How to make a heart valve: From embryonic development to bioengineering of living valve substitutes

Cold Spring Harbor Perspectives in Medicine

Volumn 4, Issue 11, 2014, Pages

  Macgrogan, Donal ^a   Luxán, Guillermo ^a   Driessen Mol, Anita ^b   Bouten, Carlijn ^b   Baaijens, Frank ^b   De La Pompa, José Luis ^a  

^a CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

^b EINDHOVEN UNIVERSITY OF TECHNOLOGY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BIOENGINEERING; BIOMECHANICS; CELL FUNCTION; CELL FUSION; CELL LINEAGE; CELL STRUCTURE; CELLS BY BODY ANATOMY; EMBRYO DEVELOPMENT; ENDOCARDIAL CUSHION; ENDOTHELIUM CELL; EPITHELIAL MESENCHYMAL TRANSITION; EXTRACELLULAR MATRIX; HEART ATRIOVENTRICULAR VALVE; HEART ATRIUM REMODELING; HEART DEVELOPMENT; HEART FUNCTION; HEART VALVE; HUMAN; IN VITRO STUDY; MORPHOGENESIS; TISSUE ENGINEERING; TISSUE SCAFFOLD; ANATOMY AND HISTOLOGY; ANIMAL; CYTOLOGY; EMBRYOLOGY; HEART VALVE PROSTHESIS; PHYSIOLOGY;

ANIMALS; EXTRACELLULAR MATRIX; HEART VALVE PROSTHESIS; HEART VALVES; HUMANS; MORPHOGENESIS; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84923862552     PISSN: None     EISSN: 21571422     Source Type: Journal    
DOI: 10.1101/cshperspect.a013912     Document Type: Article

References (203)

1. Abu-Issa R, Kirby ML. 2007. Heart field: From mesoderm to heart tube. Annu Rev Cell Dev Biol 23: 45-68.
2. Aikawa E, Whittaker P, Farber M, Mendelson K, Padera RF, Aikawa M, Schoen FJ. 2006. Human semilunar cardiac valve remodeling by activated cells from fetus to adult: Implications for postnatal adaptation, pathology, and tissue engineering. Circulation 113: 1344-1352.
3. Akiyama H, Chaboissier MC, Behringer RR, Rowitch DH, Schedl A, Epstein JA, de Crombrugghe B. 2004. Essential role of Sox9 in the pathway that controls formation of cardiac valves and septa. Proc Natl Acad Sci 101: 6502-6507.
4. Alfieri CM, Cheek J, Chakraborty S, Yutzey KE. 2010. Wnt signaling in heart valve development and osteogenic gene induction. Dev Biol 338: 127-135.
5. Anderson RH, Webb S, Brown NA, Lamers W, Moorman A. 2003. Development of the heart: (3) Formation of the ventricular outflow tracts, arterial valves, and intrapericardial arterial trunks. Heart 89: 1110-1118.
6. Armstrong EJ, Bischoff J. 2004. Heart valve development: Endothelial cell signaling and differentiation. Circ Res 95: 459-470.
7. Badylak SF, Gilbert TW. 2008. Immune response to biologic scaffold materials. Semin Immunol 20: 109-116.
8. 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. AmJ Physiol Heart Circ Physiol 296: H756-H764.
9. Balguid A, Rubbens MP, Mol A, Bank RA, Bogers AJ, van Kats JP, de Mol BA, Baaijens FP, Bouten CV. 2007. The role of collagen cross-links in biomechanical behavior of human aortic heart valve leaflets—Relevance for tissue engineering. Tissue Eng 13: 1501-1511.
10. Bischoff J, Aikawa E. 2011. Progenitor cells confer plasticity to cardiac valve endothelium. J Cardiovasc Transl Res 4: 710-719.
11. Bloch O, Golde P, Dohmen PM, Posner S, Konertz W, Erdbrugger W. 2011. Immune response in patients receiving a bioprosthetic heart valve: Lack of response with decellularized valves. Tissue Eng Part A 17: 2399-2405.
12. Bouten CV, Dankers PY, Driessen-Mol A, Pedron S, Brizard AM, Baaijens FP. 2011. Substrates for cardiovascular tissue engineering. Adv Drug Deliv Rev 63: 221-241.
13. Bouten CV, Driessen-Mol A, Baaijens FP. 2012. In situ heart valve tissue engineering: Simple devices, smart materials, complex knowledge. Exp Rev Med Devices 9: 453-455.
14. Brand T. 2003. Heart development: Molecular insights into cardiac specification and early morphogenesis. Dev Biol 258: 1-19.
15. Buckingham M, Meilhac S, Zaffran S. 2005. Building the mammalian heart from two sources of myocardial cells. Nat Rev Genet 6: 826-835.
16. Butcher JT, Markwald RR. 2007. Valvulogenesis: The moving target. Philos Trans R Soc Lond B Biol Sci 362: 1489-1503.
17. Butcher JT, Nerem RM. 2004. Porcine aortic valve interstitial cells in three-dimensional culture: Comparison of phenotype with aortic smooth muscle cells. J Heart Valve Dis 13: 485-476.
18. Butcher JT, Nerem RM. 2006. Valvular endothelial cells regulate the phenotype of interstitial cells in co-culture: Effects of steady shear stress. Tissue Eng 12: 905-915.
19. Cai CL, Liang X, Shi Y, Chu PH, Pfaff SL, Chen J, Evans S. 2003. Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Dev Cell 5: 877-889.
20. Camenisch TD, Schroeder JA, Bradley J, Klewer SE, McDonald JA. 2002. Heart-valve mesenchyme formation is dependent on hyaluronan-augmented activation of ErbB2-ErbB3 receptors. Nat Med 8: 850-855.
21. Cebotari S, Lichtenberg A, Tudorache I, Hilfiker A, Mertsching H, Leyh R, Breymann T, Kallenbach K, Maniuc L, Batrinac A, et al. 2006. Clinical application of tissue engineered human heart valves using autologous progenitor cells. Circulation 114: I132-I137.
22. Cebotari S, Tudorache I, Ciubotaru A, Boethig D, Sarikouch S, Goerler A, Lichtenberg A, Cheptanaru E, Barnaciuc S, Cazacu A, et al. 2011.Use of fresh decellularized allografts for pulmonary valve replacement may reduce the reoperation rate in children and young adults: Early report. Circulation 124: S115-S123.
23. Chakraborty S, Cheek J, Sakthivel B, Aronow BJ, Yutzey KE. 2008. Shared gene expression profiles in developing heart valves and osteoblast progenitor cells. Physiol Genomics 35: 75-85.
24. Chakraborty S, Wirrig EE, Hinton RB, Merrill WH, Spicer DB, Yutzey KE. 2010. 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: 167-179.
25. Chang CP, Neilson JR, Bayle JH, Gestwicki JE, Kuo A, Stankunas K, Graef IA, Crabtree GR. 2004. A field of myocardial-endocardial NFAT signaling underlies heart valve morphogenesis. Cell 118: 649-663.
26. Cheek JD, Wirrig EE, Alfieri CM, James JF, Yutzey KE. 2012. Differential activation of valvulogenic, chondrogenic, and osteogenic pathways in mouse models of myxomatous and calcific aortic valve disease. J Mol Cell Cardiol 52: 689-700.
27. 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: 1510-1524.
28. Combs MD, Yutzey KE. 2009. Heart valve development: Regulatory networks in development and disease. Circ Res 105: 408-421.
29. Courtney T, Sacks MS, Stankus J, Guan J, Wagner WR. 2006. Design and analysis of tissue engineering scaffolds that mimic soft tissue mechanical anisotropy. Biomaterials 27: 3631-3638.
30. Cox MA, Kortsmit J, Driessen N, Bouten CV, Baaijens FP. 2010. Tissue-engineered heart valves develop native-like collagen fiber architecture. Tissue Eng Part A 16: 1527-1537.
31. de Lange FJ, Moorman AF, Anderson RH, Manner J, Soufan AT, Gier-de Vries C, Schneider MD, Webb S, van den Hoff MJ, Christoffels VM. 2004. Lineage and morphogenetic analysis of the cardiac valves. Circ Res 95: 645-654.
32. de la Pompa JL, Epstein JA. 2012. Coordinating tissue interactions: Notch signaling in cardiac development and disease. Dev Cell 22: 244-254.
33. de la Pompa JL, Timmerman LA, Takimoto H, Yoshida H, Elia AJ, Samper E, Potter J, Wakeham A, Marengere L, Langille BL, et al. 1998. Role of the NF-ATc transcription factor in morphogenesis of cardiac valves and septum. Nature 392: 182-186.
34. DelMonte G, Grego-Bessa J, Gonzalez-Rajal A, Bolos V, De La Pompa JL. 2007.Monitoring Notch1 activity in development: Evidence for a feedback regulatory loop. Dev Dyn 236: 2594-2614.
35. De Visscher G, Vranken I, Lebacq A, Van Kerrebroeck C, Ganame J, Verbeken E, Flameng W. 2007. In vivo cellularization of a cross-linked matrix by intraperitoneal implantation: A new tool in heart valve tissue engineering. Eur Heart J 28: 1389-1396.
36. De Visscher G, Lebacq A, Mesure L, Blockx H, Vranken I, Plusquin R, Meuris B, Herregods MC, Van Oosterwyck H, Flameng W. 2010. The remodeling of cardiovascular bioprostheses under influence of stem cell homing signal pathways. Biomaterials 31: 20-28.
37. de Vlaming A, Sauls K, Hajdu Z, Visconti RP, Mehesz AN, Levine RA, Slaugenhaupt SA, Hagege A, Chester AH, Markwald RR, et al. 2012. Atrioventricular valve development: New perspectives on an old theme. Differentiation 84: 103-116.
38. Dijkman PE, Driessen-Mol A, Frese L, Hoerstrup SP, Baaijens FP. 2012. Decellularized homologous tissue-engineered heart valves as off-the-shelf alternatives to xenoand homografts. Biomaterials 33: 4545-4554.
39. Dor Y, Camenisch TD, Itin A, Fishman GI, McDonald JA, Carmeliet P, Keshet E. 2001. A novel role for VEGF in endocardialcushionformationanditspotential contribution to congenital heart defects. Development 128: 1531-1538.
40. Dyer LA, Kirby ML. 2009. The role of secondary heart field in cardiac development. Dev Biol 336: 137-144.
41. Egorova AD, Khedoe PP, Goumans MJ, Yoder BK, Nauli SM, ten Dijke P, Poelmann RE, Hierck BP. 2011. Lack of primary cilia primes shear-induced endothelial-to-mesenchymal transition. Circ Res 108: 1093-1101.
42. Eisenberg LM, Markwald RR. 1995. Molecular regulation of atrioventricular valvuloseptal morphogenesis. Circ Res 77: 1-6.
43. El-Hamamsy I, Balachandran K, Yacoub MH, Stevens LM, Sarathchandra P, Taylor PM, Yoganathan AP, Chester AH. 2009. Endothelium-dependent regulation of the mechanical properties of aortic valve cusps. J Am Coll Cardiol 53: 1448-1455.
44. El-Hamamsy I, Eryigit Z, Stevens LM, Sarang Z, George R, Clark L, Melina G, Takkenberg JJ, Yacoub MH. 2010. Long-term outcomes after autograft versus homograft aortic root replacement in adults with aortic valve disease: Arandomised controlled trial. Lancet 376: 524-531.
45. Elkins RC, Goldstein S, Hewitt CW, Walsh SP, Dawson PE, Ollerenshaw JD, Black KS, Clarke DR, O’Brien MF. 2001. Recellularization of heart valve grafts by a process of adaptive remodeling. Semin Thorac Cardiovasc Surg 13: 87-92.
46. Engleka KA, Manderfield LJ, Brust RD, Li L, Cohen A, Dymecki SM, Epstein JA. 2012. Islet1 derivatives in the heart are of both neural crest and second heart field origin. Circ Res 110: 922-926.
47. Erdbrugger W, Konertz W, Dohmen PM, Posner S, Ellerbrok H, Brodde OE, Robenek H, Modersohn D, Pruss A, Holinski S, et al. 2006. Decellularized xenogenic heart valves reveal remodeling and growth potential in vivo. Tissue Eng 12: 2059-2068.
48. Fernandez B, Duran AC, Fernandez-Gallego T, Fernandez MC, Such M, Arque JM, Sans-Coma V. 2009. Bicuspid aortic valves with different spatial orientations of the leaflets are distinct etiological entities. J Am Coll Cardiol 54: 2312-2318.
49. Flanagan TC, Sachweh JS, Frese J, Schnoring H, Gronloh N, Koch S, Tolba RH, Schmitz-Rode T, Jockenhoevel S. 2009. In vivo remodeling and structural characterization of fibrin-based tissue-engineered heart valves in the adult sheep model. Tissue Eng Part A 15: 2965-2976.
50. Fondard O, Detaint D, Iung B, Choqueux C, Adle-Biassette H, Jarraya M, Hvass U, Couetil JP, Henin D, Michel JB, et al. 2005. Extracellular matrix remodelling in human aortic valve disease: The role ofmatrix metalloproteinases and their tissue inhibitors. Eur Heart J 26: 1333-1341.
51. Garg V, Muth AN, Ransom JF, Schluterman MK, Barnes R, King IN, Grossfeld PD, Srivastava D. 2005. Mutations in NOTCH1 cause aortic valve disease. Nature 437: 270-274.
52. Gaussin V, Morley GE, Cox L, Zwijsen A, Vance KM, Emile L, Tian Y, Liu J, Hong C, Myers D, et al. 2005. Alk3/Bmpr1a receptor is required for development of the atrioventricular canal into valves and annulus fibrosus. Circ Res 97: 219-226.
53. Gessert S, Kuhl M. 2010. The multiple phases and faces of wnt signaling during cardiac differentiation and development. Circ Res 107: 186-199.
54. Gitler AD, Zhu Y, Ismat FA, Lu MM, Yamauchi Y, Parada LF, Epstein JA. 2003. Nf1 has an essential role in endothelial cells. Nat Genet 33: 75-79.
55. Gittenberger-de Groot AC, Vrancken Peeters MP, Mentink MM, Gourdie RG, Poelmann RE. 1998. Epicardium-derived cells contribute a novel population to the myocardial wall and the atrioventricular cushions. Circ Res 82: 1043-1052.
56. Goldstein S, Clarke DR, Walsh SP, Black KS, O’Brien MF. 2000. Transpecies heart valve transplant: Advanced studies of a bioengineered xeno-autograft. Ann Thorac Surg 70: 1962-1969.
57. Gottlieb D, Kunal T, Emani S, Aikawa E, Brown DW, Powell AJ, Nedder A, Engelmayr GC Jr, Melero-Martin JM, Sacks MS, et al. 2010. In vivo monitoring of function of autologous engineered pulmonary valve. J Thorac Cardiovasc Surg 139: 723-731.
58. Gupta V, Grande-Allen KJ. 2006. Effects of static and cyclic loading in regulating extracellular matrix synthesis by cardiovascular cells. Cardiovasc Res 72: 375-383.
59. Gupta V, Barzilla JE, Mendez JS, Stephens EH, Lee EL, Collard CD, Laucirica R, Weigel PH, Grande-Allen KJ. 2009a. Abundance and location of proteoglycans and hyaluronan within normal and myxomatous mitral valves. Cardiovasc Pathol 18: 191-197.
60. Gupta V, Tseng H, Lawrence BD, Grande-Allen KJ. 2009b. Effect of cyclic mechanical strain on glycosaminoglycan and proteoglycan synthesis by heart valve cells. Acta Biomater 5: 531-540.
61. Guy TS, Hill AC. 2012. Mitral valve prolapse. Annu RevMed 63: 277-292.
62. Hajdu Z, Romeo SJ, Fleming PA, Markwald RR, Visconti RP, Drake CJ. 2011. Recruitment of bone marrow-derived valve interstitial cells is a normal homeostatic process. J Mol Cell Cardiol 51: 955-965.
63. Harvey RP. 2002. Patterning the vertebrate heart. Nat Rev Genet 3: 544-556.
64. Hashi CK, Zhu Y, Yang GY, Young WL, Hsiao BS, Wang K, Chu B, Li S. 2007. Antithrombogenic property of bone marrow mesenchymal stem cells in nanofibrous vascular grafts. Proc Natl Acad Sci 104: 11915-11920.
65. Hay DA, Low FN. 1972. The fusion of dorsal and ventral endocardial cushions in the embryonic chick heart: A study in fine structure. Am J Anat 133: 1-23.
66. Hayashida K, Kanda K, Yaku H, Ando J, Nakayama Y. 2007. Development of an in vivo tissue-engineered, autologous heart valve (the biovalve): Preparation of a prototype model. J Thorac Cardiovasc Surg 134: 152-159.
67. Hibino N, Yi T, Duncan DR, Rathore A, Dean E, Naito Y, Dardik A, Kyriakides T, Madri J, Pober JS, et al. 2011. A critical role for macrophages in neovessel formation and the development of stenosis in tissue-engineered vascular grafts. FASEB J 25: 4253-4263.
68. Hiemann NE, Mani M, Huebler M, Meyer R, Hetzer R, Thieme R, Bethge C. 2010. Complete destruction of a tissue-engineered porcine xenograft in pulmonary valve position after the Ross procedure. J Thorac Cardiovasc Surg 139: e67-e68.
69. Hinton RB, Yutzey KE. 2011. Heart valve structure and function in development and disease. Annu Rev Physiol 73: 29-46.
70. Hinton RB Jr, Lincoln J, Deutsch GH, Osinska H, Manning PB, Benson DW, Yutzey KE. 2006. Extracellular matrix remodeling and organization in developing and diseased aortic valves. Circ Res 98: 1431-1438.
71. Hoerstrup SP, Sodian R, Daebritz S, Wang J, Bacha EA, Martin DP, Moran AM, Guleserian KJ, Sperling JS, Kaushal S, et al. 2000. Functional living trileaflet heart valves grown in vitro. Circulation 102: III44-III49.
72. Hoerstrup SP, Kadner A, Melnitchouk S, Trojan A, Eid K, Tracy J, Sodian R, Visjager JF, Kolb SA, Grunenfelder J, et al. 2002. Tissue engineering of functional trileaflet heart valves from human marrow stromal cells. Circulation 106: I143-I150.
73. Human P, Zilla P. 2001. The possible role of immune responses in bioprosthetic heart valve failure. J Heart Valve Dis 10: 460-466.
74. Hurle JM. 1979. Scanning and light microscope studies of the development of the chick embryo semilunar heart valves. Anat Embryol (Berl) 157: 69-80.
75. Hurle JM, Colvee E, Blanco AM. 1980. Development of mouse semilunar valves. Anat Embryol (Berl) 160: 83-91.
76. Hutson MR, Kirby ML. 2007. Model systems for the study of heart development and disease. Cardiac neural crest and conotruncal malformations. Semin Cell Dev Biol 18: 101-110.
77. Iop L, Renier V, Naso F, Piccoli M, Bonetti A, Gandaglia A, Pozzobon M, Paolin A, Ortolani F, Marchini M, et al. 2009. The influence of heart valve leaflet matrix characteristics on the interaction between human mesenchymal stem cells and decellularized scaffolds. Biomaterials 30: 4104-4116.
78. Iwamoto R, Mekada E. 2006. ErbB and HB-EGF signaling in heart development and function. Cell Struct Funct 31: 1-14.
79. Iwamoto R, Yamazaki S, Asakura M, Takashima S, Hasuwa H, Miyado K, Adachi S, Kitakaze M, Hashimoto K, Raab G, et al. 2003. Heparin-binding EGF-like growth factor and ErbB signaling is essential for heart function. Proc Natl Acad Sci 100: 3221-3226.
80. Jackson LF, Qiu TH, Sunnarborg SW, Chang A, Zhang C, Patterson C, Lee DC. 2003. Defective valvulogenesis in HB-EGF and TACE-null mice is associated with aberrant BMP signaling. EMBO J 22: 2704-2716.
81. Jain R, Engleka KA, Rentschler SL, Manderfield LJ, Li L, Yuan L, Epstein JA. 2011. Cardiac neural crest orchestrates remodeling and functional maturation of mouse semilunar valves. J Clin Invest 121: 422-430.
82. Jiang X, Rowitch DH, Soriano P, McMahon AP, Sucov HM. 2000. Fate of the mammalian cardiac neural crest. Development 127: 1607-1616.
83. Joziasse IC, van de Smagt JJ, Smith K, Bakkers J, Sieswerda GJ, Mulder BJ, Doevendans PA. 2008. Genes in congenital heart disease: Atrioventricular valve formation. Basic Res Cardiol 103: 216-227.
84. Kelly RG, Buckingham ME. 2002. The anterior heart-forming field: Voyage to the arterial pole of the heart. Trends Genet 18: 210-216.
85. Kern CB, Twal WO, Mjaatvedt CH, Fairey SE, Toole BP, Iruela-Arispe ML, Argraves WS. 2006. Proteolytic cleavage of versican during cardiac cushion morphogenesis. Dev Dyn 235: 2238-2247.
86. Kokubo H, Tomita-Miyagawa S, Hamada Y, Saga Y. 2007. Hesr1 and Hesr2 regulate atrioventricular boundary formation in the developing heart through the repression of Tbx2. Development 134: 747-755.
87. Kortsmit J, Driessen NJ, Rutten MC, Baaijens FP. 2009. Real time, non-invasive assessment of leaflet deformation in heart valve tissue engineering. Ann Biomed Eng 37: 532-541.
88. Krenz M, Yutzey KE, Robbins J. 2005. Noonan syndrome mutation Q79R in Shp2 increases proliferation of valve primordia mesenchymal cells via extracellular signal-regulated kinase 1/2 signaling. Circ Res 97: 813-820.
89. Kruithof BP, Krawitz SA, Gaussin V. 2007. Atrioventricular valve development during late embryonic and postnatal stages involves condensation and extracellular matrix remodeling. Dev Biol 302: 208-217.
90. Kruithof BP, Duim SN, Moerkamp AT, Goumans MJ. 2012. TGF-b and BMP signaling in cardiac cushion formation: Lessons from mice and chicken. Differentiation 84: 89-102.
91. Ku CH, Johnson PH, Batten P, Sarathchandra P, Chambers RC, Taylor PM, Yacoub MH, Chester AH. 2006. Collagen synthesis by mesenchymal stem cells and aortic valve interstitial cells in response to mechanical stretch. Cardiovasc Res 71: 548-556.
92. Lamers WH, Viragh S, Wessels A, Moorman AF, Anderson RH. 1995. Formation of the tricuspid valve in the human heart. Circulation 91: 111-121.
93. Lange AW, Yutzey KE. 2006. NFATc1 expression in the developing heart valves is responsive to the RANKL pathway and is required for endocardial expression of cathepsin K. Dev Biol 292: 407-417.
94. Latif N, Sarathchandra P, Taylor PM, Antoniw J, Yacoub MH. 2005. Localization and pattern of expression of extracellular matrix components in human heart valves. J Heart Valve Dis 14: 218-227.
95. Latif N, Sarathchandra P, Thomas PS, Antoniw J, Batten P, Chester AH, Taylor PM, Yacoub MH. 2007. Characterization of structural and signaling molecules by human valve interstitial cells and comparison to human mesenchymal stem cells. J Heart Valve Dis 16: 56-66.
96. Leask RL, Jain N, Butany J. 2003. Endothelium and valvular diseases of the heart. Microsc Res Tech 60: 129-137.
97. Lencinas A, Tavares AL, Barnett JV, Runyan RB. 2011. Collagen gel analysis of epithelial-mesenchymal transition in the embryo heart: An in vitro model system for the analysis of tissue interaction, signal transduction, and environmental effects. Birth Defects Res C Embryo Today 93: 298-311.
98. Lepage L, Krapf L, Hekimian G, Duval X, Nataf P, Hvass U, Vahanian A, Messika-Zeitoun D. 2012. Unusual presentation of cryolife O’Brien stentless aortic valve bioprosthesis dysfunction mimicking infective endocarditis. Eur J Cardiothorac Surg 41: 800-805.
99. Levay AK, Peacock JD, Lu Y, Koch M, Hinton RB Jr, Kadler KE, Lincoln J. 2008. Scleraxis is required for cell lineage differentiation and extracellular matrix remodeling during murine heart valve formation in vivo. Circ Res 103: 948-956.
100. Leyh RG, Wilhelmi M, Rebe P, Fischer S, Kofidis T, Haverich A, Mertsching H. 2003. In vivo repopulation of xenogeneic and allogeneic acellular valve matrix conduits in the pulmonary circulation. Ann Thorac Surg 75: 1457-1463;discussion 1463.
101. Lie-Venema H, van den Akker NM, Bax NA, Winter EM, Maas S, Kekarainen T, Hoeben RC, deRuiter MC, Poelmann RE, Gittenberger-de Groot AC. 2007. Origin, fate, and function of epicardium-derived cells (EPDCs) in normal and abnormal cardiac development. Scientific World Journal 7: 1777-1798.
102. Lim J, Thiery JP. 2012. Epithelial-mesenchymal transitions: Insights from development. Development 139: 3471-3486.
103. Lin CJ, Lin CY, Chen CH, Zhou B, Chang CP. 2012. Partitioning the heart: Mechanisms of cardiac septation and valve development. Development 139: 3277-3299.
104. Lincoln J, Alfieri CM, Yutzey KE. 2004. Development of heart valve leaflets and supporting apparatus in chicken and mouse embryos. Dev Dyn 230: 239-250.
105. Lincoln J, Alfieri CM, Yutzey KE. 2006a. BMP and FGF regulatory pathways control cell lineage diversification of heart valve precursor cells. Dev Biol 292: 292-302.
106. Lincoln J, Lange AW, Yutzey KE. 2006b. Hearts and bones: Shared regulatory mechanisms in heart valve, cartilage, tendon, and bone development. Dev Biol 294: 292-302.
107. Lincoln J, Kist R, Scherer G, Yutzey KE. 2007. Sox9 is required for precursor cell expansion and extracellular matrix organization during mouse heart valve development. Dev Biol 305: 120-132.
108. Liu AC, Gotlieb AI. 2007. Characterization of cell motility in single heart valve interstitial cells in vitro. Histol Histopathol 22: 873-882.
109. Lockhart M, Wirrig E, Phelps A, Wessels A. 2011. Extracellular matrix and heart development. Birth Defects Res A Clin Mol Teratol 91: 535-550.
110. Luna-Zurita L, Prados B, Grego-Bessa J, Luxan G, delMonte G, Benguria A, Adams RH, Perez-Pomares JM, dela Pompa JL. 2010. Integration of a Notch-dependent mesenchymal gene program and Bmp2-driven cell invasiveness regulates murine cardiac valve formation. J Clin Invest 120: 3493-3507.
111. Ma L, Lu MF, Schwartz RJ, Martin JF. 2005. Bmp2 is essential for cardiac cushion epithelial-mesenchymal transition and myocardial patterning. Development 132: 5601-5611.
112. Manner J. 2009. The anatomy of cardiac looping: A step towards the understanding of the morphogenesis of several forms of congenital cardiac malformations. Clin Anat 22: 21-35.
113. Maron BJ, Hutchins GM. 1974. The development of the semilunar valves in the human heart. Am J Pathol 74: 331-344.
114. Martin LJ, Ramachandran V, Cripe LH, Hinton RB, Andelfinger G, Tabangin M, Shooner K, Keddache M, Benson DW. 2007. Evidence in favor of linkage to human chromosomal regions 18q, 5q and 13q for bicuspid aortic valve and associated cardiovascular malformations. Hum Genet 121: 275-284.
115. 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. AmJ Physiol Heart Circ Physiol 290: H224-H231.
116. Miller DV, Edwards WD, Zehr KJ. 2006. Endothelial and smooth muscle cell populations in a decellularized cryopreserved aortic homograft (SynerGraft) 2 years after implantation. J Thorac Cardiovasc Surg 132: 175-176.
117. Mirza A, Hyvelin JM, Rochefort GY, Lermusiaux P, Antier D, Awede B, Bonnet P, Domenech J, Eder V. 2008. Undifferentiated mesenchymal stem cells seeded on a vascular prosthesis contribute to the restoration of a physiologic vascular wall. J Vasc Surg 47: 1313-1321.
118. Mol A, Driessen NJ, Rutten MC, Hoerstrup SP, Bouten CV, Baaijens FP. 2005a. Tissue engineering of human heart valve leaflets: A novel bioreactor for a strain-based conditioning approach. Ann Biomed Eng 33: 1778-1788.
119. Mol A, van Lieshout MI, Dam-de Veen CG, Neuenschwander S, Hoerstrup SP, Baaijens FP, Bouten CV. 2005b. Fibrin as a cell carrier in cardiovascular tissue engineering applications. Biomaterials 26: 3113-3121.
120. Mol A, Rutten MC, Driessen NJ, Bouten CV, Zund G, Baaijens FP, Hoerstrup SP. 2006. Autologous human tissueengineered heart valves: Prospects for systemic application. Circulation 114: I152-I158.
121. Nakamura T, Colbert MC, Robbins J. 2006.Neural crest cells retain multipotential characteristics in the developing valves and label the cardiac conduction system. Circ Res 98: 1547-1554.
122. Neidert MR, Tranquillo RT. 2006. Tissue-engineered valves with commissural alignment. Tissue Eng 12: 891-903.
123. Niessen K, Fu Y, Chang L, Hoodless PA, McFadden D, Karsan A. 2008. Slug is a direct Notch target required for initiation of cardiac cushion cellularization. J Cell Biol 182: 315-325.
124. Norris RA, Moreno-Rodriguez RA, Sugi Y, Hoffman S, Amos J, Hart MM, Potts JD, Goodwin RL, Markwald RR. 2008. Periostin regulates atrioventricular valve maturation. Dev Biol 316: 200-213.
125. Norris RA, Moreno-Rodriguez R, Hoffman S, Markwald RR. 2009. The many facets of the matricelluar protein periostin during cardiac development, remodeling, and pathophysiology. J Cell Commun Signal 3: 275-286.
126. Peacock JD, Lu Y, Koch M, Kadler KE, Lincoln J. 2008. Temporal and spatial expression of collagens during murine atrioventricular heart valve development and maintenance. Dev Dyn 237: 3051-3058.
127. Person AD, Klewer SE, Runyan RB. 2005. Cell biology of cardiaccushion development. IntRevCytol 243:287-335.
128. Pittenger MF, Martin BJ. 2004.Mesenchymal stem cells and their potential as cardiac therapeutics. Circ Res 95: 9-20.
129. Poelmann RE, Gittenberger-de Groot AC. 2005. Apoptosis as an instrument in cardiovascular development. Birth Defects Res C Embryo Today 75: 305-313.
130. Prodromo J, D’Ancona G, Amaducci A, Pilato M. 2012. Aortic valve repair for aortic insufficiency: A review. J Cardiothorac Vasc Anesth 26: 923-932.
131. Rabkin E, Aikawa M, Stone JR, Fukumoto Y, Libby P, Schoen FJ. 2001. Activated interstitialmyofibroblasts express catabolic enzymes and mediate matrix remodeling in myxomatous heart valves. Circulation 104: 2525-2532.
132. Rabkin-Aikawa E, Farber M, Aikawa M, Schoen FJ. 2004. Dynamic and reversible changes of interstitial cell phenotype during remodeling of cardiac valves. J Heart Valve Dis 13: 841-847.
133. Ranger AM, Grusby MJ, Hodge MR, Gravallese EM, dela Brousse FC, Hoey T, Mickanin C, Baldwin HS, Glimcher LH. 1998. The transcription factor NF-ATc is essential for cardiac valve formation. Nature 392: 186-190.
134. Rieder E, Seebacher G, Kasimir MT, Eichmair E, Winter B, Dekan B, Wolner E, Simon P, Weigel G. 2005. Tissue engineering of heart valves: Decellularized porcine and human valve scaffolds differ importantly in residual potential to attractmonocytic cells. Circulation 111: 2792-2797.
135. Riem Vis PW, Kluin J, Sluijter JP, van Herwerden LA, Bouten CV. 2011. Environmental regulation of valvulogenesis: Implications for tissue engineering. Eur J Cardiothorac Surg 39: 8-17.
136. Rivera-Feliciano J, Lee KH, Kong SW, Rajagopal S, Ma Q, Springer Z, Izumo S, Tabin CJ, Pu WT. 2006. Development of heart valves requires Gata4 expression in endothelial-derived cells. Development 133: 3607-3618.
137. Rodgers LS, Lalani S, Hardy KM, Xiang X, Broka D, Antin PB, Camenisch TD. 2006. Depolymerized hyaluronan induces vascular endothelial growth factor, a negative regulator of developmental epithelial-to-mesenchymal transformation. Circ Res 99: 583-589.
138. Roh JD, Sawh-Martinez R, Brennan MP, Jay SM, Devine L, Rao DA, Yi T, Mirensky TL, Nalbandian A, Udelsman B, et al. 2010. Tissue-engineered vascular grafts transform into mature blood vessels via an inflammation-mediated process of vascular remodeling. Proc Natl Acad Sci 107: 4669-4674.
139. Romano LA, Runyan RB. 1999. Slug is a mediator of epithelial-mesenchymal cell transformation in the developing chicken heart. Dev Biol 212: 243-254.
140. Rubbens MP, Driessen-Mol A, Boerboom RA, Koppert MM, van Assen HC, TerHaar Romeny BM, Baaijens FP, Bouten CV. 2009. Quantification of the temporal evolution of collagen orientation in mechanically conditioned engineered cardiovascular tissues. Ann Biomed Eng 37: 1263-1272.
141. Ruffer A, Purbojo A, Cicha I, Glockler M, Potapov S, Dittrich S, Cesnjevar RA. 2010. Early failure of xenogenous de-cellularised pulmonary valve conduits—A word of caution! Eur J Cardiothorac Surg 38: 78-85.
142. Sacks MS, Yoganathan AP. 2007. Heart valve function: A biomechanical perspective. Philos Trans R Soc Lond B Biol Sci 362: 1369-1391.
143. Sales VL, Engelmayr GC Jr, Johnson JA Jr, Gao J, Wang Y, Sacks MS, Mayer JE Jr. 2007. Protein precoating of elastomeric tissue-engineering scaffolds increased cellularity, enhanced extracellular matrix protein production, and differentially regulated the phenotypes of circulating endothelial progenitor cells. Circulation 116: I55-63.
144. Sales VL, Mettler BA, Engelmayr GC Jr, Aikawa E, Bischoff J, Martin DP, Exarhopoulos A, Moses MA, Schoen FJ, Sacks MS, et al. 2010. Endothelial progenitor cells as a sole source for ex vivo seeding of tissue-engineered heart valves. Tissue Eng Part A 16: 257-267.
145. Sanchez-Soria P, Camenisch TD. 2010. ErbB signaling in cardiac development and disease. Semin Cell Dev Biol 21: 929-935.
146. Sander EA, Barocas VH, Tranquillo RT. 2011. Initial fiber alignment pattern alters extracellular matrix synthesis in fibroblast-populated fibrin gel cruciforms and correlates with predicted tension. Ann Biomed Eng 39: 714-729.
147. Sayk F, Bos I, Schubert U, Wedel T, Sievers HH. 2005. Histopathologic findings in a novel decellularized pulmonary homograft: An autopsy study. Ann Thorac Surg 79: 1755-1758.
148. Scherz PJ, Huisken J, Sahai-Hernandez P, Stainier DYR. 2008. High-speed imaging of developing heart valves reveals interplay of morphogenesis and function. Development 135: 1179-1187.
149. Schmidt D, Achermann J, Odermatt B, Breymann C, Mol A, Genoni M, Zund G, Hoerstrup SP. 2007. Prenatally fabricated autologous human living heart valves based on amniotic fluid derived progenitor cells as single cell source. Circulation 116: I64-I70.
150. Schmidt D, Dijkman PE, Driessen-Mol A, Stenger R, Mariani C, Puolakka A, Rissanen M, Deichmann T, Odermatt B, Weber B, et al. 2010. Minimally invasive implantation of living tissue engineered heart valves: A comprehensive approach from autologous vascular cells to stem cells. J Am Coll Cardiol 56: 510-520.
151. Schoen FJ. 2008. Evolving concepts of cardiac valve dynamics: The continuum of development, functional structure, pathobiology, and tissue engineering. Circulation 118: 1864-1880.
152. Schoen FJ, Levy RJ. 2005. Calcification of tissue heart valve substitutes: Progress toward understanding and prevention. Ann Thorac Surg 79: 1072-1080.
153. Schroeder JA, Jackson LF, Lee DC, Camenisch TD. 2003. Form and function of developing heart valves: Coordination by extracellular matrix and growth factor signaling. J Mol Med (Berl) 81: 392-403.
154. Shelton EL, Yutzey KE. 2007. Tbx20 regulation of endocardial cushion cell proliferation and extracellular matrix gene expression. Dev Biol 302: 376-388.
155. Shinoka T, Breuer CK, Tanel RE, Zund G, Miura T, Ma PX, Langer R, Vacanti JP, Mayer JE Jr. 1995. Tissue engineering heart valves: Valve leaflet replacement study in a lamb model. Ann Thorac Surg 60: S513-S516.
156. Simmons CA, Grant GR, Manduchi E, Davies PF. 2005. Spatial heterogeneity of endothelial phenotypes correlates with side-specific vulnerability to calcification in normal porcine aortic valves. Circ Res 96: 792-799.
157. Simon P, Kasimir MT, Seebacher G, Weigel G, Ullrich R, Salzer-Muhar U, Rieder E, Wolner E. 2003. Early failure of the tissue engineered porcine heart valve SYNERGRAFT in pediatric patients. Eur J Cardiothorac Surg 23: 1002-1006; discussion 1006.
158. Singh MK, Christoffels VM, Dias JM, Trowe MO, Petry M, Schuster-Gossler K, Burger A, Ericson J, Kispert A. 2005. Tbx20 is essential for cardiac chamber differentiation and repression of Tbx2. Development 132: 2697-2707.
159. Siu SC, Silversides CK. 2010. Bicuspid aortic valve disease. J Am Coll Cardiol 55: 2789-2800.
160. Snarr BS, Kern CB, Wessels A. 2008. Origin and fate of cardiac mesenchyme. Dev Dyn 237: 2804-2819.
161. Snider P, Hinton RB, Moreno-Rodriguez RA, Wang J, Rogers R, Lindsley A, Li F, Ingram DA, Menick D, Field L, et al. 2008. Periostin is required for maturation and extracellular matrix stabilization of noncardiomyocyte lineages of the heart. Circ Res 102: 752-760.
162. Soini Y, Satta J, Maatta M, Autio-Harmainen H. 2001. Expression of MMP2, MMP9, MT1-MMP, TIMP1, and TIMP2 mRNA in valvular lesions of the heart. J Pathol 194: 225-231.
163. Srivastava D. 2006. Making or breaking the heart: From lineage determination to morphogenesis. Cell 126: 1037-1048.
164. Stankunas K, Ma GK, Kuhnert FJ, Kuo CJ, Chang CP. 2010. VEGF signaling has distinct spatiotemporal roles during heart valve development. Dev Biol 347: 325-336.
165. Stella JA, D’Amore A, Wagner WR, Sacks MS. 2010. On the biomechanical function of scaffolds for engineering loadbearing soft tissues. Acta Biomater 6: 2365-2381.
166. Stennard FA, Costa MW, Lai D, Biben C, Furtado MB, Solloway MJ, McCulley DJ, Leimena C, Preis JI, Dunwoodie SL, et al. 2005. Murine T-box transcription factor Tbx20 acts as a repressor during heart development, and is essential for adult heart integrity, function and adaptation. Development 132: 2451-2462.
167. Stephens EH, Post AD, Laucirica DR, Grande-Allen KJ. 2010. Perinatal changes in mitral and aortic valve structure and composition. Pediatr Dev Pathol 13: 447-458.
168. Sun Y, Liang X, Najafi N, Cass M, Lin L, Cai CL, Chen J, Evans SM. 2007. Islet 1 is expressed in distinct cardiovascular lineages, including pacemaker and coronary vascular cells. Dev Biol 304: 286-296.
169. Sutherland FW, Perry TE, Yu Y, Sherwood MC, Rabkin E, Masuda Y, Garcia GA, McLellan DL, Engelmayr GC Jr, Sacks MS, et al. 2005. From stem cells to viable autologous semilunar heart valve. Circulation 111: 2783-2791.
170. Syedain ZH, Weinberg JS, Tranquillo RT. 2008. Cyclic distension of fibrin-based tissue constructs: Evidence of adaptation during growth of engineered connective tissue. Proc Natl Acad Sci 105: 6537-6542.
171. Syedain ZH, Bradee AR, Kren S, Taylor DA, Tranquillo RT. 2013. Decellularized tissue-engineered heart valve leaflets with recellularization potential. Tissue Eng Part A 19: 759-769.
172. Tan H, Junor L, Price RL, Norris RA, Potts JD, Goodwin RL. 2011. Expression and deposition of fibrous extracellular matrix proteins in cardiac valves during chick development. Microsc Microanal 17: 91-100.
173. Tao G, Kotick JD, Lincoln J. 2012. Heart valve development, maintenance, and disease: The role of endothelial cells. Curr Top Dev Biol 100: 203-232.
174. Taylor PM, Batten P, Brand NJ, Thomas PS, Yacoub MH. 2003. The cardiac valve interstitial cell. Int J Biochem Cell Biol 35: 113-118.
175. Timmerman LA, Grego-Bessa J, Raya A, Bertran E, Perez-Pomares JM, Diez J, Aranda S, Palomo S, McCormick F, Izpisua-Belmonte JC, et al. 2004. Notch promotes epithelialmesenchymal transition during cardiac development and oncogenic transformation. Genes Dev 18: 99-115.
176. Uccelli A, Moretta L, Pistoia V. 2006. Immunoregulatory function of mesenchymal stem cells. Eur J Immunol 36: 2566-2573.
177. van Vlimmeren MA, Driessen-Mol A, Oomens CW, Baaijens FP. 2012. Passive and active contributions to generated force and retraction in heart valve tissue engineering. Biomech Model Mechanobiol 11: 1015-1027.
178. Verzi MP, McCulley DJ, De Val S, Dodou E, Black BL. 2005. The right ventricle, outflow tract, and ventricular septum comprise a restricted expression domain within the secondary/anterior heart field. Dev Biol 287: 134-145.
179. Vincentelli A, Wautot F, Juthier F, Fouquet O, Corseaux D, Marechaux S, Le Tourneau T, Fabre O, Susen S, Van Belle E, et al. 2007. In vivo autologous recellularization of a tissue-engineered heart valve: Are bone marrow mesenchymal stem cells the best candidates? J Thorac Cardiovasc Surg 134: 424-432.
180. von Gise A, Pu WT. 2012. Endocardial and epicardial epithelial to mesenchymal transitions in heart development and disease. Circ Res 110: 1628-1645.
181. Walsh EC, Stainier DYR. 2001. UDP-glucose dehydrogenase required for cardiac valve formation in zebrafish. Science 293: 1670-1673.
182. Warnock JN, Nanduri B, Pregonero Gamez CA, Tang J, Koback D, Muir WM, Burgess SC. 2011. Gene profiling of aortic valve interstitial cells under elevated pressure conditions: Modulation of inflammatory gene networks. Int J Inflam 2011: 176412.
183. Weber B, Scherman J, Emmert MY, Gruenenfelder J, Verbeek R, Bracher M, Black M, Kortsmit J, Franz T, Schoenauer R, et al. 2011. Injectable living marrow stromal cell-based autologous tissue engineered heart valves: First experiences with a one-step intervention in primates. Eur Heart J 32: 2830-2840.
184. Weber B, Emmert MY, Hoerstrup SP. 2012. Stem cells for heart valve regeneration. Swiss Med Wkly 142: w13622.
185. Weinberg EJ, Mack PJ, Schoen FJ, Garcia-Cardena G, KaazempurMofrad MR. 2010. Hemodynamic environments from opposing sides of human aortic valve leaflets evoke distinct endothelial phenotypes in vitro. Cardiovasc Eng 10: 5-11.
186. Wessels A, Sedmera D. 2003. Developmental anatomy of the heart:Atale of mice andman. Physiol Genom 15: 165-176.
187. Wessels A, van den Hoff MJ, Adamo RF, Phelps AL, Lockhart MM, Sauls K, Briggs LE, Norris RA, van Wijk B, Perez-Pomares JM, et al. 2012. Epicardially derived fibroblasts preferentially contribute to the parietal leaflets of the atrioventricular valves in the murine heart. Dev Biol 366: 111-124.
188. Weston MW, Yoganathan AP. 2001. Biosynthetic activity in heart valve leaflets in response to in vitro flow environments. Ann Biomed Eng 29: 752-763.
189. Wirrig EE, Hinton RB, Yutzey KE. 2011. Differential expression of cartilage and bone-related proteins in pediatric and adult diseased aortic valves. JMolCellCardiol 50: 561-569.
190. Wu B, Wang Y, Lui W, Langworthy M, Tompkins KL, Hatzopoulos AK, Baldwin HS, Zhou B. 2011. Nfatc1 coordinates valve endocardial cell lineage development required for heart valve formation. Circ Res 109: 183-192.
191. Yacoub MH, Takkenberg JJ. 2005. Will heart valve tissue engineering change the world? Nat Clin Pract Cardiovasc Med 2: 60-61.
192. Yamada M, Revelli JP, Eichele G, Barron M, Schwartz RJ. 2000. Expression of chick Tbx-2, Tbx-3, and Tbx-5 genes during early heart development: Evidence for BMP2 induction of Tbx2. Dev Biol 228: 95-105.
193. Yamagishi T, Ando K, Nakamura H. 2009. Roles of TGF-b and BMP during valvulo-septal endocardial cushion formation. Anat Sci Int 84: 77-87.
194. Yamanami M, Yahata Y, Uechi M, Fujiwara M, Ishibashi-Ueda H, Kanda K, Watanabe T, Tajikawa T, Ohba K, Yaku H, et al. 2010. Development of a completely autologous valved conduit with the sinus of Valsalva using inbody tissue architecture technology: A pilot study in pulmonary valve replacement in a beagle model. Circulation 122: S100-S106.
195. Yang L, Cai CL, Lin L, Qyang Y, Chung C, Monteiro RM, Mummery CL, Fishman GI, Cogen A, Evans S. 2006. Isl1Cre reveals a common Bmp pathway in heart and limb development. Development 133: 1575-1585.
196. Ye Q, Zund G, Benedikt P, Jockenhoevel S, Hoerstrup SP, Sakyama S, Hubbell JA, Turina M. 2000. Fibrin gel as a three dimensional matrix in cardiovascular tissue engineering. Eur J Cardiothorac Surg 17: 587-591.
197. 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: 936-942.
198. Yoganathan AP, Lemmon JD, Ellis JT. 2000. Heart valve dynamics. In The biomedical engineering handbook, 2nd ed. (ed. Bronzino JD). CRC, Boca Raton, FL.
199. Yutzey KE, Colbert M, Robbins J. 2005. Ras-related signaling pathways in valve development: Ebb and flow. Physiology (Bethesda) 20: 390-397.
200. Zaffran S, Kelly RG, Meilhac SM, Buckingham ME, Brown NA. 2004. Right ventricular myocardium derives from the anterior heart field. Circ Res 95: 261-268.
201. Zhao B, Etter L, Hinton RB Jr, Benson DW. 2007. BMP and FGF regulatory pathways in semilunar valve precursor cells. Dev Dyn 236: 971-980.
202. Zhou B, von Gise A, Ma Q, Hu YW, Pu WT. 2010. Genetic fate mapping demonstrates contribution of epicardiumderived cells to the annulus fibrosis of the mammalian heart. Dev Biol 338: 251-261.
203. Zilla P, Brink J, Human P, Bezuidenhout D. 2008. Prosthetic heart valves: Catering for the few. Biomaterials 29: 385-406.