 97 (1998) 1708-1715
37. Janicki J.S. Collagen degradation in the heart. In: Eghbali-Webb M. (Ed). Molecular biology of collagen matrix in the heart (1995), R.G. Landes Company, Austin 61-75
38. Brower G.L., Henegar J.R., and Janicki J.S. Temporal evaluation of left ventricular remodeling and function in rats with chronic volume overload. Am J Physiol Heart Circ Physiol 271 (1996) H2071-H2078
39. Brower G.L., Chancey A.L., Thanigaraj S., Matsubara B.B., and Janicki J.S. Cause and effect relationship between myocardial mast cell number and matrix metalloproteinase activity. Am J Physiol Heart Circ Physiol 283 (2002) H518-H525
40. Chancey A.L., Brower G.L., Peterson J.T., and Janicki J.S. Effects of matrix metalloproteinase inhibition on ventricular remodeling due to volume overload. Circulation 105 (2002) 1983-1988
41. Peterson J.T., Hallak H., Johnson L., Li H., O'Brien P.M., Sliskovic D.R., Bocan T.M., Coker M.L., Etoh T., and Spinale F.G. Matrix metalloproteinase inhibition attenuates left ventricular remodeling and dysfunction in a rat model of progressive heart failure. Circulation 103 (2001) 2303-2309
42. Rohde L.E., Ducharme A., Arroyo L.H., AIkawa M., Sukhova G.H., Lopez-Anaya A., McClure K.F., Mitchell P.G., Libby P., and Lee R.T. Matrix metalloproteinase inhibition attenuates early left ventricular enlargement after experimental myocardial infarction in mice. Circulation 99 (1999) 3063-3070
43. Spinale F.G., Coker M.L., Krombach S.R., Mukherjee R., Hallak H., Houck W.V., Clair M.J., Kribbs S.B., Johnson L.L., Peterson J.T., and Zile M.R. Matrix metalloproteinase inhibition during the development of congestive heart failure: effects on left ventricular dimensions and function. Circ Res 85 (1999) 364-376
44. Burgess M.L., Buggy J., Price R.L., Abel F.L., Terracio L., Samarel A.M., and Borg T.K. Exercise- and hypertension-induced collagen changes are related to left ventricular function in rat hearts. Am J Physiol Heart Circ Physiol 270 (1996) H151-H159
45. Marijianowski M.M.H., Teeling P., Mann J., and Becker A.E. Dilated cardiomyopathy is associated with an increase in the type I/type III collagen ratio: a quantitative assessment. J Am Coll Cardiol 25 (1995) 1263-1272
46. Wei S., Chow L.T., Shum I.O., Qin L., and Sanderson J.E. Left and right ventricular collagen type I/III ratios and remodeling post-myocardial infarction. J Card Fail 5 (1999) 117-126
47. Shimizu M., Umeda K., Sugihara N., Yoshio H., Ino H., Takeda R., Okada Y., and Nakanishi I. Collagen remodelling in myocardia of patients with diabetes. J Clin Pathol 46 (1993) 32-36
48. Liu J., Masurekar M.R., Vatner D.E., Jyothirmayi G.N., Regan T.J., Vatner S.F., Meggs L.G., and Malhotra A. Glycation end-product cross-link breaker reduces collagen and improves cardiac function in aging diabetic heart. Am J Physiol Heart Circ Physiol 285 (2003) H2587-H2591
49. Linehan K.A., Seymour A.M., and Williams P.E. Semiquantitative analysis of collagen types in the hypertrophied left ventricle. J Anat 198 (1998) 83-92
50. Asif M., Egan J., Vasan S., Jyothirmayi G.N., Masurekar M.R., Lopez S., Williams C., Torres R.L., Wagle D., Ulrich P., Cerami A., Brines M., and Regan T.J. An advanced glycation endproduct cross-link breaker can reverse age-related increases in myocardial stiffness. Proc Natl Acad Sci 97 (2000) 2809-2813
51. Norton G.R., Tsotetsi J., Trifunovic B., Hartford C., Candy G.P., and Woodiwiss A.J. Myocardial stiffness is attributed to alterations in cross-linked collagen rather than total collagen or phenotypes in spontaneously hypertensive rats. Circulation 96 (1997) 1991-1998
52. Woodiwiss A.J., Tsotetsi O.J., Sprott S., Lancaster E.J., Mela T., Chung E.S., Meyer T.E., and Norton G.R. Reduction in myocardial collagen cross-linking parallels left ventricular dilatation in rat models of systolic chamber dysfunction. Circulation 103 (2001) 155-160
53. Iimoto D.S., Covell J.W., and Harper E. Increase in cross-linking of type I and type III collagens associated with volume-overload hypertrophy. Circ Res 63 (1988) 399-408
54. Herrmann K.L., McCulloch A.D., and Omens J.H. Glycated collagen cross-linking alters cardiac mechanics in volume-overload hypertrophy. Am J Physiol Heart Circ Physiol 284 (2003) H1277-H1284
55. Avendano G.F., Agarwal R.K., Bashey R.I., Lyons M.M., Soni B.J., Jyothirmayi G.N., and Regan T.J. Effects of glucose intolerance on myocardial function and collagen-linked glycation. Diabetes 48 (1999) 1443-1447
56. Susic D., Vargic J., and Ahn J.F.E.D. Crosslink breakers: a new approach to cardiovascular therapy. Curr Opin Cardiol 19 (2004) 336-340
57. Badenhorst D., Maseko M., Tsotetsi O.J., Naidoo A., Brooksbank R., Norton G.R., and Woodiwiss A.J. Cross-linking influences the impact of quantitative changes in myocardial collagen on cardiac stiffness and remodelling in hypertension in rats. Cardiovasc Res 57 (2003) 632-641
58. Lamberts R.R., Willemsen M.J.J.M.F., Perez N.G., Sipkema P., and Westerhof N. Acute and specific collagen type I degradation increases diastolic and developed tension in perfused rat papillary muscle. Am J Physiol Heart Circ Physiol 286 (2004) H889-H894
59. Murray D.B., Gardner J.D., Brower G.L., and Janicki J.S. Endothelin-1 mediates cardiac mast cell degranulation, matrix metalloproteinase activation and myocardial remodeling in rats. Am J Physiol Heart Circ Physiol 287 (2004) H2295-H2299
60. Chancey A.L., Brower G.L., and Janicki J.S. Cardiac mast cell-mediated activation of gelatinase and alteration of ventricular diastolic function. Am J Physiol Heart Circ Physiol 282 (2002) H2152-H2158
61. Heneghan M.A., Malone D., and Dervan P.A. Myocardial collagen network in dilated cardiomyopathy. Morphometry and scanning electron microscopy study. Ir J Med Sci 160 (1991) 399-401
62. Rossi M.A. Patterns of myocardial fibrosis in idiopathic cardiomyopathies and chronic chagasic cardiopathy. Can J Cardiol 7 (1991) 287-294
63. Schaper J., Froede R., Hein S., Buck A., Hashizume H., Speiser B., Friedl A., and Bleese N. Impairment of the myocardial ultrastructural and changes of the cytoskeleton in dialted cardiomyopathy. Circulation 83 (1991) 504-514
64. Burkhoff D., Klotz S., and Mancini D.M. LVAD-induced reverse remodeling: basic and clinical implications for myocardial recovery. J Card Fail 12 (2006) 227-239
65. Wohlschlaeger J., Schmitz K.J., Schmid C., Schmid K.W., Keul P., Takeda A., Weis S., Levkau B., and Baba H.A. Reverse remodeling following insertion of left ventricular assist devices (LVAD): a review of the morphological and molecular changes. Cardiovasc Res 68 (2005) 376-386
66. Mann D.L., and Willerson J.T. Left ventricular assist devices and the failing heart: a bridge to recovery, a permanent assist device, or a bridge too far?. Circulation 98 (1998) 2367-2369
67. Thompson L.O., Skrabal C.A., Loebe M., Lafuente J.A., Roberts R.R., Akgul A., Jones V., Bruckner B.A., Thohan V., Noon G.P., and Youker K.A. Plasma neurohormone levels correlate with left ventricular functional and morphological improvement in LVAD patients. J Surg Res 123 (2005) 25-32
68. Kucuker S.A., Stetson S.J., Becker K.A., Akgul A., Loebe M., Lafuente J.A., Noon G.P., Koerner M.M., Entman M.L., and Torre-Amione G. Evidence of improved right ventricular structure after LVAD support in patients with end-stage cardiomyopathy. J Heart Lung Transplant 23 (2004) 28-35
69. Bruckner B.A., Stetson S.J., Perez-Verdia A., Youker K.A., Radovancevic B., Connelly J.H., Koerner M.M., Entman M.E., Frazier O.H., Noon G.P., and Torre-Amione G. Regression of fibrosis and hypertrophy in failing myocardium following mechanical circulatory support. J Heart Lung Transplant 20 (2001) 457-464
70. Bruckner B.A., Stetson S.J., Farmer J.A., Radovancevic B., Frazier O.H., Noon G.P., Entman M.L., Torre-Amione G., and Youker K.A. The implications for cardiac recovery of left ventricular assist device support on myocardial collagen content. Am J Surg 180 (2000) 498-501
71. Thohan V., Stetson S.J., Nagueh S.F., Rivas-Gotz C., Koerner M.M., Lafuente J.A., Loebe M., Noon G.P., and Torre-Amione G. Cellular and hemodynamics responses of failing myocardium to continuous flow mechanical circulatory support using the DeBakey-Noon left ventricular assist device: a comparative analysis with pulsatile-type devices. J Heart Lung Transplant 24 (2005) 566-575
72. Klotz S., Foronjy R.F., Dickstein M.L., Gu A., Garrelds I.M., Danser J., Oz M., D'Armiento J., and Burkhoff D. Mechanical unloading during left ventricular assist device support increases left ventricular collagen cross-linking and myocardial stiffness. Circulation 112 (2005) 364-374
73. Barbone A., Holmes J.W., Heerdt P.M., The' A.H., Naka Y., Joshi N., Daines M., Marks A.R., Oz M.C., and Burkhoff D. Comparison of right and left ventricular responses to left ventricular assist device support in patients with severe heart failure: a primary role of mechanical unloading underlying reverse remodeling. Circulation 104 (2001) 670-675
74. Madigan J.D., Barbone A., Choudhri A.F., Morales D.L., Cai B., Oz M.C., and Burkhoff D. Time course of reverse remodeling of the left ventricle during support with a left ventricular assist device. J Thorac Cardiovasc Surg 121 (2001) 902-908
75. McCarthy P.M., Nakatani S., Vargo R., Kottke-Marchant K., Harasaki H., James K.B., Savage R.M., and Thomas J.D. Structural and left ventricular histologic changes after implantable LVAD insertion. Ann Thorac Surg 59 (1995) 609-613
76. Li Y.Y., Feng Y., McTiernan C.F., Pei W., Moravec C.S., Wang P., Rosenblum W., Kormos R.L., and Feldman A.M. Downregulation of matrix metalloproteinases and reduction in collagen damage in the failing human heart after support with left ventricular assist devices. Circulation 104 (2001) 1147-1152
77. Janicki J.S., Brower G.L., and Henegar J.R. Interstitial collagen remodeling in chronic heart failure. Basic Appl. Myology 5 (1995) 339-348