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Antennal sensilla of two female anopheline sibling species with differing host ranges
R Jason Pitts, Laurence J Zwiebel
Malaria Journal , 2006, DOI: 10.1186/1475-2875-5-26
Abstract: Scanning electron and light microscopy were used to examine the antennae ultrastructures of adult female An. gambiae s.s. and An. quadriannulatus. Sensory structures, called sensilla, were categorized and counted; their distributions are reported here as well as densities calculated for each species.Both An. gambiae s.s. and An. quadriannulatus bear five classes of sensilla on their antennae: chaetica (bristles), trichodea (hairs), basiconica (pegs), coeloconica (pitted pegs), and ampullacea (pegs in tubes). Female An. quadriannulatus antennae have approximately one-third more sensilla, and a proportionally larger surface area, than female An. gambiae s.s. antennae.The same types of sensilla are found on the antennae of both species. While An. quadriannulatus has greater numbers of each sensilla type, sensilla densities are very similar for each species, suggesting that other factors may be more important to such olfactory-driven behaviours as host preference.Odors are the principle sensory signals that direct female mosquitoes to their preferred blood meal hosts [1,2]. Antennae of adult mosquitoes bear numerous sensory structures called sensilla, which are the physical sites of chemical detection. Within sensilla, olfactory signal transduction relies on odorant receptor proteins localized on the dendritic membranes of olfactory receptor neurons to initiate the events that ultimately lead to the perception of both the quality and the quantity of odors. Behavioural responses to volatile cues, including host finding by female mosquitoes, are critical components of vectorial capacity, the ability of an insect to transmit disease [2]. Two closely related mosquito sibling species, An. gambiae s.s. and An. quadriannulatus, display very different patterns of blood meal host preference. An. gambiae s.s. exhibits a high degree of anthropophily, while An. quadriannulatus exhibits strong zoophily [2]. Indeed, the strong preference for human blood meals by An. gambiae s.s. fema
Ultrastructural Characterization of Olfactory Sensilla and Immunolocalization of Odorant Binding and Chemosensory Proteins from an Ectoparasitoid Scleroderma guani (Hymenoptera: Bethylidae)
Xiangrui Li, Daguang Lu, Xiaoxia Liu, Qingwen Zhang, Xuguo Zhou
International Journal of Biological Sciences , 2011,
Abstract: The three-dimensional structures of two odorant binding proteins (OBPs) and one chemosensory protein (CSP) from a polyphagous ectoparasitoid Scleroderma guani (Hymenoptera: Bethylidae) were resolved bioinformatically. The results show that both SguaOBP1 and OBP2 are classic OBPs, whereas SguaCSP1 belongs to non-classic CSPs which are considered as the “Plus-C” CSP in this report. The structural differences between the two OBPs and between OBP and CSP are thoroughly described, and the structural and functional significance of the divergent C-terminal regions (e.g., the prolonged C-terminal region in SguaOBP2 and the additional pair of cysteines in SguaCSP1) are discussed. The immunoblot analyses with antisera raised against recombinant SguaOBP1, OBP2, and CSP1, respectively, indicate that two SguaOBPs are specific to antennae, whereas SguaCSP1, which are more abundant than OBPs and detected in both male and female wasps, expresses ubiquitously across different tissues. We also describe the ultrastructure of the antennal sensilla types in S. guani and compare them to 19 species of parasitic Hymenoptera. There are 11 types of sensilla in the flagellum and pedicel segments of antennae in both male and female wasps. Seven of them, including sensilla placodea (SP), long sensilla basiconica (LSB), sensilla coeloconica (SC), two types of double-walled wall pore sensilla (DWPS-I and DWPS-II), and two types of sensilla trichodea (ST-I and ST-II), are multiporous chemosensilla. The ultralsturctures of these sensilla are morphologically characterized. In comparison to monophagous specialists, the highly polyphagous generalist ectoparasitoids such as S. guani possess more diverse sensilla types which are likely related to their broad host ranges and complex life styles. Our immunocytochemistry study demonstrated that each of the seven sensilla immunoreacts with at least one antiserum against SguaOBP1, OBP2, and CSP1, respectively. Anti-OBP2 is specifically labeled in DWPS-II, whereas the anti-OBP1 shows a broad spectrum of immunoactivity toward four different sensilla (LSB, SP, ST-I and ST-II). On the other hand, anti-CSP1 is immunoactive toward SP, DWPS-I and SC. Interestingly, a cross co-localization pattern between SguaOBP1 and CSP1 is documented for the first time. Given that the numbers of OBPs and CSPs in many insect species greatly outnumber their antennal sensilla types, it is germane to suggest such phenomenon could be the rule rather than the exception.
Antennal expression pattern of two olfactory receptors and an odorant binding protein implicated in host odor detection by the malaria vector Anopheles gambiae
Danuta Schymura, Maike Forstner, Anna Schultze, Thomas Kr?ber, Luc Swevers, Kostas Iatrou, Jürgen Krieger
International Journal of Biological Sciences , 2010,
Abstract: Odor-detection in the malaria mosquito Anopheles gambiae involves large families of diverse proteins, including multiple odorant binding proteins (AgOBPs) and olfactory receptors (AgORs). The receptors AgOR1 and AgOR2, as well as the binding protein AgOBP1, have been implicated in the recognition of human host odors. In this study, we have explored the expression of these olfactory proteins, as well as the ubiquitous odorant receptor heteromerization partner AgOR7, in the thirteen flagellomeres (segments) of female and male antenna. Expressing cells were visualized by adapting a whole mount fluorescence in situ hybridization method. In female mosquitoes, AgOR1-expressing olfactory receptor neurons (ORNs) were almost exclusively segregated in segments 3 to 9, whereas AgOR2-expressing ORNs were distributed over flagellomeres 2 to 13. Different individuals comprised a similar number of cells expressing a distinct AgOR type, although their antennal topography and number per flagellomere varied. AgOBP1-expressing support cells were present in segments 3 to 13 of the female antenna, with increasing numbers towards the distal end. In male mosquitoes, total numbers of AgOR- and AgOBP1-expressing cells were much lower. While AgOR2-expressing cells were found on both terminal flagellomeres, AgOR1 cells were restricted to the most distal segment. High densities of AgOBP1-expressing cells were identified in segment 13, whereas segment 12 comprised very few. Altogether, the results demonstrate that both sexes express the two olfactory receptor types as well as the binding protein AgOBP1 but there is a significant sexual dimorphism concerning the number and distribution of these cells. This may suggest gender-specific differences in the ability to detect distinct odorants, specifically human host-derived volatiles.
Scanning electron microscopic observations of Monochamus alternatus antennal sensilla and their electroantennographic responses
松褐天牛触角感器电镜扫描和触角电位反应

WANG Sibao,ZHOU Hongchun,MIAO Xuexia,FAN Meizhen,LI Zengzhi,SI Shengli,HUANG Yongping,
王四宝
,周弘春,苗雪霞,樊美,李增智,司胜利,黄勇平

应用生态学报 , 2005,
Abstract: With scanning electron microscope (SEM), this paper observed the shape, category, amount and distribution of the main antenna sensilla of adult Monochamus alternatus, and tested their electroantennographic (EAG) responses to the main volatiles of Pinus spp.. There were seven types of antennal sensilla, i. e., sensilla trichoid, sensilla basiconica, sensilla digit-like, sensilla rod-like, sensilla bottle-like, sensilla bud-like and sensilla chaetica, among which, sensilla trichoid and sensilla basiconica were the most abundant on the antenna surface, and each of them could be divided into three subtypes. Two subtypes of sensilla digit-like could also be observed. The II and III subtypes of sensilla trichoid and I and II subtypes of sensilla basiconica had deep longitudinal grooves on their surface, the typical characteristics of olfactory receptor. The comparison of the EAG response of different parts of Monochamus alternatus antennae to alpha-Pinene showed that each volatile and their compounds could provoke significant EAG responses of both females and males. The dose-response test showed that there was a certain rule in the EAG responses of M. alternatus.
Distinct Olfactory Signaling Mechanisms in the Malaria Vector Mosquito Anopheles gambiae  [PDF]
Chao Liu,R. Jason Pitts,Jonathan D. Bohbot,Patrick L. Jones,Guirong Wang,Laurence J. Zwiebel
PLOS Biology , 2012, DOI: 10.1371/journal.pbio.1000467
Abstract: Anopheles gambiae is the principal Afrotropical vector for human malaria, in which olfaction mediates a wide range of both adult and larval behaviors. Indeed, mosquitoes depend on the ability to respond to chemical cues for feeding, host preference, and mate location/selection. Building upon previous work that has characterized a large family of An. gambiae odorant receptors (AgORs), we now use behavioral analyses and gene silencing to examine directly the role of AgORs, as well as a newly identified family of candidate chemosensory genes, the An. gambiae variant ionotropic receptors (AgIRs), in the larval olfactory system. Our results validate previous studies that directly implicate specific AgORs in behavioral responses to DEET as well as other odorants and reveal the existence of at least two distinct olfactory signaling pathways that are active in An. gambiae. One system depends directly on AgORs; the other is AgOR-independent and requires the expression and activity of AgIRs. In addition to clarifying the mechanistic basis for olfaction in this system, these advances may ultimately enhance the development of vector control strategies, targeting olfactory pathways in mosquitoes to reduce the catastrophic effects of malaria and other mosquito-borne diseases.
Distinct Olfactory Signaling Mechanisms in the Malaria Vector Mosquito Anopheles gambiae  [PDF]
Chao Liu equal contributor,R. Jason Pitts equal contributor,Jonathan D. Bohbot,Patrick L. Jones,Guirong Wang,Laurence J. Zwiebel
PLOS Biology , 2010, DOI: 10.1371/journal.pbio.1000467
Abstract: Anopheles gambiae is the principal Afrotropical vector for human malaria, in which olfaction mediates a wide range of both adult and larval behaviors. Indeed, mosquitoes depend on the ability to respond to chemical cues for feeding, host preference, and mate location/selection. Building upon previous work that has characterized a large family of An. gambiae odorant receptors (AgORs), we now use behavioral analyses and gene silencing to examine directly the role of AgORs, as well as a newly identified family of candidate chemosensory genes, the An. gambiae variant ionotropic receptors (AgIRs), in the larval olfactory system. Our results validate previous studies that directly implicate specific AgORs in behavioral responses to DEET as well as other odorants and reveal the existence of at least two distinct olfactory signaling pathways that are active in An. gambiae. One system depends directly on AgORs; the other is AgOR-independent and requires the expression and activity of AgIRs. In addition to clarifying the mechanistic basis for olfaction in this system, these advances may ultimately enhance the development of vector control strategies, targeting olfactory pathways in mosquitoes to reduce the catastrophic effects of malaria and other mosquito-borne diseases.
Female Anopheles gambiae antennae: increased transcript accumulation of the mosquito-specific odorant-binding-protein OBP2
Seth A Hoffman, Lakshminarayanan Aravind, Soundarapandian Velmurugan
Parasites & Vectors , 2012, DOI: 10.1186/1756-3305-5-27
Abstract: Our initial focus is on odorant binding proteins with differential transcript accumulation between female and male mosquitoes. We report that the odorant binding protein, OBP2 (AGAP003306), had increased expression in the antennae of female vs. male Anopheles gambiae sensu stricto (G3 strain). The increased expression in antennae of females of this gene by quantitative RT-PCR was 4.2 to 32.3 fold in three independent biological replicates and two technical replicate experiments using A. gambiae from two different laboratories. OBP2 is a member of the vast OBP superfamily of insect odorant binding proteins and belongs to the predominantly dipteran clade that includes the Culex oviposition kairomone-binding OBP1. Phylogenetic analysis indicates that its orthologs are present across culicid mosquitoes and are likely to play a conserved role in recognizing a molecule that might be critical for female behavior.OBP2 has increased mRNA transcript accumulation in the antennae of female as compared to male A. gambiae. This molecule and related molecules may play an important role in female mosquito feeding and breeding behavior. This finding may be a step toward providing a foundation for understanding mosquito olfactory requirements and developing control strategies based on reducing mosquito feeding and breeding success.Factors that influence mosquito fitness, especially host seeking and mate finding are complex and modulated by multiple cues, of which olfactory cues are most important [1-4]. Detection of odor molecules requires odorant binding proteins (OBPs) that are abundant in antennal chemosensilla [5,6]. OBPs are low molecular weight soluble proteins that bind and transport odor molecules from sensillae to G-protein-coupled receptors in olfactory sensory neurons [6]. The finding of receptor AgamOBP1 binding to its ligand indole demonstrated the significance of OBPs in odor recognition [7]. Understanding olfactory function could lead to development of malaria control
Identification and expression profiling of putative odorant-binding proteins in the malaria mosquitoes, Anopheles gambiae and A. arabiensis
Zhengxi Li,Jing-Jiang Zhou,Zuorui Shen,Field Lin
Science China Life Sciences , 2004, DOI: 10.1360/03yc0232
Abstract: Olfaction plays a major role in host-seeking behaviour of mosquitoes. An informatics-based genome-wide analysis of odorant-binding protein (OBP) homologues is undertaken, and 32 putative OBP genes in total in the whole genome sequences of Anopheles gambiae are identified. Tissue-specific expression patterns of all A. gambiae OBP candidates are determined by semi-quantitative Reverse Transcription (RT)-PCR using mosquito actin gene as internal expression control standard. The results showed that 20 OBP candidates had strong expression in mosquito olfactory tissues (female antennae), which indicate that OBPs may play an important role in regulating mosquito olfactory behaviours. Species-specific expression patterns of all putative anopheline OBPs are also studied in two of the most important malaria vectors in A. gambiae complex, i.e. A. gambiae and A. arabiensis, which found 12 of the putative OBP genes examined displayed species-differential expression patterns. The cumulative relative expression intensity of the OBPs in A. arabiensis antennae was higher than that in A. gambiae (the ratio is 1441.45:1314.12), which might be due to their different host preference behaviour. While A. gambiae is a highly anthropophilic mosquito, A. arabiensis is more opportunistic (varying from anthropophilic to zoophilic). So the latter should need more OBPs to support its host selection preference. Identification of mosquito OBPs and verification of their tissue- and species-specific expression patterns represent the first step towards further molecular analysis of mosquito olfactory mechanism, such as recombinant expression and ligand identification.
The location of olfactory receptors within olfactory epithelium is independent of odorant volatility and solubility
Tatjana Abaffy, Anthony R DeFazio
BMC Research Notes , 2011, DOI: 10.1186/1756-0500-4-137
Abstract: Odorants detected by ORs from the dorsal and ventral regions showed overlap in volatility and water solubility. We did not find evidence for a correlation between the solubility and volatility of odorants and the functional expression of olfactory receptors in the dorsal or ventral region of the olfactory epithelia.No simple clustering or relationship between chemical properties of odorants could be associated with the different regions of the olfactory epithelium. These results suggest that the location of ORs within the epithelium is not organized based on the physico-chemical properties of their ligands.The molecular events that lead to olfactory perception can be divided into peripheral (detection by olfactory receptors (ORs) in the nasal epithelium) and central (olfactory bulb and cortex). The events that occur at the peripheral level are not only represented by odorant-receptor affinity, but also include the physico-chemical characteristics of odorants, their diffusion through the mucus, air flow dynamics, as well as the spatial distribution of olfactory receptors within the olfactory epithelium [1-3]. The main olfactory system has a diverse population of receptors (for review see [4]). Most of these receptors remain orphans with no known ligand. Thus, the functional organization of the peripheral olfactory system remains theoretical, particularly in mammals.Odorant discrimination is mediated by ORs using combinatorial coding: a single OR can be activated by multiple odorants and most odorants activate more than one OR [5,6]. Odorants represent a vast array of different chemical structures and each receptor samples a specific region of "chemical space" meaning that it is activated by one or a few combinations of chemical features [7]. A small change in the odorant molecule can result in a fundamental change of its molecular properties (such as functional group, length, flexibility, hydrophobicity, volatility, polarity, chemical bonds) and consequently may chan
A Proteomic Investigation of Soluble Olfactory Proteins in Anopheles gambiae  [PDF]
Guido Mastrobuoni, Huili Qiao, Immacolata Iovinella, Simona Sagona, Alberto Niccolini, Francesca Boscaro, Beniamino Caputo, Marta R. Orejuela, Alessandra della Torre, Stefan Kempa, Antonio Felicioli, Paolo Pelosi, Gloriano Moneti, Francesca Romana Dani
PLOS ONE , 2013, DOI: 10.1371/journal.pone.0075162
Abstract: Odorant-binding proteins (OBPs) and chemosensory proteins (CSPs) are small soluble polypeptides that bind semiochemicals in the lymph of insect chemosensilla. In the genome of Anopheles gambiae, 66 genes encode OBPs and 8 encode CSPs. Here we monitored their expression through classical proteomics (2D gel-MS analysis) and a shotgun approach. The latter method proved much more sensitive and therefore more suitable for tiny biological samples as mosquitoes antennae and eggs. Females express a larger number and higher quantities of OBPs in their antennae than males (24 vs 19). OBP9 is the most abundant in the antennae of both sexes, as well as in larvae, pupae and eggs. Of the 8 CSPs, 4 were detected in antennae, while SAP3 was the only one expressed in larvae. Our proteomic results are in fairly good agreement with data of RNA expression reported in the literature, except for OBP4 and OBP5, that we could not identify in our analysis, nor could we detect in Western Blot experiments. The relatively limited number of soluble olfactory proteins expressed at relatively high levels in mosquitoes makes further studies on the coding of chemical messages at the OBP level more accessible, providing for few specific targets. Identification of such proteins in Anopheles gambiae might facilitate future studies on host finding behavior in this important disease vector.
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