Modulation of oligodendrocyte generation during a critical temporal window after NG2 cell division

Nature Neuroscience

Volumn 17, Issue 11, 2014, Pages 1518-1527

  Hill, Robert A ^a,b   Patel, Kiran D ^a   Goncalves, Christopher M ^a   Grutzendler, Jaime ^b   Nishiyama, Akiko ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MYELIN; ANTIGEN; CHONDROITIN SULFATE PROTEOGLYCAN 4; PROTEOGLYCAN;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DAMAGE; CELL DIVISION; CELL FATE; CELL MATURATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; CORPUS CALLOSUM; DAUGHTER CELL; FEMALE; MALE; MOUSE; MYELINATION; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NEUROMODULATION; NONHUMAN; OLIGODENDROCYTE PRECURSOR CELL; OLIGODENDROGLIA; SOMATOSENSORY CORTEX; STEREOTYPY; TIME LAPSE IMAGING; ANIMAL; ASTROCYTE; BRAIN; CELL DIFFERENTIATION; CELL LINEAGE; CYTOLOGY; GENETICS; GLIA; METABOLISM; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY; TIME FACTOR; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS; ASTROCYTES; BRAIN; CELL DIFFERENTIATION; CELL DIVISION; CELL LINEAGE; CELL PROLIFERATION; FEMALE; MALE; MICE; MICE, TRANSGENIC; NEUROGENESIS; NEUROGLIA; OLIGODENDROGLIA; PROTEOGLYCANS; TIME FACTORS;

EID: 84908565263     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3815     Document Type: Article

References (54)

1. Nishiyama, A., Komitova, M., Suzuki, R. & Zhu, X. Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity. Nat. Rev. Neurosci. 10, 9-22 (2009
2. Hill, R.A. & Nishiyama, A. NG2 cells (polydendrocytes): Listeners to the neural network with diverse properties. Glia 62, 1195-1210 (2014
3. Dimou, L., Simon, C., Kirchhoff, F., Takebayashi, H. & Gotz, M. Progeny of Olig2-expressing progenitors in the gray and white matter of the adult mouse cerebral cortex. J. Neurosci. 28, 10434-10442 (2008
4. Kang, S.H., Fukaya, M., Yang, J.K., Rothstein, J.D. & Bergles, D.E. NG2+ CNS glial progenitors remain committed to the oligodendrocyte lineage in postnatal life and following neurodegeneration. Neuron 68, 668-681 (2010
5. Rivers, L.E. et al. PDGFRA/NG2 glia generate myelinating oligodendrocytes and piriform projection neurons in adult mice. Nat. Neurosci. 11, 1392-1401 (2008
6. Zhu, X. et al. Age-dependent fate and lineage restriction of single NG2 cells. Development 138, 745-753 (2011
7. Viganò, F., Möbius, W., Götz, M. & Dimou, L. Transplantation reveals regional differences in oligodendrocyte differentiation in the adult brain. Nat. Neurosci. 16, 1370-1372 (2013
8. Young, K.M. et al. Oligodendrocyte dynamics in the healthy adult CNS: evidence for myelin remodeling. Neuron 77, 873-885 (2013
9. Chong, S.Y.C. & Chan, J.R. Tapping into the glial reservoir: cells committed to remaining uncommitted. J. Cell Biol. 188, 305-312 (2010
10. Zuchero, J.B. & Barres, B.A. Intrinsic and extrinsic control of oligodendrocyte development. Curr. Opin. Neurobiol. 23, 914-920 (2013
11. Nishiyama, A. Polydendrocytes: NG2 cells with many roles in development and repair of the CNS. Neuroscientist 13, 62-76 (2007
12. Demerens, C. et al. Induction of myelination in the central nervous system by electrical activity. Proc. Natl. Acad. Sci. USA 93, 9887-9892 (1996
13. Malone, M. et al. Neuronal activity promotes myelination via a cAMP pathway. Glia 61, 843-854 (2013
14. Liu, J. et al. Impaired adult myelination in the prefrontal cortex of socially isolated mice. Nat. Neurosci. 15, 1621-1623 (2012
15. Simon, C., Gotz, M. & Dimou, L. Progenitors in the adult cerebral cortex: cell cycle properties and regulation by physiological stimuli and injury. Glia 59, 869-881 (2011
16. Hirrlinger, P.G. et al. Expression of reef coral fluorescent proteins in the central nervous system of transgenic mice. Mol. Cell. Neurosci. 30, 291-303 (2005
17. Schain, A.J., Hill, R.A. & Grutzendler, J. Label-free in vivo imaging of myelinated axons in health and disease with spectral confocal reflectance microscopy. Nat. Med. 20, 443-449 (2014
18. Zhu, X., Bergles, D.E. & Nishiyama, A. NG2 cells generate both oligodendrocytes and gray matter astrocytes. Development 135, 145-157 (2008
19. Zhu, X., Hill, R.A. & Nishiyama, A. NG2 cells generate oligodendrocytes and gray matter astrocytes in the spinal cord. Neuron Glia Biol. 4, 19-26 (2008
20. Psachoulia, K., Jamen, F., Young, K.M. & Richardson, W.D. Cell cycle dynamics of NG2 cells in the postnatal and ageing brain. Neuron Glia Biol. 5, 57-67 (2009
21. Dawson, M.R., Polito, A., Levine, J.M. & Reynolds, R. NG2-expressing glial progenitor cells: an abundant and widespread population of cycling cells in the adult rat CNS. Mol. Cell. Neurosci. 24, 476-488 (2003
22. Bu, J., Banki, A., Wu, Q. & Nishiyama, A. Increased NG2+ glial cell proliferation and oligodendrocyte generation in the hypomyelinating mutant shiverer. Glia 48, 51-63 (2004
23. Watanabe, M., Toyama, Y. & Nishiyama, A. Differentiation of proliferated NG2-positive glial progenitor cells in a remyelinating lesion. J. Neurosci. Res. 69, 826-836 (2002
24. Hill, R.A., Patel, K.D., Medved, J., Reiss, A.M. & Nishiyama, A. NG2 cells in white matter but not gray matter proliferate in response to PDGF. J. Neurosci. 33, 14558-14566 (2013
25. Birgbauer, E., Rao, T.S. & Webb, M. Lysolecithin induces demyelination in vitro in a cerebellar slice culture system. J. Neurosci. Res. 78, 157-166 (2004
26. Fancy, S.P. et al. Axin2 as regulatory and therapeutic target in newborn brain injury and remyelination. Nat. Neurosci. 14, 1009-1016 (2011
27. Hall, S.M. The effect of injections of lysophosphatidyl choline into white matter of the adult mouse spinal cord. J. Cell Sci. 10, 535-546 (1972
28. Gensert, J.M. & Goldman, J.E. Endogenous progenitors remyelinate demyelinated axons in the adult CNS. Neuron 19, 197-203 (1997
29. Sugiarto, S. et al. Asymmetry-defective oligodendrocyte progenitors are glioma precursors. Cancer Cell 20, 328-340 (2011
30. Kukley, M. et al. Glial cells are born with synapses. FASEB J. 22, 2957-2969 (2008
31. Ge, W.P., Zhou, W., Luo, Q., Jan, L.Y. & Jan, Y.N. Dividing glial cells maintain differentiated properties including complex morphology and functional synapses. Proc. Natl. Acad. Sci. USA 106, 328-333 (2009
32. Hughes, E.G., Kang, S.H., Fukaya, M. & Bergles, D.E. Oligodendrocyte progenitors balance growth with self-repulsion to achieve homeostasis in the adult brain. Nat. Neurosci. 16, 668-676 (2013
33. Czopka, T., Ffrench-Constant, C. & Lyons, D.A. Individual oligodendrocytes have only a few hours in which to generate new myelin sheaths in vivo. Dev. Cell 25, 599-609 (2013
34. Liu, J. & Casaccia, P. Epigenetic regulation of oligodendrocyte identity. Trends Neurosci. 33, 193-201 (2010
35. Imayoshi, I. et al. Oscillatory control of factors determining multipotency and fate in mouse neural progenitors. Science 342, 1203-1208 (2013
36. Kirby, B.B. et al. In vivo time-lapse imaging shows dynamic oligodendrocyte progenitor behavior during zebrafish development. Nat. Neurosci. 9, 1506-1511 (2006
37. Hill, R.A., Natsume, R., Sakimura, K. & Nishiyama, A. NG2 cells are uniformly distributed and NG2 is not required for barrel formation in the somatosensory cortex. Mol. Cell. Neurosci. 46, 689-698 (2011
38. Mangin, J.-M., Li, P., Scafidi, J. & Gallo, V. Experience-dependent regulation of NG2 progenitors in the developing barrel cortex. Nat. Neurosci. 15, 1192-1194 (2012
39. Barres, B.A. et al. Cell death and control of cell survival in the oligodendrocyte lineage. Cell 70, 31-46 (1992
40. Trapp, B.D. Differentiation and death of premyelinating oligodendrocytes in developing rodent brain. J. Cell Biol. 137, 459-468 (1997
41. Marty, S., Berzaghi Mda, P. & Berninger, B. Neurotrophins and activity-dependent plasticity of cortical interneurons. Trends Neurosci. 20, 198-202 (1997
42. VonDran, M.W., Singh, H., Honeywell, J.Z. & Dreyfus, C.F. Levels of BDNF impact oligodendrocyte lineage cells following a cuprizone lesion. J. Neurosci. 31, 14182-14190 (2011
43. Barres, B.A., Jacobson, M.D., Schmid, R., Sendtner, M. & Raff, M.C. Does oligodendrocyte survival depend on axons?. Curr. Biol. 3, 489-497 (1993
44. Ueda, H., Levine, J.M., Miller, R.H. & Trapp, B.D. Rat optic nerve oligodendrocytes develop in the absence of viable retinal ganglion cell axons. J. Cell Biol. 146, 1365-1374 (1999
45. Stevens, B., Tanner, S. & Fields, R.D. Control of myelination by specific patterns of neural impulses. J. Neurosci. 18, 9303-9311 (1998
46. Wake, H., Lee, P.R. & Fields, R.D. Control of local protein synthesis and initial events in myelination by action potentials. Science 333, 1647-1651 (2011
47. Gibson, E.M. et al. Neuronal activity promotes oligodendrogenesis and adaptive myelination in the mammalian brain. Science 344, 1252304 (2014
48. Makinodan, M., Rosen, K.M., Ito, S. & Corfas, G. A critical period for social experience-dependent oligodendrocyte maturation and myelination. Science 337, 1357-1360 (2012
49. Novak, A., Guo, C., Yang, W., Nagy, A. & Lobe, C.G. Z/EG, a double reporter mouse line that expresses enhanced green fluorescent protein upon Cre-mediated excision. Genes. (New York, N.Y. 2000) 28, 147-155 (2000
50. Fuss, B. et al. Purification and analysis of in vivo-differentiated oligodendrocytes expressing the green fluorescent protein. Dev. Biol. 218, 259-274 (2000
51. Mallon, B.S., Shick, H.E., Kidd, G.J. & Macklin, W.B. Proteolipid promoter activity distinguishes two populations of NG2-positive cells throughout neonatal cortical development. J. Neurosci. 22, 876-885 (2002
52. Grutzendler, J., Kasthuri, N. & Gan, W.-B. Long-term dendritic spine stability in the adult cortex. Nature 420, 812-816 (2002
53. McLean, I.W. & Nakane, P.K. Periodate-lysine-paraformaldehyde fixative. A new fixation for immunoelectron microscopy. J. Histochem. Cytochem. 22, 1077-1083 (1974
54. Yamamura, T., Konola, J.T., Wekerle, H. & Lees, M.B. Monoclonal antibodies against myelin proteolipid protein: identification and characterization of two major determinants. J. Neurochem. 57, 1671-1680 (1991