Rheumatoid arthritis: the role of reactive oxygen species in disease development and therapeutic strategies.

Autoimmune diseases such as rheumatoid arthritis (RA) are chronic diseases that cannot be prevented or cured If the pathologic basis of such disease would be known, it might be easier to develop new drugs interfering with critical pathway. Genetic analysis of animal models for autoimmune diseases can result in discovery of proteins and pathways that play key function in pathogenesis, which may provide rationales for new therapeutic strategies. Currently, only the MHC class II is clearly associated with human RA and animal models for RA. However, recent data from rats and mice with a polymorphism in Ncf1, a member of the NADPH oxidase complex, indicate a role for oxidative burst in protection from arthritis. Oxidative burst-activating substances can treat and prevent arthritis in rats, as efficiently as clinically applied drugs, suggesting a novel pathway to a therapeutic target in human RA. Here, the authors discuss the role of oxygen radicals in regulating the immune system and autoimmune disease. It is proposed that reactive oxygen species set the threshold for T cell activation and thereby regulate chronic autoimmune inflammatory diseases like RA. In the light of this new hypothesis, new possibilities for preventive and therapeutic treatment of chronic inflammatory diseases are discussed.

[1]  B. Babior NADPH Oxidase: An Update , 1999 .

[2]  K. Krause,et al.  A Ca2+-activated NADPH Oxidase in Testis, Spleen, and Lymph Nodes* , 2001, The Journal of Biological Chemistry.

[3]  Jorge R. Oksenberg,et al.  The Influence of the Proinflammatory Cytokine, Osteopontin, on Autoimmune Demyelinating Disease , 2001, Science.

[4]  K. Schulze-Osthoff,et al.  Enhancement of T Cell Receptor Signaling by a Mild Oxidative Shift in the Intracellular Thiol Pool1 , 2000, The Journal of Immunology.

[5]  T Nose,et al.  Role of Src homology 3 domains in assembly and activation of the phagocyte NADPH oxidase. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[6]  R. Holmdahl,et al.  Maintained pregnancy levels of oestrogen afford complete protection from post‐partum exacerbation of collagen‐induced arthritis , 1991, Clinical and experimental immunology.

[7]  R. Holmdahl,et al.  T lymphocytes are not required for the spontaneous development of entheseal ossification leading to marginal ankylosis in the DBA/1 mouse. , 2000, Arthritis and rheumatism.

[8]  Steven J. Schrodi,et al.  A missense single-nucleotide polymorphism in a gene encoding a protein tyrosine phosphatase (PTPN22) is associated with rheumatoid arthritis. , 2004, American journal of human genetics.

[9]  F. Breedveld,et al.  Nutrient supplementation with polyunsaturated fatty acids and micronutrients in rheumatoid arthritis: clinical and biochemical effects , 2004, European Journal of Clinical Nutrition.

[10]  G. Alarcón,et al.  Supplementation with Folic Acid during Methotrexate Therapy for Rheumatoid Arthritis: A Double-Blind, Placebo-Controlled Trial , 1994, Annals of Internal Medicine.

[11]  O. Inanami,et al.  The leukocyte NADPH oxidase subunit p47PHOX: the role of the cysteine residues. , 1998, Archives of biochemistry and biophysics.

[12]  M. Liang,et al.  The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. , 1988, Arthritis and rheumatism.

[13]  K. Vasquez,et al.  Glutathione levels in antigen-presenting cells modulate Th1 versus Th2 response patterns. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[14]  S. Desiderio,et al.  BAP-135, a target for Bruton's tyrosine kinase in response to B cell receptor engagement. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[15]  R. Curi,et al.  Arachidonic acid triggers an oxidative burst in leukocytes. , 2003, Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas.

[16]  E. Pieterman,et al.  Discovery of distinctive gene expression profiles in rheumatoid synovium using cDNA microarray technology: evidence for the existence of multiple pathways of tissue destruction and repair , 2003, Genes and Immunity.

[17]  R. Holmdahl Rheumatoid arthritis viewed using a headache paradigm , 2000, Arthritis research.

[18]  R. M. Smith,et al.  The cytosolic components of the respiratory burst oxidase exist as a M(r) approximately 240,000 complex that acquires a membrane-binding site during activation of the oxidase in a cell-free system. , 1992, The Journal of biological chemistry.

[19]  J. Coffey,et al.  Inflammation and collagenase production in rats with adjuvant arthritis reduced with 13-cis-retinoic acid. , 1983, Science.

[20]  G. Kingsley,et al.  Tumor necrosis factor inhibitors for rheumatoid arthritis. , 2006, The New England journal of medicine.

[21]  A. Swaak,et al.  Superoxide production by polymorphonuclear leucocytes in rheumatoid arthritis and osteoarthritis: in vivo inhibition by the antirheumatic drug piroxicam due to interference with the activation of the NADPH-oxidase. , 1986, Annals of the rheumatic diseases.

[22]  J. Lambeth NOX enzymes and the biology of reactive oxygen , 2004, Nature Reviews Immunology.

[23]  David A. Williams,et al.  Mouse model of X–linked chronic granulomatous disease, an inherited defect in phagocyte superoxide production , 1995, Nature Genetics.

[24]  D. Leibfritz,et al.  Free radicals and antioxidants in normal physiological functions and human disease. , 2007, The international journal of biochemistry & cell biology.

[25]  R. Holmdahl,et al.  Genetic control of arthritis onset, severity and chronicity in a model for rheumatoid arthritis in rats , 1998, Nature Genetics.

[26]  M. Dinauer,et al.  Impaired NADPH oxidase activity in Rac2‐deficient murine neutrophils does not result from defective translocation of p47phox and p67phox and can be rescued by exogenous arachidonic acid , 2006, Journal of leukocyte biology.

[27]  D. Heinegård,et al.  Comment on "The Influence of the Proinflammatory Cytokine, Osteopontin, on Autoimmune Demyelinating Disease" , 2003, Science.

[28]  S. Holland,et al.  The p47phox mouse knock-out model of chronic granulomatous disease , 1995, The Journal of experimental medicine.

[29]  M. Geiszt,et al.  The Nox Family of NAD(P)H Oxidases: Host Defense and Beyond* , 2004, Journal of Biological Chemistry.

[30]  L. Genestier,et al.  Immunosuppressive properties of methotrexate: apoptosis and clonal deletion of activated peripheral T cells. , 1998, The Journal of clinical investigation.

[31]  E. Green,et al.  A p47-phox pseudogene carries the most common mutation causing p47-phox- deficient chronic granulomatous disease. , 1997, The Journal of clinical investigation.

[32]  M. Geisow,et al.  The respiratory burst of phagocytic cells is associated with a rise in vacuolar pH , 1981, Nature.

[33]  P. Gregersen Gaining insight into PTPN22 and autoimmunity , 2005, Nature Genetics.

[34]  Michael Reth,et al.  Hydrogen peroxide as second messenger in lymphocyte activation , 2002, Nature Immunology.

[35]  Josep M. Guerrero,et al.  Dual effect of melatonin as proinflammatory and antioxidant in collagen‐induced arthritis in rats , 2005, Journal of pineal research.

[36]  A. Shiose,et al.  Arachidonic Acid and Phosphorylation Synergistically Induce a Conformational Change of p47 phox to Activate the Phagocyte NADPH Oxidase* , 2000, The Journal of Biological Chemistry.

[37]  M. Dinauer,et al.  Absence of Respiratory Burst in X-linked Chronic Granulomatous Disease Mice Leads to Abnormalities in Both Host Defense and Inflammatory Response to Aspergillus fumigatus , 1997, The Journal of experimental medicine.

[38]  D. Borderie,et al.  Serum protein oxidation in patients with rheumatoid arthritis and effects of infliximab therapy. , 2006, Clinica chimica acta; international journal of clinical chemistry.

[39]  L. Pérez-Jurado,et al.  Evolutionary mechanisms shaping the genomic structure of the Williams-Beuren syndrome chromosomal region at human 7q11.23. , 2005, Genome research.

[40]  K. Asadullah,et al.  Dissociation of transactivation from transrepression by a selective glucocorticoid receptor agonist leads to separation of therapeutic effects from side effects , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[41]  A. Koçyiğit,et al.  Plasma total antioxidant capacity, lipid peroxidation, and erythrocyte antioxidant enzyme activities in patients with rheumatoid arthritis and osteoarthritis. , 2005, Clinical biochemistry.

[42]  R. Holmdahl,et al.  Expression of a transgenic class II Ab gene confers susceptibility to collagen‐induced arthritis , 1994, European journal of immunology.

[43]  F. Breedveld,et al.  Evidence for the role of an altered redox state in hyporesponsiveness of synovial T cells in rheumatoid arthritis. , 1997, Journal of immunology.

[44]  H. Nakamura,et al.  Redox regulation of cellular activation. , 1997, Annual review of immunology.

[45]  T. Kuratsuji,et al.  A novel cytosolic component, p40phox, of respiratory burst oxidase associates with p67phox and is absent in patients with chronic granulomatous disease who lack p67phox. , 1994, Biochemical and biophysical research communications.

[46]  R. Holmdahl Association of MHC and rheumatoid arthritis: Why is rheumatoid arthritis associated with the MHC genetic region? An introduction , 2000, Arthritis research.

[47]  S. Chanock,et al.  Genomic structure of the human p47-phox (NCF1) gene. , 2000, Blood cells, molecules & diseases.

[48]  Jeen-Woo Park,et al.  Possible target components for the inhibitory effect of N‐ethylmaleimide on the activation of neutrophil NADPH oxidase , 1998, Biochemistry and molecular biology international.

[49]  H. Westerhoff,et al.  A wave of reactive oxygen species (ROS)-induced ROS release in a sea of excitable mitochondria. , 2006, Antioxidants & redox signaling.

[50]  G. V. Ommen,et al.  Copy number variation in regions flanked (or unflanked) by duplicons among patients with developmental delay and/or congenital malformations; detection of reciprocal and partial Williams-Beuren duplications , 2006, European Journal of Human Genetics.

[51]  G. Buettner,et al.  Ascorbate Reacts with Singlet Oxygen to Produce Hydrogen Peroxide , 2006, Photochemistry and photobiology.

[52]  P. Hogg,et al.  Presence of closely spaced protein thiols on the surface of mammalian cells , 2000, Protein science : a publication of the Protein Society.

[53]  Dean P. Jones,et al.  Effects of N-acetyl-L-cysteine on T-cell apoptosis are not mediated by increased cellular glutathione. , 1995, Immunology letters.

[54]  M. Roederer,et al.  Cytokine-stimulated human immunodeficiency virus replication is inhibited by N-acetyl-L-cysteine. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[55]  T. Nomura,et al.  Altered thymic T-cell selection due to a mutation of the ZAP-70 gene causes autoimmune arthritis in mice , 2003, Nature.

[56]  L. Herzenberg,et al.  Lymphocyte surface thiol levels , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[57]  A. Dietrich,et al.  Assessment of collagen type II induced arthritis in mice by whole blood chemiluminescence. , 1994, Autoimmunity.

[58]  L. Joosten,et al.  Deficiency of NADPH oxidase components p47phox and gp91phox caused granulomatous synovitis and increased connective tissue destruction in experimental arthritis models. , 2003, The American journal of pathology.

[59]  M. Valko,et al.  Free radicals, metals and antioxidants in oxidative stress-induced cancer. , 2006, Chemico-biological interactions.

[60]  R. Holmdahl,et al.  Type II Collagen Autoimmunity in Animals and Provocations Leading to Arthritis , 1990, Immunological reviews.

[61]  P. Henkart,et al.  Do cytotoxic lymphocytes kill via reactive oxygen species? , 2005, Immunity.

[62]  P. Hawkins,et al.  PtdIns3P binding to the PX domain of p40phox is a physiological signal in NADPH oxidase activation , 2006, The EMBO journal.

[63]  G. Kroemer,et al.  Glutathione depletion is an early and calcium elevation is a late event of thymocyte apoptosis. , 1997, Journal of immunology.

[64]  J. Díez,et al.  The C242T CYBA polymorphism of NADPH oxidase is associated with essential hypertension , 2006, Journal of hypertension.

[65]  R. Woods,et al.  Geographic distribution of rheumatoid arthritis in ancient North America: implications for pathogenesis. , 1992, Seminars in arthritis and rheumatism.

[66]  J. Kwon,et al.  T cell receptor stimulation, reactive oxygen species, and cell signaling. , 2004, Free radical biology & medicine.

[67]  E. Gulbins,et al.  Lipid Raft Clustering and Redox Signaling Platform Formation in Coronary Arterial Endothelial Cells , 2006, Hypertension.

[68]  K. Kinoshita,et al.  Anti-inflammatory effect of all-trans-retinoic acid in inflammatory arthritis. , 2006, Clinical immunology.

[69]  F. Wolfe,et al.  Termination of slow acting antirheumatic therapy in rheumatoid arthritis: a 14-year prospective evaluation of 1017 consecutive starts. , 1990, The Journal of rheumatology.

[70]  A. Silman,et al.  Twin concordance rates for rheumatoid arthritis: results from a nationwide study. , 1993, British journal of rheumatology.

[71]  J. Dumont,et al.  Cloning of Two Human Thyroid cDNAs Encoding New Members of the NADPH Oxidase Family* , 2000, The Journal of Biological Chemistry.

[72]  B. Babior,et al.  Functional defect in neutrophil cytosols from two patients with autosomal recessive cytochrome-positive chronic granulomatous disease. , 1989, The Journal of clinical investigation.

[73]  J. Vane,et al.  Inhibition of prostaglandin synthesis as a mechanism of action for aspirin-like drugs. , 1971, Nature: New biology.

[74]  C. Sen Redox signaling and the emerging therapeutic potential of thiol antioxidants. , 1998, Biochemical pharmacology.

[75]  M. Weinblatt,et al.  Efficacy of low-dose methotrexate in rheumatoid arthritis. , 1985, The New England journal of medicine.

[76]  F. Breedveld,et al.  CTLA-4IG suppresses reactive oxygen species by preventing synovial adherent cell-induced inactivation of Rap1, a Ras family GTPASE mediator of oxidative stress in rheumatoid arthritis T cells. , 2006, Arthritis and rheumatism.

[77]  F. Breedveld,et al.  Defective TCR-mediated signaling in synovial T cells in rheumatoid arthritis. , 1997, Journal of immunology.

[78]  K. Kanazawa,et al.  Polymorphism of the NADH/NADPH oxidase p22 phox gene in patients with coronary artery disease. , 1998, Circulation.

[79]  A. Silman,et al.  Epidemiology of rheumatoid arthritis , 1994, APMIS : acta pathologica, microbiologica, et immunologica Scandinavica.

[80]  P. Hogg,et al.  Disulfide bonds as switches for protein function. , 2003, Trends in biochemical sciences.

[81]  D. Williams,et al.  Deficiency of the hematopoietic cell-specific Rho family GTPase Rac2 is characterized by abnormalities in neutrophil function and host defense. , 1999, Immunity.

[82]  R. Holmdahl,et al.  Identification of genes controlling collagen-induced arthritis in mice: striking homology with susceptibility loci previously identified in the rat. , 1999, Journal of immunology.

[83]  L. Dekker,et al.  Lipid rafts determine efficiency of NADPH oxidase activation in neutrophils , 2003, FEBS letters.

[84]  R. Holmdahl,et al.  T cell surface redox levels determine T cell reactivity and arthritis susceptibility , 2006, Proceedings of the National Academy of Sciences.

[85]  K. Arnold,et al.  Cartilage degradation by stimulated human neutrophils: reactive oxygen species decrease markedly the activity of proteolytic enzymes. , 2000, Chemistry & biology.

[86]  M. Mannie,et al.  Inhibition of activation‐induced death in T cell hybridomas by thiol antioxidants: oxidative stress as a mediator of apoptosis , 1994, Journal of leukocyte biology.

[87]  L. Provinciali,et al.  Intracellular oxidative activity and respiratory burst of leukocytes isolated from multiple sclerosis patients , 2006, Neurochemistry International.

[88]  W. Dröge,et al.  Macrophages regulate intracellular glutathione levels of lymphocytes. Evidence for an immunoregulatory role of cysteine. , 1990, Cellular immunology.

[89]  B. Cronstein,et al.  The antiinflammatory mechanism of methotrexate. Increased adenosine release at inflamed sites diminishes leukocyte accumulation in an in vivo model of inflammation. , 1993, The Journal of clinical investigation.

[90]  S. Chanock,et al.  Recombination events between the p47-phox gene and its highly homologous pseudogenes are the main cause of autosomal recessive chronic granulomatous disease. , 2000, Blood.

[91]  B. Joe Quest for arthritis-causative genetic factors in the rat. , 2006, Physiological genomics.

[92]  J. Saldanha,et al.  Reshaping a human antibody to inhibit the interleukin 6-dependent tumor cell growth. , 1993, Cancer research.

[93]  E. Vellenga,et al.  The reduced GM‐CSF priming of ROS production in granulocytes from patients with myelodysplasia is associated with an impaired lipid raft formation , 2007, Journal of leukocyte biology.

[94]  H. Yamawaki,et al.  Thioredoxin: a multifunctional antioxidant enzyme in kidney, heart and vessels , 2005, Current opinion in nephrology and hypertension.

[95]  J. Kaprio,et al.  Occurrence of rheumatoid arthritis in a nationwide series of twins. , 1986, The Journal of rheumatology.

[96]  K. Woollard,et al.  The anti‐inflammatory actions of methotrexate are critically dependent upon the production of reactive oxygen species , 2003, British journal of pharmacology.

[97]  C. Thompson,et al.  Antigen-presenting cells control T cell proliferation by regulating amino acid availability , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[98]  F. Buttgereit,et al.  Developments in glucocorticoid therapy. , 2005, Rheumatic diseases clinics of North America.

[99]  A. Levine,et al.  Redox Equilibrium in Mucosal T Cells Tunes the Intestinal TCR Signaling Threshold1 , 2005, The Journal of Immunology.

[100]  G. Çok,et al.  Effect of different levels of cigarette smoking on lipid peroxidation, glutathione enzymes and paraoxonase 1 activity in healthy people , 2005, Clinical and Experimental Medicine.

[101]  F. Baas,et al.  Inactivating mutations in the gene for thyroid oxidase 2 (THOX2) and congenital hypothyroidism. , 2002, The New England journal of medicine.

[102]  C. Friman,et al.  Effect of diclofenac sodium, tolfenamic acid and indomethacin on the production of superoxide induced by N-formyl-methionyl-leucyl-phenylalanine in normal human polymorphonuclear leukocytes. , 1986, Scandinavian journal of rheumatology.

[103]  J. Kwon,et al.  T cells express a phagocyte-type NADPH oxidase that is activated after T cell receptor stimulation , 2004, Nature Immunology.

[104]  M. Conese,et al.  Retinoids inhibit the respiratory burst and degranulation of stimulated human polymorphonuclear leukocytes , 1991, Agents and Actions.

[105]  J. Palmblad,et al.  Chronic granulomatous disease caused by mutations other than the common GT deletion in NCF1, the gene encoding the p47phox component of the phagocyte NADPH oxidase , 2006, Human mutation.

[106]  K. Nabbe,et al.  NADPH-oxidase-driven oxygen radical production determines chondrocyte death and partly regulates metalloproteinase-mediated cartilage matrix degradation during interferon-γ-stimulated immune complex arthritis , 2005, Arthritis research & therapy.

[107]  Ash A. Alizadeh,et al.  Rheumatoid arthritis is a heterogeneous disease: evidence for differences in the activation of the STAT-1 pathway between rheumatoid tissues. , 2003, Arthritis and rheumatism.

[108]  Yang Du,et al.  Correction of X-linked chronic granulomatous disease by gene therapy, augmented by insertional activation of MDS1-EVI1, PRDM16 or SETBP1 , 2006, Nature Medicine.

[109]  C. Hitchon,et al.  Oxidation in rheumatoid arthritis , 2004, Arthritis research & therapy.

[110]  M. Tassabehji,et al.  A complete physical contig and partial transcript map of the Williams syndrome critical region. , 1999, Genomics.

[111]  M. Feldmann,et al.  Cytokine stimulation of T lymphocytes regulates their capacity to induce monocyte production of tumor necrosis factor‐α, but not interleukin‐10: Possible relevance to pathophysiology of rheumatoid arthritis , 1997, European journal of immunology.

[112]  A S Rigby,et al.  Characterizing the quantitative genetic contribution to rheumatoid arthritis using data from twins. , 2000, Arthritis and rheumatism.

[113]  T. Buttke,et al.  Redox regulation of programmed cell death in lymphocytes. , 1995, Free radical research.

[114]  Y. Hirabayashi,et al.  Rapid and specific reactive oxygen species generation via NADPH oxidase activation during Fas‐mediated apoptosis , 1998, FEBS letters.

[115]  R. Wait,et al.  Detection and Mapping of Widespread Intermolecular Protein Disulfide Formation during Cardiac Oxidative Stress Using Proteomics with Diagonal Electrophoresis* , 2004, Journal of Biological Chemistry.

[116]  V. Taneja,et al.  Association of MHC and rheumatoid arthritis: Regulatory role of HLA class II molecules in animal models of RA - studies on transgenic/knockout mice , 2000, Arthritis research.

[117]  S. Altrichter,et al.  Suppression of type II collagen-induced arthritis by N-acetyl-L-cysteine in mice. , 1997, General pharmacology.

[118]  V. Kouskoff,et al.  The arthritogenic T cell receptor and its ligand in a model of spontaneous arthritis. , 1999, Arthritis and rheumatism.

[119]  M. Feldmann,et al.  Anti-tumor necrosis factor ameliorates joint disease in murine collagen-induced arthritis. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[120]  M. Feldmann,et al.  Anti-TNF alpha therapy of rheumatoid arthritis: what have we learned? , 2001, Annual review of immunology.

[121]  G. Kollias,et al.  Tumor Necrosis Factor (TNF) Receptor Shedding Controls Thresholds of Innate Immune Activation That Balance Opposing TNF Functions in Infectious and Inflammatory Diseases , 2004, The Journal of experimental medicine.

[122]  T. Hussell,et al.  An absence of reactive oxygen species improves the resolution of lung influenza infection , 2006, European journal of immunology.

[123]  R. Holmdahl,et al.  The pineal hormone melatonin exaggerates development of collagen-induced arthritis in mice , 1992, Journal of Neuroimmunology.

[124]  T. Yanagawa,et al.  CTLA-4 gene polymorphism in Japanese patients with rheumatoid arthritis. , 2000, The Journal of rheumatology.

[125]  T. Assari Chronic Granulomatous Disease; fundamental stages in our understanding of CGD , 2006, Medical immunology.

[126]  M. Roederer,et al.  Intracellular thiols regulate activation of nuclear factor kappa B and transcription of human immunodeficiency virus. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[127]  B. Sahaf,et al.  Thioredoxin expression and localization in human cell lines: detection of full-length and truncated species. , 1997, Experimental cell research.

[128]  B. Ames,et al.  Antioxidant defenses and lipid peroxidation in human blood plasma. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[129]  L. Zhan,et al.  P47phox ‐deficient NADPH oxidase defect in neutrophils of diabetic mouse strains, C57BL/6J‐m db/db and db/+ , 2000, Journal of leukocyte biology.

[130]  P. Lipsky,et al.  T cell activation as starter and motor of rheumatic inflammation. , 2006, Current topics in microbiology and immunology.

[131]  A. Aromaa,et al.  Serum antioxidants and risk of rheumatoid arthritis. , 1994, Annals of the rheumatic diseases.

[132]  P. Stastny Mixed lymphocyte cultures in rheumatoid arthritis. , 1976, The Journal of clinical investigation.

[133]  S. Holland,et al.  Genetic, biochemical, and clinical features of chronic granulomatous disease. , 2000, Medicine.

[134]  C. Baecher-Allan,et al.  Isolation and functional characterization of regulatory CD25brightCD4+ T cells from the target organ of patients with rheumatoid arthritis , 2003, European journal of immunology.

[135]  D. Borderie,et al.  High redox thioredoxin but low thioredoxin reductase activities in the serum of patients with rheumatoid arthritis. , 2006, Clinica chimica acta; international journal of clinical chemistry.

[136]  P. Emery,et al.  Efficacy of B-cell-targeted therapy with rituximab in patients with rheumatoid arthritis. , 2004, The New England journal of medicine.

[137]  J. Smolen,et al.  Interleukin-6: a new therapeutic target , 2006, Arthritis research & therapy.

[138]  C. Gentile,et al.  The chemistry of melatonin's interaction with reactive species , 2003, Journal of pineal research.

[139]  F. Breedveld,et al.  Intracellular free radical production in synovial T lymphocytes from patients with rheumatoid arthritis. , 2005, Arthritis and rheumatism.

[140]  M. Bayés,et al.  Hemizygosity at the NCF1 gene in patients with Williams-Beuren syndrome decreases their risk of hypertension. , 2006, American journal of human genetics.

[141]  A. Descoteaux,et al.  Phagocytosis of Leishmania donovani amastigotes is Rac1 dependent and occurs in the absence of NADPH oxidase activation , 2006, European journal of immunology.

[142]  D. Kelley,et al.  Modulation of human immune and inflammatory responses by dietary fatty acids. , 2001, Nutrition.

[143]  P. Gregersen,et al.  Microheterogeneity of HLA-DR4 haplotypes: DNA sequence analysis of LD"KT2" and LD"TAS" haplotypes. , 1987, Human immunology.

[144]  S. Farber,et al.  Advances in chemotherapy of cancer in man. , 1956, Advances in cancer research.

[145]  G. Raposo,et al.  NOX2 Controls Phagosomal pH to Regulate Antigen Processing during Crosspresentation by Dendritic Cells , 2006, Cell.

[146]  M. Bayés,et al.  Mutational mechanisms of Williams-Beuren syndrome deletions. , 2003, American journal of human genetics.

[147]  Christine D. Dijkstra,et al.  Reactive oxygen species are involved in the pathogenesis of experimental allergic encephalomyelitis in Lewis rats , 1995, Journal of Neuroimmunology.

[148]  S. Chrubasik Vitamin E for rheumatoid arthritis or osteoarthritis: low evidence of effectiveness , 2003, Zeitschrift für Rheumatologie.

[149]  V. Koshkin,et al.  The Cytosolic Component p47phox Is Not a Sine Qua Non Participant in the Activation of NADPH Oxidase but Is Required for Optimal Superoxide Production* , 1996, The Journal of Biological Chemistry.

[150]  D. Noack,et al.  Identification of a novel NCF-1 (p47-phox) pseudogene not containing the signature GT deletion: significance for A47 degrees chronic granulomatous disease carrier detection. , 2002, Blood.

[151]  N. Zurgil,et al.  Low dose methotrexate induces apoptosis with reactive oxygen species involvement in T lymphocytic cell lines to a greater extent than in monocytic lines , 2005, Inflammation Research.

[152]  R. Holmdahl,et al.  Pristane, a Non-Antigenic Adjuvant, Induces MHC Class II-Restricted, Arthritogenic T Cells in the Rat1 , 2006, The Journal of Immunology.

[153]  B. Babior Phagocytes and oxidative stress. , 2000, The American journal of medicine.

[154]  Y. Ozkan,et al.  Oxidative status in rheumatoid arthritis , 2006, Clinical Rheumatology.

[155]  G. Filomeni,et al.  Antigen-presenting dendritic cells provide the reducing extracellular microenvironment required for T lymphocyte activation , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[156]  M. Dougados,et al.  Treatment of rheumatoid arthritis by selective inhibition of T-cell activation with fusion protein CTLA4Ig. , 2003, The New England journal of medicine.

[157]  S. Lebègue,et al.  Pro-oxidant properties of methotrexate: evaluation and prevention by an anti-oxidant drug. , 1994, Die Pharmazie.

[158]  L. Oberley,et al.  Discrete Generation of Superoxide and Hydrogen Peroxide by T Cell Receptor Stimulation , 2002, The Journal of experimental medicine.

[159]  J. Roudier Association of MHC and rheumatoid arthritis: Association of RA with HLA-DR4 - the role of repertoire selection , 2000, Arthritis research.

[160]  D. Harrison,et al.  C242T CYBA Polymorphism of the NADPH Oxidase Is Associated With Reduced Respiratory Burst in Human Neutrophils , 2004, Hypertension.

[161]  B. Kidd,et al.  Putative analgesic activity of repeated oral doses of vitamin E in the treatment of rheumatoid arthritis. Results of a prospective placebo controlled double blind trial , 1997, Annals of the rheumatic diseases.

[162]  J. De Keyser,et al.  Oxidative stress in serum and peripheral blood leukocytes in patients with different disease courses of multiple sclerosis , 2006, Journal of Neurology.

[163]  L. Davis,et al.  Oxidative Stress Promotes Polarization of Human T Cell Differentiation Toward a T Helper 2 Phenotype1 , 2006, The Journal of Immunology.

[164]  Erwin G. Van Meir,et al.  Homologs of gp91phox: cloning and tissue expression of Nox3, Nox4, and Nox5. , 2001, Gene.

[165]  F. Breedveld,et al.  Displacement of Linker for Activation of T Cells from the Plasma Membrane Due to Redox Balance Alterations Results in Hyporesponsiveness of Synovial Fluid T Lymphocytes in Rheumatoid Arthritis , 2000, The Journal of Immunology.

[166]  P. Krammer,et al.  HIV-1 Trans-Activator of Transcription Substitutes for Oxidative Signaling in Activation-Induced T Cell Death 1 , 2005, The Journal of Immunology.

[167]  G L Johnson,et al.  Human neutrophil immunodeficiency syndrome is associated with an inhibitory Rac2 mutation. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[168]  K. Schulze-Osthoff,et al.  IL‐2 gene expression and NF‐kappa B activation through CD28 requires reactive oxygen production by 5‐lipoxygenase. , 1995, The EMBO journal.

[169]  R. Luna,et al.  Enhanced apoptosis in the thymus of transgenic mice expressing constitutively activated forms of human Rac2GTPase , 1997, Oncogene.

[170]  P. Ghezzi,et al.  Redox regulation of surface protein thiols: Identification of integrin α-4 as a molecular target by using redox proteomics , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[171]  K. Griendling,et al.  Giant atrial septal aneurysm simulating a right atrial tumour , 2004, Heart.

[172]  P. Ghezzi,et al.  Protein glutathionylation: coupling and uncoupling of glutathione to protein thiol groups in lymphocytes under oxidative stress and HIV infection. , 2002, Molecular immunology.

[173]  W. Fischer,et al.  Protein Disulfide Bond Formation in the Cytoplasm during Oxidative Stress* , 2004, Journal of Biological Chemistry.

[174]  D. Shore,et al.  Multimerization of Hsp42p, a Novel Heat Shock Protein of Saccharomyces cerevisiae, Is Dependent on a Conserved Carboxyl-terminal Sequence (*) , 1996, The Journal of Biological Chemistry.

[175]  K. Krause,et al.  A mammalian H+ channel generated through alternative splicing of the NADPH oxidase homolog NOH-1. , 2000, Science.

[176]  S. Sollott,et al.  Mitochondrial ROS-induced ROS release: an update and review. , 2006, Biochimica et biophysica acta.

[177]  S. Lorenzini,et al.  Altered thiol pattern in plasma of subjects affected by rheumatoid arthritis. , 2005, Clinical and experimental rheumatology.

[178]  M. Ehrenfeld,et al.  The Immunosuppressive Effect of Methotrexate in Active Rheumatoid Arthritis Patients vs. its Stimulatory Effect in Nonactive Patients, as Indicated by Cytometric Measurements of CD4 + T Cell Subpopulations , 2004, Immunological investigations.

[179]  R. Holmdahl,et al.  Enhanced autoimmunity, arthritis, and encephalomyelitis in mice with a reduced oxidative burst due to a mutation in the Ncf1 gene. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[180]  D. Kimpel,et al.  Animal models of rheumatoid arthritis and their relevance to human disease. , 2005, Pathophysiology : the official journal of the International Society for Pathophysiology.

[181]  Yusuke Nakamura,et al.  Functional haplotypes of PADI4, encoding citrullinating enzyme peptidylarginine deiminase 4, are associated with rheumatoid arthritis , 2003, Nature Genetics.

[182]  K. Bergsteinsdottir,et al.  Evidence for Common Autoimmune Disease Genes Controlling Onset, Severity, and Chronicity Based on Experimental Models for Multiple Sclerosis and Rheumatoid Arthritis1 , 2000, The Journal of Immunology.

[183]  R. Holmdahl,et al.  Elucidation of pathways leading to rheumatoid arthritis by genetic analysis of animal models. , 2001, Current directions in autoimmunity.

[184]  H. C. Mehta,et al.  Antioxidant status in rheumatoid arthritis and role of antioxidant therapy. , 2003, Clinica chimica acta; international journal of clinical chemistry.

[185]  JL Newton,et al.  A review of the MHC genetics of rheumatoid arthritis , 2004, Genes and Immunity.

[186]  P. Ghezzi,et al.  Thiol-disulfide balance: from the concept of oxidative stress to that of redox regulation. , 2005, Antioxidants & redox signaling.

[187]  M. Kurosaka,et al.  Thioredoxin protects against joint destruction in a murine arthritis model. , 2006, Free radical biology & medicine.

[188]  W. Hunter,et al.  The antioxidants curcumin and quercetin inhibit inflammatory processes associated with arthritis , 2006, Inflammation Research.

[189]  E. Ogier-Denis,et al.  Interleukin-8-induced Priming of Neutrophil Oxidative Burst Requires Sequential Recruitment of NADPH Oxidase Components into Lipid Rafts* , 2005, Journal of Biological Chemistry.

[190]  Gerd Geisslinger,et al.  Cyclooxygenase‐independent actions of cyclooxygenase inhibitors , 2001, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[191]  J. Pincemail,et al.  Vitamin E uncouples joint destruction and clinical inflammation in a transgenic mouse model of rheumatoid arthritis. , 2002, Arthritis and rheumatism.

[192]  K. Rittinger,et al.  Activation and assembly of the NADPH oxidase: a structural perspective. , 2005, The Biochemical journal.

[193]  Jens Holmberg,et al.  Positional identification of Ncf1 as a gene that regulates arthritis severity in rats , 2003, Nature Genetics.

[194]  P. Heyworth,et al.  Chronic granulomatous disease. , 2003, Current opinion in immunology.

[195]  P. Hawkins,et al.  Neutrophils from p40phox−/− mice exhibit severe defects in NADPH oxidase regulation and oxidant-dependent bacterial killing , 2006, The Journal of experimental medicine.

[196]  C. Herfarth,et al.  Thiol-Mediated Redox Regulation of Intestinal Lamina Propria T Lymphocytes , 2000, The Journal of experimental medicine.

[197]  Yun Jung Ha,et al.  Role of TNF Receptor-Associated Factor 3 in the CD40 Signaling by Production of Reactive Oxygen Species through Association with p40phox, a Cytosolic Subunit of Nicotinamide Adenine Dinucleotide Phosphate Oxidase 1 , 2004, The Journal of Immunology.

[198]  F. Franconi,et al.  Thiolation and nitrosation of cysteines in biological fluids and cells , 2003, Amino Acids.

[199]  O. Firuzi,et al.  Oxidative stress parameters in different systemic rheumatic diseases , 2006, The Journal of pharmacy and pharmacology.

[200]  L. Alfredsson,et al.  Mechanisms of Disease: genetic susceptibility and environmental triggers in the development of rheumatoid arthritis , 2006, Nature Clinical Practice Rheumatology.

[201]  H. Esterbauer,et al.  4-Hydroxynonenal formation during ischemia and reperfusion of rat small intestine. , 1995, Life sciences.

[202]  R. Holmdahl,et al.  A New Arthritis Therapy with Oxidative Burst Inducers , 2006, PLoS medicine.

[203]  R. Jonsson,et al.  Pristane-induced arthritis in rats: a new model for rheumatoid arthritis with a chronic disease course influenced by both major histocompatibility complex and non-major histocompatibility complex genes. , 1996, The American journal of pathology.

[204]  E. Zanelli,et al.  Critical residues on HLA-DRB1*0402 HV3 peptide for HLA-DQ8-restricted immunogenicity: implications for rheumatoid arthritis predisposition. , 1997, Journal of immunology.