Reactive oxygen and nitrogen species induce protein and DNA modifications driving arthrofibrosis following total knee arthroplasty
Fibrogenesis & Tissue Repair - 2009
Tóm tắt
Arthrofibrosis, occurring in 3%-4% of patients following total knee arthroplasty (TKA), is a challenging condition for which there is no defined cause. The hypothesis for this study was that disregulated production of reactive oxygen species (ROS) and nitrogen species (RNS) mediates matrix protein and DNA modifications, which result in excessive fibroblastic proliferation. We found increased numbers of macrophages and lymphocytes, along with elevated amounts of myeloperoxidase (MPO) in arthrofibrotic tissues when compared to control tissues. MPO expression, an enzyme that generates ROS/RNS, is usually limited to neutrophils and some macrophages, but was found by immunohistochemistry to be expressed in both macrophages and fibroblasts in arthrofibrotic tissue. As direct measurement of ROS/RNS is not feasible, products including DNA hydroxylation (8-OHdG), and protein nitrosylation (nitrotyrosine) were measured by immunohistochemistry. Quantification of the staining showed that 8-OHdg was significantly increased in arthrofibrotic tissue. There was also a direct correlation between the intensity of inflammation and ROS/RNS to the amount of heterotopic ossification (HO). In order to investigate the aberrant expression of MPO, a real-time oxidative stress polymerase chain reaction array was performed on fibroblasts isolated from arthrofibrotic and control tissues. The results of this array confirmed the upregulation of MPO expression in arthrofibrotic fibroblasts and highlighted the downregulated expression of the antioxidants, superoxide dismutase1 and microsomal glutathione S-transferase 3, as well as the significant increase in thioredoxin reductase, a known promoter of cell proliferation, and polynucleotide kinase 3'-phosphatase, a key enzyme in the base excision repair pathway for oxidative DNA damage. Based on our current findings, we suggest that ROS/RNS initiate and sustain the arthrofibrotic response driving aggressive fibroblast proliferation and subsequent HO.
Từ khóa
Tài liệu tham khảo
Bong MR, Di Cesare PE: Stiffness after total knee arthroplasty. Journal of the American Academy of Orthopaedic Surgeons. 2004, 12: 164-171.
Laskin RS, Beksac B: Stiffness after total knee arthroplasty. Journal of Arthroplasty. 2004, 19: 41-46.
Yercan HS, Sugun TS, Bussiere C, Ait Si Selmi T, Davies A, Neyret P: Stiffness after total knee arthroplasty: prevalence, management and outcomes. Knee. 2006, 13: 111-117.
Kim J, Nelson CL, Lotke PA: Stiffness after total knee arthroplasty. Prevalence of the complication and outcomes of revision. Journal of Bone & Joint Surgery American. 2004, 86: 1479-1484.
Anouchi YS, McShane M, Kelly F, Elting J, Stiehl J: Range of motion in total knee replacement. Clinical Orthopaedics & Related Research. 1996, 331: 87-92.
Diduch DR, Scuderi GR, Scott WN, Insall JN, Kelly MA: The efficacy of arthroscopy following total knee replacement. Arthroscopy. 1997, 13: 166-171.
Markel DC, Luessenhop CP, Windsor RE, Sculco TA: Arthroscopic treatment of peripatellar fibrosis after total knee arthroplasty. Journal of Arthroplasty. 1996, 11: 293-297.
Mont MA, Serna FK, Krackow KA, Hungerford DS: Exploration of radiographically normal total knee replacements for unexplained pain. Clinical Orthopaedics & Related Research. 1996, 331: 216-220.
Nicholls DW, Dorr LD: Revision surgery for stiff total knee arthroplasty. Journal of Arthroplasty. 1990, 5 (Suppl): S73-7.
Ries MD, Badalamente M: Arthrofibrosis after total knee arthroplasty. Clinical Orthopaedics & Related Research. 2000, 380: 177-183.
Parvizi J, Tarity TD, Steinbeck MJ, Politi RG, Joshi A, Purtill JJ, Sharkey PF: Management of stiffness following total knee arthroplasty. Journal of Bone and Joint Surgery. 2006, 88: 175-181.
Furia JP, Pellegrini VD: Heterotopic ossification following primary total knee arthroplasty [see comment]. Journal of Arthroplasty. 1995, 10: 413-419.
Freeman TA, Parvizi J, Della Valle C, Steinbeck MJ: Mast cells and hypoxia drive tissue metaplasia and heterotopic ossification in idiopathic arthrofibrosis. Fibrogenesis and Tissue Repair. 2009, Submitted
Wynn TA: Fibrotic disease and the th1/th2 paradigm. Nature Reviews Immunology. 2004, 4: 583-594.
Abe R, Donnelly SC, Peng T, Bucala R, Metz CN: Peripheral blood fibrocytes: differentiation pathway and migration to wound sites. Journal of Immunology. 2001, 166: 7556-7562.
Stramer BM, Mori R, Martin P: The inflammation-fibrosis link? A Jekyll and Hyde role for blood cells during wound repair. Journal of Investigative Dermatology. 2007, 127: 1009-1017.
Martin P, Leibovich SJ: Inflammatory cells during wound repair: the good, the bad and the ugly. Trends in Cell Biol. 2005, 15: 599-607.
Baran CP, Zeigler MM, Tridandapani S, Marsh CB: The role of ROS and RNS in regulating life and death of blood monocytes. Current Pharmaceutical Design. 2004, 10: 855-866.
Cochrane AL, Ricardo SD: Oxidant stress and regulation of chemokines in the development of renal interstitial fibrosis. Contributions to Nephrology. 2003, 139: 102-119.
Diamond JR, Ricardo SD, Klahr S: Mechanisms of interstitial fibrosis in obstructive nephropathy. Seminars in Nephrology. 1998, 18: 594-602.
Ferrini MG, Vernet D, Magee TR, Shahed A, Qian A, Rajfer J, Gonzalez-Cadavid NF: Antifibrotic role of inducible nitric oxide synthase. Nitric Oxide. 2002, 6: 283-294.
Marsh CB, Kelley TW, Graham MM, Dong C, Goldschmidt-Clermont PJ: Monocytes may regulate tissue fibrosis. Chest. 2001, 120: 15S-16S.
Poli G: Pathogenesis of liver fibrosis: role of oxidative stress. Molecular Aspects of Medicine. 2000, 21: 49-98.
Poli G, Parola M: Oxidative damage and fibrogenesis. Free Radical Biology & Medicine. 1997, 22: 287-305.
Ricardo SD, Diamond JR: The role of macrophages and reactive oxygen species in experimental hydronephrosis. Seminars in Nephrology. 1998, 18: 612-621.
Swindle EJ, Hunt JA, Coleman JW: A comparison of reactive oxygen species generation by rat peritoneal macrophages and mast cells using the highly sensitive real-time chemiluminescent probe pholasin: inhibition of antigen-induced mast cell degranulation by macrophage-derived hydrogen peroxide. Journal of Immunology. 2002, 169: 5866-5873.
Puxeddu I, Piliponsky AM, Bachelet I, Levi-Schaffer F: Mast cells in allergy and beyond. International Journal of Biochemistry and Cell Biology. 2003, 35: 1601-1607.
Murrell GA: The role of the fibroblast in Dupuytren's contracture. Hand Clinics. 1991, 7: 669-680.
Murrell GA: Scientific comment. Basic science of Dupuytren's disease. Annales de Chirurgie de la Main et du Membre Superieur. 1992, 11: 355-361.
Murrell GA: An insight into Dupuytren's contracture. Annals of the Royal College of Surgeons of England. 1992, 74: 156-160.
Yi IS, Johnson G, Moneim MS: Etiology of Dupuytren's disease. Hand Clinics. 1999, 15: 43-51.
Cracowski J-L: Isoprostanes as a tool to investigate oxidative stress in scleroderma spectrum disorders--advantages and limitations. Rheumatology. 2006, 45: 922-923.
Sambo P, Baroni SS, Luchetti M, Paroncini P, Dusi S, Orlandini G, Gabrielli A: Oxidative stress in scleroderma: maintenance of scleroderma fibroblast phenotype by the constitutive up-regulation of reactive oxygen species generation through the NADPH oxidase complex pathway [see comment]. Arthritis & Rheumatism. 2001, 44: 2653-2664.
Kruidenier L, Kuiper I, Van Duijn W, Mieremet-Ooms MA, van Hogezand RA, Lamers CB, Verspaget HW: Imbalanced secondary mucosal antioxidant response in inflammatory bowel disease. Journal of Pathology. 2003, 201: 17-27.
Risques RA, Rabinovitch PS, Brentnall TA: Cancer surveillance in inflammmatory bowel disease: new molecular approaches. Current Opinion in Gastroenterology. 2006, 22: 382-390.
Harrison JE, Schultz J: Studies on the chlorinating activity of myeloperoxidase. Journal of Biological Chemistry. 1976, 251: 1371-1374.
Halliwell B: Oxidative stress and cancer: have we moved forward?. Biochem J. 2007, 401: 1-11.
Heijnem HF, van Donselaar E, Slot JW, Fries DM, Blachard-Fillion B, Hodara R, Lightfoot R, Polydoro M, Spielberg DL, et al: Subcellular localization of tyrosine-nitrated proteins is dictated by reactive oxygen species generating enzymes and by proximity to nitric oxide synthase. Free Radical Biology & Medicine. 2006, 40: 1903-1913.
van Dalen CJ, Winterbourn CC, Senthilmohan R, Kettle AJ: Nitrite as a substrate and inhibitor of myeloperoxidase. Implications for nitration and hypochlorous acid production at sites of inflammation. J Biol Chem. 2000, 275: 11638-11644.
Takeshita J, Byun J, Nhan TQ, Pritchard DK, Pennathur S, Schwartz SM, Chait A, Heinecke JW: Myeloperoxidase generates 5-chlorouracil in human atherosclerotic tissue: a potential pathway for somatic mutagenesis by macrophages. J Biol Chem. 2006, 281: 3096-3104.
Henderson JP, Byun J, Takeshita J, Heinecke JW: Phagocytes produce 5-chlorouracil and 5-bromouracil, two mutagenic products of myeloperoxidase, in human inflammatory tissue. J Biol Chem. 2003, 278: 23522-23528.
Fitzgerald AM, Kirkpatrick JJ, Naylor IL: Dupuytren's disease. The way forward?. Journal of Hand Surgery British. 1999, 24: 395-399.
Murrell GA, Hueston JT: Aetiology of Dupuytren's contracture. Australian & New Zealand Journal of Surgery. 1990, 60: 247-252.
Wynn TA: Common and unique mechanisms regulate fibrosis in various fibroproliferative diseases. Journal of Clinical Investigation. 2007, 117: 524-529.
Murakami S, Muneta T, Furuya K, Saito I, Miyasaka N, Yamamoto H: Immunohistologic analysis of synovium in infrapatellar fat pad after anterior cruciate ligament injury. The American Journal of Sports Medicine. 1995, 23: 763-768.
Bosch U, Zeichen J, Skutek M, Haeder L, van Griensven M: Arthrofibrosis is the result of a T cell mediated immune response. Knee Surgery, Sports Traumatology, Arthroscopy. 2001, 9: 282-289.
Howard PS, Renfrow D, Schechter NM, Kucich U: Mast cell chymase is a possible mediator of neurogenic bladder fibrosis. Neurourology & Urodynamics. 2004, 23: 374-382.
Kaplan FS, Glaser DL, Hebela N, Shore EM: Heterotopic ossification. Journal of the American Academy of Orthopaedic Surgeons. 2004, 12: 116-125.
Kubiak EN, Moskovich R, Errico TJ, Di Cesare PE: Orthopaedic management of ankylosing spondylitis. Journal of the American Academy of Orthopaedic Surgeons. 2005, 13: 267-278.
Liu K, Tripp S, Layfield LJ: Heterotopic ossification: review of histologic findings and tissue distribution in a 10-year experience. Pathology, Research & Practice. 2007, 203: 633-640.
Rifas L: T-cell cytokine induction of BMP-2 regulates human mesenchymal stromal cell differentiation and mineralization. Journal of Cellular Biochemistry. 2006, 98: 706-714.
Steiner I, Kasparova P, Kohout A, Dominik J: Bone formation in cardiac valves: a histopathological study of 128 cases. Virchows Archiv. 2007, 450: 653-657.
Darley-Usmar V, Wiseman H, Halliwell B: Nitric oxide and oxygen radicals: a question of balance. FEBS Letters. 1995, 369: 131-135.
Brown GC, Borutaite V: Interactions between nitric oxide, oxygen, reactive oxygen species and reactive nitrogen species. Biochem Society Transactions. 2006, 34: 953-956.
Hurst JK, Barrette WC: Leukocytic oxygen activation and microbicidal oxidative toxins. Critical Reviews in Biochemistry & Molecular Biology. 1989, 24: 271-328.
Daumer KM, Khan AU, Steinbeck MJ: Chlorination of pyridinium compounds. Possible role of hypochlorite, N-chloramines, and chlorine in the oxidation of pyridinoline cross-links of articular cartilage collagen type II during acute inflammation. Journal of Biological Chemistry. 2000, 275: 34681-34692.
Steinbeck MJ, Nesti LJ, Sharkey PF, Parvizi J: Myeloperoxidase and chlorinated peptides in osteoarthritis: potential biomarkers of the disease. J Ortho Res. 2007, 25: 1128-1135.
Reynolds WF, Patel K, Pianko S, Blatt LM, Nicholas JJ, McHutchison JG: A genotypic association implicates myeloperoxidase in the progression of hepatic fibrosis in chronic hepatitis c virus infection. Genes and Immunity. 2002, 3: 345-349.
Reynolds WF, Sermet-Gaudelus I, Gausson V, Feuillet M-N, Bonnefont J-P, Descamps-Latscha B, Witko-Sarsat V: Myeloperoxidase promoter polymorphism -463G is associated with more severe clinical expression of cystic fibrosis pulmonary disease. Mediators of Inflammation. 2006, 36735: 1-8.
Blom IE, Goldschmeding R, Leask A: Gene regulation of connective tissue growth factor: new targets for antifibrotic therapy?. Matrix Biology. 2002, 21: 473-482.
Schafer M, Werner S: Oxidative stress in normal and impaired wound repair. Pharmacological Research. 2008, 58: 165-171.
Hazra TK, Das A, Das S, Choudhury S, Kow YW, Roy R: Oxidative DNA damage repair in mammalian cells: a new perspective. DNA Repair. 2007, 6: 470-480.
Mustacich D, Powis G: Thioredoxin reductase. Biochem J. 2000, 346: 1-8.
Yu YP, Yu G, Tseng G, Cieply K, Nelson J, Defrances M, Zarnegar R, Michalopoulos G, Luo J-H: Glutathione peroxidase 3, deleted or methylated in prostate cancer, suppresses prostate cancer growth and metastasis. Cancer Res. 2007, 67: 8043-8050.
Scanzello CR, Plaas A, Crow MK: Innate immune system activation in osteoarthritis: is osteoarthritis a chronic wound?. Current Opinion in Rheumatology. 2008, 20: 565-572.
Jones KL, Tarochione-Utt KD: DNA methylation in bovine adult and fetal fibroblast cells. Cloning & Stem Cells. 2004, 6: 259-266.