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SYG/Nephrin/IrreC Family of Adhesion Proteins Mediate Asymmetric Cell–Cell Adhesion in Development

  • Kang ShenEmail author
Chapter
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Abstract

A hallmark of the development of the multicellular organisms is the cell–cell interaction. One specific type of cellular junction structures that is essential for the function of the nervous system is the chemical synapses. Chemical synapses release chemicals from neurons to their target cells to transmit electrical signals. To establish and maintain such a junctional structure, transsynaptic adhesion molecules play important roles at different developmental stages. Indeed, a number of adhesion molecules have been implicated in the various stages of the “life” of synapses to bring and hold the pre- and postsynaptic partners together in developing and mature synapses. Relatively little is known about which membrane molecules mediate the initial recognition during the process of synaptogenesis. In this chapter, we will focus our discussion on the IrreC/Nephrin/SYG-1 family of adhesion molecules, whose function in synaptic target selection has been studied in much detail in the nematode Caenorhabditis elegans. Interestingly, the members of this family in Drosophila and vertebrates also play essential functions in mediating the cellular recognition in myoblast fusion, eye morphogenesis, and kidney slit membrane formation. These findings suggest that this group of adhesive molecules carry out asymmetric cellular recognition events in diverse developmental events.

Keywords

Adhesion molecules Immunoglobulin Superfamily Proteins synapse formation synaptic specificity 

References

  1. Aoto J and Chen L (2007) Bidirectional ephrin/Eph signaling in synaptic functions. Brain Res 1184:72–80CrossRefPubMedGoogle Scholar
  2. Bao S and Cagan R (2005) Preferential adhesion mediated by Hibris and Roughest regulates morphogenesis and patterning in the Drosophila eye. Dev Cell 8:925–935CrossRefPubMedGoogle Scholar
  3. Barletta GM, Kovari IA, Verma RK, Kerjaschki D and Holzman LB (2003) Nephrin and Neph1 co-localize at the podocyte foot process intercellular junction and form cis hetero-oligomers. J Biol Chem 278:19266–19271CrossRefPubMedGoogle Scholar
  4. Benson DL, Colman DR and Huntley GW (2001) Molecules, maps and synapse specificity. Nature Rev 2:899–909CrossRefGoogle Scholar
  5. Biederer T, Sara Y, Mozhayeva M, Atasoy D, Liu X, Kavalali ET and Südhof TC (2002) SynCAM, a synaptic adhesion molecule that drives synapse assembly. Science (New York, NY) 297:1525–1531Google Scholar
  6. Bour BA, Chakravarti M, West JM and Abmayr SM (2000) Drosophila SNS, a member of the immunoglobulin superfamily that is essential for myoblast fusion. Genes Dev 14:1498–1511PubMedGoogle Scholar
  7. Chen EH and Olson EN (2004) Towards a molecular pathway for myoblast fusion in Drosophila. Trends Cell Biol 14:452–460CrossRefPubMedGoogle Scholar
  8. Craig AM and Kang Y (2007) Neurexin-neuroligin signaling in synapse development. Curr Opin Neurobiol 17:43–52CrossRefPubMedGoogle Scholar
  9. Ding M, Chao D, Wang G and Shen K (2007) Spatial regulation of an E3 ubiquitin ligase directs selective synapse elimination. Science (New York, NY) 317:947–951Google Scholar
  10. Donoviel DB, Freed DD, Vogel H, Potter DG, Hawkins E, Barrish JP, Mathur BN, Turner CA, Geske R, Montgomery CA et al. (2001) Proteinuria and perinatal lethality in mice lacking NEPH1, a novel protein with homology to NEPHRIN. Mol Cell Biol 21:4829–4836CrossRefPubMedGoogle Scholar
  11. Gerke P, Benzing T, Hohne M, Kispert A, Frotscher M, Walz G and Kretz O (2006) Neuronal expression and interaction with the synaptic protein CASK suggest a role for Neph1 and Neph2 in synaptogenesis. J Comp Neurol 498:466–475CrossRefPubMedGoogle Scholar
  12. Gerke P, Huber TB, Sellin L, Benzing T and Walz G (2003) Homodimerization and heterodimerization of the glomerular podocyte proteins nephrin and NEPH1. J Am Soc Nephrol 14:918–926CrossRefPubMedGoogle Scholar
  13. Jones N, Blasutig IM, Eremina V, Ruston JM, Bladt F, Li H, Huang H, Larose L, Li SS, Takano T et al. (2006) Nck adaptor proteins link nephrin to the actin cytoskeleton of kidney podocytes. Nature 440:818–823CrossRefPubMedGoogle Scholar
  14. Kestila M, Lenkkeri U, Mannikko M, Lamerdin J, McCready P, Putaala H, Ruotsalainen V, Morita T, Nissinen M, Herva R et al. (1998). Positionally cloned gene for a novel glomerular protein – nephrin – is mutated in congenital nephrotic syndrome. Mol Cell 1:575–582CrossRefPubMedGoogle Scholar
  15. Khoshnoodi J, Sigmundsson K, Ofverstedt LG, Skoglund U, Obrink B, Wartiovaara J and Tryggvason K (2003) Nephrin promotes cell–cell adhesion through homophilic interactions. Am J Pathol 163:2337–2346PubMedGoogle Scholar
  16. Missler M, Zhang W, Rohlmann A, Kattenstroth G, Hammer RE, Gottmann K and Südhof TC (2003) Alpha-neurexins couple Ca2+ channels to synaptic vesicle exocytosis. Nature 423:939–948CrossRefPubMedGoogle Scholar
  17. Patrakka J and Tryggvason K (2007) Nephrin – a unique structural and signaling protein of the kidney filter. Trends Mol Med 13:396–403CrossRefPubMedGoogle Scholar
  18. Richardson BE, Nowak SJ and Baylies MK (2008) Myoblast fusion in fly and vertebrates: new genes, new processes and new perspectives. Traffic (Copenhagen, Denmark) 9:1050–1059CrossRefGoogle Scholar
  19. Rusconi JC, Hays R and Cagan RL (2000) Programmed cell death and patterning in Drosophila. Cell Death Differ 7:1063–1070CrossRefPubMedGoogle Scholar
  20. Serizawa S, Miyamichi K, Takeuchi H, Yamagishi Y, Suzuki M and Sakano H (2006) A neuronal identity code for the odorant receptor-specific and activity-dependent axon sorting. Cell 127:1057–1069CrossRefPubMedGoogle Scholar
  21. Shen K and Bargmann CI (2003). The immunoglobulin superfamily protein SYG-1 determines the location of specific synapses in C. elegans. Cell 112:619–630CrossRefPubMedGoogle Scholar
  22. Shen K, Fetter RD and Bargmann CI (2004). Synaptic specificity is generated by the synaptic guidepost protein SYG-2 and its receptor, SYG-1. Cell 116:869–881.CrossRefPubMedGoogle Scholar
  23. Srinivas BP, Woo J, Leong WY and Roy S (2007). A conserved molecular pathway mediates myoblast fusion in insects and vertebrates. Nature Genet 39:781–786CrossRefPubMedGoogle Scholar
  24. Strunkelnberg M, Bonengel B, Moda LM, Hertenstein A, de Couet HG, Ramos RG and Fischbach KF (2001) rst and its paralogue kirre act redundantly during embryonic muscle development in Drosophila. Development (Cambridge, England) 128:4229–4239Google Scholar
  25. Varoqueaux F, Aramuni G, Rawson RL, Mohrmann R, Missler M, Gottmann K, Zhang W, Südhof TC and Brose N (2006) Neuroligins determine synapse maturation and function. Neuron 51:741–754CrossRefPubMedGoogle Scholar
  26. Verma R, Kovari I, Soofi A, Nihalani D, Patrie K and Holzman LB (2006) Nephrin ectodomain engagement results in Src kinase activation, nephrin phosphorylation, Nck recruitment, and actin polymerization. J Clin Invest 116:1346–1359CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  1. 1.Department of Biology and PathologyHoward Hughes Medical Institute, Stanford UniversityStanfordUSA

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