Revisiting adult neurogenesis and the role of erythropoietin for neuronal and oligodendroglial differentiation in the hippocampus

Molecular Psychiatry

Volumn 21, Issue 12, 2016, Pages 1752-1767

  Hassouna, I ^a,k   Ott, C ^a   Wustefeld L ^a   Offen, N ^b   Neher, R A ^c   Mitkovski, M ^a   Winkler, D ^a   Sperling, S ^a   Fries, L ^b   Goebbels, S ^a   Vreja, I C ^d,e   Hagemeyer, N ^a   Dittrich, M ^b   Rossetti, M F ^a   Krohnert K ^d   Hannke, K ^a   Boretius, S ^f   Zeug, A ^g   Hoschen C ^h   Dandekar, T ^b   Dere, E ^a   Neher, E ^i,j   Rizzoli, S O ^d,j   Nave, K A ^a,j   Siren A L ^b   Ehrenreich, H ^a,j   more..

^a MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

^d UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^e INTERNATIONAL MAX PLANCK RESEARCH SCHOOL FOR MOLECULAR BIOLOGY   (Germany)

^f UNIVERSITY OF KIEL   (Germany)

^g HANNOVER MEDICAL SCHOOL   (Germany)

^h TECHNICAL UNIVERSITY OF MUNICH   (Germany)

ⁱ MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^j Deutsche Forschungsgemeinschaft   (Germany)

^k Menoufia University   (Egypt)

more..

Author keywords

[No Author keywords available]

Indexed keywords

DNA; ERYTHROPOIETIN; KI 67 ANTIGEN; MICRORNA; MICRORNA124; MYELIN PROTEIN; TRANSCRIPTION FACTOR SOX9; UNCLASSIFIED DRUG; RECOMBINANT PROTEIN;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN INJURY; BRAIN REGION; CELL MATURATION; CELL PROLIFERATION; COGNITION; CONTROLLED STUDY; DNA SYNTHESIS; GENE EXPRESSION; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; IN VIVO STUDY; MALE; MOUSE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; ANIMAL; BRAIN; C57BL MOUSE; CELL DIFFERENTIATION; CENTRAL NERVOUS SYSTEM; DRUG EFFECTS; HIPPOCAMPUS; METABOLISM; NERVE CELL; PHYSIOLOGY;

ANIMALS; BRAIN; CELL DIFFERENTIATION; CENTRAL NERVOUS SYSTEM; COGNITION; ERYTHROPOIETIN; HIPPOCAMPUS; MALE; MICE; MICE, INBRED C57BL; NEUROGENESIS; NEURONS; OLIGODENDROGLIA; PYRAMIDAL CELLS; RECOMBINANT PROTEINS;

EID: 84955598616     PISSN: 13594184     EISSN: 14765578     Source Type: Journal    
DOI: 10.1038/mp.2015.212     Document Type: Article

References (69)

1. Brines M, Cerami A. Emerging biological roles for erythropoietin in the nervous system. Nat Rev Neurosci 2005; 6: 484-494
2. Sirén AL, Fasshauer T, Bartels C, Ehrenreich H. Therapeutic potential of erythropoietin and its structural or functional variants in the nervous system. Neurotherapeutics 2009; 6: 108-127
3. Ehrenreich H, Hasselblatt M, Knerlich F, von Ahsen N, Jacob S, Sperling S, et al. A hematopoietic growth factor, thrombopoietin, has a proapoptotic role in the brain. Proc Natl Acad Sci USA 2005; 102: 862-867
4. Digicaylioglu M, Bichet S, Marti HH, Wenger RH, Rivas LA, Bauer C, et al. Localization of specific erythropoietin binding sites in defined areas of the mouse brain. Proc Natl Acad Sci USA 1995; 92: 3717-3720
5. Marti HH, Wenger RH, Rivas LA, Straumann U, Digicaylioglu M, Henn V, et al. Erythropoietin gene expression in human, monkey and murine brain. Eur J Neurosci 1996; 8: 666-676
6. Ott C, Martens H, Hassouna I, Oliveira B, Erck C, Zafeiriou MP, et al. Widespread expression of erythropoietin receptor in brain and its induction by injury. Mol Med 2015 (in press
7. Adamcio B, Sargin D, Stradomska A, Medrihan L, Gertler C, Theis F, et al. Erythropoietin enhances hippocampal long-term potentiation and memory. BMC Biol 2008; 6: 37
8. Miskowiak K, O'Sullivan U, Harmer CJ. Erythropoietin enhances hippocampal response during memory retrieval in humans. J Neurosci 2007; 27: 2788-2792
9. Ehrenreich H, Fischer B, Norra C, Schellenberger F, Stender N, Stiefel M, et al. Exploring recombinant human erythropoietin in chronic progressive multiple sclerosis. Brain 2007; 130: 2577-2588
10. Wustenberg T, Begemann M, Bartels C, Gefeller O, Stawicki S, Hinze-Selch D, et al. Recombinant human erythropoietin delays loss of gray matter in chronic schizophrenia. Mol Psychiatry 2011; 16: 21
11. Miskowiak KW, Vinberg M, Macoveanu J, Ehrenreich H, Koster N, Inkster B, et al. Effects of erythropoietin on hippocampal volume and memory in mood disorders. Biol Psychiatry 2014; 78: 270-277
12. Ehrenreich H, Degner D, Meller J, Brines M, Behe M, Hasselblatt M, et al. Erythropoietin: a candidate compound for neuroprotection in schizophrenia. Mol Psychiatry 2004; 9: 42-54
13. Ehrenreich H, Hinze-Selch D, Stawicki S, Aust C, Knolle-Veentjer S, Wilms S, et al. Improvement of cognitive functions in chronic schizophrenic patients by recombinant human erythropoietin. Mol Psychiatry 2007; 12: 206-220
14. Leist M, Ghezzi P, Grasso G, Bianchi R, Villa P, Fratelli M, et al. Derivatives of erythropoietin that are tissue protective but not erythropoietic. Science 2004; 305: 239-242
15. Sargin D, El-Kordi A, Agarwal A, Muller M, Wojcik SM, Hassouna I, et al. Expression of constitutively active erythropoietin receptor in pyramidal neurons of cortex and hippocampus boosts higher cognitive functions in mice. BMC Biol 2011; 9: 27
16. Ransome MI, Turnley AM. Systemically delivered erythropoietin transiently enhances adult hippocampal neurogenesis. J Neurochem 2007; 102: 1953-1965
17. Shingo T, Sorokan ST, Shimazaki T, Weiss S. Erythropoietin regulates the in vitro and in vivo production of neuronal progenitors by mammalian forebrain neural stem cells. J Neurosci 2001; 21: 9733-9743
18. Tsai PT, Ohab JJ, Kertesz N, Groszer M, Matter C, Gao J, et al. A critical role of erythropoietin receptor in neurogenesis and post-stroke recovery. J Neurosci 2006; 26: 1269-1274
19. Leconte C, Bihel E, Lepelletier FX, Bouet V, Saulnier R, Petit E, et al. Comparison of the effects of erythropoietin and its carbamylated derivative on behaviour and hippocampal neurogenesis in mice. Neuropharmacology 2011; 60: 354-364
20. Hattangadi SM, Wong P, Zhang L, Flygare J, Lodish HF. From stem cell to red cell: regulation of erythropoiesis at multiple levels by multiple proteins, RNAs, and chromatin modifications. Blood 2011; 118: 6258-6268
21. Altman J, Das GD. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 1965; 124: 319-335
22. Aimone JB, Li Y, Lee SW, Clemenson GD, Deng W, Gage FH. Regulation and function of adult neurogenesis: from genes to cognition. Physiol Rev 2014; 94: 991-1026
23. Gould E. How widespread is adult neurogenesis in mammals? Nat Rev Neurosci 2007; 8: 481-488
24. Kaplan MS, Hinds JW. Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science 1977; 197: 1092-1094
25. Rakic P. Adult neurogenesis in mammals: an identity crisis. J Neurosci 2002; 22: 614-618
26. Hughes EG, Kang SH, Fukaya M, Bergles DE. Oligodendrocyte progenitors balance growth with self-repulsion to achieve homeostasis in the adult brain. Nat Neurosci 2013; 16: 668-676
27. Kang SH, Fukaya M, Yang JK, Rothstein JD, Bergles DE. NG2+ CNS glial progenitors remain committed to the oligodendrocyte lineage in postnatal life and following neurodegeneration. Neuron 2010; 68: 668-681
28. Morrens J, Van Den Broeck W, Kempermann G. Glial cells in adult neurogenesis. Glia 2012; 60: 159-174
29. Nishiyama A, Komitova M, Suzuki R, Zhu X. Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity. Nat Rev Neurosci 2009; 10: 9-22
30. Richardson WD, Young KM, Tripathi RB, McKenzie I. NG2-glia as multipotent neural stem cells: fact or fantasy? Neuron 2011; 70: 661-673
31. Leuner B, Gould E, Shors TJ. Is there a link between adult neurogenesis and learning? Hippocampus 2006; 16: 216-224
32. Deng W, Aimone JB, Gage FH. New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nat Rev Neurosci 2010; 11: 339-350
33. Burke SN, Barnes CA. Neural plasticity in the ageing brain. Nat Rev Neurosci 2006; 7: 30-40
34. Huang W, Zhao N, Bai X, Karram K, Trotter J, Goebbels S, et al. Novel NG2-CreERT2 knock-in mice demonstrate heterogeneous differentiation potential of NG2 glia during development. Glia 2014; 62: 896-913
35. Muzumdar MD, Tasic B, Miyamichi K, Li L, Luo L. A global double-fluorescent Cre reporter mouse. Genesis 2007; 45: 593-605
36. Breunig JJ, Arellano JI, Macklis JD, Rakic P. Everything that glitters isn't gold: a critical review of postnatal neural precursor analyses. Cell Stem Cell 2007; 1: 612-627
37. Izquierdo A, Wiedholz LM, Millstein RA, Yang RJ, Bussey TJ, Saksida LM, et al. Genetic and dopaminergic modulation of reversal learning in a touchscreenbased operant procedure for mice. Behav Brain Res 2006; 171: 181-188
38. Hagemeyer N, Boretius S, Ott C, Von Streitberg A, Welpinghus H, Sperling S, et al. Erythropoietin attenuates neurological and histological consequences of toxic demyelination in mice. Mol Med 2012; 18: 628-635
39. Keuker JI, Vollmann-Honsdorf GK, Fuchs E. How to use the optical fractionator: an example based on the estimation of neurons in the hippocampal CA1 and CA3 regions of tree shrews. Brain Res Protoc 2001; 7: 211-221
40. West MJ, Gundersen HJ. Unbiased stereological estimation of the number of neurons in the human hippocampus. J Comp Neurol 1990; 296: 1-22
41. Saka SK, Vogts A, Krohnert K, Hillion F, Rizzoli SO, Wessels JT. Correlated optical and isotopic nanoscopy. Nat Commun 2014; 5: 3664
42. Ahlenius H, Kokaia Z. Isolation and generation of neurosphere cultures from embryonic and adult mouse brain. Methods Mol Biol 2010; 633: 241-252
43. Neher RA, Mitkovski M, Kirchhoff F, Neher E, Theis FJ, Zeug A. Blind source separation techniques for the decomposition of multiply labeled fluorescence images. Biophys J 2009; 96: 3791-3800
44. Sargin D, Hassouna I, Sperling S, Sirén AL, Ehrenreich H. Uncoupling of neurodegeneration and gliosis in a murine model of juvenile cortical lesion. Glia 2009; 57: 693-702
45. Cohen J. Statistical Power Analysis for the Behavioral Sciences 2 (edn). Lawrence Erlbaum Associates: Hillsdale 1988
46. Leid M, Ishmael JE, Avram D, Shepherd D, Fraulob V, Dolle P. CTIP1 and CTIP2 are differentially expressed during mouse embryogenesis. Gene Expr Patterns 2004; 4: 733-739
47. Fidalgo C, Conejo NM, Gonzalez-Pardo H, Arias JL. Functional interaction between the dorsal hippocampus and the striatum in visual discrimination learning. J Neurosci Res 2012; 90: 715-720
48. Lee AC, Yeung LK, Barense MD. The hippocampus and visual perception. Front Hum Neurosci 2012; 6: 91
49. Reynolds BA, Rietze RL. Neural stem cells and neurospheres-re-evaluating the relationship. Nat Methods 2005; 2: 333-336
50. Conti L, Pollard SM, Gorba T, Reitano E, Toselli M, Biella G, et al. Niche-independent symmetrical self-renewal of a mammalian tissue stem cell. PLoS Biol 2005; 3: e283
51. Pasca AM, Sloan SA, Clarke LE, Tian Y, Makinson CD, Huber N, et al. Functional cortical neurons and astrocytes from human pluripotent stem cells in 3D culture. Nat Methods 2015; 12: 671-678
52. Cheng LC, Pastrana E, Tavazoie M, Doetsch F. miR-124 regulates adult neurogenesis in the subventricular zone stem cell niche. Nat Neurosci 2009; 12: 399-408
53. Scott CE, Wynn SL, Sesay A, Cruz C, Cheung M, Gomez Gaviro MV, et al. SOX9 induces and maintains neural stem cells. Nat Neurosci 2010; 13: 1181-1189
54. Papagiannakopoulos T, Kosik KS. microRNA-124: micromanager of neurogenesis. Cell Stem Cell 2009; 4: 375-376
55. Grabrucker A, Vaida B, Bockmann J, Boeckers TM. Synaptogenesis of hippocampal neurons in primary cell culture. Cell Tissue Res 2009; 338: 333-341
56. Matteoli M, Takei K, Perin MS, Sudhof TC, De Camilli P. Exo-endocytotic recycling of synaptic vesicles in developing processes of cultured hippocampal neurons. J Cell Biol 1992; 117: 849-861
57. Brines ML, Ghezzi P, Keenan S, Agnello D, de Lanerolle NC, Cerami C, et al. Erythropoietin crosses the blood-brain barrier to protect against experimental brain injury. Proc Natl Acad Sci USA 2000; 97: 10526-10531
58. Indra AK, Warot X, Brocard J, Bornert JM, Xiao JH, Chambon P, et al. Temporallycontrolled site-specific mutagenesis in the basal layer of the epidermis: comparison of the recombinase activity of the tamoxifen-inducible Cre-ER(T) and Cre-ER(T2) recombinases. Nucleic Acids Res 1999; 27: 4324-4327
59. Encinas JM, Michurina TV, Peunova N, Park JH, Tordo J, Peterson DA, et al. Divisioncoupled astrocytic differentiation and age-related depletion of neural stem cells in the adult hippocampus. Cell Stem Cell 2011; 8: 566-579
60. Cayre M, Canoll P, Goldman JE. Cell migration in the normal and pathological postnatal mammalian brain. Prog Neurobiol 2009; 88: 41-63
61. Nakatomi H, Kuriu T, Okabe S, Yamamoto S, Hatano O, Kawahara N, et al. Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors. Cell 2002; 110: 429-441
62. Schmidt W, Reymann KG. Proliferating cells differentiate into neurons in the hippocampal CA1 region of gerbils after global cerebral ischemia. Neurosci Lett 2002; 334: 153-156
63. Kronenberg G, Wang LP, Geraerts M, Babu H, Synowitz M, Vicens P, et al. Local origin and activity-dependent generation of nestin-expressing protoplasmic astrocytes in CA1. Brain Struct Funct 2007; 212: 19-35
64. Seaberg RM, van Der Kooy D. Adult rodent neurogenic regions: the ventricular subependyma contains neural stem cells, but the dentate gyrus contains restricted progenitors. J Neurosci 2002; 22: 1784-1793
65. Liu X, Wang Q, Haydar TF, Bordey A. Nonsynaptic GABA signaling in postnatal subventricular zone controls proliferation of GFAP-expressing progenitors. Nat Neurosci 2005; 8: 1179-1187
66. Kriegstein AR. GABA puts the brake on stem cells. Nat Neurosci 2005; 8: 1132-1133
67. Chen ZY, Asavaritikrai P, Prchal JT, Noguchi CT. Endogenous erythropoietin signaling is required for normal neural progenitor cell proliferation. J Biol Chem 2007; 282: 25875-25883
68. Banzhaf-Strathmann J, Benito E, May S, Arzberger T, Tahirovic S, Kretzschmar H, et al. MicroRNA-125b induces tau hyperphosphorylation and cognitive deficits in Alzheimer's disease. EMBO J 2014; 33: 1667-1680
69. Zovoilis A, Agbemenyah HY, Agis-Balboa RC, Stilling RM, Edbauer D, Rao P, et al. microRNA-34c is a novel target to treat dementias. EMBO J 2011; 30: 4299-4308