Daily rhythms in antennal protein and olfactory sensitivity in the malaria mosquito Anopheles gambiae

Samuel S.C. Rund; Nicolle A. Bonar; Matthew M. Champion; John P. Ghazi; Cameron M. Houk; Matthew T. Leming; Zainulabeuddin Syed; Giles E. Duffield

doi:10.1038/srep02494

Daily rhythms in antennal protein and olfactory sensitivity in the malaria mosquito Anopheles gambiae

Samuel S.C. Rund
, Nicolle A. Bonar
, Matthew M. Champion
, John P. Ghazi
, Cameron M. Houk
, Matthew T. Leming
, Zainulabeuddin Syed
, Giles E. Duffield

Research output: Contribution to journal › Article › peer-review

76 Scopus citations

Abstract

We recently characterized 24-hr daily rhythmic patterns of gene expression in Anopheles gambiae mosquitoes. These include numerous odorant binding proteins (OBPs), soluble odorant carrying proteins enriched in olfactory organs. Here we demonstrate that multiple rhythmically expressed genes including OBPs and takeout proteins, involved in regulating blood feeding behavior, have corresponding rhythmic protein levels as measured by quantitative proteomics. This includes AgamOBP1, previously shown as important to An. gambiae odorant sensing. Further, electrophysiological investigations demonstrate time-of-day specific differences in olfactory sensitivity of antennae to major host-derived odorants. The pre-dusk/dusk peaks in OBPs and takeout gene expression correspond with peak protein abundance at night, and in turn coincide with the time of increased olfactory sensitivity to odorants requiring OBPs and times of increased blood-feeding behavior. This suggests an important role for OBPs inmodulating temporal changes in odorant sensitivity, enabling the olfactory system to coordinate with the circadian niche of An. gambiae.

Original language	English
Article number	2494
Journal	Scientific Reports
Volume	3
DOIs	https://doi.org/10.1038/srep02494
State	Published - Aug 29 2013

Bibliographical note

Funding Information:
This research was supported by grants (to G.E.D.) from Eck Institute for Global Health, and the Center for Rare and Neglected Diseases, University of Notre Dame (UND); and the Indiana Clinical Translational Sciences Institute; and UND College of Science-Summer Undergraduate Research Fellowships (to J.P.G. and C.M.H.). We thank L. Zwiebel and R. Pitts for anti-Agam\Orco serum54; R. Hut for providing CircWave v1.4 software; X. Li for technical assistance; and B. Boggess and M. Joyce for proteomics assistance. OBP crystal structure cartoons in Fig. 1 are from15 and Protein Data Bank (PDB) 3R1O. Mosquito head image from USDA Technical Bulletin 1447.

Funding

This research was supported by grants (to G.E.D.) from Eck Institute for Global Health, and the Center for Rare and Neglected Diseases, University of Notre Dame (UND); and the Indiana Clinical Translational Sciences Institute; and UND College of Science-Summer Undergraduate Research Fellowships (to J.P.G. and C.M.H.). We thank L. Zwiebel and R. Pitts for anti-AgamOrco serum54; R. Hut for providing CircWave v1.4 software; X. Li for technical assistance; and B. Boggess and M. Joyce for proteomics assistance. OBP crystal structure cartoons in Fig. 1 are from15 and Protein Data Bank (PDB) 3R1O. Mosquito head image from USDA Technical Bulletin 1447.

Funders	Funder number
Center for Rare and Neglected Diseases, University of Notre Dame
National Institute of General Medical Sciences DP2GM119177 Sophie Dumont National Institute of General Medical Sciences	R01GM087508
Indiana Clinical and Translational Sciences Institute
University of North Dakota
Eck Institute for Global Health, University of Notre Dame

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 3 Good Health and Well-being

ASJC Scopus subject areas

General

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10.1038/srep02494

Cite this

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title = "Daily rhythms in antennal protein and olfactory sensitivity in the malaria mosquito Anopheles gambiae",

abstract = "We recently characterized 24-hr daily rhythmic patterns of gene expression in Anopheles gambiae mosquitoes. These include numerous odorant binding proteins (OBPs), soluble odorant carrying proteins enriched in olfactory organs. Here we demonstrate that multiple rhythmically expressed genes including OBPs and takeout proteins, involved in regulating blood feeding behavior, have corresponding rhythmic protein levels as measured by quantitative proteomics. This includes AgamOBP1, previously shown as important to An. gambiae odorant sensing. Further, electrophysiological investigations demonstrate time-of-day specific differences in olfactory sensitivity of antennae to major host-derived odorants. The pre-dusk/dusk peaks in OBPs and takeout gene expression correspond with peak protein abundance at night, and in turn coincide with the time of increased olfactory sensitivity to odorants requiring OBPs and times of increased blood-feeding behavior. This suggests an important role for OBPs inmodulating temporal changes in odorant sensitivity, enabling the olfactory system to coordinate with the circadian niche of An. gambiae.",

author = "Rund, \{Samuel S.C.\} and Bonar, \{Nicolle A.\} and Champion, \{Matthew M.\} and Ghazi, \{John P.\} and Houk, \{Cameron M.\} and Leming, \{Matthew T.\} and Zainulabeuddin Syed and Duffield, \{Giles E.\}",

note = "Funding Information: This research was supported by grants (to G.E.D.) from Eck Institute for Global Health, and the Center for Rare and Neglected Diseases, University of Notre Dame (UND); and the Indiana Clinical Translational Sciences Institute; and UND College of Science-Summer Undergraduate Research Fellowships (to J.P.G. and C.M.H.). We thank L. Zwiebel and R. Pitts for anti-Agam\textbackslash{}Orco serum54; R. Hut for providing CircWave v1.4 software; X. Li for technical assistance; and B. Boggess and M. Joyce for proteomics assistance. OBP crystal structure cartoons in Fig. 1 are from15 and Protein Data Bank (PDB) 3R1O. Mosquito head image from USDA Technical Bulletin 1447.",

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AU - Syed, Zainulabeuddin

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Daily rhythms in antennal protein and olfactory sensitivity in the malaria mosquito Anopheles gambiae

Abstract

Bibliographical note

Funding

UN SDGs

ASJC Scopus subject areas

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