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Research Paper

Comparative transcriptomic analysis of rabbit interscapular brown adipose tissue whitening under physiological conditions

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Pages 529-549 | Received 28 Apr 2022, Accepted 04 Aug 2022, Published online: 29 Aug 2022

References

  • Bluher M. Obesity: global epidemiology and pathogenesis. Nat Rev Endocrinol. 2019;15:288–298.
  • Pan X-F, Wang L, Pan A. Epidemiology and determinants of obesity in China. Lancet Diabetes Endocrinol. 2021;9:373–392.
  • Harms M, Seale P. Brown and beige fat: development, function and therapeutic potential. Nat Med. 2013;19:1252–1263.
  • Scheele C, Nielsen S. Metabolic regulation and the anti-obesity perspectives of human brown fat. Redox Biol. 2017;12:770–775.
  • Schrauwen P, van Marken Lichtenbelt WD. Combatting type 2 diabetes by turning up the heat. Diabetologia. 2016;59:2269–2279.
  • Chouchani ET, Kazak L, Spiegelman BM. New advances in adaptive thermogenesis: UCP1 and beyond. Cell Metab. 2019;29:27–37.
  • Lean ME. Brown adipose tissue in humans. Proc Nutr Soc. 1989;48:243–256.
  • Lidell ME. Brown adipose tissue in human infants. Handb Exp Pharmacol. 2019;251:107–123.
  • Basse AL, Dixen K, Yadav R, et al. Global gene expression profiling of brown to white adipose tissue transformation in sheep reveals novel transcriptional components linked to adipose remodeling. BMC Genomics. 2015;16:215.
  • Oelkrug R, Polymeropoulos ET, Jastroch M. Brown adipose tissue: physiological function and evolutionary significance. J Comp Physiol B. 2015;185:587–606.
  • Du K, Bai, X., Yang, L., et al. De Novo Reconstruction of transcriptome identified long non-coding RNA regulator of aging-related brown adipose tissue whitening in rabbits. Biology (Basel). 2021;10:1176.
  • Derry DM, Morrow E, Sadre N, et al. Brown and white fat during the life of the rabbit. Dev Biol. 1972;27:204–216.
  • Cypess AM, Lehman S, Williams G, et al. Identification and importance of brown adipose tissue in adult humans. N Engl J Med. 2009;360:1509–1517.
  • van Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM, et al. Cold-activated brown adipose tissue in healthy men. N Engl J Med. 2009;360:1500–1508.
  • Virtanen KA, Lidell ME, Orava J, et al. Functional brown adipose tissue in healthy adults. N Engl J Med. 2009;360:1518–1525.
  • Yoneshiro T, Aita S, Matsushita M, et al. Recruited brown adipose tissue as an antiobesity agent in humans. J Clin Invest. 2013;123:3404–3408.
  • Yoneshiro T, Aita S, Matsushita M, et al. Age-related decrease in cold-activated brown adipose tissue and accumulation of body fat in healthy humans. Obesity (Silver Spring). 2011;19:1755–1760.
  • Aherne W, Hull D. Brown adipose tissue and heat production in the newborn infant. J Pathol Bacteriol. 1966;91:223–234.
  • Heaton JM. The distribution of brown adipose tissue in the human. J Anat. 1972;112:35–39.
  • Astrup A, Bülow J, Christensen NJ, et al. Ephedrine-induced thermogenesis in man: no role for interscapular brown adipose tissue. Clin Sci (Lond). 1984;66:179–186.
  • Dawkins MJ, Hull D. BROWN ADIPOSE TISSUE AND THE RESPONSE OF NEW-BORN RABBITS TO COLD. J Physiol. 1964;172:216–238.
  • Rogers NH, Landa A, Park S, et al. Aging leads to a programmed loss of brown adipocytes in murine subcutaneous white adipose tissue. Aging Cell. 2012;11:1074–1083.
  • Scambi I, Peroni D, Nodari A, et al. The transcriptional profile of adipose-derived stromal cells (ASC) mirrors the whitening of adipose tissue with age. Eur J Cell Biol. 2022;101:151206.
  • Cypess AM, White AP, Vernochet C, et al. Anatomical localization, gene expression profiling and functional characterization of adult human neck brown fat. Nat Med. 2013;19:635–639.
  • Jespersen NZ, Larsen T, Peijs L, et al. A classical brown adipose tissue mRNA signature partly overlaps with brite in the supraclavicular region of adult humans. Cell Metab. 2013;17:798–805.
  • de Jong JM, Larsson O, Cannon B, et al. A stringent validation of mouse adipose tissue identity markers. Am J Physiol Endocrinol Metab. 2015;308:E1085–1105.
  • Shinoda K, Luijten IHN, Hasegawa Y, et al. Genetic and functional characterization of clonally derived adult human brown adipocytes. Nat Med. 2015;21:389–394.
  • Roh HC, Tsai LTY, Shao M, et al. Warming induces significant reprogramming of beige, but not brown, adipocyte cellular identity. Cell Metab. 2018;27:1121–1137.e1125.
  • Perdikari A, Leparc GG, Balaz M, et al. BATLAS: deconvoluting brown adipose tissue. Cell Rep. 2018;25:784–797.e784.
  • Altshuler-Keylin S, Kajimura S. Mitochondrial homeostasis in adipose tissue remodeling. Sci Signal. 2017;10. DOI:10.1126/scisignal.aai9248
  • Russell SA, Bashaw GJ. Axon guidance pathways and the control of gene expression. Dev Dyn. 2018;247:571–580.
  • Mestas J, Hughes CC. Of mice and not men: differences between mouse and human immunology. J Immunol. 2004;172:2731–2738.
  • Schlein C, Fischer AW, Sass F, et al. Endogenous fatty acid synthesis drives brown adipose tissue involution. Cell Rep. 2021;34:108624.
  • Bonnot E. The interscapular gland. J Anat Physiol. 1908;43:43–58.
  • Sakers A, De Siqueira MK, Seale P, et al. Adipose-tissue plasticity in health and disease. Cell. 2022;185:419–446.
  • Collins S, Daniel KW, Petro AE, et al. Strain-specific response to beta 3-adrenergic receptor agonist treatment of diet-induced obesity in mice. Endocrinology. 1997;138:405–413.
  • Lim S, Honek J, Xue Y, et al. Cold-induced activation of brown adipose tissue and adipose angiogenesis in mice. Nat Protoc. 2012;7:606–615.
  • Feldmann HM, Golozoubova V, Cannon B, et al. UCP1 ablation induces obesity and abolishes diet-induced thermogenesis in mice exempt from thermal stress by living at thermoneutrality. Cell Metab. 2009;9:203–209.
  • Kalinovich AV, de Jong JM, Cannon B, et al. UCP1 in adipose tissues: two steps to full browning. Biochimie. 2017;134:127–137.
  • Bachman ES, Dhillon H, Zhang C-Y, et al. betaAR signaling required for diet-induced thermogenesis and obesity resistance. Science. 2002;297:843–845.
  • Kotzbeck P, Giordano A, Mondini E, et al. Brown adipose tissue whitening leads to brown adipocyte death and adipose tissue inflammation. J Lipid Res. 2018;59:784–794.
  • Shimizu I, Aprahamian T, Kikuchi R, et al. Vascular rarefaction mediates whitening of brown fat in obesity. J Clin Invest. 2014;124:2099–2112.
  • Wei C, Ma X, Su K, et al. ChREBP-β regulates thermogenesis in brown adipose tissue. J Endocrinol. 2020;245:343–356.
  • Cervera C, fernandez-carmona J. Nutrition and the climatic environment. In: Nutrition of the Rabbit. 2nd ed. Wallingford, UK: CABI Publishing. 2010. p. 267–284.
  • Ferraz PFP, Hernández-Julio, Y. F., Ferraz, G. A. E. S., et al. Decision trees for predicting the physiological responses of rabbits. Animals (Basel). 2019;9:994.
  • Huang Z, Zhang Z, Moazzami Z, et al. Brown adipose tissue involution associated with progressive restriction in progenitor competence. Cell Rep. 2022;39:110575.
  • Kim D, Kim, J. H., Kang, Y. H., et al. Suppression of brown adipocyte autophagy improves energy metabolism by regulating mitochondrial turnover. Int J Mol Sci. 2019;20:3520.
  • Ro SH, Jang Y, Bae J, et al. Autophagy in adipocyte browning: emerging drug target for intervention in obesity. Front Physiol. 2019;10:22.
  • Sass F, Schlein C, Jaeckstein MY, et al. TFEB deficiency attenuates mitochondrial degradation upon brown adipose tissue whitening at thermoneutrality. Mol Metab. 2021;47:101173.
  • Deng J, Guo Y, Yuan F, et al. Autophagy inhibition prevents glucocorticoid-increased adiposity via suppressing BAT whitening. Autophagy. 2020;16:451–465.
  • Rangel-Azevedo C, Santana-Oliveira DA, Miranda CS, et al. Progressive brown adipocyte dysfunction: whitening and impaired nonshivering thermogenesis as long-term obesity complications. J Nutr Biochem. 2022;105:109002.
  • Christiaens V, Lijnen HR. Angiogenesis and development of adipose tissue. Mol Cell Endocrinol. 2010;318:2–9.
  • Herold J, Kalucka J. Angiogenesis in adipose tissue: the interplay between adipose and endothelial cells. Front Physiol. 2020;11:624903.
  • Conceição EP, Madden CJ, Morrison SF. Glycinergic inhibition of BAT sympathetic premotor neurons in rostral raphe pallidus. Am J Physiol Regul Integr Comp Physiol. 2017;312:R919–r926.
  • Madden CJ, Santos da Conceicao EP, Morrison SF. Vagal afferent activation decreases brown adipose tissue (BAT) sympathetic nerve activity and BAT thermogenesis. Temperature (Austin). 2017;4:89–96.
  • Cao Y, Wang H, Wang Q, et al. Three-dimensional volume fluorescence-imaging of vascular plasticity in adipose tissues. Mol Metab. 2018;14:71–81.
  • Jiang H, Ding X, Cao Y, et al. Dense intra-adipose sympathetic arborizations are essential for cold-induced beiging of mouse white adipose tissue. Cell Metab. 2017;26:686–692.e683.
  • Eto H, Suga H, Matsumoto D, et al. Characterization of structure and cellular components of aspirated and excised adipose tissue. Plast Reconstr Surg. 2009;124:1087–1097.
  • Rodeheffer MS, Birsoy K, Friedman JM. Identification of white adipocyte progenitor cells in vivo. Cell. 2008;135:240–249.
  • Tang W, Zeve D, Suh JM, et al. White fat progenitor cells reside in the adipose vasculature. Science. 2008;322:583–586.
  • Corvera S. Cellular heterogeneity in adipose tissues. Annu Rev Physiol. 2021;83:257–278.
  • Wang T, Sharma AK, Wolfrum C. Novel insights into adipose tissue heterogeneity. Rev Endocr Metab Disord. 2022;23:5–12.
  • Nodari A, Scambi I, Peroni D, et al. Interferon regulatory factor 7 impairs cellular metabolism in aging adipose-derived stromal cells. J Cell Sci. 2021;134. DOI:10.1242/jcs.256230.
  • Simon AK, Hollander GA, McMichael A. Evolution of the immune system in humans from infancy to old age. Proc Biol Sci. 2015;282:20143085.
  • Skaggs H, Chellman GJ, Collinge M, et al. Comparison of immune system development in nonclinical species and humans: closing information gaps for immunotoxicity testing and human translatability. Reprod Toxicol. 2019;89:178–188.
  • Pan XX, Yao K-L, Yang Y-F, et al. Senescent T cell induces brown adipose tissue “whitening” via secreting IFN-γ. Front Cell Dev Biol. 2021;9:637424.
  • Sárvári AK, Van Hauwaert EL, Markussen LK, et al. Plasticity of epididymal adipose tissue in response to diet-induced obesity at single-nucleus resolution. Cell Metab. 2021;33:437–453.e435.
  • Emont MP, Jacobs C, Essene AL, et al. A single-cell atlas of human and mouse white adipose tissue. Nature. 2022;603:926–933.
  • Sun W, Dong H, Balaz M, et al. snRNA-seq reveals a subpopulation of adipocytes that regulates thermogenesis. Nature. 2020;587:98–102.
  • Song Z, Xiaoli AM, Yang F. Regulation and metabolic significance of de novo lipogenesis in adipose tissues. Nutrients. 2018;10:1383.
  • Park YJ, Han SM, Huh JY, et al. Emerging roles of epigenetic regulation in obesity and metabolic disease. J Biol Chem. 2021;297:101296.
  • Park YJ, Lee S, Lim S, et al. DNMT1 maintains metabolic fitness of adipocytes through acting as an epigenetic safeguard of mitochondrial dynamics. Proc Natl Acad Sci U S A. 2021;118. DOI:10.1073/pnas.2021073118.
  • Cheng C, Zou C, Liang C, et al. Fat-water separation using a region-growing algorithm with self-feeding phasor estimation. Magn Reson Med. 2017;77:2390–2401.
  • Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics. 2011;12:323.
  • Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550.
  • Xie C, Mao X, Huang J, et al. KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res. 2011;39:W316–322.
  • Conesa A, Nueda MJ, Ferrer A, et al. maSigPro: a method to identify significantly differential expression profiles in time-course microarray experiments. Bioinformatics. 2006;22:1096–1102.
  • Ernst J, Bar-Joseph Z. STEM: a tool for the analysis of short time series gene expression data. BMC Bioinformatics. 2006;7:191.