Kallikrein-related peptidase 14 acts on proteinase-activated receptor 2 to induce signaling pathway in colon cancer cells

American Journal of Pathology

Volumn 179, Issue 5, 2011, Pages 2625-2636

  Gratio, Valérie ^a   Loriot, Céline ^a   Virca, G Duke ^b   Oikonomopoulou, Katerina ^c,d   Walker, Francine ^a   Diamandis, Eleftherios P ^c   Hollenberg, Morley D ^d   Darmoul, Dalila ^a  

^a INSERM   (France)

^b AMGEN INC   (United States)

^c MOUNT SINAI HOSPITAL   (Canada)

^d UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; KALLIKREIN RELATED PEPTIDASE 14; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEINASE ACTIVATED RECEPTOR 2; TUMOR MARKER; UNCLASSIFIED DRUG;

ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL DIVISION; CELL PROLIFERATION; CELL STRAIN HT29; COLON ADENOCARCINOMA; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ADENOCARCINOMA; CALCIUM SIGNALING; COLONIC NEOPLASMS; HT29 CELLS; HUMANS; KALLIKREINS; MAP KINASE SIGNALING SYSTEM; RECEPTOR, PAR-2; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 80055003183     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2011.07.016     Document Type: Article

References (53)

1. O.R. Mook, W.M. Frederiks, and C.J. Van Noorden The role of gelatinases in colorectal cancer progression and metastasis Biochim Biophys Acta 1705 2004 69 89
2. C. Lopez-Otin, and L.M. Matrisian Emerging roles of proteases in tumour suppression Nat Rev Cancer 7 2007 800 808
3. O. Dery, C.U. Corvera, M. Steinhoff, and N.W. Bunnett Proteinase-activated receptors: novel mechanisms of signaling by serine proteases Am J Physiol 274 1998 C1429 C1452
4. S.R. Macfarlane, M.J. Seatter, T. Kanke, G.D. Hunter, and R. Plevin Proteinase-activated receptors Pharmacol Rev 53 2001 245 282
5. V.S. Ossovskaya, and N.W. Bunnett Protease-activated receptors: contribution to physiology and disease Physiol Rev 84 2004 579 621
6. M.D. Hollenberg, K. Oikonomopoulou, K.K. Hansen, M. Saifeddine, R. Ramachandran, and E.P. Diamandis Kallikreins and proteinase-mediated signaling: proteinase-activated receptors (PARs) and the pathophysiology of inflammatory diseases and cancer Biol Chem 389 2008 643 651
7. M.N. Adams, R. Ramachandran, M.K. Yau, J.Y. Suen, D.P. Fairlie, M.D. Hollenberg, and J.D. Hooper Structure, function and pathophysiology of protease activated receptors Pharmacol Ther 130 2011 248 282
8. D. Darmoul, J.C. Marie, H. Devaud, V. Gratio, and M. Laburthe Initiation of human colon cancer cell proliferation by trypsin acting at protease-activated receptor-2 Br J Cancer 85 2001 772 779
9. D. Darmoul, V. Gratio, H. Devaud, T. Lehy, and M. Laburthe Aberrant expression and activation of the thrombin receptor protease-activated receptor-1 induces cell proliferation and motility in human colon cancer cells Am J Pathol 162 2003 1503 1513
10. M.D. Hollenberg, and S.J. Compton International Union of Pharmacology, XXVIII: proteinase-activated receptors Pharmacol Rev 54 2002 203 217
11. D. Darmoul, V. Gratio, H. Devaud, F. Peiretti, and M. Laburthe Activation of proteinase-activated receptor 1 promotes human colon cancer cell proliferation through epidermal growth factor receptor transactivation Mol Cancer Res 2 2004 514 522
12. D. Darmoul, V. Gratio, H. Devaud, and M. Laburthe Protease-activated receptor 2 in colon cancer: trypsin-induced MAPK phosphorylation and cell proliferation are mediated by epidermal growth factor receptor transactivation J Biol Chem 279 2004 20927 20934
13. V. Gratio, F. Walker, T. Lehy, M. Laburthe, and D. Darmoul Aberrant expression of proteinase-activated receptor 4 promotes colon cancer cell proliferation through a persistent signaling that involves Src and ErbB-2 kinase Int J Cancer 124 2009 1517 1525
14. S. Even-Ram, B. Uziely, P. Cohen, S. Grisaru-Granovsky, M. Maoz, Y. Ginzburg, R. Reich, I. Vlodavsky, and R. Bar-Shavit Thrombin receptor overexpression in malignant and physiological invasion processes Nat Med 4 1998 909 914
15. M.L. Nierodzik, and S. Karpatkin Thrombin induces tumor growth, metastasis, and angiogenesis: evidence for a thrombin-regulated dormant tumor phenotype Cancer Cell 10 2006 355 362
16. R. Ramachandran, and M.D. Hollenberg Proteinases and signalling: pathophysiological and therapeutic implications via PARs and more Br J Pharmacol 153 2008 S263 S282
17. A.J. Ramsay, J.C. Reid, M.N. Adams, H. Samaratunga, Y. Dong, J.A. Clements, and J.D. Hooper Prostatic trypsin-like kallikrein-related peptidases (KLKs) and other prostate-expressed tryptic proteinases as regulators of signalling via proteinase-activated receptors (PARs) Biol Chem 389 2008 653 668
18. K. Oikonomopoulou, E.P. Diamandis, and M.D. Hollenberg Kallikrein-related peptidases: proteolysis and signaling in cancer, the new frontier Biol Chem 391 2010 299 310
19. G.M. Yousef, C.A. Borgono, C. Popalis, G.M. Yacoub, M.E. Polymeris, A. Soosaipillai, and E.P. Diamandis In-silico analysis of kallikrein gene expression in pancreatic and colon cancers Anticancer Res 24 2004 43 51
20. C.V. Obiezu, and E.P. Diamandis Human tissue kallikrein gene family: applications in cancer Cancer Lett 224 2005 1 22
21. K. Oikonomopoulou, K.K. Hansen, M. Saifeddine, I. Tea, M. Blaber, S.I. Blaber, I. Scarisbrick, P. Andrade-Gordon, G.S. Cottrell, N.W. Bunnett, E.P. Diamandis, and M.D. Hollenberg Proteinase-activated receptors, targets for kallikrein signaling J Biol Chem 281 2006 32095 32112
22. K. Stefansson, M. Brattsand, D. Roosterman, C. Kempkes, G. Bocheva, M. Steinhoff, and T. Egelrud Activation of proteinase-activated receptor-2 by human kallikrein-related peptidases J Invest Dermatol 128 2008 18 25
23. A.J. Ramsay, Y. Dong, M.L. Hunt, M. Linn, H. Samaratunga, J.A. Clements, and J.D. Hooper Kallikrein-related peptidase 4 (KLK4) initiates intracellular signaling via protease-activated receptors (PARs): KLK4 and PAR-2 are co-expressed during prostate cancer progression J Biol Chem 283 2008 12293 12304
24. G.J. Mize, W. Wang, and T.K. Takayama Prostate-specific kallikreins-2 and -4 enhance the proliferation of DU-145 prostate cancer cells through protease-activated receptors-1 and -2 Mol Cancer Res 6 2008 1043 1051
25. V. Gratio, N. Beaufort, L. Seiz, J. Maier, G.D. Virca, M. Debela, N. Grebenchtchikov, V. Magdolen, and D. Darmoul Kallikrein-related peptidase 4: a new activator of the aberrantly expressed protease-activated receptor 1 in colon cancer cells Am J Pathol 176 2010 1452 1461
26. M. Brattsand, K. Stefansson, C. Lundh, Y. Haasum, and T. Egelrud A proteolytic cascade of kallikreins in the stratum corneum J Invest Dermatol 124 2005 198 203
27. T. Kanke, H. Ishiwata, M. Kabeya, M. Saka, T. Doi, Y. Hattori, A. Kawabata, and R. Plevin Binding of a highly potent protease-activated receptor-2 (PAR2) activating peptide, [3H]2-furoyl-LIGRL-NH2, to human PAR2 Br J Pharmacol 145 2005 255 263
28. C.A. Borgono, I.P. Michael, J.L. Shaw, L.Y. Luo, M.C. Ghosh, A. Soosaipillai, L. Grass, D. Katsaros, and E.P. Diamandis Expression and functional characterization of the cancer-related serine protease, human tissue kallikrein 14 J Biol Chem 282 2007 2405 2422
29. C.A. Borgono, L. Grass, A. Soosaipillai, G.M. Yousef, C.D. Petraki, D.H. Howarth, S. Fracchioli, D. Katsaros, and E.P. Diamandis Human kallikrein 14: a new potential biomarker for ovarian and breast cancer Cancer Res 63 2003 9032 9041
30. Agence Nationale d'Accréditation et d'Evaluation en Santé Recommendations for cryopreservation of cell tumor tissues to be used for molecular analyses (in French) Ann Pathol 21 2001 184 201
31. French Bioethics Law, No. 2004-800 August 6, 2004 Art. L. 1232-1, Art. L. 1235-2, Art. L. 1245-2
32. R. Salomon, A. Couvineau, C. Rouyer-Fessard, T. Voisin, D. Lavallee, A. Blais, D. Darmoul, and M. Laburthe Characterization of a common VIP-PACAP receptor in human small intestinal epithelium Am J Physiol 264 1993 E294 E300
33. J.L. Shaw, and E.P. Diamandis Distribution of 15 human kallikreins in tissues and biological fluids Clin Chem 53 2007 1423 1432
34. T.J. Harvey, J.D. Hooper, S.A. Myers, S.A. Stephenson, L.K. Ashworth, and J.A. Clements Tissue-specific expression patterns and fine mapping of the human kallikrein (KLK) locus on proximal 19q13.4 J Biol Chem 275 2000 37397 37406
35. J. Trejo Protease-activated receptors: new concepts in regulation of G protein-coupled receptor signaling and trafficking J Pharmacol Exp Ther 307 2003 437 442
36. M. Talieri, L. Li, Y. Zheng, D.K. Alexopoulou, A. Soosaipillai, A. Scorilas, D. Xynopoulos, and E.P. Diamandis The use of kallikrein-related peptidases as adjuvant prognostic markers in colorectal cancer Br J Cancer 100 2009 1659 1665
37. B. Feng, W.B. Xu, M.H. Zheng, J.J. Ma, Q. Cai, Y. Zhang, J. Ji, A.G. Lu, Y. Qu, J.W. Li, M.L. Wang, W.G. Hu, B.Y. Liu, and Z.G. Zhu Clinical significance of human kallikrein 10 gene expression in colorectal cancer and gastric cancer J Gastroenterol Hepatol 21 2006 1596 1603
38. M. Talieri, K. Mathioudaki, P. Prezas, D.K. Alexopoulou, E.P. Diamandis, D. Xynopoulos, A. Ardavanis, N. Arnogiannaki, and A. Scorilas Clinical significance of kallikrein-related peptidase 7 (KLK7) in colorectal cancer Thromb Haemost 101 2009 741 747
39. K. Ogawa, T. Utsunomiya, K. Mimori, F. Tanaka, H. Inoue, H. Nagahara, S. Murayama, and M. Mori Clinical significance of human kallikrein gene 6 messenger RNA expression in colorectal cancer Clin Cancer Res 11 2005 2889 2893
40. I.A. Scarisbrick, S.I. Blaber, J.T. Tingling, M. Rodriguez, M. Blaber, and G.P. Christophi Potential scope of action of tissue kallikreins in CNS immune-mediated disease J Neuroimmunol 178 2006 167 176
41. M.G. Lawrence, J. Lai, and J.A. Clements Kallikreins on steroids: structure, function, and hormonal regulation of prostate-specific antigen and the extended kallikrein locus Endocr Rev 31 2010 407 446
42. R.S. Henkhaus, E.W. Gerner, and N.A. Ignatenko Kallikrein 6 is a mediator of K-RAS-dependent migration of colon carcinoma cells Biol Chem 389 2008 757 764
43. C.A. Borgono, and E.P. Diamandis The emerging roles of human tissue kallikreins in cancer Nat Rev Cancer 4 2004 876 890
44. K. Soreide, E.A. Janssen, H. Korner, and J.P. Baak Trypsin in colorectal cancer: molecular biological mechanisms of proliferation, invasion, and metastasis J Pathol 209 2006 147 156
45. G. Sotiropoulou, G. Pampalakis, and E.P. Diamandis Functional roles of human kallikrein-related peptidases J Biol Chem 284 2009 32989 32994
46. M. Blaber, H. Yoon, M.A. Juliano, I.A. Scarisbrick, and S.I. Blaber Functional intersection of the kallikrein-related peptidases (KLKs) and thrombostasis axis Biol Chem 391 2010 311 320
47. J.I. Zwicker, B.C. Furie, and B. Furie Cancer-associated thrombosis Crit Rev Oncol Hematol 62 2007 126 136
48. D.H. Berger Plasmin/plasminogen system in colorectal cancer World J Surg 26 2002 767 771
49. J. Grondahl-Hansen, E. Ralfkiaer, L.T. Kirkeby, P. Kristensen, L.R. Lund, and K. Dano Localization of urokinase-type plasminogen activator in stromal cells in adenocarcinomas of the colon in humans Am J Pathol 138 1991 111 117
50. N. Emami, and E.P. Diamandis Utility of kallikrein-related peptidases (KLKs) as cancer biomarkers Clin Chem 54 2008 1600 1607
51. K. Oikonomopoulou, K.K. Hansen, M. Saifeddine, N. Vergnolle, I. Tea, E.P. Diamandis, and M.D. Hollenberg Proteinase-mediated cell signalling: targeting proteinase-activated receptors (PARs) by kallikreins and more Biol Chem 387 2006 677 685
52. U.J. Soh, M.R. Dores, B. Chen, and J. Trejo Signal transduction by protease-activated receptors Br J Pharmacol 160 2010 191 203
53. R. Ramachandran, K. Mihara, M. Mathur, M. Rochdi, M. Bouvier, K. Defea, and M.D. Hollenberg Agonist-biased signaling via proteinase activated receptor-2: differential activation of calcium and mitogen-activated protein kinase pathways Mol Pharmacol 76 2009 791 801