skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: The crystal structure of pseudokinase PEAK1 (Sugen kinase 269) reveals an unusual catalytic cleft and a novel mode of kinase fold dimerization

Journal Article · · Journal of Biological Chemistry
 [1];  [1]
  1. Yale Univ., New Haven, CT (United States)

The pseudokinase group encompasses some 10% of protein kinases, but pseudokinases diverge from canonical kinases in key motifs. The two members of the small new kinase family 3 (NKF3) group are considered pseudokinases. These proteins, pseudopodium-enriched atypical kinase 1 (PEAK1, Sugen kinase 269, or SgK269) and pragmin (Sugen kinase 223 or SgK223), act as scaffolds in growth factor signaling pathways, and both contain a kinase fold with degraded kinase motifs at their C termini. These kinases may harbor regions that mediate oligomerization or control other aspects of signal transduction, but a lack of structural information has precluded detailed investigations into their functional roles. In this study reported herein, we determined the X-ray crystal structure of the PEAK1 pseudokinase domain to 2.3 Å resolution. The structure revealed that the PEAK1 kinase-like domain contains a closed nucleotide-binding cleft that in this conformation may deleteriously affect nucleotide binding. Moreover, we found that N- and C-terminal extensions create a highly unusual all α-helical split-dimerization region, termed here the split helical dimerization (SHED) region. Sequence conservation analysis suggested that this region facilitates a dimerization mode that is conserved between PEAK1 and pragmin. Finally, we observed structural similarities between the PEAK1 SHED region and the C-terminal extension of the Parkinson's disease-associated kinase PINK1. In summary, PEAK1's kinase cleft is occluded, and its newly identified SHED region may promote an unexpected dimerization mode. Similarities of PEAK1 with the active kinase PINK1 may reclassify the latter as a member of the new kinase family 3 group.

Research Organization:
Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
Sponsoring Organization:
National Institutes of Health (NIH)
Grant/Contract Number:
R01NS085078; R01GM109487; R01GM114621; R01GM102262; S10OD018007; GM103403; RR029205.
OSTI ID:
1430318
Journal Information:
Journal of Biological Chemistry, Vol. 293, Issue 5; ISSN 0021-9258
Publisher:
American Society for Biochemistry and Molecular BiologyCopyright Statement
Country of Publication:
United States
Language:
ENGLISH
Citation Metrics:
Cited by: 29 works
Citation information provided by
Web of Science

References (48)

A robust methodology to subclassify pseudokinases based on their nucleotide-binding properties journal December 2013
Structural Basis for Noncanonical Substrate Recognition of Cofilin/ADF Proteins by LIM Kinases journal May 2016
Emerging roles of pseudokinases journal September 2006
eIF5A-PEAK1 Signaling Regulates YAP1/TAZ Protein Expression and Pancreatic Cancer Cell Growth journal April 2017
BALBES : a molecular-replacement pipeline journal December 2007
Live and let die: insights into pseudoenzyme mechanisms from structure journal December 2017
Structure of PINK1 and mechanisms of Parkinson's disease-associated mutations journal October 2017
The proximal signaling network of the BCR-ABL1 oncogene shows a modular organization journal August 2010
Characterization of Size-Fractionated cDNA Libraries Generated by the in vitro Recombination-Assisted Method journal January 2002
Structure of SgK223 pseudokinase reveals novel mechanisms of homotypic and heterotypic association journal October 2017
A Dimeric PINK1-containing Complex on Depolarized Mitochondria Stimulates Parkin Recruitment journal November 2013
ConSurf 2005: the projection of evolutionary conservation scores of residues on protein structures journal July 2005
Quantitative Phosphoproteomics Reveals a Cluster of Tyrosine Kinases That Mediates Src Invasive Activity in Advanced Colon Carcinoma Cells journal March 2009
PDBsum new things journal January 2009
Inference of Macromolecular Assemblies from Crystalline State journal September 2007
Data publication with the structural biology data grid supports live analysis journal March 2016
A Phosphorylated Pseudokinase Complex Controls Cell Wall Synthesis in Mycobacteria journal January 2012
Pseudokinases-remnants of evolution or key allosteric regulators? journal December 2010
Tyrosine Phosphorylation Profiling Reveals the Signaling Network Characteristics of Basal Breast Cancer Cells journal September 2010
KRas Induces a Src/PEAK1/ErbB2 Kinase Amplification Loop That Drives Metastatic Growth and Therapy Resistance in Pancreatic Cancer journal May 2012
Pseudopodium-enriched atypical kinase 1 regulates the cytoskeleton and cancer progression journal June 2010
A Hypusine-eIF5A-PEAK1 Switch Regulates the Pathogenesis of Pancreatic Cancer journal September 2014
PEAK1, a Novel Kinase Target in the Fight Against Cancer journal July 2010
Surface comparison of active and inactive protein kinases identifies a conserved activation mechanism journal November 2006
Dali/FSSP classification of three-dimensional protein folds journal January 1997
Features and development of Coot journal March 2010
Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features journal December 1983
Dynamic Phosphorylation of Tyrosine 665 in Pseudopodium-enriched Atypical Kinase 1 (PEAK1) Is Essential for the Regulation of Cell Migration and Focal Adhesion Turnover journal October 2012
PHENIX: a comprehensive Python-based system for macromolecular structure solution journal January 2010
The Protein Kinase Complement of the Human Genome journal December 2002
Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega journal January 2011
Temporal regulation of EGF signalling networks by the scaffold protein Shc1 journal July 2013
Identification of a PEAK1/ZEB1 signaling axis during TGFβ/fibronectin-induced EMT in breast cancer journal September 2015
The pseudokinase SgK223 promotes invasion of pancreatic ductal epithelial cells through JAK1/Stat3 signaling journal July 2015
p190RhoGAP proteins contain pseudoGTPase domains journal September 2017
Assessing the range of kinase autoinhibition mechanisms in the insulin receptor family journal November 2012
PEAK1 Acts as a Molecular Switch to Regulate Context-Dependent TGFβ Responses in Breast Cancer journal August 2015
Nucleotide-binding mechanisms in pseudokinases journal January 2016
Structure of PINK1 in complex with its substrate ubiquitin journal October 2017
[20] Processing of X-ray diffraction data collected in oscillation mode book January 1997
Surprising similarities in structure comparison journal June 1996
Homo- and Heterotypic Association Regulates Signaling by the SgK269/PEAK1 and SgK223 Pseudokinases journal August 2016
Involvement of Lyn and the Atypical Kinase SgK269/PEAK1 in a Basal Breast Cancer Signaling Pathway journal February 2013
X-Ray Diffraction data from PEAK1 (Sugen Kinase 269, SgK269), source of 6BHC structure dataset January 2017
PARP1 exhibits enhanced association and catalytic efficiency with γH2A.X-nucleosome journal December 2019
Cavin1 intrinsically disordered domains are essential for fuzzy electrostatic interactions and caveola formation journal February 2021
Data publication with the structural biology data grid supports live analysis text January 2016
PHENIX: a comprehensive Python-based system for macromolecular structure solution. text January 2010

Cited By (8)

Pseudopodium-enriched atypical kinase 1 mediates angiogenesis by modulating GATA2-dependent VEGFR2 transcription journal May 2018
Prospects for pharmacological targeting of pseudokinases journal March 2019
PEAK3/C19orf35 pseudokinase, a new NFK3 kinase family member, inhibits CrkII through dimerization journal July 2019
New insights into the structure of PINK1 and the mechanism of ubiquitin phosphorylation journal July 2018
Sequence assignment for low-resolution modelling of protein crystal structures journal July 2019
The PEAK family of pseudokinases, their role in cell signalling and cancer journal November 2019
Emerging concepts in pseudoenzyme classification, evolution, and signaling journal August 2019
Pseudokinases: From Allosteric Regulation of Catalytic Domains and the Formation of Macromolecular Assemblies to Emerging Drug Targets journal September 2019