Transcriptome analysis of Traf6 function in the innate immune response of zebrafish embryos

Molecular Immunology

Volumn 48, Issue 1-3, 2010, Pages 179-190

  Stockhammer, Oliver W ^a   Rauwerda, Han ^b   Wittink, Floyd R ^b   Breit, Timo M ^b   Meijer, Annemarie H ^a   Spaink, Herman P ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Bacterial infection; Gene regulation; Microarray; RNAseq; Signal transduction; Toll like receptors

Indexed keywords

TRANSCRIPTOME; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIMICROBIAL ACTIVITY; ARTICLE; AUTOPHAGY; CONTROLLED STUDY; DNA DAMAGE; EMBRYO; GENE IDENTIFICATION; GENE SEQUENCE; GENE SILENCING; IMMUNE RESPONSE; IN VIVO CULTURE; INNATE IMMUNITY; MICROARRAY ANALYSIS; NONHUMAN; PRIORITY JOURNAL; SALMONELLA; SALMONELLA TYPHIMURIUM; TRANSLATION REGULATION; ZEBRA FISH;

ANIMALS; EMBRYO, NONMAMMALIAN; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; IMMUNITY, INNATE; IN SITU HYBRIDIZATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; TNF RECEPTOR-ASSOCIATED FACTOR 6; ZEBRAFISH; ZEBRAFISH PROTEINS;

BACTERIA (MICROORGANISMS); DANIO RERIO; MUS; SALMONELLA;

EID: 78649518544     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2010.08.011     Document Type: Article

References (67)

1. Abbott D.W., Yang Y., Hutti J.E., Madhavarapu S., Kelliher M.A., Cantley L.C. Coordinated regulation of Toll-like receptor and NOD2 signaling by K63-linked polyubiquitin chains. Mol. Cell. Biol. 2007, 27:6012-6025.
2. Ahmad R., Sylvester J., Zafarullah M. MyD88, IRAK1 and TRAF6 knockdown in human chondrocytes inhibits interleukin-1-induced matrix metalloproteinase-13 gene expression and promoter activity by impairing MAP kinase activation. Cell. Signal. 2007, 19:2549-2557.
3. Asmann Y.W., Wallace M.B., Thompson E.A. Transcriptome profiling using next-generation sequencing. Gastroenterology 2008, 135:1466-1468.
4. Beisvag V., Junge F.K., Bergum H., Jolsum L., Lydersen S., Gunther C.C., Ramampiaro H., Langaas M., Sandvik A.K., Laegreid A. GeneTools - application for functional annotation and statistical hypothesis testing. BMC Bioinformatics 2006, 7:470.
5. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 1995, 57:289-300.
6. Cao Z., Xiong J., Takeuchi M., Kurama T., Goeddel D.V. TRAF6 is a signal transducer for interleukin-1. Nature 1996, 383:443-446.
7. Chakraborty A., Brooks H., Zhang P., Smith W., McReynolds M.R., Hoying J.B., Bick R., Truong L., Poindexter B., Lan H., Elbjeirami W., Sheikh-Hamad D. Stanniocalcin-1 regulates endothelial gene expression and modulates transendothelial migration of leukocytes. Am. J. Physiol. Renal Physiol. 2007, 292:F895-F904.
8. Chen H.F., Jeung E.B., Stephenson M., Leung P.C. Human peripheral blood mononuclear cells express gonadotropin-releasing hormone (GnRH), GnRH receptor, and interleukin-2 receptor gamma-chain messenger ribonucleic acids that are regulated by GnRH in vitro. J. Clin. Endocrinol. Metab. 1999, 84:743-750.
9. Crighton D., Wilkinson S., O'Prey J., Syed N., Smith P., Harrison P.R., Gasco M., Garrone O., Crook T., Ryan K.M. DRAM, a p53-induced modulator of autophagy, is critical for apoptosis. Cell 2006, 126:121-134.
10. Dahlquist K.D., Salomonis N., Vranizan K., Lawlor S.C., Conklin B.R. GenMAPP, a new tool for viewing and analyzing microarray data on biological pathways. Nat. Genet. 2002, 31:19-20.
11. Darnay B.G., Ni J., Moore P.A., Aggarwal B.B. Activation of NF-kappaB by RANK requires tumor necrosis factor receptor-associated factor (TRAF) 6 and NF-kappaB-inducing kinase. Identification of a novel TRAF6 interaction motif. J. Biol. Chem. 1999, 274:7724-7731.
12. Davidson A.J., Zon L.I. The 'definitive' (and 'primitive') guide to zebrafish hematopoiesis. Oncogene 2004, 23:7233-7246.
13. 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.
14. Deng L., Wang C., Spencer E., Yang L., Braun A., You J., Slaughter C., Pickart C., Chen Z.J. Activation of the IkappaB kinase complex by TRAF6 requires a dimeric ubiquitin-conjugating enzyme complex and a unique polyubiquitin chain. Cell 2000, 103:351-361.
15. Galibert L., Tometsko M.E., Anderson D.M., Cosman D., Dougall W.C. The involvement of multiple tumor necrosis factor receptor (TNFR)-associated factors in the signaling mechanisms of receptor activator of NF-kappaB, a member of the TNFR superfamily. J. Biol. Chem. 1998, 273:34120-34127.
16. Hall C., Flores M.V., Crosier K., Crosier P. Live cell imaging of zebrafish leukocytes. Methods Mol. Biol. 2009, 546:255-271.
17. Hegedus Z., Zakrzewska A., Agoston V.C., Ordas A., Racz P., Mink M., Spaink H.P., Meijer A.H. Deep sequencing of the zebrafish transcriptome response to mycobacterium infection. Mol. Immunol. 2009, 46:2918-2930.
18. Herbomel P., Thisse B., Thisse C. Ontogeny and behaviour of early macrophages in the zebrafish embryo. Development 1999, 126:3735-3745.
19. Herbomel P., Thisse B., Thisse C. Zebrafish early macrophages colonize cephalic mesenchyme and developing brain, retina, and epidermis through a M-CSF receptor-dependent invasive process. Dev. Biol. 2001, 238:274-288.
20. Ishida T., Mizushima S., Azuma S., Kobayashi N., Tojo T., Suzuki K., Aizawa S., Watanabe T., Mosialos G., Kieff E., Yamamoto T., Inoue J. Identification of TRAF6, a novel tumor necrosis factor receptor-associated factor protein that mediates signaling from an amino-terminal domain of the CD40 cytoplasmic region. J. Biol. Chem. 1996, 271:28745-28748.
21. Kanayama A., Seth R.B., Sun L., Ea C.K., Hong M., Shaito A., Chiu Y.H., Deng L., Chen Z.J. TAB2 and TAB3 activate the NF-kappaB pathway through binding to polyubiquitin chains. Mol. Cell 2004, 15:535-548.
22. Kawai T., Akira S. TLR signaling. Semin. Immunol. 2007, 19:24-32.
23. Kerr M.K., Martin M., Churchill G.A. Analysis of variance for gene expression microarray data. J. Comput. Biol. 2000, 7:819-837.
24. Kobayashi T., Walsh M.C., Choi Y. The role of TRAF6 in signal transduction and the immune response. Microbes Infect. 2004, 6:1333-1338.
25. Kobayashi T., Walsh P.T., Walsh M.C., Speirs K.M., Chiffoleau E., King C.G., Hancock W.W., Caamano J.H., Hunter C.A., Scott P., Turka L.A., Choi Y. TRAF6 is a critical factor for dendritic cell maturation and development. Immunity 2003, 19:353-363.
26. Koening C.L., Miller J.C., Nelson J.M., Ward D.M., Kushner J.P., Bockenstedt L.K., Weis J.J., Kaplan J., De Domenico I. Toll-like receptors mediate induction of hepcidin in mice infected with Borrelia burgdorferi. Blood 2009, 114:1913-1918.
27. Kumar D., Nath L., Kamal M.A., Varshney A., Jain A., Singh S., Rao K.V. Genome-wide analysis of the host intracellular network that regulates survival of Mycobacterium tuberculosis. Cell 2010, 140:731-743.
28. Lam S.H., Chua H.L., Gong Z., Lam T.J., Sin Y.M. Development and maturation of the immune system in zebrafish, Danio rerio: a gene expression profiling, in situ hybridization and immunological study. Dev. Comp. Immunol. 2004, 28:9-28.
29. Lesley R., Ramakrishnan L. Insights into early mycobacterial pathogenesis from the zebrafish. Curr. Opin. Microbiol. 2008, 11:277-283.
30. Lomaga M.A., Yeh W.C., Sarosi I., Duncan G.S., Furlonger C., Ho A., Morony S., Capparelli C., Van G., Kaufman S., van der Heiden A., Itie A., Wakeham A., Khoo W., Sasaki T., Cao Z., Penninger J.M., Paige C.J., Lacey D.L., Dunstan C.R., Boyle W.J., Goeddel D.V., Mak T.W. TRAF6 deficiency results in osteopetrosis and defective interleukin-1, CD40, and LPS signaling. Genes Dev. 1999, 13:1015-1024.
31. Mathias J.R., Perrin B.J., Liu T.X., Kanki J., Look A.T., Huttenlocher A. Resolution of inflammation by retrograde chemotaxis of neutrophils in transgenic zebrafish. J. Leukoc. Biol. 2006, 80:1281-1288.
32. Meeker N.D., Trede N.S. Immunology and zebrafish: spawning new models of human disease. Dev. Comp. Immunol. 2008, 32:745-757.
33. Meijer A.H., Gabby Krens S.F., Medina Rodriguez I.A., He S., Bitter W., Ewa Snaar-Jagalska B., Spaink H.P. Expression analysis of the Toll-like receptor and TIR domain adaptor families of zebrafish. Mol. Immunol. 2004, 40:773-783.
34. 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.
35. Min J.Y., Park M.H., Lee J.K., Kim H.J., Park Y.K. Gonadotropin-releasing hormone modulates immune system function via the nuclear factor-kappaB pathway in murine Raw264.7 macrophages. Neuroimmunomodulation 2009, 16:177-184.
36. Mogensen T.H. Pathogen recognition and inflammatory signaling in innate immune defenses. Clin. Microbiol. Rev. 2009, 22:240-273. (Table of Contents).
37. Mortazavi A., Williams B.A., McCue K., Schaeffer L., Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 2008, 5:621-628.
38. Munz C. Enhancing immunity through autophagy. Annu. Rev. Immunol. 2009, 27:423-449.
39. Murayama E., Kissa K., Zapata A., Mordelet E., Briolat V., Lin H.F., Handin R.I., Herbomel P. Tracing hematopoietic precursor migration to successive hematopoietic organs during zebrafish development. Immunity 2006, 25:963-975.
40. Muzio M., Natoli G., Saccani S., Levrero M., Mantovani A. The human toll signaling pathway: divergence of nuclear factor kappaB and JNK/SAPK activation upstream of tumor necrosis factor receptor-associated factor 6 (TRAF6). J. Exp. Med. 1998, 187:2097-2101.
41. Naito A., Azuma S., Tanaka S., Miyazaki T., Takaki S., Takatsu K., Nakao K., Nakamura K., Katsuki M., Yamamoto T., Inoue J. Severe osteopetrosis, defective interleukin-1 signalling and lymph node organogenesis in TRAF6-deficient mice. Genes Cells 1999, 4:353-362.
42. O'Prey J., Skommer J., Wilkinson S., Ryan K.M. Analysis of DRAM-related proteins reveals evolutionarily conserved and divergent roles in the control of autophagy. Cell Cycle 2009, 8:2260-2265.
43. Pearce E.L., Walsh M.C., Cejas P.J., Harms G.M., Shen H., Wang L.S., Jones R.G., Choi Y. Enhancing CD8 T-cell memory by modulating fatty acid metabolism. Nature 2009, 460:103-107.
44. Phelps H.A., Neely M.N. Evolution of the zebrafish model: from development to immunity and infectious disease. Zebrafish 2005, 2:87-103.
45. Redd M.J., Kelly G., Dunn G., Way M., Martin P. Imaging macrophage chemotaxis in vivo: studies of microtubule function in zebrafish wound inflammation. Cell Motil. Cytoskeleton 2006, 63:415-422.
46. Renshaw S.A., Loynes C.A., Trushell D.M., Elworthy S., Ingham P.W., Whyte M.K. A transgenic zebrafish model of neutrophilic inflammation. Blood 2006, 108:3976-3978.
47. Solis M., Wilkinson P., Romieu R., Hernandez E., Wainberg M.A., Hiscott J. Gene expression profiling of the host response to HIV-1 B, C, or A/E infection in monocyte-derived dendritic cells. Virology 2006, 352:86-99.
48. Sorrentino A., Thakur N., Grimsby S., Marcusson A., von Bulow V., Schuster N., Zhang S., Heldin C.H., Landstrom M. The type I TGF-beta receptor engages TRAF6 to activate TAK1 in a receptor kinase-independent manner. Nat. Cell Biol. 2008, 10:1199-1207.
49. Stein C., Caccamo M., Laird G., Leptin M. Conservation and divergence of gene families encoding components of innate immune response systems in zebrafish. Genome Biol. 2007, 8:R251.
50. Stockhammer O.W., Zakrzewska A., Hegedus Z., Spaink H.P., Meijer A.H. Transcriptome profiling and functional analyses of the zebrafish embryonic innate immune response to Salmonella infection. J. Immunol. 2009, 182:5641-5653.
51. Sundaram K., Nishimura R., Senn J., Youssef R.F., London S.D., Reddy S.V. RANK ligand signaling modulates the matrix metalloproteinase-9 gene expression during osteoclast differentiation. Exp. Cell Res. 2007, 313:168-178.
52. Tanriverdi F., Silveira L.F., MacColl G.S., Bouloux P.M. The hypothalamic-pituitary-gonadal axis: immune function and autoimmunity. J. Endocrinol. 2003, 176:293-304.
53. Tsukamoto N., Kobayashi N., Azuma S., Yamamoto T., Inoue J. Two differently regulated nuclear factor kappaB activation pathways triggered by the cytoplasmic tail of CD40. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:1234-1239.
54. van der Sar A.M., Musters R.J., van Eeden F.J., Appelmelk B.J., Vandenbroucke-Grauls C.M., Bitter W. Zebrafish embryos as a model host for the real time analysis of Salmonella typhimurium infections. Cell. Microbiol. 2003, 5:601-611.
55. Van der Sar A.M., Stockhammer O.W., van der Laan C., Spaink H.P., Bitter W., Meijer A.H. MyD88 innate immune function in a zebrafish embryo infection model. Infect. Immun. 2006, 74:2436-2441.
56. 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.
57. Wang C., Deng L., Hong M., Akkaraju G.R., Inoue J., Chen Z.J. TAK1 is a ubiquitin-dependent kinase of MKK and IKK. Nature 2001, 412:346-351.
58. Ward A.C., McPhee D.O., Condron M.M., Varma S., Cody S.H., Onnebo S.M., Paw B.H., Zon L.I., Lieschke G.J. The zebrafish spi1 promoter drives myeloid-specific expression in stable transgenic fish. Blood 2003, 102:3238-3240.
59. Wellen K.E., Fucho R., Gregor M.F., Furuhashi M., Morgan C., Lindstad T., Vaillancourt E., Gorgun C.Z., Saatcioglu F., Hotamisligil G.S. Coordinated regulation of nutrient and inflammatory responses by STAMP2 is essential for metabolic homeostasis. Cell 2007, 129:537-548.
60. Willett C.E., Cortes A., Zuasti A., Zapata A.G. Early hematopoiesis and developing lymphoid organs in the zebrafish. Dev. Dyn. 1999, 214:323-336.
61. Witten P.E., Hansen A., Hall B.K. Features of mono- and multinucleated bone resorbing cells of the zebrafish Danio rerio and their contribution to skeletal development, remodeling, and growth. J. Morphol. 2001, 250:197-207.
62. Wong B.R., Josien R., Lee S.Y., Vologodskaia M., Steinman R.M., Choi Y. The TRAF family of signal transducers mediates NF-kappaB activation by the TRANCE receptor. J. Biol. Chem. 1998, 273:28355-28359.
63. Wu H., Kerr K., Cui X., Churchill G.A. MAANOVA: a software package for the analysis of spotted cDNA microarray experiments. The analysis of gene expression data: methods and software 2003, 313-341. Springer, Heidelberg. G. Parmigiani, E.S. Garett, R.A. Irizarry (Eds.).
64. Wu S., Page L., Sherwood N.M. A role for GnRH in early brain regionalization and eye development in zebrafish. Mol. Cell. Endocrinol. 2006, 257-258:47-64.
65. Xiao C., Shim J.H., Kluppel M., Zhang S.S., Dong C., Flavell R.A., Fu X.Y., Wrana J.L., Hogan B.L., Ghosh S. Ecsit is required for Bmp signaling and mesoderm formation during mouse embryogenesis. Genes Dev. 2003, 17:2933-2949.
66. Yamashita M., Fatyol K., Jin C., Wang X., Liu Z., Zhang Y.E. TRAF6 mediates Smad-independent activation of JNK and p38 by TGF-beta. Mol. Cell 2008, 31:918-924.
67. Yoshiko Y., Maeda N., Aubin J.E. Stanniocalcin 1 stimulates osteoblast differentiation in rat calvaria cell cultures. Endocrinology 2003, 144:4134-4143.