Proteomic analysis of Src family kinases signaling complexes in golgi/endosomal fractions using a site-selective anti-phosphotyrosine antibody: Identification of LRP1-insulin receptor complexes

Journal of Proteome Research

Volumn 9, Issue 2, 2010, Pages 708-717

  Bilodeau, Nicolas ^a   Fiset, Annie ^a   Boulanger, Marie Chloé ^a   Bhardwaj, Sanjeev ^b   Winstall, Éric ^a   Lavoie, Josée N ^a   Faure, Robert L ^a  

^a UNIVERSITÉ LAVAL   (Canada)

^b Applied Biosystems Framingham   (United States)

Author keywords

Endosomes; Fractions; Golgi; Insulin clearance; Insulin receptor; Liver; Low density lipoprotein receptor related protein 1 (LRP1); Phosphoproteins; Proteomics; Src signaling

Indexed keywords

CARRIER PROTEIN; INSULIN; INSULIN RECEPTOR; LIPOPROTEIN; LOW DENSITY LIPOPROTEIN RELATED PROTEIN 1; PHOSPHOTYROSINE ANTIBODY; PROTEIN ANTIBODY; PROTEIN KINASE LYN; PROTEIN TYROSINE KINASE; PROTEINASE; PROTEOME; STRUCTURAL PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AFFINITY CHROMATOGRAPHY; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CHEMICAL LABELING; CONTROLLED STUDY; ELECTRON MICROSCOPY; ELECTROPHORESIS; ENDOCYTOSIS; ENDOSOME; ENZYME PHOSPHORYLATION; FEMALE; FUNCTIONAL PROTEOMICS; GOLGI COMPLEX; INSULIN CLEARANCE; INTERNALIZATION; MASS SPECTROMETRY; MEMBRANE PERMEABILITY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN DETERMINATION; PROTEIN ISOLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; TRANSPORT KINETICS;

ANIMALS; ENDOSOMES; FEMALE; GOLGI APPARATUS; ISOELECTRIC FOCUSING; MICE; MICE, INBRED C57BL; MICROSCOPY, FLUORESCENCE; PHOSPHOTYROSINE; PROTEOME; RECEPTOR, INSULIN; RECEPTORS, LDL; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; TUMOR SUPPRESSOR PROTEINS;

EID: 76149128373     PISSN: 15353893     EISSN: None     Source Type: Journal    
DOI: 10.1021/pr900481b     Document Type: Article

References (58)

1. Courtneidge, S. A. Role of Src in signal transduction pathways. The Jubilee Lecture. Biochem. Soc. Trans. 2002, 30 (2), 11-7.
2. Frame, M. C. Newest findings on the oldest oncogene; how activated src does it. J. Cell Sci. 2004, 117 (Pt. 7), 989-98.
3. Sandilands, E.; Akbarzadeh, S.; Vecchione, A.; McEwan, D. G.; Frame, M. C.; Heath, J. K. Src kinase modulates the activation, transport and signalling dynamics of fibroblast growth factor receptors. EMBO Rep. 2007, 8 (12), 1162-9.
4. Sandilands, E.; Frame, M. C. Endosomal trafficking of Src tyrosine kinase. Trends Cell Biol. 2008, 18 (7), 322-9.
5. Yates, J. R.; Gilchrist, A.; Howell, K. E.; Bergeron, J. J. Proteomics of organelles and large cellular structures. Nat. Rev. Mol. Cell Biol. 2005, 6 (9), 702-14.
6. Andersen, J. S.; Mann, M. Organellar proteomics: turning inventories into insights. EMBO Rep. 2006, 7 (9), 874-9.
7. Au, C. E.; Bell, A. W.; Gilchrist, A.; Hiding, J.; Nilsson, T.; Bergeron, J. J. Organellar proteomics to create the cell map. Curr. Opin. Cell Biol. 2007, 19 (4), 376-85.
8. Borner, G. H.; Harbour, M.; Hester, S.; Lilley, K. S.; Robinson, M. S. Comparative proteomics of clathrin-coated vesicles. J. Cell Biol. 2006, 175 (4), 571-8.
9. Bodenmiller, B.; Mueller, L. N.; Mueller, M.; Domon, B.; Aebersold, R. Reproducible isolation of distinct, overlapping segments of the phosphoproteome. Nat. Methods 2007, 4 (3), 231-7.
10. Champagne, C.; Landry, M. C.; Gingras, M. C.; Lavoie, J. N. Activation of adenovirus type 2 early region 4 ORF4 cytoplasmic death function by direct binding to Src kinase domain. J. Biol. Chem. 2004, 279 (24), 25905-15.
11. Landry, M. C.; Sicotte, A.; Champagne, C.; Lavoie, J. N. Regulation of cell death by recycling endosomes and golgi membrane dynamics via a pathway involving Src-family kinases, Cdc42 and Rab11a. Mol. Biol. Cell 2009, 20 (18), 4091-4106.
12. Zhang, H.; Zha, X.; Tan, Y.; Hornbeck, P. V.; Mastrangelo, A. J.; Alessi, D. R.; Polakiewicz, R. D.; Comb, M. J. Phosphoprotein analysis using antibodies broadly reactive against phosphorylated motifs. J. Biol. Chem. 2002, 277 (42), 39379-87.
13. Bilodeau, N.; Fiset, A.; Poirier, G. G.; Fortier, S.; Gingras, M. C.; Lavoie, J. N.; Faure, R. L. Insulin-dependent phosphorylation of DPP IV in liver. Evidence for a role of compartmentalized c-Src. FEBS J. 2006, 273 (5), 992-1003.
14. Gingras, M. C.; Champagne, C.; Roy, M.; Lavoie, J. N. Cytoplasmic death signal triggered by SRC-mediated phosphorylation of the adenovirus E4orf4 protein. Mol. Cell. Biol. 2002, 22 (1), 41-56.
15. Posner, B. I.; Faure, R.; Burgess, J. W.; Bevan, A. P.; Lachance, D.; Zhang-Sun, G.; Fantus, I. G.; Ng, J. B.; Hall, D. A.; Lum, B. S.; et al. , Peroxovanadium compounds. A new class of potent phosphotyrosine phosphatase inhibitors which are insulin mimetics. J. Biol. Chem. 1994, 269 (6), 4596-604.
16. Khan, M. N.; Savoie, S.; Bergeron, J. J.; Posner, B. I. Characterization of rat liver endosomal fractions. In vivo activation of insulinstimulable receptor kinase in these structures. J. Biol. Chem. 1986, 261 (18), 8462-72.
17. Gaulin, J. F.; Fiset, A.; Fortier, S.; Faure, R. L. Characterization of Cdk2-cyclin E complexes in plasma membrane and endosomes of liver parenchyma. Insulin-dependent regulation. J. Biol. Chem. 2000, 275 (22), 16658-65.
18. Shevchenko, A.; Wilm, M.; Vorm, O.; Mann, M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 1996, 68 (5), 850-8.
19. Havlis, J.; Thomas, H.; Sebela, M.; Shevchenko, A. Fast-response proteomics by accelerated in-gel digestion of proteins. Anal. Chem. 2003, 75 (6), 1300-6.
20. Keller, A.; Nesvizhskii, A. I.; Kolker, E.; Aebersold, R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 2002, 74 (20), 5383-92.
21. Nesvizhskii, A. I.; Keller, A.; Kolker, E.; Aebersold, R. A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 2003, 75 (17), 4646-58.
22. Moissoglu, K.; Gelman, I. H. v-Src rescues actin-based cytoskeletal architecture and cell motility and induces enhanced anchorage independence during oncogenic transformation of focal adhesion kinase-null fibroblasts. J. Biol. Chem. 2003, 278 (48), 47946-59.
23. Robert, A.; Miron, M. J.; Champagne, C.; Gingras, M. C.; Branton, P. E.; Lavoie, J. N. Distinct cell death pathways triggered by the adenovirus early region 4 ORF 4 protein. J. Cell Biol. 2002, 158 (3), 519-28.
24. Khan, M. N.; Baquiran, G.; Brule, C.; Burgess, J.; Foster, B.; Bergeron, J. J.; Posner, B. I. Internalization and activation of the rat liver insulin receptor kinase in vivo. J. Biol. Chem. 1989, 264 (22), 12931-40.
25. Caron, D.; Winstall, E.; Inaguma, Y.; Michaud, S.; Lettre, F.; Bourassa, S.; Kelly, I.; Poirier, G. G.; Faure, R. L.; Tanguay, R. M. Proteomic characterization of mouse cytosolic and membrane prostate fractions: high levels of free SUMO peptides are androgenregulated. J. Proteome Res. 2008, 7 (10), 4492-9.
26. Hopkins, C. R. Intracellular routing of transferrin and transferrin receptors in epidermoid carcinoma A431 cells. Cell 1983, 35 (1), 321-30.
27. Sabharanjak, S.; Sharma, P.; Parton, R. G.; Mayor, S. GPI-anchored proteins are delivered to recycling endosomes via a distinct cdc42-regulated, clathrin-independent pinocytic pathway. Dev. Cell 2002, 2 (4), 411-23.
28. Yamashiro, D. J.; Tycko, B.; Fluss, S. R.; Maxfield, F. R. Segregation of transferrin to a mildly acidic (pH 6.5) para-Golgi compartment in the recycling pathway. Cell 1984, 37 (3), 789-800.
29. van der Geer, P. Phosphorylation of LRP1: regulation of transport and signal transduction. Trends Cardiovasc. Med. 2002, 12 (4), 160-5.
30. Barnes, H.; Ackermann, E. J.; van der Geer, P. v-Src induces Shc binding to tyrosine 63 in the cytoplasmic domain of the LDL receptor-related protein 1. Oncogene 2003, 22 (23), 3589-97.
31. Futter, C. E.; White, I. J. Annexins and endocytosis. Traffic 2007, 8 (8), 951-8.
32. Hayes, M. J.; Moss, S. E. Annexin 2 has a dual role as regulator and effector of V-Src in cell transformation. J. Biol. Chem. 2009, 284 (15), 10202-10.
33. Christofk, H. R.; Vander Heiden,M. G.; Harris,M. H.; Ramanathan, A.; Gerszten, R. E.; Wei, R.; Fleming, M. D.; Schreiber, S. L.; Cantley, L. C. The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 2008, 452 (7184), 230-3.
34. Piedra, J.; Martinez, D.; Castano, J.; Miravet, S.; Dunach, M.; de Herreros, A. G. Regulation of beta-catenin structure and activity by tyrosine phosphorylation. J. Biol. Chem. 2001, 276 (23), 20436-43.
35. Pooley, R. D.; Reddy, S.; Soukoulis, V.; Roland, J. T.; Goldenring, J. R.; Bader, D. M. CytLEK1 is a regulator of plasma membrane recycling through its interaction with SNAP-25. Mol. Biol. Cell 2006, 17 (7), 3176-86.
36. Rincon, E.; Santos, T.; Avila-Flores, A.; Albar, J. P.; Lalioti, V.; Lei, C.; Hong, W.; Merida, I. Proteomics identification of sorting nexin 27 as a diacylglycerol kinase zeta-associated protein: new diacylglycerol kinase roles in endocytic recycling. Mol. Cell. Proteomics 2007, 6 (6), 1073-87.
37. Huang, Y. W.; Yan, M.; Collins, R. F.; Diciccio, J. E.; Grinstein, S.; Trimble, W. S. Mammalian septins are required for phagosome formation. Mol. Biol. Cell 2008, 19 (4), 1717-26.
38. Wu, Q.; Ortegon, A. M.; Tsang, B.; Doege, H.; Feingold, K. R.; Stahl, A. FATP1 is an insulin-sensitive fatty acid transporter involved in diet-induced obesity. Mol. Cell. Biol. 2006, 26 (9), 3455-67.
39. Kruger, M.; Kratchmarova, I.; Blagoev, B.; Tseng, Y. H.; Kahn, C. R.; Mann, M. Dissection of the insulin signaling pathway via quantitative phosphoproteomics. Proc. Natl. Acad. Sci. U S.A. 2008, 105 (7), 2451-6.
40. Jedrychowski, M. P.; Gartner, C. A.; Gygi, S. P.; Zhou, L.; Herz, J.; Kandror, K. V.; Pilch, P. F. Proteomic analysis of GLUT4 storage vesicles (GSVS) reveals low-density lipoprotein receptor-related protein 1 (LRP1) to be an important vesicle component and target of insulin signaling. J. Biol. Chem. [Online early access]. DOI: 10.1074/jbc.M109.040428. Published online: Oct 28, 2009.
41. Komatsu, M.; Chiba, T.; Tatsumi, K.; Iemura, S.; Tanida, I.; Okazaki, N.; Ueno, T.; Kominami, E.; Natsume, T.; Tanaka, K. A novel protein-conjugating system for Ufm1, a ubiquitin-fold modifier. EMBO J. 2004, 23 (9), 1977-86.
42. Sasakawa, H.; Sakata, E.; Yamaguchi, Y.; Komatsu, M.; Tatsumi, K.; Kominami, E.; Tanaka, K.; Kato, K. Solution structure and dynamics of Ufm1, a ubiquitin-fold modifier 1. Biochem. Biophys. Res. Commun. 2006, 343 (1), 21-6.
43. Lu, H.; Yang, Y.; Allister, E. M.; Wijesekara, N.; Wheeler, M. B. The identification of potential factors associated with the development of type 2 diabetes: a quantitative proteomics approach. Mol. Cell. Proteomics 2008, 7 (8), 1434-51.
44. Tsukita, S.; Oishi, K.; Akiyama, T.; Yamanashi, Y.; Yamamoto, T. Specific proto-oncogenic tyrosine kinases of src family are enriched in cell-to-cell adherens junctions where the level of tyrosine phosphorylation is elevated. J. Cell Biol. 1991, 113 (4), 867-79.
45. Herz, J.; Strickland, D. K. LRP: a multifunctional scavenger and signaling receptor. J. Clin. Invest. 2001, 108 (6), 779-84.
46. Yamada, S.; Pokutta, S.; Drees, F.; Weis, W. I.; Nelson, W. J. Deconstructing the cadherin-catenin-actin complex. Cell 2005, 123 (5), 889-901.
47. Duchesne, C.; Charland, S.; Asselin, C.; Nahmias, C.; Rivard, N. Negative regulation of beta-catenin signaling by tyrosine phosphatase SHP-1 in intestinal epithelial cells. J. Biol. Chem. 2003, 278 (16), 14274-83.
48. Roura, S.; Miravet, S.; Piedra, J.; Garcia de Herreros, A.; Dunach, M. Regulation of E-cadherin/Catenin association by tyrosine phosphorylation. J. Biol. Chem. 1999, 274 (51), 36734-40.
49. Gates, J.; Peifer, M. Can 1000 reviews be wrong? Actin, alpha-Catenin, and adherens junctions. Cell 2005, 123 (5), 769-72.
50. Izumi, S.; Manabe, A.; Tomoyasu, A.; Kihara-Negishi, F.; Ariga, H. Molecular cloning of the complementary DNA for the mouse pyruvate kinase M-2 gene whose expression is dependent upon cell differentiation. Biochim. Biophys. Acta 1995, 1267 (2-3), 135-8.
51. Tisdale, E. J.; Artalejo, C. R. A GAPDH mutant defective in Srcdependent tyrosine phosphorylation impedes Rab2-mediated events. Traffic 2007, 8 (6), 733-41.
52. Goodwin, R. L.; Pabon-Pena, L. M.; Foster, G. C.; Bader, D. The cloning and analysis of LEK1 identifies variations in the LEK/centromere protein F/mitosin gene family. J. Biol. Chem. 1999, 274 (26), 18597-604.
53. Soukoulis, V.; Reddy, S.; Pooley, R. D.; Feng, Y.; Walsh, C. A.; Bader, D. M. Cytoplasmic LEK1 is a regulator of microtubule function through its interaction with the LIS1 pathway. Proc. Natl. Acad. Sci. U.S.A. 2005, 102 (24), 8549-54.
54. Glenney, J. R., Jr. Phosphorylation of p36 in vitro with pp60src. Regulation by Ca2+ and phospholipid. FEBS Lett. 1985, 192 (1), 79-82.
55. Saris, C. J.; Tack, B. F.; Kristensen, T.; Glenney, J. R., Jr.; Hunter, T. The cDNA sequence for the protein-tyrosine kinase substrate p36 (calpactin I heavy chain) reveals a multidomain protein with internal repeats. Cell 1986, 46 (2), 201-12.
56. White, I. J.; Bailey, L. M.; Aghakhani, M. R.; Moss, S. E.; Futter, C. E. EGF stimulates annexin 1-dependent inward vesiculation in a multivesicular endosome subpopulation. EMBO J. 2006, 25 (1), 1-12.
57. Duckworth, W. C.; Hamel, F. G.; Peavy, D. E. Hepatic metabolism of insulin. Am. J. Med. 1988, 85 (5A), 71-6.
58. Carpentier, J. L. Robert Feulgen Prize Lecture 1993. The journey of the insulin receptor into the cell: from cellular biology to pathophysiology. Histochemistry 1993, 100 (3), 169-84.