Injured cardiomyocytes promote dental pulp mesenchymal stem cell homing

Biochimica et Biophysica Acta - General Subjects

Volumn 1840, Issue 7, 2014, Pages 2152-2161

  Di Scipio, F ^a   Sprio, A E ^a   Folino, A ^a   Carere, M E ^a   Salamone, P ^a   Yang, Z ^a   Berrone, M ^b   Prat, M ^c   Losano, G ^a   Rastaldo, R ^a,d   Berta, G N ^a,d  

^a UNIVERSITY OF TURIN   (Italy)

^b SAN LUIGI GONZAGA HOSPITAL   (Italy)

^c UNIVERSITY OF EASTERN PIEDMONT   (Italy)

^d National Institute of Cardiovascular Research INRC   (Italy)

Author keywords

Cardiac ischemia; Cell migration; Dental pulp stem cell; Hypoxic cardiomyocyte

Indexed keywords

CONNEXIN 43; FIBROBLAST GROWTH FACTOR 2; GROWTH FACTOR; HGF PROTEIN; NERVE CELL ADHESION MOLECULE; SDF 1 PROTEIN; UNCLASSIFIED DRUG; VASCULOTROPIN; VON WILLEBRAND FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL CONTACT; CELL DAMAGE; CELL DIFFERENTIATION; CELL HOMING; CELL INTERACTION; CELL MIGRATION; CHEMOTAXIS; CONTROLLED STUDY; EMBRYO; EMBRYONIC STRUCTURES; EX VIVO STUDY; HEART; HEART DEVELOPMENT; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; IN VITRO STUDY; MESENCHYMAL STEM CELL; NEURAL CREST CELL; NONHUMAN; ORGANOGENESIS; PRIORITY JOURNAL; RAT; SPLANCHNOCRANIUM; TOOTH PULP;

CARDIAC ISCHEMIA; CELL MIGRATION; DENTAL PULP STEM CELL; HYPOXIC CARDIOMYOCYTE;

ANIMALS; DENTAL PULP; HEART INJURIES; HUMANS; ISCHEMIA; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MYOCARDIAL INFARCTION; MYOCYTES, CARDIAC; RATS; REGENERATION;

EID: 84899883026     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2014.03.005     Document Type: Article

References (61)

1. P. Anversa, J. Kajstura, and G. Olivetti Myocyte death in heart failure Curr. Opin. Cardiol. 11 1996 245 251
2. J.J. Gajarsa, and R.A. Kloner Left ventricular remodeling in the post-infarction heart: a review of cellular, molecular mechanisms, and therapeutic modalities Heart Fail. Rev. 16 2011 13 21
3. B.I. Jugdutt Remodeling of the myocardium and potential targets in the collagen degradation and synthesis pathways Curr. Drug Targets Cardiovasc. Haematol. Disord. 3 2003 1 30
4. B.I. Jugdutt Ventricular remodeling after infarction and the extracellular collagen matrix: when is enough enough? Circulation 108 2003 1395 1403
5. G. Forte, S. Pagliari, F. Pagliari, M. Ebara, P. Di Nardo, and T. Aoyagi Towards the generation of patient-specific patches for cardiac repair Stem Cell Rev. 9 2013 313 325
6. J. Liu, Z. Zhang, Y. Liu, C. Guo, Y. Gong, S. Yang, M. Ma, Z. Li, W.Q. Gao, and Z. He Generation, characterization, and potential therapeutic applications of cardiomyocytes from various stem cells Stem Cells Dev. 21 2012 2095 2110
7. E. Willems, M. Lanier, E. Forte, F. Lo, J. Cashman, and M. Mercola A chemical biology approach to myocardial regeneration J. Cardiovasc. Transl. Res. 3 2011 340 350
8. P.Z. Gerczuk, and R.A. Kloner An update on cardioprotection: a review of the latest adjunctive therapies to limit myocardial infarction size in clinical trials J. Am. Coll. Cardiol. 59 2012 969 978
9. J. Leor, Y. Amsalem, and S. Cohen Cells, scaffolds, and molecules for myocardial tissue engineering Pharmacol. Ther. 105 2005 151 163
10. G. Forte, S. Pietronave, G. Nardone, A. Zamperone, E. Magnani, S. Pagliari, F. Pagliari, C. Giacinti, C. Nicoletti, A. Musaró, M. Rinaldi, M. Ribezzo, C. Comoglio, E. Traversa, T. Okano, M. Minieri, M. Prat, and P. Di Nardo Human cardiac progenitor cell grafts as unrestricted source of supernumerary cardiac cells in healthy murine hearts Stem Cells 29 2011 2051 2061
11. A. Zamperone, S. Pietronave, S. Merlin, D. Colangelo, G. Ranaldo, E. Medico, F. Di Scipio, G.N. Berta, A. Follenzi, and M. Prat Isolation and characterization of a spontaneously immortalized multipotent mesenchymal cell line derived from mouse subcutaneous adipose tissue Stem Cells Dev. 22 2013 2873 2884
12. R. Bolli, A.R. Chugh, D. D'Amario, J.H. Loughran, M.F. Stoddard, S. Ikram, G.M. Beache, S.G. Wagner, A. Leri, T. Hosoda, F. Sanada, J.B. Elmore, P. Goichberg, D. Cappetta, N.K. Solankhi, I. Fahsah, D.G. Rokosh, M.S. Slaughter, J. Kajstura, and P. Anversa Cardiac stem cells in patients with ischaemic cardiomyopathy (SCIPIO): initial results of a randomised phase 1 trial Lancet 378 2011 1847 1857
13. E. Forte, I. Chimenti, L. Barile, R. Gaetani, F. Angelini, V. Ionta, E. Messina, and A. Giacomello Cardiac cell therapy: the next (re)generation Stem Cell Rev. 7 2011 1018 1030
14. A.R. Williams, and J.M. Hare Mesenchymal stem cells: biology, pathophysiology, translational findings, and therapeutic implications for cardiac disease Circ. Res. 109 2011 923 940
15. D.K. Singla Stem cells in the infarcted heart J. Cardiovasc. Transl. Res. 3 2010 73 78
16. M.P. Gallo, R. Ramella, G. Alloatti, C. Penna, P. Pagliaro, A. Marcantoni, F. Bonafé, G. Losano, and R. Levi Limited plasticity of mesenchymal stem cells cocultured with adult cardiomyocytes J. Cell. Biochem. 100 2007 86 99
17. A.E. Sprio, F. Di Scipio, S. Raimondo, P. Salamone, F. Pagliari, S. Pagliari, A. Folino, G. Forte, S. Geuna, P. Di Nardo, and G.N. Berta Self-renewal and multipotency coexist in a long-term cultured adult rat dental pulp stem cell line: an exception to the rule? Stem Cells Dev. 21 2012 3278 3288
18. F. Bonavita, C. Stefanelli, E. Giordano, M. Columbaro, A. Facchini, F. Bonafè, C.M. Caldarera, and C. Guarnieri H9c2 cardiac myoblasts undergo apoptosis in a model of ischemia consisting of serum deprivation and hypoxia: inhibition by PMA FEBS Lett. 536 2003 85 91
19. G.N. Berta, P. Salamone, A.E. Sprio, F. Di Scipio, L.M. Marinos, S. Sapino, M.E. Carlotti, R. Cavalli, and F. Di Carlo Chemoprevention of 7,12-dimethylbenz[a]anthracene (DMBA)-induced oral carcinogenesis in hamster cheek pouch by topical application of resveratrol complexed with 2-hydroxypropyl-beta-cyclodextrin Oral Oncol. 46 2010 42 48
20. A.L. Ponte, E. Marais, N. Gallay, A. Langonné, B. Delorme, O. Hérault, P. Charbord, and J. Domenech The in vitro migration capacity of human bone marrow mesenchymal stem cells: comparison of chemokine and growth factor chemotactic activities Stem Cells 25 2007 1737 1745
21. I.A. Potapova, I.S. Cohen, and S.V. Doronin Apoptotic endothelial cells demonstrate increased adhesiveness for human mesenchymal stem cells J. Cell. Physiol. 219 2009 23 30
22. R. Rastaldo, S. Cappello, A. Folino, G.N. Berta, A.E. Sprio, G. Losano, M. Samaja, and P. Pagliaro Apelin-13 limits infarct size and improves cardiac postischemic mechanical recovery only if given after ischemia Am. J. Physiol. Heart Circ. Physiol. 300 2011 H2308 H2315
23. C. Penna, S. Raimondo, G. Ronchi, R. Rastaldo, D. Mancardi, S. Cappello, G. Losano, S. Geuna, and P. Pagliaro Early homing of adult mesenchymal stem cells in normal and infarcted isolated beating hearts J. Cell. Mol. Med. 12 2008 507 521
24. M.L. Kirby, and M.R. Hutson Factors controlling cardiac neural crest cell migration Cell Adh. Migr. 4 2010 609 621
25. M. Morganti, A. Carpi, B. Amo-Takyi, A. Sagripanti, A. Nicolini, R. Giardino, and C. Mittermayer Von Willebrand's factor mediates the adherence of human tumoral cells to human endothelial cells and ticlopidine interferes with this effect Biomed. Pharmacother. 54 2000 431 436
26. I.A. Potapova, I.S. Cohen, and S.V. Doronin Von Willebrand factor increases endothelial cell adhesiveness for human mesenchymal stem cells by activating p38 mitogen-activated protein kinase Stem Cell Res. Ther. 1 2010 35
27. J.Y. Kresh, and A. Chopra Intercellular and extracellular mechanotransduction in cardiac myocytes Pflugers Arch. 462 2011 75 87
28. G.L. Radice N-cadherin-mediated adhesion and signaling from development to disease: lessons from mice Prog. Mol. Biol. Transl. Sci. 116 2013 263 289
29. A.T. Askari, S. Unzek, Z.B. Popovic, C.K. Goldman, F. Forudi, M. Kiedrowski, A. Rovner, S.G. Ellis, J.D. Thomas, P.E. DiCorleto, E.J. Topol, and M.S. Penn Effect of stromal-cell-derived factor 1 on stem-cell homing and tissue regeneration in ischaemic cardiomyopathy Lancet 362 2003 697 703
30. S. Liao, J. Bodmer, D. Pietras, M. Azhar, T. Doetschman, and J. Schultz Jel Biological functions of the low and high molecular weight protein isoforms of fibroblast growth factor-2 in cardiovascular development and disease Dev. Dyn. 238 2009 249 264
31. S.Q. Liu, B.J. Tefft, D. Zhang, D. Roberts, D.J. Schuster, and A. Wu Cardioprotective mechanisms activated in response to myocardial ischemia Mol. Cell. Biomech. 8 2011 319 338
32. T. Nakamura, S. Mizuno, K. Matsumoto, Y. Sawa, H. Matsuda, and T. Nakamura Myocardial protection from ischemia/reperfusion injury by endogenous and exogenous HGF J. Clin. Invest. 106 2000 1511 1519
33. N.G. Frangogiannis, C.W. Smith, and M.L. Entman The inflammatory response in myocardial infarction Cardiovasc. Res. 53 2002 31 47
34. K. Pillarisetti, and S.K. Gupta Cloning and relative expression analysis of rat stromal cell derived factor-1 (SDF-1)1: SDF-1 alpha mRNA is selectively induced in rat model of myocardial infarction Inflammation 25 2001 293 300
35. G.M. Ellison, B. Nadal-Ginard, and D. Torella Optimizing cardiac repair and regeneration through activation of the endogenous cardiac stem cell compartment J. Cardiovasc. Transl. Res. 5 2012 667 677
36. G.M. Ellison, C. Vicinanza, A.J. Smith, I. Aquila, A. Leone, C.D. Waring, B.J. Henning, G.G. Stirparo, R. Papait, M. Scarfò, V. Agosti, G. Viglietto, G. Condorelli, C. Indolfi, S. Ottolenghi, D. Torella, and B. Nadal-Ginard Adult c-kitpos cardiac stem cells are necessary and sufficient for functional cardiac regeneration and repair Cell 154 2013 827 842
37. F.L. Xiang, X. Lu, Y. Liu, and Q. Feng Cardiomyocyte-specific overexpression of human stem cell factor protects against myocardial ischemia and reperfusion injury Int. J. Cardiol. 168 2013 3486 3494
38. B.C. Jensen, and C. Patterson Heart factory or fiction? Cardiac progenitor cells and regeneration Circulation 128 2013 2181 2182
39. M.J. Goumans, T.P. de Boer, A.M. Smits, L.W. van Laake, P. van Vliet, C.H. Metz, T.H. Korfage, K.P. Kats, R. Hochstenbach, G. Pasterkamp, M.C. Verhaar, M.A. van der Heyden, D. de Kleijn, C.L. Mummery, T.A. van Veen, J.P. Sluijter, and P.A. Doevendans TGF-beta1 induces efficient differentiation of human cardiomyocyte progenitor cells into functional cardiomyocytes in vitro Stem Cell Res. 1 2007 138 149
40. S.J. Kattman, E.D. Adler, and G.M. Keller Specification of multipotential cardiovascular progenitor cells during embryonic stem cell differentiation and embryonic development Trends Cardiovasc. Med. 17 2007 240 246
41. Y. Chai, X. Jiang, Y. Ito, P. Bringas Jr., J. Han, D.H. Rowitch, P. Soriano, A.P. McMahon, and H.M. Sucov Fate of the mammalian cranial neural crest during tooth and mandibular morphogenesis Development 127 2000 1671 1679
42. T. Nakamura, M.C. Colbert, and J. Robbins Neural crest cells retain multipotential characteristics in the developing valves and label the cardiac conduction system Circ. Res. 98 2006 1547 1554
43. J.E. Sadler Biochemistry and genetics of von Willebrand factor Annu. Rev. Biochem. 67 1998 395 424
44. C.J. Wei, R. Francis, X. Xu, and C.W. Lo Connexin43 associated with an N-cadherin-containing multiprotein complex is required for gap junction formation in NIH3T3 cells J. Biol. Chem. 280 2005 19925 19936
45. N.J. Severs, A.F. Bruce, E. Dupont, and S. Rothery Remodelling of gap junctions and connexin expression in diseased myocardium Cardiovasc. Res. 80 2008 9 19
46. J.F. Dong, J.L. Moake, L. Nolasco, A. Bernardo, W. Arceneaux, C.N. Shrimpton, A.J. Schade, L.V. McIntire, K. Fujikawa, and J.A. López ADAMTS-13 rapidly cleaves newly secreted ultralarge von Willebrand factor multimers on the endothelial surface under flowing conditions Blood 100 2002 4033 4039
47. C. Gandhi, D.G. Motto, M. Jensen, S.R. Lentz, and A.K. Chauhan ADAMTS13 deficiency exacerbates VWF-dependent acute myocardial ischemia/reperfusion injury in mice Blood 120 2012 5224 5230
48. E. Andermarcher, M.A. Surani, and E. Gherardi Co-expression of the HGF/SF and c-met genes during early mouse embryogenesis precedes reciprocal expression in adjacent tissues during organogenesis Dev. Genet. 18 1996 254 266
49. R.T. Böttcher, and C. Niehrs Fibroblast growth factor signaling during early vertebrate development Endocr. Rev. 26 2005 63 77
50. Y. Kubota, and K. Ito Chemotactic migration of mesencephalic neural crest cells in the mouse Dev. Dyn. 217 2000 170 179
51. R. McLennan, J.M. Teddy, J.C. Kasemeier-Kulesa, M.H. Romine, and P.M. Kulesa Vascular endothelial growth factor (VEGF) regulates cranial neural crest migration in vivo Dev. Biol. 339 2010 114 125
52. D.A. Rappolee, A. Iyer, and Y. Patel Hepatocyte growth factor and its receptor are expressed in cardiac myocytes during early cardiogenesis Circ. Res. 78 1996 1028 1036
53. P. Spirito, Y.M. Fu, Z.X. Yu, S.E. Epstein, and W. Casscells Immunohistochemical localization of basic and acidic fibroblast growth factors in the developing rat heart Circulation 84 1991 322 332
54. C. Roggia, C. Ukena, M. Böhm, and H. Kilter Hepatocyte growth factor (HGF) enhances cardiac commitment of differentiating embryonic stem cells by activating PI3 kinase Exp. Cell Res. 313 2007 921 930
55. A. Chiriac, A. Terzic, S. Park, Y. Ikeda, R. Faustino, and T.J. Nelson SDF-1-enhanced cardiogenesis requires CXCR4 induction in pluripotent stem cells J. Cardiovasc. Transl. Res. 3 2010 674 682
56. J. Tao, Y. Doughman, K. Yang, D. Ramirez-Bergeron, and M. Watanabe Epicardial HIF signaling regulates vascular precursor cell invasion into the myocardium Dev. Biol. 376 2013 136 149
57. H.E. Olivey, L.A. Compton, and J.V. Barnett Coronary vessel development: the epicardium delivers Trends Cardiovasc. Med. 14 2004 247 251
58. H. Lie-Venema, N.M. van den Akker, N.A. Bax, E.M. Winter, S. Maas, T. Kekarainen, R.C. Hoeben, M.C. deRuiter, R.E. Poelmann, and A.C. Gittenberger-de Groot Origin, fate, and function of epicardium-derived cells (EPDCs) in normal and abnormal cardiac development ScientificWorldJournal 12 2007 1777 1798
59. K.J. Lavine, and D.M. Ornitz Fibroblast growth factors and Hedgehogs: at the heart of the epicardial signaling center Trends Genet. 24 2008 33 40
60. C.D. Rogers, A. Saxena, and M.E. Bronner Sip1 mediates an E-cadherin-to-N-cadherin switch during cranial neural crest EMT J. Cell Biol. 203 2013 835 847
61. C. Gandia, A. Armiñan, J.M. García-Verdugo, E. Lledó, A. Ruiz, M.D. Miñana, J. Sanchez-Torrijos, R. Payá, V. Mirabet, F. Carbonell-Uberos, M. Llop, J.A. Montero, and P. Sepúlveda Human dental pulp stem cells improve left ventricular function, induce angiogenesis, and reduce infarct size in rats with acute myocardial infarction Stem Cells 26 2008 638 645