Notch1 in bone marrow-derived cells mediates cardiac repair after myocardial infarction

Circulation

Volumn 123, Issue 8, 2011, Pages 866-876

  Li, Yuxin ^a,d   Hiroi, Yukio ^a   Ngoy, Soeun ^a,b   Okamoto, Ryuji ^a   Noma, Kensuke ^a   Wang, Chao Yung ^a   Wang, Hong Wei ^a   Zhou, Qian ^a   Radtke, Freddy ^c   Liao, Ronglih ^a,b   Liao, James K ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD STEM CELL INSTITUTE   (United States)

^c UNIVERSITY OF LAUSANNE   (Switzerland)

^d NIHON UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

angiogenesis; gene therapy; myocardial infarction; stem cells

Indexed keywords

NOTCH1 RECEPTOR;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; BONE MARROW TRANSPLANTATION; CELL FUNCTION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; GENE DELETION; GENE OVEREXPRESSION; HEART FUNCTION; HEART INFARCTION; HEART INFARCTION SIZE; HEART LEFT VENTRICLE CONTRACTION; HEART MUSCLE CELL; HEART MUSCLE INJURY; HEART MUSCLE ISCHEMIA; HEART PROTECTION; HEART REPAIR; HEMIZYGOSITY; MALE; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; TISSUE REPAIR; WILD TYPE;

ANIMALS; BONE MARROW CELLS; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; DISEASE MODELS, ANIMAL; GREEN FLUORESCENT PROTEINS; MALE; MESENCHYMAL STEM CELLS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOCARDIAL INFARCTION; MYOCYTES, CARDIAC; RECEPTOR, NOTCH1; SIGNAL TRANSDUCTION; TISSUE THERAPY;

EID: 79952449930     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.110.947531     Document Type: Article

References (52)

1. 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. 2005;96:127-137 (Pubitemid 40095762)
2. Li Y, Fukuda N, Yokoyama S, Kusumi Y, Hagikura K, Kawano T, Takayama T, Matsumoto T, Satomi A, Honye J, Mugishima H, Mitsumata M, Saito S. Effects of G-CSF on cardiac remodeling and arterial hyperplasia in rats. Eur J Pharmacol. 2006;549:98-106 (Pubitemid 44441254)
3. Strauer BE, Brehm M, Zeus T, Kostering M, Hernandez A, Sorg RV, Kogler G, Wernet P. Repair of infarcted myocardium by autologous intracoronary mononuclear bone marrow cell transplantation in humans. Circulation. 2002;106:1913-1918 (Pubitemid 35176294)
4. Schachinger V, Erbs S, Elsasser A, Haberbosch W, Hambrecht R, Holschermann 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)
5. Hare JM, Traverse JH, Henry TD, Dib N, Strumpf RK, Schulman SP, Gerstenblith G, DeMaria AN, Denktas AE, Gammon RS, Hermiller JB Jr, Reisman MA, Schaer GL, Sherman W. A randomized, double-blind, placebo-controlled, dose-escalation study of intravenous adult human mesenchymal stem cells (prochymal) after acute myocardial infarction. J Am Coll Cardiol. 2009;54:2277-2286
6. Schachinger V, Erbs S, Elsasser A, Haberbosch W, Hambrecht R, Holschermann H, Yu J, Corti R, Mathey DG, Hamm CW, Suselbeck T, Werner N, Haase J, Neuzner J, Germing A, Mark B, Assmus B, Tonn T, Dimmeler S, Zeiher AM. Improved clinical outcome after intracoronary administration of bone-marrow-derived progenitor cells in acute myocardial infarction: final 1-year results of the REPAIR-AMI trial. Eur Heart J. 2006;27:2775-2783 (Pubitemid 44871463)
7. Assmus B, Rolf A, Erbs S, Elsasser A, Haberbosch W, Hambrecht R, Tillmanns H, Yu J, Corti R, Mathey DG, Hamm CW, Suselbeck T, Tonn T, Dimmeler S, Dill T, Zeiher AM, Schachinger V. Clinical outcome 2 years after intracoronary administration of bone marrow-derived progenitor cells in acute myocardial infarction. Circ Heart Fail. 2010;3:89-96
8. Chiba S. Notch signaling in stem cell systems. Stem Cells. 2006;24: 2437-2447 (Pubitemid 44674304)
9. Niessen K, Karsan A. Notch signaling in the developing cardiovascular system. Am J Physiol Cell Physiol. 2007;293:C1-C11 (Pubitemid 47105000)
10. Nemir M, Pedrazzini T. Functional role of Notch signaling in the developing and postnatal heart. J Mol Cell Cardiol. 2008;45:495-504
11. Li Y, Takeshita K, Liu PY, Satoh M, Oyama N, Mukai Y, Chin MT, Krebs L, Kotlikoff MI, Radtke F, Gridley T, Liao JK. Smooth muscle Notch1 mediates neointimal formation after vascular injury. Circulation. 2009;119:2686-2692
12. Varnum-Finney B, Xu L, Brashem-Stein C, Nourigat C, Flowers D, Bakkour S, Pear WS, Bernstein ID. Pluripotent, cytokine-dependent, hematopoietic stem cells are immortalized by constitutive Notch1 signaling. Nat Med. 2000;6:1278-1281
13. Conboy IM, Conboy MJ, Wagers AJ, Girma ER, Weissman IL, Rando TA. Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature. 2005;433:760-764 (Pubitemid 40292986)
14. Mizutani K, Yoon K, Dang L, Tokunaga A, Gaiano N. Differential Notch signalling distinguishes neural stem cells from intermediate progenitors. Nature. 2007;449:351-355 (Pubitemid 47443472)
15. Bolos V, Grego-Bessa J, de la Pompa JL. Notch signaling in development and cancer. Endocr Rev. 2007;28:339-363 (Pubitemid 46984831)
16. Takeshita K, Satoh M, Ii M, Silver M, Limbourg FP, Mukai Y, Rikitake Y, Radtke F, Gridley T, Losordo DW, Liao JK. Critical role of endothelial Notch1 signaling in postnatal angiogenesis. Circ Res. 2007;100:70-78 (Pubitemid 46066775)
17. Kwon SM, Eguchi M, Wada M, Iwami Y, Hozumi K, Iwaguro H, Masuda H, Kawamoto A, Asahara T. Specific Jagged-1 signal from bone marrow microenvironment is required for endothelial progenitor cell development for neovascularization. Circulation. 2008;118:157-165
18. Boni A, Urbanek K, Nascimbene A, Hosoda T, Zheng H, Delucchi F, Amano K, Gonzalez A, Vitale S, Ojaimi C, Rizzi R, Bolli R, Yutzey KE, Rota M, Kajstura J, Anversa P, Leri A. Notch1 regulates the fate of cardiac progenitor cells. Proc Natl Acad Sci USA. 2008;105: 15529-15534
19. Collesi C, Zentilin L, Sinagra G, Giacca M. Notch1 signaling stimulates proliferation of immature cardiomyocytes. J Cell Biol. 2008;183: 117-128
20. Campa VM, Gutierrez-Lanza R, Cerignoli F, Diaz-Trelles R, Nelson B, Tsuji T, Barcova M, Jiang W, Mercola M. Notch activates cell cycle reentry and progression in quiescent cardiomyocytes. J Cell Biol. 2008; 183:129-141
21. Kratsios P, Catela C, Salimova E, Huth M, Berno V, Rosenthal N, Mourkioti F. Distinct roles for cell-autonomous Notch signaling in cardiomyocytes of the embryonic and adult heart. Circ Res. 2010;106: 559-572
22. Gude NA, Emmanuel G, Wu W, Cottage CT, Fischer K, Quijada P, Muraski JA, Alvarez R, Rubio M, Schaefer E, Sussman MA. Activation of Notch-mediated protective signaling in the myocardium. Circ Res. 2008;102:1025-1035 (Pubitemid 351667856)
23. Krebs LT, Shutter JR, Tanigaki K, Honjo T, Stark KL, Gridley T. Haploinsufficient lethality and formation of arteriovenous malformations in Notch pathway mutants. Genes Dev. 2004;18:2469-2473 (Pubitemid 39362888)
24. Agah R, Frenkel PA, French BA, Michael LH, Overbeek PA, Schneider MD. Gene recombination in postmitotic cells: targeted expression of Cre recombinase provokes cardiac-restricted, site-specific rearrangement in adult ventricular muscle in vivo. J Clin Invest. 1997;100:169-179 (Pubitemid 27311255)
25. Radtke F, Wilson A, Stark G, Bauer M, van Meerwijk J, MacDonald HR, Aguet M. Deficient T cell fate specification in mice with an induced inactivation of Notch1. Immunity. 1999;10:547-558 (Pubitemid 29262657)
26. Rottman JN, Ni G, Khoo M, Wang Z, Zhang W, Anderson ME, Madu EC. Temporal changes in ventricular function assessed echocardiographically in conscious and anesthetized mice. J Am Soc Echocardiogr. 2003;16:1150-1157 (Pubitemid 37371659)
27. Xu M, Uemura R, Dai Y, Wang Y, Pasha Z, Ashraf M. In vitro and in vivo effects of bone marrow stem cells on cardiac structure and function. J Mol Cell Cardiol. 2007;42:441-448 (Pubitemid 46135600)
28. da Silva Meirelles L, Caplan AI, Nardi NB. In search of the in vivo identity of mesenchymal stem cells. Stem Cells. 2008;26:2287-2299
29. Xiang F, Sakata Y, Cui L, Youngblood JM, Nakagami H, Liao JK, Liao R, Chin MT. Transcription factor CHF1/Hey2 suppresses cardiac hypertrophy through an inhibitory interaction with GATA4. Am J Physiol Heart Circ Physiol. 2006;290:H1997-H2006
30. Xu ZL, Zhou B, Cong XL, Liu YJ, Xu B, Li YH, Gu J, Han ZC. Hemangiopoietin supports animal survival and accelerates hematopoietic recovery of chemotherapy-suppressed mice. Eur J Haematol. 2007;79:477-485 (Pubitemid 350126676)
31. Conlon RA, Reaume AG, Rossant J. Notch1 is required for the coordinate segmentation of somites. Development. 1995;121:1533-1545
32. Krebs LT, Xue Y, Norton CR, Shutter JR, Maguire M, Sundberg JP, Gallahan D, Closson V, Kitajewski J, Callahan R, Smith GH, Stark KL, Gridley T. Notch signaling is essential for vascular morphogenesis in mice. Genes Dev. 2000;14:1343-1352 (Pubitemid 30397078)
33. Swiatek PJ, Lindsell CE, del Amo FF, Weinmaster G, Gridley T. Notch1 is essential for postimplantation development in mice. Genes Dev. 1994; 8:707-719 (Pubitemid 24116765)
34. Lawson ND, Vogel AM, Weinstein BM. Sonic hedgehog and vascular endothelial growth factor act upstream of the Notch pathway during arterial endothelial differentiation. Dev Cell. 2002;3:127-136 (Pubitemid 34778401)
35. Wang W, Campos AH, Prince CZ, Mou Y, Pollman MJ. Coordinate Notch3-hairy-related transcription factor pathway regulation in response to arterial injury: mediator role of platelet-derived growth factor and ERK. J Biol Chem. 2002;277:23165-23171 (Pubitemid 34952142)
36. Brand T. Heart development: molecular insights into cardiac specification and early morphogenesis. Dev Biol. 2003;258:1-19 (Pubitemid 36637027)
37. Espinosa L, Ingles-Esteve J, Aguilera C, Bigas A. Phosphorylation by glycogen synthase kinase-3 beta down-regulates Notch activity, a link for Notch and Wnt pathways. J Biol Chem. 2003;278:32227-32235 (Pubitemid 37048415)
38. Niessen K, Karsan A. Notch signaling in cardiac development. Circ Res. 2008;102:1169-1181
39. Matsuura K, Honda A, Nagai T, Fukushima N, Iwanaga K, Tokunaga M, Shimizu T, Okano T, Kasanuki H, Hagiwara N, Komuro I. Transplantation of cardiac progenitor cells ameliorates cardiac dysfunction after myocardial infarction in mice. J Clin Invest. 2009;119:2204-2217
40. Harada M, Qin Y, Takano H, Minamino T, Zou Y, Toko H, Ohtsuka M, Matsuura K, Sano M, Nishi J, Iwanaga K, Akazawa H, Kunieda T, Zhu W, Hasegawa H, Kunisada K, Nagai T, Nakaya H, Yamauchi-Takihara K, Komuro I. G-CSF prevents cardiac remodeling after myocardial infarction by activating the Jak-Stat pathway in cardiomyocytes. Nat Med. 2005;11:305-311 (Pubitemid 40460559)
41. Bonaros N, Sondermejer H, Schuster M, Rauf R, Wang SF, Seki T, Skerrett D, Itescu S, Kocher AA. CCR3-and CXCR4-mediated interactions regulate migration of CD34- human bone marrow progenitors to ischemic myocardium and subsequent tissue repair. J Thorac Cardiovasc Surg. 2008;136:1044-1053
42. Abbott JD, Huang Y, Liu D, Hickey R, Krause DS, Giordano FJ. Stromal cell-derived factor-1alpha plays a critical role in stem cell recruitment to the heart after myocardial infarction but is not sufficient to induce homing in the absence of injury. Circulation. 2004;110:3300-3305 (Pubitemid 39557491)
43. Orlic D, Kajstura J, Chimenti S, Limana F, Jakoniuk I, Quaini F, Nadal-Ginard B, Bodine DM, Leri A, Anversa P. Mobilized bone marrow cells repair the infarcted heart, improving function and survival. Proc Natl Acad Sci USA. 2001;98:10344-10349 (Pubitemid 32803022)
44. Wang L, Wang YC, Hu XB, Zhang BF, Dou GR, He F, Gao F, Feng F, Liang YM, Dou KF, Han H. Notch-RBP-J signaling regulates the mobilization and function of endothelial progenitor cells by dynamic modulation of CXCR4 expression in mice. Available at: http://www.plosone. org/article/info%3Adoi%2F10.1371%2Fjournal. pone.0007572. Accessed January 27, 2011
45. Haider H, Jiang S, Idris NM, Ashraf M. IGF-1-overexpressing mesenchymal stem cells accelerate bone marrow stem cell mobilization via paracrine activation of SDF-1alpha/CXCR4 signaling to promote myocardial repair. Circ Res. 2008;103:1300-1308
46. Wang YC, Hu XB, He F, Feng F, Wang L, Li W, Zhang P, Li D, Jia ZS, Liang YM, Han H. Lipopolysaccharide-induced maturation of bone marrow-derived dendritic cells is regulated by Notch signaling through the up-regulation of CXCR4. J Biol Chem. 2009;284:15993-16003
47. Bigas A, Martin DI, Milner LA. Notch1 and Notch2 inhibit myeloid differentiation in response to different cytokines. Mol Cell Biol. 1998;18: 2324-2333 (Pubitemid 28152679)
48. 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 (Pubitemid 43948066)
49. Ripa RS, Jorgensen E, Wang Y, Thune JJ, Nilsson JC, Sondergaard L, Johnsen HE, Kober L, Grande P, Kastrup J. Stem cell mobilization induced by subcutaneous granulocyte-colony stimulating factor to improve cardiac regeneration after acute ST-elevation myocardial infarction: result of the double-blind, randomized, placebo-controlled Stem Cells in Myocardial Infarction (STEMMI) trial. Circulation. 2006;113:1983-1992
50. Ripa RS, Haack-Sorensen M, Wang Y, Jorgensen E, Mortensen S, Bindslev L, Friis T, Kastrup J. Bone marrow derived mesenchymal cell mobilization by granulocyte-colony stimulating factor after acute myocardial infarction: results from the Stem Cells in Myocardial Infarction (STEMMI) trial. Circulation. 2007;116(suppl):I-24-I-30
51. Iwata H, Manabe I, Fujiu K, Takeda N, Eguchi K, Sata M, R. N. Bone marrow-derived cells contribute to vascular inflammation but do not differentiate into smooth muscle cell lineages. Circulation. 2009; 120(suppl):S-1090-S-1091
52. Nahrendorf M, Swirski FK, Aikawa E, Stangenberg L, Wurdinger T, Figueiredo JL, Libby P, Weissleder R, Pittet MJ. The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. J Exp Med. 2007;204:3037-3047 (Pubitemid 350179569)