Inflammation and intracellular metabolism: New targets in OA

Osteoarthritis and Cartilage

Volumn 23, Issue 11, 2015, Pages 1835-1842

  Liu Bryan, R ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

AMPK; Cartilage homeostasis; Energy metabolism; Inflammation; SIRT1

Indexed keywords

ACETYLSALICYLIC ACID; ACTIVATING TRANSCRIPTION FACTOR 6; ADENYLATE KINASE; BERBERINE; CILOSTAZOL; CURCUMIN; CURCUMINOID; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; INITIATION FACTOR 2ALPHA; INTERLEUKIN 1BETA; MANGANESE SUPEROXIDE DISMUTASE; METFORMIN; METHOTREXATE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PIASCLEDINE; PLACEBO; PROTEIN KINASE LKB1; PROTEIN TYROSINE PHOSPHATASE 1B; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; QUERCETIN; REACTIVE OXYGEN METABOLITE; RESVERATROL; SALICYLATE SODIUM; SIMVASTATIN; SIRTUIN 1; TRANSCRIPTION FACTOR FKHRL1; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG; WNT PROTEIN; X BOX BINDING PROTEIN 1; CYTOKINE;

3' UNTRANSLATED REGION; AGING; APOPTOSIS; ARTICLE; ARTICULAR CARTILAGE; AUTOPHAGY; BIOENERGY; BIOGENESIS; BONE; BONE MASS; BONE REMODELING; CARTILAGE CELL; CARTILAGE DEGENERATION; CELL METABOLISM; DEACETYLATION; DISEASE COURSE; DRUG MEGADOSE; ENDOPLASMIC RETICULUM STRESS; ENERGY BALANCE; ENERGY METABOLISM; ENZYME ACTIVATION; ENZYME DENATURATION; ENZYME REGULATION; GLYCOLYSIS; HISTONE PHOSPHORYLATION; HUMAN; INFLAMMATION; INTRACELLULAR METABOLISM; LIPOGENESIS; NONHUMAN; OSSIFICATION; OSTEOARTHRITIS; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SYNOVIUM; TISSUE METABOLISM; UNFOLDED PROTEIN RESPONSE; ANIMAL; CHONDROCYTE; INTRACELLULAR FLUID; METABOLISM; PHYSIOLOGY;

ANIMALS; CARTILAGE, ARTICULAR; CHONDROCYTES; CYTOKINES; ENERGY METABOLISM; HUMANS; INFLAMMATION; INTRACELLULAR FLUID; OSTEOARTHRITIS;

EID: 84945272579     PISSN: 10634584     EISSN: 15229653     Source Type: Journal    
DOI: 10.1016/j.joca.2014.12.016     Document Type: Article

References (113)

1. Loeser R.F., Goldring S.R., Scanzello C.R., Goldring M.B. Osteoarthritis: a disease of the joint as an organ. Arthritis Rheum 2012, 64:1697-1707.
2. Sellam J., Berenbaum F. The role of synovitis in pathophysiology and clinical symptoms of osteoarthritis. Nat Rev Rheumatol 2010, 6:625-635.
3. Scanzello C.R., Goldring S.R. The role of synovitis in osteoarthritis pathogenesis. Bone 2012, 51:249-257.
4. Goldring M.B., Goldring S.R. Articular cartilage and subchondral bone in the pathogenesis of osteoarthritis. Ann N Y Acad Sci 2010, 1192:230-237.
5. Liu-Bryan R., Terkeltaub R. The growing array of innate inflammatory ignition switches in osteoarthritis. Arthritis Rheum 2012, 64:2055-2058.
6. Liu-Bryan R. Synovium and the innate inflammatory network in osteoarthritis progression. Curr Rheumatol Rep 2013, 15:323.
7. Sellam J., Berenbaum F. Is osteoarthritis a metabolic disease?. Jt Bone Spine 2013 Dec, 80(6):568-573.
8. O'Neill L.A., Hardie D.G. Metabolism of inflammation limited by AMPK and pseudo-starvation. Nature 2013, 493:346-355.
9. Liu T.F., Brown C.M., El Gazzar M., McPhail L., Millet P., Rao A., et al. Fueling the flame: bioenergy couples metabolism and inflammation. J Leukoc Biol 2012, 92:499-507.
10. Fullerton M.D., Steinberg G.R., Schertzer J.D. Immunometabolism of AMPK in insulin resistance and atherosclerosis. Mol Cell Endocrinol 2013, 366:224-234.
11. Salminen A., Kaarniranta K. AMP-activated protein kinase (AMPK) controls the aging process via an integrated signaling network. Ageing Res Rev 2012, 11:230-241.
12. Mobasheri A., Vannucci S.J., Bondy C.A., Carter S.D., Innes J.F., Arteaga M.F., et al. Glucose transport and metabolism in chondrocytes: a key to understanding chondrogenesis, skeletal development and cartilage degradation in osteoarthritis. Histol Histopathol 2002, 17:1239-1267.
13. Blanco F.J., López-Armada M.J., Maneiro E. Mitochondrial dysfunction in osteoarthritis. Mitochondrion 2004, 4:715-728.
14. Steinberg G.R., Kemp B.E. AMPK in health and disease. Physiol Rev 2009, 89:1025-1078.
15. Witczak C.A., Sharoff C.G., Goodyear L.J. AMP-activated protein kinase in skeletal muscle: from structure and localization to its role as a master regulator of cellular metabolism. Cell Mol Life Sci 2008, 65:3737-3755.
16. Terkeltaub R., Yang B., Lotz M., Liu-Bryan R. Chondrocyte AMP-activated protein kinase activity suppresses matrix degradation responses to inflammatory cytokines IL-1β and TNFα. Arthritis Rheum 2011, 63:1928-1937.
17. Petursson F., Husa M., June R., Lotz M., Terkeltaub R., Liu-Bryan R. Linked decreases in liver kinase B1 and AMP-activated protein kinase activity modulate matrix catabolic responses to biomechanical injury in chondrocytes. Arthritis Res Ther 2013, 24(15):R77.
18. Li X. SIRT1 and energy metabolism. Acta Biochim Biophys Sin (Shanghai) 2013, 45:51-60.
19. Chang H.C., Guarente L. SIRT1 and other sirtuins in metabolism. Trends Endocrinol Metab 2014, 25:138-145.
20. Dvir-Ginzberg M., Steinmeyer J. Towards elucidating the role of SirT1 in osteoarthritis. Front Biosci 2013, 18:343-355.
21. Fujita N., Matsushita T., Ishida K., Kubo S., Matsumoto T., Takayama K., et al. Potential involvement of SIRT1 in the pathogenesis of osteoarthritis through the modulation of chondrocyte gene expressions. J Orthop Res 2011, 29:511-515.
22. Matsuzaki T., Matsushita T., Takayama K., Matsumoto T., Nishida K., Kuroda R., et al. Disruption of Sirt1 in chondrocytes causes accelerated progression of osteoarthritis under mechanical stress and during ageing in mice. Ann Rheum Dis 2014, 73:1397-1404.
23. Gagarina V., Gabay O., Dvir-Ginzberg M., Lee E.J., Brady J.K., Quon M.J., et al. SirT1 enhances survival of human osteoarthritic chondrocytes by repressing protein tyrosine phosphatase 1B and activating the insulin-like growth factor receptor pathway. Arthritis Rheum 2010, 62:1383-1392.
24. Moon M.H., Jeong J.K., Lee Y.J., Seol J.W., Jackson C.J., Park S.Y. SIRT1, a class III histone deacetylase, regulates TNF-α-induced inflammation in human chondrocytes. Osteoarthritis Cartilage 2013, 21:470-480.
25. Matsushita T., Sasaki H., Takayama K., Ishida K., Matsumoto T., Kubo S., et al. The overexpression of SIRT1 inhibited osteoarthritic gene expression changes induced by interleukin-1β in human chondrocytes. J Orthop Res 2013, 31:531-537.
26. Dvir-Ginzberg M., Gagarina V., Lee E.J., Hall D.J. Regulation of cartilage-specific gene expression in human chondrocytes by SirT1 and nicotinamid phosphoribosyltransferase. J Biol Chem 2008, 283:36300-36310.
27. Hong E.H., Lee S.J., Kim J.S., Lee K.H., Um H.D., Kim J.H., et al. Ionizing radiation induces cellular senescence of articular chondrocytes via negative regulation of SIRT1 by p38 kinase. J Biol Chem 2010, 285:1283-1295.
28. Takayama K., Ishida K., Matsushita T., Fujita N., Hayashi S., Sasaki K., et al. SIRT1 regulation of apoptosis of human chondrocytes. Arthritis Rheum 2009, 60:2731-2740.
29. Gabay O., Oppenhiemer H., Meir H., Zaal K., Sanchez C., Dvir-Ginzberg M. Increased apoptotic chondrocytes in articular cartilage from adult heterozygous SirT1 mice. Ann Rheum Dis 2012, 71:613-616.
30. Gabay O., Sanchez C., Dvir-Ginzberg M., Gagarina V., Zaal K.J., Song Y., et al. Sirtuin 1 enzymatic activity is required for cartilage homeostasis in vivo in a mouse model. Arthritis Rheum 2013, 65:159-166.
31. Ruderman N.B., Xu X.J., Nelson L., Cacicedo J.M., Saha A.K., Lan F., et al. AMPK and SIRT1: a long-standing partnership?. Am J Physiol Endocrinol Metab 2010, 298:E751-E760.
32. Blanco F.J., Rego I., Ruiz-Romero C. The role of mitochondria in osteoarthritis. Nat Rev Rheumatol 2011, 7:161-169.
33. López-Otín C., Blasco M.A., Partridge L., Serrano M., Kroemer G. The hallmarks of aging. Cell 2013, 153:1194-1217.
34. Maneiro E., Martín M.A., de Andres M.C., López-Armada M.J., Fernández-Sueiro J.L., del Hoyo P., et al. Mitochondrial respiratory activity is altered in osteoarthritic human articular chondrocytes. Arthritis Rheum 2003, 48:700-708.
35. Johnson K., Svensson C.I., Etten D.V., Ghosh S.S., Murphy A.N., Powell H.C., et al. Mediation of spontaneous knee osteoarthritis by progressive chondrocyte ATP depletion in Hartley guinea pigs. Arthritis Rheum 2004, 50:1216-1225.
36. Terkeltaub R., Johnson K., Murphy A., Ghosh S. Invited review: the mitochondrion in osteoarthritis. Mitochondrion 2002, 1:301-319.
37. Lotz M., Loeser R.F. Effects of aging on articular cartilage homeostasis. Bone 2012, 51:241-248.
38. Lee R.B., Urban J.P. Evidence for a negative Pasteur effect in articular cartilage. Biochem J 1997, 321:95-102.
39. Lee R.B., Urban J.P. Functional replacement of oxygen by other oxidants in articular cartilage. Arthritis Rheum 2002, 46:3190-3200.
40. Martin J.A., Martini A., Molinari A., Morgan W., Ramalingam W., Buckwalter J.A., et al. Mitochondrial electron transport and glycolysis are coupled in articular cartilage. Osteoarthritis Cartilage 2012, 20:323-329.
41. Henrotin Y., Kurz B., Aigner T. Oxygen and reactive oxygen species in cartilage degradation: friends or foes?. Osteoarthritis Cartilage 2005, 13:643-654.
42. Henrotin Y.E., Bruckner P., Pujol J.P. The role of reactive oxygen species in homeostasis and degradation of cartilage. Osteoarthritis Cartilage 2003, 11:747-755.
43. Cillero-Pastor B., Rego-Pérez I., Oreiro N., Fernandez-Lopez C., Blanco F.J. Mitochondrial respiratory chain dysfunction modulates metalloproteases-1, -3 and -13 in human normal chondrocytes in culture. BMC Musculoskelet Disord 2013, 14:235.
44. Vaamonde-García C., Riveiro-Naveira R.R., Valcárcel-Ares M.N., Hermida-Carballo L., Blanco F.J., López-Armada M.J. Mitochondrial dysfunction increases inflammatory responsiveness to cytokines in normal human chondrocytes. Arthritis Rheum 2012, 64:2927-2936.
45. Zhao X., Petursson F., Viollet B., Lotz M., Terkeltaub R., Liu-Bryan R. Peroxisome proliferator-activated receptor γ coactivator 1α and FoxO3A mediate chondroprotection by AMP-activated protein kinase. Arthritis Rheumatol 2014, 66:3073-3082.
46. Olmos Y., Valle I., Borniquel S., Tierrez A., Soria E., Lamas S., et al. Mutual dependence of Foxo3a and PGC-1alpha in the induction of oxidative stress genes. J Biol Chem 2009, 284:14476-14484.
47. Kang C., Li Ji L. Role of PGC-1alpha signaling in skeletal muscle health and disease. Ann N Y Acad Sci 2012, 1271:110-117.
48. Gavriilidis C., Miwa S., von Zglinicki T., Taylor R.W., Young D.A. Mitochondrial dysfunction in osteoarthritis is associated with down-regulation of superoxide dismutase 2. Arthritis Rheum 2013, 65:378-387.
49. Scott J.L., Gabrielides C., Davidson R.K., Swingler T.E., Clark I.M., Wallis G.A., et al. Superoxide dismutase downregulation in osteoarthritis progression and end-stage disease. Ann Rheum Dis 2010, 69:1502-1510.
50. Rajagopalan S., Meng X.P., Ramasamy S., Harrison D.G., Galis Z.S. Reactive oxygen species produced by macrophage-derived foam cells regulate the activity of vascular matrix metalloproteinases in vitro. Implications for atherosclerotic plaque stability. J Clin Invest 1996, 98:2572-2579.
51. Petersen S.V., Oury T.D., Ostergaard L., Valnickova Z., Wegrzyn J., Thogersen I.B., et al. Extracellular superoxide dismutase (EC-SOD) binds to type I collagen and protects against oxidative fragmentation. J Biol Chem 2004, 279:13705-13710.
52. Loeser R.F. Molecular mechanisms of cartilage destruction in osteoarthritis. J Musculoskelet Neuronal Interact 2008, 8:303-306.
53. Salminen A., Hyttinen J.M., Kaarniranta K. AMP-activated protein kinase inhibits NF-κB signaling and inflammation: impact on health span and lifespan. J Mol Med 2011, 89:667-676.
54. Kauppinen A., Suuronen T., Ojala J., Kaarniranta K., Salminen A. Antagonistic crosstalk between NF-κB and SIRT1 in the regulation of inflammation and metabolic disorders. Cell Signal 2013, 25:1939-1948.
55. Lei M., Wang J.G., Xiao D.M., Fan M., Wang D.P., Xiong J.Y., et al. Resveratrol inhibits interleukin 1β-mediated inducible nitric oxide synthase expression in articular chondrocytes by activating SIRT1 and thereby suppressing nuclear factor-κB activity. Eur J Pharmacol 2012, 674:73-79.
56. Csaki C., Mobasheri A., Shakibaei M. Synergistic chondroprotective effects of curcumin and resveratrol in human articular chondrocytes: inhibition of IL-1beta-induced NF-kappaB-mediated inflammation and apoptosis. Arthritis Res Ther 2009, 11:R165.
57. Shakibaei M., Csaki C., Nebrich S., Mobasheri A. Resveratrol suppresses interleukin-1beta-induced inflammatory signaling and apoptosis in human articular chondrocytes: potential for use as a novel nutraceutical for the treatment of osteoarthritis. Biochem Pharmacol 2008, 76:1426-1439.
58. Dvir-Ginzberg M., Gagarina V., Lee E.J., Booth R., Gabay O., Hall D.J. Tumor necrosis actor α-mediated cleavage and inactivation of SirT1 in human osteoarthritic chondrocytes. Arthritis Rheum 2011, 63:2363-2373.
59. Yamakuchi M. MicroRNA regulation of SIRT1. Front Physiol 2012, 3:68.
60. Zhang K., Kaufman R.J. The unfolded protein response: a stress signaling pathway critical for health and disease. Neurology 2006, 66:S102-S109.
61. Dufey E., Sepúlveda D., Rojas-Rivera D., Hetz C. Cellular mechanisms of endoplasmic reticulum stress signaling in health and disease. 1. An overview. Am J Physiol Cell Physiol 2014, 307:C582-C594.
62. Husa M., Petursson F., Lotz M., Terkeltaub R., Liu-Bryan R. C/EBP homologous protein drives pro-catabolic responses in chondrocytes. Arthritis Res Ther 2013, 15(6):R218.
63. Takada K., Hirose J., Senba K., Yamabe S., Oike Y., Gotoh T., et al. Enhanced apoptotic and reduced protective response in chondrocytes following endoplasmic reticulum stress in osteoarthritic cartilage. Int J Exp Pathol 2011, 92:232-242.
64. Guo F.J., Xiong Z., Lu X., Ye M., Han X., Jiang R. ATF6 upregulates XBP1S and inhibits ER stress-mediated apoptosis in osteoarthritis cartilage. Cell Signal 2014, 26:332-342.
65. Liu Y., Zhou J., Zhao W., Li X., Jiang R., Liu C., et al. XBP1S associates with RUNX2 and regulates chondrocyte hypertrophy. J Biol Chem 2012, 287:34500-34513.
66. Oliver B.L., Cronin C.G., Zhang-Benoit Y., Goldring M.B., Tanzer M.L. Divergent stressresponses to IL-1beta, nitric oxide, and tunicamycin by chondrocytes. J Cell Physiol 2005, 204:45-50.
67. Takada K., Hirose J., Yamabe S., Uehara Y., Mizuta H. Endoplasmic reticulum stress mediates nitric oxide-induced chondrocyte apoptosis. Biomed Rep 2013, 1:315-319. E.
68. Yamabe S., Hirose J., Uehara Y., Okada T., Okamoto N., Oka K., et al. Intracellular accumulation of advanced glycation end products induces apoptosis via endoplasmic reticulum stress in chondrocytes. FEBS J 2013, 280:1617-1629.
69. Rasheed Z., Haqqi T.M. Endoplasmic reticulum stress induces the expression of COX-2 through activation of eIF2α, p38-MAPK and NF-κB in advanced glycation end products stimulated human chondrocytes. Biochim Biophys Acta 2012, 1823:2179-2189.
70. Uehara Y., Hirose J., Yamabe S., Okamoto N., Okada T., Oyadomari S., et al. Endoplasmic reticulum stress-induced apoptosis contributes to articular cartilage degeneration via C/EBP homologous protein. Osteoarthritis Cartilage 2014, 22:1007-1017.
71. Alers S., Löffler A.S., Wesselborg S., Stork B. Role of AMPK-mTOR-Ulk1/2 in the regulation of autophagy: cross talk, shortcuts, and feedbacks. Mol Cell Biol 2012, 32:2-11.
72. Lotz M., Caramés B. Autophagy: a new therapeutic target in cartilage injury and osteoarthritis. J Am Acad Orthop Surg 2012 Apr, 20(4):261-262.
73. Srinivas V., Bohensky J., Shapiro I.M. Autophagy: a new phase in the maturation of growth plate chondrocytes is regulated by HIF, mTOR and AMP kinase. Cells Tissues Organs 2009, 189:88-92.
74. Bohensky J., Leshinsky S., Srinivas V., Shapiro I.M. Chondrocyte autophagy is stimulated by HIF-1 dependent AMPK activation and mTOR suppression. Pediatr Nephrol 2010, 4:633-642.
75. Caramés B., Taniguchi N., Otsuki S., Blanco F.J., Lotz M. Autophagy is a protective mechanism in normal cartilage, and its aging-related loss is linked with cell death and osteoarthritis. Arthritis Rheum 2010, 62:791-801.
76. Caramés B., Taniguchi N., Seino D., Blanco F.J., D'Lima D., Lotz M. Mechanical injury suppresses autophagy regulators and pharmacologic activation of autophagy results in chondroprotection. Arthritis Rheum 2012, 64:1182-1192.
77. Sasaki H., Takayama K., Matsushita T., Ishida K., Kubo S., Matsumoto T., et al. Autophagy modulates osteoarthritis-related gene expression in human chondrocytes. Arthritis Rheum 2012, 64:1920-1928.
78. Zhang Y., Vasheghani F., Li Y.H., Blati M., Simeone K., Fahmi H., et al. Cartilage-specific deletion of mTOR upregulates autophagy and protects mice from osteoarthritis. Ann Rheum Dis 2014 Mar 20, (Epub ahead of print). 10.1136/annrheumdis-2013-204599.
79. Caramés B., Hasegawa A., Taniguchi N., Miyaki S., Blanco F.J., Lotz M. Autophagy activation by rapamycin reduces severity of experimental osteoarthritis. Ann Rheum Dis 2012, 71:575-581.
80. Kim H.Y., Park S.Y., Lee S.W., Lee H.R., Lee W.S., Rhim B.Y., et al. Inhibition of HMGB1-induced angiogenesis by cilostazol via SIRT1 activation in synovial fibroblasts from rheumatoid arthritis. PLoS One 2014 Aug 15, 9(8):e104743.
81. Kok S.H., Lin L.D., Hou K.L., Hong C.Y., Chang C.C., Hsiao M., et al. Simvastatin inhibits cysteine-rich protein 61 expression in rheumatoid arthritis synovial fibroblasts through the regulation of sirtuin-1/FoxO3a signaling. Arthritis Rheum 2013, 65:639-649.
82. Indo Y., Takeshita S., Ishii K.A., Hoshii T., Aburatani H., Hirao A., et al. Metabolic regulation of osteoclast differentiation and function. J Bone Miner Res 2013, 28:2392-2399.
83. Kang H., Viollet B., Wu D. Genetic deletion of catalytic subunits of AMP-activated protein kinase increases osteoclasts and reduces bone mass in young adult mice. J Biol Chem 2013, 288:12187-12196.
84. Jeyabalan J., Shah M., Viollet B., Chenu C. AMP-activated protein kinase pathway and bone metabolism. J Endocrinol 2012, 212:277-290.
85. Lee Y.S., Kim Y.S., Lee S.Y., Kim G.H., Kim B.J., Lee S.H., et al. AMP kinase acts as a negative regulator of RANKL in the differentiation of osteoclasts. Bone 2010, 47:926-937.
86. Shah M., Kola B., Bataveljic A., Arnett T.R., Viollet B., Saxon L., et al. AMP-activated protein kinase (AMPK) activation regulates in vitro bone formation and bone mass. Bone 2010, 47:309-319.
87. Quinn J.M., Tam S., Sims N.A., Saleh H., McGregor N.E., Poulton I.J., et al. Germline deletion of AMP-activated protein kinase beta subunits reduces bone mass without altering osteoclast differentiation or function. FASEB J 2010, 24:275-285.
88. Iyer S., Han L., Bartell S.M., Kim H.N., Gubrij I., de Cabo R., et al. Sirtuin1 (Sirt1) promotes cortical bone formation by preventing β-catenin sequestration by FoxO transcription factors in osteoblast progenitors. J Biol Chem 2014, 289:24069-24078.
89. Abed É., Couchourel D., Delalandre A., Duval N., Pelletier J.P., Martel-Pelletier J., et al. Low sirtuin 1 levels in human osteoarthritis subchondral osteoblasts lead to abnormal sclerostin expression which decreases Wnt/β-catenin activity. Bone 2014, 59:28-36.
90. Edwards J.R., Perrien D.S., Fleming N., Nyman J.S., Ono K., Connelly L., et al. Silent information regulator (Sir)T1 inhibits NF-κB signaling to maintain normal skeletal remodeling. J Bone Miner Res 2013, 28:960-969.
91. Cohen-Kfir E., Artsi H., Levin A., Abramowitz E., Bajayo A., Gurt I., et al. Sirt1 is a regulator of bone mass and a repressor of Sost encoding for sclerostin, a bone formation inhibitor. Endocrinology 2011, 152:4514-4524.
92. Simic P., Zainabadi K., Bell E., Sykes D.B., Saez B., Lotinun S., et al. SIRT1 regulates differentiation of mesenchymal stem cells by deacetylating β-catenin. EMBO Mol Med 2013, 5:430-440.
93. Chen H., Liu X., Chen H., Cao J., Zhang L., Hu X., et al. Role of SIRT1 and AMPK in mesenchymal stem cells differentiation. Ageing Res Rev 2014, 13:55-64.
94. Kim E.K., Lim S., Park J.M., Seo J.K., Kim J.H., Kim K.T., et al. Human mesenchymal stem cell differentiation to the osteogenic or adipogenic lineage is regulated by AMP-activated protein kinase. J Cell Physiol 2012, 227:1680-1687.
95. Bäckesjö C.M., Li Y., Lindgren U., Haldosén L.A. Activation of Sirt1 decreases adipocyte formation during osteoblast differentiation of mesenchymal stem cells. Cells Tissues Organs 2009, 189:93-97.
96. Fedor D., Kelley D.S. Prevention of insulin resistance by n-3 polyunsaturated fatty acids. Curr Opin Clin Nutr Metab Care 2009, 12:138-146.
97. Jelenik T., Rossmeisl M., Kuda O., Jilkova Z.M., Medrikova D., Kus V., et al. AMP-activated protein kinase α2 subunit is required for the preservation of hepatic insulin sensitivity by n-3 polyunsaturated fatty acids. Diabetes 2010, 59:2737-2746.
98. Suchankova G., Tekle M., Saha A.K., Ruderman N.B., Clarke S.D., Gettys T.W. Dietary polyunsaturated fatty acids enhance hepatic AMP-activated protein kinase activity in rats. Biochem Biophys Res Commun 2005, 326:851-858.
99. Rossmeisl M., Flachs P., Brauner P., Sponarova J., Matejkova O., Prazak T., et al. Role of energy charge and AMP-activated protein kinase in adipocytes in the control of body fat stores. Int J Obes Relat Metab Disord 2004, 28:S38-S44.
100. Gabler N.K., Radcliffe J.S., Spencer J.D., Webel D.M., Spurlock M.E. Feeding long-chain n-3 polyunsaturated fatty acids during gestation increases intestinal glucose absorption potentially via the acute activation of AMPK. J Nutr Biochem 2009, 20:17-25.
101. Richter E.A., Ruderman N.B. AMPK and the biochemistry of exercise: implications for human health and disease. Biochem J 2009, 418:261-275.
102. Bennell K.L., Dobson F., Hinman R.S. Exercise in osteoarthritis: moving from prescription to adherence. Best Pract Res Clin Rheumatol 2014, 28:93-117.
103. Friedrichsen M., Mortensen B., Pehmøller C., Birk J.B., Wojtaszewski J.F. Exercise-induced AMPK activity in skeletal muscle: role in glucose uptake and insulin sensitivity. Mol Cell Endocrinol 2013, 366:204-214.
104. Hardie D.G., Ross F.A., Hawley S.A. AMP-activated protein kinase: a target for drugs both ancient and modern. Chem Biol 2012, 19:1222-1236.
105. Hwang J.T., Kwon D.Y., Yoon S.H. AMP-activated protein kinase: a potential target for the diseases prevention by natural occurring polyphenols. N Biotechnol 2009, 26:17-22.
106. Abou-Raya A., Abou-Raya S., Khadrawe T. Methotrexate in the treatment of symptomatic knee osteoarthritis: randomised placebo-controlled trial. Ann Rheum Dis 2014 Mar 27, (Epub ahead of print). 10.1136/annrheumdis-2013-204856.
107. Panahi Y., Rahimnia A.R., Sharafi M., Alishiri G., Saburi A., Sahebkar A. Curcuminoid treatment for knee osteoarthritis: a randomized double-blind placebo-controlled trial. Phytother Res 2014 May 22, (Epub ahead of print). 10.1002/ptr. 5174.
108. Maheu E., Cadet C., Marty M., Moyse D., Kerloch I., Coste P., et al. Randomised, controlled trial of avocado-soybean unsaponifiable (Piascledine) effect on structure modification in hip osteoarthritis: the ERADIAS study. Ann Rheum Dis 2014, 73:376-384.
109. Christensen R., Bartels E.M., Astrup A., Bliddal H. Symptomatic efficacy of avocado-soybean unsaponifiables (ASU) in osteoarthritis (OA) patients: a meta-analysis of randomized controlled trials. Osteoarthritis Cartilage 2008, 16:399-408.
110. Maheu E., Mazières B., Valat J.P., Loyau G., Le Loët X., Bourgeois P., et al. Symptomatic efficacy of avocado/soybean unsaponifiables in the treatment of osteoarthritis of the knee and hip: a prospective, randomized, double-blind, placebo-controlled, multicenter clinical trial with a six-month treatment period and a two-month followup demonstrating a persistent effect. Arthritis Rheum 1998, 41:81-91.
111. Yamagata K., Tanaka N., Matsufuji H., Chino M. β-carotene reverses the IL-1β-mediated reduction in paraoxonase-1 expression via induction of the CaMKKII pathway in human endothelial cells. Microvasc Res 2012, 84(3):297-305.
112. Tang L., Zhang Y., Jiang Y., Willard L., Ortiz E., Wark L., et al. Dietary wolfberry ameliorates retinal structure abnormalities in db/db mice at the early stage of diabetes. Exp Biol Med (Maywood) 2011, 236:1051-1063.
113. Arunkumar E., Anuradha C.V. Genistein promotes insulin action through adenosine monophosphate-activated protein kinase activation and p70 ribosomal protein S6 kinase 1 inhibition in the skeletal muscle of mice fed a high energy diet. Nutr Res 2012, 32:617-625.