Oligodendrocyte progenitors: Adult stem cells of the central nervous system?

Experimental Neurology

Volumn 260, Issue , 2014, Pages 50-55

  Crawford, A H ^a,c   Stockley, J H ^a,c   Tripathi, R B ^b,d   Richardson, W D ^b,d   Franklin, R J M ^a,c  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Astrocyte; Multipotent; Neuron; Oligodendrocyte; Precursor cell; Progenitor cell; Regeneration; Remyelination; Schwann cell; Stem cell

Indexed keywords

ADULT STEM CELL; CELL DIVISION; CELL FUNCTION; CELL POPULATION; CELL RENEWAL; CELL TYPE; GLIA CELL; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR CLONING; MOLECULAR DYNAMICS; MULTIPOTENT STEM CELL; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; OLIGODENDROCYTE PRECURSOR CELL; PROGENY; REVIEW; ANIMAL; ASTROCYTE; CELL DIFFERENTIATION; CENTRAL NERVOUS SYSTEM; CYTOLOGY; METABOLISM; MULTIPOTENT; NERVE CELL; OLIGODENDROGLIA; PHYSIOLOGY; REGENERATION; REMYELINIZATION; SCHWANN CELL; STEM CELL;

ASTROCYTE; MULTIPOTENT; NEURON; OLIGODENDROCYTE; PRECURSOR CELL; PROGENITOR CELL; REGENERATION; REMYELINATION; SCHWANN CELL; STEM CELL;

ADULT STEM CELLS; ANIMALS; CELL DIFFERENTIATION; CENTRAL NERVOUS SYSTEM; HUMANS; OLIGODENDROGLIA; STEM CELLS;

EID: 84908364762     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2014.04.027     Document Type: Review

References (79)

1. Aguirre A., Gallo V. Postnatal neurogenesis and gliogenesis in the olfactory bulb from NG2-expressing progenitors of the subventricular zone. J. Neurosci. Off. J. Soc. Neurosci. 2004, 24:10530-10541.
2. Asakura A., Komaki M., Rudnicki M. Muscle satellite cells are multipotential stem cells that exhibit myogenic, osteogenic, and adipogenic differentiation. Differ. Res. Biol. Divers. 2001, 68:245-253.
3. Beauchamp J.R., Heslop L., Yu D.S., Tajbakhsh S., Kelly R.G., et al. Expression of CD34 and Myf5 defines the majority of quiescent adult skeletal muscle satellite cells. J. Cell Biol. 2000, 151:1221-1234.
4. Belachew S., Chittajallu R., Aguirre A.A., Yuan X., Kirby M., et al. Postnatal NG2 proteoglycan-expressing progenitor cells are intrinsically multipotent and generate functional neurons. J. Cell Biol. 2003, 161:169-186.
5. Bergles D.E., Roberts J.D., Somogyi P., Jahr C.E. Glutamatergic synapses on oligodendrocyte precursor cells in the hippocampus. Nature 2000, 405:187-191.
6. Bianco P., Cao X., Frenette P.S., Mao J.J., Robey P.G., et al. The meaning, the sense and the significance: translating the science of mesenchymal stem cells into medicine. Nat. Med. 2013, 19:35-42.
7. Black J.A., Waxman S.G., Smith K.J. Remyelination of dorsal column axons by endogenous Schwann cells restores the normal pattern of Nav1.6 and Kv1.2 at nodes of Ranvier. Brain 2006, 129:1319-1329.
8. Blakemore W.F. Remyelination by Schwann cells of axons demyelinated by intraspinal injection of 6-aminonicotinamide in the rat. J. Neurocytol. 1975, 4:745-757.
9. Blau H.M., Brazelton T.R., Weimann J.M. The evolving concept of a stem cell: entity or function?. Cell 2001, 105:829-841.
10. Clarke L.E., Young K.M., Hamilton N.B., Li H., Richardson W.D., Attwell D. Properties and fate of oligodendrocyte progenitor cells in the corpus callosum, motor cortex, and piriform cortex of the mouse. J. Neurosci. Off. J. Soc. Neurosci. 2012, 32:8173-8185.
11. Collins C.A., Olsen I., Zammit P.S., Heslop L., Petrie A., et al. Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell 2005, 122:289-301.
12. Dawson M.R., Levine J.M., Reynolds R. NG2-expressing cells in the central nervous system: are they oligodendroglial progenitors?. J. Neurosci. Res. 2000, 61:471-479.
13. 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. 2003, 24:476-488.
14. 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. Off. J. Soc. Neurosci. 2008, 28:10434-10442.
15. Doulatov S., Notta F., Laurenti E., Dick J.E. Hematopoiesis: a human perspective. Cell Stem Cell 2012, 10:120-136.
16. Duncan I.D., Hoffman R.L. Schwann cell invasion of the central nervous system of the myelin mutants. J. Anat. 1997, 190(Pt 1):35-49.
17. Dusart I., Marty S., Peschanski M. Demyelination, and remyelination by Schwann cells and oligodendrocytes after kainate-induced neuronal depletion in the central nervous system. Neuroscience 1992, 51:137-148.
18. Foudi A., Hochedlinger K., Van Buren D., Schindler J.W., Jaenisch R., et al. Analysis of histone 2B-GFP retention reveals slowly cycling hematopoietic stem cells. Nat. Biotechnol. 2009, 27:84-90.
19. Franklin R.J.M., Blakemore W.F. Requirements for Schwann cell migration within CNS environments: a viewpoint. Int. J. Dev. Neurosci. 1993, 11:641-649.
20. Franklin R.J.M., Ffrench-Constant C. Remyelination in the CNS: from biology to therapy. Nat. Rev. Neurosci. 2008, 9:839-855.
21. Fuchs E., Tumbar T., Guasch G. Socializing with the neighbors: stem cells and their niche. Cell 2004, 116:769-778.
22. Gilson J.M., Blakemore W.F. Schwann cell remyelination is not replaced by oligodendrocyte remyelination following ethidium bromide induced demyelination. Neuroreport 2002, 13:1205-1208.
23. Guo F., Maeda Y., Ma J., Xu J., Horiuchi M., et al. Pyramidal neurons are generated from oligodendroglial progenitor cells in adult piriform cortex. J. Neurosci. Off. J. Soc. Neurosci. 2010, 30:12036-12049.
24. Hall P.A., Watt F.M. Stem cells: the generation and maintenance of cellular diversity. Development 1989, 106:619-633.
25. 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. 2013, 16:668-676.
26. Ikota H., Iwasaki A., Kawarai M., Nakazato Y. Neuromyelitis optica with intraspinal expansion of Schwann cell remyelination. Neuropathology 2010, 30:427-433.
27. Ikuta K., Kina T., MacNeil I., Uchida N., Peault B., et al. A developmental switch in thymic lymphocyte maturation potential occurs at the level of hematopoietic stem cells. Cell 1990, 62:863-874.
28. Itoyama Y., Webster H.D., Richardson E.P., Trapp B.D. Schwann cell remyelination of demyelinated axons in spinal cord multiple sclerosis lesions. Ann. Neurol. 1983, 14:339-346.
29. + CNS glial progenitors remain committed to the oligodendrocyte lineage in postnatal life and following neurodegeneration. Neuron 2010, 68:668-681.
30. Karadottir R., Hamilton N.B., Bakiri Y., Attwell D. Spiking and nonspiking classes of oligodendrocyte precursor glia in CNS white matter. Nat. Neurosci. 2008, 11:450-456.
31. Knoblich J.A. The Drosophila nervous system as a model for asymmetric cell division. Symp. Soc. Exp. Biol. 2001, 75-89.
32. Komitova M., Zhu X., Serwanski D.R., Nishiyama A. NG2 cells are distinct from neurogenic cells in the postnatal mouse subventricular zone. J. Comp. Neurol. 2009, 512:702-716.
33. Kondo T., Raff M. Oligodendrocyte precursor cells reprogrammed to become multipotential CNS stem cells. Science 2000, 289:1754-1757.
34. Kuang S., Kuroda K., Le Grand F., Rudnicki M.A. Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell 2007, 129:999-1010.
35. Kukley M., Kiladze M., Tognatta R., Hans M., Swandulla D., et al. Glial cells are born with synapses. FASEB J. 2008, 22:2957-2969.
36. Lechler T., Fuchs E. Asymmetric cell divisions promote stratification and differentiation of mammalian skin. Nature 2005, 437:275-280.
37. Lee Y., Morrison B.M., Li Y., Lengacher S., Farah M.H., et al. Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature 2012, 487:443-448.
38. Lee H.J., Wu J., Chung J., Wrathall J.R. SOX2 expression is upregulated in adult spinal cord after contusion injury in both oligodendrocyte lineage and ependymal cells. J. Neurosci. Res. 2013, 91:196-210.
39. Levine J.M., Reynolds R., Fawcett J.W. The oligodendrocyte precursor cell in health and disease. Trends Neurosci. 2001, 24:39-47.
40. Montarras D., Morgan J., Collins C., Relaix F., Zaffran S., et al. Direct isolation of satellite cells for skeletal muscle regeneration. Science 2005, 309:2064-2067.
41. Morrison S.J., Kimble J. Asymmetric and symmetric stem-cell divisions in development and cancer. Nature 2006, 441:1068-1074.
42. Morrison S.J., Shah N.M., Anderson D.J. Regulatory mechanisms in stem cell biology. Cell 1997, 88:287-298.
43. Nave K.A., Trapp B.D. Axon-glial signaling and the glial support of axon function. Annu. Rev. Neurosci. 2008, 31:535-561.
44. Orkin S.H., Zon L.I. Hematopoiesis: an evolving paradigm for stem cell biology. Cell 2008, 132:631-644.
45. Oshima H., Rochat A., Kedzia C., Kobayashi K., Barrandon Y. Morphogenesis and renewal of hair follicles from adult multipotent stem cells. Cell 2001, 104:233-245.
46. Penderis J., Shields S.A., Franklin R.J.M. Impaired remyelination and depletion of oligodendrocyte progenitors does not occur following repeated episodes of focal demyelination in the rat central nervous system. Brain 2003, 126:1382-1391.
47. Potten C.S., Loeffler M. Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development 1990, 110:1001-1020.
48. Pringle N.P., Mudhar H.S., Collarini E.J., Richardson W.D. PDGF receptors in the rat CNS: during late neurogenesis, PDGF alpha-receptor expression appears to be restricted to glial cells of the oligodendrocyte lineage. Development 1992, 115:535-551.
49. 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. 2009, 5:57-67.
50. Raff M. Adult stem cell plasticity: fact or artifact?. Annu. Rev. Cell Dev. Biol. 2003, 19:1-22.
51. Raff M.C., Miller R.H., Noble M. A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium. Nature 1983, 303:390-396.
52. Richardson W.D., Young K.M., Tripathi R.B., McKenzie I. NG2-glia as multipotent neural stem cells: fact or fantasy?. Neuron 2011, 70:661-673.
53. Rivers L.E., Young K.M., Rizzi M., Jamen F., Psachoulia K., et al. PDGFRA/NG2 glia generate myelinating oligodendrocytes and piriform projection neurons in adult mice. Nat. Neurosci. 2008, 11:1392-1401.
54. Robins S.C., Trudel E., Rotondi O., Liu X., Djogo T., et al. Evidence for NG2-glia derived, adult-born functional neurons in the hypothalamus. PLoS ONE 2013, 8:e78236.
55. Robins S.C., Villemain A., Liu X., Djogo T., Kryzskaya D., et al. Extensive regenerative plasticity among adult NG2-glia populations is exclusively based on self-renewal. Glia 2013, 61:1735-1747.
56. Rossi C.A., Pozzobon M., Ditadi A., Archacka K., Gastaldello A., et al. Clonal characterization of rat muscle satellite cells: proliferation, metabolism and differentiation define an intrinsic heterogeneity. PLoS ONE 2010, 5:e8523.
57. Schultz E. Satellite cell proliferative compartments in growing skeletal muscles. Dev. Biol. 1996, 175:84-94.
58. Shen S., Sandoval J., Swiss V.A., Li J., Dupree J., et al. Age-dependent epigenetic control of differentiation inhibitors is critical for remyelination efficiency. Nat. Neurosci. 2008, 11:1024-1034.
59. Shin J.W., Buxboim A., Spinler K.R., Swift J., Christian D.A., et al. Contractile forces sustain and polarize hematopoiesis from stem and progenitor cells. Cell Stem Cell 2014, 14:81-93.
60. Sim F.J., Zhao C., Penderis J., Franklin R.J.M. The age-related decrease in CNS remyelination efficiency is attributable to an impairment of both oligodendrocyte progenitor recruitment and differentiation. J. Neurosci. Off. J. Soc. Neurosci. 2002, 22:2451-2459.
61. Snippert H.J., Haegebarth A., Kasper M., Jaks V., van Es J.H., et al. Lgr6 marks stem cells in the hair follicle that generate all cell lineages of the skin. Science 2010, 327:1385-1389.
62. Snow M.H. Myogenic cell formation in regenerating rat skeletal muscle injured by mincing. II. An autoradiographic study. Anat. Rec. 1977, 188:201-217.
63. Sugiarto S., Persson A.I., Munoz E.G., Waldhuber M., Lamagna C., et al. Asymmetry-defective oligodendrocyte progenitors are glioma precursors. Cancer Cell 2011, 20:328-340.
64. Sun T., Ye C., Zhang Z., Wu J., Huang H. Cotransplantation of olfactory ensheathing cells and Schwann cells combined with treadmill training promotes functional recovery in rats with contused spinal cords. Cell Transplant. 2013, 22(Suppl. 1):27-38.
65. + oligodendrocyte precursor cells fail to remyelinate the demyelinated adult rat spinal cord in the absence of astrocytes. Exp. Neurol. 2005, 192:11-24.
66. Tatsumi K., Takebayashi H., Manabe T., Tanaka K.F., Makinodan M., et al. Genetic fate mapping of Olig2 progenitors in the injured adult cerebral cortex reveals preferential differentiation into astrocytes. J. Neurosci. Res. 2008, 86:3494-3502.
67. Tripathi R.B., Rivers L.E., Young K.M., Jamen F., Richardson W.D. NG2 glia generate new oligodendrocytes but few astrocytes in a murine experimental autoimmune encephalomyelitis model of demyelinating disease. J. Neurosci. Off. J. Soc. Neurosci. 2010, 30:16383-16390.
68. Wagers A.J., Weissman I.L. Plasticity of adult stem cells. Cell 2004, 116:639-648.
69. Waghmare S.K., Bansal R., Lee J., Zhang Y.V., McDermitt D.J., Tumbar T. Quantitative proliferation dynamics and random chromosome segregation of hair follicle stem cells. EMBO J. 2008, 27:1309-1320.
70. Ward R.E., Huang W., Kostusiak M., Pallier P.N., Michael-Titus A.T., Priestley J.V. A characterization of white matter pathology following spinal cord compression injury in the rat. Neuroscience 2013, 260:227-239.
71. Wilson A., Laurenti E., Oser G., van der Wath R.C., Blanco-Bose W., et al. Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell 2008, 135:1118-1129.
72. Woodruff R.H., Franklin R.J. Demyelination and remyelination of the caudal cerebellar peduncle of adult rats following stereotaxic injections of lysolecithin, ethidium bromide, and complement/anti-galactocerebroside: a comparative study. Glia 1999, 25:216-228.
73. Young K.M., Psachoulia K., Tripathi R.B., Dunn S.J., Cossell L., et al. Oligodendrocyte dynamics in the healthy adult CNS: evidence for myelin remodeling. Neuron 2013, 77:873-885.
74. Zawadzka M., Rivers L.E., Fancy S.P., Zhao C., Tripathi R., et al. CNS-resident glial progenitor/stem cells produce Schwann cells as well as oligodendrocytes during repair of CNS demyelination. Cell Stem Cell 2010, 6:578-590.
75. Zhang Y.V., Cheong J., Ciapurin N., McDermitt D.J., Tumbar T. Distinct self-renewal and differentiation phases in the niche of infrequently dividing hair follicle stem cells. Cell Stem Cell 2009, 5:267-278.
76. Zhu X., Bergles D.E., Nishiyama A. NG2 cells generate both oligodendrocytes and gray matter astrocytes. Development 2008, 135:145-157.
77. Zhu X., Hill R.A., Nishiyama A. NG2 cells generate oligodendrocytes and gray matter astrocytes in the spinal cord. Neuron Glia Biol. 2008, 4:19-26.
78. Zhu Q., Whittemore S.R., Devries W.H., Zhao X., Kuypers N.J., Qiu M. Dorsally-derived oligodendrocytes in the spinal cord contribute to axonal myelination during development and remyelination following focal demyelination. Glia 2011, 59:1612-1621.
79. Zhu X., Hill R.A., Dietrich D., Komitova M., Suzuki R., Nishiyama A. Age-dependent fate and lineage restriction of single NG2 cells. Development 2011, 138:745-753.