ADAM10 is the major sheddase responsible for the release of membrane-Associated meprin A

Journal of Biological Chemistry

Volumn 289, Issue 19, 2014, Pages 13308-13322

  Herzog, Christian ^a,b   Haun, Randy S ^a   Ludwig, Andreas ^c   Shah, Sudhir V ^a,b   Kaushal, Gur P ^a,b  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^b UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^c RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; VOLATILE FATTY ACIDS;

ECTODOMAIN SHEDDING; PHORBOL 12 MYRISTATE 13 ACETATES; PROTEASE INHIBITOR; PROTEOLYTIC ENZYME; PROTEOLYTIC PROCESSING; SMALL INTERFERING RNA; THERAPEUTIC BENEFITS; TUMOR NECROSIS FACTORS;

ENZYME ACTIVITY;

ADAM10 ENDOPEPTIDASE; ILOMASTAT; IONOMYCIN; MEPRIN; PHORBOL ESTER; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR ALPHA INHIBITOR;

ACUTE KIDNEY FAILURE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME LOCALIZATION; ENZYME RELEASE; ENZYMURIA; KIDNEY PROXIMAL TUBULE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION;

ADAM ADAMTS; ADAM10; ADAM17; KIDNEY; MEPRIN; METALLOPROTEASE; MOUSE; SHEDDING; SIRNA;

ACUTE KIDNEY INJURY; ADAM PROTEINS; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; CALCIUM IONOPHORES; CARCINOGENS; CELL MEMBRANE; HEK293 CELLS; HUMANS; IONOMYCIN; MALE; MEMBRANE PROTEINS; METALLOENDOPEPTIDASES; MICE; TETRADECANOYLPHORBOL ACETATE;

EID: 84900462268     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.559088     Document Type: Article

References (71)

1. Sterchi, E. E., Stöcker, W., and Bond, J. S. (2008) Meprins, membranebound and secreted astacin metalloproteinases. Mol. Aspects Med. 29, 309-328
2. 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
3. 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
4. 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
5. Crisman, J. M., Zhang, B., Norman, L. P., and Bond, J. S. (2004) Deletion of the mouse meprin β metalloprotease gene diminishes the ability of leukocytes to disseminate through extracellular matrix. J. Immunol. 172, 4510-4519
6. Matters, G. L., Manni, A., and Bond, J. S. (2005) Inhibitors of polyamine biosynthesis decrease the expression of the metalloproteases meprin α and MMP-7 in hormone-independent human breast cancer cells. Clin. Exp. Metastasis 22, 331-339
7. Oneda, B., Lods, N., Lottaz, D., Becker-Pauly, C., Stöcker, W., Pippin, J., Huguenin, M., Ambort, D., Marti, H. P., and Sterchi, E. E. (2008) Metalloprotease meprin β in rat kidney: glomerular localization and differential expression in glomerulonephritis. PLoS One 3, e2278
8. Bertenshaw, G. P., Norcum, M. T., and Bond, J. S. (2003) Structure of homo- and hetero-oligomeric meprin metalloproteases: dimers, tetramers, and high molecular mass multimers. J. Biol. Chem. 278, 2522-2532
9. Sterchi, E. E. (2008) Special issue: metzincin metalloproteinases. Mol. Aspects Med. 29, 255-257
10. Kumar, J. M., and Bond, J. S. (2001) Developmental expression of meprin metalloprotease subunits in ICR and C3H/He mouse kidney and intestine in the embryo, postnatally and after weaning. Biochim. Biophys. Acta 1518, 106-114
11. Bond, J. S., Matters, G. L., Banerjee, S., and Dusheck, R. E. (2005) Meprin metalloprotease expression and regulation in kidney, intestine, urinary tract infections and cancer. FEBS Lett. 579, 3317-3322
12. Craig, S. S., Reckelhoff, J. F., and Bond, J. S. (1987) Distribution of meprin in kidneys from mice with high- and low-meprin activity. Am. J. Physiol. 253, C535-540
13. Bylander, J., Li, Q., Ramesh, G., Zhang, B., Reeves, W. B., and Bond, J. S. (2008) Targeted disruption of the meprin metalloproteinase β gene protects against renal ischemia-reperfusion injury in mice. Am. J. Physiol. Renal Physiol. 294, F480-490
14. Herzog, C., Seth, R., Shah, S. V., and Kaushal, G. P. (2007) Role of meprin A in renal tubular epithelial cell injury. Kidney Int. 71, 1009-1018
15. Wang, Z., Herzog, C., Kaushal, G. P., Gokden, N., and Mayeux, P. R. (2011) Actinonin, a meprin A inhibitor, protects the renal microcirculation during sepsis. Shock 35, 141-147
16. Walker, P. D., Kaushal, G. P., and Shah, S. V. (1998) Meprin A, the major matrix degrading enzyme in renal tubules, produces a novel nidogen fragment in vitro and in vivo. Kidney Int. 53, 1673-1680
17. Kaushal, G. P., Walker, P. D., and Shah, S. V. (1994) An old enzyme with a new function: purification and characterization of a distinct matrix-degrading metalloproteinase in rat kidney cortex and its identification as meprin. J. Cell Biol. 126, 1319-1327
18. Köhler, D., Kruse, M., Stöcker, W., and Sterchi, E. E. (2000) Heterologously overexpressed, affinity purified human meprin α is functionally active and cleaves components of the basement membrane in vitro. FEBS Lett. 465, 2-7
19. Kruse, M. N., Becker, C., Lottaz, D., Köhler, D., Yiallouros, I., Krell, H. W., Sterchi, E. E., and Stöcker, W. (2004) Human meprin α and β homooligomers: cleavage of basement membrane proteins and sensitivity to metalloprotease inhibitors. Biochem. J. 378, 383-389
20. Herzog, C., Haun, R. S., Kaushal, V., Mayeux, P. R., Shah, S. V., and Kaushal, G. P. (2009) Meprin A and meprin α generate biologically functional IL-1β from pro-IL-1β. Biochem. Biophys. Res. Commun. 379, 904-908
21. Herzog, C., Kaushal, G. P., and Haun, R. S. (2005) Generation of biologically active interleukin-1 β by meprin B. Cytokine 31, 394-403
22. 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
23. 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
24. Ludwig, A., Hundhausen, C., Lambert, M. H., Broadway, N., Andrews, R. C., Bickett, D. M., Leesnitzer, M. A., and Becherer, J. D. (2005) Metalloproteinase inhibitors for the disintegrin-like metalloproteinases ADAM10 and ADAM17 that differentially block constitutive and phorbol ester-inducible shedding of cell surface molecules. Comb. Chem. High Throughput Screen. 8, 161-171
25. Seth, R., Yang, C., Kaushal, V., Shah, S. V., Kaushal, G. P. (2005) p53-dependent caspase-2 activation in mitochondrial release of apoptosis-inducing factor and its role in renal tubular epithelial cell injury. J. Biol. Chem. 280, 31230-31239
26. Bergin, E., Levine, J. S., Koh, J. S., and Lieberthal, W. (2000) Mouse proximal tubular cell-cell adhesion inhibits apoptosis by a cadherin-dependent mechanism. Am. J. Physiol. Renal Physiol. 278, F758-F768
27. Kaushal, G. P., Haun, R. S., Herzog, C., Shah, S. V. (2013) Meprin A metalloproteinase and its role in acute kidney injury. Am. J. Physiol. Renal Physiol. 304, F1150-F1158
28. Endres, K., Anders, A., Kojro, E., Gilbert, S., Fahrenholz, F., and Postina, R. (2003) Tumor necrosis factor-α converting enzyme is processed by proproteinconvertases to its mature form which is degraded upon phorbol ester stimulation. Eur. J. Biochem. 270, 2386-2393
29. Gasbarri, A., Del Prete, F., Girnita, L., Martegani, M. P., Natali, P. G., and Bartolazzi, A. (2003) CD44s adhesive function spontaneous and PMAinducible CD44 cleavage are regulated at post-translational level in cells of melanocytic lineage. Melanoma Res. 13, 325-337
30. Fitzgerald, M. L., Wang, Z., Park, P. W., Murphy, G., and Bernfield, M. (2000) Shedding of syndecan-1 and -4 ectodomains is regulated by multiple signaling pathways and mediated by a TIMP-3-sensitive metalloproteinase. J. Cell Biol. 148, 811-824
31. Garton, K. J., Gough, P. J., and Raines, E. W. (2006) Emerging roles for ectodomain shedding in the regulation of inflammatory responses. J. Leukoc. Biol. 79, 1105-1116
32. Huovila, A. P., Turner, A. J., Pelto-Huikko, M., Kärkkäinen, I., and Ortiz, R. M. (2005) Shedding light on ADAM metalloproteinases. Trends Biochem. Sci. 30, 413-422
33. Deuss, M., Reiss, K., and Hartmann, D. (2008) Part-time α-secretases: the functional biology of ADAM 9, 10 and 17. Curr. Alzheimer. Res. 5, 187-201
34. Saftig, P., and Reiss, K. (2011) The "A Disintegrin And Metalloproteases" ADAM10 and ADAM17: novel drug targets with therapeutic potential? Eur. J. Cell Biol. 90, 527-535
35. Hundhausen, C., Misztela, D., Berkhout, T. A., Broadway, N., Saftig, P., Reiss, K., Hartmann, D., Fahrenholz, F., Postina, R., Matthews, V., Kallen, K. J., Rose-John, S., and Ludwig, A. (2003) The disintegrin-like metalloproteinase ADAM10 is involved in constitutive cleavage of CX3CL1 (fractalkine) and regulates CX3CL1-mediated cell-cell adhesion. Blood 102, 1186-1195
36. Scholz, F., Schulte, A., Adamski, F., Hundhausen, C., Mittag, J., Schwarz, A., Kruse, M. L., Proksch, E., and Ludwig, A. (2007) Constitutive expression and regulated release of the transmembrane chemokine CXCL16 in human and murine skin. J. Invest. Dermatol. 127, 1444-1455
37. Moss, M. L., Rasmussen, F. H., Nudelman, R., Dempsey, P. J., and Williams, J. (2010) Fluorescent substrates useful as high-throughput screening tools for ADAM9. Comb Chem High Throughput Screen 13, 358-365
38. Thadhani, R., Pascual, M., and Bonventre, J. V. (1996) Acute renal failure. N. Engl. J. Med. 334, 1448-1460
39. Yamaguchi, T., Fukase, M., Sugimoto, T., Kido, H., and Chihara, K. (1994) Purification of meprin from human kidney and its role in parathyroid hormone degradation. Biol. Chem. Hoppe Seyler. 375, 821-824
40. Bao, J., Yura, R. E., Matters, G. L., Bradley, S. G., Shi, P., Tian, F., and Bond, J. S. (2013) Meprin A impairs epithelial barrier function, enhances monocyte migration, and cleaves the tight junction protein occludin. Am. J. Physiol. Renal Physiol. 305, F714-F726
41. Banerjee, S., and Bond, J. S. (2008) Prointerleukin-18 is activated by meprin β in vitro and in vivo in intestinal inflammation. J. Biol. Chem. 283, 31371-31377
42. Kronenberg, D., Bruns, B. C., Moali, C., Vadon-Le Goff, S., Sterchi, E. E., Traupe, H., Böhm, M., Hulmes, D. J., Stöcker, W., and Becker-Pauly, C. (2010) Processing of procollagen III by meprins: new players in extracellular matrix assembly? J. Invest. Dermatol. 130, 2727-2735
43. Jefferson, T., Çauševič, M., Auf Dem Keller, U., Schilling, O., Isbert, S., Geyer, R., Maier, W., Tschickardt, S., Jumpertz, T., Weggen, S., Bond, J. S., Overall, C. M., Pietrzik, C. U., and Becker-Pauly, C. (2011) Metalloprotease meprin β generates nontoxic N-terminal amyloid precursor protein fragments in vivo. J. Biol. Chem. 286, 27741-27750
44. 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
45. Ambort, D., Brellier, F., Becker-Pauly, C., Stöcker, W., Andrejevic-Blant, S., Chiquet, M., and Sterchi, E. E. (2010) Specific processing of tenascin-C by the metalloprotease meprin β neutralizes its inhibition of cell spreading. Matrix Biol. 29, 31-42
46. Huguenin, M., Müller, E. J., Trachsel-Rösmann, S., Oneda, B., Ambort, D., Sterchi, E. E., and Lottaz, D. (2008) The metalloprotease meprin β processes E-cadherin and weakens intercellular adhesion. PLoS One 3, e2153
47. Garcia-Caballero, A., Ishmael, S. S., Dang, Y., Gillie, D., Bond, J. S., Milgram, S. L., and Stutts, M. J. (2011) (2010) Activation of the epithelial sodium channel by the metalloprotease meprin β subunit. Channels (Austin) 5, 14-22
48. Schütte A, Hedrich J, Stöcker W, Becker-Pauly C. (2010) Let it flow: morpholino knockdown in zebrafish embryos reveals a pro-Angiogenic effect of the metalloprotease meprin α2. PLoS One 5, e8835
49. Edwards, D. R., Handsley, M. M., and Pennington, C. J. (2008) TheADAM metalloproteinases. Mol. Aspects Med. 29, 258-289
50. Klein, T., and Bischoff, R. (2011) Active metalloproteases of the A Disintegrin and Metalloprotease (ADAM) family: biological function and structure. J. Proteome Res. 10, 17-33
51. Murphy, G. (2008) The ADAMs: signalling scissors in the tumour microenvironment. Nat. Rev. Cancer 8, 929-941
52. Pruessmeyer, J., and Ludwig, A. (2009) The good, the bad and the ugly substrates for ADAM10 and ADAM17 in brain pathology, inflammation and cancer. Semin. Cell Dev. Biol. 20, 164-174
53. Gibb, D. R., Saleem, S. J., Chaimowitz, N. S., Mathews, J., and Conrad, D. H. (2011) The emergence of ADAM10 as a regulator of lymphocyte development and autoimmunity. Mol. Immunol. 48, 1319-1327
54. Crawford, H. C., Dempsey, P. J., Brown, G., Adam, L., and Moss, M. L. (2009) ADAM10 as a therapeutic target for cancer and inflammation. Curr. Pharm. Des. 15, 2288-2299
55. Hahn, D., Pischitzis, A., Roesmann, S., Hansen, M. K., Leuenberger, B., Luginbuehl, U., and Sterchi, E. E. (2003) Phorbol 12-myristate 13-Acetateinduced ectodomain shedding and phosphorylation of the human meprinβ metalloprotease. J. Biol. Chem. 278, 42829-42839
56. Pischitzis, A., Hahn, D., Leuenberger, B., and Sterchi, E. E. (1999) N-Benzoyl-L-tyrosyl-p-Aminobenzoic acid hydrolase β (human meprin β): a 13-Amino-Acid sequence is required for proteolytic processing and subsequent secretion. Eur. J. Biochem. 261, 421-429
57. Le Gall, S. M., Bobé, P., Reiss, K., Horiuchi, K., Niu, X. D., Lundell, D., Gibb, D. R., Conrad, D., Saftig, P., and Blobel, C. P. (2009) ADAMs 10 and 17 represent differentially regulated components of a general shedding machinery for membrane proteins such as transforming growth factor α, L-selectin, and tumor necrosis factor α. Mol. Biol. Cell 20, 1785-1794
58. Blobel, C. P. (2005) ADAMs: key components in EGFR signalling and development. Nat. Rev. Mol. Cell Biol. 6, 32-43
59. Lichtenthaler, S. F. (2011) α-Secretase in Alzheimer's disease: molecular identity, regulation and therapeutic potential. J. Neurochem. 116, 10-21
60. Kuhn, P. H., Wang, H., Dislich, B., Colombo, A., Zeitschel, U., Ellwart, J. W., Kremmer, E., Rossner, S., and Lichtenthaler, S. F. (2010) ADAM10 is the physiologically relevant, constitutive α-secretase of the amyloid precursor protein in primary neurons. EMBO J. 29, 3020-3032
61. Jorissen, E., Prox, J., Bernreuther, C., Weber, S., Schwanbeck, R., Serneels, L., Snellinx, A., Craessaerts, K., Thathiah, A., Tesseur, I., Bartsch, U., Weskamp, G., Blobel, C. P., Glatzel, M., De Strooper, B., and Saftig, P. (2010) The disintegrin/metalloproteinase ADAM10 is essential for the establishment of the brain cortex. J. Neurosci. 30, 4833-4844
62. Weber, S., Niessen, M. T., Prox, J., Lüllmann-Rauch, R., Schmitz, A., Schwanbeck, R., Blobel, C. P., Jorissen, E., De Strooper, B., Niessen, C. M., and Saftig, P. (2011) The disintegrin/metalloproteinase Adam10 is essential for epidermal integrity and Notch-mediated signaling. Development 138, 495-505
63. Matthews, V., Schuster, B., Schütze, S., Bussmeyer, I., Ludwig, A., Hundhausen, C., Sadowski, T., Saftig, P., Hartmann, D., Kallen, K. J., and Rose-John, S. (2003) Cellular cholesterol depletion triggers shedding of the human interleukin-6 receptor by ADAM10 and ADAM17 (TACE). J. Biol. Chem. 278, 38829-38839
64. Kim, J., Lilliehook, C., Dudak, A., Prox, J., Saftig, P., Federoff, H. J., and Lim, S. T. (2010) Activity-dependent α-cleavage of nectin-1 is mediated by a disintegrin and metalloprotease 10 (ADAM10). J. Biol. Chem. 285, 22919-22926
65. Cong, R., Li, Y., and Biemesderfer, D. (2011) A disintegrin and metalloprotease 10 activity sheds the ectodomain of the amyloid precursor-like protein 2 and regulates protein expression in proximal tubule cells. Am. J. Physiol. Cell Physiol. 300, C1366-1374
66. Schramme, A., Abdel-Bakky, M. S., Gutwein, P., Obermüller, N., Baer, P. C., Hauser, I. A., Ludwig, A., Gauer, S., Schäfer, L., Sobkowiak, E., Altevogt, P., Koziolek, M., Kiss, E., Gröne, H. J., Tikkanen, R., Goren, I., Radeke, H., and Pfeilschifter, J. (2008) Characterization of CXCL16 and ADAM10 in the normal and transplanted kidney. Kidney Int. 74, 328-338
67. Carmago, S., Shah, S. V., and Walker, P. D. (2002) Meprin, a brush-border enzyme, plays an important role in hypoxic/ischemic acute renal tubular injury in rats. Kidney Int. 61, 959-966
68. Yura, R. E., Bradley, S. G., Ramesh, G., Reeves, W. B., and Bond, J. S. (2009) Meprin A metalloproteases enhance renal damage and bladder inflammation after LPS challenge. Am. J. Physiol. Renal Physiol. 296, F135-144
69. Takayama, J., Takaoka, M., Yamamoto, S., Nohara, A., Ohkita, M., and Matsumura, Y. (2008) Actinonin, a meprin inhibitor, protects ischemic acute kidney injury in male but not in female rats. Eur. J. Pharmacol. 581, 157-163
70. Trachtman, H., Valderrama, E., Dietrich, J. M., and Bond, J. S. (1995) The role of meprin A in the pathogenesis of acute renal failure. Biochem. Biophys. Res. Commun. 208, 498-505
71. 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. (2013) The substrate degradadome of meprin metalloproteases reveals an unexpected proteolytic link between meprin β and ADAM10. Cell. Mol. Life Sci. 70, 309-333