Resistance to recombinant human erythropoietin therapy in a rat model of chronic kidney disease associated anemia

International Journal of Molecular Sciences

Volumn 17, Issue 1, 2016, Pages

  Garrido, Patrícia ^a   Ribeiro, Sandra ^b   Fernandes, João ^a,b   Vala, Helena ^c   Rocha Pereira, Petronila ^d   Bronze da Rocha, Elsa ^b   Belo, Luís ^b   Costa, Elísio ^b   Santos Silva, Alice ^b   Reis, Flávio ^a,e  

^a UNIVERSITY OF COIMBRA   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

^c POLYTECHNIC INSTITUTE OF VISEU   (Portugal)

^d UNIVERSITY OF BEIRA INTERIOR   (Portugal)

^e UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

Anemia; Chronic kidney disease; Erythropoiesis; Inflammation and fibrosis; Iron metabolism; Kidney hypoxia; Remnant kidney rat model; Resistance to rHuEPO therapy

Indexed keywords

RECOMBINANT ERYTHROPOIETIN; ANTIBODY; ERYTHROPOIETIN; IRON; RECOMBINANT PROTEIN;

ANEMIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOCHEMICAL ANALYSIS; BLOOD PRESSURE MONITORING; CHRONIC KIDNEY DISEASE; CONTROLLED STUDY; ERYTHROCYTE COUNT; ERYTHROPOIESIS; GENE OVEREXPRESSION; HEMATOCRIT; HEMATOLOGIC DISEASE; HISTOPATHOLOGY; INFLAMMATION; IRON METABOLISM; MALE; NEPHRECTOMY; NONHUMAN; RAT; ANIMAL; BLOOD; CHRONIC KIDNEY FAILURE; COMPLICATION; DRUG RESISTANCE; DUODENUM; HUMAN; IMMUNOLOGY; KIDNEY; LIVER; METABOLISM; WISTAR RAT;

ANEMIA; ANIMALS; ANTIBODIES; DRUG RESISTANCE; DUODENUM; ERYTHROPOIETIN; HUMANS; IRON; KIDNEY; LIVER; MALE; RATS; RATS, WISTAR; RECOMBINANT PROTEINS; RENAL INSUFFICIENCY, CHRONIC;

EID: 84951811485     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms17010028     Document Type: Article

References (74)

1. Zhang, Q.L.; Rothenbacher, D. Prevalence of chronic kidney disease in population-based studies: Systematic review. BMC. Public Health 2008, 8, 117. [CrossRef] [PubMed]
2. Coresh, J.; Selvin, E.; Stevens, L.A.; Manzi, J.; Kusek, J.W.; Eggers, P.; van Lente, F.; Levey, A.S. Prevalence of chronic kidney disease in the United States. JAMA 2007, 298, 2038-2047. [CrossRef] [PubMed]
3. Stevens, L.A.; Li, S.; Wang, C.; Huang, C.; Becker, B.N.; Bomback, A.S.; Brown, W.W.; Burrows, N.R.; Jurkovitz, C.T.; McFarlane, S.I.; et al. Prevalence of CKD and comorbid illness in elderly patients in the United States: Results from the Kidney Early Evaluation Program (KEEP). Am. J. Kidney Dis. 2010, 55, S23-S33. [CrossRef] [PubMed]
4. Iwanaga, Y.; Miyazaki, S. Heart failure, chronic kidney disease, and biomarkers-An integrated viewpoint. Circ. J. 2010, 74, 1274-1282. [CrossRef] [PubMed]
5. Berl, T.; Henrich, W. Kidney-heart interactions: Epidemiology, pathogenesis, and treatment. Clin. J. Am. Soc. Nephrol. 2006, 1, 8-18. [CrossRef] [PubMed]
6. Ninomiya, T.; Kiyohara, Y.; Kubo, M.; Tanizaki, Y.; Doi, Y.; Okubo, K.; Wakugawa, Y.; Hata, J.; Oishi, Y.; Shikata, K.; et al. Chronic kidney disease and cardiovascular disease in a general Japanese population: The Hisayama Study. Kidney Int. 2005, 68, 228-236. [CrossRef] [PubMed]
7. Schiffrin, E.L.; Lipman, M.L.; Mann, J.F. Chronic kidney disease: Effects on the cardiovascular system. Circulation 2007, 116, 85-97. [CrossRef] [PubMed]
8. Cases-Amenos, A.; Martinez-Castelao, A.; Fort-Ros, J.; Bonal-Bastons, J.; Ruiz, M.P.; Valles-Prats, M.; Coll-Piera, E.; Galcerán-Gui, J.M. Investigadores del Estudio Micenas. Prevalence of anaemia and its clinical management in patients with stages 3-5 chronic kidney disease not on dialysis in Catalonia: MICENAS I study. Nefrologia 2014, 34, 189-198. [PubMed]
9. Lankhorst, C.E.;Wish, J.B. Anemia in renal disease: Diagnosis and management. Blood Rev. 2010, 24, 39-47. [CrossRef] [PubMed]
10. Weiss, G. Iron metabolism in the anemia of chronic disease. Biochim. Biophys. Acta 2009, 1790, 682-693. [CrossRef] [PubMed]
11. Guidi, G.C.; Lechi Santonastaso, C. Advancements in anemias related to chronic conditions. Clin. Chem. Lab. Med. 2010, 48, 1217-1226. [CrossRef] [PubMed]
12. Obrador, G.T.; Roberts, T.; St Peter,W.L.; Frazier, E.; Pereira, B.J.; Collins, A.J. Trends in anemia at initiation of dialysis in the United States. Kidney Int. 2001, 60, 1875-1884. [CrossRef] [PubMed]
13. Foley, R.N.; Parfrey, P.S.; Harnett, J.D.; Kent, G.M.; Murray, D.C.; Barre, P.E. The impact of anemia on cardiomyopathy, morbidity, and and mortality in end-stage renal disease. Am. J. Kidney Dis. 1996, 28, 53-61. [CrossRef]
14. Moreno, F.; Sanz-Guajardo, D.; Lopez-Gomez, J.M.; Jofre, R.; Valderrabano, F. Increasing the hematocrit has a beneficial effect on quality of life and is safe in selected hemodialysis patients. Spanish Cooperative Renal Patients Quality of Life Study Group of the Spanish Society of Nephrology. J. Am. Soc. Nephrol. 2000, 11, 335-342. [PubMed]
15. Palmer, S.C.; Navaneethan, S.D.; Craig, J.C.; Johnson, D.W.; Tonelli, M.; Garg, A.X.; Pellegrini, F.; Ravani, P.; Jardine, M.; Perkovic, V.; et al. Meta-analysis: Erythropoiesis-stimulating agents in patients with chronic kidney disease. Ann. Intern. Med. 2010, 153, 23-33. [CrossRef] [PubMed]
16. Clement, F.M.; Klarenbach, S.; Tonelli, M.; Johnson, J.A.; Manns, B.J. The impact of selecting a high hemoglobin target level on health-related quality of life for patients with chronic kidney disease: A systematic review and meta-analysis. Arch. Intern. Med. 2009, 169, 1104-1112. [CrossRef] [PubMed]
17. Parfrey, P.S.; Lauve, M.; Latremouille-Viau, D.; Lefebvre, P. Erythropoietin therapy and left ventricular mass index in CKD and ESRD patients: A meta-analysis. Clin. J. Am. Soc. Nephrol. 2009, 4, 755-762. [CrossRef] [PubMed]
18. Johnson, D.W.; Pollock, C.A.; Macdougall, I.C. Erythropoiesis-stimulating agent hyporesponsiveness. Nephrology 2007, 12, 321-330. [CrossRef] [PubMed]
19. Kilpatrick, R.D.; Critchlow, C.W.; Fishbane, S.; Besarab, A.; Stehman-Breen, C.; Krishnan, M.; Bradbury, B.D. Greater epoetin alfa responsiveness is associated with improved survival in hemodialysis patients. Clin. J. Am. Soc. Nephrol. 2008, 3, 1077-1083. [CrossRef] [PubMed]
20. Fukuma, S.; Yamaguchi, T.; Hashimoto, S.; Nakai, S.; Iseki, K.; Tsubakihara, Y.; Fukuhara, S. Erythropoiesis-stimulating agent responsiveness and mortality in hemodialysis patients: Results from a cohort study from the dialysis registry in Japan. Am. J. Kidney Dis. 2012, 59, 108-116. [CrossRef] [PubMed]
21. Drueke, T.B.; Eckardt, K.U. Role of secondary hyperparathyroidism in erythropoietin resistance of chronic renal failure patients. Nephrol. Dial. Transplant. 2002, 17, 28-31. [CrossRef] [PubMed]
22. Smrzova, J.; Balla, J.; Barany, P. Inflammation and resistance to erythropoiesis-stimulating agents-What do we know and what needs to be clarified? Nephrol. Dial. Transplant. 2005, 20, viii2-viii7. [CrossRef] [PubMed]
23. Costa, E.; Rocha, S.; Rocha-Pereira, P.; Reis, F.; Castro, E.; Teixeira, F.; Miranda, V.; do Sameiro Faria, M.; Loureiro, A.; Quintanilha, A.; et al. DMT1 (NRAMP2/DCT1) genetic variability and resistance to recombinant human erythropoietin therapy in chronic kidney disease patients under haemodialysis. Acta Haematol. 2008, 120, 11-13. [CrossRef] [PubMed]
24. Do Sameiro-Faria, M.; Ribeiro, S.; Rocha-Pereira, P.; Fernandes, J.; Reis, F.; Bronze-da-Rocha, E.; Miranda, V.; Quintanilha, A.; Costa, E.; Belo, L.; et al. Body mass index and resistance to recombinant human erythropoietin therapy in maintenance hemodialysis patients. Ren. Fail. 2013, 35, 1392-1398. [CrossRef] [PubMed]
25. Macdougall, I.C. Antibody-mediated pure red cell aplasia (PRCA): Epidemiology, immunogenicity and risks. Nephrol. Dial. Transplant. 2005, 20, iv9-iv15. [CrossRef] [PubMed]
26. Casadevall, N. Pure red cell aplasia and anti-erythropoietin antibodies in patients treated with epoetin. Nephrol. Dial. Transplant. 2003, 18, viii37-viii41. [CrossRef] [PubMed]
27. Eckardt, K.U.; Casadevall, N. Pure red-cell aplasia due to anti-erythropoietin antibodies. Nephrol. Dial. Transplant. 2003, 18, 865-869. [CrossRef] [PubMed]
28. Hung, S.C.; Lin, Y.P.; Tarng, D.C. Erythropoiesis-stimulating agents in chronic kidney disease: What have we learned in 25 years? J. Formos. Med. Assoc. 2014, 113, 3-10. [PubMed]
29. Garrido, P.; Ribeiro, S.; Fernandes, J.; Vala, H.; Bronze-da-Rocha, E.; Rocha-Pereira, P.; Belo, L.; Costa, E.; Santos-Silva, A.; Reis, F. Iron-hepcidin dysmetabolism, anemia and renal hypoxia, inflammation and fibrosis in the remnant kidney rat model. PLoS ONE 2015, 10, e0124048. [CrossRef] [PubMed]
30. Costa, E.; Pereira, B.J.; Rocha-Pereira, P.; Rocha, S.; Reis, F.; Castro, E.; Teixeira, F.; Miranda, V.; do Sameiro Faria, M.; Loureiro, A.; et al. Role of prohepcidin, inflammatory markers and iron status in resistance to rhEPO therapy in hemodialysis patients. Am. J. Nephrol. 2008, 28, 677-683. [CrossRef] [PubMed]
31. Nemeth, E.; Rivera, S.; Gabayan, V.; Keller, C.; Taudorf, S.; Pedersen, B.K.; Ganz, T. IL-6 mediates hypoferremia of inflammation by inducing the synthesis of the iron regulatory hormone hepcidin. J. Clin. Investig. 2004, 113, 1271-1276. [CrossRef] [PubMed]
32. Fernandes, J.C.; Garrido, P.; Ribeiro, S.; Rocha-Pereira, P.; Bronze-da-Rocha, E.; Belo, L.; Costa, E.; Reis, F.; Santos-Silva, A. Iron as the key modulator of hepcidin expression in erythroid antibody-mediated hypoplasia. Biomed. Res. Int. 2014, 2014, 421304. [CrossRef] [PubMed]
33. Garrido, P.; Costa, E.; Santos-Silva, A.; Reis, F. Animal models of kidney disease-associated anemia. In Frontiers in Drug Discovery, Erythropoietic Stimulating Agents; Costa, E., Santos-Silva, A., Reis, F., Eds.; Bentham E-Books Publisher: Berlin, Germany, 2013; pp. 61-80.
34. Strauch, M.; Gretz, N. Animal models to induce renal failure: A historical survey. Contrib. Nephrol. 1988, 60, 1-8. [PubMed]
35. Morrison, A.B. Experimentally induced chronic renal insufficiency in the rat. Lab. Investig. 1962, 11, 321-332. [PubMed]
36. Nankivell, B.J.; Chen, J.; Boadle, R.A.; Harris, D.C. The role of tubular iron accumulation in the remnant kidney. J. Am. Soc. Nephrol. 1994, 4, 1598-1607. [PubMed]
37. Nankivell, B.J.; Boadle, R.A.; Harris, D.C. Iron accumulation in human chronic renal disease. Am. J. Kidney Dis. 1992, 20, 580-584. [CrossRef]
38. Harris, D.C.; Tay, C.; Nankivell, B.J. Lysosomal iron accumulation and tubular damage in rat puromycin nephrosis and ageing. Clin. Exp. Pharmacol. Physiol. 1994, 21, 73-81. [CrossRef] [PubMed]
39. Izuhara, Y.; Nangaku, M.; Inagi, R.; Tominaga, N.; Aizawa, T.; Kurokawa, K.; van Ypersele de Strihou, C.; Miyata, T. Renoprotective properties of angiotensin receptor blockers beyond blood pressure lowering. J. Am. Soc. Nephrol. 2005, 16, 3631-3641. [CrossRef] [PubMed]
40. Egrie, J.C.; Browne, J.K. Development and characterization of darbepoetin alfa. Oncology 2002, 16, 13-22. [PubMed]
41. Higuchi, M.; Oh-eda, M.; Kuboniwa, H.; Tomonoh, K.; Shimonaka, Y.; Ochi, N. Role of sugar chains in the expression of the biological activity of human erythropoietin. J. Biol. Chem. 1992, 267, 7703-7709. [PubMed]
42. Locatelli, F.; Aljama, P.; Barany, P.; Canaud, B.; Carrera, F.; Eckardt, K.U.; Macdougall, I.C.; Macleod, A.; Hörl, W.H.; Wiecek, A.; et al. Erythropoiesis-stimulating agents and antibody-mediated pure red-cell aplasia: Here are we now and where do we go from here? Nephrol. Dial. Transplant. 2004, 19, 288-293. [CrossRef] [PubMed]
43. Casadevall, N. What is antibody-mediated pure red cell aplasia (PRCA)? Nephrol. Dial. Transplant. 2005, 20, iv3-iv8. [CrossRef] [PubMed]
44. Lombardero, M.; Kovacs, K.; Scheithauer, B.W. Erythropoietin: A hormone with multiple functions. Pathobiology 2011, 78, 41-53. [CrossRef] [PubMed]
45. Foley, R.N. Erythropoietin: Physiology and molecular mechanisms. Heart Fail. Rev. 2008, 13, 405-414. [CrossRef] [PubMed]
46. Fisher, J.W. Erythropoietin: Physiology and pharmacology update. Exp. Biol. Med. 2003, 228, 1-14.
47. Sviglerova, J.; Kuncova, J.; Nalos, L.; Tonar, Z.; Rajdl, D.; Stengl, M. Cardiovascular parameters in rat model of chronic renal failure induced by subtotal nephrectomy. Physiol. Res. 2010, 59, S81-S88. [PubMed]
48. Vaziri, N.D. Anemia and anemia correction: Surrogate markers or causes of morbidity in chronic kidney disease? Nat. Clin. Pract. Nephrol. 2008, 4, 436-445. [CrossRef] [PubMed]
49. Garimella, P.S.; Uhlig, K. Current issues in the management and monitoring of hypertension in chronic kidney disease. Curr. Opin. Nephrol. Hypertens. 2013, 22, 599-606. [CrossRef] [PubMed]
50. Vaziri, N.D. Cardiovascular effects of erythropoietin and anemia correction. Curr. Opin. Nephrol. Hypertens. 2001, 10, 633-637. [CrossRef] [PubMed]
51. Haase, V.H. Hypoxia-inducible factors in the kidney. Am. J. Physiol. Ren. Physiol. 2006, 291, F271-F281. [CrossRef] [PubMed]
52. Haase, V.H. The sweet side of HIF. Kidney Int. 2010, 78, 10-13. [CrossRef] [PubMed]
53. Shoji, K.; Tanaka, T.; Nangaku, M. Role of hypoxia in progressive chronic kidney disease and implications for therapy. Curr. Opin. Nephrol. Hypertens. 2014, 23, 161-168. [CrossRef] [PubMed]
54. Donderski, R.; Szczepanek, J.; Domagalski, K.; Tretyn, A.; Korenkiewicz, J.; Marszalek, A.; Szymański, A.; Wolski, Z.; Odrowąż -Sypniewska, G.; Manitius, J. Analysis of relative expression level of VEGF (vascular endothelial growth factor), HIF-1alpha (hypoxia inducible factor 1alpha) and CTGF (connective tissue growth factor) genes in chronic glomerulonephritis (CGN) patients. Kidney Blood Press. Res. 2013, 38, 83-91.
55. Rodriguez-Iturbe, B.; Garcia Garcia, G. The role of tubulointerstitial inflammation in the progression of chronic renal failure. Nephron Clin. Pract. 2010, 116, c81-c88. [CrossRef] [PubMed]
56. Risdon, R.A.; Sloper, J.C.; De Wardener, H.E. Relationship between renal function and histological changes found in renal-biopsy specimens from patients with persistent glomerular nephritis. Lancet 1968, 2, 363-366. [CrossRef]
57. Eddy, A.A. Progression in chronic kidney disease. Adv. Chronic Kidney Dis. 2005, 12, 353-365. [CrossRef] [PubMed]
58. Nemeth, E.; Tuttle, M.S.; Powelson, J.; Vaughn, M.B.; Donovan, A.; Ward, D.M.; Ganz, T.; Kaplan, J. Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization. Science 2004, 306, 2090-2093. [CrossRef] [PubMed]
59. Costa, E.; Swinkels, D.W.; Laarakkers, C.M.; Rocha-Pereira, P.; Rocha, S.; Reis, F.; Teixeira, F.; Miranda, V.; do Sameiro Faria, M.; Loureiro, A.; et al. Hepcidin serum levels and resistance to recombinant human erythropoietin therapy in haemodialysis patients. Acta Haematol. 2009, 122, 226-229. [CrossRef] [PubMed]
60. Preza, G.C.; Pinon, R.; Ganz, T.; Nemeth, E. Cellular catabolism of the iron-regulatory peptide hormone hepcidin. PLoS ONE 2013, 8, e58934. [CrossRef] [PubMed]
61. Zhang, A.S. Control of systemic iron homeostasis by the hemojuvelin-hepcidin axis. Adv. Nutr. 2010, 1, 38-45. [CrossRef] [PubMed]
62. Finberg, K.E. Unraveling mechanisms regulating systemic iron homeostasis. Hematol. Am. Soc. Hematol. Educ. Program. 2011, 2011, 532-537. [CrossRef] [PubMed]
63. Canavesi, E.; Alfieri, C.; Pelusi, S.; Valenti, L. Hepcidin and HFE protein: Iron metabolism as a target for the anemia of chronic kidney disease. World J. Nephrol. 2012, 1, 166-176. [CrossRef] [PubMed]
64. MacKenzie, E.L.; Iwasaki, K.; Tsuji, Y. Intracellular iron transport and storage: From molecular mechanisms to health implications. Antioxid. Redox Signal. 2008, 10, 997-1030. [CrossRef] [PubMed]
65. Zhang, A.S.; Yang, F.;Wang, J.; Tsukamoto, H.; Enns, C.A. Hemojuvelin-neogenin interaction is required for bone morphogenic protein-4-induced hepcidin expression. J. Biol. Chem. 2009, 284, 22580-22589. [CrossRef] [PubMed]
66. Tanno, T.; Porayette, P.; Sripichai, O.; Noh, S.J.; Byrnes, C.; Bhupatiraju, A.; Lee, Y.T.; Goodnough, J.B.; Harandi, O.; Ganz, T.; et al. Identification of TWSG1 as a second novel erythroid regulator of hepcidin expression in murine and human cells. Blood 2009, 114, 181-186. [CrossRef] [PubMed]
67. Suzuki, T.; Hanawa, H.; Jiao, S.; Ohno, Y.; Hayashi, Y.; Yoshida, K.; Kashimura, T.; Obata, H.; Minamino, T. Inappropriate expression of hepcidin by liver congestion contributes to anemia and relative iron deficiency. J. Card. Fail. 2014, 20, 268-277. [CrossRef] [PubMed]
68. Choi, H.S.; Song, S.H.; Lee, J.H.; Kim, H.J.; Yang, H.R. Serum hepcidin levels and iron parameters in children with iron deficiency. Korean J. Hematol. 2012, 47, 286-292. [CrossRef] [PubMed]
69. Artunc, F.; Risler, T. Serum erythropoietin concentrations and responses to anaemia in patients with or without chronic kidney disease. Nephrol. Dial. Transplant. 2007, 22, 2900-2908. [CrossRef] [PubMed]
70. Reis, F.; Rocha, L.; Ponte, L.; Alcobia, T.; Almeida, L.; Costa-Almeida, C.; Teixeira, F. Effect of preventive and regressive isosorbide 5-mononitrate treatment on catecholamine levels in plasma, platelets, adrenals, left ventricle and aorta in cyclosporin A-induced hypertensive rats. Life Sci. 2005, 77, 2514-2528. [CrossRef] [PubMed]
71. Urra, J.M.; de la Torre, M.; Alcazar, R.; Peces, R. Rapid method for detection of anti-recombinant human erythropoietin antibodies as a new form of erythropoietin resistance. Clin. Chem. 1997, 43, 848-849. [PubMed]
72. Teixeira, M.; Rodrigues-Santos, P.; Garrido, P.; Costa, E.; Parada, B.; Sereno, J.; Alves, R.; Belo, L.; Teixeira, F.; Santos-Silva, A.; et al. Cardiac antiapoptotic and proproliferative effect of recombinant human erythropoietin in a moderate stage of chronic renal failure in the rat. J. Pharm. Bioallied Sci. 2012, 4, 76-83. [PubMed]
73. Livak, K.J.; Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)). Method Methods 2001, 25, 402-408. [CrossRef] [PubMed]
74. Acs, G.; Zhang, P.J.; McGrath, C.M.; Acs, P.; McBroom, J.; Mohyeldin, A.; Liu, S.; Lu, H.; Verma, A. Hypoxia-inducible erythropoietin signaling in squamous dysplasia and squamous cell carcinoma of the uterine cervix and its potential role in cervical carcinogenesis and tumor progression. Am. J. Pathol. 2003, 162, 1789-1806. [PubMed]