The Dose Makes the Poison: Nutritional Overload Determines the Life Traits of Blood-Feeding Arthropods

Sterkel, Marcos; Oliveira, José Henrique M.; Bottino-Rojas, Vanessa; Paiva-Silva, Gabriela O.; Oliveira, Pedro L.

doi:10.1016/j.pt.2017.04.008

Cited by 86 publications

(90 citation statements)

References 101 publications

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“…Chemical inhibitors of HPPD caused the death of hematophagous arthropods (kissing bug, mosquitoes and ticks) but were not toxic to non-hematophagous insects [14]. Therefore, the degradation of free tyrosine formed in excess during digestion of a blood meal is an essential trait in the adaptation to a hematophagous way of life [11]. The key role of this pathway in the evolution of blood-feeding organisms led us to identify tyrosine degradation as a potential target in the development of novel alternative insecticides that would therefore be selective for these animals.…”

Section: Introductionmentioning

confidence: 99%

On the use of inhibitors of 4-hydroxyphenylpyruvate dioxygenase as a vector-selective insecticide in the control of mosquitoes

Ramírez

Sterkel

Martins³

et al. 2019

Preprint

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2 dioxygenase as a vector-selective insecticide in the 3 control of mosquitoes 4 5 MarlonAbstract 26Blood-sucking insects incorporate many times their body weight of blood in a 27 single meal. As proteins are the major component of vertebrate blood, its digestion in the 28 gut of hematophagous insects generates extremely high concentrations of free amino 29 acids. Previous reports showed that the tyrosine degradation pathway plays an essential 30 role in adapting these animals to blood feeding. Inhibiting 4-hydroxyphenylpyruvate 31 dioxygenase (HPPD), the rate-limiting step of tyrosine degradation, results in the death 32 of insects after a blood meal. Therefore, it was suggested that compounds that block the 33 catabolism of tyrosine could act selectively on blood-feeding insects. Here we have 34 evaluated the toxicity against mosquitoes of three HPPD inhibitors currently used as 35 herbicides and in human health. Among the compounds tested, nitisinone (NTBC) 36 proved to be more potent than mesotrione (MES) and isoxaflutole (IFT) in Aedes aegypti.

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Section: Introductionmentioning

confidence: 99%

On the use of inhibitors of 4-hydroxyphenylpyruvate dioxygenase as a vector-selective insecticide in the control of mosquitoes

Ramírez

Sterkel

Martins³

et al. 2019

Preprint

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“…Genetic loci that encode enzymes in the initial steps of the tyrosine pathway frequently produce changes in cuticle coloration as well as cuticle integrity/strength, consistent with branching of the pathway for the production of melanin and sclerotin. Accordingly, knockdowns and loss-of-function mutants for the genes encoding the initial enzymes of the pathway PAH, TH and DDC lead to loss of cuticle coloration in D. melanogaster, O. fasciatus and V. cardui, to soft cuticles in T. castaneum and Anopheles sinenses [14,48], and decrease in first instar hatching in R. prolixus and B. mori [38,49]. The reduction in hatching rates may result from softness of the eggshell, as eggshell structure depends on adequate sclerotization, making it difficult for the emerging nymphs to punch through the eggshell.…”

Section: An Alternative Strategy For Cuticle Pigmentation In R Prolixusmentioning

confidence: 99%

“…Due to the excessive amount of protein ingested during the blood meal, mounting to several times their body weight, insects depend on the detoxification of dietary tyrosine for optimal fitness. Therefore, it has been suggested that blood-feeding insects evolved strategies to reduce the redox stress employing the tyrosine pathway [38]. Thus, investigating how the melanin pathway was coopted to serve both for body color and a detox functions in blood feeding species may be particularly relevant for the biology of bloodsucking insects.…”

Section: Introductionmentioning

confidence: 99%

Pigmentation loci as markers for genome editing in the Chagas disease vector Rhodnius prolixus

Berni

Bressan

Simão

et al. 2020

Preprint

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The kissing bug Rhodnius prolixus is a major vector for Chagas disease in the Americas, and also considered as the primary model for functional studies.Prospective transgenic approaches and genome editing strategies hold great promise for controlling insect populations as well as disease propagation. In this context, identifying visible genetic markers for transgenic methodologies is of paramount importance to advance the field. Here we have identified and analyzed the function of putative cuticle and eye color genes by investigating the effect of gene knockdown on fertility, viability, and the generation of visible phenotypes. Synthesis of the dark, yellow and tan pigments present in the cuticle of most insects depends on the function of key genes encoding enzymes in the tyrosine pathway. Knockdown of the R. prolixus yellow and aaNAT/pro orthologs produces striking alterations in cuticle color.Surprisingly, knockdown of ebony does not generate visible phenotypes. Since loss of ebony function results in a dark cuticle in several insect orders, we conclude that R. prolixus evolved alternative strategies for cuticle coloration, possibly including the loss of a pigmentation function for an entire branch of the tyrosine pathway. Knockdown of the scarlet and brown genes -encoding ABC transporters -alters cuticle and eye pigmentation, implying that the transport of pigment into proper organelles is an important process both for cuticle and eye coloration in this species. Therefore, this analysis identifies for the first time potential visible markers for transgenesis in a hemipteran vector for a debilitating human disease. Author SummaryThe hemipteran Rhodnius prolixus -also known as a kissing bug -is a main vector transmitting the parasite Trypanosoma cruzi, the causative agent of Chagas disease, a debilitating infection estimated to affect more than 6 million people in Central and South America. In order to limit disease spread, an important measure is insect vector control. However, kissing bugs -like other insects -develop resistance to insecticides.Alternative strategies based on transgenesis and the recently developed CRISPRbased genome edition hold great promise to control vector population or generate parasite-resistant insects. For these approaches to be feasible in R. prolixus, it is critical to identify visible phenotypic markers. Here we identify and describe several genes controlling cuticle and eye pigmentation that are well-suited putative landing sites for transformation strategies. Among these, loss-of-function mutations in the ABC transporter encoding scarlet and the tyrosine pathway enzyme encoding aaNAT/pro generate striking and easily visible phenotypes. Importantly, the knockdown of these genes does not affect insect viability and fertility under laboratory conditions. Our results suggest that R. prolixus has developed alternative strategies for cuticle coloration involving the loss of an entire branch of tanning loci, while the other branch producing cuticle patterns by generating non-pigmented a...

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“…While insect vectors reduce mitochondrial oxidant production in different species and tissues (Gonçalves et al, ; Oliveira et al, ; Bottino‐Rojas et al, ; Gandara et al, ), blood dwelling parasites boost mitochondrial ROS generation when exposed to blood products (Gonçalves et al, ; Nogueira et al, ; Oliveira et al, ; Nogueira et al, ). Despite important biological aspects underlying the management of a blood meal, including diuresis, host hormone signaling, and nutritional overload were previously reviewed (Luckhart and Riehle, ; Orchard, ; Sterkel et al, ), here, we will discuss how blood derived products modulates energy metabolism in hematophagous organisms of medical importance, focusing on the observed changes in mitochondrial function and structure. We will also discuss how these changes would contribute to the ability of these organisms use blood as a dietary source, and the consequences to cellular redox balance.…”

Section: A Switch In Energy Metabolism As a Biochemical Hallmark In Bmentioning

confidence: 99%

“…Regardless the model, the red cells are lysed, releasing their hemoglobin content in the gut lumen, which is further degraded by an orchestrated sequence of proteases generating peptides, amino acids, and heme (Houseman and Downe, 1982;Brindley et al, 1997;Goldberg, 2005). Although amino acids can be used to either support the energy demand through their oxidation, or serve as building blocks for protein synthesis at ovaries (Bursell, 1975;Brindley et al, 1997;Wang et al, 2015), they mediate key signaling effects, regulating cellular redox balance, energy metabolism, and immune response (GraS ca- Souza et al, 2006;Sterkel et al, 2017).…”

mentioning

confidence: 99%

Modulation of mitochondrial metabolism as a biochemical trait in blood feeding organisms: the redox vampire hypothesis redux

Ferreira

Oliveira

Paes

et al. 2018

Cell Biology International

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Hematophagous organisms undergo remarkable metabolic changes during the blood digestion process, increasing fermentative glucose metabolism, and reducing respiratory rates, both consequence of functional mitochondrial remodeling. Here, we review the pathways involved in energy metabolism and mitochondrial functionality in a comparative framework across different hematophagous species, and consider how these processes regulate redox homeostasis during blood digestion. The trend across distinct species indicate that a switch in energy metabolism might represent an important defensive mechanism to avoid the potential harmful interaction of oxidants generated from aerobic energy metabolism with products derived from blood digestion. Indeed, in insect vectors, blood feeding transiently reduces respiratory rates and oxidant production, irrespective of tissue and insect model. On the other hand, a different scenario is observed in several unrelated parasite species when exposed to blood digestion products, as respiratory rates reduce and mitochondrial oxidant production increase. The emerging picture indicates that re-wiring of energy metabolism, through reduced mitochondrial function, culminates in improved tolerance to redox insults and seems to represent a key step for hematophagous organisms to cope with the overwhelming and potentially toxic blood meal.

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The Dose Makes the Poison: Nutritional Overload Determines the Life Traits of Blood-Feeding Arthropods

Cited by 86 publications

References 101 publications

On the use of inhibitors of 4-hydroxyphenylpyruvate dioxygenase as a vector-selective insecticide in the control of mosquitoes

On the use of inhibitors of 4-hydroxyphenylpyruvate dioxygenase as a vector-selective insecticide in the control of mosquitoes

Pigmentation loci as markers for genome editing in the Chagas disease vector Rhodnius prolixus

Modulation of mitochondrial metabolism as a biochemical trait in blood feeding organisms: the redox vampire hypothesis redux

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