p54^nrb/NONO Regulates Cyclic AMP-Dependent Glucocorticoid Production by Modulating Phosphodiesterase mRNA Splicing and Degradation

REFERENCES

• Yang Y-S, Hanke JH, Carayannopoulos L, Craft CM, Capra JD, Tucker PW. 1993. NonO, a non-POU-domain-containing, octamer-binding protein, is the mammalian homolog of Drosophila nonAdiss. Mol Cell Biol 13:5593–5603.
   PubMed Web of Science ®Google Scholar
• Dong B, Horowitz DS, Kobayashi R, Krainer AR. 1993. Purification and cDNA cloning of HeLa cell p54nrb, a nuclear protein with two RNA recognition motifs and extensive homology to human splicing factor PSF and Drosophila NONA/BJ6. Nucleic Acids Res 21:4085–4092. http://dx.doi.org/10.1093/nar/21.17.4085.
   PubMedGoogle Scholar
• Shav-Tal Y, Zipori D. 2002. PSF and p54(nrb)/NonO—multi-functional nuclear proteins. FEBS Lett 531:109–114. http://dx.doi.org/10.1016/S0014-5793(02)03447-6.
   PubMed Web of Science ®Google Scholar
• Emili A, Shales M, McCracken S, Xie W, Tucker PW, Kobayashi R, Blencowe BJ, Ingles CJ. 2002. Splicing and transcription-associated proteins PSF and p54nrb/nonO bind to the RNA polymerase II CTD. RNA 8:1102–1111. http://dx.doi.org/10.1017/S1355838202025037.
   PubMed Web of Science ®Google Scholar
• Patton JG, Porro EB, Galceran J, Tempst P, Nadal-Ginard B. 1993. Cloning and characterization of PSF, a novel pre-mRNA splicing factor. Genes Dev 7:393–406. http://dx.doi.org/10.1101/gad.7.3.393.
   PubMedGoogle Scholar
• DeCerbo J, Carmichael GG. 2005. Retention and repression: fates of hyperedited RNAs in the nucleus. Curr Opin Cell Biol 17:302–308. http://dx.doi.org/10.1016/j.ceb.2005.04.008.
   PubMedGoogle Scholar
• Passon DM, Lee M, Rackham O, Stanley WA, Sadowska A, Filipovska A, Fox AH, Bond CS. 2012. Structure of the heterodimer of human NONO and paraspeckle protein component 1 and analysis of its role in subnuclear body formation. Proc Natl Acad Sci U S A 109:4846–4850. http://dx.doi.org/10.1073/pnas.1120792109.
   PubMedGoogle Scholar
• Basu A, dong B, Krainer AR, Howe CC. 1997. The intracisternal A-particle proximal enhancer-binding protein activates transcription and is identical to the RNA- and DNA-binding protein p54nrb/NonO. Mol Cell Biol 17:377–686.
   Google Scholar
• Yang Y-S, Yang M-C W, Tucker PW, Capra JD. 1997. NonO enhances the association of many DNA-binding proteins to their targets. Nucleic Acids Res 25:2284–2292. http://dx.doi.org/10.1093/nar/25.12.2284.
   PubMedGoogle Scholar
• Mathur M, Tucker PW, Samuels HH. 2001. PSF is a novel corepressor that mediates its effect through Sin3A and the DNA binding domain of nuclear hormone receptors. Mol Cell Biol 21:2298–2311. http://dx.doi.org/10.1128/MCB.21.7.2298-2311.2001.
   PubMedGoogle Scholar
• Ishitani K, Yoshida T, Kitagawa H, Ohta H, Nozawa S, Kato S. 2003. p54nrb acts as a transcriptional coactivator for activation function 1 of the human androgen receptor. Biochem Biophys Res Commun 306:660–665. http://dx.doi.org/10.1016/S0006-291X(03)01021-0.
   PubMedGoogle Scholar
• Zhang Z, Carmichael GG. 2001. The fate of dsRNA in the nucleus: a p54(nrb)-containing complex mediates the nuclear retention of promiscuously A-to-I edited RNAs. Cell 106:465–475. http://dx.doi.org/10.1016/S0092-8674(01)00466-4.
   PubMed Web of Science ®Google Scholar
• Hisada-Ishii S, Ebihara M, Kobayashi N, Kitagawa Y. 2007. Bipartite nuclear localization signal of matrin 3 is essential for vertebrate cells. Biochem Biophys Res Commun 354:72–76. http://dx.doi.org/10.1016/j.bbrc.2006.12.191.
   PubMedGoogle Scholar
• Straub T, Grue P, Uhse A, Lisby M, Knudsen BR, Tange TO, Westergaard O, Boege F. 1998. The RNA-splicing factor PSF/p54 controls DNA-topoisomerase I activity by a direct interaction. J Biol Chem 273:26261–26264. http://dx.doi.org/10.1074/jbc.273.41.26261.
   PubMedGoogle Scholar
• Fox AH, Bond CS, Lamond AI. 2005. p54nrb forms a heterodimer with PSP1 that localizes to paraspeckles in an RNA-dependent manner. Mol Biol Cell 16:5304–5315. http://dx.doi.org/10.1091/mbc.E05-06-0587.
   PubMed Web of Science ®Google Scholar
• Amelio AL, Miraglia LJ, Conkright JJ, Mercer BA, Batalov S, Cavett V, Orth AP, Busby J, Hogenesch JB, Conkright MD. 2007. A coactivator trap identifies NONO (p54nrb) as a component of the cAMP-signaling pathway. Proc Natl Acad Sci U S A 104:20314–20319. http://dx.doi.org/10.1073/pnas.0707999105.
   PubMed Web of Science ®Google Scholar
• Pavao M, Huang Y-H, Hafer L, Moreland R, Traish A. 2001. Immunodetection of nmt55/p54nrb isoforms in human breast cancer. BMC Cancer 1:15. http://dx.doi.org/10.1186/1471-2407-1-15.
   PubMedGoogle Scholar
• Hallier M, Tavitian A, Moreau-Gachelin F. 1996. The transcription factor Spi-1/PU.1 binds RNA and interferes with the RNA-binding protein p54. J Biol Chem 271:11177–11181. http://dx.doi.org/10.1074/jbc.271.19.11177.
   PubMedGoogle Scholar
• Sewer MB, Dammer EB, Jagarlapudi S. 2007. Transcriptional regulation of adrenocortical steroidogenic gene expression. Drug Metab Rev 39:371–388. http://dx.doi.org/10.1080/03602530701498828.
   PubMed Web of Science ®Google Scholar
• Sewer MB, Waterman MR. 2003. ACTH modulation of transcription factors responsible for steroid hydroxylase gene expression in the adrenal cortex. Microsc Res Tech 61:300–307. http://dx.doi.org/10.1002/jemt.10339.
   PubMed Web of Science ®Google Scholar
• Dammer EB, Leon A, Sewer MB. 2007. Coregulator exchange and sphingosine-sensitive cooperativity of steroidogenic factor-1, general control nonderepressed 5, p54, and p160 coactivators regulate cyclic adenosine 3′,5′-monophosphate-dependent cytochrome P450c17 transcription rate. Mol Endocrinol 21:415–438. http://dx.doi.org/10.1210/me.2006-0361.
   PubMed Web of Science ®Google Scholar
• Sewer MB, Nguyen V, Huang C-J, Tucker PW, Kagawa N, Waterman MR. 2002. Transcriptional activation of human CYP17 in H295R adrenocortical cells depends on complex formation between p54nrb/NonO, PSF and SF-1, a complex which also participates in repression of transcription. Endocrinology 143:1280–1290. http://dx.doi.org/10.1210/endo.143.4.8748.
   PubMed Web of Science ®Google Scholar
• Bender AT, Beavo JA. 2006. Cyclic nucleotide phosphodiesterases: molecular regulation to clinical use. Pharmacol Rev 58:488–520. http://dx.doi.org/10.1124/pr.58.3.5.
   PubMed Web of Science ®Google Scholar
• Omori K, Kotera J. 2007. Overview of PDEs and their regulation. Circ Res 100:309–327. http://dx.doi.org/10.1161/01.RES.0000256354.95791.f1.
   PubMed Web of Science ®Google Scholar
• Horvath A, Boikos S, Giatzakis C, Robinson-White A, Groussin L, Griffin KJ, Stein E, Levine E, Delimpasi G, Hsiao HP, Keil M, Heyerdahl S, Matyakhina L, Libe R, Fratticci A, Kirschner LS, Cramer K, Gaillard RC, Bertagna X, Carney JA, Bertherat J, Bossis I, Stratakis CA. 2006. A genome-wide scan identifies mutations in the gene encoding phosphodiesterase 11A4 (PDE11A) in individuals with adrenocortical hyperplasia. Nat Genet 38:794–800. http://dx.doi.org/10.1038/ng1809.
   PubMed Web of Science ®Google Scholar
• Parker KL, Rice DA, Lala DS, Ikeda Y, Luo X, Wong M, Bakke M, Zhao L, Frigeri C, Hanley NA, Stallings N, Schimmer BP. 2002. Steroidogenic factor 1: an essential mediator of endocrine development. Recent Prog Horm Res 57:19–36. http://dx.doi.org/10.1210/rp.57.1.19.
   PubMedGoogle Scholar
• Schimmer BP, White PC. 2010. Steroidogenic factor 1: its roles in differentiation, development, and disease. Mol Endocrinol 24:1322–1337. http://dx.doi.org/10.1210/me.2009-0519.
   PubMedGoogle Scholar
• Bassett MH, Suzuki T, Sasano H, De Vries CJ, Jimenez PT, Carr BR, Rainey WE. 2004. The orphan nuclear receptor NGFIB regulates transcription of 3beta-hydroxysteroid dehydrogenase. implications for the control of adrenal functional zonation. J Biol Chem 279:37622–37630. http://dx.doi.org/10.1074/jbc.M405431200.
   PubMed Web of Science ®Google Scholar
• Bassett MH, Suzuki T, Sasano H, White PC, Rainey WE. 2004. The orphan nuclear receptors NURR1 and NGFIB regulate adrenal aldosterone production. Mol Endocrinol 18:279–290. http://dx.doi.org/10.1210/me.2003-0005.
   PubMed Web of Science ®Google Scholar
• Boikos SA, Horvath A, Heyerdahl S, Stein E, Robinson-White A, Bossis I, Bertherat J, Carney JA, Stratakis CA. 2008. Phosphodiesterase 11A expression in the adrenal cortex, primary pigmented nodular adrenocortical disease, and other corticotropin-independent lesions. Horm Metab Res 40:347–353. http://dx.doi.org/10.1055/s-2008-1076694.
   PubMedGoogle Scholar
• Faucz FR, Horvath A, Rothenbuhler A, Almeida MQ, Libe R, Raffin-Sanson ML, Bertherat J, Carraro DM, Soares FA, Molina Gde C, Campos AH, Alexandre RB, Bendhack ML, Nesterova M, Stratakis CA. 2011. Phosphodiesterase 11A (PDE11A) genetic variants may increase susceptibility to prostatic cancer. J Clin Endocrinol Metab 96:E135–E140. http://dx.doi.org/10.1210/jc.2010-1655.
   PubMedGoogle Scholar
• Libe R, Horvath A, Vezzosi D, Fratticci A, Coste J, Perlemoine K, Ragazzon B, Guillaud-Bataille M, Groussin L, Clauser E, Raffin-Sanson ML, Siegel J, Moran J, Drori-Herishanu L, Faucz FR, Lodish M, Nesterova M, Bertagna X, Bertherat J, Stratakis CA. 2011. Frequent phosphodiesterase 11A gene (PDE11A) defects in patients with Carney complex (CNC) caused by PRKAR1A mutations: PDE11A may contribute to adrenal and testicular tumors in CNC as a modifier of the phenotype. J Clin Endocrinol Metab 96:E208–E214. http://dx.doi.org/10.1210/jc.2010-1704.
   PubMedGoogle Scholar
• Goldstein JL, Brown MS. 2009. The LDL receptor. Arterioscler Thromb Vasc Biol 29:431–438. http://dx.doi.org/10.1161/ATVBAHA.108.179564.
   PubMed Web of Science ®Google Scholar
• Oscai LB, Essig DA, Palmer WK. 1990. Lipase regulation of muscle triglyceride hydrolysis. J Appl Physiol 69:1571–1577.
   PubMed Web of Science ®Google Scholar
• Fayard E, Auwerx J, Schoonjans K. 2004. LRH-1: an orphan nuclear receptor involved in development, metabolism and steroidogenesis. Trends Cell Biol 14:250–260. http://dx.doi.org/10.1016/j.tcb.2004.03.008.
   PubMed Web of Science ®Google Scholar
• Izumi H, McCloskey A, Shinmyozu K, Ohno M. 2014. p54nrb/NONO and PSF promote U snRNA nuclear export by accelerating its export complex assembly. Nucleic Acids Res 42:3998–4007. http://dx.doi.org/10.1093/nar/gkt1365.
   PubMed Web of Science ®Google Scholar
• West S, Gromak N, Proudfoot NJ. 2004. Human 5′→3′ exonuclease Xrn2 promotes transcription termination at co-transcriptional cleavage sites. Nature 432:522–525. http://dx.doi.org/10.1038/nature03035.
   PubMed Web of Science ®Google Scholar
• Kaneko S, Rozenblatt-Rosen O, Meyerson M, Manley JL. 2007. The multifunctional protein p54nrb/PSF recruits the exonuclease XRN2 to facilitate pre-mRNA 3′ processing and transcription termination. Genes Dev 21:1779–1789. http://dx.doi.org/10.1101/gad.1565207.
   PubMed Web of Science ®Google Scholar
• Bianconcini A, Lupo A, Capone S, Quadro L, Monti M, Zurlo D, Fucci A, Sabatino L, Brunetti A, Chiefari E, Gottesman ME, Blaner WS, Colantuoni V. 2009. Transcriptional activity of the murine retinol-binding protein gene is regulated by a multiprotein complex containing HMGA1, p54 nrb/NonO, protein-associated splicing factor (PSF) and steroidogenic factor 1 (SF1)/liver receptor homologue 1 (LRH-1). Int J Biochem Cell Biol 41:2189–2203. http://dx.doi.org/10.1016/j.biocel.2009.04.011.
   PubMedGoogle Scholar
• Ong SA, Tan JJ, Tew WL, Chen KS. 2011. Rasd1 modulates the coactivator function of NonO in the cyclic AMP pathway. PLoS One 6:e24401. http://dx.doi.org/10.1371/journal.pone.0024401.
   PubMedGoogle Scholar
• Basu A, Dong B, Krainer AR, Howe CC. 1997. The intracisternal A-particle proximal enhancer-binding protein activates transcription and is identical to the RNA- and DNA-binding protein p54nrb/NonO. Mol Cell Biol 17:677–686.
   PubMedGoogle Scholar
• Rosonina E, Ip JY, Calarco JA, Bakowski MA, Emili A, McCracken S, Tucker P, Ingles CJ, Blencowe BJ. 2005. Role for PSF in mediating transcriptional activator-dependent stimulation of pre-mRNA processing in vivo. Mol Cell Biol 25:6734–6746. http://dx.doi.org/10.1128/MCB.25.15.6734-6746.2005.
   PubMed Web of Science ®Google Scholar
• Kameoka S, Duque P, Konarska MM. 2004. p54(nrb) associates with the 5′ splice site within large transcription/splicing complexes. EMBO J 23:1782–1791. http://dx.doi.org/10.1038/sj.emboj.7600187.
   PubMedGoogle Scholar
• Yadav SP, Hao H, Yang HJ, Kautzmann MA, Brooks M, Nellissery J, Klocke B, Seifert M, Swaroop A. 2014. The transcription-splicing protein NonO/p54nrb and three NonO-interacting proteins bind to distal enhancer region and augment rhodopsin expression. Hum Mol Genet 23:2132–2144. http://dx.doi.org/10.1093/hmg/ddt609.
   PubMedGoogle Scholar
• Marko M, Leichter M, Patrinou-Georgoula M, Guialis A. 2010. hnRNP M interacts with PSF and p54(nrb) and co-localizes within defined nuclear structures. Exp Cell Res 316:390–400. http://dx.doi.org/10.1016/j.yexcr.2009.10.021.
   PubMedGoogle Scholar
• Xu K, Yang L, Zhao D, Wu Y, Qi H. 2014. AKAP3 synthesis is mediated by RNA binding proteins and PKA signaling during mouse spermatogenesis. Biol Reprod 90:119. http://dx.doi.org/10.1095/biolreprod.113.116111.
   PubMedGoogle Scholar
• Horvath A, Giatzakis C, Tsang K, Greene E, Osorio P, Boikos S, Libe R, Patronas Y, Robinson-White A, Remmers E, Bertherat J, Nesterova M, Stratakis CA. 2008. A cAMP-specific phosphodiesterase (PDE8B) that is mutated in adrenal hyperplasia is expressed widely in human and mouse tissues: a novel PDE8B isoform in human adrenal cortex. Eur J Hum Genet 16:1245–1253. http://dx.doi.org/10.1038/ejhg.2008.85.
   PubMed Web of Science ®Google Scholar
• Horvath A, Mericq V, Stratakis CA. 2008. Mutation in PDE8B, a cyclic AMP-specific phosphodiesterase in adrenal hyperplasia. N Engl J Med 358:750–752. http://dx.doi.org/10.1056/NEJMc0706182.
   PubMed Web of Science ®Google Scholar
• Arnaud-Lopez L, Usala G, Ceresini G, Mitchell BD, Pilia MG, Piras MG, Sestu N, Maschio A, Busonero F, Albai G, Dei M, Lai S, Mulas A, Crisponi L, Tanaka T, Bandinelli S, Guralnik JM, Loi A, Balaci L, Sole G, Prinzis A, Mariotti S, Shuldiner AR, Cao A, Schlessinger D, Uda M, Abecasis GR, Nagaraja R, Sanna S, Naitza S. 2008. Phosphodiesterase 8B gene variants are associated with serum TSH levels and thyroid function. Am J Hum Genet 82:1270–1280. http://dx.doi.org/10.1016/j.ajhg.2008.04.019.
   PubMed Web of Science ®Google Scholar
• Horvath A, Korde L, Greene MH, Libe R, Osorio P, Faucz FR, Raffin-Sanson ML, Tsang KM, Drori-Herishanu L, Patronas Y, Remmers EF, Nikita ME, Moran J, Greene J, Nesterova M, Merino M, Bertherat J, Stratakis CA. 2009. Functional phosphodiesterase 11A mutations may modify the risk of familial and bilateral testicular germ cell tumors. Cancer Res 69:5301–5306. http://dx.doi.org/10.1158/0008-5472.CAN-09-0884.
   PubMed Web of Science ®Google Scholar
• de Oliveira SK, Hoffmeister M, Gambaryan S, Muller-Esterl W, Guimaraes JA, Smolenski AP. 2007. Phosphodiesterase 2A forms a complex with the co-chaperone XAP2 and regulates nuclear translocation of the aryl hydrocarbon receptor. J Biol Chem 282:13656–13663. http://dx.doi.org/10.1074/jbc.M610942200.
   PubMed Web of Science ®Google Scholar
• Horvath A, Giatzakis C, Robinson-White A, Boikos S, Levine E, Griffin K, Stein E, Kamvissi V, Soni P, Bossis I, de Herder W, Carney JA, Bertherat J, Gregersen PK, Remmers EF, Stratakis CA. 2006. Adrenal hyperplasia and adenomas are associated with inhibition of phosphodiesterase 11A in carriers of PDE11A sequence variants that are frequent in the population. Cancer Res 66:11571–11575. http://dx.doi.org/10.1158/0008-5472.CAN-06-2914.
   PubMed Web of Science ®Google Scholar
• Libe R, Fratticci A, Coste J, Tissier F, Horvath A, Ragazzon B, Rene-Corail F, Groussin L, Bertagna X, Raffin-Sanson ML, Stratakis CA, Bertherat J. 2008. Phosphodiesterase 11A (PDE11A) and genetic predisposition to adrenocortical tumors. Clin Cancer Res 14:4016–4024. http://dx.doi.org/10.1158/1078-0432.CCR-08-0106.
   PubMed Web of Science ®Google Scholar
• Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G. 2000. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25:25–29. http://dx.doi.org/10.1038/75556.
   PubMed Web of Science ®Google Scholar