Leonardo Araujo de Abreu

@nupem.ufrj.br

Tenure Professor/Instituto de Biodiversidade e Sustentabilidade - NUPEM
UNIVERSIDADE FEDERAL DO RIO DE JANEIRO

Leonardo Araujo de Abreu


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https://researchid.co/leoabreu

RESEARCH, TEACHING, or OTHER INTERESTS

Biochemistry, Cell Biology, Environmental Science, Education
19

Scopus Publications

Scopus Publications

  • Erratum: Redox imbalance induces remodeling of glucose metabolism in Rhipicephalus microplus embryonic cell line (J. Biol. Chem. (2022) 298:4 (101878) DOI: 10.1016/j.jbc.2022.101599)
    Bárbara Della Noce, Renato Martins da Silva, Marcelle Vianna de Carvalho Uhl, Satoru Konnai, Kazuhiko Ohashi, Christiano Calixto, Angélica Arcanjo, Leonardo Araujo de Abreu, Stephanie Serafim de Carvalho, Itabajara da Silva Vaz, Carlos Logullo
    Journal of Biological Chemistry, 2022
    The author list should read as follows: Bárbara Della Noce1,2,‡, Renato Martins da Silva1,2,‡, Marcelle Vianna de Carvalho Uhl1,2, Satoru Konnai3, Kazuhiko Ohashi3, Christiano Calixto1,2, Angélica Arcanjo1,2, Leonardo Araujo de Abreu1,2, Stephanie Serafim de Carvalho1,2, Alessandro Gaviraghi2,4, Itabajara da Silva Vaz Jr2,5, and Carlos Logullo1,2∗ The affiliations should read as follows: 1Laboratório de Bioquímica de Artrópodes Hematófagos, IBqM-UFRJ, Rio de Janeiro and Laboratório Integrado de Bioquímica Hatisaburo Masuda, NUPEM-UFRJ, Macaé, Rio de Janeiro, Brazil; 2Instituto Nacional de Ciência e Tecnologia em Entomologia Molecular, IBqM-UFRJ, Rio de Janeiro, Rio de Janeiro, Brazil; 3Laboratory of Infectious Diseases, Hokkaido University, Sapporo, Japan; 4Laboratório de Bioquímica de Resposta ao Estresse, Instituto de Bioquímica Médica Leopoldo de Meis, Universidade Federal do Rio de Janeiro, Cidade Universitária, Rio de Janeiro, RJ, Brazil; 5Centro de Biotecnologia and Faculdade de Veterinária– UFRGS, Porto Alegre, Rio Grande do Sul, Brazil The author contributions should read as follows: Author contributions - B. D. N., C. C., and R. M. d. S. formal analysis; B. D. N., C. C., R. M. d. S., A. A., M. V. d. C. U., and A. G. investigation; I. d. S. V. Jr, S. K., K. O., and C. L. resources; R. M. d. S., I. d. S. V. Jr, S. K., and K. O. writing – original draft; L. A. d. A. and S. S. d. C. writing – review & editing; C. L. supervision; C. L. project administration. Redox imbalance induces remodeling of glucose metabolism in Rhipicephalus microplus embryonic cell lineJournal of Biological ChemistryVol. 298Issue 3PreviewCarbohydrate metabolism not only functions in supplying cellular energy but also has an important role in maintaining physiological homeostasis and in preventing oxidative damage caused by reactive oxygen species. Previously, we showed that arthropod embryonic cell lines have high tolerance to H2O2 exposure. Here, we describe that Rhipicephalus microplus tick embryonic cell line (BME26) employs an adaptive glucose metabolism mechanism that confers tolerance to hydrogen peroxide at concentrations too high for other organisms. Full-Text PDF Open Access
  • REDOX IMBALANCE INDUCES REMODELING OF GLUCOSE METABOLISM IN RHIPICEPHALUS MICROPLUS EMBRYONIC CELL LINE
    Bárbara Della Noce, Renato Martins da Silva, Marcelle Vianna de Carvalho Uhl, Satoru Konnai, Kazuhiko Ohashi, Christiano Calixto, Angélica Arcanjo, Leonardo Araujo de Abreu, Stephanie Serafim de Carvalho, Itabajara da Silva Vaz, Carlos Logullo
    Journal of Biological Chemistry, 2022
    Carbohydrate metabolism not only functions in supplying cellular energy but also has an important role in maintaining physiological homeostasis and in preventing oxidative damage caused by reactive oxygen species. Previously, we showed that arthropod embryonic cell lines have high tolerance to H 2 O 2 exposure. Here, we describe that Rhipicephalus microplus tick embryonic cell line (BME26) employs an adaptive glucose metabolism mechanism that confers tolerance to hydrogen peroxide at concentrations too high for other organisms. This adaptive mechanism sustained by glucose metabolism remodeling promotes cell survival and redox balance in BME26 cell line after millimolar H 2 O 2 exposure. The present work shows that this tick cell line could tolerate high H 2 O 2 concentrations by initiating a carbohydrate-related adaptive response. We demonstrate that gluconeogenesis was induced as a compensation strategy that involved, among other molecules, the metabolic enzymes NADP-ICDH, G6PDH, and PEPCK. We also found that this phenomenon was coupled to glycogen accumulation and glucose uptake, supporting the pentose phosphate pathway to sustain NADPH production and leading to cell survival and proliferation. Our findings suggest that the described response is not atypical, being also observed in cancer cells, which highlights the importance of this model to all proliferative cells. We propose that these results will be useful in generating basic biological information to support the development of new strategies for disease treatment and parasite control.
  • Aedes fluviatilis cell lines as new tools to study metabolic and immune interactions in mosquito-Wolbachia symbiosis
    Christiano Calixto Conceição, Jhenifer Nascimento da Silva, Angélica Arcanjo, Cíntia Lopes Nogueira, Leonardo Araujo de Abreu, Pedro Lagerblad de Oliveira, Katia C. Gondim, Bruno Moraes, Stephanie Serafim de Carvalho, Renato Martins da Silva, Itabajara da Silva Vaz, Luciano Andrade Moreira, Carlos Logullo
    Scientific Reports, 2021
    In the present work, we established two novel embryonic cell lines from the mosquito Aedes fluviatilis containing or not the naturally occurring symbiont bacteria Wolbachia, which were called wAflu1 and Aflu2, respectively. We also obtained wAflu1 without Wolbachia after tetracycline treatment, named wAflu1.tet. Morphofunctional characterization was performed to help elucidate the symbiont-host interaction in the context of energy metabolism regulation and molecular mechanisms of the immune responses involved. The presence of Wolbachia pipientis improves energy performance in A. fluviatilis cells; it affects the regulation of key energy sources such as lipids, proteins, and carbohydrates, making the distribution of actin more peripheral and with extensions that come into contact with neighboring cells. Additionally, innate immunity mechanisms were activated, showing that the wAflu1 and wAflu1.tet cells are responsive after the stimulus using Gram negative bacteria. Therefore, this work confirms the natural, mutually co-regulating symbiotic relationship between W. pipientis and A. fluviatilis, modulating the host metabolism and immune pathway activation. The results presented here add important resources to the current knowledge of Wolbachia-arthropod interactions.
  • The hallmarks of GSK-3 in morphogenesis and embryonic development metabolism in arthropods
    Camila Waltero, Renato Martins, Christiano Calixto, Rodrigo Nunes da Fonseca, Leonardo Araujo de Abreu, Itabajara da Silva Vaz, Carlos Logullo
    Insect Biochemistry and Molecular Biology, 2020
  • Carbohydrate Metabolic Compensation Coupled to High Tolerance to Oxidative Stress in Ticks
    Bárbara Della Noce, Marcelle Vianna de Carvalho Uhl, Josias Machado, Camila Fernanda Waltero, Leonardo Araujo de Abreu, Renato Martins da Silva, Rodrigo Nunes da Fonseca, Cintia Monteiro de Barros, Gabriela Sabadin, Satoru Konnai, Itabajara da Silva Vaz, Kazuhiko Ohashi, Carlos Logullo
    Scientific Reports, 2019
    Reactive oxygen species (ROS) are natural byproducts of metabolism that have toxic effects well documented in mammals. In hematophagous arthropods, however, these processes are not largely understood. Here, we describe that Rhipicephalus microplus ticks and embryonic cell line (BME26) employ an adaptive metabolic compensation mechanism that confers tolerance to hydrogen peroxide (H2O2) at concentrations too high for others organisms. Tick survival and reproduction are not affected by H2O2 exposure, while BME26 cells morphology was only mildly altered by the treatment. Furthermore, H2O2-tolerant BME26 cells maintained their proliferative capacity unchanged. We evaluated several genes involved in gluconeogenesis, glycolysis, and pentose phosphate pathway, major pathways for carbohydrate catabolism and anabolism, describing a metabolic mechanism that explains such tolerance. Genetic and catalytic control of the genes and enzymes associated with these pathways are modulated by glucose uptake and energy resource availability. Transient increase in ROS levels, oxygen consumption, and ROS-scavenger enzymes, as well as decreased mitochondrial superoxide levels, were indicative of cell adaptation to high H2O2 exposure, and suggested a tolerance strategy developed by BME26 cells to cope with oxidative stress. Moreover, NADPH levels increased upon H2O2 challenge, and this phenomenon was sustained mainly by G6PDH activity. Interestingly, G6PDH knockdown in BME26 cells did not impair H2O2 tolerance, but generated an increase in NADP-ICDH transcription. In agreement with the hypothesis of a compensatory NADPH production in these cells, NADP-ICDH knockdown increased G6PDH relative transcript level. The present study unveils the first metabolic evidence of an adaptive mechanism to cope with high H2O2 exposure and maintain redox balance in ticks.
  • TOR as a Regulatory Target in Rhipicephalus microplus Embryogenesis
    Camila Waltero, Leonardo Araujo de Abreu, Thayná Alonso, Rodrigo Nunes-da-Fonseca, Itabajara da Silva Vaz, Carlos Logullo
    Frontiers in Physiology, 2019
    Embryogenesis is a metabolically intensive process carried out under tightly controlled conditions. The insulin signaling pathway regulates glucose homeostasis and is essential for reproduction in metazoan model species. Three key targets are part of this signaling pathway: protein kinase B (PKB, or AKT), glycogen synthase kinase 3 (GSK-3), and target of rapamycin (TOR). While the role of AKT and GSK-3 has been investigated during tick embryonic development, the role of TOR remains unknown. In this study, TOR and two other downstream effectors, namely S6 kinase (S6K) and eukaryotic translation initiation factor 4E-binding protein 1 (4E-BP1), were investigated in in vitro studies using the tick embryonic cell line BME26. First, we show that exogenous insulin can stimulate TOR transcription. Second, TOR chemical inhibition led to a decrease in BME26 cell viability, loss of membrane integrity, and downregulation of S6K and 4E-BP1 transcription. Conversely, treating BME26 cells with chemical inhibitors of AKT or GSK-3 did not affect S6K and 4E-BP1 transcription, showing that TOR is specifically required to activate its downstream targets. To address the role of TOR in tick reproduction, in vivo studies were performed. Analysis of relative transcription during different stages of tick embryonic development showed different levels of transcription for TOR, and a maternal deposition of S6K and 4E-BP1 transcripts. Injection of TOR double-stranded RNA (dsRNA) into partially fed females led to a slight delay in oviposition, an atypical egg external morphology, decreased vitellin content in eggs, and decreased larval hatching. Taken together, our data show that the TOR signaling pathway is important for tick reproduction, that TOR acts as a regulatory target in Rhipicephalus microplus embryogenesis and represents a promising target for the development of compounds for tick control.
  • Glycogen Synthase Kinase-3 is involved in glycogen metabolism control and embryogenesis of Rhodnius prolixus
    FLÁVIA B. MURY, MAGDA D. LUGON, RODRIGO NUNES DA FONSECA, JOSE R. SILVA, MATEUS BERNI, HELENA M. ARAUJO, MARCIO RIBEIRO FONTENELE, LEONARDO ARAUJO DE ABREU, MARÍLVIA DANSA, GLÓRIA BRAZ, HATISABURO MASUDA, CARLOS LOGULLO
    Parasitology, 2016
    SUMMARYRhodnius prolixus is a blood-feeding insect that transmits Trypanosoma cruzi and Trypanosoma rangeli to vertebrate hosts. Rhodnius prolixus is also a classical model in insect physiology, and the recent availability of R. prolixus genome has opened new avenues on triatomine research. Glycogen synthase kinase 3 (GSK-3) is classically described as a key enzyme involved in glycogen metabolism, also acting as a downstream component of the Wnt pathway during embryogenesis. GSK-3 has been shown to be highly conserved among several organisms, mainly in the catalytic domain region. Meanwhile, the role of GSK-3 during R. prolixus embryogenesis or glycogen metabolism has not been investigated. Here we show that chemical inhibition of GSK-3 by alsterpaullone, an ATP-competitive inhibitor of GSK3, does not affect adult survival rate, though it alters oviposition and egg hatching. Specific GSK-3 gene silencing by dsRNA injection in adult females showed a similar phenotype. Furthermore, bright field and 4’−6-diamidino-2-phenylindole (DAPI) staining analysis revealed that ovaries and eggs from dsGSK-3 injected females exhibited specific morphological defects. We also demonstrate that glycogen content was inversely related to activity and transcription levels of GSK-3 during embryogenesis. Lastly, after GSK-3 knockdown, we observed changes in the expression of the Wingless (Wnt) downstream target β-catenin as well as in members of other pathways such as the receptor Notch. Taken together, our results show that GSK-3 regulation is essential for R. prolixus oogenesis and embryogenesis.
  • Erratum: Non-invasive delivery of dsRNA into de-waxed tick eggs by electroporation (PLoS ONE (2015) 10:6 (e0130008) DOI:10.1371/journal.pone.0130008))
    Newton Ruiz, Leonardo Araujo de Abreu, Luís Fernando Parizi, Tae Kwon Kim, Albert Mulenga, Gloria Regina Cardoso Braz, Itabajara da Silva Vaz, Carlos Logullo
    Plos One, 2015
    Fig 5, “Silencing of AKT and GSK changes glycogen content R. microplus eggs,” is incorrect. Please see the correct Fig 5 and its caption here. Fig 5 Silencing of AKT and GSK changes glycogen content R. microplus eggs.
  • Non-invasive delivery of dsRNA into de-waxed tick eggs by electroporation
    Newton Ruiz, Leonardo Araujo de Abreu, Luís Fernando Parizi, Tae Kwon Kim, Albert Mulenga, Gloria Regina Cardoso Braz, Itabajara da Silva Vaz, Carlos Logullo
    Plos One, 2015
    RNA interference-mediated gene silencing was shown to be an efficient tool for validation of targets that may become anti-tick vaccine components. Here, we demonstrate the application of this approach in the validation of components of molecular signaling cascades, such as the Protein Kinase B (AKT)/Glycogen Synthase Kinase (GSK) axis during tick embryogenesis. It was shown that heptane and hypochlorite treatment of tick eggs can remove wax, affecting corium integrity and but not embryo development. Evidence of AKT and GSK dsRNA delivery into de-waxed eggs of via electroporation is provided. Primers designed to amplify part of the dsRNA delivered into the electroporated eggs dsRNA confirmed its entry in eggs. In addition, it was shown that electroporation is able to deliver the fluorescent stain, 4',6-diamidino-2-phenylindole (DAPI). To confirm gene silencing, a second set of primers was designed outside the dsRNA sequence of target gene. In this assay, the suppression of AKT and GSK transcripts (approximately 50% reduction in both genes) was demonstrated in 7-day-old eggs. Interestingly, silencing of GSK in 7-day-old eggs caused 25% reduction in hatching. Additionally, the effect of silencing AKT and GSK on embryo energy metabolism was evaluated. As expected, knockdown of AKT, which down regulates GSK, the suppressor of glycogen synthesis, decreased glycogen content in electroporated eggs. These data demonstrate that electroporation of de-waxed R. microplus eggs could be used for gene silencing in tick embryos, and improve the knowledge about arthropod embryogenesis.
  • Non-classical gluconeogenesis-dependent glucose metabolism in Rhipicephalus microplus embryonic cell line BME26
    Renato Da Silva, Bárbara Della Noce, Camila Waltero, Evenilton Costa, Leonardo De Abreu, Naftaly Githaka, Jorge Moraes, Helga Gomes, Satoru Konnai, Itabajara Da Silva Vaz, Kazuhiko Ohashi, Carlos Logullo
    International Journal of Molecular Sciences, 2015
    In this work we evaluated several genes involved in gluconeogenesis, glycolysis and glycogen metabolism, the major pathways for carbohydrate catabolism and anabolism, in the BME26 Rhipicephalus microplus embryonic cell line. Genetic and catalytic control of the genes and enzymes associated with these pathways are modulated by alterations in energy resource availability (primarily glucose). BME26 cells in media were investigated using three different glucose concentrations, and changes in the transcription levels of target genes in response to carbohydrate utilization were assessed. The results indicate that several genes, such as glycogen synthase (GS), glycogen synthase kinase 3 (GSK3), phosphoenolpyruvate carboxykinase (PEPCK), and glucose-6 phosphatase (GP) displayed mutual regulation in response to glucose treatment. Surprisingly, the transcription of gluconeogenic enzymes was found to increase alongside that of glycolytic enzymes, especially pyruvate kinase, with high glucose treatment. In addition, RNAi data from this study revealed that the transcription of gluconeogenic genes in BME26 cells is controlled by GSK-3. Collectively, these results improve our understanding of how glucose metabolism is regulated at the genetic level in tick cells.
  • The modulation of the symbiont/host interaction between Wolbachia pipientis and Aedes fluviatilis embryos by glycogen metabolism
    Mariana da Rocha Fernandes, Renato Martins, Evenilton Pessoa Costa, Etiene Casagrande Pacidônio, Leonardo Araujo de Abreu, Itabajara da Silva Vaz, Luciano A. Moreira, Rodrigo Nunes da Fonseca, Carlos Logullo
    Plos One, 2014
  • The conserved role of the AKT/GSK3 axis in cell survival and glycogen metabolism in Rhipicephalus (Boophilus) microplus embryo tick cell line BME26
    Leonardo Araujo de Abreu, Christiano Calixto, Camila Fernanda Waltero, Bárbara Pitta Della Noce, Naftaly Wang'ombe Githaka, Adriana Seixas, Luís Fernando Parizi, Satoru Konnai, Itabajara da Silva Vaz, Kazuhiko Ohashi, Carlos Logullo
    Biochimica Et Biophysica Acta General Subjects, 2013
  • Germ band retraction as a landmark in glucose metabolism during Aedes aegypti embryogenesis
    Wagner Vital, Gustavo Lazzaro Rezende, Leonardo Abreu, Jorge Moraes, Francisco JA Lemos, Itabajara da Silva Vaz, Carlos Logullo
    BMC Developmental Biology, 2010
  • Expression and activity of glycogen synthase kinase during vitellogenesis and embryogenesis of Rhipicephalus (Boophilus) microplus
    Carlos Logullo, William H. Witola, Caroline Andrade, Leonardo Abreu, Josiana Gomes, Itabajara da Silva Vaz, Saiki Imamura, Satoru Konnai, Kazuhiko Ohashi, Misao Onuma
    Veterinary Parasitology, 2009
  • Exogenous insulin stimulates glycogen accumulation in Rhipicephalus (Boophilus) microplus embryo cell line BME26 via PI3K/AKT pathway
    Leonardo Araujo de Abreu, Arianne Fabres, Eliane Esteves, Aoi Masuda, Itabajara da Silva Vaz, Sirlei Daffre, Carlos Logullo
    Comparative Biochemistry and Physiology B Biochemistry and Molecular Biology, 2009
  • Kinetics of energy source utilization in Boophilus microplus (Canestrini, 1887) (Acari: Ixodidae) embryonic development
    Eldo Campos, Jorge Moraes, Arnoldo R. Façanha, Érica Moreira, Denise Valle, Leonardo Abreu, Pedro P.A. Manso, Aline Nascimento, Marcelo Pelajo-Machado, Henrique Lenzi, Aoi Masuda, Itabajara da Silva Vaz, Carlos Logullo
    Veterinary Parasitology, 2006
  • Proteolytic activity of Boophilus microplus Yolk pro-Cathepsin D (BYC) is coincident with cortical acidification during embryogenesis
    Leonardo A. Abreu, Denise Valle, Pedro P.A. Manso, Arnoldo R. Façanha, Marcelo Pelajo-Machado, Hatisaburo Masuda, Aoi Masuda, Itabajara Vaz, Henrique Lenzi, Pedro L. Oliveira, Carlos Logullo
    Insect Biochemistry and Molecular Biology, 2004
  • Heme biosynthesis and oogenesis in the blood-sucking bug, Rhodnius prolixus
    Glória R.C. Braz, Leonardo Abreu, Hatisaburo Masuda, Pedro L. Oliveira
    Insect Biochemistry and Molecular Biology, 2001
  • Isolation of an aspartic proteinase precursor from the egg of a hard tick, Boophilus microplus
    C. LOGULLO, I. DA SILVA VAZ, M. H. F. SORGINE, G. O. PAIVA-SILVA, F. S. FARIA, R. B. ZINGALI, M. F. R. DE LIMA, L. ABREU, E. FIALHO OLIVEIRA, E. W. ALVES, H. MASUDA, J. C. GONZALES, A. MASUDA, P. L. OLIVEIRA
    Parasitology, 1998