Aquaporin-4 deficiency impairs synaptic plasticity and associative fear memory in the lateral amygdala: Involvement of downregulation of glutamate transporter-1 expression

Neuropsychopharmacology

Volumn 37, Issue 8, 2012, Pages 1867-1878

  Li, Yan Kun ^a   Wang, Fang ^a,b,c   Wang, Wei ^a   Luo, Yi ^a   Wu, Peng Fei ^a   Xiao, Jun Li ^a   Hu, Zhuang Li ^a,b,c   Jin, You ^a,b,c   Hu, Gang ^d   Chen, Jian Guo ^a,b,c  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b Key Laboratory for Drug Target Researches and Pharmacodynamic Evaluation of Hubei Province   (China)

^c BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

^d NANJING MEDICAL UNIVERSITY   (China)

Author keywords

amygdala; aquaporin 4; ceftriaxone; fear memory; glutamate transporter 1; long term potentiation

Indexed keywords

AQUAPORIN 4; EXCITATORY AMINO ACID TRANSPORTER; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; VESICULAR GLUTAMATE TRANSPORTER 1;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASSOCIATIVE MEMORY; CONTROLLED STUDY; DOWN REGULATION; EXCITATORY POSTSYNAPTIC POTENTIAL; FEAR; LATERAL AMYGDALA; LONG TERM POTENTIATION; MALE; MOUSE; NERVE CELL PLASTICITY; NEUROTRANSMITTER RELEASE; NONHUMAN; PAIN THRESHOLD; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SYNAPTIC TRANSMISSION; UPREGULATION;

AMYGDALA; ANIMALS; AQUAPORIN 4; CEFTRIAXONE; DOWN-REGULATION; EXCITATORY AMINO ACID TRANSPORTER 2; EXCITATORY POSTSYNAPTIC POTENTIALS; FEAR; LONG-TERM POTENTIATION; MALE; MEMORY; MICE; MICE, KNOCKOUT; NEURAL PATHWAYS; NEURONAL PLASTICITY; RECEPTORS, N-METHYL-D-ASPARTATE; THALAMUS; UP-REGULATION;

EID: 84862307867     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2012.34     Document Type: Article

References (59)

1. Abel T, Lattal KM (2001). Molecular mechanisms of memory acquisition, consolidation and retrieval. Curr Opin Neurobiol 11: 180-187. (Pubitemid 32289404)
2. Amara SG, Fontana AC (2002). Excitatory amino acid transporters: keeping up with glutamate. Neurochem Int 41: 313-318.
3. Amiry-Moghaddam M, Ottersen OP (2003). The molecular basis of water transport in the brain. Nat Rev Neurosci 4: 991-1001. (Pubitemid 37486675)
4. Bao F, Chen M, Zhang Y, Zhao Z (2010). Hypoalgesia in mice lacking aquaporin-4 water channels. Brain Res Bull 83: 298-303.
5. Barad M, Gean PW, Lutz B (2006). The role of the amygdala in the extinction of conditioned fear. Biol Psychiatry 60: 322-328. (Pubitemid 44215854)
6. Binder DK, Papadopoulos MC, Haggie PM, Verkman AS (2004). In vivo measurement of brain extracellular space diffusion by cortical surface photobleaching. J Neurosci 24: 8049-8056. (Pubitemid 39280824)
7. Binder DK, Yao X, Zador Z, Sick TJ, Verkman AS, Manley GT (2006). Increased seizure duration and slowed potassium kinetics in mice lacking aquaporin-4 water channels. Glia 53: 631-636.
8. 25+ T regulatory cell development and severity of Parkinson's disease. Aging Cell 10: 368-382.
9. Citri A, Malenka RC (2008). Synaptic plasticity: multiple forms, functions, and mechanisms. Neuropsychopharmacology 33: 18-41. (Pubitemid 350191314)
10. Clements JD (1996). Transmitter timecourse in the synaptic cleft: its role in central synaptic function. Trends Neurosci 19: 163-171.
11. Danbolt NC (2001). Glutamate uptake. Prog Neurobiol 65: 1-105.
12. Davis M (1992). The role of the amygdala in fear and anxiety. Annu Rev Neurosci 15: 353-375.
13. Ding JY, Kreipke CW, Speirs SL, Schafer P, Schafer S, Rafols JA (2009). Hypoxia-inducible factor-1alpha signaling in aquaporin upregulation after traumatic brain injury. Neurosci Lett 453: 68-72.
14. Fan Y, Kong H, Shi X, Sun X, Ding J, Wu J et al (2008). Hypersensitivity of aquaporin 4-deficient mice to 1-methyl-4-phenyl-1,2,3,6-tetrahydropyrindine and astrocytic modulation. Neurobiol Aging 29: 1226-1236. (Pubitemid 351822407)
15. Fan Y, Zhang J, Sun XL, Gao L, Zeng XN, Ding JH et al (2005). Sex- and region-specific alterations of basal amino acid and monoamine metabolism in the brain of aquaporin-4 knockout mice. J Neurosci Res 82: 458-464. (Pubitemid 41579345)
16. Friedman B, Schachtrup C, Tsai PS, Shih AY, Akassoglou K, Kleinfeld D et al (2009). Acute vascular disruption and aquaporin 4 loss after stroke. Stroke 40: 2182-2190.
17. Gladding CM, Raymond LA (2011). Mechanisms underlying NMDA receptor synaptic/extrasynaptic distribution and function. Mol Cell Neurosci 48: 308-320.
18. Hardingham GE, Bading H (2010). Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders. Nat Rev Neurosci 11: 682-696.
19. Haydon PG, Blendy J, Moss SJ, Rob Jackson F (2009). Astrocytic control of synaptic transmission and plasticity: a target for drugs of abuse? Neuropharmacology 56(Suppl 1): 83-90.
20. Henneberger C, Papouin T, Oliet SH, Rusakov DA (2010). Long-term potentiation depends on release of D-serine from astrocytes. Nature 463: 232-236.
21. Jung SY, Kim J, Kwon OB, Jung JH, An K, Jeong AY et al (2010). Input-specific synaptic plasticity in the amygdala is regulated by neuroligin-1 via postsynaptic NMDA receptors. Proc Natl Acad Sci USA 107: 4710-4715.
22. Katagiri H, Tanaka K, Manabe T (2001). Requirement of appropriate glutamate concentrations in the synaptic cleft for hippocampal LTP induction. Eur J Neurosci 14: 547-553. (Pubitemid 34203462)
23. Kettenmann H, Ransom BR (2005). Neuroglia, 2nd edn. Oxford University Press: New York, p. xix, 601pp.
24. Kim JJ, Jung MW (2006). Neural circuits and mechanisms involved in Pavlovian fear conditioning: a critical review. Neurosci Biobehav Rev 30: 188-202. (Pubitemid 41821808)
25. Knackstedt LA, Melendez RI, Kalivas PW (2010). Ceftriaxone restores glutamate homeostasis and prevents relapse to cocaine seeking. Biol Psychiatry 67: 81-84.
26. Kong H, Sha LL, Fan Y, Xiao M, Ding JH, Wu J et al (2009). Requirement of AQP4 for antidepressive efficiency of fluoxetine: implication in adult hippocampal neurogenesis. Neuropsychopharmacology 34: 1263-1276.
27. LeDoux JE (2000). Emotion circuits in the brain. Annu Rev Neurosci 23: 155-184.
28. Lee EJ, Son GH, Chung S, Lee S, Kim J, Choi S et al (2011). Impairment of fear memory consolidation in maternally stressed male mouse offspring: evidence for nongenomic glucocorticoid action on the amygdala. J Neurosci 31: 7131-7140.
29. Li J, Verkman AS (2001). Impaired hearing in mice lacking aquaporin-4 water channels. J Biol Chem 276: 31233-31237. (Pubitemid 37384992)
30. Li S, Jin M, Koeglsperger T, Shepardson NE, Shankar GM, Selkoe DJ (2011). Soluble Abeta oligomers inhibit long-term potentiation through a mechanism involving excessive activation of extrasynaptic NR2B-containing NMDA receptors. J Neurosci 31: 6627-6638.
31. Ma T, Yang B, Gillespie A, Carlson EJ, Epstein CJ, Verkman AS (1997). Generation and phenotype of a transgenic knockout mouse lacking the mercurial-insensitive water channel aquaporin-4. J Clin Invest 100: 957-962. (Pubitemid 27386279)
32. Makkar SR, Zhang SQ, Cranney J (2010). Behavioral and neural analysis of GABA in the acquisition, consolidation, reconsolidation, and extinction of fear memory. Neuropsychopharmacology 35: 1625-1652.
33. Malenka RC (2003). The long-term potential of LTP. Nat Rev Neurosci 4: 923-926.
34. Malenka RC, Nicoll RA (1999). Long-term potentiation - a decade of progress? Science 285: 1870-1874.
35. Mayer ML, Westbrook GL (1987). The physiology of excitatory amino acids in the vertebrate central nervous system. Prog Neurobiol 28: 197-276. (Pubitemid 17023404)
36. Miller BR, Dorner JL, Shou M, Sari Y, Barton SJ, Sengelaub DR et al (2008). Up-regulation of GLT1 expression increases glutamate uptake and attenuates the Huntington's disease phenotype in the R6/2 mouse. Neuroscience 153: 329-337.
37. Mothet JP, Rouaud E, Sinet PM, Potier B, Jouvenceau A, Dutar P et al (2006). A critical role for the glial-derived neuromodulator D-serine in the age-related deficits of cellular mechanisms of learning and memory. Aging Cell 5: 267-274. (Pubitemid 43805616)
38. Nagelhus EA, Mathiisen TM, Ottersen OP (2004). Aquaporin-4 in the central nervous system: cellular and subcellular distribution and coexpression with KIR4.1. Neuroscience 129: 905-913. (Pubitemid 39556243)
39. Neves G, Cooke SF, Bliss TV (2008). Synaptic plasticity, memory and the hippocampus: a neural network approach to causality. Nat Rev Neurosci 9: 65-75. (Pubitemid 350295694)
40. Nielsen S, Nagelhus EA, Amiry-Moghaddam M, Bourque C, Agre P, Ottersen OP (1997). Specialized membrane domains for water transport in glial cells: high-resolution immunogold cytochemistry of aquaporin-4 in rat brain. J Neurosci 17: 171-180. (Pubitemid 27008860)
41. Patneau DK, Mayer ML (1990). Structure-activity relationships for amino acid transmitter candidates acting at N-methyl-D-aspartate and quisqualate receptors. J Neurosci 10: 2385-2399.
42. Perea G, Navarrete M, Araque A (2009). Tripartite synapses: astrocytes process and control synaptic information. Trends Neurosci 32: 421-431.
43. Rothstein JD, Dykes-Hoberg M, Pardo CA, Bristol LA, Jin L, Kuncl RW et al (1996). Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 16: 675-686. (Pubitemid 26103145)
44. Rothstein JD, Martin L, Levey AI, Dykes-Hoberg M, Jin L, Wu D et al (1994). Localization of neuronal and glial glutamate transporters. Neuron 13: 713-725. (Pubitemid 24300175)
45. Rothstein JD, Patel S, Regan MR, Haenggeli C, Huang YH, Bergles DE et al (2005). Beta-lactam antibiotics offer neuroprotection by increasing glutamate transporter expression. Nature 433: 73-77. (Pubitemid 40101145)
46. Saal D, Dong Y, Bonci A, Malenka RC (2003). Drugs of abuse and stress trigger a common synaptic adaptation in dopamine neurons. Neuron 37: 577-582. (Pubitemid 36262980)
47. Sari Y, Prieto AL, Barton SJ, Miller BR, Rebec GV (2010). Ceftriaxone-induced up-regulation of cortical and striatal GLT1 in the R6/2 model of Huntington's disease. J Biomed Sci 17: 62.
48. Schafe GE, LeDoux JE (2000). Memory consolidation of auditory pavlovian fear conditioning requires protein synthesis and protein kinase A in the amygdala. J Neurosci 20: RC96.
49. Skucas VA, Mathews IB, Yang J, Cheng Q, Treister A, Duffy AM et al (2011). Impairment of select forms of spatial memory and neurotrophin-dependent synaptic plasticity by deletion of glial aquaporin-4. J Neurosci 31: 6392-6397.
50. +buffering and gap junction coupling in the hippocampus. Glia 59: 973-980.
51. Suzuki A, Stern SA, Bozdagi O, Huntley GW, Walker RH, Magistretti PJ et al (2011). Astrocyte-neuron lactate transport is required for long-term memory formation. Cell 144: 810-823.
52. Takano T, Kang J, Jaiswal JK, Simon SM, Lin JH, Yu Y et al (2005). Receptor-mediated glutamate release from volume sensitive channels in astrocytes. Proc Natl Acad Sci USA 102: 16466-16471. (Pubitemid 41688937)
53. 2+ signaling events elicited by cerebral edema. Proc Natl Acad Sci USA 108: 846-851.
54. Tzingounis AV, Wadiche JI (2007). Glutamate transporters: confining runaway excitation by shaping synaptic transmission. Nat Rev Neurosci 8: 935-947. (Pubitemid 350146934)
55. Verkman AS (2005). More than just water channels: unexpected cellular roles of aquaporins. J Cell Sci 118: 3225-3232.
56. Wang ZY, Zhang YQ, Zhao ZQ (2006). Inhibition of tetanically sciatic stimulation-induced LTP of spinal neurons and Fos expression by disrupting glutamate transporter GLT-1. Neuropharmacology 51: 764-772.
57. Zeng XN, Sun XL, Gao L, Fan Y, Ding JH, Hu G (2007). Aquaporin-4 deficiency down-regulates glutamate uptake and GLT-1 expression in astrocytes. Mol Cell Neurosci 34: 34-39. (Pubitemid 46026927)
58. +channel function in brain glial cells. Mol Cell Neurosci 37: 1-10.
59. Zucker RS (1989). Short-term synaptic plasticity. Annu Rev Neurosci 12: 13-31.