Expression of genes involved in excitatory neurotransmission in anoxic crucian carp (Carassius carassius) brain

Physiological Genomics

Volumn 35, Issue 1, 2008, Pages 5-17

  Ellefsen, Stian ^a,b   Sandvik, Guro K ^a   Larsen, Helene K ^a   Stensløkken, Kåre Olav ^c   Hov, Dag Are S ^a   Kristensen, Tom A ^a   Nilsson, Göran E ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b INLAND NORWAY UNIVERSITY OF APPLIED SCIENCES   (Norway)

^c ULLEVÅL UNIVERSITY HOSPITAL   (Norway)

Author keywords

Anoxia; External RNA control; Glutamate transporter; N methyl D aspartate 3 hydroxy 5 methyl 4 isoxazole propionate receptors; Voltage gated ion channels

Indexed keywords

AMPA RECEPTOR; CALCIUM CHANNEL; GLUTAMATE TRANSPORTER; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2C; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2D; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 3A; UNCLASSIFIED DRUG; VOLTAGE GATED SODIUM CHANNEL; NR1 NMDA RECEPTOR; PROTEIN SUBUNIT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN; BRAIN HYPOXIA; CARASSIUS CARASSIUS; CARP; CONTROLLED STUDY; GENE; GENE CASSETTE; GENE EXPRESSION; GENE FUNCTION; GLYCOSYLATION; MAMMAL; MULTIGENE FAMILY; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RNA SEQUENCE; RNA SPLICING; AMINO ACID SEQUENCE; ANIMAL; CELL HYPOXIA; CHEMICAL STRUCTURE; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; PROTEIN CONFORMATION; SYNAPTIC TRANSMISSION;

CARASSIUS; CARASSIUS CARASSIUS; MAMMALIA; RATTUS;

AMINO ACID SEQUENCE; ANIMALS; BRAIN; CARPS; CELL HYPOXIA; GENE EXPRESSION; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; PROTEIN SUBUNITS; RECEPTORS, N-METHYL-D-ASPARTATE; RNA SPLICE SITES; RNA, MESSENGER; SYNAPTIC TRANSMISSION;

EID: 56149105364     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.90221.2008     Document Type: Article

References (74)

1. Armstrong N, Sun Y, Chen GQ, Gouaux E. Structure of a glutamate-receptor ligand-binding core in complex with kainate. Nature 395: 913-917, 1998.
2. Arundine M, Tymianski M. Molecular mechanisms of calcium-dependent neurodegeneration in excitotoxicity. Cell Calcium 34: 325-337, 2003.
3. Bickler PE. Clinical perspectives: neuroprotection lessons from hypoxia-tolerant organisms. J Exp Biol 207: 3243-3249, 2004.
4. Bickler PE, Buck LT. Hypoxia tolerance in reptiles, amphibians, and fishes: life with variable oxygen availability. Annu Rev Physiol 69: 145-170, 2007.
5. Bickler PE, Donohoe PH, Buck LT. Hypoxia-induced silencing of NMDA receptors in turtle neurons. J Neurosci 20: 3522-3528, 2000.
6. Bickler PE, Fahlman CS, Taylor DM. Oxygen sensitivity of NMDA receptors: relationship to NR2 subunit composition and hypoxia tolerance of neonatal neurons. Neuroscience 118: 25-35, 2003.
7. Buck LT, Bickler PE. Adenosine and anoxia reduce N-methyl-D-aspartate receptor open probability in turtle cerebrocortex. J Exp Biol 201: 289-297, 1998.
8. 2+ channels. Annu Rev Cell Dev Biol 16: 521-555, 2000.
9. Catterall WA, Goldin AL, Waxman SG. International Union of Pharmacology. XXXIX. Compendium of voltage-gated ion channels: sodium channels. Pharmacol Rev 55: 575-578, 2003.
10. Catterall WA, Striessnig J, Snutch TP, Perez-Reyes E. International Union of Pharmacology. XL. Compendium of voltage-gated ion channels: calcium channels. Pharmacol Rev 55: 579-581, 2003.
11. Chatterton JE, Awobuluyi M, Premkumar LS, Takahashi H, Talantova M, Shin Y, Cui J, Tu S, Sevarino KA, Nakanishi N, Tong G, Lipton SA, Zhang D. Excitatory glycine receptors containing the NR3 family of NMDA receptor subunits. Nature 415: 793-798, 2002.
12. Chazot PL, Cik M, Stephenson FA. An investigation into the role of N-glycosylation in the functional expression of a recombinant heteromeric NMDA receptor. Mol Membr Biol 12: 331-337, 1995.
13. Choi DW, Rothman SM. The role of glutamate neurotoxicity in hypoxic-ischemic neuronal death. Annu Rev Neurosci 13: 171-182, 1990.
14. 2+-permeable AMPA receptors: synaptic plasticity and beyond. Curr Opin Neurobiol 16: 288-297, 2006.
15. Dallas M, Boycott HE, Atkinson L, Miller A, Boyle JP, Pearson HA, Peers C. Hypoxia suppresses glutamate transport in astrocytes. J Neurosci 27: 3946-3955, 2007.
16. Danbolt NC. Glutamate uptake. Prog Neurobiol 65: 1-105, 2001.
17. Das S, Sasaki YF, Rothe T, Premkumar LS, Takasu M, Crandall JE, Dikkes P, Conner DA, Rayudu PV, Cheung W, Chen HS, Lipton SA, Nakanishi N. Increased NMDA current and spine density in mice lacking the NMDA receptor subunit NR3A. Nature 393: 377-381, 1998.
18. Dingledine R, Borges K, Bowie D, Traynelis SF. The glutamate receptor ion channels. Pharmacol Rev 51: 7-61, 1999.
19. + channels: multiplicity of expression, plasticity, functional implications and pathophysiological aspects. Eur Biophys J 33: 180-193, 2004.
20. Douen AG, Akiyama K, Hogan MJ, Wang F, Dong L, Chow AK, Hakim A. Preconditioning with cortical spreading depression decreases intraischemic cerebral glutamate levels and down-regulates excitatory amino acid transporters EAAT1 and EAAT2 from rat cerebral cortex plasma membranes. J Neurochem 75: 812-818, 2000.
21. Dunah AW, Yasuda RP, Wang Yh Luo J, Davila-Garcia MI, Gbadegesin M, Vicini S, Wolfe BB. Regional and ontogenic expression of the NMDA receptor subunit NR2D protein in rat brain using a subunit-specific antibody. J Neurochem 67: 2335-2345, 1996.
22. Ellefsen S, Stenslokken KO, Sandvik GK, Kristensen TA, Nilsson GE. Improved normalization of real time RT PCR data using an external RNA control. Anal Biochem 376: 83-93, 2008.
23. Erecinska M, Silver IA. Ions and energy in mammalian brain. Prog Neurobiol 43: 37-71, 1994.
24. Felts PA, Yokoyama S, DibHajj S, Black JA, Waxman SG. Sodium channel alpha-subunit mRNAs I, II, III, NaG, Na6 and hNE (PN1): different expression patterns in developing rat nervous system. Mol Brain Res 45: 71-82, 1997.
25. Fukaya M, Kato A, Lovett C, Tonegawa S, Watanabe M. Retention of NMDA receptor NR2 subunits in the lumen of endoplasmic reticulum in targeted NR1 knockout mice. Proc Natl Acad Sci USA 100: 4855-4860, 2003.
26. Furukawa H, Gouaux E. Mechanisms of activation, inhibition and specificity: crystal structures of the NMDA receptor NR1 ligand-binding core. EMBO J 22: 2873-2885, 2003.
27. Goebel DJ, Poosch MS. NMDA receptor subunit gene expression in the rat brain: a quantitative analysis of endogenous mRNA levels of NR1Com, NR2A, NR2B, NR2C, NR2D and NR3A. Mol Brain Res 69: 164-170, 1999.
28. 2+ influx in hippocampal CA1 neurons of gerbil. J Neurosci 17: 6179-6188, 1997.
29. Greenbaum D, Colangelo C, Williams K, Gerstein M. Comparing protein abundance and mRNA expression levels on a genomic scale. Genome Biol 4: 117, 2003.
30. Hochachka PW. Defense strategies against hypoxia and hypothermia. Science 231: 234-241, 1986.
31. Hylland P, Nilsson GE. Extracellular levels of amino acid neurotransmitters during anoxia and forced energy deficiency in crucian carp brain. Brain Res 823: 49-58, 1999.
32. Iihara K, Joo DT, Henderson J, Sattler R, Taverna FA, Lourensen S, Orser BA, Roder JC, Tymianski M. The influence of glutamate receptor 2 expression on excitotoxicity in GluR2 null mutant mice. J Neurosci 21: 2224-2239, 2001.
33. Inanobe A, Furukawa H, Gouaux E. Mechanism of partial agonist action at the NR1 subunit of NMDA receptors. Neuron 47: 71-84, 2005.
34. Jansen R, Greenbaum D, Gerstein M. Relating whole-genome expression data with protein-protein interactions. Genome Res 12: 37-46, 2002.
35. + gradient dissipation during anoxia. J Exp Biol 198: 2575-2580, 1995.
36. Kohr G. NMDA receptor function: subunit composition versus spatial distribution. Cell Tissue Res 326: 439-446, 2006.
37. Kristian T, Siesjo BK. Calcium-related damage in ischemia. Life Sci 59: 357-367, 1996.
38. Larsson E, Nanobashvili A, Kokaia Z, Lindvall O. Evidence for neuroprotective effects of endogenous brain-derived neurotrophic factor after global forebrain ischemia in rats. J Cereb Blood Flow Metab 19: 1220-1228, 1999.
39. Lee JC, Greig A, Ravindranathan A, Parks TN, Rao MS. Molecular analysis of AMPA-specific receptors: subunit composition, editing, and calcium influx determination in small amounts of tissue. Brain Res Brain Res Protoc 3: 142-154, 1998.
40. Lehle L, Strahl S, Tanner W. Protein glycosylation, conserved from yeast to man: a model organism helps elucidate congenital human diseases. Angew Chem Int Ed Engl 45: 6802-6818, 2006.
41. Lipton P. Ischemic cell death in brain neurons. Physiol Rev 79: 1431-1568, 1999.
42. Lynch MA. Long-term potentiation and memory. Physiol Rev 84: 87-136, 2004.
43. Milton SL, Thompson JW, Lutz PL. Mechanisms for maintaining extracellular glutamate levels in the anoxic turtle striatum. Am J Physiol Regul Integr Comp Physiol 282: R1317-R1323, 2002.
44. Monyer H, Burnashev N, Laurie DJ, Sakmann B, Seeburg PH. Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12: 529-540, 1994.
45. Nilsson GE. Surviving anoxia with the brain turned on. News Physiol Sci 16: 217-221, 2001.
46. Nilsson GE, Lutz PL. Anoxia tolerant brains. J Cereb Blood Flow Metab 24: 475-486, 2004.
47. Nilsson GE, Lutz PL. Release of inhibitory neurotransmitters in response to anoxia in turtle brain. Am J Physiol Regul Integr Comp Physiol 261: R32-R37, 1991.
48. Nilsson GE, Rosen PR, Johansson D. Anoxic depression of spontaneous locomotor activity in crucian carp quantified by a computerized imaging technique. J Exp Biol 180: 153-162, 1993.
49. Ohtsubo K, Marth JD. Glycosylation in cellular mechanisms of health and disease. Cell 126: 855-867, 2006.
50. K1) in ventricular myocytes of crucian carp (Carassius carassius) heart. J Membr Biol 194: 119-127, 2003.
51. Palmer GC. Neuroprotection by NMDA receptor antagonists in a variety of neuropathologies. Curr Drug Targets 2: 241-271, 2001.
52. Pamenter ME, Shin DSH, Buck LT. AMPA receptors undergo channel arrest in the anoxic turtle cortex. Am J Physiol Regul Integr Comp Physiol 294: R606-R613, 2008.
53. Pellegrini-Giampietro DE, Zukin RS, Bennett MV, Cho S, Pulsinelli WA. Switch in glutamate receptor subunit gene expression in CA1 subfield of hippocampus following global ischemia in rats. Proc Natl Acad Sci USA 89: 10499-10503, 1992.
54. Perez-Pinzon MA, Rosenthal M, Sick TJ, Lutz PL, Pablo J, Mash D. Downregulation of sodium channels during anoxia: a putative survival strategy of turtle brain. Am J Physiol Regul Integr Comp Physiol 262: R712-R715, 1992.
55. Perez-Reyes E. Molecular physiology of low-voltage-activated T-type calcium channels. Physiol Rev 83: 117-161, 2003.
56. Perez-Velazquez JL, Zhang L. In vitro hypoxia induces expression of the NR2C subunit of the NMDA receptor in rat cortex and hippocampus. J Neurochem 63: 1171-1173, 1994.
57. Ramakers C, Ruijter JM, Deprez RH, Moorman AF. Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339: 62-66, 2003.
58. Regalado MP, Villarroel A, Lerma J. Intersubunit cooperativity in the NMDA receptor. Neuron 32: 1085-1096, 2001.
59. Rozen S, Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132: 365-386, 2000.
60. Small DL, Poulter MO, Buchan AM, Morley P. Alteration in NMDA receptor subunit mRNA expression in vulnerable and resistant regions of in vitro ischemic rat hippocampal slices. Neurosci Lett 232: 87-90, 1997.
61. Smith RW, Houlihan DF, Nilsson GE, Brechin JG. Tissue-specific changes in protein synthesis rates in vivo during anoxia in crucian carp. Am J Physiol Regul Integr Comp Physiol 271: R897-R904, 1996.
62. Sommer B, Keinanen K, Verdoorn TA, Wisden W, Burnashev N, Herb A, Kohler M, Takagi T, Sakmann B, Seeburg PH. Flip and flop: a cell-specific functional switch in glutamate-operated channels of the CNS. Science 249: 1580-1585, 1990.
63. Sprengel R. Role of AMPA receptors in synaptic plasticity. Cell Tissue Res 326: 447-455, 2006.
64. Szenasi G, Harsing LG. Pharmacology and prospective therapeutic usefulness of negative allosteric modulators of AMPA receptors. Drug Discov Today 1: 69-76, 2004.
65. Tai KK, Blondelle SE, Ostresh JM, Houghten RA, Montal M. An N-methyl-D-aspartate receptor channel blocker with neuroprotective activity. Proc Natl Acad Sci USA 98: 3519-3524, 2001.
66. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882, 1997.
67. Villmann C, Becker CM. On the hypes and falls in neuroprotection: targeting the NMDA receptor. Neuroscientist 13: 594-615, 2007.
68. Vornanen M, Paajanen V. Seasonality of dihydropyridine receptor binding in the heart of an anoxia-tolerant vertebrate, the crucian carp (Carassius carassius L.). Am J Physiol Regul Integr Comp Physiol 287: R1263-R1269, 2004.
69. Wada A, Takahashi H, Lipton SA, Chen HS. NR3A modulates the outer vestibule of the "NMDA" receptor channel. J Neurosci 26: 13156-13166, 2006.
70. Walton M, Woodgate AM, Muravlev A, Xu R, During MJ, Dragunow M. CREB phosphorylation promotes nerve cell survival. J Neurochem 73: 1836-1842, 1999.
71. Wang YH, Bosy TZ, Yasuda RP, Grayson DR, Vicini S, Pizzorusso T, Wolfe BB. Characterization of NMDA receptor subunit-specific antibodies: distribution of NR2A and NR2B receptor subunits in rat brain and ontogenic profile in the cerebellum. J Neurochem 65: 176-183, 1995.
72. Wenzel A, Fritschy JM, Mohler H, Benke D. NMDA receptor heterogeneity during postnatal development of the rat brain: differential expression of the NR2A, NR2B, and NR2C subunit proteins. J Neurochem 68: 469-478, 1997.
73. Wenzel A, Villa M, Mohler H, Benke D. Developmental and regional expression of NMDA receptor subtypes containing the NR2D subunit in rat brain. J Neurochem 66: 1240-1248, 1996.
74. Yao C, Williams AJ, Cui P, Berti R, Hunter JC, Tortella FC, Dave JR. Differential pattern of expression of voltage-gated sodium channel genes following ischemic brain injury in rats. Neurotox Res 4: 67-75, 2002.