NMDA receptor subunit composition determines the polarity of leptin-induced synaptic plasticity

Neuropharmacology

Volumn 61, Issue 5-6, 2011, Pages 924-936

  Moult, Peter R ^a   Harvey, Jenni ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Leptin; MAPK; NMDA receptor; PI 3 kinase; Synaptic plasticity; Synaptic transmission

Indexed keywords

LEPTIN; MITOGEN ACTIVATED PROTEIN KINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; PHOSPHATIDYLINOSITOL 3 KINASE;

ADULTHOOD; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DRUG MECHANISM; ENZYME ACTIVITY; EVOKED RESPONSE; HORMONAL REGULATION; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MALE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; STIMULUS RESPONSE; SYNAPTIC POTENTIAL; SYNAPTIC TRANSMISSION;

AGE FACTORS; ANIMALS; BLOOD-BRAIN BARRIER; CELL POLARITY; ELECTRIC STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; GABA ANTAGONISTS; HIPPOCAMPUS; LEPTIN; LONG-TERM POTENTIATION; LONG-TERM SYNAPTIC DEPRESSION; MALE; NEURONAL PLASTICITY; PATCH-CLAMP TECHNIQUES; PHOSPHATIDYLINOSITOL 3-KINASES; PICROTOXIN; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 80051784497     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2011.06.021     Document Type: Article

References (60)

1. R.S. Ahima, C. Bjorbaek, S. Osei, and J.S. Flier Regulation of neuronal and glial proteins by leptin: implications for brain development Endocrinology 140 1999 2755 2762 (Pubitemid 32245155)
2. W.W. Anderson, and G.L. Collingridge Capabilities of the WinLTP data acquisition program extending beyond basic LTP experimental functions J. Neurosci. Methods 162 2007 346 356 (Pubitemid 46527917)
3. Y.P. Auberson, H. Allgeier, S. Bischoff, K. Lingenhoehl, R. Moretti, and M. Schmutz 5-Phosphonomethylquinoxalinediones as competitive NMDA receptor antagonists with a preference for the human 1A/2A, rather than 1A/2B receptor composition Bioorg. Med. Chem. Lett. 12 2002 1099 1102 (Pubitemid 34242811)
4. A. Barria, and R. Malinow Subunit-specific NMDA receptor trafficking to synapses Neuron 35 2002 345 353 (Pubitemid 34876735)
5. A. Barria, and R. Malinow NMDA receptor subunit composition controls synaptic plasticity by regulating binding to CaMKII Neuron 48 2005 289 301 (Pubitemid 41476362)
6. T.E. Bartlett, N.J. Bannister, V.J. Collett, S.L. Dargan, P.V. Massey, Z.A. Bortolotto, S.M. Fitzjohn, Z.I. Bashir, G.L. Collingridge, and D. Lodge Differential roles of NR2A and NR2B-containing NMDA receptors in LTP and LTD in the CA1 region of two-week old rat hippocampus Neuropharmacology 52 2007 60 70 (Pubitemid 46026825)
7. C. Bellone, and R.A. Nicoll Rapid bidirectional switching of synaptic NMDA receptors Neuron 55 2007 779 785 (Pubitemid 47321083)
8. T.V. Bliss, and G.L. Collingridge A synaptic model of memory: long-term potentiation in the hippocampus Nature 361 1993 31 39 (Pubitemid 23020772)
9. S.G. Bouret, S.J. Draper, and R.B. Simerly Trophic action of leptin on hypothalamic neurons that regulate feeding Science 304 2004 108 110 (Pubitemid 38451467)
10. M. Caprio, E. Fabbrini, A.M. Isidori, A. Aversa, and A. Fabbri Leptin in reproduction Trends Endocrinol. Metab. 12 2001 65 72 (Pubitemid 33714191)
11. D.A. Clayton, M.H. Mesches, E. Alvarez, P.C. Bickford, and M.D. Browning A hippocampal NR2B deficit can mimic age-related changes in long-term potentiation and spatial learning in the Fischer 344 rat J. Neurosci. 22 2002 3628 3637 (Pubitemid 37465767)
12. G.L. Collingridge, J.T. Isaac, and Y.T. Wang Receptor trafficking and synaptic plasticity Nat. Rev. Neurosci. 5 2004 952 962 (Pubitemid 39593358)
13. G.L. Collingridge, S. Peineau, J.G. Howland, and Y.T. Wang Long-term depression in the CNS Nat. Rev. Neurosci. 11 2010 459 473
14. S. Cull-Candy, S. Brickley, and M. Farrant NMDA receptor subunits: diversity, development and disease Curr. Opin. Neurobiol. 11 2001 327 335 (Pubitemid 32524098)
15. M. Durakoglugil, A.J. Irving, and J. Harvey Leptin induces a novel form of NMDA receptor-dependent long-term depression J. Neurochem. 95 2005 396 405 (Pubitemid 41457508)
16. N. Eikelis, G. Wiesner, G. Lambert, and M. Esler Brain leptin resistance in human obesity revisited Regul. Pept. 139 2007 45 51 (Pubitemid 46216477)
17. A.C. Flint, U.S. Maisch, J.H. Weishaupt, A.R. Kriegstein, and H. Monyer NR2A subunit expression shortens NMDA receptor synaptic currents in developing neocortex J. Neurosci. 17 1997 2469 2476 (Pubitemid 27137413)
18. K.A. Foster, N. McLaughlin, D. Edbauer, M. Phillips, A. Bolton, M. Constantine-Paton, and M. Sheng Distinct roles of NR2A and NR2B cytoplasmic tails in long-term potentiation J. Neurosci. 30 2010 2676 2685
19. P.A. Frizelle, P.E. Chen, and D.J. Wyllie Equilibrium constants for (R)-[(S)-1-(4-bromo-phenyl)-ethylamino]-(2,3-dioxo-1,2,3,4-tetrahydroquinoxalin- 5-yl)-methyl]-phosphonic acid (NVP-AAM077) acting at recombinant NR1/NR2A and NR1/NR2B N-methyl-d-aspartate receptors: Implications for studies of synaptic transmission Mol. Pharmacol. 70 2006 1022 1032 (Pubitemid 44268459)
20. F. Gardoni, D. Mauceri, M. Malinverno, F. Polli, C. Costa, A. Tozzi, S. Siliquini, B. Picconi, F. Cattabeni, P. Calabresi, and M. Di Luca Decreased NR2B subunit synaptic levels cause impaired long-term potentiation but not long-term depression J. Neurosci. 29 3 2009 669 677
21. W.H. Gispen, and G.J. Biessels Cognition and synaptic plasticity in diabetes mellitus Trends Neurosci. 23 2000 542 549
22. J. Harvey Leptin: a diverse regulator of neuronal function J. Neurochem. 100 2007 307 313 (Pubitemid 46010992)
23. J. Harvey, N. Solovyova, and A. Irving Leptin and its role in hippocampal synaptic plasticity Prog. Lipid Res. 45 2006 369 378
24. C.C. Huang, C.C. Lee, and K.S. Hsu An investigation into signal transduction mechanisms involved in insulin-induced long-term depression in the CA1 region of the hippocampus J. Neurochem. 89 2004 217 231
25. A.J. Irving, L. Wallace, D. Durakoglugil, and J. Harvey Leptin enhances NR2B-mediated N-methyl-d-aspartate responses via a mitogen-activated protein kinase-dependent process in cerebellar granule cells Neuroscience 138 2006 1137 1148 (Pubitemid 43363532)
26. D.M. Kullmann Amplitude fluctuations of dual-component EPSCs in hippocampal pyramidal cells: implications for long-term potentiation Neuron 12 1994 1111 1120 (Pubitemid 24178202)
27. T. Kutsuwada, K. Sakimura, T. Manabe, C. Takayama, N. Katakura, E. Kushiya, R. Natsume, M. Watanabe, Y. Inoue, and T. Yagi Impairment of suckling response, trigeminal neuronal pattern formation, and hippocampal LTD in NMDA receptor epsilon 2 subunit mutant mice Neuron 16 1996 333 344
28. X.L. Li, S. Aou, Y. Oomura, N. Hori, K. Fukunaga, and T. Hori Impairment of long-term potentiation and spatial memory in leptin receptor-deficient rodents Neuroscience 113 2002 607 615 (Pubitemid 34874684)
29. W. Lieb, A.S. Beiser, R.S. Vasan, Z.S. Tan, R. Au, T.B. Harris, R. Roubenoff, S. Auerbach, C. DeCarli, and P.A. Wolf Association of plasma leptin levels with incident Alzheimer disease and MRI measures of brain aging JAMA 302 2009 2565 2572
30. L. Liu, T.P. Wong, M.F. Pozza, K. Lingenhoehl, Y. Wang, M. Sheng, Y.P. Auberson, and Y.T. Wang Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity Science 304 2004 1021 1024 (Pubitemid 38638102)
31. J.M. Loftis, and A. Janowsky The N-methyl-d-aspartate receptor subunit NR2B: localization, functional properties, regulation, and clinical implications Pharmacol. Ther. 97 2003 55 85 (Pubitemid 35477804)
32. H.Y. Man, J.W. Lin, W.H. Ju, G. Ahmadian, L. Liu, L.E. Becker, M. Sheng, and Y.T. Wang Regulation of AMPA receptor-mediated synaptic transmission by clathrin-dependent receptor internalization Neuron 25 2000 649 662
33. H.Y. Man, Q. Wang, W.Y. Lu, W. Ju, G. Ahmadian, L. Liu, S. D'Souza, T.P. Wong, C. Taghibiglou, and J. Lu Activation of PI3-kinase is required for AMPA receptor insertion during LTP of mEPSCs in cultured hippocampal neurons Neuron 38 2003 611 624 (Pubitemid 36645035)
34. P.V. Massey, B.E. Johnson, P.R. Moult, Y.P. Auberson, M.W. Brown, E. Molnar, G.L. Collingridge, and Z.I. Bashir Differential roles of NR2A and NR2B-containing NMDA receptors in cortical long-term potentiation and long-term depression J. Neurosci. 24 2004 7821 7828 (Pubitemid 39215685)
35. B. McEwen Estrogen actions throughout the brain Recent Prog. Horm. Res. 57 2002 357 384
36. J.G. Mercer, N. Hoggard, L.M. Williams, C.B. Lawrence, L.T. Hannah, and P. Trayhurn Localization of leptin receptor mRNA and the long form splice variant (Ob-Rb) in mouse hypothalamus and adjacent brain regions by in situ hybridization FEBS Lett. 387 1996 113 116
37. H. Monyer, N. Burnashev, D.J. Laurie, B. Sakmann, and P.H. Seeburg Developmental and regional expression in the rat brain and functional properties of four NMDA receptors Neuron 12 1994 529 540 (Pubitemid 24100885)
38. B. Morash, A. Li, P.R. Murphy, M. Wilkinson, and E. Ur Leptin gene expression in the brain and pituitary gland Endocrinology 140 1999 5995 5998 (Pubitemid 30645391)
39. W. Morishita, W. Lu, G.B. Smith, R.A. Nicoll, M.F. Bear, and R.C. Malenka Activation of NR2B-containing NMDA receptors is not required for NMDA receptor-dependent long-term depression Neuropharmacology 52 2007 71 76 (Pubitemid 46026821)
40. P.R. Moult, A. Cross, S.D. Santos, A.L. Carvalho, Y. Lindsay, C.N. Connolly, A.J. Irving, N.R. Leslie, and J. Harvey Leptin regulates AMPA receptor trafficking via PTEN inhibition J. Neurosci. 30 2010 4088 4101
41. P.R. Moult, B. Milojkovic, and J. Harvey Leptin reverses long-term potentiation at hippocampal CA1 synapses J. Neurochem. 108 2009 685 696
42. J. Neyton, and P. Paoletti Relating NMDA receptor function to receptor subunit composition: limitations of the pharmacological approach J. Neurosci. 26 2006 1331 1333 (Pubitemid 43237003)
43. D. O'Malley, N. MacDonald, S. Mizielinska, C.N. Connolly, A.J. Irving, and J. Harvey Leptin promotes rapid dynamic changes in hippocampal dendritic morphology Mol. Cell Neurosci. 35 2007 559 572 (Pubitemid 47193112)
44. K. Plant, K.A. Pelkey, Z.A. Bortolotto, D. Morita, A. Terashima, C.J. McBain, G.L. Collingridge, and J.T. Isaac Transient incorporation of native GluR2-lacking AMPA receptors during hippocampal long-term potentiation Nat. Neurosci. 9 2006 602 604 (Pubitemid 44012255)
45. D.A. Power, J. Noel, R. Collins, and D. O'Neill Circulating leptin levels and weight loss in Alzheimer's disease patients Dement Geriatr. Cogn. Disord. 12 2001 167 170 (Pubitemid 32149724)
46. E.M. Quinlan, D.H. Olstein, and M.F. Bear Bidirectional, experience-dependent regulation of N-methyl-d-aspartate receptor subunit composition in the rat visual cortex during postnatal development Proc. Natl. Acad. Sci. U.S.A. 96 1999 12876 12880 (Pubitemid 29513596)
47. G. Rumbaugh, and S. Vicini Distinct synaptic and extrasynaptic NMDA receptors in developing cerebellar granule neurons J. Neurosci. 19 1999 10603 10610 (Pubitemid 30235707)
48. L.J. Shanley, A.J. Irving, and J. Harvey Leptin enhances NMDA receptor function and modulates hippocampal synaptic plasticity J. Neurosci. 21 2001 RC186
49. L.J. Shanley, D. O'Malley, A.J. Irving, M.L. Ashford, and J. Harvey Leptin inhibits epileptiform-like activity in rat hippocampal neurones via PI 3-kinase-driven activation of BK channels J. Physiol. 545 2002 933 944 (Pubitemid 36024431)
50. M. Sheng, J. Cummings, L.A. Roldan, Y.N. Jan, and L.Y. Jan Changing subunit composition of heteromeric NMDA receptors during development of rat cortex Nature 368 1994 144 147 (Pubitemid 24101524)
51. N. Solovyova, P.R. Moult, B. Milojkovic, J.J. Lambert, and J. Harvey Bi-directional modulation of fast inhibitory synaptic transmission by leptin J. Neurochem. 108 2009 190 201
52. B.M. Spiegelman, and J.S. Flier Obesity and the regulation of energy balance Cell 104 2001 531 543 (Pubitemid 32201948)
53. C.M. Steppan, and A.G. Swick A role for leptin in brain development Biochem. Biophys. Res. Commun. 256 1999 600 602 (Pubitemid 29301152)
54. S. Takeda, and G. Karsenty Central control of bone formation J. Bone Miner. Metab. 19 2001 195 198 (Pubitemid 32499812)
55. Y.P. Tang, E. Shimizu, G.R. Dube, C. Rampon, G.A. Kerchner, M. Zhuo, G. Liu, and J.Z. Tsien Genetic enhancement of learning and memory in mice Nature 401 1999 63 69
56. L.P. van der Heide, A. Kamal, A. Artola, W.H. Gispen, and G.M. Ramakers Insulin modulates hippocampal activity-dependent synaptic plasticity in a N-methyl-d-aspartate receptor and phosphatidyl-inositol-3-kinase-dependent manner J. Neurochem. 94 2005 1158 1166 (Pubitemid 41170602)
57. S. Vicini, J.F. Wang, J.H. Li, W.J. Zhu, Y.H. Wang, J.H. Luo, B.B. Wolfe, and D.R. Grayson Functional and pharmacological differences between recombinant N-methyl-d-aspartate receptors J. Neurophysiol. 79 1998 555 566 (Pubitemid 28095877)
58. M.J. Wayner, D.L. Armstrong, C.F. Phelix, and Y. Oomura Orexin-A (Hypocretin-1) and leptin enhance LTP in the dentate gyrus of rats in vivo Peptides 25 2004 991 996 (Pubitemid 38760287)
59. K. Williams Ifenprodil discriminates subtypes of the N-methyl-d-aspartate receptor: selectivity and mechanisms at recombinant heteromeric receptors Mol. Pharmacol. 44 1993 851 859 (Pubitemid 23317299)
60. L. Xu, N. Rensing, X.F. Yang, H.X. Zhang, L.L. Thio, S.M. Rothman, A.E. Weisenfeld, M. Wong, and K.A. Yamada Leptin inhibits 4-aminopyridine- and pentylenetetrazole-induced seizures and AMPAR-mediated synaptic transmission in rodents J. Clin. Invest. 118 2008 272 280