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Proteome of the Triatomine Digestive Tract: from Catalytic to Immune Pathways; Focusing on Annexin Expression

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Proteome of the Triatomine Digestive Tract: from Catalytic to Immune Pathways; Focusing on Annexin Expression fmolb-07-589435 December 3, 2020 Time: 17:27 # 1 ORIGINAL RESEARCH published: 09 December 2020 doi: 10.3389/fmolb.2020.589435 Proteome of the Triatomine Digestive Tract: From Catalytic to Immune Pathways; Focusing on Annexin Expression Marcia Gumiel1,2†‡, Debora Passos de Mattos3,4†, Cecília Stahl Vieira1,5, Caroline Silva Moraes1, Carlos José de Carvalho Moreira6, Marcelo Salabert Gonzalez3,4,5, André Teixeira-Ferreira7, Mariana Waghabi8, 1,3,4,5 9 Edited by: Patricia Azambuja and Nicolas Carels * Barbara Cellini, 1 Laboratório de Bioquímica e Fisiologia de Insetos, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz (IOC/FIOCRUZ), Rio University of Perugia, Italy de Janeiro, Brazil, 2 Research Department, Universidad Privada Franz Tamayo (UNIFRANZ), La Paz, Bolivia, 3 Laboratório Reviewed by: de Biologia de Insetos, Departamento de Biologia Geral, Universidade Federal Fluminense, Niterói, Brazil, 4 Programa Dong-Woo Lee, de Pós-Graduação em Ciências e Biotecnologia, Instituto de Biologia, Universidade Federal Fluminense, Niterói, Brazil, Yonsei University, South Korea 5 Departamento de Entomologia Molecular, Instituto Nacional de Entomologia Molecular (INCT-EM), Rio de Janeiro, Brazil, Qi Wu, 6 Laboratório de Doenças Parasitárias, Instituto Oswaldo Cruz, Rio de Janeiro, Brazil, 7 Laboratório de Toxinologia, Instituto Aarhus University, Denmark Oswaldo Cruz, Rio de Janeiro, Brazil, 8 Laboratório de Genômica Funcional e Bioinformática, Instituto Oswaldo Cruz, 9 *Correspondence: FIOCRUZ, Rio de Janeiro, Brazil, Laboratório de Modelagem de Sistemas Biológicos, National Institute for Science Nicolas Carels and Technology on Innovation in Neglected Diseases (INCT-IDN), Centro de Desenvolvimento Tecnológico em Saúde nicolas.carels@cdts.fiocruz.br; (CDTS), Fundação Oswaldo Cruz (FIOCRUZ), Rio de Janeiro, Brazil [email protected] †These authors have contributed Rhodnius prolixus, Panstrongylus megistus, Triatoma infestans, and Dipetalogaster equally to this work maxima are all triatomines and potential vectors of the protozoan Trypanosoma cruzi ‡Present address: Marcia Gumiel, responsible for human Chagas’ disease. Considering that the T. cruzi’s cycle occurs Department of Research, Universidad inside the triatomine digestive tract (TDT), the analysis of the TDT protein profile is an Privada Franz Tamayo (UNIFRANZ), essential step to understand TDT physiology during T. cruzi infection. To characterize Calle Heroes del Acre, La Paz, Bolivia the protein profile of TDT of D. maxima, P. megistus, R. prolixus, and T. infestans, Specialty section: a shotgun liquid chromatography-tandem mass spectrometry (LC-MS/MS) approach This article was submitted to was applied in this report. Most proteins were found to be closely related to metabolic Protein Chemistry and Enzymology, a section of the journal pathways such as gluconeogenesis/glycolysis, citrate cycle, fatty acid metabolism, Frontiers in Molecular Biosciences oxidative phosphorylation, but also to the immune system. We annotated this new Received: 31 July 2020 proteome contribution gathering it with those previously published in accordance with Accepted: 21 October 2020 Published: 09 December 2020 Gene Ontology and KEGG. Enzymes were classified in terms of class, acceptor, and Citation: function, while the proteins from the immune system were annotated by reference Gumiel M, Mattos DP, Vieira CS, to the pathways of humoral response, cell cycle regulation, Toll, IMD, JNK, Jak- Moraes CS, Moreira CJC, STAT, and MAPK, as available from the Insect Innate Immunity Database (IIID). These Gonzalez MS, Teixeira-Ferreira A, Waghabi M, Azambuja P and pathways were further subclassified in recognition, signaling, response, coagulation, Carels N (2020) Proteome of the melanization and none. Finally, phylogenetic affinities and gene expression of annexins Triatomine Digestive Tract: From Catalytic to Immune Pathways; were investigated for understanding their role in the protection and homeostasis of Focusing on Annexin Expression. intestinal epithelial cells against the inflammation. Front. Mol. Biosci. 7:589435. doi: 10.3389/fmolb.2020.589435 Keywords: chagas disease, triatomine, digestive tract, mass spectrometry, enzymes, immunity, annexin Frontiers in Molecular Biosciences| www.frontiersin.org 1 December 2020| Volume 7| Article 589435 fmolb-07-589435 December 3, 2020 Time: 17:27 # 2 Gumiel et al. The Proteome of Triatomines Digestive Tract INTRODUCTION following by multiplication or differentiation, as well as (iv) the local humoral defense mechanisms associated to the intestinal Chagas disease (Chagas, 1909, 1911) is one of the major causes bacterial microbiota after triatomine feeding (Alves et al., 2007; of acute myocarditis and progressive chronic cardiomyopathy in Nogueira et al., 2007; Gonzalez et al., 2011, 2013; da Mota et al., endemic regions of Latin America, affecting almost 6-7 million 2012; Oliveira et al., 2012; Vieira et al., 2016; Nogueira et al., 2017; people (WHO (World Health Organization), 2020). The protist Moreira et al., 2018). parasite Trypanosoma cruzi is the causative agent of Chagas To briefly summarize the molecular knowledge that has disease and its development alternates between vertebrates been recently acquired on TDT, Ribeiro et al.(2014) identified (mainly mammals, but also lizards) and triatomine hosts (Garcia thousands of genes regularly expressed, which were further et al., 1999; Ferreira et al., 2016). recognized among the 15,546 putative genes reported by Triatomines are insects classified as Hemiptera: Reduviidae Mesquita et al.(2015) in the genome of R. prolixus. Later on, with some of the most important species for Chagas disease immune-related genes were detected in Triatoma pallidipennis, transmission being Triatoma infestans, Rhodnius prolixus, and T. dimidiata, and T. infestans, using comparative transcriptomics Panstrongylus megistus (Coura and Dias, 2009; Schofield and based on gene references from the immune response of hexapods Galvão, 2009; Coura, 2015). These triatomine species have (Zumaya-Estrada et al., 2018). These studies show that the wide geographical distribution in Latin America with marked repertoire of genes in the immunological signaling pathway adaptation to domestic and peridomestic ecotopes as well as is substantially different in Hemiptera compared to Diptera. physiological features that promote T. cruzi development (Guhl, Since the methodology based on genomic sequences needs to be 2007; Coura and Dias, 2009; Noireau, 2009; Gurgel-Gonçalves complemented by the direct analysis of gene products through et al., 2012; Coura, 2015). By contrast, Dipetalogaster maxima functional genomics, a proteome analysis was, first, conducted is found in northern America, where it inhabits the sylvatic by 2D gel electrophoresis by Vieira et al.(2015) using the AM environments of Baja California Sur and Mexico. It resides in of R. prolixus and, later on, by Ouali et al.(2020) using both dry and rocky areas and usually takes its blood meal from AM and PM. These authors mainly found proteins involved in lizards, but when fasting can bite human or domestic animals detoxification, amino acids, lipids and sugar degradation; they (Guzmán-Bracho, 2001). also confirmed the existence of these proteins by reference to the Many factors influence the T. cruzi vectorial transmission, transcriptome and genome annotations by Ribeiro et al.(2014) such as: (i) The varied feeding behavior of triatomines; (ii) and Mesquita et al.(2015). The close association between triatomines and humans; (iii) In complement to sequence analyses, Antunes et al.(2013) The variety of ecotopes that triatomines occupy, which turns investigated the fecal metabolome of P. megistus, R. prolixus the control of their population difficult (Noireau et al., 2005; and T. infestans expanding the knowledge of the TDT chemical Cortez et al., 2007; Buitrago et al., 2010; Espinoza Echeverria composition. These authors reported that 80% of the metabolites et al., 2017); (iv) The wide phylogenetic divergence among the found were common to these three species, while the remaining natural clones of T. cruzi (Laurent et al., 1997); and also (v) The 20% varied among them (Antunes et al., 2013). geographic origin of T. cruzi and its vector that may constitute an Here, we aimed at investigating the complete proteomic essential factor in the parasitic cycle since local strains are usually profile of the TDT from four species: T. infestans, R. prolixus, better adapted to indigenous vector species than to exotic ones P. megistus, and D. maxima to take a step forward in the (Ryckman, 1965; Zeledón, 1987). knowledge of T. cruzi vectors biology. The shotgun proteome The life cycle of T. cruzi in the invertebrate host is restricted results described here seek to contribute to the understanding to the triatomine digestive tract (TDT) (Zeledón, 1987; Garcia of the factors that may influence the triatomine competence for et al., 1999; Gonzalez et al., 1999; Cortez et al., 2012; Dias transmitting Chagas disease. et al., 2015; Ferreira et al., 2016). Therefore, T. cruzi suffers Through shotgun proteomic approach (nano-LC/MS/MS), the influence of different factors present in the lumen of insect we identified proteins expressed in midgut epithelial cells gut (Mello et al., 1996; Moreira et al., 2003; Azambuja et al., and rectum enriched fraction of the TDT from the four 2004, 2017; Garcia et al., 2010b; Castro et al., 2012; Nogueira triatomine species analyzed in this study. We found that et al., 2015; Vieira et al., 2016); these factors
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