Structural Basis for the Interaction between Pyk2-FAT Domain and Leupaxin LD Repeats

Biochemistry

Volumn 55, Issue 9, 2016, Pages 1332-1345

  Vanarotti, Murugendra S ^a   Finkelstein, David B ^b   Guibao, Cristina D ^a   Nourse, Amanda ^a   Miller, Darcie J ^a   Zheng, Jie J ^a,c  

^a Department of Structural Biology ^*  (United States)

^b ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^c JULES STEIN EYE INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESION; AMINO ACIDS; BINS; ENZYMES; GENE EXPRESSION; PROTEINS; SCAFFOLDS (BIOLOGY);

BINDING PARTNERS; BREAST CANCER; FOCAL ADHESION KINASE; FOCAL ADHESIONS; PROLINE-RICH TYROSINE KINASE 2; SCAFFOLD PROTEIN; STRUCTURAL BASIS; TYROSINE KINASE;

BINDING SITES;

FOCAL ADHESION KINASE 2; LEUPAXIN; PAXILLIN; UNCLASSIFIED DRUG; ASPARTIC ACID; CELL ADHESION MOLECULE; LEUCINE; LPXN PROTEIN, HUMAN; PHOSPHOPROTEIN; PROTEIN BINDING;

ARTICLE; BREAST CANCER; CONTROLLED STUDY; CRYSTAL STRUCTURE; FOCAL ADHESION; GENE EXPRESSION; HUMAN; ISOTHERMAL TITRATION CALORIMETRY; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIZE EXCLUSION CHROMATOGRAPHY; X RAY CRYSTALLOGRAPHY; CHEMISTRY; CRYSTALLIZATION; METABOLISM; PHYSIOLOGY; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE;

ASPARTIC ACID; CELL ADHESION MOLECULES; CRYSTALLIZATION; FOCAL ADHESION KINASE 2; FOCAL ADHESIONS; HUMANS; LEUCINE; PHOSPHOPROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY;

EID: 84960349024     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/acs.biochem.5b01274     Document Type: Article

References (58)

1. Avraham, S., London, R., Fu, Y., Ota, S., Hiregowdara, D., Li, J., Jiang, S., Pasztor, L. M., White, R. A., and Groopman, J. E. (1995) Identification and characterization of a novel related adhesion focal tyrosine kinase (RAFTK) from megakaryocytes and brain J. Biol. Chem. 270, 27742-27751 10.1074/jbc.270.46.27742
2. Herzog, H., Nicholl, J., Hort, Y. J., Sutherland, G. R., and Shine, J. (1996) Molecular cloning and assignment of FAK2, a novel human focal adhesion kinase, to 8p11.2-p22 by nonisotopic in situ hybridization Genomics 32, 484-486 10.1006/geno.1996.0149
3. Lev, S., Moreno, H., Martinez, R., Canoll, P., Peles, E., Musacchio, J. M., Plowman, G. D., Rudy, B., and Schlessinger, J. (1995) Protein tyrosine kinase PYK2 involved in Ca(2+)-induced regulation of ion channel and MAP kinase functions Nature 376, 737-745 10.1038/376737a0
4. Sasaki, H., Nagura, K., Ishino, M., Tobioka, H., Kotani, K., and Sasaki, T. (1995) Cloning and characterization of cell adhesion kinase beta, a novel protein-tyrosine kinase of the focal adhesion kinase subfamily J. Biol. Chem. 270, 21206-21219 10.1074/jbc.270.36.21206
5. Le, H. T., Maksumova, L., Wang, J., and Pallen, C. J. (2006) Reduced NMDA receptor tyrosine phosphorylation in PTPalpha-deficient mouse synaptosomes is accompanied by inhibition of four src family kinases and Pyk2: an upstream role for PTPalpha in NMDA receptor regulation J. Neurochem. 98, 1798-1809 10.1111/j.1471-4159.2006.04075.x
6. Paulino, V. M., Yang, Z., Kloss, J., Ennis, M. J., Armstrong, B. A., Loftus, J. C., and Tran, N. L. (2010) TROY (TNFRSF19) is overexpressed in advanced glial tumors and promotes glioblastoma cell invasion via Pyk2-Rac1 signaling Mol. Cancer Res. 8, 1558-1567 10.1158/1541-7786.MCR-10-0334
7. Sun, C. K., Ng, K. T., Sun, B. S., Ho, J. W., Lee, T. K., Ng, I., Poon, R. T., Lo, C. M., Liu, C. L., Man, K., and Fan, S. T. (2007) The significance of proline-rich tyrosine kinase2 (Pyk2) on hepatocellular carcinoma progression and recurrence Br. J. Cancer 97, 50-57 10.1038/sj.bjc.6603827
8. Zhang, Y., Moschetta, M., Huynh, D., Tai, Y. T., Zhang, Y., Zhang, W., Mishima, Y., Ring, J. E., Tam, W. F., Xu, Q., Maiso, P., Reagan, M., Sahin, I., Sacco, A., Manier, S., Aljawai, Y., Glavey, S., Munshi, N. C., Anderson, K. C., Pachter, J., Roccaro, A. M., and Ghobrial, I. M. (2014) Pyk2 promotes tumor progression in multiple myeloma Blood 124, 2675-2686 10.1182/blood-2014-03-563981
9. Parsons, J. T. (2003) Focal adhesion kinase: the first ten years J. Cell Sci. 116, 1409-1416 10.1242/jcs.00373
10. Avraham, H., Avraham, S., and Taniguchi, Y. (2000) Receptor protein tyrosine phosphatases in hematopoietic cells J. Hematother. Stem Cell Res. 9, 425-432 10.1089/152581600419080
11. Schaller, M. D. and Sasaki, T. (1997) Differential signaling by the focal adhesion kinase and cell adhesion kinase beta J. Biol. Chem. 272, 25319-25325 10.1074/jbc.272.40.25319
12. Klingbeil, C. K., Hauck, C. R., Hsia, D. A., Jones, K. C., Reider, S. R., and Schlaepfer, D. D. (2001) Targeting Pyk2 to beta 1-integrin-containing focal contacts rescues fibronectin-stimulated signaling and haptotactic motility defects of focal adhesion kinase-null cells J. Cell Biol. 152, 97-110 10.1083/jcb.152.1.97
13. Tokiwa, G., Dikic, I., Lev, S., and Schlessinger, J. (1996) Activation of Pyk2 by stress signals and coupling with JNK signaling pathway Science 273, 792-794 10.1126/science.273.5276.792
14. Mitra, S. K., Hanson, D. A., and Schlaepfer, D. D. (2005) Focal adhesion kinase: in command and control of cell motility Nat. Rev. Mol. Cell Biol. 6, 56-68 10.1038/nrm1549
15. Yin, B. (2011) Focal adhesion kinase as a target in the treatment of hematological malignancies Leuk. Res. 35, 1416-1418 10.1016/j.leukres.2011.04.017
16. Zhao, J., Zheng, C., and Guan, J. (2000) Pyk2 and FAK differentially regulate progression of the cell cycle J. Cell Sci. 113, 3063-3072
17. Fan, H. and Guan, J. L. (2011) Compensatory function of Pyk2 protein in the promotion of focal adhesion kinase (FAK)-null mammary cancer stem cell tumorigenicity and metastatic activity J. Biol. Chem. 286, 18573-18582 10.1074/jbc.M110.200717
18. Sieg, D. J., Ilic, D., Jones, K. C., Damsky, C. H., Hunter, T., and Schlaepfer, D. D. (1998) Pyk2 and Src-family protein-tyrosine kinases compensate for the loss of FAK in fibronectin-stimulated signaling events but Pyk2 does not fully function to enhance FAK- cell migration EMBO J. 17, 5933-5947 10.1093/emboj/17.20.5933
19. Weis, S. M., Lim, S. T., Lutu-Fuga, K. M., Barnes, L. A., Chen, X. L., Gothert, J. R., Shen, T. L., Guan, J. L., Schlaepfer, D. D., and Cheresh, D. A. (2008) Compensatory role for Pyk2 during angiogenesis in adult mice lacking endothelial cell FAK J. Cell Biol. 181, 43-50 10.1083/jcb.200710038
20. Guinamard, R., Okigaki, M., Schlessinger, J., and Ravetch, J. V. (2000) Absence of marginal zone B cells in Pyk-2-deficient mice defines their role in the humoral response Nat. Immunol. 1, 31-36 10.1038/76882
21. Brown, M. C., Perrotta, J. A., and Turner, C. E. (1996) Identification of LIM3 as the principal determinant of paxillin focal adhesion localization and characterization of a novel motif on paxillin directing vinculin and focal adhesion kinase binding J. Cell Biol. 135, 1109-1123 10.1083/jcb.135.4.1109
22. Brown, M. C. and Turner, C. E. (2004) Paxillin: adapting to change Physiol. Rev. 84, 1315-1339 10.1152/physrev.00002.2004
23. Thomas, J. W., Cooley, M. A., Broome, J. M., Salgia, R., Griffin, J. D., Lombardo, C. R., and Schaller, M. D. (1999) The role of focal adhesion kinase binding in the regulation of tyrosine phosphorylation of paxillin J. Biol. Chem. 274, 36684-36692 10.1074/jbc.274.51.36684
24. Schlaepfer, D. D., Mitra, S. K., and Ilic, D. (2004) Control of motile and invasive cell phenotypes by focal adhesion kinase Biochim. Biophys. Acta, Mol. Cell Res. 1692, 77-102 10.1016/j.bbamcr.2004.04.008
25. Tachibana, K., Sato, T., D'Avirro, N., and Morimoto, C. (1995) Direct association of pp125FAK with paxillin, the focal adhesion-targeting mechanism of pp125FAK J. Exp. Med. 182, 1089-1099 10.1084/jem.182.4.1089
26. Yano, H., Mazaki, Y., Kurokawa, K., Hanks, S. K., Matsuda, M., and Sabe, H. (2004) Roles played by a subset of integrin signaling molecules in cadherin-based cell-cell adhesion J. Cell Biol. 166, 283-295 10.1083/jcb.200312013
27. Liu, G., Guibao, C. D., and Zheng, J. (2002) Structural insight into the mechanisms of targeting and signaling of focal adhesion kinase Mol. Cell. Biol. 22, 2751-2760 10.1128/MCB.22.8.2751-2760.2002
28. Gao, G., Prutzman, K. C., King, M. L., Scheswohl, D. M., DeRose, E. F., London, R. E., Schaller, M. D., and Campbell, S. L. (2004) NMR solution structure of the focal adhesion targeting domain of focal adhesion kinase in complex with a paxillin LD peptide: evidence for a two-site binding model J. Biol. Chem. 279, 8441-8451 10.1074/jbc.M309808200
29. Arold, S. T., Hoellerer, M. K., and Noble, M. E. (2002) The structural basis of localization and signaling by the focal adhesion targeting domain Structure 10, 319-327 10.1016/S0969-2126(02)00717-7
30. Hayashi, I., Vuori, K., and Liddington, R. C. (2002) The focal adhesion targeting (FAT) region of focal adhesion kinase is a four-helix bundle that binds paxillin Nat. Struct. Biol. 9, 101-106 10.1038/nsb755
31. Magis, A. T., Bailey, K. M., Kurenova, E. V., Hernandez Prada, J. A., Cance, W. G., and Ostrov, D. A. (2008) Crystallization of the focal adhesion kinase targeting (FAT) domain in a primitive orthorhombic space group Acta Crystallogr., Sect. F: Struct. Biol. Cryst. Commun. 64, 564-566 10.1107/S1744309108011421
32. Zhou, Z., Feng, H., and Bai, Y. (2006) Detection of a hidden folding intermediate in the focal adhesion target domain: Implications for its function and folding Proteins: Struct., Funct., Genet. 65, 259-265 10.1002/prot.21107
33. Bertolucci, C. M., Guibao, C. D., and Zheng, J. (2005) Structural features of the focal adhesion kinase-paxillin complex give insight into the dynamics of focal adhesion assembly Protein Sci. 14, 644-652 10.1110/ps.041107205
34. Lulo, J., Yuzawa, S., and Schlessinger, J. (2009) Crystal structures of free and ligand-bound focal adhesion targeting domain of Pyk2 Biochem. Biophys. Res. Commun. 383, 347-352 10.1016/j.bbrc.2009.04.011
35. Scheswohl, D. M., Harrell, J. R., Rajfur, Z., Gao, G., Campbell, S. L., and Schaller, M. D. (2014) Multiple paxillin binding sites regulate FAK function J. Mol. Signaling 3, 1 10.1186/1750-2187-3-1
36. Vanarotti, M. S., Miller, D. J., Guibao, C. D., Nourse, A., and Zheng, J. J. (2014) Structural and mechanistic insights into the interaction between Pyk2 and paxillin LD motifs J. Mol. Biol. 426, 3985-4001 10.1016/j.jmb.2014.08.014
37. Lipsky, B. P., Beals, C. R., and Staunton, D. E. (1998) Leupaxin is a novel LIM domain protein that forms a complex with PYK2 J. Biol. Chem. 273, 11709-11713 10.1074/jbc.273.19.11709
38. Sahu, S. N., Nunez, S., Bai, G., and Gupta, A. (2007) Interaction of Pyk2 and PTP-PEST with leupaxin in prostate cancer cells Am. J. Physiol Cell Physiol 292, C2288-C2296 10.1152/ajpcell.00503.2006
39. Lorenz, S., Vakonakis, I., Lowe, E. D., Campbell, I. D., Noble, M. E., and Hoellerer, M. K. (2008) Structural analysis of the interactions between paxillin LD motifs and alpha-parvin Structure 16, 1521-1531 10.1016/j.str.2008.08.007
40. Bos, P. D., Zhang, X. H., Nadal, C., Shu, W., Gomis, R. R., Nguyen, D. X., Minn, A. J., van de Vijver, M. J., Gerald, W. L., Foekens, J. A., and Massague, J. (2009) Genes that mediate breast cancer metastasis to the brain Nature 459, 1005-1009 10.1038/nature08021
41. Neidhardt, F. C., Bloch, P. L., and Smith, D. F. (1974) Culture medium for enterobacteria J. Bacteriol. 119, 736-747
42. Zhang, Z. M., Simmerman, J. A., Guibao, C. D., and Zheng, J. J. (2008) GIT1 paxillin-binding domain is a four-helix bundle, and it binds to both paxillin LD2 and LD4 motifs J. Biol. Chem. 283, 18685-18693 10.1074/jbc.M801274200
43. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics Acta Crystallogr., Sect. D: Biol. Crystallogr. 60, 2126-2132 10.1107/S0907444904019158
44. Adams, P. D., Afonine, P. V., Bunkoczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr., Sect. D: Biol. Crystallogr. 66, 213-221 10.1107/S0907444909052925
45. Chen, V. B., Arendall, W. B., 3rd, Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity: all-atom structure validation for macromolecular crystallography Acta Crystallogr., Sect. D: Biol. Crystallogr. 66, 12-21 10.1107/S0907444909042073
46. DeLano, W. L. (2002. The PyMOL Molecular Graphics System. DeLano Scientific; San Carlos.
47. Otwinowski, Z. M. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276, 307-326 10.1016/S0076-6879(97)76066-X
48. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software J. Appl. Crystallogr. 40, 658-674 10.1107/S0021889807021206
49. Kabsch, W. (2010) Xds Acta Crystallogr., Sect. D: Biol. Crystallogr. 66, 125-132 10.1107/S0907444909047337
50. Keller, R. (2004. The Computer Aided Resonance Assignment Tutorial. Verlag, Cantina, Switzerland.
51. Farmer, B. T., 2nd, Constantine, K. L., Goldfarb, V., Friedrichs, M. S., Wittekind, M., Yanchunas, J., Jr., Robertson, J. G., and Mueller, L. (1996) Localizing the NADP+ binding site on the MurB enzyme by NMR Nat. Struct. Biol. 3, 995-997 10.1038/nsb1296-995
52. Garrett, D. S., Seok, Y. J., Peterkofsky, A., Clore, G. M., and Gronenborn, A. M. (1997) Identification by NMR of the binding surface for the histidine-containing phosphocarrier protein HPr on the N-terminal domain of enzyme I of the Escherichia coli phosphotransferase system Biochemistry 36, 4393-4398 10.1021/bi970221q
53. Grzesiek, S., Bax, A., Clore, G. M., Gronenborn, A. M., Hu, J. S., Kaufman, J., Palmer, I., Stahl, S. J., and Wingfield, P. T. (1996) The solution structure of HIV-1 Nef reveals an unexpected fold and permits delineation of the binding surface for the SH3 domain of Hck tyrosine protein kinase Nat. Struct. Biol. 3, 340-345 10.1038/nsb0496-340
54. Zrihan-Licht, S., Fu, Y., Settleman, J., Schinkmann, K., Shaw, L., Keydar, I., Avraham, S., and Avraham, H. (2000) RAFTK/Pyk2 tyrosine kinase mediates the association of p190 RhoGAP with RasGAP and is involved in breast cancer cell invasion Oncogene 19, 1318-1328 10.1038/sj.onc.1203422
55. Chen, P. W. and Kroog, G. S. (2010) Leupaxin is similar to paxillin in focal adhesion targeting and tyrosine phosphorylation but has distinct roles in cell adhesion and spreading Cell adhesion & migration 4, 527-540 10.4161/cam.4.4.12399
56. Thompson, J. D., Higgins, D. G., and Gibson, T. J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Nucleic Acids Res. 22, 4673-4680 10.1093/nar/22.22.4673
57. Katsumi, A., Kiyoi, H., Abe, A., Tanizaki, R., Iwasaki, T., Kobayashi, M., Matsushita, T., Kaibuchi, K., Senga, T., Kojima, T., Kohno, T., Hamaguchi, M., and Naoe, T. (2011) FLT3/ ITD regulates leukaemia cell adhesion through alpha4beta1 integrin and Pyk2 signalling Eur. J. Haematol. 86, 191-198 10.1111/j.1600-0609.2010.01556.x
58. Sun, C. K., Ng, K. T., Lim, Z. X., Cheng, Q., Lo, C. M., Poon, R. T., Man, K., Wong, N., and Fan, S. T. (2011) Proline-rich tyrosine kinase 2 (Pyk2) promotes cell motility of hepatocellular carcinoma through induction of epithelial to mesenchymal transition PLoS One 6, e18878 10.1371/journal.pone.0018878