A robust methodology to subclassify pseudokinases based on their nucleotide-binding properties

Protein kinase-like domains that lack conserved residues known to catalyse phosphoryl transfer, termed pseudokinases, have emerged as important signalling domains across all kingdoms of life. Although predicted to function principally as catalysis-independent protein-interaction modules, several pse...

Full description

Saved in:
Bibliographic Details
Published inBiochemical journal Vol. 457; no. 2; p. 323
Main Authors Murphy, James M, Zhang, Qingwei, Young, Samuel N, Reese, Michael L, Bailey, Fiona P, Eyers, Patrick A, Ungureanu, Daniela, Hammaren, Henrik, Silvennoinen, Olli, Varghese, Leila N, Chen, Kelan, Tripaydonis, Anne, Jura, Natalia, Fukuda, Koichi, Qin, Jun, Nimchuk, Zachary, Mudgett, Mary Beth, Elowe, Sabine, Gee, Christine L, Liu, Ling, Daly, Roger J, Manning, Gerard, Babon, Jeffrey J, Lucet, Isabelle S
Format Journal Article
LanguageEnglish
Published England 15.01.2014
Subjects
Online AccessGet more information

Cover

Loading…
Abstract Protein kinase-like domains that lack conserved residues known to catalyse phosphoryl transfer, termed pseudokinases, have emerged as important signalling domains across all kingdoms of life. Although predicted to function principally as catalysis-independent protein-interaction modules, several pseudokinase domains have been attributed unexpected catalytic functions, often amid controversy. We established a thermal-shift assay as a benchmark technique to define the nucleotide-binding properties of kinase-like domains. Unlike in vitro kinase assays, this assay is insensitive to the presence of minor quantities of contaminating kinases that may otherwise lead to incorrect attribution of catalytic functions to pseudokinases. We demonstrated the utility of this method by classifying 31 diverse pseudokinase domains into four groups: devoid of detectable nucleotide or cation binding; cation-independent nucleotide binding; cation binding; and nucleotide binding enhanced by cations. Whereas nine pseudokinases bound ATP in a divalent cation-dependent manner, over half of those examined did not detectably bind nucleotides, illustrating that pseudokinase domains predominantly function as non-catalytic protein-interaction modules within signalling networks and that only a small subset is potentially catalytically active. We propose that henceforth the thermal-shift assay be adopted as the standard technique for establishing the nucleotide-binding and catalytic potential of kinase-like domains.
AbstractList Protein kinase-like domains that lack conserved residues known to catalyse phosphoryl transfer, termed pseudokinases, have emerged as important signalling domains across all kingdoms of life. Although predicted to function principally as catalysis-independent protein-interaction modules, several pseudokinase domains have been attributed unexpected catalytic functions, often amid controversy. We established a thermal-shift assay as a benchmark technique to define the nucleotide-binding properties of kinase-like domains. Unlike in vitro kinase assays, this assay is insensitive to the presence of minor quantities of contaminating kinases that may otherwise lead to incorrect attribution of catalytic functions to pseudokinases. We demonstrated the utility of this method by classifying 31 diverse pseudokinase domains into four groups: devoid of detectable nucleotide or cation binding; cation-independent nucleotide binding; cation binding; and nucleotide binding enhanced by cations. Whereas nine pseudokinases bound ATP in a divalent cation-dependent manner, over half of those examined did not detectably bind nucleotides, illustrating that pseudokinase domains predominantly function as non-catalytic protein-interaction modules within signalling networks and that only a small subset is potentially catalytically active. We propose that henceforth the thermal-shift assay be adopted as the standard technique for establishing the nucleotide-binding and catalytic potential of kinase-like domains.
Author Tripaydonis, Anne
Liu, Ling
Mudgett, Mary Beth
Fukuda, Koichi
Qin, Jun
Elowe, Sabine
Lucet, Isabelle S
Reese, Michael L
Nimchuk, Zachary
Zhang, Qingwei
Gee, Christine L
Young, Samuel N
Hammaren, Henrik
Murphy, James M
Bailey, Fiona P
Eyers, Patrick A
Chen, Kelan
Varghese, Leila N
Ungureanu, Daniela
Jura, Natalia
Manning, Gerard
Daly, Roger J
Babon, Jeffrey J
Silvennoinen, Olli
Author_xml – sequence: 1
  givenname: James M
  surname: Murphy
  fullname: Murphy, James M
– sequence: 2
  givenname: Qingwei
  surname: Zhang
  fullname: Zhang, Qingwei
  organization: ‡Department of Biochemistry and Molecular Biology, School of Biomedical Sciences, Monash University, Clayton, Victoria 3800, Australia
– sequence: 3
  givenname: Samuel N
  surname: Young
  fullname: Young, Samuel N
  organization: The Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria 3052, Australia
– sequence: 4
  givenname: Michael L
  surname: Reese
  fullname: Reese, Michael L
  organization: §Department of Microbiology and Immunology, Stanford University, Stanford, CA 24305-5124, U.S.A
– sequence: 5
  givenname: Fiona P
  surname: Bailey
  fullname: Bailey, Fiona P
  organization: ¶Department of Biochemistry, Institute of Integrative Biology, University of Liverpool, Liverpool L69 7ZB, U.K
– sequence: 6
  givenname: Patrick A
  surname: Eyers
  fullname: Eyers, Patrick A
  organization: ¶Department of Biochemistry, Institute of Integrative Biology, University of Liverpool, Liverpool L69 7ZB, U.K
– sequence: 7
  givenname: Daniela
  surname: Ungureanu
  fullname: Ungureanu, Daniela
  organization: ∥School of Medicine and Institute of Biomedical Technology, University of Tampere and Tampere University Hospital, Tampere 33014, Finland
– sequence: 8
  givenname: Henrik
  surname: Hammaren
  fullname: Hammaren, Henrik
  organization: ∥School of Medicine and Institute of Biomedical Technology, University of Tampere and Tampere University Hospital, Tampere 33014, Finland
– sequence: 9
  givenname: Olli
  surname: Silvennoinen
  fullname: Silvennoinen, Olli
  organization: ∥School of Medicine and Institute of Biomedical Technology, University of Tampere and Tampere University Hospital, Tampere 33014, Finland
– sequence: 10
  givenname: Leila N
  surname: Varghese
  fullname: Varghese, Leila N
– sequence: 11
  givenname: Kelan
  surname: Chen
  fullname: Chen, Kelan
– sequence: 12
  givenname: Anne
  surname: Tripaydonis
  fullname: Tripaydonis, Anne
  organization: The Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria 3052, Australia
– sequence: 13
  givenname: Natalia
  surname: Jura
  fullname: Jura, Natalia
  organization: Cardiovascular Research Institute and Department of Cellular and Molecular Pharmacology, University of California San Francisco, San Francisco, CA 94158-9001, U.S.A
– sequence: 14
  givenname: Koichi
  surname: Fukuda
  fullname: Fukuda, Koichi
  organization: ††Department of Molecular Cardiology, Lerner Research Institute, NB20, Cleveland Clinic, 9500 Euclid Avenue, Cleveland, OH 44195, U.S.A
– sequence: 15
  givenname: Jun
  surname: Qin
  fullname: Qin, Jun
  organization: ††Department of Molecular Cardiology, Lerner Research Institute, NB20, Cleveland Clinic, 9500 Euclid Avenue, Cleveland, OH 44195, U.S.A
– sequence: 16
  givenname: Zachary
  surname: Nimchuk
  fullname: Nimchuk, Zachary
  organization: ‡‡Department of Biology, California Institute of Technology, Pasadena, CA 91125, U.S.A
– sequence: 17
  givenname: Mary Beth
  surname: Mudgett
  fullname: Mudgett, Mary Beth
  organization: §§Department of Biology, Stanford University, Stanford, CA 24305-5020, U.S.A
– sequence: 18
  givenname: Sabine
  surname: Elowe
  fullname: Elowe, Sabine
  organization: ¶¶Centre de Recherche du Centre Hospitalier Universitaire de Québec and and Faculté de Médicine, Département de Pédiatrie, Université Laval, Québec G1V 4G2, Canada
– sequence: 19
  givenname: Christine L
  surname: Gee
  fullname: Gee, Christine L
  organization: ∥∥Australian Synchrotron, Clayton, Victoria 3168, Australia
– sequence: 20
  givenname: Ling
  surname: Liu
  fullname: Liu, Ling
  organization: Cancer Research Program, The Kinghorn Cancer Centre, Garvan Institute of Medical Research, 370 Victoria Street, Darlinghurst, Sydney, NSW 2010, Australia
– sequence: 21
  givenname: Roger J
  surname: Daly
  fullname: Daly, Roger J
  organization: Cancer Research Program, The Kinghorn Cancer Centre, Garvan Institute of Medical Research, 370 Victoria Street, Darlinghurst, Sydney, NSW 2010, Australia
– sequence: 22
  givenname: Gerard
  surname: Manning
  fullname: Manning, Gerard
  organization: †††Genentech, 1 DNA Way, MS 93, South San Francisco, CA 94010, U.S.A
– sequence: 23
  givenname: Jeffrey J
  surname: Babon
  fullname: Babon, Jeffrey J
– sequence: 24
  givenname: Isabelle S
  surname: Lucet
  fullname: Lucet, Isabelle S
  organization: ‡Department of Biochemistry and Molecular Biology, School of Biomedical Sciences, Monash University, Clayton, Victoria 3800, Australia
BackLink https://www.ncbi.nlm.nih.gov/pubmed/24107129$$D View this record in MEDLINE/PubMed
BookMark eNo1j8tOxCAUQInROA_d-AGGH6gCpQWW48RnJnGjWyc8LjNoC02hi_69JurmnN1JzgqdxhQBoStKbijh7PbuhRFaUyr4CVpSLkglBZMLtMr5kxDKCSfnaME4JYIytUQfGzwmM-WCeyjH5FKXDjMuCefJ2E7nHPyMhwyTS18h6gwZmx86nCIuRwgjjpPtIJXgoDIhuhAPeBjTAGMJkC_Qmdddhss_r9H7w_3b9qnavT4-bze7ynKqSuWNlNLWtWudkMKxhiivrPLcSgOG1Y3movEtgYYxVTfeei9bpa2uuRNCAFuj69_uMJke3H4YQ6_Hef8_yr4BkG5WRw
CitedBy_id crossref_primary_10_1042_BST20160400
crossref_primary_10_1242_jcs_221184
crossref_primary_10_1016_j_jbc_2021_100705
crossref_primary_10_1042_BST20180496
crossref_primary_10_1371_journal_pgen_1004326
crossref_primary_10_2139_ssrn_3155618
crossref_primary_10_2139_ssrn_4054459
crossref_primary_10_1016_j_str_2015_08_017
crossref_primary_10_1042_BST20180481
crossref_primary_10_1073_pnas_1816161116
crossref_primary_10_1016_j_ijpddr_2020_10_008
crossref_primary_10_1038_s41598_018_26957_6
crossref_primary_10_1038_s41467_018_04714_7
crossref_primary_10_1038_s41388_019_0931_2
crossref_primary_10_1111_cts_13435
crossref_primary_10_1126_scisignal_aat9797
crossref_primary_10_1042_BJ20131270
crossref_primary_10_1021_jasms_1c00271
crossref_primary_10_4103_1673_5374_264469
crossref_primary_10_1016_j_str_2022_08_006
crossref_primary_10_1126_scisignal_aax2713
crossref_primary_10_1186_s12859_021_04358_3
crossref_primary_10_1080_08977194_2018_1491848
crossref_primary_10_1186_s12943_015_0412_3
crossref_primary_10_1016_j_bbamcr_2015_05_015
crossref_primary_10_1080_08977194_2018_1472089
crossref_primary_10_1126_scisignal_aah3525
crossref_primary_10_3390_cells8080812
crossref_primary_10_7554_eLife_23990
crossref_primary_10_1016_j_str_2018_07_015
crossref_primary_10_3390_ijms21165931
crossref_primary_10_1016_j_celrep_2020_108397
crossref_primary_10_1016_j_jbc_2021_100267
crossref_primary_10_1371_journal_pone_0144673
crossref_primary_10_1042_BJ20141060
crossref_primary_10_1039_C8OB03152E
crossref_primary_10_1126_scisignal_aav3810
crossref_primary_10_1042_BCJ20190875
crossref_primary_10_1128_MCB_00057_14
crossref_primary_10_1021_acschembio_0c00482
crossref_primary_10_1042_BCJ20220373
crossref_primary_10_1016_j_str_2016_07_008
crossref_primary_10_1038_cddis_2016_485
crossref_primary_10_1038_s41418_022_00965_6
crossref_primary_10_1016_j_str_2020_11_004
crossref_primary_10_1042_BCJ20210572
crossref_primary_10_3390_biomedicines10102559
crossref_primary_10_1111_febs_15087
crossref_primary_10_1016_j_biotechadv_2018_02_013
crossref_primary_10_1182_blood_2015_01_621110
crossref_primary_10_1039_C6MB00466K
crossref_primary_10_1371_journal_pone_0102695
crossref_primary_10_1042_BJ20141441
crossref_primary_10_1073_pnas_1919960117
crossref_primary_10_1039_D1OB01353J
crossref_primary_10_1016_j_cell_2018_10_011
crossref_primary_10_1038_s41467_017_01279_9
crossref_primary_10_1016_j_drup_2021_100788
crossref_primary_10_1021_acs_jmedchem_1c00980
crossref_primary_10_1021_acs_jcim_8b00640
crossref_primary_10_1042_BST20180473
crossref_primary_10_1042_BCJ20220474
crossref_primary_10_1016_j_str_2024_02_021
crossref_primary_10_3389_fonc_2018_00560
crossref_primary_10_1038_icb_2016_125
crossref_primary_10_1042_BJ20131516
crossref_primary_10_1093_plphys_kiae268
crossref_primary_10_1016_j_str_2021_01_011
crossref_primary_10_1016_j_tibs_2022_04_011
crossref_primary_10_1242_bio_058528
crossref_primary_10_1016_j_redox_2019_101318
crossref_primary_10_1021_acs_chemrev_8b00467
crossref_primary_10_1016_j_str_2020_10_005
crossref_primary_10_1038_s41598_022_15339_8
crossref_primary_10_1042_BCJ20220598
crossref_primary_10_1182_bloodadvances_2017010215
crossref_primary_10_1002_cbic_202000874
crossref_primary_10_1042_BCJ20230035
crossref_primary_10_1073_pnas_1423201112
crossref_primary_10_1080_19336918_2017_1394570
crossref_primary_10_1002_iub_2698
crossref_primary_10_1074_jbc_RA117_000751
crossref_primary_10_3389_fcell_2022_942500
crossref_primary_10_3390_ijms241511928
crossref_primary_10_1016_j_sbi_2017_07_004
crossref_primary_10_4161_23723556_2014_985550
crossref_primary_10_1038_s41467_023_40823_8
crossref_primary_10_1073_pnas_1906360116
crossref_primary_10_1074_jbc_M115_672048
crossref_primary_10_4155_fmc_2016_0207
crossref_primary_10_1016_j_tibs_2018_11_002
crossref_primary_10_1021_acschembio_8b00722
crossref_primary_10_1038_s41388_024_03060_x
crossref_primary_10_1136_annrheumdis_2019_215062
crossref_primary_10_1016_j_jcmgh_2022_09_015
crossref_primary_10_1016_j_str_2018_01_017
crossref_primary_10_1002_1873_3468_12966
crossref_primary_10_1158_0008_5472_CAN_17_2291
crossref_primary_10_1042_BJ20140712
crossref_primary_10_1074_jbc_RA117_001296
crossref_primary_10_12688_f1000research_7046_1
crossref_primary_10_1021_jacs_9b10458
crossref_primary_10_1042_BCJ20220217
crossref_primary_10_1042_BSR20180960
crossref_primary_10_1111_febs_15554
crossref_primary_10_1111_nph_12841
crossref_primary_10_1042_BCJ20160189
crossref_primary_10_1073_pnas_1408987111
crossref_primary_10_3390_ijms17091378
crossref_primary_10_1021_acs_jmedchem_3c00926
crossref_primary_10_7554_eLife_06120
crossref_primary_10_1038_leu_2016_277
crossref_primary_10_1186_s12964_021_00776_1
crossref_primary_10_1126_scisignal_aau5378
crossref_primary_10_1042_BJ20150678
crossref_primary_10_1038_s41420_022_01095_1
crossref_primary_10_1039_C7MT00204A
crossref_primary_10_1016_j_molcel_2020_06_018
crossref_primary_10_1016_j_str_2016_12_008
crossref_primary_10_1186_s12870_019_2160_9
crossref_primary_10_1098_rsob_220350
crossref_primary_10_1016_j_jbc_2023_105350
crossref_primary_10_3389_fendo_2017_00361
crossref_primary_10_1042_BST20160272
crossref_primary_10_3390_catal9090778
crossref_primary_10_1042_BST20150109
crossref_primary_10_1186_s12915_016_0322_x
crossref_primary_10_1517_14728222_2015_1025753
crossref_primary_10_3389_fnmol_2022_1012784
crossref_primary_10_1016_j_str_2015_10_003
crossref_primary_10_18632_oncotarget_12303
crossref_primary_10_1126_scisignal_aau0597
crossref_primary_10_1111_febs_15096
crossref_primary_10_1086_715237
crossref_primary_10_1039_C8RA08246D
crossref_primary_10_1074_jbc_M116_748897
crossref_primary_10_1016_j_tcb_2014_03_008
crossref_primary_10_1111_febs_13504
crossref_primary_10_1016_j_cyto_2015_10_015
crossref_primary_10_1038_s41573_019_0018_3
crossref_primary_10_1038_cdd_2014_70
crossref_primary_10_1042_BCJ20180265
crossref_primary_10_1042_BCJ20180266
crossref_primary_10_1016_j_tcb_2016_11_002
crossref_primary_10_1038_s41467_021_27032_x
crossref_primary_10_1007_s00018_022_04301_6
crossref_primary_10_1111_febs_15246
crossref_primary_10_7554_eLife_32271
crossref_primary_10_1002_pro_3519
crossref_primary_10_1038_s41467_017_00483_x
crossref_primary_10_1038_s41467_021_23474_5
crossref_primary_10_1038_s42003_021_02631_y
crossref_primary_10_1042_BSR20220352
crossref_primary_10_1016_j_jaci_2018_12_1023
crossref_primary_10_1042_BST20160331
crossref_primary_10_21769_BioProtoc_1135
crossref_primary_10_1016_j_celrep_2019_08_055
crossref_primary_10_1371_journal_pgen_1004991
crossref_primary_10_1021_acs_biochem_0c00714
crossref_primary_10_1172_JCI87545
crossref_primary_10_1002_prot_26271
crossref_primary_10_1016_j_str_2017_12_012
crossref_primary_10_1002_embr_201337970
crossref_primary_10_1111_ejh_13137
crossref_primary_10_1002_prot_25981
crossref_primary_10_1371_journal_pone_0135748
crossref_primary_10_3390_ijms22158211
crossref_primary_10_1016_j_str_2015_10_020
crossref_primary_10_1093_molbev_msab272
crossref_primary_10_1016_j_str_2020_07_016
crossref_primary_10_1038_s41598_019_44542_3
crossref_primary_10_1042_BST20160327
crossref_primary_10_1038_s41467_020_16823_3
crossref_primary_10_1080_08977194_2019_1626380
crossref_primary_10_1101_cshperspect_a036376
crossref_primary_10_1021_acs_jproteome_5b00282
crossref_primary_10_1126_scisignal_aaz5599
crossref_primary_10_1038_s41388_018_0670_9
crossref_primary_10_1038_srep14602
crossref_primary_10_1016_j_sbi_2023_102665
crossref_primary_10_1038_cdd_2015_169
crossref_primary_10_1038_s41467_021_22400_z
crossref_primary_10_1042_BCJ20160991
crossref_primary_10_1042_BSR20150226
crossref_primary_10_1002_ijc_28879
crossref_primary_10_1042_BCJ20200496
crossref_primary_10_1016_j_cbpa_2017_12_013
crossref_primary_10_1126_scisignal_aat7951
crossref_primary_10_1073_pnas_1504232112
crossref_primary_10_1126_scisignal_aaf3572
crossref_primary_10_1016_j_bioorg_2020_104381
crossref_primary_10_1042_BCJ20160648
crossref_primary_10_1128_JVI_01835_18
crossref_primary_10_1002_iub_2241
crossref_primary_10_3390_ph16010075
crossref_primary_10_1038_s41467_021_21191_7
ContentType Journal Article
DBID CGR
CUY
CVF
ECM
EIF
NPM
DOI 10.1042/BJ20131174
DatabaseName Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
DatabaseTitle MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
DatabaseTitleList MEDLINE
Database_xml – sequence: 1
  dbid: NPM
  name: PubMed
  url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 2
  dbid: EIF
  name: MEDLINE
  url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search
  sourceTypes: Index Database
DeliveryMethod no_fulltext_linktorsrc
Discipline Anatomy & Physiology
Chemistry
EISSN 1470-8728
ExternalDocumentID 24107129
Genre Research Support, U.S. Gov't, Non-P.H.S
Research Support, Non-U.S. Gov't
Journal Article
Research Support, N.I.H., Extramural
GrantInformation_xml – fundername: NIGMS NIH HHS
  grantid: R01 GM109176
– fundername: NIAID NIH HHS
  grantid: AI73756
– fundername: NHLBI NIH HHS
  grantid: R01 HL058758
– fundername: Medical Research Council
  grantid: G120/1030
– fundername: NIAID NIH HHS
  grantid: R01 AI073756
– fundername: NHLBI NIH HHS
  grantid: R01 HL58758
GroupedDBID ---
-DZ
-~X
0R~
23N
2WC
4.4
53G
5GY
5RE
5VS
6J9
79B
A8Z
AABGO
AAHRG
ABPPZ
ABRJW
ACGFO
ACGFS
ACNCT
ADBBV
AEGXH
AENEX
AIAGR
AIZAD
ALMA_UNASSIGNED_HOLDINGS
BAWUL
CGR
CS3
CUY
CVF
DU5
E3Z
EBD
EBS
ECM
EIF
EJD
EMOBN
ESTFP
F5P
H13
HH6
HZ~
K-O
L7B
ML-
MV1
N9A
NPM
NTEUP
O9-
OK1
P2P
RHI
RNS
RPM
RPO
SV3
TR2
TWZ
WH7
XSW
Y6R
YNY
~02
~KM
ID FETCH-LOGICAL-c419t-fb888c33d6d787d2509f9c9f4c8beb235a475f60e522935fcff869aca34d777e2
IngestDate Sat Sep 28 08:29:10 EDT 2024
IsDoiOpenAccess false
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 2
Language English
LinkModel OpenURL
MergedId FETCHMERGED-LOGICAL-c419t-fb888c33d6d787d2509f9c9f4c8beb235a475f60e522935fcff869aca34d777e2
OpenAccessLink https://europepmc.org/articles/pmc5679212?pdf=render
PMID 24107129
ParticipantIDs pubmed_primary_24107129
PublicationCentury 2000
PublicationDate 2014-Jan-15
PublicationDateYYYYMMDD 2014-01-15
PublicationDate_xml – month: 01
  year: 2014
  text: 2014-Jan-15
  day: 15
PublicationDecade 2010
PublicationPlace England
PublicationPlace_xml – name: England
PublicationTitle Biochemical journal
PublicationTitleAlternate Biochem J
PublicationYear 2014
SSID ssj0014040
Score 2.585335
Snippet Protein kinase-like domains that lack conserved residues known to catalyse phosphoryl transfer, termed pseudokinases, have emerged as important signalling...
SourceID pubmed
SourceType Index Database
StartPage 323
SubjectTerms Amino Acid Sequence
Animals
Cell Line
Humans
Insecta
Janus Kinase 2 - chemistry
Janus Kinase 2 - classification
Janus Kinase 2 - genetics
Molecular Sequence Data
Protein Binding - physiology
Real-Time Polymerase Chain Reaction - methods
Receptor, ErbB-3 - chemistry
Receptor, ErbB-3 - classification
Receptor, ErbB-3 - genetics
Title A robust methodology to subclassify pseudokinases based on their nucleotide-binding properties
URI https://www.ncbi.nlm.nih.gov/pubmed/24107129
Volume 457
hasFullText
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1bS91AEF6O9aF9Ka22tVf2ofTlEGuS3VweD9IigoJWwafKXmYh1JMcPAmiv76zl5joaUv1JSRZEkK-L5PZ2ZlvCPnMtECvVZkoAS4jPBKR5NxEQuQqFixXzPU6PDjM9k7Z_hk_m0zGWUtdK7fVzR_rSh6DKp5DXG2V7AOQvb0pnsB9xBe3iDBu_wvj2fSykd2yDX2gvZwSOpPLTirrFVfmerpYQqebX1WNv6vl1P609LBAUFs146atNNgZsvaV6c3C5lqH3MJ-vbeynbW8tMD40e5A5TJuh_DqbSz6CO97BdWKgfkh5h1cDItBxwC-zWPI5Q8VESEmEds8lshXZW6Dt6Ms30FDG-q-g6FlXoo6MCoZmc3U1xyvmHO0KDZJfT9xqkC-nc8I18XcAYtOCDpKPnDy79F70tr90BpZywvb9-PQhnrCEhRD89br2bLk6_AQVj86XHhvLuJ8kpMX5HmYTNCZZ8ZLMoF6g2zOatE282v6hbr0XseKDfJ0t2_tt0l-zqgnDh0Rh7YNHRGH3iEOdcShTU0dcegqcehAnFfk9Pu3k929KDTaiBSLyzYysigKlaY602i_NXrFpSlVaZgqJMgk5fjRcpPtADrrZcqNMqbISqFEynSe55C8Jk_qpoYtQnG6HieSG5ZIYBmHIs0MXs04B61igLfkjX9j5wuvpnLev8t3fx15T54NJPtA1g1-vvARfcFWfnKY_Qb8yWO8
link.rule.ids 780
linkProvider National Library of Medicine
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=A+robust+methodology+to+subclassify+pseudokinases+based+on+their+nucleotide-binding+properties&rft.jtitle=Biochemical+journal&rft.au=Murphy%2C+James+M&rft.au=Zhang%2C+Qingwei&rft.au=Young%2C+Samuel+N&rft.au=Reese%2C+Michael+L&rft.date=2014-01-15&rft.eissn=1470-8728&rft.volume=457&rft.issue=2&rft.spage=323&rft_id=info:doi/10.1042%2FBJ20131174&rft_id=info%3Apmid%2F24107129&rft_id=info%3Apmid%2F24107129&rft.externalDocID=24107129