Lipopolysaccharide O-antigen prevents phagocytosis of vibrio anguillarum by rainbow trout (oncorhynchus mykiss) skin epithelial cells

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Lindell, Kristoffer ^a   Fahlgren, Anna ^a   Hjerde, Erik ^c   Willassen, Nils Peder ^c   Fällman, Maria ^a   Milton, Debra L ^a,b  

^a UMEÅ UNIVERSITY   (Sweden)

^b SOUTHERN RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF TROMSØ   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; LIPOPOLYSACCHARIDE O ANTIGEN; LYSOZYME; MANNOSE; METHYLTRANSFERASE; O ANTIGEN; POLYMYXIN B; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL COLONIZATION; CELL COMPOSITION; CELL FUNCTION; CELL PHAGOCYTOSIS; CONTROLLED STUDY; EPIDERMIS; INNATE IMMUNITY; INTESTINE; LISTONELLA ANGUILLARUM; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; PROTEIN TRANSPORT; RAINBOW TROUT; SKIN EPITHELIUM; SKIN STRUCTURE; TISSUE DISTRIBUTION;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; DNA, BACTERIAL; EPITHELIAL CELLS; GENETIC LOCI; MANNOSE; METHYLTRANSFERASES; MURAMIDASE; O ANTIGENS; ONCORHYNCHUS MYKISS; PHAGOCYTOSIS; POLYMYXIN B; SKIN; VIBRIO;

BACTERIA (MICROORGANISMS); LISTONELLA ANGUILLARUM; ONCORHYNCHUS MYKISS;

EID: 84861473544     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037678     Document Type: Article

References (56)

1. Actis LA, Tolmasky ME, Crosa JH, (2011) Vibriosis. In: Woo PTK, Bruno DW, editors. Fish Diseases and Disorders, vol 3 Viral, Bacterial, and Fungal Infections, 2nd edition Oxfordshire, UK CABI International pp. 570-605.
2. Naka H, Crosa JH, (2011) Genetic determinants of virulence in the marine fish pathogen Vibrio anguillarum. Fish Pathol 46: 1-10.
3. Hansen GH, Olafsen JA, (1999) Bacterial interactions in early life stages of marine cold water fish. Microb Ecol 38: 1-26.
4. Irie T, Watarai S, Iwasaki T, Kodama H, (2004) Binding of Vibrio anguillarum to neutral glycosphingolipids from intestinal mucosa of rainbow trout (Oncorhynchus mykiss). J Vet Med Sci 66: 205-208.
5. Muroga K, De La Cruz MC, (1987) Fate and location of Vibrio anguillarum in tissues of artificially infected ayu (Plecoglossus altivelis). Fish Pathol 22: 99-103.
6. Kanno T, Nakai T, Muroga K, (1989) Mode of transmission of vibriosis among Ayu, Plecoglossus altivelis. J Aquat Anim Health 1: 2-6.
7. Spanggaard B, Huber I, Nielsen J, Nielsen T, Gram L, (2000) Proliferation and location of Vibrio anguillarum during infection of rainbow trout, Oncorhynchus mykiss (Walbaum). J Fish Dis 23: 423-427.
8. Croxatto A, Lauritz J, Chen C, Milton DL, (2007) Vibrio anguillarum colonization of rainbow trout integument requires a DNA locus involved in exopolysaccharide transport and biosynthesis. Environ Microbiol 9: 370-382.
9. Weber B, Chen C, Milton DL, (2010) Colonization of fish skin is vital for Vibrio anguillarum to cause disease. Environ Microbiol Rep 2: 133-139.
10. Elliot D, (2000) Integumentary system. In: Ostrander GK, editors. The Laboratory Fish London, UK Academic Press pp. 271-291.
11. Rakers S, Gebert M, Uppalapati S, Meyer W, Maderson P, et al. (2010) "Fish matters": the relevance of fish skin biology to investigative dermatology. Exp Dermatol 19: 313-324.
12. Bullock AM, Marks R, Roberts RJ, (1978) The cell kinetics of teleost fish epidermis: mitotic activity of the normal epidermis at varying temperatures in plaice (Pleuronectes platessa). J Zool 184: 423-428.
13. Bereiter-Hahn J, (1986) Vertebrates. In: Bereiter-Hahn J, Matoltsy AG, Richards KS, editors. Biology of the Integument Berlin Springer-Verlag pp. 443-471.
14. Bullock AM, Marks R, Roberts RJ, (1978) Cell-kinetics of teleost fish epidermis-epidermal mitotic-activity in relation to wound-healing at varying temperatures in plaice (Pleuronectes platessa). J Zool 185: 197-204.
15. Phromsuthirak P, (1977) Electron-microscopy of wound-healing in skin of Gasterosteus aculeatus. J Fish Biol 11: 193-206.
16. Åsbakk K, Dalmo RA, (1998) Atlantic salmon (Salmo salar L.) epidermal Malpighian cells-motile cells clearing away latex beads in vitro. J Mar Biotech 6: 30-34.
17. Åsbakk K, (2001) Elimination of foreign material by epidermal malpighian cells during wound healing in fish skin. J Fish Biol 58: 953-966.
18. Karlsen C, Sørum H, Willassen N-P, Åsbakk K, (2012) Moritella viscosa bypasses Atlantic salmon epidermal keratocyte clearing activity and might use skin surfaces as a port of infection. Vet Microbiol 154: 353-362.
19. Flannagan RS, Jaumouillé V, Grinstein S, (2012) The cell biology of phagocytosis. Annu Rev Pathol Mech Dis 7: 49-86.
20. Lee J, Ishihara A, Theriot JA, Jacobson K, (1993) Principles of locomotion for simple-shaped cells. Nature 362: 167-171.
21. Mogilner A, Keren K, (2009) The shape of motile cells. Curr Biol 19: R762-R771.
22. Naka H, Dias GM, Thompson CC, Dubay C, Thompson FL, et al. (2011) Complete genome sequence of the marine fish pathogen Vibrio anguillarum harboring the pJM1 virulence plasmid and genomic comparison with other virulent strains of V. anguillarum and V. ordalii. Infect Immun 79: 2889-2900.
23. Raetz CR, Whitfield C, (2002) Lipopolysaccharide endotoxins. Annu Rev Biochem 71: 635-700.
24. Cuthbertson L, Kos V, Whitfield C, (2010) ABC transporters involved in export of cell surface glycoconjugates. Microbiol Mol Biol Rev 74: 341-362.
25. Cuthbertson L, Powers J, Whitfield C, (2005) The C-terminal domain of the nucleotide-binding domain protein Wzt determines substrate specificity in the ATP-binding cassette transporter for the lipopolysaccharide O-antigens in Escherichia coli serotypes O8 and O9a. J Biol Chem 280: 30310-30319.
26. Stroeher UH, Jedani KE, Manning PA, (1998) Genetic organization of the regions associated with surface polysaccharide synthesis in Vibrio cholerae O1, O139 and Vibrio anguillarum O1 and O2: a review. Gene 26: 269-282.
27. Clarke BR, Cuthbertson L, Whitfield C, (2004) Nonreducing terminal modifications determine the chain length of polymannose O antigens of Escherichia coli and couple chain termination to polymer export via an ATP-binding cassette transporter. J Biol Chem 279: 35709-35718.
28. Kerrigan AM, Brown GD, (2009) C-type lectins and phagocytosis. Immunobiol 214: 562-575.
29. Kania PW, Sorensen RR, Koch C, Brandt J, Kliem A, et al. (2010) Evolutionary conservation of mannan-binding lectin (MBL) in bony fish: Identification, characterization and expression analysis of three bona fide collectin homologues of MBL in the rainbow trout (Onchorhynchus mykiss). Fish Shellfish Immunol 29: 910-920.
30. Russell S, Young KM, Smith M, Hayes MA, Lumsden JS, (2008) Identification, cloning and tissue localization of a rainbow trout (Oncorhynchus mykiss) intelectin-like protein that binds bacteria and chitin. Fish Shellfish Immunol 25: 91-105.
31. Russell S, Young KM, Smith M, Hayes MA, Lumsden JS, (2008) Cloning, binding properties, and tissue localization of rainbow trout (Oncorhynchus mykiss) ladderlectin. Fish Shellfish Immunol 24: 669-683.
32. Tsutsui S, Tasumi S, Suetake H, Kikuchi K, Suzuki Y, (2005) Demonstration of the mucosal lectins in the epithelial cells of internal and external body surface tissues in pufferfish (Fugu rubripes). Dev Comp Immunol 29: 243-253.
33. Trust TJ, Courtice ID, Khouri AG, Crosa JH, Schiewe MH, (1981) Serum resistance and hemagglutination ability of marine vibrios pathogenic for fish. Infect Immun 34: 702-707.
34. Hutchens M, Luker GD, (2007) Applications of bioluminescence imaging to the study of infectious disease. Cell Microbiol 9: 2315-2322.
35. Meighen EA, Dunlap PV, (1993) Physiological, biochemical, and genetic control of bacterial bioluminescence. Adv Microb Physiol 34: 1-67.
36. Rosenfeld Y, Shai Y, (2006) Lipopolysaccharide (Endotoxin)-host defense antibacterial peptides interactions: Role in bacterial resistance and prevention of sepsis. Biochim Biophys Acta 1758: 1513-1522.
37. Ellis AE, (2001) Innate host defense mechanisms of fish against viruses and bacteria. Dev Comp Immunol 25: 827-839.
38. Austin B, Austin DA, (1999) Pathogenicity. In: Austin B, Austin DA, editors. Bacterial Fish Pathogens: Disease of Farmed and Wild Fish, 3rd edition Chichester, UK Praxis Publishing Ltd pp. 272-275.
39. Flannagan RS, Cosío G, Grinstein S, (2009) Antimicrobial mechanisms of phagocytes and bacterial evasion strategies. Nature Rev Microbiol 7: 355-366.
40. Norqvist A, Wolf-Watz H, (1993) Characterization of a novel chromosomal virulence locus involved in expression of a major surface flagellar sheath antigen of the fish pathogen Vibrio anguillarum. Infect Immun 61: 2434-2444.
41. Boesen HT, Pedersen K, Larsen JL, Koch C, Ellis AE, (1999) Vibrio anguillarum resistance to rainbow trout (Onchorynchus mykiss) serum: role of O-antigen structure of lipopolysaccharide. Infect Immun 67: 294-301.
42. Welch TJ, Crosa JH, (2005) Novel role of the lipopolysaccharide O1 side chain in ferric siderophore transport and virulence of Vibrio anguillarum. Infect Immun 73: 5864-5872.
43. Aoki T, Nomura J, Crosa JH, (1985) Virulence of Vibrio anguillarum with particular emphasis on the outer membrane components. Bull Jap Soc Sci Fish 51: 1249-1254.
44. Suzuki Y, Tasumi S, Tsutsui S, Okamoto M, Suetake H, (2003) Molecular diversity of skin mucus lectins in fish. Comp Biochem Physiol 136: 723-730.
45. Klena J, Zhang P, Schwartz O, Hull S, Chen T, (2005) The core lipopolysaccharide of Escherichia coli is a ligand for the dendritic-cell-specific intercellular adhesion molecule nonintegrin CD209 receptor. J Bacteriol 187: 1710-1715.
46. Elder K, Vizler C, Kusz E, Karcagi I, Glavinas H, et al. (2009) The role of lipopolysaccharide moieties in macrophage response to Escherichia coli. Biochem Biophys Res Commun 389: 46-51.
47. Murray GL, Attridge SR, Morona R, (2006) Altering the length of the lipopolysaccharide O antigen has an impact on the interaction of Salmonella enterica serovar Typhimurium with macrophages and complement. J Bacteriol 188: 2735-2739.
48. Saldías MS, Ortega X, Valvano MA, (2009) Burkholderia cenocepacia O antigen lipopolysaccharide prevents phagocytosis by macrophages and adhesion to epithelial cells. J Med Microbiol 58: 1542-1548.
49. Zhang P, Snyder S, Feng P, Azadi P, Zhang S, et al. (2006) Role of N-acetylglucosamine within core lipopolysaccharide of several species of gram-negative bacteria in targeting the DC-SIGN (CD209). J Immunol 177: 4002-4011.
50. Zelensky AN, Gready JE, (2004) C-type lectin-like domains in Fugu rubripes. BMC Genomics 5: 51.
51. Milton DL, O'Toole R, Hörstedt P, Wolf-Watz H, (1996) Flagellin A is essential for the virulence of Vibrio anguillarum. J Bacteriol 178: 1310-1319.
52. McGee K, Hörstedt P, Milton DL, (1996) Identification and characterization of additional flagellin genes from Vibrio anguillarum. J Bacteriol 178: 5188-5198.
53. Sambrook J, Fritsch EF, Maniatis T, (1989) Molecular Cloning: a Laboratory Manual, 2nd edn Cold Spring Harbor, NY, USA Cold Spring Harbor Laboratory.
54. Preston MA, Penner JL, (1987) Structural and antigenic properties of lipopolysaccharides from serotype reference strains of Campylobacter jejuni. Infect Immun 55: 1806-1812.
55. Laemmli UK, (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
56. Plante CJ, (2000) Role of bacterial exopolymeric capsules in protection from deposit-feeder digestion. Aquat Microb Ecol 21: 211-219.