Glycosaminoglycan entrapment by fibrin in engineered heart valve tissues

Acta Biomaterialia

Volumn 9, Issue 9, 2013, Pages 8149-8157

  Alfonso, Abraham R ^a   Rath, Sasmita ^a   Rafiee, Parvin ^a   Hernandez Espino, Mario ^a   Din, Mahreen ^a   George, Florence ^b   Ramaswamy, Sharan ^a  

^a Florida International University   (United States)

^b FLORIDA INTERNATIONAL UNIVERSITY   (United States)

Author keywords

Engineered heart valves; Fibrin; Flex flow; GAG retention; Glycosaminoglycans

Indexed keywords

HEART; HISTOLOGY; STABILITY; TISSUE; VALVES (MECHANICAL);

ENGINEERED HEART VALVE; EXTRACELLULAR MATRICES; FIBRIN; FLEX FLOW; GLYCOSAMINOGLYCAN RETENTION; GLYCOSAMINOGLYCANS; HEART VALVES; PERIODONTAL LIGAMENT CELLS; TISSUE-ENGINEERED HEART;

COLLAGEN;

COLLAGEN; DNA; FIBRIN; GENOMIC DNA; GLYCOSAMINOGLYCAN;

ADHESION; ADULT; ARTICLE; CELL STRUCTURE; HEART VALVE; HISTOLOGY; HUMAN; HUMAN CELL; PERIODONTAL LIGAMENT; PRIORITY JOURNAL; TISSUE ENGINEERING;

EID: 84880919748     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2013.06.009     Document Type: Article

References (51)

1. E.H. Stephens, D.L. Kearney, and K.J. Grande-Allen Insight into pathologic abnormalities in congenital semilunar valve disease based on advances in understanding normal valve microstructure and extracellular matrix Cardiovasc Pathol 21 2012 46 58
2. M. Scott, and I. Vesely Aortic valve cusp microstructure: the role of elastin Ann Thorac Surg 60 1995 S391 S394
3. E. Rabkin-Aikawa, J.E. Mayer Jr, and F.J. Schoen Heart valve regeneration Adv Biochem Eng Biotechnol 94 2005 141 179 (Pubitemid 44608659)
4. E.H. Stephens, C.K. Chu, and K.J. Grande-Allen Valve proteoglycan content and glycosaminoglycan fine structure are unique to microstructure, mechanical load and age: relevance to an age-specific tissue-engineered heart valve Acta Biomater 4 2008 1148 1160
5. J.J. Lovekamp, D.T. Simionescu, J.J. Mercuri, B. Zubiate, M.S. Sacks, and N.R. Vyavahare Stability and function of glycosaminoglycans in porcine bioprosthetic heart valves Biomaterials 27 2006 1507 1518 (Pubitemid 41739577)
6. M. Rothenburger, W. Volker, P. Vischer, B. Glasmacher, H.H. Scheld, and M. Deiwick Ultrastructure of proteoglycans in tissue-engineered cardiovascular structures Tissue Eng 8 2002 1049 1056 (Pubitemid 35397250)
7. C. Breymann, D. Schmidt, and S.P. Hoerstrup Umbilical cord cells as a source of cardiovascular tissue engineering Stem Cell Rev 2 2006 87 92 (Pubitemid 46132375)
8. 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 III49
9. E. Rabkin, S.P. Hoerstrup, M. Aikawa, J.E. Mayer Jr, and F.J. Schoen Evolution of cell phenotype and extracellular matrix in tissue-engineered heart valves during in-vitro maturation and in-vivo remodeling J Heart Valve Dis 11 2002 308 314 [discussion 14] (Pubitemid 34578445)
10. D. Schmidt, J. Achermann, B. Odermatt, C. Breymann, A. Mol, and M. Genoni Prenatally fabricated autologous human living heart valves based on amniotic fluid derived progenitor cells as single cell source Circulation 116 2007 I64 I70
11. D. Schmidt, and S.P. Hoerstrup Tissue engineered heart valves based on human cells Swiss Med Wkly 136 2006 618 623 (Pubitemid 44744679)
12. D. Schmidt, A. Mol, C. Breymann, J. Achermann, B. Odermatt, and M. Gossi Living autologous heart valves engineered from human prenatally harvested progenitors Circulation 114 2006 I125 I131
13. 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 2791 (Pubitemid 40791550)
14. G.C. Engelmayr Jr, D.K. Hildebrand, F.W. Sutherland, J.E. Mayer Jr, and M.S. Sacks A novel bioreactor for the dynamic flexural stimulation of tissue engineered heart valve biomaterials Biomaterials 24 2003 2523 2532 (Pubitemid 36410329)
15. 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 175 187 (Pubitemid 38789100)
16. 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 6095 (Pubitemid 44414977)
17. G.C. Engelmayr Jr, L. Soletti, S.C. Vigmostad, S.G. Budilarto, W.J. Federspiel, and K.B. Chandran A novel flex-stretch-flow bioreactor for the study of engineered heart valve tissue mechanobiology Ann Biomed Eng 36 2008 700 712
18. S.P. Hoerstrup, R. Sodian, J.S. Sperling, J.P. Vacanti, and J.E. Mayer Jr New pulsatile bioreactor for in vitro formation of tissue engineered heart valves Tissue Eng 6 2000 75 79 (Pubitemid 30123985)
19. C. Martinez, S. Rath, S. Van Gulden, D. Pelaez, A. Alfonso, N. Fernandez, L. Kos, H. Cheung, and S. Ramaswamy Periodontal ligament cells cultured under steady-flow environments demonstrate potential for use in heart valve tissue engineering Tissue Eng Part A 19 2013 458 466
20. S. Ramaswamy, D. Gottlieb, G.C. Engelmayr Jr, E. Aikawa, D.E. Schmidt, and D.M. Gaitan-Leon The role of organ level conditioning on the promotion of engineered heart valve tissue development in-vitro using mesenchymal stem cells Biomaterials 31 2010 1114 1125
21. S. Ramaswamy, P.A. Schornack, A.G. Smelko, S.M. Boronyak, J. Ivanova, and J.E. Mayer Jr Superparamagnetic iron oxide (SPIO) labeling efficiency and subsequent MRI tracking of native cell populations pertinent to pulmonary heart valve tissue engineering studies NMR Biomed 25 2012 410 417
22. M. Salinas, D.E. Schmidt, M. Libera, R.R. Lange, and S. Ramaswamy Oscillatory shear stress created by fluid pulsatility versus flexed specimen configurations Comput Meth Biomech Biomed Eng 2012 [Epub ahead of print]
23. N.J. Amoroso, A. D'Amore, Y. Hong, W.R. Wagner, and M.S. Sacks Elastomeric electrospun polyurethane scaffolds: the interrelationship between fabrication conditions, fiber topology, and mechanical properties Adv Mater 23 2012 106 111
24. A. D'Amore, J.A. Stella, W.R. Wagner, and M.S. Sacks Characterization of the complete fiber network topology of planar fibrous tissues and scaffolds Biomaterials 31 2012 5345 5354
25. C. Del Gaudio, M. Grigioni, A. Bianco, and G. De Angelis Electrospun bioresorbable heart valve scaffold for tissue engineering Int J Artif Organs 31 2008 68 75 (Pubitemid 351419333)
26. N. Grabow, K. Schmohl, A. Khosravi, M. Philipp, M. Scharfschwerdt, and B. Graf Mechanical and structural properties of a novel hybrid heart valve scaffold for tissue engineering Artif Organs 28 2004 971 979 (Pubitemid 40378873)
27. H. Hong, G.N. Dong, W.J. Shi, S. Chen, C. Guo, and P. Hu Fabrication of biomatrix/polymer hybrid scaffold for heart valve tissue engineering in vitro ASAIO J 54 2008 627 632
28. R. Sodian, J.S. Sperling, D.P. Martin, A. Egozy, U. Stock, and J.E. Mayer Jr Fabrication of a trileaflet heart valve scaffold from a polyhydroxyalkanoate biopolyester for use in tissue engineering Tissue Eng 6 2000 183 188 (Pubitemid 30227173)
29. P.S. Robinson, and R.T. Tranquillo Planar biaxial behavior of fibrin-based tissue-engineered heart valve leaflets Tissue Eng Part A 15 2009 2763 2772
30. Z.H. Syedain, J.S. Weinberg, and R.T. Tranquillo Cyclic distension of fibrin-based tissue constructs: evidence of adaptation during growth of engineered connective tissue Proc Natl Acad Sci USA 105 2008 6537 6542 (Pubitemid 351754542)
31. L.A. Loiacono, B. Sigel, E.J. Feleppa, V.K. Swami, R.E. Parsons, and J. Justin Cellularity and fibrin mesh properties as a basis for ultrasonic tissue characterization of blood clots and thrombi Ultrasound Med Biol 18 1992 399 410
32. 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 309 321 (Pubitemid 352039639)
33. 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 723 731
34. www.anpro.com. Anproline Gas Sterilization: Key Operator Training Kit. Haw River, NC: Anderson Products Inc., 2012.
35. G. Zhang, X. Wang, Z. Wang, J. Zhang, and L. Suggs A PEGylated fibrin patch for mesenchymal stem cell delivery Tissue Eng 12 2006 9 19
36. S. Ramaswamy, J.B. Greco, M.C. Uluer, Z. Zhang, K.W. Fishbein, and R.G. Spencer Magnetic resonance imaging of chondrocytes labeled with superparamagnetic iron oxide nanoparticles in tissue-engineered cartilage Tissue Eng Part A 15 2009 3899 3910
37. M.S. Sacks, and A.P. Yoganathan Heart valve function: a biomechanical perspective Philos Trans R Soc Lond B Biol Sci 362 2007 1369 1391 (Pubitemid 47195029)
38. E.A. Talman, and D.R. Boughner Effect of altered hydration on the internal shear properties of porcine aortic valve cusps Ann Thorac Surg 71 2001 S375 S378
39. M.J. Thubrikar, J.R. Skinner, R.T. Eppink, and S.P. Nolan Stress analysis of porcine bioprosthetic heart valves in vivo J Biomed Mater Res 16 1982 811 826
40. D.D. Swartz, J.A. Russell, and S.T. Andreadis Engineering of fibrin-based functional and implantable small-diameter blood vessels Am J Physiol Heart Circ Physiol 288 2005 H1451 H1460
41. C.K. Ng, C.J. Handley, B.N. Preston, and H.C. Robinson The extracellular processing and catabolism of hyaluronan in cultured adult articular cartilage explants Arch Biochem Biophys 298 1992 70 79
42. P. Divya, and L.K. Krishnan Glycosaminoglycans restrained in a fibrin matrix improve ECM remodelling by endothelial cells grown for vascular tissue engineering J Tissue Eng Regener Med 3 2009 377 388
43. T.C. Flanagan, C. Cornelissen, S. Koch, B. Tschoeke, J.S. Sachweh, and T. Schmitz-Rode The in vitro development of autologous fibrin-based tissue-engineered heart valves through optimised dynamic conditioning Biomaterials 28 2007 3388 3397 (Pubitemid 46726632)
44. T.C. Flanagan, J.S. Sachweh, J. Frese, H. Schnoring, N. Gronloh, and S. Koch In vivo remodeling and structural characterization of fibrin-based tissue-engineered heart valves in the adult sheep model Tissue Eng Part A 15 2009 2965 2976
45. S. Jockenhoevel, G. Zund, S.P. Hoerstrup, K. Chalabi, J.S. Sachweh, and L. Demircan Fibrin gel - advantages of a new scaffold in cardiovascular tissue engineering Eur J Cardiothorac Surg 19 2001 424 430 (Pubitemid 32297774)
46. S. Koch, T.C. Flanagan, J.S. Sachweh, F. Tanios, H. Schnoering, and T. Deichmann Fibrin-polylactide-based tissue-engineered vascular graft in the arterial circulation Biomaterials 31 2010 4731 4739
47. Q. Ye, G. Zund, P. Benedikt, S. Jockenhoevel, S.P. Hoerstrup, and S. Sakyama Fibrin gel as a three dimensional matrix in cardiovascular tissue engineering Eur J Cardiothorac Surg 17 2000 587 591 (Pubitemid 30256271)
48. S. Jockenhoevel, and T.C. Flanagan Cardiovascular tissue engineering based on fibrin-gel-scaffolds D. Eberli, Tissue engineering for tissue and organ regeneration 2011 Intech Rijeka 35 48
49. C.Y. Huang, D. Pelaez, J. Dominguez-Bendala, F. Garcia-Godoy, and H.S. Cheung Plasticity of stem cells derived from adult periodontal ligament Regener Med 4 2009 809 821
50. A. Borghi, S.E. New, A.H. Chester, P.M. Taylor, and M.H. Yacoub Time-dependent mechanical properties of aortic valve cusps: effect of glycosaminoglycan depletion Acta Biomater 9 2013 4645 4652
51. N. Vyavahare, M. Ogle, F.J. Schoen, R. Zand, D.C. Gloeckner, and M. Sacks Mechanisms of bioprosthetic heart valve failure: fatigue causes collagen denaturation and glycosaminoglycan loss J Biomed Mater Res 46 1999 44 50 (Pubitemid 29233179)