Cellular and Molecular Characterization of Multipolar Map5-Expressing Cells: A Subset of Newly Generated, Stage-Specific Parenchymal Cells in the Mammalian Central Nervous System

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Crociara, Paola ^a   Parolisi, Roberta ^a   Conte, Daniele ^a   Fumagalli, Marta ^b   Bonfanti, Luca ^a  

^a UNIVERSITY OF TURIN   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

MICROTUBULE ASSOCIATED PROTEIN 5;

AGED; ANIMAL CELL; ARTICLE; CELL COUNT; CELL POPULATION; CELL PROLIFERATION; CELL STRUCTURE; CELL SUBPOPULATION; CELLULAR DISTRIBUTION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DEGENERATIVE DISEASE; FEMALE; HUMAN; HUMAN TISSUE; INJURY; MALE; MAMMAL CELL; MICROTUBULE ASSOCIATED PROTEIN 5 EXPRESSING CELL; MOUSE; NONHUMAN; PARENCHYMA; PHENOTYPE; PROTEIN EXPRESSION; RABBIT; RAT;

AGING; ANIMALS; BIOLOGICAL MARKERS; BROMODEOXYURIDINE; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; CELL SHAPE; CELL SURVIVAL; CENTRAL NERVOUS SYSTEM; MAMMALS; MICE; MICROTUBULE-ASSOCIATED PROTEINS; NERVE DEGENERATION; NEUROGLIA; NEURONS; OLIGODENDROGLIA; PHENOTYPE; RABBITS; TIME FACTORS;

EID: 84877148508     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0063258     Document Type: Article

References (78)

1. 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.
2. Nishiyama A, Komitova M, Suzuki R, Zhu X, (2009) Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity. Nat Rev Neurosci 10: 9-22.
3. Bonfanti L, Peretto P, (2011) Adult neurogenesis in mammals - a theme with many variations. Eur J Neurosci 34: 930-950.
4. Stallcup WB, (1981) The NG2 antigen, a putative lineage marker: immunofluorescent localization in primary cultures of rat brain. Dev Biol 83: 154-165.
5. Nishiyama A, (2007) Polydendrocytes: NG2 cells with many roles in development and repair of the CNS. Neuroscientist 13: 62-76.
6. Butt AM, Hamilton N, Hubbard P, Pugh M, Ibrahim M, (2005) Synantocytes: the fifth element. J Anat 207: 695-706.
7. Trotter J, Karram K, Nishiyama A, (2010) NG2 cells: properties, progeny and origin. Brain Res Rev 63: 72-82.
8. Simon C, Götz M, Dimou L, (2011) Progenitors in the adult cerebral cortex: cell cycle properties and regulation by physiological stimuli and injury. Glia 59: 869-881.
9. Luzzati F, De Marchis S, Fasolo A, Peretto P, (2006) Neurogenesis in the caudate nucleus of the adult rabbit. J Neurosci 26: 609-621.
10. Ponti G, Peretto P, Bonfanti L (2008) Genesis of neuronal and glial progenitors in the cerebellar cortex of peripuberal and adult rabbits. PLoS ONE 3,e2366.
11. Schoenfeld TA, McKerracher L, Obar R, Vallee RB, (1989) MAP 1A and MAP 1B are structurally related microtubule associated proteins with distinct developmental patterns in the CNS. J Neurosci 9: 1712-1730.
12. Nothias F, Fischer I, Murray M, Mirman S, Vincent JD, (1996) Expression of a phosphorylated isoform of MAP1B is maintained in adult central nervous system areas that retain capacity for structural plasticity. J Comp Neurol 368: 317-334.
13. Ramon-Cueto A, Avila J, (1997) Differential expression of microtubule-associated protein 1B phosphorylated isoforms in the adult rat nervous system. Neuroscience 77: 485-501.
14. Ma D, Connors T, Nothias F, Fischer I, (2000) Regulation of the expression and phosphorylation of microtubule-associated protein 1B during regeneration of adult dorsal root ganglion neurons. Neuroscience 99: 157-170.
15. Chauhan N, Siegel G, (1997) Age-dependent organotypic expression of microtubule-associated proteins (MAP1, MAP2, and MAP5) in rat brain. Neurochem Res 22: 713-719.
16. Kawakami SI, Muramoto K, Ichikawa M, Kuroda Y, (2003) Localization of microtubule-associated protein (MAP) 1B in the postsynaptic densities of the rat cerebral cortex. Cell Mol Neurobiol 23: 887-894.
17. Bloom GS, Luca FC, Vallee RB, (1985) Microtubule-associated protein 1B: identification of a major component of the neuronal cytoskeleton. Proc Natl Acad Sci U S A 82: 5404-5408.
18. Oudega M, Touri F, Deenen MG, Riederer BM, Marani E, (1995) Immunocytochemical localisation of microtubule-associated proteins 1b and 2 in the developing rat spinal cord. J Anat 187: 723-737.
19. Viereck C, Tucker RP, Matus A, (1989) The adult rat olfactory system expresses microtubule-associated proteins found in the developing brain. J Neurosci 9: 3547-3557.
20. Majewska B, Skangiel-Kramska J, (2000) Phosphorylated MAP-1B isoforms in the developing mouse barrel cortex. Int J Dev Neurosci 18: 113-119.
21. Cheng A, Krueger BK, Bambrick LL, (1999) MAP5 expression in proliferating neuroblasts. Brain Res Dev Brain Res 113: 107-713.
22. Riederer BM, (1995) Differential phosphorylation of MAP1b during postnatal development of the cat brain. J Neurocytol 24: 45-54.
23. Ohyu J, Yamanouchi H, Takashima S, (1997) Immunohistochemical study of microtubule-associated protein 5 (MAP5) expression in the developing human brain. Brain Dev 19: 541-546.
24. Ulfig N, Feldhaus C, Setzer M, Bohl J, (2000) Expression of MAP1a and MAP1b in the ganglionic eminence and the internal capsule of the human fetal brain. Neurosci Res 38: 397-405.
25. Black MM, Slaughter T, Fischer I, (1994) Microtubule-associated protein 1b (MAP1b) is concentrated in the distal region of growing axons. J Neurosci 14: 857-870.
26. Gonzalez-Billault C, Avila J, Caceres A, (2001) Evidence for the role of MAP1B in axon formation. Mol Biol Cell 12: 2087-2098.
27. Wu HY, Dawson MR, Reynolds R, Hardy RJ, (2001) Expression of QKI proteins and MAP1B identifies actively myelinating oligodendrocytes in adult rat brain. Mol Cell Neurosci 17: 292-302.
28. Fischer I, Konola J, Cochary E, (1990) Microtubule associated protein (MAP1B) is present in cultured oligodendrocytes and co-localizes with tubulin. J Neurosci Res 27: 112-124.
29. Ulloa L, Ibarrola N, Avila J, Dìez-Guerra FJ, (1994) Microtubule-associated protein 1B (MAP1B) is present in glial cells phosphorylated different than in neurones. Glia 10: 266-275.
30. Vouyiouklis DA, Brophy PJ, (1993) Microtubule-associated protein MAP1B expression precedes the morphological differentiation of oligodendrocytes. J Neurosci Res 35: 257-267.
31. Vouyiouklis DA, Brophy PJ, (1995) Microtubule-associated proteins in developing oligodendrocytes: transient expression of a MAP2c isoform in oligodendrocyte precursors. J Neurosci Res 42: 803-817.
32. Zhao L, Ku L, Chen Y, Xia M, LoPresti P, et al. (2006) QKI binds MAP1B mRNA and enhances MAP1B expression during oligodendrocyte development. Mol Biol Cell 17: 4179-4186.
33. Riederer B, Cohen R, Matus A, (1986) MAP5: a novel brain microtubule associated protein under strong developmental regulation. J Neurocytol 15: 763-775.
34. Calvert RA, Anderton BH, (1985) A microtubule-associated protein (MAP1) which is expressed at elevated levels during development of the rat cerebellum. EMBO J 4: 1171-1176.
35. Greene LA, Liem RKH, Shelanski ML, (1983) Regulation of a high molecular weight microtubule-associated protein in PC12 cells by nerve growth factor. J Cell Biol 96: 76-83.
36. Tucker RP, Garner CC, Matus A, (1989) In situ localization of microtubule associated protein mRNA in the developing and adult rat brain. Neuron 2: 1245-1256.
37. Ma D, Nothias F, Boyne LJ, Fischer I, (1997) Differential regulation of microtubule-associated protein 1B (MAP1B) in rat CNS and PNS during development. J Neurosci Res 49: 319-332.
38. Mansfield SG, Diaz-Nido J, Gordon-Weeks PR, Avila J, (1991) The distribution and phosphorylation of the microtubule-associated protein MAP1B in growth cones. J Neurocytol 21: 1007-1022.
39. Tucker RP, (1990) The roles of microtubule-associated proteins in brain morphogenesis:a review. Brain Res Brain Res Rev 15: 101-120.
40. Riederer BM, (2007) Microtubule-associated protein 1B, a growth and phosphorilated scaffold protein. Brain Res Bull 71: 541-558.
41. Ma D, Chow S, Obrocka M, Connors T, Fischer I, (1999) Induction of microtubule-associated protein 1B expression in Schwann cells during nerve regeneration. Brain Res 823: 141-153.
42. Soares S, Fischer I, Ravaille-Veron M, Vincent JD, Nothias F, (1998) Induction of MAP1B phosphorylation in target-deprived afferent fibers after kainic acid lesion in the adult rat. J Compar Neurol 396: 193-210.
43. Soares S, Barnat M, Salim C, von Boxberg Y, Ravaille-Veron M, et al. (2007) Extensive structural remodeling of the injured spinal cord revealed by phosphorilated MAP1B in sprouting axons and degenerating neurons. Eur J Neurosci 26: 1446-1461.
44. Lu R, Wang H, Liang Z, Ku L, O'Donnell T, et al. (2004) The fragile X protein controls microtubule-associated protein 1B translation and microtubule stability in brain neuron development. Proc Natl Acad Sci U S A 101: 15201-15206.
45. Coffee RL Jr, Williamson AJ, Adkins CM, Gray MC, Page TL, et al. (2012) In vivo neuronal function of the fragile X mental retardation protein is regulated by phosphorilation. Hum Mol Genet 21: 900-915.
46. Allen E, Ding J, Wang W, Pramanik S, Chou J, et al. (2005) Gigaxonin-controlled degradation of MAP1B light chain is critical to neuronal survival. Nature 438: 224-228.
47. Hasegawa M, Arai T, Ihara Y, (1990) Immunochemical evidence that fragments of phosphorylated MAP5 (MAP1B) are bound to neurofibrillary tangles in Alzheimer's disease. Neuron 4: 909-918.
48. Rudrabhatla P, Jaffe H, Pant HC, (2011) Direct evidence of phosphorilated neuronal intermediate filament proteins in neurofibrillary tangles (NFTs): phosphoproteomics of Alzheimer's NFTs. FASEB J 25: 3896-3905.
49. Ponti G, Peretto P, Bonfanti L, (2006) A subpial, transitory germinal zone forms chains of neuronal precursors in the rabbit cerebellum. Dev Biol 294: 168-180.
50. Kukley M, Nishiyama A, Dietrich D, (2010) The fate of synaptic input to NG2 glial cells: neurons specifically downregulate transmitter release onto differentiating oligodendroglial cells. J Neurosci 30: 8320-8331.
51. Frohlich N, Nagy B, Hovhannisyan A, Kukley M, (2011) Fate of neuron-glia synapses during proliferation and differentiation of NG2 cells. J Anat 219: 18-32.
52. Fumagalli M, Daniele S, Lecca D, Lee PR, Parravicini C, et al. (2011) Phenotypic changes, signaling pathway, and functional correlates of GPR17-expressing neural precursor cells during oligodendrocyte differentiation. J Biol Chem 286: 10593-10604.
53. Boda E, Viganò F, Rosa P, Fumagalli M, Labat-Gest V, et al. (2011) The GPR17 receptor in NG2 expressing cells: Focus on in vivo cell maturation and participation in acute trauma and chronic damage. Glia 59: 1958-1973.
54. Watanabe M, Sakurai Y, Ichinose T, Aikawa Y, Kotani M, et al. (2006) Monoclonal antibody Rip specifically recognizes 2′,3′-cyclic nucleotide 3′-phosphodiesterase in oligodentrocytes. J Neurosci Res 84: 525-533.
55. Bradl M, Lassmann H, (2010) Oligodendrocytes: biology and pathology. Acta Neuropathol 119: 37-53.
56. Emery B, (2010) Regulation of oligodendrocyte differentiation and myelination. Science 330: 779-782.
57. Kee N, Sivalingam S, Boonstra R, Wojtowicz JM, (2002) The utility of Ki-67 and BrdU as proliferative markers of adult neurogenesis. J Neurosci Meth 115: 97-105.
58. Lecca D, Trincavelli ML, Gelosa P, Sironi L, Ciana P, et al. (2008) The recently identified P2Y-like receptor GPR17 is a sensor of brain damage and a new target for brain repair. PLoS One 3: e3579.
59. Radde R, Bolmont T, Kaeser SA, Coomaraswamy J, Lindau D, et al. (2006) Abeta42-driven cerebral amyloidosis in transgenic mice reveals early and robust pathology. EMBO Rep 7: 940-946.
60. Nishiyama A, Lin XH, Giese N, Heldin CH, Stallcup WB, (1996) Co-localization of NG2 proteoglycan and PDGF alpha-receptor on O2A progenitor cells in the developing rat brain. J Neurosci Res 43: 299-314.
61. Velez-Fort M, Audinat E, Angulo M, (2009) Functional alpha 7-containing nicotinic receptors of NG2-expressing cells in the hippocampus. Glia 57: 1104-1114.
62. Gage FH, (2000) Mammalian neural stem cells. Science 287: 1433-1438.
63. Kriegstein A, Alvarez-Buylla A, (2009) The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci 32: 149-184.
64. 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.
65. Richardson W, Young K, Tripathi R, McKenzie I, (2011) NG2-glia as multipotent neural stem cells: Fact or Fantasy? Neuron 70: 661-673.
66. Bonfanti L, Peretto P, (2007) Radial glial origin of the adult neural stem cells in the subventricular zone. Prog Neurobiol 83: 24-36.
67. Ihrie RA, Alvarez-Buylla A, (2011) Lake-front property: a unique germinal niche by the lateral ventricles of the adult brain. Neuron 70: 674-686.
68. 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.
69. Lytle JM, Chittajallu R, Wrathall JR, Gallo V, (2009) NG2 cell response in the CNP-EGFP mouse after contusive spinal cord injury. Glia 57: 270-285.
70. Robel S, Berninger B, Gotz M, (2011) The stem cell potential of glia: lessons from reactive gliosis. Nat Rev Neurosci 12: 88-104.
71. Kozorovitskiy Y, Gould E, (2003) Adult neurogenesis: a mechanism for brain repair? J Clin Exp Neuropsych 25: 721-732.
72. Bonfanti L, (2011) From hydra regeneration to human brain structural plasticity: a long trip through narrowing roads. ScientificWorldJournal 11: 1270-1299.
73. Ligon KL, Fancy SP, Franklin RJ, Rowitch DH, (2006) Olig gene function in CNS development and disease. Glia 54: 1-10.
74. Stolt CC, Wegner M, (2010) SoxE function in vertebrate nervous system development. Int J Biochem Cell Biol 42: 437-440.
75. Pevny LH, Nicolis SK, (2010) Sox2 roles in neural stem cells. Int J Biochem Cell Biol 42: 421-424.
76. Ciana P, Fumagalli M, Trincavelli ML, Verderio C, Rosa P, et al. (2006) The orphan receptor GPR17 identified as a new dual uracil nucleotides/cysteinyl-leukotrienes receptor. EMBO J 25: 4615-4627.
77. Chen Y, Wu H, Wang S, Koito H, Li J, et al. (2009) The oligodendrocyte-specific G protein-coupled receptor GPR17 is a cell-intrinsic timer of myelination. Nat Neurosci 12: 1398-1406.R.
78. Baumann N, Pham Dinh D, (2001) Biology of oligodendrocyte and myelin in the mammalian central nervous system. Physiol Rev 81: 871-927.