Human proteoglycan testican-1 inhibits the lysosomal cysteine protease cathepsin L

European Journal of Biochemistry

Volumn 270, Issue 19, 2003, Pages 4008-4015

  Bocock, Jeffrey P ^a   Edgell, Cora Jean S ^a   Marr, Henry S ^a   Erickson, Ann H ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Cathepsin L; Protease; Proteoglycan; Testican; Thyropin

Indexed keywords

CATHEPSIN B; CATHEPSIN L; CHONDROITIN SULFATE; CYSTEINE PROTEINASE; PROTEOGLYCAN; RECOMBINANT PROTEIN; TESTICAN 1; UNCLASSIFIED DRUG;

ARTICLE; CELL VACUOLE; COMPETITIVE INHIBITION; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; HUMAN; HUMAN CELL; INHIBITION KINETICS; LYSOSOME; PH; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DENATURATION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; CATHEPSIN B; CATHEPSINS; CYSTEINE ENDOPEPTIDASES; CYSTEINE PROTEINASE INHIBITORS; ENZYME STABILITY; HUMANS; HYDROGEN-ION CONCENTRATION; LYSOSOMES; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY; PROTEOGLYCANS; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 0141815490     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1033.2003.03789.x     Document Type: Article

References (55)

1. Bonnet, F., Perin, J.-P., Maillet, P., Jolles, P. & Alliel, P.M. (1992) Characterization of a human seminal plasma glycosaminoglycan-bearing polypeptide. Biochem. J. 288, 565-569.
2. Alliel, P.M., Pedrin, J.-P., Jolles, P. & Bonnet, F.J. (1993) Testican, a multidomain testicular proteoglycan resembling modulators of cell social behaviour. Eur. J. Biochem. 214, 347-350.
3. Rieber, A.J., Marr, H.S., Comer, M.B. & Edgell, C.J.S. (1993) Extent of differentiated gene expression in the human endothelium-derived EA.hy926 cell line. Thrombo. Haemost. 69, 476-480.
4. Marr, H.S., Basalamah, M.A. & Edgell, C.-J. (1997) Endothelial cell expression of testican mRNA. Endotheliurn 5, 209-219.
5. Bonnet, F., Perin, J.P., Charbonnier, F., Camuzat, A., Roussel, G., Nussbaum, J.L. & Alliel, P.M. (1996) Structure and cellular distribution of mouse brain testican. J. Biol. Chem. 271, 565-569.
6. Vannahme, C. Schubel S., Herud, M., Gosling, S., Hulsmann, H., Paulsson, M., Hartmann U. & Maurer, P. (1999) Molecular cloning of testican-2: defining a novel calcium-binding proteoglycan family expressed in brain. J. Neurochem. 73, 12-20.
7. Nakada, M., Yamada, A., Takino, T., Miyamori, H., Takahashi, T., Yamashita, J. & Sato H. (2001) Suppression of membrane-type 1 matrix metalloprinase (MMP) -mediated MMP-2 activation and tumor invasion by testican 3 and its splicing variant gene product, N-Tes. Cancer Res, 61, 8896-8902.
8. Greene, L.J., DiCarol, J.J., Sussman, A.J. & Bartelt, D.C. (1968) Two trypsin inhibitors from porcine pancreatic juice. J. Biol. Chem. 243, 1804-1815.
9. Laskowski, M. & Kato, I. (1980) Protein inhibitors of proteinases. Ann. Rev. Biochem. (Snell, E.E., Boyer, P.D., Meister, A. & Richardson, C.C., eds), pp. 593-626. Annual Reviews Inc., Palo Alto, CA.
10. Kohfeldt E., Maurer, P., Vannahme, C. & Timpl, R. (1997) Properties of the extracellular calcium binding module of the proteoglycan testican. FEBS Lett. 414, 557-561.
11. Lenarcic, B. & Bevec, T. (1998) Thyropins - new structually related proteinase inhibitors. Biol. Chem. 379, 105-111.
12. Malthiery, Y. & Lissitzky, S. (1987) Primary structure of human thyroglobulin deduced from the sequence of its 8448-base complementary DNA. Eur. J. Biochem. 165, 491-498.
13. Ogrinc, T., Dolenc, I., Ritonja, A. & Turk, V. (1993) Purification of the Complex of cathepsin L and the MHC class II-associated invariant chain fragment from human kidney. FEBS Lett. 336, 555-559.
14. Guncar, G., Pungercic, G., Klemencic, I., Turk, V. & Turk, D. (1999) Crystal structure of MHC class II-associated p41, Ii fragment bound to cathepsin L reveals the structural basis for differentiation between cathepsins L and S. EMBO J. 18, 793-803.
15. Lenarcic, B., Krishnan, G., Borukhovich R., Ruck, B., Turk, V. & Moczydlowski, E. (2000) Saxiphilin, a saxitoxin-binding protein with two thyroglobulin type 1 domains, is an inhibitor of papain-like cysteine proteinases. J. Biol. Chem. 275, 15572-15577.
16. Lenarcic, B., Ritonja, A., Strukelj, B., Turk, B. & Turk, V. (1997) Equistatin, a new inhibitor of cysteine proteinases from Actinia equina, is structurally related to thyroglobulin type-1 domain. J. Biol. Chem. 272, 13899-13903.
17. Kornfeld, S. & Mellman, I. (1989) The biogenesis of lysosomes. Annu. Rev. Cell Biol. 5, 483-525.
18. Yeyeodu, S., Ahn, K., Madden, V., Chapman, R., Song, L. & Erickson, A. (2000) Procathepsin L self-association as a mechanism for selective secretion. Traffic 1, 724-737.
19. Ahn, K., Yeyeodu, S., Collette, J., Maden, V., Arthur, J., Li, L. & Erickson, A.H. (2002) An alternate targeting pathway for procathepsin L in mouse fibroblasts. Traffic 3, 147-159.
20. Andrews, N.W. (2000) Regulated secretion of conventional lysosomes. Trends Cell Biol. 10, 316-320.
21. Blott, E.J. & Griffiths, G.M. (2002) Secretory lysosomes. Nat. Rev. Mol. Cell Biol. 3, 122-131.
22. Chapman, H., Riese, R.J. & Shi, G.-P. (1997) Emerging roles for cysteine proteases in human biology. Annu. Rev. Physiol. 59, 63-88.
23. Ishidoh, K. & Kominami, E. (1998) Gene regulation and extracellular functions of procathepsin L. Biol. Chem. 379, 131-135.
24. Turk, B., Turk, D. & Turk, V. (2000) Lysosomal cysteine proteases: more than scavengers. Biochim. Biophys. Acta. 1477, 98-111.
25. Kane, S.E. & Gottesman, M.M. (1990) The role of cathepsin L in malignant transformation. Sem. Cancer Biol. 1, 127-136.
26. Briozzo, P., Morisset, M., Capony, F., Rougeot, C. & Rochefort, H. (1988) In vitro degradation of extracellular matrix with Mr 52,000 cathepsin D secreted by breast cancer cells. Cancer Res. 48, 3688-3692.
27. Ishidoh, K. & Kominami, E. (1995) Procathepsin L degrades extracellular matrix proteins in the presence of glycosaminoglycans in vitro. Biochem. Biophys. Res. Comm. 217, 624-631.
28. Maciewicz, R.A., Etherington, D.J., Kos, J. & Turk, V. (1987) Collagenolytic cathepsins of rabbit spleen: a kinetic analysis of collagen degradation and inhibition by chicken cystatin. Collagen Relat. Res. 7, 295-304.
29. Mason, R.W., Johnson D.A., Barrett, A.J. & Chapman, H.A. (1986) Elastinolytic activity of human cathepsin L. Biochem. J. 233, 925-927.
30. Buck, M.R., Karustis, D.G., Day, N.A., Honn, K.V. & Sloane, B.F. (1992) Degradation of extracellular-matrix proteins by human cathepsin B from normal and tumour tissues. Biochem. J. 282, 273-278.
31. Barrett, A.J. & Kirschke, H. (1981) Cathepsin B, cathepsin H, and cathepsin L. Methods Enzymol. 80, 535-561.
32. Bieth, J.G. (1995) Theoretical and practical aspects of protease inhibition kinetics. Methods Enzymol. 248, 59-84.
33. Bieth, J.G. (1984) In vivo significance of kinetic constants of protein proteinase inhibitors. Biochem. Med. 32, 387-397.
34. Segel, I.H. (1975) Enzyme Kinetics. John Wiley & Sons, New York.
35. Kirschke, H., Barrett, A.J. & Rawlings, N.D. (1998) Lysosomal Cysteine Proteases. 2nd edn. Oxford University Press, Oxford.
36. Bevec, T., Stoka, V., Pungercic, G., Dolenc, I. & Turk, V. (1996) Major histocompatibility complex class II-associated p41 invariant chain fragment is a strong inhibitor of lysosomal cathepsin L. J. Exp. Med. 183, 1331-1338.
37. Dehrmann, F.M., Coetzer, T.H.T., Pike, R.N. & Dennison, C. (1995) Mature cathepsin L is substantially active in the ionic milieu of the extracellular medium. Arch. Biochem. Biophys. 324, 93-98.
38. Mason, R.W., Green, G.D.J. & Barrett, A.J. (1985) Human liver cathepsin L. Biochem. J. 226, 233-241.
39. Barrett, A.J., Rawlings, N.D., Davies, M.E., Machleidt, W., Salvesen, G. & Turk, V. (1986) Cysteine proteinase inhibitors of the cystatin superfamily. In Proteinase Inhibitors (Barrett, A.J. & Salvesen, G., eds), pp. 515-569. Elsevier, Amsterdam.
40. Trexler, M., Banyai, L. & Patthy, L. (2001) A human protein containing multiple types of protease-inhibitory modules. Proc. Natl. Acad. Sci. USA 98, 3705-3709.
41. Trexler, M., Banyai, L. & Patthy, L. (2002) Distinct expression pattern of two related human proteins containing multiple types of protease-inhibitory modules. Biol. Chem, 383, 223-228.
42. Nagy, A., Trexler, M. & Patthy, L. (2003) Expression, purification and characterization of the second Kunitz-type protease inhibitor domain of the human WFIKKN protein. Eur. J. Biochem. 270, 2101-2107.
43. Lenarcic, B., Krizaj, I., Zunec, P. & Turk, V. (1996) Differences in specificity for the interactions of stefins A, B and D with cysteine proteinases. FEBS Lett. 395, 113-118.
44. Stark, M., Danielsson, O., Griffiths, W.J., Jornvall, H. & Johansson, J. (2001) Peptide repertoire of human cerebrospinal fluid: novel proteoglytic fragments of neuroendocrine proteins. J. Chromatog. B. 754, 357-367.
45. BaSalamah, M.A., Marr, H.S., Duncan, A.W. & Edgell, C.J. (2001) Testican in human blood. Biochem. Biophys. Res. Comm. 283, 1083-1090.
46. Gottesman, M.M. (1978) Transformation-dependent secretion of a low molecular weight protein by murine fibroblasts. Proc. Natl Acad. Sci. USA 75, 2767-2771.
47. Prence, E.M., Dong, J. & Sahagian, G.G. (1990) Modulation of the transport of a lysosomal enzyme by PDGF. J. Cell Biol. 110, 319-326.
48. Erickson-Lawrence, M., Zabludoff, S.D. & Wright, W.W. (1991) Cyclic protein-2, a secretory product of rat Sertoli cells, is the proenzyme form of cathepsin L. Mol. Endocrinol. 5, 1789-1798.
49. Jaffe, R.C., Donnelly, K.M., Mavrogianis, P.A. & Verhage, H.G. (1989) Molecular cloning and characterization of a progesterone-dependent cat endometrial secretory protein complementary deoxyribonucleic acid. Mol. Endocrinol. 3, 1807-1814.
50. Lennon-Dumenil, A.-M., Bryant, A.R., Valentijn, K., Driessen, C., Overkleeft, H.S., Erickson, A., Peters, P.J., Bikoff, E., Ploegh, H.L. & Bryant, P.W. (2001) The p41 isoform of invariant chain is a chaperone for cathepsin L. EMBO J. 29, 4055-4064.
51. Fineschi, B., Arneson, L.S., Naujokas, M.F. & Miller, J. (1995) Proteolysis of major histocompatibility complex class II-associated invariant chain is regulated by the alternatively spliced gene product, p41. Proc. Natl Acad. Sci. USA 92, 10257-10261.
52. Fiebiger, E., Maehr, R., Villadangos, J., Weber, E., Erickson, A.H., Bikoff, E., Ploegh, H.L. & Lennon-Dumenil, A.-M. (2002) Invariant chain controls the activity of extracellular cathepsin L. J. Exp. Med. 196, 1263-1270.
53. Almeida, P.C., Nantes, I.L., Chagas, J.R., Rizza, C.C., Faljoini-Alario, A., Carmona, E., Juliano, L., Nader, H.B. & Tersariol, I.L. (2001) Cathepsin B activity regulation. Heparin-like glycosaminoglycans protect human cathepsin B from alkaline pH-induced activation. J. Biol. Chem. 276, 944-951.
54. Kainulainen, V., Wang, H., Schick, C. & Bernfield, M. (1998) Syndecans, heparan sulfate proteoglycans, maintain the proteolyric balance of acute wound fluids. J. Biol. Chem. 273, 11563-11569.
55. Hohenester, E., Maurer, P. & Timpl, R. (1997) Crystal structure of a pair of follistatin-like and EF-hand calcium-binding domains in BM-40. EMBO J. 16, 3778-3786.