Artículo

Naipauer, J.; Gattelli, A.; Degese, M.S.; Slomiansky, V.; Wertheimer, E.; Lamarre, J.; Castilla, L.; Abba, M.; Kordon, E.C.; Coso, O.A. "The use of alternative polyadenylation sites renders integrin β1 (Itgb1) mRNA isoforms with differential stability during mammary gland development" (2013) Biochemical Journal. 454(2):345-357
La versión final de este artículo es de uso interno. El editor solo permite incluir en el repositorio el artículo en su versión post-print. Por favor, si usted la posee enviela a
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Integrins are heterodimeric cell-surface adhesion receptors that play a critical role in tissue development. Characterization of the full-length mRNA encoding the β1 subunit (Itgb1) revealed an alternative functional cleavage and polyadenylation site that yields a new Itgb1 mRNA isoform 578 bp shorter than that previously reported. Using a variety of experimental and bioinformatic approaches, we found that the two Itgb1 isoforms are expressed at different levels in a variety of mouse tissues, including the mammary gland, where they are differentially regulated at successive developmental stages. The longer mRNA species is prevelant during lactation, whereas the shorter is induced after weaning. In 3D cultures, where expression of integrin β1 protein is required for normal formation of acini, experimental blockade of the longer isoform induced enhanced expression of the shorter species which allowed normal morphological mammary differentiation. The short isoform lacks AU-rich motifs and miRNA target sequences that are potentially implicated in the regulation of mRNA stability and translation efficiency. We further determined that the AU-binding protein HuR appears to selectively stabilize the longer isoform in the mammary gland. In summary, the results of the present study identify a newregulatory instance involved in the fine-tuning of Itgb1 expression during mammary gland development and function. © 2013 Biochemical Society.

Registro:

Documento: Artículo
Título:The use of alternative polyadenylation sites renders integrin β1 (Itgb1) mRNA isoforms with differential stability during mammary gland development
Autor:Naipauer, J.; Gattelli, A.; Degese, M.S.; Slomiansky, V.; Wertheimer, E.; Lamarre, J.; Castilla, L.; Abba, M.; Kordon, E.C.; Coso, O.A.
Filiación:Departamento de Fisiología y Biología Molecular, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires (FCEN-UBA), Buenos Aires C1428EHA, Argentina
IFIBYNE-CONICET, Buenos Aires, Argentina
Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires C1428EHA, Argentina
CEFYBO-CONICET, Facultad de Medicina, Universidad de Buenos Aires, Buenos Aires C1121ABG, Argentina
DBMS, Ontario Veterinary College, University of Guelph, Guelph, ON N1G 2W1, Canada
Program in Gene Function and Expression, University of Massachusetts Medical School, Worcester, MA 01605, United States
CINIBA, Facultad de Ciencias Médicas, Universidad Nacional de la Plata (UNLP), Buenos Aires 1900, Argentina
Palabras clave:Alternative polyadenylation; Gene expression regulation; HuR; Itgb1; Mammary gland; MRNA; beta1 integrin; caspase 3; dactinomycin; HuR protein; microRNA; RNA isoform; short hairpin RNA; article; breast development; cell differentiation; consensus sequence; differentiation; electrophoretic mobility; human; lactation; nonhuman; polyadenylation; priority journal; promoter region; protein binding; protein cleavage; protein expression; protein stability; RNA transcription; Animals; Antigens, CD29; Cell Culture Techniques; Cell Differentiation; Cell Line; Data Mining; Female; Gene Expression Regulation, Developmental; Lactation; Mammary Glands, Animal; Mice; Mice, Inbred BALB C; Polyadenylation; Pregnancy; Recombinant Proteins; RNA Isoforms; RNA Processing, Post-Transcriptional; RNA Stability; RNA, Messenger; RNA, Small Interfering; Specific Pathogen-Free Organisms; Weaning
Año:2013
Volumen:454
Número:2
Página de inicio:345
Página de fin:357
DOI: http://dx.doi.org/10.1042/BJ20130062
Título revista:Biochemical Journal
Título revista abreviado:Biochem. J.
ISSN:02646021
CODEN:BIJOA
CAS:caspase 3, 169592-56-7; dactinomycin, 1402-38-6, 1402-58-0, 50-76-0; Antigens, CD29; RNA Isoforms; RNA, Messenger; RNA, Small Interfering; Recombinant Proteins
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_02646021_v454_n2_p345_Naipauer

Referencias:

  • Schwartz, M.A., Integrins, oncogenes, and anchorage independence (1997) J. Cell Biol., 139, pp. 575-578
  • Hynes, R.O., Integrins: Bidirectional, allosteric signaling machines (2002) Cell, 110, pp. 673-687
  • Brakebusch, C., Fassler, R., β1 Integrin function in vivo: Adhesion, migration and more (2005) Cancer Metastasis Rev., 24, pp. 403-411
  • Taddei, I., Faraldo, M.M., Teuliere, J., Deugnier, M.A., Thiery, J.P., Glukhova, M.A., Integrins in mammary gland development and differentiation of mammary epithelium (2003) J. Mammary Gland Biol. Neoplasia, 8, pp. 383-394
  • Anderson, R., Fassler, R., Georges-Labouesse, E., Hynes, R.O., Bader, B.L., Kreidberg, J.A., Schaible, K., Wylie, C., Mouse primordial germ cells lacking η1 integrins enter the germline but fail to migrate normally to the gonads (1999) Development, 126, pp. 1655-1664
  • Fassler, R., Meyer, M., Consequences of lack of β1 integrin gene expression in mice (1995) Genes Dev., 9, pp. 1896-1908
  • Stephens, L.E., Sutherland, A.E., Klimanskaya, I.V., Andrieux, A., Meneses, J., Pedersen, R.A., Damsky, C.H., Deletion of β1 integrins in mice results in inner cell mass failure and peri-implantation lethality (1995) Genes Dev., 9, pp. 1883-1895
  • Klinowska, T.C., Soriano, J.V., Edwards, G.M., Oliver, J.M., Valentijn, A.J., Montesano, R., Streuli, C.H., Laminin and β1 integrins are crucial for normal mammary gland development in the mouse (1999) Dev. Biol., 215, pp. 13-32
  • Li, N., Zhang, Y., Naylor, M.J., Schatzmann, F., Maurer, F., Wintermantel, T., Schuetz, G., Hynes, N.E., β1 Integrins regulate mammary gland proliferation and maintain the integrity of mammary alveoli (2005) EMBO J., 24, pp. 1942-1953
  • Naylor, M.J., Li, N., Cheung, J., Lowe, E.T., Lambert, E., Marlow, R., Wang, P., Schuetz, G., Ablation of β1 integrin in mammary epithelium reveals a key role for integrin in glandular morphogenesis and differentiation (2005) J. Cell Biol., 171, pp. 717-728
  • Edwalds-Gilbert, G., Veraldi, K.L., Milcarek, C., Alternative poly(A) site selection in complex transcription units: Means to an end? (1997) Nucleic Acids Res., 25, pp. 2547-2561
  • Chabot, B., Directing alternative splicing: Cast and scenarios (1996) Trends Genet., 12, pp. 472-478
  • Garneau, N.L., Wilusz, J., Wilusz, C.J., The highways and byways of mRNA decay (2007) Nat. Rev. Mol. Cell Biol., 2, pp. 113-126
  • Hynes, N.E., Taverna, D., Harwerth, I.M., Ciardiello, F., Salomon, D.S., Yamamoto, T., Groner, B., Epidermal growth factor receptor, but not c-erbB-2, activation prevents lactogenic hormone induction of the β-casein gene in mouse mammary epithelial cells (1990) Mol. Cell. Biol., 10, pp. 4027-4034
  • Quaglino, A., Salierno, M., Pellegrotti, J., Rubinstein, N., Kordon, E.C., Mechanical strain induces involution-associated events in mammary epithelial cells (2009) BMC Cell Biol., 10, p. 55
  • You, Y., Chen, C.Y., Shyu, A.B., U-rich sequence-binding proteins (URBPs) interacting with a 20-nucleotide U-rich sequence in the 3 untranslated region of c-fos mRNA may be involved in the first step of c-fos mRNA degradation (1992) Mol. Cell. Biol., 12, pp. 2931-2940
  • Ji, Z., Luo, W., Li, W., Hoque, M., Pan, Z., Zhao, Y., Tian, B., Transcriptional activity regulates alternative cleavage and polyadenylation (2011) Mol. Syst. Biol., 7, p. 534
  • Saeed, A.I., Sharov, V., White, J., Li, J., Liang, W., Bhagabati, N., Braisted, J., Et Al., T.M., TM4: A free, open-source system for microarray data management and analysis (2003) Biotechniques, 34, pp. 374-378
  • Gattelli, A., Zimberlin, M.N., Meiss, R.P., Castilla, L.H., Kordon, E.C., Selection of early-occurring mutations dictates hormone-independent progression in mouse mammary tumor lines (2006) J. Virol., 80, pp. 11409-11415
  • Soulier, S., Vilotte, J.-L., L'huillier, P.J., Mercier, J.-C., Developmental regulation of murine integrin pl subunit- and Hsc73-encoding genes in mammary gland: Sequence of a new mouse Hsc73 cDNA (1996) Gene, 172, pp. 285-289
  • Brennan, C.M., Steitz, J.A., HuR and mRNA stability (2001) Cell. Mol. Life Sci., 58, pp. 266-277
  • Ji, Z., Lee, J.Y., Pan, Z., Jiang, B., Tian, B., Progressive lengthening of 3untranslated regions of mRNAs by alternative polyadenylation during mouse embryonic development (2009) Proc. Natl. Acad. Sci. U.S.A., 106, pp. 7028-7033
  • Pontier, S.M., Muller, W.J., Integrins in mammary-stem-cell biology and breast cancer progression: A role in cancer stem cells? (2009) J. Cell Sci., 122, pp. 207-214
  • Taddei, I., Deugnier, M.A., Faraldo, M.M., Petit, V., Bouvard, D., Medina, D., Fassler, R., Glukhova, M.A., β1 Integrin deletion from the basal compartment of the mammary epithelium affects stem cells (2008) Nat. Cell Biol., 10, pp. 716-722
  • McSherry, E.A., McGee, S.F., Jirstrom, K., Doyle, E.M., Brennan, D.J., Landberg, G., Dervan, P.A., Gallagher, W.M., JAM-A expression positively correlates with poor prognosis in breast cancer patients (2009) Int. J. Cancer, 125, pp. 1343-1351
  • Huang, R.Y., Ip, M.M., Differential expression of integrin mRNAs and proteins during normal rat mammary gland development and in carcinogenesis (2001) Cell Tissue Res., 303, pp. 69-80
  • Mukherjee, N., Lager, P.J., Friedersdorf, M.B., Thompson, M.A., Keene, J.D., Coordinated posttranscriptional mRNA population dynamics during T-cell activation (2009) Mol. Syst. Biol., 5, p. 288
  • Yan, W., Zhang, Y., Zhang, J., Cho, S.-J., Chen, X., HuR is necessary for mammary epithelial cell proliferation and polarity at least in part via DNp63 (2012) PLoS ONE, 7, p. 45336
  • Kriegel, A.J., Liu, Y., Fang, Y., Ding, X., Liang, M., The miR-29 family: Genomics, cell biology, and relevance to renal and cardiovascular injury (2012) Physiol. Genomics, 44, pp. 237-244
  • Li, G., Luna, C., Qiu, J., Epstein, D.L., Gonzalez, P., Targeting of integrin β1 and kinesin 2α by microRNA 183 (2010) J. Biol. Chem., 285, pp. 5461-5471
  • Li, K.K., Pang, J.C., Ching, A.K., Wong, C.K., Kong, X., Wang, Y., Zhou, L., Ng, H.K., MiR-124 is frequently down-regulated in medulloblastoma and is a negative regulator of SLC16A1 (2009) Hum. Pathol., 40, pp. 1234-1243
  • Avril-Sassen, S., Goldstein, L.D., Stingl, J., Blenkiron, C., Le Quesne, J., Spiteri, I., Karagavriilidou, K., Caldas, C., Characterisation of microRNA expression in post-natal mouse mammary gland development (2009) BMC Genomics, 10, p. 548
  • Young, L.E., Moore, A.E., Sokol, L., Meisner-Kober, N., Dixon, D.A., The mRNA stability factor HuR inhibits microRNA-16 targeting of COX-2 (2012) Mol. Cancer Res., 10, pp. 167-180
  • Tian, B., Hu, J., Zhang, H., Lutz, C.S., A large-scale analysis of mRNA polyadenylation of human and mouse genes (2005) Nucleic Acids Res., 33, pp. 201-212
  • Yang, S.H., Sharrocks, A.D., Whitmarsh, A.J., MAP kinase signalling cascades and transcriptional regulation (2013) Gene, 513, pp. 1-13
  • Kornblihtt, A.R., Coupling transcription and alternative splicing (2007) Adv. Exp. Med. Biol., 623, pp. 175-189
  • Alonso, C.R., A complex 'mRNA degradation code' controls gene expression during animal development (2012) Trends Genet., 28, pp. 78-88

Citas:

---------- APA ----------
Naipauer, J., Gattelli, A., Degese, M.S., Slomiansky, V., Wertheimer, E., Lamarre, J., Castilla, L.,..., Coso, O.A. (2013) . The use of alternative polyadenylation sites renders integrin β1 (Itgb1) mRNA isoforms with differential stability during mammary gland development. Biochemical Journal, 454(2), 345-357.
http://dx.doi.org/10.1042/BJ20130062
---------- CHICAGO ----------
Naipauer, J., Gattelli, A., Degese, M.S., Slomiansky, V., Wertheimer, E., Lamarre, J., et al. "The use of alternative polyadenylation sites renders integrin β1 (Itgb1) mRNA isoforms with differential stability during mammary gland development" . Biochemical Journal 454, no. 2 (2013) : 345-357.
http://dx.doi.org/10.1042/BJ20130062
---------- MLA ----------
Naipauer, J., Gattelli, A., Degese, M.S., Slomiansky, V., Wertheimer, E., Lamarre, J., et al. "The use of alternative polyadenylation sites renders integrin β1 (Itgb1) mRNA isoforms with differential stability during mammary gland development" . Biochemical Journal, vol. 454, no. 2, 2013, pp. 345-357.
http://dx.doi.org/10.1042/BJ20130062
---------- VANCOUVER ----------
Naipauer, J., Gattelli, A., Degese, M.S., Slomiansky, V., Wertheimer, E., Lamarre, J., et al. The use of alternative polyadenylation sites renders integrin β1 (Itgb1) mRNA isoforms with differential stability during mammary gland development. Biochem. J. 2013;454(2):345-357.
http://dx.doi.org/10.1042/BJ20130062