Genome-wide profiling of diel and circadian gene expression in the malaria vector Anopheles gambiae
Anopheles gambiae, the primary African vector of malaria parasites, exhibits numerous rhythmic behaviors including flight activity, swarming, mating, host seeking, egg laying, and sugar feeding. However, little work has been performed to elucidate the molecular basis for these daily rhythms. To stud...
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| Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 108; no. 32; pp. E421 - E430 |
|---|---|
| Main Authors | , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
National Academy of Sciences
09.08.2011
National Acad Sciences |
| Series | PNAS Plus |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0027-8424 1091-6490 1091-6490 |
| DOI | 10.1073/pnas.1100584108 |
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| Abstract | Anopheles gambiae, the primary African vector of malaria parasites, exhibits numerous rhythmic behaviors including flight activity, swarming, mating, host seeking, egg laying, and sugar feeding. However, little work has been performed to elucidate the molecular basis for these daily rhythms. To study how gene expression is regulated globally by diel and circadian mechanisms, we have undertaken a DNA microarray analysis of An. gambiae under light/dark cycle (LD) and constant dark (DD) conditions. Adult mated, non-blood-fed female mosquitoes were collected every 4 h for 48 h, and samples were processed with DNA microarrays. Using a cosine wave-fitting algorithm, we identified 1,293 and 600 rhythmic genes with a period length of 20-28 h in the head and body, respectively, under LD conditions, representing 9.7 and 4.5% of the An. gambiae gene set. A majority of these genes was specific to heads or bodies. Examination of mosquitoes under DD conditions revealed that rhythmic programming of the transcriptome is dependent on an interaction between the endogenous clock and extrinsic regulation by the LD cycle. A subset of genes, including the canonical clock components, was expressed rhythmically under both environmental conditions. A majority of genes had peak expression clustered around the day/night transitions, anticipating dawn and dusk. Genes cover diverse biological processes such as transcription/translation, metabolism, detoxification, olfaction, vision, cuticle regulation, and immunity, and include rate-limiting steps in the pathways. This study highlights the fundamental roles that both the circadian clock and light play in the physiology of this important insect vector and suggests targets for intervention. |
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| AbstractList | Anopheles gambiae, the primary African vector of malaria parasites, exhibits numerous rhythmic behaviors including flight activity, swarming, mating, host seeking, egg laying, and sugar feeding. However, little work has been performed to elucidate the molecular basis for these daily rhythms. To study how gene expression is regulated globally by diel and circadian mechanisms, we have undertaken a DNA microarray analysis of An. gambiae under light/dark cycle (LD) and constant dark (DD) conditions. Adult mated, non-blood-fed female mosquitoes were collected every 4 h for 48 h, and samples were processed with DNA microarrays. Using a cosine wave-fitting algorithm, we identified 1,293 and 600 rhythmic genes with a period length of 20-28 h in the head and body, respectively, under LD conditions, representing 9.7 and 4.5% of the An. gambiae gene set. A majority of these genes was specific to heads or bodies. Examination of mosquitoes under DD conditions revealed that rhythmic programming of the transcriptome is dependent on an interaction between the endogenous clock and extrinsic regulation by the LD cycle. A subset of genes, including the canonical clock components, was expressed rhythmically under both environmental conditions. A majority of genes had peak expression clustered around the day/night transitions, anticipating dawn and dusk. Genes cover diverse biological processes such as transcription/translation, metabolism, detoxification, olfaction, vision, cuticle regulation, and immunity, and include rate-limiting steps in the pathways. This study highlights the fundamental roles that both the circadian clock and light play in the physiology of this important insect vector and suggests targets for intervention. Anopheles gambiae, the primary African vector of malaria parasites, exhibits numerous rhythmic behaviors including flight activity, swarming, mating, host seeking, egg laying, and sugar feeding. However, little work has been performed to elucidate the molecular basis for these daily rhythms. To study how gene expression is regulated globally by diel and circadian mechanisms, we have undertaken a DNA microarray analysis of An. gambiae under light/dark cycle (LD) and constant dark (DD) conditions. Adult mated, non-blood-fed female mosquitoes were collected every 4 h for 48 h, and samples were processed with DNA microarrays. Using a cosine wave-fitting algorithm, we identified 1,293 and 600 rhythmic genes with a period length of 20-28 h in the head and body, respectively, under LD conditions, representing 9.7 and 4.5% of the An. gambiae gene set. A majority of these genes was specific to heads or bodies. Examination of mosquitoes under DD conditions revealed that rhythmic programming of the transcriptome is dependent on an interaction between the endogenous clock and extrinsic regulation by the LD cycle. A subset of genes, including the canonical clock components, was expressed rhythmically under both environmental conditions. A majority of genes had peak expression clustered around the day/night transitions, anticipating dawn and dusk. Genes cover diverse biological processes such as transcription/translation, metabolism, detoxification, olfaction, vision, cuticle regulation, and immunity, and include rate-limiting steps in the pathways. This study highlights the fundamental roles that both the circadian clock and light play in the physiology of this important insect vector and suggests targets for intervention. [PUBLICATION ABSTRACT] Anopheles gambiae, the primary African vector of malaria parasites, exhibits numerous rhythmic behaviors including flight activity, swarming, mating, host seeking, egg laying, and sugar feeding. However, little work has been performed to elucidate the molecular basis for these daily rhythms. To study how gene expression is regulated globally by diel and circadian mechanisms, we have undertaken a DNA microarray analysis of An. gambiae under light/dark cycle (LD) and constant dark (DD) conditions. Adult mated, non-blood-fed female mosquitoes were collected every 4 h for 48 h, and samples were processed with DNA microarrays. Using a cosine wave-fitting algorithm, we identified 1,293 and 600 rhythmic genes with a period length of 20-28 h in the head and body, respectively, under LD conditions, representing 9.7 and 4.5% of the An. gambiae gene set. A majority of these genes was specific to heads or bodies. Examination of mosquitoes under DD conditions revealed that rhythmic programming of the transcriptome is dependent on an interaction between the endogenous clock and extrinsic regulation by the LD cycle. A subset of genes, including the canonical clock components, was expressed rhythmically under both environmental conditions. A majority of genes had peak expression clustered around the day/night transitions, anticipating dawn and dusk. Genes cover diverse biological processes such as transcription/translation, metabolism, detoxification, olfaction, vision, cuticle regulation, and immunity, and include rate-limiting steps in the pathways. This study highlights the fundamental roles that both the circadian clock and light play in the physiology of this important insect vector and suggests targets for intervention.Anopheles gambiae, the primary African vector of malaria parasites, exhibits numerous rhythmic behaviors including flight activity, swarming, mating, host seeking, egg laying, and sugar feeding. However, little work has been performed to elucidate the molecular basis for these daily rhythms. To study how gene expression is regulated globally by diel and circadian mechanisms, we have undertaken a DNA microarray analysis of An. gambiae under light/dark cycle (LD) and constant dark (DD) conditions. Adult mated, non-blood-fed female mosquitoes were collected every 4 h for 48 h, and samples were processed with DNA microarrays. Using a cosine wave-fitting algorithm, we identified 1,293 and 600 rhythmic genes with a period length of 20-28 h in the head and body, respectively, under LD conditions, representing 9.7 and 4.5% of the An. gambiae gene set. A majority of these genes was specific to heads or bodies. Examination of mosquitoes under DD conditions revealed that rhythmic programming of the transcriptome is dependent on an interaction between the endogenous clock and extrinsic regulation by the LD cycle. A subset of genes, including the canonical clock components, was expressed rhythmically under both environmental conditions. A majority of genes had peak expression clustered around the day/night transitions, anticipating dawn and dusk. Genes cover diverse biological processes such as transcription/translation, metabolism, detoxification, olfaction, vision, cuticle regulation, and immunity, and include rate-limiting steps in the pathways. This study highlights the fundamental roles that both the circadian clock and light play in the physiology of this important insect vector and suggests targets for intervention. Anopheles gambiae , the primary African vector of malaria parasites, exhibits numerous rhythmic behaviors including flight activity, swarming, mating, host seeking, egg laying, and sugar feeding. However, little work has been performed to elucidate the molecular basis for these daily rhythms. To study how gene expression is regulated globally by diel and circadian mechanisms, we have undertaken a DNA microarray analysis of An. gambiae under light/dark cycle (LD) and constant dark (DD) conditions. Adult mated, non–blood-fed female mosquitoes were collected every 4 h for 48 h, and samples were processed with DNA microarrays. Using a cosine wave-fitting algorithm, we identified 1,293 and 600 rhythmic genes with a period length of 20–28 h in the head and body, respectively, under LD conditions, representing 9.7 and 4.5% of the An. gambiae gene set. A majority of these genes was specific to heads or bodies. Examination of mosquitoes under DD conditions revealed that rhythmic programming of the transcriptome is dependent on an interaction between the endogenous clock and extrinsic regulation by the LD cycle. A subset of genes, including the canonical clock components, was expressed rhythmically under both environmental conditions. A majority of genes had peak expression clustered around the day/night transitions, anticipating dawn and dusk. Genes cover diverse biological processes such as transcription/translation, metabolism, detoxification, olfaction, vision, cuticle regulation, and immunity, and include rate-limiting steps in the pathways. This study highlights the fundamental roles that both the circadian clock and light play in the physiology of this important insect vector and suggests targets for intervention. Our work in the An. gambiae mosquito reveals rhythmic expression of numerous genes across several biological categories. An improved understanding of the rhythmic nature of mosquito biochemistry, physiology, and behavior, including sensory perception and susceptibilities to insecticide or immune challenge, will provide opportunities for novel malarial control strategies and optimization of existing approaches. Indeed, insight into biological timing at the molecular level may prove to be key in the successful implementation of control methods and future experimental design. A number of genes involved in immunity, primarily in the immune deficiency and melanization pathways, show rhythmic expression profiles suggesting time-of-day–specific susceptibility to infection in An. gambiae . The melanization response encapsulates both bacteria and Plasmodium parasites and produces toxic antimicrobial by-products. Because a circadian rhythm of susceptibility to bacterial infection in Drosophila has been demonstrated recently ( 5 ), our results suggest that time-of-day–specific effects should be considered when developing biopesticide-based interventions for An. gambiae . The mosquito uses olfaction to detect blood-feeding hosts and nectar and to select oviposition sites ( 1 ). We identified rhythmic expression of olfaction genes dominated by odorant-binding proteins (OBPs) ( Fig. P1 ). OBPs are soluble proteins located in the olfactory sensilla and are thought to transport odor molecules through the mucous layer to the olfactory receptors, thereby facilitating their activation. Our data indicate that daily changes in OBP levels may modify the olfactory system's sensitivity to specific odors. Interestingly, the OBP genes oscillate with concordant peak phases occurring at dusk or during the early night. It is plausible that these cycles lead to increased sensitivity of the system coinciding with the time of nocturnal host- and nectar-seeking behavior ( 1 ). The odorant coreceptor, OR7 , which is the heterodimer required for all odorant receptor transduction, also was rhythmic in the head, peaking at a time similar to the rhythms of OBP genes near the end of the light phase ( Fig. P1 ). Rhythmicity of OR7 could prove to be another potential gate for diel control of olfactory sensitivity and is especially interesting because it has been implicated in the detection of the insect repellent N,N-diethyl-m-toluamide (DEET). Our analysis also identified rhythmically expressed genes of the visual system, including those contributing to rhodopsin biogenesis and to the phototransduction cascade. Phase-concordant relationships in gene expression between specific partner proteins might contribute to a time-of-day–specific gating mechanism for tuning sensitivity to light. Such temporal changes in sensitivity to light have been reported in other insect species. Our analysis revealed detoxification genes to be rhythmic, including as much as a third of the An. gambiae cytochrome P450 mono-oxygenase (P450) and glutathione S-transferase (GST) genes. These genes include CYP6Z1 , agCYP6P3 , agCYP6M2 , and GSTE2 , whose up-regulation is implicated in insecticide resistance ( Fig. P1 ) ( 4 ). These data highlight the likelihood that An. gambiae exhibits rhythmic sensitivity to insecticides, as has been observed in other insects including Aedes mosquitoes. This finding is important for maximizing exposure of the mosquito to insecticides at the time of day when they may be most susceptible. We identify biological processes whose underlying gene expression is under rhythmic control in An. gambiae and highlight those that may be important in considering measures of insect control. Metabolic demands in the mosquito vary drastically between rest and flight activity. Moreover, in An. gambiae sugar and blood feeding is restricted to the night phase ( 1 ). With these predictable temporal changes in respiratory demands and nutrient availability, it is no surprise that many steps in anabolic/catabolic metabolic pathways were identified as under rhythmic control. Genes under rhythmic control include those involved in glycolysis, the citric acid cycle, oxidative phosphorylation, and fatty acid oxidation pathways. Also, genes associated with control of intermediary metabolism and feeding, nutritional homeostasis, and nutrient mobilization were found to be rhythmic. These genes include target of rapamycin and the takeout genes, which are components of nutrient-sensing signaling pathways and are capable of modulating temporal aspects of feeding behavior. Our data indicate that metabolic activity in An. gambiae is coordinated temporally, allowing the mosquito to anticipate the differing energy demands of activity/rest and the variations in anabolic/catabolic states that occur across the 24-h period. Eukaryotic organisms possess a molecular circadian clock comprising a series of transcriptional–translational feedback loops whose completion takes ∼24 h. The organization of the clock and several of the genes involved are similar across taxonomic groups. In our study of An. gambiae , examination of clock genes revealed the presence of characteristic phase-specific rhythms, such as observed in other mosquito species and in Drosophila ( Fig. P1 ) ( 2 , 3 ). Consistent with recent studies on Aedes and Culex mosquitoes, but dissimilar to Drosophila , the transcriptional repressor and component of the negative feedback loop, cryptochrome 2 ( CRY2 ), was found to be expressed rhythmically in An. gambiae , whereas the cryptochrome 1 gene, encoding a photoreceptor of the clock, was found to be expressed constitutively. These data demonstrate that the An. gambiae circadian system, as well as that of other mosquito species, resembles other insects (e.g., butterfly) more closely than its fellow Dipteran and genetic model organism, Drosophila . Genes regulated by the clock are described as “clock-controlled genes,” and their rhythms in expression are generated by episodic activation/suppression of their promoters, either directly by canonical clock components or via downstream intermediaries. However, an important finding from our analysis in An. gambiae is that the overlap in genes rhythmically expressed under both LD and DD conditions is limited to ∼60%. This incomplete overlap suggests that the An. gambiae 24-h rhythm-generating system comprises two distinct but interlocking mechanisms, one reliant on signals directly from the environmental LD cycle and the other on signals generated internally by the endogenous circadian clock, together forming a bimodal system as similarly proposed for Drosophila ( 3 ). Downstream of this diel and circadian regulation of transcription exist additional posttranscriptional processes. Our results in An. gambiae reveal rhythms in genes involved in gene splicing, translation, and aspects of protein degradation pathways, which could produce, enhance, or modify 24-h rhythms in gene expression and protein abundance. To explore how gene expression is regulated globally in An. gambiae by diel mechanisms, processes directly driven by the environmental light/dark (LD) cycle, and by the endogenous circadian clock, we undertook a DNA microarray analysis of adult female mosquitoes sampled every 4 h over a 48-h period under both LD and constant dark (DD) conditions. This transcriptional analysis of An. gambiae rhythms allows a detailed exploration of the extent to which mosquito biochemistry, physiology, and behavior are controlled by diel and circadian mechanisms ( Fig. P1 ). We sought to characterize the molecular rhythms underlying overt rhythms already documented and to identify hitherto unknown rhythms as have been revealed in model genetic species. With the use of stringent criteria for identifying rhythmic gene-expression profiles, 2,095 genes accounting for at least 15.8% of the An. gambiae gene set were discovered to be rhythmic in either the mosquito head or body and under diel and/or circadian control. In many cases, genes were expressed rhythmically specifically in either the head or the body; these genes covered a wide range of biological functions and processes ( Fig. P1 ). The mosquito Anopheles gambiae is the major African vector o |
| Author | Duffield, Giles E Collins, Frank H Hou, Tim Y Rund, Samuel S.C Ward, Sarah M |
| Author_xml | – sequence: 1 fullname: Rund, Samuel S.C – sequence: 2 fullname: Hou, Tim Y – sequence: 3 fullname: Ward, Sarah M – sequence: 4 fullname: Collins, Frank H – sequence: 5 fullname: Duffield, Giles E |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/21715657$$D View this record in MEDLINE/PubMed |
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| Snippet | Anopheles gambiae, the primary African vector of malaria parasites, exhibits numerous rhythmic behaviors including flight activity, swarming, mating, host... Anopheles gambiae , the primary African vector of malaria parasites, exhibits numerous rhythmic behaviors including flight activity, swarming, mating, host... Anopheles gambiae , the primary African vector of malaria parasites, exhibits numerous rhythmic behaviors including flight activity, swarming, mating, host... |
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| SubjectTerms | adults Algorithms Animals Anopheles - genetics Anopheles gambiae Aquatic insects Biological Sciences Circadian Clocks - genetics circadian rhythm Circadian Rhythm - genetics Circadian rhythms Deoxyribonucleic acid Detoxification DNA DNA microarrays Environmental conditions environmental factors Female females flight Flight behavior Gene expression Gene Expression Profiling Gene Expression Regulation genes Genes, Insect - genetics Genetic Variation Genome, Insect - genetics head host seeking immunity Immunity - genetics insect vectors Insect Vectors - genetics Malaria Malaria - parasitology Membranes - metabolism Metabolic Networks and Pathways - genetics metabolism microarray technology Mosquitoes Olfaction Olfactory Pathways - metabolism oviposition Parasites PNAS Plus Protein Biosynthesis - genetics smell sugar feeding swarming Transcription, Genetic transcriptome translation (genetics) Vector-borne diseases vision Vision, Ocular - genetics |
| Title | Genome-wide profiling of diel and circadian gene expression in the malaria vector Anopheles gambiae |
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