Research progress of the donor factors and experimental factors affecting adipogenic differentiation of adipose derived stem cells_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

LIU Qin , CHEN Fang , WANG Liping ,  ZHANG Yi

Department of Medical Experiments, Wuhan General Hospital of Chinese PLA, Wuhan Hubei, 430070, P.R.China;

Corresponding author：

ZHANG Yi, Email: abcd1566@sina.com

Keywords：

Adipose tissue engineering; adipose derived stem cells; adipogenic differentiation; donor factor; experimental factor

DOI：

10.7507/1002-1892.201704057

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To summarize the donor factors and experimental factors that affect adipogenic differentiation of adipose derived stem cells, so as to provide reference for adipogenic differentiation of adipose derived stem cells. Methods The related research literature about donor factors and experimental factors affecting adipogenic differentiation of adipose derived stem cells in recent years was extensively reviewed and summarized. Results There are a lot of donor factors and experimental factors affecting adipogenic differentiation of adipose derived stem cells, but some of the factors are still controversial, such as donor age, health status, adipose tissue of different parts, and so on. These factors need to be further studied. Conclusion The donor factors and experimental factors that affect adipogenic differentiation of adipose derived stem cells should be deeply studied and the controversial issues should be clarified to lay a solid foundation for the application of adipose derived stem cells in adipose tissue engineering.

Citation： LIU Qin, CHEN Fang, WANG Liping, ZHANG Yi. Research progress of the donor factors and experimental factors affecting adipogenic differentiation of adipose derived stem cells. Chinese Journal of Reparative and Reconstructive Surgery, 2017, 31(11): 1390-1395. doi: 10.7507/1002-1892.201704057 Copy

1.	Langer R, Vacanti JP. Tissue engineering. Science, 1993, 260(5110): 920-926.
2.	张舒, 吕青. 脂肪干细胞在脂肪组织修复重建中的应用. 中国普外基础与临床杂志, 2015, 22(9): 1148-1152.
3.	Zuk PA, Zhu M, Mizuno H, et al. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Engineering, 2001, 7(2): 211-228.
4.	Wang JM, Gu Y, Pan CJ, et al. Isolation, culture and identification of human adipose-derived stem cells. Exp Ther Med, 2017, 13(3):1039-1043.
5.	倪永伟, 周永胜, 刘云松, 等. 人、兔、大鼠脂肪基质细胞的生物学性状对比. 北京大学学报 (医学版), 2009, 41(1): 95-99.
6.	李江璇, 肖丽玲, 饶从强, 等. 人与大鼠脂肪干细胞提取方法及生物学特性的比较研究. 暨南大学学报 (自然科学与医学版), 2015, 36(4): 324-329.
7.	Yang HJ, Kim KJ, Kim MK, et al. The stem cell potential and multipotency of human adipose tissue-derived stem cells vary by cell donor and are different from those of other types of stem cells. Cells Tissues Organs, 2014, 199(5-6): 373-383.
8.	Choudhery MS, Badowski M, Muise A, et al. Donor age negatively impacts adipose tissue-derived mesenchymal stem cell expansion and differentiation. J Transl Med, 2014, 12: 8.
9.	Ye X, Liao C, Liu G, et al. Age-Related Changes in the Regenerative Potential of Adipose-Derived Stem Cells Isolated from the Prominent Fat Pads in Human Lower Eyelids. PLoS One, 2016, 11(11): e0166590.
10.	Beane OS, Fonseca VC, Cooper LL, et al. Impact of aging on the regenerative properties of bone marrow-, muscle-, and adipose-derived mesenchymal stem/stromal cells. PLoS One, 2014, 9(12): e115963.
11.	Ock SA, Lee YM, Park JS, et al. Evaluation of phenotypic, functional and molecular characteristics of porcine mesenchymal stromal/stem cells depending on donor age, gender and tissue source. J Vet Med Sci, 2016, 78(6): 987-995.
12.	刘美辰. 年龄因素对人脂肪间充质干细胞生物学特性的影响. 北京: 中国医学科学院北京协和医学院, 2015.
13.	Ding DC, Chou HL, Hung WT, et al. Human adipose-derived stem cells cultured in keratinocyte serum free medium: Donor’s age does not affect the proliferation and differentiation capacities. J Biomed Sci, 2013, 20: 59.
14.	Kornicka K, Marycz K, Tomaszewski KA, et al. The Effect of Age on Osteogenic and Adipogenic Differentiation Potential of Human Adipose Derived Stromal Stem Cells (hASCs) and the Impact of Stress Factors in the Course of the Differentiation Process. Oxid Med Cell Longev, 2015, 2015: 309169.
15.	De Girolamo L, Stanco D, Salvatori L, et al. Stemness and osteogenic and adipogenic potential are differently impaired in subcutaneous and visceral adipose derived stem cells (ASCs) isolated from obese donors. Int J Immunopathol Pharmacol, 2013, 26(1 Suppl): 11-21.
16.	Pachón-Peña G, Serena C, Ejarque M, et al. Obesity Determines the Immunophenotypic Profile and Functional Characteristics of Human Mesenchymal Stem Cells From Adipose Tissue. Stem Cells Transl Med, 2016, 5(4): 464-475.
17.	Marycz K, Kornicka K, Marędziak M, et al. Equine metabolic syndrome impairs adipose stem cells osteogenic differentiation by predominance of autophagy over selective mitophagy. J Cell Mol Med, 2016, 20(12): 2384-2404.
18.	Inatani H, Yamamoto N, Hayashi K, et al. Do Mesenchymal Stem Cells Derived From Atypical Lipomatous Tumors Have Greater Differentiation Potency Than Cells From Normal Adipose Tissues? Clin Orthop Relat Res, 2017, 475(6): 1693-1701.
19.	Park JR, Lee H, Kim CH, et al. Functional characteristics of mesenchymal stem cells derived from the adipose tissue of a patient with achondroplasia. In Vitro Cell Dev Biol Anim, 2016, 52(5): 545-554.
20.	Russo V, Yu C, Belliveau P, et al. Comparison of human adipose-derived stem cells isolated from subcutaneous, omental, and intrathoracic adipose tissue depots for regenerative applications. Stem Cells Transl Med, 2014, 3(2): 206-217.
21.	Shah FS, Li J, Dietrich M, et al. Comparison of Stromal/Stem Cells Isolated from Human Omental and Subcutaneous Adipose Depots: Differentiation and Immunophenotypic Characterization. Cells Tissues Organs, 2014, 200(3-4): 204-211.
22.	Di Taranto G, Cicione C, Visconti G, et al. Qualitative and quantitative differences of adipose-derived stromal cells from superficial and deep subcutaneous lipoaspirates: a matter of fat. Cytotherapy, 2015, 17(8): 1076-1089.
23.	Siciliano C, Bordin A, Ibrahim M, et al. The adipose tissue of origin influences the biological potential of human adipose stromal cells isolated from mediastinal and subcutaneous fat depots. Stem Cell Res, 2016, 17(2): 342-351.
24.	尉志刚, 王东. 兔不同部位脂肪间充质干细胞成骨能力的差异. 中国医疗前沿, 2012, 7(2): 19-20.
25.	Choudhery MS, Badowski M, Muise A, et al. Subcutaneous Adipose Tissue-Derived Stem Cell Utility Is Independent of Anatomical Harvest Site. Biores Open Access, 2015, 4(1): 131-145.
26.	Kouidhi M, Villageois P, Mounier CM, et al. Characterization of human knee and chin adipose-derived stromal cells. Stem Cells Int, 2015, 2015: 592090.
27.	Ardeshirylajimi A, Rafeie F, Zandi-Karimi A, et al. Fat harvesting site is an important determinant of proliferation and pluripotency of adipose-derived stem cells. Biologicals, 2016, 44(1): 12-18.
28.	Barzelay A, Levy R, Kohn, et al. Power-Assisted Liposuction Versus Tissue Resection for the Isolation of Adipose Tissue-Derived Mesenchymal Stem Cells: Phenotype, Senescence, and Multipotency at Advanced Passages. Aesthet Surg J, 2015, 35(7): NP230-240.
29.	Duscher D, Luan A, Rennert RC, et al. Suction assisted liposuction does not impair the regenerative potential of adipose derived stem cells. J Transl Med, 2016, 14(1): 126.
30.	Gnanasegaran N, Govindasamy V, Musa S, et al. Different isolation methods alter the gene expression profiling of adipose derived stem cells. Int J Med Sci, 2014, 11(4): 391-403.
31.	Chen YW, Wang JR, Liao X, et al. Effect of suction pressures on cell yield and functionality of the adipose-derived stromal vascular fraction. J Plast Reconstr Aesthet Surg, 2017, 70(2): 257-266.
32.	Markarian CF, Frey GZ, Silveira MD, et al. Isolation of adipose-derived stem cells: a comparison among different methods. Biotechnol Lett, 2014, 36(4): 693-702.
33.	Priya N, Sarcar S, Majumdar AS, et al. Explant culture: a simple, reproducible, efficient and economic technique for isolation of mesenchymal stromal cells from human adipose tissue and lipoaspirate. J Tissue Eng Regen Med, 2014, 8(9): 706-716.
34.	Busser H, De Bruyn C, Urbain F, et al. Isolation of adipose-derived stromal cells without enzymatic treatment: expansion, phenotypical, and functional characterization. Stem Cells Dev, 2014, 23(19): 2390-2400.
35.	Lin CY, Huang CH, Wu YK, et al. Maintenance of human adipose derived stem cell (hASC) differentiation capabilities using a 3D culture. Biotechnol Lett, 2014, 36(7): 1529-1537.
36.	Miyamoto Y, Ikeuchi M, Noguchi H, et al. Enhanced Adipogenic Differentiation of Human Adipose-Derived Stem Cells in an In Vitro Microenvironment: The Preparation of Adipose-Like Microtissues Using a Three-Dimensional Culture. Cell Med, 2016, 9(1-2): 35-44.
37.	Roxburgh J, Metcalfe AD, Martin YH, et al. The effect of medium selection on adipose-derived stem cell expansion and differentiation: implications for application in regenerative medicine. Cytotechnology, 2016, 68(4): 957-967.
38.	Sato K, Itoh T, Kato T, et al. Serum-free isolation and culture system to enhance the proliferation and bone regeneration of adipose tissue-derived mesenchymal stem cells. In Vitro Cell Dev Biol Anim, 2015, 51(5): 515-529.
39.	Al-Saqi SH, Saliem M, Asikainen S, et al. Defined serum-free media for in vitro expansion of adipose-derived mesenchymal stem cells. Cytotherapy, 2014, 16(7): 915-926.
40.	李婷, 李勇, 田卫东, 等. 脂肪组织分泌物中蛋白浓度对诱导脂肪干细胞成脂的影响. 四川大学学报 (医学版), 2013, 44(4): 517-521.
41.	Wan Safwani WK, Wong CW, Yong KW. The effects of hypoxia and serum-free conditions on the stemness properties of human adipose-derived stem cells. Cytotechnology, 2016, 68(5): 1859-1872.
42.	Choi J, Chung JH, Kwon GY, et al. Effectiveness of autologous serum as an alternative to fetal bovine serum in adipose-derived stem cell engineering. Cell Tissue Bank, 2013, 14(3):413-422.
43.	邱彦豪, 林詠凯, 蔡錡函, 等. 以血小板浓厚液配方组合取代胎牛血清作为脂肪干細胞之培养液之初步研究. 台湾整形外科医学会杂志, 2016, 25(2): 87-100.
44.	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.
45.	Fotia C, Massa A, Boriani F, et al. Hypoxia enhances proliferation and stemness of human adipose-derived mesenchymal stem cells. Cytotechnology, 2015, 67(6): 1073-1084.
46.	Safwani WK, Makpol S, Sathapan S, et al. Impact of adipogenic differentiation on stemness and osteogenic gene expression in extensive culture of human adipose-derived stem cells. Arch Med Sci, 2014, 10(3): 597-606.
47.	Liu Y, Zhang Z, Zhang C, et al. Adipose-derived stem cells undergo spontaneous osteogenic differentiation in vitro when passaged serially or seeded at low density. Biotech Histochem, 2016, 91(5): 369-376.
48.	Lee KS, Kang HW, Lee HT, et al. Sequential sub-passage decreases the differentiation potential of canine adipose-derived mesenchymal stem cells. Res Vet Sci, 2014, 96(2): 267-275.
49.	El Atat O, Antonios D, Hilal G, et al. An Evaluation of the Stemness, Paracrine, and Tumorigenic Characteristics of Highly Expanded, Minimally Passaged Adipose-Derived Stem Cells. PLoS One, 2016, 11(9): e0162332.
50.	Wang X, Liu C, Li S, et al. Effects of continuous passage on immunomodulatory properties of human adipose-derived stem cells. Cell Tissue Bank, 2015, 16(1): 143-150.
51.	Plastini MA, Kappy N, Chang S, et al. Effect of Population Doublings on Differentiation Capacity of Human Adipose-Derived Stem Cells: Establishing Standard Guidelines for Clinical Translational Applications. Int J Stem Cell Res Transplant, 2016, S2: 001, 1-7.
52.	Yong KW, Pingguan-Murphy B, Xu F, et al. Phenotypic and functional characterization of long-term cryopreserved human adipose-derived stem cells. Sci Rep, 2015, 5: 9596.
53.	López M, Bollag RJ, Yu JC, et al. Chemically Defined and Xeno-Free Cryopreservation of Human Adipose-Derived Stem Cells. PLoS One, 2016, 11(3): e0152161.
54.	James AW, Levi B, Nelson ER, et al. Deleterious effects of freezing on osteogenic differentiation of human adipose-derived stromal cells in vitro and in vivo. Stem Cells Dev, 2011, 20(3): 427-439.
55.	Shah FS, Li J, Zanata F, et al. The Relative Functionality of Freshly Isolated and Cryopreserved Human Adipose-Derived Stromal/Stem Cells. Cells Tissues Organs, 2016. [Epub ahead of print].
56.	Gierloff M, Petersen L, Oberg HH, et al. Adipogenic differentiation potential of rat adipose tissue-derived subpopulations of stromal cells. J Plast Reconstr Aesthet Surg, 2014, 67(10): 1427-1435.
57.	Davies OG, Cooper PR, Shelton RM, et al. Isolation of adipose and bone marrow mesenchymal stem cells using CD29 and CD90 modifies their capacity for osteogenic and adipogenic differentiation. J Tissue Eng, 2015, 6: 2041731415592356.
58.	Song X, Hong C, Zheng Q, et al. Differentiation potential of rabbit CD90-positive cells sorted from adipose-derived stem cells in vitro. In Vitro Cell Dev Biol Anim, 2017, 53(1): 77-82.

1. Langer R, Vacanti JP. Tissue engineering. Science, 1993, 260(5110): 920-926.
2. 张舒, 吕青. 脂肪干细胞在脂肪组织修复重建中的应用. 中国普外基础与临床杂志, 2015, 22(9): 1148-1152.
3. Zuk PA, Zhu M, Mizuno H, et al. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Engineering, 2001, 7(2): 211-228.
4. Wang JM, Gu Y, Pan CJ, et al. Isolation, culture and identification of human adipose-derived stem cells. Exp Ther Med, 2017, 13(3):1039-1043.
5. 倪永伟, 周永胜, 刘云松, 等. 人、兔、大鼠脂肪基质细胞的生物学性状对比. 北京大学学报 (医学版), 2009, 41(1): 95-99.
6. 李江璇, 肖丽玲, 饶从强, 等. 人与大鼠脂肪干细胞提取方法及生物学特性的比较研究. 暨南大学学报 (自然科学与医学版), 2015, 36(4): 324-329.
7. Yang HJ, Kim KJ, Kim MK, et al. The stem cell potential and multipotency of human adipose tissue-derived stem cells vary by cell donor and are different from those of other types of stem cells. Cells Tissues Organs, 2014, 199(5-6): 373-383.
8. Choudhery MS, Badowski M, Muise A, et al. Donor age negatively impacts adipose tissue-derived mesenchymal stem cell expansion and differentiation. J Transl Med, 2014, 12: 8.
9. Ye X, Liao C, Liu G, et al. Age-Related Changes in the Regenerative Potential of Adipose-Derived Stem Cells Isolated from the Prominent Fat Pads in Human Lower Eyelids. PLoS One, 2016, 11(11): e0166590.
10. Beane OS, Fonseca VC, Cooper LL, et al. Impact of aging on the regenerative properties of bone marrow-, muscle-, and adipose-derived mesenchymal stem/stromal cells. PLoS One, 2014, 9(12): e115963.
11. Ock SA, Lee YM, Park JS, et al. Evaluation of phenotypic, functional and molecular characteristics of porcine mesenchymal stromal/stem cells depending on donor age, gender and tissue source. J Vet Med Sci, 2016, 78(6): 987-995.
12. 刘美辰. 年龄因素对人脂肪间充质干细胞生物学特性的影响. 北京: 中国医学科学院北京协和医学院, 2015.
13. Ding DC, Chou HL, Hung WT, et al. Human adipose-derived stem cells cultured in keratinocyte serum free medium: Donor’s age does not affect the proliferation and differentiation capacities. J Biomed Sci, 2013, 20: 59.
14. Kornicka K, Marycz K, Tomaszewski KA, et al. The Effect of Age on Osteogenic and Adipogenic Differentiation Potential of Human Adipose Derived Stromal Stem Cells (hASCs) and the Impact of Stress Factors in the Course of the Differentiation Process. Oxid Med Cell Longev, 2015, 2015: 309169.
15. De Girolamo L, Stanco D, Salvatori L, et al. Stemness and osteogenic and adipogenic potential are differently impaired in subcutaneous and visceral adipose derived stem cells (ASCs) isolated from obese donors. Int J Immunopathol Pharmacol, 2013, 26(1 Suppl): 11-21.
16. Pachón-Peña G, Serena C, Ejarque M, et al. Obesity Determines the Immunophenotypic Profile and Functional Characteristics of Human Mesenchymal Stem Cells From Adipose Tissue. Stem Cells Transl Med, 2016, 5(4): 464-475.
17. Marycz K, Kornicka K, Marędziak M, et al. Equine metabolic syndrome impairs adipose stem cells osteogenic differentiation by predominance of autophagy over selective mitophagy. J Cell Mol Med, 2016, 20(12): 2384-2404.
18. Inatani H, Yamamoto N, Hayashi K, et al. Do Mesenchymal Stem Cells Derived From Atypical Lipomatous Tumors Have Greater Differentiation Potency Than Cells From Normal Adipose Tissues? Clin Orthop Relat Res, 2017, 475(6): 1693-1701.
19. Park JR, Lee H, Kim CH, et al. Functional characteristics of mesenchymal stem cells derived from the adipose tissue of a patient with achondroplasia. In Vitro Cell Dev Biol Anim, 2016, 52(5): 545-554.
20. Russo V, Yu C, Belliveau P, et al. Comparison of human adipose-derived stem cells isolated from subcutaneous, omental, and intrathoracic adipose tissue depots for regenerative applications. Stem Cells Transl Med, 2014, 3(2): 206-217.
21. Shah FS, Li J, Dietrich M, et al. Comparison of Stromal/Stem Cells Isolated from Human Omental and Subcutaneous Adipose Depots: Differentiation and Immunophenotypic Characterization. Cells Tissues Organs, 2014, 200(3-4): 204-211.
22. Di Taranto G, Cicione C, Visconti G, et al. Qualitative and quantitative differences of adipose-derived stromal cells from superficial and deep subcutaneous lipoaspirates: a matter of fat. Cytotherapy, 2015, 17(8): 1076-1089.
23. Siciliano C, Bordin A, Ibrahim M, et al. The adipose tissue of origin influences the biological potential of human adipose stromal cells isolated from mediastinal and subcutaneous fat depots. Stem Cell Res, 2016, 17(2): 342-351.
24. 尉志刚, 王东. 兔不同部位脂肪间充质干细胞成骨能力的差异. 中国医疗前沿, 2012, 7(2): 19-20.
25. Choudhery MS, Badowski M, Muise A, et al. Subcutaneous Adipose Tissue-Derived Stem Cell Utility Is Independent of Anatomical Harvest Site. Biores Open Access, 2015, 4(1): 131-145.
26. Kouidhi M, Villageois P, Mounier CM, et al. Characterization of human knee and chin adipose-derived stromal cells. Stem Cells Int, 2015, 2015: 592090.
27. Ardeshirylajimi A, Rafeie F, Zandi-Karimi A, et al. Fat harvesting site is an important determinant of proliferation and pluripotency of adipose-derived stem cells. Biologicals, 2016, 44(1): 12-18.
28. Barzelay A, Levy R, Kohn, et al. Power-Assisted Liposuction Versus Tissue Resection for the Isolation of Adipose Tissue-Derived Mesenchymal Stem Cells: Phenotype, Senescence, and Multipotency at Advanced Passages. Aesthet Surg J, 2015, 35(7): NP230-240.
29. Duscher D, Luan A, Rennert RC, et al. Suction assisted liposuction does not impair the regenerative potential of adipose derived stem cells. J Transl Med, 2016, 14(1): 126.
30. Gnanasegaran N, Govindasamy V, Musa S, et al. Different isolation methods alter the gene expression profiling of adipose derived stem cells. Int J Med Sci, 2014, 11(4): 391-403.
31. Chen YW, Wang JR, Liao X, et al. Effect of suction pressures on cell yield and functionality of the adipose-derived stromal vascular fraction. J Plast Reconstr Aesthet Surg, 2017, 70(2): 257-266.
32. Markarian CF, Frey GZ, Silveira MD, et al. Isolation of adipose-derived stem cells: a comparison among different methods. Biotechnol Lett, 2014, 36(4): 693-702.
33. Priya N, Sarcar S, Majumdar AS, et al. Explant culture: a simple, reproducible, efficient and economic technique for isolation of mesenchymal stromal cells from human adipose tissue and lipoaspirate. J Tissue Eng Regen Med, 2014, 8(9): 706-716.
34. Busser H, De Bruyn C, Urbain F, et al. Isolation of adipose-derived stromal cells without enzymatic treatment: expansion, phenotypical, and functional characterization. Stem Cells Dev, 2014, 23(19): 2390-2400.
35. Lin CY, Huang CH, Wu YK, et al. Maintenance of human adipose derived stem cell (hASC) differentiation capabilities using a 3D culture. Biotechnol Lett, 2014, 36(7): 1529-1537.
36. Miyamoto Y, Ikeuchi M, Noguchi H, et al. Enhanced Adipogenic Differentiation of Human Adipose-Derived Stem Cells in an In Vitro Microenvironment: The Preparation of Adipose-Like Microtissues Using a Three-Dimensional Culture. Cell Med, 2016, 9(1-2): 35-44.
37. Roxburgh J, Metcalfe AD, Martin YH, et al. The effect of medium selection on adipose-derived stem cell expansion and differentiation: implications for application in regenerative medicine. Cytotechnology, 2016, 68(4): 957-967.
38. Sato K, Itoh T, Kato T, et al. Serum-free isolation and culture system to enhance the proliferation and bone regeneration of adipose tissue-derived mesenchymal stem cells. In Vitro Cell Dev Biol Anim, 2015, 51(5): 515-529.
39. Al-Saqi SH, Saliem M, Asikainen S, et al. Defined serum-free media for in vitro expansion of adipose-derived mesenchymal stem cells. Cytotherapy, 2014, 16(7): 915-926.
40. 李婷, 李勇, 田卫东, 等. 脂肪组织分泌物中蛋白浓度对诱导脂肪干细胞成脂的影响. 四川大学学报 (医学版), 2013, 44(4): 517-521.
41. Wan Safwani WK, Wong CW, Yong KW. The effects of hypoxia and serum-free conditions on the stemness properties of human adipose-derived stem cells. Cytotechnology, 2016, 68(5): 1859-1872.
42. Choi J, Chung JH, Kwon GY, et al. Effectiveness of autologous serum as an alternative to fetal bovine serum in adipose-derived stem cell engineering. Cell Tissue Bank, 2013, 14(3):413-422.
43. 邱彦豪, 林詠凯, 蔡錡函, 等. 以血小板浓厚液配方组合取代胎牛血清作为脂肪干細胞之培养液之初步研究. 台湾整形外科医学会杂志, 2016, 25(2): 87-100.
44. 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.
45. Fotia C, Massa A, Boriani F, et al. Hypoxia enhances proliferation and stemness of human adipose-derived mesenchymal stem cells. Cytotechnology, 2015, 67(6): 1073-1084.
46. Safwani WK, Makpol S, Sathapan S, et al. Impact of adipogenic differentiation on stemness and osteogenic gene expression in extensive culture of human adipose-derived stem cells. Arch Med Sci, 2014, 10(3): 597-606.
47. Liu Y, Zhang Z, Zhang C, et al. Adipose-derived stem cells undergo spontaneous osteogenic differentiation in vitro when passaged serially or seeded at low density. Biotech Histochem, 2016, 91(5): 369-376.
48. Lee KS, Kang HW, Lee HT, et al. Sequential sub-passage decreases the differentiation potential of canine adipose-derived mesenchymal stem cells. Res Vet Sci, 2014, 96(2): 267-275.
49. El Atat O, Antonios D, Hilal G, et al. An Evaluation of the Stemness, Paracrine, and Tumorigenic Characteristics of Highly Expanded, Minimally Passaged Adipose-Derived Stem Cells. PLoS One, 2016, 11(9): e0162332.
50. Wang X, Liu C, Li S, et al. Effects of continuous passage on immunomodulatory properties of human adipose-derived stem cells. Cell Tissue Bank, 2015, 16(1): 143-150.
51. Plastini MA, Kappy N, Chang S, et al. Effect of Population Doublings on Differentiation Capacity of Human Adipose-Derived Stem Cells: Establishing Standard Guidelines for Clinical Translational Applications. Int J Stem Cell Res Transplant, 2016, S2: 001, 1-7.
52. Yong KW, Pingguan-Murphy B, Xu F, et al. Phenotypic and functional characterization of long-term cryopreserved human adipose-derived stem cells. Sci Rep, 2015, 5: 9596.
53. López M, Bollag RJ, Yu JC, et al. Chemically Defined and Xeno-Free Cryopreservation of Human Adipose-Derived Stem Cells. PLoS One, 2016, 11(3): e0152161.
54. James AW, Levi B, Nelson ER, et al. Deleterious effects of freezing on osteogenic differentiation of human adipose-derived stromal cells in vitro and in vivo. Stem Cells Dev, 2011, 20(3): 427-439.
55. Shah FS, Li J, Zanata F, et al. The Relative Functionality of Freshly Isolated and Cryopreserved Human Adipose-Derived Stromal/Stem Cells. Cells Tissues Organs, 2016. [Epub ahead of print].
56. Gierloff M, Petersen L, Oberg HH, et al. Adipogenic differentiation potential of rat adipose tissue-derived subpopulations of stromal cells. J Plast Reconstr Aesthet Surg, 2014, 67(10): 1427-1435.
57. Davies OG, Cooper PR, Shelton RM, et al. Isolation of adipose and bone marrow mesenchymal stem cells using CD29 and CD90 modifies their capacity for osteogenic and adipogenic differentiation. J Tissue Eng, 2015, 6: 2041731415592356.
58. Song X, Hong C, Zheng Q, et al. Differentiation potential of rabbit CD90-positive cells sorted from adipose-derived stem cells in vitro. In Vitro Cell Dev Biol Anim, 2017, 53(1): 77-82.

Chinese Journal of Reparative and Reconstructive Surgery

Research progress of the donor factors and experimental factors affecting adipogenic differentiation of adipose derived stem cells

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