Control of adult neurogenesis by programmed cell death in the mammalian brain

Molecular Brain

Volumn 9, Issue 1, 2016, Pages

  Ryu, Jae Ryun ^a   Hong, Caroline Jeeyeon ^b   Kim, Joo Yeon ^a   Kim, Eun Kyoung ^b   Sun, Woong ^a   Yu, Seong Woon ^b  

^a Korea University College of Medicine   (South Korea)

^b Daegu Gyeongbuk Institute of Science and Technology   (South Korea)

Author keywords

Adult neurogenesis; Apoptosis; Autophagy; Necrosis; Neural stem cells; Neuroblasts; Programmed cell death

Indexed keywords

FAS ANTIGEN; SCATTER FACTOR; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

AGING; APOPTOSIS; BRAIN INJURY; BRAIN ISCHEMIA; CELL ISOLATION; CELL MIGRATION; CELL PROLIFERATION; CELL RENEWAL; ENERGY METABOLISM; HIPPOCAMPUS; HUMAN; INTRACELLULAR SIGNALING; NEOCORTEX; NERVE CELL DIFFERENTIATION; NERVE CELL NECROSIS; NERVE CELL NETWORK; NEURAL STEM CELL; NEUROBLAST; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; RETINA GANGLION CELL; REVIEW; STEM CELL TRANSPLANTATION; SUBVENTRICULAR ZONE; ANIMAL; BRAIN; CYTOLOGY; MAMMAL; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY;

AGING; ANIMALS; APOPTOSIS; BRAIN; MAMMALS; NEURAL STEM CELLS; NEUROGENESIS;

EID: 84966340354     PISSN: None     EISSN: 17566606     Source Type: Journal    
DOI: 10.1186/s13041-016-0224-4     Document Type: Review

References (272)

1. Buss RR, Sun W, Oppenheim RW. Adaptive roles of programmed cell death during nervous system development. Annu Rev Neurosci. 2006;29:1-35.
2. Oppenheim RW. Viktor Hamburger (1900-2001). Journey of a neuroembryologist to the end of the millennium and beyond. Neuron. 2001;31:179-90.
3. Oppenheim RW. Cell death of motoneurons in the chick embryo spinal cord. V. Evidence on the role of cell death and neuromuscular function in the formation of specific peripheral connections. J Neurosci. 1981;1:141-51.
4. Oppenheim RW, Chu-wang I. Spontaneous cell death of spinal motoneurons following peripheral innervation in the chick embryo. Brain Res. 1977;125:154-60.
5. Oppenheim RW, Prevette D, Yin QW, Collins F, MacDonald J. Control of embryonic motoneuron survival in vivo by ciliary neurotrophic factor. Science. 1991;251:1616-8.
6. Cowan WM. Viktor Hamburger and Rita Levi-Montalcini: the path to the discovery of nerve growth factor. Annu Rev Neurosci. 2001;24:551-600.
7. Hamburger V. Cell death in the development of the lateral motor column of the chick embryo. J Comp Neurol. 1975;160:535-46.
8. Gage FH. Mammalian neural stem cells. Science. 2000;287:1433-8.
9. Zhao C, Deng W, Gage FH. Mechanisms and functional implications of adult neurogenesis. Cell. 2008;132:645-60.
10. Lledo PM, Alonso M, Grubb MS. Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci. 2006;7:179-93.
11. Imayoshi I, Sakamoto M, Ohtsuka T, Takao K, Miyakawa T, Yamaguchi M, Mori K, Ikeda T, Itohara S, Kageyama R. Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat Neurosci. 2008;11:1153-61.
12. Perez-Domper P, Gradari S, Trejo JL. The growth factors cascade and the dendrito-/synapto-genesis versus cell survival in adult hippocampal neurogenesis: the chicken or the egg. Ageing Res Rev. 2013;12:777-85.
13. Altman J, Das GD. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol. 1965;124:319-35.
14. Ming GL, Song H. Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci. 2005;28:223-50.
15. Kuan CY, Schloemer AJ, Lu A, Burns KA, Weng WL, Williams MT, Strauss KI, Vorhees CV, Flavell RA, Davis RJ, et al. Hypoxia-ischemia induces DNA synthesis without cell proliferation in dying neurons in adult rodent brain. J Neurosci. 2004;24:10763-72.
16. Taupin P. BrdU immunohistochemistry for studying adult neurogenesis: paradigms, pitfalls, limitations, and validation. Brain Res Rev. 2007;53:198-214.
17. Price J, Turner D, Cepko C. Lineage analysis in the vertebrate nervous system by retrovirus-mediated gene transfer. Proc Natl Acad Sci U S A. 1987;84:156-60.
18. Sanes JR, Rubenstein JL, Nicolas JF. Use of a recombinant retrovirus to study post-implantation cell lineage in mouse embryos. EMBO J. 1986;5:3133-42.
19. Yan R, Zhang L, Zhang Q, Li J, Kang X, Wang H, Zhang J, Yang S, Yang X. A new finding concerning adenoviral-mediated gene transfer: a high-level, cell-specific transgene expression in the neural stem cells of adult mice. J Virol Methods. 2012;186:1-6.
20. Ge S, Goh EL, Sailor KA, Kitabatake Y, Ming GL, Song H. GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature. 2006;439:589-93.
21. Ng T, Ryu JR, Sohn JH, Tan T, Song H, Ming GL, Goh EL. Class 3 semaphorin mediates dendrite growth in adult newborn neurons through Cdk5/FAK pathway. PLoS One. 2013;8:e65572.
22. Ables JL, Decarolis NA, Johnson MA, Rivera PD, Gao Z, Cooper DC, Radtke F, Hsieh J, Eisch AJ. Notch1 is required for maintenance of the reservoir of adult hippocampal stem cells. J Neurosci. 2010;30:10484-92.
23. Dranovsky A, Picchini AM, Moadel T, Sisti AC, Yamada A, Kimura S, Leonardo ED, Hen R. Experience dictates stem cell fate in the adult hippocampus. Neuron. 2011;70:908-23.
24. Kuo CT, Mirzadeh Z, Soriano-Navarro M, Rasin M, Wang D, Shen J, Sestan N, Garcia-Verdugo J, Alvarez-Buylla A, Jan LY, Jan YN. Postnatal deletion of Numb/Numblike reveals repair and remodeling capacity in the subventricular neurogenic niche. Cell. 2006;127:1253-64.
25. Petrik D, Latchney SE, Masiulis I, Yun S, Zhang Z, Wu JI, Eisch AJ. Chromatin Remodeling Factor Brg1 Supports the Early Maintenance and Late Responsiveness of Nestin-Lineage Adult Neural Stem and Progenitor Cells. Stem Cells. 2015;33:3655-65.
26. Bergmann O, Liebl J, Bernard S, Alkass K, Yeung MS, Steier P, Kutschera W, Johnson L, Landen M, Druid H. The age of olfactory bulb neurons in humans. Neuron. 2012;74:634-9.
27. Bhardwaj RD, Curtis MA, Spalding KL, Buchholz BA, Fink D, Bjork-Eriksson T, Nordborg C, Gage FH, Druid H, Eriksson PS, Frisen J. Neocortical neurogenesis in humans is restricted to development. Proc Natl Acad Sci U S A. 2006;103:12564-8.
28. Ernst A, Alkass K, Bernard S, Salehpour M, Perl S, Tisdale J, Possnert G, Druid H, Frisen J. Neurogenesis in the striatum of the adult human brain. Cell. 2014;156:1072-83.
29. Kreutzberg GW. Microglia: a sensor for pathological events in the CNS. Trends Neurosci. 1996;19:312-8.
30. Streit WJ. Microglial response to brain injury: a brief synopsis. Toxicol Pathol. 2000;28:28-30.
31. Lu Z, Elliott MR, Chen Y, Walsh JT, Klibanov AL, Ravichandran KS, Kipnis J. Phagocytic activity of neuronal progenitors regulates adult neurogenesis. Nat Cell Biol. 2011;13:1076-83.
32. Sierra A, Encinas JM, Deudero JJ, Chancey JH, Enikolopov G, Overstreet-Wadiche LS, Tsirka SE, Maletic-Savatic M. Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis. Cell Stem Cell. 2010;7:483-95.
33. Kim WR, Kim Y, Eun B, Park OH, Kim H, Kim K, Park CH, Vinsant S, Oppenheim RW, Sun W. Impaired migration in the rostral migratory stream but spared olfactory function after the elimination of programmed cell death in Bax knock-out mice. J Neurosci. 2007;27:14392-403.
34. Kim WR, Park OH, Choi S, Choi SY, Park SK, Lee KJ, Rhyu IJ, Kim H, Lee YK, Kim HT, et al. The maintenance of specific aspects of neuronal function and behavior is dependent on programmed cell death of adult-generated neurons in the dentate gyrus. Eur J Neurosci. 2009;29:1408-21.
35. Alvarez-Buylla A, Lim DA. For the long run: maintaining germinal niches in the adult brain. Neuron. 2004;41:683-6.
36. Reh TA, Fischer AJ. Retinal stem cells. Methods Enzymol. 2006;419:52-73.
37. Seri B, Herrera DG, Gritti A, Ferron S, Collado L, Vescovi A, Garcia-Verdugo JM, Alvarez-Buylla A. Composition and organization of the SCZ: a large germinal layer containing neural stem cells in the adult mammalian brain. Cereb Cortex. 2006;16 Suppl 1:i103-111.
38. Takemura NU. Evidence for neurogenesis within the white matter beneath the temporal neocortex of the adult rat brain. Neuroscience. 2005;134:121-32.
39. Hugnot JP. Isolate and culture neural stem cells from the mouse adult spinal cord. Methods Mol Biol. 2013;1059:53-63.
40. Ghashghaei HT, Lai C, Anton ES. Neuronal migration in the adult brain: are we there yet? Nat Rev Neurosci. 2007;8:141-51.
41. Snapyan M, Lemasson M, Brill MS, Blais M, Massouh M, Ninkovic J, Gravel C, Berthod F, Gotz M, Barker PA, et al. Vasculature guides migrating neuronal precursors in the adult mammalian forebrain via brain-derived neurotrophic factor signaling. J Neurosci. 2009;29:4172-88.
42. Whitman MC, Fan W, Rela L, Rodriguez-Gil DJ, Greer CA. Blood vessels form a migratory scaffold in the rostral migratory stream. J Comp Neurol. 2009;516:94-104.
43. Lledo PM, Saghatelyan A. Integrating new neurons into the adult olfactory bulb: joining the network, life-death decisions, and the effects of sensory experience. Trends Neurosci. 2005;28:248-54.
44. Platel JC, Stamboulian S, Nguyen I, Bordey A. Neurotransmitter signaling in postnatal neurogenesis: The first leg. Brain Res Rev. 2010;63:60-71.
45. Garzotto D, Giacobini P, Crepaldi T, Fasolo A, De Marchis S. Hepatocyte growth factor regulates migration of olfactory interneuron precursors in the rostral migratory stream through Met-Grb2 coupling. J Neurosci. 2008;28:5901-9.
46. Wang TW, Zhang H, Gyetko MR, Parent JM. Hepatocyte growth factor acts as a mitogen and chemoattractant for postnatal subventricular zone-olfactory bulb neurogenesis. Mol Cell Neurosci. 2011;48:38-50.
47. Biebl M, Cooper CM, Winkler J, Kuhn HG. Analysis of neurogenesis and programmed cell death reveals a self-renewing capacity in the adult rat brain. Neurosci Lett. 2000;291:17-20.
48. Lois C, Alvarez-Buylla A. Long-distance neuronal migration in the adult mammalian brain. Science. 1994;264:1145-8.
49. Winner B, Cooper-Kuhn CM, Aigner R, Winkler J, Kuhn HG. Long-term survival and cell death of newly generated neurons in the adult rat olfactory bulb. Eur J Neurosci. 2002;16:1681-9.
50. Petreanu L, Alvarez-Buylla A. Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction. J Neurosci. 2002;22:6106-13.
51. Bath KG, Lee FS. Neurotrophic factor control of adult SVZ neurogenesis. Dev Neurobiol. 2010;70:339-49.
52. Hurtado-Chong A, Yusta-Boyo MJ, Vergano-Vera E, Bulfone A, de Pablo F, Vicario-Abejon C. IGF-I promotes neuronal migration and positioning in the olfactory bulb and the exit of neuroblasts from the subventricular zone. Eur J Neurosci. 2009;30:742-55.
53. Aberg ND, Johansson I, Aberg MA, Lind J, Johansson UE, Cooper-Kuhn CM, Kuhn HG, Isgaard J. Peripheral administration of GH induces cell proliferation in the brain of adult hypophysectomized rats. J Endocrinol. 2009;201:141-50.
54. Decressac M, Prestoz L, Veran J, Cantereau A, Jaber M, Gaillard A. Neuropeptide Y stimulates proliferation, migration and differentiation of neural precursors from the subventricular zone in adult mice. Neurobiol Dis. 2009;34:441-9.
55. Stanic D, Paratcha G, Ledda F, Herzog H, Kopin AS, Hokfelt T. Peptidergic influences on proliferation, migration, and placement of neural progenitors in the adult mouse forebrain. Proc Natl Acad Sci U S A. 2008;105:3610-5.
56. Kim WR, Sun W. Enhanced odor discrimination learning in aged Bax-KO mice. Neurosci Lett. 2013;548:196-200.
57. Sakamoto M, Ieki N, Miyoshi G, Mochimaru D, Miyachi H, Imura T, Yamaguchi M, Fishell G, Mori K, Kageyama R, Imayoshi I. Continuous postnatal neurogenesis contributes to formation of the olfactory bulb neural circuits and flexible olfactory associative learning. J Neurosci. 2014;34:5788-99.
58. Sakamoto M, Kageyama R, Imayoshi I. The functional significance of newly born neurons integrated into olfactory bulb circuits. Front Neurosci. 2014;8:121.
59. Feierstein CE, Lazarini F, Wagner S, Gabellec MM, de Chaumont F, Olivo-Marin JC, Boussin FD, Lledo PM, Gheusi G. Disruption of Adult Neurogenesis in the Olfactory Bulb Affects Social Interaction but not Maternal Behavior. Front Behav Neurosci. 2010;4:176.
60. Gonzalez-Perez O. Neural stem cells in the adult human brain. Biological and biomedical reports. 2012;2:59-69.
61. Quinones-Hinojosa A, Sanai N, Soriano-Navarro M, Gonzalez-Perez O, Mirzadeh Z, Gil-Perotin S, Romero-Rodriguez R, Berger MS, Garcia-Verdugo JM, Alvarez-Buylla A. Cellular composition and cytoarchitecture of the adult human subventricular zone: a niche of neural stem cells. J Comp Neurol. 2006;494:415-34.
62. Sanai N, Tramontin AD, Quinones-Hinojosa A, Barbaro NM, Gupta N, Kunwar S, Lawton MT, McDermott MW, Parsa AT, Manuel-Garcia Verdugo J, et al. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature. 2004;427:740-4.
63. Curtis MA, Kam M, Nannmark U, Anderson MF, Axell MZ, Wikkelso C, Holtas S, van Roon-Mom WM, Bjork-Eriksson T, Nordborg C, et al. Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science. 2007;315:1243-9.
64. Sanai N, Berger MS, Garcia-Verdugo JM, Alvarez-Buylla A. Comment on "Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension". Science. 2007;318:393. author reply 393.
65. Gu Y, Arruda-Carvalho M, Wang J, Janoschka SR, Josselyn SA, Frankland PW, Ge S. Optical controlling reveals time-dependent roles for adult-born dentate granule cells. Nat Neurosci. 2012;15:1700-6.
66. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH. Functional neurogenesis in the adult hippocampus. Nature. 2002;415:1030-4.
67. Zhou M, Li W, Huang S, Song J, Kim JY, Tian X, Kang E, Sano Y, Liu C, Balaji J, et al. mTOR Inhibition ameliorates cognitive and affective deficits caused by Disc1 knockdown in adult-born dentate granule neurons. Neuron. 2013;77:647-54.
68. Kumamoto N, Gu Y, Wang J, Janoschka S, Takemaru K, Levine J, Ge S. A role for primary cilia in glutamatergic synaptic integration of adult-born neurons. Nat Neurosci. 2012;15:399-405. S391.
69. Fitzsimons CP, van Hooijdonk LW, Schouten M, Zalachoras I, Brinks V, Zheng T, Schouten TG, Saaltink DJ, Dijkmans T, Steindler DA, et al. Knockdown of the glucocorticoid receptor alters functional integration of newborn neurons in the adult hippocampus and impairs fear-motivated behavior. Mol Psychiatry. 2013;18:993-1005.
70. Brandt MD, Maass A, Kempermann G, Storch A. Physical exercise increases Notch activity, proliferation and cell cycle exit of type-3 progenitor cells in adult hippocampal neurogenesis. Eur J Neurosci. 2010;32:1256-64.
71. Podda MV, Leone L, Barbati SA, Mastrodonato A, Li Puma DD, Piacentini R, Grassi C. Extremely low-frequency electromagnetic fields enhance the survival of newborn neurons in the mouse hippocampus. Eur J Neurosci. 2014;39:893-903.
72. Dayer AG, Ford AA, Cleaver KM, Yassaee M, Cameron HA. Short-term and long-term survival of new neurons in the rat dentate gyrus. J Comp Neurol. 2003;460:563-72.
73. Sun W, Winseck A, Vinsant S, Park OH, Kim H, Oppenheim RW. Programmed cell death of adult-generated hippocampal neurons is mediated by the proapoptotic gene Bax. J Neurosci. 2004;24:11205-13.
74. Spalding KL, Bergmann O, Alkass K, Bernard S, Salehpour M, Huttner HB, Bostrom E, Westerlund I, Vial C, Buchholz BA, et al. Dynamics of hippocampal neurogenesis in adult humans. Cell. 2013;153:1219-27.
75. Kim WR, Chun SK, Kim TW, Kim H, Ono K, Takebayashi H, Ikenaka K, Oppenheim RW, Sun W. Evidence for the spontaneous production but massive programmed cell death of new neurons in the subcallosal zone of the postnatal mouse brain. Eur J Neurosci. 2011;33:599-611.
76. Jovanov-Milosevic N, Petanjek Z, Petrovic D, Judas M, Kostovic I. Morphology, molecular phenotypes and distribution of neurons in developing human corpus callosum. Eur J Neurosci. 2010;32:1423-32.
77. Roy NS, Wang S, Harrison-Restelli C, Benraiss A, Fraser RA, Gravel M, Braun PE, Goldman SA. Identification, isolation, and promoter-defined separation of mitotic oligodendrocyte progenitor cells from the adult human subcortical white matter. J Neurosci. 1999;19:9986-95.
78. Nunes MC, Roy NS, Keyoung HM, Goodman RR, McKhann 2nd G, Jiang L, Kang J, Nedergaard M, Goldman SA. Identification and isolation of multipotential neural progenitor cells from the subcortical white matter of the adult human brain. Nat Med. 2003;9:439-47.
79. Dayer AG, Cleaver KM, Abouantoun T, Cameron HA. New GABAergic interneurons in the adult neocortex and striatum are generated from different precursors. J Cell Biol. 2005;168:415-27.
80. Huang L, DeVries GJ, Bittman EL. Photoperiod regulates neuronal bromodeoxyuridine labeling in the brain of a seasonally breeding mammal. J Neurobiol. 1998;36:410-20.
81. Gould E, Reeves AJ, Graziano MS, Gross CG. Neurogenesis in the neocortex of adult primates. Science. 1999;286:548-52.
82. Gould E, Vail N, Wagers M, Gross CG. Adult-generated hippocampal and neocortical neurons in macaques have a transient existence. Proc Natl Acad Sci U S A. 2001;98:10910-7.
83. Koketsu D, Mikami A, Miyamoto Y, Hisatsune T. Nonrenewal of neurons in the cerebral neocortex of adult macaque monkeys. J Neurosci. 2003;23:937-42.
84. Kornack DR, Rakic P. Cell proliferation without neurogenesis in adult primate neocortex. Science. 2001;294:2127-30.
85. Magavi SS, Leavitt BR, Macklis JD. Induction of neurogenesis in the neocortex of adult mice. Nature. 2000;405:951-5.
86. Gould E, Beylin A, Tanapat P, Reeves A, Shors TJ. Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci. 1999;2:260-5.
87. Gould E. How widespread is adult neurogenesis in mammals? Nat Rev Neurosci. 2007;8:481-8.
88. Weiss S, Dunne C, Hewson J, Wohl C, Wheatley M, Peterson AC, Reynolds BA. Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J Neurosci. 1996;16:7599-609.
89. Ohori Y, Yamamoto S, Nagao M, Sugimori M, Yamamoto N, Nakamura K, Nakafuku M. Growth factor treatment and genetic manipulation stimulate neurogenesis and oligodendrogenesis by endogenous neural progenitors in the injured adult spinal cord. J Neurosci. 2006;26:11948-60.
90. Yamamoto S, Yamamoto N, Kitamura T, Nakamura K, Nakafuku M. Proliferation of parenchymal neural progenitors in response to injury in the adult rat spinal cord. Exp Neurol. 2001;172:115-27.
91. Fiorelli R, Cebrian-Silla A, Garcia-Verdugo JM, Raineteau O. The adult spinal cord harbors a population of GFAP-positive progenitors with limited self-renewal potential. Glia. 2013;61:2100-13.
92. Hamilton LK, Truong MK, Bednarczyk MR, Aumont A, Fernandes KJ. Cellular organization of the central canal ependymal zone, a niche of latent neural stem cells in the adult mammalian spinal cord. Neuroscience. 2009;164:1044-56.
93. Meletis K, Barnabe-Heider F, Carlen M, Evergren E, Tomilin N, Shupliakov O, Frisen J. Spinal cord injury reveals multilineage differentiation of ependymal cells. PLoS Biol. 2008;6:e182.
94. Sabelstrom H, Stenudd M, Frisen J. Neural stem cells in the adult spinal cord. Exp Neurol. 2014;260:44-9.
95. Alcock J, Scotting P, Sottile V. Bergmann glia as putative stem cells of the mature cerebellum. Med Hypotheses. 2007;69:341-5.
96. Lee A, Kessler JD, Read TA, Kaiser C, Corbeil D, Huttner WB, Johnson JE, Wechsler-Reya RJ. Isolation of neural stem cells from the postnatal cerebellum. Nat Neurosci. 2005;8:723-9.
97. Klein C, Butt SJ, Machold RP, Johnson JE, Fishell G. Cerebellum- and forebrain-derived stem cells possess intrinsic regional character. Development. 2005;132:4497-508.
98. Fischer AJ, Reh TA. Potential of Muller glia to become neurogenic retinal progenitor cells. Glia. 2003;43:70-6.
99. Braisted JE, Essman TF, Raymond PA. Selective regeneration of photoreceptors in goldfish retina. Development. 1994;120:2409-19.
100. Chetty S, Friedman AR, Taravosh-Lahn K, Kirby ED, Mirescu C, Guo F, Krupik D, Nicholas A, Geraghty AC, Krishnamurthy A, et al. Stress and glucocorticoids promote oligodendrogenesis in the adult hippocampus. Mol Psychiatry. 2014;19(12):1275-83.
101. Del Debbio CB, Peng X, Xiong H, Ahmad I. Adult ciliary epithelial stem cells generate functional neurons and differentiate into both early and late born retinal neurons under non-cell autonomous influences. BMC Neurosci. 2013;14:130.
102. Kokoeva MV, Yin H, Flier JS. Neurogenesis in the hypothalamus of adult mice: potential role in energy balance. Science. 2005;310:679-83.
103. Pierce AA, Xu AW. De novo neurogenesis in adult hypothalamus as a compensatory mechanism to regulate energy balance. J Neurosci. 2010;30:723-30.
104. Lee DA, Bedont JL, Pak T, Wang H, Song J, Miranda-Angulo A, Takiar V, Charubhumi V, Balordi F, Takebayashi H, et al. Tanycytes of the hypothalamic median eminence form a diet-responsive neurogenic niche. Nat Neurosci. 2012;15:700-2.
105. Lee DA, Yoo S, Pak T, Salvatierra J, Velarde E, Aja S, Blackshaw S. Dietary and sex-specific factors regulate hypothalamic neurogenesis in young adult mice. Front Neurosci. 2014;8:157.
106. Pencea V, Bingaman KD, Wiegand SJ, Luskin MB. Infusion of brain-derived neurotrophic factor into the lateral ventricle of the adult rat leads to new neurons in the parenchyma of the striatum, septum, thalamus, and hypothalamus. J Neurosci. 2001;21:6706-17.
107. Zhao M, Momma S, Delfani K, Carlen M, Cassidy RM, Johansson CB, Brismar H, Shupliakov O, Frisen J, Janson AM. Evidence for neurogenesis in the adult mammalian substantia nigra. Proc Natl Acad Sci U S A. 2003;100:7925-30.
108. Frielingsdorf H, Schwarz K, Brundin P, Mohapel P. No evidence for new dopaminergic neurons in the adult mammalian substantia nigra. Proc Natl Acad Sci U S A. 2004;101:10177-82.
109. Shan X, Chi L, Bishop M, Luo C, Lien L, Zhang Z, Liu R. Enhanced de novo neurogenesis and dopaminergic neurogenesis in the substantia nigra of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced Parkinson's disease-like mice. Stem Cells. 2006;24:1280-7.
110. Codega P, Silva-Vargas V, Paul A, Maldonado-Soto AR, Deleo AM, Pastrana E, Doetsch F. Prospective identification and purification of quiescent adult neural stem cells from their in vivo niche. Neuron. 2014;82:545-59.
111. Kerr JF, Wyllie AH, Currie AR. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer. 1972;26:239-57.
112. Kroemer G, Galluzzi L, Vandenabeele P, Abrams J, Alnemri ES, Baehrecke EH, Blagosklonny MV, El-Deiry WS, Golstein P, Green DR, et al. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ. 2009;16:3-11.
113. Bleicken S, Landeta O, Landajuela A, Basanez G, Garcia-Saez AJ. Proapoptotic Bax and Bak proteins form stable protein-permeable pores of tunable size. J Biol Chem. 2013;288:33241-52.
114. Zou H, Li Y, Liu X, Wang X. An APAF-1.cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J Biol Chem. 1999;274:11549-56.
115. Gorman AM, Ceccatelli S, Orrenius S. Role of mitochondria in neuronal apoptosis. Dev Neurosci. 2000;22:348-58.
116. Elmore S. Apoptosis: a review of programmed cell death. Toxicol Pathol. 2007;35:495-516.
117. Gavathiotis E, Suzuki M, Davis ML, Pitter K, Bird GH, Katz SG, Tu HC, Kim H, Cheng EH, Tjandra N, Walensky LD. BAX activation is initiated at a novel interaction site. Nature. 2008;455:1076-81.
118. Czabotar PE, Westphal D, Dewson G, Ma S, Hockings C, Fairlie WD, Lee EF, Yao S, Robin AY, Smith BJ, et al. Bax crystal structures reveal how BH3 domains activate Bax and nucleate its oligomerization to induce apoptosis. Cell. 2013;152:519-31.
119. Daugas E, Susin SA, Zamzami N, Ferri KF, Irinopoulou T, Larochette N, Prevost MC, Leber B, Andrews D, Penninger J, Kroemer G. Mitochondrio-nuclear translocation of AIF in apoptosis and necrosis. FASEB J. 2000;14:729-39.
120. Kischkel FC, Lawrence DA, Chuntharapai A, Schow P, Kim KJ, Ashkenazi A. Apo2L/TRAIL-dependent recruitment of endogenous FADD and caspase-8 to death receptors 4 and 5. Immunity. 2000;12:611-20.
121. Yang Z, Klionsky DJ. Eaten alive: a history of macroautophagy. Nat Cell Biol. 2010;12:814-22.
122. De Duve C, Wattiaux R. Functions of lysosomes. Annu Rev Physiol. 1966;28:435-92.
123. Mizushima N, Yoshimori T, Levine B. Methods in mammalian autophagy research. Cell. 2010;140:313-26.
124. Denton D, Nicolson S, Kumar S. Cell death by autophagy: facts and apparent artefacts. Cell Death Differ. 2012;19:87-95.
125. Tsujimoto Y, Shimizu S. Another way to die: autophagic programmed cell death. Cell Death Differ. 2005;12 Suppl 2:1528-34.
126. Shen HM, Codogno P. Autophagic cell death: Loch Ness monster or endangered species? Autophagy. 2011;7:457-65.
127. Kawahara A, Ohsawa Y, Matsumura H, Uchiyama Y, Nagata S. Caspase-independent cell killing by Fas-associated protein with death domain. J Cell Biol. 1998;143:1353-60.
128. Degterev A, Hitomi J, Germscheid M, Ch'en IL, Korkina O, Teng X, Abbott D, Cuny GD, Yuan C, Wagner G, et al. Identification of RIP1 kinase as a specific cellular target of necrostatins. Nat Chem Biol. 2008;4:313-21.
129. Golstein P, Kroemer G. Cell death by necrosis: towards a molecular definition. Trends Biochem Sci. 2007;32:37-43.
130. Leist M, Single B, Castoldi AF, Kuhnle S, Nicotera P. Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J Exp Med. 1997;185:1481-6.
131. Pieper AA, Xie S, Capota E, Estill SJ, Zhong J, Long JM, Becker GL, Huntington P, Goldman SE, Shen CH, et al. Discovery of a proneurogenic, neuroprotective chemical. Cell. 2010;142:39-51.
132. Palmer TD, Ray J, Gage FH. FGF-2-responsive neuronal progenitors reside in proliferative and quiescent regions of the adult rodent brain. Mol Cell Neurosci. 1995;6:474-86.
133. Malone CD, Hasan SM, Roome RB, Xiong J, Furlong M, Opferman JT, Vanderluit JL. Mcl-1 regulates the survival of adult neural precursor cells. Mol Cell Neurosci. 2012;49:439-47.
134. Lindsten T, Golden JA, Zong WX, Minarcik J, Harris MH, Thompson CB. The proapoptotic activities of Bax and Bak limit the size of the neural stem cell pool. J Neurosci. 2003;23:11112-9.
135. Yu SW, Baek SH, Brennan RT, Bradley CJ, Park SK, Lee YS, Jun EJ, Lookingland KJ, Kim EK, Lee H, et al. Autophagic death of adult hippocampal neural stem cells following insulin withdrawal. Stem Cells. 2008;26:2602-10.
136. Bunk EC, Konig HG, Bernas T, Engel T, Henshall DC, Kirby BP, Prehn JH. BH3-only proteins BIM and PUMA in the regulation of survival and neuronal differentiation of newly generated cells in the adult mouse hippocampus. Cell death & disease. 2010;1:e15.
137. Fatt MP, Cancino GI, Miller FD, Kaplan DR. p63 and p73 coordinate p53 function to determine the balance between survival, cell death, and senescence in adult neural precursor cells. Cell Death Differ. 2014;21:1546-59.
138. Liu D, Ou L, Clemenson Jr GD, Chao C, Lutske ME, Zambetti GP, Gage FH, Xu Y. Puma is required for p53-induced depletion of adult stem cells. Nat Cell Biol. 2010;12:993-8.
139. Gil-Perotin S, Marin-Husstege M, Li J, Soriano-Navarro M, Zindy F, Roussel MF, Garcia-Verdugo JM, Casaccia-Bonnefil P. Loss of p53 induces changes in the behavior of subventricular zone cells: implication for the genesis of glial tumors. J Neurosci. 2006;26:1107-16.
140. van Lookeren Campagne M, Gill R. Tumor-suppressor p53 is expressed in proliferating and newly formed neurons of the embryonic and postnatal rat brain: comparison with expression of the cell cycle regulators p21Waf1/Cip1, p27Kip1, p57Kip2, p16Ink4a, cyclin G1, and the proto-oncogene Bax. J Comp Neurol. 1998;397:181-98.
141. Amson R, Lassalle JM, Halley H, Prieur S, Lethrosne F, Roperch JP, Israeli D, Gendron MC, Duyckaerts C, Checler F, et al. Behavioral alterations associated with apoptosis and down-regulation of presenilin 1 in the brains of p53-deficient mice. Proc Natl Acad Sci U S A. 2000;97:5346-50.
142. Rowland AA, Voeltz GK. Endoplasmic reticulum-mitochondria contacts: function of the junction. Nat Rev Mol Cell Biol. 2012;13:607-25.
143. De Stefani D, Bononi A, Romagnoli A, Messina A, De Pinto V, Pinton P, Rizzuto R. VDAC1 selectively transfers apoptotic Ca2+ signals to mitochondria. Cell Death Differ. 2012;19:267-73.
144. Marchi S, Marinello M, Bononi A, Bonora M, Giorgi C, Rimessi A, Pinton P. Selective modulation of subtype III IP(3)R by Akt regulates ER Ca(2)(+) release and apoptosis. Cell Death Dis. 2012;3:e304.
145. Scorrano L, Oakes SA, Opferman JT, Cheng EH, Sorcinelli MD, Pozzan T, Korsmeyer SJ. BAX and BAK regulation of endoplasmic reticulum Ca2+: a control point for apoptosis. Science. 2003;300:135-9.
146. Bassik MC, Scorrano L, Oakes SA, Pozzan T, Korsmeyer SJ. Phosphorylation of BCL-2 regulates ER Ca2+ homeostasis and apoptosis. EMBO J. 2004;23:1207-16.
147. Shi J, Parada LF, Kernie SG. Bax limits adult neural stem cell persistence through caspase and IP3 receptor activation. Cell Death Differ. 2005;12:1601-12.
148. Martin-Villalba A, Herr I, Jeremias I, Hahne M, Brandt R, Vogel J, Schenkel J, Herdegen T, Debatin KM. CD95 ligand (Fas-L/APO-1 L) and tumor necrosis factor-related apoptosis-inducing ligand mediate ischemia-induced apoptosis in neurons. J Neurosci. 1999;19:3809-17.
149. Knight JC, Scharf EL, Mao-Draayer Y. Fas activation increases neural progenitor cell survival. J Neurosci Res. 2010;88:746-57.
150. Ceccatelli S, Tamm C, Sleeper E, Orrenius S. Neural stem cells and cell death. Toxicol Lett. 2004;149:59-66.
151. Widera D, Mikenberg I, Elvers M, Kaltschmidt C, Kaltschmidt B. Tumor necrosis factor alpha triggers proliferation of adult neural stem cells via IKK/NF-kappaB signaling. BMC Neurosci. 2006;7:64.
152. Covacu R, Arvidsson L, Andersson A, Khademi M, Erlandsson-Harris H, Harris RA, Svensson MA, Olsson T, Brundin L. TLR activation induces TNF-alpha production from adult neural stem/progenitor cells. J Immunol. 2009;182:6889-95.
153. Ricci-Vitiani L, Pedini F, Mollinari C, Condorelli G, Bonci D, Bez A, Colombo A, Parati E, Peschle C, De Maria R. Absence of caspase 8 and high expression of PED protect primitive neural cells from cell death. J Exp Med. 2004;200:1257-66.
154. Jung AR, Kim TW, Rhyu IJ, Kim H, Lee YD, Vinsant S, Oppenheim RW, Sun W. Misplacement of Purkinje cells during postnatal development in Bax knock-out mice: a novel role for programmed cell death in the nervous system? J Neurosci. 2008;28:2941-8.
155. Kuhn HG, Winkler J, Kempermann G, Thal LJ, Gage FH. Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J Neurosci. 1997;17:5820-9.
156. Platel JC, Dave KA, Gordon V, Lacar B, Rubio ME, Bordey A. NMDA receptors activated by subventricular zone astrocytic glutamate are critical for neuroblast survival prior to entering a synaptic network. Neuron. 2010;65:859-72.
157. Lafourcade CA, Lin TV, Feliciano DM, Zhang L, Hsieh LS, Bordey A. Rheb activation in subventricular zone progenitors leads to heterotopia, ectopic neuronal differentiation, and rapamycin-sensitive olfactory micronodules and dendrite hypertrophy of newborn neurons. J Neurosci. 2013;33:2419-31.
158. Brandt MD, Jessberger S, Steiner B, Kronenberg G, Reuter K, Bick-Sander A, von der Behrens W, Kempermann G. Transient calretinin expression defines early postmitotic step of neuronal differentiation in adult hippocampal neurogenesis of mice. Mol Cell Neurosci. 2003;24:603-13.
159. Francis JS, Dragunow M, During MJ. Over expression of ATF-3 protects rat hippocampal neurons from in vivo injection of kainic acid. Brain Res Mol Brain Res. 2004;124:199-203.
160. Nacher J, Rosell DR, Alonso-Llosa G, McEwen BS. NMDA receptor antagonist treatment induces a long-lasting increase in the number of proliferating cells, PSA-NCAM-immunoreactive granule neurons and radial glia in the adult rat dentate gyrus. Eur J Neurosci. 2001;13:512-20.
161. Belvindrah R, Rougon G, Chazal G. Increased neurogenesis in adult mCD24-deficient mice. J Neurosci. 2002;22:3594-607.
162. Buss RR, Gould TW, Ma J, Vinsant S, Prevette D, Winseck A, Toops KA, Hammarback JA, Smith TL, Oppenheim RW. Neuromuscular development in the absence of programmed cell death: phenotypic alteration of motoneurons and muscle. J Neurosci. 2006;26:13413-27.
163. Vivar C, Potter MC, van Praag H. All about running: synaptic plasticity, growth factors and adult hippocampal neurogenesis. Curr Top Behav Neurosci. 2013;15:189-210.
164. Leuner B, Mendolia-Loffredo S, Kozorovitskiy Y, Samburg D, Gould E, Shors TJ. Learning enhances the survival of new neurons beyond the time when the hippocampus is required for memory. J Neurosci. 2004;24:7477-81.
165. van Praag H, Kempermann G, Gage FH. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci. 1999;2:266-70.
166. Tashiro A, Sandler VM, Toni N, Zhao C, Gage FH. NMDA-receptor-mediated, cell-specific integration of new neurons in adult dentate gyrus. Nature. 2006;442:929-33.
167. Hastings NB, Gould E. Rapid extension of axons into the CA3 region by adult-generated granule cells. J Comp Neurol. 1999;413:146-54.
168. Markakis EA, Gage FH. Adult-generated neurons in the dentate gyrus send axonal projections to field CA3 and are surrounded by synaptic vesicles. J Comp Neurol. 1999;406:449-60.
169. Zhao C, Teng EM, Summers Jr RG, Ming GL, Gage FH. Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J Neurosci. 2006;26:3-11.
170. Belluzzi O, Benedusi M, Ackman J, LoTurco JJ. Electrophysiological differentiation of new neurons in the olfactory bulb. J Neurosci. 2003;23:10411-8.
171. Carleton A, Petreanu LT, Lansford R, Alvarez-Buylla A, Lledo PM. Becoming a new neuron in the adult olfactory bulb. Nat Neurosci. 2003;6:507-18.
172. Wang S, Scott BW, Wojtowicz JM. Heterogenous properties of dentate granule neurons in the adult rat. J Neurobiol. 2000;42:248-57.
173. Sun W, Gould TW, Vinsant S, Prevette D, Oppenheim RW. Neuromuscular development after the prevention of naturally occurring neuronal death by Bax deletion. J Neurosci. 2003;23:7298-310.
174. Sahay A, Scobie KN, Hill AS, O'Carroll CM, Kheirbek MA, Burghardt NS, Fenton AA, Dranovsky A, Hen R. Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature. 2011;472:466-70.
175. Snyder JS, Kee N, Wojtowicz JM. Effects of adult neurogenesis on synaptic plasticity in the rat dentate gyrus. J Neurophysiol. 2001;85:2423-31.
176. Esposito MS, Piatti VC, Laplagne DA, Morgenstern NA, Ferrari CC, Pitossi FJ, Schinder AF. Neuronal differentiation in the adult hippocampus recapitulates embryonic development. J Neurosci. 2005;25:10074-86.
177. Tozuka Y, Fukuda S, Namba T, Seki T, Hisatsune T. GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron. 2005;47:803-15.
178. Lee JW, Kim WR, Sun W, Jung MW. Disruption of dentate gyrus blocks effect of visual input on spatial firing of CA1 neurons. J Neurosci. 2012;32:12999-3003.
179. Yamaguchi M, Mori K. Critical period for sensory experience-dependent survival of newly generated granule cells in the adult mouse olfactory bulb. Proc Natl Acad Sci U S A. 2005;102:9697-702.
180. Ha S, Ryu HY, Chung KM, Baek SH, Kim EK, Yu SW. Regulation of autophagic cell death by glycogen synthase kinase-3beta in adult hippocampal neural stem cells following insulin withdrawal. Mol Brain. 2015;8:30.
181. Xia HG, Zhang L, Chen G, Zhang T, Liu J, Jin M, Ma X, Ma D, Yuan J. Control of basal autophagy by calpain1 mediated cleavage of ATG5. Autophagy. 2010;6:61-6.
182. Chung KM, Park H, Jung S, Ha S, Yoo SJ, Woo H, Lee HJ, Kim SW, Kim EK, Moon C, Yu SW. Calpain determines the propensity of adult Hippocampal neural stem cells to autophagic cell death following insulin withdrawal. Stem Cells. 2015;33(10):3052-64.
183. Yazdankhah M, Farioli-Vecchioli S, Tonchev AB, Stoykova A, Cecconi F. The autophagy regulators Ambra1 and Beclin 1 are required for adult neurogenesis in the brain subventricular zone. Cell death & disease. 2014;5:e1403.
184. Fields RD, Burnstock G. Purinergic signalling in neuron-glia interactions. Nat Rev Neurosci. 2006;7:423-36.
185. Zheng LM, Zychlinsky A, Liu CC, Ojcius DM, Young JD. Extracellular ATP as a trigger for apoptosis or programmed cell death. J Cell Biol. 1991;112:279-88.
186. Jun DJ, Kim J, Jung SY, Song R, Noh JH, Park YS, Ryu SH, Kim JH, Kong YY, Chung JM, Kim KT. Extracellular ATP mediates necrotic cell swelling in SN4741 dopaminergic neurons through P2X7 receptors. J Biol Chem. 2007;282:37350-8.
187. Messemer N, Kunert C, Grohmann M, Sobottka H, Nieber K, Zimmermann H, Franke H, Norenberg W, Straub I, Schaefer M, et al. P2X7 receptors at adult neural progenitor cells of the mouse subventricular zone. Neuropharmacology. 2013;73:122-37.
188. Delarasse C, Gonnord P, Galante M, Auger R, Daniel H, Motta I, Kanellopoulos JM. Neural progenitor cell death is induced by extracellular ATP via ligation of P2X7 receptor. J Neurochem. 2009;109:846-57.
189. Suh H, Deng W, Gage FH. Signaling in adult neurogenesis. Annu Rev Cell Dev Biol. 2009;25:253-75.
190. Ming GL, Song H. Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron. 2011;70:687-702.
191. Ihrie RA, Alvarez-Buylla A. Lake-front property: a unique germinal niche by the lateral ventricles of the adult brain. Neuron. 2011;70:674-86.
192. Tavazoie M, Van der Veken L, Silva-Vargas V, Louissaint M, Colonna L, Zaidi B, Garcia-Verdugo JM, Doetsch F. A specialized vascular niche for adult neural stem cells. Cell Stem Cell. 2008;3:279-88.
193. Brazel CY, Nunez JL, Yang Z, Levison SW. Glutamate enhances survival and proliferation of neural progenitors derived from the subventricular zone. Neuroscience. 2005;131:55-65.
194. Sierra A, Martin-Suarez S, Valcarcel-Martin R, Pascual-Brazo J, Aelvoet SA, Abiega O, Deudero JJ, Brewster AL, Bernales I, Anderson AE, et al. Neuronal hyperactivity accelerates depletion of neural stem cells and impairs hippocampal neurogenesis. Cell Stem Cell. 2015;16:488-503.
195. O'Neill C, Kiely AP, Coakley MF, Manning S, Long-Smith CM. Insulin and IGF-1 signalling: longevity, protein homoeostasis and Alzheimer's disease. Biochem Soc Trans. 2012;40:721-7.
196. Bassil F, Fernagut PO, Bezard E, Meissner WG. Insulin, IGF-1 and GLP-1 signaling in neurodegenerative disorders: targets for disease modification? Prog Neurobiol. 2014;118:1-18.
197. Anderson MF, Aberg MA, Nilsson M, Eriksson PS. Insulin-like growth factor-I and neurogenesis in the adult mammalian brain. Brain Res Dev Brain Res. 2002;134:115-22.
198. O'Kusky JR, Ye P, D'Ercole AJ. Insulin-like growth factor-I promotes neurogenesis and synaptogenesis in the hippocampal dentate gyrus during postnatal development. J Neurosci. 2000;20:8435-42.
199. Liu W, Ye P, O'Kusky JR, D'Ercole AJ. Type 1 insulin-like growth factor receptor signaling is essential for the development of the hippocampal formation and dentate gyrus. J Neurosci Res. 2009;87:2821-32.
200. Huang EJ, Reichardt LF. Neurotrophins: roles in neuronal development and function. Annu Rev Neurosci. 2001;24:677-736.
201. Snider WD. Functions of the neurotrophins during nervous system development: what the knockouts are teaching us. Cell. 1994;77:627-38.
202. Lambiase A, Rama P, Bonini S, Caprioglio G, Aloe L. Topical treatment with nerve growth factor for corneal neurotrophic ulcers. N Engl J Med. 1998;338:1174-80.
203. McAllister AK. Neurotrophins and neuronal differentiation in the central nervous system. Cell Mol Life Sci. 2001;58:1054-60.
204. Frielingsdorf H, Simpson DR, Thal LJ, Pizzo DP. Nerve growth factor promotes survival of new neurons in the adult hippocampus. Neurobiol Dis. 2007;26:47-55.
205. Lee J, Duan W, Mattson MP. Evidence that brain-derived neurotrophic factor is required for basal neurogenesis and mediates, in part, the enhancement of neurogenesis by dietary restriction in the hippocampus of adult mice. J Neurochem. 2002;82:1367-75.
206. Nguyen N, Lee SB, Lee YS, Lee KH, Ahn JY. Neuroprotection by NGF and BDNF against neurotoxin-exerted apoptotic death in neural stem cells are mediated through Trk receptors, activating PI3-kinase and MAPK pathways. Neurochem Res. 2009;34:942-51.
207. Lee JS, Jang DJ, Lee N, Ko HG, Kim H, Kim YS, Kim B, Son J, Kim SH, Chung H, et al. Induction of neuronal vascular endothelial growth factor expression by cAMP in the dentate gyrus of the hippocampus is required for antidepressant-like behaviors. J Neurosci. 2009;29:8493-505.
208. Snyder JS, Radik R, Wojtowicz JM, Cameron HA. Anatomical gradients of adult neurogenesis and activity: young neurons in the ventral dentate gyrus are activated by water maze training. Hippocampus. 2009;19:360-70.
209. Yoshimizu T, Chaki S. Increased cell proliferation in the adult mouse hippocampus following chronic administration of group II metabotropic glutamate receptor antagonist, MGS0039. Biochem Biophys Res Commun. 2004;315:493-6.
210. Bunk EC, Konig HG, Prehn JH, Kirby BP. Effect of the N-methyl-D-aspartate NR2B subunit antagonist ifenprodil on precursor cell proliferation in the hippocampus. J Neurosci Res. 2014;92:679-91.
211. Fiske BK, Brunjes PC. NMDA receptor regulation of cell death in the rat olfactory bulb. J Neurobiol. 2001;47:223-32.
212. Castiglione M, Calafiore M, Costa L, Sortino MA, Nicoletti F, Copani A. Group I metabotropic glutamate receptors control proliferation, survival and differentiation of cultured neural progenitor cells isolated from the subventricular zone of adult mice. Neuropharmacology. 2008;55:560-7.
213. Song J, Sun J, Moss J, Wen Z, Sun GJ, Hsu D, Zhong C, Davoudi H, Christian KM, Toni N, et al. Parvalbumin interneurons mediate neuronal circuitry-neurogenesis coupling in the adult hippocampus. Nat Neurosci. 2013;16:1728-30.
214. Giachino C, De Marchis S, Giampietro C, Parlato R, Perroteau I, Schutz G, Fasolo A, Peretto P. cAMP response element-binding protein regulates differentiation and survival of newborn neurons in the olfactory bulb. J Neurosci. 2005;25:10105-18.
215. Jagasia R, Steib K, Englberger E, Herold S, Faus-Kessler T, Saxe M, Gage FH, Song H, Lie DC. GABA-cAMP response element-binding protein signaling regulates maturation and survival of newly generated neurons in the adult hippocampus. J Neurosci. 2009;29:7966-77.
216. Benninghoff J, Gritti A, Rizzi M, Lamorte G, Schloesser RJ, Schmitt A, Robel S, Genius J, Moessner R, Riederer P, et al. Serotonin depletion hampers survival and proliferation in neurospheres derived from adult neural stem cells. Neuropsychopharmacology. 2010;35:893-903.
217. Diaz SL, Narboux-Neme N, Trowbridge S, Scotto-Lomassese S, Kleine Borgmann FB, Jessberger S, Giros B, Maroteaux L, Deneris E, Gaspar P. Paradoxical increase in survival of newborn neurons in the dentate gyrus of mice with constitutive depletion of serotonin. Eur J Neurosci. 2013;38:2650-8.
218. Djavadian RL. Serotonin and neurogenesis in the hippocampal dentate gyrus of adult mammals. Acta Neurobiol Exp. 2004;64:189-200.
219. Chiu WH, Carlsson T, Depboylu C, Hoglinger GU, Oertel WH, Ries V. Selegiline normalizes, while l-DOPA sustains the increased number of dopamine neurons in the olfactory bulb in a 6-OHDA mouse model of Parkinson's disease. Neuropharmacology. 2014;79:212-21.
220. Takamura N, Nakagawa S, Masuda T, Boku S, Kato A, Song N, An Y, Kitaichi Y, Inoue T, Koyama T, Kusumi I. The effect of dopamine on adult hippocampal neurogenesis. Prog Neuro-Psychopharmacol Biol Psychiatry. 2014;50:116-24.
221. Campbell NR, Fernandes CC, Halff AW, Berg DK. Endogenous signaling through alpha7-containing nicotinic receptors promotes maturation and integration of adult-born neurons in the hippocampus. J Neurosci. 2010;30:8734-44.
222. Bruel-Jungerman E, Lucassen PJ, Francis F. Cholinergic influences on cortical development and adult neurogenesis. Behav Brain Res. 2011;221:379-88.
223. Cooper-Kuhn CM, Winkler J, Kuhn HG. Decreased neurogenesis after cholinergic forebrain lesion in the adult rat. J Neurosci Res. 2004;77:155-65.
224. Kaneko N, Okano H, Sawamoto K. Role of the cholinergic system in regulating survival of newborn neurons in the adult mouse dentate gyrus and olfactory bulb. Genes Cells. 2006;11:1145-59.
225. Mohapel P, Leanza G, Kokaia M, Lindvall O. Forebrain acetylcholine regulates adult hippocampal neurogenesis and learning. Neurobiol Aging. 2005;26:939-46.
226. Malaterre J, Ramsay RG, Mantamadiotis T. Wnt-Frizzled signalling and the many paths to neural development and adult brain homeostasis. Front Biosci. 2007;12:492-506.
227. Lie DC, Colamarino SA, Song HJ, Desire L, Mira H, Consiglio A, Lein ES, Jessberger S, Lansford H, Dearie AR, Gage FH. Wnt signalling regulates adult hippocampal neurogenesis. Nature. 2005;437:1370-5.
228. Machold R, Hayashi S, Rutlin M, Muzumdar MD, Nery S, Corbin JG, Gritli-Linde A, Dellovade T, Porter JA, Rubin LL, et al. Sonic hedgehog is required for progenitor cell maintenance in telencephalic stem cell niches. Neuron. 2003;39:937-50.
229. Kuwabara T, Hsieh J, Muotri A, Yeo G, Warashina M, Lie DC, Moore L, Nakashima K, Asashima M, Gage FH. Wnt-mediated activation of NeuroD1 and retro-elements during adult neurogenesis. Nat Neurosci. 2009;12:1097-105.
230. Jang MH, Bonaguidi MA, Kitabatake Y, Sun J, Song J, Kang E, Jun H, Zhong C, Su Y, Guo JU, et al. Secreted frizzled-related protein 3 regulates activity-dependent adult hippocampal neurogenesis. Cell Stem Cell. 2013;12:215-23.
231. Zhou L, Fester L, Haghshenas S, de Vrese X, von Hacht R, Gloger S, Brandt N, Bader M, Vollmer G, Rune GM. Oestradiol-induced synapse formation in the female hippocampus: roles of oestrogen receptor subtypes. J Neuroendocrinol. 2014;26:439-47.
232. Hamson DK, Wainwright SR, Taylor JR, Jones BA, Watson NV, Galea LA. Androgens increase survival of adult-born neurons in the dentate gyrus by an androgen receptor-dependent mechanism in male rats. Endocrinology. 2013;154:3294-304.
233. Banasr M, Hery M, Brezun JM, Daszuta A. Serotonin mediates oestrogen stimulation of cell proliferation in the adult dentate gyrus. Eur J Neurosci. 2001;14:1417-24.
234. Shingo T, Gregg C, Enwere E, Fujikawa H, Hassam R, Geary C, Cross JC, Weiss S. Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin. Science. 2003;299:117-20.
235. Furuta M, Bridges RS. Gestation-induced cell proliferation in the rat brain. Brain Res Dev Brain Res. 2005;156:61-6.
236. Zhang Z, Yang R, Zhou R, Li L, Sokabe M, Chen L. Progesterone promotes the survival of newborn neurons in the dentate gyrus of adult male mice. Hippocampus. 2010;20:402-12.
237. Marin-Burgin A, Mongiat LA, Pardi MB, Schinder AF. Unique processing during a period of high excitation/inhibition balance in adult-born neurons. Science. 2012;335:1238-42.
238. Mirescu C, Gould E. Stress and adult neurogenesis. Hippocampus. 2006;16:233-8.
239. Kempermann G, Brandon EP, Gage FH. Environmental stimulation of 129/SvJ mice causes increased cell proliferation and neurogenesis in the adult dentate gyrus. Curr Biol. 1998;8:939-42.
240. Kempermann G, Chesler EJ, Lu L, Williams RW, Gage FH. Natural variation and genetic covariance in adult hippocampal neurogenesis. Proc Natl Acad Sci U S A. 2006;103:780-5.
241. Wu CW, Chang YT, Yu L, Chen HI, Jen CJ, Wu SY, Lo CP, Kuo YM. Exercise enhances the proliferation of neural stem cells and neurite growth and survival of neuronal progenitor cells in dentate gyrus of middle-aged mice. J Appl Physiol. 2008;105:1585-94.
242. Rochefort C, Gheusi G, Vincent JD, Lledo PM. Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J Neurosci. 2002;22:2679-89.
243. Rochefort C, Lledo PM. Short-term survival of newborn neurons in the adult olfactory bulb after exposure to a complex odor environment. Eur J Neurosci. 2005;22:2863-70.
244. Corotto FS, Henegar JR, Maruniak JA. Odor deprivation leads to reduced neurogenesis and reduced neuronal survival in the olfactory bulb of the adult mouse. Neuroscience. 1994;61:739-44.
245. Alonso M, Viollet C, Gabellec MM, Meas-Yedid V, Olivo-Marin JC, Lledo PM. Olfactory discrimination learning increases the survival of adult-born neurons in the olfactory bulb. J Neurosci. 2006;26:10508-13.
246. Gould E, Tanapat P, McEwen BS, Flugge G, Fuchs E. Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc Natl Acad Sci U S A. 1998;95:3168-71.
247. Van Bokhoven P, Oomen CA, Hoogendijk WJ, Smit AB, Lucassen PJ, Spijker S. Reduction in hippocampal neurogenesis after social defeat is long-lasting and responsive to late antidepressant treatment. Eur J Neurosci. 2011;33:1833-40.
248. Lagace DC, Donovan MH, DeCarolis NA, Farnbauch LA, Malhotra S, Berton O, Nestler EJ, Krishnan V, Eisch AJ. Adult hippocampal neurogenesis is functionally important for stress-induced social avoidance. Proc Natl Acad Sci U S A. 2010;107:4436-41.
249. Bruel-Jungerman E, Davis S, Rampon C, Laroche S. Long-term potentiation enhances neurogenesis in the adult dentate gyrus. J Neurosci. 2006;26:5888-93.
250. Chun SK, Sun W, Park JJ, Jung MW. Enhanced proliferation of progenitor cells following long-term potentiation induction in the rat dentate gyrus. Neurobiol Learn Mem. 2006;86:322-9.
251. Jukkola PI, Rogers JT, Kaspar BK, Weeber EJ, Nishijima I. Secretin deficiency causes impairment in survival of neural progenitor cells in mice. Hum Mol Genet. 2011;20:1000-7.
252. Sairanen M, Lucas G, Ernfors P, Castren M, Castren E. Brain-derived neurotrophic factor and antidepressant drugs have different but coordinated effects on neuronal turnover, proliferation, and survival in the adult dentate gyrus. J Neurosci. 2005;25:1089-94.
253. Cameron HA, Gould E. Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience. 1994;61:203-9.
254. Kobilo T, Liu QR, Gandhi K, Mughal M, Shaham Y, van Praag H. Running is the neurogenic and neurotrophic stimulus in environmental enrichment. Learn Mem. 2011;18:605-9.
255. Glasper ER, Llorens-Martin MV, Leuner B, Gould E, Trejo JL. Blockade of insulin-like growth factor-I has complex effects on structural plasticity in the hippocampus. Hippocampus. 2010;20:706-12.
256. Yoshihara S, Takahashi H, Tsuboi A. Molecular Mechanisms Regulating the Dendritic Development of Newborn Olfactory Bulb Interneurons in a Sensory Experience-Dependent Manner. Front Neurosci. 2015;9:514.
257. Yon MA, Mauger SL, Pickavance LC. Relationships between dietary macronutrients and adult neurogenesis in the regulation of energy metabolism. Br J Nutr. 2013;109:1573-89.
258. Siervo M, Arnold R, Wells JC, Tagliabue A, Colantuoni A, Albanese E, Brayne C, Stephan BC. Intentional weight loss in overweight and obese individuals and cognitive function: a systematic review and meta-analysis. Obes Rev. 2011;12:968-83.
259. Garza JC, Guo M, Zhang W, Lu XY. Leptin increases adult hippocampal neurogenesis in vivo and in vitro. J Biol Chem. 2008;283:18238-47.
260. Moon M, Kim S, Hwang L, Park S. Ghrelin regulates hippocampal neurogenesis in adult mice. Endocr J. 2009;56:525-31.
261. Zhang W, Hu Y, Lin TR, Fan Y, Mulholland MW. Stimulation of neurogenesis in rat nucleus of the solitary tract by ghrelin. Peptides. 2005;26:2280-8.
262. Stranahan AM, Arumugam TV, Cutler RG, Lee K, Egan JM, Mattson MP. Diabetes impairs hippocampal function through glucocorticoid-mediated effects on new and mature neurons. Nat Neurosci. 2008;11:309-17.
263. Guo J, Yu C, Li H, Liu F, Feng R, Wang H, Meng Y, Li Z, Ju G, Wang J. Impaired neural stem/progenitor cell proliferation in streptozotocin-induced and spontaneous diabetic mice. Neurosci Res. 2010;68:329-36.
264. Olariu A, Cleaver KM, Cameron HA. Decreased neurogenesis in aged rats results from loss of granule cell precursors without lengthening of the cell cycle. J Comp Neurol. 2007;501:659-67.
265. Belluardo N, Mudo G, Bonomo A, Di Liberto V, Frinchi M, Fuxe K. Nicotine-induced fibroblast growth factor-2 restores the age-related decline of precursor cell proliferation in the subventricular zone of rat brain. Brain Res. 2008;1193:12-24.
266. Bouab M, Paliouras GN, Aumont A, Forest-Berard K, Fernandes KJ. Aging of the subventricular zone neural stem cell niche: evidence for quiescence-associated changes between early and mid-adulthood. Neuroscience. 2011;173:135-49.
267. Luo J, Daniels SB, Lennington JB, Notti RQ, Conover JC. The aging neurogenic subventricular zone. Aging Cell. 2006;5:139-52.
268. Rao MS, Hattiangady B, Shetty AK. The window and mechanisms of major age-related decline in the production of new neurons within the dentate gyrus of the hippocampus. Aging Cell. 2006;5:545-58.
269. Kim HJ, Kim JY, Sun W. Age-dependent changes in the subcallosal zone neurogenesis of mice. Neurochem Int. 2012;61:879-84.
270. Encinas JM, Sierra A. Neural stem cell deforestation as the main force driving the age-related decline in adult hippocampal neurogenesis. Behav Brain Res. 2012;227:433-9.
271. Meletis K, Wirta V, Hede SM, Nister M, Lundeberg J, Frisen J. p53 suppresses the self-renewal of adult neural stem cells. Development. 2006;133:363-9.
272. Furutachi S, Matsumoto A, Nakayama KI, Gotoh Y. p57 controls adult neural stem cell quiescence and modulates the pace of lifelong neurogenesis. EMBO J. 2013;32:970-81.