Cardiosphere conditioned media influence the plasticity of human mediastinal adipose tissue-derived mesenchymal stem cells

Cell Transplantation

Volumn 24, Issue 11, 2015, Pages 2307-2322

  Siciliano, Camilla ^a,b   Chimenti, Isotta ^a   Ibrahim, Mohsen ^c   Napoletano, Chiara ^a   Mangino, Giorgio ^a   Scafetta, Gaia ^a   Zoccai, Giuseppe Biondi ^a   Rendina, Erino Angelo ^c   Calogero, Antonella ^a   Frati, Giacomo ^a,d   De Falco, Elena ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d IRCCS NEUROMED   (Italy)

Author keywords

5 Azacytidine; Adipose tissue derived mesenchymal stem cells; Cardiac like differentiation; Cardiospheres (CSs); Conditioned media

Indexed keywords

ADIPOSE TISSUE DERIVED MESENCHYMAL STEM CELL; ADULT; ARTICLE; CARDIOSPHERE CONDITIONED MEDIUM; CELL PROLIFERATION; CELL TRANSDIFFERENTIATION; CLINICAL ARTICLE; CONTROLLED STUDY; CULTURE MEDIUM; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; HUMAN; HUMAN TISSUE; INTRACELLULAR SIGNALING; MALE; MESENCHYMAL STEM CELL; PLASTICITY; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; ADIPOSE TISSUE; ADULT STEM CELL; AGED; ANATOMY AND HISTOLOGY; CELL CULTURE TECHNIQUE; CONDITIONED MEDIUM; CYTOLOGY; DRUG EFFECTS; MEDIASTINUM; MESENCHYMAL STROMA CELL; MIDDLE AGED; SIGNAL TRANSDUCTION; STEM CELL NICHE;

CONDITIONED MEDIUM;

ADIPOSE TISSUE; ADULT; ADULT STEM CELLS; AGED; CELL CULTURE TECHNIQUES; CELL TRANSDIFFERENTIATION; CULTURE MEDIA, CONDITIONED; HUMANS; MALE; MEDIASTINUM; MESENCHYMAL STROMAL CELLS; MIDDLE AGED; SIGNAL TRANSDUCTION; STEM CELL NICHE;

EID: 84944220053     PISSN: 09636897     EISSN: 15553892     Source Type: Journal    
DOI: 10.3727/096368914X685771     Document Type: Article

References (57)

1. Altomare, C.; Barile, L.; Marangoni, S.; Rocchetti, M.; Alemanni, M.; Mostacciuolo, G.; Giacomello, A.; Messina, E.; Zaza, A. Caffeine-induced Ca(2+) signaling as an index of cardiac progenitor cells differentiation. Basic Res. Cardiol. 105(6):737–749; 2010.
2. Bayes-Genis, A.; Gálvez-Montón, C.; Prat-Vidal, C.; Soler Botija, C. Cardiac adipose tissue: A new frontier for cardiac regeneration? Int. J. Cardiol. 167(1):22–25; 2013.
3. Bergmann, O.; Bhardwaj, R. D.; Bernard, S.; Zdunek, S.; Barnabé-Heider, F.; Walsh, S.; Zupicich, J.; Alkass, K.; Buchholz, B. A.; Druid, H.; Joving, S.; Frisén, J. Evidence for cardiomyocyte renewal in humans. Science 324(5923):98–102; 2009.
4. Boquest, A. C.; Shahdadfar, A.; Frønsdal, K.; Sigurjonsson, O.; Tunheim, S. H.; Collas, P.; Brinchmann, J. E. Isolation and transcription profiling of purified uncultured human stromal stem cells: Alteration of gene expression after in vitro cell culture. Mol. Biol. Cell 16(3):1131–1141; 2005.
5. Casteilla, L.; Planat-Bénard, V.; Cousin, B.; Laharrague, P.; Bourin, P. Vascular and endothelial regeneration. Curr. Stem Cell Res. Ther. 5(2):141–144; 2010.
6. Chimenti, I.; Gaetani, R.; Barile, L.; Forte, E.; Ionta, V.; Angelini, F.; Frati, G.; Messina, E.; Giacomello, A. Isolation and expansion of adult cardiac stem/progenitor cells in the form of cardiospheres from human cardiac biopsies and murine hearts. Methods Mol. Biol. 879:327–338; 2012.
7. Chimenti, I.; Smith, R. R.; Li, T. S.; Gerstenblith, G.; Messina, E.; Giacomello, A.; Marbán, E. Relative roles of direct regeneration versus paracrine effects of human cardiosphere-derived cells transplanted into infarcted mice. Circ. Res. 106(5):971–980; 2010.
8. Choi, Y. S.; Dusting, G. J.; Stubbs, S.; Arunothayaraj, S.; Han, X. L.; Collas, P.; Morrison, W. A.; Dilley, R. J. Differentiation of human adipose-derived stem cells into beating cardiomyocytes. J. Cell. Mol. Med. 14(4):878–889; 2010.
9. Degeorge, B. R.; Rosenberg, M.; Eckstein, V.; Gao, E.; Herzog, N.; Katus, H. A.; Koch, W. J.; Frey, N.; Most, P. BMP-2 and FGF-2 synergistically facilitate adoption of a cardiac phenotype in somatic bone marrow c-kit+/Sca-1+ stem cells. Clin. Transl. Sci. 1(2):116–125; 2008.
10. DeUgarte, D. A.; Alfonso, Z.; Zuk, P. A.; Elbarbary, A.; Zhu, M.; Ashjian, P.; Benhaim, P.; Hedrick, M. H.; Fraser, J. K. Differential expression of stem cell mobilization-associated molecules on multi-lineage cells from adipose tissue and bone marrow. Immunol. Lett. 89(2–3):267–270; 2003.
11. Eshghi, S.; Schaffer, D. Engineering microenvironments to control stem cell fate and function. In: StemBook. Cambridge, MA: Harvard Stem Cell Institute; 2008.
12. Forte, E.; Chimenti, I.; Barile, L.; Gaetani, R.; Angelini, F.; Ionta, V.; Messina, E.; Giacomello, A. Cardiac cell therapy: The next (re)generation. Stem Cell Rev. 7(4):1018–1030; 2011.
13. Forte, E.; Miraldi, F.; Chimenti, I.; Angelini, F.; Zeuner, A.; Giacomello, A.; Mercola, M.; Messina, E. TGFb-dependent epithelial-to-mesenchymal transition is required to generate cardiospheres from human adult heart biopsies. Stem Cells Dev. 21(17):3081–3090; 2012.
14. Galvez-Monton, C.; Prat-Vidal, C.; Roura, S.; Soler-Botija, C.; Llucià-Valldeperas, A.; Díaz-Güemes, I.; SánchezMargallo, F. M.; Bayes-Genis, A. Post-infarction scar coverage using a pericardial-derived vascular adipose flap. Pre-clinical results. Int. J. Cardiol. 166(2):469–474; 2013.
15. Gaustad, K. G.; Boquest, A. C.; Anderson, B. E.; Gerdes, A. M.; Collas, P. Differentiation of human adipose tissue stem cells using extracts of rat cardiomyocytes. Biochem. Biophys. Res. Commun. 314(2):420–427; 2004.
16. Haider, H. K.; Ashraf, M. Preconditioning and stem cell survival. J. Cardiovasc. Transl. Res. 3(2):89–102; 2010.
17. Haigh, J. J. Role of VEGF in organogenesis. Organogenesis 4(4):247–256; 2008.
18. Hatzistergos, K. E.; Quevedo, H.; Oskouei, B. N.; Hu, Q.; Feigenbaum, G. S.; Margitich, I. S.; Mazhari, R.; Boyle, A. J.; Zambrano, J. P.; Rodriguez, J. E.; Dulce, R.; Pattany P. M.; Valdes D.; Revilla C.; Heldman A.W.; McNiece I.; Hare J. M. Bone marrow mesenchymal stem cells stimulate cardiac stem cell proliferation and differentiation. Circ. Res. 107(7):913–922; 2010.
19. Iso, Y.; Rao, K. S.; Poole, C. N.; Zaman, A. K.; Curril, I.; Sobel, B. E.; Kajstura, J.; Anversa, P.; Spees, J. L. Priming with ligands secreted by human stromal progenitor cells promotes grafts of cardiac stem/progenitor cells after myocardial infarction. Stem Cells 32(3):674–683; 2014.
20. Jakob, P.; Landmesser, U. Current status of cell-based therapy for heart failure. Curr. Heart Fail. Rep. 10(2):165–176; 2013.
21. Kannel, W. B. Incidence and epidemiology of heart failure. Heart Fail. Rev. 5(2):167–173; 2000.
22. Kinnaird, T.; Stabile, E.; Burnett, M. S.; Lee, C. W.; Barr, S.; Fuchs, S.; Epstein, S. E. Marrow-derived stromal cells express genes encoding a broad spectrum of arteriogenic cytokines and promote in vitro and in vivo arteriogenesis through paracrine mechanisms. Circ. Res. 94(5):678–685; 2004.
23. Koninckx, R.; Hensen, K.; Daniëls, A.; Moreels, M.; Lambrichts, I.; Jongen, H.; Clijsters, C.; Mees, U.; Steels, P.; Hendrikx, M.; Rummens, J. L. Human bone marrow stem cells co-cultured with neonatal rat cardiomyocytes display limited cardiomyogenic plasticity. Cytotherapy 11(6):778–792; 2009.
24. Lee, W. C.; Sepulveda, J. L.; Rubin, J. P.; Marra, K. G. Cardiomyogenic differentiation potential of human adipose precursor cells. Int. J. Cardiol. 133(3):399–401; 2009.
25. Li, L.; Xia, Y. Study of adipose tissue-derived mesenchymal stem cells transplantation for rats with dilated cardiomyopathy. Ann. Thorac. Cardiovasc. Surg. 20(5):398–406; 2014.
26. Li, T. S.; Cheng, K.; Lee, S. T.; Matsushita, S.; Davis, D.; Malliaras, K.; Zhang, Y.; Matsushita, N.; Smith, R. R.; Marbán, E. Cardiospheres recapitulate a niche-like microenvironment rich in stemness and cell-matrix interactions, rationalizing their enhanced functional potency for myocardial repair. Stem Cells 28(11):2088–2098; 2010.
27. Lizcano, J. M.; Morrice, N.; Cohen, P. Regulation of BAD by cAMP-dependent protein kinase is mediated via phosphorylation of a novel site, Ser155. Biochem. J. 349(Pt 2):547–557; 2000.
28. Malliaras, K.; Marbán, E. Cardiac cell therapy: Where we’ve been, where we are, and where we should be headed. Br. Med. Bull. 98:161–185; 2011.
29. Malliaras, K.; Zhang, Y.; Seinfeld, J.; Galang, G.; Tseliou, E.; Cheng, K.; Sun, B.; Aminzadeh, M.; Marbán, E. Cardiomyocyte proliferation and progenitor cell recruitment underlie therapeutic regeneration after myocardial infarction in the adult mouse heart. EMBO Mol. Med. 5(2):191–209; 2013.
30. Mao, Q.; Lin, C. X.; Liang, X. L.; Gao, J. S.; Xu, B. Mesenchymal stem cells overexpressing integrin-linked kinase attenuate cardiac fibroblast proliferation and collagen synthesis through paracrine actions. Mol. Med. Rep. 7(5):1617–1623; 2013.
31. Menasche, P. Cardiac cell therapy: Lessons from clinical trials. J. Mol. Cell. Cardiol. 50(2):258–265; 2011.
32. Mendez-Ferrer, S.; Michurina, T. V.; Ferraro, F.; Mazloom, A. R.; Macarthur, B. D.; Lira, S. A.; Scadden, D. T.; Ma’ayan, A.; Enikolopov, G. N.; Frenette, P. S. Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 466(7308):829–834; 2010.
33. Menna, C.; De Falco, E.; Pacini, L.; Scafetta, G.; Ruggieri, P.; Puca, R.; Petrozza, V.; Ciccone, A. M.; Rendina, E. A.; Calogero, A.; Ibrahim, M. Axitinib affects cell viability and migration of a primary foetal lung adenocarcinoma culture. Cancer. Invest. 32(1):13–21; 2014.
34. Metzele, R.; Alt, C.; Bai, X.; Yan, Y.; Zhang, Z.; Pan, Z.; Coleman, M.; Vykoukal, J.; Song, Y. H.; Alt, E. Human adipose tissue-derived stem cells exhibit proliferation potential and spontaneous rhythmic contraction after fusion with neonatal rat cardiomyocytes. FASEB J. 25(3):830–839; 2011.
35. Mirotsou, M.; Jayawardena, T. M.; Schmeckpeper, J.; Gnecchi, M.; Dzau, V. J. Paracrine mechanisms of stem cell reparative and regenerative actions in the heart. J. Mol. Cell Cardiol. 50(2):280–289; 2011.
36. Miyahara, Y.; Nagaya, N.; Kataoka, M.; Yanagawa, B.; Tanaka, K.; Hao, H.; Ishino, K.; Ishida, H.; Shimizu, T.; Kangawa, K.; Sano, S.; Okano, T.; Kitamura, S.; Mori, H. Monolayered mesenchymal stem cells repair scarred myocardium after myocardial infarction. Nat. Med. 12(4):459–465; 2006.
37. Moore, K. A.; Lemischka, I. R. Stem cells and their niches. Science 311(5769):1880–1885; 2006.
38. Mureli, S.; Gans, C. P.; Bare, D. J.; Geenen, D. L.; Kumar, N. M.; Banach, K. Mesenchymal stem cells improve cardiac conduction by upregulation of connexin 43 through paracrine signaling. Am. J. Physiol. Heart Circ. Physiol. 304(4):H600–609; 2013.
39. Murry, C. E.; Jennings, R. B.; Reimer, K. A. Preconditioning with ischemia: A delay of lethal cell injury in ischemic myocardium. Circulation 74(5):1124–1136; 1986.
40. Noiseux, N.; Gnecchi, M.; Lopez-Ilasaca, M.; Zhang, L.; Solomon, S. D.; Deb, A.; Dzau, V. J.; Pratt, R. E. Mesenchymal stem cells overexpressing Akt dramatically repair infarcted myocardium and improve cardiac function despite infrequent cellular fusion or differentiation. Mol. Ther. 14(6):840–850; 2006.
41. Patel, A. N.; Yockman, J.; Vargas, V.; Bull, D. A. Putative population of adipose-derived stem cells isolated from mediastinal tissue during cardiac surgery. Cell Transplant. 22(3):507–511; 2013.
42. Planat-Bénard, V.; Menard, C.; André, M.; Puceat, M.; Perez, A.; Garcia-Verdugo, J. M.; Pénicaud, L.; Casteilla, L. Spontaneous cardiomyocyte differentiation from adipose tissue stroma cells. Circ. Res. 94(2):223–229; 2004.
43. Ramesh, B.; Bishi, D. K.; Rallapalli, S.; Arumugam, S.; Cherian, K. M.; Guhathakurta, S. Ischemic cardiac tissue conditioned media induced differentiation of human mesenchymal stem cells into early stage cardiomyocytes. Cytotechnology 64(5):563–575; 2012.
44. Rangappa, S.; Fen, C.; Lee, E. H.; Bongso, A.; Sim, E. K.; Wei, E. K. Transformation of adult mesenchymal stem cells isolated from the fatty tissue into cardiomyocytes. Ann. Thorac. Surg. 75(3):775–779; 2003.
45. Scafetta, G.; Tricoli, E.; Siciliano, C.; Napoletano, C.; Puca, R.; Vingolo, E. M.; Cavallaro, G.; Polistena, A.; Frati, G.; De Falco, E. Suitability of human Tenon’s fibroblasts as feeder cells for culturing human limbal epithelial stem cells. Stem Cell Rev. 9(6):847–857; 2013.
46. Schäffler, A.; Büchler, C. Concise review: Adipose tissuederived stromal cells--Basic and clinical implications for novel cell-based therapies. Stem Cells 25(4):818–827; 2007.
47. Siciliano, C.; Ibrahim, M.; Scafetta, G.; Napoletano, C.; Mangino, G.; Pierelli, L.; Frati, G.; De Falco, E. Optimization of the isolation and expansion method of human mediastinaladipose tissue derived mesenchymal stem cells with virally inactivated GMP-grade platelet lysate. Cytotechnology 67 (1):154–174; 2015.
48. Song, Y. H.; Gehmert, S.; Sadat, S.; Pinkernell, K.; Bai, X.; Matthias, N.; Alt, E. VEGF is critical for spontaneous differentiation of stem cells into cardiomyocytes. Biochem. Biophys. Res. Commun. 354(4):999–1003; 2007.
49. Stastna, M.; Chimenti, I.; Marbán, E.; Van Eyk, J. E. Identification and functionality of proteomes secreted by rat cardiac stem cells and neonatal cardiomyocytes. Proteomics 10(2):245–253; 2010.
50. Strem, B. M.; Hicok, K. C.; Zhu, M.; Wulur, I.; Alfonso, Z.; Schreiber, R. E.; Fraser, J. K.; Hedrick, M. H. Multipotential differentiation of adipose tissue-derived stem cells. Keio J. Med. 54(3):132–141; 2005.
51. Strem, B. M.; Zhu, M.; Alfonso, Z.; Daniels, E. J.; Schreiber, R.; Beygui, R.; Begyui, R.; MacLellan, W. R.; Maclellan, W. R.; Hedrick, M. H.; Fraser, J. K. Expression of cardiomyocytic markers on adipose tissue-derived cells in a murine model of acute myocardial injury. Cytotherapy 7(3):282–291; 2005.
52. Supokawej, A.; Kheolamai, P.; Nartprayut, K.; U-Pratya, Y.; Manochantr, S.; Chayosumrit, M.; Issaragrisil, S. Cardiogenic and myogenic gene expression in mesenchymal stem cells after 5-azacytidine treatment. Turk. J. Haematol. 30(2):115–121; 2013.
53. Tan, S. C.; Carr, C. A.; Yeoh, K. K.; Schofield, C. J.; Davies, K. E.; Clarke, K. Identification of valid housekeeping genes for quantitative RT-PCR analysis of cardiosphere-derived cells preconditioned under hypoxia or with prolyl-4-hydroxylase inhibitors. Mol. Biol. Rep. 39(4):4857–4867; 2012.
54. Timmers, L.; Lim, S. K.; Hoefer, I. E.; Arslan, F.; Lai, R. C.; van Oorschot, A. A.; Goumans, M. J.; Strijder, C.; Sze, S. K.; Choo, A.; Piek, J. J.; Doevendans, P. A.; Pasterkamp, G.; de Kleijn, D. P. Human mesenchymal stem cell-conditioned medium improves cardiac function following myocardial infarction. Stem Cell Res. 6(3):206–214; 2011.
55. Wan Safwani, W. K.; Makpol, S.; Sathapan, S.; Chua, K. H. 5-Azacytidine is insufficient for cardiogenesis in human adipose-derived stem cells. J. Negat. Results Biomed. 11:3; 2012.
56. Williams, A. R.; Hatzistergos, K. E.; Addicott, B.; McCall, F.; Carvalho, D.; Suncion, V.; Morales, A. R.; Da Silva, J.; Sussman, M. A.; Heldman, A. W; Hare, J. M. Enhanced effect of combining human cardiac stem cells and bone marrow mesenchymal stem cells to reduce infarct size and to restore cardiac function after myocardial infarction. Circulation 127(2):213–223; 2013.
57. Yamada, Y.; Wang, X. D.; Yokoyama, S.; Fukuda, N.; Takakura, N. Cardiac progenitor cells in brown adipose tissue repaired damaged myocardium. Biochem. Biophys. Res. Commun. 342(2):662–670; 2006.