Changes in hepatic gene expression related to innate immunity, growth and iron metabolism in GH-transgenic amago salmon (Oncorhynchus masou) by cDNA subtraction and microarray analysis, and serum lysozyme activity

General and Comparative Endocrinology

Volumn 151, Issue 1, 2007, Pages 42-54

  Mori, Tsukasa ^a   Hiraka, Ikuei ^a   Kurata, Youichi ^a   Kawachi, Hiroko ^a   Mano, Nobuhiro ^a   Devlin, Robert H ^b   Nagoya, Hiroyuki ^c   Araki, Kazuo ^c  

^a NIHON UNIVERSITY   (Japan)

^b FISHERIES AND OCEANS CANADA   (Canada)

^c FISHERIES RESEARCH AGENCY   (Japan)

Author keywords

Amago; Bikunin; cDNA subtraction; DNA microarray; GFRP; GH transgenic fish; Heme oxygenase; LECT2; Lectin; Oncorhynchus masou; Serum lysozyme activity; Vitelline envelope protein; 6 Desaturase

Indexed keywords

ACYL COENZYME A; ALCOHOL DEHYDROGENASE; APOLIPOPROTEIN; CHEMOTAXIN; COMPLEMENTARY DNA; ENVELOPE PROTEIN; GROWTH HORMONE; GUANOSINE TRIPHOSPHATE CYCLOHYDROLASE I; HEME OXYGENASE; HEMOPEXIN; INTER ALPHA TRYPSIN INHIBITOR; IRON; LECTIN; LINOLEOYL COENZYME A DESATURASE; LYSOZYME; MANNOSE BINDING LECTIN; PENTRAXIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; RNA; SERINE PROTEINASE; ULINASTATIN;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME BLOOD LEVEL; GENE EXPRESSION; GENE FREQUENCY; GENE IDENTIFICATION; GENE ISOLATION; GENE SEQUENCE; INNATE IMMUNITY; IRON METABOLISM; MALE; MATURATION; MICROARRAY ANALYSIS; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; QUANTITATIVE ANALYSIS; SALMON; SUBTRACTIVE HYBRIDIZATION; TRANSGENIC ANIMAL;

EID: 33846926772     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2006.11.012     Document Type: Article

References (84)

1. Abrahams M.V., and Sutterlin A. The foraging and anti-predator behaviour of growth-enhanced transgenic Atlantic salmon. Anim. Behav. 58 (1999) 933-942
2. Angelin B., and Rudling M. Growth hormone and hepatic lipoprotein metabolism. Curr. Opin. Lipidol. 5 (1994) 160-165
3. Cook H.W. Fatty Acid Desaturation and Chain Elongation in Eukaryote (1996), Elsevier, Amsterdam
4. Cook J.T., Sutterlin A.M., and McNiven M.A. Effect of food deprivation on oxygen consumption and body composition of growth-enhanced transgenic Atlantic salmon (Salmo salar). Aquaculture 188 (2000) 47-63
5. Cook J.T., McNiven M.A., Richardson G.F., and Sutterlin A.M. Growth rate, body composition and feed digestibility/conversion of growth-enhanced transgenic Atlantic salmon (Salmo salar). Aquaculture 188 (2000) 15-32
6. Daveau M., Rouet P., Scotte M., Faye L., Hiron M., Lebreton J.P., and Salier J.P. Human inter-alpha-inhibitor family in inflammation: simultaneous synthesis of positive and negative acute-phase proteins. Biochem. J. 292 Pt 2 (1993) 485-492
7. Davidson M.D. Effect of growth hormone on carbohydrate and lipid metabolism. Endocr. Rev. 8 (1987) 115-131
8. Devlin R.H. Transgenic salmonids. In: Houdebine L.M. (Ed). Transgenic Animals: Generation and Use (1997), Harwood Academic Publishers, Amsterdam, The Netherlands
9. Devlin R.H., Johnsson J.I., Smailus D.E., Biagi C.A., Jonsson E., and Bjornsson B.T. Increased ability to compete for food by growth hormone-transgenic coho salmon Oncorhynchus kisutch (Walbaum). Aquac. Res. 30 1999 (1999) 479-482
10. Devlin R.H., Swanson P., Clarke W.C., Plisetskaya E., Dickhoff W., Moriyama S., Yesaki T.Y., and Hew C.L. Seawater adaptability and hormone levels in growth-enhanced transgenic coho salmon, Oncorhynchus kisutch. Aquaculture 191 (2000) 367-385
11. Devlin R.H., Yesaki T.Y., Biagi C.A., Donaldson E.M., Swanson P., and Chan W.K. Extraordinary salmon growth. Nature 371 (1994) 209-210
12. Dumont J.N., and Brummett A.R. The vitelline envelope, chorion and micropyle of Fundulus heteroclitis eggs. Gamete Res. 3 (1980) 25-44
13. Eales J.G., Devlin R., Higgs D.A., McLeese J.M., and Plohman J. Thyroid function in growth-hormone-transgenic coho salmon (Oncorhynchus kisutch). Can. J. Zool. 82 (2004) 1225-1229
14. Eisemann J.H., Tyrrell H.F., Hammond A.C., Reynolds P.J., Bauman D.E., Haaland G.L., McMurtry J.P., and Varga G.A. Effect of bovine growth hormone administration on metabolism of growing Hereford heifers: dietary digestibility, energy and nitrogen balance. J. Nutr. 116 (1986) 157-163
15. Emsley J., White H.E., O'Hara B.P., Oliva G., Srinivasan N., Tickle I.J., Blundell T.L., Pepys M.B., and Wood S.P. Structure of pentameric human serum amyloid P component. Nature 367 (1994) 338-345
16. Ewing J.F., and Maines M.D. Rapid induction of heme oxygenase 1 mRNA and protein by hyperthermia in rat brain: heme oxygenase 2 is not a heat shock protein. Proc. Natl. Acad. Sci. USA 88 (1991) 5364-5368
17. Fantone J.C., Kunkel S.L., and Zurier R.B. Effects of Prostaglandins on In vivo Immune and Inflammatory Reactions (1985), Martinus Nijhoff Publishing, Boston
18. Farrell A.P., Bennett W., and Devlin R.H. Growth-enhanced transgenic salmon can be inferior swimmers. Can. J. Zool. 75 (1997) 335-337
19. Frick F., Bohlooly Y.M., Linden D., Olsson B., Tornell J., Eden S., and Oscarsson J. Long-term growth hormone excess induces marked alterations in lipoprotein metabolism in mice. Am. J. Physiol. Endocrinol. Metab. 281 (2001) E1230-E1239
20. Frick F., Linden D., Ameen C., Eden S., Mode A., and Oscarsson J. Interaction between growth hormone and insulin in the regulation of lipoprotein metabolism in the rat. Am. J. Physiol. Endocrinol. Metab. 283 (2002) E1023-E1031
21. Fries E., and Kaczmarczyk A. Inter-alpha-inhibitor, hyaluronan and inflammation. Acta Biochim. Pol. 50 (2003) 735-742
22. Geisert R.D., Ashworth M.D., and Malayer J.R. Expression of inter-alpha-trypsin inhibitor heavy chains in endometrium of cyclic and pregnant gilts. Reproduction 126 (2003) 621-627
23. Goldstein I.J., Hughesr R.C., Monsigny M., Osawa T., and Sharon N. What should be called a lectin?. Nature (1980) 285 66-66
24. Hamerman D., and Sandson J. Unusual properties of hyaluronateprotein isolated from pathological synovial fluids. J. Clin. Invest. 42 (1963) 1882-1889
25. Hansen T.K., Thiel S., Dall R., Rosenfalck A.M., Trainer P., Flyvbjerg A., Jorgensen J.O., and Christiansen J.S. GH strongly affects serum concentrations of mannan-binding lectin: evidence for a new IGF-I independent immunomodulatory effect of GH. J. Clin. Endocrinol. Metab. 86 (2001) 5383-5388
26. Hiraki Y., Inoue H., Kondo J., Kamizono A., Yoshitake Y., Shukunami C., and Suzuki F. A novel growth-promoting factor derived from fetal bovine cartilage, chondromodulin II. Purification and amino acid sequence. J. Biol. Chem. 271 (1996) 22657-22662
27. Hoffmann J.A., Kafatos F.C., Janeway C.A., and Ezekowitz R.A. Phylogenetic perspectives in innate immunity. Science 284 (1999) 1313-1318
28. Horrobin D.F. Nutritional and medical importance of gamma-linolenic acid. Prog. Lipid Res. 31 (1992) 163-194
29. Hunt R.C., Handy I., and Smith A. Heme-mediated reactive oxygen species toxicity to retinal pigment epithelial cells is reduced by hemopexin. J. Cell Physiol. 168 (1996) 81-86
30. Isaksson O.G., Jansson J.O., and Gause I.A. Growth hormone stimulates longitudinal bone growth directly. Science 216 (1982) 1237-1239
31. Jeay S., Sonenshein G.E., Postel-Vinay M.C., Kelly P.A., and Baixeras E. Growth hormone can act as a cytokine controlling survival and proliferation of immune cells: new insights into signaling pathways. Mol. Cell Endocrinol. 188 (2002) 1-7
32. Jhingan E., Devlin R.H., and Iwama G.K. Disease resistance, stress response and effects of triploidy in growth hormone transgenic coho salmon. J. Fish Biol. 63 (2003) 806-823
33. Kolb-Bachofen V. A review on the biological properties of C-reactive protein. Immunobiology 183 (1991) 133-145
34. Kopchick J.J., and Andry J.M. Growth hormone (GH), GH receptor, and signal transduction. Mol. Genet. Metab. 71 (2000) 293-314
35. Krasnov A., Agren J.J., Pitaknen T.I., and Molsa H. Transfer of growth hormone (GH) transgenes into Arctic charr. (Salvelinus alpinus L.) II. Nutrient partitioning in rapidly growing fish. Genet. Anal. 15 (1999) 99-105
36. Lee C.G., Devlin R.H., and Farrell A.P. Swimming performance, oxygen uptake and oxygen debt in adult transgenic and ocean-ranched coho salmon (Oncorhynchus kisutch, Walbaum). J. Fish Biol. 62 (2003) 753-766
37. Leggatt R.A., Devlin R.H., Farrell A.P., and Randall D.J. Oxygen uptake of growth hormone transgenic coho salmon during starvation and feeding. J. Fish Biol. 62 (2003) 1053-1066
38. Linden D., Sjoberg A., Asp L., Carlsson L., and Oscarsson J. Direct effects of growth hormone on production and secretion of apolipoprotein B from rat hepatocytes. Am. J. Physiol. Endocrinol. Metab. 279 (2000) E1335-E1346
39. Lombardi G., Colao A., Ferone D., Marzullo P., Orio F., Longobardi S., and Merola B. Effect of growth hormone on cardiac function. Horm. Res. 48 Suppl 4 (1997) 38-42
40. Maines M.D. Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications. FASEB J. 2 (1988) 2557-2568
41. Marone G., Fimiani B., Torella G., Poto S., Bianco P., and Condorelli M. Possible role of arachidonic acid and of phospholipase A2 in the control of lysosomal enzyme release from human polymorphonuclear leukocytes. J. Clin. Lab. Immunol. 12 (1983) 111-116
42. McCoubrey Jr. W.K., Huang T.J., and Maines M.D. Isolation and characterization of a cDNA from the rat brain that encodes hemoprotein heme oxygenase-3. Eur. J. Biochem. 247 (1997) 725-732
43. McKeehan W.L., Sakagami Y., Hoshi H., and McKeehan K.A. Two apparent human endothelial cell growth factors from human hepatoma cells are tumor-associated proteinase inhibitors. J. Biol. Chem. 261 (1986) 5378-5383
44. Miller Y.I., Smith A., Morgan W.T., and Shaklai N. Role of hemopexin in protection of low-density lipoprotein against hemoglobin-induced oxidation. Biochemistry 35 (1996) 13112-13117
45. Milstien S., Jaffe H., Kowlessur D., and Bonner T.I. Purification and cloning of the GTP cyclohydrolase I feedback regulatory protein, GFRP. J. Biol. Chem. 271 (1996) 19743-19751
46. Mizushima S., Nii A., Kato K., and Uemura A. Gene expression of the two heavy chains and one light chain forming the inter-alpha-trypsin-inhibitor in human tissues. Biol. Pharm. Bull. 21 (1998) 167-169
47. Mori T., and Devlin R.H. Transgene and host growth hormone gene expression in pituitary and nonpituitary tissues of normal and growth hormone transgenic salmon. Mol. Cell. Endocrinol. 149 (1999) 129-139
48. Mori T., Sumiya S., and Yokota H. Electrostatic interactions of androgens and progesterone derivatives with rainbow trout estrogen receptor. J. Steroid Biochem. Mol. Biol. 75 (2000) 129-137
49. Mori Y., Hiraki Y., Shukunami C., Kakudo S., Shiokawa M., Kagoshima M., Mano H., Hakeda Y., Kurokawa T., Suzuki F., and Kumegawa M. Stimulation of osteoblast proliferation by the cartilage-derived growth promoting factors chondromodulin-I and -II. FEBS Lett. 406 (1997) 310-314
50. Muller-Eberhard U., and Fraig M. Bioactivity of heme and its containment. Am. J. Hematol. 42 (1993) 59-62
51. Murata K., Sugiyama H., Yasumasu S., Iuchi I., Yasumasu I., and Yamagami K. Cloning of cDNA and estrogen-induced hepatic gene expression for choriogenin H, a precursor protein of the fish egg envelope (chorion). Proc. Natl. Acad. Sci. USA 94 (1997) 2050-2055
52. Nakamura M.T., Phinney S.D., Tang A.B., Oberbauer A.M., German J.B., and Murray J.D. Increased hepatic delta 6-desaturase activity with growth hormone expression in the MG101 transgenic mouse. Lipids 31 (1996) 139-143
53. Nam Y.K., Noh J.K., Cho Y.S., Cho H.J., Cho K.N., Kim C.G., and Kim D.S. Dramatically accelerated growth and extraordinary gigantism of transgenic mud loach Misgurnus mizolepis. Transgenic Res. 10 (2001) 353-362
54. Nikkila H., Gitlin J.D., and Muller-Eberhard U. Rat hemopexin. Molecular cloning, primary structural characterization, and analysis of gene expression. Biochemistry 30 (1991) 823-829
55. Olsson B., Bohlooly Y.M., Brusehed O., Isaksson O.G., Ahren B., Olofsson S.O., Oscarsson J., and Tornell J. Bovine growth hormone-transgenic mice have major alterations in hepatic expression of metabolic genes. Am. J. Physiol. Endocrinol. Metab. 285 (2003) E504-E511 Epub 2003 May 7
56. Oscarsson J., Ottosson M., and Eden S. Effects of growth hormone on lipoprotein lipase and hepatic lipase. J. Endocrinol. Invest. 22 (1999) 2-9
57. Parry R.M., Chandau R.C., and Shanhani R.M. A rapid and sensitive assay of muramidase. Proc. Soc. Exp. Biol. Med. 119 (1965) 384-386
58. Pepys M.B., and Baltz M.L. Acute phase proteins with special reference to C-reactive protein and related proteins (pentaxins) and serum amyloid A protein. Adv. Immunol. 34 (1983) 141-212
59. Pursel V.G., Rexroad C.E., and Bolt D.J. Gene Transfer for Enhanced Growth of Livestock (1988), Plenum Publishing, New York
60. Rahman M.A., Mak R., Ayad H., Smith A., and Maclean N. Expression of a novel piscine growth hormone gene results in growth enhancement in transgenic tilapia (Oreochromis niloticus). Transgenic Res. 7 (1998) 357-369
61. Ren Y., and Smith A. Mechanism of metallothionein gene regulation by heme-hemopexin. Roles of protein kinase C, reactive oxygen species, and cis-acting elements. J. Biol. Chem. 270 (1995) 23988-23995
62. Rise M.L., von Schalburg K.R., Brown G.D., Mawer M.A., Devlin R.H., Kuipers N., Busby M., Beetz-Sargent M., Alberto R., Gibbs A.R., Hunt P., Shukin R., Zeznik J.A., Nelson C., Jones S.R., Smailus D.E., Jones S.J., Schein J.E., Marra M.A., Butterfield Y.S., Stott J.M., Ng S.H., Davidson W.S., and Koop B.F. Development and application of a salmonid EST database and cDNA microarray: data mining and interspecific hybridization characteristics. Genome Res. 14 (2004) 478-490
63. Rizzardini M., Terao M., Falciani F., and Cantoni L. Cytokine induction of haem oxygenase mRNA in mouse liver. Interleukin 1 transcriptionally activates the haem oxygenase gene. Biochem. J. 290 Pt 2 (1993) 343-347
64. Roberts S.B., McCauley L.A., Devlin R.H., and Goetz F.W. Transgenic salmon overexpressing growth hormone exhibit decreased myostatin transcript and protein expression. J. Exp. Biol. 207 (2004) 3741-3748
65. Shimada Y., Morita T., and Sugiyama K. Increased response of liver microsomal delta 6-desaturase activity to dietary methionine in rats. Biosci. Biotechnol. Biochem. 67 (2003) 743-751
66. Steel D.M., and Whitehead A.S. The major acute phase reactants: C-reactive protein, serum amyloid P component and serum amyloid A protein. Immunol. Today 15 (1994) 81-88
67. Stevens E.D., and Devlin R.H. Intestinal morphology in growth hormone transgenic coho salmon. J. Fish Biol. 56 (2000) 191-195
68. Stevens E.D., and Devlin R.H. Gill morphometry in growth hormone transgenic Pacific coho salmon, Onchorhyncus kisutch, differs markedly from that in GH transgenic Atlantic salmon. Environ. Biol. Fish. 58 (2000) 113-117
69. Stred S.E., and Messina J.L. Identification of hemopexin as a GH-regulated gene. Mol. Cell Endocrinol. 204 (2003) 101-110
70. Sundström L.F., Lõhmus M., and Devlin R.H. Selection on increased intrinsic growth rates in coho salmon, Oncorhynchus kisutch. Evolution 59 (2005) 1560-1569
71. Sundström L.F., Devlin R.H., Johnsson J.I., and Biagi C.A. Vertical position reflects increased feeding motivation in growth hormone transgenic coho salmon (Oncorhynchus kisutch). Ethology 109 (2003) 701-712
72. Sundström L.F., Lõhmus M., Devlin R.H., Johnsson J.I., Biagi C.A., and Bohlin T. Feeding on profitable and unprofitable prey: comparing behaviour of growth-enhanced transgenic and normal coho salmon (Oncorhynchus kisutch). Ethology 110 (2004) 381-396
73. Sundström L.F., Lohmus M., Johnsson J.I., and Devlin R.H. Growth hormone transgenic salmon pay for growth potential with increased predation mortality. Proc. Biol. Sci. 271 (2004) S350-S352
74. Szalai A.J., Agrawal A., Greenhough T.J., and Volanakis J.E. C-reactive protein structural biology, gene expression, and host defense function. Immunol. Res. 16 (1997) 127-136
75. Tiffoche C., Chesnel A., Jego P., and Le Pennec J.P. Isolation and characterization of a cDNA clone encoding a Pleurodeles lectin. Eur. J. Biochem. 213 (1993) 901-907
76. Wassarman P.M. Zona pellucida glycoproteins. Annu. Rev. Biochem. 57 (1988) 415-442
77. Yamagoe S., Mizuno S., and Suzuki K. Molecular cloning of human and bovine LECT2 having a neutrophil chemotactic activity and its specific expression in the liver. Biochim. Biophys. Acta 1396 (1998) 105-113
78. Yamagoe S., Watanabe T., Mizuno S., and Suzuki K. The mouse Lect2 gene: cloning of cDNA and genomic DNA, structural characterization and chromosomal localization. Gene 216 (1998) 171-178
79. Yamagoe S., Yamakawa Y., Matsuo Y., Minowada J., Mizuno S., and Suzuki K. Purification and primary amino acid sequence of a novel neutrophil chemotactic factor LECT2. Immunol. Lett. 52 (1996) 9-13
80. Yoshida T., Biro P., Cohen T., Muller R.M., and Shibahara S. Human heme oxygenase cDNA and induction of its mRNA by hemin. Eur. J. Biochem. 171 (1988) 457-461
81. Yoshizato H., Fujikawa T., Soya H., Tanaka M., and Nakashima K. The growth hormone (GH) gene is expressed in the lateral hypothalamus: enhancement by GH-releasing hormone and repression by restraint stress. Endocrinology 139 (1998) 2545-2551
82. Zhang H., Guo Y., and Yuan J. Conjugated linoleic acid enhanced the immune function in broiler chicks. Br. J. Nutr. 94 (2005) 746-752
83. Zhu L., Hope T.J., Hall J., Davies A., Stern M., Muller-Eberhard U., Stern R., and Parslow T.G. Molecular cloning of a mammalian hyaluronidase reveals identity with hemopexin, a serum heme-binding protein. J. Biol. Chem. 269 (1994) 32092-32097
84. Zhuo L., Hascall V.C., and Kimata K. Inter-alpha-trypsin inhibitor, a covalent protein-glycosaminoglycan-protein complex. J. Biol. Chem. 279 (2004) 38079-38082