Calcific nodule morphogenesis by heart valve interstitial cells is strain dependent

Biomechanics and Modeling in Mechanobiology

Volumn 12, Issue 1, 2013, Pages 5-17

  Fisher, Charles I ^a   Chen, Joseph ^a   Merryman, W David ^a  

^a VANDERBILT UNIVERSITY   (United States)

Author keywords

Aortic valve interstitial cell; Apoptosis; Calcific aortic valve disease; Dystrophic calcification; Mechanical strain; Mechanobiology; Myofibroblast; TGF 1; SMA

Indexed keywords

AGGREGATES; BIOMINERALIZATION; BLOOD VESSELS; MONOLAYERS; PROTEINS; VALVES (MECHANICAL);

AORTIC VALVE INTERSTITIAL CELL; AORTIC VALVES; CALCIFIC AORTIC VALVE DISEASE; DYSTROPHIC CALCIFICATION; MECHANICAL STRAIN; MECHANO-BIOLOGY; MYOFIBROBLASTS; TRANSFORMING GROWTH FACTOR-Β1; VALVE DISEASE; VALVE INTERSTITIAL CELLS; Α-SMOOTH MUSCLE ACTIN;

CELL DEATH;

TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL; AORTA DISEASE; AORTA VALVE; AORTA VALVE STENOSIS; ARTICLE; BIOLOGICAL MODEL; CALCINOSIS; COMPUTER SIMULATION; IN VITRO STUDY; MECHANICAL STRESS; MECHANOTRANSDUCTION; METABOLISM; MORPHOGENESIS; PATHOLOGY; PATHOPHYSIOLOGY; SWINE; TENSILE STRENGTH; YOUNG MODULUS;

ANIMALS; AORTIC DISEASES; AORTIC VALVE; AORTIC VALVE STENOSIS; CALCINOSIS; COMPUTER SIMULATION; ELASTIC MODULUS; MECHANOTRANSDUCTION, CELLULAR; MODELS, CARDIOVASCULAR; MORPHOGENESIS; STRESS, MECHANICAL; SWINE; TENSILE STRENGTH; TRANSFORMING GROWTH FACTOR BETA1;

MLCS; MLOWN;

EID: 84871762585     PISSN: 16177959     EISSN: 16177940     Source Type: Journal    
DOI: 10.1007/s10237-012-0377-8     Document Type: Article

References (49)

1. Balachandran K, Konduri S, Sucosky P, Jo H, Yoganathan AP (2006) An ex vivo study of the biological properties of porcine aortic valves in response to circumferential cyclic stretch. Ann Biomed Eng 34(11): 1655-1665. doi: 10.1007/s10439-006-9167-8
2. Balachandran K, Sucosky P, Jo H, Yoganathan AP (2009) Elevated cyclic stretch alters matrix remodeling in aortic valve cusps: implications for degenerative aortic valve disease. Am J Physiol Heart Circ Physiol 296(3): H756-H764. doi: 10.1152/ajpheart.00900.2008
3. Balachandran K, Sucosky P, Jo H, Yoganathan AP (2010) Elevated cyclic stretch induces aortic valve calcification in a bone morphogenic protein-dependent manner. Am J Pathol 177(1): 49-57. doi: 10.2353/ajpath.2010. 090631
4. Balestrini JL, Skorinko JK, Hera A, Gaudette GR, Billiar KL (2010) Applying controlled non-uniform deformation for in vitro studies of cell mechanobiology. Biomech Model Mechanobiol 9(3): 329-344. doi: 10.1007/s10237-009-0179-9
5. Benton JA, Kern HB, Anseth KS (2008) Substrate properties influence calcification in valvular interstitial cell culture. J Heart Valve Dis 17(6): 689-699
6. Benton JA, Kern HB, Leinwand LA, Mariner PD, Anseth KS (2009) Statins block calcific nodule formation of valvular interstitial cells by inhibiting alpha-smooth muscle actin expression. Arterioscler Thromb Vasc Biol 29(11): 1950-1957. doi: 10.1161/ATVBAHA.109.195271
7. Chen JH, Chen WL, Sider KL, Yip CY, Simmons CA beta-catenin mediates mechanically regulated, transforming growth factor-beta1-induced myofibroblast differentiation of aortic valve interstitial cells. Arterioscler Thromb Vasc Biol 31(3):590-597. doi: 10.1161/ATVBAHA.110.220061
8. Chen JH, Simmons CA (2011) Cell-matrix interactions in the pathobiology of calcific aortic valve disease: critical roles for matricellular, matricrine, and matrix mechanics cues. Circ Res 108(12): 1510-1524. doi: 10.1161/CIRCRESAHA.110.234237
9. Chen JH, Yip CY, Sone ED, Simmons CA (2009) Identification and characterization of aortic valve mesenchymal progenitor cells with robust osteogenic calcification potential. Am J Pathol 174(3): 1109-1119. doi: 10.2353/ajpath.2009.080750
10. Cushing MC, Liao JT, Anseth KS (2005) Activation of valvular interstitial cells is mediated by transforming growth factor-beta1 interactions with matrix molecules. Matrix Biol 24(6): 428-437
11. David G, Humphrey JD (2004) Redistribution of stress due to a circular hole in a nonlinear anisotropic membrane. J Biomech 37(8): 1197-1203. doi: 10.1016/j.jbiomech.2003.12.013
12. Follonier L, Schaub S, Meister JJ, Hinz B (2008) Myofibroblast communication is controlled by intercellular mechanical coupling. J Cell Sci 121(Pt 20): 3305-3316. doi: 10.1242/jcs.024521
13. Goffin JM, Pittet P, Csucs G, Lussi JW, Meister JJ, Hinz B (2006) Focal adhesion size controls tension-dependent recruitment of alpha-smooth muscle actin to stress fibers. J Cell Biol 172(2): 259-268. doi: 10.1083/jcb.200506179
14. Goldbarg SH, Elmariah S, Miller MA, Fuster V (2007) Insights into degenerative aortic valve disease. J Am Coll Cardiol 50(13): 1205-1213. doi: 10.1016/j.jacc.2007.06.024
15. Gu X, Masters KS (2009) Role of the MAPK/ERK pathway in valvular interstitial cell calcification. Am J Physiol Heart Circ Physiol 296(6): H1748-1757. doi: 10.1152/ajpheart.00099.2009
16. Gu X, Masters KS (2010) Regulation of valvular interstitial cell calcification by adhesive peptide sequences. J Biomed Mater Res A 93(4): 1620-1630. doi: 10.1002/jbm.a.32660
17. Gu X, Masters KS (2011) Role of the Rho pathway in regulating valvular interstitial cell phenotype and nodule formation. Am J Physiol Heart Circ Physiol 300(2): H448-H458. doi: 10.1152/ajpheart.01178.2009
18. Haskett D, Johnson G, Zhou A, Utzinger U, Vande Geest J (2010) Microstructural and biomechanical alterations of the human aorta as a function of age and location. Biomech Model Mechanobiol 9(6): 725-736. doi: 10.1007/s10237-010-0209-7
19. Helske S, Kupari M, Lindstedt KA, Kovanen PT (2007) Aortic valve stenosis: an active atheroinflammatory process. Curr Opin Lipidol 18(5): 483-491. doi: 10.1097/MOL.0b013e3282a66099
20. Hinz B, Mastrangelo D, Iselin CE, Chaponnier C, Gabbiani G (2001) Mechanical tension controls granulation tissue contractile activity and myofibroblast differentiation. Am J Pathol 159(3): 1009-1020. doi: 10.1016/S0002-9440(10)61776-2
21. Hinz B, Pittet P, Smith-Clerc J, Chaponnier C, Meister JJ (2004) Myofibroblast development is characterized by specific cell-cell adherens junctions. Mol Biol Cell 15(9): 4310-4320. doi: 10.1091/mbc.E04-05-0386
22. 2+) accumulation is strain-dependent and correlates with apoptosis in aortic valve fibroblasts. J Biomech doi: 10.1016/j.jbiomech. 2011.11.031
23. Jian B, Narula N, Li QY, Mohler ER, 3rd, Levy RJ (2003) Progression of aortic valve stenosis: TGF-beta1 is present in calcified aortic valve cusps and promotes aortic valve interstitial cell calcification calcification via apoptosis. Ann Thorac Surg 75(2):457-465; discussion 465-456
24. Kennedy JA, Hua X, Mishra K, Murphy GA, Rosenkranz AC, Horowitz JD (2009) Inhibition of calcifying nodule formation in cultured porcine aortic valve cells by nitric oxide donors. Eur J Pharmacol 602(1): 28-35. doi: 10.1016/j.ejphar.2008.11.029
25. Merryman WD (2008) What modulates the aortic valve interstitial cell phenotype?. Future Cardiol 4(3): 247-252. doi: 10.2217/14796678.4.3.247
26. Merryman WD (2009) Mechano-potential etiologies of aortic valve disease. J Biomech 43(1): 87-92. doi: 10.1016/j.jbiomech.2009.09.013
27. Merryman WD, Huang HY, Schoen FJ, Sacks MS (2006) The effects of cellular contraction on aortic valve leaflet flexural stiffness. J Biomech 39(1): 88-96. doi: 10.1016/j.jbiomech.2004.11.008
28. Merryman WD, Liao J, Parekh A, Candiello JE, Lin H, Sacks MS (2007) Differences in tissue-remodeling potential of aortic and pulmonary heart valve interstitial cells. Tissue Eng 13(9): 2281-2289. doi: 10.1089/ten.2006.0324
29. Merryman WD, Lukoff HD, Long RA, Engelmayr GC Jr., Hopkins RA, Sacks MS (2007) Synergistic effects of cyclic tension and transforming growth factor-beta1 on the aortic valve myofibroblast. Cardiovasc Pathol 16(5): 268-276. doi: 10.1016/j.carpath.2007.03.006
30. Merryman WD, Youn I, Lukoff HD, Krueger PM, Guilak F, Hopkins RA, Sacks MS (2006) Correlation between heart valve interstitial cell stiffness and transvalvular pressure: implications for collagen biosynthesis. Am J Physiol Heart Circ Physiol 290(1): H224-H231
31. Mohler ER 3rd, Chawla MK, Chang AW, Vyavahare N, Levy RJ, Graham L, Gannon FH (1999) Identification and characterization of calcifying valve cells from human and canine aortic valves. J Heart Valve Dis 8(3): 254-260
32. Mohler ER 3rd, Gannon F, Reynolds C, Zimmerman R, Keane MG, Kaplan FS (2001) Bone formation and inflammation in cardiac valves. Circulation 103(11): 1522-1528
33. Mori D, David G, Humphrey JD, Moore JE Jr. (2005) Stress distribution in a circular membrane with a central fixation. J Biomech Eng 127(3): 549-553
34. Piper C, Bergemann R, Schulte HD, Koerfer R, Horstkotte D (2003) Can progression of valvar aortic stenosis be predicted accurately?. Ann Thorac Surg 76(3):676-680; discussion 680
35. Pittet P, Lee K, Kulik AJ, Meister JJ, Hinz B (2008) Fibrogenic fibroblasts increase intercellular adhesion strength by reinforcing individual OB-cadherin bonds. J Cell Sci 121(Pt 6): 877-886. doi: 10.1242/jcs.024877
36. Rajamannan NM (2010) Mechanisms of aortic valve calcification: the LDL-density-radius theory: a translation from cell signaling to physiology. Am J Physiol Heart Circ Physiol 298(1): H5-H15. doi: 10.1152/ajpheart.00824.2009
37. Rajamannan NM, Evans FJ, Aikawa E, Grande-Allen KJ, Demer LL, Heistad DD, Simmons CA, Masters KS, Mathieu P, O'Brien KD, Schoen FJ, Towler DA, Yoganathan AP, Otto CM (2011) 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(16): 1783-1791. doi: 10.1161/CIRCULATIONAHA.110.006767
38. Robicsek F, Thubrikar MJ (2002) Mechanical stress as cause of aortic valve disease. Presentation of a new aortic root prosthesis. Acta Chir Belg 102(1): 1-6
39. Rodriguez KJ, Masters KS (2009) Regulation of valvular interstitial cell calcification by components of the extracellular matrix. J Biomed Mater Res A 90(4): 1043-1053. doi: 10.1002/jbm.a.32187
40. Roger VL, Go AS, Lloyd-Jones DM, Adams RJ, Berry JD, Brown TM, Carnethon MR, Dai S, de Simone G, Ford ES, Fox CS, Fullerton HJ, Gillespie C, Greenlund KJ, Hailpern SM, Heit JA, Ho PM, Howard VJ, Kissela BM, Kittner SJ, Lackland DT, Lichtman JH, Lisabeth LD, Makuc DM, Marcus GM, Marelli A, Matchar DB, McDermott MM, Meigs JB, Moy CS, Mozaffarian D, Mussolino ME, Nichol G, Paynter NP, Rosamond WD, Sorlie PD, Stafford RS, Turan TN, Turner MB, Wong ND, Wylie-Rosett J (2011) Heart disease and stroke statistics-2011 update: a report from the American Heart Association. Circulation 123(4): e18-e209. doi: 10.1161/CIR.0b013e3182009701
41. Simmons CA, Nikolovski J, Thornton AJ, Matlis S, Mooney DJ (2004) Mechanical stimulation and mitogen-activated protein kinase signaling independently regulate osteogenic differentiation and mineralization by calcifying vascular cells. J Biomech 37(10): 1531-1541. doi: 10.1016/j.jbiomech.2004.01.006
42. Tomasek JJ, Gabbiani G, Hinz B, Chaponnier C, Brown RA (2002) Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat Rev Mol Cell Biol 3(5): 349-363. doi: 10.1038/nrm809
43. Walker GA, Masters KS, Shah DN, Anseth KS, Leinwand LA (2004) Valvular myofibroblast activation by transforming growth factor-beta: implications for pathological extracellular matrix remodeling in heart valve disease. Circ Res 95(3): 253-260. doi: 10.1161/01.RES.0000136520.07995.aa
44. Weinberg EJ, Kaazempur Mofrad MR (2007) Transient, three-dimensional, multiscale simulations of the human aortic valve. Cardiovasc Eng 7(4): 140-155. doi: 10.1007/s10558-007-9038-4
45. Weinberg EJ, Mack PJ, Schoen FJ, Garcia-Cardena G, Kaazempur Mofrad MR (2010) Hemodynamic environments from opposing sides of human aortic valve leaflets evoke distinct endothelial phenotypes in vitro. Cardiovasc Eng 10(1): 5-11. doi: 10.1007/s10558-009-9089-9
46. Weinberg EJ, Schoen FJ, Mofrad MR (2009) A computational model of aging and calcification in the aortic heart valve. PLoS One 4(6): e5960. doi: 10.1371/journal.pone.0005960
47. Wipff PJ, Rifkin DB, Meister JJ, Hinz B (2007) Myofibroblast contraction activates latent TGF-β1 from the extracellular matrix. J Cell Biol 179(6): 1311-1323. doi: 10.1083/jcb.200704042
48. Yip CY, Chen JH, Zhao R, Simmons CA (2009) Calcification by valve interstitial cells is regulated by the stiffness of the extracellular matrix. Arterioscler Thromb Vasc Biol 29(6): 936-942. doi: 10.1161/ATVBAHA.108.182394
49. Yip CY, Simmons CA (2011) The aortic valve microenvironment and its role in calcific aortic valve disease. Cardiovasc Pathol 20(3): 177-182. doi: 10.1016/j.carpath.2010.12.001