Allopurinol reduces antigen-specific and polyclonal activation of human T cells

Frontiers in Immunology

Volumn 3, Issue SEP, 2012, Pages

  Pérez Mazliah, Damián ^a,c   Albareda, María C ^a   Alvarez, María G ^b   Lococo, Bruno ^b   Bertocchi, Graciela L ^b   Petti, Marcos ^b   Viotti, Rodolfo J ^b   Laucella, Susana A ^a  

^a Ciudad Autónoma de Buenos Aires ^*  (Argentina)

^b Hospital Interzonal General de Agudos Eva Peronquot   (Argentina)

^c NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

Allopurinol; Anti inflammatory; T cells; Th1 cytokines; Xanthine oxidase

Indexed keywords

EID: 84874253719     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2012.00295     Document Type: Article

References (84)

1. Albareda, M. C., Laucella, S. A., Alvarez, M. G., Armenti, A. H., Bertochi, G., Tarleton, R. L., and Postan, M. (2006). Trypanosoma cruzi modulates the profile of memory CD8+ T cells in chronic Chagas' disease patients. Int. Immunol. 18, 465-471.
2. Albareda, M. C., Olivera, G. C., Laucella, S. A., Alvarez, M. G., Fernandez, E. R., Lococo, B., Viotti, R., Tarleton, R. L., and Postan, M. (2009). Chronic human infection with Trypanosoma cruzi drives CD4+ T cells to immune senescence. J. Immunol. 183, 4103-4108.
3. Aldaba-Muruato, L. R., Moreno, M. G., Shibayama, M., Tsutsumi, V., and Muriel, P. (2012). Protective effects of allopurinol against acute liver damage and cirrhosis induced by carbon tetrachloride: modulation of NF-κB, cytokine production and oxidative stress. Biochim. Biophys. Acta 1820, 65-75.
4. Almeida, D. R., Carvalho, A. C., Branco, J. N., Pereira, A. P., Correa, L., Vianna, P. V., Buffolo, E., and Martinez, E. E. (1996). Chagas' disease reactivation after heart transplantation: efficacy of allopurinol treatment. J. Heart Lung Transplant. 15, 988-992.
5. Apt, W., Aguilera, X., Arribada, A., Pérez, C., Miranda, C, Sanchez, G., Zulantay, I., Cortés, P., Rodríguez, J., and Juri, D. (1998). Treatment of chronic Chagasandapos; disease with itraconazole and allopurinol. Am. J. Trop. Med. Hyg. 59, 133-138.
6. Apt, W., Arribada, A., Zulantay, I., Sánchez, G., Vargas, S. L., and Rodríguez, J. (2003). Itraconazole or allopurinol in the treatment of chronic American trypanosomiasis: the regression and prevention of electrocardiographic abnormalities during 9 years of follow-up. Ann. Trop. Med. Parasitol. 97, 23-29.
7. Apt, W., Arribada, A., Zulantay, I., Solari, A., Sánchez, G., Mundaca, K., Coronado, X., Rodríguez, J., Gil, L. C., and Osuna, A. (2005). Itraconazole or allopurinol in the treatment of chronic American trypanosomiasis: the results of clinical and parasitological examinations 11 years post-treatment. Ann. Trop. Med. Parasitol. 99, 733-741.
8. Arellano, F., and Sacristán, J. A. (1993). Allopurinol hypersensi-tivity syndrome: a review. Ann. Pharmacother. 27, 337-343.
9. Augustin, A. J., Böker, T., Blumenröder, S. H., Lutz, J., and Spitznas, M. (1994). Free radical scavenging and antioxidant activity of allopurinol and oxypurinol in experimental lens-induced uveitis. Invest. Ophthalmol. Vis. Sci. 35, 3897-3904.
10. Augustin, A. J., Spitznas, M., Sekundo, W., Koch, F., Lutz, J., Meller, D., Grus, F. H., Wegener, A., and Blumenröder, S. H. (1996). Effects of allopurinol and steroids on inflammation and oxidative tissue damage in experimental lens induced uveitis: a biochemical and morphological study. Br. J. Ophthalmol. 80,451-457.
11. Barnett, J. C., and Touchon, R. C. (1990). Therapy of ischemic car-diomyopathy with pentoxifylline. Angiology 41, 1048-1052.
12. Berlinger, W. G., Park, G. D., and Spector, R. (1985). The effect of dietary protein on the clearance of allopurinol and oxypurinol. N. Engl. J. Med. 313,771-776.
13. Bestetti, R. B., and Theodoropoulos, T.a.D. (2009). A systematic review of studies on heart transplantation for patients with end-stage Chagas' heart disease. J. Card. Fail. 15, 249-255.
14. Breithaupt, B., and Tittel, M. (1982). Kinetics of allopurinol after single intravenous and oral doses. Noninteraction with benzbro-marone and hydrochlorothiazide. Eur.JClin. Pharmacol. 22, 77-84.
15. Castro, P., Vukasovic, J. L., Chiong, M., Díaz-Araya, G., Alcaino, H., Copaja, M., Valenzuela, R., Greig, D., Pérez, O., Corbalán, R., and Lavandero, S. (2005). Effects of carvedilol on oxidative stress and chronotropic response to exercise in patients with chronic heart failure. Eur. J. Heart Fail. 7, 1033-1039.
16. Castro, P. F., Greig, D., Pérez, O., Moraga, F., Chiong, M., Díaz-Araya, G., Padilla, I., Nazzal, C., Jalil, J. E., Vukasovic, J. L., Moreno, M., Corbalán, R., and Lavandero, S. (2003). Relation between oxidative stress, catecholamines, and impaired chronotropic response to exercise in patients with chronic heart failure secondary to ischemic or idiopathic dilated cardiomyopathy. Am. J. Cardiol. 92, 215-218.
17. Castro, P. F., Miranda, R., Verdejo, H. E., Greig, D., Gabrielli, L. A., Alcaino, H., Chiong, M., Bustos, C., Garcia, L., Mellado, R., Vukasovic, J. L., Godoy, I., and Lavandero, S. (2008). Pleiotropic effects of atorvastatin in heart failure: role in oxidative stress, inflammation, endothelial function, and exercise capacity. J. Heart Lung Transplant. 27, 435-441.
18. Celis, R., Torre-Martinez, G., and Torre-Amione, G. (2008). Evidence for activation of immune system in heart failure: is there a role for anti-inflammatory therapy? Curr. Opin. Cardiol. 23, 254-260.
19. Cheng, X., Ding, Y., Xia, C., Tang, T., Yu, X., Xie, J., Liao, M., Yao, R., Chen, Y., Wang, M., and Liao, Y.-H. (2009). Atorvastatin modulates Th1/Th2 response in patients with chronic heart failure. J. Card. Fail. 15, 158-162.
20. Chocair, P., Duley, J., Simmonds, H. A., Cameron, J. S., Ianhez, L., Arap, S., and Sabbaga, E. (1993). Low-dose allopurinol plus azathio-prine/cyclosporin/prednisolone, a novel immunosuppressive regimen. Lancet 342, 83-84.
21. Correa-Costa, M., Braga, T. T., Semedo, P., Hayashida, C. Y., Bechara, L. R. G., Elias, R. M., Barreto, C. R., Silva-Cunha, C., Hyane, M. I., Gonçalves, G. M., Brum, P. C., Fujihara, C., Zatz, R., Pacheco-Silva, A., Zamboni, D. S., and Camara, N. O. S. (2011). Pivotal role of toll-like receptors 2 and 4, its adaptor molecule MyD88, and inflam-masome complex in experimental tubule-interstitial nephritis. PLoS ONE 6:e29004. doi: 10.1371/jour-nal.pone.0029004
22. Cosulich, M. E., Rubartelli, A., Risso, A., Cozzolino, F., and Bargellesi, A. (1987). Functional characterization of an antigen involved in an early step of T-cell activation. Proc. Natl. Acad. Sci. U.S.A. 84, 4205-4209.
23. Dardalhon, V., Korn, T., Kuchroo, V K., and Anderson, A. C. (2008). Role of Th1 and Th17 cells in organ-specific autoimmunity. J. Autoimmun. 31, 252-256.
24. Day, R. O., Miners, J., Birkett, D. J., Graham, G. G., and Whitehead, A. (1988a). Relationship between plasma oxipurinol concentrations and xanthine oxidase activity in volunteers dosed with allopurinol. Br. J. Clin. Pharmacol. 26, 429-434.
25. Day, R. O., Miners, J. O., Birkett, D. J., Whitehead, A., Naidoo, D., Hayes, J., and Savdie, E. (1988b). Allopurinol dosage selection: relationships between dose and plasma oxipurinol and urate concentrations and urinary urate excretion. Br. J. Clin. Pharmacol. 26, 423-428.
26. Demirel, U., Yalni{dotless}z, M., Aygün, C., Orhan, C., Tuzcu, M., Sahin, K., Ozercan, I. H., and Bahçecioglu, I. H. (2012). Allopurinol ameliorates thioacetamide-induced acute liver failure by regulating cellular redox-sensitive transcription factors in rats. Inflammation 35, 1549-1557.
27. Deschamps, A. M., and Spinale, E G. (2006). Pathways of matrix metalloproteinaseinduction in heart failure: bioactive molecules and transcriptional regulation. Cardiovasc. Res. 69, 666-676.
28. Devadas, S., Zaritskaya, L., Rhee, S. G., Oberley, L., and Williams, M. S. (2002). Discrete generation of superoxide and hydrogen peroxide by T cell receptor stimulation: selective regulation of mitogen-activated protein kinase activation and fas lig-and expression. J. Exp. Med. 195, 59-70.
29. Dröge, W (2002). Free radicals in the physiological control of cell function. Physiol. Rev. 82, 47-95.
30. Elion, G. B. (1988). The Purine Path to Chemotherapy. Nobel Lecture. Research Triangle Park, NC: Burroughs Welcome Co.
31. Emmerson, B. T., Gordon, R. B., Cross, M., and Thomson, D. B. (1987). Plasma oxipurinol concentrations during allopurinol therapy. Br. J. Rheumatol. 26, 445-449.
32. Gallerano, R. H., Marr, J. J., and Sosa, R. R. (1990). Therapeutic efficacy of allopurinol in patients with chronic Chagasandapos; disease. Am. J. Trop. Med. Hyg. 43, 159-166.
33. Gardiner, S. J., Gearry, R. B., Burt, M. J., Chalmers-Watson, T., Chapman, B. A., Ross, A. G., Stedman, C.a.M., Huelsen, A., and Barclay, M. L. (2011). Allopurinol might improve response to azathioprine and 6-mercaptopurine by correcting an unfavorable metabolite ratio. J. Gastroenterol. Hepatol. 26, 49-54.
34. George, J., Carr, E., Davies, J., Belch, J. J. F., and Struthers, A. (2006). High-dose allopurinol improves endothe-lial function by profoundly reducing vascular oxidative stress and not by lowering uric acid. Circulation 114, 2508-2516.
35. George, J., and Struthers, A. D. (2009). Role of urate, xanthine oxidase and the effects of allopurinol in vascular oxidative stress. Vasc. Health Risk Manag. 5, 265-272.
36. Govani, S. M., and Higgins, P. D. R. (2010). Combination of thiopurines and allopurinol: adverse events and clinical benefit in IBD. J. Crohns Colitis 4, 444-449.
37. Graham, S., Day, R. O., Wong, H., Mclachlan, A. J., Bergendal, L., Miners, J. O., and Birkett, D. J. (1996). Pharmacodynamics of oxypurinol after administration of allopurinol to healthy subjects. Br. J Clin. Pharmacol. 41, 299-304.
38. Griffiths, H. R., Dunston, C. R., Bennett, S. J., Grant, M. M., Phillips, D. C., and Kitas, G. D. (2011). Free radicals and redox signalling in T-cells during chronic inflammation and ageing. Biochem. Soc. Trans. 39, 1273-1278.
39. Grus, E H., Augustin, A. J., Loeffler, K., Lutz, J., and Pfeiffer, N. (2003). Immunological effects of allopurinol in the treatment of experimental autoimmune uveitis (EAU) after onset of the disease. Eur. J. Ophthalmol. 13, 185-191.
40. Guerra, P., Frias, J., Ruiz, B., Soto, A., Carcas, A., Govantes, C., Montuenga, C., and Fernández, A. (2001). Bioequivalence of allopurinol and its metabolite oxipurinol in two tablet formulations. J. Clin. Pharm. Ther. 26, 113-119.
41. Hara, T., Jung, L. K., Bjorndahl, J. M., and Fu, S. M. (1986). Human T cell activation. III. Rapid induction of a phosphorylated 28 kD/32 kD disulfide-linked early activation antigen (EA 1) by 12-o-tetradecanoyl phorbol-13-acetate, mitogens, and antigens. J. Exp. Med. 164, 1988-2005.
42. Hare, J. M., Mangal, B., Brown, J., Fisher, C., Freudenberger, R., Colucci, W S., Mann, D. L., Liu, P., Givertz, M. M., Schwarz, R. P., and Investigators, O.-C. (2008). Impact of oxypurinol in patients with symptomatic heart failure. Results of the OPT-CHF study. J. Am. Coll. Cardiol. 51,2301-2309.
43. Harzallah, K., Belhadj, R., Jemli, B., Haloues, M., Berraies, N., Gargouri, S., Hmida, J., Battikh, R., and Manaa, J. (2010). Visceral leishma-niasis in a renal transplant recipient treated with allopurinol. Saudi J. Kidney Dis. Transpl. 21, 105-108.
44. Kang, S.-M., Lim, S., Song, H., Chang, W., Lee, S., Bae, S.-M., Chung, J. H., Lee, H., Kim, H.-G., Yoon, D.-H., Kim, T. W., Jang, Y., Sung, J.-M., Chung, N.-S., and Hwang, K.-C. (2006). Allopurinol modulates reactive oxygen species generation and Ca2+ overload in ischemia-reperfused heart and hypoxia-reoxygenated cardiomy-ocytes. Eur. J. Pharmacol. 535, 212-219.
45. Kato, C., Sato, K., Wakabayashi, A., and Eishi, Y. (2000). The effects of allopurinol on immune function in normal BALB/c and SCID mice. Int. J. Immunopharmacol. 22, 547-556.
46. Kaya, M., Moriwaki, Y., Ka, T., Inokuchi, T., Yamamoto, A., Takahashi, S., Tsutsumi, Z., Tsuzita, J., Oku, Y., and Yamamoto, T. (2006). Plasma concentrations and urinary excretion of purine bases (uric acid, hypoxanthine, and xanthine) and oxypurinol after rigorous exercise. Metabolism 55, 103-107.
47. Kramer, W. G., and Feldman, S. (1977). Apparent metabolism of allopurinol by blood-a preliminary report. Res. Commun. Chem. Pathol. Pharmacol. 18,781-784.
48. Kurashige, S., Akuzawa, Y., and Mitsuhashi, S. (1985). Purine metabolic enzymes in lymphocytes. IV. Effects of enzyme inhibitors and enzyme substrates on the blastogenic responses of human lymphocytes. Scand. J. Immunol. 22, 1-7.
49. Landmesser, U., Spiekermann, S., Dikalov, S., Tatge, H., Wilke, R., Kohler, C., Harrison, D. G., Hornig, B., and Drexler, H. (2002). Vascular oxidative stress and endothelial dysfunction in patients with chronic heart failure: role of xanthine-oxidase and extracellular superoxide dismutase. Circulation 106, 3073-3078.
50. Laucella, S. A., Postan, M., Martin, D., Hubby Fralish, B., Albareda, M. C., Alvarez, M. G., Lococo, B., Barbieri, G., Viotti, R. J., and Tarleton, R. L. (2004). Frequency of interferon-gamma-producing T cells specific for Trypanosoma cruzi inversely correlates with disease severity in chronic human Chagas disease. J. Infect. Dis. 189,909-918.
51. Lee, H. Y., Ariyasinghe, J. T., and Thirumoorthy, T. (2008). Allopurinol hypersensitivity syndrome: a preventable severe cutaneous adverse reaction? Singapore Med. J. 49, 384-387.
52. Lee, P.-C., Ho, I.-C., and Lee, T.-C. (2005). Oxidative stress mediates sodium arsenite-induced expression of heme oxygenase-1, monocyte chemoattractant protein-1, and interleukin-6 in vascular smooth muscle cells. Toxicol Sci. 85, 541-550.
53. Los, M., Schenk, H., Hexel, K., Baeuerle, P. A., Droge, W., and Schulze-Osthoff, K. (1995). IL-2 gene expression and NF-kappa B activation through CD28 requires reactive oxygen production by 5-lipoxygenase. EMBO J. 14, 3731-3740.
54. Matsue, H., Edelbaum, D., Shalhevet, D., Mizumoto, N., Yang, C., Mummert, M. E., Oeda, J., Masayasu, H., and Takashima, A. (2003). Generation and function of reactive oxygen species in dendritic cells during antigen presentation. J. Immunol. 171, 3010-3018.
55. Matsuhiro, B., Conte, A. F., Damonte, E. B., Kolender, A. A., Matulewicz, M. C., Mejías, E. G., Pujol, C. A., and Zúñiga, E. A. (2005). Structural analysis and antiviral activity of a sulfated galactan from the red seaweed Schizymenia binderi (Gigartinales, Rhodophyta). Carbohydr. Res. 340, 2392-2402.
56. Mizuno, K., Okamoto, H., and Horio, T. (2004). Inhibitory influences of xanthine oxidase inhibitor and angiotensin I-converting enzyme inhibitor on multinucleated giant cell formation from monocytes by downregulation of adhesion molecules and purinergic receptors. Br. J. Dermatol. 150, 205-210.
57. Momeni, A., Reiszadae, M., and Aminjavaheri, M(2002). Treatment of cutaneous leish-maniasis with a combination of allopurinol and low-dose meglu-mine antimoniate. Int. J. Dermatol. 41,441-443.
58. Momeni, A. Z., and Aminjavaheri, M. (1995). Treatment of recurrent cutaneous Leishmaniasis. Int. J. Dermatol. 34, 129-133.
59. Moorhouse, P. C., Grootveld, M., Halliwell, B., Quinlan, J. G., and Gutteridge, J. M. (1987). Allopurinol and oxypurinol are hydroxyl radical scavengers. FEBS Lett. 213,23-28.
60. Murrell, G. A., and Rapeport, W. G. (1986). Clinical pharmacokinetics of allopurinol. Clin. Pharmacokinet. 11,343-353.
61. Namazi, M. R. (2004). Cetirizine and allopurinol as novel weapons against cellular autoimmune disorders. Int. Immunopharmacol. 4, 349-353.
62. Ng, S. C., Chan, F. K. L., and Sung, J. J. Y (2011). Review article: the role of non-biological drugs in refractory inflammatory bowel disease. Aliment. Pharmacol. Ther. 33, 417-427.
63. Oláh, T., Régely, K., and Mándi, Y. (1994). The inhibitory effects of allopurinol on the production and cytotoxicity of tumor necrosis factor. Naunyn Schmiedebergs Arch. Pharmacol. 350, 96-99.
64. Pacher, P., Nivorozhkin, A., and Szabó, C. (2006). Therapeutic effects of xanthine oxidase inhibitors: renaissance half a century after the discovery of allopurinol. Pharmacol. Rev. 58,87-114.
65. Panomvana, D., Sripradit, S., and Angthararak, S. (2008). Higher therapeutic plasma oxypurinol concentrations might be required for gouty patients with chronic kidney disease. J. Clin. Rheumatol. 14,6-11.
66. Pea, F. (2005). Pharmacology of drugs for hyperuricemia. Mech. Kinet. Interact. Contrib. Nephrol. 147, 35-46.
67. Pérez-Mazliah, D., Álvarez, M. G., Cooley, G., Lococo, B., Bertocchi, G., Petti, M., Albareda, M. C., Armenti, A., Tarleton, R., Laucella, S., and Viotti, R. (2012). Sequential combined treatment with allopurinol and benznidazole in the chronic phase of Trypanosoma cruzi infection: a pilot study. J. Antimicrob. Chemother. (in press).
68. Pluim, H. J., Van Deuren, M., and Wetzels, J. F. (1998). The allopurinol hypersensitivity syndrome. Neth. J. Med. 52, 107-110.
69. Risso, A., Cosulich, M. E., Rubartelli, A., Mazza, M. R., and Bargellesi, A. (1989). MLR3 molecule is an activation antigen shared by human B, T lymphocytes and T cell precursors. Eur. I Immunol. 19, 323-328.
70. Rodnan, G. P., Robin, J. A., Tolchin, S. F., and Elion, G. B. (1975). Allopurinol and gouty hyper-uricemia. Efficacy of a single daily dose. JAMA 231, 1143-1147.
71. Skudicky, D., Sliwa, K., Bergemann, A., Candy, G., and Sareli, P. (2000). Reduction in Fas/APO-1 plasma concentrations correlates with improvement in left ventricular function in patients with idiopathic dilated cardiomyopathy treated with pentoxifylline. Heart 84, 438-439.
72. Sliem, H., and Nasr, G. (2011). Left ventricular structure and function in prediabetic adults: relationship with insulin resistance. J. Cardiovasc. Dis. Res. 2, 23-28.
73. Sliwa, K., Woodiwiss, A., Candy, G., Badenhorst, D., Libhaber, C., Norton, G., Skudicky, D., and Sareli, P. (2002). Effects of pentoxifylline on cytokine profiles and left ventricular performance in patients with decompensated congestive heart failure secondary to idiopathic dilated cardiomyopathy. Am. J. Cardiol. 90, 1118-1122.
74. Sliwa, K., Woodiwiss, A., Kone, V. N., Candy, G., Badenhorst, D., Norton, G., Zambakides, C., Peters, E, and Essop, R. (2004). Therapy of ischemic cardiomyopathy with the immunomodulating agent pentoxifylline: results of a randomized study. Circulation 109, 750-755.
75. Smith, M. A., Blaker, P., Marinaki, A. M., Anderson, S. H., Irving, P. M., and Sanderson, J. D. (2012). Optimising outcome on thiopurines in inflammatory bowel disease by co-prescription of allopurinol. J. Crohns Colitis 6, 905-912.
76. Stamp, L. K., Barclay, M. L., OandApos;Donnell, J. L., Zhang, M., Drake, J., Frampton, C., and Chapman, P. T. (2011). Relationship between serum urate and plasma oxypurinol in the management of gout: determination of minimum plasma oxypurinol concentration to achieve a target serum urate level. Clin. Pharmacol. Ther. 90, 392-398.
77. Stocker, S. L., Williams, K. M., Mclachlan, A. J., Graham, G. G., and Day, R. O. (2008). Pharmacokinetic and pharmacodynamic interaction between allopurinol and probenecid in healthy subjects. Clin. Pharmacokinet. 47, 111-118.
78. Torrance, H. L., Benders, M. J., Derks, J. B., Rademaker, C. M. A., Bos, A. F., Van Den Berg, P., Longini, M., Buonocore, G., Venegas, M., Baquero, H., Visser, G. H. A., and Van Bel, E. (2009). Maternal allopurinol during fetal hypoxia lowers cord blood levels of the brain injury marker S-100B. Pediatrics 124, 350-357.
79. Turnheim, K., Krivanek, P., and Oberbauer, R. (1999). Pharmacokinetics and pharma-codynamics of allopurinol in elderly and young subjects. Br. J. Clin. Pharmacol. 48, 501-509.
80. Van Dijk, A. J., Parvizi, N., Taverne, M. A., and Fink-Gremmels, J. (2008). Placental transfer and pharmacokinetics of allopurinol in late pregnant sows and their fetuses. J. Vet. Pharmacol. Ther. 31, 489-495.
81. Williams, M. S., and Kwon, J. (2004). T cell receptor stimulation, reactive oxygen species, and cell signaling. Free Radic. Biol. Med. 37, 1144-1151.
82. Yan, Z., and Banerjee, R. (2010). Redox remodeling as an immunoregu-latory strategy. Biochemistry 49, 1059-1066.
83. Yan, Z., Garg, S. K., and Banerjee, R. (2010). Regulatory T cells interfere with glutathione metabolism in dendritic cells and T cells. J. Biol. Chem. 285,41525-41532.
84. Yano, S., Yano, N., Rodriguez, N., Baek, J. H., Que, X., Yamamura, Y., and Kim, S. J. (1998). Suppression of intracellular hydrogen peroxide generation and catalase levels in CD8+ T-lymphocytes from HIV+ individuals. Free Radic. Biol. Med. 24, 349-359