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Nat Microbiol. 2019 Sep 16. doi: 10.1038/s41564-019-0555-x. [Epub ahead of print]

Host serum iron modulates dengue virus acquisition by mosquitoes.

Zhu Y1,2,3, Tong L1,2, Nie K1,2, Wiwatanaratanabutr I4,5, Sun P1,2, Li Q1, Yu X1,2,3, Wu P1,2, Wu T6, Yu C1,2, Liu Q7, Bian Z8, Wang P9, Cheng G10,11.

Author information

1
Tsinghua-Peking Center for Life Sciences, School of Medicine, Tsinghua University, Beijing, China.
2
Institute of Pathogenic Organisms, Shenzhen Center for Disease Control and Prevention, Shenzhen, China.
3
School of Life Sciences, Tsinghua University, Beijing, China.
4
Center of Excellence in Applied Biosciences, King Mongkut's Institute of Technology Ladkrabang, Bangkok, Thailand.
5
Department of Plant Production Technology, Faculty of Agricultural Technology, King Mongkut's Institute of Technology, Ladkrabang, Bangkok, Thailand.
6
Clinical Laboratory Department, Tsinghua University Hospital Beijing, Beijing, China.
7
State Key Laboratory of Infectious Disease Prevention and Control, CCID, ICDC, China CDC, Beijing, China.
8
920 Hospital, Joint Logistics Support Force, PLA, Kunming, China.
9
Department of Immunology, School of Medicine, University of Connecticut Health Center, Farmington, CT, USA.
10
Tsinghua-Peking Center for Life Sciences, School of Medicine, Tsinghua University, Beijing, China. gongcheng@mail.tsinghua.edu.cn.
11
Institute of Pathogenic Organisms, Shenzhen Center for Disease Control and Prevention, Shenzhen, China. gongcheng@mail.tsinghua.edu.cn.

Abstract

A blood meal is the primary route through which mosquitoes acquire an arbovirus infection. Blood components or their metabolites may regulate the susceptibility of mosquitoes to arboviruses. Here we report that serum iron in human blood influences dengue virus acquisition by mosquitoes. Dengue virus acquisition by Aedes aegypti was inversely correlated with the iron concentration in serum from human donors. In a mouse-mosquito acquisition model, iron supplementation reduced dengue virus prevalence and viral load, whereas neutralization of serum iron facilitated dengue virus infection in A. aegypti mosquitoes. Of note, mosquitoes feeding on iron-deficient (sideropenic) mice exhibited a higher prevalence of dengue virus. Reversal of the sideropenic status of hosts largely reduced dengue virus acquisition and infection by mosquitoes. Serum iron, rather than haem-bound iron, was utilized by the mosquito iron metabolism pathway to boost the activity of reactive oxygen species in the gut epithelium, subsequently inhibiting infection by dengue virus. On the basis of these results, a status of iron deficiency in the human population might contribute to the vectorial permissiveness to dengue virus, thereby facilitating its spread by mosquitoes.

PMID:
31527795
DOI:
10.1038/s41564-019-0555-x

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