Dysregulated bioenergetics: A key regulator of joint inflammation

Annals of the Rheumatic Diseases

Volumn 75, Issue 12, 2016, Pages 2192-2200

  Biniecka, M ^a   Canavan, M ^b   McGarry, T ^b   Gao, W ^a   McCormick, J ^a   Cregan, S ^a   Gallagher, L ^a   Smith, T ^a   Phelan, J J ^d   Ryan, J ^e   O'Sullivan, J ^d   Ng, C T ^c   Veale, D J ^a   Fearon, U ^b  

^a ST VINCENT S UNIVERSITY HOSPITAL   (Ireland)

^b TRINITY COLLEGE DUBLIN   (Ireland)

^c SINGAPORE GENERAL HOSPITAL   (Singapore)

^d ST JAMES S HOSPITAL   (Ireland)

^e UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

Fibroblasts; Inflammation; Rheumatoid Arthritis; Synovitis; TNF alpha

Indexed keywords

3 (3 PYRIDINYL) 1 (4 PYRIDINYL) 2 PROPEN 1 ONE; ADENOSINE TRIPHOSPHATE; AUTACOID; C REACTIVE PROTEIN; CXCL1 CHEMOKINE; DIMETHYLOXALYLGLYCINE; FIBROBLAST GROWTH FACTOR 2; GLUCOSE; GLUCOSE TRANSPORTER 1; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INTERLEUKIN 6; INTERLEUKIN 8; KETONE DERIVATIVE; LACTIC ACID; MITOCHONDRIAL DNA; MONOCYTE CHEMOTACTIC PROTEIN 1; NOTCH1 RECEPTOR; OXYGEN; PROLYL HYDROXYLASE INHIBITOR; PYRUVATE KINASE; PYRUVATE KINASE M2; RANTES; REACTIVE OXYGEN METABOLITE; STAT3 PROTEIN; TUMOR NECROSIS FACTOR INHIBITOR; UNCLASSIFIED DRUG; CYTOKINE; DICARBOXYLIC AMINO ACID; OXALYLGLYCINE;

ANGIOGENESIS; ARTHROSCOPY; ARTICLE; BIOENERGY; CELL INVASION; CELL METABOLISM; CELL MIGRATION; CELLULAR PARAMETERS; CLINICAL ARTICLE; COMPUTER ASSISTED EMISSION TOMOGRAPHY; CONTROLLED STUDY; CYTOKINE RELEASE; DAS28; DERMAL MICROVASCULAR ENDOTHELIAL CELL; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME PHOSPHORYLATION; FIBROBLAST; GENE MUTATION; GLYCOLYSIS; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOXIA; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MEDIATOR RELEASE; METABOLIC RATE; MIGRATION INHIBITION; MITOCHONDRIA STRUCTURE; MITOCHONDRIAL MASS; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; NUCLEAR MAGNETIC RESONANCE IMAGING; OXIDATIVE PHOSPHORYLATION; OXYGEN TISSUE LEVEL; PATHOPHYSIOLOGY; POLYMERASE CHAIN REACTION; POSITRON EMISSION TOMOGRAPHY; POSITRON EMISSION TOMOGRAPHY MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN SECRETION; RHEUMATOID ARTHRITIS; SYNOVITIS; SYNOVIUM; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; TRANSMISSION ELECTRON MICROSCOPY; CELL CULTURE; CELL MOTION; CYTOLOGY; ENERGY METABOLISM; JOINT; METABOLISM; MITOCHONDRION; PHYSIOLOGY;

AMINO ACIDS, DICARBOXYLIC; ARTHRITIS, RHEUMATOID; CELL MOVEMENT; CELLS, CULTURED; CYTOKINES; DNA, MITOCHONDRIAL; ENERGY METABOLISM; FIBROBLASTS; GLUCOSE; HUMANS; HYPOXIA; JOINTS; LACTIC ACID; MITOCHONDRIA; REACTIVE OXYGEN SPECIES; SYNOVIAL MEMBRANE;

EID: 84962885862     PISSN: 00034967     EISSN: 14682060     Source Type: Journal    
DOI: 10.1136/annrheumdis-2015-208476     Document Type: Article

References (61)

1. Chang X, Wei C. Glycolysis and rheumatoid arthritis. Int J Rheum Dis 2011;14:217-22.
2. Scrivo R, Vasile M, Müller-Ladner U, et al. Rheumatic diseases and obesity: adipocytokines as potential comorbidity biomarkers for cardiovascular diseases. Mediators Inflamm 2013;2013:808125.
3. Choy E, Ganeshalingam K, Semb AG, et al. Cardiovascular risk in rheumatoid arthritis: recent advances in the understanding of the pivotal role of inflammation, risk predictors and the impact of treatment. Rheumatology (Oxford) 2014;53:2143-54.
4. Jiang P, Li H, Li X. Diabetes mellitus risk factors in rheumatoid arthritis: a systematic review and meta-analysis. Clin Exp Rheumatol 2015;33:115-21.
5. Reece RJ, Canete JD, Parsons WJ, et al. Distinct vascular patterns of early synovitis in psoriatic, reactive, and rheumatoid arthritis. Arthritis Rheum 1999;42:1481-4.
6. Szekanecz Z, Koch AE. Endothelial cells in inflammation and angiogenesis. Curr Drug Targets Inflamm Allergy 2005;4:319-23.
7. Kennedy A, Ng CT, Biniecka M, et al. Angiogenesis and blood vessel stability in inflammatory arthritis. Arthritis Rheum 2010;62:711-21.
8. Lefèvre S, Knedla A, Tennie C, et al. Synovial fibroblasts spread rheumatoid arthritis to unaffected joints. Nat Med 2009;15:1414-20.
9. Sivakumar B, Akhavani MA, Winlove CP, et al. Synovial hypoxia as a cause of tendon rupture in rheumatoid arthritis. J Hand Surg Am 2008;33:49-58.
10. Akhavani MA, Madden L, Buysschaert I, et al. Hypoxia upregulates angiogenesis and synovial cell migration in rheumatoid arthritis. Arthritis Res Ther 2009;11:R64.
11. Ng CT, Biniecka M, Kennedy A, et al. Synovial tissue hypoxia and inflammation in vivo. Ann Rheum Dis 2010;69:1389-95.
12. Jeon CH, Ahn JK, Chai JY, et al. Hypoxia appears at pre-arthritic stage and shows co-localization with early synovial inflammation in collagen induced arthritis. Clin Exp Rheumatol 2008;26:646-8.
13. Oliver KM, Garvey JF, Ng CT, et al. Hypoxia activates NF-kappaB-dependent gene expression through the canonical signaling pathway. Antioxid Redox Signal 2009;11:2057-64.
14. Gao W, McCormick J, Connolly M, et al. Hypoxia and STAT3 signalling interactions regulate pro-inflammatory pathways in rheumatoid arthritis. Ann Rheum Dis 2015;74:1275-83.
15. Gao W, Sweeney C, Connolly M, et al. Notch-1 mediates hypoxia-induced angiogenesis in rheumatoid arthritis. Arthritis Rheum 2012;64:2104-13.
16. Kammouni W, Wong K, Ma G, et al. Regulation of apoptosis in fibroblast-like synoviocytes by the hypoxia-induced Bcl-2 family member Bcl-2/adenovirus E1B 19-kd protein-interacting protein 3. Arthritis Rheum 2007;56:2854-63.
17. Gaber T, Schellmann S, Erekul KB, et al. Macrophage migration inhibitory factor counterregulates dexamethasone-mediated suppression of hypoxia-inducible factor-1 alpha function and differentially influences human CD4+ T cell proliferation under hypoxia. J Immunol 2011;186:764-74.
18. Hu F, Mu R, Zhu J, et al. Hypoxia and hypoxia-inducible factor-1α provoke toll-like receptor signalling-induced inflammation in rheumatoid arthritis. Ann Rheum Dis 2014;73:928-36.
19. Naughton D, Whelan M, Smith EC, et al. An investigation of the abnormal metabolic status of synovial fluid from patients with rheumatoid arthritis by high field proton nuclear magnetic resonance spectroscopy. FEBS Lett 1993;317:135-8.
20. Ciurtin C, Cojocaru VM, Miron IM, et al. Correlation between different components of synovial fluid and pathogenesis of rheumatic diseases. Rom J Intern Med 2006;44:171-81.
21. Hitchon CA, El-Gabalawy HS, Bezabeh T. Characterization of synovial tissue from arthritis patients: a proton magnetic resonance spectroscopic investigation. Rheumatol Int 2009;29:1205-11.
22. Firestein GS, Echeverri F, Yeo M, et al. Somatic mutations in the p53 tumor suppressor gene in rheumatoid arthritis synovium. Proc Natl Acad Sci USA 1997;94:10895-900.
23. Tak PP, Zvaifler NJ, Green DR, et al. Rheumatoid arthritis and p53: how oxidative stress might alter the course of inflammatory diseases. Immunol Today 2000;21:78-82.
24. Gatenby RA, Gawlinski ET. The glycolytic phenotype in carcinogenesis and tumor invasion: insights through mathematical models. Cancer Res 2003;63:3847-54.
25. Henderson B, Bitensky L, Johnstone JJ, et al. Metabolic alterations in human synovial lining cells in pigmented villonodular synovitis. Ann Rheum Dis 1979;38:463-6.
26. Peansukmanee S, Vaughan-Thomas A, Carter SD, et al. Effects of hypoxia on glucose transport in primary equine chondrocytes in vitro and evidence of reduced GLUT1 gene expression in pathologic cartilage in vivo. J Orthop Res 2009;27:529-35.
27. Ramakrishnan P, Hecht BA, Pedersen DR, et al. Oxidant conditioning protects cartilage from mechanically induced damage. J Orthop Res 2010;28:914-20.
28. Harty LC, Biniecka M, O'Sullivan J, et al. Mitochondrial mutagenesis correlates with the local inflammatory environment in arthritis. Ann Rheum Dis 2012;71:582-8.
29. Tannahill GM, Curtis AM, Adamik J, et al. Succinate is an inflammatory signal that induces IL-1β through HIF-1α. Nature 2013;496:238-42.
30. Biniecka M, Kennedy A, Fearon U, et al. Oxidative damage in synovial tissue is associated with in vivo hypoxic status in the arthritic joint. Ann Rheum Dis 2010;69:1172-8.
31. Bulua AC, Simon A, Maddipati R, et al. Mitochondrial reactive oxygen species promote production of proinflammatory cytokines and are elevated in TNFR1-associated periodic syndrome (TRAPS). J Exp Med 2011;208:519-33.
32. Biniecka M, Fox E, Gao W, et al. Hypoxia induces mitochondrial mutagenesis and dysfunction in inflammatory arthritis. Arthritis Rheum 2011;63:2172-82.
33. Zhou R, Yazdi AS, Menu P, et al. A role for mitochondria in NLRP3 inflammasome activation. Nature 2011;469:221-5.
34. Biniecka M, Connolly M, Gao W, et al. Redox-mediated angiogenesis in the hypoxic joint of inflammatory arthritis. Arthritis Rheumatol 2014;66:3300-10.
35. Yang Z, Fujii H, Mohan SV, et al. Phosphofructokinase deficiency impairs ATP generation, autophagy, and redox balance in rheumatoid arthritis T cells. J Exp Med 2013;210:2119-34.
36. Vermulst M, Bielas JH, Loeb LA. Quantification of random mutations in the mitochondrial genome. Methods 2008;46:263-8.
37. Biniecka M, Kennedy A, Ng CT, et al. Successful tumour necrosis factor (TNF) blocking therapy suppresses oxidative stress and hypoxia-induced mitochondrial mutagenesis in inflammatory arthritis. Arthritis Res Ther 2011;13:R121.
38. Moodley D, Mody G, Patel N, et al. Mitochondrial depolarisation and oxidative stress in rheumatoid arthritis patients. Clin Biochem 2008;41:1396-401.
39. Sakon S, Xue X, Takekawa M, et al. NF-kappaB inhibits TNF-induced accumulation of ROS that mediate prolonged MAPK activation and necrotic cell death. EMBO J 2003;22:3898-909.
40. Miesel R, Hartung R, Kroeger H. Priming of NADPH oxidase by tumor necrosis factor alpha in patients with inflammatory and autoimmune rheumatic diseases. Inflammation 1996;20:427-38.
41. Collins LV, Hajizadeh S, Holme E, et al. Endogenously oxidized mitochondrial DNA induces in vivo and in vitro inflammatory responses. J Leukoc Biol 2004;75:995-1000.
42. Shi LZ, Wang R, Huang G, et al. HIF1alpha-dependent glycolytic pathway orchestrates a metabolic checkpoint for the differentiation of TH17 and Treg cells. J Exp Med 2011;208:1367-76.
43. Krawczyk CM, Holowka T, Sun J, et al. Toll-like receptor-induced changes in glycolytic metabolism regulate dendritic cell activation. Blood 2010;115:4742-9.
44. Vegran F, Boidot R, Michiels C, et al. Lactate influx through the endothelial cell monocarboxylate transporter MCT1 supports an NF-κB/IL-8 pathway that drives tumor angiogenesis. Cancer Res 2011;1:2550-60.
45. Colegio OR, Chu NQ, Szabo AL, et al. Functional polarization of tumour-associated macrophages by tumour-derived lactic acid. Nature 2014;513:559-63.
46. Gregório I, Martel F, Keating E. Modulation of the uptake of critical nutrients by breast cancer cells by lactate: impact on cell survival, proliferation and migration. Exp Cell Res 2016;341:111-22.
47. Tsuboi R, Sato Y, Rifkin DB. Correlation of Cell Migration, Cell Invasion, Receptor Number, Proteinase Production, and Basic Fibroblast Growth Factor Levels in Endothelial Cells. J Cell Biol 1990;11:511-17.
48. Im HJ, Muddasani P, Natarajan V, et al. Basic fibroblast growth factor stimulates matrix metalloproteinase-13 via the molecular cross-talk between the mitogen-activated protein kinases and protein kinase C delta pathways in human adult articular chondrocytes. J Biol Chem 2007;282:11110-21.
49. Shin EY, Woo KN, Lee CS, et al. Basic fibroblast growth factor stimulates activation of Rac1 through a p85 betaPIX phosphorylation-dependent pathway. J Biol Chem 2004;279:1994-2004.
50. Palsson-McDermott EM, Curtis AM, Goel G, et al. Pyruvate kinase M2 regulates Hif-1α activity and IL-1β induction and is a critical determinant of the warburg effect in LPS-activated macrophages. Cell Metab 2015;21:65-80.
51. Iyama S, Okamoto T, Sato T, et al. Treatment of murine collagen-induced arthritis by ex vivo extracellular superoxide dismutase gene transfer. Arthritis Rheum 2001;44:2160-7.
52. Kubota M, Shimmura S, Kubota S, et al. Hydrogen and N-acetyl-L-cysteine rescue oxidative stress-induced angiogenesis in a mouse corneal alkali-burn model. Invest Ophthalmol Vis Sci 2011;52:427-33.
53. Beckers A, Organe S, Timmermans L, et al. Methotrexate enhances the antianabolic and antiproliferative effects of 5-aminoimidazole-4-carboxamide riboside. Mol Cancer Ther 2006;5:2211-17.
54. Yang Z, Kahn BB, Shi H, et al. Macrophage alpha1 AMP-activated protein kinase (alpha1AMPK) antagonizes fatty acid-induced inflammation through SIRT1. J Biol Chem 2010;285:19051-9.
55. Shackelford DB, Vasquez DS, Corbeil J, et al. mTOR and HIF-1alpha-mediated tumor metabolism in an LKB1 mouse model of Peutz-Jeghers syndrome. Proc Natl Acad Sci USA 2009;106:11137-42.
56. Clem B, Telang S, Clem A, et al. Small-molecule inhibition of 6-phosphofructo-2-kinase activity suppresses glycolytic flux and tumor growth. Mol Cancer Ther 2008;7:110-20.
57. De Bock K, Georgiadou M, Schoors S, et al. Role of PFKFB3-driven glycolysis in vessel sprouting. Cell 2013;154:651-63.
58. Schoors S, De Bock K, Cantelmo AR, et al. Partial and transient reduction of glycolysis by PFKFB3 blockade reduces pathological angiogenesis. Cell Metab 2014;19:37-48.
59. Lee JH, Suk J, Park J, et al. Notch signal activates hypoxia pathway through HES1-dependent SRC/signal transducers and activators of transcription 3 pathway. Mol Cancer Res 2009;7:1663-71.
60. Covey MV, Levison SW. Leukemia inhibitory factor participates in the expansion of neural stem/progenitors after perinatal hypoxia/ischemia. Neuroscience 2007;148:501-9.
61. Qiang L, Wu T, Zhang HW, et al. HIF-1α is critical for hypoxia-mediated maintenance of glioblastoma stem cells by activating Notch signaling pathway. Cell Death Differ 2012;19:284-94.