Brain and cancer: The protective role of erythropoietin

Medicinal Research Reviews

Volumn 25, Issue 2, 2005, Pages 245-259

  Buemi, Michele ^a,b,c,d,e   Caccamo, Chiara ^a   Nostro, Lorena ^a   Cavallaro, Emanuela ^a,f   Floccari, Fulvio ^a   Grasso, Giovanni ^a  

^a UNIVERSITY OF MESSINA   (Italy)

^b Department of Internal Medicine ^*  (Italy)

^c Department of Internal Medicine   (Italy)

^d Sch of Specialization in Nephrology   (Italy)

^e CNR   (Italy)

^f REGINA APOSTOLORUM HOSPITAL   (Italy)

Author keywords

Angiogenesis; Cancer; Erythropoietin; Hypoxia; Neuroprotection; Pleiotropy

Indexed keywords

ANGIOGENIC FACTOR; ANTINEOPLASTIC AGENT; CISPLATIN; ERYTHROPOIETIN; ERYTHROPOIETIN RECEPTOR; GROWTH FACTOR; RECOMBINANT ERYTHROPOIETIN;

ANEMIA; ANIMAL CELL; BRAIN FUNCTION; BRAIN INJURY; CANCER; CANCER PATIENT; CELL CYCLE; CENTRAL NERVOUS SYSTEM; DOSE RESPONSE; DOWN REGULATION; EMBRYO; GENE EXPRESSION; HUMAN; HUMAN CELL; HYPOXIA; MOUSE; NEOVASCULARIZATION (PATHOLOGY); NERVE CELL DIFFERENTIATION; NEUROLOGIC DISEASE; NEUROPROTECTION; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; NEWBORN; NONHUMAN; ONTOGENY; PATHOPHYSIOLOGY; RAT; REVIEW; SIGNAL TRANSDUCTION; TUMOR CELL;

EID: 14544267131     PISSN: 01986325     EISSN: None     Source Type: Journal    
DOI: 10.1002/med.20012     Document Type: Review

References (97)

1. 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.
2. Marti HH, Gassman M, Wenger RH, et al. Detection of erythropoietin in human liquor: Intrinsic erythropoietin production in the brain. Kidney Int 1997;51:416-418.
3. Buemi M, Cavallaro E, Floccari F, Sturiale A, Aloisi C, Trimarchi M, Corica F, Frisina N. The pleiotropic effects of erythropoietin in the central nervous system. J Neuropathol Exp Neurol 2003;62(3): 228-236.
4. 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;268:11208-11216.
5. 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;269:19488-19493.
6. Digicaylioglu M, Bichet S, Marti HH, Wengr RH, Rivas L, et al. Localization of specific erythropoietin binding sites in defined areas of the mouse brain. Proc Natl Acad Sci USA 1995;92:3717-3720.
7. 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;76:105-116.
8. Marti HH, Wemger RH, Rivas LA, et al. Erythropoietin gene expression in human, monkey, and murine brain. Eur J Neurosci 1996;8:666-676.
9. Li Y, Juul SE, Mrris-Wiman JA, Calhoun DA, Christensen RD. Erythropoietin receptors are expressed in the central nervous system of mid-trimester human fetuses. Pediatr Res 1996;40(3):376-380.
10. 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(2):475-477.
11. Liu C, Shen K, Liu Z, Noguchi CT. Regulated human erythropoietin receptor expression in mouse brain. J Biol Chem 1997;272(51):32395-32400.
12. Juul SE, Yachnis AT, Rojiani AM. Immunohistochemical localization of erythropoietin and its receptor in the developing human brain. Pediatr Dev Pathol 1999;2(2):148-158.
13. Juul SE, Yachnis AT, Christensen RD. Tissue distribution of erythropoietin and erythropoietin receptor in the developing human fetuses. Early Hum Dev 1998;52(3):235-249.
14. Juul SE, Anderson DK, Li Y, Cnriestenens RD. Erythropoietin and erythropoietin receptor in the developing human central nervous system. Pediatr Res 1998;43:40-49.
15. Juul SE. Erythropoietin in the neonate. Curr Probl Pediatr 1999;29(5):129-149.
16. Juul SE. Nonerythropietic roles of erythropoietin in the fetus and neonate. Neonatal Hematol 2000;27(3):527-541.
17. 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(1-2): 69-74.
18. Chin K, Yu X, Beleslin-Cokic B, Liu C, Shen K, Mohrenweiser HW, Noguchi CT. Production and processing of erythropoietin receptor transcripts in brain. Mol Brain Res 2000;81:29-42.
19. Bernaudin M, Bellail A, Marti HH, Yvon A, Vivien D, Duchatelle I, Mackanzie ET, Petit E. Neurons and astrocytes express EPO mRNA: Oxygen-sensing mechanisms that involve the redox-state of the brain. Glia 2000;30:271-278.
20. 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(3):285-296.
21. Chandel NS, Maltepe E, Goldwasser E, et al. Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc Natl Acad Sci USA 1998;95:11715-11720.
22. 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.
23. Juul SE, Harcum J, Li Y, et al. Erythropoietin is present in the cerebrospinal fluid of neonates. J Pediatr 1997;130:428-430.
24. Juul SE, Stallings SA, Christensen RD. Erythropoietin in the cerebrospinal fluid of neonates who sustained CNS injury. Pediatr Res 1999;46(5):543-547.
25. Buemi M, Allegra A, Corica F, Floccari F, D'Avella D, Aloisi C, Calapai G, Iacopino G, Frisina N. Intravenous recombinant erythropoietin does not increase erythropoietin in cerebrospinal fluid. Nephrol Dial Transpl 2000;15:422-423.
26. Brines ML, Ghezzi P, Keenan S, Agnello D, de Lanorelle NC, Cerami C, Itri LM, Cerami A. Erythropoietin crosses the blood-brain barrier to protect against experimental brain injury. PNAS 2000;97(19):10526-10531.
27. Yamaji R, Okada T, Moriya M, et al. Brain capillary endothelial cells express two forms of erythropoietin receptor mRNA. Eur J Biochem 1996;15;239(2):494-500.
28. 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.
29. 2 strong ions and their hormonal regulation. Can J Physiol Pharmacol 1994;72:1499-1512.
30. 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;782:310-313.
31. 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 Nephrol 2000;11:335-342.
32. Nissenson AR. Epoetin and cognitive function. AJKD 1992;20(Suppl 1):21-24.
33. Pickett JL, Theberege DC, Brown WS, Schweitzer SU, et al. Normalizing hematocrit in dialysis patients improves brain function. AJKD 1999;33(6):1122-1130.
34. 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.
35. Tabira T, Konishi Y, Gallyas F, Jr. Neurotrophic effect of hematopoietic cytokines on cholinergic and other neurons in vitro. Int J Dev Neurosci 1995;13:241-252.
36. Campana WM, Misasi R, O'Brien JS. Identification of a neurotrophic sequence in erythropoietin. Int J Mol Med 1998;1:235-241.
37. 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;43:1369-1374.
38. 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;45:145-151.
39. Choi DW, Rothman SM. The role of glutamate neurotoxicity in hypoxic-ischemic neuronal death. Annu Rev Neurosci 1990;13:171-182.
40. Sinor AD, Greenberg DA. Erythropoietin protects cultured cortical neurons, but not astroglia from hypoxia and AMPA toxicity. Neurosci Lett 2000;290:213-215.
41. Lewczuk P, Hasselblatt M, Kamrowski-Kruck H, Heyer A, Unzicker C, Sirèn AL, Ehrenreich H. Survival of hippocampal neurons in culture upon hypoxia: Effect of erythropoietin. Neuropharmacol Neuroxicol 2000;11(16):3485-3488.
42. Sadamoto Y, Igase K, Sakanaka M, Sato K, Otsuka H, Sasaki S, Masuda S, Sasaki R. 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 USA 1998;95:4635-4640.
44. Bernaudin M, Marti HH, Roussel S, Divoux D, Nouvelot A, MacKenzie ET, Petit E. A potential role for erythropoietin in focal permanent cerebral ischemia in mice. J Cereb Blood Flow Metab 1999;19:643-651.
45. Calapai G, Marciano MC, Corica F, Allegra A, Parisi A, Frisina N, Caputi AP, Buemi M. Erythropoietin protects against brain ischemic injury by inhibition of nitric oxide formation. Eur J Pharm 2000;401(3): 349-356.
46. Cerami A, Brines ML, Ghezzi P, Cerami JC. Effects of epoetina alfa on the central nervous system. Semin Oncol 2001;45(1):7-14.
47. Kassel NF, Sasaki T, Colohan ART, Nazar G. Cerebral vasospasm following aneurysmal subarachnoid hemorrhage: Progress review. Stroke 1985;16:562-572.
48. Bederson JB, Levy AL, Ding WH, Kahn R, DiPerna CA, Jenkins AL III, Vallabhakosyula P. Acute vasoconstriction after subarachnoid haemorrhage. Neurosurgery 1998;42:352-360.
49. Asano T, Sano K. Pathogenic role of no-reflow phenomenon in experimental subarachnoid hemorrhage in dogs. J Neurosurg 1977;46:454-466.
50. Nagai H, Katsumata T, Ohya M. Effect of subarachnoid hemorrhage on microcirculation in hypothalamus and brain stem of dogs. Neurochirurgia 1976;19:135-144.
51. Hart MN. Morphometry of brain parenchymal vessels following subarachnoid hemorrhage. Stroke 1981;11:653-655.
52. Kim P, Sundt TM, Jr., Vanhoutte PM. Alteration in endothelium-dependent responsiveness of the canine basilar artery after subarachnoid haemorrhage. J Neurosurg 1988;69:239-246.
53. Vane JR, Anggard EE, Botting RM. Regulatory functions of the vascular endothelium. N Engl J Med 1990;323:27-36.
54. Hatake K, Wakabayashi I, Kakishita E, Hishida S. Impairment of endothelium-dependent relaxation in human basilar artery after subarachnoid haemorrhage. Stroke 1992;23:1111-1117.
55. Sehba F, Schwartz AY, Chereshnev I, Bederson J. Acute decrease in cerebral nitric oxide levels after subarachnoid hemorrhage. J Cereb Blood Flow Metab 2000;20:604-611.
56. Buemi M, Grasso G, Corica F, Calapai G, Salpietro FM, Casuscelli T, Sfacteria A, Aloisi C, Alafaci C, Sturiale A, Frisina N, Tomasello F. In vivo evidence that erythropoietin has a neuroprotective effect during subarachnoid haemorrhage. Eur J Pharmacol 2000;392:31-34.
57. Alafaci C, Salpietro F, Grasso G, Sfacteria A, Passalacqua M, Morabito A, Tripodo E, Calapai G, Buemi M, Tomasello F. Effect of recombinant human erythropoietin on cerebral ischemia following experimental subarachnoid haemorrhage. Eur J Pharmacol 2000;406(2):219-225.
58. Koshimura K, Murakami Y, Sohmiya M, Tanaka J, Kato Y. Effect of erythropoietin on neuronal activity. J Neurochem 1999;72:2565-2572.
59. 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.
60. Buemi M, Allegra A, Aloisi C, Corica F, Frisina N. Hemodynamic effects of recombinant human erythropoietin. Nephron 1999;81:1-4.
61. Yamamoto M, Koshimura K, Kawaguchi M, Sohmiya M, et al. Stimulating effect of erythropoietin on the release of dopamine and acetylcholine from the rat brain slice. Neurosci Lett 2000;292:131-133.
62. Kawakami M, Iwasaki S, Sato K, Takahashi M. Erythropoietin inhibits calcium-induced neurotransmitter release from clonal neuronal cells. Biochem Biophys Res Commun 2000;279:293-297.
63. Kaplan DR, Miller FD. Signal transduction by the neurotrophin receptors. Curr Opin Cell Biol 1997;9(2):213-221.
64. Buemi M, Marino D, Marino MT, Allegra A, Squadrito F, Giacobbe MS, Frisina N. Does erythropoietin augment the Ca(2+)-mediated K + flow into the red blood cells in normotensive and hypertensive subjects? Nephron 1991;59(2):343-344.
65. Assandri R, Egger M, gassmann M, Niggli E, Bauer C, Foster J, Gorlach A. Erythropoietin modulates intracellular calcium in a human neuroblastoma cell line. J Physiol 1999;516(2):343-352.
66. Miller BA, Barber DL, Bell LL, Beattie BK, Zhang M, et al. Identification of the erythropoietin receptor domain required for calcium channel activation. J Biol Chem 1999;274(29):20465-20472.
67. Sasaki R, Masuda S, Nagao M. Erythropoietin: Multiple physiological function and regulation of biosynthesis. Biosci Biotechnol Biochem 2000;64(9):1775-1793.
68. Digicayliuglu M, Lipton SA. Erythropoietin mediated neuroprotection involves cross-talk between Jak 2 and NF-(kappa) B signaling cascades. Nature 2001;412:641-647.
69. Marti HH, Bernaudin M, Petit E, Bauer C. Neuroprotection and angiogenesis: Dual role of erythropoietin in brain ischemia. News Physiol Sci 2000;15:225-229.
70. Sirèn AL, Fratelli M, Brines M, Goamans C, Casagrande S, et al. Erythropoietin prevents neural apoptosis after cerebral ischemia and metabolic stress. Proc Natl Acad Sci USA 2001;98(7):4044-4049.
71. Trent JT III, Watts RA, Hargrove MS. Human neuroglobin, a hexacoordinate hemoglobin that reversibly binds oxygen. J Biol Chem 2001;276(32):30106-30110.
72. Erbayraktar S, Grasso G, Sfacteria A, Xie Q, Coleman T, Kreilgaard M, Torup L, Erbayrakatar Z, Gokmen N, Yilmaz O, Ghezzi P, Villa O, Fratelli M, Casagrande S, Leist M, Helboe L, Gerwein J, Christensen S, Geist MA, Pedersen LO, Cerami-Hand C, Wuerth JP, Cerami A, Brines M. Asialoerythropoietin is a non erythropoietic cytokine with broad neuroprotective activity in vivo. PNAS 2003;100(11):6741-6746.
73. Alvarez Arroyo MV, Castilla A, Gonzalez Pacheco FR, Tan D, Riesco A, Casado S, Caramelo C. Role of vascular endothelial growth factor on erythropoietin-related endothelial cell proliferation. J Am Soc Nephrol 1998;9:1998-2004.
74. Choi K, Kennedy M, Kazarov, Papadimitriou, Keller G. A common precursor for hematopoietic and endothelial cells. Development 1998;125:725-732.
75. Goldberg MA, Schneider TJ. Similarities between the oxygen-sensing mechanisms regulating the expression of vascular endothelial growth factor and erythropoietin. J Biol Chem 1994;269:4355-4359.
76. Metcalf D. Peptide factors, haemopoietic grown factors. Lancet 1989;1:825-827.
77. Buemi M, Sturiale A, Galeano MR, Sansotta C, Vaccaro M, Campo GM, Cicciarello R, Floccari F, D'Amico D, Cavallari V, Calapai G, Frisina N, Corica F, Vermiglio G. Recombinant human erythropoietin influences revascularization and healing in a random model of ischemic flaps in rats. Acta Derm Venereol 2002;82(6):411-417.
78. Dammacco F, Ribatti D, Presta M, et al. Human erythropoietin induces a pro-angiogenic phenotype in cultured endothelial cells and stimulates neovascularization in vivo. Blood 1999;93(8):2627-2636.
79. Ludwig H. Epoietin in cancer-related anemia. Nephrol Dial Transp 1999;14(Suppl 2):85-92.
80. Thatcher N, De Campo ES, Bell DR. Epoietin alpha prevents anemia and reduces transfusion requirement in patients undergoing primarily platinum-based chemotherapy for small cell lung cancer. Br J Cancer 1999;80(3-4):396-402.
81. Henke M, Guttenberger R, Barke A. Erythropoietin for patients undergoing radiotherapy: A pilot study. Radiother Oncol 1999;50(2):185-190.
82. Senzer N. Rationale for a phase III study of erythropoietin as a neurocognitive protectant in patients with lung cancer receiving prophylactic cranial irradiation. Sem Oncol 2002;29(6 Supp 19):47-52.
83. Musto P. The role of recombinant erythropoietin for the treatment of anemia in multiple myeloma. Leuk Lymphoma 1998;29(3-4):283-291.
84. Dammacco F, Silvestris F, Castoldi GL. The effectiveness and tolerability of Epoetin-α in patients with multiple myeloma refractory to chemotherapy. Int J Clin Lab Res 1998;28(2):127-134.
85. Bowen DT, Caro J, Jacobs A, Lewis T, Janows N, Wieczorek A. Serum erythropoietin in patients with myelodysplasia. Exp Hematol 1989;17:537.
86. Mitjavila MT, Villeval JL, Cramer P, et al. Effect of granulocyte-macrophage colony stimulating factor and erythropoietin on leukemic erythroid colony formation in human early erythroblastic leukemia. Blood 1987;70:965-973.
87. Motoji T, Hoshino S, Veda M, et al. Enhanced growth of clonogenic cells from acute myeloblastic leukemia by erythropoietin. Br J Haematol 1990;75:60-67.
88. Lappin TR, Maxwell AP, Johnston PG. EPO's alter ego: Erythropoietin has multiple actions. Stem Cells 2002;20:485-492.
89. Leyland-Jones B, BEST Investigators and Study Group. Breast cancer trial with erythropoietin terminated unexpectedly. Lancet Oncol 2003;4(8):459-460.
90. Henke M, Laszig R, Rübe C, Schäfer U, Haase K-D, Schilcher B, Mose S, Beer KT, Burger U, Dougherty C, Frommhold H. Erythropoietin to treat head and neck cancer patients with anaemia undergoing radiotherapy: Randomised, double-blind, placebo-controlled trial. Lancet 2003;362(9392):1255-1260.
91. Rosen FR, Haraf DJ, Kies MS, Stenson K, Portugal L, List MA, Brockstein BE, Mittal BB, Rademaker AW, Witt ME, Pelzer H, Weichselbaum RR, Vokes EE. Multicenter randomized phase II study of paclitaxel (1-hour infusion), fluorouracil, hydroxyurea, and concomitant twice daily radiation with or without erythropoietin for advanced head and neck cancer. Clin Cancer Res 2003;9(5):1689-1697.
92. Yasuda Y, Fujita Y, Matsuo T, Koinuma S, Hara S, Yazaki A, Onoza M, Hashimoto M, Musha T, Ogawa K, Fujita H, Nakamura Y, Shiozaki H, Utsumi H. Erythropoietin regulates tumor growth of human malignancies. Carcinogenesis 2003;24(6):1021-1029.
93. Acs G, Acs P, Beckwith SM, Pittis RL, Clements E, Wong K, Verma G. Erythropoietin and erythropoietin receptor expression in human cancer. Cancer Res 2001;61(9):3561-3565.
94. Breibart W. Identifying patients at risk for, and treatment of major psychiatric complications of cancer. Support Care Cancer 1995;3:45-60.
95. O'Shaughnessy J. Effects of epoetin alfa on cognitive function, mood, asthenia, a quality of life in women with breast cancer undergoing adjuvant chemotherapy. Clin Breast Cancer 2002;3(Suppl 3):S116-S120.
96. Vansteenkiste J, Rossi Gregory, Foote MA. Darbepoetin alfa: A new approach to the treatment of chemotherapy-induced anaemia. Expert Opin Biol Ther 2003;3:501-508.
97. Buemi M, Aloisi C, Cavallaro E, Corica F, Floccari F, Grasso G, Lasco A, Pettinato, Ruello A, Sturiale A, Frisina N. Recombinant human erythropoietin (rHuEPO): More than just the correction of uremic anemia. J Nephrol 2002;15(2):97-103.