Received date: 31 Jan 2013
Accepted date: 28 Mar 2013
Published date: 01 Jun 2013
Copyright
New neurons are generated throughout life in distinct areas of the mammalian brain. This process, called adult neurogenesis, has challenged previously held concepts about adult brain plasticity and opened novel therapeutic avenues to treat certain neuro-psychiatric diseases. Here, we review the current knowledge regarding the fate and potency of neural stem cells (NSCs), as well as the mechanisms underlying neuronal differentiation and subsequent integration. Furthermore, we discuss the functional significance of adult neurogenesis in health and disease, and offer brief insight into the future directions of the adult neurogenesis field.
Key words： adult neurogenesis; hippocampus; stem cell; memory; neuropsychiatric disease
Simon M.G. BRAUN , Sebastian JESSBERGER . Adult neurogenesis in the mammalian brain[J]. Frontiers in Biology, 2013 , 8(3) : 295 -304 . DOI: 10.1007/s11515-013-1263-1
| 1 |
Ables J L, Decarolis N A, Johnson M A, Rivera P D, Gao Z, Cooper D C, Radtke F, Hsieh J, Eisch A J (2010). Notch1 is required for maintenance of the reservoir of adult hippocampal stem cells. J Neurosci, 30(31): 10484-10492
|
| 2 |
Abramson S, Miller R G, Phillips R A (1977). The identification in adult bone marrow of pluripotent and restricted stem cells of the myeloid and lymphoid systems. J Exp Med, 145(6): 1567-1579
|
| 3 |
Aimone J B, Deng W, Gage F H (2011). Resolving new memories: a critical look at the dentate gyrus, adult neurogenesis, and pattern separation. Neuron, 70(4): 589-596
|
| 4 |
Altman J (1962). Are new neurons formed in the brains of adult mammals? Science, 135(3509): 1127-1128
|
| 5 |
Amaral D G, Scharfman H E, Lavenex P (2007). The dentate gyrus: fundamental neuroanatomical organization (dentate gyrus for dummies). Prog Brain Res, 163: 3-22
|
| 6 |
Arruda-Carvalho M, Sakaguchi M, Akers K G, Josselyn S A, Frankland P W (2011). Posttraining ablation of adult-generated neurons degrades previously acquired memories. J Neurosci, 31(42): 15113-15127
|
| 7 |
Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O (2002). Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med, 8(9): 963-970
|
| 8 |
Bonaguidi M A, Wheeler M A, Shapiro J S, Stadel R P, Sun G J, Ming G L, Song H (2011). In vivo clonal analysis reveals self-renewing and multipotent adult neural stem cell characteristics. Cell, 145(7): 1142-1155
|
| 9 |
Bracko O, Singer T, Aigner S, Knobloch M, Winner B, Ray J, Clemenson G D Jr, Suh H, Couillard-Despres S, Aigner L, Gage F H, Jessberger S (2012). Gene expression profiling of neural stem cells and their neuronal progeny reveals IGF2 as a regulator of adult hippocampal neurogenesis. J Neurosci, 32(10): 3376-3387
|
| 10 |
Brill M S, Ninkovic J, Winpenny E, Hodge R D, Ozen I, Yang R, Lepier A, Gascón S, Erdelyi F, Szabo G, Parras C, Guillemot F, Frotscher M, Berninger B, Hevner R F, Raineteau O, Götz M (2009). Adult generation of glutamatergic olfactory bulb interneurons. Nat Neurosci, 12(12): 1524-1533
|
| 11 |
Carleton A, Petreanu L T, Lansford R, Alvarez-Buylla A, Lledo P M (2003). Becoming a new neuron in the adult olfactory bulb. Nat Neurosci, 6(5): 507-518
|
| 12 |
Chen D Y, Stern S A, Garcia-Osta A, Saunier-Rebori B, Pollonini G, Bambah-Mukku D, Blitzer R D, Alberini C M (2011). A critical role for IGF-II in memory consolidation and enhancement. Nature, 469(7331): 491-497
|
| 13 |
Clelland C D, Choi M, Romberg C, Clemenson G D Jr, Fragniere A, Tyers P, Jessberger S, Saksida L M, Barker R A, Gage F H, Bussey T J (2009). A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science, 325(5937): 210-213
|
| 14 |
del Rio J A, Soriano E (1989). Immunocytochemical detection of 5′-bromodeoxyuridine incorporation in the central nervous system of the mouse. Brain Res Dev Brain Res, 49(2): 311-317
|
| 15 |
Deng W, Aimone J B, Gage F H (2010). New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nat Rev Neurosci, 11(5): 339-350
|
| 16 |
Deng W, Saxe M D, Gallina I S, Gage F H (2009). Adult-born hippocampal dentate granule cells undergoing maturation modulate learning and memory in the brain. J Neurosci, 29(43): 13532-13542
|
| 17 |
Doetsch F, Caillé I, Lim D A, García-Verdugo J M, Alvarez-Buylla A (1999). Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell, 97(6): 703-716
|
| 18 |
Duan X, Chang J H, Ge S, Faulkner R L, Kim J Y, Kitabatake Y, Liu X B, Yang C H, Jordan J D, Ma D K, Liu C Y, Ganesan S, Cheng H J, Ming G L, Lu B, Song H (2007). Disrupted-In-Schizophrenia 1 regulates integration of newly generated neurons in the adult brain. Cell, 130(6): 1146-1158
|
| 19 |
Ehm O, Göritz C, Covic M, Schäffner I, Schwarz T J, Karaca E, Kempkes B, Kremmer E, Pfrieger F W, Espinosa L, Bigas A, Giachino C, Taylor V, Frisén J, Lie D C (2010). RBPJkappa-dependent signaling is essential for long-term maintenance of neural stem cells in the adult hippocampus. J Neurosci, 30(41): 13794-13807
|
| 20 |
Encinas J M, Michurina T V, Peunova N, Park J H, Tordo J, Peterson D A, Fishell G, Koulakov A, Enikolopov G (2011). Division-coupled astrocytic differentiation and age-related depletion of neural stem cells in the adult hippocampus. Cell Stem Cell, 8(5): 566-579
|
| 21 |
Erickson K I, Voss M W, Prakash R S, Basak C, Szabo A, Chaddock L, Kim J S, Heo S, Alves H, White S M, Wojcicki T R, Mailey E, Vieira V J, Martin S A, Pence B D, Woods J A, McAuley E, Kramer A F (2011). Exercise training increases size of hippocampus and improves memory. Proc Natl Acad Sci USA, 108(7): 3017-3022
|
| 22 |
Eriksson P S, Perfilieva E, Björk-Eriksson T, Alborn A M, Nordborg C, Peterson D A, Gage F H (1998). Neurogenesis in the adult human hippocampus. Nat Med, 4(11): 1313-1317
|
| 23 |
Favaro R, Valotta M, Ferri A L M, Latorre E, Mariani J, Giachino C, Lancini C, Tosetti V, Ottolenghi S, Taylor V, Nicolis S K (2009). Hippocampal development and neural stem cell maintenance require Sox2-dependent regulation of Shh. Nat Neurosci, 12(10): 1248-1256
|
| 24 |
Fenno L, Yizhar O, Deisseroth K (2011). The development and application of optogenetics. Annu Rev Neurosci, 34(1): 389-412
|
| 25 |
Gage F H (2000). Mammalian neural stem cells. Science, 287(5457): 1433-1438
|
| 26 |
Gao Z, Ure K, Ables J L, Lagace D C, Nave K A, Goebbels S, Eisch A J, Hsieh J (2009). Neurod1 is essential for the survival and maturation of adult-born neurons. Nat Neurosci, 12(9): 1090-1092
|
| 27 |
Ge S, Yang C H, Hsu K S, Ming G L, Song H (2007). A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron, 54(4): 559-566
|
| 28 |
Gu Y, Arruda-Carvalho M, Wang J, Janoschka S R, Josselyn S A, Frankland P W, Ge S (2012). Optical controlling reveals time-dependent roles for adult-born dentate granule cells. Nat Neurosci, 15(12): 1700-1706
|
| 29 |
Hall P A, Watt F M (1989). Stem cells: the generation and maintenance of cellular diversity. Development, 106(4): 619-633
|
| 30 |
Imayoshi I, Sakamoto M, Ohtsuka T, Takao K, Miyakawa T, Yamaguchi M, Mori K, Ikeda T, Itohara S, Kageyama R (2008). Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat Neurosci, 11(10): 1153-1161
|
| 31 |
Jablonska B, Aguirre A, Raymond M, Szabo G, Kitabatake Y, Sailor K A, Ming G L, Song H, Gallo V (2010). Chordin-induced lineage plasticity of adult SVZ neuroblasts after demyelination. Nat Neurosci, 13(5): 541-550
|
| 32 |
Jang M H, Bonaguidi M A, Kitabatake Y, Sun J, Song J, Kang E, Jun H, Zhong C, Su Y, Guo J U, Wang M X, Sailor K A, Kim J Y, Gao Y, Christian K M, Ming G L, Song H (2013). Secreted frizzled-related protein 3 regulates activity-dependent adult hippocampal neurogenesis. Cell Stem Cell, 12(2): 215-223
|
| 33 |
Jessberger S, Aigner S, Clemenson G D Jr, Toni N, Lie D C, Karalay O, Overall R, Kempermann G, Gage F H (2008). Cdk5 regulates accurate maturation of newborn granule cells in the adult hippocampus. PLoS Biol, 6(11): e272
|
| 34 |
Jessberger S, Nakashima K, Clemenson G D Jr, Mejia E, Mathews E, Ure K, Ogawa S, Sinton C M, Gage F H, Hsieh J (2007a). Epigenetic modulation of seizure-induced neurogenesis and cognitive decline. J Neurosci, 27(22): 5967-5975
|
| 35 |
Jessberger S, Zhao C, Toni N, Clemenson G D Jr, Li Y, Gage F H (2007b). Seizure-associated, aberrant neurogenesis in adult rats characterized with retrovirus-mediated cell labeling. J Neurosci, 27(35): 9400-9407
|
| 36 |
Jin K, Zhu Y, Sun Y, Mao X O, Xie L, Greenberg D A (2002). Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc Natl Acad Sci USA, 99(18): 11946-11950
|
| 37 |
Karalay O, Doberauer K, Vadodaria K C, Knobloch M, Berti L, Miquelajauregui A, Schwark M, Jagasia R, Taketo M M, Tarabykin V, Lie D C, Jessberger S (2011). Prospero-related homeobox 1 gene (Prox1) is regulated by canonical Wnt signaling and has a stage-specific role in adult hippocampal neurogenesis. Proc Natl Acad Sci USA, 108(14): 5807-5812
|
| 38 |
Kempermann G, Kuhn H G, Gage F H (1997). More hippocampal neurons in adult mice living in an enriched environment. Nature, 386(6624): 493-495
|
| 39 |
Knobloch M, Braun S M G, Zurkirchen L, von Schoultz C, Zamboni N, Araúzo-Bravo M J, Kovacs W J, Karalay O, Suter U, Machado R A, Roccio M, Lutolf M P, Semenkovich C F, Jessberger S (2013). Metabolic control of adult neural stem cell activity by Fasn-dependent lipogenesis. Nature, 493(7431): 226-230
|
| 40 |
Knoth R, Singec I, Ditter M, Pantazis G, Capetian P, Meyer R P, Horvat V, Volk B, Kempermann G (2010). Murine features of neurogenesis in the human hippocampus across the lifespan from 0 to 100 years. PLoS ONE, 5(1): e8809
|
| 41 |
Kuhn H G, Dickinson-Anson H, Gage F H (1996). Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci, 16(6): 2027-2033
|
| 42 |
Lavado A, Lagutin O V, Chow L M L, Baker S J, Oliver G (2010). Prox1 is required for granule cell maturation and intermediate progenitor maintenance during brain neurogenesis. PLoS Biol, 8(8): 8
|
| 43 |
Lazarini F, Lledo P M (2011). Is adult neurogenesis essential for olfaction? Trends Neurosci, 34(1): 20-30
|
| 44 |
Lazic S E, Grote H, Armstrong R J E, Blakemore C, Hannan A J, van Dellen A, Barker R A (2004). Decreased hippocampal cell proliferation in R6/1 Huntington’s mice. Neuroreport, 15(5): 811-813
|
| 45 |
Lie D C, Colamarino S A, Song H J, Désiré L, Mira H, Consiglio A, Lein E S, Jessberger S, Lansford H, Dearie A R, Gage F H (2005). Wnt signalling regulates adult hippocampal neurogenesis. Nature, 437(7063): 1370-1375
|
| 46 |
Lois C, Alvarez-Buylla A (1994). Long-distance neuronal migration in the adult mammalian brain. Science, 264(5162): 1145-1148
|
| 47 |
Lois C, García-Verdugo J M, Alvarez-Buylla A (1996). Chain migration of neuronal precursors. Science, 271(5251): 978-981
|
| 48 |
Lugert S, Basak O, Knuckles P, Haussler U, Fabel K, Götz M, Haas C A, Kempermann G, Taylor V, Giachino C (2010). Quiescent and active hippocampal neural stem cells with distinct morphologies respond selectively to physiological and pathological stimuli and aging. Cell Stem Cell, 6(5): 445-456
|
| 49 |
Malberg J E, Eisch A J, Nestler E J, Duman R S (2000). Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci, 20(24): 9104-9110
|
| 50 |
Marín-Burgin A, Mongiat L A, Pardi M B, Schinder A F (2012). Unique processing during a period of high excitation/inhibition balance in adult-born neurons. Science, 335(6073): 1238-1242
|
| 51 |
Milner B, Squire L R, Kandel E R (1998). Cognitive neuroscience and the study of memory. Neuron, 20(3): 445-468
|
| 52 |
Mira H, Andreu Z, Suh H, Lie D C, Jessberger S, Consiglio A, San Emeterio J, Hortigüela R, Marqués-Torrejón M A, Nakashima K, Colak D, Götz M, Fariñas I, Gage F H (2010). Signaling through BMPR-IA regulates quiescence and long-term activity of neural stem cells in the adult hippocampus. Cell Stem Cell, 7(1): 78-89
|
| 53 |
Morrens J, Van Den Broeck W, Kempermann G (2012). Glial cells in adult neurogenesis. Glia, 60(2): 159-174
|
| 54 |
Morrison S J, Shah N M, Anderson D J (1997). Regulatory mechanisms in stem cell biology. Cell, 88(3): 287-298
|
| 55 |
Nakada D, Saunders T L, Morrison S J (2010). Lkb1 regulates cell cycle and energy metabolism in haematopoietic stem cells. Nature, 468(7324): 653-658
|
| 56 |
Nissant A, Pallotto M (2011). Integration and maturation of newborn neurons in the adult olfactory bulb—from synapses to function. Eur J Neurosci, 33(6): 1069-1077
|
| 57 |
Palmer T D, Ray J, Gage F H (1995). FGF-2-responsive neuronal progenitors reside in proliferative and quiescent regions of the adult rodent brain. Mol Cell Neurosci, 6(5): 474-486
|
| 58 |
Parent J M, Yu T W, Leibowitz R T, Geschwind D H, Sloviter R S, Lowenstein D H (1997). Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci, 17(10): 3727-3738
|
| 59 |
Potten C S, Loeffler M (1987). A comprehensive model of the crypts of the small intestine of the mouse provides insight into the mechanisms of cell migration and the proliferation hierarchy. J Theor Biol, 127(4): 381-391
|
| 60 |
Potten C S, Loeffler M (1990). Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development, 110(4): 1001-1020
|
| 61 |
Pun R Y K, Rolle I J, Lasarge C L, Hosford B E, Rosen J M, Uhl J D, Schmeltzer S N, Faulkner C, Bronson S L, Murphy B L, Richards D A, Holland K D, Danzer S C (2012). Excessive activation of mTOR in postnatally generated granule cells is sufficient to cause epilepsy. Neuron, 75(6): 1022-1034
|
| 62 |
Ramón y Cajal S (1928) Degeneration and regeneration of the nervous system. Oxford University Press.
|
| 63 |
Reynolds B A, Weiss S (1992). Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science, 255(5052): 1707-1710
|
| 64 |
Rochefort C, Gheusi G, Vincent J D, Lledo P M (2002). Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J Neurosci, 22(7): 2679-2689
|
| 65 |
Rodríguez J J, Jones V C, Tabuchi M, Allan S M, Knight E M, LaFerla F M, Oddo S, Verkhratsky A (2008). Impaired adult neurogenesis in the dentate gyrus of a triple transgenic mouse model of Alzheimer’s disease. PLoS ONE, 3(8): e2935
|
| 66 |
Sahay A, Scobie K N, Hill A S, O’Carroll C M, Kheirbek M A, Burghardt N S, Fenton A A, Dranovsky A, Hen R (2011). Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature, 472(7344): 466-470
|
| 67 |
Sanai N, Nguyen T, Ihrie R A, Mirzadeh Z, Tsai H H, Wong M, Gupta N, Berger M S, Huang E, Garcia-Verdugo J M, Rowitch D H, Alvarez-Buylla A (2011). Corridors of migrating neurons in the human brain and their decline during infancy. Nature, 478(7369): 382-386
|
| 68 |
Santarelli L, Saxe M, Gross C, Surget A, Battaglia F, Dulawa S, Weisstaub N, Lee J, Duman R, Arancio O, Belzung C, Hen R (2003). Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science, 301(5634): 805-809
|
| 69 |
Scharfman H, Goodman J, Macleod A, Phani S, Antonelli C, Croll S (2005). Increased neurogenesis and the ectopic granule cells after intrahippocampal BDNF infusion in adult rats. Exp Neurol, 192(2): 348-356
|
| 70 |
Schmidt-Hieber C, Jonas P, Bischofberger J (2004). Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature, 429(6988): 184-187
|
| 71 |
Seib D R M, Corsini N S, Ellwanger K, Plaas C, Mateos A, Pitzer C, Niehrs C, Celikel T, Martin-Villalba A (2013). Loss of Dickkopf-1 restores neurogenesis in old age and counteracts cognitive decline. Cell Stem Cell, 12(2): 204-214
|
| 72 |
Seri B, García-Verdugo J M, McEwen B S, Alvarez-Buylla A (2001). Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci, 21(18): 7153-7160
|
| 73 |
Snyder J S, Soumier A, Brewer M, Pickel J, Cameron H A (2011). Adult hippocampal neurogenesis buffers stress responses and depressive behaviour. Nature, 476(7361): 458-461
|
| 74 |
Song J, Zhong C, Bonaguidi M A, Sun G J, Hsu D, Gu Y, Meletis K, Huang Z J, Ge S, Enikolopov G, Deisseroth K, Luscher B, Christian K M, Ming G L, Song H (2012). Neuronal circuitry mechanism regulating adult quiescent neural stem-cell fate decision. Nature, 489(7414): 150-154
|
| 75 |
Squire L R (2009). The legacy of patient H.M. for neuroscience. Neuron, 61(1): 6-9
|
| 76 |
Suh H, Consiglio A, Ray J, Sawai T, D’Amour K A, Gage F H (2007). In vivo fate analysis reveals the multipotent and self-renewal capacities of Sox2+ neural stem cells in the adult hippocampus. Cell Stem Cell, 1(5): 515-528
|
| 77 |
Tashiro A, Makino H, Gage F H (2007). Experience-specific functional modification of the dentate gyrus through adult neurogenesis: a critical period during an immature stage. J Neurosci, 27(12): 3252-3259
|
| 78 |
Tashiro A, Sandler V M, Toni N, Zhao C, Gage F H (2006). NMDA-receptor-mediated, cell-specific integration of new neurons in adult dentate gyrus. Nature, 442(7105): 929-933
|
| 79 |
Toni N, Laplagne D A, Zhao C, Lombardi G, Ribak C E, Gage F H, Schinder A F (2008). Neurons born in the adult dentate gyrus form functional synapses with target cells. Nat Neurosci, 11(8): 901-907
|
| 80 |
Toni N, Teng E M, Bushong E A, Aimone J B, Zhao C, Consiglio A, van Praag H, Martone M E, Ellisman M H, Gage F H (2007). Synapse formation on neurons born in the adult hippocampus. Nat Neurosci, 10(6): 727-734
|
| 81 |
Tozuka Y, Fukuda S, Namba T, Seki T, Hisatsune T (2005). GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron, 47(6): 803-815
|
| 82 |
Vadodaria K C, Brakebusch C, Suter U, Jessberger S (2013). Stage-specific functions of the small Rho GTPases Cdc42 and Rac1 for adult hippocampal neurogenesis. J Neurosci, 33(3): 1179-1189
|
| 83 |
van Praag H, Kempermann G, Gage F H (1999). Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci, 2(3): 266-270
|
| 84 |
van Praag H, Schinder A F, Christie B R, Toni N, Palmer T D, Gage F H (2002). Functional neurogenesis in the adult hippocampus. Nature, 415(6875): 1030-1034
|
| 85 |
Wang L P, Kempermann G, Kettenmann H (2005). A subpopulation of precursor cells in the mouse dentate gyrus receives synaptic GABAergic input. Mol Cell Neurosci, 29(2): 181-189
|
| 86 |
Winner B, Lie D C, Rockenstein E, Aigner R, Aigner L, Masliah E, Kuhn H G, Winkler J (2004). Human wild-type alpha-synuclein impairs neurogenesis. J Neuropathol Exp Neurol, 63(11): 1155-1166
|
| 87 |
Yamaguchi M, Saito H, Suzuki M, Mori K (2000). Visualization of neurogenesis in the central nervous system using nestin promoter-GFP transgenic mice. Neuroreport, 11(9): 1991-1996
|
| 88 |
Zhao C, Deng W, Gage F H (2008). Mechanisms and functional implications of adult neurogenesis. Cell, 132(4): 645-660
|
| 89 |
Zhao C, Teng E M, Summers R G Jr, Ming G L, Gage F H (2006). Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J Neurosci, 26(1): 3-11
|
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|
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