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Secretion and formation of perimicrovillar membrane in the digestive system of the Sunn pest Eurygaster integriceps HemipteraScutelleridae in response to feeding.

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A r t i c l e
SECRETION AND FORMATION OF
PERIMICROVILLAR MEMBRANE IN
THE DIGESTIVE SYSTEM OF THE
SUNN PEST, Eurygaster integriceps
(HEMIPTERA: SCUTELLERIDAE) IN
RESPONSE TO FEEDING
Mohammad Mehrabadi and Ali Reza Bandani
Department of Plant Protection, University College of Agriculture
and Natural Resources, University of Tehran, Karaj, Iran
In this study, development of perimicrovillar membrane (PMM) from
midgut cells of starved and fed Eurygaster integriceps (Hemiptera:
Scutelleridae) was studied. Three different approaches, including
scanning electron microscopy (SEM), transmission electron microscopy
(TEM), marker enzymes of the PMMs (a-glucosidase), perimicrovillar
space (aminopeptidase), and microvillar membranes (b-glucosidase) were
used. Activities of these enzymes were remarkably low in the starved
insects. Moreover, microscopic observations revealed that PMM is not
present in the starved insect. Activities of enzymatic markers increased at
5 h postfeeding, and TEM and SEM observations showed the formation
of PMM as well as migration of double-membrane vesicles from center of
the columnar cell to the cell apex. The highest PMM was observed at 20 h
postfeeding which at this time marker enzyme activity, such as aglucosidase activity, was high, too. Thus, at 20 h postfeeding, PMM
system was evident and epithelial cells were completely covered by PMM
system. After 20 h postfeeding, presence of the fine holes in PMM started
to be seen and at 40 h post-feeding, observation showed degradation of
PMM system. Thus, it could be concluded that PMM in E. integriceps is
secreted by epithelial cell membrane when needed and its secretion and
formation is regulated by feeding. This system was not present in the
Grant sponsor: Iran National Science Foundation (INSF); Grant number: 86025.11.
Correspondence to: Ali Reza Bandani, Department of Plant Protection, Faculty of Agriculture Sciences and
Engineering, Agriculture and Natural Resources Campus, University of Tehran, Karaj, Iran.
E-mail: abandani@ut.ac.ir
ARCHIVES OF INSECT BIOCHEMISTRY AND PHYSIOLOGY, Vol. 78, No. 4, 190–200 (2011)
Published online in Wiley InterScience (www.interscience.wiley.com).
& 2011 Wiley Periodicals, Inc. DOI: 10.1002/arch.20452
Developing Perimicrovillar Membrane in Eurygaster Integriceps
191
C 2011
starved insects as its development takes place at 5 h postfeeding. Wiley Periodicals, Inc.
Keywords: perimicrovillar membrane (PMM); the Sunn pest; enzyme
markers; secretion; feeding
INTRODUCTION
Hemipteran and Thysanopteran midgut epithelial cells are covered with
lipoprotein membranes called perimicrovillar membranes (PMMs) that have a
physiological role similar to the peritrophic matrix seen in the midgut of other insects
(Terra, 1988).
The PMM maintains a constant distance from the inner microvillar membrane
(MM) and delimits a closed compartment, the so-called perimicrovillar space (PMS).
According to Silva et al. (1995), the PMMs are formed in the Golgi areas of
epithelial cells as internal membranes originating from double-membrane vesicles.
The double-membrane vesicles migrate to the cell apex, where the outer vesicle
membrane fuses with the MM and the inner vesicle membrane fuses with the PMM.
This model is supported by immunolocalization of a-glucosidase (a marker enzyme
of PMMs) in midgut cells of the cotton seed sucker bug Dysdercus peruvianus
(Silva and Terra, 1994; Silva et al., 1995) and the Sunn pest, Eurygaster integriceps
(Allahyari et al., 2010). PMM, such as the peritrophic matrix, is involved in
food digestion and absorption and is in close contact with ingested external
materials (Terra and Ferreira, 2005). Lectins and insecticidal proteins are known to
interact with midgut MM by binding to glycoproteins (Powell et al., 1998; Sauvion
et al., 2004; Mehlo et al., 2005; Trung et al., 2006). Membrane-bound proteins of
insect midgut play important roles in digestion, absorption, and other aspects of gut
physiology, and are potential targets for crop plant transgenes. Some of these proteins
are glycosylated and play important roles in interacting with exogenous particles, such
as Bacillus thuringiensis toxins, lectins, and other insecticidal proteins. Thus,
characterizing lumen side membrane-bound proteins of midgut epithelial cells
provides prerequisite knowledge for developing new control methods (Wilkins and
Billingsley, 2001).
Studies regarding characterization of PMM and its role in digestion revealed that
in a blood-sucking bug (Rhodnius prolixus) aminopeptidase, a-glucosidase and an
a-mannosidase are biochemical markers of PMS, PMM, and MM, respectively
(Ferreira et al., 1988), whereas in D. peruvianus, a phytophagus bug aminopeptidase,
a- and b-glucosidase are biochemical markers of PMS, PMM, and MM, respectively,
(Silva et al., 1995, 1996). Allahyari et al. (2010) showed that in E. integriceps another
phytophagus bug, b-glucosidase and aminopeptidase were markers of MM and PMS,
respectively, whereas á-glucosidase and acid phosphatase were PMM markers.
Regarding PMM secretion, Billingsley and Downe (1983, 1986) stated that
formation of PMM in R. prolixus was begun after blood feeding. In D. peruvianus, PMM
formation is carried out in biphasic trend, i.e., secretion and organization at the first
hours after feeding and disorganization at 30 h after feeding (Damasceno-Sa et al.,
2007). These studies were undertaken to elucidate the role of feeding in the secretion
and formation of PMM in E. integriceps using biochemical markers, such as a- and
b-glucosidase, and aminopeptidase, as well as microscopic studies.
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MATERIALS AND METHODS
Insect Rearing and Starvation
Populations of E. integriceps were obtained from the laboratory cultures, as described
by Allahyari et al. (2010). Then, in order to obtain female insects with midguts free of
ingested material, insects were placed in containers (plastic dishes) that have access to
water and without feeding in the laboratory conditions at 25721C and a photoperiod
of 14:10 (L:D) for 30 days. So, the insect midgut was free of materials. Then, the
starved insects were let to feed on wheat grains for 3 h. After that, they were separated
from the wheat grains and returned to previous condition and in a time course
manner after feeding, e.g., 5, 10, 20 and 40 h. Postfeeding, 20 insects were selected
and dissected, as describe in the following section. Also, 20 starved insects were also
selected and dissected as controls.
Insect Dissection and Sample Preparation
Sample preparation was based on the previously described methods with slight
modifications (Habibi et al., 2008; Bandani et al., 2009). Adult females were
individually immobilized by placing them on crushed ice (8–10 min), then they were
dissected under steromicroscope (Nikon, Tokyo, Japan) in precold 215 mM NaCl and
their alimentary canal was removed. The first ventriculus (V1) was used in this study
because of its high hydrolytic activity (Allahyari et al., 2010). Groups of V1 tissues equal
to 10 V1/ml distilled water were homogenized in a motorized potter-elvehjem
homogenizer (Omni International, Kennesaw). (Teflon pestle, 0.1 mm clearance).
Then, they were centrifuged at 15,000g for 30 min at 41C. The final volume of both
supernatant and pellet were adjusted to 1 ml by double-distilled water.
Hydrolyse Assays
a- and b-glucosidase activity were measured using 5 mM a-glucosidase and b-D,
4-nitrophenyl glucopyranoside in 50 mM citrate–phosphate buffer pH 5.0, respectively, based on the appearance of p-nitrophenol in the solution, according to Terra
et al. (1979). Aminopeptidase activity was measured using 2 mM L -leucine
p-nitroanilide (LPNA) in 50 mM Tris-HCl buffer pH 7.0 as substrate (Spungin and
Blumberg, 1989). The reaction volume was 0.1 ml for both a- and b-glucosidase and
the reaction was interrupted by the addition of 0.4 ml of a buffer containing 0.25 M
sodium carbonate, 0.25 M sodium bicarbonate, and 1% SDS. The absorbance of free
p-nitrophenolate was measured at 420 nm. The reaction volume for aminopeptidase
was 0.1 ml and the reaction was interrupted with 0.4 ml 30% acetic acid and
absorbance of free p-nitroaniline was read at 410 nm (Terra et al., 1979). For each
determination, the mixture of the reagents was kept at 301C for at least four different
periods of time and initial velocities were calculated. Controls without enzyme or
substrate were carried out and treated in a similar way to the experimental groups.
The enzyme activity was expressed in milli units (mU). One unit of enzymatic activity
was defined as the amount of enzyme that hydrolyzes 1 mmol of substrate per minute.
All experiments were repeated at least five times.
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Protein Determination
Protein concentration was measured according to the method of Bradford (1976),
using bovine serum albumin (Bio-Rad, Munchen, Germany) as a standard.
Transmission Electron Microscopy
Transmission electron microscopy (TEM) was done based on Allahyari et al. (2010).
Briefly, dissected V1 (freed from luminal contents in 215 mM NaCl) was fixed in 4%
glutaraldehyde in 0.15 M sodium cacodylate buffer (pH 7.0) for 4 h at 481C. After
rinsing with cacodylate buffer, they were postfixed in 1% OSO4 for 1.5 h and washed in
cacodylate buffer. After dehydration in graded ethanol, samples were cleared 20–30 min
in propylene oxide and embedded in resin. Ultrathin sections (0.05 mm) were cut using
a U3 ultramicrotome, followed by staining with uranyl acetate and lead citrate and
examined in a Philips CM10 Electron microscope (FEI Company, Minato-Ku, Tokyo).
Scanning Electron Microscopy (SEM)
Tissue samples were fixed in 2.5% glutaraldehyde, 4% paraformaldehyde in 0.1 M
cacodylate buffer, pH 7.0, postfixed in 1% osmium tetroxide, dehydrated through an
acetone series, and critical point dried. Samples were then coated with gold and
examined using a Zeiss SEM scanning electron microscope (Carl Zeiss AG,
Oberkochen, Germany; Damasceno-Sa et al., 2007).
Statistical Analysis
Data were compared by one-way analysis of variance (ANOVA). When ANOVA
indicated a significant difference between treatment means, individual treatment
means were compared by Fisher’s LSD (SAS Institute, 1997).
RESULTS
Time Course Activities of Enzyme Markers in Starved Insects and Postfeeding
Three biochemical markers (aminopeptidase, a- and b-glucosidase) were used to assess
whether their activity would change in insects at postfeeding hours. Moreover, the aim
was to estimate the basal activity of enzyme markers in the midguts of starved insects.
Differential activity of markers at different times postfeeding as well as different
activities in supernatant and pellet fractions were found (Figs. 1–3). a-Glucosidase
activity was found mainly in sediments resulting from centrifugation (Fig. 1). A
significant increase in activity was detected 5 h postfeeding in both soluble and pellet
fractions (LSD, Po0.01). This was followed by decreasing activity until 20 h
postfeeding for soluble fraction (LSD, Po0.01). a-Glucosidase activity was exceptionally increased at 40 hr postfeeding (LSD, Po0.01) (Fig. 1). Moreover, as shown in
Figure 1, both specific and unit activity of a-glucosidase showed the same trends. It is
noted that a minimum activity (basal activity) was detected in starved insects (Fig. 1).
As shown in Figure 2, b-glucosidase was mainly found in membrane fraction.
Although starved insects showed some b-glucosidase activity, main b-glucosidase
activity was found in fed insects. b-Glucosidase activity significantly increased at 5 h
postfeeding (LSD, Po0.05), followed by a subsequent fall at 10 h postfeeding (LSD,
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Figure 1. a-Glucosidase activity in starved (S) and fed insects at 5, 10, 20, and 40 h postfeeding. Twenty
insects were selected and dissected per replicate. Enzymatic activities for both supernatant (V1S) and pellet
(V1P) are given in vertical axis (mU gut 1 for black bars and mmol.min 1 mg protein 1 for with bars). One
unit of enzyme activity was calculated as the amount of enzyme capable of hydrolyzing 1 mmol of substrate
per minute. Bars represent S.D. of at least five independent replications. Data were compared by one-way
analysis of variance (ANOVA) followed by LSD test. For each group columns marked by Po0.05 or
Po0.01 are significantly different to S columns (starved insects) within the time course period.
Figure 2. b-Glucosidase activity in starved and fed insects. Details as described in Figure 1.
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Figure 3. Aminopeptidase activity in starved and fed insects. Details as described in Figure 1.
Po0.05). The enzyme activity was remarkably raised at 40 h postfeeding (LSD,
Po0.01) (Fig. 2).
Aminopeptidase activity was mainly concentrated in soluble fraction (Fig. 3). The
basal aminopeptidase activity observed in starved insects increased during postfeeding
period; e.g., the aminopeptidase activity almost doubled at 5 h postfeeding (LSD,
Po0.01). However, a reduction in activity was observed at 10 h postfeeding especially
in pellet fraction (LSD, Po0.05). A second increase in activity was observed 20 h
postfeeding in soluble fraction. Interestingly, the enzyme assays showed reduced
activities in membrane fraction at the respective time postfeeding. These events were
followed by the recovery of activity in membrane fraction and accentuated fall in
soluble fraction (Fig. 3).
Midgut Ultrastructure Morphological Changes Monitoring Using TEM and SEM
Observations
SEM and TEM observation of midgut showed that MM and PMM are present in first
midgut section, and also subcellular organizations (mitochondria and endoplasmic
reticulum) were present in the base of columnar cells. PMM structure was rarely
present in the apex of midgut cells of starved insects (Fig. 4A). Moreover, subcellular
organizations were evident in midgut cells of starved insects as TEM observation
showed (Fig. 4B). There is no double-membrane vesicle in the midgut cells of starved
insects. Following the feeding from wheat seeds at 5 h postfeeding, double-membrane
vesicles could be seen migrating from the center of the cell toward the base of brush
borders. Furthermore, endoplasmic reticulums and mitochondria were no longer
apparent. Instead, PMM was more developed compared with that of starved insects
(Fig. 4C). Similarly, at 10 h double-membrane vesicles was present and PMM seemed
to continue development (Fig. 4D). This was a unique image showing movement of a
double-membrane vesicle along the brush border to lose its outer membrane and to
cross brush border. Besides, another released vesicle (single membrane one) observed
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Figure 4. Transmission electron microscopy of the first section of E. integriceps midgut (V1) in starved and
fed insects. PMM structure was rarely present in the apex of midgut cells of starved insects (A). Subcellular
organizations were evident in midgut cells of starved insects as TEM observation showed (B). At 5 h
postfeeding, double-membrane vesicles could be seen migrating from the center of the cell toward base of
brush borders. PMM was more developed compared with that of starved insects (C). At 10 h, doublemembrane vesicles were present and PMM seemed to continue development (D). Moving of a doublemembrane vesicles along the brush border to lose their outer membrane and to cross brush border are also
shown (D). At 20 and 40 h, PMM structure as well as double-membrane vesicle were also present (E, F). M,
mitochondria; PMM, perimicrovillar membrane; RER, rough endoplasmic reticulum; V, Vesicle. Bars: (A, B,
C, E, F) 10 mm; (D) 5 mm.
passing the brush border (Fig. 4D). At the other postfeeding times, PMM structure as
well as double-membrane vesicle were also present (Fig. 4E and F). Totally, PMM
structure was more developed in fed insect.
To monitor PMM development on top of epithelial cells, SEM was used. First
midgut section of the midgut was used. SEM revealed that midgut epithelial cells of
starved insects were not covered by PMM. In this state, microvilli were seen free of
PMM and could be distinguished easily (Fig. 5A and B). Some portion of PMM,
however, could be found between the cells margin. In contrast, owing to covering of
cells by PMM system postfeeding, it was not possible to see such situation as seen in
starved insects. At 5 hr postfeeding, cells were completely covered by PMM system and
individual cells cannot be observed (Fig. 5C). At 10 hr postfeeding, midgut cells were
almost completely covered by PMM. However, in some regions, midgut cells were
naked and could be distinguished (Fig. 5D). At 20 h postfeeding, PMM system was
evident and epithelial cells were completely covered by PMM system (Fig. 5E). Finally,
at 40 h postfeeding, observation showed degradation of PMM system (Fig. 5F). SEM
observations showed disorganization of PMM system between 20 and 40 h postfeeding,
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Figure 5. Scanning electron microscopy of the first section of E. integriceps midgut (V1) in starved (A and
B) and fed insects at 5 h (C), 10 h (D), 20 h (E), 40 h (F), and 20–40 h postfeeding (G). Mi, microvilli; Es,
esophagus; PMM, perimicrovillar membrane; V1, first ventriculus of the midgut. Bars: (A) 200 mm; (B)
20 mm (C–H) 5 mm.
which was indicated by many fine holes at its surface (Fig. 5G). These results clearly
revealed dynamic production of PMM system in starved and fed insects at different
times postfeeding.
DISCUSSION
Using both microscopic and marker enzymes, it was found that PMM is not a static
structure but a dynamic structure which is produced in response to feeding and
degraded after feeding. All three biochemical markers (a-glucosidase, b-glucosidase
and aminopeptidase) had little activity but not zero activity in the starved insect.
However, these biochemical markers (three enzymes) activities were increased
significantly in the fed insects. It has been reported that a minimal enzyme release is
typical for many insect species (Chapman, 1998). As a rule, in discontinuous feeders,
such as seed-sucking insects, a regulated release of digestive enzymes (i.e., with stored
enzymes in the cytoplasm) occur (Lehane et al., 1996). Woodring et al. (2009)
suggested that in Gryllus bimaculatus (Orthoptera: Gryllidae) some digestive enzymes,
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such as amylase, trypsin, and aminopeptidase, are secreted continuously at a basal rate
in unfed animals.
a-Glucosidase activity was more in the pellet compared with supernatant, showing
that it is a membrane-bound enzyme, i.e., PMM marker as reported by Allahyari et al.
(2010). Although its activity is low in starved insects, activity is increased after feeding
over time. Changes in a-glucosidase activity in response to feeding has been reported
in other phytophagus bugs, D. peruvianus (Damasceno-Sa et al., 2007), D. fasciatus
(Khan and Ford, 1962), and a blood-sucking bug, R. prolixus (Silva et al., 2007). Also,
b-glucosidase activity was seen more in the pellet than supernatant, showing that it is a
membrane-bound enzyme (MM marker) (Allahyari et al., 2010). Thus, b-glucosidase
revealed similar activity profile as a-glucosidase with little differences. Similar trend of
activity (activity seen in sediment) in both a- and b-glucosidases make sense because
these enzymes are membrane bound, i.e., a-glucosidase is a PMM marker and
b-glucosidase is a MM marker. However, different pictures can be seen regarding
aminopeptidase, which is seen more in the supernatant than sediment fraction because
aminopeptidase in E. integriceps and the other Hemipteran insects is a PMS marker,
and thus it is seen in supernatant fraction (Ferreira et al., 1988; Silva et al., 1995, 1996;
Allahyari et al., 2010). It has been reported that aminopeptidase is a soluble form in
the PMS, because the highest activity of this enzyme was seen in the supernatant when
tissues were homogenized (Ferreira et al., 1988; Silva et al., 1996; Damasceno-Sa et al.,
2007; Allahyari et al., 2010). In some insects, such as Lepidoptera, Diptera, and some
Coleopteran, aminopeptidases are associated with the MM of the midgut epithelium
(Cristofoletti et al., 2003; Terra and Ferreira, 2005), and thus act as a receptor for the
toxin of bacterium B. thuringiensis (d-endotoxins). These Cry toxins bind to
aminopeptidase and cadherin receptors, producing pore in the cell membrane, and
causing cell breakdown, and finally insect death (de Maagd et al., 2001; Bravo et al.,
2007; Soberon et al., 2007). However, in some other insects, such as Hemiptera,
aminopeptidase is in a soluble form as indicated for D. Peruvianus, E. Integriceps, and
R. prolixus (Ferreira et al., 1988; Silva et al., 1996, 2007; Damasceno-Sa et al., 2007;
Allahyari et al., 2010).
As a complementary approach, TEM and SEM observations were carried out to
examine structural changes of midgut epithelial cells in the starved and fed insects.
TEM showed that PMM system had little or no development in starved insects, and as
a result midgut cell were without PMM covering (Fig. 4). Also, SEM observations
showed that midgut cells were not covered by PMM and margin of microvilli could be
clearly seen (Fig. 5). These results are consistent with those reported by Damasceno-Sa
et al. (2007) who demonstrated using TEM and SEM studies that in starved
D. peruvianus the microvilli were without PMM covering. Similar observations have
also been reported for R. prolixus that the midgut cells of starved insects were almost
deprived of PMMs (Billingsley and Downe, 1983, 1986; Silva et al., 2007). Also, it has
been reported that in D. fasciatus cytology of the midgut epithelium is changed in the
starved insects (Khan and Ford, 1962).
Epithelial cells were completely covered by PMM system at 20 h postfeeding
(Fig. 5E), and also aminopeptidase and a-glucosidase activities were abundant at this
time. At 40 h postfeeding, perforation and degradation of the membrane was observed
in some parts (Fig. 5G) Thus, it can be concluded that PMM was no longer needed to
present in developed state after about 2 days postfeeding. These results were
supported by findings of Damasceno-Sa et al. (2007) who showed that the covering of
PMMs in D. peruvianus diminished at 48 h postfeeding.
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So, in this study, we see that PMM in E. integriceps is secreted by epithelial cell
membrane when needed, and its secretion and formation is regulated by feeding. This
system was not present in the starved insects, as its development takes place at hours
postfeeding.
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Archives of Insect Biochemistry and Physiology
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feeding, formation, eurygaster, system, pest, membranes, integricepe, sunnn, response, digestive, hemipterascutelleridae, perimicrovillar, secretion
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