Elf5 conditional knockout mice reveal its role as a master regulator in mammary alveolar development: Failure of Stat5 activation and functional differentiation in the absence of Elf5

Developmental Biology

Volumn 329, Issue 2, 2009, Pages 227-241

  Choi, Yeon Sook ^a   Chakrabarti, Rumela ^a   Escamilla Hernandez, Rosalba ^a   Sinha, Satrajit ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

Alveologenesis; Conditional knockout; Elf5; Stat5; Transcription

Indexed keywords

NUCLEIC ACID BINDING PROTEIN; STAT5 PROTEIN; TRANSCRIPTION FACTOR ELF 5; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING SITE; BREAST DEVELOPMENT; BREAST DUCT; CELL DIFFERENTIATION; CELL POLARITY; CELL STRUCTURE; CONTROLLED STUDY; DOWN REGULATION; EPITHELIUM; FEMALE; KNOCKOUT MOUSE; MAMMARY GLAND; MOUSE; MULTIPLE PREGNANCY; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PUERPERIUM; REGULATORY MECHANISM; SECRETORY CELL;

ANIMALIA; MUS;

EID: 67349124434     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2009.02.032     Document Type: Article

References (50)

1. Blackman B., Russell T., Nordeen S.K., Medina D., and Neville M.C. Claudin 7 expression and localization in the normal murine mammary gland and murine mammary tumors. Breast Cancer Res. 7 (2005) R248-R255
2. Brisken C., Kaur S., Chavarria T.E., Binart N., Sutherland R.L., Weinberg R.A., Kelly P.A., and Ormandy C.J. Prolactin controls mammary gland development via direct and indirect mechanisms. Dev. Biol. 210 (1999) 96-106
3. Brisken C., and Rajaram R.D. Alveolar and lactogenic differentiation. J. Mammary Gland Biol. Neoplasia 11 (2006) 239-248
4. Cao Y., Bonizzi G., Seagroves T.N., Greten F.R., Johnson R., Schmidt E.V., and Karin M. IKKalpha provides an essential link between RANK signaling and cyclin D1 expression during mammary gland development. Cell 107 (2001) 763-775
5. Choi Y.S., and Sinha S. Determination of the consensus DNA-binding sequence and a transcriptional activation domain for ESE-2. Biochem. J. 398 (2006) 497-507
6. Choi Y.S., Cheng J., Segre J., and Sinha S. Generation and analysis of Elf5-LacZ mouse: unique and dynamic expression of Elf5 (ESE-2) in the inner root sheath of cycling hair follicles. Histochem. Cell Biol. 129 (2008) 85-94
7. Derbinski J., Pinto S., Rosch S., Hexel K., and Kyewski B. Promiscuous gene expression patterns in single medullary thymic epithelial cells argue for a stochastic mechanism. Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 657-662
8. Desmaze C., Brizard F., Turc-Carel C., Melot T., Delattre O., Thomas G., and Aurias A. Multiple chromosomal mechanisms generate an EWS/FLI1 or an EWS/ERG fusion gene in Ewing tumors. Cancer Genet. Cytogenet. 97 (1997) 12-19
9. Desprez P.Y., Sumida T., and Coppe J.P. Helix-loop-helix proteins in mammary gland development and breast cancer. J. Mammary Gland Biol. Neoplasia 8 (2003) 225-239
10. Dittmer J., and Nordheim A. Ets transcription factors and human disease. Biochim. Biophys. Acta 1377 (1998) F1-F11
11. Donnison M., Beaton A., Davey H.W., Broadhurst R., L'Huillier P., and Pfeffer P.L. Loss of the extraembryonic ectoderm in Elf5 mutants leads to defects in embryonic patterning. Development 132 (2005) 2299-2308
12. Dunbar M.E., Dann P., Brown C.W., Van Houton J., Dreyer B., Philbrick W.P., and Wysolmerski J.J. Temporally regulated overexpression of parathyroid hormone-related protein in the mammary gland reveals distinct fetal and pubertal phenotypes. J. Endocrinol. 171 (2001) 403-416
13. Faraldo M.M., Deugnier M.A., Lukashev M., Thiery J.P., and Glukhova M.A. Perturbation of beta1-integrin function alters the development of murine mammary gland. EMBO J. 17 (1998) 2139-2147
14. Grimm S.L., Seagroves T.N., Kabotyanski E.B., Hovey R.C., Vonderhaar B.K., Lydon J.P., Miyoshi K., Hennighausen L., Ormandy C.J., Lee A.V., Stull M.A., Wood T.L., and Rosen J.M. Disruption of steroid and prolactin receptor patterning in the mammary gland correlates with a block in lobuloalveolar development. Mol. Endocrinol. 16 (2002) 2675-2691
15. Harris J., Stanford P.M., Sutherland K., Oakes S.R., Naylor M.J., Robertson F.G., Blazek K.D., Kazlauskas M., Hilton H.N., Wittlin S., Alexander W.S., Lindeman G.J., Visvader J.E., and Ormandy C.J. Socs2 and elf5 mediate prolactin-induced mammary gland development. Mol. Endocrinol. 20 (2006) 1177-1187
16. Hennighausen L., and Robinson G.W. Information networks in the mammary gland. Nat. Rev., Mol. Cell Biol. 6 (2005) 715-725
17. Hilkens J., Ligtenberg M.J., Vos H.L., and Litvinov S.V. Cell membrane-associated mucins and their adhesion-modulating property. Trends Biochem. Sci. 17 (1992) 359-363
18. Lapinskas E.J., Palmer J., Ricardo S., Hertzog P.J., Hammacher A., and Pritchard M.A. A major site of expression of the ets transcription factor Elf5 is epithelia of exocrine glands. Histochem. Cell Biol. 122 (2004) 521-526
19. Long W., Wagner K.U., Lloyd K.C., Binart N., Shillingford J.M., Hennighausen L., and Jones F.E. Impaired differentiation and lactational failure of Erbb4-deficient mammary glands identify ERBB4 as an obligate mediator of STAT5. Development 130 (2003) 5257-5268
20. Ma X.J., Salunga R., Tuggle J.T., Gaudet J., Enright E., McQuary P., Payette T., Pistone M., Stecker K., Zhang B.M., Zhou Y.X., Varnholt H., Smith B., Gadd M., Chatfield E., Kessler J., Baer T.M., Erlander M.G., and Sgroi D.C. Gene expression profiles of human breast cancer progression. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 5974-5979
21. Metzger D.E., Xu Y., and Shannon J.M. Elf5 is an epithelium-specific, fibroblast growth factor-sensitive transcription factor in the embryonic lung. Dev. Dyn. 236 (2007) 1175-1192
22. Mikaelian I., Hovick M., Silva K.A., Burzenski L.M., Shultz L.D., Ackert-Bicknell C.L., Cox G.A., and Sundberg J.P. Expression of terminal differentiation proteins defines stages of mouse mammary gland development. Vet. Pathol. 43 (2006) 36-49
23. Miyoshi K., Shillingford J.M., Smith G.H., Grimm S.L., Wagner K.U., Oka T., Rosen J.M., Robinson G.W., and Hennighausen L. Signal transducer and activator of transcription (Stat) 5 controls the proliferation and differentiation of mammary alveolar epithelium. J. Cell Biol. 155 (2001) 531-542
24. Miyoshi K., Meyer B., Gruss P., Cui Y., Renou J.P., Morgan F.V., Smith G.H., Reichenstein M., Shani M., Hennighausen L., and Robinson G.W. Mammary epithelial cells are not able to undergo pregnancy-dependent differentiation in the absence of the helix-loop-helix inhibitor Id2. Mol. Endocrinol. 16 (2002) 2892-2901
25. Mori S., Nishikawa S.I., and Yokota Y. Lactation defect in mice lacking the helix-loop-helix inhibitor Id2. EMBO J. 19 (2000) 5772-5781
26. Naylor M.J., Li N., Cheung J., Lowe E.T., Lambert E., Marlow R., Wang P., Schatzmann F., Wintermantel T., Schuetz G., Clarke A.R., Mueller U., Hynes N.E., and Streuli C.H. Ablation of beta1 integrin in mammary epithelium reveals a key role for integrin in glandular morphogenesis and differentiation. J. Cell Biol. 171 (2005) 717-728
27. Ng R.K., Dean W., Dawson C., Lucifero D., Madeja Z., Reik W., and Hemberger M. Epigenetic restriction of embryonic cell lineage fate by methylation of Elf5. Nat. Cell Biol. 10 (2008) 1280-1290
28. Oakes S.R., Hilton H.N., and Ormandy C.J. The alveolar switch: coordinating the proliferative cues and cell fate decisions that drive the formation of lobuloalveoli from ductal epithelium. Breast Cancer Res. 8 (2006) 207-216
29. Oakes S.R., Naylor M.J., Asselin-Labat M.L., Blazek K.D., Gardiner-Garden M., Hilton H.N., Kazlauskas M., Pritchard M.A., Chodosh L.A., Pfeffer P.L., Lindeman G.J., Visvader J.E., and Ormandy C.J. The Ets transcription factor Elf5 specifies mammary alveolar cell fate. Genes Dev. 22 (2008) 581-586
30. Ormandy C.J., Naylor M., Harris J., Robertson F., Horseman N.D., Lindeman G.J., Visvader J., and Kelly P.A. Investigation of the transcriptional changes underlying functional defects in the mammary glands of prolactin receptor knockout mice. Recent Prog. Horm. Res. 58 (2003) 297-323
31. Peter M., Couturier J., Pacquement H., Michon J., Thomas G., Magdelenat H., and Delattre O. A new member of the ETS family fused to EWS in Ewing tumors. Oncogene 14 (1997) 1159-1164
32. Pezet A., Favre H., Kelly P.A., and Edery M. Inhibition and restoration of prolactin signal transduction by suppressors of cytokine signaling. J. Biol. Chem. 274 (1999) 24497-24502
33. Rosen J.M., Wyszomierski S.L., and Hadsell D. Regulation of milk protein gene expression. Annu. Rev. Nutr. 19 (1999) 407-436
34. Rubins N.E., Friedman J.R., Le P.P., Zhang L., Brestelli J., and Kaestner K.H. Transcriptional networks in the liver: hepatocyte nuclear factor 6 function is largely independent of Foxa2. Mol. Cell. Biol. 25 (2005) 7069-7077
35. Sharrocks A.D. The ETS-domain transcription factor family. Nat. Rev., Mol. Cell Biol. 2 (2001) 827-837
36. Sharrocks A.D., Brown A.L., Ling Y., and Yates P.R. The ETS-domain transcription factor family. Int. J. Biochem. Cell Biol. 29 (1997) 1371-1387
37. Shillingford J.M., Miyoshi K., Flagella M., Shull G.E., and Hennighausen L. Mouse mammary epithelial cells express the Na-K-Cl cotransporter, NKCC1: characterization, localization, and involvement in ductal development and morphogenesis. Mol. Endocrinol. 16 (2002) 1309-1321
38. Shillingford J.M., Miyoshi K., Robinson G.W., Bierie B., Cao Y., Karin M., and Hennighausen L. Proteotyping of mammary tissue from transgenic and gene knockout mice with immunohistochemical markers: a tool to define developmental lesions. J. Histochem. Cytochem. 51 (2003) 555-565
39. Starr R., Willson T.A., Viney E.M., Murray L.J., Rayner J.R., Jenkins B.J., Gonda T.J., Alexander W.S., Metcalf D., Nicola N.A., and Hilton D.J. A family of cytokine-inducible inhibitors of signalling. Nature 387 (1997) 917-921
40. Sum E.Y., Shackleton M., Hahm K., Thomas R.M., O'Reilly L.A., Wagner K.U., Lindeman G.J., and Visvader J.E. Loss of the LIM domain protein Lmo4 in the mammary gland during pregnancy impedes lobuloalveolar development. Oncogene 24 (2005) 4820-4828
41. Tepera S.B., McCrea P.D., and Rosen J.M. A beta-catenin survival signal is required for normal lobular development in the mammary gland. J. Cell. Sci. 116 (2003) 1137-1149
42. Thomas R.S., Ng A.N., Zhou J., Tymms M.J., Doppler W., and Kola I. The Elf group of Ets-related transcription factors. ELF3 and ELF5. Adv. Exp. Med. Biol. 480 (2000) 123-128
43. Tomic S., Chughtai N., and Ali S. SOCS-1, -2, -3: selective targets and functions downstream of the prolactin receptor. Mol. Cell. Endocrinol. 158 (1999) 45-54
44. Tummala R., and Sinha S. Differentiation-specific transcriptional regulation of the ESE-2 gene by a novel keratinocyte-restricted factor. J. Cell. Biochem. 97 (2006) 766-781
45. Wagner K.U., Wall R.J., St-Onge L., Gruss P., Wynshaw-Boris A., Garrett L., Li M., Furth P.A., and Hennighausen L. Cre-mediated gene deletion in the mammary gland. Nucleic Acids Res. 25 (1997) 4323-4330
46. Wagner K.U., McAllister K., Ward T., Davis B., Wiseman R., and Hennighausen L. Spatial and temporal expression of the Cre gene under the control of the MMTV-LTR in different lines of transgenic mice. Transgenic Res. 10 (2001) 545-553
47. Woodward W.A., Chen M.S., Behbod F., and Rosen J.M. On mammary stem cells. J. Cell. Sci. 118 (2005) 3585-3594
48. Yaniw D., and Hu J. Epithelium-specific ets transcription factor 2 upregulates cytokeratin 18 expression in pulmonary epithelial cells through an interaction with cytokeratin 18 intron 1. Cell Res. 15 (2005) 423-429
49. Zhou J., Ng A.Y., Tymms M.J., Jermiin L.S., Seth A.K., Thomas R.S., and Kola I. A novel transcription factor, ELF5, belongs to the ELF subfamily of ETS genes and maps to human chromosome 11p13-15, a region subject to LOH and rearrangement in human carcinoma cell lines. Oncogene 17 (1998) 2719-2732
50. Zhou J., Chehab R., Tkalcevic J., Naylor M.J., Harris J., Wilson T.J., Tsao S., Tellis I., Zavarsek S., Xu D., Lapinskas E.J., Visvader J., Lindeman G.J., Thomas R., Ormandy C.J., Hertzog P.J., Kola I., and Pritchard M.A. Elf5 is essential for early embryogenesis and mammary gland development during pregnancy and lactation. EMBO J. 24 (2005) 635-644