The genetics and cell biology of Wolbachia-host interactions

Annual Review of Genetics

Volumn 42, Issue , 2008, Pages 683-707

  Serbus, Laura R ^a   Casper Lindley, Catharina ^a   Landmann, Frédéric ^a   Sullivan, William ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cytoplasmic incompatibility; Drosophila; Genomics; Transmission; Wolbachia

Indexed keywords

BACTERIAL GENETICS; BACTERIAL TRANSMISSION; CYTOLOGY; DROSOPHILA; HOST PATHOGEN INTERACTION; INSECT; NONHUMAN; PRIORITY JOURNAL; REVIEW; SPERMATOGENESIS; SYMBIOSIS; WOLBACHIA;

ANIMALS; DROSOPHILA; FEMALE; HOST-PATHOGEN INTERACTIONS; INSECTS; MALE; OOCYTES; OOGENESIS; SPERMATOGENESIS; SPERMATOZOA; WOLBACHIA;

ACARI; CRUSTACEA; HEXAPODA; NEGIBACTERIA; NEMATODA; WOLBACHIA;

EID: 56749089538     PISSN: 00664197     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.genet.41.110306.130354     Document Type: Review

References (163)

1. Ahmad K, Henikoff S. 2002. The histone variant H3.3 marks active chromatin by replicationindependent nucleosome assembly. Mol. Cell 9:1191-200
2. Ashburner M. 1989. Drosophila, a Laboratory Handbook. New York: Cold Spring Harbor Lab. Press. 1331 pp.
3. Avakyan AA, Popov VL. 1984. Rickettsiaceae and Chlamydiaceae: comparative electron microscopic studies. Acta Virol. 28:159-73
4. Baldo L, Lo N, Werren JH. 2005. Mosaic nature of the Wolbachia surface protein. J. Bacteriol. 187:5406-18
5. Ballard JW. 2004. Sequential evolution of a symbiont inferred from the host: Wolbachia and Drosophila simulans. Mol. Biol. Evol. 21:428-42
6. Baumann P, Baumann L, Lai CY, Rouhbakhsh D, Moran NA, Clark MA. 1995. Genetics, physiology, and evolutionary relationships of the genus Buchnera: intracellular symbionts of aphids. Annu. Rev. Microbiol. 49:55-94
7. Bazzocchi C, Comazzi S, Santoni R, Bandi C, Genchi C, Mortarino M. 2007. Wolbachia surface protein (WSP) inhibits apoptosis in human neutrophils. Parasite Immunol. 29:73-79
8. Blake MS, Blake CM, Apicella MA, Mandrell RE. 1995. Gonococcal opacity: lectin-like interactions between Opa proteins and lipooligosaccharide. Infect. Immun. 63:1434-39
9. Boore JL. 1997. Transmission of mitochondrial DNA-playing favorites? BioEssays 19:751-53
10. Bordenstein SR, Marshall ML, Fry AJ, Kim U, Wernegreen JJ. 2006. The tripartite associations between bacteriophage, Wolbachia, and arthropods. PLoS Pathog. 2:e43
11. Bordenstein SR, Uy JJ, Werren JH. 2003. Host genotype determines cytoplasmic incompatibility type in the haplodiploid genus Nasonia. Genetics 164:223-33
12. Bordenstein SR, Wernegreen JJ. 2004. Bacteriophage flux in endosymbionts (Wolbachia): infection frequency, lateral transfer, and recombination rates. Mol. Biol. Evol. 21:1981-91
13. Bork P. 1993. Hundreds of ankyrin-like repeats in functionally diverse proteins: mobile modules that cross phyla horizontally? Proteins 17:363-74
14. Deleted in proof
15. Boyle L, O'Neill SL, Robertson HM, Karr TL. 1993. Interspecific and intraspecific horizontal transfer of Wolbachia in Drosophila. Science 260:1796-99
16. Braig HR, Zhou W, Dobson SL, O'Neill SL. 1998. Cloning and characterization of a gene encoding the major surface protein of the bacterial endosymbiont Wolbachia pipientis. J. Bacteriol. 180:2373-78
17. Breeuwer JA, Jacobs G. 1996. Wolbachia: intracellular manipulators of mite reproduction. Exp. Appl. Acarol. 20:421-34
18. Breeuwer JA, Werren JH. 1990. Microorganisms associated with chromosome destruction and reproductive isolation between two insect species. Nature 346:558-60
19. Brendza RP, Serbus LR, Duffy JB, Saxton WM. 2000. A function for kinesin I in the posterior transport of oskar mRNA and Staufen protein. Science 289:2120-22
20. Brendza RP, Serbus LR, Saxton WM, Duffy JB. 2002. Posterior localization of dynein and dorsal-ventral axis formation depend on kinesin in Drosophila oocytes. Curr. Biol. 12:1541-45
21. Bressac C, Rousset F. 1993. The reproductive incompatibility system in Drosophila simulans: DAPI-staining analysis of the Wolbachia symbionts in sperm cysts. J. Invertebr. Pathol. 61:226-30
22. Brumell JH, Scidmore MA. 2007. Manipulation of rab GTPase function by intracellular bacterial pathogens. Microbiol. Mol. Biol. Rev. 71:636-52
23. Byers JR, Wilkes A. 1970. A rickettsialike microorganism in Dahlbominus fuscipennis (Zett.) (Hymenoptera, Eulophidae): observations on its occurrence and ultrastructure. Can. J. Zool. 48:959-64
24. Callaini G, Dallai R, Riparbelli MG. 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 2):271-80
25. Callaini G, Riparbelli MG, Dallai R. 1994. The distribution of cytoplasmic bacteria in the early Drosophila embryo is mediated by astral microtubules. J. Cell Sci. 107(Pt 3):673-82
26. Carpenter T, Khalid S, Sansom MS. 2007. A multidomain outer membrane protein from Pasteurella multocida: modelling and simulation studies of PmOmpA. Biochim. Biophys. Acta 1768:2831-40
27. Deleted in proof
28. Casiraghi M, Bordenstein SR, Baldo L, Lo N, Beninati T, 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
29. Cha BJ, Serbus LR, Koppetsch BS, Theurkauf WE. 2002. Kinesin I-dependent cortical exclusion restricts pole plasm to the oocyte posterior. Nat. Cell Biol. 4:592-98
30. Charlat S, Calmet C, Mercot H. 2001. On the mod resc model and the evolution of Wolbachia compatibility types. Genetics 159:1415-22
31. Chauvatcharin N, Ahantarig A, Baimai V, Kittayapong P. 2006. Bacteriophage WO-B and Wolbachia in natural mosquito hosts: infection incidence, transmission mode and relative density. Mol. Ecol. 15:2451-61
32. Chen Y, Poon RY. 2008. The multiple checkpoint functions of CHK1 and CHK2 in maintenance of genome stability. Front. Biosci. 13:5016-29
33. Clark I, Giniger E, Ruohola-Baker H, Jan LY, Jan YN. 1994. Transient posterior localization of a kinesin fusion protein reflects anteroposterior polarity of the Drosophila oocyte. Curr. Biol. 4:289-300
34. Clark IE, Jan LY, Jan YN. 1997. Reciprocal localization of Nod and kinesin fusion proteins indicates microtubule polarity in the Drosophila oocyte, epithelium, neuron and muscle. Development 124:461-70
35. Clark ME, Veneti Z, Bourtzis K, Karr TL. 2002. The distribution and proliferation of the intracellular bacteria Wolbachia during spermatogenesis in Drosophila. Mech. Dev. 111:3-15
36. Clark ME, Veneti Z, Bourtzis K, Karr TL. 2003. Wolbachia distribution and cytoplasmic incompatibility during sperm development: the cyst as the basic cellular unit of CI expression. Mech. Dev. 120:185-98
37. de Crespigny FE, Pitt TD, Wedell N. 2006. Increased male mating rate in Drosophila is associated with Wolbachia infection. J. Evol. Biol. 19:1964-72
38. de Saint Phalle B, Sullivan W. 1998. Spindle assembly and mitosis without centrosomes in parthenogenetic Sciara embryos. J. Cell Biol. 141:1383-91
39. Dedeine F, Bouletreau M, Vavre F. 2005. Wolbachia requirement for oogenesis: occurrence within the genus Asobara (Hymenoptera, Braconidae) and evidence for intraspecific variation in A. tabida. Heredity 95:394-400
40. Dedeine F, Vavre F, Fleury F, Loppin B, Hochberg ME, Bouletreau M. 2001. Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp. Proc. Natl. Acad. Sci. USA 98:6247-52
41. Dedeine F, Vavre F, Shoemaker DD, Bouletreau M. 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
42. Dobson SL. 2003. Wolbachia pipientis: impotent by association. In Insect Symbiosis, ed. K Bourtzis, TA Miller, pp. 199-215. New York: CRC Press
43. Duron O, Bernard C, Unal S, Berthomieu A, Berticat C, Weill M. 2006. Tracking factors modulating cytoplasmic incompatibilities in the mosquito Culex pipiens. Mol. Ecol. 15:3061-71
44. Duron O, Boureux A, Echaubard P, Berthomieu A, Berticat C, et al. 2007. Variability and expression of ankyrin domain genes in Wolbachia infecting the mosquito Culex pipiens. J. Bacteriol. 189:4442-48
45. Duron O, Fort P, Weill M. 2006. Hypervariable prophage WO sequences describe an unexpected high number of Wolbachia variants in the mosquito Culex pipiens. Proc. Biol. Sci. 273:495-502
46. Duron O, Fort P, Weill M. 2007. Influence of aging on cytoplasmic incompatibility, sperm modification and Wolbachia density in Culex pipiens mosquitoes. Heredity 98:368-74
47. Dutton TJ, Sinkins SP. 2004. Strain-specific quantification of Wolbachia density in Aedes albopictus and effects of larval rearing conditions. Insect. Mol. Biol. 13:317-22
48. Ephrussi A, Dickinson LK, Lehmann R. 1991. Oskar organizes the germ plasm and directs localization of the posterior determinant nanos. Cell 66:37-50
49. Fenn K, Blaxter M. 2006. Wolbachia genomes: revealing the biology of parasitism and mutualism. Trends Parasitol. 22:60-65
50. Ferree PM, Frydman HM, Li JM, Cao J, Wieschaus E, Sullivan W. 2005. Wolbachia utilizes host microtubules and Dynein for anterior localization in the Drosophila oocyte. PLoS Pathog. 1:e14
51. Ferree PM, Sullivan W. 2006. A genetic test of the role of the maternal pronucleus in Wolbachia-induced cytoplasmic incompatibility in Drosophila melanogaster. Genetics 173:839-47
52. Foster J, Ganatra M, Kamal I, Ware J, Makarova K, et al. 2005. The Wolbachia genome of Brugia malayi: endosymbiont evolution within a human pathogenic nematode. PLoS Biol. 3:e121
53. Francois S, El Benna J, Dang PM, Pedruzzi E, Gougerot-Pocidalo MA, Elbim C. 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
54. French DM, Brown WC, Palmer GH. 1999. Emergence of Anaplasma marginale antigenic variants during persistent rickettsemia. Infect. Immun. 67:5834-40
55. Frydman HM, Li JM, Robson DN, Wieschaus E. 2006. Somatic stem cell niche tropism in Wolbachia. Nature 441:509-12
56. Fujii Y, Kubo T, Ishikawa H, Sasaki T. 2004. Isolation and characterization of the bacteriophage WO from Wolbachia, an arthropod endosymbiont. Biochem. Biophys. Res. Commun. 317:1183-88
57. Fuller MT. 1993. Spermatogenesis. In The Development of Drosophila melanogaster, ed. M Bate, AM Arias, pp. 71-147. New York: Cold Spring Harbor Lab. Press
58. Fuller MT. 1998. Genetic control of cell proliferation and differentiation in Drosophila spermatogenesis. Semin. Cell Dev. Biol. 9:433-44
59. Gavotte L, Henri H, Stouthamer R, Charif D, Charlat S, et al. 2007. A survey of the bacteriophage WO in the endosymbiotic bacteria Wolbachia. Mol. Biol. Evol. 24:427-35
60. Ghelelovitch S. 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
61. Glover DM. 1992. The centrosome in cell division and development of Drosophila. In The Centrosome, ed. VI Kalnins, pp. 219-34. New York: Academic
62. Gonzalez-Reyes A, Elliott H, St. Johnston D. 1995. Polarization of both major body axes in Drosophila by gurken-torpedo signalling. Nature 375:654-58
63. Greenwood J, Gautier J. 2005. From oogenesis through gastrulation: developmental regulation of apoptosis. Semin. Cell Dev. Biol. 16:215-24
64. Hadfield SJ, Axton JM. 1999. Germ cells colonized by endosymbiotic bacteria. Nature 402:482
65. Harris HL, Braig HR. 2003. Sperm chromatin remodelling and Wolbachia-induced cytoplasmic incompatibility in Drosophila. Biochem. Cell Biol. 81:229-40
66. Herranz H, Perez L, Martin FA, Milan M. 2008. A Wingless and Notch double-repression mechanism regulates G1-S transition in the Drosophila wing. EMBO J. 27:1633-45
67. Hilgenboecker K, Hammerstein P, Schlattmann P, Telschow A, Werren JH. 2008. How many species are infected with Wolbachia? A statistical analysis of current data. FEMS Microbiol. Lett. 281:215-20
68. Hoffmann AA, Hercus M, Dagher H. 1998. Population dynamics of the Wolbachia infection causing cytoplasmic incompatibility in Drosophila melanogaster. Genetics 148:221-31
69. Hoffmann AA, Turelli M, Harshman LG. 1990. Factors affecting the distribution of cytoplasmic incompatibility in Drosophila simulans. Genetics 126:933-48
70. Huigens ME, de Almeida RP, Boons PA, Luck RF, Stouthamer R. 2004. Natural interspecific and intraspecific horizontal transfer of parthenogenesis-inducing Wolbachia in Trichogramma wasps. Proc. Biol. Sci. 271:509-15
71. Huigens ME, Luck RF, Klaassen RH, Maas MF, Timmermans MJ, Stouthamer R. 2000. Infectious parthenogenesis. Nature 405:178-79
72. Iturbe-Ormaetxe I, Burke GR, Riegler M, O'Neill SL. 2005. Distribution, expression, and motif variability of ankyrin domain genes in Wolbachia pipientis. J. Bacteriol. 187:5136-45
73. Jaenike J. 2007. Spontaneous emergence of a new Wolbachia phenotype. Evolution Int. J. Org. Evolution 61:2244-52
74. Jiggins FM, Hurst GD, Yang Z. 2002. Host-symbiont conflicts: positive selection on an outer membrane protein of parasitic but not mutualistic Rickettsiaceae. Mol. Biol. Evol. 19:1341-49
75. Kawamura N. 2001. Fertilization and the first cleavage mitosis in insects. Dev. Growth Differ. 43:343-49
76. Kim-Ha J, Smith JL, Macdonald PM. 1991. oskar mRNA is localized to the posterior pole of the Drosophila oocyte. Cell 66:23-35
77. King RC. 1970. Ovarian Development in Drosophila melanogaster. New York: Academic. 227 pp.
78. Kittayapong P, Mongkalangoon P, Baimai V, O'Neill SL. 2002. Host age effect and expression of cytoplasmic incompatibility in field populations of Wolbachia-superinfected Aedes albopictus. Heredity 88:270-74
79. Kitzmiller JB. 1959. Parthenogenesis in Culex fatigans. Science 129:837-38
80. Kondo N, Shimada M, Fukatsu T. 2005. Infection density of Wolbachia endosymbiont affected by coinfection and host genotype. Biol. Lett. 1:488-91
81. Kose H, Karr TL. 1995. Organization of Wolbachia pipientis in the Drosophila fertilized egg and embryo revealed by an anti Wolbachia monoclonal antibody. Mech. Dev. 51:275-88
82. Lassy CW, Karr TL. 1996. Cytological analysis of fertilization and early embryonic development in incompatible crosses of Drosophila simulans. Mech. Dev. 57:47-58
83. Li K, Kaufman TC. 1996. The homeotic target gene centrosomin encodes an essential centrosomal component. Cell 85:585-96
84. Li M, McGrail M, Serr M, Hays TS. 1994. Drosophila cytoplasmic dynein, a microtubule motor that is asymmetrically localized in the oocyte. J. Cell Biol. 126:1475-94
85. Lohr CV, Brayton KA, Shkap V, Molad T, Barbet AF, et al. 2002. Expression of Anaplasma marginale major surface protein 2 operon-associated proteins during mammalian and arthropod infection. Infect. Immun. 70:6005-12
86. Lohr CV, Rurangirwa FR, McElwain TF, Stiller D, Palmer GH. 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
87. Loppin B, Bonnefoy E, Anselme C, Laurencon A, Karr TL, Couble P. 2005. The histone H3.3 chaperone HIRA is essential for chromatin assembly in the male pronucleus. Nature 437:1386-90
88. Louis C, Nigro L. 1989. Ultrastructural evidence of Wolbachia Rickettsiales in Drosophila simulans and their relationships with unidirectional cross-incompatibility. J. Invertebr. Pathol. 54:39-44
89. Mach JM, Lehmann R. 1997. An Egalitarian-BicaudalD complex is essential for oocyte specification and axis determination in Drosophila. Genes Dev. 11:423-35
90. Mahowald AP. 2001. Assembly of the Drosophila germ plasm. Int. Rev. Cytol. 203:187-213
91. Mahowald AP, Strassheim JM. 1970. Intercellular migration of centrioles in the germarium of Drosophila melanogaster. An electron microscopic study. J. Cell Biol. 45:306-20
92. Markussen FH, Michon AM, Breitwieser W, Ephrussi A. 1995. Translational control of oskar generates short OSK, the isoform that induces pole plasma assembly. Development 121:3723-32
93. Masui S, Kamoda S, Sasaki T, Ishikawa H. 2000. Distribution and evolution of bacteriophage WO in Wolbachia, the endosymbiont causing sexual alterations in arthropods. J. Mol. Evol. 51:491-97
94. Maxfield FR, McGraw TE. 2004. Endocytic recycling. Nat. Rev. Mol. Cell Biol. 5:121-32
95. McGraw EA, Merritt DJ, Droller JN, O'Neill SL. 2001. Wolbachia-mediated sperm modification is dependent on the host genotype in Drosophila. Proc. Biol. Sci. 268:2565-70
96. McGraw EA, Merritt DJ, Droller JN, O'Neill SL. 2002. Wolbachia density and virulence attenuation after transfer into a novel host. Proc. Natl. Acad. Sci. USA 99:2918-23
97. McGraw EA, O'Neill SL. 1999. Evolution of Wolbachia pipientis transmission dynamics in insects. Trends Microbiol. 7:297-302
98. Min KT, Benzer S. 1997. Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. Proc. Natl. Acad. Sci. USA 94:10792-96
99. Mohan Nair MK, Venkitanarayanan K. 2007. Role of bacterial OmpA and host cytoskeleton in the invasion of human intestinal epithelial cells by Enterobacter sakazakii. Pediatr. Res. 62:664-69
100. Mosavi LK, Cammett TJ, Desrosiers DC, Peng ZY. 2004. The ankyrin repeat as molecular architecture for protein recognition. Protein Sci. 13:1435-48
101. Mouton L, Henri H, Bouletreau M, Vavre F. 2006. Effect of temperature on Wolbachia density and impact on cytoplasmic incompatibility. Parasitology 132:49-56
102. Navarro C, Puthalakath H, Adams JM, Strasser A, Lehmann R. 2004. Egalitarian binds dynein light chain to establish oocyte polarity and maintain oocyte fate. Nat. Cell Biol. 6:427-35
103. Neuman-Silberberg FS, Schupbach T. 1993. The Drosophila dorsoventral patterning gene gurken produces a dorsally localized RNA and encodes a TGF alpha-like protein. Cell 75:165-74
104. Noh SM, Brayton KA, Knowles DP, Agnes JT, Dark MJ, et al. 2006. Differential expression and sequence conservation of the Anaplasma marginale msp2 gene superfamily outer membrane proteins. Infect. Immun. 74:3471-79
105. O'Neill SL, Pettigrew MM, Sinkins SP, Braig HR, Andreadis TG, Tesh RB. 1997. In vitro cultivation of Wolbachia pipientis in an Aedes albopictus cell line. Insect. Mol. Biol. 6:33-39
106. Pannebakker BA, Loppin B, Elemans CP, Humblot L, Vavre F. 2007. Parasitic inhibition of cell death facilitates symbiosis. Proc. Natl. Acad. Sci. USA 104:213-15
107. Pare C, Suter B. 2000. Subcellular localization of Bic-D::GFP is linked to an asymmetric oocyte nucleus. J. Cell Sci. 113(Part 12):2119-27
108. Poinsot D, Bourtzis K, Markakis G, Savakis C, Mercot H. 1998. Wolbachia transfer from Drosophila melanogaster into D. simulans: host effect and cytoplasmic incompatibility relationships. Genetics 150:227-37
109. Poinsot D, Charlat S, Mercot H. 2003. On the mechanism of Wolbachia-induced cytoplasmic incompatibility: confronting the models with the facts. BioEssays 25:259-65
110. Pokrywka NJ, Stephenson EC. 1995. Microtubules are a general component of mRNA localization systems in Drosophila oocytes. Dev. Biol. 167:363-70
111. Popov VL, Chen SM, Feng HM, Walker DH. 1995. Ultrastructural variation of cultured Ehrlichia chaffeensis. J. Med. Microbiol. 43:411-21
112. Power CP, Wang JH, Manning B, Kell MR, Aherne NJ, 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
113. Presgraves DC. 2000. A genetic test of the mechanism of Wolbachia-induced cytoplasmic incompatibility in Drosophila. Genetics 154:771-76
114. Reed KM, Werren JH. 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
115. Renault AD, Axton JM. 2003. Identification of plu genes and cis-acting elements of PCNA in the Drosophila genus using conservation of gene order. Gene 307:77-86
116. Renault AD, Zhang XH, Alphey LS, Frenz LM, Glover DM, et al. 2003. giant nuclei is essential in the cell cycle transition from meiosis to mitosis. Development 130:2997-3005
117. Reynolds KT, Thomson LJ, Hoffmann AA. 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
118. Riegler M, Sidhu M, Miller WJ, O'Neill SL. 2005. Evidence for a global Wolbachia replacement in Drosophila melanogaster. Curr. Biol. 15:1428-33
119. Riparbelli MG, Giordano R, Callaini G. 2007. Effects of Wolbachia on sperm maturation and architecture in Drosophila simulans Riverside. Mech. Dev. 124:699-714
120. Robinson JT, Wojcik EJ, Sanders MA, McGrail M, Hays TS. 1999. Cytoplasmic dynein is required for the nuclear attachment and migration of centrosomes during mitosis in Drosophila. J. Cell Biol. 146:597-608
121. Rousset F, Bouchon D, Pintureau B, Juchault P, Solignac M. 1992. Wolbachia endosymbionts responsible for various alterations of sexuality in arthropods. Proc. Biol. Sci. 250:91-98
122. Ryan SL, Saul GB 2nd. 1968. Post-fertilization effect of incompatibility factors in Mormoniella. Mol. Gen. Genet. 103:29-36
123. Salcedo SP, Holden DW. 2005. Bacterial interactions with the eukaryotic secretory pathway. Curr. Opin. Microbiol. 8:92-98
124. Deleted in proof
125. Sanogo YO, Eitam A, Dobson SL. 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
126. Sasaki T, Braig HR, O'Neill SL. 1998. Analysis of Wolbachia protein synthesis in Drosophila in vivo. Insect. Mol. Biol. 7:101-5
127. Sasaki T, Massaki N, Kubo T. 2005. Wolbachia variant that induces two distinct reproductive phenotypes in different hosts. Heredity 95:389-93
128. Schupbach T. 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
129. Serbus LR, Cha BJ, Theurkauf WE, Saxton WM. 2005. Dynein and the actin cytoskeleton control kinesin-driven cytoplasmic streaming in Drosophila oocytes. Development 132:3743-52
130. Serbus LR, Sullivan W. 2007. A cellular basis for Wolbachia recruitment to the host germline. PLoS Pathog. 3:e190
131. Sinkins SP, Walker T, Lynd AR, Steven AR, Makepeace BL, et al. 2005. Wolbachia variability and host effects on crossing type in Culex mosquitoes. Nature 436:257-60
132. Sironi M, Bandi C, Sacchi L, Di Sacco B, Damiani G, Genchi C. 1995. Molecular evidence for a close relative of the arthropod endosymbiont Wolbachia in a filarial worm. Mol. Biochem. Parasitol. 74:223-27
133. Sluder G, Thompson EA, Rieder CL, Miller FJ. 1995. Nuclear envelope breakdown is under nuclear not cytoplasmic control in sea urchin zygotes. J. Cell Biol. 129:1447-58
134. Snook RR, Cleland SY, Wolfner MF, Karr TL. 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
135. Sokolova MI, Zinkevich NS, Zakharov IA. 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
136. 133b. Sonnenblick BP. 1950. The early embryology of Drosophila melanogaster. In Biology of Drosophila, ed. M Demerec, pp. 62-167. New York: Wiley
137. Starr DJ, Cline TW. 2002. A host parasite interaction rescues Drosophila oogenesis defects. Nature 418:76-79
138. Stouthamer R, Breeuwer JA, Hurst GD. 1999. Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu. Rev. Microbiol. 53:71-102
139. Stouthamer R, Breeuwert JA, Luck RF, Werren JH. 1993. Molecular identification of microorganisms associated with parthenogenesis. Nature 361:66-68
140. Szollosi A, Debec A. 1980. Presence of Rickettsias in haploid Drosophila melanogaster cell lines. Extr. Biol. Cell. 38:129-34
141. Takada S, Kelkar A, Theurkauf WE. 2003. Drosophila checkpoint kinase 2 couples centrosome function and spindle assembly to genomic integrity. Cell 113:87-99
142. Theurkauf WE, Smiley S, Wong ML, Alberts BM. 1992. Reorganization of the cytoskeleton during Drosophila oogenesis: implications for axis specification and intercellular transport. Development 115:923-36
143. Tram U, Ferree PM, Sullivan W. 2003. Identification of Wolbachia-host interacting factors through cytological analysis. Microbes Infect. 5:999-1011
144. Tram U, Fredrick K, Werren JH, Sullivan W. 2006. Paternal chromosome segregation during the first mitotic division determines Wolbachia-induced cytoplasmic incompatibility phenotype. J. Cell Sci. 119:3655-63
145. Tram U, Sullivan W. 2002. Role of delayed nuclear envelope breakdown and mitosis in Wolbachia-induced cytoplasmic incompatibility. Science 296:1124-26
146. Turelli M, Hoffmann AA. 1995. Cytoplasmic incompatibility in Drosophila simulans: dynamics and parameter estimates from natural populations. Genetics 140:1319-38
147. Veneti Z, Clark ME, Karr TL, Savakis C, Bourtzis K. 2004. Heads or tails: host-parasite interactions in the Drosophila-Wolbachia system. Appl. Environ. Microbiol. 70:5366-72
148. Voronin DA, Dudkina NV, Kiseleva EV. 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
149. Wasserman WJ, Smith LD. 1978. The cyclic behavior of a cytoplasmic factor controlling nuclear membrane breakdown. J. Cell Biol. 78:R15-22
150. Weeks AR, Turelli M, Harcombe WR, Reynolds KT, Hoffmann AA. 2007. From parasite to mutualist: rapid evolution of Wolbachia in natural populations of Drosophila. PLoS Biol. 5:e114
151. Werren JH. 1997. Biology of Wolbachia. Annu. Rev. Entomol. 42:587-609
152. Werren JH, Zhang W, Guo LR. 1995. Evolution and phylogeny of Wolbachia: reproductive parasites of arthropods. Proc. Biol. Sci. 261:55-63
153. Williams EH, Fields S, Saul GB 2nd. 1993. Transfer of incompatibility factors between stocks of Nasonia (=Mormoniella) vitripennis. J. Invertebr. Pathol. 61:206-10
154. Wiwatanaratanabutr S, Kittayapong P. 2006. Effects of temephos and temperature on Wolbachia load and life history traits of Aedes albopictus. Med. Vet. Entomol. 20:300-7
155. Wright JD, Barr AR. 1980. The ultrastructure and symbiotic relationships of Wolbachia of mosquitoes of the Aedes scutellaris group. J. Ultrastruct. Res. 72:52-64
156. Wright JD, Barr AR. 1981. Wolbachia and the normal and incompatible eggs of Aedes polynesiensis (Diptera: Culicidae). J. Invertebr. Pathol. 38:409-18
157. Wright JD, Sjostrand FS, Portaro JK, Barr AR. 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
158. Wu M, Sun LV, Vamathevan J, Riegler M, Deboy R, et al. 2004. Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: a streamlined genome overrun by mobile genetic elements. PLoS Biol. 2:E69
159. Xi Z, Dean JL, Khoo C, Dobson SL. 2005. Generation of a novel Wolbachia infection in Aedes albopictus (Asian tiger mosquito) via embryonic microinjection. Insect Biochem. Mol. Biol. 35:903-10
160. Yen JH, Barr AR. 1974. Incompatibility in Culex pipiens. In The Use of Genetics in Insect Control, ed. R Pal, MJ Whitten, pp. 97-118. Amsterdam: Elsevier
161. Yu KR, Saint RB, Sullivan W. 2000. The Grapes checkpoint coordinates nuclear envelope breakdown and chromosome condensation. Nat. Cell Biol. 2:609-15
162. Zabalou S, Apostolaki A, Pattas S, Veneti Z, Paraskevopoulos C, et al. 2008. Multiple rescue factors within a Wolbachia strain. Genetics 178:2145-60
163. Zchori-Fein E, Roush RT, Rosen D. 1998. Distribution of parthenogenesis-inducing symbionts in ovaries and eggs of Aphytis (Hymentoptera: Aphelinidae). Curr. Microbiol. 36:1-8