<i>Drosophila</i> contactin, a homolog of vertebrate contactin, is required for septate junction organization and paracellular barrier function

Faivre‐Sarrailh, Catherine; Banerjee, Swati; Li, Jingjun; Hortsch, Michael; Laval, Monique; Bhat, Manzoor A.

doi:10.1242/dev.01372

Cited by 142 publications

(156 citation statements)

References 47 publications

(84 reference statements)

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“…Kune is required for tracheal tube size control: Since almost all characterized SJ proteins are required for tracheal tube size control (Behr et al 2003;Paul et al 2003;Faivre-Sarrailh et al 2004;Llimargas et al 2004;Hijazi et al 2009;Wu et al 2007), we examined the tracheal system of kune embryos.…”

Section: Resultsmentioning

confidence: 99%

The Drosophila Claudin Kune-kune Is Required for Septate Junction Organization and Tracheal Tube Size Control

2010

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The vertebrate tight junction is a critical claudin-based cell-cell junction that functions to prevent free paracellular diffusion between epithelial cells. In Drosophila, this barrier is provided by the septate junction, which, despite being ultrastructurally distinct from the vertebrate tight junction, also contains the claudin-family proteins Megatrachea and Sinuous. Here we identify a third Drosophila claudin, Kunekune, that localizes to septate junctions and is required for junction organization and paracellular barrier function, but not for apical-basal polarity. In the tracheal system, septate junctions have a barrierindependent function that promotes lumenal secretion of Vermiform and Serpentine, extracellular matrix modifier proteins that are required to restrict tube length. As with Sinuous and Megatrachea, loss of Kune-kune prevents this secretion and results in overly elongated tubes. Embryos lacking all three characterized claudins have tracheal phenotypes similar to any single mutant, indicating that these claudins act in the same pathway controlling tracheal tube length. However, we find that there are distinct requirements for these claudins in epithelial septate junction formation. Megatrachea is predominantly required for correct localization of septate junction components, while Sinuous is predominantly required for maintaining normal levels of septate junction proteins. Kune-kune is required for both localization and levels. Double-and triple-mutant combinations of Sinuous and Megatrachea with Kunekune resemble the Kune-kune single mutant, suggesting that Kune-kune has a more central role in septate junction formation than either Sinuous or Megatrachea.

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Section: Resultsmentioning

confidence: 99%

The Drosophila Claudin Kune-kune Is Required for Septate Junction Organization and Tracheal Tube Size Control

2010

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“…Primary antibodies used were rabbit anti-Nrx IV (Baumgartner et al, 1996), guinea pig anti-Cont (Faivre-Sarrailh et al, 2004), rabbit anti-GFP (Invitrogen, San Diego, CA), mouse anti-FAS II (Developmental Studies Hybridoma Bank, University of Iowa, Iowa City, IA), rabbit anti-␤3 tubulin (Dettman et al, 2001), rat anti-Nrg (our study), and guinea pig anti-Repo (our study). All secondary antibodies used in this study were from Jackson ImmunoResearch (West Grove, PA).…”

Section: Methodsmentioning

confidence: 99%

“…nrx IV 4304 , cont ex956 , and nrg 1 alleles have been described previously (Baumgartner et al, 1996;Faivre-Sarrailh et al, 2004). Upstream activating sequences (UAS)-tau green fluorescent protein (GFP) was obtained from S. Crews (University of North Carolina, Chapel Hill, NC), repo-GAL4 was obtained from V. Auld (University of British Columbia, Vancouver, Canada), and gcm ⌬P1 was obtained from B. Jones (University of Mississippi, Oxford, MI).…”

Section: Methodsmentioning

confidence: 99%

“…4 D, white arrows). We have shown previously that Nrx IV, Cont, and Nrg are interdependent for their epithelial SJ localization (Faivre-Sarrailh et al, 2004). Having established that Nrx IV, Cont, and Nrg colocalize in the peripheral nerves, we investigated whether these proteins are interdependent for their localization in the peripheral nerves.…”

Section: Nrx IV Cont and Nrg Are Interdependent For Their Localizatmentioning

confidence: 97%

“…We established whether NRX IV, CONT, and NRG, which we have shown previously to localize to epithelial SJs (Faivre-Sarrailh et al, 2004), are expressed in the peripheral nerves and whether these proteins are expressed by axons or glia or both. To visualize the peripheral nerves of wild-type stage 16 embryos, we performed triple immunostaining using antibodies against Nrx IV (Fig.…”

Section: Septate Junction Proteins Nrx IV Cont and Nrg Are Expressementioning

confidence: 99%

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Axonal Ensheathment and Septate Junction Formation in the Peripheral Nervous System ofDrosophila

Banerjee¹,

Pillai²,

Paik³

et al. 2006

J. Neurosci.

103

171

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Axonal insulation is critical for efficient action potential propagation and normal functioning of the nervous system. In Drosophila, the underlying basis of nerve ensheathment is the axonal insulation by glial cells and the establishment of septate junctions (SJs) between glial cell membranes. However, the details of the cellular and molecular mechanisms underlying axonal insulation and SJ formation are still obscure. Here, we report the characterization of axonal insulation in the Drosophila peripheral nervous system (PNS). Targeted expression of tau-green fluorescent protein in the glial cells and ultrastructural analysis of the peripheral nerves allowed us to visualize the glial ensheathment of axons. We show that individual or a group of axons are ensheathed by inner glial processes, which in turn are ensheathed by the outer perineurial glial cells. SJs are formed between the inner and outer glial membranes. We also show that Neurexin IV, Contactin, and Neuroglian are coexpressed in the peripheral glial membranes and that these proteins exist as a complex in the Drosophila nervous system. Mutations in neurexin IV, contactin, and neuroglian result in the disruption of blood-nerve barrier function in the PNS, and ultrastructural analyses of the mutant embryonic peripheral nerves show loss of glial SJs. Interestingly, the murine homologs of Neurexin IV, Contactin, and Neuroglian are expressed at the paranodal SJs and play a key role in axon-glial interactions of myelinated axons. Together, our data suggest that the molecular machinery underlying axonal insulation and axon-glial interactions may be conserved across species.

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The immunoglobulin superfamily of neuronal cell adhesion molecules: Lessons from animal models and correlation with human disease

Κατίδου

Vidaki

Strigini

et al. 2008

Biotechnology Journal

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Neuronal cell adhesion molecules of the immunoglobulin superfamily (IgCAMs) play a crucial role in the formation of neural circuits at different levels: cell migration, axonal and dendritic targeting as well as synapse formation. Furthermore, in perinatal and adult life, neuronal IgCAMs are required for the formation and maintenance of specialized axonal membrane domains, synaptic plasticity and neurogenesis. Mutations in the corresponding human genes have been correlated to several human neuronal disorders. Perturbing neuronal IgCAMs in animal models provides powerful means to understand the molecular and cellular basis of such human disorders. In this review, we concentrate on the NCAM, L1 and contactin subfamilies of neuronal IgCAMs summarizing recent functional studies from model systems and highlighting their links to disease pathogenesis.

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Drosophila contactin, a homolog of vertebrate contactin, is required for septate junction organization and paracellular barrier function

Cited by 142 publications

References 47 publications

The Drosophila Claudin Kune-kune Is Required for Septate Junction Organization and Tracheal Tube Size Control

The Drosophila Claudin Kune-kune Is Required for Septate Junction Organization and Tracheal Tube Size Control

Axonal Ensheathment and Septate Junction Formation in the Peripheral Nervous System ofDrosophila

The immunoglobulin superfamily of neuronal cell adhesion molecules: Lessons from animal models and correlation with human disease

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