Time-resolved analysis of the matrix metalloproteinase 10 substrate degradome

Molecular and Cellular Proteomics

Volumn 13, Issue 2, 2014, Pages 580-593

  Schlage, Pascal ^a   Egli, Fabian E ^a   Nanni, Paolo ^a   Wang, Lauren W ^b   Kizhakkedathu, Jayachandran N ^c   Apte, Suneel S ^a   Keller, Ulrich Auf Dem ^a  

^a ETH ZURICH   (Switzerland)

^b LERNER RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADAMTS LIKE PROTEIN 1; AMINE; COLLAGEN TYPE 1; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; PROTEIN; STROMELYSIN 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BIOMICS; CONTROLLED STUDY; ENZYME ANALYSIS; ENZYME DEGRADATION; ENZYME SPECIFICITY; FIBROBLAST; ISOTOPE LABELING; MOLECULAR LIBRARY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN PROCESSING; SUBSTRATE DEGRADOMICS; TIME RESOLVED ANALYSIS; WORKFLOW;

ANIMALS; BALB 3T3 CELLS; CATALYTIC DOMAIN; CELLS, CULTURED; EMBRYO, MAMMALIAN; ISOTOPE LABELING; MATRIX METALLOPROTEINASE 10; MICE; MICE, KNOCKOUT; MODELS, MOLECULAR; PEPTIDE FRAGMENTS; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEOLYSIS; PROTEOME; PROTEOMICS; SUBSTRATE SPECIFICITY; TIME FACTORS;

EID: 84893311362     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M113.035139     Document Type: Article

References (57)

1. Turk, B., Turk, D. S. A., and Turk, V. (2012) Protease signalling: the cutting edge. EMBO J. 31, 1630-1643
2. Khokha, R., Murthy, A., and Weiss, A. (2013) Metalloproteinases and their natural inhibitors in inflammation and immunity. Nat. Rev. Immunol. 13, 649-665
3. auf dem Keller, U., Doucet, A., and Overall, C. M. (2007) Protease research in the era of systems biology. Biol. Chem. 388, 1159-1162
4. Overall, C. M., and Kleifeld, O. (2006) Tumour microenvironment - opinion: validating matrix metalloproteinases as drug targets and anti-targets for cancer therapy. Nat. Rev. Cancer. 6, 227-239
5. Rogers, L., and Overall, C. M. (2013) Proteolytic post translational modification ofproteins: proteomic tools and methodology. Mol. Cell. Proteomics. 10.1074/mcp.M1113.031310
6. Plasman, K., Van Damme, P., and Gevaert, K. (2013) Contemporary positional proteomics strategies to study protein processing. Curr. Opin. Chem. Biol. 17, 66-72
7. Impens, F., Colaert, N., Helsens, K., Plasman, K., Van Damme, P., Vandekerckhove, J., and Gevaert, K. (2010) Mass spectrometry-driven protease substrate degradomics. Proteomics 10, 1284-1296
8. auf dem Keller, U., Prudova, A., Eckhard, U., Fingleton, B., and Overall, C. M. (2013) Systems-level analysis of proteolytic events in increased vascular permeability and complement activation in skin inflammation. Sci. Signal. 6, rs2
9. Tholen, S., Biniossek, M. L., Gansz, M., Gomez-Auli, A., Bengsch, F., Noel, A., Kizhakkedathu, J. N., Boerries, M., Busch, H., Reinheckel, T., and Schilling, O. (2013) Deletion of cysteine cathepsins B or L yields differential impacts on murine skin proteome and degradome. Mol. Cell. Proteomics. 12, 611-625
10. Van Damme, P., Staes, A., Bronsoms, S., Helsens, K., Colaert, N., Timmerman, E., Aviles, F. X., Vandekerckhove, J., and Gevaert, K. (2010) Complementary positional proteomics for screening substrates of endo- and exoproteases. Nat. Methods. 7, 512-515
11. Schilling, O., Barré, O., Huesgen, P. F., and Overall, C. M. (2010) Proteomewide analysis of protein carboxy termini: C terminomics. Nat. Methods. 7, 508-511
12. Plasman, K., Van Damme, P., Kaiserman, D., Impens, F., Demeyer, K., Helsens, K., Goethals, M., Bird, P. I., Vandekerckhove, J., and Gevaert, K. (2011) Probing the efficiency of proteolytic events by positional proteomics. Mol. Cell. Proteomics. 10, 10.1074/mcp.M1110.003301
13. Agard, N. J., Mahrus, S., Trinidad, J. C., Lynn, A., Burlingame, A. L., and Wells, J. A. (2012) Global kinetic analysis of proteolysis via quantitative targeted proteomics. Proc. Natl. Acad. Sci. U.S.A. 109, 1913-1918
14. Shimbo, K., Hsu, G. W., Nguyen, H., Mahrus, S., Trinidad, J. C., Burlingame, A. L., and Wells, J. A. (2012) Quantitative profiling of caspasecleaved substrates reveals different drug-induced and cell-type patterns in apoptosis. Proc. Natl. Acad. Sci. U.S.A. 109, 12432-12437
15. Prudova, A., auf dem Keller, U., Butler, G. S., and Overall, C. M. (2010) Multiplex N-terminome analysis of MMP-2 and MMP-9 substrate degradomes by iTRAQ-TAILS quantitative proteomics. Mol. Cell. Proteomics. 9, 894-911
16. Krampert, M., Bloch, W., Sasaki, T., Bugnon, P., Rülicke, T., Wolf, E., Aumailley, M., Parks, W. C., and Werner, S. (2004) Activities of the matrix metalloproteinase stromelysin-2 (MMP-10) in matrix degradation and keratinocyte organization in wounded skin. Mol. Biol. Cell. 15, 5242- 5254
17. Madlener, M., Mauch, C., Conca, W., Brauchle, M., Parks, W. C., and Werner, S. (1996) Regulation of the expression of stromelysin-2 by growth factors in keratinocytes: implications for normal and impaired wound healing. Biochem. J. 320 (Pt 2), 659-664
18. Muller, D., Breathnach, R., Engelmann, A., Millon, R., Bronner, G., Flesch, H., Dumont, P., Eber, M., and Abecassis, J. (1991) Expression of collagenase- related metalloproteinase genes in human lung or head and neck tumours. Int. J. Cancer. 48, 550-556
19. Todaro, G. J., and Green, H. (1963) Quantitative studies of the growth of mouse embryo cells in culture and their development into established lines. J. Cell Biol. 17, 299-313
20. auf dem Keller, U., Prudova, A., Gioia, M., Butler, G. S., and Overall, C. M. (2010) A statistics-based platform for quantitative N-terminome analysis and identification of protease cleavage products. Mol. Cell. Proteomics. 9, 912-927
21. Kleifeld, O., Doucet, A., Prudova, A., auf dem Keller, U., Gioia, M., Kizhakkedathu, J. N., and Overall, C. M. (2011) Identifying and quantifying proteolytic events and the natural N terminome by terminal amine isotopic labeling of substrates. Nat. Protoc. 6, 1578-1611
22. Choe, L., D'Ascenzo, M., Relkin, N. R., Pappin, D., Ross, P., Williamson, B., Guertin, S., Pribil, P., and Lee, K. H. (2007) 8-plex quantitation of changes in cerebrospinal fluid protein expression in subjects undergoing intravenous immunoglobulin treatment for Alzheimer's disease. Proteomics. 7, 3651-3660
23. Deutsch, E. W., Mendoza, L., Shteynberg, D., Farrah, T., Lam, H., Tasman, N., Sun, Z., Nilsson, E., Pratt, B., Prazen, B., Eng, J. K., Martin, D. B., Nesvizhskii, A. I., and Aebersold, R. (2010) A guided tour of the Trans- Proteomic Pipeline. Proteomics 10, 1150-1159
24. Shadforth, I. P., Dunkley, T. P., Lilley, K. S., and Bessant, C. (2005) i-Tracker: for quantitative proteomics using iTRAQ. BMC Genomics 6, 145
25. Keller, U., and Overall, C. M. (2012) CLIPPER-An add-on to the Trans-Proteomic Pipeline for the automated analysis of TAILS N-terminomics data. Biol. Chem. 393, 1477-1483
26. Kumar, L., and M, E. F. (2007) Mfuzz: a software package for soft clustering of microarray data. Bioinformation 2, 5-7
27. Schwammle, V., and Jensen, O. N. (2010) A simple and fast method to determine the parameters for fuzzy c-means cluster analysis. Bioinformatics 26, 2841-2848
28. Sing, T., Sander, O., Beerenwinkel, N., and Lengauer, T. (2005) ROCR: visualizing classifier performance in R. Bioinformatics 21, 3940-3941
29. Schilling, O., auf dem Keller, U., and Overall, C. M. (2011) Factor Xa subsite mapping by proteome-derived peptide libraries improved using Web- PICS, a resource for proteomic identification of cleavage sites. Biol. Chem. 392, 1031-1037
30. Colaert, N., Helsens, K., Martens, L., Vandekerckhove, J., and Gevaert, K. (2009) Improved visualization of protein consensus sequences by ice- Logo. Nat. Methods 6, 786-787
31. Montgomerie, S., Cruz, J. A., Shrivastava, S., Arndt, D., Berjanskii, M., and Wishart, D. S. (2008) PROTEUS2: a web server for comprehensive protein structure prediction and structure-based annotation. Nucleic Acids Res. 36, W202-209
32. Crooks, G. E., Hon, G., Chandonia, J. M., and Brenner, S. E. (2004) WebLogo: a sequence logo generator. Genome Res. 14, 1188-1190
33. Kitano, H., Funahashi, A., Matsuoka, Y., and Oda, K. (2005) Using process diagrams for the graphical representation of biological networks. Nat. Biotechnol. 23, 961-966
34. Funahashi, A., Morohashi, M., Kitano, H., and Tanimura, N. (2003) CellDesigner: a process diagram editor for gene-regulatory and biochemical networks. BIOSILICO 1, 159-162
35. Hirohata, S., Wang, L. W., Miyagi, M., Yan, L., Seldin, M. F., Keene, D. R., Crabb, J. W., and Apte, S. S. (2002) Punctin, a novel ADAMTS-like molecule, ADAMTSL-1, in extracellular matrix. J. Biol. Chem. 277, 12182-12189
36. Vizcaino, J. A., Cote, R. G., Csordas, A., Dianes, J. A., Fabregat, A., Foster, J. M., Griss, J., Alpi, E., Birim, M., Contell, J., O'Kelly, G., Schoenegger, A., Ovelleiro, D., Perez-Riverol, Y., Reisinger, F., Rios, D., Wang, R., and Hermjakob, H. (2013) The PRoteomics IDEntifications (PRIDE) database and associated tools: status in 2013. Nucleic Acids Res. 41, D1063-D1069
37. Schilling, O., and Overall, C. M. (2008) Proteome-derived, databasesearchable peptide libraries for identifying protease cleavage sites. Nat. Biotechnol. 26, 685-694
38. Houmard, J., and Drapeau, G. R. (1972) Staphylococcal protease: a proteolytic enzyme specific for glutamoyl bonds. Proc. Natl. Acad. Sci. U.S.A. 69, 3506-3509
39. Olsen, J. V., Blagoev, B., Gnad, F., Macek, B., Kumar, C., Mortensen, P., and Mann, M. (2006) Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127, 635-648
40. Kim, H. S., Shang, T., Chen, Z., Pflugfelder, S. C., and Li, D. Q. (2004) TGF-beta1 stimulates production of gelatinase (MMP-9), collagenases (MMP-1, -13) and stromelysins (MMP-3,-10,-11) by human corneal epithelial cells. Exp. Eye Res. 79, 263-274
41. Li, D. Q., Shang, T. Y., Kim, H. S., Solomon, A., Lokeshwar, B. L., and Pflugfelder, S. C. (2003) Regulated expression of collagenases MMP-1,-8, and-13 and stromelysins MMP-3,-10, and-11 by human corneal epithelial cells. Invest. Ophthalmol. Vis. Sci. 44, 2928-2936
42. Kleifeld, O., Doucet, A., auf dem Keller, U., Prudova, A., Schilling, O., Kainthan, R. K., Starr, A. E., Foster, L. J., Kizhakkedathu, J. N., and Overall, C. M. (2010) Isotopic labeling of terminal amines in complex samples identifies protein N-termini and protease cleavage products. Nat. Biotechnol. 28, 281-288
43. Aimes, R. T., and Quigley, J. P. (1995) Matrix metalloproteinase-2 is an interstitial collagenase. Inhibitor-free enzyme catalyzes the cleavage of collagen fibrils and soluble native type I collagen generating the specific 3/4- and 1/4-length fragments. J. Biol. Chem. 270, 5872-5876
44. Nicholson, R., Murphy, G., and Breathnach, R. (1989) Human and rat malignant-tumor-associated mRNAs encode stromelysin-like metalloproteinases. Biochemistry 28, 5195-5203
45. Park, J. W., Park, J. E., Park, J. K., and Lee, J. S. (2011) Purification and biochemical characterization of a novel glutamyl endopeptidase secreted by a clinical isolate of Staphylococcus aureus. Int. J. Mol. Med. 27, 637-645
46. Wehofsky, N., Wissmann, J., Alisch, M., and Bordusa, F. (2000) Engineering of substrate mimetics as novel-type substrates for glutamic acid-specific endopeptidases: design, synthesis, and application. Biochim. Biophys. Acta 1479, 114-122
47. Timmer, J. C., Zhu, W., Pop, C., Regan, T., Snipas, S. J., Eroshkin, A. M., Riedl, S. J., and Salvesen, G. S. (2009) Structural and kinetic determinants of protease substrates. Nat. Struct. Mol. Biol. 16, 1101-1108
48. Salsas-Escat, R., Nerenberg, P. S., and Stultz, C. M. (2010) Cleavage site specificity and conformational selection in type I collagen degradation. Biochemistry 49, 4147-4158
49. van Kempen, L. C. L., Rhee, J.-S., Dehne, K., Lee, J., Edwards, D. R., and Coussens, L. M. (2002) Epithelial carcinogenesis: dynamic interplay between neoplastic cells and their microenvironment. Differentiation 70, 610-623
50. P, O. C., Rhys-Evans, P. H., and Eccles, S. A. (2001) Expression of matrix metalloproteinases and their inhibitors correlates with invasion and metastasis in squamous cell carcinoma of the head and neck. Arch. Otolaryngol. Head Neck Surg. 127, 813-820
51. Patterson, M. L., Atkinson, S. J., Knauper, V., and Murphy, G. (2001) Specific collagenolysis by gelatinase A, MMP-2, is determined by the hemopexin domain and not the fibronectin-like domain. FEBS Lett. 503, 158-162
52. Barksby, H. E., Milner, J. M., Patterson, A. M., Peake, N. J., Hui, W., Robson, T., Lakey, R., Middleton, J., Cawston, T. E., Richards, C. D., and Rowan, A. D. (2006) Matrix metalloproteinase 10 promotion of collagenolysis via procollagenase activation: implications for cartilage degradation in arthritis. Arthritis Rheum. 54, 3244-3253
53. Nakamura, H., Fujii, Y., Ohuchi, E., Yamamoto, E., and Okada, Y. (1998) Activation of the precursor of human stromelysin 2 and its interactions with other matrix metalloproteinases. Eur. J. Biochem. 253, 67-75
54. Mendelson, K., Swendeman, S., Saftig, P., and Blobel, C. P. (2010) Stimulation of platelet-derived growth factor receptor beta (PDGFRbeta) activates ADAM17 and promotes metalloproteinase-dependent cross-talk between the PDGFRbeta and epidermal growth factor receptor (EGFR) signaling pathways. J. Biol. Chem. 285, 25024-25032
55. 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 degradome of meprin metalloproteases reveals an unexpected proteolytic link between meprin beta and ADAM10. Cell. Mol. Life Sci. 70, 309-333
56. Donovan, J., Shiwen, X., Norman, J., and Abraham, D. (2013) Plateletderived growth factor alpha and beta receptors have overlapping functional activities towards fibroblasts. Fibrogenesis Tissue Repair 6, 10
57. Seetharaman, A., Selman, G., Puckrin, R., Barbier, L., Wong, E., D'Souza, S. A., and Roy, P. J. (2011) MADD-4 is a secreted cue required for midline-oriented guidance in Caenorhabditis elegans. Dev. Cell 21, 669-680