Oligodendrocyte Precursor Cells Modulate the Neuronal Network by Activity-Dependent Ectodomain Cleavage of Glial NG2

PLoS Biology

Volumn 12, Issue 11, 2014, Pages

  Sakry, Dominik ^a   Neitz, Angela ^b,d   Singh, Jeet ^c   Frischknecht, Renato ^c   Marongiu, Daniele ^b   Binamé, Fabien ^a   Perera, Sumudhu S ^a   Endres, Kristina ^b   Lutz, Beat ^b   Radyushkin, Konstantin ^a   Trotter, Jacqueline ^a   Mittmann, Thomas ^b  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^c LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

^d GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADAM10 ENDOPEPTIDASE; ADAM17; ALPHA SECRETASE; AMPA RECEPTOR; CELL PROTEIN; GAMMA SECRETASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NG2 PROTEIN; PROTEIN C FOS; UNCLASSIFIED DRUG; ADAM PROTEIN; ADAM10 PROTEIN, MOUSE; ANTIGEN; CHONDROITIN SULFATE PROTEOGLYCAN 4; GLUTAMATE RECEPTOR; MEMBRANE PROTEIN; PROTEOGLYCAN; SECRETASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL INTERACTION; CONTROLLED STUDY; ENZYME ACTIVITY; EXCITATORY POSTSYNAPTIC POTENTIAL; EXTRACELLULAR MATRIX; LONG TERM POTENTIATION; MALE; MOUSE; NERVE CELL EXCITABILITY; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NONHUMAN; OLIGODENDROCYTE PRECURSOR CELL; PREPULSE INHIBITION; PROTEIN CLEAVAGE; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN SECRETION; REGULATORY MECHANISM; SENSORY GATING; SOMATOSENSORY CORTEX; SYNAPTIC TRANSMISSION; ANIMAL; CELL LINE; KNOCKOUT MOUSE; METABOLISM; NERVE CELL; OLIGODENDROGLIA; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; PYRAMIDAL NERVE CELL; SYNAPSE;

ADAM PROTEINS; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; ANTIGENS; CELL LINE; EXTRACELLULAR MATRIX; LONG-TERM POTENTIATION; MALE; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; NEURONAL PLASTICITY; NEURONS; OLIGODENDROGLIA; PROTEIN STRUCTURE, TERTIARY; PROTEOGLYCANS; PYRAMIDAL CELLS; RECEPTORS, GLUTAMATE; RECEPTORS, N-METHYL-D-ASPARTATE; SENSORY GATING; SYNAPSES;

EID: 84912535386     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001993     Document Type: Article

References (84)

1. Nishiyama A, Komitova M, Suzuki R, Zhu X, (2009) Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity. Nat Rev Neurosci 10: 9–22.
2. Trotter J, Karram K, Nishiyama A, (2010) NG2 cells: Properties, progeny and origin. Brain Res reviews 63: 72–82.
3. Clarke LE, Young KM, Hamilton NB, Li H, Richardson WD, et al. (2012) Properties and fate of oligodendrocyte progenitor cells in the corpus callosum, motor cortex, and piriform cortex of the mouse. J Neurosci 32: 8173–8185.
4. Levine JM, Stincone F, Lee YS, (1993) Development and differentiation of glial precursor cells in the rat cerebellum. Glia 7: 307–321.
5. Nishiyama A, Dahlin KJ, Prince JT, Johnstone SR, Stallcup WB, (1991) The primary structure of NG2, a novel membrane-spanning proteoglycan. J Cell Biol 114: 359–371.
6. Gallo V, Mangin JM, Kukley M, Dietrich D, (2008) Synapses on NG2-expressing progenitors in the brain: multiple functions? J Physiol 586: 3767–3781.
7. 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.
8. Bergles DE, Roberts JD, Somogyi P, Jahr CE, (2000) Glutamatergic synapses on oligodendrocyte precursor cells in the hippocampus. Nature 405: 187–191.
9. Lin SC, Bergles DE, (2004) Synaptic signaling between GABAergic interneurons and oligodendrocyte precursor cells in the hippocampus. Nat Neurosci 7: 24–32.
10. Jabs R, Pivneva T, Huttmann K, Wyczynski A, Nolte C, et al. (2005) Synaptic transmission onto hippocampal glial cells with hGFAP promoter activity. J Cell Sci 118: 3791–3803.
11. Kukley M, Capetillo-Zarate E, Dietrich D, (2007) Vesicular glutamate release from axons in white matter. Nat Neurosci 10: 311–320.
12. Kukley M, Kiladze M, Tognatta R, Hans M, Swandulla D, et al. (2008) Glial cells are born with synapses. FASEB J 22: 2957–2969.
13. Lin SC, Huck JH, Roberts JD, Macklin WB, Somogyi P, et al. (2005) Climbing fiber innervation of NG2-expressing glia in the mammalian cerebellum. Neuron 46: 773–785.
14. Ziskin JL, Nishiyama A, Rubio M, Fukaya M, Bergles DE, (2007) Vesicular release of glutamate from unmyelinated axons in white matter. Nat Neurosci 10: 321–330.
15. De Biase LM, Nishiyama A, Bergles DE, (2010) Excitability and synaptic communication within the oligodendrocyte lineage. J Neurosci 30: 3600–3611.
16. 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.
17. Mangin JM, Li P, Scafidi J, Gallo V, (2012) Experience-dependent regulation of NG2 progenitors in the developing barrel cortex. Nat Neurosci 15: 1192–1194.
18. Simon C, Gotz M, Dimou L, (2011) Progenitors in the adult cerebral cortex: cell cycle properties and regulation by physiological stimuli and injury. Glia 59: 869–881.
19. Wake H, Lee PR, Fields RD, (2011) Control of local protein synthesis and initial events in myelination by action potentials. Science 333: 1647–1651.
20. Lundgaard I, Luzhynskaya A, Stockley JH, Wang Z, Evans KA, et al. (2013) Neuregulin and BDNF Induce a Switch to NMDA Receptor-Dependent Myelination by Oligodendrocytes. PLoS Biol 11: e1001743.
21. Gibson EM, Purger D, Mount CW, Goldstein AK, Lin GL, et al. (2014) Neuronal Activity Promotes Oligodendrogenesis and Adaptive Myelination in the Mammalian Brain. Science 344: 1252304.
22. Demerens C, Stankoff B, Logak M, Anglade P, Allinquant B, et al. (1996) Induction of myelination in the central nervous system by electrical activity. Proc Natl Acad Sci U S A 93: 9887–9892.
23. Mangin JM, Gallo V, (2011) The curious case of NG2 cells: transient trend or game changer? ASN Neuro 3: e00052.
24. Bergles DE, Jabs R, Steinhauser C, (2010) Neuron-glia synapses in the brain. Brain Res Rev 63: 130–137.
25. Sakry D, Karram K, Trotter J, (2011) Synapses between NG2 glia and neurons. J Anat 219: 2–7.
26. Hill RA, Nishiyama A, (2014) NG2 cells (polydendrocytes): Listeners to the neural network with diverse properties. Glia 62: 1195–1210.
27. Trotter J, (2005) NG2-positive cells in CNS function and the pathological role of antibodies against NG2 in demyelinating diseases. J Neurol Sci 233: 37–42.
28. Aoto J, Martinelli DC, Malenka RC, Tabuchi K, Sudhof TC, (2013) Presynaptic neurexin-3 alternative splicing trans-synaptically controls postsynaptic AMPA receptor trafficking. Cell 154: 75–88.
29. Gokce O, Sudhof TC, (2013) Membrane-tethered monomeric neurexin LNS-domain triggers synapse formation. J Neurosci 33: 14617–14628.
30. Stegmuller J, Werner H, Nave KA, Trotter J, (2003) The proteoglycan NG2 is complexed with alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors by the PDZ glutamate receptor interaction protein (GRIP) in glial progenitor cells. Implications for glial-neuronal signaling. J Biol Chem 278: 3590–3598.
31. Nishiyama A, Lin XH, Stallcup WB, (1995) Generation of truncated forms of the NG2 proteoglycan by cell surface proteolysis. Mol Biol Cell 6: 1819–1832.
32. Deepa SS, Carulli D, Galtrey C, Rhodes K, Fukuda J, et al. (2006) Composition of perineuronal net extracellular matrix in rat brain: a different disaccharide composition for the net-associated proteoglycans. J Biol Chem 281: 17789–17800.
33. Reiss K, Maretzky T, Ludwig A, Tousseyn T, de Strooper B, et al. (2005) ADAM10 cleavage of N-cadherin and regulation of cell-cell adhesion and beta-catenin nuclear signalling. EMBO J 24: 742–752.
34. Suzuki K, Hayashi Y, Nakahara S, Kumazaki H, Prox J, et al. (2012) Activity-dependent proteolytic cleavage of neuroligin-1. Neuron 76: 410–422.
35. Prox J, Bernreuther C, Altmeppen H, Grendel J, Glatzel M, et al. (2013) Postnatal disruption of the disintegrin/metalloproteinase ADAM10 in brain causes epileptic seizures, learning deficits, altered spine morphology, and defective synaptic functions. J Neurosci 33: : 12915–12928, 12928a.
36. Pan D, Rubin GM, (1997) Kuzbanian controls proteolytic processing of Notch and mediates lateral inhibition during Drosophila and vertebrate neurogenesis. Cell 90: 271–280.
37. Blaumueller CM, Qi H, Zagouras P, Artavanis-Tsakonas S, (1997) Intracellular cleavage of Notch leads to a heterodimeric receptor on the plasma membrane. Cell 90: 281–291.
38. Jung M, Kramer E, Grzenkowski M, Tang K, Blakemore W, et al. (1995) Lines of murine oligodendroglial precursor cells immortalized by an activated neu tyrosine kinase show distinct degrees of interaction with axons in vitro and in vivo. Eur J Neurosci 7: 1245–1265.
39. Biname F, Sakry D, Dimou L, Jolivel V, Trotter J, (2013) NG2 Regulates Directional Migration of Oligodendrocyte Precursor Cells via Rho GTPases and Polarity Complex Proteins. J Neurosci 33: 10858–10874.
40. Watkins TA, Emery B, Mulinyawe S, Barres BA, (2008) Distinct stages of myelination regulated by gamma-secretase and astrocytes in a rapidly myelinating CNS coculture system. Neuron 60: 555–569.
41. Peixoto RT, Kunz PA, Kwon H, Mabb AM, Sabatini BL, et al. (2012) Transsynaptic signaling by activity-dependent cleavage of neuroligin-1. Neuron 76: 396–409.
42. Karram K, Goebbels S, Schwab M, Jennissen K, Seifert G, et al. (2008) NG2-expressing cells in the nervous system revealed by the NG2-EYFP-knockin mouse. Genesis 46: 743–757.
43. Yoshimura Y, Ohmura T, Komatsu Y, (2003) Two forms of synaptic plasticity with distinct dependence on age, experience, and NMDA receptor subtype in rat visual cortex. J Neurosci 23: 6557–6566.
44. Koike M, Iino M, Ozawa S, (1997) Blocking effect of 1-naphthyl acetyl spermine on Ca(2+)-permeable AMPA receptors in cultured rat hippocampal neurons. Neurosci Res 29: 27–36.
45. Hu TT, Laeremans A, Eysel UT, Cnops L, Arckens L, (2009) Analysis of c-fos and zif268 expression reveals time-dependent changes in activity inside and outside the lesion projection zone in adult cat area 17 after retinal lesions. Cereb Cortex 19: 2982–2992.
46. Geyer MA, Krebs-Thomson K, Braff DL, Swerdlow NR, (2001) Pharmacological studies of prepulse inhibition models of sensorimotor gating deficits in schizophrenia: a decade in review. Psychopharmacology 156: 117–154.
47. Chow VW, Mattson MP, Wong PC, Gleichmann M, (2010) An overview of APP processing enzymes and products. Neuromol Med 12: 1–12.
48. Riedle S, Kiefel H, Gast D, Bondong S, Wolterink S, et al. (2009) Nuclear translocation and signalling of L1-CAM in human carcinoma cells requires ADAM10 and presenilin/gamma-secretase activity. Biochem J 420: 391–402.
49. Tai CY, Kim SA, Schuman EM, (2008) Cadherins and synaptic plasticity. Curr Opin Cell Biol 20: 567–575.
50. Zolkiewska A, (2008) ADAM proteases: ligand processing and modulation of the Notch pathway. Cell Mol Life Sci 65: 2056–2068.
51. Kandachar V, Roegiers F, (2012) Endocytosis and control of Notch signaling. Curr Opin Cell Biol 24: 534–540.
52. Lieber T, Kidd S, Young MW, (2002) kuzbanian-mediated cleavage of Drosophila Notch. Gene Dev 16: 209–221.
53. Sambamurti K, Shioi J, Anderson JP, Pappolla MA, Robakis NK, (1992) Evidence for intracellular cleavage of the Alzheimer's amyloid precursor in PC12 cells. J Neurosci Res 33: 319–329.
54. Pimplikar SW, Suryanarayana A, (2011) Detection of APP intracellular domain in brain tissue. Methods Mol Biol 670: 85–91.
55. Asher RA, Morgenstern DA, Properzi F, Nishiyama A, Levine JM, et al. (2005) Two separate metalloproteinase activities are responsible for the shedding and processing of the NG2 proteoglycan in vitro. Mol Cell Neurosci 29: 82–96.
56. Makagiansar IT, Williams S, Dahlin-Huppe K, Fukushi J, Mustelin T, et al. (2004) Phosphorylation of NG2 proteoglycan by protein kinase C-alpha regulates polarized membrane distribution and cell motility. J Biol Chem 279: 55262–55270.
57. Tillet E, Ruggiero F, Nishiyama A, Stallcup WB, (1997) The membrane-spanning proteoglycan NG2 binds to collagens V and VI through the central nonglobular domain of its core protein. J Biol Chem 272: 10769–10776.
58. Otmakhov N, Khibnik L, Otmakhova N, Carpenter S, Riahi S, et al. (2004) Forskolin-induced LTP in the CA1 hippocampal region is NMDA receptor dependent. J Neurophysiol 91: 1955–1962.
59. Tauskela JS, Fang H, Hewitt M, Brunette E, Ahuja T, et al. (2008) Elevated synaptic activity preconditions neurons against an in vitro model of ischemia. J Biol Chem 283: 34667–34676.
60. Maldonado PP, Velez-Fort M, Levavasseur F, Angulo MC, (2013) Oligodendrocyte precursor cells are accurate sensors of local K+ in mature gray matter. J Neurosci 33: 2432–2442.
61. Marcello E, Gardoni F, Mauceri D, Romorini S, Jeromin A, et al. (2007) Synapse-associated protein-97 mediates alpha-secretase ADAM10 trafficking and promotes its activity. J Neurosci 27: 1682–1691.
62. Malinverno M, Carta M, Epis R, Marcello E, Verpelli C, et al. (2010) Synaptic localization and activity of ADAM10 regulate excitatory synapses through N-cadherin cleavage. J Neurosci 30: 16343–16355.
63. Brakebusch C, Seidenbecher CI, Asztely F, Rauch U, Matthies H, et al. (2002) Brevican-deficient mice display impaired hippocampal CA1 long-term potentiation but show no obvious deficits in learning and memory. Mol Cell Biol 22: 7417–7427.
64. Bukalo O, Schachner M, Dityatev A, (2001) Modification of extracellular matrix by enzymatic removal of chondroitin sulfate and by lack of tenascin-R differentially affects several forms of synaptic plasticity in the hippocampus. Neuroscience 104: 359–369.
65. Evers MR, Salmen B, Bukalo O, Rollenhagen A, Bosl MR, et al. (2002) Impairment of L-type Ca2+ channel-dependent forms of hippocampal synaptic plasticity in mice deficient in the extracellular matrix glycoprotein tenascin-C. J Neurosci 22: 7177–7194.
66. Frischknecht R, Heine M, Perrais D, Seidenbecher CI, Choquet D, et al. (2009) Brain extracellular matrix affects AMPA receptor lateral mobility and short-term synaptic plasticity. Nat Neurosci 12: 897–904.
67. Varoqueaux F, Aramuni G, Rawson RL, Mohrmann R, Missler M, et al. (2006) Neuroligins determine synapse maturation and function. Neuron 51: 741–754.
68. Krueger DD, Tuffy LP, Papadopoulos T, Brose N, (2012) The role of neurexins and neuroligins in the formation, maturation, and function of vertebrate synapses. Curr Opin Neurobiol 22: 412–422.
69. Nicoll RA, Kauer JA, Malenka RC, (1988) The current excitement in long-term potentiation. Neuron 1: 97–103.
70. Rebola N, Carta M, Lanore F, Blanchet C, Mulle C, (2011) NMDA receptor-dependent metaplasticity at hippocampal mossy fiber synapses. Nat Neurosci 14: 691–693.
71. Kamboj SK, Swanson GT, Cull-Candy SG, (1995) Intracellular spermine confers rectification on rat calcium-permeable AMPA and kainate receptors. J Physiol 486 (Pt 2): 297–303.
72. McBain CJ, Dingledine R, (1993) Heterogeneity of synaptic glutamate receptors on CA3 stratum radiatum interneurones of rat hippocampus. J Physiol 462: 373–392.
73. Jonas P, Racca C, Sakmann B, Seeburg PH, Monyer H, (1994) Differences in Ca2+ permeability of AMPA-type glutamate receptor channels in neocortical neurons caused by differential GluR-B subunit expression. Neuron 12: 1281–1289.
74. Kumar SS, Bacci A, Kharazia V, Huguenard JR, (2002) A developmental switch of AMPA receptor subunits in neocortical pyramidal neurons. J Neurosci 22: 3005–3015.
75. Noh KM, Yokota H, Mashiko T, Castillo PE, Zukin RS, et al. (2005) Blockade of calcium-permeable AMPA receptors protects hippocampal neurons against global ischemia-induced death. Proc Natl Acad Sci U S A 102: 12230–12235.
76. Wang Y, Neubauer FB, Luscher HR, Thurley K, (2010) GABAB receptor-dependent modulation of network activity in the rat prefrontal cortex in vitro. Eur J Neurosci 31: 1582–1594.
77. Beckmann G, Hanke J, Bork P, Reich JG, (1998) Merging extracellular domains: fold prediction for laminin G-like and amino-terminal thrombospondin-like modules based on homology to pentraxins. J Mol Biol 275: 725–730.
78. Rudenko G, Hohenester E, Muller YA, (2001) LG/LNS domains: multiple functions – one business end? Trends Biochem Sci 26: 363–368.
79. O'Brien RJ, Xu D, Petralia RS, Steward O, Huganir RL, et al. (1999) Synaptic clustering of AMPA receptors by the extracellular immediate-early gene product Narp. Neuron 23: 309–323.
80. Mansbach RS, Braff DL, Geyer MA, (1989) Prepulse inhibition of the acoustic startle response is disrupted by N-ethyl-3,4-methylenedioxyamphetamine (MDEA) in the rat. Eur J Pharmacol 167: 49–55.
81. Mansbach RS, Geyer MA, (1991) Parametric determinants in pre-stimulus modification of acoustic startle: interaction with ketamine. Psychopharmacology 105: 162–168.
82. Diers-Fenger M, Kirchhoff F, Kettenmann H, Levine JM, Trotter J, (2001) AN2/NG2 protein-expressing glial progenitor cells in the murine CNS: isolation, differentiation, and association with radial glia. Glia 34: 213–228.
83. Ludwig A, Hundhausen C, Lambert MH, Broadway N, Andrews RC, et al. (2005) Metalloproteinase inhibitors for the disintegrin-like metalloproteinases ADAM10 and ADAM17 that differentially block constitutive and phorbol ester-inducible shedding of cell surface molecules. Comb Chem High T Scr 8: 161–171.
84. Levenson JM, O'Riordan KJ, Brown KD, Trinh MA, Molfese DL, et al. (2004) Regulation of histone acetylation during memory formation in the hippocampus. J Biol Chem 279: 40545–40559.