Table of Contents
Journal of Signal Transduction
Volume 2013, Article ID 956580, 12 pages
http://dx.doi.org/10.1155/2013/956580
Research Article

A Novel Interaction between Pyk2 and MAP4K4 Is Integrated with Glioma Cell Migration

1Department of Biochemistry and Molecular Biology, Mayo Clinic Arizona, 13400 East Shea Boulevard, Scottsdale, AZ 85259, USA
2Translational Genomics Research Institute, Phoenix, AZ 85004, USA

Received 17 June 2013; Revised 7 August 2013; Accepted 15 August 2013

Academic Editor: Matthias Gaestel

Copyright © 2013 Joseph C. Loftus et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. Giese, R. Bjerkvig, M. E. Berens, and M. Westphal, “Cost of migration: invasion of malignant gliomas and implications for treatment,” Journal of Clinical Oncology, vol. 21, no. 8, pp. 1624–1636, 2003. View at Publisher · View at Google Scholar · View at Scopus
  2. R. Stupp, W. P. Mason, M. J. van den Bent et al., “Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma,” The New England Journal of Medicine, vol. 352, no. 10, pp. 987–996, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. M. E. Berens and A. Giese, “‘...those left behind.’ Biology and oncology of invasive glioma cells,” Neoplasia, vol. 1, no. 3, pp. 208–219, 1999. View at Google Scholar · View at Scopus
  4. F. Lefranc, J. Brotchi, and R. Kiss, “Possible future issues in the treatment of glioblastomas: special emphasis on cell migration and the resistance of migrating glioblastoma cells to apoptosis,” Journal of Clinical Oncology, vol. 23, no. 10, pp. 2411–2422, 2005. View at Publisher · View at Google Scholar · View at Scopus
  5. M. D. Schaller, “Cellular functions of FAK kinases: insight into molecular mechanisms and novel functions,” Journal of Cell Science, vol. 123, no. 7, pp. 1007–1013, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. I. H. Gelman, “Pyk2 FAKs, any two FAKs,” Cell Biology International, vol. 27, no. 7, pp. 507–510, 2003. View at Publisher · View at Google Scholar · View at Scopus
  7. H. Avraham, S.-Y. Park, K. Schinkmann, and S. Avraham, “RAFTK/Pyk2-mediated cellular signalling,” Cellular Signalling, vol. 12, no. 3, pp. 123–133, 2000. View at Publisher · View at Google Scholar · View at Scopus
  8. D. B. Hoelzinger, L. Mariani, J. Wies et al., “Gene expression profile of glioblastoma multiforme invasive phenotype points to new therapeutic targets,” Neoplasia, vol. 7, no. 1, pp. 7–16, 2005. View at Publisher · View at Google Scholar · View at Scopus
  9. C. A. Lipinski, N. L. Tran, E. Menashi et al., “The tyrosine kinase Pyk2 promotes migration and invasion of glioma cells,” Neoplasia, vol. 7, no. 5, pp. 435–445, 2005. View at Publisher · View at Google Scholar · View at Scopus
  10. C. A. Lipinski, N. L. Tran, C. Viso et al., “Extended survival of Pyk2 or FAK deficient orthotopic glioma xenografts,” Journal of Neuro-Oncology, vol. 90, no. 2, pp. 181–189, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. C. A. Lipinski, N. L. Tran, A. Dooley et al., “Critical role of the FERM domain in Pyk2 stimulated glioma cell migration,” Biochemical and Biophysical Research Communications, vol. 349, no. 3, pp. 939–947, 2006. View at Publisher · View at Google Scholar · View at Scopus
  12. J. C. Loftus, Z. Yang, N. L. Tran et al., “The Pyk2 FERM domain as a target to inhibit glioma migration,” Molecular Cancer Therapeutics, vol. 8, no. 6, pp. 1505–1514, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. A. Astier, H. Avraham, S. N. Manie et al., “The related adhesion focal tyrosine kinase is tyrosine-phosphorylated after β1-integrin stimulation in B cells and binds to p130cas,” Journal of Biological Chemistry, vol. 272, no. 1, pp. 228–232, 1997. View at Publisher · View at Google Scholar · View at Scopus
  14. K. Ueki, T. Mimura, T. Nakamoto et al., “Integrin-mediated signal transduction in cells lacking focal adhesion kinase p125FAK,” FEBS Letters, vol. 432, no. 3, pp. 197–201, 1998. View at Publisher · View at Google Scholar · View at Scopus
  15. S. Lev, H. Moreno, R. Martinez et al., “Protein tyrosine kinase PYK2 involved in Ca2+-induced regulation of ion channel and MAP kinase functions,” Nature, vol. 376, no. 6543, pp. 737–745, 1995. View at Publisher · View at Google Scholar · View at Scopus
  16. G. Tokiwa, I. Dikic, S. Lev, and J. Schlessinger, “Activation of Pyk2 by stress signals and coupling with JNK signaling pathway,” Science, vol. 273, no. 5276, pp. 792–794, 1996. View at Google Scholar · View at Scopus
  17. I. Hayashi, K. Vuori, and R. C. Liddington, “The focal adhesion targeting (FAT) region of focal adhesion kinase is a four-helix bundle that binds paxillin,” Nature Structural Biology, vol. 9, no. 2, pp. 101–106, 2002. View at Publisher · View at Google Scholar · View at Scopus
  18. G. Liu, C. D. Guibao, and J. Zheng, “Structural insight into the mechanisms of targeting and signaling of focal adhesion kinase,” Molecular and Cellular Biology, vol. 22, no. 8, pp. 2751–2760, 2002. View at Publisher · View at Google Scholar · View at Scopus
  19. A. Richardson and T. Parsons, “A mechanism for regulation of the adhesion-associated protein tyrosine kinase pp125FAK,” Nature, vol. 380, pp. 538–540, 1996. View at Google Scholar
  20. A. Richardson, R. K. Malik, J. D. Hildebrand, and J. T. Parsons, “Inhibition of cell spreading by expression of the C-terminal domain of focal adhesion kinase (FAK) is rescued by coexpression of Src or catalytically inactive FAK: a role for paxillin tyrosine phosphorylation,” Molecular and Cellular Biology, vol. 17, no. 12, pp. 6906–6914, 1997. View at Google Scholar · View at Scopus
  21. J. Lulo, S. Yuzawa, and J. Schlessinger, “Crystal structures of free and ligand-bound focal adhesion targeting domain of Pyk2,” Biochemical and Biophysical Research Communications, vol. 383, no. 3, pp. 347–352, 2009. View at Publisher · View at Google Scholar · View at Scopus
  22. D. Riggs, Z. Yang, J. Kloss, and J. C. Loftus, “The Pyk2 FERM regulates Pyk2 complex formation and phosphorylation,” Cellular Signalling, vol. 23, no. 1, pp. 288–296, 2011. View at Publisher · View at Google Scholar · View at Scopus
  23. T. Kohno, E. Matsuda, H. Sasaki, and T. Sasaki, “Protein-tyrosine kinase CAKβ/PYK2 is activated by binding Ca 2+/calmodulin to FERM F2 α2 helix and thus forming its dimer,” Biochemical Journal, vol. 410, no. 3, pp. 513–523, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. J. M. de Pereda, K. L. Wegener, E. Santelli et al., “Structural basis for phosphatidylinositol phosphate kinase type I gamma binding to talin at focal adhesions,” Journal of Biological Chemistry, vol. 280, no. 9, pp. 8381–8386, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. B. García-Alvarez, J. M. de Pereda, D. A. Calderwood et al., “Structural determinants of integrin recognition by talin,” Molecular Cell, vol. 11, no. 1, pp. 49–58, 2003. View at Publisher · View at Google Scholar · View at Scopus
  26. K. Hamada, T. Shimizu, S. Yonemura, S. Tsukita, S. Tsukita, and T. Hakoshima, “Structural basis of adhesion-molecule recognition by ERM proteins revealed by the crystal structure of the radixin-ICAM-2 complex,” EMBO Journal, vol. 22, no. 3, pp. 502–514, 2003. View at Publisher · View at Google Scholar · View at Scopus
  27. Y. Takai, K. Kitano, S. Terawaki, R. Maesaki, and T. Hakoshima, “Structural basis of PSGL-1 binding to ERM proteins,” Genes to Cells, vol. 12, no. 12, pp. 1329–1338, 2007. View at Publisher · View at Google Scholar · View at Scopus
  28. Y. Takai, K. Kitano, S. I. Terawaki, R. Maesaki, and T. Hakoshima, “Structural basis of the cytoplasmic tail of adhesion molecule CD43 and its binding to ERM proteins,” Journal of Molecular Biology, vol. 381, no. 3, pp. 634–644, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. T. Mori, K. Kitano, S.-I. Terawaki, R. Maesaki, Y. Fukami, and T. Hakoshima, “Structural basis for CD44 recognition by ERM proteins,” Journal of Biological Chemistry, vol. 283, no. 43, pp. 29602–29612, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. S.-I. Terawaki, K. Kitano, and T. Hakoshima, “Structural basis for type II membrane protein binding by ERM proteins revealed by the radixin-neutral endopeptidase 24.11 (NEP) complex,” Journal of Biological Chemistry, vol. 282, no. 27, pp. 19854–19862, 2007. View at Publisher · View at Google Scholar · View at Scopus
  31. D. F. J. Ceccarelli, H. K. Song , F. Poy, M. D. Schaller, and M. J. Eck, “Crystal structure of the FERM domain of focal adhesion kinase,” Journal of Biological Chemistry, vol. 281, no. 1, pp. 252–259, 2006. View at Publisher · View at Google Scholar · View at Scopus
  32. D. Lietha, X. Cai, D. F. J. Ceccarelli, Y. Li, M. D. Schaller, and M. J. Eck, “Structural basis for the autoinhibition of focal adhesion kinase,” Cell, vol. 129, no. 6, pp. 1177–1187, 2007. View at Publisher · View at Google Scholar · View at Scopus
  33. J. M. Dunty, V. Gabarra-Niecko, M. L. King, D. F. J. Ceccarelli, M. J. Eck, and M. D. Schaller, “FERM domain interaction promotes FAK signaling,” Molecular and Cellular Biology, vol. 24, no. 12, pp. 5353–5368, 2004. View at Publisher · View at Google Scholar · View at Scopus
  34. C. A. Lipinski, N. L. Tran, C. Bay et al., “Differential role of proline-rich tyrosine kinase 2 and focal adhesion kinase in determining glioblastoma migration and proliferation,” Molecular Cancer Research, vol. 1, no. 5, pp. 323–332, 2003. View at Google Scholar · View at Scopus
  35. J. H. Wright, X. Wang, G. Manning et al., “The STE20 kinase HGK is broadly expressed in human tumor cells and can modulate cellular transformation, invasion, and adhesion,” Molecular and Cellular Biology, vol. 23, no. 6, pp. 2068–2082, 2003. View at Publisher · View at Google Scholar · View at Scopus
  36. K. D. Mack, M. V. Goetz, M. Lin et al., “Functional identification of kinases essential for T-cell activation through a genetic suppression screen,” Immunology Letters, vol. 96, no. 1, pp. 129–145, 2005. View at Publisher · View at Google Scholar · View at Scopus
  37. C. S. Collins, J. Hong, L. Sapinoso et al., “A small interfering RNA screen for modulators of tumor cell motility identifies MAP4K4 as a promigratory kinase,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 10, pp. 3775–3780, 2006. View at Publisher · View at Google Scholar · View at Scopus
  38. A. Giese, M. D. Rief, M. A. Loo, and M. E. Berens, “Determinants of human astrocytoma migration,” Cancer Research, vol. 54, no. 14, pp. 3897–3904, 1994. View at Google Scholar · View at Scopus
  39. K. Lamszus, N. O. Schmidt, L. Jin et al., “Scatter factor promotes motility of human glioma and neuromicrovascular endothelial cells,” International Journal of Cancer, vol. 75, pp. 19–28, 1998. View at Google Scholar
  40. F. Di Cunto, E. Calautti, J. Hsiao et al., “Citron Rho-interacting kinase, a novel tissue-specific Ser/Thr kinase encompassing the Rho-Rac-binding protein citron,” Journal of Biological Chemistry, vol. 273, no. 45, pp. 29706–29711, 1998. View at Publisher · View at Google Scholar · View at Scopus
  41. Y. Su, J. Han, S. Xu, M. Cobb, and E. Skolnik, “NIK is a new Ste20-related kinase that binds NCK and MEKK1 and activates the SAPK/JNK cascade via a conserved regulatory domain,” EMBO Journal, vol. 16, no. 6, pp. 1279–1290, 1997. View at Publisher · View at Google Scholar · View at Scopus
  42. A. H. Chishti, A. C. Kim, S. M. Marfatia et al., “The FERM domain: a unique module involved in the linkage of cytoplasmic proteins to the membrane,” Trends in Biochemical Sciences, vol. 23, no. 8, pp. 281–282, 1998. View at Publisher · View at Google Scholar · View at Scopus
  43. S. Lev, J. Hernandez, R. Martinez, A. Chen, G. Plowman, and J. Schlessinger, “Identification of a novel family of targets of PYK2 related to Drosophila retinal degeneration B (rdGB) protein,” Molecular and Cellular Biology, vol. 19, no. 3, pp. 2278–2288, 1999. View at Google Scholar · View at Scopus
  44. S. Abbi, H. Ueda, C. Zheng et al., “Regulation of focal adhesion kinase by a novel protein inhibitor FIP200,” Molecular Biology of the Cell, vol. 13, no. 9, pp. 3178–3191, 2002. View at Publisher · View at Google Scholar · View at Scopus
  45. S.-T. Lim, N. L. G. Miller, J.-O. Nam, X. L. Chen, Y. Lim, and D. D. Schlaepfer, “Pyk2 inhibition of p53 as an adaptive and intrinsic mechanism facilitating cell proliferation and survival,” Journal of Biological Chemistry, vol. 285, no. 3, pp. 1743–1753, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. P. Madaule, T. Furuyashiki, T. Reid et al., “A novel partner for the GTP-bound forms of rho and rac,” FEBS Letters, vol. 377, no. 2, pp. 243–248, 1995. View at Publisher · View at Google Scholar · View at Scopus
  47. P. Poinat, A. De Arcangelis, S. Sookhareea et al., “A conserved interaction between β1 integrin/PAT-3 and Nck-interacting kinase/MIG-15 that mediates commissural axon navigation in C. elegans,” Current Biology, vol. 12, no. 8, pp. 622–631, 2002. View at Publisher · View at Google Scholar · View at Scopus
  48. Z. Yao, G. Zhou, X. S. Wang et al., “A novel human STE20-related protein kinase, HGK, that specifically activates the c-Jun N-terminal kinase signaling pathway,” Journal of Biological Chemistry, vol. 274, no. 4, pp. 2118–2125, 1999. View at Publisher · View at Google Scholar · View at Scopus
  49. J.-M. Hao, J.-Z. Chen, H.-M. Sui et al., “A five-gene signature as a potential predictor of metastasis and survival in colorectal cancer,” Journal of Pathology, vol. 220, no. 4, pp. 475–489, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. Y.-C. Su, J. E. Treisman, and E. Y. Skolnik, “The Drosophila Ste20-related kinase misshapen is required for embryonic dorsal closure and acts through a JNK MAPK module on an evolutionarily conserved signaling pathway,” Genes and Development, vol. 12, no. 15, pp. 2371–2380, 1998. View at Google Scholar · View at Scopus
  51. Y. Xue, X. Wang, Z. Li, N. Gotoh, D. Chapman, and E. Y. Skolnik, “Mesodermal patterning defect in mice lacking the Ste20 NCK interacting kinase (NIK),” Development, vol. 128, no. 9, pp. 1559–1572, 2001. View at Google Scholar · View at Scopus
  52. D. B. Ramnarain, S. Park, D. Y. Lee et al., “Differential gene expression analysis reveals generation of an autocrine loop by a mutant epidermal growth factor receptor in glioma cells,” Cancer Research, vol. 66, no. 2, pp. 867–874, 2006. View at Publisher · View at Google Scholar · View at Scopus
  53. M. Baumgartner, A. L. Sillman, E. M. Blackwood et al., “The Nck-interacting kinase phosphorylates ERM proteins for formation of lamellipodium by growth factors,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 36, pp. 13391–13396, 2006. View at Publisher · View at Google Scholar · View at Scopus
  54. S. Eden, R. Rohatgi, A. V. Podtelejnikov, M. Mann, and M. W. Kirschner, “Mechanism of regulation of WAVE1-induced actin nucleation by Rac1 and Nck,” Nature, vol. 418, no. 6899, pp. 790–793, 2002. View at Publisher · View at Google Scholar · View at Scopus
  55. R. Rohatgi, P. Nollau, H.-Y. Ho, M. W. Kirschner, and B. J. Mayer, “Nck and Phosphatidylinositol 4,5-bisphosphate synergistically activate actin polymerization through the N-WASP-Arp2/3 Pathway,” Journal of Biological Chemistry, vol. 276, no. 28, pp. 26448–26452, 2001. View at Publisher · View at Google Scholar · View at Scopus
  56. N. Machida, M. Umikawa, K. Takei et al., “Mitogen-activated protein kinase kinase kinase kinase 4 as a putative effector of Rap2 to activate the c-Jun N-terminal kinase,” Journal of Biological Chemistry, vol. 279, no. 16, pp. 15711–15714, 2004. View at Publisher · View at Google Scholar · View at Scopus
  57. C. H. Yoon, M. J. Kim, R. K. Kim et al., “c-Jun N-terminal kinase has a pivotal role in the maintenance of self-renewal and tumorigenicity in glioma stem-like cells,” Oncogene, vol. 31, pp. 4655–4666, 2012. View at Publisher · View at Google Scholar · View at Scopus
  58. A. A. Antonyak, L. C. Kenyon, A. K. Godwin et al., “Elevated JNK activation contributes to the pathogenesis of human brain tumors,” Oncogene, vol. 21, no. 33, pp. 5038–5046, 2002. View at Publisher · View at Google Scholar · View at Scopus
  59. J. Cui, S.-Y. Han, C. Wang et al., “c-Jun NH2-terminal kinase 2α2 promotes the tumorigenicity of human glioblastoma cells,” Cancer Research, vol. 66, no. 20, pp. 10024–10031, 2006. View at Publisher · View at Google Scholar · View at Scopus
  60. S. J. McLeod, A. J. Shum, R. L. Lee, F. Takei, and M. R. Gold, “The rap GTPases regulate integrin-mediated adhesion, cell spreading, actin polymerization, and Pyk2 tyrosine phosphorylation in B lymphocytes,” Journal of Biological Chemistry, vol. 279, no. 13, pp. 12009–12019, 2004. View at Publisher · View at Google Scholar · View at Scopus