Artículo

Zubeldía-Brenner, L.; De Winne, C.; Perrone, S.; Rodríguez-Seguí, S.A.; Willems, C.; Ornstein, A.M.; Lacau-Mengido, I.; Vankelecom, H.; Cristina, C.; Becu-Villalobos, D."Inhibition of Notch signaling attenuates pituitary adenoma growth in Nude mice" (2019) Endocrine-Related Cancer. 26(1):13-29
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Abstract:

Preclinical and clinical studies support that Notch signaling may play an important oncogenic role in cancer, but there is scarce information for pituitary tumors. We therefore undertook a functional study to evaluate Notch participation in pituitary adenoma growth. Tumors generated in Nude mice by subcutaneous GH3 somatolactotrope cell injection were treated in vivo with DAPT, a γ-secretase inhibitor, thus inactivating Notch signaling. This treatment led to pituitary tumor reduction, lower prolactin and GH tumor content and a decrease in angiogenesis. Furthermore, in silico transcriptomic and epigenomic analyses uncovered several tumor suppressor genes related to Notch signaling in pituitary tissue, namely Btg2, Nr4a1, Men1, Zfp36 and Cnot1. Gene evaluation suggested that Btg2, Nr4a1 and Cnot1 may be possible players in GH3 xenograft growth. Btg2 mRNA expression was lower in GH3 tumors compared to the parental line, and DAPT increased its expression levels in the tumor in parallel with the inhibition of its volume. Cnot1 mRNA levels were also increased in the pituitary xenografts by DAPT treatment. And the Nr4a1 gene was lower in tumors compared to the parental line, though not modified by DAPT. Finally, because DAPT in vivo may also be acting on tumor microenvironment, we determined the direct effect of DAPT on GH3 cells in vitro. We found that DAPT decreases the proliferative, secretory and migration potential of GH3 cells. These results position selective interruption of Notch signaling as a potential therapeutic tool in adjuvant treatments for aggressive or resistant pituitary tumors. © 2019 Society for Endocrinology Published by Bioscientifica Ltd.

Registro:

Documento: Artículo
Título:Inhibition of Notch signaling attenuates pituitary adenoma growth in Nude mice
Autor:Zubeldía-Brenner, L.; De Winne, C.; Perrone, S.; Rodríguez-Seguí, S.A.; Willems, C.; Ornstein, A.M.; Lacau-Mengido, I.; Vankelecom, H.; Cristina, C.; Becu-Villalobos, D.
Filiación:Instituto de Biología y Medicina Experimental, IBYME-CONICET, Buenos Aires, Argentina
Centro de Investigaciones y Transferencia del Noroeste de la Provincia de Buenos Aires, CITNOBA (UNNOBA-CONICET), Universidad Nacional delNoroeste de la Provincia de Buenos Aires, Buenos Aires, Argentina
Departamento de Fisiología y Biología Molecular y Celular, Universidad de Buenos Aires, Facultad de Ciencias Exactas y Naturales, Buenos Aires, Argentina
CONICET-Universidad de Buenos Aires, Instituto de Fisiología, Biología Molecular y Neurociencias (IFIBYNE), Buenos Aires, Argentina
Department of Development and Regeneration, Cluster Stem Cell and Developmental Biology, Unit of Stem Cell Research, KU Leuven (University of Leuven), Leuven, Belgium
Palabras clave:Angiogenesis; DAPT; GH; Pituitary; Prolactin; growth hormone; messenger RNA; Notch receptor; prolactin; angiogenesis; animal cell; animal experiment; animal model; Article; btg2 gene; cancer inhibition; carcinogenesis; cell migration; cell proliferation; cellular secretion; cnot1 gene; computer model; controlled study; disease association; epigenetics; GH3 cell line; hypophysis adenoma; in vitro study; in vivo study; mouse; mRNA expression level; nonhuman; Notch signaling; nr4a1 gene; rat; transcriptomics; tumor growth; tumor microenvironment
Año:2019
Volumen:26
Número:1
Página de inicio:13
Página de fin:29
DOI: http://dx.doi.org/10.1530/ERC-18-0337
Handle:http://hdl.handle.net/20.500.12110/paper_13510088_v26_n1_p13_ZubeldiaBrenner
Título revista:Endocrine-Related Cancer
Título revista abreviado:Endocr.-Relat. Cancer
ISSN:13510088
CODEN:ERCAE
CAS:growth hormone, 36992-73-1, 37267-05-3, 66419-50-9, 9002-72-6; prolactin, 12585-34-1, 50647-00-2, 9002-62-4
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_13510088_v26_n1_p13_ZubeldiaBrenner

Referencias:

  • Akiyoshi, T., Nakamura, M., Yanai, K., Nagai, S., Wada, J., Koga, K., Nakashima, H., Katano, M., Gamma-secretase inhibitors enhance taxane-induced mitotic arrest and apoptosis in colon cancer cells (2008) Gastroenterology, 134, pp. 131-144. , https://doi.org/10.1053/j.gastro.2007.10.008
  • Ansell, P.J., Zhou, Y., Schjeide, B.M., Kerner, A., Zhao, J., Zhang, X., Klibanski, A., Regulation of Growth Hormone expression by Delta-like protein 1 (Dlk1) (2007) Molecular and Cellular Endocrinology, 271, pp. 55-63. , https://doi.org/10.1016/j.mce.2007.04.002
  • Artavanis-Tsakonas, S., Muskavitch, M.A., Notch: The past, the present, and the future (2010) Current Topics in Developmental Biology, 92, pp. 1-29. , https://doi.org/10.1016/S0070-2153(10)92001-2
  • Avila, J.L., Kissil, J.L., Notch signaling in pancreatic cancer: Oncogene or tumor suppressor? (2013) Trends in Molecular Medicine, 19, pp. 320-327. , https://doi.org/10.1016/j.molmed.2013.03.003
  • Bray, S.J., Notch signalling: A simple pathway becomes complex (2006) Nature Reviews. Molecular Cell Biology, 7, pp. 678-689. , https://doi.org/10.1038/nrm2009
  • Castro, C.P., Giacomini, D., Nagashima, A.C., Onofri, C., Graciarena, M., Kobayashi, K., Paez-Pereda, M., Arzt, E., Reduced expression of the cytokine transducer gp130 inhibits hormone secretion, cell growth, and tumor development of pituitary lactosomatotrophic GH3 cells (2003) Endocrinology, 144, pp. 693-700. , https://doi.org/10.1210/en.2002-220891
  • Chen, J., Hersmus, N., Van, D.V., Caesens, P., Denef, C., Vankelecom, H., The adult pituitary contains a cell population displaying stem/ progenitor cell and early embryonic characteristics (2005) Endocrinology, 146, pp. 3985-3998. , https://doi.org/10.1210/en.2005-0185
  • Chen, J., Crabbe, A., Van, D.V., Vankelecom, H., The notch signaling system is present in the postnatal pituitary: Marked expression and regulatory activity in the newly discovered side population (2006) Molecular Endocrinology, 20, pp. 3293-3307. , https://doi.org/10.1210/me.2006-0293
  • Cheung, L., Le Tissier, P., Goldsmith, S.G., Treier, M., Lovell-Badge, R., Rizzoti, K., NOTCH activity differentially affects alternative cell fate acquisition and maintenance (2018) Elife, 7. , https://doi.org/10.7554/eLife.33318
  • Ellisen, L.W., Bird, J., West, D.C., Soreng, A.L., Reynolds, T.C., Smith, S.D., Sklar, J., TAN-1, the human homolog of the Drosophila notch gene, is broken by chromosomal translocations in T lymphoblastic neoplasms (1991) Cell, 66, pp. 649-661. , https://doi.org/10.1016/0092-8674(91)90111-B
  • Espinoza, I., Miele, L., Notch inhibitors for cancer treatment (2013) Pharmacology and Therapeutics, 139, pp. 95-110. , https://doi.org/10.1016/j.pharmthera.2013.02.003
  • Evans, C.O., Moreno, C.S., Zhan, X., McCabe, M.T., Vertino, P.M., Desiderio, D.M., Oyesiku, N.M., Molecular pathogenesis of human prolactinomas identified by gene expression profiling, RT-qPCR, and proteomic analyses (2008) Pituitary, 11, pp. 231-245. , https://doi.org/10.1007/s11102-007-0082-2
  • Farioli-Vecchioli, S., Tanori, M., Micheli, L., Mancuso, M., Leonardi, L., Saran, A., Ciotti, M.T., Pazzaglia, S., Inhibition of medulloblastoma tumorigenesis by the antiproliferative and pro-differentiative gene PC3 (2007) FASEB Journal, 21, pp. 2215-2225. , https://doi.org/10.1096/fj.06-7548com
  • Farioli-Vecchioli, S., Ceccarelli, M., Saraulli, D., Micheli, L., Cannas, S., D'Alessandro, F., Scardigli, R., Costanzi, M., Tis21 is required for adult neurogenesis in the subventricular zone and for olfactory behavior regulating cyclins, BMP4, Hes1/5 and Ids (2014) Frontiers in Cellular Neuroscience, 8, p. 98. , https://doi.org/10.3389/fncel.2014.00098
  • Funahashi, Y., Hernandez, S.L., Das, I., Ahn, A., Huang, J., Vorontchikhina, M., Sharma, A., Desilva, D.M., A notch1 ectodomain construct inhibits endothelial notch signaling, tumor growth, and angiogenesis (2008) Cancer Research, 68, pp. 4727-4735. , https://doi.org/10.1158/0008-5472.CAN-07-6499
  • Garcia-Tornadu, I., Diaz-Torga, G.S., Risso, G., Silveyra, P., Cataldi, N., Ramirez, M.C., Low, M.J., Becu-Villalobos, D., Hypothalamic orexin, OX1, αMSH, NPY and MCRs expression in dopaminergic D2R knockout mice (2009) Neuropeptides, 43, pp. 267-274. , https://doi.org/10.1016/j.npep.2009.06.002
  • Gilbert, C.A., Daou, M.C., Moser, R.P., Ross, A.H., Gamma-secretase inhibitors enhance temozolomide treatment of human gliomas by inhibiting neurosphere repopulation and xenograft recurrence (2010) Cancer Research, 70, pp. 6870-6879. , https://doi.org/10.1158/0008-5472.CAN-10-1378
  • Gordon, W.R., Arnett, K.L., Blacklow, S.C., The molecular logic of Notch signaling-a structural and biochemical perspective (2008) Journal of Cell Science, 121, pp. 3109-3119. , https://doi.org/10.1242/jcs.035683
  • Hafner, M., Ascano, M., Jr., Tuschl, T., New insights in the mechanism of microRNA-mediated target repression (2011) Nature Structural and Molecular Biology, 18, pp. 1181-1182. , https://doi.org/10.1038/nsmb.2170
  • Harrison, H., Farnie, G., Howell, S.J., Rock, R.E., Stylianou, S., Brennan, K.R., Bundred, N.J., Clarke, R.B., Regulation of breast cancer stem cell activity by signaling through the Notch4 receptor (2010) Cancer Research, 70, pp. 709-718. , https://doi.org/10.1158/0008-5472.CAN-09-1681
  • Heintzman, N.D., Stuart, R.K., Hon, G., Fu, Y., Ching, C.W., Hawkins, R.D., Barrera, L.O., Ching, K.A., Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome (2007) Nature Genetics, 39, pp. 311-318. , https://doi.org/10.1038/ng1966
  • Hurlbut, G.D., Kankel, M.W., Artavanis-Tsakonas, S., Nodal points and complexity of Notch-Ras signal integration (2009) PNAS, 106, pp. 2218-2223. , https://doi.org/10.1073/pnas.0812024106
  • Jiang, Z., Gui, S., Zhang, Y., Analysis of differential gene expression by bead-based fiber-optic array in growth-hormone-secreting pituitary adenomas (2010) Experimental and Therapeutic Medicine, 1, pp. 905-910. , https://doi.org/10.3892/etm.2010.137
  • Jiang, Z., Gui, S., Zhang, Y., Analysis of differential gene expression in plurihormonal pituitary adenomas using bead-based fiber-optic arrays (2012) Journal of Neuro-Oncology, 108, pp. 341-348. , https://doi.org/10.1007/s11060-011-0792-1
  • Kelberman, D., Rizzoti, K., Lovell-Badge, R., Robinson, I.C., Dattani, M.T., Genetic regulation of pituitary gland development in human and mouse (2009) Endocrine Reviews, 30, pp. 790-829. , https://doi.org/10.1210/er.2009-0008
  • Kent, W.J., Sugnet, C.W., Furey, T.S., Roskin, K.M., Pringle, T.H., Zahler, A.M., Haussler, D., The human genome browser at UCSC (2002) Genome Research, 12, pp. 996-1006. , https://doi.org/10.1101/gr.229102
  • Koch, U., Radtke, F., Notch signaling in solid tumors (2010) Notch Signaling, 92, pp. 411-455. , https://doi.org/10.1016/S0070-2153(10)92013-9, edn Ed R Kopan, Elsevier
  • Kovalovsky, D., Refojo, D., Liberman, A.C., Hochbaum, D., Pereda, M.P., Coso, O.A., Stalla, G.K., Arzt, E., Activation and induction of NUR77/NURR1 in corticotrophs by CRH/cAMP: Involvement of calcium, protein kinase A, and MAPK pathways (2002) Molecular Endocrinology, 16, pp. 1638-1651. , https://doi.org/10.1210/mend.16.7.0863
  • Lamy, M., Ferreira, A., Dias, J.S., Braga, S., Silva, G., Barbas, A., Notch-out for breast cancer therapies (2017) Nature Biotechnology, 39, pp. 215-221. , https://doi.org/10.1016/j.nbt.2017.08.004
  • Langmead, B., Trapnell, C., Pop, M., Salzberg, S.L., Ultrafast and memory-efficient alignment of short DNA sequences to the human genome (2009) Genome Biology, 10, p. R25. , https://doi.org/10.1186/gb-2009-10-3-r25
  • Lee, C.W., Raskett, C.M., Prudovsky, I., Altieri, D.C., Molecular dependence of estrogen receptor-negative breast cancer on a notch-survivin signaling axis (2008) Cancer Research, 68, pp. 5273-5281. , https://doi.org/10.1158/0008-5472.CAN-07-6673
  • Liu, H., Kennard, S., Lilly, B., NOTCH3 expression is induced in mural cells through an autoregulatory loop that requires endothelial-expressed JAGGED1 (2009) Circulation Research, 104, pp. 466-475. , https://doi.org/10.1161/CIRCRESAHA.108.184846
  • Liu, Z., Turkoz, A., Jackson, E.N., Corbo, J.C., Engelbach, J.A., Garbow, J.R., Piwnica-Worms, D.R., Kopan, R., Notch1 loss of heterozygosity causes vascular tumors and lethal hemorrhage in mice (2011) Journal of Clinical Investigation, 121, pp. 800-808. , https://doi.org/10.1172/JCI43114
  • Lu, R., Gao, H., Wang, H., Cao, L., Bai, J., Zhang, Y., Overexpression of the Notch3 receptor and its ligand Jagged1 in human clinically non-functioning pituitary adenomas (2013) Oncology Letters, 5, pp. 845-851. , https://doi.org/10.3892/ol.2013.1113
  • Luque, G.M., Perez-Millan, M.I., Ornstein, A.M., Cristina, C., Becu-Villalobos, D., Inhibitory effects of antivascular endothelial growth factor strategies in experimental dopamine-resistant prolactinomas (2011) Journal of Pharmacology and Experimental Therapeutics, 337, pp. 766-774. , https://doi.org/10.1124/jpet.110.177790
  • Mao, B., Zhang, Z., Wang, G., BTG2: A rising star of tumor suppressors (review) (2015) International Journal of Oncology, 46, pp. 459-464. , https://doi.org/10.3892/ijo.2014.2765
  • Mertens, F., Gremeaux, L., Chen, J., Fu, Q., Willems, C., Roose, H., Govaere, O., Becu-Villalobos, D., Pituitary tumors contain a side population with tumor stem cell-associated characteristics (2015) Endocrine-Related Cancer, 22, pp. 481-504. , https://doi.org/10.1530/ERC-14-0546
  • Miao, Z., Miao, Y., Lin, Y., Lu, X., Overexpression of the Notch3 receptor in non-functioning pituitary tumours (2012) Journal of Clinical Neuroscience, 19, pp. 107-110. , https://doi.org/10.1016/j.jocn.2011.07.029
  • Montorsi, L., Guizzetti, F., Alecci, C., Caporali, A., Martello, A., Atene, C.G., Parenti, S., Bortoluzzi, S., Loss of ZFP36 expression in colorectal cancer correlates to wnt/ß-catenin activity and enhances epithelial-to-mesenchymal transition through upregulation of zeb1, sox9 and macc1 (2016) Oncotarget, 7, pp. 59144-59157. , https://doi.org/10.18632/oncotarget.10828
  • Moreno, C.S., Evans, C.O., Zhan, X., Okor, M., Desiderio, D.M., Oyesiku, N.M., Novel molecular signaling and classification of human clinically nonfunctional pituitary adenomas identified by gene expression profiling and proteomic analyses (2005) Cancer Research, 65, pp. 10214-10222. , https://doi.org/10.1158/0008-5472.CAN-05-0884
  • Nantie, L.B., Himes, A.D., Getz, D.R., Raetzman, L.T., Notch signaling in postnatal pituitary expansion: Proliferation, progenitors, and cell specification (2014) Molecular Endocrinology, 28, pp. 731-744. , https://doi.org/10.1210/me.2013-1425
  • Ortiz, L.D., Syro, L.V., Scheithauer, B.W., Ersen, A., Uribe, H., Fadul, C.E., Rotondo, F., Kovacs, K., Anti-VEGF therapy in pituitary carcinoma (2012) Pituitary, 15, pp. 445-449. , https://doi.org/10.1007/s11102-011-0346-8
  • Pasquali, L., Gaulton, K.J., Rodriguez-Segui, S.A., Mularoni, L., Miguel-Escalada, I., Akerman, I., Tena, J.J., Van De Bunt, M., Pancreatic islet enhancer clusters enriched in type 2 diabetes risk-associated variants (2014) Nature Genetics, 46, pp. 136-143. , https://doi.org/10.1038/ng.2870
  • Perrone, S., Zubeldia-Brenner, L., Gazza, E., Demarchi, G., Baccarini, L., Baricalla, A., Mertens, F., Berner, S., Notch system is differentially expressed and activated in pituitary adenomas of distinct histotype, tumor cell lines and normal pituitaries (2017) Oncotarget, 8, pp. 57072-57088. , https://doi.org/10.18632/oncotarget.19046
  • Quinlan, A.R., Hall, I.M., BEDTools: A flexible suite of utilities for comparing genomic features (2010) Bioinformatics, 26, pp. 841-842. , https://doi.org/10.1093/bioinformatics/btq033
  • Radtke, F., Raj, K., The role of Notch in tumorigenesis: Oncogene or tumour suppressor? (2003) Nature Reviews. Cancer, 3, pp. 756-767. , https://doi.org/10.1038/nrc1186
  • Raetzman, L.T., Ross, S.A., Cook, S., Dunwoodie, S.L., Camper, S.A., Thomas, P.Q., Developmental regulation of Notch signaling genes in the embryonic pituitary: Prop1 deficiency affects Notch2 expression (2004) Developmental Biology, 265, pp. 329-340. , https://doi.org/10.1016/j.ydbio.2003.09.033
  • Raetzman, L.T., Wheeler, B.S., Ross, S.A., Thomas, P.Q., Camper, S.A., Persistent expression of Notch2 delays gonadotrope differentiation (2006) Molecular Endocrinology, 20, pp. 2898-2908. , https://doi.org/10.1210/me.2005-0394
  • Ranganathan, P., Weaver, K.L., Capobianco, A.J., Notch signalling in solid tumours: A little bit of everything but not all the time (2011) Nature Reviews. Cancer, 11, pp. 338-351. , https://doi.org/10.1038/nrc3035
  • Rouault, J.P., Falette, N., Guehenneux, F., Guillot, C., Rimokh, R., Wang, Q., Berthet, C., Pain, B., Identification of BTG2, an antiproliferative p53-dependent component of the DNA damage cellular response pathway (1996) Nature Genetics, 14, pp. 482-486. , https://doi.org/10.1038/ng1296-482
  • Sjolund, J., Johansson, M., Manna, S., Norin, C., Pietras, A., Beckman, S., Nilsson, E., Axelson, H., Suppression of renal cell carcinoma growth by inhibition of Notch signaling in vitro and in vivo (2008) Journal of Clinical Investigation, 118, pp. 217-228. , https://doi.org/10.1172/JCI32086
  • Tabuchi, Y., Kitamura, T., Fukuhara, A., Mukai, K., Onodera, T., Miyata, Y., Hamasaki, T., Morii, E., Nur77 gene expression levels were involved in different ACTH-secretion autonomy between Cushing's disease and subclinical Cushing's disease (2016) Endocrine Journal, 63, pp. 545-554. , https://doi.org/10.1507/endocrj.EJ15-0695
  • Tando, Y., Fujiwara, K., Yashiro, T., Kikuchi, M., Localization of Notch signaling molecules and their effect on cellular proliferation in adult rat pituitary (2013) Cell and Tissue Research, 351, pp. 511-519. , https://doi.org/10.1007/s00441-012-1532-3
  • Terra, R., Luo, H., Qiao, X., Wu, J., Tissue-specific expression of B-cell translocation gene 2 (BTG2) and its function in T-cell immune responses in a transgenic mouse model (2008) International Immunology, 20, pp. 317-326. , https://doi.org/10.1093/intimm/dxm152
  • Touma, W., Hoostal, S., Peterson, R.A., Wiernik, A., SantaCruz, K.S., Lou, E., Successful treatment of pituitary carcinoma with concurrent radiation, temozolomide, and bevacizumab after resection (2017) Journal of Clinical Neuroscience, 41, pp. 75-77. , https://doi.org/10.1016/j.jocn.2017.02.052
  • Trapnell, C., Pachter, L., Salzberg, S.L., TopHat: Discovering splice junctions with RNA-Seq (2009) Bioinformatics, 25, pp. 1105-1111. , https://doi.org/10.1093/bioinformatics/btp120
  • Trapnell, C., Roberts, A., Goff, L., Pertea, G., Kim, D., Kelley, D.R., Pimentel, H., Pachter, L., Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks (2012) Nature Protocols, 7, pp. 562-578. , https://doi.org/10.1038/nprot.2012.016
  • Vela, J., Perez-Millan, M.I., Becu-Villalobos, D., Diaz-Torga, G., Different kinases regulate activation of voltage-dependent calcium channels by depolarization in GH3 cells (2007) American Journal of Physiology. Cell Physiology, 293, pp. C951-C959. , https://doi.org/10.1152/ajpcell.00429.2006
  • Wang, J., Wakeman, T.P., Lathia, J.D., Hjelmeland, A.B., Wang, X.F., White, R.R., Rich, J.N., Sullenger, B.A., Notch promotes radioresistance of glioma stem cells (2010) Stem Cells, 28, pp. 17-28. , https://doi.org/10.1002/stem.261
  • Wang, Z., Li, Y., Ahmad, A., Banerjee, S., Azmi, A.S., Kong, D., Wojewoda, C., Sarkar, F.H., Down-regulation of Notch-1 is associated with Akt and FoxM1 in inducing cell growth inhibition and apoptosis in prostate cancer cells (2011) Journal of Cellular Biochemistry, 112, pp. 78-88. , https://doi.org/10.1002/jcb.25587
  • Wenzl, K., Troppan, K., Neumeister, P., Deutsch, A.J., The nuclear orphan receptor NR4A1 and NR4A3 as tumor suppressors in hematologic neoplasms (2015) Current Drug Targets, 16, pp. 38-46. , https://doi.org/10.2174/1389450115666141120112818
  • Xu, Q., Yuan, X., Tunici, P., Liu, G., Fan, X., Xu, M., Hu, J., Black, K.L., Isolation of tumour stem-like cells from benign tumours (2009) British Journal of Cancer, 101, pp. 303-311. , https://doi.org/10.1038/sj.bjc.6605142
  • Zeng, Q., Li, S., Chepeha, D.B., Giordano, T.J., Li, J., Zhang, H., Polverini, P.J., Wang, C.Y., Crosstalk between tumor and endothelial cells promotes tumor angiogenesis by MAPK activation of Notch signaling (2005) Cancer Cell, 8, pp. 13-23. , https://doi.org/10.1016/j.ccr.2005.06.004
  • Zhang, Y., Liu, T., Meyer, C.A., Eeckhoute, J., Johnson, D.S., Bernstein, B.E., Nusbaum, C., Li, W., Model-based analysis of ChIP-Seq (MACS) (2008) Genome Biology, 9, p. R137. , https://doi.org/10.1186/gb-2008-9-9-r137
  • Zukeran, A., Takahashi, A., Takaoka, S., Mohamed, H.M., Suzuki, T., Ikematsu, S., Yamamoto, T., The CCR4-NOT deadenylase activity contributes to generation of induced pluripotent stem cells (2016) Biochemical and Biophysical Research Communications, 474, pp. 233-239. , https://doi.org/10.1016/j.bbrc.2016.03.119

Citas:

---------- APA ----------
Zubeldía-Brenner, L., De Winne, C., Perrone, S., Rodríguez-Seguí, S.A., Willems, C., Ornstein, A.M., Lacau-Mengido, I.,..., Becu-Villalobos, D. (2019) . Inhibition of Notch signaling attenuates pituitary adenoma growth in Nude mice. Endocrine-Related Cancer, 26(1), 13-29.
http://dx.doi.org/10.1530/ERC-18-0337
---------- CHICAGO ----------
Zubeldía-Brenner, L., De Winne, C., Perrone, S., Rodríguez-Seguí, S.A., Willems, C., Ornstein, A.M., et al. "Inhibition of Notch signaling attenuates pituitary adenoma growth in Nude mice" . Endocrine-Related Cancer 26, no. 1 (2019) : 13-29.
http://dx.doi.org/10.1530/ERC-18-0337
---------- MLA ----------
Zubeldía-Brenner, L., De Winne, C., Perrone, S., Rodríguez-Seguí, S.A., Willems, C., Ornstein, A.M., et al. "Inhibition of Notch signaling attenuates pituitary adenoma growth in Nude mice" . Endocrine-Related Cancer, vol. 26, no. 1, 2019, pp. 13-29.
http://dx.doi.org/10.1530/ERC-18-0337
---------- VANCOUVER ----------
Zubeldía-Brenner, L., De Winne, C., Perrone, S., Rodríguez-Seguí, S.A., Willems, C., Ornstein, A.M., et al. Inhibition of Notch signaling attenuates pituitary adenoma growth in Nude mice. Endocr.-Relat. Cancer. 2019;26(1):13-29.
http://dx.doi.org/10.1530/ERC-18-0337