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The Drosophila cell adhesion molecule Neuroglian regulates Lissencephaly-1 localisation in circulating immunosurveillance cells.

Williams MJ - BMC Immunol. (2009)

Bottom Line: Interestingly in plasmatocytes from Nrg mutants the nucleokinesis regulating protein Lissencephaly-1 (Lis1) fails to localise properly around the nucleus and is instead found diffuse throughout the cytoplasm and at unidentified perinuclear structures.After attaching to the wasp egg control plasmatocytes extend filopodia laterally from their cell periphery; as well as extending lateral filopodia plasmatocytes from Nrg mutants also extend many filopodia from their apical surface.At the cell periphery of haemocytes Neuroglian may be involved in cell-cell interactions, while at the cell centre Neuroglian regulates the localisation of the nucleokinesis complex protein lissencephaly-1.

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Affiliation: Institute of Biological and Environmental Sciences, University of Aberdeen, Tillydrone Avenue, Aberdeen, UK. m.j.williams@abdn.ac.uk

ABSTRACT

Background: When the parasitoid wasp Leptopilina boulardi lays its eggs in Drosophila larvae phagocytic cells called plasmatocytes and specialized cells known as lamellocytes encapsulate the egg. This requires these circulating immunosurveillance cells (haemocytes) to change from a non-adhesive to an adhesive state enabling them to bind to the invader. Interestingly, attachment of leukocytes, platelets, and insect haemocytes requires the same adhesion complexes as epithelial and neuronal cells.

Results: Here evidence is presented showing that the Drosophila L1-type cell adhesion molecule Neuroglian (Nrg) is required for haemocytes to encapsulate L. boulardi wasp eggs. The amino acid sequence FIGQY containing a conserved phosphorylated tyrosine is found in the intracellular domain of all L1-type cell adhesion molecules. This conserved tyrosine is phosphorylated at the cell periphery of plasmatocytes and lamellocytes prior to parasitisation, but dephosphorylated after immune activation. Intriguingly, another pool of Nrg located near the nucleus of plasmatocytes remains phosphorylated after parasitisation. In mammalian neuronal cells phosphorylated neurofascin, another L1-type cell adhesion molecule interacts with a nucleokinesis complex containing the microtubule binding protein lissencephaly-1 (Lis1) 1. Interestingly in plasmatocytes from Nrg mutants the nucleokinesis regulating protein Lissencephaly-1 (Lis1) fails to localise properly around the nucleus and is instead found diffuse throughout the cytoplasm and at unidentified perinuclear structures. After attaching to the wasp egg control plasmatocytes extend filopodia laterally from their cell periphery; as well as extending lateral filopodia plasmatocytes from Nrg mutants also extend many filopodia from their apical surface.

Conclusion: The Drosophila cellular adhesion molecule Neuroglian is expressed in haemocytes and its activity is required for the encapsulation of L. boularli eggs. At the cell periphery of haemocytes Neuroglian may be involved in cell-cell interactions, while at the cell centre Neuroglian regulates the localisation of the nucleokinesis complex protein lissencephaly-1.

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Nrg expressed in plasmatocytes and lamellocytes. Plasmatocytes and lamellocytes bled from control larvae 38–40 h post-parasitisation by L. boulardi G486 and co-stained with anti-Tubulin (red) and anti-Nrg (green). In the detail figure of plasmatocytes and lamellocyte arrows indicate that Nrg protein is enriched at the tips of some filopodia.
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Figure 1: Nrg expressed in plasmatocytes and lamellocytes. Plasmatocytes and lamellocytes bled from control larvae 38–40 h post-parasitisation by L. boulardi G486 and co-stained with anti-Tubulin (red) and anti-Nrg (green). In the detail figure of plasmatocytes and lamellocyte arrows indicate that Nrg protein is enriched at the tips of some filopodia.

Mentions: To begin to elucidate if Drosophila Neuroglian (Nrg) was involved in the cellular immune response haemocytes were bled from parasitized control larvae (w1118) approximately 40 hours after parasitisation and co-stained with anti-α-Tubulin and anti-Nrg antibodies [21]. In both plasmatocytes and lamellocytes bled from parasitized control larvae Nrg was expressed at the plasma membrane, and accumulated in filopodia at the cell periphery (Figure 1, arrows).


The Drosophila cell adhesion molecule Neuroglian regulates Lissencephaly-1 localisation in circulating immunosurveillance cells.

Williams MJ - BMC Immunol. (2009)

Nrg expressed in plasmatocytes and lamellocytes. Plasmatocytes and lamellocytes bled from control larvae 38–40 h post-parasitisation by L. boulardi G486 and co-stained with anti-Tubulin (red) and anti-Nrg (green). In the detail figure of plasmatocytes and lamellocyte arrows indicate that Nrg protein is enriched at the tips of some filopodia.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2667480&req=5

Figure 1: Nrg expressed in plasmatocytes and lamellocytes. Plasmatocytes and lamellocytes bled from control larvae 38–40 h post-parasitisation by L. boulardi G486 and co-stained with anti-Tubulin (red) and anti-Nrg (green). In the detail figure of plasmatocytes and lamellocyte arrows indicate that Nrg protein is enriched at the tips of some filopodia.
Mentions: To begin to elucidate if Drosophila Neuroglian (Nrg) was involved in the cellular immune response haemocytes were bled from parasitized control larvae (w1118) approximately 40 hours after parasitisation and co-stained with anti-α-Tubulin and anti-Nrg antibodies [21]. In both plasmatocytes and lamellocytes bled from parasitized control larvae Nrg was expressed at the plasma membrane, and accumulated in filopodia at the cell periphery (Figure 1, arrows).

Bottom Line: Interestingly in plasmatocytes from Nrg mutants the nucleokinesis regulating protein Lissencephaly-1 (Lis1) fails to localise properly around the nucleus and is instead found diffuse throughout the cytoplasm and at unidentified perinuclear structures.After attaching to the wasp egg control plasmatocytes extend filopodia laterally from their cell periphery; as well as extending lateral filopodia plasmatocytes from Nrg mutants also extend many filopodia from their apical surface.At the cell periphery of haemocytes Neuroglian may be involved in cell-cell interactions, while at the cell centre Neuroglian regulates the localisation of the nucleokinesis complex protein lissencephaly-1.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Biological and Environmental Sciences, University of Aberdeen, Tillydrone Avenue, Aberdeen, UK. m.j.williams@abdn.ac.uk

ABSTRACT

Background: When the parasitoid wasp Leptopilina boulardi lays its eggs in Drosophila larvae phagocytic cells called plasmatocytes and specialized cells known as lamellocytes encapsulate the egg. This requires these circulating immunosurveillance cells (haemocytes) to change from a non-adhesive to an adhesive state enabling them to bind to the invader. Interestingly, attachment of leukocytes, platelets, and insect haemocytes requires the same adhesion complexes as epithelial and neuronal cells.

Results: Here evidence is presented showing that the Drosophila L1-type cell adhesion molecule Neuroglian (Nrg) is required for haemocytes to encapsulate L. boulardi wasp eggs. The amino acid sequence FIGQY containing a conserved phosphorylated tyrosine is found in the intracellular domain of all L1-type cell adhesion molecules. This conserved tyrosine is phosphorylated at the cell periphery of plasmatocytes and lamellocytes prior to parasitisation, but dephosphorylated after immune activation. Intriguingly, another pool of Nrg located near the nucleus of plasmatocytes remains phosphorylated after parasitisation. In mammalian neuronal cells phosphorylated neurofascin, another L1-type cell adhesion molecule interacts with a nucleokinesis complex containing the microtubule binding protein lissencephaly-1 (Lis1) 1. Interestingly in plasmatocytes from Nrg mutants the nucleokinesis regulating protein Lissencephaly-1 (Lis1) fails to localise properly around the nucleus and is instead found diffuse throughout the cytoplasm and at unidentified perinuclear structures. After attaching to the wasp egg control plasmatocytes extend filopodia laterally from their cell periphery; as well as extending lateral filopodia plasmatocytes from Nrg mutants also extend many filopodia from their apical surface.

Conclusion: The Drosophila cellular adhesion molecule Neuroglian is expressed in haemocytes and its activity is required for the encapsulation of L. boularli eggs. At the cell periphery of haemocytes Neuroglian may be involved in cell-cell interactions, while at the cell centre Neuroglian regulates the localisation of the nucleokinesis complex protein lissencephaly-1.

Show MeSH
Related in: MedlinePlus