Nitration of cathepsin D enhances its proteolytic activity during mammary gland remodelling after lactation

Biochemical Journal

Volumn 419, Issue 2, 2009, Pages 279-288

  Zaragozá, Rosa ^a   Torres, Luis ^a   García, Concha ^a   Eroles, Pilar ^a   Corrales, Fernando ^b   Bosch, Ana ^a   Lluch, Ana ^a   García Trevijano, Elena R ^a   Viña, Juan R ^a  

^a UNIVERSITY OF VALENCIA   (Spain)

^b UNIVERSITY OF NAVARRA   (Spain)

Author keywords

Cathepsin D activity; Mammary gland involution; Nitration; Nitrotyrosine; Post translational modification; Weaning

Indexed keywords

CATHEPSIN D ACTIVITY; MAMMARY GLAND INVOLUTION; NITROTYROSINE; POST-TRANSLATIONAL MODIFICATION; WEANING;

ANIMALS; COMBINATORIAL CIRCUITS; ENZYMES; NITRATION; NITRIC OXIDE;

ENZYME ACTIVITY;

CATHEPSIN D; CATHEPSIN E; CHYMOSIN; INDUCIBLE NITRIC OXIDE SYNTHASE; PEPSIN A; PEROXYNITRITE; RENIN; TYROSINE; NITRATE;

ANIMAL TISSUE; ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; HUMAN; IN VITRO STUDY; IN VIVO STUDY; KNOCKOUT MOUSE; LACTATION; MAMMARY GLAND; MAMMARY GLAND FUNCTION; MOUSE; NITRATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEOMICS; RAT; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; UPREGULATION; WEANING; WILD TYPE; AFFINITY CHROMATOGRAPHY; ANIMAL; ELECTROSPRAY MASS SPECTROMETRY; GENETICS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; LIQUID CHROMATOGRAPHY; METABOLISM; PHYSIOLOGY; PREGNANCY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TANDEM MASS SPECTROMETRY; TWO DIMENSIONAL GEL ELECTROPHORESIS; UDDER;

ANIMALIA; MUS; RATTUS;

ANIMALS; CATHEPSIN D; CHROMATOGRAPHY, AFFINITY; CHROMATOGRAPHY, LIQUID; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FEMALE; IMMUNOBLOTTING; IMMUNOPRECIPITATION; LACTATION; MAMMARY GLANDS, ANIMAL; MICE; NITRATES; NITRIC OXIDE SYNTHASE TYPE II; PREGNANCY; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; TANDEM MASS SPECTROMETRY; WEANING;

EID: 64249088369     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20081746     Document Type: Article

References (43)

1. Vorbach, C., Capecci, M. R. and Penninger, J. M. (2006) Evolution of the mammary gland from the innate immune system? BioEssays 28, 606-616
2. Green, K. A. and Streuli, C. H. (2004) Apoptosis regulation in the mammary gland. Cell. Mol. Life Sci. 61, 1867-1883
3. Baxter, F. O., Neoh, K. and Tevendale, M. C. (2007) The beginning of the end: death signaling in early involution. J. Mammary Gland Biol. Neoplasia 12, 3-13
4. Clarkson, R. W. E., Wayland, M. T., Lee, J., Freeman, T. and Watson, C. J. (2004) Gene expression profiling of mammary gland development reveals putative roles for death receptors and immune mediators in post-lactational regression. Breast Cancer Res. 6, R92-R109
5. Stein, T., Morris, J. S., Davies, C. R., Weber-Hall, S. J., Duffy, M-A., Heath, V. J., Bell, A. K., Ferrier, R. K., Sandilands, G. P. and Gusterson, B. A. (2004) Involution of the mouse mammary gland is associated with an immune cascade and an acute-phase response, involving LBP, cathepsin D14 and STAT3. Breast Cancer Res. 6, R75-R91
6. Zaragozá, R., Miralles, V. J., Rus, A. D., García, C., Carmena, R., García-Trevijano, E. R., Barber, T., Pallardó, F. V., Torres, L. and Viña, J. R. (2005) Weaning induces NOS-2 expression through NF-κ modulation in the lactating mammary gland: importance of GSH. Biochem. J. 391, 581-588
7. Chapman, R. S., Lourenco, P. C., Tonner, E., Flint, D. J., Selbert, S., Takeda, K., Akira, S., Clarke, A. R. and Watson, C. J. (1999) Suppression of epithelial apoptosis and delayed mammary gland involution in mice with a conditional knockout of Stat3. Genes Dev. 13, 2604-2616
8. Baxter, F. O., Came, P. J., Abell, K., Kedjouar, B., Huth, M., Rajewsky, K., Pasparakis, M. and Watson, C. J. (2006) IKKβ/2 induces TWEAK and apoptosis in mammary epithelium. Development 133, 3485-3494
9. Dietze, E. C., Caldwell, L. E., Marcom, K., Collins, S. J., Yee, L., Swisshelm, K., Hobbs, K. B., Bean, G. R. and Seewaldt, V. L. (2002) Retinoids and retinoic acid receptors regulate growth arrest and apoptosis in human mammary epithelial cells and modulate expression of CBP/p300. Microsc. Res. Tech. 59, 23-40
10. Zaragozá, R., Miralles, V. J., García-Trevijano, E. R., Carmena, R., García C., Mata, M., Puertes, I. R., Torres, L., Viña, J. R. and Gimeno, A. (2007) Retinoids induce MMP-9 expression through RARα during mammary gland remodelling. Am. J. Physiol. Endocrinol. Metab. 292, E1140-E1148
11. Clarkson, R. W. E., Heeley, J. L., Chapman, R., Aillet, F., Hay, R. T., Wyllie, A. and Watson, C. J. (2000) NF-κB inhibits apoptosis in murine mammary epithelia. J. Biol. Chem. 275, 12737-12742
12. MacMillan-Crow, L. A., Crow, J. P. and Thompson, J. A. (1998) Peroxynitrite-mediated inactivation of manganese superoxide dismutase involves nitration and oxidation of critical tyrosine residues. Biochemistry 37, 1613-1622
13. Görg, B., Qvartskhava, N., Voss, P., Grune, T., Häussinger, D. and Schliess, F. (2007) Reversible inhibition of mammalian glutamine synthetase by tyrosine nitration. FEBS Lett. 581, 84-90
14. Ji, Y. and Bennett, B. M. (2003) Activation of microsomal glutathione S-transferase by peroxynitrite. Mol. Pharmacol. 63, 136-146
15. Ji, Y., Neverova, I., Van Eyk, J. E. and Bennett, B. M. (2006) Nitration of tyrosine 92 mediates the activation of rat microsomal glutathione S-transferase by peroxynitrite. J. Biol. Chem. 281, 1986-1991
16. Rebrin, I., Brégère, C., Kamzalov, S., Gallaher, T. K. and Sohal, R. S. (2007) Nitration of tryptophan 372 in succinyl-CoA:3-ketoacid CoA transferase during aging in rat heart mitochondria. Biochemistry 46, 10130-10144
17. Tang, J. and Wong, R. N. (1987) Evolution in the structure and function of aspartic proteases. J. Cell. Biochem. 33, 53-63
18. Saftig, P., Hetman, M., Schmahl, W., Weber, K., Heine, L., Mossmann, H., Köster, A., Hess, B., Evers, M., von Figura, K. et al. (1995) Mice deficient for the lysosomal proteinase cathepsin D exhibit progressive atrophy of the intestinal mucosa and profound destruction of lymphoid cells. EMBO J. 14, 3599-3608
19. Rochefort, H. and Liaudet-Coopman, E. (1999) Cathepsin D in cancer metastasis: a protease and a ligand. APMIS 107, 86-95
20. Castino, R., Bellio, N., Nicotra, G., Follo, C., Trinchera, N. F. and Isidoro, C. (2007) Cathepsin D-Bax death pathway in oxidative stressed neuroblastoma cells. Free Radical Biol. Med. 42, 1305-1316
21. Castino, R., Delpal, S., Bouguyon, E., Demoz, M., Isidoro, C. and Ollivier-Bousquet, M. (2008) Prolactin promotes the secretion of active cathepsin D at the basal side of rat mammary acini. Endocrinology 149, 4095-4105
22. Khalkhali-Ellis, Z., Abbott, D. E., Bailey, C. M., Goossens, W., Margaryan, N. V., Gluck, S. L., Reuveni, M. and Hendrix, M. J. C. (2008) IFN-γ regulation of vacuolar pH, cathepsin D processing and autophagy in mammary epithelial cells. J. Cell. Biochem. 105, 208-218
23. Zaragozá, R., García, C., Rus, A. D., Pallardó, F. V., Barber, T., Torres, L., Miralles, V. J. and Viña, J. R. (2003) Inhibition of liver trans-sulphuration pathway by propargylglycine mimics gene expression changes found in the mammary gland of weaned lactating rats: role of glutathione. Biochem. J. 373, 825-834
24. Follo, C., Castino, R., Nicotra, G., Trincheri, N. F. and Isidoro, C. (2007) Folding, activity and targeting of mutated human cathepsin D that cannot be processed into the double-chain form. Int. J. Biochem. Cell Biol. 39, 638-649
25. Muñoz, J., Fernández-Irigoyen, J., Santamaría, E., Parbel, A., Obeso, J. and Corrales, F. J. (2008) Mass spectrometric characterization of mitochondrial complex I NDUFA10 variants. Proteomics 8, 1898-1908
26. Yasuda, Y., Kageyama, T, Akamine, A., Shibata, M., Kominami, E., Uchiyama, Y. and Yamamoto, K. (1999) Characterization of new fluorogenic substrates for the rapid and sensitive assay of cathepsin E and cathepsin D. J. Biochem. 125, 1137-1143
27. Radi, R., Beckman, J. S., Bush, K. M. and Freeman, B. A. (1991) Peroxynitrite oxidation of sulfhydryls: the cytotoxic potential of superoxide and nitric oxide. J. Biol. Chem. 266, 4244-4250
28. Shamay, A., Shapiro, F., Mabjeesh, S. J. and Silanikove, N. (2002) Casein-derived phosphopeptides disrupt tight junction integrity, and precipitously dry up milk secretion in goats. Life Sci. 70, 2707-2719
29. Hernández-Montes, H., Escudero, I. and Villalpando, S. (1999) Changes in cathepsin D activity of maternal tissues during lactation and weaning in rats. Arch. Med. Res. 30, 10-13
30. Helminen, H. J., Ericsson, J. L. E. and Orrenius, S. (1968) Studies on mammary gland involution. IV. Histochemical and biochemical observations on alterations in lysosomes and lysosomal enzymes. J. Ultrastruct. Res. 25, 240-252
31. Schroeder, P., Klotz, L. O., Buchczyk, D. P., Sadik, C. D., Schewe, T. and Sies, H. (2001) Epicatechin prevents nitration but not oxidation reactions of peroxynitrite. Biochem. Biophys. Res. Commun. 285, 782-787
32. Alvarez, B. and Radi, R. (2003) Peroxynitrite reactivity with amino acids and proteins. Amino Acids 25, 295-311
33. Sokolovsky, M., Riordan, J. F. and Vallee, B. L. (1967) Conversion of 3-nitrotyrosine to 3-aminotyrosine in peptides and proteins. Biochem. Biophys. Res. Commun. 27, 20-25
34. Matsuyama, S., Llopis, J, Deveraux, Q. L., Tsien, R. Y. and Reed, J. C. (2000) Changes in intramitochondrial and cytosolic pH: early events that modulate caspase activation during apoptosis. Nat. Cell Biol. 2, 318-325
35. Beaujouin, M. and Liaudet-Coopman, E. (2008) Cathepsin D overexpressed by cancer cells can enhance apoptosis-dependent chemo-sensitivity independently of its catalytic activity. Adv. Exp. Med. Biol. 617, 453-461
36. Mása, M., Maresová, L., Vondrásek, J., Horn, M., Jezek, J. and Mares, M. (2006) Cathepsin D propeptide: mechanism and regulation of its interaction with the catalytic core. Biochemistry 45, 15474-15482
37. Bossard, N., Descotes, F., Bremond, A. G., Bobin, Y., De Saint Hilaire, P., Golfier, F., Awada, A., Mathevet, P. M., Berrerd, L., Barbier, Y. and Estève, J. (2003) Keeping data continuous when analyzing the prognostic impact of a tumor marker: an example with cathepsin D in breast cancer. Breast Cancer Res. Treat. 82, 47-59
38. Benes, P., Vetvicka, V. and Fusek, M. (2008) Cathepsin D: many functions of one aspartic protease. Crit. Rev. Oncol. Hematol. 68, 12-28
39. Hu, L., Roth, J. M., Brooks, P., Luty, J. and Karpatkin, S. (2008) Thrombin up-regulates cathepsin D which enhances angiogenesis, growth and metastasis. Cancer Res. 68, 4666-4673
40. Capony, F., Rougeot, C. I., Montcourrier, P., Cavailles, V., Salazar, G. and Rochefort, H. (1989) Increased secretion, altered processing and glycosylation of pro-cathepsin D in human mammary cancer cells. Cancer Res. 49, 3904-3909
41. Pujol, P., Maudelonde, T., Daures, J. P., Rouanet, P., Brouillet, J. P., Pujol, H. and Rochefort, H. (1993) A prospective study of the prognostic value of cathepsin D levels in breast cancer cytosol. Cancer 71, 2006-2012
42. Glondu, M., Coopman, P., Laurent-Matha, V., Garcia, M., Rochefort, H. and Liaudet-Coopman, E. (2001) A mutated cathepsin-D devoid of its catalytic activity stimulates the growth of cancer cells. Oncogene 20, 6920-6929
43. Blanchard, A., Shiu, R., Booth, S., Sorensen, G., DeCorby, N., Nistor, A., Wong, P., Leygue, E. and Myal, Y. (2007) Gene expression profiling of early involuting mammary gland reveals novel genes potentially relevant to human breast cancer. Front. Biosci. 12, 2221-2232