Mosquito Midgut Prostaglandin Release Establishes Systemic Immune Priming

被引:64
作者
Barletta, Ana Beatriz F. [1 ]
Trisnadi, Nathanie [1 ,3 ]
Ramirez, Jose Luis [1 ,2 ]
Barillas-Mury, Carolina [1 ]
机构
[1] NIAID, Lab Malaria & Vector Res, NIH, Rockville, MD 20852 USA
[2] ARS, USDA, Crop Bioprotect Res Unit, Peoria, IL 61604 USA
[3] Atropos Therapeut Inc, San Carlos, CA 94070 USA
基金
美国国家卫生研究院;
关键词
FAT-BODY; COMPLEMENT; BIOSYNTHESIS; EXPRESSION;
D O I
10.1016/j.isci.2019.07.012
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
Anopheles gambiae mosquitoes that have been infected with Plasmodium mount a more effective immune response to a subsequent infection. Priming is established when Plasmodium invasion of the mosquito midgut allows contact of the gut microbiota with epithelial cells. This event is followed by a systemic release of a hemocyte differentiation factor (HDF) consisting of Lipoxin A4 bound to Evokin, a lipocalin carrier, which increases the proportion of circulating hemocytes. We show that mosquito midgut cells produce and release prostaglandin E2 (PGE2), which attracts hemocytes to the midgut surface and enhances their patrolling activity. Systemic injection of prostaglandins (PGs) recapitulates the priming response and enhances antiplasmodial immunity by triggering HDF production. Although insects lack cyclooxygenases, two heme peroxidases, HPX7 and HPX8, catalyze essential steps in PG biosynthesis in mosquitoes. Mosquito midgut PGE2 release attracts hemocytes and establishes a long-lasting enhanced systemic cellular immune response to Plasmodium infection.
引用
收藏
页码:54 / +
页数:40
相关论文
共 26 条
[1]   The roles of temperature, pH and mosquito factors as triggers of male and female gametogenesis of Plasmodium berghei in vitro [J].
Billker, O ;
Shaw, MK ;
Margos, G ;
Sinden, RE .
PARASITOLOGY, 1997, 115 :1-7
[2]   Complement-like protein TEP1 is a determinant of vectorial capacity in the malaria vector Anopheles gambiae [J].
Blandin, S ;
Shiao, SH ;
Moita, LF ;
Janse, CJ ;
Waters, AP ;
Kafatos, FC ;
Levashina, EA .
CELL, 2004, 116 (05) :661-670
[3]   Activation of mosquito complement antiplasmodial response requires cellular immunity [J].
Castillo, Julio Cesar ;
Ferreira, Ana Beatriz Barletta ;
Trisnadi, Nathanie ;
Barillas-Mury, Carolina .
SCIENCE IMMUNOLOGY, 2017, 2 (07)
[4]   Dynamic remodeling of lipids coincides with dengue virus replication in the midgut of Aedes aegypti mosquitoes [J].
Chotiwan, Nunya ;
Andre, Barbara G. ;
Sanchez-Vargas, Irma ;
Islam, M. Nurul ;
Grabowskia, Jeffrey M. ;
Hopf-Jannasch, Amber ;
Gough, Erik ;
Nakayasu, Ernesto ;
Blair, Carol D. ;
Belisle, John T. ;
Hill, Catherine A. ;
Kuhn, Richard J. ;
Perera, Rushika .
PLOS PATHOGENS, 2018, 14 (02)
[5]   Implication of the Mosquito Midgut Microbiota in the Defense against Malaria Parasites [J].
Dong, Yuemei ;
Manfredini, Fabio ;
Dimopoulos, George .
PLOS PATHOGENS, 2009, 5 (05)
[6]  
EGAN RW, 1979, J BIOL CHEM, V254, P3295
[7]   Two Mosquito LRR Proteins Function as Complement Control Factors in the TEP1-Mediated Killing of Plasmodium [J].
Fraiture, Malou ;
Baxter, Richard H. G. ;
Steinert, Stefanie ;
Chelliah, Yogarany ;
Frolet, Cecile ;
Quispe-Tintaya, Wilber ;
Hoffmann, Jules A. ;
Blandin, Stephanie A. ;
Levashina, Elena A. .
CELL HOST & MICROBE, 2009, 5 (03) :273-284
[8]   Prostaglandin E2 modulates the expression of antimicrobial peptide's in the fat body and midgut of Anopheles albimanus [J].
Gil de Munoz, F. L. Garcia ;
Martinez-Barnetche, J. ;
Lanz-Mendoza, H. ;
Rodriguez, M. H. ;
Hernandez-Hernandez, F. C. .
ARCHIVES OF INSECT BIOCHEMISTRY AND PHYSIOLOGY, 2008, 68 (01) :14-25
[9]   A Peroxidase/Dual Oxidase System Modulates Midgut Epithelial Immunity in Anopheles gambiae [J].
Kumar, Sanjeev ;
Molina-Cruz, Alvaro ;
Gupta, Lalita ;
Rodrigues, Janneth ;
Barillas-Mury, Carolina .
SCIENCE, 2010, 327 (5973) :1644-1648
[10]   Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method [J].
Livak, KJ ;
Schmittgen, TD .
METHODS, 2001, 25 (04) :402-408