Progenitors in the adult cerebral cortex: Cell cycle properties and regulation by physiological stimuli and injury

The adult brain parenchyma contains a widespread population of progenitors generating different cells of the oligodendrocyte lineage such as NG2+ cells and some mature oligodendrocytes. However, it is still largely unknown how proliferation and lineage decisions of these progenitors are regulated. H...

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Veröffentlicht in:	Glia Jg. 59; H. 6; S. 869 - 881
Hauptverfasser:	Simon, Christiane, Götz, Magdalena, Dimou, Leda
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	Hoboken Wiley Subscription Services, Inc., A Wiley Company 01.06.2011
Schlagworte:	Animals Brain injury Cell cycle cell cycle regulation Cell Differentiation - physiology Cell Lineage - physiology Cell Proliferation Cerebral Cortex - cytology Cerebral Cortex - physiology Cortex cortical injury Data processing Differentiation Disease Models, Animal Environmental effects G1 phase Mice microglia Oligodendrocytes Oligodendroglia - physiology Parenchyma Physical training Progeny reactive astrocytes running wheel Stem cells Stem Cells - cytology Stem Cells - physiology Wounds
ISSN:	0894-1491, 1098-1136, 1098-1136
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Abstract	The adult brain parenchyma contains a widespread population of progenitors generating different cells of the oligodendrocyte lineage such as NG2+ cells and some mature oligodendrocytes. However, it is still largely unknown how proliferation and lineage decisions of these progenitors are regulated. Here, we first characterized the cell cycle length, proliferative fraction, and progeny of dividing cells in the adult cerebral cortex and then compared these proliferation characteristics after two distinct stimuli, invasive acute brain injury and increased physiological activity by voluntary physical exercise. Our data show that adult parenchymal progenitors have a very long cell cycle due to an extended G1 phase, many of them can divide at least twice and only a limited proportion of the progeny differentiates into mature oligodendrocytes. After stab wound injury, however, many of these progenitors re‐enter the cell cycle very fast, suggesting that the normally long G1 phase is subject to regulation and can be abruptly shortened. In striking contrast, voluntary physical exercise shows the opposite effect with increased exit of the cell cycle followed by an enhanced and fast differentiation into mature oligodendrocytes. Taken together, our data demonstrate that the endogenous population of adult brain parenchymal progenitors is subject to profound modulation by environmental stimuli in both directions, either faster proliferation or faster differentiation. © 2011 Wiley‐Liss, Inc.
AbstractList	The adult brain parenchyma contains a widespread population of progenitors generating different cells of the oligodendrocyte lineage such as NG2+ cells and some mature oligodendrocytes. However, it is still largely unknown how proliferation and lineage decisions of these progenitors are regulated. Here, we first characterized the cell cycle length, proliferative fraction, and progeny of dividing cells in the adult cerebral cortex and then compared these proliferation characteristics after two distinct stimuli, invasive acute brain injury and increased physiological activity by voluntary physical exercise. Our data show that adult parenchymal progenitors have a very long cell cycle due to an extended G1 phase, many of them can divide at least twice and only a limited proportion of the progeny differentiates into mature oligodendrocytes. After stab wound injury, however, many of these progenitors re-enter the cell cycle very fast, suggesting that the normally long G1 phase is subject to regulation and can be abruptly shortened. In striking contrast, voluntary physical exercise shows the opposite effect with increased exit of the cell cycle followed by an enhanced and fast differentiation into mature oligodendrocytes. Taken together, our data demonstrate that the endogenous population of adult brain parenchymal progenitors is subject to profound modulation by environmental stimuli in both directions, either faster proliferation or faster differentiation.The adult brain parenchyma contains a widespread population of progenitors generating different cells of the oligodendrocyte lineage such as NG2+ cells and some mature oligodendrocytes. However, it is still largely unknown how proliferation and lineage decisions of these progenitors are regulated. Here, we first characterized the cell cycle length, proliferative fraction, and progeny of dividing cells in the adult cerebral cortex and then compared these proliferation characteristics after two distinct stimuli, invasive acute brain injury and increased physiological activity by voluntary physical exercise. Our data show that adult parenchymal progenitors have a very long cell cycle due to an extended G1 phase, many of them can divide at least twice and only a limited proportion of the progeny differentiates into mature oligodendrocytes. After stab wound injury, however, many of these progenitors re-enter the cell cycle very fast, suggesting that the normally long G1 phase is subject to regulation and can be abruptly shortened. In striking contrast, voluntary physical exercise shows the opposite effect with increased exit of the cell cycle followed by an enhanced and fast differentiation into mature oligodendrocytes. Taken together, our data demonstrate that the endogenous population of adult brain parenchymal progenitors is subject to profound modulation by environmental stimuli in both directions, either faster proliferation or faster differentiation. The adult brain parenchyma contains a widespread population of progenitors generating different cells of the oligodendrocyte lineage such as NG2+ cells and some mature oligodendrocytes. However, it is still largely unknown how proliferation and lineage decisions of these progenitors are regulated. Here, we first characterized the cell cycle length, proliferative fraction, and progeny of dividing cells in the adult cerebral cortex and then compared these proliferation characteristics after two distinct stimuli, invasive acute brain injury and increased physiological activity by voluntary physical exercise. Our data show that adult parenchymal progenitors have a very long cell cycle due to an extended G1 phase, many of them can divide at least twice and only a limited proportion of the progeny differentiates into mature oligodendrocytes. After stab wound injury, however, many of these progenitors re-enter the cell cycle very fast, suggesting that the normally long G1 phase is subject to regulation and can be abruptly shortened. In striking contrast, voluntary physical exercise shows the opposite effect with increased exit of the cell cycle followed by an enhanced and fast differentiation into mature oligodendrocytes. Taken together, our data demonstrate that the endogenous population of adult brain parenchymal progenitors is subject to profound modulation by environmental stimuli in both directions, either faster proliferation or faster differentiation. [copy 2011 Wiley-Liss, Inc. The adult brain parenchyma contains a widespread population of progenitors generating different cells of the oligodendrocyte lineage such as NG2+ cells and some mature oligodendrocytes. However, it is still largely unknown how proliferation and lineage decisions of these progenitors are regulated. Here, we first characterized the cell cycle length, proliferative fraction, and progeny of dividing cells in the adult cerebral cortex and then compared these proliferation characteristics after two distinct stimuli, invasive acute brain injury and increased physiological activity by voluntary physical exercise. Our data show that adult parenchymal progenitors have a very long cell cycle due to an extended G1 phase, many of them can divide at least twice and only a limited proportion of the progeny differentiates into mature oligodendrocytes. After stab wound injury, however, many of these progenitors re‐enter the cell cycle very fast, suggesting that the normally long G1 phase is subject to regulation and can be abruptly shortened. In striking contrast, voluntary physical exercise shows the opposite effect with increased exit of the cell cycle followed by an enhanced and fast differentiation into mature oligodendrocytes. Taken together, our data demonstrate that the endogenous population of adult brain parenchymal progenitors is subject to profound modulation by environmental stimuli in both directions, either faster proliferation or faster differentiation. © 2011 Wiley‐Liss, Inc. The adult brain parenchyma contains a widespread population of progenitors generating different cells of the oligodendrocyte lineage such as NG2+ cells and some mature oligodendrocytes. However, it is still largely unknown how proliferation and lineage decisions of these progenitors are regulated. Here, we first characterized the cell cycle length, proliferative fraction, and progeny of dividing cells in the adult cerebral cortex and then compared these proliferation characteristics after two distinct stimuli, invasive acute brain injury and increased physiological activity by voluntary physical exercise. Our data show that adult parenchymal progenitors have a very long cell cycle due to an extended G1 phase, many of them can divide at least twice and only a limited proportion of the progeny differentiates into mature oligodendrocytes. After stab wound injury, however, many of these progenitors re-enter the cell cycle very fast, suggesting that the normally long G1 phase is subject to regulation and can be abruptly shortened. In striking contrast, voluntary physical exercise shows the opposite effect with increased exit of the cell cycle followed by an enhanced and fast differentiation into mature oligodendrocytes. Taken together, our data demonstrate that the endogenous population of adult brain parenchymal progenitors is subject to profound modulation by environmental stimuli in both directions, either faster proliferation or faster differentiation. ? 2011 Wiley-Liss, Inc. The adult brain parenchyma contains a widespread population of progenitors generating different cells of the oligodendrocyte lineage such as NG2+ cells and some mature oligodendrocytes. However, it is still largely unknown how proliferation and lineage decisions of these progenitors are regulated. Here, we first characterized the cell cycle length, proliferative fraction, and progeny of dividing cells in the adult cerebral cortex and then compared these proliferation characteristics after two distinct stimuli, invasive acute brain injury and increased physiological activity by voluntary physical exercise. Our data show that adult parenchymal progenitors have a very long cell cycle due to an extended G1 phase, many of them can divide at least twice and only a limited proportion of the progeny differentiates into mature oligodendrocytes. After stab wound injury, however, many of these progenitors re-enter the cell cycle very fast, suggesting that the normally long G1 phase is subject to regulation and can be abruptly shortened. In striking contrast, voluntary physical exercise shows the opposite effect with increased exit of the cell cycle followed by an enhanced and fast differentiation into mature oligodendrocytes. Taken together, our data demonstrate that the endogenous population of adult brain parenchymal progenitors is subject to profound modulation by environmental stimuli in both directions, either faster proliferation or faster differentiation.
Author	Dimou, Leda Götz, Magdalena Simon, Christiane
Author_xml	– sequence: 1 givenname: Christiane surname: Simon fullname: Simon, Christiane organization: Physiological Genomics, Institute of Physiology, Ludwig-Maximilians University Munich, Germany – sequence: 2 givenname: Magdalena surname: Götz fullname: Götz, Magdalena organization: Physiological Genomics, Institute of Physiology, Ludwig-Maximilians University Munich, Germany – sequence: 3 givenname: Leda surname: Dimou fullname: Dimou, Leda email: leda.dimou@lrz.uni-muenchen.de organization: Physiological Genomics, Institute of Physiology, Ludwig-Maximilians University Munich, Germany
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/21446038$$D View this record in MEDLINE/PubMed
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References	Barres BA,Raff MC. 1994. Control of oligodendrocyte number in the developing rat optic nerve. Neuron 12: 935-942. 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. Zawadzka M,Rivers LE,Fancy SP,Zhao C,Tripathi R,Jamen F,Young K,Goncharevich A,Pohl H,Rizzi M,Rowitch DH,Kessaris N,Suter U,Richardson WD,Franklin RJ. 2010. CNS-resident glial progenitor/stem cells produce Schwann cells as well as oligodendrocytes during repair of CNS demyelination. Cell Stem Cell 6: 578-590. Etxeberria A,Mangin JM,Aguirre A,Gallo V. 2010. Adult-born SVZ progenitors receive transient synapses during remyelination in corpus callosum. Nat Neurosci 13: 287-289. Belachew S,Chittajallu R,Aguirre AA,Yuan X,Kirby M,Anderson S,Gallo V. 2003. Postnatal NG2 proteoglycan-expressing progenitor cells are intrinsically multipotent and generate functional neurons. J Cell Biol 161: 169-186. Geha S,Pallud J,Junier MP,Devaux B,Leonard N,Chassoux F,Chneiweiss H,Daumas-Duport C,Varlet P. 2010. NG2+/Olig2+ cells are the major cycle-related cell population of the adult human normal brain. Brain Pathol 20: 399-3411. Tripathi RB,McTigue DM. 2008. Chronically increased ciliary neurotrophic factor and fibroblast growth factor-2 expression after spinal contusion in rats. J Comp Neurol 510: 129-144. Irvine KA,Blakemore WF. 2007. A different regional response by mouse oligodendrocyte progenitor cells (OPCs) to high-dose X-irradiation has consequences for repopulating OPC-depleted normal tissue. Eur J Neurosci 25: 417-424. Psachoulia K,Jamen F,Young KM,Richardson WD. 2009. Cell cycle dynamics of NG2 cells in the postnatal and ageing brain. Neuron Glia Biol 5: 57-67. Nunes MC,Roy NS,Keyoung HM,Goodman RR,McKhann G,2nd,Jiang L,Kang J,Nedergaard M,Goldman SA. 2003. 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Adult hippocampal neurogenesis and voluntary running activity: Circadian and dose-dependent effects. J Neurosci Res 76: 216-222. Karram K,Goebbels S,Schwab M,Jennissen K,Seifert G,Steinhauser C,Nave KA,Trotter J. 2008. NG2-expressing cells in the nervous system revealed by the NG2-EYFP-knockin mouse. Genesis 46: 743-757. Wolswijk G,Noble M. 1989. Identification of an adult-specific glial progenitor cell. Development 105: 387-400. Stevens B,Porta S,Haak LL,Gallo V,Fields RD. 2002. Adenosine: A neuron-glial transmitter promoting myelination in the CNS in response to action potentials. Neuron 36: 855-868. Buffo A,Vosko MR,Erturk D,Hamann GF,Jucker M,Rowitch D,Gotz M. 2005. Expression pattern of the transcription factor Olig2 in response to brain injuries: Implications for neuronal repair. Proc Natl Acad Sci USA 102: 18183-18188. Karadottir R,Hamilton NB,Bakiri Y,Attwell D. 2008. Spiking and nonspiking classes of oligodendrocyte precursor glia in CNS white matter. 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Dimou L,Simon C,Kirchhoff F,Takebayashi H,Gotz M. 2008. Progeny of Olig2-expressing progenitors in the gray and white matter of the adult mouse cerebral cortex. J Neurosci 28: 10434-10442. Levine JM,Reynolds R. 1999. Activation and proliferation of endogenous oligodendrocyte precursor cells during ethidium bromide-induced demyelination. Exp Neurol 160: 333-347. Rhodes KE,Moon LD,Fawcett JW. 2003. Inhibiting cell proliferation during formation of the glial scar: Effects on axon regeneration in the CNS. Neuroscience 120: 41-56. Gaser C,Schlaug G. 2003. Brain structures differ between musicians and non-musicians. J Neurosci 23: 9240-9245. Redwine JM,Armstrong RC. 1998. In vivo proliferation of oligodendrocyte progenitors expressing PDGFalphaR during early remyelination. J Neurobiol 37: 413-428. 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. Levine JM,Stincone F,Lee YS. 1993. Development and differentiation of glial precursor cells in the rat cerebellum. Glia 7: 307-321. Bednarczyk MR,Aumont A,Decary S,Bergeron R,Fernandes KJ. 2009. Prolonged voluntary wheel-running stimulates neural precursors in the hippocampus and forebrain of adult CD1 mice. Hippocampus 19: 913-927. Levine JM. 1994. Increased expression of the NG2 chondroitin-sulfate proteoglycan after brain injury. J Neurosci 14: 4716-4730. Pfeiffer SE,Warrington AE,Bansal R. 1993. The oligodendrocyte and its many cellular processes. Trends Cell Biol 3: 191-197. Taupin P. 2007. BrdU immunohistochemistry for studying adult neurogenesis: Paradigms, pitfalls, limitations, and validation. Brain Res Rev 53: 198-214. 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. Anderson BJ,Eckburg PB,Relucio KI. 2002. Alterations in the thickness of motor cortical subregions after motor-skill learning and exercise. Learn Mem 9: 1-9. Mason JL,Goldman JE. 2002. A2B5+ and O4+ cycling progenitors in the adult forebrain white matter respond differentially to PDGF-AA, FGF-2, and IGF-1. Mol Cell Neurosci 20: 30-42. Yuan X,Eisen AM,McBain CJ,Gallo V. 1998. A role for glutamate and its receptors in the regulation of oligodendrocyte development in cerebellar tissue slices. Development 125: 2901-2914. Rivers LE,Young KM,Rizzi M,Jamen F,Psachoulia K,Wade A,Kessaris N,Richardson WD. 2008. PDGFRA/NG2 glia generate myelinating oligodendrocytes and piriform projection neurons in adult mice. Nat Neurosci 11: 1392-1401. Rhodes KE,Raivich G,Fawcett JW. 2006. The injury response of oligodendrocyte precursor cells is induced by platelets, macrophages and inflammation-associated cytokines. Neuroscience 140: 87-100. Barnabe-Heider F,Goritz C,Sabelstrom H,Takebayashi H,Pfrieger FW,Meletis K,Frisen J. 2010. Origin of new glial cells in intact and injured adult spinal cord. Cell Stem Cell 7: 470-482. Lin SC,Bergles DE. 2004. Synaptic signaling between GABAergic interneurons and oligodendrocyte precursor cells in the hippocampus. Nat Neurosci 7: 24-32. Hampton DW,Rhodes KE,Zhao C,Franklin RJ,Fawcett JW. 2004. The responses of oligodendrocyte precursor cells, astrocytes and 1993; 7 2004; 127 2010; 13 2004; 7 2004; 24 2003; 13 2009; 199 2008; 107 2008; 105 2001; 48 1993; 3 2010; 63 2005; 25 2004; 76 1998; 18 2010; 20 1989; 105 2009; 10 2010; 68 2005; 102 2000; 405 2008; 28 2003; 9 2003; 161 1998; 125 2007; 2 2008; 510 2009; 19 2010; 7 2007; 25 2010; 6 2003; 120 2002; 36 2002; 9 1999; 26 2000; 20 2009; 134 2010; 120 2008; 11 1999; 2 2007; 53 2005; 49 1998; 22 2009; 29 2001; 21 1998; 37 2010; 88 2002; 69 2002; 20 1999; 160 2005; 8 1994; 12 2003; 24 2009; 220 2000; 182 2006; 140 2005; 207 1994; 14 2008; 46 2009; 5 2008; 135 2005; 11 2001; 435 2003; 23 1989; 18 e_1_2_6_51_1 e_1_2_6_53_1 e_1_2_6_32_1 e_1_2_6_30_1 e_1_2_6_19_1 e_1_2_6_13_1 e_1_2_6_36_1 e_1_2_6_59_1 e_1_2_6_11_1 e_1_2_6_34_1 e_1_2_6_17_1 e_1_2_6_55_1 e_1_2_6_15_1 e_1_2_6_38_1 e_1_2_6_57_1 e_1_2_6_62_1 e_1_2_6_64_1 e_1_2_6_43_1 e_1_2_6_20_1 e_1_2_6_41_1 e_1_2_6_60_1 e_1_2_6_9_1 e_1_2_6_5_1 e_1_2_6_7_1 e_1_2_6_24_1 e_1_2_6_49_1 e_1_2_6_3_1 e_1_2_6_22_1 e_1_2_6_66_1 e_1_2_6_28_1 e_1_2_6_45_1 e_1_2_6_26_1 e_1_2_6_47_1 e_1_2_6_68_1 e_1_2_6_52_1 e_1_2_6_54_1 e_1_2_6_10_1 e_1_2_6_31_1 e_1_2_6_50_1 e_1_2_6_14_1 e_1_2_6_35_1 e_1_2_6_12_1 e_1_2_6_33_1 e_1_2_6_18_1 e_1_2_6_39_1 e_1_2_6_56_1 e_1_2_6_16_1 e_1_2_6_37_1 e_1_2_6_58_1 e_1_2_6_63_1 e_1_2_6_42_1 e_1_2_6_65_1 e_1_2_6_21_1 e_1_2_6_40_1 e_1_2_6_61_1 e_1_2_6_8_1 e_1_2_6_4_1 e_1_2_6_6_1 e_1_2_6_25_1 e_1_2_6_48_1 e_1_2_6_23_1 e_1_2_6_2_1 e_1_2_6_29_1 e_1_2_6_44_1 e_1_2_6_67_1 e_1_2_6_27_1 e_1_2_6_46_1 e_1_2_6_69_1
References_xml	– reference: Buffo A,Vosko MR,Erturk D,Hamann GF,Jucker M,Rowitch D,Gotz M. 2005. Expression pattern of the transcription factor Olig2 in response to brain injuries: Implications for neuronal repair. Proc Natl Acad Sci USA 102: 18183-18188. – reference: Dimou L,Simon C,Kirchhoff F,Takebayashi H,Gotz M. 2008. Progeny of Olig2-expressing progenitors in the gray and white matter of the adult mouse cerebral cortex. J Neurosci 28: 10434-10442. – reference: Barres BA,Raff MC. 1994. Control of oligodendrocyte number in the developing rat optic nerve. Neuron 12: 935-942. – reference: Chen ZJ,Ughrin Y,Levine JM. 2002. Inhibition of axon growth by oligodendrocyte precursor cells. Mol Cell Neurosci 20: 125-139. – reference: Taupin P. 2007. BrdU immunohistochemistry for studying adult neurogenesis: Paradigms, pitfalls, limitations, and validation. Brain Res Rev 53: 198-214. – reference: Zhu X,Bergles DE,Nishiyama A. 2008. NG2 cells generate both oligodendrocytes and gray matter astrocytes. Development 135: 145-157. – reference: Barnabe-Heider F,Goritz C,Sabelstrom H,Takebayashi H,Pfrieger FW,Meletis K,Frisen J. 2010. Origin of new glial cells in intact and injured adult spinal cord. Cell Stem Cell 7: 470-482. – reference: 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. – reference: Shi J,Marinovich A,Barres BA. 1998. Purification and characterization of adult oligodendrocyte precursor cells from the rat optic nerve. J Neurosci 18: 4627-4636. – reference: Nowakowski RS,Lewin SB,Miller MW. 1989. Bromodeoxyuridine immunohistochemical determination of the lengths of the cell cycle and the DNA-synthetic phase for an anatomically defined population. J Neurocytol 18: 311-318. – reference: Redwine JM,Armstrong RC. 1998. In vivo proliferation of oligodendrocyte progenitors expressing PDGFalphaR during early remyelination. J Neurobiol 37: 413-428. – reference: 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. – reference: Nishiyama A,Komitova M,Suzuki R,Zhu X. 2009. Polydendrocytes (NG2 cells): Multifunctional cells with lineage plasticity. Nat Rev Neurosci 10: 9-22. – reference: Geha S,Pallud J,Junier MP,Devaux B,Leonard N,Chassoux F,Chneiweiss H,Daumas-Duport C,Varlet P. 2010. NG2+/Olig2+ cells are the major cycle-related cell population of the adult human normal brain. Brain Pathol 20: 399-3411. – reference: Levine JM,Stincone F,Lee YS. 1993. Development and differentiation of glial precursor cells in the rat cerebellum. Glia 7: 307-321. – reference: Cameron HA,McKay RD. 2001. Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 435: 406-417. – reference: Anderson BJ,Eckburg PB,Relucio KI. 2002. Alterations in the thickness of motor cortical subregions after motor-skill learning and exercise. Learn Mem 9: 1-9. – reference: Tripathi RB,McTigue DM. 2008. Chronically increased ciliary neurotrophic factor and fibroblast growth factor-2 expression after spinal contusion in rats. J Comp Neurol 510: 129-144. – reference: Irvine KA,Blakemore WF. 2007. A different regional response by mouse oligodendrocyte progenitor cells (OPCs) to high-dose X-irradiation has consequences for repopulating OPC-depleted normal tissue. Eur J Neurosci 25: 417-424. – reference: Bergles DE,Roberts JD,Somogyi P,Jahr CE. 2000. Glutamatergic synapses on oligodendrocyte precursor cells in the hippocampus. Nature 405: 187-191. – reference: Pfeiffer SE,Warrington AE,Bansal R. 1993. The oligodendrocyte and its many cellular processes. Trends Cell Biol 3: 191-197. – reference: 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. – reference: Etxeberria A,Mangin JM,Aguirre A,Gallo V. 2010. Adult-born SVZ progenitors receive transient synapses during remyelination in corpus callosum. Nat Neurosci 13: 287-289. – reference: Bednarczyk MR,Aumont A,Decary S,Bergeron R,Fernandes KJ. 2009. Prolonged voluntary wheel-running stimulates neural precursors in the hippocampus and forebrain of adult CD1 mice. Hippocampus 19: 913-927. – reference: Gaser C,Schlaug G. 2003. Brain structures differ between musicians and non-musicians. J Neurosci 23: 9240-9245. – reference: Belachew S,Chittajallu R,Aguirre AA,Yuan X,Kirby M,Anderson S,Gallo V. 2003. Postnatal NG2 proteoglycan-expressing progenitor cells are intrinsically multipotent and generate functional neurons. 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Snippet	The adult brain parenchyma contains a widespread population of progenitors generating different cells of the oligodendrocyte lineage such as NG2+ cells and...
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SubjectTerms	Animals Brain injury Cell cycle cell cycle regulation Cell Differentiation - physiology Cell Lineage - physiology Cell Proliferation Cerebral Cortex - cytology Cerebral Cortex - physiology Cortex cortical injury Data processing Differentiation Disease Models, Animal Environmental effects G1 phase Mice microglia Oligodendrocytes Oligodendroglia - physiology Parenchyma Physical training Progeny reactive astrocytes running wheel Stem cells Stem Cells - cytology Stem Cells - physiology Wounds
Title	Progenitors in the adult cerebral cortex: Cell cycle properties and regulation by physiological stimuli and injury
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