Non-catalytic signaling by pseudokinase ILK for regulating cell adhesion
Abstract
Dynamic communication between integrin-containing complexes (focal adhesions, FAs) and actin filaments is critical for regulating cell adhesion. Pseudokinase ILK plays a key role in this process but the underlying mechanism remains highly elusive. Here in this paper we show that by recruiting FA adaptors PINCH and Parvin into a heterotrimeric complex (IPP), ILK triggers F-actin filament bundling – a process known to generate force/mechanical signal to promote cytoskeleton reassembly and dynamic cell adhesion. Structural, biochemical, and functional analyses revealed that the F-actin bundling is orchestrated by two previously unrecognized WASP-Homology-2 actin binding motifs within IPP, one from PINCH and the other from Parvin. Strikingly, this process is also sensitized to Mg-ATP bound to the pseudoactive site of ILK and its dysregulation severely impairs stress fibers formation, cell spreading, and migration. These data identify a crucial mechanism for ILK, highlighting its uniqueness as a pseudokinase to transduce non-catalytic signal and regulate cell adhesion.
- Authors:
-
- Cleveland Clinic, Cleveland, OH (United States)
- Cleveland Clinic, Cleveland, OH (United States); Case Western Reserve Univ., Cleveland, OH (United States)
- Case Western Reserve Univ., Cleveland, OH (United States)
- Publication Date:
- Research Org.:
- Cleveland Clinic, Cleveland, OH (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1483387
- Grant/Contract Number:
- AC02-06CH11357; HL058758; 1S10RR026820-01
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nature Communications
- Additional Journal Information:
- Journal Volume: 9; Journal Issue: 1; Journal ID: ISSN 2041-1723
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
Citation Formats
Vaynberg, Julia, Fukuda, Koichi, Lu, Fan, Bialkowska, Katarzyna, Chen, Yinghua, Plow, Edward F., and Qin, Jun. Non-catalytic signaling by pseudokinase ILK for regulating cell adhesion. United States: N. p., 2018.
Web. doi:10.1038/s41467-018-06906-7.
Vaynberg, Julia, Fukuda, Koichi, Lu, Fan, Bialkowska, Katarzyna, Chen, Yinghua, Plow, Edward F., & Qin, Jun. Non-catalytic signaling by pseudokinase ILK for regulating cell adhesion. United States. https://doi.org/10.1038/s41467-018-06906-7
Vaynberg, Julia, Fukuda, Koichi, Lu, Fan, Bialkowska, Katarzyna, Chen, Yinghua, Plow, Edward F., and Qin, Jun. Fri .
"Non-catalytic signaling by pseudokinase ILK for regulating cell adhesion". United States. https://doi.org/10.1038/s41467-018-06906-7. https://www.osti.gov/servlets/purl/1483387.
@article{osti_1483387,
title = {Non-catalytic signaling by pseudokinase ILK for regulating cell adhesion},
author = {Vaynberg, Julia and Fukuda, Koichi and Lu, Fan and Bialkowska, Katarzyna and Chen, Yinghua and Plow, Edward F. and Qin, Jun},
abstractNote = {Dynamic communication between integrin-containing complexes (focal adhesions, FAs) and actin filaments is critical for regulating cell adhesion. Pseudokinase ILK plays a key role in this process but the underlying mechanism remains highly elusive. Here in this paper we show that by recruiting FA adaptors PINCH and Parvin into a heterotrimeric complex (IPP), ILK triggers F-actin filament bundling – a process known to generate force/mechanical signal to promote cytoskeleton reassembly and dynamic cell adhesion. Structural, biochemical, and functional analyses revealed that the F-actin bundling is orchestrated by two previously unrecognized WASP-Homology-2 actin binding motifs within IPP, one from PINCH and the other from Parvin. Strikingly, this process is also sensitized to Mg-ATP bound to the pseudoactive site of ILK and its dysregulation severely impairs stress fibers formation, cell spreading, and migration. These data identify a crucial mechanism for ILK, highlighting its uniqueness as a pseudokinase to transduce non-catalytic signal and regulate cell adhesion.},
doi = {10.1038/s41467-018-06906-7},
journal = {Nature Communications},
number = 1,
volume = 9,
place = {United States},
year = {Fri Oct 26 00:00:00 EDT 2018},
month = {Fri Oct 26 00:00:00 EDT 2018}
}
Web of Science
Works referenced in this record:
Regulation of cell adhesion and anchorage-dependent growth by a new β1-integrin-linked protein kinase
journal, January 1996
- Hannigan, Gregory E.; Leung-Hagesteijn, Chungyee; Fitz-Gibbon, Linda
- Nature, Vol. 379, Issue 6560
C. elegans PAT-4/ILK Functions as an Adaptor Protein within Integrin Adhesion Complexes
journal, May 2002
- Mackinnon, A. Craig; Qadota, Hiroshi; Norman, Kenneth R.
- Current Biology, Vol. 12, Issue 10
Integrin-linked kinase (ILK) is required for polarizing the epiblast, cell adhesion, and controlling actin accumulation
journal, April 2003
- Sakai, T.
- Genes & Development, Vol. 17, Issue 7
Emerging roles of pseudokinases
journal, September 2006
- Boudeau, Jérôme; Miranda-Saavedra, Diego; Barton, Geoffrey J.
- Trends in Cell Biology, Vol. 16, Issue 9
Identification of the pertussis toxin-sensitive G proteins in platelets, megakaryocytes, and human erythroleukemia cells
journal, August 1990
- Williams, Ag; Woolkalis, Mj; Poncz, M.
- Blood, Vol. 76, Issue 4
The Structure of α-Parvin CH2-Paxillin LD1 Complex Reveals a Novel Modular Recognition for Focal Adhesion Assembly
journal, May 2008
- Wang, Xiaoxia; Fukuda, Koichi; Byeon, In-Ja
- Journal of Biological Chemistry, Vol. 283, Issue 30
Drosophila Integrin-Linked Kinase Is Required at Sites of Integrin Adhesion to Link the Cytoskeleton to the Plasma Membrane
journal, March 2001
- Zervas, Christos G.; Gregory, Stephen L.; Brown, Nicholas H.
- The Journal of Cell Biology, Vol. 152, Issue 5
Assembly of the PINCH-ILK-CH-ILKBP complex precedes and is essential for localization of each component to cell-matrix adhesion sites
journal, December 2002
- Zhang, Y.
- Journal of Cell Science, Vol. 115, Issue 24
Integration of actin dynamics and cell adhesion by a three-dimensional, mechanosensitive molecular clutch
journal, June 2015
- Case, Lindsay B.; Waterman, Clare M.
- Nature Cell Biology, Vol. 17, Issue 8
Spire and Cordon-bleu: multifunctional regulators of actin dynamics
journal, October 2008
- Renault, Louis; Bugyi, Beáta; Carlier, Marie-France
- Trends in Cell Biology, Vol. 18, Issue 10
The integrin adhesome: from genes and proteins to human disease
journal, March 2014
- Winograd-Katz, Sabina E.; Fässler, Reinhard; Geiger, Benjamin
- Nature Reviews Molecular Cell Biology, Vol. 15, Issue 4
The ILK/PINCH/parvin complex: the kinase is dead, long live the pseudokinase!
journal, December 2009
- Wickström, Sara A.; Lange, Anika; Montanez, Eloi
- The EMBO Journal, Vol. 29, Issue 2
Structure of the LKB1-STRAD-MO25 Complex Reveals an Allosteric Mechanism of Kinase Activation
journal, November 2009
- Zeqiraj, E.; Filippi, B. M.; Deak, M.
- Science, Vol. 326, Issue 5960
ILK: a pseudokinase in the center stage of cell-matrix adhesion and signaling
journal, October 2012
- Qin, Jun; Wu, Chuanyue
- Current Opinion in Cell Biology, Vol. 24, Issue 5
Expression of a Nonpolymerizable Actin Mutant in Sf9 Cells †
journal, September 2004
- Joel, Peteranne B.; Fagnant, Patricia M.; Trybus, Kathleen M.
- Biochemistry, Vol. 43, Issue 36
Integrin-linked kinase is an adaptor with essential functions during mouse development
journal, October 2009
- Lange, Anika; Wickström, Sara A.; Jakobson, Madis
- Nature, Vol. 461, Issue 7266
ILK, PINCH and parvin: the tIPP of integrin signalling
journal, December 2005
- Legate, Kyle R.; Montañez, Eloi; Kudlacek, Oliver
- Nature Reviews Molecular Cell Biology, Vol. 7, Issue 1
Structure of a Bud6/Actin Complex Reveals a Novel WH2-like Actin Monomer Recruitment Motif
journal, August 2015
- Park, Eunyoung; Graziano, Brian R.; Zheng, Wei
- Structure, Vol. 23, Issue 8
Structure of an Ultraweak Protein-Protein Complex and Its Crucial Role in Regulation of Cell Morphology and Motility
journal, February 2005
- Vaynberg, Julia; Fukuda, Tomohiko; Chen, Ka
- Molecular Cell, Vol. 17, Issue 4
A common sense approach to peak picking in two-, three-, and four-dimensional spectra using automatic computer analysis of contour diagrams
journal, December 2011
- Garrett, Daniel S.; Powers, Robert; Gronenborn, Angela M.
- Journal of Magnetic Resonance, Vol. 213, Issue 2
Determining the structures of large proteins and protein complexes by NMR
journal, January 1998
- Clore, G. Marius; Gronenborn, Angela M.
- Trends in Biotechnology, Vol. 16, Issue 1
How integrins control mammary epithelial differentiation: A possible role for the ILK-PINCH-Parvin complex
journal, May 2011
- Rooney, Nicholas; Streuli, Charles H.
- FEBS Letters, Vol. 585, Issue 11
Enhanced CRISPR/Cas9-mediated precise genome editing by improved design and delivery of gRNA, Cas9 nuclease, and donor DNA
journal, January 2017
- Liang, Xiquan; Potter, Jason; Kumar, Shantanu
- Journal of Biotechnology, Vol. 241
Mechanotransduction and extracellular matrix homeostasis
journal, October 2014
- Humphrey, Jay D.; Dufresne, Eric R.; Schwartz, Martin A.
- Nature Reviews Molecular Cell Biology, Vol. 15, Issue 12
Structural Basis of Focal Adhesion Localization of LIM-only Adaptor PINCH by Integrin-linked Kinase
journal, December 2008
- Yang, Yanwu; Wang, Xiaoxia; Hawkins, Cheryl A.
- Journal of Biological Chemistry, Vol. 284, Issue 9
Structure and function of focal adhesions
journal, February 2012
- Wehrle-Haller, Bernhard
- Current Opinion in Cell Biology, Vol. 24, Issue 1
HKL -3000: the integration of data reduction and structure solution – from diffraction images to an initial model in minutes
journal, July 2006
- Minor, Wladek; Cymborowski, Marcin; Otwinowski, Zbyszek
- Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 8
Chemical shift assignments of the catalytic and ATP-binding domain of HK853 from Thermotoga maritime
journal, January 2019
- Zhou, Yuan; Liu, Xinghong; Li, Conggang
- Biomolecular NMR Assignments, Vol. 13, Issue 1
Structure and function of focal adhesions
journal, February 2012
- Wehrle-Haller, Bernhard
- Current Opinion in Cell Biology, Vol. 24, Issue 1
Actin-bound structures of Wiskott-Aldrich syndrome protein (WASP)-homology domain 2 and the implications for filament assembly
journal, November 2005
- Chereau, D.; Kerff, F.; Graceffa, P.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 46
Purification and SAXS Analysis of the Integrin Linked Kinase, PINCH, Parvin (IPP) Heterotrimeric Complex
journal, January 2013
- Stiegler, Amy L.; Grant, Thomas D.; Luft, Joseph R.
- PLoS ONE, Vol. 8, Issue 1
ILK: a pseudokinase in the center stage of cell-matrix adhesion and signaling
journal, October 2012
- Qin, Jun; Wu, Chuanyue
- Current Opinion in Cell Biology, Vol. 24, Issue 5
Refinement of Macromolecular Structures by the Maximum-Likelihood Method
journal, May 1997
- Murshudov, G. N.; Vagin, A. A.; Dodson, E. J.
- Acta Crystallographica Section D Biological Crystallography, Vol. 53, Issue 3
The regulation of integrin-linked kinase in human platelets: evidence for involvement in the regulation of integrin alpha2beta1
journal, August 2004
- Stevens, J. M.; Jordan, P. A.; Sage, T.
- Journal of Thrombosis and Haemostasis, Vol. 2, Issue 8
NMRPipe: A multidimensional spectral processing system based on UNIX pipes
journal, November 1995
- Delaglio, Frank; Grzesiek, Stephan; Vuister, GeertenW.
- Journal of Biomolecular NMR, Vol. 6, Issue 3
A Modular Polycistronic Expression System for Overexpressing Protein Complexes in Escherichia coli
journal, February 2001
- Tan, Song
- Protein Expression and Purification, Vol. 21, Issue 1
Biochemical, Proteomic, Structural, and Thermodynamic Characterizations of Integrin-linked Kinase (ILK): CROSS-VALIDATION OF THE PSEUDOKINASE
journal, April 2011
- Fukuda, Koichi; Knight, James D. R.; Piszczek, Grzegorz
- Journal of Biological Chemistry, Vol. 286, Issue 24
Integration of actin dynamics and cell adhesion by a three-dimensional, mechanosensitive molecular clutch
journal, June 2015
- Case, Lindsay B.; Waterman, Clare M.
- Nature Cell Biology, Vol. 17, Issue 8
The secret life of kinases: insights into non-catalytic signalling functions from pseudokinases
journal, June 2017
- Jacobsen, Annette V.; Murphy, James M.
- Biochemical Society Transactions, Vol. 45, Issue 3
Integrin-linked kinase: a cancer therapeutic target unique among its ILK
journal, January 2005
- Hannigan, Gregory; Troussard, Armelle A.; Dedhar, Shoukat
- Nature Reviews Cancer, Vol. 5, Issue 1
Zebrafish integrin-linked kinase is required in skeletal muscles for strengthening the integrin–ECM adhesion complex
journal, June 2008
- Postel, Ruben; Vakeel, Padmanabhan; Topczewski, Jacek
- Developmental Biology, Vol. 318, Issue 1
Targeted wild-type and jerker espins reveal a novel, WH2-domain-dependent way to make actin bundles in cells
journal, March 2006
- Loomis, Patricia A.; Kelly, Alexander E.; Zheng, Lili
- Journal of Cell Science, Vol. 119, Issue 8
Regulation of cell adhesion and anchorage-dependent growth by a new β1-integrin-linked protein kinase
journal, January 1996
- Hannigan, Gregory E.; Leung-Hagesteijn, Chungyee; Fitz-Gibbon, Linda
- Nature, Vol. 379, Issue 6560
Mechanotransduction and extracellular matrix homeostasis
journal, October 2014
- Humphrey, Jay D.; Dufresne, Eric R.; Schwartz, Martin A.
- Nature Reviews Molecular Cell Biology, Vol. 15, Issue 12
Integrin-linked kinase (ILK) is required for polarizing the epiblast, cell adhesion, and controlling actin accumulation
journal, April 2003
- Sakai, T.
- Genes & Development, Vol. 17, Issue 7
Identification of the pertussis toxin-sensitive G proteins in platelets, megakaryocytes, and human erythroleukemia cells
journal, August 1990
- Williams, Ag; Woolkalis, Mj; Poncz, M.
- Blood, Vol. 76, Issue 4
Integrin Adhesion: When Is a Kinase a Kinase?
journal, May 2002
- Zervas, Christos G.; Brown, Nicholas H.
- Current Biology, Vol. 12, Issue 10
Structure of the LKB1-STRAD-MO25 Complex Reveals an Allosteric Mechanism of Kinase Activation
journal, November 2009
- Zeqiraj, E.; Filippi, B. M.; Deak, M.
- Science, Vol. 326, Issue 5960
CHOPCHOP: a CRISPR/Cas9 and TALEN web tool for genome editing
journal, May 2014
- Montague, Tessa G.; Cruz, José M.; Gagnon, James A.
- Nucleic Acids Research, Vol. 42, Issue W1
Integrin signalling adaptors: not only figurants in the cancer story
journal, November 2010
- Cabodi, Sara; del Pilar Camacho-Leal, Maria; Di Stefano, Paola
- Nature Reviews Cancer, Vol. 10, Issue 12
The oligomeric structures of plant cryptochromes
journal, May 2020
- Shao, Kai; Zhang, Xue; Li, Xu
- Nature Structural & Molecular Biology, Vol. 27, Issue 5
Drosophila Integrin-Linked Kinase Is Required at Sites of Integrin Adhesion to Link the Cytoskeleton to the Plasma Membrane
journal, March 2001
- Zervas, Christos G.; Gregory, Stephen L.; Brown, Nicholas H.
- The Journal of Cell Biology, Vol. 152, Issue 5
Functional plasticity of CH domains
journal, December 2001
- Gimona, Mario; Djinovic-Carugo, Kristina; Kranewitter, Wolfgang J.
- FEBS Letters, Vol. 513, Issue 1
Assembly of the PINCH-ILK-CH-ILKBP complex precedes and is essential for localization of each component to cell-matrix adhesion sites
journal, December 2002
- Zhang, Y.
- Journal of Cell Science, Vol. 115, Issue 24
ILK, PINCH and parvin: the tIPP of integrin signalling
journal, December 2005
- Legate, Kyle R.; Montañez, Eloi; Kudlacek, Oliver
- Nature Reviews Molecular Cell Biology, Vol. 7, Issue 1
How integrins control mammary epithelial differentiation: A possible role for the ILK-PINCH-Parvin complex
journal, May 2011
- Rooney, Nicholas; Streuli, Charles H.
- FEBS Letters, Vol. 585, Issue 11
Identification of the pertussis toxin-sensitive G proteins in platelets, megakaryocytes, and human erythroleukemia cells
journal, August 1990
- Williams, Ag; Woolkalis, Mj; Poncz, M.
- Blood, Vol. 76, Issue 4
Integrin-linked kinase is an adaptor with essential functions during mouse development
journal, October 2009
- Lange, Anika; Wickström, Sara A.; Jakobson, Madis
- Nature, Vol. 461, Issue 7266
PROCHECK: a program to check the stereochemical quality of protein structures
journal, April 1993
- Laskowski, R. A.; MacArthur, M. W.; Moss, D. S.
- Journal of Applied Crystallography, Vol. 26, Issue 2
Targeted wild-type and jerker espins reveal a novel, WH2-domain-dependent way to make actin bundles in cells
journal, March 2006
- Loomis, Patricia A.; Kelly, Alexander E.; Zheng, Lili
- Journal of Cell Science, Vol. 119, Issue 8
The structural basis of integrin-linked kinase-PINCH interactions
journal, December 2008
- Chiswell, B. P.; Zhang, R.; Murphy, J. W.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 52
Expression of a Nonpolymerizable Actin Mutant in Sf9 Cells †
journal, September 2004
- Joel, Peteranne B.; Fagnant, Patricia M.; Trybus, Kathleen M.
- Biochemistry, Vol. 43, Issue 36
The integrin adhesome: from genes and proteins to human disease
journal, March 2014
- Winograd-Katz, Sabina E.; Fässler, Reinhard; Geiger, Benjamin
- Nature Reviews Molecular Cell Biology, Vol. 15, Issue 4
Integrin-linked kinase: a cancer therapeutic target unique among its ILK
journal, January 2005
- Hannigan, Gregory; Troussard, Armelle A.; Dedhar, Shoukat
- Nature Reviews Cancer, Vol. 5, Issue 1
The Pseudoactive Site of ILK Is Essential for Its Binding to α-Parvin and Localization to Focal Adhesions
journal, December 2009
- Fukuda, Koichi; Gupta, Sudhiranjan; Chen, Ka
- Molecular Cell, Vol. 36, Issue 5
The ILK/PINCH/parvin complex: the kinase is dead, long live the pseudokinase!
journal, December 2009
- Wickström, Sara A.; Lange, Anika; Montanez, Eloi
- The EMBO Journal, Vol. 29, Issue 2
Emerging roles of pseudokinases
journal, September 2006
- Boudeau, Jérôme; Miranda-Saavedra, Diego; Barton, Geoffrey J.
- Trends in Cell Biology, Vol. 16, Issue 9
A Modular Polycistronic Expression System for Overexpressing Protein Complexes in Escherichia coli
journal, February 2001
- Tan, Song
- Protein Expression and Purification, Vol. 21, Issue 1
The regulation of integrin-linked kinase in human platelets: evidence for involvement in the regulation of integrin alpha2beta1
journal, August 2004
- Stevens, J. M.; Jordan, P. A.; Sage, T.
- Journal of Thrombosis and Haemostasis, Vol. 2, Issue 8
Spire and Cordon-bleu: multifunctional regulators of actin dynamics
journal, October 2008
- Renault, Louis; Bugyi, Beáta; Carlier, Marie-France
- Trends in Cell Biology, Vol. 18, Issue 10
The WH2 Domain and Actin Nucleation: Necessary but Insufficient
journal, June 2016
- Dominguez, Roberto
- Trends in Biochemical Sciences, Vol. 41, Issue 6
Enhanced CRISPR/Cas9-mediated precise genome editing by improved design and delivery of gRNA, Cas9 nuclease, and donor DNA
journal, January 2017
- Liang, Xiquan; Potter, Jason; Kumar, Shantanu
- Journal of Biotechnology, Vol. 241
Characterisation of IRTKS, a novel IRSp53/MIM family actin regulator with distinct filament bundling properties
journal, April 2007
- Millard, T. H.; Dawson, J.; Machesky, L. M.
- Journal of Cell Science, Vol. 120, Issue 9
TALOS+: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts
journal, June 2009
- Shen, Yang; Delaglio, Frank; Cornilescu, Gabriel
- Journal of Biomolecular NMR, Vol. 44, Issue 4
Zebrafish integrin-linked kinase is required in skeletal muscles for strengthening the integrin–ECM adhesion complex
journal, June 2008
- Postel, Ruben; Vakeel, Padmanabhan; Topczewski, Jacek
- Developmental Biology, Vol. 318, Issue 1
Solution Structure of the Focal Adhesion Adaptor PINCH LIM1 Domain and Characterization of Its Interaction with the Integrin-linked Kinase Ankyrin Repeat Domain
journal, November 2000
- Velyvis, Algirdas; Yang, Yanwu; Wu, Chuanyue
- Journal of Biological Chemistry, Vol. 276, Issue 7
The Pseudoactive Site of ILK Is Essential for Its Binding to α-Parvin and Localization to Focal Adhesions
journal, December 2009
- Fukuda, Koichi; Gupta, Sudhiranjan; Chen, Ka
- Molecular Cell, Vol. 36, Issue 5
Actin-bound structures of Wiskott-Aldrich syndrome protein (WASP)-homology domain 2 and the implications for filament assembly
journal, November 2005
- Chereau, D.; Kerff, F.; Graceffa, P.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 46
The Xplor-NIH NMR molecular structure determination package
journal, January 2003
- Schwieters, Charles D.; Kuszewski, John J.; Tjandra, Nico
- Journal of Magnetic Resonance, Vol. 160, Issue 1
The structural basis of integrin-linked kinase-PINCH interactions
journal, December 2008
- Chiswell, B. P.; Zhang, R.; Murphy, J. W.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 52
MOLREP an Automated Program for Molecular Replacement
journal, December 1997
- Vagin, A.; Teplyakov, A.
- Journal of Applied Crystallography, Vol. 30, Issue 6, p. 1022-1025
Structure of a Bud6/Actin Complex Reveals a Novel WH2-like Actin Monomer Recruitment Motif
journal, August 2015
- Park, Eunyoung; Graziano, Brian R.; Zheng, Wei
- Structure, Vol. 23, Issue 8
A common sense approach to peak picking in two-, three-, and four-dimensional spectra using automatic computer analysis of contour diagrams
journal, October 1991
- Garrett, Daniel S.; Powers, Robert; Gronenborn, Angela M.
- Journal of Magnetic Resonance (1969), Vol. 95, Issue 1
Multi-functionality of a tryptophan residue conserved in substrate-binding groove of GH19 chitinases
journal, January 2021
- Nagata, Takuya; Shinya, Shoko; Ohnuma, Takayuki
- Scientific Reports, Vol. 11, Issue 1
Receptor and G protein-mediated responses to thrombin in HEL cells.
journal, January 1991
- Brass, L. F.; Manning, D. R.; Williams, A. G.
- Journal of Biological Chemistry, Vol. 266, Issue 2
Works referencing / citing this record:
Cell Adhesion by Integrins
journal, October 2019
- Bachmann, Michael; Kukkurainen, Sampo; Hytönen, Vesa P.
- Physiological Reviews, Vol. 99, Issue 4
Identification of ILK as a critical regulator of VEGFR 3 signalling and lymphatic vascular growth
journal, December 2018
- Urner, Sofia; Planas‐Paz, Lara; Hilger, Laura Sophie
- The EMBO Journal, Vol. 38, Issue 2
Genetic Animal Models for Arrhythmogenic Cardiomyopathy
journal, June 2020
- Gerull, Brenda; Brodehl, Andreas
- Frontiers in Physiology, Vol. 11
Identification of ILK as a critical regulator of VEGFR 3 signalling and lymphatic vascular growth
journal, December 2018
- Urner, Sofia; Planas‐Paz, Lara; Hilger, Laura Sophie
- The EMBO Journal, Vol. 38, Issue 2
ILK supports RhoA/ROCK-mediated contractility of human intestinal epithelial crypt cells by inducing the fibrillogenesis of endogenous soluble fibronectin during the spreading process
journal, March 2020
- Gagné, David; Benoit, Yannick D.; Groulx, Jean-François
- BMC Molecular and Cell Biology, Vol. 21, Issue 1
ILK supports RhoA/ROCK-mediated contractility of human intestinal epithelial crypt cells by inducing the fibrillogenesis of endogenous soluble fibronectin during the spreading process
journal, March 2020
- Gagné, David; Benoit, Yannick D.; Groulx, Jean-François
- BMC Molecular and Cell Biology, Vol. 21, Issue 1
Emerging regulators of vascular smooth muscle cell migration
journal, June 2019
- Afewerki, TecLino; Ahmed, Sultan; Warren, Derek
- Journal of Muscle Research and Cell Motility, Vol. 40, Issue 2