Zebrafish (Danio rerio) as a model for investigating the safety of GM feed ingredients (soya and maize); Performance, stress response and uptake of dietary DNA sequences

British Journal of Nutrition

Volumn 103, Issue 1, 2010, Pages 3-15

  Sissener, Nini H ^a   Johannessen, Lene E ^b   Hevrøy, Ernst M ^a   Wiik Nielsen, Christer R ^b   Berdal, Knut G ^b   Nordgreen, Andreas ^a   Hemre, Gro Ingunn ^a  

^a INSTITUTE OF MARINE RESEARCH   (Norway)

^b NORWEGIAN VETERINARY INSTITUTE   (Norway)

Author keywords

Bt maize; GM feed; Roundup Ready soya; Zebrafish

Indexed keywords

ALDRIN; ALPHA HEXACHLOROCYCLOHEXANE; BETA ACTIN; CAMPHECLOR; CHLORDANE; COPPER ZINC SUPEROXIDE DISMUTASE; DIELDRIN; DNA; DNA FRAGMENT; ELONGATION FACTOR 1ALPHA; ENDOSULFAN; ENDRIN; GLUTATHIONE PEROXIDASE; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; HEPTACHLOR; HEXACHLOROBENZENE; HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE; LINDANE; MESSENGER RNA; NONACHLOR; OXYCHLORDANE; RAD51 PROTEIN; RIBOSOME PROTEIN; DEOXYRIBONUCLEASE; PESTICIDE RESIDUE; PLANT DNA; PLANT RNA; PRIMER DNA;

ANIMAL EXPERIMENT; ANIMAL FOOD; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DNA SEQUENCE; EXPERIMENTAL MODEL; FOOD COMPOSITION; FOOD CONTAMINATION; FOOD INTAKE; FOOD SAFETY; GAS CHROMATOGRAPHY; GENETICALLY MODIFIED FOOD; GROWTH RATE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MAIZE; MASS SPECTROMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYSICAL PERFORMANCE; POLYMERASE CHAIN REACTION; PROTEIN INTERACTION; RNA TRANSCRIPTION; SEX DIFFERENCE; SOYBEAN; STRESS; TRANSGENIC ANIMAL; VARIETAS; WEIGHT GAIN; ZEBRA FISH; ANIMAL; ANIMAL HUSBANDRY; BIOLOGICAL MODEL; FEMALE; GENETICS; GROWTH, DEVELOPMENT AND AGING; MALE; METABOLISM; PHYSIOLOGY; SEXUAL DEVELOPMENT; STANDARD;

DANIO RERIO; ZEA MAYS;

ANIMAL FEED; ANIMAL HUSBANDRY; ANIMALS; BASE SEQUENCE; DEOXYRIBONUCLEASES; DNA PRIMERS; DNA, PLANT; FEMALE; MALE; MODELS, BIOLOGICAL; PESTICIDE RESIDUES; RNA, PLANT; SEX CHARACTERISTICS; SOYBEANS; ZEA MAYS; ZEBRAFISH;

EID: 75549085980     PISSN: 00071145     EISSN: 14752662     Source Type: Journal    
DOI: 10.1017/S0007114509991401     Document Type: Article

References (88)

1. Driever W, Stemple D, Schier A, et al. (1994) Zebrafish: genetic tools for studying vertebrate development. Trends Genet 10, 152-159.
2. Fishman MC (2001) Genomics. Zebrafish-the canonical vertebrate. Science 294, 1290-1291.
3. Penberthy WT, Shafizadeh E & Lin S (2002) The zebrafish as a model for human disease. Front Biosci 7, 1439-1453.
4. Hill AJ, Teraoka H, Heideman W, et al. (2005) Zebrafish as a Model Vertebrate for Investigating Chemical Toxicity. Toxicol Sci 86, 6-19.
5. Lawrence C (2007) The husbandry of zebrafish (Danio rerio): a review. Aquaculture 269, 1-20.
6. Sanden M (2004) Genetically Modified Plant Products in Feed to Farmed Atlantic Salmon, Salmo salar L.-Effects on Growth, Feed Utilization, Fish Health and Assessment of Potential Risks. Bergen: Department of Fisheries and Marine Biology, University of Bergen.
7. Buddington RK, Krogdahl A & Bakke-McKellep AM (1997) The intestines of carnivorous fish: structure and functions and the relations with diet. Acta Physiol Scand Suppl 638, 67-80.
8. Kaushik SJ & Hemre G-I (2008) Plant proteins as alternative sources for fish feed and farmed fish quality. In Improving Farmed Fish Quality and Safety, pp. 300-319, chapter 12 [Ø Lie, editor]. Cambridge: Woodhead Publishing Limited/CRC Press.
9. Hemre GI, Sagstad A, Bakke-Mckellep AM, et al. (2007) Nutritional, physiological, and histological responses in Atlantic salmon, Salmo salar L. fed diets with genetically modified maize. Aqua Nutr 13, 186-199.
10. Sagstad A, Sanden M, Haugland Ø, et al. (2007) Evaluation of stress-and immune-response biomarkers in Atlantic salmon, Salmo salar L., fed different levels of genetically modified maize (Bt maize), compared with its near-isogenic parental line and a commercial suprex maize. J Fish Dis 30, 201-212.
11. Sanden M, Krogdahl A, Bakke-Mckellep AM, et al. (2006) Growth performance and organ development in Atlantic salmon, Salmo salar L. parr fed genetically modified (GM) soybean and maize. Aqua Nutr 12, 1-14.
12. Hammond BG, Vicini JL, Hartnell GF, et al. (1996) The feeding value of soybeans fed to rats, chickens, catfish and dairy cattle is not altered by genetic incorporation of glysophate tolerance. J Nutr 126, 717-727.
13. Hemre GI, Sanden M, Bakke-Mckellep AM, et al. (2005) Growth, feed utilization and health of Atlantic salmon Salmo salar L. fed genetically modified compared to non-modified commercial hybrid soybeans. Aqua Nutr 11, 157-167.
14. Sagstad A, Sanden M, Krogdahl A, et al. (2008) Organs development, gene expression and health of Atlantic salmon (Salmo salar L.) fed genetically modified soybeans compared to the near-isogenic non-modified parental line. Aqua Nutr 14, 556-572.
15. Chainark P, Satoh S, Hino T, et al. (2006) Avalability of genetically modified soybean meal in rainbow trout Oncorhynchus mykiss diets. Fisheries Sci 72, 1072-1078.
16. Sissener NH, Sanden M, Bakke AM, et al. (2009) A long term trial with Atlantic salmon (Salmo salar L.) fed genetically modified soy; focusing general health and performance before, during and after the parr-smolt transformation. Aquaculture 241, 108-117.
17. Bakke-McKellep AM, Sanden M, Danieli A, et al. (2008) Atlantic salmon (Salmo salar L.) parr fed genetically modified soybeans and maize: histological, digestive, metabolic, and immunological investigations. Res Vet Sci 84, 395-408.
18. Sanden M, Berntssen MHG, Krogdahl A, et al. (2005) An examination of the intestinal tract of Atlantic salmon, Salmo salar L., parr fed different varieties of soy and maize. J Fish Dis 28, 317-330.
19. Jonas DA, Elmadfa I, Engel KH, et al. (2001) Safety considerations of DNA in food. Ann Nutr Metab 45, 235-254.
20. Alexander TW, Reuter T, Aulrich K, et al. (2007) A review of the detection and fate of novel plant molecules derived from biotechnology in livestock production. Anim Feed Sci Technol 133, 31-62.
21. Sanden M, Bruce IJ, Rahman MA, et al. (2004) The fate of transgenic sequences present in genetically modified plant products in fish feed, investigating the survival of GM soybean DNA fragments during feeding trials in Atlantic salmon, Salmo salar L. Aquaculture 237, 391-405.
22. Nielsen CR, Berdal KG, Bakke-McKellep AM, et al. (2005) Dietary DNA in blood and organs of Atlantic salmon (Salmo salar L.). Eur Food Res Technol 221, 1-8.
23. Nielsen C, Holst-Jensen A, Løvseth A, et al. (2006) Persistence and distribution of intravenously injected DNA in blood and organs of Atlantic salmon (Salmo salar L.). Eur Food Res Tech-nol 222, 258-265.
24. Chainark P, Satoh S, Hirono I, et al. (2008) Availability of genetically modified feed ingredient: investigations of ingested foreign DNA in rainbow trout Oncorhynchus mykiss. Fisheries Sci 74, 380-390.
25. Sanden M, Berntssen M & Hemre G-I (2007) Intracellular localization of dietary and naked DNA in intestinal tissue of Atlantic salmon, Salmo salar L. using in situ hybridization. Eur Food Res Technol 225, 533-543.
26. EFSA (2006) Guidance document of the Scientific Panel on Genetically Modified Organisms for the risk assessment of genetically modified plants and derived food and feed. (EFSA ed.) ESFA J 1-100.
27. ILSI (2003) Best Practices for the Conduct of Animal Studies to evaluate Crops Genetically Modified for Output traits. Washington, DC: International Food Biotechnology Committee, International Life Sceinces Institute. http://wwwilsiorg/NR/rdonlyres/4A2F7C13-B4AA-4BC9-AEDE-696B4B72E3C4/0/ BestPracticesGuidelinespdf
28. Cowieson AJ (2005) Factors that affect the nutritional value of maize for broilers. Anim Feed Sci Technol 119, 293-305.
29. Lie Ø (1991) Studies of digestion, deposition and fatty acid composition of lipids in cod (Gadus morhua). PhD thesis, University of Bergen, Bergen.
30. AOAC (1995) AOAC Official Methods of Analysis Method 992.15: Crude Protein in Meat and Meat Products, Combustion Method, 16th ed. Arlington, VA: AOAC.
31. Hemre GI, Lie Ø, Lied E, et al. (1989) Starch as an energy source in feed for cod (Gadus morhua)-digestibility and retention. Aquaculture 80, 261-270.
32. CEN (2002) Foodstuffs-Determination of vitamin B6 (including its glycosylated forms) by HPLC. ENV14164 Comite' Europe'en de Normalisation (CEN) TC275 WI 00275131.
33. Julshamn K, Brenna J, Holland R, et al. (1999) Plasma source mass spectrometry-new developments and applications. R Soc Chem 241, 167-172.
34. Dmitrovic J, Chan SC & Chan SHY (2002) Analysis of pesticides and PCB congeners in serum by GC/MS with SPE sample cleanup. Toxicol Lett 134, 253-258.
35. Barranco A, Alonso-Salces RM, Bakkali A, et al. (2003) Solid-phase clean-up in the liquid chromatographic determination of polycyclic aromatic hydrocarbons in edible oils. J Chromatogr A 988, 33-40.
36. Murtha JM & Keller ET (2003) Characterization of the heat shock response in mature zebrafish (Danio rerio). Exp Gerontol 38, 683-691.
37. Olsvik P, Lie K, Stavrum A-K, et al. (2007) Gene-expression profiling in gill and liver of zebrafish exposed to produced water. Int J Environ Anal Chem 87, 195-210.
38. Malek RL, Sajadi H, Abraham J, et al. (2004) The effects of temperature reduction on gene expression and oxidative stress in skeletal muscle from adult zebrafish. Comp Biochem Physiol C Toxicol Pharmacol 138, 363-373.
39. Tang R, Dodd A, Lai D, et al. (2007) Validation of zebrafish (Danio rerio) reference genes for quantitative real-time RT-PCR normalization. Acta Biochim Biophys Sin 39, 384-390.
40. Higuchi R, Fockler C, Dollinger G, et al. (1993) Kinetic PCR analysis: real-time monitoring of DNA amplification reactions. Nat Biotech 11, 1026-1030.
41. Vandesompele J, De Preter K, Pattyn F, et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3, research0034.1-research0034.11.
42. Andersen CL, Jensen JL & Orntoft TF (2004) Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization. Applied to bladder and colon cancer data sets. Cancer Res 64, 5245-5250
43. GMO-CRL (2006) http://gmo-crl.jrc.it/detectionmethods/NK603-WEB- Protocol%20Validation.pdf
44. w soybean event-specific real-time quantitative PCR assay and estimation of the practical detection and quantification limits in GMO analyses. Eur Food Res Technol 213, 432-438
45. GMO-CRL (2006) http://gmo-crl.jrc.ec.europa.eu/summaries/Mon810- validation-report.pdf
46. Chandler DP (1998) Redefining relativity: quantitative PCR at low template concentrations for industrial and environmental microbiology. J Ind Microbiol Biotechnol 21, 128-140.
47. Berdal KG, Bøydler C, Tengs T, et al. (2008) A statistical approach for evaluation of PCR results to improve the practical limit of quantification (LOQ) of GMO analyses (SIMQUANT). Eur Food Res Technol 227, 1149-1157.
48. NMKL (2002) Measurement of uncertainty in microbiological examination in foods, NMKL-procedure No 8.
49. Ruohonen K (1998) Individual measurements and nested designs in aquaculture experiments: a simulation study. Aqua-culture 165, 149-157.
50. Ling EN & Cotter D (2003) Statistical power in comparative aquaculture studies. Aquaculture 224, 159-168.
51. Zar JH (1999) Biostatistical Analysis, 4th ed. Englewood Cliffs, NJ: Prentice Hall.
52. Bustin SA & Nolan T (2004) Pitfalls of quantitative real-time reverse-transcription polymerase chain reaction. J Biomol Tech-nol 15, 155-166.
53. Imbeaud S, Graudens E, Boulanger V, et al. (2005) Towards standardization of RNA quality assessment using user-independent classifiers of microcapillary electrophoresis traces. Nucleic Acids Res 33, e56.
54. Fleige S, Walf V, Huch S, et al. (2006) Comparison of relative mRNA quantification models and the impact of RNA integrity in quantitative real-time RT-PCR. Biotechnol Lett 28, 1601-1613.
55. De Luis R, Pérez MD, Sánchez L, et al. (2008) Kinetic and thermodynamic parameters for heat denaturation of Cry1A(b) protein from transgenic maize (Zea mays). J Food Sci 73, C447-C451.
56. Nordgarden U, Oppedal F, Taranger GL, et al. (2003) Seasonally changing metabolism in Atlantic salmon (Salmo salar L.); growth and feed conversion ratio. Aqua Nutr 9, 287-293.
57. NRC (1993) Nutrient Requirement of Fish. Washington, DC: National Research Council, National academy press.
58. Hevrøy EM, Tonheim S, Rønnestad I, et al. (2007) Zebrafish as a genetic model for the nutritional impact on growth in fish. The Norwegian Biochemical Society 43 Contact Meeting February 1-4, Lillehammer, Norway.
59. Bakan B, Melcion D, Richard-Molard D, et al. (2002) Fungal growth and fusarium mycotoxin content in isogenic traditional maize and genetically modified maize grown in France and Spain. J Agric Food Chem 50, 728-731.
60. Dowd PF (2000) Indirect reduction of ear molds and associated mycotoxins in Bacillus thuringiensis corn under controlled and open fields conditions: Utility and limitations. J Econ Entomol 1669-1679.
61. Papst C, Utz HF, Melchinger AE, et al. (2005) Mycotoxins produced by Fusarium spp. in isogenic Bt vs. non-Bt maize hybrids under European corn borer pressure. Agron J 97, 219-224.
62. Munkvold GP, Hellmich RL & Showers WB (1997) Reduced Fusarium Ear Rot and symptomless infection in kernels of maize genetically engineered for European corn borer resistance. Phytopathology 87, 1071-1077.
63. Flachowsky G, Chesson A & Aulrich K (2005) Animal nutrition with feeds from genetically modified plants. Arch Anim Nutr 1, 1-40.
64. Adlercreutz H, Höckerstedt K, Bannwart C, et al. (1987) Effect of dietary components, including lignans and phytoestrogens, on enterohepatic circulation and liver metabolism of estrogens and on sex hormone binding globulin (SHBG). J Steroid Biochem Mol Biol 27, 1135-1144.
65. Duncan AM, Merz BE, Xu X, et al. (1999) Soy isoflavones exert modest hormonal effects in premenopausal women. J Clin Endocrinol Metab 84, 192-197.
66. Bennetts HW, Uuderwood EJ & Shier FL (1946) A specific breeding problem of sheep on subterranen clover pastures in Western Australia. Aust Vet J 22, 2-12.
67. Setchell KD, Gosselin SJ, Welsh MB, et al. (1987) Dietary estrogens-a probable cause of infertility and liver disease in captive cheetahs. Gastroenterology 93, 225-233.
68. Pelissero C, Bennetau B, Babin P, et al. (1991) The estrogenic activity of certain phytoestrogens in the Siberian sturgeon Aci-penser baeri. J Steroid Biochem Mol Biol 38, 293-299.
69. Latonnelle K, Le Menn F, Kaushik SJ, et al. (2002) Effects of dietary phytoestrogens in vivo and in vitro in rainbow trout and Siberian sturgeon: interests and limits of the in vitro studies of interspecies differences. Gen Comp Endocrinol 126, 39-51.
70. Duke SO, Rimando AM, Pace PF, et al. (2003) Isoflavone, gly-phosate, and aminomethylphosphonic acid levels in seeds of glyphosate-treated, glyphosate-resistant soybean. J Agric Food Chem 51, 340-344.
71. Padgette SR, Taylor NB, Nida DL, et al. (1996) The composition of glyphosate-tolerant soybean seeds is equivalent to that of conventional soybeans. J Nutr 126, 702-716.
72. Taylor NB, Fuchs RL, MacDonald J, et al. (1999) Compositional analysis of glyphosate-tolerant soybeans treated with glyphosate. J Agric Food Chem 47, 4469-4473.
73. McCann MC, Liu K, Trujillo WA, et al. (2005) Glyphosate-tolerant soybeans remain compositionally equivalent to conventional soybeans (Glycine max L.) during three years of field testing. J Agric Food Chem 53, 5331-5335.
74. Borrás C, Sastre J, Garćia-Sala D, et al. (2003) Mitochondria from females exhibit higher antioxidant gene expression and lower oxidative damage than males. Free Radic Biol Med 34, 546-552.
75. Coto-Montes A, Boga JA, Tomás-Zapico C, et al. (2001) Physiological oxidative stress model: Syrian hamster Harderian gland-sex differences in antioxidant enzymes. Free Radic Biol Med 30, 785-792.
76. Schubbert R, Renz D, Schmitz B, et al. (1997) Foreign (M13) DNA ingested by mice reaches peripheral leukocytes, spleen, and liver via the intestinal wall mucosa and can be covalently linked to mouse DNA. Proc Natl Acad Sci USA 94, 961-966.
77. Schubbert R, Hohlweg U, Renz D, et al. (1998) On the fate of orally ingested foreign DNA in mice: chromosomal association and placental transmission to the fetus. Mol Gen Genet 259, 569-576.
78. Doerfler W & Schubbert R (1998) How dangerous is genetically engineered food. Wien Klin Wochenschr 110, 411.
79. Einspanier R, Klotz A, Kraft J, et al. (2001) The fate of forage plant DNA in farm animals: a collaborative case-study investigating cattle and chicken fed recombinant plant material. Eur Food Res Techn 212, 129-134.
80. Reuter T & Aulrich K (2003) Investigations on genetically modified maize (Bt-maize) in pig nutrition: fate of feed-ingested foreign DNA in pig bodies. Eur Food Res Techn 216, 185-192.
81. Tony MA, Butschke A, Broll H, et al. (2003) Safety assessment of Bt 176 maize in broiler nutrition: degradation of maize DNA and its metabolic fate. Arch Anim Nutr 57, 235-252.
82. Mazza R, Soave M, Morlacchini M, et al. (2005) Assessing the transfer of genetically modified DNA from feed to animal tissues. Transgenic Res 14, 775-784.
83. Rossi F, Morlacchini M, Fusconi G, et al. (2005) Effect of Bt corn on broiler growth performance and fate of feed-derived DNA in the digestive tract. Poult Sci 84, 1022-1030.
84. Sharma R, Damgaard D, Alexander TW, et al. (2006) Detection of transgenic and endogenous plant DNA in digesta and tissues of sheep and pigs fed roundup ready canola meal. J Agric Food Chem 54, 1699-1709.
85. Phipps RH, Deaville ER & Maddison BC (2003) Detection of transgenic and endogenous plant DNA in rumen fluid, duodenal digesta, milk, blood, and feces of lactating dairy cows. J Dairy Sci 86, 4070-4078.
86. Straub JA, Hertel C & Hammes WP (1999) The fate of recom-binant DNA in thermally treated fermented sausages. Eur Food Res Technol 210, 62-67.
87. Palka-Santini M, Schwarz-Herzke B, Hösel M, et al. (2003) The gastrointestinal tract as the portal of entry for foreign macromolecules: fate of DNA and proteins. Mol Genet Genomics 270, 201-215.
88. Tacon AGJ (1987) The Nutrition and Feeding of Farmed Fish and Shrimp-A Training Manual:1. The essential nutrients. Brazil: Food and Agriculture Organization of the United Nations, pp. 117. GPC/RLA/075/ITA.