Synaptic underpinnings of altered hippocampal function in glutaminase-deficient mice during maturation

Hippocampus

Volumn 22, Issue 5, 2012, Pages 1027-1039

  Gaisler Salomon, Inna ^a,b,c   Wang, Yvonne ^a,b   Chuhma, Nao ^a,b   Zhang, Hong ^a   Golumbic, Yaela N ^c   Mihali, Andra ^a,b   Arancio, Ottavio ^a   Sibille, Etienne ^d   Rayport, Stephen ^a,b  

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

^b NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

^c UNIVERSITY OF HAIFA   (Israel)

^d UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

GLS1; Glutamate; Hippocampus; NR1; Schizophrenia

Indexed keywords

GLUTAMATE RECEPTOR; GLUTAMINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN CORTEX; BRAIN DISEASE; BRAIN ELECTROPHYSIOLOGY; BRAIN MATURATION; BRAIN REGION; CONTROLLED STUDY; ENZYME DEFICIENCY; ENZYME INHIBITION; GENE EXPRESSION; GENOTYPE; GLUTAMINASE DEFICIENCY; HIPPOCAMPAL HYPOACTIVITY; HIPPOCAMPUS; MALE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCHIZOPHRENIA;

AGE FACTORS; ANIMALS; CONDITIONING (PSYCHOLOGY); FEAR; FEMALE; GENE EXPRESSION; GLUTAMIC ACID; GLUTAMINASE; HIPPOCAMPUS; INHIBITION (PSYCHOLOGY); LONG-TERM POTENTIATION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, AMPA; RECEPTORS, N-METHYL-D-ASPARTATE; SCHIZOPHRENIA; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84862777646     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.22014     Document Type: Article

References (73)

1. Abe Y, Namba H, Kato T, Iwakura Y, Nawa H. 2011. Neuregulin-1 signals from the periphery regulate AMPA receptor sensitivity and expression in GABAergic interneurons in developing neocortex. J Neurosci 31: 5699-5709.
2. Abramoff M, Magalhaes P, Ram S. 2004. Image processing with ImageJ. Biophotonics Int 11: 36-42.
3. Anand A, Charney DS, Oren DA, Berman RM, Hu XS, Cappiello A, Krystal JH. 2000. Attenuation of the neuropsychiatric effects of ketamine with lamotrigine: support for hyperglutamatergic effects of N-methyl-D-aspartate receptor antagonists. Arch Gen Psychiatr 57: 270-276.
4. Balschun D, Moechars D, Callaerts-Vegh Z, Vermaercke B, Van Acker N, Andries L, D'Hooge R. 2009. Vesicular glutamate transporter VGLUT1 has a role in hippocampal long-term potentiation and spatial reversal learning. Cereb Cortex 20: 684-693.
5. Barak S, Weiner I. 2011. The M1/M4 preferring agonist xanomeline reverses amphetamine-, MK801- and scopolamine-induced abnormalities of latent inhibition: putative efficacy against positive, negative and cognitive symptoms in schizophrenia. Int J Neuropsychopharmacol 14: 1233-1246.
6. Bardoni R, Torsney C, Tong CK, Prandini M, MacDermott AB. 2004. Presynaptic NMDA receptors modulate glutamate release from primary sensory neurons in rat spinal cord dorsal horn. J Neurosci 24: 2774-2781.
7. Belforte JE, Zsiros V, Sklar ER, Jiang Z, Yu G, Li Y, Quinlan EM, Nakazawa K. 2010. Postnatal NMDA receptor ablation in corticolimbic interneurons confers schizophrenia-like phenotypes. Nat Neurosci 13: 76-83.
8. Bookout AL, Mangelsdorf DJ. 2003. Quantitative real-time PCR protocol for analysis of nuclear receptor signaling pathways. Nucl Recept Signal 1: e012.
9. Bruneau EG, McCullumsmith RE, Haroutunian V, Davis KL, Meador-Woodruff JH. 2005. Increased expression of glutaminase and glutamine synthetase mRNA in the thalamus in schizophrenia. Schizophr Res 75: 27-34.
10. Carpenter-Hyland EP, Chandler LJ. 2007. Adaptive plasticity of NMDA receptors and dendritic spines: implications for enhanced vulnerability of the adolescent brain to alcohol addiction. Pharmacol Biochem Behav 86: 200-208.
11. Curthoys NP, Watford M. 1995. Regulation of glutaminase activity and glutamine metabolism. Annu Rev Nutr 15: 133-159.
12. Deakin JF, Lees J, McKie S, Hallak JE, Williams SR, Dursun SM. 2008. Glutamate and the neural basis of the subjective effects of ketamine: a pharmaco-magnetic resonance imaging study. Arch Gen Psychiatr 65: 154-164.
13. Duncan G, Miyamoto S, Gu H, Lieberman J, Koller B, Snouwaert J. 2002. Alterations in regional brain metabolism in genetic and pharmacological models of reduced NMDA receptor function. Brain Res 951: 166-176.
14. Duncan GE, Inada K, Farrington JS, Koller BH, Moy SS. 2009. Neural activation deficits in a mouse genetic model of NMDA receptor hypofunction in tests of social aggression and swim stress. Brain Res 1265: 186-195.
15. Frick A, Feldmeyer D, Sakmann B. 2007. Postnatal development of synaptic transmission in local networks of L5A pyramidal neurons in rat somatosensory cortex. J Physiol 585: 103-116.
16. Gaisler-Salomon I, Wang Y, McKinney SM, Ramsey AJ, Sibille EL, Rayport S. 2008. Differential expression of AMPA and NMDA receptors in the hippocampus of glutaminase-deficient mice. Society for Neuroscience Abstracts 254.2.
17. Gaisler-Salomon I, Miller GM, Chuhma N, Lee S, Zhang H, Ghoddoussi F, Lewandowski N, Fairhurst S, Wang Y, Conjard-Duplany A, Masson J, Balsam P, Hen R, Arancio O, Galloway MP, Moore HM, Small SA, Rayport S. 2009a. Glutaminase-deficient mice display hippocampal hypoactivity, insensitivity to pro-psychotic drugs and potentiated latent inhibition: relevance to schizophrenia. Neuropsychopharmacology 34: 2305-2322.
18. Gaisler-Salomon I, Schobel SA, Small SA, Rayport S. 2009b. How high-resolution basal-state functional imaging can guide the development of new pharmacotherapies for schizophrenia. Schizophr Bull 35: 1037-1044.
19. Gao C, Gill MB, Tronson NC, Guedea AL, Guzman YF, Huh KH, Corcoran KA, Swanson GT, Radulovic J. 2010. Hippocampal NMDA receptor subunits differentially regulate fear memory formation and neuronal signal propagation. Hippocampus 20: 1072-1082.
20. Gaspar PA, Bustamante ML, Silva H, Aboitiz F. 2009. Molecular mechanisms underlying glutamatergic dysfunction in schizophrenia: therapeutic implications. J Neurochem 111: 891-900.
21. Gluck MR, Thomas RG, Davis KL, Haroutunian V. 2002. Implications for altered glutamate and GABA metabolism in the dorsolateral prefrontal cortex of aged schizophrenic patients. Am J Psychiatry 159: 1165-1173.
22. Gong S, Zheng C, Doughty ML, Losos K, Didkovsky N, Schambra UB, Nowak NJ, Joyner A, Leblanc G, Hatten ME, Heintz N. 2003. A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 425: 917-925.
23. Gore AC, Wu TJ, Rosenberg JJ, Roberts JL. 1996. Gonadotropin-releasing hormone and NMDA receptor gene expression and colocalization change during puberty in female rats. J Neurosci 16: 5281-5289.
24. Grunze HC, Rainnie DG, Hasselmo ME, Barkai E, Hearn EF, McCarley RW, Greene RW. 1996. NMDA-dependent modulation of CA1 local circuit inhibition. J Neurosci 16: 2034-2043.
25. Guilarte T. 2003. Selective decrease in NR1 subunit splice variant mRNA in the hippocampus of Pb2+-exposed rats: implications for synaptic targeting and cell surface expression of NMDAR complexes. Mol Brain Res 113: 37-43.
26. Halene TB, Ehrlichman RS, Liang Y, Christian EP, Jonak GJ, Gur TL, Blendy JA, Dow HC, Brodkin ES, Schneider F, Gur RC, Siegel SJ. 2009. Assessment of NMDA receptor NR1 subunit hypofunction in mice as a model for schizophrenia. Genes Brain Behav 8: 661-675.
27. Harre EM, Galic MA, Mouihate A, Noorbakhsh F, Pittman QJ. 2008. Neonatal inflammation produces selective behavioural deficits and alters N-methyl-D-aspartate receptor subunit mRNA in the adult rat brain. Eur J Neurosci 27: 644-653.
28. Harrison PJ, Weinberger DR. 2005. Schizophrenia genes, gene expression, and neuropathology: on the matter of their convergence. Mol Psychiatr 10: 40-68.
29. Henson MA, Roberts AC, Salimi K, Vadlamudi S, Hamer RM, Gilmore JH, Jarskog LF, Philpot BD. 2008. Developmental regulation of the NMDA receptor subunits, NR3A and NR1, in human prefrontal cortex. Cereb Cortex 18: 2560-2573.
30. Hertz L, Zielke HR. 2004. Astrocytic control of glutamatergic activity: astrocytes as stars of the show. Trends Neurosci 27: 735-743.
31. Higgins GA, Ballard TM, Huwyler J, Kemp JA, Gill R. 2003. Evaluation of the NR2B-selective NMDA receptor antagonist Ro 63-1908 on rodent behaviour: evidence for an involvement of NR2B NMDA receptors in response inhibition. Neuropharmacology 44: 324-341.
32. Homayoun H, Moghaddam B. 2007. NMDA receptor hypofunction produces opposite effects on prefrontal cortex interneurons and pyramidal neurons. J Neurosci 27: 11496-11500.
33. Homayoun H, Jackson ME, Moghaddam B. 2005. Activation of metabotropic glutamate 2/3 receptors reverses the effects of NMDA receptor hypofunction on prefrontal cortex unit activity in awake rats. J Neurophysiol 93: 1989-2001.
34. Howell DC. 2010. Statistical Methods for Psychology. Belmont, CA: Cengage Wadsworth. 768 p.
35. Inta D, Monyer H, Sprengel R, Meyer-Lindenberg A, Gass P. 2010. Mice with genetically altered glutamate receptors as models of schizophrenia: a comprehensive review. Neurosci Biobehav Rev 34: 285-294.
36. Javitt DC, Zukin SR. 1991. Recent advances in the phencyclidine model of schizophrenia. Am J Psychiatr 148: 1301-1308.
37. Kam K, Nicoll R. 2007. Excitatory synaptic transmission persists independently of the glutamate-glutamine cycle. J Neurosci 27: 9192-9200.
38. Kerdsan W, Thanoi S, Nudmamud-Thanoi S. 2009. Changes in glutamate/NMDA receptor subunit 1 expression in rat brain after acute and subacute exposure to methamphetamine. J Biomed Biotechnol 2009: 329631.
39. Kvamme E, Torgner IA, Roberg BA. 2001. Kinetics and localization of brain phosphate activated glutaminase. J Neurosci Res 66: 951-958.
40. Lang UE, Puls I, Muller DJ, Strutz-Seebohm N, Gallinat J. 2007. Molecular mechanisms of schizophrenia. Cell Physiol Biochem 20: 687-702.
41. Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A, Bernard A, Boe AF, Boguski MS, Brockway KS, Byrnes EJ, Chen L, Chen L, Chen T-M, Chi Chin M, Chong J, Crook BE, Czaplinska A, Dang CN, Datta S, Dee NR, Desaki AL, Desta T, Diep E, Dolbeare TA, Donelan MJ, Dong H-W, Dougherty JG, Duncan BJ, Ebbert AJ, Eichele G, Estin LK, Faber C, Facer BA, Fields R, Fischer SR, Fliss TP, Frensley C, Gates SN, Glattfelder KJ, Halverson KR, Hart MR, Hohmann JG, Howell MP, Jeung DP, Johnson RA, Karr PT, Kawal R, Kidney JM, Knapik RH, Kuan CL, Lake JH, Laramee AR, Larsen KD, Lau C, Lemon TA, Liang AJ, Liu Y, Luong LT, Michaels J, Morgan JJ, Morgan RJ, Mortrud MT, Mosqueda NF, Ng LL, Ng R, Orta GJ, Overly CC, Pak TH, Parry SE, Pathak SD, Pearson OC, Puchalski RB, Riley ZL, Rockett HR, Rowland SA, Royall JJ, Ruiz MJ, Sarno NR, Schaffnit K, Shapovalova NV, Sivisay T, Slaughterbeck CR, Smith SC, Smith KA, Smith BI, Sodt AJ, Stewart NN, Stumpf K-R, Sunkin SM, Sutram M, Tam A, Teemer CD, Thaller C, Thompson CL, Varnam LR, Visel A, Whitlock RM, Wohnoutka PE, Wolkey CK, Wong VY, Wood M, Yaylaoglu MB, Young RC, Youngstrom BL, Yuan XF, Zhang B, Zwingman TA, Jones AR. 2007. Genome-wide atlas of gene expression in the adult mouse brain. Nature 445: 168-176.
42. Levenson J, Weeber E, Selcher JC, Kategaya LS, Sweatt JD, Eskin A. 2002. Long-term potentiation and contextual fear conditioning increase neuronal glutamate uptake. Nat Neurosci 5: 155-161.
43. Lewis DA, Moghaddam B. 2006. Cognitive dysfunction in schizophrenia: convergence of gamma-aminobutyric acid and glutamate alterations. Arch Neurol 63: 1372-1376.
44. Lisman JE, Pi HJ, Zhang Y, Otmakhova NA. 2010. A thalamo-hippocampal-ventral tegmental area loop may produce the positive feedback that underlies the psychotic break in schizophrenia. Biol Psychiatr 68: 17-24.
45. Little RJA, Rubin DB. 2002. Statistical Analysis with Missing Data. Hoboken, NJ: Wiley. 381 p.
46. Maeshima H, Ohnuma T, Sakai Y, Shibata N, Baba H, Ihara H, Higashi M, Ohkubo T, Nozawa E, Abe S, Ichikawa A, Nakano Y, Utsumi Y, Suzuki T, Arai H. 2007. Increased plasma glutamate by antipsychotic medication and its relationship to glutaminase 1 and 2 genotypes in schizophrenia-Juntendo University Schizophrenia Projects (JUSP). Prog Neuropsychopharmacol Biol Psychiatr 31: 1410-1418.
47. Maren S, Holt W. 2000. The hippocampus and contextual memory retrieval in Pavlovian conditioning. Behav Brain Res 110: 97-108.
48. Masson J, Darmon M, Conjard A, Chuhma N, Ropert N, Thoby-Brisson M, Foutz A, Parrot S, Miller GM, Jorisch R, Polan J, Hamon M, Hen R, Rayport S. 2006. Mice lacking brain/kidney phosphate-activated glutaminase (GLS1) have impaired glutamatergic synaptic transmission, altered breathing, disorganized goal-directed behavior and die shortly after birth. J Neurosci 26: 4660-4671.
49. McGuinness L, Taylor C, Taylor RD, Yau C, Langenhan T, Hart ML, Christian H, Tynan PW, Donnelly P, Emptage NJ. 2010. Presynaptic NMDARs in the hippocampus facilitate transmitter release at theta frequency. Neuron 68: 1109-1127.
50. McHugh TJ, Tonegawa S. 2009. CA3 NMDA receptors are required for the rapid formation of a salient contextual representation. Hippocampus 19: 1153-1158.
51. Moghaddam B. 2003. Bringing order to the glutamate chaos in schizophrenia. Neuron 40: 881-884.
52. Moghaddam B, Adams BW. 1998. Reversal of phencyclidine effects by a group II metabotropic glutamate receptor agonist in rats. Science 281: 1349-1352.
53. Mohn AR, Gainetdinov RR, Caron MG, Koller BH. 1999. Mice with reduced NMDA receptor expression display behaviors related to schizophrenia. Cell 98: 427-436.
54. Najlerahim A, Harrison PJ, Barton AJ, Heffernan J, Pearson RC. 1990. Distribution of messenger RNAs encoding the enzymes glutaminase, aspartate aminotransferase and glutamic acid decarboxylase in rat brain. Mol Brain Res 7: 317-333.
55. Nihei MK, Desmond NL, McGlothan JL, Kuhlmann AC, Guilarte TR. 2000. N-methyl-D-aspartate receptor subunit changes are associated with lead-induced deficits of long-term potentiation and spatial learning. Neuroscience 99: 233-242.
56. Parent AS, Rasier G, Matagne V, Lomniczi A, Lebrethon MC, Gerard A, Ojeda SR, Bourguignon JP. 2008. Oxytocin facilitates female sexual maturation through a glia-to-neuron signaling pathway. Endocrinology 149: 1358-1365.
57. Patil ST, Zhang L, Martenyi F, Lowe SL, Jackson KA, Andreev BV, Avedisova AS, Bardenstein LM, Gurovich IY, Morozova MA, Mosolov SN, Neznanov NG, Reznik AM, Smulevich AB, Tochilov VA, Johnson BG, Monn JA, Schoepp DD. 2007. Activation of mGlu2/3 receptors as a new approach to treat schizophrenia: a randomized Phase 2 clinical trial. Nat Med 13: 1102-1107.
58. Petralia RS, Wang YX, Wenthold RJ. 1994. The NMDA receptor subunits NR2A and NR2B show histological and ultrastructural localization patterns similar to those of NR1. J Neurosci 14: 6102-6120.
59. Pfaffl MW, Tichopad A, Prgomet C, Neuvians TP. 2004. Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper-Excel-based tool using pair-wise correlations. Biotechnol Lett 26: 509-515.
60. Rao VR, Finkbeiner S. 2007. NMDA and AMPA receptors: old channels, new tricks. Trends Neurosci 30: 284-291.
61. Rozen S, Skaletsky H. 2000. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132: 365-386.
62. Saxe MD, Malleret G, Vronskaya S, Mendez I, Garcia AD, Sofroniew MV, Kandel ER, Hen R. 2007. Paradoxical influence of hippocampal neurogenesis on working memory. Proc Natl Acad Sci USA 104: 4642-4646.
63. Schilström B, Yaka R, Argilli E, Suvarna N, Schumann J, Chen BT, Carman M, Singh V, Mailliard WS, Ron D, Bonci A. 2006. Cocaine enhances NMDA receptor-mediated currents in ventral tegmental area cells via dopamine D5 receptor-dependent redistribution of NMDA receptors. J Neurosci 26: 8549-8558.
64. Schobel SA, Lewandowski NM, Corcoran CM, Moore H, Brown T, Malaspina D, Small SA. 2009. Differential targeting of the CA1 subfield of the hippocampal formation by schizophrenia and related psychotic disorders. Arch Gen Psychiatry 66: 938-946.
65. Shadach E, Gaisler I, Schiller D, Weiner I. 2000. The latent inhibition model dissociates between clozapine, haloperidol, and ritanserin. Neuropsychopharmacology 23: 151-161.
66. Shepherd JD, Huganir RL. 2007. The cell biology of synaptic plasticity: AMPA receptor trafficking. Annu Rev Cell Dev Biol 23: 613-643.
67. Sibille E, Su J, Leman S, Le Guisquet AM, Ibarguen-Vargas Y, Joeyen-Waldorf J, Glorioso C, Tseng GC, Pezzone M, Hen R, Belzung C. 2007. Lack of serotonin1B receptor expression leads to age-related motor dysfunction, early onset of brain molecular aging and reduced longevity. Mol Psychiatr 12: 1042-1056, 975.
68. 13C glucose infusion. J Neurochem 76: 975-989.
69. Sisk CL, Foster DL. 2004. The neural basis of puberty and adolescence. Nat Neurosci 7: 1040-1047.
70. Tani H, Dulla CG, Huguenard JR, Reimer RJ. 2010. Glutamine is required for persistent epileptiform activity in the disinhibited neocortical brain slice. J Neurosci 30: 1288-1300.
71. Wang X, Bao X, Pal R, Agbas A, Michaelis EK. 2010. Transcriptomic responses in mouse brain exposed to chronic excess of the neurotransmitter glutamate. BMC Genomics 11: 360.
72. Yang J, Woodhall GL, Jones RS. 2006. Tonic facilitation of glutamate release by presynaptic NR2B-containing NMDA receptors is increased in the entorhinal cortex of chronically epileptic rats. J Neurosci 26: 406-410.
73. Yano H, Ninan I, Zhang H, Milner TA, Arancio O, Chao MV. 2006. BDNF-mediated neurotransmission relies upon a myosin VI motor complex. Nat Neurosci 9: 1009-1018.