Metabolic regulation of adult stem cell-derived neurons

Ruth Beckervordersandforth, Benjamin M. Häberle, D. Chichung Lie

PDF(1537 KB)
PDF(1537 KB)
Front. Biol. ›› 2015, Vol. 10 ›› Issue (2) : 107-116. DOI: 10.1007/s11515-015-1351-5
MINI-REVIEW
MINI-REVIEW

Metabolic regulation of adult stem cell-derived neurons

Author information +
History +

Abstract

The discovery of continuous generation of functional neurons throughout life has emerged as a major contributor to plasticity in defined regions of the adult mammalian brain. Work over the past decades identified cellular constituents of the distinct adult neurogenic niches as well as numerous signaling pathways, transcriptional and epigenetic regulators that exert tight control over the production of new neurons from resident stem cells. Recent studies uncovered developmental stage-specific adaptations of metabolic circuits and have provided evidence for their central regulatory function in the adult neurogenic lineage. Moreover, there is increasing evidence for a regulatory impact of a wide range of systemic metabolic factors including exercise induced metabolic changes and diet on the development of adult-born neurons. Here, we will summarize current knowledge and emerging principles underlying the metabolic control of neuronal maturation in adult neurogenesis.

Keywords

metabolism / adult neurogenesis / mitochondria / diet

Cite this article

Download citation ▾
Ruth Beckervordersandforth, Benjamin M. Häberle, D. Chichung Lie. Metabolic regulation of adult stem cell-derived neurons. Front. Biol., 2015, 10(2): 107‒116 https://doi.org/10.1007/s11515-015-1351-5

References

[1]
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
CrossRef Pubmed Google scholar
[2]
Alle H, Roth A, Geiger J R (2009). Energy-efficient action potentials in hippocampal mossy fibers. Science, 325(5946): 1405–1408
CrossRef Pubmed Google scholar
[3]
Altarejos J Y, Montminy M (2011). CREB and the CRTC co-activators: sensors for hormonal and metabolic signals. Nat Rev Mol Cell Biol, 12(3): 141–151
CrossRef Pubmed Google scholar
[4]
Alvarez J I, Katayama T, Prat A (2013). Glial influence on the blood brain barrier. Glia, 61(12): 1939–1958
CrossRef Pubmed Google scholar
[5]
Amiri A, Cho W, Zhou J, Birnbaum S G, Sinton C M, McKay R M, Parada L F (2012). Pten deletion in adult hippocampal neural stem/progenitor cells causes cellular abnormalities and alters neurogenesis. J Neurosci, 32(17): 5880–5890
CrossRef Pubmed Google scholar
[6]
Arai Y, Kojima T, Takayama M, Hirose N (2009). The metabolic syndrome, IGF-1, and insulin action. Mol Cell Endocrinol, 299(1): 124–128
CrossRef Pubmed Google scholar
[7]
Attardi G, Schatz G (1988). Biogenesis of mitochondria. Annu Rev Cell Biol, 4(1): 289–333
CrossRef Pubmed Google scholar
[8]
Attwell D, Laughlin S B (2001). An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab, 21(10): 1133–1145
CrossRef Pubmed Google scholar
[9]
Bélanger M, Allaman I, Magistretti P J (2011). Brain energy metabolism: focus on astrocyte-neuron metabolic cooperation. Cell Metab, 14(6): 724–738
CrossRef Pubmed Google scholar
[10]
Bertholet A M, Millet A M, Guillermin O, Daloyau M, Davezac N, Miquel M C, Belenguer P (2013). OPA1 loss of function affects in vitro neuronal maturation. Brain, 136(Pt 5): 1518–1533
CrossRef Pubmed Google scholar
[11]
Broughton S, Partridge L (2009). Insulin/IGF-like signalling, the central nervous system and aging. Biochem J, 418(1): 1–12
CrossRef Pubmed Google scholar
[12]
Cheng A, Hou Y, Mattson M P (2010). Mitochondria and neuroplasticity. ASN Neuro, 2(5): e00045
CrossRef Pubmed Google scholar
[13]
Cheng A, Wan R, Yang J L, Kamimura N, Son T G, Ouyang X, Luo Y, Okun E, Mattson M P (2012). Involvement of PGC-1α in the formation and maintenance of neuronal dendritic spines. Nat Commun, 3: 1250
CrossRef Pubmed Google scholar
[14]
Courchet J, Lewis T L Jr, Lee S, Courchet V, Liou D Y, Aizawa S, Polleux F (2013). Terminal axon branching is regulated by the LKB1-NUAK1 kinase pathway via presynaptic mitochondrial capture. Cell, 153(7): 1510–1525
CrossRef Pubmed Google scholar
[15]
Dickey A S, Strack S (2011). PKA/AKAP1 and PP2A/Bβ2 regulate neuronal morphogenesis via Drp1 phosphorylation and mitochondrial bioenergetics. J Neurosci, 31(44): 15716–15726
CrossRef Pubmed Google scholar
[16]
Dietrich M O, Andrews Z B, Horvath T L (2008). Exercise-induced synaptogenesis in the hippocampus is dependent on UCP2-regulated mitochondrial adaptation. J Neurosci, 28(42): 10766–10771
CrossRef Pubmed Google scholar
[17]
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
CrossRef Pubmed Google scholar
[18]
Espósito M S, Piatti V C, Laplagne D A, Morgenstern N A, Ferrari C C, Pitossi F J, Schinder A F (2005). Neuronal differentiation in the adult hippocampus recapitulates embryonic development. J Neurosci, 25(44): 10074–10086
CrossRef Pubmed Google scholar
[19]
Fabel K, Fabel K, Tam B, Kaufer D, Baiker A, Simmons N, Kuo C J, Palmer T D (2003). VEGF is necessary for exercise-induced adult hippocampal neurogenesis. Eur J Neurosci, 18(10): 2803–2812
CrossRef Pubmed Google scholar
[20]
Fabel K, Kempermann G (2008). Physical activity and the regulation of neurogenesis in the adult and aging brain. Neuromolecular Med, 10(2): 59–66
CrossRef Pubmed Google scholar
[21]
Fabel K, Wolf S A, Ehninger D, Babu H, Leal-Galicia P, Kempermann G (2009). Additive effects of physical exercise and environmental enrichment on adult hippocampal neurogenesis in mice. Front Neurosci, 3: 50
Pubmed
[22]
Frayling C, Britton R, Dale N (2011). ATP-mediated glucosensing by hypothalamic tanycytes. J Physiol, 589(Pt 9): 2275–2286
CrossRef Pubmed Google scholar
[23]
Fujioka T, Fujioka A, Duman R S (2004). Activation of cAMP signaling facilitates the morphological maturation of newborn neurons in adult hippocampus. J Neurosci, 24(2): 319–328
CrossRef Pubmed Google scholar
[24]
Ge S, Goh E L, Sailor K A, Kitabatake Y, Ming G L, Song H (2006). GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature, 439(7076): 589–593
CrossRef Pubmed Google scholar
[25]
Ge S, Pradhan D A, Ming G L, Song H (2007). GABA sets the tempo for activity-dependent adult neurogenesis. Trends Neurosci, 30(1): 1–8
CrossRef Pubmed Google scholar
[26]
Giachino C, De Marchis S, Giampietro C, Parlato R, Perroteau I, Schütz G, Fasolo A, Peretto P (2005). cAMP response element-binding protein regulates differentiation and survival of newborn neurons in the olfactory bulb. J Neurosci, 25(44): 10105–10118
CrossRef Pubmed Google scholar
[27]
Gouazé A, Brenachot X, Rigault C, Krezymon A, Rauch C, Nédélec E, Lemoine A, Gascuel J, Bauer S, Pénicaud L, Benani A (2013). Cerebral cell renewal in adult mice controls the onset of obesity. PLoS ONE, 8(8): e72029
CrossRef Pubmed Google scholar
[28]
Hawley J A, Hargreaves M, Joyner M J, Zierath J R (2014). Integrative biology of exercise. Cell, 159(4): 738–749
CrossRef Pubmed Google scholar
[29]
Herold S, Jagasia R, Merz K, Wassmer K, Lie D C (2011). CREB signalling regulates early survival, neuronal gene expression and morphological development in adult subventricular zone neurogenesis. Mol Cell Neurosci, 46(1): 79–88
CrossRef Pubmed Google scholar
[30]
Herrero-Mendez A, Almeida A, Fernández E, Maestre C, Moncada S, Bolaños J P (2009). The bioenergetic and antioxidant status of neurons is controlled by continuous degradation of a key glycolytic enzyme by APC/C-Cdh1. Nat Cell Biol, 11(6): 747–752
CrossRef Pubmed Google scholar
[31]
Itoh Y, Esaki T, Shimoji K, Cook M, Law M J, Kaufman E, Sokoloff L (2003). Dichloroacetate effects on glucose and lactate oxidation by neurons and astroglia in vitro and on glucose utilization by brain in vivo. Proc Natl Acad Sci USA, 100(8): 4879–4884
CrossRef Pubmed Google scholar
[32]
Jagasia R, Steib K, Englberger E, Herold S, Faus-Kessler T, Saxe M, Gage F H, Song H, Lie D C (2009). GABA-cAMP response element-binding protein signaling regulates maturation and survival of newly generated neurons in the adult hippocampus. J Neurosci, 29(25): 7966–7977
CrossRef Pubmed Google scholar
[33]
Kheirbek M A, Klemenhagen K C, Sahay A, Hen R (2012). Neurogenesis and generalization: a new approach to stratify and treat anxiety disorders. Nat Neurosci, 15(12): 1613–1620
CrossRef Pubmed Google scholar
[34]
Kim D Y, Rhee I, Paik J (2014). Metabolic circuits in neural stem cells. Cell Mol Life Sci, 71(21): 4221–4241
CrossRef Pubmed Google scholar
[35]
Kim J Y, Duan X, Liu C Y, Jang M H, Guo J U, Pow-anpongkul N, Kang E, Song H, Ming G L (2009). DISC1 regulates new neuron development in the adult brain via modulation of AKT-mTOR signaling through KIAA1212. Neuron, 63(6): 761–773
CrossRef Pubmed Google scholar
[36]
Kim J Y, Liu C Y, Zhang F, Duan X, Wen Z, Song J, Feighery E, Lu B, Rujescu D, St Clair D, Christian K, Callicott J H, Weinberger D R, Song H, Ming G L (2012). Interplay between DISC1 and GABA signaling regulates neurogenesis in mice and risk for schizophrenia. Cell, 148(5): 1051–1064
CrossRef Pubmed Google scholar
[37]
Kivelä R, Bry M, Robciuc M R, Räsänen M, Taavitsainen M, Silvola J M, Saraste A, Hulmi J J, Anisimov A, Mäyränpää M I, Lindeman J H, Eklund L, Hellberg S, Hlushchuk R, Zhuang Z W, Simons M, Djonov V, Knuuti J, Mervaala E, Alitalo K (2014). VEGF-B-induced vascular growth leads to metabolic reprogramming and ischemia resistance in the heart. EMBO Mol Med, 6(3): 307–321
Pubmed
[38]
Klempin F, Beis D, Mosienko V, Kempermann G, Bader M, Alenina N (2013). Serotonin is required for exercise-induced adult hippocampal neurogenesis. J Neurosci, 33(19): 8270–8275
CrossRef Pubmed Google scholar
[39]
Knobloch M, Braun S M, 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
CrossRef Pubmed Google scholar
[40]
Kokoeva M V, Yin H, Flier J S (2005). Neurogenesis in the hypothalamus of adult mice: potential role in energy balance. Science, 310(5748): 679–683
CrossRef Pubmed Google scholar
[41]
Kokoeva M V, Yin H, Flier J S (2007). Evidence for constitutive neural cell proliferation in the adult murine hypothalamus. J Comp Neurol, 505(2): 209–220
CrossRef Pubmed Google scholar
[42]
Kumar V B, Binu S, Soumya S J, K H, Sudhakaran P R (2014). Regulation of vascular endothelial growth factor by metabolic context of the cell. Glycoconj J, 31(6-7): 427–434
CrossRef Pubmed Google scholar
[43]
Lee D A, Bedont J L, Pak T, Wang H, Song J, Miranda-Angulo A, Takiar V, Charubhumi V, Balordi F, Takebayashi H, Aja S, Ford E, Fishell G, Blackshaw S (2012). Tanycytes of the hypothalamic median eminence form a diet-responsive neurogenic niche. Nat Neurosci, 15(5): 700–702
CrossRef Pubmed Google scholar
[44]
Lee D A, Blackshaw S (2012). Functional implications of hypothalamic neurogenesis in the adult mammalian brain. Int J Dev Neurosci, 30(8): 615–621
CrossRef Pubmed Google scholar
[45]
Lee D A, Yoo S, Pak T, Salvatierra J, Velarde E, Aja S, Blackshaw S (2014). Dietary and sex-specific factors regulate hypothalamic neurogenesis in young adult mice. Front Neurosci, 8: 157
CrossRef Pubmed Google scholar
[46]
Li Z, Jo J, Jia J M, Lo S C, Whitcomb D J, Jiao S, Cho K, Sheng M (2010). Caspase-3 activation via mitochondria is required for long-term depression and AMPA receptor internalization. Cell, 141(5): 859–871
CrossRef Pubmed Google scholar
[47]
Li Z, Okamoto K, Hayashi Y, Sheng M (2004). The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell, 119(6): 873–887
CrossRef Pubmed Google scholar
[48]
Lipton J O, Sahin M (2014). The neurology of mTOR. Neuron, 84(2): 275–291
CrossRef Pubmed Google scholar
[49]
MacAskill A F, Atkin T A, Kittler J T (2010). Mitochondrial trafficking and the provision of energy and calcium buffering at excitatory synapses. Eur J Neurosci, 32(2): 231–240
CrossRef Pubmed Google scholar
[50]
Macaskill A F, Rinholm J E, Twelvetrees A E, Arancibia-Carcamo I L, Muir J, Fransson A, Aspenstrom P, Attwell D, Kittler J T (2009). Miro1 is a calcium sensor for glutamate receptor-dependent localization of mitochondria at synapses. Neuron, 61(4): 541–555
CrossRef Pubmed Google scholar
[51]
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
CrossRef Pubmed Google scholar
[52]
Mattson M P (2012). Energy intake and exercise as determinants of brain health and vulnerability to injury and disease. Cell Metab, 16(6): 706–722
CrossRef Pubmed Google scholar
[53]
Merz K, Herold S, Lie D C (2011). CREB in adult neurogenesis—master and partner in the development of adult-born neurons? Eur J Neurosci, 33(6): 1078–1086
CrossRef Pubmed Google scholar
[54]
Mihaylova M M, Sabatini D M, Yilmaz O H (2014). Dietary and metabolic control of stem cell function in physiology and cancer. Cell Stem Cell, 14(3): 292–305
CrossRef Pubmed Google scholar
[55]
Ming G L, Song H (2011). Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron, 70(4): 687–702
CrossRef Pubmed Google scholar
[56]
Mishra P, Chan D C (2014). Mitochondrial dynamics and inheritance during cell division, development and disease. Nat Rev Mol Cell Biol, 15(10): 634–646
CrossRef Pubmed Google scholar
[57]
Nakagawa S, Kim J E, Lee R, Chen J, Fujioka T, Malberg J, Tsuji S, Duman R S (2002). Localization of phosphorylated cAMP response element-binding protein in immature neurons of adult hippocampus. J Neurosci, 22(22): 9868–9876
Pubmed
[58]
Orellana J A, Sáez P J, Cortés-Campos C, Elizondo R J, Shoji K F, Contreras-Duarte S, Figueroa V, Velarde V, Jiang J X, Nualart F, Sáez J C, García M A (2012). Glucose increases intracellular free Ca2+ in tanycytes via ATP released through connexin 43 hemichannels. Glia, 60(1): 53–68
CrossRef Pubmed Google scholar
[59]
Oruganty-Das A, Ng T, Udagawa T, Goh E L, Richter J D (2012). Translational control of mitochondrial energy production mediates neuron morphogenesis. Cell Metab, 16(6): 789–800
CrossRef Pubmed Google scholar
[60]
Osman C, Voelker D R, Langer T (2011). Making heads or tails of phospholipids in mitochondria. J Cell Biol, 192(1): 7–16
CrossRef Pubmed Google scholar
[61]
Pellerin L, Magistretti P J (1994). Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc Natl Acad Sci USA, 91(22): 10625–10629
CrossRef Pubmed Google scholar
[62]
Pereira A C, Huddleston D E, Brickman A M, Sosunov A A, Hen R, McKhann G M, Sloan R, Gage F H, Brown T R, Small S A (2007). An in vivo correlate of exercise-induced neurogenesis in the adult dentate gyrus. Proc Natl Acad Sci USA, 104(13): 5638–5643
CrossRef Pubmed Google scholar
[63]
Piatti V C, Davies-Sala M G, Espósito M S, Mongiat L A, Trinchero M F, Schinder A F (2011). The timing for neuronal maturation in the adult hippocampus is modulated by local network activity. J Neurosci, 31(21): 7715–7728
CrossRef Pubmed Google scholar
[64]
Pieper A A, Xie S, Capota E, Estill S J, Zhong J, Long J M, Becker G L, Huntington P, Goldman S E, Shen C H, Capota M, Britt J K, Kotti T, Ure K, Brat D J, Williams N S, MacMillan K S, Naidoo J, Melito L, Hsieh J, De Brabander J, Ready J M, McKnight S L (2010). Discovery of a proneurogenic, neuroprotective chemical. Cell, 142(1): 39–51
CrossRef Pubmed Google scholar
[65]
Pierce A A, Xu A W (2010). De novo neurogenesis in adult hypothalamus as a compensatory mechanism to regulate energy balance. J Neurosci, 30(2): 723–730
CrossRef Pubmed Google scholar
[66]
Rodriguez-Rodriguez P, Fernandez E, Almeida A, Bolaños J P (2012). Excitotoxic stimulus stabilizes PFKFB3 causing pentose-phosphate pathway to glycolysis switch and neurodegeneration. Cell Death Differ, 19(10): 1582–1589
CrossRef Pubmed Google scholar
[67]
Rouach N, Koulakoff A, Abudara V, Willecke K, Giaume C (2008). Astroglial metabolic networks sustain hippocampal synaptic transmission. Science, 322(5907): 1551–1555
CrossRef Pubmed Google scholar
[68]
Sahay A, Wilson D A, Hen R (2011). Pattern separation: a common function for new neurons in hippocampus and olfactory bulb. Neuron, 70(4): 582–588
CrossRef Pubmed Google scholar
[69]
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
CrossRef Pubmed Google scholar
[70]
Schousboe A, Scafidi S, Bak L K, Waagepetersen H S, McKenna M C (2014). Glutamate metabolism in the brain focusing on astrocytes. Adv Neurobiol, 11: 13–30
CrossRef Pubmed Google scholar
[71]
Sousa-Ferreira L, de Almeida L P, Cavadas C (2014). Role of hypothalamic neurogenesis in feeding regulation. Trends Endocrinol Metab, 25(2): 80–88
CrossRef Pubmed Google scholar
[72]
Spalding K L, Bergmann O, Alkass K, Bernard S, Salehpour M, Huttner H B, Boström E, Westerlund I, Vial C, Buchholz B A, Possnert G, Mash D C, Druid H, Frisén J (2013). Dynamics of hippocampal neurogenesis in adult humans. Cell, 153(6): 1219–1227
CrossRef Pubmed Google scholar
[73]
Spiegelman B M (2007). Transcriptional control of mitochondrial energy metabolism through the PGC1 coactivators. Novartis Found Symp, 287: 60–63, discussion 63–69
CrossRef Pubmed Google scholar
[74]
Steib K, Schäffner I, Jagasia R, Ebert B, Lie D C (2014). Mitochondria modify exercise-induced development of stem cell-derived neurons in the adult brain. J Neurosci, 34(19): 6624–6633
CrossRef Pubmed Google scholar
[75]
Steketee M B, Moysidis S N, Weinstein J E, Kreymerman A, Silva J P, Iqbal S, Goldberg J L (2012). Mitochondrial dynamics regulate growth cone motility, guidance, and neurite growth rate in perinatal retinal ganglion cells in vitro. Invest Ophthalmol Vis Sci, 53(11): 7402–7411
CrossRef Pubmed Google scholar
[76]
Stocca G, Schmidt-Hieber C, Bischofberger J (2008). Differential dendritic Ca2+ signalling in young and mature hippocampal granule cells. J Physiol, 586(16): 3795–3811
CrossRef Pubmed Google scholar
[77]
Stoll E A, Cheung W, Mikheev A M, Sweet I R, Bielas J H, Zhang J, Rostomily R C, Horner P J (2011). Aging neural progenitor cells have decreased mitochondrial content and lower oxidative metabolism. J Biol Chem, 286(44): 38592–38601
CrossRef Pubmed Google scholar
[78]
Stranahan A M, Arumugam T V, Cutler R G, Lee K, Egan J M, Mattson M P (2008). Diabetes impairs hippocampal function through glucocorticoid-mediated effects on new and mature neurons. Nat Neurosci, 11(3): 309–317
CrossRef Pubmed Google scholar
[79]
Sun G J, Sailor K A, Mahmood Q A, Chavali N, Christian K M, Song H, Ming G L (2013). Seamless reconstruction of intact adult-born neurons by serial end-block imaging reveals complex axonal guidance and development in the adult hippocampus. J Neurosci, 33(28): 11400–11411
CrossRef Pubmed Google scholar
[80]
Tatsuta T, Langer T (2008). Quality control of mitochondria: protection against neurodegeneration and ageing. EMBO J, 27(2): 306–314
CrossRef Pubmed Google scholar
[81]
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
CrossRef Pubmed Google scholar
[82]
Trejo J L, Carro E, Torres-Aleman I (2001). Circulating insulin-like growth factor I mediates exercise-induced increases in the number of new neurons in the adult hippocampus. J Neurosci, 21(5): 1628–1634
Pubmed
[83]
van Praag H (2009). Exercise and the brain: something to chew on. Trends Neurosci, 32(5): 283–290
CrossRef Pubmed Google scholar
[84]
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
CrossRef Pubmed Google scholar
[85]
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
CrossRef Pubmed Google scholar
[86]
Wang X, Schwarz T L (2009). The mechanism of Ca2+ -dependent regulation of kinesin-mediated mitochondrial motility. Cell, 136(1): 163–174
CrossRef Pubmed Google scholar
[87]
Ward P S, Thompson C B (2012). Metabolic reprogramming: a cancer hallmark even warburg did not anticipate. Cancer Cell, 21(3): 297–308
CrossRef Pubmed Google scholar
[88]
Winner B, Kohl Z, Gage F H (2011). Neurodegenerative disease and adult neurogenesis. Eur J Neurosci, 33(6): 1139–1151
CrossRef Pubmed Google scholar
[89]
Wu L E, Meoli C C, Mangiafico S P, Fazakerley D J, Cogger V C, Mohamad M, Pant H, Kang M J, Powter E, Burchfield J G, Xirouchaki C E, Mikolaizak A S, Stöckli J, Kolumam G, van Bruggen N, Gamble J R, Le Couteur D G, Cooney G J, Andrikopoulos S, James D E (2014). Systemic VEGF-A neutralization ameliorates diet-induced metabolic dysfunction. Diabetes, 63(8): 2656–2667
CrossRef Pubmed Google scholar
[90]
Yeo H, Lyssiotis C A, Zhang Y, Ying H, Asara J M, Cantley L C, Paik J H (2013). FoxO3 coordinates metabolic pathways to maintain redox balance in neural stem cells. EMBO J, 32(19): 2589–2602
CrossRef Pubmed Google scholar
[91]
Zainuddin M S, Thuret S (2012). Nutrition, adult hippocampal neurogenesis and mental health. Br Med Bull, 103(1): 89–114
CrossRef Pubmed Google scholar
[92]
Zhao C, Deng W, Gage F H (2008). Mechanisms and functional implications of adult neurogenesis. Cell, 132(4): 645–660
CrossRef Pubmed Google scholar
[93]
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
CrossRef Pubmed Google scholar
[94]
Zhou M, Li W, Huang S, Song J, Kim J Y, Tian X, Kang E, Sano Y, Liu C, Balaji J, Wu S, Zhou Y, Zhou Y, Parivash S N, Ehninger D, He L, Song H, Ming G L, Silva A J (2013). mTOR Inhibition ameliorates cognitive and affective deficits caused by Disc1 knockdown in adult-born dentate granule neurons. Neuron, 77(4): 647–654
CrossRef Pubmed Google scholar

Acknowledgements

This work was supported by the Bavarian Research Network on Human induced Pluripotent Stem Cells “FORIPS,” the University Hospital Erlangen [Interdisciplinary center for clinical research (IZKF) grants E12 and E16 to DCL] and the Deutsche Forschungsgemeinschaft (BE 5136/1-1 to RB). The authors declare no competing financial interests.
R. Beckervordersandforth, B. M. Häeberle, and D. C. Lie declare that they have no conflict of interest. This manuscript is a review article and does not involve a research protocol requiring approval by the relevant institutional review board or ethics committee.

RIGHTS & PERMISSIONS

2014 Higher Education Press and Springer-Verlag Berlin Heidelberg
PDF(1537 KB)

Accesses

Citations

Detail

Sections
Recommended

/