The (I/Y)XGG motif of adenovirus DNA polymerase affects template DNA binding and the transition from initiation to elongation

Adenovirus DNA polymerase (Ad pol) is a eukaryotic-type DNA polymerase involved in the catalysis of protein-primed initiation as well as DNA polymerization. The functional significance of the (I/Y)XGG motif, highly conserved among eukaryotic-type DNA polymerases, was analyzed in Ad pol by site-direc...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:The Journal of biological chemistry Jg. 276; H. 32; S. 29846
Hauptverfasser: Brenkman, A B, Heideman, M R, Truniger, V, Salas, M, van der Vliet, P C
Format: Journal Article
Sprache:Englisch
Veröffentlicht: United States 10.08.2001
Schlagworte:
ISSN:0021-9258
Online-Zugang:Weitere Angaben
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
Abstract Adenovirus DNA polymerase (Ad pol) is a eukaryotic-type DNA polymerase involved in the catalysis of protein-primed initiation as well as DNA polymerization. The functional significance of the (I/Y)XGG motif, highly conserved among eukaryotic-type DNA polymerases, was analyzed in Ad pol by site-directed mutagenesis of four conserved amino acids. All mutant polymerases could bind primer-template DNA efficiently but were impaired in binding duplex DNA. Three mutant polymerases required higher nucleotide concentrations for effective polymerization and showed higher exonuclease activity on double-stranded DNA. These observations suggest a local destabilization of DNA substrate at the polymerase active site. In agreement with this, the mutant polymerases showed reduced initiation activity and increased K(m)(app) for the initiating nucleotide, dCMP. Interestingly, one mutant polymerase, while capable of elongating on the primer-template DNA, failed to elongate after protein priming. Further investigation of this mutant polymerase showed that polymerization activity decreased after each polymerization step and ceased completely after formation of the precursor terminal protein-trinucleotide (pTP-CAT) initiation intermediate. Our results suggest that residues in the conserved motif (I/Y)XGG in Ad pol are involved in binding the template strand in the polymerase active site and play an important role in the transition from initiation to elongation.
AbstractList Adenovirus DNA polymerase (Ad pol) is a eukaryotic-type DNA polymerase involved in the catalysis of protein-primed initiation as well as DNA polymerization. The functional significance of the (I/Y)XGG motif, highly conserved among eukaryotic-type DNA polymerases, was analyzed in Ad pol by site-directed mutagenesis of four conserved amino acids. All mutant polymerases could bind primer-template DNA efficiently but were impaired in binding duplex DNA. Three mutant polymerases required higher nucleotide concentrations for effective polymerization and showed higher exonuclease activity on double-stranded DNA. These observations suggest a local destabilization of DNA substrate at the polymerase active site. In agreement with this, the mutant polymerases showed reduced initiation activity and increased K(m)(app) for the initiating nucleotide, dCMP. Interestingly, one mutant polymerase, while capable of elongating on the primer-template DNA, failed to elongate after protein priming. Further investigation of this mutant polymerase showed that polymerization activity decreased after each polymerization step and ceased completely after formation of the precursor terminal protein-trinucleotide (pTP-CAT) initiation intermediate. Our results suggest that residues in the conserved motif (I/Y)XGG in Ad pol are involved in binding the template strand in the polymerase active site and play an important role in the transition from initiation to elongation.Adenovirus DNA polymerase (Ad pol) is a eukaryotic-type DNA polymerase involved in the catalysis of protein-primed initiation as well as DNA polymerization. The functional significance of the (I/Y)XGG motif, highly conserved among eukaryotic-type DNA polymerases, was analyzed in Ad pol by site-directed mutagenesis of four conserved amino acids. All mutant polymerases could bind primer-template DNA efficiently but were impaired in binding duplex DNA. Three mutant polymerases required higher nucleotide concentrations for effective polymerization and showed higher exonuclease activity on double-stranded DNA. These observations suggest a local destabilization of DNA substrate at the polymerase active site. In agreement with this, the mutant polymerases showed reduced initiation activity and increased K(m)(app) for the initiating nucleotide, dCMP. Interestingly, one mutant polymerase, while capable of elongating on the primer-template DNA, failed to elongate after protein priming. Further investigation of this mutant polymerase showed that polymerization activity decreased after each polymerization step and ceased completely after formation of the precursor terminal protein-trinucleotide (pTP-CAT) initiation intermediate. Our results suggest that residues in the conserved motif (I/Y)XGG in Ad pol are involved in binding the template strand in the polymerase active site and play an important role in the transition from initiation to elongation.
Adenovirus DNA polymerase (Ad pol) is a eukaryotic-type DNA polymerase involved in the catalysis of protein-primed initiation as well as DNA polymerization. The functional significance of the (I/Y)XGG motif, highly conserved among eukaryotic-type DNA polymerases, was analyzed in Ad pol by site-directed mutagenesis of four conserved amino acids. All mutant polymerases could bind primer-template DNA efficiently but were impaired in binding duplex DNA. Three mutant polymerases required higher nucleotide concentrations for effective polymerization and showed higher exonuclease activity on double-stranded DNA. These observations suggest a local destabilization of DNA substrate at the polymerase active site. In agreement with this, the mutant polymerases showed reduced initiation activity and increased K(m)(app) for the initiating nucleotide, dCMP. Interestingly, one mutant polymerase, while capable of elongating on the primer-template DNA, failed to elongate after protein priming. Further investigation of this mutant polymerase showed that polymerization activity decreased after each polymerization step and ceased completely after formation of the precursor terminal protein-trinucleotide (pTP-CAT) initiation intermediate. Our results suggest that residues in the conserved motif (I/Y)XGG in Ad pol are involved in binding the template strand in the polymerase active site and play an important role in the transition from initiation to elongation.
Author Brenkman, A B
Heideman, M R
Truniger, V
Salas, M
van der Vliet, P C
Author_xml – sequence: 1
  givenname: A B
  surname: Brenkman
  fullname: Brenkman, A B
  organization: University Medical Center, Department of Physiological Chemistry and Center for Biomedical Genetics, Utrecht, The Netherlands
– sequence: 2
  givenname: M R
  surname: Heideman
  fullname: Heideman, M R
– sequence: 3
  givenname: V
  surname: Truniger
  fullname: Truniger, V
– sequence: 4
  givenname: M
  surname: Salas
  fullname: Salas, M
– sequence: 5
  givenname: P C
  surname: van der Vliet
  fullname: van der Vliet, P C
BackLink https://www.ncbi.nlm.nih.gov/pubmed/11390396$$D View this record in MEDLINE/PubMed
BookMark eNo1kD1PwzAYhD0U0Q9YGZEnBENb27GTeKwKlEoFliLBVL1JXhdXiV1iF6kD_52qlFtOj-50w_VJx3mHhFxxNuIsk-NNUY6eOUu40oKxDukxJvhQC5V3ST-EDTtIan5OupwnmiU67ZGf5SfS2_n44-59NqONj9ZQbyhU6Py3bXeB3r9M6NbX-wZbCEjBGCxjoBGbbQ0Rj3lhXWXdmoKraDwMxhZcsNF6R03rG2rdAeDI0VOsvVsf6YKcGagDXp58QN4eH5bTp-HidTafThbDUkoWhypByZQQCmSRVwnHDJkyKs90WqCAFAwyAJaoNK-qTMvSJDyVoBU3UGAOYkBu_na3rf_aYYirxoYS6xoc-l1YZZylTEtxKF6firuiwWq1bW0D7X71f5j4BTr9bcM
CitedBy_id crossref_primary_10_1128_JVI_77_2_915_922_2003
crossref_primary_10_1038_sj_emboj_7601780
crossref_primary_10_1128_JVI_76_12_5857_5865_2002
crossref_primary_10_1128_JVI_76_16_8200_8207_2002
crossref_primary_10_1002_1873_3468_13695
crossref_primary_10_1093_nar_gkl769
crossref_primary_10_1128_JVI_78_4_1928_1935_2004
crossref_primary_10_1128_JVI_00739_12
ContentType Journal Article
DBID CGR
CUY
CVF
ECM
EIF
NPM
7X8
DOI 10.1074/jbc.M103159200
DatabaseName Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
MEDLINE - Academic
DatabaseTitle MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
MEDLINE - Academic
DatabaseTitleList MEDLINE - Academic
MEDLINE
Database_xml – sequence: 1
  dbid: NPM
  name: PubMed
  url: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 2
  dbid: 7X8
  name: MEDLINE - Academic
  url: https://search.proquest.com/medline
  sourceTypes: Aggregation Database
DeliveryMethod no_fulltext_linktorsrc
Discipline Anatomy & Physiology
Chemistry
ExternalDocumentID 11390396
Genre Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, P.H.S
Journal Article
GrantInformation_xml – fundername: NIGMS NIH HHS
  grantid: 2RO1 GM27242-21
GroupedDBID ---
-DZ
-ET
-~X
.55
.GJ
0R~
186
18M
2WC
34G
39C
3O-
53G
5BI
5GY
5RE
5VS
6TJ
79B
85S
AAEDW
AAFWJ
AALRI
AARDX
AAXUO
ABDNZ
ABOCM
ABPPZ
ABRJW
ABTAH
ACGFO
ACNCT
ADBBV
ADIYS
ADNWM
ADVLN
AENEX
AEXQZ
AFFNX
AFOSN
AFPKN
AI.
AITUG
AKRWK
ALMA_UNASSIGNED_HOLDINGS
AMRAJ
BTFSW
C1A
CGR
CJ0
CS3
CUY
CVF
DIK
DU5
E3Z
EBS
ECM
EIF
EJD
F5P
FA8
FDB
FRP
GROUPED_DOAJ
GX1
H13
HH5
IH2
KQ8
L7B
MVM
N9A
NHB
NPM
OHT
OK1
P-O
P0W
P2P
PKN
R.V
RHF
RHI
RNS
ROL
RPM
SJN
TBC
TN5
TR2
UHB
UKR
UPT
UQL
VH1
VQA
W8F
WH7
WHG
WOQ
X7M
XSW
Y6R
YQT
YSK
YWH
YYP
YZZ
Z5M
ZE2
ZGI
ZY4
~02
~KM
.7T
7X8
AAYWO
ACVFH
ADCNI
ADXHL
AEUPX
AFPUW
AIGII
AKBMS
AKYEP
ID FETCH-LOGICAL-c440t-53e405225a4b8d31e7e05f58796be2a6afe0aa03568dd794cf3164a951fabe8a2
IEDL.DBID 7X8
ISICitedReferencesCount 14
ISICitedReferencesURI http://www.webofscience.com/api/gateway?GWVersion=2&SrcApp=Summon&SrcAuth=ProQuest&DestLinkType=CitingArticles&DestApp=WOS_CPL&KeyUT=000170558000034&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D
ISSN 0021-9258
IngestDate Thu Oct 02 11:14:40 EDT 2025
Wed Feb 19 02:29:33 EST 2025
IsDoiOpenAccess false
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 32
Language English
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c440t-53e405225a4b8d31e7e05f58796be2a6afe0aa03568dd794cf3164a951fabe8a2
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
OpenAccessLink http://www.jbc.org/article/S0021925820896823/pdf
PMID 11390396
PQID 71060942
PQPubID 23479
ParticipantIDs proquest_miscellaneous_71060942
pubmed_primary_11390396
PublicationCentury 2000
PublicationDate 2001-08-10
PublicationDateYYYYMMDD 2001-08-10
PublicationDate_xml – month: 08
  year: 2001
  text: 2001-08-10
  day: 10
PublicationDecade 2000
PublicationPlace United States
PublicationPlace_xml – name: United States
PublicationTitle The Journal of biological chemistry
PublicationTitleAlternate J Biol Chem
PublicationYear 2001
SSID ssj0000491
Score 1.732781
Snippet Adenovirus DNA polymerase (Ad pol) is a eukaryotic-type DNA polymerase involved in the catalysis of protein-primed initiation as well as DNA polymerization....
SourceID proquest
pubmed
SourceType Aggregation Database
Index Database
StartPage 29846
SubjectTerms Adenoviridae - enzymology
Amino Acid Motifs
Amino Acid Sequence
Amino Acids - chemistry
Binding Sites
Catalysis
DNA - metabolism
DNA Mutational Analysis
DNA-Binding Proteins - metabolism
DNA-Directed DNA Polymerase - chemistry
Dose-Response Relationship, Drug
Glycerol - pharmacology
Kinetics
Molecular Sequence Data
Mutagenesis, Site-Directed
Mutation
Protein Binding
Title The (I/Y)XGG motif of adenovirus DNA polymerase affects template DNA binding and the transition from initiation to elongation
URI https://www.ncbi.nlm.nih.gov/pubmed/11390396
https://www.proquest.com/docview/71060942
Volume 276
WOSCitedRecordID wos000170558000034&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D
hasFullText
inHoldings 1
isFullTextHit
isPrint
link http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwpV1Na9tAEB3cuNBe0iRO2jRNModSmoPilVYfKygUk8RODjY5tOCezK52N7i4khs7Bh_63zO7sugp5JCLQAiBGM3OvJl9Ow_gc2ZVnhpeBFxLHcQZN4HKQxtkNlTaFpqStvJiE9loJMbj_LYF35qzMI5W2cREH6h1VbgeeZcyYUqlSPR9_jdwmlFub3UjoPEK2pyAjFuW2fj_rHDCvrVeniMhRIloRjZmcfe3Ks6HXuAgjxh7Glz6JNN_97LP24HtDbjEXu0Nu9Ay5R50eiUV1n_W-AU93dP30ffgzUUj9daBf-Qs-PWm--tsPBigo-dZrCxKiknVanr_sMDLUQ_n1WztWlgLg7JmgaAbbDUjtOqfq6k_IYOy1EiwEpcuDXpGGLpDLDh1PCXvCLis0Myq8s7f7cPP_tWPi-tgo8sQFHHMlkHCDcE8CgQyVkLz0GSGJTYRWZ4qE8lUWsOkZDxJhda03gvLqSiThOWsVEbI6AC2yqo0HwDddDCRkr-IwsZch1LZkEsVcRULyZg9hNPG3BOyidvMkKWpHhaTxuCH8L7-Y5N5PZ6DahqeM56nH5999wje1pQyN-H2E7QtrXhzDK-L1XK6uD_x7kTX0e3wEame1rU
linkProvider ProQuest
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=The+%28I%2FY%29XGG+motif+of+adenovirus+DNA+polymerase+affects+template+DNA+binding+and+the+transition+from+initiation+to+elongation&rft.jtitle=The+Journal+of+biological+chemistry&rft.au=Brenkman%2C+A+B&rft.au=Heideman%2C+M+R&rft.au=Truniger%2C+V&rft.au=Salas%2C+M&rft.date=2001-08-10&rft.issn=0021-9258&rft.volume=276&rft.issue=32&rft.spage=29846&rft_id=info:doi/10.1074%2Fjbc.M103159200&rft.externalDBID=NO_FULL_TEXT
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=0021-9258&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=0021-9258&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=0021-9258&client=summon