Structural Basis for Interactions Between Contactin Family Members and Protein-tyrosine Phosphatase Receptor Type G in Neural Tissues
Abstract
Protein-tyrosine phosphatase receptor type G (RPTPγ/PTPRG) interacts in vitro with contactin-3-6 (CNTN3-6), a group of glycophosphatidylinositol-anchored cell adhesion molecules involved in the wiring of the nervous system. In addition to PTPRG, CNTNs associate with multiple transmembrane proteins and signal inside the cell via cis-binding partners to alleviate the absence of an intracellular region. Here, we use comprehensive biochemical and structural analyses to demonstrate that PTPRG·CNTN3-6 complexes share similar binding affinities and a conserved arrangement. Furthermore, as a first step to identifying PTPRG·CNTN complexes in vivo, we found that PTPRG and CNTN3 associate in the outer segments of mouse rod photoreceptor cells. In particular, PTPRG and CNTN3 form cis-complexes at the surface of photoreceptors yet interact in trans when expressed on the surfaces of apposing cells. Further structural analyses suggest that all CNTN ectodomains adopt a bent conformation and might lie parallel to the cell surface to accommodate these cis and trans binding modes. Taken together, these studies identify a PTPRG·CNTN complex in vivo and provide novel insights into PTPRG- and CNTN-mediated signaling.
- Authors:
-
- Univ. of Missouri, Kansas City, MO (United States)
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Inst. Pasteur de Paris (France); Univ. Paris Diderot (France)
- Univ. Paris Diderot (France)
- Univ. of Missouri, Kansas City, MO (United States). School of Medicine
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1408402
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Journal of Biological Chemistry
- Additional Journal Information:
- Journal Volume: 291; Journal Issue: 41; Journal ID: ISSN 0021-9258
- Publisher:
- American Society for Biochemistry and Molecular Biology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Nikolaienko, Roman M., Hammel, Michal, Dubreuil, Véronique, Zalmai, Rana, Hall, David R., Mehzabeen, Nurjahan, Karuppan, Sebastian J., Harroch, Sheila, Stella, Salvatore L., and Bouyain, Samuel. Structural Basis for Interactions Between Contactin Family Members and Protein-tyrosine Phosphatase Receptor Type G in Neural Tissues. United States: N. p., 2016.
Web. doi:10.1074/jbc.M116.742163.
Nikolaienko, Roman M., Hammel, Michal, Dubreuil, Véronique, Zalmai, Rana, Hall, David R., Mehzabeen, Nurjahan, Karuppan, Sebastian J., Harroch, Sheila, Stella, Salvatore L., & Bouyain, Samuel. Structural Basis for Interactions Between Contactin Family Members and Protein-tyrosine Phosphatase Receptor Type G in Neural Tissues. United States. https://doi.org/10.1074/jbc.M116.742163
Nikolaienko, Roman M., Hammel, Michal, Dubreuil, Véronique, Zalmai, Rana, Hall, David R., Mehzabeen, Nurjahan, Karuppan, Sebastian J., Harroch, Sheila, Stella, Salvatore L., and Bouyain, Samuel. Thu .
"Structural Basis for Interactions Between Contactin Family Members and Protein-tyrosine Phosphatase Receptor Type G in Neural Tissues". United States. https://doi.org/10.1074/jbc.M116.742163. https://www.osti.gov/servlets/purl/1408402.
@article{osti_1408402,
title = {Structural Basis for Interactions Between Contactin Family Members and Protein-tyrosine Phosphatase Receptor Type G in Neural Tissues},
author = {Nikolaienko, Roman M. and Hammel, Michal and Dubreuil, Véronique and Zalmai, Rana and Hall, David R. and Mehzabeen, Nurjahan and Karuppan, Sebastian J. and Harroch, Sheila and Stella, Salvatore L. and Bouyain, Samuel},
abstractNote = {Protein-tyrosine phosphatase receptor type G (RPTPγ/PTPRG) interacts in vitro with contactin-3-6 (CNTN3-6), a group of glycophosphatidylinositol-anchored cell adhesion molecules involved in the wiring of the nervous system. In addition to PTPRG, CNTNs associate with multiple transmembrane proteins and signal inside the cell via cis-binding partners to alleviate the absence of an intracellular region. Here, we use comprehensive biochemical and structural analyses to demonstrate that PTPRG·CNTN3-6 complexes share similar binding affinities and a conserved arrangement. Furthermore, as a first step to identifying PTPRG·CNTN complexes in vivo, we found that PTPRG and CNTN3 associate in the outer segments of mouse rod photoreceptor cells. In particular, PTPRG and CNTN3 form cis-complexes at the surface of photoreceptors yet interact in trans when expressed on the surfaces of apposing cells. Further structural analyses suggest that all CNTN ectodomains adopt a bent conformation and might lie parallel to the cell surface to accommodate these cis and trans binding modes. Taken together, these studies identify a PTPRG·CNTN complex in vivo and provide novel insights into PTPRG- and CNTN-mediated signaling.},
doi = {10.1074/jbc.M116.742163},
journal = {Journal of Biological Chemistry},
number = 41,
volume = 291,
place = {United States},
year = {Thu Aug 18 00:00:00 EDT 2016},
month = {Thu Aug 18 00:00:00 EDT 2016}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 25 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Shape Complementarity at Protein/Protein Interfaces
journal, December 1993
- Lawrence, Michael C.; Colman, Peter M.
- Journal of Molecular Biology, Vol. 234, Issue 4
Uniqueness of ab initio shape determination in small-angle scattering
journal, April 2003
- Volkov, Vladimir V.; Svergun, Dmitri I.
- Journal of Applied Crystallography, Vol. 36, Issue 3, p. 860-864
Neurofascin Is a Glial Receptor for the Paranodin/Caspr-Contactin Axonal Complex at the Axoglial Junction
journal, February 2002
- Charles, Perrine; Tait, Steven; Faivre-Sarrailh, Catherine
- Current Biology, Vol. 12, Issue 3
Overview of the CCP 4 suite and current developments
journal, March 2011
- Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D.
- Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4
DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering
journal, January 2009
- Franke, Daniel; Svergun, Dmitri I.
- Journal of Applied Crystallography, Vol. 42, Issue 2, p. 342-346
Contactins: Emerging key roles in the development and function of the nervous system
journal, January 2009
- Shimoda, Yasushi; Watanabe, Kazutada
- Cell Adhesion & Migration, Vol. 3, Issue 1
Structural Model and trans-Interaction of the Entire Ectodomain of the Olfactory Cell Adhesion Molecule
journal, February 2011
- Kulahin, Nikolaj; Kristensen, Ole; Rasmussen, Kim K.
- Structure, Vol. 19, Issue 2
The Crystal Structure of the α-Neurexin-1 Extracellular Region Reveals a Hinge Point for Mediating Synaptic Adhesion and Function
journal, June 2011
- Miller, Meghan T.; Mileni, Mauro; Comoletti, Davide
- Structure, Vol. 19, Issue 6
Electron tomography of paranodal septate-like junctions and the associated axonal and glial cytoskeletons in the central nervous system
journal, December 2010
- Nans, Andrea; Einheber, Steven; Salzer, James L.
- Journal of Neuroscience Research, Vol. 89, Issue 3
The Structure of Neurexin 1α Reveals Features Promoting a Role as Synaptic Organizer
journal, June 2011
- Chen, Fang; Venugopal, Vandavasi; Murray, Beverly
- Structure, Vol. 19, Issue 6
Advances and pitfalls of protein structural alignment
journal, June 2009
- Hasegawa, Hitomi; Holm, Liisa
- Current Opinion in Structural Biology, Vol. 19, Issue 3
Contactin-4 Mediates Axon-Target Specificity and Functional Development of the Accessory Optic System
journal, May 2015
- Osterhout, Jessica A.; Stafford, Benjamin K.; Nguyen, Phong L.
- Neuron, Vol. 86, Issue 4
BIG-1: A new TAG-1/F3-related member of the immunoglobulin superfamily with neurite outgrowth-promoting activity
journal, August 1994
- Yoshihara, Yoshihiro; Kawasaki, Miwa; Tani, Akiko
- Neuron, Vol. 13, Issue 2
Accurate SAXS Profile Computation and its Assessment by Contrast Variation Experiments
journal, August 2013
- Schneidman-Duhovny, Dina; Hammel, Michal; Tainer, John A.
- Biophysical Journal, Vol. 105, Issue 4
A mechanistic basis for converting a receptor tyrosine kinase agonist to an antagonist
journal, September 2007
- Tolbert, W. D.; Daugherty, J.; Gao, C.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 37
A time- and cost-efficient system for high-level protein production in mammalian cells
journal, September 2006
- Aricescu, A. Radu; Lu, Weixian; Jones, E. Yvonne
- Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 10
Deficiency of neural recognition molecule NB-2 affects the development of glutamatergic auditory pathways from the ventral cochlear nucleus to the superior olivary complex in mouse
journal, December 2009
- Toyoshima, Manabu; Sakurai, Kunie; Shimazaki, Kuniko
- Developmental Biology, Vol. 336, Issue 2
Molecular Mechanisms of Synaptic Specificity in Developing Neural Circuits
journal, October 2010
- Williams, Megan E.; de Wit, Joris; Ghosh, Anirvan
- Neuron, Vol. 68, Issue 1
The HSPGs Syndecan and Dallylike Bind the Receptor Phosphatase LAR and Exert Distinct Effects on Synaptic Development
journal, February 2006
- Johnson, Karl G.; Tenney, Alan P.; Ghose, Aurnab
- Neuron, Vol. 49, Issue 4
Inference of Macromolecular Assemblies from Crystalline State
journal, September 2007
- Krissinel, Evgeny; Henrick, Kim
- Journal of Molecular Biology, Vol. 372, Issue 3
UCSF Chimera?A visualization system for exploratory research and analysis
journal, January 2004
- Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C.
- Journal of Computational Chemistry, Vol. 25, Issue 13
Neuropilins lock secreted semaphorins onto plexins in a ternary signaling complex
journal, October 2012
- Janssen, Bert J. C.; Malinauskas, Tomas; Weir, Greg A.
- Nature Structural & Molecular Biology, Vol. 19, Issue 12
Robust, high-throughput solution structural analyses by small angle X-ray scattering (SAXS)
journal, July 2009
- Hura, Greg L.; Menon, Angeli L.; Hammel, Michal
- Nature Methods, Vol. 6, Issue 8
No Obvious Abnormality in Mice Deficient in Receptor Protein Tyrosine Phosphatase beta
journal, October 2000
- Harroch, S.; Palmeri, M.; Rosenbluth, J.
- Molecular and Cellular Biology, Vol. 20, Issue 20
BIG-2 Mediates Olfactory Axon Convergence to Target Glomeruli
journal, March 2008
- Kaneko-Goto, Tomomi; Yoshihara, Sei-ichi; Miyazaki, Haruko
- Neuron, Vol. 57, Issue 6
Interaction of amyloid precursor protein with contactins and NgCAM in the retinotectal system
journal, February 2008
- Osterfield, M.; Egelund, R.; Young, L. M.
- Development, Vol. 135, Issue 6
Modulation of Rod Photoreceptor Cyclic Nucleotide-Gated Channels by Tyrosine Phosphorylation
journal, December 1997
- Molokanova, Elena; Trivedi, Bhavya; Savchenko, Alexei
- The Journal of Neuroscience, Vol. 17, Issue 23
Receptor protein tyrosine phosphatases are expressed by cycling retinal progenitor cells and involved in neuronal development of mouse retina
journal, March 2008
- Horvat-Bröcker, A.; Reinhard, J.; Illes, S.
- Neuroscience, Vol. 152, Issue 3
Neuronal Ig/Caspr Recognition Promotes the Formation of Axoaxonic Synapses in Mouse Spinal Cord
journal, January 2014
- Ashrafi, Soha; Betley, J. Nicholas; Comer, John D.
- Neuron, Vol. 81, Issue 1
Distribution of different isoforms of receptor protein tyrosine phosphatase γ (Ptprg-RPTP γ) in adult mouse brain: upregulation during neuroinflammation
journal, March 2013
- Lorenzetto, Erika; Moratti, Elisabetta; Vezzalini, Marzia
- Brain Structure and Function, Vol. 219, Issue 3
Proteoglycan-Specific Molecular Switch for RPTP Clustering and Neuronal Extension
journal, March 2011
- Coles, C. H.; Shen, Y.; Tenney, A. P.
- Science, Vol. 332, Issue 6028
Receptor protein tyrosine phosphatases regulate neural development and axon guidance
journal, November 2004
- Ensslen-Craig, Sonya E.; Brady-Kalnay, Susann M.
- Developmental Biology, Vol. 275, Issue 1
Growth factors regulate phototransduction in retinal rods by modulating cyclic nucleotide-gated channels through dephosphorylation of a specific tyrosine residue
journal, April 2001
- Savchenko, A.; Kraft, T. W.; Molokanova, E.
- Proceedings of the National Academy of Sciences, Vol. 98, Issue 10
Receptor Protein Tyrosine Phosphatase Is a Marker for Pyramidal Cells and Sensory Neurons in the Nervous System and Is Not Necessary for Normal Development
journal, June 2006
- Lamprianou, S.; Vacaresse, N.; Suzuki, Y.
- Molecular and Cellular Biology, Vol. 26, Issue 13
Synaptic formation in subsets of glutamatergic terminals in the mouse hippocampal formation is affected by a deficiency in the neural cell recognition molecule NB-3
journal, April 2010
- Sakurai, Kunie; Toyoshima, Manabu; Takeda, Yasuo
- Neuroscience Letters, Vol. 473, Issue 2
A Contactin–Receptor-Like Protein Tyrosine Phosphatase β Complex Mediates Adhesive Communication Between Astroglial Cells and Gonadotrophin-Releasing Hormone Neurones
journal, November 2007
- Parent, A. -S.; Mungenast, A. E.; Lomniczi, A.
- Journal of Neuroendocrinology, Vol. 19, Issue 11
Coot model-building tools for molecular graphics
journal, November 2004
- Emsley, Paul; Cowtan, Kevin
- Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132
Transient Mammalian Cell Transfection with Polyethylenimine (PEI)
book, January 2013
- Longo, Patti A.; Kavran, Jennifer M.; Kim, Min-Sung
- Methods in Enzymology
Structural basis for extracellular cis and trans RPTPσ signal competition in synaptogenesis
journal, November 2014
- Coles, Charlotte H.; Mitakidis, Nikolaos; Zhang, Peng
- Nature Communications, Vol. 5, Issue 1
A cis-complex of NB-2/contactin-5 with amyloid precursor-like protein 1 is localized on the presynaptic membrane
journal, February 2012
- Shimoda, Yasushi; Koseki, Fumiya; Itoh, Masaki
- Neuroscience Letters, Vol. 510, Issue 2
VE-PTP regulates VEGFR2 activity in stalk cells to establish endothelial cell polarity and lumen formation
journal, April 2013
- Hayashi, Makoto; Majumdar, Arindam; Li, Xiujuan
- Nature Communications, Vol. 4, Issue 1
Fiji: an open-source platform for biological-image analysis
journal, June 2012
- Schindelin, Johannes; Arganda-Carreras, Ignacio; Frise, Erwin
- Nature Methods, Vol. 9, Issue 7
PHENIX: a comprehensive Python-based system for macromolecular structure solution
journal, January 2010
- Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221
Crystal structure of Caenorhabditis elegans HER-1 and characterization of the interaction between HER-1 and TRA-2A
journal, August 2004
- Hamaoka, B. Y.; Dann, C. E.; Geisbrecht, B. V.
- Proceedings of the National Academy of Sciences, Vol. 101, Issue 32
Ephrin-Mediated cis-Attenuation of Eph Receptor Signaling Is Essential for Spinal Motor Axon Guidance
journal, July 2011
- Kao, Tzu-Jen; Kania, Artur
- Neuron, Vol. 71, Issue 1
Contactins
book, January 2011
- Zuko, Amila; Bouyain, Samuel; van der Zwaag, Bert
- Advances in Protein Chemistry and Structural Biology
Structural basis for Notch1 engagement of Delta-like 4
journal, February 2015
- Luca, V. C.; Jude, K. M.; Pierce, N. W.
- Science, Vol. 347, Issue 6224
Direct observation of individual endogenous protein complexes in situ by proximity ligation
journal, October 2006
- Söderberg, Ola; Gullberg, Mats; Jarvius, Malin
- Nature Methods, Vol. 3, Issue 12, p. 995-1000
A complex between contactin-1 and the protein tyrosine phosphatase PTPRZ controls the development of oligodendrocyte precursor cells
journal, October 2011
- Lamprianou, S.; Chatzopoulou, E.; Thomas, J. -L.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 42
Structure-based mutagenesis of the substrate-recognition domain of Nrdp1/FLRF identifies the binding site for the receptor tyrosine kinase ErbB3
journal, February 2007
- Bouyain, S.; Leahy, D. J.
- Protein Science, Vol. 16, Issue 4
Cis–trans interactions of cell surface receptors: biological roles and structural basis
journal, August 2011
- Held, Werner; Mariuzza, Roy A.
- Cellular and Molecular Life Sciences, Vol. 68, Issue 21
Upgrading SELEX Technology by Using Lambda Exonuclease Digestion for Single-Stranded DNA Generation
journal, December 2009
- Avci-Adali, Meltem; Paul, Angel; Wilhelm, Nadj
- Molecules, Vol. 15, Issue 1
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
Activity-Dependent Modulation of Rod Photoreceptor Cyclic Nucleotide-Gated Channels Mediated by Phosphorylation of a Specific Tyrosine Residue
journal, June 1999
- Molokanova, Elena; Maddox, Floyd; Luetje, Charles W.
- The Journal of Neuroscience, Vol. 19, Issue 12
The protein tyrosine phosphatases PTPRZ and PTPRG bind to distinct members of the contactin family of neural recognition molecules
journal, January 2010
- Bouyain, S.; Watkins, D. J.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 6
Identification of a carbonic anhydrase-like domain in the extracellular region of RPTP gamma defines a new subfamily of receptor tyrosine phosphatases.
journal, March 1993
- Barnea, G.; Silvennoinen, O.; Shaanan, B.
- Molecular and Cellular Biology, Vol. 13, Issue 3
Phaser crystallographic software
journal, July 2007
- McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D.
- Journal of Applied Crystallography, Vol. 40, Issue 4
Association of Shank 1A Scaffolding Protein with Cone Photoreceptor Terminals in the Mammalian Retina
journal, September 2012
- Stella, Salvatore L.; Vila, Alejandro; Hung, Albert Y.
- PLoS ONE, Vol. 7, Issue 9
Neural recognition molecules CHL1 and NB-3 regulate apical dendrite orientation in the neocortex via PTPα
journal, November 2007
- Ye, Haihong; Tan, Yen Ling Jessie; Ponniah, Sathivel
- The EMBO Journal, Vol. 27, Issue 1
[20] Processing of X-ray diffraction data collected in oscillation mode
book, January 1997
- Otwinowski, Zbyszek; Minor, Wladek
- Macromolecular Crystallography Part A, 307-326
Works referencing / citing this record:
Architecture of cell–cell adhesion mediated by sidekicks
journal, August 2018
- Tang, Hua; Chang, Haishuang; Dong, Yue
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 37
Affinity capture of polyribosomes followed by RNAseq (ACAPseq), a discovery platform for protein-protein interactions
journal, October 2018
- Peng, Xi; Emiliani, Francesco; Smallwood, Philip M.
- eLife, Vol. 7
Genetic study links components of the autonomous nervous system to heart-rate profile during exercise
journal, March 2018
- Verweij, Niek; van de Vegte, Yordi J.; van der Harst, Pim
- Nature Communications, Vol. 9, Issue 1
Keratan sulfate ( KS )‐proteoglycans and neuronal regulation in health and disease: the importance of KS ‐glycodynamics and interactive capability with neuroregulatory ligands
journal, January 2019
- Melrose, James
- Journal of Neurochemistry, Vol. 149, Issue 2
Latrophilin’s Social Protein Network
journal, June 2019
- Burbach, J. Peter H.; Meijer, Dimphna H.
- Frontiers in Neuroscience, Vol. 13
Defining the binding interface of Amyloid Precursor Protein (APP) and Contactin3 (CNTN3) by site-directed mutagenesis
journal, July 2019
- Peng, Xi; Williams, John; Smallwood, Philip M.
- PLOS ONE, Vol. 14, Issue 7
Genetic study links components of the autonomous nervous system to heart-rate profile during exercise
journal, October 2017
- Verweij, Niek; van de Vegte, Yordi; van der Harst, Pim
- Nature Communications