N-methyl-D-aspartate receptor mechanosensitivity is governed by C terminus of NR2B subunit

Journal of Biological Chemistry

Volumn 287, Issue 6, 2012, Pages 4348-4359

  Singh, Pallab ^c   Doshi, Shachee ^a   Spaethling, Jennifer M ^c   Hockenberry, Adam J ^c   Patel, Tapan P ^c   Geddes Klein, Donna M ^c   Lynch, David R ^a,b   Meaney, David F ^c  

^a CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

C TERMINUS; CORTICAL NEURONS; HEK293 CELLS; MECHANICAL STRETCH; MECHANOSENSITIVITY; N METHYL D ASPARTATE RECEPTOR; NEUROLOGICAL SIGNALING; NEURONAL RESPONSE; PHOSPHORYLATION SITES; POINT MUTATIONS; TRAUMATIC BRAIN INJURIES;

PHOSPHORYLATION;

BRAIN;

N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; PROTEIN KINASE C; SERINE;

ARTICLE; BRAIN CELL; CARBOXY TERMINAL SEQUENCE; CELL ACTIVITY; CELL STRAIN HEK293; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME REGULATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MECHANOSENSITIVITY; PHYSICAL SENSITIVITY; POINT MUTATION; PRIORITY JOURNAL; STRETCHING;

ANIMALS; BRAIN INJURIES; HEK293 CELLS; HUMANS; MECHANOTRANSDUCTION, CELLULAR; NEURONS; POINT MUTATION; PROTEIN KINASE C; RATS; RECEPTORS, N-METHYL-D-ASPARTATE; TRANSFECTION;

EID: 84856756653     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.253740     Document Type: Article

References (75)

1. Hardingham, G. E., Fukunaga, Y., and Bading, H. (2002) Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat. Neurosci. 5, 405-414 (Pubitemid 34454245)
2. Hetman, M., and Kharebava, G. (2006) Survival signaling pathways activated by NMDA receptors. Curr. Top Med. Chem. 6, 787-799
3. Ikonomidou, C., Bosch, F., Miksa, M., Bittigau, P., Vöckler, J., Dikranian, K., Tenkova, T. I., Stefovska, V., Turski, L., and Olney, J. W. (1999) Blockade of NMDA receptors and apoptotic neurodegeneration in the developing brain. Science 283, 70-74 (Pubitemid 29044848)
4. Cull-Candy, S. G., and Leszkiewicz, D. N. (2004) Role of distinct NMDA receptor subtypes at central synapses. Sci. STKE 2004, re16
5. Dingledine, R., Borges, K., Bowie, D., and Traynelis, S. F. (1999) The glutamate receptor ion channels. Pharmacol. Rev. 51, 7-61 (Pubitemid 29113865)
6. Monyer, H., Burnashev, N., Laurie, D. J., Sakmann, B., and Seeburg, P. H. (1994) Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12, 529-540 (Pubitemid 24100885)
7. Liu, X. B., Murray, K. D., and Jones, E. G. (2004) Switching of NMDA receptor 2A and 2B subunits at thalamic and cortical synapses during early postnatal development. J. Neurosci. 24, 8885-8895 (Pubitemid 39362984)
8. Williams, K., Russell, S. L., Shen, Y. M., and Molinoff, P. B. (1993) Developmental switch in the expression of NMDA receptors occurs in vivo and in vitro. Neuron 10, 267-278 (Pubitemid 23079548)
9. Jin, S. X., and Feig, L. A. (2010) Long-term potentiation in the CA1 hippocampus induced by NR2A subunit-containing NMDA glutamate receptors is mediated by Ras-GRF2/Erk Map kinase signaling. PLoS One 5, e11732
10. Kim, M. J., Dunah, A. W., Wang, Y. T., and Sheng, M. (2005) Differential roles of NR2A- and NR2B-containing NMDA receptors in Ras-ERK signaling and AMPA receptor trafficking. Neuron 46, 745-760 (Pubitemid 40733130)
11. Köhr, G., Jensen, V., Koester, H. J., Mihaljevic, A. L., Utvik, J. K., Kvello, A., Ottersen, O. P., Seeburg, P. H., Sprengel, R., and Hvalby, Ø. (2003) Intracellular domains of NMDA receptor subtypes are determinants for long-term potentiation induction. J. Neurosci. 23, 10791-10799
12. Li, S., Tian, X., Hartley, D. M., and Feig, L. A. (2006) Distinct roles for Ras-guanine nucleotide-releasing factor 1 (Ras-GRF1) and Ras-GRF2 in the induction of long-term potentiation and long-term depression. J. Neurosci. 26, 1721-1729 (Pubitemid 43236984)
13. Arundine, M., and Tymianski, M. (2004) Molecular mechanisms of glutamate-dependent neurodegeneration in ischemia and traumatic brain injury. Cell Mol. Life Sci. 61, 657-668 (Pubitemid 38446410)
14. Hardingham, G. E., and Bading, H. (2010) Synaptic versus extrasynaptic NMDA receptor signalling. Implications for neurodegenerative disorders. Nat. Rev. Neurosci. 11, 682-696
15. Lynch, D. R., and Guttmann, R. P. (2002) Excitotoxicity. Perspectives based on N-methyl-D-aspartate receptor subtypes. J. Pharmacol. Exp. Ther. 300, 717-723 (Pubitemid 34164971)
16. Waxman, E. A., and Lynch, D. R. (2005) N-Methyl-D-aspartate receptor subtypes. Multiple roles in excitotoxicity and neurological disease. Neuroscientist 11, 37-49 (Pubitemid 40223089)
17. Ikonomidou, C., Stefovska, V., and Turski, L. (2000) Neuronal death enhanced by N-methyl-D-aspartate antagonists. Proc. Natl. Acad. Sci. U.S.A. 97, 12885-12890
18. Liu, L., Wong, T. P., Pozza, M. F., Lingenhoehl, K., Wang, Y., Sheng, M., Auberson, Y. P., and Wang, Y. T. (2004) Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science 304, 1021-1024 (Pubitemid 38638102)
19. Massey, P. V., Johnson, B. E., Moult, P. R., Auberson, Y. P., Brown, M. W., Molnar, E., Collingridge, G. L., and Bashir, Z. I. (2004) Differential roles of NR2A and NR2B-containing NMDA receptors in cortical long-term potentiation and long-term depression. J. Neurosci. 24, 7821-7828 (Pubitemid 39215685)
20. Ewald, R. C., Van Keuren-Jensen, K. R., Aizenman, C. D., and Cline, H. T. (2008) Roles of NR2A and NR2B in the development of dendritic arbor morphology in vivo. J. Neurosci. 28, 850-861 (Pubitemid 351159000)
21. DeRidder, M. N., Simon, M. J., Siman, R., Auberson, Y. P., Raghupathi, R., and Meaney, D. F. (2006) Traumatic mechanical injury to the hippocampus in vitro causes regional caspase-3 and calpain activation that is influenced by NMDA receptor subunit composition. Neurobiol. Dis. 22, 165-176
22. Kinney, J. W., Davis, C. N., Tabarean, I., Conti, B., Bartfai, T., and Behrens, M. M. (2006)Aspecific role for NR2A-containing NMDA receptors in the maintenance of parvalbumin and GAD67 immunoreactivity in cultured interneurons. J. Neurosci. 26, 1604-1615 (Pubitemid 43237031)
23. Zhou, M., and Baudry, M. (2006) Developmental changes in NMDA neurotoxicity reflect developmental changes in subunit composition of NMDA receptors. J. Neurosci. 26, 2956-2963
24. Chen, M., Lu, T. J., Chen, X. J., Zhou, Y., Chen, Q., Feng, X. Y., Xu, L., Duan, W. H., and Xiong, Z. Q. (2008) Differential roles of NMDA receptor subtypes in ischemic neuronal cell death and ischemic tolerance. Stroke 39, 3042-3048
25. Gogas, K. R. (2006) Glutamate-based therapeutic approaches. NR2B receptor antagonists. Curr. Opin. Pharmacol. 6, 68-74
26. Okiyama, K., Smith, D. H., White, W. F., Richter, K., and McIntosh, T. K. (1997) Effects of the novel NMDA antagonists CP-98,113, CP-101,581 and CP-101,606 on cognitive function and regional cerebral edema following experimental brain injury in the rat. J. Neurotrauma 14, 211-222 (Pubitemid 27205177)
27. von Engelhardt, J., Coserea, I., Pawlak, V., Fuchs, E. C., Köhr, G., Seeburg, P. H., and Monyer, H. (2007) Excitotoxicity in vitro by NR2A- and NR2B-containing NMDA receptors. Neuropharmacology 53, 10-17 (Pubitemid 47125951)
28. Faden, A. I., Demediuk, P., Panter, S. S., and Vink, R. (1989) The role of excitatory amino acids and NMDA receptors in traumatic brain injury. Science 244, 798-800 (Pubitemid 19163864)
29. Geddes-Klein, D. M., Serbest, G., Mesfin, M. N., Cohen, A. S., and Meaney, D. F. (2006) Pharmacologically induced calcium oscillations protect neurons from increases in cytosolic calcium after trauma. J. Neurochem. 97, 462-474
30. McIntosh, T. K., Vink, R., Soares, H., Hayes, R., and Simon, R. (1990) Effect of noncompetitive blockade of N-methyl-D-aspartate receptors on the neurochemical sequelae of experimental brain injury. J. Neurochem. 55, 1170-1179
31. Shapira, Y., Yadid, G., Cotev, S., Niska, A., and Shohami, E. (1990) Protective effect of MK801 in experimental brain injury. J. Neurotrauma 7, 131-139 (Pubitemid 20371632)
32. Smith, D. H., Okiyama, K., Gennarelli, T. A., and McIntosh, T. K. (1993) Magnesium and ketamine attenuate cognitive dysfunction following experimental brain injury. Neurosci. Lett. 157, 211-214 (Pubitemid 23245531)
33. Bullock, R., Zauner, A., Myseros, J. S., Marmarou, A., Woodward, J. J., and Young, H. F. (1995) Evidence for prolonged release of excitatory amino acids in severe human head trauma. Relationship to clinical events. Ann. N.Y. Acad. Sci. 765, 290-297 (Pubitemid 26136254)
34. Nilsson, P., Ronne-Engström, E., Flink, R., Ungerstedt, U., Carlson, H., and Hillered, L. (1994) Epileptic seizure activity in the acute phase following cortical impact trauma in rat. Brain Res. 637, 227-232 (Pubitemid 24061052)
35. Palmer, A. M., Marion, D. W., Botscheller, M. L., Swedlow, P. E., Styren, S. D., and DeKosky, S. T. (1993) Traumatic brain injury-induced excitotoxicity assessed in a controlled cortical impact model. J. Neurochem. 61, 2015-2024 (Pubitemid 23354056)
36. 2+ blockade of NMDA current in mechanically injured neurons. Science 274, 1921-1923
37. Liu, Y., Wong, T. P., Aarts, M., Rooyakkers, A., Liu, L., Lai, T. W., Wu, D. C., Lu, J., Tymianski, M., Craig, A. M., and Wang, Y. T. (2007) NMDA receptor subunits have differential roles in mediating excitotoxic neuronal death both in vitro and in vivo. J. Neurosci. 27, 2846-2857 (Pubitemid 46438991)
38. Boeckman, F. A., and Aizenman, E. (1994) Stable transfection of the NR1 subunit in Chinese hamster ovary cells fails to produce a functional N-methyl-D-aspartate receptor. Neurosci. Lett. 173, 189-192
39. Boeckman, F. A., and Aizenman, E. (1996) Pharmacological properties of acquired excitotoxicity in Chinese hamster ovary cells transfected with N-methyl-D-aspartate receptor subunits. J. Pharmacol. Exp. Ther. 279, 515-523 (Pubitemid 27166821)
40. Gallagher, M. J., Huang, H., Pritchett, D. B., and Lynch, D. R. (1996) Interactions between ifenprodil and the NR2B subunit of the N-methyl-D-aspartate receptor. J. Biol. Chem. 271, 9603-9611
41. Wu, H. Y., Hsu, F. C., Gleichman, A. J., Baconguis, I., Coulter, D. A., and Lynch, D. R. (2007) Fyn-mediated phosphorylation of NR2B Tyr-1336 controls calpain-mediated NR2B cleavage in neurons and heterologous systems. J. Biol. Chem. 282, 20075-20087 (Pubitemid 47100033)
42. Lusardi, T. A., Rangan, J., Sun, D., Smith, D. H., and Meaney, D. F. (2004) A device to study the initiation and propagation of calcium transients in cultured neurons after mechanical stretch. Ann. Biomed. Eng. 32, 1546-1558 (Pubitemid 40044500)
43. Hatton, C. J., and Paoletti, P. (2005) Modulation of triheteromeric NMDA receptors by N-terminal domain ligands. Neuron 46, 261-274 (Pubitemid 40545781)
44. Monyer, H., Sprengel, R., Schoepfer, R., Herb, A., Higuchi, M., Lomeli, H., Burnashev, N., Sakmann, B., and Seeburg, P. H. (1992) Heteromeric NMDA receptors. Molecular and functional distinction of subtypes. Science 256, 1217-1221
45. Foster, K. A., McLaughlin, N., Edbauer, D., Phillips, M., Bolton, A., Constantine-Paton, M., and Sheng, M. (2010) Distinct roles of NR2A and NR2B cytoplasmic tails in long-term potentiation. J. Neurosci. 30, 2676-2685
46. Krapivinsky, G., Krapivinsky, L., Manasian, Y., Ivanov, A., Tyzio, R., Pellegrino, C., Ben-Ari, Y., Clapham, D. E., and Medina, I. (2003) The NMDA receptor is coupled to the ERK pathway by a direct interaction between NR2B and RasGRF1. Neuron 40, 775-784 (Pubitemid 37431037)
47. Wechsler, A., and Teichberg, V. I. (1998) Brain spectrin binding to the NMDA receptor is regulated by phosphorylation, calcium and calmodulin. EMBO J. 17, 3931-3939 (Pubitemid 28333979)
48. Wyszynski, M., Lin, J., Rao, A., Nigh, E., Beggs, A. H., Craig, A. M., and Sheng, M. (1997) Competitive binding of α-actinin and calmodulin to the NMDA receptor. Nature 385, 439-442 (Pubitemid 27065929)
49. Chen, B. S., and Roche, K. W. (2007) Regulation of NMDA receptors by phosphorylation. Neuropharmacology 53, 362-368
50. Casado, M., and Ascher, P. (1998) Opposite modulation of NMDA receptors by lysophospholipids and arachidonic acid. Common features with mechanosensitivity. J. Physiol. 513, 317-330 (Pubitemid 28562951)
51. Paoletti, P., and Ascher, P. (1994) Mechanosensitivity of NMDA receptors in cultured mouse central neurons. Neuron 13, 645-655 (Pubitemid 24300169)
52. Grant, E. R., Bacskai, B. J., Anegawa, N. J., Pleasure, D. E., and Lynch, D. R. (1998) Opposing contributions of NR1 and NR2 to protein kinase C modulation of NMDA receptors. J. Neurochem. 71, 1471-1481 (Pubitemid 28443019)
53. Guttmann, R. P., Baker, D. L., Seifert, K. M., Cohen, A. S., Coulter, D. A., and Lynch, D. R. (2001) Specific proteolysis of the NR2 subunit at multiple sites by calpain. J. Neurochem. 78, 1083-1093 (Pubitemid 32823157)
54. Kendrick, S. J., Lynch, D. R., and Pritchett, D. B. (1996) Characterization of glutamate binding sites in receptors assembled from transfected NMDA receptor subunits. J. Neurochem. 67, 608-616 (Pubitemid 26255655)
55. Lynch, D. R., and Guttmann, R. P. (2001) NMDA receptor pharmacology. Perspectives from molecular biology. Curr. Drug Targets 2, 215-231 (Pubitemid 32821467)
56. Neyton, J., and Paoletti, P. (2006) Relating NMDA receptor function to receptor subunit composition. Limitations of the pharmacological approach. J. Neurosci. 26, 1331-1333 (Pubitemid 43237003)
57. Ehlers, M. D., Fung, E. T., O'Brien, R. J., and Huganir, R. L. (1998) Splice variant-specific interaction of the NMDA receptor subunit NR1 with neuronal intermediate filaments. J. Neurosci. 18, 720-730 (Pubitemid 28041908)
58. Matsuda, S., and Hirai, H. (1999) The clustering of NMDA receptor NR1 subunit is regulated by the interaction between the C-terminal exon cassettes and the cytoskeleton. Neurosci. Res. 34, 157-163 (Pubitemid 29421720)
59. Kashiwagi, K., Masuko, T., Nguyen, C. D., Kuno, T., Tanaka, I., Igarashi, K., and Williams, K. (2002) Channel blockers acting at N-methyl-D-aspartate receptors. Differential effects of mutations in the vestibule and ion channel pore. Mol. Pharmacol. 61, 533-545 (Pubitemid 34171919)
60. Jones, M. L., and Leonard, J. P. (2005) PKC site mutations reveal differential modulation by insulin of NMDA receptors containing NR2A or NR2B subunits. J. Neurochem. 92, 1431-1438 (Pubitemid 40389212)
61. Salter, M. W., and Kalia, L. V. (2004) Src kinases. A hub for NMDA receptor regulation. Nat. Rev. Neurosci. 5, 317-328 (Pubitemid 38478658)
62. Liao, G. Y., Wagner, D. A., Hsu, M. H., and Leonard, J. P. (2001) Evidence for direct protein kinase-C mediated modulation of N-methyl-D-aspartate receptor current. Mol. Pharmacol. 59, 960-964 (Pubitemid 32381573)
63. 2+ block of NMDA-receptor channels as a mechanism of modulation. Nature 356, 521-523
64. Zohar, O., Lavy, R., Zi, X., Nelson, T. J., Hongpaisan, J., Pick, C. G., and Alkon, D. L. (2011) PKC activator therapeutic for mild traumatic brain injury in mice. Neurobiol. Dis. 41, 329-337
65. Nelson, T. J., Sun, M. K., Hongpaisan, J., and Alkon, D. L. (2008) Insulin, PKC signaling pathways and synaptic remodeling during memory storage and neuronal repair. Eur. J. Pharmacol. 585, 76-87
66. Erreger, K., Dravid, S. M., Banke, T. G., Wyllie, D. J., and Traynelis, S. F. (2005) Subunit-specific gating controls rat NR1/NR2A and NR1/NR2B NMDA channel kinetics and synaptic signalling profiles. J. Physiol. 563, 345-358 (Pubitemid 40360896)
67. Santucci, D. M., and Raghavachari, S. (2008) The effects of NR2 subunit-dependent NMDA receptor kinetics on synaptic transmission and CaMKII activation. PLoS Comput. Biol. 4, e1000208
68. Singh, P., Hockenberry, A. J., Tiruvadi, V. R., and Meaney, D. F. (2011) Computational investigation of the changing patterns of subtype specific NMDA receptor activation during physiological glutamatergic neurotransmission. PLoS Comput. Biol. 7, e1002106
69. Sattler, R., Xiong, Z., Lu, W. Y., Hafner, M., MacDonald, J. F., and Tymianski, M. (1999) Specific coupling of NMDA receptor activation to nitric oxide neurotoxicity by PSD-95 protein. Science 284, 1845-1848
70. Rao, V. L., Dogan, A., Todd, K. G., Bowen, K. K., and Dempsey, R. J. (2001) Neuroprotection by memantine, a non-competitive NMDA receptor antagonist after traumatic brain injury in rats. Brain Res. 911, 96-100 (Pubitemid 32728243)
71. Spaethling, J. M., Geddes-Klein, D. M., Miller, W. J., von Reyn, C. R., Singh, P., Mesfin, M., Bernstein, S. J., and Meaney, D. F. (2007) Linking impact to cellular and molecular sequelae of CNS injury. Modeling in vivo complexity with in vitro simplicity. Prog. Brain Res. 161, 27-39 (Pubitemid 47017398)
72. Dempsey, R. J., Bakaya, M. K., and Doan, A. (2000) Attenuation of brain edema, blood-brain barrier breakdown, and injury volume by ifenprodil, a polyamine-site N-methyl-D-aspartate receptor antagonist, after experimental traumatic brain injury in rats. Neurosurgery 47, 399-406 (Pubitemid 32049346)
73. Al-Hallaq, R. A., Conrads, T. P., Veenstra, T. D., and Wenthold, R. J. (2007) NMDA di-heteromeric receptor populations and associated proteins in rat hippocampus. J. Neurosci. 27, 8334-8343 (Pubitemid 47219608)
74. Rauner, C., and Köhr, G. (2011) Triheteromeric NR1/NR2A/NR2B receptors constitute the major N-methyl-D-aspartate receptor population in adult hippocampal synapses. J. Biol. Chem. 286, 7558-7566
75. Tovar, K. R., and Westbrook, G. L. (1999) The incorporation of NMDA receptors with a distinct subunit composition at nascent hippocampal synapses in vitro. J. Neurosci. 19, 4180-4188 (Pubitemid 29222289)