Diving seals, ischemia-reperfusion and oxygen radicals

Elsner, Robert; Øyasæter, Stephanie; Almaas, Runar; Saugstad, Ola Didrik

doi:10.1016/s1095-6433(98)00012-9

Cited by 69 publications

(52 citation statements)

References 21 publications

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“…The present study shows that repetitive exposure to breathholds in seals increases muscle XO protein expression along with an increase in Nrf2 nuclear content, SOD1 and catalase protein expression, without increasing muscle NT or circulating 8-isoPGF 2 , HNE, NT or protein carbonyls, suggesting that XO-derived oxidant production does not induce oxidative damage, and rather contributes to the activation of the protective response against oxidative stress. The latter is consistent with the observed increases in plasma xanthine, HX and XO activity at the end of the apneas and during recovery, with the previously reported increases in HX after ex vivo exposure to ischemia in seal heart and kidney (Elsner et al, 1998), and with the increased content of muscle HNE after repetitive apneas, as HNE also contributes to the activation of the Nrf2-mediated oxidative stress response (Siow et al, 2007;Tanito et al, 2007). Nrf2 induces the transcription of genes involved in antioxidant defense such as SOD1 and catalase (Immenschuh and BaumgartVogt, 2005;Jaiswal, 2004).…”

Section: Eupneasupporting

confidence: 92%

“…lipid peroxidation and protein carbonyls) in their tissues or red blood cells (RBCs) in comparison with terrestrial mammals (Vázquez-Medina et al, 2007;Wilhelm Filho et al, 2002;ZentenoSavín et al, 2002). Interestingly, seal tissues do accumulate HX after ex vivo exposure to ischemia (Elsner et al, 1998). Moreover, basal capacity to produce O 2…”

Section: Introductionmentioning

confidence: 99%

“…Apnea in seals is characterized by a series cardiovascular adjustments (reduction in cardiac output, bradycardia, peripheral vasoconstriction) that allow seals to maximize the use of their oxygen stores but at the same time result in blood oxygen depletion and blood flow redistribution towards obligatory oxygendependent tissues, exposing seals to critical levels of ischemia and hypoxemia (Castellini et al, 1994;Elsner, 1999;Kooyman and Ponganis, 1998;Stockard et al, 2007). At the end of an apnea bout, an increase in cardiac output and ventilation restores blood flow to tissues and blood oxygen content, presenting seals with potential increases in oxidant production and oxidative stress (Elsner et al, 1998;Zenteno-Savín et al, 2002).…”

Section: Introductionmentioning

confidence: 99%

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Apnea stimulates the adaptive response to oxidative stress in elephant seal pups

Vázquez‐Medina

Zenteno‐Savín

Tift

et al. 2011

Journal of Experimental Biology

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SUMMARYExtended breath-hold (apnea) bouts are routine during diving and sleeping in seals. These apneas result in oxygen store depletion and blood flow redistribution towards obligatory oxygen-dependent tissues, exposing seals to critical levels of ischemia and hypoxemia. The subsequent reperfusion/reoxygenation has the potential to increase oxidant production and thus oxidative stress. The contributions of extended apnea to oxidative stress in adapted mammals are not well defined. To address the hypothesis that apnea in seals is not associated with increased oxidative damage, blood samples were collected from northern elephant seal pups (N6) during eupnea, rest-and voluntary submersion-associated apneas, and post-apnea (recovery). Plasma 4-hydroxynonenal (HNE), 8-isoprostanes (8-isoPGF 2 ), nitrotyrosine (NT), protein carbonyls, xanthine and hypoxanthine (HX) levels, along with xanthine oxidase (XO) activity, were measured. Protein content of XO, superoxide dismutase 1 (Cu,ZnSOD), catalase and myoglobin (Mb), as well as the nuclear content of hypoxia inducible factor 1 (HIF-1) and NF-E2-related factor 2 (Nrf2), were measured in muscle biopsies collected before and after the breath-hold trials. HNE, 8-iso PGF 2 , NT and protein carbonyl levels did not change among eupnea, apnea or recovery. XO activity and HX and xanthine concentrations were increased at the end of the apneas and during recovery. Muscle protein content of XO, CuZnSOD, catalase, Mb, HIF-1 and Nrf2 increased 25-70% after apnea. Results suggest that rather than inducing the damaging effects of hypoxemia and ischemia/reperfusion that have been reported in non-diving mammals, apnea in seals stimulates the oxidative stress and hypoxic hormetic responses, allowing these mammals to cope with the potentially detrimental effects associated with this condition.

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Section: Eupneasupporting

confidence: 92%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Apnea stimulates the adaptive response to oxidative stress in elephant seal pups

Vázquez‐Medina

Zenteno‐Savín

Tift

et al. 2011

Journal of Experimental Biology

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“…Along with being exposed to prolonged fasting while on land, seals are also exposed to ischemia during breath-holding while diving and sleeping (Castellini et al, 1994;Elsner, 1999;Meir et al, 2009;Stockard et al, 2007). Seal tissues accumulate HX after ex vivo exposure to ischemia (Elsner et al, 1998). Seal heart and kidney, however, produce less HX than pig tissues, suggesting that seals have a greater capacity to conserve or salvage purines (Elsner et al, 1995;Elsner et al, 1998).…”

Section: Introductionmentioning

confidence: 99%

Prolonged fasting increases purine recycling in post-weaned northern elephant seals

Soñanez‐Organis

Vázquez‐Medina

Zenteno‐Savín³

et al. 2012

Journal of Experimental Biology

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SUMMARYNorthern elephant seals are naturally adapted to prolonged periods (1-2months) of absolute food and water deprivation (fasting). In terrestrial mammals, food deprivation stimulates ATP degradation and decreases ATP synthesis, resulting in the accumulation of purines (ATP degradation byproducts). Hypoxanthine-guanine phosphoribosyl transferase (HGPRT) salvages ATP by recycling the purine degradation products derived from xanthine oxidase (XO) metabolism, which also promotes oxidant production. The contributions of HGPRT to purine recycling during prolonged food deprivation in marine mammals are not well defined. In the present study we cloned and characterized the complete and partial cDNA sequences that encode for HGPRT and xanthine oxidoreductase (XOR) in northern elephant seals. We also measured XO protein expression and circulating activity, along with xanthine and hypoxanthine plasma content in fasting northern elephant seal pups. Blood, adipose and muscle tissue samples were collected from animals after 1, 3, 5 and 7weeks of their natural post-weaning fast. The complete HGPRT and partial XOR cDNA sequences are 771 and 345bp long and encode proteins of 218 and 115 amino acids, respectively, with conserved domains important for their function and regulation. XOR mRNA and XO protein expression increased 3-fold and 1.7-fold with fasting, respectively, whereas HGPRT mRNA (4-fold) and protein (2-fold) expression increased after 7weeks in adipose tissue and muscle. Plasma xanthine (3-fold) and hypoxanthine (2.5-fold) levels, and XO (1.7-to 20-fold) and HGPRT (1.5-to 1.7-fold) activities increased during the last 2weeks of fasting. Results suggest that prolonged fasting in elephant seal pups is associated with increased capacity to recycle purines, which may contribute to ameliorating oxidant production and enhancing the supply of ATP, both of which would be beneficial during prolonged food deprivation and appear to be adaptive in this species.

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“…The repetitive episodes of hypoxia-reoxygenation associated to diving apnea could increase ROS production, inducing oxidative stress and altering the NO availability by cells (Elsner et al, 1998;Sureda et al, 2004a). The effects of the diet supplementation with vitamin C in the erythrocyte capability to generate NO after hypoxia-reoxygenation could contribute to explain the vasodilatador effects of ascorbate.…”

Section: Introductionmentioning

confidence: 99%

Vitamin C supplementation influences the antioxidant response and nitric oxide handling of erythrocytes and lymphocytes to diving apnea

Sureda

Batle²,

Tauler

et al. 2006

Eur J Clin Nutr

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Objective: We have investigated the influence of vitamin C diet supplementation on the antioxidant response and nitrite levels in lymphocytes and erythrocytes during diving apnea. Subjects: Seven male professional apnea divers participated in a double blind crossover study. Divers were randomly assigned to either vitamin C supplemented or placebo groups. The subjects did not take any other supplements than the ones provided for this study. Intervention: One group was supplemented with vitamin C capsules (1 g per day) for 7 days while the other group took a placebo composed of lactose. The usual dietary habits of participants were assessed using a self-reported 7-days 24-h recall before the day of the study. Blood samples were taken under basal conditions, immediately after diving apnea for 4 h and after 1 h of recovery. Results: Catalase activity increased in erythrocytes (23%) and superoxide dismutase increased in lymphocytes (35%) during the recovery only in the placebo group. Lymphocyte ascorbate levels increased in the supplemented group after diving (85%) and maintained high at recovery. Plasma nitrite levels increased about twofold in both groups during the recovery. Erythrocyte nitrite levels increased after diving (50%) and about twofold during the recovery in the supplemented group. Nitrite levels and iNOS levels in lymphocytes were higher in the placebo group than in the supplemented during the recovery. Erythrocyte carbonyl derivates were unchanged in all situations. Conclusions: Vitamin C supplementation influenced the antioxidant response and NO handling in erythrocytes and lymphocytes to the oxidative stress induced by hypoxia-reoxygenation.

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Diving seals, ischemia-reperfusion and oxygen radicals

Cited by 69 publications

References 21 publications

Apnea stimulates the adaptive response to oxidative stress in elephant seal pups

Apnea stimulates the adaptive response to oxidative stress in elephant seal pups

Prolonged fasting increases purine recycling in post-weaned northern elephant seals

Vitamin C supplementation influences the antioxidant response and nitric oxide handling of erythrocytes and lymphocytes to diving apnea

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