Origin and evolution of TNF and TNF receptor superfamilies

Developmental and Comparative Immunology

Volumn 35, Issue 12, 2011, Pages 1324-1335

  Wiens, Gregory D ^a   Glenney, Gavin W ^b  

^a NATIONAL CENTER FOR COOL AND COLD WATER AQUACULTURE   (United States)

^b Northeast Fishery Center   (United States)

Author keywords

Evolution; Genome duplication; Teleost; Tumor necrosis factor superfamily

Indexed keywords

TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RECEPTOR; TUMOR NECROSIS FACTOR RECEPTOR 1;

AMPHIBIA; ARTHROPOD; ARTICLE; BIOINFORMATICS; BIRD; CELL LINEAGE; EXPRESSED SEQUENCE TAG; FISH GENETICS; GENE DOSAGE; GENE DUPLICATION; GENE TRANSLOCATION; GENETIC ANALYSIS; HUMAN; INVERTEBRATE; LIGAND BINDING; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE; TANDEM REPEAT; TUMOR NECROSIS FACTOR RECEPTOR SUPERFAMILY GENE; TUMOR NECROSIS FACTOR SUPERFAMILY GENE; UNINDEXED SEQUENCE; VERTEBRATE; ZEBRA FISH;

ANIMALIA; ARTHROPODA; DANIO RERIO; INVERTEBRATA; TELEOSTEI; VERTEBRATA;

EID: 80054924745     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2011.03.031     Document Type: Article

References (99)

1. Bates J.M., Akerlund J., Mittge E., Guillemin K. Intestinal alkaline phosphatase detoxifies lipopolysaccharide and prevents inflammation in zebrafish in response to the gut microbiota. Cell Host Microbe 2007, 2(6):371-382.
2. Bishop G.R., Taylor S., Jaso-Friedmann L., Evans D.L. Mechanisms of nonspecific cytotoxic cell regulation of apoptosis: cytokine-like activity of Fas ligand. Fish Shellfish Immunol. 2002, 13(1):47-67.
3. Bobe J., Goetz F.W. Molecular cloning and expression of a TNF receptor and two TNF ligands in the fish ovary. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2001, 129(2-3):475-481.
4. Bodmer J.L., Schneider P., Tschopp J. The molecular architecture of the TNF superfamily. Trends Biochem. Sci. 2002, 27(1):19-26.
5. Bossen C., Ingold K., Tardivel A., Bodmer J.L., Gaide O., Hertig S., et al. Interactions of tumor necrosis factor (TNF) and TNF receptor family members in the mouse and human. J. Biol. Chem. 2006, 281(20):13964-13971.
6. Bossen C., Cachero T.G., Tardivel A., Ingold K., Willen L., Dobles M., et al. TACI, unlike BAFF-R, is solely activated by oligomeric BAFF and APRIL to support survival of activated B cells and plasmablasts. Blood 2008, 111(3):1004-1012.
7. Brandt S.M., Dionne M.S., Khush R.S., Pham L.N., Vigdal T.J., Schneider D.S. Secreted bacterial effectors and host-produced eiger/TNF drive death in a Salmonella-infected fruit fly. PLoS Biol. 2004, 2(12):e418.
8. Bridgham J.T., Wilder J.A., Hollocher H., Johnson A.L. All in the family: evolutionary and functional relationships among death receptors. Cell Death Differ. 2003, 10(1):19-25.
9. Chang M.X., Nie P., Xie H.X., Wang G.L., Gao Y. Characterization and expression analysis of TNF-related apoptosis inducing ligand (TRAIL) in grass carp Ctenopharyngodon idella. Vet. Immunol. Immunopathol. 2006, 110(1-2):51-63.
10. Chattopadhyay K., Ramagopal U.A., Brenowitz M., Nathenson S.G., Almo S.C. Evolution of GITRL immune function: murine GITRL exhibits unique structural and biochemical properties within the TNF superfamily. Proc. Natl. Acad. Sci. U.S.A. 2008, 105(2):635-640.
11. 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(2):283-294.
12. Collette Y., Gilles A., Pontarotti P., Olive D. A co-evolution perspective of the TNFSF and TNFRSF families in the immune system. Trends Immunol. 2003, 24(7):387-394.
13. Colosimo P.F., Hosemann K.E., Balabhadra S., Villarreal G., Dickson M., Grimwood J., et al. Widespread parallel evolution in sticklebacks by repeated fixation of Ectodysplasin alleles. Science 2005, 307(5717):1928-1933.
14. Cosma C.L., Swaim L.E., Volkman H., Ramakrishnan L., Davis J.M. Zebrafish and frog models of Mycobacterium marinum infection. Curr. Protoc. Microbiol. 2006, Chapter 10Unit 10B 2.
15. Covello J.M., Bird S., Morrison R.N., Battaglene S.C., Secombes C.J., Nowak B.F. Cloning and expression analysis of three striped trumpeter (Latris lineata) pro-inflammatory cytokines, TNF-alpha, IL-1beta and IL-8, in response to infection by the ectoparasitic, Chondracanthus goldsmidi. Fish Shellfish Immunol. 2009, 26(5):773-786.
16. Crespo D., Bonnet E., Roher N., MacKenzie S.A., Krasnov A., Goetz F.W., et al. Cellular and molecular evidence for a role of tumor necrosis factor alpha in the ovulatory mechanism of trout. Reprod. Biol. Endocrinol. 2010, 834.
17. Dalloul R.A., Long J.A., Zimin A.V., Aslam L., Beal K., Ann Blomberg L., et al. Multi-platform next-generation sequencing of the domestic turkey (Meleagris gallopavo): genome assembly and analysis. PLoS Biol. 2010, 8.(9).
18. Danzmann R.G., Davidson E.A., Ferguson M.M., Gharbi K., Koop B.F., Hoyheim B., et al. Distribution of ancestral proto-Actinopterygian chromosome arms within the genomes of 4R-derivative salmonid fishes (Rainbow trout and Atlantic salmon). BMC Genom. 2008, 9557.
19. De Zoysa M., Jung S., Lee J. First molluscan TNF-alpha homologue of the TNF superfamily in disk abalone: molecular characterization and expression analysis. Fish Shellfish Immunol. 2009, 26(4):625-631.
20. De Zoysa M., Nikapitiya C., Moon D.O., Whang I., Kim G.Y., Lee J. A novel Fas ligand in mollusk abalone: molecular characterization, immune responses and biological activity of the recombinant protein. Fish Shellfish Immunol. 2009, 27(3):423-432.
21. Degli-Esposti M. To die or not to die - the quest of the TRAIL receptors. J. Leukoc. Biol. 1999, 65(5):535-542.
22. Eimon P.M., Ashkenazi A. The zebrafish as a model organism for the study of apoptosis. Apoptosis 2010, 15(3):331-349.
23. Eimon P.M., Kratz E., Varfolomeev E., Hymowitz S.G., Stern H., Zha J., et al. Delineation of the cell-extrinsic apoptosis pathway in the zebrafish. Cell Death Differ. 2006, 13(10):1619-1630.
24. Flajnik M.F., Kasahara M. Origin and evolution of the adaptive immune system: genetic events and selective pressures. Nat. Rev. Genet. 2010, 11(1):47-59.
25. Flynn J.L., Goldstein M.M., Chan J., Triebold K.J., Pfeffer K., Lowenstein C.J., et al. Tumor necrosis factor-alpha is required in the protective immune response against Mycobacterium tuberculosis in mice. Immunity 1995, 2(6):561-572.
26. Forlenza M., Magez S., Scharsack J.P., Westphal A., Savelkoul H.F., Wiegertjes G.F. Receptor-mediated and lectin-like activities of carp (Cyprinus carpio) TNF-alpha. J. Immunol. 2009, 183(8):5319-5332.
27. Garcia-Castillo J., Pelegrin P., Mulero V., Meseguer J. Molecular cloning and expression analysis of tumor necrosis factor alpha from a marine fish reveal its constitutive expression and ubiquitous nature. Immunogenetics 2002, 54(3):200-207.
28. Glenney G.W., Wiens G.D. Early diversification of the TNF superfamily in teleosts: genomic characterization and expression analysis. J. Immunol. 2007, 178(12):7955-7973.
29. Goetz F.W., Planas J.V., MacKenzie S. Tumor necrosis factors. Dev. Comp. Immunol. 2004, 28(5):487-497.
30. Gong Y.F., Xiang L.X., Shao J.Z. CD154-CD40 interactions are essential for thymus-dependent antibody production in zebrafish: insights into the origin of costimulatory pathway in helper T cell-regulated adaptive immunity in early vertebrates. J. Immunol. 2009, 182(12):7749-7762.
31. Grayfer L., Belosevic M. Molecular characterization of tumor necrosis factor receptors 1 and 2 of the goldfish (Carassius aurutus L.). Mol. Immunol. 2009, 46(11-12):2190-2199.
32. 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(5):532-543.
33. Harris M.P., Rohner N., Schwarz H., Perathoner S., Konstantinidis P., Nusslein-Volhard C. Zebrafish eda and edar mutants reveal conserved and ancestral roles of ectodysplasin signaling in vertebrates. PLoS Genet. 2008, 4(10):e1000206.
34. Haugland O., Mercy I.S., Romoren K., Torgersen J., Evensen O. Differential expression profiles and gene structure of two tumor necrosis factor-alpha variants in Atlantic salmon (Salmo salar L.). Mol. Immunol. 2007, 44(7):1652-1663.
35. Hedges S.B., Dudley J., Kumar S., TimeTree: a public knowledge-base of divergence times among organisms. Bioinformatics 2006, 22(23):2971-2972.
36. Hibino T., Loza-Coll M., Messier C., Majeske A.J., Cohen A.H., Terwilliger D.P., et al. The immune gene repertoire encoded in the purple sea urchin genome. Dev. Biol. 2006, 300(1):349-365.
37. Hino K., Nakamura O., Yoshiura Y., Suetake H., Suzuki Y., Watanabe T. TNF induces the growth of thymocytes in rainbow trout. Dev. Comp. Immunol. 2006, 30(7):639-647.
38. Hirono I., Nam B.H., Kurobe T., Aoki T. Molecular cloning, characterization, and expression of TNF cDNA and gene from Japanese flounder Paralychthys olivaceus. J. Immunol. 2000, 165(8):4423-4427.
39. Igaki T., Kanda H., Yamamoto-Goto Y., Kanuka H., Kuranaga E., Aigaki T., et al. Eiger, a TNF superfamily ligand that triggers the Drosophila JNK pathway. EMBO J. 2002, 21(12):3009-3018.
40. Kadowaki T., Harada H., Sawada Y., Kohchi C., Soma G., Takahashi Y., et al. Two types of tumor necrosis factor-alpha in bluefin tuna (Thunnus orientalis) genes: molecular cloning and expression profile in response to several immunological stimulants. Fish Shellfish Immunol. 2009, 27(5):585-594.
41. Kaiser P., Poh T.Y., Rothwell L., Avery S., Balu S., Pathania U.S., et al. A genomic analysis of chicken cytokines and chemokines. J. Interferon Cytokine Res. 2005, 25(8):467-484.
42. Kanda H., Igaki T., Kanuka H., Yagi T., Miura M. Wengen, a member of the Drosophila tumor necrosis factor receptor superfamily, is required for Eiger signaling. J. Biol. Chem. 2002, 277(32):28372-28375.
43. Kanther M., Rawls J.F. Host-microbe interactions in the developing zebrafish. Curr. Opin. Immunol. 2010, 22(1):10-19.
44. Kasahara M. Genome duplication and T cell immunity. Prog. Mol. Biol. Transl. Sci. 2010, 927-936.
45. Kauppila S., Maaty W.S., Chen P., Tomar R.S., Eby M.T., Chapo J., et al. Eiger and its receptor, Wengen, comprise a TNF-like system in Drosophila. Oncogene 2003, 22(31):4860-4867.
46. Keane J., Gershon S., Wise R.P., Mirabile-Levens E., Kasznica J., Schwieterman W.D., et al. Tuberculosis associated with infliximab, a tumor necrosis factor alpha-neutralizing agent. N. Engl. J. Med. 2001, 345(15):1098-1104.
47. Kono T., Zou J., Bird S., Savan R., Sakai M., Secombes C.J. Identification and expression analysis of lymphotoxin-beta like homologues in rainbow trout Oncorhynchus mykiss. Mol. Immunol. 2006, 43(9):1390-1401.
48. Kuraku S., Meyer A. The evolution and maintenance of Hox gene clusters in vertebrates and the teleost-specific genome duplication. Int. J. Dev. Biol. 2009, 53(5-6):765-773.
49. Kurobe T., Hirono I., Kondo H., Saito-Taki T., Aoki T. Molecular cloning, characterization, expression and functional analysis of Japanese flounder Paralichthys olivaceus Fas ligand. Dev. Comp. Immunol. 2007, 10.1016/j.dci.2006.08.006.
50. Kwan T.T., Liang R., Verfaillie C.M., Ekker S.C., Chan L.C., Lin S., et al. Regulation of primitive hematopoiesis in zebrafish embryos by the death receptor gene. Exp. Hematol. 2006, 34(1):27-34.
51. Laing K.J., Wang T., Zou J., Holland J., Hong S., Bols N., et al. Cloning and expression analysis of rainbow trout Oncorhynchus mykiss tumour necrosis factor-alpha. Eur. J. Biochem. 2001, 268(5):1315-1322.
52. Laurikkala J., Pispa J., Jung H.S., Nieminen P., Mikkola M., Wang X., et al. Regulation of hair follicle development by the TNF signal ectodysplasin and its receptor Edar. Development 2002, 129(10):2541-2553.
53. Letunic I., Doerks T., Bork P. SMART6: recent updates and new developments. Nucleic Acids Res. 2009, 37(Database issue):D229-D232.
54. Li L., Qiu L., Song L., Song X., Zhao J., Wang L., et al. First molluscan TNFR homologue in Zhikong scallop: molecular characterization and expression analysis. Fish Shellfish Immunol. 2009, 27(5):625-632.
55. Liang Z., Kong Y., Luo C., Shen Y., Zhang S. Molecular cloning, functional characterization and phylogenetic analysis of B-cell activating factor in zebrafish (Danio rerio). Fish Shellfish Immunol. 2010, 29(2):233-240.
56. Locksley R.M., Killeen N., Lenardo M.J. The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell 2001, 104(4):487-501.
57. Long Q., Huang H., Shafizadeh E., Liu N., Lin S. Stimulation of erythropoiesis by inhibiting a new hematopoietic death receptor in transgenic zebrafish. Nat. Cell Biol. 2000, 2(8):549-552.
58. Long S., Wilson M., Bengten E., Clem L.W., Miller N.W., Chinchar V.G. Identification and characterization of a FasL-like protein and cDNAs encoding the channel catfish death-inducing signaling complex. Immunogenetics 2004, 56(7):518-530.
59. Mawaribuchi S., Tamura K., Okano S., Takayama S., Yaoita Y., Shiba T., et al. Tumor necrosis factor-alpha attenuates thyroid hormone-induced apoptosis in vascular endothelial cell line XLgoo established from Xenopus tadpole tails. Endocrinology 2008, 149(7):3379-3389.
60. Mekata T., Sudhakaran R., Okugawa S., Inada M., Kono T., Sakai M., et al. A novel gene of tumor necrosis factor ligand superfamily from kuruma shrimp, Marsupenaeus japonicus. Fish Shellfish Immunol. 2010, 28(4):571-578.
61. Moghadam H.K., Ferguson M.M., Danzmann R.G. Evolution of Hox clusters in Salmonidae: a comparative analysis between Atlantic salmon (Salmo salar) and rainbow trout (Oncorhynchus mykiss). J. Mol. Evol. 2005, 61(5):636-649.
62. Moreno E., Yan M., Basler K. Evolution of TNF signaling mechanisms: JNK-dependent apoptosis triggered by Eiger, the Drosophila homolog of the TNF superfamily. Curr. Biol. 2002, 12(14):1263-1268.
63. Morrison R.N., Zou J., Secombes C.J., Scapigliati G., Adams M.B., Nowak B.F. Molecular cloning and expression analysis of tumour necrosis factor-alpha in amoebic gill disease (AGD)-affected Atlantic salmon (Salmo salar L.). Fish Shellfish Immunol. 2007, 23(5):1015-1031.
64. Narasimamurthy R., Geuking P., Ingold K., Willen L., Schneider P., Basler K. Structure-function analysis of Eiger, the Drosophila TNF homolog. Cell Res. 2009, 19(3):392-394.
65. Nascimento D.S., Pereira P.J., Reis M.I., do Vale A., Zou J., Silva M.T., et al. Molecular cloning and expression analysis of sea bass (Dicentrarchus labrax L.) tumor necrosis factor-alpha (TNF-alpha). Fish Shellfish Immunol. 2007, 23(3):701-710.
66. Nocentini G., Ronchetti S., Cuzzocrea S., Riccardi C. GITR/GITRL: more than an effector T cell co-stimulatory system. Eur. J. Immunol. 2007, 37(5):1165-1169.
67. Ohno S. Evolution by Gene Duplication 1970, Springer.
68. Ohta Y., Goetz W., Hossain M.Z., Nonaka M., Flajnik M.F. Ancestral organization of the MHC revealed in the amphibian Xenopus. J. Immunol. 2006, 176(6):3674-3685.
69. Ordas M.C., Costa M.M., Roca F.J., Lopez-Castejon G., Mulero V., Meseguer J., et al. Turbot TNFalpha gene: molecular characterization and biological activity of the recombinant protein. Mol. Immunol. 2007, 44(4):389-400.
70. Orlinick J.R., Chao M.V. TNF-related ligands and their receptors. Cell Signal. 1998, 10(8):543-551.
71. Pantalacci S., Chaumot A., Benoit G., Sadier A., Delsuc F., Douzery E.J., et al. Conserved features and evolutionary shifts of the EDA signaling pathway involved in vertebrate skin appendage development. Mol. Biol. Evol. 2008, 25(5):912-928.
72. Parrinello N., Vizzini A., Arizza V., Salerno G., Parrinello D., Cammarata M., et al. Enhanced expression of a cloned and sequenced Ciona intestinalis TNFalpha-like (CiTNF alpha) gene during the LPS-induced inflammatory response. Cell Tissue Res. 2008, 334(2):305-317.
73. Peterson K.J., Butterfield N.J. Origin of the Eumetazoa: testing ecological predictions of molecular clocks against the Proterozoic fossil record. Proc. Natl. Acad. Sci. U.S.A. 2005, 102(27):9547-9552.
74. Poulton L.D., Nolan K.F., Anastasaki C., Waldmann H., Patton E.E. A novel role for glucocorticoid-induced TNF receptor ligand (Gitrl) in early embryonic zebrafish development. Int. J. Dev. Biol. 2010, 54(5):815-825.
75. Rautenschlein S., Subramanian A., Sharma J.M. Bioactivities of a tumour necrosis-like factor released by chicken macrophages. Dev. Comp. Immunol. 1999, 23(7-8):629-640.
76. Robertson A.J., Croce J., Carbonneau S., Voronina E., Miranda E., McClay D.R., et al. The genomic underpinnings of apoptosis in Strongylocentrotus purpuratus. Dev. Biol. 2006, 300(1):321-334.
77. Roca F.J., Mulero I., Lopez-Munoz A., Sepulcre M.P., Renshaw S.A., Meseguer J., et al. Evolution of the inflammatory response in vertebrates: fish TNF-alpha is a powerful activator of endothelial cells but hardly activates phagocytes. J. Immunol. 2008, 181(7):5071-5081.
78. Saeij J.P., Stet R.J., de Vries B.J., van Muiswinkel W.B., Wiegertjes G.F. Molecular and functional characterization of carp TNF: a link between TNF polymorphism and trypanotolerance?. Dev. Comp. Immunol. 2003, 27(1):29-41.
79. Saera-Vila A., Calduch-Giner J.A., Navarro I., Perez-Sanchez J. Tumour necrosis factor (TNF)alpha as a regulator of fat tissue mass in the Mediterranean gilthead sea bream (Sparus aurata L.). Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2007, 146(3):338-345.
80. Sakamaki K., Nozaki M., Kominami K., Satou Y. The evolutionary conservation of the core components necessary for the extrinsic apoptotic signaling pathway, in Medaka fish. BMC Genom. 2007, 8141.
81. Savan R., Sakai M. Presence of multiple isoforms of TNF alpha in carp (Cyprinus carpio L.): genomic and expression analysis. Fish Shellfish Immunol. 2004, 17(1):87-94.
82. Savan R., Kono T., Igawa D., Sakai M. A novel tumor necrosis factor (TNF) gene present in tandem with theTNF-alpha gene on the same chromosome in teleosts. Immunogenetics 2005, 57(1-2):140-150.
83. Scientists GKCo Genome 10K: a proposal to obtain whole-genome sequence for 10,000 vertebrate species. J. Hered. 2009, 100(6):659-674.
84. Sedy J.R., Spear P.G., Ware C.F. Cross-regulation between herpesviruses and the TNF superfamily members. Nat. Rev. Immunol. 2008, 8(11):861-873.
85. Sharpe P.T. Fish scale development: hair today, teeth and scales yesterday?. Curr. Biol. 2001, 11(18):R751-R752.
86. Tamura K., Noyama T., Ishizawa Y.H., Takamatsu N., Shiba T., Ito M. Xenopus death receptor-M1 and -M2, new members of the tumor necrosis factor receptor superfamily, trigger apoptotic signaling by differential mechanisms. J. Biol. Chem. 2004, 279(9):7629-7635.
87. Tamura K., Mawaribuchi S., Yoshimoto S., Shiba T., Takamatsu N., Ito M. Tumor necrosis factor-related apoptosis-inducing ligand 1 (TRAIL1) enhances the transition of red blood cells from the larval to adult type during metamorphosis in Xenopus. Blood 2010, 115(4):850-859.
88. Tansey M.G., Szymkowski D.E. The TNF superfamily in 2009: new pathways, new indications, and new drugs. Drug Discov. Today 2009, 14(23-24):1082-1088.
89. Tobin D.M., Vary J.C., Ray J.P., Walsh G.S., Dunstan S.J., Bang N.D., et al. The lta4h locus modulates susceptibility to mycobacterial infection in zebrafish and humans. Cell 2010, 140(5):717-730.
90. Ware C.F. The TNF superfamily. Cytokine Growth Factor Rev. 2003, 14(3-4):181-184.
91. Woods I.G., Kelly P.D., Chu F., Ngo-Hazelett P., Yan Y.L., Huang H., et al. A comparative map of the zebrafish genome. Genome Res. 2000, 10(12):1903-1914.
92. Xiao J., Zhou Z.C., Chen C., Huo W.L., Yin Z.X., Weng S.P., et al. Tumor necrosis factor-alpha gene from mandarin fish, Siniperca chuatsi: molecular cloning, cytotoxicity analysis and expression profile. Mol. Immunol. 2007, 44(14):3615-3622.
93. Xie F.J., Zhang Z.P., Lin P., Wang S.H., Zou Z.H., Wang Y.L. Cloning and infection response of tumour-necrosis factor alpha in large yellow croaker Pseudosciaena crocea (Richardson). J. Fish Biol. 2008, 73(5):1149-1160.
94. Yuan S., Yu Y., Huang S., Liu T., Wu T., Dong M., et al. Bbt-TNFR1 and Bbt-TNFR2, two tumor necrosis factor receptors from Chinese amphioxus involve in host defense. Mol. Immunol. 2007, 44(5):756-762.
95. Zhang J. Evolution by gene duplication: an update. Trends Ecol. Evol. 2003, 18(6):292-298.
96. Zhang X., Luan W., Jin S., Xiang J. A novel tumor necrosis factor ligand superfamily member (CsTL) from Ciona savignyi: molecular identification and expression analysis. Dev. Comp. Immunol. 2008, 32(11):1362-1373.
97. Zhou Z., Tone Y., Song X., Furuuchi K., Lear J.D., Waldmann H., et al. Structural basis for ligand-mediated mouse GITR activation. Proc. Natl. Acad. Sci. U.S.A. 2008, 105(2):641-645.
98. Zou J., Wang T., Hirono I., Aoki T., Inagawa H., Honda T., et al. Differential expression of two tumor necrosis factor genes in rainbow trout, Oncorhynchus mykiss. Dev. Comp. Immunol. 2002, 26(2):161-172.
99. Zou J., Secombes C.J., Long S., Miller N., Clem L.W., Chinchar V.G. Molecular identification and expression analysis of tumor necrosis factor in channel catfish (Ictalurus punctatus). Dev. Comp. Immunol. 2003, 27(10):845-858.