AMPA receptor pHluorin-GluA2 reports NMDA receptor-induced intracellular acidification in hippocampal neurons

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 35, 2013, Pages 14426-14431

  Rathje, Mette ^a   Fang, Huaqiang ^b,c   Bachman, Julia L ^b,c   Anggono, Victor ^b,c,d   Gether, Ulrik ^a   Huganir, Richard L ^b,c   Madsen, Kenneth L ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b Department of Neuroscience ^*  (United States)

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

^d UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Brain ischemia; Glutamate receptors; Internalization and recycling; Scaffolding proteins; Synaptic plasticity

Indexed keywords

AMPA RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN INTERACTING WITH PROTEIN KINASE C; SHORT HAIRPIN RNA; ZONIPORIDE;

ACIDIFICATION; ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; CELL MIGRATION; CELL PH; CONTROLLED STUDY; DENDRITIC CELL; FLUORESCENCE; GENE SILENCING; INTRACELLULAR MEMBRANE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SOMATIC CELL; WILD TYPE;

BRAIN ISCHEMIA; GLUTAMATE RECEPTORS; INTERNALIZATION AND RECYCLING; SCAFFOLDING PROTEINS; SYNAPTIC PLASTICITY;

ACIDOSIS; ANIMALS; CELLS, CULTURED; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; N-METHYLASPARTATE; NEURONS; RATS; RATS, WISTAR; RECEPTORS, AMPA; RECEPTORS, N-METHYL-D-ASPARTATE; THROMBIN;

EID: 84883387680     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1312982110     Document Type: Article

References (41)

1. Nicholls DG (2004) Mitochondrial dysfunction and glutamate excitotoxicity studied in primary neuronal cultures. Curr Mol Med 4(2):149-177.
2. Furukawa H, Singh SK, Mancusso R, Gouaux E (2005) Subunit arrangement and function in NMDA receptors. Nature 438(7065):185-192.
3. Shepherd JD, Huganir RL (2007) The cell biology of synaptic plasticity: AMPA receptor trafficking. Annu Rev Cell Dev Biol 23:613-643.
4. Carroll RC, Lissin DV, von Zastrow M, Nicoll RA, Malenka RC (1999) Rapid redistribution of glutamate receptors contributes to long-term depression in hippocampal cultures. Nat Neurosci 2(5):454-460.
5. Ehlers MD (2000) Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting. Neuron 28(2):511-525.
6. Sankaranarayanan S, De Angelis D, Rothman JE, Ryan TA (2000) The use of pHluorins for optical measurements of presynaptic activity. Biophys J 79(4):2199-2208.
7. Ashby MC, et al. (2004) Removal of AMPA receptors (AMPARs) from synapses is preceded by transient endocytosis of extrasynaptic AMPARs. J Neurosci 24(22):5172-5176.
8. Lin DT, Huganir RL (2007) PICK1 and phosphorylation of the glutamate receptor 2 (GluR2) AMPA receptor subunit regulates GluR2 recycling after NMDA receptorinduced internalization. J Neurosci 27(50):13903-13908.
9. Chaineau M, Danglot L, Proux-Gillardeaux V, Galli T (2008) Role of HRB in clathrindependent endocytosis. J Biol Chem 283(49):34365-34373.
10. Hildick KL, González-González IM, Jaskolski F, Henley JM (2012) Lateral diffusion and exocytosis of membrane proteins in cultured neurons assessed using fluorescence recovery and fluorescence-loss photobleaching. J Vis Exp 60:3747.
11. Thorsen TS, et al. (2010) Identification of a small-molecule inhibitor of the PICK1 PDZ domain that inhibits hippocampal LTP and LTD. Proc Natl Acad Sci USA 107(1): 413-418.
12. Sanderson TM, Collingridge GL, Fitzjohn SM (2011) Differential trafficking of AMPA receptors following activation of NMDA receptors and mGluRs. Mol Brain 4:30.
13. Zhang J, et al. (2011) The AAA+ ATPase Thorase regulates AMPA receptor-dependent synaptic plasticity and behavior. Cell 145(2):284-299.
14. Staudinger J, Lu J, Olson EN (1997) Specific interaction of the PDZ domain protein PICK1 with the COOH terminus of protein kinase C-alpha. J Biol Chem 272(51): 32019-32024.
15. Xia J, Zhang X, Staudinger J, Huganir RL (1999) Clustering of AMPA receptors by the synaptic PDZ domain-containing protein PICK1. Neuron 22(1):179-187.
16. Dev KK, et al. (2000) PICK1 interacts with and regulates PKC phosphorylation of mGLUR7. J Neurosci 20(19):7252-7257.
17. Bassan M, et al. (2008) Interaction between the glutamate transporter GLT1b and the synaptic PDZ domain protein PICK1. Eur J Neurosci 27(1):66-82.
18. Torres GE, et al. (2001) Functional interaction between monoamine plasma membrane transporters and the synaptic PDZ domain-containing protein PICK1. Neuron 30:1):121-134.
19. Citri A, et al. (2010) Calcium binding to PICK1 is essential for the intracellular retention of AMPA receptors underlying long-term depression. J Neurosci 30(49): 16437-16452.
20. Terashima A, et al. (2008) An essential role for PICK1 in NMDA receptor-dependent bidirectional synaptic plasticity. Neuron 57(6):872-882.
21. Nakamura Y, et al. (2011) PICK1 inhibition of the Arp2/3 complex controls dendritic spine size and synaptic plasticity. EMBO J 30(4):719-730.
22. Gardner SM, et al. (2005) Calcium-permeable AMPA receptor plasticity is mediated by subunit-specific interactions with PICK1 and NSF. Neuron 45(6):903-915.
23. Steinberg JP, et al. (2006) Targeted in vivo mutations of the AMPA receptor subunit GluR2 and its interacting protein PICK1 eliminate cerebellar long-term depression. Neuron 49(6):845-860.
24. Takamiya K, Mao L, Huganir RL, Linden DJ (2008) The glutamate receptor-interacting protein family of GluR2-binding proteins is required for long-term synaptic depression expression in cerebellar Purkinje cells. J Neurosci 28(22):5752-5755.
25. Volk L, Kim CH, Takamiya K, Yu Y, Huganir RL (2010) Developmental regulation of protein interacting with C kinase 1 (PICK1) function in hippocampal synaptic plasticity and learning. Proc Natl Acad Sci USA 107(50):21784-21789.
26. Makuch L, et al. (2011) Regulation of AMPA receptor function by the human memoryassociated gene KIBRA. Neuron 71(6):1022-1029.
27. Hartley Z, Dubinsky JM (1993) Changes in intracellular pH associated with glutamate excitotoxicity. J Neurosci 13(11):4690-4699.
28. Irwin RP, Lin SZ, Long RT, Paul SM (1994) N-methyl-D-aspartate induces a rapid, reversible, and calcium-dependent intracellular acidosis in cultured fetal rat hippocampal neurons. J Neurosci 14(3 Pt 1):1352-1357.
29. Zhan RZ, et al. (1997) NMDA induces a biphasic change in intracellular pH in rat hippocampal slices. Brain Res 760(1-2):179-186.
30. Wu MM, et al. (2000) Organelle pH studies using targeted avidin and fluoresceinbiotin. Chem Biol 7(3):197-209.
31. Greger IH, Khatri L, Ziff EB (2002) RNA editing at arg607 controls AMPA receptor exit from the endoplasmic reticulum. Neuron 34(5):759-772.
32. Austin C, Wray S (1993) Changes of intracellular pH in rat mesenteric vascular smooth muscle with high-K+ depolarization. J Physiol 469:1-10.
33. Yu FH, Shull GE, Orlowski J (1993) Functional properties of the rat Na/H exchanger NHE-2 isoform expressed in Na/H exchanger-deficient Chinese hamster ovary cells. J Biol Chem 268(34):25536-25541.
34. Orlowski J (1993) Heterologous expression and functional properties of amiloride high affinity (NHE-1) and low affinity (NHE-3) isoforms of the rat Na/H exchanger. J Biol Chem 268(22):16369-16377.
35. Marala RB, et al. (2002) Zoniporide: A potent and highly selective inhibitor of human Na(+)/H(+) exchanger-1. Eur J Pharmacol 451(1):37-41.
36. Thomas GM, Hayashi T, Chiu SL, Chen CM, Huganir RL (2012) Palmitoylation by DHHC5/8 targets GRIP1 to dendritic endosomes to regulate AMPA-R trafficking. Neuron 73(3):482-496.
37. Lee SH, Simonetta A, Sheng M (2004) Subunit rules governing the sorting of internalized AMPA receptors in hippocampal neurons. Neuron 43(2):221-236.
38. Kuner T, Augustine GJ (2000) A genetically encoded ratiometric indicator for chloride: Capturing chloride transients in cultured hippocampal neurons. Neuron 27(3): 447-459.
39. Xiang Z, Bergold PJ (2000) Synaptic depression and neuronal loss in transiently acidic hippocampal slice cultures. Brain Res 881(1):77-87.
40. Madsen KL, Thorsen TS, Rahbek-Clemmensen T, Eriksen J, Gether U (2012) Protein interacting with C kinase 1 (PICK1) reduces reinsertion rates of interaction partners sorted to Rab11-dependent slow recycling pathway. J Biol Chem 287(15):12293-12308.
41. Wang Z, et al. (2008) Myosin Vb mobilizes recycling endosomes and AMPA receptors for postsynaptic plasticity. Cell 135(3):535-548.