Oligodendroglia metabolically support axons and contribute to neurodegeneration

Nature

Volumn 487, Issue 7408, 2012, Pages 443-448

  Lee, Youngjin ^a   Morrison, Brett M ^a   Li, Yun ^a   Lengacher, Sylvain ^b   Farah, Mohamed H ^a   Hoffman, Paul N ^a   Liu, Yiting ^a   Tsingalia, Akivaga ^a   Jin, Lin ^a   Zhang, Ping Wu ^a   Pellerin, Luc ^c   Magistretti, Pierre J ^b   Rothstein, Jeffrey D ^a,d  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EPFL   (Switzerland)

^c UNIVERSITY OF LAUSANNE   (Switzerland)

^d JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MONOCARBOXYLATE TRANSPORTER 1;

BIOCHEMISTRY; BRAIN; CYTOLOGY; EPIDEMIOLOGY; FUNCTIONAL ROLE; GLUCOSE; METABOLITE; NERVOUS SYSTEM DISORDER; NEUROLOGY; RODENT; SURVIVAL; TUMOR;

AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; CELL CULTURE; CELL LOSS; CELL SURVIVAL; DOWN REGULATION; IN VITRO STUDY; IN VIVO STUDY; NERVE CELL LESION; NERVE DEGENERATION; NERVE FIBER; NEUROPATHY; OLIGODENDROGLIA; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; AXONS; CELL LINE; CELL SURVIVAL; DISEASE MODELS, ANIMAL; DOWN-REGULATION; HETEROZYGOTE; HUMANS; LACTIC ACID; MICE; MICE, TRANSGENIC; MONOCARBOXYLIC ACID TRANSPORTERS; MOTOR NEURONS; MYELIN SHEATH; NERVE DEGENERATION; OLIGODENDROGLIA; PROTEIN TRANSPORT; RNA, SMALL INTERFERING; SUPEROXIDE DISMUTASE; SYMPORTERS;

ANIMALIA;

EID: 84864200035     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature11314     Document Type: Article

References (49)

1. Trapp, B. D. et al. Axonal transection in the lesions of multiple sclerosis. N. Engl. J. Med. 338, 278-285 (1998).
2. Garbern, J. Y. et al. Patients lacking the major CNS myelin protein, proteolipid protein 1, develop length-dependent axonal degeneration in the absence of demyelination and inflammation. Brain 125, 551-561 (2002).
3. Griffiths, I. et al. Axonal swellings and degeneration in mice lacking the major proteolipid of myelin. Science 280, 1610-1613 (1998).
4. Lappe-Siefke, C. et al. Disruption of Cnp1 uncouples oligodendroglial functions in axonal support and myelination. Nature Genet. 33, 366-374 (2003).
5. Fü nfschilling, U. et al. Glycolytic oligodendrocytes maintain myelin and long-term axonal integrity. Nature 485, 517-521 (2012).
6. Pierre, K. & Pellerin, L. Monocarboxylate transporters in the central nervous system: distribution, regulation and function. J. Neurochem. 94, 1-14 (2005).
7. Koehler-Stec, E. M., Simpson, I. A., Vannucci, S. J., Landschulz, K. T. & Landschulz, W. H. Monocarboxylate transporter expression inmouse brain. Am. J. Physiol. 275, E516-E524 (1998).
8. Pierre, K., Pellerin, L., Debernardi, R., Riederer, B. M. & Magistretti, P. J. Cell-specific localization of monocarboxylate transporters, MCT1 AND MCT2, in the adult mouse brain revealed by double immunohistochemical labeling and confocal microscopy. Neuroscience 100, 617-627 (2000).
9. Halestrap, A. P. & Price, N. T. The proton-linked monocarboxylate transporter (MCT) family: structure, function and regulation. Biochem. J. 343, 281-299 (1999).
10. Rinholm, J. E. et al.Regulation of oligodendrocyte development andmyelination by glucose and lactate. J. Neurosci. 31, 538-548 (2011).
11. Pellerin, L. & Magistretti, P. J. Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc. Natl Acad. Sci. USA 91, 10625-10629 (1994).
12. Walz, W. & Mukerji, S. Lactate production and release in cultured astrocytes. Neurosci. Lett. 86, 296-300 (1988).
13. Pellerin, L. et al. Evidence supporting the existence of an activity-dependent astrocyte-neuron lactate shuttle. Dev. Neurosci. 20, 291-299 (1998).
14. Berthet, C. et al. Neuroprotective role of lactate after cerebral ischemia. J. Cereb. Blood Flow Metab. 29, 1780-1789 (2009).
15. Suzuki, A. et al. Astrocyte-neuron lactate transport is required for long-term memory formation. Cell 144, 810-823 (2011).
16. Benarroch, E. E. Oligodendrocytes: susceptibility to injury and involvement in neurologic disease. Neurology 72, 1779-1785 (2009).
17. Yamanaka, K. et al. Astrocytes as determinants of disease progression in inherited amyotrophic lateral sclerosis. Nature Neurosci. 11, 251-253 (2008).
18. Kang, S. H., Fukaya, M., Yang, J. K., Rothstein, J. D. & Bergles, D. E. NG21 CNS glial progenitors remain committed to the oligodendrocyte lineage in postnatal life and following neurodegeneration. Neuron 68, 668-681 (2010).
19. Pellerin, L., Pellegri, G., Martin, J. L. & Magistretti, P. J. Expression of monocarboxylate transportermRNAs inmouse brain: support for a distinct role of lactate as an energy substrate for the neonatal vs. adult brain. Proc. Natl Acad. Sci. USA 95, 3990-3995 (1998).
20. Chiry, O. et al. Expression of the monocarboxylate transporter MCT1 in the adult human brain cortex. Brain Res. 1070, 65-70 (2006).
21. Gerhart, D. Z., Enerson, B. E., Zhdankina, O. Y., Leino, R. L.&Drewes, L. R. Expression ofmonocarboxylate transporterMCT1 by brain endotheliumand glia in adult and suckling rats. Am. J. Physiol. 273, E207-E213 (1997).
22. Regan, M. R. et al. Variations in promoter activity reveal a differential expression and physiology of glutamate transporters by glia in the developing and mature CNS. J. Neurosci. 27, 6607-6619 (2007).
23. Zhou, Q., Wang, S. & Anderson, D. J. Identification of a novel family of oligodendrocyte lineage-specific basic helix-loop-helix transcription factors. Neuron 25, 331-343 (2000).
24. Hanu, R.,McKenna, M., O'Neill, A., Resneck, W. G.&Bloch, R. J.Monocarboxylic acid transporters, MCT1 AND MCT2, in cortical astrocytes in vitro and in vivo. Am. J. Physiol. Cell Physiol. 278, C921-C930 (2000).
25. Pellerin, L., Bergersen, L. H., Halestrap, A. P. & Pierre, K. Cellular and subcellular distribution of monocarboxylate transporters in cultured brain cells and in the adult brain. J. Neurosci. Res. 79, 55-64 (2005).
26. Bergersen, L., Rafiki, A. & Ottersen, O. P. Immunogold cytochemistry identifies specialized membrane domains for monocarboxylate transport in the central nervous system. Neurochem. Res. 27, 89-96 (2002).
27. Murray, C. M. et al. Monocarboxylate transporter MCT1 is a target for immunosuppression. Nature Chem. Biol. 1, 371-376 (2005).
28. Suh, S. W. et al. Astrocyte glycogen sustains neuronal activity during hypoglycemia: studies with the glycogen phosphorylase inhibitor CP-316,819 (R-R*,S*-5-chloro-N-2-hydroxy-3-(methoxymethylamino) -3-oxo-1-(phenylmet hyl)propyl-1H-indole-2-carboxamide). J. Pharmacol. Exp. Ther. 321, 45-50 (2007).
29. Heyer, E. J., Nowak, L. M. & Macdonald, R. L. Membrane depolarization and prolongation of calcium-dependent action potentials of mouse neurons in cell culture by two convulsants: bicuculline and penicillin. Brain Res. 232, 41-56 (1982).
30. Mayer, M. L. & Westbrook, G. L. Mixed-agonist action of excitatory amino acids on mouse spinal cord neurones under voltage clamp. J. Physiol. (Lond.) 354, 29-53 (1984).
31. Edgar, J. M. et al. Early ultrastructural defects of axons and axon-glia junctions in mice lacking expression of Cnp1. Glia 57, 1815-1824 (2009).
32. Morrison, B. M., Shu, I. W., Wilcox, A. L., Gordon, J. W. & Morrison, J. H. Early and selective pathology of light chain neurofilament in the spinal cord and sciatic nerve of G86R mutant superoxide dismutase transgenic mice. Exp. Neurol. 165, 207-220 (2000).
33. Sasaki, S. & Maruyama, S. Increase in diameter of the axonal initial segment is an early change in amyotrophic lateral sclerosis. J. Neurol. Sci. 110, 114-120 (1992).
34. Tekkök, 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. 81, 644-652 (2005).
35. Ventura, A. et al. Cre-lox-regulated conditional RNA interference fromtransgenes. Proc. Natl Acad. Sci. USA 101, 10380-10385 (2004).
36. Doerflinger, N. H., Macklin, W. B. & Popko, B. Inducible site-specific recombination in myelinating cells. Genesis 35, 63-72 (2003).
37. Kirk, P. et al.CD147 is tightly associated with lactate transportersMCT1 andMCT4 and facilitates their cell surface expression. EMBO J. 19, 3896-3904 (2000).
38. Sánchez-Abarca, L. I., Tabernero, A. & Medina, J. M. Oligodendrocytes use lactate as a source of energy and as a precursor of lipids. Glia 36, 321-329 (2001).
39. Rinholm, J. E. et al.Regulation of oligodendrocyte development andmyelination by glucose and lactate. J. Neurosci. 31, 538-548 (2011).
40. Seilhean, D. et al. Accumulation of TDP-43 and a-actin in an amyotrophic lateral sclerosis patient with the K17I ANG mutation. Acta Neuropathol. 118, 561-573 (2009).
41. Brenner, M., Kisseberth, W. C., Su, Y., Besnard, F. & Messing, A. GFAP promoter directs astrocyte-specific expression in transgenic mice. J. Neurosci. 14, 1030-1037 (1994).
42. Yang, Y. et al. Molecular comparison of GLT11 AND ALDH1L11 astrocytes in vivo in astroglial reporter mice. Glia 59, 200-207 (2011).
43. Doyle, J. P. et al. Application of a translational profiling approach for the comparative analysis of CNS cell types. Cell 135, 749-762 (2008).
44. Buntinx, M. et al. Characterization of three human oligodendroglial cell lines as a model to study oligodendrocyte injury: morphology and oligodendrocytespecific gene expression. J. Neurocytol. 32, 25-38 (2003).
45. You, F., Osawa, Y., Hayashi, S. & Nakashima, S. Immediate early gene IEX-1 induces astrocytic differentiation of U87-MG human glioma cells. J. Cell. Biochem. 100, 256-265 (2007).
46. Maekawa, F., Minehira, K., Kadomatsu, K. & Pellerin, L. Basal and stimulated lactate fluxes in primary cultures of astrocytes are differentially controlled by distinct proteins. J. Neurochem. 107, 789-798 (2008).
47. Rothstein, J. D., Jin, L., Dykes-Hoberg, M. & Kuncl, R. W. Chronic inhibition of glutamate uptake produces a model of slow neurotoxicity. Proc. Natl Acad. Sci. USA 90, 6591-6595 (1993).
48. McIver, S. R. et al. Lentiviral transduction of murine oligodendrocytes in vivo. J. Neurosci. Res. 82, 397-403 (2005).
49. Yang, Y., Gozen, O., Vidensky, S., Robinson, M. B. & Rothstein, J. D. Epigenetic regulation of neuron-dependent induction of astroglial synaptic protein GLT1. Glia 58, 277-286 (2010).