Quantification of oligodendrocyte progenitor cells in human and cat optic nerve: Implications for endogenous repair in multiple sclerosis

GLIA

Volumn 58, Issue 12, 2010, Pages 1425-1436

  Jennings, Alison ^a   Carroll, William ^b  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b SIR CHARLES GAIRDNER HOSPITAL   (Australia)

Author keywords

Demyelination; Neuroglia; NG2cells; Oligodendrocytes; Remyelination

Indexed keywords

OLIGODENDROCYTE TRANSCRIPTION FACTOR 1; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; UNCLASSIFIED DRUG; ANTIGEN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; CHONDROITIN SULFATE PROTEOGLYCAN 4; NERVE PROTEIN; OLIG1 PROTEIN, HUMAN; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; PROTEOGLYCAN;

ADULT; AGED; ANIMAL CELL; ARTICLE; CAT; DEMYELINATION; FEMALE; GRAY MATTER; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; MULTIPLE SCLEROSIS; NERVE FIBER; NONHUMAN; OLIGODENDROGLIA; OPTIC NERVE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL; WHITE MATTER; ADOLESCENT; ADULT STEM CELL; ANIMAL; CELL COUNT; CELL DIFFERENTIATION; CLASSIFICATION; CYTOLOGY; METABOLISM; MIDDLE AGED; PHYSIOLOGY; PROCEDURES; SPINAL CORD; VERY ELDERLY;

ADOLESCENT; ADULT STEM CELLS; AGED; AGED, 80 AND OVER; ANIMALS; ANTIGENS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CATS; CELL COUNT; CELL DIFFERENTIATION; FEMALE; HUMANS; MALE; MIDDLE AGED; NERVE TISSUE PROTEINS; OLIGODENDROGLIA; OPTIC NERVE; PROTEOGLYCANS; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR ALPHA; SPINAL CORD;

EID: 77956564351     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.21018     Document Type: Article

References (71)

1. Aguirre A, Dupree JL, Mangin JM, Gallo V. 2007. A functional role for EGFR signaling in myelination and remyelination. Nat Neurosci 10:990-1002.
2. Arnett HA, Fancy SPJ, Alberta JA, Zhao C, Plant SR, Kaing S, Raine CS, Rowitch DH, Franklin RJM, Stiles CD. 2004. bHLH transcription factor Olig1 is required to repair demyelinated lesions in the CNS. Science 306:2111-2115. (Pubitemid 40007666)
3. Baer AS, Syed YA, Kang SU, Mitteregger D, Vig R, ffrench-Constant C, Franklin RJM, Altmann F, Lubec G, Kotter MR. 2009. Myelin-mediated inhibition of oligodendrocyte precursor differentiation can be overcome by pharmacological modulation of Fyn-RhoA and protein kinase C signalling. Brain 132:465-481.
4. Beckstead JH. 1994. A simple technique for preservation of fixation-sensitive antigens in paraffin-embedded tissues. J Histochem Cytochem 42:1127-1134.
5. Belachew S, Gallo V. 2004. Synaptic and extrasynaptic neurotransmitter receptors in glial precursors' quest for identity. Glia 48:185
6. Bergles DE, Roberts JDB, Somogyi P, Jahr CE. 2000. Glutamatergic synapses on oligodendrocyte precursor cells in the hippocampus. Nature 405:187-191.
7. Blakemore WF, Keirstead HS. 1999. The origin of remyelinating cells in the central nervous system. J Neuroimmunol 98:69-76.
8. Bolton S, Butt AM. 2005. The optic nerve: A model for axon-glial interactions. J Pharmacol Toxicol Methods 51:221-233.
9. Bunge RP, Bunge MB, Ris H. 1960. Electron microscopic study of demyelination in an experimentally induced lesion in adult cat spinal cord. J Biophys Biochem Cytol 7:685-712.
10. Butt AM, Duncan A, Hornby MF, Kirvell SL, Hunter A, Levine JM, Berry M. 1999. Cells expressing the NG2 antigen contact nodes of Ranvier in adult CNS white matter. Glia 26:84-91.
11. Butt AM, Hamilton N, Hubbard P, Pugh M, Ibrahim M. 2005. Synantocytes: The fifth element. J Anat 207:695-706.
12. Butt AM, Kiff J, Hubbard P, Berry M. 2002. Synantocytes: New functions for novel NG2 expressing glia. J Neurocytol 31:551-565.
13. Calza L, Fernandez M, Giuliani A, D'Intino G, Pirondi S, Sivilia S, Paradisi M, DeSordi N, Giardino L. 2005. Thyroid hormone and remyelination in adult central nervous system: A lesson from an inflammatory-demyelinating disease. Brain Res Rev 48:339-346.
14. Carroll WM, Jennings AR. 1994. Early recruitment of oligodendrocyte precursors in CNS demyelination. Brain 117:563-578.
15. Carroll WM, Jennings AR, Ironside LJ. 1998. Identification of the adult resting progenitor cell by autoradiographic tracking of oligodendrocyte precursors in experimental CNS demyelination. Brain 121:293-302.
16. Carroll WM, Jennings AR, Mastaglia FL. 1990. The origin of remyelinating oligodendrocytes in antiserum-mediated demyelinative optic neuropathy. Brain 113:953-973.
17. Carroll WM, Jennings AR, Mastaglia FL. 1985. Galactocerebroside antiserum causes demyelination of cat optic nerve. Brain Res 330:378-381.
18. Cerghet M, Skoff RP, Bessert D, Zhang Z, Mullins C, Ghandour MS. 2006. Proliferation and death of oligodendrocytes and myelin proteins are differentially regulated in male and female rodents. J Neurosci 26:1439-1447.
19. Cerghet M, Skoff RP, Swamydas M, Bessert D. 2009. Sexual dimorphism in the white matter of rodents. J Neurol Sci 286:76-80.
20. Chittajallu R, Aguirre A, Gallo V. 2004. NG2-positive cells in the mouse white and grey matter display distinct physiological properties. J Physiol (Lond) 561:109-122.
21. Cook RD. 1979. Observations on focal demyelinating lesions in cat optic nerves. Neuropathol Appl Neurobiol 5:395-404.
22. Dawson MRL, 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.
23. Ffrench-Constant C, Raff MC. 1986. Proliferating bipotential glial progenitor cells in adult rat optic nerve. Nature 319:499-502.
24. Franklin RJ, Gilson JM, Blakemore WF. 1997. Local recruitment of remyelinating cells in the repair of demyelination in the central nervous system. J Neurosci Res 50:337-344.
25. Friese MA, Montalban X, Willcox N, Bell JI, Martin R, Fugger L. 2006. The value of animal models for drug development in multiple sclerosis. Brain 129:1940-1952.
26. Fu H, Cai J, Clevers H, Fast E, Gray S, Greenberg R, Jain MK, Ma Q, Qiu M, Rowitch DH, Taylor CM, Stiles CD. 2009. A genome-wide screen for spatially restricted expression patterns identifies transcription factors that regulate glial development. J Neurosci 29:11399-11408.
27. Fulton BP, Burne JF, Raff MC. 1992. Visualization of O-2A progenitor cells in developing and adult rat optic nerve by quisqualate-stimulated cobalt uptake. J Neurosci 12:4816-4833.
28. Gallo V, Armstrong RC. 2008. Myelin repair strategies: A cellular view. Curr Opin Neurol 21:278-283.
29. Greenwood K, Butt AM. 2003. Evidence that perinatal and adult NG2- glia are not conventional oligodendrocyte progenitors and do not depend on axons for their survival. Mol Cell Neurosci 23:544-558. (Pubitemid 36970217)
30. Hamilton N, Hubbard PS, Butt AM. 2009. Effects of glutamate receptor activation on NG2-glia in the rat optic nerve. J Anat 214:208-218.
31. Hogan MJ, Zimmerman EA. 1968. Optic nerve. In: Hogan MJ, Zimmerman LE, editors. Ophthalmic pathology: An atlas and textbook. Philadelphia: W. B. Saunders. pp 571-629.
32. Horner PJ, Thallmair M, Gage FH. 2002. Defining the NG2-expressing cell of the adult CNS. J Neurocytol 31:469-480.
33. Jennings A, Carroll W. 1999. GSLII positivity is not confined to oligodendrocytes in adult mammalian CNS. J Neurocytol 28:239-248.
34. Jennings AR, Kirilak Y, Carroll WM. 2002. In situ characterisation of oligodendrocyte progenitor cells in adult mammalian optic nerve. J Neurocytol 31:27-39.
35. Jones LL, Yamaguchi Y, Stallcup WB, Tuszynski MH. 2002. NG2 is a major chondroitin sulfate proteoglycan produced after spinal cord injury and is expressed by macrophages and oligodendrocyte progenitors. J Neurosci 22:2792-2803. (Pubitemid 37465828)
36. Keirstead HS, Blakemore WF. 1999. The role of oligodendrocytes and oligodendrocyte progenitors in CNS remyelination. Adv Exp Med Biol 468:183-197.
37. Keirstead HS, Levine JM, Blakemore WF. 1998. Response of the oligodendrocyte progenitor cell population (defined by NG2 labelling) to demyelination of the adult spinal cord. Glia 22:161-170.
38. Kitada M, Rowitch DH. 2006. Transcription factor co-expression patterns indicate heterogeneity of oligodendroglial subpopulations in adult spinal cord. Glia 54:35-46.
39. Ligon KL, Kesari S, Kitada M, Sun T, Arnett HA, Alberta JA, Anderson DJ, Stiles CD, Rowitch DH. 2006. Development of NG2 neural progenitor cells requires Olig gene function. PNAS 103:7853-7858.
40. Lubetzki C. 2008. Regenerative capacity in multiple sclerosis. Bull Acad Natl Med 192:495-504.
41. Lykidis D, Noorden SV, Armstrong A, Spencer-Dene B, Li J, Zhuang Z, Stamp GWH. 2007. Novel zinc-based fixative for high quality DNA, RNA and protein analysis. Nucleic Acids Res 35:1-10.
42. McTigue DMP, Tripathi RM, Wei P. 2006. NG2 colocalizes with axons and is expressed by a mixed cell population in spinal cord lesions. J Neuropathol Exp Neurol 65:406-420. (Pubitemid 44264837)
43. Miron VE, Rajasekharan S, Jarjour AA, Zamvil SS, Kennedy TE, Antel JP. 2007. Simvastatin regulates oligodendroglial process dynamics and survival. Glia 55:130-143.
44. Namimatsu S, Ghazizadeh M, Sugisaki Y. 2005. Reversing the effects of formalin fixation with citraconic anhydride and heat: A universal antigen retrieval method. J Histochem Cytochem 53:3-11.
45. Nishiyama A. 2007. Polydendrocytes: NG2 cells with many roles in development and repair of the CNS. Neurosci 13:62-76.
46. Nishiyama A, Komitova M, Suzuki R, Zhu X. 2009. Polydendrocytes (NG2 cells): Multifunctional cells with lineage plasticity. Nat Rev Neurosci 10:9-22.
47. Nishiyama A, Watanabe M, Yang ZS, Bu J. 2002. Identity, distribution, and development of polydendrocytes: NG2-expressing glial cells. J Neurocytol 31:437-455. (Pubitemid 37378257)
48. Omari KM, Lutz SE, Santambrogio L, Lira SA, Raine CS. 2009. Neuroprotection and remyelination after autoimmune demyelination in mice that inducibly overexpress CXCL1. Am J Pathol 174:164-176.
49. Ozerdem U, Monosov E, Stallcup WB. 2002. NG2 proteoglycan expression by pericytes in pathological microvasculature. Microvasc Res 63:129-134.
50. Peters A. 2002. The effects of normal aging on myelin and nerve fibers: A review. J Neurocytol 31:581-593.
51. Peters A. 2004. A fourth type of neuroglial cell in the adult central nervous system. J Neurocytol 33:345-357.
52. Peters A, Verderosa A, Sethares C. 2008. The neuroglial population in the primary visual cortex of the aging rhesus monkey. Glia 56:1151-1161.
53. Polito A, Reynolds R. 2005. NG2-expressing cells as oligodendrocyte progenitors in the normal and demyelinated adult central nervous system. J Anat 207:707-716.
54. Reynolds R, Dawson M, Papadopoulos D, Polito A, Di Bello IC, Pham- Dinh D, Levine J. 2002. The response of NG2-expressing oligodendrocyte progenitors to demyelination in MOG-EAE and MS. J Neurocytol 31:523-536.
55. Ring A, Rajandran H, Harvey A, Ghosh S. 2004. Changes in electrical thresholds for evoking movements from the cat cerebral cortex following lesions of the sensori-motor area. Somatosens Motor Res 21:117-136. (Pubitemid 38998644)
56. Rist JM, Franklin RJ. 2008. Taking ageing into account in remyelination- based therapies for multiple sclerosis. J Neurol Sci 274:64-67.
57. Rose KA, Levick WR, Burke W. 1997. Changes in the receptive fields of cat retinal ganglion cells affected by pressure on the optic nerve. Aust NZ J Ophthalmol 25:S61-S63. (Pubitemid 27337285)
58. Sandell JH, Peters A. 2002. Effects of age on the glial cells in the rhesus monkey optic nerve. J Comp Neurol 445:13-28.
59. Shen S, Sandoval J, Swiss VA, Li J, Dupree J, Franklin RJM, Casaccia-Bonnefil P. 2008. Age-dependent epigenetic control of differentiation inhibitors is critical for remyelination efficiency. Nat Neurosci 11:1024-1034.
60. Sim FJ, Zhao C, Penderis J, Franklin RJM. 2002. The age-related decrease in CNS remyelination efficiency is attributable to an impairment of both oligodendrocyte progenitor recruitment and differentiation. J Neurosci 22:2451-2459.
61. Small RK, Riddle P, Noble M. 1987. Evidence for migration of oligodendrocyte- type-2 astrocyte progenitor cells into the developing rat optic nerve. Nature 328:155-157. (Pubitemid 17108214)
62. Staugaitis SM, Trapp BD. 2009. NG2-positive glia in the human central nervous system. Neuron Glia Biol First View 1-10.
63. Tan AM, Zhang W, Levine JM. 2005. NG2: A component of the glial scar that inhibits axon growth. J Anat 207:717-725.
64. Tanaka K, Nogawa S, Suzuki S, Dembo T, Kosakai A. 2003. Upregulation of oligodendrocyte progenitor cells associated with restoration of mature oligodendrocytes and myelination in peri-infarct area in the rat brain. Brain Res 989:172-179.
65. Ulrich J, Groebke-Lorenz W. 1983. The optic nerve in MS: A morphological study with retrospective clinicopathological correlation. Neurol Ophthalmol 3:149-159.
66. Wigley R, Butt AM. 2009. Integration of NG2-glia (" synantocytes") into the neuroglial network. Neuron Glia Biol First View 1-8.
67. Wilson HC, Scolding NJ, Raine CS. 2006. Co-expression of PDGF a receptor and NG2 by oligodendrocyte precursors in human CNS, multiple sclerosis lesions. J Neuroimmunol 176:162-173.
68. Wolswijk G. 2002. Oligodendrocyte precursor cells in the demyelinated multiple sclerosis spinal cord. Brain 125:338-349.
69. Xin M, Yue T, Ma Z, Wu Ff, Gow A, Lu QR. 2005. Myelinogenesis and axonal recognition by oligodendrocytes in brain are uncoupled in olig1-null mice. J Neurosci 25:1354-1365.
70. Yang Z, Suzuki R, Daniels SB, Brunquell CB, Sala CJ, Nishiyama A. 2006. NG2 glial cells provide a favorable substrate for growing axons. J Neurosci 26:3829-3839.
71. Yokoo H, Nobusawa S, Takebayashi H, Ikenaka K, Isoda K, Kamiya M, Sasaki A, Hirato J, Nakazato Y. 2004. Anti-human Olig2 antibody as a useful immunohistochemical marker of normal oligodendrocytes and gliomas. Am J Pathol 164:1717-1725.