Skip to main content

Advertisement

SpringerLink
Log in

Correlation of oxidant status with oxidative tissue damage in patients with rheumatoid arthritis

  • Original Article
  • Published:
Clinical Rheumatology Aims and scope Submit manuscript

Abstract

Rheumatoid arthritis (RA) is a debilitating autoimmune disease whose etiology remains unknown, but studies have consistently implicated a plethora of inflammatory mechanisms culminating in chronic symmetric and erosive synovitis. Importantly, reactive oxygen species (ROS) have been attributed to directly contribute towards the destructive, proliferative synovitis evident in RA. Accordingly, this study aimed to establish whether the degree of oxidative stress and disease activity score (DAS28) correlated with the downstream effects of oxidative damage. The redox status of neutrophils sourced from synovial fluid (SF) was measured by flow cytometry in terms of total ROS and hydroxyl radicals. Among the molecular damage markers, protein carbonylation and lipid peroxidation were detected by spectrophotometry and S-nitrosothiols by fluorimetry. Neutrophils constituted the major cellular component of the SF of patients with RA and their levels of ROS and hydroxyl radicals correlated strongly with protein carbonylation and lipid peroxidation. However, all the oxidative damage markers correlated positively with DAS28. Taken together, in patients with RA, the strong correlation between levels of ROS and DAS28 with markers of oxidative damage suggests that measurement of oxidative stress could serve as a biomarker for monitoring disease severity in RA.

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
Fig. 4

Similar content being viewed by others

References

  1. Filippin LI, Vercelino R, Marroni NP, Xavier RM (2008) Redox signaling and the inflammatory response in rheumatoid arthritis. Clin Exp Immunol 152:415–422

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  2. Mirshafiey A, Mohsenzadegan M (2008) The role of reactive oxygen species in immunopathogenesis of rheumatoid arthritis. Iran J Allergy Asthma Immunol 7:195–202

    PubMed  CAS  Google Scholar 

  3. Goldsby RA, Kindt TJ, Osborne BA, Kuby J (2003) Leukocyte migration and inflammation. In: Immunology, 5th edn. WH Freeman, New York, pp 338–358

    Google Scholar 

  4. Dalle-Donne I, Rossi R, Colombo R, Giustarini D, Milzani A (2006) Biomarkers of oxidative damage in human disease. Clin Chem 52:601–623

    Article  PubMed  CAS  Google Scholar 

  5. Forman HJ, Fukuto JM, Torres M (2004) Redox signaling: thiol chemistry defines which reactive oxygen and nitrogen species can act as second messengers. Am J Physiol Cell Physiol 287:C246–C256

    Article  PubMed  CAS  Google Scholar 

  6. Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Fries JF, Cooper NS et al (1988) The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 31:315–324

    Article  PubMed  CAS  Google Scholar 

  7. van der Linden MP, Batstra MR, Bakker-Jonges LE (2011) Towards a data-driven evaluation of the 2010 American College of Rheumatology/European League Against Rheumatism criteria for rheumatoid arthritis: is it sensible to look at levels of rheumatoid factor? Arthritis Rheum 63:1190–1199

    Article  PubMed  Google Scholar 

  8. van Gestel AM, Haagsma CJ, van Riel PL (1998) Validation of rheumatoid arthritis improvement criteria that include simplified joint counts. Arthritis Rheum 41:1845–1850

    Article  PubMed  Google Scholar 

  9. Mandal G, Wyllie S, Singh N, Sundar S, Fairlamb AH, Chatterjee M (2007) Increased levels of thiols protect antimony unresponsive Leishmania donovani field isolates against reactive oxygen species generated by trivalent antimony. Parasitology 134:1679–1687

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  10. Kundu S, Ghosh P, Datta S, Ghosh A, Chattopadhyay S, Chatterjee M (2012) Oxidative stress as a potential biomarker for determining disease activity in patients with Rheumatoid Arthritis. Free Radic Res 46:1482–1489

    Article  PubMed  CAS  Google Scholar 

  11. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    PubMed  CAS  Google Scholar 

  12. Guilpain P, Chéreau C, Goulvestre C, Servettaz A, Montani D, Tamas N, Pagnoux C, Hachulla E, Weill B, Guillevin L, Mouthon L, Batteux F (2011) The oxidation induced by anti myeloperoxidase antibodies triggers fibrosis in microscopic polyangiitis. Eur Respir J 37:1503–1513

    Article  PubMed  CAS  Google Scholar 

  13. Firuzi O, Fuksa L, Spadaro C, Bousová I, Riccieri V, Spadaro A, Petrucci R, Marrosu G, Saso L (2006) Oxidative stress parameters in different systemic rheumatic diseases. J Pharm Pharmacol 58:951–957

    Article  PubMed  CAS  Google Scholar 

  14. Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz AG, Shalfier S, Stadtman ER (1990) Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol 186:464–478

    Article  PubMed  CAS  Google Scholar 

  15. Mantle D, Falkous G, Walker D (1999) Quantification of protease activities in synovial fluid from rheumatoid and osteoarthritis cases: comparison with antioxidant and free radical damage markers. Clin Chim Acta 284:45–58

    Article  PubMed  CAS  Google Scholar 

  16. Marzinzig M, Nussler AK, Stadler J, Marzinzig E, Barthen W, Nussler NC, Beger HG, Morris SM Jr, Brückner UB (1997) Improved methods to measure end products of nitric oxide in biological fluids: nitrite, nitrate, and S-nitrosothiols. Nitric Oxide 1:177–189

    Article  PubMed  CAS  Google Scholar 

  17. Beuge JA, Aust SD (1978) Microsomal lipid peroxidation. Methods Enzymol 52:302–310

    Article  Google Scholar 

  18. Seven A, Güzel S, Aslan M, Hamuryudan V (2008) Lipid, protein, DNA oxidation and antioxidant status in rheumatoid arthritis. Clin Biochem 41:538–543

    Article  PubMed  CAS  Google Scholar 

  19. Kundu S, Bala A, Ghosh P, Mukhopadhyay D, Mitra A, Sarkar A, Bauri AK, Ghosh A, Chattopadhyay S, Chatterjee M (2011) Attenuation of oxidative stress by allylpyrocatechol in synovial cellular infiltrate of patients with Rheumatoid Arthritis. Free Radic Res 45:518–526

    Article  PubMed  CAS  Google Scholar 

  20. Santulli P, Borghese B, Lemaréchal H, Leconte M, Millischer AE, Batteux F, Chapron C, Borderie D (2013) Increased serum oxidative stress markers in women with uterine leiomyoma. 36. PLoS One 8:e72069

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  21. Stalmer JS, Singel DJ, Loscalzo J (1992) Biochemistry of nitric oxide and its redox-activated forms. Science 258:1898–1902

    Article  Google Scholar 

  22. Mylonas C, Kouretas D (1999) Lipid peroxidation and tissue damage. In Vivo 13:295–309

    PubMed  CAS  Google Scholar 

  23. Halliwell B (2007) Free radicals in biology and medicine. Oxford University Press, New York

    Google Scholar 

  24. Dhiman M, Coronado YA, Vallejo CK, Petersen JR, Ejilemele A, Nuñez S, Zago MP, Spratt H, Garg NJ (2013) Innate immune responses and antioxidant/oxidant imbalance are major determinants of human Chagas disease. PLoS Negl Trop Dis 7:e2364

    Article  PubMed  PubMed Central  Google Scholar 

  25. Chang D, Zhang X, Rong S, Sha Q, Liu P, Han T, Pan H (2013) Serum antioxidative enzymes levels and oxidative stress products in age-related cataract patients. Oxidative Med Cell Longev. doi:10.1155/2013/587826

    Google Scholar 

  26. Bansal S, Chawla D, Siddarth M, Banerjee BD, Madhu SV, Tripathi AK (2013) A study on serum advanced glycation end products and its association with oxidative stress and paraoxonase activity in type 2 diabetic patients with vascular complications. Clin Biochem 46:109–114

    Article  PubMed  CAS  Google Scholar 

  27. Yang XH, Liu X, Shang J, Liu HG, Xu YJ (2013) Correlation between the serum level of advanced oxidation protein products and the cognitive function in patients with obstructive sleep apnea hypopnea syndrome. Zhonghua Jie He He Hu Xi Za Zhi 36:274–279

    PubMed  Google Scholar 

  28. Dalle-Donne I, Giustarini D, Colombo R, Rossi R, Milzani A (2003) Protein carbonylation in human diseases. Trends Mol Med 9:169–176

    Article  PubMed  CAS  Google Scholar 

  29. Bhattacharya S, Mula S, Gamre S, Kamat JP, Bandyopadhyay SK, Chattopadhyay S (2007) Inhibitory property of Piper betel extract against photosensitization-induced damages to lipids and proteins. Food Chem 100:1474–1480

    Article  CAS  Google Scholar 

  30. Mahmoud AA, Ismail MA (2011) Serum protein carbonyl content, total thiol and nitric oxide in patients with rheumatoid arthritis. J Am Sci 7:683–686

    Google Scholar 

  31. Marin DP, Bolin AP, dos Santos RC, Curi R, Otton R (2010) Testosterone suppresses oxidative stress in human neutrophils. Cell Biochem Funct 28:394–402

    Article  PubMed  CAS  Google Scholar 

  32. Roy S, Sannigrahi S, Vaddepalli RP, Ghosh B, Pusp P (2012) A novel combination of methotrexate and epigallocatechin attenuates the overexpression of pro-inflammatory cartilage cytokines and modulates antioxidant status in adjuvant arthritic rats. Inflammation 35:1435–1447

    Article  PubMed  CAS  Google Scholar 

  33. Drafi F, Bauerova K, Kuncirova V, Ponist S, Mihalova D, Fedorova T, Harmatha J, Nosal R (2012) Pharmacological influence on processes of adjuvant arthritis: effect of the combination of an antioxidant active substance with methotrexate. Interdiscip Toxicol 5:84–91

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  34. Banji D, Pinnapureddy J, Banji OJ, Saidulu A, Hayath MS (2011) Synergistic activity of curcumin with methotrexate in ameliorating Freund’s complete adjuvant induced arthritis with reduced hepatotoxicity in experimental animals. Eur J Pharmacol 668:293–298

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Financial assistance was provided by the Department of Biotechnology, Govt. of India. SK is a recipient of Senior Research Fellowship from Indian Council of Medical Research, Govt. of India.

Disclosures

None.

Author information

Authors and Affiliations

  1. Department of Pharmacology, Institute of Post Graduate Medical Education and Research, 244 B Acharya JC Bose Road, Kolkata, 700 020, India

    Suhana Datta, Sunanda Kundu, Soumita De & Mitali Chatterjee

  2. Department Rheumatology and Clinical Immunology, Institute of Post Graduate Medical Education and Research, 244 B Acharya JC Bose Road, Kolkata, 700 020, India

    Parasar Ghosh & Alakendu Ghosh

Authors
  1. Suhana Datta
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sunanda Kundu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Parasar Ghosh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Soumita De
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Alakendu Ghosh
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mitali Chatterjee
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mitali Chatterjee.

Additional information

Suhana Datta and Sunanda Kundu contributed equally to this work and are considered as joint first authors.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Datta, S., Kundu, S., Ghosh, P. et al. Correlation of oxidant status with oxidative tissue damage in patients with rheumatoid arthritis. Clin Rheumatol 33, 1557–1564 (2014). https://doi.org/10.1007/s10067-014-2597-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10067-014-2597-z

Keywords

Search

Navigation