Wolbachia: Can we save lives with a great pandemic?

Trends in Parasitology

Volumn 29, Issue 8, 2013, Pages 385-393

  LePage, Daniel ^a   Bordenstein, Seth R ^a  

^a VANDERBILT UNIVERSITY   (United States)

Author keywords

Filarial disease; Vector control; Wolbachia pipientis

Indexed keywords

ANTIFILARIAL AGENT; DNA; DOXYCYCLINE; INSECTICIDE; IVERMECTIN;

AEDES AEGYPTI; AFRICAN TRYPANOSOMIASIS; ANTIBIOTIC RESISTANCE; BACTERIAL INFECTION; BACTERIOPHAGE; CHIKUNGUNYA; CHIKUNGUNYA ALPHAVIRUS; CYTOLOGY; CYTOPLASM; DENGUE; DENGUE VIRUS; DISEASE CARRIER; DISEASE TRANSMISSION; DROSOPHILA MELANOGASTER; DRUG TARGETING; FERTILIZATION; FILARIASIS; GENOME; GENOMICS; GLOSSINIDAE; HORIZONTAL GENE TRANSFER; HOST PARASITE INTERACTION; HUMAN; INFECTION CONTROL; LYMPHATIC FILARIASIS; MALARIA; MOSQUITO; NEMATODE; NONHUMAN; ONCHOCERCIASIS; PANDEMIC; PROTEIN PROTEIN INTERACTION; REPRODUCTION; REVIEW; TRYPANOSOMA; VECTOR CONTROL; WOLBACHIA PIPIENTIS;

FILARIAL DISEASE; VECTOR CONTROL; WOLBACHIA PIPIENTIS;

ANIMALS; CULICIDAE; FEMALE; FILARIASIS; HUMANS; INSECT VECTORS; MALE; NEMATODA; PANDEMICS; PEST CONTROL, BIOLOGICAL; REPRODUCTION; WOLBACHIA; WORLD HEALTH;

ANIMALIA; BACTERIA (MICROORGANISMS); INVERTEBRATA; WOLBACHIA; WOLBACHIA PIPIENTIS;

EID: 84880953819     PISSN: 14714922     EISSN: 14715007     Source Type: Journal    
DOI: 10.1016/j.pt.2013.06.003     Document Type: Review

References (111)

1. Zug R., Hammerstein P. Still a host of hosts for Wolbachia: analysis of recent data suggests that 40% of terrestrial arthropod species are infected. PLoS ONE 2012, 7:e38544.
2. Ferri E., et al. New insights into the evolution of Wolbachia infections in filarial nematodes inferred from a large range of screened species. PLoS ONE 2011, 6:e20843.
3. Le Clec'h W., et al. Cannibalism and predation as paths for horizontal passage of Wolbachia between terrestrial isopods. PLoS ONE 2013, 8:e60232.
4. Frydman H.M., et al. Somatic stem cell niche tropism in Wolbachia. Nature 2006, 441:509-512.
5. Iturbe-Ormaetxe I., et al. Wolbachia and the biological control of mosquito-borne disease. EMBO Rep. 2011, 12:508-518.
6. Van den Hurk A.F., et al. Impact of Wolbachia on infection with chikungunya and yellow fever viruses in the mosquito vector Aedes aegypti. PLoS Negl. Trop. Dis. 2012, 6:e1892.
7. Melnikow E., et al. A potential role for the interaction of Wolbachia surface proteins with the Brugia malayi glycolytic enzymes and cytoskeleton in maintenance of endosymbiosis. PLoS Negl. Trop. Dis. 2013, 7:e2151.
8. Darby A.C., et al. Analysis of gene expression from the Wolbachia genome of a filarial nematode supports both metabolic and defensive roles within the symbiosis. Genome Res. 2012, 22:2467-2477.
9. Serbus L.R., et al. The genetics and cell biology of Wolbachia-host interactions. Annu. Rev. Genet. 2008, 42:683-707.
10. Ghelelovitch S. Genetic determinism of sterility in the cross-breeding of various strains of Culex autogenicus. C. R. Hebd Seances Acad. Sci. 1952, 234:2386-2388.
11. Alam U., et al. Wolbachia symbiont infections induce strong cytoplasmic incompatibility in the tsetse fly Glossina morsitans. PLoS Pathog. 2011, 7:e1002415.
12. Sarasa J., et al. Wolbachia induced cytogenetical effects as evidenced in Chorthippus parallelus (Orthoptera). Cytogenet. Genome Res. 2013, 139:36-43.
13. Tram U., et al. Paternal chromosome segregation during the first mitotic division determines Wolbachia-induced cytoplasmic incompatibility phenotype. J. Cell Sci. 2006, 119:3655-3663.
14. Tram U. Role of delayed nuclear envelope breakdown and mitosis in Wolbachia-induced cytoplasmic incompatibility. Science 2002, 296:1124-1126.
15. Landmann F., et al. Wolbachia-mediated cytoplasmic incompatibility is associated with impaired histone deposition in the male pronucleus. PLoS Pathog. 2009, 5:e1000343.
16. Callaini G., et al. Wolbachia-induced delay of paternal chromatin condensation does not prevent maternal chromosomes from entering anaphase in incompatible crosses of Drosophila simulans. J. Cell Sci. 1997, 110:271-280.
17. Lassya C.W., Karrb T.L. Cytological analysis of fertilization and early embryonic development incompatible crosses of Drosophila simulans. Mech. Dev. 1996, 57:47-58.
18. Takada S., et al. Drosophila checkpoint kinase 2 couples centrosome function and spindle assembly to genomic integrity. Cell 2003, 113:87-99.
19. Werren J.H. Biology of Wolbachia. Annu. Rev. Entomol. 1997, 42:587-609.
20. Poinsot D., et al. On the mechanism of Wolbachia-induced cytoplasmic incompatibility: confronting the models with the facts. Bioessays 2003, 25:259-265.
21. Ferree P.M., Sullivan W. A genetic test of the role of the maternal pronucleus in Wolbachia-induced cytoplasmic incompatibility in Drosophila melanogaster. Genetics 2006, 173:839-847.
22. Duron O., et al. Rapid evolution of Wolbachia incompatibility types. Proc. R. Soc. B: Biol. Sci. 2012, 279:4473-4480.
23. Zabalou S., et al. Multiple rescue factors within a Wolbachia strain. Genetics 2008, 178:2145-2160.
24. Poinsot D., et al. Wolbachia transfer from Drosophila melanogaster into D. simulans: host effect andcytoplasmic incompatibility relationships. Genetics 1998, 150:227-237.
25. Bossan B., et al. A new model and method for understanding Wolbachia-induced cytoplasmic incompatibility. PLoS ONE 2011, 6:e19757.
26. Bourtzis K., et al. Wolbachia infection and cytoplasmic incompatibility in Drosophila species. Genetics 1996, 144:1063-1073.
27. Sinkins S.P., et al. Wolbachia pipientis: bacterial density and unidirectional cytoplasmic incompatibilty between infected populations of Aedes albopictus. Exp. Parasitol. 1995, 81:284-291.
28. Zheng Y., et al. Wolbachia-induced cytoplasmic incompatibility is associated with decreased Hira expression in male Drosophila. PLoS ONE 2011, 6:e19512.
29. Yamada R., et al. Functional test of the influence of Wolbachia genes on cytoplasmic incompatibility expression in Drosophila melanogaster. Insect Mol. Biol. 2011, 20:75-85.
30. Papafotiou G., et al. Regulation of Wolbachia ankyrin domain encoding genes in Drosophila gonads. Res. Microbiol. 2011, 162:764-772.
31. Duron O., et al. Variability and expression of ankyrin domain genes in Wolbachia variants infecting the mosquito Culex pipiens. J. Bacteriol. 2007, 189:4442-4448.
32. Brennan L.J., et al. Disruption of redox homeostasis leads to oxidative DNA damage in spermatocytes of Wolbachia-infected Drosophila simulans. Insect Mol. Biol. 2012, 21:510-520.
33. Zhu L-Y., et al. Wolbachia strengthens cardinium-induced cytoplasmic incompatibility in the spider mite Tetranychus piercei McGregor. Curr. Microbiol. 2012, 65:516-523.
34. Penz T., et al. Comparative genomics suggests an independent origin of cytoplasmic incompatibility in Cardinium hertigii. PLoS Genet. 2012, 8:e1003012.
35. Riparbelli M.G., et al. Wolbachia-mediated male killing is associated with defective chromatin remodeling. PLoS ONE 2012, 7:e30045.
36. Sasaki T., et al. Wolbachia variant that induces two distinct reproductive phenotypes in different hosts. Heredity 2005, 95:389-393.
37. Jaenike J. Spontaneous emergence of a new Wolbachia phenotype. Evolution 2007, 61:2244-2252.
38. Veneti Z., et al. Loss of reproductive parasitism following transfer of male-killing Wolbachia to Drosophila melanogaster and Drosophila simulans. Heredity 2012, 109:306-312.
39. Hurst G.D., et al. Male-killing Wolbachia in Drosophila: a temperature-sensitive trait with a threshold bacterial density. Genetics 2000, 156:699-709.
40. Moreira L., et al. A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium. Cell 2009, 139:1268-1278.
41. Glaser R.L., Meola M. The native Wolbachia endosymbionts of Drosophila melanogaster and Culex quinquefasciatus increase host resistance to West Nile virus infection. PLoS ONE 2010, 5:e11977.
42. Wong Z.S., et al. Wolbachia-mediated antibacterial protection and immune gene regulation in Drosophila. PLoS ONE 2011, 6:e25430.
43. Hughes G.L., et al. Wolbachia strain wAlbB enhances infection by the rodent malaria parasite Plasmodium berghei in Anopheles gambiae mosquitoes. Appl. Environ. Microbiol. 2012, 78:1491-1495.
44. O'Connor L., et al. Open release of male mosquitoes infected with a Wolbachia biopesticide: field performance and infection containment. PLoS Negl. Trop. Dis. 2012, 6:e1797.
45. Apostolaki A., et al. Transinfection of the olive fruit fly Bactrocera oleae with Wolbachia: towards a symbiont-based population control strategy. J. Appl. Entomol. 2011, 135:546-553.
46. Atyame C.M., et al. Cytoplasmic incompatibility as a means of controlling Culex pipiens quinquefasciatus mosquito in the islands of the south-western Indian Ocean. PLoS Negl. Trop. Dis. 2011, 5:e1440.
47. Schraiber J.G., et al. Constraints on the use of lifespan-shortening Wolbachia to control dengue fever. J. Theor. Biol. 2012, 297:26-32.
48. McMeniman C.J., et al. Stable introduction of a life-shortening Wolbachia infection into the mosquito Aedes aegypti. Science 2009, 323:141-144.
49. Walker T., et al. The wMel Wolbachia strain blocks dengue and invades caged Aedes aegypti populations. Nature 2011, 476:450-453.
50. Hoffmann A.A., et al. Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature 2011, 476:454-457.
51. Bhatt S., et al. The global distribution and burden of dengue. Nature 2013, 496:504-507.
52. Kambris Z., et al. Wolbachia stimulates immune gene expression and inhibits plasmodium development in Anopheles gambiae. PLoS Pathog. 2010, 6:e1001143.
53. Jin C., et al. The virulent Wolbachia strain wMelPop efficiently establishes somatic infections in the malaria vector Anopheles gambiae. Appl. Environ. Microbiol. 2009, 75:3373-3376.
54. Bian G., et al. Wolbachia invades Anopheles stephensi populations and induces refractoriness to Plasmodium infection. Science 2013, 340:748-751.
55. Osei-Poku J., et al. Identification of Wolbachia strains in mosquito disease vectors. PLoS ONE 2012, 7:e49922.
56. Meriweather M., et al. A 454 survey reveals the community composition and core microbiome of the common bed bug (Cimex lectularius) across an urban landscape. PLoS ONE 2013, 8:e61465.
57. Doudoumis V., et al. Tsetse-Wolbachia symbiosis: comes of age and has great potential for pest and disease control. J. Invertebr. Pathol. 2012, 112:S94-S103.
58. Teixeira L., et al. The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol. 2008, 6:e2.
59. Hedges L.M., et al. Wolbachia and virus protection in insects. Science 2008, 322:702.
60. Kamalakannan V., et al. Wolbachia heat shock protein 60 induces pro-inflammatory cytokines and apoptosis in monocytes in vitro. Microbes Infect. 2012, 14:610-618.
61. Pinto S.B., et al. Wolbachia surface protein induces innate immune responses in mosquito cells. BMC Microbiol. 2012, 12(Suppl. 1):S11.
62. Frentiu F.D., et al. Wolbachia-mediated resistance to dengue virus infection and death at the cellular level. PLoS ONE 2010, 5:e13398.
63. Rancès E., et al. The relative importance of innate immune priming in Wolbachia-mediated dengue interference. PLoS Pathog. 2012, 8:e1002548.
64. Pan X., et al. 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. 2012, 109:E23-E31.
65. Hedges L.M., et al. The small interfering RNA pathway is not essential for Wolbachia-mediated antiviral protection in Drosophila melanogaster. Appl. Environ. Microbiol. 2012, 78:6773-6776.
66. Osborne S.E., et al. Antiviral protection and the importance of Wolbachia density and tissue tropism in Drosophila simulans. Appl. Environ. Microbiol. 2012, 78:6922-6929.
67. Longdon B., et al. Male-killing Wolbachia do not protect Drosophila bifasciata against viral infection. BMC Microbiol. 2012, 12(Suppl. 1):S8.
68. Graham R.I., et al. Wolbachia in a major African crop pest increases susceptibility to viral disease rather than protects. Ecol. Lett. 2012, 15:993-1000.
69. Hussain M., et al. Wolbachia uses host microRNAs to manipulate host gene expression and facilitate colonization of the dengue vector Aedes aegypti. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:9250-9255.
70. Osei-Amo S., et al. Wolbachia-induced aae-miR-12 miRNA negatively regulates the expression of MCT1 and MCM6 genes in Wolbachia-infected mosquito cell line. PLoS ONE 2012, 7:e50049.
71. Zhang G., et al. Wolbachia uses a host microRNA to regulate transcripts of a methyltransferase, contributing to dengue virus inhibition in Aedes aegypti. Proc. Natl. Acad. Sci. U.S.A. 2013, 108:9250-9255.
72. Saint André A.V., et al. The role of endosymbiotic Wolbachia bacteria in the pathogenesis of river blindness. Science 2002, 295:1892-1895.
73. Taylor M.J., et al. Wolbachia filarial interactions. Cell. Microbiol. 2012, 10.1111/cmi.12084.
74. Foster J., et al. The Wolbachia genome of Brugia malayi: endosymbiont evolution within a human pathogenic nematode. PLoS Biol. 2005, 3:e121.
75. Ghedin E., et al. Draft genome of the filarial nematode parasite Brugia malayi. Science 2007, 317:1756-1760.
76. Hosokawa T., et al. Wolbachia as a bacteriocyte-associated nutritional mutualist. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:769-774.
77. Fenn K., Blaxter M. Quantification of Wolbachia bacteria in Brugia malayi through the nematode lifecycle. Mol. Biochem. Parasitol. 2004, 137:361-364.
78. Fischer K., et al. Tissue and stage-specific distribution of Wolbachia in Brugia malayi. PLoS Negl. Trop. Dis. 2011, 5:e1174.
79. McGarry H.F., et al. Population dynamics of Wolbachia bacterial endosymbionts in Brugia malayi. Mol. Biochem. Parasitol. 2004, 135:57-67.
80. Landmann F., et al. Asymmetric Wolbachia segregation during early Brugia malayi embryogenesis determines its distribution in adult host tissues. PLoS Negl. Trop. Dis. 2010, 4:e758.
81. Landmann F., et al. Both asymmetric mitotic segregation and cell-to-cell invasion are required for stable germline transmission of Wolbachia in filarial nematodes. Biol. Open 2012, 1:536-547.
82. Voronin D., et al. Autophagy regulates Wolbachia populations across diverse symbiotic associations. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:E1638-E1646.
83. Dunning Hotopp J.C., et al. Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 2007, 317:1753-1756.
84. Brelsfoard C., Dobson S. Wolbachia effects on hostfitness and the influence of male aging on cytoplasmic incompatibility in Aedes polynesiensis. J. Med. Entomol. 2011, 48:1008-1015.
85. Almeida F., et al. Effects of Wolbachia on fitness of Culex quinquefasciatus (Diptera; Culicidae). Infect Genet. Evol. 2011, 11:2138-2143.
86. Zhang H., et al. Population dynamics of noncytoplasmic incompatibility-inducing Wolbachia in Nilaparvata lugens and its effects on host adult life span and female fitness. Environ. Entomol. 2010, 39:1801-1809.
87. Turley A.P., et al. Transinfected Wolbachia have minimal effects on male reproductive success in Aedes aegypti. Parasit. Vectors 2013, 6:36.
88. Lewis Z., et al. Wolbachia infection lowers fertile sperm transfer in a moth. Biol. Lett. 2011, 7:187-189.
89. Chen S-J., et al. Identification and biological role of the endosymbionts Wolbachia in rice water weevil (Coleoptera: Curculionidae). Environ. Entomol. 2012, 41:469-477.
90. Dedeine F., et al. Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:6247-6252.
91. Fast E.M., et al. Wolbachia enhance Drosophila stem cell proliferation and target the germline stem cell niche. Science 2011, 334:990-992.
92. Weeks A.R., et al. From parasite to mutualist: rapid evolution of Wolbachia in natural populations of Drosophila. PLoS Biol. 2007, 5:e114.
93. Landmann F., et al. Anti-filarial activity of antibiotic therapy is due to extensive apoptosis after Wolbachia depletion from filarial nematodes. PLoS Pathog. 2011, 7:e1002351.
94. Slatko B.E., et al. The Wolbachia endosymbiont as an anti-filarial nematode target. Symbiosis 2010, 51:55-65.
95. Desjardins C.A., et al. Genomics of Loa loa, a Wolbachia-free filarial parasite of humans. Nat. Genet. 2013, 45:495-500.
96. Wu B., et al. The heme biosynthetic pathway of the obligate Wolbachia endosymbiont of Brugia malayi as a potential anti-filarial drug target. PLoS Negl. Trop. Dis. 2009, 3:e475.
97. +-dependent DNA ligase from Wolbachia endosymbiont of lymphatic filarial parasite Brugia malayi. PLoS ONE 2012, 7:e41113.
98. Palayam M., et al. Preliminary analysis to target pyruvate phosphate dikinase from Wolbachia endosymbiont of Brugia malayi for desiging anti-filarial agents. Interdiscip. Sci. 2012, 4:74-82.
99. Li Z., et al. Targeting the Wolbachia cell division protein FtsZ as a new approach for antifilarial therapy. PLoS Negl. Trop. Dis. 2011, 5:e1411.
100. Schiefer A., et al. The ClpP peptidase of Wolbachia endobacteria is a novel target for drug development against filarial infections. J. Antimicrob. Chemother. 2013, 10.1093/jac/dkt105.
101. Sharma R., et al. Filamentation temperature-sensitive protein Z (FtsZ) of Wolbachia, endosymbiont of Wuchereria bancrofti: a potential target for anti-filarial chemotherapy. Acta Trop. 2013, 125:330-338.
102. Johnston K.L., et al. Lipoprotein biosynthesis as a target for anti-Wolbachia treatment of filarial nematodes. Parasit. Vectors 2010, 3:99.
103. Gayen P., et al. A double-blind controlled field trial of doxycycline and albendazole in combination for the treatment of bancroftian filariasis in India. Acta Trop. 2013, 125:150-156.
104. Sjölund M., et al. Persistence of resistant Staphylococcus epidermidis after single course of clarithromycin. Emerg. Infect. Dis. 2005, 11:1389-1393.
105. Jernberg C., et al. Long-term ecological impacts of antibiotic administration on the human intestinal microbiota. ISME J. 2007, 1:56-66.
106. Dugan J., et al. Tetracycline resistance in Chlamydia suis mediated by genomic islands inserted into the chlamydial inv-like gene. Antimicrob. Agents Chemother. 2004, 48:3989-3995.
107. Nag J.K., et al. Recombinant translation initiation factor-1 of Wolbachia is an immunogenic excretory secretory protein that elicits Th2 mediated immune protection against Brugia malayi. Comp. Immunol. Microbiol. Infect. Dis. 2013, 36:25-38.
108. Scott A.L., et al. Filarial and Wolbachia genomics. Parasite Immunol. 2013, 34:121-129.
109. Mavingui P., et al. Whole-genome sequence of Wolbachia strain wAlbB, an endosymbiont of tiger mosquito vector Aedes albopictus. J. Bacteriol. 2012, 194:1840.
110. Maren Ellegaard K., et al. Comparative genomics of Wolbachia and the bacterial species concept. PLoS Genet. 2013, 9:e1003381.
111. Metcalf J.A., Bordenstein S.R. The complexity of virus systems: the case of endosymbionts. Curr. Opin. Microbiol. 2012, 15:546-552.