HaCaT keratinocytes secrete lysosomal cysteine proteinases during migration

European Journal of Cell Biology

Volumn 83, Issue 11-12, 2004, Pages 781-795

  Büth, Heiko ^a   Wolters, Brit ^a   Hartwig, Benedikt ^b   Meier Bornheim, Roland ^c   Veith, Henrike ^a   Hansen, Maren ^d   Sommerhoff, Christian P ^e   Schaschke, Norbert ^f   Machleidt, Werner ^g   Fusenig, Norbert E ^d   Boukamp, Petra ^d   Brix, Klaudia ^a  

^a JACOBS UNIVERSITY BREMEN   (Germany)

^b UNIVERSITY OF COLOGNE   (Germany)

^c UNIVERSITY OF BONN   (Germany)

^d GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^e LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^f MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^g UNIVERSITY OF MUNICH   (Germany)

Author keywords

Cathepsins; Extracellular proteolysis; Keratinocytes; Migration; Secretion

Indexed keywords

CATHEPSIN B; CYSTEINE PROTEINASE; LACTATE DEHYDROGENASE; LYSOSOME ENZYME;

ARTICLE; CELL CULTURE; CELL LINE; CELL MIGRATION; CONTROLLED STUDY; CYTOCHEMISTRY; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; HUMAN TISSUE; KERATINOCYTE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN SECRETION; UPREGULATION; WOUND HEALING;

EID: 19944429298     PISSN: 01719335     EISSN: None     Source Type: Journal    
DOI: 10.1078/0171-9335-00428     Document Type: Article

References (67)

1. Airola, K., Fusenig, N. E., 2001. Differential stromal regulation of MMP-1 expression in benign and malignant keratinocytes. J. Invest. Dermatol. 116, 85-92.
2. Bailey, A. J., 2000. Perspective article: the fate of collagen implants in tissue defects. Wound Repair Regen. 8, 5-12.
3. Bajou, K., Masson, V., Gerard, R. D., Schmitt, P. M., Albert, V., Praus, M., Lund, L. R., Frandsen, T. L., Brunner, N., Dano, K., Fusenig, N. E., Weidle, U., Carmeliet, G., Loskutoff, D., Collen, D., Carmeliet, P., Foidart, J. M., Noel, A., 2001. The plasminogen activator inhibitor PAI-1 controls in vivo tumor vascularization by interaction with proteases, not vitronectin. Implications for antiangiogenic strategies. J. Cell Biol. 152, 777-784.
4. Bernard, D., Mehul, B., Thomas-Collignon, A., Simonetti, L., Remy, V., Bernard, M. A., Schmidt, R., 2003. Analysis of proteins with caseinolytic activity in a human stratum corneum extract revealed a yet unidentified cysteine protease and identified the so-called "stratum corneum thiol protease" as cathepsin L2. J. Invest. Dermatol. 120, 592-600.
5. Boukamp, P., Petrussevska, R. T., Breitkreutz, D., Hornung, J., Markham, A., Fusenig, N. E., 1988. Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J. Cell Biol. 106, 761-771.
6. Bradford, M. M., 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
7. Brix, K., Lemansky, L., Herzog, V., 1996. Evidence for extracellularly acting cathepsins mediating thyroid hormone liberation in thyroid epithelial cells. Endocrinology 137, 1963-1974.
8. Brix, K., Linke M., Tepel, C., Herzog, V., 2001. Cysteine proteinases mediate extracellular prohormone processing in the thyroid. Biol. Chem. 382, 717-725.
9. Burk, R. R., 1973. A factor from a transformed cell line that affects cell migration. Proc. Natl. Acad. Sci. USA 70, 369-372.
10. Burton, K. A., 1956. Study of the conditions and mechanism of the diphenylamine reaction for the colorimetric estimation of deoxy-ribonucleic acid. Biochem. J. 62, 315-323.
11. Cavallo-Medved, D., Dosescu, J., Linebaugh, B. E., Sameni, M., Rudy, D., Sloane, B. F., 2003. Mutant K-ras regulates cathepsin B localization on the surface of human colorectal carcinoma cells. Neoplasia 5, 507-519.
12. Chapman, H. A., Riese, R. J., Shi, G. P., 1997. Emerging roles for cysteine proteases in human biology. Annu. Rev. Physiol. 59, 63-88.
13. Creemers, L. B., Jansen, I. D., Docherty, A. J., Reynolds, J. J., Beertsen, W., Everts, V., 1998. Gelatinase A (MMP-2) and cysteine proteinases are essential for the degradation of collagen in soft connective tissue. Matrix Biol. 17, 35-46.
14. Doering, T., Proia, R. L., Sandhoff, K., 1999. Accumulation of protein-bound epidermal glucosylceramides in beta- glucocerebrosidase deficient type 2 Gaucher mice. FEBS Lett. 447, 167-170.
15. Felbor, U., Dreier, L., Bryant, R. A., Ploegh, H. L., Olsen, B. R., Mothes, W., 2000. Secreted cathepsin L generates endostatin from collagen XVIII. EMBO J. 19, 1187-1194.
16. Franzke, C. W., Baici, A., Bartels, J., Christophers, E., Wiedow, O., 1996. Antileukoprotease inhibits stratum corneum chymotryptic enzyme. Evidence for a regulative function in desquamation. J. Biol. Chem. 271, 21886-21890.
17. Friedrichs, B., Tepel, C., Reinheckel, T., Deussing, J., von Figura, K., Herzog, V., Peters, C., Saftig, P., Brix, K., 2003. Thyroid functions of mouse cathepsins B, K, and L. J. Clin. Invest. 111, 1733-1745.
18. Fuchs, E., Raghavan, S., 2002. Getting under the skin of epidermal morphogenesis. Nat. Rev. Genet. 3, 199-209.
19. Gagnoux-Palacios, L., Allegra, M., Spirito, F., Pommeret, O., Romero, C., Ortonne, J. P., Meneguzzi, G., 2001. The short arm of the laminin gamma2 chain plays a pivotal role in the incorporation of laminin 5 into the extracellular matrix and in cell adhesion. J. Cell Biol. 153, 835-849.
20. Gao, X., Devoe, L. D., Given, K. S., 1994. Effects of amniotic fluid on proteases: a possible role of amniotic fluid in fetal wound healing. Ann. Plast. Surg. 33, 128-134; discussion 134- 135.
21. Goldberg, G. I., Frisch, S. M., He, C., Wilhelm, S. M., Reich, R., Collier, I. E., 1990. Secreted proteases. Regulation of their activity and their possible role in metastasis. Ann. N. Y. Acad. Sci. 580, 375-384.
22. Goldfinger, L. E., Stack, M. S., Jones, J. C., 1998. Processing of laminin-5 and its functional consequences: role of plasmin and tissue-type plasminogen activator. J. Cell Biol. 141, 255-265.
23. Goldmann, T., Suter, L., Ribbert, D., Otto, F., 1999. The expression of proteolytic enzymes at the dermal invading front of primary cutaneous melanoma predicts metastasis. Pathol. Res. Pract. 195, 171-175.
24. Greenbaum, D., Medzihradszky, K. F., Burlingame, A., Bogyo, M., 2000. Epoxide electrophiles as activity-dependent cysteine protease profiling and discovery tools. Chem. Biol. 7, 569-581.
25. Guo, M., Mathieu, P. A., Linebaugh, B., Sloane, B. F., Reiners, Jr., J. J., 2002. Phorbol ester activation of a proteolytic cascade capable of activating latent transforming growth factor-betaL a process initiated by the exocytosis of cathepsin B. J. Biol. Chem. 277, 14829-14837.
26. Hackam, D. J., Ford, H. R., 2002. Cellular, biochemical, and clinical aspects of wound healing. Surg. Infect. (Larchmt.) 3, S23-S35.
27. Kahari, V. M., Saarialho-Kere, U., 1997. Matrix metalloproteinases in skin. Exp. Dermatol. 6, 199-213.
28. Katz, A. B., Taichman, L. B., 1999. A partial catalog of proteins secreted by epidermal keratinocytes in culture. J. Invest. Dermatol. 112, 818-821.
29. Kawada, A., Hara, K., Kominami, E., Hiruma, M., Akiyama M., Ishibashi, A., Abe, H., Ichikawa, E., Nakamura, Y., Watanabe, S., Yamamoto, T., Umeda, T., Nishioka K., 1997. Expression of cathepsin D and B in invasion and metastasis of squamous cell carcinoma. Br. J. Dermatol. 137, 361-366.
30. Keppler, D., Sameni, M., Moin, K., Mikkelsen, T., Diglio, C. A., Sloane, B. F., 1996. Tumor progression and angiogenesis: cathepsin B & Co. Biochem. Cell Biol. 74, 799-810.
31. Kostoulas, G., Lang, A., Nagase, H., Baici, A., 1999. Stimulation of angiogenesis through cathepsin B inactivation of the tissue inhibitors of matrix metalloproteinases. FEBS Lett. 455, 286-290.
32. Kramer, M. D., Reinartz, J., Brunner, G., Schirrmacher, V., 1994. Plasmin in pericellular proteolysis and cellular invasion. Invasion Metastasis 14, 210-222.
33. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
34. Linke, M., Herzog, V., Brix, K., 2002. Trafficking of lysosomal cathepsin B-green flourescent protein to the surface of thyroid epithelial cells involves the endosomal/lysosomal compartment. J. Cell Sci. 115, 4877-4889.
35. Lipton, A., Klinger, I., Paul, D., Holley, R. W., 1971. Migration of mouse 3T3 fibroblasts in response to a serum factor. Proc. Natl. Acad. Sci. USA 68, 2799-2801.
36. Lukomski, S., Montgomery., C. A., Rurangirwa, J., Geske, R. S., Barrish, J. P., Adams, G. J., Musser, J. M., 1999. Extracellular cysteine protease produced by Streptococcus pyogenes participates in the pathogenesis of invasive skin infection and dissemination in mice. Infect. Immun. 67, 1779-1788.
37. Mach, L., Stüwe, K., Hagen, A., Ballaun, C., Glössl, J., 1992. Proteolytic processing and glycosylation of cathepsin B. The role of the primary structure of the latent precursor and of the carbohydrate moiety for cell-type-specific molecular forms of the enzyme. Biochem. J. 282, 577-582.
38. Madlener, M., Parks, W. C., Werner, S., 1998. Matrix metalloproteinases (MMPs) and their physiological inhibitors (TIMPs) are differentially expressed during excisional skin wound repair. Exp. Cell Res. 242, 201-210.
39. Mai, J., Finley, R. L., Jr., Waisman, D. M., Sloane. B. F., 2000. Human procathepsin B interacts with the annexin II tetramer on the surface of tumor cells. J. Biol. Chem. 275, 12806-12812.
40. Martin, P., 1997. Wound healing - aiming for perfect skin regeneration. Science 276, 75-81.
41. Menon, G. K., Ghadially, R., Williams, M. L., Elias, P. M., 1992. Lamellar bodies as delivery systems of hydrolytic enzymes: implications for normal and abnormal desquamation. Br. J. Dermatol. 126, 337-345.
42. Mignatti, P., Rifkin, D. B., Welgus, H. G., Parks, W. C., 1996. Proteinases and Tissue Remodeling, in: Clark, R. A. F. (Ed.), The molecular and Cellular Biology of Wound Repair. Plenum Press, New York, 2nd ed., pp. 427-474.
43. Mort, J. S., Buttle, D. J., 1997. Cathepsin B. Int. J. Biochem. Cell Biol. 29, 715-720.
44. Mort, J. S., Magny, M. C., Lee, E. R., 1998. Cathepsin B: an alternative protease for the generation of an aggrecan 'metalloproteinase' cleavage neoepitope. Biochem. J. 335, 491-494.
45. Mueller, M. M., Fusenig, N. E., 2002. Tumor-stroma interactions directing phenotype and progression of epithelial skin tumor cells. Differentiation 70, 486-497.
46. Murphy, G., Gavrilovic, J., 1999. Proteolysis and cell migration: creating a path? Curr. Opin. Cell Biol. 11, 614-621.
47. O'Toole, E. A., 2001. Extracellular matrix and keratinocyte migration. Clin. Exp. Dermatol. 26, 525-530.
48. Quiec, D., Maziere, C., Auclair, M., Santus, R., Gardette, J., Redziniak, G., Franchi, J., Dubertret, L., Maziere, J. C., 1995. Lovastatin enhances the photocytotoxicity of UVA radiation towards cultured N.C.T.C. 2544 human keratinocytes: prevention by cholesterol supplementation and by a cathepsin inhibitor. Biochem. J. 310, 305-309.
49. Ravanti, L., Kahari, V. M. 2000. Matrix metalloproteinases in wound repair (review). Int. J. Mol. Med. 6, 391-407.
50. Saarialho-Kere, U. K., 1998. Patterns of matrix metalloproteinase and TIMP expression in chronic ulcers. Arch. Dermatol. Res. 290, S47-S54.
51. Schaschke, N., Assfalg-Machleidt, I., Machleidt, W., Moroder, L., 1998. Substrate/propeptide-derived endo-epoxysuccinyl peptides as highly potent and selective cathepsin B inhibitors. FEBS Lett. 421, 80-82.
52. Schaschke, N., Assfalg-Machleidt, I., Lassleben, T., Sommerhoff, C. P., Moroder, L., Machleidt, W., 2000. Epoxysuccinyl peptide-derived affinity labels for cathepsin B. FEBS Lett. 482, 91-96.
53. Schlagenhauff, B., Klessen, C., Teichmann-Dorr, S., Breuninger, H., Rassner, G., 1992. Demonstration of proteases in basal cell carcinomas. A histochemical study using amino acid-4-methoxy-2-naphthylamides as chromogenic substrates. Cancer. 70, 1133-1140.
54. Singer, A. J., Clark, R. A.F., 1999. Cutaneous wound healing. New Engl. J. Med. 341, 738-746.
55. Sloanem, B. F., Moin, K., Krepela, E., Rozhin, J., 1990. Cathepsin B and its endogenous inhibitors: the role in tumor malignancy. Cancer Metas. Rev. 9, 333-352.
56. Stamenkovic, I., 2003. Extracellular matrix remodelling: the role of matrix metalloproteinases. J. Pathol. 200. 448-464.
57. Szabowski, A., Maas-Szabowski, N., Andrecht, S., Kolbus, A., Schorpp-Kistner, M., Fusenig, N. E., Angel, P., 2000. c-Jun and JunB antagonistically control cytokine-regulated mesenchymal-epidermal interaction in skin. Cell 103, 745-755.
58. Thomas, P. S., Farquhar, M. N., 1978. Sepcific measurement of DNA in nuclei and nucleic acids using diaminobenzoic acid. Anal. Biochem. 89, 35-44.
59. Turk, V., Turk, B., Turk, D., 2001. Lysosomal cysteine proteases: facts and opportunities. EMBO J. 20, 4629-4633.
60. van Kley, H., Hale, S. M., 1977. Assay for protein by dye binding. Anal. Biochem. 81, 485-487.
61. Varani, J., Burmeister, B., Sitrin, R. G., Shollenberger, S. B., Inman, D. R., Fligiel, S. E., Gibbs, D. F., Johnson, K., 1994. Expression of serine proteinases and metalloproteinases in organ-cultured human skin. Altered levels in the presence of retinoic acid and possible relationship to retinoid-induced loss of epidermal cohesion. Am. J. Pathol. 145, 561-573.
62. von Figura, K., 1991. Molecular recognition and targeting of lysosomal proteins. Curr. Opin. Cell Biol. 3, 642-646.
63. von Figura, K., Hasilik, A., 1986. Lysosomal enzymes and their receptors. Annu. Rev. Biochem. 55, 167-193.
64. Watkinson, A., 1999. Stratum corneum thiol protease (SCTP): a novel cysteine protease of late epidermal differentiation. Arch. Dermatol. Res. 291, 260-268.
65. Werner, S., Smola, H., 2001. Paracrine regulation of keratinocyte proliferation and differentiation. Trends Cell Biol. 11, 143-146.
66. Zatterstrom, U. K., Felbor, U., Fukai, N., Olsen, B. R., 2000. Collagen XVIII/endostatin structure and functional role in angiogenesis. Cell Struct. Funct. 25, 97-101.
67. Zhang, K., Kramer, R. H., 1996. Laminin 5 deposition promotes keratinocyte motility. Exp. Cell Res. 227, 309-322.