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The handle http://hdl.handle.net/1887/135944 holds various files of this Leiden University

dissertation.

Author: Zhang, H.

Title: Computational, biochemical, and NMR-driven structural studies on histone

variant H2A.B

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Computational, biochemical, and

NMR-driven structural studies on

histone variant H2A.B

Proefschrift

ter verkrijging van

de graad van Doctor aan de Universiteit Leiden, op gezag van Rector Magnificus prof.mr. C.J.J.M. Stolker,

volgens besluit van het College voor Promoties te verdedigen op dinsdag 25 augustus 2020

klokke 10:00 uur

door Heyi Zhang geboren te Wuxi, China

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Computational, biochemical, and NMR-driven structural studies on histone variant H2A.B

Doctoral thesis, Leiden University, 2020 Cover design: Heyi Zhang

ISBN number: 978-94-91546-17-4 ã2020, Heyi Zhang

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Promotor: Prof.dr. M. Ubbink Co-promotor: Dr. H. van Ingen

Promotiecommissie: Prof.dr. H.S. Overkleeft (voorzitter) Prof.dr.ir. S.J.T. van Noort (secretaris) Dr. R.T. Dame

Prof.dr. R. Boelens (Universiteit Utrecht) Prof.dr. T.K. Sixma (Nederlands Kanker Instituut)

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Table of Contents

ABBREVIATIONS ... 1

CHAPTER 1.GENERAL INTRODUCTION ... 3

CHAPTER 2.ISOTOPE-LABELING STRATEGIES FOR SOLUTION NMR STUDIES OF MACROMOLECULAR ASSEMBLIES ... 23

CHAPTER 3.VARIANT H2A.B-H2B HISTONE DIMER IS MORE STABLE THAN THE CANONICAL DIMER ... 45

CHAPTER 4.STRUCTURE AND DYNAMICS OF THE H2A.B VARIANT NUCLEOSOME ... 77

CHAPTER 5.THE ELECTROSTATIC POTENTIAL OF THE NUCLEOSOME ACIDIC PATCH ... 109

CHAPTER 6.DISCUSSION ... 144

SUMMARY ... 156

SAMENVATTING... 159

CURRICULUM VITAE ... 162

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1

Abbreviations

AEP AFM AP ATP Bp BME BMRB CHES ChIP ChIP-seq CPMG CS CSI CSP DNA DTT EDTA EPL FRET GFP HAC HDAC HSQC IPTG LB LEGO MD MES MNase MQ mRNA NCP NMR NOE NOESY Asparaginyl endopeptidases Atomic force microscopy Acidic patch

Adenosine triphosphate Base pairs

β-mercapto-ethanol

Biological magnetic resonance data bank N-Cyclohexyl-2-aminoethanesulfonic acid Chromatin immunoprecipitation

ChIP sequencing

Carr-Purcell-Meiboom-Gill sequence Chemical shift

Chemical shift indices Chemical shift perturbation Deoxyribonucleic acid Dithiothreitol

Ethylenediaminetetraacetic acid Expressed protein ligation

Fluorescence resonance energy transfer Green fluorescent protein

Acetic acid

Histone deacetylase

Heteronuclear single quantum coherence spectroscopy

Isopropyl β-D-1-thiogalactopyranosid Lysogeny broth

Label, express and generate oligomers Molecular dynamics

2-ethanesulfonic acid Micrococcal nuclease Multiple quantum Messenger RNA

Nucleosome core particle Nuclear magnetic resonance Nuclear overhauser effect

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2 NTD PCR PDB Pi PMSF PTM PTS R2 RMSD RNA RNA Pol II RDC SAXS SAIL SDS-PAGE SHL SrtA S/N Tm TROSY TSA tc wt Xi N-terminal domain

Polymerase chain reaction Protein data bank

Inorganic phosphate

Phenylmethylsulfonyl fluoride Post translational modification Protein trans-splicing

Transverse relaxation rate Root mean square deviation Ribonucleic acid

RNA polymerase II Residual dipolar coupling Small angle X-ray scattering Stereo-array isotope libeling

Sodium dodecyl sulfate polyacrylamide gel electrophoresis

Super helix location Sortase A

Signal to noise ratio Melting temperature

Transverse relaxation optimized spectroscopy Thermal shift assay

Rotational correlation time Wild type

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