Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-14T11:32:52.291Z Has data issue: false hasContentIssue false
  • English
  • Français

Parasite-induced oxidative stress in liver tissue of fathead minnows exposed to trematode cercariae

Published online by Cambridge University Press:  16 August 2012

A. D. STUMBO ,
C. P. GOATER  and
A. HONTELA
A. D. STUMBO*
Affiliation:
Department of Biological Sciences, Water Institute for Sustainable Environments (WISE), University of Lethbridge, 4401 University Drive West, Lethbridge, AB, CanadaT1 K 3M4
C. P. GOATER
Affiliation:
Department of Biological Sciences, Water Institute for Sustainable Environments (WISE), University of Lethbridge, 4401 University Drive West, Lethbridge, AB, CanadaT1 K 3M4
A. HONTELA
Affiliation:
Department of Biological Sciences, Water Institute for Sustainable Environments (WISE), University of Lethbridge, 4401 University Drive West, Lethbridge, AB, CanadaT1 K 3M4
*
*Corresponding author: Tel:+403 329 2319. E-mail:anthony.stumbo@uleth.ca
Get access Rights & Permissions [Opens in a new window]

Summary

Although results from field surveys have linked parasites to oxidative stress in their fish hosts, direct evidence involving experimentally infected hosts is lacking. We evaluated the effects of experimental infections with larval trematodes on induction of oxidative stress in fathead minnows, Pimephales promelas. Juvenile fish were exposed in the laboratory to the larvae (cercariae) of 2 species of trematode: Ornithodiplostomum sp. that develops in the liver, and O. ptychocheilus that develops in the brain. For Ornithodiplostomum sp., lipid peroxidation concentration in liver tissue increased 5 days after exposure and remained higher than controls until the end of the experiment at 28 days. For O. ptychocheilus, liver lipid peroxidation concentration was higher than controls at 5 days, but not thereafter. Sustained elevation in lipid peroxidation concentration for the liver trematode may be explained by direct tissue damage caused by developing larvae in the liver, or by an immune response. These experimental results support those from field studies, indicating that the lipid peroxidation assay may be an effective biomonitor for parasite-induced oxidative stress in fish, and that the nature of the oxidative stress response is species and/or tissue specific.

Keywords

lipid peroxidationmetacercariaePimephales promelas
Type
Research Article
Information
Parasitology , Volume 139 , Issue 12 , October 2012 , pp. 1666 - 1671
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Allen, P. C. and Fetterer, R. H. (2002). Recent advances in biology and immunobiology of Eimeria species and in diagnosis and control of infection with these coccidian parasites of poultry. Clinical Microbiology Reviews 15, 58–65.CrossRefGoogle ScholarPubMed
Belló, A. R., Belló-Klein, A., Belló, A. A., Llesuy, S. F., Robaldo, R. B. and Bianchini, A. (2000). Lipid peroxidation induced by Clinostomum detruncatum in muscle of the freshwater fish Rhamdia quelen. Diseases of Aquatic Organisms 42, 233–236.CrossRefGoogle ScholarPubMed
Conn, D. B., Goater, C. P. and Bray, D. (2008). Developmental and functional ultrastructure of Ornithodiplostomum ptychocheilus diplostomula (Trematoda: Strigeoidea) during invasion of the brain of the fish intermediate host, Pimephales promelas. Journal of Parasitology 94, 635–642.CrossRefGoogle ScholarPubMed
Dautremepuits, C., Betoulle, S. and Vernet, G. (2003). Stimulation of antioxidant enzymes levels in carp (Cyrinus carpio L.) infected by Ptychobothrium sp. (Cestoda). Fish and Shellfish Immunology 15, 467–471.CrossRefGoogle Scholar
Di Giulio, R. T., Washburn, P. C., Wenning, R. J., Winston, G. W. and Jewell, C. S. (1989). Biochemical responses in aquatic animals: a review of determinants of oxidative stress. Environmental Toxicology and Chemistry 8, 1103–1123.CrossRefGoogle Scholar
Esterbauer, H., Schaur, R. J. and Zollner, H. (1991). Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radical Biology and Medicine 11, 81–128.CrossRefGoogle ScholarPubMed
James, C. T., Noyes, K. J., Stumbo, A. D., Wisenden, B. D. and Goater, C. P. (2008). Cost of exposure to trematode cercariae and learned recognition and avoidance of parasite risk by fathead minnows. Journal of Fish Biology 73, 2238–2248.CrossRefGoogle Scholar
Jacobson, K. C., Arkoosh, M. R., Kagley, A. N., Clemons, E. R., Collier, T. K. and Casillas, E. (2003). Cumulative effects of natural and anthropogenic stress on immune function and disease resistance in juvenile chinook salmon. Journal of Aquatic Animal Health 15, 1–12.2.0.CO;2>CrossRefGoogle Scholar
Kelly, S., Havrilla, C., Brady, T., Abramo, K. H. and Levin, E. (1998). Oxidative stress in toxicology: established mammalian and emerging piscine model systems. Environmental Health Perspectives 106, 375–84.CrossRefGoogle ScholarPubMed
Kurtz, J., Wegner, K. M., Kalbe, M., Reusch, T. B. H., Schaschl, J., Hasseiquist, D. and Milinski, M. (2006). MHC genes and oxidative stress in sticklebacks: an immuno-ecological approach. Proceedings of the Royal Society of London, B 273, 1407–1414.Google ScholarPubMed
Marcogliese, D., Brambilla, L. G., Gagne, F. and Gendron, A. D. (2005). Joint effects of parasitism and pollution on oxidative stress biomarkers in yellow perch Perca flavescens. Diseases of Aquatic Organisms 63, 77–84.CrossRefGoogle ScholarPubMed
Marcogliese, D. J. and Pietrock, M. (2011). Combined effects of parasites and contaminants on animal health: parasites do matter. Trends in Parasitology 27, 123–130.CrossRefGoogle ScholarPubMed
Matisz, C. E. and Goater, C. P. (2010). Migration, site selection and development of Ornithodiplostomum sp. metacercariae (Digenea: Strigeoidea) in fathead minnows (Pimephales promelas). International Journal for Parasitology 40, 1489–1496.CrossRefGoogle ScholarPubMed
Matisz, C. E., Goater, C. P. and Bray, D. (2010). Migration and site selection of Ornithodiplostomum ptychocheilus (Trematoda: Digenea) metacercariae in the brain of fathead minnows (Pimephales promelas). Parasitology 137, 719–731.CrossRefGoogle ScholarPubMed
Miller, L. L., Wang, F., Palace, V. P. and Hontela, A. (2007). Effects of acute and subchronic exposures to waterborne selenite on the physiological stress response and oxidative stress indicators in juvenile rainbow trout. Aquatic Toxicology 83, 263–271.CrossRefGoogle ScholarPubMed
Muscatello, J. R., Bennett, P. M., Himbeault, K. T., Belknap, A. M., Janz, D. M. (2006). Larval deformities associated with selenium accumulation in northern pike (Esox lucius) exposed to metal mining effluent. Environmental Science and Technology 40, 6506–6512.CrossRefGoogle ScholarPubMed
Muñoz, P., Calduch-Giner, J. A., Sitja-Bobadilla, A., Alvarez-Pellitero, P. and Perez- Sanchez, J. (1998). Modulation of the respiratory burst activity of Mediterranean sea bass (Dicentrarchus labrax L.) phagocytes by growth hormone and parasitic status. Fish and Shellfish Immunology 8, 25–36.CrossRefGoogle Scholar
Oost, R. v. d., Beyer, J. and Vermeulen, N. P. E. (2003). Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environmental Toxicology and Pharmacology 13, 57–149.CrossRefGoogle ScholarPubMed
Palmer, H. and Paulson, K. E. (1997). Reactive oxygen species and antioxidants in signal transduction and gene expression. Nutrition Reviews 55, 353–361.CrossRefGoogle ScholarPubMed
Sandland, G. J. and Goater, C. P. (2000). Development and intensity-dependence of Ornithodiplostomum ptychocheilus metacercariae in fathead minnows (Pimephales promelas). Journal of Parasitology 86, 1056–1060.CrossRefGoogle ScholarPubMed
Sandland, G. J. and Goater, C. P. (2001). Parasite-induced variation in host morphology: brain-encysting trematodes in fathead minnows. Journal of Parasitology 87, 267–272.CrossRefGoogle ScholarPubMed
Sandland, G. J., Goater, C. P. and Danylchuk, A. (2001). Population dynamics of Ornithodiplostomum ptychocheilus metacercariae in fathead minnows (Pimephales promelas) from 4 northern-Alberta lakes. Journal of Parasitology 87, 744–748.CrossRefGoogle ScholarPubMed
Scharsack, J. P., Kalbe, M., Harrod, C. and Rauch, G. (2007). Habitat-specific adaptation of immune responses of stickleback (Gasterosteus aculeatus) lake and river ecotypes. Proceedings of the Royal Society of London 274, 1523–1532.Google ScholarPubMed
Shirakashi, S. and Goater, C. P. (2005). Chronology of parasite-induced alteration of fish behaviour: effects of parasite maturation and host experience. Parasitology 130, 177–183.CrossRefGoogle ScholarPubMed
Spallholz, J. E., Palace, V. P. and Reid, T. W. (2004). Methioninase and selenomethionine but not Se-methylselenocysteine generate methylselenol and superoxide in an in vitro chemiluminescent assay: implications for the nutritional carcinostatic activity of selenoamino acids. Biochemical Pharmacology 67, 547–554.CrossRefGoogle ScholarPubMed
Spector, A. (2000). Review: Oxidative stress and disease. Journal of Ocular Pharmacology and Therapeutics 16, 193–201.CrossRefGoogle ScholarPubMed
Stables, J. N. and Chappell, L. H. (1986). The epidemiology of diplostomiasis in farmed rainbow trout from north-east Scotland. Parasitology 92, 699–710.CrossRefGoogle ScholarPubMed
Toyokuni, S. (2002). Reactive oxygen species-induced molecular damage and its application in pathology. Pathology International 49, 91–102.CrossRefGoogle Scholar
Velkova-Jordanoska, L. and Kostoski, G. (2005). Histopathological analysis of liver in fish (Barbus meridionalis petenyi Heckel) in reservoir Trebenista. Croatian Natural History Museum 14, 147–53.Google Scholar
Wang, D., Malo, D. and Hekimi, S. (2010). Elevated mitochondrial reactive oxygen species generation affects the immune response via hypoxia-inducible factor-1α in long-lived Mclk1+/− mouse mutants. The Journal of Immunology 184, 582–590.CrossRefGoogle ScholarPubMed
Whyte, S. K., Chappell, L. H. and Secombes, C. J. (1990). Protection of rainbow trout, Oncorhynchus mykiss (Richardson), against Diplostomum spathaceum (Digenea): the role of specific antibody and activated macrophages. Journal of Fish Diseases 13, 281–291.CrossRefGoogle Scholar
Wilson, M. E., Andersen, K. A. and Britigan, B. E. (1994). Responses of Leishmania chagasi promastigotes to oxidant stress. Infection and Immunity 62, 5133–5141.CrossRefGoogle ScholarPubMed