Meprinα transactivates the epidermal growth factor receptor (EGFR) via ligand shedding, thereby enhancing colorectal cancer cell proliferation and migration

Journal of Biological Chemistry

Volumn 287, Issue 42, 2012, Pages 35201-35211

  Minder, Petra ^a   Bayha, Elke ^a   Becker Pauly, Christoph ^b   Sterchi, Erwin E ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b UNIVERSITY OF KIEL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COLONOCYTES; COLORECTAL ADENOCARCINOMA; COLORECTAL CANCER; COLORECTAL CANCER CELL; EGFR SIGNALING; ELISA ASSAY; EPIDERMAL GROWTH FACTOR RECEPTORS; EPIDERMAL GROWTH FACTORS; METALLO-PROTEASE; PHYSIOLOGICAL EFFECTS; SIGNALING PATHWAYS; TRANSACTIVATION; TRANSFORMING GROWTH FACTORS; TUMOR SITE; TUMOR-STROMA;

CELL MEMBRANES; CELL PROLIFERATION; ENZYME INHIBITION; GROWTH KINETICS; LIGANDS; PHOSPHATASES; PHOSPHORYLATION; TUMORS;

DISEASES;

ACTINONIN; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; MEPRIN; MEPRIN ALPHA; MITOGEN ACTIVATED PROTEIN KINASE 1; TRANSFORMING GROWTH FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CANCER GROWTH; CELL MIGRATION; CELL PROLIFERATION; CELL STRAIN CACO 2; COLORECTAL CANCER; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANTI-BACTERIAL AGENTS; CACO-2 CELLS; CELL MOVEMENT; CELL PROLIFERATION; COLORECTAL NEOPLASMS; HUMANS; HYDROXAMIC ACIDS; LIGANDS; MAP KINASE SIGNALING SYSTEM; METALLOENDOPEPTIDASES; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; NEOPLASM PROTEINS; PHOSPHORYLATION; RECEPTOR, EPIDERMAL GROWTH FACTOR; TRANSFORMING GROWTH FACTOR ALPHA;

EID: 84867406255     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.368910     Document Type: Article

References (62)

1. Fischer, O. M., Hart, S., Gschwind, A., and Ullrich, A. (2003) EGFR signal transactivation in cancer cells. Biochem. Soc. Trans. 31, 1203-1208 (Pubitemid 38030939)
2. Parkin, D. M., Bray, F., Ferlay, J., and Pisani, P. (2005) Global cancer statistics, 2002. CA Cancer J. Clin. 55, 74-108 (Pubitemid 40372904)
3. Yarom, N., and Jonker, D. J. (2011) The role of the epidermal growth factor receptor in the mechanism and treatment of colorectal cancer. Discov.Med. 11, 95-105
4. Cohen, S. (1965) The stimulation of epidermal proliferation by a specific protein (EGF). Dev. Biol. 12, 394-407
5. Higashiyama, S., Abraham, J. A., Miller, J., Fiddes, J. C., and Klagsbrun, M. (1991)Aheparin-binding growth factor secreted by macrophage-like cells that is related to EGF. Science 251, 936-939 (Pubitemid 21926188)
6. Derynck, R., Roberts, A. B., Winkler, M. E., Chen, E. Y., and Goeddel, D. V. (1984) Human transforming growth factor-α: precursor structure and expression in E. coli. Cell 38, 287-297 (Pubitemid 15216556)
7. Shing, Y., Christofori, G., Hanahan, D., Ono, Y., Sasada, R., Igarashi, K., and Folkman, J. (1993) Betacellulin: a mitogen from pancreatic beta cell tumors. Science 259, 1604-1607 (Pubitemid 23114638)
8. Shoyab, M., Plowman, G. D., McDonald, V. L., Bradley, J. G., and Todaro, G. J. (1989) Structure and function of human amphiregulin: a member of the epidermal growth factor family. Science 243, 1074-1076 (Pubitemid 19072586)
9. Toyoda, H., Komurasaki, T., Uchida, D., Takayama, Y., Isobe, T., Okuyama, T., and Hanada, K. (1995) Epiregulin. A novel epidermal growth factor with mitogenic activity for rat primary hepatocytes. J. Biol. Chem. 270, 7495-7500
10. Strachan, L., Murison, J. G., Prestidge, R. L., Sleeman, M. A., Watson, J. D., and Kumble, K. D. (2001) Cloning and biological activity of epigen, a novel member of the epidermal growth factor superfamily. J. Biol. Chem. 276, 18265-18271
11. Harris, R. C., Chung, E., and Coffey, R. J. (2003) EGF receptor ligands. Exp. Cell Res. 284, 2-13 (Pubitemid 36331964)
12. Prenzel, N., Zwick, E., Daub, H., Leserer, M., Abraham, R., Wallasch, C., and Ullrich, A. (1999) EGF receptor transactivation by G-protein-coupled receptors requires metalloproteinase cleavage of proHB-EGF. Nature 402, 884-888
13. Peschon, J. J., Slack, J. L., Reddy, P., Stocking, K. L., Sunnarborg, S. W., Lee, D. C., Russell, W. E., Castner, B. J., Johnson, R. S., Fitzner, J. N., Boyce, R. W., Nelson, N., Kozlosky, C. J., Wolfson, M. F., Rauch, C. T., Cerretti, D. P., Paxton, R. J., March, C. J., and Black, R. A. (1998) An essential role for ectodomain shedding in mammalian development. Science 282, 1281-1284 (Pubitemid 28524483)
14. Merlos-Suárez, A., Ruiz-Paz, S., Baselga, J., and Arribas, J. (2001) Metalloprotease-dependent protransforming growth factor-α ectodomain shedding in the absence of tumor necrosis factor-α-converting enzyme. J. Biol. Chem. 276, 48510-48517
15. Sunnarborg, S. W., Hinkle, C. L., Stevenson, M., Russell, W. E., Raska, C. S., Peschon, J. J., Castner, B. J., Gerhart, M. J., Paxton, R. J., Black, R. A., and Lee, D. C. (2002) Tumor necrosis factor-α converting enzyme (TACE) regulates epidermal growth factor receptor ligand availability. J. Biol. Chem. 277, 12838-12845 (Pubitemid 34952648)
16. Sahin, U., Weskamp, G., Kelly, K., Zhou, H. M., Higashiyama, S., Peschon, J., Hartmann, D., Saftig, P., and Blobel, C. P. (2004) Distinct roles for ADAM10 and ADAM17 in ectodomain shedding of six EGFR ligands. J. Cell Biol. 164, 769-779 (Pubitemid 38282960)
17. Sahin, U., and Blobel, C. P. (2007) Ectodomain shedding of the EGF-receptor ligand epigen is mediated by ADAM17. FEBS Lett. 581, 41-44 (Pubitemid 46001649)
18. Horiuchi, K., Le Gall, S., Schulte, M., Yamaguchi, T., Reiss, K., Murphy, G., Toyama, Y., Hartmann, D., Saftig, P., and Blobel, C. P. (2007) Substrate selectivity of epidermal growth factor-receptor ligand sheddases and their regulation by phorbol esters and calcium influx. Mol. Biol. Cell 18, 176-188 (Pubitemid 46066719)
19. Edwards, D. R., Handsley, M. M., and Pennington, C. J. (2008) TheADAM metalloproteinases. Mol. Aspects Med. 29, 258-289
20. Mochizuki, S., and Okada, Y. (2007) ADAMs in cancer cell proliferation and progression. Cancer Sci. 98, 621-628 (Pubitemid 46563436)
21. Tousseyn, T., Jorissen, E., Reiss, K., and Hartmann, D. (2006) (Make) stick and cut loose-disintegrin metalloproteases in development and disease. Birth Defects Res. C. Embryo Today 78, 24-46 (Pubitemid 43726174)
22. Bergin, D. A., Greene, C. M., Sterchi, E. E., Kenna, C., Geraghty, P., Belaaouaj, A., Taggart, C. C., O'Neill, S. J., and McElvaney, N. G. (2008) Activation of the epidermal growth factor receptor (EGFR) by a novel metalloprotease pathway. J. Biol. Chem. 283, 31736-31744
23. Barrett, A. J., Rawlings, N. D., and O'Brien, E. A. (2001) The MEROPS database as a protease information system. J. Struct. Biol. 134, 95-102
24. Beynon, R. J., Shannon, J. D., and Bond, J. S. (1981) Purification and characterization of a metallo-endoproteinase from mouse kidney. Biochem. J. 199, 591-598
25. Sterchi, E. E., Green, J. R., and Lentze, M. J. (1982) Non-pancreatic hydrolysis of N-benzoyl-L-tyrosyl-p-aminobenzoic acid (PABA-peptide) in the human small intestine. Clin. Sci. 62, 557-560 (Pubitemid 12127238)
26. Kenny, A. J., and Ingram, J. (1987) Proteins of the kidney microvillar membrane. Purification and properties of the phosphoramidon-insensitive endopeptidase ('endopeptidase-2') from rat kidney. Biochem. J. 245, 515-524
27. Bode, W., Gomis-Rüth, F. X., Huber, R., Zwilling, R., and Stöcker, W. (1992) Structure of astacin and implications for activation of astacins and zinc-ligation of collagenases. Nature 358, 164-167
28. Grünberg, J., Dumermuth, E., Eldering, J. A., and Sterchi, E. E. (1993) Expression of the alpha subunit of PABA peptide hydrolase (EC 3.4.24.18) in MDCK cells. Synthesis and secretion of an enzymatically inactive homodimer. FEBS Lett. 335, 376-379 (Pubitemid 23355965)
29. Dumermuth, E., Eldering, J. A., Grünberg, J., Jiang, W., and Sterchi, E. E. (1993) Cloning of the PABA peptide hydrolase α subunit (PPH α) from human small intestine and its expression in COS-1 cells. FEBS Lett. 335, 367-375 (Pubitemid 23355964)
30. Sterchi, E. E., Naim, H. Y., Lentze, M. J., Hauri, H. P., and Fransen, J. A. (1988) N-benzoyl-L-tyrosyl-p-aminobenzoic acid hydrolase: a metalloendopeptidase of the human intestinal microvillus membrane which degrades biologically active peptides. Arch. Biochem. Biophys. 265, 105-118
31. Marchand, P., Tang, J., and Bond, J. S. (1994) Membrane association and oligomeric organization of the α and β subunits of mouse meprin A. J. Biol. Chem. 269, 15388-15393 (Pubitemid 24198393)
32. Ishmael, F. T., Norcum, M. T., Benkovic, S. J., and Bond, J. S. (2001) Multimeric structure of the secreted meprin A metalloproteinase and characterization of the functional protomer. J. Biol. Chem. 276, 23207-23211
33. Eldering, J. A., Grünberg, J., Hahn, D., Croes, H. J., Fransen, J. A., and Sterchi, E. E. (1997) Polarized expression of human intestinal N-benzoyl-L-tyrosyl-p-aminobenzoic acid hydrolase (human meprin) α and β subunits in Madin-Darby canine kidney cells. Eur. J. Biochem. 247, 920-932 (Pubitemid 27337047)
34. Lottaz, D., Hahn, D., Müller, S., Müller, C., and Sterchi, E. E. (1999) Secretion of human meprin from intestinal epithelial cells depends on differential expression of the α and β subunits. Eur. J. Biochem. 259, 496-504 (Pubitemid 29030875)
35. Lottaz, D., Maurer, C. A., Hahn, D., Büchler, M. W., and Sterchi, E. E. (1999) Nonpolarized secretion of human meprin α in colorectal cancer generates an increased proteolytic potential in the stroma. Cancer Res. 59, 1127-1133 (Pubitemid 29135976)
36. Rösmann, S., Hahn, D., Lottaz, D., Kruse, M. N., Stöcker, W., and Sterchi, E. E. (2002) Activation of human meprin-α in a cell culture model of colorectal cancer is triggered by the plasminogen-activating system. J. Biol. Chem. 277, 40650-40658 (Pubitemid 35215646)
37. Lottaz, D., Maurer, C. A., Noel, A., Blacher, S., Huguenin, M., Nievergelt, A., Niggli, V., Kern, A., Muller, S., Seibold, F., Friess, H., Becker-Pauly, C., Stocker, W., and Sterchi, E. E. (2011) Enhanced activity of meprin-alpha, a pro-migratory and pro-angiogenic protease, in colorectal cancer. PLoS ONE 6, e26450
38. Schutte, A., Hedrich, J., Stocker, W., and Becker-Pauly, C. (2010) Let it flow: Morpholino knockdown in zebrafish embryos reveals a pro-angiogenic effect of the metalloprotease meprin alpha2. PLoS ONE 5, e8835
39. Becker, C., Kruse, M. N., Slotty, K. A., Köhler, D., Harris, J. R., Rösmann, S., Sterchi, E. E., and Stöcker, W. (2003) Differences in the activation mechanism between the α and β subunits of human meprin. Biol. Chem. 384, 825-831 (Pubitemid 36747944)
40. Becker-Pauly, C., Höwel, M., Walker, T., Vlad, A., Aufenvenne, K., Oji, V., Lottaz, D., Sterchi, E. E., Debela, M., Magdolen, V., Traupe, H., and Stöcker, W. (2007) The α and β subunits of the metalloprotease meprin are expressed in separate layers of human epidermis, revealing different functions in keratinocyte proliferation and differentiation. J. Invest Dermatol. 127, 1115-1125 (Pubitemid 46625146)
41. Tokumaru, S., Higashiyama, S., Endo, T., Nakagawa, T., Miyagawa, J. I., Yamamori, K., Hanakawa, Y., Ohmoto, H., Yoshino, K., Shirakata, Y., Matsuzawa, Y., Hashimoto, K., and Taniguchi, N. (2000) Ectodomain shedding of epidermal growth factor receptor ligands is required for keratinocyte migration in cutaneous wound healing. J. Cell Biol. 151, 209-220
42. Ahmed, S. A., Gogal, R. M., Jr., and Walsh, J. E. (1994) A new rapid and simple non-radioactive assay to monitor and determine the proliferation of lymphocytes: an alternative to [3H]thymidine incorporation assay. J. Immunol. Methods 170, 211-224 (Pubitemid 24122510)
43. Anoopkumar-Dukie, S., Carey, J. B., Conere, T., O'Sullivan, E., van Pelt, F. N., and Allshire, A. (2005) Resazurin assay of radiation response in cultured cells. Br. J. Radiol 78, 945-947 (Pubitemid 41582247)
44. Crouch, S. P., Kozlowski, R., Slater, K. J., and Fletcher, J. (1993) The use of ATP bioluminescence as a measure of cell proliferation and cytotoxicity. J. Immunol. Methods 160, 81-88
45. Wells, A. (1999) EGF receptor. Int. J. Biochem. Cell Biol. 31, 637-643
46. Ohler, A., Debela, M., Wagner, S., Magdolen, V., and Becker-Pauly, C. (2010) Analyzing the protease web in skin: meprin metalloproteases are activated specifically by KLK4, 5 and 8 vice versa leading to processing of proKLK7 thereby triggering its activation. Biol. Chem. 391, 455-460
47. Roux, P. P., and Blenis, J. (2004) ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions. Microbiol Mol. Biol. Rev. 68, 320-344 (Pubitemid 38756868)
48. Choudry, Y., and Kenny, A. J. (1991) Hydrolysis of transforming growth factor-α by cell-surface peptidases in vitro. Biochem. J. 280, 57-60
49. Huguenin, M., Müller, E. J., Trachsel-Rösmann, S., Oneda, B., Ambort, D., Sterchi, E. E., and Lottaz, D. (2008) The metalloprotease meprinbeta processes E-cadherin and weakens intercellular adhesion. PLoS ONE 3, e2153
50. Bertenshaw, G. P., Turk, B. E., Hubbard, S. J., Matters, G. L., Bylander, J. E., Crisman, J. M., Cantley, L. C., and Bond, J. S. (2001) Marked differences between metalloproteases meprin A and B in substrate and peptide bond specificity. J. Biol. Chem. 276, 13248-13255
51. Becker-Pauly, C., Barre, O., Schilling, O., Auf dem Keller, U., Ohler, A., Broder, C., Schutte, A., Kappelhoff, R., Stocker, W., and Overall, C. M. (2011) Proteomic analyses reveal an acidic prime side specificity for the astacin metalloprotease family reflected by physiological substrates. Mol. Cell Proteomics 10, M111 009233
52. Hedrich, J., Lottaz, D., Meyer, K., Yiallouros, I., Jahnen-Dechent, W., Stöcker, W., and Becker-Pauly, C. (2010) Fetuin-A and cystatin C are endogenous inhibitors of human meprin metalloproteases. Biochemistry 49, 8599-8607
53. Jackson, L. F., Qiu, T. H., Sunnarborg, S. W., Chang, A., Zhang, C., Patterson, C., and Lee, D. C. (2003) Defective valvulogenesis in HB-EGF and TACE-null mice is associated with aberrant BMP signaling. EMBO J. 22, 2704-2716 (Pubitemid 36712367)
54. Mann, G. B., Fowler, K. J., Gabriel, A., Nice, E. C., Williams, R. L., and Dunn, A. R. (1993) Mice with a null mutation of the TGF α gene have abnormal skin architecture, wavy hair, and curly whiskers and often develop corneal inflammation. Cell 73, 249-261 (Pubitemid 23123305)
55. Hartmann, D., de Strooper, B., Serneels, L., Craessaerts, K., Herreman, A., Annaert, W., Umans, L., Lübke, T., Lena Illert, A., von Figura, K., and Saftig, P. (2002) The disintegrin/metalloproteaseADAM10 is essential for Notch signaling but not for α-secretase activity in fibroblasts. Hum. Mol. Genet. 11, 2615-2624 (Pubitemid 35174691)
56. Half, E., Broaddus, R., Danenberg, K. D., Danenberg, P. V., Ayers, G. D., and Sinicrope, F. A. (2004) HER-2 receptor expression, localization, and activation in colorectal cancer cell lines and human tumors. Int. J. Cancer 108, 540-548 (Pubitemid 38036654)
57. Yasui, W., Sumiyoshi, H., Hata, J., Kameda, T., Ochiai, A., Ito, H., and Tahara, E. (1988) Expression of epidermal growth factor receptor in human gastric and colonic carcinomas. Cancer Res. 48, 137-141 (Pubitemid 18030342)
58. Ciardiello, F., Kim, N., Saeki, T., Dono, R., Persico, M. G., Plowman, G. D., Garrigues, J., Radke, S., Todaro, G. J., and Salomon, D. S. (1991) Differential expression of epidermal growth factor-related proteins in human colorectal tumors. Proc. Natl. Acad. Sci. U.S.A. 88, 7792-7796 (Pubitemid 21915240)
59. Tampellini, M., Longo, M., Cappia, S., Bacillo, E., Alabiso, I., Volante, M., Dogliotti, L., and Papotti, M. (2007) Co-expression of EGF receptor,TGFα and S6 kinase is significantly associated with colorectal carcinomas with distant metastases at diagnosis. Virchows Arch. 450, 321-328 (Pubitemid 46376567)
60. Citri, A., and Yarden, Y. (2006) EGF-ERBB signaling: towards the systems level. Nat. Rev. Mol. Cell Biol. 7, 505-516 (Pubitemid 44036456)
61. Yarden, Y., and Sliwkowski, M. X. (2001) Untangling the ErbB signalling network. Nat. Rev. Mol. Cell Biol. 2, 127-137 (Pubitemid 33674041)
62. Jefferson, T., Auf dem Keller, U., Bellac, C., Metz, V. V., Broder, C., Hedrich, J., Ohler, A., Maier, W., Magdolen, V., Sterchi, E., Bond, J. S., Jayakumar, A., Traupe, H., Chalaris, A., Rose-John, S., Pietrzik, C. U., Postina, R., Overall, C. M., and Becker-Pauly, C. (2012) The substrate degradome of meprin metalloproteases reveals an unexpected proteolytic link between meprin beta and ADAM10. Cell. Mol. Life Sciences, in press