"Effects of recombinant human erythropoietin high mimicking abuse doses on oxidative stress processes in rats"

Biomedicine and Pharmacotherapy

Volumn 82, Issue , 2016, Pages 355-363

  Bianchi, Sara ^a   Fusi, Jonathan ^a   Franzoni, Ferdinando ^a   Giovannini, Luca ^a   Galetta, Fabio ^a   Mannari, Claudio ^a   Guidotti, Emanuele ^a   Tocchini, Leonardo ^a   Santoro, Gino ^a  

^a UNIVERSITY OF PISA   (Italy)

Author keywords

Erythropoietin; Free radicals; Hydroxyl radicals; Peroxyl radicals; Peroxynitrite

Indexed keywords

8 ISOPROSTAGLANDIN F2 ALPHA; 8 ISOPROSTANE; ERYTHROPOIETIN; NITRIC OXIDE; RECOMBINANT ERYTHROPOIETIN; 8-EPI-PROSTAGLANDIN F2ALPHA; EPO PROTEIN, HUMAN; NITRIC ACID DERIVATIVE; NITRITE; PROSTAGLANDIN F2 ALPHA; REACTIVE OXYGEN METABOLITE; RECOMBINANT PROTEIN; SCAVENGER;

ANIMAL EXPERIMENT; ANTIOXIDANT ACTIVITY; ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DOPING; DRUG DOSE COMPARISON; DRUG MEGADOSE; DRUG SCREENING; HEMATOCRIT; IN VIVO STUDY; KIDNEY CONCENTRATING CAPACITY; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; WISTAR RAT; ANALOGS AND DERIVATIVES; ANIMAL; BLOOD; DOSE RESPONSE; DRUG EFFECTS; HUMAN; METABOLISM; SUBCUTANEOUS DRUG ADMINISTRATION; URINE;

ANIMALS; DINOPROST; DOSE-RESPONSE RELATIONSHIP, DRUG; ERYTHROPOIETIN; FREE RADICAL SCAVENGERS; HEMATOCRIT; HUMANS; INJECTIONS, SUBCUTANEOUS; MALE; NITRATES; NITRITES; OXIDATIVE STRESS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; RECOMBINANT PROTEINS;

EID: 84970015774     PISSN: 07533322     EISSN: 19506007     Source Type: Journal    
DOI: 10.1016/j.biopha.2016.05.022     Document Type: Article

References (73)

1. Lacombe C., Mayeux P. Biology of erythropoietin. Haematologica 1998, 83:724-732.
2. Pitsiladis Y.P., Durussel J., Rabin O. An integrative 'omics' solution to the detection of recombinant human erythropoietin and blood doping. Br. J. Sports Med. 2014, 48:856-861. 10.1136/bjsports-2014-093529.
3. Jelkmann W. Regulation of erythropoietin production. J. Physiol. 2011, 589:1251-1258. 10.1113/jphysiol.2010.195057.
4. Wang L., Di L., Noguchi C.T. Erythropoietin, a novel versatile player regulating energy metabolism beyond the erythroid system. Int. J. Biol. Sci. 2014, 10:921-939. (Review). 10.7150/ijbs.9518.
5. Kumar R., Jaggi A.S., Singh N. Effects of erythropoietin on memory deficits and brain oxidative stress in the mouse models of dementia. Korean J. Physiol. Pharmacol. 2010, 14:345-352. 10.4196/kjpp.2010.14.5.345.
6. Jelkmann W. Erythropoietin: structure, control of production, and function. Physiol. Rev. 1992, 72:449-489.
7. Elliott S. Erythropoiesis-stimulating agents and other methods to enhance oxygen transport. Br. J. Pharmacol. 2008, 154:529-541. 10.1038/bjp.2008.89.
8. Stohlawetz P.J., Dzirlo L., Hergovich N., Lackner E., Mensik C., Eichler H.G., et al. Effects of erythropoietin on platelet reactivity and thrombopoiesis in humans. Blood 2000, 95:2983-2999.
9. Gareau R., Audran M., Baynes R.D., Flowers C.H., Duvallet A., Senécal L., et al. Erythropoietin abuse in athletes. Nature 1996, 380:113.
10. Adamson J.W., Vapnek D. Recombinant erythropoietin to improve athletic performance. N. Engl. J. Med. 1991, 324:698-699.
11. Li H., Förstermann U. Nitric oxide in the pathogenesis of vascular disease. J. Pathol. 2000, 190:244-254.
12. Packer L. Oxidants, antioxidants nutrients and the athlete. J. Sports Sci. 1997, 15:353-363.
13. Vaziri N.D., Zhou X.J., Smith J., Oveisi F., Baldwin K., Purdy R.E. In vivo and in vitro pressor effects of erythropoietin in rats. Am. J. Physiol. 1995, 269:838-845.
14. Katavetin P., Tungsanga K., Eiam-Ong S., Nangaku M. Antioxidative effects of erythropoietin. Kidney Int. Suppl. 2007, 107:10-15.
15. Rjiba-Touati K., Ayed-Boussema I., Guedri Y., Achour A., Bacha H., Abid-Essefi S. Effect of recombinant human erythropoietin on mitomycin C-induced oxidative stress and genotoxicity in rat kidney and heart tissues. Hum. Exp. Toxicol. 2016, 35:53-62. 10.1177/0960327115577521.
16. Inal M., Kanbak G., Sen S., Akyüz F., Sunal E. Antioxidant status and lipid peroxidation in hemodialysis patients undergoing erythropoietin and erythropoietin-vitamin E combined therapy. Free Radic. Res. 1999, 31:211-216.
17. Mimic-Oka J., Simic T., Djukanovic L. Epoetin treatment improves red blood cell and plasma antioxidant capacity in hemodialysis patients. Renal Fail. 2002, 24:77-87.
18. Calò L.A., Stanic L., Davis P.A., Pagnin E., Munaretto G., Fusaro M., et al. Effect of epoetin on HO-1 mRNA level and plasma antioxidants in hemodialysis patients. Int. J. Clin. Pharmacol. Ther. 2003, 41:187-192.
19. Rancourt M.E., Rodrigue M.E., Agharazii M., Lariviere R., Lebel M. Role of oxidative stress in erythropoietin-induced hypertension in uremic rats. Am. J. Hypertens. 2010, 23:314-320. 10.1038/ajh.2009.242.
20. Winston G.W., Regoli F., Dugas A.J., Fong J.H., Blanchard K.A. A rapid gas chromatographic assay for determining oxyradical scavenging capacity of antioxidants and biological fluids. Free Radic. Biol. Med. 1998, 24:480-493.
21. Regoli F., Winston G.W. Quantification of total oxidant scavenging capacity of antioxidants for peroxynitrite, peroxyl radicals, and hydroxyl radicals. Toxicol. Appl. Pharmacol. 1999, 156:96-105.
22. Franzoni F., Quiñones-Galvan A., Regoli F., Ferrannini E., Galetta F. A comparative study of the in vitro antioxidant activity of statins. Int. J. Cardiol. 2003, 90:317-321.
23. Franzoni F., Plantinga Y., Femia F.R., Bartolomucci F., Gaudio C., Regoli F., et al. Plasma antioxidant activity and cutaneous microvascular endothelial function in athletes and sedentary controls. Biomed. Pharmacother. 2004, 58:432-436.
24. Siems W., Carluccio F., Radenkovic S., Grune T., Hampl H. Oxidative stress in renal anemia of hemodialysis patients is mitigated by epoetin treatment. Kidney Blood Press. Res. 2005, 28:295-301.
25. Lamon S., Russell A.P. The role and regulation of erythropoietin (EPO) and its receptor in skeletal muscle: how much do we really know?. Front. Physiol. 2013, 4:176. 10.3389/fphys.2013.00176.
26. Smith K.J., Bleyer A.J., Little W.C., Sane D.C. The cardiovascular effects of erythropoietin. Cardiovasc. Res. 2003, 59:538-548.
27. Heuberger J.A., Cohen Tervaert J.M., Schepers F.M., Vliegenthart A.D., Rotmans J.I., Daniels J.M., et al. Erythropoietin doping in cycling: lack of evidence for efficacy and a negative risk-benefit. Br. J. Clin. Pharmacol. 2013, 75:1406-1421. 10.1111/bcp.12034.
28. Cao X., Chen Z., Yu Z., Ge Y., Zeng X. Pharmacokinetics of PEGylated recombinant human erythropoietin in rats. J Anal Methods Chem. 2014, 10.1155/2014/918686.
29. Vaziri N.D. Mechanism of erythropoietin-induced hypertension. Am. J. Kidney Dis. 1999, 33:821-828.
30. Bode-Böger S.M., Böger R.H., Kuhn M., Radermacher J., Frolich J.C. Recombinant human erythropoietin enhances vasoconstrictor tone via endothelin-1 and constrictor prostanoids. Kidney Int. 1996, 50:1255-1261.
31. Tsakiris D. Morbidity and mortality reduction associated with the use of erythropoietin. Nephron 2000, 85:2-8.
32. Spivak J.L., Hogans B.B. The in vivo metabolism of recombinant human erythropoietin in the rat. Blood 1989, 73:90-99.
33. Kinoshita H., Ohishi N., Tokura S., Okazaki A. Pharmacokinetics and distribution of recombinant human erythropoietin in rats with renal dysfunction. Arzneimittelforschung 1992, 42:682-686.
34. Statler P.A., McPherson R.J., Bauer L.A., Kellert B.A., Juul S.E. Pharmacokinetics of high-dose recombinant erythropoietin in plasma and brain of neonatal rats. Pediatr. Res. 2007, 61:671-675.
35. Fisher J.W. Erythropoietin: physiology and pharmacology update. Exp. Biol. Med. 2003, 228:1-14. (Review).
36. Ehrenreich H., Hasselblatt M., Dembowski C., Cepek L., Lewczuk P., Stiefel M., et al. Erythropoietin therapy for acute stroke is both safe and beneficial. Mol. Med. 2002, 8:495-505.
37. Chen H.C., Tsai J.C., Tsai J.H., Lai Y.H. Recombinant human erythropoietin enhances superoxide production by FMLP-stimulated polymorphonuclear leukocytes in hemodialysis patients. Kidney Int. 1997, 52:1390-1394.
38. Toba H., Sawai N., Morishita M., Murata S., Yoshida M., Nakashima K., et al. Chronic treatment with recombinant human erythropoietin exerts renoprotective effects beyond hematopoiesis in streptozotocin-induced diabetic rat. Eur. J. Pharmacol. 2009, 612:106-114. 10.1016/j.ejphar.2009.03.065.
39. Toba H., Nakashima K., Oshima Y., Kojima Y., Tojo C., Nakano A., et al. Erythropoietin prevents vascular inflammation and oxidative stress in subtotal nephrectomized rat aorta beyond haematopoiesis. Clin. Exp. Pharmacol. Physiol. 2010, 37:1139-1146. 10.1111/j.1440-1681.2010.05445.
40. Al-Qahtani J.M., Abdel-Wahab B.A., Abd El-Aziz S.M. Long-term moderate dose exogenous erythropoietin treatment protects from intermittent hypoxia-induced spatial learning deficits and hippocampal oxidative stress in young rats. Neurochem. Res. 2014, 39:161-171. 10.1007/s11064-013-1201-2.
41. Usberti M., Gerardi G.M., Bufano G., Tira P., Micheli A., Albertini A., et al. Effects of erythropoietin and vitamin E-modified membrane on plasma oxidative stress markers and anemia of hemodialyzed patients. Am. J. Kidney Dis. 2002, 40:90-599.
42. Hirayama A., Nagase S., Gotoh M., Ueda A., Ishizu T., Yoh K., et al. Reduced serum hydroxyl radical scavenging activity in erythropoietin therapy resistant renal anemia. Free Radic. Res. 2002, 36:1155-1161.
43. Wang X.Q., Vaziri N.D. Erythropoietin depresses nitric oxide synthase expression by human endothelial cells. Hypertension 1999, 33:894-899.
44. Kanagy N.L., Perrine M.F., Cheung D.K., Walker B.R. Erythropoietin administration in vivo increases vascular nitric oxide synthase expression. J. Cardiovasc. Pharmacol. 2003, 42:527-533.
45. Vaziri N.D., Zhou X.J., Naqvi F., Smith J., Oveisi F., Wang Z.Q., et al. Role of nitric oxide resistance in erythropoietin-induced hypertension in rats with chronic renal failure. Am. J. Physiol. 1996, 271:113-122.
46. Banerjee D., Rodriguez M., Nag M., Adamson J.W. Exposure of endothelial cells to recombinant human erythropoietin induces nitric oxide synthase activity. Kidney Int. 2000, 57:1895-1904.
47. Ni Z., Wang X.Q., Vaziri N.D. Nitric oxide metabolism in erythropoietininduced hypertension: effect of calcium channel blockade. Hypertension 1998, 32:724-729.
48. Wilcox C.S., Deng X., Doll A.H., Snellen H., Welch W.J. Nitric oxide mediates renal vasodilation during erythropoietin-induced polycythemia. Kidney Int. 1993, 44:430-435.
49. Kusano E., Akimoto T., Inoue M., Masunaga Y., Umino T., Ono S., et al. Human recombinant erythropoietin inhibits interleukin-1beta-stimulated nitric oxide and cyclic guanosine monophosphate production in cultured rat vascular smooth-muscle cells. Nephrol. Dial. Transplant. 1999, 14:597-603.
50. Moreau C., Larivière R., Kingma I., Grose J.H., Lebel M. Chronic nitric oxide inhibition aggravates hypertension in erythropoietin-treated renal failure rats. Clin. Exp. Hypertens. 2000, 22:663-674.
51. Ruschitzka F.T., Wenger R.H., Stallmach T., Quaschning T., de Wit C., Wagner K., et al. Nitric oxide prevents cardiovascular disease and determines survival in polyglobulic mice overexpressing erythropoietin. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:11609-11613.
52. Noguchi K., Yamashiro S., Matsuzaki T., Sakanashi M., Nakasone J., Miyagi K., et al. Effect of 1-week treatment with erythropoietin on the vascular endothelial function in anaesthetized rabbits. Br. J. Pharmacol. 2001, 133:395-405.
53. Halliwell B., Gutteridge J.M.C. Free Radicals in Biology and Medicine 1999, Oxford University Press, Oxford. 3rd ed.
54. Massey K.A., Nicolaou A. Lipidomics of polyunsaturatedfatty-acid-derived oxygenatedmetabolites. Biochem. Soc. Trans. 2011, 39:1240-1246.
55. Massey K.A., Nicolaou A. Lipidomics of oxidized polyunsaturated fatty acids. Free Radic. Biol. Med. 2013, 59:45-55.
56. Halliwell B., Chirico S. Lipid peroxidation: its mechanism, measurement, and significance. Am. J. Clin. Nutr. 1993, 57:715S-724S.
57. Gutteridge J.M. Lipid peroxidation and antioxidants as biomarkers of tissue damage. Clin. Chem. 1995, 41:1819-1828. (Review).
58. Moore K., Roberts L.J. Measurement of lipid peroxidation. Free Radic. Res. 1998, 28:659-671. (Review).
59. De Zwart L.L., Meerman J.H., Commandeur J.N., Vermeulen N.P. Biomarkers of free radical damage applications in experimental animals and in humans. Free Radic. Biol. Med. 1999, 26:202-226. (Review).
60. Wagner B.A., Buettner G.R., Burns C.P. Free radical-mediated lipid peroxidation in cells: oxidizability is a function of cell lipid bis-allylic hydrogen content. Biochemistry 1994, 33:4449-4453.
61. Porter N.A., Caldwell S.E., Mills K.A. Mechanisms of free radical oxidation of unsaturated lipids. Lipids 1995, 30:277-290. (Review).
62. Roberts L.J., Morrow J.D. Measurement of F2-isoprostanes as an index of oxidative stress in vivo. Free Radic. Biol. Med. 2000, 28:505-513.
63. Galano J.M., Lee Y.Y., Durand T., Lee J.C. Special issue on analytical methods for oxidized biomolecules and antioxidants the use of isoprostanoids as biomarkers of oxidative damage, and their role in human dietary intervention studies. Free Radic. Res. 2015, 49:583-598.
64. Petrosino T., Serafini M. Antioxidant modulation of F2-isoprostanes in humans: a systematic review. Crit. Rev. Food Sci. Nutr. 2014, 54:1202-1221.
65. Spickett C.M., Wiswedel I., Siems W., Zarkovic K., Zarkovic N. Advances in methods for the determination of biologically relevant lipid peroxidation products. Free Radic. Res. 2010, 44:1172-1202.
66. Gopaul N.K., Nourooz-Zadeh J., Mallet A.I., Änggård E.E. Formation of PGF2- isoprostanes during the oxidative modification of low density lipoprotein. Biochem. Biophys. Res. Commun. 1994, 200:338-343.
67. Montuschi P., Barnes P.J., Roberts L.J. Isoprostanes: markers and mediators of oxidative stress. FASEB J. 2004, 18:1780-1791. (Review).
68. Morrow J.D., Awad J.A., Boss H.J., Blair I.A., Roberts J. Non-cyclooxygenase derived prostanoids (F2-isoprostanes) are formed in situ on phospholipids. Proc. Natl. Acad. Sci. 1992, 89:10721-10725.
69. Morrow J.D., Hill K.E., Burk R.F., Nammour T., Badr K., Roberts L.J. A series of prostaglandin F2-like compounds are produced in vivo in humans by a non-cyclooxygenase, free-radical-catalyzed mechanism. Proc. Natl. Acad. Sci. 1990, 87:9383-9387.
70. Griffiths H., Moller L., Bartosz G., Bas A., Bertoni-Freddari C., Collins A., et al. Biomarkers. Mol. Aspects Med. 2002, 23:101-208.
71. Roberts L.J., Morrow J.D. The generation and actions of isoprostanes. Biochim. Biophys. Acta 1997, 1345:121-135.
72. Miller E., Morel A., Saso L., Saluk J. Isoprostanes and neuroprostanes as biomarkers of oxidative stress in neurodegenerative diseases. Oxid. Med. Cell. Longev. 2014, 2014:1-10.
73. Guertin K.A., Grant R.K., Arnold K.B., Burwell L., Hartline J., Goodman P.J., et al. Effect of long-term vitamin E and selenium supplementation on urine F(2)-isoprostanes, a biomarker of oxidative stress. Free Radic. Biol. Med. 2016, 95:349-356.