Adult neurogenesis is a process that generates new and functional neurons from neural stem cells (NSCs) in a specialized neurogenic niche throughout life. Misregulated neurogenesis is detrimental to normal brain functions. To ensure proper neurogenesis, the niche cells must respond to extrinsic cues while fulfilling the intrinsic requirements of the neurogenic program and adapting their roles accordingly to influence NSC behavior. Understanding how the neurogenic niche executes its functions may guide strategies to maintain its integrative process and provide a permissive milieu for neurogenesis. In this review, we summarize the recent discoveries of interactive regulation of NSCs and neurogenesis by neurogenic niche and its implications in functional integrity of adult brain and neurological disorders.
BoekhoornKJoelsMLucassenPJ. 2006. Increased proliferation reflects glial and vascular-associated changes, but not neurogenesis in the presenile Alzheimer hippocampus. Neurobiol Dis24(1):1–14.
4.
BoeseACHamblinMHLeeJP. 2020. Neural stem cell therapy for neurovascular injury in Alzheimer’s disease. Exp Neurol324:113112.
5.
BondAMMingGLSongHJ. 2015. Adult mammalian neural stem cells and neurogenesis: five decades later. Cell Stem Cell17(4):385–95.
6.
CasseFRichetinKToniN.2018. Astrocytes’ contribution to adult neurogenesis in physiology and Alzheimer’s disease. Front Cell Neurosci12:432.
7.
ChoiSHVeeraraghavaluKLazarovOMarlerSRansohoffRMRamirezJM, and others. 2008. Non-cell-autonomous effects of presenilin 1 variants on enrichment-mediated hippocampal progenitor cell proliferation and differentiation. Neuron59(4):568–80.
8.
Del BigioMR. 1995. The ependyma: a protective barrier between brain and cerebrospinal fluid. Glia14(1):1–13.
9.
DongJPanYBWuXRHeLNLiuXDFengDF, and others. 2019. A neuronal molecular switch through cell-cell contact that regulates quiescent neural stem cells. Sci Adv5(2):eaav4416.
GemmaCBachstetterAD. 2013. The role of microglia in adult hippocampal neurogenesis. Front Cell Neurosci7:229.
12.
GengatharanABammannRRSaghatelyanA.2016. The role of astrocytes in the generation, migration, and integration of new neurons in the adult olfactory bulb. Front Neurosci10:149.
13.
GoncalvesJTSchaferSTGageFH. 2016. Adult neurogenesis in the hippocampus: from stem cells to behavior. Cell167(4):897–914.
14.
GuoWZhangLChristopherDMTengZQFausettSRLiuC, and others. 2011. RNA-binding protein FXR2 regulates adult hippocampal neurogenesis by reducing Noggin expression. Neuron70(5):924–38.
15.
HaggT. 2009. From neurotransmitters to neurotrophic factors to neurogenesis. Neuroscientist15(1):20–7.
16.
HoglingerGUArias-CarrionOIpachBOertelWH. 2014. Origin of the dopaminergic innervation of adult neurogenic areas. J Comp Neurol522(10):2336–48.
17.
HunterMDemaraisNJFaullRLMGreyACCurtisMA. 2018. Subventricular zone lipidomic architecture loss in Huntington’s disease. J Neurochem146(5):613–30.
18.
JohansonCEStopaEGMcMillanPN. 2011. The blood-cerebrospinal fluid barrier: structure and functional significance. Methods Mol Biol686:101–31.
19.
KandasamyMCouillard-DespresSRaberKAStephanMLehnerBWinnerB, and others. 2010. Stem cell quiescence in the hippocampal neurogenic niche is associated with elevated transforming growth factor-beta signaling in an animal model of Huntington disease. J Neuropathol Exp Neurol69(7):717–28.
20.
KanekoNMarinOKoikeMHirotaYUchiyamaYWuJY, and others. 2010. New neurons clear the path of astrocytic processes for their rapid migration in the adult brain. Neuron67(2):213–23.
21.
KatsimpardiLLittermanNKScheinPAMillerCMLoffredoFSWojtkiewiczGR, and others. 2014. Vascular and neurogenic rejuvenation of the aging mouse brain by young systemic factors. Science344(6184):630–4.
22.
KjellJFischer-SternjakJThompsonAJFriessCSticcoMJSalinasF, and others. 2020. Defining the adult neural stem cell niche proteome identifies key regulators of adult neurogenesis. Cell Stem Cell26(2):277–93.
23.
KohlZBen AbdallahNVogelgsangJTischerLDeusserJAmatoD, and others. 2016. Severely impaired hippocampal neurogenesis associates with an early serotonergic deficit in a BAC alpha-synuclein transgenic rat model of Parkinson’s disease. Neurobiol Dis85:206–17.
24.
KohlZRegensburgerMAignerRKandasamyMWinnerBAignerL, and others. 2010. Impaired adult olfactory bulb neurogenesis in the R6/2 mouse model of Huntington’s disease. BMC Neurosci11:114.
25.
KokovayEWangYKusekGWursterRLedermanPLowryN, and others. 2012. VCAM1 is essential to maintain the structure of the SVZ niche and acts as an environmental sensor to regulate SVZ lineage progression. Cell Stem Cell11(2):220–30.
26.
LeeJKFandakovaYJohnsonEGCohenNJBungeSAGhettiS.2019. Changes in anterior and posterior hippocampus differentially predict item-space, item-time, and item-item memory improvement. Dev Cogn Neurosci41:100741.
27.
LehtinenMKBjornssonCSDymeckiSMGilbertsonRJHoltzmanDMMonukiES. 2013. The choroid plexus and cerebrospinal fluid: emerging roles in development, disease, and therapy. J Neurosci33(45):17553–9.
28.
LepkoTPuschMMullerTSchulteDEhsesJKieblerM, and others. 2019. Choroid plexus-derived miR-204 regulates the number of quiescent neural stem cells in the adult brain. EMBO J38(17):e100481.
29.
LichtTKeshetE.2015. The vascular niche in adult neurogenesis. Mech Dev138(Pt 1):56–62.
30.
LimDATramontinADTrevejoJMHerreraDGGarcia-VerdugoJMAlvarez-BuyllaA.2000. Noggin antagonizes BMP signaling to create a niche for adult neurogenesis. Neuron28(3):713–26.
31.
LiuXWangQHaydarTFBordeyA.2005. Nonsynaptic GABA signaling in postnatal subventricular zone controls proliferation of GFAP-expressing progenitors. Nat Neurosci8(9):1179–87.
32.
LuZElliottMRChenYWalshJTKlibanovALRavichandranKS, and others. 2011. Phagocytic activity of neuronal progenitors regulates adult neurogenesis. Nat Cell Biol13(9):1076–83.
33.
MatarredonaERTalaveronRPastorAM. 2018. Interactions between neural progenitor cells and microglia in the subventricular zone: physiological implications in the neurogenic niche and after implantation in the injured brain. Front Cell Neurosci12:268.
34.
MirzadehZMerkleFTSoriano-NavarroMGarcia-VerdugoJMAlvarez-BuyllaA.2008. Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. Cell Stem Cell3(3):265–78.
35.
MortonAJSkillingsEAWoodNIZhengZ.2019. Antagonistic pleiotropy in mice carrying a CAG repeat expansion in the range causing Huntington’s disease. Sci Rep9(1):37.
36.
MosherKIAndresRHFukuharaTBieriGHasegawa-MoriyamaMHeY, and others. 2012. Neural progenitor cells regulate microglia functions and activity. Nat Neurosci15(11):1485–7.
37.
OttoneCKruscheBWhitbyAClementsMQuadratoGPitulescuME, and others. 2014. Direct cell-cell contact with the vascular niche maintains quiescent neural stem cells. Nat Cell Biol16(11):1045–56.
38.
OttoneCParrinelloS.2015. Multifaceted control of adult SVZ neurogenesis by the vascular niche. Cell Cycle14(14):2222–5.
39.
PalmerTD. 2002. Adult neurogenesis and the vascular Nietzsche. Neuron34(6):856–8.
PlatelJCDaveKAGordonVLacarBRubioMEBordeyA.2010. NMDA receptors activated by subventricular zone astrocytic glutamate are critical for neuroblast survival prior to entering a synaptic network. Neuron65(6):859–72.
42.
RedzicZBPrestonJEDuncanJAChodobskiASzmydynger-ChodobskaJ.2005. The choroid plexus-cerebrospinal fluid system: from development to aging. Curr Top Dev Biol71:1–52.
43.
SatoYUchidaYHuJYoung-PearseTLNiikuraTMukouyamaYS. 2017. Soluble APP functions as a vascular niche signal that controls adult neural stem cell number. Development144(15):2730–6.
44.
SawamotoKWichterleHGonzalez-PerezOCholfinJAYamadaMSpasskyN, and others. 2006. New neurons follow the flow of cerebrospinal fluid in the adult brain. Science311(5761):629–32.
45.
SchofieldR. 1978. The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells4(1–2):7–25.
46.
ShenJWangDWangXGuptaSAylooBWuS, and others. 2019. Neurovascular coupling in the dentate gyrus regulates adult hippocampal neurogenesis. Neuron103(5): 878–890.e3.
47.
ShenQWangYKokovayELinGChuangSMGoderieSK, and others. 2008. Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions. Cell Stem Cell3(3):289–300.
48.
SierraAEncinasJMDeuderoJJChanceyJHEnikolopovGOverstreet-WadicheLS, and others. 2010. Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis. Cell Stem Cell7(4):483–95.
49.
SunGJZhouYStadelRPMossJYongJHItoS, and others. 2015. Tangential migration of neuronal precursors of glutamatergic neurons in the adult mammalian brain. Proc Natl Acad Sci U S A112(30):9484–9.
SultanSLiLYMossJPetrelliFCasseFGebaraE, and others. 2015. Synaptic integration of adult-born hippocampal neurons is locally controlled by astrocytes. Neuron88(5):957–72.
52.
TangCWangMWangPWangLWuQGuoW.2019. Neural stem cells behave as a functional niche for the maturation of newborn neurons through the secretion of PTN. Neuron101(1):32–44.e6.
53.
TavazoieMVan der VekenLSilva-VargasVLouissaintMColonnaLZaidiB, and others. 2008. A specialized vascular niche for adult neural stem cells. Cell Stem Cell3(3):279–88.
54.
TongCKChenJCebrian-SillaAMirzadehZObernierKGuintoCD, and others. 2014. Axonal control of the adult neural stem cell niche. Cell Stem Cell14(4):500–11.
55.
VicidominiCGuoNSahayA.2020. Communication, cross talk, and signal integration in the adult hippocampal neurogenic niche. Neuron105(2):220–35.
56.
WangJCuiYXYuZYWangWJChengXJiWL, and others. 2019. Brain endothelial cells maintain lactate homeostasis and control adult hippocampal neurogenesis. Cell Stem Cell25(6):754–67.
57.
WinnerBWinklerJ.2015. Adult neurogenesis in neurodegenerative diseases. Cold Spring Harb Perspect Biol7(4):a021287.
58.
WuJTianWJLiuYWangHJZhengJWangX, and others. 2020. Ependyma-expressed CCN1 restricts the size of the neural stem cell pool in the adult ventricular-subventricular zone. EMBO J:e101679.
59.
YehCYAsricanBMossJQuintanillaLJHeTMaoX, and others. 2018. Mossy cells control adult neural stem cell quiescence and maintenance through a dynamic balance between direct and indirect pathways. Neuron99(3): 493–510.e4.
60.
ZhengJLiHLTianNLiuFWangLYinY, and others. 2020. Interneuron accumulation of phosphorylated tau impairs adult hippocampal neurogenesis by suppressing GABAergic transmission. Cell Stem Cell26(3):331–45.e6. doi:10.1016/j.stem.2019.12.015
