Condensation of the central nervous system in embryonic Drosophila is inhibited by blocking hemocyte migration or neural activity

Abstract

Condensation is a process whereby a tissue undergoes a coordinated decrease in size and increase in cellular density during development. Although it occurs in many developmental contexts, the mechanisms underlying this process are largely unknown. Here, we investigate condensation in the embryonic Drosophila ventral nerve cord (VNC). Two major events coincide with condensation during embryogenesis: the deposition of extracellular matrix by hemocytes, and the onset of central nervous system activity. We find that preventing hemocyte migration by removing the function of the Drosophila VEGF receptor homologue, Pvr, or by disrupting Rac1 function in these cells, inhibits condensation. In the absence of hemocytes migrating adjacent to the developing VNC, the extracellular matrix components Collagen IV, Viking and Peroxidasin are not deposited around this tissue. Blocking neural activity by targeted expression of tetanus toxin light chain or an inwardly rectifying potassium channel also inhibits condensation. We find that disrupting Rac1 function in either glia or neurons, including those located in the nerve cord, causes a similar phenotype. Our data suggest that condensation of the VNC during Drosophila embryogenesis depends on both hemocyte-deposited extracellular matrix and neural activity, and allow us to propose a mechanism whereby these processes work together to shape the developing central nervous system.

Requirement for a core 1 galactosyltransferase in the Drosophila nervous system

“…The secretion of extracellular matrix by hemocytes appears to be particularly important for VNC condensation, as disrupting hemocyte migration impairs both the deposition of extracellular matrix around the VNC and VNC condensation (Olofsson and Page, 2005). Intriguingly, in addition to the PNA reactivity associated with the amnioserosa and VNC, we noticed PNA staining on scattered cells whose number and distribution suggested that they correspond to hemocytes.…”

“…To facilitate characterization of VNC condensation, we examined animals in which GFP was expressed in the VNC under nrv2-Gal4 or elavGal4 control. In wild-type, condensation begins during stage 15, and continues through hatching (Olofsson and Page, 2005). In C1GalTA mutants, VNC condensation occurs, but fails to reach the same extent of condensation as in wild-type, as the VNC is obviously elongated in first instar larvae ( Fig.…”

Organization and Function of the Blood–Brain Barrier inDrosophila

“…The following fly strains were used in this study: gcm N7-4 (Vincent et al, 1996); moody ⌬17 ; nrxIV 4304 (Baumgartner et al, 1996); nrxIV EP604 ; nrg 14 (Bloomington Stock Center, Bloomington, IN); nrv2 k13315 (Genova and Fehon, 2003); coracle 5 (Lamb et al, 1998); Df(3R)ED5020 to remove contactin (Faivre-Sarrailh et al, 2004); sinu NWU7 (Wu et al, 2004); Df(1)RR79 to remove the Claudin CG6398; Df(2R)M60E to remove the Claudin CG3770; Df(2R)nap2 to remove the Claudin CG1298; Df(3R)Excel6192 to remove the Claudin CG6982; pck EA97 (megatrachea) (Behr et al, 2003); 454 NeurexinIV:GFP, 125 Lachesin:GFP (Edenfeld et al, 2006); 173 nervana2:GFP (U. Lammel, unpublished observations); UAS:GFP; UAS:laminGFP; UAS:flp, nervana2Gal4 (Bloomington stock center); pvr 7.1 Viking:GFP (Olofsson and Page, 2005); 43Gal4 (Bloomington stock center); c527Gal4 (Hummel et al, 2002); FasIIGal4 (Mz507 ) (B. Altenhein, personal communication); chaGal4 (Salvaterra and Kitamoto, 2001);and SPG:Gal4 (Bainton et al, 2005). All deficiencies were obtained from the Bloomington stock collection.…”

“…In mutants with reduced hemocyte motility no lamella is formed (supplemental Fig. 1C, available at www.jneurosci.org as supplemental material) (Olofsson and Page, 2005).…”

Cell lineage tracing reveals the plasticity of the hemocyte lineages and of the hematopoietic compartments in Drosophila melanogaster

“…To study the Drosophila hemocyte lineages, we first used time-lapse confocal microscopy to investigate the expression pattern of the embryonic hemocyte compartment specific croquemort-GAL4 (crq-GAL4) driver [active in embryonic macrophages (Olofsson et al, 2005 and Fig. 1A)] and the Dorothy-GAL4 (Dot-GAL4) driver [expressed in the embryonic lymph gland (Kimbrell et al, 2002 and Fig.…”