High Uric Acid Activates the ROS-AMPK Pathway, Impairs CD68 Expression and Inhibits OxLDL-Induced Foam-Cell Formation in a Human Monocytic Cell Line, THP-1

Cellular Physiology and Biochemistry

Volumn 40, Issue 3-4, 2016, Pages 538-548

  Luo, Chaohuan ^a   Lian, Xueke ^c   Hong, Liangli ^b   Zou, Jingfang ^a   Li, Zhi ^a   Zhu, Yuzhang ^a   Huang, Tianliang ^a   Zhang, Yongneng ^a   Hu, Yaqiu ^a   Yuan, Huier ^a   Wen, Tengfei ^a   Zhuang, Wanling ^a   Cai, Bozhi ^a   Zhang, Xin ^a   Hisatome, Ichiro ^d   Yamamoto, Tetsuya ^e   Huang, Jiexiong ^b   Cheng, Jidong ^a  

^a THE FIRST AFFILIATED HOSPITAL OF SHANTOU UNIVERSITY MEDICAL COLLEGE   (China)

^b Department of Pathology ^*  (China)

^c GUANGZHOU UNIVERSITY OF CHINESE MEDICINE   (China)

^d TOTTORI UNIVERSITY   (Japan)

^e HYOGO COLLEGE OF MEDICINE   (Japan)

Author keywords

CD68; Foam cell formation; High uric acid; Monocytes macrophages; ROS AMPK pathway

Indexed keywords

ABC TRANSPORTER A1; ABC TRANSPORTER G1; ACETYLCYSTEINE; CD86 ANTIGEN; CYCLOOXYGENASE 2; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; OXIDIZED LOW DENSITY LIPOPROTEIN; PHORBOL 13 ACETATE 12 MYRISTATE; REACTIVE OXYGEN METABOLITE; URIC ACID; ABCG1 PROTEIN, HUMAN; CD68 ANTIGEN, HUMAN; DIFFERENTIATION ANTIGEN; LEUKOCYTE ANTIGEN; LOW DENSITY LIPOPROTEIN; TRANSCRIPTION FACTOR RELA;

ARTICLE; CELL DIFFERENTIATION; CELL LINE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; FLOW CYTOMETRY; FOAM CELL; HUMAN; HUMAN CELL; MACROPHAGE FUNCTION; MONOCYTE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; THP 1 CELL LINE; WESTERN BLOTTING; BIOLOGICAL MODEL; CYTOLOGY; DRUG EFFECTS; METABOLISM; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TIME FACTOR;

ACETYLCYSTEINE; AMP-ACTIVATED PROTEIN KINASES; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, MYELOMONOCYTIC; ATP BINDING CASSETTE TRANSPORTER, SUB-FAMILY G, MEMBER 1; CELL DIFFERENTIATION; CELL LINE; CYCLOOXYGENASE 2; FOAM CELLS; HUMANS; LIPOPROTEINS, LDL; MODELS, BIOLOGICAL; MONOCYTES; OXIDATIVE STRESS; PHOSPHORYLATION; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; TETRADECANOYLPHORBOL ACETATE; TIME FACTORS; TRANSCRIPTION FACTOR RELA; URIC ACID;

EID: 85001036861     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000452567     Document Type: Article

References (47)

1. Wu XW, Muzny DM, Lee CC, Caskey CT: Two independent mutational events in the loss of urate oxidase during hominoid evolution. J Mol Evol 1992;34:78-84.
2. Oda M, Satta Y, Takenaka O, Takahata N: Loss of urate oxidase activity in hominoids and its evolutionary implications. Mol Biol Evol 2002;19:640-653.
3. Chizynski K, Rozycka M: [Hyperuricemia]. Pol Merkur Lekarski 2005;19:693-696.
4. Chuang SY, Lee SC, Hsieh YT, Pan WH: Trends in hyperuricemia and gout prevalence: Nutrition and Health Survey in Taiwan from 1993-1996 to 2005-2008. Asia Pac J Clin Nutr 2011;20:301-308.
5. Conen D, Wietlisbach V, Bovet P, Shamlaye C, Riesen W, Paccaud F, Burnier M: Prevalence of hyperuricemia and relation of serum uric acid with cardiovascular risk factors in a developing country. BMC Public Health 2004;4:9.
6. Krishnan E, Bennett M, Chen L: Aging, not menopause, is associated with higher prevalence of hyperuricemia among older women. Menopause 2014;21:1211-1216.
7. Villegas R, Xiang YB, Cai Q, Fazio S, Linton M, Li H, Elasy T, Zheng W, Shu XO: Prevalence and determinants of hyperuricemia in middle-aged, urban Chinese men. Metab Syndr Relat Disord 2010;8:263-270.
8. Zavaroni I, Mazza S, Fantuzzi M, Dall'Aglio E, Bonora E, Delsignore R, Passeri M, Reaven GM: Changes in insulin and lipid metabolism in males with asymptomatic hyperuricaemia. J Intern Med 1993;234:25-30.
9. Busque SM, Stange G, Wagner CA: Dysregulation of the glutamine transporter Slc38a3 (SNAT3) and ammoniagenic enzymes in obese, glucose-intolerant mice. Cell Physiol Biochem 2014;34:575-589.
10. Kleber ME, Delgado G, Grammer TB, Silbernagel G, Huang J, Kramer BK, Ritz E, Marz W: Uric Acid and Cardiovascular Events: A Mendelian Randomization Study. J Am Soc Nephrol 2015;26:2831-2838.
11. Kuo D, Crowson CS, Gabriel SE, Matteson EL: Hyperuricemia and incident cardiovascular disease and noncardiac vascular events in patients with rheumatoid arthritis. Int J Rheumatol 2014;2014:523897.
12. Li C, Hsieh MC, Chang SJ: Metabolic syndrome, diabetes, and hyperuricemia. Curr Opin Rheumatol 2013;25:210-216.
13. Guo Y, Jiang Q, Gui D, Wang N: Chinese Herbal Formulas Si-Wu-Tang and Er-Miao-San Synergistically Ameliorated Hyperuricemia and Renal Impairment in Rats Induced by Adenine and Potassium Oxonate. Cell Physiol Biochem 2015;37:1491-1502.
14. Jia G, Habibi J, Bostick BP, Ma L, DeMarco VG, Aroor AR, Hayden MR, Whaley-Connell AT, Sowers JR: Uric acid promotes left ventricular diastolic dysfunction in mice fed a Western diet. Hypertension 2015;65:531-539.
15. Hong Q, Yu S, Mei Y, Lv Y, Chen D, Wang Y, Geng W, Wu D, Cai G, Chen X: Smilacis Glabrae Rhizoma reduces oxidative stress caused by hyperuricemia via upregulation of catalase. Cell Physiol Biochem 2014;34:1675-1685.
16. Dalbeth N, Pool B, Gamble GD, Smith T, Callon KE, McQueen FM, Cornish J: Cellular characterization of the gouty tophus: A quantitative analysis. Arthritis Rheum 2010;62:1549-1556.
17. Kraakman MJ, Murphy AJ, Jandeleit-Dahm K, Kammoun HL: Macrophage polarization in obesity and type 2 diabetes: weighing down our understanding of macrophage function Front Immunol 2014;5:470.
18. Liang CP, Han S, Senokuchi T, Tall AR: The macrophage at the crossroads of insulin resistance and atherosclerosis. Circ Res 2007;100:1546-1555.
19. Tabas I, Seimon T, Arellano J, Li Y, Forcheron F, Cui D, Han S, Liang CP, Tall A, Accili D: The impact of insulin resistance on macrophage death pathways in advanced atherosclerosis. Novartis Found Symp 2007;286:99-109; discussion 109-112, 162-103, 196-203.
20. Holness CL, Simmons DL: Molecular cloning of CD68, a human macrophage marker related to lysosomal glycoproteins. Blood 1993;81:1607-1613.
21. Kurushima H, Ramprasad M, Kondratenko N, Foster DM, Quehenberger O, Steinberg D: Surface expression and rapid internalization of macrosialin (mouse CD68) on elicited mouse peritoneal macrophages. J Leukoc Biol 2000;67:104-108.
22. Ramprasad MP, Fischer W, Witztum JL, Sambrano GR, Quehenberger O, Steinberg D: The 94-to 97-kDa mouse macrophage membrane protein that recognizes oxidized low density lipoprotein and phosphatidylserine-rich liposomes is identical to macrosialin, the mouse homologue of human CD68. Proc Natl Acad Sci USA 1995;92:9580-9584.
23. Ramprasad MP, Terpstra V, Kondratenko N, Quehenberger O, Steinberg D: Cell surface expression of mouse macrosialin and human CD68 and their role as macrophage receptors for oxidized low density lipoprotein. Proc Natl Acad Sci USA 1996;93:14833-14838.
24. Bergeron R, Russell RR, 3rd, Young LH, Ren JM, Marcucci M, Lee A, Shulman GI: Effect of AMPK activation on muscle glucose metabolism in conscious rats. Am J Physiol 1999;276:E938-944.
25. Ojuka EO: Role of calcium and AMP kinase in the regulation of mitochondrial biogenesis and GLUT4 levels in muscle. Proc Nutr Soc 2004;63:275-278.
26. Winder WW: Energy-sensing and signaling by AMP-activated protein kinase in skeletal muscle. J Appl Physiol (1985) 2001;91:1017-1028.
27. Sag D, Carling D, Stout RD, Suttles J: Adenosine 5'-monophosphate-activated protein kinase promotes macrophage polarization to an anti-inflammatory functional phenotype. J Immunol 2008;181:8633-8641.
28. Vasamsetti SB, Karnewar S, Kanugula AK, Thatipalli AR, Kumar JM, Kotamraju S: Metformin inhibits monocyte-to-macrophage differentiation via AMPK-mediated inhibition of STAT3 activation: potential role in atherosclerosis. Diabetes 2015;64:2028-2041.
29. Baldwin W, McRae S, Marek G, Wymer D, Pannu V, Baylis C, Johnson RJ, Sautin YY: Hyperuricemia as a mediator of the proinflammatory endocrine imbalance in the adipose tissue in a murine model of the metabolic syndrome. Diabetes 2011;60:1258-1269.
30. Convento MS, Pessoa E, Dalboni MA, Borges FT, Schor N: Pro-inflammatory and oxidative effects of noncrystalline uric acid in human mesangial cells: contribution to hyperuricemic glomerular damage. Urol Res 2011;39:21-27.
31. Sautin YY, Nakagawa T, Zharikov S, Johnson RJ: Adverse effects of the classic antioxidant uric acid in adipocytes: NADPH oxidase-mediated oxidative/nitrosative stress. Am J Physiol Cell Physiol 2007;293:C584-596.
32. Yu MA, Sanchez-Lozada LG, Johnson RJ, Kang DH: Oxidative stress with an activation of the renin-angiotensin system in human vascular endothelial cells as a novel mechanism of uric acid-induced endothelial dysfunction. J Hypertens 2010;28:1234-1242.
33. Zhang Y, Hong Q, Huang Z, Xue P, Lv Y, Fu B, Chen X, Wu D: ALDR enhanced endothelial injury in hyperuricemia screened using SILAC. Cell Physiol Biochem 2014;33:479-490.
34. Zhang Y, Yamamoto T, Hisatome I, Li Y, Cheng W, Sun N, Cai B, Huang T, Zhu Y, Li Z, Jing X, Zhou R, Cheng J: Uric acid induces oxidative stress and growth inhibition by activating adenosine monophosphate-activated protein kinase and extracellular signal-regulated kinase signal pathways in pancreatic beta cells. Mol Cell Endocrinol 2013;375:89-96.
35. Zhu Y, Hu Y, Huang T, Zhang Y, Li Z, Luo C, Luo Y, Yuan H, Hisatome I, Yamamoto T, Cheng J: High uric acid directly inhibits insulin signalling and induces insulin resistance. Biochem Biophys Res Commun 2014;447:707-714.
36. Boyce JA, Peebles RS: Regulation of Th9-type pulmonary immune responses: A new role for COX-2. Am J Respir Crit Care Med 2013;187:785-786.
37. Bryn T, Yaqub S, Mahic M, Henjum K, Aandahl EM, Tasken K: LPS-activated monocytes suppress T-cell immune responses and induce FOXP3+ T cells through a COX-2-PGE2-dependent mechanism. Int Immunol 2008;20:235-245.
38. Hatada EN, Krappmann D, Scheidereit C: NF-kappaB and the innate immune response. Curr Opin Immunol 2000;12:52-58.
39. Hayden MS, West AP, Ghosh S: NF-kappaB and the immune response. Oncogene 2006;25:6758-6780.
40. Laouini D, Elkhal A, Yalcindag A, Kawamoto S, Oettgen H, Geha RS: COX-2 inhibition enhances the TH2 immune response to epicutaneous sensitization. J Allergy Clin Immunol 2005;116:390-396.
41. Yang Y, Bazhin AV, Werner J, Karakhanova S: Reactive oxygen species in the immune system. Int Rev Immunol 2013;32:249-270.
42. Guo Y, Zhang Y, Hong K, Luo F, Gu Q, Lu N, Bai A: AMPK inhibition blocks ROS-NFkappaB signaling and attenuates endotoxemia-induced liver injury. PLoS One 2014;9:e86881.
43. Poltorak A, He X, Smirnova I, Liu MY, Van Huffel C, Du X, Birdwell D, Alejos E, Silva M, Galanos C, Freudenberg M, Ricciardi-Castagnoli P, Layton B, Beutler B: Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 1998;282:2085-2088.
44. Hagenbuch B, Meier PJ: Organic anion transporting polypeptides of the OATP/ SLC21 family: phylogenetic classification as OATP/ SLCO superfamily, new nomenclature and molecular/functional properties. Pflugers Arch 2004;447:653-665.
45. Tsukamoto K, Kinoshita M, Kojima K, Mikuni Y, Kudo M, Mori M, Fujita M, Horie E, Shimazu N, Teramoto T: Synergically increased expression of CD36, CLA-1 and CD68, but not of SR-A and LOX-1, with the progression to foam cells from macrophages. J Atheroscler Thromb 2002;9:57-64.
46. Li D, Wang D, Wang Y, Ling W, Feng X, Xia M: Adenosine monophosphate-activated protein kinase induces cholesterol efflux from macrophage-derived foam cells and alleviates atherosclerosis in apolipoprotein E-deficient mice. J Biol Chem 2010;285:33499-33509.
47. Kushiyama A, Okubo H, Sakoda H, Kikuchi T, Fujishiro M, Sato H, Kushiyama S, Iwashita M, Nishimura F, Fukushima T, Nakatsu Y, Kamata H, Kawazu S, Higashi Y, Kurihara H, Asano T: Xanthine oxidoreductase is involved in macrophage foam cell formation and atherosclerosis development. Arterioscler Thromb Vasc Biol 2012;32:291-298.