Adult neurogenesis and gliogenesis: Possible mechanisms for neurorestoration

Experimental Neurobiology

Volumn 25, Issue 3, 2016, Pages 103-112

  Rusznák, Zoltán ^a,d   Henskens, Willem ^a,b   Schofield, Emma ^a   Kim, Woojin S ^a,c   Fu, Yu Hong ^a,c  

^a NEUROSCIENCE RESEARCH AUSTRALIA   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

^d AUSTRALIAN CATHOLIC UNIVERSITY   (Australia)

Author keywords

Aging; Gliogenesis; Neurodegeneration; Neurogenesis; Neurorestoration

Indexed keywords

EID: 84995554090     PISSN: 12262560     EISSN: 20938144     Source Type: Journal    
DOI: 10.5607/en.2016.25.3.103     Document Type: Article

References (107)

1. Bergmann O, Frisén J (2013) Neuroscience. Why adults need new brain cells. Science 340:695-696.
2. Braun SM, Jessberger S (2014) Adult neurogenesis: mechanisms and functional significance. Development 141:1983-1986.
3. Winner B, Winkler J (2015) Adult neurogenesis in neurodegenerative diseases. Cold Spring Harb Perspect Biol 7:a021287.
4. Choi SS, Lee SR, Lee HJ (2016). Neurorestorative role of stem cells in Alzheimer's disease: astrocyte involvement. Curr Alzheimer Res 13:419-427.
5. Marxreiter F, Regensburger M, Winkler J (2013) Adult neurogenesis in Parkinson's disease. Cell Mol Life Sci 70:459-473.
6. Gil-Mohapel J, Simpson JM, Ghilan M, Christie BR (2011) Neurogenesis in Huntington's disease: can studying adult neurogenesis lead to the development of new therapeutic strategies? Brain Res 1406:84-105.
7. Nait-Oumesmar B, Picard-Riéra N, Kerninon C, Baron-Van Evercooren A (2008) The role of SVZ-derived neural precursors in demyelinating diseases: from animal models to multiple sclerosis. J Neurol Sci 265:26-31.
8. Foltynie T (2015) Can Parkinson's disease be cured by stimulating neurogenesis? J Clin Invest 125:978-980.
9. Bonfanti L, Peretto P (2011) Adult neurogenesis in mammals-a theme with many variations. Eur J Neurosci 34:930-950.
10. Peretto P, Bonfanti L (2015) Adult neurogenesis 20 years later: physiological function vs. brain repair. Front Neurosci 9:71.
11. Ernst A, Frisén J (2015) Adult neurogenesis in humanscommon and unique traits in mammals. PLoS Biol 13:e1002045.
12. Magnusson JP, Frisén J (2016) Stars from the darkest night: unlocking the neurogenic potential of astrocytes in different brain regions. Development 143:1075-1086.
13. Spalding KL, Bergmann O, Alkass K, Bernard S, Salehpour M, Huttner HB, Boström E, Westerlund I, Vial C, Buchholz BA, Possnert G, Mash DC, Druid H, Frisén J (2013) Dynamics of hippocampal neurogenesis in adult humans. Cell 153:1219-1227.
14. Bergmann O, Liebl J, Bernard S, Alkass K, Yeung MS, Steier P, Kutschera W, Johnson L, Landén M, Druid H, Spalding KL, Frisén J (2012) The age of olfactory bulb neurons in humans. Neuron 74:634-639.
15. Ernst A, Alkass K, Bernard S, Salehpour M, Perl S, Tisdale J, Possnert G, Druid H, Frisén J (2014) Neurogenesis in the striatum of the adult human brain. Cell 156:1072-1083.
16. Spalding KL, Bhardwaj RD, Buchholz BA, Druid H, Frisén J (2005) Retrospective birth dating of cells in humans. Cell 122:133-143.
17. Huttner HB, Bergmann O, Salehpour M, Rácz A, Tatarishvili J, Lindgren E, Csonka T, Csiba L, Hortobágyi T, Méhes G, Englund E, Solnestam BW, Zdunek S, Scharenberg C, Ström L, Ståhl P, Sigurgeirsson B, Dahl A, Schwab S, Possnert G, Bernard S, Kokaia Z, Lindvall O, Lundeberg J, Frisén J (2014) The age and genomic integrity of neurons after cortical stroke in humans. Nat Neurosci 17:801-803.
18. Houweling AR, Brecht M (2008) Behavioural report of single neuron stimulation in somatosensory cortex. Nature 451:65-68.
19. Snyder JS, Radik R, Wojtowicz JM, Cameron HA (2009) Anatomical gradients of adult neurogenesis and activity: young neurons in the ventral dentate gyrus are activated by water maze training. Hippocampus 19:360-370.
20. Kang HJ, Kawasawa YI, Cheng F, Zhu Y, Xu X, Li M, Sousa AM, Pletikos M, Meyer KA, Sedmak G, Guennel T, Shin Y, Johnson MB, Krsnik Z, Mayer S, Fertuzinhos S, Umlauf S, Lisgo SN, Vortmeyer A, Weinberger DR, Mane S, Hyde TM, Huttner A, Reimers M, Kleinman JE, Sestan N (2011) Spatiotemporal transcriptome of the human brain. Nature 478:483-489.
21. Bonfanti L (2013) The (real) neurogenic/gliogenic potential of the postnatal and adult brain parenchyma. ISRN Neurosci 2013:354136.
22. Belachew S, Chittajallu R, Aguirre AA, Yuan X, Kirby M, Anderson S, Gallo V (2003) Postnatal NG2 proteoglycanexpressing progenitor cells are intrinsically multipotent and generate functional neurons. J Cell Biol 161:169-186.
23. Yokoyama A, Yang L, Itoh S, Mori K, Tanaka J (2004) Microglia, a potential source of neurons, astrocytes, and oligodendrocytes. Glia 45:96-104.
24. Rieske P, Azizi SA, Augelli B, Gaughan J, Krynska B (2007) A population of human brain parenchymal cells express markers of glial, neuronal and early neural cells and differentiate into cells of neuronal and glial lineages. Eur J Neurosci 25:31-37.
25. Huttner WB (2015) Stem cells: slow and steady wins the race. Nat Neurosci 18:613-614.
26. Katsimpardi L, Litterman NK, Schein PA, Miller CM, Loffredo FS, Wojtkiewicz GR, Chen JW, Lee RT, Wagers AJ, Rubin LL (2014) Vascular and neurogenic rejuvenation of the aging mouse brain by young systemic factors. Science 344:630-634.
27. Yousef H, Conboy MJ, Morgenthaler A, Schlesinger C, Bugaj L, Paliwal P, Greer C, Conboy IM, Schaffer D (2015) Systemic attenuation of the TGF-beta pathway by a single drug simultaneously rejuvenates hippocampal neurogenesis and myogenesis in the same old mammal. Oncotarget 6:11959-11978.
28. Curtis MA, Low VF, Faull RL (2012) Neurogenesis and progenitor cells in the adult human brain: a comparison between hippocampal and subventricular progenitor proliferation. Dev Neurobiol 72:990-1005.
29. Lepousez G, Nissant A, Lledo PM (2015) Adult neurogenesis and the future of the rejuvenating brain circuits. Neuron 86:387-401.
30. Snyder JS, Choe JS, Clifford MA, Jeurling SI, Hurley P, Brown A, Kamhi JF, Cameron HA (2009) Adult-born hippocampal neurons are more numerous, faster maturing, and more involved in behavior in rats than in mice. J Neurosci 29:14484-14495.
31. Ramirez-Amaya V, Marrone DF, Gage FH, Worley PF, Barnes CA (2006) Integration of new neurons into functional neural networks. J Neurosci 26:12237-12241.
32. Cameron HA, Glover LR (2015) Adult neurogenesis: beyond learning and memory. Annu Rev Psychol 66:53-81.
33. Vivar C (2015) Adult hippocampal neurogenesis, aging and neurodegenerative diseases: possible strategies to prevent cognitive impairment. Curr Top Med Chem 15:2175-2192.
34. Martinez-Canabal A (2014) Reconsidering hippocampal neurogenesis in Alzheimer's disease. Front Neurosci 8:147.
35. Voss MW, Vivar C, Kramer AF, van Praag H (2013) Bridging animal and human models of exercise-induced brain plasticity. Trends Cogn Sci 17:525-544.
36. Singh C, Liu L, Wang JM, Irwin RW, Yao J, Chen S, Henry S, Thompson RF, Brinton RD (2012) Allopregnanolone restores hippocampal-dependent learning and memory and neural progenitor survival in aging 3xTgAD and nonTg mice. Neurobiol Aging 33:1493-1506.
37. Opendak M, Gould E (2015) Adult neurogenesis: a substrate for experience-dependent change. Trends Cogn Sci 19:151-161.
38. Bouchard J, Villeda SA (2015) Aging and brain rejuvenation as systemic events. J Neurochem 132:5-19.
39. Irwin RW, Solinsky CM, Loya CM, Salituro FG, Rodgers KE, Bauer G, Rogawski MA, Brinton RD (2015) Allopregnanolone preclinical acute pharmacokinetic and pharmacodynamic studies to predict tolerability and efficacy for Alzheimer's disease. PLoS One 10:e0128313.
40. Lazarini F, Gabellec MM, Moigneu C, de Chaumont F, Olivo-Marin JC, Lledo PM (2014) Adult neurogenesis restores dopaminergic neuronal loss in the olfactory bulb. J Neurosci 34:14430-14442.
41. Gheusi G, Lepousez G, Lledo PM (2013) Adult-born neurons in the olfactory bulb: integration and functional consequences. Curr Top Behav Neurosci 15:49-72.
42. Alvarez-Buylla A, Garcia-Verdugo JM (2002) Neurogenesis in adult subventricular zone. J Neurosci 22:629-634.
43. Sakamoto M, Kageyama R, Imayoshi I (2014) The functional significance of newly born neurons integrated into olfactory bulb circuits. Front Neurosci 8:121.
44. Merkle FT, Fuentealba LC, Sanders TA, Magno L, Kessaris N, Alvarez-Buylla A (2014) Adult neural stem cells in distinct microdomains generate previously unknown interneuron types. Nat Neurosci 17:207-214.
45. Wang W, Lu S, Li T, Pan YW, Zou J, Abel GM, Xu L, Storm DR, Xia Z (2015) Inducible activation of ERK5 MAP kinase enhances adult neurogenesis in the olfactory bulb and improves olfactory function. J Neurosci 35:7833-7849.
46. Persson L, Witt RM, Galligan M, Greer PL, Eisner A, Pazyra-Murphy MF, Datta SR, Segal RA (2014) Shh-proteoglycan interactions regulate maturation of olfactory glomerular circuitry. Dev Neurobiol 74:1255-1267.
47. Aguirre A, Gallo V (2004) Postnatal neurogenesis and gliogenesis in the olfactory bulb from NG2-expressing progenitors of the subventricular zone. J Neurosci 24:10530-10541.
48. Maresh A, Rodriguez Gil D, Whitman MC, Greer CA (2008) Principles of glomerular organization in the human olfactory bulb-implications for odor processing. PLoS One 3:e2640.
49. Huisman E, Uylings HB, Hoogland PV (2004) A 100% increase of dopaminergic cells in the olfactory bulb may explain hyposmia in Parkinson's disease. Mov Disord 19:687-692.
50. Maheu ME, Devorak J, Freibauer A, Davoli MA, Turecki G, Mechawar N (2015) Increased doublecortin (DCX) expression and incidence of DCX-immunoreactive multipolar cells in the subventricular zone-olfactory bulb system of suicides. Front Neuroanat 9:74.
51. Knoth R, Singec I, Ditter M, Pantazis G, Capetian P, Meyer RP, 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:e8809.
52. Sanai N, Nguyen T, Ihrie RA, Mirzadeh Z, Tsai HH, Wong M, Gupta N, Berger MS, Huang E, Garcia-Verdugo JM, Rowitch DH, Alvarez-Buylla A (2011) Corridors of migrating neurons in the human brain and their decline during infancy. Nature 478:382-386.
53. Paez-Gonzalez P, Asrican B, Rodriguez E, Kuo CT (2014) Identification of distinct ChAT(+) neurons and activitydependent control of postnatal SVZ neurogenesis. Nat Neurosci 17:934-942.
54. Young SZ, Taylor MM, Bordey A (2011) Neurotransmitters couple brain activity to subventricular zone neurogenesis. Eur J Neurosci 33:1123-1132.
55. Tong CK, Chen J, Cebrián-Silla A, Mirzadeh Z, Obernier K, Guinto CD, Tecott LH, García-Verdugo JM, Kriegstein A, Alvarez-Buylla A (2014) Axonal control of the adult neural stem cell niche. Cell Stem Cell 14:500-511.
56. Pilz GA, Jessberger S (2014) ChAT me up: how neurons control stem cells. Nat Neurosci 17:897-898.
57. Dawson MR, Polito A, Levine JM, Reynolds R (2003) NG2-expressing glial progenitor cells: an abundant and widespread population of cycling cells in the adult rat CNS. Mol Cell Neurosci 24:476-488.
58. Aguirre AA, Chittajallu R, Belachew S, Gallo V (2004) NG2-expressing cells in the subventricular zone are type C-like cells and contribute to interneuron generation in the postnatal hippocampus. J Cell Biol 165:575-589.
59. Butt AM, Hamilton N, Hubbard P, Pugh M, Ibrahim M (2005) Synantocytes: the fifth element. J Anat 207:695-706.
60. Niu W, Zang T, Zou Y, Fang S, Smith DK, Bachoo R, Zhang CL (2013) In vivo reprogramming of astrocytes to neuroblasts in the adult brain. Nat Cell Biol 15:1164-1175.
61. Horner PJ, Power AE, Kempermann G, Kuhn HG, Palmer TD, Winkler J, Thal LJ, Gage FH (2000) Proliferation and differentiation of progenitor cells throughout the intact adult rat spinal cord. J Neurosci 20:2218-2228.
62. Dayer AG, Cleaver KM, Abouantoun T, Cameron HA (2005) New GABAergic interneurons in the adult neocortex and striatum are generated from different precursors. J Cell Biol 168:415-427.
63. Kokoeva MV, Yin H, Flier JS (2005) Neurogenesis in the hypothalamus of adult mice: potential role in energy balance. Science 310:679-683.
64. Nishiyama A, Komitova M, Suzuki R, Zhu X (2009) Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity. Nat Rev Neurosci 10:9-22.
65. Boda E, Buffo A (2010) Glial cells in non-germinal territories: insights into their stem/progenitor properties in the intact and injured nervous tissue. Arch Ital Biol 148:119-136.
66. Guan T, Kong J (2015) Functional regeneration of the brain: white matter matters. Neural Regen Res 10:355-356.
67. Gibson EM, Purger D, Mount CW, Goldstein AK, Lin GL, Wood LS, Inema I, Miller SE, Bieri G, Zuchero JB, Barres BA, Woo PJ, Vogel H, Monje M (2014) Neuronal activity promotes oligodendrogenesis and adaptive myelination in the mammalian brain. Science 344:1252304.
68. Miyamoto N, Maki T, Shindo A, Liang AC, Maeda M, Egawa N, Itoh K, Lo EK, Lok J, Ihara M, Arai K (2015) Astrocytes promote oligodendrogenesis after white matter damage via brain-derived neurotrophic factor. J Neurosci 35:14002-14008.
69. Ge WP, Miyawaki A, Gage FH, Jan YN, Jan LY (2012) Local generation of glia is a major astrocyte source in postnatal cortex. Nature 484:376-380.
70. Buffo A, Rite I, Tripathi P, Lepier A, Colak D, Horn AP, Mori T, Götz M (2008) Origin and progeny of reactive gliosis: a source of multipotent cells in the injured brain. Proc Natl Acad Sci U S A 105:3581-3586.
71. Barnabé-Heider F, Göritz C, Sabelström H, Takebayashi H, Pfrieger FW, Meletis K, Frisén J (2010) Origin of new glial cells in intact and injured adult spinal cord. Cell Stem Cell 7:470-482.
72. Weissman IL (2000) Stem cells: units of development, units of regeneration, and units in evolution. Cell 100:157-168.
73. Adlaf EW, Mitchell-Dick A, Kuo CT (2016) Discerning neurogenic vs. non-neurogenic postnatal lateral ventricular astrocytes via activity-dependent input. Front Neurosci 10:111.
74. Buffo A, Vosko MR, Ertürk D, Hamann GF, Jucker M, Rowitch D, Götz M (2005) Expression pattern of the transcription factor Olig2 in response to brain injuries: implications for neuronal repair. Proc Natl Acad Sci U S A 102:18183-18188.
75. Robel S, Berninger B, Götz M (2011) The stem cell potential of glia: lessons from reactive gliosis. Nat Rev Neurosci 12:88-104.
76. Shaltouki A, Peng J, Liu Q, Rao MS, Zeng X (2013) Efficient generation of astrocytes from human pluripotent stem cells in defined conditions. Stem Cells 31:941-952.
77. Smith C, Berry M, Clarke WE, Logan A (2001) Differential expression of fibroblast growth factor-2 and fibroblast growth factor receptor 1 in a scarring and nonscarring model of CNS injury in the rat. Eur J Neurosci 13:443-456.
78. Smith GM, Strunz C (2005) Growth factor and cytokine regulation of chondroitin sulfate proteoglycans by astrocytes. Glia 52:209-218.
79. Liu B, Chen H, Johns TG, Neufeld AH (2006) Epidermal growth factor receptor activation: an upstream signal for transition of quiescent astrocytes into reactive astrocytes after neural injury. J Neurosci 26:7532-7540.
80. Amankulor NM, Hambardzumyan D, Pyonteck SM, Becher OJ, Joyce JA, Holland EC (2009) Sonic hedgehog pathway activation is induced by acute brain injury and regulated by injury-related inflammation. J Neurosci 29:10299-10308.
81. Bonfanti L (2011) From hydra regeneration to human brain structural plasticity: a long trip through narrowing roads. ScientificWorldJournal 11:1270-1299.
82. Bonfanti L, Mackay-Sim A (2010) Exploring neurogenesis outside the niche: atypical locations of mammalian neural stem/progenitor cells. Arch Ital Biol 148:43-45.
83. Gritti A, Vescovi AL, Galli R (2002) Adult neural stem cells: plasticity and developmental potential. J Physiol Paris 96:81-90.
84. Bauer HC, Tempfer H, Bernroider G, Bauer H (2006) Neuronal stem cells in adults. Exp Gerontol 41:111-116.
85. Coskun V, Wu H, Blanchi B, Tsao S, Kim K, Zhao J, Biancotti JC, Hutnick L, Krueger RC Jr, Fan G, de Vellis J, Sun YE (2008) CD133+ neural stem cells in the ependyma of mammalian postnatal forebrain. Proc Natl Acad Sci U S A 105:1026-1031.
86. Zhang RL, Zhang ZG, Wang Y, LeTourneau Y, Liu XS, Zhang X, Gregg SR, Wang L, Chopp M (2007) Stroke induces ependymal cell transformation into radial glia in the subventricular zone of the adult rodent brain. J Cereb Blood Flow Metab 27:1201-1212.
87. Niwa A, Nishibori M, Hamasaki S, Kobori T, Liu K, Wake H, Mori S, Yoshino T, Takahashi H (2016) Voluntary exercise induces neurogenesis in the hypothalamus and ependymal lining of the third ventricle. Brain Struct Funct 221:1653-1666.
88. Maggi R, Zasso J, Conti L (2015) Neurodevelopmental origin and adult neurogenesis of the neuroendocrine hypothalamus. Front Cell Neurosci 8:440.
89. Qin Y, Zhang W, Yang P (2015) Current states of endogenous stem cells in adult spinal cord. J Neurosci Res 93:391-398.
90. Hugnot JP, Franzen R (2011) The spinal cord ependymal region: a stem cell niche in the caudal central nervous system. Front Biosci (Landmark Ed) 16:1044-1059.
91. Yoshimi K, Ren YR, Seki T, Yamada M, Ooizumi H, Onodera M, Saito Y, Murayama S, Okano H, Mizuno Y, Mochizuki H (2005) Possibility for neurogenesis in substantia nigra of parkinsonian brain. Ann Neurol 58:31-40.
92. Wang S, Okun MS, Suslov O, Zheng T, McFarland NR, Vedam-Mai V, Foote KD, Roper SN, Yachnis AT, Siebzehnrubl FA, Steindler DA (2012) Neurogenic potential of progenitor cells isolated from postmortem human Parkinsonian brains. Brain Res 1464:61-72.
93. Wang JM (2014) Allopregnanolone and neurogenesis in the nigrostriatal tract. Front Cell Neurosci 8:224.
94. Paul G, Zachrisson O, Varrone A, Almqvist P, Jerling M, Lind G, Rehncrona S, Linderoth B, Bjartmarz H, Shafer LL, Coffey R, Svensson M, Mercer KJ, Forsberg A, Halldin C, Svenningsson P, Widner H, Frisén J, Pålhagen S, Haegerstrand A (2015) Safety and tolerability of intracerebroventricular PDGF-BB in Parkinson's disease patients. J Clin Invest 125:1339-1346.
95. Lin R, Iacovitti L (2015) Classic and novel stem cell niches in brain homeostasis and repair. Brain Res 1628:327-342.
96. Li L, Candelario KM, Thomas K, Wang R, Wright K, Messier A, Cunningham LA (2014) Hypoxia inducible factor-1alpha (HIF-1alpha) is required for neural stem cell maintenance and vascular stability in the adult mouse SVZ. J Neurosci 34:16713-16719.
97. Cunningham LA, Candelario K, Li L (2012) Roles for HIF-1alpha in neural stem cell function and the regenerative response to stroke. Behav Brain Res 227:410-417.
98. Hu Q, Liang X, Chen D, Chen Y, Doycheva D, Tang J, Tang J, Zhang JH (2014) Delayed hyperbaric oxygen therapy promotes neurogenesis through reactive oxygen species/hypoxia-inducible factor-1alpha/beta-catenin pathway in middle cerebral artery occlusion rats. Stroke 45:1807-1814.
99. Vieira HL, Alves PM, Vercelli A (2011) Modulation of neuronal stem cell differentiation by hypoxia and reactive oxygen species. Prog Neurobiol 93:444-455.
100. Colak D, Mori T, Brill MS, Pfeifer A, Falk S, Deng C, Monteiro R, Mummery C, Sommer L, Götz M (2008) Adult neurogenesis requires Smad4-mediated bone morphogenic protein signaling in stem cells. J Neurosci 28:434-446.
101. Hack MA, Sugimori M, Lundberg C, Nakafuku M, Götz M (2004) Regionalization and fate specification in neurospheres: the role of Olig2 and Pax6. Mol Cell Neurosci 25:664-678.
102. Doetsch F, Petreanu L, Caille I, Garcia-Verdugo JM, Alvarez-Buylla A (2002) EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 36:1021-1034.
103. Heins N, Malatesta P, Cecconi F, Nakafuku M, Tucker KL, Hack MA, Chapouton P, Barde YA, Götz M (2002) Glial cells generate neurons: the role of the transcription factor Pax6. Nat Neurosci 5:308-315.
104. Berninger B, Costa MR, Koch U, Schroeder T, Sutor B, Grothe B, Götz M (2007) Functional properties of neurons derived from in vitro reprogrammed postnatal astroglia. J Neurosci 27:8654-8664.
105. Blum R, Heinrich C, Sánchez R, Lepier A, Gundelfinger ED, Berninger B, Götz M (2011) Neuronal network formation from reprogrammed early postnatal rat cortical glial cells. Cereb Cortex 21:413-424.
106. Heinrich C, Blum R, Gascón S, Masserdotti G, Tripathi P, Sánchez R, Tiedt S, Schroeder T, Götz M, Berninger B (2010) Directing astroglia from the cerebral cortex into subtype specific functional neurons. PLoS Biol 8:e1000373.
107. Jackson EL, Garcia-Verdugo JM, Gil-Perotin S, Roy M, Quinones-Hinojosa A, VandenBerg S, Alvarez-Buylla A (2006) PDGFR alpha-positive B cells are neural stem cells in the adult SVZ that form glioma-like growths in response to increased PDGF signaling. Neuron 51:187-199.