Polyamines modulate AMPA receptor-dependent synaptic responses in immature layer V pyramidal neurons

Journal of Neurophysiology

Volumn 93, Issue 5, 2005, Pages 2634-2643

  Shin, Jieun ^a   Shen, Fran ^a   Huguenard, John R ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; CALCIUM; GLUTAMATE RECEPTOR 2; ORNITHINE DECARBOXYLASE; POLYAMINE; SPERMINE;

ANIMAL TISSUE; ARTICLE; CENTRAL NERVOUS SYSTEM; EXCITATION; EXCITATORY POSTSYNAPTIC POTENTIAL; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; NEOCORTEX; NERVE CELL PLASTICITY; NERVE POTENTIAL; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SYNAPSE; WESTERN BLOTTING;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BLOTTING, WESTERN; EFLORNITHINE; ELECTRIC STIMULATION; ENZYME INHIBITORS; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; IMMUNOHISTOCHEMISTRY; NEOCORTEX; NEURONAL PLASTICITY; PATCH-CLAMP TECHNIQUES; POLYAMINES; PYRAMIDAL CELLS; QUINOXALINES; RATS; RECEPTORS, AMPA; SPERMINE; SYNAPSES; TIME FACTORS;

EID: 17644371987     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.01054.2004     Document Type: Article

References (84)

1. Aizenman CD, Munoz-Elias G, and Cline HT. Visually driven modulation of glutamatergic synaptic transmission is mediated by the regulation of intracellular polyamines. Neuron 34: 623-634, 2002.
2. Baukrowitz T, Schulte U, Oliver D, Herlitze S, Krauter T, Tucker SJ, Ruppersberg JP, and Fakler B. PIP2 and PIP as determinants for ATP inhibition of KATP channels. Science 282: 1141-1144, 1998.
3. Ben-Ari Y and Khrestchatisky M. The GluR2 (GIuRB) hypothesis in ischemia: missing links. Trends Neurosci 6: 241-242, 1998.
4. Benveniste M and Mayer ML. Multiple effects of spermine on N-methyl-D-aspartic acid receptor responses of rat cultured hippocampal neurones. J Physiol 464: 131-163, 1993.
5. Benveniste M and Mayer ML. Trapping of glutamate and glycine during open channel block of rat hippocampal neuron NMDA receptors by 9-aminoacridine. J Physiol 483: 367-384, 1995.
6. Bernstein HG and Muller M. The cellular localization of the L-ornithine decarboxylase/polyamine system in normal and diseased central nervous systems. Prog Neurobiol 57: 485-505, 1999.
7. Burnashev N, Monyer H, Seeburg PH, and Sakmann B. Divalent ion permeability of AMPA receptor channels is dominated by the edited form of a single subunit. Neuron 8: 189-198, 1992.
8. Burnashev N, Villarroel A, and Sakmann B. Dimensions and ion selectivity of recombinant AMPA and kainate receptor channels and their dependence on Q/R site residues. J Physiol 496: 165-173, 1996.
9. Camon L, de Vera N, and Martinez E. Polyamine metabolism and glutamate receptor agonists-mediated excitotoxicity in the rat brain. J Neurosci Res 66: 1101-1111, 2001.
10. Casero RA and Woster PM. Terminally alkylated polyamine analogues as chemotherapeutic agents. J Med Chem 44: 1-26, 2001.
11. Choi MH, Kim KR, Kim IS, Lho DS, and Chung BC. Increased hair polyamine levels in patients with Alzheimer's disease. Ann Neurol 50: 128, 2001.
12. Chung HJ, Steinberg JP, Huganir RL, and Linden DJ. Requirement of AMPA receptor GluR2 phosphorylation for cerebellar long-term depression. Science 300: 1751-1755, 2003.
13. Chung HJ, Xia J, Scannevin RH, Zhang X, and Huganir RL. Phosphorylation of the AMPA receptor subunit GluR2 differentially regulates its interaction with PDZ domain-containing proteins. J Neurosci 20: 7258-7267, 2000.
14. Coburn RF, Jones DH, Morgan CP, Baron CB, and Cockcroft S. Spermine increases phosphatidylinositol 4,5-bisphosphate content in permeabilized and nonpermeabilized HL60 cells. Biochim Biophys Acta 1584: 20-30, 2002.
15. Debanne D, Guerineau NC, Gahwiler BH, and Thompson SM. Paired-pulse facilitation and depression at unitary synapses in rat hippocampus: quantal fluctuation affects subsequent release. J Physiol 491: 163-76, 1996.
16. Dobrunz LE and Stevens CF. Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron 6: 995-1008, 1997.
17. Donevan SD and Rogawski MA. Intracellular polyamines mediate inward rectification of Ca(2+)-permeable alpha-amino-3-hydroxy-5-methyl-4- isoxazolepropionic acid receptors. Proc Natl Acad Sci USA 92: 9298-9302, 1995.
18. Essin K, Nistri A, and Magazanik L. Evaluation of GluR2 subunit involvement in AMPA receptor function of neonatal rat hypoglossal motoneurons. Eur J Neurosci 12: 1899-1906, 2002.
19. Ferchmin PA, Eterovic VA, Rivera EM, and Teyler TJ. Spermine increases paired-pulse facilitation in area CA1 of hippocampus in a calcium-dependent manner. Brain Res 689: 189-196, 1995.
20. 2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron 15: 193-204, 1995.
21. Gilad GM and Gilad VH. Beta-aminopropionitrile treatment can accelerate recovery of mice after spinal cord injury. Eur J Pharmacol 430: 69-72, 2001.
22. Gilad GM and Gilad VH. Stress-induced dynamic changes in mouse brain polyamines. Role in behavioral reactivity. Brain Res 943: 23-29, 2002.
23. Goda Y and Stevens CF. Readily releasable pool size changes associated with long term depression. Proc Natl Acad Sci USA 95: 1283-1288, 1998.
24. 2+-permeable AMPA receptors. Nature 381: 793-796, 1996.
25. Herman MD, Reuveny E, and Narahashi T. The effect of polyamines on voltage-activated calcium channels in mouse neuroblastoma cells. J Physiol 462: 645-660, 1993.
26. Higuchi F, Single N, Kohler M, Sommer B, Sprengel R, and Seeburg PH. RNA editing of AMPA receptor subunit GluR-B: a base-paired intron-exon structure determines position and efficiency. Cell 75: 1361-1370, 1993.
27. Hirai H. Modification of AMPA receptor clustering regulates cerebellar synaptic plasticity. Neurosci Res 39: 261-267, 2001.
28. 2+ permeability of KA-AMPA-gated glutamate receptor channel depends on subunit composition. Science 252: 851-853, 1991.
29. Hollmann M and Heinemann S. Cloned glutamate receptors. Annu Rev Nerosci 17: 31-108, 1994.
30. Hoyt MA, Zhang M, and Coffino P. Ubiquitin-independent mechanisms of mouse ornithine decarboxylase degradation are conserved between mammalian and fungal cells. J Biol Chem 278: 12135-12143, 2003.
31. 2+)-ATPase by spermine and other polycationic compounds. Biochemistry 33: 4745-4754, 1994.
32. Isa T, Iino M, Itazawa S, and Ozawa S. Spermine mediates inward rectification of Ca(2+)-permeable AMPA receptor channels. Neuroreport 6: 2045-2048, 1995.
33. Ishihara K. Time-dependent outward currents through the inward rectifier potassium channel IRK1. The role of weak blocking molecules. J Gen Physiol 109: 229-243, 1997.
34. Ishihara K, Yan DH, Yamamoto S, and Ehara T. Inward rectifier K(+) current under physiological cytoplasmic conditions in guinea-pig cardiac ventricular cells. J Physiol 540: 831-841, 2002.
35. Izquierdo I. Pharmacological evidence for a role of long-term potentiation in memory. FASEB J 14: 1139-1145, 1994.
36. Janne J, Alhonen L, Pietila M, and Keinanen TA. Genetic approaches to the cellular functions of polyamines in mammals. Eur J Biochem 271: 877-894, 2004.
37. Jayakar SS and Dikshit M. AMPA receptor regulation mechanisms: future target for safer neuroprotective drugs. Int J Neurosci 114: 695-734, 2004.
38. Jonas P and Burnashev N. Molecular mechanisms controlling calcium entry through AMPA-type glutamate receptor channels. Neuron 15: 987-990, 1995.
39. Jonas P, Racca C, Sakmann B, Seeburg PH, and Monyer H. Differences in Ca2+ permeability of AMPA-type glutamate receptor channels in neocortical neurons caused by differential GluR-B subunit expression. Neuron 12: 1281-1289, 1994.
40. Jonas P and Sakmann B. Glutamate receptor channels in isolated patches from CA1 and CA3 pyramidal cells of rat hippocampal slices. J Physiol 455: 143-171, 1992.
41. Kamboj SK, Swanson GT, and Cull-Candy SG. Intracellular spermine confers rectification on rat calcium-permeable AMPA and kainate receptors. J Physiol 486: 297-303, 1995.
42. Kim CH, Chung HJ, Lee HK, and Huganir RL. Interaction of the AMPA receptor subunit GluR2/3 with PDZ domains regulates hippocampal long-term depression. Proc Natl Acad Sci USA 98: 11725-11730, 2001.
43. Kirby BP and Shaw GG. The neuroprotective effects of N1-dansyl-spermine in the gerbil model of cerebral ischaemia. Brain Res 1011: 74-83, 2004.
44. 2+- permeable AMPA receptors in rat brain by intracellular polyamines generates double rectification. J Physiol 486: 305-312, 1995.
45. Kumar SS, Bacci A, Kharazia V, and Huguenard JR. A developmental switch of AMPA receptor subunits in neocortical pyramidal neurons. J Neurosci 22: 3005-3015, 2002.
46. Kumar SS and Huguenard JR. Properties of excitatory synaptic connections mediated by the corpus callosum in the developing rat neocortex. J Neurophysiol 86: 2973-2985, 2001.
47. Laube G and Veh RW. Astrocytes, not neurons, show most prominent staining for spermidine/spermine-like immunoreactivity in adult rat brain. Glia 2: 171-179, 1997.
48. Lee HK, Barbarosie M, Kameyama K, Bear MF, and Huganir RL. Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity. Nature 405: 955-959, 2000.
49. Mathern GW, Pretorius JK, Mendoza B, Lozada A, and Kornblum HI. Hippocampal AMPA and NMDA mRNA levels correlate with aberrant fascia dentata mossy fiber sprouting in the pilocarpine model of spontaneous limbic epilepsy. J Neurosci Res 54: 734-753, 1998.
50. Matsuda S, Launey T, Mikawa S, and Hirai H. Disruption of AMPA receptor GluR2 clusters following long-term depression induction in cerebellar Purkinje neurons. EMBO J 9: 2765-2774, 2000.
51. McBain CJ and Dingledine R. Heterogeneity of synaptic glutamate receptors on CA3 stratum radiatum interneurones of rat hippocampus. J Physiol 462: 373-392, 1993.
52. McGlade-McCulloh E, Yamamoto H, Tan SE, Brickey DA, and Soderling TR. Phosphorylation and regulation of glutamate receptors by calcium/calmodulin- dependent protein kinase II. Nature 362: 640-642, 1993.
53. Morrison LD, Cao XC, and Kish SJ. Ornithine decarboxylase in human brain: influence of aging, regional distribution, and Alzheimer's disease. J Neurochem 71: 288-294, 1998.
54. Morrison LD and Kish SJ. Brain polyamine levels are altered in Alzheimer's disease. Neurosci Lett 197: 5-8, 1995.
55. Moshier JA, Skunca M, Wu W, Boppana SM, Rauscher FJ III, and Dosescu J. Regulation of ornithine decarboxylase gene expression by the Wilms' tumor suppressor WT1. Nucleic Acids Res 24: 1149-1157, 1996.
56. + channels. Eur J Biochem 267: 5824-5829, 2000.
57. Orzi F, Zoli M, Passarelli F, Ferraguti F, Fieschi C, and Agnati LF. Repeated electroconvulsive shock increases glial fibrillary acidic protein, ornithine decarboxylase, somatostatin and cholecystokinin immunoreactivities in the hippocampal formation of the rat. Brain Res 533: 223-231, 1990.
58. Otieno MA and Kensler TW. A role for protein kinase C-delta in the regulation of ornithine decarboxylase expression by oxidative stress. Cancer Res 60: 4391-4396, 2000.
59. Ozaki S, DeWald DB, Shope JC, Chen J, and Prestwich GD. Intracellular delivery of phosphoinositides and inositol phosphates using polyamine carriers. Proc Natl Acad Sci USA 97: 11286-11291, 2000.
60. Panchenko VA, Glasser CR, Partin KM, and Mayer ML. Amino acid substitutions in the pore of rat glutamate receptors at sites influencing block by polyamines. J Physiol 520: 337-357, 1999.
61. Paschen W. Polyamine metabolism in reversible cerebral ischemia. Cerebrovasc Brain Metab Rev 4: 59-88, 1992.
62. Paschen W, Csiba L, Rohn G, and Bereczki D. Polyamine metabolism in transient focal ischemia of rat brain. Brain Res 566: 354-357, 1991.
63. Pellegrini-Giampietro DE. An activity-dependent spermine-mediated mechanism that modulates glutamate transmission. Trends Neurosci 26: 9-11, 2003.
64. Porter CW and Bergeron RJ. Spermidine requirement for cell proliferation in eukaryotic cells: structural specificity and quantitation. Science 219: 1083-1085, 1983.
65. Reddy SG, McIlheran SM, Cochran BJ, Worth LL, Bishop LA, Brown PJ, Knutson VP, and Haddox MK. Multisite phosphorylation of ornithine decarboxylase in transformed macrophages results in increased intracellular enzyme stability and catalytic efficiency. J Biol Chem 271: 24945-24953, 1996.
66. Rozov A and Burnashev N. Polyamine-dependent facilitation of postsynaptic AMPA receptors counteracts paired-pulse depression. Nature 401: 594-598, 1999.
67. 2+-permeable AMPA receptor channels by activity-dependent relief from polyamine block. J Physiol 511: 361-377, 1998.
68. Seiler N. Thirty years of polyamine-related approaches to cancer therapy. Retrospect and prospect. Part 1 and Part 2. Structural analogues and derivatives. Curr Drug Targets 7: 565-585, 2003.
69. Smith SE and Chesler M. Effect of divalent cations on AMPA-evoked extracellular alkaline shifts in rat hippocampal slices. J Neurophysiol 82: 1902-1908, 1999.
70. Sommer B, Kohler M, Sprengel R, and Seeburg PH. RNA editing in brain controls a determinant of ion flow in glutamate-gated channels. Cell 67: 11-19, 1991.
71. Soulet D and Rivest S. Polyamines play a critical role in the control of the innate immune response in the mouse central nervous system. J Cell Biol 162: 257-268, 2003.
72. Staudinger J, Lu J, and Olson EN. Specific interaction of the PDZ domain protein PICK1 with the COOH terminus of protein kinase C-alpha. J Biol Chem 272: 32019-32024, 1997.
73. Staudinger J, Zhou J, Burgess R, Elledge SJ, and Olson EN. PICK1: a perinuclear binding protein and substrate for protein kinase C isolated by the yeast two-hybrid system. J Cell Biol 128: 263-271, 1995.
74. Thomas T, Balabhadrapathruni S, Gallo MA, and Thomas TJ. Development of polyamine analogs as cancer therapeutic agents. Oncol Res 13: 123-135, 2002.
75. Verma AK, Hsiao KM, Ahrens H, Suganuma M, Fujiki H, Matsufuji S, and Hayashi H. Superinduction of mouse epidermal ornithine decarboxylase activity by repeated 12-o-tetradecanoylphorbol-13-acetate treatments. Mol Cell Biochem 155: 139-151, 1996.
76. Vertino PM, Beerman TA, Kelly EJ, Bergeron RJ, and Porter CW. Selective cellular depletion of mitochondrial DNA by the polyamine analog N1,N12-bis(ethyl)spermine and its relationship to polyamine structure and function. Mol Pharmacol 39: 487-494, 1991.
77. Wallace HM, Fraser AV, and Hughes A. A perspective of polyamine metabolism. Biochem J 376: 1-14, 2003.
78. Washburn MS and Dingledine R. Block of -amino-3-hydroxy-5-methyl-4- isoxazolepropionic acid (AMPA) receptors by polyamines and polyamine toxins. J Pharmacol Exp Ther 278: 669-678, 1996.
79. Washburn MS, Numberger M, Zhang S, and Dingledine R. Differential dependence on GluR2 expression of three characteristic features of AMPA receptors. J Neurosci 17: 9393-9406, 1997.
80. Wheeler DL, Reddig PJ, Dreckschmidt NE, Leitges M, and Verma AK. Protein kinase Cdelta-mediated signal to ornithine decarboxylase induction is independent of skin tumor suppression. Oncogene 21: 3620-3630, 2002.
81. Williams K. Interactions of polyamines with ion channels. Biochem J 325: 289-297, 1997.
82. Worth LL, Cochran BJ, and Haddox MK. Phosphorylation of ornithine decarboxylase at both serine and threonine residues in the ODC-overproducing, Abelson virus-transformed RAW264 cell line. Cancer Res 54: 3967-3970, 1994.
83. Zilles K, Qu M, Schleicher A, and Luhmann HJ. Characterization of neuronal migration disorders in neocortical structures: quantitative receptor autoradiography of ionotropic glutamate, GABA(A) and GABA(B) receptors. Eur J Neurosci 10: 3095-3106, 1998.
84. Zoli M, Zini I, Grimaldi R, Biagini G, and Agnati LF. Effects of polyamine synthesis blockade on neuronal loss and astroglial reaction after transient forebrain ischemia. Int J Dev Neurosci 2: 175-87, 1993.