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Modulation of Specific Apoptotic DNA Fragmentation after Short Term Exposure to Natural UVR in Fish Larvae

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DOI: 10.4236/ojapo.2014.33005    2,545 Downloads   3,220 Views   Citations

ABSTRACT

The goal of this study was to determine the short-term effects of the quality (UV-A/UV-B ratio) and quantity (irradiance) of natural ultraviolet radiation (UVR) on the apoptosis levels in Yellow perch (Perca flavescens) larvae. Apoptosis, or programmed cell death, is an essential event in many physiological processes as well as in pathological conditions. Western blots were used to measure the expression of several key proteins of the apoptotic cascade, such as p53, Bax, Bcl-2, and PARP-1, whereas specific apoptotic DNA fragmentation was measured by an ELISA assay. We predicted that higher UVR exposure would be related to higher levels of apoptosis. Our results showed that specific apoptotic DNA fragmentation was reduced by visible light + UV-A as well as by visible light + UV-A and UV-B treatments although it was not significantly affected by light quantity. However, the expression of p53, Bax/Bcl-2 ratio and PARP-1 were not significantly affected in larvae by the quantity or the quality of the light after two days of exposure. Altogether our results suggest that UVR may modulate the apoptotic process in Yellow perch larvae proposing an interesting role for this stressor on the early development of living organism under natural exposure condition.

Conflicts of Interest

The authors declare no conflicts of interest.

Cite this paper

Provencher, C. , Bertolo, A. , Magnan, P. and Martinoli, M. (2014) Modulation of Specific Apoptotic DNA Fragmentation after Short Term Exposure to Natural UVR in Fish Larvae. Open Journal of Apoptosis, 3, 39-51. doi: 10.4236/ojapo.2014.33005.

References

[1] Williamson, C.E. (1995) What Role Does UV-B Radiation Play in Fresh-Water Ecosystems. Limnology and Oceanography, 40, 386-392. http://dx.doi.org/10.4319/lo.1995.40.2.0386
[2] Bancroft, B.A., Baker, N.J. and Blaustein, A.R. (2007) Effects of UVB Radiation on Marine and Freshwater Organisms: A Synthesis through Meta-Analysis. Ecology Letters, 10, 332-345.
http://dx.doi.org/10.1111/j.1461-0248.2007.01022.x
[3] Hunter, R.J., Taylor, J.H. and Moser, G.H. (1979) Effects of Ultraviolet Radiation on Eggs and Larvae of the Northern Anchovy, Engraulis mordax, and the Pacific Mackarel, Scomber japonicus, during Embryonic Stage. Photochemistry and Photobiology, 29, 325-338.
http://dx.doi.org/10.1111/j.1751-1097.1979.tb07055.x
[4] Cadet, J., Sage, E. and Douki, T. (2005) Ultraviolet Radiation-Mediated Damage to Cellular DNA. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, 571, 3-17.
http://dx.doi.org/10.1016/j.mrfmmm.2004.09.012
[5] Malloy, K.D., Holman, M.A., Mitchell, D. and Detrich, H.W. (1997) Solar UVB-Induced DNA Damage and Photoenzymatic DNA Repair in Antarctic Zooplankton. Proceedings of the National Academy of Sciences of the United States of America, 94, 1258-1263. http://dx.doi.org/10.1073/pnas.94.4.1258
[6] Zeng, Z., Richardson, J., Verduzco, D., Mitchell, D.L. and Patton, E.E. (2009) Zebrafish Have a Competent p53-Dependent Nucleotide Excision Repair Pathway to Resolve Ultraviolet B-Induced DNA Damage in the Skin. Zebrafish, 6, 405-415. http://dx.doi.org/10.1089/zeb.2009.0611
[7] Lesser, M.P., Farrell, J.H. and Walker, C.W. (2001) Oxidative Stress, DNA Damage and p53 Expression in the Larvae of Atlantic Cod (Gadus morhua) Exposed to Ultraviolet (290 - 400 nm) Radiation. The Journal of Experimental Biology, 204, 157-164.
[8] Gewies, A. (2003) Introduction to Apoptosis. ApoReview, 1-26.
[9] Batista, L.F., Kaina, B., Meneghini, R. and Menck, C.F. (2009) How DNA Lesions Are Turned into Powerful Killing Structures: Insights from UV-Induced Apoptosis. Mutation Research/Reviews in Mutation Research, 681, 197-208. http://dx.doi.org/10.1016/j.mrrev.2008.09.001
[10] Krumschnabel, G. and Podrabsky J.E. (2009) Fish as a Model System for the Study of Vertebrate Apoptosis. Apoptosis, 14, 1-21. http://dx.doi.org/10.1007/s10495-008-0281-y
[11] Greenwood, J. and Gautier, J. (2005) From Oogenesis through Gastrulation: Developmental Regulation of Apoptosis. Seminars in Cell & Developmental Biology, 16, 215-224.
http://dx.doi.org/10.1016/j.semcdb.2004.12.002
[12] Penaloza, C., Lin, L., Lockshin, R.A. and Zakeri, Z. (2006) Cell Death in Development: Shaping the Embryo. Histochemistry and Cell Biology, 126, 149-158. http://dx.doi.org/10.1007/s00418-006-0214-1
[13] Eimon, P.M. and Ashkenazi, A. (2010) The Zebrafish as a Model Organism for the Study of Apoptosis. Apoptosis, 15, 331-349. http://dx.doi.org/10.1007/s10495-009-0432-9
[14] Douki, T., Reynaud-Angelin, A., Cadet, J., Sage, E. (2003) Bipyrimidine Photoproducts Rather than Oxidative Lesions Are the Main Type of DNA Damage Involved in the Genotoxic Effect of Solar UVA Radiation. Biochemistry, 42, 9221-9226. http://dx.doi.org/10.1021/bi034593c
[15] Mitani, H., Uchida, N. and Shima, A. (1996) Induction of Cyclobutane Pyrimidine Dimer Photolyase in Cultured Fish Cells by UVA and Blue Light. Photochemistry and Photobiology, 64, 943-948.
http://dx.doi.org/10.1111/j.1751-1097.1996.tb01859.x
[16] Rochette, P.J., Therrien, J.P., Drouin, R., Perdiz, D., Bastien, N., Drobetsky, E.A. and Sage, E. (2003) UVA-Induced Cyclobutane Pyrimidine Dimers Form Predominantly at Thymine-Thymine Dipyrimidines and Correlate with the Mutation Spectrum in Rodent Cells. Nucleic Acids Research, 31, 2786-2794. http://dx.doi.org/10.1093/nar/gkg402
[17] Sage, E., Drouin, R. and Rouabhia, M. (2005) From DNA Photolesions to Mutations, Skin Cancer and Cell Death. RSC (Comprehensive Series in Photochemical & Photobiological Series) RSC Publishing, London. http://dx.doi.org/10.1039/9781847552501
[18] Monaghan, P. (2009) Oxidative Stress as a Mediator of Life History Trade-Offs: Mechanisms, Measurements and Interpretation. Ecology Letters, 12, 75-92.
http://dx.doi.org/10.1111/j.1461-0248.2008.01258.x
[19] Friedberg, E.C. (2003) DNA Damage and Repair. Nature. 421, 436-440.
http://dx.doi.org/10.1038/nature01408
[20] Häkkinen, J. and Oikari, A. (2004) A Field Methodology to Study Effects of UV Radiation on Fish Larvae. Water Research, 38, 2891-2897. http://dx.doi.org/10.1016/j.watres.2004.04.004
[21] Dahms, H.U. and Lee, J.S. (2010) UV Radiation in Marine Ectotherms: Molecular Effects and Responses. Aquatic Toxicology, 97, 3-14. http://dx.doi.org/10.1016/j.aquatox.2009.12.002
[22] Béland, F., Browman, H.I., Rodriguez, C.A. and St-Pierre, J.F. (1999) Effect of Solar Ultraviolet Radiation (280 - 400 nm) on the Eggs and Larvae of Atlantic Cod (Gadus morhua). Canadian Journal of Fisheries and Aquatic Sciences, 56, 1058-1067.
[23] Boily, V., Bertolo, A., Magnan, P., Martinoli, M.G. and Thérien, H.M. (2011) The Effects of UVR Irradiance and Spectral Composition on Yellow Perch (Perca flavescens) Larvae Survival. Aquatic Sciences, 73, 345-354. http://dx.doi.org/10.1007/s00027-011-0182-y
[24] Williamson, C.E., Metgar, S.L., Lovera, P.A. and Moeller, R.E. (1997) Solar Ultraviolet Radiation and the Spawning Habitat of Yellow Perch, Perca Flavescens. Ecological Applications, 7, 1017-1023
http://dx.doi.org/10.1890/1051-0761(1997)007[1017:SURATS]2.0.CO;2
[25] Huggins, K., Frenette, J.J. and Arts, M.T. (2004) Nutritional Quality of Biofilms with Respect to Light Regime in Lake Saint-Pierre (Québec, Canada). Freshwater Biology, 49, 945-959.
http://dx.doi.org/10.1111/j.1365-2427.2004.01236.x
[26] Bournival, J., Francoeur, M.A., Renaud, J. and Martinoli, M.G. (2012) Quercetin and Sesamin Protect Neuronal PC12 Cells from High-Glucose-Induced Oxidation, Nitrosative Stress and Apoptosis. Rejuvenation Research, 15, 322-333. http://dx.doi.org/10.1089/rej.2011.1242
[27] Frankfurt, O.S. and Krishan, A. (2001) Enzyme-Linked Immunosorbent Assay (ELISA) for the Specific Detection of Apoptotic Cells and Its Application to Rapid Drug Screening. Journal of Immunological Methods, 253, 133-144. http://dx.doi.org/10.1016/S0022-1759(01)00387-8
[28] Haan, C. and Behrmann, I. (2007) A Cost Effective Non-Commercial ECL-Solution for Western Blot Detections Yielding Strong Signals and Low Background. Journal of Immunological Methods, 318, 11-19. http://dx.doi.org/10.1016/j.jim.2006.07.027
[29] Burnham, K.P. and Anderson, D.R. (2002) Model Selection and Multimodel Inference: A Practical Information- Theoretic Approach. Springer-Verlag, New York.
[30] Zuur, A.F., Ieno, E.N., Walker, N.J., Saveliev, A.A. and Smith, G.M. (2009) Mixed Effects Modelling for Nested Data. In: Mixed Effects Models and Extensions in Ecology with R., Vol. 65, Springer, New York, 101-142.
[31] Deschênes, J. and Rodriguez, M.A. (2007) Hierarchical Analysis of Relationships between Brook Trout (Salvelinus fontinalis) Density and Stream Habitat Features. Canadian Journal of Fisheries and Aquatic Sciences, 64, 777-785. http://dx.doi.org/10.1139/f07-053
[32] Carange, J., Longpré, F., Daoust, B. and Martinoli, M.G. (2011) 24-Epibrassinolide, a Phytosterol from the Brassinosteroid Family, Protects Dopaminergic Cells against MPP+-Induced Oxidative Stress and Apoptosis. Journal of Toxicology, 2011, Article ID: 392859, 13 pages.
[33] Bounival, J., Plouffe, M., Renaud, J., Provencher, C. and Martinoli, M.G. (2012) Quercetin and Sesamin Protect Dopaminegic Cells from MPP+-Induced Neuroinflammation in a Microglial (N9)-Neuronal (PC12) Coculture System. Oxidative Medicine and Cellular Longevity, 2012, Article ID: 921941, 11 pages. http://dx.doi.org/10.1155/2012/921941
[34] Macip, S., Igarashi, M., Berggren, P., Yu, J., Lee, S.W. and Aaronson, S.A. (2003) Influence of Induced Reactive Oxygen Species in p53-Mediated Cell Fate Decision. Molecular and Cellular Biology, 23, 8576-8585. http://dx.doi.org/10.1128/MCB.23.23.8576-8585.2003
[35] Cory, S. and Adams, J.M. (2002) The Bcl2 Family: Regulators of the Cellular Life-or-Death Switch. Nature Reviews Cancer, 2, 647-656. http://dx.doi.org/10.1038/nrc883
[36] Olson, M.H., Colip, M.R., Gerlach, J.S. and Mitchell, D.L. (2006) Quantifying Ultraviolet Radiation Mortality in Bluegill Larvae: Effects of Nest Location. Ecological Applications, 16, 328-338.
http://dx.doi.org/10.1890/05-0287
[37] Aranda, M., Banaszak, A.T., Bayer, T., Luyten, J.R., Medina, M. and Voolstra, C.R. (2011) Differential Sensitivity of Coral Larvae to Natural Levels of Ultraviolet Radiation during Onset of Larval Competence. Molecular Ecology, 20, 2955-2972. http://dx.doi.org/10.1111/j.1365-294X.2011.05153.x
[38] Gollapudi, S., McCormick, M.J. and Gupta, S. (2003) Changes in Mitochondrial Membrane Potential and Mitochondrial Mass Occur Independent of the Activation of Caspase-8 and Caspase-3 during CD95-Mediated Apoptosis in Peripheral Blood T Cells. International Journal of Oncology, 22, 597-600.
[39] Tsujimoto, Y. and Shimizu, S. (2000) VDAC Regulation by the Bcl-2 Family of Proteins. Cell Death & Differentiation, 7, 1174-1181. http://dx.doi.org/10.1038/sj.cdd.4400780
[40] Kang, M.H. and Reynolds, C.P. (2009) Bcl-2 Inhibitors: Targeting Mitochondrial Apoptotic Pathways in Cancer Therapy. Clinical Cancer Research, 15, 1126-1132.
http://dx.doi.org/10.1158/1078-0432.CCR-08-0144
[41] Wang, Z., Wang, F., Tang, T. and Guo, C. (2012) The Role of PARP1 in the DNA Damage Response and Its Application in Tumor Therapy. Frontiers of Medicine, 6, 156-164.
http://dx.doi.org/10.1007/s11684-012-0197-3
[42] Virág, L., Robaszkiewicz, A., Vargas, J.M. and Oliver, J.F. (2013) Poly(ADP-ribose) Signaling in Cell Death. Molecular Aspects of Medicine, 34, 1153-1167.
[43] Bivik, C.A., Larsson, P.K., Kagedal, K.M., Rosdahl, I.K. and Ollinger, K.M. (2006) UVA/B-Induced Apoptosis in Human Melanocytes Involves Translocation of Cathepsins and Bcl-2 Family Members. Journal of Investigative Dermatology, 126, 1119-1127. http://dx.doi.org/10.1038/sj.jid.5700124
[44] Sitailo, L.A., Tibudan, S.S. and Denning, M.F. (2002) Activation of Caspase-9 Is Required for UV-Induced Apoptosis of Human Keratinocytes. Journal of Biological Chemistry, 277, 19346-19352.
http://dx.doi.org/10.1074/jbc.M200401200
[45] Timares, L., Katiyar, S.K. and Elmets, C.A. (2008) DNA Damage, Apoptosis and Langerhans Cells—Activators of UV-Induced Immune Tolerance. Photochemistry and Photobiology, 84, 422-436.
http://dx.doi.org/10.1111/j.1751-1097.2007.00284.x
[46] Lee, K.C., Goh, W.L., Xu, M., Kua, N., Lunny, D., Wong, J.S., Coomber, D., Vojtesek, B., Lane, E.B. and Lane, D.P. (2008) Detection of the p53 Response in Zebrafish Embryos Using New Monoclonal Antibodies. Oncogene, 27, 629- 640. http://dx.doi.org/10.1038/sj.onc.1210695
[47] Lesser, M.P., Kruse, V.A. and Barry, T.M. (2003) Exposure to Ultraviolet Radiation Causes Apoptosis in Developing Sea Urchin Embryos. Journal of Experimental Biology, 206, 4097-4103.
http://dx.doi.org/10.1242/jeb.00621
[48] Hildesheim, J. and Fornace Jr., A.J. (2004) The Dark Side of Light: The Damaging Effects of UV Rays and the Protective Efforts of MAP Kinase Signaling in the Epidermis. DNA Repair, 3, 567-580.
http://dx.doi.org/10.1016/j.dnarep.2004.02.012
[49] Kulms, D., Poppelmann, B., Yarosh, D., Luger, T.A., Krutmann, J. and Schwarz, T. (1999) Nuclear and Cell Membrane Effects Contribute Independently to the Induction of Apoptosis in Human Cells Exposed to UVB Radiation. Proceedings of the National Academy of Sciences of the United States of America, 96, 7974-7979. http://dx.doi.org/10.1073/pnas.96.14.7974
[50] Yabu, T., Todoriki, S. and Yamashita, M. (2001) Stress-Induced Apoptosis by Heat Shock, UV and Gamma-Ray Irradiation in Zebrafish Embryos Detected by Increased Caspase Activity and Whole-Mount TUNEL Staining. Fisheries Science, 67, 333-340. http://dx.doi.org/10.1046/j.1444-2906.2001.00233.x
[51] Vetter, R.D., Kurtzman, A. and Mori, T. (1999) Diel Cycles of DNA Damage and Repair in Eggs and Larvae of Northern Anchovy, Engraulis mordax, Exposed to Solar Ultraviolet Radiation. Photochemistry and Photobiology, 69, 27-33. http://dx.doi.org/10.1111/j.1751-1097.1999.tb05302.x
[52] Karentz, D., Bosch, I. and Mitchell, D.M. (2004) Limited Effects of Antarctic Ozone Depletion on Sea Urchin Development. Marine Biology, 145, 277-292. http://dx.doi.org/10.1007/s00227-004-1310-1
[53] Bonaventura, R., Poma, V., Costa, C. and Matranga, V. (2005) UVB Radiation Prevents Skeleton Growth and Stimulates the Expression of Stress Markers in Sea Urchin Embryos. Biochemical and Biophysical Research Communications, 328, 150-157. http://dx.doi.org/10.1016/j.bbrc.2004.12.161

  
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