Mapping proteolytic processing in the secretome of gastric cancer-associated myofibroblasts reveals activation of MMP-1, MMP-2, and MMP-3

Journal of Proteome Research

Volumn 12, Issue 7, 2013, Pages 3413-3422

  Holmberg, Christopher ^a   Ghesquière, Bart ^b,c   Impens, Francis ^b,c   Gevaert, Kris ^b,c   Kumar, J Dinesh ^a   Cash, Nicole ^a   Kandola, Sandhir ^a   Hegyi, Peter ^d   Wang, Timothy C ^e   Dockray, Graham J ^a   Varro, Andrea ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c GHENT UNIVERSITY   (Belgium)

^d UNIVERSITY OF SZEGED   (Hungary)

^e New York Presbyterian Morgan Stanley Children's Hospital   (United States)

Author keywords

COFRADIC; degradome; myofibroblast; neo N termini; secretome

Indexed keywords

GELATINASE A; INTERSTITIAL COLLAGENASE; METHIONINE DERIVATIVE; PEPTIDE DERIVATIVE; PROTEOME; SECRETOME; STROMELYSIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL; CANCER GROWTH; CELL MIGRATION; CHEMICAL LABELING; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ASSAY; ENZYME SYNTHESIS; HUMAN; HUMAN CELL; MOUSE; MYOFIBROBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN ISOLATION; PROTEIN MODIFICATION; PROTEIN PROCESSING; STOMACH CANCER; STROMA CELL; TUMOR MICROENVIRONMENT; WESTERN BLOTTING;

ANIMALS; CELL PROLIFERATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MATRIX METALLOPROTEINASE 1; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 3; MICE; MYOFIBROBLASTS; PROTEOLYSIS; STOMACH NEOPLASMS; TUMOR MICROENVIRONMENT; XENOGRAFT MODEL ANTITUMOR ASSAYS;

MUS;

EID: 84879937087     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr400270q     Document Type: Article

References (46)

1. Bissell, M. J.; Radisky, D. Putting tumours in context Nat. Rev. Cancer 2001, 1 (1) 46-54
2. Tlsty, T. D.; Coussens, L. M. Tumor stroma and regulation of cancer development Annu. Rev. Pathol. 2006, 1, 119-150
3. Hanahan, D.; Weinberg, R. A. Hallmarks of cancer: the next generation Cell 2011, 144 (5) 646-674
4. Faca, V. M.; Ventura, A. P.; Fitzgibbon, M. P.; Pereira-Faca, S. R.; Pitteri, S. J.; Green, A. E.; Ireton, R. C.; Zhang, Q.; Wang, H.; O'Briant, K. C.; Drescher, C. W.; Schummer, M.; McIntosh, M. W.; Knudsen, B. S.; Hanash, S. M. Proteomic analysis of ovarian cancer cells reveals dynamic processes of protein secretion and shedding of extra-cellular domains PLoS One 2008, 3 (6) e2425
5. Kulasingam, V.; Diamandis, E. P. Proteomics analysis of conditioned media from three breast cancer cell lines: a mine for biomarkers and therapeutic targets Mol. Cell. Proteomics 2007, 6 (11) 1997-2011
6. Lawlor, K.; Nazarian, A.; Lacomis, L.; Tempst, P.; Villanueva, J. Pathway-based biomarker search by high-throughput proteomics profiling of secretomes J. Proteome Res. 2009, 8 (3) 1489-1503
7. Marimuthu, A.; Subbannayya, Y.; Sahasrabuddhe, N. A.; Balakrishnan, L.; Syed, N.; Sekhar, N. R.; Katte, T. V.; Pinto, S. M.; Srikanth, S. M.; Kumar, P.; Pawar, H.; Kashyap, M. K.; Maharudraiah, J.; Ashktorab, H.; Smoot, D. T.; Ramaswamy, G.; Kumar, R. V.; Cheng, Y.; Meltzer, S. J.; Roa, J. C.; Chaerkady, R.; Prasad, T. S.; Harsha, H. C.; Chatterjee, A.; Pandey, A. SILAC-based quantitative proteomic analysis of gastric cancer secretome Proteomics: Clin. Appl. 2012, 10.1002/prca.201200069
8. Khwaja, F. W.; Svoboda, P.; Reed, M.; Pohl, J.; Pyrzynska, B.; Van Meir, E. G. Proteomic identification of the wt-p53-regulated tumor cell secretome Oncogene 2006, 25 (58) 7650-7661
9. Volmer, M. W.; Radacz, Y.; Hahn, S. A.; Klein-Scory, S.; Stuhler, K.; Zapatka, M.; Schmiegel, W.; Meyer, H. E.; Schwarte-Waldhoff, I. Tumor suppressor Smad4 mediates downregulation of the anti-adhesive invasion-promoting matricellular protein SPARC: Landscaping activity of Smad4 as revealed by a "secretome" analysis Proteomics 2004, 4 (5) 1324-1334
10. Zhong, L.; Roybal, J.; Chaerkady, R.; Zhang, W.; Choi, K.; Alvarez, C. A.; Tran, H.; Creighton, C. J.; Yan, S.; Strieter, R. M.; Pandey, A.; Kurie, J. M. Identification of secreted proteins that mediate cell-cell interactions in an in vitro model of the lung cancer microenvironment Cancer Res. 2008, 68 (17) 7237-7245
11. De Boeck, A.; Hendrix, A.; Maynard, D.; Van Bockstal, M.; Daniels, A.; Pauwels, P.; Gespach, C.; Bracke, M.; De Wever, O. Differential secretome analysis of cancer-associated fibroblasts and bone marrow-derived precursors to identify microenvironmental regulators of colon cancer progression Proteomics 2013, 13 (2) 379-388
12. Xu, B. J.; Yan, W.; Jovanovic, B.; An, A. Q.; Cheng, N.; Aakre, M. E.; Yi, Y.; Eng, J.; Link, A. J.; Moses, H. L. Quantitative analysis of the secretome of TGF-beta signaling-deficient mammary fibroblasts Proteomics 2010, 10 (13) 2458-2470
13. Egeblad, M.; Werb, Z. New functions for the matrix metalloproteinases in cancer progression Nat. Rev. Cancer 2002, 2 (3) 161-174
14. Lopez-Otin, C.; Matrisian, L. M. Emerging roles of proteases in tumour suppression Nat. Rev. Cancer 2007, 7 (10) 800-808
15. Overall, C. M.; Kleifeld, O. Tumour microenvironment-opinion: validating matrix metalloproteinases as drug targets and anti-targets for cancer therapy Nat. Rev. Cancer 2006, 6 (3) 227-239
16. Bhowmick, N. A.; Neilson, E. G.; Moses, H. L. Stromal fibroblasts in cancer initiation and progression Nature 2004, 432 (7015) 332-337
17. Kalluri, R.; Zeisberg, M. Fibroblasts in cancer Nat. Rev. Cancer 2006, 6 (5) 392-401
18. De Wever, O.; Demetter, P.; Mareel, M.; Bracke, M. Stromal myofibroblasts are drivers of invasive cancer growth Int. J. Cancer 2008, 123 (10) 2229-2238
19. Holmberg, C.; Quante, M.; Steele, I.; Kumar, J.; Balabanova, S.; Duval, C.; Czepan, M.; Rakonczayjr, Z.; Tiszlavicz, L.; Nemeth, I.; Lazar, G.; Simonka, Z.; Jenkins, R.; Hegyi, P.; Wang, T.; Dockray, G.; Varro, A. Release of TGFbetaig-h3 by gastric myofibroblasts slows tumor growth and is decreased with cancer progression Carcinogenesis 2012, 33, 1553-1562
20. Powell, D. W.; Mifflin, R. C.; Valentich, J. D.; Crowe, S. E.; Saada, J. I.; West, A. B. Myofibroblasts. I. Paracrine cells important in health and disease Am. J. Physiol. 1999, 277 (1 Pt 1) C1-C9
21. Powell, D. W.; Pinchuk, I. V.; Saada, J. I.; Chen, X.; Mifflin, R. C. Mesenchymal cells of the intestinal lamina propria Annu. Rev. Physiol. 2011, 73, 213-237
22. Houghton, J.; Stoicov, C.; Nomura, S.; Rogers, A. B.; Carlson, J.; Li, H.; Cai, X.; Fox, J. G.; Goldenring, J. R.; Wang, T. C. Gastric cancer originating from bone marrow-derived cells Science 2004, 306 (5701) 1568-1571
23. Quante, M.; Tu, S. P.; Tomita, H.; Gonda, T.; Wang, S. S.; Takashi, S.; Baik, G. H.; Shibata, W.; Diprete, B.; Betz, K. S.; Friedman, R.; Varro, A.; Tycko, B.; Wang, T. C. Bone marrow-derived myofibroblasts contribute to the mesenchymal stem cell niche and promote tumor growth Cancer Cell 2011, 19 (2) 257-272
24. Jiang, L.; Gonda, T. A.; Gamble, M. V.; Salas, M.; Seshan, V.; Tu, S.; Twaddell, W. S.; Hegyi, P.; Lazar, G.; Steele, I.; Varro, A.; Wang, T. C.; Tycko, B. Global hypomethylation of genomic DNA in cancer-associated myofibroblasts Cancer Res. 2008, 68 (23) 9900-9908
25. Gevaert, K.; Van Damme, J.; Goethals, M.; Thomas, G. R.; Hoorelbeke, B.; Demol, H.; Martens, L.; Puype, M.; Staes, A.; Vandekerckhove, J. Chromatographic isolation of methionine-containing peptides for gel-free proteome analysis: identification of more than 800 Escherichia coli proteins Mol. Cell. Proteomics 2002, 1 (11) 896-903
26. Gevaert, K.; Goethals, M.; Martens, L.; Van, D. J.; Staes, A.; Thomas, G. R.; Vandekerckhove, J. Exploring proteomes and analyzing protein processing by mass spectrometric identification of sorted N-terminal peptides Nat. Biotechnol. 2003, 21 (5) 566-569
27. Staes, A.; Impens, F.; Van Damme, P.; Ruttens, B.; Goethals, M.; Demol, H.; Timmerman, E.; Vandekerckhove, J.; Gevaert, K. Selecting protein N-terminal peptides by combined fractional diagonal chromatography Nat. Protoc. 2011, 6 (8) 1130-1141
28. Ghesquiere, B.; Colaert, N.; Helsens, K.; Dejager, L.; Vanhaute, C.; Verleysen, K.; Kas, K.; Timmerman, E.; Goethals, M.; Libert, C.; Vandekerckhove, J.; Gevaert, K. In vitro and in vivo protein-bound tyrosine nitration characterized by diagonal chromatography Mol. Cell. Proteomics 2009, 8 (12) 2642-2652
29. Impens, F.; Colaert, N.; Helsens, K.; Ghesquiere, B.; Timmerman, E.; De Bock, P. J.; Chain, B. M.; Vandekerckhove, J.; Gevaert, K. A quantitative proteomics design for systematic identification of protease cleavage events Mol. Cell. Proteomics 2010, 9 (10) 2327-2333
30. Helsens, K.; Colaert, N.; Barsnes, H.; Muth, T.; Flikka, K.; Staes, A.; Timmerman, E.; Wortelkamp, S.; Sickmann, A.; Vandekerckhove, J.; Gevaert, K.; Martens, L. ms-lims, a simple yet powerful open source laboratory information management system for MS-driven proteomics Proteomics 2010, 10 (6) 1261-1264
31. Colaert, N.; Helsens, K.; Impens, F.; Vandekerckhove, J.; Gevaert, K. Rover: a tool to visualize and validate quantitative proteomics data from different sources Proteomics 2010, 10 (6) 1226-1229
32. Barsnes, H.; Vizcaino, J. A.; Eidhammer, I.; Martens, L. PRIDE Converter: making proteomics data-sharing easy Nat. Biotechnol. 2009, 27 (7) 598-599
33. Hemers, E.; Duval, C.; McCaig, C.; Handley, M.; Dockray, G. J.; Varro, A. Insulin-like growth factor binding protein-5 is a target of matrix metalloproteinase-7: implications for epithelial-mesenchymal signaling Cancer Res. 2005, 65 (16) 7363-7369
34. Netzel-Arnett, S.; Fields, G. B.; Birkedal-Hansen, H.; Van Wart, H. E. Sequence specificities of human fibroblast and neutrophil collagenases J. Biol. Chem. 1991, 266 (11) 6747-6755
35. McCaig, C.; Duval, C.; Hemers, E.; Steele, I.; Pritchard, D. M.; Przemeck, S.; Dimaline, R.; Ahmed, S.; Bodger, K.; Kerrigan, D. D.; Wang, T. C.; Dockray, G. J.; Varro, A. The role of matrix metalloproteinase-7 in redefining the gastric microenvironment in response to Helicobacter pylori Gastroenterology 2006, 130 (6) 1754-1763
36. Varro, A.; Noble, P. J.; Pritchard, D. M.; Kennedy, S.; Hart, C. A.; Dimaline, R.; Dockray, G. J. Helicobacter pylori induces plasminogen activator inhibitor 2 (PAI-2) in gastric epithelial cells through NF-kB and RhoA: implications for invasion and apoptosis Cancer Res. 2004, 64, 1695-1702
37. Jacobsen, E. J.; Mitchell, M. A.; Hendges, S. K.; Belonga, K. L.; Skaletzky, L. L.; Stelzer, L. S.; Lindberg, T. J.; Fritzen, E. L.; Schostarez, H. J.; O'Sullivan, T. J.; Maggiora, L. L.; Stuchly, C. W.; Laborde, A. L.; Kubicek, M. F.; Poorman, R. A.; Beck, J. M.; Miller, H. R.; Petzold, G. L.; Scott, P. S.; Truesdell, S. E.; Wallace, T. L.; Wilks, J. W.; Fisher, C.; Goodman, L. V.; Kaytes, P. S. Synthesis of a series of stromelysin-selective thiadiazole urea matrix metalloproteinase inhibitors J. Med. Chem. 1999, 42 (9) 1525-1536
38. Koivunen, E.; Arap, W.; Valtanen, H.; Rainisalo, A.; Medina, O. P.; Heikkila, P.; Kantor, C.; Gahmberg, C. G.; Salo, T.; Konttinen, Y. T.; Sorsa, T.; Ruoslahti, E.; Pasqualini, R. Tumor targeting with a selective gelatinase inhibitor Nat. Biotechnol. 1999, 17 (8) 768-774
39. Hanash, S.; Taguchi, A. The grand challenge to decipher the cancer proteome Nat. Rev. Cancer 2010, 10 (9) 652-660
40. Kleifeld, O.; Doucet, A.; auf dem Keller, U.; Prudova, A.; Schilling, O.; Kainthan, R. K.; Starr, A. E.; Foster, L. J.; Kizhakkedathu, J. N.; Overall, C. M. Isotopic labeling of terminal amines in complex samples identifies protein N-termini and protease cleavage products Nat. Biotechnol. 2010, 28 (3) 281-288
41. Dean, R. A.; Overall, C. M. Proteomics discovery of metalloproteinase substrates in the cellular context by iTRAQ labeling reveals a diverse MMP-2 substrate degradome Mol. Cell. Proteomics 2007, 6 (4) 611-623
42. Prudova, A.; auf dem, K. U.; Butler, G. S.; Overall, C. M. Multiplex N-terminome analysis of MMP-2 and MMP-9 substrate degradomes by iTRAQ-TAILS quantitative proteomics Mol. Cell. Proteomics 2010, 9 (5) 894-911
43. Dowling, P.; Clynes, M. Conditioned media from cell lines: a complementary model to clinical specimens for the discovery of disease-specific biomarkers Proteomics 2011, 11 (4) 794-804
44. Skalnikova, H.; Motlik, J.; Gadher, S. J.; Kovarova, H. Mapping of the secretome of primary isolates of mammalian cells, stem cells and derived cell lines Proteomics 2011, 11 (4) 691-708
45. Van Wart, H. E.; Birkedal-Hansen, H. The cysteine switch: a principle of regulation of metalloproteinase activity with potential applicability to the entire matrix metalloproteinase gene family Proc. Natl. Acad. Sci. U. S. A. 1990, 87 (14) 5578-5582
46. Anton, K.; Glod, J. Targeting the tumor stroma in cancer therapy Curr. Pharm. Biotechnol. 2009, 10 (2) 185-191