Cathepsin D released by lactating rat mammary epithelial cells is involved in prolactin cleavage under physiological conditions

Journal of Cell Science

Volumn 117, Issue 21, 2004, Pages 5155-5164

  Lkhider, Mustapha ^a   Castino, Roberta ^b   Bouguyon, Edwige ^c   Isidoro, Ciro ^b   Ollivier Bousquet, Michèle ^c  

^a FACULTÉ DES SCIENCES   (Morocco)

^b UNIVERSITY OF EASTERN PIEDMONT   (Italy)

^c INRA Institut National de la Recherche Agronomique   (France)

Author keywords

Endosomes; Hormone; Lactation; Lysosomes; Mammary gland; Proteolysis

Indexed keywords

BREFELDIN A; CATHEPSIN D; HIRUDIN; MILK PROTEIN; PEPSTATIN; PROLACTIN; THROMBIN INHIBITOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BASOLATERAL MEMBRANE; BREAST EPITHELIUM; CELL PH; CONTROLLED STUDY; CULTURE MEDIUM; ENDOSOME; ENZYME ACTIVITY; EPITHELIUM CELL; EXTRACELLULAR SPACE; FEMALE; LACTATION; LYSOSOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN SECRETION; PROTEIN TRANSPORT; RAT; STROMA CELL; TEMPERATURE;

ANIMALS; BREFELDIN A; CATHEPSIN D; CULTURE MEDIA, CONDITIONED; ENDOSOMES; EPITHELIAL CELLS; FEMALE; HIRUDINS; HYDROGEN-ION CONCENTRATION; LACTATION; LYSOSOMES; MAMMARY GLANDS, ANIMAL; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, FLUORESCENCE; PEPSTATINS; PROLACTIN; PROTEIN STRUCTURE, TERTIARY; RATS; TEMPERATURE; TIME FACTORS;

ANIMALIA;

EID: 8744233052     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.01396     Document Type: Article

References (49)

1. Baldocchi, R. A., Tan, L. and Nicoll, C. S. (1992). Processing of rat prolactin by rat tissue explants and serum in vitro. Endocrinology 130, 1653-1659.
2. Baldocchi, R. A., Tan, L., King, D. S. and Nicoll, C. S. (1993). Mass spectrometric analysis of the fragments produced by cleavage and reduction of rat prolactin: evidence that the cleaving enzyme is cathepsin D. Endocrinology 133, 935-938.
3. Benes, P., Koelsch, G., Dvorak, B., Fusek, M. and Vetvicka, V. (2002). Detection of procathepsin D in rat milk. Comp. Biochem. Physiol. B, Biochem. Mol. Biol. 133, 113-118.
4. Ben-Jonathan, N., Mershon, J. L., Allen, D. L. and Steinmetz, R. W. (1996). Extrapituitary prolactin: distribution, regulation, functions and clinical aspects. Endocr. Rev. 17, 639-669.
5. Berg, T., Gjöen, T. and Bakke, O. (1995). Physiological functions of endosomal proteolysis. Biochem. J. 307, 313-326.
6. Bidère, N., Lorenzo, H. K., Carmona, S., Laforge, M., Harper, F., Dumont, C. and Senik, A. (2003). Cathepsin D triggers Bax activation, resulting in selective AIF relocation in T lymphocytes entering the early commitment phase to apoptosis. J. Biol. Chem. 278, 31401-31411.
7. Bole-Feysot, C., Goffin, V., Edery, M., Binart, N. and Kelly, P. A. (1998). Prolactin (PRL) and its receptor actions, signal transduction pathways and phenotypes observed in PRL receptor knockout mice. Endocr. Rev. 19, 225-268.
8. Capony, F., Rougeot, V., Montrourrier, 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, 3904-3905.
9. 2+-dependent exocytosis of lysosomes. J. Cell Sci. 117, 1065-1077.
10. Chiarpotto, E., Domenicotti, C., Paola, D., Vitali, A., Nitti, M. P., Pronzato, M. A., Biasi, F., Cottalasso, D., Marinari, U. M., Dragonetti, A. et al. (1999). Regulation of rat hepatocyte protein kinase C β-isoenzymes by the lipid peroxidation product 4-hydroxy-2,3-nonenal: signal pathway to modulate vesicular transport of glycoproteins. Hepatology 29, 1565-1572.
11. Clapp, C. (1987). Analysis of the proteolytic cleavage of prolactin by the mammary gland and liver of the rat: characterization of the cleaved and 16K forms. Endocrinology 121, 2055-2064.
12. Clapp, C., Martial, J. A., Guzman, R. C., Rentier-Delrue, F. and Weiner, R. I. (1993). The 16-kilodalton N-terminal fragment of human prolactin is a potent inhibitor of angiogenesis. Endocrinology 133, 1292-1299.
13. Corbacho, A. M., Martinez de la Escalera, G. and Clapp, C. (2002). Roles of prolactin and related members of the prolactin/growth hormone/placental lactogen family in angiogenesis. J. Endocrinol. 173, 219-238.
14. Daudet, F., Augeron, C. and Ollivier-Bousquet, M. (1981). Effet rapide in vitro de la colchicine, du chlorure d'ammonium et de la prolactine sur la sécrétion des lipides du lait dans la glande mammaire. Eur. J. Cell Biol. 24, 197-202.
15. Demoz, M., Castino, R., Dragonetti, A., Raiteri, E., Baccino, F. M. and Isidoro, C. (1999). Transformation by oncogenic ras-p21 alters the processing and subcellular localization of the lysosomal protease cathepsin D. J. Cell Biochem. 73, 370-378.
16. De Stefanis, D., Demoz, M., Dragonetti, A., Houri, J. J., Ogier-Denis, E., Codogno, P., Bacino, F. M. and Isidoro, C. (1997). Differenciation-induced changes in the content, secretion and subcellular distribution of lysosomal cathepsins in the human colon cancer HT-29 cell line. Cell Tissue Res. 289, 109-117.
17. Devinoy, E., Stinnakre, M.-G., Lavialle, F., Thépot, D. and Ollivier-Bousquet, M. (1995). Intracellular routing and release of caseins and growth hormone produced into milk from transgenic mice. Exp. Cell. Res. 221, 272-280.
18. Dragonetti, A., Baldassarre, M., Castino, R., Demoz, M., Luini, A., Buccione, R. and Isidoro, C. (2000). The lysosomal protease cathepsin D is efficiently sorted to and secreted from regulated secretory components in the rat basophilic/mast cell line RBL. J. Cell. Sci. 113, 3289-3298.
19. Ellis, L. A. and Picciano, M. F. (1995). Bioactive and immunoreactive prolactin variants in human milk. Endocrinology 136, 2711-2720.
20. Ferrara, N., Clapp, C. and Weiner, R. (1991). The 16K fragment of prolactin specifically inhibits basal or fibroblast growth factor stimulated growth of capillary endothelial cells. Endocrinology 129, 896-900.
21. Freeman, M. E., Kanyicska, B., Lerant, A. and Nagy, G. (2000). Prolactin: structure, function and regulation of secretion. Phys. Rev. 80, 1523-1631.
22. Goffin, V., Binart, N., Touraine, P. and Kelly, P. A. (2002). Prolactin: the new biology of an old hormone. Annu. Rev. Physiol. 64, 47-67.
23. Hasilik, A. and Neufeld, E. F. (1980). Biosynthesis of lysosomal enzymes in fibroblasts. Synthesis as precursors of higher molecular weight. J. Biol. Chem. 255, 4937-4945.
24. Hennighausen, L., Robinson, G. W., Wagner, K. U. and Liu, W. (1997). Prolactin signaling in mammary gland development. Biol. Chem. 272, 7567-7569.
25. Isidoro, C., Mesiti, A., Bonelli, G., Tessitore, L., Hasilik, A. and Baccino, F. M. (1991). Synthesis and secretion of cathepsin D in normal and tumor human cells. In Chemical Carcinogenesis, Vol. 2 (ed. A. Columbano, F. Feo, R. Pascale and P. Panis), pp. 409-418. New York, NY: Plenum Publishing.
26. Isidoro, C., Demoz, M., de Stefanis, D., Mainferme, F., Wattiaux, R. and Baccino, F. M. (1995a). Altered intracellular processing and enhanced secretion of procathepsin D in a highly-deviated rat hepatoma. Int. J. Cancer 61, 60-64.
27. Isidoro, C., Demoz, M., de Stefanis, D., Baccino, F. M. and Bonelli, G. (1995b). Synthesis, maturation and extracellular release of procathepsin D as influenced by cell proliferation or transformation. Int. J. Cancer 63, 866-871.
28. Isidoro, C., Demoz, M., de Stefanis, D., Baccino, F. M., Hasilik, A. and Bonelli, G. (1997a). Differential targeting and processing of procathepsin D in normal and transformed murine 3T3 fibroblasts. Int. J. Cancer 70, 10-314.
29. Isidoro, C., Baccino, F. M. and Hasilik, A. (1997b). Mis-sorting of procathepsin D in metastogenic tumor cells is not due to impaired synthesis of the phosphomannosyl signal. Int. J. Cancer 70, 561-566.
30. Khurana, S., Liby, K., Buckley, A. R. and Ben-Jonathan, N. (1999). Proteolysis of human prolactin: resistance to cathepsin D and formation of a nonangiostatic, C-terminal 16K fragment by thrombin. Endocrinology 140, 4127-4132.
31. Larsen, L. B. and Petersen, T. E. (1995). Identification of five molecular forms of cathepsin D in bovine milk. Adv. Exp. Med. Biol. 362, 279-283.
32. Lee, H., Struman, I., Clapp, C., Martial, J. and Weiner, R. I. (1998). Inhibition of urokinase activity by the antiangiogenic factor 16K prolactin: activation of plasminogen activator inhibitor 1 expression. Endocrinology 139, 3696-3703.
33. Lkhider, M., Delpal, S. and Ollivier-Bousquet, M. (1996). Rat prolactin in serum, milk and mammary tissue: characterisation and intracellular localisation. Endocrinology 137, 4969-4979.
34. Lkhider, M., Delpal, S., le Provost, F. and Ollivier-Bousquet, M. (1997). Rat prolactin synthesis by lactating mammary epithelial cells. FEBS Lett. 401, 117-122.
35. Lkhider, M., Petridou, B., Aubourg, A. and Ollivier-Bousquet, M. (2001). Prolactin signalling to milk protein secretion but not to gene expression depends on the integrity of the Golgi region. J. Cell. Sci. 114, 1883-1891.
36. Martini, J. F., Piot, C., Humeau, L. M., Struman, I., Martial, J. A. and Weimer, R. I. (2000). The anti-angiogenic factor 16K PRL induces programmed cell death in endothelial cells by caspase activation. Mol. Endocrinol. 14, 1536-1549.
37. Ollivier-Bousquet, M. (1980). Effet des agents lysosomotropes sur la stimulation par la prolactine de la sé crétion des protéines du lait. Biol. Cell. 39, 21-30.
38. Ollivier-Bousquet, M. (1998). Transferrin and prolactin transcytosis in lactating mammary epithelial cell. J. Mam. Gland Biol. Neoplasia 3, 303-313.
39. Pauloin, A., Delpal, S., Chanat, E., Lavialle, F., Aubourg, A. and Ollivier-Bousquet, M. (1997). Brefeldin A differently affects basal and prolactin-stimulated milk protein secretion in lactating rabbit mammary epithelial cells. Eur. J. Cell Biol. 72 324-336.
40. Radons, J., Isidoro, C. and Hasilik, A. (1990). Brefeldin A prevents uncovering but not phosphorylation of the recognition marker in Cathepsin D. Biol. Chem. Hoppe-Seyler 371 567-573.
41. Richert, M. M., Schwertfeger, K. L., Ryder, J. W. and Anderson, S. M. (2000). An atlas of mouse mammary gland development. J. Mam. Gland Biol. Neoplasia 5, 227-241.
42. Rochefort, H. and Liaudet-Coopman, E. (1999). Cathepsin D in cancer metastatis, a protease and a ligand. APMIS 107, 86-95.
43. Seddiki, T. and Ollivier-Bousquet, M. (1991). Temperature dependence of prolactin endocytosis and casein exocytosis in epithelial mammary cells. Eur. J. Cell Biol. 55, 60-70.
44. Seddiki, T., Delpal, S., Aubourg, A., Durand, G. and Ollivier-Bousquet, M. (2002). Endocytic prolactin routes to the secretory pathway in lactating mammary epithelial cells. Biol. Cell 94, 173-185.
45. Sinha, Y. N. (1995). Structural variants of prolactin: occurence and physiological significance. Endocr. Rev. 16, 354-369.
46. Struman, Z., Bentzien, F., Lee, H., Mainfroid, V., D'Angelo, G., Goffin, V., Weiner, R. I. and Martial, J. A. (1999). Opposing actions of intact and N-terminal fragments of the human prolactin/growth hormone family members on angiogenesis: an efficient mechanism for the regulation of angiogenesis. Proc. Natl Acad. Sci. USA 96, 1246-1251.
47. Von Figura, K. and Hasilik, A. (1986). Lysosomal enzymes and their receptors. Annu. Rev. Biochem. 55, 167-193.
48. Warner, M. D., Sinha, Y. N. and Peabody, C. A. (1993). Growth hormone and prolactin variants in normal subjects. Horm. Metab. Res. 25, 425-429.
49. Wong, V. L. Y., Compton, M. M. and Witorsch, R. J. (1986). Proteolytic modification of rat prolactin by subcellular fractions of the lactating rat mammary gland. Biochim. Biophys. Acta 881, 167-174.