Oxidative Stress Response’s Kinetics after 60 Minutes at Different (30% or 100%) Normobaric Hyperoxia Exposures
Abstract
:1. Introduction
2. Results
2.1. Reactive Oxygen Species (ROS) Rate and Isoprostane Levels after One Hour of Oxygen Exposure at a FiO2 of 30% or 100%
2.2. Antioxidant Response (TAC, SOD, CAT) after One Hour of Oxygen Exposure at a FiO2 of 30% or 100%
2.3. Inflammatory Response (IL-6, Neopterin, Creatinine, and Urates) after One Hour of Oxygen Exposure at a FiO2 of 30% or 100%
2.4. Percent of Expressed Proteins and Reactive Oxygen Species (ROS) after One Hour of Oxygen Exposure at a FiO2 of 30% or 100%
3. Discussion
Limitations
- −
- This study is to our knowledge one of the first to tackle the kinetics of responses to a single normobaric oxygen exposure at 30% and 100% of FiO2.
- −
- The measurements were conducted until 48 h post exposure and putatively open the door to new possible therapeutic outcomes for oxygen administration protocols.
- −
- The sampling was a standard plasmatic withdrawal, and the analysis is possible in a usual clinical setting without very specialized machinery or procedures.
- −
- The number of subjects is limited, but the sample can be considered to be homogenous since all were healthy young students and gender balanced.
- −
- The analysis was not made in the nucleus of the cells but in the plasma; this could be considered a weakness for some, but analysis in the nucleus would need a thoroughly different experimental setting.
4. Materials and Methods
4.1. Experimental Protocol
4.2. Blood Sample Analysis
4.2.1. Determination of ROS and TAC by Electron Paramagnetic Resonance (EPR)
4.2.2. Super-Oxide Dismutase (SOD), Catalase (CAT)
4.3. Urine Sample Analysis
4.3.1. Lipid Peroxidation (8-iso-PGF2α)
4.3.2. Interleukin-6
4.3.3. Creatinine, Neopterin, and Uric acid Concentrations
4.4. Statistical Analysis
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Abbreviations
FIH | Factor inhibiting HIF |
PHD | Prolyl hydroxylase domain |
REST | Repressor Element 1-Silencing Transcription factor |
CAT | Catalase |
FiO2 | Inspired fraction of oxygen |
HIF-1α | Hypoxia Inducible Factor-1α |
IL-6 | Interleukin-6 |
NOP | Normobaric oxygen paradox |
NF-κB | Nuclear factor-kappa B |
NRF2 | Nuclear Factor Erythroid 2 Related–Factor 2 |
PO2 | Oxygen partial pressure |
ROS | Reactive oxygen species |
SOD | Superoxide dismutase |
TAC | Total antioxidant capacity |
HRE | Hypoxia responsive element |
References
- Poulton, S.W.; Bekker, A.; Cumming, V.M.; Zerkle, A.L.; Canfield, D.E.; Johnston, D.T. A 200-million-year delay in permanent atmospheric oxygenation. Nature 2021, 592, 232–236. [Google Scholar] [CrossRef]
- Bitterman, H. Bench-to-bedside review: Oxygen as a drug. Crit. Care 2009, 13, 205. [Google Scholar] [CrossRef] [Green Version]
- Nakane, M. Biological effects of the oxygen molecule in critically ill patients. J. Intensive Care 2020, 8, 95. [Google Scholar] [CrossRef] [PubMed]
- van Vliet, T.; Demaria, F.C.M. To breathe or not to breathe: Understanding how oxygen sensing contributes to age-related phenotypes. Ageing Res. Rev. 2021, 67, 101267. [Google Scholar] [CrossRef] [PubMed]
- Fu, Q.; Duan, R.; Sun, Y.; Li, Q. Hyperbaric oxygen therapy for healthy aging: From mechanisms to therapeutics. Redox Biol. 2022, 53, 102352. [Google Scholar] [CrossRef] [PubMed]
- Okada, K.; Mori, D.; Makii, Y.; Nakamoto, H.; Murahashi, Y.; Yano, F.; Chang, S.H.; Taniguchi, Y.; Kobayashi, H.; Semba, H.; et al. Hypoxia-inducible factor-1 alpha maintains mouse articular cartilage through suppression of NF-κB signaling. Sci. Rep. 2020, 10, 5425. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Serebrovska, Z.O.; Serebrovska, T.V.; Kholin, V.A.; Tumanovska, L.V.; Shysh, A.M.; Pashevin, D.A.; Goncharov, S.V.; Stroy, D.; Grib, O.N.; Shatylo, V.B.; et al. Intermittent Hypoxia-Hyperoxia Training Improves Cognitive Function and Decreases Circulating Biomarkers of Alzheimer’s Disease in Patients with Mild Cognitive Impairment: A Pilot Study. Int. J. Mol. Sci. 2019, 20, 5405. [Google Scholar] [CrossRef] [Green Version]
- Burtscher, J.; Mallet, R.T.; Burtscher, M.; Millet, G.P. Hypoxia and brain aging: Neurodegeneration or neuroprotection? Ageing Res. Rev. 2021, 68, 101343. [Google Scholar] [CrossRef]
- Bestavashvili, A.; Glazachev, O.; Bestavashvili, A.; Suvorov, A.; Zhang, Y.; Zhang, X.; Rozhkov, A.; Kuznetsova, N.; Pavlov, C.; Glushenkov, D.; et al. Intermittent Hypoxic-Hyperoxic Exposures Effects in Patients with Metabolic Syndrome: Correction of Cardiovascular and Metabolic Profile. Biomedicines 2022, 10, 566. [Google Scholar] [CrossRef]
- Matta, A.; Nader, V.; Lebrin, M.; Gross, F.; Prats, A.C.; Cussac, D.; Galinier, M.; Roncalli, J. Pre-Conditioning Methods and Novel Approaches with Mesenchymal Stem Cells Therapy in Cardiovascular Disease. Cells 2022, 11, 1620. [Google Scholar] [CrossRef]
- Balestra, C.; Lambrechts, K.; Mrakic-Sposta, S.; Vezzoli, A.; Levenez, M.; Germonpre, P.; Virgili, F.; Bosco, G.; Lafere, P. Hypoxic and Hyperoxic Breathing as a Complement to Low-Intensity Physical Exercise Programs: A Proof-of-Principle Study. Int. J. Mol. Sci. 2021, 22, 9600. [Google Scholar] [CrossRef] [PubMed]
- Balestra, C.; Theunissen, S.; Papadopoulou, V.; Le Mener, C.; Germonpre, P.; Guerrero, F.; Lafere, P. Pre-dive Whole-Body Vibration Better Reduces Decompression-Induced Vascular Gas Emboli than Oxygenation or a Combination of Both. Front. Physiol. 2016, 7, 586. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Webb, J.T.; Pilmanis, A.A. Fifty years of decompression sickness research at Brooks AFB, TX: 1960-2010. Aviat. Space Env. Med. 2011, 82 (Suppl. S5), A1–A25. [Google Scholar] [CrossRef] [PubMed]
- Sannigrahi, P.; Sushree, S.K.; Agarwal, A. Aeromedical Concerns and Lessons Learnt during Oxygen Jump at Dolma Sampa. Indian J. Aerosp. Med. 2018, 62, 16–20. [Google Scholar]
- Balestra, C.; Arya, A.K.; Leveque, C.; Virgili, F.; Germonpre, P.; Lambrechts, K.; Lafere, P.; Thom, S.R. Varying Oxygen Partial Pressure Elicits Blood-Borne Microparticles Expressing Different Cell-Specific Proteins-Toward a Targeted Use of Oxygen? Int. J. Mol. Sci. 2022, 23, 7888. [Google Scholar] [CrossRef]
- Halliwell, B.; Gutteridge, J.M.C. Free Radicals in Biology and Medicine; Oxford University Press: Oxford, UK, 2015. [Google Scholar]
- Sies, H.; Belousov, V.V.; Chandel, N.S.; Davies, M.J.; Jones, D.P.; Mann, G.E.; Murphy, M.P.; Yamamoto, M.; Winterbourn, C. Defining roles of specific reactive oxygen species (ROS) in cell biology and physiology. Nat. Rev. Mol. Cell Biol. 2022, 23, 499–515. [Google Scholar] [CrossRef]
- La Sala, L.; Tagliabue, E.; Mrakic-Sposta, S.; Uccellatore, A.C.; Senesi, P.; Terruzzi, I.; Trabucchi, E.; Rossi-Bernardi, L.; Luzi, L. Lower miR-21/ROS/HNE levels associate with lower glycemia after habit-intervention: DIAPASON study 1-year later. Cardiovasc. Diabetol. 2022, 21, 35. [Google Scholar] [CrossRef]
- Cova, E.; Pandolfi, L.; Colombo, M.; Frangipane, V.; Inghilleri, S.; Morosini, M.; Mrakic-Sposta, S.; Moretti, S.; Monti, M.; Pignochino, Y.; et al. Pemetrexed-loaded nanoparticles targeted to malignant pleural mesothelioma cells: An in vitro study. Int. J. Nanomed. 2019, 14, 773–785. [Google Scholar] [CrossRef] [Green Version]
- Mrakic-Sposta, S.; Vezzoli, A.; Maderna, L.; Gregorini, F.; Montorsi, M.; Moretti, S.; Greco, F.; Cova, E.; Gussoni, M. R(+)-Thioctic Acid Effects on Oxidative Stress and Peripheral Neuropathy in Type II Diabetic Patients: Preliminary Results by Electron Paramagnetic Resonance and Electroneurography. Oxid. Med. Cell Longev. 2018, 2018, 1767265. [Google Scholar] [CrossRef]
- Calabrese, E.J.; Mattson, M.P. How does hormesis impact biology, toxicology, and medicine? NPJ Aging Mech. Dis. 2017, 3, 13. [Google Scholar] [CrossRef] [Green Version]
- Lennicke, C.; Cochemé, H.M. Redox metabolism: ROS as specific molecular regulators of cell signaling and function. Mol. Cell 2021, 81, 3691–3707. [Google Scholar] [CrossRef] [PubMed]
- Chelombitko, M.A. Role of Reactive Oxygen Species in Inflammation: A Minireview. Mosc. Univ. Biol. Sci. Bull. 2018, 73, 199–202. [Google Scholar] [CrossRef] [Green Version]
- Hadanny, A.; Efrati, S. The Hyperoxic-Hypoxic Paradox. Biomolecules 2020, 10, 958. [Google Scholar] [CrossRef] [PubMed]
- Balestra, C.; Germonpré, P.; Poortmans, J.R.; Marroni, A. Serum erythropoietin levels in healthy humans after a short period of normobaric and hyperbaric oxygen breathing: The "normobaric oxygen paradox". J. Appl. Physiol. 2006, 100, 512–518. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cimino, F.; Balestra, C.; Germonpre, P.; De Bels, D.; Tillmans, F.; Saija, A.; Speciale, A.; Virgili, F. Pulsed high oxygen induces a hypoxic-like response in human umbilical endothelial cells and in humans. J. Appl. Physiol. 2012, 113, 1684–1689. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Khalife, M.; Ben Aziz, M.; Balestra, C.; Valsamis, J.; Sosnowski, M. Physiological and Clinical Impact of Repeated Inhaled Oxygen Variation on Erythropoietin Levels in Patients After Surgery. Front. Physiol. 2021, 12, 744074. [Google Scholar] [CrossRef] [PubMed]
- Lafere, P.; Schubert, T.; De Bels, D.; Germonpre, P.; Balestra, C. Can the normobaric oxygen paradox (NOP) increase reticulocyte count after traumatic hip surgery? J. Clin. Anesth. 2013, 25, 129–134. [Google Scholar] [CrossRef] [Green Version]
- Fratantonio, D.; Virgili, F.; Zucchi, A.; Lambrechts, K.; Latronico, T.; Lafere, P.; Germonpre, P.; Balestra, C. Increasing Oxygen Partial Pressures Induce a Distinct Transcriptional Response in Human PBMC: A Pilot Study on the "Normobaric Oxygen Paradox". Int. J. Mol. Sci. 2021, 22, 458. [Google Scholar] [CrossRef]
- Calabrese, E. Hormesis: Path and Progression to Significance. Int. J. Mol. Sci. 2018, 19, 2871. [Google Scholar] [CrossRef] [Green Version]
- Franceschi, C.; Bonafè, M.; Valensin, S.; Olivieri, F.; De Luca, M.; Ottaviani, E.; De Benedictis, G. Inflamm-aging. An evolutionary perspective on immunosenescence. Ann. N. Y. Acad. Sci. 2000, 908, 244–254. [Google Scholar] [CrossRef]
- Franceschi, C.; Campisi, J. Chronic inflammation (inflammaging) and its potential contribution to age-associated diseases. J. Gerontol. A Biol. Sci. Med. Sci. 2014, 69 (Suppl. S1), S4–S9. [Google Scholar] [CrossRef] [PubMed]
- Furman, D.; Campisi, J.; Verdin, E.; Carrera-Bastos, P.; Targ, S.; Franceschi, C.; Ferrucci, L.; Gilroy, D.W.; Fasano, A.; Miller, G.W.; et al. Chronic inflammation in the etiology of disease across the life span. Nat. Med. 2019, 25, 1822–1832. [Google Scholar] [CrossRef] [PubMed]
- Akhigbe, R.; Ajayi, A. The impact of reactive oxygen species in the development of cardiometabolic disorders: A review. Lipids Health Dis. 2021, 20, 23. [Google Scholar] [CrossRef] [PubMed]
- Checa, J.; Aran, J.M. Reactive Oxygen Species: Drivers of Physiological and Pathological Processes. J. Inflamm. Res. 2020, 13, 1057–1073. [Google Scholar] [CrossRef]
- Balestra, C.; Kot, J. Oxygen: A Stimulus, Not "Only" a Drug. Medicina 2021, 57, 1161. [Google Scholar] [CrossRef] [PubMed]
- Rocco, M.; D’Itri, L.; De Bels, D.; Corazza, F.; Balestra, C. The "normobaric oxygen paradox": A new tool for the anesthetist? Minerva Anestesiol. 2014, 80, 366–372. [Google Scholar]
- Bel’skaya, L.V.; Kosenok, V.K.; Sarf, E.A. Chronophysiological features of the normal mineral composition of human saliva. Arch. Oral. Biol. 2017, 82, 286–292. [Google Scholar] [CrossRef]
- Teng, R.J.; Jing, X.; Martin, D.P.; Hogg, N.; Haefke, A.; Konduri, G.G.; Day, B.W.; Naylor, S.; Pritchard, K.A., Jr. N-acetyl-lysyltyrosylcysteine amide, a novel systems pharmacology agent, reduces bronchopulmonary dysplasia in hyperoxic neonatal rat pups. Free Radic. Biol. Med. 2021, 166, 73–89. [Google Scholar] [CrossRef]
- Chen, C.; He, M.; Li, X.; Yu, L.; Liu, Y.; Yang, Y.; Li, L.; Jia, J.; Li, B. H2O2/DEM-Promoted Maft Promoter Demethylation Drives Nrf2/ARE Activation in Zebrafish. Life 2022, 12, 1436. [Google Scholar] [CrossRef]
- Semenza, G.L. HIF-1: Mediator of physiological and pathophysiological responses to hypoxia. J. Appl. Physiol. 2000, 88, 1474–1480. [Google Scholar] [CrossRef] [Green Version]
- Cavadas, M.A.S.; Mesnieres, M.; Crifo, B.; Manresa, M.C.; Selfridge, A.C.; Scholz, C.C.; Cummins, E.P.; Cheong, A.; Taylor, C.T. REST mediates resolution of HIF-dependent gene expression in prolonged hypoxia. Sci. Rep. 2015, 5, 17851. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cavadas, M.A.S.; Mesnieres, M.; Crifo, B.; Manresa, M.C.; Selfridge, A.C.; Keogh, C.E.; Fabian, Z.; Scholz, C.C.; Nolan, K.A.; Rocha, L.M.A.; et al. REST is a hypoxia-responsive transcriptional repressor. Sci. Rep. 2016, 6, 31355. [Google Scholar] [CrossRef] [PubMed]
- De Bels, D.; Corazza, F.; Germonpre, P.; Balestra, C. The normobaric oxygen paradox: A novel way to administer oxygen as an adjuvant treatment for cancer? Med. Hypotheses 2010, 76, 467–470. [Google Scholar] [CrossRef] [PubMed]
- Sies, H. Role of Metabolic H2O2 Generation. J. Biol. Chem. 2014, 289, 8735–8741. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Basang, Z.; Zhang, S.; Yang, L.; Quzong, D.; Li, Y.; Ma, Y.; Hao, M.; Pu, W.; Liu, X.; Xie, H.; et al. Correlation of DNA methylation patterns to the phenotypic features of Tibetan elite alpinists in extreme hypoxia. J. Genet. Genom. 2021, 48, 928–935. [Google Scholar] [CrossRef]
- Wilson, J.W.; Shakir, D.; Batie, M.; Frost, M.; Rocha, S. Oxygen-sensing mechanisms in cells. FEBS J. 2020, 287, 3888–3906. [Google Scholar] [CrossRef]
- Kobayashi, E.H.; Suzuki, T.; Funayama, R.; Nagashima, T.; Hayashi, M.; Sekine, H.; Tanaka, N.; Moriguchi, T.; Motohashi, H.; Nakayama, K.; et al. Nrf2 suppresses macrophage inflammatory response by blocking proinflammatory cytokine transcription. Nat. Commun. 2016, 7, 11624. [Google Scholar] [CrossRef] [Green Version]
- Gao, W.; Guo, L.; Yang, Y.; Wang, Y.; Xia, S.; Gong, H.; Zhang, B.K.; Yan, M. Dissecting the Crosstalk Between Nrf2 and NF-κB Response Pathways in Drug-Induced Toxicity. Front. Cell Dev. Biol. 2021, 9, 809952. [Google Scholar] [CrossRef]
- Kuzkaya, N.; Weissmann, N.; Harrison, D.G.; Dikalov, S. Interactions of peroxynitrite with uric acid in the presence of ascorbate and thiols: Implications for uncoupling endothelial nitric oxide synthase. Biochem. Pharm. 2005, 70, 343–354. [Google Scholar] [CrossRef]
- Gu, X.; El-Remessy, A.B.; Brooks, S.E.; Al-Shabrawey, M.; Tsai, N.T.; Caldwell, R.B. Hyperoxia induces retinal vascular endothelial cell apoptosis through formation of peroxynitrite. Am. J. Physiol. Cell Physiol. 2003, 285, C546–C554. [Google Scholar] [CrossRef] [Green Version]
- World Medical, A. World Medical Association Declaration of Helsinki: Ethical principles for medical research involving human subjects. JAMA 2013, 310, 2191–2194. [Google Scholar]
- Mrakic-Sposta, S.; Vezzoli, A.; D’Alessandro, F.; Paganini, M.; Dellanoce, C.; Cialoni, D.; Bosco, G. Change in Oxidative Stress Biomarkers During 30 Days in Saturation Dive: A Pilot Study. Int. J. Env. Res. Public Health 2020, 17, 7118. [Google Scholar] [CrossRef] [PubMed]
- Moretti, S.; Mrakic-Sposta, S.; Roncoroni, L.; Vezzoli, A.; Dellanoce, C.; Monguzzi, E.; Branchi, F.; Ferretti, F.; Lombardo, V.; Doneda, L.; et al. Oxidative stress as a biomarker for monitoring treated celiac disease. Clin. Transl. Gastroenterol. 2018, 9, 157. [Google Scholar] [CrossRef] [PubMed]
- Mrakic-Sposta, S.; Vezzoli, A.; Rizzato, A.; Della Noce, C.; Malacrida, S.; Montorsi, M.; Paganini, M.; Cancellara, P.; Bosco, G. Oxidative stress assessment in breath-hold diving. Eur. J. Appl. Physiol. 2019, 119, 2449–2456. [Google Scholar] [CrossRef]
- Bosco, G.; Rizzato, A.; Quartesan, S.; Camporesi, E.; Mrakic-Sposta, S.; Moretti, S.; Balestra, C.; Rubini, A. Spirometry and oxidative stress after rebreather diving in warm water. Undersea Hyperb. Med. 2018, 45, 191–198. [Google Scholar] [CrossRef]
- Mrakic-Sposta, S.; Gussoni, M.; Montorsi, M.; Porcelli, S.; Vezzoli, A. A quantitative method to monitor reactive oxygen species production by electron paramagnetic resonance in physiological and pathological conditions. Oxid. Med. Cell Longev. 2014, 2014, 306179. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bosco, G.; Paganini, M.; Giacon, T.A.; Oppio, A.; Vezzoli, A.; Dellanoce, C.; Moro, T.; Paoli, A.; Zanotti, F.; Zavan, B.; et al. Oxidative Stress and Inflammation, MicroRNA, and Hemoglobin Variations after Administration of Oxygen at Different Pressures and Concentrations: A Randomized Trial. Int. J. Env. Res. Public Health 2021, 18, 9755. [Google Scholar] [CrossRef]
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Leveque, C.; Mrakic-Sposta, S.; Lafère, P.; Vezzoli, A.; Germonpré, P.; Beer, A.; Mievis, S.; Virgili, F.; Lambrechts, K.; Theunissen, S.; et al. Oxidative Stress Response’s Kinetics after 60 Minutes at Different (30% or 100%) Normobaric Hyperoxia Exposures. Int. J. Mol. Sci. 2023, 24, 664. https://doi.org/10.3390/ijms24010664
Leveque C, Mrakic-Sposta S, Lafère P, Vezzoli A, Germonpré P, Beer A, Mievis S, Virgili F, Lambrechts K, Theunissen S, et al. Oxidative Stress Response’s Kinetics after 60 Minutes at Different (30% or 100%) Normobaric Hyperoxia Exposures. International Journal of Molecular Sciences. 2023; 24(1):664. https://doi.org/10.3390/ijms24010664
Chicago/Turabian StyleLeveque, Clément, Simona Mrakic-Sposta, Pierre Lafère, Alessandra Vezzoli, Peter Germonpré, Alexandre Beer, Stéphane Mievis, Fabio Virgili, Kate Lambrechts, Sigrid Theunissen, and et al. 2023. "Oxidative Stress Response’s Kinetics after 60 Minutes at Different (30% or 100%) Normobaric Hyperoxia Exposures" International Journal of Molecular Sciences 24, no. 1: 664. https://doi.org/10.3390/ijms24010664