Krüppel homologue 1 acts as a repressor and an activator in the transcriptional response to juvenile hormone in adult mosquitoes

Ojani, Reyhaneh; Fu, Xiaonan; Ahmed, Tahmina Hossain; Liu, Peng-Cheng; Zhu, Jinsong

doi:10.1111/imb.12370

Cited by 42 publications

(50 citation statements)

References 39 publications

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“…The role of Kr-h1 in JH-regulated female reproduction appears to vary among insect species. In the mosquito Aedes aegypti, Kr-h1 can activate and repress the expression of its target genes for previtellogenic development and egg production in response to JH (Ojani et al, 2018;Shin et al, 2012;Zou et al, 2013). Depletion of Kr-h1 in adult females of the common bed bug Cimex lectularius does not reduce the egg number but severely reduces the egg hatchability (Gujar and Palli, 2016).…”

Section: Introductionmentioning

confidence: 99%

The microRNAs let-7 and miR-278 regulate insect metamorphosis and oogenesis by targeting the juvenile hormone early-response gene Krüppel-homolog 1

Song

Zhao

et al. 2018

Development

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Krüppel-homolog 1 (Kr-h1), a zinc-finger transcription factor, inhibits larval metamorphosis and promotes adult reproduction by transducing juvenile hormone (JH). Although the transcriptional regulation of Kr-h1 has been extensively studied, little is known about its regulation at the post-transcriptional level. Using the migratory locust Locusta migratoria as a model system, we report here that the microRNAs let-7 and miR-278 bound to the Kr-h1 coding sequence and downregulated its expression. Application of let-7 and miR-278 mimics (agomiRs) significantly reduced the level of Kr-h1 transcripts, resulting in partially precocious metamorphosis in nymphs as well as markedly decreased yolk protein precursors, arrested ovarian development and blocked oocyte maturation in adults. Moreover, the expression of let-7 and miR-278 was repressed by JH, constituting a regulatory loop of JH signaling. This study thus reveals a previously unknown regulatory mechanism whereby JH suppresses the expression of let-7 and miR-278, which, together with JH induction of Kr-h1 transcription, prevents the precocious metamorphosis of nymphs and stimulates the reproduction of adult females. These results advance our understanding of the coordination of JH and miRNA regulation in insect development.

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Section: Introductionmentioning

confidence: 99%

The microRNAs let-7 and miR-278 regulate insect metamorphosis and oogenesis by targeting the juvenile hormone early-response gene Krüppel-homolog 1

Song

Zhao

et al. 2018

Development

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“…Kr-h1 represses the transcription of Broad-complex (Br-C), which triggers pupal commitment in holometabolous insects (13-15). Kr-h1 also inhibits the transcription of Ecdysone induced protein 93F (E93) (16), which is defined as an adult specifier promoting adult metamorphosis in both hemimetabolous and holometabolous insects (16)(17)(18)(19)(20).Vitellogenesis, vitellogenin (Vg) synthesized in the fat body, transported by hemolymph, and taken up by maturing oocytes, is a prerequisite to egg production of many insects. In hemimetabolous insects, including the migratory locust Locusta migratoria, the linden bug Pyrrhocoris apterus, and the cockroach Blattella germanica, JH acts independent of 20E to promote vitellogenesis and oocyte maturation (4, 8, 21-24).…”

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confidence: 99%

Juvenile hormone–dependent Kazal‐type serine protease inhibitor Greglin safeguards insect vitellogenesis and egg production

Guo

Yang

et al. 2018

The FASEB Journal

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In addition to preventing insect metamorphosis, juvenile hormone (JH) is known to stimulate aspects of insect reproduction. However, the molecular mechanisms of JH action in insect reproduction remain largely unknown. By reanalyzing the transcriptomic data from adults and other developmental stages of the migratory locust Locusta migratoria, we identified a gene coding for Kazal-type protease inhibitor, previously named Greglin. Greglin is specifically expressed in adult females and most abundant in the fat body and ovaries. Interestingly, Greglin is among the top 3 of highly expressed genes in adult female locusts, after 2 vitellogenin ( Vg) genes. Greglin is induced by JH and expressed at remarkably high levels in the vitellogenic stage. Knockdown of Greglin in adult female locusts results in accelerated degradation of serine protease substrate and significantly reduced levels of Greglin protein in hemolymph and ovaries. The consequent phenotypes include blocked oocyte maturation, arrested ovarian growth and shrunken follicular epithelium, as well as declines in egg number and hatchability. The data provide the first evidence, to our knowledge, that JH-dependent Greglin is involved in locust vitellogenesis and oocyte maturation likely by protecting vitellogenesis and other forms of yolk precursors from proteolysis. The result offers new insights into the regulation of JH and function of protease inhibitors in insect vitellogenesis, oocyte maturation and fecundity.-Guo, W., Wu, Z., Yang, L., Cai, Z., Zhao, L., Zhou, S. Juvenile hormone-dependent Kazal-type serine protease inhibitor Greglin safeguards insect vitellogenesis and egg production.

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“…The Ae. aegypti Liverpool strain was reared as described previously [64]. Mosquitoes were maintained at 28°C and 60-70% relative humidity on a 14:10 h light: dark cycle.…”

Section: Mosquito Rearingmentioning

confidence: 99%

“…Expression of the Met gene was knocked down by injection of double-stranded RNA (dsRNA) into newly emerged adult female mosquitoes as described previously [64]. DsRNA for the presented as mean ± SD from three independent replicates.…”

Section: Rnai-mediated Gene Silencingmentioning

confidence: 99%

The juvenile hormone receptor Methoprene-tolerant is involved in the sterilizing effect of pyriproxyfen on adultAedes aegyptimosquitoes

Ahmed

Saunders

Mullins

et al. 2020

Preprint

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Exposure of adult mosquitoes to pyriproxyfen (PPF), an analog of insect juvenile hormone (JH), has shown promise to effectively sterilize female mosquitoes. However, the underlying mechanisms of the PPF-induced decrease in mosquito fecundity are largely unknown. We performed a comprehensive study to dissect the mode of PPF action in Aedes aegypti mosquitoes. Exposure to PPF prompted the overgrowth of primary follicles in sugar-fed Ae.aegypti females but blocked the development of primary follicles at Christopher's Stage III after blood feeding. Secondary follicles were precociously activated in PPF-treated mosquitoes.Moreover, PPF substantially altered the expression of many genes that are essential for mosquito physiology and oocyte development in the fat body and ovary. In particular, many metabolic genes were differentially expressed in response to PPF treatment, thereby affecting the mobilization and utilization of energy reserves. Furthermore, PPF treatment on the previtellogenic female adults considerably modified mosquito responses to JH and 20hydroxyecdysone (20E), two major hormones that govern mosquito reproduction. Krüppel homolog 1, a JH-inducible transcriptional regulator, showed consistently elevated expression after PPF exposure. Conversely, PPF upregulated the expression of several key players of the 20E regulatory cascades, including HR3 and E75A, in the previtellogenic stage. After bloodfeeding, the expression of these 20E response genes was significantly weaker in PPF-treated mosquitoes than the solvent-treated control groups. RNAi-mediated knockdown of the Methoprene-tolerant (Met) protein, the JH receptor, partially rescued the impaired follicular development after PPF exposure and substantially increased the hatching of the eggs produced by PPF-treated female mosquitoes. Thus, the results suggested that PPF relied on Met to exert its sterilizing effects on female mosquitoes. In summary, this study finds that PPF exposure disturbs normal hormonal responses and metabolism in Ae. aegypti, shedding light on the molecular targets and the downstream signaling pathways activated by PPF. Author summaryAedes aegypti mosquitoes are responsible for the transmission of dengue, yellow fever, chikungunya, and Zika fever. Insecticides are widely used as the primary tool in the prevention and control of these infectious diseases. In light of the rapid increase of insecticide resistance in mosquito populations, there is an urgent need to find new classes of insecticides with a different mode of action. Here we found that pyriproxyfen, an analog of insect juvenile hormone (JH), had a large impact on the oocyte development, both before and after blood feeding, in female mosquitoes. Pyriproxyfen disturbed normal hormonal responses and caused metabolic shifting in female adults. These actions appear to collectively impair oocyte development and substantially reduce viable progenies of female mosquitoes. Besides, we demonstrated the involvement of the JH receptor Met in pyriproxyfen-induced female sterilization. ...

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Krüppel homologue 1 acts as a repressor and an activator in the transcriptional response to juvenile hormone in adult mosquitoes

Cited by 42 publications

References 39 publications

The microRNAs let-7 and miR-278 regulate insect metamorphosis and oogenesis by targeting the juvenile hormone early-response gene Krüppel-homolog 1

The microRNAs let-7 and miR-278 regulate insect metamorphosis and oogenesis by targeting the juvenile hormone early-response gene Krüppel-homolog 1

Juvenile hormone–dependent Kazal‐type serine protease inhibitor Greglin safeguards insect vitellogenesis and egg production

The juvenile hormone receptor Methoprene-tolerant is involved in the sterilizing effect of pyriproxyfen on adultAedes aegyptimosquitoes

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