Preconditioning of bone marrow mesenchymal stem cells by prolyl hydroxylase inhibition enhances cell survival and angiogenesis in vitro and after transplantation into the ischemic heart of rats

Stem Cell Research and Therapy

Volumn 5, Issue 5, 2014, Pages

  Liu, Xian Bao ^a,b   Wang, Jian An ^a   Ji, Xiao Ya ^b   Yu, Shan Ping ^b   Wei, Ling ^b  

^a ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENIC PROTEIN; DIMETHYLOXALYLGLYCINE; GLUCOSE TRANSPORTER 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; PROLYL HYDROXYLASE INHIBITOR; PROTEIN KINASE B; UNCLASSIFIED DRUG; VASCULOTROPIN; DICARBOXYLIC AMINO ACID; OXALYLGLYCINE;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW DERIVED MESENCHYMAL STEM CELL; CELL DEATH; CELL PROTECTION; CELL SURVIVAL; CELL TRANSDIFFERENTIATION; CELL VIABILITY; CONTROLLED STUDY; ENZYME INHIBITION; HEART FUNCTION; HEART INFARCTION; HEART INFARCTION SIZE; HEART LEFT VENTRICLE EJECTION FRACTION; HEART LEFT VENTRICLE ENDDIASTOLIC VOLUME; HEART LEFT VENTRICLE ENDSYSTOLIC VOLUME; HEART MUSCLE ISCHEMIA; IN VITRO STUDY; IN VIVO STUDY; MESENCHYMAL STEM CELL TRANSPLANTATION; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; PROCEDURES CONCERNING CELLS; PROTEIN EXPRESSION; RAT; STEM CELL HYPOXIA PRECONDITIONING; THERAPY EFFECT; TRANSTHORACIC ECHOCARDIOGRAPHY; TREATMENT DURATION; UPREGULATION; ANIMAL; BONE MARROW TRANSPLANTATION; CELL DIFFERENTIATION; CYTOLOGY; DRUG EFFECTS; ECHOCARDIOGRAPHY; MESENCHYMAL STROMA CELL; MYOCARDIAL INFARCTION; PATHOLOGY; PROCEDURES; RANDOMIZATION; TRANSGENIC RAT; TRANSPLANTATION CONDITIONING;

RATTUS;

AMINO ACIDS, DICARBOXYLIC; ANIMALS; BONE MARROW TRANSPLANTATION; CELL DIFFERENTIATION; CELL SURVIVAL; ECHOCARDIOGRAPHY; IN VITRO TECHNIQUES; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MYOCARDIAL INFARCTION; NEOVASCULARIZATION, PHYSIOLOGIC; PROLYL-HYDROXYLASE INHIBITORS; RANDOM ALLOCATION; RATS; RATS, TRANSGENIC; TRANSPLANTATION CONDITIONING;

EID: 84934901905     PISSN: None     EISSN: 17576512     Source Type: Journal    
DOI: 10.1186/scrt499     Document Type: Article

References (51)

1. Braunwald E, Bristow MR: Congestive heart failure: fifty years of progress. Circulation 2000, 102: IV14-IV23.
2. Williams AR, Hare JM: Mesenchymal stem cells: biology, pathophysiology, translational findings, and therapeutic implications for cardiac disease. Circulation Res 2011, 109: 923-940. 10.1161/CIRCRESAHA.111.243147
3. Tang YL, Tang Y, Zhang YC, Qian K, Shen L, Phillips MI: Improved graft mesenchymal stem cell survival in ischemic heart with a hypoxia-regulated heme oxygenase-1 vector. J Am College Cardiol 2005, 46: 1339-1350. 10.1016/j.jacc.2005.05.079
4. Bartunek J, Croissant JD, Wijns W, Gofflot S, de Lavareille A, Vanderheyden M, Kaluzhny Y, Mazouz N, Willemsen P, Penicka M, Mathieu M, Homsy C, De Bruyne B, McEntee K, Lee IW, Heyndrickx GR: Pretreatment of adult bone marrow mesenchymal stem cells with cardiomyogenic growth factors and repair of the chronically infarcted myocardium. Am J Physiol Heart Circ Physiol 2007, 292: H1095-H1104.
5. Behfar A, Yamada S, Crespo-Diaz R, Nesbitt JJ, Rowe LA, Perez-Terzic C, Gaussin V, Homsy C, Bartunek J, Terzic A: Guided cardiopoiesis enhances therapeutic benefit of bone marrow human mesenchymal stem cells in chronic myocardial infarction. J Am Coll Cardiol 2010, 56: 721-734. 10.1016/j.jacc.2010.03.066
6. McGinley LM, McMahon J, Stocca A, Duffy A, Flynn A, O'Toole D, O'Brien T: Mesenchymal stem cell survival in the infarcted heart is enhanced by lentivirus vector-mediated heat shock protein 27 expression. Human Gene Ther 2013, 24: 840-851. 10.1089/hum.2011.009
7. Wei L, Fraser JL, Lu ZY, Hu X, Yu SP: Transplantation of hypoxia preconditioned bone marrow mesenchymal stem cells enhances angiogenesis and neurogenesis after cerebral ischemia in rats. Neurobiol Dis 2012, 46: 635-645. 10.1016/j.nbd.2012.03.002
8. Wang L, Pasha Z, Wang S, Li N, Feng Y, Lu G, Millard RW, Ashraf M: Protein kinase G1 alpha overexpression increases stem cell survival and cardiac function after myocardial infarction. PLoS One 2013, 8: e60087. 10.1371/journal.pone.0060087
9. Kim SW, Lee DW, Yu LH, Zhang HZ, Kim CE, Kim JM, Park TH, Cha KS, Seo SY, Roh MS, Lee KC, Jung JS, Kim MH: Mesenchymal stem cells overexpressing GCP-2 improve heart function through enhanced angiogenic properties in a myocardial infarction model. Cardiovasc Res 2012, 95: 495-506. 10.1093/cvr/cvs224
10. Hu X, Yu SP, Fraser JL, Lu Z, Ogle ME, Wang JA, Wei L: Transplantation of hypoxia-preconditioned mesenchymal stem cells improves infarcted heart function via enhanced survival of implanted cells and angiogenesis. J Thorac Cardiovasc Surg 2008, 135: 799-808. 10.1016/j.jtcvs.2007.07.071
11. Kim HW, Haider HK, Jiang S, Ashraf M: Ischemic preconditioning augments survival of stem cells via miR-210 expression by targeting caspase-8-associated protein 2. J Biol Chem 2009, 284: 33161-33168. 10.1074/jbc.M109.020925
12. Chacko SM, Ahmed S, Selvendiran K, Kuppusamy ML, Khan M, Kuppusamy P: Hypoxic preconditioning induces the expression of prosurvival and proangiogenic markers in mesenchymal stem cells. Am J Physiol Cell Physiol 2010, 299: C1562-C1570. 10.1152/ajpcell.00221.2010
13. Jaussaud J, Biais M, Calderon J, Chevaleyre J, Duchez P, Ivanovic Z, Couffinhal T, Barandon L: Hypoxia-preconditioned mesenchymal stromal cells improve cardiac function in a swine model of chronic myocardial ischaemia. Eur J Cardiothorac Surg 2013, 43: 1050-1057. 10.1093/ejcts/ezs549
14. Tang YL, Zhu W, Cheng M, Chen L, Zhang J, Sun T, Kishore R, Phillips MI, Losordo DW, Qin G: Hypoxic preconditioning enhances the benefit of cardiac progenitor cell therapy for treatment of myocardial infarction by inducing CXCR4 expression. Circ Res 2009, 104: 1209-1216. 10.1161/CIRCRESAHA.109.197723
15. Francis KR, Wei L: Human embryonic stem cell neural differentiation and enhanced cell survival promoted by hypoxic preconditioning. Cell Death Dis 2011, 1: e22.
16. Hu X, Wei L, Taylor TM, Wei J, Zhou X, Wang JA, Yu SP: Hypoxic preconditioning enhances bone marrow mesenchymal stem cell migration via Kv2.1 channel and FAK activation. Am J Physiol Cell Physiol 2011, 301: C362-C372. 10.1152/ajpcell.00013.2010
17. Theus MH, Wei L, Cui L, Francis K, Hu X, Keogh C, Yu SP: In vitro hypoxic preconditioning of embryonic stem cells as a strategy of promoting cell survival and functional benefits after transplantation into the ischemic rat brain. Exp Neurol 2008, 210: 656-670. 10.1016/j.expneurol.2007.12.020
18. Wei N, Yu SP, Gu X, Taylor TM, Song D, Liu XF, Wei L: Delayed intranasal delivery of hypoxic-preconditioned bone marrow mesenchymal stem cells enhanced cell homing and therapeutic benefits after ischemic stroke in mice. Cell Transplant 2012, 22: 977-991.
19. Haider H, Ashraf M: Strategies to promote donor cell survival: combining preconditioning approach with stem cell transplantation. J Mol Cell Cardiol 2008, 45: 554-566. 10.1016/j.yjmcc.2008.05.004
20. Kohin S, Stary CM, Howlett RA, Hogan MC: Preconditioning improves function and recovery of single muscle fibers during severe hypoxia and reoxygenation. Am J Physiol Cell Physiol 2001, 281: C142-C146.
21. Yu SP, Wei Z, Wei L: Preconditioning strategy in stem cell transplantation therapy. Transl Stroke Res 2013, 4: 76-88. 10.1007/s12975-012-0251-0
22. Haider KH, Ashraf M: Preconditioning approach in stem cell therapy for the treatment of infarcted heart. Prog Mol Biol Transl Sci 2012, 111: 323-356.
23. Li SC, Acevedo J, Wang L, Jiang H, Luo J, Pestell RG, Loudon WG, Chang AC: Mechanisms for progenitor cell-mediated repair for ischemic heart injury. Curr Stem Cell Res Ther 2012, 7: 2-14. 10.2174/157488812798483449
24. Mottaghi S, Larijani B, Sharifi AM: Apelin 13: a novel approach to enhance efficacy of hypoxic preconditioned mesenchymal stem cells for cell therapy of diabetes. Med Hypotheses 2012, 79: 717-718. 10.1016/j.mehy.2012.08.007
25. Sakata H, Niizuma K, Wakai T, Narasimhan P, Maier CM, Chan PH: Neural stem cells genetically modified to overexpress cu/zn-superoxide dismutase enhance amelioration of ischemic stroke in mice. Stroke 2012, 43: 2423-2429. 10.1161/STROKEAHA.112.656900
26. Zeng X, Yu SP, Taylor T, Ogle M, Wei L: Protective effect of apelin on cultured rat bone marrow mesenchymal stem cells against apoptosis. Stem Cell Res 2012, 8: 357-367. 10.1016/j.scr.2011.12.004
27. Afzal MR, Haider H, Idris NM, Jiang S, Ahmed RP, Ashraf M: Preconditioning promotes survival and angiomyogenic potential of mesenchymal stem cells in the infarcted heart via NF-κB signaling. Antioxid Redox Signal 2009, 12: 693-702.
28. Niagara MI, Haider H, Jiang S, Ashraf M: 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. 10.1161/01.RES.0000258460.41160.ef
29. Nagy K, Kis B, Rajapakse NC, Bari F, Busija DW: Diazoxide preconditioning protects against neuronal cell death by attenuation of oxidative stress upon glutamate stimulation. J Neurosci Res 2004, 76: 697-704. 10.1002/jnr.20120
30. Bao W, Qin P, Needle S, Erickson-Miller CL, Duffy KJ, Ariazi JL, Zhao S, Olzinski AR, Behm DJ, Pipes GC, Jucker BM, Hu E, Lepore JJ, Willette RN: Chronic inhibition of hypoxia-inducible factor prolyl 4-hydroxylase improves ventricular performance, remodeling, and vascularity after myocardial infarction in the rat. J Cardiovasc Pharmacol 2010, 56: 147-155. 10.1097/FJC.0b013e3181e2bfef
31. Kim JW, Tchernyshyov I, Semenza GL, Dang CV: HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab 2006, 3: 177-185. 10.1016/j.cmet.2006.02.002
32. Iyer NV, Kotch LE, Agani F, Leung SW, Laughner E, Wenger RH, Gassmann M, Gearhart JD, Lawler AM, Yu AY, Semenza GL: Cellular and developmental control of O 2 homeostasis by hypoxia-inducible factor 1 alpha. Genes Dev 1998, 12: 149-162. 10.1101/gad.12.2.149
33. Lomb DJ, Straub JA, Freeman RS: Prolyl hydroxylase inhibitors delay neuronal cell death caused by trophic factor deprivation. J Neurochem 2007, 103: 1897-1906. 10.1111/j.1471-4159.2007.04873.x
34. Ogle ME, Gu X, Espinera AR, Wei L: Inhibition of prolyl hydroxylases by dimethyloxaloylglycine after stroke reduces ischemic brain injury and requires hypoxia inducible factor-1α. Neurobiol Dis 2011, 45: 733-742.
35. Rey S, Luo W, Shimoda LA, Semenza GL: Metabolic reprogramming by HIF-1 promotes the survival of bone marrow-derived angiogenic cells in ischemic tissue. Blood 2011, 117: 4988-4998. 10.1182/blood-2010-11-321190
36. Sasabe E, Tatemoto Y, Li D, Yamamoto T, Osaki T: Mechanism of HIF-1α -dependent suppression of hypoxia-induced apoptosis in squamous cell carcinoma cells. Cancer Sci 2005, 96: 394-402. 10.1111/j.1349-7006.2005.00065.x
37. Liu XB, Wang JA, Ogle ME, Wei L: Prolyl hydroxylase inhibitor dimethyloxalylglycine enhances mesenchymal stem cell survival. J Cell Biochem 2009, 106: 903-911. 10.1002/jcb.22064
38. Campagnoli C, Roberts IA, Kumar S, Bennett PR, Bellantuono I, Fisk NM: Identification of mesenchymal stem/progenitor cells in human first-trimester fetal blood, liver, and bone marrow. Blood 2001, 98: 2396-2402. 10.1182/blood.V98.8.2396
39. Cai H, Zhang Z, Yang GY: Preconditioned stem cells: a promising strategy for cell-based ischemic stroke therapy. Curr Drug Targets 2014, 15: 771-779. 10.2174/1389450115666140623120010
40. Min JY, Sandmann S, Meissner A, Unger T, Simon R: Differential effects of mibefradil, verapamil, and amlodipine on myocardial function and intracellular Ca(2+) handling in rats with chronic myocardial infarction. J Pharmacol Exp Ther 1999, 291: 1038-1044.
41. Misra MK, Sarwat M, Bhakuni P, Tuteja R, Tuteja N: Oxidative stress and ischemic myocardial syndromes. Med Sci Monit 2009, 15: RA209-RA219.
42. Leenen FH, Huang BS, Yu H, Yuan B: Brain 'ouabain' mediates sympathetic hyperactivity in congestive heart failure. Circ Res 1995, 77: 993-1000. 10.1161/01.RES.77.5.993
43. Ockaili R, Natarajan R, Salloum F, Fisher BJ, Jones D, Fowler AA 3rd, Kukreja RC: HIF-1 activation attenuates postischemic myocardial injury: role for heme oxygenase-1 in modulating microvascular chemokine generation. Am J Physiol Heart Circ Physiol 2005, 289: H542-H548. 10.1152/ajpheart.00089.2005
44. Takaku M, Tomita S, Kurobe H, Kihira Y, Morimoto A, Higashida M, Ikeda Y, Ushiyama A, Hashimoto I, Nakanishi H, Tamaki T: Systemic preconditioning by a prolyl hydroxylase inhibitor promotes prevention of skin flap necrosis via HIF-1-induced bone marrow-derived cells. PLoS One 2012, 7: e42964. 10.1371/journal.pone.0042964
45. Psaltis PJ, Zannettino AC, Worthley SG, Gronthos S: Concise review: mesenchymal stromal cells: potential for cardiovascular repair. Stem Cells 2008, 26: 2201-2210. 10.1634/stemcells.2008-0428
46. Olson SD, Pollock K, Kambal A, Cary W, Mitchell GM, Tempkin J, Stewart H, McGee J, Bauer G, Kim HS, Tempkin T, Wheelock V, Annett G, Dunbar G, Nolta JA: Genetically engineered mesenchymal stem cells as a proposed therapeutic for Huntington's disease. Mol Neurobiol 2012, 45: 87-98. 10.1007/s12035-011-8219-8
47. Yu X, Chen D, Zhang Y, Wu X, Huang Z, Zhou H, Zhang Z: Overexpression of CXCR4 in mesenchymal stem cells promotes migration, neuroprotection and angiogenesis in a rat model of stroke. J Neurol Sci 2012, 316: 141-149. 10.1016/j.jns.2012.01.001
48. Meuillet EJ, Mahadevan D, Vankayalapati H, Berggren M, Williams R, Coon A, Kozikowski AP, Powis G: Specific inhibition of the Akt1 pleckstrin homology domain by D-3-deoxy-phosphatidyl-myo-inositol analogues. Mol Cancer Ther 2003, 2: 389-399.
49. Kotch LE, Iyer NV, Laughner E, Semenza GL: Defective vascularization of HIF-1alpha-null embryos is not associated with VEGF deficiency but with mesenchymal cell death. Dev Biol 1999, 209: 254-267. 10.1006/dbio.1999.9253
50. Asikainen TM, Waleh NS, Schneider BK, Clyman RI, White CW: Enhancement of angiogenic effectors through hypoxia-inducible factor in preterm primate lung in vivo. Am J Physiol Lung Cell Mol Physiol 2006, 291: L588-L595. 10.1152/ajplung.00098.2006
51. Jiang BH, Liu LZ: PI3K/PTEN signaling in angiogenesis and tumorigenesis. Adv Cancer Res 2009, 102: 19-65.