Pathophysiological functions of cathepsin D: Targeting its catalytic activity versus its protein binding activity?

Biochimie

Volumn 92, Issue 11, 2010, Pages 1635-1643

  Masson, Olivier ^a,b,c   Bach, Anne Sophie ^a,b,c   Derocq, Danielle ^a,b,c   Prébois, Christine ^a,b,c   Laurent Matha, Valérie ^a,b,c   Pattingre, Sophie ^a,b,c   Liaudet Coopman, Emmanuelle ^a,b,c  

^a INSTITUT DE RECHERCHE EN CANCÉROLOGIE DE MONTPELLIER   (France)

^b UNIV MONTPELLIER   (France)

^c CENTRE VAL D AURELLE   (France)

Author keywords

Apoptosis; Cancer; Cathepsin D; Proliferation; Protease

Indexed keywords

ANTINEOPLASTIC AGENT; BIOLOGICAL MARKER; CATHEPSIN D; CATHEPSIN D INHIBITOR; ENZYME INHIBITOR; PEPSTATIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; BREAST CANCER; CANCER CHEMOTHERAPY; CANCER GROWTH; CANCER SURVIVAL; CELL ACTIVITY; CELL DEATH; CELL INTERACTION; DEGENERATIVE DISEASE; DISEASE MARKER; DRUG EFFECT; DRUG STRUCTURE; DRUG TARGETING; ENDOCYTOSIS; ENZYME ACTIVITY; ENZYME BINDING; ENZYME INHIBITOR INTERACTION; ENZYME LOCALIZATION; ENZYME MECHANISM; ENZYME SUBSTRATE; FETUS DEVELOPMENT; FETUS DISEASE; HEART FAILURE; HUMAN; KNOCKOUT MOUSE; METASTASIS; NONHUMAN; PATHOGENESIS; PATHOPHYSIOLOGY; PH; PLANT LEAF; PROGNOSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEOMICS; REVIEW; TOMATO; TUMOR MICROENVIRONMENT;

ANIMALS; APOPTOSIS; BIOCATALYSIS; CATHEPSIN D; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; NEOPLASMS; PROTEIN BINDING;

EID: 77958546273     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2010.05.009     Document Type: Review

References (169)

1. Smith H.W., Marshall C.J. Regulation of cell signalling by uPAR. Nat. Rev. Mol. Cell Biol. 2010, 11:23-36.
2. Roy R., Yang J., Moses M.A. Matrix metalloproteinases as novel biomarkers and potential therapeutic targets in human cancer. J. Clin. Oncol. 2009, 27:5287-5297.
3. Palermo C., Joyce J.A. Cysteine cathepsin proteases as pharmacological targets in cancer. Trends Pharmacol. Sci. 2008, 29:22-28.
4. Liaudet-Coopman E., Beaujouin M., Derocq D., Garcia M., Glondu-Lassis M., Laurent-Matha V., Prebois C., Rochefort H., Vignon F. Cathepsin D: newly discovered functions of a long-standing aspartic protease in cancer and apoptosis. Cancer Lett. 2006, 237:167-179.
5. Mohamed M.M., Sloane B.F. Cysteine cathepsins: multifunctional enzymes in cancer. Nat. Rev. Cancer 2006, 6:764-775.
6. Koblinski J.E., Dosescu J., Sameni M., Moin K., Clark K., Sloane B.F. Interaction of human breast fibroblasts with collagen I increases secretion of procathepsin B. J. Biol. Chem. 2002, 277:32220-32227.
7. Joyce J.A., Baruch A., Chehade K., Meyer-Morse N., Giraudo E., Tsai F.Y., Greenbaum D.C., Hager J.H., Bogyo M., Hanahan D. Cathepsin cysteine proteases are effectors of invasive growth and angiogenesis during multistage tumorigenesis. Cancer Cell 2004, 5:443-453.
8. Joyce J.A., Hanahan D. Multiple roles for cysteine cathepsins in cancer. Cell Cycle 2004, 3:1516-1619.
9. Gocheva V., Joyce J.A. Cysteine cathepsins and the cutting edge of cancer invasion. Cell Cycle 2007, 6:60-64.
10. Gocheva V., Zeng W., Ke D., Klimstra D., Reinheckel T., Peters C., Hanahan D., Joyce J.A. Distinct roles for cysteine cathepsin genes in multistage tumorigenesis. Genes Dev. 2006, 20:543-556.
11. Ivanova S., Repnik U., Bojic L., Petelin A., Turk V., Turk B. Lysosomes in apoptosis. Methods Enzymol. 2008, 442:183-199.
12. Chapman H.A. Cathepsins as transcriptional activators?. Dev. Cell 2004, 6:610-611.
13. Mueller M.M., Fusenig N.E. Tumor-stroma interactions directing phenotype and progression of epithelial skin tumor cells. Differentiation 2002, 70:486-497.
14. Affara N.I., Andreu P., Coussens L.M. Delineating protease functions during cancer development. Methods Mol. Biol. 2009, 539:1-32.
15. Cudic M., Fields G.B. Extracellular proteases as targets for drug development. Curr. Protein Pept. Sci. 2009, 10:297-307.
16. Augereau P., Garcia M., Mattei M.G., Cavailles V., Depadova F., Derocq D., Capony F., Ferrara P., Rochefort H. Cloning and sequencing of the 52K cathepsin D complementary deoxyribonucleic acid of MCF7 breast cancer cells and mapping on chromosome 11. Mol. Endocrinol. 1988, 2:186-192.
17. Samarel A.M., Ferguson A.G., Decker R.S., Lesch M. Effects of cysteine protease inhibitors on rabbit cathepsin D maturation. Am. J. Physiol. 1989, 257:C1069-C1079.
18. Gieselmann V., Hasilik A., von Figura K. Processing of human cathepsin D in lysosomes in vitro. J. Biol. Chem. 1985, 260:3215-3220.
19. Laurent-Matha V., Derocq D., Prebois C., Katunuma N., Liaudet-Coopman E. Processing of human cathepsin D is independent of its catalytic function and auto-activation: involvement of cathepsins L and B. J. Biochem. 2006, 139:363-371.
20. Felbor U., Kessler B., Mothes W., Goebel H.H., Ploegh H.L., Bronson R.T., Olsen B.R. Neuronal loss and brain atrophy in mice lacking cathepsins B and L. Proc. Natl. Acad. Sci. U S A 2002, 99:7883-7888.
21. Wille A., Gerber A., Heimburg A., Reisenauer A., Peters C., Saftig P., Reinheckel T., Welte T., Buhling F. Cathepsin L is involved in cathepsin D processing and regulation of apoptosis in A549 human lung epithelial cells. Biol. Chem. 2004, 385:665-670.
22. Metcalf P., Fusek M. Two crystal structures for cathepsin D: the lysosomal targeting signal and active site. EMBO J. 1993, 12:1293-1302.
23. Baldwin E.T., Bhat T.N., Gulnik S., Hosur M.V., Sowder R.C., Cachau R.E., Collins J., Silva A.M., Erickson J.W. Crystal structures of native and inhibited forms of human cathepsin D: implications for lysosomal targeting and drug design. Proc. Natl. Acad. Sci. U S A 1993, 90:6796-6800.
24. Goldfarb N.E., Lam M.T., Bose A.K., Patel A.M., Duckworth A.J., Dunn B.M. Electrostatic switches that mediate the pH-dependent conformational change of "short" recombinant human pseudocathepsin D. Biochemistry 2005, 44:15725-15733.
25. Lee A.Y., Gulnik S.V., Erickson J.W. Conformational switching in an aspartic proteinase. Nat. Struct. Biol. 1998, 5:866-871.
26. Cavailles V., Augereau P., Garcia M., Rochefort H. Estrogens and growth factors induce the mRNA of the 52K-pro-cathepsin-D secreted by breast cancer cells. Nucleic Acids Res. 1988, 16:1903-1919.
27. Giamarchi C., Solanas M., Chailleux C., Augereau P., Vignon F., Rochefort H., Richard-Foy H. Chromatin structure of the regulatory regions of pS2 and cathepsin D genes in hormone-dependent and -independent breast cancer cell lines. Oncogene 1999, 18:533-541.
28. Capony F., Rougeot C., Montcourrier P., Cavailles V., Salazar G., Rochefort H. Increased secretion, altered processing, and glycosylation of pro-cathepsin D in human mammary cancer cells. Cancer Res. 1989, 49:3904-3909.
29. Castino R., Delpal S., Bouguyon E., Demoz M., Isidoro C., Ollivier-Bousquet M. Prolactin promotes the secretion of active cathepsin D at the basal side of rat mammary acini. Endocrinology 2008, 149:4095-4105.
30. Laurent-Matha V., Farnoud M.R., Lucas A., Rougeot C., Garcia M., Rochefort H. Endocytosis of pro-cathepsin D into breast cancer cells is mostly independent of mannose-6-phosphate receptors. J. Cell Sci. 1998, 111(Pt 17):2539-2549.
31. Capony F., Braulke T., Rougeot C., Roux S., Montcourrier P., Rochefort H. Specific mannose-6-phosphate receptor-independent sorting of pro-cathepsin D in breast cancer cells. Exp. Cell Res. 1994, 215:154-163.
32. Laurent-Matha V., Lucas A., Huttler S., Sandhoff K., Garcia M., Rochefort H. Procathepsin D interacts with prosaposin in cancer cells but its internalization is not mediated by LDL receptor-related protein. Exp. Cell Res. 2002, 277:210-219.
33. Canuel M., Korkidakis A., Konnyu K., Morales C.R. Sortilin mediates the lysosomal targeting of cathepsins D and H. Biochem. Biophys. Res. Commun. 2008, 373:292-297.
34. Kageyama T., Tatematsu M., Ichinose M., Yahagi N., Miki K., Moriyama A., Yonezawa S. Development-dependent expression of cathepsins d and e in various rat tissues, with special reference to the high expression of cathepsin e in fetal liver. Zoolog. Sci. 1998, 15:517-523.
35. Saftig P., Hetman M., Schmahl W., Weber K., Heine L., Mossmann H., Koster A., Hess B., Evers M., von Figura K., et al. Mice deficient for the lysosomal proteinase cathepsin D exhibit progressive atrophy of the intestinal mucosa and profound destruction of lymphoid cells. EMBO J. 1995, 14:3599-3608.
36. Koike M., Nakanishi H., Saftig P., Ezaki J., Isahara K., Ohsawa Y., Schulz-Schaeffer W., Watanabe T., Waguri S., Kametaka S., Shibata M., Yamamoto K., Kominami E., Peters C., von Figura K., Uchiyama Y. Cathepsin D deficiency induces lysosomal storage with ceroid lipofuscin in mouse CNS neurons. J. Neurosci. 2000, 20:6898-6906.
37. Koike M., Shibata M., Ohsawa Y., Nakanishi H., Koga T., Kametaka S., Waguri S., Momoi T., Kominami E., Peters C., Figura K., Saftig P., Uchiyama Y. Involvement of two different cell death pathways in retinal atrophy of cathepsin D-deficient mice. Mol. Cell Neurosci. 2003, 22:146-161.
38. Walls K.C., Klocke B.J., Saftig P., Shibata M., Uchiyama Y., Roth K.A., Shacka J.J. Altered regulation of phosphatidylinositol 3-kinase signaling in cathepsin D-deficient brain. Autophagy 2007, 3:222-229.
39. Myllykangas L., Tyynela J., Page-McCaw A., Rubin G.M., Haltia M.J., Feany M.B. Cathepsin D-deficient Drosophila recapitulate the key features of neuronal ceroid lipofuscinoses. Neurobiol. Dis. 2005, 19:194-199.
40. Tyynela J., Sohar I., Sleat D.E., Gin R.M., Donnelly R.J., Baumann M., Haltia M., Lobel P. A mutation in the ovine cathepsin D gene causes a congenital lysosomal storage disease with profound neurodegeneration. EMBO J. 2000, 19:2786-2792.
41. Awano T., Katz M.L., O'Brien D.P., Taylor J.F., Evans J., Khan S., Sohar I., Lobel P., Johnson G.S. A mutation in the cathepsin D gene (CTSD) in American Bulldogs with neuronal ceroid lipofuscinosis. Mol. Genet. Metab. 2006, 87:341-348.
42. Siintola E., Partanen S., Stromme P., Haapanen A., Haltia M., Maehlen J., Lehesjoki A.E., Tyynela J. Cathepsin D deficiency underlies congenital human neuronal ceroid-lipofuscinosis. Brain 2006, 129:1438-1445.
43. Steinfeld R., Reinhardt K., Schreiber K., Hillebrand M., Kraetzner R., Bruck W., Saftig P., Gartner J. Cathepsin D deficiency is associated with a human neurodegenerative disorder. Am. J. Hum. Genet. 2006, 78:988-998.
44. Tyynela J., Sohar I., Sleat D.E., Gin R.M., Donnelly R.J., Baumann M., Haltia M., Lobel P. Congenital ovine neuronal ceroid lipofuscinosis-a cathepsin D deficiency with increased levels of the inactive enzyme. Eur. J. Paediatr. Neurol. 2001, 5(Suppl. A):43-45.
45. Fritchie K., Siintola E., Armao D., Lehesjoki A.E., Marino T., Powell C., Tennison M., Booker J.M., Koch S., Partanen S., Suzuki K., Tyynela J., Thorne L.B. Novel mutation and the first prenatal screening of cathepsin D deficiency (CLN10). Acta Neuropathol. 2009, 117:201-208.
46. Cullen V., Lindfors M., Ng J., Paetau A., Swinton E., Kolodziej P., Boston H., Saftig P., Woulfe J., Feany M.B., Myllykangas L., Schlossmacher M.G., Tyynela J. Cathepsin D expression level affects alpha-synuclein processing, aggregation, and toxicity in vivo. Mol. Brain 2009, 2:5.
47. Hilfiker-Kleiner D., Kaminski K., Podewski E., Bonda T., Schaefer A., Sliwa K., Forster O., Quint A., Landmesser U., Doerries C., Luchtefeld M., Poli V., Schneider M.D., Balligand J.L., Desjardins F., Ansari A., Struman I., Nguyen N.Q., Zschemisch N.H., Klein G., Heusch G., Schulz R., Hilfiker A., Drexler H. A cathepsin D-cleaved 16 kDa form of prolactin mediates postpartum cardiomyopathy. Cell 2007, 128:589-600.
48. Sheikh A.M., Li X., Wen G., Tauqeer Z., Brown W.T., Malik M. Cathepsin D and apoptosis related proteins are elevated in the brain of autistic subjects. Neuroscience 2010, 165:363-370.
49. Emert-Sedlak L., Shangary S., Rabinovitz A., Miranda M.B., Delach S.M., Johnson D.E. Involvement of cathepsin D in chemotherapy-induced cytochrome c release, caspase activation, and cell death. Mol. Cancer Ther. 2005, 4:733-742.
50. Vasiljeva O., Turk B. Dual contrasting roles of cysteine cathepsins in cancer progression: apoptosis versus tumour invasion. Biochimie 2008, 90:380-386.
51. Minarowska A., Minarowski L., Karwowska A., Gacko M. Regulatory role of cathepsin D in apoptosis. Folia Histochem. Cytobiol. 2007, 45:159-163.
52. Zuzarte-Luis V., Montero J.A., Torre-Perez N., Garcia-Porrero J.A., Hurle J.M. Cathepsin D gene expression outlines the areas of physiological cell death during embryonic development. Dev. Dyn. 2007, 236:880-885.
53. Berchem G., Glondu M., Gleizes M., Brouillet J.P., Vignon F., Garcia M., Liaudet-Coopman E. Cathepsin-D affects multiple tumor progression steps in vivo: proliferation, angiogenesis and apoptosis. Oncogene 2002, 21:5951-5955.
54. Sagulenko V., Muth D., Sagulenko E., Paffhausen T., Schwab M., Westermann F. Cathepsin D protects human neuroblastoma cells from doxorubicin-induced cell death. Carcinogenesis 2008, 29:1869-1877.
55. Deiss L.P., Galinka H., Berissi H., Cohen O., Kimchi A. Cathepsin D protease mediates programmed cell death induced by interferon-gamma, Fas/APO-1 and TNF-alpha. EMBO J. 1996, 15:3861-3870.
56. Ollinger K. Inhibition of cathepsin D prevents free-radical-induced apoptosis in rat cardiomyocytes. Arch. Biochem. Biophys. 2000, 373:346-351.
57. Kagedal K., Johansson U., Ollinger K. The lysosomal protease cathepsin D mediates apoptosis induced by oxidative stress. FASEB J. 2001, 15:1592-1594.
58. Roberg K., Ollinger K. Oxidative stress causes relocation of the lysosomal enzyme cathepsin D with ensuing apoptosis in neonatal rat cardiomyocytes. Am. J. Pathol. 1998, 152:1151-1156.
59. Takuma K., Kiriu M., Mori K., Lee E., Enomoto R., Baba A., Matsuda T. Roles of cathepsins in reperfusion-induced apoptosis in cultured astrocytes. Neurochem. Int. 2003, 42:153-159.
60. Johansson A.C., Steen H., Ollinger K., Roberg K. Cathepsin D mediates cytochrome c release and caspase activation in human fibroblast apoptosis induced by staurosporine. Cell Death Differ. 2003, 10:1253-1259.
61. Beaujouin M., Baghdiguian S., Glondu-Lassis M., Berchem G., Liaudet-Coopman E. Overexpression of both catalytically active and -inactive cathepsin D by cancer cells enhances apoptosis-dependent chemo-sensitivity. Oncogene 2006, 25:1967-1973.
62. Gan Y., Zhao X., Hu J., Wang Z.G., Zhao X.T. HCCS1 overexpression induces apoptosis via cathepsin D and intracellular calcium, and HCCS1 disruption in mice causes placental abnormality. Cell Death Differ. 2008, 15:1481-1490.
63. Miura Y., Sakurai Y., Hayakawa M., Shimada Y., Zempel H., Sato Y., Hisanaga S., Endo T. Translocation of lysosomal cathepsin D caused by oxidative stress or proteasome inhibition in primary cultured neurons and astrocytes. Biol. Pharm. Bull. 2010, 33:22-28.
64. Roberg K., Kagedal K., Ollinger K. Microinjection of cathepsin d induces caspase-dependent apoptosis in fibroblasts. Am. J. Pathol. 2002, 161:89-96.
65. Roberg K., Johansson U., Ollinger K. Lysosomal release of cathepsin D precedes relocation of cytochrome c and loss of mitochondrial transmembrane potential during apoptosis induced by oxidative stress. Free Radic. Biol. Med. 1999, 27:1228-1237.
66. Heinrich M., Neumeyer J., Jakob M., Hallas C., Tchikov V., Winoto-Morbach S., Wickel M., Schneider-Brachert W., Trauzold A., Hethke A., Schutze S. Cathepsin D links TNF-induced acid sphingomyelinase to Bid-mediated caspase-9 and -3 activation. Cell Death Differ. 2004, 11:550-563.
67. Blomgran R., Zheng L., Stendahl O. Cathepsin-cleaved Bid promotes apoptosis in human neutrophils via oxidative stress-induced lysosomal membrane permeabilization. J. Leukoc. Biol. 2007, 81:1213-1223.
68. Bidere N., Lorenzo H.K., Carmona S., Laforge M., Harper F., Dumont C., Senik A. Cathepsin D triggers Bax activation, resulting in selective apoptosis-inducing factor (AIF) relocation in T lymphocytes entering the early commitment phase to apoptosis. J. Biol. Chem. 2003, 278:31401-31411.
69. Conus S., Perozzo R., Reinheckel T., Peters C., Scapozza L., Yousefi S., Simon H.U. Caspase-8 is activated by cathepsin D initiating neutrophil apoptosis during the resolution of inflammation. J. Exp. Med. 2008, 205:685-698.
70. S. Zhao, E.R. Aviles, Jr., D.G. Fujikawa, Nuclear translocation of mitochondrial cytochrome c, lysosomal cathepsins B and D, and three other death-promoting proteins within the first 60 minutes of generalized seizures, J. Neurosci. Res., in press.
71. N. Grdovic, M. Vidakovic, M. Mihailovic, S. Dinic, A. Uskokovic, J. Arambasic, G. Poznanovic, Proteolytic events in cryonecrotic cell death: proteolytic activation of endonuclease P23, Cryobiology, in press.
72. Demoz M., Castino R., Cesaro P., Baccino F.M., Bonelli G., Isidoro C. Endosomal-lysosomal proteolysis mediates death signalling by TNFalpha, not by etoposide, in L929 fibrosarcoma cells: evidence for an active role of cathepsin D. Biol. Chem. 2002, 383:1237-1248.
73. Shibata M., Kanamori S., Isahara K., Ohsawa Y., Konishi A., Kametaka S., Watanabe T., Ebisu S., Ishido K., Kominami E., Uchiyama Y. Participation of cathepsins B and D in apoptosis of PC12 cells following serum deprivation. Biochem. Biophys. Res. Commun. 1998, 251:199-203.
74. Tardy C., Tyynela J., Hasilik A., Levade T., Andrieu-Abadie N. Stress-induced apoptosis is impaired in cells with a lysosomal targeting defect but is not affected in cells synthesizing a catalytically inactive cathepsin D. Cell Death Differ. 2003, 10:1090-1100.
75. Schestkowa O., Geisel D., Jacob R., Hasilik A. The catalytically inactive precursor of cathepsin D induces apoptosis in human fibroblasts and HeLa cells. J. Cell Biochem. 2007, 101:1558-1566.
76. Westley B.R., May F.E. Prognostic value of cathepsin D in breast cancer. Br. J. Cancer 1999, 79:189-190.
77. Ferrandina G., Scambia G., Bardelli F., Benedetti Panici P., Mancuso S., Messori A. Relationship between cathepsin-D content and disease-free survival in node-negative breast cancer patients: a meta-analysis. Br. J. Cancer 1997, 76:661-666.
78. Foekens J.A., Look M.P., Bolt-de Vries J., Meijer-van Gelder M.E., van Putten W.L., Klijn J.G. Cathepsin-D in primary breast cancer: prognostic evaluation involving 2810 patients. Br. J. Cancer 1999, 79:300-307.
79. Fitzgibbons P.L., Page D.L., Weaver D., Thor A.D., Allred D.C., Clark G.M., Ruby S.G., O'Malley F., Simpson J.F., Connolly J.L., Hayes D.F., Edge S.B., Lichter A., Schnitt S.J. Prognostic factors in breast cancer. College of American pathologists consensus statement 1999. Arch. Pathol. Lab. Med. 2000, 124:966-978.
80. Harbeck N., Alt U., Berger U., Kates R., Kruger A., Thomssen C., Janicke F., Graeff H., Schmitt M. Long-term follow-up confirms prognostic impact of PAI-1 and cathepsin D and L in primary breast cancer. Int. J. Biol. Markers 2000, 15:79-83.
81. Greco S., Marsigliante S., Leo G., Storelli C. Co-expression of thymidine kinase and cathepsin D in 200 primary breast carcinomas. Cancer Lett. 2000, 160:13-19.
82. Gaci Z., Bouin-Pineau M.H., Gaci M., Daban A., Ingrand P., Metaye T. Prognostic impact of cathepsin D and c-erbB-2 oncoprotein in a subgroup of node-negative breast cancer patients with low histological grade tumors. Int. J. Oncol. 2001, 18:793-800.
83. Bossard N., Descotes F., Bremond A.G., Bobin Y., De Saint Hilaire P., Golfier F., Awada A., Mathevet P.M., Berrerd L., Barbier Y., Esteve J. Keeping data continuous when analyzing the prognostic impact of a tumor marker: an example with cathepsin D in breast cancer. Breast Cancer Res. Treat. 2003, 82:47-59.
84. Kute T.E., Russell G.B., Zbieranski N., Long R., Johnston S., Williams H., Stackhouse C., Wilkins L., Evans I., Berry P., Rimmer K., Tucker E. Prognostic markers in node-negative breast cancer: a prospective study. Cytometry B Clin. Cytom. 2004, 59:24-31.
85. Rodriguez J., Vazquez J., Corte M.D., Lamelas M., Bongera M., Corte M.G., Alvarez A., Allende M., Gonzalez L., Sanchez M., Vijande M., Garcia Muniz J., Vizoso F. Clinical significance of cathepsin D concentration in tumor cytosol of primary breast cancer. Int. J. Biol. Markers 2005, 20:103-111.
86. Anim J.T., John B., Abdulsathar S.S., Prasad A., Saji T., Akhtar N., Ali V., Al-Saleh M. Relationship between the expression of various markers and prognostic factors in breast cancer. Acta Histochem. 2005, 107:87-93.
87. Cheng A.L., Huang W.G., Chen Z.C., Zhang P.F., Li M.Y., Li F., Li J.L., Li C., Yi H., Peng F., Duan C.J., Xiao Z.Q. Identificating cathepsin D as a biomarker for differentiation and prognosis of nasopharyngeal carcinoma by laser capture microdissection and proteomic analysis. J. Proteome Res. 2008, 7:2415-2426.
88. Vasudev N.S., Sim S., Cairns D.A., Ferguson R.E., Craven R.A., Stanley A., Cartledge J., Thompson D., Selby P.J., Banks R.E. Pre-operative urinary cathepsin D is associated with survival in patients with renal cell carcinoma. Br. J. Cancer 2009, 101:1175-1182.
89. Roger P., Montcourrier P., Maudelonde T., Brouillet J.P., Pages A., Laffargue F., Rochefort H. Cathepsin D immunostaining in paraffin-embedded breast cancer cells and macrophages: correlation with cytosolic assay. Hum. Pathol. 1994, 25:863-871.
90. Brouillet J.P., Dufour F., Lemamy G., Garcia M., Schlup N., Grenier J., Mani J.C., Rochefort H. Increased cathepsin D level in the serum of patients with metastatic breast carcinoma detected with a specific pro-cathepsin D immunoassay. Cancer 1997, 79:2132-2136.
91. Szajda S.D., Snarska J., Jankowska A., Roszkowska-Jakimiec W., Puchalski Z., Zwierz K. Cathepsin D and carcino-embryonic antigen in serum, urine and tissues of colon adenocarcinoma patients. Hepatogastroenterology 2008, 55:388-393.
92. Szajda S.D., Snarska J., Roszkowska-Jakimiec W., Waszkiewicz N., Siedlecka K., Zwierz K., Krupkowska A. Pol Arch. Med. Wewn. 2006, 116:1150-1154.
93. Selicharova I., Sanda M., Mladkova J., Ohri S.S., Vashishta A., Fusek M., Jiracek J., Vetvicka V. 2-DE analysis of breast cancer cell lines 1833 and 4175 with distinct metastatic organ-specific potentials: comparison with parental cell line MDA-MB-231. Oncol. Rep. 2008, 19:1237-1244.
94. Roth U., Razawi H., Hommer J., Engelmann K., Schwientek T., Muller S., Baldus S.E., Patsos G., Corfield A.P., Paraskeva C., Hanisch F.G. Differential expression proteomics of human colorectal cancer based on a syngeneic cellular model for the progression of adenoma to carcinoma. Proteomics 2010, 10:194-202.
95. Vignon F., Capony F., Chambon M., Freiss G., Garcia M., Rochefort H. Autocrine growth stimulation of the MCF 7 breast cancer cells by the estrogen-regulated 52 K protein. Endocrinology 1986, 118:1537-1545.
96. Garcia M., Derocq D., Pujol P., Rochefort H. Overexpression of transfected cathepsin D in transformed cells increases their malignant phenotype and metastatic potency. Oncogene 1990, 5:1809-1814.
97. Fusek M., Vetvicka V. Mitogenic function of human procathepsin D: the role of the propeptide. Biochem. J. 1994, 303(Pt 3):775-780.
98. Vetvicka V., Vektvickova J., Fusek M. Effect of human procathepsin D on proliferation of human cell lines. Cancer Lett. 1994, 79:131-135.
99. Liaudet E., Derocq D., Rochefort H., Garcia M. Transfected cathepsin D stimulates high density cancer cell growth by inactivating secreted growth inhibitors. Cell Growth Differ. 1995, 6:1045-1052.
100. Ohri S.S., Vashishta A., Proctor M., Fusek M., Vetvicka V. Depletion of procathepsin D gene expression by RNA interference: a potential therapeutic target for breast cancer. Cancer Biol. Ther. 2007, 6:1081-1087.
101. Ohri S.S., Vashishta A., Proctor M., Fusek M., Vetvicka V. The propeptide of cathepsin D increases proliferation, invasion and metastasis of breast cancer cells. Int. J. Oncol. 2008, 32:491-498.
102. Liaudet E., Garcia M., Rochefort H. Cathepsin D maturation and its stimulatory effect on metastasis are prevented by addition of KDEL retention signal. Oncogene 1994, 9:1145-1154.
103. Glondu M., Liaudet-Coopman E., Derocq D., Platet N., Rochefort H., Garcia M. Down-regulation of cathepsin-D expression by antisense gene transfer inhibits tumor growth and experimental lung metastasis of human breast cancer cells. Oncogene 2002, 21:5127-5134.
104. Vashishta A., Ohri S.S., Proctor M., Fusek M., Vetvicka V. Ribozyme-targeting procathepsin D and its effect on invasion and growth of breast cancer cells: an implication in breast cancer therapy. Int. J. Oncol. 2007, 30:1223-1230.
105. Glondu M., Coopman P., Laurent-Matha V., Garcia M., Rochefort H., Liaudet-Coopman E. A mutated cathepsin-D devoid of its catalytic activity stimulates the growth of cancer cells. Oncogene 2001, 20:6920-6929.
106. Vetvicka V., Vetvickova J., Fusek M. Effect of procathepsin D and its activation peptide on prostate cancer cells. Cancer Lett. 1998, 129:55-59.
107. Vetvicka V., Vetvickova J., Benes P. Role of enzymatically inactive procathepsin D in lung cancer. Anticancer Res. 2004, 24:2739-2743.
108. Nirde P., Derocq D., Maynadier M., Chambon M., Basile I., Gary-Bobo M., Garcia M. Heat shock cognate 70 protein secretion as a new growth arrest signal for cancer cells. Oncogene 2010, 29:117-127.
109. Mathieu M., Rochefort H., Barenton B., Prebois C., Vignon F. Interactions of cathepsin-D and insulin-like growth factor-II (IGF-II) on the IGF-II/mannose-6-phosphate receptor in human breast cancer cells and possible consequences on mitogenic activity of IGF-II. Mol. Endocrinol. 1990, 4:1327-1335.
110. Faridi J.S., Mohan S., De Leon D.D. Modulation of cathepsin D routing by IGF-II involves IGF-II binding to IGF-II/M6P receptor in MCF-7 breast cancer cells. Growth Factors 2004, 22:169-177.
111. Vetvicka V., Benes P., Fusek M. Procathepsin D in breast cancer: what do we know? Effects of ribozymes and other inhibitors. Cancer Gene Ther. 2002, 9:854-863.
112. Vetvicka V., Vetvickova J., Fusek M. Anti-human procathepsin D activation peptide antibodies inhibit breast cancer development. Breast Cancer Res. Treat. 1999, 57:261-269.
113. Vashishta A., Ohri S.S., Proctor M., Fusek M., Vetvicka V. Role of activation peptide of procathepsin D in proliferation and invasion of lung cancer cells. Anticancer Res. 2006, 26:4163-4170.
114. Briozzo P., Badet J., Capony F., Pieri I., Montcourrier P., Barritault D., Rochefort H. MCF7 mammary cancer cells respond to bFGF and internalize it following its release from extracellular matrix: a permissive role of cathepsin D. Exp. Cell Res. 1991, 194:252-259.
115. Griffiths J.R. Are cancer cells acidic?. Br. J. Cancer 1991, 64:425-427.
116. Rochefort H., Liaudet-Coopman E. Cathepsin D in cancer metastasis: a protease and a ligand. APMIS 1999, 107:86-95.
117. Mueller M.M., Fusenig N.E. Friends or foes - bipolar effects of the tumour stroma in cancer. Nat. Rev. Cancer 2004, 4:839-849.
118. Liotta L.A., Kohn E.C. The microenvironment of the tumour-host interface. Nature 2001, 411:375-379.
119. Masson R., Lefebvre O., Noel A., Fahime M.E., Chenard M.P., Wendling C., Kebers F., LeMeur M., Dierich A., Foidart J.M., Basset P., Rio M.C. In vivo evidence that the stromelysin-3 metalloproteinase contributes in a paracrine manner to epithelial cell malignancy. J. Cell Biol. 1998, 140:1535-1541.
120. Laurent-Matha V., Maruani-Herrmann S., Prebois C., Beaujouin M., Glondu M., Noel A., Alvarez-Gonzalez M.L., Blacher S., Coopman P., Baghdiguian S., Gilles C., Loncarek J., Freiss G., Vignon F., Liaudet-Coopman E. Catalytically inactive human cathepsin D triggers fibroblast invasive growth. J. Cell Biol. 2005, 168:489-499.
121. Heylen N., Vincent L.M., Devos V., Dubois V., Remacle C., Trouet A. Fibroblasts capture cathepsin D secreted by breast cancer cells: possible role in the regulation of the invasive process. Int. J. Oncol. 2002, 20:761-767.
122. Hu L., Roth J.M., Brooks P., Luty J., Karpatkin S. Thrombin up-regulates cathepsin D which enhances angiogenesis, growth, and metastasis. Cancer Res. 2008, 68:4666-4673.
123. Wolf M., Clark-Lewis I., Buri C., Langen H., Lis M., Mazzucchelli L. Cathepsin D specifically cleaves the chemokines macrophage inflammatory protein-1 alpha, macrophage inflammatory protein-1 beta, and SLC that are expressed in human breast cancer. Am. J. Pathol. 2003, 162:1183-1190.
124. Erdmann S., Ricken A., Hummitzsch K., Merkwitz C., Schliebe N., Gaunitz F., Strotmann R., Spanel-Borowski K. Inflammatory cytokines increase extracellular procathepsin D in permanent and primary endothelial cell cultures. Eur. J. Cell Biol. 2008, 87:311-323.
125. Goulet B., Baruch A., Moon N.S., Poirier M., Sansregret L.L., Erickson A., Bogyo M., Nepveu A. A cathepsin L isoform that is devoid of a signal peptide localizes to the nucleus in S phase and processes the CDP/Cux transcription factor. Mol. Cell 2004, 14:207-219.
126. Maubach G., Lim M.C., Zhuo L. Nuclear cathepsin F regulates activation markers in rat hepatic stellate cells. Mol. Biol. Cell 2008, 19:4238-4248.
127. Duncan E.M., Muratore-Schroeder T.L., Cook R.G., Garcia B.A., Shabanowitz J., Hunt D.F., Allis C.D. Cathepsin L proteolytically processes histone H3 during mouse embryonic stem cell differentiation. Cell 2008, 135:284-294.
128. Ceru S., Konjar S., Maher K., Repnik U., Krizaj I., Bencina M., Renko M., Nepveu A., Zerovnik E., Turk B., Kopitar-Jerala N. Stefin B interacts with histones and cathepsin L in the nucleus. J. Biol. Chem. 2010, 285:10078-10086.
129. Goulet B., Sansregret L., Leduy L., Bogyo M., Weber E., Chauhan S.S., Nepveu A. Increased expression and activity of nuclear cathepsin L in cancer cells suggests a novel mechanism of cell transformation. Mol. Cancer Res. 2007, 5:899-907.
130. Sullivan S., Tosetto M., Kevans D., Coss A., Wang L., O'Donoghue D., Hyland J., Sheahan K., Mulcahy H., O'Sullivan J. Localization of nuclear cathepsin L and its association with disease progression and poor outcome in colorectal cancer. Int. J. Cancer 2009, 125:54-61.
131. Dash C., Kulkarni A., Dunn B., Rao M. Aspartic peptidase inhibitors: implications in drug development. Crit. Rev. Biochem. Mol. Biol. 2003, 38:89-119.
132. Riccioni G., Vitulano N., D'Orazio N., Bellocci F. Aliskiren, the first approved renin inhibitor: clinical application and safety in the treatment of hypertension. Adv. Ther. 2009, 26:700-710.
133. Bjorklund C., Oscarson S., Benkestock K., Borkakoti N., Jansson K., Lindberg J., Vrang L., Hallberg A., Rosenquist A., Samuelsson B. Design and synthesis of potent and selective BACE-1 inhibitors. J. Med. Chem. 2010, 53:1458-1464.
134. Johansson P.O., Chen Y., Belfrage A.K., Blackman M.J., Kvarnstrom I., Jansson K., Vrang L., Hamelink E., Hallberg A., Rosenquist A., Samuelsson B. Design and synthesis of potent inhibitors of the malaria aspartyl proteases plasmepsin I and II. Use of solid-phase synthesis to explore novel statine motifs. J. Med. Chem. 2004, 47:3353-3366.
135. Lefebvre E., Schiffer C.A. Resilience to resistance of HIV-1 protease inhibitors: profile of darunavir. AIDS Rev. 2008, 10:131-142.
136. Estes K.E., Penzak S.R., Calis K.A., Walsh T.J. Pharmacology and antifungal properties of anidulafungin, a new echinocandin. Pharmacotherapy 2009, 29:17-30.
137. Gonias S.L., Pizzo S.V. Conformation and protease binding activity of binary and ternary human alpha 2-macroglobulin-protease complexes. J. Biol. Chem. 1983, 258:14682-14685.
138. Barrett A.J., Starkey P.M. The interaction of alpha 2-macroglobulin with proteinases. Characteristics and specificity of the reaction, and a hypothesis concerning its molecular mechanism. Biochem. J. 1973, 133:709-724.
139. Gacko M., Minarowska A., Karwowska A., Minarowski L. Cathepsin D inhibitors. Folia Histochem. Cytobiol. 2007, 45:291-313.
140. Minarowska A., Karwowska A., Gacko M. Quantitative determination and localization of cathepsin D and its inhibitors. Folia Histochem. Cytobiol. 2009, 47:153-177.
141. Kick E.K., Roe D.C., Skillman A.G., Liu G., Ewing T.J., Sun Y., Kuntz I.D., Ellman J.A. Structure-based design and combinatorial chemistry yield low nanomolar inhibitors of cathepsin D. Chem. Biol. 1997, 4:297-307.
142. Ellman J.A. Combinatorial Methods to Engineer Small Molecules for Functional Genomics 2000, Ernst Schering Res Found Workshop, 183-204.
143. Bi X., Haque T.S., Zhou J., Skillman A.G., Lin B., Lee C.E., Kuntz I.D., Ellman J.A., Lynch G. Novel cathepsin D inhibitors block the formation of hyperphosphorylated tau fragments in hippocampus. J. Neurochem. 2000, 74:1469-1477.
144. Wood W.J., Patterson A.W., Tsuruoka H., Jain R.K., Ellman J.A. Substrate activity screening: a fragment-based method for the rapid identification of nonpeptidic protease inhibitors. J. Am. Chem. Soc. 2005, 127:15521-15527.
145. Srivastava V., Saxena H.O., Shanker K., Kumar J.K., Luqman S., Gupta M.M., Khanuja S.P., Negi A.S. Synthesis of gallic acid based naphthophenone fatty acid amides as cathepsin D inhibitors. Bioorg. Med. Chem. Lett. 2006, 16:4603-4608.
146. Fusek M., Mares M., Vagner J., Voburka Z., Baudys M. Inhibition of aspartic proteinases by propart peptides of human procathepsin D and chicken pepsinogen. FEBS Lett. 1991, 287:160-162.
147. Masa M., Maresova L., Vondrasek J., Horn M., Jezek J., Mares M. Cathepsin D propeptide: mechanism and regulation of its interaction with the catalytic core. Biochemistry 2006, 45:15474-15482.
148. Knight C.G., Barrett A.J. Interaction of human cathepsin D with the inhibitor pepstatin. Biochem. J. 1976, 155:117-125.
149. Tumminello F.M., Leto G., Gebbia N., Rausa L., Bernacki R.J. Evaluation of antitumor and antimetastatic activity of pepstatin A in some experimental tumor models. J. Chemother. 1989, 1:1135-1138.
150. Bessodes M., Antonakis K., Herscovici J., Garcia M., Rochefort H., Capony F., Lelievre Y., Scherman D. Inhibition of cathepsin D by tripeptides containing statine analogs. Biochem. Pharmacol. 1999, 58:329-333.
151. Lison P., Rodrigo I., Conejero V. A novel function for the cathepsin D inhibitor in tomato. Plant Physiol. 2006, 142:1329-1339.
152. Cater S.A., Lees W.E., Hill J., Brzin J., Kay J., Phylip L.H. Aspartic proteinase inhibitors from tomato and potato are more potent against yeast proteinase A than cathepsin D. Biochim. Biophys. Acta 2002, 1596:76-82.
153. Lenarcic B., Turk V. Thyroglobulin type-1 domains in equistatin inhibit both papain-like cysteine proteinases and cathepsin D. J. Biol. Chem. 1999, 274:563-566.
154. Strukelj B., Lenarcic B., Gruden K., Pungercar J., Rogelj B., Turk V., Bosch D., Jongsma M.A. Equistatin, a protease inhibitor from the sea anemone actinia equina, is composed of three structural and functional domains. Biochem. Biophys. Res. Commun. 2000, 269:732-736.
155. Shibata M., Koike M., Waguri S., Zhang G., Koga T., Uchiyama Y. Cathepsin D is specifically inhibited by deoxyribonucleic acids. FEBS Lett. 2002, 517:281-284.
156. Vetvicka V., Vetvickova J., Hilgert I., Voburka Z., Fusek M. Analysis of the interaction of procathepsin D activation peptide with breast cancer cells. Int. J. Cancer 1997, 73:403-409.
157. Dunn B.M., Hung S. The two sides of enzyme-substrate specificity: lessons from the aspartic proteinases. Biochim. Biophys. Acta 2000, 1477:231-240.
158. Schilling O., Overall C.M. Proteome-derived, database-searchable peptide libraries for identifying protease cleavage sites. Nat. Biotechnol. 2008, 26:685-694.
159. Lkhider M., Castino R., Bouguyon E., Isidoro C., Ollivier-Bousquet M. Cathepsin D released by lactating rat mammary epithelial cells is involved in prolactin cleavage under physiological conditions. J. Cell Sci. 2004, 117:5155-5164.
160. Piwnica D., Fernandez I., Binart N., Touraine P., Kelly P.A., Goffin V. A new mechanism for prolactin processing into 16K PRL by secreted cathepsin D. Mol. Endocrinol. 2006, 20:3263-3278.
161. Sevlever D., Jiang P., Yen S.H. Cathepsin D is the main lysosomal enzyme involved in the degradation of alpha-synuclein and generation of its carboxy-terminally truncated species. Biochemistry 2008, 47:9678-9687.
162. Sakaguchi M., Murata H., Sonegawa H., Sakaguchi Y., Futami J., Kitazoe M., Yamada H., Huh N.H. Truncation of annexin A1 is a regulatory lever for linking epidermal growth factor signaling with cytosolic phospholipase A2 in normal and malignant squamous epithelial cells. J. Biol. Chem. 2007, 282:35679-35686.
163. Christensen B., Schack L., Klaning E., Sorensen E.S. Osteopontin is cleaved at multiple sites close to its integrin-binding motifs in milk and is a novel substrate for plasmin and cathepsin D. J. Biol. Chem. 2010, 285:7929-7937.
164. Schilling O., Overall C.M. Proteomic discovery of protease substrates. Curr. Opin. Chem. Biol. 2007, 11:36-45.
165. Overall C.M., Blobel C.P. In search of partners: linking extracellular proteases to substrates. Nat. Rev. Mol. Cell Biol. 2007, 8:245-257.
166. Doucet A., Overall C.M. Protease proteomics: revealing protease in vivo functions using systems biology approaches. Mol. Aspects Med. 2008, 29:339-358.
167. Butler G.S., Dean R.A., Smith D., Overall C.M. Membrane protease degradomics: proteomic identification and quantification of cell surface protease substrates. Methods Mol. Biol. 2009, 528:159-176.
168. 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, 6:611-623.
169. Faust P.L., Kornfeld S., Chirgwin J.M. Cloning and sequence analysis of cDNA for human cathepsin D. Proc. Natl. Acad. Sci. U S A 1985, 82:4910-4914.