The pleiotropic effects of erythropoietin in the central nervous system

Journal of Neuropathology and Experimental Neurology

Volumn 62, Issue 3, 2003, Pages 228-236

  Buemi, Michele ^a   Cavallaro, E ^a   Floccari, F ^a   Sturiale, A ^a   Aloisi, C ^a   Trimarchi, M ^a   Corica, F ^a   Frisina, N ^a  

^a UNIVERSITY OF MESSINA   (Italy)

Author keywords

Astrocytes; Brain; Erythropoietin; Neurons; Neuroprotection

Indexed keywords

ANTIOXIDANT; CATALASE; ERYTHROPOIETIN; ERYTHROPOIETIN RECEPTOR; ESTRADIOL; FREE RADICAL; GLUTAMIC ACID; GLUTATHIONE PEROXIDASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; NITRIC OXIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; PROTEIN KINASE B; RAS PROTEIN; RECOMBINANT ERYTHROPOIETIN; STAT5 PROTEIN; SUPEROXIDE DISMUTASE;

ADULT; ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ASTROCYTE; BLOOD BRAIN BARRIER; BRAIN; BRAIN HYPOXIA; CENTRAL NERVOUS SYSTEM; CEREBROSPINAL FLUID; CONTROLLED STUDY; ENZYME ACTIVITY; FETUS; FETUS LIVER; GENE EXPRESSION REGULATION; HORMONAL REGULATION; HORMONE SYNTHESIS; HUMAN; HYPOGLYCEMIA; KIDNEY; NERVE CELL; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; PLEIOTROPY; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; SIGNAL TRANSDUCTION; TISSUE SPECIFICITY; UTERUS;

EID: 0037339634     PISSN: 00223069     EISSN: None     Source Type: Journal    
DOI: 10.1093/jnen/62.3.228     Document Type: Review

References (79)

1. Erslev AJ. Erythropoietin. N Engl J Med 1991;324:1339-44
2. Maxwell PH, Osmond MK, Pugh CW, et al. Identification of the renal erythropoietin-producing cells using transgenic mice. Kidney Int 1993;44:1149-62
3. Ratcliffe PJ, O'Rourke JF, Maxwell PH, Pugh CW. Oxygen sensing, hypoxia-inducible factor-1 and the regulation of mammalian gene expression. J Exp Biol 1998;201:1153-62
4. Miller BA, Bell LL, Lynch CJ, Cheung JY. Erythropoietin modulation of intracellular calcium: A role for tyrosine phosphorylation. Cell Calcium 1994;16:481-90
5. Buemi M, Corica F, Aloisi C, et al. Recombinant human erythropoietin (rHuEPO): A drug beyond the correction of uremic anaemia. J Nephrol 2002;15:97-103
6. Chikuma M, Masuda S, Kobayashi T, Nagao M, Sasaki R. Tissue-specific regulation of erythropoietin production in the murine kidney, brain and uterus. Am J Physiol Endocrinol Metab 2000;279: E1242-E1248
7. Marti HH, Gassman M, Wenger RH, et al. Detection of erythropoietin in human liquor: Intrinsic erythropoietin production in the brain. Kidney Int 1997;51:416-18
8. Masuda S, Nagao M, Takahata K, et al. Functional erythropoietin receptor of the cells with neural characteristics. Comparison with receptor properties of erythroid cells. J Biol Chem 1993;268:11208-16
9. Masuda S, Okano M, Yamagishi K, Nagao M, et al. A novel site of erythropoietin production. Oxygen-dependent production in cultured rat astrocytes. J Biol Chem 1994;269:19488-93
10. 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 U S A 1995;92:3717-20
11. Morishida 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;76:105-16
12. Marti HH, Wemger RH, Rivas LA, et al. Erythropoietin gene expression in human, monkey and murine brain. Eur J Neurosci 1996;8:666-76
13. Li Y, Juul SE, Morris-Wiman JA, Calhoun DA, Christensen RD. Erythropoietin receptors are expressed in the central nervous system of mid-trimester human fetuses. Pediatr Res 1996;40:376-80
14. Chun Liu, Kun Shen, Ziyao Liu, Noguchi C Tom. Regulated human erythropoietin receptor expression in mouse brain. J Biol Chem 1997;272:32395-400
15. Juul SE, Yachnis AT, Rojiani AM. Immunohistochemical localization of erythropoietin and its receptor in the developing human brain. Pediatr Dev Pathol 1999;2:148-58
16. Juul SE, Yachnis AT, Christensen RD. Tissue distribution of erythropoietin and erythropoietin receptor in developing human fetuses. Early Hum Dev 1998;52:235-49
17. Juul SE. Erythropoietin in the neonate. Current Probl Pediatr 1999;29:129-49
18. Juul SE. Nonerythropietic roles of erythropoietin in the fetus and neonate. Clin Perinatol 2000;27:697-716
19. Dame C, Bartmann P, Wolber E, Fahnenstich H, Hofmann D, Fandrey J. Erythropoietin gene expression in different areas of the developing human central nervous system. Brain Res Dev Brain Res 2000;125:69-74
20. Yu X, Lin CS, Costantini F, Noguchi CT. The human erythropoietin receptor gene rescues erythropoiesis and developmental defects in the erythropoietin receptor null mouse. Blood 2001;98:475-77
21. Chin K, Yu X, Beleslin-Cokic B, et al. Production and processing of erythropoietin receptor transcripts in brain. Mol Brain Res 2000;81:29-42
22. Juul SE, Anderson DK, Li Y, Chriestenens RD. Erythropoietin and erythropoietin receptor in the developing human central nervous system. Pediatr Res 1998;43:40-49
23. Bernaudin M, Bellail A, Marti HH, et al. Neurons and astrocytes express EPO mRNA: Oxygen-sensing mechanisms that involve the redox-state of the brain. Glia 2000;30:271-78
24. Bergeron M, Gidday J, Yu AY, Semenza GL, Ferriero DM, Sharp FR. Role of hypoxia-inducible factor-1 in hypoxia induced ischemic tolerance in neonatal rat brain. Ann Neurol 2000;48:285-96
25. Chandel NS, Maltepe E, Goldwasser E, et al. Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc Natl Acad Sci U S A 1998;95:11715-20
26. Masuda S, Chikuma M, Susaki R. Insulin-like growth factors and insulin stimulate erythropoietin production in primary cultured astrocytes. Brain Res 1997;745:63-70
27. Juul SE, Hareum J, Li Y, et al. Erythropoietin is present in the cerebrospinal fluid of neonates. J Pediatr 1997;130:428-30
28. Juul SE, Stallings SA, Christensen RD. Erythropoietin in the cerebrospinal fluid of neonates who sustained CNS injury. Pediatr Res 1999;46:543-47
29. Buemi M, Allegra A, Corica F, et al. Intravenous recombinant erythropoietin does not increase erythropoietin in cerebrospinal fluid. Nephrol Dial Transpl 2000;15:422-23
30. Brines ML, Ghezzi P, Keenan S, et al. Erythropoietin crosses the blood-brain barrier to protect against experimental brain injury. Proc Natl Acad Sci U S A 2000;97:10526-31
31. Yamaji R, Okada T, Moriya M, et al. Brain capillary endothelial cells express two forms of erythropoietin receptor mRNA. Eur J Biochem 1996;239:494-500
32. Nakamura T, Ebihara I, Shimada N, Koide H. Elevated levels of erythropoietin in cerebrospinal fluid of depressed patients. Am J Med Sci 1998;315:199-201
33. Jennings DB. The physiochemistry of (H) and respiratory control: Roles of PCO2 strong ions and their hormonal regulation. Can J Physiol Pharmac 1994;72:1499-1512
34. Velisek L, Veliskova J, Mosha SL. Site-specific effects of local pH changes in the substantia nigra pars reticulata on flurothyl-induced seizures. Brain Res 1998;782:310-13
35. Moreno F, Sanz-Guajardo D, Lopez Gomez JM, et al. Increasing the hematocrit has a beneficial effect on quality of life and is safe in selected hemodialysis patients. J Am Soc Neph 2000;11:335-42
36. Nissenson AR. Epoietin and cognitive function. Am J Kidney Dis 1992;20(Suppl 1):21-24
37. Pickett JL, Theberge DC, Brown WS, et al. Normalizing hematocrit in dialysis patients improves brain function. Am J Kidney Dis June 1999;33:1122-30
38. Konishi Y, Chui DH, Hirose H, Kunishita T, Tabira T. Trophic effect of erythropoietin and other hematopoietic factors on central cholinergic neurons in vitro and in vivo. Brain Res 1993;609:29-35
39. Tabira T, Konishi Y, Gallyas F Jr. Neurotrophic effect of hematopoietic cytokines on cholinergic and other neurons in vitro. Int J Dev Neurosci 1995;13:241-52
40. Campana WM, Misasi R, O'Brien JS. Identification of a neurotrophic sequence in erythropoietin. Int J Mol Med 1998;1:235-41
41. Lewczuk P, Hasselblatt M, Kamrowski-Kruck H, et al. Survival of hippocampal neurons in culture upon hypoxia: Effect of erythropoietin. Neuroreport 2000;11:3485-88
42. Sadamoto Y, Igase K, Sakanaka M, et al. Erythropoietin prevents place navigation disability and cortical infarction in rats with permanent occlusion of the middle cerebral artery. Biochem Biophys Res Commun 1998;253:26-32
43. Sakanaka M, Wen TC, Matsuda S, Morishita E, Nagao M, Sasaki R. In vivo evidence that erythropoietin protects neurons from ischemic damage. Proc Natl Acad Sci U S A 1998;95:4653-40
44. 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;19:643-51
45. Siren AL, Fratelli M, Brines M, et al. Erythropoietin prevents neural apoptosis after cerebral ischemia and metabolic stress. Proc Natl Acad Sci U S A 2001;98:74044-49
46. Catania MA, Marciano MC, Parisi A, et al. Erythropoietin prevents cognition impairment induced by transient brain ischemia in gerbils. Eur J Pharmacol 2002;437:147-50
47. Calapai G, Marciano MC, Corica F, et al. Erythropoietin protects against brain ischemic injury by inhibition of nitric oxide formation. Eur J Pharm 2000;401:349-56
48. Cerami A, Brines ML, Ghezzi P, Cerami JC. Effects of epoietina alfa on the central nervous system. Semin Oncol 2001;45:7-14
49. Benveniste H, Drejer J, Schousboe A, Diemer NH. Elevation of extracellular concentrations of glutamate and aspartate in rat hippocampus during transient cerebral ischemia monitored by intracerebral microdialysis. J Neurochem 1984;43:1369-74
50. Drejer J, Benveniste H, Diemer NH, Schousboe A. Cellular origin of ischemia-induced glutamate release from brain tissue in vivo and in vitro. J Neurochem 1985;45:145-51
51. Choi DW, Rothman SM. The role of glutamate neurotoxicity in hypoxic-ischemic neuronal death. Annu Rev Neurosci 1990;13:171-82
52. Sinor AD, Greenberg DA. Erythropoietin protects cultured cortical neurons, but not astroglia from hypoxia and AMPA toxicity. Neurosci Lett 2000;290:213-15
53. Sasaki R, Masuda S, Nagao M. Erythropoietin: Multiple physiological function and regulation of biosynthesis. Biosci Biotechnol Biochem 2000;64:1775-93
54. Buemi M, Grasso G, Corica F, et al. In vivo evidence that erythropoietin has a neuroprotective effect during subarachnoid hemorrhage. Eur J Pharmacol 2000;392:31-34
55. Kassel NF, Sasaki T, Colohan ART, Nazar G. Cerebral vasospasm following aneurysmal subarachnoid hemorrhage: Progress review. Stroke 1985;16:562-72
56. Bederson JB, Levy AL, Ding WH, et al. Acute vasoconstriction after subarachnoid hemorrhage. Neurosurgery 1998;42:352-60
57. Asano T, Sano K. Pathogenic role of no-reflow phenomenon in experimental subarachnoid hemorrhage in dogs. J Neurosurg 1977;46:454-66
58. Nagai H, Katsumata T, Ohya M. Effect of subarachnoid hemorrhage on microcirculation in hypothalamus and brain stem of dogs. Neurochirurgia 1976;19:135-44
59. Hart MN. Morphometry of brain parenchymal vessels following subarachnoid hemorrhage. Stroke 1981;11:653-55
60. Kim P, Sundt TM Jr, Vanhoutte PM. Alteration in endothelium-dependent responsiveness of the canine basilar artery after subarachnoid hemorrhage. J Neurosurg 1988;69:239-46
61. Vane JR, Anggard EE, Botting RM. Regulatory functions of the vascular endothelium. N Engl J Med 1990;323:27-36
62. Hatake K, Wakabayashi I, Kakishita E, Hishida S. Impairment of endothelium-dependent relaxation in human basilar artery after subarachnoid hemorrhage. Stroke 1992;23:1111-17
63. Sehba F, Schwartz AY, Chereshnev I, Bederson J. Acute decrease in cerebral nitric oxide levels after subarachnoid hemorrhage. J Cereb Blood Flow Metab 2000;20:604-11
64. Shimada N, Graf R, Rosner G, et al. Ischemic flow threshold for extracellular glutamate increase in cat cortex. J Cereb Blood Flow Metab 1989;9:603-6
65. Alafaci C, Salpietro F, Grasso G, et al. Effect of recombinant human erythropoietin on cerebral ischemia following experimental subarachnoid hemorrhage. Eur J Pharmacol 2000;406:219-25
66. Springborg JB, Ma X, Rochat P, et al. A single subcutaeous bolus of erythropoietin normalizes cerebral blood flow autoregulation after subarachnoid haemorrhage in rats. Br J Pharmacol 2002;135:823-29
67. Koshimura K, Murakami Y, Sohmiya M, Tanaka J, Kato Y. Effect of erythropoietin on neuronal activity. J Neurochem 1999;72:2565-72
68. Banerjee D, Rodriguez M, Nag M, Adamson JW. Exposure of endothelial cells to recombinant human erythropoietin induces nitric oxide synthase activity. Kidney Int 2000;57:1895-1904
69. Buemi M, Allegra A, Aloisi C, Corica F, Frisina N. Hemodynamic effects of recombinant human erythropoietin. Nephron 1999;81:1-4
70. Yamamoto M, Koshimura K, Kawaguchi M, et al. Stimulating effect of erythropoietin on the release of dopamine and acetylcholine from the rat brain slice. Neurosci Lett 2000;292:131-33
71. Kawakami M, Iwasaki S, Sato K, Takahashi M. Erythropoietin inhibits calcium-induced neurotransmitter release from clonal neuronal cells. Biochem Biophys Res Commun 2000;279:293-97
72. Kaplan DR, Miller FD. Neurotrophin signal transduction in the nervous system. Curr Opin Neurobiol 2000;10:381-91
73. Marti HH, Bernaudin M, Petit E, Bauer C. Neuroprotection and angiogenesis: Dual role of erythropoietin in brain ischemia. News Physiol Sci 2000;15:225-29
74. Buemi M, Sturiale A, Galeano MR, et al. Recombinant human erythropoietin influences revascularization and healing in a random model of ischemic flaps in rat. Arch Dermatol Res (in press)
75. Trent JT III, Watts RA, Hargrove MS. Human neuroglobin, a hexacoordinate hemoglobin that reversibly binds oxygen. J Biol Chem 2001;276:30106-10
76. Buemi M, Marino D, Marino MT et al. Does erythropoietin augment the Ca(2+)-mediated K+ flow into the red blood cells in normotensive and hypertensive subjects? Nephron 1991;59:343-44
77. Assandri R, Egger M, Gassmann M, et al. Erythropoietin modulates intracellular calcium in a human neuroblastoma cell line. J Physiology 1999;516:343-52
78. Miller BA, Barber DL, Bell LL, et al. Identification of the Erythropoietin receptor domain required for calcium channel activation. J Biol Chem 1999;274:20465-72
79. Digicayliuglu M, Lipton SA. Erythropoietin mediated neuroprotection involves cross-talk between Jak 2 and NF-(kappa) B signaling cascades. Nature 2001;412:641-47