Influence of a contaminated fish diet on germline expanded-simple-tandem-repeat mutation frequency in mice
Corresponding Author
Christopher M. Somers
Department of Biology, McMaster University, Hamilton, Ontario, Canada
Department of Biology, University of Regina, Regina, SK, Canada, S4S 0A2Search for more papers by this authorEduardo V. Valdes
Nutrition Centre, Metropolitan Toronto Zoo, Scarborough, Ontario, Canada
Search for more papers by this authorVictoria A. Kjoss
Department of Biology, McMaster University, Hamilton, Ontario, Canada
Search for more papers by this authorAndre L. Vaillancourt
Sport Fish and Biomonitoring Unit, Environmental Monitoring and Reporting Branch, Ontario Ministry of the Environment, Etobicoke, Ontario, Canada
Search for more papers by this authorJames S. Quinn
Department of Biology, McMaster University, Hamilton, Ontario, Canada
Search for more papers by this authorCorresponding Author
Christopher M. Somers
Department of Biology, McMaster University, Hamilton, Ontario, Canada
Department of Biology, University of Regina, Regina, SK, Canada, S4S 0A2Search for more papers by this authorEduardo V. Valdes
Nutrition Centre, Metropolitan Toronto Zoo, Scarborough, Ontario, Canada
Search for more papers by this authorVictoria A. Kjoss
Department of Biology, McMaster University, Hamilton, Ontario, Canada
Search for more papers by this authorAndre L. Vaillancourt
Sport Fish and Biomonitoring Unit, Environmental Monitoring and Reporting Branch, Ontario Ministry of the Environment, Etobicoke, Ontario, Canada
Search for more papers by this authorJames S. Quinn
Department of Biology, McMaster University, Hamilton, Ontario, Canada
Search for more papers by this authorAbstract
Herring gulls (Larus argentatus) in polluted areas on the North American Great Lakes were previously shown to have elevated germline mutation frequencies at minisatellite DNA loci. Airborne or dietary contaminants likely caused induced mutations, but the importance of each exposure type was unknown. Follow-up experiments with lab mice determined that air pollution significantly induced germline mutations; however, an evaluation of mutations induced by the diet of herring gulls has not yet been conducted. To address this issue, we fed mice a high-fish diet (58% wet mass) of the most common prey species for herring gulls nesting in Hamilton Harbour, a polluted industrial area on Lake Ontario. We bred the mice and screened pedigrees for germline mutations at expanded-simple-tandem-repeat (ESTR) DNA loci. Mutation frequencies were compared to those in a reference group that was fed fish from Atlantic Canada, and a control group that was fed commercial chow. Germline mutation frequencies were highest in mice fed contaminated fish, but were only marginally or not significantly affected by diet treatment. Statistical power to detect differences among treatment groups was low, and the effect of diet may have more clearly emerged if larger sample sizes were available. Levels of organic pollutants in the fish from Hamilton Harbour were higher than those from Atlantic Canada, but their ability to induce ESTR mutations is unknown. Our findings suggest that a contaminated fish diet may contribute to the elevated germline mutation frequencies observed previously in gulls at this site, but air pollution is likely a more important route of exposure. Environ. Mol. Mutagen. 2008. © 2008 Wiley-Liss, Inc.
REFERENCES
- Arnold DL,Stapley R,Bryce F,Mahon D. 1998. A multigenerational study to ascertain the toxicological effects of Great Lakes salmon fed to rats: Study overview and design. Regul Toxicol Pharmacol 27: s1–s7.
- Beattie MK,Gerstenberger SL,Hoffman R,Dellinger JA. 1996. Rodent neurotoxicity bioassays for screening contaminated Great Lakes fish. Environ Toxicol Chem 15: 313–318.
- Bois P,Williamson J,Brown J,Dubrova YE,Jeffreys AJ. 1998. A novel unstable mouse VNTR family expanded from SINE B1 elements. Genomics 49: 122–128.
- Ceccarelli AV,Rozengurt N. 2002. Outbreak of hind limb paralysis in young CFW Swiss Webster mice. Compar Med 52: 171–175.
- Cleland GB,Leatherland JF,Sonstegard RA. 1987. Toxic effects in C57B1/6 and DBA/2 mice following consumption of halogenated aromatic hydrocarbon contaminated Great Lakes Coho Salmon (Oncorhynchus kisutch Walbaum). Environ Health Perspect 75: 153–157.
- Cleland GB,Oliver BG,Sonstegard RA. 1988. Bioaccumulation of halogenated aromatic hydrocarbons in C57Bl/6 and DBA/2 mice following consumption of Great Lakes coho salmon (Oncorhynchus kisutch). Chemosphere 17: 405–420.
- Cole DC,Sheeshka J,Murkin EJ,Kearney J,Scott F,Ferron LA,Weber, J-P. 2002. Dietary intakes and plasma organochlorine contaminant levels among Great Lakes fish eaters. Arch Environ Health 57: 496–509.
- Dubrova YE,Plumb M,Brown J,Fennelly J,Bois P,Goodhead D,Jeffreys AJ. 1998. Stage specificity, dose response, and doubling dose for mouse minisatellite germline mutation induced by acute radiation. Proc Natl Acad Sci USA 95: 6251–6255.
- Ewins PJ,Weseloh DV,Norstrom, RJ,Legierse K,Auman HJ,Ludwig, JP. 1994. Caspian terns on the Great Lakes: Organochlorine contamination, reproduction, diet, and population changes, 1972–1991. Environment Canada. Canadian Wildlife Service Occasional Paper No. 85.
- Faroon OM,Keith S,Jones D,De Rosa C. 2001. Carcinogenic effects of polychlorinated biphenyls. Toxicol Ind Health 17: 41–62.
- Feeley MM,Jordan SA,Gilman AP. 1998. The health Canada Great Lakes multigeneration s—Summary and regulatory considerations. Regul Toxicol Pharmacol 27: s90–s98.
- Gerstenberger SL,Heimler I,Smies R,Hutz RJ,Dasmahapatra AK,Tripoli V,Dellinger JA. 2000. Minimal endocrine alterations in rodents after consumption of lake trout (Salvelinus namaycush). Arch Environ Contam Toxicol 38: 371–376.
- Gibbs M,Collick A,Kelly R,Jeffreys AJ. 1993. A tetranucleotide repeat mouse minisatellite displaying substantial somatic instability during early preimplantation development. Genomics 17: 121–128.
- Hansen GM,Skapura D,Justice MJ. 2000. Genetic profile of insertion mutations in mouse leukemias and lymphomas. Genome Res 10: 237–243.
- Hedenskog M,Sjogren M,Cederberg H,Rannug U. 1997. Induction of germline length mutations at the minisatellites PC-1 and PC-2 in male mice exposed to polychlorinated biphenyls and diesel exhaust emissions. Environ Mol Mutagen 30: 254–259.
- Hites RA,Foran JA,Carpenter DO,Hamilton MC,Knuth BA,Schwager SJ. 2004. Global assessment of organic contaminants in farmed salmon. Science 303: 226–229.
- Jin G,Tsuruyama T,Yamada Y,Hiai Y. 2003. Svi3: A provirus common integration site in c-myc in SL/Kh pre-B lymphomas. Cancer Sci 94: 791–795.
- Kassa H,Bisesi MS. 2001. Levels of polychlorinated biphenyls (PCBs) in fish: The influence on local decision making about fish consumption. J Environ Health 63: 29–35.
- Kearney JP,Cole DC,Ferron LA,Weber, J-P. 1999. Blood PCB, p,p-DDE, and mirex levels in Great Lakes fish and waterfowl consumers in two Ontario communities. Environ Res A 80: s138–s149.
- Kelly R,Bulfield G,Collick A,Gibbs M,Jeffreys AJ. 1989. Characterization of a highly unstable mouse minisatellite locus: Evidence for somatic mutation during early development. Genomics 5: 844–856.
- Molitoris SJ,Blankenship SJ,Iribeck NA. 1998. Palatability of a nutritional gel fish substitute for traditional fish diets in zoos. In: Symposia of the Comparative Nutrition Society No. 2, Banff, Alberta, Canada. pp. 134–138.
- Nadon S,Kosatsky T,Przybysz R. 2002. Contaminant exposure among women of childbearing age who eat St. Lawrence River sport fish. Arch Environ Health 57: 473–481.
- Oakberg E. 1956. Duration of spermatogenesis in the mouse and timing of stages of the cycle of the seminiferous epithelium. Am J Anat 99: 507–516.
- Ontario Ministry of the Environment. 2007. Guide to Eating Ontario Sport Fish 2007–2008. Queen's Printer for Ontario, ISSN 0826–9653.
- Oyarzun S,Santor C. 1980. A preliminary report on the use of gelatin-based diets for zoo animals. In: Proceedings of the First Annual Dr. Scholl Nutrition Conference, Lincoln Park Zoological Gardens, Chicago IL, USA. pp. 173–183.
- Reichrtova E,Foltinova J,Takac L. 1995. A non-traditional approach to risk assessment of respiratory exposure to outdoor air pollutants. J Aerosol Med 8: 233–241.
- Restum JC,Bursian SJ,Giesy JP,Render JA,Helferich WG,Shipp EB,Verbrugge DA. 1998. Multigenerational study of the effects of consumption of PCB-contaminated carp from Saginaw Bay, Lake Huron, on mink, Part 1. Effects on mink reproduction, kit growth and survival, and selected biological parameters. J Toxicol Environ Health 54: 343–375.
- Reymao MSF,Cury PM,Lichtenfels, AJFC,Lemos M,Battlehner CN,Conceicao GMS,Capelozzi VL,Montes GS,Junior MF,Martins MA,Bohm GM,Saldiva PHN. 1997. Urban air pollution enhances the formation of urethane-induced lung tumours in mice. Environ Res 74: 150–158.
- Ryckman DP,Weseloh DV,Bishop CA. 2000. Contaminants in herring gull eggs from the Great Lakes: 25 years of monitoring levels and effects. Environment Canada Fact Sheet. Ottawa, Ontario, Canada: Environment Canada, p 12. Available at: www.on.ec.gc.ca/wildlife/factsheets/fs_herring_gulls-e.html.
- Schantz SL,Gardiner JC,Gasior DM,Sweeney AM,Humphrey HEB,McCaffrey RJ. 1999. Motor function in aging Great Lakes fisheaters. Environ Res A 80: s46–s56.
- Simes RJ. 1986. An improved Bonferroni procedure for multiple tests of significance. Biometrika 73: 751–754.
- Sokal RR,Rohlf FJ. 1995. Biometry: The Principles and Practice of Statistics in Biological Research, 3rd ed. New York: W. H. Freeman. 887p. ISBN: 0-7167-2411–1.
- Somers CM. 2006. Expanded simple tandem repeat (ESTR) mutation induction in the male germline: Lessons learned from lab mice. Mutat Res 598: 35–49.
- Somers CM,Yauk CL,White PA,Parfett CLJ,Quinn JS. 2002. Air pollution induces heritable DNA mutations. Proc Natl Acad Sci USA 99: 15904–15907.
- Somers CM,McCarry BE,Malek F,Quinn JS. 2004a. Reduction of particulate air pollution lowers risk of heritable mutations in mice. Science 304: 1008–1010.
- Somers CM,Sharma R,Quinn JS,Boreham DR. 2004b. Gamma-radiation induced heritable mutations at repetitive DNA loci in out-bred mice. Mutat Res 568: 69–78.
- Somers CM,Kwiecien JM,Quinn JS. 2005. A marine fish diet reduces spontaneous lymphoma in out-bred Swiss-Webster mice. Leukemia Lymphoma 46: 1797–1800.
- Somers CM,Valdes EV,Quinn JS. 2006. An approach to feeding high percentage fish diets to mice for human and wildlife toxicology studies. Ecotoxicol Environ Safety 63: 481–487.
- Stapleton M,Dunn PO,McCarty J,Secord A,Whittingham LA. 2001. Polychlorinated biphenyl contamination and minisatellite DNA mutation rates of tree swallows. Environ Toxicol Chem 20: 2263–2267.
- Stewart P,Pagano J,Sargent D,Darvill T,Lonky E,Reihman J. 2000. Effects of Great Lakes fish consumption on brain PCB pattern, concentration, and progressive-ratio performance. Environ Res A 82: 18–32.
- Taddesse-Heath L,Chattopadhyay SK,Dillehay DL,Lander MR,Nagashfar Z,MorseIII,HC,Hartely JW. 2000. Lymphomas and high-level expression of murine leukemia viruses in CFW mice. J Virol 74: 6832–6837.
- Vilarino-Guell C,Smith AG,Dubrova YE. 2003. Germline mutation induction at mouse repeat DNA loci by chemical mutagens. Mutat Res 526: 63–73.
- Weidhass JB,Angelichio EL,Fenner S,Coffin JM. 2000. Relationship between retroviral DNA integration and gene expression. J Virol 74: 8382–8389.
- Yauk CL,Quinn JS. 1996. Multilocus DNA fingerprinting reveals high rate of heritable genetic mutation in herring gulls nesting in an industrialized urban site. Proc Natl Acad Sci USA 93: 12137–12141.
- Yauk CL,Fox GA,McCarry BE,Quinn JS. 2000. Induced minisatellite germline mutations in herring gulls (Larus argentatus) living near steel mills. Mutat Res 452: 211–218.
- Yauk CL,Dubrova YE,Grant G,Jeffreys AJ. 2002. A novel single molecule analysis of spontaneous and radiation-induced mutation at a mouse tandem repeat locus. Mutat Res 500: 147–156.