Studies on mosquito-borne viruses in their vectors: I. The normal fine structure of the midgut epithelium of the adult female Aedes aegypti (L.) and the functional significance of its modification following a blood meal

Abstract

1. 1) The following organelles and components of the normal fine structure of the midgut cells of adult female Aedes aegypti, as observed in sectioned material studied by electron microscopy, are discussed and illustrated by electron micrographs: the microvilli of the luminal surface, and septa invaginated from the basal cell membrane; the intercellular boundary; a basement membrane and associated tracheoles, muscles and connective tissue; nucleus and nucleolus; Golgi complex or dictyosomes; endoplasmic reticulum; ribonucleoprotein granules of the cytoplasmic matrix; various vesicles, and vacuoles. 2. 2) In starved and sugar-fed mosquitoes, or mosquitoes given water only, the granular endoplasmic reticulum appears, in sections, in the perinuclear zone as distinctive whorls which, however, following a blood meal and during its digestion, unfold to become a complex system ramifying widely throughout the cell cytoplasm. Reversion to whorls takes place on completion of blood digestion and a subsequent diet of sugar fails to stimulate the whorls to unfold. Whorls, and their distension during blood digestion, were also seen in females of Aedes togoi. 3. 3) Some emphasis is given to the possible role of this reversible whorl formation in the segregation and transportation, when unfolded, of proteolytic enzymes for the digestion of the blood meal in the gut lumen. Cytochemical studies by light microscopy confirm the morphological, and suggest some support for this functional, interpretation of these whorls. But, no completely conclusive explanation of function is yet practicable; possible alternatives are considered. 4. 4) Immediately (within at most half-an-hour) after ingesting blood, a finely granular material, which is to form the peritrophic membrane, appears in the gut lumen between and beyond the tips of the microvilli, apparently secreted from their surfaces. Secretion appears to cease about the 15th hour, or earlier, by which time the membrane is a discrete, finely granular, compacted layer on the surface of the well-digested blood. 5. 5) These electron microscopy studies reveal rapid and elaborate responses by the midgut cells to the presence in the gut of a blood meal ingested by normal feeding on an infant mouse. The fate of virus in mosquitoes infected through a membrane with artificial food mixtures — which are only partially of blood — may be, it is suggested, atypical and inadmissible for the interpretation of virus-vector relationship in mosquitoes infected naturally by engorging from a viraemic host. 6. 6) All intracellular structures and profiles of midgut cells described and illustrated, and changes in them associated with natural blood meals, were seen in Ae. aegypti whether fed on healthy baby mice, or infected with Semliki Forest virus by engorgement from viraemic mice. 7. 7) The paper provides a foundation of normal intracellular structure to be seen in mosquito midgut cells by electron microscopy against which the abnormal in mosquitoes infected with viruses, or other pathogens, may be sought. It also indicates opportunities for the further elucidation of cell function by studies correlating intracellular morphology and its transformations, as observed by electron microscopy, with biochemical, physiological and other experimental analyses.