Reconstruction of insulin signal flow from phosphoproteome and metabolome data

Cell Reports

Volumn 8, Issue 4, 2014, Pages 1171-1183

  Yugi, Katsuyuki ^a   Kubota, Hiroyuki ^a,c,e   Toyoshima, Yu ^a   Noguchi, Rei ^a   Kawata, Kentaro ^a   Komori, Yasunori ^a   Uda, Shinsuke ^a,c   Kunida, Katsuyuki ^a   Tomizawa, Yoko ^a   Funato, Yosuke ^b   Miki, Hiroaki ^b   Matsumoto, Masaki ^c   Nakayama, Keiichi I ^c   Kashikura, Kasumi ^d   Endo, Keiko ^d   Ikeda, Kazutaka ^d   Soga, Tomoyoshi ^d   Kuroda, Shinya ^a,e  

^a UNIVERSITY OF TOKYO   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c KYUSHU UNIVERSITY   (Japan)

^d KEIO UNIVERSITY   (Japan)

^e JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

1 PHOSPHOFRUCTOKINASE; INSULIN; 2 OXOGLUTARIC ACID; 6 PHOSPHOFRUCTOKINASE; CITRIC ACID; CYCLIC AMP DEPENDENT PROTEIN KINASE; FRUCTOSE 1,6 BISPHOSPHATE; FRUCTOSE 6 PHOSPHATE; FUMARIC ACID; GLUCOSE 6 PHOSPHATASE; GLYCERALDEHYDE 3 PHOSPHATE; GLYCOGEN SYNTHASE KINASE 3BETA; MALIC ACID; PHOSPHOENOLPYRUVATE; PROTEIN KINASE B; PROTEIN KINASE C; S6 KINASE; SUCCINYL COENZYME A; PHOSPHOPROTEIN; PROTEOME;

ALLOSTERISM; ANIMAL CELL; ARTICLE; CELL METABOLISM; GLYCOLYSIS; HOMEOSTASIS; HORMONE ACTION; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; METABOLIC REGULATION; METABOLOME; METABOLOMICS; MOLECULAR INTERACTION; NONHUMAN; PHOSPHOPROTEOMICS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEOMICS; RAT; ANIMAL EXPERIMENT; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; HUMAN TISSUE; INSULIN METABOLISM; LIVER CELL CARCINOMA; PROTEIN DATABASE; PROTEIN FUNCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; ANIMAL; HEK293 CELL LINE; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN PROCESSING; TUMOR CELL LINE;

ALLOSTERIC REGULATION; ANIMALS; CELL LINE, TUMOR; HEK293 CELLS; HUMANS; INSULIN; METABOLIC NETWORKS AND PATHWAYS; METABOLOME; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOME; RATS; SIGNAL TRANSDUCTION;

EID: 84908356647     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.07.021     Document Type: Article

References (62)

1. Alves R., Chaleil R.A., Sternberg M.J. Evolution of enzymes in metabolism: a network perspective. J.Mol. Biol. 2002, 320:751-770.
2. Atsumi T., Nishio T., Niwa H., Takeuchi J., Bando H., Shimizu C., Yoshioka N., Bucala R., Koike T. Expression of inducible 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase/PFKFB3 isoforms in adipocytes and their potential role in glycolytic regulation. Diabetes 2005, 54:3349-3357.
3. Bartke T., Vermeulen M., Xhemalce B., Robson S.C., Mann M., Kouzarides T. Nucleosome-interacting proteins regulated by DNA and histone methylation. Cell 2010, 143:470-484.
4. Bennett B.D., Kimball E.H., Gao M., Osterhout R., Van Dien S.J., Rabinowitz J.D. Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli. Nat. Chem. Biol. 2009, 5:593-599.
5. Bertone P., Stolc V., Royce T.E., Rozowsky J.S., Urban A.E., Zhu X., Rinn J.L., Tongprasit W., Samanta M., Weissman S., et al. Global identification of human transcribed sequences with genome tiling arrays. Science 2004, 306:2242-2246.
6. Berwick D.C., Hers I., Heesom K.J., Moule S.K., Tavare J.M. The identification of ATP-citrate lyase as a protein kinase B (Akt) substrate in primary adipocytes. J.Biol. Chem. 2002, 277:33895-33900.
7. Bloxham D.P., Lardy H.A. Phosphofructokinase. The Enzymes 1973, 239-278. Academic Press, New York. P.B. Boyer (Ed.).
8. Brabant G., Prank K., Schofl C. Pulsatile patterns in hormone secretion. Trends Endocrinol. Metab. 1992, 3:183-190.
9. Brazhnik P., de la Fuente A., Mendes P. Gene networks: how to put the function in genomics. Trends Biotechnol. 2002, 20:467-472.
10. Buescher J.M., Liebermeister W., Jules M., Uhr M., Muntel J., Botella E., Hessling B., Kleijn R.J., Le Chat L., Lecointe F., et al. Global network reorganization during dynamic adaptations of Bacillus subtilis metabolism. Science 2012, 335:1099-1103.
11. Camacho D., de la Fuente A., Mendes P. The origin of correlations in metabolomics data. Metabolomics 2005, 1:53-63.
12. Cheng Z., Tseng Y., White M.F. Insulin signaling meets mitochondria in metabolism. Trends Endocrinol. Metab. 2010, 21:589-598.
13. Feist A.M., Herrgård M.J., Thiele I., Reed J.L., Palsson B.O. Reconstruction of biochemical networks in microorganisms. Nat. Rev. Microbiol. 2009, 7:129-143.
14. Fiehn O., Kopka J., Dörmann P., Altmann T., Trethewey R.N., Willmitzer L. Metabolite profiling for plant functional genomics. Nat. Biotechnol. 2000, 18:1157-1161.
15. Fischer E., Sauer U. Large-scale invivo flux analysis shows rigidity and suboptimal performance of Bacillus subtilis metabolism. Nat. Genet. 2005, 37:636-640.
16. Friedman A.A., Tucker G., Singh R., Yan D., Vinayagam A., Hu Y., Binari R., Hong P., Sun X., Porto M., et al. Proteomic and functional genomic landscape of receptor tyrosine kinase and ras to extracellular signal-regulated kinase signaling. Sci. Signal. 2011, 4:rs10.
17. Gerosa L., Sauer U. Regulation and control of metabolic fluxes in microbes. Curr. Opin. Biotechnol. 2011, 22:566-575.
18. Ghaemmaghami S., Huh W.K., Bower K., Howson R.W., Belle A., Dephoure N., O'Shea E.K., Weissman J.S. Global analysis of protein expression in yeast. Nature 2003, 425:737-741.
19. Güell M., van Noort V., Yus E., Chen W.H., Leigh-Bell J., Michalodimitrakis K., Yamada T., Arumugam M., Doerks T., Kühner S., et al. Transcriptome complexity in a genome-reduced bacterium. Science 2009, 326:1268-1271.
20. Hornbeck P.V., Kornhauser J.M., Tkachev S., Zhang B., Skrzypek E., Murray B., Latham V., Sullivan M. PhosphoSitePlus: a comprehensive resource for investigating the structure and function of experimentally determined post-translational modifications in man and mouse. Nucleic Acids Res. 2012, 40:D261-D270.
21. Hsu P.P., Kang S.A., Rameseder J., Zhang Y., Ottina K.A., Lim D., Peterson T.R., Choi Y., Gray N.S., Yaffe M.B., et al. The mTOR-regulated phosphoproteome reveals a mechanism of mTORC1-mediated inhibition of growth factor signaling. Science 2011, 332:1317-1322.
22. Humphrey S.J., Yang G., Yang P., Fazakerley D.J., Stöckli J., Yang J.Y., James D.E. Dynamic adipocyte phosphoproteome reveals that Akt directly regulates mTORC2. Cell Metab. 2013, 17:1009-1020.
23. Ishihama Y., Sato T., Tabata T., Miyamoto N., Sagane K., Nagasu T., Oda Y. Quantitative mouse brain proteomics using culture-derived isotope tags as internal standards. Nat. Biotechnol. 2005, 23:617-621.
24. Ishii N., Nakahigashi K., Baba T., Robert M., Soga T., Kanai A., Hirasawa T., Naba M., Hirai K., Hoque A., et al. Multiple high-throughput analyses monitor the response of E.coli to perturbations. Science 2007, 316:593-597.
25. IUPAC-IUBMB Joint Commission on Biochemical Nomenclature (JCBN) and Nomenclature Committee of IUBMB (NC-IUBMB), newsletter 1999. Eur. J. Biochem. 1999, 264:607-609. IUBMB.
26. Iwasaki M., Miwa S., Ikegami T., Tomita M., Tanaka N., Ishihama Y. One-dimensional capillary liquid chromatographic separation coupled with tandem mass spectrometry unveils the Escherichia coli proteome on a microarray scale. Anal. Chem. 2010, 82:2616-2620.
27. Jørgensen C., Sherman A., Chen G.I., Pasculescu A., Poliakov A., Hsiung M., Larsen B., Wilkinson D.G., Linding R., Pawson T. Cell-specificinformation processing in segregating populations of Eph receptor ephrin-expressing cells. Science 2009, 326:1502-1509.
28. Joughin B.A., Liu C., Lauffenburger D.A., Hogue C.W., Yaffe M.B. Protein kinases display minimal interpositional dependence on substrate sequence: potential implications for the evolution of signalling networks. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2012, 367:2574-2583.
29. Joyce A.R., Palsson B.O. The model organism as a system: integrating 'omics' data sets. Nat. Rev. Mol. Cell Biol. 2006, 7:198-210.
30. Kanehisa M., Goto S., Sato Y., Furumichi M., Tanabe M. KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res. 2012, 40:D109-D114.
31. Kubota H., Noguchi R., Toyoshima Y., Ozaki Y., Uda S., Watanabe K., Ogawa W., Kuroda S. Temporal coding of insulin action through multiplexing of the AKT pathway. Mol. Cell 2012, 46:820-832.
32. Kühner S., van Noort V., Betts M.J., Leo-Macias A., Batisse C., Rode M., Yamada T., Maier T., Bader S., Beltran-Alvarez P., et al. Proteome organization in a genome-reduced bacterium. Science 2009, 326:1235-1240.
33. Li C., Donizelli M., Rodriguez N., Dharuri H., Endler L., Chelliah V., Li L., He E., Henry A., Stefan M.I., et al. BioModels Database: An enhanced, curated and annotated resource for published quantitative kinetic models. BMC Syst. Biol. 2010, 4:92.
34. Linding R., Jensen L.J., Ostheimer G.J., van Vugt M.A., Jørgensen C., Miron I.M., Diella F., Colwill K., Taylor L., Elder K., et al. Systematic discovery of invivo phosphorylation networks. Cell 2007, 129:1415-1426.
35. Lindsay J.R., McKillop A.M., Mooney M.H., Flatt P.R., Bell P.M., O'harte F.P. Meal-induced 24-hour profile of circulating glycated insulin in type 2 diabetic subjects measured by a novel radioimmunoassay. Metabolism 2003, 52:631-635.
36. Link H., Kochanowski K., Sauer U. Systematic identification of allosteric protein-metabolite interactions that control enzyme activity invivo. Nat. Biotechnol. 2013, 31:357-361.
37. Locasale J.W., Grassian A.R., Melman T., Lyssiotis C.A., Mattaini K.R., Bass A.J., Heffron G., Metallo C.M., Muranen T., Sharfi H., et al. Phosphoglycerate dehydrogenase diverts glycolytic flux and contributes to oncogenesis. Nat. Genet. 2011, 43:869-874.
38. Lowery D.M., Clauser K.R., Hjerrild M., Lim D., Alexander J., Kishi K., Ong S.E., Gammeltoft S., Carr S.A., Yaffe M.B. Proteomic screen defines the Polo-box domain interactome and identifies Rock2 as a Plk1 substrate. EMBO J. 2007, 26:2262-2273.
39. Miller M.L., Jensen L.J., Diella F., Jørgensen C., Tinti M., Li L., Hsiung M., Parker S.A., Bordeaux J., Sicheritz-Ponten T., et al. Linear motif atlas for phosphorylation-dependent signaling. Sci. Signal. 2008, 1:ra2.
40. Monetti M., Nagaraj N., Sharma K., Mann M. Large-scale phosphosite quantification in tissues by a spike-in SILAC method. Nat. Methods 2011, 8:655-658.
41. Mor I., Cheung E.C., Vousden K.H. Control of glycolysis through regulation of PFK1: old friends and recent additions. Cold Spring Harb. Symp. Quant. Biol. 2011, 76:211-216.
42. Nilsson T., Mann M., Aebersold R., Yates J.R., Bairoch A., Bergeron J.J. Mass spectrometry in high-throughput proteomics: ready for the big time. Nat. Methods 2010, 7:681-685.
43. Nimmo H.G., Tipton K.F. The purification of fructose 1,6-diphosphatase from ox liver and its activation by ethylenediaminetetra-acetate. Biochem. J. 1975, 145:323-334.
44. Noguchi R., Kubota H., Yugi K., Toyoshima Y., Komori Y., Soga T., Kuroda S. The selective control of glycolysis, gluconeogenesis and glycogenesis by temporal insulin patterns. Mol. Syst. Biol. 2013, 9:664.
45. O'Connell B.C., Adamson B., Lydeard J.R., Sowa M.E., Ciccia A., Bredemeyer A.L., Schlabach M., Gygi S.P., Elledge S.J., Harper J.W. A genome-wide camptothecin sensitivity screen identifies a mammalian MMS22L-NFKBIL2 complex required for genomic stability. Mol. Cell 2010, 40:645-657.
46. Oliveira A.P., Ludwig C., Picotti P., Kogadeeva M., Aebersold R., Sauer U. Regulation of yeast central metabolism by enzyme phosphorylation. Mol. Syst. Biol. 2012, 8:623.
47. Olsen J.V., Blagoev B., Gnad F., Macek B., Kumar C., Mortensen P., Mann M. Global, invivo, and site-specific phosphorylation dynamics in signaling networks. Cell 2006, 127:635-648.
48. Palsson B. Systems biology: simulation of dynamic network states 2011, Cambridge University Press, Cambridge.
49. Passonneau J.V., Lowry O.H. P-Fructokinase and the control of the citric acid cycle. Biochem. Biophys. Res. Commun. 1963, 13:372-379.
50. Polonsky K.S., Given B.D., Van Cauter E. Twenty-four-hour profiles and pulsatile patterns of insulin secretion in normal and obese subjects. J.Clin. Invest. 1988, 81:442-448.
51. Rakus D., Skalecki K., Dzugaj A. Kinetic properties of pig (Susscrofa domestica) and bovine (Bos taurus) D-fructose-1,6-bisphosphate 1-phosphohydrolase (F1,6BPase): liver-like isozymes in mammalian lung tissue. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2000, 127:123-134.
52. Rider M.H., Bertrand L., Vertommen D., Michels P.A., Rousseau G.G., Hue L. 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase: head-to-head with a bifunctional enzyme that controls glycolysis. Biochem. J. 2004, 381:561-579.
53. Schomburg I., Chang A., Placzek S., Söhngen C., Rother M., Lang M., Munaretto C., Ulas S., Stelzer M., Grote A., et al. BRENDA in 2013: integrated reactions, kinetic data, enzyme function data, improved disease classification: new options and contents in BRENDA. Nucleic Acids Res. 2013, 41:D764-D772.
54. Schöneberg T., Kloos M., Brüser A., Kirchberger J., Sträter N. Structure and allosteric regulation of eukaryotic 6-phosphofructokinases. Biol. Chem. 2013, 394:977-993.
55. Shyh-Chang N., Locasale J.W., Lyssiotis C.A., Zheng Y., Teo R.Y., Ratanasirintrawoot S., Zhang J., Onder T., Unternaehrer J.J., Zhu H., et al. Influence of threonine metabolism on S-adenosylmethionine and histone methylation. Science 2013, 339:222-226.
56. Simpson C.J., Fothergill-Gilmore L.A. Isolation and sequence of a cDNA encoding human platelet phosphofructokinase. Biochem. Biophys. Res. Commun. 1991, 180:197-203.
57. Soga T., Ueno Y., Naraoka H., Ohashi Y., Tomita M., Nishioka T. Simultaneous determination of anionic intermediates for Bacillus subtilis metabolic pathways by capillary electrophoresis electrospray ionization mass spectrometry. Anal. Chem. 2002, 74:2233-2239.
58. Vander Heiden M.G., Locasale J.W., Swanson K.D., Sharfi H., Heffron G.J., Amador-Noguez D., Christofk H.R., Wagner G., Rabinowitz J.D., Asara J.M., Cantley L.C. Evidence for an alternative glycolytic pathway in rapidly proliferating cells. Science 2010, 329:1492-1499.
59. Whiteman E.L., Cho H., Birnbaum M.J. Role of Akt/protein kinase B in metabolism. Trends Endocrinol. Metab. 2002, 13:444-451.
60. Wiley H.S. Integrating multiple types of data for signaling research: challenges and opportunities. Sci. Signal. 2011, 4:pe9.
61. Wittmann C., Hans M., van Winden W.A., Ras C., Heijnen J.J. Dynamics of intracellular metabolites of glycolysis and TCA cycle during cell-cycle-related oscillation in Saccharomyces cerevisiae. Biotechnol. Bioeng. 2005, 89:839-847.
62. Yus E., Maier T., Michalodimitrakis K., van Noort V., Yamada T., Chen W.H., Wodke J.A., Güell M., Martínez S., Bourgeois R., et al. Impact of genome reduction on bacterial metabolism and its regulation. Science 2009, 326:1263-1268.