Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2024-12-24T11:20:15.355Z Has data issue: false hasContentIssue false
  • English
  • Français

Immune defence mechanisms of triatomines against bacteria, viruses, fungi and parasites

Published online by Cambridge University Press:  17 June 2015

A.L. Flores-Villegas ,
P.M. Salazar-Schettino ,
A. Córdoba-Aguilar ,
A.E. Gutiérrez-Cabrera ,
G.E. Rojas-Wastavino ,
M.I. Bucio-Torres  and
M. Cabrera-Bravo
A.L. Flores-Villegas
Affiliation:
Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autónoma de México, Circuito Interior, Avenida Universidad 3000, Ciudad Universitaria, 04510, Coyoacán, Distrito Federal, México
P.M. Salazar-Schettino
Affiliation:
Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autónoma de México, Circuito Interior, Avenida Universidad 3000, Ciudad Universitaria, 04510, Coyoacán, Distrito Federal, México
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, México
A.E. Gutiérrez-Cabrera
Affiliation:
Departamento de Bioquímica, Facultad de Medicina, Universidad Nacional Autónoma de México, Ciudad Universitaria, 04510, Coyoacán, Distrito Federal, México
G.E. Rojas-Wastavino
Affiliation:
Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autónoma de México, Circuito Interior, Avenida Universidad 3000, Ciudad Universitaria, 04510, Coyoacán, Distrito Federal, México
M.I. Bucio-Torres
Affiliation:
Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autónoma de México, Circuito Interior, Avenida Universidad 3000, Ciudad Universitaria, 04510, Coyoacán, Distrito Federal, México
M. Cabrera-Bravo*
Affiliation:
Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autónoma de México, Circuito Interior, Avenida Universidad 3000, Ciudad Universitaria, 04510, Coyoacán, Distrito Federal, México
*
*Authors for correspondence Phone: 52 (55) 56232464 and 56232468 E-mail: [email protected] Phone: 52 (55) 56229003 E-mail: [email protected]
*Authors for correspondence Phone: 52 (55) 56232464 and 56232468 E-mail: [email protected] Phone: 52 (55) 56229003 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Triatomines are vectors that transmit the protozoan haemoflagellate Trypanosoma cruzi, the causative agent of Chagas disease. The aim of the current review is to provide a synthesis of the immune mechanisms of triatomines against bacteria, viruses, fungi and parasites to provide clues for areas of further research including biological control. Regarding bacteria, the triatomine immune response includes antimicrobial peptides (AMPs) such as defensins, lysozymes, attacins and cecropins, whose sites of synthesis are principally the fat body and haemocytes. These peptides are used against pathogenic bacteria (especially during ecdysis and feeding), and also attack symbiotic bacteria. In relation to viruses, Triatoma virus is the only one known to attack and kill triatomines. Although the immune response to this virus is unknown, we hypothesize that haemocytes, phenoloxidase (PO) and nitric oxide (NO) could be activated. Different fungal species have been described in a few triatomines and some immune components against these pathogens are PO and proPO. In relation to parasites, triatomines respond with AMPs, including PO, NO and lectin. In the case of T. cruzi this may be effective, but Trypanosoma rangeli seems to evade and suppress PO response. Although it is clear that three parasite-killing processes are used by triatomines – phagocytosis, nodule formation and encapsulation – the precise immune mechanisms of triatomines against invading agents, including trypanosomes, are as yet unknown. The signalling processes used in triatomine immune response are IMD, Toll and Jak-STAT. Based on the information compiled, we propose some lines of research that include strategic approaches of biological control.

Keywords

Triatomineantimicrobial peptidesphenoloxidasenitric oxidehaemocytepathogens
Type
Review Paper
Information
Bulletin of Entomological Research , Volume 105 , Issue 5 , October 2015 , pp. 523 - 532
Check for updates
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Araújo, C.A.C., Waniek, P.J., Stock, P., Mayer, C., Jansen, A.M. & Schaub, G.A. (2006) Sequence characterization and expression patterns of defensin and lysozyme encoding genes from the gut of the reduviid bug Triatoma brasiliensis . Insect Biochemistry and Molecular Biology 36, 547–560.CrossRefGoogle ScholarPubMed
Avulova, S. & Rosengaus, R.B. (2011) Losing the battle against fungal infection: Supression of termite immune defenses during mycosis. Journal of Insect Physiology 57, 966–971.Google Scholar
Azambuja, P. & Garcia, E.S. (1987) Characterization of inducible lysozyme activity in the hemolymph of Rhodnius prolixus . Brazilian Journal of medical and Biological Research 20, 539–548.Google ScholarPubMed
Azambuja, P., Mello, C.B. & Feder, D. (1997) Influence of the triatominae cellular and humoral defense system on the development of trypanosomatids. pp. 709–733 in Carcavallo, R., Galíndez-Girón, I. & Jurberg, J. (Eds) Atlas of Chagas Disease Vectors in the Americas. Rio de Janeiro, Editora Fiocruz.Google Scholar
Azambuja, P., Feder, D., Mello, C.B., Gomes, S.A.O. & Garcia, E.S. (1999) Immunity in Rhodnius prolixus: Trypanosomatid–vector interactions. Memorias do Instituto Oswaldo Cruz 94, 219–222.CrossRefGoogle ScholarPubMed
Azambuja, P., Feder, D. & Garcia, E.S. (2004) Isolation of Serratia marcescens in the midgut of Rhodnius prolixus: impact on the establishment of the parasite Trypanosoma cruzi in the vector. Experimental Parasitology 107, 89–96.Google Scholar
Balczun, C., Knorr, E., Topal, H., Meiser, C.K., Kollien, A.H. & Schaub, G.A. (2008) Sequence characterization of an unusual lysozyme gene expressed in the intestinal tract of the reduviid bug Triatoma infestans (Insecta). Parasitology Research 102, 229–232.CrossRefGoogle ScholarPubMed
Beard, C.B., Dotson, E.M., Pennigton, P.M., Eichler, S., Cordon-Rosales, C. & Durvasula, R.V. (2001) Bacterial symbiosis and paratransgenic control of vector-borne Chagas disease. International Journal of Parasitology 31, 621–627.Google Scholar
Beard, C.B., Cordon-Rosales, C. & Durvasula, R.V. (2002) Bacterial symbionts of the Triatominae and their potential use in control of Chagas disease transmission. Annual Review of Entomology 47, 123–141.CrossRefGoogle ScholarPubMed
Beckage, N.E. (2011) Insect Immunology. San Diego, California, USA, Academic Press.Google Scholar
Bedding, R.A. & Molyneux, A.S. (1982) Penetration of insect cuticle by infective juveniles of Heterorhabditis spp. (Heterorhabditidae: Nematoda). Nematologica 28, 354–359.Google Scholar
Borges, A.R., Santos, P.N., Furtado, A.F. & Figueiredo, R.C.B.Q. (2008) Phagocytosis of latex beads and bacteria by hemocytes of the triatomine bug Rhodnius prolixus (Hemiptera: Reduvidae). Micron 39, 486–494.Google Scholar
Boucias, D.G. & Pendland, J.C. (1991) The fungal cell wall and its involvement in the pathogenic process in insects hosts. pp. 303–316 in Boucias, D. & Latgé, J.P. (Eds) Fungal Cell Wall and Immune Response. Berlin, Springer-Verlag.Google Scholar
Boulanger, N., Bulet, P. & Lowenberger, C. (2006) Antimicrobial peptides in the interactions between insects and flagellates parasites. Trends in Parasitology 6, 262–268.Google Scholar
Casteels, P. (1998) Immune responses in Hymenoptera. pp. 92–110 in Brey, P.T. & Hultmark, D. (Eds) Molecular Mechanisms of Immune Responses in Insects. New York, USA, Chapman & Hall.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 decreases microbiota in Rhodnius prolixus gut and is crucial for parasite survival and development. PLoS ONE 7, e36591.Google Scholar
Cator, L.J., Lynch, P.A., Read, A.F. & Thomas, M.B. (2012) Do malaria parasites manipulate mosquitoes? Trends in Parasitology 28, 466–470.Google Scholar
Cerenius, L., Lee, B.L. & Soderhall, K. (2008) The proPO-system: pros and cons for its role in invertebrate immunity. Trends in Immunology 29, 263–271.Google Scholar
Cisarovsky, G., Schmid-Hempel, P. & Sadd, B.M. (2012) Robustness of the outcome of adult bumblebee infection with a trypanosome parasite after varied parasite exposures during larval development. Journal of Evolutionary Biology 25, 1053–1059.Google Scholar
Clayton, A.M., Dong, Y. & Dimopoulos, G. (2014) The Anopheles innate immune system in the defense against malaria infection. Journal of Innate Immunity 6, 169–181.Google Scholar
Dong, Y., Taylor, H.E. & Dimopoulos, G. (2006) AgDscam, a hypervariable immunoglobulin domain-containing receptor of the Anopheles gambiae innate immune system. PLoS Biology 4, e229.Google Scholar
Dotson, E.M., Plikaytis, B., Shinnick, T.M., Durvasula, R.V. & Beard, C.B. (2003) Transformation of Rhodococcus rhodnii, a symbiont of the Chagas disease vector Rhodnius prolixus, with integrative elements of the L1 mycobacteriophage. Infection, Genetics and Evolution 3, 103–109.Google Scholar
Durvasula, R.V., Gumbs, A., Panackal, A., Kruglov, A., Taneja, J., Kang, A.S., Cordon-Rosales, C., Richards, F.F., Whitham, R.G. & Beard, C.B. (1999) Expression of a functional antibody fragment in the gut of Rhodnius prolixus via transgenic bacterial symbiont Rhodococcus rhodnii . Medical and Veterinary Entomology 13, 115–119.Google Scholar
Engstrom, P., Carlsson, A., Engstrom, Z.J.T. & Bennich, H. (1984) The antibacterial effect of attacins from the silk moth Hyalophora cecropia is directed against the outer membrane of Escherichia coli . The EMBO Journal 3, 3347–3351.Google Scholar
Fieck, A., Hurwitz, I., Kang, A.S. & Durvasula, R. (2010) Trypansoma cruzi: synergistic cytotoxicity of multiple amphipathic anti-microbial peptides to T. cruzi and potential bacterial hosts. Experimental Parasitology 125, 342–347.Google Scholar
Fujita, A. (2004) Lysozymes in insects: what role do they play in nitrogen metabolism? Physiological Entomology 29, 305–310.Google Scholar
Genta, F.A., Souza, R.S., García, E.S. & Azambuja, P. (2010) Phenol oxidases from Rhodnius prolixus: temporal and tissue expression pattern and regulation by ecdysone. Journal of Insect Physiology 56, 1253–1259.Google Scholar
Gillespie, J.P., Kanost, M.R. & Trenczek, T. (1997) Biological mediators of insect immunity. Annual Review of Entomology 42, 611–643.Google Scholar
Gillespie, J.P., Burnett, C. & Charnley, A.K. (2000) The immune response of the desert locust Schistocerca gregaria during mycosis of the entomopathogenic fungus, Metarhizium anisopliae var acridum . Journal of Insect Physiology 46, 429–437.Google Scholar
Gomes, S.A.O., Feder, D., Thomas, N.E.S., Garcia, E.S. & Azambuja, P. (1999) Rhodnius prolixus infected with Trypanosoma rangeli: in vivo and in vitro experiments. Journal of Invertebrate Pathology 73, 289–293.Google Scholar
Gomes, S.A.O., Feder, D., Garcia, E.S. & Azambuja, P. (2003) Supression of the prophenoloxidase system in Rhodnius prolixus orally infected with Trypanosoma rangeli . Journal of Insect Physiology 49, 829–837.Google Scholar
González-Santoyo, I. & Córdoba-Aguilar, A. (2012) Phenoloxidase: a key component of the insect immune system. Entomologia Experimentalis et Applicata 142, 1–16.Google Scholar
Gourbière, S., Dorn, P., Tripet, F. & Dumonteil, F. (2012) Genetics and evolution of triatomines: from phylogeny to vector control. Heredity 108, 190–202.Google Scholar
Gregorio, E.A. & Ratcliffe, N.A. (1991) The prophenoloxidase system and in vitro interaction of Trypanosoma rangeli with Rhodnius prolixus and Triatoma infestans . Parasite Immunology 13, 551–564.Google Scholar
Grisard, E.C., Teixeira, S.M.R., De Almeida, L.G.P., Stoco, P.H., Gerber, A.L., Talavera-López, C., Lima, O.C., Andersson, B. & De Vasconcelos, A.T.R. (2014) Trypanosoma cruzi clone Dm28c draft genome sequence. Genome Announcements 2, 1–2.Google Scholar
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
Hoffman, J.A. & Reichhart, J.M. (2002) Drosophila innate immunity: an evolutionary perspective. Nature Immunology 3, 121–126.Google Scholar
Hu, Y. & Aksoy, S. (2005) An antimicrobial peptide with trypanocidal activity characterized from Glossina morsitans morsitans . Insect Biochemistry and Molecular Biology 35, 105–115.Google Scholar
Hultmark, D. Steiner, H., Rasmuson, T. & Boman, H.G. (1980) Insect immunity. Purification and properties of three inducible bactericidal proteins from hemolymph of immunized pupae of Hyalophora cecropia . European Journal of Biochemistry 106, 7–16.Google Scholar
Johnson, K.N. (2015) Bacterial and antiviral immunity in insects. Current Opinion in Insect Science 8, 1–7.Google Scholar
Kingsolver, B. & Hardy, R.W. (2012) Making connections in insect innate immunity. Proceedings of the National Academy of Sciences of the United States of America 46, 18639–18640.Google Scholar
Kollien, A.H., Fechner, S., Waniek, P.J. & Schaub, G. (2003) Isolation and characterization of a cDNA encoding for a lysozyme from the gut of the Reduviid bug Triatoma infestans . Archives of Insect Biochemistry and Physiology 53, 134–145.Google Scholar
Laughton, A.M. & Siva-Jothy, M.T. (2011) A standarised protocol for measuring phenoloxidase and prophenoloxidase in the honey bee, Apis mellifera . Apidologie 42, 140–149.Google Scholar
Lavine, M.D. & Strand, M.R. (2002) Insect hemocytes and their role in immunity. Insect Biochemistry and Molecular Biology 32, 1259–1309.Google Scholar
Lopez, L., Morales, G., Ursic, R., Wolff, M. & Lowenberger, C. (2003) Isolation and characterization of a novel insect defensin from Rhodnius prolixus, a vector of Chagas disease. Insect Biochemistry and Molecular Biology 33, 439–447.Google Scholar
Mello, C.B., Garcia, E.S., Ratcliffe, N.A. & Azambuja, P. (1995) Trypanosoma cruzi and Trypanosoma rangeli interplay with hemolymph components of Rhodnius prolixus . Journal of Invertebrate Pathology 65, 261–268.Google Scholar
Michel, K. & Kafatos, F.C. (2005) Mosquito immunity against Plasmodium . Insect Biochemistry and Molecular Biology 35, 677–689.Google Scholar
Moraes, A.M.L., Junqueira, A.C.V., Costa, G.L., Celano, V. & Coura, J.R. (2000) Fungal flora of the digestive tract of 5 species of triatomines vectors of Trypanosoma cruzi, Chagas 1909. Mycopathologia 151, 41–48.Google Scholar
Moraes, A.M.L., Junqueira, A.C.V., Celano, V., Lara da Costa, G. & Rodrigues Coura, J. (2004) Fungal Flora of the digestive tract of Rhodnius prolixus, Rhodnius neglectus, Dipetalogaster maximus and Panstrongylus megistus vectors of Trypanosoma cruzi, Chagas, 1909. Brazilian Journal of Microbiology 35, 288–291.Google Scholar
Moreira, C.J.C., Waniek, P.J., Valente, R.H., Carvalho, P.C., Perales, J., Feder, D., Geraldo, R.B., Castro, H.C., Azambuja, P., Ratcliffe, N.A. & Mello, C.B. (2014) Isolation and molecular characterization of a major hemolymph serpin from the triatomine, Panstrongylus megistus . Parasites and Vectors 7, 1–16.Google Scholar
Muscio, O.A., La Torre, J.L. & Scodeller, E.A. (1987) Small nonoccluded viruses from triatominae Bug Triatoma infestans (Hemiptera: Reduviidae). Journal of Invertebrate Pathology 49, 218–220.Google Scholar
Muscio, O.A., La Torre, J.L., Bonder, M.A. & Scodeller, E.A. (1997) Triatoma virus pathogenicity in laboratory colonies of Triatoma infestans (Hemiptera: Reduviidae). Journal of Medical Entomology 34, 253–256.Google Scholar
Muscio, O., Bonder, M.A., La Torre, J.L. & Scodeller, E.A. (2000) Horizontal transmission of Triatoma virus through the fecal–oral route in Triatoma infestans (Hemiptera: Triatomidae). Journal of Medical Entomology 37, 271–275.Google Scholar
Nakamura, A., Stiebler, R., Fantappié, M.R., Fialho, E., Masuda, H. & Oliveira, M.F. (2007) Effects of retinoids and juvenoids on moult and on phenoloxidase activity in the blood-sucking insect Rhodnius prolixus . Acta Tropica 103, 222–230.Google Scholar
Nava-Sánchez, A., Munguía-Steyer, R., González-Tokman, D. & Córdoba-Aguilar, A. (2015) Does mating activity impair phagocytosis-mediated priming immune response? A test using the house cricket, Acheta domesticus . Acta Ethologica. Doi: 10.1007/s10211-015-0215-y.Google Scholar
Ourth, D.D. & Renis, H.E. (1993) Antiviral melanization reaction of Heliothis virescens hemolymph against DNA and RNA viruses in vitro . Comparative Biochemistry and Physiology 105, 719–723.Google Scholar
Querido, J.F.B., Agirre, J., Marti, G.A., Guérin, D.M. & Silva, S.M. (2013) Inoculation of Triatoma virus (Dicistroviridae: Cripavirus) elicits a non-infective immune response in mice. Parasites and Vectors 6, 1–6.Google Scholar
Rassi, A. Jr, Rassi, A. & Neto, M. (2010) Chagas disease. The Lancet 375, 1388–1402.Google Scholar
Ratcliffe, N.A., Nigam, Y., Mello, C.B., Garcia, E.S. & Azambuja, P. (1996) Trypanosoma cruzi and erythrocyte agglutinins: a comparative study of occurrence and properties in the gut and hemolymph of Rhodnius prolixus . Experimental Parasitology 83, 83–93.Google Scholar
Ribeiro, J.C.M., Genta, F.A., Sorgine, M.H.F., Logullo, R., Mesquita, R.D., Paiva-Silva, G.O., Majerowicz, D., Medeiros, M., Koerich, L., Terra, W.R., Ferreira, C., Pimentel, A.C., Bisch, P.M., Leite, D.C., Diniz, M.M.P, Lídio da, S.G.V. Junior, J., Da Silva, M.L., Araujo, R.N., Caroline, A., Gandara, P., Brosson, S., Salmon, D., Bousbata, S., González-Caballero, N. Silber, A.M., Alves-Bezerra, M., Gondim, K.C., Silva-Neto, M.A.C., Atella, G.C., Araujo, H. Dias, F.A., Polycarpo, C., Vionette-Amaral, R.J., Fampa, P., Melo, A.C.A., Tanaka, A.S., Balczun, C., Oliveira, J.H.M., Gonçalves, R.L.S., Lazoski, C., Rivera-Pomar, R., Diambra, L., Schaub, G.A., Garcia, E.S., Azambuja, P., Braz, G.R.C. & Oliveira, P.L. (2014) An insight into the transcriptome of the digestive tract of the bloodsucking Bug, Rhodnius prolixus . PloS Neglected Tropical Diseases 8, e2594.Google Scholar
Rivero, A. (2006) Nitric oxide: an antiparasitic molecule of invertebrates. Trends in Parasitology 22, 219–225.Google Scholar
Rohlfs, M. & Churchill, A.C.L. (2011) Fungal secondary metabolites as modulators of interactions with insects and other arthropods. Fungal Genetics and Biology 48, 23–34.Google Scholar
Rozas-Dennis, G.S., La Torre, J.L., Muscio, O.A. & Guérin, M.A. (2000) Direct methods for detecting Picorna-like virus from dead and alive Triatomines insects. Memorias del Instituto Oswaldo Cruz 95, 323–327.Google Scholar
Rückert, C., Bell-Sakyi, L., Fazakerley, J.K. & Fragkoudis, R. (2014) Antiviral responses of arthropod vectors: an update of recent advances. Virus Disease 25, 249–260.Google Scholar
Ruiz-Sanchez, E., Orchard, I. & Lange, A.B. (2010) Effects of the cyclopeptide mycotoxin destruxin A on the Malpighian tubules of Rhodnius prolixus (Stal). Toxicon 55, 1162–1170.Google Scholar
Sassera, D., Epis, S., Pajoro, M. & Bandi, C. (2013) Microbial symbiosis and the control of vector-borne pathogens in tsetse flies, human lice and triatomine bugs. Pathogens and Global Health 6, 285–292.Google Scholar
Schaub, G.A. (1989) Does Trypanosoma cruzi stress its vectors? Parasitology Today 5, 185–188.Google Scholar
Schaub, G.A., Meiser, C.K. & Balczun, C. (2011) Interactions of Trypanosoma cruzi and Triatomines. pp. 155–178 in Mehlhorn, H. (Ed.) Progress in Parasitology. Berlin, Springer-Verlag.Google Scholar
Schmid-Hempel, P. (2005) Evolutionary ecology of insect immune defenses. Annual Review of Entomology 50, 529–551.Google Scholar
Schofield, C.J. & Galvao, C. (2009) Classification, evolution and species groups within the Triatominae. Acta Tropica 11, 88–100.Google Scholar
Shah, P.A. & Pell, J.K. (2003) Entomopathogenic fungi as biological control agents. Applied Microbiology and Biotechnology 61, 413–423.Google Scholar
Sistrom, M., Evans, B., Bjornson, R., Gibson, W., Balmer, O., Máser, P., Aksoy, S. & Caccone, A. (2014) Comparative genomics reveals multiple genetic backgrounds of human pathogenicity in the Trypanosoma brucei complex. Genome Biology and Evolution 6, 2811–2819.Google Scholar
Strand, M.R. (2008) Insect hemocytes and their role in immunity. pp. 25–47 in Beckage, N.E. (Ed.) Insect Immunity. San Diego, California, USA, Academic Press.Google Scholar
Thomas, M.B. & Read, A.F. (2007) Can fungal biopesticides control malaria? Nature Reviews Microbiology 5, 377–383.Google Scholar
Ursic-Bedoya, R.J. & Lowenberger, C.A. (2007) Rhodnius prolixus: identification of immune-related genes up-regulated in response to pathogens and parasites using suppressive subtractive hybridization. Developmental and Comparative Immunology 31, 109–120.Google Scholar
Ursic-Bedoya, R.J., Nazzari, H., Cooper, D., Triana, O., Wolff, M. & Lowenberger, C. (2008) Identification and characterization of two novel lysozymes from Rhodnius prolixus, a vector of Chagas disease. Journal of Insect Physiology 54, 593–603.Google Scholar
Ursic-Bedoya, R.J., Buchhop, J., Joy, J.B., Durvasula, R. & Lowenberger, C. (2011) Prolixicin: a novel antimicrobial peptide isolated from Rhodnius prolixus with differential activity against bacteria and Trypanosoma cruzi . Insect Molecular Biology 20, 775–786.Google Scholar
Vieira, C.S., Waniek, P.J., Mattos, D.P., Castro, D.P., Mello, C.B., Ratcliffe, N.A., Garcia, E.S. & Azambuja, P. (2014) Humoral responses in Rhodnius prolixus: bacterial feeding induces differential patterns of antibacterial activity and enhances mRNA levels of antimicrobial peptides in the midgut. Parasites and Vectors 7, 1–13.Google Scholar
Waniek, P.J., Castro, H.C., Sathler, P.C., Miceli, L., Jansen, A.M. & Araújo, C.A.C. (2009) Two novel defensin-encoding genes of the Chagas disease vector Triatoma brasiliensis (Reduviidae, Triatominae): gene expression and peptide-structure modeling. Journal Insect Physiology 55, 840–848.Google Scholar
Waniek, P.J., Jansen, A.M. & Araújo, C.A.C. (2011) Trypanosoma cruzi infection modulates the expression of Triatoma brasiliensis def 1 in the midgut. Vector Borne Zoonotic Diseases 11, 845–847.Google Scholar
Whitten, M., Sun, F., Tew, I., Schaub, G., Soukou, Ch., Nappi, A. & Ratcliffe, N. (2007) Differential modulation of Rhodnius prolixus nitric oxide activities following challenge with Trypanosoma rangeli, T. cruzi and bacterial cell wall components. Insect Biochemistry and Molecular Biology 37, 440–452.Google Scholar
Whitten, M.M.A., Mello, C.B., Gomes, S.A.O., Nigam, Y., Azambuja, P., Garcia, E.S. & Ratcliffe, N.A. (2001) Role of superoxide and reactive nitrogen intermediates in Rhodnius prolixus (Reduviidae)/Trypanosoma rangeli interactions. Experimental Parasitology 98, 44–57.Google Scholar
Yi, H.Y., Chowdhury, M., Huang, Y.D. & Yu, X.Q. (2014) Insect antimicrobial peptides and their applications. Applied Microbiology Biotechnology 98, 5807–5822.Google Scholar
Supplementary material: PDF

Flores-Villegas supplementary material

Figure

Download Flores-Villegas supplementary material(PDF)
PDF 1.3 MB
Supplementary material: File

Flores-Villegas supplementary material

Flores-Villegas supplementary material 1

Download Flores-Villegas supplementary material(File)
File 59.2 KB