Time and site of assembly of the peritrophic membrane of the mosquito Aedes aegypti (original) (raw)
Summary
We determined the time and site of secretion of the precursors of the peritrophic membrane (PM) in Aedes aegypti and when the structure is assembled. The fine structure of the developing membrane of blood-feed females was described, and the pattern of secretion of injected tritiated glucosamine analyzed autoradiographically. Immediately following blood feeding, ingested red cells rapidly become compressed, such that the surrounding plasma is extruded to the margin of the midgut contents. Thereby, ingested fluids form a narrow margin separating the blood mass from the midgut epithelium. By electron microscopy, the PM first becomes evident at about 4 to 8 h after blood is ingested, and the membrane attains mature texture by 12 h. The compacted mass of ingested erythrocytes seems to serve as a template for the forming structure. In contrast, tritiated glucosamine, injected into freshly engorged mosquitoes, begins to concentrate on the midgut microvilli by 2 h after feeding. By 8 h the label assumes the layered appearance that characterizes the fine structure of the mature membrane. In contrast to the prevailing concept that the PM of mosquitoes first assumes texture anteriorly immediately after blood is ingested, we find that this potential barrier to pathogen development forms no earlier than 4 h after feeding and that it is formed from precursors secreted along the entire length of the epithelium overlying the food mass.
Access this article
Subscribe and save
- Get 10 units per month
- Download Article/Chapter or eBook
- 1 Unit = 1 Article or 1 Chapter
- Cancel anytime Subscribe now
Buy Now
Price excludes VAT (USA)
Tax calculation will be finalised during checkout.
Instant access to the full article PDF.
Similar content being viewed by others
References
- Berner R, Rudin W, Hecker H (1983) Peritrophic membranes and protease activity in the midgut of the malaria mosquito, Anopheles stephensi (Liston) (Insecta: Diptera) under normal and experimental conditions. J Ultrastruct Res 83:195–204
Google Scholar - Bertram DS, Bird RG (1961) Studies on mosquito-borne viruses in their vectors, 1. The normal fine structure of the midgut epithelium of the adult female Aedes aegypti (L.) and the functional significance of its modifications following a blood meal. Trans R Soc Trop Med Hyg 55:404–423
Google Scholar - Day MF, Waterhouse DF (1953) Structure of the alimentary system. Function of the alimentary system. The mechanism of digestion. In: Roder KD (ed) Insect Physiology. John Wiley, New York, pp 273–330
Google Scholar - DeMets R, Jeuniaux C (1962) Sur les substances organiques constituant la membrane péritrophique des insectes. Arch Int Physiol Biochim 70:93–96
Google Scholar - Freyvogel T, Jaquet C (1965) The prerequisites for the formation of a peritrophic membrane in Culicidae females. Acta Trop 22:148–154
Google Scholar - Freyvogel T, Staubli W (1965) The formation of the peritrophic membrane in Culicidae. Acta Trop 22:118–147
Google Scholar - Gander E (1968) Zur Histologie und Histochemie des Mitteldarmes von Aedes aegypti und Anopheles stephensi im Zusammenhang mit der Blutverdauung. Acta Trop 25:133–175
Google Scholar - Hecker H (1977) Structure and function of midgut epithelial cells in Culicidae mosquitoes (Insecta, Diptera). Cell Tissue Res 184:321–341
Google Scholar - Howard LM (1962) Studies of the mechanism of infection of the mosquito midgut by Plasmodium gallinaceum. Am J Hyg 75:287–300
Google Scholar - Houk EJ (1977) Midgut ultrastructure of Culex tarsalis (Diptera: Culicidae) before and after a bloodmeal. Tissue Cell 9:103–118
Google Scholar - Houk EJ, Hardy JL (1982) Midgut cellular responses to bloodmeal digestion in the mosquito, Culex tarsalis Coquillet (Diptera: Culicidae). Int J Insect Morphol Embryol 11:109–119
Google Scholar - Houk EJ, Obie F, Hardy JL (1979) Peritrophic membrane formation and the midgut barrier to arboviral infection in the mosquito Culex tarsalis Coquillett (Insecta, Diptera). Acta Trop 36:39–45
Google Scholar - Kaznowski CE, Scheiderman HA, Bryant PJ (1986) The incorporation of precursors into Drosophila larval cuticle. J Insect Physiol 32:133–142
Google Scholar - Locke M (1964) The structure and formation of the integument in insects. Physiol Insecta 3:380–466
Google Scholar - Neville AC (1967) Chitin orientation in cuticle and its control. Adv Insect Physiol 4:213–286
Google Scholar - Orihel TC (1975) The peritrophic membrane: its role as a barrier to infection of the arthropod host. In: Maramorosch K, Shope RE (eds) Invertebrate Immunity Academic Press, New York, p 65–73
Google Scholar - Pearse AGE (1961) Histochemistry Theoretical and Applied. 2nd ed Little, Brown and Co., Boston
Google Scholar - Perrone JB, DeMaio J, Spielman A (1986) Regions of mosquito salivary glands distinguished by surface lectin-binding characteristics. Insect Biochem 16:313–318
Google Scholar - Richards GA, Richards PA (1977) The peritrophic membrane of insects. Ann Rev Entomol 22:219–240
Google Scholar - Richardson M, Romoser WS (1972) The formation of the peritrophic membrane in adult Aedes triseriatus (Say) (Diptera: Culicdae). J Med Entomol 9:494–500
Google Scholar - Romoser WS, Cody E (1975) The formation and fate of the peritrophic membrane in adult Culex nigripalpus (Diptera: Culicidae). J Med Entomol 12:371–378
Google Scholar - Stohler H (1957) Analyse des Infektionsverlaufes von Plasmodium gallinaceum im Darme von Aedes aegypti. Acta Trop 14:303–352
Google Scholar - Sutherland DR, Christensen BM, Lasee BA (1986) Midgut barrier as a possible factor in filarial worm vector competency in Aedes trivittatus. J Invert Pathol 47:1–7
Google Scholar - Tormey JM (1964) Differences in membrane configuration between osmium tetroxide-fixed and glutaraldehyde-fixed ciliary epithelium. J Cell Biol 23:658–664
Google Scholar - Waterhouse DF (1953) The occurrence and significance of the peritrophic membrane, with special reference to adult Lepidoptera and Diptera. Aust J Zool 1:299–318
Google Scholar - Wigglesworth VB (1965) The Principles of Insect Physiology. 6th ed Methuen and Co. Ltd., London
Google Scholar - Williams JC, Hagedorn HH, Beyenbach KW (1983) Dynamic changes in flow rate and compostion of urine during the postbloodmeal diuresis in Aedes aegypti (L.). J Comp Physiol 153:257–265
Google Scholar - Zhuzhikov DP (1962) The formation of the peritrophic membranes in Aedes aegypti L. mosquitoes. Nauchn Dokl Vyssh Shk Biol 4:25–27
Google Scholar
Author information
Authors and Affiliations
- Department of Tropical Public Health, Harvard School of Public Health, Boston, Massachusetts, USA
Joseph B. Perrone & Andrew Spielman
Authors
- Joseph B. Perrone
You can also search for this author inPubMed Google Scholar - Andrew Spielman
You can also search for this author inPubMed Google Scholar
Rights and permissions
About this article
Cite this article
Perrone, J.B., Spielman, A. Time and site of assembly of the peritrophic membrane of the mosquito Aedes aegypti.Cell Tissue Res. 252, 473–478 (1988). https://doi.org/10.1007/BF00214391
- Accepted: 12 November 1987
- Issue Date: May 1988
- DOI: https://doi.org/10.1007/BF00214391