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Malaria transmission block by vector Anopheles mosquito gut symbiotic bacteria: 20 years progress and prospect

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  • CAS Key Laboratory of Insect Developmental and Evolutionary Biology, CAS Center for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai 200032, China

Received date: 2021-08-08

  Online published: 2021-10-20

Supported by

Supported by the National Key R&D Program of China (No. 2020YFC1200100) and National Natural Science Foundation of China (No. 31830086, 32021001)

Abstract

Malaria is a life-threatening disease caused by Plasmodium parasites,which are transmitted to people through the bites of female Anopheles mosquitoes. The mainstay of current malaria control programs relies on insecticides to control vector mosquito population density and antimalarial drugs to treat infections. However,the emergence and increasing spread of mosquito insecticide resistance and parasite drug resistance have stalled the progress against malaria over the past few years,and call for new intervention strategies. Impeding malaria parasite infection in the vector Anopheles mosquito is a novel strategy to block malaria transmission at the source. The strategy of symbiotic control, using gut microbiota to inhibit parasite development in the mosquito midgut, has been regarded as a promising way to thwart malaria transmission. In this paper the development of symbiotic control including paratransgenesis during the past two decades has been summarized and the future direction of this promising malaria-control strategy has been discussed.

Cite this article

GAO Han, WANG Si-bao . Malaria transmission block by vector Anopheles mosquito gut symbiotic bacteria: 20 years progress and prospect[J]. Chinese Journal of Vector Biology and Control, 2021 , 32(5) : 509 -512 . DOI: 10.11853/j.issn.1003.8280.2021.05.001

References

[1] World Health Organization. World malaria report 2019[R]. Geneva:World Health Organization,2019:4-15.
[2] Talapko J,Škrlec I,Alebić T,et al. Malaria:the past and the present[J]. Microorganisms,2019,7(6):179. DOI:10.3390/microorganisms7060179.
[3] Raghavendra K,Barik TK,Reddy BPN,et al. Malaria vector control:from past to future[J]. Parasitol Res,2011,108(4):757-779. DOI:10.1007/s00436-010-2232-0.
[4] World Health Organization. Global vector control response 2017-2030[EB/OL]. (2017-10-02)[2021-08-04]. https://www.who.int/publications/i/item/9789241512978.
[5] Hamilton WL,Amato R,van der Pluijm RW,et al. Evolution and expansion of multidrug-resistant malaria in southeast Asia:a genomic epidemiology study[J]. Lancet Infect Dis,2019,19(9):943-951. DOI:10.1016/S1473-3099(19)30392-5.
[6] Zhou S,Li ZJ,Cotter C,et al. Trends of imported malaria in China 2010-2014:analysis of surveillance data[J]. Malaria J,2016,15(1):39. DOI:10.1186/s12936-016-1093-0.
[7] 咸越,王曼丽,邵天,等. 我国疟疾防治政策演变及趋势分析[J]. 中国卫生政策研究,2017,10(3):70-74. DOI:10.3969/j.issn.1674-2982.2017.03.012.Xian Y,Wang ML,Shao T,et al. Analysis on the evolution and trend of malaria prevention and control policies in China[J]. Chin J Health Policy,2017,10(3):70-74. DOI:10.3969/j.issn.1674-2982.2017.03.012.
[8] Dondorp AM,Yeung S,White L,et al. Artemisinin resistance:current status and scenarios for containment[J]. Nat Rev Microbiol,2010,8(4):272-280. DOI:10.1038/nrmicro2331.
[9] Ranson H,Lissenden N. Insecticide resistance in african Anopheles mosquitoes:a worsening situation that needs urgent action to maintain malaria control[J]. Trends Parasitol,2016,32(3):187-196. DOI:10.1016/j.pt.2015.11.010.
[10] van der Pluijm RW,Imwong M,Chau NH,et al. Determinants of dihydroartemisinin-piperaquine treatment failure in Plasmodium falciparum malaria in Cambodia,Thailand,and Vietnam:a prospective clinical,pharmacological,and genetic study[J]. Lancet Infect Dis,2019,19(9):952-961. DOI:10.1016/S1473-3099(19)30391-3.
[11] Imwong M,Hien TT,Thuy-Nhien NT,et al. Spread of a single multidrug resistant malaria parasite lineage (PfPailin) to Vietnam[J]. Lancet Infect Dis,2017,17(10):1022-1023. DOI:10.1016/S1473-3099(17)30524-8.
[12] Haldar K,Bhattacharjee S,Safeukui I. Drug resistance in Plasmodium[J]. Nat Rev Microbiol,2018,16(3):156-170. DOI:10.1038/nrmicro.2017.161.
[13] Bhatt S,Weiss DJ,Cameron E,et al. The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015[J]. Nature,2015,526(7572):207-211. DOI:10.1038/nature15535.
[14] Alonso PL,Tanner M. Public health challenges and prospects for malaria control and elimination[J]. Nat Med,2013,19(2):150-155. DOI:10.1038/nm.3077.
[15] Wang SB,Jacobs-Lorena M. Genetic approaches to interfere with malaria transmission by vector mosquitoes[J]. Trends Biotechnol,2013,31(3):185-193. DOI:10.1016/j.tibtech.2013. 01.001.
[16] 崔春来,陈晶晶,王四宝. 蚊媒传染病的遗传控制和共生控制[J]. 应用昆虫学报,2015,52(5):1061-1071. DOI:10.7679/j.issn.2095?1353.2015.127.Cui CL,Chen JJ,Wang SB. Genetic control and paratransgenesis of mosquito-borne diseases[J]. Chin J Appl Entomol,2015,52(5):1061-1071. DOI:10.7679/j.issn.2095?1353.2015.127.
[17] Wang SB,Ghosh AK,Bongio N,et al. Fighting malaria with engineered symbiotic bacteria from vector mosquitoes[J]. Proc Natl Acad Sci USA,2012,109(31):12734-12739. DOI:10. 1073/pnas.1204158109.
[18] Strand MR. Composition and functional roles of the gut microbiota in mosquitoes[J]. Curr Opin Insect Sci,2018,28:59-65. DOI:10.1016/j.cois.2018.05.008.
[19] Straif SC,Mbogo CNM,Toure AM,et al. Midgut bacteria in Anopheles gambiae and An. funestus (Diptera:Culicidae) from Kenya and Mali[J]. J Med Entomol,1998,35(3):222-226. DOI:10.1093/jmedent/35.3.222.
[20] Wang Y,Gilbreath III TM,Kukutla P,et al. Dynamic gut microbiome across life history of the malaria mosquito Anopheles gambiae in Kenya[J]. PLoS One,2011,6(9):e24767. DOI:10.1371/journal.pone.0024767.
[21] Whitten MMA,Shiao SH,Levashina EA. Mosquito midguts and malaria:cell biology,compartmentalization and immunology[J]. Parasite Immunol,2006,28(4):121-130. DOI:10.1111/j.1365-3024.2006.00804.x.
[22] Abraham EG,Jacobs-Lorena M. Mosquito midgut barriers to malaria parasite development[J]. Insect Biochem Mol Biol,2004,34(7):667-671. DOI:10.1016/j.ibmb.2004.03.019.
[23] Drexler AL,Vodovotz Y,Luckhart S. Plasmodium development in the mosquito:biology bottlenecks and opportunities for mathematical modeling[J]. Trends Parasitol,2008,24(8):333-336. DOI:10.1016/j.pt.2008.05.005.
[24] Pumpuni CB,Demaio J,Kent M,et al. Bacterial population dynamics in three anopheline species:the impact on Plasmodium sporogonic development[J]. Am J Trop Med Hyg,1996,54(2):214-218. DOI:10.4269/ajtmh.1996.54.214.
[25] Gao H,Cui CL,Wang LL,et al. Mosquito microbiota and implications for disease control[J]. Trends Parasitol,2020,36(2):98-111. DOI:10.1016/j.pt.2019.12.001.
[26] Riehle MA,Moreira CK,Lampe D,et al. Using bacteria to express and display anti-Plasmodium molecules in the mosquito midgut[J]. Int J Parasitol,2007,37(6):595-603. DOI:10.1016/j.ijpara.2006.12.002.
[27] Yoshida S,Ioka D,Matsuoka H,et al. Bacteria expressing single-chain immunotoxin inhibit malaria parasite development in mosquitoes[J]. Mol Biochem Parasitol,2001,113(1):89-96. DOI:10.1016/S0166-6851(00)00387-X.
[28] Fang WG,Vega-Rodríguez J,Ghosh AK,et al. Development of transgenic fungi that kill human malaria parasites in mosquitoes[J]. Science,2011,331(6020):1074-1077. DOI:10.1126/science.1199115.
[29] Shane JL,Grogan CL,Cwalina C,et al. Blood meal-induced inhibition of vector-borne disease by transgenic microbiota[J]. Nat Commun,2018,9:4127. DOI:10.1038/s41467-018-06580-9.
[30] Cirimotich CM,Dong YM,Clayton AM,et al. Natural microbe-mediated refractoriness to Plasmodium infection in Anopheles gambiae[J]. Science,2011,332(6031):855-858. DOI:10.1126/science.1201618.
[31] Cui CL,Wang Y,Liu JN,et al. A fungal pathogen deploys a small silencing RNA that attenuates mosquito immunity and facilitates infection[J]. Nat Commun,2019,10:4298. DOI:10.1038/s41467-019-12323-1.
[32] Cappelli A,Valzano M,Cecarini V,et al. Killer yeasts exert anti-plasmodial activities against the malaria parasite Plasmodium berghei in the vector mosquito Anopheles stephensi and in mice[J]. Parasit Vectors,2019,12(1):329. DOI:10.1186/s13071-019-3587-4.
[33] Ricci I,Damiani C,Scuppa P,et al. The yeast Wickerhamomyces anomalus(Pichia anomala) inhabits the midgut and reproductive system of the Asian malaria vector Anopheles stephensi[J]. Environ Microbiol,2011,13(4):911-921. DOI:10.1111/j.1462-2920.2010.02395.x.
[34] Bando H,Okado K,Guelbeogo WM,et al. Intra-specific diversity of Serratia marcescens in Anopheles mosquito midgut defines Plasmodium transmission capacity[J]. Sci Rep,2013,3:1641. DOI:10.1038/srep01641.
[35] Wang SB,Dos-Santos ALA,Huang W,et al. Driving mosquito refractoriness to Plasmodium falciparum with engineered symbiotic bacteria[J]. Science,2017,357(6358):1399-1402. DOI:10.1126/science.aan5478.
[36] Bai L,Wang LL,Vega-Rodríguez J,et al. A gut symbiotic bacterium Serratia marcescens renders mosquito resistance to Plasmodium infection through activation of mosquito immune responses[J]. Front Microbiol,2019,10:1580. DOI:10.3389/fmicb.2019.01580.
[37] Gao H,Bai L,Jiang YM,et al. A natural symbiotic bacterium drives mosquito refractoriness to Plasmodium infection via secretion of an antimalarial lipase[J]. Nat Microbiol,2021,6(6):806-817. DOI:10.1038/s41564-021-00899-8.
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