Literature DB >> 24881879

Differential adhesion determines the organization of synaptic fascicles in the Drosophila visual system.

Tina Schwabe1, Jolanta A Borycz2, Ian A Meinertzhagen2, Thomas R Clandinin3.   

Abstract

BACKGROUND: Neuronal circuits in worms, flies, and mammals are organized so as to minimize wiring length for a functional number of synaptic connections, a phenomenon called wiring optimization. However, the molecular mechanisms that establish optimal wiring during development are unknown. We addressed this question by studying the role of N-cadherin in the development of optimally wired neurite fascicles in the peripheral visual system of Drosophila.
RESULTS: Photoreceptor axons surround the dendrites of their postsynaptic targets, called lamina cells, within a concentric fascicle called a cartridge. N-cadherin is expressed at higher levels in lamina cells than in photoreceptors, and all genetic manipulations that invert these relative differences displace lamina cells to the periphery and relocate photoreceptor axon terminals into the center.
CONCLUSIONS: Differential expression of a single cadherin is both necessary and sufficient to determine cartridge structure because it positions the most-adhesive elements that make the most synapses at the core and the less-adhesive elements that make fewer synapses at the periphery. These results suggest a general model by which differential adhesion can be utilized to determine the relative positions of axons and dendrites to establish optimal wiring.
Copyright © 2014 Elsevier Ltd. All rights reserved.

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Year:  2014        PMID: 24881879      PMCID: PMC4500537          DOI: 10.1016/j.cub.2014.04.047

Source DB:  PubMed          Journal:  Curr Biol        ISSN: 0960-9822            Impact factor:   10.834


  53 in total

1.  Increased cell bond tension governs cell sorting at the Drosophila anteroposterior compartment boundary.

Authors:  Katharina P Landsberg; Reza Farhadifar; Jonas Ranft; Daiki Umetsu; Thomas J Widmann; Thomas Bittig; Amani Said; Frank Jülicher; Christian Dahmann
Journal:  Curr Biol       Date:  2009-10-29       Impact factor: 10.834

2.  Neuroblast ablation in Drosophila P[GAL4] lines reveals origins of olfactory interneurons.

Authors:  R F Stocker; G Heimbeck; N Gendre; J S de Belle
Journal:  J Neurobiol       Date:  1997-05

3.  The variable transmembrane domain of Drosophila N-cadherin regulates adhesive activity.

Authors:  Shinichi Yonekura; Chun-Yuan Ting; Guilherme Neves; Kimberly Hung; Shu-Ning Hsu; Akira Chiba; Andrew Chess; Chi-Hon Lee
Journal:  Mol Cell Biol       Date:  2006-09       Impact factor: 4.272

4.  The LRR proteins capricious and Tartan mediate cell interactions during DV boundary formation in the Drosophila wing.

Authors:  M Milán; U Weihe; L Pérez; S M Cohen
Journal:  Cell       Date:  2001-09-21       Impact factor: 41.582

5.  Developmental changes in expression, subcellular distribution, and function of Drosophila N-cadherin, guided by a cell-intrinsic program during neuronal differentiation.

Authors:  Mitsuhiko Kurusu; Takeo Katsuki; Kai Zinn; Emiko Suzuki
Journal:  Dev Biol       Date:  2012-04-19       Impact factor: 3.582

6.  Neurite morphogenesis of identified visual interneurons and its relationship to photoreceptor synaptogenesis in the flies, Musca domestica and Drosophila melanogaster.

Authors:  I A Meinertzhagen; S T Piper; X J Sun; A Fröhlich
Journal:  Eur J Neurosci       Date:  2000-04       Impact factor: 3.386

7.  Persistence of coordinated long-term potentiation and dendritic spine enlargement at mature hippocampal CA1 synapses requires N-cadherin.

Authors:  Ozlem Bozdagi; Xiao-bin Wang; Jessica S Nikitczuk; Tonya R Anderson; Erik B Bloss; Glenn L Radice; Qiang Zhou; Deanna L Benson; George W Huntley
Journal:  J Neurosci       Date:  2010-07-28       Impact factor: 6.167

8.  Cadherin-mediated cell adhesion and tissue segregation: qualitative and quantitative determinants.

Authors:  Duke Duguay; Ramsey A Foty; Malcolm S Steinberg
Journal:  Dev Biol       Date:  2003-01-15       Impact factor: 3.582

9.  Synaptic organization of columnar elements in the lamina of the wild type in Drosophila melanogaster.

Authors:  I A Meinertzhagen; S D O'Neil
Journal:  J Comp Neurol       Date:  1991-03-08       Impact factor: 3.215

10.  Contributions of the 12 neuron classes in the fly lamina to motion vision.

Authors:  John C Tuthill; Aljoscha Nern; Stephen L Holtz; Gerald M Rubin; Michael B Reiser
Journal:  Neuron       Date:  2013-07-10       Impact factor: 17.173

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  23 in total

1.  N-Cadherin Orchestrates Self-Organization of Neurons within a Columnar Unit in the Drosophila Medulla.

Authors:  Olena Trush; Chuyan Liu; Xujun Han; Yasuhiro Nakai; Rie Takayama; Hideki Murakawa; Jose A Carrillo; Hiroki Takechi; Satoko Hakeda-Suzuki; Takashi Suzuki; Makoto Sato
Journal:  J Neurosci       Date:  2019-06-07       Impact factor: 6.167

Review 2.  Micro-connectomics: probing the organization of neuronal networks at the cellular scale.

Authors:  Manuel Schröter; Ole Paulsen; Edward T Bullmore
Journal:  Nat Rev Neurosci       Date:  2017-02-02       Impact factor: 34.870

3.  A conserved plan for wiring up the fan-shaped body in the grasshopper and Drosophila.

Authors:  George Boyan; Yu Liu; Sat Kartar Khalsa; Volker Hartenstein
Journal:  Dev Genes Evol       Date:  2017-07-27       Impact factor: 0.900

4.  Regulated Alternative Splicing of Drosophila Dscam2 Is Necessary for Attaining the Appropriate Number of Photoreceptor Synapses.

Authors:  Sarah K Kerwin; Joshua Shing Shun Li; Peter G Noakes; Grace Ji-Eun Shin; S Sean Millard
Journal:  Genetics       Date:  2017-12-05       Impact factor: 4.562

5.  Drosophila Sidekick is required in developing photoreceptors to enable visual motion detection.

Authors:  Sergio Astigarraga; Jessica Douthit; Dorota Tarnogorska; Matthew S Creamer; Omer Mano; Damon A Clark; Ian A Meinertzhagen; Jessica E Treisman
Journal:  Development       Date:  2018-02-05       Impact factor: 6.868

6.  Brain Wiring in the Fourth Dimension.

Authors:  Mathias F Wernet; Claude Desplan
Journal:  Cell       Date:  2015-07-02       Impact factor: 41.582

Review 7.  Adhesion Protein Structure, Molecular Affinities, and Principles of Cell-Cell Recognition.

Authors:  Barry Honig; Lawrence Shapiro
Journal:  Cell       Date:  2020-04-30       Impact factor: 41.582

8.  The Developmental Rules of Neural Superposition in Drosophila.

Authors:  Marion Langen; Egemen Agi; Dylan J Altschuler; Lani F Wu; Steven J Altschuler; Peter Robin Hiesinger
Journal:  Cell       Date:  2015-06-25       Impact factor: 41.582

9.  Control of Synaptic Specificity by Establishing a Relative Preference for Synaptic Partners.

Authors:  Chundi Xu; Emma Theisen; Ryan Maloney; Jing Peng; Ivan Santiago; Clarence Yapp; Zachary Werkhoven; Elijah Rumbaut; Bryan Shum; Dorota Tarnogorska; Jolanta Borycz; Liming Tan; Maximilien Courgeon; Tessa Griffin; Raina Levin; Ian A Meinertzhagen; Benjamin de Bivort; Jan Drugowitsch; Matthew Y Pecot
Journal:  Neuron       Date:  2019-07-09       Impact factor: 17.173

Review 10.  Beyond Molecular Codes: Simple Rules to Wire Complex Brains.

Authors:  Bassem A Hassan; P Robin Hiesinger
Journal:  Cell       Date:  2015-10-08       Impact factor: 41.582

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