Impact of Trypanosoma Cruzi on Antimicrobial Peptide Gene Expression and Activity in the Fat Body and Midgut of Rhodnius Prolixus

Overview

Journal Parasit Vectors

Publisher Biomed Central

Specialties Parasitology
Tropical Medicine

Date 2016 Mar 3

PMID 26931761

Citations 33

Authors

C S Vieira

P J Waniek

D P Castro

D P Mattos

O C Moreira

P Azambuja

Affiliations

Soon will be listed here.

Abstract

Background: Rhodnius prolixus is a major vector of Trypanosoma cruzi, the causative agent of Chagas disease in Latin America. In natural habitats, these insects are in contact with a variety of bacteria, fungi, virus and parasites that they acquire from both their environments and the blood of their hosts. Microorganism ingestion may trigger the synthesis of humoral immune factors, including antimicrobial peptides (AMPs). The objective of this study was to compare the expression levels of AMPs (defensins and prolixicin) in the different midgut compartments and the fat body of R. prolixus infected with different T. cruzi strains. The T. cruzi Dm 28c clone (TcI) successfully develops whereas Y strain (TcII) does not complete its life- cycle in R. prolixus. The relative AMP gene expressions were evaluated in the insect midgut and fat body infected on different days with the T. cruzi Dm 28c clone and the Y strain. The influence of the antibacterial activity on the intestinal microbiota was taken into account.

Methods: The presence of T. cruzi in the midgut of R. prolixus was analysed by optical microscope. The relative expression of the antimicrobial peptides encoding genes defensin (defA, defB, defC) and prolixicin (prol) was quantified by RT-qPCR. The antimicrobial activity of the AMPs against Staphylococcus aureus, Escherichia coli and Serratia marcescens were evaluated in vitro using turbidimetric tests with haemolymph, anterior and posterior midgut samples. Midgut bacteria were quantified using colony forming unit (CFU) assays and real time quantitative polymerase chain reaction (RT-qPCR).

Results: Our results showed that the infection of R. prolixus by the two different T. cruzi strains exhibited different temporal AMP induction profiles in the anterior and posterior midgut. Insects infected with T. cruzi Dm 28c exhibited an increase in defC and prol transcripts and a simultaneous reduction in the midgut cultivable bacteria population, Serratia marcescens and Rhodococcus rhodnii. In contrast, the T. cruzi Y strain neither induced AMP gene expression in the gut nor reduced the number of colony formation units in the anterior midgut. Beside the induction of a local immune response in the midgut after feeding R. prolixus with T. cruzi, a simultaneous systemic response was also detected in the fat body.

Conclusions: R. prolixus AMP gene expressions and the cultivable midgut bacterial microbiota were modulated in distinct patterns, which depend on the T. cruzi genotype used for infection.

Citing Articles

Azadirachtin disrupts ecdysone signaling and alters sand fly immunity.

Vieira C, Bisogno S, Salvemini M, Loza Telleria E, Volf P Parasit Vectors. 2024; 17(1):526.

PMID: 39707409 PMC: 11662615. DOI: 10.1186/s13071-024-06589-8.

Immune signaling pathways in in the context of infection: cellular and humoral immune responses and microbiota modulation.

Pereira S, de Mattos D, Gonzalez M, Mello C, Azambuja P, de Castro D Front Physiol. 2024; 15:1435447.

PMID: 39210973 PMC: 11357937. DOI: 10.3389/fphys.2024.1435447.

Interaction of , Triatomines and the Microbiota of the Vectors-A Review.

Schaub G Microorganisms. 2024; 12(5).

PMID: 38792688 PMC: 11123833. DOI: 10.3390/microorganisms12050855.

Malpighian tubules of : More than post-prandial diuresis.

Orchard I, Al-Dailami A, Leyria J, Lange A Front Insect Sci. 2024; 3:1167889.

PMID: 38469518 PMC: 10926411. DOI: 10.3389/finsc.2023.1167889.

Evidence of a conserved mammalian immunosuppression mechanism in upon infection with .

Loza Telleria E, Tinoco-Nunes B, Forrest D, Di-Blasi T, Lestinova T, Chang K Front Immunol. 2023; 14:1162596.

PMID: 38022562 PMC: 10652419. DOI: 10.3389/fimmu.2023.1162596.

References

Hao Z, Kasumba I, Aksoy S . Proventriculus (cardia) plays a crucial role in immunity in tsetse fly (Diptera: Glossinidiae). Insect Biochem Mol Biol. 2003; 33(11):1155-64. DOI: 10.1016/j.ibmb.2003.07.001. View

Miles M, Souza A, Povoa M, Shaw J, Lainson R, Toye P . Isozymic heterogeneity of Trypanosoma cruzi in the first autochthonous patients with Chagas' disease in Amazonian Brazil. Nature. 1978; 272(5656):819-21. DOI: 10.1038/272819a0. View

Garcia E, Genta F, de Azambuja P, Schaub G . Interactions between intestinal compounds of triatomines and Trypanosoma cruzi. Trends Parasitol. 2010; 26(10):499-505. DOI: 10.1016/j.pt.2010.07.003. View

Castro D, Seabra S, Garcia E, De Souza W, Azambuja P . Trypanosoma cruzi: ultrastructural studies of adhesion, lysis and biofilm formation by Serratia marcescens. Exp Parasitol. 2007; 117(2):201-7. DOI: 10.1016/j.exppara.2007.04.014. View

Araujo C, Waniek P, Xavier S, Jansen A . Genotype variation of Trypanosoma cruzi isolates from different Brazilian biomes. Exp Parasitol. 2010; 127(1):308-12. DOI: 10.1016/j.exppara.2010.07.013. View

Waniek P, Castro H, Sathler P, Miceli L, Jansen A, Araujo C . Two novel defensin-encoding genes of the Chagas disease vector Triatoma brasiliensis (Reduviidae, Triatominae): gene expression and peptide-structure modeling. J Insect Physiol. 2009; 55(9):840-8. DOI: 10.1016/j.jinsphys.2009.05.015. View

Garcia E, Azambuja P . Development and interactions of Trypanosoma cruzi within the insect vector. Parasitol Today. 1991; 7(9):240-4. DOI: 10.1016/0169-4758(91)90237-i. View

Castro D, Moraes C, Gonzalez M, Ratcliffe N, Azambuja P, Garcia E . Trypanosoma cruzi immune response modulation decreases microbiota in Rhodnius prolixus gut and is crucial for parasite survival and development. PLoS One. 2012; 7(5):e36591. PMC: 3344921. DOI: 10.1371/journal.pone.0036591. View

Livak K, Schmittgen T . Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2002; 25(4):402-8. DOI: 10.1006/meth.2001.1262. View

10.

Cortez M, Provencano A, Silva C, Mello C, Zimmermann L, Schaub G . Trypanosoma cruzi: effects of azadirachtin and ecdysone on the dynamic development in Rhodnius prolixus larvae. Exp Parasitol. 2012; 131(3):363-71. DOI: 10.1016/j.exppara.2012.05.005. View

11.

Meister S, Agianian B, Turlure F, Relogio A, Morlais I, Kafatos F . Anopheles gambiae PGRPLC-mediated defense against bacteria modulates infections with malaria parasites. PLoS Pathog. 2009; 5(8):e1000542. PMC: 2715215. DOI: 10.1371/journal.ppat.1000542. View

12.

Abel L, Ferreira L, Navarro I, Baron M, Kalil J, Gazzinelli R . Induction of IL-12 production in human peripheral monocytes by Trypanosoma cruzi Is mediated by glycosylphosphatidylinositol-anchored mucin-like glycoproteins and potentiated by IFN- γ and CD40-CD40L interactions. Mediators Inflamm. 2014; 2014:345659. PMC: 4120781. DOI: 10.1155/2014/345659. View

13.

Lopez L, Morales G, Ursic R, Wolff M, Lowenberger C . Isolation and characterization of a novel insect defensin from Rhodnius prolixus, a vector of Chagas disease. Insect Biochem Mol Biol. 2003; 33(4):439-47. DOI: 10.1016/s0965-1748(03)00008-0. View

14.

Coura J . The main sceneries of Chagas disease transmission. The vectors, blood and oral transmissions--a comprehensive review. Mem Inst Oswaldo Cruz. 2014; 110(3):277-82. PMC: 4489464. DOI: 10.1590/0074-0276140362. View

15.

Vieira C, Waniek P, Mattos D, Castro D, Mello C, Ratcliffe N . Humoral responses in Rhodnius prolixus: bacterial feeding induces differential patterns of antibacterial activity and enhances mRNA levels of antimicrobial peptides in the midgut. Parasit Vectors. 2014; 7:232. PMC: 4032158. DOI: 10.1186/1756-3305-7-232. View

16.

Hu Y, Aksoy S . An antimicrobial peptide with trypanocidal activity characterized from Glossina morsitans morsitans. Insect Biochem Mol Biol. 2005; 35(2):105-15. DOI: 10.1016/j.ibmb.2004.10.007. View

17.

Eichler S, Schaub G . Development of symbionts in triatomine bugs and the effects of infections with trypanosomatids. Exp Parasitol. 2002; 100(1):17-27. DOI: 10.1006/expr.2001.4653. View

18.

Freire-de-Lima L, Fonseca L, Oeltmann T, Mendonca-Previato L, Previato J . The trans-sialidase, the major Trypanosoma cruzi virulence factor: Three decades of studies. Glycobiology. 2015; 25(11):1142-9. DOI: 10.1093/glycob/cwv057. View

19.

Zingales B, Andrade S, Briones M, Campbell D, Chiari E, Fernandes O . A new consensus for Trypanosoma cruzi intraspecific nomenclature: second revision meeting recommends TcI to TcVI. Mem Inst Oswaldo Cruz. 2009; 104(7):1051-4. DOI: 10.1590/s0074-02762009000700021. View

20.

Dong Y, Manfredini F, Dimopoulos G . Implication of the mosquito midgut microbiota in the defense against malaria parasites. PLoS Pathog. 2009; 5(5):e1000423. PMC: 2673032. DOI: 10.1371/journal.ppat.1000423. View