An isoform of Taiman that contains a PRD-repeat motif is indispensable for transducing the vitellogenic juvenile hormone signal in Locusta migratoria

Wang, Zhiming; Yang, Liman; Song, Jiazheng; Kang, Le; Zhou, Shutang

doi:10.1016/j.ibmb.2017.01.009

Cited by 35 publications

(34 citation statements)

References 49 publications

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“…To determine whether the JHreceptor directly activates the transcription of Grp78-2, we performed luciferase assays using S2 cells co-transfected with the wild-type or mutational pGL4.10-Grp78-2(Ϫ2068 to Ϫ24) plus pAc5.1/Flag-Met(1-3108) and/or pAc5.1/V5-Tai(1-1785 plus 4581-4961). It must be noted that this Tai variant is Tai-A isoform with the INDEL-1/PRD motif (52). In Drosophila, Met has a paralogue, Germ cell-expressed (Gce; FlyBase: FBpp0292296), which shares about 40% identity of amino acids (59,60).…”

Section: Differential Regulation Of Grp78-1 and Grp78-2 By Jhmentioning

confidence: 99%

“…For the recombinant proteins, locust Met (GenBank TM KF471131; nt 1-3108) and Tai (Tai-A isoform, GenBank TM KU315327; nt 1-1785 plus 4581-4961) cDNA were cloned into pAc5.1/FLAG and pAc5.1/V5 vectors (Invitrogen), respectively (52). Drosophila S2 cells were transfected with pAc5.1/Flag-Met and/or pAc5.1/V5-Tai using Lipofectamine 2000 (Invitrogen) for 48 h, followed by treatment with 10 M methoprene for 6 h. Cells were then lysed with the ice-cold lysis buffer and cleared by centrifugation.…”

Section: Western Blot Analysis and Immunoprecipitationmentioning

confidence: 99%

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Juvenile hormone differentially regulates two Grp78 genes encoding protein chaperones required for insect fat body cell homeostasis and vitellogenesis

Luo

Wang

et al. 2017

Journal of Biological Chemistry

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Juvenile hormone (JH) has a well known role in stimulating insect vitellogenesis ( yolk deposition) and oocyte maturation, but the molecular mechanisms of JH action in insect reproduction are unclear. The 78-kDa glucose-regulated protein (Grp78) is a heat shock protein 70-kDa family member and one of the most abundant chaperones in the endoplasmic reticulum (ER) where it helps fold newly synthesized peptides. Because of its prominent role in protein folding, and also ER stress, we hypothesized that might be involved in fat body cell homeostasis and vitellogenesis and a regulatory target of JH. We report here that the migratory locust possesses two genes that are differentially regulated by JH. We found that is regulated by JH through Mcm4/7-dependent DNA replication and polyploidization, whereas expression is directly activated by the JH-receptor complex comprising methoprene-tolerant and Taiman proteins. Interestingly, expression in the fat body is about 10-fold higher than that of Knockdown of either or significantly reduced levels of vitellogenin (Vg) protein, accompanied by retarded maturation of oocytes. Depletion of both and resulted in ER stress and apoptosis in the fat body and in severely defective Vg synthesis and oocyte maturation. These results indicate a crucial role of Grp78 in JH-dependent vitellogenesis and egg production. The presence and differential regulation of two genes in likely help accelerate the production of this chaperone in the fat body to facilitate folding of massively synthesized Vg and other proteins.

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Section: Differential Regulation Of Grp78-1 and Grp78-2 By Jhmentioning

confidence: 99%

Section: Western Blot Analysis and Immunoprecipitationmentioning

confidence: 99%

Juvenile hormone differentially regulates two Grp78 genes encoding protein chaperones required for insect fat body cell homeostasis and vitellogenesis

Luo

Wang

et al. 2017

Journal of Biological Chemistry

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“…During insect vitellogenesis, vitellogenin (Vg) 2 and other forms of yolk proteins are mostly synthesized in the fat body (analogue to the liver and adipose tissue in vertebrates), secreted into the hemolymph, and taken up by the developing oocytes (1)(2)(3). This process is stimulated by the arthropod-specific sesquiterpenoid hormone, juvenile hormone (JH), in insects belonging to diverse orders, such as the coleopteran beetle Tribolium castaneum, the dictyopteran cockroach Blattella germanica, and the orthopteram migratory locust Locusta migratoria (1)(2)(3)(4)(5). In the process of insect vitellogenesis, JH acts on follicle cells, initiating the intercellular channels (termed patency) to permit Vg in the hemolymph to gain access to the oocyte membrane where Vg is internalized into maturing oocytes by receptor-mediated endocytosis (6 -9).…”

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confidence: 99%

Protein kinase C mediates juvenile hormone–dependent phosphorylation of Na+/K+-ATPase to induce ovarian follicular patency for yolk protein uptake

Jing

Zhang

et al. 2018

Journal of Biological Chemistry

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In oviparous animals, vitellogenesis is prerequisite to egg production and embryonic growth after oviposition. For successful insect vitellogenesis and oogenesis, vitellogenin (Vg) synthesized in the fat body (homologue to vertebrate liver and adipose tissue) must pass through the intercellular channels, a condition known as patency in the follicular epithelium, to reach the surface of oocytes. This process is controlled by juvenile hormone (JH) in many insect species, but the underlying mechanisms remain elusive. Previous work has suggested the possible involvement of Na ؉ /K ؉ -ATPase in patency initiation, but again, the regulatory cascade of Na ؉ /K ؉ -ATPase for patency initiation has been lacking. Using the migratory locust Locusta migratoria as a model system, we report here that RNAi-mediated knockdown of gene coding for Na ؉ /K ؉ -ATPase, inhibition of its phosphorylation, or suppression of its activity causes loss of patency, resulting in blocked Vg uptake, arrested oocyte maturation, and impaired ovarian growth. JH triggers G proteincoupled receptor (GPCR), receptor tyrosine kinase (RTK), phospholipase C (PLC), inositol trisphosphate receptor (IP3R), and protein kinase C (PKC) to phosphorylate Na ؉ /K ؉ -ATPase ␣-subunit at amino acid residue Ser 8 , consequently activating Na ؉ /K ؉ -ATPase for the induction of patency in vitellogenic follicular epithelium. Our results thus point to a previously unidentified mechanism by which JH induces the phosphorylation and activation of Na ؉ /K ؉ -ATPase via a signaling cascade of GPCR, RTK, PLC, IP3R, and PKC. The findings advance our understanding of JH regulation in insect vitellogenesis and oogenesis.

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“…The hormone 20E acts by binding to its receptors ecdysteroid receptor (EcR) and ultraspiracle (USP) to form a complex, which binds to ecdysone response element (EcRE) to initiate the transcription of 20E primary-response genes such as E74A, E75B, hormone receptor 3 (HR3) and carbA (Zheng et al, 2010), subsequently activating downstream signalling pathways to promote moulting and metamorphosis in insects. Then Met binds to another basic helix-loop-helix PAS transcription factor named Taiman (also known as steroid receptor co-activator) to form a transcriptionally active heterodimer to promote the transcription of JH-regulated Krüppel homologue 1 (Krh1) to maintain the larval status (Zhu et al, 2006;Charles et al, 2011;Li et al, 2011;Zhang et al, 2011;Zhao et al, 2014;Wang et al, 2017). High levels of JH during larval stages can counteract 20E action to prevent metamorphosis, and low levels or absence of JH at the end of the larval stages allow 20E to promote metamorphosis in Lepidoptera (Zhou and Riddiford, 2002).…”

Section: Introductionmentioning

confidence: 99%

“…JH exerts its effect by its receptor, methoprene-tolerant protein (Met) (Ashok et al, 1998), which binds to JH III with high affinity by its C-terminal Per-Arnt-Sim (PAS) domain (Charles et al, 2011). Then Met binds to another basic helix-loop-helix PAS transcription factor named Taiman (also known as steroid receptor co-activator) to form a transcriptionally active heterodimer to promote the transcription of JH-regulated Krüppel homologue 1 (Krh1) to maintain the larval status (Zhu et al, 2006;Charles et al, 2011;Li et al, 2011;Zhang et al, 2011;Zhao et al, 2014;Wang et al, 2017). It has also been reported that Met regulated Krh1 through a conserved JH response element containing an E-box motif (CACGTG) (Kayukawa et al, 2012;Cui et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Vrille is required for larval moulting and metamorphosis of Helicoverpa armigera (Lepidoptera: Noctuidae)

Liu

Zhang

Liu

et al. 2019

Insect Molecular Biology

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Vrille (Vri), a basic leucine zipper transcription factor, plays important roles in insect circadian clock regulation, tracheal development, proliferation, flight and metamorphosis. Here, Helicoverpa armigera was used as a model to investigate the role of Vri in larval moulting and metamorphosis. Sequence analysis results revealed that H. armigera Vri (HaVri) shares a high amino acid identity with other Lepidoptera Vri homologues. Spatial–temporal expression pattern data showed that HaVri expression was highly abundant in larval moulting and metamorphosis stages and was mainly expressed in the midgut and Malpighian tubule during metamorphosis. HaVri knockdown by RNA interference in the fourth‐instar larvae prevented larval moulting, and HaVri knockdown in the fifth‐instar larvae suppressed midgut remodelling and delayed or blocked metamorphosis. Further studies confirmed that 20‐hydroxyecdysone (20E) activated HaVri expression via its heterodimer receptors, ecdysone receptor (EcRB1) and ultraspiracle protein (USP1), whereas methoprene [juvenile hormone analogue (JHA)] promoted HaVri expression via its intracellular receptor methoprene‐tolerant (Met1). However, 20E and JHA can counteract each other in the activation of HaVri expression. Together, the present results suggested that HaVri was involved in larval moulting and metamorphosis and was regulated by 20E and JHA in H. armigera.

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An isoform of Taiman that contains a PRD-repeat motif is indispensable for transducing the vitellogenic juvenile hormone signal in Locusta migratoria

Cited by 35 publications

References 49 publications

Juvenile hormone differentially regulates two Grp78 genes encoding protein chaperones required for insect fat body cell homeostasis and vitellogenesis

Juvenile hormone differentially regulates two Grp78 genes encoding protein chaperones required for insect fat body cell homeostasis and vitellogenesis

Protein kinase C mediates juvenile hormone–dependent phosphorylation of Na+/K+-ATPase to induce ovarian follicular patency for yolk protein uptake

Vrille is required for larval moulting and metamorphosis of Helicoverpa armigera (Lepidoptera: Noctuidae)

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