5-Azacytidine-treated human mesenchymal stem/progenitor cells derived from umbilical cord, cord blood and bone marrow do not generate cardiomyocytes in vitro at high frequencies

Vox Sanguinis

Volumn 95, Issue 2, 2008, Pages 137-148

  Martin Rendon, E ^a,b   Sweeney, D ^a   Lu, F ^a,b,c   Girdlestone, J ^d,e   Navarrete, C ^d,e   Watt, S M ^a,b  

^a JOHN RADCLIFFE HOSPITAL   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF HONG KONG   (Hong Kong)

^d NHS BLOOD AND TRANSPLANT   (United Kingdom)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

5 azacytidine; Bone marrow; Cord blood; Mesenchymal stem progenitor cells; Umbilical cord

Indexed keywords

AZACITIDINE; CD146 ANTIGEN; VASCULAR CELL ADHESION MOLECULE 1;

ADIPOCYTE; ARTICLE; BONE MARROW; CARTILAGE CELL; CELL DIFFERENTIATION; CELL ISOLATION; CONTROLLED STUDY; HEART MUSCLE CELL; HUMAN; HUMAN CELL; IMMUNOPHENOTYPING; IN VITRO STUDY; MESENCHYMAL STEM CELL; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL; UMBILICAL CORD BLOOD;

ADIPOCYTES; ADULT; ANTIGENS, DIFFERENTIATION; AZACITIDINE; BONE MARROW CELLS; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; CHONDROCYTES; FEASIBILITY STUDIES; FETAL BLOOD; GENE EXPRESSION PROFILING; HUMANS; IMMUNOPHENOTYPING; INFANT, NEWBORN; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STEM CELLS; MUSCLE PROTEINS; MYOCYTES, CARDIAC; ORGAN SPECIFICITY; OSTEOBLASTS; UMBILICAL CORD;

EID: 46749089254     PISSN: 00429007     EISSN: 14230410     Source Type: Journal    
DOI: 10.1111/j.1423-0410.2008.01076.x     Document Type: Article

References (60)

1. Gratwohl A, Baldomero H, Passweg J, Frassoni F, Niederwieser D, Schmitz N, Urbano-Ispizua A : Hematopoietic stem cell transplantation for hematological malignancies in Europe. Leukemia 2003 17 : 941 959
2. Metcalf D : Hematopoietic stem cells: old and new. Biomed Pharmacother 2001 55 : 75 78
3. McCulloch EA : Stem cells and diversity. Leukemia 2003 17 : 1042 1048
4. Friedenstein AJ, Gorskaja JF, Kulagina NN : Fibroblast precursors in normal and irradiated mouse hematopoietic organs. Exp Hematol 1976 4 : 267 274
5. Colter DC, Sekiya I, Prockop DJ : Identification of a subpopulation of rapidly self-renewing and multipotential adult stem cells in colonies of human marrow stromal cells. Proc Natl Acad Sci USA 2001 98 : 7841 7845
6. Le Blanc K, Rasmusson I, Sundberg B, Götherström C, Hassan M, Uzunel M, Ringdén O : Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet 2004 363 : 1439 1441
7. Ringden O, Uzunel M, Rasmusson I, Remberger M, Sundberg B, Lönnies H, Marschall HU, Dlugosz A, Szakos A, Hassan Z, Omazic B, Aschan J, Barkholt L, Le Blanc K : Mesenchymal stem cells for treatment of therapy-resistant graft-versus-host disease. Transplantation 2006 81 : 1390 1397
8. Gerdoni E, Gallo B, Casazza S, Musio S, Bonanni I, Pedemonte E, Mantegazza R, Frassoni F, Mancardi G, Pedotti R, Uccelli A : Mesenchymal stem cells effectively modulate pathogenic immune response in experimental autoimmune encephalomyelitis. Ann Neurol 2007 61 : 219 227
9. Augello A, Tasso R, Negrini SM, Cancedda R, Pennesi G : Cell therapy using allogeneic bone marrow mesenchymal stem cells prevents tissue damage in collagen-induced arthritis. Arthritis Rheum 2007 56 : 1175 1186
10. Laflamme MA, Murry CE : Regenerating the heart. Nat Biotechnol 2005 23 : 845 856
11. Krabbe C, Zimmer J, Meyer M : Neural transdifferentiation of mesenchymal stem cells - a critical review. APMIS 2005 113 : 831 844
12. Jiang Y, Jahagirdar BN, Reinhardt RE, Schwartz RL, Keene CD, Ortiz-Gonzalez XR, Reyes M, Lenvik T, Lund T, Blackstad M, Du JB, Aldrich S, Lisberg A, Low WC, Largaespada DA, Verfaillie CM : Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 2002 418 : 41 49
13. Li C, Zhang W, Jiang X, Mao N : Human-placenta-derived mesenchymal stem cells inhibit proliferation and function of allogeneic immune cells. Cell Tissue Res 2007 330 : 437 446
14. Liu XD, Liu B, Liu B, Mao N : Isolation and identification of mesenchymal stem cells from perfusion of human umbilical cord vein. Zhongguo Shi Yan Xue Ye Xue Za Zhi 2007 15 : 1019 1022
15. Lechner V, Höcht B, Ulrichs K, Thiede A, Meyer T : Obtaining of mesenchymal progenitor cells from the human umbilical cord. Zentralbl Chir 2007 132 : 358 364
16. Manca MF, Zwart I, Beo J, Palasingham R, Jen LS, Navarrete R, Girdlestone J, Navarrete CV : Characterization of mesenchymal stromal cells derived from full-term umbilical cord blood. Cytotherapy 2008 10 : 54 68
17. Erices A, Conget P, Minguell JJ : Mesenchymal progenitor cells in human umbilical cord blood. Br J Haematol 2000 109 : 235 242
18. Lee OK, Ko Y-C, Kuo TK, Chou S-H, Li H-J, Chen W-M, Chen T-H, Yeu SU : Fluvastatin and lovastatin but not pravastatin induce neuroglial differentiation in human mesenchymal stem cells. J Cell Biochem 2004 93 : 917 928
19. Parekkadan B, Sethu P, van Poll D, Yarmush ML, Toner M : Osmotic selection of human mesenchymal stem/progenitor cells from umbilical cord blood. Tissue Eng 2007 13 : 2465 2473
20. Sarugaser R, Lickorish D, Baksh D, Hosseini MM, Davies JE : Human umbilical cord perivascular (HUCPV) cells: a source of mesenchymal progenitors. Stem Cells 2005 23 : 220 229
21. Wang HS, Hung S-C, Peng S-T, Huang C-C, Wei H-M, Guo Y-J, Fu Y-S, Lai M-C, Chen C-C : Mesenchymal stem cells in the Wharton's jelly of the human umbilical cord. Stem Cells 2004 22 : 1330 1337
22. Mangi AA, Noiseux N, Kong D, He H, Rezvani M, Ingwall JS, Dzau VJ : Mesenchymal stem cells modified with Akt prevent remodeling and restore performance of infarcted hearts. Nat Med 2003 9 : 1195 1201
23. Chen SL, Fang WW, Ye F, Liu YH, Qian J, Shan SJ, Zhang JJ, Chunhua RZ, Liao LM, Lin S, Sun JP : Effect on left ventricular function of intracoronary transplantation of autologous bone marrow mesenchymal stem cell in patients with acute myocardial infarction. Am J Cardiol 2004 94 : 92 95
24. Toma C, Pittenger MF, Cahill KS, Cahill KS, Byrne BJ, Kessler PD : Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation 2002 105 : 93 98
25. Mohyeddin-Bonab M, Mohamad-Hassani M-R, Alimoghaddam K, Sanatkar M, Gasemi M, Mirkhani H, Radmehr H, Salehi M, Eslami M, Farhig-Parsa A, Emami-Razavi H, Ghasemi al-Mohamad M, Solimani A-A, Ghavamzadeh A, Nikbin B : Autologous in vitro expanded mesenchymal stem cell therapy for human old myocardial infarction. Arch Iran Med 2007 10 : 467 473
26. Stuckey DJ, Carr CA, Martin-Rendon E, Tyler DJ, Willmott C, Cassidy PJ, Hale SJM, Schneider JE, Tatton L, Harding SE, Radda GK, Watt S, Clarke K : Iron particles for noninvasive monitoring of bone marrow stromal cell engraftment into, and isolation of viable engrafted donor cells from, the heart. Stem Cells 2006 24 : 1968 75
27. Dai W, Hale SL, Kloner RA : Stem cell transplantation for the treatment of myocardial infarction. Transpl Immunol 2005 15 : 91 97
28. Silva GV, Litovsky S, Assad JA, Sousa AL, Martin BJ, Vela D, Coulter SC, Lin J, Ober J, Vaughn WK, Branco RV, Oliveira EM, He R, Geng YJ, Willerson JT, Perin EC : Mesenchymal stem cells differentiate into an endothelial phenotype, enhance vascular density, and improve heart function in a canine chronic ischemia model. Circulation 2005 111 : 150 156
29. Hung SC, Pochampally RR, Chen S-C, Hsu S-C, Prockop DJ : Angiogenic effects of human multipotent stromal cell conditioned medium activate the PI3K-Akt pathway in hypoxic endothelial cells to inhibit apoptosis, increase survival, and stimulate angiogenesis. Stem Cells 2007 25 : 2363 2370
30. Kinnaird T, Stabile E, Burnett MS, Lee CW, Barr S, Fuchs S, Epstein SE : Marrow-derived stromal cells express genes encoding a broad spectrum of arteriogenic cytokines and promote in vitro and in vivo arteriogenesis through paracrine mechanisms. Circ Res 2004 94 : 678 685
31. Potier E, Ferreira E, Andriamanalijaona R, Pujol JP, Oudina K, Logeart-Avramoglou D, Petite H : Hypoxia affects mesenchymal stromal cell osteogenic differentiation and angiogenic factor expression. Bone 2007 40 : 1078 1087
32. Ceradini DJ, Kulkarni AR, Callaghan MJ, Tepper OM, Bastidas N, Kleinman ME, Capla JM, Galiano RD, Levine JP, Gurtner GC : Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med 2004 10 : 858 864
33. Martin-Rendon E, Hale SJ, Ryan D, Baban D, Forde SP, Roubelakis M, Sweeney D, Moukayed M, Harris AL, Davies K, Watt SM : Transcriptional profiling of human cord blood CD133+ and cultured bone marrow mesenchymal stem cells in response to hypoxia. Stem Cells 2007 25 : 1003 1012
34. Watt SM, Butler LH, Tavian M, Bühring HJ, Rappold I, Simmons PJ, Zannettino AC, Buck D, Fuchs A, Doyonnas R, Chan JY, Levesque JP, Peault B, Roxanis I : Functionally defined CD164 epitopes are expressed on CD34(+) cells throughout ontogeny but display distinct distribution patterns in adult hematopoietic and nonhematopoietic tissues. Blood 2000 95 : 3113 3124
35. Jackson KA, Majka SM, Wang H, Pocius J, Hartley CJ, Majesky MW, Entman ML, Michael LH, Hirschi KK, Goodell MA : Regeneration of ischemic cardiac muscle and vascular endothelium by adult stem cells. J Clin Invest 2001 107 : 1395 1402
36. Laflamme MA, Myerson D, Saffitz JE, Murry CE : Evidence for cardiomyocyte repopulation by extracardiac progenitors in transplanted human hearts. Circ Res 2002 90 : 634 640
37. 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 1999 103 : 697 705
38. Tomita S, Li RK, Weisel RD, Mickle DA, Kim EJ, Sakai T, Jia ZQ : Autologous transplantation of bone marrow cells improves damaged heart function. Circulation 1999 100 (suppl. 19) : II247 256
39. Zannettino AC, Paton S, Arthur A, Khor F, Itescu S, Gimble JM, Gronthos S : Multipotential human adipose-derived stromal stem cells exhibit a perivascular phenotype in vitro and in vivo. J Cell Physiol 2008 214 : 413 421
40. Sacchetti B, Funari A, Michienzi S, Di Cesare S, Piersanti S, Saggio I, Tagliafico E, Ferrari S, Robey PG, Riminucci M, Bianco P : Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell 2007 131 : 324 336
41. Gronthos S, Zannettino ACW, Hay SJ, Shi S, Graves SE, Kortesidis A, Simmons PJ : Molecular and cellular characterisation of highly purified stromal stem cells derived from human bone marrow. J Cell Sci 2003 116 : 1827 1835
42. Rider DA, Dombrowski C, Sawyer AA, Ng GH, Leong D, Hutmacher DW, Nurcombe V, Cool SM : Autocrine FGF2 Increases the Multipotentiality of Human Adipose-Derived Mesenchymal Stem Cells. Stem Cells 2008 Epub ahead of print
43. Wagner W, Wein F, Seckinger A, Frankhauser M, Wirkner U, Krause U, Blake J, Schwager C, Eckstein V, Ansorge W, Ho AD : Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbilical cord blood. Exp Hematol 2005 33 : 1402 1416
44. Levesque JP, Takamatsu Y, Nilsson SK, Haylock DN, Simmons PJ : Vascular cell adhesion molecule-1 (CD106) is cleaved by neutrophil proteases in the bone marrow following hematopoietic progenitor cell mobilization by granulocyte colony-stimulating factor. Blood 2001 98 : 1289 1297
45. Zwart I, Hill AJ, Girdlestone J, Manca MF, Navarrete R, Navarrete C, Jen LS : Analysis of neural potential of human umbilical cord blood-derived multipotent mesenchymal stem cells in response to a range of neurogenic stimuli. J Neurosc Res 2008 Epub ahead of print
46. Joannides A, Gaughwin P, Scott M, Watt S, Compston A, Chandran S : Postnatal astrocytes promote neural induction from adult human bone marrow-derived stem cells. J Hematother Stem Cell Res 2003 12 : 681 688
47. Kadivar M, Khatami S, Mortazavi Y, Shokrgozar MA, Taghikhani M, Soleimani M : In vitro cardiomyogenic potential of human umbilical vein-derived mesenchymal stem cells. Biochem Biophys Res Commun 2006 340 : 639 647
48. Nishiyama N, Miyoshi S, Hida N, Uyama T, Okamoto K, Ikegami Y, Miyado K, Segawa K, Terai M, Sakamoto M, Ogawa S, Umezawa A : The significant cardiomyogenic potential of human umbilical cord blood-derived mesenchymal stem cells in vitro. Stem Cells 2007 25 : 2017 2024
49. Ye NS, Chen J, Luo GA, Zhang RL, Wang YM : Proteomic profiling of rat bone marrow mesenchymal stem cells induced by 5-azacytidine. Stem Cells Dev 2006 15 : 665 676
50. Balana B, Nicoletti C, Zahanich I, Graf EM, Christ T, Boxberger S, Ravens U : 5-Azacytidine induces changes in electrophysiological properties of human mesenchymal stem cells. Cell Res 2006 16 : 949 960
51. Gnecchi M, He H, Liang OD, Melo LG, Morello F, Mu H, Noiseux N, Zhang L, Pratt RE, Ingwall JS, Dzau VJ : Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells. Nat Med 2005 11 : 367 368
52. Gnecchi M, He H, Noiseux N, Liang OD, Zhang L, Morello F, Mu H, Melo LG, Pratt RE, Ingwall JS, Dzau VJ : Evidence supporting paracrine hypothesis for Akt-modified mesenchymal stem cell-mediated cardiac protection and functional improvement. FASEB J 2006 20 : 661 669
53. Mirotsou M, Zhang Z, Deb A, Zhang L, Gnecchi M, Noiseux N, Mu H, Pachori A, Dzau V : Secreted frizzled related protein 2 (Sfrp2) is the key Akt-mesenchymal stem cell-released paracrine factor mediating myocardial survival and repair. Proc Natl Acad Sci USA 2007 104 : 1643 1648
54. Noiseux N, Gnecchi M, Lopez-Ilasaca M, Zhang L, Solomon SD, Deb A, Dzau VJ, Pratt RE : Mesenchymal stem cells overexpressing Akt dramatically repair infarcted myocardium and improve cardiac function despite infrequent cellular fusion or differentiation. Mol Ther 2006 14 : 840 850
55. 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 2003 107 : 1024 1032
56. 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 2005 66 : 482 492
57. Yeh ET, Zhang S, Wu HD, Körbling M, Willerson JT, Estrov Z : Transdifferentiation of human peripheral blood CD34+-enriched cell population into cardiomyocytes, endothelial cells, and smooth muscle cells in vivo. Circulation 2003 108 : 2070 2073
58. 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 2001 410 : 701 705
59. 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 2004 428 : 664 668
60. Balsam LB, Wagers AJ, CHristensen JL, Kofidis T, Weissman IL, Robbins RC : Haematopoietic stem cells adopt mature haematopoietic fates in ischaemic myocardium. Nature 2004 428 : 668 673