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Cellular and Molecular Life Sciences

, Volume 77, Issue 1, pp 115–128 | Cite as

Adipocyte–progenitor cell communication that influences adipogenesis

  • William Lloyd Haylett
  • William Frank FerrisEmail author
Review

Abstract

Adipose tissue is located in discrete depots that are differentially associated with elevated risk of metabolic complications, with fat accretion in visceral depots being most detrimental to metabolic health. Currently, the regulation of specific adipose depot expansion, by adipocyte hypertrophy and hyperplasia and consequently fat distribution, is not well understood. However, a growing body of evidence from in vitro investigations indicates that mature adipocytes secrete factors that modulate the proliferation and differentiation of progenitor, adipose-derived stem cells (ADSCs). It is therefore plausible that endocrine communication between adipocytes and ADSCs located in different depots influences fat distribution, and may therefore contribute to the adverse health outcomes associated with visceral adiposity. This review will explore the available evidence of paracrine and endocrine crosstalk between mature adipocytes and ADSCs that affects adipogenesis, as a better understanding of the regulatory roles of the extracellular signalling mechanisms within- and between adipose depots may profoundly change the way we view adipose tissue growth in obesity and related comorbidities.

Keywords

Adipose Adipocytes Adipose-derived stem cells Adipogenesis Paracrine Endocrine 

Notes

Acknowledgements

This work is based on the research supported wholly/in part by the National Research Foundation of South Africa (Grant Numbers 118565 and 118990), the South African Sugar Association (Project 257) and The Harry Crossley Foundation; WLH is supported by the Faculty of Medicine and Health Sciences, Stellenbosch University, South Africa.

References

  1. 1.
    Gregg EW, Shaw JE (2017) Global health effects of overweight and obesity. N Engl J Med 377:80–81.  https://doi.org/10.1056/NEJMe1706095 CrossRefPubMedGoogle Scholar
  2. 2.
    Bianchini F, Kaaks R, Vainio H (2002) Overweight, obesity, and cancer risk. Lancet Oncol 3:565–574CrossRefGoogle Scholar
  3. 3.
    Després J-P, Lemieux I (2006) Abdominal obesity and metabolic syndrome. Nature 444:881–887.  https://doi.org/10.1038/nature05488 CrossRefPubMedGoogle Scholar
  4. 4.
    Booth A, Magnuson A, Foster M (2014) Detrimental and protective fat: body fat distribution and its relation to metabolic disease. Horm Mol Biol Clin Investig 17:13–27.  https://doi.org/10.1515/hmbci-2014-0009 CrossRefPubMedGoogle Scholar
  5. 5.
    Sun K, Kusminski CM, Scherer PE (2011) Adipose tissue remodeling and obesity. J Clin Invest 121:2094–2101.  https://doi.org/10.1172/JCI45887 CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Sethi JK, Vidal-Puig AJ (2007) Thematic review series: adipocyte biology. Adipose tissue function and plasticity orchestrate nutritional adaptation. J Lipid Res 48:1253–1262.  https://doi.org/10.1194/jlr.R700005-JLR200 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Wood IS, de Heredia FP, Wang B, Trayhurn P (2009) Cellular hypoxia and adipose tissue dysfunction in obesity. Proc Nutr Soc 68:370–377.  https://doi.org/10.1017/S0029665109990206 CrossRefPubMedGoogle Scholar
  8. 8.
    Rosen ED, MacDougald OA (2006) Adipocyte differentiation from the inside out. Nat Rev Mol Cell Biol 7:885–896.  https://doi.org/10.1038/nrm2066 CrossRefPubMedGoogle Scholar
  9. 9.
    Wajchenberg BL (2000) Subcutaneous and visceral adipose tissue: their relation to the metabolic syndrome. Endocr Rev 21:697–738.  https://doi.org/10.1210/edrv.21.6.0415 CrossRefPubMedGoogle Scholar
  10. 10.
    Neeland IJ, Ayers CR, Rohatgi AK et al (2013) Associations of visceral and abdominal subcutaneous adipose tissue with markers of cardiac and metabolic risk in obese adults. Obes Silver Spring Md 21:E439–E447.  https://doi.org/10.1002/oby.20135 CrossRefGoogle Scholar
  11. 11.
    Ibrahim MM (2010) Subcutaneous and visceral adipose tissue: structural and functional differences. Obes Rev Off J Int Assoc Study Obes 11:11–18.  https://doi.org/10.1111/j.1467-789X.2009.00623.x CrossRefGoogle Scholar
  12. 12.
    Roca-Rivada A, Alonso J, Al-Massadi O et al (2011) Secretome analysis of rat adipose tissues shows location-specific roles for each depot type. J Proteom 74:1068–1079.  https://doi.org/10.1016/j.jprot.2011.03.010 CrossRefGoogle Scholar
  13. 13.
    Sam S, Mazzone T (2014) Adipose tissue changes in obesity and the impact on metabolic function. Transl Res J Lab Clin Med 164:284–292.  https://doi.org/10.1016/j.trsl.2014.05.008 CrossRefGoogle Scholar
  14. 14.
    McGown C, Birerdinc A, Younossi ZM (2014) Adipose tissue as an endocrine organ. Clin Liver Dis 18:41–58.  https://doi.org/10.1016/j.cld.2013.09.012 CrossRefPubMedGoogle Scholar
  15. 15.
    Cook KS, Min HY, Johnson D et al (1987) Adipsin: a circulating serine protease homolog secreted by adipose tissue and sciatic nerve. Science 237:402–405CrossRefGoogle Scholar
  16. 16.
    Zhang Y, Proenca R, Maffei M et al (1994) Positional cloning of the mouse obese gene and its human homologue. Nature 372:425–432.  https://doi.org/10.1038/372425a0 CrossRefPubMedGoogle Scholar
  17. 17.
    Scherer PE, Williams S, Fogliano M et al (1995) A novel serum protein similar to C1q, produced exclusively in adipocytes. J Biol Chem 270:26746–26749CrossRefGoogle Scholar
  18. 18.
    Goralski KB, McCarthy TC, Hanniman EA et al (2007) Chemerin, a novel adipokine that regulates adipogenesis and adipocyte metabolism. J Biol Chem 282:28175–28188.  https://doi.org/10.1074/jbc.M700793200 CrossRefPubMedGoogle Scholar
  19. 19.
    Dahlman I, Elsen M, Tennagels N et al (2012) Functional annotation of the human fat cell secretome. Arch Physiol Biochem 118:84–91.  https://doi.org/10.3109/13813455.2012.685745 CrossRefPubMedGoogle Scholar
  20. 20.
    Roca-Rivada A, Bravo SB, Pérez-Sotelo D et al (2015) CILAIR-based secretome analysis of obese visceral and subcutaneous adipose tissues reveals distinctive ECM remodeling and inflammation mediators. Sci Rep 5:12214.  https://doi.org/10.1038/srep12214 CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Deng Y, Scherer PE (2010) Adipokines as novel biomarkers and regulators of the metabolic syndrome. Ann N Y Acad Sci 1212:E1–E19.  https://doi.org/10.1111/j.1749-6632.2010.05875.x CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Nakamura K, Fuster JJ, Walsh K (2014) Adipokines: a link between obesity and cardiovascular disease. J Cardiol 63:250–259.  https://doi.org/10.1016/j.jjcc.2013.11.006 CrossRefPubMedGoogle Scholar
  23. 23.
    Spalding KL, Arner E, Westermark PO et al (2008) Dynamics of fat cell turnover in humans. Nature 453:783–787.  https://doi.org/10.1038/nature06902 CrossRefPubMedGoogle Scholar
  24. 24.
    Armani A, Mammi C, Marzolla V et al (2010) Cellular models for understanding adipogenesis, adipose dysfunction, and obesity. J Cell Biochem 110:564–572.  https://doi.org/10.1002/jcb.22598 CrossRefPubMedGoogle Scholar
  25. 25.
    Lee M-J, Fried SK (2014) Optimal protocol for the differentiation and metabolic analysis of human adipose stromal cells. Methods Enzymol 538:49–65.  https://doi.org/10.1016/B978-0-12-800280-3.00004-9 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Wang QA, Scherer PE, Gupta RK (2014) Improved methodologies for the study of adipose biology: insights gained and opportunities ahead. J Lipid Res 55:605–624.  https://doi.org/10.1194/jlr.R046441 CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Cristancho AG, Lazar MA (2011) Forming functional fat: a growing understanding of adipocyte differentiation. Nat Rev Mol Cell Biol 12:722–734.  https://doi.org/10.1038/nrm3198 CrossRefPubMedGoogle Scholar
  28. 28.
    Kuk JL, Saunders TJ, Davidson LE, Ross R (2009) Age-related changes in total and regional fat distribution. Ageing Res Rev 8:339–348.  https://doi.org/10.1016/j.arr.2009.06.001 CrossRefPubMedGoogle Scholar
  29. 29.
    Shillabeer G, Forden JM, Lau DC (1989) Induction of preadipocyte differentiation by mature fat cells in the rat. J Clin Invest 84:381–387CrossRefGoogle Scholar
  30. 30.
    Pairault J, Green H (1979) A study of the adipose conversion of suspended 3T3 cells by using glycerophosphate dehydrogenase as differentiation marker. Proc Natl Acad Sci USA 76:5138–5142CrossRefGoogle Scholar
  31. 31.
    Shillabeer G, Forden JM, Russell JC, Lau DC (1990) Paradoxically slow preadipocyte replication and differentiation in corpulent rats. Am J Physiol-Endocrinol Metab 258:E368–E376.  https://doi.org/10.1152/ajpendo.1990.258.2.E368 CrossRefGoogle Scholar
  32. 32.
    Carraro R, Li ZH, Johnson JE, Gregerman RI (1992) Adipocytes of old rats produce a decreased amount of differentiation factor for preadipocytes derived from adipose tissue islets. J Gerontol 47:B198–B201CrossRefGoogle Scholar
  33. 33.
    Li Z-H, Carraro R, Gregerman RI, Lau DCW (1998) Adipocyte differentiation factor (adf): a protein secreted by mature fat cells that induces preadipocyte differentiation in culture. Cell Biol Int 22:253–270.  https://doi.org/10.1006/cbir.1998.0237 CrossRefPubMedGoogle Scholar
  34. 34.
    Li J, Qiao X, Yu M et al (2014) Secretory factors from rat adipose tissue explants promote adipogenesis and angiogenesis. Artif Organs 38:E33–E45.  https://doi.org/10.1111/aor.12162 CrossRefPubMedGoogle Scholar
  35. 35.
    Ailhaud G, Amri E, Bardon S et al (1990) The adipocyte: relationships between proliferation and adipose cell differentiation. Am Rev Respir Dis 142:S57–S59.  https://doi.org/10.1164/ajrccm/142.6_Pt_2.S57 CrossRefPubMedGoogle Scholar
  36. 36.
    Stacey DH, Hanson SE, Lahvis G et al (2009) In vitro adipogenic differentiation of preadipocytes varies with differentiation stimulus, culture dimensionality, and scaffold composition. Tissue Eng Part A 15:3389–3399.  https://doi.org/10.1089/ten.TEA.2008.0293 CrossRefPubMedGoogle Scholar
  37. 37.
    Janderová L, McNeil M, Murrell AN et al (2003) Human mesenchymal stem cells as an in vitro model for human adipogenesis. Obes Res 11:65–74.  https://doi.org/10.1038/oby.2003.11 CrossRefPubMedGoogle Scholar
  38. 38.
    Sarkanen J-R, Kaila V, Mannerström B et al (2012) Human adipose tissue extract induces angiogenesis and adipogenesis in vitro. Tissue Eng Part A 18:17–25.  https://doi.org/10.1089/ten.tea.2010.0712 CrossRefPubMedGoogle Scholar
  39. 39.
    Song K, Li W, Wang H et al (2012) Investigation of coculture of human adipose-derived stem cells and mature adipocytes. Appl Biochem Biotechnol 167:2381–2387.  https://doi.org/10.1007/s12010-012-9764-y CrossRefPubMedGoogle Scholar
  40. 40.
    Janke J, Engeli S, Gorzelniak K et al (2002) Mature adipocytes inhibit in vitro differentiation of human preadipocytes via angiotensin type 1 receptors. Diabetes 51:1699–1707.  https://doi.org/10.2337/diabetes.51.6.1699 CrossRefPubMedGoogle Scholar
  41. 41.
    Ailhaud G, Fukamizu A, Massiera F et al (2000) Angiotensinogen, angiotensin II and adipose tissue development. Int J Obes Relat Metab Disord J Int Assoc Study Obes 24(Suppl 4):S33–S35CrossRefGoogle Scholar
  42. 42.
    Pinterova L, Krizanova O, Zorad S (2000) Rat epididymal fat tissue express all components of the renin-angiotensin system. Gen Physiol Biophys 19:329–334PubMedGoogle Scholar
  43. 43.
    Frigolet ME, Torres N, Tovar AR (2013) The renin–angiotensin system in adipose tissue and its metabolic consequences during obesity. J Nutr Biochem 24:2003–2015.  https://doi.org/10.1016/j.jnutbio.2013.07.002 CrossRefPubMedGoogle Scholar
  44. 44.
    Townsend RR (2001) The effects of angiotensin-II on lipolysis in humans. Metabolism 50:468–472.  https://doi.org/10.1053/meta.2001.21021 CrossRefPubMedGoogle Scholar
  45. 45.
    Considine RV, Nyce MR, Morales LM et al (1996) Paracrine stimulation of preadipocyte-enriched cell cultures by mature adipocytes. Am J Physiol-Endocrinol Metab 270:E895–E899.  https://doi.org/10.1152/ajpendo.1996.270.5.E895 CrossRefGoogle Scholar
  46. 46.
    Hirsch J, Batchelor B (1976) Adipose tissue cellularity in human obesity. Clin Endocrinol Metab 5:299–311CrossRefGoogle Scholar
  47. 47.
    Maumus M, Sengenès C, Decaunes P et al (2008) Evidence of in situ proliferation of adult adipose tissue-derived progenitor cells: influence of fat mass microenvironment and growth. J Clin Endocrinol Metab 93:4098–4106.  https://doi.org/10.1210/jc.2008-0044 CrossRefPubMedGoogle Scholar
  48. 48.
    Valet P, Pagès C, Jeanneton O et al (1998) Alpha2-adrenergic receptor-mediated release of lysophosphatidic acid by adipocytes. A paracrine signal for preadipocyte growth. J Clin Invest 101:1431–1438.  https://doi.org/10.1172/JCI806 CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Wagoner B, Hausman DB, Harris RBS (2006) Direct and indirect effects of leptin on preadipocyte proliferation and differentiation. Am J Physiol Regul Integr Comp Physiol 290:R1557–R1564.  https://doi.org/10.1152/ajpregu.00860.2005 CrossRefPubMedGoogle Scholar
  50. 50.
    Blaber SP, Webster RA, Hill CJ et al (2012) Analysis of in vitro secretion profiles from adipose-derived cell populations. J Transl Med 10:172.  https://doi.org/10.1186/1479-5876-10-172 CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Blagovic K, Kim LY, Voldman J (2011) Microfluidic perfusion for regulating diffusible signaling in stem cells. PLoS One 6:e22892.  https://doi.org/10.1371/journal.pone.0022892 CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Hemmingsen M, Vedel S, Skafte-Pedersen P et al (2013) The role of paracrine and autocrine signaling in the early phase of adipogenic differentiation of adipose-derived stem cells. PLoS One.  https://doi.org/10.1371/journal.pone.0063638 CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Ferland-McCollough D, Masseli D, Spinetti G et al (2018) MCP-1 Feedback Loop Between adipocytes and mesenchymal stromal cells causes fat accumulation and contributes to hematopoietic stem cell rarefaction in the bone marrow of diabetic patients. Diabetes.  https://doi.org/10.2337/db18-0044 CrossRefPubMedGoogle Scholar
  54. 54.
    Younce C, Kolattukudy P (2012) MCP-1 induced protein promotes adipogenesis via oxidative stress, endoplasmic reticulum stress and autophagy. Cell Physiol Biochem Int J Exp Cell Physiol Biochem Pharmacol 30:307–320.  https://doi.org/10.1159/000339066 CrossRefGoogle Scholar
  55. 55.
    Panee J (2012) Monocyte chemoattractant protein 1 (MCP-1) in obesity and diabetes. Cytokine 60:1–12.  https://doi.org/10.1016/j.cyto.2012.06.018 CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Green H, Meuth M (1974) An established pre-adipose cell line and its differentiation in culture. Cell 3:127–133CrossRefGoogle Scholar
  57. 57.
    Zebisch K, Voigt V, Wabitsch M, Brandsch M (2012) Protocol for effective differentiation of 3T3-L1 cells to adipocytes. Anal Biochem 425:88–90.  https://doi.org/10.1016/j.ab.2012.03.005 CrossRefPubMedGoogle Scholar
  58. 58.
    Huang W-C, Chang W-T, Wu S-J et al (2013) Phloretin and phlorizin promote lipolysis and inhibit inflammation in mouse 3T3-L1 cells and in macrophage-adipocyte co-cultures. Mol Nutr Food Res 57:1803–1813.  https://doi.org/10.1002/mnfr.201300001 CrossRefPubMedGoogle Scholar
  59. 59.
    Lai N, Sims JK, Jeon NL, Lee K (2012) Adipocyte induction of preadipocyte differentiation in a gradient chamber. Tissue Eng Part C Methods 18:958–967.  https://doi.org/10.1089/ten.tec.2012.0168 CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Chang C-C, Chen C-Y, Wen H-C et al (2017) Caveolin-1 secreted from adipose tissues and adipocytes functions as an adipogenesis enhancer. Obesity 25:1932–1940.  https://doi.org/10.1002/oby.21970 CrossRefPubMedGoogle Scholar
  61. 61.
    Wei Y-T, Xia D-S, Yang W-K et al (2014) Secretion of adipocytes and macrophages under conditions of inflammation and/or insulin resistance and effect of adipocytes on preadipocytes under these conditions. Biochem Mosc 79:663–671.  https://doi.org/10.1134/S0006297914070086 CrossRefGoogle Scholar
  62. 62.
    Bacakova L, Zarubova J, Travnickova M et al (2018) Stem cells: their source, potency and use in regenerative therapies with focus on adipose-derived stem cells—a review. Biotechnol Adv 36:1111–1126.  https://doi.org/10.1016/j.biotechadv.2018.03.011 CrossRefPubMedGoogle Scholar
  63. 63.
    Green H, Kehinde O (1979) Formation of normally differentiated subcutaneous fat pads by an established preadipose cell line. J Cell Physiol 101:169–171CrossRefGoogle Scholar
  64. 64.
    Kimura Y, Ozeki M, Inamoto T, Tabata Y (2003) Adipose tissue engineering based on human preadipocytes combined with gelatin microspheres containing basic fibroblast growth factor. Biomaterials 24:2513–2521.  https://doi.org/10.1016/S0142-9612(03)00049-8 CrossRefPubMedGoogle Scholar
  65. 65.
    Tsuji W, Inamoto T, Yamashiro H et al (2009) Adipogenesis induced by human adipose tissue-derived stem cells. Tissue Eng Part A 15:83–93.  https://doi.org/10.1089/ten.tea.2007.0297 CrossRefPubMedGoogle Scholar
  66. 66.
    Wong JC, Krueger KC, Costa MJ et al (2016) A glucocorticoid- and diet-responsive pathway toggles adipocyte precursor cell activity in vivo. Sci Signal 9:ra103.  https://doi.org/10.1126/scisignal.aag0487 CrossRefPubMedGoogle Scholar
  67. 67.
    Lee M-J, Pramyothin P, Karastergiou K, Fried SK (2014) Deconstructing the roles of glucocorticoids in adipose tissue biology and the development of central obesity. Biochim Biophys Acta 1842:473–481.  https://doi.org/10.1016/j.bbadis.2013.05.029 CrossRefPubMedGoogle Scholar
  68. 68.
    Wu L, Wang T, Ge Y et al (2012) Secreted factors from adipose tissue increase adipogenic differentiation of mesenchymal stem cells. Cell Prolif 45:311–319.  https://doi.org/10.1111/j.1365-2184.2012.00823.x CrossRefPubMedGoogle Scholar
  69. 69.
    Rinker TE, Hammoudi TM, Kemp ML et al (2014) Interactions between mesenchymal stem cells, adipocytes, and osteoblasts in a 3D tri-culture model of hyperglycemic conditions in the bone marrow microenvironment. Integr Biol Quant Biosci Nano Macro 6:324–337.  https://doi.org/10.1039/c3ib40194d CrossRefGoogle Scholar
  70. 70.
    Challa TD, Straub LG, Balaz M et al (2015) Regulation of de novo adipocyte differentiation through cross talk between adipocytes and preadipocytes. Diabetes 64:4075–4087.  https://doi.org/10.2337/db14-1932 CrossRefPubMedGoogle Scholar
  71. 71.
    Schwalie PC, Dong H, Zachara M et al (2018) A stromal cell population that inhibits adipogenesis in mammalian fat depots. Nature 559:103–108.  https://doi.org/10.1038/s41586-018-0226-8 CrossRefPubMedGoogle Scholar
  72. 72.
    Williams GA, Wang Y, Callon KE et al (2009) In vitro and in vivo effects of adiponectin on bone. Endocrinology 150:3603–3610.  https://doi.org/10.1210/en.2008-1639 CrossRefPubMedGoogle Scholar
  73. 73.
    Kudoh A, Satoh H, Hirai H et al (2018) Preliminary evidence for adipocytokine signals in skeletal muscle glucose uptake. Front Endocrinol 9:295.  https://doi.org/10.3389/fendo.2018.00295 CrossRefGoogle Scholar
  74. 74.
    Seo K, Suzuki T, Kobayashi K, Nishimura T (2018) Adipocytes suppress differentiation of muscle cells in a co-culture system. Anim Sci J Nihon Chikusan Gakkaiho.  https://doi.org/10.1111/asj.13145 CrossRefPubMedGoogle Scholar
  75. 75.
    Maenhaut N, Van de Voorde J (2011) Regulation of vascular tone by adipocytes. BMC Med 9:25.  https://doi.org/10.1186/1741-7015-9-25 CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Huh JY, Park YJ, Ham M, Kim JB (2014) Crosstalk between adipocytes and immune cells in adipose tissue inflammation and metabolic dysregulation in obesity. Mol Cells 37:365–371.  https://doi.org/10.14348/molcells.2014.0074 CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Lim J-M, Sherling D, Teo CF et al (2008) Defining the regulated secreted proteome of rodent adipocytes upon the induction of insulin resistance. J Proteome Res 7:1251–1263.  https://doi.org/10.1021/pr7006945 CrossRefPubMedGoogle Scholar
  78. 78.
    Lehr S, Hartwig S, Lamers D et al (2012) Identification and validation of novel adipokines released from primary human adipocytes. Mol Cell Proteomics MCP 11(M111):010504.  https://doi.org/10.1074/mcp.M111.010504 CrossRefPubMedGoogle Scholar
  79. 79.
    Chen X, Hunt D, Cushman SW, Hess S (2009) Proteomic characterization of thiazolidinedione regulation of obese adipose secretome in Zucker obese rats. Proteomics Clin Appl 3:1099–1111.  https://doi.org/10.1002/prca.200900026 CrossRefPubMedGoogle Scholar
  80. 80.
    Krey G, Braissant O, L’Horset F et al (1997) Fatty acids, eicosanoids, and hypolipidemic agents identified as ligands of peroxisome proliferator-activated receptors by coactivator-dependent receptor ligand assay. Mol Endocrinol Baltim Md 11:779–791.  https://doi.org/10.1210/mend.11.6.0007 CrossRefGoogle Scholar
  81. 81.
    Hutley LJ, Newell FM, Joyner JM et al (2003) Effects of rosiglitazone and linoleic acid on human preadipocyte differentiation. Eur J Clin Invest 33:574–581CrossRefGoogle Scholar
  82. 82.
    Massiera F, Saint-Marc P, Seydoux J et al (2003) Arachidonic acid and prostacyclin signaling promote adipose tissue development: a human health concern? J Lipid Res 44:271–279.  https://doi.org/10.1194/jlr.M200346-JLR200 CrossRefPubMedGoogle Scholar
  83. 83.
    Mathivanan S, Ji H, Simpson RJ (2010) Exosomes: extracellular organelles important in intercellular communication. J Proteomics 73:1907–1920.  https://doi.org/10.1016/j.jprot.2010.06.006 CrossRefPubMedGoogle Scholar
  84. 84.
    Dai M, Yu M, Zhang Y, Tian W (2017) Exosome-like vesicles derived from adipose tissue provide biochemical cues for adipose tissue regeneration. Tissue Eng Part A 23:1221–1230.  https://doi.org/10.1089/ten.tea.2017.0045 CrossRefPubMedGoogle Scholar
  85. 85.
    Sano S, Izumi Y, Yamaguchi T et al (2014) Lipid synthesis is promoted by hypoxic adipocyte-derived exosomes in 3T3-L1 cells. Biochem Biophys Res Commun 445:327–333.  https://doi.org/10.1016/j.bbrc.2014.01.183 CrossRefPubMedGoogle Scholar
  86. 86.
    Hartwig S, De Filippo E, Göddeke S et al (2018) Exosomal proteins constitute an essential part of the human adipose tissue secretome. Biochim Biophys Acta BBA Proteins Proteom.  https://doi.org/10.1016/j.bbapap.2018.11.009 CrossRefGoogle Scholar
  87. 87.
    Rui L (2017) Brown and beige adipose tissues in health and disease. In: Terjung R (ed) Comprehensive physiology. Wiley, Hoboken, pp 1281–1306CrossRefGoogle Scholar
  88. 88.
    Scheideler M, Herzig S, Georgiadi A (2017) Endocrine and autocrine/paracrine modulators of brown adipose tissue mass and activity as novel therapeutic strategies against obesity and type 2 diabetes. Horm Mol Biol Clin Investig.  https://doi.org/10.1515/hmbci-2017-0043 CrossRefPubMedGoogle Scholar
  89. 89.
    Ali Khan A, Hansson J, Weber P et al (2018) Comparative secretome analyses of primary murine white and brown adipocytes reveal novel adipokines. Mol Cell Proteom 17:2358–2370.  https://doi.org/10.1074/mcp.RA118.000704 CrossRefGoogle Scholar
  90. 90.
    Gnad T, Scheibler S, von Kügelgen I et al (2014) Adenosine activates brown adipose tissue and recruits beige adipocytes via A2A receptors. Nature 516:395–399.  https://doi.org/10.1038/nature13816 CrossRefPubMedGoogle Scholar
  91. 91.
    Tseng Y-H, Kokkotou E, Schulz TJ et al (2008) New role of bone morphogenetic protein 7 in brown adipogenesis and energy expenditure. Nature 454:1000–1004.  https://doi.org/10.1038/nature07221 CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Whittle AJ, Carobbio S, Martins L et al (2012) BMP8B increases brown adipose tissue thermogenesis through both central and peripheral actions. Cell 149:871–885.  https://doi.org/10.1016/j.cell.2012.02.066 CrossRefPubMedPubMedCentralGoogle Scholar
  93. 93.
    Klepac K, Kilić A, Gnad T et al (2016) The Gq signalling pathway inhibits brown and beige adipose tissue. Nat Commun 7:10895.  https://doi.org/10.1038/ncomms10895 CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Villarroya F, Cereijo R, Villarroya J, Giralt M (2017) Brown adipose tissue as a secretory organ. Nat Rev Endocrinol 13:26–35.  https://doi.org/10.1038/nrendo.2016.136 CrossRefPubMedGoogle Scholar
  95. 95.
    Poulos SP, Dodson MV, Hausman GJ (2010) Cell line models for differentiation: preadipocytes and adipocytes. Exp Biol Med 235:1185–1193.  https://doi.org/10.1258/ebm.2010.010063 CrossRefGoogle Scholar
  96. 96.
    Chusyd DE, Wang D, Huffman DM, Nagy TR (2016) Relationships between rodent white adipose fat pads and human white adipose fat depots. Front Nutr 3:10.  https://doi.org/10.3389/fnut.2016.00010 CrossRefPubMedPubMedCentralGoogle Scholar
  97. 97.
    Steppan CM, Bailey ST, Bhat S et al (2001) The hormone resistin links obesity to diabetes. Nature 409:307–312.  https://doi.org/10.1038/35053000 CrossRefPubMedGoogle Scholar
  98. 98.
    Patel L, Buckels AC, Kinghorn IJ et al (2003) Resistin is expressed in human macrophages and directly regulated by PPAR gamma activators. Biochem Biophys Res Commun 300:472–476.  https://doi.org/10.1016/s0006-291x(02)02841-3 CrossRefPubMedGoogle Scholar
  99. 99.
    Blaszkiewicz M, Willows JW, Johnson CP, Townsend KL (2019) The importance of peripheral nerves in adipose tissue for the regulation of energy balance. Biology.  https://doi.org/10.3390/biology8010010 CrossRefPubMedPubMedCentralGoogle Scholar
  100. 100.
    Wang QA, Scherer PE (2014) The AdipoChaser mouse: a model tracking adipogenesis in vivo. Adipocyte 3:146–150.  https://doi.org/10.4161/adip.27656 CrossRefPubMedPubMedCentralGoogle Scholar
  101. 101.
    Wolfrum C, Straub LG (2019) Lessons from cre-mice and indicator mice. In: Pfeifer A, Klingenspor M, Herzig S (eds) Brown adipose tissue. Springer International Publishing, Cham, pp 37–54Google Scholar
  102. 102.
    Rydén M, Uzunel M, Hård JL et al (2015) Transplanted bone marrow-derived cells contribute to human adipogenesis. Cell Metab 22:408–417.  https://doi.org/10.1016/j.cmet.2015.06.011 CrossRefPubMedGoogle Scholar
  103. 103.
    Arner E, Westermark PO, Spalding KL et al (2010) Adipocyte turnover: relevance to human adipose tissue morphology. Diabetes 59:105–109.  https://doi.org/10.2337/db09-0942 CrossRefPubMedGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Medicine, Faculty of Medicine and Health SciencesStellenbosch UniversityCape TownSouth Africa

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