Characterization of Transcription Factors That Regulate the Type IV Secretion System and Riboflavin Biosynthesis in Wolbachia of Brugia malayi

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Li, Zhiru ^a   Carlow, Clotilde K S ^a  

^a NEW ENGLAND BIOLABS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOXYCYCLINE; RIBOFLAVIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR WBMXR1; TRANSCRIPTION FACTOR WBMXR2; UNCLASSIFIED DRUG; VIRB PROTEIN;

ARTICLE; BRUGIA MALAYI; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVITY; FERTILITY; GENE; GENE EXPRESSION REGULATION; GENE INTERACTION; HOST; NONHUMAN; NUCLEOTIDE SEQUENCE; NUTRITIONAL VALUE; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; RIBA GENE; SYMBIONT; TRANSCRIPTION REGULATION; TYPE IV SECRETION SYSTEM; VIRB4 2 GENE; VIRB8 1 GENE; VIRB9 2 GENE; VITAMIN METABOLISM; VITAMIN SUPPLEMENTATION; WBMXR1 GENE; WBMXR2 GENE; WOLBACHIA;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; BIOSYNTHETIC PATHWAYS; BRUGIA MALAYI; DNA, INTERGENIC; DOXYCYCLINE; GENE EXPRESSION REGULATION, BACTERIAL; GENES, REPORTER; HOST-PARASITE INTERACTIONS; HUMANS; LIFE CYCLE STAGES; MOLECULAR SEQUENCE DATA; OPERON; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RECOMBINANT PROTEINS; RIBOFLAVIN; SEQUENCE HOMOLOGY, AMINO ACID; TRANSCRIPTION FACTORS; WOLBACHIA;

BACTERIA (MICROORGANISMS); BRUGIA MALAYI; WOLBACHIA;

EID: 84870955829     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0051597     Document Type: Article

References (62)

1. Hoerauf A, Volkmann L, Hamelmann C, Adjei O, Autenrieth IB, et al. (2000) Endosymbiotic bacteria in worms as targets for a novel chemotherapy in filariasis. Lancet 355: 1242-1243.
2. 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.
3. Taylor MJ, Makunde WH, McGarry HF, Turner JD, Mand S, et al. (2005) Macrofilaricidal activity after doxycycline treatment of Wuchereria bancrofti: a double-blind, randomised placebo-controlled trial. Lancet 365: 2116-2121.
4. Debrah AY, Mand S, Marfo-Debrekyei Y, Batsa L, Albers A, et al. (2011) Macrofilaricidal Activity in Wuchereria bancrofti after 2 Weeks Treatment with a Combination of Rifampicin plus Doxycycline. J Parasitol Res 2011: 201617.
5. Debrah AY, Mand S, Specht S, Marfo-Debrekyei Y, Batsa L, et al. (2006) Doxycycline reduces plasma VEGF-C/sVEGFR-3 and improves pathology in lymphatic filariasis. PLoS Pathog 2: e92.
6. Debrah AY, Mand S, Marfo-Debrekyei Y, Batsa L, Pfarr K, et al. (2007) Macrofilaricidal effect of 4 weeks of treatment with doxycycline on Wuchereria bancrofti. Trop Med Int Health 12: 1433-1441.
7. Hoerauf A, Marfo-Debrekyei Y, Buttner M, Debrah AY, Konadu P, et al. (2008) Effects of 6-week azithromycin treatment on the Wolbachia endobacteria of Onchocerca volvulus. Parasitol Res 103: 279-286.
8. Mand S, Pfarr K, Sahoo PK, Satapathy AK, Specht S, et al. (2009) Macrofilaricidal activity and amelioration of lymphatic pathology in bancroftian filariasis after 3 weeks of doxycycline followed by single-dose diethylcarbamazine. Am J Trop Med Hyg 81: 702-711.
9. Jeyaprakash A, Hoy MA, (2000) Long PCR improves Wolbachia DNA amplification: wsp sequences found in 76% of sixty-three arthropod species. Insect Mol Biol 9: 393-405.
10. Werren JH, Windsor DM, (2000) Wolbachia infection frequencies in insects: evidence of a global equilibrium? Proc Biol Sci 267: 1277-1285.
11. Bennett GM, Pantoja NA, O'Grady PM (2012) Diversity and phylogenetic relationships of Wolbachia in Drosophila and other native Hawaiian insects. Fly (Austin) 6.
12. Zug R, 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.
13. Sunish IP, Rajendran R, Paramasivan R, Dhananjeyan KJ, Tyagi BK, (2011) Wolbachia endobacteria in a natural population of Culex quinquefasciatus from filariasis endemic villages of south India and its phylogenetic implication. Trop Biomed 28: 569-576.
14. McGraw EA, O'Neill SL, (2004) Wolbachia pipientis: intracellular infection and pathogenesis in Drosophila. Curr Opin Microbiol 7: 67-70.
15. Narita S, Kageyama D, Nomura M, Fukatsu T, (2007) Unexpected mechanism of symbiont-induced reversal of insect sex: feminizing Wolbachia continuously acts on the butterfly Eurema hecabe during larval development. Appl Environ Microbiol 73: 4332-4341.
16. Werren JH, (1997) Biology of Wolbachia. Annu Rev Entomol 42: 587-609.
17. Alvarez-Martinez CE, Christie PJ, (2009) Biological diversity of prokaryotic type IV secretion systems. Microbiol Mol Biol Rev 73: 775-808.
18. Llosa M, Roy C, Dehio C, (2009) Bacterial type IV secretion systems in human disease. Mol Microbiol 73: 141-151.
19. Zechner EL, Lang S, Schildbach JF, (2012) Assembly and mechanisms of bacterial type IV secretion machines. Philos Trans R Soc Lond B Biol Sci 367: 1073-1087.
20. Christie PJ, Atmakuri K, Krishnamoorthy V, Jakubowski S, Cascales E, (2005) Biogenesis, architecture, and function of bacterial type IV secretion systems. Annu Rev Microbiol 59: 451-485.
21. Pichon S, Bouchon D, Cordaux R, Chen L, Garrett RA, et al. (2009) Conservation of the Type IV secretion system throughout Wolbachia evolution. Biochem Biophys Res Commun 385: 557-562.
22. Masui S, Sasaki T, Ishikawa H, (2000) Genes for the type IV secretion system in an intracellular symbiont, Wolbachia, a causative agent of various sexual alterations in arthropods. J Bacteriol 182: 6529-6531.
23. Rances E, Voronin D, Tran-Van V, Mavingui P, (2008) Genetic and functional characterization of the type IV secretion system in Wolbachia. J Bacteriol 190: 5020-5030.
24. Felix C, Pichon S, Braquart-Varnier C, Braig H, Chen L, et al. (2008) Characterization and transcriptional analysis of two gene clusters for type IV secretion machinery in Wolbachia of Armadillidium vulgare. Res Microbiol 159: 481-485.
25. Martinez-Nunez C, Altamirano-Silva P, Alvarado-Guillen F, Moreno E, Guzman-Verri C, et al. (2010) The two-component system BvrR/BvrS regulates the expression of the type IV secretion system VirB in Brucella abortus. J Bacteriol 192: 5603-5608.
26. de Jong MF, Sun YH, den Hartigh AB, van Dijl JM, Tsolis RM, (2008) Identification of VceA and VceC, two members of the VjbR regulon that are translocated into macrophages by the Brucella type IV secretion system. Mol Microbiol 70: 1378-1396.
27. Altman E, Segal G, (2008) The response regulator CpxR directly regulates expression of several Legionella pneumophila icm/dot components as well as new translocated substrates. J Bacteriol 190: 1985-1996.
28. Zusman T, Aloni G, Halperin E, Kotzer H, Degtyar E, et al. (2007) The response regulator PmrA is a major regulator of the icm/dot type IV secretion system in Legionella pneumophila and Coxiella burnetii. Mol Microbiol 63: 1508-1523.
29. Cheng Z, Wang X, Rikihisa Y, (2008) Regulation of type IV secretion apparatus genes during Ehrlichia chaffeensis intracellular development by a previously unidentified protein. J Bacteriol 190: 2096-2105.
30. Kelley LA, Sternberg MJ, (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4: 363-371.
31. Mathews SA, Volp KM, Timms P, (1999) Development of a quantitative gene expression assay for Chlamydia trachomatis identified temporal expression of sigma factors. FEBS Lett 458: 354-358.
32. Li Z, Garner AL, Gloeckner C, Janda KD, Carlow CK, (2011) Targeting the Wolbachia cell division protein FtsZ as a new approach for antifilarial therapy. PLoS Negl Trop Dis 5: e1411.
33. Simons RW, Houman F, Kleckner N, (1987) Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene 53: 85-96.
34. Miller MA, editor (1972) Experiments in Moleculary Genetics: Cold Spring Harbor Laboratory. 352-355 p.
35. Rao RU, Moussa H, Weil GJ, (2002) Brugia malayi: effects of antibacterial agents on larval viability and development in vitro. Exp Parasitol 101: 77-81.
36. Wang X, Kikuchi T, Rikihisa Y, (2007) Proteomic identification of a novel Anaplasma phagocytophilum DNA binding protein that regulates a putative transcription factor. J Bacteriol 189: 4880-4886.
37. Aravind L, Anantharaman V, Balaji S, Babu MM, Iyer LM, (2005) The many faces of the helix-turn-helix domain: transcription regulation and beyond. FEMS Microbiol Rev 29: 231-262.
38. Kozek WJ, (1977) Transovarially-transmitted intracellular microorganisms in adult and larval stages of Brugia malayi. J Parasitol 63: 992-1000.
39. 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.
40. McGarry HF, Egerton GL, Taylor MJ, (2004) Population dynamics of Wolbachia bacterial endosymbionts in Brugia malayi. Mol Biochem Parasitol 135: 57-67.
41. Baron C, (2006) VirB8: a conserved type IV secretion system assembly factor and drug target. Biochem Cell Biol 84: 890-899.
42. Ghedin E, Wang S, Spiro D, Caler E, Zhao Q, et al. (2007) Draft genome of the filarial nematode parasite Brugia malayi. Science 317: 1756-1760.
43. 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.
44. Debrah AY, Mand S, Marfo-Debrekyei Y, Larbi J, Adjei O, et al. (2006) Assessment of microfilarial loads in the skin of onchocerciasis patients after treatment with different regimens of doxycycline plus ivermectin. Filaria J 5: 1.
45. Hoerauf A, Specht S, Marfo-Debrekyei Y, Buttner M, Debrah AY, et al. (2009) Efficacy of 5-week doxycycline treatment on adult Onchocerca volvulus. Parasitol Res 104: 437-447.
46. Baron C, Coombes B, (2007) Targeting bacterial secretion systems: benefits of disarmament in the microcosm. Infect Disord Drug Targets 7: 19-27.
47. Ohashi N, Zhi N, Lin Q, Rikihisa Y, (2002) Characterization and transcriptional analysis of gene clusters for a type IV secretion machinery in human granulocytic and monocytic ehrlichiosis agents. Infect Immun 70: 2128-2138.
48. Rikihisa Y, Lin M, Niu H, (2010) Type IV secretion in the obligatory intracellular bacterium Anaplasma phagocytophilum. Cell Microbiol 12: 1213-1221.
49. Rikihisa Y, Lin M, Niu H, Cheng Z, (2009) Type IV secretion system of Anaplasma phagocytophilum and Ehrlichia chaffeensis. Ann N Y Acad Sci 1166: 106-111.
50. Darby AC, Armstrong SD, Bah GS, Kaur G, Hughes MA, et al. (2012) Analysis of gene expression from the Wolbachia genome of a filarial nematode supports both metabolic and defensive roles within the symbiosis. Genome Res.
51. Paschos A, den Hartigh A, Smith MA, Atluri VL, Sivanesan D, et al. (2011) An in vivo high-throughput screening approach targeting the type IV secretion system component VirB8 identified inhibitors of Brucella abortus 2308 proliferation. Infect Immun 79: 1033-1043.
52. Fernandez-Lopez R, Machon C, Longshaw CM, Martin S, Molin S, et al. (2005) Unsaturated fatty acids are inhibitors of bacterial conjugation. Microbiology 151: 3517-3526.
53. Hilleringmann M, Pansegrau W, Doyle M, Kaufman S, MacKichan ML, et al. (2006) Inhibitors of Helicobacter pylori ATPase Cagalpha block CagA transport and cag virulence. Microbiology 152: 2919-2930.
54. Bennuru S, Meng Z, Ribeiro JM, Semnani RT, Ghedin E, et al. (2011) Stage-specific proteomic expression patterns of the human filarial parasite Brugia malayi and its endosymbiont Wolbachia. Proc Natl Acad Sci U S A 108: 9649-9654.
55. Abbas CA, Sibirny AA, (2011) Genetic control of biosynthesis and transport of riboflavin and flavin nucleotides and construction of robust biotechnological producers. Microbiol Mol Biol Rev 75: 321-360.
56. 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.
57. Hosokawa T, Koga R, Kikuchi Y, Meng XY, Fukatsu T, (2010) Wolbachia as a bacteriocyte-associated nutritional mutualist. Proc Natl Acad Sci U S A 107: 769-774.
58. Zientz E, Dandekar T, Gross R, (2004) Metabolic interdependence of obligate intracellular bacteria and their insect hosts. Microbiol Mol Biol Rev 68: 745-770.
59. Lamelas A, Gosalbes MJ, Manzano-Marin A, Pereto J, Moya A, et al. (2011) Serratia symbiotica from the aphid Cinara cedri: a missing link from facultative to obligate insect endosymbiont. PLoS Genet 7: e1002357.
60. Nakabachi A, Ishikawa H, (1999) Provision of riboflavin to the host aphid, Acyrthosiphon pisum, by endosymbiotic bacteria, Buchnera. J Insect Physiol 45: 1-6.
61. Bermingham J, Rabatel A, Calevro F, Vinuelas J, Febvay G, et al. (2009) Impact of host developmental age on the transcriptome of the symbiotic bacterium Buchnera aphidicola in the pea aphid (Acyrthosiphon pisum). Appl Environ Microbiol 75: 7294-7297.
62. Wu B, Novelli J, Foster J, Vaisvila R, Conway L, et al. (2009) The heme biosynthetic pathway of the obligate Wolbachia endosymbiont of Brugia malayi as a potential anti-filarial drug target. PLoS Negl Trop Dis 3: e475.