Inhibition of adenosine deaminase by erythro-9-(2-hydroxy-3- nonyl)adenine (EHNA) mimics the effect of inescapable shock on escape learning in rats

Behavioral Neuroscience

Volumn 112, Issue 2, 1998, Pages 399-409

  Woodson, James C ^c   Minor, Thomas R ^b   Soames Job, R F ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NONE

Author keywords

[No Author keywords available]

Indexed keywords

9 (2 HYDROXY 3 NONYL)ADENINE; ADENOSINE; ADENOSINE DEAMINASE; CAFFEINE;

ANIMAL EXPERIMENT; ARTICLE; ENZYME INHIBITION; ESCAPE BEHAVIOR; LEARNED HELPLESSNESS; LEARNING; MALE; NONHUMAN; RAT;

ADENINE; ADENOSINE; ADENOSINE DEAMINASE; ANALYSIS OF VARIANCE; ANIMALS; CAFFEINE; CENTRAL NERVOUS SYSTEM STIMULANTS; ELECTROSHOCK; ENZYME INHIBITORS; ESCAPE REACTION; FEAR; HELPLESSNESS, LEARNED; MALE; NEURAL INHIBITION; RATS; RATS, SPRAGUE-DAWLEY; REACTION TIME; RECEPTORS, PURINERGIC P1; RESTRAINT, PHYSICAL; STRESS, PSYCHOLOGICAL;

EID: 0031978904     PISSN: 07357044     EISSN: None     Source Type: Journal    
DOI: 10.1037/0735-7044.112.2.399     Document Type: Article

References (88)

1. Agarwal, R. P. (1982). Inhibitors of adenosine deamiriase. Pharmacological Therapy, 17, 399-429.
2. Anisman, H., Remington, G., & Sklar, L. S. (1979). Effect of inescapable shock on subsequent escape performance: Catecholaminergic and cholinergic mediation of response initiation and maintenance. Psychopharmacology 61, 107-124.
3. Anisman, H., & Sklar, L. S. (1979). Catecholamine depletion in mice upon reexposure to stress: Mediation of the escape deficits produced by inescapable shock. Journal of Comparative and Physiological Psychology, 93, 610-625.
4. Anisman, H., & Zacharko, R. M. (1986). Behavioral and neurochemical consequences associated with Stressors. In D. D. Kelly (Ed.)., Annals of the New York Academy of Sciences: Stress- induced analgesia: Vol. 467 (pp. 205-225). New York: New York Academy of Sciences.
5. Arch, R. S., & Newsholme, E. A. (1978). Activities and some properties of 5′-nucleotidase, adenosine kinase and adenosine deaminase in tissues from vertebrates and invertebrates in relation to the control of the concentration and the physiological role of adenosine. Journal of Biochemistry, 174, 965-977.
6. Astrup, C. (1965). Pavlovian psychiatry: A new synthesis. Springfield, IL: Charles C Thomas.
7. Bruns, R. F. (1990). Structure activity relationship for adenosine antagonists. In K. A. Jacobson, J. W. Daly, & V. Manganiello (Eds.), Purines in cellular signaling: Targets for new drugs (pp. 126-135). Berlin, Germany: Springer-Verlag.
8. Choi, D. W. (1988). Glutamate neurotoxicity and diseases of the nervous system. Neuron, 1, 623-634.
9. Coffin, V. L., & Spealman, R. D. (1989). Psychomotor-stimulant actions of 3-isobutyl-1-methylxanthine: Comparison with caffeine and 7-(2-chloroethyl) theophylline. European Journal of Pharmacology, 170, 35-40.
10. Daly, J. W., Bruns, R. F., & Snyder, S. H. (1981). Adenosine receptors in the central nervous system: Relationship to the central actions of methylxanthines. Life Sciences, 28, 2083-2097.
11. Dowdall, M. J. (1978). Adenine nucleotides in cholinergic transmission: Presynaptic aspects. Journal of Physiology, 74, 497-501.
12. Drugan, R. C., Ryan, S. M., Minor, T. R., & Maier, S. F. (1984). Librium prevents the analgesia and shuttlebox escape deficit typically observed following inescapable shock. Pharmacology, Biochemistry and Behavior, 21, 749-754.
13. Engel, G. L., & Schmale, A. H. (1972). Conservation-withdrawal: A primary regulatory process for organismic homeostasis. Ciba Foundation Symposium, 8, 57-75.
14. Fredholm, B. B., Herrera-Marschitz, M., Jonzon, B., Lindstrom, K., & Ungerstedt, U. (1983). On the mechanism by which methylxanthines enhance apomorphine-induced rotation behaviour in the rat. Pharmacology Biochemistry and Behavior, 19, 535-541.
15. Geiger, J. D., Padua, R. A., & Nagy, J. I. (1991). Adenosine deaminase regulation of purine actions. In J. W. Phillis (Ed.), Adenosine and adenine nucleotides as regulators of cellular function (pp. 71-84). Boca Raton, FL: CRC Press.
16. Gould, R. J., Murphy, K. M. M., Katims, J. J., & Snyder, S. H. (1984). Caffeine actions and adenosine. Psychopharmacology Bulletin, 20, 436-440.
17. Gray, J. A. (1964). Pavlov's typology. New York: Macmillan.
18. Grossman, A., & Costa, A. (1993). The regulation of hypothalamic CRH: Impact of in vitro studies on the central control of the stress response. Functional Neurology, 8, 325-334.
19. Haracz, J. L., Minor, T. R., Wilkins, J. N., & Zimmermann, E. G. (1988). Learned helplessness: An experimental model of the DST in rats. Biological Psychiatry, 23, 388-396.
20. Harms, H. H., Wardeh, G., & Mulder, A. H. (1979). Effects of adenosine on depolarization-induced release of various radiolabelled neurotransmitters from slices of rat corpus striatum. Neuropharmacology, 18, 577-580.
21. Headrick, J. P., Bendall, M. R., Faden, A. I., & Vink, R. (1994). Dissociation of adenosine levels from bioenergetic state in experimental brain trauma: Potential role in secondary injury. Journal of Cerebral Blood Flow and Metabolism, 14, 853-861.
22. Hertz, L. (1978). Kinetics of adenosine uptake into astrocytes. Journal of Neurochemistry, 31, 55-62.
23. Hoehn, K., & White, T. D. (1990). Role of excitatory amino acid receptors in K+ and glutamate-evoked release of endogenous adenosine from rat cortical slices. Journal of Neurochemistry, 54, 256-265.
24. Karalis, K., Muglia, L. J., Bae, D., Hilderbrand, H., & Majzoub, J. A. (1997). CRH and the immune system. Journal of Neuroimmunology, 72(2), 131-136.
25. Kolassa, N., Plank, B., & Turnheim, K. (1978). pH and temperature-dependence of adenosine uptake in human erythrocytes. European Journal of Pharmacology, 52, 345-351.
26. Lloyd, H. G., Lindstrom, K., & Fredholm, B. B. (1993). Intracellular formation and release of adenosine from rat hippocampal slices evoked by electrical stimulation or energy depletion. Neurochemistry International, 23, 173-185.
27. Maier, S. F. (1990). The role of fear in mediating shuttle escape deficits produced by inescapable shock. Journal of Experimental Psychology: Animal Behavior Processes, 16, 137-149.
28. Maier, S. F. (1993). Learned helplessness, fear, and anxiety. In C. Stanford & P. Salmon (Eds.), Stress: From synapse to syndrome (pp. 207-248). London: Academic Press.
29. Maier, S. F., Albin, R. W., & Testa, T. J. (1973). Failure to learn to escape in rats previously exposed to inescapable shock depends on the nature of the escape response. Journal of Comparative and Physiological Psychology, 85, 581-592.
30. Maier, S. F., & Seligman, M. E. P. (1976). Learned helplessness: Theory and evidence. Journal of Experimental Psychology: General 105, 3-46.
31. Maier, S. F., & Watkins, L. R. (1995). Intracerebroventricular interleukin-1 receptor antagonist blocks the enhancement of fear conditioning and interference with escape produced by inescapable shock. Brain Research, 695, 279-282.
32. Martin, L. R., Lloyd, H. G. E., & Cowan, A. I. (1994). The early events of oxygen and glucose deprivation: Setting the scene for neuronal death? Trends in Neuroscience, 17, 251-256.
33. Meghji, P. (1991). Adenosine production and metabolism. In T. W. Stone (Ed.), Adenosine in the nervous system (pp. 25-42). London: Academic Press.
34. Mineka, S., Cook, M., & Miller, S. (1984). Fear conditioned following escapable and inescapable shock. Journal of Experimental Psychology: Animal Behavior Processes, 10, 307-324.
35. Minor, T. R. (1990). Conditioned fear and neophobia following inescapable shock. Animal Learning and Behavior, 18, 212-226.
36. Minor, T. R., Chang, W. C., & Winslow, J. L. (1994a). Stress and adenosine: I. Effect of methylxanthine and amphetamine stimulants on learned helplessness in rats. Behavioral Neuroscience, 108, 254-264.
37. Minor, T. R., Dess, N. K., Ben-David, E., & Chang, W. C. (1994b). Individual differences in vulnerability to inescapable shock in rats. Journal of Experimental Psychology: Animal Behavior Processes, 20, 402-412.
38. Minor, T. R., Dess, N. K., & Overmier, J. B. (1991). Inverting the traditional view of "learned helplessness." In M. R. Denny (Ed.), Fear, avoidance, & phobias: A fundamental analysis. Hillsdale, NJ: Erlbaum.
39. Minor, T. R., Job, R. F. S., Ferguson, E., & Saade, S. (1997). Stress and adenosine: III. Escape deficits induced by inescapable shock and metabolic inhibition are reversed by adenosine receptor antagonists. Manuscript submitted for publication.
40. Minor, T. R., & LoLordo, V. M. (1984). Escape deficits following inescapable shock: The role of contextual odor. Journal of Experimental Psychology: Animal Behavior Processes, 70, 168-181.
41. Minor, T. R., Pellymounter, M. A., & Maier, S. F. (1988). Uncontrollable shock, forebrain norepinephrine, and stimulus selection during choice escape learning. Psychobiology, 16, 135-145.
42. Minor, T. R., & Saade, S. (1997). Poststress glucose mitigates behavioral impairment in rats in the "learned helplessness" model of psychopathology. Biological Psychiatry, 42, 324-334.
43. Minor, T. R., Trauner, M. A., Lee, C. Y. & Dess, N. K. (1990). Modeling signal features of escape response: Effects of cessation conditioning in ''learned helplessness" paradigm. Journal of Experimental Psychology: Animal Behavior Processes, 16, 123-136.
44. Minor, T. R., Winslow, J. L., & Chang, W. C. (1994c). Stress and adenosine: II. Adenosine analogs mimic the effect of inescapable shock on shuttle-escape performance in rats. Behavioral Neuroscience, 108, 265-276.
45. Nagy, J. I., Geiger, J. D., & Staines, W. A. (1990). Adenosine deaminase and purinergic neuroregulation. Neurochemistry International, 16, 211-221.
46. Nehlig, A., Daval, J. L., & Boyet, S. (1994). Effects of selective adenosine A1 and A2 receptor agonists and antagonists on local rates of energy metabolism in the rat brain. European Journal of Pharmacology, 258, 57-66.
47. Newby, A. C. (1981). The interaction of inhibitors with adenosine metabolizing enzymes in intact isolated cells. Biochemical Pharmacology, 30, 2611-2615.
48. Newby, A. C. (1984). Adenosine and the concept of "retaliatory metabolites." Trends in Biochemical Science, 9, 42-44.
49. Northup, J. K. (1989). Regulation of cyclic nucleotides in the nervous system. In G. J. Siegel, B. W. Agranoff, R. W. Albers, & P. B. Molinoff (Eds.), Basic neitrochemistry: Molecular, cellular, and medical aspects (pp. 349-372). New York: Raven Press.
50. Novelli, A., Reilly, J. A., Lysko, P. G., & Henneberry, R. C. (1988). Glutamate becomes neurotoxic via the N-methyl-D-aspartate receptor when intracellular energy levels are reduced. Brain Research, 451, 205-212.
51. Orr, T. E., Meyerhoff, J. L., Mougey, E. H., & Bunnell, B. N. (1990). Hyperresponsiveness of the rat neuroendocrine system due to repeated exposure to stress. Psychoneuroendocrinology, 75, 317-328.
52. Oswald, I. (1959). Experimental studies of rhythm, anxiety and cerebral vigilance. Journal of Mental Sciences, 105, 269-294.
53. Oswald, I., Taylor, A. M., & Treisman, M. (1960). Discriminative responses to stimulation during human sleep. Brain, 83, 440-453.
54. Overmier, J. B., & Seligman, M. E. P. (1967). Effects of inescapable shock upon subsequent escape and avoidance responding. Journal of Comparative and Physiological Psychology, 63, 28-33.
55. Pavlov, I. P. (1927). Conditioned reflexes. Oxford, England: University Press.
56. Pavlov, I. P. (1941). Conditioned reflexes and psychiatry. New York: International Publishers Co., Inc.
57. Paxinos, G., & Watson, C. (1986). The rat brain in stereotaxic coordinates. (2nd ed.). New York: Academic Press.
58. Pellegrini-Giampietro, D. E., Cherici, G., Alesiani M., Caria, V., & Moroni, F. (1990). Excitatory amino acid release and free radical formation may cooperate in the genesis of ischemia-induced neuronal damage. Journal of Neuroscience, 10, 1035-1041.
59. Petty, F., & Sherman, A. D. (1980). Regional aspects of the prevention of learned helplessness by desiprimine. Life Science, 26, 1447-1452.
60. Podzuweit, T., Nennstiel, P., & Muller, A. (1995). Isozyme selective inhibition of cGMP-stimulated cyclic nucleotide phosphodiesterases by erythro-9-(2-hydroxy-3-nonyl) adenine. Cellular Signalling, 7, 733-738.
61. Radulovacki, M. (1982). N6(L-phenylisopropyl) adenosine (L-PIA) increases slow wave sleep and decreases wakefulness in rats. Brain Research, 246, 178-180.
62. Radulovacki, M., & Virus, R. M. (1988). Dose-response effects of 8-cyclopropyltheophylline on sleep and wakefulness in rats. Psychopharmacology, 94, 417-420.
63. Radulovacki, M., & Virus, R. M. (1995). A comparison of the dose response effects of pyrimidine ribonucleosides and adenosine on sleep in rats. Psychopharmacology, 87, 136-140.
64. Rail, T. W. (1982). Evolution of the mechanism of action of methylxanthines: From calcium mobilizers to antagonist of adenosine receptors. The 1982 Theodore Weicker Memorial Award Oration, 277-287.
65. Santos, M. S., Moreno, A. J., & Carvalho, A. P. (1996). Relationships between ATP depletion, membrane potential, and the release of neurotransmitters in rat nerve terminals: An in vitro study under conditions that mimic anoxia, hypoglycemia, and ischemia. Stroke, 27, 941-950.
66. Sapolsky, R. M. (1992). Stress in the aging brain, and the mechanisms of neuron death. Cambridge, MA: MIT Press.
67. Sapolsky, R. M., Krey, L. C., & McEwen, B. S. (1985). Prolonged glucocorticoid exposure reduces hippocampal neuron number: Implications for aging. Journal of Neuroscience, 5, 1222-1227.
68. Sattin, A., & Rail, T. W. (1970). The effect of adenosine and adenine nucleotides on the cyclic adenosine 3′,5′-phosphate content of guinea pig cerebral cortex slices. Molecular Pharmacology, 6, 13-23.
69. Sawynok, J., & Sweeney, M. I. (1989). The role of purines in nociception. Neuroscience, 32, 557-569.
70. Sciotti, V. M., Park, T. S., Berne, R. M., & Van Wylen, D. G. L. (1993). Changes in extracellular adenosine during chemical or electrical brain stimulation. Brain Research, 613, 16-20.
71. Sciotti, V. M., & Van Wylen, D. G. L. (1993). Increases in interstitial adenosine and cerebral blood flow with inhibition of adenosine kinase and adenosine deaminase. Journal of Cerebral Blood Flow and Metabolism, 13, 201-207.
72. Seligman, M. E., & Maier, S. F. (1967). Failure to escape traumatic shock. Journal of Experimental Psychology, 74, 1-9.
73. Selye, H. (1942). The story of the adaptation syndrome. Montreal. Canada: Acta, Inc.
74. Servatius, R. J., Ottenweller, J. E., & Natelson, B. H. (1995). Delayed startle sensitization distinguishes rats exposed to one or three stress sessions: Further evidence toward an animal model of PTSD. Biological Psychiatry, 38, 539-546.
75. Shors, T. J., & Servatius, R. J. (1995). Stress-induced sensitization and facilitated learning require NMDA receptor activation. Neuroreport, 6, 677-680.
76. Simson, P. E., & Weiss, J. M. (1988). Altered activity of the locus coeruleus in an animal model of depression. Neuropsychopharmacology, 1, 287-295.
77. Snyder, S. H., Katims, J. J., Annau, Z., Bruns, R. F., & Daly, J. W. (1981). Adenosine receptors and behavioral actions of methylxanthines. Proceedings of the National Academy of Sciences, 78, 3260-3264.
78. Sollevi, A., & Fredholm, B. B. (1981). Role of adenosine in adipose tissue circulation. Acta Physiologica Scandinavica, 112, 293-298.
79. Stone, T. W. (1981). Physiological roles of adenosine and adenosine 5′-triphosphate in the nervous system. Neuroscience, 6, 523-555.
80. Stone, T. W. (1991). Adenosine as a neuroactive compound in the central nervous system. In J. W. Phillis (Ed.), Adenosine and adenine nucleotides as regulators of cellular function (pp. 329-338). Boca Raton, FL: CRC Press.
81. Stone, T. W., & Taylor, D. A. (1978). An electrophysiological demonstration of a synergistic interaction between norepinephrine and adenosine in the cerebral cortex. Brain Research, 147, 396-400.
82. Taylor, D. A., & Stone, T. W. (1980). The action of adenosine and noradrenergic inhibition induced by stimulation of locus coeruleus. Brain Research, 183, 367-376.
83. Van Calker, D., Muller, M., & Hamprecht, B. (1979). Adenosine regulates via two different types of receptors the accumulation of cyclic AMP in cultured brain cells. Journal of Neurochemisiry, 33, 99-105.
84. Weiss, J. M., Goodman, P. A., Losito, B. G., Corrigan, S., Charry, J. M., & Bailey, W. H. (1981). Behavioral depression produced by an uncontrollable Stressor: Relationship to norepinephrine, dopamine, and serotonin in various regions of rat brain. Brain Research Reviews, 3, 167-205.
85. Weiss, J. M., & Simson, P. E. (1985). Mechanisms underlying stress-induced behavioral depression. In T. Field, P. McCabe, & N. Schneiderman (Eds.), Stress and coping (pp. 99-116). Hillsdale, NJ: Erlbaum.
86. Weiss, J. M., & Simson, P. E. (1988). Neurochemical and electrophysioiogical events underlying stress-induced depression in an animal model. Advances in Experimental Medicine und Biology, 245, 425-440.
87. Winder, D. G., & Conn, P. J. (1993). Activation of metabotropic glutamate receptors increases cAMP accumulation in hippocampus by potentiating responses to endogenous adenosine. Journal of Neuroscience, 13, 38-44.
88. Yager, J. Y., & Asselin, J. (1996). Effect of mild hypothermia on cerebral energy metabolism during the evolution of hypoxicischemic brain damage in the immature rat. Stroke, 27, 919-925.