Calcineurin-mediated Dephosphorylation of Acetyl-coA Carboxylase is Required for Pheromone Biosynthesis Activating Neuropeptide (PBAN)-induced Sex Pheromone Biosynthesis in Helicoverpa armigera

Du, Mingliang; Liu, Xiaoguang; Ma, Nana; Liu, Xiao‐Ming; Wei, Jinbei; X, Yin; Zhou, Shutang; Rafaeli, Ada; Song, Qisheng; An, Shiheng

doi:10.1074/mcp.ra117.000065

Cited by 36 publications

(63 citation statements)

References 54 publications

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“…The color presented on the insect body surface is regulated by multiple products in the pigment synthesis regulation network, which is reflected by the diverse phenotypes in response to melanin-related gene knockdown in BPH. Recently, pheromone biosynthesis activating neuropeptide has been found to directly activate acetyl-coA carboxylase, a key component in pheromone biosynthesis activating neuropeptideinduced sex pheromone biosynthesis via Ca 2+ / calcineurin-mediated dephosphorylation and cAMP/ PKA/AMPK-induced phosphorylation (38). Therefore, further efforts are required to examine whether or not elevenin signaling directly affects the activity of enzymes involved in the melanization pathway via phosphorylation and dephosphorylation.…”

Section: Discussionmentioning

confidence: 99%

Elevenin signaling modulates body color through the tyrosine‐mediated cuticle melanism pathway

Wang

et al. 2019

FASEB j.

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Elevenin is a newly discovered novel neuropeptide. Knockdown of either elevenin or orphan receptor NlA42 transcript expression by RNA interference caused severe cuticle melanization in the brown planthopper (BPH). Injection of a synthetic elevenin peptide not only rescued the body color phenotype in dselevenin‐pretreated individuals but also suppressed melanization of black insects grown in natural conditions. Real‐time quantitative PCR results revealed that elevenin expression levels were highest in the brain and salivary gland. Immunohistochemistry analysis confirmed that a precursor peptide of elevenin was generated in the salivary gland, suggesting that the salivary gland might be an important neurosecretory tissue in addition to the brain in BPH. Furthermore, double‐strand RNA–mediated silencing of elevenin and NlA42 resulted in down‐regulation of arylalkylamine‐N‐acetyltransferase and up‐regulation of tyrosine hydroxylase, whereas elevenin peptide injection resulted in up‐regulation of N‐β‐alanyldopamine synthase and aspartate 1‐decarboxylase, indicating a complex regulation network for cuticle pigmentation. In addition, functional characterization demonstrated that NlA42 is a cognate receptor for elevenin, and couples to Gq and Gs proteins, triggering both PLC/Ca2+/PKC and AC/cAMP/PKA signaling pathways in response to elevenin treatment. These findings suggest that the elevenin signaling functions control BPH body color through the tyrosine‐mediated cuticle melanism pathway.—Wang, S.‐L., Wang, W.‐W., Ma, Q., Shen, Z.‐F., Zhang, M.‐Q., Zhou, N.‐M., Zhang, C.‐X. Elevenin signaling modulates body color through the tyrosine‐mediated cuticle melanism pathway. FASEB J. 33, 9731–9741 (2019). http://www.fasebj.org

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Section: Discussionmentioning

confidence: 99%

Elevenin signaling modulates body color through the tyrosine‐mediated cuticle melanism pathway

Wang

et al. 2019

FASEB j.

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“…Further Blast search and subsequent phylogenetic analyses demonstrated that this gene indeed encodes SREBP‐1c. The time expression profiles demonstrated that the fluctuation of the HaSEBP‐1c mRNA level is similar with that of other genes involved in sex pheromone biosyntheses, such as PBAN receptor, fatty acid reductase, desaturase, and ACC in H. armigera (Du et al, ). The expression pattern of HaSREBP‐1c is also similar to the changes of sex pheromone component titre, indicating that this gene possibly has associated with sex pheromone biosynthesis.…”

Section: Discussionmentioning

confidence: 90%

“…The nucleotide sequence of HaSREBP‐1c was first obtained from PG transcriptome data of H. armigera (Du et al, ) and further verified by PCR. Sequence analysis demonstrated that the open reading frame of HaSREBP‐1c consists of 3201 bp nucleotides that encode 1066 amino acid residues (Figure ).…”

Section: Resultsmentioning

confidence: 99%

“…PBAN was also found to influence ACC activity in H. zea , Mamestra brassicae, Spodoptera exigua , and Argyrotaenia velutinana (Jacquin, Jurenka, Ljungberg, Nagnan, & Löfstedt, ; Jurenka, ; Tang et al, ). A recent study further provides an evidence that calcineurin activated by PBAN/G‐protein receptor/Ca 2+ signal, in turn, activates ACC via dephosphorylation, thus to influence sex pheromone biosynthesis in H. armigera (Du et al, ). All these results provide irrefutable evidence that ACC activated by the PBAN/G‐protein receptor/Ca 2+ /calcineurin pathway is a rate‐limiting enzyme in the sex pheromone biosynthesis step in these species.…”

Section: Discussionmentioning

confidence: 99%

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Molecular identification of sterol regulatory element‐binding protein‐1c from Helicoverpa armigera pheromone gland

Zhang

Yin

et al. 2018

Arch Insect Biochem Physiol

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Sterol regulatory element‐binding protein‐1c (SREBP‐1c) is a basic helix‐loop‐helix type transcription factor that regulates the fatty acid and cholesterol biosynthesis. Lepidoptera sex pheromone is a product of fatty acid biosynthesis followed by carbon chain modifications. However, the role of SREBP‐1c on sex pheromone biosynthesis remains elusive. In the present study, Helicoverpa armigera was used as a model to investigate the role of SREBP‐1c on sex pheromone biosynthesis (HaSREBP‐1c). Sequence analysis demonstrated that the open reading frame of HaSREBP‐1c consists of 3201 bp nucleotides that encode 1066 amino acid residues. Blast searches based on amino acid sequences demonstrated that HaSREBP‐1c shares higher amino acid identity with lepidopteran homologues. Development expression profiles demonstrated that HaSREBP‐1c transcript could be detected at 72 hr before adult emergence, then gradually increased, and finally reached its peak at 24 hr after adult emergence. The spatial expression pattern demonstrated that HaSREBP‐1c was ubiquitously expressed in all examined tissues. The decrease of HaSREBP‐1c messenger RNA (mRNA) levels as shown by RNA interference caused significant decreases in acetyl‐coA carboxylase (ACC) mRNA levels and subsequent sex pheromone production. Behavior analysis demonstrated that the decrease of HaSREBP‐1c mRNA level caused a significant decrease in the female’s ability to attract males. Altogether our results demonstrated that HaSREBP‐1c acts as a transcription factor to regulate ACC mRNA expression and, therefore, to influence female sex pheromone biosynthesis.

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“…Our present work also demonstrated that both the inhibitors and RNAi‐mediated knockdown of HaCNA caused a significant decrease in the male sex pheromone components in H. armigera male moths, consistent with the results in the female PGs of B. mori . Our previous data on H. armigera also demonstrated that CN was involved in female sex pheromone biosynthesis (Du et al ., ). Taken together, these results reveal that Ca 2+ /CN is a conserved signal in PBAN‐regulated sex pheromone biosynthesis in both sexes.…”

Section: Discussionmentioning

confidence: 97%

Calcineurin is required for male sex pheromone biosynthesis and female acceptance

Zhao

Zhang

et al. 2018

Insect Molecular Biology

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Lepidoptera sex pheromone biosynthesis is regulated by pheromone biosynthesis activating neuropeptide (PBAN). PBAN regulates not only female sex pheromone biosynthesis but also male sex pheromone biosynthesis. Previous research has confirmed that PBAN regulates sex pheromone biosynthesis using Ca as a secondary messenger in all examined species to date. However, the downstream signal of Ca has remained elusive. In the present study, calcineurin A (CNA), a downstream signal of Ca , was discovered in Helicoverpa armigera male hairpencil and named HaCNA. Sequence analysis demonstrated that the open reading frame of HaCNA contains 1488 nucleotides encoding 495 amino acid residues. A homology search revealed that HaCNA shares a high amino acid identity with the CNA of other insects. Developmental and spatial expression analyses revealed that the mRNA levels of HaCNA peaked at 24 h after emergence and that HaCNA expression was ubiquitous in all examined tissues. Activity analysis revealed that PBAN activates HaCNA, and a Ca inhibitor, Lacl , attenuated the effect of PBAN by decreasing HaCNA activity. Pharmacological inhibitor and RNA interference-mediated knockdown assays revealed that both activity inhibition and decreased mRNA levels of HaCNA led to a significant decrease in the production of the male sex pheromone components [octadecanol and (Z)-11 hexadecanol)] and in the efficacy of female mating acceptance. Our results demonstrate that HaCNA acts as downstream signal of PBAN/Ca and plays an important role in PBAN-induced male sex pheromone biosynthesis and female mating acceptance.

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Calcineurin-mediated Dephosphorylation of Acetyl-coA Carboxylase is Required for Pheromone Biosynthesis Activating Neuropeptide (PBAN)-induced Sex Pheromone Biosynthesis in Helicoverpa armigera

Cited by 36 publications

References 54 publications

Elevenin signaling modulates body color through the tyrosine‐mediated cuticle melanism pathway

Elevenin signaling modulates body color through the tyrosine‐mediated cuticle melanism pathway

Molecular identification of sterol regulatory element‐binding protein‐1c from Helicoverpa armigera pheromone gland

Calcineurin is required for male sex pheromone biosynthesis and female acceptance

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