Conditional deletion of the L-type calcium channel cav1.2 in oligodendrocyte progenitor cells affects postnatal myelination in mice

Journal of Neuroscience

Volumn 36, Issue 42, 2016, Pages 10853-10869

  Cheli, Veronica T ^a   González, Diara A Santiago ^a   Lama, Tenzing Namgyal ^a   Spreuer, Vilma ^a   Handley, Vance ^b   Murphy, Geoffrey G ^c   Paez, Pablo M ^a  

^a UNIVERSITY AT BUFFALO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Calcium; Cav1.2; Myelination; Oligodendrocytes; Voltage operated Ca2+ channels

Indexed keywords

CALCIUM CHANNEL L TYPE; CACNA1C PROTEIN, MOUSE; MYELIN PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW PROGENITOR CELL; CELL MIGRATION ASSAY; CELL PROLIFERATION ASSAY; CONDITIONING; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DEGENERATIVE DISEASE; ELECTRON MICROSCOPY; GENOTYPE PHENOTYPE CORRELATION; IMMUNOCYTOCHEMISTRY; MOUSE; MYELINATION; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; ANIMAL; BIOSYNTHESIS; CELL PROLIFERATION; FEMALE; GENE DELETION; GENETICS; KNOCKOUT MOUSE; MALE; MYELIN SHEATH; NEURAL STEM CELL; NEWBORN; PHYSIOLOGY; PRIMARY CELL CULTURE;

ANIMALS; ANIMALS, NEWBORN; CALCIUM CHANNELS, L-TYPE; CELL PROLIFERATION; FEMALE; GENE DELETION; MALE; MICE; MICE, KNOCKOUT; MYELIN PROTEINS; MYELIN SHEATH; NEURAL STEM CELLS; OLIGODENDROGLIA; PRIMARY CELL CULTURE;

EID: 84991822112     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1770-16.2016     Document Type: Article

References (49)

1. ++ currents. Glia 17:181–194.
2. Amur-Umarjee S, Phan T, Campagnoni AT (1993) Myelin basic protein mRNA translocation in oligodendrocytes is inhibited by astrocytes in vitro. J Neurosci Res 36: 99–110.
3. Bahr BA, Kessler M, Rivera S, Vanderklish PW, Hall RA, Mutneja MS, Gall C, Hoffman KB (1995) Stable maintenance of glutamate receptors and other synaptic components in long-term hippocampal slices. Hippocampus 5:425–439.
4. Berger T, Schnitzer J, Orkand PM, Kettenmann H (1992) Sodium and calcium currents in glial cells of the mouse corpus callosum slice. Eur J Neurosci 4:1271–1284.
5. Borges K, Wolswijk G, Ohlemeyer C, Kettenmann H (1995) Adult rat optic nerve oligodendrocyte progenitor cells express a distinct repertoire of voltage- and ligand-gated ion channels. J Neurosci Res 40:591–605.
6. ++ entry promotes oligodendrocyte progenitor cells maturation and myelination in vitro. Exp Neurol 265:69–83.
7. Chittajallu R, Aguirre A, Gallo V (2004) NG2-positive cells in the mouse white and grey matter display distinct physiological properties. J Physiol 561:109–122.
8. Dawitz J, Kroon T, Hjorth JJ, Meredith RM (2011) Functional calcium imaging in developing cortical networks. J Vis Exp pii:3550.
9. Dyer CA, Benjamins JA (1989) Organization of oligodendroglial membrane sheets: II. Galactocerebroside:antibody interactions signal changes in cy-toskeleton and myelin basic protein. J Neurosci Res 24:212–221.
10. Ertel EA, Campbell KP, Harpold MM, Hofmann F, Mori Y, Perez-Reyes E, Schwartz A, Snutch TP, Tanabe T, Birnbaumer L, Tsien RW, Catterall WA (2000) Nomenclature of voltage-gated calcium channels. Neuron 25: 533–535.
11. Foran DR, Peterson AC (1992) Myelin acquisition in the central nervous system of the mouse revealed by an MBP-Lac Z transgene. J Neurosci 12:4890–4897.
12. ++ currents and process mophology in white matter oligodendrocyte precursor cells by golli-myelin proteins. Glia 58:1292–1303.
13. Gallin WJ, Greenberg ME (1995) Calcium regulation of gene expression in neurons: the mode of entry matters. Curr Opin Neurobiol 5:367–374.
14. Gallo V, Mangin JM, Kukley M, Dietrich D (2008) Synapses on NG2-expressing progenitors in the brain: multiple functions? J Physiol 586: 3767–3781.
15. Ge WP, Zhou W, Luo Q, Jan LY, Jan YN (2009) Dividing glial cells maintain differentiated properties including complex morphology and functional synapses. Proc Natl Acad Sci U S A 106:328–333.
16. Ghiani CA, Starcevic M, Rodriguez-Fernandez IA, Nazarian R, Cheli VT, Chan LN, Malvar JS, de Vellis J, Sabatti C, Dell’Angelica EC (2010) The dysbindin-containing complex (BLOC-1) in brain: developmental regulation, interaction with SNARE proteins and role in neurite outgrowth. Mol Psychiatry 15:204–215.
17. Grynkiewicz G, Poenie M, Tsien RY (1985) A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem 260: 3440–3450.
18. ++-signaling pathways and highly motile processes. PLoS One 6:e17575.
19. Hamilton N, Vayro S, Wigley R, Butt AM (2010) Axons and astrocytes release ATP and glutamate to evoke calcium signals in NG2-glia. Glia 58: 66–79.
20. Hell JW, Westenbroek RE, Warner C, Ahlijanian MK, Prystay W, Gilbert MM, Snutch TP, Catterall WA (1993) Identification and differential subcellular localization of the neuronal class C and class D L-type calcium channel alpha 1 subunits. J Cell Biol 123:949–962.
21. Jacobs EC, Pribyl TM, Feng JM, Kampf K, Spreur V, Campagnoni C, Colwell CS, Reyes SD, Martin M, Handley V, Hiltner TD, Readhead C, Jacobs RE, Messing A, Fisher RS, Campagnoni AT (2005) Region-specific myelin pathology in mice lacking the golli products of the myelin basic protein gene. J Neurosci 25:7004–7013.
22. + CNS glial progenitors remain committed to the oligodendrocyte lineage in postnatal life and following neurodegeneration. Neuron 68:668–681.
23. 2+ channels in cells of the oligodendrocyte lineage. Glia 13:1–12.
24. Kukley M, Kiladze M, Tognatta R, Hans M, Swandulla D, Schramm J, Dietrich D (2008) Glial cells are born with synapses. FASEB J 22:2957– 2969.
25. + cells: matching physiological studies with gene expression profiles. Brain Res 1638:138–160.
26. Lin SC, Bergles DE (2004) Synaptic signaling between GABAergic interneurons and oligodendrocyte precursor cells in the hippocampus. Nat Neurosci 7:24–32.
27. Lu QR, Sun T, Zhu Z, Ma N, Garcia M, Stiles CD, Rowitch DH (2002) Common developmental requirement for Olig function indicates a motor neuron/oligodendrocyte connection. Cell 109:75–86.
28. + in mature gray matter. J Neurosci 33:2432–2442.
29. Marques S et al. (2016) Oligodendrocyte heterogeneity in the mouse juvenile and adult central nervous system. Science 352:1326–1329.
30. Paez PM, Spreuer V, Handley V, Feng JM, Campagnoni C, Campagnoni AT (2007) Increased expression of golli myelin basic proteins enhances calcium influx into oligodendroglial cells. J Neurosci 27:12690–12699.
31. ++ influx. J Neurosci 29:6663–6676.
32. ++ channels in the proliferation and death of oligodendrocyte precursor cells by Golli proteins. ASN Neuro 1: pii: e00003.
33. ++ influx and migration in oligodendrocyte precursor cells. J Neurosci 30:6422–6433.
34. Paez PM, Fulton D, Spreuer V, Handley V, Campagnoni AT (2011) Modulation of canonical transient receptor potential channel 1 in the proliferation of oligodendrocyte precursor cells by the golli products of the myelin basic protein gene. J Neurosci 31:3625–3637.
35. ++ channels. Cell 102:89–97.
36. ++ channels are essential for glutamate-mediated creb phosphorylation and C-Fos gene expression in striatal neurons. J Neurosci 19:6348–6359.
37. Reyes SD, Campagnoni AT (2002) Two separate domains in the golli myelin basic proteins are responsible for nuclear targeting and process extension in transfected cells. J Neurosci Res 69:587–596.
38. Sperber BR, McMorris FA (2001) Fyn tyrosine kinase regulates oligodendroglial cell development but is not required for morphological differentiation of oligodendrocytes. J Neurosci Res 63:303–312.
39. Suzumura A, Bhat S, Eccleston PA, Lisak RP, Silberberg DH (1984) The isolation and long-term culture of oligodendrocytes from newborn mouse brain. Brain Res 324:379–383.
40. Takebayashi H, Nabeshima Y, Yoshida S, Chisaka O, Ikenaka K, Nabeshima Y (2002) The basic helix-loop-helix factor Olig2 is essential for the development of motoneuron and oligodendrocyte lineages. Curr Biol 12:1157– 1163.
41. ++ exchang-ers is required for GABA-induced NG2 cell migration. J Cell Biol 186:113– 128.
42. Verkhratsky AN, Trotter J, Kettenmann H (1990) Cultured glial precursor cells from mousecortex express two types of calcium currents. Neurosci Lett 112:194–198.
43. ++ channel expression in the oligodendrocyte lineage. Eur J Neurosci 4:1035–1048.
44. White JA, McKinney BC, John MC, Powers PA, Kamp TJ, Murphy GG (2008) Conditional forebrain deletion of the L-type calcium channel CaV1.2 disrupts remote spatial memories in mice. Learn Mem 15:1–5.
45. Young KM, Psachoulia K, Tripathi RB, Dunn SJ, Cossell L, Attwell D, To-hyama K, Richardson WD (2013) Oligodendrocyte dynamics in the healthy adult CNS: evidence for myelin remodeling. Neuron 77:873–885.
46. 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.
47. Zhang Y, Chen K, Sloan SA, Bennett ML, Scholze AR, O’Keeffe S, Phatnani HP, Guarnieri P, Caneda C, Ruderisch N, Deng S, Liddelow SA, Zhang C, Daneman R, Maniatis T, Barres BA, Wu JQ (2014) An RNA-sequencing transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex. J Neurosci 34:11929–11947.
48. Zhou Q, Anderson DJ (2002) The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 109:61–73.
49. Zhu X, Hill RA, Dietrich D, Komitova M, Suzuki R, Nishiyama A (2011) Age-dependent fate and lineage restriction of single NG2 cells. Development 138:745–753.