The progression of calcific aortic valve disease through injury, cell dysfunction, and disruptive biologic and physical force feedback loops

Cardiovascular Pathology

Volumn 22, Issue 1, 2013, Pages 1-8

  Li, Chen ^a   Xu, Songyi ^a   Gotlieb, Avrum I ^a  

^a UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

Calcific aortic valve disease; Matrix remodeling; Physical forces; Valve interstitial cell

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; BONE MORPHOGENETIC PROTEIN; COLLAGENASE 3; FIBROBLAST GROWTH FACTOR 2; GELATINASE A; INTERSTITIAL COLLAGENASE; PROLINE; TISSUE INHIBITOR OF METALLOPROTEINASE; TRANSCRIPTION FACTOR MSX1; TRANSCRIPTION FACTOR MSX2; TRANSCRIPTION FACTOR NFAT; TRANSCRIPTION FACTOR TWIST; TRANSFORMING GROWTH FACTOR BETA; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; AORTA VALVE STENOSIS; BONE DEVELOPMENT; CALCIFIC AORTIC VALVE DISEASE; CELL INTERACTION; CELL MIGRATION; CELL PROLIFERATION; CELL TRANSFORMATION; CHONDROGENESIS; DISEASE COURSE; EMBRYO DEVELOPMENT; ENCHONDRAL OSSIFICATION; FEEDBACK SYSTEM; FORCE; HISTOPATHOLOGY; HUMAN; HYPOTHESIS; IN VITRO STUDY; IN VIVO STUDY; MECHANOTRANSDUCTION; NONHUMAN; PATHOGENESIS; PHENOTYPE; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROMOTER REGION; REVIEW;

ANIMALS; AORTIC VALVE; AORTIC VALVE STENOSIS; BIOMECHANICS; CALCINOSIS; CELL MOVEMENT; CELL PROLIFERATION; CHONDROGENESIS; DISEASE PROGRESSION; EXTRACELLULAR MATRIX; FEEDBACK; HEMODYNAMICS; HUMANS; INFLAMMATION MEDIATORS; MECHANOTRANSDUCTION, CELLULAR; NEOVASCULARIZATION, PATHOLOGIC; OSTEOGENESIS; PHENOTYPE; SEVERITY OF ILLNESS INDEX; STRESS, MECHANICAL;

EID: 84870878926     PISSN: 10548807     EISSN: 18791336     Source Type: Journal    
DOI: 10.1016/j.carpath.2012.06.005     Document Type: Review

References (77)

1. A.C. Liu, V.R. Joag, and A.I. Gotlieb The emerging role of valve interstitial cell phenotypes in regulating heart valve pathobiology Am J Pathol 171 2007 1407 1418 (Pubitemid 350158303)
2. M.H. Yacoub, P.J. Kilner, E.J. Birks, and M. Misfeld The aortic outflow and root: a tale of dynamism and crosstalk Ann Thorac Surg 68 1999 S37 S43
3. C.A. Simmons, G.R. Grant, E. Manduchi, and P.F. Davies Spatial heterogeneity of endothelial phenotypes correlates with side-specific vulnerability to calcification in normal porcine aortic valves Circ Res 96 2005 792 799 (Pubitemid 40559519)
4. R.B. Hinton Jr., J. Lincoln, G.H. Deutsch, H. Osinska, P.B. Manning, and D.W. Benson Extracellular matrix remodeling and organization in developing and diseased aortic valves Circ Res 98 2006 1431 1438 (Pubitemid 43948068)
5. E.H. Stephens, J. Shangkuan, J.J. Kuo, J.L. Carroll, D.L. Kearney, and K.E. Carberry Extracellular matrix remodeling and cell phenotypic changes in dysplastic and hemodynamically altered semilunar human cardiac valves Cardiovasc Pathol 20 2011 e157 e167
6. F.J. Schoen Evolving concepts of cardiac valve dynamics: the continuum of development, functional structure, pathobiology, and tissue engineering Circulation 118 2008 1864 1880
7. E. Aikawa, P. Whittaker, M. Farber, K. Mendelson, R.F. Padera, and M. Aikawa Human semilunar cardiac valve remodeling by activated cells from fetus to adult: implications for postnatal adaptation, pathology, and tissue engineering Circulation 113 2006 1344 1352 (Pubitemid 43739456)
8. B.F. Stewart, D. Siscovick, B.K. Lind, J.M. Gardin, J.S. Gottdiener, and V.E. Smith Clinical factors associated with calcific aortic valve disease. Cardiovascular Health Study J Am Coll Cardiol 29 1997 630 634 (Pubitemid 27116107)
9. C.M. Otto, I.G. Burwash, M.E. Legget, B.I. Munt, M. Fujioka, and N.L. Healy Prospective study of asymptomatic valvular aortic stenosis. Clinical, echocardiographic, and exercise predictors of outcome Circulation 95 1997 2262 2270 (Pubitemid 27191003)
10. K.D. O'Brien Pathogenesis of calcific aortic valve disease: a disease process comes of age (and a good deal more) Arterioscler Thromb Vasc Biol 26 2006 1721 1728 (Pubitemid 44305324)
11. C. Napoli, and F. Cacciatore Novel pathogenic insights in the primary prevention of cardiovascular disease Prog Cardiovasc Dis 51 2009 503 523
12. S.J. Cowell, D.E. Newby, R.J. Prescott, P. Bloomfield, J. Reid, and D.B. Northridge A randomized trial of intensive lipid-lowering therapy in calcific aortic stenosis N Engl J Med 352 2005 2389 2397 (Pubitemid 40958435)
13. N.M. Rajamannan, M. Subramaniam, M. Springett, T.C. Sebo, M. Niekrasz, and J.P. McConnell Atorvastatin inhibits hypercholesterolemia-induced cellular proliferation and bone matrix production in the rabbit aortic valve Circulation 105 2002 2660 2665 (Pubitemid 34596044)
14. A.B. Rossebo, T.R. Pedersen, K. Boman, P. Brudi, J.B. Chambers, and K. Egstrup Intensive lipid lowering with simvastatin and ezetimibe in aortic stenosis N Engl J Med 359 2008 1343 1356
15. G. Kaleschke, and H. Baumgartner Asymptomatic aortic stenosis: when to operate? Curr Cardiol Rep 13 2011 220 225
16. B.A. Carabello, and W.J. Paulus Aortic stenosis Lancet 373 2009 956 966
17. J. Rodes-Cabau Transcatheter aortic valve implantation: current and future approaches Nat Rev Cardiol 9 2012 15 29
18. J. Butany, and A.I. Gotlieb Native valvular heart disease B.M. McManus, Atlas of cardiovascular pathology for the clinician ed 2 2001 Current Medicine Inc. Philadelphia 201 215
19. M.C. Drolet, E. Roussel, Y. Deshaies, J. Couet, and M. Arsenault A high fat/high carbohydrate diet induces aortic valve disease in C57BL/6J mice J Am Coll Cardiol 47 2006 850 855 (Pubitemid 43243111)
20. K. Tanaka, M. Sata, D. Fukuda, Y. Suematsu, N. Motomura, and S. Takamoto Age-associated aortic stenosis in apolipoprotein E-deficient mice J Am Coll Cardiol 46 2005 134 141 (Pubitemid 40905141)
21. R.M. Weiss, M. Ohashi, J.D. Miller, S.G. Young, and D.D. Heistad Calcific aortic valve stenosis in old hypercholesterolemic mice Circulation 114 2006 2065 2069 (Pubitemid 44706883)
22. A.D. Durbin, and A.I. Gotlieb Advances towards understanding heart valve response to injury Cardiovasc Pathol 11 2002 69 77 (Pubitemid 34273661)
23. W.M. Lester, and A.I. Gotlieb In vitro repair of the wounded porcine mitral valve Circ Res 62 1988 833 845
24. N.M. Rajamannan, F.J. Evans, E. Aikawa, K.J. Grande-Allen, L.L. Demer, and D.D. Heistad Calcific aortic valve disease: not simply a degenerative process: a review and agenda for research from the National Heart and Lung and Blood Institute Aortic Stenosis Working Group. Executive summary: calcific aortic valve disease - 2011 update Circulation 124 2011 1783 1791
25. M.D. Combs, and K.E. Yutzey Heart valve development: regulatory networks in development and disease Circ Res 105 2009 408 421
26. R.B. Hinton, and K.E. Yutzey Heart valve structure and function in development and disease Annu Rev Physiol 73 2011 29 46
27. R.R. Markwald, R.A. Norris, R. Moreno-Rodriguez, and R.A. Levine Developmental basis of adult cardiovascular diseases: valvular heart diseases Ann N Y Acad Sci 1188 2010 177 183
28. B. Hinz The myofibroblast: paradigm for a mechanically active cell J Biomech 43 2010 146 155
29. F.J. Schoen Mechanisms of function and disease of natural and replacement heart valves Annu Rev Pathol 2012 161 183
30. D.L. Mulholland, and A.I. Gotlieb Cell biology of valvular interstitial cells Can J Cardiol 12 1996 231 236 (Pubitemid 26097855)
31. B. Hinz, S.H. Phan, V.J. Thannickal, M. Prunotto, A. Desmouliere, and J. Varga Recent developments in myofibroblast biology: paradigms for connective tissue remodeling Am J Pathol 180 2012 1340 1355
32. N.W. Shworak Angiogenic modulators in valve development and disease: does valvular disease recapitulate developmental signaling pathways? Curr Opin Cardiol 19 2004 140 146 (Pubitemid 38373128)
33. Z. Hajdu, S.J. Romeo, P.A. Fleming, R.R. Markwald, R.P. Visconti, and C.J. Drake Recruitment of bone marrow-derived valve interstitial cells is a normal homeostatic process J Mol Cell Cardiol 51 2011 955 965
34. N.M. Rajamannan Calcific aortic valve disease: cellular origins of valve calcification Arterioscler Thromb Vasc Biol 31 2011 2777 2778
35. H.V. Leskela, J. Satta, J. Oiva, H. Eriksen, R. Juha, and P. Korkiamaki Calcification and cellularity in human aortic heart valve tissue determine the differentiation of bone-marrow-derived cells J Mol Cell Cardiol 41 2006 642 649 (Pubitemid 44374546)
36. R.P. Visconti, Y. Ebihara, A.C. LaRue, P.A. Fleming, T.C. McQuinn, and M. Masuya An in vivo analysis of hematopoietic stem cell potential: hematopoietic origin of cardiac valve interstitial cells Circ Res 98 2006 690 696
37. E.E. Wirrig, R.B. Hinton, and K.E. Yutzey Differential expression of cartilage and bone-related proteins in pediatric and adult diseased aortic valves J Mol Cell Cardiol 50 2011 561 569
38. P.J. Schneider, and J.D. Deck Tissue and cell renewal in the natural aortic-valve of rats - an autoradiographic study Cardiovasc Res 15 1981 181 189 (Pubitemid 11107405)
39. I.E.M.G. Willems, M.G. Havenith, J.F.M. Smits, and M.J.A.P. Daemen Structural alterations in heart-valves during left-ventricular pressure-overload in the rat Lab Invest 71 1994 127 133 (Pubitemid 24246029)
40. S. Chakraborty, M.D. Combs, and K.E. Yutzey Transcriptional regulation of heart valve progenitor cells Pediatr Cardiol 31 2010 414 421
41. E.E. Wirrig, and K.E. Yutzey Transcriptional regulation of heart valve development and disease Cardiovasc Pathol 20 2011 162 167
42. S. Chakraborty, E.E. Wirrig, R.B. Hinton, W.H. Merrill, D.B. Spicer, and K.E. Yutzey Twist1 promotes heart valve cell proliferation and extracellular matrix gene expression during development in vivo and is expressed in human diseased aortic valves Dev Biol 347 2010 167 179
43. Y.H. Chen, M. Ishii, H.M. Sucov, and R.E. Maxson Jr. Msx1 and Msx2 are required for endothelial-mesenchymal transformation of the atrioventricular cushions and patterning of the atrioventricular myocardium BMC Dev Biol 8 2008 75
44. T.L. Blevins, S.B. Peterson, E.L. Lee, A.M. Bailey, J.D. Frederick, and T.N. Huynh Mitral valvular interstitial cells demonstrate regional, adhesional, and synthetic heterogeneity Cells Tissues Organs 187 2008 113 122 (Pubitemid 351252946)
45. M.W. Chan, B. Hinz, and C.A. McCulloch Mechanical induction of gene expression in connective tissue cells Methods Cell Biol 98 2010 178 205
46. K. Balachandran, M.A. Bakay, J.M. Connolly, X. Zhang, A.P. Yoganathan, and R.J. Levy Aortic valve cyclic stretch causes increased remodeling activity and enhanced serotonin receptor responsiveness Ann Thorac Surg 92 2011 147 153
47. J.T. Butcher, and R.M. Nerem Valvular endothelial cells regulate the phenotype of interstitial cells in co-culture: effects of steady shear stress Tissue Eng 12 2006 905 915 (Pubitemid 43726531)
48. J.T. Butcher, C.A. Simmons, and J.N. Warnock Mechanobiology of the aortic heart valve J Heart Valve Dis 17 2008 62 73
49. A.C. Liu, and A.I. Gotlieb Transforming growth factor-beta regulates in vitro heart valve repair by activated valve interstitial cells Am J Pathol 173 2008 1275 1285
50. G.A. Walker, K.S. Masters, D.N. Shah, K.S. Anseth, and L.A. Leinwand Valvular myofibroblast activation by transforming growth factor-beta: implications for pathological extracellular matrix remodeling in heart valve disease Circ Res 95 2004 253 260 (Pubitemid 39056285)
51. A.V. Villar, M. Cobo, M. Llano, C. Montalvo, F. Gonzalez-Vilchez, and R. Martin-Duran Plasma levels of transforming growth factor-beta1 reflect left ventricular remodeling in aortic stenosis PLoS One 4 2009 e8476
52. C. Li, and A.I. Gotlieb Transforming growth factor-beta regulates the growth of valve interstitial cells in vitro Am J Pathol 179 2011 1746 1755
53. M. Laiho, J.A. DeCaprio, J.W. Ludlow, D.M. Livingston, and J. Massague Growth inhibition by TGF-beta linked to suppression of retinoblastoma protein phosphorylation Cell 62 1990 175 185
54. A. Moustakas, K. Pardali, A. Gaal, and C.H. Heldin Mechanisms of TGF-beta signaling in regulation of cell growth and differentiation Immunol Lett 82 2002 85 91 (Pubitemid 34468039)
55. C.H. Heldin, M. Landstrom, and A. Moustakas Mechanism of TGF-beta signaling to growth arrest, apoptosis, and epithelial-mesenchymal transition Curr Opin Cell Biol 21 2009 166 176
56. R.A. Rahimi, and E.B. Leof TGF-beta signaling: a tale of two responses J Cell Biochem 102 2007 593 608 (Pubitemid 47557414)
57. Han L and Gotlieb AI. Fibroblast growth factor-2 promotes in vitro heart valve interstitial cell repair through the Akt1 pathway. Cardiovasc Pathol [Epub ahead of print] 2012.
58. S.E. New, and E. Aikawa Molecular imaging insights into early inflammatory stages of arterial and aortic valve calcification Circ Res 108 2011 1381 1391
59. C.M. Otto, J. Kuusisto, D.D. Reichenbach, A.M. Gown, and K.D. O'Brien Characterization of the early lesion of 'degenerative' valvular aortic stenosis. Histological and immunohistochemical studies Circulation 90 1994 844 853 (Pubitemid 24242754)
60. G.J. Mahler, and J.T. Butcher Inflammatory regulation of valvular remodeling: the good(?), the bad, and the ugly Int J Inflam 2011 2011 721419
61. J.H. Lee, X. Meng, M.J. Weyant, T.B. Reece, J.C. Cleveland Jr., and D.A. Fullerton Stenotic aortic valves have dysfunctional mechanisms of anti-inflammation: implications for aortic stenosis J Thorac Cardiovasc Surg 141 2011 481 486
62. K.D. O'Brien, D.M. Shavelle, M.T. Caulfield, T.O. McDonald, K. Olin-Lewis, and C.M. Otto Association of angiotensin-converting enzyme with low-density lipoprotein in aortic valvular lesions and in human plasma Circulation 106 2002 2224 2230 (Pubitemid 35222217)
63. Z. Yu, K. Seya, K. Daitoku, S. Motomura, I. Fukuda, and K. Furukawa Tumor necrosis factor-alpha accelerates the calcification of human aortic valve interstitial cells obtained from patients with calcific aortic valve stenosis via the BMP2-Dlx5 pathway J Pharmacol Exp Ther 337 2011 16 23
64. M. Yoshioka, S. Yuasa, K. Matsumura, K. Kimura, T. Shiomi, and N. Kimura Chondromodulin-I maintains cardiac valvular function by preventing angiogenesis Nat Med 12 2006 1151 1159 (Pubitemid 44527350)
65. Y. Soini, T. Salo, and J. Satta Angiogenesis is involved in the pathogenesis of nonrheumatic aortic valve stenosis Hum Pathol 34 2003 756 763 (Pubitemid 37040610)
66. F. Chalajour, H. Treede, A. Ebrahimnejad, H. Lauke, H. Reichenspurner, and S. Ergun Angiogenic activation of valvular endothelial cells in aortic valve stenosis Exp Cell Res 298 2004 455 464 (Pubitemid 38950862)
67. I. El-Hamamsy, K. Balachandran, M.H. Yacoub, L.M. Stevens, P. Sarathchandra, and P.M. Taylor Endothelium-dependent regulation of the mechanical properties of aortic valve cusps J Am Coll Cardiol 53 2009 1448 1455
68. A. Mammoto, and D.E. Ingber Cytoskeletal control of growth and cell fate switching Curr Opin Cell Biol 21 2009 864 870
69. W.D. Merryman, H.D. Lukoff, R.A. Long, G.C. Engelmayr Jr., R.A. Hopkins, and M.S. Sacks Synergistic effects of cyclic tension and transforming growth factor-beta1 on the aortic valve myofibroblast Cardiovasc Pathol 16 2007 268 276 (Pubitemid 47375116)
70. K. Akat, M. Borggrefe, and J.J. Kaden Aortic valve calcification: basic science to clinical practice Heart 95 2009 616 623
71. O. Fondard, D. Detaint, B. Iung, C. Choqueux, H. Adle-Biassette, and M. Jarraya Extracellular matrix remodelling in human aortic valve disease: the role of matrix metalloproteinases and their tissue inhibitors Eur Heart J 26 2005 1333 1341 (Pubitemid 41435466)
72. E.R. Mohler 3rd, F. Gannon, C. Reynolds, R. Zimmerman, M.G. Keane, and F.S. Kaplan Bone formation and inflammation in cardiac valves Circulation 103 2001 1522 1528 (Pubitemid 32226259)
73. J.N. Clark-Greuel, J.M. Connolly, E. Sorichillo, N.R. Narula, H.S. Rapoport, and E.R. Mohler 3rd Transforming growth factor-beta1 mechanisms in aortic valve calcification: increased alkaline phosphatase and related events Ann Thorac Surg 83 2007 946 953 (Pubitemid 46328821)
74. H. Zhou, W. Mak, Y. Zheng, C.R. Dunstan, and M.J. Seibel Osteoblasts directly control lineage commitment of mesenchymal progenitor cells through Wnt signaling J Biol Chem 283 2008 1936 1945
75. N.M. Rajamannan, M. Subramaniam, D. Rickard, S.R. Stock, J. Donovan, and M. Springett Human aortic valve calcification is associated with an osteoblast phenotype Circulation 107 2003 2181 2184 (Pubitemid 36547209)
76. K. Wyss, C.Y. Yip, Z. Mirzaei, X. Jin, J.H. Chen, and C.A. Simmons The elastic properties of valve interstitial cells undergoing pathological differentiation J Biomech 45 2012 882 887
77. E. Beckmann, J.B. Grau, R. Sainger, P. Poggio, and G. Ferrari Insights into the use of biomarkers in calcific aortic valve disease J Heart Valve Dis 19 2010 441 452