Arthropod-borne diseases: vector control in the genomics era

Hill, Catherine A.; Kafatos, Fotis C.; Stansfield, Sally K.; Collins, Frank H.

doi:10.1038/nrmicro1101

Cited by 128 publications

(112 citation statements)

References 16 publications

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“…Diseases transmitted by insects result in a million deaths per year (1), and insect infestation leads to annual losses of agricultural products worth billions of US dollars (2). The high toxicity of currently available insecticides presents environmental and health risks, and growing resistance and cross-resistance of insects to these existing insecticides gravely complicates the situation.…”

mentioning

confidence: 99%

Identification of plant compounds that disrupt the insect juvenile hormone receptor complex

Lee

Fāng

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Insects impact human health through vector-borne diseases and cause major economic losses by damaging crops and stored agricultural products. Insect-specific growth regulators represent attractive control agents because of their safety to the environment and humans. We identified plant compounds that serve as juvenile hormone antagonists (PJHANs). Using the yeast twohybrid system transformed with the mosquito JH receptor as a reporter system, we demonstrate that PJHANs affect the JH receptor, methoprene-tolerant (Met), by disrupting its complex with CYCLE or FISC, formation of which is required for mediating JH action. We isolated five diterpene secondary metabolites with JH antagonist activity from two plants: Lindera erythrocarpa and Solidago serotina. They are effective in causing mortality of mosquito larvae at relatively low LD 50 values. Topical application of two diterpenes caused reduction in the expression of Met target genes and retardation of follicle development in mosquito ovaries. Hence, the newly discovered PJHANs may lead to development of a new class of safe and effective pesticides. Diseases transmitted by insects result in a million deaths per year (1), and insect infestation leads to annual losses of agricultural products worth billions of US dollars (2). The high toxicity of currently available insecticides presents environmental and health risks, and growing resistance and cross-resistance of insects to these existing insecticides gravely complicates the situation. Hence, there is an urgent need to develop novel effective insecticides.Insect growth regulators (IGRs) have been devised based on insect-specific functions. Three major classes of IGRs are commercially available (3). These IGRs include juvenile hormone (JH) agonists (methoprene and pyriproxyfen), ecdysone agonists (halofenozide and tebufenozide), and chitin synthase inhibitors (buprofezine). They possess low off-target toxicity and environmental danger and have been used to control pests. JHbased IGRs are of particular interest because JH is an insectspecific hormone. JH agonists (JHAs) disrupt insect endocrine regulation, causing abnormal development and larval fatality (4). However, JHAs have limitations in the scope of their applications because they mimic and enhance the JH mode of action. Theoretically, JH antagonists (JHANs) could be used as a powerful alternative, but no effective JHANs have yet been developed.Recent studies identified methoprene-tolerant (Met) as the JH receptor (5, 6). Met is a member of the family of basic helixloop-helix (bHLH)-Per-Arnt-Sim (PAS) transcription factors that requires homo-or heterodimerization for DNA binding and transcriptional regulation (7). In the Aedes aegypti mosquito, Met forms a heterodimer with other bHLH-PAS factors, the steroid receptor coactivator (SRC/FISC), or Cycle (CYC) in a JHdependent manner (8, 9). JH-mediated Met-CYC binding has been quantitatively simulated using the two-hybrid yeast β-galactosidase assay in a yeast cell, Y187 (9). Thus, it is possible to test both J...

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Identification of plant compounds that disrupt the insect juvenile hormone receptor complex

Lee

Fāng

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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“…nfectious agents that are transmitted by blood-feeding arthropods cause significant morbidity, mortality, and economic loss throughout the world (Hill et al 2005). Although mosquitoes surpass ticks as vectors of public health importance, ticks transmit the greatest variety of microbial pathogens of any arthropod vector including established, emerging, and resurging infectious agents (Walker 1998, Childs and Paddock 2003, Jongejan and Uilenberg 2004, Telford and Goethert 2004, Dennis and Piesman 2005, Ginsberg and Stafford 2005, Hanincová et al 2006, Walker 2005.…”

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confidence: 99%

Dermatologic Changes Induced by RepeatedIxodes scapularisBites and Implications for Prevention of Tick-Borne Infection

Krause

Grant‐Kels

Tahan

et al. 2009

Vector-Borne and Zoonotic Diseases

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Previous studies in rodents and people have demonstrated that repeated tick exposure is associated with reduced Borrelia burgdorferi transmission but the mechanism of prevention remains unclear. We examined the acute histopathologic reactions to initial and repeated Ixodes scapularis bites in BALB/c mice and in people. Skin biopsies of BALB/c mice infested for the first time by I. scapularis nymphs revealed vascular dilatation and an accumulation of inflammatory cells adjacent to the bite site but absent at the site of tick attachment. Such changes would enhance tick-borne pathogen transmission. Mice reexposed to I. scapularis nymphs experienced a decrease in vascular dilatation and a marked increase in inflammatory cells at the site of tick attachment. Skin biopsies of people with attached I. scapularis nymphs revealed similar histologic patterns. These results indicate that cellular changes at the tick-dermal interface following I. scapularis attachment are likely to allow for successful transmission of tick-borne pathogens in non-tick-immune hosts and to inhibit tick-borne pathogen transmission in hosts that have developed tick immunity.

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“…Many of these arthropods are blood feeders and transmit or acquire microorganisms during engorgement (1,2). Arthropods harbor a diverse group of native microbes ranging from bacteria to fungi, and the microbiota play critical functions in vector physiology, nutrition, and digestion (3)(4)(5)(6)(7)(8).…”

mentioning

confidence: 99%

Pathogen-mediated manipulation of arthropod microbiota to promote infection

Abraham

Liu

Jutras

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

220

295

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Arthropods transmit diverse infectious agents; however, the ways microbes influence their vector to enhance colonization are poorly understood.Ixodes scapularisticks harbor numerous human pathogens, includingAnaplasma phagocytophilum,the agent of human granulocytic anaplasmosis. We now demonstrate thatA. phagocytophilummodifies theI. scapularismicrobiota to more efficiently infect the tick.A. phagocytophiluminduces ticks to expressIxodes scapularisantifreeze glycoprotein (iafgp), which encodes a protein with several properties, including the ability to alter bacterial biofilm formation. IAFGP thereby perturbs the tick gut microbiota, which influences the integrity of the peritrophic matrix and gut barrier—critical obstacles forAnaplasmacolonization. Mechanistically, IAFGP binds the terminald-alanine residue of the pentapeptide chain of bacterial peptidoglycan, resulting in altered permeability and the capacity of bacteria to form biofilms. These data elucidate the molecular mechanisms by which a human pathogen appropriates an arthropod antibacterial protein to alter the gut microbiota and more effectively colonize the vector.

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Arthropod-borne diseases: vector control in the genomics era

Cited by 128 publications

References 16 publications

Identification of plant compounds that disrupt the insect juvenile hormone receptor complex

Identification of plant compounds that disrupt the insect juvenile hormone receptor complex

Dermatologic Changes Induced by RepeatedIxodes scapularisBites and Implications for Prevention of Tick-Borne Infection

Pathogen-mediated manipulation of arthropod microbiota to promote infection

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