Antioxidant capacity develops with maturation in the deep-diving hooded seal

Journal of Experimental Biology

Volumn 214, Issue 17, 2011, Pages 2903-2910

  Vázquez Medina, José Pablo ^a   Soñanez Organis, José Guadalupe ^a   Burns, Jennifer M ^b   Zenteno Savín, Tania ^c   Ortiz, Rudy M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF ALASKA ANCHORAGE   (United States)

^c CENTRO DE INVESTIGACIONES BIOLÓGICAS DEL NOROESTE   (Mexico)

Author keywords

Antioxidant; Ischemia; Maturation; Reperfusion; Seal

Indexed keywords

ANTIOXIDANT; CATALASE; GLUTAREDOXIN; GLUTATHIONE; GLUTATHIONE PEROXIDASE; PEROXIDE; THIOREDOXIN; THIOREDOXIN REDUCTASE; TRANSCRIPTION FACTOR NRF2;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; PHOCA; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ANIMALS; ANTIOXIDANTS; CATALASE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLUTAREDOXINS; GLUTATHIONE; GLUTATHIONE PEROXIDASE; MOLECULAR SEQUENCE DATA; NF-E2-RELATED FACTOR 2; PEROXIDES; SEALS, EARLESS; SEQUENCE ALIGNMENT; THIOREDOXIN-DISULFIDE REDUCTASE; THIOREDOXINS;

CYSTOPHORA (MAMMALIA); MAMMALIA;

EID: 80051719698     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.057935     Document Type: Article

References (46)

1. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. and Lipman, D. J. (1990). Basic local alignment search tool. J. Mol. Biol. 215, 403-410.
2. Arnér, E. S. J. and Holmgren, A. (2000). Physiological functions of thioredoxin and thioredoxin reductase. FEBS J. 267, 6102-6109.
3. Björnstedt, M., Xue, J., Huang, W., Akesson, B. and Holmgren, A. (1994). The thioredoxin and glutaredoxin systems are efficient electron donors to human plasma glutathione peroxidase. J. Biol. Chem. 269, 29382-29384. (Pubitemid 24365080)
4. Bloom, D. A. and Jaiswal, A. K. (2003). Phosphorylation of Nrf2 at Ser40 by protein kinase C in response to antioxidants leads to the release of Nrf2 from INrf2, but is not required for Nrf2 stabilization/accumulation in the nucleus and transcriptional activation of antioxidant response element-mediated NAD(P)H: quinine oxidoreductase-1 gene expression. J. Biol. Chem. 278, 44675-44682. (Pubitemid 37377224)
5. Bowen, W. D., Boness, D. J. and Oftedal, O. T. (1987). Mass transfer from mother to pup and subsequent mass loss by the weaned pup in the hooded seal, Cystophora cristata. Can. J. Zool. 65, 1-8.
6. Brown, J. M., Terada, L. S., Grosso, M. A., Whitmann, G. J., Velasco, S. E., Patt, A., Harken, A. H. and Repine, J. E. (1988). Xanthine oxidase produces hydrogen peroxide which contributes to reperfusion injury of ischemic, isolated, perfused rat hearts. J. Clin. Invest. 81, 1297-1301.
7. Burns, J., Lestyk, K., Folkow, L., Hammill, M. and Blix, A. (2007). Size and distribution of oxygen stores in harp and hooded seals from birth to maturity. J. Comp. Physiol. B 177, 687-700. (Pubitemid 47106434)
8. Burns, J., Skomp, N., Bishop, N., Lestyk, K. and Hammill, M. (2010). Development of aerobic and anaerobic metabolism in cardiac and skeletal muscles from harp and hooded seals. J. Exp. Biol. 213, 740-748.
9. Chan, K. and Kan, Y. W. (1999). Nrf2 is essential for protection against acute pulmonary injury in mice. Proc. Natl. Acad. Sci. USA 96, 12731-12736. (Pubitemid 29513571)
10. Cho, H. Y., Jedlicka, A. E., Reddy, S. P. M., Kensler, T. W., Yamamoto, M., Zhang, L. Y. and Kleeberger, S. R. (2002). Role of NRF2 in protection against hyperoxic lung injury in mice. Am. J. Respir. Cell Mol. Biol. 26, 175-182. (Pubitemid 34107870)
11. Chowdhury, I., Mo, Y., Gao, L., Kazi, A., Fisher, A. B. and Feinstein, S. I. (2009). Oxidant stress stimulates expression of the human peroxiredoxin 6 gene by a transcriptional mechanism involving an antioxidant response element. Free Radic. Biol. Med. 46, 146-153.
12. Elsner, R. (1999). Living in water: solutions to physiological problems. In Biology of Marine Mammals (ed. J. E. I. Reynolds and S. A. Rommel), pp. 73-116. Washington, DC: Smithsonian Institution Press.
13. Elsner, R., Øyasæter, S., Almaas, R. and Saugstad, O. D. (1998). Diving seals, ischemia-reperfusion and oxygen radicals. Comp. Biochem. Physiol. 119A, 975-980. (Pubitemid 28389209)
14. Fisher, A. B. (2011). Peroxiredoxin 6: a bifunctional enzyme with glutathione peroxidase and phospholipase A2 activities. Antioxid. Redox Signal. 15, 831-844.
15. Folkow, L. P. and Blix, A. S. (1999). Diving behaviour of hooded seals (Cystophora cristata) in the Greenland and Norwegian Seas. Polar Biol. 22, 61-74. (Pubitemid 29308093)
16. Folkow, L., Nordøy, E. and Blix, A. (2010). Remarkable development of diving performance and migrations of hooded seals (Cystophora cristata) during their first year of life. Polar Biol. 33, 433-441.
17. Furtado-Filho, O. V., Polcheira, C., Machado, D. P., Mourão, G. and Hermes-Lima, M. (2007). Selected oxidative stress markers in a South American crocodilian species. Comp. Biochem. Physiol. 146C, 241-254. (Pubitemid 47064524)
18. Griffith, O. W. (1980). Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal. Biochem. 106, 207-212. (Pubitemid 11246585)
19. Halliwell, B. and Gutteridge, J. (2007). Free Radicals in Biology and Medicine. New York: Oxford University Press.
20. Immenschuh, S. and Baumgart-Vogt, E. (2005). Peroxiredoxins, oxidative stress, and cell proliferation. Antioxid. Redox Signal. 7, 768-777. (Pubitemid 40563217)
21. Itoh, K., Chiba, T., Takahashi, S., Ishii, T., Igarashi, K., Katoh, Y., Oyake, T., Hayashi, N., Satoh, K. and Hatayama, I. (1997). An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem. Biophys. Res. Commun. 236, 313-322. (Pubitemid 27373291)
22. Jaiswal, A. K. (2004). Nrf2 signaling in coordinated activation of antioxidant gene expression. Free Radic. Biol. Med. 36, 1199-1207. (Pubitemid 38526313)
23. Kim, H. S., Pak, J. H., Gonzales, L. W., Feinstein, S. I. and Fisher, A. B. (2002). Regulation of 1-cys peroxiredoxin expression in lung epithelial cells. Am. J. Respir. Cell Mol. Biol. 27, 227-233. (Pubitemid 34780803)
24. Kobayashi, A., Kang, M. I., Okawa, H., Ohtsuji, M., Zenke, Y., Chiba, T., Igarashi, K. and Yamamoto, M. (2004). Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2. Mol. Cell. Biol. 24, 7130-7139. (Pubitemid 39014439)
25. Kobayashi, A., Kang, M. I., Watai, Y., Tong, K. I., Shibata, T., Uchida, K. and Yamamoto, M. (2006). Oxidative and electrophilic stresses activate Nrf2 through inhibition of ubiquitination activity of Keap1. Mol. Cell. Biol. 26, 221-229.
26. Kooyman, G. and Ponganis, P. (1998). The physiological basis of diving to depth: birds and mammals. Annu. Rev. Physiol. 60, 19-32. (Pubitemid 28157862)
27. Kuppusamy, P. and Zweier, J. (1989). Characterization of free radical generation by xanthine oxidase. Evidence for hydroxyl radical generation. J. Biol. Chem. 264, 9880-9884. (Pubitemid 19159252)
28. Lestyk, K., Folkow, L., Blix, A., Hammill, M. and Burns, J. (2009). Development of myoglobin concentration and acid buffering capacity in harp (Pagophilus groenlandicus) and hooded (Cystophora cristata) seals from birth to maturity. J. Comp. Physiol. B 179, 985-996.
29. McCord, J. (1985). Oxygen-derived free radicals in postischemic tissue injury. N. Engl. J. Med. 312, 159-163. (Pubitemid 15192863)
30. Meir, J. U., Champagne, C. D., Costa, D. P., Williams, C. L. and Ponganis, P. J. (2009). Extreme hypoxemic tolerance and blood oxygen depletion in diving elephant seals. Am. J. Physiol. Regul. Integr. Comp. Physiol. 297, R927-R929.
31. Murphy, B. J. and Hochachka, P. W. (1981). Free amino acid profiles in blood during diving and recovery in the Antarctic Weddell seal. Can. J. Zool. 59, 455-459.
32. Prestera, T. and Talalay, P. (1995). Electrophile and antioxidant regulation of enzymes that detoxify carcinogens. Proc. Natl. Acad. Sci. USA 92, 8965-8969.
33. Sambrook, J. and Russell, D. W. (2001). Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
34. Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680. (Pubitemid 24354800)
35. Thompson-Gorman, S. L. and Zweier, J. L. (1990). Evaluation of the role of xanthine oxidase in myocardial reperfusion injury. J. Biol. Chem. 265, 6656-6663.
36. Valdivia, P. A., Zenteno-Savín, T., Gardner, S. C. and Alonso Aguirre, A. (2007). Basic oxidative stress metabolites in eastern Pacific green turtles (Chelonia mydas agassizii). Comp. Biochem. Physiol. 146C, 111-117. (Pubitemid 47064521)
37. Vázquez-Medina, J. P., Zenteno-Savín, T. and Elsner, R. (2006). Antioxidant enzymes in ringed seal tissues: potential protection against dive-associated ischemia/reperfusion. Comp. Biochem. Physiol. 142C, 198-204.
38. Vázquez-Medina, J. P., Zenteno-Savín, T. and Elsner, R. (2007). Glutathione protection against dive-associated ischemia/reperfusion in ringed seal tissues. J. Exp. Mar. Biol. Ecol. 345, 110-118. (Pubitemid 46680329)
39. Vázquez-Medina, J. P., Crocker, D. E., Forman, H. J. and Ortiz, R. M. (2010). Prolonged fasting does not increase oxidative damage or inflammation in postweaned northern elephant seal pups. J. Exp. Biol. 213, 2524-2530.
40. Vázquez-Medina, J. P., Olguín-Monroy, N. O., Maldonado, P. D., Santamaría, A., Königsberg, M., Elsner, R., Hammilll, M. O., Burns, J. M. and Zenteno-Savín, T. (2011a). Maturarion increases superoxide radical production without increasing oxidative damage in the skeletal muscle of hooded seals (Cystophora cristata). Can. J. Zool. 89, 206-212.
41. Vázquez-Medina, J. P., Zenteno-Savín, T., Crocker, D. E., Forman, H. J. and Ortiz, R. M. (2011b). Prolonged fasting increases glutathione biosynthesis in postweaned northern elephant seals. J. Exp. Biol. 14, 1294-1299.
42. Wilhelm Filho, D., Sell, F., Ribeiro, L., Ghislandi, M., Carrasquedo, F., Fraga, C. G., Wallauer, J. P., Simões-Lopes, P. C. and Uhart, M. M. (2002). Comparison between the antioxidant status of terrestrial and diving mammals. Comp. Biochem. Physiol. 133A, 885-892. (Pubitemid 35351481)
43. Yang, H., Magilnick, N., Lee, C., Kalmaz, D., Ou, X., Chan, J. Y. and Lu, S. C. (2005). Nrf1 and Nrf2 regulate rat glutamate-cysteine ligase catalytic subunit transcription indirectly via NF-κB and AP-1. Mol. Cell. Biol. 25, 5933-5946. (Pubitemid 40949988)
44. Zenteno-Savín, T., Clayton-Hernandez, E. and Elsner, R. (2002). Diving seals: are they a model for coping with oxidative stress? Comp. Biochem. Physiol. 133C, 527-536. (Pubitemid 35373944)
45. Zenteno-Savín, T., St Leger, J. and Ponganis, P. J. (2010). Hypoxemic and ischemic tolerance in emperor penguins. Comp. Biochem. Physiol. 152C, 18-23.
46. Zhang, D. D. and Hannink, M. (2003). Distinct cysteine residues in Keap1 are required for Keap1-dependent ubiquitination of Nrf2 and for stabilization of Nrf2 by chemopreventive agents and oxidative stress. Mol. Cell. Biol. 23, 8137-8151. (Pubitemid 37377505)