Protective effects of mesenchymal stem cells with CXCR4 up-regulation in a rat renal transplantation model

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Cao, Zhiqiang ^a   Zhang, Geng ^a   Wang, Fuli ^a   Liu, Hongbao ^a   Liu, Long ^b   Han, Yaling ^a,b   Zhang, Jian ^c   Yuan, Jianlin ^a  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b GENERAL HOSPITAL OF NORTHERN THEATER COMMAND   (China)

^c FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; CELL MOVEMENT; CHEMOKINE CXCL12; GRAFT REJECTION; GREEN FLUORESCENT PROTEINS; KIDNEY TRANSPLANTATION; MESENCHYMAL STEM CELL TRANSPLANTATION; MODELS, ANIMAL; RATS; RECEPTORS, CXCR4; TRANSPLANTS; UP-REGULATION;

EID: 84893587153     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0082949     Document Type: Article

References (99)

1. Xu G, Zhang L, Ren G, Yuan Z, Zhang Y, et al. (2007) Immunosuppressive properties of cloned bone marrow mesenchymal stem cells. Cell Res 17: 240-248. (Pubitemid 46438724)
2. Bryan CF, Luger AM, Martinez J, Muruve N, Nelson PW, et al. (2001) Cold ischemia time: an independent predictor of increased HLA class I antibody production after rejection of a primary cadaveric renal allograft. Transplantation 71: 875-879. (Pubitemid 32417346)
3. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, et al. (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284: 143-147. (Pubitemid 29282067)
4. Hoogduijn MJ, Popp FC, Grohnert A, Crop MJ, van RM, et al. (2010) Advancement of mesenchymal stem cell therapy in solid organ transplantation (MISOT). Transplantation 90: 124-126.
5. Reinders ME, Fibbe WE, Rabelink TJ (2010) Multipotent mesenchymal stromal cell therapy in renal disease and kidney transplantation. Nephrol Dial Transplant 25: 17-24.
6. Kosieradzki M, Rowinski W (2008) Ischemia/reperfusion injury in kidney transplantation: mechanisms and prevention. Transplant Proc 40: 3279-3288.
7. Vatazin AV, Astakhov PV, Zul'karnaev AB, Kantariia RO, Artemov DV (2012) [Cellular factors of ischemia/reperfusion injury pathogenesis in the renal transplantation]. Ross Fiziol Zh Im I M Sechenova 98: 906-914.
8. Ge W, Jiang J, Arp J, Liu W, Garcia B, et al. (2010) Regulatory T-cell generation and kidney allograft tolerance induced by mesenchymal stem cells associated with indoleamine 2,3-dioxygenase expression. Transplantation 90: 1312-1320.
9. De Martino M, Zonta S, Rampino T, Gregorini M, Frassoni F, et al. (2010) Mesenchymal stem cells infusion prevents acute cellular rejection in rat kidney transplantation. Transplant Proc 42: 1331-1335.
10. Yoo KH, Jang IK, Lee MW, Kim HE, Yang MS, et al. (2009) Comparison of immunomodulatory properties of mesenchymal stem cells derived from adult human tissues. Cell Immunol 259: 150-156.
11. Kale S, Karihaloo A, Clark PR, Kashgarian M, Krause DS, et al. (2003) Bone marrow stem cells contribute to repair of the ischemically injured renal tubule. J Clin Invest 112: 42-49. (Pubitemid 38056374)
12. Le BK, Tammik C, Rosendahl K, Zetterberg E, Ringden O (2003) HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Exp Hematol 31: 890-896. (Pubitemid 37211373)
13. Lu LL, Liu YJ, Yang SG, Zhao QJ, Wang X, et al. (2006) Isolation and characterization of human umbilical cord mesenchymal stem cells with hematopoiesis-supportive function and other potentials. Haematologica 91: 1017-1026.
14. Munn DH, Sharma MD, Lee JR, Jhaver KG, Johnson TS, et al. (2002) Potential regulatory function of human dendritic cells expressing indoleamine 2,3-dioxygenase. Science 297: 1867-1870. (Pubitemid 35024345)
15. Le BK, Rasmusson I, Sundberg B, Gotherstrom C, Hassan M, et al. (2004) Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet 363: 1439-1441. (Pubitemid 38586721)
16. Deans RJ, Moseley AB (2000) Mesenchymal stem cells: biology and potential clinical uses. Exp Hematol 28: 875-884.
17. Nauta AJ, Fibbe WE (2007) Immunomodulatory properties of mesenchymal stromal cells. Blood 110: 3499-3506. (Pubitemid 350159613)
18. Poulsom R, Forbes SJ, Hodivala-Dilke K, Ryan E, Wyles S, et al. (2001) Bone marrow contributes to renal parenchymal turnover and regeneration. J Pathol 195: 229-235. (Pubitemid 32899033)
19. Lin F, Cordes K, Li L, Hood L, Couser WG, et al. (2003) Hematopoietic stem cells contribute to the regeneration of renal tubules after renal ischemia-reperfusion injury in mice. J Am Soc Nephrol 14: 1188-1199. (Pubitemid 36514661)
20. Riella LV, Chandraker A (2012) Stem cell therapy in kidney transplantation. JAMA 308: 130; author reply 130-131.
21. Togel F, Hu Z, Weiss K, Isaac J, Lange C, et al. (2005) Administered mesenchymal stem cells protect against ischemic acute renal failure through differentiation-independent mechanisms. Am J Physiol Renal Physiol 289: F31-F42. (Pubitemid 40863570)
22. Shyu WC, Lee YJ, Liu DD, Lin SZ, Li H (2006) Homing genes, cell therapy and stroke. Front Biosci 11: 899-907. (Pubitemid 43253445)
23. Chavakis E, Urbich C, Dimmeler S (2008) Homing and engraftment of progenitor cells: a prerequisite for cell therapy. J Mol Cell Cardiol 45: 514-522.
24. Sordi V (2009) Mesenchymal stem cell homing capacity. Transplantation 87: S42-S45.
25. Zonta S, De Martino M, Bedino G, Piotti G, Rampino T, et al. (2010) Which is the most suitable and effective route of administration for mesenchymal stem cell-based immunomodulation therapy in experimental kidney transplantation: endovenous or arterial. Transplant Proc 42: 1336-1340.
26. Duffield JS, Park KM, Hsiao LL, Kelley VR, Scadden DT, et al. (2005) Restoration of tubular epithelial cells during repair of the postischemic kidney occurs independently of bone marrow-derived stem cells. J Clin Invest 115: 1743-1755. (Pubitemid 40979713)
27. Fan VH, Tamama K, Au A, Littrell R, Richardson LB, et al. (2007) Tethered epidermal growth factor provides a survival advantage to mesenchymal stem cells. Stem Cells 25: 1241-1251. (Pubitemid 46684884)
28. Mylotte LA, Duffy AM, Murphy M, O'Brien T, Samali A, et al. (2008) Metabolic flexibility permits mesenchymal stem cell survival in an ischemic environment. Stem Cells 26: 1325-1336.
29. Schantz JT, Chim H, Whiteman M (2007) Cell guidance in tissue engineering: SDF-1 mediates site-directed homing of mesenchymal stem cells within three-dimensional polycaprolactone scaffolds. Tissue Eng 13: 2615-2624. (Pubitemid 350076752)
30. Shi M, Li J, Liao L, Chen B, Li B, et al. (2007) Regulation of CXCR4 expression in human mesenchymal stem cells by cytokine treatment: role in homing efficiency in NOD/SCID mice. Haematologica 92: 897-904. (Pubitemid 350144236)
31. Zhuang Y, Chen X, Xu M, Zhang LY, Xiang F (2009) Chemokine stromal cell-derived factor 1/CXCL12 increases homing of mesenchymal stem cells to injured myocardium and neovascularization following myocardial infarction. Chin Med J (Engl) 122: 183-187.
32. Belema-Bedada F, Uchida S, Martire A, Kostin S, Braun T (2008) Efficient homing of multipotent adult mesenchymal stem cells depends on FROUNT-mediated clustering of CCR2. Cell Stem Cell 2: 566-575. (Pubitemid 351729213)
33. Son BR, Marquez-Curtis LA, Kucia M, Wysoczynski M, Turner AR, et al. (2006) Migration of bone marrow and cord blood mesenchymal stem cells in vitro is regulated by stromal-derived factor-1-CXCR4 and hepatocyte growth factor-c-met axes and involves matrix metalloproteinases. Stem Cells 24: 1254-1264. (Pubitemid 44464694)
34. Kyriakou C, Rabin N, Pizzey A, Nathwani A, Yong K (2008) Factors that influence short-term homing of human bone marrow-derived mesenchymal stem cells in a xenogeneic animal model. Haematologica 93: 1457-1465.
35. Pasha Z, Wang Y, Sheikh R, Zhang D, Zhao T, et al. (2008) Preconditioning enhances cell survival and differentiation of stem cells during transplantation in infarcted myocardium. Cardiovasc Res 77: 134-142. (Pubitemid 351195153)
36. Liu H, Liu S, Li Y, Wang X, Xue W, et al. (2012) The role of SDF-1-CXCR4/ CXCR7 axis in the therapeutic effects of hypoxia-preconditioned mesenchymal stem cells for renal ischemia/reperfusion injury. PLoS One 7: e34608.
37. Kortesidis A, Zannettino A, Isenmann S, Shi S, Lapidot T, et al. (2005) Stromal-derived factor-1 promotes the growth, survival, and development of human bone marrow stromal stem cells. Blood 105: 3793-3801. (Pubitemid 40656121)
38. Otsuru S, Tamai K, Yamazaki T, Yoshikawa H, Kaneda Y (2008) Circulating bone marrow-derived osteoblast progenitor cells are recruited to the bone-forming site by the CXCR4/stromal cell-derived factor-1 pathway. Stem Cells 26: 223-234.
39. Djouad F, Plence P, Bony C, Tropel P, Apparailly F, et al. (2003) Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals. Blood 102: 3837-3844. (Pubitemid 37409409)
40. Dominici M, Le BK, Mueller I, Slaper-Cortenbach I, Marini F, et al. (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8: 315-317. (Pubitemid 44269669)
41. Tan J, Wu W, Xu X, Liao L, Zheng F, et al. (2012) Induction therapy with autologous mesenchymal stem cells in living-related kidney transplants: a randomized controlled trial. JAMA 307: 1169-1177.
42. Bi B, Schmitt R, Israilova M, Nishio H, Cantley LG (2007) Stromal cells protect against acute tubular injury via an endocrine effect. J Am Soc Nephrol 18: 2486-2496. (Pubitemid 47378865)
43. Devine SM, Cobbs C, Jennings M, Bartholomew A, Hoffman R (2003) Mesenchymal stem cells distribute to a wide range of tissues following systemic infusion into nonhuman primates. Blood 101: 2999-3001. (Pubitemid 36857986)
44. Lee RH, Pulin AA, Seo MJ, Kota DJ, Ylostalo J, et al. (2009) Intravenous hMSCs improve myocardial infarction in mice because cells embolized in lung are activated to secrete the anti-inflammatory protein TSG-6. Cell Stem Cell 5: 54-63.
45. Sordi V, Malosio ML, Marchesi F, Mercalli A, Melzi R, et al. (2005) Bone marrow mesenchymal stem cells express a restricted set of functionally active chemokine receptors capable of promoting migration to pancreatic islets. Blood 106: 419-427. (Pubitemid 40981232)
46. Ji JF, He BP, Dheen ST, Tay SS (2004) Interactions of chemokines and chemokine receptors mediate the migration of mesenchymal stem cells to the impaired site in the brain after hypoglossal nerve injury. Stem Cells 22: 415-427. (Pubitemid 38736625)
47. Schioppa T, Uranchimeg B, Saccani A, Biswas SK, Doni A, et al. (2003) Regulation of the chemokine receptor CXCR4 by hypoxia. J Exp Med 198: 1391-1402. (Pubitemid 37392484)
48. Askari AT, Unzek S, Popovic ZB, Goldman CK, Forudi F, et al. (2003) Effect of stromal-cell-derived factor 1 on stem-cell homing and tissue regeneration in ischaemic cardiomyopathy. Lancet 362: 697-703. (Pubitemid 37101067)
49. Kim K, Lee KM, Han DJ, Yu E, Cho YM (2008) Adult stem cell-like tubular cells reside in the corticomedullary junction of the kidney. Int J Clin Exp Pathol 1: 232-241.
50. Wood KJ (2003) Passenger leukocytes and microchimerism: what role in tolerance induction. Transplantation 75: 17S-20S.
51. van der Woude FJ, Schnuelle P, Yard BA (2004) Preconditioning strategies to limit graft immunogenicity and cold ischemic organ injury. J Investig Med 52: 323-329. (Pubitemid 39447363)
52. Li B, Cohen A, Hudson TE, Motlagh D, Amrani DL, et al. (2010) Mobilized human hematopoietic stem/progenitor cells promote kidney repair after ischemia/reperfusion injury. Circulation 121: 2211-2220.
53. Masereeuw R (2009) Contribution of bone marrow-derived cells in renal repair after acute kidney injury. Minerva Urol Nefrol 61: 373-384.
54. Morigi M, Introna M, Imberti B, Corna D, Abbate M, et al. (2008) Human bone marrow mesenchymal stem cells accelerate recovery of acute renal injury and prolong survival in mice. Stem Cells 26: 2075-2082.
55. Szczypka MS, Westover AJ, Clouthier SG, Ferrara JL, Humes HD (2005) Rare incorporation of bone marrow-derived cells into kidney after folic acid-induced injury. Stem Cells 23: 44-54. (Pubitemid 40105290)
56. Kucia M, Reca R, Miekus K, Wanzeck J, Wojakowski W, et al. (2005) Trafficking of normal stem cells and metastasis of cancer stem cells involve similar mechanisms: pivotal role of the SDF-1-CXCR4 axis. Stem Cells 23: 879-894. (Pubitemid 41170944)
57. Ruster B, Gottig S, Ludwig RJ, Bistrian R, Muller S, et al. (2006) Mesenchymal stem cells display coordinated rolling and adhesion behavior on endothelial cells. Blood 108: 3938-3944. (Pubitemid 44864580)
58. Ip JE, Wu Y, Huang J, Zhang L, Pratt RE, Dzau VJ (2007) Mesenchymal stem cells use integrin beta1 not CXC chemokine receptor 4 for myocardial migration and engraftment. Mol Biol Cell 18: 2873-2882. (Pubitemid 47235295)
59. Annabi B, Lee YT, Turcotte S, Naud E, Desrosiers RR, et al. (2003) Hypoxia promotes murine bone-marrow-derived stromal cell migration and tube formation. Stem Cells 21: 337-347. (Pubitemid 36623175)
60. Bonig H, Priestley GV, Papayannopoulou T (2006) Hierarchy of molecular-pathway usage in bone marrow homing and its shift by cytokines. Blood 107: 79-86. (Pubitemid 43053527)
61. Liechty KW, MacKenzie TC, Shaaban AF, Radu A, Moseley AM, et al. (2000) Human mesenchymal stem cells engraft and demonstrate site-specific differentiation after in utero transplantation in sheep. Nat Med 6: 1282-1286.
62. Bochev I, Elmadjian G, Kyurkchiev D, Tzvetanov L, Altankova I, et al. (2008) Mesenchymal stem cells from human bone marrow or adipose tissue differently modulate mitogen-stimulated B-cell immunoglobulin production in vitro. Cell Biol Int 32: 384-393.
63. Karlsson H, Samarasinghe S, Ball LM, Sundberg B, Lankester AC, et al. (2008) Mesenchymal stem cells exert differential effects on alloantigen and virus-specific T-cell responses. Blood 112: 532-541.
64. Stagg J, Pommey S, Eliopoulos N, Galipeau J (2006) Interferon-gamma- stimulated marrow stromal cells: a new type of nonhematopoietic antigen-presenting cell. Blood 107: 2570-2577. (Pubitemid 43348704)
65. Karussis D, Kassis I, Kurkalli BG, Slavin S (2008) Immunomodulation and neuroprotection with mesenchymal bone marrow stem cells (MSCs): a proposed treatment for multiple sclerosis and other neuroimmunological/neurodegener-ative diseases. J Neurol Sci 265: 131-135.
66. Chabannes D, Hill M, Merieau E, Rossignol J, Brion R, et al. (2007) A role for heme oxygenase-1 in the immunosuppressive effect of adult rat and human mesenchymal stem cells. Blood 110: 3691-3694. (Pubitemid 350159638)
67. Krampera M, Glennie S, Dyson J, Scott D, Laylor R, et al. (2003) Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigen-specific T cells to their cognate peptide. Blood 101: 3722-3729. (Pubitemid 36857965)
68. Shi Y, Hu G, Su J, Li W, Chen Q, et al. (2010) Mesenchymal stem cells: a new strategy for immunosuppression and tissue repair. Cell Res 20: 510-518.
69. Patel SA, Meyer JR, Greco SJ, Corcoran KE, Bryan M, et al. (2010) Mesenchymal stem cells protect breast cancer cells through regulatory T cells: role of mesenchymal stem cell-derived TGF-beta. J Immunol 184: 5885-5894.
70. English K, Ryan JM, Tobin L, Murphy MJ, Barry FP, et al. (2009) Cell contact, prostaglandin E(2) and transforming growth factor beta 1 play non-redundant roles in human mesenchymal stem cell induction of CD4+CD25(High) forkhead box P3+ regulatory T cells. Clin Exp Immunol 156: 149-160.
71. Selmani Z, Naji A, Zidi I, Favier B, Gaiffe E, et al. (2008) Human leukocyte antigen-G5 secretion by human mesenchymal stem cells is required to suppress T lymphocyte and natural killer function and to induce CD4+CD25high-FOXP3+ regulatory T cells. Stem Cells 26: 212-222.
72. Goodnow CC, Sprent J, de St Groth B F, Vinuesa CG (2005) Cellular and genetic mechanisms of self tolerance and autoimmunity. Nature 435: 590-597. (Pubitemid 40825498)
73. Di IM, Del PB, De Ioanni M, Moretti L, Bonifacio E, et al. (2008) Mesenchymal cells recruit and regulate T regulatory cells. Exp Hematol 36: 309-318. (Pubitemid 351221170)
74. Sun L, Akiyama K, Zhang H, Yamaza T, Hou Y, et al. (2009) Mesenchymal stem cell transplantation reverses multiorgan dysfunction in systemic lupus erythematosus mice and humans. Stem Cells 27: 1421-1432.
75. Rafei M, Hsieh J, Fortier S, Li M, Yuan S, et al. (2008) Mesenchymal stromal cell-derived CCL2 suppresses plasma cell immunoglobulin production via STAT3 inactivation and PAX5 induction. Blood 112: 4991-4998.
76. Aggarwal S, Pittenger MF (2005) Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 105: 1815-1822. (Pubitemid 40223708)
77. Martinet L, Fleury-Cappellesso S, Gadelorge M, Dietrich G, Bourin P, et al. (2009) A regulatory cross-talk between Vgamma9Vdelta2 T lymphocytes and mesenchymal stem cells. Eur J Immunol 39: 752-762.
78. Ren G, Zhang L, Zhao X, Xu G, Zhang Y, et al. (2008) Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Cell Stem Cell 2: 141-150. (Pubitemid 351181031)
79. Ren G, Zhao X, Zhang L, Zhang J, L'Huillier A, et al. (2010) Inflammatory cytokine-induced intercellular adhesion molecule-1 and vascular cell adhesion molecule-1 in mesenchymal stem cells are critical for immunosuppression. J Immunol 184: 2321-2328.
80. Nemeth K, Keane-Myers A, Brown JM, Metcalfe DD, Gorham JD, et al. (2010) Bone marrow stromal cells use TGF-beta to suppress allergic responses in a mouse model of ragweed-induced asthma. Proc Natl Acad Sci U S A 107: 5652-5657.
81. Ghannam S, Pene J, Torcy-Moquet G, Jorgensen C, Yssel H (2010) Mesenchymal stem cells inhibit human Th17 cell differentiation and function and induce a T regulatory cell phenotype. J Immunol 185: 302-312.
82. English K, Barry FP, Field-Corbett CP, Mahon BP (2007) IFN-gamma and TNF-alpha differentially regulate immunomodulation by murine mesenchymal stem cells. Immunol Lett 110: 91-100. (Pubitemid 46830943)
83. Yagi H, Soto-Gutierrez A, Parekkadan B, Kitagawa Y, Tompkins RG, et al. (2010) Mesenchymal stem cells: mechanisms of immunomodulation and homing. Cell Transplant 19: 667-679.
84. Larrick JW, Graham D, Toy K, Lin LS, Senyk G, et al. (1987) Recombinant tumor necrosis factor causes activation of human granulocytes. Blood 69: 640-644. (Pubitemid 17022041)
85. Smith AN, Willis E, Chan VT, Muffley LA, Isik FF, et al. (2010) Mesenchymal stem cells induce dermal fibroblast responses to injury. Exp Cell Res 316: 48-54.
86. Fontenot JD, Rudensky AY (2005) A well adapted regulatory contrivance: regulatory T cell development and the forkhead family transcription factor Foxp3. Nat Immunol 6: 331-337. (Pubitemid 41716769)
87. Lange C, Togel F, Ittrich H, Clayton F, Nolte-Ernsting C, et al. (2005) Administered mesenchymal stem cells enhance recovery from ischemia/reperfusion- induced acute renal failure in rats. Kidney Int 68: 1613-1617. (Pubitemid 43169906)
88. Choi S, Park M, Kim J, Hwang S, Park S, Lee Y (2009) The role of mesenchymal stem cells in the functional improvement of chronic renal failure. Stem Cells Dev 18: 521-529.
89. Hara Y, Stolk M, Ringe J, Dehne T, Ladhoff J, et al. (2011) In vivo effect of bone marrow-derived mesenchymal stem cells in a rat kidney transplantation model with prolonged cold ischemia. Transpl Int 24: 1112-1123.
90. Togel F, Weiss K, Yang Y, Hu Z, Zhang P, et al. (2007) Vasculotropic, paracrine actions of infused mesenchymal stem cells are important to the recovery from acute kidney injury. Am J Physiol Renal Physiol 292: F1626-F1635. (Pubitemid 46701891)
91. Pino CJ, Humes HD (2010) Stem cell technology for the treatment of acute and chronic renal failure. Transl Res 156: 161-168.
92. Aldinucci A, Rizzetto L, Pieri L, Nosi D, Romagnoli P, et al. (2010) Inhibition of immune synapse by altered dendritic cell actin distribution: a new pathway of mesenchymal stem cell immune regulation. J Immunol 185: 5102-5110.
93. English K, Barry FP, Mahon BP (2008) Murine mesenchymal stem cells suppress dendritic cell migration, maturation and antigen presentation. Immunol Lett 115: 50-58. (Pubitemid 350298590)
94. Jiang XX, Zhang Y, Liu B, Zhang SX, Wu Y, et al. (2005) Human mesenchymal stem cells inhibit differentiation and function of monocyte-derived dendritic cells. Blood 105: 4120-4126. (Pubitemid 40656164)
95. Nauta AJ, Kruisselbrink AB, Lurvink E, Willemze R, Fibbe WE (2006) Mesenchymal stem cells inhibit generation and function of both CD34+-derived and monocyte-derived dendritic cells. J Immunol 177: 2080-2087. (Pubitemid 44200965)
96. Lee PT, Lin HH, Jiang ST, Lu PJ, Chou KJ, et al. (2010) Mouse kidney progenitor cells accelerate renal regeneration and prolong survival after ischemic injury. Stem Cells 28: 573-584.
97. Inoue S, Popp FC, Koehl GE, Piso P, Schlitt HJ, et al. (2006) Immunomodulatory effects of mesenchymal stem cells in a rat organ transplant model. Transplantation 81: 1589-1595. (Pubitemid 43890897)
98. Gheisari Y, Azadmanesh K, Ahmadbeigi N, Nassiri SM, Golestaneh AF, et al. (2012) Genetic modification of mesenchymal stem cells to overexpress CXCR4 and CXCR7 does not improve the homing and therapeutic potentials of these cells in experimental acute kidney injury. Stem Cells Dev 21: 2969-2980.
99. Gupta S, Li S, Abedin MJ, Wang L, Schneider E, et al. (2010) Effect of Notch activation on the regenerative response to acute renal failure. Am J Physiol Renal Physiol 298: F209-F215.