Steroid Hormone Function Controls Non-competitive Plasmodium Development in Anopheles

被引:64
作者
Werling, Kristine [1 ]
Shaw, W. Robert [1 ]
Itoe, Maurice A. [1 ]
Westervelt, Kathleen A. [1 ]
Marcenac, Perrine [1 ]
Paton, Douglas G. [1 ]
Peng, Duo [1 ]
Singh, Naresh [1 ]
Smidler, Andrea L. [1 ,2 ]
South, Adam [1 ,9 ,10 ]
Deik, Amy A. [3 ]
Mancio-Silva, Liliana [4 ]
Demas, Allison R. [4 ]
March, Sandra [4 ]
Calvo, Eric [5 ]
Bhatia, Sangeeta N. [3 ,4 ,6 ,7 ,8 ]
Clish, Clary B. [3 ]
Catteruccia, Flaminia [1 ]
机构
[1] Harvard TH Chan Sch Publ Hlth, Dept Immunol & Infect Dis, Boston, MA 02115 USA
[2] Wyss Inst Biol Inspired Engn, Boston, MA 02115 USA
[3] Broad Inst, Cambridge, MA 02142 USA
[4] MIT, Inst Med Engn & Sci, Cambridge, MA 02142 USA
[5] NIAID, Lab Malaria & Vector Res, NIH, Rockville, MD 20852 USA
[6] Howard Hughes Med Inst, Chevy Chase, MD 20815 USA
[7] Koch Inst Integrat Canc Res, Cambridge, MA 02142 USA
[8] Brigham & Womens Hosp, Dept Med, 75 Francis St, Boston, MA 02115 USA
[9] Tufts Univ, Dept Infect Dis & Global Hlth, Grafton, MA 01536 USA
[10] Tufts Univ, Dept Biol, Medford, MA 02155 USA
关键词
HUMAN MALARIA PARASITES; YOELII-NIGERIENSIS; REPRODUCTIVE FITNESS; FEMALE REPRODUCTION; GENE-EXPRESSION; HEPATIC STAGES; MOSQUITO; GAMBIAE; FALCIPARUM; INFECTION;
D O I
10.1016/j.cell.2019.02.036
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
Transmission of malaria parasites occurs when a female Anopheles mosquito feeds on an infected host to acquire nutrients for egg development. How parasites are affected by oogenetic processes, principally orchestrated by the steroid hormone 20-hydroxyecdysone (20E), remains largely unknown. Here we show that Plasmodium falciparum development is intimately but not competitively linked to processes shaping Anopheles gambiae reproduction. We unveil a 20E-mediated positive correlation between egg and oocyst numbers; impairing oogenesis by multiple 20E manipulations decreases parasite intensities. These manipulations, however, accelerate Plasmodium growth rates, allowing sporozoites to become infectious sooner. Parasites exploit mosquito lipids for faster growth, but they do so without further affecting egg development. These results suggest that P. falciparum has adopted a non-competitive evolutionary strategy of resource exploitation to optimize transmission while minimizing fitness costs to its mosquito vector. Our findings have profouad implications for currently proposed control strategies aimed at suppressing mosquito populations.
引用
收藏
页码:315 / +
页数:25
相关论文
共 76 条
[31]   Mosquito immune responses and compatibility between Plasmodium parasites and anopheline mosquitoes [J].
Jaramillo-Gutierrez, Giovanna ;
Rodrigues, Janneth ;
Ndikuyeze, Georges ;
Povelones, Michael ;
Molina-Cruz, Alvaro ;
Barillas-Mury, Carolina .
BMC MICROBIOLOGY, 2009, 9
[32]   Fungal Ecdysteroid-22-oxidase, a New Tool for Manipulating Ecdysteroid Signaling and Insect Development [J].
Kamimura, Manabu ;
Saito, Hitoshi ;
Niwa, Ryusuke ;
Niimi, Teruyuki ;
Toyoda, Kinuko ;
Ueno, Chihiro ;
Kanamori, Yasushi ;
Shimura, Sachiko ;
Kiuchi, Makoto .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2012, 287 (20) :16488-16498
[33]   Towards evolution-proof malaria control with insecticides [J].
Koella, Jacob C. ;
Lynch, Penelope A. ;
Thomas, Matthew B. ;
Read, Andrew F. .
EVOLUTIONARY APPLICATIONS, 2009, 2 (04) :469-480
[34]  
MacDONALD G., 1956, BULL WORLD HEALTH ORGAN, V15, P613
[35]   Metabolomic and Ecdysteroid Variations in Anopheles gambiae s. l. Mosquitoes Exposed to the Stressful Conditions of the Dry Season in Burkina Faso, West Africa [J].
Mamai, W. ;
Mouline, K. ;
Blais, C. ;
Larvor, V. ;
Dabire, K. R. ;
Ouedraogo, G. A. ;
Simard, F. ;
Renault, D. .
PHYSIOLOGICAL AND BIOCHEMICAL ZOOLOGY, 2014, 87 (03) :486-497
[36]   Micropatterned coculture of primary human hepatocytes and supportive cells for the study of hepatotropic pathogens [J].
March, Sandra ;
Ramanan, Vyas ;
Trehan, Kartik ;
Ng, Shengyong ;
Galstian, Ani ;
Gural, Nil ;
Scull, Margaret A. ;
Shlomai, Amir ;
Mota, Maria M. ;
Fleming, Heather E. ;
Khetani, Salman R. ;
Rice, Charles M. ;
Bhatia, Sangeeta N. .
NATURE PROTOCOLS, 2015, 10 (12) :2027-2053
[37]   A Microscale Human Liver Platform that Supports the Hepatic Stages of Plasmodium falciparum and vivax [J].
March, Sandra ;
Ng, Shengyong ;
Velmurugan, Soundarapandian ;
Galstian, Ani ;
Shan, Jing ;
Logan, David J. ;
Carpenter, Anne E. ;
Thomas, David ;
Sim, B. Kim Lee ;
Mota, Maria M. ;
Hoffman, Stephen L. ;
Bhatia, Sangeeta N. .
CELL HOST & MICROBE, 2013, 14 (01) :104-115
[38]   Genome-wide analysis of gene expression in adult Anopheles gambiae [J].
Marinotti, O ;
Calvo, E ;
Nguyen, QK ;
Dissanayake, S ;
Ribeiro, JMC ;
James, AA .
INSECT MOLECULAR BIOLOGY, 2006, 15 (01) :1-12
[39]   COMPLETE DEVELOPMENT OF HEPATIC STAGES OF PLASMODIUM-FALCIPARUM INVITRO [J].
MAZIER, D ;
BEAUDOIN, RL ;
MELLOUK, S ;
DRUILHE, P ;
TEXIER, B ;
TROSPER, J ;
MILTGEN, F ;
LANDAU, I ;
PAUL, C ;
BRANDICOURT, O ;
GUGUENGUILLOUZO, C ;
LANGLOIS, P .
SCIENCE, 1985, 227 (4685) :440-442
[40]   Oleic acid is indispensable for intraerythrocytic proliferation of Plasmodium falciparum [J].
Mi-Ichi, F. ;
Kano, S. ;
Mitamura, T. .
PARASITOLOGY, 2007, 134 :1671-1677