Application of Adipose-Derived Stem Cells for Repairment and Regeneration of Adipose Tissue: A Review_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

 ZHANGShu ,  LÜQing

Department of Breast Surgery, West China Hospital of Sichuan University, Chengdu 610041, Sichuan Province, China;

Corresponding author：

LÜQing, Email: lqlq1963@163.com

Keywords：

Adipose-derived stem cells; Tissue engineering; Adipocyte; Adipose tissue

DOI：

10.7507/1007-9424.20150298

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To summarize the isolation procedures, molecular characterization, and differentiation and vascularization capacity of adipose-derived stem cells (ADSCs), in order to discuss the potential value of ADSCs for the repairment and regeneration of adipose tissues. Methods Related literatures about ADSCs were retrieved to summarize the potential value of ADSCs for the repairment and regeneration of adipose tissues. Results As mesenchymal stem cells, ADSCs was rich in human adipose tissues. ADSCs possessed the potential to differentiate toward a variety of cell lineages, such as adipogenic, chondrogenic, osteogenic, cardiomyogenic, myogenic, and angiogenic. Besides, its capacity of adipogenic differentiation could maintain several passages. The most importantly, ADSCs could secrete significant amounts of angiogenesis-related cytokines, such as vascular endothelial growth factor (VEGF) and fibroblast growth factor-2 (FGF-2), which increased the angiogenesis of adipose tissue. Conclusions ADSCs play a key role in adipose tissue engineering, autologous adipose tissue grafting, and soft tissue wound repairing, which have important application prospect for breast reconstruction.

Citation： ZHANGShu, LÜQing. Application of Adipose-Derived Stem Cells for Repairment and Regeneration of Adipose Tissue: A Review. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2015, 22(9): 1148-1152. doi: 10.7507/1007-9424.20150298 Copy

1.	中华人民共和国卫生部医政司,中华人民共和国卫生部办公厅. 乳腺癌诊疗规范(2011年版). 中国实用外科杂志, 2011, 30(10):902-907.
2.	Brayfield CA, Marra KG, Rubin JP. Adipose tissue regeneration. Curr Stem Cell Res Ther, 2010, 5(2):116-121.
3.	Kasem A, Wazir U, Headon H, et al. Breast lipofilling:a review of current practice. Arch Plast Surg, 2015, 42(2):126-130.
4.	Butler DL, Goldstein SA, Guilak F. Functional tissue engineering:the role of biomechanics. J Biomech Eng, 2000, 122(6):570-575.
5.	Gimble JM. Adipose tissue-derived therapeutics. Expert Opin Biol Ther, 2003, 3(5):705-713.
6.	Caspar-Bauguil S, Cousin B, Galinier A, et al. Adipose tissues as an ancestral immune organ:site-specific change in obesity. FEBS Lett, 2005, 579(17):3487-3492.
7.	Boquest AC, Shahdadfar A, Brinchmann JE, et al. Isolation of stromal stem cells from human adipose tissue. Methods Mol Biol, 2006, 325:35-46.
8.	Strem BM, Hicok KC, Zhu M, et al. Multipotential differentiation of adipose tissue-derived stem cells. Keio J Med, 2005, 54(3):132-141.
9.	Tsuji W, Inamoto T, Yamashiro H, et al. Adipogenesis induced by human adipose tissue-derived stem cells. Tissue Eng Part A, 2009, 15(1):83-93.
10.	Sterodimas A, De Faria J, Nicaretta B, et al. Tissue engineering with adipose-derived stem cells (ADSCs):current and future applications. J Plast Reconstr Aesthet Surg, 2010, 63(11):1886-1892.
11.	Zimmerlin L, Donnenberg VS, Pfeifer ME, et al. Stromal vascular progenitors in adult human adipose tissue. Cytometry A, 2010, 77(1):22-30.
12.	Mitchell JB, Mcintosh K, Zvonic S, et al. Immunophenotype of human adipose-derived cells:temporal changes in stromal-associated and stem cell-associated markers. Stem Cells, 2006, 24(2):376-385.
13.	Dominici M, Le Blanc K, Mueller I, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy, 2006, 8(4):315-317.
14.	Prunet-Marcassus B, Cousin B, Caton D, et al. From heterogeneity to plasticity in adipose tissues:site-specific differences. Exp Cell Res, 2006, 312(6):727-736.
15.	Schipper BM, Marra KG, Zhang W, et al. Regional anatomic and age effects on cell function of human adipose-derived stem cells. Ann Plast Surg, 2008, 60(5):538-544.
16.	Choi YS, Cha SM, Lee YY, et al. Adipogenic differentiation of adipose tissue derived adult stem cells in nude mouse. Biochem Biophys Res Commun, 2006, 345(2):631-637.
17.	Estes BT, Guilak F. Three-dimensional culture systems to induce chondrogenesis of adipose-derived stem cells. Methods Mol Biol, 2011, 702:201-217.
18.	Lee JA, Parrett BM, Conejero JA, et al. Biological alchemy:enginee-ring bone and fat from fat-derived stem cells. Ann Plast Surg, 2003, 50(6):610-617.
19.	Lee WC, Sepulveda JL, Rubin JP, et al. Cardiomyogenic differentia-tion potential of human adipose precursor cells. Int J Cardiol, 2009, 133(3):399-401.
20.	Mizuno H, Zuk PA, Zhu M, et al. Myogenic differentiation by human processed lipoaspirate cells. Plast Reconstr Surg, 2002, 109 (1):199-209.
21.	Brzoska M, Geiger H, Gauer S, et al. Epithelial differentiation of human adipose tissue-derived adult stem cells. Biochem Biophys Res Commun, 2005, 330(1):142-150.
22.	Safford KM, Hicok KC, Safford SD, et al. Neurogenic differentiation of murine and human adipose-derived stromal cells. Biochem Biophys Res Commun, 2002, 294(2):371-379.
23.	Boquest AC, Noer A, Collas P. Epigenetic programming of mesen-chymal stem cells from human adipose tissue. Stem Cell Rev, 2006, 2(4):319-329.
24.	Kimura Y, Ozeki M, Inamoto T, et al. Adipose tissue engineering based on human preadipocytes combined with gelatin microspheres containing basic fibroblast growth factor. Biomaterials, 2003, 24(14):2513-2521.
25.	Cheung HK, Han TT, Marecak DM, et al. Composite hydrogel scaffolds incorporating decellularized adipose tissue for soft tissue engineering with adipose-derived stem cells. Biomaterials, 2014, 35(6):1914-1923.
26.	Mesimäki K, Lindroos B, Törnwall J, et al. Novel maxillary reconstruction with ectopic bone formation by GMP adipose stem cells. Int J Oral Maxillofac Surg, 2009, 38(3):201-209.
27.	Gaustad KG, Boquest AC, Anderson BE, et al. Differentiation of human adipose tissue stem cells using extracts of rat cardiomyoc-ytes. Biochem Biophys Res Commun, 2004, 314(2):420-427.
28.	Yamada Y, Wang XD, Yokoyama S, et al. Cardiac progenitor cells in brown adipose tissue repaired damaged myocardium. Biochem Biophys Res Commun, 2006, 342(2):662-670.
29.	Kim SJ, Park KC, Lee JU, et al. Therapeutic potential of adipose tissue-derived stem cells for liver failure according to the transplan-tation routes. J Korean Surg Soc, 2011, 81(3):176-186.
30.	Seo MJ, Suh SY, Bae YC, et al. Differentiation of human adipose stromal cells into hepatic lineage in vitro and in vivo. Biochem Biophys Res Commun, 2005, 328(1):258-264.
31.	Timper K, Seboek D, Eberhardt M, et al. Human adipose tissue-derived mesenchymal stem cells differentiate into insulin, somatosta-tin, and glucagon expressing cells. Biochem Biophys Res Commun, 2006, 341(4):1135-1140.
32.	Deng M, Gu Y, Liu Z, et al. Endothelial differentiation of human adipose-derived stem cells on polyglycolic acid/polylactic acid mesh. Stem Cells Int, 2015, 2015:350718.
33.	Wei J, Xu M, Zhang X, et al. Enhanced osteogenic behavior of ADSCs produced by deproteinized antler cancellous bone and evidence for involvement of ERK signaling pathway. Tissue Eng Part A, 2015, 21(11-12):1810-1821.
34.	Liu S, Zhang H, Zhang X, et al. Synergistic angiogenesis promoting effects of extracellular matrix scaffolds and adipose-derived stem cells during wound repair. Tissue Eng Part A, 2011, 17(5-6):725-739.
35.	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.
36.	Traktuev DO, Merfeld-Clauss S, Li J, et al. A population of multipotent CD34-positive adipose stromal cells share pericyte and mesenchymal surface markers, reside in a periendothelial location, and stabilize endothelial networks. Circ Res, 2008, 102(1):77-85.
37.	Cao Y, Sun Z, Liao L, et al. Human adipose tissue-derived stem cells differentiate into endothelial cells in vitro and improve postnatal neovascularization in vivo. Biochem Biophys Res Commun, 2005, 332(2):370-379.
38.	Flynn L, Prestwich GD, Semple JL, et al. Adipose tissue engineering with naturally derived scaffolds and adipose-derived stem cells. Biomaterials, 2007, 28(26):3834-3842.
39.	Flynn L, Prestwich GD, Semple JL, et al. Adipose tissue engineering in vivo with adipose-derived stem cells on naturally derived scaffolds. J Biomed Mater Res A, 2009, 89(4):929-941.
40.	Zhou Y, Yan Z, Zhang H, et al. Expansion and delivery of adipose-derived mesenchymal stem cells on three microcarriers for soft tissue regeneration. Tissue Eng Part A, 2011, 17(23-24):2981-2997.
41.	Dicker A, Le Blanc K, Aström G, et al. Functional studies of mesenchymal stem cells derived from adult human adipose tissue. Exp Cell Res, 2005, 308(2):283-290.
42.	von Heimburg D, Hemmrich K, Zachariah S, et al. Oxygen consum-ption in undifferentiated versus differentiated adipogenic mesench-ymal precursor cells. Respir Physiol Neurobiol, 2005, 146(2-3):107-116.
43.	Gimble JM, Katz AJ, Bunnell BA. Adipose-derived stem cells for regenerative medicine. Circ Res, 2007, 100(9):1249-1260.
44.	Akita S, Akino K, Hirano A, et al. Mesenchymal stem cell therapy for cutaneous radiation syndrome. Health Phys, 2010, 98(6):858-862.
45.	Rigotti G, Marchi A, Galiè M, et al. Clinical treatment of radiotherapy tissue damage by lipoaspirate transplant:a healing process mediated by adipose-derived adult stem cells. Plast Reconstr Surg, 2007, 119 (5):1409-1422.
46.	Nambu M, Kishimoto S, Nakamura S, et al. Accelerated wound healing in healing-impaired db/db mice by autologous adipose tissue-derived stromal cells combined with atelocollagen matrix. Ann Plast Surg, 2009, 62(3):317-321.
47.	Yoshimura K, Sato K, Aoi N, et al. Cell-assisted lipotransfer for cosmetic breast augmentation:supportive use of adipose-derived stem/stromal cells. Aesthetic Plast Surg, 2008, 32(1):48-55.
48.	Kamakura T, Ito K. Autologous cell-enriched fat grafting for breast augmentation. Aesthetic Plast Surg, 2011, 35(6):1022-1030.
49.	Pérez-Cano R, Vranckx JJ, Lasso JM, et al. Prospective trial of adipose-derived regenerative cell (ADRC)-enriched fat grafting for partial mastectomy defects:the RESTORE-2 trial. Eur J Surg Oncol, 2012, 38(5):382-389.
50.	Shin KK, Lee AL, Kim JY, et al. MiR-21 modulates tumor outgrowth induced by human adipose tissue-derived mesenchymal stem cells in vivo. Biochem Biophys Res Commun, 2012, 422(4):633-638.
51.	Karnoub AE, Dash AB, Vo AP, et al. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature, 2007, 449(7162):557-563.
52.	Kakudo N, Tanaka Y, Morimoto N, et al. Adipose-derived regenera-tive cell (ADRC)-enriched fat grafting:optimal cell concentration and effects on grafted fat characteristics. J Transl Med, 2013, 11:254.

1. 中华人民共和国卫生部医政司,中华人民共和国卫生部办公厅. 乳腺癌诊疗规范(2011年版). 中国实用外科杂志, 2011, 30(10):902-907.
2. Brayfield CA, Marra KG, Rubin JP. Adipose tissue regeneration. Curr Stem Cell Res Ther, 2010, 5(2):116-121.
3. Kasem A, Wazir U, Headon H, et al. Breast lipofilling:a review of current practice. Arch Plast Surg, 2015, 42(2):126-130.
4. Butler DL, Goldstein SA, Guilak F. Functional tissue engineering:the role of biomechanics. J Biomech Eng, 2000, 122(6):570-575.
5. Gimble JM. Adipose tissue-derived therapeutics. Expert Opin Biol Ther, 2003, 3(5):705-713.
6. Caspar-Bauguil S, Cousin B, Galinier A, et al. Adipose tissues as an ancestral immune organ:site-specific change in obesity. FEBS Lett, 2005, 579(17):3487-3492.
7. Boquest AC, Shahdadfar A, Brinchmann JE, et al. Isolation of stromal stem cells from human adipose tissue. Methods Mol Biol, 2006, 325:35-46.
8. Strem BM, Hicok KC, Zhu M, et al. Multipotential differentiation of adipose tissue-derived stem cells. Keio J Med, 2005, 54(3):132-141.
9. Tsuji W, Inamoto T, Yamashiro H, et al. Adipogenesis induced by human adipose tissue-derived stem cells. Tissue Eng Part A, 2009, 15(1):83-93.
10. Sterodimas A, De Faria J, Nicaretta B, et al. Tissue engineering with adipose-derived stem cells (ADSCs):current and future applications. J Plast Reconstr Aesthet Surg, 2010, 63(11):1886-1892.
11. Zimmerlin L, Donnenberg VS, Pfeifer ME, et al. Stromal vascular progenitors in adult human adipose tissue. Cytometry A, 2010, 77(1):22-30.
12. Mitchell JB, Mcintosh K, Zvonic S, et al. Immunophenotype of human adipose-derived cells:temporal changes in stromal-associated and stem cell-associated markers. Stem Cells, 2006, 24(2):376-385.
13. Dominici M, Le Blanc K, Mueller I, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy, 2006, 8(4):315-317.
14. Prunet-Marcassus B, Cousin B, Caton D, et al. From heterogeneity to plasticity in adipose tissues:site-specific differences. Exp Cell Res, 2006, 312(6):727-736.
15. Schipper BM, Marra KG, Zhang W, et al. Regional anatomic and age effects on cell function of human adipose-derived stem cells. Ann Plast Surg, 2008, 60(5):538-544.
16. Choi YS, Cha SM, Lee YY, et al. Adipogenic differentiation of adipose tissue derived adult stem cells in nude mouse. Biochem Biophys Res Commun, 2006, 345(2):631-637.
17. Estes BT, Guilak F. Three-dimensional culture systems to induce chondrogenesis of adipose-derived stem cells. Methods Mol Biol, 2011, 702:201-217.
18. Lee JA, Parrett BM, Conejero JA, et al. Biological alchemy:enginee-ring bone and fat from fat-derived stem cells. Ann Plast Surg, 2003, 50(6):610-617.
19. Lee WC, Sepulveda JL, Rubin JP, et al. Cardiomyogenic differentia-tion potential of human adipose precursor cells. Int J Cardiol, 2009, 133(3):399-401.
20. Mizuno H, Zuk PA, Zhu M, et al. Myogenic differentiation by human processed lipoaspirate cells. Plast Reconstr Surg, 2002, 109 (1):199-209.
21. Brzoska M, Geiger H, Gauer S, et al. Epithelial differentiation of human adipose tissue-derived adult stem cells. Biochem Biophys Res Commun, 2005, 330(1):142-150.
22. Safford KM, Hicok KC, Safford SD, et al. Neurogenic differentiation of murine and human adipose-derived stromal cells. Biochem Biophys Res Commun, 2002, 294(2):371-379.
23. Boquest AC, Noer A, Collas P. Epigenetic programming of mesen-chymal stem cells from human adipose tissue. Stem Cell Rev, 2006, 2(4):319-329.
24. Kimura Y, Ozeki M, Inamoto T, et al. Adipose tissue engineering based on human preadipocytes combined with gelatin microspheres containing basic fibroblast growth factor. Biomaterials, 2003, 24(14):2513-2521.
25. Cheung HK, Han TT, Marecak DM, et al. Composite hydrogel scaffolds incorporating decellularized adipose tissue for soft tissue engineering with adipose-derived stem cells. Biomaterials, 2014, 35(6):1914-1923.
26. Mesimäki K, Lindroos B, Törnwall J, et al. Novel maxillary reconstruction with ectopic bone formation by GMP adipose stem cells. Int J Oral Maxillofac Surg, 2009, 38(3):201-209.
27. Gaustad KG, Boquest AC, Anderson BE, et al. Differentiation of human adipose tissue stem cells using extracts of rat cardiomyoc-ytes. Biochem Biophys Res Commun, 2004, 314(2):420-427.
28. Yamada Y, Wang XD, Yokoyama S, et al. Cardiac progenitor cells in brown adipose tissue repaired damaged myocardium. Biochem Biophys Res Commun, 2006, 342(2):662-670.
29. Kim SJ, Park KC, Lee JU, et al. Therapeutic potential of adipose tissue-derived stem cells for liver failure according to the transplan-tation routes. J Korean Surg Soc, 2011, 81(3):176-186.
30. Seo MJ, Suh SY, Bae YC, et al. Differentiation of human adipose stromal cells into hepatic lineage in vitro and in vivo. Biochem Biophys Res Commun, 2005, 328(1):258-264.
31. Timper K, Seboek D, Eberhardt M, et al. Human adipose tissue-derived mesenchymal stem cells differentiate into insulin, somatosta-tin, and glucagon expressing cells. Biochem Biophys Res Commun, 2006, 341(4):1135-1140.
32. Deng M, Gu Y, Liu Z, et al. Endothelial differentiation of human adipose-derived stem cells on polyglycolic acid/polylactic acid mesh. Stem Cells Int, 2015, 2015:350718.
33. Wei J, Xu M, Zhang X, et al. Enhanced osteogenic behavior of ADSCs produced by deproteinized antler cancellous bone and evidence for involvement of ERK signaling pathway. Tissue Eng Part A, 2015, 21(11-12):1810-1821.
34. Liu S, Zhang H, Zhang X, et al. Synergistic angiogenesis promoting effects of extracellular matrix scaffolds and adipose-derived stem cells during wound repair. Tissue Eng Part A, 2011, 17(5-6):725-739.
35. 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.
36. Traktuev DO, Merfeld-Clauss S, Li J, et al. A population of multipotent CD34-positive adipose stromal cells share pericyte and mesenchymal surface markers, reside in a periendothelial location, and stabilize endothelial networks. Circ Res, 2008, 102(1):77-85.
37. Cao Y, Sun Z, Liao L, et al. Human adipose tissue-derived stem cells differentiate into endothelial cells in vitro and improve postnatal neovascularization in vivo. Biochem Biophys Res Commun, 2005, 332(2):370-379.
38. Flynn L, Prestwich GD, Semple JL, et al. Adipose tissue engineering with naturally derived scaffolds and adipose-derived stem cells. Biomaterials, 2007, 28(26):3834-3842.
39. Flynn L, Prestwich GD, Semple JL, et al. Adipose tissue engineering in vivo with adipose-derived stem cells on naturally derived scaffolds. J Biomed Mater Res A, 2009, 89(4):929-941.
40. Zhou Y, Yan Z, Zhang H, et al. Expansion and delivery of adipose-derived mesenchymal stem cells on three microcarriers for soft tissue regeneration. Tissue Eng Part A, 2011, 17(23-24):2981-2997.
41. Dicker A, Le Blanc K, Aström G, et al. Functional studies of mesenchymal stem cells derived from adult human adipose tissue. Exp Cell Res, 2005, 308(2):283-290.
42. von Heimburg D, Hemmrich K, Zachariah S, et al. Oxygen consum-ption in undifferentiated versus differentiated adipogenic mesench-ymal precursor cells. Respir Physiol Neurobiol, 2005, 146(2-3):107-116.
43. Gimble JM, Katz AJ, Bunnell BA. Adipose-derived stem cells for regenerative medicine. Circ Res, 2007, 100(9):1249-1260.
44. Akita S, Akino K, Hirano A, et al. Mesenchymal stem cell therapy for cutaneous radiation syndrome. Health Phys, 2010, 98(6):858-862.
45. Rigotti G, Marchi A, Galiè M, et al. Clinical treatment of radiotherapy tissue damage by lipoaspirate transplant:a healing process mediated by adipose-derived adult stem cells. Plast Reconstr Surg, 2007, 119 (5):1409-1422.
46. Nambu M, Kishimoto S, Nakamura S, et al. Accelerated wound healing in healing-impaired db/db mice by autologous adipose tissue-derived stromal cells combined with atelocollagen matrix. Ann Plast Surg, 2009, 62(3):317-321.
47. Yoshimura K, Sato K, Aoi N, et al. Cell-assisted lipotransfer for cosmetic breast augmentation:supportive use of adipose-derived stem/stromal cells. Aesthetic Plast Surg, 2008, 32(1):48-55.
48. Kamakura T, Ito K. Autologous cell-enriched fat grafting for breast augmentation. Aesthetic Plast Surg, 2011, 35(6):1022-1030.
49. Pérez-Cano R, Vranckx JJ, Lasso JM, et al. Prospective trial of adipose-derived regenerative cell (ADRC)-enriched fat grafting for partial mastectomy defects:the RESTORE-2 trial. Eur J Surg Oncol, 2012, 38(5):382-389.
50. Shin KK, Lee AL, Kim JY, et al. MiR-21 modulates tumor outgrowth induced by human adipose tissue-derived mesenchymal stem cells in vivo. Biochem Biophys Res Commun, 2012, 422(4):633-638.
51. Karnoub AE, Dash AB, Vo AP, et al. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature, 2007, 449(7162):557-563.
52. Kakudo N, Tanaka Y, Morimoto N, et al. Adipose-derived regenera-tive cell (ADRC)-enriched fat grafting:optimal cell concentration and effects on grafted fat characteristics. J Transl Med, 2013, 11:254.

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Application of Adipose-Derived Stem Cells for Repairment and Regeneration of Adipose Tissue: A Review

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