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Origin, evolution and function of the hemipteran perimicrovillar membrane with emphasis on Reduviidae that transmit Chagas disease

Published online by Cambridge University Press:  07 December 2015

A.E. Gutiérrez-Cabrera ,
A. Córdoba-Aguilar ,
E. Zenteno ,
C. Lowenberger  and
B. Espinoza
A.E. Gutiérrez-Cabrera
Affiliation:
Departamento de Inmunología, Instituto de Investigaciones Biomedicas, Universidad Nacional Autónoma de México, Apdo. 70228, Circuito Exterior, Ciudad Universitaria, 04510, Coyoacán, Distrito Federal, México Departamento de Bioquímica, Facultad de Medicina, Universidad Nacional Autónoma de México, Ciudad Universitaria, 04510 D.F., Mexico
A. Córdoba-Aguilar
Affiliation:
Departamento de Ecología Evolutiva, Instituto de Ecología, Universidad Nacional Autónoma de México, Apdo. P. 70-275, Circuito Exterior, Ciudad Universitaria, 04510, Coyoacán, Distrito Federal, Mexico
E. Zenteno
Affiliation:
Departamento de Bioquímica, Facultad de Medicina, Universidad Nacional Autónoma de México, Ciudad Universitaria, 04510 D.F., Mexico
C. Lowenberger
Affiliation:
Department of Biological Sciences, Simon Fraser University, Burnaby, B.C., V5A 1S6, Canada
B. Espinoza*
Affiliation:
Departamento de Inmunología, Instituto de Investigaciones Biomedicas, Universidad Nacional Autónoma de México, Apdo. 70228, Circuito Exterior, Ciudad Universitaria, 04510, Coyoacán, Distrito Federal, México
*
*Author for correspondence Phone: +52 55 56 22 89 43/44 E-mail: besgu@biomedicas.unam.mx; besgu@iibiomedicas.gmail.com
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Abstract

The peritrophic matrix is a chitin-protein structure that envelops the food bolus in the midgut of the majority of insects, but is absent in some groups which have, instead, an unusual extra-cellular lipoprotein membrane named the perimicrovillar membrane. The presence of the perimicrovillar membrane (PMM) allows these insects to exploit restricted ecological niches during all life stages. It is found only in some members of the superorder Paraneoptera and many of these species are of medical and economic importance. In this review we present an overview of the midgut and the digestive system of insects with an emphasis on the order Paraneoptera and differences found across phylogenetic groups. We discuss the importance of the PMM in Hemiptera and the apparent conservation of this structure among hemipteran groups, suggesting that the basic mechanism of PMM production is the same for different hemipteran species. We propose that the PMM is intimately involved in the interaction with parasites and as such should be a target for biological and chemical control of hemipteran insects of economic and medical importance.

Keywords

evolutionperimicrovillar membraneinsectstriatomines
Type
Review Paper
Information
Bulletin of Entomological Research , Volume 106 , Issue 3 , June 2016 , pp. 279 - 291
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Copyright © Cambridge University Press 2015 

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References

Agrawal, S., Kelkenberg, M., Begum, K., Steinfeld, L., Williams, C.E., Kramer, K.J., Beeman, R.W., Park, Y., Muthukrishnan, S. & Merzendorfer, H. (2014) Two essential peritrophic matrix proteins mediate matrix barrier functions in the insect midgut. Insect Biochemistry and Molecular Biology 49, 24–34.CrossRefGoogle ScholarPubMed
Albuquerque-Cunha, J.M., Mello, C.B., Garcia, E.S., Azambuja, P., de Souza, W., Gonzalez, M.S. & Nogueira, N.F. (2004) Effect of blood components, abdominal distension, and ecdysone therapy on the ultrastructural organization of posterior midgut epithelial cells and perimicrovillar membranes in Rhodnius prolixus. Memórias do Instituto Oswaldo Cruz 99, 815–822.Google Scholar
Albuquerque-Cunha, J.M., Gonzalez, M.S., Garcia, E.S., Mello, C.B., Azambuja, P., Almeida, J.C., de Souza, W. & Nogueira, N.F. (2009) Cytochemical characterization of microvillar and perimicrovillar membranes in the posterior midgut epithelium of Rhodnius prolixus. Arthropod Structure and Development 38, 31–44.Google Scholar
Allahyari, M., Bandani, A.R. & Habibi-Rezaei, M. (2010) Subcellular fractionation of midgut cells of the sunn pest Eurygaster integriceps (Hemiptera: Scutelleridae): enzyme markers of microvillar and perimicrovillar membranes. Journal of Insect Physiology 56, 710–717.Google Scholar
Alves, C.R., Albuquerque-Cunha, J.M., Mello, C.B., Garcia, E.S., Nogueira, N.F., Bourguingnon, S.C., de Souza, W., Azambuja, P. & Gonzalez, M.S. (2007) Trypanosoma cruzi: attachment to perimicrovillar membrane glycoproteins of Rhodnius prolixus. Experimental Parasitology 116, 44–52.Google Scholar
Ashford, D.A., Smith, W.A. & Douglas, A.E. (2000) Living on a high sugar diet: the fate of sucrose ingested by a phloem-feeding insect, the pea aphid Acyrthosiphon pisum. Journal of Insect Physiology 46, 335–341.Google Scholar
Azambuja, P., Feder, D. & Garcia, E.S. (1993) Effects of erythrocyte component diets on ecdysteroid production and ecdysis of Rhodnius prolixus larvae. Journal of Insect Physiology 39, 13–16.Google Scholar
Azambuja, P., Ratcliffe, N.A. & Garcia, E.S. (2005) Towards an understanding of the interactions of Trypanosoma cruzi and Trypanosoma rangeli within the reduviid insect host Rhodnius prolixus. Anais da Academia Brasileira de Ciências 77, 397–404.Google Scholar
Azevedo, D.O., Neves, C.A., Mallet, J.R., dos, S., Gonçalves, T.C.M., Zanuncio, J.C. & Serrão, J.E. (2009) Notes on midgut ultrastructure of Cimex hemipterus (Hemiptera: Cimicidae). Journal of Medical Entomology 46, 435–441.Google Scholar
Balbiani, E.G. (1890) Études anatomiques et histologiques sur le tube digestif des Cryotops. Archives of Zoological Experimental Genetics Notes Review 8, 1–82.Google Scholar
Balczun, C., Siemanowski, J., Pausch, J.K., Helling, S., Marcus, K., Stephan, C., Meyer, H.E., Schneider, T., Cizmowski, C., Oldenburg, M., Höhn, S., Meiser, C.K., Schuhmann, W. & Schaub, G.A. (2012) Intestinal aspartate proteases TiCatD and TiCatD2 of the haematophagous bug Triatoma infestans (Reduviidae): sequence characterization, expression pattern and characterization of proteolytic activity. Insect Biochemistry and Molecular Biology 42, 240–250.CrossRefGoogle ScholarPubMed
Bifano, T.D., Alegria, T.G.P. & Terra, W.R. (2010) Transporters involved in glucose and water absorption in the Dysdercus peruvianus (Hemiptera: Pyrrhocoridae) anterior midgut. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 157, 1–9.CrossRefGoogle ScholarPubMed
Billingsley, P.F. (1990) The midgut ultrastructure of hematophagous insects. Annual Review of Entomology 35, 219–248.Google Scholar
Billingsley, P.F. & Downe, A.E. (1986) The surface morphology of the midgut cells of Rhodnius prolixus Stål (Hemiptera: Reduviidae) during blood digestion. Acta Tropica 43, 355–366.Google ScholarPubMed
Billingsley, P.F. & Downe, A.E.R. (1988) Ultrastructural localisation of cathepsin B in the midgut of Rhodnius prolixus Stål (Hemiptera: Reduviidae) during blood digestion. International Journal of Insect Morphology and Embryology 17, 295–302.Google Scholar
Billingsley, P.F. & Lehane, M.J. (1996) Structure and ultrastructure of the insect midgut. pp. 3–30in Lehane, M.J. & Billingsley, P.F. (Eds) Biology of the Insect Midgut. London, Chapman and Hall.Google Scholar
Bittencourt-Cunha, P.R., Silva-Cardoso, L., de Oliveira, G.A., da Silva, J.R., da Silveira, A.B., Kluck, G.E.G., Souza-Lima, M., Gondim, K.C., Dansa-Petretsky, M., Silva, C.P., Masuda, H., da Silva, M.A.C. & Atella, G.C. (2013) Perimicrovillar membrane assembly: the fate of phospholipids synthesised by the midgut of Rhodnius prolixus. Memórias do Instituto Oswaldo Cruz 108, 494–500.Google Scholar
Bolognesi, R., Terra, W.R. & Ferreira, C. (2008) Peritrophic membrane role in enhancing digestive efficiency: theoretical and experimental models. Journal of Insect Physiology 54, 1413–1422.CrossRefGoogle ScholarPubMed
Bonay, P., Molina, R. & Fresno, M. (2001) Binding specificity of mannose-specific carbohydrate-binding protein from the cell surface of Trypanosoma cruzi. Glycobiology 11, 719–729.Google Scholar
Bower, S.M. & Woo, P.T.K. (1981) Development of Trypanosoma (Schizotrypanum) hedricki in Cimex brevis (Hemiptera: Cimicidae). Canadian Journal of Zoology 59, 546–554.Google Scholar
Brenière, S.F., Aznar, C. & Hontebeyrie, M. (2010) Vector transmission. pp. 525–538in Telleria, J. & Tibayrenc, M. (Eds) American Trypanosomiasis: Chagas Disease One Hundred Years of Research. New York, Elsevier.Google Scholar
Burgos, M.H. & Gutiérrez, L.S. (1976) The intestine of Triatoma infestans. I. Cytology of the midgut. Journal of Ultrastructure Research 57, 1–9.Google Scholar
Burgos, M.H., Gutierrez, L.S., Lammel, E. & Isola, E.L.D. (1989) Midgut extract rich in peritrophic membrane from Triatoma infestans induces differentiation of Trypanosoma cruzi. Microscopia Eletronica et Biologia Celular 13, 151–166.Google Scholar
Burton, G.J. (1963) Bedbugs in relation to transmission of human diseases. Public Health Reports 78, 513–524.Google Scholar
Castro, D.P., Moraes, C.S., Gonzalez, M.S., Ratcliffe, N.A., Azambuja, P. & Garcia, E.S. (2012) Trypanosoma cruzi immune response modulation decrease microbiota in Rhodnius prolixus gut and is crucial for parasite survival and development. Plos One 7, e36591.Google Scholar
Chapman, R.F. (1998) The Insects: Structure and Function. 4th edn.Cambridge, UK, Cambridge University Press.Google Scholar
Chang, X. & Chao, D. (1999) Comparative study on the insect forms of a low virulence isolate of Trypanosoma cruzi (Kinetoplastida: Trypanosomatidae) developed in cimicid bugs and in its regular insect vector species. Chinese Journal of Entomology 19, 145–152.Google Scholar
Cortez, M.R., Gonzalez, M.S., Cabral, M.M., Garcia, E.S. & Azambuja, P. (2002) Dynamic development of Trypanosoma cruzi in Rhodnius prolixus: role of decapitation and ecdysone therapy. Parasitology Research 88, 697–703.Google Scholar
Cortez, M.R., Provençano, A., Silva, C.E., Mello, C.B., Zimmermann, L.T., Schaub, G.A., Garcia, E.S., Azambuja, P. & Gonzalez, M.S. (2012) Trypanosoma cruzi: effects of azadirachtin and ecdysone on the dynamic development in Rhodnius prolixus larvae. Experimental Parasitology 131, 363–371.Google Scholar
Cranston, P.S. & Gullan, P.J. (2009) Phylogeny of insects. pp. 780–793in Resh, V.H. & Cardé, R.T. (Eds) Encyclopedia of Insects. New York, Academic Press.CrossRefGoogle Scholar
Cristofoletti, P.T., Ribeiro, A.F., Deraison, C., Rahbé, Y. & Terra, W.R. (2003) Midgut adaptation and digestive enzyme distribution in a phloem feeding insect, the pea aphid Acyrthosiphon pisum. Journal of Insect Physiology 49, 11–24.Google Scholar
Damasceno-Sá, J.C., Carneiro, C.N.B., DaMatta, R.A., Samuels, R.I., Terra, W.R. & Silva, C.P. (2007) Biphasic perimicrovillar membrane production following feeding by previously starved Dysdercus peruvianus (Hemiptera: Pyrrhocoridae). Journal of Insect Physiology 53, 592–600.Google Scholar
Dedryver, C.A., Le Ralec, A. & Fabre, F. (2010) The conflicting relationships between aphids and men: a review of aphid damage and control strategies. Comptes Rendus Biologies 333, 539–553.CrossRefGoogle Scholar
Del Bene, G., Dallai, R. & Marchini, D. (1991) Ultrastructure of the midgut and the adhering tubular salivary glands of Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). International Journal of Insect Morphology and Embryology 20, 15–24.Google Scholar
Dinglasan, R.R. & Jacobs-Lorena, M. (2005) Insight into a conserved lifestyle: protein-carbohydrate adhesion strategies of vector-borne pathogens. Infection and Immunity 73, 7797–7807.Google Scholar
Douglas, A.E. (2003) The nutritional physiology of aphids. Advances in Insect Physiology 31, 73–140.CrossRefGoogle Scholar
Dow, J.A.T. (1987) Insect midgut function. Advances in Insect Physiology 19, 187–328.Google Scholar
East, I.J., Fitzgerald, C.J., Pearson, R.D., Donaldson, R.A., Vuocolo, T., Cadogan, L.C., Tellam, R.L. & Eisemann, C.H. (1993) Lucilia cuprina: inhibition of larval growth induced by immunization of host sheep with extracts of larval peritrophic membrane. International Journal for Parasitology 23, 221–229.Google Scholar
Eisemann, C.H. & Binnington, K.C. (1994) The peritrophic membrane: its formation, structure, chemical composition and permeability in relation to vaccination against ectoparasitic arthropods. International Journal for Parasitology 24, 15–26.Google Scholar
Eisemann, C.H., Pearson, R.D., Donaldson, R.A., Cadogan, L.C. & Vuocolo, T. (1993) Uptake and fate of specific antibody in feeding larvae of the sheep blowfly, Lucilia cuprina. Medical and Veterinary Entomology 7, 177–185.Google Scholar
Ferreira, C., Ribeiro, A.F., Garcia, E.S. & Terra, W.R. (1988) Digestive enzymes trapped between and associated with the double plasma membranes of Rhodnius prolixus posterior midgut cells. Insect Biochemistry 18, 521–530.Google Scholar
Ferreira, C., Capella, A.N., Sitnik, R. & Terra, W.R. (1994) Properties of the digestive enzymes and the permeability of the peritrophic membrane of Spodoptera frugiperda (Lepidoptera) larvae. Comparative Biochemistry and Physiology Part A: Physiology 107, 631–640.Google Scholar
Fialho, M. do C.Q., Zanuncio, J.C., Neves, C.A., Ramalho, F.S. & Serrão, J.E. (2009) Ultrastructure of the digestive cells in the midgut of the predator Brontocoris tabidus (Heteroptera: Pentatomidae) after different feeding periods on prey and plants. Annals of the Entomological Society of America 102, 119–127.Google Scholar
Fialho, M.C.Q., Moreira, N.R., Zanuncio, J.C., Ribeiro, A.F., Terra, W.R. & Serrão, J.E. (2012) Prey digestion in the midgut of the predatory bug Podisus nigrispinus (Hemiptera: Pentatomidae). Journal of Insect Physiology 58, 850–856.Google Scholar
Fialho, M. do C.Q., Terra, W.R., Moreira, N.R., Zanuncio, J.C. & Serrão, J.E. (2013) Ultrastructure and immunolocalization of digestive enzymes in the midgut of Podisus nigrispinus (Heteroptera: Pentatomidae). Arthropod Structure and Development 42, 277–285.Google Scholar
Fonseca, F.V., Silva, J.R., Samuels, R.I., Da Matta, R.A., Terra, W.R. & Silva, C.P. (2010) Purification and partial characterization of a midgut membrane-bound α-glucosidase from Quesada gigas (Hemiptera: Cicadidae). Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 155, 20–25.Google Scholar
Foy, B.D., Magalhaes, T., Injera, W.E., Sutherland, I., Devenport, M., Thanawastien, A., Ripley, D., Cárdenas-Freytag, L. & Beier, J.C. (2003) Induction of mosquitocidal activity in mice immunized with Anopheles gambiae midgut cDNA. Infection and Immunity 71, 2032–2040.Google Scholar
Garcia, E.S. & Azambuja, P. (1991) Development and interactions of Trypanosoma cruzi within the insect vector. Parasitology Today 7, 240–244.Google Scholar
Garcia, E.S., Gonzalez, M.S., Azambuja, P. & Rembold, H. (1989) Chagas’ disease and its insect vector. Effect of azadirachtin A on the interaction of a triatomine host (Rhodnius prolixus) and its parasite (Trypanosoma cruzi). Zeitschrift für Naturforschung. C, Journal of Biosciences 44, 317–322.Google Scholar
Garcia, E.S., Azambuja, P., de Souza, W., Feder, D., Nogueira, N.F. & Gonzalez, M.S. (1998) Role of the head in the ultrastructural midgut organization in Rhodnius prolixus larvae: evidence from head transplantation experiments and ecdysone therapy. Journal of Insect Physiology 44, 553–560.Google Scholar
Garcia, E.S., Ratcliffe, N.A., Whitten, M.M., Gonzalez, M.S. & Azambuja, P. (2007) Exploring the role of insect host factors in the dynamics of Trypanosoma cruzi–Rhodnius prolixus interactions. Journal of Insect Physiology 53, 11–21.Google Scholar
Garcia, E.S., Genta, F.A., Azambuja, P. & Schaub, G.A. (2010) Interactions between intestinal compounds of triatomines and Trypanosoma cruzi. Trends in Parasitology 26, 499–505.Google Scholar
Gardner, R.A. & Molyneux, D.H. (1988) Trypanosoma (Megatrypanum) incertum from Pipistrellus pipistrellus: development and transmission by cimicid bugs. Parasitology 96, 433–447.Google Scholar
Geer, L.Y., Domrachev, M., Lipman, D.J. & Bryant, S.H. (2002) CDART: protein homology by domain architecture. Genome Research 12, 1619–1623.Google Scholar
Gillott, C. (1995) Entomology. 2nd edn. New York, Springer.Google Scholar
Gonzalez, M.S. & Garcia, E.S. (1992) Effect of azadirachtin on the development of Trypanosoma cruzi in different species of triatomine insect vectors: long-term and comparative studies. Journal of Invertebrate Pathology 60, 201–205.Google Scholar
Gonzalez, M.S., Nogueira, N.F., Mello, C.B., de Souza, W., Schaub, G.A., Azambuja, P. & Garcia, E.S. (1999) Influence of brain and azadirachtin on Trypanosoma cruzi development in the vector, Rhodnius prolixus. Experimental Parasitology 92, 100–108.Google Scholar
Gonzalez, M.S., Hamedi, A., Albuquerque-Cunha, J.M., Nogueira, N.F., de Souza, W., Ratcliffe, N.A., Azambuja, P., Garcia, E.S. & Mello, C.B. (2006) Antiserum against perimicrovillar membranes and midgut tissue reduces the development of Trypanosoma cruzi in the insect vector, Rhodnius prolixus. Experimental Parasitology 114, 297–304.Google Scholar
Goddard, J., & deShazo, R. (2009) Bed bugs (Cimex lectularius) and clinical consequences of their bites. Journal of the American Medical Association 301, 1358–1366.CrossRefGoogle ScholarPubMed
Gutiérrez-Cabrera, A.E., Alejandre-Aguilar, R., Hernández-Martínez, S. & Espinoza, B. (2014) Development and glycoprotein composition of the perimicrovillar membrane in Triatoma (Meccus) pallidipennis (Hemiptera: Reduviidae). Arthropod Structure and Development 43, 571–578.Google Scholar
Hegedus, D., Erlandson, M., Gillott, C. & Toprak, U. (2009) New insights into peritrophic matrix synthesis, architecture and function. Annual Review of Entomology 54, 285–302.CrossRefGoogle ScholarPubMed
Jacobson, R.L. & Doyle, R.J. (1996) Lectin-parasite interactions. Parasitology Today 12, 55–61.Google Scholar
Kitajima, E.W. (1975) A peculiar type of glycocalyx on the microvilli of the midgut epithelial cells of the thrips Frankliniella sp. (Thysanoptera: Thripidae). Cytobiologie 11, 299–303.Google Scholar
Kollien, A. & Schaub, G.A. (2000) The development of Trypanosoma cruzi in Triatominae. Parasitology Today 16, 381–387.Google Scholar
Kollien, A.H., Schmidt, J. & Schaub, G.A. (1998) Modes of association of Trypanosoma cruzi with the intestinal tract of the vector Triatoma infestans. Acta Tropica 70, 127–141.Google Scholar
Kollien, A.H., Waniek, P.J., Pröls, F., Habedank, B. & Schaub, G.A. (2004) Cloning and characterization of a trypsin-encoding cDNA of the human body louse Pediculus humanus. Insect Molecular Biology 13, 9–18.Google Scholar
Kuraishi, T., Binggeli, O., Opota, O., Buchon, N. & Lemaitre, B. (2011) Genetic evidence for a protective role of the peritrophic matrix against intestinal bacterial infection in Drosophila melanogaster. Proceedings of the National Academy of Sciences 108, 15966–15971.Google Scholar
Lehane, M.J. (1997) Peritrophic matrix structure and function. Annual Review of Entomology 42, 525–550.Google Scholar
Lehane, M.J. & Billingsley, P.F. (Eds) (1996) Biology of the Insect Midgut. London, Chapman & Hall.Google Scholar
Lane, N.J. & Harrison, J.B. (1979) An unusual cell surface modification: a double plasma membrane. Journal of Cell Science 39, 355–372.Google Scholar
Liu, X., Zhang, H., Li, S., Zhu, K.Y., Ma, E. & Zhang, J. (2012) Characterization of a midgut-specific chitin synthase gene (LmCHS2) responsible for biosynthesis of chitin of peritrophic matrix in Locusta migratoria. Insect Biochemistry and Molecular Biology 42, 902–910.Google Scholar
Marques-Silva, S., Serrão, J.E. & Mezêncio, J.M.S. (2005) Peritrophic membrane protein in the larval stingless bee Melipona quadrifasciata anthidioides: immunolocalization of secretory sites. Acta Histochemica 107, 23–30.Google Scholar
Mehrabadi, M. & Bandani, A.R. (2011) Secretion and formation of perimicrovillar membrane in the digestive system of the sunn pest, Eurygaster integriceps (Hemiptera: Scutelleridae) in response to feeding. Archives of Insect Biochemistry and Physiology 78, 190–200.Google Scholar
Misof, B., Liu, S., Meusemann, K., Peters, R.S., Donath, A., Mayer, C., Frandsen, P.B., Ware, J., Flouri, T., Beutel, R.G., Niehuis, O., Petersen, M., Izquierdo-Carrasco, F., Wappler, T., Rust, J., Aberer, A.J., Aspöck, U., Aspöck, H., Bartel, D., Blanke, A., Berger, S., Böhm, A., Buckley, T.R., Calcott, B., Chen, J., Friedrich, F., Fukui, M., Fujita, M., Greve, C., Grobe, P., Gu, S., Huang, Y., Jermiin, L.S., Kawahara, A.Y., Krogmann, L., Kubiak, M., Lanfear, R., Letsch, H., Li, Y., Li, Z., Li, J., Lu, H., Machida, R., Mashimo, Y., Kapli, P., McKenna, D.D., Meng, G., Nakagaki, Y., Navarrete-Heredia, J.L., Ott, M., Ou, Y., Pass, G., Podsiadlowski, L., Pohl, H., Reumont, B.M. von, Schütte, K., Sekiya, K., Shimizu, S., Slipinski, A., Stamatakis, A., Song, W., Su, X., Szucsich, N.U., Tan, M., Tan, X., Tang, M., Tang, J., Timelthaler, G., Tomizuka, S., Trautwein, M., Tong, X., Uchifune, T., Walzl, M.G., Wiegmann, B.M., Wilbrandt, J., Wipfler, B., Wong, T.K.F., Wu, Q., Wu, G., Xie, Y., Yang, S., Yang, Q., Yeates, D.K., Yoshizawa, K., Zhang, Q., Zhang, R., Zhang, W., Zhang, Y., Zhao, J., Zhou, C., Zhou, L., Ziesmann, T., Zou, S., Li, Y., Xu, X., Zhang, Y., Yang, H., Wang, J., Wang, J., Kjer, K.M. & Zhou, X. (2014) Phylogenomics resolves the timing and pattern of insect evolution. Science 346, 763–767.Google Scholar
Moussian, B. (2013) The apical plasma membrane of chitin-synthesizing epithelia. Insect Science 20, 139–146.Google Scholar
Mury, F.B., da Silva, J.R., Ferreira, L.S., Ferreira, B., dos, S., de Souza-Filho, G.A., de Souza-Neto, J.A., Ribolla, P.E.M., Silva, C.P., do Nascimento, V.V., Machado, O.L.T., Berbert-Molina, M.A. & Dansa-Petretski, M. (2009) Alpha-glucosidase promotes hemozoin formation in a blood-sucking bug: an evolutionary history. PLoS ONE 4, e6966.Google Scholar
Nogueira, N.F., Gonzales, M., Garcia, E.M. & de Souza, W. (1997) Effect of azadirachtin A on the fine structure of the midgut of Rhodnius prolixus. Journal of Invertebrate Pathology 69, 58–63.Google Scholar
Nogueira, N.F., Gonzalez, M.S., Gomes, J.E., de Souza, W., Garcia, E.S., Azambuja, P., Nohara, L.L., Almeida, I.C., Zingales, B. & Colli, W. (2007) Trypanosoma cruzi: involvement of glycoinositolphospholipids in the attachment to the luminal midgut surface of Rhodnius prolixus. Experimental Parasitology 116, 120–128.Google Scholar
Oliveira, M.F., Silva, J.R., Dansa-Petretski, M., de Souza, W., Braga, C.M.S., Masuda, H. & Oliveira, P.L. (2000) Haemozoin formation in the midgut of the blood-sucking insect Rhodnius prolixus. FEBS Letters 477, 95–98.Google Scholar
Otranto, D. & Stevens, J.R. (2002) Molecular approaches to the study of myiasis-causing larvae. International Journal for Parasitology 32, 1345–1360.Google Scholar
Parrella, G., Gognalons, P., Gebre-Selassie, K., Vovlas, C. & Machoux, G. (2003) An update of the host range of Tomato spotted wilt virus. Journal of Plant Pathology 85, 227–264.Google Scholar
Pereira, M.E., Andrade, A.F. & Ribeiro, J.M. (1981) Lectins of distinct specificity in Rhodnius prolixus interact selectively with Trypanosoma cruzi. Science 211, 597–600.Google Scholar
Peters, W. (1992) Peritrophic Membrane. Zoophysiology Series. Berlin, Springer Verlag.Google Scholar
Pinheiro, D.O., Quagio-Grassiotto, I. & Gregório, E.A. (2008) Morphological regional differences of epithelial cells along the midgut in Diatraea saccharalis Fabricius (Lepidoptera: Crambidae) larvae. Neotropical Entomology 37, 413–419.Google Scholar
Reger, J.F. (1971) Fine structure of the surface coat of midgut epithelial cells in the homopteran, Phylloscelis atra (Fulgorid). Journal of Submicroscopic Cytology 3, 353–358.Google Scholar
Reinhardt, K. & Siva-Jothy, M.T. (2007) Biology of the bed bugs (Cimicidae). Annual Review of Entomology 52, 351–374.Google Scholar
Riley, D.G., Joseph, S.V., Srinivasan, R. & Diffie, S. (2011) Thrips vectors of Tospoviruses. Journal of Integrated Pest Management 1, I1–I10.Google Scholar
Rudin, W. & Hecker, H. (1989) Lectin-binding sites in the midgut of the mosquitoes Anopheles stephensi Liston and Aedes aegypti L. (Diptera: Culicidae). Parasitology Research 75, 268–279.Google Scholar
Ryckman, R.E., Bentley, D.G. & Archbold, E.F. (1981) The Cimicidae of the Americas and Oceanic Islands: a checklist and bibliography. Bulletin of the Society for Vector Ecology 6, 93–142.Google Scholar
Salazar, R., Castillo-Neyra, R., Tustin, A.W., Borrini-Mayorí, K., Náquira, C. & Levy, M.Z. (2015) Bed bugs (Cimex lectularius) as vectors of Trypanosoma cruzi. The American Journal of Tropical Medicine and Hygiene 92, 331–335.Google Scholar
Schaub, G.A. (1989) Does Trypanosoma cruzi stress its vectors? Parasitology Today 5, 185–188.Google Scholar
Shipp, J.L., Hao, X., Papadopoulos, A.P. & Binns, M.R. (1998) Impact of western flower thrips (Thysanoptera: Thripidae) on growth, photosynthesis and productivity of greenhouse sweet pepper. Scientia Horticulturae 72, 87–102.CrossRefGoogle Scholar
Silva, C.P. & Terra, W.R. (1994) Digestive and absorptive sites along the midgut of the cotton seed sucker bug Dysdercus peruvianus (Hemiptera: Pyrrhocoridae). Insect Biochemistry and Molecular Biology 24, 493–505.Google Scholar
Silva, C.P. & Terra, W.R. (1995) An α-glucosidase from perimicrovillar membranes of Dysdercus peruvianus (Hemiptera: Pyrrhocoridae) midgut cells. Purification and properties. Insect Biochemistry and Molecular Biology 25, 487–494.CrossRefGoogle Scholar
Silva, C.P., Ribeiro, A.F., Gulbenkian, S. & Terra, W.R. (1995) Organization, origin and function of the outer microvillar (perimicrovillar) membranes of Dysdercus peruvianus (Hemiptera) midgut cells. Journal of Insect Physiology 41, 1093–1103.Google Scholar
Silva, C.P., Silva, J.R., Vasconcelos, F.F., Petretski, M.D.A., Damatta, R.A., Ribeiro, A.F. & Terra, W.R. (2004) Occurrence of midgut perimicrovillar membranes in paraneopteran insect orders with comments on their function and evolutionary significance. Arthropod Structure and Development 33, 139–148.Google Scholar
Silva, J.R., Mury, F.B., Oliveira, M.F., Oliveira, P.L., Silva, C.P. & Dansa-Petretski, M. (2007) Perimicrovillar membranes promote hemozoin formation into Rhodnius prolixus midgut. Insect Biochemistry and Molecular Biology 37, 523–531.Google Scholar
Silverman, A.L., Qu, L.H., Blow, J., Zitron, I.M., Gordon, S.C. & Walker, E.D. (2001) Assessment of hepatitis B virus DNA and hepatitis C virus RNA in the common bedbug (Cimex lectularius L.) and kissing bug (Rodnius prolixus). The American Journal of Gastroenterology 96, 2194–2198.Google Scholar
Takano-Lee, M. & Edman, J.D. (2002) Lack of manipulation of Rhodnius prolixus (Hemiptera: Reduviidae) vector competence by Trypanosoma cruzi. Journal of Medical Entomology 39, 44–51.Google Scholar
Teixeira, A., das, D., Marques-Araújo, S., Zanuncio, J.C. & Serrão, J.E. (2015) Peritrophic membrane origin in adult bees (Hymenoptera): immunolocalization. Micron 68, 91–97.Google Scholar
Tellam, W.R. (1996) The peritrophic matrix. pp. 86–114in Lehane, M.J. & Billingsley, P.F. (Eds) Biology of the Insect Midgut. London, Chapman & Hall.Google Scholar
Tellam, R.L. & Eisemann, C.H. (1998) Inhibition of growth of Lucilia cuprina larvae using serum from sheep vaccinated with first-instar larval antigens. International Journal for Parasitology 28, 439–450.Google Scholar
Tellam, R.L., Wijffels, G. & Willadsen, P. (1999) Peritrophic matrix proteins. Insect Biochemistry and Molecular Biology 29, 87–101.Google Scholar
Terra, W.R. (1988) Physiology and biochemistry of insect digestion: an evolutionary perspective. Brazilian Journal of Medical and Biological Research 21, 675–734.Google Scholar
Terra, W.R. (1990) Evolution of digestive systems of insects. Annual Review of Entomology 35, 181–200.Google Scholar
Terra, W.R. (2001) The origin and functions of the insect peritrophic membrane and peritrophic gel. Archives of Insect Biochemistry and Physiology 47, 47–61.Google Scholar
Terra, W.R. & Ferreira, C. (1994) Insect digestive enzymes: properties, compartmentalization and function. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry 109, 1–62.Google Scholar
Terra, W.R. & Ferreira, C. (2005) Biochemistry of digestion. pp. 171–224in Gilbert, L.I. & Latrou, K., Gill, S.S. (Eds) Comprehensive Molecular Insect Science, vol. 4. Oxford, Elsevier.Google Scholar
Terra, W.R. & Ferreira, C. (2009) Digestive system. pp. 365–419in Resh, V.H. & Cardé, R.T. (Eds) Encyclopedia of Insects. 2nd edn. San Diego, Academic Press.Google Scholar
Terra, W.R. & Ferreira, C. (2012) Biochemistry and molecular biology of digestion. pp. 365–418in Gilbert, L.I. (Ed) Insect Molecular Biology and Biochemistry. New York, Elsevier.Google Scholar
Terra, W.R., Valentin, A. & Santos, C.D. (1987) Utilization of sugars, hemicellulose, starch, protein, fat and minerals by Erinnyis ello larvae and the digestive role of their midgut hydrolases. Insect Biochemistry 17, 1143–1147.CrossRefGoogle Scholar
Terra, W.R., Ferreira, C. & Baker, J.E. (1996) Compartmentalization of digestion. pp. 206–234in Lehane, M.J. & Billingsley, P.F. (Eds) Biology of the Insect Midgut. London, Chapman & Hall.Google Scholar
Terra, W.R., Costa, R.H. & Ferreira, C. (2006) Plasma membranes from insect midgut cells. Anais da Academia Brasileira de Ciências 78, 255–269.Google Scholar
Ullman, D.E., Westcot, D.M., Hunter, W.B. & Mau, R.F.L. (1989) Internal anatomy and morphology of Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) with special reference to interactions between thrips and tomato spotted wilt virus. International Journal of Insect Morphology and Embryology 18, 289–310.Google Scholar
Ullman, D.E., Meideros, R., Campbell, L.R., Whitfield, A.E., Sherwood, J.L. & German, T.L. (2002) Thrips as vectors of Tospoviruses. Advances in Botanical Research 36, 113–140.Google Scholar
Waniek, P.J. (2009) The digestive system of human lice: current advances and potential applications. Physiological Entomology 34, 203–210.Google Scholar
Waniek, P.J., Hendgen-Cotta, U.B., Stock, P., Mayer, C., Kollien, A.H. & Schaub, G.A. (2005) Serine proteinases of the human body louse (Pediculus humanus): sequence characterization and expression patterns. Parasitology Research 97, 486–500.Google Scholar
Wheeler, W.C., Whiting, M., Wheeler, Q.D. & Carpenter, J.M. (2001) The phylogeny of the extant hexapod orders. Cladistics 17, 113–169.Google Scholar
WHO (2015) Chagas disease. Available online at http://www.who.int/mediacentre/factsheets/fs340/en/. (Accessed 3 August 2015).Google Scholar
Wijffels, G., Hughes, S., Gough, J., Allen, J., Don, A., Marshall, K., Kay, B. & Kemp, D. (1999) Peritrophins of adult dipteran ectoparasites and their evaluation as vaccine antigens. International Journal for Parasitology 29, 1363–1377.Google Scholar
Wu, D., Daugherty, S.C., Van Aken, S.E., Pai, G.H., Watkins, K.L., Khouri, H., Tallon, L.J., Zaborsky, J.M., Dunbar, H.E., Tran, P.L., Moran, N.A. & Eisen, J.A. (2006) Metabolic complementarity and genomics of the dual bacterial symbiosis of sharpshooters. PLoS Biol 4, e188.Google Scholar
Zhong, H., Zhang, Y. & Wei, C. (2013) Anatomy and fine structure of the alimentary canal of the spittlebug Lepyronia coleopterata (L.) (Hemiptera: Cercopoidea). Arthropod Structure and Development 42, 521–530.Google Scholar