COMPARISON OF BIOLOGICAL DIFFERENCE BETWEEN BONE MARROW AND PLACENTA-DERIVED MESENCHIMAL STEM CELLS IN HYPOXIA_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

XIABo ,  TANMeiyun

Department of Bone and Joint Surgery, the Affiliated Hospital of Luzhou Medical College, Luzhou Sichuan, 646000, P. R. China;

Corresponding author：

TANMeiyun, Email: lzmcorth@163.com

Keywords：

Bone marrow mesenchymal stem cells; Placenta-derived MSCs; Hypoxia; Seed cells; Regenerative medicine

DOI：

10.7507/1002-1892.20150021

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To comprehensively analyze and compare the biological difference between bone marrow mesenchymal stem cells (BMSCs) and placenta-derived MSCs (PMSCs) in hypoxia and to extend the knowledge for seed cells selection. Methods The domestic and foreign related literature about the effects of hypoxia microenvironment on proliferation, apoptosis, differentiation, paracrine secretion, migration, and homing ability of BMSCs and PMSCs were summarized and analysed. Results PMSCs proliferated much faster and more sensitive to the hypoxia than BMSCs; in addition, PMSCs showed stronger survivability. Similar to BMSCs, PMSCs can home to hypoxic-ischemic tissues efficiently, secrete a lot of growth factors and differentiate into tissue-specific cells to stimulate tissue regeneration. Conclusion PMSCs as the seed cells will have broad application prospects in the regenerative medicine.

Citation： XIABo, TANMeiyun. COMPARISON OF BIOLOGICAL DIFFERENCE BETWEEN BONE MARROW AND PLACENTA-DERIVED MESENCHIMAL STEM CELLS IN HYPOXIA. Chinese Journal of Reparative and Reconstructive Surgery, 2015, 29(1): 103-107. doi: 10.7507/1002-1892.20150021 Copy

1.	Rylova JV, Andreeva ER, Gogvadze VG, et al. Etoposide and hypoxia do not activate apoptosis of multipotent mesenchymal stromal cells in vitro. Bull Exp Biol Med, 2012, 154(1):141-144.
2.	ou M, Cui J, Liu J, et al. Angiopoietin-like 4 confers resistance to hypoxia/serum deprivation-induced apoptosis through pi3k/akt and erk1/2 signaling pathways in mesenchymal stem cells. PLoS One, 2014, 9(1):e85808.
3.	Huang YC, Yang ZM, Jiang NG, et al. Characterization of MSCs from human placental decidua basalis in hypoxia and serum deprivation. Cell Biology International, 2010, 34(3):237-243.
4.	Jin J, Wang J, Huang J, et al. Transplantation of human placentaderived mesenchymal stem cells in a silk fibroin/hydroxyapatite scaffold improves bone repair in rabbits. Journal of Bioscience and Bioengineering, 2014, 118(5):593-598.
5.	Dos Santos F, Andrade PZ, Boura JS, et al. Ex vivo expansion of human mesenchymal stem cells:A more effective cell proliferation kinetics and metabolism under hypoxia. J Cell Physiol, 2010, 223(1):27-35.
6.	Hung SP, Ho JH, Shih YR, et al. Hypoxia promotes proliferation and osteogenic differentiation potentials of human mesenchymal stem cells. J Orthop Res, 2012, 30(2):260-266.
7.	Hung SC. Effects of hypoxic culture on bone marrow mesenchymal stem cells:from bench to bedside. Formosan Journal of Surgery, 2013, 46:35-38.
8.	Huang YC, Yang ZM, Chen XH, et al. Isolation of mesenchymal stem cells from human placental decidua basalis and resistance to hypoxia and serum deprivation. Stem Cell Rev, 2009, 5(3):247-255.
9.	黄永灿, 陈晓禾, 王佳, 等. 低氧对胎盘基蜕膜间充质干细胞增殖、凋亡和血管内皮细胞生长因子表达的影响. 生理学报, 2008, 60(6):783-789.
10.	Drela K, Sarnowska A, Siedlecka P, et al. Low oxygen atmosphere facilitates proliferation and maintains undifferentiated state of umbilical cord mesenchymal stem cells in an hypoxia inducible factor-dependent manner. Cytotherapy, 2014, 16(7):881-892.
11.	Martin-Rendon E, Hale SJ, Ryan D, et al. Transcriptional profiling of human cord blood CD133+ and cultured bone marrow mesenchymal stem cells in response to hypoxia. Stem Cells, 2007, 25(4):1003-1012.
12.	Dionigi B, Ahmed A, Pennington EC, et al. A comparative analysis of human mesenchymal stem cell response to hypoxia in vitro:Implications to translational strategies. J Pediatr Surg, 2014, 49(6):915-918.
13.	Hass R, Kasper C, Böhm S, et al. Different populations and sources of human mesenchymal stem cells (MSC):A comparison of adult and neonatal tissue-derived MSC. Cell Commun Signal, 2011, 9:12.
14.	Lee Y, Jung J, Cho KJ, et al. Increased SCF/c-kit by hypoxia promotes autophagy of human placental chorionic plate-derived mesenchymal stem cells via regulating the phosphorylation of mTOR. J Cell Biochem, 2013, 114(1):79-88.
15.	陈亭, 周燕, 张治萍, 等. 间充质干细胞在低氧环境下的增殖、代谢与成骨分化:胎盘羊膜及骨髓来源间充质干细胞的对比. 中国组织工程研究与临床康复, 2010, 14(6):957-961.
16.	王佳, 陈晓禾, 黄永灿, 等. 缺氧对hBMSCs和胎盘来源MSCs增殖的影响. 中国修复重建外科杂志, 2009, 23(2):136-139.
17.	Bantubungi K, Blum D, Cuvelier L, et al. Stem cell factor and mesenchymal and neural stem cell transplantation in a rat model of huntington's disease. Mol Cell Neurosci, 2008, 37(3):454-470.
18.	廖凤玲, 陈日玲, 姜杉, 等. Notch信号通路对VEGF促大鼠间充质干细胞增殖的作用. 中国实验血液学杂志, 2014, 22(4):1068-1071.
19.	Wang L, Hu X, Zhu W, et al. Increased leptin by hypoxicpreconditioning promotes autophagy of mesenchymal stem cells and protects them from apoptosis. Sci China Life Sci, 2014, 57(2):171-180.
20.	Zepeda AB, Pessoa A Jr, Castillo RL, et al. Cellular and molecular mechanisms in the hypoxic tissue:role of HIF-1 and ROS. Cell Biochem Funct, 2013, 31(6):451-459.
21.	Chen J, Shehadah A, Pal A, et al. Neuroprotective effect of human placenta-derived cell treatment of stroke in rats. Cell Transplant, 2013, 22(5):871-879.
22.	Kong P, Xie X, Li F, et al. Placenta mesenchymal stem cell accelerates wound healing by enhancing angiogenesis in diabetic Goto-kakizaki (GK) rats. Biochem Biophys Res Commun, 2013, 438(2):410-419.
23.	Greijer AE, van der Wall E. The role of hypoxia inducible factor 1(HIF-1) in hypoxia induced apoptosis. J Clin Pathol, 2004, 57(10):1009-1014.
24.	Baumgartner L, Arnhold S, Brixius K, et al. Human mesenchymal stem cells:Influence of oxygen pressure on proliferation and chondrogenic differentiation in fibrin glue in vitro. J Biomed Mater Res A, 2010, 93(3):930-940.
25.	Lee HH, Chang CC, Shieh MJ, et al. Hypoxia enhances chondrogenesis and prevents terminal differentiation through pi3k/akt/foxo dependent anti-apoptotic effect. Sci Rep, 2013, 3:2683.
26.	Shang J, Liu H, Li J, et al. Roles of hypoxia during the chondrogenic differentiation of mesenchymal stem cells. Curr Stem Cell Res Ther, 2014, 9(2):141-147.
27.	Wang Y, Li J, Wang Y, et al. Effects of hypoxia on osteogenic differentiation of rat bone marrow mesenchymal stem cells. Mol Cell Biochem, 2012, 362(1-2):25-33.
28.	Xu N, Liu H, Qu F, et al. Hypoxia inhibits the differentiation of mesenchymal stem cells into osteoblasts by activation of notch signaling. Exp Mol Pathol, 2013, 94(1):33-39.
29.	Huang YC, Zhu HM, Cai JQ, et al. Hypoxia inhibits the spontaneous calcification of bone marrow-derived mesenchymal stem cells. J Cell Biochem, 2012, 113(4):1407-1415.
30.	Hsu SH, Chen CT, Wei YH. Inhibitory effects of hypoxia on metabolic switch and osteogenic differentiation of human mesenchymal stem cells. Stem Cells, 2013, 31(12):2779-2788.
31.	Huang J, Deng F, Wang L, et al. Hypoxia induces osteogenesisrelated activities and expression of core binding factor alpha1 in mesenchymal stem cells. Tohoku J Exp Med, 2011, 224(1):7-12.
32.	Wagegg M, Gaber T, Lohanatha FL, et al. Hypoxia promotes osteogenesis but suppresses adipogenesis of human mesenchymal stromal cells in a hypoxia-inducible factor-1 dependent manner. PLoS One, 2012, 7(9):e46483.
33.	Grayson WL, Zhao F, Bunnell B, et al. Hypoxia enhances proliferation and tissue formation of human mesenchymal stem cells. Biochem Biophysical Res Commun, 2007, 358(3):948-953.
34.	Chang CP, Chio CC, Cheong CU, et al. Hypoxic preconditioning enhances the therapeutic potential of the secretome from cultured human mesenchymal stem cells in experimental traumatic brain injury. Clin Sci (London), 2013, 124(3):165-176.
35.	唐军, 徐斌, 刘毅. 低氧对人脐带间充质干细胞成脂肪分化的影响. 中国美容医学, 2011, 20(7):1100-1102.
36.	Lönne M, Lavrentieva A, Walter JG, et al. Analysis of oxygendependent cytokine expression in human mesenchymal stem cells derived from umbilical cord. Cell and Tissue Research, 2013, 353(1):117-122.
37.	Zhang HC, Liu XB, Huang S, et al. Microvesicles derived from human umbilical cord mesenchymal stem cells stimulated by hypoxia promote angiogenesis both in vitro and in vivo. Stem Cells and Dev, 2012, 21(18):3289-3297.
38.	Wysoczynski M, Ratajczak MZ. Lung cancer secreted microvesicles:underappreciated modulators of microenvironment in expanding tumors. Int J Cancer, 2009, 125(7):1595-1603.
39.	Kinnaird T, Stabile E, Burnett MS, et al. Local delivery of marrowderived stromal cells augments collateral perfusion through paracrine mechanisms. Circulation, 2004, 109(12):1543-1549.
40.	Zhao JJ, Liu XC, Kong F, et al. Bone marrow mesenchymal stem cells improve myocardial function in a swine model of acute myocardial infarction. Mol Med Rep, 2014, 10(3):1448-1454.
41.	Sabry MM, Elkalawy SA, Abo-Elnour RK, et al. Histolgical and immunohistochemical study on the effect of stem cell therapy on bleomycin induced pulmonary fibrosis in albino rat. Int J Stem Cells, 2014, 7(1):33-42.
42.	Donega V, Nijboer CH, van Tilborg G, et al. Intranasally administered mesenchymal stem cells promote a regenerative niche for repair of neonatal ischemic brain injury. Experimental Neurology, 2014, (261):53-64.
43.	Makhoul G, Chiu RC, Cecere R. Placental mesenchymal stem cells:a unique source for cellular cardiomyoplasty. Ann Thorac Surg, 2013, 95(5):1827-1833.
44.	Zhang Y, Xia Y, Ni S, et al. Transplantation of umbilical cord mesenchymal stem cells alleviates pneumonitis of mrl/lpr mice. J Thoracic Dis, 2014, 6(2):109-117.
45.	Zhao FY, Qu Y, Liu H, et al. Umbilical cord blood mesenchymal stem cells co-modified by TERT and BDNF:A novel neuroprotective therapy for neonatal hypoxic-ischemic brain damage. International Journal of Developmental Neuroscience, 2014, 38:147-154.
46.	López Y, Lutjemeier B, Seshareddy K, et al. Wharton's jelly or bone marrow mesenchymal stromal cells improve cardiac function following myocardial infarction for more than 32 weeks in a rat model:a preliminary report. Curr Stem Cell Res Ther, 2013, 8(1):46-59.
47.	Kim SW, Zhang HZ, Guo L, et al. Amniotic mesenchymal stem cells enhance wound healing in diabetic nod/scid mice through high angiogenic and engraftment capabilities. PLoS ONE, 2012, 7(7):e41105.
48.	Nakamura Y, Ishikawa H, Kawai K, et al. Enhanced wound healing by topical administration of mesenchymal stem cells transfected with stromal cell-derived factor-1. Biomaterials, 2013, 34(37):9393-9400.
49.	Phillips AW, Johnston MV, Fatemi A. The potential for cell-based therapy in perinatal brain injuries. Transl Stroke Res, 2013, 4(2):137-148.
50.	王立维, 赵渝, 黄旭, 等. 氧体积分数变化与大鼠骨髓间充质干细胞的增殖及迁移. 中国组织工程研究, 2012, 16(19):3442-3446.
51.	Saller MM, Prall WC, Docheva D, et al. Increased stemness and migration of human mesenchymal stem cells in hypoxia is associated with altered integrin expression. Biochem Biophys Res Commun, 2012, 423(2):379-385.
52.	Wang Z, Moran E, Ding L, et al. PPARα regulates mobilization and homing of endothelial progenitor cells through the HIF-1α/SDF-1 pathway. Invest Ophthalmol Vis Sci, 2014, 55(6):3820-3832.
53.	Brooke G, Tong H, Levesque JP, et al. Molecular trafficking mechanisms of multipotent mesenchymal stem cells derived from human bone marrow and placenta. Stem Cells Dev, 2008, 17(5):929-940.

1. Rylova JV, Andreeva ER, Gogvadze VG, et al. Etoposide and hypoxia do not activate apoptosis of multipotent mesenchymal stromal cells in vitro. Bull Exp Biol Med, 2012, 154(1):141-144.
2. ou M, Cui J, Liu J, et al. Angiopoietin-like 4 confers resistance to hypoxia/serum deprivation-induced apoptosis through pi3k/akt and erk1/2 signaling pathways in mesenchymal stem cells. PLoS One, 2014, 9(1):e85808.
3. Huang YC, Yang ZM, Jiang NG, et al. Characterization of MSCs from human placental decidua basalis in hypoxia and serum deprivation. Cell Biology International, 2010, 34(3):237-243.
4. Jin J, Wang J, Huang J, et al. Transplantation of human placentaderived mesenchymal stem cells in a silk fibroin/hydroxyapatite scaffold improves bone repair in rabbits. Journal of Bioscience and Bioengineering, 2014, 118(5):593-598.
5. Dos Santos F, Andrade PZ, Boura JS, et al. Ex vivo expansion of human mesenchymal stem cells:A more effective cell proliferation kinetics and metabolism under hypoxia. J Cell Physiol, 2010, 223(1):27-35.
6. Hung SP, Ho JH, Shih YR, et al. Hypoxia promotes proliferation and osteogenic differentiation potentials of human mesenchymal stem cells. J Orthop Res, 2012, 30(2):260-266.
7. Hung SC. Effects of hypoxic culture on bone marrow mesenchymal stem cells:from bench to bedside. Formosan Journal of Surgery, 2013, 46:35-38.
8. Huang YC, Yang ZM, Chen XH, et al. Isolation of mesenchymal stem cells from human placental decidua basalis and resistance to hypoxia and serum deprivation. Stem Cell Rev, 2009, 5(3):247-255.
9. 黄永灿, 陈晓禾, 王佳, 等. 低氧对胎盘基蜕膜间充质干细胞增殖、凋亡和血管内皮细胞生长因子表达的影响. 生理学报, 2008, 60(6):783-789.
10. Drela K, Sarnowska A, Siedlecka P, et al. Low oxygen atmosphere facilitates proliferation and maintains undifferentiated state of umbilical cord mesenchymal stem cells in an hypoxia inducible factor-dependent manner. Cytotherapy, 2014, 16(7):881-892.
11. Martin-Rendon E, Hale SJ, Ryan D, et al. Transcriptional profiling of human cord blood CD133+ and cultured bone marrow mesenchymal stem cells in response to hypoxia. Stem Cells, 2007, 25(4):1003-1012.
12. Dionigi B, Ahmed A, Pennington EC, et al. A comparative analysis of human mesenchymal stem cell response to hypoxia in vitro:Implications to translational strategies. J Pediatr Surg, 2014, 49(6):915-918.
13. Hass R, Kasper C, Böhm S, et al. Different populations and sources of human mesenchymal stem cells (MSC):A comparison of adult and neonatal tissue-derived MSC. Cell Commun Signal, 2011, 9:12.
14. Lee Y, Jung J, Cho KJ, et al. Increased SCF/c-kit by hypoxia promotes autophagy of human placental chorionic plate-derived mesenchymal stem cells via regulating the phosphorylation of mTOR. J Cell Biochem, 2013, 114(1):79-88.
15. 陈亭, 周燕, 张治萍, 等. 间充质干细胞在低氧环境下的增殖、代谢与成骨分化:胎盘羊膜及骨髓来源间充质干细胞的对比. 中国组织工程研究与临床康复, 2010, 14(6):957-961.
16. 王佳, 陈晓禾, 黄永灿, 等. 缺氧对hBMSCs和胎盘来源MSCs增殖的影响. 中国修复重建外科杂志, 2009, 23(2):136-139.
17. Bantubungi K, Blum D, Cuvelier L, et al. Stem cell factor and mesenchymal and neural stem cell transplantation in a rat model of huntington's disease. Mol Cell Neurosci, 2008, 37(3):454-470.
18. 廖凤玲, 陈日玲, 姜杉, 等. Notch信号通路对VEGF促大鼠间充质干细胞增殖的作用. 中国实验血液学杂志, 2014, 22(4):1068-1071.
19. Wang L, Hu X, Zhu W, et al. Increased leptin by hypoxicpreconditioning promotes autophagy of mesenchymal stem cells and protects them from apoptosis. Sci China Life Sci, 2014, 57(2):171-180.
20. Zepeda AB, Pessoa A Jr, Castillo RL, et al. Cellular and molecular mechanisms in the hypoxic tissue:role of HIF-1 and ROS. Cell Biochem Funct, 2013, 31(6):451-459.
21. Chen J, Shehadah A, Pal A, et al. Neuroprotective effect of human placenta-derived cell treatment of stroke in rats. Cell Transplant, 2013, 22(5):871-879.
22. Kong P, Xie X, Li F, et al. Placenta mesenchymal stem cell accelerates wound healing by enhancing angiogenesis in diabetic Goto-kakizaki (GK) rats. Biochem Biophys Res Commun, 2013, 438(2):410-419.
23. Greijer AE, van der Wall E. The role of hypoxia inducible factor 1(HIF-1) in hypoxia induced apoptosis. J Clin Pathol, 2004, 57(10):1009-1014.
24. Baumgartner L, Arnhold S, Brixius K, et al. Human mesenchymal stem cells:Influence of oxygen pressure on proliferation and chondrogenic differentiation in fibrin glue in vitro. J Biomed Mater Res A, 2010, 93(3):930-940.
25. Lee HH, Chang CC, Shieh MJ, et al. Hypoxia enhances chondrogenesis and prevents terminal differentiation through pi3k/akt/foxo dependent anti-apoptotic effect. Sci Rep, 2013, 3:2683.
26. Shang J, Liu H, Li J, et al. Roles of hypoxia during the chondrogenic differentiation of mesenchymal stem cells. Curr Stem Cell Res Ther, 2014, 9(2):141-147.
27. Wang Y, Li J, Wang Y, et al. Effects of hypoxia on osteogenic differentiation of rat bone marrow mesenchymal stem cells. Mol Cell Biochem, 2012, 362(1-2):25-33.
28. Xu N, Liu H, Qu F, et al. Hypoxia inhibits the differentiation of mesenchymal stem cells into osteoblasts by activation of notch signaling. Exp Mol Pathol, 2013, 94(1):33-39.
29. Huang YC, Zhu HM, Cai JQ, et al. Hypoxia inhibits the spontaneous calcification of bone marrow-derived mesenchymal stem cells. J Cell Biochem, 2012, 113(4):1407-1415.
30. Hsu SH, Chen CT, Wei YH. Inhibitory effects of hypoxia on metabolic switch and osteogenic differentiation of human mesenchymal stem cells. Stem Cells, 2013, 31(12):2779-2788.
31. Huang J, Deng F, Wang L, et al. Hypoxia induces osteogenesisrelated activities and expression of core binding factor alpha1 in mesenchymal stem cells. Tohoku J Exp Med, 2011, 224(1):7-12.
32. Wagegg M, Gaber T, Lohanatha FL, et al. Hypoxia promotes osteogenesis but suppresses adipogenesis of human mesenchymal stromal cells in a hypoxia-inducible factor-1 dependent manner. PLoS One, 2012, 7(9):e46483.
33. Grayson WL, Zhao F, Bunnell B, et al. Hypoxia enhances proliferation and tissue formation of human mesenchymal stem cells. Biochem Biophysical Res Commun, 2007, 358(3):948-953.
34. Chang CP, Chio CC, Cheong CU, et al. Hypoxic preconditioning enhances the therapeutic potential of the secretome from cultured human mesenchymal stem cells in experimental traumatic brain injury. Clin Sci (London), 2013, 124(3):165-176.
35. 唐军, 徐斌, 刘毅. 低氧对人脐带间充质干细胞成脂肪分化的影响. 中国美容医学, 2011, 20(7):1100-1102.
36. Lönne M, Lavrentieva A, Walter JG, et al. Analysis of oxygendependent cytokine expression in human mesenchymal stem cells derived from umbilical cord. Cell and Tissue Research, 2013, 353(1):117-122.
37. Zhang HC, Liu XB, Huang S, et al. Microvesicles derived from human umbilical cord mesenchymal stem cells stimulated by hypoxia promote angiogenesis both in vitro and in vivo. Stem Cells and Dev, 2012, 21(18):3289-3297.
38. Wysoczynski M, Ratajczak MZ. Lung cancer secreted microvesicles:underappreciated modulators of microenvironment in expanding tumors. Int J Cancer, 2009, 125(7):1595-1603.
39. Kinnaird T, Stabile E, Burnett MS, et al. Local delivery of marrowderived stromal cells augments collateral perfusion through paracrine mechanisms. Circulation, 2004, 109(12):1543-1549.
40. Zhao JJ, Liu XC, Kong F, et al. Bone marrow mesenchymal stem cells improve myocardial function in a swine model of acute myocardial infarction. Mol Med Rep, 2014, 10(3):1448-1454.
41. Sabry MM, Elkalawy SA, Abo-Elnour RK, et al. Histolgical and immunohistochemical study on the effect of stem cell therapy on bleomycin induced pulmonary fibrosis in albino rat. Int J Stem Cells, 2014, 7(1):33-42.
42. Donega V, Nijboer CH, van Tilborg G, et al. Intranasally administered mesenchymal stem cells promote a regenerative niche for repair of neonatal ischemic brain injury. Experimental Neurology, 2014, (261):53-64.
43. Makhoul G, Chiu RC, Cecere R. Placental mesenchymal stem cells:a unique source for cellular cardiomyoplasty. Ann Thorac Surg, 2013, 95(5):1827-1833.
44. Zhang Y, Xia Y, Ni S, et al. Transplantation of umbilical cord mesenchymal stem cells alleviates pneumonitis of mrl/lpr mice. J Thoracic Dis, 2014, 6(2):109-117.
45. Zhao FY, Qu Y, Liu H, et al. Umbilical cord blood mesenchymal stem cells co-modified by TERT and BDNF:A novel neuroprotective therapy for neonatal hypoxic-ischemic brain damage. International Journal of Developmental Neuroscience, 2014, 38:147-154.
46. López Y, Lutjemeier B, Seshareddy K, et al. Wharton's jelly or bone marrow mesenchymal stromal cells improve cardiac function following myocardial infarction for more than 32 weeks in a rat model:a preliminary report. Curr Stem Cell Res Ther, 2013, 8(1):46-59.
47. Kim SW, Zhang HZ, Guo L, et al. Amniotic mesenchymal stem cells enhance wound healing in diabetic nod/scid mice through high angiogenic and engraftment capabilities. PLoS ONE, 2012, 7(7):e41105.
48. Nakamura Y, Ishikawa H, Kawai K, et al. Enhanced wound healing by topical administration of mesenchymal stem cells transfected with stromal cell-derived factor-1. Biomaterials, 2013, 34(37):9393-9400.
49. Phillips AW, Johnston MV, Fatemi A. The potential for cell-based therapy in perinatal brain injuries. Transl Stroke Res, 2013, 4(2):137-148.
50. 王立维, 赵渝, 黄旭, 等. 氧体积分数变化与大鼠骨髓间充质干细胞的增殖及迁移. 中国组织工程研究, 2012, 16(19):3442-3446.
51. Saller MM, Prall WC, Docheva D, et al. Increased stemness and migration of human mesenchymal stem cells in hypoxia is associated with altered integrin expression. Biochem Biophys Res Commun, 2012, 423(2):379-385.
52. Wang Z, Moran E, Ding L, et al. PPARα regulates mobilization and homing of endothelial progenitor cells through the HIF-1α/SDF-1 pathway. Invest Ophthalmol Vis Sci, 2014, 55(6):3820-3832.
53. Brooke G, Tong H, Levesque JP, et al. Molecular trafficking mechanisms of multipotent mesenchymal stem cells derived from human bone marrow and placenta. Stem Cells Dev, 2008, 17(5):929-940.

Chinese Journal of Reparative and Reconstructive Surgery

COMPARISON OF BIOLOGICAL DIFFERENCE BETWEEN BONE MARROW AND PLACENTA-DERIVED MESENCHIMAL STEM CELLS IN HYPOXIA

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