Journal of Animal Science and Technology

Korean Society of Animal Sciences and Technology (한국축산학회)
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The Regulation of Lipolysis in Adipose Tissue

  • Serr, Julie (Department of Animal Sciences, The Ohio State University) ;
  • Li, Xiang (Department of Animal Sciences, The Ohio State University) ;
  • Lee, Kichoon (Department of Animal Sciences, The Ohio State University)
  • Received : 2013.04.04
  • Accepted : 2013.08.01
  • Published : 2013.08.31
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Abstract

Knowledge regarding lipid catabolism has been of great interest in the field of animal sciences. In the livestock industry, excess fat accretion in meat is costly to the producer and undesirable to the consumer. However, intramuscular fat (marbling) is desirable to enhance carcass and product quality. The manipulation of lipid content to meet the goals of animal production requires an understanding of the detailed mechanisms of lipid catabolism to help meticulously design nutritional, pharmacological, and physiological approaches to regulate fat accretion. The concept of a basic system of lipases and their co-regulators has been identified. The major lipases cleave triacylglycerol (TAG) stored in lipid droplets in a sequential manner. In adipose tissue, adipose triglyceride lipase (ATGL) performs the first and rate-limiting step of TAG breakdown through hydrolysis at the sn-1 position of TAG to release a non-esterified fatty acid (NEFA) and diacylglycerol (DAG). Subsequently, cleavage of DAG occurs via the rate-limiting enzyme hormone-sensitive lipase (HSL) for DAG catabolism, which is followed by monoglyceride lipase (MGL) for monoacylglycerol (MAG) hydrolysis. Recent identification of the co-activator (Comparative Gene Identification-58) and inhibitor [G(0)/G(1) Switch Gene 2] of ATGL have helped elucidate this important initial step of TAG breakdown, while also generating more questions. Additionally, the roles of these lipolysis-related enzymes in muscle, liver and skin tissue have also been found to be of great importance for the investigation of systemic lipolytic regulation.

Keywords

References

  1. Ailhaud, G. and Hauner, H. 2004. Development of white adipose tissue. Handbook of Obesity, Etiology and Pathophysiology, 2nd edition, eds. G. A. Bray and C. Bouchard, Marcel Dekker, New York, NY, pp. 48.
  2. Bernlohr, D. A., Jenkins, A. E. and Bennaars, A. A. 2002. Adipose tissue and lipid metabolism. Fourth edition ed. Vance, D. E., Vance, J. E., Biochemistry of Lipids, Lipoproteins and Membrances, Elsevier, Amsterdam, pp. 263-289.
  3. Bertrand, T., Auge, F., Houtmann, J., Rak, A., Vallee, F., Mikol, V., Berne, P. F., Michot, N., Cheuret, D., Hoornaert, C. and Mathieu, M. 2010. Structural basis for human monoglyceride lipase inhibition. J. Mol. Biol. 396:663-673. https://doi.org/10.1016/j.jmb.2009.11.060
  4. Borgstrom, B. and Erlanson, C. 1971. Pancreatic juice co-lipase: physiological importance. Biochim. Biophys. Acta. 20:509-513.
  5. Chakrabarti, P., English, T., Shi, J., Smas, C. M. and Kandror, K. V. 2010. Mammalian target of rapamycin complex 1 suppresses lipolysis, stimulates lipogenesis, and promotes fat storage. Diabetes 59:775-781. https://doi.org/10.2337/db09-1602
  6. Chanarin, I., Patel, A., Slavin, G., Willis, E. J., Andrews, T. M. and Stewart, G. 1975. Neutral-lipid storage disease: a new disorder of lipid metabolism. Br. Med. J. 1:553-555. https://doi.org/10.1136/bmj.1.5957.553
  7. Cinti, S. 2006. The role of brown adipose tissue in human obesity. Nutr. Metab. Cardiovasc. Dis. 16:569-574. https://doi.org/10.1016/j.numecd.2006.07.009
  8. Cornaciu, I., Boeszoermenyi, A., Lindermuth, H., Nagy, H. M., Cerk, I. K., Ebner, C., Salzburger, B., Gruber, A., Schweiger, M., Zechner, R., Lass, A., Zimmermann, R. and Oberer, M. 2011. The minimal domain of adipose triglyceride lipase (ATGL) ranges until leucine 254 and can be activated and inhibited by CGI-58 and G0S2, respectively. PLoS One 6:26349. https://doi.org/10.1371/journal.pone.0026349
  9. Coppack, S. W., Jensen, M. D. and Miles, J. M. 1994. In vivo regulation of lipolysis in humans. J. Lipid Res. 35:177-193.
  10. DeFronzo, R. A. 2004. Pathogenesis of type 2 diabetes mellitus. Med. Clin. North Am. 88:787-835. https://doi.org/10.1016/j.mcna.2004.04.013
  11. Deiuliis, J. A. 2007. The metabolic and molecular regulation of adipose triglyceride lipase. Ph. D. Dissertation. The Ohio State University, Columbus.
  12. Deiuliis, J. A., Shin, J., Bae, D., Azain, M. J., Barb, R. and Lee, K. 2008. Developmental, hormonal, and nutritional regulation of porcine adipose triglyceride lipase (ATGL). Lipids 43:215-225. https://doi.org/10.1007/s11745-007-3146-1
  13. Eastmond, P. J. 2006. Sugar-dependent1 encodes a patatin domain triacylglycerol lipase that initiates storage oil breakdown in germinating Arabidopsis seeds. Plant Cell. 18:665-675. https://doi.org/10.1105/tpc.105.040543
  14. Enerback, S. 2010. Human brown adipose tissue. Cell Metab. 11:248-252. https://doi.org/10.1016/j.cmet.2010.03.008
  15. Festuccia, W. T., Laplante, M., Berthiaume, M., Gelinas, Y. and Deshaies, Y. 2006. PPARgamma agonism increases rat adipose tissue lipolysis, expression of glyceride lipases, and the response of lipolysis to hormonal control. Diabetologia. 49:2427-2436. https://doi.org/10.1007/s00125-006-0336-y
  16. Fischer, J., Negre-Salvayre, A. and Slavayre, R. 2007. Neutral lipid storage diseases and ATGL (adipose triglyceride lipase) and CGI-58/ABHD5 (alpha-beta hydrolase domain-containing 5) deficiency: myopathy, ichthyosis, but not obesity. Med. Sci. (Paris). 23:575-578. https://doi.org/10.1051/medsci/20072367575
  17. Fortin, A., Robertson, W. M. and Tong, A. K. W. 2005. The eating quality of Canadian pork and its relationship with intramuscular fat. Meat Sci. 69:297-305. https://doi.org/10.1016/j.meatsci.2004.07.011
  18. Gardan, D., Gondret, F. and Louveau, I. 2006. Lipid metabolism and secretory function of porcine intramuscular adipocytes compared with subcutaneous and perirenal adipocytes. Am. J. Physiol. Endocrinol. Metab. 291:372-380. https://doi.org/10.1152/ajpendo.00482.2005
  19. Ghosh, A. K., Ramakrishnan, G., Chandramohan, C. and Rajasekharan, R. 2008. CGI-58, the causative gene for Chanarin-Dorfman syndrome, mediates acylation of lysophosphatidic acid. J. Biol.Chem. 283:24525-24533. https://doi.org/10.1074/jbc.M801783200
  20. Giordano, A., Frontini, A. and Cinti, S. 2008. Adipose organ nerves revealed by immunohistochemistry. Methods Mol. Biol. 456:83-95. https://doi.org/10.1007/978-1-59745-245-8_6
  21. Gjerlaug-Enger, E., Aass, L., Odegard, J. and Vangen, O. 2010. Genetic parameters of meat quality traits in two pig breeds measured by rapid methods. Animal 4:1832-1843. https://doi.org/10.1017/S175173111000114X
  22. Granneman, J. G., Moore, H. P., Granneman, R. L., Greenberg, A. S., Obin, M. S. and Zhu, Z. 2007. Analysis of lipolytic protein trafficking and interactions in adipocytes. J. Biol. Chem. 282:5726-5735. https://doi.org/10.1074/jbc.M610580200
  23. Gruber, A., Cornaciu, I., Lass, A., Schweiger, M., Poeschl, M., Eder, C., Kumari, M., Schoiswohl, G., Wolinski, H., Kohlwein, S. D., Zechner, R., Zimmermann, R. and Oberer, M. 2010. The N-terminal region of comparative gene identification-58 (CGI-58) is important for lipid droplet binding and activation of adipose triglyceride lipase. J. Biol. Chem. 285:12289-12298. https://doi.org/10.1074/jbc.M109.064469
  24. Hamill, R. M., McBryan, J., McGee, C., Mullen, A. M., Sweeney, T., Talbot, A., Cairns, M. T. and Davey, G. C. 2012. Functional analysis of muscle gene expression profiles associated with tenderness and intramuscular fat content in pork. Meat Sci. 92:440-450. https://doi.org/10.1016/j.meatsci.2012.05.007
  25. Hausman, G. J., Dodson, M. V., Ajuwon, K., Azain, M., Barnes, K. M., Guan, L. L., Jiang, Z., Poulos, S. P., Sainz, R. D., Smith, S., Spurlock, M., Novakofski, J., Fernyhough, M. E. and Bergen, W. G. 2009. Board-invited review: the biology and regulation of preadipocytes and adipocytes in meat animals. J. Anim. Sci. 87:1218-1246. https://doi.org/10.2527/jas.2008-1427
  26. Holm, C., Belfrage, P. and Fredrikson, G. 1987. Immunological evidence for the presence of hormone-sensitive lipase in rat tissues other than adipose tissue. Biochem. Biophys. Res. Commun. 148:99-105. https://doi.org/10.1016/0006-291X(87)91081-3
  27. Holm, C., Belfrage, P., Osterlund, T., Davis, R. C., Schotz, M. C. and Langin, D. 1994. Hormone-sensitive lipase: structure, function, evolution and overproduction in insect cells using the baculovirus expression system. Protein Eng. 7:537-541. https://doi.org/10.1093/protein/7.4.537
  28. Hovenier, R., Kanis, E. and Verhoeven, J. A. 1993. Repeatability of taste panel tenderness scores and their relationships to objective pig meat quality traits. J. Anim. Sci. 71:2018-2025. https://doi.org/10.2527/1993.7182018x
  29. Jenkins, C. M., Mancuso, D. J., Yan, W., Sims, H. F., Gibson, B. and Gross, R. W. 2004. Identification, cloning, expression, and purification of three novel human calcium-independent phospholipase A2 family members possessing triacylglycerol lipase and acylglycerol transacylase activities. J. Biol. Chem. 279:48968-48975. https://doi.org/10.1074/jbc.M407841200
  30. Jeong, J., Kwon, E. G., Im, S. K., Seo, K. S. and Baik, M. 2012. Expression of fat deposition and fat removal genes is associated with intramuscular fat content in longissimus dorsi muscle of Korean cattle steers. J. Anim. Sci. 90:2044-20453. https://doi.org/10.2527/jas.2011-4753
  31. Jocken, J. W., Langin, D., Smit, E., Saris, W. H., Valle, C., Hul, G. B., Holm, C., Arner, P. and Blaak, E. E. 2007. Adipose triglyceride lipase and hormone-sensitive lipase protein expression is decreased in the obese insulin-resistant state. J. Clin. Endocrinol. Metab. 92:2292-2299. https://doi.org/10.1210/jc.2006-1318
  32. Karlsson, M., Contreras, J. A., Hellman, U., Tornqvist, H. and Holm, C. 1997. cDNA cloning, tissue distribution, and identification of the catalytic triad of monoglyceride lipase. Evolutionary relationship to esterases, lysophospholipases, and haloperoxidases. J. Biol. Chem. 272:27218-27223. https://doi.org/10.1074/jbc.272.43.27218
  33. Kershaw, E. E., Hamm, J. K., Verhagen, L. A., Peroni, O., Katic, M. and Flier, J. S. 2006. Adipose triglyceride lipase: function, regulation by insulin, and comparison with adiponutrin. Diabetes 55:148-157. https://doi.org/10.2337/diabetes.55.01.06.db05-0982
  34. Kim, J. Y., Tillison, K., Lee, J. H., Rearick, D. A. and Smas, C. M. 2006. The adipose tissue triglyceride lipase ATGL/PNPLA2 is downregulated by insulin and TNF-alpha in 3T3-L1 adipocytes and is a target for transactivation by PPARgamma. Am. J. Physiol. Endocrinol. Metab. 291:E115-127. https://doi.org/10.1152/ajpendo.00317.2005
  35. Kinnunen, P. K., Jackson, R. L., Smith, L. C., Gotto, A. M. Jr. and Sparrow, J. T. 1977. Activation of lipoprotein lipase by native and synthetic fragments of human plasma apolipoprotein C-II. Proc. Natl. Acad. Sci. USA. 74:4848-4851. https://doi.org/10.1073/pnas.74.11.4848
  36. Kraemer, F. B., Patel, S., Sadi, M. S. and Sztalryd, C. 1993. Detection of hormone-sensitive lipase in various tissues. I. Expression of an HSL/bacterial fusion protein and generation of anti-HSL antibodies. J. Lipid Res. 34:663-671.
  37. Kralisch, S., Klein, J., Lossner, U., Bluher, M., Paschke, R., Stumvoll, M. and Fasshauer, M. 2005. Isoproterenol, TNFalpha, and insulin downregulate adipose triglyceride lipase in 3T3-L1 adipocytes. Mol. Cell. Endocrinol. 240:43-49. https://doi.org/10.1016/j.mce.2005.06.002
  38. Labar, G. C., Bauvois, F. B., Ferrer, J. L., Wouters, J. and Lambert, D. M. 2010. Crystal structure of the human mono-acylglycerol lipase, a key actor in endocannabinoid signaling. Chembiochem. 11:218-227. https://doi.org/10.1002/cbic.200900621
  39. Lake, A. C., Sun, Y., Li, J. L., Johnson, J. W., Li, D., Revett, T., Shih, H. H., Liu, W., Paulsen, J. E. and Gimeno, R. E. 2005. Expression, regulation, and triglyceride hydrolase activity of Adiponutrin family members. J. Lipid Res. 46:2477-2487. https://doi.org/10.1194/jlr.M500290-JLR200
  40. Langin, D., Laurell, H., Holst, L. S., Belfrage, P. and Holm, C. 1993. Gene organization and primary structure of human hormone-sensitive lipase: possible significance of a sequence homology with a lipase of Moraxella TA144, an antartic bacterium. Proc. Natl. Acad. Sci. 90:4897-4901. https://doi.org/10.1073/pnas.90.11.4897
  41. Lass, A., Zimmermann, R., Oberer, M. and Zechner, R. 2011. Lipolysis- a highly regulated multi-enzyme complex mediates the catabolism of cellular fat stores. Prog. Lipid Res. 50:14-27. https://doi.org/10.1016/j.plipres.2010.10.004
  42. Lass, A., Zimmermann, R., Haemmerle, G., Riederer, M., Schoiswohl, G., Schweiger, M., Kienesberger, P., Strauss, J. G., Gokiewicz, G. and Zechner, R. 2006. Adipose triglyceride lipase-mediated lipolysis of cellular fat stores is activated by CGI-58 and defective in Chanarin-Dorfman Syndrome. Cell Metab. 3:309-319. https://doi.org/10.1016/j.cmet.2006.03.005
  43. Lau, D. C., Dhillon, B., Yan, H., Szmitko, P. E. and Verma, S. 2005. Adipokines: molecular links between obesity and atherosclerosis. Am. J. Physiol. Heart Circ. Physiol. 288(5):H2031-41. https://doi.org/10.1152/ajpheart.01058.2004
  44. Lee, S. H., Park, E. W., Cho, Y. M., Kim, S. K., Lee, J. H., Jeon, J. T., Lee, C. S., Im, S. K., Oh, S. J., Thompson, J. M. and Yoon, D. 2007. Identification of differentially expressed genes related to intramuscular fat development in the early and late fattening stages of hanwoo steers. J. Biochem. Mol. Biol. 40:757-764. https://doi.org/10.5483/BMBRep.2007.40.5.757
  45. Lee, K., Shin, J., Latshaw, J. D., Suh, Y. and Serr, J. 2009. Cloning of adipose triglyceride lipase in poultry and expression of adipose triglyceride lipase during development of adipose in chickens. Poult. Sci. 88:620-630. https://doi.org/10.3382/ps.2008-00265
  46. Lefevre, C., Jobard, F., Caux, F., Bouadjar, B., Karaduman, A., Heilig, R., Lakhdar, H., Wollenberg, A., Verret, J. L., Weissenbach, J., Ozguc, M., Lathrop, M., Prud'homme, J. F. and Fischer, J. 2001. Mutations in CGI-58, the gene encoding a new protein of the esterase/lipase/thioesterase subfamily, in Chanarin-Dorfman syndrome. Am. J. Hum. Genet. 69:1002-1012. https://doi.org/10.1086/324121
  47. Lefevre, C., Jobard, F., Caux, F., Bouadjar, B., Karaduman, A., Heilig, R., Lakhdar, H., Wollenberg, A.., Verret, J. L., Weissenbach, J., Ozguc, M., Lathrop, M., Prud'homme, J. F. and Fischer, J. 2001. Mutations in CGI-58, the gene encoding a new protein of the esterase/lipase/thioesterase subfamily, in Chanarin-Dorfman syndrome. Am. J. Hum. Genet. 69:1002-1012. https://doi.org/10.1086/324121
  48. Li, X., Suh, Y., Kim, B. R., Moeller, S. J. and Lee, K. 2012. Alternative splicing and developmental and hormonal regulation of porcine comparative gene identification-58 (CGI-58) mRNA. J. Anim. Sci. 90:4346-4354. https://doi.org/10.2527/jas.2012-5151
  49. Li, Y., Zheng, X. and Yang, G. 2008. Effects of leptin on porcine primary adipocytes lipolysis and mRNA expression of key lipolytic enzymes. Sheng Wu Gong Cheng Xue Bao. 24:1612-1619.
  50. Li, Y. C., Zheng, X. L., Liu, B. T. and Yang, G. S. 2010. Regulation of ATGL expression mediated by leptin in vitro in porcine adipocyte lipolysis. Mol. Cell Biochem. 333(1-2):121-8. https://doi.org/10.1007/s11010-009-0212-4
  51. Liu, L. F., Purushotham, A., Wendel, A. A., Koba, K., Deiuliis, J., Lee, K. and Belury, M. A. 2009. Regulation of adipose triglyceride lipase by rosiglitazone. Diabetes Obes. Metab. 11:131-142. https://doi.org/10.1111/j.1463-1326.2008.00916.x
  52. Lu, X., Yang, X. and Liu, J. 2010. Differential control of ATGL-mediated lipid droplet degradation by CGI-58 and G0S2. Cell Cycle. 9:2719-2725.
  53. McGarry, J. D. 2002. Banting lecture 2001: Dysregulation of fatty acid metabolism in the etiology of type 2 diabetes. Diabetes 51:7-18. https://doi.org/10.2337/diabetes.51.1.7
  54. Miyoshi, H., Perfield, J. W., Obin, M. S. and Greenberg, A. S. 2008. Adipose triglyceride lipase regulates basal lipolysis and lipid droplet size in adipocytes. J. Cell Biochem. 105:1430-1436. https://doi.org/10.1002/jcb.21964
  55. Miyoshi, H., Souza, S. C., Zhang, H. H., Strissel, K. J., Christoffolete, M. A., Kovsan, J., Rudich, A., Kraemer, F. B., Bianco, A. C., Obin, M. S. and Greenberg, A. S. 2006. Perilipin promotes hormone-sensitive lipase-mediated adipocyte lipolysis via phosphorylation-dependent and -independent mechanisms. J. Biol. Chem. 281:15837-15844. https://doi.org/10.1074/jbc.M601097200
  56. Montero-Moran, G., Caviglia, J. M., McMahon, D., Rothenberg, A., Subramanian, V., Xu, Z., Lara-Gonzalex, S., Storch, J., Carman, J. G. and Brasaemle, D. L. 2010. CGI-58/ABHD5 is a coenzyme A-dependent lysophosphatidic acid acyltransferase. J. Lipid Res. 51:709-719. https://doi.org/10.1194/jlr.M001917
  57. Mourot, J. and Kouba, M. 1998. Lipogenic enzyme activities in muscles of growing Large White and Meishan Pigs. Livest. Prod. Sci. 55:127-133 https://doi.org/10.1016/S0301-6226(98)00129-8
  58. Notari, L, Baladron, V., Aroca-Aguilar, J. D., Balko, N., Heredia, R., Meyer, C., Notario, P. M., Saravanamuthu, S., Nueda, M. L., Sanchez-Sanchez, F., Escribano, J., Laborda, J. and Becerra, S. P. 2006. Identification of a lipase-linked cell membrane receptor for pigment epithelium-derived factor. J. Biol. Chem. 281:38022-38037. https://doi.org/10.1074/jbc.M600353200
  59. Oh, S. A., Suh, Y., Pang, M. G. and Lee, K. 2010. Cloning of avian G(0)/G(1) switch gene 2 genes and developmental and nutritional regulation of G(0)/G(1) switch gene 2 in chicken adipose tissue. J. Anim. Sci. 89:367-375.
  60. Ollis, D. L., Cheah, E., Cygler, M., Dijkstra, B., Frolow, F., Franken, S. M., Harel, M., Remington, S. J., Silman, I. and Schrag, J. 1992. The alpha/beta hydrolase fold. Protein Eng. 5:197-211. https://doi.org/10.1093/protein/5.3.197
  61. Osterlund, T., Danielsson, B., Degerman, E., Contreras, J. A., Edgren, G., Davis, R. C., Schotz, M. C. and Holm, C. 1996. Domain-structure analysis of recombinant rat hormone-sensitive lipase. Biochem. J. 319:411-420. https://doi.org/10.1042/bj3190411
  62. Pagnon, J., Matzaris, M., Stark, R., Meex, R. C., Lance Macaulay, S., Brown, W., O'Brien, P. E., Tiganis, T. and Watt, M. J. 2012. Identification and Functional Characterization of Protein Kinase A Phosphorylation Sites in the Major Lipolytic Protein, Adipose Triglyceride Lipase. Endocrinology 153:4278-4289. https://doi.org/10.1210/en.2012-1127
  63. Pethick, D. W., Harper, G. S., Oddy, V. H. 2004. Growth, development and nutritional manipulation of marbling in cattle: a review. Aust. J. Exp.Agric. 44:705-715. https://doi.org/10.1071/EA02165
  64. Peyot, M. L., Guay, C., Latour, M. G., Lamontagne, J., Lussier, R., Pineda, M., Ruderman, N. B., Haemmerle, G., Zechner, R., Joly, E., Madiraju, S. R., Poitout, V. and Prentki, M. 2009. Adipose triglyceride lipase is implicated in fuel- and non-fuel-stimulated insulin secretion. J. Biol. Chem. 284:16848-16859. https://doi.org/10.1074/jbc.M109.006650
  65. Radner, F. P., Grond, S., Haemmerle, G., Lass, A. and Zechner, R. 2011. Fat in the skin: Triacylglycerol metabolism in keratinocytes and its role in the development of neutral lipid storage disease. Dermatoendocrinol. 3:77-83. https://doi.org/10.4161/derm.3.2.15472
  66. Russell, L. and Forsdyke, D. R. 1991. A human putative lymphocyte G0/G1 switch gene containing a CpG-rich island encodes a small basic protein with the potential to be phosphorylated. DNA Cell Biol. 10:581-591. https://doi.org/10.1089/dna.1991.10.581
  67. Schlosburg, J. E., Blankman, J. L., Long, J. Z., Nomura, D. K., Pan, B., Kinsey, S. G., Nguyen, P. T., Ramesh, D., Booker, L., Burston, J. J., Thomas, E. A., Selley, D. E., Sim-Selley, L. J., Liu, Q. S., Lichtman, A. H. and Cravatt, B. F. 2010. Chronic monoacylglycerol lipase blockade causes functional antagonism of the endocannabinoid system. Nat. Neurosci. 13:1113-1119. https://doi.org/10.1038/nn.2616
  68. Schweiger, M., Lass, A., Zimmermann, R., Eichmann, T. O. and Zechner, R. 2009. Neutral lipid storage disease: genetic disorders caused by mutations in adipose triglyceride lipase/PNPLA2 or CGI-58/ABHD5. Am. J. Physiol. Endocrinol. Metab. 297:E289-296. https://doi.org/10.1152/ajpendo.00099.2009
  69. Schweiger, M., Schoiswohl, G., Lass, A., Radner, F. P., Haemmerle, G., Malli, R., Graier, W., Cornaciu, I., Oberer, M., Salvayre, R., Fischer, J., Zechner, R. and Zimmermann, R. 2008. The C-terminal region of human adipose triglyceride lipase affects enzyme activity and lipid droplet binding. J. Biol. Chem. 283:17211-17220. https://doi.org/10.1074/jbc.M710566200
  70. Serr, J., Suh, Y. and Lee, K. 2009. Regulation of adipose triglyceride lipase by fasting and refeeding in avian species. Poult. Sci. 88:2585-2591. https://doi.org/10.3382/ps.2009-00265
  71. Serr, J., Suh, Y. and Lee, K. 2011. Cloning of comparative gene identification-58 gene in avian species and investigation of its developmental and nutritional regulation in chicken adipose tissue. J. Anim. Sci. 89:3490-3500. https://doi.org/10.2527/jas.2011-3897
  72. Shan, T., Wu, T., Reng, Y. and Wang, Y. 2009. Breed difference and regulation of the porcine adipose triglyceride lipase and hormone sensitive lipase by TNFalpha. Anim. Genet. 40:863-870. https://doi.org/10.1111/j.1365-2052.2009.01927.x
  73. Shen, W. J., Liang, Y., Hong, R., Patel, S., Natu, V., Sridhar, K., Jenkins, A., Bernlohr, D. A. and Kraemer, F. B. 2001. Characterization of the functional interaction of adipocyte lipid-binding protein with hormone-sensitive lipase. J. Biol. Chem. 376:49443-49448.
  74. Smekal, G., von Duvillard, S. P., Pokan, R., Tschan, H., Baron, R., Hofmann, P., Wonisch, M. and Bachl, N. 2003. Effect of endurance training on muscle fat metabolism during prolonged exercise: agreements and disagreements. Nutrition 19:891-900. https://doi.org/10.1016/S0899-9007(03)00171-0
  75. Subramanian, V., Rothenberg, A., Gomez, C., Cohen, A. W., Garcia, A., Bhattacharyya, S., Shapiro, L., Dolios, G., Wang, R., Lisanti, M. P. and Brasaemle, D. L. 2004. Perilipin A mediates the reversible binding of CGI-58 to lipid droplets in 3T3-L1 adipocytes. J. Biol. Chem. 279:42062-42071. https://doi.org/10.1074/jbc.M407462200
  76. Tornqvist, H. and Belfrage, P. 1976. Determination of protein in adipose tissue extracts. FEBS Lett. 75:259-264.
  77. Vaughan, M., Berger, J. E. and Steinberg, D. 1964. Hormone-sensitive lipase and monoglyceride lipase activities in adipose tissue. J. Biol. Chem. 239:401-409.
  78. Villena, J. A., Roy, S., Sarkadi-Nagy, E., Kim, K. H. and Sul, H. S. 2004. Desnutrin, an adipocyte gene encoding a novel patatin domain-containing protein, is induced by fasting and glucocorticoids: ectopic expression of desnutrin increases triglyceride hydrolysis. J. Biol. Chem. 279:47066-47075. https://doi.org/10.1074/jbc.M403855200
  79. Waki, H. and Tontonoz, P. 2007. Endocrine functions of adipose tissue. Annu. Rev. Pathol. 2:31-56. https://doi.org/10.1146/annurev.pathol.2.010506.091859
  80. Watt, M. J. and Steinberg, G. R. 2008. Regulation and function of triacylglycerol lipases in cellular metabolism. Biochem. J. 414:313-325. https://doi.org/10.1042/BJ20080305
  81. Xu, C., Jinhan, H., Jiang, H., Zu, L., Zhai, W., Pu, S. and Xu, G. 2009. Direct effect of glucocorticoids on lipolysis in adipocytes. Mol. Endocrinol. 23:1161-1170. https://doi.org/10.1210/me.2008-0464
  82. Yamaguchi, T., Omatsu, N., Matsushita, S. and Osumi, T. 2004. CGI-58 interacts with perilipin and is localized to lipid droplets. Possible involvement of CGI-58 mislocalization in Chanarin-Dorfman syndrome. J. Biol. Chem. 279:30490-30497. https://doi.org/10.1074/jbc.M403920200
  83. Yang, X., Lu, X. and Liu, J. 2010a. Identification of a novel splicing isoform of murine CGI-58. FEBS Lett. 584:903-910. https://doi.org/10.1016/j.febslet.2009.12.058
  84. Yang, X., Lu, X., Lombes, M., Rha, G. B., Chi, Y. I., Guerin, T. M., Smart, E. J. and Liu, J. 2010b. The G(0)/G(1) switch gene 2 regulates adipose lipolysis through association with adipose triglyceride lipase. Cell Metab. 11:194-205. https://doi.org/10.1016/j.cmet.2010.02.003
  85. Zandenbergen, F., Madard, S., Escher, P., Tan, N. S., Patsouris, D., Jatkoe, T., Rojas-Caro, S., Madore, S., Wahli, W., Tafuri, S., Muller, M. and Kersten, S. 2005. The G0/G1 switch gene 2 is a novel PPAR target gene. Biochem. 392:313-24. https://doi.org/10.1042/BJ20050636
  86. Zechner, R., Strauss, J. G., Haemmerle, G., Lass, A. and Zimmermann, R. 2005. Lipolysis: pathway under construction. Curr. Opin. Lipidol. 16:333-340. https://doi.org/10.1097/01.mol.0000169354.20395.1c
  87. Zhang, Y., Proenca, R., Maffei, M., Barone, M., Leopold, L. and Friedman, J. M. 1994. Positional cloning of the mouse obese gene and its human homologue. Nature 372:425-432. https://doi.org/10.1038/372425a0
  88. Zhao, S. M., Ren, L. J., Chen, L., Zhang, X., Cheng, M. L., Li, W. Z., Zhang, Y. Y. and Gao, S. Z. 2009. Differential expression of lipid metabolism related genes in porcine muscle tissue leading to different intramuscular fat deposition. Lipids 44:1029-1037. https://doi.org/10.1007/s11745-009-3356-9
  89. Zimmermann, R., Strauss, J. G., Haemmerle, G., Schoiswohl, G., Birner-Gruenberger, R., Riederer, M., Lass, A., Neuberger, G., Eisenhaber, F., Hermetter, A. and Zechner, R. 2004. Fat mobilization in adipose tissue is promoted by adipose triglyceride lipase. Science 306:1383-1386. https://doi.org/10.1126/science.1100747

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