Ehrlichia chaffeensis infections in Drosophila melanogaster

Infection and Immunity

Volumn 77, Issue 11, 2009, Pages 4815-4826

  Luce Fedrow, Alison ^a   Von Ohlen, Tonia ^a   Chapes, Stephen K ^a  

^a KANSAS STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATTACIN; DIPTERICIN; DROSOMYCIN; POLYPEPTIDE ANTIBIOTIC AGENT; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; BLOOD CELL; CELLULAR IMMUNITY; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; EHRLICHIA CHAFFEENSIS; FEMALE; GENE MUTATION; HOST RESISTANCE; HUMAN GRANULOCYTIC ANAPLASMOSIS; HUMAN MONOCYTIC EHRLICHIOSIS; HUMORAL IMMUNITY; MACROPHAGE; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHAGOCYTOSIS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SURVIVAL RATE;

ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EHRLICHIA CHAFFEENSIS; EHRLICHIOSIS; FEMALE; HOST-PARASITE INTERACTIONS; MALE; MUTATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TOLL-LIKE RECEPTORS;

EID: 70350437304     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00594-09     Document Type: Article

References (67)

1. Anderson, K. V., G. Jurgens, and C. Nusslein-Volhard. 1985. Establishment of dorsal-ventral polarity in the Drosophila embryo: genetic studies on the role of the Toll gene product. Cell 42:779-789. (Pubitemid 16083719)
2. Anderson, K. V., and C. Nusslein-Volhard. 1984. Information for the dorsalventral pattern of the Drosophila embryo is stored as maternal mRNA. Nature 311:223-227.
3. Basset, A., R. S. Khush, A. Braun, L. Gardan, F. Boccard, J. A. Hoffmann, and B. Lemaitre. 2000. The phytopathogenic bacteria Erwinia carotovora infects Drosophila and activates an immune response. Proc. Natl. Acad. Sci. USA 97:3376-3381.
4. Belvin, M. P., and K. V. Anderson. 1996. A conserved signaling pathway: the Drosophila Toll-dorsal pathway. Annu. Rev. Cell Dev. Biol. 12:393-416.
5. Bergmann, A., D. Stein, R. Geisler, S. Hagenmaier, B. Schmid, N. Fernandez, B. Schnell, and C. Nusslein-Volhard. 1996. A gradient of cytoplasmic Cactus degradation establishes the nuclear localization gradient of the dorsal morphogen in Drosophila. Mech. Dev. 60:109-123.
6. Boutros, M., H. Agaisse, and N. Perrimon. 2002. Sequential activation of signaling pathways during innate immune responses in Drosophila. Dev. Cell 3:711-722. (Pubitemid 35339488)
7. Brandt, S. M., M. S. Dionne, R. S. Khush, L. N. Pham, T. J. Vigdal, and D. S. Schneider. 2004. Secreted bacterial effectors and host-produced Eiger/TNF drive death in a Salmonella-infected fruit fly. PLoS Biol. 2:e418.
8. Castillo, J. C., A. E. Robertson, and M. R. Strand. 2006. Characterization of hemocytes from the mosquitoes Anopheles gambiae and Aedes aegypti. Insect Biochem. Mol. Biol. 36:891-903.
9. Chapes, S. K., and A. A. Beharka. 1998. Salmonella infections in the absence of the major histocompatibility complex II. J. Leukoc. Biol. 63:297-304.
10. Chapes, S. K., and S. Haskill. 1982. Role of Corynebacterium parvum in the activation of peritoneal macrophages. 1. Association between intracellular C. parvum and cytotoxic macrophages. Cell. Immunol. 70:65-75.
11. Damas, J. K., M. Jensenius, T. Ueland, K. Otterdal, A. Yndestad, S. S. Froland, J. M. Rolain, B. Myrvang, D. Raoult, and P. Aukrust. 2006. Increased levels of soluble CD40L in African tick bite fever: possible involvement of TLRs in the pathogenic interaction between Rickettsia africae, endothelial cells, and platelets. J. Immunol. 177:2699-2706.
12. De Gregorio, E., P. T. Spellman, P. Tzou, G. M. Rubin, and B. Lemaitre. 2002. The Toll and Imd pathways are the major regulators of the immune response in Drosophila. EMBO J. 21:2568-2579. (Pubitemid 34619373)
13. Dionne, M. S., N. Ghori, and D. S. Schneider. 2003. Drosophila melanogaster is a genetically tractable model host for Mycobacterium marinum. Infect. Immun. 71:3540-3550.
14. Domanitskaya, E. V., H. Liu, S. Chen, and E. Kubli. 2007. The hydroxyproline motif of male sex peptide elicits the innate immune response in Drosophila females. FEBS J. 274:5659-5668.
15. Eicher, S. D., and D. S. McVey. 1995. Dietary modulation of Kupffer cell and splenocyte function during a Salmonella typhimurium challenge in mice. J. Leukoc. Biol. 58:32-39.
16. Elrod-Erickson, M., S. Mishra, and D. Schneider. 2000. Interactions between the cellular and humoral immune responses in Drosophila. Curr. Biol. 10:781-784.
17. Erturk-Hasdemir, D., M. Broemer, F. Leulier, W. S. Lane, N. Paquette, D. Hwang, C. H. Kim, S. Stoven, P. Meier, and N. Silverman. 2009. Two roles for the Drosophila IKK complex in the activation of Relish and the induction of antimicrobial peptide genes. Proc. Natl. Acad. Sci. USA 106:9779-9784.
18. Erturk-Hasdemir, D., N. Paquette, K. Aggarwal, and N. Silverman. 2008. Bug versus bug: humoral immune responses in Drosophila melanogaster, p. 43-63. In H. Heine (ed.), Innate immunity of plants, animals, and humans. Springer-Verlag, Berlin, Germany.
19. Fedorka, K. M., J. E. Linder, W. Winterhalter, and D. Promislow. 2007. Post-mating disparity between potential and realized immune response in Drosophila melanogaster. Proc. Biol. Sci. 274:1211-1217.
20. Felek, S., A. Unver, R. W. Stich, and Y. Rikihisa. 2001. Sensitive detection of Ehrlichia chaffeensis in cell culture, blood, and tick specimens by reverse transcription-PCR. J. Clin. Microbiol. 39:460-463.
21. Ganta, R. R., C. Cheng, E. C. Miller, B. L. McGuire, L. Peddireddi, K. R. Sirigireddy, and S. K. Chapes. 2007. Differential clearance and immune responses to tick cell-derived versus macrophage culture-derived Ehrlichia chaffeensis in mice. Infect. Immun. 75:135-145.
22. Ganta, R. R., M. J. Wilkerson, C. Cheng, A. M. Rokey, and S. K. Chapes. 2002. Persistent Ehrlichia chaffeensis infection occurs in the absence of functional major histocompatibility complex class II genes. Infect. Immun. 70: 380-388.
23. Hedengren-Olcott, M., M. C. Olcott, D. T. Mooney, S. Ekengren, B. L. Geller, and B. J. Taylor. 2004. Differential activation of the NF-kappaB-like factors Relish and Dif in Drosophila melanogaster by fungi and Grampositive bacteria. J. Biol. Chem. 279:21121-21127.
24. Hu, X., Y. Yagi, T. Tanji, S. Zhou, and Y. T. Ip. 2004. Multimerization and interaction of Toll and Spatzle in Drosophila. Proc. Natl. Acad. Sci. USA 101:9369-9374.
25. Huang, H., M. Lin, X. Wang, T. Kikuchi, H. Mottaz, A. Norbeck, and Y. Rikihisa. 2008. Proteomic analysis of and immune responses to Ehrlichia chaffeensis lipoproteins. Infect. Immun. 76:3405-3414.
26. Ivory, A., K. Randle, and L. Wu. 2008. Cellular immune responses in Drosophila melanogaster, p. 73-91. In H. Heine (ed.), Innate immunity of plants, animals, and humans. Springer-Verlag, Berlin, Germany.
27. Jordan, J. M., M. E. Woods, J. Olano, and D. H. Walker. 2008. The absence of Toll-like receptor 4 signaling in C3H/HeJ mice predisposes them to overwhelming rickettsial infection and decreased protective Th1 responses. Infect. Immun. 76:3717-3724.
28. Kavanagh, K., and E. Reeves. 2007. Insect and mammalian innate immune responses are much alike. Microbe 2:596-599. (Pubitemid 350291723)
29. Kurucz, E., B. Vaczi, R. Markus, B. Laurinyecz, P. Vilmos, J. Zsamboki, K. Csorba, E. Gateff, D. Hultmark, and I. Ando. 2007. Definition of Drosophila hemocyte subsets by cell-type specific antigens. Acta Biol. Hung. 58(Suppl): 95-111.
30. Lau, G. W., B. C. Goumnerov, C. L. Walendziewicz, J. Hewitson, W. Xiao, S. Mahajan-Miklos, R. G. Tompkins, L. A. Perkins, and L. G. Rahme. 2003. The Drosophila melanogaster Toll pathway participates in resistance to infection by the gram-negative human pathogen Pseudomonas aeruginosa. Infect. Immun. 71:4059-4066.
31. Lemaitre, B., and J. Hoffmann. 2007. The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 25:697-743.
32. Lemaitre, B., M. Meister, S. Govind, P. Georgel, R. Steward, J. M. Reichhart, and J. A. Hoffmann. 1995. Functional analysis and regulation of nuclear import of dorsal during the immune response in Drosophila. EMBO J. 14:536-545.
33. Lemaitre, B., E. Nicolas, L. Michaut, J. M. Reichhart, and J. A. Hoffmann. 1996. The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86:973-983. (Pubitemid 26336801)
34. Lemaitre, B., J. M. Reichhart, and J. A. Hoffmann. 1997. Drosophila host defense: differential induction of antimicrobial peptide genes after infection by various classes of microorganisms. Proc. Natl. Acad. Sci. USA 94:14614-14619.
35. Leulier, F., A. Rodriguez, R. S. Khush, J. M. Abrams, and B. Lemaitre. 2000. The Drosophila caspase Dredd is required to resist gram-negative bacterial infection. EMBO Rep. 1:353-358.
36. Levin, M. L., L. Killmaster, G. Zemtsova, D. Grant, K. Y. Mumcuoglu, M. E. Eremeeva, and G. A. Dasch. Incongruent effects of two isolates of Rickettsia conorii on the survival of Rhipicephalus sanguineus ticks. Exp. Appl. Acarol., in press.
37. Lin, M., and Y. Rikihisa. 2003. Ehrlichia chaffeensis and Anaplasma phagocytophilum lack genes for lipid A biosynthesis and incorporate cholesterol for their survival. Infect. Immun. 71:5324-5331.
38. Luce-Fedrow, A., T. Von Ohlen, D. Boyle, R. R. Ganta, and S. K. Chapes. 2008. Use of Drosophila S2 cells as a model for studying Ehrlichia chaffeensis infections. Appl. Environ. Microbiol. 74:1886-1891.
39. Maillet, F., V. Bischoff, C. Vignal, J. Hoffmann, and J. Royet. 2008. The Drosophila peptidoglycan recognition protein PGRP-LF blocks PGRP-LC and IMD/JNK pathway activation. Cell Host Microbe 3:293-303. (Pubitemid 351637430)
40. Mansfield, B. E., M. S. Dionne, D. S. Schneider, and N. E. Freitag. 2003. Exploration of host-pathogen interactions using Listeria monocytogenes and Drosophila melanogaster. Cell. Microbiol. 5:901-911.
41. McNabb, S. J., R. A. Jajosky, P. A. Hall-Baker, D. A. Adams, P. Sharp, C. Worshams, W. J. Anderson, A. J. Javier, G. J. Jones, D. A. Nitschke, A. Rey, and M. S. Wodajo. 2008. Summary of notifiable diseases-United States, 2006. MMWR Morb. Mortal. Wkly. Rep. 55:1-92.
42. Nehme, N. T., S. Liégeois, B. Kele, P. Giammarinaro, E. Pradel, J. A. Hoffmann, J. J. Ewbank, and D. Ferrandon. 2007. A model of bacterial intestinal infections in Drosophila melanogaster. PLoS Pathog. 2:1694-1709. (Pubitemid 350291605)
43. Nicolas, E., J. M. Reichhart, J. A. Hoffmann, and B. Lemaitre. 1998. In vivo regulation of the IkappaB homologue cactus during the immune response of Drosophila. J. Biol. Chem. 273:10463-10469.
44. Niebylski, M. L., M. G. Peacock, and T. G. Schwan. 1999. Lethal effect of Rickettsia rickettsii on its tick vector (Dermacentor andersoni). Appl. Environ. Microbiol. 65:773-778.
45. Paddock, C. D., and J. E. Childs. 2003. Ehrlichia chaffeensis: a prototypical emerging pathogen. Clin. Microbiol. Rev. 16:37-64.
46. Peng, J., P. Zipperlen, and E. Kubli. 2005. Drosophila sex-peptide stimulates female innate immune system after mating via the Toll and Imd pathways. Curr. Biol. 15:1690-1694.
47. Pham, L. N., M. S. Dionne, M. Shirasu-Hiza, and D. S. Schneider. 2007. A specific primed immune response in Drosophila is dependent on phagocytes. PLoS Pathog. 3:e26.
48. Pili-Floury, S., F. Leulier, K. Takahashi, K. Saigo, E. Samain, R. Ueda, and B. Lemaitre. 2004. In vivo RNA interference analysis reveals an unexpected role for GNBP1 in the defense against Gram-positive bacterial infection in Drosophila adults. J. Biol. Chem. 279:12848-12853.
49. Ray, R. P., K. Arora, C. Nusslein-Volhard, and W. M. Gelbart. 1991. The control of cell fate along the dorsal-ventral axis of the Drosophila embryo. Development 113:35-54.
50. Ross, D. E., and M. L. Levin. 2004. Effects of Anaplasma phagocytophilum infection on the molting success of Ixodes scapularis (Acari: Ixodidae) larvae. J. Med. Entomol. 41:476-483.
51. Roth, S., Y. Hiromi, D. Godt, and C. Nusslein-Volhard. 1991. Cactus, a maternal gene required for proper formation of the dorsoventralmorphogen gradient in Drosophila embryos. Development 112:371-388.
52. Schneider, D., and M. Shahabuddin. 2000. Malaria parasite development in a Drosophila model. Science 288:2376-2379. (Pubitemid 30448164)
53. Schneider, D. S., K. L. Hudson, T. Y. Lin, and K. V. Anderson. 1991. Dominant and recessive mutations define functional domains of Toll, a transmembrane protein required for dorsal-ventral polarity in the Drosophila embryo. Genes Dev. 5:797-807.
54. Shelton, C. A., and S. A. Wasserman. 1993. pelle encodes a protein kinase required to establish dorsoventral polarity in the Drosophila embryo. Cell 72:515-525. (Pubitemid 23077740)
55. Sirigireddy, K. R., and R. R. Ganta. 2005. Multiplex detection of Ehrlichia and Anaplasma species pathogens in peripheral blood by real-time reverse transcriptase-polymerase chain reaction. J. Mol. Diagn. 7:308-316.
56. Socolovschi, C., O. Mediannikov, D. Raoult, and P. Parola. 2009. The relationship between spotted fever group Rickettsiae and Ixodid ticks. Vet. Res. 40:34.
57. Stoven, S., N. Silverman, A. Junell, M. Hedengren-Olcott, D. Erturk, Y. Engstrom, T. Maniatis, and D. Hultmark. 2003. Caspase-mediated processing of the Drosophila NF-kappaB factor Relish. Proc. Natl. Acad. Sci. USA 100:5991-5996.
58. Tanji, T., X. Hu, A. N. Weber, and Y. T. Ip. 2007. Toll and IMD pathways synergistically activate an innate immune response in Drosophila melanogaster. Mol. Cell. Biol. 27:4578-4588.
59. Tauszig-Delamasure, S., H. Bilak, M. Capovilla, J. A. Hoffmann, and J. L. Imler. 2002. Drosophila MyD88 is required for the response to fungal and Gram-positive bacterial infections. Nat. Immunol. 3:91-97.
60. Telford, S. R., III, and J. E. Dawson. 1996. Persistent infection of C3H/HeJ mice by Ehrlichia chaffeensis. Vet. Microbiol. 52:103-112.
61. Towb, P., A. Bergmann, and S. A. Wasserman. 2001. The protein kinase Pelle mediates feedback regulation in the Drosophila Toll signaling pathway. Development 128:4729-4736.
62. Tzou, P., S. Ohresser, D. Ferrandon, M. Capovilla, J. M. Reichhart, B. Lemaitre, J. A. Hoffmann, and J. L. Imler. 2000. Tissue-specific inducible expression of antimicrobial peptide genes in Drosophila surface epithelia. Immunity 13:737-748.
63. Vodovar, N., C. Acosta, B. Lemaitre, and F. Boccard. 2004. Drosophila: a polyvalent model to decipher host-pathogen interactions. Trends Microbiol. 12:235-242. (Pubitemid 38534628)
64. Vonkavaara, M., M. V. Telepnev, P. Rydén, A. Sjöstedt, and S. Stöven. 2008. Drosophila melanogaster as a model for elucidating the pathogenicity of Francisella tularensis. Cell. Microbiol. 10:1327-1338.
65. Weber, A. N., S. Tauszig-Delamasure, J. A. Hoffmann, E. Lelievre, H. Gascan, K. P. Ray, M. A. Morse, J. L. Imler, and N. J. Gay. 2003. Binding of the Drosophila cytokine Spatzle to Toll is direct and establishes signaling. Nat. Immunol. 4:794-800.
66. Williams, M. J., M. L. Wiklund, S. Wikman, and D. Hultmark. 2006. Rac1 signalling in the Drosophila larval cellular immune response. J. Cell Sci. 119:2015-2024.
67. Zhang, J. Z., M. Sinha, B. A. Luxon, and X. J. Yu. 2004. Survival strategy of obligately intracellular Ehrlichia chaffeensis: novel modulation of immune response and host cell cycles. Infect. Immun. 72:498-507.