Research progress of adipose-derived stem cells on refractory wounds_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

XIONG Jiachao ¹ ,  SONG Jianxing ²

1. Graduate School, the Second Military Medical University, Shanghai, 200433, P.R.China;
2. Department of Plastic Surgery, Changhai Hospital, the Second Military Medical University, Shanghai, 200433, P.R.China;

Corresponding author：

SONG Jianxing, Email: drsong@163.com

Keywords：

Adipose-derived stem cells; refractory wound; paracrine; angiogenesis; scaffold

DOI：

10.7507/1002-1892.201712078

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To summarize the recent advances in the research of adipose-derived stem cells (ADSCs) for the treatment of refractory wounds. Methods The related literature about using ADSCs for treating refractory wounds in recent years was reviewed, and their repair mechanism and treatment progress were summarized in detail. Results Tremendous progress has been achieved in using ADSCs in combination with single stent technology, sheet technology, and other methods to promote the healing of refractory wounds. ADSCs can accelerate wound angiogenesis and promote the healing of refractory wounds through its own mechanisms of paracrine, proangiogenic, anti-oxidative and apoptosis. Conclusion With the advantages of adequate sources, easy to extract and culture, non-immune rejection, multidirectional differentiation potential, and significant angiogenic potential, ADSCs has become the ideal seed cells of tissue regeneration. However, it is necessary to improve stem cell transmission technology and develop biomaterials for clinical application in order to improve the refractory wounds healing.

Citation： XIONG Jiachao, SONG Jianxing. Research progress of adipose-derived stem cells on refractory wounds. Chinese Journal of Reparative and Reconstructive Surgery, 2018, 32(4): 457-461. doi: 10.7507/1002-1892.201712078 Copy

1.	Bertozzi N, Simonacci F, Grieco MP, et al. The biological and clinical basis for the use of adipose-derived stem cells in the field of wound healing. Ann Med Surg (Lond), 2017, 20: 41-48.
2.	Li Q, Guo Y, Chen F, et al. Stromal cell-derived factor-1 promotes human adipose tissue-derived stem cell survival and chronic wound healing. Exp Ther Med, 2016, 12(1): 45-50.
3.	Hassan WU, Greiser U, Wang W. Role of adipose-derived stem cells in wound healing. Wound Repair Regen, 2014, 22(3): 313-325.
4.	Bajek A, Gutowska N, Olkowska J, et al. Adipose-derived stem cells as a tool in cell-based therapies. Arch Immunol Ther Exp (Warsz), 2016, 64(6): 443-454.
5.	Musina RA, Bekchanova ES, Sukhikh GT. Comparison of mesenchymal stem cells obtained from different human tissues. Bull Exp Biol Med, 2005, 139(4): 504-509.
6.	Cerqueira MT, Pirraco RP, Santos TC, et al. Human adipose stem cells cell sheet constructs impact epidermal morphogenesis in full-thickness excisional wounds. Biomacromolecules, 2013, 14(11): 3997-4008.
7.	Niemeyer P, Vohrer J, Schmal H, et al. Survival of human mesenchymal stromal cells from bone marrow and adipose tissue after xenogenic transplantation in immunocompetent mice. Cytotherapy, 2008, 10(8): 784-795.
8.	Zuk PA, Zhu M, Mizuno H, et al. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng, 2001, 7(2): 211-228.
9.	Zuk PA, Zhu M, Ashjian P, et al. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell, 2002, 13(12): 4279-4295.
10.	Rodriguez LV, Alfonso Z, Zhang R, et al. Clonogenic multipotent stem cells in human adipose tissue differentiate into functional smooth muscle cells. Proc Nat Acad Sci U S A, 2006, 103(32): 12167-12172.
11.	Fraser JK, Schreiber R, Strem B, et al. Plasticity of human adipose stem cells toward endothelial cells and cardiomyocytes. Nat Clin Pract Cardiovasc Med, 2006, 3 Suppl 1: S33-37.
12.	Kim WS, Han J, Hwang SJ, et al. An update on niche composition, signaling and functional regulation of the adipose-derived stem cells. Expert Opin Biol Ther, 2014, 14(8): 1091-1102.
13.	Kim WS, Park BS, Sung JH. The wound-healing and antioxidant effects of adipose-derived stem cells. Expert Opin Biol Ther, 2009, 9(7): 879-887.
14.	Park BS, Kim WS, Choi JS, et al. Hair growth stimulated by conditioned medium of adipose-derived stem cells is enhanced by hypoxia: evidence of increased growth factor secretion. Biomed Res, 2010, 31(1): 27-34.
15.	Zhang P, Kling RE, Ravuri SK, et al. A review of adipocyte lineage cells and dermal papilla cells in hair follicle regeneration. J Tissue Eng, 2014, 5: 2041731414556850.
16.	Gonzalez-Rey E, Gonzalez MA, Varela N, et al. Human adipose-derived mesenchymal stem cells reduce inflammatory and T cell responses and induce regulatory T cells in vitro in rheumatoid arthritis. Ann Rheum Dis, 2010, 69(1): 241-248.
17.	Javazon EH, Keswani SG, Badillo AT, et al. Enhanced epithelial gap closure and increased angiogenesis in wounds of diabetic mice treated with adult murine bone marrow stromal progenitor cells. Wound Repair Regen, 2007, 15(3): 350-359.
18.	Wu DC, Boyd AS, Wood KJ. Embryonic stem cell transplantation: potential applicability in cell replacement therapy and regenerative medicine. Front Biosci, 2007, 12: 4525-4535.
19.	Kim WS, Park BS, Kim HK, et al. Evidence supporting antioxidant action of adipose-derived stem cells: protection of human dermal fibroblasts from oxidative stress. J Dermatol Sci, 2008, 49(2): 133-142.
20.	Baregamian N, Song J, Jeschke MG, et al. IGF-1 protects intestinal epithelial cells from oxidative stress-induced apoptosis. J Surg Res, 2006, 136(1): 31-37.
21.	Shibuki H, Katai N, Kuroiwa S, et al. Expression and neuroprotective effect of hepatocyte growth factor in retinal ischemia-reperfusion injury. Invest Ophthalmol Vis Sci, 2002, 43(2): 528-536.
22.	Lee CY, Shin S, Lee J, et al. MicroRNA-mediated down-regulation of apoptosis signal-regulating kinase 1(ASK1) attenuates the apoptosis of human mesenchymal stem cells (MSCs) transplanted into infarcted heart. Int J Mol Sci, 2016, 17(10): pii: E1752.
23.	Kokai LE, Marra K, Rubin JP. Adipose stem cells: biology and clinical applications for tissue repair and regeneration. Transl Res, 2014, 163(4): 399-408.
24.	Dong Y, Sigen A, Rodrigues M, et al. Injectable and tunable gelatin hydrogels enhance stem cell retention and improve cutaneous wound healing. Adv Functional Materials, 2017, 27(24): 1606619.
25.	Huang SP, Huang CH, Shyu JF, et al. Promotion of wound healing using adipose-derived stem cells in radiation ulcer of a rat model. J Biomed Sci, 2013, 20: 51.
26.	Yang J, Yamato M, Kohno C, et al. Cell sheet engineering: recreating tissues without biodegradable scaffolds. Biomaterials, 2005, 26(33): 6415-6422.
27.	Sivan U, Jayakumar K, Keishnan LK. Constitution of fibrin-based niche for in vitro differentiation of adipose-derived mesenchymal stem cells to keratinocytes. Biores Open Access, 2014, 3(6): 339-347.
28.	Kao CT, Lin CC, Chen YW, et al. Poly (dopamine) coating of 3D printed poly (lactic acid) scaffolds for bone tissue engineering. Mater Sci Eng C Mater Biol Appl, 2015, 56: 165-173.
29.	Sukho P, Cohen A, Hesselink JW, et al. Adipose tissue-derived stem cell sheet application for tissue healing in vivo: a systematic review. Tissue Eng Part B Rev, 2018, 24(1): 37-52.
30.	Feng J, Mineda K, Wu SH, et al. An injectable non-cross-linked hyaluronic-acid gel containing therapeutic spheroids of human adipose-derived stem cells. Sci Rep, 2017, 7(1): 1548.
31.	Park IS, Chung PS, Ahn JC. Enhanced angiogenic effect of adipose-derived stromal cell spheroid with low-level light therapy in hind limb ischemia mice. Biomaterials, 2014, 35(34): 9280-9289.
32.	Mineda K, Feng J, Ishimine H, et al. Therapeutic potential of human adipose-derived stem/stromal cell microspheroids prepared by three-dimensional culture in non-cross-linked hyaluronic acid gel. Stem Cells Transl Med, 2015, 4(12): 1511-1522.
33.	Dong Y, Hassan W, Zheng Y, et al. Thermoresponsive hyperbranched copolymer with multi acrylate functionality for in situ cross-linkable hyaluronic acid composite semi-IPN hydrogel. J Mat Sci Mat Med, 2012, 23(1): 25-35.
34.	Lozano Picazo P, Pérez Garnes M, Martínez Ramos C, et al. New semi-biodegradable materials from semi-interpenetrated networks of poly (ε-caprolactone) and poly (ethyl acrylate). Macromol Biosci, 2015, 15(2): 229-240.
35.	Dong Y, Hassan WU, Kennedy R, et al. Performance of an in situ formed bioactive hydrogel dressing from a PEG-based hyperbranched multifunctional copolymer. Acta Biomater, 2014, 10(5): 2076-2085.
36.	Hassan W, Dong Y, Wang W. Encapsulation and 3D culture of human adipose-derived stem cells in an in-situ crosslinked hybrid hydrogel composed of PEG-based hyperbranched copolymer and hyaluronic acid. Stem Cell Res Ther, 2013, 4(2): 32.
37.	Stessul T, Puzzi MB, Chaim EA, et al. Platelet-rich plasma (PRP) and adipose-derived mesenchymal stem cells: stimulatory effects on proliferation and migration of fibroblasts and keratinocytes in vitro. Arch Dermatol Res, 2016, 308(7): 511-520.
38.	Kakudo N, Minakata T, Mitsui T, et al. Proliferation-promoting effect of platelet-rich plasma on human adipose-derived stem cells and human dermal fibroblasts. Plast Reconstr Surg, 2008, 122(5): 1352-1360.
39.	Greenspoon JA, Moulton SG, Millett PJ, et al. The role of platelet rich plasma (PRP) and other biologics for rotator cuff repair. Open Orthop J, 2016, 10: 309-314.
40.	Marques LF, Stessuk T, Camargo IC, et al. Platelet-rich plasma (PRP): methodological aspects and clinical applications. Platelets, 2015, 26(2): 101-113.
41.	Raposio E, Beryozzi N, Bonomini S, et al. Adipose-derived stem cells added to platelet-rich plasma for chronic skin ulcer therapy. Wounds, 2016, 28(4): 126-131.
42.	Tartarini D, Mele E. Adult stem cell therapies for wound healing: biomaterials and computational models. Front Bioeng Biotechnol, 2016, 3: 206.
43.	Akita S, Yoshimoto H, Akino K, et al. Early experiences with stem cells in treating chronic wounds. Clin Plast Surg, 2012, 39(3): 281-292.
44.	Kim WS, Park BS, Sung JH, et al. Wound healing effect of adipose-derived stem cells: a critical role of secretory factors on human dermal fibroblasts. J Dermatol Sci, 2007, 48(1): 15-24.
45.	Shingyochi Y, Orbay H, Mizuno H. Adipose-derived stem cells for wound repair and regeneration. Exp Opin Biol Ther, 2015, 15(9): 1285-1292.
46.	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.
47.	Nie C, Yang D, Xu J, et al. Locally administered adipose-derived stem cells accelerate wound healing through differentiation and vasculogenesis. Cell Transplant, 2011, 20(2): 205-216.
48.	Lee JH, Fisher DE. Melanocyte stem cells as potential therapeutics in skin disorders. Exp Opin Biol Ther, 2014, 14(11): 1569-1579.

1. Bertozzi N, Simonacci F, Grieco MP, et al. The biological and clinical basis for the use of adipose-derived stem cells in the field of wound healing. Ann Med Surg (Lond), 2017, 20: 41-48.
2. Li Q, Guo Y, Chen F, et al. Stromal cell-derived factor-1 promotes human adipose tissue-derived stem cell survival and chronic wound healing. Exp Ther Med, 2016, 12(1): 45-50.
3. Hassan WU, Greiser U, Wang W. Role of adipose-derived stem cells in wound healing. Wound Repair Regen, 2014, 22(3): 313-325.
4. Bajek A, Gutowska N, Olkowska J, et al. Adipose-derived stem cells as a tool in cell-based therapies. Arch Immunol Ther Exp (Warsz), 2016, 64(6): 443-454.
5. Musina RA, Bekchanova ES, Sukhikh GT. Comparison of mesenchymal stem cells obtained from different human tissues. Bull Exp Biol Med, 2005, 139(4): 504-509.
6. Cerqueira MT, Pirraco RP, Santos TC, et al. Human adipose stem cells cell sheet constructs impact epidermal morphogenesis in full-thickness excisional wounds. Biomacromolecules, 2013, 14(11): 3997-4008.
7. Niemeyer P, Vohrer J, Schmal H, et al. Survival of human mesenchymal stromal cells from bone marrow and adipose tissue after xenogenic transplantation in immunocompetent mice. Cytotherapy, 2008, 10(8): 784-795.
8. Zuk PA, Zhu M, Mizuno H, et al. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng, 2001, 7(2): 211-228.
9. Zuk PA, Zhu M, Ashjian P, et al. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell, 2002, 13(12): 4279-4295.
10. Rodriguez LV, Alfonso Z, Zhang R, et al. Clonogenic multipotent stem cells in human adipose tissue differentiate into functional smooth muscle cells. Proc Nat Acad Sci U S A, 2006, 103(32): 12167-12172.
11. Fraser JK, Schreiber R, Strem B, et al. Plasticity of human adipose stem cells toward endothelial cells and cardiomyocytes. Nat Clin Pract Cardiovasc Med, 2006, 3 Suppl 1: S33-37.
12. Kim WS, Han J, Hwang SJ, et al. An update on niche composition, signaling and functional regulation of the adipose-derived stem cells. Expert Opin Biol Ther, 2014, 14(8): 1091-1102.
13. Kim WS, Park BS, Sung JH. The wound-healing and antioxidant effects of adipose-derived stem cells. Expert Opin Biol Ther, 2009, 9(7): 879-887.
14. Park BS, Kim WS, Choi JS, et al. Hair growth stimulated by conditioned medium of adipose-derived stem cells is enhanced by hypoxia: evidence of increased growth factor secretion. Biomed Res, 2010, 31(1): 27-34.
15. Zhang P, Kling RE, Ravuri SK, et al. A review of adipocyte lineage cells and dermal papilla cells in hair follicle regeneration. J Tissue Eng, 2014, 5: 2041731414556850.
16. Gonzalez-Rey E, Gonzalez MA, Varela N, et al. Human adipose-derived mesenchymal stem cells reduce inflammatory and T cell responses and induce regulatory T cells in vitro in rheumatoid arthritis. Ann Rheum Dis, 2010, 69(1): 241-248.
17. Javazon EH, Keswani SG, Badillo AT, et al. Enhanced epithelial gap closure and increased angiogenesis in wounds of diabetic mice treated with adult murine bone marrow stromal progenitor cells. Wound Repair Regen, 2007, 15(3): 350-359.
18. Wu DC, Boyd AS, Wood KJ. Embryonic stem cell transplantation: potential applicability in cell replacement therapy and regenerative medicine. Front Biosci, 2007, 12: 4525-4535.
19. Kim WS, Park BS, Kim HK, et al. Evidence supporting antioxidant action of adipose-derived stem cells: protection of human dermal fibroblasts from oxidative stress. J Dermatol Sci, 2008, 49(2): 133-142.
20. Baregamian N, Song J, Jeschke MG, et al. IGF-1 protects intestinal epithelial cells from oxidative stress-induced apoptosis. J Surg Res, 2006, 136(1): 31-37.
21. Shibuki H, Katai N, Kuroiwa S, et al. Expression and neuroprotective effect of hepatocyte growth factor in retinal ischemia-reperfusion injury. Invest Ophthalmol Vis Sci, 2002, 43(2): 528-536.
22. Lee CY, Shin S, Lee J, et al. MicroRNA-mediated down-regulation of apoptosis signal-regulating kinase 1(ASK1) attenuates the apoptosis of human mesenchymal stem cells (MSCs) transplanted into infarcted heart. Int J Mol Sci, 2016, 17(10): pii: E1752.
23. Kokai LE, Marra K, Rubin JP. Adipose stem cells: biology and clinical applications for tissue repair and regeneration. Transl Res, 2014, 163(4): 399-408.
24. Dong Y, Sigen A, Rodrigues M, et al. Injectable and tunable gelatin hydrogels enhance stem cell retention and improve cutaneous wound healing. Adv Functional Materials, 2017, 27(24): 1606619.
25. Huang SP, Huang CH, Shyu JF, et al. Promotion of wound healing using adipose-derived stem cells in radiation ulcer of a rat model. J Biomed Sci, 2013, 20: 51.
26. Yang J, Yamato M, Kohno C, et al. Cell sheet engineering: recreating tissues without biodegradable scaffolds. Biomaterials, 2005, 26(33): 6415-6422.
27. Sivan U, Jayakumar K, Keishnan LK. Constitution of fibrin-based niche for in vitro differentiation of adipose-derived mesenchymal stem cells to keratinocytes. Biores Open Access, 2014, 3(6): 339-347.
28. Kao CT, Lin CC, Chen YW, et al. Poly (dopamine) coating of 3D printed poly (lactic acid) scaffolds for bone tissue engineering. Mater Sci Eng C Mater Biol Appl, 2015, 56: 165-173.
29. Sukho P, Cohen A, Hesselink JW, et al. Adipose tissue-derived stem cell sheet application for tissue healing in vivo: a systematic review. Tissue Eng Part B Rev, 2018, 24(1): 37-52.
30. Feng J, Mineda K, Wu SH, et al. An injectable non-cross-linked hyaluronic-acid gel containing therapeutic spheroids of human adipose-derived stem cells. Sci Rep, 2017, 7(1): 1548.
31. Park IS, Chung PS, Ahn JC. Enhanced angiogenic effect of adipose-derived stromal cell spheroid with low-level light therapy in hind limb ischemia mice. Biomaterials, 2014, 35(34): 9280-9289.
32. Mineda K, Feng J, Ishimine H, et al. Therapeutic potential of human adipose-derived stem/stromal cell microspheroids prepared by three-dimensional culture in non-cross-linked hyaluronic acid gel. Stem Cells Transl Med, 2015, 4(12): 1511-1522.
33. Dong Y, Hassan W, Zheng Y, et al. Thermoresponsive hyperbranched copolymer with multi acrylate functionality for in situ cross-linkable hyaluronic acid composite semi-IPN hydrogel. J Mat Sci Mat Med, 2012, 23(1): 25-35.
34. Lozano Picazo P, Pérez Garnes M, Martínez Ramos C, et al. New semi-biodegradable materials from semi-interpenetrated networks of poly (ε-caprolactone) and poly (ethyl acrylate). Macromol Biosci, 2015, 15(2): 229-240.
35. Dong Y, Hassan WU, Kennedy R, et al. Performance of an in situ formed bioactive hydrogel dressing from a PEG-based hyperbranched multifunctional copolymer. Acta Biomater, 2014, 10(5): 2076-2085.
36. Hassan W, Dong Y, Wang W. Encapsulation and 3D culture of human adipose-derived stem cells in an in-situ crosslinked hybrid hydrogel composed of PEG-based hyperbranched copolymer and hyaluronic acid. Stem Cell Res Ther, 2013, 4(2): 32.
37. Stessul T, Puzzi MB, Chaim EA, et al. Platelet-rich plasma (PRP) and adipose-derived mesenchymal stem cells: stimulatory effects on proliferation and migration of fibroblasts and keratinocytes in vitro. Arch Dermatol Res, 2016, 308(7): 511-520.
38. Kakudo N, Minakata T, Mitsui T, et al. Proliferation-promoting effect of platelet-rich plasma on human adipose-derived stem cells and human dermal fibroblasts. Plast Reconstr Surg, 2008, 122(5): 1352-1360.
39. Greenspoon JA, Moulton SG, Millett PJ, et al. The role of platelet rich plasma (PRP) and other biologics for rotator cuff repair. Open Orthop J, 2016, 10: 309-314.
40. Marques LF, Stessuk T, Camargo IC, et al. Platelet-rich plasma (PRP): methodological aspects and clinical applications. Platelets, 2015, 26(2): 101-113.
41. Raposio E, Beryozzi N, Bonomini S, et al. Adipose-derived stem cells added to platelet-rich plasma for chronic skin ulcer therapy. Wounds, 2016, 28(4): 126-131.
42. Tartarini D, Mele E. Adult stem cell therapies for wound healing: biomaterials and computational models. Front Bioeng Biotechnol, 2016, 3: 206.
43. Akita S, Yoshimoto H, Akino K, et al. Early experiences with stem cells in treating chronic wounds. Clin Plast Surg, 2012, 39(3): 281-292.
44. Kim WS, Park BS, Sung JH, et al. Wound healing effect of adipose-derived stem cells: a critical role of secretory factors on human dermal fibroblasts. J Dermatol Sci, 2007, 48(1): 15-24.
45. Shingyochi Y, Orbay H, Mizuno H. Adipose-derived stem cells for wound repair and regeneration. Exp Opin Biol Ther, 2015, 15(9): 1285-1292.
46. 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.
47. Nie C, Yang D, Xu J, et al. Locally administered adipose-derived stem cells accelerate wound healing through differentiation and vasculogenesis. Cell Transplant, 2011, 20(2): 205-216.
48. Lee JH, Fisher DE. Melanocyte stem cells as potential therapeutics in skin disorders. Exp Opin Biol Ther, 2014, 14(11): 1569-1579.

Chinese Journal of Reparative and Reconstructive Surgery

Research progress of adipose-derived stem cells on refractory wounds

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