1932

Abstract

are gram-negative bacteria that are widespread in nature, carried by the majority of insect species as well as some mites, crustaceans, and filarial nematodes. can range from parasitic to symbiotic, depending upon the interaction with the host species. The success of is attributed to efficient maternal transmission and manipulations of host reproduction that favor infected females, such as sperm-egg cytoplasmic incompatibility (CI). Much remains unknown about the mechanistic basis for -host interactions. Here we summarize the current understanding of interaction with insect hosts, with a focus on . The areas of discussion include transmission in oogenesis, distribution in spermatogenesis, induction and rescue of the CI phenotype, genomics, and -membrane interactions.

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2008-12-01
2024-10-14
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Literature Cited

  1. Ahmad K, Henikoff S. 1.  2002. The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol. Cell 9:1191–200 [Google Scholar]
  2. Ashburner M. 2.  1989. Drosophila, a Laboratory Handbook New York: Cold Spring Harbor Lab. Press1331 pp. [Google Scholar]
  3. Avakyan AA, Popov VL. 3.  1984. Rickettsiaceae and Chlamydiaceae: comparative electron microscopic studies. Acta Virol. 28:159–73 [Google Scholar]
  4. Baldo L, Lo N, Werren JH. 4.  2005. Mosaic nature of the Wolbachia surface protein. J. Bacteriol. 187:5406–18 [Google Scholar]
  5. Ballard JW. 5.  2004. Sequential evolution of a symbiont inferred from the host: Wolbachia and Drosophila simulans. Mol. Biol. Evol. 21:428–42 [Google Scholar]
  6. Baumann P, Baumann L, Lai CY, Rouhbakhsh D, Moran NA, Clark MA. 6.  1995. Genetics, physiology, and evolutionary relationships of the genus Buchnera: intracellular symbionts of aphids. Annu. Rev. Microbiol. 49:55–94 [Google Scholar]
  7. Bazzocchi C, Comazzi S, Santoni R, Bandi C, Genchi C, Mortarino M. 7.  2007. Wolbachia surface protein (WSP) inhibits apoptosis in human neutrophils. Parasite Immunol. 29:73–79 [Google Scholar]
  8. Blake MS, Blake CM, Apicella MA, Mandrell RE. 8.  1995. Gonococcal opacity: lectin-like interactions between Opa proteins and lipooligosaccharide. Infect. Immun. 63:1434–39 [Google Scholar]
  9. Boore JL. 9.  1997. Transmission of mitochondrial DNA–playing favorites?. BioEssays 19:751–53 [Google Scholar]
  10. Bordenstein SR, Marshall ML, Fry AJ, Kim U, Wernegreen JJ. 10.  2006. The tripartite associations between bacteriophage, Wolbachia, and arthropods. PLoS Pathog. 2:e43 [Google Scholar]
  11. Bordenstein SR, Uy JJ, Werren JH. 11.  2003. Host genotype determines cytoplasmic incompatibility type in the haplodiploid genus Nasonia. Genetics 164:223–33 [Google Scholar]
  12. Bordenstein SR, Wernegreen JJ. 12.  2004. Bacteriophage flux in endosymbionts (Wolbachia): infection frequency, lateral transfer, and recombination rates. Mol. Biol. Evol. 21:1981–91 [Google Scholar]
  13. Bork P. 13.  1993. Hundreds of ankyrin-like repeats in functionally diverse proteins: mobile modules that cross phyla horizontally?. Proteins 17:363–74 [Google Scholar]
  14. 14.  Deleted in proof
  15. Boyle L, O'Neill SL, Robertson HM, Karr TL. 15.  1993. Interspecific and intraspecific horizontal transfer of Wolbachia in Drosophila. Science 260:1796–99 [Google Scholar]
  16. Braig HR, Zhou W, Dobson SL, O'Neill SL. 16.  1998. Cloning and characterization of a gene encoding the major surface protein of the bacterial endosymbiont Wolbachia pipientis. J. Bacteriol. 180:2373–78 [Google Scholar]
  17. Breeuwer JA, Jacobs G. 17.  1996. Wolbachia: intracellular manipulators of mite reproduction. Exp. Appl. Acarol. 20:421–34 [Google Scholar]
  18. Breeuwer JA, Werren JH. 18.  1990. Microorganisms associated with chromosome destruction and reproductive isolation between two insect species. Nature 346:558–60 [Google Scholar]
  19. Brendza RP, Serbus LR, Duffy JB, Saxton WM. 19.  2000. A function for kinesin I in the posterior transport of oskar mRNA and Staufen protein. Science 289:2120–22 [Google Scholar]
  20. Brendza RP, Serbus LR, Saxton WM, Duffy JB. 20.  2002. Posterior localization of dynein and dorsal-ventral axis formation depend on kinesin in Drosophila oocytes. Curr. Biol. 12:1541–45 [Google Scholar]
  21. Bressac C, Rousset F. 21.  1993. The reproductive incompatibility system in Drosophila simulans: DAPI-staining analysis of the Wolbachia symbionts in sperm cysts. J. Invertebr. Pathol. 61:226–30 [Google Scholar]
  22. Brumell JH, Scidmore MA. 22.  2007. Manipulation of rab GTPase function by intracellular bacterial pathogens. Microbiol. Mol. Biol. Rev. 71:636–52 [Google Scholar]
  23. Byers JR, Wilkes A. 23.  1970. A rickettsialike microorganism in Dahlbominus fuscipennis (Zett.) (Hymenoptera, Eulophidae): observations on its occurrence and ultrastructure. Can. J. Zool. 48:959–64 [Google Scholar]
  24. Callaini G, Dallai R, Riparbelli MG. 24.  1997. Wolbachia-induced delay of paternal chromatin condensation does not prevent maternal chromosomes from entering anaphase in incompatible crosses of Drosophila simulans. J. Cell Sci. 110:Pt 2271–80 [Google Scholar]
  25. Callaini G, Riparbelli MG, Dallai R. 25.  1994. The distribution of cytoplasmic bacteria in the early Drosophila embryo is mediated by astral microtubules. J. Cell Sci. 107:Pt 3673–82 [Google Scholar]
  26. Carpenter T, Khalid S, Sansom MS. 26.  2007. A multidomain outer membrane protein from Pasteurella multocida: modelling and simulation studies of PmOmpA. Biochim. Biophys. Acta 1768:2831–40 [Google Scholar]
  27. 27.  Deleted in proof
  28. Casiraghi M, Bordenstein SR, Baldo L, Lo N, Beninati T. 28.  et al. 2005. Phylogeny of Wolbachia pipientis based on gltA, groEL and ftsZ gene sequences: clustering of arthropod and nematode symbionts in the F supergroup, and evidence for further diversity in the Wolbachia tree. Microbiology 151:4015–22 [Google Scholar]
  29. Cha BJ, Serbus LR, Koppetsch BS, Theurkauf WE. 29.  2002. Kinesin I-dependent cortical exclusion restricts pole plasm to the oocyte posterior. Nat. Cell Biol. 4:592–98 [Google Scholar]
  30. Charlat S, Calmet C, Mercot H. 30.  2001. On the mod resc model and the evolution of Wolbachia compatibility types. Genetics 159:1415–22 [Google Scholar]
  31. Chauvatcharin N, Ahantarig A, Baimai V, Kittayapong P. 31.  2006. Bacteriophage WO-B and Wolbachia in natural mosquito hosts: infection incidence, transmission mode and relative density. Mol. Ecol. 15:2451–61 [Google Scholar]
  32. Chen Y, Poon RY. 32.  2008. The multiple checkpoint functions of CHK1 and CHK2 in maintenance of genome stability. Front. Biosci. 13:5016–29 [Google Scholar]
  33. Clark I, Giniger E, Ruohola-Baker H, Jan LY, Jan YN. 33.  1994. Transient posterior localization of a kinesin fusion protein reflects anteroposterior polarity of the Drosophila oocyte. Curr. Biol. 4:289–300 [Google Scholar]
  34. Clark IE, Jan LY, Jan YN. 34.  1997. Reciprocal localization of Nod and kinesin fusion proteins indicates microtubule polarity in the Drosophila oocyte, epithelium, neuron and muscle. Development 124:461–70 [Google Scholar]
  35. Clark ME, Veneti Z, Bourtzis K, Karr TL. 35.  2002. The distribution and proliferation of the intracellular bacteria Wolbachia during spermatogenesis in Drosophila. Mech. Dev. 111:3–15 [Google Scholar]
  36. Clark ME, Veneti Z, Bourtzis K, Karr TL. 36.  2003. Wolbachia distribution and cytoplasmic incompatibility during sperm development: the cyst as the basic cellular unit of CI expression. Mech. Dev. 120:185–98 [Google Scholar]
  37. de Crespigny FE, Pitt TD, Wedell N. 37.  2006. Increased male mating rate in Drosophila is associated with Wolbachia infection. J. Evol. Biol. 19:1964–72 [Google Scholar]
  38. de Saint Phalle B, Sullivan W. 38.  1998. Spindle assembly and mitosis without centrosomes in parthenogenetic Sciara embryos. J. Cell Biol. 141:1383–91 [Google Scholar]
  39. Dedeine F, Bouletreau M, Vavre F. 39.  2005. Wolbachia requirement for oogenesis: occurrence within the genus Asobara (Hymenoptera, Braconidae) and evidence for intraspecific variation in A. tabida. Heredity 95:394–400 [Google Scholar]
  40. Dedeine F, Vavre F, Fleury F, Loppin B, Hochberg ME, Bouletreau M. 40.  2001. Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp. Proc. Natl. Acad. Sci. USA 98:6247–52 [Google Scholar]
  41. Dedeine F, Vavre F, Shoemaker DD, Bouletreau M. 41.  2004. Intra-individual coexistence of a Wolbachia strain required for host oogenesis with two strains inducing cytoplasmic incompatibility in the wasp Asobara tabida. Evol. Int. J. Org. Evol. 58:2167–74 [Google Scholar]
  42. Dobson SL. 41b.  2003. Wolbachia pipientis: impotent by association. Insect Symbiosis K Bourtzis, TA Miller 199–215 New York: CRC Press [Google Scholar]
  43. Duron O, Bernard C, Unal S, Berthomieu A, Berticat C, Weill M. 42.  2006. Tracking factors modulating cytoplasmic incompatibilities in the mosquito Culex pipiens. Mol. Ecol. 15:3061–71 [Google Scholar]
  44. Duron O, Boureux A, Echaubard P, Berthomieu A, Berticat C. 43.  et al. 2007. Variability and expression of ankyrin domain genes in Wolbachia infecting the mosquito Culex pipiens. J. Bacteriol. 189:4442–48 [Google Scholar]
  45. Duron O, Fort P, Weill M. 44.  2006. Hypervariable prophage WO sequences describe an unexpected high number of Wolbachia variants in the mosquito Culex pipiens. Proc. Biol. Sci. 273:495–502 [Google Scholar]
  46. Duron O, Fort P, Weill M. 45.  2007. Influence of aging on cytoplasmic incompatibility, sperm modification and Wolbachia density in Culex pipiens mosquitoes. Heredity 98:368–74 [Google Scholar]
  47. Dutton TJ, Sinkins SP. 46.  2004. Strain-specific quantification of Wolbachia density in Aedes albopictus and effects of larval rearing conditions. Insect. Mol. Biol. 13:317–22 [Google Scholar]
  48. Ephrussi A, Dickinson LK, Lehmann R. 47.  1991. Oskar organizes the germ plasm and directs localization of the posterior determinant nanos. Cell 66:37–50 [Google Scholar]
  49. Fenn K, Blaxter M. 48.  2006. Wolbachia genomes: revealing the biology of parasitism and mutualism. Trends Parasitol. 22:60–65 [Google Scholar]
  50. Ferree PM, Frydman HM, Li JM, Cao J, Wieschaus E, Sullivan W. 49.  2005. Wolbachia utilizes host microtubules and Dynein for anterior localization in the Drosophila oocyte. PLoS Pathog. 1:e14 [Google Scholar]
  51. Ferree PM, Sullivan W. 50.  2006. A genetic test of the role of the maternal pronucleus in Wolbachia-induced cytoplasmic incompatibility in Drosophila melanogaster. Genetics 173:839–47 [Google Scholar]
  52. Foster J, Ganatra M, Kamal I, Ware J, Makarova K. 51.  et al. 2005. The Wolbachia genome of Brugia malayi: endosymbiont evolution within a human pathogenic nematode. PLoS Biol. 3:e121 [Google Scholar]
  53. Francois S, El Benna J, Dang PM, Pedruzzi E, Gougerot-Pocidalo MA, Elbim C. 52.  2005. Inhibition of neutrophil apoptosis by TLR agonists in whole blood: involvement of the phosphoinositide 3-kinase/Akt and NF-kappaB signaling pathways, leading to increased levels of Mcl-1, A1, and phosphorylated Bad. J. Immunol. 174:3633–42 [Google Scholar]
  54. French DM, Brown WC, Palmer GH. 53.  1999. Emergence of Anaplasma marginale antigenic variants during persistent rickettsemia. Infect. Immun. 67:5834–40 [Google Scholar]
  55. Frydman HM, Li JM, Robson DN, Wieschaus E. 54.  2006. Somatic stem cell niche tropism in Wolbachia. Nature 441:509–12 [Google Scholar]
  56. Fujii Y, Kubo T, Ishikawa H, Sasaki T. 55.  2004. Isolation and characterization of the bacteriophage WO from Wolbachia, an arthropod endosymbiont. Biochem. Biophys. Res. Commun. 317:1183–88 [Google Scholar]
  57. Fuller MT. 56.  1993. Spermatogenesis. The Development of Drosophila melanogaster M Bate, AM Arias 71–147 New York: Cold Spring Harbor Lab. Press [Google Scholar]
  58. Fuller MT. 57.  1998. Genetic control of cell proliferation and differentiation in Drosophila spermatogenesis. Semin. Cell Dev. Biol. 9:433–44 [Google Scholar]
  59. Gavotte L, Henri H, Stouthamer R, Charif D, Charlat S. 58.  et al. 2007. A survey of the bacteriophage WO in the endosymbiotic bacteria Wolbachia. Mol. Biol. Evol. 24:427–35 [Google Scholar]
  60. Ghelelovitch S. 59.  1952. Genetic determinism of sterility in the cross-breeding of various strains of Culex autogenicus Roubaud. C. R. Hebd. Seances. Acad. Sci. 234:2386–88 [Google Scholar]
  61. Glover DM. 59b.  1992. The centrosome in cell division and development of Drosophila. The Centrosome VI Kalnins 219–34 New York: Academic [Google Scholar]
  62. Gonzalez-Reyes A, Elliott H, Johnston D St.. 60.  1995. Polarization of both major body axes in Drosophila by gurken-torpedo signalling. Nature 375:654–58 [Google Scholar]
  63. Greenwood J, Gautier J. 61.  2005. From oogenesis through gastrulation: developmental regulation of apoptosis. Semin. Cell Dev. Biol. 16:215–24 [Google Scholar]
  64. Hadfield SJ, Axton JM. 62.  1999. Germ cells colonized by endosymbiotic bacteria. Nature 402:482 [Google Scholar]
  65. Harris HL, Braig HR. 63.  2003. Sperm chromatin remodelling and Wolbachia-induced cytoplasmic incompatibility in Drosophila. Biochem. Cell Biol. 81:229–40 [Google Scholar]
  66. Herranz H, Perez L, Martin FA, Milan M. 64.  2008. A Wingless and Notch double-repression mechanism regulates G1-S transition in the Drosophila wing. EMBO J. 27:1633–45 [Google Scholar]
  67. Hilgenboecker K, Hammerstein P, Schlattmann P, Telschow A, Werren JH. 65.  2008. How many species are infected with Wolbachia? A statistical analysis of current data. FEMS Microbiol. Lett. 281:215–20 [Google Scholar]
  68. Hoffmann AA, Hercus M, Dagher H. 66.  1998. Population dynamics of the Wolbachia infection causing cytoplasmic incompatibility in Drosophila melanogaster. Genetics 148:221–31 [Google Scholar]
  69. Hoffmann AA, Turelli M, Harshman LG. 67.  1990. Factors affecting the distribution of cytoplasmic incompatibility in Drosophila simulans. Genetics 126:933–48 [Google Scholar]
  70. Huigens ME, de Almeida RP, Boons PA, Luck RF, Stouthamer R. 68.  2004. Natural interspecific and intraspecific horizontal transfer of parthenogenesis-inducing Wolbachia in Trichogramma wasps. Proc. Biol. Sci. 271:509–15 [Google Scholar]
  71. Huigens ME, Luck RF, Klaassen RH, Maas MF, Timmermans MJ, Stouthamer R. 69.  2000. Infectious parthenogenesis. Nature 405:178–79 [Google Scholar]
  72. Iturbe-Ormaetxe I, Burke GR, Riegler M, O'Neill SL. 70.  2005. Distribution, expression, and motif variability of ankyrin domain genes in Wolbachia pipientis. J. Bacteriol. 187:5136–45 [Google Scholar]
  73. Jaenike J. 71.  2007. Spontaneous emergence of a new Wolbachia phenotype. Evolution Int. J. Org. Evolution 61:2244–52 [Google Scholar]
  74. Jiggins FM, Hurst GD, Yang Z. 72.  2002. Host-symbiont conflicts: positive selection on an outer membrane protein of parasitic but not mutualistic Rickettsiaceae. Mol. Biol. Evol. 19:1341–49 [Google Scholar]
  75. Kawamura N. 73.  2001. Fertilization and the first cleavage mitosis in insects. Dev. Growth Differ. 43:343–49 [Google Scholar]
  76. Kim-Ha J, Smith JL, Macdonald PM. 74.  1991. oskar mRNA is localized to the posterior pole of the Drosophila oocyte. Cell 66:23–35 [Google Scholar]
  77. King RC. 75.  1970. Ovarian Development in Drosophila melanogaster New York: Academic227 pp. [Google Scholar]
  78. Kittayapong P, Mongkalangoon P, Baimai V, O'Neill SL. 76.  2002. Host age effect and expression of cytoplasmic incompatibility in field populations of Wolbachia-superinfected Aedes albopictus. Heredity 88:270–74 [Google Scholar]
  79. Kitzmiller JB. 77.  1959. Parthenogenesis in Culex fatigans. Science 129:837–38 [Google Scholar]
  80. Kondo N, Shimada M, Fukatsu T. 78.  2005. Infection density of Wolbachia endosymbiont affected by coinfection and host genotype. Biol. Lett. 1:488–91 [Google Scholar]
  81. Kose H, Karr TL. 79.  1995. Organization of Wolbachia pipientis in the Drosophila fertilized egg and embryo revealed by an antiWolbachia monoclonal antibody. Mech. Dev. 51:275–88 [Google Scholar]
  82. Lassy CW, Karr TL. 80.  1996. Cytological analysis of fertilization and early embryonic development in incompatible crosses of Drosophila simulans. Mech. Dev. 57:47–58 [Google Scholar]
  83. Li K, Kaufman TC. 81.  1996. The homeotic target gene centrosomin encodes an essential centrosomal component. Cell 85:585–96 [Google Scholar]
  84. Li M, McGrail M, Serr M, Hays TS. 82.  1994. Drosophila cytoplasmic dynein, a microtubule motor that is asymmetrically localized in the oocyte. J. Cell Biol. 126:1475–94 [Google Scholar]
  85. Lohr CV, Brayton KA, Shkap V, Molad T, Barbet AF. 83.  et al. 2002. Expression of Anaplasma marginale major surface protein 2 operon-associated proteins during mammalian and arthropod infection. Infect. Immun. 70:6005–12 [Google Scholar]
  86. Lohr CV, Rurangirwa FR, McElwain TF, Stiller D, Palmer GH. 84.  2002. Specific expression of Anaplasma marginale major surface protein 2 salivary gland variants occurs in the midgut and is an early event during tick transmission. Infect. Immun. 70:114–20 [Google Scholar]
  87. Loppin B, Bonnefoy E, Anselme C, Laurencon A, Karr TL, Couble P. 85.  2005. The histone H3.3 chaperone HIRA is essential for chromatin assembly in the male pronucleus. Nature 437:1386–90 [Google Scholar]
  88. Louis C, Nigro L. 86.  1989. Ultrastructural evidence of Wolbachia Rickettsiales in Drosophila simulans and their relationships with unidirectional cross-incompatibility. J. Invertebr. Pathol. 54:39–44 [Google Scholar]
  89. Mach JM, Lehmann R. 87.  1997. An Egalitarian-BicaudalD complex is essential for oocyte specification and axis determination in Drosophila. Genes Dev. 11:423–35 [Google Scholar]
  90. Mahowald AP. 88.  2001. Assembly of the Drosophila germ plasm. Int. Rev. Cytol. 203:187–213 [Google Scholar]
  91. Mahowald AP, Strassheim JM. 89.  1970. Intercellular migration of centrioles in the germarium of Drosophila melanogaster. An electron microscopic study. J. Cell Biol. 45:306–20 [Google Scholar]
  92. Markussen FH, Michon AM, Breitwieser W, Ephrussi A. 90.  1995. Translational control of oskar generates short OSK, the isoform that induces pole plasma assembly. Development 121:3723–32 [Google Scholar]
  93. Masui S, Kamoda S, Sasaki T, Ishikawa H. 91.  2000. Distribution and evolution of bacteriophage WO in Wolbachia, the endosymbiont causing sexual alterations in arthropods. J. Mol. Evol. 51:491–97 [Google Scholar]
  94. Maxfield FR, McGraw TE. 92.  2004. Endocytic recycling. Nat. Rev. Mol. Cell Biol. 5:121–32 [Google Scholar]
  95. McGraw EA, Merritt DJ, Droller JN, O'Neill SL. 93.  2001. Wolbachia-mediated sperm modification is dependent on the host genotype in Drosophila. Proc. Biol. Sci. 268:2565–70 [Google Scholar]
  96. McGraw EA, Merritt DJ, Droller JN, O'Neill SL. 94.  2002. Wolbachia density and virulence attenuation after transfer into a novel host. Proc. Natl. Acad. Sci. USA 99:2918–23 [Google Scholar]
  97. McGraw EA, O'Neill SL. 95.  1999. Evolution of Wolbachia pipientis transmission dynamics in insects. Trends Microbiol. 7:297–302 [Google Scholar]
  98. Min KT, Benzer S. 96.  1997. Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. Proc. Natl. Acad. Sci. USA 94:10792–96 [Google Scholar]
  99. Mohan Nair MK, Venkitanarayanan K. 97.  2007. Role of bacterial OmpA and host cytoskeleton in the invasion of human intestinal epithelial cells by Enterobacter sakazakii. Pediatr. Res. 62:664–69 [Google Scholar]
  100. Mosavi LK, Cammett TJ, Desrosiers DC, Peng ZY. 98.  2004. The ankyrin repeat as molecular architecture for protein recognition. Protein Sci. 13:1435–48 [Google Scholar]
  101. Mouton L, Henri H, Bouletreau M, Vavre F. 99.  2006. Effect of temperature on Wolbachia density and impact on cytoplasmic incompatibility. Parasitology 132:49–56 [Google Scholar]
  102. Navarro C, Puthalakath H, Adams JM, Strasser A, Lehmann R. 100.  2004. Egalitarian binds dynein light chain to establish oocyte polarity and maintain oocyte fate. Nat. Cell Biol. 6:427–35 [Google Scholar]
  103. Neuman-Silberberg FS, Schupbach T. 101.  1993. The Drosophila dorsoventral patterning gene gurken produces a dorsally localized RNA and encodes a TGF alpha-like protein. Cell 75:165–74 [Google Scholar]
  104. Noh SM, Brayton KA, Knowles DP, Agnes JT, Dark MJ. 102.  et al. 2006. Differential expression and sequence conservation of the Anaplasma marginale msp2 gene superfamily outer membrane proteins. Infect. Immun. 74:3471–79 [Google Scholar]
  105. O'Neill SL, Pettigrew MM, Sinkins SP, Braig HR, Andreadis TG, Tesh RB. 103.  1997. In vitro cultivation of Wolbachia pipientis in an Aedes albopictus cell line. Insect. Mol. Biol. 6:33–39 [Google Scholar]
  106. Pannebakker BA, Loppin B, Elemans CP, Humblot L, Vavre F. 104.  2007. Parasitic inhibition of cell death facilitates symbiosis. Proc. Natl. Acad. Sci. USA 104:213–15 [Google Scholar]
  107. Pare C, Suter B. 105.  2000. Subcellular localization of Bic-D::GFP is linked to an asymmetric oocyte nucleus. J. Cell Sci. 113:Part 122119–27 [Google Scholar]
  108. Poinsot D, Bourtzis K, Markakis G, Savakis C, Mercot H. 106.  1998. Wolbachia transfer from Drosophila melanogaster into D. simulans: host effect and cytoplasmic incompatibility relationships. Genetics 150:227–37 [Google Scholar]
  109. Poinsot D, Charlat S, Mercot H. 107.  2003. On the mechanism of Wolbachia-induced cytoplasmic incompatibility: confronting the models with the facts. BioEssays 25:259–65 [Google Scholar]
  110. Pokrywka NJ, Stephenson EC. 108.  1995. Microtubules are a general component of mRNA localization systems in Drosophila oocytes. Dev. Biol. 167:363–70 [Google Scholar]
  111. Popov VL, Chen SM, Feng HM, Walker DH. 109.  1995. Ultrastructural variation of cultured Ehrlichia chaffeensis. J. Med. Microbiol. 43:411–21 [Google Scholar]
  112. Power CP, Wang JH, Manning B, Kell MR, Aherne NJ. 110.  et al. 2004. Bacterial lipoprotein delays apoptosis in human neutrophils through inhibition of caspase-3 activity: regulatory roles for CD14 and TLR-2. J. Immunol. 173:5229–37 [Google Scholar]
  113. Presgraves DC. 111.  2000. A genetic test of the mechanism of Wolbachia-induced cytoplasmic incompatibility in Drosophila. Genetics 154:771–76 [Google Scholar]
  114. Reed KM, Werren JH. 112.  1995. Induction of paternal genome loss by the paternal-sex-ratio chromosome and cytoplasmic incompatibility bacteria (Wolbachia): a comparative study of early embryonic events. Mol. Reprod. Dev. 40:408–18 [Google Scholar]
  115. Renault AD, Axton JM. 113.  2003. Identification of plu genes and cis-acting elements of PCNA in the Drosophila genus using conservation of gene order. Gene 307:77–86 [Google Scholar]
  116. Renault AD, Zhang XH, Alphey LS, Frenz LM, Glover DM. 114.  et al. 2003. giant nuclei is essential in the cell cycle transition from meiosis to mitosis. Development 130:2997–3005 [Google Scholar]
  117. Reynolds KT, Thomson LJ, Hoffmann AA. 115.  2003. The effects of host age, host nuclear background and temperature on phenotypic effects of the virulent Wolbachia strain popcorn in Drosophila melanogaster. Genetics 164:1027–34 [Google Scholar]
  118. Riegler M, Sidhu M, Miller WJ, O'Neill SL. 116.  2005. Evidence for a global Wolbachia replacement in Drosophila melanogaster. Curr. Biol. 15:1428–33 [Google Scholar]
  119. Riparbelli MG, Giordano R, Callaini G. 117.  2007. Effects of Wolbachia on sperm maturation and architecture in Drosophila simulans Riverside. Mech. Dev. 124:699–714 [Google Scholar]
  120. Robinson JT, Wojcik EJ, Sanders MA, McGrail M, Hays TS. 118.  1999. Cytoplasmic dynein is required for the nuclear attachment and migration of centrosomes during mitosis in Drosophila. J. Cell Biol. 146:597–608 [Google Scholar]
  121. Rousset F, Bouchon D, Pintureau B, Juchault P, Solignac M. 119.  1992. Wolbachia endosymbionts responsible for various alterations of sexuality in arthropods. Proc. Biol. Sci. 250:91–98 [Google Scholar]
  122. Ryan SL, Saul GB 2nd. 120.  1968. Post-fertilization effect of incompatibility factors in Mormoniella. Mol. Gen. Genet. 103:29–36 [Google Scholar]
  123. Salcedo SP, Holden DW. 121.  2005. Bacterial interactions with the eukaryotic secretory pathway. Curr. Opin. Microbiol. 8:92–98 [Google Scholar]
  124. 122.  Deleted in proof
  125. Sanogo YO, Eitam A, Dobson SL. 123.  2005. No evidence for bacteriophage WO orf7 correlation with Wolbachia-induced cytoplasmic incompatibility in the Culex pipiens complex (Culicidae: Diptera). J. Med. Entomol. 42:789–94 [Google Scholar]
  126. Sasaki T, Braig HR, O'Neill SL. 124.  1998. Analysis of Wolbachia protein synthesis in Drosophila in vivo. Insect. Mol. Biol. 7:101–5 [Google Scholar]
  127. Sasaki T, Massaki N, Kubo T. 125.  2005. Wolbachia variant that induces two distinct reproductive phenotypes in different hosts. Heredity 95:389–93 [Google Scholar]
  128. Schupbach T. 126.  1987. Germ line and soma cooperate during oogenesis to establish the dorsoventral pattern of egg shell and embryo in Drosophila melanogaster. Cell 49:699–707 [Google Scholar]
  129. Serbus LR, Cha BJ, Theurkauf WE, Saxton WM. 127.  2005. Dynein and the actin cytoskeleton control kinesin-driven cytoplasmic streaming in Drosophila oocytes. Development 132:3743–52 [Google Scholar]
  130. Serbus LR, Sullivan W. 128.  2007. A cellular basis for Wolbachia recruitment to the host germline. PLoS Pathog. 3:e190 [Google Scholar]
  131. Sinkins SP, Walker T, Lynd AR, Steven AR, Makepeace BL. 129.  et al. 2005. Wolbachia variability and host effects on crossing type in Culex mosquitoes. Nature 436:257–60 [Google Scholar]
  132. Sironi M, Bandi C, Sacchi L, Di Sacco B, Damiani G, Genchi C. 130.  1995. Molecular evidence for a close relative of the arthropod endosymbiont Wolbachia in a filarial worm. Mol. Biochem. Parasitol. 74:223–27 [Google Scholar]
  133. Sluder G, Thompson EA, Rieder CL, Miller FJ. 131.  1995. Nuclear envelope breakdown is under nuclear not cytoplasmic control in sea urchin zygotes. J. Cell Biol. 129:1447–58 [Google Scholar]
  134. Snook RR, Cleland SY, Wolfner MF, Karr TL. 132.  2000. Offsetting effects of Wolbachia infection and heat shock on sperm production in Drosophila simulans: analyses of fecundity, fertility and accessory gland proteins. Genetics 155:167–78 [Google Scholar]
  135. Sokolova MI, Zinkevich NS, Zakharov IA. 133.  2002. Bacteria in ovarioles of females from maleless families of ladybird beetles Adalia bipunctata L. (Coleoptera: Coccinellidae) naturally infected with Rickettsia, Wolbachia, and Spiroplasma. J. Invertebr. Pathol. 79:72–79 [Google Scholar]
  136. Sonnenblick BP. 133b.  1950. The early embryology of Drosophila melanogaster. Biology of Drosophila M Demerec 62–167 New York: Wiley [Google Scholar]
  137. Starr DJ, Cline TW. 134.  2002. A host parasite interaction rescues Drosophila oogenesis defects. Nature 418:76–79 [Google Scholar]
  138. Stouthamer R, Breeuwer JA, Hurst GD. 135.  1999. Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu. Rev. Microbiol. 53:71–102 [Google Scholar]
  139. Stouthamer R, Breeuwert JA, Luck RF, Werren JH. 136.  1993. Molecular identification of microorganisms associated with parthenogenesis. Nature 361:66–68 [Google Scholar]
  140. Szollosi A, Debec A. 137.  1980. Presence of Rickettsias in haploid Drosophila melanogaster cell lines. Extr. Biol. Cell. 38:129–34 [Google Scholar]
  141. Takada S, Kelkar A, Theurkauf WE. 138.  2003. Drosophila checkpoint kinase 2 couples centrosome function and spindle assembly to genomic integrity. Cell 113:87–99 [Google Scholar]
  142. Theurkauf WE, Smiley S, Wong ML, Alberts BM. 139.  1992. Reorganization of the cytoskeleton during Drosophila oogenesis: implications for axis specification and intercellular transport. Development 115:923–36 [Google Scholar]
  143. Tram U, Ferree PM, Sullivan W. 140.  2003. Identification of Wolbachia–host interacting factors through cytological analysis. Microbes Infect. 5:999–1011 [Google Scholar]
  144. Tram U, Fredrick K, Werren JH, Sullivan W. 141.  2006. Paternal chromosome segregation during the first mitotic division determines Wolbachia-induced cytoplasmic incompatibility phenotype. J. Cell Sci. 119:3655–63 [Google Scholar]
  145. Tram U, Sullivan W. 142.  2002. Role of delayed nuclear envelope breakdown and mitosis in Wolbachia-induced cytoplasmic incompatibility. Science 296:1124–26 [Google Scholar]
  146. Turelli M, Hoffmann AA. 143.  1995. Cytoplasmic incompatibility in Drosophila simulans: dynamics and parameter estimates from natural populations. Genetics 140:1319–38 [Google Scholar]
  147. Veneti Z, Clark ME, Karr TL, Savakis C, Bourtzis K. 144.  2004. Heads or tails: host-parasite interactions in the Drosophila-Wolbachia system. Appl. Environ. Microbiol. 70:5366–72 [Google Scholar]
  148. Voronin DA, Dudkina NV, Kiseleva EV. 145.  2004. A new form of symbiotic bacteria Wolbachia found in the endoplasmic reticulum of early embryos of Drosophila melanogaster. Dokl. Biol. Sci. 396:227–29 [Google Scholar]
  149. Wasserman WJ, Smith LD. 146.  1978. The cyclic behavior of a cytoplasmic factor controlling nuclear membrane breakdown. J. Cell Biol. 78:R15–22 [Google Scholar]
  150. Weeks AR, Turelli M, Harcombe WR, Reynolds KT, Hoffmann AA. 147.  2007. From parasite to mutualist: rapid evolution of Wolbachia in natural populations of Drosophila. PLoS Biol. 5:e114 [Google Scholar]
  151. Werren JH. 148.  1997. Biology of Wolbachia. Annu. Rev. Entomol. 42:587–609 [Google Scholar]
  152. Werren JH, Zhang W, Guo LR. 149.  1995. Evolution and phylogeny of Wolbachia: reproductive parasites of arthropods. Proc. Biol. Sci. 261:55–63 [Google Scholar]
  153. Williams EH, Fields S, Saul GB 2nd. 150.  1993. Transfer of incompatibility factors between stocks of Nasonia (=Mormoniella) vitripennis. J. Invertebr. Pathol. 61:206–10 [Google Scholar]
  154. Wiwatanaratanabutr S, Kittayapong P. 151.  2006. Effects of temephos and temperature on Wolbachia load and life history traits of Aedes albopictus. Med. Vet. Entomol. 20:300–7 [Google Scholar]
  155. Wright JD, Barr AR. 152.  1980. The ultrastructure and symbiotic relationships of Wolbachia of mosquitoes of the Aedes scutellaris group. J. Ultrastruct. Res. 72:52–64 [Google Scholar]
  156. Wright JD, Barr AR. 153.  1981. Wolbachia and the normal and incompatible eggs of Aedes polynesiensis (Diptera: Culicidae). J. Invertebr. Pathol. 38:409–18 [Google Scholar]
  157. Wright JD, Sjostrand FS, Portaro JK, Barr AR. 154.  1978. The ultrastructure of the rickettsia-like microorganism Wolbachia pipientis and associated virus-like bodies in the mosquito Culex pipiens. J. Ultrastruct. Res. 63:79–85 [Google Scholar]
  158. Wu M, Sun LV, Vamathevan J, Riegler M, Deboy R. 155.  et al. 2004. Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: a streamlined genome overrun by mobile genetic elements. PLoS Biol. 2:E69 [Google Scholar]
  159. Xi Z, Dean JL, Khoo C, Dobson SL. 156.  2005. Generation of a novel Wolbachia infection in Aedes albopictus (Asian tiger mosquito) via embryonic microinjection. Insect Biochem. Mol. Biol. 35:903–10 [Google Scholar]
  160. Yen JH, Barr AR. 157.  1974. Incompatibility in Culex pipiens. The Use of Genetics in Insect Control R Pal, MJ Whitten 97–118 Amsterdam: Elsevier [Google Scholar]
  161. Yu KR, Saint RB, Sullivan W. 158.  2000. The Grapes checkpoint coordinates nuclear envelope breakdown and chromosome condensation. Nat. Cell Biol. 2:609–15 [Google Scholar]
  162. Zabalou S, Apostolaki A, Pattas S, Veneti Z, Paraskevopoulos C. 159.  et al. 2008. Multiple rescue factors within a Wolbachia strain. Genetics 178:2145–60 [Google Scholar]
  163. Zchori-Fein E, Roush RT, Rosen D. 160.  1998. Distribution of parthenogenesis-inducing symbionts in ovaries and eggs of Aphytis (Hymentoptera: Aphelinidae). Curr. Microbiol. 36:1–8 [Google Scholar]
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