Erythropoietin improves neurobehavior by reducing dopaminergic neuron loss in a 6-hydroxydopamine-induced rat model

International Journal of Molecular Medicine

Volumn 34, Issue 2, 2014, Pages 440-450

  Qi, Chen ^a   Xu, Mingxin ^b   Gan, Jing ^a   Yang, Xinxin ^a   Wu, Na ^a   Song, Lu ^a   Yuan, Weien ^a,b   Liu, Zhenguo ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b SHANGHAI JIAO TONG UNIVERSITY   (China)

Author keywords

Erythropoietin; Mitogen activated protein kinases; Parkinson's disease; Tyrosine hydroxylase

Indexed keywords

CASPASE 3; ERYTHROPOIETIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; OXIDOPAMINE; SODIUM CHLORIDE; STRESS ACTIVATED PROTEIN KINASE; TYROSINE 3 MONOOXYGENASE; DOPAMINE DERIVATIVE; MITOGEN ACTIVATED PROTEIN KINASE KINASE; NEUROPROTECTIVE AGENT;

ADULT; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CIRCLING BEHAVIOR; COGNITION; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DRUG CEREBROSPINAL FLUID LEVEL; DRUG EFFICACY; DRUG MEGADOSE; ENZYME ACTIVATION; ENZYME LINKED IMMUNOSORBENT ASSAY; EXPERIMENTAL PARKINSONISM; FEMALE; IMMUNOCOMPETENT CELL; IMMUNOCYTOCHEMISTRY; MEDIAL FOREBRAIN BUNDLE; NEUROPHARMACOLOGY; NEUROPROTECTION; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; PRIORITY JOURNAL; RAT; RAT MODEL; SIGNAL TRANSDUCTION; SUBSTANTIA NIGRA; SYSTEMIC THERAPY; WESTERN BLOTTING; ANIMAL; DISEASE MODEL; DRUG EFFECTS; HUMAN; METABOLISM; PARKINSON DISEASE; PATHOLOGY; TOXICITY;

ANIMALS; DISEASE MODELS, ANIMAL; DOPAMINERGIC NEURONS; ERYTHROPOIETIN; HUMANS; HYDROXYDOPAMINES; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; NEUROPROTECTIVE AGENTS; PARKINSON DISEASE; RATS; TYROSINE 3-MONOOXYGENASE;

EID: 84904246230     PISSN: 11073756     EISSN: 1791244X     Source Type: Journal    
DOI: 10.3892/ijmm.2014.1810     Document Type: Article

References (46)

1. Samii A, Nutt JG and Ransom BR: Parkinson's disease. Lancet 363: 1783-1793, 2004. (Pubitemid 38698383)
2. Chaudhuri KR, Healy DG and Schapira AH: Non-motor symptoms of Parkinson's disease: diagnosis and management. Lancet Neurol 5: 235-245, 2006. (Pubitemid 43238347)
3. Fahn S, Oakes D, Shoulson I, et al: Levodopa and the progression of Parkinson's disease. N Engl J Med 351: 2498-2508, 2004.
4. Olanow CW and Jankovic J: Neuroprotective therapy in Parkinson's disease and motor complications: a search for a pathogenesis-targeted, disease-modifying strategy. Mov Disord 20 (Suppl 11): 3-10, 2005.
5. Signore AP, Weng Z, Hastings T, et al: Erythropoietin protects against 6-hydroxydopamine-induced dopaminergic cell death. J Neurochem 96: 428-443, 2006.
6. Csete M, Rodriguez L, Wilcox M and Chadalavada S: Erythropoietin receptor is expressed on adult rat dopaminergic neurons and erythropoietin is neurotrophic in cultured dopaminergic neuroblasts. Neurosci Lett 359: 124-126, 2004. (Pubitemid 38446653)
7. Brines ML, Ghezzi P, Keenan S, et al: Cerami, Erythropoietin crosses the blood-brain barrier to protect against experimental brain injury. Proc Natl Acad Sci USA 97: 10526-10531, 2000.
8. Wei L, Han BH, Li Y, Keogh CL, Holtzman DM and Yu SP: Cell death mechanism and protective effect of erythropoietin after focal ischemia in the whisker-barrel cortex of neonatal rats. J Pharmacol Exp Ther 317: 109-116, 2006.
9. Lu D, Mahmood A, Qu C, Goussev A, Schallert T and Chopp M: Erythropoietin enhances neurogenesis and restores spatial memory in rats after traumatic brain injury. J Neurotrauma 22: 1011-1017, 2005. (Pubitemid 41362067)
10. 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 99: 2258-2263, 2002. (Pubitemid 34169048)
11. Zhang LJ, Xue YQ, Yang C, Yang WH, Chen L, Zhang QJ, Qu TY, Huang S, Zhao LR, Wang XM and Duan WM: Human albumin prevents 6-hydroxydopamine-induced loss of tyrosine hydroxylase in in vitro and in vivo. PLoS One 7: e41226, 2012.
12. Xue YQ, Zhao LR, Guo WP and Duan WM: Intrastriatal administration of erythropoietin protects dopaminergic neurons and improves neurobehavioral outcome in a rat model of Parkinson's disease. Neuroscience 146: 1245-1258, 2007.
13. Paxinos G and Watson C: The Rat Brain in Stereotaxic Coordinates. 6th edition. Amsterdam, Academic Press/Elsevier, p221, 2007.
14. Woodlee MT, Asseo-García AM, Zhao X, Liu SJ, Jones TA, and Schallert T: Testing forelimb placing 'across the midline' reveals distinct, lesion-dependent patterns of recovery in rats. Exp Neurol 191: 310-317, 2005. (Pubitemid 40092874)
15. Ziegler M and Szechtman H: Differences in the behavioral profile of circling under amphetamine and apomorphine in rats with unilateral lesions of the substantia nigra. Behav Neurosci 102: 276-288, 1988.
16. Pegg, CC, He C, Stroink AR, Kattner KA and Wang CX: Technique for collection of cerebrospinal fluid from the cisterna magna in rat. J Neurosci Methods 187: 8-12, 2010.
17. 2 dopamine receptor-mediated motor behaviors. Neuropsychopharmacology 33: 1667-1679, 2008.
18. Granado N, Lastres-Becker I, Ares-Santos S, et al: Nrf2 deficiency potentiates methamphetamine-induced dopaminergic axonal damage and gliosis in the striatum. Glia 59: 1850-1863, 2011.
19. Tan CC, Eckardt KU, Firth JD and Ratcliffe PJ: Feedback modulation of renal and hepatic erythropoietin mRNA in response to graded anemia and hypoxia. Am J Physiol 263: F474-F481, 1992.
20. Marti HH, Wenger RH, Rivas LA, et al: Erythropoietin gene expression in human, monkey and murine brain. Eur J Neurosci 8: 666-676, 1996. (Pubitemid 26114611)
21. Juul SE, Yachnis AT, Rojiani AM and Christensen RD: Immunohistochemical localization of erythropoietin and its receptor in the developing human brain. Pediatr Dev Pathol 2: 148-158, 1999. (Pubitemid 29130201)
22. Nagai A, Nakagawa E, Choi HB, Hatori K, Kobayashi S and Kim SU: Erythropoietin and erythropoietin receptors in human CNS neurons, astrocytes, microglia, and oligodendrocytes grown in culture. J Neuropathol Exp Neurol 60: 386-392, 2001. (Pubitemid 32274054)
23. Knabe W, Knerlich F, Washausen S, et al: Expression patterns of erythropoietin and its receptor in the developing midbrain. Anat Embryol (Berl) 207: 503-512, 2004. (Pubitemid 38392097)
24. 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 92: 3717-3720, 1995.
25. Xue YQ, Ma BF, Zhao LR, et al: AAV9-mediated erythropoietin gene delivery into the brain protects nigral dopaminergic neurons in a rat model of Parkinson's disease. Gene Ther 17: 83-94, 2010.
26. McLeod M, Hong M, Mukhida K, Sadi D, Ulalia R and Mendez I: Erythropoietin and GDNF enhance ventral mesencephalic fiber outgrowth and capillary proliferation following neural transplantation in a rodent model of Parkinson's disease. Eur J Neurosci 24: 361-370, 2006. (Pubitemid 44100328)
27. Zhang F, Signore AP, Zhou Z, Wang S, Cao G and Chen J: Erythropoietin protects CA1 neurons against global cerebral ischemia in rat: potential signaling mechanisms. J Neurosci Res 83: 1241-1251, 2006. (Pubitemid 43668007)
28. Kadota T, Shingo T, Yasuhara T, et al: Continuous intraventricular infusion of erythropoietin exerts neuroprotective/rescue effects upon Parkinson's disease model of rats with enhanced neurogenesis. Brain Res 1254: 120-127, 2009.
29. Lieutaud T, Andrews PJ, Rhodes JK and Williamson R: Characterization of the pharmacokinetics of human recombinant erythropoietin in blood and brain when administered immediately after lateral fluid percussion brain injury and its pharmacodynamic effects on IL-1beta and MIP-2 in rats. J Neurotrauma 25: 1179-1185, 2008.
30. Statler PA, McPherson RJ, Bauer LA Kellert BA and Juul SE: Pharmacokinetics of high-dose recombinant erythropoietin in plasma and brain of neonatal rats. Pediatr Res 61: 671-675, 2007. (Pubitemid 46800274)
31. Xenocostas A, Cheung WK, Farrell F, et al: The pharmacokinetics of erythropoietin in the cerebrospinal fluid after intravenous administration of recombinant human erythropoietin. Eur J Clin Pharmacol 61: 189-195, 2005. (Pubitemid 40768551)
32. Yamada M, Burke C, Colditz P, Johnson DW and Gobe GC: Erythropoietin protects against apoptosis and increases expression of non-neuronal cell markers in the hypoxia-injured developing brain. J Pathol 224: 101-109, 2011.
33. Sifringer M, Brait D, Weichelt U, et al: Erythropoietin attenuates hyperoxia-induced oxidative stress in the developing rat brain. Brain Behav Immun 24: 792-799, 2010.
34. Aluf Y, Vaya J, Khatib S, Loboda Y, Kizhner S and Finberg JP: Specific oxidative stress profile associated with partial striatal dopaminergic depletion by 6-hydroxydopamine as assessed by a novel multifunctional marker molecule. Free Radic Res 44: 635-644, 2010.
35. Lee JY, Koh HC, Chang MY, Park CH, Lee YS and Lee SH: Erythropoietin and bone morphogenetic protein 7 mediate ascorbate-induced dopaminergic differentiation from embryonic mesencephalic precursors. Neuroreport 14: 1401-1404, 2003. (Pubitemid 36936734)
36. Yamamoto M, Koshimura K, Kawaguchi M, Sohmiya M, Murakami Y and Kato Y: Stimulating effect of erythropoietin on the release of dopamine and acetylcholine from the rat brain slice. Neurosci Lett 292: 131-133, 2000.
37. Leist M, Ghezzi P, Grasso G, et al: Derivatives of erythropoietin that are tissue protective but not erythropoietic. Science 305: 239-242, 2004. (Pubitemid 38886736)
38. Zhao W, Kitidis C, Fleming MD, Lodish HF and Ghaffari S: Erythropoietin stimulates phosphorylation and activation of GATA-1 via the PI3-kinase/AKT signaling pathway. Blood 107: 907-915, 2006. (Pubitemid 43158401)
39. Um M and Lodish HF: Antiapoptotic effects of erythropoietin in differentiated neuroblastoma SH-SY5Y cells require activation of both the STAT5 and AKT signaling pathways. J Biol Chem 281: 5648-5656, 2006. (Pubitemid 43847662)
40. Rodriguez-Blanco J, Martin V, Herrera F, Garcia-Santos G, Antolin I and Rodriguez C: Intracellular signaling pathways involved in post-mitotic dopaminergic PC12 cell death induced by 6-hydroxydopamine. J Neurochem 107: 127-140, 2008.
41. Baines CP, Zhang J, Wang GW, et al: Mitochondrial PKCepsilon and MAPK form signaling modules in the murine heart: enhanced mitochondrial PKCepsilon-MAPK interactions and differential MAPK activation in PKCepsilon-induced cardioprotection. Circ Res 90: 390-397, 2002. (Pubitemid 34633907)
42. Zhuang S and Schnellmann RG: A death-promoting role for extracellular signal-regulated kinase. J Pharmacol Exp Ther 319: 991-997, 2006.
43. Pan J, Zhao YX, Wang ZQ, Jin L, Sun ZK and Chen SD: Expression of FasL and its interaction with Fas are mediated by c-Jun N-terminal kinase (JNK) pathway in 6-OHDA-induced rat model of Parkinson disease. Neurosci Lett 428: 82-87, 2007. (Pubitemid 350051174)
44. Wu SS and Frucht SJ: Treatment of Parkinson's disease: what's on the horizon? CNS Drugs 19: 723-743, 2005. (Pubitemid 41324061)
45. Fyhrquist N, Matikainen S and Lauerma A: MK2 signaling: lessons on tissue specificity in modulation of inflammation. J Invest Dermatol 130: 342-344, 2010.
46. Lapchak PA: Carbamylated erythropoietin to treat neuronal injury: new development strategies. Expert Opin Investig Drugs 17: 1175-1186, 2008.