Changes in follicular cells architecture during vitellogenin transport in the ovary of social Hymenoptera

Abstract

Vitellogenins are the major yolk proteins, synthesized in the fat body, released into the hemolymph and captured by the developing oocytes, but the mechanisms by which these proteins cross the follicular cell layer are still poorly understood. This study describes the actin distribution in follicular cells during vitellogenin transport to the oocyte in social Hymenoptera represented by bees Apis mellifera and Melipona quadrifasciata, the wasp Mischocyttarus cassununga and the ant Pachycondyla curvinodis. In oocytic chambers of vitellogenic follicles, vitellogenin was found within the follicular cells, perivitelline space and oocyte, indicating a transcellular route from the hemolymph to the perivitelline space. The cortical actin cytoskeleton in follicular cells underwent reorganization during transport of vitellogenin across this epithelium suggesting that in the ovary of social hymenopterans, vitellogenin delivery to oocytes requires a dynamic cytoskeletal rearrangement of actin filaments in the follicular cells.

Evidence for a transcellular route for vitellogenin transport in the telotrophic ovary of Podisus nigrispinus (Hemiptera: Pentatomidae)

“…Those studies show accumulation of hemolymph proteins in the intercellular spaces of follicular cells, which has been interpreted as an evidence that these proteins, including vitellogenin, are transported to the oocyte surface via a paracellular route. However, in bees, ants, and wasps, although patency occurs, vitellogenin is transported to the oocyte surface by receptor-mediated endocytosis, that is, via a transcellular route 25,32 .…”

“…Transmission electron microscopy and immunohistochemical studies in Hyalophora cecropia (Lepidoptera) 26–28 and Bemisia tabaci (Hemiptera) 29 , dynamics of the vital dyes trypan blue in Aedes aegypti (Diptera) 30 and Evan’s blue in Rhodnius prolixus (Hemiptera) 31 suggest the occurrence of paracellular transport of proteins trough the ovarian follicular epithelium. Conversely, in social Hymenoptera with meroistic polytrophic ovaries, ultrastructural studies indicate patency in the follicular epithelium 25 , but immunocytochemistry of vitellogenin and VgR show that both are localized in the plasma membrane and cytoplasm of follicular cells, suggesting a transcellular route in which vitellogenin initially diffuses through intercellular spaces to the follicular cells surface, bind to VgR, following clathrin-mediated endocytosis and transport to another plasma membrane domain (transcytosis) closely associated with oocyte surface 32 . This recent finding stimulated us to verify whether in other insects with meroistic telotrophic ovaries, patency is already an evidence of paracellular route for the vitellogenin transport to the oocyte surface for further endocytosis.…”

“…These VgRs have been reported to combine with some different ligands in vertebrates 21 , and their mRNA are also detected in the hypopharingeal glands 22 and fat body 16,23 in insects, suggesting that VgR may recognize other ligands, but in insect ovary vitellogenin is the unique ligand of VgR endocytosed by oocytes 11,13–15,24 . However, to reach the oocyte surface, vitellogenin must be transported through the follicular epithelium 25 , which surrounds the oocyte 2,6 and regulates the flow of vitellogenin to the oocyte 5,7 .…”

Juvenile hormone downregulates vitellogenin production in Ectatomma tuberculatum (Hymenoptera: Formicidae) sterile workers

“…In S. invicta, there is a peak of JH in the haemolymph of queens during the oviposition period (Brent and Vargo, 2003). JH activates ion channels in ovarian follicular cells, increasing the intercellular space as a result of changes in the architecture of the actin filaments (Ronnau et al, 2015) and facilitating vitellogenin to reach the surface of oocytes, where it is endocytosed Tufail and Takeda, 2009). In this way, the reduction of the circulating vitellogenin in the haemolymph in JH-treated ants may be associated with the uptake of vitellogenin for growing oocytes, since all workers used in the experiment have developing trophic eggs (Hora et al, 2001(Hora et al, , 2007.…”

As formigas poneromorfas do Brasil

“…Embora haja indicação que os nutrientes da hemolinfa atinjam a superfície do ovócito por entre os espaços intercelulares das células foliculares, há também evidências de transporte transcelular (por dentro das células foliculares). Terminado o acú-mulo de vitelo pelos ovócitos, as células foliculares se reorganizam e iniciam a síntese do córion que corresponde ao envoltório (casca) dos ovócitos, que nos insetos é de composição basicamente proteica (KING & AKAI, 1982;RONNAU et al, 2015).…”