The association of rheumatoid arthritis with glucose- 6-phosphate dehydrogenase deficiency—results from a case-control study. G6PD and Rheumatoid Arthritis
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Keywords
Glucose-6-phosphate dehydrogenase deficiency, autoimmunity, oxidative stress, inflammation, connective tissue-diseases
Abstract
Carriers of G6PD deficiency were at an increased risk of RA. This finding opens new windows to better understanding the RA pathogenesis.
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References
1. Goss SJ, Harris H. Gene transfer by means of cell fusion I. Statistical mapping of the human X-chromosome by analysis of radiation-induced gene segregation. J Cell Sci. Jun 1977;25:17-37. doi:10.1242/jcs.25.1.17
2. Weiss SJ. The role of superoxide in the destruction of erythrocyte targets by human neutrophils. J Biol Chem. Oct 25 1980;255(20):9912-7.
3. Luzzatto L, Ally M, Notaro R. Glucose-6-phosphate dehydrogenase deficiency. Blood. Sep 10 2020;136(11):1225-1240. doi:10.1182/blood.2019000944
4. Parsanathan R, Jain SK. Glucose-6-phosphate dehydrogenase (G6PD) deficiency is linked with cardiovascular disease. Hypertens Res. Jun 2020;43(6):582-584. doi:10.1038/s41440-020-0402-8
5. Bocchetta A. Psychotic mania in glucose-6-phosphate-dehydrogenase-deficient subjects. Ann Gen Hosp Psychiatry. Jun 13 2003;2(1):6. doi:10.1186/1475-2832-2-6
6. Israel A, Schäffer AA, Berkovitch M, et al. Glucose-6-phosphate dehydrogenase deficiency and long-term risk of immune-related disorders. Original Research. Frontiers in Immunology. 2023-September-11 2023;14doi:10.3389/fimmu.2023.1232560
7. Dore MP, Fanciulli G, Pes GM. Is Glucose-6-Phosphate Dehydrogenase Deficiency a Risk Factor for Autoimmune Thyroid Disease? A Retrospective Case-Control Study. Int J Environ Res Public Health. Feb 3 2023;20(3)doi:10.3390/ijerph20032709
8. Erre GL, Mameli G, Cossu D, et al. Increased Epstein-Barr Virus DNA Load and Antibodies Against EBNA1 and EA in Sardinian Patients with Rheumatoid Arthritis. Viral Immunol. Sep 2015;28(7):385-90. doi:10.1089/vim.2015.0035
9. Mangoni AA, Tommasi S, Sotgia S, et al. Asymmetric Dimethylarginine: a Key Player in the Pathophysiology of Endothelial Dysfunction, Vascular Inflammation and Atherosclerosis in Rheumatoid Arthritis? Curr Pharm Des. 2021;27(18):2131-2140. doi:10.2174/1381612827666210106144247
10. Bo M, Erre GL, Bach H, et al. PtpA and PknG Proteins Secreted by Mycobacterium avium subsp. paratuberculosis are Recognized by Sera from Patients with Rheumatoid Arthritis: A Case-Control Study. J Inflamm Res. 2019;12:301-308. doi:10.2147/JIR.S220960
11. England BR, Thiele GM, Anderson DR, Mikuls TR. Increased cardiovascular risk in rheumatoid arthritis: mechanisms and implications. BMJ. Apr 23 2018;361:k1036. doi:10.1136/bmj.k1036
12. Gardi C, Bauerova K, Stringa B, et al. Quercetin reduced inflammation and increased antioxidant defense in rat adjuvant arthritis. Arch Biochem Biophys. Oct 1 2015;583:150-7. doi:10.1016/j.abb.2015.08.008
13. Wruck CJ, Fragoulis A, Gurzynski A, et al. Role of oxidative stress in rheumatoid arthritis: insights from the Nrf2-knockout mice. Ann Rheum Dis. May 2011;70(5):844-50. doi:10.1136/ard.2010.132720
14. Hassan MQ, Hadi RA, Al-Rawi ZS, Padron VA, Stohs SJ. The glutathione defense system in the pathogenesis of rheumatoid arthritis. J Appl Toxicol. Jan-Feb 2001;21(1):69-73. doi:10.1002/jat.736
15. Fiorelli G, Meloni T, Palomba V, Manoussakis C, Villa S, Cappellini MD. Gene frequency of glucose-6-phosphate dehydrogenase (G6PD) polymorphic variants in Sardinia. Gene Geogr. Dec 1990;4(3):139-42.
16. De Vita G, Alcalay M, Sampietro M, Cappelini MD, Fiorelli G, Toniolo D. Two point mutations are responsible for G6PD polymorphism in Sardinia. Am J Hum Genet. Feb 1989;44(2):233-40.
17. Sardu C, Cocco E, Mereu A, et al. Population based study of 12 autoimmune diseases in Sardinia, Italy: prevalence and comorbidity. PLoS One. 2012;7(3):e32487. doi:10.1371/journal.pone.0032487
18. Rossini M, Rossi E, Bernardi D, et al. Prevalence and incidence of rheumatoid arthritis in Italy. Rheumatol Int. May 2014;34(5):659-64. doi:10.1007/s00296-014-2974-6
19. Aletaha D, Neogi T, Silman AJ, et al. 2010 Rheumatoid arthritis classification criteria: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Arthritis Rheum. Sep 2010;62(9):2569-81. doi:10.1002/art.27584
20. Arnett FC, Edworthy SM, Bloch DA, et al. The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum. Mar 1988;31(3):315-24. doi:10.1002/art.1780310302
21. Bampton JL, Cawston TE, Kyle MV, Hazleman BL. Measurement of rheumatoid factors by an enzyme-linked immunosorbent assay (ELISA) and comparison with other methods. Ann Rheum Dis. Jan 1985;44(1):13-9. doi:10.1136/ard.44.1.13
22. Mosca A, Paleari R, Rosti E, et al. Simultaneous automated determination of glucose 6-phosphate dehydrogenase and 6-phosphogluconate dehydrogenase activities in whole blood. Eur J Clin Chem Clin Biochem. May 1996;34(5):431-8. doi:10.1515/cclm.1996.34.5.431
23. Pes GM, Errigo A, Bitti A, Dore MP. Effect of age, period and birth-cohort on the frequency of glucose-6-phosphate dehydrogenase deficiency in Sardinian adults. Ann Med. Feb 2018;50(1):68-73. doi:10.1080/07853890.2017.1390247
24. Li P, Stuart EA, Allison DB. Multiple Imputation: A Flexible Tool for Handling Missing Data. JAMA. Nov 10 2015;314(18):1966-7. doi:10.1001/jama.2015.15281
25. Dore MP, Portoghese M, Pes GM. The Elderly with Glucose-6-Phosphate Dehydrogenase Deficiency are More Susceptible to Cardiovascular Disease. J Atheroscler Thromb. Jun 1 2021;28(6):604-610. doi:10.5551/jat.56531
26. Gheita TA, Kenawy SA, El Sisi RW, Gheita HA, Khalil H. Subclinical reduced G6PD activity in rheumatoid arthritis and Sjogren's Syndrome patients: relation to clinical characteristics, disease activity and metabolic syndrome. Mod Rheumatol. Jul 2014;24(4):612-7. doi:10.3109/14397595.2013.851639
27. Errigo A, Bitti A, Galistu F, Salis R, Pes GM, Dore MP. Relationship between Glucose-6-Phosphate Dehydrogenase Deficiency, X-Chromosome Inactivation and Inflammatory Markers. Antioxidants (Basel). Jan 31 2023;12(2)doi:10.3390/antiox12020334
28. Filippin LI, Vercelino R, Marroni NP, Xavier RM. Redox signalling and the inflammatory response in rheumatoid arthritis. Clin Exp Immunol. Jun 2008;152(3):415-22. doi:10.1111/j.1365-2249.2008.03634.x
29. Quinonez-Flores CM, Gonzalez-Chavez SA, Del Rio Najera D, Pacheco-Tena C. Oxidative Stress Relevance in the Pathogenesis of the Rheumatoid Arthritis: A Systematic Review. Biomed Res Int. 2016;2016:6097417. doi:10.1155/2016/6097417
30. Wang X, Fan D, Cao X, et al. The Role of Reactive Oxygen Species in the Rheumatoid Arthritis-Associated Synovial Microenvironment. Antioxidants (Basel). Jun 13 2022;11(6)doi:10.3390/antiox11061153
31. Hadjigogos K. The role of free radicals in the pathogenesis of rheumatoid arthritis. Panminerva Med. Mar 2003;45(1):7-13.
32. TeSlaa T, Ralser M, Fan J, Rabinowitz JD. The pentose phosphate pathway in health and disease. Nat Metab. Aug 2023;5(8):1275-1289. doi:10.1038/s42255-023-00863-2
33. Kalpakcioglu B, Senel K. The interrelation of glutathione reductase, catalase, glutathione peroxidase, superoxide dismutase, and glucose-6-phosphate in the pathogenesis of rheumatoid arthritis. Clin Rheumatol. Feb 2008;27(2):141-5. doi:10.1007/s10067-007-0746-3
34. Sanna F, Bonatesta RR, Frongia B, et al. Production of inflammatory molecules in peripheral blood mononuclear cells from severely glucose-6-phosphate dehydrogenase-deficient subjects. J Vasc Res. 2007;44(4):253-63. doi:10.1159/000100903
35. Bira Y, Tani K, Nishioka Y, et al. Transforming growth factor beta stimulates rheumatoid synovial fibroblasts via the type II receptor. Mod Rheumatol. 2005;15(2):108-13. doi:10.1007/s10165-004-0378-2
36. Dore MP, Vidili G, Marras G, Assy S, Pes GM. Inverse Association between Glucose‒6‒Phosphate Dehydrogenase Deficiency and Hepatocellular Carcinoma. Asian Pac J Cancer Prev. Apr 27 2018;19(4):1069-1073. doi:10.22034/APJCP.2018.19.4.1069
2. Weiss SJ. The role of superoxide in the destruction of erythrocyte targets by human neutrophils. J Biol Chem. Oct 25 1980;255(20):9912-7.
3. Luzzatto L, Ally M, Notaro R. Glucose-6-phosphate dehydrogenase deficiency. Blood. Sep 10 2020;136(11):1225-1240. doi:10.1182/blood.2019000944
4. Parsanathan R, Jain SK. Glucose-6-phosphate dehydrogenase (G6PD) deficiency is linked with cardiovascular disease. Hypertens Res. Jun 2020;43(6):582-584. doi:10.1038/s41440-020-0402-8
5. Bocchetta A. Psychotic mania in glucose-6-phosphate-dehydrogenase-deficient subjects. Ann Gen Hosp Psychiatry. Jun 13 2003;2(1):6. doi:10.1186/1475-2832-2-6
6. Israel A, Schäffer AA, Berkovitch M, et al. Glucose-6-phosphate dehydrogenase deficiency and long-term risk of immune-related disorders. Original Research. Frontiers in Immunology. 2023-September-11 2023;14doi:10.3389/fimmu.2023.1232560
7. Dore MP, Fanciulli G, Pes GM. Is Glucose-6-Phosphate Dehydrogenase Deficiency a Risk Factor for Autoimmune Thyroid Disease? A Retrospective Case-Control Study. Int J Environ Res Public Health. Feb 3 2023;20(3)doi:10.3390/ijerph20032709
8. Erre GL, Mameli G, Cossu D, et al. Increased Epstein-Barr Virus DNA Load and Antibodies Against EBNA1 and EA in Sardinian Patients with Rheumatoid Arthritis. Viral Immunol. Sep 2015;28(7):385-90. doi:10.1089/vim.2015.0035
9. Mangoni AA, Tommasi S, Sotgia S, et al. Asymmetric Dimethylarginine: a Key Player in the Pathophysiology of Endothelial Dysfunction, Vascular Inflammation and Atherosclerosis in Rheumatoid Arthritis? Curr Pharm Des. 2021;27(18):2131-2140. doi:10.2174/1381612827666210106144247
10. Bo M, Erre GL, Bach H, et al. PtpA and PknG Proteins Secreted by Mycobacterium avium subsp. paratuberculosis are Recognized by Sera from Patients with Rheumatoid Arthritis: A Case-Control Study. J Inflamm Res. 2019;12:301-308. doi:10.2147/JIR.S220960
11. England BR, Thiele GM, Anderson DR, Mikuls TR. Increased cardiovascular risk in rheumatoid arthritis: mechanisms and implications. BMJ. Apr 23 2018;361:k1036. doi:10.1136/bmj.k1036
12. Gardi C, Bauerova K, Stringa B, et al. Quercetin reduced inflammation and increased antioxidant defense in rat adjuvant arthritis. Arch Biochem Biophys. Oct 1 2015;583:150-7. doi:10.1016/j.abb.2015.08.008
13. Wruck CJ, Fragoulis A, Gurzynski A, et al. Role of oxidative stress in rheumatoid arthritis: insights from the Nrf2-knockout mice. Ann Rheum Dis. May 2011;70(5):844-50. doi:10.1136/ard.2010.132720
14. Hassan MQ, Hadi RA, Al-Rawi ZS, Padron VA, Stohs SJ. The glutathione defense system in the pathogenesis of rheumatoid arthritis. J Appl Toxicol. Jan-Feb 2001;21(1):69-73. doi:10.1002/jat.736
15. Fiorelli G, Meloni T, Palomba V, Manoussakis C, Villa S, Cappellini MD. Gene frequency of glucose-6-phosphate dehydrogenase (G6PD) polymorphic variants in Sardinia. Gene Geogr. Dec 1990;4(3):139-42.
16. De Vita G, Alcalay M, Sampietro M, Cappelini MD, Fiorelli G, Toniolo D. Two point mutations are responsible for G6PD polymorphism in Sardinia. Am J Hum Genet. Feb 1989;44(2):233-40.
17. Sardu C, Cocco E, Mereu A, et al. Population based study of 12 autoimmune diseases in Sardinia, Italy: prevalence and comorbidity. PLoS One. 2012;7(3):e32487. doi:10.1371/journal.pone.0032487
18. Rossini M, Rossi E, Bernardi D, et al. Prevalence and incidence of rheumatoid arthritis in Italy. Rheumatol Int. May 2014;34(5):659-64. doi:10.1007/s00296-014-2974-6
19. Aletaha D, Neogi T, Silman AJ, et al. 2010 Rheumatoid arthritis classification criteria: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Arthritis Rheum. Sep 2010;62(9):2569-81. doi:10.1002/art.27584
20. Arnett FC, Edworthy SM, Bloch DA, et al. The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum. Mar 1988;31(3):315-24. doi:10.1002/art.1780310302
21. Bampton JL, Cawston TE, Kyle MV, Hazleman BL. Measurement of rheumatoid factors by an enzyme-linked immunosorbent assay (ELISA) and comparison with other methods. Ann Rheum Dis. Jan 1985;44(1):13-9. doi:10.1136/ard.44.1.13
22. Mosca A, Paleari R, Rosti E, et al. Simultaneous automated determination of glucose 6-phosphate dehydrogenase and 6-phosphogluconate dehydrogenase activities in whole blood. Eur J Clin Chem Clin Biochem. May 1996;34(5):431-8. doi:10.1515/cclm.1996.34.5.431
23. Pes GM, Errigo A, Bitti A, Dore MP. Effect of age, period and birth-cohort on the frequency of glucose-6-phosphate dehydrogenase deficiency in Sardinian adults. Ann Med. Feb 2018;50(1):68-73. doi:10.1080/07853890.2017.1390247
24. Li P, Stuart EA, Allison DB. Multiple Imputation: A Flexible Tool for Handling Missing Data. JAMA. Nov 10 2015;314(18):1966-7. doi:10.1001/jama.2015.15281
25. Dore MP, Portoghese M, Pes GM. The Elderly with Glucose-6-Phosphate Dehydrogenase Deficiency are More Susceptible to Cardiovascular Disease. J Atheroscler Thromb. Jun 1 2021;28(6):604-610. doi:10.5551/jat.56531
26. Gheita TA, Kenawy SA, El Sisi RW, Gheita HA, Khalil H. Subclinical reduced G6PD activity in rheumatoid arthritis and Sjogren's Syndrome patients: relation to clinical characteristics, disease activity and metabolic syndrome. Mod Rheumatol. Jul 2014;24(4):612-7. doi:10.3109/14397595.2013.851639
27. Errigo A, Bitti A, Galistu F, Salis R, Pes GM, Dore MP. Relationship between Glucose-6-Phosphate Dehydrogenase Deficiency, X-Chromosome Inactivation and Inflammatory Markers. Antioxidants (Basel). Jan 31 2023;12(2)doi:10.3390/antiox12020334
28. Filippin LI, Vercelino R, Marroni NP, Xavier RM. Redox signalling and the inflammatory response in rheumatoid arthritis. Clin Exp Immunol. Jun 2008;152(3):415-22. doi:10.1111/j.1365-2249.2008.03634.x
29. Quinonez-Flores CM, Gonzalez-Chavez SA, Del Rio Najera D, Pacheco-Tena C. Oxidative Stress Relevance in the Pathogenesis of the Rheumatoid Arthritis: A Systematic Review. Biomed Res Int. 2016;2016:6097417. doi:10.1155/2016/6097417
30. Wang X, Fan D, Cao X, et al. The Role of Reactive Oxygen Species in the Rheumatoid Arthritis-Associated Synovial Microenvironment. Antioxidants (Basel). Jun 13 2022;11(6)doi:10.3390/antiox11061153
31. Hadjigogos K. The role of free radicals in the pathogenesis of rheumatoid arthritis. Panminerva Med. Mar 2003;45(1):7-13.
32. TeSlaa T, Ralser M, Fan J, Rabinowitz JD. The pentose phosphate pathway in health and disease. Nat Metab. Aug 2023;5(8):1275-1289. doi:10.1038/s42255-023-00863-2
33. Kalpakcioglu B, Senel K. The interrelation of glutathione reductase, catalase, glutathione peroxidase, superoxide dismutase, and glucose-6-phosphate in the pathogenesis of rheumatoid arthritis. Clin Rheumatol. Feb 2008;27(2):141-5. doi:10.1007/s10067-007-0746-3
34. Sanna F, Bonatesta RR, Frongia B, et al. Production of inflammatory molecules in peripheral blood mononuclear cells from severely glucose-6-phosphate dehydrogenase-deficient subjects. J Vasc Res. 2007;44(4):253-63. doi:10.1159/000100903
35. Bira Y, Tani K, Nishioka Y, et al. Transforming growth factor beta stimulates rheumatoid synovial fibroblasts via the type II receptor. Mod Rheumatol. 2005;15(2):108-13. doi:10.1007/s10165-004-0378-2
36. Dore MP, Vidili G, Marras G, Assy S, Pes GM. Inverse Association between Glucose‒6‒Phosphate Dehydrogenase Deficiency and Hepatocellular Carcinoma. Asian Pac J Cancer Prev. Apr 27 2018;19(4):1069-1073. doi:10.22034/APJCP.2018.19.4.1069