Cellular and Molecular Life Sciences

, Volume 69, Issue 16, pp 2635–2656 | Cite as

Regenerating functional heart tissue for myocardial repair

Review

Abstract

Heart disease is one of the leading causes of death worldwide and the number of patients with the disease is likely to grow with the continual decline in health for most of the developed world. Heart transplantation is one of the only treatment options for heart failure due to an acute myocardial infarction, but limited donor supply and organ rejection limit its widespread use. Cellular cardiomyoplasty, or cellular implantation, combined with various tissue-engineering methods aims to regenerate functional heart tissue. This review highlights the numerous cell sources that have been used to regenerate the heart as well as cover the wide range of tissue-engineering strategies that have been devised to optimize the delivery of these cells. It will probably be a long time before an effective regenerative therapy can make a serious impact at the bedside.

Keywords

Myocardial repair Tissue engineering Tissue regeneration Heart tissue Cardiac tissue Heart repair Heart regeneration 

Abbreviations

CABG

Coronary artery bypass graft

ESC

Embryonic stem cells

HSC

Hematopoietic stem cells

hESC-CM

Human embryonic stem cell-derived cardiomyocytes

iPSC

Induced pluripotent stem cells

Isl-1

Islet 1 transcription factor

LAD

Left anterior descending

LVAD

Left ventricular assist device

LVEDV

Left ventricular end-diastolic volume

LVEF

Left ventricular ejection fraction

MI

Myocardial infarct

PCL

Poly ε-caprolactone

PGA

Polyglycolic acid

PIPAAm

Poly(N-isopropylacrylamide)

PLA

Polylactic acid

Sca-1

Stem cell antigen 1

Tbx18

T-box transcription factor 18

TB4

Thymosin-β4

TMRM

Tetramethylrhodamine methyl ester perchlorate

Wt1

Wilm’s tumor 1

References

  1. 1.
    Lloyd-Jones D, Adams RJ, Brown TM, Carnethon M, Dai S, De Simone G, Ferguson TB, Ford E, Furie K, Gillespie C, Go A, Greenlund K, Haase N, Hailpern S, Ho PM, Howard V, Kissela B, Kittner S, Lackland D, Lisabeth L, Marelli A, McDermott MM, Meigs J, Mozaffarian D, Mussolino M, Nichol G, Roger VL, Rosamond W, Sacco R, Sorlie P, Roger VL, Thom T, Wasserthiel-Smoller S, Wong ND, Wylie-Rosett J (2010) Heart disease and stroke statistics—2010 update: a report from the American heart association. Circulation 121(7):e46–e215PubMedGoogle Scholar
  2. 2.
    van den Borne SW, Diez J, Blankesteijn WM, Verjans J, Hofstra L, Narula J (2010) Myocardial remodeling after infarction: the role of myofibroblasts. Nat Rev Cardiol 7(1):30–37PubMedGoogle Scholar
  3. 3.
    Wang H, Zhou J, Liu Z, Wang C (2010) Injectable cardiac tissue engineering for the treatment of myocardial infarction. J Cell Mol Med 14(5):1044–1055PubMedGoogle Scholar
  4. 4.
    Sui R, Liao X, Zhou X, Tan Q (2011) The current status of engineering myocardial tissue. Stem Cell Rev 7(1):172–180PubMedGoogle Scholar
  5. 5.
    Caccamo M, Eckman P, John R (2011) Current state of ventricular assist devices. Curr Heart Fail Rep 8(2):91–98PubMedGoogle Scholar
  6. 6.
    Durrani S, Konoplyannikov M, Ashraf M, Haider KH (2010) Skeletal myoblasts for cardiac repair. Regen Med 5(6):919–932PubMedGoogle Scholar
  7. 7.
    Orlic D, Kajstura J, Chimenti S, Jakoniuk I, Anderson SM, Li B, Pickel J, McKay R, Nadal-Ginard B, Bodine DM, Leri A, Anversa P (2001) Bone marrow cells regenerate infarcted myocardium. Nature 410(6829):701–705PubMedGoogle Scholar
  8. 8.
    van Laake LW, Passier R, Doevendans PA, Mummery CL (2008) Human embryonic stem cell-derived cardiomyocytes and cardiac repair in rodents. Circ Res 102(9):1008–1010PubMedGoogle Scholar
  9. 9.
    Singla DK, Long X, Glass C, Singla RD, Yan B (2011) Induced pluripotent stem (iPS) cells repair and regenerate infarcted myocardium. Mol Pharm 8(5):1573–1581PubMedGoogle Scholar
  10. 10.
    Laugwitz KL, Moretti A, Lam J, Gruber P, Chen Y, Woodard S, Lin LZ, Cai CL, Lu MM, Reth M, Platoshyn O, Yuan JX, Evans S, Chien KR (2005) Postnatal isl1+ cardioblasts enter fully differentiated cardiomyocyte lineages. Nature 433(7026):647–653PubMedGoogle Scholar
  11. 11.
    Smart N, Bollini S, Dube KN, Vieira JM, Zhou B, Davidson S, Yellon D, Riegler J, Price AN, Lythgoe MF, Pu WT, Riley PR (2011) De novo cardiomyocytes from within the activated adult heart after injury. Nature 474(7353):640–644PubMedGoogle Scholar
  12. 12.
    Beltrami AP, Barlucchi L, Torella D, Baker M, Limana F, Chimenti S, Kasahara H, Rota M, Musso E, Urbanek K, Leri A, Kajstura J, Nadal-Ginard B, Anversa P (2003) Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 114(6):763–776PubMedGoogle Scholar
  13. 13.
    Matsuura K, Nagai T, Nishigaki N, Oyama T, Nishi J, Wada H, Sano M, Toko H, Akazawa H, Sato T, Nakaya H, Kasanuki H, Komuro I (2004) Adult cardiac Sca-1-positive cells differentiate into beating cardiomyocytes. J Biol Chem 279(12):11384–11391PubMedGoogle Scholar
  14. 14.
    Shimizu T, Yamato M, Kikuchi A, Okano T (2001) Two-dimensional manipulation of cardiac myocyte sheets utilizing temperature-responsive culture dishes augments the pulsatile amplitude. Tissue Eng 7(2):141–151PubMedGoogle Scholar
  15. 15.
    Zhang Y, Thorn S, DaSilva JN, Lamoureux M, DeKemp RA, Beanlands RS, Ruel M, Suuronen EJ (2008) Collagen-based matrices improve the delivery of transplanted circulating progenitor cells: development and demonstration by ex vivo radionuclide cell labeling and in vivo tracking with positron-emission tomography. Circ Cardiovasc Imaging 1(3):197–204PubMedGoogle Scholar
  16. 16.
    Ryu JH, Kim IK, Cho SW, Cho MC, Hwang KK, Piao H, Piao S, Lim SH, Hong YS, Choi CY, Yoo KJ, Kim BS (2005) Implantation of bone marrow mononuclear cells using injectable fibrin matrix enhances neovascularization in infarcted myocardium. Biomaterials 26(3):319–326PubMedGoogle Scholar
  17. 17.
    Lu WN, Lu SH, Wang HB, Li DX, Duan CM, Liu ZQ, Hao T, He WJ, Xu B, Fu Q, Song YC, Xie XH, Wang CY (2009) Functional improvement of infarcted heart by co-injection of embryonic stem cells with temperature-responsive chitosan hydrogel. Tissue Eng Part A 15(6):1437–1447PubMedGoogle Scholar
  18. 18.
    Guo HD, Cui GH, Wang HJ, Tan YZ (2010) Transplantation of marrow-derived cardiac stem cells carried in designer self-assembling peptide nanofibers improves cardiac function after myocardial infarction. Biochem Biophys Res Commun 399(1):42–48PubMedGoogle Scholar
  19. 19.
    Hansson EM, Lindsay ME, Chien KR (2009) Regeneration next: toward heart stem cell therapeutics. Cell Stem Cell 5(4):364–377PubMedGoogle Scholar
  20. 20.
    Riminton DS, Hartung HP, Reddel SW (2011) Managing the risks of immunosuppression. Curr Opin Neurol 24(3):217–223PubMedGoogle Scholar
  21. 21.
    Reinecke H, MacDonald GH, Hauschka SD, Murry CE (2000) Electromechanical coupling between skeletal and cardiac muscle. Implications for infarct repair. J Cell Biol 149(3):731–740PubMedGoogle Scholar
  22. 22.
    Murry CE, Soonpaa MH, Reinecke H, Nakajima H, Nakajima HO, Rubart M, Pasumarthi KB, Virag JI, Bartelmez SH, Poppa V, Bradford G, Dowell JD, Williams DA, Field LJ (2004) Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature 428(6983):664–668PubMedGoogle Scholar
  23. 23.
    Reinecke H, Poppa V, Murry CE (2002) Skeletal muscle stem cells do not transdifferentiate into cardiomyocytes after cardiac grafting. J Mol Cell Cardiol 34(2):241–249PubMedGoogle Scholar
  24. 24.
    Moretti A, Caron L, Nakano A, Lam JT, Bernshausen A, Chen Y, Qyang Y, Bu L, Sasaki M, Martin-Puig S, Sun Y, Evans SM, Laugwitz KL, Chien KR (2006) Multipotent embryonic isl1+ progenitor cells lead to cardiac, smooth muscle, and endothelial cell diversification. Cell 127(6):1151–1165PubMedGoogle Scholar
  25. 25.
    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(6):877–889PubMedGoogle Scholar
  26. 26.
    Passier R, Denning C, Mummery C (2006) Cardiomyocytes from human embryonic stem cells. Handb Exp Pharmacol 174:101–122PubMedGoogle Scholar
  27. 27.
    Zhang J, Wilson GF, Soerens AG, Koonce CH, Yu J, Palecek SP, Thomson JA, Kamp TJ (2009) Functional cardiomyocytes derived from human induced pluripotent stem cells. Circ Res 104(4):e30–e41PubMedGoogle Scholar
  28. 28.
    Moretti A, Bellin M, Jung CB, Thies TM, Takashima Y, Bernshausen A, Schiemann M, Fischer S, Moosmang S, Smith AG, Lam JT, Laugwitz KL (2010) Mouse and human induced pluripotent stem cells as a source for multipotent Isl1+ cardiovascular progenitors. FASEB J 24(3):700–711PubMedGoogle Scholar
  29. 29.
    Csete M (2010) Translational prospects for human induced pluripotent stem cells. Regen Med 5(4):509–519PubMedGoogle Scholar
  30. 30.
    Murry CE, Whitney ML, Reinecke H (2002) Muscle cell grafting for the treatment and prevention of heart failure. J Card Fail 8(Suppl 6):S532–S541PubMedGoogle Scholar
  31. 31.
    Menasche P, Hagege AA, Vilquin JT, Desnos M, Abergel E, Pouzet B, Bel A, Sarateanu S, Scorsin M, Schwartz K, Bruneval P, Benbunan M, Marolleau JP, Duboc D (2003) Autologous skeletal myoblast transplantation for severe postinfarction left ventricular dysfunction. J Am Coll Cardiol 41(7):1078–1083PubMedGoogle Scholar
  32. 32.
    Dib N, Michler RE, Pagani FD, Wright S, Kereiakes DJ, Lengerich R, Binkley P, Buchele D, Anand I, Swingen C, Di Carli MF, Thomas JD, Jaber WA, Opie SR, Campbell A, McCarthy P, Yeager M, Dilsizian V, Griffith BP, Korn R, Kreuger SK, Ghazoul M, MacLellan WR, Fonarow G, Eisen HJ, Dinsmore J, Diethrich E (2005) Safety and feasibility of autologous myoblast transplantation in patients with ischemic cardiomyopathy: four-year follow-up. Circulation 112(12):1748–1755PubMedGoogle Scholar
  33. 33.
    Menasche P, Alfieri O, Janssens S, McKenna W, Reichenspurner H, Trinquart L, Vilquin JT, Marolleau JP, Seymour B, Larghero J, Lake S, Chatellier G, Solomon S, Desnos M, Hagege AA (2008) The myoblast autologous grafting in ischemic cardiomyopathy (MAGIC) trial: first randomized placebo-controlled study of myoblast transplantation. Circulation 117(9):1189–1200PubMedGoogle Scholar
  34. 34.
    Reinecke H, Murry CE (2000) Transmural replacement of myocardium after skeletal myoblast grafting into the heart. Too much of a good thing? Cardiovasc Pathol 9(6):337–344PubMedGoogle Scholar
  35. 35.
    Zhang M, Methot D, Poppa V, Fujio Y, Walsh K, Murry CE (2001) Cardiomyocyte grafting for cardiac repair: graft cell death and anti-death strategies. J Mol Cell Cardiol 33(5):907–921PubMedGoogle Scholar
  36. 36.
    Chiu RC, Zibaitis A, Kao RL (1995) Cellular cardiomyoplasty: myocardial regeneration with satellite cell implantation. Ann Thorac Surg 60(1):12–18PubMedGoogle Scholar
  37. 37.
    DA Taylor AB, Hungspreugs P, Jones TR, Reedy MC, Hutcheson KA, Glower DD, Kraus WE (1998) Regenerating functional myocardium—improved performance after skeletal myoblast transplantation. Nat Med 4(8):929–933PubMedGoogle Scholar
  38. 38.
    Pouzet B, Vilquin JT, Hagege AA, Scorsin M, Messas E, Fiszman M, Schwartz K, Menasche P (2001) Factors affecting functional outcome after autologous skeletal myoblast transplantation. Ann Thorac Surg 71(3):844–850 (discussion 841–850)PubMedGoogle Scholar
  39. 39.
    Ghostine S, Carrion C, Souza LC, Richard P, Bruneval P, Vilquin JT, Pouzet B, Schwartz K, Menasche P, Hagege AA (2002) Long-term efficacy of myoblast transplantation on regional structure and function after myocardial infarction. Circulation 106(12 Suppl 1):I131–I136PubMedGoogle Scholar
  40. 40.
    Gavira JJ, Herreros J, Perez A, Garcia-Velloso MJ, Barba J, Martin-Herrero F, Canizo C, Martin-Arnau A, Marti-Climent JM, Hernandez M, Lopez-Holgado N, Gonzalez-Santos JM, Martin-Luengo C, Alegria E, Prosper F (2006) Autologous skeletal myoblast transplantation in patients with nonacute myocardial infarction: 1-year follow-up. J Thorac Cardiovasc Surg 131(4):799–804PubMedGoogle Scholar
  41. 41.
    Smits PC, van Geuns RJ, Poldermans D, Bountioukos M, Onderwater EE, Lee CH, Maat AP, Serruys PW (2003) Catheter-based intramyocardial injection of autologous skeletal myoblasts as a primary treatment of ischemic heart failure: clinical experience with six-month follow-up. J Am Coll Cardiol 42(12):2063–2069Google Scholar
  42. 42.
    Jackson KA, Majka SM, Wang H, Pocius J, Hartley CJ, Majesky MW, Entman ML, Michael LH, Hirschi KK, Goodell MA (2001) Regeneration of ischemic cardiac muscle and vascular endothelium by adult stem cells. J Clin Invest 107(11):1395–1402PubMedGoogle Scholar
  43. 43.
    Balsam LB, Wagers AJ, Christensen JL, Kofidis T, Weissman IL, Robbins RC (2004) Haematopoietic stem cells adopt mature haematopoietic fates in ischaemic myocardium. Nature 428(6983):668–673PubMedGoogle Scholar
  44. 44.
    Alvarez-Dolado MPR, Garcia-Verdugo JM, Fike JR, Lee HO, Pfeffer K, Lois C, Morrison SJ, Alvarez-Buylla A (2003) Fusion of bone-marrow-derived cells with Purkinje neurons, cardiomyocytes and hepatocytes. Nature 425(6961):968–973PubMedGoogle Scholar
  45. 45.
    Terada N, Hamazaki T, Oka M, Hoki M, Mastalerz DM, Nakano Y, Meyer EM, Morel L, Petersen BE, Scott EW (2002) Bone marrow cells adopt the phenotype of other cells by spontaneous cell fusion. Nature 416(6880):542–545PubMedGoogle Scholar
  46. 46.
    Nygren JM, Jovinge S, Breitbach M, Sawen P, Roll W, Hescheler J, Taneera J, Fleischmann BK, Jacobsen SE (2004) Bone marrow-derived hematopoietic cells generate cardiomyocytes at a low frequency through cell fusion, but not transdifferentiation. Nat Med 10(5):494–501PubMedGoogle Scholar
  47. 47.
    Strauer BE (2002) Repair of infarcted myocardium by autologous intracoronary mononuclear bone marrow cell transplantation in humans. Circulation 106(15):1913–1918PubMedGoogle Scholar
  48. 48.
    Assmus B (2002) Transplantation of progenitor cells and regeneration enhancement in acute myocardial infarction (TOPCARE-AMI). Circulation 106(24):3009–3017PubMedGoogle Scholar
  49. 49.
    Leistner DM, Fischer-Rasokat U, Honold J, Seeger FH, Schachinger V, Lehmann R, Martin H, Burck I, Urbich C, Dimmeler S, Zeiher AM, Assmus B (2011) Transplantation of progenitor cells and regeneration enhancement in acute myocardial infarction (TOPCARE-AMI): final 5-year results suggest long-term safety and efficacy. Clin Res Cardiol 100(10):925–934PubMedGoogle Scholar
  50. 50.
    Zhang C, Sun A, Zhang S, Yao K, Wu C, Fu M, Wang K, Zou Y, Ge J (2010) Efficacy and safety of intracoronary autologous bone marrow-derived cell transplantation in patients with acute myocardial infarction: insights from randomized controlled trials with 12 or more months follow-up. Clin Cardiol 33(6):353–360PubMedGoogle Scholar
  51. 51.
    Kinnaird T, Stabile E, Burnett MS, Shou M, Lee CW, Barr S, Fuchs S, Epstein SE (2004) Local delivery of marrow-derived stromal cells augments collateral perfusion through paracrine mechanisms. Circulation 109(12):1543–1549PubMedGoogle Scholar
  52. 52.
    Tang YL, Zhao Q, Zhang YC, Cheng L, Liu M, Shi J, Yang YZ, Pan C, Ge J, Phillips MI (2004) Autologous mesenchymal stem cell transplantation induce VEGF and neovascularization in ischemic myocardium. Regul Pept 117(1):3–10PubMedGoogle Scholar
  53. 53.
    Fazel S, Cimini M, Chen L, Li S, Angoulvant D, Fedak P, Verma S, Weisel RD, Keating A, Li RK (2006) Cardioprotective c-kit+ cells are from the bone marrow and regulate the myocardial balance of angiogenic cytokines. J Clin Invest 116(7):1865–1877PubMedGoogle Scholar
  54. 54.
    Gnecchi M, He H, Liang OD, Melo LG, Morello F, Mu H, Noiseux N, Zhang L, Pratt RE, Ingwall JS, Dzau VJ (2005) Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells. Nat Med 11(4):367–368PubMedGoogle Scholar
  55. 55.
    Uemura R, Xu M, Ahmad N, Ashraf M (2006) Bone marrow stem cells prevent left ventricular remodeling of ischemic heart through paracrine signaling. Circ Res 98(11):1414–1421PubMedGoogle Scholar
  56. 56.
    Trachtenberg B, Velazquez DL, Williams AR, McNiece I, Fishman J, Nguyen K, Rouy D, Altman P, Schwarz R, Mendizabal A, Oskouei B, Byrnes J, Soto V, Tracy M, Zambrano JP, Heldman AW, Hare JM (2011) Rationale and design of the transendocardial injection of autologous human cells (bone marrow or mesenchymal) in chronic ischemic left ventricular dysfunction and heart failure secondary to myocardial infarction (TAC-HFT) trial: a randomized, double-blind, placebo-controlled study of safety and efficacy. Am Heart J 161(3):487–493PubMedGoogle Scholar
  57. 57.
    Bergmann O, Bhardwaj RD, Bernard S, Zdunek S, Barnabe-Heider F, Walsh S, Zupicich J, Alkass K, Buchholz BA, Druid H, Jovinge S, Frisen J (2009) Evidence for cardiomyocyte renewal in humans. Science 324(5923):98–102PubMedGoogle Scholar
  58. 58.
    Kajstura J, Urbanek K, Perl S, Hosoda T, Zheng H, Ogorek B, Ferreira-Martins J, Goichberg P, Rondon-Clavo C, Sanada F, D’Amario D, Rota M, Del Monte F, Orlic D, Tisdale J, Leri A, Anversa P (2010) Cardiomyogenesis in the adult human heart. Circ Res 107(2):305–315PubMedGoogle Scholar
  59. 59.
    Quaini F, Urbanek K, Beltrami AP, Finato N, Beltrami CA, Nadal-Ginard B, Kajstura J, Leri A, Anversa P (2002) Chimerism of the transplanted heart. N Engl J Med 346(1):5–15PubMedGoogle Scholar
  60. 60.
    Tillmanns J, Rota M, Hosoda T, Misao Y, Esposito G, Gonzalez A, Vitale S, Parolin C, Yasuzawa-Amano S, Muraski J, De Angelis A, Lecapitaine N, Siggins RW, Loredo M, Bearzi C, Bolli R, Urbanek K, Leri A, Kajstura J, Anversa P (2008) Formation of large coronary arteries by cardiac progenitor cells. Proc Natl Acad Sci USA 105(5):1668–1673PubMedGoogle Scholar
  61. 61.
    Dawn B, Stein AB, Urbanek K, Rota M, Whang B, Rastaldo R, Torella D, Tang XL, Rezazadeh A, Kajstura J, Leri A, Hunt G, Varma J, Prabhu SD, Anversa P, Bolli R (2005) Cardiac stem cells delivered intravascularly traverse the vessel barrier, regenerate infarcted myocardium, and improve cardiac function. Proc Natl Acad Sci USA 102(10):3766–3771PubMedGoogle Scholar
  62. 62.
    Oh H, Bradfute SB, Gallardo TD, Nakamura T, Gaussin V, Mishina Y, Pocius J, Michael LH, Behringer RR, Garry DJ, Entman ML, Schneider MD (2003) Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proc Natl Acad Sci USA 100(21):12313–12318PubMedGoogle Scholar
  63. 63.
    Martin CM, Meeson AP, Robertson SM, Hawke TJ, Richardson JA, Bates S, Goetsch SC, Gallardo TD, Garry DJ (2004) Persistent expression of the ATP-binding cassette transporter, Abcg2, identifies cardiac SP cells in the developing and adult heart. Dev Biol 265(1):262–275PubMedGoogle Scholar
  64. 64.
    Urbanek K, Rota M, Cascapera S, Bearzi C, Nascimbene A, De Angelis A, Hosoda T, Chimenti S, Baker M, Limana F, Nurzynska D, Torella D, Rotatori F, Rastaldo R, Musso E, Quaini F, Leri A, Kajstura J, Anversa P (2005) Cardiac stem cells possess growth factor-receptor systems that after activation regenerate the infarcted myocardium, improving ventricular function and long-term survival. Circ Res 97(7):663–673PubMedGoogle Scholar
  65. 65.
    Messina E, De Angelis L, Frati G, Morrone S, Chimenti S, Fiordaliso F, Salio M, Battaglia M, Latronico MV, Coletta M, Vivarelli E, Frati L, Cossu G, Giacomello A (2004) Isolation and expansion of adult cardiac stem cells from human and murine heart. Circ Res 95(9):911–921PubMedGoogle Scholar
  66. 66.
    Massberg S, Schaerli P, Knezevic-Maramica I, Kollnberger M, Tubo N, Moseman EA, Huff IV, Junt T, Wagers AJ, Mazo IB, von Andrian UH (2007) Immunosurveillance by hematopoietic progenitor cells trafficking through blood, lymph, and peripheral tissues. Cell 131(5):994–1008PubMedGoogle Scholar
  67. 67.
    Pouly J, Bruneval P, Mandet C, Proksch S, Peyrard S, Amrein C, Bousseaux V, Guillemain R, Deloche A, Fabiani JN, Menasche P (2008) Cardiac stem cells in the real world. J Thorac Cardiovasc Surg 135(3):673–678PubMedGoogle Scholar
  68. 68.
    Bu L, Jiang X, Martin-Puig S, Caron L, Zhu S, Shao Y, Roberts DJ, Huang PL, Domian IJ, Chien KR (2009) Human ISL1 heart progenitors generate diverse multipotent cardiovascular cell lineages. Nature 460(7251):113–117PubMedGoogle Scholar
  69. 69.
    Qyang Y, Martin-Puig S, Chiravuri M, Chen S, Xu H, Bu L, Jiang X, Lin L, Granger A, Moretti A, Caron L, Wu X, Clarke J, Taketo MM, Laugwitz KL, Moon RT, Gruber P, Evans SM, Ding S, Chien KR (2007) The renewal and differentiation of Isl1+ cardiovascular progenitors are controlled by a Wnt/beta-catenin pathway. Cell Stem Cell 1(2):165–179PubMedGoogle Scholar
  70. 70.
    Martin-Puig S, Wang Z, Chien KR (2008) Lives of a heart cell: tracing the origins of cardiac progenitors. Cell Stem Cell 2(4):320–331PubMedGoogle Scholar
  71. 71.
    Pfaff SL, Mendelsohn M, Stewart CL, Edlund T, Jessell TM (1996) Requirement for LIM homeobox gene Isl1 in motor neuron generation reveals a motor neuron-dependent step in interneuron differentiation. Cell 84(2):309–320PubMedGoogle Scholar
  72. 72.
    Ahlgren U, Pfaff SL, Jessell TM, Edlund T, Edlund H (1997) Independent requirement for ISL1 in formation of pancreatic mesenchyme and islet cells. Nature 385(6613):257–260PubMedGoogle Scholar
  73. 73.
    Genead R, Danielsson C, Andersson AB, Corbascio M, Franco-Cereceda A, Sylven C, Grinnemo KH (2010) Islet-1 cells are cardiac progenitors present during the entire lifespan: from the embryonic stage to adulthood. Stem Cells Dev 19(10):1601–1615PubMedGoogle Scholar
  74. 74.
    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(1):286–296PubMedGoogle Scholar
  75. 75.
    Chung J, Kee K, Barral JK, Dash R, Kosuge H, Wang X, Weissman I, Robbins RC, Nishimura D, Quertermous T, Reijo-Pera RA, Yang PC (2011) In vivo molecular MRI of cell survival and teratoma formation following embryonic stem cell transplantation into the injured murine myocardium. Magn Reson Med 66:1378–1381Google Scholar
  76. 76.
    Ueno S, Weidinger G, Osugi T, Kohn AD, Golob JL, Pabon L, Reinecke H, Moon RT, Murry CE (2007) Biphasic role for Wnt/beta-catenin signaling in cardiac specification in zebrafish and embryonic stem cells. Proc Natl Acad Sci USA 104(23):9685–9690PubMedGoogle Scholar
  77. 77.
    Kwon C, Arnold J, Hsiao EC, Taketo MM, Conklin BR, Srivastava D (2007) Canonical Wnt signaling is a positive regulator of mammalian cardiac progenitors. Proc Natl Acad Sci USA 104(26):10894–10899PubMedGoogle Scholar
  78. 78.
    Ai D, Fu X, Wang J, Lu MF, Chen L, Baldini A, Klein WH, Martin JF (2007) Canonical Wnt signaling functions in second heart field to promote right ventricular growth. Proc Natl Acad Sci USA 104(22):9319–9324PubMedGoogle Scholar
  79. 79.
    Lin L, Cui L, Zhou W, Dufort D, Zhang X, Cai CL, Bu L, Yang L, Martin J, Kemler R, Rosenfeld MG, Chen J, Evans SM (2007) Beta-catenin directly regulates Islet1 expression in cardiovascular progenitors and is required for multiple aspects of cardiogenesis. Proc Natl Acad Sci USA 104(22):9313–9318PubMedGoogle Scholar
  80. 80.
    Cohen ED, Wang Z, Lepore JJ, Lu MM, Taketo MM, Epstein DJ, Morrisey EE (2007) Wnt/beta-catenin signaling promotes expansion of Isl-1-positive cardiac progenitor cells through regulation of FGF signaling. J Clin Invest 117(7):1794–1804PubMedGoogle Scholar
  81. 81.
    Barzelay A, Ben-Shoshan J, Entin-Meer M, Maysel-Auslender S, Afek A, Barshack I, Keren G, George J (2010) A potential role for islet-1 in post-natal angiogenesis and vasculogenesis. Thromb Haemost 103(1):188–197PubMedGoogle Scholar
  82. 82.
    Eschenhagen T, Zimmermann WH (2005) Engineering myocardial tissue. Circ Res 97(12):1220–1231PubMedGoogle Scholar
  83. 83.
    Itzhaki-Alfia A, Leor J, Raanani E, Sternik L, Spiegelstein D, Netser S, Holbova R, Pevsner-Fischer M, Lavee J, Barbash IM (2009) Patient characteristics and cell source determine the number of isolated human cardiac progenitor cells. Circulation 120(25):2559–2566PubMedGoogle Scholar
  84. 84.
    Ma Q, Zhou B, Pu WT (2008) Reassessment of Isl1 and Nk2–5 cardiac fate maps using a Gata4-based reporter of Cre activity. Dev Biol 323(1):98–104PubMedGoogle Scholar
  85. 85.
    Prall OW, Menon MK, Solloway MJ, Watanabe Y, Zaffran S, Bajolle F, Biben C, McBride JJ, Robertson BR, Chaulet H, Stennard FA, Wise N, Schaft D, Wolstein O, Furtado MB, Shiratori H, Chien KR, Hamada H, Black BL, Saga Y, Robertson EJ, Buckingham ME, Harvey RP (2007) An Nk2–5/Bmp2/Smad1 negative feedback loop controls heart progenitor specification and proliferation. Cell 128(5):947–959PubMedGoogle Scholar
  86. 86.
    Zhou B, Ma Q, Rajagopal S, Wu SM, Domian I, Rivera-Feliciano J, Jiang D, von Gise A, Ikeda S, Chien KR, Pu WT (2008) Epicardial progenitors contribute to the cardiomyocyte lineage in the developing heart. Nature 454(7200):109–113PubMedGoogle Scholar
  87. 87.
    Cai CL, Martin JC, Sun Y, Cui L, Wang L, Ouyang K, Yang L, Bu L, Liang X, Zhang X, Stallcup WB, Denton CP, McCulloch A, Chen J, Evans SM (2008) A myocardial lineage derives from Tbx18 epicardial cells. Nature 454(7200):104–108PubMedGoogle Scholar
  88. 88.
    Smart N, Risebro CA, Melville AA, Moses K, Schwartz RJ, Chien KR, Riley PR (2007) Thymosin beta4 induces adult epicardial progenitor mobilization and neovascularization. Nature 445(7124):177–182PubMedGoogle Scholar
  89. 89.
    Bock-Marquette I, Saxena A, White MD, Dimaio JM, Srivastava D (2004) Thymosin beta4 activates integrin-linked kinase and promotes cardiac cell migration, survival and cardiac repair. Nature 432(7016):466–472PubMedGoogle Scholar
  90. 90.
    Bock-Marquette I, Shrivastava S, Pipes GC, Thatcher JE, Blystone A, Shelton JM, Galindo CL, Melegh B, Srivastava D, Olson EN, DiMaio JM (2009) Thymosin beta4 mediated PKC activation is essential to initiate the embryonic coronary developmental program and epicardial progenitor cell activation in adult mice in vivo. J Mol Cell Cardiol 46(5):728–738PubMedGoogle Scholar
  91. 91.
    Kehat I (2001) Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes. J Clin Investig 108(3):407–414PubMedGoogle Scholar
  92. 92.
    Fernandes S, Naumova AV, Zhu WZ, Laflamme MA, Gold J, Murry CE (2010) Human embryonic stem cell-derived cardiomyocytes engraft but do not alter cardiac remodeling after chronic infarction in rats. J Mol Cell Cardiol 49(6):941–949PubMedGoogle Scholar
  93. 93.
    van Laake LW, Passier R, Monshouwer-Kloots J, Verkleij AJ, Lips DJ, Freund C, den Ouden K, Ward-van Oostwaard D, Korving J, Tertoolen LG, van Echteld CJ, Doevendans PA, Mummery CL (2007) Human embryonic stem cell-derived cardiomyocytes survive and mature in the mouse heart and transiently improve function after myocardial infarction. Stem Cell Res 1(1):9–24PubMedGoogle Scholar
  94. 94.
    Laflamme MA, Chen KY, Naumova AV, Muskheli V, Fugate JA, Dupras SK, Reinecke H, Xu C, Hassanipour M, Police S, O’Sullivan C, Collins L, Chen Y, Minami E, Gill EA, Ueno S, Yuan C, Gold J, Murry CE (2007) Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat Biotechnol 25(9):1015–1024PubMedGoogle Scholar
  95. 95.
    Caspi O, Huber I, Kehat I, Habib M, Arbel G, Gepstein A, Yankelson L, Aronson D, Beyar R, Gepstein L (2007) Transplantation of human embryonic stem cell-derived cardiomyocytes improves myocardial performance in infarcted rat hearts. J Am Coll Cardiol 50(19):1884–1893PubMedGoogle Scholar
  96. 96.
    Laflamme MA, Gold J, Xu C, Hassanipour M, Rosler E, Police S, Muskheli V, Murry CE (2005) Formation of human myocardium in the rat heart from human embryonic stem cells. Am J Pathol 167(3):663–671PubMedGoogle Scholar
  97. 97.
    Kehat I, Khimovich L, Caspi O, Gepstein A, Shofti R, Arbel G, Huber I, Satin J, Itskovitz-Eldor J, Gepstein L (2004) Electromechanical integration of cardiomyocytes derived from human embryonic stem cells. Nat Biotechnol 22(10):1282–1289PubMedGoogle Scholar
  98. 98.
    Xu C (2002) Characterization and enrichment of cardiomyocytes derived from human embryonic stem cells. Circ Res 91(6):501–508PubMedGoogle Scholar
  99. 99.
    Ladd AN, Yatskievych TA, Antin PB (1998) Regulation of avian cardiac myogenesis by activin/TGFbeta and bone morphogenetic proteins. Dev Biol 204(2):407–419PubMedGoogle Scholar
  100. 100.
    Yang L, Soonpaa MH, Adler ED, Roepke TK, Kattman SJ, Kennedy M, Henckaerts E, Bonham K, Abbott GW, Linden RM, Field LJ, Keller GM (2008) Human cardiovascular progenitor cells develop from a KDR+ embryonic-stem-cell-derived population. Nature 453(7194):524–528PubMedGoogle Scholar
  101. 101.
    Hattori F, Chen H, Yamashita H, Tohyama S, Satoh YS, Yuasa S, Li W, Yamakawa H, Tanaka T, Onitsuka T, Shimoji K, Ohno Y, Egashira T, Kaneda R, Murata M, Hidaka K, Morisaki T, Sasaki E, Suzuki T, Sano M, Makino S, Oikawa S, Fukuda K (2010) Nongenetic method for purifying stem cell-derived cardiomyocytes. Nat Methods 7(1):61–66PubMedGoogle Scholar
  102. 102.
    Mummery C, Ward-van Oostwaard D, Doevendans P, Spijker R, van den Brink S, Hassink R, van der Heyden M, Opthof T, Pera M, de la Riviere AB, Passier R, Tertoolen L (2003) Differentiation of human embryonic stem cells to cardiomyocytes: role of coculture with visceral endoderm-like cells. Circulation 107(21):2733–2740PubMedGoogle Scholar
  103. 103.
    Zimmermann WH, Schneiderbanger K, Schubert P, Didie M, Munzel F, Heubach JF, Kostin S, Neuhuber WL, Eschenhagen T (2002) Tissue engineering of a differentiated cardiac muscle construct. Circ Res 90(2):223–230PubMedGoogle Scholar
  104. 104.
    Pearl JI, Lee AS, Leveson-Gower DB, Sun N, Ghosh Z, Lan F, Ransohoff J, Negrin RS, Davis MM, Wu JC (2011) Short-term immunosuppression promotes engraftment of embryonic and induced pluripotent stem cells. Cell Stem Cell 8(3):309–317PubMedGoogle Scholar
  105. 105.
    Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131(5):861–872PubMedGoogle Scholar
  106. 106.
    Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, Nie J, Jonsdottir GA, Ruotti V, Stewart R, Slukvin II, Thomson JA (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318(5858):1917–1920PubMedGoogle Scholar
  107. 107.
    Zhao T, Zhang ZN, Rong Z, Xu Y (2011) Immunogenicity of induced pluripotent stem cells. Nature 474:212–215PubMedGoogle Scholar
  108. 108.
    Narazaki G, Uosaki H, Teranishi M, Okita K, Kim B, Matsuoka S, Yamanaka S, Yamashita JK (2008) Directed and systematic differentiation of cardiovascular cells from mouse induced pluripotent stem cells. Circulation 118(5):498–506PubMedGoogle Scholar
  109. 109.
    Mauritz C, Schwanke K, Reppel M, Neef S, Katsirntaki K, Maier LS, Nguemo F, Menke S, Haustein M, Hescheler J, Hasenfuss G, Martin U (2008) Generation of functional murine cardiac myocytes from induced pluripotent stem cells. Circulation 118(5):507–517PubMedGoogle Scholar
  110. 110.
    Ren Y, Lee MY, Schliffke S, Paavola J, Amos PJ, Ge X, Ye M, Zhu S, Senyei G, Lum L, Ehrlich BE, Qyang Y (2011) Small molecule Wnt inhibitors enhance the efficiency of BMP-4-directed cardiac differentiation of human pluripotent stem cells. J Mol Cell Cardiol 51(3):280–287PubMedGoogle Scholar
  111. 111.
    Stadtfeld M, Nagaya M, Utikal J, Weir G, Hochedlinger K (2008) Induced pluripotent stem cells generated without viral integration. Science 322(5903):945–949PubMedGoogle Scholar
  112. 112.
    Okita K, Nakagawa M, Hyenjong H, Ichisaka T, Yamanaka S (2008) Generation of mouse induced pluripotent stem cells without viral vectors. Science 322(5903):949–953PubMedGoogle Scholar
  113. 113.
    Kaji K, Norrby K, Paca A, Mileikovsky M, Mohseni P, Woltjen K (2009) Virus-free induction of pluripotency and subsequent excision of reprogramming factors. Nature 458(7239):771–775PubMedGoogle Scholar
  114. 114.
    Woltjen K, Michael IP, Mohseni P, Desai R, Mileikovsky M, Hamalainen R, Cowling R, Wang W, Liu P, Gertsenstein M, Kaji K, Sung HK, Nagy A (2009) piggyBac transposition reprograms fibroblasts to induced pluripotent stem cells. Nature 458(7239):766–770PubMedGoogle Scholar
  115. 115.
    Zhou H, Wu S, Joo JY, Zhu S, Han DW, Lin T, Trauger S, Bien G, Yao S, Zhu Y, Siuzdak G, Scholer HR, Duan L, Ding S (2009) Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem Cell 4(5):381–384PubMedGoogle Scholar
  116. 116.
    Warren L, Manos PD, Ahfeldt T, Loh YH, Li H, Lau F, Ebina W, Mandal PK, Smith ZD, Meissner A, Daley GQ, Brack AS, Collins JJ, Cowan C, Schlaeger TM, Rossi DJ (2010) Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA. Cell Stem Cell 7(5):618–630PubMedGoogle Scholar
  117. 117.
    Jia F, Wilson KD, Sun N, Gupta DM, Huang M, Li Z, Panetta NJ, Chen ZY, Robbins RC, Kay MA, Longaker MT, Wu JC (2010) A nonviral minicircle vector for deriving human iPS cells. Nat Methods 7(3):197–199PubMedGoogle Scholar
  118. 118.
    Polo JM, Liu S, Figueroa ME, Kulalert W, Eminli S, Tan KY, Apostolou E, Stadtfeld M, Li Y, Shioda T, Natesan S, Wagers AJ, Melnick A, Evans T, Hochedlinger K (2010) Cell type of origin influences the molecular and functional properties of mouse induced pluripotent stem cells. Nat Biotechnol 28(8):848–855PubMedGoogle Scholar
  119. 119.
    Kim EY, Jeon K, Park HY, Han YJ, Yang BC, Park SB, Chung HM, Park SP (2010) Differences between cellular and molecular profiles of induced pluripotent stem cells generated from mouse embryonic fibroblasts. Cell Reprogram 12(6):627–639PubMedGoogle Scholar
  120. 120.
    Chin MH, Mason MJ, Xie W, Volinia S, Singer M, Peterson C, Ambartsumyan G, Aimiuwu O, Richter L, Zhang J, Khvorostov I, Ott V, Grunstein M, Lavon N, Benvenisty N, Croce CM, Clark AT, Baxter T, Pyle AD, Teitell MA, Pelegrini M, Plath K, Lowry WE (2009) Induced pluripotent stem cells and embryonic stem cells are distinguished by gene expression signatures. Cell Stem Cell 5(1):111–123PubMedGoogle Scholar
  121. 121.
    Stadtfeld MNM, Utikal J, Weir G, Hochedlinger K (2008) Induced pluripotent stem cells generated without viral integration. Science 322(5903):945–949PubMedGoogle Scholar
  122. 122.
    Sullivan GJ, Bai Y, Fletcher J, Wilmut I (2010) Induced pluripotent stem cells: epigenetic memories and practical implications. Mol Hum Reprod 16(12):880–885PubMedGoogle Scholar
  123. 123.
    Kofidis T, Akhyari P, Boublik J, Theodorou P, Martin U, Ruhparwar A, Fischer S, Eschenhagen T, Kubis HP, Kraft T, Leyh R, Haverich A (2002) In vitro engineering of heart muscle: artificial myocardial tissue. J Thorac Cardiovasc Surg 124(1):63–69PubMedGoogle Scholar
  124. 124.
    Li RK, Jia ZQ, Weisel RD, Mickle DA, Choi A, Yau TM (1999) Survival and function of bioengineered cardiac grafts. Circulation 100(Suppl 19):II63–II69PubMedGoogle Scholar
  125. 125.
    Fukuhara S, Tomita S, Nakatani T, Fujisato T, Ohtsu Y, Ishida M, Yutani C, Kitamura S (2005) Bone marrow cell-seeded biodegradable polymeric scaffold enhances angiogenesis and improves function of the infarcted heart. Circ J 69(7):850–857PubMedGoogle Scholar
  126. 126.
    Alperin C, Zandstra PW, Woodhouse KA (2005) Polyurethane films seeded with embryonic stem cell-derived cardiomyocytes for use in cardiac tissue engineering applications. Biomaterials 26(35):7377–7386PubMedGoogle Scholar
  127. 127.
    Furuta A, Miyoshi S, Itabashi Y, Shimizu T, Kira S, Hayakawa K, Nishiyama N, Tanimoto K, Hagiwara Y, Satoh T, Fukuda K, Okano T, Ogawa S (2006) Pulsatile cardiac tissue grafts using a novel three-dimensional cell sheet manipulation technique functionally integrates with the host heart, in vivo. Circ Res 98(5):705–712PubMedGoogle Scholar
  128. 128.
    Miyagawa S, Sawa Y, Sakakida S, Taketani S, Kondoh H, Memon IA, Imanishi Y, Shimizu T, Okano T, Matsuda H (2005) Tissue cardiomyoplasty using bioengineered contractile cardiomyocyte sheets to repair damaged myocardium: their integration with recipient myocardium. Transplantation 80(11):1586–1595PubMedGoogle Scholar
  129. 129.
    Shimizu T, Yamato M, Akutsu T, Shibata T, Isoi Y, Kikuchi A, Umezu M, Okano T (2002) Electrically communicating three-dimensional cardiac tissue mimic fabricated by layered cultured cardiomyocyte sheets. J Biomed Mater Res 60(1):110–117PubMedGoogle Scholar
  130. 130.
    Miyagawa S, Roth M, Saito A, Sawa Y, Kostin S (2011) Tissue-engineered cardiac constructs for cardiac repair. Ann Thorac Surg 91(1):320–329PubMedGoogle Scholar
  131. 131.
    Kofidis T, de Bruin JL, Hoyt G, Lebl DR, Tanaka M, Yamane T, Chang CP, Robbins RC (2004) Injectable bioartificial myocardial tissue for large-scale intramural cell transfer and functional recovery of injured heart muscle. J Thorac Cardiovasc Surg 128(4):571–578PubMedGoogle Scholar
  132. 132.
    Landa N, Miller L, Feinberg MS, Holbova R, Shachar M, Freeman I, Cohen S, Leor J (2008) Effect of injectable alginate implant on cardiac remodeling and function after recent and old infarcts in rat. Circulation 117(11):1388–1396PubMedGoogle Scholar
  133. 133.
    Suuronen EJ, Veinot JP, Wong S, Kapila V, Price J, Griffith M, Mesana TG, Ruel M (2006) Tissue-engineered injectable collagen-based matrices for improved cell delivery and vascularization of ischemic tissue using CD133+ progenitors expanded from the peripheral blood. Circulation 114(Suppl 1):I138–I144PubMedGoogle Scholar
  134. 134.
    Leor J, Aboulafia-Etzion S, Dar A, Shapiro L, Barbash IM, Battler A, Granot Y, Cohen S (2000) Bioengineered cardiac grafts: a new approach to repair the infarcted myocardium? Circulation 102(19 Suppl 3):III56–III61PubMedGoogle Scholar
  135. 135.
    Dvir T, Kedem A, Ruvinov E, Levy O, Freeman I, Landa N, Holbova R, Feinberg MS, Dror S, Etzion Y, Leor J, Cohen S (2009) Prevascularization of cardiac patch on the omentum improves its therapeutic outcome. Proc Natl Acad Sci USA 106(35):14990–14995PubMedGoogle Scholar
  136. 136.
    Amir G, Miller L, Shachar M, Feinberg MS, Holbova R, Cohen S, Leor J (2009) Evaluation of a peritoneal-generated cardiac patch in a rat model of heterotopic heart transplantation. Cell Transplant 18(3):275–282PubMedGoogle Scholar
  137. 137.
    Eschenhagen T, Fink C, Remmers U, Scholz H, Wattchow J, Weil J, Zimmermann W, Dohmen HH, Schafer H, Bishopric N, Wakatsuki T, Elson EL (1997) Three-dimensional reconstitution of embryonic cardiomyocytes in a collagen matrix: a new heart muscle model system. FASEB J 11(8):683–694PubMedGoogle Scholar
  138. 138.
    Zimmermann WH, Fink C, Kralisch D, Remmers U, Weil J, Eschenhagen T (2000) Three-dimensional engineered heart tissue from neonatal rat cardiac myocytes. Biotechnol Bioeng 68(1):106–114PubMedGoogle Scholar
  139. 139.
    Fink C, Ergun S, Kralisch D, Remmers U, Weil J, Eschenhagen T (2000) Chronic stretch of engineered heart tissue induces hypertrophy and functional improvement. FASEB J 14(5):669–679PubMedGoogle Scholar
  140. 140.
    Radisic M, Park H, Shing H, Consi T, Schoen FJ, Langer R, Freed LE, Vunjak-Novakovic G (2004) Functional assembly of engineered myocardium by electrical stimulation of cardiac myocytes cultured on scaffolds. Proc Natl Acad Sci USA 101(52):18129–18134PubMedGoogle Scholar
  141. 141.
    Zimmermann WH, Didie M, Wasmeier GH, Nixdorff U, Hess A, Melnychenko I, Boy O, Neuhuber WL, Weyand M, Eschenhagen T (2002) Cardiac grafting of engineered heart tissue in syngenic rats. Circulation 106(12 Suppl 1):I151–I157PubMedGoogle Scholar
  142. 142.
    Zimmermann WH, Melnychenko I, Wasmeier G, Didie M, Naito H, Nixdorff U, Hess A, Budinsky L, Brune K, Michaelis B, Dhein S, Schwoerer A, Ehmke H, Eschenhagen T (2006) Engineered heart tissue grafts improve systolic and diastolic function in infarcted rat hearts. Nat Med 12(4):452–458PubMedGoogle Scholar
  143. 143.
    Naito H, Melnychenko I, Didie M, Schneiderbanger K, Schubert P, Rosenkranz S, Eschenhagen T, Zimmermann WH (2006) Optimizing engineered heart tissue for therapeutic applications as surrogate heart muscle. Circulation 114(Suppl 1):I72–I78PubMedGoogle Scholar
  144. 144.
    Chachques JC, Trainini JC, Lago N, Cortes-Morichetti M, Schussler O, Carpentier A (2008) Myocardial assistance by grafting a new bioartificial upgraded myocardium (MAGNUM trial): clinical feasibility study. Ann Thorac Surg 85(3):901–908PubMedGoogle Scholar
  145. 145.
    Jawad H, Lyon AR, Harding SE, Ali NN, Boccaccini AR (2008) Myocardial tissue engineering. Br Med Bull 87:31–47PubMedGoogle Scholar
  146. 146.
    Ott HC, Matthiesen TS, Goh SK, Black LD, Kren SM, Netoff TI, Taylor DA (2008) Perfusion-decellularized matrix: using nature’s platform to engineer a bioartificial heart. Nat Med 14(2):213–221PubMedGoogle Scholar
  147. 147.
    Godier-Furnemont AF, Martens TP, Koeckert MS, Wan L, Parks J, Arai K, Zhang G, Hudson B, Homma S, Vunjak-Novakovic G (2011) Composite scaffold provides a cell delivery platform for cardiovascular repair. Proc Natl Acad Sci USA 108(19):7974–7979PubMedGoogle Scholar
  148. 148.
    Seif-Naraghi SB, Salvatore MA, Schup-Magoffin PJ, Hu DP, Christman KL (2010) Design and characterization of an injectable pericardial matrix gel: a potentially autologous scaffold for cardiac tissue engineering. Tissue Eng Part A 16(6):2017–2027PubMedGoogle Scholar
  149. 149.
    Akhyari P, Aubin H, Gwanmesia P, Barth M, Hoffmann S, Huelsmann J, Preuss K, Lichtenberg A (2011) The quest for an optimized protocol for whole-heart decellularization: a comparison of three popular and a novel decellularization technique and their diverse effects on crucial extracellular matrix qualities. Tissue Eng Part C Methods 17(9):915–926PubMedGoogle Scholar
  150. 150.
    Shin M, Ishii O, Sueda T, Vacanti JP (2004) Contractile cardiac grafts using a novel nanofibrous mesh. Biomaterials 25(17):3717–3723PubMedGoogle Scholar
  151. 151.
    Matsubayashi K, Fedak PW, Mickle DA, Weisel RD, Ozawa T, Li RK (2003) Improved left ventricular aneurysm repair with bioengineered vascular smooth muscle grafts. Circulation 108(Suppl 1):II219–II225PubMedGoogle Scholar
  152. 152.
    Bursac N, Papadaki M, Cohen RJ, Schoen FJ, Eisenberg SR, Carrier R, Vunjak-Novakovic G, Freed LE (1999) Cardiac muscle tissue engineering: toward an in vitro model for electrophysiological studies. Am J Physiol 277(2 Pt 2):H433–H444PubMedGoogle Scholar
  153. 153.
    Ke Q, Yang Y, Rana JS, Chen Y, Morgan JP, Xiao YF (2005) Embryonic stem cells cultured in biodegradable scaffold repair infarcted myocardium in mice. Sheng Li Xue Bao 57(6):673–681PubMedGoogle Scholar
  154. 154.
    Ozawa T, Mickle DA, Weisel RD, Koyama N, Ozawa S, Li RK (2002) Optimal biomaterial for creation of autologous cardiac grafts. Circulation 106(12 Suppl 1):I176–I182PubMedGoogle Scholar
  155. 155.
    McDevitt TC, Woodhouse KA, Hauschka SD, Murry CE, Stayton PS (2003) Spatially organized layers of cardiomyocytes on biodegradable polyurethane films for myocardial repair. J Biomed Mater Res A 66(3):586–595PubMedGoogle Scholar
  156. 156.
    Fujimoto KL, Tobita K, Merryman WD, Guan J, Momoi N, Stolz DB, Sacks MS, Keller BB, Wagner WR (2007) An elastic, biodegradable cardiac patch induces contractile smooth muscle and improves cardiac remodeling and function in subacute myocardial infarction. J Am Coll Cardiol 49(23):2292–2300PubMedGoogle Scholar
  157. 157.
    Chen QZ, Bismarck A, Hansen U, Junaid S, Tran MQ, Harding SE, Ali NN, Boccaccini AR (2008) Characterisation of a soft elastomer poly(glycerol sebacate) designed to match the mechanical properties of myocardial tissue. Biomaterials 29(1):47–57PubMedGoogle Scholar
  158. 158.
    Liang SL, Cook WD, Thouas GA, Chen QZ (2010) The mechanical characteristics and in vitro biocompatibility of poly(glycerol sebacate)-bioglass elastomeric composites. Biomaterials 31(33):8516–8529PubMedGoogle Scholar
  159. 159.
    Ishii O, Shin M, Sueda T, Vacanti JP (2005) In vitro tissue engineering of a cardiac graft using a degradable scaffold with an extracellular matrix-like topography. J Thorac Cardiovasc Surg 130(5):1358–1363PubMedGoogle Scholar
  160. 160.
    Kai D, Prabhakaran MP, Jin G, Ramakrishna S (2011) Guided orientation of cardiomyocytes on electrospun aligned nanofibers for cardiac tissue engineering. J Biomed Mater Res B Appl Biomater 98B(2):379–386PubMedGoogle Scholar
  161. 161.
    Iyer RK, Chiu LL, Radisic M (2009) Microfabricated poly(ethylene glycol) templates enable rapid screening of triculture conditions for cardiac tissue engineering. J Biomed Mater Res A 89(3):616–631PubMedGoogle Scholar
  162. 162.
    Kellar RS, Shepherd BR, Larson DF, Naughton GK, Williams SK (2005) Cardiac patch constructed from human fibroblasts attenuates reduction in cardiac function after acute infarct. Tissue Eng 11(11–12):1678–1687PubMedGoogle Scholar
  163. 163.
    Shimizu T (2002) Fabrication of pulsatile cardiac tissue grafts using a novel 3-dimensional cell sheet manipulation technique and temperature-responsive cell culture surfaces. Circ Res 90(3):e40–e48PubMedGoogle Scholar
  164. 164.
    Haraguchi Y, Shimizu T, Yamato M, Kikuchi A, Okano T (2006) Electrical coupling of cardiomyocyte sheets occurs rapidly via functional gap junction formation. Biomaterials 27(27):4765–4774PubMedGoogle Scholar
  165. 165.
    Shimizu T, Sekine H, Yang J, Isoi Y, Yamato M, Kikuchi A, Kobayashi E, Okano T (2006) Polysurgery of cell sheet grafts overcomes diffusion limits to produce thick, vascularized myocardial tissues. FASEB J 20(6):708–710PubMedGoogle Scholar
  166. 166.
    Sekine H, Shimizu T, Kosaka S, Kobayashi E, Okano T (2006) Cardiomyocyte bridging between hearts and bioengineered myocardial tissues with mesenchymal transition of mesothelial cells. J Heart Lung Transplant 25(3):324–332PubMedGoogle Scholar
  167. 167.
    Memon IA, Sawa Y, Fukushima N, Matsumiya G, Miyagawa S, Taketani S, Sakakida SK, Kondoh H, Aleshin AN, Shimizu T, Okano T, Matsuda H (2005) Repair of impaired myocardium by means of implantation of engineered autologous myoblast sheets. J Thorac Cardiovasc Surg 130(5):1333–1341PubMedGoogle Scholar
  168. 168.
    Miyagawa S, Saito A, Sakaguchi T, Yoshikawa Y, Yamauchi T, Imanishi Y, Kawaguchi N, Teramoto N, Matsuura N, Iida H, Shimizu T, Okano T, Sawa Y (2010) Impaired myocardium regeneration with skeletal cell sheets–a preclinical trial for tissue-engineered regeneration therapy. Transplantation 90(4):364–372PubMedGoogle Scholar
  169. 169.
    Miyahara Y, Nagaya N, Kataoka M, Yanagawa B, Tanaka K, Hao H, Ishino K, Ishida H, Shimizu T, Kangawa K, Sano S, Okano T, Kitamura S, Mori H (2006) Monolayered mesenchymal stem cells repair scarred myocardium after myocardial infarction. Nat Med 12(4):459–465PubMedGoogle Scholar
  170. 170.
    Kobayashi H, Shimizu T, Yamato M, Tono K, Masuda H, Asahara T, Kasanuki H, Okano T (2008) Fibroblast sheets co-cultured with endothelial progenitor cells improve cardiac function of infarcted hearts. J Artif Organs 11(3):141–147PubMedGoogle Scholar
  171. 171.
    Sekiya S, Shimizu T, Yamato M, Kikuchi A, Okano T (2006) Bioengineered cardiac cell sheet grafts have intrinsic angiogenic potential. Biochem Biophys Res Commun 341(2):573–582PubMedGoogle Scholar
  172. 172.
    Christman KL, Fok HH, Sievers RE, Fang Q, Lee RJ (2004) Fibrin glue alone and skeletal myoblasts in a fibrin scaffold preserve cardiac function after myocardial infarction. Tissue Eng 10(3–4):403–409PubMedGoogle Scholar
  173. 173.
    Chekanov V, Akhtar M, Tchekanov G, Dangas G, Shehzad MZ, Tio F, Adamian M, Colombo A, Roubin G, Leon MB, Moses JW, Kipshidze NN (2003) Transplantation of autologous endothelial cells induces angiogenesis. Pacing Clin Electrophysiol 26(1 Pt 2):496–499PubMedGoogle Scholar
  174. 174.
    Martens TP, Godier AF, Parks JJ, Wan LQ, Koeckert MS, Eng GM, Hudson BI, Sherman W, Vunjak-Novakovic G (2009) Percutaneous cell delivery into the heart using hydrogels polymerizing in situ. Cell Transplant 18(3):297–304PubMedGoogle Scholar
  175. 175.
    Kutschka I, Chen IY, Kofidis T, Arai T, von Degenfeld G, Sheikh AY, Hendry SL, Pearl J, Hoyt G, Sista R, Yang PC, Blau HM, Gambhir SS, Robbins RC (2006) Collagen matrices enhance survival of transplanted cardiomyoblasts and contribute to functional improvement of ischemic rat hearts. Circulation 114(Suppl 1):I167–I173PubMedGoogle Scholar
  176. 176.
    Tsur-Gang O, Ruvinov E, Landa N, Holbova R, Feinberg MS, Leor J, Cohen S (2009) The effects of peptide-based modification of alginate on left ventricular remodeling and function after myocardial infarction. Biomaterials 30(2):189–195PubMedGoogle Scholar
  177. 177.
    Leor J, Tuvia S, Guetta V, Manczur F, Castel D, Willenz U, Petnehazy O, Landa N, Feinberg MS, Konen E, Goitein O, Tsur-Gang O, Shaul M, Klapper L, Cohen S (2009) Intracoronary injection of in situ forming alginate hydrogel reverses left ventricular remodeling after myocardial infarction in Swine. J Am Coll Cardiol 54(11):1014–1023PubMedGoogle Scholar
  178. 178.
    Kofidis T, Lebl DR, Martinez EC, Hoyt G, Tanaka M, Robbins RC (2005) Novel injectable bioartificial tissue facilitates targeted, less invasive, large-scale tissue restoration on the beating heart after myocardial injury. Circulation 112(Suppl 9):I173–I177PubMedGoogle Scholar
  179. 179.
    Huang NF, Yu J, Sievers R, Li S, Lee RJ (2005) Injectable biopolymers enhance angiogenesis after myocardial infarction. Tissue Eng 11(11–12):1860–1866PubMedGoogle Scholar
  180. 180.
    Zhang P, Zhang H, Wang H, Wei Y, Hu S (2006) Artificial matrix helps neonatal cardiomyocytes restore injured myocardium in rats. Artif Organs 30(2):86–93PubMedGoogle Scholar
  181. 181.
    Kim IY, Seo SJ, Moon HS, Yoo MK, Park IY, Kim BC, Cho CS (2008) Chitosan and its derivatives for tissue engineering applications. Biotechnol Adv 26(1):1–21PubMedGoogle Scholar
  182. 182.
    Lu S, Wang H, Lu W, Liu S, Lin Q, Li D, Duan C, Hao T, Zhou J, Wang Y, Gao S, Wang C (2010) Both the transplantation of somatic cell nuclear transfer- and fertilization-derived mouse embryonic stem cells with temperature-responsive chitosan hydrogel improve myocardial performance in infarcted rat hearts. Tissue Eng Part A 16(4):1303–1315PubMedGoogle Scholar
  183. 183.
    Davis ME, Hsieh PC, Grodzinsky AJ, Lee RT (2005) Custom design of the cardiac microenvironment with biomaterials. Circ Res 97(1):8–15PubMedGoogle Scholar
  184. 184.
    Davis ME, Hsieh PC, Takahashi T, Song Q, Zhang S, Kamm RD, Grodzinsky AJ, Anversa P, Lee RT (2006) Local myocardial insulin-like growth factor 1 (IGF-1) delivery with biotinylated peptide nanofibers improves cell therapy for myocardial infarction. Proc Natl Acad Sci USA 103(21):8155–8160PubMedGoogle Scholar
  185. 185.
    Padin-Iruegas ME, Misao Y, Davis ME, Segers VF, Esposito G, Tokunou T, Urbanek K, Hosoda T, Rota M, Anversa P, Leri A, Lee RT, Kajstura J (2009) Cardiac progenitor cells and biotinylated insulin-like growth factor-1 nanofibers improve endogenous and exogenous myocardial regeneration after infarction. Circulation 120(10):876–887PubMedGoogle Scholar
  186. 186.
    Hamdi H, Furuta A, Bellamy V, Bel A, Puymirat E, Peyrard S, Agbulut O, Menasche P (2009) Cell delivery: intramyocardial injections or epicardial deposition? A head-to-head comparison. Ann Thorac Surg 87(4):1196–1203PubMedGoogle Scholar
  187. 187.
    Sekine H, Shimizu T, Hobo K, Sekiya S, Yang J, Yamato M, Kurosawa H, Kobayashi E, Okano T (2008) Endothelial cell coculture within tissue-engineered cardiomyocyte sheets enhances neovascularization and improves cardiac function of ischemic hearts. Circulation 118(Suppl 14):S145–S152PubMedGoogle Scholar

Copyright information

© Springer Basel AG 2012

Authors and Affiliations

  • Andre Alcon
    • 1
  • Esra Cagavi Bozkulak
    • 2
  • Yibing Qyang
    • 2
  1. 1.Yale University School of MedicineYale UniversityNew HavenUSA
  2. 2.Section of Cardiovascular Medicine, Department of Internal Medicine, Yale Cardiovascular Research Center, Yale Stem Cell Center, Yale School of MedicineYale UniversityNew HavenUSA

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