The Prolyl Isomerase Pin1 Targets Stem-Loop Binding Protein (SLBP) To Dissociate the SLBP-Histone mRNA Complex Linking Histone mRNA Decay with SLBP Ubiquitination

REFERENCES

• Albert A, Lavoie S, Vincent M. 1999. A hyperphosphorylated form of RNA polymerase II is the major interphase antigen of the phosphoprotein antibody MPM-2 and interacts with the peptidyl-prolyl isomerase Pin1. J. Cell Sci. 112(Part 15):2493–2500.
   PubMedGoogle Scholar
• Alterman RB, et al. 1984. Cell cycle regulation of mouse H3 histone mRNA metabolism. Mol. Cell. Biol. 4:123–132.
   PubMed Web of Science ®Google Scholar
• Borchers CH, et al. 2006. Combined top-down and bottom-up proteomics identifies a phosphorylation site in stem-loop-binding proteins that contributes to high-affinity RNA binding. Proc. Natl. Acad. Sci. U. S. A. 103:3094–3099.
   PubMed Web of Science ®Google Scholar
• Crenshaw DG, Yang J, Means AR, Kornbluth S. 1998. The mitotic peptidyl-prolyl isomerase, Pin1, interacts with Cdc25 and Plx1. EMBO J. 17:1315–1327.
   PubMedGoogle Scholar
• Dimitrova DS, Berezney R. 2002. The spatio-temporal organization of DNA replication sites is identical in primary, immortalized and transformed mammalian cells. J. Cell Sci. 115:4037–4051.
   PubMed Web of Science ®Google Scholar
• Dominski Z, Erkmann JA, Greenland JA, Marzluff WF. 2001. Mutations in the RNA binding domain of stem-loop binding protein define separable requirements for RNA binding and for histone pre-mRNA processing. Mol. Cell. Biol. 21:2008–2017.
   PubMedGoogle Scholar
• Dominski Z, et al. 2002. 3′ end processing of Drosophila melanogaster histone pre-mRNAs: requirement for phosphorylated Drosophila stem-loop binding protein and coevolution of the histone pre-mRNA processing system. Mol. Cell. Biol. 22:6648–6660.
   PubMed Web of Science ®Google Scholar
• Dougherty MK, et al. 2005. Regulation of Raf-1 by direct feedback phosphorylation. Mol. Cell 17:215–224.
   PubMed Web of Science ®Google Scholar
• Erkmann JA, et al. 2005. Nuclear import of the stem-loop binding protein and localization during the cell cycle. Mol. Biol. Cell 16:2960–2971.
   PubMed Web of Science ®Google Scholar
• Esnault S, Shen ZJ, Whitesel E, Malter JS. 2006. The peptidyl-prolyl isomerase Pin1 regulates granulocyte-macrophage colony-stimulating factor mRNA stability in T lymphocytes. J. Immunol. 177:6999–7006.
   PubMedGoogle Scholar
• Finn G, Lu KP. 2008. Phosphorylation-specific prolyl isomerase Pin1 as a new diagnostic and therapeutic target for cancer. Curr. Cancer Drug Targets 8:223–229.
   PubMedGoogle Scholar
• Gnad F, Gunawardena J, Mann M. 2011. PHOSIDA 2011: the posttranslational modification database. Nucleic Acids Res. 39:D253–D260.
   PubMed Web of Science ®Google Scholar
• Greenwood AI, et al. 2011. Complete determination of the Pin1 catalytic domain thermodynamic cycle by NMR lineshape analysis. J. Biomol. NMR 51:21–34.
   PubMedGoogle Scholar
• Haupt Y. 2004. p53 regulation: a family affair. Cell Cycle 3:884–885.
   PubMedGoogle Scholar
• Heintz N, Sive HL, Roeder RG. 1983. Regulation of human histone gene expression: kinetics of accumulation and changes in the rate of synthesis and in the half-lives of individual histone mRNAs during the HeLa cell cycle. Mol. Cell. Biol. 3:539–550.
   PubMed Web of Science ®Google Scholar
• Hirosawa M, Hoshida M, Ishikawa M, Toya T. 1993. MASCOT: multiple alignment system for protein sequences based on three-way dynamic programming. Comput. Appl. Biosci. 9:161–167.
   PubMedGoogle Scholar
• Hutchins JR, Clarke PR. 2004. Many fingers on the mitotic trigger: post-translational regulation of the Cdc25C phosphatase. Cell Cycle 3:41–45.
   PubMed Web of Science ®Google Scholar
• Jacobs DM, et al. 2002. 1H, 13C and 15N backbone resonance assignment of the peptidyl-prolyl cis-trans isomerase Pin1. J. Biomol. NMR 23:163–164.
   PubMedGoogle Scholar
• Jacobs DM, et al. 2003. Peptide binding induces large scale changes in inter-domain mobility in human Pin1. J. Biol. Chem. 278:26174–26182.
   PubMedGoogle Scholar
• Kaygun H, Marzluff WF. 2005. Regulated degradation of replication-dependent histone mRNAs requires both ATR and Upf1. Nat. Struct. Mol. Biol. 12:794–800.
   PubMed Web of Science ®Google Scholar
• Kim HH, et al. 2008. Nuclear HuR accumulation through phosphorylation by Cdk1. Genes Dev. 22:1804–1815.
   PubMed Web of Science ®Google Scholar
• Kolev NG, Steitz JA. 2005. Symplekin and multiple other polyadenylation factors participate in 3′-end maturation of histone mRNAs. Genes Dev. 19:2583–2592.
   PubMedGoogle Scholar
• Koseoglu MM, Graves LM, Marzluff WF. 2008. Phosphorylation of threonine 61 by cyclin a/Cdk1 triggers degradation of stem-loop binding protein at the end of S phase. Mol. Cell. Biol. 28:4469–4479.
   PubMed Web of Science ®Google Scholar
• Krishnamurthy S, Ghazy MA, Moore C, Hampsey M. 2009. Functional interaction of the Ess1 prolyl isomerase with components of the RNA polymerase II initiation and termination machineries. Mol. Cell. Biol. 29:2925–2934.
   PubMedGoogle Scholar
• Kumar R. 2009. Pin1 regulates parathyroid hormone mRNA stability. J. Clin. Invest. 119:2887–2891.
   PubMed Web of Science ®Google Scholar
• Labeikovsky W, Eisenmesser EZ, Bosco DA, Kern D. 2007. Structure and dynamics of Pin1 during catalysis by NMR. J. Mol. Biol. 367:1370–1381.
   PubMedGoogle Scholar
• Landrieu I, et al. 2010. NMR spectroscopy of the neuronal tau protein: normal function and implication in Alzheimer's disease. Biochem. Soc. Trans. 38:1006–1011.
   PubMed Web of Science ®Google Scholar
• Landrieu I, et al. 2011. Molecular implication of PP2A and Pin1 in the Alzheimer's disease specific hyperphosphorylation of Tau. PLoS One 6:e21521. https://doi.org/10.1371/journal.pone.0021521.
   PubMedGoogle Scholar
• Lanzotti DJ, et al. 2004. Drosophila stem-loop binding protein intracellular localization is mediated by phosphorylation and is required for cell cycle-regulated histone mRNA expression. Mol. Biol. Cell 15:1112–1123.
   PubMedGoogle Scholar
• Laroia G, Cuesta R, Brewer G, Schneider RJ. 1999. Control of mRNA decay by heat shock-ubiquitin-proteasome pathway. Science 284:499–502.
   PubMed Web of Science ®Google Scholar
• Laroia G, Sarkar B, Schneider RJ. 2002. Ubiquitin-dependent mechanism regulates rapid turnover of AU-rich cytokine mRNAs. Proc. Natl. Acad. Sci. U. S. A. 99:1842–1846.
   PubMed Web of Science ®Google Scholar
• Lee TH, Pastorino L, Lu KP. 2011. Peptidyl-prolyl cis-trans isomerase Pin1 in ageing, cancer and Alzheimer disease. Expert Rev. Mol. Med. 13:e21.
   PubMed Web of Science ®Google Scholar
• Levine BJ, Chodchoy N, Marzluff WF, Skoultchi AI. 1987. Coupling of replication type histone mRNA levels to DNA synthesis requires the stem-loop sequence at the 3′ end of the mRNA. Proc. Natl. Acad. Sci. U. S. A. 84:6189–6193.
   PubMed Web of Science ®Google Scholar
• Liu W, Youn HD, Zhou XZ, Lu KP, Liu JO. 2001. Binding and regulation of the transcription factor NFAT by the peptidyl prolyl cis-trans isomerase Pin1. FEBS Lett. 496:105–108.
   PubMedGoogle Scholar
• Lu KP. 2004. Pinning down cell signaling, cancer and Alzheimer's disease. Trends Biochem. Sci. 29:200–209.
   PubMed Web of Science ®Google Scholar
• Lu KP, Finn G, Lee TH, Nicholson LK. 2007. Prolyl cis-trans isomerization as a molecular timer. Nat. Chem. Biol. 3:619–629.
   PubMed Web of Science ®Google Scholar
• Lu KP, Hanes SD, Hunter T. 1996. A human peptidyl-prolyl isomerase essential for regulation of mitosis. Nature 380:544–547.
   PubMed Web of Science ®Google Scholar
• Lu KP, Zhou XZ. 2007. The prolyl isomerase PIN1: a pivotal new twist in phosphorylation signalling and disease. Nat. Rev. Mol. Cell Biol. 8:904–916.
   PubMed Web of Science ®Google Scholar
• Maguire O, Collins C, O'Loughlin K, Miecznikowski J, Minderman H. 2011. Quantifying nuclear p65 as a parameter for NF-kappaB activation: correlation between ImageStream cytometry, microscopy, and Western blot. Cytometry A 79:461–469.
   PubMed Web of Science ®Google Scholar
• Marzluff WF, Wagner EJ, Duronio RJ. 2008. Metabolism and regulation of canonical histone mRNAs: life without a poly(A) tail. Nat. Rev. Genet. 9:843–854.
   PubMed Web of Science ®Google Scholar
• Morris DP, Phatnani HP, Greenleaf AL. 1999. Phospho-carboxyl-terminal domain binding and the role of a prolyl isomerase in pre-mRNA 3′-end formation. J. Biol. Chem. 274:31583–31587.
   PubMed Web of Science ®Google Scholar
• Nakayasu H, Berezney R. 1989. Mapping replicational sites in the eucaryotic cell nucleus. J. Cell Biol. 108:1–11.
   PubMed Web of Science ®Google Scholar
• Pastorino L, et al. 2006. The prolyl isomerase Pin1 regulates amyloid precursor protein processing and amyloid-beta production. Nature 440:528–534.
   PubMed Web of Science ®Google Scholar
• Pawlicki JM, Steitz JA. 2009. Subnuclear compartmentalization of transiently expressed polyadenylated pri-microRNAs: processing at transcription sites or accumulation in SC35 foci. Cell Cycle 8:345–356.
   PubMed Web of Science ®Google Scholar
• Ranganathan R, Lu KP, Hunter T, Noel JP. 1997. Structural and functional analysis of the mitotic rotamase Pin1 suggests substrate recognition is phosphorylation dependent. Cell 89:875–886.
   PubMed Web of Science ®Google Scholar
• Ritt DA, Monson DM, Specht SI, Morrison DK. 2010. Impact of feedback phosphorylation and Raf heterodimerization on normal and mutant B-Raf signaling. Mol. Cell. Biol. 30:806–819.
   PubMed Web of Science ®Google Scholar
• Sànchez R, Marzluff WF. 2002. The stem-loop binding protein is required for efficient translation of histone mRNA in vivo and in vitro. Mol. Cell. Biol. 22:7093–7104.
   PubMed Web of Science ®Google Scholar
• Sariban E, Wu RS, Erickson LC, Bonner WM. 1985. Interrelationships of protein and DNA syntheses during replication of mammalian cells. Mol. Cell. Biol. 5:1279–1286.
   PubMed Web of Science ®Google Scholar
• Shaw PE. 2007. Peptidyl-prolyl cis/trans isomerases and transcription: is there a twist in the tail? EMBO Rep. 8:40–45.
   PubMedGoogle Scholar
• Shen ZJ, Esnault S, Malter JS. 2005. The peptidyl-prolyl isomerase Pin1 regulates the stability of granulocyte-macrophage colony-stimulating factor mRNA in activated eosinophils. Nat. Immunol. 6:1280–1287.
   PubMed Web of Science ®Google Scholar
• Singh N, et al. 2009. The Ess1 prolyl isomerase is required for transcription termination of small noncoding RNAs via the Nrd1 pathway. Mol. Cell 36:255–266.
   PubMedGoogle Scholar
• Takahashi K, Uchida C, Shin RW, Shimazaki K, Uchida T. 2008. Prolyl isomerase, Pin1: new findings of post-translational modifications and physiological substrates in cancer, asthma and Alzheimer's disease. Cell. Mol. Life Sci. 65:359–375.
   PubMed Web of Science ®Google Scholar
• Uchida T, et al. 2003. Pin1 and Par14 peptidyl prolyl isomerase inhibitors block cell proliferation. Chem. Biol. 10:15–24.
   PubMedGoogle Scholar
• Verdecia MA, Bowman ME, Lu KP, Hunter T, Noel JP. 2000. Structural basis for phosphoserine-proline recognition by group IV WW domains. Nat. Struct. Biol. 7:639–643.
   PubMedGoogle Scholar
• Wagner EJ, Garcia-Blanco MA. 2002. RNAi-mediated PTB depletion leads to enhanced exon definition. Mol. Cell 10:943–949.
   PubMed Web of Science ®Google Scholar
• Werner-Allen JW, et al. 2011. cis-Proline-mediated Ser(P)5 dephosphorylation by the RNA polymerase II C-terminal domain phosphatase Ssu72. J. Biol. Chem. 286:5717–5726.
   PubMed Web of Science ®Google Scholar
• Whitfield ML, et al. 2004. SLBP is associated with histone mRNA on polyribosomes as a component of the histone mRNP. Nucleic Acids Res. 32:4833–4842.
   PubMedGoogle Scholar
• Whitfield ML, et al. 2000. Stem-loop binding protein, the protein that binds the 3′ end of histone mRNA, is cell cycle regulated by both translational and posttranslational mechanisms. Mol. Cell. Biol. 20:4188–4198.
   PubMed Web of Science ®Google Scholar
• Williams AS, Marzluff WF. 1995. The sequence of the stem and flanking sequences at the 3′ end of histone mRNA are critical determinants for the binding of the stem-loop binding protein. Nucleic Acids Res. 23:654–662.
   PubMed Web of Science ®Google Scholar
• Xu YX, Manley JL. 2007. New insights into mitotic chromosome condensation: a role for the prolyl isomerase Pin1. Cell Cycle 6:2896–2901.
   PubMed Web of Science ®Google Scholar
• Xu YX, Manley JL. 2007. Pin1 modulates RNA polymerase II activity during the transcription cycle. Genes Dev. 21:2950–2962.
   PubMed Web of Science ®Google Scholar
• Xu YX, Manley JL. 2004. Pinning down transcription: regulation of RNA polymerase II activity during the cell cycle. Cell Cycle 3:432–435.
   PubMedGoogle Scholar
• Yeh ES, Lew BO, Means AR. 2006. The loss of PIN1 deregulates cyclin E and sensitizes mouse embryo fibroblasts to genomic instability. J. Biol. Chem. 281:241–251.
   PubMed Web of Science ®Google Scholar
• Yeh ES, Means AR. 2007. PIN1, the cell cycle and cancer. Nat. Rev. Cancer 7:381–388.
   PubMed Web of Science ®Google Scholar
• Zhang M, Lam TT, Tonelli M, Marzluff WF, Thapar R. 2012. Interaction of histone mRNA hairpin with stem-loop binding protein and regulation of the SLBP-RNA complex by phosphorylation and proline isomerization. Biochemistry 51:3215–3231.
   PubMed Web of Science ®Google Scholar
• Zhang Y, et al. 2007. Structural basis for high-affinity peptide inhibition of human Pin1. ACS Chem. Biol. 2:320–328.
   PubMed Web of Science ®Google Scholar
• Zheng L, et al. 2003. Phosphorylation of stem-loop binding protein (SLBP) on two threonines triggers degradation of SLBP, the sole cell cycle-regulated factor required for regulation of histone mRNA processing, at the end of S phase. Mol. Cell. Biol. 23:1590–1601.
   PubMed Web of Science ®Google Scholar
• Zhou XZ, et al. 2000. Pin1-dependent prolyl isomerization regulates dephosphorylation of Cdc25C and tau proteins. Mol. Cell 6:873–883.
   PubMed Web of Science ®Google Scholar