Valvular interstitial cell seeded poly(glycerol sebacate) scaffolds: Toward a biomimetic in vitro model for heart valve tissue engineering

Acta Biomaterialia

Volumn 9, Issue 4, 2013, Pages 5974-5988

  Masoumi, Nafiseh ^a   Johnson, Katherine L ^a   Howell, M Christian ^a   Engelmayr Jr , George C ^b  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b Duke University   (United States)

Author keywords

Aortic valve; Heart valve; Microfabricated; Pulmonary valve; Tissue engineered

Indexed keywords

ANISOTROPY; BIOMECHANICS; BIOMIMETICS; BLOOD VESSELS; CELLS; COLLAGEN; CYTOLOGY; SCAFFOLDS (BIOLOGY); SCANNING ELECTRON MICROSCOPY; VALVES (MECHANICAL);

'CURRENT; AORTIC VALVES; HEART VALVES; IN-VITRO MODELS; INTERSTITIALS; MICROFABRICATED; POLIES (GLYCEROLSEBACATE); POLY(GLYCEROL SEBACATE); PULMONARY VALVES; TISSUE ENGINEERED;

TISSUE;

BIOMIMETIC MATERIAL; COLLAGEN; DNA; ELASTOMER; POLY(GLYCEROL SEBACATE); TISSUE SCAFFOLD; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANISOTROPY; ARTICLE; CELL CULTURE; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; HEART VALVE PROSTHESIS; IN VITRO STUDY; LEYDIG CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPY; TISSUE ENGINEERING; VALVULAR INTERSTITIAL CELL;

SUS;

EID: 84875370720     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2013.01.001     Document Type: Article

References (73)

1. A. Starr, C.L. Fessler, G. Grunkemeier, and G.W. He Heart valve replacement surgery: past, present and future Clin Exp Pharmacol Physiol 29 2002 735 738
2. E. Rabkin-Aikawa, M. Aikawa, M. Farber, J.R. Kratz, G. Garcia-Cardena, and N.T. Kouchoukos Clinical pulmonary autograft valves: pathologic evidence of adaptive remodeling in the aortic site J Thorac Cardiovasc Surg 128 2004 552
3. J. Perron, A.M. Moran, K. Gauvreau, P.J. del Nido, J.E. Mayer Jr, and R.A. Jonas Valved homograft conduit repair of the right heart in early infancy Ann Thorac Surg 68 1999 542
4. M.S. Sacks, F.J. Schoen, and J.E. Mayer Bioengineering challenges for heart valve tissue engineering Annu Rev Biomed Eng 11 2009 289
5. C.K. Breuer, T. Shin'oka, R.E. Tanel, G. Zund, D.J. Mooney, and P.X. Ma Tissue engineering lamb heart valve leaflets Biotechnol Bioeng 50 1996 562 567
6. T. Shinoka, C.K. Breuer, R.E. Tanel, G. Zund, T. Miura, and P.X. Ma Tissue engineering heart valves: valve leaflet replacement study in a lamb model Ann Thorac Surg 60 1995 S513
7. S.P. Hoerstrup, R. Sodian, S. Daebritz, J. Wang, E.A. Bacha, and D.P. Martin Functional living trileaflet heart valves grown in vitro Circulation 102 2000 III44
8. J.E. Jordan, J.K. Williams, S.J. Lee, D. Raghavan, A. Atala, and J.J. Yoo Bioengineered self-seeding heart valves J Thorac Cardiovasc Surg 143 2012 201 208
9. P.M. Dohmen, A. Lembcke, S. Holinski, A. Pruss, and W. Konertz Ten years of clinical results with a tissue-engineered pulmonary valve Ann Thorac Surg 92 2011 1308 1314
10. R.A. Hopkins, A.A. Bert, S.L. Hilbert, R.W. Quinn, K.M. Brasky, and W.B. Drake Bioengineered human and allogeneic pulmonary valve conduits chronically implanted orthotopically in baboons: hemodynamic performance and immunologic consequences J Thorac Cardiovasc Surg 2012 [Epub ahead of print]
11. P.E. Dijkman, A. Driessen-Mol, L. Frese, S.P. Hoerstrup, and F.P. Baaijens Decellularized homologous tissue-engineered heart valves as off-the-shelf alternatives to xeno- and homografts Biomaterials 33 2012 4545 4554
12. T.N. McAllister, N. Dusserre, N. Chronos, and N. L'Heureux A Completely biological, tissue engineered valve leaflet suitable for TAVI. Heart valve biology and tissue engineering 2012 QScience Mykonos
13. N. Masoumi, A. Jean, J.T. Zugates, K.L. Johnson, and G.C. Engelmayr Jr Laser microfabricated poly(glycerol sebacate) scaffolds for heart valve tissue engineering J Biomed Mater Res A 101 2013 104 114
14. N.J. Amoroso, A. D'Amore, Y. Hong, C.P. Rivera, M.S. Sacks, and W.R. Wagner Microstructural manipulation of electrospun scaffolds for specific bending stiffness for heart valve tissue engineering Acta Biomater 8 2012 4268 4277
15. L.A. Hockaday, K.H. Kang, N.W. Colangelo, P.Y. Cheung, B. Duan, and E. Malone Rapid 3D printing of anatomically accurate and mechanically heterogeneous aortic valve hydrogel scaffolds Biofabrication 4 2012 035005
16. B. Duan, L.A. Hockaday, K.H. Kang, and J.T. Butcher 3D Bioprinting of heterogeneous aortic valve conduits with alginate/gelatin hydrogels J Biomed Mater Res A 2012 http://dx.doi.org/10.1002/jbm.a.34420/ [Epub ahead of print]
17. J.L. Berry, J.A. Steen, J. Koudy Williams, J.E. Jordan, A. Atala, and J.J. Yoo Bioreactors for development of tissue engineered heart valves Ann Biomed Eng 38 2010 3272
18. D. Schmidt, P.E. Dijkman, A. Driessen-Mol, R. Stenger, C. Mariani, and A. Puolakka Minimally-invasive implantation of living tissue engineered heart valves: a comprehensive approach from autologous vascular cells to stem cells J Am Coll Cardiol 56 2010 510
19. B. Weber, M.Y. Emmert, L. Behr, R. Schoenauer, C. Brokopp, and C. Drogemuller Prenatally engineered autologous amniotic fluid stem cell-based heart valves in the fetal circulation Biomaterials 33 2012 4031 4043
20. F.W. Sutherland, T.E. Perry, Y. Yu, M.C. Sherwood, E. Rabkin, and Y. Masuda From stem cells to viable autologous semilunar heart valve Circulation 111 2005 2783
21. D. Gottlieb, T. Kunal, S. Emani, E. Aikawa, D.W. Brown, and A.J. Powell In vivo monitoring of function of autologous engineered pulmonary valve J Thorac Cardiovasc Surg 139 2010 723
22. F. Colazzo, P. Sarathchandra, R.T. Smolenski, A.H. Chester, Y.T. Tseng, and J.T. Czernuszka Extracellular matrix production by adipose-derived stem cells: implications for heart valve tissue engineering Biomaterials 32 2011 119
23. 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
24. W.D. Merryman, I. Youn, H.D. Lukoff, P.M. Krueger, F. Guilak, and R.A. Hopkins Correlation between heart valve interstitial cell stiffness and transvalvular pressure: implications for collagen biosynthesis Am J Physiol Heart Circ Physiol 290 2006 H224
25. I.G. Aldous, S.P. Veres, A. Jahangir, and J.M. Lee Differences in collagen cross-linking between the four valves of the bovine heart: a possible role in adaptation to mechanical fatigue Am J Physiol Heart Circ Physiol 296 2009 H1898 H1906
26. A.D. Lewinsohn, A. Anssari-Benham, D.A. Lee, P.M. Taylor, A.H. Chester, and M.H. Yacoub Anisotropic strain transfer through the aortic valve and its relevance to the cellular mechanical environment Proc Inst Mech Eng H 225 2011 821 830
27. H.Y. Huang, J. Liao, and M.S. Sacks In-situ deformation of the aortic valve interstitial cell nucleus under diastolic loading J Biomech Eng 129 2007 880
28. 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
29. H. Wang, S.M. Haeger, A.M. Kloxin, L.A. Leinwand, and K.S. Anseth Redirecting valvular myofibroblasts into dormant fibroblasts through light-mediated reduction in substrate modulus PLoS One 7 2012 e39969
30. E.H. Stephens, C.A. Durst, J.L. West, and K.J. Grande-Allen Mitral valvular interstitial cell responses to substrate stiffness depend on age and anatomic region Acta Biomater 7 2011 75 82
31. J.D. Hutcheson, R. Venkataraman, F.J. Baudenbacher, and W.D. Merryman Intracellular Ca(2+) accumulation is strain-dependent and correlates with apoptosis in aortic valve fibroblasts J Biomech 45 2012 888 894
32. P. Thayer, K. Balachandran, S. Rathan, C.H. Yap, S. Arjunon, and H. Jo The effects of combined cyclic stretch and pressure on the aortic valve interstitial cell phenotype Ann Biomed Eng 39 2011 1654 1667
33. K.E. Smith, S.A. Metzler, and J.N. Warnock Cyclic strain inhibits acute pro-inflammatory gene expression in aortic valve interstitial cells Biomech Model Mechanobiol 9 2010 117 125
34. A.M. Throm Quinlan, L.N. Sierad, A.K. Capulli, L.E. Firstenberg, and K.L. Billiar Combining dynamic stretch and tunable stiffness to probe cell mechanobiology in vitro PLoS One 6 2011 e23272
35. N. Latif, P. Sarathchandra, P.S. Thomas, J. Antoniw, P. Batten, and A.H. Chester Characterization of structural and signaling molecules by human valve interstitial cells and comparison to human mesenchymal stem cells J Heart Valve Dis 16 2007 56
36. C.H. Ku, P.H. Johnson, P. Batten, P. Sarathchandra, R.C. Chambers, and P.M. Taylor Collagen synthesis by mesenchymal stem cells and aortic valve interstitial cells in response to mechanical stretch Cardiovasc Res 71 2006 548
37. 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
38. P.M. Taylor, E. Sachlos, S.A. Dreger, A.H. Chester, J.T. Czernuszka, and M.H. Yacoub Interaction of human valve interstitial cells with collagen matrices manufactured using rapid prototyping Biomaterials 27 2006 2733
39. W.D. Merryman, J. Liao, A. Parekh, J.E. Candiello, H. Lin, and M.S. Sacks Differences in tissue-remodeling potential of aortic and pulmonary heart valve interstitial cells Tissue Eng 13 2007 2281
40. K.S. Masters, D.N. Shah, L.A. Leinwand, and K.S. Anseth Crosslinked hyaluronan scaffolds as a biologically active carrier for valvular interstitial cells Biomaterials 26 2005 2517
41. J.A. Benton, B.D. Fairbanks, and K.S. Anseth Characterization of valvular interstitial cell function in three dimensional matrix metalloproteinase degradable PEG hydrogels Biomaterials 30 2009 6593
42. R.A. Gould, K. Chin, T.P. Santisakultarm, A. Dropkin, J.M. Richards, and C.B. Schaffer Cyclic strain anisotropy regulates valvular interstitial cell phenotype and tissue remodeling in three-dimensional culture Acta Biomater 8 2012 1710 1719
43. V. Gupta, H. Tseng, B.D. Lawrence, and K.J. Grande-Allen Effect of cyclic mechanical strain on glycosaminoglycan and proteoglycan synthesis by heart valve cells Acta Biomater 5 2009 531
44. Y. Wang, G.A. Ameer, B.J. Sheppard, and R. Langer A tough biodegradable elastomer Nat Biotechnol 20 2002 602
45. R. Rai, M. Tallawi, A. Grigore, and A.R. Boccaccini Synthesis, properties and biomedical applications of poly(glycerol sebacate) (PGS): a review Prog Polym Sci 37 2012 1051 1078
46. G.C. Engelmayr Jr, M. Cheng, C.J. Bettinger, J.T. Borenstein, R. Langer, and L.E. Freed Accordion-like honeycombs for tissue engineering of cardiac anisotropy Nat Mater 7 2008 1003
47. M.D. Guillemette, H. Park, J.C. Hsiao, S.R. Jain, B.L. Larson, and R. Langer Combined technologies for microfabricating elastomeric cardiac tissue engineering scaffolds Macromol Biosci 10 2010 1330
48. H. Park, B.L. Larson, M.D. Guillemette, S.R. Jain, C. Hua, and G.C. Engelmayr Jr The significance of pore microarchitecture in a multi-layered elastomeric scaffold for contractile cardiac muscle constructs Biomaterials 32 2011 1856
49. W.L. Neeley, S. Redenti, H. Klassen, S. Tao, T. Desai, and M.J. Young A microfabricated scaffold for retinal progenitor cell grafting Biomaterials 29 2008 418
50. J.M. Kemppainen, and S.J. Hollister Tailoring the mechanical properties of 3D-designed poly(glycerol sebacate) scaffolds for cartilage applications J Biomed Mater Res A 94 2010 9
51. 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
52. W.D. Merryman, H.Y. Huang, F.J. Schoen, and M.S. Sacks The effects of cellular contraction on aortic valve leaflet flexural stiffness J Biomech 39 2006 88
53. M.S. Sacks, W. David Merryman, and D.E. Schmidt On the biomechanics of heart valve function J Biomech 42 2009 1804 1824
54. J.M. Kelm, M.Y. Emmert, A. Zurcher, D. Schmidt, Y. Begus Nahrmann, and K.L. Rudolph Functionality, growth and accelerated aging of tissue engineered living autologous vascular grafts Biomater 33 2012 8277 8285
55. D. van Geemen, A. Driessen-Mol, L.G. Grootzwagers, R.S. Soekhradj-Soechit, P.W. Riem Vis, and F.P. Baaijens Variation in tissue outcome of ovine and human engineered heart valve constructs: relevance for tissue engineering Regen Med 7 2012 59 70
56. C.J. Bettinger, E.J. Weinberg, K.M. Kulig, J.P. Vacanti, Y. Wang, and J.T. Borenstein Three-dimensional microfluidic tissue-engineering scaffolds using a flexible biodegradable polymer Adv Mater 18 2005 165 169
57. W. Bian, B. Liau, N. Badie, and N. Bursac Mesoscopic hydrogel molding to control the 3D geometry of bioartificial muscle tissues Nat Protoc 4 2009 1522
58. G.C. Engelmayr Jr, E. Rabkin, F.W. Sutherland, F.J. Schoen, J.E. Mayer Jr, and M.S. Sacks The independent role of cyclic flexure in the early in vitro development of an engineered heart valve tissue Biomaterials 26 2005 175
59. G.C. Engelmayr Jr, V.L. Sales, J.E. Mayer Jr, and M.S. Sacks Cyclic flexure and laminar flow synergistically accelerate mesenchymal stem cell-mediated engineered tissue formation: Implications for engineered heart valve tissues Biomaterials 27 2006 6083
60. H.Y. Huang, B.N. Balhouse, and S. Huang Application of simple biomechanical and biochemical tests to heart valve leaflets: implications for heart valve characterization and tissue engineering Proc Inst Mech Eng H 226 2012 868 876
61. G.C. Engelmayr Jr, G.D. Papworth, S.C. Watkins, J.E. Mayer Jr, and M.S. Sacks Guidance of engineered tissue collagen orientation by large-scale scaffold microstructures J Biomech 39 2006 1819
62. G.C. Engelmayr Jr, and M.S. Sacks Prediction of extracellular matrix stiffness in engineered heart valve tissues based on nonwoven scaffolds Biomech Model Mechanobiol 7 2008 309
63. I. Pomerantseva, N. Krebs, A. Hart, C.M. Neville, A.Y. Huang, and C.A. Sundback Degradation behavior of poly(glycerol sebacate) J Biomed Mater Res A 91 2009 1038
64. D. Mavrilas, and Y. Missirlis An approach to the optimization of preparation of bioprosthetic heart valves J Biomech 24 1991 331 339
65. M.S. Sacks, T.V. Lam, and J.E. Mayer Jr A structural constitutive model for the native pulmonary valve IEEE Eng Med Biol Soc Conf 5 2004 3734 3736
66. G.W. Christie, and B.G. Barratt-Boyes Mechanical properties of porcine pulmonary valve leaflets: how do they differ from aortic leaflets? Ann Thorac Surg 60 1995 S195 S199
67. P. Stradins, R. Lacis, I. Ozolanta, B. Purina, V. Ose, and L. Feldmane Comparison of biomechanical and structural properties between human aortic and pulmonary valve Eur J Cardiothorac Surg 26 2004 634 639
68. A. Mol, M.C. Rutten, N.J. Driessen, C.V. Bouten, G. Zund, and F.P. Baaijens Autologous human tissue-engineered heart valves: prospects for systemic application Circulation 114 2006 I152 I158
69. L.J. Gibson, M.F. Ashby, G.S. Schajer, and C.I. Robertson The mechanics of two-dimensional cellular materials Proc R Soc Lond A 382 1982 25 42
70. Y. Wang, Y.M. Kim, and R. Langer In vivo degradation characteristics of poly(glycerol sebacate) J Biomed Mater Res A 66 2003 192
71. S.L. Liang, X.Y. Yang, X.Y. Fang, W.D. Cook, G.A. Thouas, and Q.Z. Chen In vitro enzymatic degradation of poly (glycerol sebacate)-based materials Biomaterials 32 2011 8486 8496
72. C. Martin, and W. Sun Biomechanical characterization of aortic valve tissue in humans and common animal models J Biomed Mater Res 100 2012 1591 1599
73. 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