Apelin-13 increases myocardial progenitor cells and improves repair postmyocardial infarction

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 303, Issue 5, 2012, Pages

  Li, Lanfang ^a   Zeng, Heng ^a   Chen, Jian Xiong ^a  

^a UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

Author keywords

c kit; Jagged1 notch3; Myocardial repair; Stromal cell derived factor 1 C X C chemokine receptor 4; Vascular progenitor cell

Indexed keywords

APELIN 13; CARDIAC AGENT; CD133 ANTIGEN; CHEMOKINE RECEPTOR CXCR4; ENDOTHELIAL NITRIC OXIDE SYNTHASE; JAGGED1; NOTCH3 RECEPTOR; PROTEIN KINASE B; STROMAL CELL DERIVED FACTOR 1ALPHA; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL HOMING; CONTROLLED STUDY; CORONARY ARTERY LIGATION; DRESSLER SYNDROME; HEART FUNCTION; HEART INFARCTION; HEART MUSCLE CELL; HEART MUSCLE FIBROSIS; HEART VENTRICLE HYPERTROPHY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; STEM CELL; UPREGULATION;

ANIMALS; ANTIGENS, CD; ANTIGENS, LY; APOPTOSIS; BIOLOGICAL MARKERS; CALCIUM-BINDING PROTEINS; CARDIOMEGALY; CARDIOTONIC AGENTS; CELL MOVEMENT; CELLS, CULTURED; CHEMOKINE CXCL12; DISEASE MODELS, ANIMAL; FIBROSIS; GLYCOPROTEINS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MYOCARDIAL INFARCTION; MYOCYTES, CARDIAC; NEOVASCULARIZATION, PHYSIOLOGIC; NITRIC OXIDE SYNTHASE TYPE III; PEPTIDES; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-KIT; RECEPTORS, CXCR4; RECEPTORS, NOTCH; RECOVERY OF FUNCTION; REGENERATION; STEM CELLS; TIME FACTORS; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VENTRICULAR FUNCTION, LEFT;

EID: 84865723579     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00366.2012     Document Type: Article

References (45)

1. Arboleda-Velasquez JF, Zhou Z, Shin HK, Louvi A, Kim HH, Savitz SI, Liao JK, Salomone S, Ayata C, Moskowitz MA, Artavanis-Tsakonas S. Linking notch signaling to ischemic stroke. Proc Natl Acad Sci USA 105: 4856-4861, 2008.
2. Askari AT, Unzek S, Popovic ZB, Goldman CK, Forudi F, Kiedrowski M, Rovner A, Ellis SG, Thomas JD, DiCorleto PE, Topol EJ, Penn MS. Effect of stromal-cell-derived factor 1 on stem-cell homing and tissue regeneration in ischaemic cardiomyopathy. Lancet 362: 697-703, 2003.
3. Barcelos LS, Duplaa C, Krankel N, Graiani G, Invernici G, Katare R, Siragusa M, Meloni M, Campesi I, Monica M, Simm A, Campagnolo P, Mangialardi G, Stevanato L, Alessandri G, Emanueli C, Madeddu P. Human CD133+ progenitor cells promote the healing of diabetic ischemic ulcers by paracrine stimulation of angiogenesis and activation of Wnt signaling. Circ Res 104: 1095-1102, 2009.
4. Britten MB, Abolmaali ND, Assmus B, Lehmann R, Honold J, Schmitt J, Vogl TJ, Martin H, Schachinger V, Dimmeler S, Zeiher AM. Infarct remodeling after intracoronary progenitor cell treatment in patients with acute myocardial infarction (TOPCARE-AMI): mechanistic insights from serial contrast-enhanced magnetic resonance imaging. Circulation 108: 2212-2218, 2003.
5. Chen JX, Stinnett A. Ang-1 gene therapy inhibits hypoxia-inducible factor-1α (HIF-1α)-prolyl-4-hydroxylase-2, stabilizes HIF-1α expression, and normalizes immature vasculature in db/db mice. Diabetes 57: 3335-3343, 2008.
6. Cox CM, D'Agostino SL, Miller MK, Heimark RL, Krieg PA. Apelin, the ligand for the endothelial G-protein-coupled receptor, APJ, is a potent angiogenic factor required for normal vascular development of the frog embryo. Dev Biol 296: 177-189, 2006.
7. Crisostomo PR, Abarbanell AM, Wang M, Lahm T, Wang Y, Meldrum DR. Embryonic stem cells attenuate myocardial dysfunction and inflammation after surgical global ischemia via paracrine actions. Am J Physiol Heart Circ Physiol 295: H1726-H1735, 2008.
8. D'Aniello C, Lonardo E, Iaconis S, Guardiola O, Liguoro AM, Liguori GL, Autiero M, Carmeliet P, Minchiotti G. G protein-coupled receptor APJ and its ligand apelin act downstream of Cripto to specify embryonic stem cells toward the cardiac lineage through extracellular signal-regulated kinase/p70S6 kinase signaling pathway. Circ Res 105: 231-238, 2009.
9. Dichgans M. Genetics of ischaemic stroke. Lancet Neurol 6: 149-161, 2007.
10. Domenga V, Fardoux P, Lacombe P, Monet M, Maciazek J, Krebs LT, Klonjkowski B, Berrou E, Mericskay M, Li Z, Tournier-Lasserve E, Gridley T, Joutel A. Notch3 is required for arterial identity and maturation of vascular smooth muscle cells. Genes Dev 18: 2730-2735, 2004.
11. Foldes G, Horkay F, Szokodi I, Vuolteenaho O, Ilves M, Lindstedt KA, Mayranpaa M, Sarman B, Seres L, Skoumal R, Lako-Futo Z, deChatel R, Ruskoaho H, Toth M. Circulating and cardiac levels of apelin, the novel ligand of the orphan receptor APJ, in patients with heart failure. Biochem Biophys Res Commun 308: 480-485, 2003.
12. Frederick JR, Fitzpatrick JR, III, McCormick RC, Harris DA, Kim AY, Muenzer JR, Marotta N, Smith MJ, Cohen JE, Hiesinger W, Atluri P, Woo YJ. Stromal cell-derived factor-1α activation of tissueengineered endothelial progenitor cell matrix enhances ventricular function after myocardial infarction by inducing neovasculogenesis. Circulation 122: S107-S117, 2010.
13. Gao LR, Xu RY, Zhang NK, Chen Y, Wang ZG, Zhu ZM, Fei YX, Cao Y, Xu HT, Yang Y. Increased apelin following bone marrow mononuclear cell transplantation contributes to the improvement of cardiac function in patients with severe heart failure. Cell Transplant 18: 1311-1318, 2009.
14. Gao LR, Zhang NK, Bai J, Ding QA, Wang ZG, Zhu ZM, Fei YX, Yang Y, Xu RY, Chen Y. The apelin-APJ pathway exists in cardiomyogenic cells derived from mesenchymal stem cells in vitro and in vivo. Cell Transplant 19: 949-958, 2010.
15. High FA, Jain R, Stoller JZ, Antonucci NB, Lu MM, Loomes KM, Kaestner KH, Pear WS, Epstein JA. Murine jagged1/notch signaling in the second heart field orchestrates Fgf8 expression and tissue-tissue interactions during outflow tract development. J Clin Invest 119: 1986-1996, 2009.
16. Hu X, Dai S, Wu WJ, Tan W, Zhu X, Mu J, Guo Y, Bolli R, Rokosh G. Stromal cell derived factor-1α confers protection against myocardial ischemia/reperfusion injury: role of the cardiac stromal cell derived factor-1α-CXCR4 axis. Circulation 116: 654-663, 2007.
17. Inui M, Fukui A, Ito Y, Asashima M. Xapelin and Xmsr are required for cardiovascular development in Xenopus laevis. Dev Biol 298: 188-200, 2006.
18. Invernici G, Madeddu P, Emanueli C, Parati EA, Alessandri G. Human fetal aorta-derived vascular progenitor cells: identification and potential application in ischemic diseases. Cytotechnology 58: 43-47, 2008.
19. Isner JM, Asahara T. Angiogenesis and vasculogenesis as therapeutic strategies for postnatal neovascularization. J Clin Invest 103: 1231-1236, 1999.
20. Jameel MN, Zhang J. Stem cell therapy for ischemic heart disease. Antioxid Redox Signal 13: 1879-1897, 2010.
21. Japp AG, Newby DE. The apelin-APJ system in heart failure: pathophysiologic relevance and therapeutic potential. Biochem Pharmacol 75: 1882-1892, 2008.
22. Joutel A, Monet-Lepretre M, Gosele C, Baron-Menguy C, Hammes A, Schmidt S, Lemaire-Carrette B, Domenga V, Schedl A, Lacombe P, Hubner N. Cerebrovascular dysfunction and microcirculation rarefaction precede white matter lesions in a mouse genetic model of cerebral ischemic small vessel disease. J Clin Invest 120: 433-445, 2010.
23. Kalin RE, Kretz MP, Meyer AM, Kispert A, Heppner FL, Brandli AW. Paracrine and autocrine mechanisms of apelin signaling govern embryonic and tumor angiogenesis. Dev Biol 305: 599-614, 2007.
24. Kidoya H, Ueno M, Yamada Y, Mochizuki N, Nakata M, Yano T, Fujii R, Takakura N. Spatial and temporal role of the apelin/APJ system in the caliber size regulation of blood vessels during angiogenesis. EMBO J 27: 522-534, 2008.
25. Kleinz MJ, Baxter GF. Apelin reduces myocardial reperfusion injury independently of PI3K/Akt and P70S6 kinase. Regul Pept 146: 271-277, 2008.
26. Kleinz MJ, Davenport AP. Immunocytochemical localization of the endogenous vasoactive peptide apelin to human vascular and endocardial endothelial cells. Regul Pept 118: 119-125, 2004.
27. Lee DK, Cheng R, Nguyen T, Fan T, Kariyawasam AP, Liu Y, Osmond DH, George SR, O'Dowd BF. Characterization of apelin, the ligand for the APJ receptor. J Neurochem 74: 34-41, 2000.
28. Lesnik Oberstein SA, Jukema JW, Van Duinen SG, Macfarlane PW, van Houwelingen HC, Breuning MH, Ferrari MD, Haan J. Myocardial infarction in cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy (CADASIL). Medicine (Baltimore) 82: 251-256, 2003.
29. O'Dowd BF, Heiber M, Chan A, Heng HH, Tsui LC, Kennedy JL, Shi X, Petronis A, George SR, Nguyen T. A human gene that shows identity with the gene encoding the angiotensin receptor is located on chromosome 11. Gene 136: 355-360, 1993.
30. Quazi R, Palaniswamy C, Frishman WH. The emerging role of apelin in cardiovascular disease and health. Cardiol Rev 17: 283-286, 2009.
31. Rastaldo R, Cappello S, Folino A, Berta GN, Sprio AE, Losano G, Samaja M, Pagliaro P. Apelin-13 limits infarct size and improves cardiac postischemic mechanical recovery only if given after ischemia. Am J Physiol Heart Circ Physiol 300: H2308-H2315, 2011.
32. Sasaki H, Fukuda S, Otani H, Zhu L, Yamaura G, Engelman RM, Das DK, Maulik N. Hypoxic preconditioning triggers myocardial angiogenesis: a novel approach to enhance contractile functional reserve in rat with myocardial infarction. J Mol Cell Cardiol 34: 335-348, 2002.
33. Schachinger V, Assmus B, Britten MB, Honold J, Lehmann R, Teupe C, Abolmaali ND, Vogl TJ, Hofmann WK, Martin H, Dimmeler S, Zeiher AM. Transplantation of progenitor cells and regeneration enhancement in acute myocardial infarction: final one-year results of the TOPCARE-AMI trial. J Am Coll Cardiol 44: 1690-1699, 2004.
34. Scott IC, Masri B, D'Amico LA, Jin SW, Jungblut B, Wehman AM, Baier H, Audigier Y, Stainier DY. The g protein-coupled receptor agtrl1b regulates early development of myocardial progenitors. Dev Cell 12: 403-413, 2007.
35. Simpkin JC, Yellon DM, Davidson SM, Lim SY, Wynne AM, Smith CC. Apelin-13 and apelin-36 exhibit direct cardioprotective activity against ischemia-reperfusion injury. Basic Res Cardiol 102: 518-528, 2007.
36. Suchting S, Freitas C, le NF, Benedito R, Breant C, Duarte A, Eichmann A. Negative regulators of vessel patterning. Novartis Found Symp 283: 77-80, 2007.
37. Szokodi I, Tavi P, Foldes G, Voutilainen-Myllyla S, Ilves M, Tokola H, Pikkarainen S, Piuhola J, Rysa J, Toth M, Ruskoaho H. Apelin, the novel endogenous ligand of the orphan receptor APJ, regulates cardiac contractility. Circ Res 91: 434-440, 2002.
38. Tano N, Kim HW, Ashraf M. microRNA-150 regulates mobilization and migration of bone marrow-derived mononuclear cells by targeting Cxcr4. PLos One 6: e23114, 2011.
39. Tatemoto K, Hosoya M, Habata Y, Fujii R, Kakegawa T, Zou MX, Kawamata Y, Fukusumi S, Hinuma S, Kitada C, Kurokawa T, Onda H, Fujino M. Isolation and characterization of a novel endogenous peptide ligand for the human APJ receptor. Biochem Biophys Res Commun 251: 471-476, 1998.
40. Tuo QH, Zeng H, Stinnett A, Yu H, Aschner JL, Liao DF, Chen JX. Critical role of angiopoietins/Tie-2 in hyperglycemic exacerbation of myocardial infarction and impaired angiogenesis. Am J Physiol Heart Circ Physiol 294: H2547-H2557, 2008.
41. van den Akker NM, Caolo V, Wisse LJ, Peters PP, Poelmann RE, Carmeliet P, Molin DG, Gittenberger-de Groot AC. Developmental coronary maturation is disturbed by aberrant cardiac vascular endothelial growth factor expression and notch signalling. Cardiovasc Res 78: 366-375, 2008.
42. Voo S, Dunaeva M, Eggermann J, Stadler N, Waltenberger J. Diabetes mellitus impairs CD133+ progenitor cell function after myocardial infarction. J Intern Med 265: 238-249, 2009.
43. Zeng H, Li L, Chen JX. Overexpression of angiopoietin-1 increases CD133+/c-kit+ cells and reduces myocardial apoptosis in db/db mouse infarcted hearts. PLos One 7: e35905, 2012.
44. Zeng XJ, Zhang LK, Wang HX, Lu LQ, Ma LQ, Tang CS. Apelin protects heart against ischemia/reperfusion injury in rat. Peptides 30: 1144-1152, 2009.
45. Zeng XX, Wilm TP, Sepich DS, Solnica-Krezel L. Apelin and its receptor control heart field formation during zebrafish gastrulation. Dev Cell 12: 391-402, 2007.