Tumor progression locus 2 mediates signal-induced increases in cytoplasmic calcium and cell migration

Science Signaling

Volumn 4, Issue 187, 2011, Pages

  Hatziapostolou, Maria ^a   Koukos, Georgios ^a   Polytarchou, Christos ^a   Kottakis, Filippos ^a   Serebrennikova, Oksana ^a   Kuliopulos, Athan ^a   Tsichlis, Philip N ^a  

^a TUFTS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; G PROTEIN COUPLED RECEPTOR; INOSITOL 1,4,5 TRISPHOSPHATE; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 1BETA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; PHOSPHOLIPASE C BETA3; PROTEIN KINASE C; PROTEINASE ACTIVATED RECEPTOR 1; SPHINGOSINE 1 PHOSPHATE; TUMOR PROGRESSION LOCUS 2; UNCLASSIFIED DRUG; WNT5A PROTEIN; CALCIUM; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; MAP3K8 PROTEIN, HUMAN; ONCOPROTEIN; WNT PROTEIN; WNT5A PROTEIN, HUMAN; WNT5A PROTEIN, MOUSE;

ARTICLE; CALCIUM SIGNALING; CALCIUM TRANSPORT; CANCER CELL; CELL MIGRATION; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVATION; ENZYME REGULATION; FEEDBACK SYSTEM; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; CELL LINE; CELL MOTION; CELL STRAIN HEK293; GENETICS; METABOLISM; MOUSE; MOUSE MUTANT; PHOSPHORYLATION; PHYSIOLOGY;

ANIMALS; CALCIUM; CALCIUM SIGNALING; CELL LINE, TRANSFORMED; CELL MOVEMENT; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GTP-BINDING PROTEIN ALPHA SUBUNIT, GI2; HEK293 CELLS; HUMANS; INOSITOL 1,4,5-TRISPHOSPHATE; MAP KINASE KINASE KINASES; MAP KINASE SIGNALING SYSTEM; MICE; MICE, KNOCKOUT; PHOSPHORYLATION; PROTEIN KINASE C; PROTO-ONCOGENE PROTEINS; RECEPTOR, PAR-1; RECEPTORS, INTERLEUKIN-1; WNT PROTEINS;

EID: 80052194279     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2002006     Document Type: Article

References (56)

1. E. Carafoli, Calcium signaling: A tale for all seasons. Proc. Natl. Acad. Sci. U.S.A. 99, 1115-1122 (2002).
2. D. E. Clapham, Calcium signaling. Cell 131, 1047-1058 (2007).
3. M. J. Berridge, Inositol trisphosphate and calcium signalling mechanisms. Biochim. Biophys. Acta 1793, 933-940 (2009).
4. 2+ store to the plasma membrane. Nature 437, 902-905 (2005).
5. S. G. Rhee, Y. S. Bae, Regulation of phosphoinositide-specific phospholipase C isozymes. J. Biol. Chem. 272, 15045-15048 (1997).
6. G. Carpenter, Q. Ji, Phospholipase C-γ as a signal-transducing element. Exp. Cell Res. 253, 15-24 (1999).
7. H. Mellor, P. J. Parker, The extended protein kinase C superfamily. Biochem. J. 332, 281-292 (1998).
8. M. Katan, New insights into the families of PLC enzymes: Looking back and going forward. Biochem. J. 391, e7-e9 (2005).
9. M. Vig, J. P. Kinet, Calcium signaling in immune cells. Nat. Immunol. 10, 21-27 (2009).
10. G. Giannone, P. Rondé, M. Gaire, J. Beaudouin, J. Haiech, J. Ellenberg, K. Takeda, Calcium rises locally trigger focal adhesion disassembly and enhance residency of focal adhesion kinase at focal adhesions. J. Biol. Chem. 279, 28715-28723 (2004).
11. X. D. Ren, W. B. Kiosses, D. J. Sieg, C. A. Otey, D. D. Schlaepfer, M. A. Schwartz, Focal adhesion kinase suppresses Rho activity to promote focal adhesion turnover. J. Cell Sci. 113, 3673-3678 (2000).
12. S. Yang, J. J. Zhang, X. Y. Huang, Orai1 and STIM1 are critical for breast tumor cell migration and metastasis. Cancer Cell 15, 124-134 (2009).
13. C. Arrieumerlou, T. Meyer, A local coupling model and compass parameter for eukaryotic chemotaxis. Dev. Cell 8, 215-227 (2005).
14. E. M. Gardiner, K. N. Pestonjamasp, B. P. Bohl, C. Chamberlain, K. M. Hahn, G. M. Bokoch, Spatial and temporal analysis of Rac activation during live neutrophil chemotaxis. Curr. Biol. 12, 2029-2034 (2002).
15. 2+ influx is an essential component of the positive-feedback loop that maintains leading-edge structure and activity in macrophages. Proc. Natl. Acad. Sci. U.S.A. 104, 16176-16181 (2007).
16. C. Wei, X. Wang, M. Chen, K. Ouyang, L. S. Song, H. Cheng, Calcium flickers steer cell migration. Nature 457, 901-905 (2009).
17. C. Patriotis, A. Makris, S. E. Bear, P. N. Tsichlis, Tumor progression locus 2 (Tpl-2) encodes a protein kinase involved in the progression of rodent T-cell lymphomas and in T-cell activation. Proc. Natl. Acad. Sci. U.S.A. 90, 2251-2255 (1993).
18. K. M. Erny, J. Peli, J. F. Lambert, V. Muller, H. Diggelmann, Involvement of the Tpl-2/cot oncogene in MMTV tumorigenesis. Oncogene 13, 2015-2020 (1996).
19. C. Patriotis, A. Makris, J. Chernoff, P. N. Tsichlis, Tpl-2 acts in concert with Ras and Raf-1 to activate mitogen-activated protein kinase. Proc. Natl. Acad. Sci. U.S.A. 91, 9755-9759 (1994).
20. A. Salmeron, T. B. Ahmad, G. W. Carlile, D. Pappin, R. P. Narsimhan, S. C. Ley, Activation of MEK-1 and SEK-1 by Tpl-2 proto-oncoprotein, a novel MAP kinase kinase kinase. EMBO J. 15, 817-826 (1996).
21. C. Tsatsanis, C. Patriotis, P. N. Tsichlis, Tpl-2 induces IL-2 expression in T-cell lines by triggering multiple signaling pathways that activate NFAT and NF-κB. Oncogene 17, 2609-2618 (1998).
22. J. D.Ceci, C. P. Patriotis, C. Tsatsanis, A. M. Makris, R. Kovatch, D. A. Swing, N. A. Jenkins, P. N. Tsichlis, N. G. Copeland, Tpl-2 is an oncogenic kinase that is activated by carboxyterminal truncation. Genes Dev. 11, 688-700 (1997).
23. C. M. Johannessen, J. S. Boehm, S. Y. Kim, S. R. Thomas, L. Wardwell, L. A. Johnson, C. M. Emery, N. Stransky, A. P. Cogdill, J. Barretina, G. Caponigro, H. Hieronymus, R. R. Murray, K. Salehi-Ashtiani, D. E. Hill, M. Vidal, J. J. Zhao, X. Yang, O. Alkan, S. Kim, J. L. Harris, C. J. Wilson, V. E. Myer, P. M. Finan, D. E. Root, T. M. Roberts, T. Golub, K. T. Flaherty, R. Dummer, B. L. Weber, W. R. Sellers, R. Schlegel, J.A.Wargo,W.C.Hahn, L. A. Garraway, COT drives resistance to RAF inhibition through MAP kinase pathway reactivation. Nature 468, 968-972 (2010).
24. C. D. Dumitru, J. D. Ceci, C. Tsatsanis, D. Kontoyiannis, K. Stamatakis, J. H. Lin, C. Patriotis, N. A. Jenkins, N. G. Copeland, G. Kollias, P. N. Tsichlis, TNF-α induction by LPS is regulated posttranscriptionally via a Tpl2/ERK-dependent pathway. Cell 103, 1071-1083 (2000).
25. C. Tsatsanis, K. Vaporidi, V. Zacharioudaki, A. Androulidaki, Y. Sykulev, A. N. Margioris, P. N. Tsichlis, Tpl2 and ERK transduce antiproliferative T cell receptor signals and inhibit transformation of chronically stimulated T cells. Proc. Natl. Acad. Sci. U.S.A. 105, 2987-2992 (2008).
26. A. G. Eliopoulos, C. C. Wang, C. D. Dumitru, P. N. Tsichlis, Tpl2 transduces CD40 and TNF signals that activate ERK and regulates IgE induction by CD40. EMBO J. 22, 3855-3864 (2003).
27. M. Hatziapostolou, C. Polytarchou, D. Panutsopulos, L. Covic, P. N. Tsichlis, Proteinase-activated receptor-1-triggered activation of tumor progression locus-2 promotes actin cytoskeleton reorganization and cell migration. Cancer Res. 68, 1851-1861 (2008).
28. S. R. Coughlin, Thrombin signalling and protease-activated receptors. Nature 407, 258-264 (2000).
29. 2+ response in glial cells. Mol. Cells 19, 375-381 (2005).
30. H. R. Kaslow, D. L. Burns, Pertussis toxin and target eukaryotic cells: Binding, entry, and activation. FASEB J. 6, 2684-2690 (1992).
31. L. Covic, A. L. Gresser, A. Kuliopulos, Biphasic kinetics of activation and signaling for PAR1 and PAR4 thrombin receptors in platelets. Biochemistry 39, 5458-5467 (2000).
32. L. M. Keranen, E. M. Dutil, A. C. Newton, Protein kinase C is regulated in vivo by three functionally distinct phosphorylations. Curr. Biol. 5, 1394-1403 (1995).
33. A. C. Newton, Protein kinase C: Poised to signal. Am. J. Physiol. Endocrinol. Metab. 298, E395-E402 (2010).
34. A. C. Newton, Regulation of the ABC kinases by phosphorylation: Protein kinase C as a paradigm. Biochem. J. 370, 361-371 (2003).
35. A. C. Newton, The ins and outs of protein kinase C. Methods Mol. Biol. 233, 3-7 (2003).
36. H. Jiang, Y. Kuang, Y. Wu, A. Smrcka, M. I. Simon, D. Wu, Pertussis toxin-sensitive activation of phospholipase C by the C5a and fMet-Leu-Phe receptors. J. Biol. Chem. 271, 13430-13434 (1996).
37. 2+/calmodulin-dependent protein kinase II to phosphorylate phospholipase Cβ3 on 537-Ser. Mol. Cell. Endocrinol. 175, 149-156 (2001).
38. q. J. Biol. Chem. 273, 18023-18027 (1998).
39. 3 isoform of phospholipase C. Cell. Signal. 21, 737-744 (2009).
40. J. Lee, A. Ishihara, G. Oxford, B. Johnson, K. Jacobson, Regulation of cell movement is mediated by stretch-activated calcium channels. Nature 400, 382-386 (1999).
41. E. J. Joslin, L. K. Opresko, A. Wells, H. S. Wiley, D. A. Lauffenburger, EGF-receptor-mediated mammary epithelial cell migration is driven by sustained ERK signaling from autocrine stimulation. J. Cell Sci. 120, 3688-3699 (2007).
42. D. D. Schlaepfer, T. Hunter, 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 (1997).
43. D. D. Schlaepfer, K. C. Jones, T. Hunter, Multiple Grb2-mediated integrin-stimulated signaling pathways to ERK2/mitogen-activated protein kinase: Summation of both c-Srcand focal adhesion kinase-initiated tyrosine phosphorylation events. Mol. Cell. Biol. 18, 2571-2585 (1998).
44. H. Rosen, P. J. Gonzalez-Cabrera, M. G. Sanna, S. Brown, Sphingosine 1-phosphate receptor signaling. Annu. Rev. Biochem. 78, 743-768 (2009).
45. Y. A. Hannun, L. M. Obeid, Principles of bioactive lipid signalling: Lessons from sphingolipids. Nat. Rev. Mol. Cell Biol. 9, 139-150 (2008).
46. B3/EDG-3. J. Biol. Chem. 276, 33697-33704 (2001).
47. M. Nishita, M. Enomoto, K. Yamagata, Y. Minami, Cell/tissue-tropic functions of Wnt5a signaling in normal and cancer cells. Trends Cell Biol. 20, 346-354 (2010).
48. C. A. Dinarello, Immunological and inflammatory functions of the interleukin-1 family. Annu. Rev. Immunol. 27, 519-550 (2009).
49. M. Grell, G. Zimmermann, E. Gottfried, C. M. Chen, U. Grünwald, D. C. Huang, Y. H. Wu Lee, H. Dürkop, H. Engelmann, P. Scheurich, H. Wajant, A. Strasser, Induction of cell death by tumour necrosis factor (TNF) receptor 2, CD40 and CD30: A role for TNF-R1 activation by endogenous membrane-anchored TNF. EMBO J. 18, 3034-3043 (1999).
50. R. T. Dorsam, J. S. Gutkind, G-protein-coupled receptors and cancer. Nat. Rev. Cancer 7, 79-94 (2007).
51. 2 recognition by its C2 domain. Mol. Biol. Cell 17, 56-66 (2006).
52. S. Corbalán-García, M. Guerrero-Valero, C. Marín-Vicente, J. C. Gómez-Fernández, The C2 domains of classical/conventional PKCs are specific PtdIns(4,5)P(2)-sensing domains. Biochem. Soc. Trans. 35, 1046-1048 (2007).
53. F. Niessen, F. Schaffner, C. Furlan-Freguia, R. Pawlinski, G. Bhattacharjee, J. Chun, C. K. Derian, P. Andrade-Gordon, H. Rosen, W. Ruf, Dendritic cell PAR1-S1P3 signalling couples coagulation and inflammation. Nature 452, 654-658 (2008).
54. D. Iliopoulos, C. Polytarchou, M. Hatziapostolou, F. Kottakis, I. G. Maroulakou, K. Struhl, P. N. Tsichlis, MicroRNAs differentially regulated by Akt isoforms control EMT and stem cell renewal in cancer cells. Sci. Signal. 2, ra62 (2009).
55. S. Swift, A. J. Leger, J. Talavera, L. Zhang, A. Bohm, A. Kuliopulos, Role of the PAR1 receptor 8th helix in signaling: The 7-8-1 receptor activation mechanism. J. Biol. Chem. 281, 4109-4116 (2006).
56. 3 double knockout mice, respectively. Funding: Supported by NIH grants RO1 CA 095431 and R01 CA124835 (P.N.T.) and R01 HL64701 (A.K.). C.P. was a fellow of the Leukemia and Lymphoma Society. Author contributions: M.H., G.K., C.P., F.K., and O.S. performed the experiments; M.H., G.K., and C.P. analyzed the data; and M.H., A.K., and P.N.T. designed the experiments and wrote the paper. Competing interests: The authors declare that they have no competing interests.