Interactions of the protein-tyrosine phosphatase-α with the focal adhesion targeting domain of focal adhesion kinase are involved in interleukin-1 signaling in fibroblasts

Journal of Biological Chemistry

Volumn 289, Issue 26, 2014, Pages 18427-18441

  Wang, Qin ^a   Wang, Yongqiang ^a   Fritz, Dominik ^a   Rajshankar, Dhaarmini ^a   Downey, Gregory P ^b,c,d   McCulloch, Christopher A ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b DEPARTMENT OF MEDICINE   (United States)

^c Division of Pulmonary Sciences and Critical Care Medicine   (United States)

^d UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CELL CULTURE; CELL MEMBRANES; FIBROBLASTS; IMMUNOLOGY; PHOSPHATASES; PROTEINS; SIGNAL TRANSDUCTION; SIGNALING;

CYTOSKELETAL PROTEINS; DIRECT INTERACTIONS; ENDOPLASMIC RETICULUM; FOCAL ADHESION KINASE; IMMUNOPRECIPITATIONS; MOUSE EMBRYONIC FIBROBLASTS; PROTEIN-TYROSINE PHOSPHATASE; PURIFIED PROTEIN;

ADHESION;

CALCIUM ION; FOCAL ADHESION KINASE; GELATINASE B; INTERLEUKIN 1; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN TYROSINE PHOSPHATASE; PROTEIN TYROSINE PHOSPHATASE ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; EMBRYO; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; FIBROBLAST; FOCAL ADHESION; GENE SILENCING; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION;

CELL ADHESION; FIBROBLAST; MATRIX METALLOPROTEINASE (MMP); PHOSPHATASE; SIGNALING; TYROSINE-PROTEIN KINASE (TYROSINE KINASE);

ANIMALS; CALCIUM; CELLS, CULTURED; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FIBROBLASTS; FOCAL ADHESION PROTEIN-TYROSINE KINASES; FOCAL ADHESIONS; INTERLEUKIN-1; MATRIX METALLOPROTEINASE 9; MICE; MICE, KNOCKOUT; NIH 3T3 CELLS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECEPTOR-LIKE PROTEIN TYROSINE PHOSPHATASES, CLASS 4; SIGNAL TRANSDUCTION;

EID: 84903539708     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.540294     Document Type: Article

References (49)

1. Smith, D. E., Renshaw, B. R., Ketchem, R. R., Kubin, M., Garka, K. E., and Sims, J. E. (2000) Four new members expand the interleukin-1 superfamily. J. Biol. Chem. 275, 1169-1175
2. Dinarello, C. A. (2003) Setting the cytokine trap for autoimmunity. Nat. Med. 9, 20-22
3. Isshiki, H., Akira, S., Tanabe, O., Nakajima, T., Shimamoto, T., Hirano, T., and Kishimoto, T. (1990) Constitutive and interleukin-1 (IL-1)-inducible factors interact with the IL-1-responsive element in the IL-6 gene. Mol. Cell. Biol. 10, 2757-2764
4. Goldring, S. R. (2003) Pathogenesis of bone and cartilage destruction in rheumatoid arthritis. Rheumatology 42, Suppl. 2, 11-16
5. Ruhul Amin, A. R., Senga, T., Oo, M. L., Thant, A. A., and Hamaguchi, M. (2003) Secretion of matrix metalloproteinase-9 by the proinflammatory cytokine, IL-1β: a role for the dual signalling pathways, Akt and Erk. Genes Cells 8, 515-523
6. Wang, Q., Rajshankar, D., Laschinger, C, Talior-Volodarsky, I., Wang, Y., Downey, G. P., and McCulloch, C. A. (2010) Importance of protein-tyrosine phosphatase-α catalytic domains for interactions with SHP-2 and interleukin-1-induced matrix metalloproteinase-3 expression. J. Biol. Chem. 285, 22308-22317
7. Liang, K. C., Lee, C. W., Lin, W. N., Lin, C. C., Wu, C. B., Luo, S. F., and Yang, C. M. (2007) Interleukin-1β induces MMP-9 expression via p42/p44 MAPK, p38 MAPK, JNK, and nuclear factor-kB signaling pathways in human tracheal smooth muscle cells. J. Cell Physiol. 211, 759-770
8. Shibata, K., Kikkawa, F., Nawa, A., Thant, A. A., Naruse, K., Mizutani, S., and Hamaguchi, M. (1998) Both focal adhesion kinase and c-Ras are required for the enhanced matrix metalloproteinase 9 secretion by fibronectin in ovarian cancer cells. Cancer Res. 58, 900-903
9. Wehrle-Haller, B., and Imhof, B. (2002) The inner lives of focal adhesions. Trends Cell Biol. 12, 382-389
10. Burridge, K., and Chrzanowska-Wodnicka, M. (1996) Focal adhesions, contractility, and signaling. Annu. Rev. Cell Dev. Biol. 12, 463-518
11. Arora, P. D., Ma, J., Min, W., Cruz, T., and McCulloch, C. A. (1995) Interleukin-1-induced calcium flux in human fibroblasts is mediated through focal adhesions. J. Biol. Chem. 270, 6042-6049
12. Luo, L., Cruz, T., and McCulloch, C. (1997) Interleukin 1-induced calcium signalling in chondrocytes requires focal adhesions. Biochem. J. 324, 653-658
13. 2+ from internal stores is dependent on cellmatrix interactions and regulates ERK activation. FASEBJ. 17, 1898-1900
14. Lo, Y. Y., Luo, L., McCulloch, C A., and Cruz, T. F. (1998) Requirements of focal adhesions and calcium fluxes for interleukin-1-induced ERK kinase activation and c-fos expression in fibroblasts. J. Biol. Chem. 273, 7059-7065
15. MacGillivray, M. K., Cruz, T. F., and McCulloch, C. A. (2000) The recruitment of the interleukin-1 (IL-1) receptor-associated kinase (IRAK) into focal adhesion complexes is required for IL-1β-induced ERK activation. J. Biol. Chem. 275, 23509-23515
16. Reunanen, N., Westermarck, J., Häkkinen, L., Holmström, T. H., Elo, I., Eriksson, J. E., and Kähäri, V. M. (1998) Enhancement of fibroblast collagenase (matrix metalloproteinase-1) gene expression by ceramide is mediated by extracellular signal-regulated and stress-activated protein kinase pathways. J. Biol. Chem. 273, 5137-5145
17. Schlaepfer, D. D., and Hunter, T. (1997) Focal adhesion kinase overexpression enhances ras-dependent integrin signaling to ERK2/mitogen- activated protein kinase through interactions with and activation of c-Src. J. Biol. Chem. 272, 13189-13195
18. Hanks, S. K., Calalb, M. B., Harper, M. C, and Patel, S. K. (1992) Focal adhesion protein-tyrosine kinase phosphorylated in response to cell attachment to fibronectin. Proc. Natl. Acad. Sci. U. S. A. 89, 8487-8491
19. Zheng, C., Xing, Z., Bian, Z. C, Guo, C, Akbay, A., Warner, L., and Guan, J. L. (1998) Differential regulation of Pyk2 and focal adhesion kinase (FAK). The C-terminal domain of FAK confers response to cell adhesion. J. Biol. Chem. 273, 2384-2389
20. Schaller, M. D., Hildebrand, J. D., Shannon, J. D., Fox, J. W., Vines, R. R., and Parsons, J. T. (1994) Autophosphorylation of the focal adhesion kinase, pp125FAK, directs SH2-dependent binding of pp60src. Mol. Cell. Biol. 14, 1680-1688
21. Schlaepfer, D. D., and Hunter, T. (1996) Evidence for in vivo phosphorylation of the Grb2 SH2-domain binding site on focal adhesion kinase by Src-family protein-tyrosine kinases. Mol. Cell. Biol. 16, 5623-5633
22. Panetti, T. S. (2002) Tyrosine phosphorylation of paxillin, FAK, and p130CAS: effects on cell spreading and migration. Front. Biosci. 7, d143-d150
23. Herrera Abreu, M. T., Penton, P. C, Kwok, V., Vachon, E., Shalloway, D., Vidali, L., Lee, W., McCulloch, C. A., and Downey, G. P. (2008) Tyrosine phosphatase PTPa regulates focal adhesion remodeling through Rac1 activation. Am. J. Physiol. Cell Physiol. 294, C931-C944
24. Harder, K. W., Moller, N. P., Peacock, J. W., and Jirik, F. R. (1998) Proteintyrosine phosphatase α regulates Src family kinases and alters cell-substratum adhesion. J. Biol. Chem. 273, 31890-31900
25. Ponniah, S., Wang, D. Z., Lim, K. L., and Pallen, C. J. (1999) Targeted disruption of the tyrosine phosphatase PTPa leads to constitutive downregulation of the kinases Src and Fyn. Curr. Biol. 9, 535-538
26. Su, J., Muranjan, M., and Sap, J. (1999) Receptor protein-tyrosine phosphatase α activates Src-family kinases and controls integrin-mediated responses in fibroblasts. Curr. Biol. 9, 505-511
27. Lammers, R., Lerch, M. M., and Ullrich, A. (2000) The carboxyl-terminal tyrosine residue of protein-tyrosine phosphatase α mediates association with focal adhesion plaques. J. Biol. Chem. 275, 3391-3396
28. Von Wichert, G., Jiang, G., Kostic, A., De Vos, K., Sap, J., and Sheetz, M. P. (2003) RPTP-a acts as a transducer of mechanical force on αv/β3-integrin-cytoskeleton linkages. J. Cell Biol. 161, 143-153
29. Chen, M., Chen, S. C, and Pallen, C. J. (2006) Integrin-induced tyrosine phosphorylation of protein-tyrosine phosphatase-α is required for cytoskeletal reorganization and cell migration. J. Biol. Chem. 281, 11972-11980
30. 2+ signaling. J. Biol. Chem. 284, 20763-20772
31. Brown, M., McCormack, M., Zinn, K. G., Farrell, M. P., Bikel, I., and Livingston, D. M. (1986) A recombinant murine retrovirus for simian virus 40 large T cDNA transforms mouse fibroblasts to anchorage-independent growth. J. Virol. 60, 290-293
32. Golubovskaya, V. M., and Cance, W. G. (2007) Focal adhesion kinase and p53 signaling in cancer cells. Int. Rev. Cytol. 263, 103-153
33. Oakes, S. A., Scorrano, L., Opferman, J. T., Bassik, M. C, Nishino, M., Pozzan, T., and Korsmeyer, S. J. (2005) Proapoptotic BAX and BAK regulate the type 1 inositol trisphosphate receptor and calcium leak from the endoplasmic reticulum. Proc. Natl. Acad. Sci. U. S. A. 102, 105-110
34. McCulloch, C. A., Downey, G. P., and El-Gabalawy, H. (2006) Signalling platforms that modulate the inflammatory response: new targets for drug development. Nat Rev. Drug Discov. 5, 864-876
35. Bolte, S., and Cordelières, F. P. (2006) A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc. 224, 213-232
36. Ilic, D., Furuta, Y., Kanazawa, S., Takeda, N., Sobue, K., Nakatsuji, N., Nomura, S., Fujimoto, J., Okada, M., and Yamamoto, T. (1995) Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 377, 539-544
37. Zheng, X. M., Wang, Y., and Pallen, C. J. (1992) Cell transformation and activation of pp60c-src by overexpression of a protein-tyrosine phosphatase. Nature 359, 336-339
38. Den Hertog, J., Pals, C. E., Peppelenbosch, M. P., Tertoolen, L. G., De Laat, S. W., and Kruijer, W. (1993) Receptor protein-tyrosine phosphatase a activates pp60c-src and is involved in neuronal differentiation. EMBO J. 12, 3789-3798
39. Zeng, L., Si, X., Yu, W. P., Le, H. T., Ng, K. P., Teng, R. M., Ryan, K., Wang, D. Z., Ponniah, S., and Pallen, C. J. (2003) PTPa regulates integrin-stimulated FAK autophosphorylation and cytoskeletal rearrangement in cell spreading and migration. J. Cell Biol. 160, 137-146
40. Arold, S. T. (2011) How focal adhesion kinase achieves regulation by linking ligand binding, localization and action. Curr. Opin. Struct. Biol. 21, 808-813
41. Aplin, A. E., and Juliano, R. L. (1999) Integrin and cytoskeletal regulation of growth factor signaling to the MAP kinase pathway. J. Cell Sci. 112, 695-706
42. Schaller, M. D. (2010) Cellular functions of FAK kinases: insight into molecular mechanisms and novel functions. J. Cell Sci. 123, 1007-1013
43. 2+ signals through the modulation of Ras signaling. Curr. Opin. Cell Biol. 18, 157-161
44. Herrera Abreu, M. T., Wang, Q., Vachon, E., Suzuki, T., Chow, C. W., Wang, Y., Hong, O., Villar, J., McCulloch, C A., and Downey, G. P. (2006) Tyrosine phosphatase SHP-2 regulates IL-1 signaling in fibroblasts through focal adhesions. J. Cell. Physiol. 207, 132-143
45. Arias-Salgado, E. G., Lizano, S., Sarkar, S., Brugge, J. S., Ginsberg, M. H, and Shattil, S. J. (2003) Src kinase activation by direct interaction with the integrin β cytoplasmic domain. Proc. Natl. Acad. Sci. U. S. A. 100, 13298-13302
46. Schaller, M. D., Hildebrand, J. D., and Parsons, J. T. (1999) Complex formation with focal adhesion kinase: A mechanism to regulate activity and subcellular localization of Src kinases. Mol. Biol. Cell 10, 3489-3505
47. Mitra, S. K., and Schlaepfer, D. D. (2006) Integrin-regulated FAK-Src signaling in normal and cancer cells. Curr. Opin. Cell Biol. 18, 516-523
48. Tonks, N. K. (2005) Redox redux: revisiting PTPs and the control of cell signaling. Cell 121, 667-670
49. Alonso, A., Sasin, J., Bottini, N., Friedberg, I., Friedberg, I., Osterman, A., Godzik, A., Hunter, T., Dixon, J., and Mustelin, T. (2004) Protein-tyrosine phosphatases in the human genome. Cell 117, 699-711