Sca-1+ cardiac stem cells mediate acute cardioprotection via paracrine factor SDF-1 following myocardial ischemia/reperfusion

PLoS ONE

Volumn 6, Issue 12, 2011, Pages

  Huang, Chunyan ^a   Gu, Hongmei ^a   Yu, Qing ^a   Manukyan, Mariuxi C ^a   Poynter, Jeffrey A ^a   Wang, Meijing ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA1 INTEGRIN; CD31 ANTIGEN; CD34 ANTIGEN; CD45 ANTIGEN; CHEMOKINE RECEPTOR CXCR4; HERMES ANTIGEN; PLERIXAFOR; SMALL INTERFERING RNA; STAT3 PROTEIN; STEM CELL FACTOR RECEPTOR; STROMAL CELL DERIVED FACTOR 1; TRANSCRIPTION FACTOR GATA 4; VASCULOTROPIN; CARDIOTONIC AGENT; LY ANTIGEN; LY6A PROTEIN, MOUSE; MEMBRANE PROTEIN; MESSENGER RNA; PROTEIN KINASE B; VASCULOTROPIN A;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DOWN REGULATION; GENETIC TRANSFECTION; HEART FUNCTION; HEART MUSCLE CELL; HEART MUSCLE INJURY; HEART MUSCLE ISCHEMIA; HEART MUSCLE REPERFUSION; HEART PROTECTION; MALE; MOUSE; NONHUMAN; PARACRINE SIGNALING; PROTEIN EXPRESSION; RECEPTOR BLOCKING; STEM CELL; ANIMAL; C57BL MOUSE; CULTURE MEDIUM; CYTOLOGY; DRUG EFFECT; GENETICS; HEART FUNCTION TEST; HEART MUSCLE; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; REPERFUSION INJURY; SIGNAL TRANSDUCTION; STEM CELL TRANSPLANTATION;

ANIMALS; ANTIGENS, LY; CARDIOTONIC AGENTS; CELL DIFFERENTIATION; CHEMOKINE CXCL12; CULTURE MEDIA, CONDITIONED; HEART FUNCTION TESTS; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; PARACRINE COMMUNICATION; PROTO-ONCOGENE PROTEINS C-AKT; RNA, MESSENGER; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; STEM CELL TRANSPLANTATION; STEM CELLS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 83455205944     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0029246     Document Type: Article

References (48)

1. Uemura R, Xu M, Ahmad N, Ashraf M, (2006) Bone marrow stem cells prevent left ventricular remodeling of ischemic heart through paracrine signaling. Circ Res 98: 1414-1421.
2. Mirotsou M, Zhang Z, Deb A, Zhang L, Gnecchi M, et al. (2007) 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 U S A 104: 1643-1648.
3. Cho HJ, Lee N, Lee JY, Choi YJ, Ii M, et al. (2007) Role of host tissues for sustained humoral effects after endothelial progenitor cell transplantation into the ischemic heart. J Exp Med 204: 3257-3269.
4. Lim SY, Kim YS, Ahn Y, Jeong MH, Hong MH, et al. (2006) The effects of mesenchymal stem cells transduced with Akt in a porcine myocardial infarction model. Cardiovasc Res 70: 530-542.
5. Wang Y, Abarbanell AM, Herrmann JL, Weil BR, Manukyan MC, et al. TLR4 inhibits mesenchymal stem cell (MSC) STAT3 activation and thereby exerts deleterious effects on MSC-mediated cardioprotection. PLoS One 5: e4206.
6. Wang M, Tan J, Wang Y, Meldrum KK, Dinarello CA, et al. (2009) IL-18 binding protein-expressing mesenchymal stem cells improve myocardial protection after ischemia or infarction. Proc Natl Acad Sci U S A 106: 17499-17504.
7. Markel TA, Wang Y, Herrmann JL, Crisostomo PR, Wang M, et al. (2008) VEGF is critical for stem cell-mediated cardioprotection and a crucial paracrine factor for defining the age threshold in adult and neonatal stem cell function. Am J Physiol Heart Circ Physiol 295: H2308-2314.
8. Oh H, Bradfute SB, Gallardo TD, Nakamura T, Gaussin V, et al. (2003) Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proc Natl Acad Sci U S A 100: 12313-12318.
9. Matsuura K, Nagai T, Nishigaki N, Oyama T, Nishi J, et al. (2004) Adult cardiac Sca-1-positive cells differentiate into beating cardiomyocytes. J Biol Chem 279: 11384-11391.
10. Mouquet F, Pfister O, Jain M, Oikonomopoulos A, Ngoy S, et al. (2005) Restoration of cardiac progenitor cells after myocardial infarction by self-proliferation and selective homing of bone marrow-derived stem cells. Circ Res 97: 1090-1092.
11. Pfister O, Mouquet F, Jain M, Summer R, Helmes M, et al. (2005) CD31- but Not CD31+ cardiac side population cells exhibit functional cardiomyogenic differentiation. Circ Res 97: 52-61.
12. Beltrami AP, Barlucchi L, Torella D, Baker M, Limana F, et al. (2003) Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 114: 763-776.
13. Urbanek K, Quaini F, Tasca G, Torella D, Castaldo C, et al. (2003) Intense myocyte formation from cardiac stem cells in human cardiac hypertrophy. Proc Natl Acad Sci U S A 100: 10440-10445.
14. Domian IJ, Chiravuri M, van der Meer P, Feinberg AW, Shi X, et al. (2009) Generation of functional ventricular heart muscle from mouse ventricular progenitor cells. Science 326: 426-429.
15. Bu L, Jiang X, Martin-Puig S, Caron L, Zhu S, et al. (2009) Human ISL1 heart progenitors generate diverse multipotent cardiovascular cell lineages. Nature 460: 113-117.
16. Laugwitz KL, Moretti A, Lam J, Gruber P, Chen Y, et al. (2005) Postnatal isl1+ cardioblasts enter fully differentiated cardiomyocyte lineages. Nature 433: 647-653.
17. Beltrami AP, Urbanek K, Kajstura J, Yan SM, Finato N, et al. (2001) Evidence that human cardiac myocytes divide after myocardial infarction. N Engl J Med 344: 1750-1757.
18. Chimenti I, Smith RR, Li TS, Gerstenblith G, Messina E,et al. Relative roles of direct regeneration versus paracrine effects of human cardiosphere-derived cells transplanted into infarcted mice. Circ Res 106: 971-980.
19. Matsuura K, Honda A, Nagai T, Fukushima N, Iwanaga K, et al. (2009) Transplantation of cardiac progenitor cells ameliorates cardiac dysfunction after myocardial infarction in mice. J Clin Invest 119: 2204-2217.
20. Miyamoto S, Kawaguchi N, Ellison GM, Matsuoka R, Shin'oka T, et al. (2010) Characterization of long-term cultured c-kit+ cardiac stem cells derived from adult rat hearts. Stem Cells Dev 19: 105-116.
21. Llamas B, Belanger S, Picard S, Deschepper CF, (2007) Cardiac mass and cardiomyocyte size are governed by different genetic loci on either autosomes or chromosome Y in recombinant inbred mice. Physiol Genomics 31: 176-182.
22. Muller P, Kazakov A, Semenov A, Bohm M, Laufs U, (2008) Pressure-induced cardiac overload induces upregulation of endothelial and myocardial progenitor cells. Cardiovasc Res 77: 151-159.
23. Hu X, Dai S, Wu WJ, Tan W, Zhu X, et al. (2007) Stromal cell derived factor-1 alpha confers protection against myocardial ischemia/reperfusion injury: role of the cardiac stromal cell derived factor-1 alpha CXCR4 axis. Circulation 116: 654-663.
24. Huang C, Gu H, Zhang W, Manukyan MC, Shou W, et al. (2011) SDF-1/CXCR4 mediates acute protection of cardiac function through myocardial STAT3 signaling following global ischemia/reperfusion injury. Am J Physiol Heart Circ Physiol 301: H1496-1505.
25. Huang C, Gu H, Wang Y, Wang M, (2011) Estrogen-induced SDF-1 production is mediated by estrogen receptor-alpha in female hearts after acute ischemia and reperfusion. Surgery 150: 197-203.
26. Saxena A, Fish JE, White MD, Yu S, Smyth JW, et al. (2008) Stromal cell-derived factor-1alpha is cardioprotective after myocardial infarction. Circulation 117: 2224-2231.
27. Ahr B, Denizot M, Robert-Hebmann V, Brelot A, Biard-Piechaczyk M, (2005) Identification of the cytoplasmic domains of CXCR4 involved in Jak2 and STAT3 phosphorylation. J Biol Chem 280: 6692-6700.
28. Gao H, Priebe W, Glod J, Banerjee D, (2009) Activation of signal transducers and activators of transcription 3 and focal adhesion kinase by stromal cell-derived factor 1 is required for migration of human mesenchymal stem cells in response to tumor cell-conditioned medium. Stem Cells 27: 857-865.
29. Wang Y, Haider HK, Ahmad N, Xu M, Ge R, et al. (2006) Combining pharmacological mobilization with intramyocardial delivery of bone marrow cells over-expressing VEGF is more effective for cardiac repair. J Mol Cell Cardiol 40: 736-745.
30. Tang YL, Zhao Q, Zhang YC, Cheng L, Liu M, et al. (2004) Autologous mesenchymal stem cell transplantation induce VEGF and neovascularization in ischemic myocardium. Regul Pept 117: 3-10.
31. Pfeiffer M, Hartmann TN, Leick M, Catusse J, Schmitt-Graeff A, et al. (2009) Alternative implication of CXCR4 in JAK2/STAT3 activation in small cell lung cancer. Br J Cancer 100: 1949-1956.
32. Burger M, Hartmann T, Krome M, Rawluk J, Tamamura H, et al. (2005) Small peptide inhibitors of the CXCR4 chemokine receptor (CD184) antagonize the activation, migration, and antiapoptotic responses of CXCL12 in chronic lymphocytic leukemia B cells. Blood 106: 1824-1830.
33. Negoro S, Kunisada K, Tone E, Funamoto M, Oh H, et al. (2000) Activation of JAK/STAT pathway transduces cytoprotective signal in rat acute myocardial infarction. Cardiovasc Res 47: 797-805.
34. Schwarze MM, Hawley RG, (1995) Prevention of myeloma cell apoptosis by ectopic bcl-2 expression or interleukin 6-mediated up-regulation of bcl-xL. Cancer Res 55: 2262-2265.
35. Bromberg J, (2002) Stat proteins and oncogenesis. J Clin Invest 109: 1139-1142.
36. Brar BK, Stephanou A, Wagstaff MJ, Coffin RS, Marber MS, et al. (1999) Heat shock proteins delivered with a virus vector can protect cardiac cells against apoptosis as well as against thermal or hypoxic stress. J Mol Cell Cardiol 31: 135-146.
37. Stephanou A, Latchman DS, (1999) Transcriptional regulation of the heat shock protein genes by STAT family transcription factors. Gene Expr 7: 311-319.
38. Meldrum DR, Meng X, Shames BD, Pomerantz B, Donnahoo KK, et al. (1999) Liposomal delivery of heat-shock protein 72 into the heart prevents endotoxin-induced myocardial contractile dysfunction. Surgery 126: 135-141.
39. Osugi T, Oshima Y, Fujio Y, Funamoto M, Yamashita A, et al. (2002) Cardiac-specific activation of signal transducer and activator of transcription 3 promotes vascular formation in the heart. J Biol Chem 277: 6676-6681.
40. Jacoby JJ, Kalinowski A, Liu MG, Zhang SS, Gao Q, et al. (2003) Cardiomyocyte-restricted knockout of STAT3 results in higher sensitivity to inflammation, cardiac fibrosis, and heart failure with advanced age. Proc Natl Acad Sci U S A 100: 12929-12934.
41. Hilfiker-Kleiner D, Hilfiker A, Fuchs M, Kaminski K, Schaefer A, et al. (2004) Signal transducer and activator of transcription 3 is required for myocardial capillary growth, control of interstitial matrix deposition, and heart protection from ischemic injury. Circ Res 95: 187-195.
42. Wang M, Zhang W, Crisostomo P, Markel T, Meldrum KK, et al. (2007) STAT3 mediates bone marrow mesenchymal stem cell VEGF production. J Mol Cell Cardiol 42: 1009-1015.
43. Wang M, Tsai BM, Crisostomo PR, Meldrum DR, (2006) Tumor necrosis factor receptor 1 signaling resistance in the female myocardium during ischemia. Circulation 114: I282-289.
44. Wang M, Crisostomo PR, Markel TA, Wang Y, Meldrum DR, (2008) Mechanisms of sex differences in TNFR2-mediated cardioprotection. Circulation 118: S38-45.
45. Huang C, Gu H, Zhang W, Manukyan MC, Shou W, et al. (2011) SDF-1/CXCR4 mediates acute protection of cardiac function through myocardial STAT3 signaling following global ischemia/reperfusion injury. Am J Physiol Heart Circ Physiol [In press].
46. Wang M, Crisostomo P, Wairiuko GM, Meldrum DR, (2006) Estrogen receptor-alpha mediates acute myocardial protection in females. Am J Physiol Heart Circ Physiol 290: H2204-2209.
47. Wang M, Wang Y, Weil B, Abarbanell A, Herrmann J, et al. (2009) Estrogen receptor beta mediates increased activation of PI3K/Akt signaling and improved myocardial function in female hearts following acute ischemia. Am J Physiol Regul Integr Comp Physiol 296: R972-978.
48. Goodman MD, Koch SE, Fuller-Bicer GA, Butler KL, (2008) Regulating RISK: a role for JAK-STAT signaling in postconditioning? Am J Physiol Heart Circ Physiol 295: H1649-1656.