The role of myelin and oligodendrocytes in axonal energy metabolism

Current Opinion in Neurobiology

Volumn 23, Issue 6, 2013, Pages 1065-1072

  Saab, Aiman S ^a   Tzvetanova, Iva D ^a   Nave, Klaus Armin ^a  

^a MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; GLUCOSE; LACTIC ACID; MONOCARBOXYLATE TRANSPORTER 1; MYELIN;

AMYOTROPHIC LATERAL SCLEROSIS; CELL ACTIVITY; DEGENERATIVE DISEASE; DEMYELINATING DISEASE; ENERGY METABOLISM; GLIA CELL; GLYCOLYSIS; HUMAN; LEUKODYSTROPHY; MULTIPLE SCLEROSIS; MYELINATION; NERVE FIBER; NERVE POTENTIAL; NEUROTRANSMISSION; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW;

ANIMALS; AXONS; ENERGY METABOLISM; HUMANS; MYELIN SHEATH; OLIGODENDROGLIA;

EID: 84887404159     PISSN: 09594388     EISSN: 18736882     Source Type: Journal    
DOI: 10.1016/j.conb.2013.09.008     Document Type: Review

References (62)

1. Nave K.A., Trapp B.D. Axon-glial signaling and the glial support of axon function. Annu Rev Neurosci 2008, 31:535-561.
2. Takahashi N., Sakurai T., Davis K.L., Buxbaum J.D. Linking oligodendrocyte and myelin dysfunction to neurocircuitry abnormalities in schizophrenia. Prog Neurobiol 2011, 93:13-24.
3. Gold B.T., Johnson N.F., Powell D.K., Smith C.D. White matter integrity and vulnerability to Alzheimer's disease: preliminary findings and future directions. Biochim Biophys Acta 2012, 1822:416-422.
4. Griffiths I., Klugmann M., Anderson T., Yool D., Thomson C., Schwab M.H., Schneider A., Zimmermann F., McCulloch M., Nadon N., Nave K.A. Axonal swellings and degeneration in mice lacking the major proteolipid of myelin. Science 1998, 280:1610-1613.
5. Lappe-Siefke C., Goebbels S., Gravel M., Nicksch E., Lee J., Braun P.E., Griffiths I.R., Nave K.A. Disruption of Cnp1 uncouples oligodendroglial functions in axonal support and myelination. Nat Genet 2003, 33:366-374.
6. Fünfschilling U., Supplie L.M., Mahad D., Boretius S., Saab A.S., Edgar J., Brinkmann B.G., Kassmann C.M., Tzvetanova I.D., Mobius W., et al. Glycolytic oligodendrocytes maintain myelin and long-term axonal integrity. Nature 2012, 485:517-521.
7. Lee Y., Morrison B.M., Li Y., Lengacher S., Farah M.H., Hoffman P.N., Liu Y., Tsingalia A., Jin L., Zhang P.W., et al. Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature 2012, 487:443-448.
8. Nave K.A. Myelination and support of axonal integrity by glia. Nature 2010, 468:244-252.
9. Tress O., Maglione M., May D., Pivneva T., Richter N., Seyfarth J., Binder S., Zlomuzica A., Seifert G., Theis M., et al. Panglial gap junctional communication is essential for maintenance of myelin in the CNS. J Neurosci 2012, 32:7499-7518.
10. Menichella D.M., Majdan M., Awatramani R., Goodenough D.A., Sirkowski E., Scherer S.S., Paul D.L. Genetic and physiological evidence that oligodendrocyte gap junctions contribute to spatial buffering of potassium released during neuronal activity. J Neurosci 2006, 26:10984-10991.
11. Rash J.E. Molecular disruptions of the panglial syncytium block potassium siphoning and axonal saltatory conduction: pertinence to neuromyelitis optica and other demyelinating diseases of the central nervous system. Neuroscience 2010, 168:982-1008.
12. Harris J.J., Attwell D. The energetics of CNS white matter. J Neurosci 2012, 32:356-371.
13. Nave K.A. Myelination and the trophic support of long axons. Nat Rev Neurosci 2010, 11:275-283.
14. David G., Barrett J.N., Barrett E.F. Activation of internodal potassium conductance in rat myelinated axons. J Physiol 1993, 472:177-202.
15. Young E.A., Fowler C.D., Kidd G.J., Chang A., Rudick R., Fisher E., Trapp B.D. Imaging correlates of decreased axonal Na+/K+ ATPase in chronic multiple sclerosis lesions. Ann Neurol 2008, 63:428-435.
16. Ohno N., Kidd G.J., Mahad D., Kiryu-Seo S., Avishai A., Komuro H., Trapp B.D. Myelination and axonal electrical activity modulate the distribution and motility of mitochondria at CNS nodes of Ranvier. J Neurosci 2011, 31:7249-7258.
17. Zala D., Hinckelmann M.V., Yu H., Lyra da Cunha M.M., Liot G., Cordelieres F.P., Marco S., Saudou F. Vesicular glycolysis provides on-board energy for fast axonal transport. Cell 2013, 152:479-491.
18. Brown A.M., Wender R., Ransom B.R. Metabolic substrates other than glucose support axon function in central white matter. J Neurosci Res 2001, 66:839-843.
19. Tekkok S.B., Brown A.M., Westenbroek R., Pellerin L., Ransom B.R. Transfer of glycogen-derived lactate from astrocytes to axons via specific monocarboxylate transporters supports mouse optic nerve activity. J Neurosci Res 2005, 81:644-652.
20. Wyss M.T., Jolivet R., Buck A., Magistretti P.J., Weber B. In vivo evidence for lactate as a neuronal energy source. J Neurosci 2011, 31:7477-7485.
21. Wender R., Brown A.M., Fern R., Swanson R.A., Farrell K., Ransom B.R. Astrocytic glycogen influences axon function and survival during glucose deprivation in central white matter. J Neurosci 2000, 20:6804-6810.
22. Brown A.M., Baltan T.S., Ransom B.R. Energy transfer from astrocytes to axons: the role of CNS glycogen. Neurochem Int 2004, 45:529-536.
23. Pellerin L., Magistretti P.J. Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc Natl Acad Sci U S A 1994, 91:10625-10629.
24. Kasischke K.A., Vishwasrao H.D., Fisher P.J., Zipfel W.R., Webb W.W. Neural activity triggers neuronal oxidative metabolism followed by astrocytic glycolysis. Science 2004, 305:99-103.
25. Magistretti P.J. Neuron-glia metabolic coupling and plasticity. J Exp Biol 2006, 209:2304-2311.
26. Suzuki A., Stern S.A., Bozdagi O., Huntley G.W., Walker R.H., Magistretti P.J., Alberini C.M. Astrocyte-neuron lactate transport is required for long-term memory formation. Cell 2011, 144:810-823.
27. Kimelberg H.K. The role of hypotheses in current research, illustrated by hypotheses on the possible role of astrocytes in energy metabolism and cerebral blood flow: from Newton to now. J Cereb Blood Flow Metab 2004, 24:1235-1239.
28. Dienel G.A. Astrocytic energetics during excitatory neurotransmission: what are contributions of glutamate oxidation and glycolysis?. Neurochem Int 2013, 63:244-258.
29. Almeida A., Almeida J., Bolanos J.P., Moncada S. Different responses of astrocytes and neurons to nitric oxide: the role of glycolytically generated ATP in astrocyte protection. Proc Natl Acad Sci U S A 2001, 98:15294-15299.
30. Herrero-Mendez A., Almeida A., Fernandez E., Maestre C., Moncada S., Bolanos J.P. The bioenergetic and antioxidant status of neurons is controlled by continuous degradation of a key glycolytic enzyme by APC/C-Cdh1. Nat Cell Biol 2009, 11:747-752.
31. Klugmann M., Schwab M.H., Puhlhofer A., Schneider A., Zimmermann F., Griffiths I.R., Nave K.A. Assembly of CNS myelin in the absence of proteolipid protein. Neuron 1997, 18:59-70.
32. Edgar J.M., McLaughlin M., Werner H.B., McCulloch M.C., Barrie J.A., Brown A., Faichney A.B., Snaidero N., Nave K.A., Griffiths I.R. Early ultrastructural defects of axons and axon-glia junctions in mice lacking expression of Cnp1. Glia 2009, 57:1815-1824.
33. Ferguson B., Matyszak M.K., Esiri M.M., Perry V.H. Axonal damage in acute multiple sclerosis lesions. Brain 1997, 120(Pt 3):393-399.
34. Trapp B.D., Peterson J., Ransohoff R.M., Rudick R., Mork S., Bo L. Axonal transection in the lesions of multiple sclerosis. N Engl J Med 1998, 338:278-285.
35. Trapp B.D., Nave K.A. Multiple sclerosis: an immune or neurodegenerative disorder?. Annu Rev Neurosci 2008, 31:247-269.
36. Edgar J.M., McLaughlin M., Yool D., Zhang S.C., Fowler J.H., Montague P., Barrie J.A., McCulloch M.C., Duncan I.D., Garbern J., Nave K.A., Griffiths I.R. Oligodendroglial modulation of fast axonal transport in a mouse model of hereditary spastic paraplegia. J Cell Biol 2004, 166:121-131.
37. Ferreirinha F., Quattrini A., Pirozzi M., Valsecchi V., Dina G., Broccoli V., Auricchio A., Piemonte F., Tozzi G., Gaeta L., et al. Axonal degeneration in paraplegin-deficient mice is associated with abnormal mitochondria and impairment of axonal transport. J Clin Invest 2004, 113:231-242.
38. Tarrade A., Fassier C., Courageot S., Charvin D., Vitte J., Peris L., Thorel A., Mouisel E., Fonknechten N., Roblot N., et al. A mutation of spastin is responsible for swellings and impairment of transport in a region of axon characterized by changes in microtubule composition. Hum Mol Genet 2006, 15:3544-3558.
39. Werner H.B., Kuhlmann K., Shen S., Uecker M., Schardt A., Dimova K., Orfaniotou F., Dhaunchak A., Brinkmann B.G., Mobius W., et al. Proteolipid protein is required for transport of sirtuin 2 into CNS myelin. J Neurosci 2007, 27:7717-7730.
40. Rinholm J.E., Hamilton N.B., Kessaris N., Richardson W.D., Bergersen L.H., Attwell D. Regulation of oligodendrocyte development and myelination by glucose and lactate. J Neurosci 2011, 31:538-548.
41. Diaz F., Thomas C.K., Garcia S., Hernandez D., Moraes C.T. Mice lacking COX10 in skeletal muscle recapitulate the phenotype of progressive mitochondrial myopathies associated with cytochrome c oxidase deficiency. Hum Mol Genet 2005, 14:2737-2748.
42. Wang Y.Z., Xu T.L. Acidosis, acid-sensing ion channels, and neuronal cell death. Mol Neurobiol 2011, 44:350-358.
43. Debernardi R., Pierre K., Lengacher S., Magistretti P.J., Pellerin L. Cell-specific expression pattern of monocarboxylate transporters in astrocytes and neurons observed in different mouse brain cortical cell cultures. J Neurosci Res 2003, 73:141-155.
44. Butt A.M., Jenkins H.G. Morphological changes in oligodendrocytes in the intact mouse optic nerve following intravitreal injection of tumour necrosis factor. J Neuroimmunol 1994, 51:27-33.
45. Nikic I., Merkler D., Sorbara C., Brinkoetter M., Kreutzfeldt M., Bareyre F.M., Bruck W., Bishop D., Misgeld T., Kerschensteiner M. A reversible form of axon damage in experimental autoimmune encephalomyelitis and multiple sclerosis. Nat Med 2011, 17:495-499.
46. Nagan N., Zoeller R.A. Plasmalogens: biosynthesis and functions. Prog Lipid Res 2001, 40:199-229.
47. Braverman N.E., Moser A.B. Functions of plasmalogen lipids in health and disease. Biochim Biophys Acta 2012, 1822:1442-1452.
48. Edgar J.M., McCulloch M.C., Montague P., Brown A.M., Thilemann S., Pratola L., Gruenenfelder F.I., Griffiths I.R., Nave K.A. Demyelination and axonal preservation in a transgenic mouse model of Pelizaeus-Merzbacher disease. EMBO Mol Med 2010, 2:42-50.
49. Ip C.W., Kroner A., Groh J., Huber M., Klein D., Spahn I., Diem R., Williams S.K., Nave K.A., Edgar J.M., Martini R. Neuroinflammation by cytotoxic T-lymphocytes impairs retrograde axonal transport in an oligodendrocyte mutant mouse. PLoS One 2012, 7:e42554.
50. Ghosh A., Manrique-Hoyos N., Voigt A., Schulz J.B., Kreutzfeldt M., Merkler D., Simons M. Targeted ablation of oligodendrocytes triggers axonal damage. PLoS One 2011, 6:e22735.
51. Pohl H.B., Porcheri C., Mueggler T., Bachmann L.C., Martino G., Riethmacher D., Franklin R.J., Rudin M., Suter U. Genetically induced adult oligodendrocyte cell death is associated with poor myelin clearance, reduced remyelination, and axonal damage. J Neurosci 2011, 31:1069-1080.
52. Oluich L.J., Stratton J.A., Xing Y.L., Ng S.W., Cate H.S., Sah P., Windels F., Kilpatrick T.J., Merson T.D. Targeted ablation of oligodendrocytes induces axonal pathology independent of overt demyelination. J Neurosci 2012, 32:8317-8330.
53. Locatelli G., Wortge S., Buch T., Ingold B., Frommer F., Sobottka B., Kruger M., Karram K., Buhlmann C., Bechmann I., et al. Primary oligodendrocyte death does not elicit anti-CNS immunity. Nat Neurosci 2012, 15:543-550.
54. Traka M., Arasi K., Avila R.L., Podojil J.R., Christakos A., Miller S.D., Soliven B., Popko B. A genetic mouse model of adult-onset, pervasive central nervous system demyelination with robust remyelination. Brain 2010, 133:3017-3029.
55. Viader A., Golden J.P., Baloh R.H., Schmidt R.E., Hunter D.A., Milbrandt J. Schwann cell mitochondrial metabolism supports long-term axonal survival and peripheral nerve function. J Neurosci 2011, 31:10128-10140.
56. Viader A., Sasaki Y., Kim S., Strickland A., Workman C.S., Yang K., Gross R.W., Milbrandt J. Aberrant Schwann cell lipid metabolism linked to mitochondrial deficits leads to axon degeneration and neuropathy. Neuron 2013, 77:886-898.
57. Nave K.A., Sereda M.W., Ehrenreich H. Mechanisms of disease: inherited demyelinating neuropathies-from basic to clinical research. Nat Clin Pract Neurol 2007, 3:453-464.
58. Zenker J., Ziegler D., Chrast R. Novel pathogenic pathways in diabetic neuropathy. Trends Neurosci 2013, 36:439-449.
59. Kang S.H., Li Y., Fukaya M., Lorenzini I., Cleveland D.W., Ostrow L.W., Rothstein J.D., Bergles D.E. Degeneration and impaired regeneration of gray matter oligodendrocytes in amyotrophic lateral sclerosis. Nat Neurosci 2013, 16:571-579.
60. Philips T., Bento-Abreu A., Nonneman A., Haeck W., Staats K., Geelen V., Hersmus N., Kusters B., Van Den Bosch L., Van D.P., Richardson W.D., Robberecht W. Oligodendrocyte dysfunction in the pathogenesis of amyotrophic lateral sclerosis. Brain 2013, 136:471-482.
61. Bartzokis G. Age-related myelin breakdown: a developmental model of cognitive decline and Alzheimer's disease. Neurobiol Aging 2004, 25:5-18.
62. Takahashi N., Sakurai T. Roles of glial cells in schizophrenia: possible targets for therapeutic approaches. Neurobiol Dis 2013, 53:49-60.