Interaction of francisella asiatica with tilapia (oreochromis niloticus) innate immunity

Infection and Immunity

Volumn 78, Issue 5, 2010, Pages 2070-2078

  Soto, Esteban ^a   Fernandez, Denise ^a   Thune, Ronald ^a   Hawke, John P ^a  

^a LOUISIANA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MANNOSE RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERICIDAL ACTIVITY; BACTERIUM MUTANT; BLOOD SAMPLING; CELL VACUOLE; CONTROLLED STUDY; CYTOPLASM; CYTOTOXICITY; ELECTRON MICROSCOPY; FRANCISELLA; FRANCISELLA ASIATICA; GENE; HEAT; IN VITRO STUDY; INNATE IMMUNITY; INOCULATION; KIDNEY; MACROPHAGE; MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; TILAPIA; WILD TYPE;

ANIMALS; APOPTOSIS; BACTERIAL PROTEINS; BLOOD BACTERICIDAL ACTIVITY; CELL SURVIVAL; CICHLIDS; CYTOPLASM; FRANCISELLA; GENE DELETION; GENETIC COMPLEMENTATION TEST; IMMUNITY, INNATE; MACROPHAGES; MICROSCOPY, ELECTRON, TRANSMISSION; SERUM; VACUOLES; VIRULENCE FACTORS;

EID: 77951242174     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01308-09     Document Type: Article

References (63)

1. Abd, H., T. Johansson, I. Golovliov, G. Sandstrom, and M. Forsman. 2003. Survival and growth of Francisella tularensis in Acanthamoeba castellanii. Appl. Environ. Microbiol. 69:600-606.
2. Acosta, F., A. E. Ellis, J. Vivas, D. Padilla, B. Acosta, S. Deniz, J. Bravo, and F. Real. 2006. Complement consumption by Photobacterium damselae subsp. piscicida in seabream, red porgy and seabass normal and immune serum. Effect of the capsule on the bactericidal effect. Fish Shellfish Immunol. 20:709-717.
3. Allen, L. A. 2003. Mechanisms of pathogenesis: evasion of killing by polymorphonuclear leukocytes. Microbes Infect. 5:1329-1335.
4. Anthony, L. S. D., R. D. Burke, and F. E. Nano. 1991. Growth of Francisella spp. in rodent macrophages. Infect. Immun. 59:3291-3296.
5. Baker, C. N., D. G. Hollis, and C. Thornsberry. 1985. Antimicrobial susceptibility testing of Francisella tularensis with a modified Mueller-Hinton broth. J. Clin. Microbiol. 22:212-215.
6. Balagopal, A., A. S. MacFarlane, N. Mohapatra, S. Soni, J. S. Gunn, and L. S. Schlesinger. 2006. Characterization of the receptor-ligand pathways important for entry and survival of Francisella tularensis in human macrophages. Infect. Immun. 74:5114-5125.
7. Barker, J. R., and K. E. Klose. 2007. Molecular and genetic basis of pathogenesis in Francisella tularensis. Ann. N. Y. Acad. Sci. 1105:138-159.
8. Barnes, A. C., C. Guyot, B. G. Hansen, K. Mackenzie, M. T. Horne, and A. E. Ellis. 2002. Resistance to serum killing may contribute to differences in the abilities of capsulate and non-capsulated isolates of Lactococcus garvieae to cause disease in rainbow trout (Oncorhynchus mykiss L.). Fish Shellfish Immunol. 12:155-168.
9. Barnes, C. A., F. M. Young, M. T. Horne, and A. E. Ellis. 2003. Streptococcus iniae: serological differences, presence of capsule and resistance to immune serum killing. Dis. Aquat. Org. 53:241-247.
10. Baron, G. S., and F. E. Nano. 1998. MglA and MglB are required for the intramacrophage growth of Francisella novicida. Mol. Microbiol. 29:247-259.
11. Barreda, D. R., and M. Belosevic. 2001. Characterization of growth enhancing factor production in different phases of in vitro fish macrophage development. Fish Shellfish Immunol. 11:169-185.
12. Ben Nasr, A., J. Haithcoat, J. E. Masterson, J. S. Gunn, T. Eaves-Pyles, and G. R. Klimpel. 2006. Critical role for serum opsonins and complement receptors CR3 (CD11b/CD18) and CR4 (CD11c/CD18) in phagocytosis of Francisella tularensis by human dendritic cells (DC): uptake of Francisella leads to activation of immature DC and intracellular survival of the bacteria. J. Leukoc. Biol. 80:774-786.
13. Ben Nasr, A., and G. R. Klimpel. 2008. Subversion of complement activation at the bacterial surface promotes serum resistance and opsonophagocytosis of Francisella tularensis. J. Leukoc. Biol. 84:77-85.
14. Birkbeck, T. H., M. Bordevik, M. K. Frøystad, and Å Baklien. 2007. Identification of Francisella sp. from atlantic salmon, Salmo salar L., in Chile. J. Fish Dis. 30:505-507. (Pubitemid 47074913)
15. Bönquist, L., H. Lindgren, I. Golovliov, T. Guina, and A. Sjöstedt. 2008. MglA and Igl proteins contribute to the modulation of Francisella tularensis live vaccine strain-containing phagosomes in murine macrophages. Infect. Immun. 76:3502-3510.
16. Booth, N. J., A. Elkamel, and R. L. Thune. 2006. Intracellular replication of Edwardsiella ictaluri in channel catfish macrophages. J. Aquat. Anim. Health 18:101-108.
17. Brotcke, A., D. S. Weiss, C. C. Kim, P. Chain, S. Malfatti, E. Garcia, and D. M. Monack. 2006. Identification of MglA-regulated genes reveals novel virulence factors in Francisella tularensis. Infect. Immun. 74:6642-6655.
18. Clemens, D. L., B.-Y Lee, and M. A. Horwitz. 2005. Francisella tularensis enters macrophages via a novel process involving pseudopod loops. Infect. Immun. 73:5892-5902.
19. Clemens, D. L., and M. A. Horwitz. 2007. Uptake and intracellular fate of Francisella tularensis in human macrophages. Ann. N. Y. Acad. Sci. 1105:160-186.
20. de Bruin, O. M., J. S. Ludu, and F. E. Nano. 2007. The Francisella pathogenicity island protein IglA localizes to the bacterial cytoplasm and is needed for intracellular growth. BMC Microbiol. 7:1.
21. Dennis, D. T., T. V. Inglesby, D. A. Henderson, J. G. Bartlett, M. S. Ascher, E. Eitzen, A. D. Fine, A. M. Friedlander, J. Hauer, M. Layton, S. R. Lillibridge, J. E. McDade, M. T. Osterholm, T. O'Toole, G. Parker, T. M. Perl, P. K. Russell, and K. Tonat. 2001. Tularemia as a biological weapon: medical and public health management. JAMA 285:2763-2773. (Pubitemid 32525374)
22. Elkamel, A. A., J. P. Hawke, W. G. Henk, and R. L. Thune. 2003. Photobacterium damselae subsp. piscicida is capable of replicating in hybrid striped bass macrophages. J. Aquat. Anim. Health 15:175-183.
23. Ellsaesser, C., N. Miller, C. J. Lobb, and L. W. Clem. 1984. A new method for the cytochemical staining of cells immobilized in agarose. Histochemistry 80:559-562. (Pubitemid 14087264)
24. Gessani, S., L. Fantuzzi, P. Puddu, and F. Belardelli. 2000. Purification of macrophages, p. 31-60. In D. M. Paulnock (ed.), Macrophages: a practical approach. Oxford University Press, Oxford, United Kingdom.
25. Golovliov, I., M. Ericsson, G. Sandstrom, A. Tarnvik, and A. Sjöstedt. 1997. Identification of proteins of Francisella tularensis induced during growth in macrophages and cloning of the gene encoding a prominently induced 23-kilodalton protein. Infect. Immun. 65:2183-2189.
26. Golovliov, I., V. Baranov, Z. Krocova, H. Kovarova, and A. Sjöstedt. 2003. An attenuated strain of the facultative intracellular bacterium Francisella tularensis can escape the phagosome of monocytic cells. Infect. Immun. 71:5940-5950.
27. Gomez, D. G., and J. L. Balcazar. 2008. A review on the interactions between gut microbiota and innate immunity of fish. FEMS Immunol. Med. Microbiol. 52:145-154.
28. Gunn, J. S., and R. K. Ernst. 2007. The structure and function of Francisella lipopolysaccharide. Ann. N. Y. Acad. Sci. 1105:202-218.
29. Hood, A. M. 1977. Virulence factors of Francisella tularensis. J. Hyg. 79:47-60.
30. Hsieh, C. Y., M. C. Tung, C. Tu, C. D. Chang, and S. S. Tsai. 2006. Enzootics of visceral granulomas associated with Francisella-like organism infection in tilapia (Oreochromis spp.). Aquaculture 254:129-138.
31. Kamaishi, T., Y. Fukuda, M. Nishiyama, H. Kawakami, T. Matsuyama, T. Yoshinaga, and N. Oseko. 2005. Identification and pathogenicity of intracellular Francisella bacterium in three-line grunt Parapristipoma trilineatum. Fish Pathol. 40:67-71. (Pubitemid 41360628)
32. Kay, W., B. O. Petersen, J. Ø. Duus, M. B. Perry, and E. Vinogradov. 2006. Characterization of the lipopolysaccharide and beta-glucan of the fish pathogen Francisella victoria. FEBS J. 273:3002-3013.
33. Keim, P., A. Johansson, and D. M. Wagner. 2007. Molecular epidemiology, evolution, and ecology of Francisella. Ann. N. Y. Acad. Sci. 1105:30-66.
34. Lai, X. H., I. Golovliov, and A. Sjostedt. 2001. Francisella tularensis induces cytopathogenicity and apoptosis in murine macrophages via a mechanism that requires intracellular bacterial multiplication. Infect. Immun. 69:4691-4694.
35. Lai, X. H., I. Golovliov, and A. Sjostedt. 2004. Expression of IglC is necessary for intracellular growth and induction of apoptosis in murine macrophages by Francisella tularensis. Microb. Pathog. 37:225-230.
36. Lauriano, C. M., J. R. Barker, F. E. Nano, B. P. Arulanandam, and K. E. Klose. 2003. Allelic exchange in Francisella tularensis using PCR products. FEMS Microbiol. Lett. 229:195-202.
37. Lauriano, C. M., J. R. Barker, S. S. Yoon, F. E. Nano, B. P. Arulanandam, D. J. Hassett, and K. E. Klose. 2004. MglA regulates transcription of virulence factors necessary for Francisella tularensis intraamoebae and intramacrophage survival. Proc. Natl. Acad. Sci. U. S. A. 101:4246-4249.
38. Lindgren, H., I. Golovliov, V. Baranov, R. K. Ernst, M. Telepnev, and A. Sjöstedt. 2004. Factors affecting the escape of Francisella tularensis from the phagolysosome. J. Med. Microbiol. 53:953-958.
39. Ludu, J. S., O. M. de Bruin, B. N. Duplantis, C. L. Schmerk, A. Y. Chou, K. L. Elkins, and F. E. Nano. 2008. The Francisella pathogenicity island protein PdpD is required for full virulence and associates with homologues of the type VI secretion system. J. Bacteriol. 190:4584-4595.
40. Mauel, M. J., E. Soto, J. A. Morales, and J. Hawke. 2007. A piscirickettsiosis-like syndrome in cultured Nile tilapia in Latin America with Francisella spp. as the pathogenic agent. J. Aquat. Anim. Health 19:27-34.
41. McCarthy, U. M., J. E. Bron, L. Brown, F. Pourahmad, I. R. Bricknell, K. D. Thompson, A. Adams, and A. E. Ellis. 2008. Survival and replication of Piscirickettsia salmonis in rainbow trout head kidney macrophages. Fish Shellfish Immunol. 25:477-484.
42. Mikalsen, J., A. B. Olsen, T. Tengs, and D. J. Colquohoun. 2007. Francisella philomiragia subsp noatunensis subsp nov., isolated from farmed Atlantic cod (Gadus morhua L). Int. J. Syst. Evol. Microbiol. 57:1960-1965.
43. Mikalsen, J., and D. J. Colquhoun. 2009. Francisella asiatica sp. nov. isolated from farmed tilapia (Oreochromis sp.) and elevation of Francisella philomiragia subsp. noatunensis to species rank as Francisella noatunensis comb. nov., sp. nov. Int. J. Syst. Evol. Microbiol. [Epub ahead of print.] doi: 10.1099/ijs.0.002139-0.
44. Miles, D. J. C., S. Kanchanakhan, J. H. Lilley, K. D. Thompson, S. Chinabut, and A. Adams. 2001. Effect of macrophages and serum of fish susceptible or resistant to epizootic ulcerative syndrome (EUS) on the EUS pathogen, Aphanomyces invadans. Fish Shellfish Immunol. 11:569-584.
45. Nano, F. E., N. Zhang, S. C. Cowley, K. E. Klose, K. K. Cheung, M. J. Roberts, J. S. Ludu, G. W. Letendre, A. I. Meierovics, G. Stephens, and K. L. Elkins. 2004. A Francisella tularensis pathogenicity island required for intramacrophage growth. J. Bacteriol. 186:6430-6436.
46. Nano, F. E., and C. Schmerk. 2007. The Francisella pathogenicity island. Ann. N. Y. Acad. Sci. 1105:122-137.
47. Neumann, N. F., D. R. Barreda, and M. Belosevic. 2000. Generation and functional analysis of distinct macrophage sub-populations from goldfish (Carassius auratus L.) kidney leukocyte cultures. Fish Shellfish Immunol. 10:1-20.
48. Ostland, V. E., J. A. Stannard, J. J. Creek, R. P. Hedrick, H. W. Ferguson, J. M. Carlberg, and M. E. Westerman. 2006. Aquatic Francisella-like bacterium associated with mortality of intensively cultured hybrid striped bass Morone chrysops x M. saxatilis. Dis. Aquat. Org 72:135-145.
49. Ottem, K. F., A. Nylund, E. Karlsbakk, A. Friis-Moller, B. Krossoy, and D. Knappskog. 2007. New species in the genus Francisella (Gammaproteobacteria; Francisellaceae); Francisella piscicida sp. nov. isolated from cod (Gadus morhua). Arch. Microbiol. 188:547-550.
50. Ottem, K. F., A. Nylund, E. Karlsbakk, A. Friis-Moller, and T. Kamaishi. 2009. Elevation of Francisella philomiragia subsp. noatunensis Mikalsen et al. (2007) to Francisella noatunensis comb. nov. [syn. Francisella piscicida Ottem et al. (2008) syn. nov.] and characterization of Francisella noatunensis subsp. orientalis subsp. nov., two important fish pathogens. J. Appl. Microbiol. 106:1231-1243.
51. Pierini, L. M. 2006. Uptake of serum-opsonized Francisella tularensis by macrophages can be mediated by class A scavenger receptors. Cell. Microbiol. 8:1361-1370.
52. Ray, K., B. Marteyn, P. J. Sansonetti, and C. M. Tang. 2009. Life on the inside: the intracellular lifestyle of cytosolic bacteria. Nat. Rev. Microbiol. 7:333-340.
53. Santic, M., M. Molmeret, K. E. Klose, S. Jones, and Y. A. Kwaik. 2005. The Francisella tularensis pathogenicity island protein IglC and its regulator MglA are essential for modulating phagosome biogenesis and subsequent bacterial escape into the cytoplasm. Cell. Microbiol. 7:969-979.
54. Schulert, G. S., and L.-H. Allen. 2006. Differential infection of mononuclear phagocytes by Francisella tularensis: role of the macrophage mannose receptor. J. Leukoc. Biol. 80:563-571.
55. Secombes, C. J. 1990. Isolation of salmonid macrophages and analysis of their killing acticity, p. 137-154. In J. S. Stolen, T. C. Fletcher, D. P. Anderson, B. S. Robertson, and W. B. van Muiswinkel (ed.), Techniques in fish immunology, vol. 1. SOS Publications, Fair Haven, NJ.
56. Sjostedt, A. 2007. Tularemia: history, epidemiology, pathogen physiology, an clinical manifestations. Ann. N. Y. Acad. Sci. 1105:1-29.
57. Soto, E., J. Hawke, D. Fernandez, and J. A. Morales. 2009. Francisella sp., an emerging pathogen of tilapia (Oreochromis niloticus) in Costa Rica. J. Fish Dis. 32:713-722.
58. Soto, E., D. Fernandez, and J. P. Hawke. 2009. Attenuation of the fish pathogen Francisella sp. by mutation of the iglC gene. J. Aquat. Anim. Health 21:140-149.
59. Stafford, J. L., N. F. Neumann, and M. Belosevic. 2001. Products of proteolytic cleavage of transferrin induce nitric oxide response of goldfish macrophages. Dev. Comp. Immunol. 25:101-115.
60. Vojtech, L. N., G. E. Sanders, C. Conway, V. Ostland, and J. D. Hansen. 2009. Host immune response and acute disease in a zebrafish model of Francisella pathogenesis. Infect. Immun. 77:914-925.
61. Vonkavaara, M., M. V. Telepnev, P. Ryden, A. Sjostedt, and S. Stoven. 2008. Drosophila melanogaster as a model for elucidating the pathogenicity of Francisella tularensis. Cell. Microbiol. 10:1327-1338.
62. Wiklund, T., and I. Dalsgaard. 2002. Survival of Flavobacterium psychrophilum in rainbow trout (Oncorhynchus mykiss) serum in vitro. Fish Shellfish Immunol. 12:141-153. (Pubitemid 34140155)
63. Zogaj, X., S. Chakraborty, J. Liu, D. G. Thanassi, and K. E. Klose. 2008. Characterization of the Francisella tularensis subsp. novicida type IV pilus. Microbiology 154:2139-2150.