Biphasic coupling of neuronal nitric oxide synthase phosphorylation to the NMDA receptor regulates AMPA receptor trafficking and neuronal cell death

Journal of Neuroscience

Volumn 27, Issue 13, 2007, Pages 3445-3455

  Rameau, Gerald A ^a   Tukey, David S ^b   Garcin Hosfield, Elsa D ^c   Titcombe, Roseann F ^b   Misra, Charu ^b   Khatri, Latika ^b   Getzoff, Elizabeth D ^c   Ziff, Edward B ^b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

AMPA receptor; Dephosphorylation; Excitotoxicity; Neuronal nitric oxide synthase; NMDA receptor; nNOS; Phosphorylation

Indexed keywords

AMPA RECEPTOR; CALMODULIN; GLUTAMATE RECEPTOR 2; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NITRIC OXIDE SYNTHASE; PHOSPHOPEPTIDE; PROTEIN KINASE B;

ANIMAL CELL; ANTIBODY SPECIFICITY; ARTICLE; BRAIN CELL; CELL DEATH; DEPHOSPHORYLATION; ELECTRON TRANSPORT; EMBRYO; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; EXCITOTOXICITY; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; RAT; STIMULUS RESPONSE;

ANIMALS; CELL DEATH; CELLS, CULTURED; CEREBRAL CORTEX; GLUTAMIC ACID; HIPPOCAMPUS; NEURONS; NITRIC OXIDE SYNTHASE; PHOSPHORYLATION; PROTEIN TRANSPORT; RATS; RECEPTORS, AMPA; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 34047148363     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4799-06.2007     Document Type: Article

References (67)

1. Adachi N, Lei B, Soutani M, Arai T (2000) Different roles of neuronal and endothelial nitric oxide synthases on ischemic nitric oxide production in gerbil striatum. Neurosci Lett 288:151-154.
2. Adak S, Santolini J, Tikunova S, Wang Q, Johnson JD, Stuehr DJ (2001a) Neuronal nitric-oxide synthase mutant (Ser-1412 → Asp) demonstrates surprising connections between heme reduction, NO complex formation, and catalysis. J Biol Chem 276:1244-1252.
3. Adak S, Aulak KS, Stuehr DJ (2001b) Chimeras of nitric-oxide synthase types I and III establish fundamental correlates between heme reduction, heme-NO complex formation, and catalytic activity. J Biol Chem 276:23246-23252.
4. Aizenman E, Brimecombe JC, Potthoff WK, Rosenberg PA (1998) Why is the role of nitric oxide in NMDA receptor function and dysfunction so controversial? Prog Brain Res 118:53-71.
5. Ankarcrona M, Dypbukt JM, Bonfoco E, Zhivotovsky B, Orrenius S, Lipton SA, Nicotera P (1995) Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 15:961-973.
6. Ayata C, Ayata G, Hara H, Matthews RT, Beal MF, Ferrante RJ, Endres M, Kim A, Christie RH, Waeber C, Huang PL, Hyman BT, Moskowitz MA (1997) Mechanisms of reduced striatal NMDA excitotoxicity in type I nitric oxide synthase knock-out mice. J Neurosci 17:6908-6917.
7. Balazs R, Hack N, Jorgensen OS (1988) Stimulation of the N-methyl-D-aspartate receptor has a trophic effect on differentiating cerebellar granule cells. Neurosci Lett 87:80-86.
8. Balda MA, Anderson KL, Itzhak Y (2006) Adolescent and adult responsiveness to the incentive value of cocaine reward in mice: role of neuronal nitric oxide synthase (nNOS) gene. Neuropharmacology 51:341-349.
9. Bambrick LL, Yarowsky PJ, Krueger BK (1995) Glutamate as a hippocampal neuron survival factor: an inherited defect in the trisomy 16 mouse. Proc Natl Acad Sci USA 92:9692-9696.
10. Bredt DS (2003) Nitric oxide signaling specificity-the heart of the problem. J Cell Sci 116:9-15.
11. Bredt DS, Snyder SH (1989) Nitric oxide mediates glutamate-linked enhancement of cGMP levels in the cerebellum. Proc Natl Acad Sci USA 86:9030-9033.
12. Choi DW (1994) Glutamate receptors and the induction of excitotoxic neuronal death. Prog Brain Res 100:47-51.
13. Christopherson KS, Hillier BJ, Lim WA, Bredt DS (1999) PSD-95 assembles a ternary complex with the N-methyl-D-aspartic acid receptor and a bivalent neuronal NO synthase PDZ domain. J Biol Chem 274:27467-27473.
14. Chung KK, Thomas B, Li X, Pletnikova O, Troncoso JC, Marsh L, Dawson VL, Dawson TM (2004) S-nitrosylation of parkin regulates ubiquitination and compromises parkin's protective function. Science 304:1328-1331.
15. Cohen PT (2002) Protein phosphatase 1 - targeted in many directions. J Cell Sci 115:241-256.
16. Dawson VL, Kizushi VM, Huang PL, Snyder SH, Dawson TM (1996) Resistance to neurotoxicity in cortical cultures from neuronal nitric oxide synthase-deficient mice. J Neurosci 16:2479-2487.
17. Dell'Acqua ML, Smith KE, Gorski JA, Horne EA, Gibson ES, Gomez LL (2006) Regulation of neuronal PKA signaling through AKAP targeting dynamics. Eur J Cell Biol 85:627-633.
18. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM (1999) Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 399:601-605.
19. Eliasson MJ, Huang Z, Ferrante RJ, Sasamata M, Molliver ME, Snyder SH, Moskowitz MA (1999) Neuronal nitric oxide synthase activation and peroxynitrite formation in ischemic stroke linked to neural damage. J Neurosci 19:5910-5918.
20. Estevez AG, Crow JP, Sampson JB, Reiter C, Zhuang Y, Richardson GJ, Tarpey MM, Barbeito L, Beckman JS (1999) Induction of nitric oxide-dependent apoptosis in motor neurons by zinc-deficient superoxide dismutase. Science 286:2498-2500.
21. Fassbender K, Fatar M, Ragoschke A, Picard M, Bertsch T, Kuehl S, Hennerici M (2000) Subacute but not acute generation of nitric oxide in focal cerebral ischemia. Stroke 31:2208-2211.
22. Fulton D, Gratton JP, McCabe TJ, Fontana J, Fujio Y, Walsh K, Franke TF, Papapetropoulos A, Sessa WC (1999) Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature 399:597-601.
23. Gallis B, Corthals GL, Goodlett DR, Ueba H, Kim F, Presnell SR, Figeys D, Harrison DG, Berk BC, Aebersold R, Corson MA (1999) Identification of flow-dependent endothelial nitric-oxide synthase phosphorylation sites by mass spectrometry and regulation of phosphorylation and nitric oxide production by the phosphatidylinositol 3-kinase inhibitor LY294002. J Biol Chem 274:30101-30108.
24. Garcin ED, Bruns CM, Lloyd SJ, Hosfield DJ, Tiso M, Gachhui R, Stuehr DJ, Tainer JA, Getzoff ED (2004) Structural basis for isozyme-specific regulation of electron transfer in nitric-oxide synthase. J Biol Chem 279:37918-37927.
25. Garthwaite J, Garthwaite G, Palmer RM, Moncada S (1989) NMDA receptor activation induces nitric oxide synthesis from arginine in rat brain slices. Eur J Pharmacol 172:413-416.
26. Giasson BI, Duda JE, Murray IV, Chen Q, Souza JM, Hurtig HI, Ischiropoulos H, Trojanowski JQ, Lee VM (2000) Oxidative damage linked to neurodegeneration by selective alpha-synuclein nitration in synucleinopathy lesions. Science 290:985-989.
27. Groth RD, Dunbar RL, Mermelstein PG (2003) Calcineurin regulation of neuronal plasticity. Biochem Biophys Res Commun 311:1159-1171.
28. Hardingham GE, Bading H (2003) The yin and yang of NMDA receptor signalling. Trends Neurosci 26:81-89.
29. Hardingham GE, Fukunaga Y, Bading H (2002) Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat Neurosci 5:405-414.
30. Hayashi Y, Nishio M, Naito Y, Yokokura H, Nimura Y, Hidaka H, Watanabe Y (1999) Regulation of neuronal nitric-oxide synthase by calmodulin kinases. J Biol Chem 274:20597-20602.
31. Hisatsune C, Umemori H, Mishina M, Yamamoto T (1999) Phosphorylation- dependent interaction of the N-methyl-D-aspartate receptor epsilon 2 subunit with phosphatidylinositol 3-kinase. Genes Cells 4:657-666.
32. Huang Y, Man HY, Sekine-Aizawa Y, Han Y, Juluri K, Luo H, Cheah J, Lowenstein C, Huganir RL, Snyder SH (2005) S-nitrosylation of N-ethylmaleimide sensitive factor mediates surface expression of AMPA receptors. Neuron 46:533-540.
33. Huang Z, Huang PL, Panahian N, Dalkara T, Fishman MC, Moskowitz MA (1994) Effects of cerebral ischemia in mice deficient in neuronal nitric oxide synthase. Science 265:1883-1885.
34. Ischiropoulos H (1998) Biological tyrosine nitration: a pathophysiological function of nitric oxide and reactive oxygen species. Arch Biochem Biophys 356:1-11.
35. Jiang X, Tian F, Mearow K, Okagaki P, Lipsky RH, Marini AM (2005) The excitoprotective effect of N-methyl-D-aspartate receptors is mediated by a brain-derived neurotrophic factor autocrine loop in cultured hippocampal neurons. J Neurochem 94:713-722.
36. Keynes RG, Garthwaite J (2004) Nitric oxide and its role in ischaemic brain injury. Curr Mol Med 4:179-191.
37. Kohler M, Kornau HC, Seeburg PH (1994) The organization of the gene for the functionally dominant alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptor subunit GluR-B. J Biol Chem 269:17367-17370.
38. Kolleker A, Zhu JJ, Schupp BJ, Qin Y, Mack V, Borchardt T, Kohr G, Malinow R, Seeburg PH, Osten P (2003) Glutamatergic plasticity by synaptic delivery of GluR-B(long)-containing AMPA receptors. Neuron 40:1199-1212.
39. Komeima K, Hayashi Y, Naito Y, Watanabe Y (2000) Inhibition of neuronal nitric-oxide synthase by calcium/calmodulin-dependent protein kinase IIalpha through Ser847 phosphorylation in NG108-15 neuronal cells. J Biol Chem 275:28139-28143.
40. Kornau HC, Schenker LT, Kennedy MB, Seeburg PH (1995) Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science 269:1737-1740.
41. Kornau HC, Seeburg PH, Kennedy MB (1997) Interaction of ion channels and receptors with PDZ domain proteins. Curr Opin Neurobiol 7:368-373.
42. Lin SZ, Chiou AL, Wang Y (1996) Ketamine antagonizes nitric oxide release from cerebral cortex after middle cerebral artery ligation in rats. Stroke 27:747-752.
43. Malenka RC, Bear MF (2004) LTP and LTD: an embarrassment of riches. Neuron 44:5-21.
44. Malinow R, Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25:103-126.
45. McBain CJ, Mayer ML (1994) N-methyl-D-aspartic acid receptor structure and function. Physiol Rev 74:723-760.
46. Michaels RL, Rothman SM (1990) Glutamate neurotoxicity in vitro: antagonist pharmacology and intracellular calcium concentrations. J Neurosci 10:283-292.
47. Michell BJ, Griffiths JE, Mitchelhill KI, Rodriguez-Crespo I, Tiganis T, Bozinovski S, de Montellano PR, Kemp BE, Pearson RB (1999) The Akt kinase signals directly to endothelial nitric oxide synthase. Curr Biol 9:845-848.
48. Rameau GA, Akaneya Y, Chiu L, Ziff EB (2000) Role of NMDA receptor functional domains in excitatory cell death. Neuropharmacology 39:2255-2266.
49. Rameau GA, Chiu LY, Ziff EB (2003) NMDA receptor regulation of nNOS phosphorylation and induction of neuron death. Neurobiol Aging 24:1123-1133.
50. Rameau GA, Chiu LY, Ziff EB (2004) Bidirectional regulation of neuronal nitric-oxide synthase phosphorylation at serine 847 by the N-methyl- D-aspartate receptor. J Biol Chem 279:14307-14314.
51. Raymond LA, Moshaver A, Tingley WG, Huganir RL (1996) Glutamate receptor ion channel properties predict vulnerability to cytotoxicity in a transfected nonneuronal cell line. Mol Cell Neurosci 7:102-115.
52. 2+/calmodulin-dependent protein kinase II activity by regulated interactions with N-methyl-D-aspartate receptor NR2B subunits and alpha-actinin. J Biol Chem 280:39316-39323.
53. Rose SP (2000) God's organism? The chick as a model system for memory studies. Learn Mem 7:1-17.
54. Samdani AF, Dawson TM, Dawson VL (1997a) Nitric oxide synthase in models of focal ischemia. Stroke 28:1283-1288.
55. Samdani AF, Newcamp C, Resink A, Facchinetti F, Hoffman BE, Dawson VL, Dawson TM (1997b) Differential susceptibility to neurotoxicity mediated by neurotrophins and neuronal nitric oxide synthase. J Neurosci 17:4633-4641.
56. Schafe GE, Bauer EP, Rosis S, Farb CR, Rodrigues SM, LeDoux JE (2005) Memory consolidation of Pavlovian fear conditioning requires nitric oxide signaling in the lateral amygdala. Eur J Neurosci 22:201-211.
57. Sekaran S, Cunningham J, Neal MJ, Hartell NA, Djamgoz MB (2005) Nitric oxide release is induced by dopamine during illumination of the carp retina: serial neurochemical control of light adaptation. Eur J Neurosci 21:2199-2208.
58. Soriano FX, Papadia S, Hofmann F, Hardingham NR, Bading H, Hardingham GE (2006) Preconditioning doses of NMDA promote neuroprotection by enhancing neuronal excitability. J Neurosci 26:4509-4518.
59. Stingele R, Wilson DA, Traystman RJ, Hanley DF (1998) Tyrosine confounds oxidative electrochemical detection of nitric oxide. Am J Physiol 274:H1698-H1704.
60. Tominaga T, Sato S, Ohnishi T, Ohnishi ST (1993) Potentiation of nitric oxide formation following bilateral carotid occlusion and focal cerebral ischemia in the rat: in vivo detection of the nitric oxide radical by electron paramagnetic resonance spin trapping. Brain Res 614:342-346.
61. Uehara T, Nakamura T, Yao D, Shi ZQ, Gu Z, Ma Y, Masliah E, Nomura Y, Lipton SA (2006) S-nitrosylated protein-disulphide isomerase links protein misfolding to neurodegeneration. Nature 441:513-517.
62. Vanhoutte P, Bading H (2003) Opposing roles of synaptic and extrasynaptic NMDA receptors in neuronal calcium signalling and BDNF gene regulation. Curr Opin Neurobiol 13:366-371.
63. Waxman EA, Lynch DR (2005) N-methyl-D-aspartate receptor subtype mediated bidirectional control of p38 mitogen-activated protein kinase. J Biol Chem 280:29322-29333.
64. Wei G, Dawson VL, Zweier JL (1999) Role of neuronal and endothelial nitric oxide synthase in nitric oxide generation in the brain following cerebral ischemia. Biochim Biophys Acta 1455:23-34.
65. Westbrook GL (1993) Glutamate receptors and excitotoxicity. Res Publ Assoc Res Nerv Ment Dis 71:35-50.
66. Xia Z, Storm DR (2005) The role of calmodulin as a signal integrator for synaptic plasticity. Nat Rev Neurosci 6:267-276.
67. Zanelli SA, Ashraf QM, Mishra OP (2002) Nitration is a mechanism of regulation of the NMDA receptor function during hypoxia. Neuroscience 112:869-877.