Localization of cathepsins D and B at the maternal-fetal interface and the invasiveness of the trophoblast during the postimplantation period in the mouse

Cells Tissues Organs

Volumn 193, Issue 6, 2011, Pages 417-425

  Amarante Paffaro, A M ^a,b,c   Hoshida, M S ^b   Yokota, S ^d   Goncalves C R ^b   Joazeiro, P P ^a   Bevilacqua, E ^b   Yamada, A T ^a  

^a UNIVERSITY OF CAMPINAS   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c FEDERAL UNIVERSITY OF ALFENAS   (Brazil)

^d UNIVERSITY OF YAMANASHI   (Japan)

Author keywords

Cathepsin B; Cathepsin D; Ectoplacental cone; Lysosomal proteinases; Phagocytosis; Placenta

Indexed keywords

CATHEPSIN B; CATHEPSIN D;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ENDOMETRIUM CELL; EXTRACELLULAR MATRIX; FEMALE; GIANT CELL; IMMUNOHISTOCHEMISTRY; IMMUNOLOCALIZATION; MOUSE; NIDATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TROPHOBLAST;

ANIMALS; CATHEPSIN B; CATHEPSIN D; CELL MOVEMENT; EMBRYO IMPLANTATION; FEMALE; IMMUNOHISTOCHEMISTRY; MATERNAL-FETAL EXCHANGE; MICE; PREGNANCY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TROPHOBLASTS;

MURINAE;

EID: 79956152108     PISSN: 14226405     EISSN: 14226421     Source Type: Journal    
DOI: 10.1159/000320546     Document Type: Article

References (72)

1. Abraham, R., R. Hendy, W. J. Dougherty, J. C. Fulfs, L. Golberg (1970) Participation of lysosomes in early implantation in the rabbit. Exp Mol Pathol 13:329-345.
2. Abrahamsohn, P. A., T. M. Zorn (1993) Implantation and decidualization in rodents. J Exp Zool 266:603-628.
3. Afonso, S., L. Romagnano, B. Babiarz (1997) The expression and function of cystatin C and cathepsin B and cathepsin L during mouse embryo implantation and placentation. Development 124:3415-3425. (Pubitemid 27440456)
4. Afonso, S., L. Romagnano, B. Babiarz (1999) Expression of cathepsin proteinases by mouse trophoblast in vivo and in vitro. Dev Dyn 216:374-384.
5. Afonso S., C. Tovar, L. Romagnano, B. Babiarz (2002) Control and expression of cystatin C by mouse decidual cultures. Mol Reprod Dev 61:155-163. (Pubitemid 34037467)
6. Alexander, C. M., E. J. Hansell, O. Behrendtsen, M. L. Flannery, N. S. Kishnani, S. P. Hawkes, Z. Werb (1996) Expression and function of matrix metalloproteinases and their inhibitors at the maternal-embryonic boundary during mouse embryo implantation. Development 122:1723-1736. (Pubitemid 26192738)
7. Baston-Buest, D. M., A. Schanz, S. Buest, J. C. Fischer, J. S. Kruessel, A. P. Hess (2010) The embryo's cystatin C and F expression functions as a protective mechanism against the maternal proteinase cathepsin S in mice. Reproduction 139:741-748.
8. Behrendtsen, O., C. M. Alexander, Z. Werb (1992) Metalloproteinases mediate extracellular matrix degradation by cells from mouse blastocyst outgrowths. Development 114:447-456.
9. Bevilacqua, E., P. A. Abrahamsohn (1988) Ultrastructure of trophoblast giant cell transformation during the invasive stage of implantation of the mouse embryo. J Morphol 198:341-351. (Pubitemid 19108643)
10. Bevilacqua, E., P. A. Abrahamsohn (1989) Trophoblast invasion during implantation of the mouse embryo. Arch Biol Med Exp 22:107-118. (Pubitemid 19257596)
11. Bevilacqua, E., M. S. Hoshida, A. Amarante-Paffaro, A. Albieri-Borges, S. Zago-Gomes (2010) Trophoblast phagocytic program: roles in different placental systems. Int J Dev Biol 54:495-505.
12. Bischof P., M. Martelli, A. Campana, Y. Itoh, Y. Ogata, H. Nagase (1995) Importance of matrix metalloproteinases in human trophoblast invasion. Early Pregnancy 1:263-269.
13. Blankenship, T. N., R. L. Given (1992) Penetration of the uterine epithelial basement membrane during blastocyst implantation in the mouse. Anat Rec 233:196-204.
14. Briozzo, P., M. Morisset, F. Capony, C. Rougeot, H. Rochefort (1988) In vitro degradation of extracellular matrix with M r 52, 000 cathepsin D secreted by breast cancer cells. Cancer Res 48:3688-3692.
15. Cohen, M., P. Bischof (2007) Factors regulating trophoblast invasion. Gynecol Obstet Invest 64:126-130. (Pubitemid 47574869)
16. Creemers, L. B., K. A. Hoeben, D. C. Jansen, D. J. Buttle, W. Beertsen, V. Everts (1998) Participation of intracellular cysteine proteinases, in particular cathepsin B, in degradation of collagen in periosteal tissue explants. Matrix Biol 16:575-584. (Pubitemid 28165735)
17. Denker, H. W. (1977) Implantation: the role of proteinases, and blockage of implantation by proteinase inhibitors. Adv Anat Embryol Cell Biol 53 Fasc. 5:3-123.
18. Denker, H. W. (1980) Role of proteinases in implantation. Prog Reprod Biol 7:28-42.
19. Denker, H. W. (1982) Proteases of the blastocyst and of the uterus; in Beier, H. M., P. Karlson (eds): Proteins and Steroids in Early Pregnancy. Berlin, Springer, pp 183-208.
20. Denker, H. W., L. A. Eng, C. E. Hamner (1978) Studies on the early development and implantation in the cat. 2. Implantation: proteinases. Anat Embryol 154:39-54. (Pubitemid 8383408)
21. Denker, H. W., C. H. Tyndale-Biscoe (1986) Embryo implantation and proteinase activities in a marsupial (Macropus eugenii): histochemical patterns of proteinases in various gestational stages. Cell Tissue Res 246:279-291. (Pubitemid 16026770)
22. Dickson, A. D. (1966) The form of the mouse blastocyst. J Anat 100:29-68.
23. Dong, Z., M. Katar, B. E. Linebaugh, B. F. Sloane, R. S. Berk (2001) Expression of cathepsins B, D and L in mouse corneas infected with Pseudomonas aeruginosa. Eur J Biochem 268:6408-6416. (Pubitemid 34014748)
24. Ebert, W., H. Knoch, B. Werle, G. Trefz, T. Muley, E. Spiess (1994) Prognostic value of increased lung tumor tissue cathepsin B. Anticancer Res 14:895-899. (Pubitemid 24272541)
25. Elangovan, S., B. C. Moulton (1980) Blastocyst implantation in the rat and the immunohistochemical distribution and rate of synthesis of uterine lysosomal cathepsin D. Biol Reprod 23:663-668. (Pubitemid 11211968)
26. Enders A. C., A. O. Welsh (1993) Structural interactions of trophoblast and uterus during hemochorial placenta formation. J Exp Zool 266:578-587.
27. Enders, A. C., S. Schlafke (1969) Cytological aspects of trophoblast-uterine interaction in early implantation. Am J Anat 125:1-29.
28. Fazleabas, A. T., P. D. Geisert, F. W. Barer, P. M. Roberts (1983) Relationship between release of plasminogen activator and estrogen by blastocysts and secretion of plasmin inhibitor by uterine endometrium in the pregnant pig. Biol Reprod 29:225-238.
29. Gan, Y., X. Zhao, J. Hu, Z. G. Wang, X. T. Zhao (2008) HCCS1 overexpression induces apoptosis via cathepsin D and intracellular calcium, and HCCS1 disruption in mice causes placental abnormality. Cell Death Differ 15:1481-1490.
30. Georgiades, P., A. C. Ferguson-Smith, G. J. Burton (2002) Comparative developmental anatomy of the murine and human definitive placentae. Placenta 23:3-19. (Pubitemid 41110436)
31. Glass, R. H., J. Aggeler, A. Spindle, R. A. Pederson, Z. Werb (1983) Degradation of extracellular matrix by mouse trophoblast outgrowths: a model for implantation. J Cell Biol 96:1108-1116. (Pubitemid 13083493)
32. Graham, C. H., P. K. Lala (1992) Mechanism of placental invasion of the uterus and their control. Biochem Cell Biol 70:867-874.
33. Gu, Y., G. M. Jow, B. C. Moulton, C. Lee, J. A. Sensibar, O. K. Park-Sarge, T. J. Chen, G. Gibori (1994) Apoptosis in decidual tissue regression and reorganization. Endocrinology 135:1272-1279. (Pubitemid 24271226)
34. Henskens, Y. M., E. C. Veerman, A. V. Nieuw Amerongen (1996) Cystatins in health and disease. Biol Chem Hoppe Seyler 377:71-86. (Pubitemid 26089038)
35. Heylen, N., L. M. Vincent, V. Devos, V. Dubois, C. Remacle, A. Trouet (2002) Fibroblasts capture cathepsin D secreted by breast cancer cells: possible role in the regulation of the invasive process. Int J Oncol 20:761-767.
36. Hoshida, M. S., R. Gorjão, C. Lima, S. Daher, R. Curi, E. Bevilacqua (2007) Regulation of gene expression in mouse trophoblast cells by interferon-gamma. Placenta 28:1059-1072. (Pubitemid 47370900)
37. Hu, L., J. M. Roth, P. Brooks, J. Luty, S. Karpatkin (2008) Thrombin up-regulates cathepsin D which enhances angiogenesis, growth, and metastasis. Cancer Res 68:4666-4673.
38. Jokimaa, V., S. Oksjoki, H. Kujari, E. Vuorio, L. Anttila (2001) Expression patterns of cathepsins B, H, K, L and S in the human endometrium. Mol Hum Reprod 7:73-78. (Pubitemid 32101767)
39. Joswig, A., H. D. Gabriel, M. Kibschull, E. Winterhager (2003) Apoptosis in uterine epithelium and decidua in response to implantation: evidence for two different pathways. Reprod Biol Endocrinol 1:44.
40. Kliman H. J., R. E. Feimberg (1990) Human trophoblastextracellular matrix (ECM) interactions in vitro: ECM thickness modulates morphology and proteolytic activity. Proc Natl Acad Sci USA 87:3057-3061.
41. Li, W. G., R. C. Jaffe, A. T. Fazleabas, H. G. Verhage (1991) Progesterone-dependent cathepsin L proteolytic activity in cat uterine flushings. Biol Reprod 44:625-631.
42. Liaudet-Coopman, E., M. Beaujouin, D. Derocq, M. Garcia, M. Glondu-Lassis, V. Laurent-Matha, C. Prébois, H. Rochefort, F. Vignon (2006) Cathepsin D: newly discovered functions of a long-standing aspartic protease in cancer and apoptosis. Cancer Lett 237:167-179. (Pubitemid 43777078)
43. Lkhider, M., R. Castino, E. Bouguyon, C. Isidoro, M. Ollivier-Bousquet (2004) Cathepsin D released by lactating rat mammary epithelial cells is involved in prolactin cleavage under physiological conditions. J Cell Sci 117:5155-5164. (Pubitemid 39517530)
44. Lyons, R. M., L. E. Gentry, A. F. Purchio, H. L. Moses (1990) Mechanism of activation of latent recombinant transforming growth factor beta 1 by plasmin. J Cell Biol 110:1361-1367.
45. Moulton, B. C. (1974) Ovum implantation and uterine lysosomal enzyme activity. Biol Reprod 10:543-548.
46. Moulton, B. C., B. B. Koenig, S. C. Borkan (1978) Uterine lysosomal enzyme activity during ovum implantation and early decidualization. Biol Reprod 19:167-170. (Pubitemid 8392741)
47. Müntener, M., Y. C. Hsu (1977) Development of trophoblast and placenta of the mouse: a reinvestigation with regard to the in vitro culture of mouse trophoblast and placenta. Acta Anat 98:241-252. (Pubitemid 8132724)
48. Mylonas, I., J. Makovitzky, D. U. Richter, U. Jeschke, V. Briese, K. Friese (2003) Cathepsin D expression in normal, hyperplastic and malignant endometrial tissue: an immunohistochemical analysis. Acta Histochem 105:245-252. (Pubitemid 37046257)
49. Nakanishi, T., Y. Ozaki, K. Blomgren, H. Tateyama, M. Sugiura-Ogasawara, K. Suzumori (2005) Role of cathepsins and cystatins in patients with recurrent miscarriage. Mol Hum Reprod 11:351-355. (Pubitemid 41417868)
50. Owers, N. O. (1971) Ingestive properties of guinea pig trophoblast grown in tissue culture: a possible lysosomal mechanism; in Blandau, R. J. (ed): The Biology of the Blastocyst. Chicago, The University of Chicago Press, pp 225-241.
51. Owers, N. O., R. J. Blandau (1971) Proteolytic activity of the rat and guinea pig blastocyst in vitro; in Blandau, R. J. (ed): The Biology of the Blastocyst. Chicago, The University of Chicago Press, pp 207-223.
52. Parr, E. L., H. N. Tung, M. B. Parr (1987) Apoptosis as the mode of uterine epithelial cell death during embryo implantation in mice and rats. Biol Reprod 36:211-225.
53. Piwnica, D., I. Fernandez, N. Binart, P. Touraine, P. A. Kelly, V. Goffin (2006) A new mechanism for prolactin processing into 16K PRL by secreted cathepsin D. Mol Endocrinol 20:3263-3278. (Pubitemid 44833570)
54. Rageh, M. A., E. E. Moussad, A. K. Wilson, D. R. Brigstock (2001) Steroidal regulation of connective tissue growth factor (CCN2; CTGF) synthesis in the mouse uterus. Mol Pathol 54:338-346. (Pubitemid 32928261)
55. Scambia, G., P. B. Panici, G. Ferradina, G. Salerno, G. D'Agostino, M. Distefano, R. De Vicenso, A. Ercolli, S. Mancuso (1994) Clinical significance of cathepsin D in primary ovarian cancer. Eur J Cancer 30:935-940. (Pubitemid 24256238)
56. Schultz, D. C., S. Bazel, L. M. Wright, S. Tucker, M. K. Lange, T. Tachovsky, S. Longo, S. Niedbala, J. A. Alhadeff (1994) Western blotting and enzymatic activity analysis of cathepsin D in breast tissue and sera of patients with breast cancer and benign breast disease and of normal controls. Cancer Res 54:48-54. (Pubitemid 24042087)
57. Screen, M., W. Dean, J. C. Cross, M. Hemberger (2008) Cathepsin proteases have distinct roles in trophoblast function and vascular remodeling. Development 135:3311-3320.
58. Sharma, R. K. (1998) Mouse trophoblastic cell lines: 2. Relationship between invasive potential and proteases. In Vivo 12:209-218.
59. Shimonovitz, S., A. Hurwitz, M. Dushnik, E. Anteby, T. Geva-Eldar, S. Yagel (1994) Developmental regulation of the expression of 72 and 92 kd type IV collagenases in human trophoblasts: a possible mechanism for control of trophoblast invasion. Am J Obstet Gynecol 171:832-838. (Pubitemid 24312373)
60. Simmons, D. G., A. L. Fortier, J. C. Cross (2007) Diverse subtypes and developmental origins of trophoblast giant cells in the mouse placenta. Dev Biol 304:567-578. (Pubitemid 46533975)
61. Skrzydlewska, E., M. Sulkowska, M. Koda, S. Sulkoski (2005) Proteolytic-antiproteolytic balance and its regulation in carcinogenesis. World J Gastroenterol 11:1251-1266. (Pubitemid 40425906)
62. Soares, M. J., T. Konno, S. M. K. Alam (2007) The prolactin family: effectors of pregnancy-specific adaptations. Trends Endocrinol Metab 18:114-121. (Pubitemid 46464021)
63. Song, G., D. W. Bailey, K. A. Dunlap, R. C. Burghardt, T. E. Spencer, F. W. Bazer, G. A. Johnson (2010) Cathepsin B, cathepsin L and cystatin C in the porcine uterus and placenta: potential roles in endometrial/placental remodeling and in fluid-phase transport of proteins secreted by uterine epithelia across placental areolae. Biol Reprod 82:854-864.
64. Song, G., F. W. Bazer, T. E. Spencer (2007) Differential expression of cathepsins and cystatin C in ovine uteroplacental tissues. Placenta 28:1091-1098. (Pubitemid 47355235)
65. Sukoh, N., S. Abe, S. Ogura, H. Isobe, H. Takekawa, K. Inoue, Y. Kawakami (1994) Immunohistochemical study of cathepsin B: prognostic significance in human lung cancer. Cancer 74:46-51. (Pubitemid 24187608)
66. Talieri, M., S. Papadopoulou, A. Scorilas, D. Xynopoulos, N. Arnogianaki, G. Plataniotis, J. Yotis, N. Agnanti (2004) Cathepsin B and cathepsin D expression in the progression of colorectal adenoma to carcinoma. Cancer Lett 205:97-106. (Pubitemid 38230144)
67. Teesalu, T., F. Blasi, D. Talarico (1998) Expression and function of the urokinase type plasminogen activator during mouse hemochorial placental development. Dev Dyn 213:27-38. (Pubitemid 28394905)
68. Teesalu, T., R. Masson, P. Basset, F. Blasi, D. Talarico (1999) Expression of matrix metalloproteinases during murine chorioallantoic placenta maturation. Dev Dyn 214:248-258. (Pubitemid 29117585)
69. Weisinger, G., M. Gavish, C. Mazurika, O. Zinder (1999) Transcription of actin, cyclophilin and glyceraldehyde phosphate dehydrogenase genes: tissue-and treatmentspecificity. Biochim Biophys Acta 1446:225-232. (Pubitemid 29401895)
70. Welsh, A. O., A. C. Enders (1987) Trophoblast-decidual cell interaction and establishment of maternal blood circulation in the parietal yolk sac placenta of the rat. Anat Rec 217:203-219. (Pubitemid 17017641)
71. Yokota, S., H. Tsuji, K. Kato (1985) Immunocytochemical localization of cathepsin D in lysosomes of cortical collecting tubule cells of the rat kidney. J Histochem Cytochem 33:191-200. (Pubitemid 15130007)
72. Yokota, S., H. Tsuji, K. Kato (1986) Immunocytochemical localization of cathepsin B in rat kidney. 1. Light microscopic study using the indirect immunoenzyme technique. J Histochem Cytochem 34:891-897. (Pubitemid 16067458)