Drosophila melanogaster brain invasion: Pathogenic Wolbachia in central nervous system of the fly

Insect Science

Volumn 23, Issue 2, 2016, Pages 253-264

  Strunov, Anton ^a   Kiseleva, Elena ^a  

^a INSTITUTE OF CYTOLOGY AND GENETICS   (Russian Federation)

Author keywords

Bacterial morphology dynamics; Brain; Drosophila melanogaster; Electron microscopy; Pathogenic endosymbiont; Wolbachia strain wMelPop

Indexed keywords

ANIMAL; BRAIN; DROSOPHILA MELANOGASTER; FEMALE; GLIA; MICROBIOLOGY; NERVE CELL; PHYSIOLOGY; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; WOLBACHIA;

ANIMALS; BRAIN; DROSOPHILA MELANOGASTER; FEMALE; MICROSCOPY, ELECTRON, TRANSMISSION; NEUROGLIA; NEURONS; WOLBACHIA;

EID: 84961198793     PISSN: 16729609     EISSN: 17447917     Source Type: Journal    
DOI: 10.1111/1744-7917.12187     Document Type: Article

References (43)

1. Albertson, R., Casper-Lindley, C., Cao, J., Tram, U. and Sullivan, W. (2009) Symmetric and asymmetric mitotic segregation patterns influence Wolbachia distribution in host somatic tissue. Journal of Cell Science, 122, 4570-4583.
2. Albertson, R., Tan, V., Leads, R.R., Reyes, M., Sullivan, W. and Casper-Lindley, C. (2013) Mapping Wolbachia distributions in the adult Drosophila brain. Cellular Microbiology, 15, 1527-1544.
3. Bian, G., Joshi, D., Dong, Y., Lu, P., Zhou, G., Pan, X., Xu, Y., Dimopoulos, G. and Xi, Z. (2013) Wolbachia invades Anopheles stephensi populations and induces refractoriness to Plasmodium infection. Science, 340, 748-751.
4. Braig, H.R., Zhou, W., Dobson, S.L. and O'Neill, S.L. (1998) Cloning and characterization of a gene encoding the major surface protein of the bacterial endosymbiont Wolbachia pipientis. Journal of Bacteriology, 180, 2373-2378.
5. Callaini, G., Riparbelli, M.G. and Dallai, R. (1994) The distribution of cytoplasmic bacteria in the early Drosophila embryo is mediated by astral microtubules. Journal of Cell Science, 107, 673-682.
6. Chrostek, E., Marialva, M.S., Esteves, S.S., Weinert, L.A., Martinez, J., Jiggins, F.M. and Teixeira, L. (2013) Wolbachia variants induce differential protection to viruses in Drosophila melanogaster: A phenotypic and phylogenomic analysis. PLoS Genetics, 9, e1003896.
7. de Crespigny, F.E., Pitt, T.D. and Wedell, N. (2006) Increased male mating rate in Drosophila is associated with Wolbachia infection. Journal of Evolutionary Biology, 19, 1964-1972.
8. Dobson, S.L., Bourtzis, K., Braig, H.R., Jones, B.F., Zhou, W., Rousset, F. and O'Neill, S.L. (1999) Wolbachia infections are distributed throughout insect somatic and germ line tissues. Insect Biochemistry and Molecular Biology, 29, 153-160.
9. Dons, L., Jin, Y., Kristensson, K. and Rottenberg, M.E. (2007) Axonal transport of Listeria monocytogenes and nerve-cell-induced bacterial killing. Journal of Neuroscience Research, 85, 2529-2537.
10. Eleftherianos, I., Atri, J., Accetta, J. and Castillo, J.C. (2013) Endosymbiotic bacteria in insects: guardians of the immune system? Frontiers in Physiology, 4, 46, 1-10.
11. Fast, E.M., Toomey, M.E., Panaram, K., Desjardins, D., Kolaczyk, E.D. and Frydman, H.M. (2011) Wolbachia enhance Drosophila stem cell proliferation and target the germline stem cell niche. Science, 334, 990-992.
12. Ferree, P.M., Frydman, H.M., Li, J.M., Cao, J., Wieschaus, E. and Sullivan, W. (2005) Wolbachia utilizes host microtubules and dynein for anterior localization in the Drosophila oocyte. PLoS Pathogens, 1, e14.
13. Fischer, K., Beatty, W.L., Weil, G.J. and Fischer, P.U. (2014) High pressure freezing/freeze substitution fixation improves the ultrastructural assessment of Wolbachia endosymbiont-filarial nematode host interaction. PLoS ONE, 9, e86383.
14. Frydman, H.M., Li, J.M., Robson, D.N. and Wieschaus, E. (2006) Somatic stem cell niche tropism in Wolbachia. Nature, 441, 509-512.
15. Hannah, A.M. (1949) Proceedings of the 8th International Congress of Genetics (Hereditas Suppl Vol.) Stockholm. Radiation mutations involving the cut locus in Drosophila, pp. 588-589.
16. Hayes, S.F. and Burgdorfer, W. (1982) Reactivation of Rickettsia rickettsii in Dermacentor andersoni ticks: an ultrastructural analysis. Infection and Immunity, 37, 779-785.
17. Hoffmann, A.A., Montgomery, B.L., Popovici, J., Iturbe-Ormaetxe, I., Johnson, P.H., Muzzi, F., Greenfield, M., Durkan, M., Leong, Y.S., Dong, Y., Cook, H., Axford, J., Callahan, A.G., Kenny, N., Omodei, C., McGraw, E.A., Ryan, P.A., Ritchie, S.A., Turelli, M. and O'Neill, S.L. (2011) Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature, 476, 454-457.
18. Karlberg, E.O. and Andersson, S.G. (2003) Mitochondrial gene history and mRNA localization: is there a correlation? Nature Reviews Genetics, 4, 391-397.
19. Koukou, K., Pavlikaki, H., Kilias, G., Werren, J.H., Bourtzis, K. and Alahiotis, S.N. (2006) Influence of antibiotic treatment and Wolbachia curing on sexual isolation among Drosophila melanogaster cage populations. Evolution, 60, 87-96.
20. Kozek, W.J. (2005) What is new in the Wolbachia/Dirofilaria interaction? Veterinary Parasitology, 133, 127-132.
21. Landmann, F., Bain, O., Martin, C., Uni, S., Taylor, M.J. and Sullivan, W. (2012) Both asymmetric mitotic segregation and cell-to-cell invasion are required for stable germline transmission of Wolbachia in filarial nematodes. Biology Open, 1, 536-547.
22. Lane, N.J. (1985) Structure of components of the nervous system. Comprehensive Insect Physiology, Biochemistry and Pharmacology (eds. G.A. Kerkut & L.I. Gilbert ), Vol. 5, pp 1-47, Pergamon, Oxford.
23. Louis, C. and Nigro, L. (1989) Ultrastructural evidence of Wolbachia Rickettsiales in Drosophila simulans and their relationship with unidirectional cross-incompatibility. Journal of Invertebrate Pathology, 54, 34 - 44.
24. McGraw, E.A., Merritt, D.J., Droller, J.N. and O'Neill, S.L. (2002) Wolbachia density and virulence attenuation after transfer into a novel host. Proceedings of the National Academy of Sciences of the United States of America, 99, 2918-2923.
25. McGraw, E.A. and O'Neill, S.L. (2013) Beyond insecticides: new thinking on an ancient problem. Nature Reviews Microbiology, 11, 181-193.
26. Miller, W.J., Ehrman, L. and Schneider, D. (2010) Infectious speciation revisited: impact of symbiont-depletion on female fitness and mating behavior of Drosophila paulistorum. PLoS Pathogens, 6, e1001214.
27. Min, K.T. and Benzer, S. (1997) Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. Proceedings of the National Academy of Sciences of the United States of America, 94, 10792-10796.
28. Moreira, L.A., Iturbe-Ormaetxe, I., Jeffery, J.A., Lu, G., Pyke, A.T., Hedges, L.M., Rocha, B.C., Hall-Mendelin, S., Day, A., Riegler, M., Hugo, L.E., Johnson, K.N., Kay, B.H., McGraw, E.A., van den Hurk, A.F., Ryan, P.A. and O'Neill, S.L. (2009a) A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium. Cell, 139, 1268-1278.
29. Moreira, L.A., Saig, E., Turley, A.P., Ribeiro, J.M., O'Neill, S.L. and McGraw, E.A. (2009b) Human probing behavior of Aedes aegypti when infected with a life-shortening strain of Wolbachia. PLoS Neglected Tropical Diseases, 3, e568.
30. O'Neill, S.L., Giordano, R., Colbert, A.M., Karr, T.L. and Robertson, H.M. (1992) 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proceedings of the National Academy of Sciences of the United States of America, 89, 2699-2702.
31. Peng, Y., Nielsen, J.E., Cunningham, J.P. and McGraw, E.A. (2008) Wolbachia infection alters olfactory-cued locomotion in Drosophila spp. Applied and Environmental Microbiology, 74, 3943-3948.
32. Roy, C.R. (2002) Exploitation of the endoplasmic reticulum by bacterial pathogens. Trends in Microbiology, 10, 418-424.
33. Saxton, W.M. and Hollenbeck, P.J. (2012) The axonal transport of mitochondria. Journal of Cell Science, 125, 2095-2104.
34. Sinai, A.P., Webster, P. and Joiner, K.A. (1997) Association of host cell endoplasmic reticulum and mitochondria with the Toxoplasma gondii parasitophorous vacuole membrane: a high affinity interaction. Journal of Cell Science, 110, 2117-2128.
35. Strunov, A., Kiseleva, E. and Gottlieb, Y. (2013) Spatial and temporal distribution of pathogenic Wolbachia strain wMelPop in Drosophila melanogaster central nervous system under different temperature conditions. Journal of Invertebrate Pathology, 114, 22-30.
36. Terasaki, M., Runft, L.L. and Hand, A.R. (2001) Changes in organization of the endoplasmic reticulum during Xenopus oocyte maturation and activation. Molecular Biology of the Cell, 12, 1103-1116.
37. Turley, A.P., Moreira, L.A., O'Neill, S.L. and McGraw, E.A. (2009) Wolbachia infection reduces blood-feeding success in the dengue fever mosquito, Aedes aegypti. PLoS Neglected Tropical Diseases, 3, e516.
38. Villella, A. and Hall, J.C. (2008) Neurogenetics of courtship and mating in Drosophila. Advances in Genetics, 62, 67-184.
39. Werren, J.H., Baldo, L. and Clark, M.E. (2008) Wolbachia: master manipulators of invertebrate biology. Nature Reviews Microbiology, 6, 741-751.
40. Woolfit, M., Iturbe-Ormaetxe, I., Brownlie, J.C., Walker, T., Riegler, M., Seleznev, A., Popovici, J., Rancès, E., Wee, B.A., Pavlides, J., Sullivan, M.J., Beatson, S.A., Lane, A., Sidhu, M., McMeniman, C.J., McGraw, E.A. and O'Neill, S.L. (2013) Genomic evolution of the pathogenic Wolbachia strain, wMelPop. Genome Biology and Evolution, 5, 2189-2204.
41. Wright, J.D., Sjöstrand, F.S., Portaro, J.K. and Barr, A.R. (1978) The ultrastructure of the rickettsia-like microorganism Wolbachia pipientis and associated virus-like bodies in the mosquito Culex pipiens. Journal of Ultrastructural Research, 63, 79-85.
42. Zhukova, M.V., Voronin, D.A. and Kiseleva, E.V. (2008) High temperature initiates changes of Wolbachia ultrastructure in the ovaries and early embryos of Drosophila melanogaster. Tsitologiia, 50, 1050-1060.
43. Zug, R. and Hammerstein, P. (2012) Still a host of hosts for Wolbachia: analysis of recent data suggests that 40% of terrestrial arthropod species are infected. PLoS ONE, 7, e38544.