Artículo

Goddio, M.V.; Gattelli, A.; Tocci, J.M.; Cuervo, L.P.; Stedile, M.; Stumpo, D.J.; Hynes, N.E.; Blackshear, P.J.; Meiss, R.P.; Kordon, E.C. "Expression of the mRNA stability regulator Tristetraprolin is required for lactation maintenance in the mouse mammary gland" (2018) Oncotarget. 9(9):8278-8289
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Abstract:

Tristetraprolin (TTP), an mRNA-binding protein that negatively controls levels of inflammatory factors, is highly expressed in the lactating mouse mammary gland. To determine the biological relevance of this expression profile, we developed bi-transgenic mice in which this protein is specifically down-regulated in the secretory mammary epithelium in the secretory mammary epithelium during lactation. Our data show that TTP conditional KO mice produced underweight litters, possibly due to massive mammary cell death induced during lactation without the requirement of additional stimuli. This effect was linked to overexpression of inflammatory cytokines, activation of STAT3 and down-regulation of AKT phosphorylation. Importantly, blocking TNFa activity in the lactating conditional TTP KO mice inhibited cell death and similar effects were observed when this treatment was applied to wild-type animals during 48 h after weaning. Therefore, our results demonstrate that during lactation TTP wards off early involution by preventing the increase of local inflammatory factors. In addition, our data reveal the relevance of locally secreted TNFa for triggering programmed cell death after weaning. © Goddio et al.

Registro:

Documento: Artículo
Título:Expression of the mRNA stability regulator Tristetraprolin is required for lactation maintenance in the mouse mammary gland
Autor:Goddio, M.V.; Gattelli, A.; Tocci, J.M.; Cuervo, L.P.; Stedile, M.; Stumpo, D.J.; Hynes, N.E.; Blackshear, P.J.; Meiss, R.P.; Kordon, E.C.
Filiación:IFIBYNE-UBA-CONICET, Departamento de Química Biológica, FCEN-UBA, Buenos Aires, Argentina
Friedrich Miescher Institute for Biomedical Research, Basel, Switzerland
Signal Transduction Laboratory, National Institute of Environmental Health Sciences, Research Triangle Park, Durham, NC, United States
National Academy of Medicine, Buenos Aires, Argentina
Palabras clave:Autophagy; Cell death; Lactation; Mammary involution; TNF alpha; Tristetraprolin; messenger RNA; protein kinase B; STAT3 protein; tristetraprolin; tumor necrosis factor; adult; animal cell; animal tissue; apoptosis; Article; controlled study; cytokine release; down regulation; enzyme activation; enzyme activity; enzyme inhibition; female; in vivo study; lactation; limit of quantitation; mammary gland; mouse; nonhuman; protein expression; protein phosphorylation; protein RNA binding; RNA stability
Año:2018
Volumen:9
Número:9
Página de inicio:8278
Página de fin:8289
DOI: http://dx.doi.org/10.18632/oncotarget.23904
Título revista:Oncotarget
Título revista abreviado:Oncotarget
ISSN:19492553
CAS:protein kinase B, 148640-14-6
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_19492553_v9_n9_p8278_Goddio

Referencias:

  • Chen, C.Y., Shyu, A.B., AU-rich elements: characterization and importance in mRNA degradation (1995) Trends Biochem Sci., 20, pp. 465-470
  • Guhaniyogi, J., Brewer, G., Regulation of mRNA stability in mammalian cells (2001) Gene., 265, pp. 11-23
  • Barreau, C., Paillard, L., Osborne, H.B., AU-rich elements and associated factors: are there unifying principles? (2005) Nucleic Acids Res, 33, pp. 7138-7150. , https://doi.org/10.1093/nar/gki1012
  • Carballo, E., Lai, W.S., Blackshear, P.J., Feedback inhibition of macrophage tumor necrosis factor-alpha production by tristetraprolin (1998) Science., 281, pp. 1001-1005
  • Taylor, G.A., Carballo, E., Lee, D.M., Lai, W.S., Thompson, M.J., Patel, D.D., Schenkman, D.I., Blackshear, P.J., A pathogenetic role for TNF alpha in the syndrome of cachexia, arthritis, and autoimmunity resulting from tristetraprolin (TTP) deficiency (1996) Immunity., 4, pp. 445-454
  • Brooks, S.A., Blackshear, P.J., Tristetraprolin (TTP): interactions with mRNA and proteins, and current thoughts on mechanisms of action (2013) Biochim Biophys Acta., 1829, pp. 666-679. , https://doi.org/10.1016/j.bbagrm.2013.02.003
  • Ishmael, F.T., Fang, X., Galdiero, M.R., Atasoy, U., Rigby, W.F., Gorospe, M., Cheadle, C., Stellato, C., Role of the RNA-binding protein tristetraprolin in glucocorticoid-mediated gene regulation (2008) Journal of immunology., 180, pp. 8342-8353
  • Smoak, K., Cidlowski, J.A., Glucocorticoids regulate tristetraprolin synthesis and posttranscriptionally regulate tumor necrosis factor alpha inflammatory signaling (2006) Mol Cell Biol., 26, pp. 9126-9135. , https://doi.org/10.1128/MCB.00679-06
  • Goddio, M.V., Gattelli, A., Slomiansky, V., Lacunza, E., Gingerich, T., Tocci, J.M., Facchinetti, M.M., Kordon, E.C., Mammary differentiation induces expression of Tristetraprolin, a tumor suppressor AU-rich mRNA-binding protein (2012) Breast Cancer Res Treat., 135, pp. 749-758. , https://doi.org/10.1007/s10549-012-2216-0
  • Wakao, H., Gouilleux, F., Groner, B., Mammary gland factor (MGF) is a novel member of the cytokine regulated transcription factor gene family and confers the prolactin response (1994) EMBO J., 13, pp. 2182-2191
  • Reichardt, H.M., Horsch, K., Grone, H.J., Kolbus, A., Beug, H., Hynes, N., Schutz, G., Mammary gland development and lactation are controlled by different glucocorticoid receptor activities (2001) Eur J Endocrinol., 145, pp. 519-527
  • Hennighausen, L., Robinson, G.W., Signaling pathways in mammary gland development (2001) Developmental cell., 1, pp. 467-475
  • Walker, N.I., Bennett, R.E., Kerr, J.F., Cell death by apoptosis during involution of the lactating breast in mice and rats (1989) The American journal of anatomy., 185, pp. 19-32. , https://doi.org/10.1002/aja.1001850104
  • Quarrie, L.H., Addey, C.V., Wilde, C.J., Programmed cell death during mammary tissue involution induced by weaning, litter removal, and milk stasis (1996) J Cell Physiol., 168, pp. 559-569. , https://doi.org/10.1002/(SICI)1097-4652(199609)168:3<559::AID-JCP8>3.0.CO;2-O
  • Li, M., Liu, X., Robinson, G., Bar-Peled, U., Wagner, K.U., Young, W.S., Hennighausen, L., Furth, P.A., Mammary-derived signals activate programmed cell death during the first stage of mammary gland involution (1997) Proc Natl Acad Sci U S A., 94, pp. 3425-3430
  • Quarrie, L.H., Addey, C.V., Wilde, C.J., Local regulation of mammary apoptosis in the lactating goat (1994) Biochem Soc Trans, 22, p. 178S
  • Shamay, A., Shapiro, F., Mabjeesh, S.J., Silanikove, N., Casein-derived phosphopeptides disrupt tight junction integrity, and precipitously dry up milk secretion in goats (2002) Life Sci., 70, pp. 2707-2719
  • Zhao, L., Melenhorst, J.J., Hennighausen, L., Loss of interleukin 6 results in delayed mammary gland involution: a possible role for mitogen-activated protein kinase and not signal transducer and activator of transcription 3 (2002) Mol Endocrinol., 16, pp. 2902-2912. , https://doi.org/10.1210/me.2001-0330
  • Kritikou, E.A., Sharkey, A., Abell, K., Came, P.J., Anderson, E., Clarkson, R.W., Watson, C.J., A dual, non-redundant, role for LIF as a regulator of development and STAT3-mediated cell death in mammary gland (2003) Development., 130, pp. 3459-3468
  • Schere-Levy, C., Buggiano, V., Quaglino, A., Gattelli, A., Cirio, M.C., Piazzon, I., Vanzulli, S., Kordon, E.C., Leukemia inhibitory factor induces apoptosis of the mammary epithelial cells and participates in mouse mammary gland involution (2003) Exp Cell Res., 282, pp. 35-47
  • Clarkson, R.W., Wayland, M.T., Lee, J., Freeman, T., Watson, C.J., Gene expression profiling of mammary gland development reveals putative roles for death receptors and immune mediators in post-lactational regression (2004) Breast Cancer Res., 6, pp. R92-R109. , https://doi.org/10.1186/bcr754
  • Baxter, F.O., Came, P.J., Abell, K., Kedjouar, B., Huth, M., Rajewsky, K., Pasparakis, M., Watson, C.J., IKKbeta/2 induces TWEAK and apoptosis in mammary epithelial cells (2006) Development., 133, pp. 3485-3494. , https://doi.org/10.1242/dev.02502
  • Clarkson, R.W., Heeley, J.L., Chapman, R., Aillet, F., Hay, R.T., Wyllie, A., Watson, C.J., NF-kappaB inhibits apoptosis in murine mammary epithelia (2000) J Biol Chem., 275, pp. 12737-12742
  • Chapman, R.S., Lourenco, P.C., Tonner, E., Flint, D.J., Selbert, S., Takeda, K., Akira, S., Watson, C.J., Suppression of epithelial apoptosis and delayed mammary gland involution in mice with a conditional knockout of Stat3 (1999) Genes Dev., 13, pp. 2604-2616
  • Humphreys, R.C., Bierie, B., Zhao, L., Raz, R., Levy, D., Hennighausen, L., Deletion of Stat3 blocks mammary gland involution and extends functional competence of the secretory epithelium in the absence of lactogenic stimuli (2002) Endocrinology., 143, pp. 3641-3650. , https://doi.org/10.1210/en.2002-220224
  • Kreuzaler, P.A., Staniszewska, A.D., Li, W., Omidvar, N., Kedjouar, B., Turkson, J., Poli, V., Watson, C.J., Stat3 controls lysosomal-mediated cell death in vivo (2011) Nat Cell Biol., 13, pp. 303-309. , https://doi.org/10.1038/ncb2171
  • Arnandis, T., Ferrer-Vicens, I., Garcia-Trevijano, E.R., Miralles, V.J., Garcia, C., Torres, L., Vina, J.R., Zaragoza, R., Calpains mediate epithelial-cell death during mammary gland involution: mitochondria and lysosomal destabilization (2012) Cell Death Differ., 19, pp. 1536-1548. , https://doi.org/10.1038/cdd.2012.46
  • Stein, T., Salomonis, N., Gusterson, B.A., Mammary gland involution as a multi-step process (2007) J Mammary Gland Biol Neoplasia., 12, pp. 25-35. , https://doi.org/10.1007/s10911-007-9035-7
  • Watson, C.J., Involution: apoptosis and tissue remodelling that convert the mammary gland from milk factory to a quiescent organ (2006) Breast Cancer Res., 8, p. 203. , https://doi.org/10.1186/bcr1401
  • Lyons, T.R., Schedin, P.J., Borges, V.F., Pregnancy and breast cancer: when they collide (2009) J Mammary Gland Biol Neoplasia., 14, pp. 87-98. , https://doi.org/10.1007/s10911-009-9119-7
  • Brennan, S.E., Kuwano, Y., Alkharouf, N., Blackshear, P.J., Gorospe, M., Wilson, G.M., The mRNA-destabilizing protein tristetraprolin is suppressed in many cancers, altering tumorigenic phenotypes and patient prognosis (2009) Cancer Res., 69, pp. 5168-5176. , https://doi.org/10.1158/0008-5472.CAN-08-4238
  • Shipman, L.J., Docherty, A.H., Knight, C.H., Wilde, C.J., Metabolic adaptations in mouse mammary gland during a normal lactation cycle and in extended lactation (1987) Q J Exp Physiol., 72, pp. 303-311
  • Schwertfeger, K.L., Richert, M.M., Anderson, S.M., Mammary gland involution is delayed by activated Akt in transgenic mice (2001) Mol Endocrinol., 15, pp. 867-881. , https://doi.org/10.1210/mend.15.6.0663
  • Abell, K., Bilancio, A., Clarkson, R.W., Tiffen, P.G., Altaparmakov, A.I., Burdon, T.G., Asano, T., Watson, C.J., Stat3-induced apoptosis requires a molecular switch in PI(3)K subunit composition (2005) Nat Cell Biol., 7, pp. 392-398. , https://doi.org/10.1038/ncb1242
  • Creamer, B.A., Sakamoto, K., Schmidt, J.W., Triplett, A.A., Moriggl, R., Wagner, K.U., Stat5 promotes survival of mammary epithelial cells through transcriptional activation of a distinct promoter in Akt1 (2010) Mol Cell Biol., 30, pp. 2957-2970. , https://doi.org/10.1128/MCB.00851-09
  • Van Tubergen, E., Vander Broek, R., Lee, J., Wolf, G., Carey, T., Bradford, C., Prince, M., D'Silva, N.J., Tristetraprolin regulates interleukin-6, which is correlated with tumor progression in patients with head and neck squamous cell carcinoma (2011) Cancer., 117, pp. 2677-2689. , https://doi.org/10.1002/cncr.25859
  • Lai, W.S., Parker, J.S., Grissom, S.F., Stumpo, D.J., Blackshear, P.J., Novel mRNA targets for tristetraprolin (TTP) identified by global analysis of stabilized transcripts in TTP-deficient fibroblasts (2006) Mol Cell Biol., 26, pp. 9196-9208. , https://doi.org/10.1128/MCB.00945-06
  • Levy, C.S., Slomiansky, V., Gattelli, A., Nahmod, K., Pelisch, F., Blaustein, M., Srebrow, A., Kordon, E.C., Tumor necrosis factor alpha induces LIF expression through ERK1/2 activation in mammary epithelial cells (2010) J Cell Biochem., 110, pp. 857-865. , https://doi.org/10.1002/jcb.22595
  • Silanikove, N., Natural and abrupt involution of the mammary gland affects differently the metabolic and health consequences of weaning (2014) Life Sci., 102, pp. 10-15. , https://doi.org/10.1016/j.lfs.2014.02.034
  • Booth, B.W., Boulanger, C.A., Smith, G.H., Alveolar progenitor cells develop in mouse mammary glands independent of pregnancy and lactation (2007) J Cell Physiol., 212, pp. 729-736. , https://doi.org/10.1002/jcp.21071
  • Aslam, N., Zaheer, I., The biosynthesis characteristics of TTP, TNF can be regulated through a posttranscriptional molecular loop (2011) J Biol Chem., 286, pp. 3767-3776. , https://doi.org/10.1074/jbc.M110.168757M110.168757
  • Stocklin, E., Wissler, M., Gouilleux, F., Groner, B., Functional interactions between Stat5 and the glucocorticoid receptor (1996) Nature., 383, pp. 726-728. , https://doi.org/10.1038/383726a0
  • Carballo, E., Blackshear, P.J., Roles of tumor necrosis factor-alpha receptor subtypes in the pathogenesis of the tristetraprolin-deficiency syndrome (2001) Blood., 98, pp. 2389-2395
  • Wallach, D., The TNF cytokine family: one track in a road paved by many (2013) Cytokine., 63, pp. 225-229. , https://doi.org/10.1016/j.cyto.2013.05.027
  • Hennigar, S.R., Seo, Y.A., Sharma, S., Soybel, D.I., Kelleher, S.L., ZnT2 is a critical mediator of lysosomal-mediated cell death during early mammary gland involution (2015) Sci Rep., 5, p. 8033. , https://doi.org/10.1038/srep08033
  • Hennigar, S.R., Kelleher, S.L., TNFalpha Post-Translationally Targets ZnT2 to Accumulate Zinc in Lysosomes (2015) J Cell Physiol., 230, pp. 2345-2350. , https://doi.org/10.1002/jcp.24992
  • Clarkson, R.W., Watson, C.J., Microarray analysis of the involution switch (2003) J Mammary Gland Biol Neoplasia., 8, pp. 309-319
  • Tiffen, P.G., Omidvar, N., Marquez-Almuina, N., Croston, D., Watson, C.J., Clarkson, R.W., A dual role for oncostatin M signaling in the differentiation and death of mammary epithelial cells in vivo (2008) Mol Endocrinol., 22, pp. 2677-2688. , https://doi.org/10.1210/me.2008-0097
  • Qiu, L.Q., Stumpo, D.J., Blackshear, P.J., Myeloid-specific tristetraprolin deficiency in mice results in extreme lipopolysaccharide sensitivity in an otherwise minimal phenotype (2012) J Immunol., 188, pp. 5150-5159. , https://doi.org/10.4049/jimmunol.1103700
  • Wagner, K.U., Wall, R.J., St-Onge, L., Gruss, P., Wynshaw-Boris, A., Garrett, L., Li, M., Hennighausen, L., Cre-mediated gene deletion in the mammary gland (1997) Nucleic Acids Res., 25, pp. 4323-4330
  • Yoshitaka, T., Ishida, S., Mukai, T., Kittaka, M., Reichenberger, E.J., Ueki, Y., Etanercept administration to neonatal SH3BP2 knock-in cherubism mice prevents TNF-alpha-induced inflammation and bone loss (2014) J Bone Miner Res., 29, pp. 1170-1182. , https://doi.org/10.1002/jbmr.2125
  • Bertucci, P.Y., Quaglino, A., Pozzi, A.G., Kordon, E.C., Pecci, A., Glucocorticoid-induced impairment of mammary gland involution is associated with STAT5 and STAT3 signaling modulation (2010) Endocrinology., 151, pp. 5730-5740. , https://doi.org/10.1210/en.2010-0517

Citas:

---------- APA ----------
Goddio, M.V., Gattelli, A., Tocci, J.M., Cuervo, L.P., Stedile, M., Stumpo, D.J., Hynes, N.E.,..., Kordon, E.C. (2018) . Expression of the mRNA stability regulator Tristetraprolin is required for lactation maintenance in the mouse mammary gland. Oncotarget, 9(9), 8278-8289.
http://dx.doi.org/10.18632/oncotarget.23904
---------- CHICAGO ----------
Goddio, M.V., Gattelli, A., Tocci, J.M., Cuervo, L.P., Stedile, M., Stumpo, D.J., et al. "Expression of the mRNA stability regulator Tristetraprolin is required for lactation maintenance in the mouse mammary gland" . Oncotarget 9, no. 9 (2018) : 8278-8289.
http://dx.doi.org/10.18632/oncotarget.23904
---------- MLA ----------
Goddio, M.V., Gattelli, A., Tocci, J.M., Cuervo, L.P., Stedile, M., Stumpo, D.J., et al. "Expression of the mRNA stability regulator Tristetraprolin is required for lactation maintenance in the mouse mammary gland" . Oncotarget, vol. 9, no. 9, 2018, pp. 8278-8289.
http://dx.doi.org/10.18632/oncotarget.23904
---------- VANCOUVER ----------
Goddio, M.V., Gattelli, A., Tocci, J.M., Cuervo, L.P., Stedile, M., Stumpo, D.J., et al. Expression of the mRNA stability regulator Tristetraprolin is required for lactation maintenance in the mouse mammary gland. Oncotarget. 2018;9(9):8278-8289.
http://dx.doi.org/10.18632/oncotarget.23904