Phosphoproteomic profiling of in vivo signaling in liver by the mammalian target of rapamycin complex 1 (mTORC1)

PLoS ONE

Volumn 6, Issue 6, 2011, Pages

  Demirkan, Gokhan ^a,b   Yu, Kebing ^b,c   Boylan, Joan M ^a   Salomon, Arthur R ^b,c   Gruppuso, Philip A ^a,b  

^a BROWN UNIVERSITY   (United States)

^b BROWN UNIVERSITY   (United States)

^c BROWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE KINASE; ADENYLATE KINASE 2; GEPHYRIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; PHOSPHOPROTEIN; PROLINE RICH PROTEIN; PROTEIN PRAS40; RAPAMYCIN; UNCLASSIFIED DRUG; TARGET OF RAPAMYCIN KINASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; FUNCTIONAL PROTEOMICS; HUMAN; HUMAN CELL; IN VIVO STUDY; LIVER HOMOGENATE; MALE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; RAT; REFEEDING; SIGNAL TRANSDUCTION; STARVATION; ANIMAL; LIVER; MASS SPECTROMETRY; METABOLISM; METHODOLOGY; PROTEOMICS; SPRAGUE DAWLEY RAT;

MAMMALIA; RATTUS;

ANIMALS; LIVER; MALE; MASS SPECTROMETRY; PHOSPHOPROTEINS; PROTEOMICS; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 79959597793     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0021729     Document Type: Article

References (76)

1. Wullschleger S, Loewith R, Hall MN, (2006) TOR signaling in growth and metabolism. Cell 124: 471-484.
2. Alessi DR, Pearce LR, Garcia-Martinez JM, (2009) New insights into mTOR signaling: mTORC2 and beyond. Sci Signal 2: e27.
3. Dunlop EA, Tee AR, (2009) Mammalian target of rapamycin complex 1: signalling inputs, substrates and feedback mechanisms. Cell Signal 21: 827-835.
4. Guertin DA, Sabatini DM, (2009) The pharmacology of mTOR inhibition. Sci Signal 2: e24.
5. Abraham RT, (2002) Identification of TOR signaling complexes: more TORC for the cell growth engine. Cell 111: 9-12.
6. Hay N, Sonenberg N, (2004) Upstream and downstream of mTOR. Genes Dev 18: 1926-1945.
7. Foster KG, Fingar DC, (2010) Mammalian target of rapamycin (mTOR): conducting the cellular signaling symphony. J Biol Chem 285: 14071-14077.
8. Hidalgo M, Rowinsky EK, (2000) The rapamycin-sensitive signal transduction pathway as a target for cancer therapy. Oncogene 19: 6680-6686.
9. Loewith R, Jacinto E, Wullschleger S, Lorberg A, Crespo JL, et al. (2002) Two TOR complexes, only one of which is rapamycin sensitive, have distinct roles in cell growth control. Mol Cell 10: 457-468.
10. Wool IG, (1979) The structure and function of eukaryotic ribosomes. Annu Rev Biochem 48: 719-754.
11. Gingras AC, Raught B, Sonenberg N, (2004) mTOR signaling to translation. Curr Top Microbiol Immunol 279: 169-197.
12. Ma XM, Blenis J, (2009) Molecular mechanisms of mTOR-mediated translational control. Nat Rev Mol Cell Biol 10: 307-318.
13. Nojima H, Tokunaga C, Eguchi S, Oshiro N, Hidayat S, et al. (2003) The mammalian target of rapamycin (mTOR) partner, raptor, binds the mTOR substrates p70 S6 kinase and 4E-BP1 through their TOR signaling (TOS) motif. J Biol Chem 278: 15461-15464.
14. Choo AY, Blenis J, (2009) Not all substrates are treated equally: implications for mTOR, rapamycin-resistance and cancer therapy. Cell Cycle 8: 567-572.
15. Efeyan A, Sabatini DM, (2010) mTOR and cancer: many loops in one pathway. Curr Opin Cell Biol 22: 169-176.
16. Polak P, Hall MN, (2009) mTOR and the control of whole body metabolism. Curr Opin Cell Biol 21: 209-218.
17. Anand P, Gruppuso PA, (2005) The regulation of hepatic protein synthesis during fasting in the rat. J Biol Chem 280: 16427-16436.
18. Anand P, Gruppuso PA, (2006) Rapamycin inhibits liver growth during refeeding in rats via control of ribosomal protein translation but not cap-dependent translation initiation. J Nutr 136: 27-33.
19. Jin WH, Dai J, Zhou H, Xia QC, Zou HF, et al. (2004) Phosphoproteome analysis of mouse liver using immobilized metal affinity purification and linear ion trap mass spectrometry. Rapid Commun Mass Spectrom 18: 2169-2176.
20. Moser K, White FM, (2006) Phosphoproteomic analysis of rat liver by high capacity IMAC and LC-MS/MS. J Proteome Res 5: 98-104.
21. Villen J, Beausoleil SA, Gerber SA, Gygi SP, (2007) Large-scale phosphorylation analysis of mouse liver. Proc Natl Acad Sci U S A 104: 1488-1493.
22. Han G, Ye M, Zhou H, Jiang X, Feng S, et al. (2008) Large-scale phosphoproteome analysis of human liver tissue by enrichment and fractionation of phosphopeptides with strong anion exchange chromatography. Proteomics 8: 1346-1361.
23. Han G, Ye M, Liu H, Song C, Sun D, et al. (2010) Phosphoproteome analysis of human liver tissue by long-gradient nanoflow LC coupled with multiple stage MS analysis. Electrophoresis 31: 1080-1089.
24. Salomon AR, Ficarro SB, Brill LM, Brinker A, Phung QT, et al. (2003) Profiling of tyrosine phosphorylation pathways in human cells using mass spectrometry. Proc Natl Acad Sci U S A 100: 443-448.
25. Zhang Y, Wolf-Yadlin A, Ross PL, Pappin DJ, Rush J, et al. (2005) Time-resolved mass spectrometry of tyrosine phosphorylation sites in the epidermal growth factor receptor signaling network reveals dynamic modules. Mol Cell Proteomics 4: 1240-1250.
26. Cao L, Yu K, Salomon AR, (2006) Phosphoproteomic analysis of lymphocyte signaling. Adv Exp Med Biol 584: 277-288.
27. Gronborg M, Kristiansen TZ, Stensballe A, Andersen JS, Ohara O, et al. (2002) A mass spectrometry-based proteomic approach for identification of serine/threonine-phosphorylated proteins by enrichment with phospho-specific antibodies: identification of a novel protein, Frigg, as a protein kinase A substrate. Mol Cell Proteomics 1: 517-527.
28. Villen J, Gygi SP, (2008) The SCX/IMAC enrichment approach for global phosphorylation analysis by mass spectrometry. Nat Protoc 3: 1630-1638.
29. Kweon HK, Hakansson K, (2006) Selective zirconium dioxide-based enrichment of phosphorylated peptides for mass spectrometric analysis. Anal Chem 78: 1743-1749.
30. Larsen MR, Thingholm TE, Jensen ON, Roepstorff P, Jorgensen TJ, (2005) Highly selective enrichment of phosphorylated peptides from peptide mixtures using titanium dioxide microcolumns. Mol Cell Proteomics 4: 873-886.
31. Wolschin F, Wienkoop S, Weckwerth W, (2005) Enrichment of phosphorylated proteins and peptides from complex mixtures using metal oxide/hydroxide affinity chromatography (MOAC). Proteomics 5: 4389-4397.
32. Hubbard MJ, Cohen P, (1993) On target with a new mechanism for the regulation of protein phosphorylation. Trends Biochem Sci 18: 172-177.
33. Olsen JV, Blagoev B, Gnad F, Macek B, Kumar C, et al. (2006) Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127: 635-648.
34. Thingholm TE, Jorgensen TJ, Jensen ON, Larsen MR, (2006) Highly selective enrichment of phosphorylated peptides using titanium dioxide. Nat Protoc 1: 1929-1935.
35. Huber A, Bodenmiller B, Uotila A, Stahl M, Wanka S, et al. (2009) Characterization of the rapamycin-sensitive phosphoproteome reveals that Sch9 is a central coordinator of protein synthesis. Genes Dev 23: 1929-1943.
36. Yu K, Salomon AR, (2009) PeptideDepot: flexible relational database for visual analysis of quantitative proteomic data and integration of existing protein information. Proteomics 9: 5350-5358.
37. Yu K, Sabelli A, DeKeukelaere L, Park R, Sindi S, et al. (2009) Integrated platform for manual and high-throughput statistical validation of tandem mass spectra. Proteomics 9: 3115-3125.
38. Yu K, Salomon AR, (2010) HTAPP: high-throughput autonomous proteomic pipeline. Proteomics 10: 2113-2122.
39. Cao L, Yu K, Banh C, Nguyen V, Ritz A, et al. (2007) Quantitative time-resolved phosphoproteomic analysis of mast cell signaling. J Immunol 179: 5864-5876.
40. Nguyen V, Cao L, Lin JT, Hung N, Ritz A, et al. (2009) A new approach for quantitative phosphoproteomic dissection of signaling pathways applied to T cell receptor activation. Mol Cell Proteomics 8: 2418-2431.
41. Ficarro SB, Salomon AR, Brill LM, Mason DE, Stettler-Gill M, et al. (2005) Automated immobilized metal affinity chromatography/nano-liquid chromatography/electrospray ionization mass spectrometry platform for profiling protein phosphorylation sites. Rapid Commun Mass Spectrom 19: 57-71.
42. Elias JE, Gygi SP, (2010) Target-decoy search strategy for mass spectrometry-based proteomics. Methods Mol Biol 604: 55-71.
43. Beausoleil SA, Villen J, Gerber SA, Rush J, Gygi SP, (2006) A probability-based approach for high-throughput protein phosphorylation analysis and site localization. Nat Biotechnol 24: 1285-1292.
44. Beausoleil SA, Jedrychowski M, Schwartz D, Elias JE, Villen J, et al. (2004) Large-scale characterization of HeLa cell nuclear phosphoproteins. Proc Natl Acad Sci U S A 101: 12130-12135.
45. Sugiyama N, Masuda T, Shinoda K, Nakamura A, Tomita M, et al. (2007) Phosphopeptide enrichment by aliphatic hydroxy acid-modified metal oxide chromatography for nano-LC-MS/MS in proteomics applications. Mol Cell Proteomics 6: 1103-1109.
46. Kyono Y, Sugiyama N, Imami K, Tomita M, Ishihama Y, (2008) Successive and selective release of phosphorylated peptides captured by hydroxy acid-modified metal oxide chromatography. J Proteome Res 7: 4585-4593.
47. Bronshtein IN, Semendyayev KA, Musoil G, Muehlig H, (2004) Handbook of Mathematics New York Springer-Verlag.
48. Chen RQ, Yang QK, Lu BW, Yi W, Cantin G, et al. (2009) CDC25B mediates rapamycin-induced oncogenic responses in cancer cells. Cancer Res 69: 2663-2668.
49. Foster KG, Acosta-Jaquez HA, Romeo Y, Ekim B, Soliman GA, et al. (2010) Regulation of mTOR complex 1 (mTORC1) by raptor Ser863 and multisite phosphorylation. J Biol Chem 285: 80-94.
50. Shor B, Wu J, Shakey Q, Toral-Barza L, Shi C, et al. (2010) Requirement of the mTOR kinase for the regulation of Maf1 phosphorylation and control of RNA polymerase III-dependent transcription in cancer cells. J Biol Chem 285: 15380-15392.
51. Keranen LM, Dutil EM, Newton AC, (1995) Protein kinase C is regulated in vivo by three functionally distinct phosphorylations. Curr Biol 5: 1394-1403.
52. Dalby KN, Morrice N, Caudwell FB, Avruch J, Cohen P, (1998) Identification of regulatory phosphorylation sites in mitogen-activated protein kinase (MAPK)-activated protein kinase-1a/p90rsk that are inducible by MAPK. J Biol Chem 273: 1496-1505.
53. Wang L, Harris TE, Lawrence JC, (2008) Regulation of proline-rich Akt substrate of 40 kDa (PRAS40) function by mammalian target of rapamycin complex 1 (mTORC1)-mediated phosphorylation. J Biol Chem 283: 15619-15627.
54. Sabatini DM, Barrow RK, Blackshaw S, Burnett PE, Lai MM, et al. (1999) Interaction of RAFT1 with gephyrin required for rapamycin-sensitive signaling. Science 284: 1161-1164.
55. Cheng SW, Fryer LG, Carling D, Shepherd PR, (2004) Thr2446 is a novel mammalian target of rapamycin (mTOR) phosphorylation site regulated by nutrient status. J Biol Chem 279: 15719-15722.
56. Vander HE, Lee SI, Bandhakavi S, Griffin TJ, Kim DH, (2007) Insulin signalling to mTOR mediated by the Akt/PKB substrate PRAS40. Nat Cell Biol 9: 316-323.
57. Prasad TS, Kandasamy K, Pandey A, (2009) Human Protein Reference Database and Human Proteinpedia as discovery tools for systems biology. Methods Mol Biol 577: 67-79.
58. Xia Q, Cheng D, Duong DM, Gearing M, Lah JJ, et al. (2008) Phosphoproteomic analysis of human brain by calcium phosphate precipitation and mass spectrometry. J Proteome Res 7: 2845-2851.
59. Zanivan S, Gnad F, Wickstrom SA, Geiger T, Macek B, et al. (2008) Solid tumor proteome and phosphoproteome analysis by high resolution mass spectrometry. J Proteome Res 7: 5314-5326.
60. Liao L, McClatchy DB, Park SK, Xu T, Lu B, et al. (2008) Quantitative analysis of brain nuclear phosphoproteins identifies developmentally regulated phosphorylation events. J Proteome Res 7: 4743-4755.
61. Alcolea MP, Kleiner O, Cutillas PR, (2009) Increased confidence in large-scale phosphoproteomics data by complementary mass spectrometric techniques and matching of phosphopeptide data sets. J Proteome Res 8: 3808-3815.
62. Wu J, Warren P, Shakey Q, Sousa E, Hill A, et al. (2010) Integrating titania enrichment, iTRAQ labeling, and Orbitrap CID-HCD for global identification and quantitative analysis of phosphopeptides. Proteomics 10: 2224-2234.
63. Hunter T, Sefton BM, (1980) Transforming gene product of Rous sarcoma virus phosphorylates tyrosine. Proc Natl Acad Sci U S A 77: 1311-1315.
64. Mayeur GL, Fraser CS, Peiretti F, Block KL, Hershey JW, (2003) Characterization of eIF3k: a newly discovered subunit of mammalian translation initiation factor elF3. Eur J Biochem 270: 4133-4139.
65. Holz MK, Ballif BA, Gygi SP, Blenis J, (2005) mTOR and S6K1 mediate assembly of the translation preinitiation complex through dynamic protein interchange and ordered phosphorylation events. Cell 123: 569-580.
66. Morishita R, Kawagoshi A, Sawasaki T, Madin K, Ogasawara T, et al. (1999) Ribonuclease activity of rat liver perchloric acid-soluble protein, a potent inhibitor of protein synthesis. J Biol Chem 274: 20688-20692.
67. Oka T, Tsuji H, Noda C, Sakai K, Hong YM, et al. (1995) Isolation and characterization of a novel perchloric acid-soluble protein inhibiting cell-free protein synthesis. J Biol Chem 270: 30060-30067.
68. Kimura N, Tokunaga C, Dalal S, Richardson C, Yoshino K, et al. (2003) A possible linkage between AMP-activated protein kinase (AMPK) and mammalian target of rapamycin (mTOR) signalling pathway. Genes Cells 8: 65-79.
69. Gruppuso PA, Tsai SW, Boylan JM, Sanders JA, (2008) Hepatic translation control in the late-gestation fetal rat. Am J Physiol Regul Integr Comp Physiol 295: R558-R567.
70. Hall MN, (2008) mTOR-what does it do? Transplant Proc 40: S5-S8.
71. Choo AY, Yoon SO, Kim SG, Roux PP, Blenis J, (2008) Rapamycin differentially inhibits S6Ks and 4E-BP1 to mediate cell-type-specific repression of mRNA translation. Proc Natl Acad Sci U S A 105: 17414-17419.
72. Dowling RJ, Topisirovic I, Alain T, Bidinosti M, Fonseca BD, et al. (2010) mTORC1-mediated cell proliferation, but not cell growth, controlled by the 4E-BPs. Science 328: 1172-1176.
73. Thingholm TE, Jensen ON, Larsen MR, (2009) Analytical strategies for phosphoproteomics. Proteomics 9: 1451-1468.
74. Wu J, Warren P, Shakey Q, Sousa E, Hill A, et al. (2010) Integrating titania enrichment, iTRAQ labeling, and Orbitrap CID-HCD for global identification and quantitative analysis of phosphopeptides. Proteomics 10: 2224-2234.
75. Lemeer S, Heck AJ, (2009) The phosphoproteomics data explosion. Curr Opin Chem Biol 13: 414-420.
76. Knebel A, Morrice N, Cohen P, (2001) A novel method to identify protein kinase substrates: eEF2 kinase is phosphorylated and inhibited by SAPK4/p38delta. EMBO J 20: 4360-4369.