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Glutathione S-transferase, catalase, and mitochondrial superoxide dismutase gene polymorphisms modulate redox potential in systemic lupus erythematosus patients from Manaus, Amazonas, Brazil

  • Original Article
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Clinical Rheumatology Aims and scope Submit manuscript

Abstract

Objective

To investigate the frequency of glutathione S-transferase (GST), catalase, and SOD2 genetic polymorphisms and their correlation with SLE.

Methods

A total of 290 females (patients = 151; controls= 139) were recruited. Multiplex PCR was performed for genotyping GSTM1 and GSTT1 genes, whereas real-time qPCR was used for determination of SNPs: CAT C262T, SOD2 C47T, GSTP1 A313G and GSTP1 IVS6 -C16T.

Results

Thiol levels are decreased in SLE patients (p<0.001), while MDA levels were significantly higher (p<0.001) and those carrying the polymorphisms had higher rates of oxidative stress. Patients with double null deletion GSTT1null/GSTM1null had a frequency almost five times higher than the controls (p<0.001, OR 4.81, CI 1.98–12.11). SLE patients had a lower wild-type frequency of SOD2CC allele compared to controls (12.4% vs 27.3%). Statistical significances were observed on the association between the GSTT1null and GSTM1null with SOD2mut (p<0.001, OR 0.15, CI 0.05–0.47), with GSTP1 A303G (p=0.012, OR 0.19, CI 0.05–0.69), and with GSTP1 IVS6 (p=0.008, OR 0.14, CI 0.03–0.63). The same was observed between SOD2 C47T with GSTP1 A303G (p=0.09, OR 0.27, CI 0.09–0.74) and GSTP1 IVS6 (p=0.036, OR 0.41, CI 0.18–0.92).

Conclusions

The deletion GSTT1null/GSTM1null may contribute to the increased of the oxidative stress in SLE patients. Isolated GSTP1 and CAT polymorphisms do not seem to influence the increased oxidative stress, neither SLE clinical manifestations. SOD2 47CT/TT allele may have greater oxidative stress due to structural change in the protein and decreased H2O2 production. The combination of polymorphic genes may be involved in the pathogenesis of the disease.

Key points

• Major question of our paper: Many studies have shown that the antioxidant status levels are decreased in patients with SLE, especially in severe stages of disease. We believe that this paper will be of interest to the readership of your journal had the involvement of polymorphisms and mutations in several genes that contribute to the genetic etiology of SLE, suggesting that these may influence the mechanisms of disease.

• Our results. Thiol level was significantly (p<.001) lower and MDA level significantly increased (p<.001) among SLE patients. Those carrying the polymorphisms had higher rates of oxidative stress. SLE Patients had a frequency almost five times higher of double null deletion GSTT1null/GSTM1null than the controls. SLE Patients had a lower wild type frequency of SOD2CC allele compared to controls (12.4% vs 27.3%). We believed the deletion GSTT1null/GSTM1null may contribute to the increased of the oxidative stress in SLE patients while carriers of the mutant SOD2 47CT/TT allele may have greater oxidative stress due to structural change in the protein and decreased H2O2 production. The combination of polymorphic genes may be involved in the pathogenesis of the disease.

• Implications of our results: Evidence for the involvement of genetic factors in severe clinical to lupus is compelling. This manuscript shows genetic insights in pathogenic pathways that may lead to severe clinical implications to LES. Therefore, it is necessary to understand their impact on overall disease pathogenesis and prognosis in these patients. We understand from general consensus about environmental factors can modify disease, however, maybe just in individuals who have a permissive genetic background. Even that no single gene predisposes some individuals to LES, we believe the genetic factors described in this manuscript are important elements in susceptibility to severe clinical to LES

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Acknowledgments

The authors wish to thank all blood donors attending the FHEMOAM for contributing and participating in this study. Also, the authors thank the staff of the Molecular Biology Laboratory of the Federal University of Amazonas (UFAM) and Gonçalo Moniz Institute (IGM) (FIOCRUZ/BAHIA) for the technical support. Finally, the authors thank the Foundation for Research Support of the State of Amazonas (FAPEAM) for financial support. The sponsors of this study are public or nonprofit organizations that support science in general. They had no role in gathering, analyzing, or interpreting the data.

Funding

Financial support was provided by grants from the Fundação de Amparo à Pesquisa do Estado do Amazonas (FAPEAM)–Processo: 1094/2013-FAPEAM and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Authors and Affiliations

  1. Faculdade de Ciências Farmacêuticas, Universidade Federal do Amazonas, Avenida General Rodrigo Otávio Jordão Ramos 6200 - Coroado, Manaus - AM, CEP: 69067-005, Brazil

    Marco Aurélio Almeida de Oliveira, Neila Hiraishi Mallmann, Giselle Katiane Bonfim Bacellar de Souza, Thiago de Jesus Bacha & Emerson Silva Lima

  2. Faculdade de Medicina, Universidade Federal do Amazonas, Manaus, Amazonas, Brazil

    Domingos Sávio Nunes de Lima & Luiz Fernando de Souza Passos

  3. Centro de Pesquisas Gonçalo Moniz, Fundação Oswaldo Cruz, Salvador, Bahia, Brazil

    Marilda de Souza Gonçalves

  4. Faculdade de Ciências Farmacêuticas, Universidade Federal do Amazonas, Manaus, Amazonas, Brazil

    José Pereira de Moura Neto

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Correspondence to José Pereira de Moura Neto.

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de Oliveira, M.A.A., Mallmann, N.H., de Souza, G.K.B.B. et al. Glutathione S-transferase, catalase, and mitochondrial superoxide dismutase gene polymorphisms modulate redox potential in systemic lupus erythematosus patients from Manaus, Amazonas, Brazil. Clin Rheumatol 40, 3639–3649 (2021). https://doi.org/10.1007/s10067-021-05680-0

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