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Articles, Cellular/Molecular

Protein Tyrosine Phosphatase Receptor Type O Inhibits Trigeminal Axon Growth and Branching by Repressing TrkB and Ret Signaling

Graziana Gatto, Irina Dudanova, Philipp Suetterlin, Alun M. Davies, Uwe Drescher, John L. Bixby and Rüdiger Klein
Journal of Neuroscience 20 March 2013, 33 (12) 5399-5410; DOI: https://doi.org/10.1523/JNEUROSCI.4707-12.2013
Graziana Gatto
1Department of Molecules–Signaling–Development, Max Planck Institute of Neurobiology, D-82152, Martinsried, Germany,
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Irina Dudanova
1Department of Molecules–Signaling–Development, Max Planck Institute of Neurobiology, D-82152, Martinsried, Germany,
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Philipp Suetterlin
2Medical Research Council Centre for Developmental Neurobiology, King's College London, SE1 1UL, London, United Kingdom,
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Alun M. Davies
3School of Biosciences, CF10 3AT, Cardiff, United Kingdom, and
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Uwe Drescher
2Medical Research Council Centre for Developmental Neurobiology, King's College London, SE1 1UL, London, United Kingdom,
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John L. Bixby
4Miami Project to Cure Paralysis, University of Miami Miller School of Medicine, Miami, Florida 33136
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Rüdiger Klein
1Department of Molecules–Signaling–Development, Max Planck Institute of Neurobiology, D-82152, Martinsried, Germany,
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Abstract

Axonal branches of the trigeminal ganglion (TG) display characteristic growth and arborization patterns during development. Subsets of TG neurons express different receptors for growth factors, but these are unlikely to explain the unique patterns of axonal arborizations. Intrinsic modulators may restrict or enhance cellular responses to specific ligands and thereby contribute to the development of axon growth patterns. Protein tyrosine phosphatase receptor type O (PTPRO), which is required for Eph receptor-dependent retinotectal development in chick and for development of subsets of trunk sensory neurons in mouse, may be such an intrinsic modulator of TG neuron development. PTPRO is expressed mainly in TrkB-expressing (TrkB+) and Ret+ mechanoreceptors within the TG during embryogenesis. In PTPRO mutant mice, subsets of TG neurons grow longer and more elaborate axonal branches. Cultured PTPRO−/− TG neurons display enhanced axonal outgrowth and branching in response to BDNF and GDNF compared with control neurons, indicating that PTPRO negatively controls the activity of BDNF/TrkB and GDNF/Ret signaling. Mouse PTPRO fails to regulate Eph signaling in retinocollicular development and in hindlimb motor axon guidance, suggesting that chick and mouse PTPRO have different substrate specificities. PTPRO has evolved to fine tune growth factor signaling in a cell-type-specific manner and to thereby increase the diversity of signaling output of a limited number of receptor tyrosine kinases to control the branch morphology of developing sensory neurons. The regulation of Eph receptor-mediated developmental processes by protein tyrosine phosphatases has diverged between chick and mouse.

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The Journal of Neuroscience: 33 (12)
Journal of Neuroscience
Vol. 33, Issue 12
20 Mar 2013
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Protein Tyrosine Phosphatase Receptor Type O Inhibits Trigeminal Axon Growth and Branching by Repressing TrkB and Ret Signaling
Graziana Gatto, Irina Dudanova, Philipp Suetterlin, Alun M. Davies, Uwe Drescher, John L. Bixby, Rüdiger Klein
Journal of Neuroscience 20 March 2013, 33 (12) 5399-5410; DOI: 10.1523/JNEUROSCI.4707-12.2013

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Protein Tyrosine Phosphatase Receptor Type O Inhibits Trigeminal Axon Growth and Branching by Repressing TrkB and Ret Signaling
Graziana Gatto, Irina Dudanova, Philipp Suetterlin, Alun M. Davies, Uwe Drescher, John L. Bixby, Rüdiger Klein
Journal of Neuroscience 20 March 2013, 33 (12) 5399-5410; DOI: 10.1523/JNEUROSCI.4707-12.2013
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