Myelin Proteolipid Protein Complexes with αv Integrin and AMPA Receptors In Vivo and Regulates AMPA-Dependent Oligodendrocyte Progenitor Cell Migration Through the Modulation of Cell-Surface GluR2 Expression

Overview

Journal J Neurosci

Specialty Neurology

Date 2015 Aug 28

PMID 26311781

Citations 24

Authors

Danielle E Harlow

Katherine E Saul

Hitoshi Komuro

Wendy B Macklin

Affiliations

Soon will be listed here.

Abstract

Significance Statement: After demyelination, such as occurs in multiple sclerosis, remyelination of axons is often incomplete, leading to loss of neuronal function and clinical disability. Remyelination may fail because oligodendrocyte precursor cells (OPCs) do not completely migrate into demyelinated areas or OPCs in lesions may not mature into myelinating oligodendrocytes. We have found that the myelin proteolipid protein is critical to regulating OPC migratory responses to the neurotransmitter glutamate through modulation of cell-surface expression of the calcium-impermeable GluR2 subunit of the AMPA glutamate receptor and increased intercellular Ca(2+) signaling. Altered glutamate homeostasis has been reported in demyelinated lesions. Therefore, understanding how OPCs respond to glutamate has important implications for treatment after white matter injury and disease.

Citing Articles

A New Acquaintance of Oligodendrocyte Precursor Cells in the Central Nervous System.

Ma Z, Zhang W, Wang C, Su Y, Yi C, Niu J Neurosci Bull. 2024; 40(10):1573-1589.

PMID: 39042298 PMC: 11422404. DOI: 10.1007/s12264-024-01261-8.

Norepinephrine modulates calcium dynamics in cortical oligodendrocyte precursor cells promoting proliferation during arousal in mice.

Lu T, Hanumaihgari P, Hsu E, Agarwal A, Kawaguchi R, Calabresi P Nat Neurosci. 2023; 26(10):1739-1750.

PMID: 37697112 PMC: 10630072. DOI: 10.1038/s41593-023-01426-0.

Recent Insights into the Functional Role of AMPA Receptors in the Oligodendrocyte Lineage Cells In Vivo.

Kukley M Int J Mol Sci. 2023; 24(4).

PMID: 36835546 PMC: 9967469. DOI: 10.3390/ijms24044138.

GABA Receptor Agonists Protect From Excitotoxic Damage Induced by AMPA in Oligodendrocytes.

Bayon-Cordero L, Ochoa-Bueno B, Ruiz A, Ozalla M, Matute C, Sanchez-Gomez M Front Pharmacol. 2022; 13:897056.

PMID: 35959434 PMC: 9360600. DOI: 10.3389/fphar.2022.897056.

Cannabinoids modulate proliferation, differentiation, and migration signaling pathways in oligodendrocytes.

de Almeida V, Seabra G, Reis-de-Oliveira G, Zuccoli G, Rumin P, Fioramonte M Eur Arch Psychiatry Clin Neurosci. 2022; 272(7):1311-1323.

PMID: 35622101 DOI: 10.1007/s00406-022-01425-5.

References

Suzuki S, Goldman J . Multiple cell populations in the early postnatal subventricular zone take distinct migratory pathways: a dynamic study of glial and neuronal progenitor migration. J Neurosci. 2003; 23(10):4240-50. PMC: 6741090. View

Mallon B, Shick H, Kidd G, Macklin W . Proteolipid promoter activity distinguishes two populations of NG2-positive cells throughout neonatal cortical development. J Neurosci. 2002; 22(3):876-85. PMC: 6758537. View

Bagayogo I, Dreyfus C . Regulated release of BDNF by cortical oligodendrocytes is mediated through metabotropic glutamate receptors and the PLC pathway. ASN Neuro. 2009; 1(1). PMC: 2695578. DOI: 10.1042/AN20090006. View

Haydar T, Wang F, Schwartz M, Rakic P . Differential modulation of proliferation in the neocortical ventricular and subventricular zones. J Neurosci. 2000; 20(15):5764-74. PMC: 3823557. View

Platel J, Lacar B, Bordey A . GABA and glutamate signaling: homeostatic control of adult forebrain neurogenesis. J Mol Histol. 2007; 38(4):303-11. PMC: 2556597. DOI: 10.1007/s10735-007-9103-8. View

Bercury K, Dai J, Sachs H, Ahrendsen J, Wood T, Macklin W . Conditional ablation of raptor or rictor has differential impact on oligodendrocyte differentiation and CNS myelination. J Neurosci. 2014; 34(13):4466-80. PMC: 3965777. DOI: 10.1523/JNEUROSCI.4314-13.2014. View

Yuan X, Eisen A, McBain C, Gallo V . A role for glutamate and its receptors in the regulation of oligodendrocyte development in cerebellar tissue slices. Development. 1998; 125(15):2901-14. DOI: 10.1242/dev.125.15.2901. View

Blakemore W . Regeneration and repair in multiple sclerosis: the view of experimental pathology. J Neurol Sci. 2007; 265(1-2):1-4. DOI: 10.1016/j.jns.2007.03.006. View

Etxeberria A, Mangin J, Aguirre A, Gallo V . Adult-born SVZ progenitors receive transient synapses during remyelination in corpus callosum. Nat Neurosci. 2010; 13(3):287-289. PMC: 4681435. DOI: 10.1038/nn.2500. View

10.

Brand-Schieber E, Werner P . AMPA/kainate receptors in mouse spinal cord cell-specific display of receptor subunits by oligodendrocytes and astrocytes and at the nodes of Ranvier. Glia. 2003; 42(1):12-24. DOI: 10.1002/glia.10136. View

11.

Curtis R, Cohen J, Hanley M, Gregson N, Reynolds R, Wilkin G . Development of macroglial cells in rat cerebellum. I. Use of antibodies to follow early in vivo development and migration of oligodendrocytes. J Neurocytol. 1988; 17(1):43-54. DOI: 10.1007/BF01735376. View

12.

Narayanan S, Flores A, Wang F, Macklin W . Akt signals through the mammalian target of rapamycin pathway to regulate CNS myelination. J Neurosci. 2009; 29(21):6860-70. PMC: 2757755. DOI: 10.1523/JNEUROSCI.0232-09.2009. View

13.

Yang Q, Xiong J, Yao Z . Neuron-NG2 cell synapses: novel functions for regulating NG2 cell proliferation and differentiation. Biomed Res Int. 2013; 2013:402843. PMC: 3747365. DOI: 10.1155/2013/402843. View

14.

Bjartmar C, Trapp B . Axonal and neuronal degeneration in multiple sclerosis: mechanisms and functional consequences. Curr Opin Neurol. 2001; 14(3):271-8. DOI: 10.1097/00019052-200106000-00003. View

15.

Huang J, Jarjour A, Nait Oumesmar B, Kerninon C, Williams A, Krezel W . Retinoid X receptor gamma signaling accelerates CNS remyelination. Nat Neurosci. 2010; 14(1):45-53. PMC: 4013508. DOI: 10.1038/nn.2702. View

16.

Paukert M, Bergles D . Synaptic communication between neurons and NG2+ cells. Curr Opin Neurobiol. 2006; 16(5):515-21. DOI: 10.1016/j.conb.2006.08.009. View

17.

Micu I, Jiang Q, Coderre E, Ridsdale A, Zhang L, Woulfe J . NMDA receptors mediate calcium accumulation in myelin during chemical ischaemia. Nature. 2005; 439(7079):988-92. DOI: 10.1038/nature04474. View

18.

Griffiths I, Klugmann M, Anderson T, Thomson C, Vouyiouklis D, Nave K . Current concepts of PLP and its role in the nervous system. Microsc Res Tech. 1998; 41(5):344-58. DOI: 10.1002/(SICI)1097-0029(19980601)41:5<344::AID-JEMT2>3.0.CO;2-Q. View

19.

Holtzclaw L, Gallo V, Russell J . AMPA receptors shape Ca2+ responses in cortical oligodendrocyte progenitors and CG-4 cells. J Neurosci Res. 1995; 42(1):124-30. DOI: 10.1002/jnr.490420114. View

20.

Salter M, Fern R . NMDA receptors are expressed in developing oligodendrocyte processes and mediate injury. Nature. 2005; 438(7071):1167-71. DOI: 10.1038/nature04301. View