Plasmodium evasion of mosquito immunity and global malaria transmission: The lock-and-key theory

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 49, 2015, Pages 15178-15183

  Molina Cruz, Alvaro ^a   Canepa, Gaspar E ^a   Kamath, Nitin ^a   Pavlovic, Noelle V ^a   Mu, Jianbing ^a   Ramphul, Urvashi N ^a   Ramirez, Jose Luis ^a   Carolina Barillas Mury, ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

Anopheles immunity; Immune evasion; Malaria globalization; Pfs47; Plasmodium selection

Indexed keywords

PFS47 PROTEIN; PROTOZOAL PROTEIN; UNCLASSIFIED DRUG;

AFRICA; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ASIA; CONTROLLED STUDY; DISEASE TRANSMISSION; FEMALE; GENETIC TRAIT; GEOGRAPHIC ORIGIN; HAPLOTYPE; HUMAN; IMMUNE EVASION; IMMUNE SYSTEM; MALARIA FALCIPARUM; MOSQUITO; NONHUMAN; PARASITE IMMUNITY; PARASITE ISOLATION; PLASMODIUM FALCIPARUM; POPULATION STRUCTURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; WESTERN HEMISPHERE; ANIMAL; ANOPHELES GAMBIAE; IMMUNOLOGY; INSECT VECTOR; MOLECULAR GENETICS; PARASITOLOGY; PHYSIOLOGY; TRANSMISSION;

ANIMALS; ANOPHELES GAMBIAE; IMMUNE EVASION; INSECT VECTORS; MALARIA, FALCIPARUM; MOLECULAR SEQUENCE DATA; PLASMODIUM FALCIPARUM;

EID: 84949239034     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1520426112     Document Type: Article

References (41)

1. Liu W, et al. (2010) Origin of the human malaria parasite Plasmodium falciparum in gorillas. Nature 467(7314):420-425.
2. Hartl DL (2004) The origin of malaria: Mixed messages from genetic diversity. Nat Rev Microbiol 2(1):15-22.
3. Sinka ME, et al. (2012) A global map of dominant malaria vectors. Parasit Vectors 5:69.
4. Neafsey DE, et al. (2015) Mosquito genomics. Highly evolvable malaria vectors: The genomes of 16 Anopheles mosquitoes. Science 347(6217):1258522.
5. Molina-Cruz A, Barillas-Mury C (2014) The remarkable journey of adaptation of the Plasmodium falciparum malaria parasite to New World anopheline mosquitoes. Mem Inst Oswaldo Cruz 109(5):662-667.
6. Grieco JP, Achee NL, Roberts DR, Andre RG (2005) Comparative susceptibility of three species of Anopheles from Belize, Central America, to Plasmodium falciparum (NF-54). J Am Mosq Control Assoc 21(3):279-290.
7. Garver LS, Dong Y, Dimopoulos G (2009) Caspar controls resistance to Plasmodium falciparum in diverse anopheline species. PLoS Pathog 5(3):e1000335.
8. Baton LA, Ranford-Cartwright LC (2012) Ookinete destruction within the mosquito midgut lumen explains Anopheles albimanus refractoriness to Plasmodium falcipa-rum (3D7A) oocyst infection. Int J Parasitol 42(3):249-258.
9. Hume JC, Tunnicliff M, Ranford-Cartwright LC, Day KP (2007) Susceptibility of Anopheles gambiae and Anopheles stephensi to tropical isolates of Plasmodium falciparum. Malar J 6:139.
10. Joy DA, et al. (2008) Local adaptation and vector-mediated population structure in Plasmodium vivax malaria. Mol Biol Evol 25(6):1245-1252.
11. Li J, et al. (2001) Geographic subdivision of the range of the malaria parasite Plas-modium vivax. Emerg Infect Dis 7(1):35-42.
12. Blandin S, et al. (2004) Complement-like protein TEP1 is a determinant of vectorial capacity in the malaria vector Anopheles gambiae. Cell 116(5):661-670.
13. Molina-Cruz A, et al. (2012) Some strains of Plasmodium falciparum, a human malaria parasite, evade the complement-like system of Anopheles gambiae mosquitoes. Proc Natl Acad Sci USA 109(28):E1957-E1962.
14. Molina-Cruz A, et al. (2013) The human malaria parasite Pfs47 gene mediates evasion of the mosquito immune system. Science 340(6135):984-987.
15. Povelones M, Waterhouse RM, Kafatos FC, Christophides GK (2009) Leucine-rich repeat protein complex activates mosquito complement in defense against Plasmodium parasites. Science 324(5924):258-261.
16. Fraiture M, et al. (2009) Two mosquito LRR proteins function as complement control factors in the TEP1-mediated killing of Plasmodium. Cell Host Microbe 5(3):273-284.
17. Oliveira G de A, Lieberman J, Barillas-Mury C (2012) Epithelial nitration by a peroxidase/NOX5 system mediates mosquito antiplasmodial immunity. Science 335(6070):856-859.
18. Ramphul UN, Garver LS, Molina-Cruz A, Canepa GE, Barillas-Mury C (2015) Plasmodium falciparum evades mosquito immunity by disrupting JNK-mediated apoptosis of invaded midgut cells. Proc Natl Acad Sci USA 112(5):1273-1280.
19. Garver LS, de Almeida Oliveira G, Barillas-Mury C (2013) The JNK pathway is a key mediator of Anopheles gambiae antiplasmodial immunity. PLoS Pathog 9(9):e1003622.
20. van Schaijk BC, et al. (2006) Pfs47, paralog of the male fertility factor Pfs48/45, is a female specific surface protein in Plasmodium falciparum. Mol Biochem Parasitol 149(2):216-222.
21. Waterhouse RM, et al. (2007) Evolutionary dynamics of immune-related genes and pathways in disease-vector mosquitoes. Science 316(5832):1738-1743.
22. Tonkin ML, et al. (2013) Structural and biochemical characterization of Plasmodium falciparum 12 (Pf12) reveals a unique interdomain organization and the potential for an antiparallel arrangement with Pf41. J Biol Chem 288(18):12805-12817.
23. Anthony TG, Polley SD, Vogler AP, Conway DJ (2007) Evidence of non-neutral polymorphism in Plasmodium falciparum gamete surface protein genes Pfs47 and Pfs48/45. Mol Biochem Parasitol 156(2):117-123.
24. Manske M, et al. (2012) Analysis of Plasmodium falciparum diversity in natural infections by deep sequencing. Nature 487(7407):375-379.
25. Lambrechts L, Halbert J, Durand P, Gouagna LC, Koella JC (2005) Host genotype by parasite genotype interactions underlying the resistance of anopheline mosquitoes to Plasmodium falciparum. Malar J 4:3.
26. Harris C, et al. (2012) Plasmodium falciparum produce lower infection intensities in local versus foreign Anopheles gambiae populations. PLoS One 7(1):e30849.
27. Ariey F, et al. (2014) A molecular marker of artemisinin-resistant Plasmodium falciparum malaria. Nature 505(7481):50-55.
28. Trager W, Jensen JB (1976) Human malaria parasites in continuous culture. Science 193(4254):673-675.
29. Zolg JW, MacLeod AJ, Dickson IH, Scaife JG (1982) Plasmodium falciparum: Modifications of the in vitro culture conditions improving parasitic yields. J Parasitol 68(6):1072-1080.
30. Ifediba T, Vanderberg JP (1981) Complete in vitro maturation of Plasmodium falciparum gametocytes. Nature 294(5839):364-366.
31. Molina-Cruz A, et al. (2008) Reactive oxygen species modulate Anopheles gambiae immunity against bacteria and Plasmodium. J Biol Chem 283(6):3217-3223.
32. Jaramillo-Gutierrez G, et al. (2009) Mosquito immune responses and compatibility between Plasmodium parasites and anopheline mosquitoes. BMC Microbiol 9:154.
33. Librado P, Rozas J (2009) DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25(11):1451-1452.
34. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30(12):2725-2729.
35. Lacroix C, et al. (2011) FLP/FRT-mediated conditional mutagenesis in pre-erythrocytic stages of Plasmodium berghei. Nat Protoc 6(9):1412-1428.
36. Nkrumah LJ, et al. (2006) Efficient site-specific integration in Plasmodium falciparum chromosomes mediated by mycobacteriophage Bxb1 integrase. Nat Methods 3(8):615-621.
37. Maier AG, et al. (2008) Exported proteins required for virulence and rigidity of Plasmodium falciparum-infected human erythrocytes. Cell 134(1):48-61.
38. Utatsu I, Sakamoto S, Imura T, Toh-e A (1987) Yeast plasmids resembling 2 micron DNA: Regional similarities and diversities at the molecular level. J Bacteriol 169(12):5537-5545.
39. Deitsch K, Driskill C, Wellems T (2001) Transformation of malaria parasites by the spontaneous uptake and expression of DNA from human erythrocytes. Nucleic Acids Res 29(3): 850-853.
40. Adjalley SH, Lee MC, Fidock DA (2010) A method for rapid genetic integration into Plasmodium falciparum utilizing mycobacteriophage Bxb1 integrase. Methods Mol Biol 634:87-100.
41. Caro F, Miller MG, DeRisi JL (2012) Plate-based transfection and culturing technique for genetic manipulation of Plasmodium falciparum. Malar J 11:22.