Cardiomyogenic differentiation-independent improvement of cardiac function by human cardiomyocyte progenitor cell injection in ischaemic mouse hearts

Journal of Cellular and Molecular Medicine

Volumn 16, Issue 7, 2012, Pages 1508-1521

  Den Haan, Melina C ^a   Grauss, Robert W ^a   Smits, Anke M ^a   Winter, Elizabeth M ^a   Van Tuyn, John ^a   Pijnappels, Daniël A ^a   Steendijk, Paul ^a   Gittenberger De Groot, Adriana C ^a   van der Laarse, Arnoud ^a   Fibbe, Willem E ^a   De Vries, Antoine A F ^a   Schalij, Martin J ^a   Doevendans, Pieter A ^b   Goumans, Marie José ^a   Atsma, Douwe E ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Angiogenesis; Cardiomyocyte progenitor cell; Myocardial infarction; Paracrine factors; Remodelling

Indexed keywords

ENHANCED GREEN FLUORESCENT PROTEIN; GREEN FLUORESCENT PROTEIN;

ANIMAL; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CYTOLOGY; HEART INFARCTION; HEART LEFT VENTRICLE FUNCTION; HEART MUSCLE CELL; HEART VENTRICLE REMODELING; HUMAN; ISCHEMIA; MALE; METABOLISM; MOUSE; MOUSE MUTANT; MYOBLAST; NONOBESE DIABETIC MOUSE; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; TRANSPLANTATION;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; GREEN FLUORESCENT PROTEINS; HUMANS; ISCHEMIA; MAGNETIC RESONANCE IMAGING; MALE; MICE; MICE, INBRED NOD; MICE, SCID; MYOBLASTS; MYOCARDIAL INFARCTION; MYOCYTES, CARDIAC; VENTRICULAR FUNCTION, LEFT; VENTRICULAR REMODELING;

ANIMALIA; MURINAE; MUS;

EID: 84863113271     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2011.01468.x     Document Type: Article

References (60)

1. Orlic D, Kajstura J, Chimenti S, et al. Bone marrow cells regenerate infarcted myocardium. Nature. 2001; 410: 701-5.
2. Pittenger MF, Martin BJ. Mesenchymal stem cells and their potential as cardiac therapeutics. Circ Res. 2004; 95: 9-20.
3. Hodgson DM, Behfar A, Zingman LV, et al. Stable benefit of embryonic stem cell therapy in myocardial infarction. Am J Physiol Heart Circ Physiol. 2004; 287: H471-9.
4. Murtuza B, Suzuki K, Bou-Gharios G, et al. Transplantation of skeletal myoblasts secreting an IL-1 inhibitor modulates adverse remodeling in infarcted murine myocardium. Proc Natl Acad Sci U S A. 2004; 101: 4216-21.
5. Badorff C, Brandes RP, Popp R, et al. Transdifferentiation of blood-derived human adult endothelial progenitor cells into functionally active cardiomyocytes. Circulation. 2003; 107: 1024-32.
6. Rosenzweig A. Cardiac cell therapy-mixed results from mixed cells. N Engl J Med. 2006; 355: 1274-7.
7. Reffelmann T, Konemann S, Kloner RA. Promise of blood- and bone marrow-derived stem cell transplantation for functional cardiac repair: putting it in perspective with existing therapy. J Am Coll Cardiol. 2009; 53: 305-8.
8. Nagaya N, Kangawa K, Itoh T, et al. Transplantation of mesenchymal stem cells improves cardiac function in a rat model of dilated cardiomyopathy. Circulation. 2005; 112: 1128-35.
9. Tang YL, Zhao Q, Qin X, et al. Paracrine action enhances the effects of autologous mesenchymal stem cell transplantation on vascular regeneration in rat model of myocardial infarction. Ann Thorac Surg. 2005; 80: 229-36.
10. Kinnaird T, Stabile E, Burnett MS, et al. Local delivery of marrow-derived stromal cells augments collateral perfusion through paracrine mechanisms. Circulation. 2004; 109: 1543-9.
11. Berry MF, Engler AJ, Woo YJ, et al. Mesenchymal stem cell injection after myocardial infarction improves myocardial compliance. Am J Physiol Heart Circ Physiol. 2006; 290: H2196-203.
12. Murry CE, Soonpaa MH, Reinecke H, et al. Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature. 2004; 428: 664-8.
13. Nakamura Y, Wang X, Xu C, et al. Xenotransplantation of long-term-cultured swine bone marrow-derived mesenchymal stem cells. Stem Cells. 2007; 25: 612-20.
14. Smits AM, Ramkisoensing AA, Atsma DE, et al. Young at heart. An update on cardiac regeneration. Minerva Med. 2010; 101: 255-70.
15. Goumans MJ, de Boer TP, Smits AM, et al. TGF-beta1 induces efficient differentiation of human cardiomyocyte progenitor cells into functional cardiomyocytes in vitro. Stem Cell Res. 2007; 1: 138-49.
16. Smits AM, van Laake LW, den Ouden K, et al. Human cardiomyocyte progenitor cell transplantation preserves long-term function of the infarcted mouse myocardium. Cardiovasc Res. 2009; 83: 527-35.
17. van Tuyn J, Knaan-Shanzer S, van de Watering MJ, et al. Activation of cardiac and smooth muscle-specific genes in primary human cells after forced expression of human myocardin. Cardiovasc Res. 2005; 67: 245-55.
18. Grauss RW, van Tuyn J, Steendijk P, et al. Forced myocardin expression enhances the therapeutic effect of human mesenchymal stem cells after transplantation in ischemic mouse hearts. Stem Cells. 2008; 26: 1083-93.
19. Grauss RW, Winter EM, van Tiun J, et al. Mesenchymal stem cells from ischemic heart disease patients improve left ventricular function after acute myocardial infarction. Am J Physiol Heart Circ Physiol. 2007; 293: H2438-47.
20. Winter EM, Grauss RW, Atsma DE, et al. Left ventricular function in the post-infarct failing mouse heart by magnetic resonance imaging and conductance catheter: a comparative analysis. Acta Physiol. 2008; 194: 111-22.
21. Steendijk P, Baan J. Comparison of intravenous and pulmonary artery injections of hypertonic saline for the assessment of conductance catheter parallel conductance. Cardiovasc Res. 2000; 46: 82-9.
22. Lips DJ, van der Nagel T, Steendijk P, et al. Left ventricular pressure-volume measurements in mice: comparison of closed-chest versus open-chest approach. Basic Res Cardiol. 2004; 99: 351-9.
23. Wei S, Chow LT, Shum IO, et al. Left and right ventricular collagen type I/III ratios and remodeling post-myocardial infarction. J Card Fail. 1999; 5: 117-26.
24. Beltrami AP, Urbanek K, Kajstura J, et al. Evidence that human cardiac myocytes divide after myocardial infarction. N Engl J Med. 2001; 344: 1750-7.
25. Bergmann O, Bhardwaj RD, Bernard S, et al. Evidence for cardiomyocyte renewal in humans. Science. 2009; 324: 98-102.
26. Kajstura J, Urbanek K, Perl S, et al. Cardiomyogenesis in the adult human heart. Circ Res. 2010; 107: 305-15.
27. Parmacek MS, Epstein JA. Cardiomyocyte renewal. N Engl J Med. 2009; 361: 86-8.
28. Hsieh PC, Segers VF, Davis ME, et al. Evidence from a genetic fate-mapping study that stem cells refresh adult mammalian cardiomyocytes after injury. Nat Med. 2007; 13: 970-4.
29. Poss KD, Wilson LG, Keating MT. Heart regeneration in zebrafish. Science. 2002; 298: 2188-90.
30. Kikuchi K, Holdway JE, Werdich AA, et al. Primary contribution to zebrafish heart regeneration by gata4(+) cardiomyocytes. Nature. 2010; 464: 601-5.
31. Jopling C, Sleep E, Raya M, et al. Zebrafish heart regeneration occurs by cardiomyocyte dedifferentiation and proliferation. Nature. 2010; 464: 606-9.
32. Zuo S, Jones WK, Li H, et al. Paracrine effect of Wnt11-overexpressing me enchymal stem cells on ischemic injury. Stem Cells Dev. 2011; in press: doi:10.1089/scd.2011.0071.
33. Wang M, Crisostomo PR, Herring C, et al. Human progenitor cells from bone marrow or adipose tissue produce VEGF, HGF, and IGF-I in response to TNF by a p38 MAPK-dependent mechanism. Am J Physiol Regul Integr Comp Physiol. 2006; 291: R880-4.
34. Linke A, Muller P, Nurzynska D, et al. Stem cells in the dog heart are self-renewing, clonogenic, and multipotent and regenerate infarcted myocardium, improving cardiac function. Proc Natl Acad Sci U S A. 2005; 102: 8966-71.
35. Beltrami AP, Barlucchi L, Torella D, et al. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell. 2003; 114: 763-76.
36. Pfister O, Mouquet F, Jain M, et al. CD31- but not CD31+ cardiac side population cells exhibit functional cardiomyogenic differentiation. Circ Res. 2005; 97: 52-61.
37. Messina E, De Angelis L, Frati G, et al. Isolation and expansion of adult cardiac stem cells from human and murine heart. Circ Res. 2004; 95: 911-21.
38. Laugwitz KL, Moretti A, Lam J, et al. Postnatal isl1+ cardioblasts enter fully differentiated cardiomyocyte lineages. Nature. 2005; 433: 647-53.
39. Oh H, Bradfute SB, Gallardo TD, et al. Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proc Natl Acad Sci U S A. 2003; 100: 12313-8.
40. Smith RR, Barile L, Cho HC, et al. Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation. 2007; 115: 896-908.
41. Chimenti I, Smith RR, Li TS, et al. Relative roles of direct regeneration versus paracrine effects of human cardiosphere-derived cells transplanted into infarcted mice. Circ Res. 2010; 106: 971-80.
42. Smits AM, van Vliet P, Metz CH, et al. Human cardiomyocyte progenitor cells differentiate into functional mature cardiomyocytes: an in vitro model for studying human cardiac physiology and pathophysiology. Nat Protoc. 2009; 4: 232-43.
43. Winter EM, van Oorschot AA, Hogers B, et al. A new direction for cardiac regeneration therapy: application of synergistically acting epicardium-derived cells and cardiomyocyte progenitor cells. Circ Heart Fail. 2009; 2: 643-53.
44. van Oorschot AA, Smits AM, Pardali E, et al. Low oxygen tension positively influences cardiomyocyte progenitor cell function. J Cell Mol Med. 2011; in press: doi:10.1111/j.1582-4934.2011.01270.x.
45. Essers J, Theil AF, Baldeyron C, et al. Nuclear dynamics of PCNA in DNA replication and repair. Mol Cell Biol. 2005; 25: 9350-9.
46. Frangogiannis NG, Perrard JL, Mendoza LH, et al. Stem cell factor induction is associated with mast cell accumulation after canine myocardial ischemia and reperfusion. Circulation. 1998; 98: 687-98.
47. Frangogiannis NG, Michael LH, Entman ML. Myofibroblasts in reperfused myocardial infarcts express the embryonic form of smooth muscle myosin heavy chain (SMemb). Cardiovasc Res. 2000; 48: 89-100.
48. Hatzistergos KE, Quevedo H, Oskouei BN, et al. Bone marrow mesenchymal stem cells stimulate cardiac stem cell proliferation and differentiation. Circ Res. 2010; 107: 913-22.
49. Tang XL, Rokosh G, Sanganalmath SK, et al. Intracoronary administration of cardiac progenitor cells alleviates left ventricular dysfunction in rats with a 30-day-old infarction. Circulation. 2010; 121: 293-305.
50. Dow J, Simkhovich BZ, Kedes L, et al. Washout of transplanted cells from the heart: a potential new hurdle for cell transplantation therapy. Cardiovasc Res. 2005; 67: 301-7.
51. Teng CJ, Luo J, Chiu RC, et al. Massive mechanical loss of microspheres with direct intramyocardial injection in the beating heart: implications for cellular cardiomyoplasty. J Thorac Cardiovasc Surg. 2006; 132: 628-32.
52. Hudson W, Collins MC, deFreitas D, et al. Beating and arrested intramyocardial injections are associated with significant mechanical loss: implications for cardiac cell transplantation. J Surg Res. 2007; 142: 263-7.
53. Hou D, Youssef EA, Brinton TJ, et al. Radiolabeled cell distribution after intramyocardial, intracoronary, and interstitial retrograde coronary venous delivery: implications for current clinical trials. Circulation. 2005; 112: I150-6.
54. Hayashi M, Li TS, Ito H, et al. Comparison of intramyocardial and intravenous routes of delivering bone marrow cells for the treatment of ischemic heart disease: an experimental study. Cell Transplant. 2004; 13: 639-47.
55. Henning RJ, Burgos JD, Vasko M, et al. Human cord blood cells and myocardial infarction: effect of dose and route of administration on infarct size. Cell Transplant. 2007; 16: 907-17.
56. Orlic D, Kajstura J, Chimenti S, et al. Mobilized bone marrow cells repair the infarcted heart, improving function and survival. Proc Natl Acad Sci U S A. 2001; 98: 10344-9.
57. Huber BC, Brunner S, Segeth A, et al. Parathyroid hormone is a DPP-IV inhibitor and increases SDF-1-driven homing of CXCR4(+) stem cells into the ischaemic heart. Cardiovasc Res. 2011; 90: 529-37.
58. Theiss HD, Vallaster M, Rischpler C, et al. Dual stem cell therapy after myocardial infarction acts specifically by enhanced homing via the SDF-1/CXCR4 axis. Stem Cell Res. 2011; 7: 244-55.
59. Martin-Rendon E, Brunskill SJ, Hyde CJ, et al. Autologous bone marrow stem cells to treat acute myocardial infarction: a systematic review. Eur Heart J. 2008; 29: 1807-18.
60. Wen Y, Meng L, Xie J, et al. Direct autologous bone marrow-derived stem cell transplantation for ischemic heart disease: a meta-analysis. Expert Opin Biol Ther. 2011; 11: 559-67.