Erythropoietin: A candidate treatment for mood symptoms and memory dysfunction in depression

Psychopharmacology

Volumn 219, Issue 3, 2012, Pages 687-698

  Miskowiak, Kamilla W ^a,b   Vinberg, Maj ^a   Harmer, Catherine J ^b   Ehrenreich, Hannelore ^c   Kessing, Lars V ^a  

^a Rigshospitalet   (Denmark)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

Author keywords

Antidepressant; EPO; Erythropoietin; Hippocampus; Memory; Mood disorder

Indexed keywords

BIOLOGICAL MARKER; ERYTHROPOIETIN; PLACEBO;

ANTIDEPRESSANT ACTIVITY; ANXIETY; ATTITUDE TO MENTAL ILLNESS; COGNITIVE DEFECT; DEPRESSION; DRUG EFFECT; HEMATOCRIT; HIPPOCAMPUS; HUMAN; MEMORY; MEMORY DISORDER; MOOD CHANGE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SYSTEMATIC REVIEW; TRANQUILIZING ACTIVITY; UPREGULATION;

AFFECT; ANIMALS; CONTROLLED CLINICAL TRIALS AS TOPIC; DEPRESSION; ERYTHROPOIETIN; HUMANS; MEMORY DISORDERS; MOOD DISORDERS;

EID: 84856672725     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-011-2511-1     Document Type: Review

References (104)

1. B Adamcio D Sargin A Stradomska L Medrihan C Gertler F Theis, et al. 2008 Erythropoietin enhances hippocampal long-term potentiation and memory BMC Biol 6 37 18782446 10.1186/1741-7007-6-37
2. D Agnello P Bigini P Villa T Mennini A Cerami ML Brines, et al. 2002 Erythropoietin exerts an anti-inflammatory effect on the CNS in a model of experimental autoimmune encephalomyelitis Brain Res 952 128 134 12363412 10.1016/S0006-8993(02)03239-0 1:CAS:528:DC%2BD38XnsVSns7o%3D (Pubitemid 35279495)
3. JB Aimone J Wiles FH Gage 2006 Potential role for adult neurogenesis in the encoding of time in new memories Nat Neurosci 9 723 727 16732202 10.1038/nn1707 1:CAS:528:DC%2BD28XltVeqtLg%3D
4. RJ Baldessarini 1989 Current status of antidepressants: clinical pharmacology and therapy J Clin Psychiatry 50 117 126 2647712 1:STN:280:DyaL1M7nsVCksg%3D%3D (Pubitemid 19117705)
5. A Behnken S Schoning J Gerss C Konrad R de Jong-Meyer P Zwanzger, et al. 2010 Persistent non-verbal memory impairment in remitted major depression-caused by encoding deficits? J Affect Disord 122 144 148 19692126 10.1016/j.jad.2009. 07.010
6. RH Belmaker G Agam 2008 Mechanisms of disease: major depressive disorder N Engl J Med 358 55 68 18172175 10.1056/NEJMra073096 1:CAS:528: DC%2BD1cXisFWjsQ%3D%3D
7. O Berton EJ Nestler 2006 New approaches to antidepressant drug discovery: beyond monoamines Nat Rev Neurosci 7 137 151 16429123 10.1038/nrn1846 1:CAS:528:DC%2BD28XlvV2qug%3D%3D (Pubitemid 43151600)
8. R Bierer MC Peceny CH Hartenberger RK Ohls 2006 Erythropoietin concentrations and neurodevelopmental outcome in preterm infants Pediatrics 118 e635 e640 16908620 10.1542/peds.2005-3186 (Pubitemid 46089988)
9. E Biringer A Mykletun K Sundet R Kroken KI Stordal A Lund 2007 A longitudinal analysis of neurocognitive function in unipolar depression J Clin Exp Neuropsychol 29 879 891 17852600 10.1080/13803390601147686 (Pubitemid 350145776)
10. BO Boran A Colak M Kutlay 2005 Erythropoietin enhances neurological recovery after experimental spinal cord injury Restor Neurol Neurosci 23 341 345 16477096 1:CAS:528:DC%2BD2MXht1OmsLbN (Pubitemid 41746167)
11. E Borcel L Perez-Alvarez AI Herrero T Brionne E Varea V Berezin, et al. 2008 Chronic stress in adulthood followed by intermittent stress impairs spatial memory and the survival of newborn hippocampal cells in aging animals: prevention by FGL, a peptide mimetic of neural cell adhesion molecule Behav Pharmacol 19 41 49 18195593 10.1097/FBP.0b013e3282f3fca9
12. AL Bouhuys E Geerts MC Gordijn 1999 Depressed patients' perceptions of facial emotions in depressed and remitted states are associated with relapse: a longitudinal study J Nerv Ment Dis 187 595 602 10535652 10.1097/00005053- 199910000-00002 1:STN:280:DC%2BD3c%2FgsVeisg%3D%3D (Pubitemid 29489502)
13. BP Bradley K Mogg R Williams 1995 Implicit and explicit memory for emotion-congruent information in clinical depression and anxiety Behav Res Ther 33 755 770 7677713 10.1016/0005-7967(95)00029-W 1:STN:280:DyaK2MvgvVahug%3D%3D
14. M Brines A Cerami 2005 Emerging biological roles for erythropoietin in the nervous system Nat Rev Neurosci 6 484 494 15928718 10.1038/nrn1687 1:CAS:528:DC%2BD2MXks1Oitb8%3D (Pubitemid 40769173)
15. ML Brines P Ghezzi S Keenan D Agnello NC de Lanerolle C Cerami, et al. 2000 Erythropoietin crosses the blood-brain barrier to protect against experimental brain injury Proc Natl Acad Sci U S A 97 10526 10531 10984541 10.1073/pnas.97.19.10526 1:CAS:528:DC%2BD3cXms1Crtrk%3D
16. JC Britton SF Taylor KD Sudheimer I Liberzon 2006 Facial expressions and complex IAPS pictures: common and differential networks Neuroimage 31 906 919 16488159 10.1016/j.neuroimage.2005.12.050 (Pubitemid 43776660)
17. MS Brown D Eichorst B Lala-Black R Gonzalez 2009 Higher cumulative doses of erythropoietin and developmental outcomes in preterm infants Pediatrics 124 e681 e687 19786428 10.1542/peds.2008-2701
18. N Byts AL Siren 2009 Erythropoietin: a multimodal neuroprotective agent Exp Transl Stroke Med 1 4 20142991 10.1186/2040-7378-1-4
19. S Campbell G Macqueen 2004 The role of the hippocampus in the pathophysiology of major depression J Psychiatry Neurosci 29 417 426 15644983 (Pubitemid 40075713)
20. S Cansino P Maquet RJ Dolan MD Rugg 2002 Brain activity underlying encoding and retrieval of source memory Cereb Cortex 12 1048 1056 12217968 10.1093/cercor/12.10.1048
21. E Castilla-Ortega C Pedraza G Estivill-Torrus LJ Santin 2011 When is adult hippocampal neurogenesis necessary for learning? Evidence from animal research Rev Neurosci 22 267 283 21591906 10.1515/RNS.2011.027
22. RA Chambers MN Potenza RE Hoffman W Miranker 2004 Simulated apoptosis/neurogenesis regulates learning and memory capabilities of adaptive neural networks Neuropsychopharmacology 29 747 758 14702022 10.1038/sj.npp. 1300358 (Pubitemid 38402482)
23. G Ding Q Jiang L Li L Zhang Y Wang ZG Zhang, et al. 2010 Cerebral tissue repair and atrophy after embolic stroke in rat: a magnetic resonance imaging study of erythropoietin therapy J Neurosci Res 88 3206 3214 20722071 10.1002/jnr.22470 1:CAS:528:DC%2BC3cXhtFOqsrzK
24. WC Drevets 2003 Neuroimaging abnormalities in the amygdala in mood disorders Ann N Y Acad Sci 985 420 444 12724175 10.1111/j.1749-6632.2003. tb07098.x (Pubitemid 36521131)
25. SC Dulawa R Hen 2005 Recent advances in animal models of chronic antidepressant effects: the novelty-induced hypophagia test Neurosci Biobehav Rev 29 771 783 15890403 10.1016/j.neubiorev.2005.03.017 1:CAS:528: DC%2BD2MXltFWlu78%3D (Pubitemid 40762599)
26. RS Duman LM Monteggia 2006 A neurotrophic model for stress-related mood disorders Biol Psychiatry 59 1116 1127 16631126 10.1016/j.biopsych.2006.02.013 1:CAS:528:DC%2BD28XmtVOisbc%3D
27. RS Duman J Malberg J Thome 1999 Neural plasticity to stress and antidepressant treatment Biol Psychiatry 46 1181 1191 10560024 10.1016/S0006-3223(99)00177-8 1:CAS:528:DyaK1MXotVOktr0%3D (Pubitemid 30114436)
28. H Ehrenreich D Degner J Meller M Brines M Behe M Hasselblatt, et al. 2004 Erythropoietin: a candidate compound for neuroprotection in schizophrenia Mol Psychiatry 9 42 54 14581931 1:CAS:528:DC%2BD3sXhtVWhtr7E (Pubitemid 38175081)
29. H Ehrenreich B Fischer C Norra F Schellenberger N Stender M Stiefel, et al. 2007 Exploring recombinant human erythropoietin in chronic progressive multiple sclerosis Brain 130 2577 2588 17728357 10.1093/brain/awm203 (Pubitemid 47511714)
30. H Ehrenreich D Hinze-Selch S Stawicki C Aust S Knolle-Veentjer S Wilms, et al. 2007 Improvement of cognitive functions in chronic schizophrenic patients by recombinant human erythropoietin Mol Psychiatry 12 206 220 17033631 10.1038/sj.mp.4001907 1:CAS:528:DC%2BD2sXoslSisA%3D%3D (Pubitemid 46160985)
31. A El-Kordi K Radyushkin H Ehrenreich 2009 Erythropoietin improves operant conditioning and stability of cognitive performance in mice BMC Biol 7 37 19586522 10.1186/1741-7007-7-37
32. S Erbayraktar G Grasso A Sfacteria QW Xie T Coleman M Kreilgaard, et al. 2003 Asialoerythropoietin is a nonerythropoietic cytokine with broad neuroprotective activity in vivo Proc Natl Acad Sci U S A 100 6741 6746 12746497 10.1073/pnas.1031753100 1:CAS:528:DC%2BD3sXktlygsLY%3D (Pubitemid 36666650)
33. K Erickson W Drevets J Schulkin 2003 Glucocorticoid regulation of diverse cognitive functions in normal and pathological emotional states Neurosci Biobehav Rev 27 233 246 12788335 10.1016/S0149-7634(03)00033-2 1:CAS:528:DC%2BD3sXkt1Giu7c%3D (Pubitemid 36677431)
34. Eriksson TM, Delagrange P, Spedding M, Popoli M, Mathe AA, Ogren SO et al (2011) Emotional memory impairments in a genetic rat model of depression: involvement of 5-HT/MEK/Arc signaling in restoration. Mol Psychiatry
35. JC Garcia-Rodriguez I Sosa-Teste 2009 The nasal route as a potential pathway for delivery of erythropoietin in the treatment of acute ischemic stroke in humans Sci World J 9 970 981 10.1100/tsw.2009.103
36. S Genc Z Zadeoglulari MG Oner K Genc M Digicaylioglu 2011 Intranasal erythropoietin therapy in nervous system disorders Expert Opin Drug Deliv 8 19 32 21143002 10.1517/17425247.2011.540236 1:CAS:528:DC%2BC3cXhs1Srt7nN
37. P Giacobbe HS Mayberg AM Lozano 2009 Treatment resistant depression as a failure of brain homeostatic mechanisms: implications for deep brain stimulation Exp Neurol 219 44 52 19426730 10.1016/j.expneurol.2009.04.028
38. MJ Girgenti J Hunsberger CH Duman M Sathyanesan R Terwilliger SS Newton 2009 Erythropoietin induction by electroconvulsive seizure, gene regulation, and antidepressant-like behavioral effects Biol Psychiatry 66 267 274 19185286 10.1016/j.biopsych.2008.12.005 1:CAS:528:DC%2BD1MXotF2nsr4%3D
39. JP Hamilton IH Gotlib 2008 Neural substrates of increased memory sensitivity for negative stimuli in major depression Biol Psychiatry 63 1155 1162 18281017 10.1016/j.biopsych.2007.12.015
40. AR Hariri TE Goldberg VS Mattay BS Kolachana JH Callicott MF Egan, et al. 2003 Brain-derived neurotrophic factor val66met polymorphism affects human memory-related hippocampal activity and predicts memory performance J Neurosci 23 6690 6694 12890761 1:CAS:528:DC%2BD3sXmtFensbg%3D (Pubitemid 36951196)
41. CJ Harmer 2010 Antidepressant drug action: a neuropsychological perspective Depress Anxiety 27 231 233 20196098 10.1002/da.20680
42. CJ Harmer Z Bhagwagar DI Perrett BA Vollm PJ Cowen GM Goodwin 2003 Acute SSRI administration affects the processing of social cues in healthy volunteers Neuropsychopharmacology 28 148 152 12496951 10.1038/sj.npp.1300004 1:CAS:528:DC%2BD3sXhtlWitrk%3D
43. CJ Harmer NC Shelley PJ Cowen GM Goodwin 2004 Increased positive versus negative affective perception and memory in healthy volunteers following selective serotonin and norepinephrine reuptake inhibition Am J Psychiatry 161 1256 1263 15229059 10.1176/appi.ajp.161.7.1256 (Pubitemid 38859176)
44. CJ Harmer CE Mackay CB Reid PJ Cowen GM Goodwin 2006 Antidepressant drug treatment modifies the neural processing of nonconscious threat cues Biol Psychiatry 59 816 820 16460693 10.1016/j.biopsych.2005.10.015 1:CAS:528:DC%2BD28XjsFOnt7w%3D
45. Harmer CJ, Cowen PJ, Goodwin GM (2010) Efficacy markers in depression. J Psychopharmacol
46. Hasselbalch J, Hasselbalch SG, Gade A, Knorr UB, Kessing LV (2010) Cognitive function in the remitted state of unipolar disorder and the association with the course of illness. In.
47. J Herbert 2008 Neurogenesis and depression: breakthrough or blind alley? J Neuroendocrinol 20 413 414 18194427 10.1111/j.1365-2826.2008.01649.x 1:CAS:528:DC%2BD1cXjt1Crtbg%3D (Pubitemid 351280105)
48. Jacobson LO, Goldwasser E, Fried W, Plzak LF (1957) Studies on erythropoiesis. VII. The role of the kidney in the production of erythropoietin. In. pp 305-317.
49. W Jelkmann 1992 Erythropoietin: structure, control of production, and function Physiol Rev 72 449 489 1557429 1:CAS:528:DyaK38XisVylsro%3D
50. W Jelkmann J Bohlius M Hallek AJ Sytkowski 2008 The erythropoietin receptor in normal and cancer tissues Crit Rev Oncol Hematol 67 39 61 18434185 10.1016/j.critrevonc.2008.03.006
51. LV Kessing 1998 Cognitive impairment in the euthymic phase of affective disorder Psychol Med 28 1027 1038 9794010 10.1017/S0033291798006862 1:STN:280:DyaK1M%2FhtVChtw%3D%3D (Pubitemid 28458459)
52. E Kitraki O Kremmyda D Youlatos M Alexis C Kittas 2004 Spatial performance and corticosteroid receptor status in the 21-day restraint stress paradigm Ann N Y Acad Sci 1018 323 327 15240385 10.1196/annals.1296.039 1:CAS:528:DC%2BD2cXms12ntb8%3D (Pubitemid 38951423)
53. A Kumral E Ozer O Yilmaz M Akhisaroglu N Gokmen N Duman, et al. 2003 Neuroprotective effect of erythropoietin on hypoxic-ischemic brain injury in neonatal rats Biol Neonate 83 224 228 12660442 10.1159/000068926 1:CAS:528:DC%2BD3sXitl2iur4%3D (Pubitemid 36351232)
54. Lang PJ, Bradley MM, Cuthbert BN (1997) International Affective Picture System (IAPS): technical manual and affective ratings. In: NIMH Center for the Study of Emotion and Attention. University of Florida, Gainesville FL
55. C Leconte E Bihel FX Lepelletier V Bouet R Saulnier E Petit, et al. 2011 Comparison of the effects of erythropoietin and its carbamylated derivative on behaviour and hippocampal neurogenesis in mice Neuropharmacology 60 354 364 20932982 10.1016/j.neuropharm.2010.09.025 1:CAS:528:DC%2BC3MXhtlemug%3D%3D
56. M Leist P Ghezzi G Grasso R Bianchi P Villa M Fratelli, et al. 2004 Derivatives of erythropoietin that are tissue protective but not erythropoietic Science 305 239 242 15247477 10.1126/science.1098313 1:CAS:528: DC%2BD2cXlsV2gsbo%3D (Pubitemid 38886736)
57. A Lembke TA Ketter 2002 Impaired recognition of facial emotion in mania Am J Psychiatry 159 302 304 11823275 10.1176/appi.ajp.159.2.302 (Pubitemid 34126910)
58. W Li Y Maeda RR Yuan S Elkabes S Cook P Dowling 2004 Beneficial effect of erythropoietin on experimental allergic encephalomyelitis Ann Neurol 56 767 777 15562412 10.1002/ana.20274 1:CAS:528:DC%2BD2MXit1ChtA%3D%3D (Pubitemid 39578439)
59. Lupien SJ, de LM, de SS, Convit A, Tarshish C, Nair NP et al (1998) Cortisol levels during human aging predict hippocampal atrophy and memory deficits. Nat Neurosci 1:69-73 (Pubitemid 128652645)
60. HK Manji GJ Moore G Rajkowska G Chen 2000 Neuroplasticity and cellular resilience in mood disorders Mol Psychiatry 5 578 593 11126389 10.1038/sj.mp.4000811 1:CAS:528:DC%2BD3cXosFSgsrk%3D
61. Manji HK, Quiroz JA, Sporn J, Payne JL, Denicoff K, A Gray N et al (2003) Enhancing neuronal plasticity and cellular resilience to develop novel, improved therapeutics for difficult-to-treat depression. Biol Psychiatry 53:707-742 (Pubitemid 39658487)
62. Marti HH, Wenger RH, Rivas LA, Straumann U, Digicaylioglu M, Henn V, et al (1996) Erythropoietin gene expression in human, monkey and murine brain. Eur J Neurosci. 8(4):666-676 (Pubitemid 26114611)
63. A Martinez-Aran E Vieta F Colom C Torrent J Sanchez-Moreno M Reinares, et al. 2004 Cognitive impairment in euthymic bipolar patients: implications for clinical and functional outcome Bipolar Disord 6 224 232 15117401 10.1111/j.1399-5618.2004.00111.x 1:STN:280:DC%2BD2c3lslyksg%3D%3D (Pubitemid 38702298)
64. BS McEwen 2005 Glucocorticoids, depression, and mood disorders: structural remodeling in the brain Metabolism 54 20 23 15877308 10.1016/j.metabol.2005.01.008 1:CAS:528:DC%2BD2MXjsVers7o%3D (Pubitemid 40546018)
65. JW Meyer KH Eichhorn K Vetter S Christen E Schleusner A Klos, et al. 1995 Does recombinant human erythropoietin not only treat anemia but reduce postpartum (emotional) distress as well? J Perinat Med 23 99 109 7658328 10.1515/jpme.1995.23.1-2.99 1:STN:280:DyaK2Mzoslanug%3D%3D
66. AH Miller V Maletic CL Raison 2009 Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression Biol Psychiatry 65 732 741 19150053 10.1016/j.biopsych.2008.11.029 1:CAS:528:DC%2BD1MXktV2qsb0%3D
67. K Miskowiak B Inkster S Selvaraj G Goodwin C Harmer 2007 Erythropoietin has no effect on hippocampal response during memory retrieval 3 days post-administration Psychopharmacology (Berl) 195 451 453 10.1007/s00213-007- 0907-8 1:CAS:528:DC%2BD2sXhtlWktbzN (Pubitemid 350160271)
68. K Miskowiak U O'Sullivan CJ Harmer 2007 Erythropoietin enhances hippocampal response during memory retrieval in humans J Neurosci 27 2788 2792 17360900 10.1523/JNEUROSCI.5013-06.2007 1:CAS:528:DC%2BD2sXjs1Wqurg%3D (Pubitemid 46438961)
69. K Miskowiak U O'Sullivan CJ Harmer 2007 Erythropoietin reduces neural and cognitive processing of fear in human models of antidepressant drug action Biol Psychiatry 62 1244 1250 17553466 10.1016/j.biopsych.2007.01.011 1:CAS:528:DC%2BD2sXht1ymu7jL (Pubitemid 350060886)
70. K Miskowiak B Inkster U O'Sullivan S Selvaraj GM Goodwin CJ Harmer 2008 Differential effects of erythropoietin on neural and cognitive measures of executive function 3 and 7 days post-administration Exp Brain Res 184 313 321 17828390 10.1007/s00221-007-1102-1 1:CAS:528:DC%2BD2sXhsVaqtL7M (Pubitemid 350275880)
71. K Miskowiak B Inkster S Selvaraj R Wise GM Goodwin CJ Harmer 2008 Erythropoietin improves mood and modulates the cognitive and neural processing of emotion 3 days post administration Neuropsychopharmacology 33 611 618 17473836 10.1038/sj.npp.1301439 1:CAS:528:DC%2BD1cXmsFSlsg%3D%3D
72. KW Miskowiak E Favaron S Hafizi B Inkster GM Goodwin PJ Cowen, et al. 2009 Effects of erythropoietin on emotional processing biases in patients with major depression: an exploratory fMRI study Psychopharmacology (Berl) 207 133 142 10.1007/s00213-009-1641-1 1:CAS:528:DC%2BD1MXhtVegtrzJ
73. KW Miskowiak E Favaron S Hafizi B Inkster GM Goodwin PJ Cowen, et al. 2010 Erythropoietin modulates neural and cognitive processing of emotional information in biomarker models of antidepressant drug action in depressed patients Psychopharmacology (Berl) 210 419 428 10.1007/s00213-010-1842-7 1:CAS:528:DC%2BC3cXkvVGnsLw%3D
74. KW Miskowiak M Vinberg CJ Harmer H Ehrenreich GM Knudsen J Macoveanu, et al. 2010 Effects of erythropoietin on depressive symptoms and neurocognitive deficits in depression and bipolar disorder Trials 11 97 20942940 10.1186/1745-6215-11-97
75. AC Miu AI Olteanu I Chis RM Heilman 2004 Have no fear, erythropoietin is here: erythropoietin protects fear conditioning performances after functional inactivation of the amygdala Behav Brain Res 155 223 229 15364481 10.1016/j.bbr.2004.04.019 1:CAS:528:DC%2BD2cXnsFSrtrY%3D (Pubitemid 39208904)
76. J Mogensen K Miskowiak TA Sorensen CT Lind NV Olsen JB Springborg, et al. 2004 Erythropoietin improves place learning in fimbria-fornix-transected rats and modifies the search pattern of normal rats Pharmacol Biochem Behav 77 381 390 14751468 10.1016/j.pbb.2003.11.017 1:CAS:528:DC%2BD2cXnvVOhtA%3D%3D (Pubitemid 38125172)
77. E Morishita S Masuda M Nagao Y Yasuda R Sasaki 1997 Erythropoietin receptor is expressed in rat hippocampal and cerebral cortical neurons, and erythropoietin prevents in vitro glutamate-induced neuronal death Neuroscience 76 105 116 8971763 10.1016/S0306-4522(96)00306-5 1:CAS:528:DyaK28Xns1Wqu70%3D (Pubitemid 26407940)
78. S Moussavi S Chatterji E Verdes A Tandon V Patel B Ustun 2007 Depression, chronic diseases, and decrements in health: results from the World Health Surveys Lancet 370 851 858 17826170 10.1016/S0140-6736(07)61415-9 (Pubitemid 47362344)
79. AP Neubauer W Voss M Wachtendorf T Jungmann 2010 Erythropoietin improves neurodevelopmental outcome of extremely preterm infants Ann Neurol 67 657 666 20437563 1:CAS:528:DC%2BC3cXmvF2lsrg%3D
80. S Paradiso GJ Lamberty MJ Garvey RG Robinson 1997 Cognitive impairment in the euthymic phase of chronic unipolar depression J Nerv Ment Dis 185 748 754 9442186 10.1097/00005053-199712000-00005 1:STN:280:DyaK1c7gsVaitw%3D%3D (Pubitemid 28050033)
81. JL Pickett DC Theberge WS Brown SU Schweitzer AR Nissenson 1999 Normalizing hematocrit in dialysis patients improves brain function Am J Kidney Dis 33 1122 1130 10352201 10.1016/S0272-6386(99)70150-2 1:STN:280: DyaK1M3ot1Wntg%3D%3D (Pubitemid 29252683)
82. G Pourtois S Schwartz ML Seghier F Lazeyras P Vuilleumier 2006 Neural systems for orienting attention to the location of threat signals: an event-related fMRI study Neuroimage 31 920 933 16487729 10.1016/j.neuroimage. 2005.12.034 (Pubitemid 43792469)
83. M Preiss H Kucerova J Lukavsky H Stepankova P Sos R Kawaciukova 2009 Cognitive deficits in the euthymic phase of unipolar depression Psychiatry Res 169 235 239 19765829 10.1016/j.psychres.2008.06.042
84. MI Ransome AM Turnley 2007 Systemically delivered erythropoietin transiently enhances adult hippocampal neurogenesis J Neurochem 102 1953 1965 17555554 10.1111/j.1471-4159.2007.04684.x 1:CAS:528:DC%2BD2sXhtVyksLfF (Pubitemid 47329277)
85. S Reppermund J Zihl S Lucae S Horstmann S Kloiber F Holsboer, et al. 2007 Persistent cognitive impairment in depression: the role of psychopathology and altered hypothalamic-pituitary-adrenocortical (HPA) system regulation Biol Psychiatry 62 400 406 17188252 10.1016/j.biopsych.2006.09.027 1:CAS:528:DC%2BD2sXpsFGlsrs%3D (Pubitemid 47284019)
86. M Sakanaka TC Wen S Matsuda S Masuda E Morishita M Nagao, et al. 1998 In vivo evidence that erythropoietin protects neurons from ischemic damage Proc Natl Acad Sci U S A 95 4635 4640 9539790 10.1073/pnas.95.8.4635 1:CAS:528:DyaK1cXis1Ogsbo%3D (Pubitemid 28207965)
87. L Santarelli M Saxe C Gross A Surget F Battaglia S Dulawa, et al. 2003 Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants Science 301 805 809 12907793 10.1126/science.1083328 1:CAS:528:DC%2BD3sXmtVGqsrY%3D (Pubitemid 36962615)
88. D Sargin I Hassouna S Sperling AL Siren H Ehrenreich 2009 Uncoupling of neurodegeneration and gliosis in a murine model of juvenile cortical lesion Glia 57 693 702 18985736 10.1002/glia.20797
89. D Sargin H Friedrichs A El-Kordi H Ehrenreich 2010 Erythropoietin as neuroprotective and neuroregenerative treatment strategy: comprehensive overview of 12 years of preclinical and clinical research Best Pract Res Clin Anaesthesiol 24 573 594 21619868 10.1016/j.bpa.2010.10.005 1:CAS:528: DC%2BC3cXhsVyhtLvF
90. D Sargin A El-Kordi A Agarwal M Muller SM Wojcik I Hassouna, et al. 2011 Expression of constitutively active erythropoietin receptor in pyramidal neurons of cortex and hippocampus boosts higher cognitive functions in mice BMC Biol 9 27 21527022 10.1186/1741-7007-9-27 1:CAS:528:DC%2BC3MXlsl2ns7c%3D
91. MB Sattler D Merkler K Maier C Stadelmann H Ehrenreich M Bahr, et al. 2004 Neuroprotective effects and intracellular signaling pathways of erythropoietin in a rat model of multiple sclerosis Cell Death Differ 11 Suppl 2 S181 S192 15459752 10.1038/sj.cdd.4401504
92. LI Sinclair DM Christmas SD Hood JP Potokar A Robertson A Isaac, et al. 2009 Antidepressant-induced jitteriness/anxiety syndrome: systematic review Br J Psychiatry 194 483 490 19478285 10.1192/bjp.bp.107.048371
93. AL Siren K Radyushkin S Boretius D Kammer CC Riechers O Natt, et al. 2006 Global brain atrophy after unilateral parietal lesion and its prevention by erythropoietin Brain 129 480 489 16339796 10.1093/brain/awh703 (Pubitemid 43164370)
94. AL Siren T Fasshauer C Bartels H Ehrenreich 2009 Therapeutic potential of erythropoietin and its structural or functional variants in the nervous system Neurotherapeutics 6 108 127 19110203 10.1016/j.nurt.2008.10.041 1:CAS:528:DC%2BD1MXnsF2ntbs%3D
95. DJ Smith WJ Muir DH Blackwood 2006 Neurocognitive impairment in euthymic young adults with bipolar spectrum disorder and recurrent major depressive disorder Bipolar Disord 8 40 46 16411979 10.1111/j.1399-5618.2006.00275.x (Pubitemid 43356019)
96. LO Stratton CA Gibson KG Kolar AJ Kastin 1976 Neonatal treatment with TRH affects development, learning, and emotionality in the rat Pharmacol Biochem Behav 5 65 67 827750 10.1016/0091-3057(76)90330-0 1:STN:280:DyaE2s7gtlSjsQ%3D%3D
97. B Viviani S Bartesaghi E Corsini P Villa P Ghezzi A Garau, et al. 2005 Erythropoietin protects primary hippocampal neurons increasing the expression of brain-derived neurotrophic factor J Neurochem 93 412 421 15816864 10.1111/j.1471-4159.2005.03033.x 1:CAS:528:DC%2BD2MXjslajsr4%3D (Pubitemid 40547498)
98. L Wang Z Zhang Y Wang R Zhang M Chopp 2004 Treatment of stroke with erythropoietin enhances neurogenesis and angiogenesis and improves neurological function in rats Stroke 35 1732 1737 15178821 10.1161/01.STR.0000132196.49028.a4 1:CAS:528:DC%2BD2cXltVOjurc%3D (Pubitemid 38823656)
99. P Weiland-Fiedler K Erickson T Waldeck DA Luckenbaugh D Pike O Bonne, et al. 2004 Evidence for continuing neuropsychological impairments in depression J Affect Disord 82 253 258 15488254 10.1016/j.jad.2003.10.009 (Pubitemid 39370827)
100. T Wustenberg M Begemann C Bartels O Gefeller S Stawicki D Hinze-Selch, et al. 2011 Recombinant human erythropoietin delays loss of gray matter in chronic schizophrenia Mol Psychiatry 16 26-36 1 10.1038/mp.2010.126
101. I Yatsiv N Grigoriadis C Simeonidou PF Stahel OI Schmidt AG Alexandrovitch, et al. 2005 Erythropoietin is neuroprotective, improves functional recovery, and reduces neuronal apoptosis and inflammation in a rodent model of experimental closed head injury FASEB J 19 1701 1703 16099948 1:CAS:528:DC%2BD2MXhtFSjsbrN (Pubitemid 41429535)
102. U Yis SH Kurul A Kumral K Tugyan S Cilaker O Yilmaz, et al. 2008 Effect of erythropoietin on oxygen-induced brain injury in the newborn rat Neurosci Lett 448 245 249 18973793 10.1016/j.neulet.2008.10.060 1:CAS:528: DC%2BD1cXhsVWnurzL
103. YP Yu QQ Xu Q Zhang WP Zhang LH Zhang EQ Wei 2005 Intranasal recombinant human erythropoietin protects rats against focal cerebral ischemia Neurosci Lett 387 5 10 16054296 10.1016/j.neulet.2005.07.008 1:CAS:528:DC%2BD2MXns1Wmtb8%3D (Pubitemid 41138199)
104. J Yun H Koike D Ibi E Toth H Mizoguchi A Nitta, et al. 2010 Chronic restraint stress impairs neurogenesis and hippocampus-dependent fear memory in mice: possible involvement of a brain-specific transcription factor Npas4 J Neurochem 114 1840 1851 20626564 10.1111/j.1471-4159.2010.06893.x 1:CAS:528:DC%2BC3cXhtFyksr%2FJ