The peritrophic membrane of Spodoptera frugiperda: Secretion of peritrophins and role in immobilization and recycling digestive enzymes

Abstract

A peritrophin from the Spodoptera frugiperda peritrophic membrane (PM) and microvillar proteins from S. frugiperda anterior midgut cells were isolated and used to raise antibodies in a rabbit. These antibodies, as well as a Tenebrio molitor amylase antibody that cross-reacts with S. frugiperda amylases, and wheat-germ aglutinin were used in immunolocalization experiments performed with the aid of confocal fluorescence and immunogold techniques. The results showed that the peritrophin was secreted by anterior midgut columnar cells in vesicles pinched-off the microvilli (microapocrine secretion). The resulting double membrane vesicles become single membrane vesicles by membrane fusion, releasing peritrophin and part of the amylase and trypsin. The remaining membranes still containing microvillar proteins and membrane-bound amylase and trypsin are incorporated into a jelly-like material associated with PM. Calcofluor-treated larvae lacking a PM were shown to lose the decreasing gradient of trypsin and chymotrypsin observed along the midgut of control larvae. This gradient is thought to be formed by a countercurrent flux of fluid (in the space between PM and midgut cells) that powers enzyme recycling.

Densovirus Crosses the Insect Midgut by Transcytosis and Disturbs the Epithelial Barrier Function

“…Such interactions of the viral particles are reminiscent of what is observed in vivo with the peritrophic membrane, which the virus must first bind and then pass through. The labeling of the PM obtained with JcDNV antibody is similar to what has been described with peritrophin and chitin antibodies, suggesting an affinity of the viral capsids for some of the PM proteoglycan components (34). A lectin-like affinity of the densovirus particles might be important in determining the virus tropism, as already shown for the binding and/or the infectivity of a number of vertebrate parvoviruses, including the transcytosis of adeno-associated viruses, the only parvoviruses shown to transcytose epithelial barriers among this group (7; reviewed in references 35 and 36).…”

Insect feeding mobilizes a unique plant defense protease that disrupts the peritrophic matrix of caterpillars

“…A number of studies have demonstrated that increased PM permeability harms insects. For example, increased PM permeability impaired normal nutrient and enzyme cycling between the endoperitrophic and ectoperitrophic spaces (17,20). Disruption of the chitin network with lectins or chemicals increased both PM permeability and insect mortality (21).…”

“…The protease has an acidic pH optimum (9), which suggests that it might not be active in the alkaline caterpillar gut. However, in fall armyworm, digestive enzymes are released from anterior midgut cells by a microapocrine process and remain associated with membranes until released into the PM jelly (20). The release of membrane contents at the PM may create microenvironment with a pH favorable for the 33-kDa cysteine protease to be active.…”

Structural and biochemical characteristics of chitin-binding protein SeCBP66 from Spodoptera exigua (Hübner)

“…One class of the major PM proteins includes members with multiple chitin-binding domains (CBDs) that can only be removed by mild or strong denaturants, which cross-link with chitin fibrils to form the PM Granados, 1997, 2001). Given that the PM plays an important role in gut physiology, this disruption would decrease the permeability of the PM, which has harmful effects to insects and can even cause death (Wang and Granados, 2000;Bolognesi et al, 2001). Therefore, detailed study of the structure, biochemical properties, and function of PM proteins will help to understand the formation mechanism of the PM, which would further enrich our understanding of the mechanism of pathogenic bacterial infections and the interaction between the PM and microorganisms.…”