Tif1γ is essential for the terminal differentiation of mammary alveolar epithelial cells and for lactation through SMAD4 inhibition

Development (Cambridge)

Volumn 140, Issue 1, 2013, Pages 167-175

  Hesling, Cédric ^a   Lopez, Jonathan ^a,b,c   Fattet, Laurent ^a   Gonzalo, Philippe ^a,b,c   Treilleux, Isabelle ^a   Blanchard, Daphné ^a   Losson, Régine ^d   Goffin, Vincent ^e   Pigat, Natascha ^e   Puisieux, Alain ^a,b   Mikaelian, Ivan ^a,b   Gillet, Germain ^a,b   Rimokh, Ruth ^a,b  

^a CENTRE LÉON BÉRARD   (France)

^b UNIVERSITÉ DE LYON   (France)

^c CROIX ROUSSE HOSPITAL   (France)

^d INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^e INSERM   (France)

Author keywords

(Trim33); Lactation; Mouse; SMAD4; STAT5; TGF and beta; ; Tif1 and gamma

Indexed keywords

CRE RECOMBINASE; MEMBRANE PROTEIN; PROLACTIN; PROLACTIN RECEPTOR; SMAD4 PROTEIN; STAT5 PROTEIN; TIF1 GAMMA PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BREAST CELL; CELL DIFFERENTIATION; CONTROLLED STUDY; EPITHELIUM CELL; FEMALE; GENOTYPE; HISTOLOGY; IMMUNOBLOTTING; INHIBITION KINETICS; LACTATION; LIFESPAN; MALE; MAMMARY ALVEOLAR EPITHELIAL CELL; MAMMARY GLAND; MOUSE; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSACTIVATION;

ANIMALS; CELL DIFFERENTIATION; EPITHELIAL CELLS; FEMALE; LACTATION; MALE; MAMMARY GLANDS, ANIMAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; PREGNANCY; SIGNAL TRANSDUCTION; SMAD4 PROTEIN; TRANSCRIPTION FACTORS;

MUS; VERTEBRATA;

EID: 84870674998     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.085068     Document Type: Article

References (36)

1. Argetsinger, L. S., Campbell, G. S., Yang, X., Witthuhn, B. A., Silvennoinen, O., Ihle, J. N. and Carter-Su, C. (1993). Identification of JAK2 as a growth hormone receptor-associated tyrosine kinase. Cell 74, 237-244.
2. Aucagne, R., Droin, N., Paggetti, J., Lagrange, B., Largeot, A., Hammann, A., Bataille, A., Martin, L., Yan, K.-P., Fenaux, P. et al. (2011). Transcription intermediary factor 1γ is a tumor suppressor in mouse and human chronic myelomonocytic leukemia. J. Clin. Invest. 121, 2361-2370.
3. Barbieri, I., Pensa, S., Pannellini, T., Quaglino, E., Maritano, D., Demaria, M., Voster, A., Turkson, J., Cavallo, F., Watson, C. J. et al. (2010). Constitutively active Stat3 enhances neu-mediated migration and metastasis in mammary tumors via upregulation of Cten. Cancer Res. 70, 2558-2567.
4. Bernichtein, S., Jeay, S., Vaudry, R., Kelly, P. A. and Goffin, V. (2003). New homologous bioassays for human lactogens show that agonism or antagonism of various analogs is a function of assay sensitivity. Endocrine 20, 177-190.
5. Bierie, B., Gorska, A. E., Stover, D. G. and Moses, H. L. (2009). TGF-β promotes cell death and suppresses lactation during the second stage of mammary involution. J. Cell. Physiol. 219, 57-68.
6. Campbell, G. S., Argetsinger, L. S., Ihle, J. N., Kelly, P. A., Rillema, J. A. and Carter-Su, C. (1994). Activation of JAK2 tyrosine kinase by prolactin receptors in Nb2 cells and mouse mammary gland explants. Proc. Natl. Acad. Sci. USA 91, 5232-5236.
7. Cocolakis, E., Dai, M., Drevet, L., Ho, J., Haines, E., Ali, S. and Lebrun, J.-J. (2008). Smad signaling antagonizes STAT5-mediated gene transcription and mammary epithelial cell differentiation. J. Biol. Chem. 283, 1293-1307.
8. Diaz, N., Minton, S., Cox, C., Bowman, T., Gritsko, T., Garcia, R., Eweis, I., Wloch, M., Livingston, S., Seijo, E. et al. (2006). Activation of stat3 in primary tumors from high-risk breast cancer patients is associated with elevated levels of activated SRC and survivin expression. Clin. Cancer Res. 12, 20-28.
9. Dupont, S., Mamidi, A., Cordenonsi, M., Montagner, M., Zacchigna, L., Adorno, M., Martello, G., Stinchfield, M. J., Soligo, S., Morsut, L. et al. (2009). FAM/USP9x, a deubiquitinating enzyme essential for TGFbeta signaling, controls Smad4 monoubiquitination. Cell 136, 123-135.
10. Guyette, W. A., Matusik, R. J. and Rosen, J. M. (1979). Prolactin-mediated transcriptional and post-transcriptional control of casein gene expression. Cell 17, 1013-1023.
11. He, W., Dorn, D. C., Erdjument-Bromage, H., Tempst, P., Moore, M. A. S. and Massagué, J. (2006). Hematopoiesis controlled by distinct TIF1γ and Smad4 branches of the TGFβ pathway. Cell 125, 929-941.
12. Hennighausen, L. and Robinson, G. W. (2005). Information networks in the mammary gland. Nat. Rev. Mol. Cell Biol. 6, 715-725.
13. Herquel, B., Ouararhni, K., Khetchoumian, K., Ignat, M., Teletin, M., Mark, M., Béchade, G., Van Dorsselaer, A., Sanglier-Cianférani, S., Hamiche, A. et al. (2011). Transcription cofactors TRIM24, TRIM28, and TRIM33 associate to form regulatory complexes that suppress murine hepatocellular carcinoma. Proc. Natl. Acad. Sci. USA 108, 8212-8217.
14. Hesling, C., Fattet, L., Teyre, G., Jury, D., Gonzalo, P., Lopez, J., Vanbelle, C., Morel, A. P., Gillet, G., Mikaelian, I. et al. (2011). Antagonistic regulation of EMT by TIF1γ and Smad4 in mammary epithelial cells. EMBO Rep. 12, 665-672.
15. Ihle, J. N. and Kerr, I. M. (1995). Jaks and Stats in signaling by the cytokine receptor superfamily. Trends Genet. 11, 69-74.
16. Jain, S., Singhal, S., Francis, F., Hajdu, C., Wang, J. H., Suriawinata, A., Wang, Y. Q., Zhang, M., Weinshel, E. H., Francois, F. et al. (2011). Association of overexpression of TIF1γ with colorectal carcinogenesis and advanced colorectal adenocarcinoma. World J. Gastroenterol. 17, 3994-4000.
17. Jhappan, C., Geiser, A. G., Kordon, E. C., Bagheri, D., Hennighausen, L., Roberts, A. B., Smith, G. H. and Merlino, G. (1993). Targeting expression of a transforming growth factor beta 1 transgene to the pregnant mammary gland inhibits alveolar development and lactation. EMBO J. 12, 1835-1845.
18. Kelly, P. A., Djiane, J., Postel-Vinay, M. C. and Edery, M. (1991). The prolactin/growth hormone receptor family. Endocr. Rev. 12, 235-251.
19. Kim, J. and Kaartinen, V. (2008). Generation of mice with a conditional allele for Trim33. Genesis 46, 329-333.
20. Levy, L., Howell, M., Das, D., Harkin, S., Episkopou, V. and Hill, C. S. (2007). Arkadia activates Smad3/Smad4-dependent transcription by triggering signalinduced SnoN degradation. Mol. Cell. Biol. 27, 6068-6083.
21. Li, W., Qiao, W., Chen, L., Xu, X., Yang, X., Li, D., Li, C., Brodie, S. G., Meguid, M. M., Hennighausen, L. et al. (2003). Squamous cell carcinoma and mammary abscess formation through squamous metaplasia in Smad4/Dpc4 conditional knockout mice. Development 130, 6143-6153.
22. Mieth, M., Boehmer, F. D., Ball, R., Groner, B. and Grosse, R. (1990). Transforming growth factor-beta inhibits lactogenic hormone induction of betacasein expression in HC11 mouse mammary epithelial cells. Growth Factors 4, 9-15.
23. Morsut, L., Yan, K.-P., Enzo, E., Aragona, M., Soligo, S. M., Wendling, O., Mark, M., Khetchoumian, K., Bressan, G., Chambon, P. et al. (2010). Negative control of Smad activity by ectodermin/Tif1gamma patterns the mammalian embryo. Development 137, 2571-2578.
24. Nguyen, A. V. and Pollard, J. W. (2000). Transforming growth factor beta3 induces cell death during the first stage of mammary gland involution. Development 127, 3107-3118.
25. Razanajaona, D., Joguet, S., Ay, A.-S., Treilleux, I., Goddard-Léon, S., Bartholin, L. and Rimokh, R. (2007). Silencing of FLRG, an antagonist of activin, inhibits human breast tumor cell growth. Cancer Res. 67, 7223-7229.
26. Robinson, G. W. and Hennighausen, L. (2011). MMTV-Cre transgenes can adversely affect lactation: considerations for conditional gene deletion in mammary tissue. Anal. Biochem. 412, 92-95.
27. Robinson, S. D., Silberstein, G. B., Roberts, A. B., Flanders, K. C. and Daniel, C. W. (1991). Regulated expression and growth inhibitory effects of transforming growth factor-beta isoforms in mouse mammary gland development. Development 113, 867-878.
28. Serra, R. and Crowley, M. R. (2005). Mouse models of transforming growth factor beta impact in breast development and cancer. Endocr. Relat. Cancer 12, 749-760.
29. Thiery, J. P., Acloque, H., Huang, R. Y. J. and Nieto, M. A. (2009). Epithelialmesenchymal transitions in development and disease. Cell 139, 871-890.
30. Vafaizadeh, V., Klemmt, P., Brendel, C., Weber, K., Doebele, C., Britt, K., Grez, M., Fehse, B., Desriviéres, S. and Groner, B. (2010). Mammary epithelial reconstitution with gene-modified stem cells assigns roles to Stat5 in luminal alveolar cell fate decisions, differentiation, involution, and mammary tumor formation. Stem Cells 28, 928-938.
31. Vincent, D. F., Yan, K.-P., Treilleux, I., Gay, F., Arfi, V., Kaniewski, B., Marie, J. C., Lepinasse, F., Martel, S., Goddard-Leon, S. et al. (2009). Inactivation of TIF1γ cooperates with Kras to induce cystic tumors of the pancreas. PLoS Genet. 5, e1000575.
32. Vincent, D. F., Gout, J., Chuvin, N., Arfi, V., Pommier, R. M., Bertolino, P., Jonckheere, N., Ripoche, D., Kaniewski, B., Martel, S. et al. (2012). Tif1 suppresses murine pancreatic tumoral transformation by a Smad4-independent pathway. Am. J. Pathol. 180, 2214-2221.
33. Wagner, K. U., Wall, R. J., St-Onge, L., Gruss, P., Wynshaw-Boris, A., Garrett, L., Li, M., Furth, P. A. and Hennighausen, L. (1997). Cre-mediated gene deletion in the mammary gland. Nucleic Acids Res. 25, 4323-4330.
34. Wu, W.-J., Lee, C.-F., Hsin, C.-H., Du, J.-Y., Hsu, T.-C., Lin, T.-H., Yao, T.-Y., Huang, C.-H. and Lee, Y.-J. (2008). TGF-β inhibits prolactin-induced expression of β-casein by a Smad3-dependent mechanism. J. Cell. Biochem. 104, 1647-1659.
35. Yan, K. P., Dollé, P., Mark, M., Lerouge, T., Wendling, O., Chambon, P. and Losson, R. (2004). Molecular cloning, genomic structure, and expression analysis of the mouse transcriptional intermediary factor 1 gamma gene. Gene 334, 3-13.
36. Yu, H. and Jove, R. (2004). The STATs of cancer-new molecular targets come of age. Nat. Rev. Cancer 4, 97-105.