Skip to main content

Molecular Basis of Lamina-Specific Synaptic Connections in the Retina: Sidekick Immunoglobulin Superfamily Molecules

  • Chapter
  • First Online:
The Sticky Synapse

Abstract

During the development of the nervous system, neurons must assemble a vast network of synaptic connections to form functional neuronal circuits. Each neuron sends axons to reach the general target region and then must choose the appropriate target from a multitude of neurons to make proper connections and to form synapses. How are such specific neuronal connections established? Sidekick proteins (Sdks) are synaptic adhesion molecules of the immunoglobulin (Ig) superfamily that have been suggested to mediate targeting specificity in the synaptic layers in the retina. These cell adhesion molecules, along with their close homologs, Down’s syndrome cell adhesion molecules (DSCAMs), provide a molecular code for lamina-specific synaptic connections that is governed by homophilic molecular interactions.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 139.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 179.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abramowicz M, Ribai P and Cordonnier M (2005) Congenital stationary night blindness: report of an autosomal recessive family and linkage analysis. Am J Med Genet 132A:76–79

    Article  PubMed  Google Scholar 

  • Agarwala KL, Ganesh S, Tsutsumi Y et al. (2001) Cloning and functional characterization of DSCAML1, a novel DSCAM-like cell adhesion molecule that mediates homophilic intercellular adhesion. Biochem Biophys Res Commun 285:760–772

    Article  CAS  PubMed  Google Scholar 

  • Agarwala KL, Nakamura S, Tsutsumi Y et al. (2000) Down syndrome cell adhesion molecule DSCAM mediates homophilic intercellular adhesion. Brain Res Mol Brain Res 79:118–126

    Article  CAS  PubMed  Google Scholar 

  • Bodnarenko SR, Jeyarasasingam G and Chalupa LM (1995) Development and regulation of dendritic stratification in retinal ganglion cells by glutamate-mediated afferent activity. J Neurosci 15:7037–7045

    CAS  PubMed  Google Scholar 

  • Coombs J, van der List D, Wang GY et al. (2006) Morphological properties of mouse retinal ganglion cells. Neuroscience 140:123–136

    Article  CAS  PubMed  Google Scholar 

  • Dacey DM, Peterson BB, Robinson FR et al. (2003) Fireworks in the primate retina: in vitro photodynamics reveals diverse LGN-projecting ganglion cell types. Neuron 37:15–27

    Article  CAS  PubMed  Google Scholar 

  • Famiglietti EV, Jr. and Kolb H (1976) Structural basis for ON-and OFF-center responses in retinal ganglion cells. Science 194:193–195

    Article  PubMed  Google Scholar 

  • Fuerst PG, Koizumi A, Masland RH et al. (2008) Neurite arborization and mosaic spacing in the mouse retina require DSCAM. Nature 451:470–474

    Article  CAS  PubMed  Google Scholar 

  • Hayashi K, Kaufman L, Ross MD et al. (2005) Definition of the critical domains required for homophilic targeting of mouse sidekick molecules. FASEB J 19:614–616

    CAS  PubMed  Google Scholar 

  • Karten HJ, Keyser KT and Brecha NC (1990) Biochemical and morphological heterogeneity of retinal ganglion cells. Res Publ Assoc Res Nerv Ment Dis 67:19–33

    CAS  PubMed  Google Scholar 

  • Kaufman L (2004) Sidekick-1 is upregulated in glomeruli in HIV-Associated Nephropathy. J Am Soc Nephrol 15:1721–1730

    Article  CAS  PubMed  Google Scholar 

  • Kaufman L, Hayashi K, Ross MJ et al. (2004) Sidekick-1 is upregulated in glomeruli in HIV-associated nephropathy. J Am Soc Nephrol 15:1721–1730

    Article  CAS  PubMed  Google Scholar 

  • Kaufman L, Yang G, Hayashi K et al. (2007) The homophilic adhesion molecule sidekick-1 contributes to augmented podocyte aggregation in HIV-associated nephropathy. FASEB J 21:1367–1375

    Article  CAS  PubMed  Google Scholar 

  • Kim E and Sheng M (2004) PDZ domain proteins of synapses. Nat Rev Neurosci 5:771–781

    Article  CAS  PubMed  Google Scholar 

  • Kong J, Fish D, Rockhill R et al. (2005) Diversity of ganglion cells in the mouse retina: unsupervised morphological classification and its limits. J Comp Neurol 489:293–310

    Article  PubMed  Google Scholar 

  • Lee R, Clandinin T, Lee C et al. (2003) The protocadherin Flamingo is required for axon target selection in the Drosophila visual system. Nat Neurosci 6:557–563

    Article  CAS  PubMed  Google Scholar 

  • Ly A, Nikolaev A, Suresh G et al. (2008) DSCAM is a netrin receptor that collaborates with DCC in mediating turning responses to netrin-1. Cell 133:1241–1254

    Article  CAS  PubMed  Google Scholar 

  • Masland RH (2001) Neuronal diversity in the retina. Curr Opin Neurobiol 11:431–436

    Article  CAS  PubMed  Google Scholar 

  • Meyer G, Varoqueaux F, Neeb A et al. (2004) The complexity of PDZ domain-mediated interactions at glutamatergic synapses: a case study on neuroligin. Neuropharmacology 47:724–733

    Article  CAS  PubMed  Google Scholar 

  • Mumm JS, Godinho L, Morgan JL et al. (2005) Laminar circuit formation in the vertebrate retina. Prog Brain Res 147:155–169

    Article  PubMed  Google Scholar 

  • Nguyen DN, Liu Y, Litsky ML et al. (1997) The sidekick gene, a member of the immunoglobulin superfamily, is required for pattern formation in the Drosophila eye. Development 124:3303–3312

    CAS  PubMed  Google Scholar 

  • Rockhill RL, Daly FJ, MacNeil MA et al. (2002) The diversity of ganglion cells in a mammalian retina. J Neurosci 22:3831–3843

    CAS  PubMed  Google Scholar 

  • Roska B and Werblin F (2001) Vertical interactions across ten parallel, stacked representations in the mammalian retina. Nature 410:583–587

    Article  CAS  PubMed  Google Scholar 

  • Sanes JR and Yamagata M (1999) Formation of lamina-specific synaptic connections. Curr Opin Neurobiol 9:79–87

    Article  CAS  PubMed  Google Scholar 

  • Scheiffele P (2003) Cell-cell signaling during synapse formation in the CNS. Annu Rev Neurosci 26:485–508

    Article  CAS  PubMed  Google Scholar 

  • Schmucker D, Clemens JC, Shu H et al. (2000) Drosophila Dscam is an axon guidance receptor exhibiting extraordinary molecular diversity. Cell 101:671–684

    Article  CAS  PubMed  Google Scholar 

  • Soba P, Zhu S, Emoto K et al. (2007) Drosophila sensory neurons require Dscam for dendritic self-avoidance and proper dendritic field organization. Neuron 54:403–416

    Article  CAS  PubMed  Google Scholar 

  • Südhof TC (2001) The synaptic cleft and synaptic cell adhesion. In: Cowan WM, Südhof TC and Stevens CF (eds) Synapses. Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Sun W, Li N and He S (2002) Large-scale morphological survey of mouse retinal ganglion cells. J Comp Neurol 451:115–126

    Article  PubMed  Google Scholar 

  • Takeichi M and Abe K (2005) Synaptic contact dynamics controlled by cadherin and catenins. Trends Cell Biol 15:216–221

    Article  CAS  PubMed  Google Scholar 

  • Wassle H and Boycott BB (1991) Functional architecture of the mammalian retina. Physiol Rev 71:447–480

    CAS  PubMed  Google Scholar 

  • Yamagata M and Sanes J (2008a) Association of retinal target recognition molecules, Sidekicks and Dscams, with synaptic PDZ domain-containing proteins of the MAGI and PSD families. Society for Neuroscience Meeting Abstract, 325.5/B32

    Google Scholar 

  • Yamagata M and Sanes J (2008b) Dscam and Sidekick proteins direct lamina-specific synaptic connections in vertebrate retina. Nature 451:465–469

    Article  CAS  PubMed  Google Scholar 

  • Yamagata M and Sanes JR (1995) Target-independent diversification and target-specific projection of chemically defined retinal ganglion cell subsets. Development 121:3763–3776

    CAS  PubMed  Google Scholar 

  • Yamagata M, Sanes JR and Weiner JA (2003) Synaptic adhesion molecules. Curr Opin Cell Biol 15:621–632

    Article  CAS  PubMed  Google Scholar 

  • Yamagata M, Weiner J, Dulac C et al. (2006) Labeled lines in the retinotectal system: Markers for retinorecipient sublaminae and the retinal ganglion cell subsets that innervate them. Mol Cell Neurosci 33:296–310

    Article  CAS  PubMed  Google Scholar 

  • Yamagata M, Weiner JA and Sanes JR (2002) Sidekicks: synaptic adhesion molecules that promote lamina-specific connectivity in the retina. Cell 110:649–660

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Y. Kate Hong .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Hong, Y.K., Yamagata, M. (2009). Molecular Basis of Lamina-Specific Synaptic Connections in the Retina: Sidekick Immunoglobulin Superfamily Molecules. In: Umemori, H., Hortsch, M. (eds) The Sticky Synapse. Springer, New York, NY. https://doi.org/10.1007/978-0-387-92708-4_10

Download citation

Publish with us

Policies and ethics