Localisation of N-acetylaspartate in oligodendrocytes/myelin

详细信息    查看全文

• 作者：Kaja Nordengen (1)
  Christoph Heuser (1) (2)
  Johanne Egge Rinholm (1) (3)
  Reuben Matalon (4)
  Vidar Gundersen (1) (5)
  
  1. Department of Anatomy ; Institute of Basic Medical Sciences ; University of Oslo ; PO Box 1105 ; 0317 ; Oslo ; Norway
  2. Institute of Molecular Medicine and Experimental Immunology ; Rheinische Friedrich Wilhelms University ; Bonn ; Germany
  3. Janelia Farm Research Campus ; Howard Hughes Medical Institute ; Ashburn ; USA
  4. Department of Pediatrics ; University of Texas Medical Branch ; Galveston ; USA
  5. Department of Neurology ; Oslo University Hospital ; Rikshospitalet ; Oslo ; Norway
  
• 关键词：Cerebellum ; Immunogold ; leukodystrophy ; Canavan disease ; Glutamate ; Aspartate
• 刊名：Brain Structure and Function
• 出版年：2015
• 出版时间：March 2015
• 年：2015
• 卷：220
• 期：2
• 页码：899-917
• 全文大小：18,108 KB
• 参考文献：1. Adachi, M, Torii, J, Schneck, L, Volk, BW (1972) Electron microscopic and enzyme histochemical studies of the cerebellum in spongy degeneration (van Bogaert and Bertrans type). Acta Neuropathol 20: pp. 22-31 CrossRef
  2. Ariyannur, PS, Moffett, JR, Manickam, P, Pattabiraman, N, Arun, P, Nitta, A (2010) Methamphetamine-induced neuronal protein NAT8L is the NAA biosynthetic enzyme: implications for specialized acetyl coenzyme A metabolism in the CNS. Brain Res 1335: pp. 1-13 CrossRef
  3. Arnold, DL, Stefano, N, Matthews, PM, Trapp, BD (2001) N-acetylaspartate: usefulness as an indicator of viable neuronal tissue. Ann Neurol 50: pp. 823-825 CrossRef
  4. Arun P, Moffett JR, Namboodiri AM (2009) Evidence for mitochondrial and cytoplasmic N-acetylaspartate synthesis in SH-SY5Y neuroblastoma cells. Neurochem Int 55:219鈥?25
  5. Baslow, MH (2003) Brain N-acetylaspartate as a molecular water pump and its role in the etiology of Canavan disease: a mechanistic explanation. J Mol Neurosci 21: pp. 185-190 5/JMN:21:3:185" target="_blank" title="It opens in new window">CrossRef
  6. Bergersen, LH, Storm-Mathisen, J, Gundersen, V (2008) Immunogold quantification of amino acids and proteins in complex subcellular compartments. Nat Protoc 3: pp. 144-152 525" target="_blank" title="It opens in new window">CrossRef
  7. Bhakoo, KK, Pearce, D (2000) In vitro expression of N-acetyl aspartate by oligodendrocytes: implications for proton magnetic resonance spectroscopy signal in vivo. J Neurochem 74: pp. 254-262 59.2000.0740254.x" target="_blank" title="It opens in new window">CrossRef
  8. Boltshauser, E, Schmitt, B, Wevers, RA, Engelke, U, Burlina, AB, Burlina, AP (2004) Follow-up of a child with hypoacetylaspartia. Neuropediatrics 35: pp. 255-258 55/s-2004-821036" target="_blank" title="It opens in new window">CrossRef
  9. Burlina, AP, Ferrari, V, Divry, P, Gradowska, W, Jakobs, C, Bennett, MJ (1999) N-acetylaspartylglutamate in Canavan disease: an adverse effector?. Eur J Pediatr 158: pp. 406-409 51102" target="_blank" title="It opens in new window">CrossRef
  10. Burri, R, Steffen, C, Herschkowitz, N (1991) N-acetyl-l-aspartate is a major source of acetyl groups for lipid synthesis during rat brain development. Dev Neurosci 13: pp. 403-411 59/000112191" target="_blank" title="It opens in new window">CrossRef
  11. Canavan, MM (1931) Schilder鈥檚 encephalitis periaxialis diffusa鈥攔eport or a case in a child aged sixteen and one-half months. Arch Neurol Psychiatry 25: pp. 299-308 5005" target="_blank" title="It opens in new window">CrossRef
  12. Chakraborty, G, Ledeen, R (2003) Fatty acid synthesizing enzymes intrinsic to myelin. Brain Res Mol Brain Res 112: pp. 46-52 CrossRef
  13. Chakraborty, G, Mekala, P, Yahya, D, Wu, G, Ledeen, RW (2001) Intraneuronal N-acetylaspartate supplies acetyl groups for myelin lipid synthesis: evidence for myelin-associated aspartoacylase. J Neurochem 78: pp. 736-745 59.2001.00456.x" target="_blank" title="It opens in new window">CrossRef
  14. De SA, Yu LM (2006) Preparation of organotypic hippocampal slice cultures: interface method. Nat Protoc 1:1439鈥?445
  15. Stefano, N, Matthews, PM, Antel, JP, Preul, M, Francis, G, Arnold, DL (1995) Chemical pathology of acute demyelinating lesions and its correlation with disability. Ann Neurol 38: pp. 901-909 CrossRef
  16. Einstein, O, Friedman-Levi, Y, Grigoriadis, N, Ben-Hur, T (2009) Transplanted neural precursors enhance host brain-derived myelin regeneration. J Neurosci 29: pp. 15694-15702 523/JNEUROSCI.3364-09.2009" target="_blank" title="It opens in new window">CrossRef
  17. Gotoh, M, Davies, SE, Obrenovitch, TP (1997) Brain tissue acidosis: effects on the extracellular concentration of N-acetylaspartate. J Neurochem 69: pp. 655-661 59.1997.69020655.x" target="_blank" title="It opens in new window">CrossRef
  18. Gundersen, V, Chaudhry, FA, Bjaalie, JG, Fonnum, F, Ottersen, OP, Storm-Mathisen, J (1998) Synaptic vesicular localisation and exocytosis of l-aspartate in excitatory nerve terminals: a quantitative immunogold analysis in rat hippocampus. J Neurosci 18: pp. 6059-6070
  19. Janson, CG, McPhee, SW, Francis, J, Shera, D, Assadi, M, Freese, A (2006) Natural history of Canavan disease revealed by proton magnetic resonance spectroscopy (1H-MRS) and diffusion-weighted MRI. Neuropediatrics 37: pp. 209-221 55/s-2006-924734" target="_blank" title="It opens in new window">CrossRef
  20. Kamada, K, Takeuchi, F, Houkin, K, Kitagawa, M, Kuriki, S, Ogata, A (2001) Reversible brain dysfunction in MELAS: MEG, and (1)H MRS analysis. J Neurol Neurosurg Psychiatry 70: pp. 675-678 5.675" target="_blank" title="It opens in new window">CrossRef
  21. Karadottir, R, Cavelier, P, Bergersen, LH, Attwell, D (2005) NMDA receptors are expressed in oligodendrocytes and activated in ischaemia. Nature 438: pp. 1162-1166 CrossRef
  22. Kaul, R, Casanova, J, Johnson, AB, Tang, P, Matalon, R (1991) Purification, characterization, and localisation of aspartoacylase from bovine brain. J Neurochem 56: pp. 129-135 59.1991.tb02571.x" target="_blank" title="It opens in new window">CrossRef
  23. Kaul, R, Gao, GP, Balamurugan, K, Matalon, R (1993) Cloning of the human aspartoacylase cDNA and a common missense mutation in Canavan disease. Nat Genet 5: pp. 118-123 CrossRef
  24. Klugmann, M, Symes, CW, Klaussner, BK, Leichtlein, CB, Serikawa, T, Young, D (2003) Identification and distribution of aspartoacylase in the postnatal rat brain. Neuroreport 14: pp. 1837-1840 56-200310060-00016" target="_blank" title="It opens in new window">CrossRef
  25. Kolodziejczyk, K, Hamilton, NB, Wade, A, Karadottir, R, Attwell, D (2009) The effect of N-acetyl-aspartyl-glutamate and N-acetyl-aspartate on white matter oligodendrocytes. Brain 132: pp. 1496-1508 CrossRef
  26. Lee Y, Morrison BM, Li Y, Lengacher S, Farah MH, Hoffman PN et al (2012)聽 Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature 487:443鈥?48
  27. Ledeen RW, Golly F, Haley JE (1992) Axon-myelin transfer of phospholipids and phospholipid precursors. Labeling of myelin phosphoinositides through axonal transport. Mol Neurobiol 6:179鈥?90
  28. Long PM, Moffett JR, Namboodiri AM, Viapiano MS, Lawler SE, Jaworski DM (2013) N-acetylaspartate (NAA) and N-acetylaspartylglutamate (NAAG) promote growth and inhibit differentiation of glioma stem-like cells. J Biol Chem 288:26188鈥?6200
  29. Madhavarao CN, Chinopoulos C, Chandrasekaran K, Namboodiri MA (2003) Characterization of the N-acetylaspartate biosynthetic enzyme from rat brain. J Neurochem 86:824鈥?35
  30. Madhavarao, CN, Moffett, JR, Moore, RA, Viola, RE, Namboodiri, MA, Jacobowitz, DM (2004) Immunohistochemical localisation of aspartoacylase in the rat central nervous system. J Comp Neurol 472: pp. 318-329 CrossRef
  31. Madhavarao, CN, Arun, P, Moffett, JR, Szucs, S, Surendran, S, Matalon, R (2005) Defective N-acetylaspartate catabolism reduces brain acetate levels and myelin lipid synthesis in Canavan鈥檚 disease. Proc Natl Acad Sci USA 102: pp. 5221-5226 CrossRef
  32. Mahloudji, M, Daneshbod, K, Karjoo, M (1970) Familial spongy degeneration of the brain. Arch Neurol 22: pp. 294-298 CrossRef
  33. Martin, E, Capone, A, Schneider, J, Hennig, J, Thiel, T (2001) Absence of N-acetylaspartate in the human brain: impact on neurospectroscopy?. Ann Neurol 49: pp. 518-521 CrossRef
  34. Matalon, R, Rady, PL, Platt, KA, Skinner, HB, Quast, MJ, Campbell, GA (2000) Knock-out mouse for Canavan disease: a model for gene transfer to the central nervous system. J Gene Med 2: pp. 165-175 521-2254(200005/06)2:3<165::AID-JGM107>3.0.CO;2-R" target="_blank" title="It opens in new window">CrossRef
  35. Mathiisen TM, Lehre KP, Danbolt NC, Ottersen OP (2010) The perivascular astroglial sheath provides a complete covering of the brain microvessels: an electron microscopic 3D reconstruction. Glia 58:1094鈥?103
  36. Mattan, NS, Ghiani, CA, Lloyd, M, Matalon, R, Bok, D, Casaccia, P (2010) Aspartoacylase deficiency affects early postnatal development of oligodendrocytes and myelination. Neurobiol Dis 40: pp. 432-443 CrossRef
  37. Mehta, V, Namboodiri, MA (1995) N-acetylaspartate as an acetyl source in the nervous system. Brain Res Mol Brain Res 31: pp. 151-157 5)00044-S" target="_blank" title="It opens in new window">CrossRef
  38. Mersmann, N, Tkachev, D, Jelinek, R, Roth, PT, Mobius, W, Ruhwedel, T (2011) Aspartoacylase-lacZ knockin mice: an engineered model of Canavan disease. PLoS One 6: pp. e20336 CrossRef
  39. Moffett, JR, Namboodiri, MA (1995) Differential distribution of N-acetylaspartylglutamate and N-acetylaspartate immunoreactivities in rat forebrain. J Neurocytol 24: pp. 409-433 CrossRef
  40. Moffett, JR, Namboodiri, AM (2006) Expression of N-acetylaspartate and N-acetylaspartylglutamate in the nervous system. Adv Exp Med Biol 576: pp. 7-26 CrossRef
  41. Moffett, JR, Namboodiri, MA, Cangro, CB, Neale, JH (1991) Immunohistochemical localisation of N-acetylaspartate in rat brain. Neuroreport 2: pp. 131-134 56-199103000-00005" target="_blank" title="It opens in new window">CrossRef
  42. Moffett, JR, Namboodiri, MA, Neale, JH (1993) Enhanced carbodiimide fixation for immunohistochemistry: application to the comparative distributions of N-acetylaspartylglutamate and N-acetylaspartate immunoreactivities in rat brain. J Histochem Cytochem 41: pp. 559-570 50195" target="_blank" title="It opens in new window">CrossRef
  43. Moffett, JR, Arun, P, Ariyannur, PS, Garbern, JY, Jacobowitz, DM, Namboodiri, AM (2011) Extensive aspartoacylase expression in the rat central nervous system. Glia 59: pp. 1414-1434 CrossRef
  44. Namboodiri, AM, Moffett, JR, Arun, P, Mathew, R, Namboodiri, S, Potti, A (2006) Defective myelin lipid synthesis as a pathogenic mechanism of Canavan disease. Adv Exp Med Biol 576: pp. 145-163 CrossRef
  45. Narayana, PA, Doyle, TJ, Lai, D, Wolinsky, JS (1998) Serial proton magnetic resonance spectroscopic imaging, contrast-enhanced magnetic resonance imaging, and quantitative lesion volumetry in multiple sclerosis. Ann Neurol 43: pp. 56-571 CrossRef
  46. Ormel L, Stensrud MJ, Bergersen LH, Gundersen V (2012a)聽 VGLUT1 is localized in astrocytic processes in several brain regions. Glia 60:229鈥?38
  47. Ormel L, Stensrud MJ, Chaudhry FA, Gundersen V (2012b) A distinct set of synaptic-like microvesicles in atroglial cells contain VGLUT3. Glia 60:1289鈥?300
  48. Ottersen, OP, Storm-Mathisen, J (1984) Glutamate- and GABA-containing neurons in the mouse and rat brain, as demonstrated with a new immunocytochemical technique. J Comp Neurol 229: pp. 374-392 CrossRef
  49. Patel TB, Clark JB (1979) Synthesis of N-acetyl-L-aspartate by rat brain mitochondria and its involvement in mitochondrial/cytosolic carbon transport. Biochem J 184:539鈥?46
  50. Reichelt, KL, Fonnum, F (1969) Subcellular localisation of N-acetyl-aspartyl-glutamate, N-acetyl-glutamate and glutathione in brain. J Neurochem 16: pp. 1409-1416 59.1969.tb05993.x" target="_blank" title="It opens in new window">CrossRef
  51. Rinholm, JE, Bergersen, LH (2012) Neuroscience: the wrap that feeds neurons. Nature 487: pp. 435-436 5a" target="_blank" title="It opens in new window">CrossRef
  52. Rinholm, JE, Hamilton, NB, Kessaris, N, Richardson, WD, Bergersen, LH, Attwell, D (2011) Regulation of oligodendrocyte development and myelination by glucose and lactate. J Neurosci 31: pp. 538-548 523/JNEUROSCI.3516-10.2011" target="_blank" title="It opens in new window">CrossRef
  53. Schuff, N, Ezekiel, F, Gamst, AC, Amend, DL, Capizzano, AA, Maudsley, AA (2001) Region and tissue differences of metabolites in normally aged brain using multislice 1H magnetic resonance spectroscopic imaging. Magn Reson Med 45: pp. 899-907 CrossRef
  54. Simmons, ML, Frondoza, CG, Coyle, JT (1991) Immunocytochemical localisation of N-acetyl-aspartate with monoclonal antibodies. Neuroscience 45: pp. 37-45 522(91)90101-S" target="_blank" title="It opens in new window">CrossRef
  55. Soher, BJ, Zijl, PC, Duyn, JH, Barker, PB (1996) Quantitative proton MR spectroscopic imaging of the human brain. Magn Reson Med 35: pp. 356-363 50313" target="_blank" title="It opens in new window">CrossRef
  56. Sparrow N, Manetti ME, Bott M, Fabianac T, Petrilli A, Bates ML et al (2012) The actin-severing protein cofilin is downstream of neuregulin signaling and is essential for Schwann cell myelination. J Neurosci 32:5284鈥?297
  57. Surendran, S, Matalon, KM, Tyring, SK, Matalon, R (2003) Molecular basis of Canavan鈥檚 disease: from human to mouse. J Child Neurol 18: pp. 604-610 CrossRef
  58. Tallan, HH, Moore, S, Stein, WH (1956) N-Acetyl-l-aspartic acid in brain. J Biol Chem 219: pp. 257-264
  59. Tedeschi, G, Bertolino, A, Righini, A, Campbell, G, Raman, R, Duyn, JH (1995) Brain regional distribution pattern of metabolite signal intensities in young adults by proton magnetic resonance spectroscopic imaging. Neurology 45: pp. 1384-1391 5.7.1384" target="_blank" title="It opens in new window">CrossRef
  60. Traka, M, Wollmann, RL, Cerda, SR, Dugas, J, Barres, BA, Popko, B (2008) Nur7 is a nonsense mutation in the mouse aspartoacylase gene that causes spongy degeneration of the CNS. J Neurosci 28: pp. 11537-11549 523/JNEUROSCI.1490-08.2008" target="_blank" title="It opens in new window">CrossRef
  61. Truckenmiller, ME, Namboodiri, MA, Brownstein, MJ, Neale, JH (1985) N-Acetylation of l-aspartate in the nervous system: differential distribution of a specific enzyme. J Neurochem 45: pp. 1658-1662 59.1985.tb07240.x" target="_blank" title="It opens in new window">CrossRef
  62. Tsai, G, Coyle, JT (1995) N-acetylaspartate in neuropsychiatric disorders. Prog Neurobiol 46: pp. 531-540 5)00014-M" target="_blank" title="It opens in new window">CrossRef
  63. Wang, J, Matalon, R, Bhatia, G, Wu, G, Li, H, Liu, T (2007) Bimodal occurrence of aspartoacylase in myelin and cytosol of brain. J Neurochem 101: pp. 448-457 59.2006.04380.x" target="_blank" title="It opens in new window">CrossRef
  64. Wang, J, Leone, P, Wu, G, Francis, JS, Li, H, Jain, MR (2009) Myelin lipid abnormalities in the aspartoacylase-deficient tremor rat. Neurochem Res 34: pp. 138-148 5" target="_blank" title="It opens in new window">CrossRef
  65. Wevers, RA, Engelke, U, Wendel, U, Jong, JG, Gabreels, FJ, Heerschap, A (1995) Standardized method for high-resolution 1H-NMR of cerebrospinal fluid. Clin Chem 41: pp. 744-751
  66. Wiame, E, Tyteca, D, Pierrot, N, Collard, F, Amyere, M, Noel, G (2010) Molecular identification of aspartate N-acetyltransferase and its mutation in hypoacetylaspartia. Biochem J 425: pp. 127-136 CrossRef
  67. Wirt SE, Adler AS, Gebala V, Weimann JM, Schaffer BE, Saddic LA et al (2010) G1 arrest and differentiation can occur independently of Rb family function. J Cell Biol聽 191:809鈥?25
  68. Zeis T, Graumann U, Reynolds R, Schaeren-Wiemers N (2008) Normal-appearing white matter in multiple sclerosis is in a subtle balance between inflammation and neuroprotection. Brain 131:288鈥?03
  
• 刊物主题：Neurosciences; Cell Biology; Neurology;
• 出版者：Springer Berlin Heidelberg
• ISSN：1863-2661

文摘

The role of N-acetylaspartate in the brain is unclear. Here we used specific antibodies against N-acetylaspartate and immunocytochemistry of carbodiimide-fixed adult rodent brain to show that, besides staining of neuronal cell bodies in the grey matter, N-acetylaspartate labelling was present in oligodendrocytes/myelin in white matter tracts. Immunoelectron microscopy of the rat hippocampus showed that N-acetylaspartate was concentrated in the myelin. Also neuronal cell bodies and axons contained significant amounts of N-acetylaspartate, while synaptic elements and astrocytes were low in N-acetylaspartate. Mitochondria in axons and neuronal cell bodies contained higher levels of N-acetylaspartate compared to the cytosol, compatible with synthesis of N-acetylaspartate in mitochondria. In aspartoacylase knockout mice, in which catabolism of N-acetylaspartate is blocked, the levels of N-acetylaspartate were largely increased in oligodendrocytes/myelin. In these mice, the highest myelin concentration of N-acetylaspartate was found in the cerebellum, a region showing overt dysmyelination. In organotypic cortical slice cultures there was no evidence for N-acetylaspartate-induced myelin toxicity, supporting the notion that myelin damage is induced by the lack of N-acetylaspartate for lipid production. Our findings also implicate that N-acetylaspartate signals on magnetic resonance spectroscopy reflect not only vital neurons but also vital oligodendrocytes/myelin.