Research progress on effects of high glucose microenvironment on biological activity of adipose-derived stem cells_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

ZHENG Yongjian , ZHANG Fengling , DENG Chengliang ,  WEI Zairong

Department of Burn and Plastic Surgery, Affiliated Hospital of Zunyi Medical University, Zunyi Guizhou, 563000, P.R.China;

Corresponding author：

WEI Zairong, Email: zairongwei@sina.com

Keywords：

Diabetes; glycosylation; high glucose microenvironment; adipose-derived stem cells

DOI：

10.7507/1002-1892.202003094

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To summarize the research progress of the effects of high glucose microenvironment on the biological activity of adipose-derived stem cells (ADSCs).Methods The literature on the high glucose microenvironment and ADSCs at home and abroad in recent years was reviewed, and the effects of high glucose microenvironment on the general characteristics, differentiation potential, angiogenesis, and nerve regeneration of ADSCs were summarized.Results The accumulation of advanced glycosylation end products (AGEs) in the high glucose microenvironment led to changes in the biological activities of ADSCs through various pathways, including cell surface markers, proliferation, migration, multi-lineage differentiation, secretory function, and tissue repair ability. The ability of ADSCs to promote angiogenesis and nerve regeneration in high glucose microenvironment is still controversial.Conclusion High glucose microenvironment can affect the biological activity of ADSCs, and the effect and mechanism of ADSCs on angiogenesis and nerve regeneration in high glucose microenvironment need to be further studied.

Citation： ZHENG Yongjian, ZHANG Fengling, DENG Chengliang, WEI Zairong. Research progress on effects of high glucose microenvironment on biological activity of adipose-derived stem cells. Chinese Journal of Reparative and Reconstructive Surgery, 2020, 34(12): 1602-1606. doi: 10.7507/1002-1892.202003094 Copy

1.	Francis SL, Serena D, Carmine O, et al. Adipose-derived mesenchymal stem cells in the use of cartilage tissue engineering: the need for a rapid isolation procedure. Stem Cells International, 2018, 2018: 1-9.
2.	Urdzíková LM, Růžička J, LaBagnara M, et al. Human mesenchymal stem cells modulate inflammatory cytokines after spinal cord injury in rat. Int J Mol Sci, 2014, 15(7): 11275-11293.
3.	Arboleda D, Forostyak S, Jendelova P, et al. Transplantation of predifferentiated adipose-derived stromal cells for the treatment of spinal cord injury. Cell Mol Neurobiol, 2011, 31(7): 1113-1122.
4.	Zografou A, Papadopoulos O, Tsigris C, et al. Autologous transplantation of adipose-derived stem cells enhances skin graft survival and wound healing in diabetic rats. Ann Plast Surg, 2013, 71(2): 225-232.
5.	邓呈亮, 冯晶玮, 鲁峰. 脂肪来源干细胞促进难愈性创面愈合研究进展. 中华整形外科杂志, 2017, 33(6): 477-480.
6.	Bertani N, Malatesta P, Volpi G, et al. Neurogenic potential of human mesenchymal stem cells revisited: analysis by immunostaining, time-lapse video and microarray. J Cell Sci, 2005, 118(Pt 17): 3925-3936.
7.	Pittenger MF, Martin BJ. Mesenchymal stem cells and their potential as cardiac therapeutics. Circ Res, 2004, 95(1): 9-20.
8.	Tomlinson DR, Gardiner NJ. Glucose Neurotoxicity. Nat Rev Neurosci, 2008, 9(1): 36-45.
9.	许晓茹, 方开秀, 王力峰, 等. 2 型糖尿病大鼠脂肪干细胞体外成骨能力的研究. 牙体牙髓牙周病学杂志, 2016, 26(4): 202-207.
10.	Chen XJ, Wu WJ, Zhou Q, et al. Advanced glycation end-products induce oxidative stress through the Sirt1/Nrf2 axis by interacting with the receptor of AGEs under diabetic conditions. J Cell Biochem, 2019, 120(2): 2159-2170.
11.	Cheng NC, Hsieh TY, Lai HS, et al. High glucose-induced reactive oxygen species generation promotes stemness in human adipose-derived stem cells. Cytotherapy, 2016, 18(3): 371-383.
12.	Stolzing A, Coleman N, Scutt A. Glucose-induced replicative senescence in mesenchymal stem cells. Rejuvenation Research, 2006, 9(1): 31-35.
13.	许言文, 李加辅, 朱瑞祥, 等. 糖尿病慢性溃疡患者与非糖尿病者脂肪干细胞形态及增殖能力的差异. 中华医学美学美容杂志, 2016, 22(2): 105-108.
14.	El-Ftesi S, Chang EI, Longaker MT, et al. Aging and diabetes impair the neovascular potential of adipose-derived stromal cells. Plast Reconstr Surg, 2009, 123(2): 475-485.
15.	Cianfarani F, Toietta G, Di Rocco G, et al. Diabetes impairs adipose tissue-derived stem cell function and efficiency in promoting wound healing. Wound Repair Regen, 2013, 21(4): 545-553.
16.	Cramer C, Freisinger E, Jones RK, et al. Persistent high glucose concentrations alter the regenerative potential of mesenchymal stem cells. Stem Cells Dev, 2010, 19(12): 1875-1884.
17.	Ramia N, Kreydiyyeh SI. TNF-alpha reduces the Na+/K+ ATPase activity in LLC-PK1 cells by activating caspases and JNK and inhibiting NF-kappaB. Cell Biol Int, 2010, 34(6): 607-613.
18.	Zhang D, Lu H, Chen Z, et al. High glucose induces the aging of mesenchymal stem cells via Akt/mTOR signaling. Mol Med Rep, 2017, 16(2): 1685-1690.
19.	Bufalo MC, Almeida ME, Franca IA, et al. Advanced glycation endproducts produced by in vitro glycation of type Ⅰ collagen modulate the functional and secretory behavior of dorsal root ganglion cells cultivated in two-dimensional system. Exp Cell Res, 2019, 382(2): 111475.
20.	Alikhani M, Maclellan CM, Raptis M, et al. Advanced glycation end products induce apoptosis in fibroblasts through activation of ROS, MAP kinases, and the FOXO1 transcription factor. Am J Physiol Cell Physiol, 2006, 292(2): C850-C856.
21.	Davies LC, Alm JJ, Heldring N, et al. Type 1 diabetes mellitus donor mesenchymal stromal cells exhibit comparable potency to healthy controls in vitro. Stem Cells Transl Med, 2016, 5(11): 1485-1495.
22.	金鑫, 王宝泉, 童伟, 等. 糖基化改装人脂肪来源干细胞促进其骨髓归巢及成骨的研究. 中华老年骨科与康复电子杂志, 2018, 4(5): 287-295.
23.	Shin L, Peterson DA. Impaired therapeutic capacity of autologous stem cells in a model of type 2 diabetes. Stem Cells Transl Med, 2012, 1(2): 125-135.
24.	Baer PC, Geiger H. Adipose-derived mesenchymal stromal/stem cells: tissue localization, characterization, and heterogeneity. Stem Cells Int, 2012, 2012: 812693.
25.	Liu MH, Li Y, Han L, et al. Adipose-derived stem cells were impaired in testricting CD4+ T cell proliferation and polarization in type 2 diabetic ApoE –/– mouse. Mol Immunol, 2017, 87: 152-160.
26.	姚远镇, 邓呈亮, 王波. 糖尿病对脂肪源性间充质干细胞生物学功能影响的研究进展. 中华烧伤杂志, 2018, 34(9): 653-656.
27.	Kuo YR, Wang CT, Cheng JT, et al. Adipose-derived stem cells accelerate diabetic wound healing through the induction of autocrine and paracrine effects. Cell Transplant, 2016, 25(1): 71-81.
28.	Chuah YK, Basir R, Talib H, et al. Receptor for advanced glycation end products and its involvement in inflammatory diseases. Int J Inflam, 2013, 2013: 403460.
29.	Keats E, Khan ZA. Unique responses of stem cell-derived vascular endothelial and mesenchymal cells to high levels of glucose. PLoS One, 2012, 7(6): e38752.
30.	Trinh NT, Yamashita T, Ohneda K, et al. Increased expression of EGR-1 in diabetic human adipose tissue-derived mesenchymal stem cells reduces their wound healing capacity. Stem Cells Dev, 2016, 25(10): 760-773.
31.	Zhang M, Yong L, Rao PC, et al. Blockade of receptors of advanced glycation end products ameliorates diabetic osteogenesis of adipose-derived stem cells through DNA methylation and Wnt signalling pathway. Cell Prolif, 2018, 51: e12471.
32.	Li YM, Schilling T, Benisch P, et al. Effects of high glucose on mesenchymal stem cell proliferation and differentiation. Biochem Biophys Res Commun, 2007, 363(1): 209-215.
33.	杨卉馨, 黄小会, 董晓惠, 等. 高糖环境对小鼠成骨前体细胞及脂肪干细胞成骨分化的影响. 解放军医学院学报, 2019, 40(5): 449-453, 469.
34.	García-Hernández A, Arzate H, Gil-Chavarría I, et al. High glucose concentrations alter the biomineralization process in human osteoblastic cells. Bone, 2012, 50(1): 276-288.
35.	Sawangmake C, Pavasant P, Chansiripornchai P, et al. High glucose condition suppresses neurosphere formation by human periodontal ligament-derived mesenchymal stem cells. J Cell Biochem, 2014, 115(5): 928-939.
36.	Hiraiwa H, Sakai T, Mitsuyama H, et al. Inflammatory effect of advanced glycation end products on human meniscal cells from osteoarthritic knees. Inflamm Res, 2011, 60(11): 1039-1048.
37.	Tareck R, Stéphanie L. High glucose level impairs human mature bone marrow adipocyte function through increased ROS production. Front Endocrinol (Lausanne), 2019, 10: 607.
38.	Rennert RC, Sorkin M, Januszyk M, et al. Diabetes impairs the angiogenic potential of adipose-derived stem cells by selectively depleting cellular subpopulations. Stem Cell Res Ther, 2014, 5(3): 79.
39.	Harris LJ, Zhang P, Abdollahi H, et al. Availability of adipose-derived stem cells in patients undergoing vascular surgical procedures. J Surg Res, 2010, 163(2): e105-112.
40.	伍锋, 贺治青, 纪睿圳, 等. 晚期糖基化终产物对脂肪干细胞功能、血管新生能力的影响及丹红注射液保护作用的实验研究. 中国中西医结合杂志, 2014, 34(7): 839-845.
41.	王哲, 刘晓玉, 张殿宝, 等. 晚期糖基化终产物对人脂肪间充质干细胞功能影响的体外研究. 中国病理生理杂志, 2014, 30(5): 897-901.
42.	Gu JH, Lee JS, Kim DW, et al. Neovascular potential of adipose-derived stromal cells (ASCs) from diabetic patients. Wound Repair Regen, 2012, 20(2): 243-252.
43.	Świderska E, Podolska M, Strycharz J, et al. Hyperglycemia changes expression of key adipogenesis markers (C/EBPα and PPARγ) and morphology of differentiating human visceral adipocytes. Nutrients, 2019, 11(8): 1835.
44.	Rubina K, Kalinina N, Efimenko A, et al. Adipose stromal cells stimulate angiogenesis via promoting progenitor cell differentiation, secretion of angiogenic factors, and enhancing vessel maturation. Tissue Eng Part A, 2009, 15(8): 2039-2050.
45.	Lafosse A, Dufeys C, Beauloye C, et al. Impact of hyperglycemia and low oxygen tension on adipose-derived stem cells compared with dermal fibroblasts and keratinocytes: importance for wound healing in type 2 diabetes. PLoS One, 2016, 11(12): e0168058.
46.	Policha A, Zhang P, Chang L, et al. Endothelial differentiation of diabetic adipose-derived stem cells. J Surg Res, 2014, 192(2): 656-663.
47.	Kim SM, Kim YH, Jun YJ, et al. The effect of diabetes on the wound healing potential of adipose-tissue derived stem cells. Int Wound J, 2016, 13 Suppl 1: 33-41.
48.	Napoli I, Noon LA, Ribeiro S, et al. A central role for the ERK-signaling pathway in controlling Schwann cell plasticity and peripheral nerve regeneration in vivo. Neuron, 2012, 73(4): 729-742.
49.	Hsu MN, Liao HT, Truong VA, et al. CRISPR-based activation of endogenous neurotrophic genes in adipose stem cell sheets to stimulate peripheral nerve regeneration. Theranostics, 2019, 9(21): 6099-6111.
50.	Faroni A, Smith RJ, Lu L, et al. Human Schwann-like cells derived from adipose-derived mesenchymal stem cells rapidly de-differentiate in the absence of stimulating medium. Eur J Neurosci, 2016, 43(3): 417-430.
51.	Kaewkhaw R, Scutt AM, Haycock JW. Anatomical site influences the differentiation of adipose-derived stem cells for Schwann-cell phenotype and function. Glia, 2011, 59(5): 734-749.
52.	Feldman EL, Nave KA, Jensen TS, et al. New horizons in diabetic neuropathy: mechanisms, bioenergetics, and pain. Neuron, 2017, 93(6): 1296-1313.
53.	Chen J, Li C, Liu W, et al. miRNA-155 silencing reduces sciatic nerve injury in diabetic peripheral neuropathy. J Mol Endocrinol, 2019, 63(3): 227-238.
54.	Han JW, Choi D, Lee MY, et al. Bone marrow-derived mesenchymal stem cells improve diabetic neuropathy by direct modulation of both angiogenesis and myelination in peripheral nerves. Cell Transplant, 2016, 25(2): 313-326.
55.	贺治青. 晚期糖基化终产物诱导人脂肪来源干细胞功能紊乱的机制研究. 上海: 第二军医大学, 2009.
56.	Rojas DR, Tegeder I, Kuner R, et al. Hypoxia-inducible factor 1α protects peripheral sensory neurons from diabetic peripheral neuropathy by suppressing accumulation of reactive oxygen species. J Mol Med, 2018, 96(12): 1395-1405.
57.	Xiao S, Liu Z, Yao Y, et al. Diabetic human adipose-derived stem cells accelerate pressure ulcer healing by inducing angiogenesis and neurogenesis. Stem Cells Dev, 2019, 28(5): 319-328.

1. Francis SL, Serena D, Carmine O, et al. Adipose-derived mesenchymal stem cells in the use of cartilage tissue engineering: the need for a rapid isolation procedure. Stem Cells International, 2018, 2018: 1-9.
2. Urdzíková LM, Růžička J, LaBagnara M, et al. Human mesenchymal stem cells modulate inflammatory cytokines after spinal cord injury in rat. Int J Mol Sci, 2014, 15(7): 11275-11293.
3. Arboleda D, Forostyak S, Jendelova P, et al. Transplantation of predifferentiated adipose-derived stromal cells for the treatment of spinal cord injury. Cell Mol Neurobiol, 2011, 31(7): 1113-1122.
4. Zografou A, Papadopoulos O, Tsigris C, et al. Autologous transplantation of adipose-derived stem cells enhances skin graft survival and wound healing in diabetic rats. Ann Plast Surg, 2013, 71(2): 225-232.
5. 邓呈亮, 冯晶玮, 鲁峰. 脂肪来源干细胞促进难愈性创面愈合研究进展. 中华整形外科杂志, 2017, 33(6): 477-480.
6. Bertani N, Malatesta P, Volpi G, et al. Neurogenic potential of human mesenchymal stem cells revisited: analysis by immunostaining, time-lapse video and microarray. J Cell Sci, 2005, 118(Pt 17): 3925-3936.
7. Pittenger MF, Martin BJ. Mesenchymal stem cells and their potential as cardiac therapeutics. Circ Res, 2004, 95(1): 9-20.
8. Tomlinson DR, Gardiner NJ. Glucose Neurotoxicity. Nat Rev Neurosci, 2008, 9(1): 36-45.
9. 许晓茹, 方开秀, 王力峰, 等. 2 型糖尿病大鼠脂肪干细胞体外成骨能力的研究. 牙体牙髓牙周病学杂志, 2016, 26(4): 202-207.
10. Chen XJ, Wu WJ, Zhou Q, et al. Advanced glycation end-products induce oxidative stress through the Sirt1/Nrf2 axis by interacting with the receptor of AGEs under diabetic conditions. J Cell Biochem, 2019, 120(2): 2159-2170.
11. Cheng NC, Hsieh TY, Lai HS, et al. High glucose-induced reactive oxygen species generation promotes stemness in human adipose-derived stem cells. Cytotherapy, 2016, 18(3): 371-383.
12. Stolzing A, Coleman N, Scutt A. Glucose-induced replicative senescence in mesenchymal stem cells. Rejuvenation Research, 2006, 9(1): 31-35.
13. 许言文, 李加辅, 朱瑞祥, 等. 糖尿病慢性溃疡患者与非糖尿病者脂肪干细胞形态及增殖能力的差异. 中华医学美学美容杂志, 2016, 22(2): 105-108.
14. El-Ftesi S, Chang EI, Longaker MT, et al. Aging and diabetes impair the neovascular potential of adipose-derived stromal cells. Plast Reconstr Surg, 2009, 123(2): 475-485.
15. Cianfarani F, Toietta G, Di Rocco G, et al. Diabetes impairs adipose tissue-derived stem cell function and efficiency in promoting wound healing. Wound Repair Regen, 2013, 21(4): 545-553.
16. Cramer C, Freisinger E, Jones RK, et al. Persistent high glucose concentrations alter the regenerative potential of mesenchymal stem cells. Stem Cells Dev, 2010, 19(12): 1875-1884.
17. Ramia N, Kreydiyyeh SI. TNF-alpha reduces the Na+/K+ ATPase activity in LLC-PK1 cells by activating caspases and JNK and inhibiting NF-kappaB. Cell Biol Int, 2010, 34(6): 607-613.
18. Zhang D, Lu H, Chen Z, et al. High glucose induces the aging of mesenchymal stem cells via Akt/mTOR signaling. Mol Med Rep, 2017, 16(2): 1685-1690.
19. Bufalo MC, Almeida ME, Franca IA, et al. Advanced glycation endproducts produced by in vitro glycation of type Ⅰ collagen modulate the functional and secretory behavior of dorsal root ganglion cells cultivated in two-dimensional system. Exp Cell Res, 2019, 382(2): 111475.
20. Alikhani M, Maclellan CM, Raptis M, et al. Advanced glycation end products induce apoptosis in fibroblasts through activation of ROS, MAP kinases, and the FOXO1 transcription factor. Am J Physiol Cell Physiol, 2006, 292(2): C850-C856.
21. Davies LC, Alm JJ, Heldring N, et al. Type 1 diabetes mellitus donor mesenchymal stromal cells exhibit comparable potency to healthy controls in vitro. Stem Cells Transl Med, 2016, 5(11): 1485-1495.
22. 金鑫, 王宝泉, 童伟, 等. 糖基化改装人脂肪来源干细胞促进其骨髓归巢及成骨的研究. 中华老年骨科与康复电子杂志, 2018, 4(5): 287-295.
23. Shin L, Peterson DA. Impaired therapeutic capacity of autologous stem cells in a model of type 2 diabetes. Stem Cells Transl Med, 2012, 1(2): 125-135.
24. Baer PC, Geiger H. Adipose-derived mesenchymal stromal/stem cells: tissue localization, characterization, and heterogeneity. Stem Cells Int, 2012, 2012: 812693.
25. Liu MH, Li Y, Han L, et al. Adipose-derived stem cells were impaired in testricting CD4+ T cell proliferation and polarization in type 2 diabetic ApoE –/– mouse. Mol Immunol, 2017, 87: 152-160.
26. 姚远镇, 邓呈亮, 王波. 糖尿病对脂肪源性间充质干细胞生物学功能影响的研究进展. 中华烧伤杂志, 2018, 34(9): 653-656.
27. Kuo YR, Wang CT, Cheng JT, et al. Adipose-derived stem cells accelerate diabetic wound healing through the induction of autocrine and paracrine effects. Cell Transplant, 2016, 25(1): 71-81.
28. Chuah YK, Basir R, Talib H, et al. Receptor for advanced glycation end products and its involvement in inflammatory diseases. Int J Inflam, 2013, 2013: 403460.
29. Keats E, Khan ZA. Unique responses of stem cell-derived vascular endothelial and mesenchymal cells to high levels of glucose. PLoS One, 2012, 7(6): e38752.
30. Trinh NT, Yamashita T, Ohneda K, et al. Increased expression of EGR-1 in diabetic human adipose tissue-derived mesenchymal stem cells reduces their wound healing capacity. Stem Cells Dev, 2016, 25(10): 760-773.
31. Zhang M, Yong L, Rao PC, et al. Blockade of receptors of advanced glycation end products ameliorates diabetic osteogenesis of adipose-derived stem cells through DNA methylation and Wnt signalling pathway. Cell Prolif, 2018, 51: e12471.
32. Li YM, Schilling T, Benisch P, et al. Effects of high glucose on mesenchymal stem cell proliferation and differentiation. Biochem Biophys Res Commun, 2007, 363(1): 209-215.
33. 杨卉馨, 黄小会, 董晓惠, 等. 高糖环境对小鼠成骨前体细胞及脂肪干细胞成骨分化的影响. 解放军医学院学报, 2019, 40(5): 449-453, 469.
34. García-Hernández A, Arzate H, Gil-Chavarría I, et al. High glucose concentrations alter the biomineralization process in human osteoblastic cells. Bone, 2012, 50(1): 276-288.
35. Sawangmake C, Pavasant P, Chansiripornchai P, et al. High glucose condition suppresses neurosphere formation by human periodontal ligament-derived mesenchymal stem cells. J Cell Biochem, 2014, 115(5): 928-939.
36. Hiraiwa H, Sakai T, Mitsuyama H, et al. Inflammatory effect of advanced glycation end products on human meniscal cells from osteoarthritic knees. Inflamm Res, 2011, 60(11): 1039-1048.
37. Tareck R, Stéphanie L. High glucose level impairs human mature bone marrow adipocyte function through increased ROS production. Front Endocrinol (Lausanne), 2019, 10: 607.
38. Rennert RC, Sorkin M, Januszyk M, et al. Diabetes impairs the angiogenic potential of adipose-derived stem cells by selectively depleting cellular subpopulations. Stem Cell Res Ther, 2014, 5(3): 79.
39. Harris LJ, Zhang P, Abdollahi H, et al. Availability of adipose-derived stem cells in patients undergoing vascular surgical procedures. J Surg Res, 2010, 163(2): e105-112.
40. 伍锋, 贺治青, 纪睿圳, 等. 晚期糖基化终产物对脂肪干细胞功能、血管新生能力的影响及丹红注射液保护作用的实验研究. 中国中西医结合杂志, 2014, 34(7): 839-845.
41. 王哲, 刘晓玉, 张殿宝, 等. 晚期糖基化终产物对人脂肪间充质干细胞功能影响的体外研究. 中国病理生理杂志, 2014, 30(5): 897-901.
42. Gu JH, Lee JS, Kim DW, et al. Neovascular potential of adipose-derived stromal cells (ASCs) from diabetic patients. Wound Repair Regen, 2012, 20(2): 243-252.
43. Świderska E, Podolska M, Strycharz J, et al. Hyperglycemia changes expression of key adipogenesis markers (C/EBPα and PPARγ) and morphology of differentiating human visceral adipocytes. Nutrients, 2019, 11(8): 1835.
44. Rubina K, Kalinina N, Efimenko A, et al. Adipose stromal cells stimulate angiogenesis via promoting progenitor cell differentiation, secretion of angiogenic factors, and enhancing vessel maturation. Tissue Eng Part A, 2009, 15(8): 2039-2050.
45. Lafosse A, Dufeys C, Beauloye C, et al. Impact of hyperglycemia and low oxygen tension on adipose-derived stem cells compared with dermal fibroblasts and keratinocytes: importance for wound healing in type 2 diabetes. PLoS One, 2016, 11(12): e0168058.
46. Policha A, Zhang P, Chang L, et al. Endothelial differentiation of diabetic adipose-derived stem cells. J Surg Res, 2014, 192(2): 656-663.
47. Kim SM, Kim YH, Jun YJ, et al. The effect of diabetes on the wound healing potential of adipose-tissue derived stem cells. Int Wound J, 2016, 13 Suppl 1: 33-41.
48. Napoli I, Noon LA, Ribeiro S, et al. A central role for the ERK-signaling pathway in controlling Schwann cell plasticity and peripheral nerve regeneration in vivo. Neuron, 2012, 73(4): 729-742.
49. Hsu MN, Liao HT, Truong VA, et al. CRISPR-based activation of endogenous neurotrophic genes in adipose stem cell sheets to stimulate peripheral nerve regeneration. Theranostics, 2019, 9(21): 6099-6111.
50. Faroni A, Smith RJ, Lu L, et al. Human Schwann-like cells derived from adipose-derived mesenchymal stem cells rapidly de-differentiate in the absence of stimulating medium. Eur J Neurosci, 2016, 43(3): 417-430.
51. Kaewkhaw R, Scutt AM, Haycock JW. Anatomical site influences the differentiation of adipose-derived stem cells for Schwann-cell phenotype and function. Glia, 2011, 59(5): 734-749.
52. Feldman EL, Nave KA, Jensen TS, et al. New horizons in diabetic neuropathy: mechanisms, bioenergetics, and pain. Neuron, 2017, 93(6): 1296-1313.
53. Chen J, Li C, Liu W, et al. miRNA-155 silencing reduces sciatic nerve injury in diabetic peripheral neuropathy. J Mol Endocrinol, 2019, 63(3): 227-238.
54. Han JW, Choi D, Lee MY, et al. Bone marrow-derived mesenchymal stem cells improve diabetic neuropathy by direct modulation of both angiogenesis and myelination in peripheral nerves. Cell Transplant, 2016, 25(2): 313-326.
55. 贺治青. 晚期糖基化终产物诱导人脂肪来源干细胞功能紊乱的机制研究. 上海: 第二军医大学, 2009.
56. Rojas DR, Tegeder I, Kuner R, et al. Hypoxia-inducible factor 1α protects peripheral sensory neurons from diabetic peripheral neuropathy by suppressing accumulation of reactive oxygen species. J Mol Med, 2018, 96(12): 1395-1405.
57. Xiao S, Liu Z, Yao Y, et al. Diabetic human adipose-derived stem cells accelerate pressure ulcer healing by inducing angiogenesis and neurogenesis. Stem Cells Dev, 2019, 28(5): 319-328.

Chinese Journal of Reparative and Reconstructive Surgery

Research progress on effects of high glucose microenvironment on biological activity of adipose-derived stem cells

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