Differential expression of ITP and ITPL indicate multiple functions in the silkworm Bombyx mori

Klöcklerová, Vanda; Gáliková, Zuzana; Roller, Ladislav; Žitňan, Dušan

doi:10.1007/s00441-023-03752-y

Cited by 10 publications

(5 citation statements)

References 42 publications

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“…In the silkworm Bombyx mori and the red flour beetle Tribolium castaneum, ITP gene products are also expressed outside the nervous system (Begum et al ., 2009, Klocklerova et al ., 2023). This peripheral source of ITP isoforms in Bombyx and Tribolium includes the gut enteroendocrine cells.…”

Section: Resultsmentioning

confidence: 99%

“…ITPa is produced by a small set of interneurons and neurosecretory cells in the Drosophila brain and ventral nerve cord (Dircksen et al ., 2008). While the expression of the ITPL peptides has not yet been investigated in Drosophila , studies in other insects indicate partial overlap with ITPa expressing neurons (Drexler et al ., 2007, Klocklerova et al ., 2023). In order to delineate the targets of ITPa and ITPL and determine their modes of action, it is first necessary to identify, functionally characterize and localize the distribution of their cognate receptors.…”

Section: Introductionmentioning

confidence: 99%

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Anti-diuretic hormone ITP signals via a guanylate cyclase receptor to modulate systemic homeostasis inDrosophila

Gera,

Agard,

Nave

et al. 2024

Preprint

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Insects have evolved a variety of neurohormones that enable them to maintain their nutrient and osmotic homeostasis. While the identities and functions of various insect metabolic and diuretic hormones have been well-established, the characterization of an anti-diuretic signaling system that is conserved across most insects is still lacking. To address this, here we characterized the ion transport peptide (ITP) signaling system inDrosophila. TheDrosophila ITPgene encodes five transcript variants which generate three different peptide isoforms: ITP amidated (ITPa) and two ITP-like (ITPL1 and ITPL2) isoforms. Using a combination of anatomical mapping and single-cell transcriptome analyses, we comprehensively characterized the expression of all three ITP isoforms in the nervous system and peripheral tissues. Our analyses reveal widespread expression of ITP isoforms. Moreover, we show that ITPa is released during dehydration and recombinantDrosophilaITPa inhibits diuretic peptide-induced renal tubule secretionex vivo, thus confirming its role as an anti-diuretic hormone. Using a phylogenetic-driven approach and theex vivosecretion assay, we identified and functionally characterized Gyc76C, a membrane guanylate cyclase, as an elusiveDrosophilaITPa receptor. Thus, knockdown of Gyc76C in renal tubules abolishes the inhibitory effect of ITPa on diuretic hormone secretion. Extensive anatomical mapping of Gyc76C reveals that it is highly expressed in larval and adult tissues associated with osmoregulation (renal tubules and rectum) and metabolic homeostasis (fat body). Consistent with this expression, knockdown of Gyc76C in renal tubules impacts tolerance to osmotic and ionic stresses, whereas knockdown specifically in the fat body impacts feeding, nutrient homeostasis and associated behaviors. We also complement receptor knockdown experiments with ITPa overexpression in ITP neurons. Interestingly, ITPa-Gyc76C pathways deciphered here are reminiscent of the atrial natriuretic peptide signaling in mammals. Lastly, we utilized connectomics and single-cell transcriptomics to identify synaptic and paracrine pathways upstream and downstream of ITP-expressing neurons. Taken together, our systematic characterization of the ITP signaling establishes a tractable system to decipher how a small set of neurons integrates diverse inputs to orchestrate systemic homeostasis inDrosophila.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Anti-diuretic hormone ITP signals via a guanylate cyclase receptor to modulate systemic homeostasis inDrosophila

Gera,

Agard,

Nave

et al. 2024

Preprint

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“…Indeed ITP and ITP-L are multifunctional neuropeptides involved in metabolism, regulation of water and ion homeostasis, cuticle expansion and melanization, and reproduction (Begum et al, 2009; Dircksen, 2009; Gáliková et al, 2018; Yu et al, 2016). The role in reproduction has been supported by ITPL expression in the B. mori male reproductive system with innervations of the accessory glands, the seminal vesicles, and the ejaculatory ducts (Klöcklerova, et al, 2023), all organs critical for successful mating and reproduction. ITPL expression has also been found in the seminal fluid of the brown plant hopper, Nilaparvata lugens (Yu et al, 2016), which is transferred to females during mating.…”

Section: Discussionmentioning

confidence: 99%

Molecular characterization, localization, and physiological roles of ITP and ITP-L in the mosquito,Aedes aegypti

Sajadi,

Paluzzi

2024

Preprint

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The insect ion transport peptide (ITP) and its alternatively spliced variant, ITP-like peptide (ITP-L), belong to the crustacean hyperglycemic hormone family of peptides and are widely conserved among insect species. While limited, studies have characterized the ITP/ITP-L signaling system within insects, and putative functions including regulation of ion and fluid transport, ovarian maturation, and thirst/excretion have been proposed. Herein, we aimed to molecularly investigate Itp and Itp-l expression profiles in the mosquito Aedes aegypti, examine peptide immunolocalization and distribution within the adult central nervous system, and elucidate physiological roles for these neuropeptides. Transcript expression profiles of both AedaeItp and AedaeItp-l revealed distinct enrichment patterns in adults, with AedaeItp expressed in the brain and AedaeItp-l expression predominantly within the abdominal ganglia. Immunohistochemical analysis within the central nervous system revealed expression of AedaeITP peptide in a number of cells in the brain and in the terminal ganglion. Comparatively, AedaeITP-L peptide was localized solely within the pre-terminal abdominal ganglia of the central nervous system. Interestingly, prolonged desiccation stress caused upregulation of AedaeItp and AedaeItp-l levels in adult mosquitoes, suggesting possible functional roles in water conservation and feeding-related activities. RNAi-mediated knockdown of AedaeItp caused an increase in urine excretion, while knockdown of both AedaeItp and AedaeItp-l reduced blood feeding and egg-laying in females as well as hindered egg viability, suggesting roles in reproductive physiology and behaviour. Altogether, this study identifies AedaeITP and AedaeITP-L as key pleiotropic hormones, regulating various critical physiological processes in the disease vector, A. aegypti.

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“…Indeed ITP and ITP-L are multifunctional neuropeptides involved in metabolism, regulation of water and ion homeostasis, cuticle expansion and melanization, and reproduction ( 13 , 15 , 20 , 23 ). The role in reproduction has been supported by ITPL expression in the B. mori male reproductive system with innervations of the accessory glands, the seminal vesicles, and the ejaculatory ducts ( 62 ), all organs critical for successful mating and reproduction. ITPL expression has also been found in the seminal fluid of the brown plant hopper, Nilaparvata lugens ( 23 ), which is transferred to females during mating.…”

Section: Discussionmentioning

confidence: 99%

Molecular characterization, localization, and physiological roles of ITP and ITP-L in the mosquito, Aedes aegypti

Sajadi,

Paluzzi

2024

Front. Insect Sci.

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The insect ion transport peptide (ITP) and its alternatively spliced variant, ITP-like peptide (ITP-L), belong to the crustacean hyperglycemic hormone family of peptides and are widely conserved among insect species. While limited, studies have characterized the ITP/ITP-L signaling system within insects, and putative functions including regulation of ion and fluid transport, ovarian maturation, and thirst/excretion have been proposed. Herein, we aimed to molecularly investigate Itp and Itp-l expression profiles in the mosquito, Aedes aegypti, examine peptide immunolocalization and distribution within the adult central nervous system, and elucidate physiological roles for these neuropeptides. Transcript expression profiles of both AedaeItp and AedaeItp-l revealed distinct enrichment patterns in adults, with AedaeItp expressed in the brain and AedaeItp-l expression predominantly within the abdominal ganglia. Immunohistochemical analysis within the central nervous system revealed expression of AedaeITP peptide in a number of cells in the brain and in the terminal ganglion. Comparatively, AedaeITP-L peptide was localized solely within the pre-terminal abdominal ganglia of the central nervous system. Interestingly, prolonged desiccation stress caused upregulation of AedaeItp and AedaeItp-l levels in adult mosquitoes, suggesting possible functional roles in water conservation and feeding-related activities. RNAi-mediated knockdown of AedaeItp caused an increase in urine excretion, while knockdown of both AedaeItp and AedaeItp-l reduced blood feeding and egg-laying in females as well as hindered egg viability, suggesting roles in reproductive physiology and behavior. Altogether, this study identifies AedaeITP and AedaeITP-L as key pleiotropic hormones, regulating various critical physiological processes in the disease vector, A. aegypti.

show abstract

Differential expression of ITP and ITPL indicate multiple functions in the silkworm Bombyx mori

Cited by 10 publications

References 42 publications

Anti-diuretic hormone ITP signals via a guanylate cyclase receptor to modulate systemic homeostasis inDrosophila

Anti-diuretic hormone ITP signals via a guanylate cyclase receptor to modulate systemic homeostasis inDrosophila

Molecular characterization, localization, and physiological roles of ITP and ITP-L in the mosquito,Aedes aegypti

Molecular characterization, localization, and physiological roles of ITP and ITP-L in the mosquito, Aedes aegypti

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