Human cord blood CD34+ progenitor cells acquire functional cardiac properties through a cell fusion process

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 300, Issue 5, 2011, Pages

  Avitabile, Daniele ^b   Crespi, Alessia ^a   Brioschi, Chiara ^a   Parente, Valeria ^b   Toietta, Gabriele ^c   Devanna, Paolo ^b   Baruscotti, Mirko ^a   Truffa, Silvia ^c   Scavone, Angela ^a   Rusconi, Francesca ^a   Biondi, Andrea ^d   D'Alessandra, Yuri ^b   Vigna, Elisa ^e   Difrancesco, Dario ^a   Pesce, Maurizio ^b   Capogrossi, Maurizio C ^c   Barbuti, Andrea ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b CENTRO CARDIOLOGICO MONZINO   (Italy)

^c LABORATORIO DI PATOLOGIA VASCOLARE   (Italy)

^d UNIVERSITY OF MILANO BICOCCA   (Italy)

^e CANDIOLO CANCER INSTITUTE   (Italy)

Author keywords

Cardiac repair; CD34; Cell fusion; Cord blood; Stem cells

Indexed keywords

ENHANCED GREEN FLUORESCENT PROTEIN; LENTIVIRUS VECTOR; RED FLUORESCENT PROTEIN;

ANIMAL CELL; ARTICLE; CD34 SELECTION; CELL CULTURE; CELL DIFFERENTIATION; CELL FUSION; CELL ISOLATION; CELL MEMBRANE DEPOLARIZATION; CELL MEMBRANE STEADY POTENTIAL; CELL SELECTION; CELL TRANSDIFFERENTIATION; CONTROLLED STUDY; DIASTOLE; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; HEART BEAT; HEART ELECTROPHYSIOLOGY; HEART FUNCTION; HEART MUSCLE CELL; HEART MUSCLE FIBER MEMBRANE STEADY POTENTIAL; HEART VENTRICLE; HUMAN; HUMAN CELL; LENTIVIRINAE; MAXIMUM DIASTOLIC POTENTIAL; NONHUMAN; PRIORITY JOURNAL; REPORTER GENE; STEM CELL; UMBILICAL CORD BLOOD;

ANIMALS; ANTIGENS, CD34; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL FUSION; CELLS, CULTURED; COCULTURE TECHNIQUES; CORD BLOOD STEM CELL TRANSPLANTATION; FETAL BLOOD; GREEN FLUORESCENT PROTEINS; HUMANS; MODELS, ANIMAL; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; RATS; STEM CELLS;

EID: 79955758992     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00523.2010     Document Type: Article

References (48)

1. Alvarez-Dolado M, Pardal R, Garcia-Verdugo JM, Fike JR, Lee HO, Pfeffer K, Lois C, Morrison SJ, Alvarez-Buylla A. Fusion of bonemarrow- derived cells with Purkinje neurons, cardiomyocytes and hepatocytes. Nature 425: 968-973, 2003.
2. Anversa P, Kajstura J, Leri A. If I can stop one heart from breaking. Circulation 115: 829-832, 2007.
3. Anversa P, Leri A, Rota M, Hosoda T, Bearzi C, Urbanek K, Kajstura J, Bolli R. Concise review: stem cells, myocardial regeneration, and methodological artifacts. Stem Cells 25: 589-601, 2007.
4. Araki H, Baluchamy S, Yoshinaga K, Petro B, Petiwala S, Parajuli R, Milhem M, Lavelle D, DeSimone J, Mahmud N. Cord blood stem cell expansion is permissive to epigenetic regulation and environmental cues. Exp Hematol 37: 1084-1095, 2009.
5. Badorff C, Brandes RP, Popp R, Rupp S, Urbich C, Aicher A, Fleming I, Busse R, Zeiher AM, Dimmeler S. Transdifferentiation of blood-derived human adult endothelial progenitor cells into functionally active cardiomyocytes. Circulation 107: 1024-1032, 2003.
6. Balsam LB, Wagers AJ, Christensen JL, Kofidis T, Weissman IL, Robbins RC. Haematopoietic stem cells adopt mature haematopoietic fates in ischaemic myocardium. Nature 428: 668-673, 2004.
7. Barbuti A, Baruscotti M, DiFrancesco D. The pacemaker current: from basics to the clinics. J Cardiovasc Electrophysiol 18: 342-347, 2007.
8. Barbuti A, Crespi A, Capilupo D, Mazzocchi N, Baruscotti M, Di- Francesco D. Molecular composition and functional properties of f-channels in murine embryonic stem cell-derived pacemaker cells. J Mol Cell Cardiol 46: 343-351, 2009.
9. Bearzi C, Rota M, Hosoda T, Tillmanns J, Nascimbene A, De AA, Yasuzawa-Amano S, Trofimova I, Siggins RW, Lecapitaine N, Cascapera S, Beltrami AP, D'Alessandro DA, Zias E, Quaini F, Urbanek K, Michler RE, Bolli R, Kajstura J, Leri A, Anversa P. Human cardiac stem cells. Proc Natl Acad Sci U S A 104: 14068-14073, 2007.
10. Behfar A, Perez-Terzic C, Faustino RS, Arrell DK, Hodgson DM, Yamada S, Puceat M, Niederlander N, Alekseev AE, Zingman LV, Terzic A. Cardiopoietic programming of embryonic stem cells for tumorfree heart repair. J Exp Med 204: 405-420, 2007.
11. Cerbai E, Pino R, Sartiani L, Mugelli A. Influence of postnataldevelopment on I(f) occurrence and properties in neonatal rat ventricular myocytes. Cardiovasc Res 42: 416-423, 1999.
12. Chang MG, Tung L, Sekar RB, Chang CY, Cysyk J, Dong P, Marban E, Abraham MR. Proarrhythmic potential of mesenchymal stem cell transplantation revealed in an in vitro coculture model. Circulation 113: 1832-1841, 2006.
13. Condorelli G, Borello U, De Angelis L, Latronico M, Sirabella D, Coletta M, Galli R, Balconi G, Follenzi A, Frati G, Cusella De Angelis MG, Gioglio L, Amuchastegui S, Adorini L, Naldini L, Vescovi A, Dejana E, Cossu G. Cardiomyocytes induce endothelial cells to transdifferentiate into cardiac muscle: implications for myocardium regeneration. Proc Natl Acad Sci U S A 98: 10733-10738, 2001.
14. DiFrancesco D. Pacemaker mechanisms in cardiac tissue. Annu Rev Physiol 55: 455-472, 1993.
15. DiFrancesco D, Ferroni A, Mazzanti M, Tromba C. Properties of the hyperpolarizing-activated current (if) in cells isolated from the rabbit sino-atrial node. J Physiol 377: 61-88, 1986.
16. Dudley SC Jr. Beware of cells bearing gifts: cell replacement therapy and arrhythmic risk. Circ Res 97: 99-101, 2005.
17. Fernandes S, Amirault JC, Lande G, Nguyen JM, Forest V, Bignolais O, Lamirault G, Heudes D, Orsonneau JL, Heymann MF, Charpentier F, Lemarchand P. Autologous myoblast transplantation after myocardial infarction increases the inducibility of ventricular arrhythmias. Cardiovasc Res 69: 348-358, 2006.
18. Garbade J, Schubert A, Rastan AJ, Lenz D, Walther T, Gummert JF, Dhein S, Mohr FW. Fusion of bone marrow-derived stem cells with cardiomyocytes in a heterologous in vitro model. Eur J Cardiothorac Surg 28: 685-691, 2005.
19. Gruh I, Beilner J, Blomer U, Schmiedl A, Schmidt-Richter I, Kruse ML, Haverich A, Martin U. No evidence of transdifferentiation of human endothelial progenitor cells into cardiomyocytes after coculture with neonatal rat cardiomyocytes. Circulation 113: 1326-1334, 2006.
20. Guan K, Wagner S, Unsold B, Maier LS, Kaiser D, Hemmerlein B, Nayernia K, Engel W, Hasenfuss G. Generation of functional cardiomyocytes from adult mouse spermatogonial stem cells. Circ Res 100: 1615-1625, 2007.
21. Habib M, Caspi O, Gepstein L. Human embryonic stem cells for cardiomyogenesis. J Mol Cell Cardiol 45: 462-474, 2008.
22. Hagege AA, Marolleau JP, Vilquin JT, Alheritiere A, Peyrard S, Duboc D, Abergel E, Messas E, Mousseaux E, Schwartz K, Desnos M, Menasche P. Skeletal myoblast transplantation in ischemic heart failure: long-term follow-up of the first phase I cohort of patients. Circulation 114: I108-I113, 2006.
23. Hescheler J, Fleischmann BK, Lentini S, Maltsev VA, Rohwedel J, Wobus AM, Addicks K. Embryonic stem cells: a model to study structural and functional properties in cardiomyogenesis. Cardiovasc Res 36: 149-162, 1997.
24. Ishikawa F, Shimazu H, Shultz LD, Fukata M, Nakamura R, Lyons B, Shimoda K, Shimoda S, Kanemaru T, Nakamura K, Ito H, Kaji Y, Perry AC, Harada M. Purified human hematopoietic stem cells contribute to the generation of cardiomyocytes through cell fusion. FASEB J 20: 950-952, 2006.
25. Joggerst SJ, Hatzopoulos AK. Stem cell therapy for cardiac repair: benefits and barriers. Expert Rev Mol Med 11: e20, 2009.
26. Kajstura J, Rota M, Whang B, Cascapera S, Hosoda T, Bearzi C, Nurzynska D, Kasahara H, Zias E, Bonafe M, Nadal-Ginard B, Torella D, Nascimbene A, Quaini F, Urbanek K, Leri A, Anversa P. Bone marrow cells differentiate in cardiac cell lineages after infarction independently of cell fusion. Circ Res 96: 127-137, 2005.
27. Koyanagi M, Haendeler J, Badorff C, Brandes RP, Hoffmann J, Pandur P, Zeiher AM, Kuhl M, Dimmeler S. Non-canonical Wnt signaling enhances differentiation of human circulating progenitor cells to cardiomyogenic cells. J Biol Chem 280: 16838-16842, 2005.
28. Labovsky V, Hofer EL, Feldman L, Fernandez VV, Garcia RH, Bayes-Genis A, Hernando IA, Levin MJ, Chasseing NA. Cardiomyogenic differentiation of human bone marrow mesenchymal cells: Role of cardiac extract from neonatal rat cardiomyocytes. Differentiation 79: 93-101, 2010.
29. Lagostena L, Avitabile D, De Falco E, Orlandi A, Grassi F, Iachininoto MG, Ragone G, Fucile S, Pompilio G, Eusebi F, Pesce M, Capogrossi MC. Electrophysiological properties of mouse bone marrow c-kit+ cells co-cultured onto neonatal cardiac myocytes. Cardiovasc Res 66: 482-492, 2005.
30. Makino S, Fukuda K, Miyoshi S, Konishi F, Kodama H, Pan J, Sano M, Takahashi T, Hori S, Abe H, Hata J, Umezawa A, Ogawa S. Cardiomyocytes can be generated from marrow stromal cells in vitro. J Clin Invest 103: 697-705, 1999.
31. Matsuura K, Wada H, Nagai T, Iijima Y, Minamino T, Sano M, Akazawa H, Molkentin JD, Kasanuki H, Komuro I. Cardiomyocytes fuse with surrounding noncardiomyocytes and reenter the cell cycle. J Cell Biol 167: 351-363, 2004.
32. Mummery C, Ward-van Oostwaard D, Doevendans P, Spijker R, van den BS, Hassink R, van der HM, Opthof T, Pera M, de la Riviere AB, Passier R, Tertoolen L. Differentiation of human embryonic stem cells to cardiomyocytes: role of coculture with visceral endoderm-like cells. Circulation 107: 2733-2740, 2003.
33. 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. Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature 428: 664-668, 2004.
34. Nygren JM, Jovinge S, Breitbach M, Sawen P, Roll W, Hescheler J, Taneera J, Fleischmann BK, Jacobsen SE. Bone marrow-derived hematopoietic cells generate cardiomyocytes at a low frequency through cell fusion, but not transdifferentiation. Nat Med 10: 494-501, 2004.
35. Oh H, Bradfute SB, Gallardo TD, Nakamura T, Gaussin V, Mishina Y, Pocius J, Michael LH, Behringer RR, Garry DJ, Entman ML, Schneider MD. Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proc Natl Acad Sci U S A 100: 12313-12318, 2003.
36. Orlandi A, Pagani F, Avitabile D, Bonanno G, Scambia G, Vigna E, Grassi F, Eusebi F, Fucile S, Pesce M, Capogrossi MC. Functional properties of cells obtained from human cord blood CD34 stem cells and mouse cardiac myocytes in coculture. Am J Physiol Heart Circ Physiol 294: H1541-H1549, 2008.
37. 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. Bone marrow cells regenerate infarcted myocardium. Nature 410: 701-705, 2001.
38. Pesce M, Orlandi A, Iachininoto MG, Straino S, Torella AR, Rizzuti V, Pompilio G, Bonanno G, Scambia G, Capogrossi MC. Myoendothelial differentiation of human umbilical cord blood-derived stem cells in ischemic limb tissues. Circ Res 93: e51-e62, 2003.
39. Pfister O, Mouquet F, Jain M, Summer R, Helmes M, Fine A, Colucci WS, Liao R. CD31- but Not CD31+ cardiac side population cells exhibit functional cardiomyogenic differentiation. Circ Res 97: 52-61, 2005.
40. Qu J, Barbuti A, Protas L, Santoro B, Cohen IS, Robinson RB. HCN2 overexpression in newborn and adult ventricular myocytes: distinct effects on gating and excitability. Circ Res 89: E8-E14, 2001.
41. Qu J, Cohen IS, Robinson RB. Sympathetic innervation alters activation of pacemaker current (If) in rat ventricle. J Physiol 526: 561-569, 2000.
42. Rota M, Kajstura J, Hosoda T, Bearzi C, Vitale S, Esposito G, Iaffaldano G, Padin-Iruegas ME, Gonzalez A, Rizzi R, Small N, Muraski J, Alvarez R, Chen X, Urbanek K, Bolli R, Houser SR, Leri A, Sussman MA, Anversa P. Bone marrow cells adopt the cardiomyogenic fate in vivo. Proc Natl Acad Sci U S A 104: 17783-17788, 2007.
43. Suzuki M, Harashima A, Okochi A, Yamamoto M, Nakamura S, Motoda R, Yamasaki F, Orita K. 5-Azacytidine supports the long-term repopulating activity of cord blood CD34(+) cells. Am J Hematol 77: 313-315, 2004.
44. Terada N, Hamazaki T, Oka M, Hoki M, Mastalerz DM, Nakano Y, Meyer EM, Morel L, Petersen BE, Scott EW. Bone marrow cells adopt the phenotype of other cells by spontaneous cell fusion. Nature 416: 542-545, 2002.
45. Yasui K, Liu W, Opthof T, Kada K, Lee JK, Kamiya K, Kodama I. I(f) current and spontaneous activity in mouse embryonic ventricular myocytes. Circ Res 88: 536-542, 2001.
46. Zhang J, Wilson GF, Soerens AG, Koonce CH, Yu J, Palecek SP, Thomson JA, Kamp TJ. Functional cardiomyocytes derived from human induced pluripotent stem cells. Circ Res 104: e30-e41, 2009.
47. Zhang S, Shpall E, Willerson JT, Yeh ET. Fusion of human hematopoietic progenitor cells and murine cardiomyocytes is mediated by alpha 4 beta 1 integrin/vascular cell adhesion molecule-1 interaction. Circ Res 100: 693-702, 2007.
48. Zhang S, Wang D, Estrov Z, Raj S, Willerson JT, Yeh ET. Both cell fusion and transdifferentiation account for the transformation of human peripheral blood CD34-positive cells into cardiomyocytes in vivo. Circulation 110: 3803-3807, 2004.