281
Views
6
CrossRef citations to date
0
Altmetric
Research Article

Multilevel Differential Control of Hormone Gene Expression Programs by hnRNP L and LL in Pituitary Cells

, , , , , , , & show all
Article: e00651-17 | Received 19 Dec 2017, Accepted 22 Mar 2018, Published online: 03 Mar 2023

REFERENCES

  • Dreyfuss G, Kim VN, Kataoka N. 2002. Messenger-RNA-binding proteins and the messages they carry. Nat Rev Mol Cell Biol 3:195–205. https://doi.org/10.1038/nrm760.
  • Dreyfuss G, Matunis MJ, Pinol-Roma S, Burd CG. 1993. hnRNP proteins and the biogenesis of mRNA. Annu Rev Biochem 62:289–321. https://doi.org/10.1146/annurev.bi.62.070193.001445.
  • Busch A, Hertel KJ. 2012. Evolution of SR protein and hnRNP splicing regulatory factors. Wiley Interdiscip Rev RNA 3:1–12. https://doi.org/10.1002/wrna.100.
  • Martinez-Contreras R, Cloutier P, Shkreta L, Fisette JF, Revil T, Chabot B. 2007. hnRNP proteins and splicing control. Adv Exp Med Biol 623:123–147.
  • Han SP, Tang YH, Smith R. 2010. Functional diversity of the hnRNPs: past, present and perspectives. Biochem J 430:379–392. https://doi.org/10.1042/BJ20100396.
  • Pagani F, Baralle FE. 2004. Genomic variants in exons and introns: identifying the splicing spoilers. Nat Rev Genet 5:389–396. https://doi.org/10.1038/nrg1327.
  • Zarnack K, Konig J, Tajnik M, Martincorena I, Eustermann S, Stevant I, Reyes A, Anders S, Luscombe NM, Ule J. 2013. Direct competition between hnRNP C and U2AF65 protects the transcriptome from the exonization of Alu elements. Cell 152:453–466. https://doi.org/10.1016/j.cell.2012.12.023.
  • Ling JP, Chhabra R, Merran JD, Schaughency PM, Wheelan SJ, Corden JL, Wong PC. 2016. PTBP1 and PTBP2 repress nonconserved cryptic exons. Cell Rep 17:104–113. https://doi.org/10.1016/j.celrep.2016.08.071.
  • Ling JP, Pletnikova O, Troncoso JC, Wong PC. 2015. TDP-43 repression of nonconserved cryptic exons is compromised in ALS-FTD. Science 349:650–655. https://doi.org/10.1126/science.aab0983.
  • Clower CV, Chatterjee D, Wang Z, Cantley LC, Vander Heiden MG, Krainer AR. 2010. The alternative splicing repressors hnRNP A1/A2 and PTB influence pyruvate kinase isoform expression and cell metabolism. Proc Natl Acad Sci U S A 107:1894–1899. https://doi.org/10.1073/pnas.0914845107.
  • Garneau D, Revil T, Fisette JF, Chabot B. 2005. Heterogeneous nuclear ribonucleoprotein F/H proteins modulate the alternative splicing of the apoptotic mediator Bcl-x. J Biol Chem 280:22641–22650. https://doi.org/10.1074/jbc.M501070200.
  • Makeyev EV, Zhang J, Carrasco MA, Maniatis T. 2007. The microRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol Cell 27:435–448. https://doi.org/10.1016/j.molcel.2007.07.015.
  • Boutz PL, Stoilov P, Li Q, Lin CH, Chawla G, Ostrow K, Shiue L, Ares M, Jr, Black DL. 2007. A post-transcriptional regulatory switch in polypyrimidine tract-binding proteins reprograms alternative splicing in developing neurons. Genes Dev 21:1636–1652. https://doi.org/10.1101/gad.1558107.
  • Woolaway K, Asai K, Emili A, Cochrane A. 2007. hnRNP E1 and E2 have distinct roles in modulating HIV-1 gene expression. Retrovirology 4:28. https://doi.org/10.1186/1742-4690-4-28.
  • Xie J. 2014. Differential evolution of signal-responsive RNA elements and upstream factors that control alternative splicing. Cell Mol Life Sci 71:4347–4360. https://doi.org/10.1007/s00018-014-1688-y.
  • Hui J, Hung LH, Heiner M, Schreiner S, Neumuller N, Reither G, Haas SA, Bindereif A. 2005. Intronic CA-repeat and CA-rich elements: a new class of regulators of mammalian alternative splicing. EMBO J 24:1988–1998. https://doi.org/10.1038/sj.emboj.7600677.
  • Smith SA, Ray D, Cook KB, Mallory MJ, Hughes TR, Lynch KW. 2013. Paralogs hnRNP L and hnRNP LL exhibit overlapping but distinct RNA binding constraints. PLoS One 8:e80701. https://doi.org/10.1371/journal.pone.0080701.
  • Oberdoerffer S, Moita LF, Neems D, Freitas RP, Hacohen N, Rao A. 2008. Regulation of CD45 alternative splicing by heterogeneous ribonucleoprotein, hnRNP LL. Science 321:686–691. https://doi.org/10.1126/science.1157610.
  • Chang X, Li B, Rao A. 2015. RNA-binding protein hnRNPLL regulates mRNA splicing and stability during B-cell to plasma-cell differentiation. Proc Natl Acad Sci U S A 112:E1888–E1897. https://doi.org/10.1073/pnas.1422490112.
  • Chang X. 2016. RNA-binding protein hnRNPLL as a critical regulator of lymphocyte homeostasis and differentiation. Wiley Interdiscip Rev RNA 7:295–302. https://doi.org/10.1002/wrna.1335.
  • Hung LH, Heiner M, Hui J, Schreiner S, Benes V, Bindereif A. 2008. Diverse roles of hnRNP L in mammalian mRNA processing: a combined microarray and RNAi analysis. RNA 14:284–296. https://doi.org/10.1261/rna.725208.
  • Shankarling G, Cole BS, Mallory MJ, Lynch KW. 2014. Transcriptome-wide RNA interaction profiling reveals physical and functional targets of hnRNP L in human T cells. Mol Cell Biol 34:71–83. https://doi.org/10.1128/MCB.00740-13.
  • Huang Y, Li W, Yao X, Lin QJ, Yin JW, Liang Y, Heiner M, Tian B, Hui J, Wang G. 2012. Mediator complex regulates alternative mRNA processing via the MED23 subunit. Mol Cell 45:459–469. https://doi.org/10.1016/j.molcel.2011.12.022.
  • Gaudreau MC, Grapton D, Helness A, Vadnais C, Fraszczak J, Shooshtarizadeh P, Wilhelm B, Robert F, Heyd F, Moroy T. 2016. Heterogeneous nuclear ribonucleoprotein L is required for the survival and functional integrity of murine hematopoietic stem cells. Sci Rep 6:27379. https://doi.org/10.1038/srep27379.
  • Gaudreau MC, Heyd F, Bastien R, Wilhelm B, Moroy T. 2012. Alternative splicing controlled by heterogeneous nuclear ribonucleoprotein L regulates development, proliferation, migration of thymic pre-T cells. J Immunol 188:5377–5388. https://doi.org/10.4049/jimmunol.1103142.
  • Loh TJ, Cho S, Moon H, Jang HN, Williams DR, Jung DW, Kim IC, Ghigna C, Biamonti G, Zheng X, Shen H. 2015. hnRNP L inhibits CD44 V10 exon splicing through interacting with its upstream intron. Biochim Biophys Acta 1 849:743–750. https://doi.org/10.1016/j.bbagrm.2015.01.004.
  • Rossbach O, Hung LH, Khrameeva E, Schreiner S, Konig J, Curk T, Zupan B, Ule J, Gelfand MS, Bindereif A. 2014. Crosslinking-immunoprecipitation (iCLIP) analysis reveals global regulatory roles of hnRNP L. RNA Biol 11:146–155. https://doi.org/10.4161/rna.27991.
  • Yu J, Hai Y, Liu G, Fang T, Kung SK, Xie J. 2009. The heterogeneous nuclear ribonucleoprotein L is an essential component in the Ca2+/calmodulin-dependent protein kinase IV-regulated alternative splicing through cytidine-adenosine repeats. J Biol Chem 284:1505–1513. https://doi.org/10.1074/jbc.M805113200.
  • Liu G, Razanau A, Hai Y, Yu J, Sohail M, Lobo VG, Chu J, Kung SK, Xie J. 2012. A conserved serine of heterogeneous nuclear ribonucleoprotein L (hnRNP L) mediates depolarization-regulated alternative splicing of potassium channels. J Biol Chem 287:22709–22716. https://doi.org/10.1074/jbc.M112.357343.
  • Liu G, Lei L, Yu J, Kung S, Xie J. 2014. Refinement of the spectra of exon usage by combined effects of extracellular stimulus and intracellular factors. Biochim Biophys Acta 1 839:537–545. https://doi.org/10.1016/j.bbagrm.2014.05.002.
  • Tashjian AH, Jr, Bancroft FC, Levine L. 1970. Production of both prolactin and growth hormone by clonal strains of rat pituitary tumor cells. Differential effects of hydrocortisone and tissue extracts. J Cell Biol 47:61–70.
  • Simmons DM, Voss JW, Ingraham HA, Holloway JM, Broide RS, Rosenfeld MG, Swanson LW. 1990. Pituitary cell phenotypes involve cell-specific Pit-1 mRNA translation and synergistic interactions with other classes of transcription factors. Genes Dev 4:695–711. https://doi.org/10.1101/gad.4.5.695.
  • Mullis PE. 2010. Genetics of isolated growth hormone deficiency. J Clin Res Pediatr Endocrinol 2:52–62. https://doi.org/10.4274/jcrpe.v2i2.52.
  • Serri O, Chik CL, Ur E, Ezzat S. 2003. Diagnosis and management of hyperprolactinemia. CMAJ 169:575–581.
  • Zargar AH, Masoodi SR, Laway BA, Shah NA, Salahudin M. 1997. Familial puerperal alactogenesis: possibility of a genetically transmitted isolated prolactin deficiency. Br J Obstet Gynaecol 104:629–631. https://doi.org/10.1111/j.1471-0528.1997.tb11548.x.
  • Goffin V, Binart N, Touraine P, Kelly PA. 2002. Prolactin: the new biology of an old hormone. Annu Rev Physiol 64:47–67. https://doi.org/10.1146/annurev.physiol.64.081501.131049.
  • Anders S, Reyes A, Huber W. 2012. Detecting differential usage of exons from RNA-seq data. Genome Res 22:2008–2017. https://doi.org/10.1101/gr.133744.111.
  • Yeo G, Burge CB. 2004. Maximum entropy modeling of short sequence motifs with applications to RNA splicing signals. J Comput Biol 11:377–394. https://doi.org/10.1089/1066527041410418.
  • Karolchik D, Barber GP, Casper J, Clawson H, Cline MS, Diekhans M, Dreszer TR, Fujita PA, Guruvadoo L, Haeussler M, Harte RA, Heitner S, Hinrichs AS, Learned K, Lee BT, Li CH, Raney BJ, Rhead B, Rosenbloom KR, Sloan CA, Speir ML, Zweig AS, Haussler D, Kuhn RM, Kent WJ. 2014. The UCSC Genome Browser database: 2014 update. Nucleic Acids Res 42:D764–D770. https://doi.org/10.1093/nar/gkt1168.
  • Broutin I, Jomain JB, Tallet E, van Agthoven J, Raynal B, Hoos S, Kragelund BB, Kelly PA, Ducruix A, England P, Goffin V. 2010. Crystal structure of an affinity-matured prolactin complexed to its dimerized receptor reveals the topology of hormone binding site 2. J Biol Chem 285:8422–8433. https://doi.org/10.1074/jbc.M109.089128.
  • Biasini M, Bienert S, Waterhouse A, Arnold K, Studer G, Schmidt T, Kiefer F, Gallo Cassarino T, Bertoni M, Bordoli L, Schwede T. 2014. SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res 42:W252–W258. https://doi.org/10.1093/nar/gku340.
  • Nagy E, Maquat LE. 1998. A rule for termination-codon position within intron-containing genes: when nonsense affects RNA abundance. Trends Biochem Sci 23:198–199. https://doi.org/10.1016/S0968-0004(98)01208-0.
  • Isken O, Maquat LE. 2007. Quality control of eukaryotic mRNA: safeguarding cells from abnormal mRNA function. Genes Dev 21:1833–1856. https://doi.org/10.1101/gad.1566807.
  • Schoenberg DR, Maquat LE. 2012. Regulation of cytoplasmic mRNA decay. Nat Rev Genet 13:246–259. https://doi.org/10.1038/nrg3160.
  • Dominski Z, Kole R. 1991. Selection of splice sites in pre-mRNAs with short internal exons. Mol Cell Biol 11:6075–6083. https://doi.org/10.1128/MCB.11.12.6075.
  • Xie JY, Black DL. 2001. A CaMK IV responsive RNA element mediates depolarization-induced alternative splicing of ion channels. Nature 410:936–939. https://doi.org/10.1038/35073593.
  • Berg MG, Singh LN, Younis I, Liu Q, Pinto AM, Kaida D, Zhang Z, Cho S, Sherrill-Mix S, Wan L, Dreyfuss G. 2012. U1 snRNP determines mRNA length and regulates isoform expression. Cell 150:53–64. https://doi.org/10.1016/j.cell.2012.05.029.
  • Flavell SW, Kim TK, Gray JM, Harmin DA, Hemberg M, Hong EJ, Markenscoff-Papadimitriou E, Bear DM, Greenberg ME. 2008. Genome-wide analysis of MEF2 transcriptional program reveals synaptic target genes and neuronal activity-dependent polyadenylation site selection. Neuron 60:1022–1038. https://doi.org/10.1016/j.neuron.2008.11.029.
  • Mayr C, Bartel DP. 2009. Widespread shortening of 3′UTRs by alternative cleavage and polyadenylation activates oncogenes in cancer cells. Cell 138:673–684. https://doi.org/10.1016/j.cell.2009.06.016.
  • Sandberg R, Neilson JR, Sarma A, Sharp PA, Burge CB. 2008. Proliferating cells express mRNAs with shortened 3′ untranslated regions and fewer microRNA target sites. Science 320:1643–1647. https://doi.org/10.1126/science.1155390.
  • Ishigaki Y, Li X, Serin G, Maquat LE. 2001. Evidence for a pioneer round of mRNA translation: mRNAs subject to nonsense-mediated decay in mammalian cells are bound by CBP80 and CBP20. Cell 106:607–617. https://doi.org/10.1016/S0092-8674(01)00475-5.
  • Fujishige K, Kotera J, Michibata H, Yuasa K, Takebayashi S, Okumura K, Omori K. 1999. Cloning and characterization of a novel human phosphodiesterase that hydrolyzes both cAMP and cGMP (PDE10A). J Biol Chem 274:18438–18445. https://doi.org/10.1074/jbc.274.26.18438.
  • Tisdale EJ. 2000. Rab2 requires PKC iota/lambda to recruit beta-COP for vesicle formation. Traffic 1:702–712. https://doi.org/10.1034/j.1600-0854.2000.010903.x.
  • Kretschmannova K, Gonzalez-Iglesias AE, Tomic M, Stojilkovic SS. 2006. Dependence of hyperpolarisation-activated cyclic nucleotide-gated channel activity on basal cyclic adenosine monophosphate production in spontaneously firing GH3 cells. J Neuroendocrinol 18:484–493. https://doi.org/10.1111/j.1365-2826.2006.01438.x.
  • Calejo AI, Jorgacevski J, Rituper B, Gucek A, Pereira PM, Santos MA, Potokar M, Vardjan N, Kreft M, Goncalves PP, Zorec R. 2014. Hyperpolarization-activated cyclic nucleotide-gated channels and cAMP-dependent modulation of exocytosis in cultured rat lactotrophs. J Neurosci 34:15638–15647. https://doi.org/10.1523/JNEUROSCI.5290-13.2014.
  • Kucka M, Bjelobaba I, Tomic M, Stojilkovic SS. 2013. The role of cyclic nucleotides in pituitary lactotroph functions. Front Endocrinol (Lausanne) 4:122.
  • Rahman MA, Masuda A, Ohe K, Ito M, Hutchinson DO, Mayeda A, Engel AG, Ohno K. 2013. hnRNP L and hnRNP LL antagonistically modulate PTB-mediated splicing suppression of CHRNA1 pre-mRNA. Sci Rep 3:2931. https://doi.org/10.1038/srep02931.
  • Rossbach O, Hung LH, Schreiner S, Grishina I, Heiner M, Hui J, Bindereif A. 2009. Auto- and cross-regulation of the hnRNP L proteins by alternative splicing. Mol Cell Biol 29:1442–1451. https://doi.org/10.1128/MCB.01689-08.
  • Hui J, Reither G, Bindereif A. 2003. Novel functional role of CA repeats and hnRNP L in RNA stability. RNA 9:931–936. https://doi.org/10.1261/rna.5660803.
  • Hahm B, Cho OH, Kim JE, Kim YK, Kim JH, Oh YL, Jang SK. 1998. Polypyrimidine tract-binding protein interacts with hnRNP L. FEBS Lett 425:401–406. https://doi.org/10.1016/S0014-5793(98)00269-5.
  • Burd CG, Dreyfuss G. 1994. RNA binding specificity of hnRNP A1: significance of hnRNP A1 high-affinity binding sites in pre-mRNA splicing. EMBO J 13:1197–1204.
  • Geissler R, Simkin A, Floss D, Patel R, Fogarty EA, Scheller J, Grimson A. 2016. A widespread sequence-specific mRNA decay pathway mediated by hnRNPs A1 and A2/B1. Genes Dev 30:1070–1085. https://doi.org/10.1101/gad.277392.116.
  • Cho V, Mei Y, Sanny A, Chan S, Enders A, Bertram EM, Tan A, Goodnow CC, Andrews TD. 2014. The RNA-binding protein hnRNPLL induces a T cell alternative splicing program delineated by differential intron retention in polyadenylated RNA. Genome Biol 15:R26. https://doi.org/10.1186/gb-2014-15-1-r26.
  • Pastor T, Pagani F. 2011. Interaction of hnRNPA1/A2 and DAZAP1 with an Alu-derived intronic splicing enhancer regulates ATM aberrant splicing. PLoS One 6:e23349. https://doi.org/10.1371/journal.pone.0023349.
  • Sohail M, Xie J. 2015. Evolutionary emergence of a novel splice variant with an opposite effect on the cell cycle. Mol Cell Biol 35:2203–2214. https://doi.org/10.1128/MCB.00190-15.
  • Sohail M, Cao W, Mahmood N, Myschyshyn M, Hong SP, Xie J. 2014. Evolutionarily emerged G tracts between the polypyrimidine tract and 3′ AG are splicing silencers enriched in genes involved in cancer. BMC Genomics 15:1143. https://doi.org/10.1186/1471-2164-15-1143.
  • Yeo G, Hoon S, Venkatesh B, Burge CB. 2004. Variation in sequence and organization of splicing regulatory elements in vertebrate genes. Proc Natl Acad Sci U S A 101:15700–15705. https://doi.org/10.1073/pnas.0404901101.
  • Chabot B, Shkreta L. 2016. Defective control of pre-messenger RNA splicing in human disease. J Cell Biol 212:13–27. https://doi.org/10.1083/jcb.201510032.
  • Zhang J, Manley JL. 2013. Misregulation of pre-mRNA alternative splicing in cancer. Cancer Discov 3:1228–1237. https://doi.org/10.1158/2159-8290.CD-13-0253.
  • Feng D, Xie J. 2013. Aberrant splicing in neurological diseases. Wiley Interdiscip Rev RNA 4:631–649. https://doi.org/10.1002/wrna.1184.
  • Fisher CL, Pei GK. 1997. Modification of a PCR-based site-directed mutagenesis method. Biotechniques 23:570–574.
  • Ma S, Liu G, Sun Y, Xie J. 2007. Relocalization of the polypyrimidine tract-binding protein during PKA-induced neurite growth. Biochim Biophys Acta 1 773:912–923. https://doi.org/10.1016/j.bbamcr.2007.02.006.
  • Xie J, Lee JA, Kress TL, Mowry KL, Black DL. 2003. Protein kinase A phosphorylation modulates transport of the polypyrimidine tract-binding protein. Proc Natl Acad Sci U S A 100:8776–8781. https://doi.org/10.1073/pnas.1432696100.
  • Robinson MD, McCarthy DJ, Smyth GK. 2010. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140. https://doi.org/10.1093/bioinformatics/btp616.
  • McCarthy DJ, Chen Y, Smyth GK. 2012. Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucleic Acids Res 40:4288–4297. https://doi.org/10.1093/nar/gks042.
  • Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP. 2011. Integrative genomics viewer. Nat Biotechnol 29:24–26. https://doi.org/10.1038/nbt.1754.
  • Colgan DF, Manley JL. 1997. Mechanism and regulation of mRNA polyadenylation. Genes Dev 11:2755–2766. https://doi.org/10.1101/gad.11.21.2755.
  • Bhat BM, Wold WS. 1985. ATTAAA as well as downstream sequences are required for RNA 3′-end formation in the E3 complex transcription unit of adenovirus. Mol Cell Biol 5:3183–3193. https://doi.org/10.1128/MCB.5.11.3183.
  • Huang DW, Sherman BT, Lempicki RA. 2009. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4:44–57.
  • Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675. https://doi.org/10.1038/nmeth.2089.
  • Cao W, Razanau A, Feng D, Lobo VG, Xie J. 2012. Control of alternative splicing by forskolin through hnRNP K during neuronal differentiation. Nucleic Acids Res 40:8059–8071. https://doi.org/10.1093/nar/gks504.

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.