Atorvastatin improves survival of implanted stem cells in a rat model of renal ischemia-reperfusion injury

American Journal of Nephrology

Volumn 39, Issue 6, 2014, Pages 466-475

  Cai, Jieru ^a   Yu, Xiaofang ^a   Zhang, Bingying ^a   Zhang, Hui ^a   Fang, Yi ^a   Liu, Shaopeng ^a   Liu, Tongqiang ^a   Ding, Xiaoqiang ^a  

^a FUDAN UNIVERSITY   (China)

Author keywords

Atorvastatin; Inflammation; Mesenchymal stem cells; Renal ischemia reperfusion injury

Indexed keywords

ATORVASTATIN; CREATININE; TOLL LIKE RECEPTOR 4; HBP1 PROTEIN, RAT; HEPTANOIC ACID DERIVATIVE; HIGH MOBILITY GROUP B1 PROTEIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; PYRROLE DERIVATIVE; TLR4 PROTEIN, RAT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; CREATININE BLOOD LEVEL; DISEASE SEVERITY; INFLAMMATION; INNATE IMMUNITY; KIDNEY FUNCTION; KIDNEY ISCHEMIA; KIDNEY STRUCTURE; KIDNEY TUBULE CELL; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; THERAPY EFFECT; UREA NITROGEN BLOOD LEVEL; ACUTE KIDNEY FAILURE; ANIMAL; DRUG EFFECTS; GRAFT SURVIVAL; KIDNEY; MESENCHYMAL STROMA CELL; METABOLISM; REPERFUSION INJURY; VASCULARIZATION; ANIMAL TISSUE; DRUG MECHANISM; PROTEIN EXPRESSION;

ACUTE KIDNEY INJURY; ANIMALS; GRAFT SURVIVAL; HEPTANOIC ACIDS; HMGB1 PROTEIN; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; IMMUNITY, INNATE; INFLAMMATION; KIDNEY; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; OXIDATIVE STRESS; PYRROLES; RATS; REPERFUSION INJURY; TOLL-LIKE RECEPTOR 4;

EID: 84900893887     PISSN: 02508095     EISSN: 14219670     Source Type: Journal    
DOI: 10.1159/000362623     Document Type: Article

References (42)

1. Thadhani R, Pascual M, Bonventre JV: Acute renal failure. N Engl J Med 1996; 334: 1448-1460. (Pubitemid 126590563)
2. Fang Y, Ding X, Zhong Y, Zou J, Teng J, Tang Y, Lin J, Lin P: Acute kidney injury in a Chinese hospitalized population. Blood Purif 2010; 30: 120-126.
3. Devarajan P: Update on mechanisms of ischemic acute kidney injury. J Am Soc Nephrol 2006; 17: 1503-1520. (Pubitemid 43841396)
4. Lin F: Stem cells in kidney regeneration following acute renal injury. Pediatr Res 2006; 59: 74R-78R. (Pubitemid 43740039)
5. Herrera MB, Bussolati B, Bruno S, Fonsato V, Romanazzi GM, Camussi G: Mesenchymal stem cells contribute to the renal repair of acute tubular epithelial injury. Int J Mol Med 2004; 14: 1035-1041.
6. Morigi M, Imberti B, Zoja C, Corna D, Tomasoni S, Abbate M, Rottoli D, Angioletti S, Benigni A, Perico N, Alison M, Remuzzi G: 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. (Pubitemid 38822058)
7. Duffield JS, Park KM, Hsiao LL, Kelley VR, Scadden DT, Ichimura T, Bonventre JV: Restoration of tubular epithelial cells during repair of the postischemic kidney occurs independently of bone marrow-derived stem cells. J Clin Invest 2005; 115: 1743-1755. (Pubitemid 40979713)
8. Lange C, Togel F, Ittrich H, Clayton F, Nolte- Ernsting C, Zander AR, Westenfelder C: Administered mesenchymal stem cells enhance recovery from ischemia/reperfusion-induced acute renal failure in rats. Kidney Int 2005; 68: 1613-1617. (Pubitemid 43169906)
9. Burst VR, Gillis M, Putsch F, Herzog R, Fischer JH, Heid P, Muller-Ehmsen J, Schenk K, Fries JWU, Baldamus CA, Benzing T: Poor cell survival limits the beneficial impact of mesenchymal stem cell transplantation on acute kidney injury. Nephron Exp Nephrol 2010; 114:E107-E116.
10. Togel F, Hu ZM, Weiss K, Isaac J, Lange C, Westenfelder C: Administered mesenchymal stem cells protect against ischemic acute renal failure through differentiation-independent mechanisms. Am J Physiol Renal Physiol 2005; 289:F31-F42. (Pubitemid 40863570)
11. Togel F, Yang Y, Zhang P, Hu ZM, Westenfelder C: Bioluminescence imaging to monitor the in vivo distribution of administered mesenchymal stem cells in acute kidney injury. Am J Physiol Renal Physiol 2008; 295:F315-F321.
12. Chen YT, Sun CK, Lin YC, Chang LT, Chen YL, Tsai TH, Chung SY, Chua S, Kao YH, Yen CH, Shao PL, Chang KC, Leu S, Yip HK: Adipose- derived mesenchymal stem cell protects kidneys against ischemia-reperfusion injury through suppressing oxidative stress and inflammatory reaction. J Transl Med 2011; 9: 51.
13. Yang YJ, Qian HY, Huang J, Geng YJ, Gao RL, Dou KF, Yang GS, Li JJ, Shen R, He ZX, Lu MJ, Zhao SH: Atorvastatin treatment improves survival and effects of implanted mesenchymal stem cells in post-infarct swine hearts. Eur Heart J 2008; 29: 1578-1590. (Pubitemid 351881977)
14. Zhang YQ, Zhang RS, Li Y, He GP, Zhang DG, Zhang FM: Simvastatin augments the efficacy of therapeutic angiogenesis induced by bone marrow-derived mesenchymal stem cells in a murine model of hindlimb ischemia. Mol Biol Rep 2012; 39: 285-293.
15. Joyce M, Kelly C, Winter D, Chen G, Leahy A, Bouchier-Hayes D: Pravastatin, a 3-hydroxy- 3-methylglutaryl coenzyme a reductase inhibitor, attenuates renal injury in an experimental model of ischemia-reperfusion. J Surg Res 2001; 101: 79-84. (Pubitemid 33030111)
16. Gueler F, Rong S, Park JK, Fiebeler A, Menne J, Elger M, Mueller DN, Hampich F, Dechend R, Kunter U, Luft FC, Haller H: Postischemic acute renal failure is reduced by short-term statin treatment in a rat model. J Am Soc Nephrol 2002; 13: 2288-2298. (Pubitemid 34925239)
17. Gueler F, Park JK, Rong S, Kirsch T, Lindschau C, Zheng W, Elger M, Fiebeler A, Fliser D, Luft FC, Haller H: Statins attenuate ischemia- reperfusion injury by inducing heme oxygenase-1 in infiltrating macrophages. Am J Pathol 2007; 170: 1192-1199. (Pubitemid 47339327)
18. Gottmann U, Brinkkoetter PT, Hoeger S, Gutermann K, Coutinho ZM, Ruf T, Hui S, Liu ZZ, Schnuelle P, van der Woude FJ, Braun C: Atorvastatin donor pretreatment prevents ischemia/reperfusion injury in renal transplantation in rats: possible role for aldose-reductase inhibition. Transplantation 2007; 84: 755-762. (Pubitemid 47480661)
19. Qu Z, Xu H, Tian Y, Jiang X: Atorvastatin improves microenvironment to enhance the beneficial effects of BMSCS therapy in a rabbit model of acute myocardial infarction. Cell Physiol Biochem 2013; 32: 380-389.
20. Song L, Yang YJ, Dong QT, Qian HY, Gao RL, Qiao SB, Shen R, He ZX, Lu MJ, Zhao SH, Geng YJ, Gersh BJ: Atorvastatin enhance efficacy of mesenchymal stem cells treatment for swine myocardial infarction via activation of nitric oxide synthase. PLoS One 2013; 8:e65702.
21. Yu X, Lu C, Liu H, Rao S, Cai J, Liu S, Kriegel AJ, Greene AS, Liang M, Ding X: Hypoxic preconditioning with cobalt of bone marrow mesenchymal stem cells improves cell migration and enhances therapy for treatment of ischemic acute kidney injury. PLoS One 2013; 8:e62703.
22. Haylor JL, Harris KP, Nicholson ML, Waller HL, Huang Q, Yang B: Atorvastatin improving renal ischemia reperfusion injury via direct inhibition of active caspase-3 in rats. Exp Biol Med (Maywood) 2011; 236: 755-763.
23. Allam R, Scherbaum CR, Darisipudi MN, Mulay SR, Hagele H, Lichtnekert J, Hagemann JH, Rupanagudi KV, Ryu M, Schwarzenberger C, Hohenstein B, Hugo C, Uhl B, Reichel CA, Krombach F, Monestier M, Liapis H, Moreth K, Schaefer L, Anders HJ: Histones from dying renal cells aggravate kidney injury via TLR2 and TLR4. J Am Soc Nephrol 2012; 23: 1375-1388.
24. Tian HB, Lu Y, Shah SP, Wang QS, Hong S: 14S,21R-dihydroxy- docosahexaenoic acid treatment enhances mesenchymal stem cell amelioration of renal ischemia/reperfusion injury. Stem Cells Dev 2012; 21: 1187-1199.
25. Yuan L, Wu MJ, Sun HY, Xiong J, Zhang Y, Liu CY, Fu LL, Liu DM, Liu HQ, Mei CL: VEGF-modified human embryonic mesenchymal stem cell implantation enhances protection against cisplatin-induced acute kidney injury. Am J Physiol Renal Physiol 2011; 300:F207-F218.
26. Eliopoulos N, Zhao J, Forner K, Birman E, Young YK, Bouchentouf M: Erythropoietin gene-enhanced marrow mesenchymal stromal cells decrease cisplatin-induced kidney injury and improve survival of allogeneic mice. Mol Ther 2011; 19: 2072-2083.
27. Cantoni S, Cavallini C, Bianchi F, Bonavita F, Vaccari V, Olivi E, Frascari I, Tassinari R, Valente S, Lionetti V, Ventura C: Rosuvastatin elicits kdr-dependent vasculogenic response of human placental stem cells through PI3K/ AKT pathway. Pharmacol Res 2012; 65: 275-284.
28. Jahromi GP, Seidi S, Sadr SS, Shabanzadeh AP, Keshavarz M, Kaka GR, Hosseini SK, Sohanaki H, Charish J: Therapeutic effects of a combinatorial treatment of simvastatin and bone marrow stromal cells on experimental embolic stroke. Basic Clin Pharmacol Toxicol 2012; 110: 487-493.
29. Mottaghi S, Larijani B, Sharifi AM: Atorvastatin: an efficient step forward in mesenchymal stem cell therapy of diabetic retinopathy. Cytotherapy 2013; 15: 263-266.
30. Song L, Yang YJ, Dong QT, Qian HY, Xu H, Meng XM, Tang Y: Atorvastatin protects swine bone marrow mesenchymal stem cells from apoptosis through AMPK but not PI3K/ AKT pathway. Zhonghua Xin Xue Guan Bing Za Zhi 2011; 39: 1033-1038.
31. Todorovic Z, Nesic Z, Stojanovic R, Basta-Jovanovic G, Radojevic-Skodric S, Velickovic R, Chatterjee PK, Thiemermann C, Prostran M: Acute protective effects of simvastatin in the rat model of renal ischemia-reperfusion injury: it is never too late for the pretreatment. J Pharmacol Sci 2008; 107: 465-470.
32. Nesic Z, Todorovic Z, Stojanovic R, Basta-Jovanovic G, Radojevic-Skodric S, Velickovic R, Chatterjee PK, Thiemermann C, Prostran M: Single-dose intravenous simvastatin treatment attenuates renal injury in an experimental model of ischemia-reperfusion in the rat. J Pharmacol Sci 2006; 102: 413-417. (Pubitemid 44954601)
33. Eltzschig HK, Eckle T: Ischemia and reperfusion-from mechanism to translation. Nat Med 2011; 17: 1391-1401.
34. Mkaddem SB, Bens M, Vandewalle A: Differential activation of Toll-like receptor-mediated apoptosis induced by hypoxia. Oncotarget 2010; 1: 741-750.
35. Klune JR, Tsung A: Molecular biology of liver ischemia/reperfusion injury: established mechanisms and recent advancements. Surg Clin North Am 2010; 90: 665-677.
36. Wang L, Zhang X, Liu L, Yang R, Cui L, Li M: Atorvastatin protects rat brains against permanent focal ischemia and downregulates HMGB1, HMGB1 receptors (RAGE and TLR4), NF-κB expression. Neurosci Lett 2010; 471: 152-156.
37. Ajamieh H, Farrell G, Wong HJ, Yu J, Chu E, Chen J, Teoh N: Atorvastatin protects obese mice against hepatic ischemia-reperfusion injury by Toll-like receptor-4 suppression and endothelial nitric oxide synthase activation. J Gastroenterol Hepatol 2012; 27: 1353-1361.
38. Calisto KL, Carvalho Bde M, Ropelle ER, Mittestainer FC, Camacho AC, Guadagnini D, Carvalheira JB, Saad MJ: Atorvastatin improves survival in septic rats: effect on tissue inflammatory pathway and on insulin signaling. PLoS One 2010; 5:e14232.
39. Zhang Q, Yang YJ, Wang H, Dong QT, Wang TJ, Qian HY, Xu H: Autophagy activation: a novel mechanism of atorvastatin to protect mesenchymal stem cells from hypoxia and serum deprivation via AMP-activated protein kinase/mammalian target of rapamycin pathway. Stem Cells Dev 2012; 21: 1321-1332.
40. Mias C, Trouche E, Seguelas MH, Calcagno F, Dignat-George F, Sabatier F, Piercecchi-Marti MD, Daniel L, Bianchi P, Calise D, Bourin P, Parini A, Cussac D: Ex vivo pretreatment with melatonin improves survival, proangiogenic/ mitogenic activity, and efficiency of mesenchymal stem cells injected into ischemic kidney. Stem Cells 2008; 26: 1749-1757.
41. Qian H, Yang H, Xu W, Yan Y, Chen Q, Zhu W, Cao H, Yin Q, Zhou H, Mao F, Chen Y: Bone marrow mesenchymal stem cells ameliorate rat acute renal failure by differentiation into renal tubular epithelial-like cells. Int J Mol Med 2008; 22: 325-332.
42. Humphreys BD, Bonventre JV: Mesenchymal stem cells in acute kidney injury. Annu Rev Med 2008; 59: 311-325. (Pubitemid 351287940)