Chronic ceftriaxone treatment rescues hippocampal memory deficit in AQP4 knockout mice via activation of GLT-1

Neuropharmacology

Volumn 75, Issue , 2013, Pages 213-222

  Yang, Jun ^a   Li, Ming Xing ^a   Luo, Yi ^a   Chen, Tao ^a   Liu, Jing ^a   Fang, Peng ^a   Jiang, Bo ^a   Hu, Zhuang Li ^a,b,c   Jin, You ^a,b,c   Chen, Jian Guo ^a,b,c   Wang, Fang ^a,b,c  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

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

Author keywords

AQP4; Ceftriaxone; GLT 1; Long term potentiation; Memory

Indexed keywords

AQUAPORIN 4; CEFTRIAXONE; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; VESICULAR GLUTAMATE TRANSPORTER 1;

AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; DENDRITIC SPINE; DENTATE GYRUS; DOWN REGULATION; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPUS; LONG TERM POTENTIATION; MALE; MEMORY CONSOLIDATION; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; UPREGULATION;

6-CYANO-7- NITROQUINOXALINE-2, 3-DIONE; ACSF; AMPA; AQP4; AQUAPORIN-4; ARTIFICIAL CEREBROSPINAL FLUID; BOVINE SERUM ALBUMIN; BSA; CEF; CEFTRIAXONE; CNQX; DENTATE GYRUS; DG; DL-AMINOPHOSPHONOVALERIC ACID; DL-APV; EPSCS; EXCITATORY POSTSYNAPTIC CURRENTS; FEPSP; FIELD EXCITATORY POSTSYNAPTIC POTENTIAL; GLT-1; GLUTAMATE TRANSPORTER-1; HPLC-ECD; KNOCKOUT; KO; LONG-TERM POTENTIATION; LTP; MEMORY; N-METHYL-D-ASPARTATE; NMDA; PBS; PERFORANT PATH; PHOSPHATE-BUFFERED SALINE; POPULATION SPIKE; PP; PS; REVERSE-PHASE HPLC COUPLED TO ELECTROCHEMICAL DETECTION; TBS; THETA-BURST STIMULATION; Α-AMINO-3-HYDROXY-5-METHYL-4-ISOXAZOLEPROPIONIC ACID;

ACTION POTENTIALS; ANIMALS; AQUAPORIN 4; CEFTRIAXONE; CONDITIONING, CLASSICAL; EXCITATORY AMINO ACID AGENTS; EXCITATORY AMINO ACID TRANSPORTER 2; EXPLORATORY BEHAVIOR; FEAR; GENE EXPRESSION REGULATION; HIPPOCAMPUS; MEMORY DISORDERS; MICE; MICE, KNOCKOUT; NEURONAL PLASTICITY; PAIN THRESHOLD; PATCH-CLAMP TECHNIQUES; SYNAPSES;

EID: 84883535475     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2013.08.009     Document Type: Article

References (46)

1. M. Amiry-Moghaddam, R. Xue, F.M. Haug, J.D. Neely, A. Bhardwaj, P. Agre, M.E. Adams, S.C. Froehner, S. Mori, and O.P. Ottersen Alpha-syntrophin deletion removes the perivascular but not endothelial pool of aquaporin-4 at the blood-brain barrier and delays the development of brain edema in an experimental model of acute hyponatremia FASEB J. 18 2004 542 544
2. A. Araque, V. Parpura, R.P. Sanzgiri, and P.G. Haydon Tripartite synapses: glia, the unacknowledged partner Trends Neurosci. 22 1999 208 215 (Pubitemid 29202082)
3. J.L. Arriza, W.A. Fairman, J.I. Wadiche, G.H. Murdoch, M.P. Kavanaugh, and S.G. Amara Functional comparisons of three glutamate transporter subtypes cloned from human motor cortex J. Neurosci. 14 1994 5559 5569 (Pubitemid 24279072)
4. J. Badaut, F. Lasbennes, P.J. Magistretti, and L. Regli Aquaporins in brain: distribution, physiology, and pathophysiology J. Cereb. Blood Flow Metab. 22 2002 367 378 (Pubitemid 34273593)
5. J.S. Bains, and S.H. Oliet Glia: they make your memories stick! Trends Neurosci. 30 2007 417 424 (Pubitemid 47088717)
6. D.K. Binder, X. Yao, Z. Zador, T.J. Sick, A.S. Verkman, and G.T. Manley Increased seizure duration and slowed potassium kinetics in mice lacking aquaporin-4 water channels Glia 53 2006 631 636
7. T.V. Bliss, and T. Lomo Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path J. Physiol. 232 1973 331 356
8. F. Cai, F. Wang, F.K. Lin, C. Liu, L.Q. Ma, J. Liu, W.N. Wu, W. Wang, J.H. Wang, and J.G. Chen Redox modulation of long-term potentiation in the hippocampus via regulation of the glycogen synthase kinase-3beta pathway Free Radic. Biol. Med. 45 2008 964 970
9. D.R. Curtis, and G.A. Johnston Amino acid transmitters in the mammalian central nervous system Ergeb Physiol. 69 1974 97 188
10. M. D'Ascenzo, T. Fellin, M. Terunuma, R. Revilla-Sanchez, D.F. Meaney, Y.P. Auberson, S.J. Moss, and P.G. Haydon mGluR5 stimulates gliotransmission in the nucleus accumbens Proc. Natl. Acad. Sci. U. S. A. 104 2007 1995 2000 (Pubitemid 46239892)
11. N.C. Danbolt Glutamate uptake Prog. Neurobiol. 65 2001 1 105 (Pubitemid 32479155)
12. B.A. Donzanti, and B.K. Yamamoto An improved and rapid HPLC-EC method for the isocratic separation of amino acid neurotransmitters from brain tissue and microdialysis perfusates Life Sci. 43 1988 913 922
13. F. Fonnum Glutamate: a neurotransmitter in mammalian brain J. Neurochem. 42 1984 1 11 (Pubitemid 14216942)
14. B. Friedman, C. Schachtrup, P.S. Tsai, A.Y. Shih, K. Akassoglou, D. Kleinfeld, and P.D. Lyden Acute vascular disruption and aquaporin 4 loss after stroke Stroke 40 2009 2182 2190
15. J.S. Guan, S.J. Haggarty, E. Giacometti, J.H. Dannenberg, N. Joseph, J. Gao, T.J. Nieland, Y. Zhou, X. Wang, R. Mazitschek, J.E. Bradner, R.A. DePinho, R. Jaenisch, and L.H. Tsai HDAC2 negatively regulates memory formation and synaptic plasticity Nature 459 2009 55 60
16. P.G. Haydon, J. Blendy, S.J. Moss, and F. Rob Jackson Astrocytic control of synaptic transmission and plasticity: a target for drugs of abuse? Neuropharmacology 56 Suppl. 1 2009 83 90
17. M.S. Hsu, M. Seldin, D.J. Lee, G. Seifert, C. Steinhauser, and D.K. Binder Laminar-specific and developmental expression of aquaporin-4 in the mouse hippocampus Neuroscience 178 2011 21 32
18. P. Jedlicka, T. Papadopoulos, T. Deller, H. Betz, and S.W. Schwarzacher Increased network excitability and impaired induction of long-term potentiation in the dentate gyrus of collybistin-deficient mice in vivo Mol. Cell Neurosci. 41 2009 94 100
19. P. Jedlicka, S.W. Schwarzacher, R. Winkels, F. Kienzler, M. Frotscher, C.R. Bramham, C. Schultz, C. Bas Orth, and T. Deller Impairment of in vivo theta-burst long-term potentiation and network excitability in the dentate gyrus of synaptopodin-deficient mice lacking the spine apparatus and the cisternal organelle Hippocampus 19 2009 130 140
20. P. Jourdain, L.H. Bergersen, K. Bhaukaurally, P. Bezzi, M. Santello, M. Domercq, C. Matute, F. Tonello, V. Gundersen, and A. Volterra Glutamate exocytosis from astrocytes controls synaptic strength Nat. Neurosci. 10 2007 331 339
21. H. Katagiri, K. Tanaka, and T. Manabe Requirement of appropriate glutamate concentrations in the synaptic cleft for hippocampal LTP induction Eur. J. Neurosci. 14 2001 547 553 (Pubitemid 34203462)
22. S.G. Lee, Z.Z. Su, L. Emdad, P. Gupta, D. Sarkar, A. Borjabad, D.J. Volsky, and P.B. Fisher Mechanism of ceftriaxone induction of excitatory amino acid transporter-2 expression and glutamate uptake in primary human astrocytes J. Biol. Chem. 283 2008 13116 13123
23. Y.K. Li, F. Wang, W. Wang, Y. Luo, P.F. Wu, J.L. Xiao, Z.L. Hu, Y. Jin, G. Hu, and J.G. Chen Aquaporin-4 deficiency impairs synaptic plasticity and associative fear memory in the lateral amygdala: involvement of downregulation of glutamate transporter-1 expression Neuropsychopharmacology 37 2012 1867 1878
24. Y. Lin, G. Tian, K. Roman, C. Handy, J.B. Travers, C.L. Lin, and R.L. Stephens Jr. Increased glial glutamate transporter EAAT2 expression reduces visceral nociceptive response in mice Am. J. Physiol. Gastrointest. Liver Physiol. 296 2009 G129 G134
25. T. Ma, B. Yang, A. Gillespie, E.J. Carlson, C.J. Epstein, and A.S. Verkman Generation and phenotype of a transgenic knockout mouse lacking the mercurial-insensitive water channel aquaporin-4 J. Clin. Invest. 100 1997 957 962 (Pubitemid 27386279)
26. G.T. Manley, M. Fujimura, T. Ma, N. Noshita, F. Filiz, A.W. Bollen, P. Chan, and A.S. Verkman Aquaporin-4 deletion in mice reduces brain edema after acute water intoxication and ischemic stroke Nat. Med. 6 2000 159 163 (Pubitemid 30082359)
27. N. Melzer, S.G. Meuth, D. Torres-Salazar, S. Bittner, A.L. Zozulya, C. Weidenfeller, A. Kotsiari, M. Stangel, C. Fahlke, and H. Wiendl A beta-lactam antibiotic dampens excitotoxic inflammatory CNS damage in a mouse model of multiple sclerosis PLoS One 3 2008 e3149
28. A. Mitani, and K. Tanaka Functional changes of glial glutamate transporter GLT-1 during ischemia: an in vivo study in the hippocampal CA1 of normal mice and mutant mice lacking GLT-1 J. Neurosci. 23 2003 7176 7182 (Pubitemid 36975882)
29. J.P. Mothet, L. Pollegioni, G. Ouanounou, M. Martineau, P. Fossier, and G. Baux Glutamate receptor activation triggers a calcium-dependent and SNARE protein-dependent release of the gliotransmitter D-serine Proc. Natl. Acad. Sci. U. S. A. 102 2005 5606 5611 (Pubitemid 40530304)
30. M.D. Munoz, O. Herreras, A.S. Herranz, J.M. Solis, R. Martin del Rio, and J. Lerma Effects of dihydrokainic acid on extracellular amino acids and neuronal excitability in the in vivo rat hippocampus Neuropharmacology 26 1987 1 8 (Pubitemid 17232289)
31. A. Omrani, M. Melone, M. Bellesi, V. Safiulina, T. Aida, K. Tanaka, E. Cherubini, and F. Conti Up-regulation of GLT-1 severely impairs LTD at mossy fibre-CA3 synapses J. Physiol. 587 2009 4575 4588
32. M.C. Papadopoulos, G.T. Manley, S. Krishna, and A.S. Verkman Aquaporin-4 facilitates reabsorption of excess fluid in vasogenic brain edema FASEB J. 18 2004 1291 1293 (Pubitemid 39561580)
33. D.K. Patneau, and M.L. Mayer Structure-activity relationships for amino acid transmitter candidates acting at N-methyl-D-aspartate and quisqualate receptors J. Neurosci. 10 1990 2385 2399
34. C. Paul, F. Schoberl, P. Weinmeister, V. Micale, C.T. Wotjak, F. Hofmann, and T. Kleppisch Signaling through cGMP-dependent protein kinase I in the amygdala is critical for auditory-cued fear memory and long-term potentiation J. Neurosci. 28 2008 14202 14212
35. J. Pham, S.M. Cabrera, C. Sanchis-Segura, and M.A. Wood Automated scoring of fear-related behavior using EthoVision software J. Neurosci. Methods 178 2009 323 326
36. G. Pines, N.C. Danbolt, M. Bjoras, Y. Zhang, A. Bendahan, L. Eide, H. Koepsell, J. Storm-Mathisen, E. Seeberg, and B.I. Kanner Cloning and expression of a rat brain L-glutamate transporter Nature 360 1992 464 467
37. J.D. Rothstein Excitotoxicity and neurodegeneration in amyotrophic lateral sclerosis Clin. Neurosci. 3 1995 348 359 (Pubitemid 27052169)
38. J.D. Rothstein, S. Patel, M.R. Regan, C. Haenggeli, Y.H. Huang, D.E. Bergles, L. Jin, M. Dykes Hoberg, S. Vidensky, D.S. Chung, S.V. Toan, L.I. Bruijn, Z.Z. Su, P. Gupta, and P.B. Fisher Beta-lactam antibiotics offer neuroprotection by increasing glutamate transporter expression Nature 433 2005 73 77 (Pubitemid 40101145)
39. V.A. Skucas, I.B. Mathews, J. Yang, Q. Cheng, A. Treister, A.M. Duffy, A.S. Verkman, B.L. Hempstead, M.A. Wood, D.K. Binder, and H.E. Scharfman Impairment of select forms of spatial memory and neurotrophin-dependent synaptic plasticity by deletion of glial aquaporin-4 J. Neurosci. 31 2011 6392 6397
40. (+)-dependent glutamate/aspartate transporter from rat brain Proc. Natl. Acad. Sci. U. S. A. 89 1992 10955 10959
41. + buffering and gap junction coupling in the hippocampus Glia 59 2011 973 980
42. T. Takano, J. Kang, J.K. Jaiswal, S.M. Simon, J.H. Lin, Y. Yu, Y. Li, J. Yang, G. Dienel, H.R. Zielke, and M. Nedergaard Receptor-mediated glutamate release from volume sensitive channels in astrocytes Proc. Natl. Acad. Sci. U. S. A. 102 2005 16466 16471 (Pubitemid 41688937)
43. K. Tanaka, K. Watase, T. Manabe, K. Yamada, M. Watanabe, K. Takahashi, H. Iwama, T. Nishikawa, N. Ichihara, T. Kikuchi, S. Okuyama, N. Kawashima, S. Hori, M. Takimoto, and K. Wada Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1 Science 276 1997 1699 1702 (Pubitemid 27421977)
44. Z.Y. Wang, Y.Q. Zhang, and Z.Q. Zhao Inhibition of tetanically sciatic stimulation-induced LTP of spinal neurons and Fos expression by disrupting glutamate transporter GLT-1 Neuropharmacology 51 2006 764 772
45. H. Wolosker, S. Blackshaw, and S.H. Snyder Serine racemase: a glial enzyme synthesizing D-serine to regulate glutamate-N-methyl-D-aspartate neurotransmission Proc. Natl. Acad. Sci. U. S. A. 96 1999 13409 13414
46. X.N. Zeng, X.L. Sun, L. Gao, Y. Fan, J.H. Ding, and G. Hu Aquaporin-4 deficiency down-regulates glutamate uptake and GLT-1 expression in astrocytes Mol. Cell Neurosci. 34 2007 34 39 (Pubitemid 46026927)