#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Infections Are Virulent and Inhibit the Human Malaria Parasite in


Endosymbiotic Wolbachia bacteria are potent modulators of pathogen infection and transmission in multiple naturally and artificially infected insect species, including important vectors of human pathogens. Anopheles mosquitoes are naturally uninfected with Wolbachia, and stable artificial infections have not yet succeeded in this genus. Recent techniques have enabled establishment of somatic Wolbachia infections in Anopheles. Here, we characterize somatic infections of two diverse Wolbachia strains (wMelPop and wAlbB) in Anopheles gambiae, the major vector of human malaria. After infection, wMelPop disseminates widely in the mosquito, infecting the fat body, head, sensory organs and other tissues but is notably absent from the midgut and ovaries. Wolbachia initially induces the mosquito immune system, coincident with initial clearing of the infection, but then suppresses expression of immune genes, coincident with Wolbachia replication in the mosquito. Both wMelPop and wAlbB significantly inhibit Plasmodium falciparum oocyst levels in the mosquito midgut. Although not virulent in non-bloodfed mosquitoes, wMelPop exhibits a novel phenotype and is extremely virulent for approximately 12–24 hours post-bloodmeal, after which surviving mosquitoes exhibit similar mortality trajectories to control mosquitoes. The data suggest that if stable transinfections act in a similar manner to somatic infections, Wolbachia could potentially be used as part of a strategy to control the Anopheles mosquitoes that transmit malaria.


Vyšlo v časopise: Infections Are Virulent and Inhibit the Human Malaria Parasite in. PLoS Pathog 7(5): e32767. doi:10.1371/journal.ppat.1002043
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002043

Souhrn

Endosymbiotic Wolbachia bacteria are potent modulators of pathogen infection and transmission in multiple naturally and artificially infected insect species, including important vectors of human pathogens. Anopheles mosquitoes are naturally uninfected with Wolbachia, and stable artificial infections have not yet succeeded in this genus. Recent techniques have enabled establishment of somatic Wolbachia infections in Anopheles. Here, we characterize somatic infections of two diverse Wolbachia strains (wMelPop and wAlbB) in Anopheles gambiae, the major vector of human malaria. After infection, wMelPop disseminates widely in the mosquito, infecting the fat body, head, sensory organs and other tissues but is notably absent from the midgut and ovaries. Wolbachia initially induces the mosquito immune system, coincident with initial clearing of the infection, but then suppresses expression of immune genes, coincident with Wolbachia replication in the mosquito. Both wMelPop and wAlbB significantly inhibit Plasmodium falciparum oocyst levels in the mosquito midgut. Although not virulent in non-bloodfed mosquitoes, wMelPop exhibits a novel phenotype and is extremely virulent for approximately 12–24 hours post-bloodmeal, after which surviving mosquitoes exhibit similar mortality trajectories to control mosquitoes. The data suggest that if stable transinfections act in a similar manner to somatic infections, Wolbachia could potentially be used as part of a strategy to control the Anopheles mosquitoes that transmit malaria.


Zdroje

1. DongYManfrediniFDimopoulosG 2009 Implication of the mosquito midgut microbiota in the defense against malaria parasites. PLoS Pathog 5 e1000423

2. WerrenJHBaldoLClarkME 2008 Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6 741 751

3. StouthamerRBreeuwerJAHurstGD 1999 Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu Rev Microbiol 53 71 102

4. HedgesLMBrownlieJCO'NeillSLJohnsonKN 2008 Wolbachia and virus protection in insects. Science 322 702 702

5. KambrisZCookPEPhucHKSinkinsSP 2009 Immune activation by life-shortening Wolbachia and reduced filarial competence in mosquitoes. Science 326 134 136

6. MoreiraLAIturbe-OrmaetxeIJefferyJALuGPykeAT 2009 A Wolbachia symbiont in Aedes aegypti limits infection with Dengue, Chikungunya, and Plasmodium. Cell 139 1268 1278

7. GlaserRLMeolaMA 2010 The native Wolbachia endosymbionts of Drosophila melanogaster and Culex quinquefasciatus increase host resistance to West Nile virus infection. PLoS ONE 5 e11977

8. BianGXuYLuPXieYXiZ 2010 The endosymbiotic bacterium Wolbachia induces resistance to Dengue virus in Aedes aegypti. PLos Pathog 6 e1000833

9. TeixeiraLFerreiraAAshburnerM 2008 The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol 6 e1000002

10. OsborneSELeongYSO'NeillSLJohnsonKN 2009 Variation in antiviral protection mediated by different Wolbachia strains in Drosophila simulans. PLoS Pathog 5 e1000656

11. KambrisZBlagboroughAMPintoSBBlagroveMSCGodfrayHCJ 2010 Wolbachia stimulates immune gene expression and inhibits Plasmodium development in Anopheles gambiae. PLoS Pathog 6 e1001143

12. McMenimanCJLaneAMCassBNFongAWCSidhuM 2009 Stable introduction of a life-shortening Wolbachia infection into the mosquito Aedes aegypti. Science 323 141 144

13. MinKTBenzerS 1997 Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. Proc Natl Acad Sci USA 94 10792 10796

14. CookPMcMenimanCJO'NeillSL 2008 Modifying insect population age structure to control vector-borne disease. Adv Exp Med Biol 627 126 140

15. SinkinsSPO'NeillSL 2000 Wolbachia as a vehicle to modify insect populations. HandlerAFJamesAA Insect Transgenesis: Methods and Applications New York CRC Press 271 287

16. RasgonJLRenXPetridisM 2006 Can Anopheles gambiae be infected with Wolbachia pipientis? Insights from an in vitro system. Appl Environ Microbiol 72 7718 7722

17. JinCRenXRasgonJL 2009 The virulent Wolbachia strain wMelPop efficiently establishes somatic infections in the malaria vector Anopheles gambiae. Appl Environ Microbiol 75 3373 3376

18. Ruang-AreerateTKittayapongP 2006 Wolbachia transinfection in Aedes aegypti: A potential gene driver of dengue vectors. Proc Natl Acad Sci USA 103 12534 12539

19. KangLMaXCaiLLiaoSSunL 2003 Superinfection of Laodelphax striatellus with Wolbachia from Drosophila simulans. Heredity 90 71 76

20. FrydmanHMLiJMRobsonDNWieschausE 2006 Somatic stem cell niche tropism in Wolbachia. Nature 441 509 512

21. KawaiSMatsumotoYGotohTNodaH 2009 Transinfection of Wolbachia in planthoppers: nymphal injection of cultured Wolbachia and infection dynamics. Environ Entomol 38 1626 1633

22. KageyamaDNaritaSNodaH 2008 Transfection of feminizing Wolbachia endosymbionts of the butterfly, Eurema hecabe, into the cell culture and various immature stages of the silkmoth, Bombyx mori. Microb Ecol 56 733 741

23. AhmedAMHurdH 2006 Immune stimulation and malaria infection impose reproductive costs in Anopheles gambiae via follicular apoptosis. Microbes Infect 8 308 315

24. McMenimanCJLaneAMFongAWCVoroninDAIturbe-OrmaetxeI 2008 Host adaptation of a Wolbachia strain after long-term serial passage in mosquito cell lines. Appl Environ Microbiol 74 6963 6969

25. HughesGLRenXRamirezJLSakamotoJMBaileyJA 2011 Wolbachia infections in Anopheles gambiae cells: transcriptomic characterization of a novel host-symbiont interaction. PLoS Pathog 7 e1001296

26. SandersHREvansAMRossLSGillSS 2003 Blood meal induces global changes in midgut gene expression in the disease vector, Aedes aegypti. Insect Biochem Mol Biol 33 1105 1122

27. RibeiroJM 2003 A catalogue of Anopheles gambiae transcripts significantly more or less expressed following a blood meal. Insect Biochem Mol Biol 33 865 882

28. MarinottiONguyenQKCalvoEJamesAARibeiroJM 2005 Microarray analysis of genes showing variable expression following a blood meal in Anopheles gambiae. Insect Mol Biol 14 365 373

29. HoltRA 2002 The genome sequence of the malaria mosquito Anopheles gambiae. Science 298 129 149

30. DanaANHongYSKernMKHillenmeyerMEHarkerBW 2005 Gene expression patterns associated with blood-feeding in the malaria mosquito Anopheles gambiae. BMC Genomics 6 5

31. BrownlieJCCassBNRieglerMWitsenburgJJIturbe-OrmaetxeI 2009 Evidence for metabolic provisioning by a common invertebrate endosymbiont, Wolbachia pipientis, during periods of nutritional stress. PLoS Pathog 5 e1000368

32. KremerNVoroninDACharifDMavinguiPMollereauB 2009 Wolbachia interferes with ferritin expression and iron metabolism in insects. PLoS Pathog 5 e1000630

33. MagalhaesTBrackneyDEBeierJCFoyBD 2008 Silencing an Anopheles gambiae catalase and sulfhydryl oxidase increases mosquito mortality after a blood meal. Arch Insect Biochem Physiol 68 134 143

34. OliveiraJHMGonçalvesRLSLaraFADiasFAGandaraACP 2011 Blood Meal-Derived Heme Decreases ROS Levels in the Midgut of Aedes aegypti and Allows Proliferation of Intestinal Microbiota. PLoS Pathog 7 e1001320

35. McMenimanCJHughesGLO'NeillSL 2011 A Wolbachia symbiont in Aedes aegypti disrupts mosquito egg development to a greater extent when mosquitoes feed on nonhuman versus human blood. J Med Entomol 48 76 84

36. RasgonJLGamstonCRenXX 2006 Survival of Wolbachia pipientis in cell-free medium. Appl Environ Microbiol 72 6934 6937

37. KonoMKogaRShimadaMFukatsuT 2008 Infection dynamics of coexisting beta- and gammaproteobacteria in the nested endosymbiotic system of mealybugs. Appl Environ Microbiol 74 4175 4184

38. HeddiAGrenierAMKhatchadourianCCharlesHNardonP 1999 Four intracellular genomes direct weevil biology: nuclear, mitochondrial, principal endosymbiont, and Wolbachia. Proc Natl Acad Sci USA 96 6814 6819

39. DasSRadtkeAChoiY-JMendesAMValenzuelaJG 2010 Transcriptomic and functional analysis of the Anopheles gambiae salivary gland in relation to blood feeding. BMC Genomics 11 566

40. PfafflMWHorganGWDempfleL 2002 Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30 e36

41. JoehanesRNelsonJC 2008 QGene 4.0, an extensible Java QTL-analysis platform. Bioinformatics 24 2788 2789

42. CarterRRanford-CartwrightLAlanoP 1993 The culture and preparation of gametocytes of Plasmodium falciparum for immunochemical, molecular, and mosquito infectivity studies. Methods Mol Biol 21 67 88

Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

Článok vyšiel v časopise

PLOS Pathogens


2011 Číslo 5
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#