Region- and age-dependent alterations of glial-neuronal metabolic interactions correlate with CNS pathology in a mouse model of globoid cell leukodystrophy

Journal of Cerebral Blood Flow and Metabolism

Volumn 33, Issue 7, 2013, Pages 1127-1137

  Meisingset, Tore Wergeland ^a   Ricca, Alessandra ^b   Neri, Margherita ^b   Sonnewald, Ursula ^a   Gritti, Angela ^b  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^b SAN RAFFAELE SCIENTIFIC INSTITUTE   (Italy)

Author keywords

Astrocytes; MR spectroscopy; neurodegeneration; neuronal glial interactions; white matter disease; white matter oligodendrocytes

Indexed keywords

N ACETYLASPARTIC ACID; N ACETYLASPARTYLGLUTAMIC ACID;

ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; ASTROCYTOSIS; CARBON NUCLEAR MAGNETIC RESONANCE; CELL ACTIVATION; CEREBELLUM; CONTROLLED STUDY; DISEASE COURSE; FOREBRAIN; GLIA; GLOBOID CELL LEUKODYSTROPHY; GLUCOSE METABOLISM; MICROGLIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; SPINAL CORD;

AGING; AMINO ACIDS; ANIMALS; ASTROCYTES; BRAIN; CENTRAL NERVOUS SYSTEM; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DISEASE MODELS, ANIMAL; GLIOSIS; LECTINS; LEUKODYSTROPHY, GLOBOID CELL; MAGNETIC RESONANCE SPECTROSCOPY; MICE; MICE, INBRED C57BL; MICE, NEUROLOGIC MUTANTS; NEUROGLIA; NEURONS; SPINAL CORD;

EID: 84880333655     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2013.64     Document Type: Article

References (40)

1. Kobayashi T, Goto I, Yamanaka T, Suzuki Y, Nakano T, Suzuki K. Infantile and fetal globoid cell leukodystrophy: Analysis of galactosylceramide and galactosylsphingosine. Ann Neurol 1988; 24: 517-522
2. Suzuki K. Globoid cell leukodystrophy (Krabbés disease): Update. J Child Neurol 2003; 18: 595-603
3. Ballabio A, Gieselmann V. Lysosomal disorders: From storage to cellular damage. Biochim Biophys Acta 2009; 1793: 684-696
4. Strasberg P. Cerebrosides and psychosine disrupt mitochondrial functions. Biochem Cell Biol 1986; 64: 485-489
5. Santambrogio S, Ricca A, Maderna C, Ieraci A, Aureli M, Sonnino S et al. The galactocerebrosidase enzyme contributes to maintain a functional neurogenic niche during early postnatal CNS development. Hum Mol Genet 2012; 21: 4732-4750
6. Castelvetri LC, Givogri MI, Zhu H, Smith B, Lopez-Rosas A, Qiu X et al. Axonopathy is a compounding factor in the pathogenesis of Krabbe disease. Acta neuropathologica 2011; 122: 35-48
7. Nave KA, Trapp BD. Axon-glial signaling and the glial support of axon function. Annu Rev Neurosci 2008; 31: 535-561
8. Funfschilling U, Supplie LM, Mahad D, Boretius S, Saab AS, Edgar J et al. Glycolytic oligodendrocytes maintain myelin and long-term axonal integrity. Nature 2012; 485: 517-521
9. Lee Y, Morrison BM, Li Y, Lengacher S, Farah MH, Hoffman PN et al. Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature 2012; 487: 443-448
10. Robinson N, Cumings JN. Biochemical and histochemical observations on Krabbés disease. (Globoid body diffuse sclerosis). Acta neuropathologica 1967; 9: 280-289
11. Pouwels PJ, Brockmann K, Kruse B, Wilken B, Wick M, Hanefeld F et al. Regional age dependence of human brain metabolites from infancy to adulthood as detected by quantitative localized proton MRS. Pediatr Res 1999; 46: 474-485
12. Kruse B, Hanefeld F, Christen HJ, Bruhn H, Michaelis T, Hanicke W et al. Alterations of brain metabolites in metachromatic leukodystrophy as detected by localized proton magnetic resonance spectroscopy in vivo. J Neurol 1993; 241: 68-74
13. Brockmann K, Dechent P, Wilken B, Rusch O, Frahm J, Hanefeld F. Proton MRS profile of cerebral metabolic abnormalities in Krabbe disease. Neurology 2003; 60: 819-825
14. Lattanzi A, Neri M, Maderna C, di Girolamo I, Martino S, Orlacchio A et al. Widespread enzymatic correction of CNS tissues by a single intracerebral injection of therapeutic lentiviral vector in leukodystrophy mouse models. Hum Mol Genet 2010; 19: 2208-2227
15. Neri M, Ricca A, di Girolamo I, Alcalá-Franco B, Cavazzin C, Orlacchio A et al. Neural stem cell gene therapy ameliorates pathology and function in a mouse model of globoid cell leukodystrophy. Stem Cells 2011; 29: 1559-1571
16. Suzuki K. The twitcher mouse: A model for Krabbe disease and for experimental therapies. Brain Pathol 1995; 5: 249-258
17. Gritti A, Dal Molin M, Foroni C, Bonfanti L. Effects of developmental age, brain region, and time in culture on long-term proliferation and multipotency of neural stem cell populations. J Comp Neurol 2009; 517: 333-349
18. Le Belle JE, Harris NG, Williams SR, Bhakoo KK. A comparison of cell and tissue extraction techniques using high-resolution 1H-NMR spectroscopy. NMR Biomed 2002; 15: 37-44
19. Geddes JW, Wood JD. Changes in the amino-Acid content of nerve endings (synaptosomes) induced by drugs that alter the metabolism of glutamate and gamma-Aminobutyric acid. J Neurochem 1984; 42: 16-24
20. Luzi P, Abraham RM, Rafi MA, Curtis M, Hooper DC, Wenger DA. Effects of treatments on inflammatory and apoptotic markers in the CNS of mice with globoid cell leukodystrophy. Brain Res 2009; 1300: 146-158
21. Hunt D, Raivich G, Anderson PN. Activating transcription factor 3 and the nervous system. Frontiers Mol Neurosci 2012; 5: 7.
22. Galbiati F, Givogri MI, Cantuti L, Rosas AL, Cao H, van Breemen R et al. Combined hematopoietic and lentiviral gene-transfer therapies in newborn Twitcher mice reveal contemporaneous neurodegeneration and demyelination in Krabbe disease. J Neurosci Res 2009; 87: 1748-1759
23. Rafiki A, Boulland JL, Halestrap AP, Ottersen OP, Bergersen L. Highly differential expression of the monocarboxylate transporters MCT2 and MCT4 in the developing rat brain. Neuroscience 2003; 122: 677-688
24. Shank RP, Bennett GS, Freytag SO, Campbell GL. Pyruvate carboxylase: An astrocyte-specific enzyme implicated in the replenishment of amino-Acid neurotransmitter pools. Brain Res 1985; 329: 364-367
25. Slusher BS, Robinson MB, Tsai G, Simmons ML, Richards SS, Coyle JT. Rat brain N-Acetylated alpha-linked acidic dipeptidase activity. Purification and immunologic characterization. J Biol Chem 1990; 265: 21297-21301
26. Madhavarao CN, Moffett JR, Moore RA, Viola RE, Namboodiri MA, Jacobowitz DM. Immunohistochemical localization of aspartoacylase in the rat central nervous system. J Comp Neurol 2004; 472: 318-329
27. Tkac I, Rao R, Georgieff MK, Gruetter R. Developmental and regional changes in the neurochemical profile of the rat brain determined by in vivo 1H NMR spectroscopy. Magn Reson Med 2003; 50: 24-32
28. Brand A, Richter-Landsberg C, Leibfritz D, Multinuclear NMR. Studies on the energy metabolism of glial and neuronal cells. Dev Neurosci 1993; 15: 289-298
29. Bakshi R, Miletich RS, Kinkel PR, Emmet ML, Kinkel WR. High-resolution fluorodeoxyglucose positron emission tomography shows both global and regional cerebral hypometabolism in multiple sclerosis. J Neuroimag 1998; 8: 228-234
30. Bluml S, Moreno A, Hwang JH, Ross BD. 1-(13)C glucose magnetic resonance spectroscopy of pediatric and adult brain disorders. NMR Biomed 2001; 14: 19-32
31. Pouwels PJ, Kruse B, Korenke GC, Mao X, Hanefeld FA, Frahm J. Quantitative proton magnetic resonance spectroscopy of childhood adrenoleukodystrophy. Neuropediatrics 1998; 29: 254-264
32. Moffett JR, Namboodiri AM. Expression of N-Acetylaspartate and N-Acetylaspartylglutamate in the nervous system. Adv Exp Med Biol 2006; 576: 7-26
33. Francis JS, Strande L, Markov V, Leone P. Aspartoacylase supports oxidative energy metabolism during myelination. J Cereb Blood Flow Metab 2012; 32: 1725-1736
34. Wood PL, Smith T, Pelzer L, Goodenowe DB. Targeted metabolomic analyses of cellular models of Pelizaeus-Merzbacher disease reveal plasmalogen and myoinositol solute carrier dysfunction. Lipids Health Dis 2011; 10: 102
35. Meisingset TW, Risa O, Brenner M, Messing A, Sonnewald U. Alteration of glialneuronal metabolic interactions in a mouse model of Alexander disease. Glia 2010; 58: 1228-1234
36. Dominguez E, Mauborgne A, Mallet J, Desclaux M, Pohl M. SOCS3-mediated blockade of JAK/STAT3 signaling pathway reveals its major contribution to spinal cord neuroinflammation and mechanical allodynia after peripheral nerve injury. J.Neurosci 2010; 30: 5754-5766
37. Xu GY, Liu S, Hughes MG, McAdoo DJ. Glutamate-induced losses of oligodendrocytes and neurons and activation of caspase-3 in the rat spinal cord. Neuroscience 2008; 153: 1034-1047
38. Olstad E, Qu H, Sonnewald U. Glutamate is preferred over glutamine for intermediary metabolism in cultured cerebellar neurons. J Cereb Blood Flow Metab 2007; 27: 811-820
39. Korbo L, Andersen BB, Ladefoged O, Moller A. Total number of various cell types in rat cerebellar cortex estimated using an unbiased stereological method. Brain Res 1993; 609: 262-268
40. Qu H, Haberg A, Haraldseth O, Unsgard G, Sonnewald U. (13)C MR spectroscopy study of lactate as substrate for rat brain. Dev Neurosci 2000; 22: 429-436