Ex vivo pretreatment with melatonin improves survival, proangiogenic/ mitogenic activity, and efficiency of mesenchymal stem cells injected into ischemic kidney

Stem Cells

Volumn 26, Issue 7, 2008, Pages 1749-1757

  Mias, Céline ^a   Trouche, Elodie ^a   Seguelas, Marie Hélène ^a   Calcagno, Fabien ^c   Dignat George, Françoise ^c   Sabatier, Florence ^c   Piercecchi Marti, Marie Dominique ^c   Daniel, Laurent ^d   Bianchi, Pascale ^a   Calise, Denis ^a   Bourin, Philippe ^e   Parini, Angelo ^a,b,f   Cussac, Daniel ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ DE TOULOUSE   (France)

^c CNRS   (France)

^d AIX MARSEILLE UNIVERSITY   (France)

^e ETABLISSEMENT FRANÇAIS DU SANG   (France)

^f CHU RANGUEIL   (France)

Author keywords

Angiogenesis; Melatonin; Mesenchymal stem cell; Survival; Therapeutic efficacy

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR; CATALASE; COPPER ZINC SUPEROXIDE DISMUTASE; HYDROGEN PEROXIDE; MELATONIN; SCATTER FACTOR;

ANGIOGENESIS; ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CULTURE; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; ENDOTHELIUM CELL; IN VIVO STUDY; KIDNEY FUNCTION; KIDNEY ISCHEMIA; MESENCHYMAL STEM CELL; MITOGENESIS; NONHUMAN; PROTEIN EXPRESSION; RAT;

ANIMALS; BONE MARROW CELLS; CELL PROLIFERATION; CELL SURVIVAL; FIBROBLAST GROWTH FACTOR 2; HEPATOCYTE GROWTH FACTOR; HUMANS; ISCHEMIA; KIDNEY; MELATONIN; MESENCHYMAL STEM CELLS; NEOVASCULARIZATION, PATHOLOGIC; RATS; RATS, INBRED LEW; REPERFUSION INJURY;

RATTUS;

EID: 55049135589     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1634/stemcells.2007-1000     Document Type: Article

References (44)

1. Beyer Nardi N, da Silva Meirelles L. Mesenchymal stem cells: Isolation, in vitro expansion and characterization. Handb Exp Pharmacol 2006:249-282.
2. Jiang Y, Jahagirdar BN, Reinhardt RL et al. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 2002;418:41-49.
3. Kassem M, Kristiansen M, Abdallah BM. Mesenchymal stem cells: Cell biology and potential use in therapy. Basic Clin Pharmacol Toxicol 2004;95:209-214.
4. Pittenger MF, Mackay AM, Beck SC et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999;284:143-147.
5. Morigi M, Imberti B, Zoja C et al. Mesenchymal stem cells are renotropic, helping to repair the kidney and improve function in acute renal failure. J Am Soc Nephrol 2004;15:1794-1804.
6. Kunter U, Rong S, Djuric Z et al. Transplanted mesenchymal stem cells accelerate glomerular healing in experimental glomerulonephritis. J Am Soc Nephrol 2006;17:2202-2212.
7. Tang J, Xie Q, Pan G et al. Mesenchymal stem cells participate in angiogenesis and improve heart function in rat model of myocardial ischemia with reperfusion. Eur J Cardiothorac Surg 2006;30:353-361.
8. Tögel F, Weiss K, Yang Y et al. Vasculotropic, paracrine actions of infused mesenchymal stem cells are important to the recovery from acute kidney injury. Am J Physiol Renal Physiol 2007;292:F1626-F1635.
9. Wu Y, Chen L, Scott PG et al. Mesenchymal stem cells enhance wound healing through differentiation and angiogenesis. STEM CELLS 2007;25:2648-2659.
10. Maurel A, Azarnoush K, Sabbah L et al. Can cold or heat shock improve skeletal myoblast engraftment in infarcted myocardium? Transplantation 2005;80:660-665.
11. Müller-Ehmsen J, Whittaker P, Kloner RA et al. Survival and development of neonatal rat cardiomyocytes transplanted into adult myocardium. J Mol Cell Cardiol 2002;34:107-116.
12. Reinecke H, Zhang M, Bartosek T et al. Survival, integration, and differentiation of cardiomyocyte grafts: A study in normal and injured rat hearts. Circulation 1999;100:193-202.
13. Tambara K, Sakakibara Y, Sakaguchi G et al. Transplanted skeletal myoblasts can fully replace the infarcted myocardium when they survive in the host in large numbers. Circulation 2003;108(suppl 1):II259-II263.
14. Toma C, Pittenger MF, Cahill KS et al. Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation 2002;105:93-98.
15. Niagara MI, Haider H, Jiang S et al. Pharmacologically preconditioned skeletal myoblasts are resistant to oxidative stress and promote angiomyogenesis via release of paracrine factors in the infarcted heart. Circ Res 2007;100:545-555.
16. Qu Z, Balkir L, van Deutekom JC et al. Development of approaches to improve cell survival in myoblast transfer therapy. J Cell Biol 1998;142:1257-1267.
17. Suzuki K, Murtuza B, Beauchamp JR et al. Dynamics and mediators of acute graft attrition after myoblast transplantation to the heart. FASEB J 2004;18:1153-1155.
18. Suzuki K, Smolenski RT, Jayakumar J et al. Heat shock treatment enhances graft cell survival in skeletal myoblast transplantation to the heart. Circulation 2000;102:III216-III221.
19. Tang YL, Tang Y, Zhang YC et al. Improved graft mesenchymal stem cell survival in ischemic heart with a hypoxia-regulated heme oxygenase-1 vector. J Am Coll Cardiol 2005;46:1339-1350.
20. Vanecek J. Cellular mechanisms of melatonin action. Physiol Rev 1998;78:687-721.
21. Cardinali DP, Brusco LI, Lloret SP et al. Melatonin in sleep disorders and jet-lag. Neuro Endocrinol Lett 2002;23(suppl 1):9-13.
22. Pévet P. Melatonin and biological rhythms. Biol Signals Recept 2000;9:203-212.
23. Skwarlo-Sonta K. Melatonin in immunity: Comparative aspects. Neuro Endocrinol Lett 2002;23(suppl 1):61-66.
24. Garcia-Mauriño S, Gonzalez-Haba MG, Calvo JR et al. Melatonin enhances IL-2, IL-6, and IFN-gamma production by human circulating CD4+ cells: A possible nuclear receptor-mediated mechanism Involving T helper type 1 lymphocytes and monocytes. J Immunol 1997;159:574-581.
25. Reiter RJ, Tan DX, Gitto E et al. Pharmacological utility of melatonin in reducing oxidative cellular and molecular damage. Pol J Pharmacol 2004;56:159-170.
26. Reiter RJ, Tan DX, Mayo JC et al. Melatonin as an antioxidant: Biochemical mechanisms and pathophysiological implications in humans. Acta Biochim Pol 2003;50:1129-1146.
27. Reiter RJ, Tan DX, Osuna C et al. Actions of melatonin in the reduction of oxidative stress. A review. J Biomed Sci 2000;7:444-458.
28. Bandyopadhyay D, Chattopadhyay A. Reactive oxygen species-induced gastric ulceration: Protection by melatonin. Curr Med Chem 2006;13:1187-1202.
29. Welin AK, Svedin P, Lapatto R et al. Melatonin reduces inflammation and cell death in white matter in the mid-gestation fetal sheep following umbilical cord occlusion. Pediatr Res 2007;61:153-158.
30. Vinay P, Gougoux A, Lemieux G. Isolation of a pure suspension of rat proximal tubules. Am J Physiol 1981;241:F403-F411.
31. Basire A, Sabatier F, Ravet S et al. High urokinase expression contributes to the angiogenic properties of endothelial cells derived from circulating progenitors. Thromb Haemost 2006;95:678-688.
32. Muller-Borer BJ, Collins MC, Gunst PR et al. Quantum dot labeling of mesenchymal stem cells. J Nanobiotechnology 2007;5:9.
33. Rosen AB, Kelly DJ, Schuldt AJ et al. Finding fluorescent needles in the cardiac haystack: Tracking human mesenchymal stem cells labeled with quantum dots for quantitative in vivo three-dimensional fluorescence analysis. STEM CELLS 2007;25:2128-2138.
34. Conget PA, Minguell JJ. Phenotypical and functional properties of human bone marrow mesenchymal progenitor cells. J Cell Physiol 1999;181:67-73.
35. Hardeland R. Antioxidative protection by melatonin: Multiplicity of mechanisms from radical detoxification to radical avoidance. Endocrine 2005;27:119-130.
36. Kunduzova OR, Escourrou G, Seguelas MH et al. Prevention of apoptotic and necrotic cell death, caspase-3 activation, and renal dysfunction by melatonin after ischemia/reperfusion. FASEB J 2003;17:872-874.
37. Lagneux C, Joyeux M, Demenge P et al. Protective effects of melatonin against ischemia-reperfusion injury in the isolated rat heart. Life Sci 2000;66:503-509.
38. Efthimiadou A, Lambropoulou M, Pagonopoulou O et al. The role of basic-fibroblast growth factor (b-FGF) in cyclosporine-induced nephrotoxicity. In Vivo 2006;20:265-269.
39. Ryan JM, Barry FP, Murphy JM et al. Mesenchymal stem cells avoid allogeneic rejection. J Inflamm (Lond) 2005;2:8.
40. Xin X, Yang S, Ingle G et al. Hepatocyte growth factor enhances vascular endothelial growth factor-induced angiogenesis in vitro and in vivo. Am J Pathol 2001;158:1111-1120.
41. Dzau VJ, Gnecchi M, Pachori AS. Enhancing stem cell therapy through genetic modification. J Am Coll Cardiol 2005;46:1351-1353.
42. Gnecchi M, He H, Liang OD et al. Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells. Nat Med 2005;11:367-368.
43. Gnecchi M, He H, Noiseux N et al. Evidence supporting paracrine hypothesis for Akt-modified mesenchymal stem cell-mediated cardiac protection and functional improvement. FASEB J 2006;20:661-669.
44. Mangi AA, Noiseux N, Kong D et al. Mesenchymal stem cells modified with Akt prevent remodeling and restore performance of infarcted hearts. Nat Med 2003;9:1195-1201.