What the loss of the hormone neuroparsin in the melanogaster subgroup of Drosophila can tell us about its function

Veenstra, Jan A.

doi:10.1016/j.ibmb.2010.03.001

Cited by 43 publications

(35 citation statements)

References 46 publications

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“…An exception is the genus Drosophila, where Drosophila mojavensis and most other species have a recognizable neuroparsin gene and Drosophila melanogaster and four other closely related species do not (16). This suggests that neuroparsins have been lost from the melanogaster subgroup (16), which we reasoned might also be coupled with loss of a neuroparsin receptor.…”

Section: Resultsmentioning

confidence: 95%

“…A shrimp neuroparsin was recently shown to be provitellogenic (35), which is similar to the activity of OEH. In contrast, studies from locusts suggest neuroparsins have multiple functions (16,17), whereas the loss of neuroparsins from the melanogaster subgroup argues these factors may be dispensable due potentially to overlap with ILP function (16).…”

Section: Oeh Binds To Aael001915 and Activates Phosphosphorylation Ofmentioning

confidence: 90%

“…The comparative literature thereafter showed that OEH is a neuroparsin (15,16), whereas experimental data showed that OEH and ILPs exhibit partially overlapping activity in regulating egg formation in mosquitoes (8,9). Because OEH and ILP3 both activate downstream components of the insulin signaling cascade, we originally speculated that OEH functions by interacting with ILPs and/or the IR.…”

Section: Oeh Binds To Aael001915 and Activates Phosphosphorylation Ofmentioning

confidence: 99%

“…That OEH binding to AAEL001915 in S2 cells stimulates phosphorylation of Akt as occurs in the mosquito ovary is notable given the absence of endogenous OEH or AAEL001915 orthologs in D. melanogaster. On the other hand, this loss is also a relatively recent evolutionary event given the presence of neuroparsin and AAEL001915 orthologs in other drosophilids (13,16). Thus, downstream components of the insulin signaling cascade, such as the IR substrate Chico, appear to be sufficiently conserved in D. melanogaster to interact with AAEL001915, whose intracellular tyrosine kinase domain structurally shares features with the IR (13, 23).…”

Section: Oeh Binds To Aael001915 and Activates Phosphosphorylation Ofmentioning

confidence: 99%

“…Studies in A. aegypti also establish that ILP3 activity depends upon binding to the insulin receptor (IR), a receptor tyrosine kinase (RTK), which triggers phosphorylation of downstream components in the insulin signaling pathway including Akt (4,9,14). OEH in contrast belongs to a poorly characterized family of neuropeptides known only from arthropods called neuroparsins (13,15,16). Limited sequence similarity with vertebrate insulin growth factor binding proteins initially suggested that neuroparsins function as ILP binding proteins, which could affect ILP binding to the IR and downstream signaling (15,17).…”

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confidence: 99%

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Ovary ecdysteroidogenic hormone requires a receptor tyrosine kinase to activate egg formation in the mosquito Aedes aegypti

Vogel

Brown

Strand

2015

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

121

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Mosquitoes are major disease vectors because most species must feed on blood from a vertebrate host to produce eggs. Blood feeding by the vector mosquito Aedes aegypti triggers the release of two neurohormones, ovary ecdysteroidogenic hormone (OEH) and insulin-like peptides (ILPs), which activate multiple processes required for egg formation. ILPs function by binding to the insulin receptor, which activates downstream components in the canonical insulin signaling pathway. OEH in contrast belongs to a neuropeptide family called neuroparsins, whose receptor is unknown. Here we demonstrate that a previously orphanized receptor tyrosine kinase (RTK) from A. aegypti encoded by the gene AAEL001915 is an OEH receptor. Phylogenetic studies indicated that the protein encoded by this gene, designated AAEL001915, belongs to a clade of RTKs related to the insulin receptor, which are distinguished by an extracellular Venus flytrap module. Knockdown of AAEL001915 by RNAi disabled OEH-mediated egg formation in A. aegypti. AAEL001915 was primarily detected in the mosquito ovary in association with follicular epithelial cells. Both monomeric and dimeric AAEL001915 were detected in mosquito ovaries and transfected Drosophila S2 cells. Functional assays further indicated that OEH bound to dimeric AAEL001915, which resulted in downstream phosphorylation of Ak strain transforming factor (Akt). We hypothesize that orthologs of AAEL001915 in other insects are neuroparsin receptors.insect | vector | reproduction | mosquito | oogenesis

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Section: Resultsmentioning

confidence: 95%

Section: Oeh Binds To Aael001915 and Activates Phosphosphorylation Ofmentioning

confidence: 90%

Section: Oeh Binds To Aael001915 and Activates Phosphosphorylation Ofmentioning

confidence: 99%

Section: Oeh Binds To Aael001915 and Activates Phosphosphorylation Ofmentioning

confidence: 99%

mentioning

confidence: 99%

See 3 more Smart Citations

Ovary ecdysteroidogenic hormone requires a receptor tyrosine kinase to activate egg formation in the mosquito Aedes aegypti

Vogel

Brown

Strand

2015

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

121

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Insulin/IGF signaling in Drosophila and other insects: factors that regulate production, release and post-release action of the insulin-like peptides

Nässel

Broeck

2015

Cell. Mol. Life Sci.

284

305

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Insulin, insulin-like growth factors (IGFs) and insulin-like peptides (ILPs) are important regulators of metabolism, growth, reproduction and lifespan, and mechanisms of insulin/IGF signaling (IIS) have been well conserved over evolution. In insects, between one and 38 ILPs have been identified in each species. Relatively few insect species have been investigated in depth with respect to ILP functions, and therefore we focus mainly on the well-studied fruitfly Drosophila melanogaster. In Drosophila eight ILPs (DILP1-8), but only two receptors (dInR and Lgr3) are known. DILP2, 3 and 5 are produced by a set of neurosecretory cells (IPCs) in the brain and their biosynthesis and release are controlled by a number of mechanisms differing between larvae and adults. Adult IPCs display cell-autonomous sensing of circulating glucose, coupled to evolutionarily conserved mechanisms for DILP release. The glucose-mediated DILP secretion is modulated by neurotransmitters and neuropeptides, as well as by factors released from the intestine and adipocytes. Larval IPCs, however, are indirectly regulated by glucose-sensing endocrine cells producing adipokinetic hormone, or by circulating factors from the intestine and fat body. Furthermore, IIS is situated within a complex physiological regulatory network that also encompasses the lipophilic hormones, 20-hydroxyecdysone and juvenile hormone. After release from IPCs, the ILP action can be modulated by circulating proteins that act either as protective carriers (binding proteins), or competitive inhibitors. Some of these proteins appear to have additional functions that are independent of ILPs. Taken together, the signaling with multiple ILPs is under complex control, ensuring tightly regulated IIS in the organism.

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Hormonal axes in Drosophila: regulation of hormone release and multiplicity of actions

Nässel

Zandawala

2020

Cell Tissue Res

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Hormones regulate development, as well as many vital processes in the daily life of an animal. Many of these hormones are peptides that act at a higher hierarchical level in the animal with roles as organizers that globally orchestrate metabolism, physiology and behavior. Peptide hormones can act on multiple peripheral targets and simultaneously convey basal states, such as metabolic status and sleep-awake or arousal across many central neuronal circuits. Thereby, they coordinate responses to changing internal and external environments. The activity of neurosecretory cells is controlled either by (1) cell autonomous sensors, or (2) by other neurons that relay signals from sensors in peripheral tissues and (3) by feedback from target cells. Thus, a hormonal signaling axis commonly comprises several components. In mammals and other vertebrates, several hormonal axes are known, such as the hypothalamic-pituitary-gonad axis or the hypothalamic-pituitary-thyroid axis that regulate reproduction and metabolism, respectively. It has been proposed that the basic organization of such hormonal axes is evolutionarily old and that cellular homologs of the hypothalamic-pituitary system can be found for instance in insects. To obtain an appreciation of the similarities between insect and vertebrate neurosecretory axes, we review the organization of neurosecretory cell systems in Drosophila. Our review outlines the major peptidergic hormonal pathways known in Drosophila and presents a set of schemes of hormonal axes and orchestrating peptidergic systems. The detailed organization of the larval and adult Drosophila neurosecretory systems displays only very basic similarities to those in other arthropods and vertebrates.

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What the loss of the hormone neuroparsin in the melanogaster subgroup of Drosophila can tell us about its function

Cited by 43 publications

References 46 publications

Ovary ecdysteroidogenic hormone requires a receptor tyrosine kinase to activate egg formation in the mosquito Aedes aegypti

Ovary ecdysteroidogenic hormone requires a receptor tyrosine kinase to activate egg formation in the mosquito Aedes aegypti

Insulin/IGF signaling in Drosophila and other insects: factors that regulate production, release and post-release action of the insulin-like peptides

Hormonal axes in Drosophila: regulation of hormone release and multiplicity of actions

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