Role of erythropoietin in the brain

Critical Reviews in Oncology/Hematology

Volumn 64, Issue 2, 2007, Pages 159-171

  Noguchi, Constance Tom ^a   Asavaritikrai, Pundit ^a   Teng, Ruifeng ^a   Jia, Yi ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

Blood brain barrier; Brain ischemia; Endothelium; Erythropoietin; Ischemic preconditioning; Neurogenesis; Neuroprotection; Receptor

Indexed keywords

ERYTHROPOIETIN; ERYTHROPOIETIN RECEPTOR; NITRIC OXIDE;

ANEMIA; APOPTOSIS; BLOOD BRAIN BARRIER; BRAIN HYPOXIA; BRAIN ISCHEMIA; CARBAMOYLATION; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CEREBROSPINAL FLUID; COGNITION; DISEASE SEVERITY; DRUG EFFECT; DRUG HALF LIFE; ENDOTHELIUM CELL; ERYTHROID CELL; GLIA CELL; GLYCOSYLATION; HEMATOPOIETIC STEM CELL; HUMAN; HYPOXIA; IN VITRO STUDY; ISCHEMIC PRECONDITIONING; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEUROPROTECTION; NONHUMAN; OLIGODENDROGLIA; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; REVIEW;

ANIMALS; BRAIN CHEMISTRY; ENDOTHELIAL CELLS; ERYTHROPOIETIN; HUMANS; MICE; NEURONS; NEUROPROTECTIVE AGENTS; RECEPTORS, ERYTHROPOIETIN; STEM CELLS;

EID: 34848919488     PISSN: 10408428     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.critrevonc.2007.03.001     Document Type: Review

References (119)

1. Anagnostou A., Liu Z., Steiner M., et al. Erythropoietin receptor mRNA expression in human endothelial cells. Proc Natl Acad Sci USA 91 9 (1994) 3974-3978
2. Anagnostou A., Lee E.S., Kessimian N., Levinson R., and Steiner M. Erythropoietin has a mitogenic and positive chemotactic effect on endothelial cells. Proc Natl Acad Sci USA 87 15 (1990) 5978-5982
3. Morishita E., Masuda S., Nagao M., Yasuda Y., and Sasaki R. Erythropoietin receptor is expressed in rat hippocampal and cerebral cortical neurons, and erythropoietin prevents in vitro glutamate-induced neuronal death. Neuroscience 76 1 (1997) 105-116
4. Jelkmann W., and Wagner K. Beneficial and ominous aspects of the pleiotropic action of erythropoietin. Ann Hematol 83 11 (2004) 673-686
5. Wu H., Liu X., Jaenisch R., and Lodish H.F. Generation of committed erythroid BFU-E and CFU-E progenitors does not require erythropoietin or the erythropoietin receptor. Cell 83 1 (1995) 59-67
6. Lin C.S., Lim S.K., D'Agati V., and Costantini F. Differential effects of an erythropoietin receptor gene disruption on primitive and definitive erythropoiesis. Genes Dev 10 2 (1996) 154-164
7. Yu X., Shacka J.J., Eells J.B., et al. Erythropoietin receptor signalling is required for normal brain development. Development 129 2 (2002) 505-516
8. Tsai P.T., Ohab J.J., Kertesz N., et al. A critical role of erythropoietin receptor in neurogenesis and post-stroke recovery. J Neurosci 26 4 (2006) 1269-1274
9. Masuda S., Okano M., Yamagishi K., Nagao M., Ueda M., and Sasaki R. A novel site of erythropoietin production. Oxygen-dependent production in cultured rat astrocytes. J Biol Chem 269 30 (1994) 19488-19493
10. Marti H.H., Wenger R.H., Rivas L.A., et al. Erythropoietin gene expression in human, monkey and murine brain. Eur J Neurosci 8 4 (1996) 666-676
11. Bernaudin M., Marti H.H., Roussel S., et al. A potential role for erythropoietin in focal permanent cerebral ischemia in mice. J Cereb Blood Flow Metab 19 6 (1999) 643-651
12. Marti H.H. Erythropoietin and the hypoxic brain. J Exp Biol 207 Pt 18 (2004) 3233-3242
13. Ogilvie M., Yu X., Nicolas-Metral V., et al. Erythropoietin stimulates proliferation and interferes with differentiation of myoblasts. J Biol Chem 275 50 (2000) 39754-39761
14. Shingo T., Sorokan S.T., Shimazaki T., and Weiss S. Erythropoietin regulates the in vitro and in vivo production of neuronal progenitors by mammalian forebrain neural stem cells. J Neurosci 21 24 (2001) 9733-9743
15. Yu X., Lin C.S., Costantini F., and Noguchi C.T. The human erythropoietin receptor gene rescues erythropoiesis and developmental defects in the erythropoietin receptor null mouse. Blood 98 2 (2001) 475-477
16. Suzuki N., Ohneda O., Takahashi S., et al. Erythroid-specific expression of the erythropoietin receptor rescued its null mutant mice from lethality. Blood 100 7 (2002) 2279-2288
17. Satoh K., Kagaya Y., Nakano M., et al. Important role of endogenous erythropoietin system in recruitment of endothelial progenitor cells in hypoxia-induced pulmonary hypertension in mice. Circulation 113 11 (2006) 1442-1450
18. Jelkmann W. Effects of erythropoietin on brain function. Curr Pharm Biotechnol 6 1 (2005) 65-79
19. Quelle F.W., Wang D., Nosaka T., et al. Erythropoietin induces activation of Stat5 through association with specific tyrosines on the receptor that are not required for a mitogenic response. Mol Cell Biol 16 4 (1996) 1622-1631
20. Zhao W., Kitidis C., Fleming M.D., Lodish H.F., and Ghaffari S. Erythropoietin stimulates phosphorylation and activation of GATA-1 via the PI3-kinase/AKT signaling pathway. Blood 107 3 (2006) 907-915
21. Digicaylioglu M., and Lipton S.A. Erythropoietin-mediated neuroprotection involves cross-talk between Jak2 and NF-kappaB signalling cascades. Nature 412 6847 (2001) 641-647
22. Chong Z.Z., Kang J.Q., and Maiese K. Erythropoietin is a novel vascular protectant through activation of Akt1 and mitochondrial modulation of cysteine proteases. Circulation 106 23 (2002) 2973-2979
23. Liu C., Shen K., Liu Z., and Noguchi C.T. Regulated human erythropoietin receptor expression in mouse brain. J Biol Chem 272 51 (1997) 32395-32400
24. Juul S.E., Anderson D.K., Li Y., and Christensen R.D. Erythropoietin and erythropoietin receptor in the developing human central nervous system. Pediatr Res 43 1 (1998) 40-49
25. Knabe W., Knerlich F., Washausen S., et al. Expression patterns of erythropoietin and its receptor in the developing midbrain. Anat Embryol (Berl) 207 6 (2004) 503-512
26. David R.B., Lim G.B., Moritz K.M., Koukoulas I., and Wintour E.M. Quantitation of the mRNA levels of Epo and EpoR in various tissues in the ovine fetus. Mol Cell Endocrinol 188 1-2 (2002) 207-218
27. Digicaylioglu M., Bichet S., Marti H.H., et al. Localization of specific erythropoietin binding sites in defined areas of the mouse brain. Proc Natl Acad Sci USA 92 9 (1995) 3717-3720
28. Chin K., Yu X., Beleslin-Cokic B., et al. Production and processing of erythropoietin receptor transcripts in brain. Brain Res Mol Brain Res 81 1-2 (2000) 29-42
29. Lewczuk P., Hasselblatt M., Kamrowski-Kruck H., et al. Survival of hippocampal neurons in culture upon hypoxia: effect of erythropoietin. Neuroreport 11 16 (2000) 3485-3488
30. Nagai A., Nakagawa E., Choi H.B., Hatori K., Kobayashi S., and Kim S.U. Erythropoietin and erythropoietin receptors in human CNS neurons, astrocytes, microglia, and oligodendrocytes grown in culture. J Neuropathol Exp Neurol 60 4 (2001) 386-392
31. Chin K., Oda N., Shen K., and Noguchi C.T. Regulation of transcription of the human erythropoietin receptor gene by proteins binding to GATA-1 and Sp1 motifs. Nucleic Acids Res 23 15 (1995) 3041-3049
32. Pandolfi P.P., Roth M.E., Karis A., et al. Targeted disruption of the GATA3 gene causes severe abnormalities in the nervous system and in fetal liver haematopoiesis. Nat Genet 11 1 (1995) 40-44
33. Yamaji R., Okada T., Moriya M., et al. Brain capillary endothelial cells express two forms of erythropoietin receptor mRNA. Eur J Biochem 239 2 (1996) 494-500
34. Livnah O., Stura E.A., Middleton S.A., Johnson D.L., Jolliffe L.K., and Wilson I.A. Crystallographic evidence for preformed dimers of erythropoietin receptor before ligand activation. Science 283 5404 (1999) 987-990
35. Kilic E., Kilic U., Soliz J., Bassetti C.L., Gassmann M., and Hermann D.M. Brain-derived erythropoietin protects from focal cerebral ischemia by dual activation of ERK-1/-2 and Akt pathways. FASEB J 19 14 (2005) 2026-2028
36. Chong Z.Z., Kang J.Q., and Maiese K. Erythropoietin fosters both intrinsic and extrinsic neuronal protection through modulation of microglia, Akt1, Bad, and caspase-mediated pathways. Br J Pharmacol 138 6 (2003) 1107-1118
37. Um M., and Lodish H.F. Antiapoptotic effects of erythropoietin in differentiated neuroblastoma SH-SY5Y cells require activation of both the STAT5 and AKT signaling pathways. J Biol Chem 281 9 (2006) 5648-5656
38. Bunn H.F., Gu J., Huang L.E., Park J.W., and Zhu H. Erythropoietin: a model system for studying oxygen-dependent gene regulation. J Exp Biol 201 Pt 8 (1998) 1197-1201
39. Prass K., Scharff A., Ruscher K., et al. Hypoxia-induced stroke tolerance in the mouse is mediated by erythropoietin. Stroke 34 8 (2003) 1981-1986
40. Chikuma M., Masuda S., Kobayashi T., Nagao M., and Sasaki R. Tissue-specific regulation of erythropoietin production in the murine kidney, brain, and uterus. Am J Physiol Endocrinol Metab 279 6 (2000) E1242-E1248
41. Studer L., Csete M., Lee S.H., et al. Enhanced proliferation, survival, and dopaminergic differentiation of CNS precursors in lowered oxygen. J Neurosci 20 19 (2000) 7377-7383
42. Wang L., Zhang Z.G., Zhang R.L., et al. Neurogenin 1 mediates erythropoietin enhanced differentiation of adult neural progenitor cells. J Cereb Blood Flow Metab 26 4 (2006) 556-564
43. Warnecke C., Zaborowska Z., Kurreck J., et al. Differentiating the functional role of hypoxia-inducible factor (HIF)-1alpha and HIF-2alpha (EPAS-1) by the use of RNA interference: erythropoietin is a HIF-2alpha target gene in Hep3B and Kelly cells. FASEB J 18 12 (2004) 1462-1464
44. Chavez J.C., Baranova O., Lin J., and Pichiule P. The transcriptional activator hypoxia inducible factor 2 (HIF-2/EPAS-1) regulates the oxygen-dependent expression of erythropoietin in cortical astrocytes. J Neurosci 26 37 (2006) 9471-9481
45. Bunn H.F. New agents that stimulate erythropoiesis. Blood 109 3 (2007) 868-873
46. Juul S. Erythropoietin in the central nervous system, and its use to prevent hypoxic-ischemic brain damage. Acta Paediatr Suppl 91 438 (2002) 36-42
47. Juul S.E., Stallings S.A., and Christensen R.D. Erythropoietin in the cerebrospinal fluid of neonates who sustained CNS injury. Pediatr Res 46 5 (1999) 543-547
48. 2 homeostasis by hypoxia-inducible factor 1 alpha. Genes Dev 12 2 (1998) 149-162
49. Siren A.L., Knerlich F., Poser W., Gleiter C.H., Bruck W., and Ehrenreich H. Erythropoietin and erythropoietin receptor in human ischemic/hypoxic brain. Acta Neuropathol (Berl) 101 3 (2001) 271-276
50. Marti H.H., Gassmann M., Wenger R.H., et al. Detection of erythropoietin in human liquor: intrinsic erythropoietin production in the brain. Kidney Int 51 2 (1997) 416-418
51. Springborg J.B., Sonne B., Frederiksen H.J., et al. Erythropoietin in the cerebrospinal fluid of patients with aneurysmal subarachnoid haemorrhage originates from the brain. Brain Res 984 1-2 (2003) 143-148
52. Brines M.L., Ghezzi P., Keenan S., et al. Erythropoietin crosses the blood-brain barrier to protect against experimental brain injury. Proc Natl Acad Sci USA 97 19 (2000) 10526-10531
53. Banks W.A., Jumbe N.L., Farrell C.L., Niehoff M.L., and Heatherington A.C. Passage of erythropoietic agents across the blood-brain barrier: a comparison of human and murine erythropoietin and the analog darbepoetin alfa. Eur J Pharmacol 505 1-3 (2004) 93-101
54. Abraham C.S., Harada N., Deli M.A., and Niwa M. Transient forebrain ischemia increases the blood-brain barrier permeability for albumin in stroke-prone spontaneously hypertensive rats. Cell Mol Neurobiol 22 4 (2002) 455-462
55. Xenocostas A., Cheung W.K., Farrell F., et al. The pharmacokinetics of erythropoietin in the cerebrospinal fluid after intravenous administration of recombinant human erythropoietin. Eur J Clin Pharmacol 61 3 (2005) 189-195
56. Ehrenreich H., Degner D., Meller J., et al. Erythropoietin: a candidate compound for neuroprotection in schizophrenia. Mol Psychiatry 9 1 (2004) 42-54
57. Juul S.E., McPherson R.J., Farrell F.X., Jolliffe L., Ness D.J., and Gleason C.A. Erytropoietin concentrations in cerebrospinal fluid of nonhuman primates and fetal sheep following high-dose recombinant erythropoietin. Biol Neonate 85 2 (2004) 138-144
58. Uzum G., Sarper Diler A., Bahcekapili N., and Ziya Ziylan Y. Erythropoietin prevents the increase in blood-brain barrier permeability during pentylentetrazol induced seizures. Life Sci 78 22 (2006) 2571-2576
59. Martinez-Estrada O.M., Rodriguez-Millan E., Gonzalez-De Vicente E., Reina M., Vilaro S., and Fabre M. Erythropoietin protects the in vitro blood-brain barrier against VEGF-induced permeability. Eur J Neurosci 18 9 (2003) 2538-2544
60. Wang L., Zhang Z., Wang Y., Zhang R., and Chopp M. Treatment of stroke with erythropoietin enhances neurogenesis and angiogenesis and improves neurological function in rats. Stroke 35 7 (2004) 1732-1737
61. Wang L., Zhang Z.G., Zhang R.L., et al. Matrix metalloproteinase 2 (MMP2) and MMP9 secreted by erythropoietin-activated endothelial cells promote neural progenitor cell migration. J Neurosci 26 22 (2006) 5996-6003
62. Ribatti D., Presta M., Vacca A., et al. Human erythropoietin induces a pro-angiogenic phenotype in cultured endothelial cells and stimulates neovascularization in vivo. Blood 93 8 (1999) 2627-2636
63. Ribatti D., Vacca A., Roccaro A.M., Crivellato E., and Presta M. Erythropoietin as an angiogenic factor. Eur J Clin Invest 33 10 (2003) 891-896
64. Yasuda Y., Masuda S., Chikuma M., Inoue K., Nagao M., and Sasaki R. Estrogen-dependent production of erythropoietin in uterus and its implication in uterine angiogenesis. J Biol Chem 273 39 (1998) 25381-25387
65. Masuda S., Kobayashi T., Chikuma M., Nagao M., and Sasaki R. The oviduct produces erythropoietin in an estrogen- and oxygen-dependent manner. Am J Physiol Endocrinol Metab 278 6 (2000) E1038-E1044
66. Heeschen C., Aicher A., Lehmann R., et al. Erythropoietin is a potent physiologic stimulus for endothelial progenitor cell mobilization. Blood 102 4 (2003) 1340-1346
67. Bahlmann F.H., De Groot K., Spandau J.M., et al. Erythropoietin regulates endothelial progenitor cells. Blood 103 3 (2004) 921-926
68. Urao N., Okigaki M., Yamada H., et al. Erythropoietin-mobilized endothelial progenitors enhance reendothelialization via Akt-endothelial nitric oxide synthase activation and prevent neointimal hyperplasia. Circ Res 98 11 (2006) 1405-1413
69. Kertesz N., Wu J., Chen T.H., Sucov H.M., and Wu H. The role of erythropoietin in regulating angiogenesis. Dev Biol 276 1 (2004) 101-110
70. Wang X.Q., and Vaziri N.D. Erythropoietin depresses nitric oxide synthase expression by human endothelial cells. Hypertension 33 3 (1999) 894-899
71. Banerjee D., Rodriguez M., Nag M., and Adamson J.W. Exposure of endothelial cells to recombinant human erythropoietin induces nitric oxide synthase activity. Kidney Int 57 5 (2000) 1895-1904
72. Beleslin-Cokic B.B., Cokic V.P., Yu X., Weksler B.B., Schechter A.N., and Noguchi C.T. Erythropoietin and hypoxia stimulate erythropoietin receptor and nitric oxide production by endothelial cells. Blood 104 7 (2004) 2073-2080
73. Ruschitzka F.T., Wenger R.H., Stallmach T., et al. Nitric oxide prevents cardiovascular disease and determines survival in polyglobulic mice overexpressing erythropoietin. Proc Natl Acad Sci USA 97 21 (2000) 11609-11613
74. Quaschning T., Ruschitzka F., Stallmach T., et al. Erythropoietin-induced excessive erythrocytosis activates the tissue endothelin system in mice. FASEB J 17 2 (2003) 259-261
75. Kanagy N.L., Perrine M.F., Cheung D.K., and Walker B.R. Erythropoietin administration in vivo increases vascular nitric oxide synthase expression. J Cardiovasc Pharmacol 42 4 (2003) 527-533
76. Defouilloy C., Teiger E., Sediame S., et al. Polycythemia impairs vasodilator response to acetylcholine in patients with chronic hypoxemic lung disease. Am J Respir Crit Care Med 157 5 Pt 1 (1998) 1452-1460
77. Santhanam A.V., Smith L.A., Nath K.A., and Katusic Z.S. In vivo stimulatory effect of erythropoietin on endothelial nitric oxide synthase in cerebral arteries. Am J Physiol Heart Circ Physiol 291 2 (2006) H781-H786
78. Calapai G., Marciano M.C., Corica F., et al. Erythropoietin protects against brain ischemic injury by inhibition of nitric oxide formation. Eur J Pharmacol 401 3 (2000) 349-356
79. Genc K., Genc S., Baskin H., and Semin I. Erythropoietin decreases cytotoxicity and nitric oxide formation induced by inflammatory stimuli in rat oligodendrocytes. Physiol Res 55 1 (2006) 33-38
80. Bernaudin M., Nedelec A.S., Divoux D., MacKenzie E.T., Petit E., and Schumann-Bard P. Normobaric hypoxia induces tolerance to focal permanent cerebral ischemia in association with an increased expression of hypoxia-inducible factor-1 and its target genes, erythropoietin and VEGF, in the adult mouse brain. J Cereb Blood Flow Metab 22 4 (2002) 393-403
81. Malhotra S., Savitz S.I., Ocava L., and Rosenbaum D.M. Ischemic preconditioning is mediated by erythropoietin through PI-3 kinase signaling in an animal model of transient ischemic attack. J Neurosci Res 83 1 (2006) 19-27
82. Ruscher K., Freyer D., Karsch M., et al. Erythropoietin is a paracrine mediator of ischemic tolerance in the brain: evidence from an in vitro model. J Neurosci 22 23 (2002) 10291-10301
83. Grimm C., Wenzel A., Groszer M., et al. HIF-1-induced erythropoietin in the hypoxic retina protects against light-induced retinal degeneration. Nat Med 8 7 (2002) 718-724
84. Grimm C., Wenzel A., Stanescu D., et al. Constitutive overexpression of human erythropoietin protects the mouse retina against induced but not inherited retinal degeneration. J Neurosci 24 25 (2004) 5651-5658
85. Sakanaka M., Wen T.C., Matsuda S., et al. In vivo evidence that erythropoietin protects neurons from ischemic damage. Proc Natl Acad Sci USA 95 8 (1998) 4635-4640
86. 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 253 1 (1998) 26-32
87. Wen T.C., Rogido M., Genetta T., and Sola A.E. Permanent focal cerebral ischemia activates erythropoietin receptor in the neonatal rat brain. Neurosci Lett 355 3 (2004) 165-168
88. Genc S., Kuralay F., Genc K., et al. Erythropoietin exerts neuroprotection in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-treated C57/BL mice via increasing nitric oxide production. Neurosci Lett 298 2 (2001) 139-141
89. Sun Y., Zhou C., Polk P., Nanda A., and Zhang J.H. Mechanisms of erythropoietin-induced brain protection in neonatal hypoxia-ischemia rat model. J Cereb Blood Flow Metab 24 2 (2004) 259-270
90. Yatsiv I., Grigoriadis N., Simeonidou C., et al. Erythropoietin is neuroprotective, improves functional recovery, and reduces neuronal apoptosis and inflammation in a rodent model of experimental closed head injury. FASEB J 19 12 (2005) 1701-1703
91. Celik M., Gokmen 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 4 (2002) 2258-2263
92. Gorio A., Gokmen N., Erbayraktar S., et al. Recombinant human erythropoietin counteracts secondary injury and markedly enhances neurological recovery from experimental spinal cord trauma. Proc Natl Acad Sci USA 99 14 (2002) 9450-9455
93. Villa P., Bigini P., Mennini T., et al. Erythropoietin selectively attenuates cytokine production and inflammation in cerebral ischemia by targeting neuronal apoptosis. J Exp Med 198 6 (2003) 971-975
94. Viviani B., Bartesaghi S., Corsini E., et al. Erythropoietin protects primary hippocampal neurons increasing the expression of brain-derived neurotrophic factor. J Neurochem 93 2 (2005) 412-421
95. Soliz J., Joseph V., Soulage C., et al. Erythropoietin regulates hypoxic ventilation in mice by interacting with brainstem and carotid bodies. J Physiol 568 Pt 2 (2005) 559-571
96. Springborg J.B., Ma X., Rochat P., et al. A single subcutaneous bolus of erythropoietin normalizes cerebral blood flow autoregulation after subarachnoid haemorrhage in rats. Br J Pharmacol 135 3 (2002) 823-829
97. Sugawa M., Sakurai Y., Ishikawa-Ieda Y., Suzuki H., and Asou H. Effects of erythropoietin on glial cell development; oligodendrocyte maturation and astrocyte proliferation. Neurosci Res 44 4 (2002) 391-403
98. Li W., Maeda Y., Yuan R.R., Elkabes S., Cook S., and Dowling P. Beneficial effect of erythropoietin on experimental allergic encephalomyelitis. Ann Neurol 56 6 (2004) 767-777
99. Zhang J., Li Y., Cui Y., et al. Erythropoietin treatment improves neurological functional recovery in EAE mice. Brain Res 1034 1-2 (2005) 34-39
100. Arishima Y., Setoguchi T., Yamaura I., Yone K., and Komiya S. Preventive effect of erythropoietin on spinal cord cell apoptosis following acute traumatic injury in rats. Spine 31 21 (2006) 2432-2438
101. Vitellaro-Zuccarello L., Mazzetti S., Madaschi L., Bosisio P., Gorio A., and De Biasi S. Erythropoietin-mediated preservation of the white matter in rat spinal cord injury. Neuroscience 144 3 (2007) 865-877
102. Shen Q., Goderie S.K., Jin L., et al. Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 304 5675 (2004) 1338-1340
103. Wiessner C., Allegrini P.R., Ekatodramis D., Jewell U.R., Stallmach T., and Gassmann M. Increased cerebral infarct volumes in polyglobulic mice overexpressing erythropoietin. J Cereb Blood Flow Metab 21 7 (2001) 857-864
104. Ogunshola O.O., Djonov V., Staudt R., Vogel J., and Gassmann M. Chronic excessive erythrocytosis induces endothelial activation and damage in mouse brain. Am J Physiol Regul Integr Comp Physiol 290 3 (2006) R678-R684
105. Ehrenreich H., Hasselblatt M., Dembowski C., et al. Erythropoietin therapy for acute stroke is both safe and beneficial. Mol Med 8 8 (2002) 495-505
106. Hasselblatt M., Ehrenreich H., and Siren A.L. The brain erythropoietin system and its potential for therapeutic exploitation in brain disease. J Neurosurg Anesthesiol 18 2 (2006) 132-138
107. Vaziri N.D., Zhou X.J., Naqvi F., et al. Role of nitric oxide resistance in erythropoietin-induced hypertension in rats with chronic renal failure. Am J Physiol 271 1 Pt 1 (1996) E113-E122
108. Fukuda M.N., Sasaki H., Lopez L., and Fukuda M. Survival of recombinant erythropoietin in the circulation: the role of carbohydrates. Blood 73 1 (1989) 84-89
109. Imai N., Higuchi M., Kawamura A., 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 194 2 (1990) 457-462
110. Dong Y.J., Kung C., and Goldwasser E. Receptor binding of asialoerythropoietin. J Cell Biochem 48 3 (1992) 269-276
111. Erbayraktar S., Grasso G., Sfacteria A., et al. Asialoerythropoietin is a nonerythropoietic cytokine with broad neuroprotective activity in vivo. Proc Natl Acad Sci USA 100 11 (2003) 6741-6746
112. Wang X., Zhu C., Wang X., et al. The nonerythropoietic asialoerythropoietin protects against neonatal hypoxia-ischemia as potently as erythropoietin. J Neurochem 91 4 (2004) 900-910
113. Grasso G., Sfacteria A., Erbayraktar S., et al. Amelioration of spinal cord compressive injury by pharmacological preconditioning with erythropoietin and a nonerythropoietic erythropoietin derivative. J Neurosurg Spine 4 4 (2006) 310-318
114. Leist M., Ghezzi P., Grasso G., et al. Derivatives of erythropoietin that are tissue protective but not erythropoietic. Science 305 5681 (2004) 239-242
115. Hanazono Y., Sasaki K., Nitta H., Yazaki Y., and Hirai H. Erythropoietin induces tyrosine phosphorylation of the beta chain of the GM-CSF receptor. Biochem Biophys Res Commun 208 3 (1995) 1060-1066
116. Jubinsky P.T., Krijanovski O.I., Nathan D.G., Tavernier J., and Sieff C.A. The beta chain of the interleukin-3 receptor functionally associates with the erythropoietin receptor. Blood 90 5 (1997) 1867-1873
117. Scott C.L., Robb L., Papaevangeliou B., Mansfield R., Nicola N.A., and Begley C.G. Reassessment of interactions between hematopoietic receptors using common beta-chain and interleukin-3-specific receptor beta-chain-null cells: no evidence of functional interactions with receptors for erythropoietin, granulocyte colony-stimulating factor, or stem cell factor. Blood 96 4 (2000) 1588-1590
118. Brines M., Grasso G., Fiordaliso F., et al. Erythropoietin mediates tissue protection through an erythropoietin and common beta-subunit heteroreceptor. Proc Natl Acad Sci USA 101 41 (2004) 14907-14912
119. Brines M., and Cerami A. Emerging biological roles for erythropoietin in the nervous system. Nat Rev Neurosci 6 6 (2005) 484-494