The involvement of Aeromonas salmonicida virulence factors in bacterial translocation across the rainbow trout, Oncorhynchus mykiss (Walbaum), intestine

Journal of Fish Diseases

Volumn 31, Issue 2, 2008, Pages 141-151

  Jutfelt, F ^a   Sundh, H ^a   Glette, J ^b   Mellander, L ^a   Thrandur Bjornsson B ^a   Sundell, K ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b INSTITUTE OF MARINE RESEARCH   (Norway)

Author keywords

Barrier function; Fish; Furunculosis; Intestinal epithelium; Teleost; Ussing chamber

Indexed keywords

LIPOPOLYSACCHARIDE; VIRULENCE FACTOR;

AEROMONAS SALMONICIDA; ANIMAL; ANIMAL DISEASE; ARTICLE; BACTERIAL TRANSLOCATION; DRUG EFFECT; FISH DISEASE; FURUNCULOSIS; GRAM NEGATIVE INFECTION; HEAT; IMPEDANCE; INTESTINE; MICROBIAL VIABILITY; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; RAINBOW TROUT; TIME;

AEROMONAS SALMONICIDA; ANIMALS; BACTERIAL TRANSLOCATION; ELECTRIC IMPEDANCE; FISH DISEASES; FURUNCULOSIS; GRAM-NEGATIVE BACTERIAL INFECTIONS; HEAT; INTESTINES; LIPOPOLYSACCHARIDES; MICROBIAL VIABILITY; ONCORHYNCHUS MYKISS; TIME FACTORS; VIRULENCE FACTORS;

AEROMONAS SALMONICIDA; BACTERIA (MICROORGANISMS); ONCORHYNCHUS MYKISS; SALMONIDAE; TELEOSTEI;

EID: 38449083275     PISSN: 01407775     EISSN: 13652761     Source Type: Journal    
DOI: 10.1111/j.1365-2761.2007.00879.x     Document Type: Article

References (66)

1. Arnesen J., Eggset G. Jorgensen T.O. (1995) Partial purification and characterization of extracellular metalloproteases from Aeromonas salmonicidas ssp. salmonicida. Journal of Fish Diseases 18, 283 295.
2. Aschenbach J.R., Seidler T., Ahrens F., Schrodl W., Buchholz I., Garz B., Kruger M. Gabel G. (2003) Luminal salmonella endotoxin affects epithelial and mast cell function in the proximal colon of pigs. Scandinavian Journal of Gastroenterology 38, 719 726.
3. Beutler B., Hoebe K., Du X. Ulevitch R.J. (2003) How we detect microbes and respond to them: the Toll-like receptors and their transducers. Journal of Leucocyte Biology 74, 479 485.
4. Björnsson B.Th., Sundell K., Jönsson E., Jutfelt F., Geurden I., Ruohonen K., Forsman A., Olsen R.E. Ringo E. (2004) GUTINTEGRITY - Gastrointestinal Functions and Food Intake Regulation in Salmonids: Impact of Dietary Vegetable Lipids. EU project Q5RS-2000-31656 Final Report, Göteborgs Universitet, Göteborg.
5. Burr S.E., Stuber K., Wahli T. Frey J. (2002) Evidence for a type III secretion system in Aeromonas salmonicida subsp. salmonicida. Journal of Bacteriology 184, 5966 5970.
6. Burr S.E., Pugovkin D., Wahli T., Segner H. Frey J. (2005) Attenuated virulence of an Aeromonas salmonicida subsp. salmonicida type III secretion mutant in a rainbow trout model. Microbiology 151, 2111 2118.
7. Cipriano R.C. Bullock G.L. (2001) Furunculosis and Other Diseases Caused by Aeromonas salmonicida. Fish Disease Leaflet, USGS, National Fish Health Laboratory, Kearneysville, W. Virginia.
8. Cossart P. Sansonetti P.J. (2004) Bacterial invasion: the paradigms of enteroinvasive pathogens. Science 304, 242 248.
9. Dalmo R.A. Bogwald J. (1996) Distribution of intravenously and perorally administered Aeromonas salmonicida lipopolysaccharide in Atlantic salmon, Salmo salar L. Fish & Shellfish Immunology 6, 427 441.
10. Ellis A. (1991) An appraisal of the extracellular toxins of Aeromonas salmonicida ssp. salmonicida. Journal of Fish Diseases 14, 265 277.
11. Ellis A.E. (1997) Immunization with bacterial antigens: furunculosis. Developments in Biological Standardisation 90, 107 116.
12. Ellis A.E. (1998) Meeting the requirements for delayed release of oral vaccines for fish. Journal of Applied Ichthyology 14, 149 152.
13. Fasano A. (2002) Toxins and the gut: role in human disease. Gut 50 (Suppl. 3 III9 III14.
14. Fasano A. Nataro J.P. (2004) Intestinal epithelial tight junctions as targets for enteric bacteria-derived toxins. Advances in Drug Delivery Reviews 56, 795 807.
15. Ferguson Y., Bricknell I.R., Glover L.A., Macgregor D.M. Prosser J.I. (1998) Colonisation and transmission of lux-marked and wild-type Aeromonas salmonicida strains in Atlantic salmon (Salmo salar L.). FEMS Microbiology Ecology 27, 251 260.
16. Fujihara M., Muroi M., Tanamoto K., Suzuki T., Azuma H. Ikeda H. (2003) Molecular mechanisms of macrophage activation and deactivation by lipopolysaccharide: roles of the receptor complex. Pharmacological Therapeutics 100, 171 194.
17. Garduno R.A., Phipps B.M. Kay W.W. (1995) Physical and functional s-layer reconstitution in Aeromonas salmonicida. Journal of Bacteriology 177, 2684 2694.
18. Garduno R.A., Moore A.R., Olivier G., Lizama A.L., Garduno E. Kay W.W. (2000) Host cell invasion and intracellular residence by Aeromonas salmonicida: role of the S-layer. Canadian Journal of Microbiology 46, 660 668.
19. Georgopoulou U. Vernier J.M. (1986) Local immunological response in the posterior intestinal segment of the rainbow trout after oral administration of macromolecules. Developmental and Comparative Immunology 10, 529 537.
20. Go L.L., Healey P.J., Watkins S.C., Simmons R.L. Rowe M.I. (1995) The effect of endotoxin on intestinal mucosal permeability to bacteria in vitro. Archives of Surgery 130, 53 58.
21. Goetz F.W., Iliev D.B., McCauley L.A., Liarte C.Q., Tort L.B., Planas J.V. Mackenzie S. (2004) Analysis of genes isolated from lipopolysaccharide- stimulated rainbow trout (Oncorhynchus mykiss) macrophages. Molecular Immunology 41, 1199 1210.
22. Grisez L., Chair M., Sorgeloos P. Ollevier F. (1996) Mode of infection and spread of Vibrio anguillarum in turbot Scophthalmus maximus larvae after oral challenge through live feed. Diseases of Aquatic Organisms 26, 181 187.
23. Gudding R., Lillehaug A. Evensen O. (1999) Recent developments in fish vaccinology. Veterinary Immunology and Immunopathology 72, 203 212.
24. Hansen G.H. Olafsen J.A. (1999) Bacterial interactions in early life stages of marine cold water fish. Microbial Ecology 38, 1 26.
25. Hart S., Wrathmell A.B., Harris J.E. Grayson T.H. (1988) Gut immunology in fish: a review. Developmental and Comparative Immunology 12, 453 480.
26. Hastein T., Gudding R. Evensen O. (2005) Bacterial vaccines for fish - an update of the current situation worldwide. Developments in Biology (Basel) 121, 55 74.
27. Hussain I., Mackie C., Cox D., Alderson R. Birkbeck T.H. (2000) Suppression of the humoral immune response of Atlantic salmon (Salmo salar L.) by the 64 kDa serine protease of Aeromonas salmonicida. Fish & Shellfish Immunology 10, 359 373.
28. Iliev D.B., Liarte C.Q., MacKenzie S. Goetz F.W. (2005a) Activation of rainbow trout (Oncorhynchus mykiss) mononuclear phagocytes by different pathogen associated molecular pattern (PAMP) bearing agents. Molecular Immunology 42, 1215 1223.
29. Iliev D.B., Roach J.C., Mackenzie S., Planas J.V. Goetz F.W. (2005b) Endotoxin recognition: in fish or not in fish? FEBS Letters 579, 6519 6528.
30. Inglis V., Roberts R.J. Bromage N.R. (1993) Bacterial Diseases of Fish. Blackwell Scientific Publications, Oxford.
31. Jutfelt F. (2006) The Intestinal Epithelium of Salmonids: Transepithelial Transport, Barrier Function and Bacterial Interactions. PhD thesis, Department of Zoology/Zoophysiology, Göteborg University, Göteborg, Sweden.
32. Jutfelt F., Olsen R.E., Glette J., Ringo E. Sundell K. (2006) Translocation of viable Aeromonas salmonicida across the intestine of rainbow trout, Oncorhynchus mykiss (Walbaum). Journal of Fish Diseases 29, 255 262.
33. Jutfelt F., Olsen R.E., Björnsson B.Th. Sundell K. (2007) Parr-smolt transformation and dietary vegetable lipids affect intestinal nutrient uptake, barrier function and plasma cortisol levels in Atlantic salmon. doi :.
34. Kucharzik T., Lugering N., Rautenberg K., Lugering A., Schmidt M.A., Stoll R. Domschke W. (2000) Role of M cells in intestinal barrier function. Annals of the New York Academy of Sciences 915, 171 183.
35. Kurkchubasche A.G., Cardona M., Watkins S.C., Smith S.D., Albanese C.T., Simmons R.L., Rowe M.I. Ford H.R. (1998) Transmucosal passage of bacteria across rat intestinal epithelium in the Ussing chamber: effect of nutritional factors and bacterial virulence. Shock 9, 121 127.
36. Lee K.K. Ellis A.E. (1990) Glycerophospholipid:cholesterol acyltransferase complexed with lipopolysaccharide (LPS) is a major lethal exotoxin and cytolysin of Aeromonas salmonicida: LPS stabilizes and enhances toxicity of the enzyme. Journal of Bacteriology 172, 5382 5393.
37. Lødemel J.B., Mayhew T.M., Myklebust R., Olsen R.E., Espelid S. Ringø E. (2001) Effect of three dietary oils on disease susceptibility in Arctic charr (Salvelinus alpinus L.) during cohabitant challenge with Aeromonas salmonicida ssp. salmonicida. Aquaculture Research 32, 935 945.
38. Masada C.L., LaPatra S.E., Morton A.W. Strom M.S. (2002) An Aeromonas salmonicida type IV pilin is required for virulence in rainbow trout Oncorhynchus mykiss. Diseases of Aquatic Organisms 51, 13 25.
39. McNamara B.P., Koutsouris A., O'Connell C.B., Nougayrede J.P., Donnenberg M.S. Hecht G. (2001) Translocated EspF protein from enteropathogenic Escherichia coli disrupts host intestinal barrier function. Journal of Clinical Investigation 107, 621 629.
40. Munford R.S. (2005) Detoxifying endotoxin: time, place and person. Journal of Endotoxin Research 11, 69 84.
41. Mutoloki S., Brudeseth B., Reite O.B. Evensen O. (2006) The contribution of Aeromonas salmonicida extracellular products to the induction of inflammation in Atlantic salmon (Salmo salar L.) following vaccination with oil-based vaccines. Fish & Shellfish Immunology 20, 1 11.
42. Nikoskelainen S., Ouwehand A.C., Bylund G., Salminen S. Lilius E.M. (2003) Immune enhancement in rainbow trout (Oncorhynchus mykiss) by potential probiotic bacteria (Lactobacillus rhamnosus). Fish & Shellfish Immunology 15, 443 452.
43. Noonan B. Trust T.J. (1997) The synthesis, secretion and role in virulence of the paracrystalline surface protein layers of Aeromonas salmonicida and A. hydrophila. FEMS Microbiology Letters 154, 1 7.
44. Nougayrede J.P., Fernandes P.J. Donnenberg M.S. (2003) Adhesion of enteropathogenic Escherichia coli to host cells. Cell Microbiology 5, 359 372.
45. O'Donnell G.B., Smith P.R., Kilmartin J.J. Moran A.P. (1994) Uptake and fate of orally administered bacterial lipopolysaccharide in brown trout (Salmo trutta). Fish & Shellfish Immunology 4, 285 299.
46. O'Toole R., Von Hofsten J., Rosqvist R., Olsson P.E. Wolf-Watz H. (2004) Visualisation of zebrafish infection by GFP-labelled Vibrio anguillarum. Microbial Pathogenesis 37, 41 46.
47. Olsson J.C., Jöborn A., Westerdahl A., Blomberg L., Kjelleberg S. Conway P.L. (1996) Is the turbot, Scophthalmus maximus (L.), intestine a portal of entry for the fish pathogen Vibrio anguillarum? Journal of Fish Diseases 19, 225 234.
48. Osman N.E., Westrom B. Karlsson B. (1998) Serosal but not mucosal endotoxin exposure increases intestinal permeability in vitro in the rat. Scandinavian Journal of Gastroenterology 33, 1170 1174.
49. Parsot C. (2005) Shigella spp. and enteroinvasive Escherichia coli pathogenicity factors. FEMS Microbiology Letters 252, 11 18.
50. Paulsen S.M., Lunde H., Engstad R.E. Robertsen B. (2003) In vivo effects of beta-glucan and LPS on regulation of lysozyme activity and mRNA expression in Atlantic salmon (Salmo salar L.). Fish & Shellfish Immunology 14, 39 54.
51. Petrie A.G. Ellis A.E. (2006) Evidence of particulate uptake by the gut of Atlantic salmon (Salmo salar L.). Fish & Shellfish Immunology 20, 660 664.
52. Press C.M. Lillehaug A. (1995) Vaccination in European salmonid aquaculture: a review of practices and prospects. British Veterinary Journal 151, 45 69.
53. Ringø E. Olsen R.E. (1999) The effect of diet on aerobic bacterial flora associated with intestine of Arctic charr (Salvelinus alpinus L.). Journal of Applied Microbiology 86, 22 28.
54. Ringo E., Jutfelt F., Kanapathippillai P., Bakken Y., Sundell K., Glette J., Mayhew T.M., Myklebust R. Olsen R.E. (2004) Damaging effect of the fish pathogen Aeromonas salmonicida ssp. salmonicida on intestinal enterocytes of Atlantic salmon (Salmo salar L.). Cell & Tissue Research 318, 305 311.
55. Ringø E., Lodemel J.B., Myklebust R., Kaino T., Mayhew T.M. Olsen R.E. (2001) Epithelium-associated bacteria in the gastrointestinal tract of Arctic charr (Salvelinus alpinus L.). An electron microscopical study. Journal of Applied Microbiology 90, 294 300.
56. Ringø E., Olsen R.E., Mayhew T.M. Myklebust R. (2003) Electron microscopy of the intestinal microflora of fish. Aquaculture 227, 395 415.
57. Rombout J.H.W.M. Joosten P.H.M. (1998) Immunology of fishes. In: Handbook of Vertebrate Immunology (ed. by P.P. Pastoret, P. Griebel, H. Bazin A. Goaverts). Academic Press Limited, San Diego.
58. Rombout J.W., Blok L.J., Lamers C.H. Egberts E. (1986) Immunization of carp (Cyprinus carpio) with a Vibrio anguillarum bacterin: indications for a common mucosal immune system. Developmental and Comparative Immunology 10, 341 351.
59. Rose A.S., Ellis A.E. Munro A.L.S. (1989) The infectivity by different routes of exposure and shedding rates of Aeromonas salmonicida ssp salmonicida in Atlantic salmon, Salmo salar L., held in sea water. Journal of Fish Diseases 12, 573 578.
60. Samuelsen O.B., Hjeltnes B. Torkildsen L. (1999) Efficacy of orally administered oxolinic acid and Vetoquinol, an oxolinic acid ester, for the treatment of furunculosis in Atlantic salmon Salmo salar held in seawater. Diseases of Aquatic Organisms 37, 53 59.
61. Sansonetti P. (2002) Host-pathogen interactions: the seduction of molecular cross talk. Gut 50 (Suppl. 3 III2 III8.
62. Schep L.J., Tucker I.G., Young G. Butt A.G. (1997) Regional permeability differences between the proximal and distal portions of the isolated salmonid posterior intestine. Journal of Comparative Physiology, B, Biochemical Systemic and Environmental Physiology 167, 370 377.
63. Sjursen H., Bjerknes R., Halstensen A., Naess A., Sornes S. Solberg C.O. (1989) Flow cytometric assay for the measurement of serum opsonins to Neisseria-meningitidis. Journal of Immunological Methods 116, 235 244.
64. Sundell K., Jutfelt F., Agustsson T., Olsen R.-E., Sandblom E., Hansen T. Björnsson B.Th. (2003) Intestinal transport mechanisms and plasma cortisol levels during normal and out-of-season parr-smolt transformation of Atlantic salmon (Salmo salar). Aquaculture 222, 265 285.
65. Svendsen Y.S. Bøgwald J. (1997) Influence of artificial wound and non-intact mucus layer on mortality of Atlantic salmon (Salmo salar L.) following a bath challenge with Vibrio anguillarum and Aeromonas salmonicida. Fish & Shellfish Immunology 7, 317 325.
66. Vandenberg G.W. (2004) Oral vaccines for finfish: academic theory or commercial reality? Animal Health Research Reviews 5, 301 304.