Structure Analysis Suggests Ess1 Isomerizes the Carboxy-terminal Domain of RNA Polymerase II Via a Bivalent Anchoring Mechanism

Overview

Journal Commun Biol

Specialty Biology

Date 2021 Mar 26

PMID 33767358

Citations 5

Authors

Kevin E W Namitz

Tongyin Zheng

Ashley J Canning

Nilda L Alicea-Velazquez

Carlos A Castaneda

Michael S Cosgrove

Steven D Hanes

Affiliations

Soon will be listed here.

Abstract

Accurate gene transcription in eukaryotes depends on isomerization of serine-proline bonds within the carboxy-terminal domain (CTD) of RNA polymerase II. Isomerization is part of the "CTD code" that regulates recruitment of proteins required for transcription and co-transcriptional RNA processing. Saccharomyces cerevisiae Ess1 and its human ortholog, Pin1, are prolyl isomerases that engage the long heptad repeat (YSPTSPS) of the CTD by an unknown mechanism. Here, we used an integrative structural approach to decipher Ess1 interactions with the CTD. Ess1 has a rigid linker between its WW and catalytic domains that enforces a distance constraint for bivalent interaction with the ends of long CTD substrates (≥4-5 heptad repeats). Our binding results suggest that the Ess1 WW domain anchors the proximal end of the CTD substrate during isomerization, and that linker divergence may underlie evolution of substrate specificity.

Citing Articles

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Coevolution of the Ess1-CTD axis in polar fungi suggests a role for phase separation in cold tolerance.

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References

McNaughton L, Li Z, Van Roey P, Hanes S, LeMaster D . Restricted domain mobility in the Candida albicans Ess1 prolyl isomerase. Biochim Biophys Acta. 2010; 1804(7):1537-41. PMC: 2951753. DOI: 10.1016/j.bbapap.2010.03.005. View

Hall J, Fushman D . Characterization of the overall and local dynamics of a protein with intermediate rotational anisotropy: Differentiating between conformational exchange and anisotropic diffusion in the B3 domain of protein G. J Biomol NMR. 2003; 27(3):261-75. DOI: 10.1023/a:1025467918856. View

Jacobs D, Saxena K, Vogtherr M, Bernado P, Pons M, Fiebig K . Peptide binding induces large scale changes in inter-domain mobility in human Pin1. J Biol Chem. 2003; 278(28):26174-82. DOI: 10.1074/jbc.M300796200. View

Zhang Y, Daum S, Wildemann D, Zhou X, Verdecia M, Bowman M . Structural basis for high-affinity peptide inhibition of human Pin1. ACS Chem Biol. 2007; 2(5):320-8. PMC: 2692202. DOI: 10.1021/cb7000044. View

Berlin K, Longhini A, Dayie T, Fushman D . Deriving quantitative dynamics information for proteins and RNAs using ROTDIF with a graphical user interface. J Biomol NMR. 2013; 57(4):333-52. PMC: 3939081. DOI: 10.1007/s10858-013-9791-1. View

Xu Y, Hirose Y, Zhou X, Lu K, Manley J . Pin1 modulates the structure and function of human RNA polymerase II. Genes Dev. 2003; 17(22):2765-76. PMC: 280625. DOI: 10.1101/gad.1135503. View

Sheffield P, Garrard S, Derewenda Z . Overcoming expression and purification problems of RhoGDI using a family of "parallel" expression vectors. Protein Expr Purif. 1999; 15(1):34-9. DOI: 10.1006/prep.1998.1003. View

Adams P, Afonine P, Bunkoczi G, Chen V, Davis I, Echols N . PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr. 2010; 66(Pt 2):213-21. PMC: 2815670. DOI: 10.1107/S0907444909052925. View

Innes B, Bailey M, Brandl C, Shilton B, Litchfield D . Non-catalytic participation of the Pin1 peptidyl-prolyl isomerase domain in target binding. Front Physiol. 2013; 4:18. PMC: 3571201. DOI: 10.3389/fphys.2013.00018. View

10.

Ranganathan R, Lu K, Hunter T, Noel J . Structural and functional analysis of the mitotic rotamase Pin1 suggests substrate recognition is phosphorylation dependent. Cell. 1997; 89(6):875-86. DOI: 10.1016/s0092-8674(00)80273-1. View

11.

Raveh B, London N, Schueler-Furman O . Sub-angstrom modeling of complexes between flexible peptides and globular proteins. Proteins. 2010; 78(9):2029-40. DOI: 10.1002/prot.22716. View

12.

Atencio D, Barnes C, Duncan T, Willis I, Hanes S . The yeast Ess1 prolyl isomerase controls Swi6 and Whi5 nuclear localization. G3 (Bethesda). 2014; 4(3):523-37. PMC: 3962490. DOI: 10.1534/g3.113.008763. View

13.

Hanes S . The Ess1 prolyl isomerase: traffic cop of the RNA polymerase II transcription cycle. Biochim Biophys Acta. 2014; 1839(4):316-33. PMC: 4049342. DOI: 10.1016/j.bbagrm.2014.02.001. View

14.

Wang X, Mahoney B, Zhang M, Zintsmaster J, Peng J . Negative Regulation of Peptidyl-Prolyl Isomerase Activity by Interdomain Contact in Human Pin1. Structure. 2015; 23(12):2224-2233. PMC: 4670574. DOI: 10.1016/j.str.2015.08.019. View

15.

Lunde B, Reichow S, Kim M, Suh H, Leeper T, Yang F . Cooperative interaction of transcription termination factors with the RNA polymerase II C-terminal domain. Nat Struct Mol Biol. 2010; 17(10):1195-201. PMC: 2950884. DOI: 10.1038/nsmb.1893. View

16.

Vranken W, Boucher W, Stevens T, Fogh R, Pajon A, Llinas M . The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins. 2005; 59(4):687-96. DOI: 10.1002/prot.20449. View

17.

Steger M, Murina O, Huhn D, Ferretti L, Walser R, Hanggi K . Prolyl isomerase PIN1 regulates DNA double-strand break repair by counteracting DNA end resection. Mol Cell. 2013; 50(3):333-43. DOI: 10.1016/j.molcel.2013.03.023. View

18.

Daum S, Lucke C, Wildemann D, Schiene-Fischer C . On the benefit of bivalency in peptide ligand/pin1 interactions. J Mol Biol. 2007; 374(1):147-61. DOI: 10.1016/j.jmb.2007.09.019. View

19.

Rogals M, Greenwood A, Kwon J, Lu K, Nicholson L . Neighboring phosphoSer-Pro motifs in the undefined domain of IRAK1 impart bivalent advantage for Pin1 binding. FEBS J. 2016; 283(24):4528-4548. PMC: 5298935. DOI: 10.1111/febs.13943. View

20.

Lee Y, Liou Y . Gears-In-Motion: The Interplay of WW and PPIase Domains in Pin1. Front Oncol. 2018; 8:469. PMC: 6232885. DOI: 10.3389/fonc.2018.00469. View