Parathyroid hormone-related protein signaling is necessary for sexual dimorphism during embryonic mammary development

Development

Volumn 126, Issue 16, 1999, Pages 3485-3493

  Dunbar, Maureen E ^a   Dann, Pamela R ^a   Robinson, Gertraud W ^b   Hennighausen, Lothar ^b   Zhang, Jian Ping ^a   Wysolmerski, John J ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

Androgen receptor; Apoptosis; Epithelial mesenchymal interaction; Mouse; PTH PTHrP receptor; Tenascin C

Indexed keywords

ANDROGEN; ANDROGEN RECEPTOR; CELL MARKER; PARATHYROID HORMONE RELATED PROTEIN; TENASCIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; BREAST DEVELOPMENT; BREAST EPITHELIUM; CELL FATE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EPIDERMIS; FEMALE; GENE OVEREXPRESSION; KNOCKOUT MOUSE; MALE; MAMMARY GLAND; MESENCHYME; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEX DIFFERENCE; TRANSGENE;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; APOPTOSIS; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HETEROZYGOTE; MALE; MAMMARY GLANDS, ANIMAL; MESODERM; MICE; MICE, KNOCKOUT; PARATHYROID HORMONE-RELATED PROTEIN; PROTEINS; RECEPTOR, PARATHYROID HORMONE, TYPE 1; RECEPTORS, ANDROGEN; RECEPTORS, PARATHYROID HORMONE; SEX CHARACTERISTICS; TENASCIN;

ANIMALIA; MAMMALIA;

EID: 0032842385     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (43)

1. Behrendtsen, O., Alexander, C. M. and Werb, Z. (1995). Cooperative interactions between extracellular matrix, integrins and parathyroid hormone-related peptide regulate parietal endoderm differentiation in mouse embryos. Development 121, 4137-4146.
2. Birchmeier, C. and Birchmeier, W. (1993). Molecular aspects of mesenchymal-epithelial interactions. Ann. Rev. Cell Biol. 9, 511-540.
3. Chen, F. and Capecchi, M. D. (1999). Paralogous mouse Hox genes Hoxa 9, Hoxb 9, and Hoxd 9, function together to control development of the mammary gland in response to pregnancy. Proc. Natl Acad. Sci. USA 96, 541-546.
4. Chung, V., Lanske, B., Lee, K., Li, E. and Kronenberg, H. (1998). The parathyroid hormone/parathyroid hormone-related peptide receptor coordinates endochondral bone development by directly controlling chondrocyte differentiation. Proc. Natl Acad. Sci. USA 95, 13030-13035.
5. Cunha, G. R. (1994). Role of mesenchymal-epithelial interactions in normal and abnormal development of the mammary gland and prostate. Cancer 74, 1030-1044.
6. Cunha, G. R., Young, P., Christov, K., Guzman, R., Nandi, J., Talamsutes, F. and Thorderson, G. (1995). Mammary phenotypic expression induced in epidermal cells by embryonic mammary mesenchyme. Acta Anat. 152, 195-204.
7. Cunha, G. R. and Horn, Y. K. (1996). Role of mesenchymal-epithelial interactions in mammary gland development. J. Mamm. Gland Biol. Neopl. 1, 21-35.
8. de Stolpe, A., Karperian, M., Lowik, C. W. G. M., Jüppner, H., Segre, G. V., Abou-Samra, A. B., deLaat, S. W. and Defize, L. H. K. (1993). Parathyroid hormone-related peptide as an endogenous inducer of parietal endoderm differentiation. J. Cell Biol. 120, 235-243.
9. Dunbar, M. E., Young, P., Zhang, J. P., McCaughern-Carucci, J., Lanske, B., Orloff, J. J., Karaplis, A., Cunha, G. and Wysolmerski, J. J. (1998). Stromal cells are critical targets in the regulation of mammary ductal morphogenesis by parathyroid hormone-related protein. Dev. Biol. 203, 75-89.
10. Erickson, H. P. and Bourdon M. A. (1989). Tenascin: an extracellular matrix protein prominent in specialized embryonic tissues and tumors. Annual Rev. Cell Biol. 5, 71-92.
11. Gilbert, S. F. (1994). Sex determination. In Developmental Biology pp. 754-787. Sunderland, MA: Sinauer Associates.
12. Grumbach, M. M. and Conte, F. A. (1992). Disorders of sex differentiation. In Williams Textbook of Endocrinology 8th Edition. (ed. J. D. Wilson and D. W. Foster) pp. 853-952. Philadelphia, PA: W. B. Saunders Co.
13. Heuberger, B., Fitzka, I., Wasner, G. and Kratochwil, K. (1982). Induction of androgen receptor formation by epithelial-mesenchymal interaction in embryonic mouse mammary gland. Proc. Natl Acad. Sci. USA 79, 2957-2961.
14. Hoshino, K. (1965). Development and function of mammary glands of mice prenatally exposed to testosterone propionate. Endocrinology 76, 789-794.
15. Inaguma, Y., Kusakabe, M., Mackie, E. J., Pearson, C. A., Chiquet-Ehrisman, R. and Sakakura, T. (1988). Epithelial induction of stromal tenascin in the mouse mammary gland: from embryogenesis to carcinogenesis. Dev. Biol. 128, 245-255.
16. Jüppner, H., Abou-Samra, A. B., Freeman, M., Kong, X. F., Schipani, E., Richards, J., Kolakowski, L. F., Hock, J., Potts, J. T., Kronenberg, H. M. and Segre, G. V. (1991). A G protein-linked receptor for parathyroid hormone and parathyroid hormone-related peptide. Science 254, 1024-1026.
17. Kalembey, I., Yoshida, T., Iriyama, K. and Sakakura, T. (1997). Analysis of tenascin mRNA expression in the murine mammary gland from embryogenesis to carcinogenesis: an in situ hybridization study. Int. J. Dev. Biol. 41, 569-573.
18. Kopan, R. and Fuchs, E. (1989). A new look at an old problem: keratins as tools to investigate determination morphogenesis and differentiation in skin. Genes Dev. 3, 1-15.
19. Kratochwil, K. (1977). Development and loss of androgen responsiveness in the embryonic mammary rudiment of the mouse mammary gland. Dev. Biol. 61, 358-365.
20. Kratochwil, K and Schwartz, P. (1977). Tissue interaction in androgen response of embryonic mammary rudiment of mouse: identification of target tissue for testosterone. Proc. Natl Acad. Sci. USA 73, 4041-4044.
21. Kratochwil, K., Dull, M., Farinas, I., Galceran, J. and Grosschedl, R. ( 1996). Let1 expression is activated by BMP-4 and regulates inductive tissue interactions in tooth and hair development. Genes Dev. 10,1382-1394.
22. Lee, K., Deeds, J. D. and Segre, G. V. (1995). Expression of parathyroid hormone-related peptide and its receptor messenger ribonucleic acids during fetal development of rats. Endocrinol. 136, 453-463.
23. Majdic, G., Millar, M. R. and Saunders, P. T. K. (1995). Immunolocalization of androgen receptor to interstitial cells in fetal rat testes and to mesenchymal and epithelial cells of associated ducts. J Endocrinol. 147,285-293.
24. Neumann, F., Berswordt-Wallrabe, Elger, W., Steinbech, H., Hahn, J. D. and Kramer, M. (1970). Aspects of androgen-dependent events as studied by anti-androgens. Recent Prog. Horm. Res. 26, 337-410.
25. Philbrick, W. M., Wysolmerski, J. J., Galbraith, S., Orloff, J. J., Yang, K. H., Vasavada, R. C., Weir, E. C., Broadus, A. E. and Stewart, A. F. (1996). Defining the roles of parathyroid hormone-related protein in normal physiology. Physiol. Rev. 76, 127-173.
26. Philbrick, W. M., Dreyer, B. E., Nakchbandi, I. A. and Karaplis A. C. (1998). Parathyroid hormone-related protein is required for tooth eruption. Proc. Natl Acad. Sci. USA 95, 11846-11851.
27. Phippard, D. J., Weber-Hall, S. J., Sharpe P. T., Naylor, H., Jayatalake, H., Mass, R., Woo, D., Roberts-Clark, D., Francis-West, P. H., Liu, Y. H., Maxson, R., Hill, R. E. and Dale, T. C. (1996). Regulation of Msx-1, Msx-2, Bmp-2 and Bmp-4 during foetal and postnatal mammary gland development. Development 122, 2729-2737.
28. Propper, A. and Gomot, L. (1967). Interactions tissulaires au cours de l'organogenèse de la gland mammaire de l'embryon de Lapin. C. R. Acad. Sci. Paris 264, 2573-2575.
29. Raynaud, A. (1949). Nouvelles observations sur l'appareil mammaire des foetus de souris provent de mères ayant reçu des injections de testostérone pendant la gestation. Annals Endocrin. 10, 54-62.
30. Raynaud, A. and Frilley, M. (1947). Destruction des glandes genitales de l'embryon de souris per une irradiation au moyen des rayon x, a l'aye de treizejours. Ann. Endocrinol. Paris 8, 400-419.
31. Robinson, G. W., Karpf, A. B. C. and Kratochwil, K. (1999). Regulation of mammary gland development by tissue interaction. J. Mamm. Gland Biol. Neopl. 4.
32. Rubin, L. P., Kifor, O., Hua, J., Brown, E. M. and Torday, J. S. (1994). Parathyroid hormone (PTH) and PTH-related protein stimulate surfactant phospholipid synthesis in rat fetal lung, apparently by a mesenchymalepithelial mechanism. Biochim. Biophys. Acta 1223, 91-100.
33. Saga, Y., Yagi, T., Ikawa, Y., Sakakura, T. and Aizawa, S. (1992) Mice develop normally without tenascin. Genes Dev. 6, 1821-1831.
34. Salmivirta, M., Elenius, K., Vaino, S., Hofen, V., Chiquet-Ehrisman, R., Thesleff, I. and Jalkanen, M. (1991). Syndecan from embryonic tooth mesenchyme hinds tenascin. J. Biol. Chem. 266, 7733-7739.
35. Sakakura, T. (1987). Mammary embryogenesis. In The Mammary Gland. Development, Regulation and Function, (ed. M. C. Neville, C. W. Daniel) pp 37-65. New York: Plenum Press.
36. Thesleff, I., Vaahtokari, A. and Partanen, A. M. (1995). Regulation of organogenesis. Common molecular mechanisms regulating the development of teeth and other organs. Int. J. Dev. Biol. 39, 35-50.
37. Turner, C. W. and Gomez, E. T. (1933). The normal development of the mammary gland of the male and female albino mouse. I. Intra-uterine. Bull. Mo. Agric. Exp. Stn 182, 3-20.
38. van Genderen, C., Okamura, R. M., Farinas, I., Quo, R., Parslow, T. G., Bruhn, L. and Grosschedl, R. (1994). Development of several organs that require inductive epithelial-mesenchymal interactions is impaired in LEF-1-deficient mice. Genes Dev. 8, 2691-2703.
39. Weil, M., Itin, A. and Keshet, E. (1995). A role for mesenchyme-derived tachykinins in tooth and mammary gland morphogenesis. Development 121, 2419-2428.
40. Wysolmerski, J. J., Broadus, A. E., Zhou, J., Fuchs, E., Milstone, L. M. and Philbrick, W. M. (1994). Overexpression of parathyroid hormone-related protein in the skin of transgenic mice interferes with hair follicle development. Proc. Natl Acad. Sci. USA 91, 1133-1137.
41. Wysolmerski, J. J., McCaughern-Carucci, J. F., Daifotis, A. G., Broadus, A. E. and Philbrick, W. M. (1995). Overexpression of parathyroid hormone-related protein or parathyroid hormone in transgenic mice impairs branching morphogenesis during mammary gland development. Development 121, 3539-3547.
42. Wysolmerski, J. J. and Stewart, A. F. (1998). The physiology of parathyroid hormone-related protein: an emerging role as a developmental factor. Ann. Rev. Physiol. 60, 431-460.
43. Wysolmerski, J. J., Philbrick, W. M., Dunbar, M. E., Lanske, B., Kronenberg, H., Karaplis, A. and Broadus, A. E. (1998). Rescue of the parathyroid hormone-related protein knockout mouse demonstrates that parathyroid hormone-related protein is essential for mammary gland development. Development 125, 1285-1294.