Role of stromal cell derived factor-1/CXC chemokine receptor 4 pathway in mesenchymal stem cells therapies in the management of diabetic retinopathy_Chinese Journal of Ocular Fundus Diseases

Authors：

WangJian ,  ChenSong

Clinical College of Ophthalmology of Tianjin Medical University, Tianjin Eye Hospital, Tianjin Key Lab of Ophthalmology and Visual Science, Tianjin Institute of Ophthalmology, Tianjin 300020, China;

Corresponding author：

ChenSong, Email: chensong20@hotmail.com

Keywords：

Diabetic retinopathy/therapy; Chemokine CXCL12; Receptors; CXCR4; Mesenchymal stem cells; Review

DOI：

10.3760/cma.j.issn.1005-1015.2016.06.029

Video：

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Abstract Full text Figures/Tables Video References Cited by

Mesenchymal stem cells (MSC) are considered to have important value in the treatment of various diseases because of their low immunogenicity, transferability, and strong tissue repair capacity. Stromal cell derived factor-1 (SDF-1) and its receptor CXC chemokine receptor 4 (CXCR4) pathway plays an important role in migration of MSC. The induction of homing of MSC to retina by regulating SDF-1/CXCR4 may exert the curative effect on diabetic retinopathy to greatest exent.

Citation： WangJian, ChenSong. Role of stromal cell derived factor-1/CXC chemokine receptor 4 pathway in mesenchymal stem cells therapies in the management of diabetic retinopathy. Chinese Journal of Ocular Fundus Diseases, 2016, 32(6): 663-666. doi: 10.3760/cma.j.issn.1005-1015.2016.06.029 Copy

1.	Krampera M, Glennie S, Dyson J, et al. Bone marrow mesenchymal stem cells inhibit the response of naïve and memory antigen-specific T cells to their cognate peptide[J].Blood, 2003, 101(9):3722-3729.
2.	Yan H, Wu M, Yuan Y, et al. Priming of Toll-like receptor 4 pathway in mesenchymal stem cells increases expression of B cell activating factor[J].Biochem Biophys Res Commun, 2014, 448(2):212-217.DOI:10.1016/j.bbrc.2014.04.097.
3.	Chiesa S, Morbelli S, Morando S, et al. Mesenchymal stem cells impair in vivo T-cell priming by dendritic cells[J]. Proc Natl Acad Sci USA, 2011, 108(42):17384-17389. DOI:10.1073/pnas.1103650108.
4.	姜鉴洪, 孔佳慧, 陈松, 等.神经干细胞玻璃体腔移植对糖尿病大鼠视网膜功能及结构的影响[J].中华眼底病杂志, 2016, 32(4):418-422.DOI:10.3760/cma.j.issn.1005-1015.2016.04.017.Jiang JH, Kong JH, Chen S, et al. The effects on the function and structure of retina in diabetic rats by intravitreal transplantation of human umbilical cord cells-induced neuronal stem cells[J].Chin J Ocul Fundus Dis, 2016, 32(4):418-422.DOI:10.3760/cma.j.issn.1005-1015.2016.04.017.
5.	Shaw LC, Neu MB, Grant MB. Cell-based therapies for diabetic retinopathy[J].Curr Diab Rep, 2011, 11(4):265-274.DOI:10.1007/s11892-011-0197-8.
6.	Kojima H, Kim J, Chan L. Emerging roles of hematopoietic cells in the pathobiology of diabetic complications[J].Trends Endocrinol Metab, 2014, 25(4):178-187.DOI:10.1016/j.tem.2014.01.002.
7.	Megaw R, Dhillon B. Stem cell therapies in the management of diabetic retinopathy[J].Curr Diab Rep, 2014, 14(7):498. DOI:10.1007/s11892-014-0498-9.
8.	Rajashekhar G. Mesenchymal stem cells:new players in retinopathy therapy[J].Front Endocrinol (Lausanne), 2014, 5:59.DOI:10.3389/fendo.2014.00059.
9.	Yang Z, Li K, Yan X, et al. Amelioration of diabetic retinopathy by engrafted human adipose-derived mesenchymal stem cells in streptozotocin diabetic rats[J].Graefe's Arch Clin Exp Ophthalmol, 2010, 248(10):1415-1422. DOI:10.1007/s00417-010-1384-z.
10.	Scalinci SZ, Scorolli L, Corradetti G, et al. Potential role of intravitreal human placental stem cell implants in inhibiting progression of diabetic retinopathy in type 2 diabetes:neuroprotective growth factors in the vitreous[J].Clin Ophthalmol, 2011, 5:691-696.DOI:10.2147/OPTH.S21161.
11.	毕雪, 陈松, 林锦镛, 等.不同途径移植人脐带间充质干细胞对糖尿病大鼠视网膜病变的影响[J].中华眼底病杂志, 2014, 30(2):166-170. DOI:10.3760/cma.j.issn.1005-1015.2014.02.012.Bi X, Chen S, Lin JY, et al. Systemic and ocular transplantation of human umbilical cord mesenchymal stem cells into rats with diabetic retinopathy[J].Chin J Ocul Fundus Dis, 2014, 30(2):166-170. DOI:10.3760/cma.j.issn.1005-1015.2014.02.012.
12.	何远东, 王玉, 彭江, 等.人脐带间充质干细胞中神经营养因子的表达[J].中华神经医学杂志, 2012, 11(5):438-442.DOI:10.3760/cma.j.issn.1671-8925.2012.05.002.He YD, Wang Y, Peng J, et al. Expregsion of neurotrophic factors in human umbilical cord-derived mesenchymal stromal cells[J].Chin J Neuromed, 2012, 11(5):438-442.DOI:10.3760/cma.j.issn.1671-8925.2012.05.002.
13.	Hammes HP, Lin J, Renner O, et al. Pericytes and the pathogenesis of diabetic retinopathy[J].Diabetes, 2002, 51(10):3107-3112.
14.	Yi T, Song SU. Immunomodulatory properties of mesenchymal stem cells and their therapeutic applications[J].Arch Pharm Res, 2012, 35(2):213-221.DOI:10.1007/s12272-012-0202-z.
15.	Galipeau J. The mesenchymal stromal cells dilemma--does a negative phase Ⅲ trial of random donor mesenchymal stromal cells in steroid-resistant graft-versus-host disease represent a death knell or a bump in the road?[J]. Cytotherapy, 2013, 15(1):2-8. DOI:10.1016/j.jcyt.2012.10.002.
16.	Taghavi S, George JC. Homing of stem cells to ischemic myocardium[J].Am J Transl Res, 2013, 5(4):404-411.
17.	Honczarenko M, Le Y, Swierkowski M, et al. Human bone marrow stromal cells express a distinct set of biologically functional chemokine receptors[J].Stem Cells, 2006, 24(4):1030-1041.
18.	Chen W, Li M, Cheng H, et al. Overexpression of the mesenchymal stem cell CXCR4 gene in irradiated mice increases the homing capacity of these cells[J].Cell Biochem Biophys, 2013, 67(3):1181-1191.DOI:10.1007/s12013-013-9632-6.
19.	Shirozu M, Nakano T, Inazawa J, et al. Structure and chromosomal localization of the human stromal cell-derived factor 1(SDF1) gene[J].Genomics, 1995, 28(3):495-500.
20.	Cencioni C, Capogrossi MC, Napolitano M. The SDF-1/CXCR4 axis in stem cell preconditioning[J].Cardiovasc Res, 2012, 94(3):400-407.DOI:10.1093/cvr/cvs132.
21.	Penn MS, Pastore J, Miller T, et al. SDF-1 in myocardial repair[J].Gene Ther, 2012, 19(6):583-587.DOI:10.1038/gt.2012.32.
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23.	Xu X, Zhu F, Zhang M, et al. Stromal cell-derived factor-1 enhances wound healing through recruiting bone marrow-derived mesenchymal stem cells to the wound area and promoting neovaseularization[J].Cells Tissues Organs, 2013, 197(2):103-113.DOI:10.1159/000342921.
24.	Kitaori T, Ito H, Schwarz EM, et al. Stromal cell-derived factor 1/CXCR4 signaling is critical for the recruitment of mesenchymal stem cells to the fracture site during skeletal repair in a mouse model[J].Arthritis Rheum, 2009, 60(3):813-823.DOI:10.1002/art.24330.
25.	Son BR, Marquez-Curtis LA, Kucia M, et al. 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[J]. Stem Cells, 2006, 24(5):1254-1264.
26.	Butler JM, Guthrie SM, Koc M, et al. SDF-1 is both necessary and sufficient to promote proliferative retinopathy[J].J Clin Invest, 2005, 115(1):86-93.
27.	Stich S, Haag M, Häupl T, et al. Gene expression profiling of human mesenchymal stem cells chemotactically induced with CXCL12[J].Cell Tissue Res, 2009, 336(2):225-236. DOI:10.1007/s00441-009-0768-z.
28.	Liu N, Tian J, Cheng J, et al. Migration of CXCR4 gene-modified bone marrow-derived mesenchymal stem cells to the acute injured kidney[J].J Cell Biochem, 2013, 114(12):2677-2689. DOI:10.1002/jcb.24615.
29.	Liu N, Patzak A, Zhang J. CXCR4-overexpressing bone marrow-derived mesenchymal stem cells improve repair of acute kidney injury[J].Am J Physiol Renal Physiol, 2013, 305(7):1064-1073. DOI:10.1152/ajprenal.00178.2013.
30.	刘楠梅, 梅长林, 张金元, 等.过表达CXCR4的骨髓间充质干细胞对共培养低氧/复氧肾小管上皮细胞的修复作用[J].中华肾脏病杂志, 2013, 29(11):830-836.DOI:10.3760/cma.j.issn.1001-7097.2013.11.007.Liu NM, Mei CL, Zhang JY, et al. Effect of CXCR4-overexpressing bone marrow-derived mesenchymal stem cells on the repair of the co-cultured hypoxia/re-oxygenation renal tubular epithelial cells and its possible mechanism[J].Chin J Nephrol, 2013, 29(11):830-836.DOI:10.3760/cma.j.issn.1001-7097.2013.11.007.
31.	Cheng Z, Ou L, Zhou X, et al. Targeted migration of mesenchymal stem cells modified with CXCR4 gene to infarcted myocardium improves cardiac performance[J].Mol Ther, 2008, 16(3):571-579. DOI:10.1038/sj.mt.6300374.
32.	Dong F, Harvey J, Finan A, et al. Myocardial CXCR4 expression is required for mesenchymal stem cell mediated repair following acute myocardial infarction[J].Circulation, 2012, 126(3):314-324.DOI:10.1161/CIRCULATIONAHA.111.082453.
33.	Hu C, Yong X, Li C, et al. CXCL12/CXCR4 axis promotes mesenchymal stem cell mobilization to burn wounds and contributes to wound repair[J].J Surg Res, 2013, 183(1):427-434.DOI:10.1016/j.jss.2013.01.019.
34.	Yu X, Chen D, Zhang Y, et al. Overexpression of CXCR4 in mesenchymal stem cells promotes migration, neuroprotection and angiogenesis in a rat model of stroke[J].J Neurol Sci, 2012, 316(1-2):141-149.DOI:10.1016/j.jns.2012.01.001.
35.	Honczarenko M, Le Y, Swierkowski M, et al. Human bone marrow stromal cells express a distinct set of biologically functional chemokine receptors[J].Stem Cells, 2006, 24(4):1030-1041.
36.	Wynn RF, Hart CA, Corradi-Perini C, et al. A small proportion of mesenchymal stem cells strongly expresses functionally active CXCR4 receptor capable of promoting migration to bone marrow[J].Blood, 2004, 104(9):2643-2645.
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38.	Chen W, Li M, Cheng H, et al. Overexpression of the mesenchymal stem cell CXCR4 gene in irradiated mice increases the homing capacity of these cells[J].Cell Biochem Biophys, 2013, 67(3):1181-1191. DOI:10.1007/s12013-013-9632-6.
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1. Krampera M, Glennie S, Dyson J, et al. Bone marrow mesenchymal stem cells inhibit the response of naïve and memory antigen-specific T cells to their cognate peptide[J].Blood, 2003, 101(9):3722-3729.
2. Yan H, Wu M, Yuan Y, et al. Priming of Toll-like receptor 4 pathway in mesenchymal stem cells increases expression of B cell activating factor[J].Biochem Biophys Res Commun, 2014, 448(2):212-217.DOI:10.1016/j.bbrc.2014.04.097.
3. Chiesa S, Morbelli S, Morando S, et al. Mesenchymal stem cells impair in vivo T-cell priming by dendritic cells[J]. Proc Natl Acad Sci USA, 2011, 108(42):17384-17389. DOI:10.1073/pnas.1103650108.
4. 姜鉴洪, 孔佳慧, 陈松, 等.神经干细胞玻璃体腔移植对糖尿病大鼠视网膜功能及结构的影响[J].中华眼底病杂志, 2016, 32(4):418-422.DOI:10.3760/cma.j.issn.1005-1015.2016.04.017.Jiang JH, Kong JH, Chen S, et al. The effects on the function and structure of retina in diabetic rats by intravitreal transplantation of human umbilical cord cells-induced neuronal stem cells[J].Chin J Ocul Fundus Dis, 2016, 32(4):418-422.DOI:10.3760/cma.j.issn.1005-1015.2016.04.017.
5. Shaw LC, Neu MB, Grant MB. Cell-based therapies for diabetic retinopathy[J].Curr Diab Rep, 2011, 11(4):265-274.DOI:10.1007/s11892-011-0197-8.
6. Kojima H, Kim J, Chan L. Emerging roles of hematopoietic cells in the pathobiology of diabetic complications[J].Trends Endocrinol Metab, 2014, 25(4):178-187.DOI:10.1016/j.tem.2014.01.002.
7. Megaw R, Dhillon B. Stem cell therapies in the management of diabetic retinopathy[J].Curr Diab Rep, 2014, 14(7):498. DOI:10.1007/s11892-014-0498-9.
8. Rajashekhar G. Mesenchymal stem cells:new players in retinopathy therapy[J].Front Endocrinol (Lausanne), 2014, 5:59.DOI:10.3389/fendo.2014.00059.
9. Yang Z, Li K, Yan X, et al. Amelioration of diabetic retinopathy by engrafted human adipose-derived mesenchymal stem cells in streptozotocin diabetic rats[J].Graefe's Arch Clin Exp Ophthalmol, 2010, 248(10):1415-1422. DOI:10.1007/s00417-010-1384-z.
10. Scalinci SZ, Scorolli L, Corradetti G, et al. Potential role of intravitreal human placental stem cell implants in inhibiting progression of diabetic retinopathy in type 2 diabetes:neuroprotective growth factors in the vitreous[J].Clin Ophthalmol, 2011, 5:691-696.DOI:10.2147/OPTH.S21161.
11. 毕雪, 陈松, 林锦镛, 等.不同途径移植人脐带间充质干细胞对糖尿病大鼠视网膜病变的影响[J].中华眼底病杂志, 2014, 30(2):166-170. DOI:10.3760/cma.j.issn.1005-1015.2014.02.012.Bi X, Chen S, Lin JY, et al. Systemic and ocular transplantation of human umbilical cord mesenchymal stem cells into rats with diabetic retinopathy[J].Chin J Ocul Fundus Dis, 2014, 30(2):166-170. DOI:10.3760/cma.j.issn.1005-1015.2014.02.012.
12. 何远东, 王玉, 彭江, 等.人脐带间充质干细胞中神经营养因子的表达[J].中华神经医学杂志, 2012, 11(5):438-442.DOI:10.3760/cma.j.issn.1671-8925.2012.05.002.He YD, Wang Y, Peng J, et al. Expregsion of neurotrophic factors in human umbilical cord-derived mesenchymal stromal cells[J].Chin J Neuromed, 2012, 11(5):438-442.DOI:10.3760/cma.j.issn.1671-8925.2012.05.002.
13. Hammes HP, Lin J, Renner O, et al. Pericytes and the pathogenesis of diabetic retinopathy[J].Diabetes, 2002, 51(10):3107-3112.
14. Yi T, Song SU. Immunomodulatory properties of mesenchymal stem cells and their therapeutic applications[J].Arch Pharm Res, 2012, 35(2):213-221.DOI:10.1007/s12272-012-0202-z.
15. Galipeau J. The mesenchymal stromal cells dilemma--does a negative phase Ⅲ trial of random donor mesenchymal stromal cells in steroid-resistant graft-versus-host disease represent a death knell or a bump in the road?[J]. Cytotherapy, 2013, 15(1):2-8. DOI:10.1016/j.jcyt.2012.10.002.
16. Taghavi S, George JC. Homing of stem cells to ischemic myocardium[J].Am J Transl Res, 2013, 5(4):404-411.
17. Honczarenko M, Le Y, Swierkowski M, et al. Human bone marrow stromal cells express a distinct set of biologically functional chemokine receptors[J].Stem Cells, 2006, 24(4):1030-1041.
18. Chen W, Li M, Cheng H, et al. Overexpression of the mesenchymal stem cell CXCR4 gene in irradiated mice increases the homing capacity of these cells[J].Cell Biochem Biophys, 2013, 67(3):1181-1191.DOI:10.1007/s12013-013-9632-6.
19. Shirozu M, Nakano T, Inazawa J, et al. Structure and chromosomal localization of the human stromal cell-derived factor 1(SDF1) gene[J].Genomics, 1995, 28(3):495-500.
20. Cencioni C, Capogrossi MC, Napolitano M. The SDF-1/CXCR4 axis in stem cell preconditioning[J].Cardiovasc Res, 2012, 94(3):400-407.DOI:10.1093/cvr/cvs132.
21. Penn MS, Pastore J, Miller T, et al. SDF-1 in myocardial repair[J].Gene Ther, 2012, 19(6):583-587.DOI:10.1038/gt.2012.32.
22. Marquez-Curtis LA, Janowska-Wieczorek A. Enhancing the migration ability of mesenchymal stromal cells by targeting the SDF-1/CXCR4 axis[J/OL].Biomed Res Int, 2013, 2013:561098[2013-12-05].http://europepmc.org/abstralt/MED/24381939.DOI:10.1155/2013/561098" target="_blank">10.1155/2013/561098">http://europepmc.org/abstralt/MED/24381939.DOI:10.1155/2013/561098.
23. Xu X, Zhu F, Zhang M, et al. Stromal cell-derived factor-1 enhances wound healing through recruiting bone marrow-derived mesenchymal stem cells to the wound area and promoting neovaseularization[J].Cells Tissues Organs, 2013, 197(2):103-113.DOI:10.1159/000342921.
24. Kitaori T, Ito H, Schwarz EM, et al. Stromal cell-derived factor 1/CXCR4 signaling is critical for the recruitment of mesenchymal stem cells to the fracture site during skeletal repair in a mouse model[J].Arthritis Rheum, 2009, 60(3):813-823.DOI:10.1002/art.24330.
25. Son BR, Marquez-Curtis LA, Kucia M, et al. 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[J]. Stem Cells, 2006, 24(5):1254-1264.
26. Butler JM, Guthrie SM, Koc M, et al. SDF-1 is both necessary and sufficient to promote proliferative retinopathy[J].J Clin Invest, 2005, 115(1):86-93.
27. Stich S, Haag M, Häupl T, et al. Gene expression profiling of human mesenchymal stem cells chemotactically induced with CXCL12[J].Cell Tissue Res, 2009, 336(2):225-236. DOI:10.1007/s00441-009-0768-z.
28. Liu N, Tian J, Cheng J, et al. Migration of CXCR4 gene-modified bone marrow-derived mesenchymal stem cells to the acute injured kidney[J].J Cell Biochem, 2013, 114(12):2677-2689. DOI:10.1002/jcb.24615.
29. Liu N, Patzak A, Zhang J. CXCR4-overexpressing bone marrow-derived mesenchymal stem cells improve repair of acute kidney injury[J].Am J Physiol Renal Physiol, 2013, 305(7):1064-1073. DOI:10.1152/ajprenal.00178.2013.
30. 刘楠梅, 梅长林, 张金元, 等.过表达CXCR4的骨髓间充质干细胞对共培养低氧/复氧肾小管上皮细胞的修复作用[J].中华肾脏病杂志, 2013, 29(11):830-836.DOI:10.3760/cma.j.issn.1001-7097.2013.11.007.Liu NM, Mei CL, Zhang JY, et al. Effect of CXCR4-overexpressing bone marrow-derived mesenchymal stem cells on the repair of the co-cultured hypoxia/re-oxygenation renal tubular epithelial cells and its possible mechanism[J].Chin J Nephrol, 2013, 29(11):830-836.DOI:10.3760/cma.j.issn.1001-7097.2013.11.007.
31. Cheng Z, Ou L, Zhou X, et al. Targeted migration of mesenchymal stem cells modified with CXCR4 gene to infarcted myocardium improves cardiac performance[J].Mol Ther, 2008, 16(3):571-579. DOI:10.1038/sj.mt.6300374.
32. Dong F, Harvey J, Finan A, et al. Myocardial CXCR4 expression is required for mesenchymal stem cell mediated repair following acute myocardial infarction[J].Circulation, 2012, 126(3):314-324.DOI:10.1161/CIRCULATIONAHA.111.082453.
33. Hu C, Yong X, Li C, et al. CXCL12/CXCR4 axis promotes mesenchymal stem cell mobilization to burn wounds and contributes to wound repair[J].J Surg Res, 2013, 183(1):427-434.DOI:10.1016/j.jss.2013.01.019.
34. Yu X, Chen D, Zhang Y, et al. Overexpression of CXCR4 in mesenchymal stem cells promotes migration, neuroprotection and angiogenesis in a rat model of stroke[J].J Neurol Sci, 2012, 316(1-2):141-149.DOI:10.1016/j.jns.2012.01.001.
35. Honczarenko M, Le Y, Swierkowski M, et al. Human bone marrow stromal cells express a distinct set of biologically functional chemokine receptors[J].Stem Cells, 2006, 24(4):1030-1041.
36. Wynn RF, Hart CA, Corradi-Perini C, et al. A small proportion of mesenchymal stem cells strongly expresses functionally active CXCR4 receptor capable of promoting migration to bone marrow[J].Blood, 2004, 104(9):2643-2645.
37. Cao Z, Zhang G, Wang F, et al. Protective effects of mesenchymal stem cells with CXCR4 up-regulation in a rat renal transplantation model[J/OL].PLoS One, 2013, 8(12):82949[2013-12-30]. 10.1371/journal.pone.0082949">http://dx.plos.org/10.1371/journal.pone.0082949. DOI:10.1371/journal.pone.0082949.
38. Chen W, Li M, Cheng H, et al. Overexpression of the mesenchymal stem cell CXCR4 gene in irradiated mice increases the homing capacity of these cells[J].Cell Biochem Biophys, 2013, 67(3):1181-1191. DOI:10.1007/s12013-013-9632-6.
39. Li P, Gao Y, Liu Z, et al. DNA transfection of bone marrow stromal cells using microbubble-mediated ultrasound and polyethylenimine:an in vitro study[J].Cell Biochem Biophys, 2013, 66(3):775-786.DOI:10.1007/s12013-013-9523-x.
40. Shi M, Li J, Liao L, et al. Regulation of CXCR4 expression in human mesenchymal stem cells by cytokine treatment:role in homing efficiency in NOD/SCID mice[J].Haematologica, 2007, 92(7):897-904.
41. Tsai LK, Leng Y, Wang Z, et al. The mood stabilizers valproic acid and lithium enhance mesenchymal stem cell migration via distinct mechanisms[J]. Neuropsychopharmacology, 2010, 35(11):2225-2237.DOI:10.1038/npp.2010.97.
42. Najafi R, Sharifi AM. Deferoxamine preconditioning potentiates mesenchymal stem cell homing in vitro and in streptozotocin-diabetic rats[J].Expert Opin Biol Ther, 2013, 13(7):959-972.DOI:10.1517/14712598.2013.782390.
43. Li S, Deng Y, Feng J, et al. Oxidative preconditioning promotes bone marrow mesenchymal stem cells migration and prevents apoptosis[J].Cell Biol Int, 2009, 33(3):411-418.DOI:10.1016/j.cellbi.2009.01.012.
44. Liu H, Liu S, Li Y, et al. The role of SDF-1-CXCR4/CXCR7 axis in the therapeutic effects of hypoxia-preconditioned mesenchymal stem cells for renal ischemia/reperfusion injury[J/OL]. PLoS One, 2012, 7(4):34608[2012-04-12]. 10.1371/journal.pone.0034608">http://dx.plos.org/10.1371/journal.pone.0034608. DOI:10.1371/journal.pone.0034608.
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