Asialoerythropoietin exerts stronger Angiogenic activity than erythropoietin via its binding affinity to tissue

Cardiovascular Drugs and Therapy

Volumn 27, Issue 2, 2013, Pages 117-124

  Yanagawa, Takao ^a   Toba, Ken ^a,c   Kato, Kiminori ^a   Suzuki, Tomoyasu ^a   Minagawa, Shiro ^a   Saigawa, Takashi ^a   Ozawa, Takuya ^a   Oda, Masato ^a   Takayama, Tsugumi ^a   Hanawa, Haruo ^a   Higuchi, Masato ^b   Saito, Hideki ^b   Aizawa, Yoshifusa ^a  

^a NIIGATA UNIVERSITY MEDICAL AND DENTAL HOSPITAL   (Japan)

^b CHUGAI PHARMACEUTICAL CO LTD   (Japan)

^c NIIGATA UNIVERSITY GRADUATE SCHOOL OF MEDICAL AND DENTAL SCIENCES   (Japan)

Author keywords

Angiogenesis; Asialoerythropoietin; Erythropoietin; Tissue affinity

Indexed keywords

ANGIOGENESIS MODULATOR; RECOMBINANT ASIALOERYTHROPOIETIN; RECOMBINANT ERYTHROPOIETIN; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANGIOGENIC ACTIVITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DRUG ACTIVITY; DRUG BINDING; DRUG CLEARANCE; DRUG DISTRIBUTION; DRUG MECHANISM; DRUG TISSUE LEVEL; IN VITRO STUDY; IN VIVO STUDY; LEG ISCHEMIA; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; ASIALOGLYCOPROTEINS; ERYTHROPOIETIN; HEPARIN; INJECTIONS, INTRAMUSCULAR; ISCHEMIA; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED ICR; NEOVASCULARIZATION, PHYSIOLOGIC; PROTEIN BINDING;

EID: 84878344508     PISSN: 09203206     EISSN: 15737241     Source Type: Journal    
DOI: 10.1007/s10557-013-6438-0     Document Type: Article

References (45)

1. Isner JM. Therapeutic angiogenesis: A new frontier for vascular therapy. Vasc Med. 1996;1:79-87.
2. Rajagopalan S, Mohler 3rd ER, Lederman RJ, Mendelsohn FO, Saucedo JF, Goldman CK, et al. Regional angiogenesis with vascular endothelial growth factor in peripheral arterial disease: A phase II randomized, double-blind, controlled study of adenoviral delivery of vascular endothelial growth factor 121 in patients with disabling intermittent claudication. Circulation. 2003;108:1933-8.
3. Powell RJ, Simons M, Mendelsohn FO, Daniel G, Henry TD, Koga M, et al. Results of a double-blind, placebo-controlled study to assess the safety of intramuscular injection of hepatocyte growth factor plasmid to improve limb perfusion in patients with critical limb ischemia. Circulation. 2008;118:58-65.
4. Tateishi-Yuyama E, Matsubara H, Murohara T, Ikeda U, Shintani S, Masaki H, et al. Therapeutic angiogenesis for patients with limb ischemia by autologous transplantation of bone-marrow cells: A pilot study and a randomized control trial. Lancet. 2002;360:427-35.
5. Ribatti D, Vacca A, Roccaro AM, Crivellato E, Presta M. Erythropoietin as an angiogenic factor. Eur J Clin Invest. 2003;33:891-6.
6. Sasaki H, Bothner B, Dell A, Fukuda M. Carbohydrate structure of erythropoietin expressed in Chinese hamster ovary cells by a human erythropoietin cDNA. J Biol Chem. 1987;262:12059-76.
7. Imai N, Kawamura A, Higuchi M, Oh-eda M, Orita T, Kawaguchi T, et al. Physicochemical and biological comparison of recombinant human erythropoietin with human urinary erythropoietin. J Biochem. 1990;107:352-9.
8. Imai N, HiguchiM, Kawamura A, Tomonoh K, Oh-Eda M, Fujiwara M, et al. Physicochemical and biological characterization of asialoerythropoietin. Suppressive effects of sialic acid in the expression of biological activity of human erythropoietin in vitro. Eur J Biochem. 1990;194:457-62.
9. Fukuda MN, Sasaki H, Lopez L, Fukuda M. Survival of recombinant erythropoietin in the circulation: the role of carbohydrates. Blood. 1989;73:84-9.
10. Weigel PH, Yik JH. Glycans as endocytosis signals: the cases of the asialoglycoprotein and hyaluronan/chondroitin sulfate receptors. Biochim Biophys Acta. 2002;1572:341-63.
11. Genc S, Koroglu TF, Genc K. Erythropoietin and the nervous system. Brain Res. 2004;1000:19-31.
12. Satoh K, Kagaya Y, Nakano M, Ito Y, Ohta J, Tada H, et al. Important role of endogenous erythropoietin system in recruitment of endothelial progenitor cells in hypoxia-induced pulmonary hypertension in mice. Circulation. 2006;113:1442-50.
13. Nakano M, Satoh K, Fukumoto Y, Ito Y, Kagaya Y, Ishii N, et al. Important role of erythropoietin receptor to promote VEGF expression and angiogenesis in peripheral ischemia in mice. Circ Res. 2007;100:662-9.
14. Tada H, Kagaya Y, Takeda M, Ohta J, Asaumi Y, Satoh K, et al. Endogenous erythropoietin system in non-hematopoietic lineage cells plays a protective role in myocardial ischemia/reperfusion. Cardiovasc Res. 2006;71:466-77.
15. Hirata A, Minamino T, Asanuma H, Fujita M,Wakeno M, Myoishi M, et al. Erythropoietin enhances neovascularization of ischemic myocardium and improves left ventricular dysfunction after myocardial infarction in dogs. J Am Coll Cardiol. 2006;48:176-84.
16. Erbayraktar S, Grasso G, Sfacteria A, Xie QW, Coleman T, Kreilgaard M, et al. Asialoerythropoietin is a nonerythropoietic cytokine with broad neuroprotective activity in vivo. Proc Natl Acad Sci USA. 2003;100:6741-6.
17. Ogino A, Takemura G, Kawasaki M, Tsujimoto A, Kanamori H, Li L, et al. Erythropoietin receptor signaling mitigates renal dysfunction-associated heart failure by mechanisms unrelated to relief of anemia. J Am Coll Cardiol. 2010;56:1949-58.
18. Shintani S, Murohara T, Ikeda H, Ueno T, Sasaki K, Duan J, et al. Augmentation of postnatal neovascularization with autologous bone marrow transplantation. Circulation. 2001;103:897-903.
19. Nordenman B, Nyström C, Björk I. The size and shape of human and bovine antithrombin III. Eur J Biochem. 1977;78:195-203.
20. Fraser JR, Laurent TC, Laurent UB. Hyaluronan: its nature, distribution, functions and turnover. J Intern Med. 1997;242:27-33.
21. Schraufstatter I, Serobyan N, DiScipio R, Feofanova N, Orlovskaya I, Khaldoyanidi SK. Hyaluronan stimulates mobilization of mature hematopoietic cells but not hematopoietic progenitors. J Stem Cells. 2009;4:191-202.
22. Risau W. Mechanism of angiogenesis. Nature. 1997;386:671-4.
23. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science. 1997;275:964-7.
24. Crosby JR, Kaminski WE, Schatteman G, Martin PJ, Raines EW, Seifert RA, et al. Endothelial cells of hematopoietic origin make a significant contribution to adult blood vessel formation. Circ Res. 2000;87:728-30.
25. Heeschen C, Aicher A, Lehmann R, Fichtlscherer S, VasaM, Urbich C, et al. Erythropoietin is a potent physiologic stimulus for endothelial progenitor cell mobilization. Blood. 2003;102:1340-6.
26. Joshi D, Tsui J, Ho TK, Selvakumar S, Abraham DJ, Baker DM. Review of the role of erythropoietin in critical leg ischemia. Angiology. 2010;61:541-50.
27. Ueda K, Takano H, Niitsuma Y, Hasegawa H, Uchiyama R, Oka T, et al. Sonic hedgehog is a critical mediator of erythropoietin-induced cardiac protection in mice. J Clin Invest. 2010;120:2016-29.
28. Chong ZZ, Kang JQ, Maiese K. Erythropoietin is a novel vascular protectant through activation of Akt1 and mitochondrial modulation of cysteine proteases. Circulation. 2002;106:2973-9.
29. Baker JE, Kozik D, Hsu AK, Fu X, Tweddell JS, Gross GJ. Darbepoetin alfa protects the rat heart against infarction: dose- response, phase of action, and mechanisms. J Cardiovasc Pharmacol. 2007;49:337-45.
30. Kanellakis P, Pomilio G, Agrotis A, Gao X, Du XJ, Curtis D, et al. Darbepoetin-mediated cardioprotection after myocardial infarction involves multiple mechanisms independent of erythropoietin receptor-common beta-chain heteroreceptor. Br J Pharmacol. 2010;160:2085-96.
31. Kronman C, Chitlaru T, Elhanany E, Velan B, Shafferman A. Hierarchy of post-Translational modifications involved in the circulatory longevity of glycoproteins. Demonstration of concerted contributions of glycan sialylation and subunit assembly to the pharmacokinetic behavior of bovine acetylcholinesterase. J Biol Chem. 2000;275:29488-502.
32. Kolb-Bachofen V, Schlepper-Schäfer J, Vogell W, Kolb H. Electron microscopic evidence for an asialoglycoprotein receptor on Kupffer cells: localization of lectin-mediated endocytosis. Cell. 1982;29:859-66.
33. Erbayraktar S, Yilmaz O, Gökmen N, Brines M. Erythropoietin is a multifunctional tissue-protective cytokine. Curr Hematol Rep. 2003;2:465-70.
34. Parsa CJ, Matsumoto A, Kim J, Riel RU, Pascal LS,Walton GB, et al. A novel protective effect of erythropoietin in the infarcted heart. J Clin Invest. 2003;112:999-1007.
35. Ozawa T, Toba K, Suzuki H, Kato K, Iso Y, Akutsu Y, et al. Single-dose intravenous administration of recombinant human erythropoietin is a promising treatment for patients with acute myocardial infarction - randomized controlled pilot trial of EPO/ AMI-1 study -. Circ J. 2010;74:1415-23.
36. Taniguchi N, Nakamura T, Sawada T, Matsubara K, Furukawa K, Hadase M, et al. Erythropoietin prevention trial of coronary restenosis and cardiac remodeling after ST-elevated acute myocardial infarction (EPOC-AMI): A pilot, randomized, placebocontrolled study. Circ J. 2010;74:2365-71.
37. Yoshimura N, Toba K, Ozawa T, Aizawa Y, Hosoya T. A novel program to accurately quantify infarction volume by (99 m)Tc MIBI SPECT, and its application for re-analyzing the effect of erythropoietin administration in patients with acute myocardial infarction. Circ J. 2010;74:2741-3.
38. Streja E, Kovesdy CP, Greenland S, Kopple JD, McAllister CJ, Nissenson AR, et al. Erythropoietin, iron depletion, and relative thrombocytosis: A possible explanation for hemoglobin-survival paradox in hemodialysis. Am J Kidney Dis. 2008;52:727-36.
39. Vaziri ND. Thrombocytosis in EPO-Treated dialysis patients may be mediated by EPO rather than iron deficiency. Am J Kidney Dis. 2009;53:733-6.
40. Oda A, Miyakawa Y, Druker BJ, Ozaki K, Yabusaki K, Shirasawa Y, et al. Thrombopoietin primes human platelet aggregation induced by shear stress and by multiple agonists. Blood. 1996;87:4664-70.
41. Voors AA, Belonje AM, Zijlstra F, Hillege HL, Anker SD, Slart RH, et al. A single dose of erythropoietin in ST-elevation myocardial infarction. Eur Heart J. 2010;31:2593-600.
42. Ott I, Schulz S, Mehilli J, Fichtner S, Hadamitzky M, Hoppe K, 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. 2010;3:408-13.
43. Najjar SS, Rao SV, Melloni C, Raman SV, Povsic TJ, Melton L, et al. Intravenous erythropoietin in patients with ST-segment elevation myocardial infarction: REVEAL: A randomized controlled trial. JAMA. 2011;305:1863-72.
44. Okada T, Sawada T, Kubota K. Asialoerythropoietin has strong renoprotective effects against ischemia-reperfusion injury in a murine model. Transplantation. 2007;84:504-10.
45. Takeyama T, Takemura G, Kanamori H, Kawaguchi T, Ogino A, Watanabe T, et al. Asialoerythropoietin, a nonerythropoietic derivative of erythropoietin, displays broad anti-heart failure activity. Circ Heart Fail. 2012;5(2):274-85.