Novel, selective EPO receptor ligands lacking erythropoietic activity reduce infarct size in acute myocardial infarction in rats

Pharmacological Research

Volumn 113, Issue , 2016, Pages 62-70

  Kiss, Krisztina ^a   Csonka, Csaba ^b   Pálóczi, János ^a,c   Pipis, Judit ^a,c   Görbe, Anikó ^a,c   Kocsis, Gabriella F ^a,c   Murlasits, Zsolt ^c,d   Sárközy, Márta ^b   Szűcs, Gergő ^b   Holmes, Christopher P ^f   Pan, Yijun ^f   Bhandari, Ashok ^f   Csont, Tamás ^b   Shamloo, Mehrdad ^e   Woodburn, Kathryn W ^f,g   Ferdinandy, Péter ^a,c,h   Bencsik, Péter ^a,c  

^a UNIVERSITY OF SZEGED   (Hungary)

^b UNIVERSITY OF SZEGED   (Hungary)

^c PHARMAHUNGARY GROUP   (Hungary)

^d QATAR UNIVERSITY   (Qatar)

^e STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f AFFYMAX RESEARCH INSTITUTE   (United States)

^g Avalanche Biotechnologies   (United States)

^h SEMMELWEIS UNIVERSITY   (Hungary)

Author keywords

Acute myocardial infarction; B type natriuretic peptide; Cardioprotection; Darbepoetin; Erythropoietin; Non erythropoietic EPO receptor ligand

Indexed keywords

ALANYLCYSTEINYLLEUCYLTYROSYLLEUCYLCYSTEINYLARGINYLTYROSYLGLYCYLARGINYLVALYLHISTIDINYLASPARAGINYLALANYLLEUCYLGLUTAMYLCYSTEINYLGLUTAMINYLPROLYLLEUCYLARGINYLLYSINE 1,1' [OXYBIS[(1 OXO 2,1 ETHANEDIYL)OXY]]BIS 2,5 PYRROLIDINEDIONE; ALANYLCYSTEINYLTYROSYLALANYLCYSTEINYLHISTIDINYLTYROSYLGLYCYLPROLYLISOLEUCYLTHREONYLASPARAGINYLALANYLLEUCYLVALYLCYSTEINYLGLUTAMINYLPROLYLPROLYLLYSINE IMINODIACETIC ACID; BRAIN NATRIURETIC PEPTIDE; CYCLOSPORIN A; ERYTHROPOIETIN; NOVEL ERYTHROPOIESIS STIMULATING PROTEIN; RECOMBINANT ERYTHROPOIETIN; UNCLASSIFIED DRUG; CARDIOTONIC AGENT; ERYTHROPOIETIN, RAT; LIGAND;

ACUTE HEART INFARCTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CARDIAC MUSCLE CELL; CELL PROTECTION; CONTROLLED STUDY; CORONARY ARTERY OCCLUSION; DOSE RESPONSE; DRUG ACTIVITY; DRUG HALF LIFE; ERYTHROPOIETIC ACTIVITY; HEART INFARCTION SIZE; HUMAN; HUMAN CELL; IN VIVO STUDY; MALE; NEWBORN; NONHUMAN; PILOT STUDY; PRIORITY JOURNAL; RAT; REPERFUSION INJURY; ANIMAL; CARDIAC MUSCLE; DRUG EFFECTS; HEART INFARCTION; METABOLISM; MYOCARDIAL ISCHEMIA REPERFUSION INJURY; WISTAR RAT;

ANIMALS; CARDIOTONIC AGENTS; ERYTHROPOIETIN; LIGANDS; MALE; MYOCARDIAL INFARCTION; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; MYOCYTES, CARDIAC; NATRIURETIC PEPTIDE, BRAIN; PILOT PROJECTS; RATS; RATS, WISTAR;

EID: 84982145768     PISSN: 10436618     EISSN: 10961186     Source Type: Journal    
DOI: 10.1016/j.phrs.2016.08.013     Document Type: Article

References (51)

1. [1] Bokemeyer, C., Aapro, M.S., Courdi, A., et al. EORTC guidelines for the use of erythropoietic proteins in anaemic patients with cancer: 2006 update. Eur. J. Cancer 43 (2007), 258–270.
2. [2] Sanchis-Gomar, F., Garcia-Gimenez, J.L., Pareja-Galeano, H., Romagnoli, M., Perez-Quilis, C., Lippi, G., Erythropoietin and the heart: physiological effects and the therapeutic perspective. Int. J. Cardiol. 171 (2014), 116–125.
3. [3] Wright, G.L., Hanlon, P., Amin, K., Steenbergen, C., Murphy, E., Arcasoy, M.O., Erythropoietin receptor expression in adult rat cardiomyocytes is associated with an acute cardioprotective effect for recombinant erythropoietin during ischemia-reperfusion injury. FASEB J. 18 (2004), 1031–1033.
4. [4] Depping, R., Kawakami, K., Ocker, H., et al. Expression of the erythropoietin receptor in human heart. J. Thorac. Cardiovasc. Surg. 130 (2005), 877–878.
5. [5] Brines, M., Grasso, G., Fiordaliso, F., et al. Erythropoietin mediates tissue protection through an erythropoietin and common beta-subunit heteroreceptor. Proc. Natl. Acad. Sci. U. S. A. 101 (2004), 14907–14912.
6. [6] Collino, M., Thiemermann, C., Cerami, A., Brines, M., Flipping the molecular switch for innate protection and repair of tissues: long-lasting effects of a non-erythropoietic small peptide engineered from erythropoietin. Pharmacol. Ther., 10, 2015.
7. [7] Xu, K., George, I., Klotz, S., et al. Erythropoietin derivate improves left ventricular systolic performance and attenuates left ventricular remodeling in rats with myocardial infarct-induced heart failure. J. Cardiovasc. Pharmacol. 56 (2010), 506–512.
8. [8] Latini, R., Brines, M., Fiordaliso, F., Do non-hemopoietic effects of erythropoietin play a beneficial role in heart failure. Heart Fail. Rev. 13 (2008), 415–423.
9. [9] Lipsic, E., Schoemaker, R.G., van der Meer, P., Voors, A.A., van Veldhuisen, D.J., van Gilst, W.H., Protective effects of erythropoietin in cardiac ischemia: from bench to bedside. J. Am. Coll. Cardiol. 48 (2006), 2161–2167.
10. [10] Palazzuoli, A., Ruocco, G., Pellegrini, M., et al. The role of erythropoietin stimulating agents in anemic patients with heart failure: solved and unresolved questions. Ther Clin Risk Manag 10 (2014), 641–650, 10.2147/TCRM.S61551 eCollection.
11. [11] Leist, M., Ghezzi, P., Grasso, G., et al. Derivatives of erythropoietin that are tissue protective but not erythropoietic. Science 305 (2004), 239–242.
12. [12] Besarab, A., Bolton, W.K., Browne, J.K., et al. The effects of normal as compared with low hematocrit values in patients with cardiac disease who are receiving hemodialysis and epoetin. N. Engl. J. Med. 339 (1998), 584–590.
13. [13] Najjar, S.S., Rao, S.V., Melloni, C., et al. Intravenous erythropoietin in patients with ST-segment elevation myocardial infarction: REVEAL: a randomized controlled trial. JAMA 305 (2011), 1863–1872.
14. [14] Ott, I., Schulz, S., Mehilli, J., et al. Erythropoietin in patients with acute ST-segment elevation myocardial infarction undergoing primary percutaneous coronary intervention: a randomized, double-blind trial. Circ. Cardiovasc. Interv. 3 (2010), 408–413.
15. [15] Fan, Q., Leuther, K.K., Holmes, C.P., et al. Preclinical evaluation of Hematide, a novel erythropoiesis stimulating agent, for the treatment of anemia. Exp. Hematol. 34 (2006), 1303–1311.
16. [16] Bennett, C.L., Jacob, S., Hymes, J., Usvyat, L.A., Maddux, F.W., Anaphylaxis and hypotension after administration of peginesatide. N. Engl. J. Med. 370 (2014), 2055–2056.
17. [17] Fiordaliso, F., Chimenti, S., Staszewsky, L., et al. A nonerythropoietic derivative of erythropoietin protects the myocardium from ischemia-reperfusion injury. Proc. Natl. Acad. Sci. U. S. A. 102 (2005), 2046–2051.
18. [18] Moon, C., Krawczyk, M., Paik, D., et al. Erythropoietin, modified to not stimulate red blood cell production, retains its cardioprotective properties. J. Pharmacol. Exp. Ther. 316 (2006), 999–1005.
19. [19] Takeyama, T., Takemura, G., Kanamori, H., et al. Asialoerythropoietin, a nonerythropoietic derivative of erythropoietin, displays broad anti-heart failure activity. Circ. Heart Fail. 5 (2012), 274–285.
20. [20] Xu, X., Cao, Z., Cao, B., et al. Carbamylated erythropoietin protects the myocardium from acute ischemia/reperfusion injury through a PI3K/Akt-dependent mechanism. Surgery 146 (2009), 506–514.
21. [21] Brines, M., Cerami, A., Erythropoietin-mediated tissue protection: reducing collateral damage from the primary injury response. J. Intern. Med. 264 (2008), 405–432.
22. [22] Casadevall, N., Nataf, J., Viron, B., et al. Pure red-cell aplasia and antierythropoietin antibodies in patients treated with recombinant erythropoietin. N. Engl. J. Med. 346 (2002), 469–475.
23. [23] Fan, Q., Leuther, K.K., Holmes, C.P., et al. Preclinical evaluation of Hematide, a novel erythropoiesis stimulating agent, for the treatment of anemia. Exp. Hematol. 34 (2006), 1303–1311.
24. [24] Burger, D., Xenocostas, A., Feng, Q.P., Molecular basis of cardioprotection by erythropoietin. Curr. Mol. Pharmacol. 2 (2009), 56–69.
25. [25] Burley, D.S., Baxter, G.F., B-type natriuretic peptide at early reperfusion limits infarct size in the rat isolated heart. Basic Res. Cardiol. 102 (2007), 529–541.
26. [26] Kemperman, H., van den Berg, M., Kirkels, H., de Jonge, N., B-type natriuretic peptide (BNP) and N-terminal proBNP in patients with end-stage heart failure supported by a left ventricular assist device. Clin. Chem. 50 (2004), 1670–1672.
27. [27] Csont, T., Gorbe, A., Bereczki, E., et al. Biglycan protects cardiomyocytes against hypoxia/reoxygenation injury: role of nitric oxide. J. Mol. Cell. Cardiol. 48 (2010), 649–652.
28. [28] Görbe, A., Giricz, Z., Szunyog, A., et al. Role of cGMP-PKG signaling in the protection of neonatal rat cardiac myocytes subjected to simulated ischemia/reoxygenation. Basic Res. Cardiol. 105 (2010), 643–650.
29. [29] Bencsik, P., Paloczi, J., Kocsis, G.F., et al. Moderate inhibition of myocardial matrix metalloproteinase-2 by ilomastat is cardioprotective. Pharmacol. Res. 80 (2014), 36–42, 10.1016/j.phrs.2013.12.007 Epub.
30. [30] Csonka, C., Kupai, K., Kocsis, G.F., et al. Measurement of myocardial infarct size in preclinical studies. J. Pharmacol. Toxicol. Methods 61 (2010), 163–170.
31. [31] Calvillo, L., Latini, R., Kajstura, J., et al. Recombinant human erythropoietin protects the myocardium from ischemia-reperfusion injury and promotes beneficial remodeling. Proc. Natl. Acad. Sci. U. S. A. 100 (2003), 4802–4806.
32. [32] Lipsic, E., van der Meer, P., Henning, R.H., et al. Timing of erythropoietin treatment for cardioprotection in ischemia/reperfusion. J. Cardiovasc. Pharmacol. 44 (2004), 473–479.
33. [33] Bullard, A.J., Govewalla, P., Yellon, D.M., Erythropoietin protects the myocardium against reperfusion injury in vitro and in vivo. Basic Res. Cardiol. 100 (2005), 397–403.
34. [34] Nishihara, M., Miura, T., Miki, T., et al. Erythropoietin affords additional cardioprotection to preconditioned hearts by enhanced phosphorylation of glycogen synthase kinase-3 beta. Am. J. Physiol. Heart Circ. Physiol. 291 (2006), H748–H755.
35. [35] 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. 61 (2007), 671–675.
36. [36] Baker, J.E., Kozik, D., Hsu, A.K., Fu, X., Tweddell, J.S., Gross, G.J., Darbepoetin alfa protects the rat heart against infarction: dose-response, phase of action, and mechanisms. J. Cardiovasc. Pharmacol. 49 (2007), 337–345.
37. [37] Gao, E., Boucher, M., Chuprun, J.K., Zhou, R.H., Eckhart, A.D., Koch, W.J., Darbepoetin alfa, a long-acting erythropoietin analog, offers novel and delayed cardioprotection for the ischemic heart. Am. J. Physiol. Heart Circ. Physiol. 293 (2007), H60–H68.
38. [38] Ren, B., Wu, H., Yin, R., et al. B-type natriuretic peptide pretreatment attenuates heart ischemia-reperfusion injury in rats. Transplant. Proc. 42 (2010), 4496–4498.
39. [39] Wu, B., Jiang, H., Lin, R., Cui, B., Wen, H., Lu, Z., Pretreatment with B-type natriuretic peptide protects the heart from ischemia-reperfusion injury by inhibiting myocardial apoptosis. Tohoku J. Exp. Med. 219 (2009), 107–114.
40. [40] Fang, J., Wu, L., Chen, L., Postconditioning attenuates cardiocyte ultrastructure injury and apoptosis by blocking mitochondrial permeability transition in rats. Acta Cardiol. 63 (2008), 377–387.
41. [41] Huhn, R., Heinen, A., Weber, N.C., Hollmann, M.W., Schlack, W., Preckel, B., Hyperglycaemia blocks sevoflurane-induced postconditioning in the rat heart in vivo: cardioprotection can be restored by blocking the mitochondrial permeability transition pore. Br. J. Anaesth. 100 (2008), 465–471.
42. [42] Lim, W.Y., Messow, C.M., Berry, C., Cyclosporin variably and inconsistently reduces infarct size in experimental models of reperfused myocardial infarction: a systematic review and meta-analysis. Br. J. Pharmacol. 165 (2012), 2034–2043.
43. [43] De Paulis, D., Chiari, P., Teixeira, G., et al. Cyclosporine A at reperfusion fails to reduce infarct size in the in vivo rat heart. Basic Res. Cardiol., 108, 2013, 379.
44. [44] Brines, M., Patel, N.S., Villa, P., et al. Nonerythropoietic, tissue-protective peptides derived from the tertiary structure of erythropoietin. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 10925–10930.
45. [45] Ahmet, I., Tae, H.J., Juhaszova, M., et al. A small nonerythropoietic helix B surface peptide based upon erythropoietin structure is cardioprotective against ischemic myocardial damage. Mol. Med. 17 (2011), 194–200.
46. [46] Ali-Hassan-Sayegh, S., Mirhosseini, S.J., Tahernejad, M., et al. Administration of erythropoietin in patients with myocardial infarction: does it make sense? An updated and comprehensive meta-analysis and systematic review. Cardiovasc. Revasc. Med. 16 (2015), 179–189.
47. [47] van Rijt, W.G., van, G.H., Ploeg, R.J., Leuvenink, H.G., Erythropoietin-mediated protection in kidney transplantation: nonerythropoietic EPO derivatives improve function without increasing risk of cardiovascular events. Transpl. Int. 27 (2014), 241–248.
48. [48] Brines, M., Dunne, A.N., van, V.M., et al. ARA 290, a nonerythropoietic peptide engineered from erythropoietin, improves metabolic control and neuropathic symptoms in patients with type 2 diabetes. Mol. Med. 20 (2015), 658–666, 10.2119/molmed.2014.00215.
49. [49] Boesch, S., Nachbauer, W., Mariotti, C., et al. Safety and tolerability of carbamylated erythropoietin in Friedreich's ataxia. Mov. Disord. 29 (2014), 935–939.
50. [50] van Rijt, W.G., Nieuwenhuijs-Moeke, G.J., van, G.H., et al. ARA290, a non-erythropoietic EPO derivative, attenuates renal ischemia/reperfusion injury. J. Transl. Med., 11, 2013, 9, 10.1186/1479-5876-11-9.
51. [51] Dahan, A., Dunne, A., Swartjes, M., et al. ARA 290 improves symptoms in patients with sarcoidosis-associated small nerve fiber loss and increases corneal nerve fiber density. Mol. Med. 19 (2013), 334–345, 10.2119/molmed.2013.00122.