Identification of novel SHPS-1-associated proteins and their roles in regulation of insulin-like growth factor-dependent responses in vascular smooth muscle cells

Molecular and Cellular Proteomics

Volumn 8, Issue 7, 2009, Pages 1539-1551

  Shen, Xinchun ^a   Xi, Gang ^a   Radhakrishnan, Yashwanth ^a   Clemmons, David R ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; HEAT SHOCK PROTEIN; MOLECULAR SCAFFOLD; PHOSPHATASE; PROTEIN KINASE; PROTEIN KINASE B; PROTEIN P85; PROTEIN SHC; PROTEIN TYROSINE PHOSPHATASE; PROTEIN TYROSINE PHOSPHATASE SHP 2; SOMATOMEDIN; SOMATOMEDIN C; STAT1 PROTEIN; TYROSINE PHOSPHATASE NON RECEPTOR TYPE SUBSTRATE 1; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; CYTOPLASM; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; ONCOGENE SRC; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; PROTEOMICS; SCREENING; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE;

ANIMALS; ANTIGENS, DIFFERENTIATION; CELL DEATH; CELL LINE; HSP70 HEAT-SHOCK PROTEINS; HUMANS; HYPERGLYCEMIA; INSULIN-LIKE GROWTH FACTOR I; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; PROTEIN BIOSYNTHESIS; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, IMMUNOLOGIC; SIGNAL TRANSDUCTION; SWINE;

EID: 70349162087     PISSN: 15359476     EISSN: None     Source Type: Journal    
DOI: 10.1074/mcp.M800543-MCP200     Document Type: Article

References (73)

1. Clemmons, D. R. (2007) Modifying IGF1 activity: an approach to treat endocrine disorders, atherosclerosis and cancer. Nat. Rev. Drug Discov. 6, 821-833
2. Ling, Y., Maile, L. A., Lieskovska, J., Badley-Clarke, J., and Clemmons, D. R. (2005) Role of SHPS-1 in the regulation of insulin-like growth factor I-stimulated Shc and mitogen-activated protein kinase activation in vascular smooth muscle cells. Mol. Biol. Cell 16, 3353-3364
3. Fujioka, Y., Matozaki, T., Noguchi, T., Iwamatsu, A., Yamao, T., Takahashi, N., Tsuda, M., Takada, T., and Kasuga, M. (1996) A novel membrane glycoprotein, SHPS-1, that binds the SH2-domain-containing protein tyrosine phosphatase SHP-2 in response to mitogens and cell adhesion. Mol. Cell. Biol. 16, 6887-6899
4. Takada, T., Matozaki, T., Takeda, H., Fukunaga, K., Noguchi, T., Fujioka, Y., Okazaki, I., Tsuda, M., Yamao, T., Ochi, F., and Kasuga, M. (1998) Roles of the complex formation of SHPS-1 with SHP-2 in insulin-stimulated mitogen-activated protein kinase activation. J. Biol. Chem. 273, 9234-9242
5. Oh, E. S., Gu, H., Saxton, T. M., Timms, J. F., Hausdorff, S., Frevert, E. U., Kahn, B. B., Pawson, T., Neel, B. G., and Thomas, S. M. (1999) Regulation of early events in integrin signaling by protein tyrosine phosphatase SHP-2. Mol. Cell. Biol. 19, 3205-3215
6. Oshima, K., Ruhul Amin, A. R., Suzuki, A., Hamaguchi, M., and Matsuda, S. (2002) SHPS-1, a multifunctional transmembrane glycoprotein. FEBS Lett. 519, 1-7
7. Kharitonenkov, A., Chen, Z., Sures, I., Wang, H., Schilling, J., and Ullrich, A. (1997) A family of proteins that inhibit signalling through tyrosine kinase receptors. Nature 386, 181-186 (Pubitemid 27131446)
8. Gresham, H. D., Dale, B. M., Potter, J. W., Chang, P. W., Vines, C. M., Lowell, C. A., Lagenaur, C. F., and Willman, C. L. (2000) Negative regulation of phagocytosis in murine macrophages by the Src kinase family member, Fgr. J. Exp. Med. 191, 515-528
9. Timms, J. F., Swanson, K. D., Marie-Cardine, A., Raab, M., Rudd, C. E., Schraven, B., and Neel, B. G. (1999) SHPS-1 is a scaffold for assembling distinct adhesion-regulated multi-protein complexes in macrophages. Curr. Biol. 9, 927-930
10. Ling, Y., Maile, L. A., and Clemmons, D. R. (2003) Tyrosine phosphorylation of the beta3-subunit of the alphaVbeta3 integrin is required for embrane association of the tyrosine phosphatase SHP-2 and its further recruitment to the insulin-like growth factor I receptor. Mol. Endocrinol. 17, 1824-1833
11. Maile, L. A., Badley-Clarke, J., and Clemmons, D. R. (2003) The association between integrin-associated protein and SHPS-1 regulates insulin-like growth factor-I receptor signaling in vascular smooth muscle cells. Mol. Biol. Cell 14, 3519-3528
12. Lieskovska, J., Ling, Y., Badley-Clarke, J., and Clemmons, D. R. (2006) The role of Src kinase in insulin-like growth factor-dependent mitogenic signaling in vascular smooth muscle cells. J. Biol. Chem. 281, 25041-25053
13. Maile, L. A., Capps, B. E., Ling, Y., Xi, G., and Clemmons, D. R. (2007) Hyperglycemia alters the responsiveness of smooth muscle cells to insulin-like growth factor-I. Endocrinology 148, 2435-2443 (Pubitemid 46997046)
14. Radhakrishnan, Y., Maile, L. A., Ling, Y., Graves, L. M., and Clemmons, D. R. (2008) Insulin-like growth factor-I stimulates Shc-dependent phosphatidylinositol 3-kinase activation via Grb2-associated p85 in vascular smooth muscle cells. J. Biol. Chem. 283, 16320-16331
15. Alberts, B. (1998) The cell as a collection of protein machines: preparing the next generation of molecular biologists. Cell 92, 291-294
16. Papin, J. A., Hunter, T., Palsson, B. O., and Subramaniam, S. (2005) Reconstruction of cellular signalling networks and analysis of their properties. Nat. Rev. Mol. Cell Biol. 6, 99-111
17. Roberts, R. W., and Szostak, J. W. (1997) RNA-peptide fusions for the in vitro selection of peptides and proteins. Proc. Natl. Acad. Sci. U. S. A. 94, 12297-12302
18. Liu, R., Barrick, J. E., Szostak, J. W., and Roberts, R. W. (2000) Optimized synthesis of RNA-protein fusions for in vitro protein selection. Methods Enzymol. 318, 268-293 (Pubitemid 30421654)
19. Shen, X., Valencia, C. A., Szostak, J. W., Szostak, J., Dong, B., and Liu, R. (2005) Scanning the human proteome for calmodulin-binding proteins. Proc. Natl. Acad. Sci. U. S. A. 102, 5969-5974
20. Takahashi, T. T., Austin, R. J., and Roberts, R. W. (2003) mRNA display: ligand discovery, interaction analysis and beyond. Trends Biochem. Sci. 28, 159-165
21. 2+)/Calmodulin-binding proteins from the C. elegans proteome. Cell Calcium 43, 444-456
22. Nemoto, N., Miyamoto-Sato, E., Husimi, Y., and Yanagawa, H. (1997) In vitro virus: bonding of mRNA bearing puromycin at the 3′-terminal end to the C-terminal end of its encoded protein on the ribosome in vitro. FEBS Lett. 414, 405-408
23. Miyamoto-Sato, E., Takashima, H., Fuse, S., Sue, K., Ishizaka, M., Tateyama, S., Horisawa, K., Sawasaki, T., Endo, Y., and Yanagawa, H. (2003) Highly stable and efficient mRNA templates for mRNA-protein fusions and C-temninally labeled proteins. Nucleic Acids Res. 31, e78
24. Miyamoto-Sato, E., Ishizaka, M., Horisawa, K., Tateyama, S., Takashima, H., Fuse, S., Sue, K., Hirai, N., Masuoka, K., and Yanagawa, H. (2005) Cell-free cotranslation and selection using in vitro virus for high-throughput analysis of protein-protein interactions and complexes. Genome Res. 15, 710-717 (Pubitemid 41043641)
25. Rigaut, G., Shevchenko, A., Rutz, B., Wilm, M., Mann, M., and Séraphin, B. (1999) A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol. 17, 1030-1032
26. Puig, O., Caspary, F., Rigaut, G., Rutz, B., Bouveret, E., Bragado-Nilsson, E., Wilm, M., and Séraphin, B. (2001) The tandem affinity purification (TAP) method: a general procedure of protein complex purification. Methods 24, 218-229 (Pubitemid 32846428)
27. Gavin, A. C., Bösche, M., Krause, R., Grandi, P., Marzioch, M., Bauer, A., Schultz, J., Rick, J. M., Michon, A. M., Cruciat, C. M., Remor, M., Höfert, C., Schelder, M., Brajenovic, M., Ruffner, H., Merino, A., Klein, K., Hudak, M., Dickson, D., Rudi, T., Gnau, V., Bauch, A., Bastuck, S., Huhse, B., Leutwein, O., Heurtier, M. A., Copley, R. R., Edelmann, A., Querfurth, E., Rybin, V., Drewes, G., Raida, M., Bouwmeester, T., Bork, P., Seraphin, B., Kuster, B., Neubauer, G., and Superti-Furga, G. (2002) Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415, 141-147 (Pubitemid 34059510)
28. Ho, Y., Gruhler, A., Heilbut, A., Bader, G. D., Moore, L., Adams, S. L., Millar, A., Taylor, P., Bennett, K., Boutilier, K., Yang, L., Wolting, C., Donaldson, I., Schandorff, S., Shewnarane, J., Vo, M., Taggart, J., Goudreault, M., Muskat, B., Arfarano, C., Dewar, D., Lin, Z., Michalickova, K., Willems, A. R., Sassi, H., Nielsen, P. A., Rasmussen, K. J., Andersen, J. R., Johansen, L. E., Hansen, L. H., Jespersen, H., Podtelejnikov, A., Nielsen, E., Crawford, J., Poulsen, V., Sørensen, B. D., Matthiesen, J., Hendrickson, R. C., Gleeson, F., Pawson, T., Moran, M. F., Durocher, D., Mann, M., Hogue, C. W., Figeys, D., and Tyers, M. (2002) Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 415, 180-183
29. Kemmeren, P., van Berkum, N. L., Vilo, J., Bijma, T., Donders, R., Brazma, A., and Holstege, F. C. (2002) Protein interaction verification and functional annotation by integrated analysis of genome-scale data. Mol. Cell 9, 1133-1143 (Pubitemid 34626681)
30. Butland, G., Peregrin-Alvarez, J. M., Li, J., Yang, W., Yang, X., Canadien, V., Starostine, A., Richards, D., Beattie, B., Krogan, N., Davey, M., Parkinson, J., Greenblatt, J., and Emili, A. (2005) Interaction network containing conserved and essential protein complexes in Escherichia coli. Nature 433, 531-537
31. Bürckstümmer, T., Bennett, K. L., Preradovic, A., Schütze, G., Hantschel, O., Superti-Furga, G., and Bauch, A. (2006) An efficient tandem affinity purification procedure for interaction proteomics in mammalian cells. Nat. Methods 3, 1013-1019 (Pubitemid 44782701)
32. Gavin, A. C., Aloy, P., Grandi, P., Krause, R., Boesche, M., Marzioch, M., Rau, C., Jensen, L. J., Bastuck, S., Dümpelfeld, B., Edelmann, A., Heurtier, M. A., Hoffman, V., Hoefert, C., Klein, K., Hudak, M., Michon, A. M., Schelder, M., Schirle, M., Remor, M., Rudi, T., Hooper, S., Bauer, A., Bouwmeester, T., Casari, G., Drewes, G., Neubauer, G., Rick, J. M., Kuster, B., Bork, P., Russell, R. B., and Superti-Furga, G. (2006) Proteome survey reveals modularity of the yeast cell machinery. Nature 440, 631-636
33. Daulat, A. M., Maurice, P., Froment, C., Guillaume, J. L., Broussard, C., Monsarrat, B., Delagrange, P., and Jockers, R. (2007) Purification and identification of G protein-coupled receptor protein complexes under native conditions. Mol. Cell Proteomics 6, 835-844 (Pubitemid 46831935)
34. Parker, A., Gockerman, A., Busby, W. H., and Clemmons, D. R. (1995) Properties of an insulin-like growth factor-binding protein-4 protease that is secreted by smooth muscle cells. Endocrinology 136, 2470-2476
35. Kurz, M., Gu, K., and Lohse, P. A. (2000) Psoralen photo-crosslinked mRNA-puromycin conjugates: a novel template for the rapid and facile preparation of mRNA-protein fusions. Nucleic Acids Res. 28, E83
36. Maile, L. A., and Clemmons, D. R. (2002) Regulation of insulin-like growth factor I receptor dephosphorylation by SHPS-1 and the tyrosine phosphatase SHP-2. J. Biol. Chem. 277, 8955-8960
37. Xi, G., Shen, X., and Clemmons, D. R. (2008) p66shc Negatively regulates insulin-like growth factor I signal transduction via inhibition of p52shc binding to Src homology 2 domain-containing protein tyrosine phosphatase substrate-1 leading to impaired growth factor receptor-bound protein-2 membrane recruitment. Mol. Endocrinol. 22, 2162-2175
38. Mao, H., Wang, Y., Li, Z., Ruchalski, K. L., Yu, X., Schwartz, J. H., and Borkan, S. C. (2004) Hsp72 interacts with paxillin and facilitates the reassembly of focal adhesions during recovery from ATP depletion. J. Biol. Chem. 279, 15472-15480
39. Zhou, W., and Freed, C. R. (2004) Tyrosine-to-cysteine modification of human alpha-synuclein enhances protein aggregation and cellular toxicity. J. Biol. Chem. 279, 10128-10135
40. Zheng, B., and Clemmons, D. R. (1998) Blocking ligand occupancy of the alphaVbeta3 integrin inhibits insulin-like growth factor I signaling in vascular smooth muscle cells. Proc. Natl. Acad. Sci. U. S. A. 95, 11217-11222
41. Nguyen, H., Ramana, C. V., Bayes, J., and Stark, G. R. (2001) Roles of phosphatidylinositol 3-kinase in interferon-gamma-dependent phosphorylation of STAT1 on serine 727 and activation of gene expression. J. Biol. Chem. 276, 33361-33368
42. Sadzak, I., Schiff, M., Gattermeier, I., Glinitzer, R., Sauer, I., Saalmûller, A., Yang, E., Schaljo, B., and Kovarik, P. (2008) Recruitment of Stat1 to chromatin is required for interferon-induced serine phosphorylation of Stat1 transactivation domain. Proc. Natl. Acad. Sci. U. S. A. 105, 8944-8949
43. Harrington, E. A., Bennett, M. R., Fanidi, A., and Evan, G. I. (1994) c-Myc-induced apoptosis in fibroblasts is inhibited by specific cytokines. EMBO J. 13, 3286-3295 (Pubitemid 24226943)
44. Wang, L., Ma, W., Markovich, R., Chen, J. W., and Wang, P. H. (1998) Regulation of cardiomyocyte apoptotic signaling by insulin-like growth factor I. Circ. Res. 83, 516-522
45. Wang, L., Ma, W., Markovich, R., Lee, W. L., and Wang, P. H. (1998) Insulin-like growth factor I modulates induction of apoptotic signaling in H9C2 cardiac muscle cells. Endocrinology 139, 1354-1360 (Pubitemid 28510157)
46. Kim, H. S., Skurk, C., Maatz, H., Shiojima, I., Ivashchenko, Y., Yoon, S. W., Park, Y. B., and Walsh, K. (2005) Akt/FOXO3a signaling modulates the endothelial stress response through regulation of heat shock protein 70 expression. FASEB J. 19, 1042-1044 (Pubitemid 40827745)
47. LeRoith, D., Neuenschwander, S., Wood, T. L., and Hennighausen, L. (1995) Insulin-like growth factor-I and insulin-like growth factor binding protein-3 inhibit involution of the mammary gland following lactation: studies in transgenic mice. Prog. Growth Factor Res. 6, 433-436
48. Jones, J. I., Prevette, T., Gockerman, A., and Clemmons, D. R. (1996) Ligand occupancy of the alpha-V-beta3 integrin is necessary for smooth muscle cells to migrate in response to insulin-like growth factor. Proc. Natl. Acad. Sci. U. S. A. 93, 2482-2487
49. Howell, J. M., Winstone, T. L., Coorssen, J. R., and Turner, R. J. (2006) An evaluation of in vitro protein-protein interaction techniques: assessing contaminating background proteins. Proteomics 6, 2050-2069
50. Mitsuhashi, H., Futai, E., Sasagawa, N., Hayashi, Y., Nishino, I., and Ishiura, S. (2008) Csk-homologous kinase interacts with SHPS-1 and enhances neurite outgrowth of PC12 cells. J. Neurochem. 105, 101-112
51. Hayashi, K., Takahashi, M., Kimura, K., Nishida, W., Saga, H., and Sobue, K. (1999) Changes in the balance of phosphoinositide 3-kinase/protein kinase B (Akt) and the mitogen-activated protein kinases (ERK/p38MAPK) determine a phenotype of visceral and vascular smooth muscle cells. J. Cell Biol. 145, 727-740 (Pubitemid 29240851)
52. Imai, Y., and Clemmons, D. R. (1999) Roles of phosphatidylinositol 3-kinase and mitogen-activated protein kinase pathways in stimulation of vascular smooth muscle cell migration and deoxyriboncleic acid synthesis by insulin-like growth factor-I. Endocrinology 140, 4228-4235 (Pubitemid 30647121)
53. Liu, Z. P., Wang, Z., Yanagisawa, H., and Olson, E. N. (2005) Phenotypic modulation of smooth muscle cells through interaction of Foxo4 and myocardin. Dev. Cell 9, 261-270 (Pubitemid 41051744)
54. Romano, F., Chiarenza, C., Palombi, F., Filippini, A., Padula, F., Ziparo, E., and De Cesaris, P. (2006) Platelet-derived growth factor-BB-induced hypertrophy of peritubular smooth muscle cells is mediated by activation of p38 MAP-kinase and of Rho-kinase. J. Cell. Physiol. 207, 123-131
55. Laurino, L., Wang, X. X., de la Houssaye, B. A., Sosa, L., Dupraz, S., Cáceres, A., Pfenninger, K. H., and Quiroga, S. (2005) PI3K activation by IGF-1 is essential for the regulation of membrane expansion at the nerve growth cone. J. Cell Sci. 118, 3653-3662 (Pubitemid 41309412)
56. Radcliff, K., Tang, T. B., Lim, J., Zhang, Z., Abedin, M., Demer, L. L., and Tintut, Y. (2005) Insulin-like growth factor-I regulates proliferation and osteoblastic differentiation of calcifying vascular cells via extracellular signal-regulated protein kinase and phosphatidylinositol 3-kinase pathways. Circ. Res. 96, 398-400
57. Zaka, M., Rafi, M. A., Rao, H. Z., Luzi, P., and Wenger, D. A. (2005) Insulin-like growth factor-1 provides protection against psychosine-induced apoptosis in cultured mouse oligodendrocyte progenitor cells using primarily the PI3K/Akt pathway. Mol. Cell Neurosci. 30, 398-407
58. Matthews, L. C., Taggart, M. J., and Westwood, M. (2008) Modulation of caveolin-1 expression can affect signalling through the phosphatidylinositol 3-kinase/Akt pathway and cellular proliferation in response to insulin-like growth factor I. Endocrinology 149, 5199-5208
59. Cohen, P., Alessi, D. R., and Cross, D. A. (1997) PDK1, one of the missing links in insulin signal transduction? FEBS Lett. 410, 3-10
60. Toker, A., and Newton, A. C. (2000) Cellular signaling: pivoting around PDK-1. Cell 103, 185-188
61. Block, K., Eid, A., Griendling, K. K., Lee, D. Y., Wittrant, Y., and Gorin, Y. (2008) Nox4 NAD(P)H oxidase mediates Src-dependent tyrosine phosphorylation of PDK-1 in response to angiotensin II: role in mesangial cell hypertrophy and fibronectin expression. J. Biol. Chem. 283, 24061-24076
62. Shen, W. H., Boyle, D. W., Wisniowski, P., Bade, A., and Liechty, E. A. (2005) Insulin and IGF-I stimulate the formation of the eukaryotic initiation factor 4F complex and protein synthesis in C2C12 myotubes independent of availability of external amino acids. J. Endocrinol. 185, 275-289 (Pubitemid 40691794)
63. Jefferies, H. B., Fumagalli, S., Dennis, P. B., Reinhard, C., Pearson, R. B., and Thomas, G. (1997) Rapamycin suppresses 5′TOP mRNA translation through inhibition of p70s6k. EMBO J. 16, 3693-3704 (Pubitemid 27250062)
64. Wang, H., Kouri, G., and Wollheim, C. B. (2005) ER stress and SREBP-1 activation are implicated in beta-cell glucolipotoxicity. J. Cell Sci. 118, 3905-3915 (Pubitemid 41410274)
65. Werstuck, G. H., Khan, M. I., Femia, G., Kim, A. J., Tedesco, V., Trigatti, B., and Shi, Y. (2006) Glucosamine-induced endoplasmic reticulum dysfunction is associated with accelerated atherosclerosis in a hyperglycemic mouse model. Diabetes 55, 93-101 (Pubitemid 43343303)
66. Kaufman, R. J. (1999) Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev. 13, 1211-1233
67. Mori, K. (2000) Tripartite management of unfolded proteins in the endoplasmic reticulum. Cell 101, 451-454
68. Bence, N. F., Sampat, R. M., and Kopito, R. R. (2001) Impairment of the ubiqurtin-proteasome system by protein aggregation. Science 292, 1552-1555
69. Pilon, M., and Schekman, R. (1999) Protein translocation: how Hsp70 pulls it off. Cell 97, 679-682 (Pubitemid 29278040)
70. Hartl, F. U., and Hayer-Hartl, M. (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295, 1852-1858
71. Kristiansen, M., Messenger, M. J., Klöhn, P. C., Brandner, S., Wadsworth, J. D., Collinge, J., and Tabrizi, S. J. (2005) Disease-related prion protein forms aggresomes in neuronal cells leading to caspase activation and apoptosis. J. Biol. Chem. 280, 38851-38861
72. Beere, H. M. (2001) Stressed to death: regulation of apoptotic signaling pathways by the heat shock proteins. Sci. STKE 2001, re1
73. Cho, D. Y., Yang, G. H., Ryu, C. J., and Hong, H. J. (2003) Molecular chaperone GRP78/BiP interacts with the large surface protein of hepatitis B virus in vitro and in vivo. J. Virol. 77, 2784-2788