A comprehensive transcriptomic view of renal function in the malaria vector, Anopheles gambiae

Gayle Overend; Pablo Cabrero; Kenneth Agerlin Halberg; Lisa C. Ranford-Cartwright; Debra J. Woods; Shireen A. Davies; Julian A.T. Dow

doi:10.1016/j.ibmb.2015.05.007

A comprehensive transcriptomic view of renal function in the malaria vector, Anopheles gambiae

Gayle Overend, Pablo Cabrero, Kenneth Agerlin Halberg, Lisa C. Ranford-Cartwright, Debra J. Woods, Shireen A. Davies, Julian A.T. Dow

Molecular Integrative Physiology

21 Citationer (Scopus)

Abstract

Renal function is essential to maintain homeostasis. This is particularly significant for insects that undergo complete metamorphosis; larval mosquitoes must survive a freshwater habitat whereas adults are terrestrial, and mature females must maintain ion and fluid homeostasis after blood feeding. To investigate the physiological adaptations required for successful development to adulthood, we studied the Malpighian tubule transcriptome of Anopheles gambiae using Affymetrix arrays. We assessed transcription under several conditions; as third instar larvae, as adult males fed on sugar, as adult females fed on sugar, and adult females after a blood meal. In addition to providing the most detailed transcriptomic data to date on the Anopheles Malpighian tubules, the data provide unique information on the renal adaptations required for the switch from freshwater to terrestrial habitats, on gender differences, and on the contrast between nectar-feeding and haematophagy. We found clear differences associated with ontogenetic change in lifestyle, gender and diet, particularly in the neuropeptide receptors that control fluid secretion, and the water and ion transporters that impact volume and composition. These data were also combined with transcriptomics from the Drosophila melanogaster tubule, allowing meta-analysis of the genes which underpin tubule function across Diptera. To further investigate renal conservation across species we selected four D. melanogaster genes with orthologues highly enriched in the Anopheles tubules, and generated RNAi knockdown flies. Three of these genes proved essential, showing conservation of critical functions across 150 million years of phylogenetic separation. This extensive data-set is available as an online resource, MozTubules.org, and could potentially be mined for novel insecticide targets that can impact this critical organ in this pest species.

Originalsprog	Engelsk
Tidsskrift	Insect Biochemistry and Molecular Biology
Vol/bind	67
Sider (fra-til)	47-58
Antal sider	12
ISSN	0965-1748
DOI	https://doi.org/10.1016/j.ibmb.2015.05.007
Status	Udgivet - 2015

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10.1016/j.ibmb.2015.05.007

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title = "A comprehensive transcriptomic view of renal function in the malaria vector, Anopheles gambiae",

abstract = "Renal function is essential to maintain homeostasis. This is particularly significant for insects that undergo complete metamorphosis; larval mosquitoes must survive a freshwater habitat whereas adults are terrestrial, and mature females must maintain ion and fluid homeostasis after blood feeding. To investigate the physiological adaptations required for successful development to adulthood, we studied the Malpighian tubule transcriptome of Anopheles gambiae using Affymetrix arrays. We assessed transcription under several conditions; as third instar larvae, as adult males fed on sugar, as adult females fed on sugar, and adult females after a blood meal. In addition to providing the most detailed transcriptomic data to date on the Anopheles Malpighian tubules, the data provide unique information on the renal adaptations required for the switch from freshwater to terrestrial habitats, on gender differences, and on the contrast between nectar-feeding and haematophagy. We found clear differences associated with ontogenetic change in lifestyle, gender and diet, particularly in the neuropeptide receptors that control fluid secretion, and the water and ion transporters that impact volume and composition. These data were also combined with transcriptomics from the Drosophila melanogaster tubule, allowing meta-analysis of the genes which underpin tubule function across Diptera. To further investigate renal conservation across species we selected four D. melanogaster genes with orthologues highly enriched in the Anopheles tubules, and generated RNAi knockdown flies. Three of these genes proved essential, showing conservation of critical functions across 150 million years of phylogenetic separation. This extensive data-set is available as an online resource, MozTubules.org, and could potentially be mined for novel insecticide targets that can impact this critical organ in this pest species.",

keywords = "Anopheles gambiae, Drosophila melanogaster, Haematophagy, Malpighian tubules, Transcriptomics",

author = "Gayle Overend and Pablo Cabrero and Halberg, {Kenneth Agerlin} and Ranford-Cartwright, {Lisa C.} and Woods, {Debra J.} and Davies, {Shireen A.} and Dow, {Julian A.T.}",

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language = "English",

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T1 - A comprehensive transcriptomic view of renal function in the malaria vector, Anopheles gambiae

AU - Overend, Gayle

AU - Cabrero, Pablo

AU - Halberg, Kenneth Agerlin

AU - Ranford-Cartwright, Lisa C.

AU - Woods, Debra J.

AU - Davies, Shireen A.

AU - Dow, Julian A.T.

PY - 2015

Y1 - 2015

N2 - Renal function is essential to maintain homeostasis. This is particularly significant for insects that undergo complete metamorphosis; larval mosquitoes must survive a freshwater habitat whereas adults are terrestrial, and mature females must maintain ion and fluid homeostasis after blood feeding. To investigate the physiological adaptations required for successful development to adulthood, we studied the Malpighian tubule transcriptome of Anopheles gambiae using Affymetrix arrays. We assessed transcription under several conditions; as third instar larvae, as adult males fed on sugar, as adult females fed on sugar, and adult females after a blood meal. In addition to providing the most detailed transcriptomic data to date on the Anopheles Malpighian tubules, the data provide unique information on the renal adaptations required for the switch from freshwater to terrestrial habitats, on gender differences, and on the contrast between nectar-feeding and haematophagy. We found clear differences associated with ontogenetic change in lifestyle, gender and diet, particularly in the neuropeptide receptors that control fluid secretion, and the water and ion transporters that impact volume and composition. These data were also combined with transcriptomics from the Drosophila melanogaster tubule, allowing meta-analysis of the genes which underpin tubule function across Diptera. To further investigate renal conservation across species we selected four D. melanogaster genes with orthologues highly enriched in the Anopheles tubules, and generated RNAi knockdown flies. Three of these genes proved essential, showing conservation of critical functions across 150 million years of phylogenetic separation. This extensive data-set is available as an online resource, MozTubules.org, and could potentially be mined for novel insecticide targets that can impact this critical organ in this pest species.

AB - Renal function is essential to maintain homeostasis. This is particularly significant for insects that undergo complete metamorphosis; larval mosquitoes must survive a freshwater habitat whereas adults are terrestrial, and mature females must maintain ion and fluid homeostasis after blood feeding. To investigate the physiological adaptations required for successful development to adulthood, we studied the Malpighian tubule transcriptome of Anopheles gambiae using Affymetrix arrays. We assessed transcription under several conditions; as third instar larvae, as adult males fed on sugar, as adult females fed on sugar, and adult females after a blood meal. In addition to providing the most detailed transcriptomic data to date on the Anopheles Malpighian tubules, the data provide unique information on the renal adaptations required for the switch from freshwater to terrestrial habitats, on gender differences, and on the contrast between nectar-feeding and haematophagy. We found clear differences associated with ontogenetic change in lifestyle, gender and diet, particularly in the neuropeptide receptors that control fluid secretion, and the water and ion transporters that impact volume and composition. These data were also combined with transcriptomics from the Drosophila melanogaster tubule, allowing meta-analysis of the genes which underpin tubule function across Diptera. To further investigate renal conservation across species we selected four D. melanogaster genes with orthologues highly enriched in the Anopheles tubules, and generated RNAi knockdown flies. Three of these genes proved essential, showing conservation of critical functions across 150 million years of phylogenetic separation. This extensive data-set is available as an online resource, MozTubules.org, and could potentially be mined for novel insecticide targets that can impact this critical organ in this pest species.

KW - Anopheles gambiae

KW - Drosophila melanogaster

KW - Haematophagy

KW - Malpighian tubules

KW - Transcriptomics

U2 - 10.1016/j.ibmb.2015.05.007

DO - 10.1016/j.ibmb.2015.05.007

M3 - Journal article

AN - SCOPUS:84949623575

SN - 0965-1748

VL - 67

SP - 47

EP - 58

JO - Insect Biochemistry and Molecular Biology

JF - Insect Biochemistry and Molecular Biology

ER -

A comprehensive transcriptomic view of renal function in the malaria vector, Anopheles gambiae

Abstract

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