E93 confers steroid hormone responsiveness of digestive enzymes to promote blood meal digestion in the midgut of the mosquito Aedes aegypti

He, Ya-Zhou; Ding, Yike; Wang, Xueli; Zou, Zhen; Raikhel, Alexander S.

doi:10.1016/j.ibmb.2021.103580

Cited by 8 publications

(9 citation statements)

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“…Within hours of blood feeding, translation of this pool of transcripts is initiated and peptidase activity begins to increase ( Felix et al, 1991 ). Next, rising ecdysone titers drive the transcription of a “late” cohort of peptidases, which complete the digestive process ( He et al, 2021 ). Finally, early peptidases are transcribed anew ( Bian et al, 2008 ; Noriega et al, 1996 ) amid a postprandial surge of JH ( Hernández-Martínez et al, 2015 ; Lucas et al, 2015 ; Shapiro et al, 1986 ; Zhao et al, 2016 ), restoring the gut to a state of readiness for its next blood meal.…”

Section: Discussionmentioning

confidence: 99%

“…In the first phase, mRNAs encoding a cohort of ‘early’ serine endopeptidases, transcribed in response to juvenile hormone (JH) secretion during previtellogenic maturation, are translated ( Bian et al, 2008 ; Felix et al, 1991 ; Jiang et al, 1997 ; Noriega et al, 1996 ; Noriega et al, 1997 ; Noriega et al, 2001 ). In the second, ecdysone signaling mediates the transcription of a ‘late’ cohort of endo and exopeptidases, with the transcripts of key peptidases and overall proteolytic activity typically peaking around 24 hr post blood meal (pbm) ( Barillas-Mury et al, 1991 ; Brackney et al, 2010 ; Gooding, 1966 ; Graf and Briegel, 1982 ; Graf et al, 1998 ; He et al, 2021 ; Isoe et al, 2009b ; Noriega et al, 2002 ). The transcriptional timeline is, however, more complex than a simple early translation/late transcription paradigm might suggest.…”

Section: Introductionmentioning

confidence: 99%

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A transcriptomic atlas of Aedes aegypti reveals detailed functional organization of major body parts and gut regional specializations in sugar-fed and blood-fed adult females

Hixson

Bing

Yang

et al. 2022

eLife

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Mosquito vectors transmit numerous pathogens, but large gaps remain in our understanding of their physiology. To facilitate future explorations of mosquito biology, with specific attention to the major vector Aedes aegypti, we have created Aegypti-Atlas (http://aegyptiatlas.buchonlab.com/), an online resource hosting RNAseq profiles of Ae. aegypti body parts (head, thorax, abdomen, gut, Malpighian tubules, and ovaries), gut regions (crop, proventriculus, anterior and posterior midgut, and hindgut), and a time course of blood meal digestion in the gut. Using Aegypti-Atlas, we provide new insights into the regionalization of gut function, blood feeding response, and immune defenses. We find that the anterior and posterior regions of the mosquito midgut possess clearly delineated digestive specializations which are preserved in the blood-fed state. Blood feeding initiates the sequential transcriptional induction and repression/depletion of multiple cohorts of peptidases throughout blood meal digestion. With respect to defense, immune signaling components, but not recognition or effector molecules, show enrichment in ovaries. Basal expression of antimicrobial peptides is dominated by two genes, holotricin and gambicin, that are expressed in the carcass and the digestive tissues, respectively, in a near mutually exclusive manner. In the midgut, gambicin and other immune effector genes are almost exclusively expressed in the anterior regions, while the posterior midgut exhibits the hallmarks of immune tolerance. Finally, in a cross-species comparison between the midguts of Ae. aegypti and Anopheles gambiae (s.l.), we observe that regional digestive and immune specializations are closely conserved, indicating that our data may yield inferences that are broadly relevant to multiple mosquito vector species. We further demonstrate that the expression of orthologous genes is highly correlated, with the exception of a ‘species signature’ comprising a small number of highly/disparately expressed genes. With this work, we show the potential of Aegypti-Atlas to unlock a more complete understanding of mosquito biology.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

A transcriptomic atlas of Aedes aegypti reveals detailed functional organization of major body parts and gut regional specializations in sugar-fed and blood-fed adult females

Hixson

Bing

Yang

et al. 2022

eLife

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show abstract

“…Within hours of blood feeding, translation of this pool of transcripts is initiated and peptidase activity begins to increase [37]. Next, rising ecdysone titers drive the transcription of a "late" cohort of peptidases, which complete the digestive process [48]. Finally, early peptidases are transcribed anew [38,40] amid a postprandial surge of JH [73][74][75][76], restoring the gut to a state of readiness for its next blood meal.…”

Section: Gut Peptidases Are Dynamically Up and Downregulated In Sequential Transcriptional Waves Upon Blood Feedingmentioning

confidence: 99%

“…Peptidase activity peaks somewhere between 18 and 36 hours pbm [43,44,47], as do transcripts for some of the highest expressed "late" phase peptidases [49,50,52]. However, a few publications have documented peptidases peaking at earlier timepoints [51][52][53], and that at least one of these (SPI) is directly responsive to/dependent on ecdysone signaling [48]. Here, our genome-wide multi-timepoint series has demonstrated that these early-peaking genes are not isolated and exceptional but are, rather, members of large transcriptional cohorts.…”

Section: Gut Peptidases Are Dynamically Up and Downregulated In Sequential Transcriptional Waves Upon Blood Feedingmentioning

confidence: 99%

“…In the first phase mRNAs encoding a cohort of "early" serine endopeptidases, transcribed in response to juvenile hormone (JH) secretion during previtellogenic maturation, are translated [37][38][39][40][41][42]. In the second, ecdysone signaling mediates the transcription of a "late" cohort of endo and exopeptidases, with the transcripts of key peptidases and overall proteolytic activity typically peaking around 24 hrs post blood meal (pbm) [43][44][45][46][47][48][49][50]. The transcriptional timeline is, however, more complex than a simple early translation/late transcription paradigm might suggest.…”

Section: Introductionmentioning

confidence: 99%

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A transcriptomic atlas ofAedes aegyptireveals detailed functional organization of major body parts and gut regional specializations in sugar-fed and blood-fed adult females

Hixson

Bing

Yang

et al. 2021

Preprint

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Mosquito vectors transmit numerous pathogens, but large gaps remain in our understanding of their physiology. To facilitate future explorations of mosquito biology, with specific attention to the major vector Aedes aegypti, we have created Aegypti-Atlas (http://aegyptiatlas.buchonlab.com/), an online resource hosting RNAseq profiles of Ae. aegypti body parts (head, thorax, abdomen, gut, Malpighian tubules, and ovaries), gut regions (crop, proventriculus, anterior and posterior midgut, and hindgut), and a time course of blood meal digestion in the gut. Using Aegypti-Atlas, we provide new insights into the regionalization of gut function, blood feeding response, and immune defenses. We find that the anterior and posterior regions of the mosquito midgut possess clearly delineated digestive specializations which are preserved in the blood-fed state. Blood feeding initiates the sequential transcriptional induction and repression/depletion of multiple cohorts of peptidases throughout blood meal digestion. With respect to defense, immune signaling components, but not recognition or effector molecules, show enrichment in ovaries. Basal expression of antimicrobial peptides is dominated by two genes, holotricin and gambicin, that are expressed in the carcass and the digestive tissues, respectively, in a near mutually exclusive manner. In the midgut, gambicin and other immune effector genes are almost exclusively expressed in the anterior regions, while the posterior midgut exhibits the hallmarks of immune tolerance. Finally, in a cross-species comparison between the midguts of Ae. aegypti and Anopheles gambiae, we observe that regional digestive and immune specializations are closely conserved, indicating that our data may yield inferences that are broadly relevant to multiple mosquito vector species. We further demonstrate that the expression of orthologous genes is highly correlated, with the exception of a ‘species signature’ comprising a small number of highly/disparately expressed genes. With this work, we show the potential of Aegypti-Atlas to unlock a more complete understanding of mosquito biology.

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Insulin-like peptides and ovary ecdysteroidogenic hormone differentially stimulate physiological processes regulating egg formation in the mosquito Aedes aegypti

Chen,

Dou,

Eum

et al. 2023

Insect Biochemistry and Molecular Biology

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E93 confers steroid hormone responsiveness of digestive enzymes to promote blood meal digestion in the midgut of the mosquito Aedes aegypti

Cited by 8 publications

References 50 publications

A transcriptomic atlas of Aedes aegypti reveals detailed functional organization of major body parts and gut regional specializations in sugar-fed and blood-fed adult females

A transcriptomic atlas of Aedes aegypti reveals detailed functional organization of major body parts and gut regional specializations in sugar-fed and blood-fed adult females

A transcriptomic atlas ofAedes aegyptireveals detailed functional organization of major body parts and gut regional specializations in sugar-fed and blood-fed adult females

Insulin-like peptides and ovary ecdysteroidogenic hormone differentially stimulate physiological processes regulating egg formation in the mosquito Aedes aegypti

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