#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Reactive Oxygen Species Production and Survivorship in with Artificial Infection Types


Heterologous transinfection with the endosymbiotic bacterium Wolbachia has been shown previously to induce pathogen interference phenotypes in mosquito hosts. Here we examine an artificially infected strain of Aedes polynesiensis, the primary vector of Wuchereria bancrofti, which is the causative agent of Lymphatic filariasis (LF) throughout much of the South Pacific. Embryonic microinjection was used to transfer the wAlbB infection from Aedes albopictus into an aposymbiotic strain of Ae. polynesiensis. The resulting strain (designated “MTB”) experiences a stable artificial infection with high maternal inheritance. Reciprocal crosses of MTB with naturally infected wild-type Ae. polynesiensis demonstrate strong bidirectional incompatibility. Levels of reactive oxygen species (ROS) in the MTB strain differ significantly relative to that of the wild-type, indicating an impaired ability to regulate oxidative stress. Following a challenge with Brugia pahangi, the number of filarial worms achieving the infective stage is significantly reduced in MTB as compared to the naturally infected and aposymbiotic strains. Survivorship of MTB differed significantly from that of the wild-type, with an interactive effect between survivorship and blood feeding. The results demonstrate a direct correlation between decreased ROS levels and decreased survival of adult female Aedes polynesiensis. The results are discussed in relation to the interaction of Wolbachia with ROS production and antioxidant expression, iron homeostasis and the insect immune system. We discuss the potential applied use of the MTB strain for impacting Ae. polynesiensis populations and strategies for reducing LF incidence in the South Pacific.


Vyšlo v časopise: Reactive Oxygen Species Production and Survivorship in with Artificial Infection Types. PLoS Pathog 8(12): e32767. doi:10.1371/journal.ppat.1003075
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1003075

Souhrn

Heterologous transinfection with the endosymbiotic bacterium Wolbachia has been shown previously to induce pathogen interference phenotypes in mosquito hosts. Here we examine an artificially infected strain of Aedes polynesiensis, the primary vector of Wuchereria bancrofti, which is the causative agent of Lymphatic filariasis (LF) throughout much of the South Pacific. Embryonic microinjection was used to transfer the wAlbB infection from Aedes albopictus into an aposymbiotic strain of Ae. polynesiensis. The resulting strain (designated “MTB”) experiences a stable artificial infection with high maternal inheritance. Reciprocal crosses of MTB with naturally infected wild-type Ae. polynesiensis demonstrate strong bidirectional incompatibility. Levels of reactive oxygen species (ROS) in the MTB strain differ significantly relative to that of the wild-type, indicating an impaired ability to regulate oxidative stress. Following a challenge with Brugia pahangi, the number of filarial worms achieving the infective stage is significantly reduced in MTB as compared to the naturally infected and aposymbiotic strains. Survivorship of MTB differed significantly from that of the wild-type, with an interactive effect between survivorship and blood feeding. The results demonstrate a direct correlation between decreased ROS levels and decreased survival of adult female Aedes polynesiensis. The results are discussed in relation to the interaction of Wolbachia with ROS production and antioxidant expression, iron homeostasis and the insect immune system. We discuss the potential applied use of the MTB strain for impacting Ae. polynesiensis populations and strategies for reducing LF incidence in the South Pacific.


Zdroje

1. BurkotT, IchimoriK (2002) The PacELF programme: will mass drug administration be enough? Trends Parasitol 18: 109–115.

2. BrelsfoardCL, SechanY, DobsonSL (2008) Interspecific hybridization yields strategy for South Pacific Filariasis vector elimination. PLoS Neglect Trop D 2 (1)

e129.

3. WerrenJH, BaldoL, ClarkME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6: 741–751.

4. HilgenboeckerK, HammersteinP, SchlattmannP, TelschowA, WerrenJH (2008) How many species are infected with Wolbachia? - a statistical analysis of current data. Fems Microbiol Lett 281: 215–220.

5. TurelliM, HoffmannAA (1999) Microbe-induced cytoplasmic incompatibility as a mechanism for introducing transgenes into arthropod populations. Insect Mol Biol 8: 243–255.

6. DobsonSL (2005) Progress toward manipulating mosquito disease vector populations via releases of Wolbachia infected mosquitoes. Am J Trop Med Hyg 73: 348–348.

7. DobsonSL, FoxCW, JigginsFM (2002) The effect of Wolbachia-induced cytoplasmic incompatibility on host population size in natural and manipulated systems. Proc R Soc Lond B Biol Sci 269: 437–445.

8. HoffmannAA, MontgomeryBL, PopoviciJ, Iturbe-OrmaetxeI, JohnsonPH, et al. (2011) Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature 476: 454–U107.

9. WalkerT, JohnsonPH, MoreiraLA, Iturbe-OrmaetxeI, FrentiuFD, et al. (2011) The wMel Wolbachia strain blocks dengue and invades caged Aedes aegypti populations. Nature 476: 450–U101.

10. HedgesLM, BrownlieJC, O'NeillSL, JohnsonKN (2008) Wolbachia and virus protection in insects. Science 322: 702–702.

11. GlaserRL, MeolaMA (2010) The native Wolbachia endosymbionts of Drosophila melanogaster and Culex quinquefasciatus increase host resistance to West Nile virus infection. PLoS One 5 (8)

e11977.

12. KambrisZ, CookPE, PhucHK, SinkinsSP (2009) Immune activation by life-shortening Wolbachia and reduced filarial competence in mosquitoes. Science 326: 134–136.

13. MoreiraLA, Iturbe-OrmaetxeI, JefferyJA, LuGJ, PykeAT, et al. (2009) A Wolbachia symbiont in Aedes aegypti limits infection with dengue, chikungunya, and Plasmodium. Cell 139: 1268–1278.

14. HughesGL, KogaR, XueP, FukatsuT, RasgonJL (2011) Wolbachia infections are virulent and inhibit the human Malaria parasite Plasmodium falciparum in Anopheles gambiae. PLoS Pathog 7 (2)

e1001296.

15. BianG, XuY, LuP, XieY, XiZ (2010) The endosymbiotic bacterium Wolbachia induces resistance to Dengue virus in Aedes aegypti. PLoS Pathog 6 (4)

e1000833.

16. BrennanLJ, KeddieBA, BraigHR, HarrisHL (2008) The endosymbiont Wolbachia pipientis induces the expression of host antioxidant proteins in an Aedes albopictus cell line. PLoS One 3 (5)

e2083.

17. PanX, ZhouG, WuJ, BianG, LuP, et al. (2011) Wolbachia induces reactive oxygen species (ROS)-dependent activation of the Toll pathway to control dengue virus in the mosquito Aedes aegypti. Proc Natl Acad Sci U S A 109: E23–E31.

18. SiesH (1997) Oxidative stress: Oxidants and antioxidants. Exp Physiol 82: 291–295.

19. DeJongRJ, MillerLM, Molina-CruzA, GuptaL, KumarS, et al. (2007) Reactive oxygen species detoxification by catalase is a major determinant of fecundity in the mosquito Anopheles gambiae. Proc Natl Acad Sci U S A 104: 2121–2126.

20. MagalhaesT, BrackneyDE, BeierJC, FoyBD (2008) Silencing an Anopheles gambiae catalase and sulfhydryl oxidase increases mosquito mortality after a blood meal. Arch Insect Biochem 68: 134–143.

21. CirimotichCM, DongYM, ClaytonAM, SandifordSL, Souza-NetoJA, et al. (2011) Natural microbe-mediated refractoriness to Plasmodium infection in Anopheles gambiae. Science 332: 855–858.

22. KumarS, ChristophidesGK, CanteraR, CharlesB, HanYS, et al. (2003) The role of reactive oxygen species on Plasmodium melanotic encapsulation in Anopheles gambiae. Proc Natl Acad Sci U S A 100: 14139–14144.

23. XiZY, DobsonSL (2005) Characterization of Wolbachia transfection efficiency by using microinjection of embryonic cytoplasm and embryo homogenate. Appl Environ Microb 71: 3199–3204.

24. XiZY, KhooCCH, DobsonSL (2006) Interspecific transfer of Wolbachia into the mosquito disease vector Aedes albopictus. Proc R Soc Lond, B, Biol Sci 273: 1317–1322.

25. XiZY, KhooCCH, DobsonSL (2005) Wolbachia establishment and invasion in an Aedes aegypti laboratory population. Science 310: 326–328.

26. HaE-M, OhC-T, BaeYS, LeeW-J (2005) A direct role for dual oxidase in Drosophila gut immunity. Science 310: 847–850.

27. Molina-CruzA, DejongRJ, CharlesB, GuptaL, KumarS, et al. (2008) Reactive oxygen species modulate Anopheles gambiae immunity against bacteria and Plasmodium. J Biol Chemistry 283: 3217–3223.

28. OliveiraJHM, GoncalvesRLS, LaraFA, DiasFA, GandaraACP, et al. (2011) Blood meal-derived heme decreases ROS levels in the midgut of Aedes aegypti and allows proliferation of intestinal microbiota. PLoS Pathog 7 (3)

e1001320.

29. FuYQ, GavotteL, MercerDR, DobsonSL (2010) Artificial triple Wolbachia infection in Aedes albopictus yields a new pattern of unidirectional cytoplasmic incompatibility. Appl Environ Microb 76: 5887–5891.

30. DeanJL, DobsonSL (2004) Characterization of Wolbachia infections and interspecific crosses of Aedes (Stegomyia) polynesiensis and Ae. (Stegomyia) riversi (Diptera: Culicidae). J Med Entomol 41: 894–900.

31. XiZY, DeanJL, KhooC, DobsonSL (2005) Generation of a novel Wolbachia infection in Aedes albopictus (Asian tiger mosquito) via embryonic microinjection. Insect Biochem Molec 35: 903–910.

32. O'NeillSL, PettigrewMM, SinkinsSP, BraigHR, AndreadisTG, et al. (1997) In vitro cultivation of Wolbachia pipientis in an Aedes albopictus cell line. Insect Mol Biol 6: 33–39.

33. PoinsotD, MercotH (2001) Wolbachia injection from usual to naive host in Drosophila simulans (Diptera: Drosophilidae). Eur J Entomol 98: 25–30.

34. RieglerM, CharlatS, StaufferC, MercotH (2004) Wolbachia transfer from Rhagoletis cerasi to Drosophila simulans: Investigating the outcomes of host-symbiont coevolution. Appl Environ Microb 70: 273–279.

35. DuttonTJ, SinkinsSP (2004) Strain-specific quantification of Wolbachia density in Aedes albopictus and effects of larval rearing conditions. Insect Mol Biol 13: 317–322.

36. Graca-SouzaAV, Maya-MonteiroC, Paiva-SilvaGO, BrazGRC, PaesMC, et al. (2006) Adaptations against heme toxicity in blood-feeding arthropods. Insect Biochem Molec 36: 322–335.

37. BrownlieJC, CassBN, RieglerM, WitsenburgJJ, Iturbe-OrmaetxeI, et al. (2009) Evidence for metabolic provisioning by a common invertebrate endosymbiont, Wolbachia pipientis, during periods of nutritional stress. PLoS Pathog 5 (4)

e1000368.

38. KremerN, VoroninD, CharifD, MavinguiP, MollereauB, et al. (2009) Wolbachia interferes with ferritin expression and iron metabolism in insects. PLoS Pathog 5 (10)

e1000630.

39. NicholH, LawJH, WinzerlingJJ (2002) Iron metabolism in insects. Annu Rev Entomol 47: 535–559.

40. ZhouGL, KohlheppP, GeiserD, FrasquilloMDC, Vazquez-MorenoL, et al. (2007) Fate of blood meal iron in mosquitoes. J Insect Physiol 53: 1169–1178.

41. SchaibleME, KaufmannSHE (2004) Iron and microbial infection. Nat Rev Microbiol 2: 946–953.

42. GeiserDL, ChavezCA, Flores-MunguiaR, WinzerlingJJ, PhamDQD (2003) Aedes aegypti ferritin - A cytotoxic protector against iron and oxidative challenge? Eur J Biochem 270: 3667–3674.

43. PhamDQD, DouglassPL, ChavezCA, ShafferJJ (2005) Regulation of the ferritin heavy-chain homologue gene in the yellow fever mosquito, Aedes aegypti. Insect Mol Biol 14: 223–236.

44. PhamDQD, WinzerlingJJ (2010) Insect ferritins: Typical or atypical? BBA-Gen Subjects 1800: 824–833.

45. HaEM, LeeKA, SeoYY, KimSH, LimJH, et al. (2009) Coordination of multiple dual oxidase-regulatory pathways in responses to commensal and infectious microbes in Drosophila gut. Nat Immunol 10: 949–U919.

46. KumarS, Molina-CruzA, GuptaL, RodriguesJ, Barillas-MuryC (2010) A peroxidase/dual oxidase system modulates midgut epithelial immunity in Anopheles gambiae. Science 327: 1644–1648.

47. MeitzlerJL, de MontellanoPRO (2009) Caenorhabditis elegans and human dual oxidase 1 (DUOX1) “peroxidase” domains: Insights into heme binding and catalytic activity. J Biol Chem 284: 18634–18643.

48. JeneyV, BallaJ, YachieA, VargaZ, VercellottiGM, et al. (2002) Pro-oxidant and cytotoxic effects of circulating heme. Blood 100: 879–887.

49. FosterJ, GanatraM, KamalI, WareJ, MakarovaK, et al. (2005) The Wolbachia genome of Brugia malayi: Endosymbiont evolution within a human pathogenic nematode. PLoS Biol 3: 599–614.

50. GhedinE, WangSL, SpiroD, CalerE, ZhaoQ, et al. (2007) Draft genome of the filarial nematode parasite Brugia malayi. Science 317: 1756–1760.

51. WuB, NovelliJ, FosterJ, VaisvilaR, ConwayL, et al. (2009) The heme biosynthetic pathway of the obligate Wolbachia endosymbiont of Brugia malayi as a potential anti-filarial drug target. PLoS Neglect Trop D 3 (7)

e475.

52. GoncalvesRLS, MachadoACL, Paiva-SilvaGO, SorgineMHF, MomoliMM, et al. (2009) Blood-feeding induces reversible functional changes in flight muscle mitochondria of Aedes aegypti mosquito. PLoS One 4 (11)

e7854.

53. DuttonTJ, SinkinsSP (2005) Filarial susceptibility and effects of Wolbachia in Aedes pseudoscutellaris mosquitoes. Med Vet Entomol 19: 60–65.

54. BrelsfoardCL, DobsonSL (2011) Wolbachia effects on host fitness and the influence of male aging on cytoplasmic incompatibility in Aedes polynesiensis (Diptera: Culicidae). J Med Entomol 48: 1008–1015.

55. McMenimanCJ, LaneRV, CassBN, FongAWC, SidhuM, et al. (2009) Stable introduction of a life-shortening Wolbachia infection into the mosquito Aedes aegypti. Science 323: 141–144.

56. SuhE, MercerDR, FuYQ, DobsonSL (2009) Pathogenicity of life-shortening Wolbachia in Aedes albopictus after transfer from Drosophila melanogaster. Appl Environ Microb 75: 7783–7788.

57. HiebWF, StokstadEL, RothsteiM (1970) Heme requirement for reproduction of a free-living nematode. Science 168: 143–144.

58. RaoAU, CartaLK, LesuisseE, HamzaI (2005) Lack of heme synthesis in a free-living eukaryote. Proc Natl Acad Sci U S A 102: 4270–4275.

59. FaillouxAB, ChanteauS, ChungueE, LonckeS, SechanY (1991) Oral Infection of Aedes polynesiensis by Wuchereria bancrofti by using Parafilm membrane feeding. J Am Mosquito Contr 7: 660–662.

60. GublerDJ, InuiTS, BlackHR, BhattachNC (1973) Comparisons of microfilaria density in blood sampled by finger-prick, venipuncture and ingestion by mosquitoes. Am J Trop Med Hyg 22: 174–178.

61. LowrieRC, EberhardML, LammiePJ, RaccurtCP, KatzSP, et al. (1989) Uptake and development of Wuchereria bancrofti in Culex quinquefasciatus that fed on Haitian carriers with different microfilaria densities. Am J Trop Med Hyg 41: 429–429.

62. HockmeyerWT, SchieferBA, RedingtonBC, EldridgeBF (1975) Brugia pahangi - effects upon flight capability of Aedes aegypti. Exp Parasitol 38: 1–5.

63. PerroneJB, SpielmanA (1986) Microfilarial perforation of the midgut of a mosquito. J Parasitol 72: 723–727.

64. BerryWJ, RowleyWA, ChristensenBM (1986) Influence of developing Brugia pahangi on spontaneous flight activity of Aedes aegypti (Diptera, Culicidae). J Med Entomol 23: 441–445.

65. IbrahimMS, TrpisM (1987) The effect of Brugia pahangi infection on survival of susceptible and refractory species of the Aedes scutellaris complex. Med Vet Entomol 1: 329–337.

66. HarringtonLC, EdmanJD, ScottTW (2001) Why do female Aedes aegypti (Diptera: Culicidae) feed preferentially and frequently on human blood? J Med Entomol 38: 411–422.

67. ScottTW, NaksathitA, DayJF, KittayapongP, EdmanJD (1997) A fitness advantage for Aedes aegypti and the viruses it transmits when females feed only on human blood. Am J Trop Med Hyg 57: 235–239.

68. StyerLM, MinnickSL, SunAK, ScottTW (2007) Mortality and reproductive dynamics of Aedes aegypti (Diptera: Culicidae) fed human blood. Vector-Borne Zoonot 7: 86–98.

69. HancockPA, SinkinsSP, GodfrayHCJ (2011) Strategies for introducing Wolbachia to reduce transmission of mosquito-borne diseases. PLoS Neglect Trop D 5 (4)

e1024.

70. SinkinsSP, BraigHR, OneillSL (1995) Wolbachia superinfections and the expression of cytoplasmic incompatibility. P Roy Soc B-Biol Sci 261: 325–330.

71. PlichartC, LegrandAM (2005) Detection and characterization of Wolbachia infections in Wuchereria bancrofti (Spirurida: Onchocercidae) var. pacifica and Aedes (stegomyia) polynesiensis (Diptera: Culicidae). Am J Trop Med Hyg 73: 354–358.

72. ZhouWG, RoussetF, O'NeillS (1998) Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. P Roy Soc B-Biol Sci 265: 509–515.

73. BenjaminiY, HochbergY (1995) Controlling the false discovery rate - a practical and powerful approach to multiple testing. J Roy Stat Soc B Met 57: 289–300.

Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

Článok vyšiel v časopise

PLOS Pathogens


2012 Číslo 12
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#