Lipidomics of Adipogenic Differentiation of Mesenchymal Stem Cells

  • Kambiz Gilany
  • Moloud Payab
  • Parisa Goodarzi
  • Akram Tayanloo-Beik
  • Sepideh Alavi-Moghadam
  • Maryamossadat Mousavi
  • Babak Arjmand
  • Tannaz Safaralizadeh
  • Mina Abedi
  • Maryam Arabi
  • Hamid Reza Aghayan
  • Bagher Larijani
Part of the Stem Cell Biology and Regenerative Medicine book series (STEMCELL)


Mesenchymal stem cells are defined as multipotent cells which have the ability to differentiate into various types of cell. Under the adipogenic stimuli, mesenchymal stem cells possess the ability to differentiate into adipocytes through adipogenesis processes. Adipogenesis is defined as the process of pre-adipocyte differentiation to mature adipocytes. Adipocytes are a type of cells with the ability to maintain energy balance through storage excess energy. However, several abnormal conditions including various types of disease can result from energy imbalance. Accordingly, obesity as a worldwide problem is one of the prevalent outcomes of increasing fat mass and there is a global effort to combat it. Accumulation of excess fat in adipocytes leads to adipocyte hypertrophy. Consequently, hypertrophic adipocyte can secrete several endocrine factors that induce hyperplasia (one of the major causes of obesity) and signal proliferation and differentiation of pre-adipocytes. Therefore, it has been demonstrated that adipogenic differentiation of mesenchymal stem cells undergoes different signaling pathways with various regulatory factors, while elucidation of these controllers can help scientists to develop more effective treatments for obesity and other related diseases. Therein, lipids have been presented as pivotal mediators of cellular processes and could induce several signaling pathways. Additionally, lipids are fundamental metabolites which use as cellular biomarkers to indicate different biological states and cellular activity. Total content of lipids in cells is known as lipidome. Any slight changes in the lipidome reflect different cellular changes. Tracking and comparing these changes between different stages of mesenchymal stem cell differentiation can provide identification of essential metabolic pathways involved in adipogenesis. In this context, lipidomics has been introduced as an emerging field of stem cell and regenerative medicine. Through the large-scale analysis of lipids, lipidomics provides more efficient methods to the investigation of adipocytes, and also prediction of the prognosis of obesity and its prevention and treatment.


Biomarkers Lipids Lipidomics Mesenchymal stem cell Obesity 



Brown adipose tissue


Body mass index


CCAAT/enhancer binding proteins


Carbon 1


Carbon 2


Carbon 3


Cyclin-dependent kinase inhibitors


Coenzyme A




Fatty acids


Growth arrest




Human mesenchymal stem cells






Interleukin 6


International Society for Cell Therapy


Lipid droplets


Clonal expansion


Mesenchymal stem cells


Mevalonic acid




Peroxisome proliferator-activated receptor γ


Peroxisome proliferator-activated receptor ϒ


Pluripotent stem cells


Sterol regulatory element binding protein






Transforming growth factor-β3


Tumor necrosis factor α


White adipose tissue


  1. 1.
    Huang C, Freter C. Lipid metabolism, apoptosis and cancer therapy. Int J Mol Sci. 2015;16(1):924–49.PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Rolim AE, et al. Lipidomics in the study of lipid metabolism: current perspectives in the omic sciences. Gene. 2015;554:131–9.PubMedCrossRefPubMedCentralGoogle Scholar
  3. 3.
    Kiamehr M, et al. Lipidomic profiling of patient-specific iPSC-derived hepatocyte-like cells. Dis Model Mech. 2017;10(9):1141–53.PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Pébay A, Wong RC. Lipidomics of stem cells. New York: Springer; 2017.CrossRefGoogle Scholar
  5. 5.
    Bieberich E, Wang G. Bioactive lipids in stem cell differentiation, in embryonic stem cells-differentiation and pluripotent alternatives. London: IntechOpen; 2011.Google Scholar
  6. 6.
    van Meer G, Voelker DR, Feigenson GW. Membrane lipids: where they are and how they behave. Nat Rev Mol Cell Biol. 2008;9(2):112–24.PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Bieberich E. It’s a lipid’s world: bioactive lipid metabolism and signaling in neural stem cell differentiation. Neurochem Res. 2012;37(6):1208–29.PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    de Meyer FJM, et al. Molecular simulation of the effect of cholesterol on lipid-mediated protein-protein interactions. Biophys J. 2010;99(11):3629–38.PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    van Meer G. Cellular lipidomics. EMBO J. 2005;24(18):3159–65.PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Harkewicz R, Dennis EA. Applications of mass spectrometry to lipids and membranes. Annu Rev Biochem. 2011;80:301–25.PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Dowhan W, Mileykovskaya E, Bogdanov M. Diversity and versatility of lipid-protein interactions revealed by molecular genetic approaches. Biochim Biophys Acta. 2004;1666(1–2):19–39.PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Wenk MR. The emerging field of lipidomics. Nat Rev Drug Discov. 2005;4(7):594.PubMedCrossRefPubMedCentralGoogle Scholar
  13. 13.
    Shevchenko A, Simons K. Lipidomics: coming to grips with lipid diversity. Nat Rev Mol Cell Biol. 2010;11(8):593.PubMedCrossRefPubMedCentralGoogle Scholar
  14. 14.
    Vance JE, Vance DE. Biochemistry of lipids, lipoproteins and membranes. Amsterdam: Elsevier; 2008.Google Scholar
  15. 15.
    Ridgway N, McLeod R. Biochemistry of lipids, lipoproteins and membranes. Amsterdam: Elsevier; 2015.Google Scholar
  16. 16.
    Dowhan W, Mileykovskaya E, Bogdanov M. Diversity and versatility of lipid–protein interactions revealed by molecular genetic approaches. Biochim Biophys Acta Biomembr. 2004;1666(1):19–39.CrossRefGoogle Scholar
  17. 17.
    Harayama T, Riezman H. Understanding the diversity of membrane lipid composition. Nat Rev Mol Cell Biol. 2018;19:281.PubMedCrossRefPubMedCentralGoogle Scholar
  18. 18.
    Chatgilialoglu A, et al. Restored in vivo-like membrane lipidomics positively influence in vitro features of cultured mesenchymal stromal/stem cells derived from human placenta. Stem Cell Res Ther. 2017;8(1):31.PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Campos AM, et al. Lipidomics of mesenchymal stromal cells: understanding the adaptation of phospholipid profile in response to pro-inflammatory cytokines. J Cell Physiol. 2016;231(5):1024–32.PubMedCrossRefPubMedCentralGoogle Scholar
  20. 20.
    Goodarzi P, et al. Therapeutic abortion and ectopic pregnancy: alternative sources for fetal stem cell research and therapy in Iran as an Islamic country. Cell Tissue Bank. 2019;20(1):11–24.PubMedCrossRefPubMedCentralGoogle Scholar
  21. 21.
    Shirian S, et al. Comparison of capability of human bone marrow mesenchymal stem cells and endometrial stem cells to differentiate into motor neurons on electrospun poly (ε-caprolactone) scaffold. Mol Neurobiol. 2016;53(8):5278–87.PubMedCrossRefPubMedCentralGoogle Scholar
  22. 22.
    Larijani B, et al. Human fetal skin fibroblasts: extremely potent and allogenic candidates for treatment of diabetic wounds. Med Hypotheses. 2015;84(6):577–9.PubMedCrossRefPubMedCentralGoogle Scholar
  23. 23.
    Goodarzi P, et al. Stem cell-based approach for the treatment of Parkinson’s disease. Med J Islam Repub Iran. 2015;29:168.PubMedPubMedCentralGoogle Scholar
  24. 24.
    Goodarzi P, et al. Stem cell therapy for treatment of epilepsy. Acta Med Iran. 2014;52(9):651–5.PubMedPubMedCentralGoogle Scholar
  25. 25.
    Wang M, Yuan Q, Xie L. Mesenchymal stem cell-based immunomodulation: properties and clinical application. Stem Cells Int. 2018;2018:3057624.PubMedPubMedCentralGoogle Scholar
  26. 26.
    Rohban R, Pieber TR. Mesenchymal stem and progenitor cells in regeneration: tissue specificity and regenerative potential. Stem Cells Int. 2017;2017:5173732.PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Larijani B, et al. GMP-grade human fetal liver-derived mesenchymal stem cells for clinical transplantation. In: Stem cells and good manufacturing practices. New York: Springer; 2014. p. 123–36.Google Scholar
  28. 28.
    Derakhshanrad N, et al. Case report: combination therapy with mesenchymal stem cells and granulocyte-colony stimulating factor in a case of spinal cord injury. Basic Clin Neurosci. 2015;6(4):299.PubMedPubMedCentralGoogle Scholar
  29. 29.
    Goodarzi P, et al. Adipose tissue-derived stromal cells for wound healing. Adv Exp Med Biol. 2018;1119:133–49.PubMedCrossRefPubMedCentralGoogle Scholar
  30. 30.
    Minguell JJ, Erices A, Conget P. Mesenchymal stem cells. Exp Biol Med. 2001;226(6):507–20.CrossRefGoogle Scholar
  31. 31.
    Kassem M. Mesenchymal stem cells: biological characteristics and potential clinical applications. Cloning Stem Cells. 2004;6(4):369–74.PubMedCrossRefGoogle Scholar
  32. 32.
    Mahmood R, Shaukat M, Choudhery MS. Biological properties of mesenchymal stem cells derived from adipose tissue, umbilical cord tissue and bone marrow. AIMS Cell Tissue Eng. 2018;2(2):78–90.CrossRefGoogle Scholar
  33. 33.
    Ma J, et al. Comparative analysis of mesenchymal stem cells derived from amniotic membrane, umbilical cord, and chorionic plate under serum-free condition. Stem Cell Res Ther. 2019;10(1):19.PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Sheykhhasan M, et al. Mesenchymal stem cells as a valuable agent in osteoarthritis treatment. Stem Cell Investig. 2018;5:41.PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Phelps J, et al. Bioprocessing of mesenchymal stem cells and their derivatives: toward cell-free therapeutics. Stem Cells Int. 2018;2018:9415367.PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Anderson HJ, et al. Mesenchymal stem cell fate: applying biomaterials for control of stem cell behavior. Front Bioeng Biotechnol. 2016;4:38.PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Sekiya I, et al. Adipogenic differentiation of human adult stem cells from bone marrow stroma (MSCs). J Bone Miner Res. 2004;19(2):256–64.PubMedCrossRefPubMedCentralGoogle Scholar
  38. 38.
    Kilroy G, et al. Isolation of murine adipose-derived stromal/stem cells for adipogenic differentiation or flow cytometry-based analysis. Methods Mol Biol. 2018;1773:137–46.PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Jaiswal N, et al. Osteogenic differentiation of purified, culture-expanded human mesenchymal stem cells in vitro. J Cell Biochem. 1997;64(2):295–312.PubMedCrossRefPubMedCentralGoogle Scholar
  40. 40.
    Song IH, Caplan AI, Dennis JE. In vitro dexamethasone pretreatment enhances bone formation of human mesenchymal stem cells in vivo. J Orthop Res. 2009;27(7):916–21.PubMedCrossRefGoogle Scholar
  41. 41.
    Barry F, et al. Chondrogenic differentiation of mesenchymal stem cells from bone marrow: differentiation-dependent gene expression of matrix components. Exp Cell Res. 2001;268(2):189–200.PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Mauck R, Yuan X, Tuan R. Chondrogenic differentiation and functional maturation of bovine mesenchymal stem cells in long-term agarose culture. Osteoarthr Cartil. 2006;14(2):179–89.PubMedCrossRefGoogle Scholar
  43. 43.
    Fan L, et al. Enhancement of the chondrogenic differentiation of mesenchymal stem cells and cartilage repair by ghrelin. J Orthop Res. 2019;37(6):1387–97.PubMedCrossRefGoogle Scholar
  44. 44.
    Ghaben AL, Scherer PE. Adipogenesis and metabolic health. Nat Rev Mol Cell Biol. 2019;20(4):242–58.PubMedCrossRefGoogle Scholar
  45. 45.
    Villarroya F, et al. Brown adipose tissue as a secretory organ. Nat Rev Endocrinol. 2017;13(1):26.PubMedCrossRefGoogle Scholar
  46. 46.
    Smitka K, Marešová D. Adipose tissue as an endocrine organ: an update on pro-inflammatory and anti-inflammatory microenvironment. Prague Med Rep. 2015;116(2):87–111.PubMedCrossRefGoogle Scholar
  47. 47.
    Churm R, et al. Ghrelin function in human obesity and type 2 diabetes: a concise review. Obes Rev. 2017;18(2):140–8.PubMedCrossRefGoogle Scholar
  48. 48.
    Gustafson B, et al. Insulin resistance and impaired adipogenesis. Trends Endocrinol Metab. 2015;26(4):193–200.PubMedCrossRefGoogle Scholar
  49. 49.
    Reisin E, Owen J. Treatment: special conditions: metabolic syndrome: obesity and the hypertension connection. J Am Soc Hypertens. 2015;9(2):156–9.PubMedCrossRefGoogle Scholar
  50. 50.
    Chappell VA, et al. Tetrabromobisphenol-A promotes early adipogenesis and lipogenesis in 3T3-L1 cells. Toxicol Sci. 2018;166(2):332–44.PubMedCrossRefGoogle Scholar
  51. 51.
    Tung Y-C, et al. Cellular models for the evaluation of the antiobesity effect of selected phytochemicals from food and herbs. J Food Drug Anal. 2017;25(1):100–10.PubMedCrossRefGoogle Scholar
  52. 52.
    De Sa PM, et al. Transcriptional regulation of adipogenesis. Compr Physiol. 2017;7:635–74.Google Scholar
  53. 53.
    Tencerova M, Kassem M. The bone marrow-derived stromal cells: commitment and regulation of adipogenesis. Front Endocrinol. 2016;7:127.CrossRefGoogle Scholar
  54. 54.
    Rony RIK, et al. Differential expression of PPARγ and CHOP-10 during Adipogenic differentiation of human bone marrow derived mesenchymal stem cells. FASEB J. 2018;32(1_suppl):lb17.Google Scholar
  55. 55.
    Fu M, et al. A nuclear receptor atlas: 3T3-L1 adipogenesis. Mol Endocrinol. 2005;19(10):2437–50.PubMedCrossRefGoogle Scholar
  56. 56.
    Ruiz-Ojeda F, et al. Cell models and their application for studying adipogenic differentiation in relation to obesity: a review. Int J Mol Sci. 2016;17(7):1040.PubMedCentralCrossRefPubMedGoogle Scholar
  57. 57.
    Forni MF, et al. Murine mesenchymal stem cell commitment to differentiation is regulated by mitochondrial dynamics. Stem Cells. 2016;34(3):743–55.PubMedCrossRefGoogle Scholar
  58. 58.
    Moreno-Navarrete JM, Fernández-Real JM. Adipocyte differentiation. In: Adipose tissue biology. New York: Springer; 2017. p. 69–90.CrossRefGoogle Scholar
  59. 59.
    Yuan Z, et al. PPARγ and Wnt signaling in adipogenic and osteogenic differentiation of mesenchymal stem cells. Curr Stem Cell Res Ther. 2016;11(3):216–25.PubMedCrossRefGoogle Scholar
  60. 60.
    Bennett CN, et al. Regulation of Wnt signaling during adipogenesis. J Biol Chem. 2002;277(34):30998–1004.PubMedCrossRefGoogle Scholar
  61. 61.
    Gross B, et al. PPARs in obesity-induced T2DM, dyslipidaemia and NAFLD. Nat Rev Endocrinol. 2017;13(1):36.PubMedCrossRefGoogle Scholar
  62. 62.
    Salazar-Roa M, Malumbres M. Fueling the cell division cycle. Trends Cell Biol. 2017;27(1):69–81.PubMedCrossRefGoogle Scholar
  63. 63.
    Chiurchiù V, Leuti A, Maccarrone M. Bioactive lipids and chronic inflammation: managing the fire within. Front Immunol. 2018;9:38.PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Nagao K, Yanagita T. Bioactive lipids in metabolic syndrome. Prog Lipid Res. 2008;47(2):127–46.PubMedCrossRefGoogle Scholar
  65. 65.
    Fahy E, et al. Update of the LIPID MAPS comprehensive classification system for lipids. J Lipid Res. 2009;50(Suppl):S9–S14.PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Fahy E, et al. A comprehensive classification system for lipids. Eur J Lipid Sci Technol. 2005;107(5):337–64.CrossRefGoogle Scholar
  67. 67.
    Holm R. Bridging the gaps between academic research and industrial product developments of lipid-based formulations. Adv Drug Deliv Rev, 2019. Scholar
  68. 68.
    Jones SF, Infante JR. Molecular pathways: fatty acid synthase. Clin Cancer Res. 2015;21(24):5434–8.PubMedCrossRefGoogle Scholar
  69. 69.
    Hashimoto M, Hossain S. Fatty acids: from membrane ingredients to signaling molecules, in biochemistry and health benefits of fatty acids. London: IntechOpen; 2018.Google Scholar
  70. 70.
    Han X, Zhou Y. Application of lipidomics in nutrition research. In: Metabolomics as a tool in nutrition research. Amsterdam: Elsevier; 2015. p. 63–84.CrossRefGoogle Scholar
  71. 71.
    Matsumaru T, et al. Synthesis of glycerolipids containing simple linear acyl chains or aromatic rings and evaluation of their Mincle signaling activity. Chem Commun. 2019;55(5):711–4.CrossRefGoogle Scholar
  72. 72.
    Khoury S, et al. Quantification of lipids: model, reality, and compromise. Biomol Ther. 2018;8(4):174.Google Scholar
  73. 73.
    Lingwood D, Simons K. Lipid rafts as a membrane-organizing principle. Science. 2010;327(5961):46–50.PubMedCrossRefPubMedCentralGoogle Scholar
  74. 74.
    Merrill AH Jr. Sphingolipids. In: Biochemistry of lipids, lipoproteins and membranes. Amsterdam: Elsevier; 2008. p. 363–97.CrossRefGoogle Scholar
  75. 75.
    Chun J, Hartung H-P. Mechanism of action of oral fingolimod (FTY720) in multiple sclerosis. Clin Neuropharmacol. 2010;33(2):91–101.PubMedPubMedCentralCrossRefGoogle Scholar
  76. 76.
    Dickson RC, Lester RL. Sphingolipid functions in Saccharomyces cerevisiae. Biochim Biophys Acta. 2002;1583(1):13–25.PubMedCrossRefGoogle Scholar
  77. 77.
    Fahy E, et al. A comprehensive classification system for lipids. J Lipid Res. 2005;46:839–61.PubMedCrossRefGoogle Scholar
  78. 78.
    Raetz CR, et al. Discovery of new biosynthetic pathways: the lipid A story. J Lipid Res. 2009;50(Suppl):S103–8.PubMedPubMedCentralCrossRefGoogle Scholar
  79. 79.
    Pfeifer BA, Khosla C. Biosynthesis of polyketides in heterologous hosts. Microbiol Mol Biol Rev. 2001;65(1):106–18.PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    Lim Y, Go M, Yew W. Exploiting the biosynthetic potential of type III polyketide synthases. Molecules. 2016;21(6):806.PubMedCentralCrossRefGoogle Scholar
  81. 81.
    Demel RA, De Kruyff B. The function of sterols in membranes. Biochim Biophys Acta. 1976;457(2):109–32.PubMedCrossRefPubMedCentralGoogle Scholar
  82. 82.
    Wolstenholme GEW, O’Connor CM. Quinones in electron transport, vol. 947. Hoboken: Wiley; 2009.Google Scholar
  83. 83.
    Lydic TA, Goo Y-H. Lipidomics unveils the complexity of the lipidome in metabolic diseases. Clin Transl Med. 2018;7(1):4–4.PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Zhao YY, et al. Lipidomics applications for disease biomarker discovery in mammal models. Biomark Med. 2015;9(2):153–68.PubMedCrossRefPubMedCentralGoogle Scholar
  85. 85.
    Zhao YY, Cheng XL, Lin RC. Lipidomics applications for discovering biomarkers of diseases in clinical chemistry. Int Rev Cell Mol Biol. 2014;313:1–26.PubMedCrossRefPubMedCentralGoogle Scholar
  86. 86.
    Liaw L, et al. Lipid profiling of in vitro cell models of adipogenic differentiation: relationships with mouse adipose tissues. J Cell Biochem. 2016;117(9):2182–93.PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Yang J-Y, et al. Regulation of adipogenesis by medium-chain fatty acids in the absence of hormonal cocktail. J Nutr Biochem. 2009;20(7):537–43.PubMedCrossRefPubMedCentralGoogle Scholar
  88. 88.
    Kim H-K, et al. Docosahexaenoic acid inhibits adipocyte differentiation and induces apoptosis in 3T3-L1 preadipocytes. J Nutr. 2006;136(12):2965–9.PubMedCrossRefPubMedCentralGoogle Scholar
  89. 89.
    Dwyer JR, et al. Oxysterols are novel activators of the hedgehog signaling pathway in pluripotent mesenchymal cells. J Biol Chem. 2007;282(12):8959–68.PubMedCrossRefPubMedCentralGoogle Scholar
  90. 90.
    Eaton S. Multiple roles for lipids in the hedgehog signalling pathway. Nat Rev Mol Cell Biol. 2008;9(6):437.PubMedCrossRefPubMedCentralGoogle Scholar
  91. 91.
    Gregg EW, Shaw JE. Global health effects of overweight and obesity. N Engl J Med. 2017;377(1):80–1.PubMedCrossRefPubMedCentralGoogle Scholar
  92. 92.
    Dixon J. The global burden of obesity and diabetes. In: Minimally invasive bariatric surgery. New York: Springer; 2015. p. 1–6.Google Scholar
  93. 93.
    Hossain P, Kawar B, El Nahas M. Obesity and diabetes in the developing world—a growing challenge. N Engl J Med. 2007;356(3):213–5.PubMedCrossRefPubMedCentralGoogle Scholar
  94. 94.
    Low S, Chin MC, Deurenberg-Yap M. Review on epidemic of obesity. Ann Acad Med Singap. 2009;38(1):57.PubMedPubMedCentralGoogle Scholar
  95. 95.
    Lavie CJ, et al. Management of cardiovascular diseases in patients with obesity. Nat Rev Cardiol. 2018;15(1):45.PubMedCrossRefPubMedCentralGoogle Scholar
  96. 96.
    Hurt RT, et al. Obesity epidemic: overview, pathophysiology, and the intensive care unit conundrum. J Parenter Enter Nutr. 2011;35(5_suppl):4S–13S.CrossRefGoogle Scholar
  97. 97.
    Arnold M, et al. Obesity and cancer: an update of the global impact. Cancer Epidemiol. 2016;41:8–15.PubMedCrossRefPubMedCentralGoogle Scholar
  98. 98.
    Collaborators GO. Health effects of overweight and obesity in 195 countries over 25 years. N Engl J Med. 2017;377(1):13–27.CrossRefGoogle Scholar
  99. 99.
    Rennie K, Jebb S. Prevalence of obesity in Great Britain. Obes Rev. 2005;6(1):11–2.PubMedCrossRefPubMedCentralGoogle Scholar
  100. 100.
    Husky MM, et al. Differential associations between excess body weight and psychiatric disorders in men and women. J Women’s Health. 2018;27(2):183–90.CrossRefGoogle Scholar
  101. 101.
    Webb P, et al. Hunger and malnutrition in the 21st century. BMJ. 2018;361:k2238.PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Jacob CS, de Alba Carolina T. An evidence-based review of dietary supplements on inflammatory biomarkers in obesity. Curr Res Nutr Food Sci J. 2018;6(2):284–93.CrossRefGoogle Scholar
  103. 103.
    Khan M. Complications of cryolipolysis: paradoxical adipose hyperplasia (PAH) and beyond. Aesthet Surg J. 2019;39(8):NP334–42.PubMedCrossRefPubMedCentralGoogle Scholar
  104. 104.
    Considine RV, et al. Paracrine stimulation of preadipocyte-enriched cell cultures by mature adipocytes. Am J Physiol Endocrinol Metab. 1996;270(5):E895–9.CrossRefGoogle Scholar
  105. 105.
    Tang QQ, Lane MD. Adipogenesis: from stem cell to adipocyte. Annu Rev Biochem. 2012;81:715–36.PubMedCrossRefPubMedCentralGoogle Scholar
  106. 106.
    Cook D, Genever P. Regulation of mesenchymal stem cell differentiation, in transcriptional and translational regulation of stem cells. Adv Exp Med Biol. 2013;786:213–29.PubMedCrossRefPubMedCentralGoogle Scholar
  107. 107.
    Lindroos B, Suuronen R, Miettinen S. The potential of adipose stem cells in regenerative medicine. Stem Cell Rev Rep. 2011;7(2):269–91.PubMedCrossRefPubMedCentralGoogle Scholar
  108. 108.
    Ong WK, Sugii S. Adipose-derived stem cells: fatty potentials for therapy. Int J Biochem Cell Biol. 2013;45(6):1083–6.PubMedCrossRefPubMedCentralGoogle Scholar
  109. 109.
    Coelho M, Oliveira T, Fernandes R. Biochemistry of adipose tissue: an endocrine organ. Arch Med Sci. 2013;9(2):191.PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Galic S, Oakhill JS, Steinberg GR. Adipose tissue as an endocrine organ. Mol Cell Endocrinol. 2010;316(2):129–39.PubMedCrossRefPubMedCentralGoogle Scholar
  111. 111.
    Jo J, et al. Hypertrophy and/or hyperplasia: dynamics of adipose tissue growth. PLoS Comput Biol. 2009;5(3):e1000324.PubMedPubMedCentralCrossRefGoogle Scholar
  112. 112.
    Payab M, et al. Stem cell and obesity: current state and future perspective. Adv Exp Med Biol. 2018;1089:1–22.PubMedCrossRefPubMedCentralGoogle Scholar
  113. 113.
    Joe AW, et al. Depot-specific differences in adipogenic progenitor abundance and proliferative response to high-fat diet. Stem Cells. 2009;27(10):2563–70.PubMedCrossRefPubMedCentralGoogle Scholar
  114. 114.
    Matsushita K, Dzau VJ. Mesenchymal stem cells in obesity: insights for translational applications. Lab Investig. 2017;97(10):1158.PubMedCrossRefPubMedCentralGoogle Scholar
  115. 115.
    Niemelä S, et al. Adipose tissue and adipocyte differentiation: molecular and cellular aspects and tissue engineering applications. Top Tissue Eng. 2008;4(1):26.Google Scholar
  116. 116.
    Cleal L, Aldea T, Chau Y-Y. Fifty shades of white: understanding heterogeneity in white adipose stem cells. Adipocytes. 2017;6(3):205–16.CrossRefGoogle Scholar
  117. 117.
    Cawthorn WP, Scheller EL, MacDougald OA. Adipose tissue stem cells meet preadipocyte commitment: going back to the future. J Lipid Res. 2012;53(2):227–46.PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    Tang W, et al. White fat progenitor cells reside in the adipose vasculature. Science. 2008;322(5901):583–6.PubMedPubMedCentralCrossRefGoogle Scholar
  119. 119.
    Matsushita K. Mesenchymal stem cells and metabolic syndrome: current understanding and potential clinical implications. Stem Cells Int. 2016;2016:2892840.PubMedPubMedCentralCrossRefGoogle Scholar
  120. 120.
    Poulos SP, et al. The increasingly complex regulation of adipocyte differentiation. Exp Biol Med. 2016;241(5):449–56.CrossRefGoogle Scholar
  121. 121.
    Moseti D, Regassa A, Kim W-K. Molecular regulation of adipogenesis and potential anti-adipogenic bioactive molecules. Int J Mol Sci. 2016;17(1):124.PubMedCentralCrossRefGoogle Scholar
  122. 122.
    Postle AD. Lipidomics. Curr Opin Clin Nutr Metab Care. 2012;15(2):127–33.PubMedPubMedCentralGoogle Scholar
  123. 123.
    Murphy SA, Nicolaou A. Lipidomics applications in health, disease and nutrition research. Mol Nutr Food Res. 2013;57(8):1336–46.PubMedCrossRefPubMedCentralGoogle Scholar
  124. 124.
    Yang K, Han X. Lipidomics: techniques, applications, and outcomes related to biomedical sciences. Trends Biochem Sci. 2016;41(11):954–69.PubMedPubMedCentralCrossRefGoogle Scholar
  125. 125.
    Han X. Lipidomics for studying metabolism. Nat Rev Endocrinol. 2016;12(11):668.PubMedCrossRefPubMedCentralGoogle Scholar
  126. 126.
    Cristancho AG, Lazar MA. Forming functional fat: a growing understanding of adipocyte differentiation. Nat Rev Mol Cell Biol. 2011;12(11):722.PubMedCrossRefPubMedCentralGoogle Scholar
  127. 127.
    Lapid K, Graff JM. Form(ul)ation of adipocytes by lipids. Adipocytes. 2017;6(3):176–86.CrossRefGoogle Scholar
  128. 128.
    de Ferranti S, Mozaffarian D. The perfect storm: obesity, adipocyte dysfunction, and metabolic consequences. Clin Chem. 2008;54(6):945–55.PubMedCrossRefPubMedCentralGoogle Scholar
  129. 129.
    Hammarstedt A, et al. Impaired adipogenesis and dysfunctional adipose tissue in human hypertrophic obesity. Physiol Rev. 2018;98(4):1911–41.PubMedCrossRefPubMedCentralGoogle Scholar
  130. 130.
    Han X. An update on lipidomics: progress and application in biomarker and drug development. Curr Opin Mol Ther. 2007;9(6):586–91.PubMedPubMedCentralGoogle Scholar
  131. 131.
    Haraszti RA, et al. High-resolution proteomic and lipidomic analysis of exosomes and microvesicles from different cell sources. J Extracell Vesicles. 2016;5(1):32570.PubMedCrossRefGoogle Scholar
  132. 132.
    Nguyen A, et al. Using lipidomics analysis to determine signalling and metabolic changes in cells. Curr Opin Biotechnol. 2017;43:96–103.PubMedCrossRefGoogle Scholar
  133. 133.
    Qian S-W, et al. Characterization of adipocyte differentiation from human mesenchymal stem cells in bone marrow. BMC Dev Biol. 2010;10:47.PubMedPubMedCentralCrossRefGoogle Scholar
  134. 134.
    Mohammadi Z, et al. Differentiation of adipocytes and osteocytes from human adipose and placental mesenchymal stem cells. Iran J Basic Med Sci. 2015;18(3):259–66.PubMedPubMedCentralGoogle Scholar
  135. 135.
    Marquez MP, et al. The role of cellular proliferation in adipogenic differentiation of human adipose tissue-derived mesenchymal stem cells. Stem Cells Dev. 2017;26(21):1578–95.PubMedPubMedCentralCrossRefGoogle Scholar
  136. 136.
    Montacir H, et al. N-glycosylation profile of undifferentiated and adipogenically differentiated human bone marrow Mesenchymal stem cells: towards a next generation of stem cell markers. Stem Cells Dev. 2013;22(23):3100–13.CrossRefGoogle Scholar
  137. 137.
    Sarantopoulos CN, et al. Elucidating the preadipocyte and its role in adipocyte formation: a comprehensive review. Stem Cell Rev. 2018;14(1):27–42.CrossRefGoogle Scholar
  138. 138.
    Masoodi M, et al. Lipid signaling in adipose tissue: connecting inflammation & metabolism. Biochim Biophys Acta. 2015;1851(4):503–18.PubMedCrossRefGoogle Scholar
  139. 139.
    Lee Y-H, Mottillo EP, Granneman JG. Adipose tissue plasticity from WAT to BAT and in between. Biochim Biophys Acta. 2014;1842(3):358–69.PubMedCrossRefGoogle Scholar
  140. 140.
    Titz B, et al. Proteomics and lipidomics in inflammatory bowel disease research: from mechanistic insights to biomarker identification. Int J Mol Sci. 2018;19(9):2775.PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Kambiz Gilany
    • 1
    • 2
  • Moloud Payab
    • 3
  • Parisa Goodarzi
    • 4
  • Akram Tayanloo-Beik
    • 5
  • Sepideh Alavi-Moghadam
    • 5
  • Maryamossadat Mousavi
    • 6
  • Babak Arjmand
    • 5
    • 6
  • Tannaz Safaralizadeh
    • 5
  • Mina Abedi
    • 6
  • Maryam Arabi
    • 6
  • Hamid Reza Aghayan
    • 5
  • Bagher Larijani
    • 7
  1. 1.Department of Biomedical SciencesUniversity of AntwerpAntwerpBelgium
  2. 2.Integrative Oncology Department, Breast Cancer Research CenterMotamed Cancer Institute, ACECRTehranIran
  3. 3.Obesity and Eating Habits Research Center, Endocrinology and Metabolism Molecular-Cellular Sciences InstituteTehran University of Medical SciencesTehranIran
  4. 4.Brain and Spinal Cord Injury Research Center, Neuroscience InstituteTehran University of Medical SciencesTehranIran
  5. 5.Cell Therapy and Regenerative Medicine Research Center, Endocrinology and Metabolism Molecular-Cellular Sciences InstituteTehran University of Medical SciencesTehranIran
  6. 6.Metabolomics and Genomics Research Center, Endocrinology and Metabolism Molecular-Cellular Sciences InstituteTehran University of Medical SciencesTehranIran
  7. 7.Endocrinology and Metabolism Research Center, Endocrinology and Metabolism Clinical Sciences InstituteTehran University of Medical SciencesTehranIran

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