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Acute and chronic cold exposure differentially affects the browning of porcine white adipose tissue

Published online by Cambridge University Press:  16 November 2017

Y. Gao ,
N. R. Qimuge ,
J. Qin ,
R. Cai ,
X. Li ,
G. Y. Chu ,
W. J. Pang  and
G. S. Yang
Y. Gao
Affiliation:
Laboratory of Animal Fat Deposition & Muscle Development, College of Animal Science and Technology, Northwest A&F University, Yangling, Shaanxi 712100, China
N. R. Qimuge
Affiliation:
Laboratory of Animal Fat Deposition & Muscle Development, College of Animal Science and Technology, Northwest A&F University, Yangling, Shaanxi 712100, China
J. Qin
Affiliation:
Laboratory of Animal Fat Deposition & Muscle Development, College of Animal Science and Technology, Northwest A&F University, Yangling, Shaanxi 712100, China
R. Cai
Affiliation:
Laboratory of Animal Fat Deposition & Muscle Development, College of Animal Science and Technology, Northwest A&F University, Yangling, Shaanxi 712100, China
X. Li
Affiliation:
Laboratory of Animal Fat Deposition & Muscle Development, College of Animal Science and Technology, Northwest A&F University, Yangling, Shaanxi 712100, China
G. Y. Chu
Affiliation:
Laboratory of Animal Fat Deposition & Muscle Development, College of Animal Science and Technology, Northwest A&F University, Yangling, Shaanxi 712100, China
W. J. Pang*
Affiliation:
Laboratory of Animal Fat Deposition & Muscle Development, College of Animal Science and Technology, Northwest A&F University, Yangling, Shaanxi 712100, China
G. S. Yang*
Affiliation:
Laboratory of Animal Fat Deposition & Muscle Development, College of Animal Science and Technology, Northwest A&F University, Yangling, Shaanxi 712100, China
*
†E-mail: pwj1226@nwsuaf.edu.cn; gsyang999@hotmail.com
†E-mail: pwj1226@nwsuaf.edu.cn; gsyang999@hotmail.com
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Abstract

Piglets are characteristically cold intolerant and thus susceptible to high mortality. However, browning of white adipose tissue (WAT) can induce non-shivering thermogenesis as a potential strategy to facilitate the animal’s response to cold. Whether cold exposure can induce browning of subcutaneous WAT (sWAT) in piglets in a similar manner as it can in humans remains largely unknown. In this study, piglets were exposed to acute cold (4°C, 10 h) or chronic cold exposure (8°C, 15 days), and the genes and proteins of uncoupling protein 1 (UCP1)-dependent and independent thermogenesis, mitochondrial biogenesis, lipogenic and lipolytic processes were analysed. Interestingly, acute cold exposure induced browning of porcine sWAT, smaller adipocytes and the upregulated expression of UCP1, PGC1α, PGC1β, C/EBPβ, Cidea, UCP3, CKMT1 and PM20D1. Conversely, chronic cold exposure impaired the browning process, reduced mitochondrial numbers and the expression of browning markers, including UCP1, PGC1α and PRDM16. The present study demonstrated that acute cold exposure (but not chronic cold exposure) induces porcine sWAT browning. Thus, browning of porcine sWAT could be a novel strategy to balance the body temperature of piglets, and thus could be protective against cold exposure.

Keywords

pigwhite adipose tissuebrowninguncoupling protein 1-independent thermogenesismitochondria
Type
Research Article
Information
animal , Volume 12 , Issue 7 , July 2018 , pp. 1435 - 1441
Copyright
© The Animal Consortium 2017 

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References

Balsbaugh, RK, Curtis, SE, Meyer, RC and Norton, HW 1986. Cold resistance and environmental temperature preference in diarrheic piglets. Journal of Animal Science 62, 315–326.Google Scholar
Bellinger, DA, Merricks, EP and Nichols, TC 2006. Swine models of type 2 diabetes mellitus: insulin resistance, glucose tolerance, and cardiovascular complications. Institute for Laboratory Animal Research Journal 47, 243–258.Google ScholarPubMed
Bi, P, Shan, T, Liu, W, Yue, F, Yang, X, Liang, XR, Wang, J, Li, J, Carlesso, N, Liu, X and Kuang, S 2014. Inhibition of notch signaling promotes browning of white adipose tissue and ameliorates obesity. Nature Medicine 20, 911–918.Google Scholar
Collins, S 2011. Β-Adrenoceptor signaling networks in adipocytes for recruiting stored fat and energy expenditure. Frontiers in Endocrinology (Lausanne) 2, 102.Google ScholarPubMed
Cypess, AM, Weiner, LS, Roberts-Toler, C, Franquet, EE, Kessler, SH, Kahn, PA, English, J, Chatman, K, Trauger, SA, Doria, A and Kolodny, GM 2015. Activation of human brown adipose tissue by a beta3-adrenergic receptor agonist. Cell Metabolism 21, 33–38.Google Scholar
Dodd, GT, Decherf, S, Loh, K, Simonds, SE, Wiede, F, Balland, E, Merry, TL, Munzberg, H, Zhang, ZY, Kahn, BB, Neel, BG, Bence, KK, Andrews, ZB, Cowley, MA and Tiganis, T 2015. Leptin and insulin act on POMC neurons to promote the browning of white fat. Cell 160, 88–104.Google Scholar
Fedorenko, A, Lishko, PV and Kirichok, Y 2012. Mechanism of fatty-acid-dependent UCP1 uncoupling in brown fat mitochondria. Cell 151, 400–413.CrossRefGoogle ScholarPubMed
Harms, M and Seale, P 2013. Brown and beige fat: development, function and therapeutic potential. Nature Medicine 19, 1252–1263.Google Scholar
Jespersen, NZ, Larsen, TJ, Peijs, L, Daugaard, S, Homoe, P, Loft, A, de Jong, J, Mathur, N, Cannon, B, Nedergaard, J, Pedersen, BK, Moller, K and Scheele, C 2013. A classical brown adipose tissue mRNA signature partly overlaps with brite in the supraclavicular region of adult humans. Cell Metabolism 17, 798–805.CrossRefGoogle ScholarPubMed
Kajimura, S, Spiegelman, BM and Seale, P 2015. Brown and beige fat: physiological roles beyond heat generation. Cell Metabolism 22, 546–559.CrossRefGoogle Scholar
Kazak, L, Chouchani, ET, Jedrychowski, MP, Erickson, BK, Shinoda, K, Cohen, P, Vetrivelan, R, Lu, GZ, Laznik-Bogoslavski, D, Hasenfuss, SC, Kajimura, S, Gygi, SP and Spiegelman, BM 2015. A creatine-driven substrate cycle enhances energy expenditure and thermogenesis in beige fat. Cell 163, 643–655.CrossRefGoogle ScholarPubMed
Lin, J, Cao, C, Tao, C, Ye, R, Dong, M, Zheng, Q, Wang, C, Jiang, X, Qin, G, Yan, C, Li, K, Speakman, JR, Wang, Y, Jin, W and Zhao, J 2017. Cold adaptation in pigs depends on UCP3 in beige adipocytes. Journal ofMolecular Cell Biology 2017, 1–12.Google Scholar
Long, JZ, Svensson, KJ, Bateman, LA, Lin, H, Kamenecka, T, Lokurkar, IA, Lou, J, Rao, RR, Chang, MR, Jedrychowski, MP, Paulo, JA, Gygi, SP, Griffin, PR, Nomura, DK and Spiegelman, BM 2016. The secreted enzyme PM20D1 regulates lipidated amino acid uncouplers of mitochondria. Cell 166, 424–435.CrossRefGoogle ScholarPubMed
Lowell, BB and Spiegelman, BM 2000. Towards a molecular understanding of adaptive thermogenesis. Nature 404, 652–660.CrossRefGoogle ScholarPubMed
Puigserver, P and Spiegelman, BM 2003. Peroxisome proliferator-activated receptor-gamma coactivator 1 alpha (PGC-1 alpha): transcriptional coactivator and metabolic regulator. Endocrine Reviews 24, 78–90.Google Scholar
Rosenwald, M, Perdikari, A, Rulicke, T and Wolfrum, C 2013. Bi-directional interconversion of brite and white adipocytes. Nature Cell Biology 15, 659–667.Google Scholar
Seale, P and Lazar, MA 2009. Brown fat in humans: turning up the heat on obesity. Diabetes 58, 1482–1484.Google Scholar
Seki, T, Hosaka, K, Lim, S, Fischer, C, Honek, J, Yang, Y, Andersson, P, Nakamura, M, Naslund, E, Yla-Herttuala, S, Sun, M, Iwamoto, H, Li, X, Liu, Y, Samani, NJ and Cao, Y 2016. Endothelial PDGF-CC regulates angiogenesis-dependent thermogenesis in beige fat. Nature Communications 7, 12152.CrossRefGoogle ScholarPubMed
Shabalina, IG, Petrovic, N, de Jong, JM, Kalinovich, AV, Cannon, B and Nedergaard, J 2013. UCP1 in brite/beige adipose tissue mitochondria is functionally thermogenic. Cell Reports 5, 1196–1203.CrossRefGoogle ScholarPubMed
Sidossis, LS, Porter, C, Saraf, MK, Borsheim, E, Radhakrishnan, RS, Chao, T, Ali, A, Chondronikola, M, Mlcak, R, Finnerty, CC, Hawkins, HK, Toliver-Kinsky, T and Herndon, DN 2015. Browning of subcutaneous white adipose tissue in humans after severe adrenergic stress. Cell Metabolism 22, 219–227.Google Scholar
Spurlock, ME and Gabler, NK 2008. The development of porcine models of obesity and the metabolic syndrome. The Journal of Nutrition 138, 397–402.Google Scholar
van der Lans, AA, Hoeks, J, Brans, B, Vijgen, GH, Visser, MG, Vosselman, MJ, Hansen, J, Jorgensen, JA, Wu, J, Mottaghy, FM, Schrauwen, P and van Marken, LW 2013. Cold acclimation recruits human brown fat and increases nonshivering thermogenesis. Journal of Clinical Investigation 123, 3395–3403.Google Scholar
Wang, WS and Seale, P 2016. Control of brown and beige fat development. Nature Reviews Molecular Cell Biology 17, 691–702.CrossRefGoogle Scholar
Wu, J, Bostrom, P, Sparks, LM, Ye, L, Choi, JH, Giang, AH, Khandekar, M, Virtanen, KA, Nuutila, P, Schaart, G, Huang, K, Tu, H, van Marken, LW, Hoeks, J, Enerback, S, Schrauwen, P and Spiegelman, BM 2012. Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell 150, 366–376.Google Scholar
Wu, ZD, Puigserver, P, Andersson, U, Zhang, CY, Adelmant, G, Mootha, V, Troy, A, Cinti, S, Lowell, B, Scarpulla, RC and Spiegelman, BM 1999. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98, 115–124.Google Scholar
Xue, Y, Petrovic, N, Cao, R, Larsson, O, Lim, S, Chen, S, Feldmann, HM, Liang, Z, Zhu, Z, Nedergaard, J, Cannon, B and Cao, Y 2009. Hypoxia-independent angiogenesis in adipose tissues during cold acclimation. Cell Metabolism 9, 99–109.Google Scholar
Xue, Y, Xu, X, Zhang, XQ, Farokhzad, OC and Langer, R 2016. Preventing diet-induced obesity in mice by adipose tissue transformation and angiogenesis using targeted nanoparticles. Proceedings of the National Academy of Sciences of the United States of America 113, 5552–5557.Google Scholar
Yoneshiro, T, Aita, S, Matsushita, M, Kayahara, T, Kameya, T, Kawai, Y, Iwanaga, T and Saito, M 2013. Recruited brown adipose tissue as an antiobesity agent in humans. Journal of Clinical Investigation 123, 3404–3408.Google Scholar
Yoneshiro, T, Aita, S, Matsushita, M, Okamatsu-Ogura, Y, Kameya, T, Kawai, Y, Miyagawa, M, Tsujisaki, M and Saito, M 2011. Age-related decrease in cold-activated brown adipose tissue and accumulation of body fat in healthy humans. Obesity 19, 1755–1760.Google Scholar
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