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      Heat shock proteins, thermotolerance, and insecticide resistance in mosquitoes

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          Abstract

          Mosquitoes transmit pathogens that pose a threat to millions of people globally. Unfortunately, widespread insecticide resistance makes it difficult to control these public health pests. General mechanisms of resistance, such as target site mutations or increased metabolic activity, are well established. However, many questions regarding the dynamics of these adaptations in the context of developmental and environmental conditions require additional exploration. One aspect of resistance that deserves further study is the role of heat shock proteins (HSPs) in insecticide tolerance. Studies show that mosquitoes experiencing heat stress before insecticide exposure demonstrate decreased mortality. This is similar to the observed reciprocal reduction in mortality in mosquitoes exposed to insecticide prior to heat stress. The environmental shifts associated with climate change will result in mosquitoes occupying environments with higher ambient temperatures, which could enhance existing insecticide resistance phenotypes. This physiological relationship adds a new dimension to the problem of insecticide resistance and further complicates the challenges that vector control and public health personnel face. This article reviews studies illustrating the relationship between insecticide resistance and HSPs or hsp genes as well as the intersection of thermotolerance and insecticide resistance. Further study of HSPs and insecticide resistance could lead to a deeper understanding of how environmental factors modulate the physiology of these important disease vectors to prepare for changing climatic conditions and the development of novel strategies to prevent vector-borne disease transmission.

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          Most cited references49

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          Heat-shock protein 70 inhibits apoptosis by preventing recruitment of procaspase-9 to the Apaf-1 apoptosome.

          The cellular-stress response can mediate cellular protection through expression of heat-shock protein (Hsp) 70, which can interfere with the process of apoptotic cell death. Stress-induced apoptosis proceeds through a defined biochemical process that involves cytochrome c, Apaf-1 and caspase proteases. Here we show, using a cell-free system, that Hsp70 prevents cytochrome c/dATP-mediated caspase activation, but allows the formation of Apaf-1 oligomers. Hsp70 binds to Apaf-1 but not to procaspase-9, and prevents recruitment of caspases to the apoptosome complex. Hsp70 therefore suppresses apoptosis by directly associating with Apaf-1 and blocking the assembly of a functional apoptosome.
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            The evolutionary origins of pesticide resistance

            Abstract Durable crop protection is an essential component of current and future food security. However, the effectiveness of pesticides is threatened by the evolution of resistant pathogens, weeds and insect pests. Pesticides are mostly novel synthetic compounds, and yet target species are often able to evolve resistance soon after a new compound is introduced. Therefore, pesticide resistance provides an interesting case of rapid evolution under strong selective pressures, which can be used to address fundamental questions concerning the evolutionary origins of adaptations to novel conditions. We ask: (i) whether this adaptive potential originates mainly from de novo mutations or from standing variation; (ii) which pre‐existing traits could form the basis of resistance adaptations; and (iii) whether recurrence of resistance mechanisms among species results from interbreeding and horizontal gene transfer or from independent parallel evolution. We compare and contrast the three major pesticide groups: insecticides, herbicides and fungicides. Whilst resistance to these three agrochemical classes is to some extent united by the common evolutionary forces at play, there are also important differences. Fungicide resistance appears to evolve, in most cases, by de novo point mutations in the target‐site encoding genes; herbicide resistance often evolves through selection of polygenic metabolic resistance from standing variation; and insecticide resistance evolves through a combination of standing variation and de novo mutations in the target site or major metabolic resistance genes. This has practical implications for resistance risk assessment and management, and lessons learnt from pesticide resistance should be applied in the deployment of novel, non‐chemical pest‐control methods.
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              Small heat shock proteins are molecular chaperones.

              Small heat shock proteins (sHsp) with a molecular mass of 15-30 kDa are ubiquitous and conserved. Up to now their function has remained enigmatic. Increased expression under heat shock conditions and their protective effect on cell viability at elevated temperatures suggest that they may have a function in the formation or maintenance of the native conformation of cytosolic proteins. To test this hypothesis we studied the influence of murine Hsp25, human Hsp27, and bovine alpha-B-crystallin (an eye lens protein homologous to sHsps) on the unfolding and refolding of citrate synthase and alpha-glucosidase in vitro. Here we show that all sHsps investigated act as molecular chaperones in these folding reactions. At stoichiometric amounts they maximally prevent the aggregation of citrate synthase and alpha-glucosidase under heat shock conditions and stabilize the proteins. Furthermore, they promote the functional refolding of these proteins after urea denaturation similar to GroE and Hsp90. The interaction both with unfolding and refolding proteins seems to be ATP-independent.
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                Author and article information

                Contributors
                URI : https://loop.frontiersin.org/people/1358581Role: Role:
                URI : https://loop.frontiersin.org/people/994432Role:
                Journal
                Front Insect Sci
                Front Insect Sci
                Front. Insect Sci.
                Frontiers in Insect Science
                Frontiers Media S.A.
                2673-8600
                2673-8600
                25 January 2024
                2024
                : 4
                : 1309941
                Affiliations
                [1] Department of Entomology and Nematology, University of California, Davis , Davis, CA, United States
                Author notes

                Edited by: Nicholas Teets, University of Kentucky, United States

                Reviewed by: Michelle Marie Riehle, Medical College of Wisconsin, United States

                Oluwaseun Ajayi, University of Cincinnati, United States

                *Correspondence: Geoffrey M. Attardo, gmattardo@ 123456ucdavis.edu
                Article
                10.3389/finsc.2024.1309941
                10926544
                38469339
                4f85d056-b0a7-4b2c-a8fa-38a115f652df
                Copyright © 2024 Mack and Attardo

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 09 October 2023
                : 08 January 2024
                Page count
                Figures: 2, Tables: 0, Equations: 0, References: 51, Pages: 7, Words: 2886
                Funding
                This work was supported by funding from the Agricultural Experiment Station Grant (NIFA) - CA-D-ENM-2477-H and a by cooperative agreement U01CK000649 funded by the U.S. Centers for Disease Control and Prevention. Its contents are solely the responsibility of the authors and do not necessarily represent the official views of the Centers for Disease Control and Prevention or the Department of Health and Human Services.
                Categories
                Insect Science
                Mini Review
                Custom metadata
                Insect Physiology

                hsps (heat shock proteins),mosquito,insecticide resistance,thermotolerance,heat shock protein genes

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