Role of an aquaporin in the sheep tick Ixodes ricinus

assessment as a potential control target

Ewan M. Campbell, Marion Burdin, Stefan Hoppler, Alan S. Bowman (Corresponding Author)

Research output: Contribution to journalArticle

30 Citations (Scopus)

Abstract

Ticks undergo tremendous osmoregulatory stress as they take on up to 100 times their body weight in blood, returning about 75% of the ingested water and ions via their saliva into the host. We postulated that water channels, or aquaporins, involved in this mass water transport might be good targets for acaricide development. An aquaporin (IrAQP1) identified in the sheep tick, Ixodes ricinus, was present only in tissues involved in mass water flux, namely the gut, rectal sac and especially abundant in the salivary glands. IrAQP1 was localised by in situ hybridisation in specific cell and acini types, possibly Type III acini, but absent from the type I acini that are responsible for rehydration of ticks in the non-feeding phase. Gene knockdown of IrAQP1 in isolated salivary glands completely inhibited dopamine-stimulated secretion. Further, IrAQP1 knockdown adult females had 50% reduced body weight gains over the first 5 days feeding on an artificial feeding apparatus and 21% at the point of engorgement on hosts. Haemolymph osmolarity was increased in the IrAQP1-knockdown ticks. Importantly, the blood volume ingested per body weight was reduced by 30%. Overall, it would appear that water passage from the gut to the saliva was disrupted and tick guts were simply too "full" to ingest more blood. However, double-stranded RNA interference of IrAQP1 did not affect mortality of the ticks which successfully fed to detachment at day 9. Overall, our data indicate that IrAQP1 plays a pivotal role in blood meal water handling through the gut and salivary gland, and although its disruption by double-stranded RNA interference dramatically affects feeding performance, ticks remained feeding on the host with subsequent potential pathogen transmission and, therefore, IrAQP1 is not a suitable candidate target for tick control.

Original languageEnglish
Pages (from-to)15-23
Number of pages9
JournalInternational Journal for Parasitology
Volume40
Issue number1
Early online date25 Jul 2009
DOIs
Publication statusPublished - Jan 2010

Keywords

  • tick
  • aquaporin
  • osmoregulation
  • salivary gland
  • RNA-interference
  • knockdown
  • ixodes ricinus
  • in situ hybridisation
  • amblyomma-americanum
  • salivary-glands
  • rhipicephalus-sanguineus
  • protein secretion
  • water-balance
  • hard ticks
  • dog tick
  • ixodidae
  • acari
  • synaptobrevin

Cite this

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title = "Role of an aquaporin in the sheep tick Ixodes ricinus: assessment as a potential control target",
abstract = "Ticks undergo tremendous osmoregulatory stress as they take on up to 100 times their body weight in blood, returning about 75{\%} of the ingested water and ions via their saliva into the host. We postulated that water channels, or aquaporins, involved in this mass water transport might be good targets for acaricide development. An aquaporin (IrAQP1) identified in the sheep tick, Ixodes ricinus, was present only in tissues involved in mass water flux, namely the gut, rectal sac and especially abundant in the salivary glands. IrAQP1 was localised by in situ hybridisation in specific cell and acini types, possibly Type III acini, but absent from the type I acini that are responsible for rehydration of ticks in the non-feeding phase. Gene knockdown of IrAQP1 in isolated salivary glands completely inhibited dopamine-stimulated secretion. Further, IrAQP1 knockdown adult females had 50{\%} reduced body weight gains over the first 5 days feeding on an artificial feeding apparatus and 21{\%} at the point of engorgement on hosts. Haemolymph osmolarity was increased in the IrAQP1-knockdown ticks. Importantly, the blood volume ingested per body weight was reduced by 30{\%}. Overall, it would appear that water passage from the gut to the saliva was disrupted and tick guts were simply too {"}full{"} to ingest more blood. However, double-stranded RNA interference of IrAQP1 did not affect mortality of the ticks which successfully fed to detachment at day 9. Overall, our data indicate that IrAQP1 plays a pivotal role in blood meal water handling through the gut and salivary gland, and although its disruption by double-stranded RNA interference dramatically affects feeding performance, ticks remained feeding on the host with subsequent potential pathogen transmission and, therefore, IrAQP1 is not a suitable candidate target for tick control.",
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author = "Campbell, {Ewan M.} and Marion Burdin and Stefan Hoppler and Bowman, {Alan S.}",
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TY - JOUR

T1 - Role of an aquaporin in the sheep tick Ixodes ricinus

T2 - assessment as a potential control target

AU - Campbell, Ewan M.

AU - Burdin, Marion

AU - Hoppler, Stefan

AU - Bowman, Alan S.

PY - 2010/1

Y1 - 2010/1

N2 - Ticks undergo tremendous osmoregulatory stress as they take on up to 100 times their body weight in blood, returning about 75% of the ingested water and ions via their saliva into the host. We postulated that water channels, or aquaporins, involved in this mass water transport might be good targets for acaricide development. An aquaporin (IrAQP1) identified in the sheep tick, Ixodes ricinus, was present only in tissues involved in mass water flux, namely the gut, rectal sac and especially abundant in the salivary glands. IrAQP1 was localised by in situ hybridisation in specific cell and acini types, possibly Type III acini, but absent from the type I acini that are responsible for rehydration of ticks in the non-feeding phase. Gene knockdown of IrAQP1 in isolated salivary glands completely inhibited dopamine-stimulated secretion. Further, IrAQP1 knockdown adult females had 50% reduced body weight gains over the first 5 days feeding on an artificial feeding apparatus and 21% at the point of engorgement on hosts. Haemolymph osmolarity was increased in the IrAQP1-knockdown ticks. Importantly, the blood volume ingested per body weight was reduced by 30%. Overall, it would appear that water passage from the gut to the saliva was disrupted and tick guts were simply too "full" to ingest more blood. However, double-stranded RNA interference of IrAQP1 did not affect mortality of the ticks which successfully fed to detachment at day 9. Overall, our data indicate that IrAQP1 plays a pivotal role in blood meal water handling through the gut and salivary gland, and although its disruption by double-stranded RNA interference dramatically affects feeding performance, ticks remained feeding on the host with subsequent potential pathogen transmission and, therefore, IrAQP1 is not a suitable candidate target for tick control.

AB - Ticks undergo tremendous osmoregulatory stress as they take on up to 100 times their body weight in blood, returning about 75% of the ingested water and ions via their saliva into the host. We postulated that water channels, or aquaporins, involved in this mass water transport might be good targets for acaricide development. An aquaporin (IrAQP1) identified in the sheep tick, Ixodes ricinus, was present only in tissues involved in mass water flux, namely the gut, rectal sac and especially abundant in the salivary glands. IrAQP1 was localised by in situ hybridisation in specific cell and acini types, possibly Type III acini, but absent from the type I acini that are responsible for rehydration of ticks in the non-feeding phase. Gene knockdown of IrAQP1 in isolated salivary glands completely inhibited dopamine-stimulated secretion. Further, IrAQP1 knockdown adult females had 50% reduced body weight gains over the first 5 days feeding on an artificial feeding apparatus and 21% at the point of engorgement on hosts. Haemolymph osmolarity was increased in the IrAQP1-knockdown ticks. Importantly, the blood volume ingested per body weight was reduced by 30%. Overall, it would appear that water passage from the gut to the saliva was disrupted and tick guts were simply too "full" to ingest more blood. However, double-stranded RNA interference of IrAQP1 did not affect mortality of the ticks which successfully fed to detachment at day 9. Overall, our data indicate that IrAQP1 plays a pivotal role in blood meal water handling through the gut and salivary gland, and although its disruption by double-stranded RNA interference dramatically affects feeding performance, ticks remained feeding on the host with subsequent potential pathogen transmission and, therefore, IrAQP1 is not a suitable candidate target for tick control.

KW - tick

KW - aquaporin

KW - osmoregulation

KW - salivary gland

KW - RNA-interference

KW - knockdown

KW - ixodes ricinus

KW - in situ hybridisation

KW - amblyomma-americanum

KW - salivary-glands

KW - rhipicephalus-sanguineus

KW - protein secretion

KW - water-balance

KW - hard ticks

KW - dog tick

KW - ixodidae

KW - acari

KW - synaptobrevin

U2 - 10.1016/j.ijpara.2009.06.010

DO - 10.1016/j.ijpara.2009.06.010

M3 - Article

VL - 40

SP - 15

EP - 23

JO - International Journal for Parasitology

JF - International Journal for Parasitology

SN - 0020-7519

IS - 1

ER -