Intranasal formulation of erythropoietin (EPO) showed potent protective activity against amyloid toxicity in the Aβ25-35 non-transgenic mouse model of Alzheimer's disease

Journal of Psychopharmacology

Volumn 27, Issue 11, 2013, Pages 1044-1057

  Maurice, Tangui ^a,b   Mustafa, Muhammad Hariri ^a,b   Desrumaux, Catherine ^a,b   Keller, Emeline ^a,b,c   Naert, Gaëlle ^a,b   García Barceló, María De La C ^d   Rodríguez Cruz, Yamila ^d   Garcia Rodríguez, Julío César ^e  

^a University of Montpellier   (France)

^b PSL RESEARCH UNIVERSITY   (France)

^c AMYLGEN   (France)

^d Havana Medical Sciences University   (Cuba)

^e State Council   (Cuba)

Author keywords

Alzheimer's disease; Erythopoietin; intranasal formulation; learning and memory; neuroprotection

Indexed keywords

AMYLOID; AMYLOID BETA PROTEIN[25-35]; ERYTHROPOIETIN; INTERLEUKIN 1BETA; NEURO EPO; PROTEIN BAX; PROTEIN KINASE B; RECOMBINANT ERYTHROPOIETIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CELL LOSS; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG EFFICACY; DRUG FORMULATION; DRUG SAFETY; ENZYME ACTIVATION; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; LEARNING DISORDER; LIPID PEROXIDATION; LONG TERM MEMORY; MALE; MAZE TEST; MOUSE; MOUSE MODEL; MOUSE STRAIN; NEUROPROTECTION; NONHUMAN; PASSIVE AVOIDANCE; PRIORITY JOURNAL; SHORT TERM MEMORY; SPATIAL MEMORY;

ALZHEIMER'S DISEASE; ERYTHOPOIETIN; INTRANASAL FORMULATION; LEARNING AND MEMORY; NEUROPROTECTION;

ADMINISTRATION, INTRANASAL; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; CELL COUNT; CHEMISTRY, PHARMACEUTICAL; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ERYTHROPOIETIN; HIPPOCAMPUS; HUMANS; INTERLEUKIN-1BETA; LIPID PEROXIDATION; MALE; MAZE LEARNING; MICE; NEUROPROTECTIVE AGENTS; PEPTIDE FRAGMENTS; RECEPTORS, ERYTHROPOIETIN; RECOGNITION (PSYCHOLOGY); RECOMBINANT PROTEINS; RETENTION (PSYCHOLOGY); SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84885762681     PISSN: 02698811     EISSN: 14617285     Source Type: Journal    
DOI: 10.1177/0269881113494939     Document Type: Article

References (71)

1. Adamcio B, Sargin D, Stradomska A, et al. Erythropoietin enhances hippocampal long-term potentiation and memory. BMC Biol. 2008 ; 6: 37
2. Assaraf MI, Diaz Z, Liberman A, et al. Brain erythropoietin receptor expression in Alzheimer disease and mild cognitive impairment. J Neuropathol Exp Neurol. 2007 ; 66: 389-398
3. Bartesaghi S, Marinovich M, Corsini E, et al. Erythropoietin: A novel neuroprotective cytokine. Neurotoxicology. 2005 ; 26: 923-928
4. Bernaudin M, Marti HH, Roussel S, et al. A potential role for erythropoietin in focal permanent cerebral ischemia in mice. J Cereb Blood Flow Metab. 1999 ; 19: 643-651
5. Bhat RV, Shanley J, Correll MP, et al. Regulation and localization of tyrosine216 phosphorylation of glycogen synthase kinase-3β in cellular and animal models of neuronal degeneration. Proc Natl Acad Sci USA. 2000 ; 97: 11074-11079
6. Brines ML, Ghezzi P, Keenan S, et al. Erythropoietin crosses the blood-brain barrier to protect against experimental brain injury. Proc Natl Acad Sci USA. 2000 ; 97: 10526-10531
7. Brunet A, Bonni A, Zigmond MJ, et al. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell. 1999 ; 96: 857-868
8. Celik M, Gökmen N, Erbayraktar S, et al. Erythropoietin prevents motor neuron apoptosis and neurologic disability in experimental spinal cord ischemic injury. Proc Natl Acad Sci USA. 2002 ; 99: 2258-2263
9. Chavant F, Deguil J, Pain S, et al. Imipramine, in part through tumor necrosis factor α inhibition, prevents cognitive decline and β-amyloid accumulation in a mouse model of Alzheimer's disease. J Pharmacol Exp Ther. 2010 ; 332: 505-514
10. Cheng IH, Scearce-Levie K, Legleiter J, et al. Accelerating amyloid-β fibrillization reduces oligomer levels and functional deficits in Alzheimer disease mouse models. J Biol Chem. 2007 ; 282: 23818-23828
11. Chin K, Yu X, Beleslin-Cokic B, et al. Production and processing of erythropoietin receptor transcripts in brain. Brain Res Mol Brain Res. 2000 ; 81: 29-42
12. Chong ZZ, Kang JK, Maiese K. Apaf-1, Bcl-xL, cytochrome c, and caspase-9 Form the critical elements for cerebral vascular protection by erythropoietin. J Cereb Blood Flow Metab. 2003b ; 23: 320-330
13. Chong ZZ, Kang JK, Maiese K. Akt1 drives endothelial cell membrane asymmetry and microglial activation through Bcl-x(L) and caspase 1, 3, and 9. Exp Cell Res. 2004 ; 296: 196-207
14. Chong ZZ, Li F, Maiese K. Erythropoietin requires NF-κB and its nuclear translocation to prevent early and late apoptotic neuronal injury during β-amyloid toxicity. Curr Neurovasc Res. 2005 ; 2: 387-399
15. Chong ZZ, Lin SH, Kang JK, et al. Erythropoietin prevents early and late neuronal demise through modulation of Akt1 and induction of caspase 1, 3, and 8. J Neurosci Res. 2003a ; 71: 659-669
16. Craft S, Baker LD, Montine TJ, et al. Intranasal insulin therapy for Alzheimer disease and amnestic mild cognitive impairment: A pilot clinical trial. Arch Neurol. 2012 ; 69: 29-38
17. Delobette S, Privat A, Maurice T. In vitro aggregation facilities β-amyloid peptide- (25-35)-induced amnesia in the rat. Eur J Pharmacol. 1997 ; 319: 1-4
18. Digicaylioglu M, Bichet S, Marti HH, et al. Localization of specific erythropoietin binding-sites in defined areas of the mouse-brain. Proc Natl Acad Sci USA. 1995 ; 92: 3717-3720
19. Fletcher L, Kohli S, Sprague SM, et al. Intranasal delivery of erythropoietin plus insulin-like growth factor-I for acute neuroprotection in stroke. J Neurosurg. 2009 ; 111: 164-170
20. Garcia-Rodríguez JC, Rodríguez-Cruz Y. The therapeutic potential of Neuro-EPO administered nasally on acute cerebrovascular disease. Curr Psychopharmacol. 2012 ; 1: 228-232
21. Garcia-Rodríguez JC, Sosa-Testé I. The nasal route as a potential pathway for delivery of erythropoietin in the treatment of acute ischemic stroke in humans. Sci World J. 2009 ; 9: 970-981
22. Genc S, Zadeoglulari Z, Oner MG, et al. Intranasal erythropoietin therapy in nervous system disorders. Expert Opin Drug Deliv. 2011 ; 8: 19-32
23. Grunfeld JF, Barhum Y, Blondheim N, et al. Erythropoietin delays disease onset in an amyotrophic lateral sclerosis model. Exp Neurol. 2007 ; 204: 260-263
24. Hooper C, Killick R, Lovestone S. The GSK-3 hypothesis of Alzheimer's disease. J Neurochem. 2008 ; 104: 1433-1439
25. Hoynck van Papendrecht MA, Jeekel H, Busch OR, et al. Efficacy of recombinant erythropoietin for stimulating erythropoiesis after blood loss and surgery. An experimental study in rats. Eur J Surg. 1992 ; 158: 83-87
26. Hsiao K, Chapman P, Nilsen S, et al. Correlative memory deficits, Aβ elevation, and amyloid plaques in transgenic mice. Science. 1996 ; 274: 99-102
27. Juul SE, Yachnis AT, Christensen RD. Tissue distribution of erythropoietin and erythropoietin receptor in the developing human fetus. Early Hum Dev. 1998 ; 52: 235-249
28. Kamal A, Al Shaibani T, Ramakers G. Erythropoietin decreases the excitatory neurotransmitter release probability and enhances synaptic plasticity in mice hippocampal slices. Brain Res. 2011 ; 1410: 33-37
29. Kawakami M, Sekiguchi M, Sato K, et al. Erythropoietin receptor-mediated inhibition of exocytotic glutamate release confers neuroprotection during chemical ischemia. J Biol Chem ; 2001 ; 2001. 39469.
30. Klementiev B, Novikova T, Novitskaya V, et al. A neural cell adhesion molecule-derived peptide reduces neuropathological signs and cognitive impairment induced by Aβ25-35. Neuroscience. 2007 ; 145: 209-224
31. Klyubin I, Walsh DM, Lemere CA, et al. Amyloid-β protein immunotherapy neutralizes Aβ oligomers that disrupt synaptic plasticity in vivo. Nat Med. 2005 ; 11: 556-561
32. Kosik KS. Cellular aspects of Alzheimer neurofibrillary pathology. Prog Clin Biol Res. 1992 ; 379: 183-193
33. Kumral A, Uysal N, Tugyan K, et al. Erythropoietin improves long-term spatial memory deficits and brain injury following neonatal hypoxia-ischemia in rats. Behav Brain Res. 2004 ; 153: 77-86
34. Lee ST, Chu K, Park JE, et al. Erythropoietin improves memory function with reducing endothelial dysfunction and amyloid-β burden in Alzheimer's disease models. J Neurochem. 2012 ; 120: 115-124
35. Lee ST, Chu K, Sinn DI, et al. Erythropoietin reduces perihematomal inflammation and cell death with eNOS and STAT3 activations in experimental intracerebral hemorrhage. J Neurochem. 2006 ; 96: 1728-1739
36. Li G, Ma R, Huang C, et al. Protective effect of erythropoietin on β-amyloid-induced PC12 cell death through antioxidant mechanisms. Neurosci Lett. 2008 ; 442: 143-147
37. Li W, Maeda Y, Yuan RR, et al. Beneficial effect of erythropoietin on experimental allergic encephalomyelitis. Ann Neurol. 2004 ; 56: 767-777
38. Lue LF, Kuo YM, Roher AE, et al. Soluble amyloid β peptide concentration as a predictor of synaptic change in Alzheimer's disease. Amer J Pathol. 1999 ; 155: 853-862
39. Ma R, Xiong N, Huang C, et al. Erythropoietin protects PC12 cells from β-amyloid25-35-induced apoptosis via PI3K/Akt signaling pathway. Neuropharmacology. 2009 ; 56: 1027-1034
40. Maiese K, Chong ZZ, Li F, et al. Erythropoietin: Elucidating new cellular targets that broaden therapeutic strategies. Prog Neurobiol. 2008 ; 85: 194-213
41. Maiese K, Li F, Chong ZZ. Erythropoietin in the brain: can the promise to protect be fulfilled?. Trends Pharmacol Sci. 2004 ; 25: 577-583
42. Majumdar A, Cruz D, Asamoah N, et al. Activation of microglia acidifies lysosomes and leads to degradation of Alzheimer amyloid fibrils. Mol Biol Cell. 2007 ; 18: 1490-1496
43. Martín D, Salinas M, López-Valdaliso R, et al. Effect of the Alzheimer amyloid fragment Aβ25-35 on Akt/PKB kinase and survival of PC12 cells. J Neurochem. 2001 ; 78: 1000-1008
44. Mattson MP. Pathways towards and away from Alzheimer's disease. Nature. 2004 ; 430: 631-639
45. Maurice T, Lockhart BP, Privat A. Amnesia induced in mice by centrally administered β-amyloid peptides involves cholinergic dysfunction. Brain Res. 1996 ; 706: 181-193
46. McLean CA, Cherny RA, Fraser FW, et al. Soluble pool of Aβ amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease. Ann Neurol. 1999 ; 46: 860-866
47. Meunier J, Ieni J, Maurice T. The anti-amnesic and neuroprotective effects of donepezil against amyloid β25-35 peptide-induced toxicity in mice involve an interaction with the σ1 receptor. Br J Pharmacol. 2006 ; 149: 998-1012
48. Mitrasinovic OM, Murphy GM. Microglial overexpression of the M-CSF receptor augments phagocytosis of opsonized Abeta. Neurobiol Aging. 2003 ; 24: 807-815
49. Mitrasinovic OM, Vincent VA, Simsek D, et al. Macrophage colony stimulating factor promotes phagocytosis by murine microglia. Neurosci Lett. 2003 ; 344: 185-188
50. Morishita E, Masuda S, Nagao M, et al. Erythropoietin receptor is expressed in rat hippocampal and cerebral cortical neurons, and erythropoietin prevents in vitro glutamate-induced neuronal death. Neuroscience. 1997 ; 76: 105-116
51. Nadam J, Navarro F, Sanchez P, et al. Neuroprotective effects of erythropoietin in the rat hippocampus after pilocarpine-induced status epilepticus. Neurobiol Dis. 2007 ; 25: 412-426
52. Naert G, Rivest S. The role of microglial cell subsets in Alzheimer's disease. Curr Alzheimer Res. 2011 ; 8: 151-155
53. Nagai A, Nakagawa E, Choi HB, et al. Erythropoietin and erythropoietin receptors in human CNS neurons, astrocytes, microglia, and oligodendrocytes grown in culture. J Neuropathol Exp Neurol. 2001 ; 60: 386-392
54. Paradis E, Douillard H, Koutroumanis M, et al. Amyloid β peptide of Alzheimer's disease downregulates Bcl-2 and upregulates bax expression in human neurons. J Neurosci. 1996 ; 16: 7533-7539
55. Paxinos G, Franklin KBJ San Diego, USA: Elsevier Academic Press ; 2004 :
56. Rabie T, Marti HH. Brain protection by erythropoietin: a manifold task. Physiology (Bethesda). 2008 ; 23: 263-274
57. Rodríguez Cruz Y, Mengana Támos Y, Muñoz Cernuda A, et al. Treatment with nasal neuro-EPO improves the neurological, cognitive, and histological state in a gerbil model of focal ischemia. Sci World J. 2010 ; 10: 2288-2300
58. Sakanaka M, Wen TC, Matsuda S, et al. In vivo evidence that erythropoietin protects neurons from ischemic damage. Proc Natl Acad Sci USA. 1998 ; 95: 4635-4640
59. Sanchez PE, Fares RP, Risso JJ, et al. Optimal neuroprotection by erythropoietin requires elevated expression of its receptor in neurons. Proc Natl Acad Sci USA. 2009 ; 106: 9848-9853
60. Scopes DIC, O'Hare E, Jeggo R, et al. Aβ oligomer toxicity inhibitor protects memory in models of synaptic toxicity. Br J Pharmacol. 2012 ; 167: 383-392
61. Selkoe DJ. Alzheimer's disease: Genes, proteins, and therapy. Physiol Rev. 2001 ; 81: 741-766
62. Somervaille TC, Linch DC, Khwaja A. Growth factor withdrawal from primary human erythroid progenitors induces apoptosis through a pathway involving glycogen synthase kinase-3 and Bax. Blood. 2001 ; 98: 1374-1381
63. Sosa Testé I, García Rodríguez JC, García Salman JD, et al. Intranasal administration of recombinant human erythropoietin exerts neuroprotective effects on post-ischemic brain injury in mongolian gerbils. Pharmacol Online. 2006 ; 1: 100-112
64. Stepanichev MY, Moiseeva YV, Lazareva NA, et al. Single intracerebroventricular administration of amyloid-β25-35 peptide induces impairment in short-term rather than long-term memory in rats. Brain Res Bull. 2003 ; 61: 197-205
65. Stepanichev MY, Zdobnova IM, Zarubenko II, et al. Amyloid-β25-35- induced memory impairments correlate with cell loss in rat hippocampus. Physiol Behav. 2004 ; 80: 647-655
66. Stepanichev MY, Zdobnova IM, Zarubenko II, et al. Studies of the effects of central administration of β-amyloid peptide (25-35): Pathomorphological changes in the hippocampus and impairment of spatial memory. Neurosci Behav Physiol. 2006 ; 36: 101-106
67. Villard V, Espallergues J, Keller E, et al. Antiamnesic and neuroprotective effects of the aminotetrahydrofuran derivative ANAVEX1-41 against amyloid β25-35-induced toxicity in mice. Neuropsychopharmacology. 2009 ; 34: 1552-1566
68. Villard V, Espallergues J, Keller E, et al. Anti-amnesic and neuroprotective potentials of the mixed muscarinic receptor/sigma1 (σ1) ligand ANAVEX2-73, a novel aminotetrahydrofuran derivative. J Psychopharmacol. 2011 ; 25: 1101-1117
69. Walsh DM, Selkoe DJ. Aβ oligomers - a decade of discovery. J Neurochem. 2007 ; 101: 1172-1184
70. Wenger RH. Mammalian oxygen sensing, signalling and gene regulation. J Exp Biol. 2000 ; 203: 1253-1263
71. Zussy C, Brureau A, Delair B, et al. Time-course and regional analyses of the physiopathological changes induced after cerebral injection of an amyloid β fragment in rats. Am J Pathol. 2011 ; 179: 315-334