Research progress of adipose-derived stem cells in skin scar prevention and treatment_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

HE Tao ^1,2 , YANG Jiqiao ¹ , LIU Pengcheng ^1,2 , XU Li ^1,2 ,  LÜ Qing ¹ ,  TAN Qiuwen ^1,2

1. Department of Breast Surgery, West China Hospital, Sichuan University, Chengdu Sichuan, 610041, P.R.China;
2. Laboratory of Stem Cell and Tissue Engineering, West China Hospital, Sichuan University, Chengdu Sichuan, 610041, P.R.China;

Corresponding author：

LÜ Qing, Email: lvqingwestchina@163.com; TAN Qiuwen, Email: hxtanqiuwen@163.com

Keywords：

Adipose-derived stem cells; skin scar; prevent; treatment; research progress

DOI：

10.7507/1002-1892.202007083

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To review the research progress of adipose-derived stem cells (ADSCs) in skin scar prevention and treatment.Methods The related literature was extensively reviewed and analyzed. The recent in vitro and in vivo experiments and clinical studies on the role of ADSCs in skin scar prevention and treatment, and the possible mechanisms and biomaterials to optimize the effect of ADSCs were summarized.Results As demonstrated by in vitro and in vivo experiments and clinical studies, ADSCs participate in the whole process of skin wound healing and may prevent and treat skin scars by reducing inflammation, promoting angiogenesis, or inhibiting (muscle) fibroblasts activity to reduce collagen deposition through the p38/mitogen-activated protein kinase, peroxisome proliferator activated receptor γ, transforming growth factor β₁/Smads pathways. Moreover, bioengineered materials such as hydrogel from acellular porcine adipose tissue, porcine small-intestine submucosa, and poly (3-hydroxybutyrate-co-hydroxyvalerate) scaffold may further enhance the efficacy of ADSCs in preventing and treating skin scars.Conclusion Remarkable progress has been made in the application of ADSCs in skin scar prevention and treatment. While, further studies are still needed to explore the application methods of ADSCs in the clinic.

Citation： HE Tao, YANG Jiqiao, LIU Pengcheng, XU Li, LÜ Qing, TAN Qiuwen. Research progress of adipose-derived stem cells in skin scar prevention and treatment. Chinese Journal of Reparative and Reconstructive Surgery, 2021, 35(2): 234-240. doi: 10.7507/1002-1892.202007083 Copy

1.	Zhao JC, Zhang BR, Shi K, et al. Lower energy radial shock wave therapy improves characteristics of hypertrophic scar in a rabbit ear model. Exp Ther Med, 2018, 15(1): 933-939.
2.	Chen SH, Chou PY, Chen ZY, et al. Electrospun water-borne polyurethane nanofibrous membrane as a barrier for preventing postoperative peritendinous adhesion. Int J Mol Sci, 2019, 20(7): 1625.
3.	Zhang X, Lan D, Ning S, et al. Botulinum toxin type A prevents the phenotypic transformation of fibroblasts induced by TGF-β1 via the PTEN/PI3K/Akt signaling pathway. Int J Mol Med, 2019, 44(2): 661-671.
4.	Chen XE, Liu J, Bin Jameel AA, et al. Combined effects of long-pulsed neodymium-yttrium-aluminum-garnet laser, diprospan and 5-fluorouracil in the treatment of keloid scars. Exp Ther Med, 2017, 13(6): 3607-3612.
5.	Spiekman M, van Dongen JA, Willemsen JC, et al. The power of fat and its adipose-derived stromal cells: emerging concepts for fibrotic scar treatment. J Tissue Eng Regen Med, 2017, 11(11): 3220-3235.
6.	Ai G, Meng M, Wang L, et al. microRNA-196a promotes osteogenic differentiation and inhibit adipogenic differentiation of adipose stem cells via regulating β-catenin pathway. Am J Transl Res, 2019, 11(5): 3081-3091.
7.	Harris WM, Zhang P, Plastini M, et al. Evaluation of function and recovery of adipose-derived stem cells after exposure to paclitaxel. Cytotherapy, 2017, 19(2): 211-221.
8.	Marangoni RG, Lu TT. The roles of dermal white adipose tissue loss in scleroderma skin fibrosis. Curr Opin Rheumatol, 2017, 29(6): 585-590.
9.	Yu J, Wang MY, Tai HC, et al. Cell sheet composed of adipose-derived stem cells demonstrates enhanced skin wound healing with reduced scar formation. Acta Biomater, 2018, 77: 191-200.
10.	Borovikova AA, Ziegler ME, Banyard DA, et al. Adipose-derived tissue in the treatment of dermal fibrosis: Antifibrotic effects of adipose-derived stem cells. Ann Plast Surg, 2018, 80(3): 297-307.
11.	Zonari A, Martins TM, Paula AC, et al. Polyhydroxybutyrate-co-hydroxyvalerate structures loaded with adipose stem cells promote skin healing with reduced scarring. Acta Biomater, 2015, 17: 170-181.
12.	Franz A, Wood W, Martin P. Fat body cells are motile and actively migrate to wounds to drive repair and prevent infection. Dev Cell, 2018, 44(4): 460-470.
13.	Schmidt BA, Horsley V. Intradermal adipocytes mediate fibroblast recruitment during skin wound healing. Development, 2013, 140(7): 1517-1527.
14.	Kruglikov IL, Scherer PE. Dermal adipocytes: from irrelevance to metabolic targets? Trends Endocrinol Metab, 2016, 27(1): 1-10.
15.	Ng M, Thakkar D, Southam L, et al. A Genome-wide association study of dupuytren disease reveals 17 additional variants implicated in fibrosis. Am J Hum Genet, 2017, 101(3): 417-427.
16.	Spiekman M, Przybyt E, Plantinga JA, et al. Adipose tissue-derived stromal cells inhibit TGF-β1-induced differentiation of human dermal fibroblasts and keloid scar-derived fibroblasts in a paracrine fashion. Plast Reconstr Surg, 2014, 134(4): 699-712.
17.	Wang XX, Ma Y, Gao Z, et al. Human adipose-derived stem cells inhibit bioactivity of keloid fibroblasts. Stem Cell Res Ther, 2018, 9(1): 40. doi: 10.1186/s13287-018-0786-4.
18.	Chai CY, Song J, Tan Z, et al. Adipose tissue-derived stem cells inhibit hypertrophic scar (HS) fibrosis via p38/MAPK pathway. J Cell Biochem, 2019, 120(3): 4057-4064.
19.	Lee SH, Lee JH, Cho KH. Effects of human adipose-derived stem cells on cutaneous wound healing in nude mice. Ann Dermatol, 2011, 23(2): 150-155.
20.	Yun IS, Jeon YR, Lee WJ, et al. Effect of human adipose derived stem cells on scar formation and remodeling in a pig model: a pilot study. Dermatol Surg, 2012, 38(10): 1678-1688.
21.	Castiglione F, Hedlund P, Van der Aa F, et al. Intratunical injection of human adipose tissue-derived stem cells prevents fibrosis and is associated with improved erectile function in a rat model of Peyronie’s disease. Eur Urol, 2013, 63(3): 551-560.
22.	Lam MT, Nauta A, Meyer NP, et al. Effective delivery of stem cells using an extracellular matrix patch results in increased cell survival and proliferation and reduced scarring in skin wound healing. Tissue Eng Part A, 2013, 19(5-6): 738-747.
23.	Uysal CA, Tobita M, Hyakusoku H, et al. The effect of bone-marrow-derived stem cells and adipose-derived stem cells on wound contraction and epithelization. Adv Wound Care (New Rochelle), 2014, 3(6): 405-413.
24.	Zhang Q, Liu LN, Yong Q, et al. Intralesional injection of adipose-derived stem cells reduces hypertrophic scarring in a rabbit ear model. Stem Cell Res Ther, 2015, 6(1): 145. doi: 10.1186/s13287-015-0133-y.
25.	Franck CL, Senegaglia AC, Leite LMB, et al. Influence of adipose tissue-derived stem cells on the burn wound healing process. Stem Cells Int, 2019, 2019: 2340725. doi: 10.1155/2019/2340725.eCollection2019.
26.	Bellini E, Grieco MP, Raposio E. The science behind autologous fat grafting. Ann Med Surg (Lond), 2017, 24: 65-73.
27.	Hong KY, Yim S, Kim HJ, et al. The fate of the adipose-derived stromal cells during angiogenesis and adipogenesis after cell-assisted lipotransfer. Plast Reconstr Surg, 2018, 141(2): 365-375.
28.	Wu SH, Shirado T, Mashiko T, et al. Therapeutic effects of human adipose-derived products on impaired wound healing in irradiated tissue. Plast Reconstr Surg, 2018, 142(2): 383-391.
29.	Akita S, Yoshimoto H, Ohtsuru A, et al. Autologous adipose-derived regenerative cells are effective for chronic intractable radiation injuries. Radiat Prot Dosimetry, 2012, 151(4): 656-660.
30.	Tiryaki T, Findikli N, Tiryaki D. Staged stem cell-enriched tissue (SET) injections for soft tissue augmentation in hostile recipient areas: a preliminary report. Aesthetic Plast Surg, 2011, 35(6): 965-971.
31.	Zhou BR, Zhang T, Bin Jameel AA, et al. The efficacy of conditioned media of adipose-derived stem cells combined with ablative carbon dioxide fractional resurfacing for atrophic acne scars and skin rejuvenation. J Cosmet Laser Ther, 2016, 18(3): 138-148.
32.	Rehman J, Traktuev D, Li J, et al. Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells. Circulation, 2004, 109(10): 1292-1298.
33.	Atalay S, Coruh A, Deniz K. Stromal vascular fraction improves deep partial thickness burn wound healing. Burns, 2014, 40(7): 1375-1383.
34.	Horton JA, Hudak KE, Chung EJ, et al. Mesenchymal stem cells inhibit cutaneous radiation-induced fibrosis by suppressing chronic inflammation. Stem Cells, 2013, 31(10): 2231-2241.
35.	董瑶, 董飞君, 李幼华. 脂肪干细胞调节创面炎症反应并促进创面愈合. 医学研究杂志, 2012, 41(3): 100-103.
36.	Manning CN, Martel C, Sakiyama-Elbert SE, et al. Adipose-derived mesenchymal stromal cells modulate tendon fibroblast responses to macrophage-induced inflammation in vitro. Stem Cell Res Ther, 2015, 6(1): 74. doi: 10.1186/s13287-015-0059-4.
37.	Zhang W, Bai X, Zhao B, et al. Cell-free therapy based on adipose tissue stem cell-derived exosomes promotes wound healing via the PI3K/Akt signaling pathway. Exp Cell Res, 2018, 370(2): 333-342.
38.	Bajek A, Gurtowska 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.
39.	Park J, Lee JH, Yoon BS, et al. Additive effect of bFGF and selenium on expansion and paracrine action of human amniotic fluid-derived mesenchymal stem cells. Stem Cell Res Ther, 2018, 9(1): 293. doi: 10.1186/s13287-018-1058-z.
40.	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.
41.	Li Y, Zhang W, Gao J, et al. Adipose tissue-derived stem cells suppress hypertrophic scar fibrosis via the p38/MAPK signaling pathway. Stem Cell Res Ther, 2016, 7(1): 102. doi: 10.1186/s13287-016-0356-6.
42.	Mirza AZ, Althagafi II, Shamshad H. Role of PPAR receptor in different diseases and their ligands: Physiological importance and clinical implications. Eur J Med Chem, 2019, 166: 502-513.
43.	Ho YY, Lagares D, Tager AM, et al. Fibrosis—a lethal component of systemic sclerosis. Nat Rev Rheumatol, 2014, 10(7): 390-402.
44.	Vallée A, Lecarpentier Y, Guillevin R, et al. Interactions between TGF-β1, canonical WNT/β-catenin pathway and PPAR γ in radiation-induced fibrosis. Oncotarget, 2017, 8(52): 90579-90604.
45.	Zhang LT, Peng XB, Fang XQ, et al. Human umbilical cord mesenchymal stem cells inhibit proliferation of hepatic stellate cells in vitro. Int J Mol Med, 2018, 41(5): 2545-2552.
46.	Han Y, Lu JS, Xu Y, et al. Rutin ameliorates renal fibrosis and proteinuria in 5/6-nephrectomized rats by anti-oxidation and inhibiting activation of TGFβ1-smad signaling. Int J Clin Exp Pathol, 2015, 8(5): 4725-4734.
47.	Zhang Y, Zhao H, Li H, et al. Protective effects of amarogentin against carbon tetrachloride-induced liver fibrosis in mice. Molecules, 2017, 22(5): 754. doi: 10.3390/molecules22050754.
48.	Ikushima H, Miyazono K. TGF-β signal transduction spreading to a wider field: a broad variety of mechanisms for context-dependent effects of TGF-β. Cell Tissue Res, 2012, 347(1): 37-49.
49.	许言文. 脂肪干细胞旁分泌作用基于 TGF-β₁/Smads 通路对增生性瘢痕影响的实验研究. 乌鲁木齐: 新疆医科大学, 2016.
50.	Johnstone RM, Adam M, Hammond JR, et al. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Biol Chem, 1987, 262(19): 9412-9420.
51.	Wang L, Hu L, Zhou X, et al. Exosomes secreted by human adipose mesenchymal stem cells promote scarless cutaneous repair by regulating extracellular matrix remodelling. Sci Rep, 2017, 7(1): 13321. doi: 10.1038/s41598-017-12919-x.
52.	张静. 干细胞外泌体生物学功能及临床应用前景. 中国美容医学杂志, 2017, 26(4): 136-140.
53.	Li P, Kaslan M, Lee SH, et al. Progress in exosome isolation techniques. Theranostics, 2017, 7(3): 789-804.
54.	卢颖洁. 人脂肪干细胞来源的外泌体通过 miR-486-5p 介导促进皮肤创面愈合的机制研究. 南昌: 南昌大学, 2020.
55.	王江文, 易阳艳, 朱元正, 等. 脂肪干细胞来源外泌体促进糖尿病小鼠创面愈合的实验研究. 中国修复重建外科杂志, 2020, 34(1): 124-131.
56.	李全. ADSC-exo 对肉芽组织成纤维细胞增殖影响及修复裸鼠皮肤缺损的研究. 天津: 天津医科大学, 2019.
57.	Tan QW, Zhang Y, Luo JC, et al. Hydrogel derived from decellularized porcine adipose tissue as a promising biomaterial for soft tissue augmentation. J Biomed Mater Res A, 2017, 105(6): 1756-1764.
58.	Tan QW, Tang SL, Zhang Y, et al. Hydrogel from acellular porcine adipose tissue accelerates wound healing by inducing intradermal adipocyte regeneration. J Invest Dermatol, 2019, 139(2): 455-463.

1. Zhao JC, Zhang BR, Shi K, et al. Lower energy radial shock wave therapy improves characteristics of hypertrophic scar in a rabbit ear model. Exp Ther Med, 2018, 15(1): 933-939.
2. Chen SH, Chou PY, Chen ZY, et al. Electrospun water-borne polyurethane nanofibrous membrane as a barrier for preventing postoperative peritendinous adhesion. Int J Mol Sci, 2019, 20(7): 1625.
3. Zhang X, Lan D, Ning S, et al. Botulinum toxin type A prevents the phenotypic transformation of fibroblasts induced by TGF-β1 via the PTEN/PI3K/Akt signaling pathway. Int J Mol Med, 2019, 44(2): 661-671.
4. Chen XE, Liu J, Bin Jameel AA, et al. Combined effects of long-pulsed neodymium-yttrium-aluminum-garnet laser, diprospan and 5-fluorouracil in the treatment of keloid scars. Exp Ther Med, 2017, 13(6): 3607-3612.
5. Spiekman M, van Dongen JA, Willemsen JC, et al. The power of fat and its adipose-derived stromal cells: emerging concepts for fibrotic scar treatment. J Tissue Eng Regen Med, 2017, 11(11): 3220-3235.
6. Ai G, Meng M, Wang L, et al. microRNA-196a promotes osteogenic differentiation and inhibit adipogenic differentiation of adipose stem cells via regulating β-catenin pathway. Am J Transl Res, 2019, 11(5): 3081-3091.
7. Harris WM, Zhang P, Plastini M, et al. Evaluation of function and recovery of adipose-derived stem cells after exposure to paclitaxel. Cytotherapy, 2017, 19(2): 211-221.
8. Marangoni RG, Lu TT. The roles of dermal white adipose tissue loss in scleroderma skin fibrosis. Curr Opin Rheumatol, 2017, 29(6): 585-590.
9. Yu J, Wang MY, Tai HC, et al. Cell sheet composed of adipose-derived stem cells demonstrates enhanced skin wound healing with reduced scar formation. Acta Biomater, 2018, 77: 191-200.
10. Borovikova AA, Ziegler ME, Banyard DA, et al. Adipose-derived tissue in the treatment of dermal fibrosis: Antifibrotic effects of adipose-derived stem cells. Ann Plast Surg, 2018, 80(3): 297-307.
11. Zonari A, Martins TM, Paula AC, et al. Polyhydroxybutyrate-co-hydroxyvalerate structures loaded with adipose stem cells promote skin healing with reduced scarring. Acta Biomater, 2015, 17: 170-181.
12. Franz A, Wood W, Martin P. Fat body cells are motile and actively migrate to wounds to drive repair and prevent infection. Dev Cell, 2018, 44(4): 460-470.
13. Schmidt BA, Horsley V. Intradermal adipocytes mediate fibroblast recruitment during skin wound healing. Development, 2013, 140(7): 1517-1527.
14. Kruglikov IL, Scherer PE. Dermal adipocytes: from irrelevance to metabolic targets? Trends Endocrinol Metab, 2016, 27(1): 1-10.
15. Ng M, Thakkar D, Southam L, et al. A Genome-wide association study of dupuytren disease reveals 17 additional variants implicated in fibrosis. Am J Hum Genet, 2017, 101(3): 417-427.
16. Spiekman M, Przybyt E, Plantinga JA, et al. Adipose tissue-derived stromal cells inhibit TGF-β1-induced differentiation of human dermal fibroblasts and keloid scar-derived fibroblasts in a paracrine fashion. Plast Reconstr Surg, 2014, 134(4): 699-712.
17. Wang XX, Ma Y, Gao Z, et al. Human adipose-derived stem cells inhibit bioactivity of keloid fibroblasts. Stem Cell Res Ther, 2018, 9(1): 40. doi: 10.1186/s13287-018-0786-4.
18. Chai CY, Song J, Tan Z, et al. Adipose tissue-derived stem cells inhibit hypertrophic scar (HS) fibrosis via p38/MAPK pathway. J Cell Biochem, 2019, 120(3): 4057-4064.
19. Lee SH, Lee JH, Cho KH. Effects of human adipose-derived stem cells on cutaneous wound healing in nude mice. Ann Dermatol, 2011, 23(2): 150-155.
20. Yun IS, Jeon YR, Lee WJ, et al. Effect of human adipose derived stem cells on scar formation and remodeling in a pig model: a pilot study. Dermatol Surg, 2012, 38(10): 1678-1688.
21. Castiglione F, Hedlund P, Van der Aa F, et al. Intratunical injection of human adipose tissue-derived stem cells prevents fibrosis and is associated with improved erectile function in a rat model of Peyronie’s disease. Eur Urol, 2013, 63(3): 551-560.
22. Lam MT, Nauta A, Meyer NP, et al. Effective delivery of stem cells using an extracellular matrix patch results in increased cell survival and proliferation and reduced scarring in skin wound healing. Tissue Eng Part A, 2013, 19(5-6): 738-747.
23. Uysal CA, Tobita M, Hyakusoku H, et al. The effect of bone-marrow-derived stem cells and adipose-derived stem cells on wound contraction and epithelization. Adv Wound Care (New Rochelle), 2014, 3(6): 405-413.
24. Zhang Q, Liu LN, Yong Q, et al. Intralesional injection of adipose-derived stem cells reduces hypertrophic scarring in a rabbit ear model. Stem Cell Res Ther, 2015, 6(1): 145. doi: 10.1186/s13287-015-0133-y.
25. Franck CL, Senegaglia AC, Leite LMB, et al. Influence of adipose tissue-derived stem cells on the burn wound healing process. Stem Cells Int, 2019, 2019: 2340725. doi: 10.1155/2019/2340725.eCollection2019.
26. Bellini E, Grieco MP, Raposio E. The science behind autologous fat grafting. Ann Med Surg (Lond), 2017, 24: 65-73.
27. Hong KY, Yim S, Kim HJ, et al. The fate of the adipose-derived stromal cells during angiogenesis and adipogenesis after cell-assisted lipotransfer. Plast Reconstr Surg, 2018, 141(2): 365-375.
28. Wu SH, Shirado T, Mashiko T, et al. Therapeutic effects of human adipose-derived products on impaired wound healing in irradiated tissue. Plast Reconstr Surg, 2018, 142(2): 383-391.
29. Akita S, Yoshimoto H, Ohtsuru A, et al. Autologous adipose-derived regenerative cells are effective for chronic intractable radiation injuries. Radiat Prot Dosimetry, 2012, 151(4): 656-660.
30. Tiryaki T, Findikli N, Tiryaki D. Staged stem cell-enriched tissue (SET) injections for soft tissue augmentation in hostile recipient areas: a preliminary report. Aesthetic Plast Surg, 2011, 35(6): 965-971.
31. Zhou BR, Zhang T, Bin Jameel AA, et al. The efficacy of conditioned media of adipose-derived stem cells combined with ablative carbon dioxide fractional resurfacing for atrophic acne scars and skin rejuvenation. J Cosmet Laser Ther, 2016, 18(3): 138-148.
32. Rehman J, Traktuev D, Li J, et al. Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells. Circulation, 2004, 109(10): 1292-1298.
33. Atalay S, Coruh A, Deniz K. Stromal vascular fraction improves deep partial thickness burn wound healing. Burns, 2014, 40(7): 1375-1383.
34. Horton JA, Hudak KE, Chung EJ, et al. Mesenchymal stem cells inhibit cutaneous radiation-induced fibrosis by suppressing chronic inflammation. Stem Cells, 2013, 31(10): 2231-2241.
35. 董瑶, 董飞君, 李幼华. 脂肪干细胞调节创面炎症反应并促进创面愈合. 医学研究杂志, 2012, 41(3): 100-103.
36. Manning CN, Martel C, Sakiyama-Elbert SE, et al. Adipose-derived mesenchymal stromal cells modulate tendon fibroblast responses to macrophage-induced inflammation in vitro. Stem Cell Res Ther, 2015, 6(1): 74. doi: 10.1186/s13287-015-0059-4.
37. Zhang W, Bai X, Zhao B, et al. Cell-free therapy based on adipose tissue stem cell-derived exosomes promotes wound healing via the PI3K/Akt signaling pathway. Exp Cell Res, 2018, 370(2): 333-342.
38. Bajek A, Gurtowska 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.
39. Park J, Lee JH, Yoon BS, et al. Additive effect of bFGF and selenium on expansion and paracrine action of human amniotic fluid-derived mesenchymal stem cells. Stem Cell Res Ther, 2018, 9(1): 293. doi: 10.1186/s13287-018-1058-z.
40. 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.
41. Li Y, Zhang W, Gao J, et al. Adipose tissue-derived stem cells suppress hypertrophic scar fibrosis via the p38/MAPK signaling pathway. Stem Cell Res Ther, 2016, 7(1): 102. doi: 10.1186/s13287-016-0356-6.
42. Mirza AZ, Althagafi II, Shamshad H. Role of PPAR receptor in different diseases and their ligands: Physiological importance and clinical implications. Eur J Med Chem, 2019, 166: 502-513.
43. Ho YY, Lagares D, Tager AM, et al. Fibrosis—a lethal component of systemic sclerosis. Nat Rev Rheumatol, 2014, 10(7): 390-402.
44. Vallée A, Lecarpentier Y, Guillevin R, et al. Interactions between TGF-β1, canonical WNT/β-catenin pathway and PPAR γ in radiation-induced fibrosis. Oncotarget, 2017, 8(52): 90579-90604.
45. Zhang LT, Peng XB, Fang XQ, et al. Human umbilical cord mesenchymal stem cells inhibit proliferation of hepatic stellate cells in vitro. Int J Mol Med, 2018, 41(5): 2545-2552.
46. Han Y, Lu JS, Xu Y, et al. Rutin ameliorates renal fibrosis and proteinuria in 5/6-nephrectomized rats by anti-oxidation and inhibiting activation of TGFβ1-smad signaling. Int J Clin Exp Pathol, 2015, 8(5): 4725-4734.
47. Zhang Y, Zhao H, Li H, et al. Protective effects of amarogentin against carbon tetrachloride-induced liver fibrosis in mice. Molecules, 2017, 22(5): 754. doi: 10.3390/molecules22050754.
48. Ikushima H, Miyazono K. TGF-β signal transduction spreading to a wider field: a broad variety of mechanisms for context-dependent effects of TGF-β. Cell Tissue Res, 2012, 347(1): 37-49.
49. 许言文. 脂肪干细胞旁分泌作用基于 TGF-β₁/Smads 通路对增生性瘢痕影响的实验研究. 乌鲁木齐: 新疆医科大学, 2016.
50. Johnstone RM, Adam M, Hammond JR, et al. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Biol Chem, 1987, 262(19): 9412-9420.
51. Wang L, Hu L, Zhou X, et al. Exosomes secreted by human adipose mesenchymal stem cells promote scarless cutaneous repair by regulating extracellular matrix remodelling. Sci Rep, 2017, 7(1): 13321. doi: 10.1038/s41598-017-12919-x.
52. 张静. 干细胞外泌体生物学功能及临床应用前景. 中国美容医学杂志, 2017, 26(4): 136-140.
53. Li P, Kaslan M, Lee SH, et al. Progress in exosome isolation techniques. Theranostics, 2017, 7(3): 789-804.
54. 卢颖洁. 人脂肪干细胞来源的外泌体通过 miR-486-5p 介导促进皮肤创面愈合的机制研究. 南昌: 南昌大学, 2020.
55. 王江文, 易阳艳, 朱元正, 等. 脂肪干细胞来源外泌体促进糖尿病小鼠创面愈合的实验研究. 中国修复重建外科杂志, 2020, 34(1): 124-131.
56. 李全. ADSC-exo 对肉芽组织成纤维细胞增殖影响及修复裸鼠皮肤缺损的研究. 天津: 天津医科大学, 2019.
57. Tan QW, Zhang Y, Luo JC, et al. Hydrogel derived from decellularized porcine adipose tissue as a promising biomaterial for soft tissue augmentation. J Biomed Mater Res A, 2017, 105(6): 1756-1764.
58. Tan QW, Tang SL, Zhang Y, et al. Hydrogel from acellular porcine adipose tissue accelerates wound healing by inducing intradermal adipocyte regeneration. J Invest Dermatol, 2019, 139(2): 455-463.

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