Immunological stimuli change expression of genes and neutrophil function in fathead minnow Pimephales promelas Rafinesque

Journal of Fish Biology

Volumn 78, Issue 4, 2011, Pages 1054-1072

  Jovanovic B ^a   Goetz, F W ^b   Goetz, G W ^b   Palic D ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

Author keywords

CDNA libraries; Fish immunology; Granulocyte function; Immunogenomics; Lipopolysaccharide; Polyinosinic polycytidylic acid

Indexed keywords

FISH PROTEIN; IMMUNOLOGICAL ADJUVANT; LIPOPOLYSACCHARIDE; POLYINOSINIC POLYCYTIDYLIC ACID;

ANIMAL; ARTICLE; CYPRINIFORMES; DRUG EFFECT; EXPRESSED SEQUENCE TAG; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; NEUTROPHIL;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; CYPRINIDAE; EXPRESSED SEQUENCE TAGS; FISH PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; LIPOPOLYSACCHARIDES; NEUTROPHILS; POLY I-C;

BACTERIA (MICROORGANISMS); ORTHOMYXOVIRIDAE; PIMEPHALES PROMELAS; PISCES;

EID: 79953672177     PISSN: 00221112     EISSN: 10958649     Source Type: Journal    
DOI: 10.1111/j.1095-8649.2011.02919.x     Document Type: Article

References (71)

1. Aderem, A. & Ulevitch, R. J. (2000). Toll-like receptors in the induction of the innate immune response. Nature 406, 782-787.
2. Ankley, G. T. & Villeneuve, D. L. (2006). The fathead minnow in aquatic toxicology: past, present and future. Aquatic Toxicology 78, 91-102.
3. Arigita, C., Luijkx, T., Jiskoot, W., Poelen, M., Hennink, W. E., Crommelin, D. J. A., Ley, P., Els, C. & Kersten, G. F. A. (2005). Well-defined and potent liposomal meningococcal B vaccines adjuvated with LPS derivatives. Vaccine 23, 5091-5098.
4. Bahl, K., Kim, S.-K., Calcagno, C., Ghersi, D., Puzone, R., Celada, F., Selin, L. K. & Welsh, R. M. (2006). IFN-induced attrition of CD8 T cells in the presence or absence of cognate antigen during the early stages of viral infections. Journal of Immunology 176, 4284-4295.
5. Baoprasertkul, P., He, C., Peatman, E., Zhang, S., Li, P. & Liu, Z. (2005). Constitutive expression of three novel catfish CXC chemokines: homeostatic chemokines in teleost fish. Molecular Immunology 42, 1355-1366.
6. Berkman, N., Krishnan, V. L., Gilbey, T., Newton, R., O'Connor, B., Barnes, P. J. & Chung, K. F. (1996). Expression of RANTES mRNA and protein in airways of patients with mild asthma. American Journal of Respiratory and Critical Care Medicine 154, 1804-1811.
7. Beutler, B. (2002). LPS in microbial pathogenesis: promise and fulfilment. Journal of Endotoxin Research 8, 329-335.
8. 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 Leukocyte Biology 74, 1-7.
9. Biales, A. D., Bencic, D. C., Flick, R. W., Lazorchak, J. & Lattier, D. L. (2007). Quantification and associated variability of induced vitellogenin gene transcripts in fathead minnow (Pimephales promelas) by quantitative real-time polymerase chain reaction assay. Environmental Toxicology and Chemistry 26, 287-296.
10. Blaxhall, P. C. & Daisley, K. W. (1973). Routine haematological methods for use with fish blood. Journal of Fish Biology 5, 771-781.
11. Chomczynski, P. & Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Analytical Biochemistry 162, 156-159.
12. Chomczynski, P. & Sacchi, N. (2006). The single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction: twenty-something years on. Nature Protocols 1, 581-585.
13. Chuammitri, P., Ostojic, J., Andreasen, C. B., Redmond, S. B., Lamont, S. J. & Palić, D. (2009). Chicken heterophil extracellular traps (HETs): novel defense mechanism of chicken heterophils. Veterinary Immunology and Immunopathology 129, 126-131.
14. Dahlgren, C. & Karlsson, A. (1999). Respiratory burst in human neutrophils. Journal of Immunological Methods 232, 3-14.
15. De Becker, G., Moulin, V., Pajak, B., Bruck, C., Francotte, M., Thiriart, C., Urbain, J. & Moser, M. (2000). The adjuvant monophosphoryl lipid A increases the function of antigen-presenting cells. International Immunology 12, 807-815.
16. DeWitte-Orr, S. J., Leong, J.-A. C. & Bols, N. C. (2007). Induction of antiviral genes, Mx and vig-1, by dsRNA and Chum salmon reovirus in rainbow trout monocyte/macrophage and fibroblast cell lines. Fish & Shellfish Immunology 23, 670-682.
17. Fäldt, J., Dahlgren, C., Ridell, M. & Karlsson, A. (2001). Priming of human neutrophils by mycobacterial lipoarabinomannans: role of granule mobilisation. Microbes and Infection 3, 1101-1109.
18. Freudenberg, M. A., Tchaptchet, S., Keck, S., Fejer, G., Huber, M., Schütze, N., Beutler, B. & Galanos, C. (2008). Lipopolysaccharide sensing an important factor in the innate immune response to gram-negative bacterial infections: benefits and hazards of LPS hypersensitivity. Immunobiology 213, 193-203.
19. Fuchs, T. A., Abed, U., Goosmann, C., Hurwitz, R., Schulze, I., Wahn, V., Weinrauch, Y., Brinkmann, V. & Zychlinsky, A. (2007). Novel cell death program leads to neutrophil extracellular traps. Journal of Cell Biology 176, 231-241.
20. Goetz, F. W., Iliev, D. B., McCauley, L. A. R., 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.
21. Grayfer, L. & Belosevic, M. (2009). Molecular characterization, expression and functional analysis of goldfish (Carassius auratus L.) interferon gamma. Developmental & Comparative Immunology 33, 235-246.
22. Henricson, B. E., Manthey, C. L., Perera, P. Y., Hamilton, T. A. & Vogel, S. N. (1993). Dissociation of lipopolysaccharide (LPS)-inducible gene expression in murine macrophages pretreated with smooth LPS versus monophosphoryl lipid A. Infection and Immunity 61, 2325-2333.
23. Hermann, A. C., Millard, P. J., Blake, S. L. & Kim, C. H. (2004). Development of a respiratory burst assay using zebrafish kidneys and embryos. Journal of Immunological Methods 292, 119-129.
24. Holzinger, D., Jorns, C., Stertz, S., Boisson-Dupuis, S., Thimme, R., Weidmann, M., Casanova, J.-L., Haller, O. & Kochs, G. (2007). Induction of MxA gene expression by influenza A virus requires type I or type III interferon signaling. Journal of Virology 81, 7776-7785.
25. Huising, M. O., Meulen, T., Flik, G. & Verburg-van Kemenade, B. M. L. (2004). Three novel carp CXC chemokines are expressed early in ontogeny and at nonimmune sites. European Journal of Biochemistry 271, 4094-4106.
26. Iliev, D. B., Roach, J. C., Mackenzie, S., Planas, J. V. & Goetz, F. W. (2005). Endotoxin recognition: in fish or not in fish? FEBS Letters 579, 6519-6528.
27. Iliev, D. B., Goetz, G. W., MacKenzie, S., Planas, J. V. & Goetz, F. W. (2006). Pathogen-associated gene expression profiles in rainbow trout macrophages. Comparative Biochemistry and Physiology D 1, 416-422.
28. Janeway, C. A. & Medzhitov, R. (2002). Innate immune recognition. Annual Review of Immunology 20, 197-216.
29. Janeway, C. A., Murphy, K. P., Travers, P. & Walport, M. (2008). Janeway's Immuno Biology. New York, NY: Garland Science.
30. Jia, W. & Guo, Q. (2008). Gene structures and promoter characteristics of interferon regulatory factor 1 (IRF-1), IRF-2 and IRF-7 from snakehead Channa argus. Molecular Immunology 45, 2419-2428.
31. Jirillo, E., Caccavo, D., Magrone, T., Piccigallo, E., Amati, L., Lembo, A., Kalis, C. & Gumenscheimer, M. (2002). The role of the liver in the response to LPS: experimental and clinical findings. Innate Immunity 8, 319-327.
32. Kerr, D. E., Latshaw, M., Pareek, R., Zheng, J. & Bond, J. P. (2009). Genomic responses of the bovine mammary gland and epithelial cells to acute LPS challenge. Veterinary Immunology and Immunopathology 128, 214.
33. Kileng, Ø., Albuquerque, A. & Robertsen, B. (2008). Induction of interferon system genes in Atlantic salmon by the imidazoquinoline S-27609, a ligand for Toll-like receptor 7. Fish & Shellfish Immunology 24, 514-522.
34. Kraaijeveld, A. O., de Jager, S. C. A., de Jager, W. J., Prakken, B. J., McColl, S. R., Haspels, I., Putter, H., van Berkel, T. J. C., Nagelkerken, L., Jukema, J. W. & Biessen, E. A. L. (2007). CC chemokine ligand-5 (CCL5/RANTES) and CC chemokine ligand-18 (CCL18/PARC) are specific markers of refractory unstable angina pectoris and are transiently raised during severe ischemic symptoms. Circulation 116, 1931-1941.
35. Kuna, P., Alam, R., Ruta, U. & Gorski, P. (1998). RANTES induces nasal mucosal inflammation rich in eosinophils, basophils, and lymphocytes in vivo. American Journal of the Respiratory and Critical Care Medicine 157, 873-879.
36. Leu, J.-H., Yan, S.-J., Lee, T.-F., Chou, C.-M., Chen, S.-T., Hwang, P.-P., Chou, C.-K. & Huang, C.-J. (2000). Complete genomic organization and promoter analysis of the round-spotted pufferfish JAK1, JAK2, JAK3, and TYK2 genes. DNA and Cell Biology 19, 431-446.
37. Lockhart, K., Bowden, T. J. & Ellis, A. E. (2004). Poly I:C-induced Mx responses in Atlantic salmon parr, post-smolts and growers. Fish & Shellfish Immunology 17, 245-254.
38. MacKenzie, S., Liarte, C., Iliev, D., Planas, J. V., Tort, L. & Goetz, F. W. (2004). Characterization of a highly inducible novel CC chemokine from differentiated rainbow trout (Oncorhynchus mykiss) macrophages. Immunogenetics 56, 611-615.
39. MacKenzie, S., Roher, N., Boltana, S. & Goetz, F. W. (2010). Peptidoglycan, not endotoxin, is the key mediator of lipopolysaccharide-induced cytokine expression in trout macrophages. Molecular Immunology 47, 1450-1457.
40. Mager, E. M., Wintz, H., Vulpe, C. D., Brix, K. V. & Grosell, M. (2008). Toxicogenomics of water chemistry influence on chronic lead exposure to the fathead minnow (Pimephales promelas). Aquatic Toxicology 87, 200-209.
41. Mamane, Y., Heylbroeck, C., Génin, P., Algarté, M., Servant, M. J., LePage, C., DeLuca, C., Kwon, H., Lin, R. & Hiscott, J. (1999). Interferon regulatory factors: the next generation. Gene 237, 1-14.
42. Matsumoto, M. & Seya, T. (2008). TLR3: interferon induction by double-stranded RNA including poly(I:C). Advanced Drug Delivery Reviews 60, 805-812.
43. Matsuo, A., Oshiumi, H., Tsujita, T., Mitani, H., Kasai, H., Yoshimizu, M., Matsumoto, M. & Seya, T. (2008). Teleost TLR22 recognizes RNA duplex to induce IFN and protect cells from Birnaviruses. Journal of Immunology 181, 3474-3485.
44. Medzhitov, R. (2001). Toll-like receptors and innate immunity. Nature Reviews Immunology 1, 135-145.
45. Nhu, Q. M., Cuesta, N. & Vogel, S. N. (2006). Transcriptional regulation of lipopolysaccharide (LPS)-induced Toll-like receptor (TLR) expression in murine macrophages: role of interferon regulatory factors 1 (IRF-1) and 2 (IRF-2). Innate Immunity 12, 285-295.
46. Nigou, J., Gilleron, M. & Puzo, G. (2003). Lipoarabinomannans: from structure to biosynthesis. Biochimie 85, 153-166.
47. Nomiyama, H., Hieshima, K., Osada, N., Kato-Unoki, Y., Otsuka-Ono, K., Takegawa, S., Izawa, T., Yoshizawa, A., Kikuchi, Y., Tanase, S., Miura, R., Kusuda, J., Nakao, M. & Yoshie, O. (2008). Extensive expansion and diversification of the chemokine gene family in zebrafish: identification of a novel chemokine subfamily CX. BMC Genomics 9, 222.
48. Palić, D., Andreasen, C. B., Menzel, B. W. & Roth, J. A. (2005a). A rapid, direct assay to measure degranulation of primary granules in neutrophils from kidney of fathead minnow (Pimephales promelas Rafinesque, 1820). Fish & Shellfish Immunology 19, 217-227.
49. Palić, D., Andreasen, C. B., Frank, D. E., Menzel, B. W. & Roth, J. A. (2005b). Gradient separation and cytochemical characterisation of neutrophils from kidney of fathead minnow (Pimephales promelas Rafinesque, 1820). Fish & Shellfish Immunology 18, 263-267.
50. Palić, D., Herolt, D. M., Andreasen, C. B., Menzel, B. W. & Roth, J. A. (2006a). Anesthetic efficacy of tricaine methanesulfonate, metomidate and eugenol: effects on plasma cortisol concentration and neutrophil function in fathead minnows (Pimephales promelas Rafinesque, 1820). Aquaculture 254, 675-685.
51. Palić, D., Andreasen, C. B., Herolt, D. M., Menzel, B. W. & Roth, J. A. (2006b). Immunomodulatory effects of β-glucan on neutrophil function in fathead minnows (Pimephales promelas Rafinesque, 1820). Developmental & Comparative Immunology 30, 817-830.
52. Palić, D., Ostojic, J., Andreasen, C. B. & Roth, J. A. (2007a). Fish cast NETs: neutrophil extracellular traps are released from fish neutrophils. Developmental & Comparative Immunology 31, 805-816.
53. Palić, D., Andreasen, C. B., Ostojić, J., Tell, R. M. & Roth, J. A. (2007b). Zebrafish (Danio rerio) whole kidney assays to measure neutrophil extracellular trap release and degranulation of primary granules. Journal of Immunological Methods 319, 87-97.
54. Papayannopoulos, V. & Zychlinsky, A. (2009). NETs: a new strategy for using old weapons. Trends in Immunology 30, 513-521.
55. Pease, J. E. & Williams, T. J. (2006). Chemokines and their receptors in allergic disease. Journal of Allergy and Clinical Immunology 118, 305-318.
56. Roberts, S., Goetz, G., White, S. & Goetz, F. (2009). Analysis of genes isolated from plated hemocytes of the Pacific oyster, Crassostrea gigas. Marine Biotechnology 11, 24-44.
57. Robertsen, B. (2006). The interferon system of teleost fish. Fish & Shellfish Immunology 20, 172-191.
58. Segal, A. W. (2005). How neutrophils kill microbes. Annual Review of Immunology 23, 197-223.
59. Shi, Y., Zhao, Z., Yin, J.-K., Zhu, X.-P., Chen, K.-C., Pan, D.-B. & Gui, J.-F. (2010). Interferon regulatory factor-2 in orange-spotted grouper (Epinephelus coioides): gene, inductive expression pattern and subcellular localization. Comparative Biochemistry and Physiology B 155, 110-117.
60. Sun, B., Chang, M., Chen, D. & Nie, P. (2006). Gene structure and transcription of IRF-2 in the mandarin fish Siniperca chuatsi with the finding of alternative transcripts and microsatellite in the coding region. Immunogenetics 58, 774-784.
61. Tamassia, N., Le Moigne, V., Rossato, M., Donini, M., McCartney, S., Calzetti, F., Colonna, M., Bazzoni, F. & Cassatella, M. A. (2008). Activation of an immunoregulatory and antiviral gene expression program in poly(I:C)-transfected human neutrophils. Journal of Immunology 181, 6563-6573.
62. Taniguchi, T., Ogasawara, K., Takaoka, A. & Tanaka, N. (2001). IRF family of transcription factors as regulators of host defence. Annual Review of Immunology 19, 623-655.
63. Tian, C., Chen, Y., Ao, J. & Chen, X. (2010). Molecular characterization and bioactivity of a CXCL13 chemokine in large yellow croaker Pseudosciaena crocea. Fish & Shellfish Immunology 28, 445-452.
64. Triantafilou, M. & Triantafilou, K. (2005). The dynamics of LPS recognition: complex orchestration of multiple receptors. Journal of Endotoxin Research 11, 5-11.
65. USEPA (1987). Guidelines for the Culture of Fathead Minnows Pimephales promelas for use in Toxicity Tests. Duluth, MN: USEPA.
66. Villeneuve, D. L., Knoebl, I., Larkin, P., Miracle, A. L., Carter, B. J., Denslow, N. D. & Ankley, G. T. (2008). Altered gene expression in the brain and liver of female fathead minnows Pimephales promelas Rafinesque exposed to fadrozole. Journal of Fish Biology 72, 2281-2340.
67. Yost, C. C., Cody, M. J., Harris, E. S., Thornton, N. L., McInturff, A. M., Martinez, M. L., Chandler, N. B., Rodesch, C. K., Albertine, K. H., Petti, C. A., Weyrich, A. S. & Zimmerman, G. A. (2009). Impaired neutrophil extracellular trap (NET) formation: a novel innate immune deficiency of human neonates. Blood 113, 6419-6427.
68. Yu, S., Chen, X. & Ao, J. (2009). Molecular characterization and expression analysis of β-microglobulin in large yellow croaker Pseudosciaena crocea. Molecular Biology Reports 36, 1715-1723.
69. Zhang, Y.-B. & Gui, J.-F. (2004a). Identification and expression analysis of two IFN-inducible genes in crucian carp (Carassius auratus L.). Gene 325, 43-51.
70. Zhang, Y.-B. & Gui, J.-F. (2004b). Molecular characterization and IFN signal pathway analysis of Carassius auratus CaSTAT1 identified from the cultured cells in response to virus infection. Developmental & Comparative Immunology 28, 211-227.
71. Zhao, S. & Fernald, R. D. (2005). Comprehensive algorithm for quantitative real-time polymerase chain reaction. Journal of Computational Biology 12, 1047-1064.