A1 adenosine receptors mediate hypoglycemia-induced neuronal injury

Journal of Molecular Endocrinology

Volumn 32, Issue 1, 2004, Pages 129-144

  Turner, C P ^a,c   Blackburn, M R ^b   Rivkees, Scott A ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^c WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

8 CYCLOPENTYL 1,3 DIPROPYLXANTHINE; 9 CHLORO 2 (2 FURYL) 5 PHENYLACETYLAMINO 1,2,4 TRIAZOLO[1,5 C]QUINAZOLINE; 9 METHYLADENINE; ADENOSINE A1 RECEPTOR; ADENOSINE A1 RECEPTOR ANTAGONIST; CALCIUM; CASPASE 3; GLUCOSE; ADENOSINE; CASP3 PROTEIN, RAT; CASPASE; XANTHINE DERIVATIVE;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CELL DEATH; CELL ISOLATION; CELL VIABILITY; CONCENTRATION (PARAMETERS); CONFOCAL MICROSCOPY; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; HYPOGLYCEMIA; MOLECULAR MECHANICS; NERVE CELL LESION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STATISTICAL ANALYSIS; ANIMAL; BRAIN CORTEX; CELL SURVIVAL; DRUG ANTAGONISM; ENZYME ACTIVATION; METABOLISM; NERVE CELL; NERVOUS SYSTEM INJURY; PATHOPHYSIOLOGY; PHYSIOLOGY; PRENATAL DEVELOPMENT; SPRAGUE DAWLEY RAT;

ADENOSINE; ANIMALS; CALCIUM; CASPASE 3; CASPASES; CELL SURVIVAL; CEREBRAL CORTEX; EMBRYO; ENZYME ACTIVATION; HYPOGLYCEMIA; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, ADENOSINE A1; TRAUMA, NERVOUS SYSTEM; XANTHINES;

EID: 1542270997     PISSN: 09525041     EISSN: None     Source Type: Journal    
DOI: 10.1677/jme.0.0320129     Document Type: Article

References (75)

1. Agardh CD, Kalimo H, Olsson Y & Siesjo BK 1980 Hypoglycemic brain injury. I. Metabolic and light microscopic findings in rat cerebral cortex during profound insulin-induced hypoglycemia and in the recovery period following glucose administration. Acta Neuropathologica 50 31-41.
2. Auer RN 1986 Progress review: hypoglycemic brain damage. Stroke 17 699-708.
3. Auer RN & Siesjo BK 1993 Hypoglycaemia: brain neurochemistry and neuropathology. Bailliere's Clinical Endocrinology and Metabolism 7 611-625.
4. Barth A, Newell DW, Nguyen LB, Winn HR, Wender R, Meno JR & Janigro D 1997 Neurotoxicity in organotypic hippocampal slices mediated by adenosine analogues and nitric oxide. Brain Research 762 79-88.
5. Berridge MJ, Lipp P & Bootman MD 2000 The versatility and universality of calcium signalling. Nature Reviews. Molecular Cell Biology 1 11-21.
6. Blackburn MR, Datta SK & Kellems RE 1998 Adenosine deaminase-deficient mice generated using a two-stage genetic engineering strategy exhibit a combined immunodeficiency. Journal of Biological Chemistry 273 5093-5100.
7. Breder J, Sabelhaus CF, Opitz T, Reymann KG & Schroder UH 2000 Inhibition of different pathways influencing Na(+) homeostasis protects organotypic hippocampal slice cultures from hypoxic/hypoglycemic injury. Neuropharmacology 39 1779-1787.
8. Brewer GJ & Price PJ 1996 Viable cultured neurons in ambient carbon dioxide and hibernation storage for a month. Neuroreport 7 1509-1512.
9. Brewer GJ, Torricelli JR, Evege EK & Price PJ 1993 Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination. Journal of Neuroscience Research 35 567-576.
10. Butcher SP, Sandberg M, Hagberg H & Hamberger A 1987 Cellular origins of endogenous amino acids released into the extracellular fluid of the rat striatum during severe insulin-induced hypoglycemia. Journal of Neurochemistry 48 722-728.
11. Calabresi P, Centonze D, Pisani A & Bernardi G 1997 A possible mechanism for the aglycemia-induced depression of glutamatergic excitation in the striatum. Journal of Cerebral Blood Flow and Metabolism 17 1121-1126.
12. Cheng B & Mattson MP 1991 NGF and bFGF protect rat hippocampal and human cortical neurons against hypoglycemic damage by stabilizing calcium homeostasis. Neuron 7 1031-1041.
13. Cheng B, McMahon DG & Mattson MP 1993 Modulation of calcium current, intracellular calcium levels and cell survival by glucose deprivation and growth factors in hippocampal neurons. Brain Research 607 275-285.
14. Collatz MB, Rudel R & Brinkmeier H 1997 Intracellular calcium chelator BAPTA protects cells against toxic calcium overload but also alters physiological calcium responses. Cell Calcium 21 453-459.
15. Cooper AJ & Plum F 1987 Biochemistry and physiology of brain ammonia. Physiological Reviews 67 440-519.
16. Cox DW & Bachelard HS 1988 Partial attenuation of dentate granule cell evoked activity by the alternative substrates, lactate and pyruvate: evidence for a postsynaptic action. Experimental Brain Research 69 368-372.
17. Dixon AK, Gubitz AK, Sirinathsinghji DJ, Richardson PJ & Freeman TC 1996 Tissue distribution of adenosine receptor mRNAs in the rat. British Journal of Phamacology 118 1461-1468.
18. Duchen MR 2000 Mitochondria and calcium: from cell signalling to cell death. Journal of Physiology 529 57-68.
19. Dunwiddie TV & Masino SA 2001 The role and regulation of adenosine in the central nervous system. Annual Review of Neuroscience 24 31-55.
20. Fastbom J, Pazos A & Palacios JM 1987 The distribution of adenosine A1 receptors and 5′-nucleotidase in the brain of some commonly used experimental animals. Neuroscience 22 813-826.
21. Fink JS, Weaver DR, Rivkees SA, Peterfreund RA, Pollack AE, Adler EM & Reppert SM 1992 Molecular cloning of the rat A2 adenosine receptor: selective co-expression with D2 dopamine receptors in rat striatum. Brain Research. Molecular Brain Research 14 186-195.
22. Fowler JC 1993 Glucose deprivation results in a lactate preventable increase in adenosine and depression of synaptic transmission in rat hippocampal slices. Journal of Neurochemistry 60 572-576.
23. Franklin JL & Johnson EM Jr 1992 Suppression of programmed neuronal death by sustained elevation of cytoplasmic calcium. Trends in Neurosciences 15 501-508.
24. Fredholm BB, Abbracchio MP, Burnstock G, Daly JW, Harden TK, Jacobson KA, Leff P & Williams M 1994 Nomenclature and classification of purinoceptors. Pharmacological Reviews 46 143-156.
25. Haas HL & Selbach O 2000 Functions of neuronal adenosine receptors. Naunyn-Schmiedeberg's Archives of Pharmacology 362 375-381.
26. Han KS, Kang HJ, Kim EY, Yoon WJ, Sohn S, Kwon HJ & Gwag BJ 2001 1,2-bis(2-Aminophenoxy)ethane-N,N,N′,N′-tetraacetic acid induces caspase-mediated apoptosis and reactive oxygen species-mediated necrosis in cultured cortical neurons. Journal of Neurochemistry 78 230-239.
27. Hawdon JM 1999 Hypoglycaemia and the neonatal brain. European Journal of Pediatrics 158 (Suppl 1) S9-S12.
28. Hertz L, Yu AC, Kala G & Schousboe A 2000 Neuronal-astrocytic and cytosolic-mitochondrial metabolite trafficking during brain activation, hyperammonemia and energy deprivation. Neurochemistry International 37 83-102.
29. Honegger P, Braissant O, Henry H, Boulat O, Bachmann C, Zurich MG & Pardo B 2002 Alteration of amino acid metabolism in neuronal aggregate cultures exposed to hypoglycaemic conditions. Journal of Neurochemistry 81 1141-1151.
30. Ikonomidou C, Bosch F, Miksa M, Bittigau P, Vockler J, Dikranian K, Tenkova TI, Stefovska V, Turski L & Olney JW 1999 Blockade of NMDA receptors and apoptotic neurodegeneration in the developing brain. Science 283 70-74.
31. Izumi Y, Benz AM, Zorumski CF & Olney JW 1994 Effects of lactate and pyruvate on glucose deprivation in rat hippocampal slices. Neuroreport 5 617-620.
32. Johnson EM Jr, Koike T & Franklin J 1992a A 'calcium set-point hypothesis' of neuronal dependence on neurotrophic factor. Experimental Neurology 115 163-166.
33. Johnson EM Jr, Koike T & Franklin J 1992b A 'calcium set-point hypothesis' of neuronal dependence on neurotrophic factor. Experimental Neurology 115 163-166.
34. Kluck RM, McDougall CA, Harmon BV & Halliday JW 1994 Calcium chelators induce apoptosis - evidence that raised intracellular ionised calcium is not essential for apoptosis. Biochimica et Biophysica Acta 1223 247-254.
35. Knudsen TB, Winters RS, Otey SK, Blackburn MR, Airhart MJ, Church JK & Skalko RG 1992 Effects of (R)-deoxycoformycin (pentostatin) on intrauterine nucleoside catabolism and embryo viability in the pregnant mouse. Teratology 45 91-103.
36. Koshiba M, Kosaka H, Nakazawa T, Hayashi N, Saura R, Kitamura N & Kumagai S 2002 2-Chloroadenosine but not adenosine induces apoptosis in rheumatoid fibroblasts independently of cell surface adenosine receptor signalling. British Journal of Pharmacology 135 1477-1486.
37. i in the ATP-induced heat sensitization process of rat nociceptive neurons. Journal of Neurophysiology 81 2612-2619.
38. Lobner D & Choi DW 1994 Dipyridamole increases oxygen-glucose deprivation-induced injury in cortical cell culture. Stroke 25 2085-2089 [discussion 2089-2090].
39. Lohse MJ, Klotz KN, Lindenborn-Fotinos J, Reddington M, Schwabe U & Olsson RA 1987 8-Cyclopentyl-1,3-dipropylxanthine (DPCPX - a selective high affinity antagonist radioligand for A1 adenosine receptors. Naunyn-Schmiedeberg's Archives of Pharmacology 336 204-210.
40. Mattson MP, Zhang Y & Bose S 1993 Growth factors prevent mitochondrial dysfunction, loss of calcium homeostasis, and cell injury, but not ATP depletion in hippocampal neurons deprived of glucose. Experimental Neurology 121 1-13.
41. McGowan JE, Zanelli SA, Haynes-Laing AG, Mishra OP & Delivoria-Papadopoulos M 2002 Modification of glutamate binding sites in newborn brain during hypoglycemia. Brain Research 927 80-86.
42. Merkel LA, Rivera LM, Colussi DJ, Perrone MH, Smits GJ & Cox BF 1993 In vitro and in vivo characterization of an A1-selective adenosine agonist, RG14202. Journal of Pharmacology and Experimental Therapeutics 265 699-706.
43. Mobbs CV, Kow LM & Yang XJ 2001 Brain glucose-sensing mechanisms: ubiquitous silencing by aglycemia vs. hypothalamic neuroendocrine responses. American Journal of Physiology. Endocrinology and Metabolism 281 E649-E654.
44. Moran J, Itoh T, Reddy UR, Chen M, Alnemri ES & Pleasure D 1999 Caspase-3 expression by cerebellar granule neurons is regulated by calcium and cyclic AMP. Journal of Neurochemistry 73 568-577.
45. Mynlieff M & Beam KG 1994 Adenosine acting at an A1 receptor decreases N-type calcium current in mouse motoneurons. Journal of Neuroscience 14 3628-3634.
46. Nicholson DW 1999 Caspase structure, proteolytic substrates, and function during apoptotic cell death. Cell Death and Differentiation 6 1028-1042.
47. Nonner D, Barrett EF & Barrett JN 2000 Brief exposure to neurotrophins produces a calcium-dependent increase in choline acetyltransferase activity in cultured rat septal neurons. Journal of Neurochemistry 74 988-999.
48. Olah ME & Stiles GL 1995 Adenosine receptor subtypes: characterization and therapeutic regulation. Annual Review of Pharmacology and Toxicology 35 581-606.
49. Ouanonou A, Zhang Y & Zhang L 1999 Changes in the calcium dependence of glutamate transmission in the hippocampal CA1 region after brief hypoxia-hypoglycemia. Journal of Neurophysiology 82 1147-1155.
50. Ouyang YB, He QP, Li PA, Janelidze S, Wang GX & Siesjo BK 2000 Is neuronal injury caused by hypoglycemic coma of the necrotic or apoptotic type? Neurochemical Research 25 661-667.
51. Reppert SM, Weaver DR, Stehle JH & Rivkees SA 1991 Molecular cloning and characterization of a rat A1-adenosine receptor that is widely expressed in brain and spinal cord. Molecular Endocrinology 5 1037-1048.
52. Rivkees SA, Price SL & Zhou FC 1995 Immunohistochemical detection of A1 adenosine receptors in rat brain with emphasis on localization in the hippocampal formation, cerebral cortex, cerebellum, and basal ganglia. Brain Research 677 193-203.
53. Rivkees SA, Thevananther S & Hao H 2000 Are A3 adenosine receptors expressed in the brain? Neuroreport 11 1025-1030.
54. Rivkees SA, Zhao Z, Porter G & Turner C 2001 Influences of adenosine on the fetus and newborn. Molecular Genetics and Metabolism 74 160-171.
55. Rotman B & Papermaster BW 1966 Membrane properties of living mammalian cells as studied by enzymatic hydrolysis of fluorogenic esters. PNAS 55 134-141.
56. Silver IA, Deas J & Erecinska M 1997 Ion homeostasis in brain cells: differences in intracellular ion responses to energy limitation between cultured neurons and glial cells. Neuroscience 78 589-601.
57. Simpson RE, O'Regan MH, Perkins LM & Phillis JW 1992 Excitatory transmitter amino acid release from the ischemic rat cerebral cortex: effects of adenosine receptor agonists and antagonists. Journal of Neurochemistry 58 1683-1690.
58. Tekkok SB, Godfraind JM & Krnjevic K 2002 Moderate hypoglycemia aggravates effects of hypoxia in hippocampal slices from diabetic rats. Neuroscience 113 11-21.
59. Thastrup O, Cullen PJ, Drobak BK, Hanley MR & Dawson AP 1990 Thapsigargin, a tumor promoter, discharges intracellular Ca2+ stores by specific inhibition of the endoplasmic reticulum Ca2(+)-ATPase. PNAS 87 2466-2470.
60. Turner CP, Pulciani D & Rivkees SA 2002a Reduction in intracellular calcium levels induces injury in developing neurons. Experimental Neurology 178 21-32.
61. Turner CP, Yan H, Schwartz M, Othman T & Rivkees SA 2002b A1 adenosine receptor activation induces ventriculomegaly and white matter loss. Neuroreport 13 1199-1204.
62. Turner CP, Seli M, Ment L, Stewart W, Yan H, Johansson B, Fredholm BB, Blackburn M & Rivkees SA 2003 A1 adenosine receptors mediate hypoxia-induced ventriculomegaly. PNAS 100 11718-11722.
63. Ukena D, Padgett WL, Hong O, Daly JW, Daly DT & Olsson RA 1987 N6-substituted 9-methyladenines: a new class of adenosine receptor antagonists. FEBS Letters 215 203-208.
64. Vannucci RC & Yager JY 1992 Glucose, lactic acid, and perinatal hypoxic-ischemic brain damage. Pediatric Neurology 8 3-12.
65. Vannucci RC & Vannucci SJ 2001 Hypoglycemic brain injury. Seminars in Neonatology 6 147-155.
66. von Lubitz DK 1999 Adenosine and cerebral ischemia: therapeutic future or death of a brave concept? European Journal of Pharmacology 371 85-102.
67. von Lubitz DK & Marangos PJ 1990 Cerebral ischemia in gerbils: postischemic administration of cyclohexyl adenosine and 8-sulfophenyl-theophylline. Journal of Molecular Neuroscience 2 53-59.
68. Wieloch T 1985 Hypoglycemia-induced neuronal damage prevented by an N-methyl-D-aspartate antagonist. Science 230 681-683.
69. Wolf HK, Buslei R, Schmidt-Kastner R, Schmidt-Kastner PK, Pietsch T, Wiestler OD & Bluhmke I 1996 NeuN: a useful neuronal marker for diagnostic histopathology. Journal of Histochemistry and Cytochemistry 44 1167-1171.
70. Wu LG & Saggau P 1994 Adenosine inhibits evoked synaptic transmission primarily by reducing presynaptic calcium influx in area CA1 of hippocampus. Neuron 12 1139-1148.
71. Yager JY, Heitjan DF, Towfighi J & Vannucci RC 1992 Effect of insulin-induced and fasting hypoglycemia on perinatal hypoxic-ischemic brain damage. Pediatric Research 31 138-142.
72. Yuan J, Shaham S, Ledoux S, Ellis HM & Horvitz HR 1993 The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1 beta-converting enzyme. Cell 75 641-652.
73. Zhu LP, Yu XD, Ling S, Brown RA & Kuo TH 2000 Mitochondrial Ca(2+)homeostasis in the regulation of apoptotic and necrotic cell deaths. Cell Calcium 28 107-117.
74. Zhu PJ & Krnjevic K 1993 Adenosine release is a major cause of failure of synaptic transmission during hypoglycaemia in rat hippocampal slices. Neuroscience Letters 155 128-131.
75. Zipfel GJ, Babcock DJ, Lee JM & Choi DW 2000 Neuronal apoptosis after CNS injury: the roles of glutamate and calcium. Journal of Neurotrauma 17 857-869.