Protein acetylation mechanisms in the regulation of insulin and insulin-like growth factor 1 signalling

Molecular and Cellular Endocrinology

Volumn 362, Issue 1-2, 2012, Pages 1-10

  Pirola, Luciano ^a   Zerzaihi, Ouafa ^a   Vidal, Hubert ^a   Solari, Florence ^b  

^a UNIVERSITÉ LYON 1   (France)

^b CENTRE DE GÉNÉTIQUE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

HDACs; Histone acetyltransferases; Insulin signalling; Lysine acetylation; Sirtuins

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; HISTONE ACETYLTRANSFERASE; HISTONE ACETYLTRANSFERASE PCAF; HISTONE DEACETYLASE; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; INSULIN; INSULIN RECEPTOR SUBSTRATE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PHOSPHOINOSITIDE DEPENDENT PROTEIN KINASE 1; PROTEIN KINASE B; PROTEIN P300; PROTEIN TRB3; SIRTUIN 1; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR FOXO; UNCLASSIFIED DRUG;

ACETYLATION; DEACYLATION; HUMAN; MAMMAL CELL; METABOLIC RATE; METABOLIC REGULATION; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION;

ACETYLATION; ANIMALS; GENE EXPRESSION REGULATION; HUMANS; INSULIN; INSULIN-LIKE GROWTH FACTOR I; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECEPTOR CROSS-TALK; RECEPTOR, IGF TYPE 1; SIGNAL TRANSDUCTION;

EID: 84865299042     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2012.05.011     Document Type: Review

References (86)

1. Banks A.S., Kim-Muller J.Y., Mastracci T.L., Kofler N.M., Qiang L., Haeusler R.A., Jurczak M.J., Laznik D., Heinrich G., Samuel V.T., Shulman G.I., Papaioannou V.E., Accili D. Dissociation of the glucose and lipid regulatory functions of FoxO1 by targeted knockin of acetylation-defective alleles in mice. Cell Metab. 2011, 14:587-597.
2. Banks A.S., Kon N., Knight C., Matsumoto M., Gutierrez-Juarez R., Rossetti L., Gu W., Accili D. SirT1 gain of function increases energy efficiency and prevents diabetes in mice. Cell Metab. 2008, 8:333-341.
3. Barthel A., Schmoll D., Unterman T.G. FoxO proteins in insulin action and metabolism. Trends Endocrinol. Metab. 2005, 16:183-189.
4. Baur J.A., Pearson K.J., Price N.L., Jamieson H.A., Lerin C., Kalra A., Prabhu V.V., Allard J.S., Lopez-Lluch G., Lewis K., Pistell P.J., Poosala S., Becker K.G., Boss O., Gwinn D., Wang M., Ramaswamy S., Fishbein K.W., Spencer R.G., Lakatta E.G., Le Couteur D., Shaw R.J., Navas P., Puigserver P., Ingram D.K., de Cabo R., Sinclair D.A. Resveratrol improves health and survival of mice on a high-calorie diet. Nature 2006, 444:337-342.
5. Baur J.A., Sinclair D.A. Therapeutic potential of resveratrol: the in vivo evidence. Nat. Rev. Drug. Discov. 2006, 5:493-506.
6. Bordone L., Motta M.C., Picard F., Robinson A., Jhala U.S., Apfeld J., McDonagh T., Lemieux M., McBurney M., Szilvasi A., Easlon E.J., Lin S.J., Guarente L. Sirt1 regulates insulin secretion by repressing UCP2 in pancreatic beta cells. PLoS Biol. 2006, 4:e31.
7. Boura-Halfon S., Zick Y. Phosphorylation of IRS proteins, insulin action, and insulin resistance. Am. J. Physiol. Endocrinol. Metab. 2009, 296:E581-591.
8. Brognard J., Sierecki E., Gao T., Newton A.C. PHLPP and a second isoform, PHLPP2, differentially attenuate the amplitude of Akt signaling by regulating distinct Akt isoforms. Mol. Cell 2007, 25:917-931.
9. Brunet A., Sweeney L.B., Sturgill J.F., Chua K.F., Greer P.L., Lin Y., Tran H., Ross S.E., Mostoslavsky R., Cohen H.Y., Hu L.S., Cheng H.L., Jedrychowski M.P., Gygi S.P., Sinclair D.A., Alt F.W., Greenberg M.E. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 2004, 303:2011-2015.
10. Chae H.D., Broxmeyer H.E. SIRT1 deficiency downregulates PTEN/JNK/FOXO1 pathway to block reactive oxygen species-induced apoptosis in mouse embryonic stem cells. Stem Cells Dev. 2011, 20:1277-1285.
11. Cherasse Y., Maurin A.C., Chaveroux C., Jousse C., Carraro V., Parry L., Deval C., Chambon C., Fafournoux P., Bruhat A. The p300/CBP-associated factor (PCAF) is a cofactor of ATF4 for amino acid-regulated transcription of CHOP. Nucleic Acids Res. 2007, 35:5954-5965.
12. Choudhary C., Kumar C., Gnad F., Nielsen M.L., Rehman M., Walther T.C., Olsen J.V., Mann M. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 2009, 325:834-840.
13. Christensen D.P., Dahllof M., Lundh M., Rasmussen D.N., Nielsen M.D., Billestrup N., Grunnet L.G., Mandrup-Poulsen T. Histone deacetylase (HDAC) inhibition as a novel treatment for diabetes mellitus. Mol. Med. 2011, 17:378-390.
14. Daitoku H., Hatta M., Matsuzaki H., Aratani S., Ohshima T., Miyagishi M., Nakajima T., Fukamizu A. Silent information regulator 2 potentiates Foxo1-mediated transcription through its deacetylase activity. Proc. Natl. Acad. Sci. USA 2004, 101:10042-10047.
15. Daitoku H., Sakamaki J., Fukamizu A. Regulation of FoxO transcription factors by acetylation and protein-protein interactions. Biochim. Biophys. Acta 2011, 1813:1954-1960.
16. DeBerardinis R.J., Thompson C.B. Cellular metabolism and disease: what do metabolic outliers teach us?. Cell 2012, 148:1132-1144.
17. Domon B., Aebersold R. Mass spectrometry and protein analysis. Science 2006, 312:212-217.
18. Du K., Herzig S., Kulkarni R.N., Montminy M. TRB3: a tribbles homolog that inhibits Akt/PKB activation by insulin in liver. Science 2003, 300:1574-1577.
19. Frescas D., Valenti L., Accili D. Nuclear trapping of the forkhead transcription factor FoxO1 via Sirt-dependent deacetylation promotes expression of glucogenetic genes. J. Biol. Chem. 2005, 280:20589-20595.
20. Frojdo S., Durand C., Molin L., Carey A.L., El-Osta A., Kingwell B.A., Febbraio M.A., Solari F., Vidal H., Pirola L. Phosphoinositide 3-kinase as a novel functional target for the regulation of the insulin signaling pathway by SIRT1. Mol. Cell. Endocrinol. 2011, 335:166-176.
21. Frye R.A. Characterization of five human cDNAs with homology to the yeast SIR2 gene: Sir2-like proteins (sirtuins) metabolize NAD and may have protein ADP-ribosyltransferase activity. Biochem. Biophys. Res. Commun. 1999, 260:273-279.
22. Frye R.A. Phylogenetic classification of prokaryotic and eukaryotic Sir2-like proteins. Biochem. Biophys. Res. Commun. 2000, 273:793-798.
23. Fukuoka M., Daitoku H., Hatta M., Matsuzaki H., Umemura S., Fukamizu A. Negative regulation of forkhead transcription factor AFX (Foxo4) by CBP-induced acetylation. Int. J. Mol. Med. 2003, 12:503-508.
24. Furuyama T., Kitayama K., Shimoda Y., Ogawa M., Sone K., Yoshida-Araki K., Hisatsune H., Nishikawa S., Nakayama K., Nakayama K., Ikeda K., Motoyama N., Mori N. Abnormal angiogenesis in Foxo1 (Fkhr)-deficient mice. J. Biol. Chem. 2004, 279:34741-34749.
25. Glidden E.J., Gray L.G., Vemuru S., Li D., Harris T.E., Mayo M.W. multiple site acetylation of rictor stimulates mammalian target of rapamycin complex 2 (mTORC2)-dependent phosphorylation of Akt protein. J. Biol. Chem. 2012, 287:581-588.
26. Gregoire S., Xiao L., Nie J., Zhang X., Xu M., Li J., Wong J., Seto E., Yang X.J. Histone deacetylase 3 interacts with and deacetylates myocyte enhancer factor 2. Mol. Cell. Biol. 2007, 27:1280-1295.
27. Gu W., Roeder R.G. Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell 1997, 90:595-606.
28. Guarente L. Sirtuins as potential targets for metabolic syndrome. Nature 2006, 444:868-874.
29. Guarente L. The logic linking protein acetylation and metabolism. Cell Metab. 2011, 14:151-153.
30. Haberland M., Montgomery R.L., Olson E.N. The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat. Rev. Genet. 2009, 10:32-42.
31. Hosaka T., Biggs W.H., Tieu D., Boyer A.D., Varki N.M., Cavenee W.K., Arden K.C. Disruption of forkhead transcription factor (FOXO) family members in mice reveals their functional diversification. Proc. Natl. Acad. Sci. USA 2004, 101:2975-2980.
32. Howitz K.T., Bitterman K.J., Cohen H.Y., Lamming D.W., Lavu S., Wood J.G., Zipkin R.E., Chung P., Kisielewski A., Zhang L.L., Scherer B., Sinclair D.A. Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature 2003, 425:191-196.
33. Hubbard S.R. Crystal structure of the activated insulin receptor tyrosine kinase in complex with peptide substrate and ATP analog. EMBO J. 1997, 16:5572-5581.
34. Ikenoue T., Inoki K., Zhao B., Guan K.L. PTEN acetylation modulates its interaction with PDZ domain. Cancer Res. 2008, 68:6908-6912.
35. Jing E., Gesta S., Kahn C.R. SIRT2 regulates adipocyte differentiation through FoxO1 acetylation/deacetylation. Cell Metab. 2007, 6:105-114.
36. Kaiser C., James S.R. Acetylation of insulin receptor substrate-1 is permissive for tyrosine phosphorylation. BMC Biol. 2004, 2:23.
37. Kim S.C., Sprung R., Chen Y., Xu Y., Ball H., Pei J., Cheng T., Kho Y., Xiao H., Xiao L., Grishin N.V., White M., Yang X.J., Zhao Y. Substrate and functional diversity of lysine acetylation revealed by a proteomics survey. Mol. Cell 2006, 23:607-618.
38. Kim W.J., Rivera M.N., Coffman E.J., Haber D.A. The WTX tumor suppressor enhances p53 acetylation by CBP/p300. Mol. Cell 2012, 45:587-597.
39. Lagouge M., Argmann C., Gerhart-Hines Z., Meziane H., Lerin C., Daussin F., Messadeq N., Milne J., Lambert P., Elliott P., Geny B., Laakso M., Puigserver P., Auwerx J. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell 2006, 127:1109-1122.
40. Levine A.J., Feng Z., Mak T.W., You H., Jin S. Coordination and communication between the p53 and IGF-1-AKT-TOR signal transduction pathways. Genes Dev. 2006, 20:267-275.
41. Li L., Wang L., Li L., Wang Z., Ho Y., McDonald T., Holyoake T.L., Chen W., Bhatia R. Activation of p53 by SIRT1 inhibition enhances elimination of CML leukemia stem cells in combination with imatinib. Cancer Cell 2012, 21:266-281.
42. Li T., Du Y., Wang L., Huang L., Li W., Lu M., Zhang X., Zhu W.G. Characterization and prediction of lysine (k)-acetyl-transferase specific acetylation sites. Mol. Cell Proteomics 2012, 11:M111011080.
43. Li Y., Xu W., McBurney M.W., Longo V.D. SirT1 inhibition reduces IGF-I/IRS-2/Ras/ERK1/2 signaling and protects neurons. Cell Metab. 2008, 8:38-48.
44. Liu X., Wang L., Zhao K., Thompson P.R., Hwang Y., Marmorstein R., Cole P.A. The structural basis of protein acetylation by the p300/CBP transcriptional coactivator. Nature 2008, 451:846-850.
45. Manning B.D., Cantley L.C. AKT/PKB signaling: navigating downstream. Cell 2007, 129:1261-1274.
46. Marmorstein R., Roth S.Y. Histone acetyltransferases: function, structure, and catalysis. Curr. Opin. Genet. Dev. 2001, 11:155-161.
47. Matsuzaki H., Daitoku H., Hatta M., Aoyama H., Yoshimochi K., Fukamizu A. Acetylation of Foxo1 alters its DNA-binding ability and sensitivity to phosphorylation. Proc. Natl. Acad. Sci. USA 2005, 102:11278-11283.
48. Mihaylova M.M., Vasquez D.S., Ravnskjaer K., Denechaud P.D., Yu R.T., Alvarez J.G., Downes M., Evans R.M., Montminy M., Shaw R.J. Class IIa histone deacetylases are hormone-activated regulators of FOXO and mammalian glucose homeostasis. Cell 2011, 145:607-621.
49. Motta M.C., Divecha N., Lemieux M., Kamel C., Chen D., Gu W., Bultsma Y., McBurney M., Guarente L. Mammalian SIRT1 represses forkhead transcription factors. Cell 2004, 116:551-563.
50. Moynihan K.A., Grimm A.A., Plueger M.M., Bernal-Mizrachi E., Ford E., Cras-Meneur C., Permutt M.A., Imai S. Increased dosage of mammalian Sir2 in pancreatic beta cells enhances glucose-stimulated insulin secretion in mice. Cell Metab. 2005, 2:105-117.
51. Musselman C.A., Kutateladze T.G. PHD fingers: epigenetic effectors and potential drug targets. Mol. Interv. 2009, 9:314-323.
52. Okumura K., Mendoza M., Bachoo R.M., DePinho R.A., Cavenee W.K., Furnari F.B. PCAF modulates PTEN activity. J. Biol. Chem. 2006, 281:26562-26568.
53. Perrot V., Rechler M.M. The coactivator p300 directly acetylates the forkhead transcription factor Foxo1 and stimulates Foxo1-induced transcription. Mol. Endocrinol. 2005, 19:2283-2298.
54. Pfluger P.T., Herranz D., Velasco-Miguel S., Serrano M., Tschop M.H. Sirt1 protects against high-fat diet-induced metabolic damage. Proc. Natl. Acad. Sci. USA 2008, 105:9793-9798.
55. Picard F., Kurtev M., Chung N., Topark-Ngarm A., Senawong T., Machado De Oliveira R., Leid M., McBurney M.W., Guarente L. Sirt1 promotes fat mobilization in white adipocytes by repressing PPAR-gamma. Nature 2004, 429:771-776.
56. Qiang L., Banks A.S., Accili D. Uncoupling of acetylation from phosphorylation regulates FoxO1 function independent of its subcellular localization. J. Biol. Chem. 2010, 285:27396-27401.
57. Rodgers J.T., Lerin C., Haas W., Gygi S.P., Spiegelman B.M., Puigserver P. Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1. Nature 2005, 434:113-118.
58. Santos-Rosa H., Valls E., Kouzarides T., Martinez-Balbas M. Mechanisms of P/CAF auto-acetylation. Nucleic Acids Res. 2003, 31:4285-4292.
59. Sarbassov D.D., Guertin D.A., Ali S.M., Sabatini D.M. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 2005, 307:1098-1101.
60. Schenk S., McCurdy C.E., Philp A., Chen M.Z., Holliday M.J., Bandyopadhyay G.K., Osborn O., Baar K., Olefsky J.M. Sirt1 enhances skeletal muscle insulin sensitivity in mice during caloric restriction. J. Clin. Invest. 2011, 121:4281-4288.
61. Senf S.M., Sandesara P.B., Reed S.A., Judge A.R. P300 acetyltransferase activity differentially regulates the localization and activity of the FOXO homologues in skeletal muscle. Am. J. Physiol. Cell Physiol. 2011, 300:C1490-1501.
62. Sengupta N., Seto E. Regulation of histone deacetylase activities. J. Cell. Biochem. 2004, 93:57-67.
63. Song H., Li C.W., Labaff A.M., Lim S.O., Li L.Y., Kan S.F., Chen Y., Zhang K., Lang J., Xie X., Wang Y., Huo L.F., Hsu S.C., Chen X., Zhao Y., Hung M.C. Acetylation of EGF receptor contributes to tumor cell resistance to histone deacetylase inhibitors. Biochem. Biophys. Res. Commun. 2011, 404:68-73.
64. Stephens L., Anderson K., Stokoe D., Erdjument-Bromage H., Painter G.F., Holmes A.B., Gaffney P.R., Reese C.B., McCormick F., Tempst P., Coadwell J., Hawkins P.T. Protein kinase B kinases that mediate phosphatidylinositol 3,4,5-trisphosphate-dependent activation of protein kinase B. Science 1998, 279:710-714.
65. Sun C., Zhang F., Ge X., Yan T., Chen X., Shi X., Zhai Q. SIRT1 improves insulin sensitivity under insulin-resistant conditions by repressing PTP1B. Cell Metab. 2007, 6:307-319.
66. Sun C., Zhou J. Trichostatin A improves insulin stimulated glucose utilization and insulin signaling transduction through the repression of HDAC2. Biochem. Pharmacol. 2008, 76:120-127.
67. Sun H., Tu X., Prisco M., Wu A., Casiburi I., Baserga R. Insulin-like growth factor I receptor signaling and nuclear translocation of insulin receptor substrates 1 and 2. Mol. Endocrinol. 2003, 17:472-486.
68. Sundaresan N.R., Pillai V.B., Wolfgeher D., Samant S., Vasudevan P., Parekh V., Raghuraman H., Cunningham J.M., Gupta M., Gupta M.P. The deacetylase SIRT1 promotes membrane localization and activation of Akt and PDK1 during tumorigenesis and cardiac hypertrophy. Sci. Signal. 2011, 4:ra46.
69. Tamguney T., Stokoe D. New insights into PTEN. J. Cell Sci. 2007, 120:4071-4079.
70. Tato I., Bartrons R., Ventura F., Rosa J.L. Amino acids activate mammalian target of rapamycin complex 2 (mTORC2) via PI3K/Akt signaling. J. Biol. Chem. 2011, 286:6128-6142.
71. van der Horst A., Tertoolen L.G., de Vries-Smits L.M., Frye R.A., Medema R.H., Burgering B.M. FOXO4 is acetylated upon peroxide stress and deacetylated by the longevity protein hSir2(SIRT1). J. Biol. Chem. 2004, 279:28873-28879.
72. Vaziri H., Dessain S.K., Ng Eaton E., Imai S.I., Frye R.A., Pandita T.K., Guarente L., Weinberg R.A. HSIR2(SIRT1) functions as an NAD-dependent p53 deacetylase. Cell 2001, 107:149-159.
73. Verdin E., Hirschey M.D., Finley L.W., Haigis M.C. Sirtuin regulation of mitochondria: energy production, apoptosis, and signaling. Trends Biochem. Sci. 2010, 35:669-675.
74. Wang B., Moya N., Niessen S., Hoover H., Mihaylova M.M., Shaw R.J., Yates J.R., Fischer W.H., Thomas J.B., Montminy M. A hormone-dependent module regulating energy balance. Cell 2011, 145:596-606.
75. Wang F., Tong Q. SIRT2 suppresses adipocyte differentiation by deacetylating FOXO1 and enhancing FOXO1's repressive interaction with PPARgamma. Mol. Biol. Cell 2009, 20:801-808.
76. Wang Q., Zhang Y., Yang C., Xiong H., Lin Y., Yao J., Li H., Xie L., Zhao W., Yao Y., Ning Z.B., Zeng R., Xiong Y., Guan K.L., Zhao S., Zhao G.P. Acetylation of metabolic enzymes coordinates carbon source utilization and metabolic flux. Science 2010, 327:1004-1007.
77. Yamauchi T., Oike Y., Kamon J., Waki H., Komeda K., Tsuchida A., Date Y., Li M.X., Miki H., Akanuma Y., Nagai R., Kimura S., Saheki T., Nakazato M., Naitoh T., Yamamura K., Kadowaki T. Increased insulin sensitivity despite lipodystrophy in Crebbp heterozygous mice. Nat. Genet. 2002, 30:221-226.
78. Yang T., Fu M., Pestell R., Sauve A.A. SIRT1 and endocrine signaling. Trends Endocrinol. Metab. 2006, 17:186-191.
79. Yang Y., Hou H., Haller E.M., Nicosia S.V., Bai W. Suppression of FOXO1 activity by FHL2 through SIRT1-mediated deacetylation. EMBO J. 2005, 24:1021-1032.
80. Yao X.H., Nyomba B.L. Hepatic insulin resistance induced by prenatal alcohol exposure is associated with reduced PTEN and TRB3 acetylation in adult rat offspring. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2008, 294:R1797-1806.
81. Zhang J. The direct involvement of SirT1 in insulin-induced insulin receptor substrate-2 tyrosine phosphorylation. J. Biol. Chem. 2007, 282:34356-34364.
82. Zhang M., Poplawski M., Yen K., Cheng H., Bloss E., Zhu X., Patel H., Mobbs C.V. Role of CBP and SATB-1 in aging, dietary restriction, and insulin-like signaling. PLoS Biol. 2009, 7:e1000245.
83. Zhang Q., Zeng S.X., Zhang Y., Zhang Y., Ding D., Ye Q., Meroueh S.O., Lu H. A small molecule Inauhzin inhibits SIRT1 activity and suppresses tumour growth through activation of p53. EMBO Mol. Med. 2012, 4:298-312.
84. Zhao S., Xu W., Jiang W., Yu W., Lin Y., Zhang T., Yao J., Zhou L., Zeng Y., Li H., Li Y., Shi J., An W., Hancock S.M., He F., Qin L., Chin J., Yang P., Chen X., Lei Q., Xiong Y., Guan K.L. Regulation of cellular metabolism by protein lysine acetylation. Science 2010, 327:1000-1004.
85. Zhao Y., Wang Y., Zhu W.G. Applications of post-translational modifications of FoxO family proteins in biological functions. J. Mol. Cell Biol. 2011, 3:276-282.
86. Zhou X.Y., Shibusawa N., Naik K., Porras D., Temple K., Ou H., Kaihara K., Roe M.W., Brady M.J., Wondisford F.E. Insulin regulation of hepatic gluconeogenesis through phosphorylation of CREB-binding protein. Nat. Med. 2004, 10:633-637.