Rat brown adipose tissue thermogenic markers are modulated by estrous cycle phases and short-term fasting.

brown adipose tissue cellular plasticity estrous cycle short-term fasting thermogenic markers

Journal

BioFactors (Oxford, England)
ISSN: 1872-8081
Titre abrégé: Biofactors
Pays: Netherlands
ID NLM: 8807441

Informations de publication

Date de publication:
21 Jul 2023
Historique:
received: 11 04 2023
accepted: 06 07 2023
medline: 24 7 2023
pubmed: 24 7 2023
entrez: 24 7 2023
Statut: aheadofprint

Résumé

Brown adipose tissue (BAT) converts chemical energy into heat to maintain body temperature. Although fatty acids (FAs) represent a primary substrate for uncoupling protein 1 (UCP1)-dependent thermogenesis, BAT also utilizes glucose for the same purpose. Considering that estrous cycle effects on BAT are not greatly explored, we examined those of 6-h fasting on interscapular BAT (iBAT) thermogenic markers in proestrus and diestrus. We found that the percentage of multilocular adipocytes was lower in proestrus than in diestrus, although it was increased after fasting in both analyzed estrous cycle stages. Furthermore, the percentage of paucilocular adipocytes was increased by fasting, unlike the percentage of unilocular cells, which decreased in both analyzed stages of the estrous cycle. The UCP1 amount was lower in proestrus irrespectively of the examined dietary regimens. Regarding FA transporters, it was shown that iBAT CD36 content was increased in fasted rats in diestrus. In contrast to GLUT1, the level of GLUT4 was interactively modulated by selected estrous cycle phases and fasting. There was no change in insulin receptor and ERK1/2 activation, while AKT activation was interactively modulated by fasting and estrous cycle stages. Our study showed that iBAT exhibits morphological and functional changes in proestrus and diestrus. Moreover, iBAT undergoes additional dynamic functional and morphological changes during short-term fasting to modulate nutrient utilization and adjust energy expenditure.

Identifiants

pubmed: 37482913
doi: 10.1002/biof.1993
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Ministry of Science, Technological Development and Innovation of the Republic of Serbia
ID : 451-03-47/2023-01/ 200178

Informations de copyright

© 2023 International Union of Biochemistry and Molecular Biology.

Références

Cannon B, Nedergaard J. Brown adipose tissue: function and physiological significance. Physiol Rev. 2004;84:277-359.
Zhang W, Bi S. Hypothalamic regulation of brown adipose tissue thermogenesis and energy homeostasis. Front Endocrinol (Lausanne). 2015;6:136. https://doi.org/10.3389/fendo.2015.00136
Cao W, Medvedev AV, Daniel KW, Collins S. Beta-adrenergic activation of p38 MAP kinase in adipocytes: cAMP induction of the uncoupling protein 1 (UCP1) gene requires p38 MAP kinase. J Biol Chem. 2001;276:27077-27082.
Zingaretti MC, Crosta F, Vitali A, Guerrieri M, Frontini A, Cannon B, et al. The presence of UCP1 demonstrates that metabolically active adipose tissue in the neck of adult humans truly represents brown adipose tissue. FASEB J. 2009;23:3113-3120.
Ouellet V, Labbé SM, Blondin DP, Phoenix S, Guérin B, Haman F, et al. Brown adipose tissue oxidative metabolism contributes to energy expenditure during acute cold exposure in humans. J Clin Invest. 2012;122:545-552.
Fedorenko A, Lishko PV, Kirichok Y. Mechanism of fatty-acid-dependent UCP1 uncoupling in brown fat mitochondria. Cell. 2012;151:400-413.
Abumrad NA, El-Maghrabi MR, Amri EZ, Lopez E, Grimaldi PA. Cloning of a rat adipocyte membrane protein implicated in binding or transport of long-chain fatty acids that is induced during preadipocyte differentiation. Homology with human CD36. J Biol Chem. 1993;268:17665-17668.
Putri M, Syamsunarno MRAA, Iso T, Yamaguchi A, Hanaoka H, Sunaga H, et al. CD36 is indispensable for thermogenesis under conditions of fasting and cold stress. Biochem Biophys Res Commun. 2015;457:520-525.
Wu Q, Kazantzis M, Doege H, Ortegon AM, Tsang B, Falcon A, et al. Fatty acid transport protein 1 is required for nonshivering thermogenesis in brown adipose tissue. Diabetes. 2006;55:3229-3237.
Shabalina IG, Jacobsson A, Cannon B, Nedergaard J. Native UCP1 displays simple competitive kinetics between the regulators purine nucleotides and fatty acids. J Biol Chem. 2004;279:38236-38248.
Bertholet AM, Kirichok Y. The mechanism FA-dependent H+ transport by UCP1. Handb Exp Pharmacol. 2019;251:143-159. https://doi.org/10.1007/164_2018_138
Shin H, Ma Y, Chanturiya T, Cao Q, Wang Y, Kadegowda AKG, et al. Lipolysis in Brown adipocytes is not essential for cold-induced thermogenesis in mice. Cell Metab. 2017;26:764-777.
Chitraju C, Fischer AW, Farese RV, Walther TC. Lipid droplets in Brown adipose tissue are dispensable for cold-induced thermogenesis. Cell Rep. 2020;33:108348.
Khedoe PPSJ, Hoeke G, Kooijman S, Dijk W, Buijs JT, Kersten S, et al. Brown adipose tissue takes up plasma triglycerides mostly after lipolysis. J Lipid Res. 2015;56:51-59.
Dallner OS, Chernogubova E, Brolinson KA, Bengtsson T. β3-adrenergic receptors stimulate glucose uptake in brown adipocytes by two mechanisms independently of glucose transporter 4 translocation. Endocrinology. 2006;147:5730-5739.
Marette A, Bukowiecki LJ. Stimulation of glucose transport by insulin and norepinephrine in isolated rat brown adipocytes. Am J Physiol. 1989;257:C714-C721.
Bryant NJ, Govers R, James DE. Regulated transport of the glucose transporter GLUT4. Nat Rev Mol Cell Biol. 2002;3:267-277.
García-Casarrubios E, de Moura C, Arroba AI, Pescador N, Calderon-Dominguez M, Garcia L, et al. Rapamycin negatively impacts insulin signaling, glucose uptake and uncoupling protein-1 in brown adipocytes. Biochim Biophys Acta. 2016;1861:1929-1941.
Ma SWY, Foster DO. Uptake of glucose and release of fatty acids and glycerol by rat brown adipose tissue in vivo. Can J Physiol Pharmacol. 1986;64:609-614.
Isler D, Hill HP, Meier MK. Glucose metabolism in isolated brown adipocytes under β-adrenergic stimulation. Quantitative contribution of glucose to total thermogenesis. Biochem J. 1987;245:789-793.
Winther S, Isidor MS, Basse AL, Skjoldborg N, Cheung A, Quistorff B, et al. Restricting glycolysis impairs brown adipocyte glucose and oxygen consumption. Am J Physiol-Endocrinol Metab. 2018;314:E214-E223.
Zhang F, Hao G, Shao M, Nham K, An Y, Wang Q, et al. An adipose tissue atlas: An image-guided identification of human-like BAT and Beige depots in rodents. Cell Metab. 2018;27:252-262.
Wang Z, Ning T, Song A, Rutter J, Wang QA, Jiang L. Chronic cold exposure enhances glucose oxidation in brown adipose tissue. EMBO Rep. 2020;21:e50085.
Olsen JM, Csikasz RI, Dehvari N, Lu L, Sandström A, Öberg AI, et al. β3-Adrenergically induced glucose uptake in brown adipose tissue is independent of UCP1 presence or activity: mediation through the mTOR pathway. Mol Metab. 2017;6:611-619.
Chondronikola M, Volpi E, Børsheim E, Porter C, Annamalai P, Enerbäck S, et al. Brown adipose tissue improves whole-body glucose homeostasis and insulin sensitivity in humans. Diabetes. 2014;63:4089-4099.
Caron A, Labbé SM, Carter S, Roy MC, Lecomte R, Ricquier D, et al. Loss of UCP2 impairs cold-induced non-shivering thermogenesis by promoting a shift toward glucose utilization in brown adipose tissue. Biochimie. 2017;134:118-126.
Held NM, Kuipers EN, Van Weeghel M, Van Klinken JB, Denis SW, Lombès M, et al. Pyruvate dehydrogenase complex plays a central role in brown adipocyte energy expenditure and fuel utilization during short-term beta-adrenergic activation. Sci Rep. 2018;8:9562.
Roh HC, Tsai LTY, Shao M, Tenen D, Shen Y, Kumari M, et al. Warming induces significant reprogramming of beige, but not brown adipocyte cellular identity. Cell Metab. 2018;27:1121-1137.
Kotzbeck P, Giordano A, Mondini E, Murano I, Severi I, Venema W, et al. Brown adipose tissue whitening leads to brown adipocyte death and adipose tissue inflammation. J Lipid Res. 2018;59:784-794.
Rodríguez-Cuenca S, Pujol E, Justo R, Frontera M, Oliver J, Gianotti M, et al. Sex-dependent thermogenesis, differences in mitochondrial morphology and function, and adrenergic response in brown adipose tissue. J Biol Chem. 2002;277:42958-42963.
McDonald RB, Hamilton JS, Horwitz BA. Influence of age and gender on Brown adipose tissue norepinephrine turnover. Proc Soc Exp Biol Med. 1993;204:117-121.
Kim SN, Jung YS, Kwon HJ, Seong JK, Granneman JG, Lee YH. Sex differences in sympathetic innervation and browning of white adipose tissue of mice. Biol Sex Differ. 2016;7:67.
Pedersen SB, Bruun JM, Kristensen K, Richelsen B. Regulation of UCP1, UCP2, and UCP3 mRNA expression in brown adipose tissue, white adipose tissue, and skeletal muscle in rats by estrogen. Biochem Biophys Res Commun. 2001;288:191-197.
Chou TJ, Lu CW, Liao CC, Chiang CH, Huang CC, Huang KC. Ovariectomy interferes with proteomes of Brown adipose tissue in rats. Int J Med Sci. 2022;19:499-510.
Butera PC. Estradiol and the control of food intake. Physiol Behav. 2010;99:175-180.
Asarian L, Geary N. Cyclic estradiol treatment normalizes body weight and restores physiological patterns of spontaneous feeding and sexual receptivity in ovariectomized rats. Horm Behav. 2002;42:461-471.
Wade GN, Schneider JE. Metabolic fuels and reproduction in female mammals. Neurosci Biobehav Rev. 1992;16:235-272.
Hansen MF, Fahmy N, Nielsen HJ. The influence of sexual hormones on lipogenesis and lipolysis in rat fat cells. Acta Endocrinol. 1980;95:566-570.
Kim HJ, Kalkhoff RK. Sex steroid influence on triglyceride metabolism. J Clin Invest. 1975;56:888-896.
Giles ED, Jackman MR, Johnson GC, Schedin PJ, Houser JL, MacLean PS. Effect of the estrous cycle and surgical ovariectomy on energy balance, fuel utilization, and physical activity in lean and obese female rats. Am J Physiol Regul Integr Comp Physiol. 2010;299:R1634-R1642.
Santiago AM, Clegg DJ, Routh VH. Ventromedial hypothalamic glucose sensing and glucose homeostasis vary throughout the estrous cycle. Physiol Behav. 2016;167:248-254.
Reinisch I, Schreiber R, Prokesch A. Regulation of thermogenic adipocytes during fasting and cold. Mol Cell Endocrinol. 2020;512:110869.
Rothwell NJ, Stock MJ. A role for brown adipose tissue in diet-induced thermogenesis. Nature. 1979;281:31-35. https://doi.org/10.1038/281031a0
Westerterp KR. Diet induced thermogenesis. Nutr Metab. 2004;1:1-5.
Champigny O, Ricquier D. Effects of fasting and refeeding on the level of uncoupling protein mRNA in rat brown adipose tissue: evidence for diet-induced and cold-induced responses. J Nutr. 1990;120:1730-1736.
Zhan XM, Li YL, Wang DH. Effects of fasting and refeeding on body mass, thermogenesis and serum leptin in Brandt's voles (Lasiopodomys brandtii). J Therm Biol. 2009;34:237-243.
McLean AC, Valenzuela N, Fai S, Bennett SAL. Performing vaginal lavage, crystal violet staining, and vaginal cytological evaluation for mouse estrous cycle staging identification. J Vis Exp. 2012;67:e4389.
Duncombe WG. The colorimetric micro-determination of non-esterified fatty acids in plasma. Clin Chim Acta. 1964;9:122-125.
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin-phenol reagent. J Biol Cemistry. 1951;193:265-275.
Giordano A, Smorlesi A, Frontini A, Barbatelli G, Cint S. White, brown and pink adipocytes: the extraordinary plasticity of the adipose organ. Eur J Endocrinol. 2014;170:R159-R171.
Goldman JM, Murr AS, Cooper RL. The rodent estrous cycle: characterization of vaginal cytology and its utility in toxicological studies. Birth Defects Res B Dev Reprod Toxicol. 2007;80:84-97.
Yamaguchi M, Katoh S, Morimoto C, Sakayama K, Shiosaka T, Masuno H, et al. The hormonal responses of lipoprotein lipase activity and lipolysis in adipose tissue differ depending on the stage of the estrous cycle in female rats. Int J Obes (Lond). 2002;26:610-617.
Smith MS, Freeman ME, Neill JD. The control of progesterone secretion during the estrous cycle and early pseudopregnancy in the rat: prolactin, gonadotropin and steroid levels associated with rescue of the corpus luteum of pseudopregnancy. Endocrinology. 1975;96:219-226.
Butcher RL, Collins WE, Fugo NW. Plasma concentration of LH, FSH, prolactin, progesterone and estradiol-17beta throughout the 4-day estrous cycle of the rat. Endocrinology. 1974;94:1704-1708.
Tang HN, Tang CY, Man XF, Tan SW, Guo Y, Tang J, et al. Plasticity of adipose tissue in response to fasting and refeeding in male mice. Nutr Metab. 2017;14:3.
de Jong JMA, Sun W, Pires ND, Frontini A, Balaz M, Jespersen NZ, et al. Human brown adipose tissue is phenocopied by classical brown adipose tissue in physiologically humanized mice. Nat Metab. 2019;1:830-843.
Duncan RE, Ahmadian M, Jaworski K, Sarkadi-Nagy E, Sul HS. Regulation of lipolysis in adipocytes. Annu Rev Nutr. 2007;27:79-101.
Markussen L, Rondini E, Johansen O, Madsen J, Sustarsic E, Marcher A, et al. Lipolysis regulates major transcriptional programs in brown adipocytes. Nat Commun. 2022;13:3956.
Cao Q, Wang S, Wang H, Cui X, Jing J, Yu L, et al. Fatty acids rescue the thermogenic function of sympathetically denervated brown fat. Biomolecules. 2021;11:1428.
Dakic T, Markelic M, Ruzicic A, Jevdjovic T, Lakic I, Djordjevic J, et al. Hypothalamic insulin expression remains unaltered after short-term fasting in female rats. Endocrine. 2022;78:476-483.
Liao Y, Hung MC. Physiological regulation of Akt activity and stability. Am J Transl Res. 2010;2:19-42.
Nabatame Y, Hosooka T, Aoki C, Hosokawa Y, Imamori M, Tamori Y, et al. Kruppel-like factor 15 regulates fuel switching between glucose and fatty acids in brown adipocytes. J Diabetes Investig. 2021;12:1144-1151.

Auteurs

Tamara Dakic (T)

Department for Comparative Physiology and Ecophysiology, Institute for Physiology and Biochemistry, University of Belgrade-Faculty for Biology, Belgrade, Serbia.

Ksenija Velickovic (K)

Department of Cell and Tissue Biology, Institute for Zoology, University of Belgrade-Faculty of Biology, Belgrade, Serbia.

Iva Lakic (I)

Department for Comparative Physiology and Ecophysiology, Institute for Physiology and Biochemistry, University of Belgrade-Faculty for Biology, Belgrade, Serbia.

Aleksandra Ruzicic (A)

Department for Comparative Physiology and Ecophysiology, Institute for Physiology and Biochemistry, University of Belgrade-Faculty for Biology, Belgrade, Serbia.

Andjela Milicevic (A)

Department for Comparative Physiology and Ecophysiology, Institute for Physiology and Biochemistry, University of Belgrade-Faculty for Biology, Belgrade, Serbia.

Nikola Plackic (N)

Department for Comparative Physiology and Ecophysiology, Institute for Physiology and Biochemistry, University of Belgrade-Faculty for Biology, Belgrade, Serbia.

Predrag Vujovic (P)

Department for Comparative Physiology and Ecophysiology, Institute for Physiology and Biochemistry, University of Belgrade-Faculty for Biology, Belgrade, Serbia.

Tanja Jevdjovic (T)

Department for Comparative Physiology and Ecophysiology, Institute for Physiology and Biochemistry, University of Belgrade-Faculty for Biology, Belgrade, Serbia.

Classifications MeSH