Contribution of cathepsin L to secretome composition and cleavage pattern of mouse embryonic fibroblasts

Biological Chemistry

Volumn 392, Issue 11, 2011, Pages 961-971

  Tholen, Stefan ^a   Biniossek, Martin L ^a   Geßler, Anna Lena ^a   Müller, Sebastian ^a   Weißer, Juliane ^a   Kizhakkedathu, Jayachandran N ^b   Reinheckel, Thomas ^a   Schilling, Oliver ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

cell conditioned medium; cysteine protease; matrix metalloprotease 2; periostin; protease specificity; proteolysis

Indexed keywords

CATHEPSIN L; GELATINASE A; PROLINE; PROTEINASE; PROTEINASE INHIBITOR; PROTEOME; SECRETOME; TRANSCRIPTION FACTOR RUNX2; UNCLASSIFIED DRUG;

AMINO ACID COMPOSITION; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL DIVISION; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; ENZYME SPECIFICITY; EXTRACELLULAR MATRIX; FIBROBLAST; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEOMICS;

AMINO ACID SEQUENCE; ANIMALS; CATHEPSIN L; CELL LINE; FIBROBLASTS; GENE DELETION; MICE; MOLECULAR SEQUENCE DATA; PROTEOME; PROTEOMICS;

EID: 80053631796     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/BC.2011.162     Document Type: Article

References (72)

1. Acuff, H.B., Carter, K.J., Fingleton, B., Gorden, D.L., and Matrisian, L.M. (2006). Matrix metalloproteinase-9 from bone marrow-derived cells contributes to survival but not growth of tumor cells in the lung microenvironment. Cancer Res. 66, 259-266. (Pubitemid 43166032)
2. auf dem Keller, U. and Schilling, O. (2010). Proteomic techniques and activity-based probes for the system-wide study of proteoly-sis. Biochimie 92, 1705-1714.
3. Bao, S., Ouyang, G., Bai, X., Huang, Z., Ma, C., Liu, M., Shao, R., Anderson, R.M., Rich, J.N., and Wang, X.F. (2004). Periostin potently promotes metastatic growth of colon cancer by augmenting cell survival via the Akt/PKB pathway. Cancer Cell 5, 329-339. (Pubitemid 38482069)
4. Barbarin, A. and Frade, R. (2011). Procathepsin L secretion, which triggers tumor progression, is regulated by Rab4A in human melanoma cells. Biochem. J. 437, 97-107.
5. Benavides, F., Perez, C., Blando, J., Contreras, O., Shen, J., Coussens, L.M., Fischer, S.M., Kusewitt, D.F., Digiovanni, J., and Conti, C.J. (2011). Protective role of cathepsin L in mouse skin car-cinogenesis. Molecular Carcinogenesis. doi:10.1002/mc.20792; 2011 May.
6. Bernhardt, A., Kuester, D., Roessner, A., Reinheckel, T., and Krueger, S. (2010). Cathepsin X-defi cient gastric epithelial cells in co-culture with macrophages: characterization of cytokine response and migration capability after Helicobacter pylori infection. J. Biol. Chem. 285, 33691-33700.
7. Boersema, P.J., Raijmakers, R., Lemeer, S., Mohammed, S., and Heck, A.J. (2009). Multiplex peptide stable isotope dimethyl labeling for quantitative proteomics. Nat. Protoc. 4, 484-494.
8. Butcher, J.T., Norris, R.A., Hoffman, S., Mjaatvedt, C.H., and Markwald, R.R. (2007). Periostin promotes atrioventricular mes-enchyme matrix invasion and remodeling mediated by integrin signaling through Rho/PI 3-kinase. Dev. Biol. 302, 256-266. (Pubitemid 46099041)
9. Choe, Y., Leonetti, F., Greenbaum, D.C., Lecaille, F., Bogyo, M., Bromme, D., Ellman, J.A., and Craik, C.S. (2006). Substrate profi ling of cysteine proteases using a combinatorial peptide library identifi es functionally unique specifi cities. J. Biol. Chem. 281, 12824-12832. (Pubitemid 43855375)
10. Craig, R. and Beavis, R.C. (2004). TANDEM: matching proteins with tandem mass spectra. Bioinformatics 20, 1466-1467. (Pubitemid 38931421)
11. Curran, S. and Murray, G.I. (1999). Matrix metalloproteinases in tumour invasion and metastasis. J. Pathol. 189, 300-308. (Pubitemid 29489213)
12. Dean, R.A., Butler, G.S., Hamma-Kourbali, Y., Delbe, J., Brigstock, D.R., Courty, J., and Overall, C.M. (2007). Identifi cation of candidate angiogenic inhibitors processed by matrix metalloprotei-nase 2 (MMP-2) in cell-based proteomic screens: disruption of vascular endothelial growth factor (VEGF)/heparin affi n regulatory peptide (pleiotrophin) and VEGF/connective tissue growth factor angiogenic inhibitory complexes by MMP-2 proteolysis. Mol. Cell. Biol. 27, 8454-8465.
13. Dean, R.A. and Overall, CM. (2007). Proteomics discovery of metalloproteinase substrates in the cellular context by iTRAQ labeling reveals a diverse MMP-2 substrate degradome. Mol. Cell. Proteomics 6, 611-623. (Pubitemid 46630094)
14. Dehrmann, F.M., Coetzer, T.H., Pike, R.N., and Dennison, C. (1995). Mature cathepsin L is substantially active in the ionic milieu of the extracellular medium. Arch. Biochem. Biophys. 324, 93-98.
15. Dennemarker, J., Lohmuller, T., Mayerle, J., Tacke, M., Lerch, M.M., Coussens, L.M., Peters, C, and Reinheckel, T. (2010a). Defi ciency for the cysteine protease cathepsin L promotes tumor progression in mouse epidermis. Oncogene 29, 1611-1621.
16. Dennemarker, J., Lohmuller, T., Muller, S., Aguilar, S.V., Tobin, DJ., Peters, C, and Reinheckel, T. (2010b). Impaired turnover of autophagolysosomes in cathepsin L defi ciency. Biol. Chem. 391, 913-922.
17. Egeblad, M. and Werb, Z. (2002). New functions for the matrix metalloproteinases in cancer progression. Nat. Rev. Cancer 2, 161-174. (Pubitemid 37328786)
18. Felbor, U., Dreier, L., Bryant, R.A., Ploegh, H.L., Olsen, B.R., and Mothes, W. (2000). Secreted cathepsin L generates endostatin from collagen XVIII. EMBO J. 19, 1187-1194. (Pubitemid 30151015)
19. Friedrichs, B., Tepel, C, Reinheckel, T, Deussing, J., von Figura, K., Herzog, V, Peters, C, Saftig, P., and Brix, K. (2003). Thyroid functions of mouse cathepsins B, K, and L. J. Clin. Invest. 111, 1733-1745. (Pubitemid 38057754)
20. Funkelstein, L., Toneff, T, Mosier, C, Hwang, S.R., Beuschlein, F, Lichtenauer, U.D., Reinheckel, T., Peters, C, and Hook, V (2008). Major role of cathepsin L for producing the peptide hormones ACTH, ß-endorphin, and a-MSH, illustrated by protease gene knockout and expression. J. Biol. Chem. 283, 35652-35659.
21. Gocheva, V, Zeng, W., Ke, D., Klimstra, D., Reinheckel, T, Peters, C, Hanahan, D., and Joyce, J.A. (2006). Distinct roles for cysteine cathepsin genes in multistage tumorigenesis. Genes Dev. 20, 543-556. (Pubitemid 43345321)
22. Gocheva, V, Wang, H.W., Gadea, B.B., Shree, T, Hunter, K.E., Garfall, A.L., Berman, T, and Joyce, J.A. (2010). IL-4 induces cathepsin protease activity in tumor-associated macrophages to promote cancer growth and invasion. Genes Dev. 24, 241-255.
23. Gosalia, D.N., Salisbury, CM., Ellman, J.A., and Diamond, S.L. (2005). High throughput substrate specifi city profi ling of serine and cysteine proteases using solution-phase fl uorogenic peptide microarrays. Mol. Cell. Proteomics 4, 626-636. (Pubitemid 40867268)
24. Greenbaum, D., Luscombe, N.M., Jansen, R., Qian, J., and Gerstein, M. (2001). Interrelating different types of genomic data, from proteome to secretome: ' oming in on function. Genome Res. 11, 1463-1468. (Pubitemid 32894671)
25. Guo, K., Ji, C, and Li, L. (2007). Stable-isotope dimethylation labeling combined with LC-ESI MS for quantifi cation of amine-containing metabolites in biological samples. Anal. Chem. 79, 8631-8638. (Pubitemid 350171373)
26. Han, D.K., Eng, J., Zhou, H, and Aebersold, R. (2001). Quantitative profi ling of differentiation-induced microsomal proteins using isotope-coded affi nity tags and mass spectrometry. Nat. Biotechnol. 19, 946-951. (Pubitemid 32947573)
27. + T cell selection independently of its effect on invariant chain: a role in the generation of positively selecting peptide ligands. J. Exp. Med. 195, 1349-1358. (Pubitemid 34564336)
28. Horiuchi, K., Amizuka, N, Takeshita, S., Takamatsu, H, Katsuura, M., Ozawa, H., Toyama, Y., Bonewald, L.F., and Kudo, A. (1999). Identifi cation and characterization of a novel protein, periostin, with restricted expression to periosteum and periodontal ligament and increased expression by transforming growth factor β. J. Bone Miner. Res. 14, 1239-1249. (Pubitemid 29314070)
29. Imai, K., Hiramatsu, A., Fukushima, D., Pierschbacher, M.D., and Okada, Y. (1997). Degradation of decorin by matrix metallo-proteinases: identifi cation of the cleavage sites, kinetic analyses and transforming growth factor-β 1 release. Biochem. J. 322, 809-814. (Pubitemid 27135628)
30. Jedeszko, C. and Sloane, B.F. (2004). Cysteine cathepsins in human cancer. Biol. Chem. 385, 1017-1027. (Pubitemid 39600309)
31. Jordans, S., Jenko-Kokalj, S., Kuhl, N.M., Tedelind, S., Sendt, W., Bromme, D., Turk, D., and Brix, K. (2009). Monitoring compart-ment-specifi c substrate cleavage by cathepsins B, K, L, and S at physiological pH and redox conditions. BMC Biochem. 10, 23.
32. Joyce, J.A., Baruch, A., Chehade, K., Meyer-Morse, N., Giraudo, E., Tsai, F.Y., Greenbaum, D.C., Hager, J.H., Bogyo, M., and Hanahan, D. (2004). Cathepsin cysteine proteases are effectors of invasive growth and angiogenesis during multistage tumori-genesis. Cancer Cell 5, 443-453. (Pubitemid 38610246)
33. Keller, A., Nesvizhskii, A.I., Kolker, E., and Aebersold, R. (2002). Empirical statistical model to estimate the accuracy of peptide identifi cations made by MS/MS and database search. Anal. Chem. 74, 5383-5392. (Pubitemid 35215372)
34. Kersey, P.J., Duarte, J., Williams, A., Karavidopoulou, Y., Birney, E., and Apweiler, R. (2004). The International Protein Index: an integrated database for proteomics experiments. Proteomics 4, 1985-1988. (Pubitemid 38880363)
35. Kirschke, H., Kembhavi, A.A., Bohley, P., and Barrett, A.J. (1982). Action of rat liver cathepsin L on collagen and other substrates. Biochem. J. 201, 367-372. (Pubitemid 12160167)
36. 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 identifi es protein N-termini and protease cleavage products. Nat. Biotechnol. 28, 281-288.
37. Kleifeld, O., Doucet, A., Prudova, A., auf dem Keller, U., Gioia, M., Kizhakkedathu, J., and Overall, C.M. (2011). System-wide pro-teomic identifi cation of protease cleavage products by terminal amine isotopic labeling of substrates. Nat. Prot. 28, 281-288.
38. Li, X.J., Zhang, H., Ranish, J.A., and Aebersold, R. (2003). Automated statistical analysis of protein abundance ratios from data generated by stable-isotope dilution and tandem mass spec-trometry. Anal. Chem. 75, 6648-6657. (Pubitemid 37493927)
39. Loffek, S., Schilling, O., and Franzke, C.W. (2011). Series "matrix metalloproteinases in lung health and disease": Biological role of matrix metalloproteinases: a critical balance. Eur. Respir. J. 38, 191-208.
40. Mason, R.W., Gal, S., and Gottesman, M.M. (1987). The identifi-cation of the major excreted protein (MEP) from a transformed mouse fi broblast cell line as a catalytically active precursor form of cathepsin L. Biochem. J. 248, 449-454.
41. Mohamed, M.M. and Sloane, B.F. (2006). Cysteine cathepsins: multifunctional enzymes in cancer. Nat. Rev. Cancer 6, 764-775. (Pubitemid 44450465)
42. Molloy, M.P., Brzezinski, E.E., Hang, J., McDowell, M.T., and VanBogelen, R.A. (2003). Overcoming technical variation and biological variation in quantitative proteomics. Proteomics 3, 1912-1919. (Pubitemid 37305885)
43. Morgenstern, J.P. and Land, H. (1990). Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res. 18, 3587-3596.
44. Mort, J.S. (2004). Cathepsin B. In: Handbook of Proteolytic Enzymes, A.J. Barrett, N.D. Rawlings and J.F. Woessner, eds. (Montreal: Elsevier Academic Press), p. 1081.
45. Nakagawa, T., Roth, W., Wong, P., Nelson, A., Farr, A., Deussing, J., Villadangos, J.A., Ploegh, H., Peters, C., and Rudensky, A.Y. (1998). Cathepsin L: critical role in Ii degradation and CD4 T cell selection in the thymus. Science 280, 450-453. (Pubitemid 28208170)
46. Nesvizhskii, A.I., Keller, A., Kolker, E., and Aebersold, R. (2003). A statistical model for identifying proteins by tandem mass spec-trometry. Anal. Chem. 75, 4646-4658. (Pubitemid 37082259)
47. Norris, R.A., Damon, B., Mironov, V., Kasyanov, V., Ramamurthi, A., Moreno-Rodriguez, R., Trusk, T., Potts, J.D., Goodwin, R.L., Davis, J., et al. (2007). Periostin regulates collagen fi brillogen-esis and the biomechanical properties of connective tissues. J. Cell. Biochem. 101, 695-711. (Pubitemid 46698854)
48. Norris, R.A., Moreno-Rodriguez, R.A., Sugi, Y., Hoffman, S., Amos, J., Hart, M.M., Potts, J.D., Goodwin, R.L., and Markwald, R.R. (2008). Periostin regulates atrioventricular valve maturation. Dev. Biol. 316, 200-213.
49. Olsen, J.V., Ong, S.E., and Mann, M. (2004). Trypsin cleaves exclusively C-terminal to arginine and lysine residues. Mol. Cell. Proteomics 3, 608-614. (Pubitemid 38878520)
50. Petermann, I., Mayer, C., Stypmann, J., Biniossek, M.L., Tobin, D.J., Engelen, M.A., Dandekar, T., Grune, T., Schild, L., Peters, C., et al. (2006). Lysosomal, cytoskeletal, and metabolic alterations in cardiomyopathy of cathepsin L knockout mice. FASEB J. 20, 1266-1268.
51. Planque, C., Kulasingam, V., Smith, C.R., Reckamp, K., Goodglick, L., and Diamandis, E.P. (2009). Identifi cation of fi ve candidate lung cancer biomarkers by proteomics analysis of conditioned media of four lung cancer cell lines. Mol. Cell. Proteomics 8, 2746-2758.
52. 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 proteom-ics. Mol. Cell. Proteomics 9, 894-911.
53. Rappsilber, J., Ishihama, Y., and Mann, M. (2003). Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteom-ics. Anal. Chem. 75, 663-670. (Pubitemid 36176744)
54. Rawlings, N.D., Barrett, A.J., and Bateman, A. (2010). MEROPS: the peptidase database. Nucleic Acids Res. 38, D227-D233.
55. Reinheckel, T., Hagemann, S., Dollwet-Mack, S., Martinez, E., Lohmuller, T., Zlatkovic, G., Tobin, D.J., Maas-Szabowski, N., and Peters, C. (2005). The lysosomal cysteine protease cathepsin L regulates keratinocyte proliferation by control of growth factor recycling. J. Cell Sci. 11 8, 3387-3395. (Pubitemid 41246094)
56. Roth, W., Deussing, J., Botchkarev, V.A., Pauly-Evers, M., Saftig, P., Hafner, A., Schmidt, P., Schmahl, W., Scherer, J., AntonLamprecht, I., et al. (2000). Cathepsin L defi ciency as molecular defect of furless: hyperproliferation of keratinocytes and pertu-bation of hair follicle cycling. FASEB J. 14, 2075-2086.
57. Ruan, K., Bao, S., and Ouyang, G. (2009). The multifaceted role of periostin in tumorigenesis. Cell. Mol. Life Sci. 66, 2219-2230.
58. Schilling, O. and Overall, C.M. (2008). Proteome-derived, database-searchable peptide libraries for identifying protease cleavage sites. Nat. Biotechnol. 26, 685-694. (Pubitemid 351809596)
59. Schilling, O., Huesgen, P.F., Barre, O., auf dem Keller, U., and Overall, C.M. (2011). Characterization of the prime and non-prime active site specifi cities of proteases by proteome-derived peptide libraries and tandem mass spectrometry. Nat. Protoc. 6, 111-120.
60. Sevenich, L., Schurigt, U., Sachse, K., Gajda, M., Werner, F., Muller, S., Vasiljeva, O., Schwinde, A., Klemm, N., Deussing, J., et al. (2010). Synergistic antitumor effects of combined cathepsin B and cathepsin Z defi ciencies on breast cancer progression and metastasis in mice. Proc. Natl. Acad. Sci. USA 107, 2497-2502.
61. Sidhu, S.S., Yuan, S., Innes, A.L., Kerr, S., Woodruff, P.G., Hou, L., Muller, S.J., and Fahy, J.V. (2010). Roles of epithelial cell-derived periostin in TGF-β activation, collagen production, and collagen gel elasticity in asthma. Proc. Natl. Acad. Sci. USA 107, 14170-14175.
62. Snider, P., Hinton, R.B., Moreno-Rodriguez, R.A., Wang, J., Rogers, R., Lindsley, A., Li, F., Ingram, D.A., Menick, D., Field, L., et al. (2008). Periostin is required for maturation and extracellular matrix stabilization of noncardiomyocyte lineages of the heart. Circ. Res. 102, 752-760. (Pubitemid 351521582)
63. Soneoka, Y., Cannon, P.M., Ramsdale, E.E., Griffiths, J.C., Romano, G., Kingsman, S.M., and Kingsman, A.J. (1995). A transient three-plasmid expression system for the production of high titer retroviral vectors. Nucleic Acids Res. 23, 628-633.
64. Spira, D., Stypmann, J., Tobin, D.J., Petermann, I., Mayer, C., Hagemann, S., Vasiljeva, O., Gunther, T., Schule, R., Peters, C., et al. (2007). Cell type-specifi c functions of the lysosomal protease cathepsin L in the heart. J. Biol. Chem. 282, 37045-37052.
65. Strojnik, T., Kavalar, R., Trinkaus, M., and Lah, T.T. (2005). Cathepsin L in glioma progression: comparison with cathepsin B. Cancer Detect. Prev. 29, 448-455. (Pubitemid 41406140)
66. Tang, Q., Cai, J., Shen, D., Bian, Z., Yan, L., Wang, Y.X., Lan, J., Zhuang, G.Q., Ma, W.Z., and Wang, W. (2009). Lysosomal cysteine peptidase cathepsin L protects against cardiac hypertrophy through blocking AKT/GSK3 β signaling. J. Mol. Med. 87, 249-260.
67. Tobin, D.J., Foitzik, K., Reinheckel, T., Mecklenburg, L., Botchkarev, V.A., Peters, C., and Paus, R. (2002). The lysosomal protease cathepsin L is an important regulator of keratinocyte and mel-anocyte differentiation during hair follicle morphogenesis and cycling. Am. J. Pathol. 160, 1807-1821. (Pubitemid 34525660)
68. Turk, B., Dolenc, I., Turk, V., and Bieth, J.G. (1993). Kinetics of the pH-induced inactivation of human cathepsin L. Biochemistry 32, 375-380. (Pubitemid 23033357)
69. Turk, B., Bieth, J.G., Bjork, I., Dolenc, I., Turk, D., Cimerman, N., Kos, J., Colic, A., Stoka, V., and Turk, V. (1995). Regulation of the activity of lysosomal cysteine proteinases by pH-induced inactivation and/or endogenous protein inhibitors, cystatins. Biol. Chem. Hoppe-Seyler 376, 225-230.
70. Turk, V., Turk, B., and Turk, D. (2001). Lysosomal cysteine proteases: facts and opportunities. EMBO J. 20, 4629-4633. (Pubitemid 32848615)
71. Xu, B.J., Yan, W., Jovanovic, B., An, A.Q., Cheng, N., Aakre, M.E., Yi, Y., Eng, J., Link, A.J., and Moses, H.L. (2010). Quantitative analysis of the secretome of TGF-β signaling-defi cient mammary fi broblasts. Proteomics 10, 2458-2470.
72. Yasothornsrikul, S., Greenbaum, D., Medzihradszky, K.F., Toneff, T., Bundey, R., Miller, R., Schilling, B., Petermann, I., Dehnert, J., Logvinova, A., et al. (2003). Cathepsin L in secretory vesicles functions as a prohormone-processing enzyme for production of the enkephalin peptide neurotransmitter. Proc. Natl. Acad. Sci. USA 100, 9590-9595. (Pubitemid 37033972)