Insulin-induced gene: A new regulator in lipid metabolism

Peptides

Volumn 31, Issue 11, 2010, Pages 2145-2150

  Dong, Xiao Ying ^a   Tang, Sheng Qiu ^a  

^a SHAOGUAN UNIVERSITY   (China)

Author keywords

Cholesterol metabolism; Disease; Glucose homeostasis; HMG CoA reductase; Insigs; Lipogenesis; SCAP

Indexed keywords

HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; INSULIN; INSULIN INDUCED GENE 1 PROTEIN; INSULIN INDUCED GENE 2 PROTEIN; MEVINOLIN; STEROL REGULATORY ELEMENT BINDING PROTEIN; UBIQUITIN; UNCLASSIFIED DRUG;

ADIPOGENESIS; ADIPOSE TISSUE; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; CELL CULTURE; CHOLESTEROL METABOLISM; CLEFTING SYNDROME; CONGENITAL MALFORMATION; DNA POLYMORPHISM; ENDOPLASMIC RETICULUM; ENZYME BINDING; ENZYME DEGRADATION; GENE ACTIVITY; GENE CONTROL; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE INDUCTION; GENE SILENCING; GENETIC ASSOCIATION; GENETIC DISORDER; GLUCOSE HOMEOSTASIS; HUMAN; INSULIN DEFICIENCY; INSULIN RESISTANCE; LIPID METABOLISM; LIPOGENESIS; LIVER; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FAMILY; PROTEIN PROCESSING; PROTEIN STABILITY; PROTEIN STRUCTURE; REVIEW;

AMINO ACID SEQUENCE; ANIMALS; CHOLESTEROL; HOMEOSTASIS; HUMANS; INSULIN; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIPID METABOLISM; LIPOGENESIS; MEMBRANE PROTEINS; POLYMORPHISM, GENETIC; STEROL REGULATORY ELEMENT BINDING PROTEINS;

EID: 77957843089     PISSN: 01969781     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.peptides.2010.07.020     Document Type: Review

References (83)

1. C.M. Adams, J.L. Goldstein, and M.S. Brown Cholesterol-induced conformational change in SCAP enhanced by Insig proteins and mimicked by cationic amphiphiles Proc Natl Acad Sci USA 100 19 2003 10647 10652
2. C.M. Adams, J. Reitz, J.K. De Brabander, J.D. Feramisco, L. Li, and M.S. Brown Cholesterol and 25-hydroxycholesterol inhibit activation of SREBPs by different mechanisms, both involving SCAP and insigs J Biol Chem 279 2004 52772 52780
3. A.D. Attie Insig: a significant integrator of nutrient and hormonal signals J Clin Invest 113 8 2004 1112 1114
4. E. Bonzón-Kulichenko, D. Schwudke, N. Gallardo, E. Moltó, T. Fernández-Agulló, A. Shevchenko, and A. Andrés Central leptin regulates total ceramide content and sterol regulatory element binding protein-1C proteolytic maturation in rat white adipose tissue Endocrinology 150 1 2009 169 178
5. M.S. Brown, and J.L. Goldstein A proteolytic pathway that controls the cholesterol content of membranes, cells, and blood Proc Natl Acad Sci USA 96 20 1999 11041 11048
6. J.S. Burg, D.W. Powell, R. Chai, A.L. Hughes, A.J. Link, and P.J. Espenshade Insig regulates HMG-CoA reductase by controlling enzyme phosphorylation in fission yeast Cell Metab 8 6 2008 522 531
7. A.C. Cervino, G. Li, S. Edwards, J. Zhu, C. Laurie, and G. Tokiwa Integrating QTL and high-density SNP analyses in mice to identify Insig2 as a susceptibility gene for plasma cholesterol levels Genomics 86 5 2005 505 517
8. S.R. Commerford, L. Peng, J.J. Dubé, and R.M. O'Doherty In vivo regulation of SREBP-1c in skeletal muscle: effects of nutritional status, glucose, insulin, and leptin Am J Physiol Regul Integr Comp Physiol 287 1 2004 R218 R227
9. L.J. Engelking, B.M. Evers, J.A. Richardson, J.L. Goldstein, M.S. Brown, and G. Liang Severe facial clefting in Insig-deficient mouse embryos caused by sterol accumulation and reversed by lovastatin J Clin Invest 116 9 2006 2356 2365
10. L.J. Engelking, H. Kuriyama, R.E. Hammer, J.D. Horton, M.S. Brown, and J.L. Goldstein Overexpression of Insig-1 in the livers of transgenic mice inhibits SREBP processing and reduces insulin-stimulated lipogenesis J Clin Invest 113 8 2004 1168 1175
11. P.J. Espenshade, and A.L. Hughes Regulation of sterol synthesis in eukaryotes Annu Rev Genet 41 2007 401 427
12. B.M. Evers, M.S. Farooqi, J.M. Shelton, J.A. Richardson, J.L. Goldstein, and M.S. Brown Hair growth defects in insig-deficient mice caused by cholesterol precursor accumulation and reversed by simvastatin J Invest Dermatol 130 5 2010 1237 1248
13. J.D. Feramisco, J.L. Goldstein, and M.S. Brown Membrane topology of human insig-1, a protein regulator of lipid synthesis J Biol Chem 279 9 2004 8487 8496
14. A. Fernández-Alvarez, M.S. Alvarez, C. Cucarella, and M. Casado Characterization of the human insulin induced gene 2 (insig2) promoter: the role of ETS-binding motifs J Biol Chem 285 16 2010 11765 11774
15. I. Flury, R. Garza, A. Shearer, J. Rosen, S. Cronin, and R.Y. Hampton INSIG: a broadly conserved transmembrane chaperone for sterol-sensing domain proteins EMBO J 24 22 2005 3917 3926
16. F. Foufelle, and P. Ferré New perspectives in the regulation of hepatic glycolytic and lipogenic genes by insulin and glucose: a role for the transcription factor sterol regulatory element binding protein-1c Biochem J 366 2002 377 391
17. G. Gil, J.R. Faust, D.J. Chin, J.L. Goldstein, and M.S. Brown Membrane-bound domain of HMG CoA reductase is required for sterol-enhanced degradation of the enzyme Cell 41 1985 249 258
18. J.L. Goldstein, and M.S. Brown Regulation of the mevalonate pathway Nature 343 1990 425 430
19. J.L. Goldstein, R.A. DeBose-Boyd, and M.S. Brown Protein sensors for membrane sterols Cell 124 1 2006 35 46
20. J.L. Goldstein, R.B. Rawson, and M.S. Brown Mutant mammalian cells as tools to delineate the sterol regulatory element-binding pathway for feedback regulation of lipid synthesis Arch Biochem Biophys 397 2002 139 148
21. Y. Gong, J.N. Lee, M.S. Brown, J.L. Goldstein, and J. Ye Juxtamembranous aspartic acid in Insig-1 and Insig-2 is required for cholesterol homeostasis Proc Natl Acad Sci USA 103 16 2006 6154 6159
22. Y. Gong, J.N. Lee, P.C. Lee, J.L. Goldstein, M.S. Brown, and J. Ye Sterol-regulated ubiquitination and degradation of Insig-1 creates a convergent mechanism for feedback control of cholesterol synthesis and uptake Cell Metab 3 1 2006 15 24
23. R.Y. Hampton Proteolysis and sterol regulation Annu Rev Cell Dev Biol 18 2002 345 378
24. L.Q. Han, H.J. Li, Y.Y. Wang, H.S. Zhu, L.F. Wang, and Y.J. Guo mRNA abundance and expression of SLC27A, ACC, SCD, FADS, LPIN, INSIG, and PPARGC1 gene isoforms in mouse mammary glands during the lactation cycle Genet Mol Res 9 2 2010 1250 1257
25. A. Herbert, N.P. Gerry, M.B. McQueen, I.M. Heid, A. Pfeufer, and T. Illig A common genetic variant is associated with adult and childhood obesity Science 312 5771 2006 279 283
26. J.D. Horton, J.L. Goldstein, and M.S. Brown SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver J Clin Invest 109 9 2002 1125 1131
27. J.D. Horton, N.A. Shah, J.A. Warrington, N.N. Anderson, S.W. Park, and M.S. Brown Combined analysis of oligonucleotide microarray data from transgenic and knockout mice identifies direct SREBP target genes Proc Natl Acad Sci USA 100 2003 12027 12032
28. X. Hua, A. Nohturfft, J.L. Goldstein, and M.S. Brown Sterol resistance in CHO cells traced to point mutation in SREBP cleavage activating protein Cell 87 1996 415 426
29. M.L. Hubbert, Y. Zhang, F.Y. Lee, and P.A. Edwards Regulation of hepatic Insig-2 by the farnesoid X receptor Mol Endocrinol 21 6 2007 1359 1369
30. Y. Ikeda, G.N. Demartino, M.S. Brown, J.N. Lee, J.L. Goldstein, and J. Ye Regulated endoplasmic reticulum-associated degradation of a polytopic protein: p97 recruits proteasomes to Insig-1 before extraction from membranes J Biol Chem 284 50 2009 34889 34900
31. B.A. Janowski The hypocholesterolemic agent LY295427 up-regulates INSIG-1, identifying the INSIG-1 protein as a mediator of cholesterol homeostasis through SREBP Proc Natl Acad Sci USA 99 20 2002 12675 12680
32. T. Kakuma, Y. Lee, M. Higa, Z. Wang, W. Pan, I. Shimomura, and R.H. Unger Leptin, troglitazone, and the expression of sterol regulatory element binding proteins in liver and pancreatic islets Proc Natl Acad Sci U S A 97 15 2000 8536 8541
33. S.O. Ka, K.A. Kim, K.B. Kwon, J.W. Park, and B.H. Park Silibinin attenuates adipogenesis in 3T3-L1 preadipocytes through a potential upregulation of the insig pathway Int J Mol Med 23 5 2009 633 637
34. H.R. Kast-Woelbern, S.L. Dana, R.M. Cesario, L. Sun, L.Y. de Grandpre, and M.E. Brooks Rosiglitazone induction of Insig-1 in white adipose tissue reveals a novel interplay of peroxisome proliferator-activated receptor gamma and sterol regulatory element-binding protein in the regulation of adipogenesis J Biol Chem 279 23 2004 23908 23915
35. A.B. Keeton, K.D. Bortoff, J.L. Franklin, and J.L. Messina Blockade of rapid versus prolonged extracellularly regulated kinase 1/2 activation has differential effects on insulin-induced gene expression Endocrinology 146 6 2005 2716 2725
36. W.J. Kovacs, K.N. Tape, J.E. Shackelford, T.M. Wikander, M.J. Richards, and S.J. Fliesler Peroxisome deficiency causes a complex phenotype because of hepatic SREBP/Insig dysregulation associated with endoplasmic reticulum stress J Biol Chem 284 11 2009 7232 7245
37. S. Krapivner, E. Chernogubova, M. Ericsson, C. Ahlbeck-Glader, A. Hamsten, and F.M. van't Hooft Human evidence for the involvement of insulin-induced gene 1 in the regulation of plasma glucose concentration Diabetologia 50 1 2007 94 102
38. S. Krapivner, S. Popov, E. Chernogubova, M.L. Hellénius, R.M. Fisher, and A. Hamsten Insulin-induced gene 2 involvement in human adipocyte metabolism and body weight regulation J Clin Endocrinol Metab 93 5 2008 1995 2001
39. P.E. Kuwabara, and M. Labouesse The sterol-sensing domain: multiple families, a unique role? Trends Genet 18 2002 193 201
40. J.N. Lee, Y. Gong, X. Zhang, and J. Ye Proteasomal degradation of ubiquitinated Insig proteins is determined by serine residues flanking ubiquitinated lysines Proc Natl Acad Sci USA 103 13 2006 4958 4963
41. J.N. Lee, B. Song, R.A. DeBose-Boyd, and J. Ye Sterol-regulated degradation of Insig-1 mediated by the membrane-bound ubiquitin ligase gp78 J Biol Chem 281 51 2006 39308 39315
42. J.N. Lee, and J. Ye Proteolytic activation of sterol regulatory element-binding protein induced by cellular stress through depletion of Insig-1 J Biol Chem 279 43 2004 45257 45265
43. J.N. Lee, X. Zhang, J.D. Feramisco, Y. Gong, and J. Ye Unsaturated fatty acids inhibit proteasomal degradation of Insig-1 at a postubiquitination step J Biol Chem 283 48 2008 33772 33783
44. P.C. Lee, and R.A. DeBose-Boyd Intramembrane glycine mediates multimerization of Insig-2, a requirement for sterol regulation in Chinese hamster ovary cells J Lipid Res 51 1 2010 192 201
45. P.C. Lee, P. Liu, W.P. Li, and R.A. Debose-Boyd Amplification of the gene for SCAP, coupled with Insig-1 deficiency, confers sterol resistance in mutant Chinese hamster ovary cells J Lipid Res 48 9 2007 1944 1954
46. P.C. Lee, N. Sever, and R.A. Debose-Boyd Isolation of sterol-resistant Chinese hamster ovary cells with genetic deficiencies in both Insig-1 and Insig-2 J Biol Chem 280 26 2005 25242 25249
47. S. Lee, D.K. Lee, E. Choi, and J.W. Lee Identification of a functional vitamin D response element in the murine Insig-2 promoter and its potential role in the differentiation of 3T3-L1 preadipocytes Mol Endocrinol 19 2 2005 399 408
48. S. Le Hellard, F.M. Theisen, M. Haberhausen, M.B. Raeder, J. Fernø, and S. Gebhardt Association between the insulin-induced gene 2 (INSIG2) and weight gain in a German sample of antipsychotic-treated schizophrenic patients: perturbation of SREBP-controlled lipogenesis in drug-related metabolic adverse effects? Mol Psychiatry 14 3 2009 308 317
49. G.S. Leichner, R. Avner, D. Harats, and J. Roitelman Dislocation of HMG-CoA reductase and Insig-1, two polytopic endoplasmic reticulum proteins, en route to proteasomal degradation Mol Biol Cell 20 14 2009 3330 3341
50. J. Li, K. Takaishi, W. Cook, S.K. McCorkle, and R.H. Unger Insig-1 “brakes” lipogenesis in adipocytes and inhibits differentiation of preadipocytes Proc Natl Acad Sci USA 100 16 2003 9476 9481
51. J. Li, X. Yu, W. Pan, and R.H. Unger Gene expression profile of rat adipose tissue at the onset of high-fat-diet obesity Am J Physiol 282 2002 E1334 E1341
52. K.L. Ma, Z. Varghese, Y. Ku, S.H. Powis, Y. Chen, and J.F. Moorhead Sirolimus inhibits endogenous cholesterol synthesis induced by inflammatory stress in human vascular smooth muscle cells Am J Physiol Heart Circ Physiol 298 6 2010 H1646 H1651
53. M. Matsuda, B.S. Korn, R.E. Hammer, Y.A. Moon, R. Komuro, and J.D. Horton SREBP cleavage-activating protein (SCAP) is required for increased lipid synthesis in liver induced by cholesterol deprivation and insulin elevation Genes Dev 15 2001 1206 1216
54. R. McPherson, and A. Gauthier Molecular regulation of SREBP function: the Insig-SCAP connection and isoform-specific modulation of lipid synthesis Biochem Cell Biol 82 1 2004 201 211
55. A. Nogalska, E. Sucajtys-Szulc, and J. Swierczynski Leptin decreases lipogenic enzyme gene expression through modification of SREBP-1c gene expression in white adipose tissue of aging rats Metabolism 54 8 2005 1041 1047
56. A. Nohturfft, M.S. Brown, and J.L. Goldstein Topology of SREBP cleavage-activating protein, a polytopic membrane protein with a sterol-sensing domain J Biol Chem 273 1998 17243 17250
57. A. Nohturfft, R.A. DeBose-Boyd, S. Scheek, J.L. Goldstein, and M.S. Brown Sterols regulate cycling of SREBP cleavage-activating protein (SCAP) between endoplasmic reticulum and Golgi Proc Natl Acad Sci USA 96 1999 11235 11240
58. A. Nohturfft, D. Yabe, J.L. Goldstein, M.S. Brown, and P.J. Espenshade Regulated step in cholesterol feedback localized to budding of SCAP from ER membranes Cell 102 2000 315 323
59. K. Oki, K. Yamane, N. Kamei, T. Asao, T. Awaya, and N. Kohno The single nucleotide polymorphism upstream of insulin-induced gene 2 (INSIG2) is associated with the prevalence of hypercholesterolaemia, but not with obesity, in Japanese American women Br J Nutr 101 3 2009 322 327
60. Y. Peng, E.J. Schwarz, M.A. Lazar, A. Genin, N.B. Spinner, and R. Taub Cloning, human chromosomal assignment, and adipose and hepatic expression of the CL-6/INSIG1 gene Genomics 43 3 1997 278 284 (Pubitemid 27353703)
61. X. Qin, X. Xie, Y. Fan, J. Tian, Y. Guan, and X. Wang Peroxisome proliferator-activated receptor-delta induces insulin-induced gene-1 and suppresses hepatic lipogenesis in obese diabetic mice Hepatology 48 2 2008 432 441
62. A. Radhakrishnan, Y. Ikeda, H.J. Kwon, M.S. Brown, and J.L. Goldstein Sterol-regulated transport of SREBPs from endoplasmic reticulum to Golgi: oxysterols block transport by binding to Insig Proc Natl Acad Sci USA 104 16 2007 6511 6518
63. J. Roitelman, E.H. Olender, S. Bar-Nun, W.A. Dunn Jr, and R.D. Simon Immunological evidence for eight spans in the membrane domain of 3-hydroxy-3-methylglutaryl coenzyme A reductase: implications for enzyme degradation in the endoplasmic reticulum J Cell Biol 117 1992 959 973
64. A. Roth, R. Looser, M. Kaufmann, S.M. Blättler, F. Rencurel, and W. Huang Regulatory cross-talk between drug metabolism and lipid homeostasis: constitutive androstane receptor and pregnane X receptor increase Insig-1 expression Mol Pharmacol 73 4 2008 1282 1289
65. J. Sakai, E.A. Duncan, R.B. Rawson, X. Hua, M.S. Brown, and J.L. Goldstein Sterol-regulated release of SREBP-2 from cell membranes requires two sequential cleavages, one within a transmembrane segment Cell 85 7 1996 1037 1046
66. J. Sakai, A. Nohturfft, D. Cheng, Y.K. Ho, M.S. Brown, and J.L. Goldstein Identification of complexes between the COOH terminal domains of sterol regulatory element-binding proteins (SREBPs) and SREBP cleavage-activating protein J Biol Chem 272 1997 20213 20221
67. N. Sever, P.C. Lee, B.L. Song, R.B. Rawson, and R.A. Debose-Boyd Isolation of mutant cells lacking Insig-1 through selection with SR-12813, an agent that stimulates degradation of 3-hydroxy-3-methylglutaryl-coenzyme A reductase J Biol Chem 279 41 2004 43136 43147
68. N. Sever, B.L. Song, D. Yabe, J.L. Goldstein, M.S. Brown, and R.A. DeBose-Boyd Insig-dependent ubiquitination and degradation of mammalian 3-hydroxy-3-methylglutaryl-CoA reductase stimulated by sterols and geranylgeraniol J Biol Chem 278 52 2003 52479 52490
69. N. Sever, T. Yang, M.S. Brown, J.L. Goldstein, and R.A. DeBose-Boyd Accelerated degradation of HMG CoA reductase mediated by binding of insig-1 to its sterol-sensing domain Mol Cell 11 1 2003 25 33
70. C. Sewter, D. Berger, R.V. Considine, G. Medina, J. Rochford, and T. Ciaraldi Human obesity and type 2 diabetes are associated with alterations in SREBP1 isoform expression that are reproduced ex vivo by tumor necrosis factor-alpha Diabetes 51 4 2002 1035 1041
71. L.P. Sun, L. Li, J.L. Goldstein, and M.S. Brown Insig required for sterol-mediated inhibition of Scap/SREBP binding to COPII proteins in vitro J Biol Chem 280 28 2005 26483 26490
72. L.P. Sun, J. Seemann, J.L. Goldstein, and M.S. Brown Sterol-regulated transport of SREBPs from endoplasmic reticulum to Golgi: Insig renders sorting signal in Scap inaccessible to COPII proteins Proc Natl Acad Sci U S A 104 16 2007 6519 6526
73. M. Szopa, A. Meirhaeghe, J. Luan, L.A. Moreno, M. Gonzalez-Gross, and A. Vidal-Puig No association between polymorphisms in the INSIG1 gene and the risk of type 2 diabetes and related traits Am J Clin Nutr 92 1 2010 252 257
74. K. Takaishi, L. Duplomb, M.Y. Wang, J. Li, and R.H. Unger Hepatic insig-1 or -2 overexpression reduces lipogenesis in obese Zucker diabetic fatty rats and in fasted/refed normal rats Proc Natl Acad Sci USA 101 18 2004 7106 7111
75. A.K. Tiwari, C.C. Zai, H.Y. Meltzer, J.A. Lieberman, D.J. Müller, and J.L. Kennedy Association study of polymorphisms in Insulin Induced Gene 2 (INSIG2) with antipsychotic-induced weight gain in European and African-American schizophrenia patients Hum Psychopharmacol 25 3 2010 253 259
76. -/- mouse liver J Biol Chem 276 42 2001 38337 38340
77. S.M. Vallett, H.B. Sanchez, J.M. Rosenfeld, and T.F. Osborne A direct role for sterol regulatory element binding protein in activation of 3-hydroxy-3-methylglutaryl coenzyme A reductase gene J Biol Chem 271 1996 12247 12253
78. Y.H. Xie, Z.H. Mo, K. Chen, Y.B. Yang, X.W. Xing, and E.Y. Liao Effect of different glucose concentrations on the expressions of insig-1 and insig-2 mRNA during the differentiation of 3T3-L1 cells Zhong Nan Da Xue Xue Bao Yi Xue Ban 33 3 2008 238 244
79. D. Yabe, M.S. Brown, and J.L. Goldstein Insig-2, a second endoplasmic reticulum protein that binds SCAP and blocks export of sterol regulatory element-binding proteins Proc Natl Acad Sci USA 99 20 2002 12753 12758
80. D. Yabe, R. Komuro, G. Liang, J.L. Goldstein, and M.S. Brown Liver-specific mRNA for Insig-2 down-regulated by insulin: implications for fatty acid synthesis Proc Natl Acad Sci USA 100 6 2003 3155 3160
81. D. Yabe, Z.P. Xia, C.M. Adams, and R.B. Rawson Three mutations in sterol-sensing domain of SCAP block interaction with insig and render SREBP cleavage insensitive to sterols Proc Natl Acad Sci USA 99 26 2002 16672 16677
82. T. Yang, P.J. Espenshade, M.E. Wright, D. Yabe, Y. Gong, and R. Aebersold Crucial step in cholesterol homeostasis: sterols promote binding of SCAP to INSIG-1, a membrane protein that facilitates retention of SREBPs in ER Cell 110 4 2002 489 500
83. C.R. Yellaturu, X. Deng, E.A. Park, R. Raghow, and M.B. Elam Insulin enhances the biogenesis of nuclear sterol regulatory element-binding protein (SREBP)-1c by posttranscriptional down-regulation of Insig-2A and its dissociation from SREBP cleavage-activating protein (SCAP).SREBP-1c complex J Biol Chem 284 46 2009 31726 31734