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Influence of nutritional metabolism of Anopheles on its transmission capability of malaria parasites

  • Xiu-mei SONG ,
  • Jing-wen WANG
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  • 1 School of Life Sciences, Fudan University, Shanghai 200438, China
    2 Ministry of Education Key Laboratory of Contemporary Anthropology, School of Life Sciences, Fudan University, Shanghai 200438, China

Received date: 2021-10-11

  Revised date: 2021-10-26

  Online published: 2021-11-10

Supported by

National Natural Science Foundation of China(31822051);National Natural Science Foundation of China(U1902211);National Institutes of Health Research Grant Program(R01AI129819)

Abstract

Nutritional metabolism of mosquitoes provides a variety of nutrients and signaling molecules to ensure their growth, development and reproduction. At the same time, malaria parasites utilize Anopheles’ nutritional metabolism for acquisition of nutrients to ensure their own development and proliferation. Up to now, little is known regarding the impact of malaria parasite invasion on Anopheles host metabolism, and how mosquito metabolism affects itself reproduction, immune response and other physiological changes during pathogenic invasion. This review summarizes the interplay between Anopheles metabolism and malaria parasite from the aspects of metabolism of glucose, lipids and amino acids, to provide clues for development of mosquito-borne infectious diseases.

Cite this article

Xiu-mei SONG , Jing-wen WANG . Influence of nutritional metabolism of Anopheles on its transmission capability of malaria parasites[J]. CHINESE JOURNAL OF PARASITOLOGY AND PARASITIC DISEASES, 2021 , 39(5) : 617 -620 . DOI: 10.12140/j.issn.1000-7423.2021.05.009

References

[1] WHO. World Malaria Report 2020[R]. Geneva: WHO, 2020.
[2] Aly AS, Vaughan AM, Kappe SH. Malaria parasite development in the mosquito and infection of the mammalian host[J]. Annu Rev Microbiol, 2009, 63:195-221.
[3] Yassine H, Osta MA. Anopheles gambiae innate immunity[J]. Cell Microbiol, 2010, 12(1):1-9.
[4] Smith RC, Joel VR, Marcelo JL. The Plasmodium bottleneck: malaria parasite losses in the mosquito vector[J]. Memórias Do Instituto Oswaldo Cruz, 2014, 109(5):644-661.
[5] Foster WA. Mosquito sugar feeding and reproductive energetics[J]. Annu Rev Entomol, 1995, 40:443-474.
[6] Barredo E, [R] M. Not just from blood: mosquito nutrient acquisition from nectar sources[J]. Trends Parasitol, 2020, 36(5):473-484.
[7] Lea AO, Dimond JB, DeLong DM. Role of diet in egg development by mosquitoes (Aedes aegypti)[J]. Science, 1956, 123(3203):890-891.
[8] Billingsley PF, Hecker H. Blood digestion in the mosquito, Anopheles stephensi liston (Diptera ∶ Culicidae) and distribution of trypsin, aminopeptidase, and α-glucosidase in the midgut[J]. J Med Entomol, 1991, 28(6):865-871.
[9] Dana AN, Hong YS, Kern MK, et al. Gene expression patterns associated with blood-feeding in the malaria mosquito Anopheles gambiae[J]. BMC Genomics, 2005, 6:5.
[10] Manda H, Gouagna LC, Nyandat E, et al. Discriminative feeding behaviour of Anopheles gambiae s.s. on endemic plants in western Kenya[J]. Med Vet Entomol, 2007, 21(1):103-111.
[11] Manda H, Gouagna LC, Foster WA, et al. Effect of discriminative plant-sugar feeding on the survival and fecundity of Anopheles gambiae[J]. Malar J, 2007, 6:113.
[12] Yu BT, Hu Y, Ding YM, et al. Feeding on different attractive flowering plants affects the energy reserves of Culex pipiens pallens adults[J]. Parasitol Res, 2018, 117(1):67-73.
[13] Gouagna LC, Kerampran R, Lebon C, et al. Sugar-source preference, sugar intake and relative nutritional benefits in Anopheles arabiensis males[J]. Acta Trop, 2014, 132:S70-S79.
[14] Hien DF, Dabiré KR, Roche B, et al. Plant-mediated effects on mosquito capacity to transmit human malaria[J]. PLoS Pathog, 2016, 12(8):e1005773.
[15] Becker A, Schlöder P, Steele JE, et al. The regulation of trehalose metabolism in insects[J]. Experientia, 1996, 52(5):433-439.
[16] Wang M, An Y, Gao L, et al. Glucose-mediated proliferation of a gut commensal bacterium promotes Plasmodium infection by increasing mosquito midgut pH[J]. Cell Rep, 2021, 35(3):108992.
[17] Liu K, Dong Y, Huang Y, et al. Impact of trehalose transporter knockdown on Anopheles gambiae stress adaptation and susceptibility to Plasmodium falciparum infection[J]. Proc Natl Acad Sci USA, 2013, 110(43):17504-17509.
[18] Surachetpong W, Pakpour N, Cheung KW, et al. Reactive oxygen species-dependent cell signaling regulates the mosquito immune response to Plasmodium falciparum[J]. Antioxid Redox Signal, 2011, 14(6):943-955.
[19] Pakpour N, Corby-Harris V, Green GP, et al. Ingested human insulin inhibits the mosquito NF-κB-dependent immune response to Plasmodium falciparum[J]. Infect Immun, 2012, 80(6):2141-2149.
[20] Pietri JE, Pakpour N, Napoli E, et al. Two insulin-like peptides differentially regulate malaria parasite infection in the mosquito through effects on intermediary metabolism[J]. Biochem J, 2016, 473(20):3487-3503.
[21] Nyasembe VO, Teal PEA, Sawa P, et al. Plasmodium falciparum infection increases Anopheles gambiae attraction to nectar sources and sugar uptake[J]. Curr Biol, 2014, 24(2):217-221.
[22] Reynolds JA, Poelchau MF, Rahman Z, et al. Transcript profiling reveals mechanisms for lipid conservation during diapause in the mosquito, Aedes albopictus[J]. J Insect Physiol, 2012, 58(7):966-973.
[23] Zhou G, Miesfeld RL. Energy metabolism during diapause in Culex pipiens mosquitoes[J]. J Insect Physiol, 2009, 55(1):40-46.
[24] van Handel E. Fuel metabolism of the mosquito (Culex quinquefasciatus) embryo[J]. J Insect Physiol, 1993, 39(10):831-833.
[25] Chotiwan N, Andre BG, Sanchez-Vargas I, et al. Dynamic remodeling of lipids coincides with dengue virus replication in the midgut of Aedes aegypti mosquitoes[J]. PLoS Pathog, 2018, 14(2):e1006853.
[26] Atella GC, Bittencourt-Cunha PR, Nunes RD, et al. The major insect lipoprotein is a lipid source to mosquito stages of malaria parasite[J]. Acta Trop, 2009, 109(2):159-162.
[27] Werling K, Shaw WR, Itoe MA, et al. Steroid hormone function controls non-competitive Plasmodium development in Anopheles[J]. Cell, 2019, 177(2): 315-325. e14.
[28] Costa G, Eldering M, Lindquist RL, et al. Mosquito lipids regulate Plasmodium sporogony and infectivity to the mammalian host[J/OL]. bioRxiv, 2017. https://www.biorxiv.org/content/10. 1101/149443v1.
[29] Cheon HM, Shin SW, Bian G, et al. Regulation of lipid metabolism genes, lipid carrier protein lipophorin, and its receptor during immune challenge in the mosquito Aedes aegypti[J]. J Biol Chem, 2006, 281(13):8426-8435.
[30] Gupta L, Noh JY, Jo YH, et al. Apolipophorin-Ⅲ mediates antiplasmodial epithelial responses in Anopheles gambiae (G3) mosquitoes[J]. PLoS One, 2010, 5(11):e15410.
[31] Hansen IA, Attardo GM, Park JH, et al. Target of rapamycin-mediated amino acid signaling in mosquito anautogeny[J]. Proc Natl Acad Sci USA, 2004, 101(29):10626-10631.
[32] Hansen IA, Attardo GM, Roy SG, et al. Target of rapamycin-dependent activation of S6 kinase is a central step in the transduction of nutritional signals during egg development in a mosquito[J]. J Biol Chem, 2005, 280(21):20565-20572.
[33] Sherman IW. Amino acid metabolism and protein synjournal in malarial parasites[J]. Bull World Health Organ, 1977, 55(2/3):265-276.
[34] Payne SH, Loomis WF. Retention and loss of amino acid biosynthetic pathways based on analysis of whole-genome sequences[J]. Eukaryot Cell, 2006, 5(2):272-276.
[35] Liu J, Istvan ES, Gluzman IY, et al. Plasmodium falciparum ensures its amino acid supply with multiple acquisition pathways and redundant proteolytic enzyme systems[J]. Proc Natl Acad Sci USA, 2006, 103(23):8840-8845.
[36] Arai M, Billker O, Morris HR, et al. Both mosquito-derived xanthurenic acid and a host blood-derived factor regulate gametogenesis of Plasmodium in the midgut of the mosquito[J]. Mol Biochem Parasitol, 2001, 116(1):17-24.
[37] Lampe L, Jentzsch M, Kierszniowska S, et al. Metabolic balancing by miR-276 shapes the mosquito reproductive cycle and Plasmodium falciparum development[J]. Nat Commun, 2019, 10(1):5634.
[38] Fuchs S, Behrends V, Bundy JG, et al. Phenylalanine metabolism regulates reproduction and parasite melanization in the malaria mosquito[J]. PLoS One, 2014, 9(1):e84865.
[39] Oliveira JH, Gonçalves RL, Oliveira GA, et al. Energy metabolism affects susceptibility of Anopheles gambiae mosquitoes to Plasmodium infection[J]. Insect Biochem Mol Biol, 2011, 41(6):349-355.
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