Differential sorting of constitutively co-secreted proteins in the ovarian follicle cells of Drosophila.
Conventional and freeze-fracture electron microscopy, immuno-electron microscopy of ovarian cryosections and confocal immunofluorescence were used to analyze the ovarian distribution of the major protein classes being secreted by the follicle cells during the vitellogenic and choriogenic stages of Drosophila oogenesis. Our results clearly demonstrated that at vitellogenic stages the follicle cells co-secrete constitutively vitelline membrane and yolk proteins that are either sorted into distinct secretory vesicles or they are segregated in different parts of bipartite vesicles by differential condensation. Following their exocytosis only the vitelline membrane proteins are incorporated into the forming vitelline membrane. The yolk proteins (along with their hemolymph circulating counterparts) diffuse through gaps amongst the incomplete vitelline membrane and are internalized through endocytosis by the oocyte where they are finally stored into modified lysosomes referred to as alpha-yolk granules. The unexpected immunolocalization of vitelline membrane antigens in the associated body of the alpha-yolk granules may indicate that this structure is a transient repository for the proteins being internalized into the oocyte along with the yolk proteins. In the early choriogenic follicle cells the vitelline membrane and early chorion proteins were found to be co-secreted and to be evenly intermixed into the same secretory vesicles. These findings illuminate new details concerning the follicle cells secretory and oocyte endocytic pathways and provide for the first time evidence for condensation-mediated sorting of constitutively secreted proteins in Drosophila.
Trougakos
I P
IP
Department of Cell Biology and Biophysics, Faculty of Biology, Athens University, Greece.
Papassideri
I S
IS
Waring
G L
GL
Margaritis
L H
LH
D000818:Animals; D004331:Drosophila melanogaster; D004527:Egg Proteins / Q000032:analysis / Q000378:metabolism*; D005260:Female; D005614:Freeze Fracturing; D016253:Microscopy, Immunoelectron; D009865:Oocytes / Q000737:chemistry / Q000378:metabolism / Q000648:ultrastructure; D015388:Organelles / Q000378:metabolism; D006080:Ovarian Follicle / Q000737:chemistry / Q000378:metabolism*; D021381:Protein Transport / Q000502:physiology; D014817:Vitelline Membrane / Q000737:chemistry / Q000378:metabolism
D004527:Egg Proteins