Cover Page
The handle http://hdl.handle.net/1887/28538 holds various files of this Leiden University
dissertation
Author: Schimmel, Joost
Title: Regulation of genome stability and cell cycle progression by SUMOylation
Issue Date: 2014-09-09
List of abbreviations
List of abbreviations
53BP1
Aos1
APC/C
ATG12
ATG8
ATP
BCA
BER
BRCA1
BRCA2
BrdU
BTB
BubR1
BZEL
C-Abl
CBX4
Cdc48
CDK1
cDNA
CENP
CFP
CID
CMV
CPC
CPT
CS
CSA
CSB
CSN
DAPI
Daxx
DDB1
DDR
DeSI
DIC
DMEM
DNA
DNMT1
DSB
DTT
DUB
DUSP
Elisa
Elk-1
FACS
Tumor suppressor p53-binding protein 1
Activation of Smt3
anaphase-promoting complex/cyclosome
Autophagy-Related Protein 12
Autophagy-Related Protein 8
Adenosine triphosphate
Bicinchoninic acid assay
Base Excision Repair
Breast Cancer Type 1 Susceptibility Protein
Breast Cancer Type 2 Susceptibility Protein
5-bromo-2'-deoxyuridine
Broad-Complex, Tramtrack and Bric-a-brac
Budding uninhibited by benzimidazoles 1 beta
Zinc finger and BTB-containing protein 46
Abelson tyrosine-protein kinase 1
Chromobox Protein Homolog 4
Cell division control protein 48
Cyclin-Dependent Kinase 1
Circular DNA
Centromere protein
Cyan Fluorescent Protein
Collision-induced dissociation
Cytomegalovirus
Chromosomal passenger complex
Camptothecin
Cockayne Syndrome
Cockayne syndrome A
Cockayne syndrome B
COP9 signalosome
4',6-diamidino-2-phenylindole
Death Domain-Associated Protein 6
DNA damage-binding protein 1
DNA damage response
Desumoylating isopeptidase
Differential Interference Contrast
Dulbecco’s Modified Eagle’s Medium
Deoxyribonucleic acid
DNA (cytosine-5)-methyltransferase 1
Double Strand Break
Dithiothreitol
Deubiquitinating enzyme
Domain present in Ubiquitin-Specific Proteases
Enzyme-Linked Immunosorbent Assay
E26 transformation-specific domain-containing protein 1
Fluorescence-Activated Cell Sorting
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List of abbreviations
FAT10
FBS
FKH
FoxM1
GATA-1
GFP
GO
GST
HA
HCD
HCSM
HDAC
HEK293
HER2C
HIF-1α
His-tag
hnRNP M
HR
HRP
HU
HUB1
IkBα
IKKγ
IMAC
IP
IPTG
IR
IRES
ISG15
LC
LDS
LFQ
LTQ
LV
LysC
m/z
MBP
MCF-7
MCODE
MDC1
MEF
MES
MMS
Mms2
MOPS
mRNA
MS
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HLA-F adjacent transcript 10
Fetal Bovine Serum
Forkhead winged helix DNA binding domain
Forkhead box protein M1
GATA-binding factor 1
Green Fluorescent Protein
Gene Ontology
Glutathione S-transferase
Hemagglutinin
Higher-Collisional Dissociation
Hydrophobic Cluster SUMOylation Motif
Histone deacetylase
Human Embryonic Kidney 293
Human epidermal growth factor receptor 2c
Hypoxia-inducible factor 1-alpha
Polyhistidine-tag
Heterogeneous nuclear ribonucleoprotein M
Homologous recombination
Horseradish peroxidase
Hydroxyurea
Histone monoubiquitination 1
NF-kB inhibitor alpha
Inhibitor of NF-kB kinase subunit gamma
Immobilized metal affinity chromatography
Immunoprecipitation
Isopropyl-β-D-thiogalactopyranoside
Ionizing Radiation
Internal Ribosome Entry Site
Interferon-stimulated gene 15
Liquid Chromatography
Lithium Dodecyl Sulphate
Label-Free Quantification
Linear Ion Trap Mass Spectrometer
Lentivirus
Lysyl Endopeptidase
Mass/charge ratio
Maltose-Binding Protein
Michigan Cancer Foundation-7
Molecular Complex Detection
Mediator of DNA damage checkpoint protein 1
Mouse embryonic fibroblast
2-(N-morpholino)ethanesulfonic acid
Methylmethane sulfonate
Methyl methanesulfonate sensitive 2
3-(N-morpholino)propanesulfonic acid
Messenger RNA
Mass spectrometry
List of abbreviations
MS/MS
NB
NDSM
Nedd
NEIL-1
NEMO
NER
NF-kB
NHEJ
Ni-NTA
NOP58
NPC
NRD
NSE2
NuRD
p53
PAGE
PARI
PARP
PBS
PBST
PcG
PCNA
PCR PDSM
PEI
PEP
PGBD3
PHYRE2
PIAS
PLA
PML
PML-RARα
Pol
ppm
PTM
RAD51
RanBP2
RanGAP1
Rap1
RAP80
RCF
Rfp
RING
RNA
RNAPII
RNF
Tandem mass spectrometry
Nuclear body
Negatively charged amino acid-Dependent SUMOylation Motif
Neural precursor cell expressed developmentally down-regulated
Nei-like protein 1
NF-kappa-B essential modulator
Nucleotide excision repair
Nuclear factor NF-kappa-Beta
Non-homologous end joining
Nickel - Nitrilotriacetic acid
Nucleolar Protein 58
Nuclear pore complex
N-terminal repressor domain
Non-structural maintenance of chromosomes element 2 homolog
Nucleosome Remodeling Deacetylase
Cellular Tumor Antigen p53
Polyacrylamide gel electrophoresis
PCNA-interacting partner
Poly ADP Ribose Polymerase
Phosphate buffered saline
Phosphate Buffered Saline containing Tween-20
Polycomb group
Proliferating cell nuclear antigen
Polymerase Chain Reaction
Phosphorylation-dependent sumoylation motif
Polyethylenimine
Posterior error probability
PiggyBac transposable element-derived protein 3
Protein Homology/analogY Recognition Engine V2.0
Protein inhibitor of activated STAT
Proximity Ligation Assay
Promyelocytic leukemia protein
PML-retinoic acid receptor alpha
Polymerase
Parts per million
Post translational modification
Radiation sensitive 51
Ran-binding protein 2
Ran GTPase-activating protein
Repressor/activator site-binding protein 1
Receptor-associated protein 80
Relative Centrifugal Force
RING finger protein
Really interesting new gene
Ribonucleic acid
RNA polymerase II
RING finger protein
203
List of abbreviations
RPA
RPB1
RPM
SAE
SART1
SD
SDS
SEM
SENP
shRNA
SILAC
SIM
Siz
SLX5/8
SMC5/6
SMRT
Smt3
Sp100
STAT
STRING
STUBL
SUMO
SWI2/SNF2 TAD
TAP
TC-NER
TDG
Topo IIα
TOPORS
U2OS
Ub
Uba2
Ubc13
Ubc9
Ubch5a
UBD
UBE1
UBL
UBL5
UCH
Ulp
Uls1
URM1
USP11
USP25
USP7
USPL1
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Replication protein A
DNA-directed RNA polymerase III largest subunit
Rounds per minute
SUMO-activating enzyme subunit
Squamous cell carcinoma antigen recognized by T-cells 1
Standard Deviation
Sodium dodecyl sulphate
Standard error of the mean
Sentrin-specific protease
Short hairpin RNA
Stable Isotope Labeling by Amino acids in Cell culture
SUMO interacting motif
SAP and Miz-finger domain-containing protein
Synthetic lethal of unknown function protein 5 and 8
Structural maintenance of chromosomes protein 5 and 6
Silencing mediator of retinoic acid and thyroid hormone receptor
Suppressor of mitochondrial initiation factor two 3
Speckled 100 kDa protien
Signal transducer and activator of transcription
Search Tool for the Retrieval of Interacting Genes/Proteins
SUMO targeted ubiquitin ligase
Small Ubiquitin-like Modifier
SWItch 2/Sucrose NonFermentable 2
Transactivation domain
Tandem Affinity Purification
Transcription Coupled NER
Thymine-DNA glycosylase
Topoisomerase IIα
Topoisomerase I-binding RING finger protein
U-2 Osteosarcoma
Ubiquitin
Ubiquitin Activating enzyme E1-like
Ubiquitin-conjugating enzyme 13
Ubiquitin carrier protein 9
Ubiquitin-Conjugating Enzyme E2 D1
Ubiquitin binding domain
Ubiquitin-Like Modifier-Activating Enzyme 1
Ubiquitin like
Ubiquitin-Like Protein 5
Ubiquitin Carboxyl-terminal Hydrolase
Ubiquitin-like-specific protease
Ubiquitin ligase for SUMO conjugates protein 1
Ubiquitin-related modifier 1
Ubiquitin-specific-processing protease 11
Ubiquitin carboxyl-terminal hydrolase 25
Ubiquitin carboxyl-terminal hydrolase 7
Ubiquitin-specific peptidase-like protein 1
List of abbreviations
UV
UVSSA
VCP/p97
WST-1
WT
XPC
YFP
ZBTB1
β-Gal
Ultraviolet
UV-stimulated scaffold protein A
Valosin-containing protein
Water-soluble tetrazolium salt-1
Wild-type
Xeroderma pigmentosum group C-complementing protein
Yellow Fluorescent Protein
Zinc Finger and BTB Domain-Containing Protein 1
Beta-galactosidase
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206
Curriculum Vitae
Curriculum Vitae
Joost Schimmel was born on the 17th of April 1984 in Lopik, the Netherlands. In
2001 he received his HAVO diploma at the CSG Willem de Zwijger in Schoonhoven.
After that he attended the HLO in Utrecht studying Molecular Biology, as part of this
study he performed an internship at the Hubrecht Institute in the lab of Prof. dr. L de
Windt. Under supervision of Dr. R.J. van Oort he studied the role of the transcription
factor MEF2 in heart failure. After the successful completion of the HLO he started
as a research technician at the department of Molecular and Cellular Biology at the
Leiden University Medical Center in the lab of Dr. A.C.O. Vertegaal. In this research
group, he started his PhD training in January 2010, studying the role of SUMOylation
in several cellular processes. Since April 2014 he is working as a postdoc in the lab
of Dr. M. Tijsterman at the department of Toxicogenetics at the Leiden University
Medical Center.
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List of publications
List of publications
1. Hendriks, I.A.*, Schimmel, J.*, Olsen, J.V. and Vertegaal, A.C. (2014) USP11
Counteracts RNF4 and Stabilizes PML Nuclear Bodies. Submitted
2. Schimmel, J.*, Eifler, K.*, Sigurethsson, J. O.*, Cuijpers, S. A., Hendriks, I. A.,
Verlaan-de, V. M., Kelstrup, C. D., Francavilla, C., Medema, R. H., Olsen, J. V.,
and Vertegaal, A. C. (2014) Uncovering SUMOylation Dynamics during CellCycle Progression Reveals FoxM1 as a Key Mitotic SUMO Target Protein.
Mol. Cell 53, 1053-1066
3. Zhang, L., Huang, H., Zhou, F., Schimmel, J., Pardo, C. G., Zhang, T., Barakat,
T. S., Sheppard, K. A., Mickanin, C., Porter, J. A., Vertegaal, A. C., van, D.
H., Gribnau, J., Lu, C. X., and ten, D. P. (2012) RNF12 controls embryonic
stem cell fate and morphogenesis in zebrafish embryos by targeting Smad7
for degradation. Mol. Cell 46, 650-661
4. Matic, I.*, Schimmel, J.*, Hendriks, I. A.*, van Santen, M. A.*, van de Rijke,
F., van, D. H., Gnad, F., Mann, M., and Vertegaal, A. C. (2010) Site-specific
identification of SUMO-2 targets in cells reveals an inverted SUMOylation
motif and a hydrophobic cluster SUMOylation motif. Mol. Cell 39, 641-652
5. Schimmel, J., Balog, C. I., Deelder, A. M., Drijfhout, J. W., Hensbergen, P.
J., and Vertegaal, A. C. (2010) Positively charged amino acids flanking a
sumoylation consensus tetramer on the 110kDa tri-snRNP component SART1
enhance sumoylation efficiency. J. Proteomics. 73, 1523-1534
6. Brouwer, A. K., Schimmel, J., Wiegant, J. C., Vertegaal, A. C., Tanke, H. J.,
and Dirks, R. W. (2009) Telomeric DNA mediates de novo PML body formation.
Mol. Biol. Cell 20, 4804-4815
7. Schimmel, J.*, Larsen, K. M.*, Matic, I.*, van, H. M., Cox, J., Mann, M.,
Andersen, J. S., and Vertegaal, A. C. (2008) The ubiquitin-proteasome system
is a key component of the SUMO-2/3 cycle. Mol. Cell Proteomics. 7, 21072122
8. Matic, I., van, H. M., Schimmel, J., Macek, B., Ogg, S. C., Tatham, M. H., Hay,
R. T., Lamond, A. I., Mann, M., and Vertegaal, A. C. (2008) In vivo identification
of human small ubiquitin-like modifier polymerization sites by high accuracy
mass spectrometry and an in vitro to in vivo strategy. Mol. Cell Proteomics. 7,
132-144
9. van Oort, R. J., van, R. E., Bourajjaj, M., Schimmel, J., Jansen, M. A., van
der Nagel, R., Doevendans, P. A., Schneider, M. D., van Echteld, C. J., and
De Windt, L. J. (2006) MEF2 activates a genetic program promoting chamber
dilation and contractile dysfunction in calcineurin-induced heart failure.
Circulation 114, 298-308
*, Equal author contributions
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