Asymmetric wolbachia segregation during Early Brugia malayi embryogenesis determines its distribution in adult host tissues

PLoS Neglected Tropical Diseases

Volumn 4, Issue 7, 2010, Pages

  Landmann, Frédéric ^a   Foster, Jeremy M ^b   Slatko, Barton ^b   Sullivan, William ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b NEW ENGLAND BIOLABS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BLASTOMERE; BRUGIA MALAYI; CELL DIVISION; CELL FUSION; CELL LINEAGE; CHROMOSOME SEGREGATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; FERTILIZATION; GERMLINE MICRONUCLEUS; HOST PARASITE INTERACTION; IMMUNOFLUORESCENCE; LYMPHATIC FILARIASIS; MALE; MEIOSIS; NEMATODE; NONHUMAN; SOMATIC CELL; SUBCUTANEOUS TISSUE; TISSUE DISTRIBUTION; WOLBACHIA; ZYGOTE; ANIMAL; ANIMAL ANATOMY; FLUORESCENT ANTIBODY TECHNIQUE; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; METHODOLOGY; MICROBIOLOGY; STAINING;

ANIMAL STRUCTURES; ANIMALS; BRUGIA MALAYI; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; MALE; STAINING AND LABELING; WOLBACHIA;

EID: 77957901428     PISSN: None     EISSN: None     Source Type: Journal    
DOI: 10.1371/journal.pntd.0000758     Document Type: Article

References (61)

1. Crompton DW (1999) How much human helminthiasis is there in the world? J Parasitol 85: 397-403.
2. Molyneux DH, Bradley M, Hoerauf A, Kyelem D, Taylor MJ (2003) Mass drug treatment for lymphatic filariasis and onchocerciasis. Trends Parasitol 19: 516-522.
3. Bandi C, Trees AJ, Brattig NW (2001) Wolbachia in filarial nematodes: evolutionary aspects and implications for the pathogenesis and treatment of filarial diseases. Vet Parasitol 98: 215-238.
4. Taylor MJ, Bandi C, Hoerauf A (2005) Wolbachia bacterial endosymbionts of filarial nematodes. Adv Parasitol 60: 245-284.
5. Hoerauf A, Mand S, Adjei O, Fleischer B, Buttner DW (2001) Depletion of wolbachia endobacteria in Onchocerca volvulus by doxycycline and microfilaridermia after ivermectin treatment. Lancet 357: 1415-1416.
6. Hoerauf A, Specht S, Buttner M, Pfarr K, Mand S, et al. (2008) Wolbachia endobacteria depletion by doxycycline as antifilarial therapy has macrofilaricidal activity in onchocerciasis: a randomized placebo-controlled study. Med Microbiol Immunol 197: 295-311.
7. Specht S, Mand S, Marfo-Debrekyei Y, Debrah AY, Konadu P, et al. (2008) Efficacy of 2- and 4-week rifampicin treatment on the Wolbachia of Onchocerca volvulus. Parasitol Res 103: 1303-1309.
8. Supali T, Djuardi Y, Pfarr KM, Wibowo H, Taylor MJ, et al. (2008) Doxycycline treatment of Brugia malayi-infected persons reduces microfilaremia and adverse reactions after diethylcarbamazine and albendazole treatment. Clin Infect Dis 46: 1385-1393.
9. Bazzocchi C, Ceciliani F, McCall JW, Ricci I, Genchi C, et al. (2000) Antigenic role of the endosymbionts of filarial nematodes: IgG response against the Wolbachia surface protein in cats infected with Dirofilaria immitis. Proc Biol Sci 267: 2511-2516.
10. Brattig NW, Rathjens U, Ernst M, Geisinger F, Renz A, et al. (2000) Lipopolysaccharide-like molecules derived from Wolbachia endobacteria of the filaria Onchocerca volvulus are candidate mediators in the sequence of inflammatory and antiinflammatory responses of human monocytes. Microbes Infect 2: 1147-1157.
11. Taylor MJ, Cross HF, Bilo K (2000) Inflammatory responses induced by the filarial nematode Brugia malayi are mediated by lipopolysaccharide-like activity from endosymbiotic Wolbachia bacteria. J Exp Med 191: 1429-1436.
12. Gillette-Ferguson I, Hise AG, Sun Y, Diaconu E, McGarry HF, et al. (2006) Wolbachia- and Onchocerca volvulus-induced keratitis (river blindness) is dependent on myeloid differentiation factor 88. Infect Immun 74: 2442-2445.
13. Saint Andre A, Blackwell NM, Hall LR, Hoerauf A, Brattig NW, et al. (2002) The role of endosymbiotic Wolbachia bacteria in the pathogenesis of river blindness. Science 295: 1892-1895.
14. Turner JD, Langley RS, Johnston KL, Gentil K, Ford L, et al. (2009) Wolbachia lipoprotein stimulates innate and adaptive immunity through Toll-like receptors 2 and 6 to induce disease manifestations of filariasis. J Biol Chem 284: 22364-22378.
15. Buckley JJ, Edeson JF (1956) On the adult morphology of Wuchereria sp. (malayi?) from a monkey (Macaca irus) and from cats in Malaya, and on Wuchereria pahangi n.sp. from a dog and a cat. J Helminthol 30: 1-20.
16. Cooray GH (1960) Some observations on filarial infection in Ceylon with special reference to its histopathology. Indian J Malariol 14: 617-632.
17. Schacher JF (1962) Developmental stages of Brugia pahangi in the final host. J Parasitol 48: 693-706.
18. Franz M, Buttner DW (1986) Histology of adult Brugia malayi. Trop Med Parasitol 37: 282-285.
19. Kozek WJ (1977) Transovarially-transmitted intracellular microorganisms in adult and larval stages of Brugia malayi. J Parasitol 63: 992-1000.
20. McLaren DJ, Worms MJ, Laurence BR, Simpson MG (1975) Micro-organisms in filarial larvae (Nematoda). Trans R Soc Trop Med Hyg 69: 509-514.
21. Sironi M, Bandi C, Sacchi L, Di Sacco B, Damiani G, et al. (1995) Molecular evidence for a close relative of the arthropod endosymbiont Wolbachia in a filarial worm. Mol Biochem Parasitol 74: 223-227.
22. Williams SA, Lizotte-Waniewski MR, Foster J, Guiliano D, Daub J, et al. (2000) The filarial genome project: analysis of the nuclear, mitochondrial and endosymbiont genomes of Brugia malayi. Int J Parasitol 30: 411-419.
23. Taylor MJ, Bilo K, Cross HF, Archer JP, Underwood AP (1999) 16S rDNA phylogeny and ultrastructural characterization of Wolbachia intracellular bacteria of the filarial nematodes Brugia malayi, B. pahangi, and Wuchereria bancrofti. Exp Parasitol 91: 356-361.
24. McGarry HF, Egerton GL, Taylor MJ (2004) Population dynamics of Wolbachia bacterial endosymbionts in Brugia malayi. Mol Biochem Parasitol 135: 57-67.
25. Fenn K, Blaxter M (2004) Quantification of Wolbachia bacteria in Brugia malayi through the nematode lifecycle. Mol Biochem Parasitol 137: 361-364.
26. Ward S, Carrel JS (1979) Fertilization and sperm competition in the nematode Caenorhabditis elegans. Dev Biol 73: 304-321.
27. Goldstein B, Hird SN (1996) Specification of the anteroposterior axis in Caenorhabditis elegans. Development 122: 1467-1474.
28. Lahl V, Halama C, Schierenberg E (2003) Comparative and experimental embryogenesis of Plectidae (Nematoda). Dev Genes Evol 213: 18-27.
29. Skiba F, Schierenberg E (1992) Cell lineages, developmental timing, and spatial pattern formation in embryos of free-living soil nematodes. Dev Biol 151: 597-610.
30. Dolinski CJBG, Thomas WK (2001) Comparative survey of early embryogenesis of Secernetea (Nematoda), with phylogenetic implication. Can J Zool 79: 82-94.
31. Goldstein B (2001) On the evolution of early development in the Nematoda. Philos Trans R Soc Lond B Biol Sci 356: 1521-1531.
32. Malakhov VV (1994) Nematodes, Structure, Development, Classification and Phylogeny: Smithsonian Institution Press.
33. Sulston JE, Schierenberg E, White JG, Thomson JN (1983) The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 100: 64-119.
34. Chisholm AD, Hardin J (2005) Epidermal morphogenesis WormBook. pp 1-22.
35. Schaner CE, Deshpande G, Schedl PD, Kelly WG (2003) A conserved chromatin architecture marks and maintains the restricted germ cell lineage in worms and flies. Dev Cell 5: 747-757.
36. Pinskaya M, Morillon A (2009) Histone H3 Lysine 4 di-methylation: a novel mark for transcriptional fidelity? Epigenetics 4: 302-306.
37. Albertson R, Casper-Lindley C, Cao J, Tram U, Sullivan W (2009) Symmetric and asymmetric mitotic segregation patterns influence Wolbachia distribution in host somatic tissue. J Cell Sci 122: 4570-4583.
38. Sato H, Kusel JR, Thornhill J (2002) Functional visualization of the excretory system of adult Schistosoma mansoni by the fluorescent marker resorufin. Parasitology 125: 527-535.
39. Ferree PM, Frydman HM, Li JM, Cao J, Wieschaus E, et al. (2005) Wolbachia utilizes host microtubules and Dynein for anterior localization in the Drosophila oocyte. PLoS Pathog 1: e14.
40. Schneider SQ, Bowerman B (2003) Cell polarity and the cytoskeleton in the Caenorhabditis elegans zygote. Annu Rev Genet 37: 221-249.
41. Goldstein B, Macara IG (2007) The PAR proteins: fundamental players in animal cell polarization. Dev Cell 13: 609-622.
42. Serbus LR, Sullivan W (2007) A cellular basis for Wolbachia recruitment to the host germline. PLoS Pathog 3: e190.
43. Serbus LR, Casper-Lindley C, Landmann F, Sullivan W (2008) The Genetic and Cell Biology of Wolbachia-host Interactions. Annu Rev Genet.
44. Hunter CP, Kenyon C (1996) Spatial and temporal controls target pal-1 blastomere-specification activity to a single blastomere lineage in C. elegans embryos. Cell 87: 217-226.
45. Baugh LR, Hill AA, Claggett JM, Hill-Harfe K, Wen JC, et al. (2005) The homeodomain protein PAL-1 specifies a lineage-specific regulatory network in the C. elegans embryo. Development 132: 1843-1854.
46. Casiraghi M, McCall JW, Simoncini L, Kramer LH, Sacchi L, et al. (2002) Tetracycline treatment and sex-ratio distortion: a role for Wolbachia in the moulting of filarial nematodes? Int J Parasitol 32: 1457-1468.
47. Sakaguchi Y, Tada I, Ash LR, Aoki Y (1983) Karyotypes of Brugia pahangi and Brugia malayi (Nematoda: Filarioidea). J Parasitol 69: 1090-1093.
48. Ercan S, Lieb JD (2009) C. elegans dosage compensation: a window into mechanisms of domain-scale gene regulation. Chromosome Res 17: 215-227.
49. Chuang PT, Lieb JD, Meyer BJ (1996) Sex-specific assembly of a dosage compensation complex on the nematode X chromosome. Science 274: 1736-1739.
50. Lieb JD, Capowski EE, Meneely P, Meyer BJ (1996) DPY-26, a link between dosage compensation and meiotic chromosome segregation in the nematode. Science 274: 1732-1736.
51. Bird AFB, Bird J (1991) The structure of Nematodes: Academic Press.
52. Howells RE, Chen SN (1981) Brugia pahangi: feeding and nutrient uptake in vitro and in vivo. Exp Parasitol 51: 42-58.
53. Ghedin E, Hailemariam T, Depasse JV, Zhang X, Oksov Y, et al. (2009) Brugia malayi Gene Expression in Response to the Targeting of the Wolbachia Endosymbiont by Tetracycline Treatment. PLoS Negl Trop Dis 3: e525.
54. Bandi C, McCall JW, Genchi C, Corona S, Venco L, et al. (1999) Effects of tetracycline on the filarial worms Brugia pahangi and Dirofilaria immitis and their bacterial endosymbionts Wolbachia. Int J Parasitol 29: 357-364.
55. Hoerauf A, Volkmann L, Nissen-Paehle K, Schmetz C, Autenrieth I, et al. (2000) Targeting of Wolbachia endobacteria in Litomosoides sigmodontis: comparison of tetracyclines with chloramphenicol, macrolides and ciprofloxacin. Trop Med Int Health 5: 275-279.
56. Bennuru S, Semnani R, Meng Z, Ribeiro JM, Veenstra TD, et al. (2009) Brugia malayi excreted/secreted proteins at the host/parasite interface: stage- and gender-specific proteomic profiling. PLoS Negl Trop Dis 3: e410.
57. Hoerauf A (2003) Control of filarial infections: not the beginning of the end, but more research is needed. Curr Opin Infect Dis 16: 403-410.
58. Kozek WJ (2005) What is new in the Wolbachia/Dirofilaria interaction? Vet Parasitol 133: 127-132.
59. Brattig NW, Buttner DW, Hoerauf A (2001) Neutrophil accumulation around Onchocerca worms and chemotaxis of neutrophils are dependent on Wolbachia endobacteria. Microbes Infect 3: 439-446.
60. Gillette-Ferguson I, Hise AG, McGarry HF, Turner J, Esposito A, et al. (2004) Wolbachia-induced neutrophil activation in a mouse model of ocular onchocerciasis (river blindness). Infect Immun 72: 5687-5692.
61. Gillette-Ferguson I, Daehnel K, Hise AG, Sun Y, Carlson E, et al. (2007) Tolllike receptor 2 regulates CXC chemokine production and neutrophil recruitment to the cornea in Onchocerca volvulus/Wolbachia-induced keratitis. Infect Immun 75: 5908-5915.