Review article: Biomedical intelligence
Vol. 142 No. 2930 (2012)
Stem cells for heart valve regeneration
- Benedikt Weber
- Maximilian Y Emmert
- Simon P. Hoerstrup
Summary
Heart valve tissue engineering holds the potential to overcome limitations of currently used heart valve prostheses. It involves the isolation and expansion of autologous patient cells, the subsequent seeding of these cells onto an appropriate scaffold material, the in vitro incubation and the in vivo implantation of the derived tissue-engineered construct into the patient from whom the cells were taken. While vascular-derived cells require harvest of intact donor tissue and show limited expansion capacities, the use of stem or progenitor cells may overcome these limitations and expand the versatility of the concept of heart valve tissue engineering. Possible sources include cells isolated from blood, bone marrow, adipose tissue, amniotic fluid, chorionic villi, umbilical cord and induced pluripotent stem cells. Here we review different stem cell sources with particular regard to cellular phenotypes and their suitability for application in heart valve tissue engineering.
References
- Yacoub MH, Takkenberg JJ. Will heart valve tissue engineering change the world? Nat Clin Pract Cardiovasc Med. 2005;2(2):60–1.
- Weber B, Hoerstrup SP. Regenerating heart valves. In: Regenerating the heart: stem cells and the cardiovascular system; 1st edition; Springer – New York, 2011.
- Schmidt D, Hoerstrup SP. Tissue engineered heart valves based on human cells. Swiss Med Wkly. 2006;136(39-40):618–23.
- Kobayashi J. Stentless aortic valve replacement: an update. Vasc Health Risk Manag. 2011;7:345–51.
- Langer R, Vacanti JP (1993) Tissue engineering. Science. 260:920–6.
- Dolgin E. Taking tissue engineering to heart. Nat Med. 2011;17(9):1032–5.
- Vogel G. Tissue engineering. Mending the youngest hearts. Science. 2011;333(6046):1088–9.
- Mol A, Bouten CV, Baaijens FP, Zünd G, Turina MI, Hoerstrup SP. Tissue engineering of semilunar heart valves: current status and future developments. J Heart Valve Dis. 2004;13(2):272–80.
- Hoerstrup SP, Sodian R, Daebritz S, Wang J, Bacha EA, Martin DP, et al. Functional living trileaflet heart valves grown in vitro. Circulation. 2000;102(19 Suppl 3):III44–9.
- De Vriese AS, Verbeuren TJ, Van de Voorde J, Lameire NH, Vanhoutte PM. Endothelial dysfunction in diabetes. Br J Pharmacol. 2000;130(5):963–74.
- Weiner LP. Definitions and criteria for stem cells. Methods Mol Biol. 2008;438:3–8.
- Vassalli G, Moccetti T. Cardiac repair with allogeneic mesenchymal stem cells after myocardial infarction. Swiss Med Wkly. 2011;141:w13209.
- Prockop DJ. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science. 1997;276(5309):71–4.
- Kadner A, Hoerstrup SP, Zund G, Eid K, Maurus C, Melnitchouk S, et al. A new source for cardiovascular tissue engineering: human bone marrow stromal cells. Eur J Cardiothorac Surg. 2002;21(6):1055–60.
- Hoerstrup SP, Kadner A, Melnitchouk S, Trojan A, Eid K, Tracy J, et al. Tissue engineering of functional trileaflet heart valves from human marrow stromal cells. Circulation. 2002;106(12 Suppl 1):I143–50
- Sutherland FW, Perry TE, Yu Y, Sherwood MC, Rabkin E, Masuda Y, et al. From stem cells to viable autologous semilunar heart valve. Circulation. 2005;31;111:2783–91.
- Schmidt D, Dijkman PE, Driessen-Mol A, Stenger R, Mariani C, Puolakka A, et al. Minimally-invasive implantation of living tissue engineered heart valves: a comprehensive approach from autologous vascular cells to stem cells. J Am Coll Cardiol. 2010;3;56(6):510–20.
- Hibino N, McGillicuddy E, Matsumura G, Ichihara Y, Naito Y, Breuer C, et al. Late-term results of tissue-engineered vascular grafts in humans. J Thorac Cardiovasc Surg. 2010;139(2):431–6, 436.e1–2.
- Matsumura G, Miyagawa-Tomita S, Shin’oka T, Ikada Y, Kurosawa H. First evidence that bone marrow cells contribute to the construction of tissue-engineered vascular autografts in vivo. Circulation. 2003;108:1729–34.
- Roh JD, Sawh-Martinez R, Brennan MP, Jay SM, Devine L, Rao DA, et al. Tissue-engineered vascular grafts transform into mature blood vessels via an inflammation-mediated process of vascular remodeling. Proc Natl Acad Sci U S A. 2010;107:4669–74.
- Shin’oka T, Matsumura G, Hibino N, Naito Y, Watanabe M, Konuma T, et al. Midterm clinical result of tissue-engineered vascular autografts seeded with autologous bone marrow cells. J Thorac Cardiovasc Surg. 2005;129:1330–8.
- Zentilin L, Tafuro S, Zacchigna S, Arsic N, Pattarini L, Sinigaglia M, et al. Bone marrow mononuclear cells are recruited to the sites of VEGF-induced neovascularization but are not incorporated into the newly formed vessels. Blood. 2006;107:3546–54.
- Weber B, Scherman J, Emmert MY, Gruenenfelder J, Verbeek R, Bracher M, et al. Injectable living marrow stromal cell-based autologous tissue engineered heart valves: first experiences with a one-step intervention in primates. Eur Heart J. 2011;32(22):2830–40.
- Pansky A, Roitzheim B, Tobiasch E. Differentiation potential of adult human mesenchymal stem cells. Clin Lab. 2007;53(1-2):81–4
- Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, et al. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng. 2001;7:211–28.
- Colazzo F, Chester AH, Taylor PM, Yacoub MH. Induction of mesenchymal to endothelial transformation of adipose-derived stem cells. J Heart Valve Dis. 2010;19(6):736.
- Colazzo F, Sarathchandra P, Smolenski RT, Chester AH, Tseng YT, Czernuszka JT, et al. Extracellular matrix production by adipose-derived stem cells: implications for heart valve tissue engineering. Biomaterials. 2011;32(1):119–27.
- El-Hamamsy I, Balachandran K, Yacoub MH, Stevens LM, Sarathchandra P, Taylor PM, et al. Endothelium-dependent regulation of the mechanical properties of aortic valve cusps. J Am Coll Cardiol. 2009;53(16):1448–55.
- Kasimir MT, Weigel G, Sharma J, Rieder E, Seebacher G, Wolner E, et al. The decellularized porcine heart valve matrix in tissue engineering: platelet adhesion and activation. Thromb Haemost. 2005;94(3):469–70.
- Alsberg E, von Recum HA, Mahoney MJ. Environmental cues to guide stem cell fate decision for tissue engineering applications. Expert Opin Biol Ther. 2006;6:847–66.
- Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science. 1997;275(5302):964–7.
- Parolini O, Soncini M, Evangelista M, Schmidt D. Amniotic membrane and amniotic fluid-derived cells: potential tools for regenerative medicine? Regen Med. 2009;4(2):275–91.
- Kaviani A, Guleserian K, Perry TE, Jennings RW, Ziegler MM, Fauza DO. Fetal tissue engineering from amniotic fluid. J Am Coll Surg. 2003;196(4):592–7.
- Schmidt D, Achermann J, Odermatt B, Breymann C, Mol A, Genoni M, et al. Prenatally fabricated autologous human living heart valves based on amniotic fluid derived progenitor cells as single cell source. Circulation. 2007;11;116(11 Suppl):I64–70.
- Schmidt D, Achermann J, Odermatt B, Genoni M, Zund G, Hoerstrup SP. Cryopreserved amniotic fluid-derived cells: a lifelong autologous fetal stem cell source for heart valve tissue engineering. J Heart Valve Dis. 2008;17(4):446–55.
- De Coppi P, Bartsch G Jr, Siddiqui MM, Xu T, Santos CC, Perin L, et al. Isolation of amniotic stem cell lines with potential for therapy. Nat Biotechnol. 2007;25(1):100–6.
- Poloni A, Rosini V, Mondini E, Maurizi G, Mancini S, Discepoli G, et al. Characterization and expansion of mesenchymal progenitor cells from first-trimester chorionic villi of human placenta. Cytotherapy. 2008;10(7):690–7.
- Schmidt D, Mol A, Breymann C, Achermann J, Odermatt B, Gössi M, et al. Living autologous heart valves engineered from human prenatally harvested progenitors. Circulation. 2006;114(1 Suppl):I125–31.
- Erices A, Conget, P, Minguell JJ. Mesenchymal progenitor cells in human umbilical cord blood. Br J Haematol. 2000;109(1):235–42.
- Sodian R, Schaefermeier P, Abegg-Zips S, Kuebler WM, Shakibaei M, Daebritz S, et al. Use of human umbilical cord blood-derived progenitor cells for tissue-engineered heart valves. Ann Thorac Surg. 2010;89(3):819–28.
- Buchheiser A, Liedtke S, Looijenga LH, Kögler G. Cord blood for tissue regeneration. J Cell Biochem. 2009;108(4):762–8.
- Schmidt D, Mol A, Neuenschwander S, Breymann C, Gössi M, Zund G, Turina M, et al. Living patches engineered from human umbilical cord derived fibroblasts and endothelial progenitor cells. Eur J Cardiothorac Surg. 2005;27(5):795–800.
- Schmidt D, Asmis LM, Odermatt B, Kelm J, Breymann C, Gössi M et al. Engineered living blood vessels: functional endothelia generated from human umbilical cord-derived progenitors. Ann Thorac Surg. 2006;82(4):1465–71.
- Schmidt D, Mol A, Odermatt B, Neuenschwander S, Breymann C, Gössi M et al. Engineering of biologically active living heart valve leaflets using human umbilical cord-derived progenitor cells. Tissue Eng. 2006;12(11):3223–32.
- Wang HS, Hung SC, Peng ST, Huang CC, Wei HM, Guo YJ, et al. Mesenchymal stem cells in Wharton’s jelly of the human umbilical cord. Stem Cells. 2004;22:1330–37.
- Kögler G, Sensken S, Airey JA, Trapp T, Müschen M, Feldhahn N, et al. A new human somatic stem cell from placental cord blood with intrinsic pluripotent differentiation potential. J Exp Med. 2004;200:123–35.
- Weiss ML, Anderson C, Medicetty S, et al. Immune properties of human umbilical cord Wharton’s jelly-derived cells. Stem Cells. 2008;26:2865–74.
- Weber B, Schoenauer R, Papadopulos F, Modregger P, Peter S, Stampanoni M, et al. Engineering of living autologous human umbilical cord cell-based septal occluder membranes using composite PGA-P4HB matrices. Biomaterials. 2011;32(36):9630–41.
- Sodian R, Lueders C, Kraemer L, Kuebler W, Shakibaei M, Reichart B, et al. Tissue engineering of autologous human heart valves using cryopreserved vascular umbilical cord cells. Ann Thorac Surg. 2006;81(6):2207–16.
- Forsberg M, Hovatta O. Challenges for the therapeutic use of pluripotent stem derived cells. Front Physiol. 2012;3:19.
- Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006;25;126(4):663–76.
- Hibino N, Duncan DR, Nalbandian A, Yi T, Qyang Y, Shin’oka T, et al. Evaluation of the use of an induced pluripotent stem cell sheet for the construction of tissue-engineered vascular grafts. J Thorac Cardiovasc Surg. 2012;1:11.
- Drews K, Jozefczuk J, Prigione A, Adjaye J. Human induced pluripotent stem cells – from mechanisms to clinical applications. J Mol Med (Berl). 2012 May 30.
- Cheung C, Bernardo AS, Trotter MW, Pedersen RA, Sinha S. Generation of human vascular smooth muscle subtypes provides insight into embryological origin-dependent disease susceptibility. Nat Biotechnol. 2012;30(2):165–73.
- Ieda M, Fu JD, Delgado-Olguin P, Vedantham V, Hayashi Y, Bruneau BG, et al. Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors. Cell. 2010;142(3):375–86.
- Efe JA, Hilcove S, Kim J, Zhou H, Ouyang K, Wang G, et al. Conversion of mouse fibroblasts into cardiomyocytes using a direct reprogramming strategy. Nat Cell Biol. 2011;13(3):215–22.