Non-Classical Gluconeogenesis-Dependent Glucose Metabolism in Rhipicephalus microplus Embryonic Cell Line BME26

Silva, Renato Martins da; Noce, Bárbara Della; Waltero, Camila Fernanda; Costa, Evenilton Pessoa; Abreu, Leonardo; Githaka, Naftaly; Moraes, João Antônio de; Gomes, Helga; Konnai, Satoru; Vaz, Itabajara da Silva; Ohashi, Kazuhiko; Logullo, Carlos

doi:10.3390/ijms16011821

Cited by 17 publications

(18 citation statements)

References 50 publications

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“…Glucose metabolism was recently characterized in the Rhipicephalus microplus BME26 embryo-derived cell line (56), and glucose was identified as one of the metabolites involved in chemosensation during tick blood feeding (57). These results highlight the importance of glucose metabolism in ticks, but information was not available on the role of this pathway during pathogen infection.…”

Section: Discussionmentioning

confidence: 99%

Integrated Metabolomics, Transcriptomics and Proteomics Identifies Metabolic Pathways Affected by Anaplasma phagocytophilum Infection in Tick Cells*

Villar

Ayllón

Alberdi

et al. 2015

Molecular & Cellular Proteomics

107

186

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Anaplasma phagocytophilum is an emerging zoonotic pathogen that causes human granulocytic anaplasmosis. These intracellular bacteria establish infection by affecting cell function in both the vertebrate host and the tick vector, Ixodes scapularis. Previous studies have characterized the tick transcriptome and proteome in response to A. phagocytophilum infection. However, in the postgenomic era, the integration of omics datasets through a systems biology approach allows network-based analyses to describe the complexity and functionality of biological systems such as host-pathogen interactions and the discovery of new targets for prevention and control of infectious diseases. This study reports the first systems biology integration of metabolomics, transcriptomics, and proteomics data to characterize essential metabolic pathways involved in the tick response to A. phagocytophilum infection. The ISE6 tick cells used in this study constitute a model for hemocytes involved in pathogen infection and immune response. The results showed that infection affected protein processing in endoplasmic reticulum and glucose metabolic pathways in tick cells. These results supported tick-Anaplasma co-evolution by providing new evidence of how tick cells limit pathogen infection, while the pathogen benefits from the tick cell response to establish infection. Additionally, ticks benefit from A. phagocytophilum infection by increasing survival while pathogens guarantee transmission. The results suggested that A. phagocytophilum induces protein misfolding to limit the tick cell response and facilitate infection but requires protein degradation to prevent ER stress and cell apoptosis to survive in infected cells. Additionally, A. phagocytophilum may benefit from the tick cell's ability to limit bacterial infection through PEPCK inhibition leading to decreased glucose metabolism, which also results in the inhibition of cell apoptosis that increases infection of tick cells. These results support the use of this experimental approach to systematically identify cell pathways and molecular mechanisms involved in tick-pathogen interactions. Data are available via ProteomeXchange with identifier PXD002181. Molecular & Cellular

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Section: Discussionmentioning

confidence: 99%

Integrated Metabolomics, Transcriptomics and Proteomics Identifies Metabolic Pathways Affected by Anaplasma phagocytophilum Infection in Tick Cells*

Villar

Ayllón

Alberdi

et al. 2015

Molecular & Cellular Proteomics

107

186

View full text Add to dashboard Cite

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“…Our findings indicate that there is mutual regulation among major enzymes of glucose metabolism at the transcriptional and enzymatic levels (SILVA et al, 2015). In our metabolomics research, metabolite levels from metabolic routes in D. melanogaster were measured.…”

Section: Energy Metabolism In the Arthropod Embryomentioning

confidence: 84%

“…This approach furthered our understanding of substrates involved in carbohydrate catabolism and anabolic pathways of insects (AN et al, 2014). These findings have expanded our knowledge about the physiology of hematophagous arthropods and energy metabolism of ticks (MORAES et al, 2007;LOGULLO et al 2009;SILVA et al, 2015). Furthermore, the investigation of key components of these metabolic pathways has provided invaluable information for the development and improvement of vaccines and drugs to control important disease vectors.…”

Section: Energy Metabolism In the Arthropod Embryomentioning

confidence: 89%

The dynamics of energy metabolism in the tick embryo

Martins

Ruiz

Fonseca

et al. 2018

Rev. Bras. Parasitol. Vet.

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The cattle tick Rhipicephalus (Boophilus) microplus is an ectoparasite capable of transmitting a large number of pathogens, causing considerable losses in the cattle industry, with substantial damage to livestock. Over the years, important stages of its life cycle, such as the embryo, have been largely ignored by researchers. Tick embryogenesis has been typically described as an energy-consuming process, sustaining cell proliferation, differentiation, and growth. During the embryonic stage of arthropods, there is mobilization of metabolites of maternal origin for the development of organs and tissues of the embryo. Glycogen resynthesis in late embryogenesis is considered as an effective indicator of embryonic integrity. In the cattle tick R.(B. (B.) microplus, glycogen resynthesis is sustained by protein degradation through the gluconeogenesis pathway at the end of the embryonic period. Despite recent advancements in research on tick energy metabolism at the molecular level, the dynamics of nutrient utilization during R. (B.) microplus embryogenesis is still poorly understood. The present review aims to describe the regulatory mechanisms of carbohydrate metabolism during maternal-zygotic transition and identify possible new targets for the development of novel drugs and other control measures against R. (B.) microplus infestations.

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“…microplus embryogenesis. Protein metabolism depends strongly on the substantial expression and activity of carbohydrate metabolism enzymes and alpha-enolase is a key glycolitic enzyme [ 36 ].…”

Section: Discussionmentioning

confidence: 99%

Ixodes ricinus and Its Endosymbiont Midichloria mitochondrii: A Comparative Proteomic Analysis of Salivary Glands and Ovaries

et al. 2015

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Hard ticks are hematophagous arthropods that act as vectors of numerous pathogenic microorganisms of high relevance in human and veterinary medicine. Ixodes ricinus is one of the most important tick species in Europe, due to its role of vector of pathogenic bacteria such as Borrelia burgdorferi and Anaplasma phagocytophilum, of viruses such as tick borne encephalitis virus and of protozoans as Babesia spp. In addition to these pathogens, I. ricinus harbors a symbiotic bacterium, Midichloria mitochondrii. This is the dominant bacteria associated to I. ricinus, but its biological role is not yet understood. Most M. mitochondrii symbionts are localized in the tick ovaries, and they are transmitted to the progeny. M. mitochondrii bacteria have however also been detected in the salivary glands and saliva of I. ricinus, as well as in the blood of vertebrate hosts of the tick, prompting the hypothesis of an infectious role of this bacterium. To investigate, from a proteomic point of view, the tick I. ricinus and its symbiont, we generated the protein profile of the ovary tissue (OT) and of salivary glands (SG) of adult females of this tick species. To compare the OT and SG profiles, 2-DE profiling followed by LC-MS/MS protein identification were performed. We detected 21 spots showing significant differences in the relative abundance between the OT and SG, ten of which showed 4- to 18-fold increase/decrease in density. This work allowed to establish a method to characterize the proteome of I. ricinus, and to detect multiple proteins that exhibit a differential expression profile in OT and SG. Additionally, we were able to use an immunoproteomic approach to detect a protein from the symbiont. Finally, the method here developed will pave the way for future studies on the proteomics of I. ricinus, with the goals of better understanding the biology of this vector and of its symbiont M. mitochondrii.

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Non-Classical Gluconeogenesis-Dependent Glucose Metabolism in Rhipicephalus microplus Embryonic Cell Line BME26

Cited by 17 publications

References 50 publications

Integrated Metabolomics, Transcriptomics and Proteomics Identifies Metabolic Pathways Affected by Anaplasma phagocytophilum Infection in Tick Cells*

Integrated Metabolomics, Transcriptomics and Proteomics Identifies Metabolic Pathways Affected by Anaplasma phagocytophilum Infection in Tick Cells*

The dynamics of energy metabolism in the tick embryo

Ixodes ricinus and Its Endosymbiont Midichloria mitochondrii: A Comparative Proteomic Analysis of Salivary Glands and Ovaries

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