G0S2: A small giant controller of lipolysis and adipose-liver fatty acid flux

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1862, Issue 10, 2017, Pages 1146-1154

  Zhang, Xiaodong ^a,b   Heckmann, Bradlee L ^c   Campbell, Latoya E ^d   Liu, Jun ^a,b  

^a MAYO GRADUATE SCHOOL   (United States)

^b MAYO CLINIC   (United States)

^c ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^d ARIZONA STATE UNIVERSITY   (United States)

Author keywords

ATGL; Fatty acid; G0S2; Lipid droplet; Lipolysis; Triglyceride

Indexed keywords

ADIPOSE TRIGLYCERIDE LIPASE; G0 G1 SWITCH 2 PROTEIN; PROTEIN; TRIACYLGLYCEROL; TRIACYLGLYCEROL LIPASE; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; FAT DROPLET; FATTY ACID; G0S2 PROTEIN, HUMAN; PNPLA2 PROTEIN, HUMAN;

ADIPOSE LIVER FATTY ACID FLUX; ADIPOSE TISSUE; DIABETIC KETOACIDOSIS; ENERGY; ENERGY METABOLISM; FATTY ACID METABOLISM; FATTY LIVER; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LIPID STORAGE; LIPOLYSIS; MUSCLE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; REVIEW; ANIMAL; ANTIBODY SPECIFICITY; GENETICS; LIVER; METABOLISM; PHYSIOLOGY;

ADIPOSE TISSUE; ANIMALS; CELL CYCLE PROTEINS; ENERGY METABOLISM; FATTY ACIDS; HUMANS; LIPASE; LIPID DROPLETS; LIPOLYSIS; LIVER; ORGAN SPECIFICITY; TRIGLYCERIDES;

EID: 85021711908     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2017.06.007     Document Type: Review

References (122)

1. van den Berghe, G., The role of the liver in metabolic homeostasis: implications for inborn errors of metabolism. J. Inherit. Metab. Dis. 14 (1991), 407–420.
2. Cohen, J.C., Horton, J.D., Hobbs, H.H., Human fatty liver disease: old questions and new insights. Science 332 (2011), 1519–1523.
3. Lin, X., Yue, P., Chen, Z., Schonfeld, G., Hepatic triglyceride contents are genetically determined in mice: results of a strain survey. Am. J. Physiol. Gastrointest. Liver Physiol. 288 (2005), G1179–G1189.
4. Guan, H.P., Goldstein, J.L., Brown, M.S., Liang, G., Accelerated fatty acid oxidation in muscle averts fasting-induced hepatic steatosis in SJL/J mice. J. Biol. Chem. 284 (2009), 24644–24652.
5. Nishikawa, S., Doi, K., Nakayama, H., Uetsuka, K., The effect of fasting on hepatic lipid accumulation and transcriptional regulation of lipid metabolism differs between C57BL/6J and BALB/cA mice fed a high-fat diet. Toxicol. Pathol. 36 (2008), 850–857.
6. Lin, E.C., Glycerol utilization and its regulation in mammals. Annu. Rev. Biochem. 46 (1977), 765–795.
7. Malhi, H., Gores, G.J., Molecular mechanisms of lipotoxicity in nonalcoholic fatty liver disease. Semin. Liver Dis. 28 (2008), 360–369.
8. Jensen, M.D., Role of body fat distribution and the metabolic complications of obesity. J. Clin. Endocrinol. Metab. 93 (2008), S57–S63.
9. Petta, S., Gastaldelli, A., Rebelos, E., Bugianesi, E., Messa, P., Miele, L., Svegliati-Baroni, G., Valenti, L., Bonino, F., Pathophysiology of non alcoholic fatty liver disease. Int. J. Mol. Sci., 17, 2016.
10. Mashek, D.G., Khan, S.A., Sathyanarayan, A., Ploeger, J.M., Franklin, M.P., Hepatic lipid droplet biology: getting to the root of fatty liver. Hepatology 62 (2015), 964–967.
11. Ueno, T., Komatsu, M., Autophagy in the liver: functions in health and disease. Nat. Rev. Gastroenterol. Hepatol. 14 (2017), 170–184.
12. Cingolani, F., Czaja, M.J., Regulation and functions of autophagic lipolysis. Trends Endocrinol. Metab. 27 (2016), 696–705.
13. Samuel, V.T., Shulman, G.I., The pathogenesis of insulin resistance: integrating signaling pathways and substrate flux. J. Clin. Invest. 126 (2016), 12–22.
14. Glass, C.K., Olefsky, J.M., Inflammation and lipid signaling in the etiology of insulin resistance. Cell Metab. 15 (2012), 635–645.
15. Zechner, R., Kienesberger, P.C., Haemmerle, G., Zimmermann, R., Lass, A., Adipose triglyceride lipase and the lipolytic catabolism of cellular fat stores. J. Lipid Res. 50 (2009), 3–21.
16. Zechner, R., Zimmermann, R., Eichmann, T.O., Kohlwein, S.D., Haemmerle, G., Lass, A., Madeo, F., FAT SIGNALS—lipases and lipolysis in lipid metabolism and signaling. Cell Metab. 15 (2012), 279–291.
17. Yang, X., Lu, X., Lombes, M., Rha, G.B., Chi, Y.I., Guerin, T.M., Smart, E.J., Liu, J., The G(0)/G(1) switch gene 2 regulates adipose lipolysis through association with adipose triglyceride lipase. Cell Metab. 11 (2010), 194–205.
18. Girousse, A., Langin, D., Adipocyte lipases and lipid droplet-associated proteins: insight from transgenic mouse models. Int. J. Obes. 36 (2012), 581–594.
19. Jenkins, C.M., Mancuso, D.J., Yan, W., Sims, H.F., Gibson, B., Gross, R.W., 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 (2004), 48968–48975.
20. Villena, J.A., Roy, S., Sarkadi-Nagy, E., Kim, K.H., Sul, H.S., 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 (2004), 47066–47075.
21. Zimmermann, R., Strauss, J.G., Haemmerle, G., Schoiswohl, G., Birner-Gruenberger, R., Riederer, M., Lass, A., Neuberger, G., Eisenhaber, F., Hermetter, A., Zechner, R., Fat mobilization in adipose tissue is promoted by adipose triglyceride lipase. Science 306 (2004), 1383–1386.
22. Lass, A., Zimmermann, R., Haemmerle, G., Riederer, M., Schoiswohl, G., Schweiger, M., Kienesberger, P., Strauss, J.G., Gorkiewicz, G., Zechner, R., Adipose triglyceride lipase-mediated lipolysis of cellular fat stores is activated by CGI-58 and defective in Chanarin-Dorfman Syndrome. Cell Metab. 3 (2006), 309–319.
23. Schweiger, M., Lass, A., Zimmermann, R., Eichmann, T.O., Zechner, R., Neutral lipid storage disease: genetic disorders caused by mutations in adipose triglyceride lipase/PNPLA2 or CGI-58/ABHD5. Am. J. Physiol. Endocrinol. Metab. 297 (2009), E289–E296.
24. Haemmerle, G., Lass, A., Zimmermann, R., Gorkiewicz, G., Meyer, C., Rozman, J., Heldmaier, G., Maier, R., Theussl, C., Eder, S., Kratky, D., Wagner, E.F., Klingenspor, M., Hoefler, G., Zechner, R., Defective lipolysis and altered energy metabolism in mice lacking adipose triglyceride lipase. Science 312 (2006), 734–737.
25. Ahmadian, M., Abbott, M.J., Tang, T., Hudak, C.S., Kim, Y., Bruss, M., Hellerstein, M.K., Lee, H.Y., Samuel, V.T., Shulman, G.I., Wang, Y., Duncan, R.E., Kang, C., Sul, H.S., Desnutrin/ATGL is regulated by AMPK and is required for a brown adipose phenotype. Cell Metab. 13 (2011), 739–748.
26. Kienesberger, P.C., Lee, D., Pulinilkunnil, T., Brenner, D.S., Cai, L., Magnes, C., Koefeler, H.C., Streith, I.E., Rechberger, G.N., Haemmerle, G., Flier, J.S., Zechner, R., Kim, Y.B., Kershaw, E.E., Adipose triglyceride lipase (ATGL) deficiency causes tissue-specific changes in insulin signaling. J. Biol. Chem., 2009.
27. Schoiswohl, G., Stefanovic-Racic, M., Menke, M.N., Wills, R.C., Surlow, B.A., Basantani, M.K., Sitnick, M.T., Cai, L., Yazbeck, C.F., Stolz, D.B., Pulinilkunnil, T., O'Doherty, R.M., Kershaw, E.E., Impact of reduced ATGL-mediated adipocyte lipolysis on obesity-associated insulin resistance and inflammation in male mice. Endocrinology 156 (2015), 3610–3624.
28. Wu, J.W., Wang, S.P., Alvarez, F., Casavant, S., Gauthier, N., Abed, L., Soni, K.G., Yang, G., Mitchell, G.A., Deficiency of liver adipose triglyceride lipase in mice causes progressive hepatic steatosis. Hepatology 54 (2011), 122–132.
29. Ong, K.T., Mashek, M.T., Bu, S.Y., Greenberg, A.S., Mashek, D.G., Adipose triglyceride lipase is a major hepatic lipase that regulates triacylglycerol turnover and fatty acid signaling and partitioning. Hepatology 53 (2011), 116–126.
30. Haemmerle, G., Moustafa, T., Woelkart, G., Buttner, S., Schmidt, A., van de Weijer, T., Hesselink, M., Jaeger, D., Kienesberger, P.C., Zierler, K., Schreiber, R., Eichmann, T., Kolb, D., Kotzbeck, P., Schweiger, M., Kumari, M., Eder, S., Schoiswohl, G., Wongsiriroj, N., Pollak, N.M., Radner, F.P., Preiss-Landl, K., Kolbe, T., Rulicke, T., Pieske, B., Trauner, M., Lass, A., Zimmermann, R., Hoefler, G., Cinti, S., Kershaw, E.E., Schrauwen, P., Madeo, F., Mayer, B., Zechner, R., ATGL-mediated fat catabolism regulates cardiac mitochondrial function via PPAR-alpha and PGC-1. Nat. Med. 17 (2011), 1076–1085.
31. Jha, P., Claudel, T., Baghdasaryan, A., Mueller, M., Halilbasic, E., Das, S.K., Lass, A., Zimmermann, R., Zechner, R., Hoefler, G., Trauner, M., Role of adipose triglyceride lipase (PNPLA2) in protection from hepatic inflammation in mouse models of steatohepatitis and endotoxemia. Hepatology 59 (2014), 858–869.
32. Reid, B.N., Ables, G.P., Otlivanchik, O.A., Schoiswohl, G., Zechner, R., Blaner, W.S., Goldberg, I.J., Schwabe, R.F., Chua, S.C. Jr., Huang, L.S., Hepatic overexpression of hormone-sensitive lipase and adipose triglyceride lipase promotes fatty acid oxidation, stimulates direct release of free fatty acids, and ameliorates steatosis. J. Biol. Chem. 283 (2008), 13087–13099.
33. Fischer, J., Lefevre, C., Morava, E., Mussini, J.M., Laforet, P., Negre-Salvayre, A., Lathrop, M., Salvayre, R., The gene encoding adipose triglyceride lipase (PNPLA2) is mutated in neutral lipid storage disease with myopathy. Nat. Genet. 39 (2007), 28–30.
34. Schreiber, R., Hofer, P., Taschler, U., Voshol, P.J., Rechberger, G.N., Kotzbeck, P., Jaeger, D., Preiss-Landl, K., Lord, C.C., Brown, J.M., Haemmerle, G., Zimmermann, R., Vidal-Puig, A., Zechner, R., Hypophagia and metabolic adaptations in mice with defective ATGL-mediated lipolysis cause resistance to HFD-induced obesity. Proc. Natl. Acad. Sci. U. S. A. 112 (2015), 13850–13855.
35. Russell, L., Forsdyke, D.R., 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 (1991), 581–591.
36. Siderovski, D.P., Blum, S., Forsdyke, R.E., Forsdyke, D.R., A set of human putative lymphocyte G0/G1 switch genes includes genes homologous to rodent cytokine and zinc finger protein-encoding genes. DNA Cell Biol. 9 (1990), 579–587.
37. Heckmann, B.L., Zhang, X., Xie, X., Liu, J., The G0/G1 switch gene 2 (G0S2): regulating metabolism and beyond. Biochim. Biophys. Acta 1831 (2013), 276–281.
38. Kioka, H., Kato, H., Fujikawa, M., Tsukamoto, O., Suzuki, T., Imamura, H., Nakano, A., Higo, S., Yamazaki, S., Matsuzaki, T., Takafuji, K., Asanuma, H., Asakura, M., Minamino, T., Shintani, Y., Yoshida, M., Noji, H., Kitakaze, M., Komuro, I., Asano, Y., Takashima, S., Evaluation of intramitochondrial ATP levels identifies G0/G1 switch gene 2 as a positive regulator of oxidative phosphorylation. Proc. Natl. Acad. Sci. U. S. A. 111 (2014), 273–278.
39. Yim, C.Y., Sekula, D.J., Hever-Jardine, M.P., Liu, X., Warzecha, J.M., Tam, J., Freemantle, S.J., Dmitrovsky, E., Spinella, M.J., G0S2 suppresses oncogenic transformation by repressing a MYC-regulated transcriptional program. Cancer Res. 76 (2016), 1204–1213.
40. Wang, Y., Zhang, Y., Zhu, Y., Zhang, P., Lipolytic inhibitor G0/G1 switch gene 2 inhibits reactive oxygen species production and apoptosis in endothelial cells. Am. J. Physiol. Cell Physiol. 308 (2015), C496–C504.
41. Matsunaga, N., Ikeda, E., Kakimoto, K., Watanabe, M., Shindo, N., Tsuruta, A., Ikeyama, H., Hamamura, K., Higashi, K., Yamashita, T., Kondo, H., Yoshida, Y., Matsuda, M., Ogino, T., Tokushige, K., Itcho, K., Furuichi, Y., Nakao, T., Yasuda, K., Doi, A., Amamoto, T., Aramaki, H., Tsuda, M., Inoue, K., Ojida, A., Koyanagi, S., Ohdo, S., Inhibition of G0/G1 switch 2 ameliorates renal inflammation in chronic kidney disease. EBioMedicine 13 (2016), 262–273.
42. Zagani, R., El-Assaad, W., Gamache, I., Teodoro, J.G., Inhibition of adipose triglyceride lipase (ATGL) by the putative tumor suppressor G0S2 or a small molecule inhibitor attenuates the growth of cancer cells. Oncotarget 6 (2015), 28282–28295.
43. Yamada, T., Park, C.S., Shen, Y., Rabin, K.R., Lacorazza, H.D., G0S2 inhibits the proliferation of K562 cells by interacting with nucleolin in the cytosol. Leuk. Res. 38 (2014), 210–217.
44. 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., Oberer, M., 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, 2011, e26349.
45. Yang, X., Lu, X., Lombes, M., Rha, G.B., Chi, Y.I., Guerin, T.M., Smart, E.J., Liu, J., The G(0)/G(1) switch gene 2 regulates adipose lipolysis through association with adipose triglyceride lipase. Cell Metab. 11 (2010), 194–205.
46. Lu, X., Yang, X., Liu, J., Differential control of ATGL-mediated lipid droplet degradation by CGI-58 and G0S2. Cell Cycle 9 (2010), 2719–2725.
47. Cerk, I.K., Salzburger, B., Boeszoermenyi, A., Heier, C., Pillip, C., Romauch, M., Schweiger, M., Cornaciu, I., Lass, A., Zimmermann, R., Zechner, R., Oberer, M., A peptide derived from G0/G1 switch gene 2 acts as non-competitive inhibitor of adipose triglyceride lipase. J. Biol. Chem., 2014.
48. Granneman, J.G., Moore, H.P., Granneman, R.L., Greenberg, A.S., Obin, M.S., Zhu, Z., Analysis of lipolytic protein trafficking and interactions in adipocytes. J. Biol. Chem. 282 (2007), 5726–5735.
49. Granneman, J.G., Moore, H.P., Krishnamoorthy, R., Rathod, M., Perilipin controls lipolysis by regulating the interactions of AB-hydrolase containing 5 (Abhd5) and adipose triglyceride lipase (Atgl). J. Biol. Chem. 284 (2009), 34538–34544.
50. Pagnon, J., Matzaris, M., Stark, R., Meex, R.C., Macaulay, S.L., Brown, W., O'Brien, P.E., Tiganis, T., Watt, M.J., Identification and functional characterization of protein kinase A phosphorylation sites in the major lipolytic protein, adipose triglyceride lipase. Endocrinology 153 (2012), 4278–4289.
51. Schweiger, M., Paar, M., Eder, C., Brandis, J., Moser, E., Gorkiewicz, G., Grond, S., Radner, F.P., Cerk, I., Cornaciu, I., Oberer, M., Kersten, S., Zechner, R., Zimmermann, R., Lass, A., G0/G1 switch gene-2 regulates human adipocyte lipolysis by affecting activity and localization of adipose triglyceride lipase. J. Lipid Res. 53 (2012), 2307–2317.
52. Yang, X., Heckmann, B.L., Zhang, X., Smas, C.M., Liu, J., Distinct mechanisms regulate ATGL-mediated adipocyte lipolysis by lipid droplet coat proteins. Mol. Endocrinol. 27 (2013), 116–126.
53. Cawthorn, W.P., Sethi, J.K., TNF-alpha and adipocyte biology. FEBS Lett. 582 (2008), 117–131.
54. Chen, X., Xun, K., Chen, L., Wang, Y., TNF-alpha, a potent lipid metabolism regulator. Cell Biochem. Funct. 27 (2009), 407–416.
55. Uysal, K.T., Wiesbrock, S.M., Marino, M.W., Hotamisligil, G.S., Protection from obesity-induced insulin resistance in mice lacking TNF-alpha function. Nature 389 (1997), 610–614.
56. Yang, X., Zhang, X., Heckmann, B.L., Lu, X., Liu, J., Relative contribution of adipose triglyceride lipase and hormone-sensitive lipase to tumor necrosis factor-alpha (TNF-alpha)-induced lipolysis in adipocytes. J. Biol. Chem. 286 (2011), 40477–40485.
57. Zhang, X., Xie, X., Heckmann, B.L., Saarinen, A.M., Czyzyk, T.A., Liu, J., Targeted disruption of g0/g1 switch gene 2 enhances adipose lipolysis, alters hepatic energy balance, and alleviates high-fat diet-induced liver steatosis. Diabetes 63 (2014), 934–946.
58. Ma, T., Lopez-Aguiar, A.G., Li, A., Lu, Y., Sekula, D., Nattie, E.E., Freemantle, S., Dmitrovsky, E., Mice lacking G0S2 are lean and cold-tolerant. Cancer Biol. Ther., 15, 2014.
59. El-Assaad, W., El-Kouhen, K., Mohammad, A.H., Yang, J., Morita, M., Gamache, I., Mamer, O., Avizonis, D., Hermance, N., Kersten, S., Tremblay, M.L., Kelliher, M.A., Teodoro, J.G., Deletion of the gene encoding G0/G1 switch protein 2 (G0s2) alleviates high-fat-diet-induced weight gain and insulin resistance, and promotes browning of white adipose tissue in mice. Diabetologia 58 (2015), 149–157.
60. Choi, H., Lee, H., Kim, T.H., Kim, H.J., Lee, Y.J., Lee, S.J., Yu, J.H., Kim, D., Kim, K.S., Park, S.W., Kim, J.W., G0/G1 switch gene 2 has a critical role in adipocyte differentiation. Cell Death Differ. 21 (2014), 1071–1080.
61. Heckmann, B.L., Zhang, X., Xie, X., Saarinen, A., Lu, X., Yang, X., Liu, J., Defective adipose lipolysis and altered global energy metabolism in mice with adipose overexpression of the lipolytic inhibitor G0/G1 switch gene 2 (G0S2). J. Biol. Chem. 289 (2014), 1905–1916.
62. Shin, S., Choi, Y.M., Han, J.Y., Lee, K., Inhibition of lipolysis in the novel transgenic quail model overexpressing G0/G1 switch gene 2 in the adipose tissue during feed restriction. PLoS One, 9, 2014, e100905.
63. Wang, Y., Zhang, Y., Qian, H., Lu, J., Zhang, Z., Min, X., Lang, M., Yang, H., Wang, N., Zhang, P., The g0/g1 switch gene 2 is an important regulator of hepatic triglyceride metabolism. PLoS One, 8, 2013, e72315.
64. Sugaya, Y., Satoh, H., Liver-specific G0/G1 switch gene 2 (G0s2) expression promotes hepatic insulin resistance by exacerbating hepatic steatosis in male Wistar rats. J. Diabetes, 2016.
65. Heier, C., Radner, F.P., Moustafa, T., Schreiber, R., Grond, S., Eichmann, T.O., Schweiger, M., Schmidt, A., Cerk, I.K., Oberer, M., Theussl, H.C., Wojciechowski, J., Penninger, J.M., Zimmermann, R., Zechner, R., G0/G1 switch gene 2 regulates cardiac lipolysis. J. Biol. Chem. 290 (2015), 26141–26150.
66. Chen, P.R., Shin, S., Choi, Y.M., Kim, E., Han, J.Y., Lee, K., Overexpression of G0/G1 switch gene 2 in adipose tissue of transgenic quail inhibits lipolysis associated with egg laying. Int. J. Mol. Sci., 17, 2016, 384.
67. Jessen, N., Nielsen, T.S., Vendelbo, M.H., Viggers, R., Stoen, O.G., Evans, A., Frobert, O., Pronounced expression of the lipolytic inhibitor G0/G1 Switch Gene 2 (G0S2) in adipose tissue from brown bears (Ursus arctos) prior to hibernation. Phys. Rep., 4, 2016.
68. Laurens, C., Badin, P.M., Louche, K., Mairal, A., Tavernier, G., Marette, A., Tremblay, A., Weisnagel, S.J., Joanisse, D.R., Langin, D., Bourlier, V., Moro, C., G0/G1 Switch Gene 2 controls adipose triglyceride lipase activity and lipid metabolism in skeletal muscle. Mol. Metab. 5 (2016), 527–537.
69. Turnbull, P.C., Longo, A.B., Ramos, S.V., Roy, B.D., Ward, W.E., Peters, S.J., Increases in skeletal muscle ATGL and its inhibitor G0S2 following 8 weeks of endurance training in metabolically different rat skeletal muscles. Am. J. Physiol. Regul. Integr. Comp. Physiol. 310 (2016), R125–R133.
70. Bachner, D., Ahrens, M., Schroder, D., Hoffmann, A., Lauber, J., Betat, N., Steinert, P., Flohe, L., Gross, G., Bmp-2 downstream targets in mesenchymal development identified by subtractive cloning from recombinant mesenchymal progenitors (C3H10T1/2). Dev. Dyn. 213 (1998), 398–411.
71. Zandbergen, F., Mandard, S., Escher, P., Tan, N.S., Patsouris, D., Jatkoe, T., Rojas-Caro, S., Madore, S., Wahli, W., Tafuri, S., Muller, M., Kersten, S., The G0/G1 switch gene 2 is a novel PPAR target gene. Biochem. J. 392 (2005), 313–324.
72. Oh, S.A., Suh, Y., Pang, M.G., Lee, K., 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 (2011), 367–375.
73. Zeng, F., Xie, L., Pang, X., Liu, W., Nie, Q., Zhang, X., Complementary deoxyribonucleic acid cloning of avian G0/G1 switch gene 2, and its expression and association with production traits in chicken. Poult. Sci. 90 (2011), 1548–1554.
74. Schweiger, M., Paar, M., Eder, C., Brandis, J., Moser, E., Gorkiewicz, G., Grond, S., Radner, F.P., Cerk, I., Cornaciu, I., Oberer, M., Kersten, S., Zechner, R., Zimmermann, R., Lass, A., G0/G1 switch gene-2 regulates human adipocyte lipolysis by affecting activity and localization of adipose triglyceride lipase. J. Lipid Res., 2012.
75. Ahn, J., Li, X., Choi, Y.M., Shin, S., Oh, S.A., Suh, Y., Nguyen, T.H., Baik, M., Hwang, S., Lee, K., Differential expressions of G0/G1 switch gene 2 and comparative gene identification-58 are associated with fat content in bovine muscle. Lipids 49 (2014), 1–14.
76. Skopp, A., May, M., Janke, J., Kielstein, H., Wunder, R., Flade-Kuthe, R., Kuthe, A., Jordan, J., Engeli, S., Regulation of G0/G1 switch gene 2 (G0S2) expression in human adipose tissue. Arch. Physiol. Biochem. 122 (2016), 47–53.
77. Nielsen, T.S., Vendelbo, M.H., Jessen, N., Pedersen, S.B., Jorgensen, J.O., Lund, S., Moller, N., Fasting, but not exercise, increases adipose triglyceride lipase (ATGL) protein and reduces G(0)/G(1) switch gene 2 (G0S2) protein and mRNA content in human adipose tissue. J. Clin. Endocrinol. Metab. 96 (2011), E1293–E1297.
78. Heckmann, B.L., Zhang, X., Saarinen, A.M., Liu, J., Regulation of G0/G1 switch gene 2 (G0S2) protein ubiquitination and stability by triglyceride accumulation and ATGL interaction. PLoS One, 11, 2016, e0156742.
79. Jaeger, D., Schoiswohl, G., Hofer, P., Schreiber, R., Schweiger, M., Eichmann, T.O., Pollak, N.M., Poecher, N., Grabner, G.F., Zierler, K.A., Eder, S., Kolb, D., Radner, F.P., Preiss-Landl, K., Lass, A., Zechner, R., Kershaw, E.E., Haemmerle, G., Fasting-induced G0/G1 switch gene 2 and FGF21 expression in the liver are under regulation of adipose tissue derived fatty acids. J. Hepatol., 2015.
80. Heckmann, B.L., Zhang, X., Saarinen, A.M., Schoiswohl, G., Kershaw, E.E., Zechner, R., Liu, J., Liver X receptor alpha mediates hepatic triglyceride accumulation through upregulation of G0/G1 Switch Gene 2 expression. JCI Insight, 2, 2017, e88735.
81. Ma, L., Robinson, L.N., Towle, H.C., ChREBP*Mlx is the principal mediator of glucose-induced gene expression in the liver. J. Biol. Chem. 281 (2006), 28721–28730.
82. Hong, C., Tontonoz, P., Liver X receptors in lipid metabolism: opportunities for drug discovery. Nat. Rev. Drug Discov. 13 (2014), 433–444.
83. Ducheix, S., Montagner, A., Theodorou, V., Ferrier, L., Guillou, H., The liver X receptor: a master regulator of the gut-liver axis and a target for non alcoholic fatty liver disease. Biochem. Pharmacol. 86 (2013), 96–105.
84. Oosterveer, M.H., van Dijk, T.H., Grefhorst, A., Bloks, V.W., Havinga, R., Kuipers, F., Reijngoud, D.J., Lxralpha deficiency hampers the hepatic adaptive response to fasting in mice. J. Biol. Chem. 283 (2008), 25437–25445.
85. Repa, J.J., Liang, G., Ou, J., Bashmakov, Y., Lobaccaro, J.M., Shimomura, I., Shan, B., Brown, M.S., Goldstein, J.L., Mangelsdorf, D.J., Regulation of mouse sterol regulatory element-binding protein-1c gene (SREBP-1c) by oxysterol receptors, LXRalpha and LXRbeta. Genes Dev. 14 (2000), 2819–2830.
86. Yoshikawa, T., Shimano, H., Amemiya-Kudo, M., Yahagi, N., Hasty, A.H., Matsuzaka, T., Okazaki, H., Tamura, Y., Iizuka, Y., Ohashi, K., Osuga, J., Harada, K., Gotoda, T., Kimura, S., Ishibashi, S., Yamada, N., Identification of liver X receptor-retinoid X receptor as an activator of the sterol regulatory element-binding protein 1c gene promoter. Mol. Cell. Biol. 21 (2001), 2991–3000.
87. Joseph, S.B., Laffitte, B.A., Patel, P.H., Watson, M.A., Matsukuma, K.E., Walczak, R., Collins, J.L., Osborne, T.F., Tontonoz, P., Direct and indirect mechanisms for regulation of fatty acid synthase gene expression by liver X receptors. J. Biol. Chem. 277 (2002), 11019–11025.
88. Shimano, H., Horton, J.D., Shimomura, I., Hammer, R.E., Brown, M.S., Goldstein, J.L., Isoform 1c of sterol regulatory element binding protein is less active than isoform 1a in livers of transgenic mice and in cultured cells. J. Clin. Invest. 99 (1997), 846–854.
89. Sun, X., Haas, M.E., Miao, J., Mehta, A., Graham, M.J., Crooke, R.M., de Barros, J.P., Wang, J.G., Aikawa, M., Masson, D., Biddinger, S.B., Insulin dissociates the effects of liver X receptor on lipogenesis, endoplasmic reticulum stress, and inflammation. J. Biol. Chem. 291 (2016), 1115–1122.
90. Dyall, S.C., Long-chain omega-3 fatty acids and the brain: a review of the independent and shared effects of EPA, DPA and DHA. Front. Aging Neurosci., 7, 2015, 52.
91. Lengqvist, J., Mata De Urquiza, A., Bergman, A.C., Willson, T.M., Sjovall, J., Perlmann, T., Griffiths, W.J., Polyunsaturated fatty acids including docosahexaenoic and arachidonic acid bind to the retinoid X receptor alpha ligand-binding domain. Mol. Cell. Proteomics 3 (2004), 692–703.
92. Nakamura, M.T., Yudell, B.E., Loor, J.J., Regulation of energy metabolism by long-chain fatty acids. Prog. Lipid Res. 53 (2014), 124–144.
93. Steineger, H.H., Arntsen, B.M., Spydevold, O., Sorensen, H.N., Gene transcription of the retinoid X receptor alpha (RXRalpha) is regulated by fatty acids and hormones in rat hepatic cells. J. Lipid Res. 39 (1998), 744–754.
94. Fan, Y.Y., Spencer, T.E., Wang, N., Moyer, M.P., Chapkin, R.S., Chemopreventive n-3 fatty acids activate RXRalpha in colonocytes. Carcinogenesis 24 (2003), 1541–1548.
95. Boergesen, M., Pedersen, T.A., Gross, B., van Heeringen, S.J., Hagenbeek, D., Bindesboll, C., Caron, S., Lalloyer, F., Steffensen, K.R., Nebb, H.I., Gustafsson, J.A., Stunnenberg, H.G., Staels, B., Mandrup, S., Genome-wide profiling of liver X receptor, retinoid X receptor, and peroxisome proliferator-activated receptor alpha in mouse liver reveals extensive sharing of binding sites. Mol. Cell. Biol. 32 (2012), 852–867.
96. Ducheix, S., Montagner, A., Polizzi, A., Lasserre, F., Marmugi, A., Bertrand-Michel, J., Podechard, N., Al Saati, T., Chetiveaux, M., Baron, S., Boue, J., Dietrich, G., Mselli-Lakhal, L., Costet, P., Lobaccaro, J.M., Pineau, T., Theodorou, V., Postic, C., Martin, P.G., Guillou, H., Essential fatty acids deficiency promotes lipogenic gene expression and hepatic steatosis through the liver X receptor. J. Hepatol. 58 (2013), 984–992.
97. Colin, S., Bourguignon, E., Boullay, A.B., Tousaint, J.J., Huet, S., Caira, F., Staels, B., Lestavel, S., Lobaccaro, J.M., Delerive, P., Intestine-specific regulation of PPARalpha gene transcription by liver X receptors. Endocrinology 149 (2008), 5128–5135.
98. Inagaki, T., Dutchak, P., Zhao, G., Ding, X., Gautron, L., Parameswara, V., Li, Y., Goetz, R., Mohammadi, M., Esser, V., Elmquist, J.K., Gerard, R.D., Burgess, S.C., Hammer, R.E., Mangelsdorf, D.J., Kliewer, S.A., Endocrine regulation of the fasting response by PPARalpha-mediated induction of fibroblast growth factor 21. Cell Metab. 5 (2007), 415–425.
99. Ide, T., Shimano, H., Yoshikawa, T., Yahagi, N., Amemiya-Kudo, M., Matsuzaka, T., Nakakuki, M., Yatoh, S., Iizuka, Y., Tomita, S., Ohashi, K., Takahashi, A., Sone, H., Gotoda, T., Osuga, J., Ishibashi, S., Yamada, N., Cross-talk between peroxisome proliferator-activated receptor (PPAR) alpha and liver X receptor (LXR) in nutritional regulation of fatty acid metabolism. II. LXRs suppress lipid degradation gene promoters through inhibition of PPAR signaling. Mol. Endocrinol. 17 (2003), 1255–1267.
100. Yoshikawa, T., Ide, T., Shimano, H., Yahagi, N., Amemiya-Kudo, M., Matsuzaka, T., Yatoh, S., Kitamine, T., Okazaki, H., Tamura, Y., Sekiya, M., Takahashi, A., Hasty, A.H., Sato, R., Sone, H., Osuga, J., Ishibashi, S., Yamada, N., Cross-talk between peroxisome proliferator-activated receptor (PPAR) alpha and liver X receptor (LXR) in nutritional regulation of fatty acid metabolism. I. PPARs suppress sterol regulatory element binding protein-1c promoter through inhibition of LXR signaling. Mol. Endocrinol. 17 (2003), 1240–1254.
101. Gao, M., Bu, L., Ma, Y., Liu, D., Concurrent activation of liver X receptor and peroxisome proliferator-activated receptor alpha exacerbates hepatic steatosis in high fat diet-induced obese mice. PLoS One, 8, 2013, e65641.
102. Zhang, W., Bu, S.Y., Mashek, M.T., O-Sullivan, I., Sibai, Z., Khan, S.A., Ilkayeva, O., Newgard, C.B., Mashek, D.G., Unterman, T.G., Integrated regulation of hepatic lipid and glucose metabolism by adipose triacylglycerol lipase and FoxO proteins. Cell Rep. 15 (2016), 349–359.
103. Deng, X., Zhang, W., O-Sullivan, I., Williams, J.B., Dong, Q., Park, E.A., Raghow, R., Unterman, T.G., Elam, M.B., FoxO1 inhibits sterol regulatory element-binding protein-1c (SREBP-1c) gene expression via transcription factors Sp1 and SREBP-1c. J. Biol. Chem. 287 (2012), 20132–20143.
104. Liu, X., Qiao, A., Ke, Y., Kong, X., Liang, J., Wang, R., Ouyang, X., Zuo, J., Chang, Y., Fang, F., FoxO1 represses LXRalpha-mediated transcriptional activity of SREBP-1c promoter in HepG2 cells. FEBS Lett. 584 (2010), 4330–4334.
105. Nielsen, T.S., Kampmann, U., Nielsen, R.R., Jessen, N., Orskov, L., Pedersen, S.B., Jorgensen, J.O., Lund, S., Moller, N., Reduced mRNA and protein expression of perilipin A and G0/G1 switch gene 2 (G0S2) in human adipose tissue in poorly controlled type 2 diabetes. J. Clin. Endocrinol. Metab. 97 (2012), E1348–E1352.
106. Svart, M., Kampmann, U., Voss, T., Pedersen, S.B., Johannsen, M., Rittig, N., Poulsen, P.L., Nielsen, T.S., Jessen, N., Moller, N., Combined insulin deficiency and endotoxin exposure stimulate lipid mobilization and alter adipose tissue signaling in an experimental model of ketoacidosis in subjects with type 1 diabetes: a randomized controlled crossover trial. Diabetes 65 (2016), 1380–1386.
107. Gibson, G., Human evolution: thrifty genes and the dairy queen. Curr. Biol. 17 (2007), R295–R296.
108. Hara, K., Kubota, N., Tobe, K., Terauchi, Y., Miki, H., Komeda, K., Tamemoto, H., Yamauchi, T., Hagura, R., Ito, C., Akanuma, Y., Kadowaki, T., The role of PPARgamma as a thrifty gene both in mice and humans. Br. J. Nutr. 84:Suppl. 2 (2000), S235–S239.
109. Genne-Bacon, E.A., Thinking evolutionarily about obesity. Yale J. Biol. Med. 87 (2014), 99–112.
110. Campbell, L.V., The thrifty gene hypothesis: maybe everyone is right?. Int. J. Obes. 32 (2008), 723–724 (author reply 725-726).
111. Joffe, B., Zimmet, P., The thrifty genotype in type 2 diabetes: an unfinished symphony moving to its finale?. Endocrine 9 (1998), 139–141.
112. Sharma, A.M., The thrifty-genotype hypothesis and its implications for the study of complex genetic disorders in man. J. Mol. Med. 76 (1998), 568–571.
113. Kurat, C.F., Natter, K., Petschnigg, J., Wolinski, H., Scheuringer, K., Scholz, H., Zimmermann, R., Leber, R., Zechner, R., Kohlwein, S.D., Obese yeast: triglyceride lipolysis is functionally conserved from mammals to yeast. J. Biol. Chem. 281 (2006), 491–500.
114. Gronke, S., Mildner, A., Fellert, S., Tennagels, N., Petry, S., Muller, G., Jackle, H., Kuhnlein, R.P., Brummer lipase is an evolutionary conserved fat storage regulator in Drosophila. Cell Metab. 1 (2005), 323–330.
115. Briand, F., Treguier, M., Andre, A., Grillot, D., Issandou, M., Ouguerram, K., Sulpice, T., Liver X receptor activation promotes macrophage-to-feces reverse cholesterol transport in a dyslipidemic hamster model. J. Lipid Res. 51 (2010), 763–770.
116. Kannisto, K., Gafvels, M., Jiang, Z.Y., Slatis, K., Hu, X., Jorns, C., Steffensen, K.R., Eggertsen, G., LXR driven induction of HDL-cholesterol is independent of intestinal cholesterol absorption and ABCA1 protein expression. Lipids 49 (2014), 71–83.
117. Ou, X., Dai, X., Long, Z., Tang, Y., Cao, D., Hao, X., Hu, Y., Li, X., Tang, C., Liver X receptor agonist T0901317 reduces atherosclerotic lesions in apoE −/− mice by up-regulating NPC1 expression. Sci. China Ser. C Life Sci. 51 (2008), 418–429.
118. Plosch, T., Kok, T., Bloks, V.W., Smit, M.J., Havinga, R., Chimini, G., Groen, A.K., Kuipers, F., Increased hepatobiliary and fecal cholesterol excretion upon activation of the liver X receptor is independent of ABCA1. J. Biol. Chem. 277 (2002), 33870–33877.
119. Yasuda, T., Grillot, D., Billheimer, J.T., Briand, F., Delerive, P., Huet, S., Rader, D.J., Tissue-specific liver X receptor activation promotes macrophage reverse cholesterol transport in vivo. Arterioscler. Thromb. Vasc. Biol. 30 (2010), 781–786.
120. Zanotti, I., Poti, F., Pedrelli, M., Favari, E., Moleri, E., Franceschini, G., Calabresi, L., Bernini, F., The LXR agonist T0901317 promotes the reverse cholesterol transport from macrophages by increasing plasma efflux potential. J. Lipid Res. 49 (2008), 954–960.
121. Cha, J.Y., Repa, J.J., The liver X receptor (LXR) and hepatic lipogenesis. The carbohydrate-response element-binding protein is a target gene of LXR. J. Biol. Chem. 282 (2007), 743–751.
122. Zhang, Y., Breevoort, S.R., Angdisen, J., Fu, M., Schmidt, D.R., Holmstrom, S.R., Kliewer, S.A., Mangelsdorf, D.J., Schulman, I.G., Liver LXRalpha expression is crucial for whole body cholesterol homeostasis and reverse cholesterol transport in mice. J. Clin. Invest. 122 (2012), 1688–1699.