The activity and localization patterns of cathepsins B and X in cells of the mouse gastrointestinal tract differ along its length

Biological Chemistry

Volumn 395, Issue 10, 2014, Pages 1201-1219

  Tamhane, Tripti ^a   Arampatzidou, Maria ^a,d   Gerganova, Veneta ^a   Tacke, Marlene ^b   Illukkumbura, Rukshala ^a   Dauth, Stephanie ^a   Schaschke, Norbert ^c   Peters, Christoph ^b   Reinheckel, Thomas ^b   Brix, Klaudia ^e  

^a JACOBS UNIVERSITY BREMEN   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c BIELEFELD UNIVERSITY   (Germany)

^d STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e HARVARD UNIVERSITY   (United States)

Author keywords

Activity based probes; Colon; Cysteine cathepsins; Duodenum; Ileum; Jejunum

Indexed keywords

CATHEPSIN B; CATHEPSIN X; COLLAGEN TYPE 4; MICROSOMAL AMINOPEPTIDASE; UVOMORULIN; CADHERIN; CATHEPSIN; CATHEPSIN X, MOUSE; CTSB PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; BASEMENT MEMBRANE; BRUSH BORDER; CONFERENCE PAPER; CONTROLLED STUDY; DUODENUM; EXTRACELLULAR MATRIX; GASTROINTESTINAL TRACT; GENOTYPE; ILEUM; IMMUNOFLUORESCENCE; JEJUNUM; LAMINA PROPRIA; LARGE INTESTINE; MOLECULAR WEIGHT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; ANIMAL; CYTOLOGY; GENETICS; KNOCKOUT MOUSE; METABOLISM;

MUS;

ANIMALS; CADHERINS; CATHEPSIN B; CATHEPSINS; GASTROINTESTINAL TRACT; ILEUM; JEJUNUM; MICE; MICE, KNOCKOUT;

EID: 84926444146     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/hsz-2014-0151     Document Type: Conference Paper

References (59)

1. Arampatzidou, M., Mayer, K., Iolyeva, M.E., Asrat, S.G., Ravichandran, M., Gunther, T., Schule, R., Reinheckel, T., and Brix, K. (2011a). Studies of intestinal morphology and cathepsin B expression in a transgenic mouse aiming at intestine-specific expression of Cath B-EGFP. Biol. Chem. 392, 983-993.
2. Arampatzidou, M., Rehders, M., Dauth, S., Yu, D.M.T., Tedelind, S., and Brix, K. (2011b). Imaging of protease functions-current guide to spotting cysteine cathepsins in classical and novel scenes of action in mammalian epithelial cells and tissues. Ital. J. Anat. Embryol. 116, 1-19.
3. Arampatzidou, M., Schütte, A., Hansson, G.C., Saftig, P., and Brix, K. (2012). Effects of cathepsin K deficiency on intercellular junction proteins, luminal mucus layers, and ECM constituents in mouse colon. Biol. Chem. 393, 1391-1403.
4. Bankus, J.M. and Bond, J.S. (1996). Expression and distribution of meprin protease subunits in mouse intestine. Arch. Biochem. Biophys. 331, 87-94.
5. Bengsch, F., Buck, A., Günther, S.C., Seiz, J.R., Tacke, M., Pfeifer, D., von Elverfeldt, L., Sevenich, L., Hillebrand, L.E., Kern, U., et al. (2013). Cell type-dependent pathogenic functions of overexpressed human cathepsin B in murine breast cancer progression. Oncogene. doi: 10.1038/onc.2013.395 [Epub ahead of print].
6. Bernhardt, A., Kuester, D., Roessner, A., Reinheckel, T., and Krueger, S. (2010). Cathepsin X-deficient 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. Bradley, S.G., Antalis, T.M., and Bond, J.S. (2013). Proteases in the mammalian digestive system. In: Proteases: Structure and Function. K. Brix and W. Stöcker, eds. (Wien: Springer-Verlag), pp. 373-393.
8. Brix, K., Dunkhorst, A., Mayer, K., and Jordans, S. (2008). Cysteine cathepsins: cellular roadmap to different functions. Biochimie 90, 194-207.
9. Brix, K., Scott, C.J., and Heck, M.M.S. (2013). Chapter 3: Compartmentalization of proteolysis. In: Proteases: Structure and Function. K. Brix and W. Stöcker, eds. (Wien: Springer-Verlag), pp. 85-125.
10. Buck, M.R., Karustis, D.G., Day, N.A., Honn, K.V., and Sloane, B.F. (1992). Degradation of extracellular-matrix proteins by human cathepsin B from normal and tumour tissues. Biochem. J. 282, 273-278.
11. Buhling, F., Peitz, U., Kruger, S., Kuster, D., Vieth, M., Gebert, I., Roessner, A., Weber, E., Malfertheiner, P., and Wex, T. (2004). Cathepsins K, L, B, X and W are differentially expressed in normal and chronically inflamed gastric mucosa. Biol. Chem. 385, 439-445.
12. Buth, H., Wolters, B., Hartwig, B., Meier-Bornheim, R., Veith, H., Hansen, M., Sommerhoff, C.P., Schaschke, N., Machleidt, W., Fusenig, N.E., et al. (2004). HaCaT keratinocytes secrete lysosomal cysteine proteinases during migration. Eur. J. Cell Biol. 83, 781-795.
13. Dauth, S., Arampatzidou, M., Rehders, M., Yu, D., Führer, D., and Brix, K. (2011). Thyroid cathepsin K - roles in physiology and thyroid disease. Clin. Rev. Bone Miner. Metab. 9, 94-106.
14. Deaton, D.N. and Tavares, F.X. (2005). Design of cathepsin K inhibitors for osteoporosis. Curr. Top. Med. Chem. 5, 1639-1675.
15. 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.
16. Gansz, M., Kern, U., Peters, C., and Reinheckel, T. (2013). Chapter 6: Exploring systemic functions of lysosomal proteases: the perspective of genetically modified mouse models. In: Proteases: Structure and Function. K. Brix and W. Stöcker, eds. (Wien: Springer-Verlag), pp. 217-233.
17. 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.
18. Gounaris, E., Tung, C.H., Restaino, C., Maehr, R., Kohler, R., Joyce, J.A., Ploegh, H., Barrett, T., Weissleder, R., and Khazaie, K. (2008). Live imaging of cysteine-cathepsin activity reveals dynamics of local inflammation, angiogenesis, and polyp growth. PLoS One. 8, e2916.
19. Halangk, W., Lerch, M.M., Brandt-Nedelev, B., Roth, W., Ruthenbuerger, M., Reinheckel, T., Domschke, W., Lippert, H., Peters, C., and Deussing, J. (2000). Role of cathepsin B in intracellular trypsinogen activation and the onset of acute pancreatitis. J. Clin. Invest. 106, 773-781.
20. Johnson, G.D. and Hersh, L.B. (1992). Cloning a rat meprin cDNA reveals the enzyme is a heterodimer. J. Biol. Chem. 267, 13505-13512.
21. Joyce, J.A. and Jeffrey, P.W. (2009). Microenvironmental regulation of metastasis. Nat. Rev. Cancer 9, 239-252.
22. Kos, J., Sekirnik, A., Premzl, A., Zavasnik Bergant, V., Langerholc, T., Turk, B., Werle, B., Golouh, R., Repnik, U., Jeras, M., et al. (2005). Carboxypeptidases cathepsins X and B display distinct protein profile in human cells and tissues. Exp. Cell Res. 306, 103-113.
23. Krueger, S., Bernhardt, A., Kalinski, T., Baldensperger, M., Zeh, M., Teller, A., Adolf, D., Reinheckel, T., Roessner, A., and Kuester, D. (2013). Induction of premalignant host responses by cathepsin x/z-deficiency in Helicobacter pylori-infected mice. PLoS One 7, e70242.
24. Lechner, A.M., Assfalg-Machleidt, I., Zahler, S., Stoeckelhuber, M., Machleidt, W., Jochum, M., and Nagler, D.K. (2006). RGD-dependent binding of procathepsin X to integrin alphavbeta3 mediates cell-adhesive properties. J. Biol. Chem. 281, 39588-39597.
25. Mayer, K., Schwartz, S., Lentze, M.J., Kalff, J.C., and Brix, K. (2006). Extracellular localization of intestinal cathepsins: implications of their actions during post-operative ileus. In: XLI Congress of the European Society for Surgical Research, B. Vollmar, ed. (Rostock, Germany: Medimond International Proceedings), pp. 63-66.
26. Mayer, K., Vreemann, A., Qu, H., and Brix, K. (2009). Release of endo-lysosomal cathepsins B, D, and L from IEC6 cells in a cell culture model mimicking intestinal manipulation. Biol. Chem. 390, 471-480.
27. Medina, C. and Radomski, M.W. (2006). Role of matrix metalloproteinases in intestinal inflammation. J. Pharmacol. Exp. Ther. 318, 933-938.
28. Menzel, K., Hausmann, M., Obermeier, F., Schreiter, K., Dunger, N., Bataille, F., Falk, W., Scholmerich, J., Herfarth, H., and Rogler, G. (2006). Cathepsins B, L and D in inflammatory bowel disease macrophages and potential therapeutic effects of cathepsin inhibition in vivo. Clin. Exp. Immunol. 146, 169-180.
29. Mina-Osorio, P. (2008). The moonlighting enzyme CD13: old and new functions to target. Trends Mol. Med. 14, 361-371.
30. Mohamed, M.M. and Sloane, B.F. (2006). Cysteine cathepsins: multifunctional enzymes in cancer. Nat. Rev. Cancer 6, 764-775.
31. Musil, D., Zucic, D., Turk, D., Engh, R.A., Mayr, I., Huber, R., Popovic, T., Turk, V., Towatari, T., Katunuma, N., et al. (1991). The refined 2.15 A X-ray crystal structure of human liver cathepsin B: the structural basis for its specificity. EMBO J. 10, 2321-2330.
32. Nagler, D.K., Storer, A.C., Portaro, F.C., Carmona, E., Juliano, L., and Menard, R. (1997). Major increase in endopeptidase activity of human cathepsin B upon removal of occluding loop contacts. Biochemistry 36, 12608-12615.
33. Nagler, D.K., Zhang, R., Tam, W., Sulea, T., Purisima, E.O., and Menard, R. (1999). Human cathepsin X: a cysteine protease with unique carboxypeptidase activity. Biochemistry 38, 12648-12654.
34. Nagler, D.K., Kruger, S., Kellner, A., Ziomek, E., Menard, R., Buhtz, P., Krams, M., Roessner, A., and Kellner, U. (2004). Up-regulation of cathepsin X in prostate cancer and prostatic intraepithelial neoplasia. Prostate 60, 109-119.
35. Neuhoff, V., Philipp, K., Zimmer, H.G., and Mesecke, S. (1979). A simple, versatile, sensitive and volume-independent method for quantitative protein determination which is independent of other external influences. Hoppe Seylers Z. Physiol. Chem. 360, 1657-1670.
36. Öbrink, B. (1986). Epithelial cell adhesion molecules. Exp. Cell Res. 163, 1-21.
37. Oppert, B., Morgan, T.D., Hartzer, K., Lenarcic, B., Galesa, K., Brzin, J., Turk, V., Yoza, K., Ohtsubo, K., and Kramer, K.J. (2003). Effects of proteinase inhibitors on digestive proteinases and growth of the red flour beetle, Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae). Comp. Biochem. Physiol. C. Toxicol. Pharmacol. 4, 481-490.
38. Podgorski, I. (2009). Future of anticathepsin K drugs: dual therapy for skeletal disease and atherosclerosis? Future Med. Chem. 1, 21-34.
39. Puzer, L., Cotrin, S.S., Cezari, M.H., Hirata, I.Y., Juliano, M.A., Stefe, I., Turk, D., Turk, B., Juliano, L., and Carmona, A.K. (2005). Recombinant human cathepsin X is a carboxymonopeptidase only: a comparison with cathepsins B and L. Biol. Chem. 386, 1191-1195.
40. Rachner, T.D., Khosla, S., and Hofbauer, L.C. (2011). Osteoporosis: now and the future. Lancet 377, 1276-1287.
41. Rao Malla, R., Gopinath, S., Alapati, K., Gorantla, B., Gondi, C.S., and Rao, J.S. (2013). Knockdown of cathepsin B and uPAR inhibits CD151 and α3β1 integrin-mediated cell adhesion and invasion in glioma. Mol. Carcinog. 10, 777-790.
42. Reiser, J., Adair, B., and Reinheckel, T. (2010). Specialized roles for cysteine cathepsins in health and disease. J. Clin. Invest. 120, 3421-3431.
43. Riese, R.J. and Chapman, H.A. (2000). Cathepsins and compartmentalization in antigen presentation. Curr. Opin. Immunol. 12, 107-113.
44. Santamaria, I., Velasco, G., Pendas, A.M., Fueyo, A., and Lopez-Otin, C. (1998). Cathepsin Z, a novel human cysteine proteinase with a short propeptide domain and a unique chromosomal location. J. Biol. Chem. 273, 16816-16823.
45. Schaschke, N., Assfalg-Machleidt, I., Lassleben, T., Sommerhoff, C.P., Moroder, L., and Machleidt, W. (2000). Epoxysuccinyl peptide-derived affinity labels for cathepsin B. FEBS Lett. 482, 91-96.
46. 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 deficiencies on breast cancer progression and metastasis in mice. Proc. Natl. Acad. Sci. USA 107, 2497-2502.
47. Sina, C., Lipinski, S., Gavrilova, O., Aden, K., Rehman, A., Till, A., Rittger, A., Podschun, R., Meyer-Hoffert, U., Haesler, R., et al. (2012). Extracellular cathepsin K exerts antimicrobial activity and is protective against chronic intestinal inflammation in mice. Gut 62, 520-530.
48. Shimoyama, Y., Yoshida, T., Terada, M., Shimosato, Y., Abe, O., and Hirohashi, S. (1989). Molecular cloning of a human Ca2+-dependent cell-cell adhesion molecule homologous to mouse placental cadherin: its low expression in humann placental tissues. J. Cell Biol. 109, 1787-1794.
49. Skvarc, M., Stubljar, D., Kopitar, A.N., Jeverica, S., Tepes, B., Kos, J., and Ihan, A. (2013). Inhibition of cathepsin X enzyme influences the immune response of THP-1 cells and dendritic cells infected with Helicobacter pylori. Radiol. Oncol. 47, 258-265.
50. Sterchi, E.E., Naim, N.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 intes-tinal microvillus membrane which degrades biologically active peptides. Arch. Biochem. Biophys. 265, 105-118.
51. Takeichi, M. (1988). The cadherins: cell-cell adhesion molecules controlling animal morphogenesis. Development 102, 639-655.
52. Tedelind, S., Jordans, S., Resemann, H., Blum, G., Bogyo, M., Führer, D., and Brix, K. (2011). Cathepsin B trafficking in thyroid carcinoma cells. Thyroid Res. 4, Suppl. 1, S2.
53. Tribolium Genome Sequencing Consortium, Richards, S., Gibbs, R.A., Weinstock, G.M., Brown, S.J., Denell, R., Beeman, R.W., Gibbs, R., Brown, S.J., Friedrich, M., et al. (2008). The genome of the model beetle and pest Tribolium castaneum. Nature 452, 949-955.
54. Turk, B. (2006). Targeting proteases: successes, failures and prospects. Nat. Rev. Drug Discov. 5, 785-799.
55. Turk, V., Turk, B., and Turk, D. (2001). Lysosomal cysteine proteases: facts and opportunities. EMBO J. 20, 4629-4633.
56. Vasiljeva, O., Papazoglou, A., Kruger, A., Brodoefel, H., Korovin, M., Deussing, J., Augustin, N., Nielsen, B.S., Almholt, K., Bogyo, M., et al. (2006). Tumor cell-derived and macrophagederived cathepsin B promotes progression and lung metastasis of mammary cancer. Cancer Res. 66, 5242-5250.
57. Vasiljeva, O., Reinheckel, T., Peters, C., Turk, D., Turk, V., and Turk, B. (2007). Emerging roles of cysteine cathepsins in disease and their potential as drug targets. Curr. Pharm. Des. 13, 387-403.
58. Vreemann, A., Qu, H., Mayer, K., Andersen, L.B., Stefana, M.I., Wehner, S., Lysson, M., Farcas, A.M., Peters, C., Reinheckel, T., et al. (2009). Cathepsin B release from rodent intestine mucosa due to mechanical injury results in extracellular matrix damage in early post-traumatic phases. Biol. Chem. 390, 481-492.
59. Yano, M., Hirai, K., Naito, Z., Yokoyama, M., Ishiwata, T., Shiraki, Y., Inokuchi, M., and Asano, G. (2001). Expression of cathepsin B and cystatin C in human breast cancer. Surg. Today. 31, 385-389.