Advancing vector biology research: a community survey for future directions, research applications and infrastructure requirements

Alain Kohl, Emilie Pondeville, Esther Schnettler, Andrea Crisanti, Clelia Supparo, George K. Christophides, Paul J. Kersey, Gareth L. Maslen, Willem Takken, Constantianus J. M. Koenraadt, Clelia F. Oliva, Núria Busquets, F. Xavier Abad, Anna-Bella Failloux, Elena A. Levashina, Anthony J. Wilson, Eva Veronesi, Maëlle Pichard, Sarah Arnaud Marsh, Frédéric Simard & Kenneth D. Vernick
Pathogens and Global Health, 2016

A survey initiated by the European Horizon 2020 INFRAVEC-2 consortium set out to canvass priorities in the vector biology research community and to determine key activities that are needed for researchers to efficiently study vectors, vector-pathogen interactions, as well as access the structures and services that allow such activities to be carried out. We summarize the most important findings of the survey which in particular reflect the priorities of researchers in European countries, and which will be of use to stakeholders that include researchers, government, and research organizations.

Transcriptional silencing and activation of paternal DNA during Plasmodium berghei zygotic development and transformation to oocyst

Chiamaka V. Ukegbu, Jee-Sun Cho, George K. Christophides, Dina Vlachou
Cellular Microbiology, 2015

This research reveals a role of epigenetic regulation in parasite’s zygotic development in the mosquito and adds to an emerging picture of complex molecular mechanisms regulating this important stage of malaria transmission.

Antibiotics in ingested human blood affect the mosquito microbiota and capacity to transmit malaria

Mathilde Gendrin, Faye H Rodgers, Rakiswendé S Yerbanga, Jean-Bosco Ouédraogo, María-Gloria Basáñez, Anna Cohuet, and George K Christophides
Nature Communications, 2015

The mosquito microbiota is shown to inhibit Plasmodium infection in the mosquito. We investigated the effects of antibiotics presence in the blood that mosquitoes ingest on their microbiota and capacity to transmit malaria. The presence of the broad spectrum antibiotic cocktail penicillin-streptomycin in the mosquito blood meal leads to reduced bacterial growth and a modified microbiota composition in the mosquito gut. Upon antibiotic treatment, mosquitoes become more permissive to Plasmodium and have a longer lifespan. These data suggest that the antibiotic usage in malaria endemic areas may affect the epidemiology of malaria.

Akinosoglou et. al, 2014
Characterization of Plasmodium Developmental Transcriptomes in A.gambiae midgut Reveals Novel Regulators of Malaria Transmission

Akinosoglou KA, Bushell ES, Ukegbu CV, Schlegelmilch T, Cho JS, Redmond S, Sala K, Christophides GK, Vlachou D
Cellular Microbiology, 2015

This manuscript report for the first time a comprehensive, genome-wide, characterization of the developmental transcriptomes of the rodent malaria parasite P. berghei in vivo, in the midgut, of the major African vector, A. gambiae, from blood bolus stages to mature oocysts. Our data provide unique insights into the transcriptional programs underpinning these developmental events and the molecular framework of interactions with the vector.

VectorBase: an updated bioinformatics resource for invertebrate vectors and other organisms related with human diseases

Gloria I. Giraldo-Calderón, Scott J. Emrich, Robert M. MacCallum, Gareth Maslen, Emmanuel Dialynas, Pantelis Topalis, Nicholas Ho, Sandra Gesing, the VectorBase Consortium, Gregory Madey, Frank H. Collins and Daniel Lawson
Nucleic Acids Research, 2015

VectorBase is a National Institute of Allergy and Infectious Diseases supported Bioinformatics Resource Center (BRC) for invertebrate vectors of human pathogens. Now in its 11th year, VectorBase currently hosts the genomes of 35 organisms including a number of non-vectors for comparative analysis. Hosted data range from genome assemblies with annotated gene features, transcript and protein expression data to population genetics including variation and insecticide-resistance phenotypes. Here we describe improvements to our resource and the set of tools available for interrogating and accessing BRC data including the integration of Web Apollo to facilitate community annotation and providing Galaxy to support user-based workflows. VectorBase also actively supports our community through hands-on workshops and online tutorials.

Climate change and vector-borne diseases of humans

Paul E. Parham, Joanna Waldock, George K. Christophides and Edwin Michael
Philosophical Transactions Royal Society B, 2015

This issue thus aims to provide not only an up-to-date synthesis of current knowledge of, and key research in, the impact of various individual components of climate change (biological, nonbiological, evolutionary and economic factors), but also, crucially, to reveal and highlight the need (and potential means) to address the effects of multiple factor interactions, nonlinearities and human reflexivity if we are to develop and establish a more rigorous agenda for future research, including the provision of useful informatics for informed public health policy-making, in this important area of climate change studies.

Anopheles gambiae blood feeding initiates an anticipatory defense response to Plasmodium berghei

Leanna M. Upton, Michael Povelones, and George K. Christophides
Journal of Innate Immunity, 2015

We screened Anopheles gambiae LRIMs by RNAi for effects on mosquito infection by rodent malaria and found that LRIM9 is a Plasmodium berghei antagonist with phenotypes distinct from family members LRIM1 and APL1C, which are key components of the mosquito complement-like pathway. LRIM9 transcript and protein levels are significantly increased after blood feeding but are unaffected by Plasmodium or midgut microbiota. Interestingly, LRIM9 in the hemolymph is strongly upregulated by direct injection of the ecdysteroid, 20-hydroxyecdysone. Our data suggest that LRIM9 may define a novel anti-Plasmodium immune defense mechanism triggered by blood feeding and that hormonal changes may alert the mosquito to bolster its defenses in anticipation of exposure to blood-borne pathogens.

Genetic dissection of Anopheles gambiae gut epithelial responses to Serratia marcescens

Stathopoulos S, Neafsey DE, Lawniczak MKN, Muskavitch MAT, Christophides GK
PLoS Pathogens, 2014

This publication reveals important players of immune homeostasis in the mosquito gut, including a family of type III fibronectin domain proteins that control the composition of gut microbiota in favour of Enterobacteriaceae. It also identifies for a first time a behavioural circuit that controls homeostatic antibacterial immune responses.

The CLIP-domain serine protease homolog SPCLIP1 regulates complement recruitment to microbial surfaces in the malaria mosquito Anopheles gambiae

Povelones M, Bhagavatula L, Yassine H, Aun Tan L, Upton LM, Osta MA, Christophides GK
PLoS Pathogens, 2013

This manuscript established for the first time the presence of a mosquito complement convertase, which functions in a fashion similar to vertebrate convertase in accumulating the C3-like protein TEP1 on the surface of bacteria and malaria parasites leading to their destruction.

Infection intensity-dependent responses of Anopheles gambiae to the African malaria parasite Plasmodium falciparum

Mendes AM, Awono-Ambene PH, Nsango SE, Cohuet A, Fontenille D, Kafatos FC, Christophides GK, Morlais I, Vlachou D
Infection and Immunity, 2011

This manuscript added substantially to our understanding of the interactions between the human malaria parasite and its most important vector in Africa, and significantly contributed to bridging the knowledge gap between laboratory models and field malaria transmission.

Leucine-rich repeat protein complex activates mosquito complement in defense against Plasmodium parasites

Povelones M, Waterhouse RM, Kafatos FC, Christophides GK
Science, 2009

This was the first time a mosquito complement pathway rather than disparate molecules functioning in defense against pathogens was described. It set the benchmark for mosquito immunity studies and marked the transformation of the field from descriptive to mechanistic.

Paternal effect of the nuclear formin-like protein MISFIT on Plasmodium development in the mosquito vector

Bushell ES, Ecker A, Schlegelmilch T, Goulding D, Dougan G, Sinden RE, Christophides GK, Kafatos FC, Vlachou D
PLoS Pathogens, 2009

Anopheles gambiae PGRPLC-mediated defense against bacteria modulates infections with malaria parasites

Meister S, Agianian B, Turlure F, Relogio A, Morlais I, Kafatos FC, Christophides GK
PLoS Pathogens, 2009

This together with a contemporary article provided the first experimental evidence that the mosquito gut microbiota play an important role in mosquito defense against malaria parasites, opening one of the most dynamic fields in mosquito research to date.

Conserved mosquito/parasite interactions affect development of Plasmodium falciparum in Africa

Mendes AM, Schlegelmilch T, Cohuet A, Awono-Ambene P, De Iorio M, Fontenille D, Morlais I, Christophides GK, Kafatos FC, Vlachou D
PLoS Pathogens, 2008

Evolutionary dynamics of immune-related genes and pathways in disease-vector mosquitoes

Waterhouse RM, Kriventseva EV, Meister S, Xi Z, Alvarez KS, Bartholomay LC, Barillas-Mury C, Bian G, Blandin S, Christensen BM, Dong Y, et al, Christophides GK
Science, 2007

Through this research the entire community came together to pioneer a new way of studying insect immunity, later adapted by other fields. By examining the immune system in modules, it revealed that its various components follow different modes of evolution.

Immune signaling pathways regulating bacterial and malaria parasite infection of the mosquito Anopheles gambiae

Meister S, Kanzok SM, Zheng XL, Luna C, Li TR, Hoa NT, Clayton JR, White KP, Kafatos FC, Christophides GK, Zheng L
Proceedings of the National Academy of Sciences of the United States of America, 2005

Functional genomic analysis of midgut epithelial responses in Anopheles during Plasmodium invasion

Vlachou D, Schlegelmilch T, Christophides GK, Kafatos FC
Current Biology, 2005

This benchmark publication showed that Plasmodium infection elicits a robust mosquito midgut response involving a large fraction of its genome, and revealed for the first time the importance of local epithelial reactions in addition to systemic immune responses.

Real-time, in vivo analysis of malaria ookinete locomotion and mosquito midgut invasion.

Vlachou D, Zimmermann T, Cantera R, Janse CJ, Waters AP, Kafatos FC
Cellular Microbiology, 2004

Effects of mosquito genes on Plasmodium development

Osta MA^, Christophides GK^, Kafatos FC
Science, 2004

This article demonstrated for the first time the presence of a fine interplay between mosquito agonists and antagonists of malaria parasites, and pioneered the use of RNAi in carrying out genetic epistasis experiments. In so doing, it created a new school in mosquito experimental biology [231 citations].

^Equal first authors

Seasonality and Locality Affect the Diversity of Anopheles gambiae and Anopheles coluzzii Midgut Microbiota from Ghana

Jewelna Akorli, Mathilde Gendrin, Nana Adjoa P Pels, Dorothy Yeboah-Manu, George K Christophides, and Michael D Wilson
PLoS One, 2016

We report an analysis of the microbiota composition of mosquitoes collected as larvae in rural and peri-urban natural habitats in Ghana, during both dry and rainy seasons. We show that the bacterial family Shewanellaceae is a prominent member of the mosquito microbiota communities in both seasons, and that the diversity of the microbiota is higher in peri-urban areas and in the dry season.

Differential Effects of azithromycin, doxycycline and co-trimoxazole in ingested blood on the vectorial capacity of malaria mosquitoes

Mathilde Gendrin, Rakiswendé S Yerbanga, Jean-Bosco Ouédraogo, Thierry Lefevre, Anna Cohuet, and George K Christophides
Open Forum Infectious Diseases, 2016

This project follows up on the previous publication by Gendrin et al in Nature Communications (2015) showing that the presence of antibiotics in the mosquito ingested blood can significantly affect the mosquito microbiota and capacity to transmit malaria. We investigated the effect on malaria transmission of antibiotics often used in malaria endemic areas and directly inhibit the development of malaria parasites, including doxycycline, azithromycin and co-trimoxazole. Our findings reveal that doxycycline increases the mosquito permissiveness to malaria infection and lifespan while azithromycin decrease these malaria-transmission parameters.

Flow cytometry analysis of the microbiota associated with the midguts of the midguts of vector mosquitoes

Tibebu Habtewold, Luc Duchateau and George K. Christophides
Parasites and Vectors, 2016

Flow cytometry combined with various cell marking dyes have been successfully applied in the field of ecological microbiology to circumvent the above shortcomings. Here, we describe FCM technique coupled with live/dead differential staining dyes SYBR Green I and Propidium Iodide to quantify and study other essential characteristics of the mosquito gut microbiota.

Large-Scale Modelling of the Environmentally-Driven Population Dynamics of Temperate Aedes albopictus (Skuse)

Kamil Erguler, Stephanie E. Smith-Unna, Joanna Waldock, Yiannis Proestos, George K. Christophides, Jos Lelieveld, Paul E. Parham
PLoS One, 2016

We investigate the theoretical limitations of its range expansion by developing an environmentally-driven mathematical model of its population dynamics. We focus on the temperate strain of Ae. albopictus and compile a comprehensive literature-based database of physiological parameters. As a novel approach, we link its population dynamics to globally-available environmental datasets by performing inference on all parameters. We adopt a Bayesian approach using experimental data as prior knowledge and the surveillance dataset of Emilia-Romagna, Italy, as evidence.

Novel factors of Anopheles gambiae haemocyte immune response to Plasmodium berghei infection

Fabrizio Lombardo and George K. Christophides
Parasites and Vectors, 2016

Here we studied the impact of a subset of genes (37 candidates) from the haemocyte-specific dsRNA collection on the development of Plasmodium in the mosquito by in vivo gene silencing. Our screening identifies 10 novel factors with a role in the mosquito response to Plasmodium. Analysis of in vivo screening phenotypes reveals a significant anti-correlation between the prevalence of oocysts and melanised ookinetes.

Detection of viable plasmodium ookinetes in the midguts of anopheles coluzzi using PMA-qrtPCR

Tibebu Habtewold, Zoe Groom, Luc Duchateau and George K. Christophides
Parasites and Vectors, 2015

Quantitative real-time (qrt) PCR in combination with Propidium Monoazide (PMA) treatment (PMA-qrtPCR) has been previously used for selectively enumerating viable microbial cells. PMA penetrates damaged cell membranes and intercalates in the DNA inhibiting its PCR amplification. Here, we tested the potential of PMA-qrtPCR to discriminate between and quantify live and dead Plasmodium berghei malarial parasites and commensal bacteria in the midgut of Anopheles coluzzii Coetzee & Wilkerson 2013 (formerly An. gambiae M-form).

Plasmodium transmission blocking activities of Vernonia amygdalina extracts and isolated compounds

Solomon M Abay, Leonardo Lucantoni, Nisha Dahiya, Geme Dori, Edson G Dembo, Fulvio Esposito, Guilio Lupidi, Sonny Ogboi, Robert K Ouédraogo, Annamaria Sinisi, Orazio Taglialatela-Scafati, R Serge Yerbanga, Massimo Bramucci, Luana Quassinti, Jean Bosco Ouédraogo, George Christophides and Annette Habluetzel
Malaria Journal, 2015

Aqueous (Ver-H2O) and ethanolic (Ver-EtOH) leaf extracts were tested in vivo for activity against sexual and asexual blood stage P. berghei parasites. In vivo transmission blocking effects of Ver-EtOH and Ver-H2O were estimated by assessing P. berghei oocyst prevalence and density in Anopheles stephensi mosquitoes. Activity targeting early sporogonic stages (ESS), namely gametes, zygotes and ookinetes was assessed in vitro using P. berghei CTRPp.GFP strain. Bioassay guided fractionation was performed to characterize V. amygdalina fractions and molecules for anti-ESS activity. Fractions active against ESS of the murine parasite were tested for ex vivo transmission blocking activity on P. falciparum field isolates. Cytotoxic effects of extracts and isolated compounds vernolide and vernodalol were evaluated on the human cell lines HCT116 and EA.hy926.

Impact of repeated NeemAzal-treated blood meals on the fitness of Anopheles stephensi mosquitoes

Edson G Dembo, Solomon M Abay, Nisha Dahiya, Johnbull S Ogboi, George K Christophides, Giulio Lupidi, Giuseppina Chianese, Leonardo Lucantoni, and Annette Habluetzel
Parasites and Vectors, 2015

Batches of An. stephensi mosquitoes were offered 5 consecutive blood meals on female BALB/c mice treated with NeemAzal® at an azadirachtin A concentration of 60, 105 or 150 mg/kg. The blood feeding capacity was estimated by measuring the haematin content of the rectal fluid excreted by the mosquitoes during feeding. The number of eggs laid was estimated by image analysis and their hatchability assessed by direct observations.

Present and future projections of habitat suitability of the Asian tiger mosquito, a vector of viral pathogens, from global climate simulation

Y. Proestos, G. K. Christophides, K. Ergüler, M. Tanarhte, J. Waldock, J. Lelieveld
Philosophical Transactions Royal Society B, 2015

Here we present global climate model simulations and evaluate the associated uncertainties in view of the main meteorological factors that may affect the distribution of the Asian tiger mosquito (Aedes albopictus), which can transmit pathogens that cause chikungunya, dengue fever, yellow fever and various encephalitides.

Climate, environmental and socio-economic change: weighing up the balance in vector-borne disease transmission

Paul E. Parham, Joanna Waldock, George K. Christophides, Deborah Hemming, Folashade Agusto, Katherine J. Evans, Nina Fefferman, Holly Gaff, Abba Gumel, Shannon LaDeau, Suzanne Lenhart, Ronald E. Mickens, Elena N. Naumova, Richard S. Ostfeld, Paul D. Ready, Matthew B. Thomas, Jorge Velasco-Hernandez, Edwin Michael
Philosophical Transactions Royal Society B, 2015

In this review, we seek to elucidate current knowledge around this topic, identify key themes and uncertainties, evaluate ongoing challenges and open research questions and, crucially, offer some solutions for the field. Although many of these challenges are ubiquitous across multiple VBDs, more specific issues also arise in different vector–pathogen systems.

Mosquito genomics. Highly evolvable malaria vectors: the genomes of 16 Anopheles mosquitoes

Neafsey DE, Waterhouse RM, Abai MR, Aganezov SS, Alekseyev MA, Allen JE, Amon J, Arcà B, Arensburger P, Artemov G, Assour LA, Basseri H, Berlin A, Birren BW, Blandin SA, Brockman AI, Burkot TR, Burt A, Chan CS, Chauve C, Chiu JC, Christensen M, Costantini C, Davidson VL, Deligianni E, Dottorini T, Dritsou V, Gabriel SB, Guelbeogo WM, Hall AB, Han MV, Hlaing T, Hughes DS, Jenkins AM, Jiang X, Jungreis I, Kakani EG, Kamali M, Kemppainen P, Kennedy RC, Kirmitzoglou IK, Koekemoer LL, Laban N, Langridge N, Lawniczak MK, Lirakis M, Lobo NF, Lowy E, MacCallum RM, Mao C, Maslen G, Mbogo C, McCarthy J, Michel K, Mitchell SN, Moore W, Murphy KA, Naumenko AN, Nolan T, Novoa EM, O’Loughlin S, Oringanje C, Oshaghi MA, Pakpour N, Papathanos PA, Peery AN, Povelones M, Prakash A, Price DP, Rajaraman A, Reimer LJ, Rinker DC, Rokas A, Russell TL, Sagnon N, Sharakhova MV, Shea T, Simão FA, Simard F, Slotman MA, Somboon P, Stegniy V, Struchiner CJ, Thomas GW, Tojo M, Topalis P, Tubio JM, Unger MF, Vontas J, Walton C, Wilding CS, Willis JH, Wu YC, Yan G, Zdobnov EM, Zhou X, Catteruccia F, Christophides GK, Collins FH, Cornman RS, Crisanti A, Donnelly MJ, Emrich SJ, Fontaine MC, Gelbart W, Hahn MW, Hansen IA, Howell PI, Kafatos FC, Kellis M, Lawson D, Louis C, Luckhart S, Muskavitch MA, Ribeiro JM, Riehle MA, Sharakhov IV, Tu Z, Zwiebel LJ, Besansky NJ.
Science, 2015

To investigate the genomic basis of vectorial capacity and explore new avenues for vector control, we sequenced the genomes of 16 anopheline mosquito species from diverse locations spanning ~100 million years of evolution.

Proteomic analysis of the Plasmodium male gamete reveals the key role for glycolysis in flagellar motility

Arthur M Talman, Judith H Prieto, Sara Marques, Ceereena Ubaida-Mohien, Mara Lawniczak, Mark N Wass, Tao Xu, Roland Frank, Andrea Ecker, Rebecca S Stanway, Sanjeev Krishna, Michael JE Sternberg, Georges K Christophides, David R Graham, Rhoel R Dinglasan, John R Yates III and Robert E Sinden
Malaria Journal, 2014

Plasmodium berghei microgametes were purified and analysed by whole-cell proteomic analysis for the first time. Data are available via ProteomeXchange with identifier PXD001163.

A serine protease homolog negatively regulates TEP1 consumption in systemic infections of the malaria vector Anopheles gambiae

Hassan Yassine, Layla Kamareddine, Soulaima Chamat, George K. Christophides, and Mike A. Osta
Journal of Innate Immunity, 2014

Here, we show that CLIPA2, a clip domain serine protease homolog of Anopheles gambiae, regulates the consumption of the mosquito complement-like protein TEP1 during systemic bacterial infections. We provide evidence that CLIPA2 localizes to microbial surfaces in a TEP1-dependent manner whereby it negatively regulates the activity of a putative TEP1 convertase, which converts the full-length TEP1-F form into active TEP1cut.

Transmission blocking activity of Azadirachta indica and Guiera senegalensis extracts on the sporogonic development of the Plasmodium falciparum field isolates in Anopheles coluzzii mosquitoes

Rakiswendé S Yerbanga, Leonardo Lucantoni, Robert K Ouédraogo, Dari F Da, Franck A Yao, Koudraogo B Yaméogo, Thomas S Churcher, Giulio Lupidi, Orazio Taglialatela-Scafati, Louis Clément Gouagna, Anna Cohuet, George K Christophides, Jean Bosco Ouédraogo and Annette Habluetzel
Parasites and Vectors, 2014

In this study, we assessed the antiplasmodial effects of 5 extracts obtained from the neem tree Azadirachta indica and Guiera senegalensis against the early vector stages of Plasmodium falciparum, using field isolates. In an ex vivo assay gametocytaemic blood was supplemented with the plant extracts and offered to Anopheles coluzzii females by membrane feeding. Transmission blocking activity was evaluated by assessing oocyst prevalence and density on the mosquito midguts.

Discovery and characterization of two Nimrod superfamily members in Anopheles gambiae

Janet Midega, Joshua Blight, Fabrizio Lombardo, Michael Povelones, Fotis Kafatos, and George K Christophides
Pathogens and Global Health, 2013

We confirm that current annotation of the An. gambiae genome incorrectly identifies AgNimB2 and AgEater as a single gene, AGAP009762.

Meeting report of the Mosquito Kolymbari Meeting 2013

Michael Povelones and George K Christophides
Pathogens and Global Health, 2013

On 15–19 July 2013 the European Molecular Biology Organization (EMBO) and the Orthodox Academy of Crete, in Kolymbari, Chania, Greece, hosted the 6th conference on the Molecular and Population Biology of Mosquitoes and Other Disease Vectors.

Comprehensive genetic dissection of the hemocyte immune response in the malaria mosquito Anopheles gambiae

Lombardo F, Ghani Y, Kafatos FC, and Christophides GK
PLoS Pathogens, 2013

We developed RNA interference screens in mosquito cultured cells to dissect networks of genes that cooperate to carry out specific functions including immune responses against pathogens. This research provided important insights into bacterial phagocytosis, antimicrobial peptide production, complement pathway regulation and cellular homeostasis.

The Anopheles Mosquito Microbiota and Their Impact on Pathogen Transmission

Gendrin M, Christophides GK
New insights into malaria vectors, Prof. Sylvie Manguin (Ed.), ISBN: 978-953-51-1188-7, InTech, 2013

This book chapter reviews the current knowledge on microbiota of Anopheles mosquitoes. After describing the composition of this microbial community and the ways the host gets colonised, the chapter focuses on the effects of microbiota on oral infections by human pathogens and discusses their potential use toward transmission blocking.

Adaptive divergence between incipient species of Anopheles gambiae increases resistance to Plasmodium

White BJ, Lawniczak MK, Cheng C, Coulibaly MB, Wilson MD, Sagnon N, Costantini C, Simard F, Christophides GK, Besansky NJ
Proceedings of the National Academy of Sciences of the United States of America, 2011

This collaborative research report highlights the potential role of mosquito complement in malaria transmission. It reveals that an allelic variant of TEP1 associated with increased resistance to infections by malaria parasites has been swept to fixation in West African mosquitoes and is geographically spreading into neighbouring regions.

SNP genotyping defines complex gene-flow boundaries among African malaria vector mosquitoes

Neafsey DE, Lawniczak MK, Park DJ, Redmond SN, Coulibaly MB, Traore SF, Sagnon N, Costantini C, Johnson C, Wiegand RC, Collins FH, Lander ES, Wirth DF, Kafatos FC, Besansky NJ, Christophides GK, Muskavitch MA
Science, 2010

This manuscript mapped the genomic landscape in which Anopheles gambiae evolution occurs and opened the path for resolving a vigorous scientific debate that lasts for decades. It also established an important tool to study mosquito population structure and phenotype-genotype associations.

Transmission blocking immunity in the malaria non-vector mosquito Anopheles quadriannulatus species A

Habtewold T, Povelones M, Blagborough AM, Christophides GK
PLoS Pathogens, 2008

This manuscript reports for the first time that differences in the capacity of mosquitoes to transmit malaria parasites between vector and nom-vector species may lie with the mosquito immune system.

Genome expression analysis of Anopheles gambiae: responses to injury, bacterial challenge, and malaria infection

Dimopoulos G, Christophides GK, Meister S, Schultz J, White KP, Barillas-Mury C, Kafatos FC
Proceedings of the National Academy of Sciences of the United States of America, 2002

Immunity-related genes and gene families in Anopheles gambiae

Christophides GK, Zdobnov E, Barillas-Mury C, Birney E, Blandin S, Blass C, Brey PT, Collins FH, Danielli A, Dimopoulos G, et al
Science, 2002

This manuscript followed the Anopheles gambiae genome sequencing and marked the beginning of mosquito innate immunity field. The genes and pathways identified in this manuscript fuelled the research in several laboratories for many years [523 citations]
Comparative genome and proteome analysis of Anopheles gambiae and Drosophila melanogaster

Zdobnov EM, von Mering C, Letunic I, Torrents D, Suyama M, Copley RR, Christophides GK, Thomasova D, Holt RA, Subramanian GM, et al
Science, 2002