Sca-1 + stem cell survival and engraftment in the infarcted heart: Dual role for preconditioning-induced connexin-43

Circulation

Volumn 119, Issue 19, 2009, Pages 2587-2596

  Lu, Gang ^a   Haider, Husnain K ^a   Jiang, Shujia ^a   Ashraf, Muhammad ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

Angiogenesis; Apoptosis; Connexin 43; Insulin like growth factor 1; Stem cells

Indexed keywords

ACTININ; ATAXIN 1; CASPASE 3; CONNEXIN 43; CYTOCHROME C; GLUCOSE; LACTATE DEHYDROGENASE; OXYGEN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; RNA; SOMATOMEDIN C; TRANSCRIPTION FACTOR GATA 4; AKT1 PROTEIN, MOUSE; LY ANTIGEN; LY6A PROTEIN, MOUSE; MEMBRANE PROTEIN; RECOMBINANT PROTEIN; SMALL INTERFERING RNA;

ACUTE HEART INFARCTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD VESSEL; CELL DENSITY; CELL DIFFERENTIATION; CELL PROTECTION; CELL SURVIVAL; CELL TRANSPLANTATION; CONFOCAL MICROSCOPY; DOWN REGULATION; ENGRAFTMENT; ENZYME INHIBITION; ENZYME RELEASE; FEMALE; HEART EJECTION FRACTION; HEART FUNCTION; HEART INFARCTION; HEART INFARCTION SIZE; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; RAT; RNA INTERFERENCE; STEM CELL; UPREGULATION; ANIMAL; APOPTOSIS; C57BL MOUSE; CELL CULTURE; CELL HYPOXIA; DRUG ANTAGONISM; DRUG EFFECT; FISCHER 344 RAT; GENETICS; HEART INFARCTION PREVENTION; MALE; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; METABOLISM; MOUSE; MULTIPOTENT STEM CELL; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; TRANSPLANTATION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; ANTIGENS, LY; APOPTOSIS; CELL HYPOXIA; CELLS, CULTURED; CONNEXIN 43; FEMALE; GLUCOSE; INSULIN-LIKE GROWTH FACTOR I; ISCHEMIC PRECONDITIONING, MYOCARDIAL; MALE; MEMBRANE PROTEINS; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STEM CELLS; MICE; MICE, INBRED C57BL; MULTIPOTENT STEM CELLS; MYOCARDIAL INFARCTION; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, INBRED F344; RECOMBINANT PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 66349117300     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.108.827691     Document Type: Article

References (40)

1. Kudo M, Wang Y, Wani MA, Xu M, Ayub A, Ashraf M. Implantation of bone marrow stem cells reduces the infarction and fibrosis in ischemic mouse heart. J Mol Cell Cardiol. 2003;35:1113-1119.
2. Kajstura J, Rota M, Whang B, Cascapera S, Hosoda T, Bearzi C, Nur-zynska 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. 2005;96:127-137.
3. 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.
4. Couzin J. Clinical trials: a shot of bone marrow can help the heart. Science. 2006;313:1715-1716.
5. Pouzet B, Vilquin JT, Hagege AA, Scorsin M, Messas E, Fiszman M, Schwartz K, Menasche P. Factors affecting functional outcome after autologous skeletal myoblast transplantation. Ann Thorac Surg. 2001;71: 844-850.
6. 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.
7. Tang YL, Tang Y, Zhang YC, Qian K, Shen L, Phillips MI. Improved graft mesenchymal stem cell survival in ischemic heart with a hypoxia-regulated heme oxygenase-1 vector. J Am Coll Cardiol. 2005;46: 1339-1350.
8. Suzuki K, Smolenski RT, Jayakumar J, Murtuza B, Brand NJ, Yacoub MH. Heat shock treatment enhances graft cell survival in skeletal myoblast transplantation to the heart. Circulation. 2000; 102: HI216-III221.
9. Giardina SF, Mikami M, Goubaeva F, Yang J. Connexin-43 confers resistance to hydrogen peroxide-mediated apoptosis. Biochem Biophys Res Commun. 2007;362:747-752.
10. Krysko DV, Mussche S, Leybaert L, D'Herde K. Gap junctional communication and connexin-43 expression in relation to apoptotic cell death and survival of granulosa cells. J Histochem Cytochem. 2004;52: 1199-1207.
11. Mese G, Richard G, White TW. Gap junctions: basic structure and function. J Invest Dermatol. 2007;127:2516-2524.
12. Duffy HS, Fort AG, Spray DC. Cardiac connexins: genes to nexus. Adv Cardiol. 2006;42:1-17.
13. Kang J, Kang N, Lovatt D, Torres A, Zhao Z, Lin J, Nedergaard M. Connexin-43 hemichannels are permeable to ATP. J Neurosci. 2008;28: 4702-4711.
14. Retamal MA, Schalper KA, Shoji KF, Orellana JA, Bennett MV, Saez JC. Possible involvement of different connexin-43 domains in plasma membrane permeabilization induced by ischemia-reperfusion. J Membr Biol. 2007;218:49-63.
15. Worsdorfer P, Maxeiner S, Markopoulos C, Kirfel G, Wulf V, Auth T, Urschel S, von Maltzahn J, Willecke K. Connexin expression and functional analysis of gap junctional communication in mouse embryonic stem cells. Stem Cells. 2008;26:431-439.
16. Lin JH, Lou N, Kang N, Takano T, Hu F, Han X, Xu Q, Lovatt D, Torres A, Willecke K, Yang J, Kang J, Nedergaard M. A central role of connexin-43 in hypoxic preconditioning. J Neurosci. 2008;28:681-695.
17. Hutnik CM, Pocrnich CE, Liu H, Laird DW, Shao Q. The protective effect of functional connexin-43 channels on a human epithelial cell line exposed to oxidative stress. Invest Ophthalmol Vis Sci. 2008;49: 800-806.
18. Goubaeva F, Mikami M, Giardina S, Ding B, Abe J, Yang J. Cardiac mitochondrial connexin-43 regulates apoptosis. Biochem Biophys Res Commun. 2007;352:97-103.
19. Roell W, Lewalter T, Sasse P, Tallini YN, Choi BR, Breitbach M, Doran R, Becher UM, Hwang SM, Bostani T, von Maltzahn J, Hofmann A, Reining S, Eiberger B, Gabris B, Pfeifer A, Welz A, Willecke K, Salama G, Schrickel JW, Kotlikoff MI, Fleischmann BK. Engraftment of connexin 43-expressing cells prevents post-infarct arrhythmia. Nature. 2007;450:819-824.
20. Srisakuldee W, Nickel BE, Fandrich RR, Jiang ZS, Kardami E. Administration of FGF-2 to the heart stimulates connexin-43 phosphorylation at protein kinase C target sites. Cell Commun Adhes. 2006; 13:13-19.
21. Kuhlmann MT, Kirchhof P, Klocke R, Hasib L, Stypmann J, Fabritz L, Stelljes M, Tian W, Zwiener M, Mueller M, Kienast J, Breithardt G, Nikol S. G-CSF/SCF reduces inducible arrhythmias in the infarcted heart potentially via increased connexin43 expression and arteriogenesis. J Exp Med. 2006;203:87-97.
22. Jia G, Mitra AK, Cheng G, Gangahar DM, Agrawal DK. Angiotensin II and IGF-1 regulate connexin-43 expression via ERK and p38 signaling pathways in vascular smooth muscle cells of coronary artery bypass conduits. J Surg Res. 2007;142:137-142.
23. Kulik G, Weber MJ. Akt-dependent and -independent survival signaling pathways utilized by IGF-I. Mol Cell Biol. 1998;18:6711-6718.
24. Desnoyers L, Simonette RA, Vandlen RL, Fendly BM. Novel non-isotopic method for the localization of receptors in tissue sections. J Histochem Cytochem. 2001;49:1509-1518.
25. Matthews KG, Devlin GP, Conaglen JV, Stuart SP, Mervyn Aitken W, Bass JJ. Changes in IGFs in cardiac tissue following myocardial infarction. J Endocrinol. 1999;163:433-445.
26. Davis ME, Hsieh PC, Takahashi T, Song Q, Zhang S, Kamm RD, Grodzinsky AJ, Anversa P, Lee RT. Local myocardial IGF-1 delivery with biotinylated peptide nanofibers improves cell therapy for myocardial infarction. Proc Natl Acad Sci U S A. 2006;103:8155-8160.
27. Kanemitsu N, Tambara K, Premaratne GU, Kimura Y, Tomita S, Kawamura T, Hasegawa K, Tabata Y, Komeda M. IGF-1 enhances the efficacy of myoblast transplantation with its multiple functions in the chronic myocardial infarction rat model. J Heart Lung Transplant. 2006; 25;1253-1262.
28. Haider HKh, Jiang S, Idris NM, Ashraf M. IGF-1-overexpressing mesenchymal stem cells accelerate bone marrow stem cell mobilization via paracrine activation of SDF-lalpha/CXCR4 signaling to promote myocardial repair. Circ Res. 2008;103:1300-1308.
29. Liu TB, Fedak PW, Weisel RD, Yasuda T, Kiani G, Mickle DA, Jia ZQ, Li RK. Enhanced IGF-1 expression improves smooth muscle cell engraftment after cell transplantation. Am J Physiol. 2004;287: H2840-H2849.
30. Kofidis T, de Bruin JL, Yamane T, Balsam LB, Lebl DR, Swijnenburg RJ, Tanaka M, Weissman IL, Robbins RC. IGF promotes engraftment, differentiation, and functional improvement after transfer of ESCs for myocardial restoration. Stem Cells. 2004;22:1239-1245.
31. Uemura R, Xu M, Ahmad N, Ashraf M. Bone marrow stem cells prevent left ventricular remodeling of ischemic heart through paracrine signaling. Circ Res. 2006;98:1414-1421.
32. Nakase T, Fushiki S, Sohl G, Theis M, Willecke K, Naus CC. Neuro-protective role of astrocytic gap junctions in ischemic stroke. Cell Commun Adhes. 2003; 10:413-417.
33. Plotkin LI, Manolagas SC, Bellido T. Transduction of cell survival signals by connexin-43 hemichannels. J Biol Chem. 2002;277: 8648-8657.
34. Boengler K, Dodoni G, Rodriguez-Sinovas A, Cabestrero A, Ruiz-Meana R, Gres P, Konietzka I, C. Lopez-Iglesias, Garcia-Dorado D, Di Lisa F, Heusch G, Schulz R. Connexin-43 in cardiomyocyte mitochondria and its increase by ischemic preconditioning. Cardiovasc Res. 2005;67: 234-244.
35. Rodriguez-Sinovas A, Boengler K, Cabestrero A, Gres P, Morente M, Ruiz-Meana M, Konietzka I, Miro E, Totzeck A, Heusch G, Schulz R, Garcia-Dorado D. Translocation of connexin-43 to the inner mitochondrial membrane of cardiomyocytes through HSP-90 dependent TOM pathway and its importance for cardioprotection. Circ Res. 2006;99: 93-101.
36. Bouchier-Hayes L, Martin SJ. CARD games in apoptosis and immunity. EMBO Rep. 2002;3:616-621.
37. Pijnappels DA, Schalij MJ, Ramkisoensing AA, van TJ, de Vries AA, van Der LA, Ypey DL, Atsma DE. Forced alignment of mesenchymal stem cells undergoing cardiomyogenic differentiation affects functional integration with cardiomyocyte cultures. Circ Res. 2008;103:167-176.
38. Bradfute SB, Graubert TA, Goodell MA. Roles of Sca-1 in hematopoietic stem/progenitor cell function. Exp Hematol. 2005;33:836-843.
39. 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. Cardiac stem cells possess growth factor-receptor systems that after activation regenerate the infarcted myocardium, improving ventricular function and long-term survival. Circ Res. 2005,97:663-673.
40. Gojo S, Gojo N, Takeda Y, Mori T, Abe H, Kyo S, Hata J, Umezawa A. In vivo cardiovasculogenesis by direct injection of isolated adult mesen chymal stem cells. Exp Cell Res. 2003;288:51-59.