Juvenile hormone promotes locust fat body cell polyploidization and vitellogenesis by activating the transcription of Cdk6 and E2f1

Wu, Zhengzheng; Guo, Wei; Yang, Liman; He, Qiongjie; Zhou, Shutang

doi:10.1016/j.ibmb.2018.09.002

Cited by 55 publications

(66 citation statements)

References 62 publications

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“…In mosquito Aedes aegypti , expression of Kr-h1 triggered by Met together with Cycle and steroid receptor coactivator SRC/FISC after adult emergence supported that sesquiterpenoid is essential for previtellogenic development ( Zhu et al, 2010 ; Shin et al, 2012 ). In migratory locust Locusta migratoria , JH together with Met/SRC complex are found to be pivotal in maintaining Vg expression and oocyte development ( Song et al, 2014 ), and can promote cell polyploidization by regulating the expression of cyclin-dependent kinase 6 ( Cdk6 ) and adenovirus E2 factor-1 ( E2f1 ) ( Wu et al, 2016 ; Wu Z. et al, 2018 ; Figure 4Aiii ). JH activates Na + /K + -ATPase for the induction of patency in vitellogenic follicular epithelium, where Vg can then reach the surface of maturing oocyte ( Jing et al, 2018 ).…”

Section: Diverse Roles Of Sesquiterpenoids In Insectsmentioning

confidence: 99%

Diversity of Insect Sesquiterpenoid Regulation

Tsang

Law

et al. 2020

Front. Genet.

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Insects are arguably the most successful group of animals in the world in terms of both species numbers and diverse habitats. The sesquiterpenoids juvenile hormone, methyl farnesoate, and farnesoic acid are well known to regulate metamorphosis, reproduction, sexual dimorphism, eusociality, and defense in insects. Nevertheless, different insects have evolved with different sesquiterpenoid biosynthetic pathway as well as products. On the other hand, non-coding RNAs such as microRNAs have been implicated in regulation of many important biological processes, and have recently been explored in the regulation of sesquiterpenoid production. In this review, we summarize the latest findings on the diversity of sesquiterpenoids reported in different groups of insects, as well as the recent advancements in the understanding of regulation of sesquiterpenoid production by microRNAs.

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Section: Diverse Roles Of Sesquiterpenoids In Insectsmentioning

confidence: 99%

Diversity of Insect Sesquiterpenoid Regulation

Tsang

Law

et al. 2020

Front. Genet.

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“…In L. migratoria, JH acts independently of 20E to promote vitellogenesis, oogenesis and egg maturation (Belles, 2004;Raikhel et al, 2005;Song et al, 2013;Song et al, 2019). During the first gonadotrophic cycle of locusts, the fat body, homologue to Development • Accepted manuscript vertebrate liver and adipose tissue, undergoes endocycling to produce up to 32C (chromatin-value) polyploid cells (Guo et al, 2014;Wu et al, 2016;Wu et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

“…The polyploidization of fat body cells in adult female locusts is induced by JH, which facilitates the massive synthesis of Vg and possibly other proteins required for multiple egg production (Guo et al, 2014;Wu et al, 2016;Wu et al, 2018). However, the regulatory mechanisms of polyploidization regulated by JH remain poorly understood.…”

Section: Introductionmentioning

confidence: 99%

Juvenile hormone acts through FoxO to promote Cdc2 and Orc5 transcription for polyploidy-dependent vitellogenesis

Zeng

et al. 2020

Development

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Vitellogenin (Vg) is prerequisite to egg production and embryonic development after oviposition in oviparous animals. In many insects, juvenile hormone (JH) promotes fat body cell polyploidization for massive Vg synthesis required for maturation of multiple oocytes, but the underlying mechanisms remain poorly understood. Using the migratory locust Locusta migratoria as a model system, we report here that JH induces the dephosphorylation of Forkhead box O transcription factor (FoxO) through a signaling cascade including leucine carboxyl methyltransferase 1 (LCMT1) and protein phosphatase 2A (PP2A). JH promotes PP2A activity via LCMT1-mediated methylation, consequently triggering FoxO dephosphorylation. Dephosphorylated FoxO binds to the upstream of two endocycle-related genes, cell-division-cycle 2 (Cdc2) and origin-recognition-complex subunit 5 (Orc5) and activates their transcription. Depletion of FoxO, Cdc2 or Orc5 results in blocked polyploidization of fat body cells, accompanied by markedly reduced Vg expression, impaired oocyte maturation and arrested ovarian development. The results suggest that JH acts via LCMT1-PP2A-FoxO to regulate Cdc2 and Orc5 expression and enhance ploidy of fat body cells in preparation for large-scale Vg synthesis required for synchronous maturation of multiple eggs.

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“…The molecular action of JH relies on its intracellular receptor Methoprene-tolerant (Met), a member of basic helix-loophelix Per-Arnt-Sim (bHLH-PAS) transcription factor family (Charles et al, 2011;Jindra et al, 2015b;Li et al, 2011). JH induces the heterodimerization of Met with another bHLH-PAS protein, Taiman (Tai), to form an active JH-receptor complex that regulates the transcription of JH-responsive genes (Guo et al, 2014;Kayukawa et al, 2012;Li et al, 2011;Luo et al, 2017;Wu et al, 2018b). Krüppel-homolog 1 (Kr-h1), a C 2 H 2 zinc-finger transcription factor, is a key player in JH signaling pathway.…”

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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Juvenile hormone promotes locust fat body cell polyploidization and vitellogenesis by activating the transcription of Cdk6 and E2f1

Cited by 55 publications

References 62 publications

Diversity of Insect Sesquiterpenoid Regulation

Diversity of Insect Sesquiterpenoid Regulation

Juvenile hormone acts through FoxO to promote Cdc2 and Orc5 transcription for polyploidy-dependent vitellogenesis

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

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