Professor Charles Wondji

Professor of Genetics/ Wellcome Trust Senior Research Fellow in Biomedical Sciences

A brief run through of your education and research/work history prior to your current post at LSTM I obtained my PhD in 2003 in Cameroon with the French research Institute IRD, working on the population genetics of the malaria vector Anopheles gambiae complex in Cameroon. I later moved in 2004 to the vector group of the Liverpool School of Tropical Medicine as a postdoctoral research associate to study the genetics and molecular basis of insecticide resistance in Anopheles funestus. In 2008 I was awarded a Wellcome Trust Research career development fellow for 5 years to characterise the mechanisms of pyrethroid resistance in natural population of Anopheles funestus in Africa. In 2013 I was awarded a Wellcome trust senior fellowship in Biomedical Sciences to improve the control of this major malaria vector in Africa by developing new molecular diagnostic tools, understanding the evolution of resistance and its impact on control interventions. I was promoted to Reader in 2014 and to Professor in Vector Genetics 2018.

Research

My main research interest is the understanding of the biology, genetics and genomics of mosquitoes, vectors of tropical diseases such as Malaria, Lymphatic Filariasis and Dengue. I primarily work on Anopheles funestus, one of the major malaria vectors in Africa which, because of the difficulty of rearing it in laboratory, is less studied than Anopheles gambiae. I am currently studying the mechanisms of insecticide resistance in field populations of An. funestus using a genetic mapping approach (Quantitative Trait Loci (QTL) mapping), transcriptomics (microarray, RNAseq), and Whole genome Sequencing (WGS) to detect resistance genes and markers. My research group also uses functional analyses (GAL4/UAS transgenic expression of mosquito genes in Drosophila, the heterologous expression of candidate genes in E. coli to confirm the ability of candidate genes to confer resistance in field populations. My aim is to use this knowledge to develop simple molecular assays to detect resistance in field populations. This will greatly facilitate the management of insecticide resistance in Africa.

I am also defining patterns of gene flow and selective sweeps to predict the evolution and spread of resistance while assessing the fitness cost of resistance and its impact on control interventions using experimental huts trials in Africa.

I also have a more general interest in insect genetics and genomics including population genetics studies in mosquito species; investigation of insecticide resistance mechanisms in other malaria vectors (An. arabiensis and An. gambiae) and in the dengue vectors Aedes aegypti and Ae albopictus and the Lymphatic filariasis vector Culex quinquefasciatus.

Part of my research team is based in Cameroon at the Centre for Research in Infectious Diseases (CRID).

PhD students

Benjamin Menze	2^nd Year	LSTM,UK
Abdullahi Mohammed	1^st year	LSTM, UK
Magellan Tchouakui	3^rd Year	University Yaoundé I, Cameroon
Leon Mugenzi	2^nd Year	University Buéa, Cameroon
Mersimine Kouamou	2^nd Year	University Yaoundé I, Cameroon
Amelie Wamba	1^st year	University Yaoundé I, Cameroon
Aurelie Yougang	1^st year	University Yaoundé I, Cameroon
Armel Tedjou	1^st year	University Yaoundé I, Cameroon
Amen Fadel	1^st year	University Yaoundé I, Cameroon

Teaching

I participate in the teaching of the BSc programme in Tropical Biology (University of Liverpool), the joint Masters programmes in Biology and Control of Parasites and Disease Vectors/Molecular Biology of Parasites and Disease Vectors and the Diploma of Tropical Medicine and Hygiene (DTMH) at LSTM.

Professional memberships

Member of World Health Organisation (WHO) prequalification team on vector control (PQT-VC) since 2017 in charge of assessing new insecticide-based vector control products

Member of Steering Committee of MARCAD DELTA consortium 2016-2021

Member of the Management board of the PIIVEC Consortium 2017-2022

Member of the Malaria Eradication Scientific Alliance (MESA)

Associate Editor BMC Genomics, Parasites and Vectors, Scientific Reports, Genes journals

Member of grant review panel of Royal Society Grand Challenge scheme since 2015

Ad hoc member of the Wellcome Trust Expert review group 5 (ERG5)

Member of the Wellcome Trust Peer-review College since 2011

Recent publications:

Selected publications

G. D. Weedall, L. M. J. Mugenzi, B. D. Menze, M. Tchouakui, S. S. Ibrahim, N. Amvongo-Adjia, H. Irving, M. J. Wondji, M. Tchoupo, R. Djouaka, J. M. Riveron, C. S. Wondji, A cytochrome P450 allele confers pyrethroid resistance on a major African malaria vector, reducing insecticide-treated bednet efficacy. Sci. Transl. Med. 11, eaat7386 (2019). full text

Riveron JM, Watsenga F, Irving H, Irish SR, Wondji CS. High Plasmodium Infection Rate and Reduced Bed Net Efficacy in Multiple Insecticide-Resistant Malaria Vectors in Kinshasa, Democratic Republic of Congo. J Infect Dis. 2018 Jan 4;217(2):320-328. doi: 10.1093/infdis/jix570.

Barnes KG, Irving H, Chiumia M, Mzilahowa T, Coleman M, Hemingway J, Wondji CS. Restriction to gene flow is associated with changes in the molecular basis of pyrethroid resistance in the malaria vector Anopheles funestus. Proc Natl Acad Sci U S A. 2017 Jan 10;114(2):286-291. doi: 10.1073/pnas.1615458114.

Barnes KG, Weedall GD, Ndula M, Irving H, Mzihalowa T, Hemingway J, Wondji CS. Genomic Footprints of Selective Sweeps from Metabolic Resistance to Pyrethroids in African Malaria Vectors Are Driven by Scale up of Insecticide-Based Vector Control. PLoS Genet. 2017 Feb 2;13(2):e1006539. doi: 10.1371/journal.pgen.1006539. eCollection 2017 Feb.

Riveron JM, Ibrahim SS, Mulamba C, Djouaka R, Irving H, Wondji MJ, Ishak IH, Wondji CS. Genome-Wide Transcription and Functional Analyses Reveal Heterogeneous Molecular Mechanisms Driving Pyrethroids Resistance in the Major Malaria Vector Anopheles funestus Across Africa. G3 (Bethesda). 2017 Jun 7;7(6):1819-1832. doi: 10.1534/g3.117.040147.

Ishak IH, Riveron JM, Ibrahim SS, Stott R, Longbottom J, Irving H, Wondji CS. The Cytochrome P450 gene CYP6P12 confers pyrethroid resistance in kdr-free Malaysian populations of the dengue vector Aedes albopictus. Sci Rep. 2016 Apr 20;6:24707. doi: 10.1038/srep24707.

Ibrahim SS, Ndula M, Riveron JM, Irving H, Wondji CS. The P450 CYP6Z1 confers carbamate/pyrethroid cross-resistance in a major African malaria vector beside a novel carbamate-insensitive N485I acetylcholinesterase-1 mutation. Mol Ecol. 2016 Jul;25(14):3436-52. doi: 10.1111/mec.13673. Epub 2016 Jun 15.

Ibrahim SS, Riveron JM, Bibby J, Irving H, Yunta C, Paine MJ, Wondji CS. Allelic Variation of Cytochrome P450s Drives Resistance to Bednet Insecticides in a Major Malaria Vector. PLoS Genet. 2015 Oct 30;11(10):e1005618. doi: 10.1371/journal.pgen.1005618. eCollection 2015 Oct.

Ibrahim SS, Riveron JM, Stott R, Irving H, Wondji CS. The cytochrome P450 CYP6P4 is responsible for the high pyrethroid resistance in knockdown resistance-free Anopheles arabiensis. Insect Biochem Mol Biol. 2016 Jan;68:23-32. doi: 10.1016/j.ibmb.2015.10.015. Epub 2015 Nov 6.

Weedall GD, Irving H, Hughes MA, Wondji CS. Molecular tools for studying the major malaria vector Anopheles funestus: improving the utility of the genome using a comparative poly(A) and Ribo-Zero RNAseq analysis. BMC Genomics. 2015 Nov 14;16:931. doi: 10.1186/s12864-015-2114-z.

Platt N, Kwiatkowska RM, Irving H, Diabaté A, Dabire R, Wondji CS. Target-site resistance mutations (kdr and RDL), but not metabolic resistance, negatively impact male mating competiveness in the malaria vector Anopheles gambiae. Heredity (Edinb). 2015 Sep;115(3):243-52. doi: 10.1038/hdy.2015.33. Epub 2015 Apr 22.

Riveron JM, Yunta C, Ibrahim SS, Djouaka R, Irving H, Menze BD, Ismail HM, Hemingway J, Ranson H, Albert A, Wondji CS. (2014) A single mutation in the GSTe2 gene allows tracking of metabolically-based insecticide resistance in a major malaria vector. Genome Biol. 2014 Feb 25;15(2):R27.

Riveron JM, Ibrahim SS, Chanda E, Mzilahowa T, Cuamba N, Irving H, Barnes KG, Ndula M, Wondji CS. The highly polymorphic CYP6M7 cytochrome P450 gene partners with the directionally selected CYP6P9a and CYP6P9b genes to expand the pyrethroid resistance front in the malaria vector Anopheles funestus in Africa. BMC Genomics. 2014 Sep 27;15:817. doi: 10.1186/1471-2164-15-817.

Jacob M. Riveron, Helen Irving, Miranda Ndula, Kayla G Barnes, Sulaiman Ibrahim, Mark Paine and Charles S. Wondji (2013). Directionally selected P450 alleles are driving resistance to pyrethroids in populations of the malaria vector Anopheles funestus in Africa. Proc Natl Acad Sci U S A 110(1): 252-257, PMCID: PMC3538203

Charles S. Wondji, Michael Coleman, Immo Kleinschmidt, Themba Mzilahowa, Helen Irving, Miranda Ndula, Andrea M Rehman, John Morgan, Kayla Barnes, and Janet Hemingway (2012). The impact of pyrethroid resistance on operational malaria control. Proc Natl Acad Sci U S A 109, 19063-19070. PMCID: PMC3511128

Irving H, Riveron JM, Ibrahim SS, Lobo NF, Wondji CS (2012) Positional cloning of rp2 QTL associates the P450 genes CYP6Z1, CYP6Z3 and CYP6M7 with pyrethroid resistance in the malaria vector Anopheles funestus. Heredity (Edinb) 109, 383-392. PMCID: PMC3499844

Gregory, R., Darby, A.C., Irving, H., Coulibaly, M.B., Hughes, M., Koekemoer, L.L., Coetzee, M., Ranson, H., Hemingway, J., Hall, N., Wondji, C.S (2011). A de novo Expression Profiling of Anopheles funestus, Malaria Vector in Africa, Using 454 Pyrosequencing. PLoS One 6, e17418. PMCID: PMC3045460

Arensburger, P., Megy, K., Waterhouse, R.M., Abrudan, J., Amedeo, P., Antelo, B., Bartholomay, L., Bidwell, S., Caler, E., Camara, F., Campbell, C.L., Campbell, K.S., Casola, C., Castro, M.T., Chandramouliswaran, I., Chapman, S.B., Christley, S., Costas, J., Eisenstadt, E., Feschotte, C., Fraser-Liggett, C., Guigo, R., Haas, B., Hammond, M., Hansson, B.S., Hemingway, J., Hill, S.R., Howarth, C., Ignell, R., Kennedy, R.C., Kodira, C.D., Lobo, N.F., Mao, C., Mayhew, G., Michel, K., Mori, A., Liu, N., Naveira, H., Nene, V., Nguyen, N., Pearson, M.D., Pritham, E.J., Puiu, D., Qi, Y., Ranson, H., Ribeiro, J.M., Roberston, H.M., Severson, D.W., Shumway, M., Stanke, M., Strausberg, R.L., Sun, C., Sutton, G., Tu, Z.J., Tubio, J.M., Unger, M.F., Vanlandingham, D.L., Vilella, A.J., White, O., White, J.R., Wondji, C.S., Wortman, J., Zdobnov, E.M., Birren, B., Christensen, B.M., Collins, F.H., Cornel, A., Dimopoulos, G., Hannick, L.I., Higgs, S., Lanzaro, G.C., Lawson, D., Lee, N.H., Muskavitch, M.A., Raikhel, A.S. and Atkinson, P.W. (2010) Sequencing of Culex quinquefasciatus establishes a platform for mosquito comparative genomics. Science 330, pp. 86-88.

Wondji CS, Irving H, Morgan J, Lobo NF, Collins FH, Hunt RH, Coetzee M, Hemingway J, Ranson H: Two duplicated P450 genes are associated with pyrethroid resistance in Anopheles funestus, a major malaria vector. Genome Research 2009, 19(3):452-459. PMCID: PMC2661802

Wondji CS, Morgan JC, Coetzee M, Hunt R, Steen K, Black WC, Hemingway J, Ranson H (2007b) Mapping a Quantitative Trait Locus conferring pyrethroid resistance in the African malaria vector Anopheles funestus. BMC Genomics 8: 34. PMCID: PMC1790900

Wondji, C., F. Simard, T. Lehmann, E. Fondjo, A. Same-Ekobo, and D. Fontenille. 2005. Impact of insecticide-treated bed nets implementation on the genetic structure of Anopheles arabiensis in an area of irrigated rice fields in the Sahelian region of Cameroon. Mol Ecol 14: 3683-3693.