1,858
Views
0
CrossRef citations to date
0
Altmetric
Research Paper

CFIm25 regulates human stem cell function independently of its role in mRNA alternative polyadenylation

, , , , , & ORCID Icon show all
Pages 686-702 | Received 17 Jan 2022, Accepted 20 Apr 2022, Published online: 01 May 2022

References

  • Colgan DF, Manley JL. Mechanism and regulation of mRNA polyadenylation. Genes Dev. 1997;11(21):2755–2766.
  • Cramer P. Organization and regulation of gene transcription. Nature. 2019;573(7772):45–54.
  • Shi Y, Di GDC, Taylor D, et al. Molecular architecture of the human pre-mRNA 3’ processing complex. Mol Cell. 2009;33(3):365–376.
  • Sun Y, Hamilton K, Tong L. Recent molecular insights into canonical pre-mRNA 3’-end processing. Transcription. 2020;11(2):83–96.
  • Sun Y, Zhang Y, Hamilton K, et al. Molecular basis for the recognition of the human AAUAAA polyadenylation signal. Proc Natl Acad Sci U S A. 2018;115(7):E1419–E1428.
  • Zhang Y, Sun Y, Shi Y, et al. Structural Insights into the Human Pre-mRNA 3’-End Processing Machinery. Mol Cell. 2020;77(4):800–809 e806.
  • Bentley DL. Coupling mRNA processing with transcription in time and space. Nat Rev Genet. 2014;15(3):163–175.
  • Fusby B, Kim S, Erickson B, et al. Coordination of RNA Polymerase II Pausing and 3’ End Processing Factor Recruitment with Alternative Polyadenylation. Mol Cell Biol. 2016;36(2):295–303.
  • Glover-Cutter K, Kim S, Espinosa J, et al. RNA polymerase II pauses and associates with pre-mRNA processing factors at both ends of genes. Nat Struct Mol Biol. 2008;15(1):71–78.
  • Dantonel JC, Murthy KG, Manley JL, et al. Transcription factor TFIID recruits factor CPSF for formation of 3’ end of mRNA. Nature. 1997;389(6649):399–402.
  • Ji Z, Luo W, Li W, et al. Transcriptional activity regulates alternative cleavage and polyadenylation. Mol Syst Biol. 2011;7(1):534.
  • Nagaike T, Logan C, Hotta I, et al. Transcriptional activators enhance polyadenylation of mRNA precursors. Mol Cell. 2011;41(4):409–418.
  • Rosonina E, Bakowski MA, McCracken S, et al. Transcriptional activators control splicing and 3’-end cleavage levels. J Biol Chem. 2003;278(44):43034–43040.
  • Davidson L, Muniz L, West S. 3’ end formation of pre-mRNA and phosphorylation of Ser2 on the RNA polymerase II CTD are reciprocally coupled in human cells. Genes Dev. 2014;28(4):342–356.
  • Licatalosi DD, Geiger G, Minet M, et al. Functional interaction of yeast pre-mRNA 3’ end processing factors with RNA polymerase II. Mol Cell. 2002;9(5):1101–1111.
  • Al Husini N, Kudla P, Ansari A. A role for CF1A 3’ end processing complex in promoter-associated transcription. PLoS Genet. 2013;9(8):e1003722.
  • Allepuz-Fuster P, O’Brien MJ, Gonzalez-Polo N, et al. RNA polymerase II plays an active role in the formation of gene loops through the Rpb4 subunit. Nucleic Acids Res. 2019;47(17):8975–8987.
  • Ansari A, Hampsey M. A role for the CPF 3’-end processing machinery in RNAP II-dependent gene looping. Genes Dev. 2005;19(24):2969–2978.
  • El Kaderi B, Medler S, Raghunayakula S, et al. Gene looping is conferred by activator-dependent interaction of transcription initiation and termination machineries. J Biol Chem. 2009;284(37):25015–25025.
  • Mapendano CK, Lykke-Andersen S, Kjems J, et al. Crosstalk between mRNA 3 ‘ End Processing and Transcription Initiation. Mol Cell. 2010;40(3):410–422.
  • Kaida D, Berg MG, Younis I, et al. U1 snRNP protects pre-mRNAs from premature cleavage and polyadenylation. Nature. 2010;468(7324):664–668.
  • Ran Y, Deng Y, Yao C. U1 snRNP telescripting: molecular mechanisms and beyond. RNA Biol. 2021;18(11):1512–1523.
  • Venters CC, Oh JM, Di C, et al. U1 snRNP Telescripting: suppression of Premature Transcription Termination in Introns as a New Layer of Gene Regulation. Cold Spring Harb Perspect Biol. 2019;11(2):a032235.
  • Cavallaro M, Walsh MD, Jones M, et al. 3 (‘)-5 (‘) crosstalk contributes to transcriptional bursting. Genome Biol. 2021;22(1):56.
  • Ruegsegger U, Beyer K, Keller W. Purification and characterization of human cleavage factor Im involved in the 3’ end processing of messenger RNA precursors. J Biol Chem. 1996;271(11):6107–6113.
  • Ruegsegger U, Blank D, Keller W. Human pre-mRNA cleavage factor Im is related to spliceosomal SR proteins and can be reconstituted in vitro from recombinant subunits. Mol Cell. 1998;1(2):243–253.
  • Kim S, Yamamoto J, Chen Y, et al. Evidence that cleavage factor Im is a heterotetrameric protein complex controlling alternative polyadenylation. Genes Cells. 2010;15(9):1003–1013.
  • Kubo T, Wada T, Yamaguchi Y, et al. Knock-down of 25 kDa subunit of cleavage factor Im in Hela cells alters alternative polyadenylation within 3’-UTRs. Nucleic Acids Res. 2006;34(21):6264–6271.
  • Martin G, Gruber AR, Keller W, et al. Genome-wide analysis of pre-mRNA 3’ end processing reveals a decisive role of human cleavage factor I in the regulation of 3’ UTR length. Cell Rep. 2012;1(6):753–763.
  • Masamha CP, Xia Z, Yang J, et al. CFIm25 links alternative polyadenylation to glioblastoma tumour suppression. Nature. 2014;510(7505):412–416.
  • Zhu Y, Wang X, Forouzmand E, et al. Molecular Mechanisms for CFIm-Mediated Regulation of mRNA Alternative Polyadenylation. Mol Cell. 2018;69(1):62–74 e64.
  • Calvo O, Manley JL. Strange bedfellows: polyadenylation factors at the promoter. Genes Dev. 2003;17(11):1321–1327.
  • Garrido-Lecca A, Saldi T, Blumenthal T. Localization of RNAPII and 3′ end formation factor CstF subunits on C. elegans genes and operons. Transcription. 2016;7(3):96–110.
  • Katahira J, Okuzaki D, Inoue H, et al. Human TREX component Thoc5 affects alternative polyadenylation site choice by recruiting mammalian cleavage factor I. Nucleic Acids Res. 2013;41(14):7060–7072.
  • Tellier M, Hardy JG, Norbury CJ, et al. Effect of CFIm25 knockout on RNA polymerase II transcription. BMC Res Notes. 2018;11(1):894.
  • Tellier M, Hardy JG, Norbury CJ, et al. Effect of CFIm68 knockdown on RNA polymerase II transcription. BMC Res Notes. 2019;12(1):554.
  • Alcott CE, Yalamanchili HK, Ji P, et al. Partial loss of CFIm25 causes learning deficits and aberrant neuronal alternative polyadenylation. Elife. 2020;9. DOI:10.7554/eLife.50895.
  • Sommerkamp P, Altamura S, Renders S, et al. Differential Alternative Polyadenylation Landscapes Mediate Hematopoietic Stem Cell Activation and Regulate Glutamine Metabolism. Cell Stem Cell. 2020;26(5):722–738 e727.
  • Tan S, Li H, Zhang W, et al. NUDT21 negatively regulates PSMB2 and CXXC5 by alternative polyadenylation and contributes to hepatocellular carcinoma suppression. Oncogene. 2018;37(35):4887–4900.
  • Weng T, Huang J, Wagner EJ, et al. Downregulation of CFIm25 amplifies dermal fibrosis through alternative polyadenylation. J Exp Med. 2020;217(2). DOI:10.1084/jem.20181384.
  • Brumbaugh J, Di Stefano B, Wang X, et al. Nudt21 Controls Cell Fate by Connecting Alternative Polyadenylation to Chromatin Signaling. Cell. 2018;172(1–2):106–120 e121.
  • Chu Y, Elrod N, Wang C, et al. Nudt21 regulates the alternative polyadenylation of Pak1 and is predictive in the prognosis of glioblastoma patients. Oncogene. 2019;38(21):4154–4168.
  • Najaf Abadi MH J, Shafabakhsh R, Asemi Z, et al. CFIm25 and alternative polyadenylation: conflicting roles in cancer. Cancer Lett. 2019;459:112–121.
  • Gennarino VA, Alcott CE, Chen CA, et al. NUDT21-spanning CNVs lead to neuropsychiatric disease and altered MeCP2 abundance via alternative polyadenylation. Elife. 2015;4. DOI:10.7554/eLife.10782.
  • Huang J, Weng T, Ko J, et al. Suppression of cleavage factor Im 25 promotes the proliferation of lung cancer cells through alternative polyadenylation. Biochem Biophys Res Commun. 2018;503(2):856–862.
  • Weng T, Ko J, Masamha CP, et al. Cleavage factor 25 deregulation contributes to pulmonary fibrosis through alternative polyadenylation. J Clin Invest. 2019;129(5):1984–1999.
  • Zhou Z, Qu J, He L, et al. Stiff matrix instigates type I collagen biogenesis by mammalian cleavage factor I complex-mediated alternative polyadenylation. JCI insight. 2020;5(3): e133972.DOI:10.1172/jci.insight.133972.
  • Xie Y, Wang D, Lan F, et al. An episomal vector-based CRISPR/Cas9 system for highly efficient gene knockout in human pluripotent stem cells. Sci Rep. 2017;7(1):2320.
  • So BR, Di C, Cai Z, et al. A Complex of U1 snRNP with Cleavage and Polyadenylation Factors Controls Telescripting, Regulating mRNA Transcription in Human Cells. Mol Cell. 2019;76(4):590–599 e594.
  • Rowton M, Guzzetta A, Rydeen AB, et al. Control of cardiomyocyte differentiation timing by intercellular signaling pathways. Semin Cell Dev Biol. 2021;118:94–106.
  • Ruan H, Liao Y, Ren Z, et al. Single-cell reconstruction of differentiation trajectory reveals a critical role of ETS1 in human cardiac lineage commitment. BMC Biol. 2019;17(1):89.
  • Lackford B, Yao C, Charles GM, et al. Fip1 regulates mRNA alternative polyadenylation to promote stem cell self-renewal. EMBO J. 2014;33(8):878–889.
  • Shi J, Deng Y, Huang S, et al. Suboptimal RNA-RNA interaction limits U1 snRNP inhibition of canonical mRNA 3’ processing. RNA Biol. 2019;16(10):1448–1460.
  • Yao C, Biesinger J, Wan J, et al. Transcriptome-wide analyses of CstF64-RNA interactions in global regulation of mRNA alternative polyadenylation. Proc Natl Acad Sci U S A. 2012;109(46):18773–18778.
  • Masui S, Ohtsuka S, Yagi R, et al. Rex1/Zfp42 is dispensable for pluripotency in mouse ES cells. BMC Dev Biol. 2008;8(1). DOI:10.1186/1471-213X-8-45
  • Son MY, Choi H, Han YM, et al. Unveiling the critical role of REX1 in the regulation of human stem cell pluripotency. Stem Cells. 2013;31(11):2374–2387.
  • Zhang S, Deng T, Tang W, et al. Epigenetic regulation of REX1 expression and chromatin binding specificity by HMGNs. Nucleic Acids Res. 2019;47(9):4449–4461.
  • Nojima T, Gomes T, Grosso ARF, et al. Mammalian NET-Seq Reveals Genome-wide Nascent Transcription Coupled to RNA Processing. Cell. 2015;161(3):526–540.
  • Hsin JP, Manley JL. The RNA polymerase II CTD coordinates transcription and RNA processing. Genes Dev. 2012;26(19):2119–2137.
  • Lyons DE, McMahon S, Ott M. A combinatorial view of old and new RNA polymerase II modifications. Transcription. 2020;11(2):66–82.
  • Tellier M, Zaborowska J, Caizzi L, et al. CDK12 globally stimulates RNA polymerase II transcription elongation and carboxyl-terminal domain phosphorylation. Nucleic Acids Res. 2020;48(14):7712–7727.
  • Routh A, Ji P, Jaworski E, et al. Poly(A)-ClickSeq: click-chemistry for next-generation 3-end sequencing without RNA enrichment or fragmentation. Nucleic Acids Res. 2017;45(12):e112.
  • Caizzi L, Monteiro-Martins S, Schwalb B, et al. Efficient RNA polymerase II pause release requires U2 snRNP function. Mol Cell. 2021;81(9):1920–1934 e1929.
  • Lin S, Coutinho-Mansfield G, Wang D, et al. The splicing factor SC35 has an active role in transcriptional elongation. Nat Struct Mol Biol. 2008;15(8):819–826.
  • Xie Y, Zheng M, Chu X, et al. Paf1 and Ctr9 subcomplex formation is essential for Paf1 complex assembly and functional regulation. Nat Commun. 2018;9(1):3795.
  • Chen YF, Li YJ, Chou CH, et al. Control of matrix stiffness promotes endodermal lineage specification by regulating SMAD2/3 via lncRNA LINC00458. Sci Adv. 2020;6(6):eaay0264.
  • Shan Z, Shakoori A, Bodaghi S, et al. TUSC1, a putative tumor suppressor gene, reduces tumor cell growth in vitro and tumor growth in vivo. PLoS One. 2013;8(6):e66114.
  • Fu X, Wu S, Li B, et al. Functions of p53 in pluripotent stem cells. Protein Cell. 2020;11(1):71–78.
  • Langer LF, Ward JM, Archer TK. Tumor suppressor SMARCB1 suppresses super-enhancers to govern hESC lineage determination. Elife. 2019;8. DOI:10.7554/eLife.45672
  • Slobodin B, Bahat A, Sehrawat U, et al. Transcription Dynamics Regulate Poly(A) Tails and Expression of the RNA Degradation Machinery to Balance mRNA Levels. Mol Cell. 2020;78(3):434–444 e435.
  • Shao W, Zeitlinger J. Paused RNA polymerase II inhibits new transcriptional initiation. Nat Genet. 2017;49(7):1045–1051.
  • Gao CC, Xu QQ, Xiao FJ, et al. NUDT21 suppresses the growth of small cell lung cancer by modulating GLS1 splicing. Biochem Biophys Res Commun. 2020;526(2):431–438.
  • Scarborough AM, Flaherty JN, Hunter OV, et al. SAM homeostasis is regulated by CFIm-mediated splicing of MAT2A. Elife. 2021;10. DOI:10.7554/eLife.64930
  • Huang C, Shi J, Guo Y, et al. A snoRNA modulates mRNA 3’ end processing and regulates the expression of a subset of mRNAs. Nucleic Acids Res. 2017;45(15):8647–8660.
  • Paulsen MT, Veloso A, Prasad J, et al. Use of Bru-Seq and BruChase-Seq for genome-wide assessment of the synthesis and stability of RNA. Methods. 2014;67(1):45–54.
  • Roberts TC, Hart JR, Kaikkonen MU, et al. Quantification of nascent transcription by bromouridine immunocapture nuclear run-on RT-qPCR. Nat Protoc. 2015;10(8):1198–1211.
  • El Kaderi B, Medler S, Ansari A. Curr Protoc Cell Biol; 2012. Chapter 22: Unit22.15,Analysis of interactions between genomic loci through Chromosome Conformation Capture (3C); DOI:10.1002/0471143030.cb2215s56.