Sox2 Transduction enhances cardiovascular repair capacity of blood-derived mesoangioblasts

Circulation Research

Volumn 106, Issue 7, 2010, Pages 1290-1302

  Koyanagi, Masamichi ^a   Iwasaki, Masayoshi ^a   Rupp, Stefan ^a,d   Tedesco, Francesco Saverio ^f   Yoon, Chang Hwan ^a   Boeckel, Jes Niels ^a   Trauth, Janina ^a,d   Schütz, Corina ^a   Ohtani, Kisho ^a   Goetz, Rebekka ^a,d   Iekushi, Kazuma ^a   Bushoven, Philipp ^a,b   Momma, Stefan ^c   Mummery, Christine ^e   Passier, Robert ^e   Henschler, Reinhard ^a   Akintuerk, Hakan ^d   Schranz, Dietmar ^d   Urbich, Carmen ^a   Galvez, Beatriz G ^f   Cossu, Giulio ^f   Zeiher, Andreas M ^b   Dimmeler, Stefanie ^a   more..

^a GOETHE UNIVERSITY   (Germany)

^b Department of Cardiology   (United States)

^c Institute of Neurology (Edinger Institute)   (United States)

^d Pediatric Heart Center   (Germany)

^e LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^f SAN RAFFAELE HOSPITAL   (Italy)

Author keywords

Circulating progenitors; Differentiation; Reprogramming; Sox2

Indexed keywords

KRUPPEL LIKE FACTOR 4; LENTIVIRUS VECTOR; MYC PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; SMOOTH MUSCLE ACTIN; TELOMERASE; TRANSCRIPTION FACTOR SOX2;

ACUTE HEART INFARCTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIOVASCULAR SYSTEM; CELL CLONE; CELL DIFFERENTIATION; CELL EXPANSION; CELL ISOLATION; CELL PROLIFERATION; CELL THERAPY; CHILD; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; ENDOTHELIUM CELL; HEART MUSCLE CELL; HEMATOPOIETIC CELL; HUMAN; HUMAN CELL; MESENCHYME CELL; MESOANGIOBLAST; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STROMA CELL; TISSUE REPAIR;

AGED; AGED, 80 AND OVER; ANIMALS; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; CELLS, CULTURED; CHILD; CHILD, PRESCHOOL; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC VECTORS; HINDLIMB; HUMANS; INFANT; INFANT, NEWBORN; ISCHEMIA; KRUPPEL-LIKE TRANSCRIPTION FACTORS; LENTIVIRUS; LEUKOCYTES, MONONUCLEAR; MALE; MICE; MICE, NUDE; MIDDLE AGED; MUSCLE, SKELETAL; MYOCARDIAL INFARCTION; MYOCYTES, CARDIAC; MYOCYTES, SMOOTH MUSCLE; NEOVASCULARIZATION, PHYSIOLOGIC; OCTAMER TRANSCRIPTION FACTOR-3; PERIPHERAL BLOOD STEM CELL TRANSPLANTATION; PHENOTYPE; PLURIPOTENT STEM CELLS; PROTO-ONCOGENE PROTEINS C-MYC; REGENERATION; SOXB1 TRANSCRIPTION FACTORS; TIME FACTORS; TRANSDUCTION, GENETIC; YOUNG ADULT;

EID: 77951278598     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.109.206045     Document Type: Article

References (49)

1. Schachinger V, Erbs S, Elsasser A, Haberbosch W, Hambrecht R, Hol-schermann H, Yu J, Corti R, Mathey DG, Hamm CW, Suselbeck T, Assmus B, Tonn T, Dimmeler S, Zeiher AM. Intracoronary bone marrow-derived progenitor cells in acute myocardial infarction. N Engl J Med. 2006;355:1210-1221. (Pubitemid 44427445)
2. Wollert KC, Meyer GP, Lotz J, Ringes-Lichtenberg S, Lippolt P, Bre-idenbach C, Fichtner S, Korte T, Hornig B, Messinger D, Arseniev L, Hertenstein B, Ganser A, Drexler H. Intracoronary autologous bone-marrow cell transfer after myocardial infarction: the BOOST randomised controlled clinical trial. Lancet. 2004;364:141-148. (Pubitemid 38891685)
3. Losordo DW, Schatz RA, White CJ, Udelson JE, Veereshwarayya V, Durgin M, Poh KK, Weinstein R, Kearney M, Chaudhry M, Burg A, Eaton L, Heyd L, Thorne T, Shturman L, Hoffmeister P, Story K, Zak V, Dowling D, Traverse JH, Olson RE, Flanagan J, Sodano D, Murayama T, Kawamoto A, Kusano KF, Wollins J, Welt F, Shah P, Soukas P, Asahara T, Henry TD. Intramyocardial transplantation of autologous CD34+ stem cells for intractable angina: a phase I/IIa double-blind, randomized controlled trial. Circulation. 2007;115:3165-3172. (Pubitemid 47018140)
4. Assmus B, Honold J, Schachinger V, Britten MB, Fischer-Rasokat U, Lehmann R, Teupe C, Pistorius K, Martin H, Abolmaali ND, Tonn T, Dimmeler S, Zeiher AM. Transcoronary transplantation of progenitor cells after myocardial infarction. N Engl J Med. 2006;355:1222-1232. (Pubitemid 44427446)
5. Perin EC, Dohmann HF, Borojevic R, Silva SA, Sousa AL, Mesquita CT, Rossi MI, Carvalho AC, Dutra HS, Dohmann HJ, Silva GV, Belem L, Vivacqua R, Rangel FO, Esporcatte R, Geng YJ, Vaughn WK, Assad JA, Mesquita ET, Willerson JT. Transendocardial, autologous bone marrow cell transplantation for severe, chronic ischemic heart failure. Circulation. 2003;107:2294-2302. (Pubitemid 36578498)
6. Lipinski MJ, Biondi-Zoccai GG, Abbate A, Khianey R, Sheiban I, Bartunek J, Vanderheyden M, Kim HS, Kang HJ, Strauer BE, Vetrovec GW. Impact of intracoronary cell therapy on left ventricular function in the setting of acute myocardial infarction: a collaborative systematic review and meta-analysis of controlled clinical trials. J Am Coll Cardiol. 2007;50:1761-1767. (Pubitemid 47600592)
7. Iso Y, Spees JL, Serrano C, Bakondi B, Pochampally R, Song YH, Sobel BE, Delafontaine P, Prockop DJ. Multipotent human stromal cells improve cardiac function after myocardial infarction in mice without long-term engraftment. Biochem Biophys Res Commun. 2007;354: 700-706. (Pubitemid 46186241)
8. 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. 2004;10:494-501. (Pubitemid 38667908)
9. Vasa M, Fichtlscherer S, Aicher A, Adler K, Urbich C, Martin H, Zeiher AM, Dimmeler S. Number and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease. Circ Res. 2001;89:e1-e7. (Pubitemid 32578123)
10. Heeschen C, Lehmann R, Honold J, Assmus B, Aicher A, Walter DH, Martin H, Zeiher AM, Dimmeler S. Profoundly reduced neovascularization capacity of bone marrow mononuclear cells derived from patients with chronic ischemic heart disease. Circulation. 2004;109:1615-1622. (Pubitemid 38451717)
11. Kissel CK, Lehmann R, Assmus B, Aicher A, Honold J, Fischer-Rasokat U, Heeschen C, Spyridopoulos I, Dimmeler S, Zeiher AM. Selective functional exhaustion of hematopoietic progenitor cells in the bone marrow of patients with postinfarction heart failure. J Am Coll Cardiol. 2007;49:2341-2349. (Pubitemid 46891715)
12. Ballard VL, Edelberg JM. Stem cells for cardiovascular repair-the challenges of the aging heart. J Mol Cell Cardiol. 2008;45:582-592.
13. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, Isner JM. Isolation of putative progenitor endothelial cells for angiogenesis. Science. 1997;275:964-967. (Pubitemid 27087709)
14. Shi Y, Desponts C, Do JT, Hahm HS, Scholer HR, Ding S. Induction of pluripotent stem cells from mouse embryonic fibroblasts by Oct4 and Klf4 with small-molecule compounds. Cell Stem Cell. 2008;3:568-574.
15. Kawada H, Fujita J, Kinjo K, Matsuzaki Y, Tsuma M, Miyatake H, Muguruma Y, Tsuboi K, Itabashi Y, Ikeda Y, Ogawa S, Okano H, Hotta T, Ando K, Fukuda K. Nonhematopoietic mesenchymal stem cells can be mobilized and differentiate into cardiomyocytes after myocardial infarction. Blood. 2004;104:3581-3587. (Pubitemid 39564430)
16. Minasi MG, Riminucci M, De Angelis L, Borello U, Berarducci B, Innocenzi A, Caprioli A, Sirabella D, Baiocchi M, De Maria R, Boratto R, Jaffredo T, Broccoli V, Bianco P, Cossu G. The meso-angioblast: a multipotent, self-renewing cell that originates from the dorsal aorta and differentiates into most mesodermal tissues. Development. 2002;129: 2773-2783. (Pubitemid 34874259)
17. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell. 2007;131:861-872. (Pubitemid 350138099)
18. Nishikawa S, Goldstein RA, Nierras CR. The promise of human induced pluripotent stem cells for research and therapy. Nat Rev Mol Cell Biol. 2008;9:725-729.
19. Ziebart T, Yoon CH, Trepels T, Wietelmann A, Braun T, Kiessling F, Stein S, Grez M, Ihling C, Muhly-Reinholz M, Carmona G, Urbich C, Zeiher AM, Dimmeler S. Sustained persistence of transplanted proan-giogenic cells contributes to neovascularization and cardiac function after ischemia. Circ Res. 2008;103:1327-1334.
20. Ball SG, Shuttleworth CA, Kielty CM. Vascular endothelial growth factor can signal through platelet-derived growth factor receptors. J Cell Biol. 2007;177:489-500. (Pubitemid 46718277)
21. Jiang Y, Vaessen B, Lenvik T, Blackstad M, Reyes M, Verfaillie CM. Multipotent progenitor cells can be isolated from postnatal murine bone marrow, muscle, and brain. Exp Hematol. 2002;30:896-904. (Pubitemid 34845893)
22. Kogler G, Sensken S, Airey JA, Trapp T, Muschen M, Feldhahn N, Liedtke S, Sorg RV, Fischer J, Rosenbaum C, Greschat S, Knipper A, Bender J, Degistirici O, Gao J, Caplan AI, Colletti EJ, Almeida-Porada G, Muller HW, Zanjani E, Wernet P. A new human somatic stem cell from placental cord blood with intrinsic pluripotent differentiation potential. J Exp Med. 2004;200:123-135. (Pubitemid 38982172)
23. Ingram DA, Mead LE, Tanaka H, Meade V, Fenoglio A, Mortell K, Pollok K, Ferkowicz MJ, Gilley D, Yoder MC. Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood. Blood. 2004;104:2752-2760. (Pubitemid 39434958)
24. Lin Y, Weisdorf DJ, Solovey A, Hebbel RP. Origins of circulating endothelial cells and endothelial outgrowth from blood. J Clin Invest. 2000;105:71-77. (Pubitemid 30036389)
25. Timmermans F, Van Hauwermeiren F, De Smedt M, Raedt R, Plasschaert F, De Buyzere ML, Gillebert TC, Plum J, Vandekerckhove B. Endothelial outgrowth cells are not derived from CD133+ cells or CD45+ hematopoietic precursors. Arterioscler Thromb Vasc Biol. 2007;27:1572-1579. (Pubitemid 46986112)
26. Cossu G, Bianco P. Mesoangioblasts-vascular progenitors for extravascular mesodermal tissues. Curr Opin Genet Dev. 2003;13: 537-542. (Pubitemid 37204932)
27. Dellavalle A, Sampaolesi M, Tonlorenzi R, Tagliafico E, Sacchetti B, Perani L, Innocenzi A, Galvez BG, Messina G, Morosetti R, Li S, Belicchi M, Peretti G, Chamberlain JS, Wright WE, Torrente Y, Ferrari S, Bianco P, Cossu G. Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells. Nat Cell Biol. 2007;9:255-267. (Pubitemid 46349927)
28. Guo Y, Chan R, Ramsey H, Li W, Xie X, Shelley WC, Martinez-Barbera JP, Bort B, Zaret K, Yoder M, Hromas R. The homeoprotein Hex is required for hemangioblast differentiation. Blood. 2003;102:2428-2435. (Pubitemid 37193579)
29. Hart A, Melet F, Grossfeld P, Chien K, Jones C, Tunnacliffe A, Favier R, Bernstein A. Fli-1 is required for murine vascular and megakaryocytic development and is hemizygously deleted in patients with thrombocytopenia. Immunity. 2000;13:167-177.
30. Kwon C, Arnold J, Hsiao EC, Taketo MM, Conklin BR, Srivastava D. Canonical Wnt signaling is a positive regulator of mammalian cardiac progenitors. Proc Natl Acad Sci USA. 2007;104:10894-10899. (Pubitemid 47175197)
31. Naito AT, Shiojima I, Akazawa H, Hidaka K, Morisaki T, Kikuchi A, Komuro I. Developmental stage-specific biphasic roles of Wnt/beta-catenin signaling in cardiomyogenesis and hematopoiesis. Proc Natl Acad Sci USA. 2006;103:19812- 19817. (Pubitemid 46037513)
32. 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. Postnatal isl1+ cardioblasts enter fully differentiated cardiomyocyte lineages. Nature. 2005;433:647-653. (Pubitemid 40282999)
33. 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. (Pubitemid 36258727)
34. Hida N, Nishiyama N, Miyoshi S, Kira S, Segawa K, Uyama T, Mori T, Miyado K, Ikegami Y, Cui C, Kiyono T, Kyo S, Shimizu T, Okano T, Sakamoto M, Ogawa S, Umezawa A. Novel cardiac precursor-like cells from human menstrual blood-derived mesenchymal cells. Stem Cells. 2008;26:1695-1704.
35. Chambers I, Colby D, Robertson M, Nichols J, Lee S, Tweedie S, Smith A. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell. 2003;113:643-655. (Pubitemid 36694189)
36. Mitsui K, Tokuzawa Y, Itoh H, Segawa K, Murakami M, Takahashi K, Maruyama M, Maeda M, Yamanaka S. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell. 2003;113:631-642. (Pubitemid 36694188)
37. Liu Y, Asakura M, Inoue H, Nakamura T, Sano M, Niu Z, Chen M, Schwartz RJ, Schneider MD. Sox17 is essential for the specification of cardiac mesoderm in embryonic stem cells. Proc Natl Acad Sci USA. 2007;104:3859-3864. (Pubitemid 47181544)
38. Lee KD, Kuo TK, Whang-Peng J, Chung YF, Lin CT, Chou SH, Chen JR, Chen YP, Lee OK. In vitro hepatic differentiation of human mesenchymal stem cells. Hepatology. 2004;40:1275-1284. (Pubitemid 39657001)
39. Romero-Ramos M, Vourc'h P, Young HE, Lucas PA, Wu Y, Chivatakarn O, Zaman R, Dunkelman N, el-Kalay MA, Chesselet MF. Neuronal differentiation of stem cells isolated from adult muscle. J Neurosci Res. 2002;69:894-907.
40. Aranguren XL, Luttun A, Clavel C, Moreno C, Abizanda G, Barajas MA, Pelacho B, Uriz M, Arana M, Echavarri A, Soriano M, Andreu EJ, Merino J, Garcia-Verdugo JM, Verfaillie CM, Prosper F. In vitro and in vivo arterial differentiation of human multipotent adult progenitor cells. Blood. 2007;109:2634-2642. (Pubitemid 46425914)
41. Galvez BG, Sampaolesi M, Barbuti A, Crespi A, Covarello D, Brunelli S, Dellavalle A, Crippa S, Balconi G, Cuccovillo I, Molla F, Staszewsky L, Latini R, Difrancesco D, Cossu G. Cardiac mesoangioblasts are committed, self-renewable progenitors, associated with small vessels of juvenile mouse ventricle. Cell Death Differ. 2008;15:1417-1428.
42. Yang L, Soonpaa MH, Adler ED, Roepke TK, Kattman SJ, Kennedy M, Henckaerts E, Bonham K, Abbott GW, Linden RM, Field LJ, Keller GM. Human cardiovascular progenitor cells develop from a KDR + embryonic-stem-cell-derived population. Nature. 2008;453:524-528. (Pubitemid 351733312)
43. Masui S, Nakatake Y, Toyooka Y, Shimosato D, Yagi R, Takahashi K, Okochi H, Okuda A, Matoba R, Sharov AA, Ko MS, Niwa H. Pluripotency governed by Sox2 via regulation of Oct3/4 expression in mouse embryonic stem cells. Nat Cell Biol. 2007;9:625-635. (Pubitemid 47214724)
44. Dimos JT, Rodolfa KT, Niakan KK, Weisenthal LM, Mitsumoto H, Chung W, Croft GF, Saphier G, Leibel R, Goland R, Wichterle H, Henderson CE, Eggan K. Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science. 2008;321:1218-1221.
45. Kim JB, Sebastiano V, Wu G, Arauzo-Bravo MJ, Sasse P, Gentile L, Ko K, Ruau D, Ehrich M, van den Boom D, Meyer J, Hubner K, Bernemann C, Ortmeier C, Zenke M, Fleischmann BK, Zaehres H, Scholer HR. Oct4-induced pluripotency in adult neural stem cells. Cell. 2009;136: 411-419.
46. Hong H, Takahashi K, Ichisaka T, Aoi T, Kanagawa O, Nakagawa M, Okita K, Yamanaka S. Suppression of induced pluripotent stem cell generation by the p53-p21 pathway. Nature. 2009;460:1132-1135.
47. Stadtfeld M, Nagaya M, Utikal J, Weir G, Hochedlinger K. Induced pluripotent stem cells generated without viral integration. Science. 2008; 322:945-949.
48. Okita K, Nakagawa M, Hyenjong H, Ichisaka T, Yamanaka S. Generation of mouse induced pluripotent stem cells without viral vectors. Science. 2008;322:949-953.
49. Huangfu D, Osafune K, Maehr R, Guo W, Eijkelenboom A, Chen S, Muhlestein W, Melton DA. Induction of pluripotent stem cells from primary human fibroblasts with only Oct4 and Sox2. Nat Biotechnol. 2008;26:1269-1275.