Advertisement

Heterogeneity in Adipose Stem Cells

  • Elio A. Prieto GonzálezEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1123)

Abstract

Adipose stem cells (ASCs) are the basis of procedures intended for tissue regeneration. These cells are heterogeneous, owing to various factors, including the donor age, sex, body mass index, and clinical condition; the isolation procedure (liposuction or fat excision); the place from where the cells were sampled (body site and depth of each adipose depot); culture surface; type of medium (whether supplemented with fetal bovine serum or xeno-free), that affect the principal phenotypic features of ASCs. The features related to ASCs heterogeneity are relevant for the success of therapeutic procedures; these features include proliferation capacity, differentiation potential, immunophenotype, and the secretome. These are important characteristics for the success of regenerative tissue engineering, not only because of their effects upon the reconstruction and healing exerted by ASCs themselves, but also because of the paracrine signaling of ASCs and its impact on recipient tissues. Knowledge of sources of heterogeneity will be helpful in the standardization of ASCs-based procedures. New avenues of research could include evaluation of the effects of the use of more homo1geneous ASCs for specific purposes, the study of ASCs-recipient interactions in heterologous cell transplantation, and the characterization of epigenetic changes in ASCs, as well as investigations of the effect of the metabolome upon ASCs behavior in culture.

Keywords

Heterogeneity Mesenchymal Adipose stem cell Adipose tissue depot Stromal vascular fraction Stemness Xeno-free Immunophenotype Gene expression analysis 

Notes

Acknowledgments

I thank the students from Nutrition Career at ISALUD who made a good research team and helped me in the gathering and selection of the relevant literature. My thanks to my colleagues from CAECIHS and the Interamerican Open University.

References

  1. 1.
    Cleal L, Aldea T, Chau YY (2017) Fifty shades of white: understanding heterogeneity in white adipose stem cells. Adipocyte 6(3):205–216.  https://doi.org/10.1080/21623945.2017.1372871. Epub 2017 Sep 12. ReviewCrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Kocan B, Maziarz A, Tabarkiewicz J, Ochiya T, Banas-Zabczyk A (2017) Trophic activity and phenotype of adipose tissue derived mesenchymal stem cells as a background of their regenerative potential. Stem Cells Int 2017:1653254.  https://doi.org/10.1155/2017/1653254 CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Liu ZY, Ying Z, Velazquez OC (2009) Trafficking and differentiation of mesenchymal stem cells. J Cell Biochem Prospect 106:984–991CrossRefGoogle Scholar
  4. 4.
    Muschler GF, Midura RJ (2002) Connective tissue progenitors: practical concepts for clinical applications. Clin Orthop Relat Res 395:66–80. ReviewCrossRefGoogle Scholar
  5. 5.
    Trojahn Kølle SF, Oliveri RS, Glovinski PV, Elberg JJ, Fischer-Nielsen A, Drzewiecki KT (2012) Importance of mesenchymal stem cells in autologous fat grafting: a systematic review of existing studies. Review. J Plast Surg Hand Surg 46(2):59–68CrossRefPubMedGoogle Scholar
  6. 6.
    Li CY, Wu XY, Tong JB, Yang XX, Zhao JL, Zheng QF, Zhao GB, … Ma ZJ (2015). Comparative analysis of human mesenchymal stem cells from bone marrow and adipose tissue under xeno-free conditions for cell therapy. Stem Cell Res Ther 6(1):55.  https://doi.org/10.1186/s13287-015-0066-5
  7. 7.
    Bacakova L, Zarubova J, Travnickova M, Musilkova J, Pajorova J, Slepicka P, Kasalkova NS, Svorcik V, Kolska Z, Motarjemi H, Molitor M (2018) Stem cells: their source, potency and use in regenerative therapies with focus on adipose-derived stem cells—a review. Biotechnol Adv 36(4):1111–1126.  https://doi.org/10.1016/j.biotechadv.2018.03.011. Epub 2018 Mar 18. ReviewCrossRefPubMedGoogle Scholar
  8. 8.
    Frese L, Dijkman PE, Hoerstrup SP (2016) Adipose tissue-derived stem cells in regenerative medicine. Transfus Med Hemother 43(4):268–274. Epub 2016 Jul 26. ReviewCrossRefPubMedCentralPubMedGoogle Scholar
  9. 9.
    Zuk PA, Zhu M, Ashjian P, De Ugarte DA, Huang JI, Mizuno H, Alfonso ZC, Fraser JK, Benhaim P, Hedrick MH (2002) Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 13:4279–4295CrossRefPubMedCentralPubMedGoogle Scholar
  10. 10.
    Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, Benhaim P, Lorenz HP, Hedrick MH (2001) Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 7(2):211–228CrossRefPubMedGoogle Scholar
  11. 11.
    West CC, Murray IR, González ZN, Hindle P, Hay DC, Stewart KJ, Péault B (2014) Ethical, legal and practical issues of establishing an adipose stem cell bank for research. J Plast Reconstr Aesthet Surg 67(6):745–751.  https://doi.org/10.1016/j.bjps.2014.01.030. Epub 2014 Feb 1. ReviewCrossRefPubMedGoogle Scholar
  12. 12.
    Bourin P, Bunnell BA, Casteilla L, Dominici M, Katz AJ, March KL, Redl H, Rubin JP, Yoshimura K, Gimble JM (2013) Stromal cells from the adipose tissue-derived stromal vascular fraction and culture expanded adipose tissue-derived stromal/stem cells: a joint statement of the International Federation for Adipose Therapeutics and Science (IFATS) and the International Society for Cellular Therapy (ISCT). Cytotherapy 15(6):641–648CrossRefPubMedCentralPubMedGoogle Scholar
  13. 13.
    Bora P, Majumdar AS (2017) Adipose tissue-derived stromal vascular fraction in regenerative medicine: a brief review on biology and translation. Stem Cell Res Ther 8:145.  https://doi.org/10.1186/s13287-017-0598-y CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Bunnell BA, Flaat M, Gagliardi C, Patel B, Ripoll C (2008) Adipose-derived stem cells: isolation, expansion and differentiation. Methods 45(2):115–120. ReviewCrossRefPubMedCentralPubMedGoogle Scholar
  15. 15.
    Aust I, Devlin S, Foster J (2004) Yield of human adipose derived adult stem cells from liposuction aspirates. Cytotherapy 6(1):7–14CrossRefPubMedGoogle Scholar
  16. 16.
    Yu G, Wu X, Dietrich MA, Polk P, Scott LK, Ptitsyn AA, Gimble JM (2010) Yield and characterization of subcutaneous human adipose-derived stem cells by flow cytometric and adipogenic mRNA analyses. Cytotherapy 12:538–546CrossRefPubMedCentralPubMedGoogle Scholar
  17. 17.
    Baer PC, Geiger H (2012) Adipose-derived mesenchymal stromal/stem cells: tissue localization, characterization, and heterogeneity. Stem Cells Int 2012:812693.  https://doi.org/10.1155/2012/812693. Epub 2012 Apr 12CrossRefGoogle Scholar
  18. 18.
    Barry FP, Murphy JM (2004) Mesenchymal stem cells: clinical applications and biological characterization. Int J Biochem Cell Biol 36(4):568–584CrossRefGoogle Scholar
  19. 19.
    Mok PL, Cheong SK, Leong CF (2008) In-vitro differentiation study on isolated human mesenchymal stem cells. Malays J Pathol 30(1):11–19PubMedGoogle Scholar
  20. 20.
    Choe SS, Huh JY, Hwang IJ, Kim JI, Kim JB (2016) Adipose tissue remodelling its role in energy metabolism and metabolic disorders. Front Endocrinol 7:30.  https://doi.org/10.3389/fendo.2016.00030 CrossRefGoogle Scholar
  21. 21.
    Toyoda M, Matsubara Y, Lin K (2009) Characterization and comparison of adipose tissue-derived cells from human subcutaneous and omental adipose tissues. Cell Biochem Funct 27:440–447CrossRefPubMedCentralPubMedGoogle Scholar
  22. 22.
    Prunet-Marcassus B, Cousin B, Caton D, André M, Pénicaud L, Casteilla L (2006) From heterogeneity to plasticity in adipose tissues: site-specific differences. Exp Cell Res 312(6):727–736CrossRefPubMedCentralPubMedGoogle Scholar
  23. 23.
    Di Taranto G, Cicione C, Visconti G, Isgrò MA, Barba M, Di Stasio E, Stigliano E, Bernardini C, Michetti F, Salgarello M, Lattanzi W (2015) Qualitative and quantitative differences of adipose-derived stromal cells from superficial and deep subcutaneous lipoaspirates: a matter of fat. Cytotherapy 17(8):1076–1089.  https://doi.org/10.1016/j.jcyt.2015.04.004. Epub 2015 May 19CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Kwok KH, Lam KS, Xu A (2016) Heterogeneity of white adipose tissue: molecular basis and clinical implications. Exp Mol Med 48:e215.  https://doi.org/10.1038/emm.2016.5. ReviewCrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Chau YY, Bandiera R, Serrels A, Martínez-Estrada OM, Qing W, Lee M, Slight J, Thornburn A, Berry R, McHaffie S, Stimson RH, Walker BR, Chapuli RM, Schedl A, Hastie N (2014) Visceral and subcutaneous fat have different origins and evidence supports a mesothelial source. Nat Cell Biol 16(4):367–375.  https://doi.org/10.1038/ncb2922. Epub 2014 Mar 9CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Porter SA, Massaro JM, Hoffmann U, Vasan RS, O’Donnel CJ, Fox CS (2009) Abdominal subcutaneous adipose tissue: a protective fat depot? Diabetes Care 32(6):1068–1075CrossRefPubMedCentralPubMedGoogle Scholar
  27. 27.
    Nedergaard J, Bengtsson T, Cannon B (2007) Unexpected evidence for active brown adipose tissue in adult humans. Am J Physiol Endocrinol Metab 293(2):E444–E452CrossRefPubMedCentralPubMedGoogle Scholar
  28. 28.
    Scheller EI, Cawthorn WP, Burr AA, Horowitz MC, Mac Dougald OA (2016) Marrow adipose tissue: trimming the fat. Trends Endocrinol Metab 27:392–403.  https://doi.org/10.1016/j.tem.2016 CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Macotela Y, Emanuelli B, Mori MA, Gesta S, Schulz TJ, Tseng YH, Kahn CR. (2012) Intrinsic differences in adipocyte precursor cells from different white fat depots. Diabetes 61 (17):1691–1699.  https://doi.org/10.2337/db11-1753. Epub 2012 May 17CrossRefPubMedCentralPubMedGoogle Scholar
  30. 30.
    Kim B, Lee B, Kim MK et al (2016) Gene expression profiles of human subcutaneous and visceral adipose-derived stem cells. Cell Biochem Funct 34(8):563–571CrossRefPubMedCentralPubMedGoogle Scholar
  31. 31.
    Tang Y, Pan ZY, Zou Y, He Y, Yang PY, Tang QQ, Yin F (2017) A comparative assessment of adipose-derived stem cells from subcutaneous and visceral fat as a potential cell source for knee osteoarthritis treatment. J Cell Mol Med 21(9):2153–2162.  https://doi.org/10.1111/jcmm.13138. Epub 2017 Apr 4CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Passaro A, Miselli MA, Sanz JM, Dalla Nora E, Morieri ML, Colonna R, Pišot R, Zuliani G (2017) Gene expression regional differences in human subcutaneous adipose tissue. BMC Genomics 18(1):202.  https://doi.org/10.1186/s12864-017-3564-2 CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Birbrair A, Zhang T, Wang ZM, Messi ML, Mintz A, Delbono O (2015) Pericytes at the intersection between tissue regeneration and pathology. Clin Sci (Lond) 128(2):81–93.  https://doi.org/10.1042/CS20140278. ReviewCrossRefGoogle Scholar
  34. 34.
    Birbrair A (2017) Stem cell microenvironments and beyond. Adv Exp Med Biol 1041:1–3.  https://doi.org/10.1007/978-3-319-69194-7_1 CrossRefPubMedGoogle Scholar
  35. 35.
    Corselli M, Chen C-W, Sun B, Yap S, Rubin JP, Péault B (2012) The tunica adventitia of human arteries and veins as a source of mesenchymal stem cells. Stem Cells Dev 21(8):1299–1308.  https://doi.org/10.1089/scd.2011.0200 CrossRefPubMedGoogle Scholar
  36. 36.
    Traktuev DO, Prater DN, Merfeld-Clauss S, Sanjeevaiah AR, Saadatzadeh MR, Murphy M, Johnstone BH, Ingram DA, March KL (2009) Robust functional vascular network formation in vivo by cooperation of adipose progenitor and endothelial cells. Circ Res 104(12):1410–1420.  https://doi.org/10.1161/CIRCRESAHA.108.190926. Epub 2009 May 1CrossRefPubMedGoogle Scholar
  37. 37.
    Hardy WR, Moldovan NI, Moldovan L, Livak KJ, Datta K, Goswami C, Corselli M, Traktuev DO, Murray IR, Péault B, March K (2017) Transcriptional networks in single perivascular cells sorted from human adipose tissue reveal a hierarchy of mesenchymal stem cells. Stem Cells 35(5):1273–1289.  https://doi.org/10.1002/stem.2599. Epub 2017 Mar 19CrossRefPubMedGoogle Scholar
  38. 38.
    Kilinc MO, Santidrian A, Minev I, Toth R, Draganov D, Nguyen D, Lander E, Berman M, Minev B, Szalay AA (2018) The ratio of ADSCs to HSC-progenitors in adipose tissue derived SVF may provide the key to predict the outcome of stem-cell therapy. Clin Transl Med 7(1):5.  https://doi.org/10.1186/s40169-018-0183- CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Navarro A, Marín S, Riol N, Carbonell-Uberos F, Miñana MD (2014) Human adipose tissue-resident monocytes exhibit an endothelial-like phenotype and display angiogenic properties. Stem Cell Res Ther 5(2):50CrossRefPubMedCentralPubMedGoogle Scholar
  40. 40.
    Prockop DJ, Brenner M, Fibbe WE, Horwitz E, Le Blanc K, Phinney DG, Simmons PJ, Sensebe L, Keating A (2010) Defining the risks of mesenchymal stromal cell therapy. Cytotherapy 12(5):576–578CrossRefPubMedGoogle Scholar
  41. 41.
    Yoshimura K, Shigeura T, Matsumoto D, Sato T, Takaki Y, Aiba-Kojima E, Sato K, Inoue K, Nagase T, Koshima I, Gonda K (2006) Characterization of freshly isolated and cultured cells derived from the fatty and fluid portions of liposuction aspirates. J Cell Physiol 208(1):64–76CrossRefPubMedGoogle Scholar
  42. 42.
    Astori G, Vignati F, Bardelli S, Tubio M, Gola M, Albertini V, Bambi F, Scali G, Castelli D, Rasini V, Soldati G, Moccetti TJ (2007) “In vitro” and multicolor phenotypic characterization of cell subpopulations identified in fresh human adipose tissue stromal vascular fraction and in the derived mesenchymal stem cells. Transl Med 5:55CrossRefGoogle Scholar
  43. 43.
    Guglielmi V, Sbraccia P (2018) Obesity phenotypes: depot-differences in adipose tissue and their clinical implications. Eat Weight Disord 23(1):3–14.  https://doi.org/10.1007/s40519-017-0467-9. Epub 2017 Dec 11. ReviewCrossRefPubMedGoogle Scholar
  44. 44.
    Lynes MD, Tseng YH (2018) Deciphering adipose tissue heterogeneity. Ann N Y Acad Sci 1411(1):5–20.  https://doi.org/10.1111/nyas.13398. Epub 2017 Aug 1. ReviewCrossRefPubMedGoogle Scholar
  45. 45.
    Schneider S, Unger M, van Griensven M, Balmayor ER (2017) Adipose-derived mesenchymal stem cells from liposuction and resected fat are feasible sources for regenerative medicine. Eur J Med Res 22:17.  https://doi.org/10.1186/s40001-017-0258-9 CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Alharbi Z, Opländer C, Almakadi S, Fritz A, Vogt M, Pallua N (2013) Conventional vs. micro-fat harvesting: how fat harvesting technique affects tissue-engineering approaches using adipose tissue-derived stem/stromal cells. J Plast Reconstr Aesthet Surg 66(9):1271–1278.  https://doi.org/10.1016/j.bjps.2013.04.015. Epub 2013 Jun 2CrossRefPubMedGoogle Scholar
  47. 47.
    Boquest AC, Shahdadfar A, Frønsdal K, Sigurjonsson O, Tunheim SH, Collas P, Brinchmann JE (2005) Isolation and transcription profiling of purified uncultured human stromal stem cells: alteration of gene expression after in vitro cell culture. Mol Biol Cell 16(3):1131–1141. Epub 2005 Jan 5CrossRefPubMedCentralPubMedGoogle Scholar
  48. 48.
    Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Dj P, Horwitz E (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8(4):315–317CrossRefPubMedCentralGoogle Scholar
  49. 49.
    Oedayrajsingh-Varma M, Ham S, Knippenberg M, Helder MN, Klein-Nulend J, Schouten T, Mjpf R, Milligen F (2006) Adipose tissue-derived mesenchymal stem cell yield and growth characteristics are affected by the tissue-harvesting procedure. Cytotherapy 8(2):166–177.  https://doi.org/10.1080/14653240600621125 CrossRefPubMedGoogle Scholar
  50. 50.
    Parsons AM, Ciombor DM, Liu PY, Darling EM (2018) Regenerative potential and inflammation-induced secretion profile of human adipose-derived stromal vascular cells are influenced by donor variability and prior breast cancer diagnosis. Stem Cell Rev 14(4):546–557.  https://doi.org/10.1007/s12015-018-9813-1 CrossRefPubMedGoogle Scholar
  51. 51.
    Jurgens WJFM, Oedayrajsingh-Varma MJ, Helder MN et al (2008) Effect of tissue-harvesting site on yield of stem cells derived from adipose tissue: implications for cell-based therapies. Cell Tissue Res 332(3):415–426CrossRefPubMedCentralPubMedGoogle Scholar
  52. 52.
    Palumbo P, Lombardi F, Siragusa G, Cifone MG, Cinque B, Giuliani M (2018) Methods of isolation, characterization and expansion of human adipose-derived stem cells (ASCs): an overview. Int J Mol Sci 19(7):e1897. Epub 2018 Jun 28CrossRefPubMedGoogle Scholar
  53. 53.
    Reumann MK, Linnemann C, Aspera-Werz RH, Arnold S, Held M, Seeliger C, Nussler AK, Ehnert S (2018) Donor site location is critical for proliferation, stem cell capacity, and osteogenic differentiation of adipose mesenchymal stem/stromal cells: implications for bone tissue engineering. Int J Mol Sci 19(7):pii: E1868.  https://doi.org/10.3390/ijms19071868 CrossRefGoogle Scholar
  54. 54.
    Tsekouras A, Mantas D, Tsilimigras DI, Moris D, Kontos M, Zografos GC (2017) Comparison of the viability and yield of adipose-derived stem cells (ASCs) from different donor areas. In Vivo 31(6):1229–1234PubMedPubMedCentralGoogle Scholar
  55. 55.
    Siddappa R, Licht R, van Blitterswijk C, de Boer J (2007) Donor variation and loss of multipotency during in vitro expansion of human mesenchymal stem cells for bone tissue engineering. J Orthop Res 25:1029–1041CrossRefPubMedGoogle Scholar
  56. 56.
    Shao X, Zhang C, Sun MA, Lu X, Xie H (2014) Deciphering the heterogeneity in DNA methylation patterns during stem cell differentiation and reprogramming. BMC Genomics 15:978.  https://doi.org/10.1186/1471-2164-15-978 CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Van Hamerlen V, Skurk T, Röhrig K et al (2003) Effect of BMI and age on adipose tissue cellularity and differentiation capacity in women. Int J Obes Relat Metab Disord 27(8):889–895CrossRefGoogle Scholar
  58. 58.
    De Girolamo L, Stanco D, Salvatori L, Coroniti G, Arrigoni E, Silecchia G, Russo MA, Niada S, Petrangeli E, Brini AT (2013) 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 26(1 Suppl):11–21CrossRefPubMedGoogle Scholar
  59. 59.
    Frazier TP, Gimble JM, Devay JW, Tucker HA, Chiu ES, Rowan BG (2013) Body mass index affects proliferation and osteogenic differentiation of human subcutaneous adipose tissue-derived stem cells. BMC Cell Biol 14:34.  https://doi.org/10.1186/1471-2121-14-34 CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Isakson P, Hammarstedt A, Gustafson B, Smith U (2009) Impaired preadipocyte differentiation in human abdominal obesity: role of Wnt, tumor necrosis factor-alpha, and inflammation. Diabetes 58(7):1550–1557CrossRefPubMedCentralPubMedGoogle Scholar
  61. 61.
    Perez LM, Bernal A, San MN, Lorenzo M, Fernandez-Veledo S, Galvez BG (2013) Metabolic rescue of obese adipose-derived stem cells by Lin28/Let7 pathway. Diabetes 62:2368–2379.  https://doi.org/10.2337/db12-1220 CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Varghese J, Griffin M, Mosahebi A, Butler P (2017) Systematic review of patient factors affecting adipose stem cell viability and function: implications for regenerative therapy. Stem Cell Res Ther 8:45.  https://doi.org/10.1186/s13287-017-0483-8 CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Yang HJ, Kim KJ, Kim MK, Lee SJ, Ryu YH, Seo BF, Oh DY, Ahn ST, Lee HY, Rhie JW (2014) 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 199(5–6):373–383.  https://doi.org/10.1159/000369969. Epub 2015 Mar 25CrossRefPubMedGoogle Scholar
  64. 64.
    Mundstock E, Sarria EE, Zatti H, Mattos Louzada F, Kich Grun L, Herbert Jones M, Guma FT, Mazzola In Memoriam J, Epifanio M, Stein RT, Barbé-Tuana FM, Mattiello R (2015) Effect of obesity on telomere length: systematic review and meta-analysis. Obesity (Silver Spring) 23(11):2165–2174.  https://doi.org/10.1002/oby.21183. Epub 2015 Sep 26. ReviewCrossRefGoogle Scholar
  65. 65.
    Stab BR, Martinez L, Grismaldo A, Lerma A, Gutiérrez ML, Barrera LA, Albarracín SL (2016) Mitochondrial functional changes characterization in young and senescent human adipose derived MSCs. Front Aging Neurosci 8:299.  https://doi.org/10.3389/fnagi.2016.00299 CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Eljaafari A, Robert M, Chehimi M, Chanon S, Durand C, Vial G, Bendridi N, Madec AM, Disse E, Laville M, Rieusset J, Lefai E, Vidal H, Pirola L (2015) Adipose tissue-derived stem cells from obese subjects contribute to inflammation and reduced insulin response in adipocytes through differential regulation of the Th1/Th17 balance and monocyte activation. Diabetes 64(7):2477–2488.  https://doi.org/10.2337/db15-0162. Epub 2015 Mar 12CrossRefPubMedGoogle Scholar
  67. 67.
    Baptista LS, Silva KR, Borojevic R (2015) Obesity and weight loss could alter the properties of adipose stem cells? World J Stem Cells 7(1):165–173.  https://doi.org/10.4252/wjsc.v7.i1.165 CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Silva KR, Côrtes I, Liechocki S, Carneiro JR, Souza AA, Borojevic R, Maya-Monteiro CM, Baptista LS (2017) Characterization of stromal vascular fraction and adipose stem cells from subcutaneous, preperitoneal and visceral morbidly obese human adipose tissue depots. PLoS One 12(3):e0174115.  https://doi.org/10.1371/journal.pone.0174115. eCollection 2017CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Russo V, Yu C, Belliveau P, Hamilton A, Flynn LE (2014) Comparison of human adipose-derived stem cells isolated from subcutaneous, omental, and intrathoracic adipose tissue depots for regenerative applications. Stem Cells Transl Med 3(2):206–217.  https://doi.org/10.5966/sctm.2013-0125. Epub 2013 Dec 20CrossRefPubMedGoogle Scholar
  70. 70.
    Boulet N, Estève D, Bouloumié A, Galitzky J (2013) Cellular heterogeneity in superficial and deep subcutaneous adipose tissues in overweight patients. J Physiol Biochem 69(3):575–583.  https://doi.org/10.1007/s13105-012-0225-4. Epub 2012 Nov 25CrossRefPubMedGoogle Scholar
  71. 71.
    Dufrane D (2017) Impact of age on human adipose stem cells for bone tissue engineering. Cell Transplant 26(9):1496–1504.  https://doi.org/10.1177/0963689717721203 CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Fickert S, Schröter-Bobsin U, Gross AF, Hempel U, Wojciechowski C, Rentsch C, Corbeil D, Günther KP (2011) Human mesenchymal stem cell proliferation and osteogenic differentiation during long-term ex vivo cultivation is not age dependent. J Bone Miner Metab 29(2):224–235.  https://doi.org/10.1007/s00774-010-0215-y. Epub 2010 Sep 2CrossRefPubMedGoogle Scholar
  73. 73.
    Mohamed-Ahmed S, Fristad I, Lie SA, Suliman S, Mustafa K, Vindenes H, Idris SB (2018) Adipose-derived and bone marrow mesenchymal stem cells: a donor-matched comparison. Stem Cell Res Ther 9(1):168.  https://doi.org/10.1186/s13287-018-0914-1. CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Choudhery MS, Badowski M, Muise A, Pierce J, Harris DT (2014) Donor age negatively impacts adipose tissue-derived mesenchymal stem cell expansion and differentiation. J Transl Med 12:8.  https://doi.org/10.1186/1479-5876-12-8 CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Nugraha Setyawan EM, Oh HJ, Kim MJ, Kim GA, Lee SH, Choi YB, Ra K, Lee BC (2018) Despite the donor’s age, human adipose-derived stem cells enhance the maturation and development rates of porcine oocytes in a co-culture system. Theriogenology 115:57–64.  https://doi.org/10.1016/j.theriogenology.2017.12.024. Epub 2017 Dec 12CrossRefPubMedGoogle Scholar
  76. 76.
    Liu M, Lei H, Dong P, Fu X, Yang Z, Yang Y, Ma J, Liu X, Cao Y, Xiao R (2017) Adipose-derived mesenchymal stem cells from the elderly exhibit decreased migration and differentiation abilities with senescent properties. Cell Transplant 26(9):1505–1519.  https://doi.org/10.1177/0963689717721221 CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Beane OS, Fonseca VC, Cooper LL, Koren G, Darling EM (2014) Impact of aging on the regenerative properties of bone marrow-, muscle-, and adipose-derived mesenchymal stem/stromal cells. PLoS One 9(12):e115963.  https://doi.org/10.1371/journal.pone.0115963. eCollectionCrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Kornicka K, Marycz K, Tomaszewski KA, Marędziak M, Śmieszek A (2015) 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 2015:309169.  https://doi.org/10.1155/2015/309169. Epub 2015 Jul 12CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Jin Y, Yang L, Zhang Y, Gao W, Yao Z, Song Y, Wang Y (2017) Effects of age on biological and functional characterization of adipose-derived stem cells from patients with end-stage liver disease. Mol Med Rep 16:3510–3518.  https://doi.org/10.3892/mmr.2017.6967 CrossRefPubMedGoogle Scholar
  80. 80.
    Kokai LE, Traktuev DO, Zhang L, Merfeld-Clauss S, DiBernardo G, Lu H, Marra KG, Donnenberg A, Donnenberg V, Meyer EM, Fodor PB, March KL, Rubin JP (2017) Adipose stem cell function maintained with age: an intra-subject study of long-term cryopreserved cells. Aesthet Surg J 37(4):454–463.  https://doi.org/10.1093/asj/sjw197 CrossRefPubMedGoogle Scholar
  81. 81.
    Ye X, Liao C, Liu G, Xu Y, Tan J et al (2016) Age-related changes in the regenerative potential of adipose-derived stem cells isolated from the prominent fat pads in human lower eyelids. PLoS One 11(11):e0166590.  https://doi.org/10.1371/journal.pone.0166590 CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Shan X, Roberts C, Kim EJ, Brenner A, Grant G, Percec I (2017) Transcriptional and cell cycle alterations mark aging of primary human adipose-derived stem cells. Stem Cells 35(5):1392–1401.  https://doi.org/10.1002/stem.2592. Epub 2017 Mar 5CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Minteer DM, Marra KG, Rubin JP (2015) Adipose stem cells: biology, safety, regulation, and regenerative potential. Clin Plast Surg 42(2):169–179.  https://doi.org/10.1016/j.cps.2014.12.007. ReviewCrossRefPubMedGoogle Scholar
  84. 84.
    Shan X, Roberts C, Lan Y, Percec I (2018) Age alters chromatin structure and expression of sumo proteins under stress conditions in human adipose-derived stem cells. Sci Rep 8(1):11,502.  https://doi.org/10.1038/s41598-018-29775-y CrossRefGoogle Scholar
  85. 85.
    Baer PC, Griesche N, Luttmann W, Schubert R, Luttmann A, Geiger H (2010) Human adipose-derived mesenchymal stem cells in vitro: evaluation of an optimal expansion medium preserving stemness. Cytotherapy 12(1):96–106.  https://doi.org/10.3109/14653240903377045 CrossRefPubMedGoogle Scholar
  86. 86.
    Kim DS, Lee MW, Yoo KH, Lee T-H, Kim HJ et al (2014) Gene expression profiles of human adipose tissue-derived mesenchymal stem cells are modified by cell culture density. PLoS One 9(1):e83363.  https://doi.org/10.1371/journal.pone.0083363 CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Calabrese G, Giuffrida R, Forte S, Fabbi C, Figallo E, Salvatorelli L, Memeo L, Parenti R, Gulisano M, Gulino R (2017) Human adipose-derived mesenchymal stem cells seeded into a collagen-hydroxyapatite scaffold promote bone augmentation after implantation in the mouse. Sci Rep 7(1):7110.  https://doi.org/10.1038/s41598-017-07672-0 CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Zanicotti DG, Duncan WJ, Seymour GJ, Coates DE (2018) Effect of titanium surfaces on the osteogenic differentiation of human adipose-derived stem cells. Int J Oral Maxillofac Implants 33(3):e77–e87.  https://doi.org/10.11607/jomi.5810 CrossRefPubMedGoogle Scholar
  89. 89.
    Riis S, Nielsen FM, Pennisi CP, Zachar V, Fink T (2016) Comparative analysis of media and supplements on initiation and expansion of adipose-derived stem cells. Stem Cells Transl Med 5(3):314–324.  https://doi.org/10.5966/sctm.2015-0148 CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    McKee C, Chaudhry GR (2017) Advances and challenges in stem cell culture. Colloids Surf B Biointerfaces 159:62–77.  https://doi.org/10.1016/j.colsurfb.2017.07.051. Epub 2017 Jul 27CrossRefPubMedGoogle Scholar
  91. 91.
    Rowlands AS, George PA, Cooper-White JJ (2008) Directing osteogenic and myogenic differentiation of MSCs: interplay of stiffness and adhesive ligand presentation. Am J Physiol 295(4):C1037–C1044CrossRefGoogle Scholar
  92. 92.
    Chaudhary JK, Rath PC (2017) Microgrooved-surface topography enhances cellular division and proliferation of mouse bone marrow-derived mesenchymal stem cells. PLoS One 12(8):e0182128.  https://doi.org/10.1371/journal.pone.0182128. eCollectionCrossRefPubMedPubMedCentralGoogle Scholar
  93. 93.
    Hiew VV, Simat SFB, Teoh PL (2018) The advancement of biomaterials in regulating stem cell fate. Stem Cell Rev 14(1):43–57.  https://doi.org/10.1007/s12015-017-9764-y CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Leach JK, Whitehead J (2018) Materials-directed differentiation of mesenchymal stem cells for tissue engineering and regeneration. ACS Biomater Sci Eng 4(4):1115–1127.  https://doi.org/10.1021/acsbiomaterials.6b00741. Epub 2017 Mar 14CrossRefPubMedGoogle Scholar
  95. 95.
    Marinkovic M, Block TJ, Rakian R, Li Q, Wang E, Reilly MA, Dean DD, Chen XD (2016) One size does not fit all: developing a cell-specific niche for in vitro study of cell behavior. Matrix Biol 52–54:426–441.  https://doi.org/10.1016/j.matbio.2016.01.004. Epub 2016 Jan 15CrossRefPubMedPubMedCentralGoogle Scholar
  96. 96.
    Mauney JR, Volloch V, Kaplan DL (2005) Matrix-mediated retention of adipogenic differentiation potential by human adult bone marrow-derived mesenchymal stem cells during ex vivo expansion. Biomaterials 26(31):6167–6175CrossRefPubMedGoogle Scholar
  97. 97.
    Kishimoto S, Ishihara M, Mori Y, Takikawa M, Hattori H, Nakamura S, Sato T (2013) Effective expansion of human adipose-derived stromal cells and bone marrow-derived mesenchymal stem cells cultured on a fragmin/protamine nanoparticles-coated substratum with human platelet-rich plasma. J Tissue Eng Regen Med 7(12):955–964.  https://doi.org/10.1002/term.1488. Epub 2012 Mar 31CrossRefPubMedGoogle Scholar
  98. 98.
    Xiong Y, He J, Zhang W, Zhou G, Cao Y, Liu W (2015) Retention of the stemness of mouse adipose-derived stem cells by their expansion on human bone marrow stromal cell-derived extracellular matrix. Tissue Eng Part A 21:1886–1894CrossRefPubMedGoogle Scholar
  99. 99.
    Ireland RG, Simmons CA (2015) Human pluripotent stem cell mechanobiology: manipulating the biophysical microenvironment for regenerative medicine and tissue engineering applications. Stem Cells 33:3187–3196CrossRefPubMedGoogle Scholar
  100. 100.
    Tristan P, Driscoll TP, Cosgrove BD, JinHeo S, Shurden ZE, Mauck RE (2015) Cytoskeletal to nuclear strain transfer regulates YAP signaling in mesenchymal stem cells. Biophys J 108(12):2783–2793.  https://doi.org/10.1016/j.bpj.2015.05.010 CrossRefGoogle Scholar
  101. 101.
    Cramer C, Freisinger E, Jones RK, Slakey DP, Dupin CL, Newsome ER, Alt EU, Izadpanah R (2010) Persistent high glucose concentrations alter the regenerative potential of mesenchymal stem cells. Stem Cells Dev 19:1875–1884.  https://doi.org/10.1089/scd.2010.0009 CrossRefPubMedPubMedCentralGoogle Scholar
  102. 102.
    Hankamolsiri W, Manochantr S, Tantrawatpan C, Tantikanlayaporn D, Pairath Tapanadechopone P, Kheolamai P (2016) The effects of high glucose on adipogenic and osteogenic differentiation of gestational tissue-derived MSCs. Stem Cells Int 2016:15.  https://doi.org/10.1155/2016/9674614 CrossRefGoogle Scholar
  103. 103.
    Marks PW, Witten CM, Califf RM (2017) Clarifying stem-cell therapy’s benefits and risks. N Engl J Med 376:1007–1009.  https://doi.org/10.1056/NEJMp1613723 CrossRefPubMedPubMedCentralGoogle Scholar
  104. 104.
    Stern-Straeter J, Bonaterra GA, Juritz S, Birk R, Goessler UR, Bieback K, Bugert P, Schultz J, Hörmann K, Kinscherf R, Faber A (2014) Evaluation of the effects of different culture media on the myogenic differentiation potential of adipose tissue- or bone marrow-derived human mesenchymal stem cells. Int J Mol Med 33(1):160–170.  https://doi.org/10.3892/ijmm.2013.1555. Epub 2013 Nov 13CrossRefPubMedPubMedCentralGoogle Scholar
  105. 105.
    Lee MS, Youn C, Kim JH, Park BJ, Ahn J, Hong S, Kim YD, Shin YK, Park SG (2017) Enhanced cell growth of adipocyte-derived mesenchymal stem cells using chemically-defined serum-free media. Int J Mol Sci 18(8):pii: E1779.  https://doi.org/10.3390/ijms18081779 CrossRefGoogle Scholar
  106. 106.
    Blázquez-Prunera A, Díez JM, Gajardo R, Grancha S (2017) Human mesenchymal stem cells maintain their phenotype, multipotentiality, and genetic stability when cultured using a defined xeno-free human plasma fraction. Stem Cell Res Ther 8(1):103.  https://doi.org/10.1186/s13287-017-0552- CrossRefPubMedPubMedCentralGoogle Scholar
  107. 107.
    Lindroos B, Boucher S, Chase L, Kuokkanen H, Huhtala H, Haataja R, Vemuri M, Suuronen R, Miettinen S (2009) Serum-free, xeno-free culture media maintain the proliferation rate and multipotentiality of adipose stem cells in vitro. Cytotherapy 11(7):958–972.  https://doi.org/10.3109/14653240903233081 CrossRefPubMedPubMedCentralGoogle Scholar
  108. 108.
    Oikonomopoulos A, van Deen WK, Manansala AR, Lacey PN, Tomakili TA, Ziman A, Hommes DW (2015) Optimization of human mesenchymal stem cell manufacturing: the effects of animal/xeno-free media. Sci Rep 5:16,570.  https://doi.org/10.1038/srep16570 CrossRefGoogle Scholar
  109. 109.
    Lai F, Kakudo N, Morimoto N, Taketani S, Hara T, Ogawa T, Kusumoto K (2018) Platelet-rich plasma enhances the proliferation of human adipose stem cells through multiple signaling pathways. Stem Cell Res Ther 9(1):107.  https://doi.org/10.1186/s13287-018-0851-z CrossRefPubMedPubMedCentralGoogle Scholar
  110. 110.
    Miyagi-Shiohira C, Kobayashi N, Saitoh I, Watanabe M, Noguchi Y, Matsushita M, Noguchi H (2016) Evaluation of serum-free, xeno-free cryopreservation solutions for human adipose-derived mesenchymal stem cells. Cell Med 9(1–2):15–20.  https://doi.org/10.3727/215517916X693122 CrossRefPubMedPubMedCentralGoogle Scholar
  111. 111.
    Volz AC, Kluger PJ (2018) Completely serum-free and chemically defined adipocyte development and maintenance. Cytotherapy 20(4):576–588.  https://doi.org/10.1016/j.jcyt.2018.01.004. Epub 2018 Mar 1CrossRefPubMedGoogle Scholar
  112. 112.
    Escobar CH, Chaparro O (2016) Xeno-free extraction, culture, and cryopreservation of human adipose-derived mesenchymal stem cells. Stem Cells Transl Med 5(3):358–365.  https://doi.org/10.5966/sctm.2015-0094. Epub 2016 Feb 2CrossRefPubMedPubMedCentralGoogle Scholar
  113. 113.
    Lensch M, Muise A, White L, Badowski M, Harris D (2018) Comparison of synthetic media designed for expansion of adipose-derived mesenchymal stromal cells. Biomedicine 6(2):pii: E54.  https://doi.org/10.3390/biomedicines6020054 CrossRefGoogle Scholar
  114. 114.
    Rajala K, Lindroos B, Hussein SM, Lappalainen RS, Pekkanen-Mattila M, Inzunza J, Skottman H (2010) A defined and xeno-free culture method enabling the establishment of clinical-grade human embryonic, induced pluripotent and adipose stem cells. PLoS One 5(4):e10246.  https://doi.org/10.1371/journal.pone.0010246 CrossRefPubMedPubMedCentralGoogle Scholar
  115. 115.
    Kim JH, Jee MK, Lee SY, Han TH, Kim BS, Kang KS, Kang SK (2009) Regulation of adipose tissue stromal cells behaviors by endogenic Oct4 expression control. PLoS One 2(9):e7166.  https://doi.org/10.1371/journal.pone.000716 CrossRefGoogle Scholar
  116. 116.
    Kashyap V, Rezende NC, Scotland KB, Shaffer SM, Persson JL, Gudas LJ, Mongan NP (2009) Regulation of stem cell pluripotency and differentiation involves a mutual regulatory circuit of the NANOG, OCT4, and SOX2 pluripotency transcription factors with polycomb repressive complexes and stem cell microRNAs. Stem Cells Dev 18(7):1093–1108.  https://doi.org/10.1089/scd.2009.0113. ReviewCrossRefPubMedPubMedCentralGoogle Scholar
  117. 117.
    Ambele MA, Dessels C, Durandt C, Pepper MS (2016) Genome-wide analysis of gene expression during adipogenesis in human adipose-derived stromal cells reveals novel patterns of gene expression during adipocyte differentiation. Stem Cell Res 16(3):725–734.  https://doi.org/10.1016/j.scr.2016.04.011. Epub 2016 Apr 19CrossRefPubMedGoogle Scholar
  118. 118.
    Satish L, Krill-Burger JM, Gallo PH, Etages SD, Liu F, Philips BJ, Ravuri S, Marra KG, LaFramboise WA, Kathju S, Rubin JP (2015) Expression analysis of human adipose-derived stem cells during in vitro differentiation to an adipocyte lineage. BMC Med Genomics 24(8):41.  https://doi.org/10.1186/s12920-015-0119-8 CrossRefGoogle Scholar
  119. 119.
    Shi C, Huang F, Gu X, Zhang M, Wen J, Wang X, You L, Cui X, Ji C, Guo X (2016) Adipogenic miRNA and meta-signature miRNAs involved in human adipocyte differentiation and obesity. Oncotarget 7(26):40,830–40,845.  https://doi.org/10.18632/oncotarget.8518. ReviewCrossRefGoogle Scholar
  120. 120.
    Liu Y, Wang Y, He X, Zhang S, Wang K, Wu H, Chen L (2018) LncRNA TINCR/miR-31-5p/C/EBP-α feedback loop modulates the adipogenic differentiation process in human adipose tissue-derived mesenchymal stem cells. Stem Cell Res 23(32):35–42.  https://doi.org/10.1016/j.scr.2018.08.016 CrossRefGoogle Scholar
  121. 121.
    Meng Y, Eirin A, Zhu XY, Tang H, Hickson LJ, Lerman A, van Wijnen AJ, Lerman LO (2018) Micro-RNAS regulate metabolic syndrome-induced senescence in porcine adipose tissue-derived mesenchymal stem cells through the P16/MAPK pathway. Cell Transplant 27:1495–1503.  https://doi.org/10.1177/0963689718795692. Epub ahead of printCrossRefPubMedPubMedCentralGoogle Scholar
  122. 122.
    Jia B, Zhang Z, Qiu X, Chu H, Sun X, Zheng X, Zhao J, Li Q (2018) Analysis of the miRNA and mRNA involved in osteogenesis of adipose-derived mesenchymal stem cells. Exp Ther 16(2):1111–1120.  https://doi.org/10.3892/etm.2018.6303. Epub 2018 Jun 13CrossRefGoogle Scholar
  123. 123.
    Mieczkowska A, Schumacher A, Filipowicz N, Wardowska A, Zieliński M, Madanecki P, Nowicka E, Langa P, Deptuła M, Zieliński J, Kondej K, Renkielska A, Buckley PG, Crossman DK, Crowley MR, Czupryn A, Mucha P, Sachadyn P, Janus Ł, Skowron P, Rodziewicz-Motowidło S, Cichorek M, Pikuła M, Piotrowski A (2018) Immunophenotyping and transcriptional profiling of in vitro cultured human adipose tissue derived stem cells. Sci Rep 8(1):11,339.  https://doi.org/10.1038/s41598-018-29477-5 CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Centre for Advanced Studies in Humanities and Health SciencesInteramerican Open UniversityBuenos AiresArgentina
  2. 2.ISALUD University, Nutrition CareerBuenos AiresArgentina

Personalised recommendations