1,549
Views
7
CrossRef citations to date
0
Altmetric
Reports

mTOR transcriptionally and post-transcriptionally regulates Npm1 gene expression to contribute to enhanced proliferation in cells with Pten inactivation

, , , , , , , , & show all
Pages 1352-1362 | Received 16 Sep 2015, Accepted 10 Mar 2016, Published online: 06 Apr 2016

References

  • Aramburu J, Ortells MC, Tejedor S, Buxade M, Lopez-Rodriguez C. Transcriptional regulation of the stress response by mTOR. Sci Signal 2014; 7:re2; PMID:24985347; http://dx.doi.org/10.1126/scisignal.2005326
  • Laplante M, Sabatini DM. mTOR signaling in growth control and disease. Cell 2012; 149:274-93; PMID:22500797; http://dx.doi.org/10.1016/j.cell.2012.03.017
  • Hara K, Maruki Y, Long X, Yoshino K, Oshiro N, Hidayat S, Tokunaga C, Avruch J, Yonezawa K. Raptor, a binding partner of target of rapamycin (TOR), mediates TOR action. Cell 2002; 110:177-89; PMID:12150926; http://dx.doi.org/10.1016/S0092-8674(02)00833-4
  • Sarbassov DD, Ali SM, Kim DH, Guertin DA, Latek RR, Erdjument-Bromage H, Tempst P, Sabatini DM. Rictor, a novel binding partner of mTOR, defines a rapamycin-insensitive and raptor-independent pathway that regulates the cytoskeleton. Curr Biol 2004; 14:1296-302; PMID:15268862; http://dx.doi.org/10.1016/j.cub.2004.06.054
  • Ma XM, Blenis J. Molecular mechanisms of mTOR-mediated translational control. Nat Rev Mol Cell Biol 2009; 10:307-18; PMID:19339977; http://dx.doi.org/10.1038/nrm2672
  • Tsang CK, Liu H, Zheng XF. mTOR binds to the promoters of RNA polymerase I- and III-transcribed genes. Cell Cycle 2010; 9:953-7; PMID:20038818; http://dx.doi.org/10.4161/cc.9.5.10876
  • Chaveroux C, Eichner LJ, Dufour CR, Shatnawi A, Khoutorsky A, Bourque G, Sonenberg N, Giguere V. Molecular and genetic crosstalks between mTOR and ERRalpha are key determinants of rapamycin-induced nonalcoholic fatty liver. Cell Metab 2013; 17:586-98; PMID:23562079; http://dx.doi.org/10.1016/j.cmet.2013.03.003
  • Feuerstein N, Mond JJ. “Numatrin,” a nuclear matrix protein associated with induction of proliferation in B lymphocytes. J Biol Chem 1987; 262:11389-97; PMID:3301855
  • Okuwaki M. The structure and functions of NPM1/Nucleophsmin/B23, a multifunctional nucleolar acidic protein. J Biochem 2008; 143:441-8; PMID:18024471; http://dx.doi.org/10.1093/jb/mvm222
  • Johansson H, Simonsson S. Core transcription factors, Oct4, Sox2 and Nanog, individually form complexes with nucleophosmin (Npm1) to control embryonic stem (ES) cell fate determination. Aging (Albany NY) 2010; 2:815-22; PMID:21076177; http://dx.doi.org/10.18632/aging.100222
  • Chan WY, Liu QR, Borjigin J, Busch H, Rennert OM, Tease LA, Chan PK. Characterization of the cDNA encoding human nucleophosmin and studies of its role in normal and abnormal growth. Biochem 1989; 28:1033-9; http://dx.doi.org/10.1021/bi00429a017
  • Feuerstein N, Chan PK, Mond JJ. Identification of numatrin, the nuclear matrix protein associated with induction of mitogenesis, as the nucleolar protein B23. Implication for the role of the nucleolus in early transduction of mitogenic signals. J Biol Chem 1988; 263:10608-12; PMID:3392030
  • Li J, Zhang X, Sejas DP, Bagby GC, Pang Q. Hypoxia-induced nucleophosmin protects cell death through inhibition of p53. J Biol Chem 2004; 279:41275-9; PMID:15310764; http://dx.doi.org/10.1074/jbc.C400297200
  • Wu MH, Chang JH, Chou CC, Yung BY. Involvement of nucleophosmin/B23 in the response of HeLa cells to UV irradiation. Int J Cancer 2002; 97:297-305; PMID:11774280; http://dx.doi.org/10.1002/ijc.1606
  • Wu MH, Yung BY. UV stimulation of nucleophosmin/B23 expression is an immediate-early gene response induced by damaged DNA. J Biol Chem 2002; 277:48234-40; PMID:12374805; http://dx.doi.org/10.1074/jbc.M206550200
  • Grisendi S, Mecucci C, Falini B, Pandolfi PP. Nucleophosmin and cancer. Nat Rev Cancer 2006; 6:493-505; PMID:16794633; http://dx.doi.org/10.1038/nrc1885
  • Chan PK, Chan FY, Morris SW, Xie Z. Isolation and characterization of the human nucleophosmin/B23 (NPM) gene: identification of the YY1 binding site at the 5′ enhancer region. Nucleic Acids Res 1997; 25:1225-32; PMID:9092633; http://dx.doi.org/10.1093/nar/25.6.1225
  • Zeller KI, Haggerty TJ, Barrett JF, Guo Q, Wonsey DR, Dang CV. Characterization of nucleophosmin (B23) as a Myc target by scanning chromatin immunoprecipitation. J Biol Chem 2001; 276:48285-91; PMID:11604407
  • Cunningham JT, Rodgers JT, Arlow DH, Vazquez F, Mootha VK, Puigserver P. mTOR controls mitochondrial oxidative function through a YY1-PGC-1alpha transcriptional complex. Nature 2007; 450:736-40; PMID:18046414; http://dx.doi.org/10.1038/nature06322
  • Duvel K, Yecies JL, Menon S, Raman P, Lipovsky AI, Souza AL, Triantafellow E, Ma Q, Gorski R, Cleaver S, et al. Activation of a metabolic gene regulatory network downstream of mTOR complex 1. Mol Cell 2010; 39:171-83; PMID:20670887; http://dx.doi.org/10.1016/j.molcel.2010.06.022
  • Leotoing L, Meunier L, Manin M, Mauduit C, Decaussin M, Verrijdt G, Claessens F, Benahmed M, Veyssiere G, Morel L, et al. Influence of nucleophosmin/B23 on DNA binding and transcriptional activity of the androgen receptor in prostate cancer cell. Oncogene 2008; 27:2858-67; PMID:18037965; http://dx.doi.org/10.1038/sj.onc.1210942
  • Loubeau G, Boudra R, Maquaire S, Lours-Calet C, Beaudoin C, Verrelle P, Morel L. NPM1 silencing reduces tumour growth and MAPK signalling in prostate cancer cells. PloS One 2014; 9:e96293; PMID:24796332; http://dx.doi.org/10.1371/journal.pone.0096293
  • Wang S, Gao J, Lei Q, Rozengurt N, Pritchard C, Jiao J, Thomas GV, Li G, Roy-Burman P, Nelson PS, et al. Prostate-specific deletion of the murine Pten tumor suppressor gene leads to metastatic prostate cancer. Cancer Cell 2003; 4:209-21; PMID:14522255; http://dx.doi.org/10.1016/S1535-6108(03)00215-0
  • Laplante M, Sabatini DM. mTOR signaling at a glance. J Cell Sci 2009; 122:3589-94; PMID:19812304; http://dx.doi.org/10.1242/jcs.051011
  • Sarbassov DD, Ali SM, Sengupta S, Sheen JH, Hsu PP, Bagley AF, Markhard AL, Sabatini DM. Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB. Mol Cell 2006; 22:159-68; PMID:16603397; http://dx.doi.org/10.1016/j.molcel.2006.03.029
  • Pelletier CL, Maggi LB, Jr, Brady SN, Scheidenhelm DK, Gutmann DH, Weber JD. TSC1 sets the rate of ribosome export and protein synthesis through nucleophosmin translation. Cancer Res 2007; 67:1609-17; PMID:17308101; http://dx.doi.org/10.1158/0008-5472.CAN-06-2875
  • Albig AR, Decker CJ. The target of rapamycin signaling pathway regulates mRNA turnover in the yeast Saccharomyces cerevisiae. Mol Biol Cell 2001; 12:3428-38; PMID:11694578; http://dx.doi.org/10.1091/mbc.12.11.3428
  • Grisendi S, Bernardi R, Rossi M, Cheng K, Khandker L, Manova K, Pandolfi PP. Role of nucleophosmin in embryonic development and tumorigenesis. Nature 2005; 437:147-53; PMID:16007073; http://dx.doi.org/10.1038/nature03915
  • Diao L, Chen YG. PTEN, a general negative regulator of cyclin D expression. Cell Res 2007; 17:291-2; PMID:17426697; http://dx.doi.org/10.1038/cr.2007.24
  • Lim MJ, Wang XW. Nucleophosmin and human cancer. Cancer Detect Prev 2006; 30:481-90; PMID:17113241; http://dx.doi.org/10.1016/j.cdp.2006.10.008
  • Lindstrom MS. NPM1/B23: A Multifunctional Chaperone in Ribosome Biogenesis and Chromatin Remodeling. Biochem Res Int 2011; 2011:195209; PMID:21152184; http://dx.doi.org/10.1155/2011/195209
  • Yung BY. Oncogenic role of nucleophosmin/B23. Chang Gung Med J 2007; 30:285-93; PMID:17939258
  • Yu Y, Maggi LB, Jr, Brady SN, Apicelli AJ, Dai MS, Lu H, Weber JD. Nucleophosmin is essential for ribosomal protein L5 nuclear export. Mol Cell Biol 2006; 26:3798-809; PMID:16648475; http://dx.doi.org/10.1128/MCB.26.10.3798-3809.2006
  • Savkur RS, Olson MO. Preferential cleavage in pre-ribosomal RNA byprotein B23 endoribonuclease. Nucleic Acids Res 1998; 26:4508-15; PMID:9742256; http://dx.doi.org/10.1093/nar/26.19.4508
  • Szebeni A, Herrera JE, Olson MO. Interaction of nucleolar protein B23 with peptides related to nuclear localization signals. Biochemistry 1995; 34:8037-42; PMID:7794916; http://dx.doi.org/10.1021/bi00025a009
  • Itahana K, Bhat KP, Jin A, Itahana Y, Hawke D, Kobayashi R, Zhang Y. Tumor suppressor ARF degrades B23, a nucleolar protein involved in ribosome biogenesis and cell proliferation. Mol Cell 2003; 12:1151-64; PMID:14636574; http://dx.doi.org/10.1016/S1097-2765(03)00431-3
  • Maggi LB, Jr, Kuchenruether M, Dadey DY, Schwope RM, Grisendi S, Townsend RR, Pandolfi PP, Weber JD. Nucleophosmin serves as a rate-limiting nuclear export chaperone for the Mammalian ribosome. Mol Cell Biol 2008; 28:7050-65; PMID:18809582; http://dx.doi.org/10.1128/MCB.01548-07
  • Iadevaia V, Zhang Z, Jan E, Proud CG. mTOR signaling regulates the processing of pre-rRNA in human cells. Nucleic Acids Res 2012; 40:2527-39; PMID:22121221; http://dx.doi.org/10.1093/nar/gkr1040
  • Cammas A, Sanchez BJ, Lian XJ, Dormoy-Raclet V, van der Giessen K, Lopez de Silanes I, Ma J, Wilusz C, Richardson J, Gorospe M, et al. Destabilization of nucleophosmin mRNA by the HuR/KSRP complex is required for muscle fibre formation. Nat Commun 2014; 5:4190; PMID:24969639; http://dx.doi.org/10.1038/ncomms5190
  • Wang X, Huang H, Young KH. The PTEN tumor suppressor gene and its role in lymphoma pathogenesis. Aging (Albany NY) 2015; 7:1032-49; PMID:26655726; http://dx.doi.org/10.18632/aging.100855
  • Yoshimoto M, Cutz JC, Nuin PA, Joshua AM, Bayani J, Evans AJ, Zielenska M, Squire JA. Interphase FISH analysis of PTEN in histologic sections shows genomic deletions in 68% of primary prostate cancer and 23% of high-grade prostatic intra-epithelial neoplasias. Cancer Genet Cytogenet 2006; 169:128-37; PMID:16938570; http://dx.doi.org/10.1016/j.cancergencyto.2006.04.003
  • McCall P, Witton CJ, Grimsley S, Nielsen KV, Edwards J. Is PTEN loss associated with clinical outcome measures in human prostate cancer? Br J Cancer 2008; 99:1296-301; PMID:18854827; http://dx.doi.org/10.1038/sj.bjc.6604680
  • Cairns P, Okami K, Halachmi S, Halachmi N, Esteller M, Herman JG, Jen J, Isaacs WB, Bova GS, Sidransky D. Frequent inactivation of PTEN/MMAC1 in primary prostate cancer. Cancer Res 1997; 57:4997-5000; PMID:9371490
  • Majumder PK, Yeh JJ, George DJ, Febbo PG, Kum J, Xue Q, Bikoff R, Ma H, Kantoff PW, Golub TR, et al. Prostate intraepithelial neoplasia induced by prostate restricted Akt activation: the MPAKT model. Proc Natl Acad Sci U S A 2003; 100:7841-6; PMID:12799464; http://dx.doi.org/10.1073/pnas.1232229100
  • Kremer CL, Klein RR, Mendelson J, Browne W, Samadzedeh LK, Vanpatten K, Highstrom L, Pestano GA, Nagle RB. Expression of mTOR signaling pathway markers in prostate cancer progression. Prostate 2006; 66:1203-12; PMID:16652388; http://dx.doi.org/10.1002/pros.20410
  • Subong EN, Shue MJ, Epstein JI, Briggman JV, Chan PK, Partin AW. Monoclonal antibody to prostate cancer nuclear matrix protein (PRO:4-216) recognizes nucleophosmin/B23. Prostate 1999; 39:298-304; PMID:10344220; http://dx.doi.org/10.1002/(SICI)1097-0045(19990601)39:4<298::AID-PROS11>3.0.CO;2-M
  • Grasso CS, Wu YM, Robinson DR, Cao X, Dhanasekaran SM, Khan AP, Quist MJ, Jing X, Lonigro RJ, Brenner JC, et al. The mutational landscape of lethal castration-resistant prostate cancer. Nature 2012; 487:239-43; PMID:22722839; http://dx.doi.org/10.1038/nature11125
  • Berthon A, Sahut-Barnola I, Lambert-Langlais S, de Joussineau C, Damon-Soubeyrand C, Louiset E, Taketo MM, Tissier F, Bertherat J, Lefrancois-Martinez AM, et al. Constitutive β-catenin activation induces adrenal hyperplasia and promotes adrenal cancer development. Hum Mol Genet 2010; 19:1561-76; PMID:20106872; http://dx.doi.org/10.1093/hmg/ddq029

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.