Erythropoietin receptor expression is concordant with erythropoietin but not with common β chain expression in the rat brain throughout the life span

Journal of Comparative Neurology

Volumn 514, Issue 4, 2009, Pages 403-414

  Sanchez, Pascal E ^a,b,c,d,e   Navarro, Fabrice P ^a,b,c,d   Fares, Raafat P ^a,b,c,d,e   Nadam, Jérémie ^a,b   Georges, Béatrice ^a,b,c,d,e   Moulin, Colette ^a,b,c,d,e   Le Cavorsin, Marion ^a,b,c,d,e   Bonnet, Chantal ^a,b,c,d,e   Ryvlin, Philippe ^e,f   Belmeguenai, Amor ^a,b,c,d,e   Bodennec, Jacques ^a,b,c,d,e   Morales, Anne ^a,b,c,d,e   Bezin, Laurent ^a,b,c,d,e  

^a UNIVERSITÉ DE LYON   (France)

^b UNIVERSITÉ LYON 1   (France)

^c Laboratoire de Physiologie Int&EACUTE grative Cellulaire et Mol&EACUTE culaire Villeurbanne   (France)

^d IFR 41   (France)

^e INSERM   (France)

^f HÔPITAL NEUROLOGIQUE   (France)

Author keywords

Ageing; Development; Hippocampus; Hypothalamus; Neocortex; PC12 cells

Indexed keywords

ERYTHROPOIETIN; ERYTHROPOIETIN RECEPTOR; MESSENGER RNA; NERVE GROWTH FACTOR;

AGING; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BETA CHAIN; CELL POPULATION; CONTROLLED STUDY; GENE LOCATION; GENETIC TRANSCRIPTION; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LIFESPAN; MALE; NERVE CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TISSUE STRUCTURE; ANALYSIS OF VARIANCE; ANIMAL; ASTROCYTE; BRAIN; CELL STRAIN; GENE EXPRESSION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROGLIA; NEURITE; SPRAGUE DAWLEY RAT;

AGING; ANALYSIS OF VARIANCE; ANIMALS; ASTROCYTES; BRAIN; ERYTHROPOIETIN; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; MALE; MICROGLIA; NEURITES; NEURONS; PC12 CELLS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ERYTHROPOIETIN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 65649093029     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22020     Document Type: Article

References (56)

1. Bernaudin M, Marti HH, Roussel S, Divoux D, Nouvelot A, MacKenzie ET, Petit E. 1999. A potential role for erythropoietin in focal permanent cerebral ischemia in mice. J Cereb Blood Flow Metab 19:643-651.
2. Bierer R, Peceny MC, Hartenberger CH, Ohls RK. 2006. Erythropoietin concentrations and neurodevelopmental outcome in preterm infants. Pediatrics 118:e635-640.
3. Brines M, Cerami A. 2005. Emerging biological roles for erythropoietin in the nervous system. Nat Rev Neurosci 6:484-494.
4. Brines ML, Ghezzi P, Keenan S, Agnello D, de-Lanerolle NC, Cerami C, Itri LM, Cerami A. 2000. Erythropoietin crosses the blood-brain barrier to protect against experimental brain injury. Proc Natl Acad Sci U S A 97:10526-10531.
5. Brines M, Grasso G, Fiordaliso F, Sfacteria A, Ghezzi P, Fratelli M, Latini R, Xie QW, Smart J, Su-Rick CJ, Pobre E, Diaz D, Gomez D, Hand C, Coleman T, Cerami A. 2004. Erythropoietin mediates tissue protection through an erythropoietin and common beta-subunit heteroreceptor. Proc Natl Acad Sci U S A 101:14907-14912.
6. Byts N, Samoylenko A, Fasshauer T, Ivanisevic M, Hennighausen L, Ehrenreich H, Siren AL. 2008. Essential role for Stat5 in the neurotrophic but not in the neuroprotective effect of erythropoietin. Cell Death Differ (in press).
7. Carbonell-Estrany X, Figueras-Aloy J, Alvarez E. 2005. Erythropoietin and prematurity - where do we stand? J Perinatal Med 33:277-286.
8. Chen ZY, Asavaritikrai P, Prchal JT, Noguchi CT. 2007. Endogenous erythropoietin signaling is required for normal neural progenitor cell proliferation. J Biol Chem 282:25875-25883.
9. Chung YH, Kim SI, Joo KM, Kim YS, Lee WB, Yun KW, Cha CI. 2004. Age-related changes in erythropoietin immunoreactivity in the cerebral cortex and hippocampus of rats. Brain Res 1018:141-146.
10. Coleman TR, Westenfelder C, Togel FE, Yang Y, Hu Z, Swenson L, Leuvenink HG, Ploeg RJ, d'Uscio LV, Katusic ZS, Ghezzi P, Zanetti A, Kaushansky K, Fox NE, Cerami A, Brines M. 2006. Cytoprotective doses of erythropoietin or carbamylated erythropoietin have markedly different procoagulant and vasoactive activities. Proc Natl Acad Sci U S A 103:5965-5970.
11. D'Andrea RJ, Gonda TJ. 2000. A model for assembly and activation of the GM-CSF, IL-3 and IL-5 receptors: insights from activated mutants of the common beta subunit. Exp Hematol 28:231-243.
12. Demers EJ, McPherson RJ, Juul SE. 2005. Erythropoietin protects dopaminergic neurons and improves neurobehavioral outcomes in juvenile rats after neonatal hypoxia-ischemia. Pediatr Res 58:297-301.
13. Ehrenreich H, Hasselblatt M, Dembowski C, Cepek L, Lewczuk P, Stiefel M, Rustenbeck HH, Breiter N, Jacob S, Knerlich F, Bohn M, Poser W, Ruther E, Kochen M, Gefeller O, Gleiter C, Wessel TC, De Ryck M, Itri L, Prange H, Cerami A, Brines M, Siren AL. 2002. Erythropoietin therapy for acute stroke is both safe and beneficial. Mol Med 8:495-505.
14. Ehrenreich H, Degner D, Meller J, Brines M, Behe M, Hasselblatt M, Woldt H, Falkai P, Knerlich F, Jacob S, von Ahsen N, Maier W, Bruck W, Ruther E, Cerami A, Becker W, Siren AL. 2004. Erythropoietin: a candidate compound for neuroprotection in schizophrenia. Mol Psychiatry 9:42-54.
15. Ehrenreich H, Fischer B, Norra C, Schellenberger F, Stender N, Stiefel M, Siren AL, Paulus W, Nave KA, Gold R, Bartels C. 2007a. Exploring recombinant human erythropoietin in chronic progressive multiple sclerosis. Brain 130:2577-2588.
16. Ehrenreich H, Hinze-Selch D, Stawicki S, Aust C, Knolle-Veentjer S, Wilms S, Heinz G, Erdag S, Jahn H, Degner D, Ritzen M, Mohr A, Wagner M, Schneider U, Bohn M, Huber M, Czernik A, Pollmacher T, Maier W, Siren AL, Klosterkotter J, Falkai P, Ruther E, Aldenhoff JB, Krampe H. 2007b. Improvement of cognitive functions in chronic schizophrenic patients by recombinant human erythropoietin. Mol Psychiatry 12: 206-220.
17. Elliott S, Busse L, Bass MB, Lu H, Sarosi I, Sinclair AM, Spahr C, Um M, Van G, Begley CG. 2006. Anti-Epo receptor antibodies do not predict Epo receptor expression. Blood 107:1892-1895.
18. Fu QL, Wu W, Wang H, Li X, Lee VW, So KF. 2008. Up-regulated endogenous erythropoietin/erythropoietin receptor system and exogenous erythropoietin rescue retinal ganglion cells after chronic ocular hypertension. Cell Mol Neurobiol 28:317-329.
19. Grasso G, Sfacteria A, Passalacqua M, Morabito A, Buemi M, Macri B, Brines ML, Tomasello F. 2005. Erythropoietin and erythropoietin receptor expression after experimental spinal cord injury encourages therapy by exogenous erythropoietin. Neurosurgery 56:821-827; discussion 821-827.
20. Greene E, Naranjo JN. 1987. Degeneration of hippocampal fibers and spatial memory deficit in the aged rat. Neurobiol Aging 8:35-43.
21. Grimm C, Wenzel A, Groszer M, Mayser H, Seeliger M, Samardzija M, Bauer C, Gassmann M, Remé CE, 2002. HIF-1-induced erythropoietin in the hypoxic retina protects against light-induced retinal degeneration. Nature Med 8:718-724.
22. Guillemin GJ, Brew BJ. 2004. Microglia, macrophages, perivascular macrophages, and pericytes: a review of function and identification. J Leukocyte Biol 75:388-397.
23. Hanazono Y, Sasaki K, Nitta H, Yazaki Y, Hirai H. 1995. Erythropoietin induces tyrosine phosphorylation of the beta chain of the GM-CSF receptor. Biochem Biophys Res Commun 208:1060-1066.
24. Hasselblatt M, Ehrenreich H, Siren AL. 2006. The brain erythropoietin system and its potential for therapeutic exploitation in brain disease. J Neurosurg Anesthesiol 18:132-138.
25. Henke M, Verma A, Acs G. 2006. Erythropoietin receptors on cancer cells: exciting perspectives, difficult to appreciate. Blood 108:1107-1108; author reply 1108-1109.
26. Jubinsky PT, Krijanovski OI, Nathan DG, Tavernier J, Sieff CA. 1997. The beta chain of the interleukin-3 receptor functionally associates with the erythropoietin receptor. Blood 90:1867-1873.
27. Juul SE, McPherson RJ, Farrell FX, Jolliffe L, Ness DJ, Gleason CA. 2004. Erytropoietin concentrations in cerebrospinal fluid of nonhuman primates and fetal sheep following high-dose recombinant erythropoietin. Biol Neonate 85:138-144.
28. Kadar T, Silbermann M, Brandeis R, Levy A. 1990. Age-related structural changes in the rat hippocampus: correlation with working memory deficiency. Brain Res 512:113-120.
29. Kirkeby A, van Beek J, Nielsen J, Leist M, Helboe L. 2007. Functional and immunochemical characterisation of different antibodies against the erythropoietin receptor. J Neurosci Methods 164:50-58.
30. Knabe W, Knerlich F, Washausen S, Kietzmann T, Siren AL, Brunnett G, Kuhn HJ, Ehrenreich H. 2004. Expression patterns of erythropoietin and its receptor in the developing midbrain. Anat Embryol 207:503-512.
31. Koshimura K, Murakami Y, Sohmiya M, Tanaka J, Kato Y. 1999. Effects of erythropoietin on neuronal activity. J Neurochem 72:2565-2572.
32. Kretz A, Happold CJ, Marticke JK, Isenmann S. 2005. Erythropoietin promotes regeneration of adult CNS neurons via Jak2/Stat3 and PI3K/AKT pathway activation. Mol Cell Neurosci 29:569-579.
33. Kumral A, Uysal N, Tugyan K, Sonmez A, Yilmaz O, Gokmen N, Kiray M, Genc S, Duman N, Koroglu TF, Ozkan H, Genc K. 2004. Erythropoietin improves long-term spatial memory deficits and brain injury following neonatal hypoxia-ischemia in rats. Behav Brain Res 153:77-86.
34. Leist M, Ghezzi P, Grasso G, Bianchi R, Villa P, Fratelli M, Savino C, Bianchi M, Nielsen J, Gerwien J, Kallunki P, Larsen AK, Helboe L, Christensen S, Pedersen LO, Nielsen M, Torup L, Sager T, Sfacteria A, Erbayraktar S, Erbayraktar Z, Gokmen N, Yilmaz O, Cerami-Hand C, Xie QW, Coleman T, Cerami A, Brines M. 2004. Derivatives of erythropoietin that are tissue protective but not erythropoietic. Science 305:239-242.
35. Liu C, Shen K, Liu Z, Noguchi CT. 1997. Regulated human erythropoietin receptor expression in mouse brain. J Biol Chem 272:32395-32400.
36. Maiese K, Li F, Chong ZZ. 2004. Erythropoietin in the brain: can the promise to protect be fulfilled? Trends Pharmacol Sci 25:577-583.
37. Maiese K, Chong ZZ, Li F, Shang YC. 2008. Erythropoietin: Elucidating new cellular targets that broaden therapeutic strategies. Prog Neurobiol 85:194-213.
38. McPherson RJ, Demers EJ, Juul SE. 2007. Safety of high-dose recombinant erythropoietin in a neonatal rat model. Neonatology 91:36-43.
39. Mullen RJ, Buck CR, Smith AM. 1992. NeuN, a neuronal specific nuclear protein in vertebrates. Development 116:201-211.
40. Nadam J, Navarro F, Sanchez P, Moulin C, Georges B, Laglaine A, Pequignot JM, Morales A, Ryvlin P, Bezin L. 2007. Neuroprotective effects of erythropoietin in the rat hippocampus after pilocarpine-induced status epilepticus. Neurobiol Dis 25:412-426.
41. Noguchi CT, Asavaritikrai P, Teng R, Jia Y. 2007. Role of erythropoietin in the brain. Crit Rev Oncol Hematol 64:159-171.
42. Ransome MI, Turnley AM. 2008. Erythropoietin promotes axonal growth in a model of neuronal polarization. Mol Cell Neurosci 38:537-547.
43. Ribatti D, Vacca A, Roccaro AM, Crivellato E, Presta M. 2003. Erythropoietin as an angiogenic factor. Eur J Clin Invest 33:891-896.
44. Sakanaka M, Wen TC, Matsuda S, Masuda S, Morishita E, Nagao M, Sasaki R. 1998. In vivo evidence that erythropoietin protects neurons from ischemic damage. Proc Natl Acad Sci U S A 95:4635-4640.
45. Sattler MB, Merkler D, Maier K, Stadelmann C, Ehrenreich H, Bahr M, Diem R. 2004. Neuroprotective effects and intracellular signaling pathways of erythropoietin in a rat model of multiple sclerosis. Cell Death Differ 11(Suppl 2):S181-S192.
46. Shein NA, Horowitz M, Alexandrovich AG, Tsenter J, Shohami E. 2005. Heat acclimation increases hypoxia-inducible factor 1alpha and erythropoietin receptor expression: implication for neuroprotection after closed head injury in mice. J Cereb Blood Flow Metab 25:1456-1465.
47. Shingo T, Sorokan ST, Shimazaki T, Weiss S. 2001. Erythropoietin regulates the in vitro and in vivo production of neuronal progenitors by mammalian forebrain neural stem cells. J Neurosci 21:9733-9743.
48. Sinclair AM, Rogers N, Busse L, Archibeque I, Brown W, Kassner PD, Watson JE, Arnold GE, Nguyen KC, Powers S, Elliott S. 2008. Erythropoietin receptor transcription is neither elevated nor predictive of surface expression in human tumour cells. Br J Cancer 98:1059-1067.
49. Soliz J, Gassmann M, Joseph V. 2007. Soluble erythropoietin receptor is present in the mouse brain and is required for the ventilatory acclimatization to hypoxia. J Physiol 583:329-336.
50. Spandou E, Papadopoulou Z, Soubasi V, Karkavelas G, Simeonidou C, Pazaiti A, Guiba-Tziampiri O. 2005. Erythropoietin prevents long-term sensorimotor deficits and brain injury following neonatal hypoxia-ischemia in rats. Brain Res 1045:22-30.
51. Tsai PT, Ohab JJ, Kertesz N, Groszer M, Matter C, Gao J, Liu X, Wu H, Carmichael ST. 2006. A critical role of erythropoietin receptor in neurogenesis and poststroke recovery. J Neurosci 26:1269-1274.
52. Um M, Gross AW, Lodish HF. 2007. A "classical" homodimeric erythropoietin receptor is essential for the antiapoptotic effects of erythropoietin on differentiated neuroblastoma SH-SY5Y and pheochromocytoma PC-12 cells. Cell Signal 19:634-645.
53. Verdier F, Gomez S, Lacombe C, Mayeux P. 2006. Selected anti-Epo receptor antibodies predict Epo receptor expression. Blood 108:1106; author reply 1107.
54. Wu H, Liu X, Jaenisch R, Lodish HF. 1995. Generation of committed erythroid BFU-E and CFU-E progenitors does not require erythropoietin or the erythropoietin receptor. Cell 83:59-67.
55. Wu Y, Shang Y, Sun S, Liang H, Liu R. 2007. Erythropoietin prevents PC12 cells from 1-methyl-4-phenylpyridinium ion-induced apoptosis via the Akt/ GSK-3beta/caspase-3 mediated signaling pathway. Apoptosis 12: 1365-1375.
56. Yu X, Shacka JJ, Eells JB, Suarez-Quian C, Przygodzki RM, Beleslin-Cokic B, Lin CS, Nikodem VM, Hempstead B, Flanders KC, Costantini F, Noguchi CT. 2002. Erythropoietin receptor signalling is required for normal brain development. Development 129:505-516.