The neuroprotective and neurorescue effects of carbamylated erythropoietin Fc fusion protein (CEPO-Fc) in a rat model of Parkinson's disease

Brain Research

Volumn 1502, Issue , 2013, Pages 55-70

  Thomas Tayra, Judith ^a   Kameda, Masahiro ^a   Yasuhara, Takao ^a   Agari, Takashi ^a   Kadota, Tomohito ^a   Wang, Feifei ^a   Kikuchi, Yoichiro ^a   Liang, Hanbai ^a   Shinko, Aiko ^a   Wakamori, Takaaki ^a   Vcelar, Brigitta ^b   Weik, Robert ^b   Date, Isao ^a  

^a OKAYAMA UNIVERSITY   (Japan)

^b POLYMUN SCIENTIFIC IMMUNBIOLOGISCHE FORSCHUNG GMBH   (Austria)

Author keywords

Carbamylated erythropoietin; Dopamine; Neuroprotection; Neurorescue; Parkinson's disease

Indexed keywords

AMPHETAMINE; CARBAMYLATED ERYTHROPOIETIN FC FUSION PROTEIN; HYBRID PROTEIN; RECOMBINANT ERYTHROPOIETIN; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; DISEASE COURSE; FEMALE; FOLLOW UP; HEMATOCRIT; HEMOGLOBIN BLOOD LEVEL; HISTOPATHOLOGY; NERVE FIBER; NEUROPROTECTION; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; RAT; ROTATION; SUBSTANTIA NIGRA;

ADRENERGIC AGENTS; AMPHETAMINE; ANALYSIS OF VARIANCE; ANIMALS; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; DRUG ADMINISTRATION SCHEDULE; ERYTHROPOIETIN; FEMALE; HEMATOCRIT; HEMOGLOBINS; NEUROPROTECTIVE AGENTS; OXIDOPAMINE; PARKINSON DISEASE; PSYCHOMOTOR PERFORMANCE; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT PROTEINS; ROTAROD PERFORMANCE TEST; STEREOTYPED BEHAVIOR; SUBSTANTIA NIGRA; TIME FACTORS; TYROSINE 3-MONOOXYGENASE;

RATTUS;

EID: 84875453515     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2013.01.042     Document Type: Article

References (77)

1. C. Adembri, A. Massagrande, A. Tani, M. Miranda, M. Margheri, R. DeGaudio, and D.E. Pellegrini-Giampietro Carbamylated erythropoietin is neuroprotective in an experimental model of traumatic brain injury Crit. Care Med. 36 2008 975 978
2. S. Ahn, and A.L. Joyner In vivo analysis of quiescent adult neural stem cells responding to Sonic hedgehog Nature 437 2005 894 897
3. Y. Aluf, J. Vaya, S. Khatib, Y. Loboda, S. Kizhner, and J.P. Finberg Specific oxidative stress profile associated with partial striatal dopaminergic depletion by 6-hydroxydopamine as assessed by a novel multifunctional marker molecule Free Radical Res. 44 2010 635 644
4. N.M. Amankulor, D. Hambardzymyan, S.M. Pyonteck, O.J. Becher, J.A. Joyce, and E.C. Holland Sonic hedgehog pathway activation is induced by acute brain injury and regulated by injury related inflammation J. Neurosci. 29 33 2009 10299 10380
5. P. Andre, D. Hartwell, and I. Hrachovinova Pro-coagulant state resulting from high levels of soluble P-selectin in blood Proc. Nat. Acad. Sci. U.S.A. 97 2000 13835 13840
6. D. Bar-Or, and G. Thomas Beneficial effects of carbamylated erythropoietin on trauma-induced brain edema: proposed mechanisms of action Crit. Care Med. 39 9 2011 2191
7. P. Bath, C. Algert, and N. Chapman Association of mega platelet volume with risk of stroke among individuals with history of cerebrovascular disease Stroke 35 2004 622 626
8. A.D. Blann, E.B. Faragher, and C.N. McCollum Increased soluble P-selectin following myocardial infarction: a new marker for the progression of atherosclerosis Blood Coagul. Fibrinolysis 8 1997 383 390
9. G. Beck, G.S. Habich, and J.L. Benach Interleukin I: a common endogenous mediator of inflammation and the local Shwartzman reaction J. Immunol. 136 1986 3025 3031
10. P. Bouzat, S. Francony, and S. Thomas Reduced brain edema and functional deficits after treatment of diffuse traumatic brain injury by carbamylated erythropoietin derivative Crit. Care Med. 39 2011 2099 2105
11. M. Brines, and A. Cerami Emerging biological roles for erythropoietin in the nervous system Nat. Rev. Neurosci. 6 2005 484 494
12. M.L. Brines, P. Ghezzi, and S. Keenan Erythropoietin crosses the blood brain barrier to protect against experimental brain injury Proc. Nat. Acad. Sci. U.S.A. 97 2000 10526 10531
13. M.L. Brines, G. Grasso, F. Fiordaliso, A. Sfacteria, P. Ghezzi, M. Fretelli, R. Latini, Q.W. Xie, J. Smart, C.J. Su-Rick, E. Pbre, D. Diaz, D. Gomez, C. Hand, T. Coleman, and A. Cerami Erythropoietin mediates tissue protection through an erythropoietin and common beta subunit receptor Proc. Nat. Acad. Sci. U.S.A. 1 2004 14907 14912
14. D.J. Capon, S.M. Chamow, J. Mordenti, S.A. Marsters, T. Gregory, H. Mitsuya, R.A. Byrn, C. Lucas, F.M. Wurm, J.E. Groopman, S. Broder, and D.H. Smith Designing CD4 immunoadhesins for AIDS therapy Nature 337 1989 525 531
15. A. Cerami The value of failure: the discovery of TNF and its natural inhibitor erythropoietin J Inter Med. 269 2011 8 15
16. A. Cerami, M.L. Brines, P. Ghezzi, and C.J. Cerami Effects of epoetin-alfa on the central nervous system Semin. Oncol. 28 2 Suppl. 8 2001 66 70
17. T.R. Coleman, C. Westenfelder, F.E. Togel, Y. Yang, and Z. Hu Cytoprotective doses of erythropoietin or carbamy-lated erythropoietin have markedly different pro-coagulant and vasoactive activities Proc. Nat. Acad. Sci. U.S.A. 103 2006 5965 5970
18. Z. Diaz, M.I. Assaraf, W.H. Miller, and H.M. Schipper Astroglial cytoprotection by erythropoietin pre-conditioning: implication for ischemic and degenerative CNS disorders J. Neurochem. 93 2005 392 402
19. H. Ehrenreich Medicine. A boost for translational neuroscience Science 305 2004 184 185
20. H. Ehrenreich, D. Degner, and J. Meller Erythropoietin: a candidate compound for neuroprotection in schizophrenia Mol. Psychiatry 9 2004 42 54
21. H. Ehrenreich, M. Hasselblatt, C. Dembowski, L. Cepek, P. Lewczuk, and M. Stiefel Erythropoietin therapy for acute stroke is both safe and beneficial Mol. Med. 8 2002 495 505
22. H. Ehrenreich, M. Hasselblatt, F. Knerlich, N. von Ahsen, S. Jacob, S. Sperling, H. Woldt, K. Vehmeyer, K.A. Nave, and A.L. Siren A hematopoietic growth factor, thrombopoietin, has a proapoptotic role in the brain Proc. Nat. Acad. Sci. U.S.A. 102 2005 862 867
23. H. Ehrenreich, K. Weissenborn, H. Prange, D. Schneider, C. Weimar, and K. Wartenberg Recombinant human erythropoeitin in the treatment of acute ischemic stroke Stroke 40 2009 e647 e656
24. S. Ebayraktar, N. Lanerolle, A. Lotbiniere, J.P. Knisely, Z. Erbayraktar, O. Yilmarz, A. Cerami, T.R. Coleman, and M. Brines Carbamylated erythropoietin reduces radiosurgically induced brain Injury Mol. Med. 12 2006 74 80
25. Z. Erbayraktar, S. Erbayraktar, O. Yilmaz, A. Cerami, T. Coleman, and A. Brines Nonerythropoietic tissue protective compounds are highly effective facilitators of wound healing Mol. Med. 15 2009 235 241
26. J.M. Fearnley, and A.J. Lees Ageing and Parkinson's disease: substantia nigra rational selectivity Brain 114 Pt. 5 1991 2283 2301
27. L. Ferruci, J.M. Guralnik, S. Bandinelli, R.D. Semba, F. Lauretani, A. Corsi, C. Ruggiero, W.B. Ershter, and D.L. Longo Unexplained anaemia in older persons is characterized by low erythrpoietin and low levels of pro-inflammatory markers Brit. J. Hemat. 136 2007 549 555
28. Z.Q. Fu, Q.L. Shao, J.L. Shen, Y.J. Zhang, X.X. Zhao, and L. Yao Effect of carbamylated erythropoietin on major histocompatibility complex expression and neural differentiation of human neural stem cells J. Neuroimmunol. 21 2010 15 24
29. S. Greisenegger, G. Endler, and K. Sheh Is elevated mean platelet volume associated with a worse outcome in patients with acute ischemic cerebrovascular events? Stroke 35 2004 1688 1691
30. M. Hashimoto, K. Ishii, Y. Nakamura, K. Watabe, S. Kohsaka, and C. Akazawa Neuroprotective effect of sonic hedgehog up-regulated in Schwann cells following sciatic nerve injury J. Neurochem. 107 2008 918 927
31. T Hirano Interleukin-6 and its relation to inflammation and disease Clin. Immunol. Immunopathol. 62 1 Pt. 2 1992 S60 S65
32. M. Hasselblat, H. Ehrenreich, and A.L. Siren The brain erythropoietin system and its potential for therapeutic exploitation in brain disease J. Neurosurg. Anesthesiol. 18 2 2006 132 138
33. O. Hornykiewicz Neurochemical pathology and the etiology of Parkinson's disease: basic facts and hypothetical possibilities Mt. Sinai J. Med. 55 1988 11 20
34. G.S. Huh, L.M. Boulanger, H. Du, P.A. Riquelme, T.M. Brotz, and C.J. Shatz Functional requirement for class I MHC in CNS development and plasticity Science 290 2000 2155 2159
35. P.T. Jubinsky, O.I. Krijanovski, D.G. Nathan, J. Tavernier, and C.A. Stieff The beta chain of the interleukin-3 receptor functionally associates with the erythropoietin receptor Blood 90 1997 1867 1873
36. T. Kadota, T. Shingo, T. Yasuhara, N. Tajiri, A. Kondo, T. Morimoto, W.J. Yuan, F. Wang, T. Baba, K. Tokunaga, Y. Miyoushi, and I. Date Continuous intraventricular infusion of erythropoietin exerts neuroprotective/rescue effects upon Parkinson's disease model of rats with enhanced neurogenesis Brain Res. 1254 2009 120 127
37. J. Kennedy, and A.M. Buchan C-EPO: ready for prime time preconditioning Cerebrovasc. Dis. 19 2005 272 273
38. Y. Kikuchi, T. Yasuhara, T. Agari, A. Kondo, S. Kuramoto, M. Kameda, and T. Kadota Urinary 8-OHdG elevations in a partial lesion rat model of Parkinson's disease correlate with behavioral symptoms and nigrostriatal dopaminergic depletion J. Cell. Physiol. 226 2011 1390 1398
39. A. Kirkeby, L. Torup, L. Bochsen, M. Kjalke, and K. Abel High dose erythropoietin alters platelet reactivity and bleeding time in rodents in contrast to the neuroprotective variant carbamyl-erythropoietin (CEPO) Thromb. Haemost. 99 2008 720 728
40. C. Leconte, E. Bihel, F.X. Lepelletier, V. Bouet, R. Saulnier, E. Petit, M. Boulouard, M. Bernaudin, and P. Schumann-Bard Comparison of the effects of erythropoietin and its carbamylated derivative on behaviour and hippocampal neurogenesis in mice Neuropharmacology 60 2011 354 364
41. S.M. Lee, T.H. Nguyen, and M.H. Park EPO receptor mediated ERK Kinase and NF-kappa B activation in erythropoietin promoted differentiation of astrocytes Biochem. Biophys. Res. Commun. 320 2004 1087 1095
42. M. Leist Derivatives of erythropoietin that are tissue protective but not erythropoietic Science 305 2004 239 242
43. G.Y. Lip, A.D. Blann, and I.S. Farooqi Sequential alterations in haemorheology, endothelial dynsfunction, platelet activation and thrombogenesis in relation to prognosis following acute stroke: the West Birmingham Stroke Project Blood Coagul. Fibrinolysis 13 2002 339 347
44. J. Liu, P. Narasimhan, F. Yu, and P.H. Chan Neuroprotection by hypoxic preconditioning involves oxidative stress mediated expression of hypoxia-inducible factor and erythropoietin Stroke 36 2005 1264 1269
45. W. Liu, Y. Shen, J.M. Plane, D.E. Pleasure, and W. Deng Neuroprotective potential of erythropoietin and its derivative carbamylated erythropoietin in periventricular leukomalacia. Exp. Neurol. 230 2011 227 239
46. A. Mahmood, D. Lu, C. Qu, A. Goussev, Z.G. Zhang, and C. Lu Treatment of traumatic brain injury in rats with erythropoietin and carbamylated erythropoietin J. Neurosurg. 107 2007 392 397
47. J.F. Martin, P.M. Bath, and M.L. Burr Influence of platelet size on outcome after myocardial infarction Lancet 338 1991 1409 1411
48. M. Motero, F.R. Poulsen, J. Noraberg, and A. Kirkeby Comparison of neuroprotective effects of erythropoietin (EPO) and carbamylerythropoeitin (CEPO) against ischemia-like-oxygen-glucose-deprivation (OGD) and NMDA excitotoxicity in mouse hippocampal slice cultures Exp. Neurol. 204 2007 106 117
49. W.N. Nijboer, P.J. Ottens, A. Dijk, H. Goor, R.J. Ploeg, and H.G.D. Leuvenink Donor pretreatment with carbamylated erythropoietin in a brain death model reduces inflammation more effectively than erythropoietin while preserving renal function Crit. Care Med. 38 2010 1155 1161
50. O.O. Ogunshola, V. Djonov, R. Staudt, J. Vogel, and M. Gassmann Chronic excessive erythrocytosis induces endothelial activation and damage in mouse brain Am. J. Physiol-Reg. I. 290 2006 R678 684
51. A.L. Oliveira, S. Thams, O. Lidman, F. Piehl, T. Hokfelt, K. Karre, H. Linda, and S. Cullheim A role for MHC class I molecules in synaptic plasticity and regeneration of neurons after axotomy Proc. Nat. Acad. Sci. U.S.A. 101 2004 17843 17848
52. G. Paxinos, and G. Watson The Rat Brain in Stereotaxic Coordinates 1998 Academic Press San Diego
53. N. Piloto, H.M. Teixeira, E.T. Lemos, and B. Parada Erythropoietin promotes deleterious cardiovascular effects and mortality risk in a rat model of chronic sports doping Cardiovasc. Toxicol. 9 2009 201 210
54. M. Sakanaka, T.C. Wen, S. Masuda, E. Morishita, and M. Nagao In vivo evidence that erythropoietin protects neurons from ischemic damage Proc. Nat. Acad. Sci. U.S.A. 95 1998 4635 4640
55. R. Sasaki Pleiotropic functions of erythropoietin Int. Med. 42 2003 142 149
56. T. Schallert, S.M. Fleming, J.L. Leasure, J.L. Tillerson, and S.T. Bland CNS plasticity and assessment of forelimb sensorimotor outcome in unilateral rat models of stroke, cortical ablation, parkinsonism and spinal cord injury Neuropharmacology 9 2000 777 787
57. R.E. Schmidt, K.G. Green, D. Feng, D.A. Dorsey, C.A. Parvin, J.M. Lee, Q. Xiao, and M. Brines Erythropoietin and its carbamylated derivative prevent the development of experimental diabetic autonomic neuropathy in STZ-induced diabetic NOD-SCID mice Exp. Neurol. 209 2008 161 170
58. K. Schriebl, E. Trummer, C. Lattenmayer, R. Weik, R. Kunert, D. Muller, H. Katinger, and U.K. Vorauer Biochemical characterization of rhEPO-Fc fusion protein expressed in CHO cells Protein Expression Purif. 49 2006 265 275
59. K.D. Sethi Clinical aspects of Parkinson disease Curr. Opin. Neurobiol. 15 2002 457 460
60. T. Shingo, S.T. Sorokan, and T. Shimasaki Erythropoietin regulates the in vitro and in vivo production of neuronal progenitors by mammalian forebrain neural stem cells J. Neurosci. 21 2001 9733 9743
61. M. Sifringer, D. Brait, U. Weichelt, G. Zimmerman, S. Endesfelder, F. Brehmer, C. von Haefen, A. Friedman, H. Soreq, I. Bendix, B. Gerstner, and U. Felderhoff-Mueser Erythropoietin attenuates hyperoxia-induced oxidative stress in the developing rat brain Brain Behav. Immun. 24 2010 792 799
62. A.L. Siren, T. Fasshauer, C. Bartels, and H. Ehrenreich Therapeutic potential of erythropoietin and its structural or functional variants in the nervous system Neurotherapeutics 6 2009 108 127
63. Sturm, B., Helminger, M., Steinkellner, H., Heidari, M.M., Goldenberg, H., Scheiber-Mojdehkar, B., 2010. Carbamylated erythropoietin increases frataxin independent from the erythropoietin receptor. Eur. J. Clin. Invest. 40, 561-565.
64. M. Sugawa, Y. Sakurai, and Y. Ishikawa Effects of erythropoietin on glial cell development; oligodendrocyte maturation and astrocyte proliferation Neurosci. Res. 44 2002 391 403
65. K. Takahashi, T. Yasuhara, T. Shingo, K. Muraoka, M. Kameda, A. Takeuchi, A. Yano, K. Kurozumi, T. Agari, Y. Miyoshi, K. Kinugasa, and I. Date Embryonic neural stem cells transplanted in middle cerebral artery occlusion model of rats demonstrated potent therapeutic effects, compared to adult neural stem cells Brain Res. 1234 2008 172 182
66. O. Verdonk, H. Lahrech, and G. Francony Erythropoietin protects from post-traumatic edema in the rat brain J. Cereb. Blood Flow Metab. 27 2007 1369 1376
67. L. Wang, ZG. Zhang, S.R. Gregg, R.L. Zhang, Z. Jiao, Y. Letourneau, W. Liu, Y. Feng, J. Gerwien, L. Torup, M. Leist, C.T. Noguchi, Z.Y. Chen, and M. Chopp The Sonic hedgehog pathway mediates carbamylated erytrhopoietin-enhanced proliferation and differentiation of adult neural progenitor cells J. Biol. Chem. 282 2007 32462 32470
68. L. Wang, Z. Zhang, Y. Wang, R. Zhang, and M. Chopp Treatment of stroke with erythropoietin enhances neurogenesis and angiogenesis and improves neurological function in rats Stroke 35 2004 1732 1737
69. L. Wang, Z. Zhang, and R. Zhang Erythropoietin up regulates SOCS 2 in neuronal progenitor cells derived from SVZ of adult rat Neuroreport 15 2004 1225 1229
70. L. Wei, B.H. Han, L. Ying, C.L. Keogh, D.M. Hotzman, and S.P. Yu Cell death mechanism and protective effect of erythropoietin after focal ischemia in the whisker-barrel cortex of neonatal rats J. Pharmacol. Exp. Ther. 317 2006 109 116
71. C.L. Wu, S.D. Chen, J.H. Yin, C.S. Hwang, and D.I. Yang Erythropoeitin and sonic hedgehog mediate the neuroprotective effects of brain derived neurotrophic factor against mitochondrial inhibition Neurobiol. Dis. 40 2010 146 154
72. Y.X. Xiong, A. Mahmood, Y. Zhang, Y. Meng, Z.G. Zhang, C. Qu, T. Sager, and M. Chopp Effects of posttraumatic carbamylated erythropoietin therapy on reducing lesion volume and hippocampal cell loss, enhancing angiogenesis and neurogenesis, and improving functional outcome in rats following traumatic brain injury J. Neurosurg. 114 2011 549 559
73. T. Yasuhara, C.V. Borlongan, and I. Date Ex vivo gene therapy: transplantation of neurotrophic factor-secreting cells for cerebral ischemia Front. Biosci. 11 2006 760 775
74. S.W. Yu, H. Wang, and M.F. Poitras Medication of poly(ADP-ribose) polymerase-1 dependent cell death by apoptosis-inducing factor Science 297 2002 259 263
75. W.J. Yuan, T. Yasuhara, T. Shingo, K. Muraoka, T. Agari, M. Kameda, T. Uozumi, N. Tajiri, and T. Morimoto Neuroprotective effects of edaravone-administration on 6-OHDA treated dopaminergic neurons BMC Neurosci. 9 2008 75
76. F. Zhang, A.P. Signore, Z. Zhou, S. Wang, G. Cao, and J. Chen Erythropoietin protects CA1 neurons against global cerebral ischemia in rat: potential signalling mechanisms J. Neurosci. Res. 83 2006 1241 1251
77. Q.H. Zhou, E.K. Hui, J.Z. Lu, R.J Boado, and W.M. Pardridge Brain penetrating IgG-erythropoietin fusion protein is neuroprotective following intravenous treatment in Parkinson's disease in the mouse Brain Res. 1382 2011 315 320