Physiological significance of oxidative stress and its role in adaptation of the human body to deleterious factors

Abstract

BACKGROUND: Oxidative stress is an extremely widespread condition manifested in an increased rate of free-radical processes and accumulation of reactive oxygen species (ROS) in the tissues. It appears in different physiologic states and pathological processes accompanied by stimulation of the sympathetic adrenal system or tissue hypoxia or under stress. However, until now, there is still no clarity on the issue of the significance of oxidative stress in the development of adaptation processes in the organism.

OBJECTIVE: In the present work we will review the most recent finding about physiologic role of oxidative stress and its participation in adaptation of an organism to effect of different adverse factors.

METHODS: A systematic literature search was performed using the Pubmed search engine. Studies published over past 18 years, i.e. between 1998 and 2015 were considered for review. Followed keywords were used: “oxidative stress,” “free radical oxidation,” “ROS,” “endogenous aldehydes,” “adaptation.”

RESULTS: The article cites arguments supporting the notion that oxidative stress serves as a nonspecific link in the adaptation of the human body to the effects of injurious factors. Oxidative stress exerts regulatory effects by changing the redox state of the cell. Oxidative stress affects on various intracellular proteins containing cysteine ​​residues, e.g., enzymes, chaperones, and transcription factors, etc. For this reason, the use of antioxidants for the treatment and prophylaxis of a wide range of diseases is not recommended.

CONCLUSION: Further investigation is needed in this field. The most attention should be paid to careful experimental verification aimed at quantitative assessment of the ROS level in tissues under oxidative stress, as well as at the study of possibility of enhancing the catabolism of free radical oxidation carbonyl products in order to prevent tissue damage under oxidative stress.

Keywords

oxidative stress / free radical oxidation / ROS / adaptation / endogenous aldehydes

References

[1] Afroze T, Sadi A M, Momen M A, Gu S, Heximer S, Husain M (2007). c-Myb-dependent inositol 1,4,5-trisphosphate receptor type-1 expression in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol, 27(6): 1305–1311

[2] Akhtar M, Wright J N (2015). Acyl-Carbon Bond Cleaving Cytochrome P450 Enzymes: CYP17A1, CYP19A1 and CYP51A1. Adv Exp Med Biol, 851: 107–130

[3] Antelmann H, Helmann J D (2011). Thiol-based redox switches and gene regulation. Antioxid Redox Signal, 14(6): 1049–1063

[4] Basse A L, Isidor M S, Winther S, Skjoldborg N B, Murholm M, Andersen E S, Pedersen S B, Wolfrum C, Quistorff B, Hansen J B (2017). Regulation of glycolysis in brown adipocytes by HIF-1a. Sci Rep, 7(1): 4052

[5] Baud O, Greene A E, Li J, Wang H, Volpe J J, Rosenberg P A (2004). Glutathione peroxidase-catalase cooperativity is required for resistance to hydrogen peroxide by mature rat oligodendrocytes. J Neurosci, 24(7): 1531–1540

[6] Becker L B (2004). New concepts in reactive oxygen species and cardiovascular reperfusion physiology. Cardiovasc Res, 6 1 (3): 461 –470

[7] Betteridge D J (2000). What is oxidative stress? Metabolism, 49(2 Suppl 1): 3–8

[8] Bleier L, Wittig I, Heide H, Steger M, Brandt U, Dröse S (2015). Generator-specific targets of mitochondrial reactive oxygen species. Free Radic Biol Med, 78: 1–10

[9] Brandes N, Schmitt S, Jakob U (2009). Thiol-based redox switches in eukaryotic proteins. Antioxid Redox Signal, 11(5): 997–1014

[10] Brown D I, Griendling K K (2015). Regulation of signal transduction by reactive oxygen species in the cardiovascular system. Circ Res, 116(3): 531–549

[11] Chandel N S, Tuveson D A (2014). The promise and perils of antioxidants for cancer patients. N Engl J Med, 371(2): 177–178

[12] Chen Y, Azad M B, Gibson S B (2009). Superoxide is the major reactive oxygen species regulating autophagy. Cell Death Differ, 16(7): 1040–1052

[13] Chen Y, Xu H, Liu J, Zhang C, Leutz A, Mo X (2007). The c-Myb functions as a downstream target of PDGF-mediated survival signal in vascular smooth muscle cells. Biochem Biophys Res Commun, 360(2): 433–436

[14] Chen Y R, Zweier J L (2014). Cardiac mitochondria and ROS generation. Circ Res, 114(3): 524–537

[15] Cheng Y, Chen G, Hong L, Zhou L, Hu M, Li B, Huang J, Xia L, Li C (2013). How does hypoxia inducible factor-1a participate in enhancing the glycolysis activity in cervical cancer? Ann Diagn Pathol, 17(3): 305–311

[16] Collins Y, Chouchani E T, James A M, Menger K E, Cochemé H M, Murphy M P (2012). Mitochondrial redox signalling at a glance. J Cell Sci, 125(Pt 4): 801–806

[17] Corre S, Galibert M D (2005). Upstream stimulating factors: highly versatile stress-responsive transcription factors. Pigment Cell Res, 18(5): 337–348

[18] Corre S, Galibert M D (2006). [USF as a key regulatory element of gene expression]. Med Sci (Paris), 22(1): 62–67

[19] Cox A G, Winterbourn C C, Hampton M B (2009). Mitochondrial peroxiredoxin involvement in antioxidant defence and redox signalling. Biochem J, 425(2): 313–325

[20] D’Autréaux B, Toledano M B (2007). ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat Rev Mol Cell Biol, 8(10): 813–824

[21] Davydov V V (2014). Age-dependent change in aldo-keto reductases composition in the blood of rats. Am J Biomed Life Sci, 2(1): 1–4

[22] Davydov V V, Bozhkov A I, Grabovetskaya E R (2014). Age-related peculiarities of change in content of free radical oxidation products in muscle during stress. Fron Biol, 9(4): 283–286

[23] Davydov V V, Bozhkov A I, Kulchitskiy O K (2012). Physiological and pathophysiological role of endogenous aldehydes, Saarbrucken: Palmarium Academic Publishing, 240 (inRussian)

[24] Davydov V V, Dobaeva N M, Bozhkov A I (2004). Possible role of alteration of aldehyde’s scavenger enzymes during aging. Exp Gerontol, 39(1): 11–16

[25] Davydov V V, Shvets V N (2001). Lipid peroxidation in the heart of adult and old rats during immobilization stress. Exp Gerontol, 36(7): 1155–1160

[26] Davydov V V, Shvets V N (2003). Age-dependent differences in the stimulation of lipid peroxidation in the heart of rats during immobilization stress. Exp Gerontol, 38(6): 693–698

[27] Dröge W (2002). Free radicals in the physiological control of cell function. Physiol Rev, 82(1): 47–95

[28] Dröse S, Brandt U, Wittig I (2014). Mitochondrial respiratory chain complexes as sources and targets of thiol-based redox-regulation. Biochim Biophys Acta, 1844(8): 1344–1354

[29] Farrell K A, Withers S B, Holt C M (2011). C-Myb function in the vessel wall. Front Biosci (Elite Ed), 3: 968–977

[30] Finkel T (2011). Signal transduction by reactive oxygen species. J Cell Biol, 194(1): 7–15

[31] Fridovich I (1999). Fundamental aspects of reactive oxygen species, or what’s the matter with oxygen? Ann N Y Acad Sci, 893(1 OXIDATIVE/ENE): 13–18

[32] Giles G I (2006). The redox regulation of thiol dependent signaling pathways in cancer. Curr Pharm Des, 12(34): 4427–4443

[33] Groitl B, Jakob U (2014). Thiol-based redox switches. Biochim Biophys Acta, 1844(8): 1335–1343

[34] Halliwell B (2009). The wanderings of a free radical. Free Radic Biol Med, 46(5): 531–542

[35] Halliwell B (2012). Free radicals and antioxidants: updating a personal view. Nutr Rev, 70(5): 257–265

[36] Harman D (1956). Aging: a theory based on free radical and radiation chemistry. J Gerontol, 11(3): 298–300

[37] Hinerfeld D, Traini M D, Weinberger R P, Cochran B, Doctrow S R, Harry J, Melov S (2004). Endogenous mitochondrial oxidative stress: neurodegeneration, proteomic analysis, specific respiratory chain defects, and efficacious antioxidant therapy in superoxide dismutase 2 null mice. J Neurochem, 88(3): 657–667

[38] Hirano F, Tanaka H, Hirano Y, Hiramoto M, Handa H, Makino I, Scheidereit C (1998). Functional interference of Sp1 and NF-kappaB through the same DNA binding site. Mol Cell Biol, 18(3): 1266–1274

[39] Imlay J A (2008). Cellular defenses against superoxide and hydrogen peroxide. Annu Rev Biochem, 77(1): 755–776

[40] Jomova K, Valko M (2011). Advances in metal-induced oxidative stress and human disease. Toxicol, 283 (2 –3): 65–87

[41] Kuntsevich N V (2010). The role of nuclear factor Nf-b in the rejection of transplatant. Vestnik transplantology and artifical organs, 1: 72–77 (in Russian)

[42] Leonarduzzi G, Sottero B, Poli G (2010). Targeting tissue oxidative damage by means of cell signaling modulators: the antioxidant concept revisited. Pharmacol Ther, 128(2): 336–374

[43] Leonarduzzi G, Sottero B, Testa G, Biasi F, Poli G (2011). New insights into redox-modulated cell signaling. Curr Pharm Des, 17(36): 3994–4006

[44] Ma Q (2013). Role of nrf2 in oxidative stress and toxicity. Annu Rev Pharmacol Toxicol, 53(1): 401–426

[45] Ma Q, and the MaQ (2008). Xenobiotic-activated receptors: from transcription to drug metabolism to disease. Chem Res Toxicol, 21(9): 1651–1671

[46] Marín-Hernández A, Gallardo-Pérez J C, Ralph S J, Rodríguez-Enríquez S, Moreno-Sánchez R (2009). HIF-1alpha modulates energy metabolism in cancer cells by inducing over-expression of specific glycolytic isoforms. Mini Rev Med Chem, 9(9): 1084–1101

[47] Meerson F Z (1984). Pathogenesis and prevention of stress and ischemic injures of heart. Moscow. Medicina (B Aires), 270 (in Russian)

[48] Menshikova E B, Lankin V Z, Zenkov N K (2006). The oxidative stress. Antioxidants and prooxidants. Moscow: Slovo, 556 (in Russian)

[49] Miki H, Funato Y (2012). Regulation of intracellular signalling through cysteine oxidation by reactive oxygen species. J Biochem, 151(3): 255–261

[50] Montuschi P, Barnes P, Roberts L J 2nd (2007). Insights into oxidative stress: the isoprostanes. Curr Med Chem, 14(6): 703–717

[51] Morigasaki S, Shimada K, Ikner A, Yanagida M, Shiozaki K (2008). Glycolytic enzyme GAPDH promotes peroxide stress signaling through multistep phosphorelay to a MAPK cascade. Mol Cell, 30(1): 108–113

[52] Muller F L, Lustgarten M S, Jang Y, Richardson A, Van Remmen H (2007). Trends in oxidative aging theories. Free Radic Biol Med, 43(4): 477–503

[53] Myung S K, Ju W, Cho B, Oh S W, Park S M, Koo B K, Park B J, and the Korean Meta-Analysis Study Group (2013). Efficacy of vitamin and antioxidant supplements in prevention of cardiovascular disease: systematic review and meta-analysis of randomised controlled trials. BMJ, 346(jan18 1): f10

[54] Nayanatara A K, Nagaraja H S, Anupama B K (2005). The effect of repeated swimming stress on organ weights and lipid peroxidation in rats. Thai J Physiol Sci, 18(1): 3–9

[55] Nietzel T, Mostertz J, Hochgräfe F, Schwarzländer M (2017). Redox regulation of mitochondrial proteins and proteomes by cysteine thiol switches. Mitochondrion, 33: 72–83

[56] O’Brein PJO, Siraki A G, Shangari N (2005). Aldehyde sources metabolism, molecular toxicity mechanisms,and possible effects on human health. Critical Reviews inToxicology, 35: 609–662

[57] Piwowar A (2010). [Advanced oxidation protein products. Part I. Mechanism of the formation, characteristics and property]. Pol Merkur Lekarski, 28(164): 166–169

[58] Plotnikov E Y, Silachev D N, Jankauskas S S, Rokitskaya T I, Chupyrkina A A, Pevzner I B, Zorova L D, Isaev N K, Antonenko Y N, Skulachev V P, Zorov D B (2012). Mild uncoupling of respiration and phosphorylation as a mechanism providing nephro- and neuroprotective effects of penetrating cations of the SkQ family. Biochemistry (Mosc), 77(9): 1029–1037

[59] Poyton R O, Ball K A, Castello P R (2009). Mitochondrial generation of free radicals and hypoxic signaling. Trends Endocrinol Metab, 20(7): 332–340

[60] Reczek C R, Chandel N S (2015). ROS-dependent signal transduction. Curr Opin Cell Biol, 33: 8–13

[61] Roginsky V A, Tashlitsky V N, Skulachev V P (2009). Chain-breaking antioxidant activity of reduced forms of mitochondria-targeted quinones, a novel type of geroprotectors. Aging (Albany NY), 1(5): 481–489

[62] Russell E G, Cotter T G (2015). New Insight into the Role of Reactive Oxygen Species (ROS) in Cellular Signal-Transduction Processes, 319: 221 –254

[63] Sahin E, Gumuslu S (2007). Immobilization stress in rat tissues: alteration of protein oxidation, lipid peroxidation and antioxidant defense system. Comp Biochem Physio. C. Toxicol Pharmacol, 144(4): 324–347

[64] Schieber M, Chandel N S (2014). ROS function in redox signaling and oxidative stress. Curr Biol, 24(10): R453–R462

[65] Sena L A, Chandel N S (2012). Physiological roles of mitochondrial reactive oxygen species. Mol Cell, 48(2): 158–167

[66] Skulachev V P (2007). A biochemical approach to the problem of aging: “megaproject” on membrane-penetrating ions. The first results and prospects. Biochemistry (Mosc), 72(12): 1385–1396

[67] Skulachev V P, Anisimov V N, Antonenko Y N, Bakeeva L E, Chernyak B V, Erichev V P, Filenko O F, Kalinina N I, Kapelko V I, Kolosova N G, Kopnin B P, Korshunova G A, Lichinitser M R, Obukhova L A, Pasyukova E G, Pisarenko O I, Roginsky V A, Ruuge E K, Senin I I, Severina I I, Skulachev M V, Spivak I M, Tashlitsky V N, Tkachuk V A, Vyssokikh M Y, Yaguzhinsky L S, Zorov D B (2009). An attempt to prevent senescence: a mitochondrial approach. Biochim Biophys Acta, 1787(5): 437–461

[68] Steinhubl S R (2008). Why have antioxidants failed in clinical trials? Am J Cardiol, 101(10 10A): 14D–19D

[69] Taverne Y J, Bogers A J, Duncker D J, Merkus D (2013). Reactive oxygen species and the cardiovascular system. Oxid Med Cell Longev, 2013: 862423

[70] Tell G, Quadrifoglio F, Tiribelli C, Kelley M R (2009). The many functions of APE1/Ref-1: not only a DNA repair enzyme. Antioxid Redox Signal, 11(3): 601–620

[71] Uchida K (2000). Role of reactive aldehyde in cardiovascular diseases. Free Radic Biol Med, 28(12): 1685–1696

[72] Uchida K (2003). 4-Hydroxy-2-nonenal: a product and mediator of oxidative stress. Prog Lipid Res, 42(4): 318–343

[73] Valko M, Izakovic M, Mazur M (2004). Role of oxygen radicals in DNA damage and cancer incidence. Mol Cell Biochem, 266 (1 – 2): 37 –56

[74] Valko M, Leibfritz D, Moncol J, Cronin M T, Mazur M, Telser J (2007). Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol, 39(1): 44–84

[75] Vivekananthan D P, Penn M S, Sapp S K, Hsu A, Topol E J (2003). Use of antioxidant vitamins for the prevention of cardiovascular disease: meta-analysis of randomised trials. Lancet, 361(9374): 2017–2023

[76] Wang G, Kawakami K, Gick G (2007). Regulation of Na,K-ATPase alpha1 subunit gene transcription in response to low K(+): role of CRE/ATF- and GC box-binding proteins. J Cell Physiol, 213(1): 167–176

[77] Welch K D, Davis T Z, Van Eden M E, Aust S D (2002). Deleterious iron-mediated oxidation of biomolecules. Free Radic Biol Med, 32(7): 577–583

[78] Wilson L A, Yamamoto H, Singh G (2004). Role of the transcription factor Ets-1 in cisplatin resistance. Mol Cancer Ther, 3(7): 823–832

[79] Winterbourn C C (2008). Reconciling the chemistry and biology of reactive oxygen species. Nat Chem Biol, 4(5): 278–286

[80] Winterbourn C C (2013). The biological chemistry of hydrogen peroxide. Methods Enzymol, 528: 3–25

[81] Ye Y, Li J, Yuan Z (2013). Effect of antioxidant vitamin supplementation on cardiovascular outcomes: a meta-analysis of randomized controlled trials. PLoS One, 8(2): e56803

[82] Yuksel S, Asma D, Yesilada O (2008). Antioxidative and metabolic responses to extended cold exposure in rats. Acta Biol Hung, 59(1): 57–66

[83] Zabłocka A, Janusz M (2008). [The two faces of reactive oxygen species]. Postepy Hig Med Dosw (Online), 62: 118–124

[84] Zhang D X, Gutterman D D (2007). Mitochondrial reactive oxygen species-mediated signaling in endothelial cells. Am J Physiol Heart Circ Physiol, 292(5): H2023–H2031

Compliance with ethics guidelines

Davydov V. V., Shestopalov A. V., and Grabovetskaya E. R. declare that they have no conflicts of interest related to this article. This article represents theoretical research. The authors did not use clinical samples or laboratory animals.

RIGHTS & PERMISSIONS

2018 Higher Education Press and Springer-Verlag GmbH Germany, part of Springer Nature