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Review Articles

Increasing adipocyte number and reducing adipocyte size: the role of retinoids in adipose tissue development and metabolism

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References

  • Abd Eldaim, M. A., S. Matsuoka, Y. Okamatsu-Ogura, A. Kamikawa, M. M. Ahmed, A. Terao, K.-I. Nakajima, and K. Kimura. 2017. Retinoic acid modulates lipid accumulation glucose concentration dependently through inverse regulation of SREBP‐1 expression in 3T3L1 adipocytes. Genes to Cells: devoted to Molecular & Cellular Mechanisms 22 (6):568–82. doi: 10.1111/gtc.12498.
  • Acosta, J. R., I. Douagi, D. P. Andersson, J. Bäckdahl, M. Rydén, P. Arner, and J. Laurencikiene. 2016. Increased fat cell size: A major phenotype of subcutaneous white adipose tissue in non-obese individuals with type 2 diabetes. Diabetologia 59 (3):560–70. doi: 10.1007/s00125-015-3810-6.
  • Akinci, B., M. Sahinoz, and E. Oral. 2018. Lipodystrophy syndromes: Presentation and treatment.
  • Almuraikhy, S., W. Kafienah, M. Bashah, I. Diboun, M. Jaganjac, F. Al-Khelaifi, H. Abdesselem, N. A. Mazloum, M. Alsayrafi, V. Mohamed-Ali, et al. 2016. Interleukin-6 induces impairment in human subcutaneous adipogenesis in obesity-associated insulin resistance. Diabetologia 59 (11):2406–16. doi: 10.1007/s00125-016-4031-3.
  • Avram, M. M., A. S. Avram, and W. D. James. 2007. Subcutaneous fat in normal and diseased states 3. Adipogenesis: From stem cell to fat cell. Journal of the American Academy of Dermatology 56 (3):472–92. doi: 10.1016/j.jaad.2006.06.022.
  • Azzu, V., M. Vacca, S. Virtue, M. Allison, and A. Vidal-Puig. 2020. Adipose tissue-liver cross talk in the control of whole-body metabolism: Implications in nonalcoholic fatty liver disease. Gastroenterology 158 (7):1899–912. doi: 10.1053/j.gastro.2019.12.054.
  • Bachman, E. S., H. Dhillon, C.-Y. Zhang, S. Cinti, A. C. Bianco, B. K. Kobilka, and B. B. Lowell. 2002. betaAR signaling required for diet-induced thermogenesis and obesity resistance. Science (New York, N.Y.) 297 (5582):843–5. doi: 10.1126/science.1073160.
  • Bakker, L. E. H., M. R. Boon, R. A. D. van der Linden, L. P. Arias-Bouda, J. B. van Klinken, F. Smit, H. J. Verberne, J. W. Jukema, J. T. Tamsma, L. M. Havekes, et al. 2014. Brown adipose tissue volume in healthy lean south Asian adults compared with white Caucasians: A prospective, case-controlled observational study. The Lancet. Diabetes & Endocrinology 2 (3):210–7. doi: 10.1016/S2213-8587(13)70156-6.
  • Bal, N. C., S. Singh, F. C. G. Reis, S. K. Maurya, S. Pani, L. A. Rowland, and M. Periasamy. 2017. Both brown adipose tissue and skeletal muscle thermogenesis processes are activated during mild to severe cold adaptation in mice. The Journal of Biological Chemistry 292 (40):16616–25. doi: 10.1074/jbc.M117.790451.
  • Barouch, L. A., D. E. Berkowitz, R. W. Harrison, C. P. O’Donnell, and J. M. Hare. 2003. Disruption of leptin signaling contributes to cardiac hypertrophy independently of body weight in mice. Circulation 108 (6):754–9. doi: 10.1161/01.CIR.0000083716.82622.FD.
  • Bartelt, A., O. T. Bruns, R. Reimer, H. Hohenberg, H. Ittrich, K. Peldschus, M. G. Kaul, U. I. Tromsdorf, H. Weller, C. Waurisch, et al. 2011. Brown adipose tissue activity controls triglyceride clearance. Nature Medicine 17 (2):200–5. doi: 10.1038/nm.2297.
  • Bento, C., A. C. Matos, A. Cordeiro, and A. Ramalho. 2018. Vitamin A deficiency is associated with body mass index and body adiposity in women with recommended intake of vitamin A. Nutricion Hospitalaria 35 (5):1072–8. doi: 10.20960/nh.1630.
  • Berry, D. C., and N. Noy. 2009. All-trans-retinoic acid represses obesity and insulin resistance by activating both peroxisome proliferation-activated receptor beta/delta and retinoic acid receptor. Molecular and Cellular Biology 29 (12):3286–96. doi: 10.1128/MCB.01742-08.
  • Berry, D. C., D. DeSantis, H. Soltanian, C. M. Croniger, and N. Noy. 2012. Retinoic acid upregulates preadipocyte genes to block adipogenesis and suppress diet-induced obesity. Diabetes 61 (5):1112–21. doi: 10.2337/db11-1620.
  • Berry, D. C., H. Soltanian, and N. Noy. 2010. Repression of cellular retinoic acid-binding protein II during adipocyte differentiation. The Journal of Biological Chemistry 285 (20):15324–32. doi: 10.1074/jbc.M110.110635.
  • Blaner, W. S. 2019. Vitamin A signaling and homeostasis in obesity, diabetes, and metabolic disorders. Pharmacology & Therapeutics 197:153–78. doi: 10.1016/j.pharmthera.2019.01.006.
  • Blaner, W. S., S. M. O’Byrne, N. Wongsiriroj, J. Kluwe, D. M. D’Ambrosio, H. Jiang, R. F. Schwabe, E. M. C. Hillman, R. Piantedosi, J. Libien, et al. 2009. Hepatic stellate cell lipid droplets: A specialized lipid droplet for retinoid storage. Biochimica et Biophysica Acta 1791 (6):467–73. doi: 10.1016/j.bbalip.2008.11.001.
  • Blomhoff, R., M. H. Green, J. B. Green, T. Berg, and K. R. Norum. 1991. Vitamin A metabolism: New perspectives on absorption, transport, and storage. Physiological Reviews 71 (4):951–90. doi: 10.1152/physrev.1991.71.4.951.
  • Blondin, D. P., A. Daoud, T. Taylor, H. C. Tingelstad, V. Bézaire, D. Richard, A. C. Carpentier, A. W. Taylor, M.-E. Harper, C. Aguer, et al. 2017. Four-week cold acclimation in adult humans shifts uncoupling thermogenesis from skeletal muscles to brown adipose ­tissue. The Journal of Physiology 595 (6):2099–113. doi: 10.1113/JP273395.
  • Bonnet, M., I. Cassar-Malek, Y. Chilliard, and B. Picard. 2010. Ontogenesis of muscle and adipose tissues and their interactions in ruminants and other species. Animal : An International Journal of Animal Bioscience 4 (7):1093–109. doi: 10.1017/S1751731110000601.
  • Brakenhielm, E, et al. 2004. Angiogenesis inhibitor, TNP-470, prevents diet-induced and genetic obesity in mice. Circ Res 94 (12):1579–88.
  • Bråkenhielm, E., N. Veitonmäki, R. Cao, S. Kihara, Y. Matsuzawa, B. Zhivotovsky, T. Funahashi, and Y. Cao. 2004. Adiponectin-induced antiangiogenesis and antitumor activity involve caspase-mediated endothelial cell apoptosis. Proceedings of the National Academy of Sciences 101 (8):2476–81. doi: 10.1073/pnas.0308671100.
  • Broch, M., J. Vendrell, W. Ricart, C. Richart, and J.-M. Fernández-Real. 2007. Circulating retinol-binding protein-4, insulin sensitivity, insulin secretion, and insulin disposition index in obese and nonobese subjects. Diabetes Care 30 (7):1802–6. doi: 10.2337/dc06-2034.
  • Bukowiecki, L., A. J. Collet, N. Follea, G. Guay, and L. Jahjah. 1982. Brown adipose tissue hyperplasia: A fundamental mechanism of adaptation to cold and hyperphagia. The American Journal of Physiology 242 (6):E353–9. doi: 10.1152/ajpendo.1982.242.6.E353.
  • Cannon, B., and J. Nedergaard. 2004. Brown adipose tissue: Function and physiological significance. Physiological Reviews 84 (1):277–359. doi: 10.1152/physrev.00015.2003.
  • Cao, W., A. V. Medvedev, K. W. Daniel, and S. Collins. 2001. beta-Adrenergic activation of p38 MAP kinase in adipocytes: CAMP induction of the uncoupling protein 1 (UCP1) gene requires p38 MAP kinase. The Journal of Biological Chemistry 276 (29):27077–82. doi: 10.1074/jbc.M101049200.
  • Cao, W., K. W. Daniel, J. Robidoux, P. Puigserver, A. V. Medvedev, X. Bai, L. M. Floering, B. M. Spiegelman, and S. Collins. 2004. p38 mitogen-activated protein kinase is the central regulator of cyclic AMP-dependent transcription of the brown fat uncoupling protein 1 gene. Molecular and Cellular Biology 24 (7):3057–67. doi: 10.1128/MCB.24.7.3057-3067.2004.
  • Cao, Y. 2007. Angiogenesis modulates adipogenesis and obesity. The Journal of Clinical Investigation 117 (9):2362–8. doi: 10.1172/JCI32239.
  • Cao, Y. 2010. Adipose tissue angiogenesis as a therapeutic target for obesity and metabolic diseases. Nature Reviews. Drug Discovery 9 (2):107–15. doi: 10.1038/nrd3055.
  • Cao, Y. 2013. Angiogenesis and vascular functions in modulation of obesity, adipose metabolism, and insulin sensitivity. Cell Metabolism 18 (4):478–89. doi: 10.1016/j.cmet.2013.08.008.
  • Cattaneo, P., D. Mukherjee, S. Spinozzi, L. Zhang, V. Larcher, W. B. Stallcup, H. Kataoka, J. Chen, S. Dimmeler, S. M. Evans, et al. 2020. Parallel lineage-tracing studies establish fibroblasts as the prevailing in vivo adipocyte progenitor. Cell Reports 30 (2):571–82.e2. doi: 10.1016/j.celrep.2019.12.046.
  • Chawla, A., J. J. Repa, R. M. Evans, and D. J. Mangelsdorf. 2001. Nuclear receptors and lipid physiology: Opening the X-files. Science (New York, N.Y.) 294 (5548):1866–70. doi: 10.1126/science.294.5548.1866.
  • Chen, H., M. Montagnani, T. Funahashi, I. Shimomura, and M. J. Quon. 2003. Adiponectin stimulates production of nitric oxide in vascular endothelial cells. The Journal of Biological Chemistry 278 (45):45021–6. doi: 10.1074/jbc.M307878200.
  • Chen, J.-T., J.-B. Liang, C.-L. Chou, R.-C. Shyu, and D.-W. Lu. 2005. Retinoic acid induces VEGF gene expression in human retinal pigment epithelial cells (ARPE-19). Journal of Ocular Pharmacology and Therapeutics 21 (6):413–9. doi: 10.1089/jop.2005.21.413.
  • Chondronikola, M., E. Volpi, E. Børsheim, T. Chao, C. Porter, P. Annamalai, C. Yfanti, S. M. Labbe, N. M. Hurren, I. Malagaris, et al. 2016. Brown adipose tissue is linked to a distinct thermoregulatory response to mild cold in people. Frontiers in Physiology 7:129. doi: 10.3389/fphys.2016.00129.
  • Cinti, S., G. Mitchell, G. Barbatelli, I. Murano, E. Ceresi, E. Faloia, S. Wang, M. Fortier, A. S. Greenberg, M. S. Obin, et al. 2005. Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans. Journal of Lipid Research 46 (11):2347–55. doi: 10.1194/jlr.M500294-JLR200.
  • Cohlan, S. Q. 1954. Congenital anomalies in the rat produced by excessive intake of vitamin A during pregnancy. Pediatrics 13 (6):556–67. doi: 10.1542/peds.13.6.556.
  • Coulthard, L. R., D. E. White, D. L. Jones, M. F. McDermott, and S. A. Burchill. 2009. p38(MAPK): stress responses from molecular mechanisms to therapeutics. Trends in Molecular Medicine 15 (8):369–79. doi: 10.1016/j.molmed.2009.06.005.
  • Crewe, C., N. Joffin, J. M. Rutkowski, M. Kim, F. Zhang, D. A. Towler, R. Gordillo, and P. E. Scherer. 2018. An endothelial-to-adipocyte extracellular vesicle axis governed by metabolic state. Cell 175 (3):695–708 e13. doi: 10.1016/j.cell.2018.09.005.
  • Crewe, C., Y. A. An, and P. E. Scherer. 2017. The ominous triad of adipose tissue dysfunction: Inflammation, fibrosis, and impaired angiogenesis. The Journal of Clinical Investigation 127 (1):74–82. doi: 10.1172/JCI88883.
  • Crisan, M., S. Yap, L. Casteilla, C.-W. Chen, M. Corselli, T. S. Park, G. Andriolo, B. Sun, B. Zheng, L. Zhang, et al. 2008. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3 (3):301–13. doi: 10.1016/j.stem.2008.07.003.
  • D’Ambrosio, D. N., R. D. Clugston, and W. S. Blaner. 2011. Vitamin A metabolism: An update. Nutrients 3 (1):63–103. doi: 10.3390/nu3010063.
  • Dani, C., A. G. Smith, S. Dessolin, P. Leroy, L. Staccini, P. Villageois, C. Darimont, and G. Ailhaud. 1997. Differentiation of embryonic stem cells into adipocytes in vitro. Journal of Cell Science 110 (11):1279–85. doi: 10.1242/jcs.110.11.1279.
  • de Carvalho Schweich-Adami, L., A. C. M. B. Antoniolli-Silva, and R. J. Oliveira. 2022. The treatment with all-trans retinoic acid causes apoptosis without chromosomal instability in adipose-derived stem cells and might act starting the browning process. Research, Society and Development 11 (3):e53511326787-e53511326787. doi: 10.33448/rsd-v11i3.26787.
  • de Souza Valente da Silva, L., G. Valeria da Veiga, and R. A. Ramalho. 2007. Association of serum concentrations of retinol and carotenoids with overweight in children and adolescents. Nutrition 23 (5):392–7. doi: 10.1016/j.nut.2007.02.009.
  • de The, H., M. del Mar Vivanco-Ruiz, P. Tiollais, H. Stunnenberg, and A. Dejean. 1990. Identification of a retinoic acid responsive element in the retinoic acid receptor beta gene. Nature 343 (6254):177–80. doi: 10.1038/343177a0.
  • Dempersmier, J., A. Sambeat, O. Gulyaeva, S. M. Paul, C. S. S. Hudak, H. F. Raposo, H.-Y. Kwan, C. Kang, R. H. F. Wong, H. S. Sul, et al. 2015. Cold-inducible Zfp516 activates UCP1 transcription to promote browning of white fat and development of brown fat. Molecular Cell 57 (2):235–46. doi: 10.1016/j.molcel.2014.12.005.
  • Di Dalmazi, G., V. Vicennati, R. Pasquali, and U. Pagotto. 2013. The unrelenting fall of the pharmacological treatment of obesity. Endocrine 44 (3):598–609. doi: 10.1007/s12020-013-9983-1.
  • Dragoo, J. L., S. A. Shapiro, H. Bradsell, and R. M. Frank. 2021. The essential roles of human adipose tissue: Metabolic, thermoregulatory, cellular, and paracrine effects. Journal of Cartilage & Joint Preservation 1 (3):100023. doi: 10.1016/j.jcjp.2021.100023.
  • Elattar, S., and A. Satyanarayana. 2015. Can brown fat win the battle against white fat? Journal of Cellular Physiology 230 (10):2311–7. doi: 10.1002/jcp.24986.
  • Elias, I., S. Franckhauser, T. Ferré, L. Vilà, S. Tafuro, S. Muñoz, C. Roca, D. Ramos, A. Pujol, E. Riu, et al. 2012. Adipose tissue overexpression of vascular endothelial growth factor protects against diet-induced obesity and insulin resistance. Diabetes 61 (7):1801–13. doi: 10.2337/db11-0832.
  • Elsen, M., S. Raschke, N. Tennagels, U. Schwahn, T. Jelenik, M. Roden, T. Romacho, and J. Eckel. 2014. BMP4 and BMP7 induce the white-to-brown transition of primary human adipose stem cells. American Journal of Physiology. Cell Physiology 306 (5):C431–40. doi: 10.1152/ajpcell.00290.2013.
  • Enerback, S. 2010. Human brown adipose tissue. Cell Metabolism. 11 (4):248–52. doi: 10.1016/j.cmet.2010.03.008.
  • Erikstrup, C., O. H. Mortensen, A. R. Nielsen, C. P. Fischer, P. Plomgaard, A. M. Petersen, R. Krogh-Madsen, B. Lindegaard, J. G. Erhardt, H. Ullum, et al. 2009. RBP‐to‐retinol ratio, but not total RBP, is elevated in patients with type 2 diabetes. Diabetes, Obesity & Metabolism 11 (3):204–12. doi: 10.1111/j.1463-1326.2008.00901.x.
  • Fajas, L., M. B. Debril, and J. Auwerx. 2001. Peroxisome proliferator-activated receptor-gamma: From adipogenesis to carcinogenesis. Journal of Molecular Endocrinology 27 (1):1–9. doi: 10.1677/jme.0.0270001.
  • Farjo, K. M., R. A. Farjo, S. Halsey, G. Moiseyev, and J.-X. Ma. 2012. Retinol-binding protein 4 induces inflammation in human endothelial cells by an NADPH oxidase- and nuclear factor kappa B-dependent and retinol-independent mechanism. Molecular and Cellular Biology 32 (24):5103–15. doi: 10.1128/MCB.00820-12.
  • Fernandez-Marcos, P. J., and J. Auwerx. 2011. Regulation of PGC-1alpha, a nodal regulator of mitochondrial biogenesis. The American Journal of Clinical Nutrition 93 (4):884S–90. doi: 10.3945/ajcn.110.001917.
  • Feve, B. 2005. Adipogenesis: Cellular and molecular aspects. Best Practice & Research Clinical Endocrinology & Metabolism 19 (4):483–99. doi: 10.1016/j.beem.2005.07.007.
  • Fischer, A. W., C. Schlein, B. Cannon, J. Heeren, and J. Nedergaard. 2019. Intact innervation is essential for diet-induced recruitment of brown adipose tissue. American Journal of Physiology. Endocrinology and Metabolism 316 (3):E487–E503. doi: 10.1152/ajpendo.00443.2018.
  • Gao, Z., A. C. Daquinag, F. Su, B. Snyder, and M. G. Kolonin. 2017. PDGFRα/PDGFRβ signaling balance modulates progenitor cell differentiation into white and beige adipocytes. Development 145 (1):dev155861. doi: 10.1242/dev.155861.
  • Gealekman, O., N. Guseva, C. Hartigan, S. Apotheker, M. Gorgoglione, K. Gurav, K.-V. Tran, J. Straubhaar, S. Nicoloro, M. P. Czech, et al. 2011. Depot-specific differences and insufficient subcutaneous adipose tissue angiogenesis in human obesity. Circulation 123 (2):186–94. doi: 10.1161/CIRCULATIONAHA.110.970145.
  • Geloen, A., A. J. Collet, and L. J. Bukowiecki. 1992. Role of sympathetic innervation in brown adipocyte proliferation. The American Journal of Physiology 263 (6 Pt 2):R1176–81. doi: 10.1152/ajpregu.1992.263.6.R1176.
  • Geloen, A., A. J. Collet, G. Guay, and L. J. Bukowiecki. 1988. Beta-adrenergic stimulation of brown adipocyte proliferation. American Journal of Physiology-Cell Physiology 254 (1):C175–C182. doi: 10.1152/ajpcell.1988.254.1.C175.
  • Gesta, S., Y. H. Tseng, and C. R. Kahn. 2007. Developmental origin of fat: Tracking obesity to its source. Cell 131 (2):242–56. doi: 10.1016/j.cell.2007.10.004.
  • Ghaben, A. L., and P. E. Scherer. 2019. Adipogenesis and metabolic health. Nature Reviews. Molecular Cell Biology 20 (4):242–58. doi: 10.1038/s41580-018-0093-z.
  • Góes, É., A. Cordeiro, C. Bento, and A. Ramalho. 2023. Vitamin A deficiency and its association with visceral adiposity in women. Biomedicines 11 (3):991. doi: 10.3390/biomedicines11030991.
  • Goodman, D. W., H. S. Huang, and T. Shiratori. 1965. Tissue distribution and metabolism of newly absorbed vitamin a in the rat. Journal of Lipid Research. 6 (3):390–6. doi: 10.1016/S0022-2275(20)39309-3.
  • Guimaraes-Camboa, N., and S. M. Evans. 2017. Are Perivascular Adipocyte Progenitors Mural Cells or Adventitial Fibroblasts? Cell Stem Cell 20 (5):587–9. doi: 10.1016/j.stem.2017.04.010.
  • Gupta, R. K., R. J. Mepani, S. Kleiner, J. C. Lo, M. J. Khandekar, P. Cohen, A. Frontini, D. C. Bhowmick, L. Ye, S. Cinti, et al. 2012. Zfp423 expression identifies committed preadipocytes and localizes to adipose endothelial and perivascular cells. Cell Metabolism 15 (2):230–9. doi: 10.1016/j.cmet.2012.01.010.
  • Gupta, R. K., Z. Arany, P. Seale, R. J. Mepani, L. Ye, H. M. Conroe, Y. A. Roby, H. Kulaga, R. R. Reed, B. M. Spiegelman, et al. 2010. Transcriptional control of preadipocyte determination by Zfp423. Nature 464 (7288):619–23. doi: 10.1038/nature08816.
  • Habek, N., M. Dobrivojević Radmilović, M. Kordić, K. Ilić, S. Grgić, V. Farkaš, R. Bagarić, S. Škokić, A. Švarc, A. Dugandžić, et al. 2020. Activation of brown adipose tissue in diet-induced thermogenesis is GC-C dependent. Pflugers Archiv : European Journal of Physiology 472 (3):405–17. doi: 10.1007/s00424-020-02347-8.
  • Haenisch, M., T. Nguyen, C. A. Fihn, A. S. Goldstein, J. K. Amory, P. Treuting, T. Brabb, and J. Paik. 2021. Investigation of an ALDH1A1-specific inhibitor for suppression of weight gain in a diet-induced mouse model of obesity. International Journal of Obesity (2005) 45 (7):1542–52. doi: 10.1038/s41366-021-00818-1.
  • Halberg, N., T. Khan, M. E. Trujillo, I. Wernstedt-Asterholm, A. D. Attie, S. Sherwani, Z. V. Wang, S. Landskroner-Eiger, S. Dineen, U. J. Magalang, et al. 2009. Hypoxia-inducible factor 1alpha induces ­fibrosis and insulin resistance in white adipose tissue. Molecular and Cellular Biology 29 (16):4467–83. doi: 10.1128/MCB.00192-09.
  • Hammarstedt, A., S. Gogg, S. Hedjazifar, A. Nerstedt, and U. Smith. 2018. Impaired adipogenesis and dysfunctional adipose tissue in ­human hypertrophic obesity. Physiological Reviews 98 (4):1911–41. doi: 10.1152/physrev.00034.2017.
  • Harari, A., A. C. F. Coster, A. Jenkins, A. Xu, J. R. Greenfield, D. Harats, A. Shaish, and D. Samocha-Bonet. 2020. Obesity and insulin resistance are inversely associated with serum and adipose tissue carotenoid concentrations in adults. The Journal of Nutrition 150 (1):38–46. doi: 10.1093/jn/nxz184.
  • Hayward, J. S., and P. A. Lisson. 1992. Evolution of brown fat: Its absence in marsupials and monotremes. Canadian Journal of Zoology 70 (1):171–9. doi: 10.1139/z92-025.
  • Ho, K. K. Y. 2018. Diet-induced thermogenesis: Fake friend or foe? The Journal of Endocrinology 238 (3):R185–R191. doi: 10.1530/JOE-18-0240.
  • Hoffmann, S., A. Rockenstein, A. Ramaswamy, I. Celik, A. Wunderlich, S. Lingelbach, L. C. Hofbauer, and A. Zielke. 2007. Retinoic acid inhibits angiogenesis and tumor growth of thyroid cancer cells. Molecular and Cellular Endocrinology 264 (1-2):74–81. doi: 10.1016/j.mce.2006.10.009.
  • Hondares, E., M. Rosell, J. Díaz-Delfín, Y. Olmos, M. Monsalve, R. Iglesias, F. Villarroya, and M. Giralt. 2011. Peroxisome proliferator-activated receptor alpha (PPARalpha) induces PPARgamma coactivator 1alpha (PGC-1alpha) gene expression and contributes to thermogenic activation of brown fat: Involvement of PRDM16. The Journal of Biological Chemistry 286 (50):43112–22. doi: 10.1074/jbc.M111.252775.
  • Huang, H., T.-J. Song, X. Li, L. Hu, Q. He, M. Liu, M. D. Lane, and Q.-Q. Tang. 2009. BMP signaling pathway is required for commitment of C3H10T1/2 pluripotent stem cells to the adipocyte lineage. Proceedings of the National Academy of Sciences of the United States of America 106 (31):12670–5. doi: 10.1073/pnas.0906266106.
  • Hudak, C. S., O. Gulyaeva, Y. Wang, S.-M. Park, L. Lee, C. Kang, and H. S. Sul. 2014. Pref-1 marks very early mesenchymal precursors required for adipose tissue development and expansion. Cell Reports 8 (3):678–87. doi: 10.1016/j.celrep.2014.06.060.
  • Huttala, O., J.-R. Sarkanen, M. Mannerström, T. Toimela, T. Heinonen, and T. Ylikomi. 2020. Development of novel human in vitro vascularized adipose tissue model with functional macrophages. Cytotechnology 72 (5):665–83. doi: 10.1007/s10616-020-00407-6.
  • Ikeda, K., P. Maretich, and S. Kajimura. 2018. The Common and Distinct Features of Brown and Beige Adipocytes. Trends in Endocrinology and Metabolism: TEM 29 (3):191–200. doi: 10.1016/j.tem.2018.01.001.
  • Janke, J., S. Engeli, M. Boschmann, F. Adams, J. Böhnke, F. C. Luft, A. M. Sharma, and J. Jordan. 2006. Retinol-binding protein 4 in human obesity. Diabetes 55 (10):2805–10. doi: 10.2337/db06-0616.
  • Janssens, P. L. H. R., R. Hursel, E. A. P. Martens, and M. S. Westerterp-Plantenga. 2013. Acute effects of capsaicin on energy expenditure and fat oxidation in negative energy balance. PloS One 8 (7):e67786. doi: 10.1371/journal.pone.0067786.
  • Kajimura, S., P. Seale, K. Kubota, E. Lunsford, J. V. Frangioni, S. P. Gygi, and B. M. Spiegelman. 2009. Initiation of myoblast to brown fat switch by a PRDM16-C/EBP-beta transcriptional complex. Nature 460 (7259):1154–8. doi: 10.1038/nature08262.
  • Kashyap, V., and L. J. Gudas. 2010. Epigenetic regulatory mechanisms distinguish retinoic acid-mediated transcriptional responses in stem cells and fibroblasts. The Journal of Biological Chemistry 285 (19):14534–48. doi: 10.1074/jbc.M110.115345.
  • Kawaguchi, R., J. Yu, J. Honda, J. Hu, J. Whitelegge, P. Ping, P. Wiita, D. Bok, and H. Sun. 2007. A membrane receptor for retinol binding protein mediates cellular uptake of vitamin A. Science (New York, N.Y.) 315 (5813):820–5. doi: 10.1126/science.1136244.
  • Khan, T., E. S. Muise, P. Iyengar, Z. V. Wang, M. Chandalia, N. Abate, B. B. Zhang, P. Bonaldo, S. Chua, P. E. Scherer, et al. 2009. Metabolic dysregulation and adipose tissue fibrosis: Role of collagen VI. Molecular and Cellular Biology 29 (6):1575–91. doi: 10.1128/MCB.01300-08.
  • Kiefer, F. W., C. Vernochet, P. O’Brien, S. Spoerl, J. D. Brown, S. Nallamshetty, M. Zeyda, T. M. Stulnig, D. E. Cohen, C. R. Kahn, et al. 2012. Retinaldehyde dehydrogenase 1 regulates a thermogenic program in white adipose tissue. Nature Medicine 18 (6):918–25. doi: 10.1038/nm.2757.
  • Kilicarslan, M., B. A. de Weijer, K. Simonyté Sjödin, P. Aryal, K. W. Ter Horst, H. Cakir, J. A. Romijn, M. T. Ackermans, I. M. Janssen, F. J. Berends, et al. 2020. RBP4 increases lipolysis in human adipocytes and is associated with increased lipolysis and hepatic insulin resistance in obese women. FASEB Journal 34 (5):6099–110. doi: 10.1096/fj.201901979RR.
  • Klein, S., L. Fontana, V. L. Young, A. R. Coggan, C. Kilo, B. W. Patterson, and B. S. Mohammed. 2004. Absence of an effect of liposuction on insulin action and risk factors for coronary heart disease. The New England Journal of Medicine 350 (25):2549–57. doi: 10.1056/NEJMoa033179.
  • Klöting, N., M. Fasshauer, A. Dietrich, P. Kovacs, M. R. Schön, M. Kern, M. Stumvoll, and M. Blüher. 2010. Insulin-sensitive obesity. American Journal of Physiology-Endocrinology and Metabolism 299 (3):E506–E515. doi: 10.1152/ajpendo.00586.2009.
  • Kogure, K., M. Morita, S. Hama, S. Nakashima, A. Tokumura, and K. Fukuzawa. 2002. Enhancement by alpha-tocopheryl hemisuccinate of nitric oxide production induced by lypopolysaccharide and interferon-gamma through the upregulation of protein kinase C in rat vascular smooth muscle cells. European Journal of Biochemistry 269 (9):2367–72. doi: 10.1046/j.1432-1033.2002.02894.x.
  • Krois, C. R., M. G. Vuckovic, P. Huang, C. Zaversnik, C. S. Liu, C. E. Gibson, M. R. Wheeler, K. M. Obrochta, J. H. Min, C. B. Herber, et al. 2019. RDH1 suppresses adiposity by promoting brown adipose adaptation to fasting and re-feeding. Cellular and Molecular Life Sciences : CMLS 76 (12):2425–47. doi: 10.1007/s00018-019-03046-z.
  • Krotkiewski, M., P. Björntorp, L. Sjöström, and U. Smith. 1983. Impact of obesity on metabolism in men and women. Importance of regional adipose tissue distribution. The Journal of Clinical Investigation 72 (3):1150–62. doi: 10.1172/JCI111040.
  • Lajevic, M. D., S. Suleiman, R. L. Cohen, and D. A. Chambers. 2011. Activation of p38 mitogen-activated protein kinase by norepinephrine in T-lineage cells. Immunology 132 (2):197–208. doi: 10.1111/j.1365-2567.2010.03354.x.
  • Lean, M. E., and W. P. T. James. 1986. Brown adipose tissue in man. Brown adipose tissue/edited by Paul Trayhurn and David G. Nicholls. London: Edward Arnold.
  • Lee, Y. S., J.-W. Kim, O. Osborne, D. Y. Oh, R. Sasik, S. Schenk, A. Chen, H. Chung, A. Murphy, S. M. Watkins, et al. 2014. Increased adipocyte O2 consumption triggers HIF-1alpha, causing inflammation and insulin resistance in obesity. Cell 157 (6):1339–52. doi: 10.1016/j.cell.2014.05.012.
  • Lee, Y.-H., A. P. Petkova, E. P. Mottillo, and J. G. Granneman. 2012. In vivo identification of bipotential adipocyte progenitors recruited by beta3-adrenoceptor activation and high-fat feeding. Cell Metabolism 15 (4):480–91. doi: 10.1016/j.cmet.2012.03.009.
  • Li, S. N., and J. F. Wu. 2020. TGF-beta/SMAD signaling regulation of mesenchymal stem cells in adipocyte commitment. Stem Cell Research & Therapy 11 (1):41. doi: 10.1186/s13287-020-1552-y.
  • Lin, Y.-W., S. W. Park, Y.-L. Lin, F. H. Burton, and L.-N. Wei. 2020. Cellular retinoic acid binding protein 1 protects mice from high-fat diet-induced obesity by decreasing adipocyte hypertrophy. International Journal of Obesity (2005) 44 (2):466–74. doi: 10.1038/s41366-019-0379-z.
  • Lingen, M. W., P. J. Polverini, and N. P. Bouck. 1996. Inhibition of squamous cell carcinoma angiogenesis by direct interaction of retinoic acid with endothelial cells. Laboratory Investigation; a Journal of Technical Methods and Pathology 74 (2):476–83.
  • Liu, J., A. Divoux, J. Sun, J. Zhang, K. Clément, J. N. Glickman, G. K. Sukhova, P. J. Wolters, J. Du, C. Z. Gorgun, et al. 2009. Genetic deficiency and pharmacological stabilization of mast cells reduce diet-induced obesity and diabetes in mice. Nature Medicine 15 (8):940–5. doi: 10.1038/nm.1994.
  • Liu, L., C. Liang, X. Wang, X. Ding, Y. Lu, J. Dong, M. Han, H. Yang, M. Gao, J. Liao, et al. 2019. Surgical fat removal exacerbates metabolic disorders but not atherogenesis in LDLR−/− mice fed on high-fat diet. Scientific Reports 9 (1):1–10. doi: 10.1038/s41598-019-54392-8.
  • Liu, R., X. Xiong, D. Nam, V. Yechoor, and K. Ma. 2020. SRF-MRTF signaling suppresses brown adipocyte development by modulating TGF-beta/BMP pathway. Molecular and Cellular Endocrinology 515:110920. doi: 10.1016/j.mce.2020.110920.
  • Lu, X., Y. Ji, L. Zhang, Y. Zhang, S. Zhang, Y. An, P. Liu, and Y. Zheng. 2012. Resistance to obesity by repression of VEGF gene expression through induction of brown-like adipocyte differentiation. Endocrinology 153 (7):3123–32. doi: 10.1210/en.2012-1151.
  • Luo, L., and M. Liu. 2016. Adipose tissue in control of metabolism. The Journal of Endocrinology 231 (3):R77–R99. doi: 10.1530/JOE-16-0211.
  • Ma, Y. N., B. Wang, Z. X. Wang, N. A. Gomez, M. J. Zhu, and M. Du. 2018. Three-dimensional spheroid culture of adipose stromal vascular cells for studying adipogenesis in beef cattle. Animal 12 (10):2123–9. doi: 10.1017/S1751731118000150.
  • MacDougald, O. A., and S. Mandrup. 2002. Adipogenesis: Forces that tip the scales. Trends in Endocrinology and Metabolism: TEM 13 (1):5–11. doi: 10.1016/s1043-2760(01)00517-3.
  • Maquoi, E., C. Munaut, A. Colige, D. Collen, and H. R. Lijnen. 2002. Modulation of adipose tissue expression of murine matrix metalloproteinases and their tissue inhibitors with obesity. Diabetes 51 (4):1093–101. doi: 10.2337/diabetes.51.4.1093.
  • Marlatt, K. L., K. Y. Chen, and E. Ravussin. 2018. Is activation of human brown adipose tissue a viable target for weight management? American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 315 (3):R479–R483. doi: 10.1152/ajpregu.00443.2017.
  • Martinez, F. O., and S. Gordon. 2014. The M1 and M2 paradigm of macrophage activation: Time for reassessment. F1000prime Reports 6:13. doi: 10.12703/P6-13.
  • McCollum, E. V., and M. Davis. 1913. The necessity of certain lipins in the diet during growth. Journal of Biological Chemistry 15 (1):167–75. doi: 10.1016/S0021-9258(18)88553-2.
  • McGlashon, J. M., M. C. Gorecki, A. E. Kozlowski, C. K. Thirnbeck, K. R. Markan, K. L. Leslie, M. E. Kotas, M. J. Potthoff, G. B. Richerson, M. P. Gillum, et al. 2015. Central serotonergic neurons activate and recruit thermogenic brown and beige fat and regulate glucose and lipid homeostasis. Cell Metabolism 21 (5):692–705. doi: 10.1016/j.cmet.2015.04.008.
  • Mills, J. P., H. C. Furr, and S. A. Tanumihardjo. 2008. Retinol to retinol-binding protein (RBP) is low in obese adults due to elevated apo-RBP. Experimental Biology and Medicine (Maywood, N.J.) 233 (10):1255–61. doi: 10.3181/0803-RM-94.
  • Min, S. Y., J. Kady, M. Nam, R. Rojas-Rodriguez, A. Berkenwald, J. H. Kim, H.-L. Noh, J. K. Kim, M. P. Cooper, T. Fitzgibbons, et al. 2016. Human ‘brite/beige’ adipocytes develop from capillary networks, and their implantation improves metabolic homeostasis in mice. Nature Medicine 22 (3):312–8. doi: 10.1038/nm.4031.
  • Morrison, S. F., C. J. Madden, and D. Tupone. 2012. Central control of brown adipose tissue thermogenesis. Frontiers in Endocrinology 3:5. doi: 10.3389/fendo.2012.00005.
  • Morrison, S. F., C. J. Madden, and D. Tupone. 2014. Central neural regulation of brown adipose tissue thermogenesis and energy expenditure. Cell Metabolism 19 (5):741–56. doi: 10.1016/j.cmet.2014.02.007.
  • Muller, S., I. Ader, J. Creff, H. Leménager, P. Achard, L. Casteilla, L. Sensebé, A. Carrière, and F. Deschaseaux. 2019. Human adipose stromal-vascular fraction self-organizes to form vascularized adipose tissue in 3D cultures. Scientific Reports 9 (1):7250. doi: 10.1038/s41598-019-43624-6.
  • Murholm, M., M. S. Isidor, A. L. Basse, S. Winther, C. Sørensen, J. Skovgaard-Petersen, M. M. Nielsen, A. S. Hansen, B. Quistorff, J. B. Hansen, et al. 2013. Retinoic acid has different effects on UCP1 expression in mouse and human adipocytes. BMC Cell Biology 14 (1):1–13. doi: 10.1186/1471-2121-14-41.
  • Nakamura, K., and S. F. Morrison. 2011. Central efferent pathways for cold-defensive and febrile shivering. The Journal of Physiology 589 (Pt 14):3641–58. doi: 10.1113/jphysiol.2011.210047.
  • Napoli, J. L. 1999. Retinoic acid: Its biosynthesis and metabolism. Progress in Nucleic Acid Research and Molecular Biology 63:139–88.
  • Nguyen, H. P., F. Lin, D. Yi, Y. Xie, J. Dinh, P. Xue, and H. S. Sul. 2021. Aging-dependent regulatory cells emerge in subcutaneous fat to inhibit adipogenesis. Developmental Cell 56 (10):1437–51 e3. doi: 10.1016/j.devcel.2021.03.026.
  • Niederreither, K., P. McCaffery, U. C. Dräger, P. Chambon, and P. Dollé. 1997. Restricted expression and retinoic acid-induced downregulation of the retinaldehyde dehydrogenase type 2 (RALDH-2) gene during mouse development. Mechanisms of Development 62 (1):67–78. doi: 10.1016/s0925-4773(96)00653-3.
  • Norseen, J., T. Hosooka, A. Hammarstedt, M. M. Yore, S. Kant, P. Aryal, U. A. Kiernan, D. A. Phillips, H. Maruyama, B. J. Kraus, et al. 2012. Retinol-binding protein 4 inhibits insulin signaling in adipocytes by inducing proinflammatory cytokines in macrophages through a c-Jun N-terminal kinase- and toll-like receptor 4-dependent and retinol-independent mechanism. Molecular and Cellular Biology 32 (10):2010–9. doi: 10.1128/MCB.06193-11.
  • Noy, N. 2013. The one-two punch: Retinoic acid suppresses obesity both by promoting energy expenditure and by inhibiting adipogenesis. Adipocyte 2 (3):184–7. doi: 10.4161/adip.23489.
  • Nuss, E. T., A. R. Valentine, Z. Zhang, H. J. Lai, and S. A. Tanumihardjo. 2017. Serum carotenoid interactions in premenopausal women reveal α-carotene is negatively impacted by body fat. Experimental Biology and Medicine (Maywood, N.J.) 242 (12):1262–70. doi: 10.1177/1535370217706962.
  • Ohno, H., K. Shinoda, K. Ohyama, L. Z. Sharp, and S. Kajimura. 2013. EHMT1 controls brown adipose cell fate and thermogenesis through the PRDM16 complex. Nature 504 (7478):163–7. doi: 10.1038/nature12652.
  • Ottaviani, E., D. Malagoli, and C. Franceschi. 2011. The evolution of the adipose tissue: A neglected enigma. General and Comparative Endocrinology 174 (1):1–4. doi: 10.1016/j.ygcen.2011.06.018.
  • Ouellet, V., S. M. Labbé, D. P. Blondin, S. Phoenix, B. Guérin, F. Haman, E. E. Turcotte, D. Richard, and A. C. Carpentier. 2012. Brown adipose tissue oxidative metabolism contributes to energy expenditure during acute cold exposure in humans. The Journal of Clinical Investigation 122 (2):545–52. doi: 10.1172/JCI60433.
  • Park, I. R., and J. Himms-Hagen. 1988. Neural influences on trophic changes in brown adipose tissue during cold acclimation. The American Journal of Physiology 255 (6 Pt 2):R874–81. doi: 10.1152/ajpregu.1988.255.6.R874.
  • Park, J., M. Kim, K. Sun, Y. A. An, X. Gu, and P. E. Scherer. 2017. VEGF-A–expressing adipose tissue shows rapid beiging and enhanced survival after transplantation and confers IL-4–independent metabolic improvements. Diabetes 66 (6):1479–90. doi: 10.2337/db16-1081.
  • Pereira, S. E., C. J. Saboya, C. Saunders, and A. Ramalho. 2012. Serum levels and liver store of retinol and their association with night blindness in individuals with class III obesity. Obesity Surgery 22 (4):602–8. doi: 10.1007/s11695-011-0522-y.
  • Puigserver, P., Z. Wu, C. W. Park, R. Graves, M. Wright, and B. M. Spiegelman. 1998. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92 (6):829–39. doi: 10.1016/s0092-8674(00)81410-5.
  • Qi, Q., Z. Yu, X. Ye, F. Zhao, P. Huang, F. B. Hu, O. H. Franco, J. Wang, H. Li, Y. Liu, et al. 2007. Elevated retinol-binding protein 4 levels are associated with metabolic syndrome in Chinese people. The Journal of Clinical Endocrinology and Metabolism 92 (12):4827–34. doi: 10.1210/jc.2007-1219.
  • Quach, J. M., E. C. Walker, E. Allan, M. Solano, A. Yokoyama, S. Kato, N. A. Sims, M. T. Gillespie, and T. J. Martin. 2011. Zinc finger protein 467 is a novel regulator of osteoblast and adipocyte commitment. The Journal of Biological Chemistry 286 (6):4186–98. doi: 10.1074/jbc.M110.178251.
  • Quadro, L., W. S. Blaner, D. J. Salchow, S. Vogel, R. Piantedosi, P. Gouras, S. Freeman, M. P. Cosma, V. Colantuoni, M. E. Gottesman, et al. 1999. Impaired retinal function and vitamin A availability in mice lacking retinol-binding protein. The EMBO Journal 18 (17):4633–44. doi: 10.1093/emboj/18.17.4633.
  • Rajakumari, S., J. Wu, J. Ishibashi, H.-W. Lim, A.-H. Giang, K.-J. Won, R. R. Reed, and P. Seale. 2013. EBF2 determines and maintains brown adipocyte identity. Cell Metabolism 17 (4):562–74. doi: 10.1016/j.cmet.2013.01.015.
  • Rennert, R. C., M. Sorkin, M. Januszyk, D. Duscher, R. Kosaraju, M. T. Chung, J. Lennon, A. Radiya-Dixit, S. Raghvendra, Z. N. Maan, et al. 2014. Diabetes impairs the angiogenic potential of adipose-derived stem cells by selectively depleting cellular subpopulations. Stem Cell Research & Therapy 5 (3):79. doi: 10.1186/scrt468.
  • Rhinn, M., and P. Dollé. 2012. Retinoic acid signalling during development. Development (Cambridge, England) 139 (5):843–58. doi: 10.1242/dev.065938.
  • Ribamar, A., S. Cruz, C. Bento, and A. Ramalho. 2022. Visceral and body adiposity are negatively associated with vitamin A nutritional status independently of Body Mass Index and recommended intake of vitamin A in Brazilian Women. The Journal of Nutritional Biochemistry 109:109120. doi: 10.1016/j.jnutbio.2022.109120.
  • Ritchie, H. E., W. S. Webster, C. Eckhoff, and D. J. Oakes. 1998. Model predicting the teratogenic potential of retinyl palmitate, using a combined in vivo/in vitro approach. Teratology 58 (3-4):113–23. doi: 10.1002/(SICI)1096-9926(199809/10)58:3/4<113::AID-TERA7>3.0.CO;2-O.
  • Rosen, E. D., and B. M. Spiegelman. 2000. Molecular regulation of adipogenesis. Annual Review of Cell and Developmental Biology 16:145–71. doi: 10.1146/annurev.cellbio.16.1.145.
  • Rosen, E. D., and B. M. Spiegelman. 2014. What we talk about when we talk about fat. Cell 156 (1-2):20–44. doi: 10.1016/j.cell.2013.12.012.
  • Rosen, E. D., and O. A. MacDougald. 2006. Adipocyte differentiation from the inside out. Nature Reviews. Molecular Cell Biology 7 (12):885–96. doi: 10.1038/nrm2066.
  • Rosenwald, M., A. Perdikari, T. Rülicke, and C. Wolfrum. 2013. Bi-directional interconversion of brite and white adipocytes. Nature Cell Biology 15 (6):659–67. doi: 10.1038/ncb2740.
  • Said, E., S. Mousa, M. Fawzi, N. A. Sabry, and S. Farid. 2021. Combined effect of high-dose vitamin A, vitamin E supplementation, and zinc on adult patients with diabetes: A randomized trial. Journal of Advanced Research 28:27–33. doi: 10.1016/j.jare.2020.06.013.
  • Saito, A., A. Sugawara, A. Uruno, M. Kudo, H. Kagechika, Y. Sato, Y. Owada, H. Kondo, M. Sato, M. Kurabayashi, et al. 2007. All-trans retinoic acid induces in vitro angiogenesis via retinoic acid receptor: Possible involvement of paracrine effects of endogenous vascular endothelial growth factor signaling. Endocrinology 148 (3):1412–23. doi: 10.1210/en.2006-0900.
  • Sandell, L. L., B. W. Sanderson, G. Moiseyev, T. Johnson, A. Mushegian, K. Young, J.-P. Rey, J-x Ma, K. Staehling-Hampton, P. A. Trainor, et al. 2007. RDH10 is essential for synthesis of embryonic retinoic acid and is required for limb, craniofacial, and organ development. Genes & Development 21 (9):1113–24. doi: 10.1101/gad.1533407.
  • Schug, T. T., D. C. Berry, N. S. Shaw, S. N. Travis, and N. Noy. 2007. Opposing effects of retinoic acid on cell growth result from alternate activation of two different nuclear receptors. Cell 129 (4):723–33. doi: 10.1016/j.cell.2007.02.050.
  • Schulz, T. J., T. L. Huang, T. T. Tran, H. Zhang, K. L. Townsend, J. L. Shadrach, M. Cerletti, L. E. McDougall, N. Giorgadze, T. Tchkonia, et al. 2011. Identification of inducible brown adipocyte progenitors residing in skeletal muscle and white fat. Proceedings of the National Academy of Sciences of the United States of America 108 (1):143–8. doi: 10.1073/pnas.1010929108.
  • Schwarz, E. J., M. J. Reginato, D. Shao, S. L. Krakow, and M. A. Lazar. 1997. Retinoic acid blocks adipogenesis by inhibiting C/EBPbeta-mediated transcription. Molecular and Cellular Biology 17 (3):1552–61. doi: 10.1128/MCB.17.3.1552.
  • Seale, P., B. Bjork, W. Yang, S. Kajimura, S. Chin, S. Kuang, A. Scimè, S. Devarakonda, H. M. Conroe, H. Erdjument-Bromage, et al. 2008. PRDM16 controls a brown fat/skeletal muscle switch. Nature 454 (7207):961–7. doi: 10.1038/nature07182.
  • Seale, P., H. M. Conroe, J. Estall, S. Kajimura, A. Frontini, J. Ishibashi, P. Cohen, S. Cinti, and B. M. Spiegelman. 2011. Prdm16 determines the thermogenic program of subcutaneous white adipose tissue in mice. The Journal of Clinical Investigation 121 (1):96–105. doi: 10.1172/JCI44271.
  • Seki, T., K. Hosaka, S. Lim, C. Fischer, J. Honek, Y. Yang, P. Andersson, M. Nakamura, E. Näslund, S. Ylä-Herttuala, et al. 2016. Endothelial PDGF-CC regulates angiogenesis-dependent thermogenesis in beige fat. Nature Communications 7:12152. doi: 10.1038/ncomms12152.
  • Seo, J. B., H. M. Moon, W. S. Kim, Y. S. Lee, H. W. Jeong, E. J. Yoo, J. Ham, H. Kang, M.-G. Park, K. R. Steffensen, et al. 2004. Activated liver X receptors stimulate adipocyte differentiation through induction of peroxisome proliferator-activated receptor gamma expression. Molecular and Cellular Biology 24 (8):3430–44. doi: 10.1128/MCB.24.8.3430-3444.2004.
  • Shao, M., J. Ishibashi, C. M. Kusminski, Q. A. Wang, C. Hepler, L. Vishvanath, K. A. MacPherson, S. B. Spurgin, K. Sun, W. L. Holland, et al. 2016. Zfp423 maintains white adipocyte identity through suppression of the beige cell thermogenic gene program. Cell Metabolism 23 (6):1167–84. doi: 10.1016/j.cmet.2016.04.023.
  • Shao, M., L. Vishvanath, N. C. Busbuso, C. Hepler, B. Shan, A. X. Sharma, S. Chen, X. Yu, Y. A. An, Y. Zhu, et al. 2018. De novo adipocyte differentiation from Pdgfrbeta(+) preadipocytes protects against pathologic visceral adipose expansion in obesity. Nature Communications 9 (1):890. doi: 10.1038/s41467-018-03196-x.
  • Shi, H., A. D. Strader, S. C. Woods, and R. J. Seeley. 2007. The effect of fat removal on glucose tolerance is depot specific in male and female mice. American Journal of Physiology. Endocrinology and Metabolism 293 (4):E1012–E1020. doi: 10.1152/ajpendo.00649.2006.
  • Sidossis, L., and S. Kajimura. 2015. Brown and beige fat in humans: Thermogenic adipocytes that control energy and glucose homeostasis. The Journal of Clinical Investigation 125 (2):478–86. doi: 10.1172/JCI78362.
  • Singh, A. M., L. Zhang, J. Avery, A. Yin, Y. Du, H. Wang, Z. Li, H. Fu, H. Yin, S. Dalton, et al. 2020. Human beige adipocytes for drug discovery and cell therapy in metabolic diseases. Nature Communications 11 (1):2758. doi: 10.1038/s41467-020-16340-3.
  • Smith, S. B., H. Kawachi, C. B. Choi, C. W. Choi, G. Wu, and J. E. Sawyer. 2009. Cellular regulation of bovine intramuscular adipose tissue development and composition. Journal of Animal Science 87 (14 Suppl):E72–82. doi: 10.2527/jas.2008-1340.
  • Spalding, K. L., E. Arner, P. O. Westermark, S. Bernard, B. A. Buchholz, O. Bergmann, L. Blomqvist, J. Hoffstedt, E. Näslund, T. Britton, et al. 2008. Dynamics of fat cell turnover in humans. Nature 453 (7196):783–7. doi: 10.1038/nature06902.
  • Spiegelman, B. M., and J. S. Flier. 1996. Adipogenesis and obesity: Rounding out the big picture. Cell 87 (3):377–89. doi: 10.1016/s0092-8674(00)81359-8.
  • Stenkula, K. G., and C. Erlanson-Albertsson. 2018. Adipose cell size: Importance in health and disease. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 315 (2):R284–R295. doi: 10.1152/ajpregu.00257.2017.
  • Strinić, I., N. Habek, and A. Dugandžić. 2021. Guanylin peptides signaling: Insights into guanylate cyclase C dependent and independent signaling pathways.
  • Strissel, K. J., Z. Stancheva, H. Miyoshi, J. W. Perfield, J. DeFuria, Z. Jick, A. S. Greenberg, and M. S. Obin. 2007. Adipocyte death, adipose tissue remodeling, and obesity complications. Diabetes 56 (12):2910–8. doi: 10.2337/db07-0767.
  • Sun, K., and P. E. Scherer. 2010. Adipose tissue dysfunction: A multistep process. In Christen, Y., Clément, K., Spiegelman, B. (eds) Novel insights into adipose cell functions. Research and Perspectives in Endocrine Interactions. Berlin, Heidelberg: Springer.
  • Sun, K., C. M. Kusminski, and P. E. Scherer. 2011. Adipose tissue remodeling and obesity. The Journal of Clinical Investigation 121 (6):2094–101. doi: 10.1172/JCI45887.
  • Sun, K., I. Wernstedt Asterholm, C. M. Kusminski, A. C. Bueno, Z. V. Wang, J. W. Pollard, R. A. Brekken, and P. E. Scherer. 2012. Dichotomous effects of VEGF-A on adipose tissue dysfunction. Proceedings of the National Academy of Sciences of the United States of America 109 (15):5874–9. doi: 10.1073/pnas.1200447109.
  • Sung, H.-K., K.-O. Doh, J. E. Son, J. G. Park, Y. Bae, S. Choi, S. M. L. Nelson, R. Cowling, K. Nagy, I. P. Michael, et al. 2013. Adipose vascular endothelial growth factor regulates metabolic homeostasis through angiogenesis. Cell Metabolism 17 (1):61–72. doi: 10.1016/j.cmet.2012.12.010.
  • Tan, N.-S., N. S. Shaw, N. Vinckenbosch, P. Liu, R. Yasmin, B. Desvergne, W. Wahli, and N. Noy. 2002. Selective cooperation between fatty acid binding proteins and peroxisome proliferator-activated receptors in regulating transcription. Molecular and Cellular Biology 22 (14):5114–27. doi: 10.1128/MCB.22.14.5114-5127.2002.
  • Tang, W., D. Zeve, J. M. Suh, D. Bosnakovski, M. Kyba, R. E. Hammer, M. D. Tallquist, and J. M. Graff. 2008. White fat progenitor cells reside in the adipose vasculature. Science (New York, N.Y.) 322 (5901):583–6. doi: 10.1126/science.1156232.
  • Taylor, E. B. 2021. The complex role of adipokines in obesity, inflammation, and autoimmunity. Clinical Science (London, England : 1979) 135 (6):731–52. doi: 10.1042/CS20200895.
  • Tran, K.-V., O. Gealekman, A. Frontini, M. C. Zingaretti, M. Morroni, A. Giordano, A. Smorlesi, J. Perugini, R. De Matteis, A. Sbarbati, et al. 2012. The vascular endothelium of the adipose tissue gives rise to both white and brown fat cells. Cell Metabolism 15 (2):222–9. doi: 10.1016/j.cmet.2012.01.008.
  • Tseng, Y.-H., E. Kokkotou, T. J. Schulz, T. L. Huang, J. N. Winnay, C. M. Taniguchi, T. T. Tran, R. Suzuki, D. O. Espinoza, Y. Yamamoto, et al. 2008. New role of bone morphogenetic protein 7 in brown adipogenesis and energy expenditure. Nature 454 (7207):1000–4. doi: 10.1038/nature07221.
  • Tsutsumi, C., M. Okuno, L. Tannous, R. Piantedosi, M. Allan, D. S. Goodman, and W. S. Blaner. 1992. Retinoids and retinoid-binding protein expression in rat adipocytes. The Journal of Biological Chemistry 267 (3):1805–10. doi: 10.1016/S0021-9258(18)46017-6.
  • U.S. Department of Agriculture, A.R.S. n.d. What We Eat in America, 2007-2008. https://www.ars.usda.gov/northeast-area/beltsville-md/beltsville-human-nutrition-research-center/food-surveys-research-group/docs/wweia-data-tables/.
  • van der Lans, A. A. J. J., J. Hoeks, B. Brans, G. H. E. J. Vijgen, M. G. W. Visser, M. J. Vosselman, J. Hansen, J. A. Jörgensen, J. Wu, F. M. Mottaghy, et al. 2013. Cold acclimation recruits human brown fat and increases nonshivering thermogenesis. The Journal of Clinical Investigation 123 (8):3395–403. doi: 10.1172/JCI68993.
  • Vidal-Puig, A. 2013. Adipose tissue expandability, lipotoxicity and the metabolic syndrome. Endocrinologia y Nutricion : Organo de la Sociedad Espanola de Endocrinologia y Nutricion 60 (Suppl 1):39–43. doi: 10.1016/s1575-0922(13)70026-3.
  • Virtanen, K. A., M. E. Lidell, J. Orava, M. Heglind, R. Westergren, T. Niemi, M. Taittonen, J. Laine, N.-J. Savisto, S. Enerbäck, et al. 2009. Functional brown adipose tissue in healthy adults. The New England Journal of Medicine 360 (15):1518–25. doi: 10.1056/NEJMoa0808949.
  • Vishvanath, L., and R. K. Gupta. 2019. Contribution of adipogenesis to healthy adipose tissue expansion in obesity. The Journal of Clinical Investigation 129 (10):4022–31. doi: 10.1172/JCI129191.
  • Vishvanath, L., J. Z. Long, B. M. Spiegelman, and R. K. Gupta. 2017. Do adipocytes emerge from mural progenitors? Cell Stem Cell 20 (5):585–6. doi: 10.1016/j.stem.2017.03.013.
  • Vishvanath, L., K. A. MacPherson, C. Hepler, Q. A. Wang, M. Shao, S. B. Spurgin, M. Y. Wang, C. M. Kusminski, T. S. Morley, R. K. Gupta, et al. 2016. Pdgfrbeta + mural preadipocytes contribute to adipocyte hyperplasia induced by high-fat-diet feeding and prolonged cold exposure in adult mice. Cell Metabolism 23 (2):350–9. doi: 10.1016/j.cmet.2015.10.018.
  • Vitkova, M., E. Klimcakova, M. Kovacikova, C. Valle, C. Moro, J. Polak, J. Hanacek, F. Capel, N. Viguerie, B. Richterova, et al. 2007. Plasma levels and adipose tissue messenger ribonucleic acid expression of retinol-binding protein 4 are reduced during calorie restriction in obese subjects but are not related to diet-induced changes in insulin sensitivity. The Journal of Clinical Endocrinology and Metabolism 92 (6):2330–5. doi: 10.1210/jc.2006-2668.
  • Vosselman, M. J., A. A. J. J. van der Lans, B. Brans, R. Wierts, M. A. van Baak, P. Schrauwen, and W. D. van Marken Lichtenbelt. 2012. Systemic β-adrenergic stimulation of thermogenesis is not accompanied by brown adipose tissue activity in humans. Diabetes 61 (12):3106–13. doi: 10.2337/db12-0288.
  • Wadey, R. M., K. D. Connolly, D. Mathew, G. Walters, D. A. Rees, and P. E. James. 2019. Inflammatory adipocyte-derived extracellular vesicles promote leukocyte attachment to vascular endothelial cells. p. Atherosclerosis 283:19–27. doi: 10.1016/j.atherosclerosis.2019.01.013.
  • Wang, B., E. E. Tsakiridis, S. Zhang, A. Llanos, E. M. Desjardins, J. M. Yabut, A. E. Green, E. A. Day, B. K. Smith, J. S. V. Lally, et al. 2021. The pesticide chlorpyrifos promotes obesity by inhibiting diet-induced thermogenesis in brown adipose tissue. Nature Communications 12 (1):5163. doi: 10.1038/s41467-021-25384-y.
  • Wang, B., X. Fu, M.-J. Zhu, and M. Du. 2017. Retinoic acid inhibits white adipogenesis by disrupting GADD45A-mediated Zfp423 DNA demethylation. Journal of Molecular Cell Biology 9 (4):338–49. doi: 10.1093/jmcb/mjx026.
  • Wang, B., X. Fu, X. Liang, J. M. Deavila, Z. Wang, L. Zhao, Q. Tian, J. Zhao, N. A. Gomez, S. C. Trombetta, et al. 2017. Retinoic acid ­induces white adipose tissue browning by increasing adipose vascularity and inducing beige adipogenesis of PDGFRalpha(+) adipose progenitors. Cell Discovery 3:17036. doi: 10.1038/celldisc.2017.36.
  • Wang, B., X. Fu, X. Liang, Z. Wang, Q. Yang, T. Zou, W. Nie, J. Zhao, P. Gao, M.-J. Zhu, et al. 2017. Maternal retinoids increase PDGFRalpha(+) progenitor population and beige adipogenesis in progeny by stimulating vascular development. EBioMedicine 18:288–99. doi: 10.1016/j.ebiom.2017.03.041.
  • Wang, E. A., D. I. Israel, S. Kelly, and D. P. Luxenberg. 1993. Bone morphogenetic protein-2 causes commitment and differentiation in C3H10T1/2 and 3T3 cells. Growth Factors (Chur, Switzerland) 9 (1):57–71. doi: 10.3109/08977199308991582.
  • Wang, F., S. E. Mullican, J. R. DiSpirito, L. C. Peed, and M. A. Lazar. 2013. Lipoatrophy and severe metabolic disturbance in mice with fat-specific deletion of PPARgamma. Proceedings of the National Academy of Sciences of the United States of America 110 (46):18656–61. doi: 10.1073/pnas.1314863110.
  • Wang, Q. A., C. Tao, R. K. Gupta, and P. E. Scherer. 2013. Tracking adipogenesis during white adipose tissue development, expansion and regeneration. Nature Medicine 19 (10):1338–44. doi: 10.1038/nm.3324.
  • Wang, S., X. Liang, Q. Yang, X. Fu, C. J. Rogers, M. Zhu, B. D. Rodgers, Q. Jiang, M. V. Dodson, M. Du, et al. 2015. Resveratrol induces brown-like adipocyte formation in white fat through activation of AMP-activated protein kinase (AMPK) alpha1. International Journal of Obesity (2005) 39 (6):967–76. doi: 10.1038/ijo.2015.23.
  • Wang, W., and P. Seale. 2016. Control of brown and beige fat development. Nature Reviews. Molecular Cell Biology 17 (11):691–702. doi: 10.1038/nrm.2016.96.
  • Weisberg, S. P., D. McCann, M. Desai, M. Rosenbaum, R. L. Leibel, and A. W. Ferrante. 2003. Obesity is associated with macrophage accumulation in adipose tissue. Journal of Clinical Investigation 112 (12):1796–808. doi: 10.1172/JCI200319246.
  • Westerterp, K. R. 2004. Diet induced thermogenesis. Nutrition & Metabolism 1 (1):5. doi: 10.1186/1743-7075-1-5.
  • White, H. M., A. J. Acton, and R. V. Considine. 2012. The angiogenic inhibitor TNP-470 decreases caloric intake and weight gain in high-fat fed mice. Obesity (Silver Spring, Md.) 20 (10):2003–9. doi: 10.1038/oby.2012.87.
  • WHO. 1998. Safe vitamin A dosage during pregnancy and lactation: Recommendations and report of a consultation. World Health Organization.
  • WHO. 2009. Global prevalence of vitamin A deficiency in population at risk: 1995-2005. http://www.who.int/vmnis/database/vitamina/x/en/.
  • Wu, J., J. M. Hansen, L. Hao, R. N. Taylor, and N. Sidell. 2011. Retinoic acid stimulation of VEGF secretion from human endometrial stromal cells is mediated by production of reactive oxygen species. The Journal of Physiology 589 (Pt 4):863–75. doi: 10.1113/jphysiol.2010.200808.
  • Wu, J., P. Boström, L. M. Sparks, L. Ye, J. H. Choi, A.-H. Giang, M. Khandekar, K. A. Virtanen, P. Nuutila, G. Schaart, et al. 2012. Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell 150 (2):366–76. doi: 10.1016/j.cell.2012.05.016.
  • Wu, J., P. Cohen, and B. M. Spiegelman. 2013. Adaptive thermogenesis in adipocytes: Is beige the new brown? Genes & Development 27 (3):234–50. doi: 10.1101/gad.211649.112.
  • Xu, H., G. T. Barnes, Q. Yang, G. Tan, D. Yang, C. J. Chou, J. Sole, A. Nichols, J. S. Ross, L. A. Tartaglia, et al. 2003. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. Journal of Clinical Investigation 112 (12):1821–30. doi: 10.1172/JCI200319451.
  • Xu, Y.-X., B. Wang, J.-N. Jing, R. Ma, Y.-H. Luo, X. Li, Z. Yan, Y.-J. Liu, L. Gao, Y.-L. Ren, et al. 2023. Whole-body adipose tissue multi-omic analyses in sheep reveal molecular mechanisms underlying local adaptation to extreme environments. Communications Biology 6 (1):159. doi: 10.1038/s42003-023-04523-9.
  • Xue, R., Y. Wan, S. Zhang, Q. Zhang, H. Ye, and Y. Li. 2014. Role of bone morphogenetic protein 4 in the differentiation of brown fat-like adipocytes. American Journal of Physiology. Endocrinology and Metabolism 306 (4):E363–72. doi: 10.1152/ajpendo.00119.2013.
  • Xue, Y., N. Petrovic, R. Cao, O. Larsson, S. Lim, S. Chen, H. M. Feldmann, Z. Liang, Z. Zhu, J. Nedergaard, et al. 2009. Hypoxia-independent angiogenesis in adipose tissues during cold acclimation. Cell Metabolism 9 (1):99–109. doi: 10.1016/j.cmet.2008.11.009.
  • Yang, D., M. G. Vuckovic, C. P. Smullin, M. Kim, C. P.-S. Lo, E. Devericks, H. S. Yoo, M. Tintcheva, Y. Deng, J. L. Napoli, et al. 2018. Modest decreases in endogenous all-trans-retinoic acid produced by a mouse Rdh10 heterozygote provoke major abnormalities in adipogenesis and lipid metabolism. Diabetes 67 (4):662–73. doi: 10.2337/db17-0946.
  • Yang, Q., T. E. Graham, N. Mody, F. Preitner, O. D. Peroni, J. M. Zabolotny, K. Kotani, L. Quadro, and B. B. Kahn. 2005. Serum retinol binding protein 4 contributes to insulin resistance in obesity and type 2 diabetes. Nature 436 (7049):356–62. doi: 10.1038/nature03711.
  • Yang, Q., X. Liang, X. Sun, L. Zhang, X. Fu, C. J. Rogers, A. Berim, S. Zhang, S. Wang, B. Wang, et al. 2016. AMPK/alpha-ketoglutarate axis dynamically mediates DNA demethylation in the prdm16 promoter and brown adipogenesis. Cell Metabolism 24 (4):542–54. doi: 10.1016/j.cmet.2016.08.010.
  • Yasmeen, R., B. Reichert, J. Deiuliis, F. Yang, A. Lynch, J. Meyers, M. Sharlach, S. Shin, K. S. Volz, K. B. Green, et al. 2013. Autocrine function of aldehyde dehydrogenase 1 as a determinant of diet- and sex-specific differences in visceral adiposity. Diabetes 62 (1):124–36. doi: 10.2337/db11-1779.
  • Yu, X., Y. Ma, Y. Luo, G. Tang, Z. Jiang, J. Zhang, B. Ye, Z. Huang, Y. Luo, M. Du, et al. 2022. Neonatal vitamin A administration increases intramuscular fat by promoting angiogenesis and preadipocyte formation. Meat Science 191:108847. doi: 10.1016/j.meatsci.2022.108847.
  • Yun, E. J., W. Lorizio, G. Seedorf, S. H. Abman, and T. H. Vu. 2016. VEGF and endothelium-derived retinoic acid regulate lung vascular and alveolar development. American Journal of Physiology. Lung Cellular and Molecular Physiology 310 (4):L287–98. doi: 10.1152/ajplung.00229.2015.
  • Zachara, M., P. Y. Rainer, H. Hashimi, J. M. Russeil, D. Alpern, R. Ferrero, M. Litovchenko, and B. Deplancke. 2022. Mammalian adipogenesis regulator (Areg) cells use retinoic acid signalling to be non‐and anti‐adipogenic in age‐dependent manner. The EMBO Journal 41 (18):e108206. p. doi: 10.15252/embj.2021108206.
  • Zhao, S., C. M. Kusminski, and P. E. Scherer. 2021. Adiponectin, leptin and cardiovascular disorders. Circulation Research 128 (1):136–49. doi: 10.1161/CIRCRESAHA.120.314458.
  • Ziouzenkova, O., G. Orasanu, M. Sharlach, T. E. Akiyama, J. P. Berger, J. Viereck, J. A. Hamilton, G. Tang, G. G. Dolnikowski, S. Vogel, et al. 2007. Retinaldehyde represses adipogenesis and diet-induced obesity. Nature Medicine 13 (6):695–702. doi: 10.1038/nm1587.
  • Zizola, C. F., S. K. Frey, S. Jitngarmkusol, B. Kadereit, N. Yan, and S. Vogel. 2010. Cellular retinol-binding protein type I (CRBP-I) regulates adipogenesis. Molecular and Cellular Biology 30 (14):3412–20. doi: 10.1128/MCB.00014-10.
  • Zou, T., B. Wang, Q. Yang, J. M. de Avila, M.-J. Zhu, J. You, D. Chen, and M. Du. 2018. Raspberry promotes brown and beige adipocyte development in mice fed high-fat diet through activation of AMP-activated protein kinase (AMPK) alpha1. The Journal of Nutritional Biochemistry 55:157–64. doi: 10.1016/j.jnutbio.2018.02.005.
  • Zou, T., D. Chen, Q. Yang, B. Wang, M.-J. Zhu, P. W. Nathanielsz, and M. Du. 2017. Resveratrol supplementation of high-fat diet-fed pregnant mice promotes brown and beige adipocyte development and prevents obesity in male offspring. The Journal of Physiology 595 (5):1547–62. doi: 10.1113/JP273478.
  • Zulet, M. A., B. Puchau, H. H. M. Hermsdorff, C. Navarro, and J. A. Martínez. 2008. Vitamin A intake is inversely related with adiposity in healthy young adults. Journal of Nutritional Science and Vitaminology 54 (5):347–52. doi: 10.3177/jnsv.54.347.

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