2ght › Citations

Determinants for dephosphorylation of the RNA polymerase II C-terminal domain by Scp1.

Zhang Y, Kim Y, Genoud N, Gao J, Kelly JW, Pfaff SL, Gill GN, Dixon JE, Noel JP
Mol Cell 24 759-770 (2006)
Cited: 76 times
EuropePMC logo PMID: 17157258

Abstract

Phosphorylation and dephosphorylation of the C-terminal domain (CTD) of RNA polymerase II (Pol II) represent a critical regulatory checkpoint for transcription. Transcription initiation requires Fcp1/Scp1-mediated dephosphorylation of phospho-CTD. Fcp1 and Scp1 belong to a family of Mg2+ -dependent phosphoserine (P.Ser)/phosphothreonine (P.Thr)-specific phosphatases. We recently showed that Scp1 is an evolutionarily conserved regulator of neuronal gene silencing. Here, we present the X-ray crystal structures of a dominant-negative form of human Scp1 (D96N mutant) bound to mono- and diphosphorylated peptides encompassing the CTD heptad repeat (Y1S2P3T4S5P6S7). Moreover, kinetic and thermodynamic analyses of Scp1-phospho-CTD peptide complexes support the structures determined. This combined structure-function analysis discloses the residues in Scp1 involved in CTD binding and its preferential dephosphorylation of P.Ser5 of the CTD heptad repeat. Moreover, these results provide a template for the design of specific inhibitors of Scp1 for the study of neuronal stem cell development.

Reviews - 2ght mentioned but not cited (4)

  1. Viewing serine/threonine protein phosphatases through the eyes of drug designers. Zhang M, Yogesha SD, Mayfield JE, Gill GN, Zhang Y. FEBS J 280 4739-4760 (2013)
  2. Dephosphorylating eukaryotic RNA polymerase II. Mayfield JE, Burkholder NT, Zhang YJ. Biochim Biophys Acta 1864 372-387 (2016)
  3. Cross-talk of phosphorylation and prolyl isomerization of the C-terminal domain of RNA Polymerase II. Yogesha SD, Mayfield JE, Zhang Y. Molecules 19 1481-1511 (2014)
  4. Targeting the C-Terminal Domain Small Phosphatase 1. Rallabandi HR, Ganesan P, Kim YJ. Life (Basel) 10 E57 (2020)

Articles - 2ght mentioned but not cited (10)

  1. cis-Proline-mediated Ser(P)5 dephosphorylation by the RNA polymerase II C-terminal domain phosphatase Ssu72. Werner-Allen JW, Lee CJ, Liu P, Nicely NI, Wang S, Greenleaf AL, Zhou P. J Biol Chem 286 5717-5726 (2011)
  2. Determinants for dephosphorylation of the RNA polymerase II C-terminal domain by Scp1. Zhang Y, Kim Y, Genoud N, Gao J, Kelly JW, Pfaff SL, Gill GN, Dixon JE, Noel JP. Mol Cell 24 759-770 (2006)
  3. The structure of Fcp1, an essential RNA polymerase II CTD phosphatase. Ghosh A, Shuman S, Lima CD. Mol Cell 32 478-490 (2008)
  4. Structural and kinetic analysis of prolyl-isomerization/phosphorylation cross-talk in the CTD code. Zhang M, Wang XJ, Chen X, Bowman ME, Luo Y, Noel JP, Ellington AD, Etzkorn FA, Zhang Y. ACS Chem Biol 7 1462-1470 (2012)
  5. Selective inactivation of a human neuronal silencing phosphatase by a small molecule inhibitor. Zhang M, Cho EJ, Burstein G, Siegel D, Zhang Y. ACS Chem Biol 6 511-519 (2011)
  6. Phosphatase activity of small C-terminal domain phosphatase 1 (SCP1) controls the stability of the key neuronal regulator RE1-silencing transcription factor (REST). Burkholder NT, Mayfield JE, Yu X, Irani S, Arce DK, Jiang F, Matthews WL, Xue Y, Zhang YJ. J Biol Chem 293 16851-16861 (2018)
  7. The dipeptidyl peptidase IV inhibitors vildagliptin and K-579 inhibit a phospholipase C: a case of promiscuous scaffolds in proteins. Chakraborty S, Rendón-Ramírez A, Ásgeirsson B, Dutta M, Ghosh AS, Oda M, Venkatramani R, Rao BJ, Dandekar AM, Goñi FM. F1000Res 2 286 (2013)
  8. Bio-molecular architects: a scaffold provided by the C-terminal domain of eukaryotic RNA polymerase II. Zhang M, Gill GN, Zhang Y. Nano Rev 1 (2010)
  9. Chemical Tools for Studying the Impact of cis/trans Prolyl Isomerization on Signaling: A Case Study on RNA Polymerase II Phosphatase Activity and Specificity. Burkholder NT, Medellin B, Irani S, Matthews W, Showalter SA, Zhang YJ. Methods Enzymol 607 269-297 (2018)
  10. Ni-Al Bronze in Molten Carbonate Manufactured by LPBF: Effect of Porosity Design on Mechanical Properties and Oxidation. Arcos C, Guerra C, Ramos-Grez JA, Sancy M. Materials (Basel) 16 3893 (2023)


Reviews citing this publication (20)

  1. Serine/threonine phosphatases: mechanism through structure. Shi Y. Cell 139 468-484 (2009)
  2. Progression through the RNA polymerase II CTD cycle. Buratowski S. Mol Cell 36 541-546 (2009)
  3. The RNA polymerase II CTD coordinates transcription and RNA processing. Hsin JP, Manley JL. Genes Dev 26 2119-2137 (2012)
  4. Cracking the RNA polymerase II CTD code. Egloff S, Murphy S. Trends Genet 24 280-288 (2008)
  5. Emerging roles of nuclear protein phosphatases. Moorhead GB, Trinkle-Mulcahy L, Ulke-Lemée A. Nat Rev Mol Cell Biol 8 234-244 (2007)
  6. Structure of eukaryotic RNA polymerases. Cramer P, Armache KJ, Baumli S, Benkert S, Brueckner F, Buchen C, Damsma GE, Dengl S, Geiger SR, Jasiak AJ, Jawhari A, Jennebach S, Kamenski T, Kettenberger H, Kuhn CD, Lehmann E, Leike K, Sydow JF, Vannini A. Annu Rev Biophys 37 337-352 (2008)
  7. Site-specific interplay between O-GlcNAcylation and phosphorylation in cellular regulation. Hu P, Shimoji S, Hart GW. FEBS Lett 584 2526-2538 (2010)
  8. RNA polymerase II C-terminal domain: Tethering transcription to transcript and template. Corden JL. Chem Rev 113 8423-8455 (2013)
  9. Structural genomics of protein phosphatases. Almo SC, Bonanno JB, Sauder JM, Emtage S, Dilorenzo TP, Malashkevich V, Wasserman SR, Swaminathan S, Eswaramoorthy S, Agarwal R, Kumaran D, Madegowda M, Ragumani S, Patskovsky Y, Alvarado J, Ramagopal UA, Faber-Barata J, Chance MR, Sali A, Fiser A, Zhang ZY, Lawrence DS, Burley SK. J Struct Funct Genomics 8 121-140 (2007)
  10. RNA polymerase II transcription elongation control. Guo J, Price DH. Chem Rev 113 8583-8603 (2013)
  11. Human HAD phosphatases: structure, mechanism, and roles in health and disease. Seifried A, Schultz J, Gohla A. FEBS J 280 549-571 (2013)
  12. The CTD code of RNA polymerase II: a structural view. Jasnovidova O, Stefl R. Wiley Interdiscip Rev RNA 4 1-16 (2013)
  13. The Ess1 prolyl isomerase: traffic cop of the RNA polymerase II transcription cycle. Hanes SD. Biochim Biophys Acta 1839 316-333 (2014)
  14. Modifications of RNA polymerase II CTD: Connections to the histone code and cellular function. Srivastava R, Ahn SH. Biotechnol Adv 33 856-872 (2015)
  15. The diverse roles of RNA polymerase II C-terminal domain phosphatase SCP1. R HR, Kim H, Noh K, Kim YJ. BMB Rep 47 192-196 (2014)
  16. Pinning Down the Transcription: A Role for Peptidyl-Prolyl cis-trans Isomerase Pin1 in Gene Expression. Hu X, Chen LF. Front Cell Dev Biol 8 179 (2020)
  17. Serine/threonine phosphatases in osteoclastogenesis and bone resorption. Karkache IY, Damodaran JR, Molstad DHH, Bradley EW. Gene 771 145362 (2021)
  18. A combinatorial view of old and new RNA polymerase II modifications. Lyons DE, McMahon S, Ott M. Transcription 11 66-82 (2020)
  19. Catalytic scaffolds for phosphoryl group transfer. Allen KN, Dunaway-Mariano D. Curr Opin Struct Biol 41 172-179 (2016)
  20. SPOC domain proteins in health and disease. Appel LM, Benedum J, Engl M, Platzer S, Schleiffer A, Strobl X, Slade D. Genes Dev 37 140-170 (2023)

Articles citing this publication (42)

  1. The microRNA miR-124 antagonizes the anti-neural REST/SCP1 pathway during embryonic CNS development. Visvanathan J, Lee S, Lee B, Lee JW, Lee SK. Genes Dev 21 744-749 (2007)
  2. Crystal structure of the human symplekin-Ssu72-CTD phosphopeptide complex. Xiang K, Nagaike T, Xiang S, Kilic T, Beh MM, Manley JL, Tong L. Nature 467 729-733 (2010)
  3. A conserved phosphatase cascade that regulates nuclear membrane biogenesis. Kim Y, Gentry MS, Harris TE, Wiley SE, Lawrence JC, Dixon JE. Proc Natl Acad Sci U S A 104 6596-6601 (2007)
  4. Exploring the binding diversity of intrinsically disordered proteins involved in one-to-many binding. Hsu WL, Oldfield CJ, Xue B, Meng J, Huang F, Romero P, Uversky VN, Dunker AK. Protein Sci 22 258-273 (2013)
  5. Deciphering the RNA polymerase II CTD code in fission yeast. Schwer B, Shuman S. Mol Cell 43 311-318 (2011)
  6. Elucidating human phosphatase-substrate networks. Li X, Wilmanns M, Thornton J, Köhn M. Sci Signal 6 rs10 (2013)
  7. Structural insights to how mammalian capping enzyme reads the CTD code. Ghosh A, Shuman S, Lima CD. Mol Cell 43 299-310 (2011)
  8. Panoramic view of a superfamily of phosphatases through substrate profiling. Huang H, Pandya C, Liu C, Al-Obaidi NF, Wang M, Zheng L, Toews Keating S, Aono M, Love JD, Evans B, Seidel RD, Hillerich BS, Garforth SJ, Almo SC, Mariano PS, Dunaway-Mariano D, Allen KN, Farelli JD. Proc Natl Acad Sci U S A 112 E1974-83 (2015)
  9. UBLCP1 is a 26S proteasome phosphatase that regulates nuclear proteasome activity. Guo X, Engel JL, Xiao J, Tagliabracci VS, Wang X, Huang L, Dixon JE. Proc Natl Acad Sci U S A 108 18649-18654 (2011)
  10. The arabidopsis RNA binding protein with K homology motifs, SHINY1, interacts with the C-terminal domain phosphatase-like 1 (CPL1) to repress stress-inducible gene expression. Jiang J, Wang B, Shen Y, Wang H, Feng Q, Shi H. PLoS Genet 9 e1003625 (2013)
  11. Structural and functional analysis of the phosphoryl transfer reaction mediated by the human small C-terminal domain phosphatase, Scp1. Zhang M, Liu J, Kim Y, Dixon JE, Pfaff SL, Gill GN, Noel JP, Zhang Y. Protein Sci 19 974-986 (2010)
  12. The yeast regulator of transcription protein Rtr1 lacks an active site and phosphatase activity. Xiang K, Manley JL, Tong L. Nat Commun 3 946 (2012)
  13. Origin and Evolutionary Alteration of the Mitochondrial Import System in Eukaryotic Lineages. Fukasawa Y, Oda T, Tomii K, Imai K. Mol Biol Evol 34 1574-1586 (2017)
  14. Structural basis for the function of Tim50 in the mitochondrial presequence translocase. Qian X, Gebert M, Höpker J, Yan M, Li J, Wiedemann N, van der Laan M, Pfanner N, Sha B. J Mol Biol 411 513-519 (2011)
  15. Rtr1 is a dual specificity phosphatase that dephosphorylates Tyr1 and Ser5 on the RNA polymerase II CTD. Hsu PL, Yang F, Smith-Kinnaman W, Yang W, Song JE, Mosley AL, Varani G. J Mol Biol 426 2970-2981 (2014)
  16. Crystal structure of Ssu72, an essential eukaryotic phosphatase specific for the C-terminal domain of RNA polymerase II, in complex with a transition state analogue. Zhang Y, Zhang M, Zhang Y. Biochem J 434 435-444 (2011)
  17. C-terminal domain (CTD) small phosphatase-like 2 modulates the canonical bone morphogenetic protein (BMP) signaling and mesenchymal differentiation via Smad dephosphorylation. Zhao Y, Xiao M, Sun B, Zhang Z, Shen T, Duan X, Yu PB, Feng XH, Lin X. J Biol Chem 289 26441-26450 (2014)
  18. C-terminal domain small phosphatase 1 and MAP kinase reciprocally control REST stability and neuronal differentiation. Nesti E, Corson GM, McCleskey M, Oyer JA, Mandel G. Proc Natl Acad Sci U S A 111 E3929-36 (2014)
  19. novel modifications on C-terminal domain of RNA polymerase II can fine-tune the phosphatase activity of Ssu72. Luo Y, Yogesha SD, Cannon JR, Yan W, Ellington AD, Brodbelt JS, Zhang Y. ACS Chem Biol 8 2042-2052 (2013)
  20. Homo sapiens dullard protein phosphatase shows a preference for the insulin-dependent phosphorylation site of lipin1. Wu R, Garland M, Dunaway-Mariano D, Allen KN. Biochemistry 50 3045-3047 (2011)
  21. Chemical Tools To Decipher Regulation of Phosphatases by Proline Isomerization on Eukaryotic RNA Polymerase II. Mayfield JE, Fan S, Wei S, Zhang M, Li B, Ellington AD, Etzkorn FA, Zhang YJ. ACS Chem Biol 10 2405-2414 (2015)
  22. SCP1 regulates c-Myc stability and functions through dephosphorylating c-Myc Ser62. Wang W, Liao P, Shen M, Chen T, Chen Y, Li Y, Lin X, Ge X, Wang P. Oncogene 35 491-500 (2016)
  23. The Small C-terminal Domain Phosphatase 1 Inhibits Cancer Cell Migration and Invasion by Dephosphorylating Ser(P)68-Twist1 to Accelerate Twist1 Protein Degradation. Sun T, Fu J, Shen T, Lin X, Liao L, Feng XH, Xu J. J Biol Chem 291 11518-11528 (2016)
  24. Vertebrate Ssu72 regulates and coordinates 3'-end formation of RNAs transcribed by RNA polymerase II. Wani S, Yuda M, Fujiwara Y, Yamamoto M, Harada F, Ohkuma Y, Hirose Y. PLoS One 9 e106040 (2014)
  25. The nuclear phosphatase SCP4 regulates FoxO transcription factors during muscle wasting in chronic kidney disease. Liu X, Yu R, Sun L, Garibotto G, Lin X, Wang Y, Thomas SS, Li R, Hu Z. Kidney Int 92 336-348 (2017)
  26. Human SCP4 is a chromatin-associated CTD phosphatase and exhibits the dynamic translocation during erythroid differentiation. Wani S, Sugita A, Ohkuma Y, Hirose Y. J Biochem 160 111-120 (2016)
  27. Palmitoylated SCP1 is targeted to the plasma membrane and negatively regulates angiogenesis. Liao P, Wang W, Li Y, Wang R, Jin J, Pang W, Chen Y, Shen M, Wang X, Jiang D, Pang J, Liu M, Lin X, Feng XH, Wang P, Ge X. Elife 6 e22058 (2017)
  28. Role of Ser7 phosphorylation of the CTD during transcription of snRNA genes. Egloff S. RNA Biol 9 1033-1038 (2012)
  29. A potent and selective inhibitor for the UBLCP1 proteasome phosphatase. He Y, Guo X, Yu ZH, Wu L, Gunawan AM, Zhang Y, Dixon JE, Zhang ZY. Bioorg Med Chem 23 2798-2809 (2015)
  30. A study of substrate specificity for a CTD phosphatase, SCP1, by proteomic screening of binding partners. Kim YJ, Bahk YY. Biochem Biophys Res Commun 448 189-194 (2014)
  31. DUSP5 promotes osteogenic differentiation through SCP1/2-dependent phosphorylation of SMAD1. Liu X, Liu X, Du Y, Hu M, Tian Y, Li Z, Lv L, Zhang X, Liu Y, Zhou Y, Zhang P. Stem Cells 39 1395-1409 (2021)
  32. In vivo putative O-GlcNAcylation of human SCP1 and evidence for possible role of its N-terminal disordered structure. Koo J, Bahk YY. BMB Rep 47 593-598 (2014)
  33. Expression and purification of the active variant of recombinant murine Golli-interacting protein (GIP)--characterization of its phosphatase activity and interaction with Golli-BG21. Bamm VV, Harauz G. Protein Expr Purif 62 36-43 (2008)
  34. Developmental Control of NRAMP1 (SLC11A1) Expression in Professional Phagocytes. Cellier MFM. Biology (Basel) 6 E28 (2017)
  35. Regulatory effect of the glial Golli-BG21 protein on the full-length murine small C-terminal domain phosphatase (SCP1, or Golli-interacting protein). Jaramillo-Tatis S, Vassall KA, Bamm VV, Harauz G. Biochem Biophys Res Commun 447 633-637 (2014)
  36. A common structural scaffold in CTD phosphatases that supports distinct catalytic mechanisms. Pons T, Paramonov I, Boullosa C, Ibáñez K, Rojas AM, Valencia A. Proteins 82 103-118 (2014)
  37. Characterization of metal binding of bifunctional kinase/phosphatase AceK and implication in activity modulation. Zhang X, Shen Q, Lei Z, Wang Q, Zheng J, Jia Z. Sci Rep 9 9198 (2019)
  38. Over-expression in E. coli and purification of functional full-length murine small C-terminal domain phosphatase (SCP1, or Golli-interacting protein). Jaramillo-Tatis S, Bamm VV, Vassall KA, Harauz G. Protein Expr Purif 101 106-114 (2014)
  39. Phosphoserines of the carboxy terminal domain of RNA polymerase II are involved in the interaction with transcription-associated proteins (TAPs). Vidyalakshmi S, Ramamurthy V. OMICS 17 130-135 (2013)
  40. Two-track virtual screening approach to identify both competitive and allosteric inhibitors of human small C-terminal domain phosphatase 1. Park H, Lee HS, Ku B, Lee SR, Kim SJ. J Comput Aided Mol Des 31 743-753 (2017)
  41. DNA intercalator stimulates influenza transcription and virus replication. Li OT, Poon LL. Virol J 8 120 (2011)
  42. Targeted Covalent Inhibition of Small CTD Phosphatase 1 to Promote the Degradation of the REST Transcription Factor in Human Cells. Medellin B, Yang W, Konduri S, Dong J, Irani S, Wu H, Matthews WL, Zhang ZY, Siegel D, Zhang Y. J Med Chem 65 507-519 (2022)


Quick links