期刊论文详细信息
Particle and Fibre Toxicology
Localization of Wolbachia-like gene transcripts and peptides in adult Onchocerca flexuosa worms indicates tissue specific expression
Peter U Fischer2  Norbert W Brattig1  Gary J Weil2  Kurt C Curtis2  Kerstin Fischer2  Samantha N McNulty2 
[1] Bernhard Nocht Institute for Tropical Medicine, Hamburg, Germany;Infectious Diseases Division, Department of Internal Medicine, Washington University School of Medicine, Saint Louis, MO, 63110, USA
关键词: Wolbachia;    immunohistology;    in situ hybridization;    horizontal gene transfer;    Filariasis;   
Others  :  1228102
DOI  :  10.1186/1756-3305-6-2
 received in 2012-11-05, accepted in 2012-12-20,  发布年份 2013
【 摘 要 】

Background

Most filarial species in the genus Onchocerca depend on Wolbachia endobacteria to successfully carry out their life cycle. O. flexuosa is a Wolbachia-free species, but its genome contains Wolbachia-like sequences presumably obtained from Wolbachia via horizontal gene transfer. Proteogenomic studies have shown that many of these Wolbachia-like sequences are expressed in adult worms.

Methods

Six Wolbachia-like sequences in O. flexuosa were chosen for further study based on their sequence conservation with Wolbachia genes, length of predicted open reading frames, and expression at the RNA and/or protein levels. In situ hybridization and immunohistochemical labeling were used to localize Wolbachia-like transcripts and peptides in adult worm tissues.

Results

RNA probes representing three of the six target sequences produced hybridization signals in worm tissues. These probes bound to transcripts in the intestine and lateral chords of both sexes, in the hypodermis, median chords and uteri in females, and in sperm precursor cells in males. Antibodies raised to three peptides corresponding to these transcripts bound to specific bands in a soluble extract of adult O. flexuosa by Western blot that were not labeled by control antibodies in pre-immune serum. Two of the three antibodies produced labeling patterns in adult worm sections that were similar to those of the RNA probes, while the third produced a different pattern.

Conclusions

A subset of the Wolbachia-like sequences present in the genome of the Wolbachia-free filarial species O. flexuosa are transcribed in tissues where Wolbachia reside in infected filarial species. Some of the peptides and/or proteins derived from these transcripts appear to be concentrated in the same tissues while others may be exported to other regions of the worm. These results suggest that horizontally transferred Wolbachia genes and gene products may replicate important Wolbachia functions in uninfected filarial worms.

【 授权许可】

   
2013 McNulty et al.; licensee BioMed Central Ltd.

附件列表
Files Size Format View
Figure 8. 200KB Image download
Figure 7. 213KB Image download
Figure 6. 205KB Image download
Figure 5. 211KB Image download
Figure 4. 146KB Image download
Figure 3. 266KB Image download
Figure 2. 177KB Image download
Figure 1. 10KB Image download
Figure 8. 200KB Image download
Figure 7. 213KB Image download
Figure 6. 205KB Image download
Figure 5. 211KB Image download
Figure 4. 146KB Image download
Figure 3. 266KB Image download
Figure 2. 177KB Image download
Figure 1. 10KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

Figure 8.

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

Figure 8.

【 参考文献 】
  • [1]Taylor MJ, Bandi C, Hoerauf A: Wolbachia bacterial endosymbionts of filarial nematodes. Adv Parasitol 2005, 60:245-284.
  • [2]Hoerauf A, Nissen-Pahle K, Schmetz C, Henkle-Duhrsen K, Blaxter ML, Buttner DW, Gallin MY, Al-Qaoud KM, Lucius R, Fleischer B: Tetracycline therapy targets intracellular bacteria in the filarial nematode Litomosoides sigmodontis and results in filarial infertility. J Clin Invest 1999, 103:11-18.
  • [3]Slatko BE, Taylor MJ, Foster JM: The Wolbachia endosymbiont as an anti-filarial nematode target. Symbiosis 2010, 51:55-65.
  • [4]Rao RU, Moussa H, Weil GJ: Brugia malayi: effects of antibacterial agents on larval viability and development in vitro. Exp Parasitol 2002, 101:77-81.
  • [5]Bandi C, Anderson TJ, Genchi C, Blaxter ML: Phylogeny of Wolbachia in filarial nematodes. Proc Biol Sci 1998, 265:2407-2413.
  • [6]Casiraghi M, Bain O, Guerrero R, Martin C, Pocacqua V, Gardner SL, Franceschi A, Bandi C: Mapping the presence of Wolbachia pipientis on the phylogeny of filarial nematodes: evidence for symbiont loss during evolution. Int J Parasitol 2004, 34:191-203.
  • [7]Ferri E, Bain O, Barbuto M, Martin C, Lo N, Uni S, Landmann F, Baccei SG, Guerrero R, de Souza Lima S, et al.: New Insights into the Evolution of Wolbachia Infections in Filarial Nematodes Inferred from a Large Range of Screened Species. PLoS One 2011, 6:e20843.
  • [8]McNulty SN, Foster JM, Mitreva M, Dunning Hotopp JC, Martin J, Fischer K, Wu B, Davis PJ, Kumar S, Brattig NW, et al.: Endosymbiont DNA in endobacteria-free filarial nematodes indicates ancient horizontal genetic transfer. PLoS One 2010, 5:e11029.
  • [9]McNulty SN, Mullin AS, Vaughan JA, Tkach VV, Weil GJ, Fischer PU: Comparing the Mitochondrial Genomes of Wolbachia-Dependent and Independent Filarial Nematode Species. BMC Genomics 2012, 13:145. BioMed Central Full Text
  • [10]McNulty SN, Abubucker S, Simon GM, Mitreva M, McNulty NP, Fischer K, Curtis KC, Brattig NW, Weil GJ, Fischer PU: Transcriptomic and Proteomic Analyses of a Wolbachia-Free Filarial Parasite Provide Evidence of Trans-Kingdom Horizontal Gene Transfer. PLoS One 2012, 7:e45777.
  • [11]Dunning Hotopp JC, Clark ME, Oliveira DC, Foster JM, Fischer P, Munoz Torres MC, Giebel JD, Kumar N, Ishmael N, Wang S, et al.: Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 2007, 317:1753-1756.
  • [12]Fischer K, Beatty WL, Jiang D, Weil GJ, Fischer PU: Tissue and Stage-Specific Distribution of Wolbachia in Brugia malayi. PLoS Negl Trop Dis 2011, 5:e1174.
  • [13]Landmann F, Foster JM, Slatko B, Sullivan W: Asymmetric Wolbachia segregation during early Brugia malayi embryogenesis determines its distribution in adult host tissues. PLoS Negl Trop Dis 2010, 4:e758.
  • [14]Kozek WJ: Transovarially-transmitted intracellular microorganisms in adult and larval stages of Brugia malayi. J Parasitol 1977, 63:992-1000.
  • [15]Kozek WJ, Marroquin HF: Intracytoplasmic bacteria in Onchocerca volvulus. AmJTrop Med Hyg 1977, 26:663-678.
  • [16]McLaren DJ, Worms MJ, Laurence BR, Simpson MG: Micro-organisms in filarial larvae (Nematoda). Trans R Soc Trop Med Hyg 1975, 69:509-514.
  • [17]Landmann F, Bain O, Martin C, Uni S, Taylor MJ, Sullivan W: Both asymmetric mitotic segregation and cell-to-cell invasion are required for stable germline transmission of Wolbachia in filarial nematodes. Biology Open 2012, 1:536-547.
  • [18]Plenge-Bonig A, Kromer M, Buttner DW: Light and electron microscopy studies on Onchocerca jakutensis and O. flexuosa of red deer show different host-parasite interactions. Parasitol Res 1995, 81:66-73.
  • [19]Michalski ML, Griffiths KG, Williams SA, Kaplan RM, Moorhead AR: The NIH-NIAID Filariasis Research Reagent Resource Center. PLoS Negl Trop Dis 2011, 5:e1261.
  • [20]Martin J, Abubucker S, Heizer E, Taylor CM, Mitreva M: Nematode.net update 2011: addition of data sets and tools featuring next-generation sequencing data. Nucleic Acids Res 2012, 40:D720-D728.
  • [21]Jiang D, Li BW, Fischer PU, Weil GJ: Localization of gender-regulated gene expression in the filarial nematode Brugia malayi. Int J Parasitol 2008, 38:503-512.
  • [22]Buttner DW, Wanji S, Bazzocchi C, Bain O, Fischer P: Obligatory symbiotic Wolbachia endobacteria are absent from Loa loa. Filaria J 2003, 2:10. BioMed Central Full Text
  • [23]Fath MJ, Kolter R: ABC transporters: bacterial exporters. Microbiol Rev 1993, 57:995-1017.
  • [24]Bennuru S, Meng Z, Ribeiro JM, Semnani RT, Ghedin E, Chan K, Lucas DA, Veenstra TD, Nutman TB: Stage-specific proteomic expression patterns of the human filarial parasite Brugia malayi and its endosymbiont Wolbachia. Proc Natl Acad Sci USA 2011, 108:9649-9654.
  • [25]Kanehisa M, Goto S: KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 2000, 28:27-30.
  • [26]Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M: KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res 2012, 40:D109-D114.
  • [27]Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, Krylov DM, Mazumder R, Mekhedov SL, Nikolskaya AN, et al.: The COG database: an updated version includes eukaryotes. BMC Bioinforma 2003, 4:41. BioMed Central Full Text
  • [28]Tatusov RL, Koonin EV, Lipman DJ: A genomic perspective on protein families. Science 1997, 278:631-637.
  • [29]Foster J, Ganatra M, Kamal I, Ware J, Makarova K, Ivanova N, Bhattacharyya A, Kapatral V, Kumar S, Posfai J, et al.: The Wolbachia genome of Brugia malayi: endosymbiont evolution within a human pathogenic nematode. PLoS Biol 2005, 3:e121.
  • [30]Darby AC, Armstrong SD, Bah GS, Kaur G, Hughes MA, Kay SM, Koldkjaer P, Radford AD, Blaxter ML, Tanya VN, et al.: Analysis of gene expression from the Wolbachia genome of a filarial nematode supports both metabolic and defensive roles within the symbiosis. Genome Res 2012, 22(12):2467-2477.
  • [31]Ghedin E, Wang S, Spiro D, Caler E, Zhao Q, Crabtree J, Allen JE, Delcher AL, Guiliano DB, Miranda-Saavedra D, et al.: Draft genome of the filarial nematode parasite Brugia malayi. Science 2007, 317:1756-1760.
  • [32]Scott AL, Ghedin E: The genome of Brugia malayi - all worms are not created equal. Parasitol Int 2009, 58:6-11.
  • [33]Bennuru S, Semnani R, Meng Z, Ribeiro JM, Veenstra TD, Nutman TB: Brugia malayi excreted/secreted proteins at the host/parasite interface: stage- and gender-specific proteomic profiling. PLoS Negl Trop Dis 2009, 3:e410.
  文献评价指标  
  下载次数:67次 浏览次数:19次