Research Progress of Ontogeny and Thermogenesis of Brown Adipose Tissue

ZHANG Yanmei; JIN Hai; LI Changqing

doi:10.3969/j.issn.1006-267x.2021.10.002

Chinese Journal of Animal Nutrition >

2021 , Vol. 33 >Issue 10: 5416 - 5423

DOI: https://doi.org/10.3969/j.issn.1006-267x.2021.10.002

Research Progress of Ontogeny and Thermogenesis of Brown Adipose Tissue

ZHANG Yanmei ,
JIN Hai ,
LI Changqing

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1. Inner Mongolia Key Laboratory of Animal Nutrition and Feed Science, College of Animal Science, Inner Mongolia Agricultural University, Hohhot 010018, China;
2. Inner Mongolia Autonomous Region Academy of Agriculture and Animal Husbandry, Hohhot 010031, China

Received date: 2021-03-30

Online published: 2021-10-16

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Abstract

Body temperature maintenance is one of the most important physiological processes initiated after birth. Brown adipose tissue (BAT) is a main place of thermogenesis in animals, by activating uncoupling protein 1 (UCP1), which is located in the inner membrane of mitochondria, it is responsible for providing heat for the body. The survival of newborn animals highly depends on bat heat production to maintain core body temperature to adapt to the peripheral cold environment. BAT differs with white adipose tissue (WAT) in the morphology, development stage and anatomical location. Under cold and β-adrenergic receptor agonist conditions, a new type of thermogenesis cell can be produced—beige adipocyte, they are similar to brown adipocytes in structure and function, both of them are based on UCP1 uncoupling and produce heat by consuming glucose and fat, therefore, they are considered as potential means to improve the survival rate of young animals and prevent and control obesity and metabolic diseases in human body. This review summarized the recent studies on thermogenesis, BAT and beige adipose tissue in sheep and rodents, mainly expatiated the thermogenesis mechanism and its developmental changes, in order to provide data for future research.

Key words： brown adipose tissue; thermogenesis; UCP1; thermostasis

Cite this article

ZHANG Yanmei , JIN Hai , LI Changqing . Research Progress of Ontogeny and Thermogenesis of Brown Adipose Tissue[J]. Chinese Journal of Animal Nutrition, 2021 , 33(10) : 5416 -5423 . DOI: 10.3969/j.issn.1006-267x.2021.10.002

References

[1] DIXON A B, KNIGHTS M, WINKLER J L, et al.Patterns of late embryonic and fetal mortality and association with several factors in sheep[J].Journal of Animal Science, 2007, 85(5):1274-1284.

[2] ONG F J, AHMED B A, ORESKOVICH S M, et al.Recent advances in the detection of brown adipose tissue in adult humans:a review[J].Clinical Science, 2018, 132(10):1039-1054.

[3] ALEXANDER G.Quantitative development of adipose tissue in foetal sheep[J].Australian Journal of Biological Sciences, 1978, 31(5):489-503.

[4] SATTERFIELD M C, WU G Y.Brown adipose tissue growth and development:significance and nutritional regulation[J].Frontiers in Bioscience (Landmark Edition), 2011, 16:1589-1608.
[5] LIDELL M E, BETZ M J, ENERBÄCK S.Brown adipose tissue and its therapeutic potential[J].Journal of Internal Medicine, 2014, 276(4):364-377.

[6] 李唐, 郑立, 贺花, 等.影响棕色脂肪代谢的调控因素及其应用[J].家畜生态学报, 2017, 38(12):6-10. LI T, ZHENG L, HE H, et al.Regulation factors affecting brown adipose tissue metabolism and their applications[J].Acta Ecologae Animalis Domastici, 2017, 38(12):6-10.(in Chinese)
[7] CANNON B, NEDERGAARD J.Brown adipose tissue:function and physiological significance[J].Physiological Reviews, 2004, 84(1):277-359.

[8] SEALE P, BJORK B, YANG W L, et al.PRDM16 controls a brown fat/skeletal muscle switch[J].Nature, 2008, 454(727):961-967.
[9] ALEXANDER G, WILLIAMS D.Shivering and non-shivering therogenesis during summit metabolism in young lambs[J].The Journal of Physiology, 1968, 198(2):251-276.

[10] KOPECNY L.Physiology of domestic animals[J].Australian Veterinary Journal, 2011, 89(10):401-401.

[11] POWER G G.Biology of temperature:the mammalian fetus[J].Journal of Developmental Physiology, 1989, 12(6):295-304.
[12] POPE M, BUDGE H, SYMONDS M E.The developmental transition of ovine adipose tissue through early Life[J].Acta Physiologica, 2014, 210(1):20-30.

[13] VERNON R G.6-the growth and metabolism of adipocytes[M]//BUTTERY P J, LINDSAY D B, HAYNES N B.Control and Manipulation of Animal Growth.London:Butterworths, 1986:67-83.
[14] VELICKOVIC K, CVORO A, SRDIC B, et al.Expression and subcellular localization of estrogen receptors α and β in human fetal brown adipose tissue[J].The Journal of Clinical Endocrinology and Metabolism, 2014, 99(1):151-159.

[15] TAGA H, CHILLIARD Y, MEUNIER B, et al.Cellular and molecular large-scale features of fetal adipose tissue:is bovine perirenal adipose tissue brown?[J].Journal of Cellular Physiology, 2012, 227(4):1688-1700.

[16] HENRY B A, BLACHE D, RAO A, et al.Disparate effects of feeding on core body and adipose tissue temperatures in animals selectively bred for Nervous or Calm temperament[J].American Journal of Physiology-Regulatory Integrative and Comparative Physiology, 2010, 299(3):R907-R917.
[17] SYMONDS M E, POPE M, BUDGE H.The ontogeny of brown adipose tissue[J].Annual Review of Nutrition, 2015, 35(1):295-320.

[18] LASAR D, JULIUS A, FROMME T, et al.Browning attenuates murine white adipose tissue expansion during postnatal development[J].Biochimica et Biophysica Acta:Molecular and Cell Biology of Lipids, 2013, 1831(5):960-968.

[19] VIRTANEN K A, LIDELL M E, ORAVA J, et al.Functional brown adipose tissue in healthy adults[J].The New England Journal of Medicine, 2009, 360(15):1518-1525.

[20] CYPESS A M, LEHMAN S, WILLIAMS G, et al.Identification and importance of brown adipose tissue in adult humans[J].The New England Journal of Medicine, 2009, 360(15):1509-1517.

[21] VERGNES L, DAVIES G R, LIN J Y, et al.Adipocyte browning and higher mitochondrial function in periadrenal but not SC fat in pheochromocytoma[J].The Journal of Clinical Endocrinology and Metabolism, 2016, 101(11):4440-4448.

[22] VAN MARKEN LICHTENBELT W D, VANHOMMERIG J W, SMULDERS N M, et al.Cold-activated brown adipose tissue in healthy men[J].The New England Journal of Medicine, 2009, 360(15):1500-1508.

[23] SCOTNEY H, SYMONDS M E, LAW J, et al.Glucocorticoids modulate human brown adipose tissue thermogenesis in vivo[J].Metabolism:Clinical and Experimental, 2017, 70:125-132.
[24] SYMONDS M E, POPE M, SHARKEY D, et al.Adipose tissue and fetal programming[J].Diabetologia, 2012, 55(6):1597-1606.

[25] HENRY B A, POPE M, BIRTWISTLE M, et al.Ontogeny and thermogenic role for sternal fat in female sheep[J].Endocrinology, 2017, 158(7):2212-2225.

[26] ASANO H, YAMADA T, HASHIMOTO O, et al.Diet-induced changes in UCP1 expression in bovine adipose tissues[J].General and Comparative Endocrinology, 2013, 184:87-92.
[27] MAGISTRELLI D, AUFY A A, PINOTTI L, et al.Analysis of weaning-induced stress in Saanen goat kids[J].Journal of Animal Physiology and Animal Nutrition, 2013, 97(4):732-739.

[28] SBARBATI A, MORRONI M, ZANCANARO C, et al.Rat interscapular brown adipose tissue at different ages:a morphometric study[J].International Journal of Obesity, 1991, 15(9):581-587.
[29] YUAN Y N, LIU W Z, LIU J H, et al.Cloning and ontogenetic expression of the uncoupling protein 1 gene UCP1 in sheep[J].Journal of Applied Genetics, 2012, 53(2):203-212.

[30] BEATTY D T, BARNES A, TAYLOR E, et al.Do changes in feed intake or ambient temperature cause changes in cattle rumen temperature relative to core temperature?[J].Journal of Thermal Biology, 2008, 33(1):12-19.

[31] DIN M U, SAARI T, RAIKO J, et al.Postprandial oxidative metabolism of human brown fat indicates thermogenesis[J].Cell Metabolism, 2018, 28(2):207-216.e3.

[32] DUBOIS-FERRIōRE R, CHINET A E.Contribution of skeletal muscle to the regulatory non-shivering thermogenesis in small mammals[J].Pflugers Archiv:European Journal of Physiology, 1981, 390(3):224-229.

[33] PUIGSERVER P, WU Z, PARK C W, et al.A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis[J].Cell, 1998, 92(6):829-839.

[34] BRONNIKOV G, HOUSTě K J, NEDERGAARD J.Beta-adrenergic, cAMP-mediated stimulation of proliferation of brown fat cells in primary culture.Mediation via beta 1 but not via beta 3 adrenoceptors[J].The Journal of Biological Chemistry, 1992, 267(3):2006-2013.

[35] CARPENTIER A C, BLONDIN D P, VIRTANEN K A, et al.Brown adipose tissue energy metabolism in humans[J].Frontiers in Endocrinology, 2018, 9:447.
[36] BLONDIN D P, FRISCH F, PHOENIX S, et al.Inhibition of intracellular triglyceride lipolysis suppresses cold-induced brown adipose tissue metabolism and increases shivering in humans[J].Cell Metabolism, 2017, 25(2):438-447.

[37] ENERBÄCK S, JACOBSSON A, SIMPSON E M, et al.Mice lacking mitochondrial uncoupling protein are cold-sensitive but not obese[J].Nature, 1997, 387:90-94.
[38] CANNON B, NEDERGAARD J.Nonshivering thermogenesis and its adequate measurement in metabolic studies[J].The Journal of Experimental Biology, 2011, 214(Pt 2):242-253.
[39] BARTELT A, BRUNS O T, REIMER R, et al.Brown adipose tissue activity controls triglyceride clearance[J].Nature Medicine, 2011, 17(2):200-205.

[40] WINTHER S, ISIDOR M S, BASSE A L, et al.Restricting glycolysis impairs brown adipocyte glucose and oxygen consumption[J].American Journal of Physiology:Endocrinology and Metabolism, 2018, 314(3):E214-E223.
[41] NGUYEN H P, YI D, LIN F, et al.Aifm2, a NADH oxidase, supports robust glycolysis and is required for cold- and diet-induced thermogenesis[J].Molecular Cell, 2020, 77(3):600-617.

[42] SCHREIBER R, DIWOKY C, SCHOISWOHL G, et al.Cold-induced thermogenesis depends on ATGL-mediated lipolysis in cardiac muscle, but not brown adipose tissue[J].Cell Metabolism, 2017, 26(5):753-763.

[43] SYMONDS M E, ANDREWS D C, JOHNSON P.The endocrine and metabolic response to feeding in the developing lamb[J].The Journal of Endocrinology, 1989, 123(2):295-302.

[44] SYMONDS M E.Brown adipose tissue growth and development[J].Scientifica, 2013, 2013:305763.
[45] STERN J H, SCHERER P E.Adipose tissue biology in 2014:advances in our understanding of adipose tissue homeostasis[J].Nature Reviews Endocrinology, 2015, 11(2):71-72.

[46] COHEN P, SPIEGELMAN B M.Brown and beige fat:molecular parts of a thermogenic machine[J].Diabetes, 2015, 64(7):2346-2351.

[47] HARMS M, SEALE P.Brown and beige fat:development, function and therapeutic potential[J].Nature Medicine, 2013, 19(10):1252-1263.

[48] ROSENWALD M, PERDIKARI A, RVLICKE T, et al.Bi-directional interconversion of brite and white adipocytes[J].Nature Cell Biology, 2013, 15:659-667.
[49] NEDERGAARD J, CANNON B.UCP1 mRNA does not produce heat[J].Biochimica et Biophysica Acta:Molecular and Cell Biology of Lipids, 2013, 1831(5):943-949.

[50] ROWLAND L A, BAL N C, KOZAK L P, et al.Uncoupling protein 1 and sarcolipin are required to maintain optimal thermogenesis, and loss of both systems compromises survival of mice under cold stress[J].The Journal of Biological Chemistry, 2015, 290(19):12282-12289.

[51] GONG D W, HE Y, KARAS M, et al.Uncoupling protein-3 is a mediator of thermogenesis regulated by thyroid hormone, beta3-adrenergic agonists, and leptin[J].The Journal of Biological Chemistry, 1997, 272(39):24129-24132.

[52] BLONDIN D P, DAOUD A, TAYLOR T, et al.Four-week cold acclimation in adult humans shifts uncoupling thermogenesis from skeletal muscles to brown adipose tissue[J].The Journal of Physiology, 2017, 595(6):2099-2113.

[53] BAL N C, MAURYA S K, SINGH S, et al.Increased reliance on muscle-based thermogenesis upon acute minimization of brown adipose tissue function[J].The Journal of Biological Chemistry, 2016, 291(33):17247-17257.

[54] WIJERS S L J, SCHRAUWEN P, SARIS W H M, et al.Human skeletal muscle mitochondrial uncoupling is associated with cold induced adaptive thermogenesis[J].PLoS One, 2008, 3(3):e1777.
[55] CLARKE S D, LEE K, ANDREWS Z B, et al.Postprandial heat production in skeletal muscle is associated with altered mitochondrial function and altered futile calcium cycling[J].American Journal of Physiology:Regulatory Integrative and Comparative Physiology, 2012, 303(10):R1071-R1079.
[56] HENRY B A, DUNSHEA F R, GOULD M, et al.Profiling postprandial thermogenesis in muscle and fat of sheep and the central effect of leptin administration[J].Endocrinology, 2008, 149(4):2019-2026.

[57] SATTERFIELD M C, DUNLAP K A, KEISLER D H, et al.Arginine nutrition and fetal brown adipose tissue development in nutrient-restricted sheep[J].Amino Acids, 2013, 45(3):489-499.

[58] BISPHAM J, GOPALAKRISHNAN G S, DANDREA J, et al.Maternal endocrine adaptation throughout pregnancy to nutritional manipulation:consequences for maternal plasma leptin and cortisol and the programming of fetal adipose tissue development[J].Endocrinology, 2003, 144(8):3575-3585.

[59] OJHA S, ROBINSON L, YAZDANI M, et al.Brown adipose tissue genes in pericardial adipose tissue of newborn sheep are downregulated by maternal nutrient restriction in late gestation[J].Pediatric Research, 2013, 74(3):246-251.

[60] 杨欢.妊娠后期宫内生长限制对蒙古绵羊胎儿肾周褐色脂肪组织生长发育的影响[D].硕士学位论文.呼和浩特:内蒙古农业大学, 2020. YANG H.Effects of intrauterine growth restriction during late pregnancy on the growth and development of perirenal brown adipose tissue in Mongolia ovine fetus[D].Master's Thesis.Hohhot:Inner Mongolia Agricultural University, 2020.(in Chinese)
[61] FELDMANN H M, 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[J].Cell Metabolism, 2009, 9(2):203-209.

[62] KANG H W, LEE S G, OTIENO D, et al.Flavonoids, potential bioactive compounds, and non-shivering thermogenesis[J].Nutrients, 2018, 10(9):1168.
[63] ZHANG T, DENG B H, ZHANG R X, et al.Dietary sea buckthorn pomace induces beige adipocyte formation in inguinal white adipose tissue in lambs[J].Animals, 2019, 9(4):193.
[64] WU J, BOSTRÖM P, SPARKS L M, et al.Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human[J].Cell, 2012, 150(2):366-376.

[65] NEDERGAARD J, CANNON B.The browning of white adipose tissue:some burning issues[J].Cell Metabolism, 2014, 20(3):396-407.

[66] ALDISS P, DAVIES G, WOODS R, et al.‘Browning’ the cardiac and peri-vascular adipose tissues to modulate cardiovascular risk[J].International Journal of Cardiology, 2017, 228:265-274.
[67] KEIPERT S, JASTROCH M.Brite/beige fat and UCP1-is it thermogenesis?[J].Biochimica et Biophysica Acta:Bioenergetics, 2014, 1837(7):1075-1082.

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