The transcriptome and metabolic gene signature of protoplasmic astrocytes in the adult murine cortex

Journal of Neuroscience

Volumn 27, Issue 45, 2007, Pages 12255-12266

  Lovatt, Ditte ^a   Sonnewald, Ursula ^b   Waagepetersen, Helle S ^c   Schousboe, Arne ^c   He, Wei ^a   Lin, Jane H C ^d   Han, Xiaoning ^a   Takano, Takahiro ^a   Wang, Su ^a   Sim, Fraser J ^a   Goldman, Steven A ^a   Nedergaard, Maiken ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d NEW YORK MEDICAL COLLEGE   (United States)

Author keywords

FACS; Glutamate; Glycolysis; Lactate; Mass spectrometry; Microarray; TCA cycle

Indexed keywords

GLUTAMIC ACID; TRANSCRIPTOME; TRICARBOXYLIC ACID;

AEROBIC METABOLISM; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN CORTEX; BRAIN METABOLISM; CELL COMPARTMENTALIZATION; CELL CULTURE; CELL FUNCTION; CELL SELECTION; CENTRAL NERVOUS SYSTEM; CITRIC ACID CYCLE; CONTROLLED STUDY; ENERGY METABOLISM; FLUORESCENCE ACTIVATED CELL SORTER; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GENE EXPRESSION; GENETIC TRANSCRIPTION; GENOMICS; GLIA; GLYCOLYSIS; MASS SPECTROMETRY; MICROARRAY ANALYSIS; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTOPLAST; SIGNAL TRANSDUCTION;

ANIMALS; ASTROCYTES; CEREBRAL CORTEX; CYTOPLASM; GENE EXPRESSION PROFILING; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC;

EID: 35548983491     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3404-07.2007     Document Type: Article

References (55)

1. Aoki C, Milner TA, Sheu KF, Blass JP, Pickel VM (1987) Regional distribution of astrocytes with intense immunoreactivity for glutamate dehydrogenase in rat brain: implications for neuron-glia interactions in glutamate transmission. J Neurosci 7:2214-2231.
2. Attwell D, Laughlin SB (2001) An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab 21:1133-1145.
3. Aubert A, Pellerin L, Magistretti PJ, Costalat R (2007) A coherent neurobiological framework for functional neuroimaging provided by a model integrating compartmentalized energy metabolism. Proc Natl Acad Sci USA 104:4188-4193.
4. Bak LK, Schousboe A, Sonnewald U, Waagepetersen HS (2006) Glucose is necessary to maintain neurotransmitter homeostasis during synaptic activity in cultured glutamatergic neurons. J Cereb Blood Flow Metab 26:1285-1297.
5. Berg JM, Tymoczko JL, Stryer L (2002) Biochemistry, Ed 5. New York: W. H. Freeman.
6. Biemann K (1962) Mass spectroscopy, organic chemistry applications. New York: McGraw.
7. Brown AM, Tekkok SB, Ransom BR (2003) Glycogen regulation and functional role in mouse white matter. J Physiol (Lond) 549:501-512.
8. Cerdan S, Rodrigues TB, Sierra A, Benito M, Fonseca LL, Fonseca CP, Garcia-Martin ML (2006) The redox switch/redox coupling hypothesis. Neurochem Int 48:523-530.
9. Cheeseman AJ, Clark JB (1988) Influence of the malate-aspartate shuttle on oxidative metabolism in synaptosomes. J Neurochem 50:1559-1565.
10. Clement AM, Nguyen MD, Roberts EA, Garcia ML, Boillee S, Rule M, Mc-Mahon AP, Doucette W, Siwek D, Ferrante RJ, Brown Jr RH, Julien JP, Goldstein LS, Cleveland DW (2003) Wild-type nonneuronal cells extend survival of SOD1 mutant motor neurons in ALS mice. Science 302:113-117.
11. Dringen R, Gebhardt R, Hamprecht B (1993) Glycogen in astrocytes: possible function as lactate supply for neighboring cells. Brain Res 623:208-214.
12. Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95:14863-14868.
13. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, Wallace M, Nerbonne JM, Lichtman JW, Sanes JR (2000) Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28:41-51.
14. Fitzpatrick SM, Cooper AJ, Duffy TE (1983) Use of beta-methylene-D,L- aspartate to assess the role of aspartate aminotransferase in cerebral oxidative metabolism. J Neurochem 41:1370-1383.
15. Goldman SA, Nedergaard M (1992) Newly generated neurons of the adult songbird brain become functionally active in long-term culture. Brain Res Dev Brain Res 68:217-223.
16. Hertz L, Peng L, Dienel GA (2007) Energy metabolism in astrocytes: high rate of oxidative metabolism and spatiotemporal dependence on glycolysis/glycogenolysis. J Cereb Blood Flow Metab 27:219-249.
17. Ibrahim MZ (1975) Glycogen and its related enzymes of metabolism in the central nervous system. Adv Anat Embryol Cell Biol 52:3-89.
18. Itoh Y, Esaki T, Shimoji K, Cook M, Law MJ, Kaufman E, Sokoloff L (2003) Dichloroacetate effects on glucose and lactate oxidation by neurons and astroglia in vitro and on glucose utilization by brain in vivo. Proc Natl Acad Sci USA 100:4879-4884.
19. Keyoung HM, Roy NS, Benraiss A, Louissaint A, Jr., Suzuki A, Hashimoto M, Rashbaum WK, Okano H, Goldman SA (2001) High-yield selection and extraction of two promoter-defined phenotypes of neural stem cells from the fetal human brain. Nat Biotechnol 19:843- 850.
20. Koehler RC, Gebremedhin D, Harder DR (2006) Role of astrocytes in cerebrovascular regulation. J Appl Physiol 100:307-317.
21. Lai JC, Murthy CR, Cooper AJ, Hertz E, Hertz L (1989) Differential effects of ammonia and beta-methylene-DL-aspartate on metabolism of glutamate and related amino acids by astrocytes and neurons in primary culture. Neurochem Res 14:377-389.
22. Lin SC, Huck JH, Roberts JD, Macklin WB, Somogyi P, Bergles DE (2005) Climbing fiber innervation of NG2-expressing glia in the mammalian cerebellum. Neuron 46:773-785.
23. Lobo MK, Karsten SL, Gray M, Geschwind DH, Yang XW (2006) FACS-array profiling of striatal projection neuron subtypes in juvenile and adult mouse brains. Nat Neurosci 9:443-452.
24. Magistretti PJ, Pellerin L, Rothman DL, Shulman RG (1999) Energy on demand. Science 283:496-497.
25. Mawhinney TP, Robinett RS, Atalay A, Madson MA (1986a) Analysis of amino acids as their tert.-butyldimethylsilyl derivatives by gas-liquid chromatography and mass spectrometry. J Chromatogr 358:231-242.
26. Mawhinney TP, Robinett RS, Atalay A, Madson MA (1986b) Gas-liquid chromatography and mass spectral analysis of mono-, di- and tricarboxylates as their tert.-butyldimethylsilyl derivatives. J Chromatogr 361:117-130.
27. McKenna MC, Waagepetersen H, Gruetter R, Sonnewald U, Schousboe A (2006) Cerebral metabolism and blood flow. In: Basic neurochemistry, Ed 7. London: Elsevier.
28. Nagai M, Re DB, Nagata T, Chalazonitis A, Jessell TM, Wichterle H, Przedborski S (2007) Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons. Nat Neurosci 10:615-622.
29. Nielsen S, Nagelhus EA, Amiry-Moghaddam M, Bourque C, Agre P, Ottersen OP (1997) Specialized membrane domains for water transport in glial cells: high-resolution immunogold cytochemistry of aquaporin-4 in rat brain. J Neurosci 17:171-180.
30. Nunes MC, Roy NS, Keyoung HM, Goodman RR, McKhann II G, Jiang L, Kang J, Nedergaard M, Goldman SA (2003) Identification and isolation of multipotential neural progenitor cells from the subcortical white matter of the adult human brain. Nat Med 9:439-447.
31. O'Brien J, Kla KM, Hopkins IB, Malecki EA, McKenna MC (2007) Kinetic parameters and lactate dehydrogenase isozyme activities support possible lactate utilization by neurons. Neurochem Res 32:597-607.
32. Olstad E, Qu H, Sonnewald U (2007) Glutamate is preferred over glutamine for intermediary metabolism in cultured cerebellar neurons. J Cereb Blood Flow Metab 27:811-820.
33. Paukert M, Bergles DE (2006) Synaptic communication between neurons and NG2+ cells. Curr Opin Neurobiol 16:515-521.
34. Pellerin L, Magistretti PJ (1994) Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc Natl Acad Sci USA 91:10625-10629.
35. Pellerin L, Magistretti PJ (2004) Neuroenergetics: calling upon astrocytes to satisfy hungry neurons. Neuroscientist 10:53-62.
36. Pfeiffer B, Meyermann R, Hamprecht B (1992) Immunohistochemical colocalization of glycogen phosphorylase with the astroglial markers glial fibrillary acidic protein and S-100 protein in rat brain sections. Histochemistry 97:405-412.
37. Pysh JJ, Khan T (1972) Variations in mitochondrial structure and content of neurons and neuroglia of rat brain: an electron microscopoy study. Brain Res 36:1-18.
38. Ramos M, del Arco A, Pardo B, Martinez-Serrano A, Martinez-Morales JR, Kobayashi K, Yasuda T, Bogonez E, Bovolenta P, Saheki T, Satrustegui J (2003) Developmental changes in the Ca2+-regulated mitochondrial aspartate-glutamate carrier aralar1 in brain and prominent expression in the spinal cord. Brain Res Dev Brain Res 143:33-46.
39. Regan MR, Huang YH, Kim YS, Dykes-Hoberg MI, Jin L, Watkins AM, Bergles DE, Rothstein JD (2007) 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.
40. Schmechel D, Marangos PJ, Zis AP, Brightman M, Goodwin FK (1978) Brain endolases as specific markers of neuronal and glial cells. Science 199:313-315.
41. Schurr A (2006) Lactate: the ultimate cerebral oxidative energy substrate? J Cereb Blood Flow Metab 26:142-152.
42. Shank RP, Bennett GS, Freytag SO, Campbell GL (1985) Pyruvate carboxylase: an astrocyte-specific enzyme implicated in the replenishment of amino acid neurotransmitter pools. Brain Res 329:364-367.
43. Sibson NR, Dhankhar A, Mason GF, Rothman DL, Behar KL, Shulman RG (1998) Stoichiometric coupling of brain glucose metabolism and glutamatergic neuronal activity. Proc Natl Acad Sci USA 95:316-321.
44. Sim F, Lang J, Waldau B, Roy N, Schwartz T, Pilcher W, Chandross K, Natesan S, Merrill J, Goldman S (2006) Complementary patterns of gene expression by adult human oligodendrocyte progenitor cells and their white matter environment. Ann Neurol 59:763-779.
45. Simard M, Arcuino G, Takano T, Liu QS, Nedergaard M (2003) Signaling at the gliovascular interface. J Neurosci 23:9254-9262.
46. Takano T, Tian GF, Peng W, Lou N, Libionka W, Han X, Nedergaard M (2006) Astrocyte-mediated control of cerebral blood flow. Nat Neurosci 9:260-267.
47. Takano T, Tian GF, Peng W, Lou N, Lovatt D, Hansen AJ, Kasischke KA, Nedergaard M (2007) Cortical spreading depression causes and coincides with tissue hypoxia. Nat Neurosci 10:754-762.
48. Volterra A, Meldolesi J (2005) Astrocytes, from brain glue to communication elements: the revolution continues. Nat Rev Neurosci 6:626-640.
49. Waagepetersen HS, Qu H, Schousboe A, Sonnewald U (2001) Elucidation of the quantitative significance of pyruvate carboxylation in cultured cerebellar neurons and astrocytes. J Neurosci Res 66:763-770.
50. Wang K, Walz W (2003) Unusual topographical pattern of proximal astrogliosis around a cortical devascularizing lesion. J Neurosci Res 73:497-506.
51. Wang S, Wu H, Jiang J, Delohery TM, Isdell F, Goldman SA (1998) Isolation of neuronal precursors by sorting embryonic forebrain transfected with GFP regulated by the T alpha 1 tubulin promoter. Nat Biotechnol 16:196-201.
52. Wender R, Brown AM, Fern R, Swanson RA, Farrell K, Ransom BR (2000) Astrocytic glycogen influences axon function and survival during glucose deprivation in central white matter. J Neurosci 20:6804-6810.
53. Wilhelm A, Volknandt W, Langer D, Nolte C, Kettenmann H, Zimmermann H (2004) Localization of SNARE proteins and secretory organelle proteins in astrocytes in vitro and in situ. Neurosci Res 48:249-257.
54. Yu AC, Drejer J, Hertz L, Schousboe A (1983) Pyruvate carboxylase activity in primary cultures of astrocytes and neurons. J Neurochem 41:1484-1487.
55. Zhuo L, Sun B, Zhang CL, Fine A, Chiu SY, Messing A (1997) Live astrocytes visualized by green fluorescent protein in transgenic mice. Dev Biol 187:36-42.