Dual roles for Id4 in the regulation of estrogen signaling in the mammary gland and ovary

Development (Cambridge)

Volumn 141, Issue 16, 2014, Pages 3159-3164

  Best, Sarah A ^a,b   Hutt, Karla J ^c,d   Fu, Nai Yang ^a,b   Vaillant, François ^a,b   Liew, Seng H ^c   Hartley, Lynne ^a   Scott, Clare L ^a,b,e   Lindeman, Geoffrey J ^a,b,e   Visvader, Jane E ^a,b  

^a WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c MONASH MEDICAL CENTRE   (Australia)

^d MONASH UNIVERSITY   (Australia)

^e ROYAL MELBOURNE HOSPITAL   (Australia)

Author keywords

Estrogen; ID proteins; Mammary gland; Mouse; Ovary

Indexed keywords

ESTROGEN; ID PROTEINS; MAMMARY GLAND; MOUSE; OVARY;

ANIMALS; BASE SEQUENCE; ESTROGEN RECEPTOR ALPHA; ESTROGENS; FEMALE; GENE DELETION; GENE EXPRESSION REGULATION; GRANULOSA CELLS; HEPATOCYTE NUCLEAR FACTOR 3-ALPHA; INHIBITOR OF DIFFERENTIATION PROTEINS; MAMMARY GLANDS, ANIMAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; OVARY; PROMOTER REGIONS, GENETIC; RECEPTORS, PROGESTERONE; SIGNAL TRANSDUCTION; UTERUS;

EID: 84905484543     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.108498     Document Type: Article

References (33)

1. Asselin-Labat, M.-L., Shackleton, M., Stingl, J., Vaillant, F., Forrest, N. C., Eaves, C. J., Visvader, J. E. and Lindeman, G. J. (2006). Steroid hormone receptor status of mouse mammary stem cells. J. Natl. Cancer Inst. 98, 1011-1014.
2. Asselin-Labat, M.-L., Sutherland, K. D., Barker, H., Thomas, R., Shackleton, M., Forrest, N. C., Hartley, L., Robb, L., Grosveld, F. G., van der Wees, J. et al. (2007). Gata-3 is an essential regulator of mammary-gland morphogenesis and luminal-cell differentiation. Nat. Cell Biol. 9, 201-209.
3. Asselin-Labat, M.-L., Vaillant, F., Sheridan, J. M., Pal, B., Wu, D., Simpson, E. R., Yasuda, H., Smyth, G. K., Martin, T. J., Lindeman, G. J. et al. (2010). Control of mammary stem cell function by steroid hormone signalling. Nature 465, 798-802.
4. Bedford, L., Walker, R., Kondo, T., van Crüchten, I., King, E. R. and Sablitzky, F. (2005). Id4 is required for the correct timing of neural differentiation. Dev. Biol. 280, 386-395.
5. Beger, C., Pierce, L. N., Kruger, M., Marcusson, E. G., Robbins, J. M., Welcsh, P., Welch, P. J., Welte, K., King, M.-C., Barber, J. R. et al. (2001). Identification of Id4 as a regulator of BRCA1 expression by using a ribozyme-library-based inverse genomics approach. Proc. Natl. Acad. Sci. USA 98, 130-135.
6. de Candia, P., Akram, M., Benezra, R. and Brogi, E. (2006). Id4 messenger RNA and estrogen receptor expression: inverse correlation in human normal breast epithelium and carcinoma. Hum. Pathol. 37, 1032-1041.
7. Dong, J., Huang, S., Caikovski, M., Ji, S., McGrath, A., Custorio, M. G., Creighton, C. J., Maliakkal, P., Bogoslovskaia, E., Du, Z. et al. (2011). ID4 regulates mammary gland development by suppressing p38MAPK activity. Development 138, 5247-5256.
8. Escudero, J. M., Haller, J. L., Clay, C. M. and Escudero, K. W. (2010). Microarray analysis of Foxl2 mediated gene regulation in the mouse ovary derived KK1 granulosa cell line: over-expression of Foxl2 leads to activation of the gonadotropin releasing hormone receptor gene promoter. J. Ovarian Res. 3, 4.
9. Frech, M., Halama, E., Tilli, M., Singh, B., Gunther, E., Chodosh, L., Flaws, J. and Furth, P. (2005). Deregulated estrogen receptor α expression in mammary epithelial cells of transgenic mice results in the development of ductal carcinoma in situ. Cancer Res. 65, 681-685.
10. Gresack, J. E. and Frick, K. M (2006). Effects of continuous and intermittent estrogen treatments on memory in aging female mice. Brain Res. 1115, 135-147.
11. Heyn, H., Engelmann, M., Schreek, S., Ahrens, P., Lehmann, U., Kreipe, H., Schlegelberger, B. and Beger, C. (2011). MicroRNA miR-335 is crucial for the BRCA1 regulatory cascade in breast cancer development. Int. J. Cancer 129, 2797-2806.
12. Hogg, K., Etherington, S. L, Young, J. M., McNeilly, A. S. and Duncan, W. C. (2010). Inhibitor of differentiation (Id) genes are expressed in the steroidogenic cells of the ovine ovary and are differentially regulated by members of the transforming growth factor-β family. Endocrinology 151, 1247-1256.
13. Hurtado, A., Holmes, K. A., Ross-Innes, C. S., Schmidt, D. and Carroll, J. S. (2011). FOXA1 is a key determinant of estrogen receptor function and endocrine response. Nat. Genet. 43, 27-33.
14. Johnson, A. L., Haugen, M. J. and Woods, D. C. (2008). Role for inhibitor of differentiation/deoxyribonucleic acid-binding (Id) proteins in granulosa cell differentiation. Endocrinology 149, 3187-3195.
15. Kerr, J. B., Duckett, R., Myers, M., Britt, K. L., Mladenovska, T. and Findlay, J. K. (2006). Quantification of healthy follicles in the neonatal and adult mouse ovary: evidence for maintenance of primordial follicle supply. Reproduction 132, 95-109.
16. Lasorella, A., Benezra, R. and Iavarone, A. (2014). The ID proteins: master regulators of cancer stem cells and tumour aggressiveness. Nat. Rev. Cancer 14, 77-91.
17. Liew, S. H., Drummond, A. E., Jones, M. E. and Findlay, J. K. (2010). The lack of estrogen and excess luteinizing hormone are responsible for the female ArKO mouse phenotype. Mol. Cell. Endocrinol. 327, 56-64.
18. Lim, E., Wu, D., Pal, B., Bouras, T., Asselin-Labat, M.-L., Vaillant, F., Yagita, H., Lindeman, G. J., Smyth, G. K. and Visvader, J. E. (2010). Transcriptome analyses of mouse and human mammary cell subpopulations reveal multiple conserved genes and pathways. Breast Cancer Res. 12, R21.
19. Molyneux, G., Geyer, F. C., Magnay, F.-A., McCarthy, A., Kendrick, H., Natrajan, R., MacKay, A., Grigoriadis, A., Tutt, A., Ashworth, A. et al. (2010). BRCA1 basallike breast cancers originate from luminal epithelial progenitors and not from basal stem cells. Cell Stem Cell 7, 403-417.
20. Myers, M., Britt, K. L., Wreford, N. G. M., Ebling, F.J. P. and Kerr, J. B. (2004). Methods for quantifying follicular numbers within the mouse ovary. Reproduction 127, 569-580.
21. Roldán, G., Delgado, L. and Musé, I. M. (2006). Tumoral expression of BRCA1, estrogen receptor alpha and ID4 protein in patients with sporadic breast cancer. Cancer Biol. Ther. 5, 505-510.
22. Shackleton, M., Vaillant, F., Simpson, K. J., Stingl, J., Smyth, G. K., Asselin-Labat, M.-L., Wu, L., Lindeman, G. J. and Visvader, J. E. (2006). Generation of a functional mammary gland from a single stem cell. Nature 439, 84-88.
23. Sharma, P., Knowell, A., Chinaranagari, S., Komaragiri, S., Nagappan, P., Patel, D., Havrda, M. C. and Chaudhary, J. (2013). Id4 deficiency attenuates prostate development and promotes PIN-like lesions by regulating androgen receptor activity and expression of NKX3.1 and PTEN. Mol. Cancer 12, 67.
24. Shehata, M., Teschendorff, A., Sharp, G., Novcic, N., Russell, I. A., Avril, S., Prater, M., Eirew, P., Caldas, C., Watson, C. J. et al. (2012). Phenotypic and functional characterisation of the luminal cell hierarchy of the mammary gland. Breast Cancer Res. 14, R134.
25. Sikder, H. A., Devlin, M. K., Dunlap, S., Ryu, B. and Alani, R. M. (2003). Id proteins in cell growth and tumourigenesis. Cancer Cell 3, 525-530.
26. Tanos, T., Rojo, L., Echeverria, P. and Brisken, C. (2012). ER and PR signaling nodes during mammary gland development. Breast Cancer Res. 14, 210.
27. Tilli, M. T., Frech, M. S., Steed, M. E., Hruska, K. S., Johnson, M. D., Flaws, J. A. and Furth, P. A. (2003). Introduction of estrogen receptor-α into the tTA/TAg conditional mouse model precipitates the development of estrogen-responsive mammary adenocarcinoma. Am. J. Pathol. 163, 1713-1719.
28. Visvader, J. (2009). Keeping abreast of the mammary epithelial hierarchy and breast tumorigenesis. Genes Dev. 23, 2563-2577.
29. Voss, A. K., Dixon, M. P., McLennan, T., Kueh, A. J. and Thomas, T. (2012). Chromatin immunoprecipitation of mouse embryos. Methods Mol. Biol. 809, 335-352.
30. Wagner, K.-U., Ward, T., Davis, B., Wiseman, R. and Hennighausen, L. (2001). Spatial and temporal expression of the Cre gene under the control of the MMTVLTR in different lines of transgenic mice. Transgenic Res. 10, 545-553.
31. Welboren, W.-J., Sweep, F. C. G. J., Span, P. and Stunnenberg, H. G. (2009). Genomic actions of estrogen receptor α: what are the targets and how are they regulated? Endocr. Relat. Cancer 16, 1073-1089.
32. Wen, Y. H., Ho, A., Patil, S., Akram, M., Catalano, J., Eaton, A., Norton, L., Benezra, R. and Brogi, E. (2012). Id4 protein is highly expressed in triplenegative breast carcinomas: possible implications for BRCA1 downregulation. Breast Cancer Res. Treat. 135, 93-102.
33. Yun, K., Mantani, A., Garel, S., Rubenstein, J. and Israel, M. A. (2004). Id4 regulates neural progenitor proliferation and differentiation in vivo. Development 131, 5441-5448.