Network of brain protein level changes in glutaminase deficient fetal mice

Journal of Proteomics

Volumn 80, Issue , 2013, Pages 236-249

  Bae, Narkhyun ^a   Wang, Yvonne ^b   Li, Lin ^a   Rayport, Stephen ^b,c   Lubec, Gert ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b Och Spine at New York Presbyterian Hospitals   (United States)

^c NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

Author keywords

Gls; Glutaminase; LC MS MS; Protein network; Schizophrenia

Indexed keywords

ALPHA TROPOMYOSIN; APOLIPOPROTEIN; BRAIN PROTEIN; CALCIUM; CELLULAR RETINOL BINDING PROTEIN 1; COLLAPSIN RESPONSE MEDIATOR PROTEIN; FASCIN; GLUTAMIC ACID; GLUTAMINASE; GLUTAMINE; HEPATOCYTE NUCLEAR FACTOR 4; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN C; HUNTINGTIN; ION CHANNEL; NEUROCALCIN; PROTEASOME; PROTEIN KINASE B; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; RETINOL; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL EXPERIMENT; ARTICLE; CELL CYCLE; ELECTROSPRAY MASS SPECTROMETRY; ENDOPLASMIC RETICULUM; FETUS; GENETIC VARIABILITY; IMMUNOBLOTTING; INTRACELLULAR SIGNALING; LIMIT OF QUANTITATION; LIPID METABOLISM; LIQUID CHROMATOGRAPHY; MALE; MOUSE; NONHUMAN; NUCLEIC ACID METABOLISM; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; PROTEOMICS; TANDEM MASS SPECTROMETRY; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ANIMALS; BRAIN; BRAIN CHEMISTRY; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FETUS; GLUTAMINASE; MALE; METABOLIC NETWORKS AND PATHWAYS; MICE; NERVE TISSUE PROTEINS; PROTEOMICS; SIGNAL TRANSDUCTION; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TANDEM MASS SPECTROMETRY;

EID: 84874568650     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2013.01.013     Document Type: Article

References (58)

1. Nicklas W.J., Zeevalk G., Hyndman A. Interactions between neurons and glia in glutamate/glutamine compartmentation. Biochem Soc Trans 1987, 15:208-210.
2. Kvamme E., Roberg B., Torgner I.A. Phosphate-activated glutaminase and mitochondrial glutamine transport in the brain. Neurochem Res 2000, 25:1407-1419.
3. Perera S.Y., Chen T.C., Curthoys N.P. Biosynthesis and processing of renal mitochondrial glutaminase in cultured proximal tubular epithelial cells and in isolated mitochondria. J Biol Chem 1990, 265:17764-17770.
4. Srinivasan M., Kalousek F., Curthoys N.P. In vitro characterization of the mitochondrial processing and the potential function of the 68-kDa subunit of renal glutaminase. J Biol Chem 1995, 270:1185-1190.
5. Curthoys N.P., Watford M. Regulation of glutaminase activity and glutamine metabolism. Annu Rev Nutr 1995, 15:133-159.
6. Elgadi K.M., Meguid R.A., Qian M., Souba W.W., Abcouwer S.F. Cloning and analysis of unique human glutaminase isoforms generated by tissue-specific alternative splicing. Physiol Genomics 1999, 1:51-62.
7. Olalla L., Gutierrez A., Campos J.A., Khan Z.U., Alonso F.J., Segura J.A., et al. Nuclear localization of L-type glutaminase in mammalian brain. J Biol Chem 2002, 277:38939-38944.
8. Aledo J.C., Gomez-Fabre P.M., Olalla L., Marquez J. Identification of two human glutaminase loci and tissue-specific expression of the two related genes. Mamm Genome 2000, 11:1107-1110.
9. Aoki C., Kaneko T., Starr A., Pickel V.M. Identification of mitochondrial and non-mitochondrial glutaminase within select neurons and glia of rat forebrain by electron microscopic immunocytochemistry. J Neurosci Res 1991, 28:531-548.
10. Laake J.H., Slyngstad T.A., Haug F.M., Ottersen O.P. Glutamine from glial cells is essential for the maintenance of the nerve terminal pool of glutamate: immunogold evidence from hippocampal slice cultures. J Neurochem 1995, 65:871-881.
11. Hertz L. Functional interactions between neurons and astrocytes I. Turnover and metabolism of putative amino acid transmitters. Prog Neurobiol 1979, 13:277-323.
12. Hertz L., Zielke H.R. Astrocytic control of glutamatergic activity: astrocytes as stars of the show. Trends Neurosci 2004, 27:735-743.
13. Kam K., Nicoll R. Excitatory synaptic transmission persists independently of the glutamate-glutamine cycle. J Neurosci 2007, 27:9192-9200.
14. Takeda K., Ishida A., Takahashi K., Ueda T. Synaptic vesicles are capable of synthesizing the VGLUT substrate glutamate from alpha-ketoglutarate for vesicular loading. J Neurochem 2012, 121:184-196.
15. Maciejewski P.K., Rothman D.L. Proposed cycles for functional glutamate trafficking in synaptic neurotransmission. Neurochem Int 2008, 52:809-825.
16. Masson J., Darmon M., Conjard A., Chuhma N., Ropert N., Thoby-Brisson M., et al. Mice lacking brain/kidney phosphate-activated glutaminase have impaired glutamatergic synaptic transmission, altered breathing, disorganized goal-directed behavior and die shortly after birth. J Neurosci 2006, 26:4660-4671.
17. Gaisler-Salomon I., Miller G.M., Chuhma N., Lee S., Zhang H., Ghoddoussi F., et al. Glutaminase-deficient mice display hippocampal hypoactivity, insensitivity to pro-psychotic drugs and potentiated latent inhibition: relevance to schizophrenia. Neuropsychopharmacology 2009, 34:2305-2322.
18. Chen W., Mahadomrongkul V., Berger U.V., Bassan M., DeSilva T., Tanaka K., et al. The glutamate transporter GLT1a is expressed in excitatory axon terminals of mature hippocampal neurons. J Neurosci 2004, 24:1136-1148.
19. Bleich S., Romer K., Wiltfang J., Kornhuber J. Glutamate and the glutamate receptor system: a target for drug action. Int J Geriatr Psychiatry 2003, 18:S33-S40.
20. Hannan A.J. Novel therapeutic targets for Huntington's disease. Expert Opin Ther Targets 2005, 9:639-650.
21. Schaeffer E.L., Gattaz W.F. Cholinergic and glutamatergic alterations beginning at the early stages of Alzheimer disease: participation of the phospholipase A2 enzyme. Psychopharmacology 2008, 198:1-27.
22. Driscoll B.F., Deibler G.E., Law M.J., Crane A.M. Damage to neurons in culture following medium change: role of glutamine and extracellular generation of glutamate. J Neurochem 1993, 61:1795-1800.
23. Choudary P.V., Molnar M., Evans S.J., Tomita H., Li J.Z., Vawter M.P., et al. Altered cortical glutamatergic and GABAergic signal transmission with glial involvement in depression. Proc Natl Acad Sci U S A 2005, 102:15653-15658.
24. Bruneau E.G., McCullumsmith R.E., Haroutunian V., Davis K.L., Meador-Woodruff J.H. Increased expression of glutaminase and glutamine synthetase mRNA in the thalamus in schizophrenia. Schizophr Res 2005, 75:27-34.
25. Gluck M.R., Thomas R.G., Davis K.L., Haroutunian V. Implications for altered glutamate and GABA metabolism in the dorsolateral prefrontal cortex of aged schizophrenic patients. Am J Psychiatry 2002, 159:1165-1173.
26. Harrison P.J., Weinberger D.R. Schizophrenia genes, gene expression, and neuropathology: on the matter of their convergence. Mol Psychiatry 2005, 10:40-68. [image 5].
27. Schobel S.A., Lewandowski N.M., Corcoran C.M., Moore H., Brown T., Malaspina D., et al. Differential targeting of the CA1 subfield of the hippocampal formation by schizophrenia and related psychotic disorders. Arch Gen Psychiatry 2009, 66:938-946.
28. Hoorn E.J., Hoffert J.D., Knepper M.A. Combined proteomics and pathways analysis of collecting duct reveals a protein regulatory network activated in vasopressin escape. J Am Soc Nephrol 2005, 16:2852-2863.
29. Raponi M., Belly R.T., Karp J.E., Lancet J.E., Atkins D., Wang Y. Microarray analysis reveals genetic pathways modulated by tipifarnib in acute myeloid leukemia. BMC Cancer 2004, 4:56.
30. Siripurapu V., Meth J., Kobayashi N., Hamaguchi M. DBC2 significantly influences cell-cycle, apoptosis, cytoskeleton and membrane-trafficking pathways. J Mol Biol 2005, 346:83-89.
31. Carr S., Aebersold R., Baldwin M., Burlingame A., Clauser K., Nesvizhskii A. The need for guidelines in publication of peptide and protein identification data: working group on publication guidelines for peptide and protein identification data. Mol Cell Proteomics 2004, 3:531-533.
32. Tsuji A., Kikuchi Y., Sato Y., Koide S., Yuasa K., Nagahama M., et al. A proteomic approach reveals transient association of reticulocalbin-3, a novel member of the CREC family, with the precursor of subtilisin-like proprotein convertase, PACE4. Biochem J 2006, 396:51-59.
33. de la Rosa V., Campos-Sandoval J.A., Martin-Rufian M., Cardona C., Mates J.M., Segura J.A., et al. A novel glutaminase isoform in mammalian tissues. Neurochem Int 2009, 55:76-84.
34. Mates J.M., Segura J.A., Campos-Sandoval J.A., Lobo C., Alonso L., Alonso F.J., et al. Glutamine homeostasis and mitochondrial dynamics. Int J Biochem Cell Biol 2009, 41:2051-2061.
35. Martin-Rufian M., Tosina M., Campos-Sandoval J.A., Manzanares E., Lobo C., Segura J.A., et al. Mammalian glutaminase Gls2 gene encodes two functional alternative transcripts by a surrogate promoter usage mechanism. PLoS One 2012, 7:e38380.
36. Aizawa S., Sakai T., Sakata I. Glutamine and glutamic acid enhance thyroid-stimulating hormone beta subunit mRNA expression in the rat pars tuberalis. J Endocrinol 2012, 212:383-394.
37. Hu W., Zhang C., Wu R., Sun Y., Levine A., Feng Z. Glutaminase 2, a novel p53 target gene regulating energy metabolism and antioxidant function. Proc Natl Acad Sci U S A 2010, 107:7455-7460.
38. Marquez J., Tosina M., de la Rosa V., Segura J.A., Alonso F.J., Mates J.M., et al. New insights into brain glutaminases: beyond their role on glutamatergic transmission. Neurochem Int 2009, 55:64-70.
39. Erecinska M., Zaleska M.M., Nelson D., Nissim I., Yudkoff M. Neuronal glutamine utilization: glutamine/glutamate homeostasis in synaptosomes. J Neurochem 1990, 54:2057-2069.
40. Kvamme E., Svenneby G., Torgner I.A. Calcium stimulation of glutamine hydrolysis in synaptosomes from rat brain. Neurochem Res 1983, 8:25-38.
41. Yoo B.C., Fountoulakis M., Cairns N., Lubec G. Changes of voltage-dependent anion-selective channel proteins VDAC1 and VDAC2 brain levels in patients with Alzheimer's disease and Down syndrome. Electrophoresis 2001, 22:172-179.
42. Kaltenbach L.S., Romero E., Becklin R.R., Chettier R., Bell R., Phansalkar A., et al. Huntingtin interacting proteins are genetic modifiers of neurodegeneration. PLoS Genet 2007, 3:e82.
43. Culver B.P., Savas J.N., Park S.K., Choi J.H., Zheng S., Zeitlin S.O., et al. Proteomic analysis of wild-type and mutant huntingtin-associated proteins in mouse brains identifies unique interactions and involvement in protein synthesis. J Biol Chem 2012, 287:21599-21614.
44. Lei G., Xia Y., Johnson K.M. The role of Akt-GSK-3beta signaling and synaptic strength in phencyclidine-induced neurodegeneration. Neuropsychopharmacology 2008, 33:1343-1353.
45. Wang Q., Liu L., Pei L., Ju W., Ahmadian G., Lu J., et al. Control of synaptic strength, a novel function of Akt. Neuron 2003, 38:915-928.
46. Pratt K.G., Zimmerman E.C., Cook D.G., Sullivan J.M. Presenilin 1 regulates homeostatic synaptic scaling through Akt signaling. Nat Neurosci 2011, 14:1112-1114.
47. Majumdar D., Nebhan C.A., Hu L., Anderson B., Webb D.J. An APPL1/Akt signaling complex regulates dendritic spine and synapse formation in hippocampal neurons. Mol Cell Neurosci 2011, 46:633-644.
48. Horwood J.M., Dufour F., Laroche S., Davis S. Signalling mechanisms mediated by the phosphoinositide 3-kinase/Akt cascade in synaptic plasticity and memory in the rat. Eur J Neurosci 2006, 23:3375-3384.
49. Bruel-Jungerman E., Veyrac A., Dufour F., Horwood J., Laroche S., Davis S. Inhibition of PI3K-Akt signaling blocks exercise-mediated enhancement of adult neurogenesis and synaptic plasticity in the dentate gyrus. PLoS One 2009, 4:e7901.
50. Beaulieu J.M., Sotnikova T.D., Marion S., Lefkowitz R.J., Gainetdinov R.R., Caron M.G. An Akt/beta-arrestin 2/PP2A signaling complex mediates dopaminergic neurotransmission and behavior. Cell 2005, 122:261-273.
51. Hou L., Klann E. Activation of the phosphoinositide 3-kinase-Akt-mammalian target of rapamycin signaling pathway is required for metabotropic glutamate receptor-dependent long-term depression. J Neurosci 2004, 24:6352-6361.
52. Yun C., Mendelson J., Blake T., Mishra L., Mishra B. TGF-beta signaling in neuronal stem cells. Dis Markers 2008, 24:251-255.
53. Yi J.J., Barnes A.P., Hand R., Polleux F., Ehlers M.D. TGF-beta signaling specifies axons during brain development. Cell 2010, 142:144-157.
54. Awasaki T., Huang Y., O'Connor M.B., Lee T. Glia instruct developmental neuronal remodeling through TGF-beta signaling. Nat Neurosci 2011, 14:821-823.
55. Vogel T., Ahrens S., Buttner N., Krieglstein K. Transforming growth factor beta promotes neuronal cell fate of mouse cortical and hippocampal progenitors in vitro and in vivo: identification of Nedd9 as an essential signaling component. Cereb Cortex 2010, 20:661-671.
56. Misumi S., Kim T.S., Jung C.G., Masuda T., Urakawa S., Isobe Y., et al. Enhanced neurogenesis from neural progenitor cells with G1/S-phase cell cycle arrest is mediated by transforming growth factor beta1. Eur J Neurosci 2008, 28:1049-1059.
57. Toresson H., Mata de Urquiza A., Fagerstrom C., Perlmann T., Campbell K. Retinoids are produced by glia in the lateral ganglionic eminence and regulate striatal neuron differentiation. Development 1999, 126:1317-1326.
58. El Hage M., Masson J., Conjard-Duplany A., Ferrier B., Baverel G., Martin G. Brain slices from glutaminase-deficient mice metabolize less glutamine: a cellular metabolomic study with carbon 13 NMR. J Cereb Blood Flow Metab 2012, 32:816-824.