Antimicrobial responses of teleost phagocytes and innate immune evasion strategies of intracellular bacteria

Developmental and Comparative Immunology

Volumn 43, Issue 2, 2014, Pages 223-242

  Grayfer, Leon ^a   Hodgkinson, Jordan W ^b   Belosevic, Miodrag ^b  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Antimicrobial response; Cytokines; Fish; Immune evasion; Macrophages; Mycobacterium marinum

Indexed keywords

BACTERIAL VACCINE; HEPCIDIN; HYDROGEN PEROXIDE; INDOLEAMINE 2,3 DIOXYGENASE; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 1; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 2; NITRIC OXIDE; PROBIOTIC AGENT; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR ALPHA; CATION TRANSPORT PROTEIN; NATURAL RESISTANCE-ASSOCIATED MACROPHAGE PROTEIN 1;

APOPTOSIS; BACTERIAL DETOXIFICATION; BACTERIAL METABOLISM; BACTERIAL SECRETION SYSTEM; BACTERIAL VIRULENCE; CYTOKINE PRODUCTION; DETOXIFICATION; DISEASE ASSOCIATION; DRUG RESISTANCE; ENTERIC SEPTICEMIA OF CATFISH; GRANULOMA; IMMUNE EVASION; IMMUNOPROPHYLAXIS; IMMUNOREGULATION; INFECTION RESISTANCE; INNATE IMMUNITY; INTRACELLULAR BACTERIUM; IRON DEPLETION; IRON DEPRIVATION; IRON METABOLISM; MACROPHAGE; MOLECULAR DYNAMICS; MORBIDITY; MORTALITY; MYCOBACTERIUM MARINUM; NEUTROPHIL; NONHUMAN; PHAGOCYTOSIS; PHAGOSOME; PRIORITY JOURNAL; RESPIRATORY BURST; REVIEW; TELEOST; VACCINATION; ANIMAL; BACTERIAL INFECTION; FISH; IMMUNOLOGY; INTRACELLULAR SPACE; METABOLISM; PHAGOCYTE;

MYCOBACTERIUM MARINUM; OSTEICHTHYES; TELEOSTEI;

ANIMALS; BACTERIAL INFECTIONS; CATION TRANSPORT PROTEINS; FISHES; IMMUNE EVASION; IMMUNITY, INNATE; INTRACELLULAR SPACE; NITRIC OXIDE; PHAGOCYTES;

EID: 84891827926     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2013.08.003     Document Type: Review

References (273)

1. Abdallah A.M., Bestebroer J., Savage N.D., de Punder K., van Zon M., Wilson L., Korbee C.J., van der Sar A.M., Ottenhoff T.H., van der Wel N.N., Bitter W., Peters P.J. Mycobacterial secretion systems ESX-1 and ESX-5 play distinct roles in host cell death and inflammasome activation. J. Immunol. 2011, 187:4744-4753.
2. Abdallah A.M., Gey van Pittius N.C., Champion P.A., Cox J., Luirink J., Vandenbroucke-Grauls C.M., Appelmelk B.J., Bitter W. Type VII secretion - mycobacteria show the way. Nat. Rev. Microbiol. 2007, 5:883-891.
3. Abdallah A.M., Savage N.D., van Zon M., Wilson L., Vandenbroucke-Grauls C.M., van der Wel N.N., Ottenhoff T.H., Bitter W. The ESX-5 secretion system of Mycobacterium marinum modulates the macrophage response. J. Immunol. 2008, 181:7166-7175.
4. Abdallah A.M., Verboom T., Weerdenburg E.M., Gey van Pittius N.C., Mahasha P.W., Jimenez C., Parra M., Cadieux N., Brennan M.J., Appelmelk B.J., Bitter W. PPE and PE_PGRS proteins of Mycobacterium marinum are transported via the type VII secretion system ESX-5. Mol. Microbiol. 2009, 73:329-340.
5. Abergel R.J., Clifton M.C., Pizarro J.C., Warner J.A., Shuh D.K., Strong R.K., Raymond K.N. The siderocalin/enterobactin interaction: a link between mammalian immunity and bacterial iron transport. J. Am. Chem. Soc. 2008, 130:11524-11534.
6. Acosta F., Real F., Ellis A.E., Tabraue C., Padilla D., Ruiz de Galarreta C.M. Influence of vaccination on the nitric oxide response of gilthead seabream following infection with Photobacterium damselae subsp. piscicida. Fish Shellfish Immunol. 2005, 18:31-38.
7. Acosta F., Real F., Ruiz de Galarreta C.M., Diaz R., Padilla D., Ellis A.E. Toxicity of nitric oxide and peroxynitrite to Photobacterium damselae subsp. piscicida. Fish Shellfish Immunol. 2003, 15:241-248.
8. Acosta F., Ruiz de Galarreta C.M., Ellis A.E., Diaz R., Gomez V., Padilla D., Real F. Activation of the nitric oxide response in gilthead seabream after experimental infection with Photobacterium damselae subsp. piscicida. Fish Shellfish Immunol. 2004, 16:581-588.
9. Aggad D., Stein C., Sieger D., Mazel M., Boudinot P., Herbomel P., Levraud J.P., Lutfalla G., Leptin M. In vivo analysis of Ifn-gamma1 and Ifn-gamma2 signaling in zebrafish. J. Immunol. 2010, 185:6774-6782.
10. Alberdi F., Alderton M.R., Coloe P.J., Smith S.C. Characterization of immunorelated peptides to porcidin P1. Immunol. Cell Biol. 1995, 73:505-510.
11. Alberdi F., Alderton M.R., Korolik V., Coloe P.J., Smith S.C. Antibacterial proteins from porcine polymorphonuclear neutrophils. Immunol. Cell Biol. 1995, 73:38-43.
12. Alejo A., Tafalla C. Chemokines in teleost fish species. Dev. Comp. Immunol. 2011, 35:1215-1222.
13. Alter-Koltunoff M., Goren S., Nousbeck J., Feng C.G., Sher A., Ozato K., Azriel A., Levi B.Z. Innate immunity to intraphagosomal pathogens is mediated by interferon regulatory factor 8 (IRF-8) that stimulates the expression of macrophage-specific Nramp1 through antagonizing repression by c-Myc. J. Biol. Chem. 2008, 283:2724-2733.
14. Andrew P.J., Mayer B. Enzymatic function of nitric oxide synthases. Cardiovasc. Res. 1999, 43:521-531.
15. Andrews S.R., Sahu N.P., Pal A.K., Mukherjee S.C., Kumar S. Yeast extract, brewer's yeast and spirulina in diets for Labeo rohita fingerlings affect haemato-immunological responses and survival following Aeromonas hydrophila challenge. Res. Vet. Sci. 2011, 91:103-109.
16. Ardo L., Jeney Z., Adams A., Jeney G. Immune responses of resistant and sensitive common carp families following experimental challenge with Aeromonas hydrophila. Fish Shellfish Immunol. 2010, 29:111-116.
17. Arias M., Rojas M., Zabaleta J., Rodriguez J.I., Paris S.C., Barrera L.F., Garcia L.F. Inhibition of virulent Mycobacterium tuberculosis by Bcg(r) and Bcg(s) macrophages correlates with nitric oxide production. J. Infect. Dis. 1997, 176:1552-1558.
18. Atkinson P.G., Barton C.H. Ectopic expression of Nramp1 in COS-1 cells modulates iron accumulation. FEBS Lett. 1998, 425:239-242.
19. Atkinson P.G., Blackwell J.M., Barton C.H. Nramp1 locus encodes a 65kDa interferon-gamma-inducible protein in murine macrophages. Biochem. J. 1997, 325(Pt 3):779-786.
20. Barker L.P., George K.M., Falkow S., Small P.L. Differential trafficking of live and dead Mycobacterium marinum organisms in macrophages. Infect. Immun. 1997, 65:1497-1504.
21. Barksdale A.R., Bernard A.C., Maley M.E., Gellin G.L., Kearney P.A., Boulanger B.R., Tsuei B.J., Ochoa J.B. Regulation of arginase expression by T-helper II cytokines and isoproterenol. Surgery 2004, 135:527-535.
22. Barnes A.C., Balebona M.C., Horne M.T., Ellis A.E. Superoxide dismutase and catalase in Photobacterium damselae subsp. piscicida and their roles in resistance to reactive oxygen species. Microbiology 1999, 145(Pt 2):483-494.
23. Barreda D.R., Hanington P.C., Stafford J.L., Belosevic M. A novel soluble form of the CSF-1 receptor inhibits proliferation of self-renewing macrophages of goldfish (Carassius auratus L.). Dev. Comp. Immunol. 2005, 29:879-894.
24. Beauregard K.E., Lee K.D., Collier R.J., Swanson J.A. PH-dependent perforation of macrophage phagosomes by listeriolysin O from Listeria monocytogenes. J. Exp. Med. 1997, 186:1159-1163.
25. Blackwell J.M., Goswami T., Evans C.A., Sibthorpe D., Papo N., White J.K., Searle S., Miller E.N., Peacock C.S., Mohammed H., Ibrahim M. SLC11A1 (formerly NRAMP1) and disease resistance. Cell. Microbiol. 2001, 3:773-784.
26. Blackwell J.M., Roberts C.W., Roach T.I., Alexander J. Influence of macrophage resistance gene Lsh/Ity/Bcg (candidate Nramp) on Toxoplasma gondii infection in mice. Clin. Exp. Immunol. 1994, 97:107-112.
27. Blackwell J.M., Searle S., Goswami T., Miller E.N. Understanding the multiple functions of Nramp1. Microbes Infect. 2000, 2:317-321.
28. Boltana S., Donate C., Goetz F.W., MacKenzie S., Balasch J.C. Characterization and expression of NADPH oxidase in LPS-, poly(I:C)- and zymosan-stimulated trout (Oncorhynchus mykiss W.) macrophages. Fish Shellfish Immunol. 2009, 26:651-661.
29. Borelli V., Banfi E., Perrotta M.G., Zabucchi G. Myeloperoxidase exerts microbicidal activity against Mycobacterium tuberculosis. Infect. Immun. 1999, 67:4149-4152.
30. Borregaard N., Cowland J.B. Granules of the human neutrophilic polymorphonuclear leukocyte. Blood 1997, 89:3503-3521.
31. Briggs R.T., Drath D.B., Karnovsky M.L., Karnovsky M.J. Localization of NADH oxidase on the surface of human polymorphonuclear leukocytes by a new cytochemical method. J. Cell. Biol. 1975, 67:566-586.
32. Brown J.S., Holden D.W. Iron acquisition by Gram-positive bacterial pathogens. Microbes Infect. 2002, 4:1149-1156.
33. Burge E.J., Gauthier D.T., Ottinger C.A., Van Veld P.A. Mycobacterium-inducible Nramp in striped bass (Morone saxatilis). Infect. Immun. 2004, 72:1626-1636.
34. Burge E.J., Gauthier D.T., Van Veld P.A. In vitro response of the striped bass natural resistance-associated macrophage protein, Nramp, to LPS and Mycobacterium marinum exposure. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2004, 138:391-400.
35. Butler A. Marine siderophores and microbial iron mobilization. Biometals 2005, 18:369-374.
36. Byrd T.F., Horwitz M.A. Interferon gamma-activated human monocytes downregulate transferrin receptors and inhibit the intracellular multiplication of Legionella pneumophila by limiting the availability of iron. J. Clin. Invest. 1989, 83:1457-1465.
37. Carlsson F., Kim J., Dumitru C., Barck K.H., Carano R.A., Sun M., Diehl L., Brown E.J. Host-detrimental role of Esx-1-mediated inflammasome activation in mycobacterial infection. PLoS Pathog. 2010, 6:e1000895.
38. Cassatella M.A., Della Bianca V., Berton G., Rossi F. Activation by gamma interferon of human macrophage capability to produce toxic oxygen molecules is accompanied by decreased Km of the superoxide-generating NADPH oxidase. Biochem. Biophys. Res. Commun. 1985, 132:908-914.
39. Chan K., Knaak T., Satkamp L., Humbert O., Falkow S., Ramakrishnan L. Complex pattern of Mycobacterium marinum gene expression during long-term granulomatous infection. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:3920-3925.
40. Chen H., Waldbieser G.C., Rice C.D., Elibol B., Wolters W.R., Hanson L.A. Isolation and characterization of channel catfish natural resistance associated macrophage protein gene. Dev. Comp. Immunol. 2002, 26:517-531.
41. Chen S.L., Xu M.Y., Ji X.S., Yu G.C. Cloning and characterisation of natural resistance associated macrophage protein (Nramp) cDNA from red sea bream (Pagrus major). Fish Shellfish Immunol. 2004, 17:305-313.
42. Chen S.L., Zhang Y.X., Xu J.Y., Meng L., Sha Z.X., Ren G.C. Molecular cloning, characterization and expression analysis of natural resistance associated macrophage protein (Nramp) cDNA from turbot (Scophthalmus maximus). Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2007, 147:29-37.
43. Cheng S., Zhang M., Sun L. The iron-cofactored superoxide dismutase of Edwardsiella tarda inhibits macrophage-mediated innate immune response. Fish Shellfish Immunol. 2010, 29:972-978.
44. Chettri J.K., Raida M.K., Kania P.W., Buchmann K. Differential immune response of rainbow trout (Oncorhynchus mykiss) at early developmental stages (larvae and fry) against the bacterial pathogen Yersinia ruckeri. Dev. Comp. Immunol. 2012, 36:463-474.
45. Clay H., Davis J.M., Beery D., Huttenlocher A., Lyons S.E., Ramakrishnan L. Dichotomous role of the macrophage in early Mycobacterium marinum infection of the zebrafish. Cell Host Microbe. 2007, 2:29-39.
46. Clay H., Volkman H.E., Ramakrishnan L. Tumor necrosis factor signaling mediates resistance to mycobacteria by inhibiting bacterial growth and macrophage death. Immunity 2008, 29:283-294.
47. Cosma C.L., Klein K., Kim R., Beery D., Ramakrishnan L. Mycobacterium marinum Erp is a virulence determinant required for cell wall integrity and intracellular survival. Infect. Immun. 2006, 74:3125-3133.
48. Costa M.M., Maehr T., Diaz-Rosales P., Secombes C.J., Wang T. Bioactivity studies of rainbow trout (Oncorhynchus mykiss) interleukin-6: effects on macrophage growth and antimicrobial peptide gene expression. Mol. Immunol. 2011, 48:1903-1916.
49. Cuesta A., Meseguer J., Esteban M.A. The antimicrobial peptide hepcidin exerts an important role in the innate immunity against bacteria in the bony fish gilthead seabream. Mol. Immunol. 2008, 45:2333-2342.
50. Davis A.S., Vergne I., Master S.S., Kyei G.B., Chua J., Deretic V. Mechanism of inducible nitric oxide synthase exclusion from mycobacterial phagosomes. PLoS Pathog. 2007, 3:e186.
51. Davis J.M., Clay H., Lewis J.L., Ghori N., Herbomel P., Ramakrishnan L. Real-time visualization of mycobacterium-macrophage interactions leading to initiation of granuloma formation in zebrafish embryos. Immunity 2002, 17:693-702.
52. Davis J.M., Ramakrishnan L. The role of the granuloma in expansion and dissemination of early tuberculous infection. Cell 2009, 136:37-49.
53. Delgado M.A., Deretic V. Toll-like receptors in control of immunological autophagy. Cell Death Differ. 2009, 16:976-983.
54. Delgado M.A., Elmaoued R.A., Davis A.S., Kyei G., Deretic V. Toll-like receptors control autophagy. Embo J. 2008, 27:1110-1121.
55. Denicola A., Rubbo H., Rodriguez D., Radi R. Peroxynitrite-mediated cytotoxicity to Trypanosoma cruzi. Arch. Biochem. Biophys. 1993, 304:279-286.
56. Densmore C.L., Smith S.A., Holladay S.D. In vitro effects of the extracellular protein of Renibacterium salmoninarum on phagocyte function in brook trout (Salvelinus fontinalis). Vet. Immunol. Immunopathol. 1998, 62:349-357.
57. Diaz-Rosales P., Chabrillon M., Arijo S., Martinez-Manzanares E., Morinigo M.A., Balebona M.C. Superoxide dismutase and catalase activities in Photobacterium damselae ssp. piscicida. J. Fish Dis. 2006, 29:355-364.
58. Douglas S.E., Gallant J.W., Liebscher R.S., Dacanay A., Tsoi S.C. Identification and expression analysis of hepcidin-like antimicrobial peptides in bony fish. Dev. Comp. Immunol. 2003, 27:589-601.
59. Durborow R.M. Health and safety concerns in fisheries and aquaculture. Occup. Med. 1999, 14:373-406.
60. El-Etr S.H., Subbian S., Cirillo S.L., Cirillo J.D. Identification of two Mycobacterium marinum loci that affect interactions with macrophages. Infect. Immun. 2004, 72:6902-6913.
61. El-Etr S.H., Yan L., Cirillo J.D. Fish monocytes as a model for mycobacterial host-pathogen interactions. Infect. Immun. 2001, 69:7310-7317.
62. Elibol-Flemming B., Waldbieser G.C., Wolters W.R., Boyle C.R., Hanson L.A. Expression analysis of selected immune-relevant genes in channel catfish during Edwardsiella ictaluri infection. J. Aquat. Anim. Health 2009, 21:23-35.
63. Fast M.D., Tse B., Boyd J.M., Johnson S.C. Mutations in the Aeromonas salmonicida subsp. salmonicida type III secretion system affect Atlantic salmon leucocyte activation and downstream immune responses. Fish Shellfish Immunol. 2009, 27:721-728.
64. Fischbach M.A., Lin H., Zhou L., Yu Y., Abergel R.J., Liu D.R., Raymond K.N., Wanner B.L., Strong R.K., Walsh C.T., Aderem A., Smith K.D. The pathogen-associated iroA gene cluster mediates bacterial evasion of lipocalin 2. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:16502-16507.
65. Flynn J.L., Chan J. Immune evasion by Mycobacterium tuberculosis: living with the enemy. Curr. Opin. Immunol. 2003, 15:450-455.
66. Forlenza M., Fink I.R., Raes G., Wiegertjes G.F. Heterogeneity of macrophage activation in fish. Dev. Comp. Immunol. 2011, 35:1246-1255.
67. Frey C. Marine injuries. Prevention and treatment. Orthop. Rev. 1994, 23:645-649.
68. Gabbiani G. The role of contractile proteins in wound healing and fibrocontractive diseases. Methods Achiev. Exp. Pathol. 1979, 9:187-206.
69. Gan H., Lee J., Ren F., Chen M., Kornfeld H., Remold H.G. Mycobacterium tuberculosis blocks crosslinking of annexin-1 and apoptotic envelope formation on infected macrophages to maintain virulence. Nat. Immunol. 2008, 9:1189-1197.
70. Ganz T. Molecular control of iron transport. J. Am. Soc. Nephrol. 2007, 18:394-400.
71. Ganz T. Iron in innate immunity: starve the invaders. Curr. Opin. Immunol. 2009, 21:63-67.
72. Ganz T., Lehrer R.I. Antimicrobial peptides of leukocytes. Curr. Opin. Hematol. 1997, 4:53-58.
73. Ganz T., Nemeth E. Regulation of iron acquisition and iron distribution in mammals. Biochim. Biophys. Acta. 2006, 1763:690-699.
74. Ganz T., Nemeth E. Iron sequestration and anemia of inflammation. Semin. Hematol. 2009, 46:387-393.
75. Gao L.Y., Laval F., Lawson E.H., Groger R.K., Woodruff A., Morisaki J.H., Cox J.S., Daffe M., Brown E.J. Requirement for kasB in Mycobacterium mycolic acid biosynthesis, cell wall impermeability and intracellular survival: implications for therapy. Mol. Microbiol. 2003, 49:1547-1563.
76. Gao L.Y., Pak M., Kish R., Kajihara K., Brown E.J. A mycobacterial operon essential for virulence in vivo and invasion and intracellular persistence in macrophages. Infect. Immun. 2006, 74:1757-1767.
77. Gey Van Pittius N.C., Gamieldien J., Hide W., Brown G.D., Siezen R.J., Beyers A.D. The ESAT-6 gene cluster of Mycobacterium tuberculosis and other high G+C Gram-positive bacteria. Genome Biol. 2001, 2. 0044.1-0044.18.
78. Goswami T., Bhattacharjee A., Babal P., Searle S., Moore E., Li M., Blackwell J.M. Natural-resistance-associated macrophage protein 1 is an H+/bivalent cation antiporter. Biochem. J. 2001, 354:511-519.
79. Goto Y., Buschman E., Skamene E. Regulation of host resistance to Mycobacterium intracellulare in vivo and in vitro by the Bcg gene. Immunogenetics 1989, 30:218-221.
80. Graham S., Secombes C.J. The production of a macrophage-activating factor from rainbow trout Salmo gairdneri leucocytes. Immunology 1988, 65:293-297.
81. Graham S., Secombes C.J. Do fish lymphocytes secrete interferon-y?. J. Fish Biol. 1990, 36:563-573.
82. Grau G.E., Fajardo L.F., Piguet P.F., Allet B., Lambert P.H., Vassalli P. Tumor necrosis factor (cachectin) as an essential mediator in murine cerebral malaria. Science 1987, 237:1210-1212.
83. Grayfer L., Belosevic M. Molecular characterization of novel interferon gamma receptor 1 isoforms in zebrafish (Danio rerio) and goldfish (Carassius auratus L.). Mol. Immunol. 2009, 46:3050-3059.
84. Grayfer L., Belosevic M. Molecular characterization, expression and functional analysis of goldfish (Carassius auratus L.) interferon gamma. Dev. Comp. Immunol. 2009, 33:235-246.
85. Grayfer L., Garcia E.G., Belosevic M. Comparison of macrophage antimicrobial responses induced by type II interferons of the goldfish (Carassius auratus L.). J. Biol. Chem. 2010, 285:23537-23547.
86. Grayfer L., Hanington P.C., Belosevic M. Macrophage colony-stimulating factor (CSF-1) induces pro-inflammatory gene expression and enhances antimicrobial responses of goldfish (Carassius auratus L.) macrophages. Fish Shellfish Immunol. 2009, 26:406-413.
87. Grayfer L., Hodgkinson J.W., Belosevic M. Analysis of the antimicrobial responses of primary phagocytes of the goldfish (Carassius auratus L.) against Mycobacterium marinum. Dev. Comp. Immunol. 2011, 35:1146-1158.
88. Grayfer L., Hodgkinson J.W., Hitchen S.J., Belosevic M. Characterization and functional analysis of goldfish (Carassius auratus L.) interleukin-10. Mol. Immunol. 2010, 10.1016/j.molimm.2010.10.013.
89. Grayfer L., Walsh J.G., Belosevic M. Characterization and functional analysis of goldfish (Carassius auratus L.) tumor necrosis factor-alpha. Dev. Comp. Immunol. 2008, 32:532-543.
90. Grayson T.H., Cooper L.F., Wrathmell A.B., Roper J., Evenden A.J., Gilpin M.L. Host responses to Renibacterium salmoninarum and specific components of the pathogen reveal the mechanisms of immune suppression and activation. Immunology 2002, 106:273-283.
91. Green S.J., Crawford R.M., Hockmeyer J.T., Meltzer M.S., Nacy C.A. Leishmania major amastigotes initiate the l-arginine-dependent killing mechanism in IFN-gamma-stimulated macrophages by induction of tumor necrosis factor-alpha. J. Immunol. 1990, 145:4290-4297.
92. Grohmann U., Bronte V. Control of immune response by amino acid metabolism. Immunol Rev. 2010, 236:243-264.
93. Gruenheid S., Canonne-Hergaux F., Gauthier S., Hackam D.J., Grinstein S., Gros P. The iron transport protein NRAMP2 is an integral membrane glycoprotein that colocalizes with transferrin in recycling endosomes. J. Exp. Med. 1999, 189:831-841.
94. Gruenheid S., Pinner E., Desjardins M., Gros P. Natural resistance to infection with intracellular pathogens: the Nramp1 protein is recruited to the membrane of the phagosome. J. Exp. Med. 1997, 185:717-730.
95. Gunshin H., Mackenzie B., Berger U.V., Gunshin Y., Romero M.F., Boron W.F., Nussberger S., Gollan J.L., Hediger M.A. Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature 1997, 388:482-488.
96. Hackam D.J., Rotstein O.D., Zhang W., Gruenheid S., Gros P., Grinstein S. Host resistance to intracellular infection: mutation of natural resistance-associated macrophage protein 1 (Nramp1) impairs phagosomal acidification. J. Exp. Med. 1998, 188:351-364.
97. Haddad G., Hanington P.C., Wilson E.C., Grayfer L., Belosevic M. Molecular and functional characterization of goldfish (Carassius auratus L.) transforming growth factor beta. Dev. Comp. Immunol. 2008, 32:654-663.
98. Hall C.J., Flores M.V., Oehlers S.H., Sanderson L.E., Lam E.Y., Crosier K.E., Crosier P.S. Infection-responsive expansion of the hematopoietic stem and progenitor cell compartment in zebrafish is dependent upon inducible nitric oxide. Cell Stem Cell. 2012, 10:198-209.
99. Harikrishnan R., Balasundaram C., Heo M.S. Potential use of probiotic- and triherbal extract-enriched diets to control Aeromonas hydrophila infection in carp. Dis. Aquat. Organ. 2010, 92:41-49.
100. Harikrishnan R., Kim M.C., Kim J.S., Han Y.J., Jang I.S., Balasundaram C., Heo M.S. Immunomodulatory effect of sodium alginate enriched diet in kelp grouper Epinephelus brneus against Streptococcus iniae. Fish Shellfish Immunol. 2011, 30:543-549.
101. Hayaishi O. Utilization of superoxide anion by indoleamine oxygenase-catalyzed tryptophan and indoleamine oxidation. Adv. Exp. Med. Biol. 1996, 398:285-289.
102. Hodgkinson J.W., Ge J.Q., Grayfer L., Stafford J., Belosevic M. Analysis of the immune response in infections of the goldfish (Carassius auratus L.) with Mycobacterium marinum. Dev. Comp. Immunol. 2012, 38:456-465.
103. Igawa D., Sakai M., Savan R. An unexpected discovery of two interferon gamma-like genes along with interleukin (IL)-22 and -26 from teleost: IL-22 and -26 genes have been described for the first time outside mammals. Mol. Immunol. 2006, 43:999-1009.
104. Iglesias E., Brandariz I., Jimenez C., Soengas R.G. Iron(III) complexation by Vanchrobactin, a siderophore of the bacterial fish pathogen Vibrio anguillarum. Metallomics 2011, 3:521-528.
105. Iniesta V., Gomez-Nieto L.C., Molano I., Mohedano A., Carcelen J., Miron C., Alonso C., Corraliza I. Arginase I induction in macrophages, triggered by Th2-type cytokines, supports the growth of intracellular Leishmania parasites. Parasite Immunol. 2002, 24:113-118.
106. Inoue Y., Kamota S., Ito K., Yoshiura Y., Ototake M., Moritomo T., Nakanishi T. Molecular cloning and expression analysis of rainbow trout (Oncorhynchus mykiss) interleukin-10 cDNAs. Fish Shellfish Immunol. 2005, 18:335-344.
107. Ischiropoulos H., Zhu L., Chen J., Tsai M., Martin J.C., Smith C.D., Beckman J.S. Peroxynitrite-mediated tyrosine nitration catalyzed by superoxide dismutase. Arch. Biochem. Biophys. 1992, 298:431-437.
108. Ishibe K., Osatomi K., Hara K., Kanai K., Yamaguchi K., Oda T. Comparison of the responses of peritoneal macrophages from Japanese flounder (Paralichthys olivaceus) against high virulent and low virulent strains of Edwardsiella tarda. Fish Shellfish Immunol. 2008, 24:243-251.
109. Ishibe K., Yamanishi T., Wang Y., Osatomi K., Hara K., Kanai K., Yamaguchi K., Oda T. Comparative analysis of the production of nitric oxide (NO) and tumor necrosis factor-alpha (TNF-alpha) from macrophages exposed to high virulent and low virulent strains of Edwardsiella tarda. Fish Shellfish Immunol. 2009, 27:386-389.
110. Iyengar R., Stuehr D.J., Marletta M.A. Macrophage synthesis of nitrite, nitrate, and N-nitrosamines: precursors and role of the respiratory burst. Proc. Natl. Acad. Sci. U.S.A. 1987, 84:6369-6373.
111. Jacobs J.M., Stine C.B., Baya A.M., Kent M.L. A review of mycobacteriosis in marine fish. J. Fish Dis. 2009, 32:119-130.
112. Joerink M., Forlenza M., Ribeiro C.M., de Vries B.J., Savelkoul H.F., Wiegertjes G.F. Differential macrophage polarisation during parasitic infections in common carp (Cyprinus carpio L.). Fish Shellfish Immunol. 2006, 21:561-571.
113. Joerink M., Ribeiro C.M., Stet R.J., Hermsen T., Savelkoul H.F., Wiegertjes G.F. Head kidney-derived macrophages of common carp (Cyprinus carpio L.) show plasticity and functional polarization upon differential stimulation. J. Immunol. 2006, 177:61-69.
114. Joerink M., Savelkoul H.F., Wiegertjes G.F. Evolutionary conservation of alternative activation of macrophages: structural and functional characterization of arginase 1 and 2 in carp (Cyprinus carpio L.). Mol. Immunol. 2006, 43:1116-1128.
115. Johnson E.E., Wessling-Resnick M. Iron metabolism and the innate immune response to infection. Microbes Infect. 2012, 14:207-216.
116. Jurecka P., Irnazarow I., Stafford J.L., Ruszczyk A., Taverne N., Belosevic M., Savelkoul H.F., Wiegertjes G.F. The induction of nitric oxide response of carp macrophages by transferrin is influenced by the allelic diversity of the molecule. Fish Shellfish Immunol. 2009, 26:632-638.
117. Kaplan D.H., Greenlund A.C., Tanner J.W., Shaw A.S., Schreiber R.D. Identification of an interferon-gamma receptor alpha chain sequence required for JAK-1 binding. J. Biol. Chem. 1996, 271:9-12.
118. Kim S., Ponka P. Effects of interferon-gamma and lipopolysaccharide on macrophage iron metabolism are mediated by nitric oxide-induced degradation of iron regulatory protein 2. J. Biol. Chem. 2000, 275:6220-6226.
119. Kindler V., Sappino A.P., Grau G.E., Piguet P.F., Vassalli P. The inducing role of tumor necrosis factor in the development of bactericidal granulomas during BCG infection. Cell 1989, 56:731-740.
120. Klionsky D.J. Autophagy: from phenomenology to molecular understanding in less than a decade. Nat. Rev. Mol. Cell. Biol. 2007, 8:931-937.
121. Kono T., Fujiki K., Nakao M., Yano T., Endo M., Sakai M. The immune responses of common carp, Cyprinus carpio L., injected with carp interleukin-1beta gene. J. Interferon Cytokine Res. 2002, 22:413-419.
122. Koo I.C., Wang C., Raghavan S., Morisaki J.H., Cox J.S., Brown E.J. ESX-1-dependent cytolysis in lysosome secretion and inflammasome activation during mycobacterial infection. Cell. Microbiol. 2008, 10:1866-1878.
123. Koul A., Herget T., Klebl B., Ullrich A. Interplay between mycobacteria and host signalling pathways. Nat. Rev. Microbiol. 2004, 2:189-202.
124. Kurenuma T., Kawamura I., Hara H., Uchiyama R., Daim S., Dewamitta S.R., Sakai S., Tsuchiya K., Nomura T., Mitsuyama M. The RD1 locus in the Mycobacterium tuberculosis genome contributes to activation of caspase-1 via induction of potassium ion efflux in infected macrophages. Infect. Immun. 2009, 77:3992-4001.
125. Ladel C.H., Blum C., Dreher A., Reifenberg K., Kopf M., Kaufmann S.H. Lethal tuberculosis in interleukin-6-deficient mutant mice. Infect. Immun. 1997, 65:4843-4849.
126. Laing K.J., Grabowski P.S., Belosevic M., Secombes C.J. A partial sequence for nitric oxide synthase from a goldfish (Carassius auratus) macrophage cell line. Immunol. Cell Biol. 1996, 74:374-379.
127. Laing K.J., Hardie L.J., Aartsen W., Grabowski P.S., Secombes C.J. Expression of an inducible nitric oxide synthase gene in rainbow trout Oncorhynchus mykiss. Dev. Comp. Immunol. 1999, 23:71-85.
128. Lauth X., Babon J.J., Stannard J.A., Singh S., Nizet V., Carlberg J.M., Ostland V.E., Pennington M.W., Norton R.S., Westerman M.E. Bass hepcidin synthesis, solution structure, antimicrobial activities and synergism, and in vivo hepatic response to bacterial infections. J. Biol. Chem. 2005, 280:9272-9282.
129. Leclercq V., Lebastard M., Belkaid Y., Louis J., Milon G. The outcome of the parasitic process initiated by Leishmania infantum in laboratory mice: a tissue-dependent pattern controlled by the Lsh and MHC loci. J. Immunol. 1996, 157:4537-4545.
130. Lerena M.C., Colombo M.I. Mycobacterium marinum induces a marked LC3 recruitment to its containing phagosome that depends on a functional ESX-1 secretion system. Cell. Microbiol. 2011, 13:814-835.
131. Leto T.L., Lomax K.J., Volpp B.D., Nunoi H., Sechler J.M., Nauseef W.M., Clark R.A., Gallin J.I., Malech H.L. Cloning of a 67-kD neutrophil oxidase factor with similarity to a noncatalytic region of p60c-src. Science 1990, 248:727-730.
132. Li N., Zhang J., Zhang L.Q., Nie P. Difference in genes between a high virulence strain G(4) and a low virulence strain G(18) of Flavobacterium columnare by using suppression subtractive hybridization. J. Fish Dis. 2010, 33:403-412.
133. Liew F.Y., Li Y., Moss D., Parkinson C., Rogers M.V., Moncada S. Resistance to Leishmania major infection correlates with the induction of nitric oxide synthase in murine macrophages. Eur. J. Immunol. 1991, 21:3009-3014.
134. Liew F.Y., Xu D., Brint E.K., O'Neill L.A. Negative regulation of toll-like receptor-mediated immune responses. Nat. Rev. Immunol. 2005, 5:446-458.
135. Litwin C.M., Byrne B.L. Cloning and characterization of an outer membrane protein of Vibrio vulnificus required for heme utilization: regulation of expression and determination of the gene sequence. Infect. Immun. 1998, 66:3134-3141.
136. Litwin C.M., Rayback T.W., Skinner J. Role of catechol siderophore synthesis in Vibrio vulnificus virulence. Infect. Immun. 1996, 64:2834-2838.
137. Lowenstein C.J., Padalko E. INOS (NOS2) at a glance. J. Cell Sci. 2004, 117:2865-2867.
138. Luo M., Fadeev E.A., Groves J.T. Mycobactin-mediated iron acquisition within macrophages. Nat. Chem. Biol. 2005, 1:149-153.
139. Ma Q., Jones D., Springer T.A. The chemokine receptor CXCR4 is required for the retention of B lineage and granulocytic precursors within the bone marrow microenvironment. Immunity 1999, 10:463-471.
140. Mathew J.A., Tan Y.P., Srinivasa Rao P.S., Lim T.M., Leung K.Y. Edwardsiella tarda mutants defective in siderophore production, motility, serum resistance and catalase activity. Microbiology 2001, 147:449-457.
141. Mayumi M., Takeda Y., Hoshiko M., Serada K., Murata M., Moritomo T., Takizawa F., Kobayashi I., Araki K., Nakanishi T., Sumimoto H. Characterization of teleost phagocyte NADPH oxidase: molecular cloning and expression analysis of carp (Cyprinus carpio) phagocyte NADPH oxidase. Mol. Immunol. 2008, 45:1720-1731.
142. Meijer A.H., van der Sar A.M., Cunha C., Lamers G.E., Laplante M.A., Kikuta H., Bitter W., Becker T.S., Spaink H.P. Identification and real-time imaging of a myc-expressing neutrophil population involved in inflammation and mycobacterial granuloma formation in zebrafish. Dev. Comp. Immunol. 2008, 32:36-49.
143. Metzger D.C., Elliott D.G., Wargo A., Park L.K., Purcell M.K. Pathological and immunological responses associated with differential survival of Chinook salmon following Renibacterium salmoninarum challenge. Dis. Aquat. Organ. 2010, 90:31-41.
144. Mizrahi A., Berdichevsky Y., Ugolev Y., Molshanski-Mor S., Nakash Y., Dahan I., Alloul N., Gorzalczany Y., Sarfstein R., Hirshberg M., Pick E. Assembly of the phagocyte NADPH oxidase complex: chimeric constructs derived from the cytosolic components as tools for exploring structure-function relationships. J. Leukoc. Biol. 2006, 79:881-895.
145. Mizushima N., Yoshimori T., Ohsumi Y. The role of Atg proteins in autophagosome formation. Annu. Rev. Cell Dev. Biol. 2010, 27:107-132.
146. Molloy A., Laochumroonvorapong P., Kaplan G. Apoptosis, but not necrosis, of infected monocytes is coupled with killing of intracellular bacillus Calmette-Guerin. J. Exp. Med. 1994, 180:1499-1509.
147. Montero M.T., Matilla J., Gomez-Mampaso E., Lasuncion M.A. Geranylgeraniol regulates negatively caspase-1 autoprocessing: implication in the Th1 response against Mycobacterium tuberculosis. J. Immunol. 2004, 173:4936-4944.
148. Mori M. Regulation of nitric oxide synthesis and apoptosis by arginase and arginine recycling. J. Nutr. 2007, 137:1616S-1620S.
149. Mott J., Rikihisa Y., Tsunawaki S. Effects of Anaplasma phagocytophila on NADPH oxidase components in human neutrophils and HL-60 cells. Infect. Immun. 2002, 70:1359-1366.
150. Nairz M., Fritsche G., Crouch M.L., Barton H.C., Fang F.C., Weiss G. Slc11a1 limits intracellular growth of Salmonella enterica vs. typhimurium by promoting macrophage immune effector functions and impairing bacterial iron acquisition. Cell. Microbiol. 2009, 11:1365-1381.
151. Najimi M., Lemos M.L., Osorio C.R. Identification of siderophore biosynthesis genes essential for growth of Aeromonas salmonicida under iron limitation conditions. Appl. Environ. Microbiol. 2008, 74:2341-2348.
152. Najimi M., Lemos M.L., Osorio C.R. Identification of iron regulated genes in the fish pathogen Aeromonas salmonicida subsp. salmonicida: genetic diversity and evidence of conserved iron uptake systems. Vet. Microbiol. 2009, 133:377-382.
153. Naka H., Chen Q., Mitoma Y., Nakamura Y., McIntosh-Tolle D., Gammie A.E., Tolmasky M.E., Crosa J.H. Two replication regions in the pJM1 virulence plasmid of the marine pathogen Vibrio anguillarum. Plasmid 2012, 67:95-101.
154. Nascimento D.S., Pereira P.J., Reis M.I., Do Vale A., Zou J., Silva M.T., Secombes C.J., dos Santos N.M. Molecular cloning and expression analysis of sea bass (Dicentrarchus labrax L.) tumor necrosis factor-alpha (TNF-alpha). Fish Shellfish Immunol. 2007, 23:701-710.
155. Nathan C., Xie Q.W. Nitric oxide synthases: roles, tolls, and controls. Cell 1994, 78:915-918.
156. Nemeth E., Rivera S., Gabayan V., Keller C., Taudorf S., Pedersen B.K., Ganz T. IL-6 mediates hypoferremia of inflammation by inducing the synthesis of the iron regulatory hormone hepcidin. J. Clin. Invest. 2004, 113:1271-1276.
157. Nemeth E., Tuttle M.S., Powelson J., Vaughn M.B., Donovan A., Ward D.M., Ganz T., Kaplan J. Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization. Science 2004, 306:2090-2093.
158. Neumann N.F., Barreda D.R., Belosevic M. Generation and functional analysis of distinct macrophage sub-populations from goldfish (Carassius auratus L.) kidney leukocyte cultures. Fish Shellfish Immunol. 2000, 10:1-20.
159. Neumann N.F., Stafford J.L., Barreda D., Ainsworth A.J., Belosevic M. Antimicrobial mechanisms of fish phagocytes and their role in host defense. Dev. Comp. Immunol. 2001, 25:807-825.
160. Ng V.H., Cox J.S., Sousa A.O., MacMicking J.D., McKinney J.D. Role of KatG catalase-peroxidase in mycobacterial pathogenesis: countering the phagocyte oxidative burst. Mol. Microbiol. 2004, 52:1291-1302.
161. Nikoskelainen S., Verho S., Airas K., Lilius E.M. Adhesion and ingestion activities of fish phagocytes induced by bacterium Aeromonas salmonicida can be distinguished and directly measured from highly diluted whole blood of fish. Dev. Comp. Immunol. 2005, 29:525-537.
162. Noss E.H., Pai R.K., Sellati T.J., Radolf J.D., Belisle J., Golenbock D.T., Boom W.H., Harding C.V. Toll-like receptor 2-dependent inhibition of macrophage class II MHC expression and antigen processing by 19-kDa lipoprotein of Mycobacterium tuberculosis. J. Immunol. 2001, 167:910-918.
163. Oladiran A., Belosevic M. Trypanosoma carassii hsp70 increases expression of inflammatory cytokines and chemokines in macrophages of the goldfish (Carassius auratus L.). Dev. Comp. Immunol. 2009, 33:1128-1136.
164. Olavarria V.H., Gallardo L., Figueroa J.E., Mulero V. Lipopolysaccharide primes the respiratory burst of Atlantic salmon SHK-1 cells through protein kinase C-mediated phosphorylation of p47phox. Dev. Comp. Immunol. 2010, 34:1242-1253.
165. Osorio C.R., Juiz-Rio S., Lemos M.L. The ABC-transporter hutCD genes of Photobacterium damselae subsp. piscicida are essential for haem utilization as iron source and are expressed during infection in fish. J. Fish Dis. 2010, 33:649-655.
166. Padros F., Zarza C., Dopazo L., Cuadrado M., Crespo S. Pathology of Edwardsiella tarda infection in turbot, Scophthalmus maximus (L.). J. Fish Dis. 2006, 29:87-94.
167. Pagan-Ramos E., Master S.S., Pritchett C.L., Reimschuessel R., Trucksis M., Timmins G.S., Deretic V. Molecular and physiological effects of mycobacterial oxyR inactivation. J. Bacteriol. 2006, 188:2674-2680.
168. Palti Y. Toll-like receptors in bony fish: from genomics to function. Dev. Comp. Immunol. 2011, 35:1263-1272.
169. Parikka M., Hammaren M.M., Harjula S.K., Halfpenny N.J., Oksanen K.E., Lahtinen M.J., Pajula E.T., Iivanainen A., Pesu M., Ramet M. Mycobacterium marinum causes a latent infection that can be reactivated by gamma irradiation in adult zebrafish. PLoS Pathog. 2012, 8:e1002944.
170. Park Y.K., Bearson B., Bang S.H., Bang I.S., Foster J.W. Internal pH crisis, lysine decarboxylase and the acid tolerance response of Salmonella typhimurium. Mol. Microbiol. 1996, 20:605-611.
171. Parkos C.A., Allen R.A., Cochrane C.G., Jesaitis A.J. Purified cytochrome b from human granulocyte plasma membrane is comprised of two polypeptides with relative molecular weights of 91,000 and 22,000. J. Clin. Invest. 1987, 80:732-742.
172. Parkos C.A., Allen R.A., Cochrane C.G., Jesaitis A.J. The quaternary structure of the plasma membrane b-type cytochrome of human granulocytes. Biochim. Biophys. Acta. 1988, 932:71-83.
173. Parkos C.A., Dinauer M.C., Walker L.E., Allen R.A., Jesaitis A.J., Orkin S.H. Primary structure and unique expression of the 22-kilodalton light chain of human neutrophil cytochrome b. Proc. Natl. Acad. Sci. U.S.A. 1988, 85:3319-3323.
174. Peddie S., McLauchlan P.E., Ellis A.E., Secombes C.J. Effect of intraperitoneally administered IL-1beta-derived peptides on resistance to viral haemorrhagic septicaemia in rainbow trout Oncorhynchus mykiss. Dis. Aquat. Organ. 2003, 56:195-200.
175. Pereiro P., Figueras A., Novoa B. A novel hepcidin-like in turbot (Scophthalmus maximus L.) highly expressed after pathogen challenge but not after iron overload. Fish Shellfish Immunol. 2012, 32:879-889.
176. Phennicie R.T., Sullivan M.J., Singer J.T., Yoder J.A., Kim C.H. Specific resistance to Pseudomonas aeruginosa infection in zebrafish is mediated by the cystic fibrosis transmembrane conductance regulator. Infect. Immun. 2010, 78:4542-4550.
177. Porcelli S.A., Jacobs W.R. Tuberculosis: unsealing the apoptotic envelope. Nat. Immunol. 2008, 9:1101-1102.
178. Pym A.S., Brodin P., Brosch R., Huerre M., Cole S.T. Loss of RD1 contributed to the attenuation of the live tuberculosis vaccines Mycobacterium bovis BCG and Mycobacterium microti. Mol. Microbiol. 2002, 46:709-717.
179. Raivio T.L. Envelope stress responses and Gram-negative bacterial pathogenesis. Mol. Microbiol. 2005, 56:1119-1128.
180. Rieger A.M., Hall B.E., Barreda D.R. Macrophage activation differentially modulates particle binding, phagocytosis and downstream antimicrobial mechanisms. Dev. Comp. Immunol. 2010, 34:1144-1159.
181. Rio S.J., Osorio C.R., Lemos M.L. Heme uptake genes in human and fish isolates of Photobacterium damselae: existence of hutA pseudogenes. Arch Microbiol. 2005, 183:347-358.
182. Roach T.I., Kiderlen A.F., Blackwell J.M. Role of inorganic nitrogen oxides and tumor necrosis factor alpha in killing Leishmania donovani amastigotes in gamma interferon-lipopolysaccharide-activated macrophages from Lshs and Lshr congenic mouse strains. Infect. Immun. 1991, 59:3935-3944.
183. Robinson J.M. Reactive oxygen species in phagocytic leukocytes. Histochem. Cell Biol. 2008, 130:281-297.
184. Robinson J.M. Phagocytic leukocytes and reactive oxygen species. Histochem. Cell Biol. 2009, 131:465-469.
185. Robinson N., Wolke M., Ernestus K., Plum G. A mycobacterial gene involved in synthesis of an outer cell envelope lipid is a key factor in prevention of phagosome maturation. Infect. Immun. 2007, 75:581-591.
186. Roca F.J., Ramakrishnan L. TNF dually mediates resistance and susceptibility to mycobacteria via mitochondrial reactive oxygen species. Cell 2013, 153:521-534.
187. Rodgers C.J., Mohan C.V., Peeler E.J. The spread of pathogens through trade in aquatic animals and their products. Rev. Sci. Tech. 2011, 30:241-256.
188. Rodriguez I., Novoa B., Figueras A. Immune response of zebrafish (Danio rerio) against a newly isolated bacterial pathogen Aeromonas hydrophila. Fish Shellfish Immunol. 2008, 25:239-249.
189. Rogall T., Flohr T., Bottger E.C. Differentiation of Mycobacterium species by direct sequencing of amplified DNA. J. Gen. Microbiol. 1990, 136:1915-1920.
190. Rogall T., Wolters J., Flohr T., Bottger E.C. Towards a phylogeny and definition of species at the molecular level within the genus Mycobacterium. Int. J. Syst. Bacteriol. 1990, 40:323-330.
191. Rombouts Y., Burguiere A., Maes E., Coddeville B., Elass E., Guerardel Y., Kremer L. Mycobacterium marinum lipooligosaccharides are unique caryophyllose-containing cell wall glycolipids that inhibit tumor necrosis factor-alpha secretion in macrophages. J. Biol. Chem. 2009, 284:20975-20988.
192. Rubbo H., Denicola A., Radi R. Peroxynitrite inactivates thiol-containing enzymes of Trypanosoma cruzi energetic metabolism and inhibits cell respiration. Arch. Biochem. Biophys. 1994, 308:96-102.
193. Ruley K.M., Ansede J.H., Pritchett C.L., Talaat A.M., Reimschuessel R., Trucksis M. Identification of Mycobacterium marinum virulence genes using signature-tagged mutagenesis and the goldfish model of mycobacterial pathogenesis. FEMS Microbiol. Lett. 2004, 232:75-81.
194. Ruley K.M., Reimschuessel R., Trucksis M. Goldfish as an animal model system for mycobacterial infection. Methods Enzymol. 2002, 358:29-39.
195. Russo R., Shoemaker C.A., Panangala V.S., Klesius P.H. In vitro and in vivo interaction of macrophages from vaccinated and non-vaccinated channel catfish (Ictalurus punctatus) to Edwardsiella ictaluri. Fish Shellfish Immunol. 2009, 26:543-552.
196. Ryckaert J., Bossier P., D'Herde K., Diez-Fraile A., Sorgeloos P., Haesebrouck F., Pasmans F. Persistence of Yersinia ruckeri in trout macrophages. Fish Shellfish Immunol. 2010, 29:648-655.
197. Saeij J.P., Stet R.J., Groeneveld A., Verburg-van Kemenade L.B., van Muiswinkel W.B., Wiegertjes G.F. Molecular and functional characterization of a fish inducible-type nitric oxide synthase. Immunogenetics 2000, 51:339-346.
198. Saeij J.P., Wiegertjes G.F., Stet R.J. Identification and characterization of a fish natural resistance-associated macrophage protein (NRAMP) cDNA. Immunogenetics 1999, 50:60-66.
199. Sahoo P.K., Rauta P.R., Mohanty B.R., Mahapatra K.D., Saha J.N., Rye M., Eknath A.E. Selection for improved resistance to Aeromonas hydrophila in Indian major carp Labeo rohita: survival and innate immune responses in first generation of resistant and susceptible lines. Fish Shellfish Immunol. 2011, 31:432-438.
200. Sandy M., Butler A. Microbial iron acquisition: marine and terrestrial siderophores. Chem. Rev. 2009, 109:4580-4595.
201. Scannell M., Flanagan M.B., deStefani A., Wynne K.J., Cagney G., Godson C., Maderna P. Annexin-1 and peptide derivatives are released by apoptotic cells and stimulate phagocytosis of apoptotic neutrophils by macrophages. J. Immunol. 2007, 178:4595-4605.
202. Schellhorn H.E. Regulation of hydroperoxidase (catalase) expression in Escherichia coli. FEMS Microbiol. Lett. 1995, 131:113-119.
203. Schmidtchen A., Frick I.M., Andersson E., Tapper H., Bjorck L. Proteinases of common pathogenic bacteria degrade and inactivate the antibacterial peptide LL-37. Mol. Microbiol. 2002, 46:157-168.
204. Searle S., Bright N.A., Roach T.I., Atkinson P.G., Barton C.H., Meloen R.H., Blackwell J.M. Localisation of Nramp1 in macrophages: modulation with activation and infection. J. Cell Sci. 1998, 111(Pt 19):2855-2866.
205. Secombes C.J. Lymphokine-release from rainbow trout leucocytes stimulated with concanavalin A. Effects upon macrophage spreading and adherence. Dev. Comp. Immunol. 1987, 11:513-520.
206. Senaldi G., Yin S., Shaklee C.L., Piguet P.F., Mak T.W., Ulich T.R. Corynebacterium parvum- and Mycobacterium bovis bacillus Calmette-Guerin-induced granuloma formation is inhibited in TNF receptor I (TNF-RI) knockout mice and by treatment with soluble TNF-RI. J. Immunol. 1996, 157:5022-5026.
207. Sepulcre M.P., Sarropoulou E., Kotoulas G., Meseguer J., Mulero V. Vibrio anguillarum evades the immune response of the bony fish sea bass (Dicentrarchus labrax L.) through the inhibition of leukocyte respiratory burst and down-regulation of apoptotic caspases. Mol. Immunol. 2007, 44:3751-3757.
208. Sharifuzzaman S.M., Abbass A., Tinsley J.W., Austin B. Subcellular components of probiotics Kocuria SM1 and Rhodococcus SM2 induce protective immunity in rainbow trout (Oncorhynchus mykiss, Walbaum) against Vibrio anguillarum. Fish Shellfish Immunol. 2011, 30:347-353.
209. Sheppard F.R., Kelher M.R., Moore E.E., McLaughlin N.J., Banerjee A., Silliman C.C. Structural organization of the neutrophil NADPH oxidase: phosphorylation and translocation during priming and activation. J. Leukoc. Biol. 2005, 78:1025-1042.
210. Sibthorpe D., Baker A.M., Gilmartin B.J., Blackwell J.M., White J.K. Comparative analysis of two slc11 (Nramp) loci in Takifugu rubripes. DNA Cell Biol. 2004, 23:45-58.
211. Simeone R., Bobard A., Lippmann J., Bitter W., Majlessi L., Brosch R., Enninga J. Phagosomal rupture by Mycobacterium tuberculosis results in toxicity and host cell death. PLoS Pathog. 2012, 8:e1002507.
212. Skamene E., Gros P., Forget A., Patel P.J., Nesbitt M.N. Regulation of resistance to leprosy by chromosome 1 locus in the mouse. Immunogenetics 1984, 19:117-124.
213. Smith J., Manoranjan J., Pan M., Bohsali A., Xu J., Liu J., McDonald K.L., Szyk A., LaRonde-LeBlanc N., Gao L.Y. Evidence for pore formation in host cell membranes by ESX-1-secreted ESAT-6 and its role in Mycobacterium marinum escape from the vacuole. Infect. Immun. 2008, 76:5478-5487.
214. Sorensen O.E., Follin P., Johnsen A.H., Calafat J., Tjabringa G.S., Hiemstra P.S., Borregaard N. Human cathelicidin, hCAP-18, is processed to the antimicrobial peptide LL-37 by extracellular cleavage with proteinase 3. Blood 2001, 97:3951-3959.
215. Srinivasa Rao P.S., Lim T.M., Leung K.Y. Opsonized virulent Edwardsiella tarda strains are able to adhere to and survive and replicate within fish phagocytes but fail to stimulate reactive oxygen intermediates. Infect. Immun. 2001, 69:5689-5697.
216. Srinivasa Rao P.S., Lim T.M., Leung K.Y. Functional genomics approach to the identification of virulence genes involved in Edwardsiella tarda pathogenesis. Infect. Immun. 2003, 71:1343-1351.
217. Srinivasa Rao P.S., Yamada Y., Leung K.Y. A major catalase (KatB) that is required for resistance to H2O2 and phagocyte-mediated killing in Edwardsiella tarda. Microbiology 2003, 149:2635-2644.
218. St John G., Brot N., Ruan J., Erdjument-Bromage H., Tempst P., Weissbach H., Nathan C. Peptide methionine sulfoxide reductase from Escherichia coli and Mycobacterium tuberculosis protects bacteria against oxidative damage from reactive nitrogen intermediates. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:9901-9906.
219. Stafford J.L., Belosevic M. Transferrin and the innate immune response of fish: identification of a novel mechanism of macrophage activation. Dev. Comp. Immunol. 2003, 27:539-554.
220. Stafford J.L., Neumann N.F., Belosevic M. Products of proteolytic cleavage of transferrin induce nitric oxide response of goldfish macrophages. Dev. Comp. Immunol. 2001, 25:101-115.
221. Stafford J.L., Wilson E.C., Belosevic M. Recombinant transferrin induces nitric oxide response in goldfish and murine macrophages. Fish Shellfish Immunol. 2004, 17:171-185.
222. Stamm L.M., Morisaki J.H., Gao L.Y., Jeng R.L., McDonald K.L., Roth R., Takeshita S., Heuser J., Welch M.D., Brown E.J. Mycobacterium marinum escapes from phagosomes and is propelled by actin-based motility. J. Exp. Med. 2003, 198:1361-1368.
223. Stamm L.M., Pak M.A., Morisaki J.H., Snapper S.B., Rottner K., Lommel S., Brown E.J. Role of the WASP family proteins for Mycobacterium marinum actin tail formation. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:14837-14842.
224. Stoop E.J., Schipper T., Huber S.K., Nezhinsky A.E., Verbeek F.J., Gurcha S.S., Besra G.S., Vandenbroucke-Grauls C.M., Bitter W., van der Sar A.M. Zebrafish embryo screen for mycobacterial genes involved in the initiation of granuloma formation reveals a newly identified ESX-1 component. Dis. Model. Mech. 2011, 4:526-536.
225. Stuehr D.J., Nathan C.F. Nitric oxide. A macrophage product responsible for cytostasis and respiratory inhibition in tumor target cells. J. Exp. Med. 1989, 169:1543-1555.
226. Sturgill-Koszycki S., Schaible U.E., Russell D.G. Mycobacterium-containing phagosomes are accessible to early endosomes and reflect a transitional state in normal phagosome biogenesis. Embo J. 1996, 15:6960-6968.
227. Sturgill-Koszycki S., Schlesinger P.H., Chakraborty P., Haddix P.L., Collins H.L., Fok A.K., Allen R.D., Gluck S.L., Heuser J., Russell D.G. Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science 1994, 263:678-681.
228. Subbian S., Mehta P.K., Cirillo S.L., Bermudez L.E., Cirillo J.D. A Mycobacterium marinum mel2 mutant is defective for growth in macrophages that produce reactive oxygen and reactive nitrogen species. Infect. Immun. 2007, 75:127-134.
229. Subbian S., Mehta P.K., Cirillo S.L., Cirillo J.D. The Mycobacterium marinum mel2 locus displays similarity to bacterial bioluminescence systems and plays a role in defense against reactive oxygen and nitrogen species. BMC Microbiol. 2007, 7:4.
230. Swaim L.E., Connolly L.E., Volkman H.E., Humbert O., Born D.E., Ramakrishnan L. Mycobacterium marinum infection of adult zebrafish causes caseating granulomatous tuberculosis and is moderated by adaptive immunity. Infect. Immun. 2006, 74:6108-6117.
231. Tan T., Lee W.L., Alexander D.C., Grinstein S., Liu J. The ESAT-6/CFP-10 secretion system of Mycobacterium marinum modulates phagosome maturation. Cell. Microbiol. 2006, 8:1417-1429.
232. Taylor M.W., Feng G.S. Relationship between interferon-gamma, indoleamine 2,3-dioxygenase, and tryptophan catabolism. Faseb J. 1991, 5:2516-2522.
233. Thi E.P., Hong C.J., Sanghera G., Reiner N.E. Identification of the Mycobacterium tuberculosis protein PE-PGRS62 as a novel effector that functions to block phagosome maturation and inhibit iNOS expression. Cell. Microbiol. 2013, 15:795-808.
234. Thomson L., Denicola A., Radi R. The trypanothione-thiol system in Trypanosoma cruzi as a key antioxidant mechanism against peroxynitrite-mediated cytotoxicity. Arch. Biochem. Biophys. 2003, 412:55-64.
235. Tsunawaki S., Kagara S., Yoshikawa K., Yoshida L.S., Kuratsuji T., Namiki H. Involvement of p40phox in activation of phagocyte NADPH oxidase through association of its carboxyl-terminal, but not its amino-terminal, with p67phox. J. Exp. Med. 1996, 184:893-902.
236. Tsunawaki S., Mizunari H., Nagata M., Tatsuzawa O., Kuratsuji T. A novel cytosolic component, p40phox, of respiratory burst oxidase associates with p67phox and is absent in patients with chronic granulomatous disease who lack p67phox. Biochem. Biophys. Res. Commun. 1994, 199:1378-1387.
237. van de Vosse E., Hoeve M.A., Ottenhoff T.H. Human genetics of intracellular infectious diseases: molecular and cellular immunity against mycobacteria and salmonellae. Lancet Infect. Dis. 2004, 4:739-749.
238. van der Vaart M., van Soest J.J., Spaink H.P., Meijer A.H. Functional analysis of a zebrafish myd88 mutant identifies key transcriptional components of the innate immune system. Dis. Model. Mech. 2013, 6:841-854.
239. van der Wel N., Hava D., Houben D., Fluitsma D., van Zon M., Pierson J., Brenner M., Peters P.J. M. tuberculosis and M. leprae translocate from the phagolysosome to the cytosol in myeloid cells. Cell 2007, 129:1287-1298.
240. Vandal O.H., Pierini L.M., Schnappinger D., Nathan C.F., Ehrt S. A membrane protein preserves intrabacterial pH in intraphagosomal Mycobacterium tuberculosis. Nat. Med. 2008, 14:849-854.
241. Vidal S., Gros P., Skamene E. Natural resistance to infection with intracellular parasites: molecular genetics identifies Nramp1 as the Bcg/Ity/Lsh locus. J. Leukoc. Biol. 1995, 58:382-390.
242. Vidal S., Tremblay M.L., Govoni G., Gauthier S., Sebastiani G., Malo D., Skamene E., Olivier M., Jothy S., Gros P. The Ity/Lsh/Bcg locus: natural resistance to infection with intracellular parasites is abrogated by disruption of the Nramp1 gene. J. Exp. Med. 1995, 182:655-666.
243. Villamil L., Figueras A., Aranguren R., Novoa B. Non-specific immune response of turbot, Scophthalmus maximus (L.), experimentally infected with a pathogenic Vibrio pelagius. J. Fish Dis. 2003, 26:321-329.
244. Volkman H.E., Pozos T.C., Zheng J., Davis J.M., Rawls J.F., Ramakrishnan L. Tuberculous granuloma induction via interaction of a bacterial secreted protein with host epithelium. Science 2010, 327:466-469.
245. Volpp B.D., Nauseef W.M., Donelson J.E., Moser D.R., Clark R.A. Cloning of the cDNA and functional expression of the 47-kilodalton cytosolic component of human neutrophil respiratory burst oxidase. Proc. Natl. Acad. Sci. U.S.A. 1989, 86:7195-7199.
246. Wandersman C., Delepelaire P. Bacterial iron sources: from siderophores to hemophores. Annu. Rev. Microbiol. 2004, 58:611-647.
247. Wang H., Dong D., Tang S., Chen X., Gao Q. PPE38 of Mycobacterium marinum triggers the cross-talk of multiple pathways involved in the host response, as revealed by subcellular quantitative proteomics. J. Proteome Res. 2013, 12:2055-2066.
248. Wang Q., Yang M., Xiao J., Wu H., Wang X., Lv Y., Xu L., Zheng H., Wang S., Zhao G., Liu Q., Zhang Y. Genome sequence of the versatile fish pathogen Edwardsiella tarda provides insights into its adaptation to broad host ranges and intracellular niches. PLoS One 2009, 4:e7646.
249. Wang T., Ward M., Grabowski P., Secombes C.J. Molecular cloning, gene organization and expression of rainbow trout (Oncorhynchus mykiss) inducible nitric oxide synthase (iNOS) gene. Biochem. J. 2001, 358:747-755.
250. Wang Y., Liu X., Ma L., Yu Y., Yu H., Mohammed S., Chu G., Mu L., Zhang Q. Identification and characterization of a hepcidin from half-smooth tongue sole Cynoglossus semilaevis. Fish Shellfish Immunol. 2012, 33:213-219.
251. Ward R.J., Crichton R.R., Taylor D.L., Della Corte L., Srai S.K., Dexter D.T. Iron and the immune system. J. Neural Transm. 2011, 118:315-328.
252. Watkins B.Y., Joshi S.A., Ball D.A., Leggett H., Park S., Kim J., Austin C.D., Paler-Martinez A., Xu M., Downing K.H., Brown E.J. Mycobacterium marinum SecA2 promotes stable granulomas and induces tumor necrosis factor alpha in vivo. Infect. Immun. 2012, 80:3512-3520.
253. Weerdenburg E.M., Abdallah A.M., Mitra S., de Punder K., van der Wel N.N., Bird S., Appelmelk B.J., Bitter W., van der Sar A.M. ESX-5-deficient Mycobacterium marinum is hypervirulent in adult zebrafish. Cell. Microbiol. 2012, 14:728-739.
254. Werner E.R., Werner-Felmayer G., Fuchs D., Hausen A., Reibnegger G., Wachter H. Parallel induction of tetrahydrobiopterin biosynthesis and indoleamine 2,3-dioxygenase activity in human cells and cell lines by interferon-gamma. Biochem. J. 1989, 262:861-866.
255. Werner-Felmayer G., Werner E.R., Fuchs D., Hausen A., Reibnegger G., Wachter H. Induction of indoleamine 2,3-dioxygenase in human cells in vitro. Adv. Exp. Med. Biol. 1991, 294:505-509.
256. Wiegertjes G.F., Forlenza M. Nitrosative stress during infection-induced inflammation in fish: lessons from a host-parasite infection model. Curr. Pharm. Des. 2010, 16:4194-4202.
257. Xiao J., Chen T., Wang Q., Zhang Y. Comparative analysis of the roles of catalases KatB and KatG in the physiological fitness and pathogenesis of fish pathogen Edwardsiella tarda. Lett. Appl. Microbiol. 2012, 54:425-432.
258. Xu J., Laine O., Masciocchi M., Manoranjan J., Smith J., Du S.J., Edwards N., Zhu X., Fenselau C., Gao L.Y. A unique Mycobacterium ESX-1 protein co-secretes with CFP-10/ESAT-6 and is necessary for inhibiting phagosome maturation. Mol. Microbiol. 2007, 66:787-800.
259. Xu T., Sun Y., Shi G., Wang R. Miiuy croaker hepcidin gene and comparative analyses reveal evidence for positive selection. PLoS One 2012, 7:e35449.
260. Xu Y., Jagannath C., Liu X.D., Sharafkhaneh A., Kolodziejska K.E., Eissa N.T. Toll-like receptor 4 is a sensor for autophagy associated with innate immunity. Immunity 2007, 27:135-144.
261. Yang C.G., Liu S.S., Sun B., Wang X.L., Wang N., Chen S.L. Iron-metabolic function and potential antibacterial role of Hepcidin and its correlated genes (Ferroportin 1 and Transferrin Receptor) in Turbot (Scophthalmus maximus). Fish Shellfish Immunol. 2013, 34:744-755.
262. Yang C.T., Cambier C.J., Davis J.M., Hall C.J., Crosier P.S., Ramakrishnan L. Neutrophils exert protection in the early tuberculous granuloma by oxidative killing of mycobacteria phagocytosed from infected macrophages. Cell Host Microbe. 2012, 12:301-312.
263. Yang M., Lv Y., Xiao J., Wu H., Zheng H., Liu Q., Zhang Y., Wang Q. Edwardsiella comparative phylogenomics reveal the new intra/inter-species taxonomic relationships, virulence evolution and niche adaptation mechanisms. PLoS One 2012, 7:e36987.
264. Yoshida R., Imanishi J., Oku T., Kishida T., Hayaishi O. Induction of pulmonary indoleamine 2,3-dioxygenase by interferon. Proc. Natl. Acad. Sci. U.S.A. 1981, 78:129-132.
265. Yuasa H.J., Takubo M., Takahashi A., Hasegawa T., Noma H., Suzuki T. Evolution of vertebrate indoleamine 2,3-dioxygenases. J. Mol. Evol. 2007, 65:705-714.
266. Zhang J., Jiang R., Takayama H., Tanaka Y. Survival of virulent Mycobacterium tuberculosis involves preventing apoptosis induced by Bcl-2 upregulation and release resulting from necrosis in J774 macrophages. Microbiol. Immunol. 2005, 49:845-852.
267. Zhang M., Xiao Z.Z., Sun L. Suppressor of cytokine signaling 3 inhibits head kidney macrophage activation and cytokine expression in Scophthalmus maximus. Dev. Comp. Immunol. 2011, 35:174-181.
268. Zheng W.J., Hu Y.H., Sun L. The two Dps of Edwardsiella tarda are involved in resistance against oxidative stress and host infection. Fish Shellfish Immunol. 2011, 31:985-992.
269. Zhou J.G., Wei J.G., Xu D., Cui H.C., Yan Y., Ou-Yang Z.L., Huang X.H., Huang Y.H., Qin Q.W. Molecular cloning and characterization of two novel hepcidins from orange-spotted grouper, Epinephelus coioides. Fish Shellfish Immunol. 2011, 30:559-568.
270. Zhu L., Gunn C., Beckman J.S. Bactericidal activity of peroxynitrite. Arch. Biochem. Biophys. 1992, 298:452-457.
271. Zou J., Carrington A., Collet B., Dijkstra J.M., Yoshiura Y., Bols N., Secombes C. Identification and bioactivities of IFN-gamma in rainbow trout Oncorhynchus mykiss: the first Th1-type cytokine characterized functionally in fish. J. Immunol. 2005, 175:2484-2494.
272. Zou J., Peddie S., Scapigliati G., Zhang Y., Bols N.C., Ellis A.E., Secombes C.J. Functional characterisation of the recombinant tumor necrosis factors in rainbow trout, Oncorhynchus mykiss. Dev. Comp. Immunol. 2003, 27:813-822.
273. Zwilling B.S., Kuhn D.E., Wikoff L., Brown D., Lafuse W. Role of iron in Nramp1-mediated inhibition of mycobacterial growth. Infect. Immun. 1999, 67:1386-1392.