Skip to main content
SpringerLink
Log in

Protective role of carbon dioxide (CO2) in generation of reactive oxygen species

  • Published:
Molecular and Cellular Biochemistry Aims and scope Submit manuscript

Abstract

The results testify to the fact that CO2 is a powerful inhibitor of reactive oxygen species (ROS) generation by cells (blood phagocytes and alveolar macrophages of 96 people and cells of inner organs and tissue phagocytes (of liver, brain, myocardium, lungs, kidneys, stomach, and skeleton muscles), as well as by mitochondria of the liver of 186 white mice and human tissues. Generation of ROS was determined using various methods with CO2 directly acting on the cells and bioptates and indirectly on the organism as a whole. CO2 in the concentration of 5.1 % (P = 37.5 mmHg), 8.2 % (P = 60.0 mmHg), and 20 % (P = 146.0 mmHg) in a mixture with air (total pressure = 730 mmHg) inhibits the basal ROS generation by phagocytes on the average by 3.52, 5.69, and 10.03 times, respectively (p < 0.05), and the stimulated by corpuscular particles: (a) zymosan by 3.24, 4.43, and 7.95 times; (b)SiO2: by 2.99, 3.24, and 5.76 times (p < 0.05). This is confirmed by the feet that CO2, along with inhibiting the O2 − generation by cells of the various organs, including the liver, as a rule, by 2.19–4.7 times, p < 0.01 or <0.001 induces simultaneously a decrease in the O2 − generation by mitochondria isolated from the liver (by 1.91–3.2 times, p < 0.001). The mechanism of CO2 influence is realized, in part, by inhibition of NADPH-oxidase activity. Taken into consideration proven role of CO2 in different pathophysiological conditions, (such as endoarteritis, bronchial asthma, and infectious diseases), present findings may be of clinical interest in terms of potential implementation of CO2 donors as adjuvant therapeutics in these diseases.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

CLb:

Basal chemiluminescent index

BIS:

Buffered isotonic solution

CO3 :

Carbonate radicals

CAT:

Catalase

CL:

Chemiluminescence

DMSO:

Demethylsulphoxide

H2O2 :

Hydrogen peroxide

·OH:

Hydroxyle radical

LP:

Lipid peroxidation

NO:

Nitric oxide

NBT:

Nitroblue tetrasolium

ONOOCO2 − :

Nitrosoperoxocarboxylate adduct

ROS:

Reactive oxygen species

O2 − :

Superoxyde anion-radical

1O2 :

Singlet oxygen

SOD:

Superoxide dismutase

References

  1. Wallace SS (2002) Biological consequences of free radical-damaged DNA bases. Free Radic Biol Med 33:1–14

    Article  CAS  PubMed  Google Scholar 

  2. Neelu S, Renuka P (2011) Antioxidants: its beneficial role against health damaging free radical. World J Sci Technol 1:46–51

    Article  Google Scholar 

  3. Halliwell B (2007) Biochemistry of oxidative stress. Biochem Soc Trans 35:1147–1150

    Article  CAS  PubMed  Google Scholar 

  4. Kogan AKh, Kudrin AN, Kaktursky LV, Losev NL (1992) Free radical peroxide mechanisms of pathogenesis of ischemia and myocardial infarction. Pathoph Exp Terapia 2:5–15

    Google Scholar 

  5. Bolevich SB, Kogan AKh, Danilyak IG (1993) Changes in free radicals and possibility of their correction in patients with bronchial asthma. Vojnosanit Pregl 50:3–18

    Google Scholar 

  6. Pham-Huy LA, He H, Pham-Huy C (2008) Free radicals, antioxidants in disease and health. Int J Biomed Sci 4:89–96

    PubMed Central  CAS  PubMed  Google Scholar 

  7. Bahorun T, Soobrattee MA, Luximon-Ramma V, Aruoma OI (2006) Free radicals and antioxidants in cardiovascular health and disease. Int J Med Update 1:1–17

    Google Scholar 

  8. Grisham M, Granger DN (1988) Neutrophile-mediated mucosal injury. Role of reactive oxygen metabolites. Dig Dis Sci 3:69–158

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  10. Droge W (2002) Free radicals in the physiological control of cell function. Physiol Rev 82:47–95

    Article  CAS  PubMed  Google Scholar 

  11. Bellavite P (1988) The superoxide-forming enzymatic system of phagocytes. Free Radic Biol Med 4:225–261

    Article  CAS  PubMed  Google Scholar 

  12. Allen RC, Stjernholm RL, Steel R (1972) Evidence for the generation of on electronic excitation state(s) in human leukocytes and its participation in bactericidal activity. Biochem Biophys Res Commun 47:679–684

    Article  CAS  PubMed  Google Scholar 

  13. Allen RC, Loose LD (1976) Phagocyte activation of a liminol-dependent chemiiuminescence in rabbits alveolus and peritoneic macrophages. Bioch Biophys Commun 69:245–252

    Article  CAS  Google Scholar 

  14. Allred CD, Margetts I, Hill HR (1986) Luminol-induced neutrophil chemiluminescence. Biochim Biophys Acta 631:380–385

    Article  Google Scholar 

  15. Manturova NE, Silina EV, Stupin VA, Smirnova GO, Bolevich SB (2012) Free radical processes in the pathogenesis of involutional skin changes. Ter Arkh 84:75–78

    CAS  PubMed  Google Scholar 

  16. Webb LS, Keele Jr, BB, Johnston Jr RB (1974) Inhibition of phagocytosis-associated chemi luminescence by superoxide dismutase. Infect Immun 9:1051–1056

    PubMed Central  CAS  PubMed  Google Scholar 

  17. Rumiantseva SA, Fedin AI, Bolevich SB, Silina EV, Vasilev IuD, Menshova NI, Iliukhina OA, Goluzova IuN (2010) Effect of early correction of energy and free-radical homeostasis on the clinical-morphological presentation of cerebral infarction. Zh Nevrol Psikhiatr Im SS Korsakova 110:16–21

    CAS  Google Scholar 

  18. Ward G, Kelly CA, Stenton SC, Duddridge M, Hendrick DJ, Walters EH (1990) The relative contribution of bronchoalveolar macrophages and neutrophiles to lucigenin- and luminol-amplified chemiluminescence. Eur Respir J 3:8–14

    Google Scholar 

  19. Boener R, Boxer A, Davis J (1976) The biochemical basis of nitroblue tetrazolium reduction in normal human and chronic granulomatous disease polymorphonuclear leukocytes. Blood 48:309–313

    Google Scholar 

  20. Shopf RE, Matter X, Meyerburg Scheiner O, Hammann KP, Lemmel EM (1984) Measurement of the respiratory burst in human monocytes and polymorphonuclear leukocytes by nitroblue tetrazolium reduction and chemiluminescence. J Immunol Methods 67:109–117

    Article  Google Scholar 

  21. Mills EL, Rholl KS, Quie PG (1980) Luminol-amplified chemiluminescence: a sensitive method for detecting the carrier state in chronic granulomatous disease. J Clin Microbiol 12:52–56

    PubMed Central  CAS  PubMed  Google Scholar 

  22. Bolevich SB, Kogan AKh, Danilyak IG (1993) Comparative study of generation of active forms of oxygen by blood leukocytes and alveolar macrophages in patients with bronchial asthma. Vojnosanit Pregl 50:244–249

    Google Scholar 

  23. English D, Noufaim AA, Horan T, McPherson TA (1976) Quantitation of leukocyte chemiluminescence following phagocytosis: technical consideration using liquid scintillation spectrometry. In: Noujam AA, Weibe L, Ediss C (eds) Liquid scintillation, science and technology. Academic Press, New York, pp 227–242

    Google Scholar 

  24. Schneider WC, Hogebom GN (1950) Intracellular distribution of enzymes. J Biol Chem 183:123

    CAS  Google Scholar 

  25. Lowry OH, Rosenbrough NJ, Farr AL, Randall RX (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–276

    CAS  PubMed  Google Scholar 

  26. Klimenko OS, Sukachova LA (1980) Influence of carbon dioxide on respiration and phosphorilation in brain cortex and liver tissue. Ukr Biokhim Zh 52:240–243

    CAS  PubMed  Google Scholar 

  27. Kogan AKh, Manuilov BM, Grachev SV, Bolevich S, Tsypin AB, Daniliak IG (1994) CO2 as a natural inhibitor of reactive oxygen species generation by leukocytes. Biull Eksp Biol Med 10:395–398

    Google Scholar 

  28. Calamaras TD, Lee C, Lan F, Ido Y, Siwik DA, Colucci WS (2015) The lipid peroxidation product 4-hydroxy-trans-2-nonenal causes protein synthesis in cardiac myocytes via activated mTORC1-p70S6K-RPS6 signaling. Free Radic Biol Med 82:137–146

    Article  CAS  PubMed  Google Scholar 

  29. Radi R (2013) Peroxynitrite, a stealthy biological oxidant. J Biol Chem 288:26464–26472

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  30. Goldstein S, Merényi G (2008) The chemistry of peroxynitrite: implications for biological activity. Methods Enzymol 436:49–61

    Article  CAS  PubMed  Google Scholar 

  31. Lymar SV, Hurst JK (1995) Rapid reaction between peroxynitrite ion and carbon dioxide: implications for biological activity. J Am Chem Soc 117:8867–8868

    Article  CAS  Google Scholar 

  32. Denicola A, Freeman BA, Trujillo M, Radi R (1996) Peroxynitrite reaction with carbon dioxide/bicarbonate: kinetics and influence on peroxynitrite-mediated oxidations. Arch Biochem Biophys 333:49–58

    Article  CAS  PubMed  Google Scholar 

  33. Ferrer-Sueta G, Radi R (2009) Chemical biology of peroxynitrite: kinetics, diffusion, and radicals. ACS Chem Biol 4:161–177

    Article  CAS  PubMed  Google Scholar 

  34. Augusto O, Bonini MG, Amanso AM, Linares E, Santos CC, De Menezes SL (2002) Nitrogen dioxide and carbonate radical anion: two emerging radicals in biology. Free Radic Biol Med 32:841–859

    Article  CAS  PubMed  Google Scholar 

  35. Rutten M (1983) Origin of life. NAUKA, Moscow, pp 155–157

    Google Scholar 

  36. McElroy WD, Seliger HH, White EH (1969) Mechanism of bioluminescence, chemiluminescence and enzyme function in the oxidation of firefly luciferin. Photochem Photobiol 10:153–170

    Article  CAS  PubMed  Google Scholar 

  37. Reed KN, Wilson G, Pearsall A, Grishko VI (2014) The role of mitochondrial reactive oxygen species in cartilage matrix destruction. Mol Cell Biochem 397(1–2):195–201

    Article  CAS  PubMed  Google Scholar 

  38. Fridovich I (1995) Superoxide radical and superoxide dismutases. Annu Rev Biochem 64:97–112

    Article  CAS  PubMed  Google Scholar 

  39. Pommerville J (2014) Fundamentals of microbiology, 10th edn. Jones & Bartlett Learning, Burlington

    Google Scholar 

  40. Romano AH, Conway T (1996) Evolution of carbohydrate metabolic pathways. Res Microbiol 147:448–455

    Article  CAS  PubMed  Google Scholar 

  41. Ma XL, Tsao PS, Viehman GE, Lefer AM (1991) Neutrophil-mediated vasoconstriction and endothelial dysfunction in low-flow perfusion-reperfused cat coronary artery. Circ Res 69:95–106

    Article  CAS  PubMed  Google Scholar 

  42. Omar HA, Cherry PD, Mortelliti MP, Burke-Wolin T, Wolin MS (1991) Inhibition of coronary artery superoxide dismutase attenuates endothelium-dependent and independent nitrovasodilatation relaxation. Circ Res 69:601–608

    Article  CAS  PubMed  Google Scholar 

  43. Aminev FS (1963) Treatment of obliterating endoarteritis by subcutaneous injection of carbon dioxide. Zdravookhraneniye Kazakhstana 2:29–31

    Google Scholar 

  44. Bolevich SB (2006) Free radicals processes and bronchial asthma. MEDICINA, Moscow 256

    Google Scholar 

  45. Etheridge DM, Steele LP, Langenfelds RL, Francey RJ, Barnola JM, Morgan VI (1996) Natural and anthropogenic changes in atmospheric CO2 over the last 1000 years from air in Antarctic ice and firn. J Geophys Res 101:4115–4128

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Human Pathology, 1st Moscow State Medical University IM Sechenov, Moscow, Russia

    Sergey Bolevich, Alekandr Haritonovic Kogan, Aleksey Aleksejevic Novikov & Sergey Ivanovic Vorobyev

  2. Department of Physiology, Faculty of Medical Sciences, University of Kragujevac, Kragujevac, Serbia

    Vladimir Zivkovic & Vladimir Jakovljevic

  3. Department of Pharmacy, Faculty of Medical Sciences, University of Kragujevac, Kragujevac, Serbia

    Dusan Djuric

Authors
  1. Sergey Bolevich
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alekandr Haritonovic Kogan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vladimir Zivkovic
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dusan Djuric
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Aleksey Aleksejevic Novikov
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sergey Ivanovic Vorobyev
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Vladimir Jakovljevic
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Vladimir Jakovljevic.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interests relevant to the manuscript.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bolevich, S., Kogan, A.H., Zivkovic, V. et al. Protective role of carbon dioxide (CO2) in generation of reactive oxygen species. Mol Cell Biochem 411, 317–330 (2016). https://doi.org/10.1007/s11010-015-2594-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11010-015-2594-9

Keywords

Search

Navigation