Enhancing Brain Adenosine Signaling With the Nucleoside Transport Blocker NBTI (S-(4-Nitrobenzyl)-6-Theoinosine) Mimics the Effects of Inescapable Shock on Later Shuttle-Escape Performance in Rats

Behavioral Neuroscience

Volumn 122, Issue 6, 2008, Pages 1236-1247

  Minor, Thomas R ^a   Rowe, Michael ^a   Cullen, Patrick K ^a   Furst, Stephanie ^a  

^a UNIVERSITY OF CALIFORNIA

Author keywords

A2A receptor; adenosine transporter; depression; helplessness; rat

Indexed keywords

8 (3 CHLOROSTYRYL)CAFFEINE; 8 CYCLOPENTYL 1,3 DIPROPYLXANTHINE; ADENOSINE; ADENOSINE A2A RECEPTOR; ADENOSINE RECEPTOR BLOCKING AGENT; CAFFEINE; NITROBENZYLTHIOINOSINE;

ANIMAL EXPERIMENT; ARTICLE; BRAIN METABOLISM; CONTROLLED STUDY; DEPRESSION; DOSE RESPONSE; ELECTRIC SHOCK; ESCAPE BEHAVIOR; HELPLESSNESS; IMMOBILIZATION STRESS; MALE; NONHUMAN; PERFORMANCE; POSTTRAUMATIC STRESS DISORDER; RAT; RECEPTOR INTRINSIC ACTIVITY;

ADENOSINE; ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; BRAIN; CAFFEINE; ELECTROSHOCK; ESCAPE REACTION; FREEZING REACTION, CATALEPTIC; MALE; NUCLEOSIDE TRANSPORT PROTEINS; PHOSPHODIESTERASE INHIBITORS; RATS; RATS, SPRAGUE-DAWLEY; REACTION TIME; SIGNAL TRANSDUCTION; THIOINOSINE; XANTHINES;

EID: 57049092803     PISSN: 07357044     EISSN: None     Source Type: Journal    
DOI: 10.1037/a0013143     Document Type: Article

References (89)

1. Anisman H., Remington G., and Sklar L.S. Effect of inescapable shock on subsequent escape performance: Catecholaminergic and cholinergic mediation of response initiation and maintenance. Psychopharmacology 61 (1979) 107-124
2. Anisman H., and Sklar L.S. Catecholamine depletion in mice upon reexposure to stress: Mediation of the escape deficits produced by inescapable shock. Journal of Comparative and Physiological Psychology 93 (1979) 610-625
3. Anisman H., and Zacharko R.M. Behavioral and neurochemical consequences associated with stressors. In: Kelly D.D. (Ed). Annals of the New York Academy of Sciences: Stress-induced analgesia 467 (1986), New York Academy of Sciences, New York 205-225
4. Arch R.S., and Newsholme E.A. 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 (1978) 965-977
5. Bodnar R.J., Kelly D.D., and Glusman M. 2-deoxy-D-glucose analgesia: Influence of opiate and nonopiate factors. Pharmacology, Biochemistry, and Behavior 21 (1979) 749-754
6. Bruns R.F., Lu G.H., and Pugsley T.A. Characterization of the A2 adenosine receptor labeled by [3H]NECA in rat striatal membranes. Molecular Pharmacology 29 (1986) 331-346
7. Calon F., Dridi M., Hornykiewicz O., Bédard P.J., Rajput A.H., and Di Paolo T. Increased adenosine A2A receptors in the brain of Parkinson's disease patients with dyskinesias. Brain 127 (2004) 1075-1084
8. Castillo-Meléndez M., Krstew E., Lawrence A.J., and Jarrott B. Presynaptic adenosine A2a receptors on soma and central terminals of rat vagal afferent neurons. Brain Research 652 (1994) 137-144
9. Coleman C.G., Baghdoyan H.A., and Lydic R. Dialysis delivery of an adenosine A2A agonist into the pontine reticular formation of C57BL/6J mouse increases pontine acetylcholine release and sleep. Journal of Neurochemistry 96 (2006) 1750-1759
10. Corset V., Nguyen-Ba-Charvet K.T., Forcet C., Moyse E., Chedotal A., and Mehlen P. Netrin-1-mediated axon outgrowth and cAMP production requires interaction with adenosine A2b receptor. Nature 407 (2000) 747-750
11. Dubey R.K., Gillespie D.G., and Jackson E.K. A (2B) adenosine receptors stimulate growth of porcine and rat arterial endothelial cells. Hypertension 39 (2002) 530-535
12. Dunwiddie T.V., and Fredholm B.B. Adenosine modulation of synaptic responses in rat hippocampus: Possible role of inhibition or activation of adenylate cyclase. Advances in Cyclic Nucleotide Protein Phosphorylation Research 19 (1985) 259-272
13. El Yacoubi M., Ledent C., Parmentier M., Bertorelli R., Ongini E., Costentin J., et al. Adenosine A2A receptor antagonists are potential antidepressants: Evidence based on pharmacology and A2A receptor knockout mice. British Journal of Pharmacology 134 (2001) 68-77
14. El Yacoubi M., and Vaugeois J.M. Genetic rodent models of depression. Current Opinion in Pharmacology 7 (2007) 3-7
15. Engel G.L., and Schmale A.H. Conservation-withdrawal: A primary regulatory process for organismic homeostasis. Ciba Foundation Symposium 8 (1972) 57-75
16. Ferré S., Diamond I., Goldberg S.R., Yao L., Hourani S.M., Huang Z.L., et al. Adenosine A2A receptors in ventral striatum, hypothalamus and nociceptive circuitry implications for drug addiction, sleep and pain. Progress in Neurobiology 83 (2007) 332-347
17. Ferré S., Fuxe K., von Euler G., Johansson B., and Fredholm B. Adenosine-dopamine interactions in the brain. Neuroscience 51 (1992) 501-512
18. Fisone G., Håkansson K., Borgkvist A., and Santini E. Signaling in the basal ganglia: Postsynaptic and presynaptic mechanisms. Physiology & Behavior 92 (2007) 8-14
19. Fredholm B.B., and Dunwiddie T.V. How does adenosine inhibit transmitter release?. Trends Pharmacological Science 9 (1988) 130-134
20. Geiger J.D., Padua R.A., and Nagy J.I. Adenosine deaminase regulation of purine actions. In: Phillis J.W. (Ed). Adenosine and adenine nucleotides as regulators of cellular function (1991), CRC Press, Boca Raton 71-84
21. Gessi S., Merighi S., Varani K., Leung E., Mac Lennan S., and Borea P.A. The A3 adenosine receptor: An enigmatic player in cell biology. Pharmacological Therapeutics 117 (2008) 123-140
22. Haas H.L., and Selbach O. Functions of neuronal adenosine receptors. Naunyn Schmiedebergs Archives of Pharmacology 362 (2000) 375-381
23. 2A signaling in two rat models of depression. Biological Psychiatry (2008) submitted
24. Harms H.H., Wardeh G., and Mulder A.H. Effect of adenosine on depolarization-induced release of various radiolabelled neurotransmitters from slices of rat corpus striatum. Neuropharmacology 18 (1979) 577-580
25. Headrick J.P., Bendall M.R., Faden A.I., and Vink R. Dissociation of adenosine levels from bioenergetic state in experimental brain trauma: Potential role in secondary injury. Journal of Cerebral Blood Flow and Metabolism 14 (1994) 853-861
26. Hoehn K., and White T.D. Role of excitatory amino acid receptors in K+ and glutamate-evoked release of endogenous adenosine from rat cortical slices. Journal of Neurochemistry 54 (1990) 256-265
27. Hunter A.M., Balleine B.W., and Minor T.R. Helplessness and escape performance: Glutamate-adenosine interactions in the frontal cortex. Behavioral Neuroscience 117 (2003) 123-135
28. Ishiwata K., Mishina M., Kimura Y., Oda K., Sasaki T., and Ishii K. First visualization of adenosine A (2A) receptors in the human brain by positron emission tomography with [11C]TMSX. Synapse 55 (2005) 133-136
29. Jackson R.L., and Minor T.R. Effects of signaling inescapable shock on subsequent escape learning: Implications for theories of coping and "learned Helplessness". Journal of Experimental Psychology: Animal Behavior Processes 14 (1988) 400-439
30. Jacobson K.A., van Galen P.J., and Williams M. Adenosine receptors: Pharmacology, structure-activity relationships, and therapeutic potential. Journal of Medicinal Chemistry 35 (1992) 407-422
31. Linden J. Structure and function of A1 adenosine receptors. FASEB Journal 5 (1991) 2668-2676
32. Linden J., Taylor H.E., Robeva A.S., Tucker A.L., Stehle J.H., Rivkees S.A., et al. Molecular cloning and functional expression of a sheep A3 adenosine receptor with widespread tissue distribution. Molecular Pharmacology 44 (1993) 524-532
33. Lloyd H.G., Lindstrom K., and Fredholm B.B. Intracellular formation and release of adenosine from rat hippocampal slices evoked by electrical stimulation or energy depletion. Neurochemistry International 23 (1993) 173-185
34. Maier S.F. The role of fear in mediating shuttle escape deficits produced by inescapable shock. Journal of Experimental Psychology: Animal Behavior Processes 16 (1990) 137-149
35. Maier S.F. Learned helplessness, fear, and anxiety. In: Stanford C., and Salmon P. (Eds). Stress: From synapse to syndrome (1993), Academic Press, London 207-248
36. Maier S.F., Albin R.W., and Testa T.J. 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 (1973) 581-592
37. Maier S.F., and Seligman M.E.P. Learned helplessness: Theory and evidence. Journal of Experimental Psychology: General 105 (1976) 3-46
38. Meghji P. Adenosine production and metabolism. In: Stone T.W. (Ed). Adenosine in the nervous system (1991), Academic Press, London 25-42
39. Mineka S., Cook M., and Miller S. Fear conditioned following escapable and inescapable shock. Journal of Experimental Psychology: Animal Behavior Processes 10 (1984) 307-324
40. Minor T.R. Conditioned fear and neophobia following inescapable shock. Animal Learning & Behavior 18 (1990) 212-226
41. Minor T.R., Chang W.C., and Winslow J.L. Stress and adenosine: I. Effect of methylxanthine and amphetamine stimulants on learned helplessness in rats. Behavioral Neuroscience 108 (1994) 254-264
42. Minor T.R., Dess N.K., Ben-David E., and Chang W.C. Individual differences in vulnerability to inescapable shock in rats. Journal of Experimental Psychology: Animal Behavior Processes 20 (1994) 402-412
43. Minor T.R., Dess N.K., and Overmier J.B. Inverting the traditional view of "Learned Helplessness.". In: Denny M.R. (Ed). Fear, avoidance, & phobias: A fundamental analysis (1991), Lawrence-Erlbaum Associates, Hillsdale
44. Minor, T. R., Foley, E. A., Cservenka, A., & Sweeney, J. B. (2008). Glucose treatment following traumatic stress eliminates symptoms of behavioral agitation, fearfulness, and helplessness. Manuscript submitted for publication.
45. Minor, T. R., & Hanff, T. (2008). Adenosine signaling in reserpine-induced depression in rats. Behavioral Brain Research (in press).
46. 2A receptor antagonists. Brain, Immunity & Behavior (2008) (under review)
47. Minor T.R., Huang Q., and Foley E.A. Cytokine-purine interactions in behavioral depression in rats. Integrative Physiology and Behavioral Science 38 (2003) 189-202
48. Minor T.R., Huang Q., and Witt A.E. Cytokine-Purine interactions in traumatic stress, behavioral depression, and sickness. CNS & Neurological Disorders-Drug Targets 5 (2006) 547-560
49. Minor T.R., and Hunter A.M. Stressor controllability and learned helplessness research in the United States: Sensitization and fatigue processes. Integrative Physiology and Behavioral Science 37 (2002) 44-58
50. Minor T.R., and LoLordo V.M. Escape deficits following inescapable shock: The role of contextual odor. Journal of Experimental Psychology: Animal Behavior Processes 10 (1984) 168-181
51. Minor T.R., Pellymounter M.A., and Maier S.F. Uncontrollable shock, forebrain norepinephrine, and stimulus selection during choice escape learning. Psychobiology 16 (1988) 135-145
52. Minor T.R., Trauner M.A., Lee C.Y., and Dess N.K. Modeling signal features of escape response: Effects of cessation conditioning in "learned helplessness" paradigm. Journal of Experimental Psychology: Animal Behavior Processes 16 (1990) 123-136
53. Minor T.R., Winslow J.L., and Chang W.C. Stress and adenosine: II. Adenosine analogs mimic the effect of inescapable shock on shuttle-escape performance in rats. Behavioral Neuroscience 108 (1994) 265-276
54. Mishina M., Ishiwata K., Kimura Y., Naganawa M., Oda K., Kobayashi S., et al. Evaluation of distribution of adenosine A2A receptors in normal human brain measured with [11C]TMSX PET. Synapse 61 (2007) 778-784
55. Nagy J.I., Geiger J.D., and Staines W.A. Adenosine deaminase and purinergic neuroregulation. Neurochemistry International 16 (1990) 211-221
56. Nehlig A., Daval J.L., and Boyet S. 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 (1994) 57-66
57. Newby A.C. The interaction of inhibitors with adenosine metabolizing enzymes in intact isolated cells. Biochemical Pharmacology 30 (1981) 2611-2615
58. Newby A.C. Adenosine and the "concept of retaliatory metabolites.". Trends in Biochemical Science 9 (1984) 42-44
59. Noji T., Karasawa A., and Ksuka H. Adenosine uptake inhibitors. European Journal of Pharmacology 495 (2004) 1-16
60. Orr T.E., Meyerhoff J.L., Mougey E.H., and Bunnell B.N. Hyperresponsiveness of the rat neuroendocrine system due to repeated exposure to stress. Psychoneuroendocrinology 15 (1990) 317-328
61. Overmier J.B., and Seligman M.E.P. Effects of inescapable shock upon subsequent escape and avoidance responding. Journal of Comparative and Physiological Psychology 63 (1967) 28-33
62. Paxinos G., and Watson C. The rat brain in stereotaxic coordinates (1982), Academic Press, New York
63. Petty F., and Sherman A.D. Regional aspects of the prevention of learned helplessness by desiprimine. Life Science 26 (1980) 1447-1452
64. Phillis J.W. Adenosine and adenine nucleotides as regulators of cerebral blood flow: Roles of acidosis, cell swelling, and KATP channels. Critical Reviews in Neurobiology 16 (2004) 237-270
65. Santos M.S., Moreno A.J., and Carvalho A.P. 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 (1996) 941-950
66. Sattin A., and Rall T.W. The effect of adenosine and adenine nucleotides on the cyclic adenosine 3′,5′-Phosphate content of guinea pig cerebral cortex slices. Molecular Pharmacology 6 (1970) 13-23
67. Sawynok J., and Sweeney M.I. The role of purines in nociception. Neuroscience 32 (1989) 557-569
68. Sciotti V.M., Park T.S., Berne R.M., and VanWylen D.G.L. Changes in extracellular adenosine during chemical or electrical brain stimulation. Brain Research 613 (1993) 16-20
69. Sciotti V.M., and Van Wylen D.G. Increases in interstitial adenosine and cerebral blood flow with inhibition of adenosine kinase and adenosine deaminase. Journal of Cerebral Blood Flow and Metabolism 13 (1993) 201-207
70. Scislo T.J., and O'Leary D.S. Vasopressin V1 receptors contribute to hemodynamic and sympathoinhibitory responses evoked by stimulation of adenosine A2a receptors in NTS. American Journal of Heart Circulation Physiology 290 (2006) H1889-98
71. Sebastião A.M., and Ribeiro J.A. Adenosine A2 receptor-mediated excitatory actions on the nervous system. Progress in Neurobiology 48 (1996) 167-189
72. Selye H. The Story of the Adaptation Syndrome (1942), Acta, Inc, Montreal
73. Shors T.J., and Servatius R.J. Stress-induced sensitization and facilitated learning require NMDA receptor activation. Neuroreport 6 (1995) 677-680
74. Simson P.E., and Weiss J.M. Altered activity of the locus coeruleus in an animal model of depression. Neuropsychopharmacology 1 (1988) 287-295
75. Snyder S.H., Katims J.J., Annau Z., Bruns R.F., and Daly J.W. Adenosine receptors and behavioral actions of methylxanthines. Proceedings of the National Academy of Sciences, USA 78 (1981) 3260-3264
76. Sollevi A., and Fredholm B.B. Role of adenosine in adipose tissue circulation. Acta Physiologica Scandinavica 112 (1981) 293-298
77. Stone T.W. Physiological roles of adenosine and adenosine 5′triphosphate in the nervous system. Neuroscience 6 (1981) 523-555
78. Stone T.W. Adenosine as a neuroactive compound in the central nervous system. In: Phillis J.W. (Ed). Adenosine and adenine nucleotides as regulators of cellular function (1991), CRC Press, Boca Raton 329-338
79. Stone T.W., and Taylor D.A. An electrophysiological demonstration of a synergistic interaction between norepinephrine and adenosine in the cerebral cortex. Brain Research 147 (1978) 396-400
80. Svenningsson P., Le Moine C., Fisone G., and Fredholm B.B. Distribution, biochemistry and function of striatal adenosine A2A receptors. Progress in Neurobiology 59 (1999) 355-396
81. Taylor D.A., and Stone T.W. The action of adenosine and noradrenergic inhibition induced by stimulation of locus coeruleus. Brain Research 183 (1980) 367-376
82. Tromp R.A., van Ameijde S., Pütz C., Sundermann C., Sundermann B., von Frijtag Drabbe Künzel J.K., et al. Inhibition of nucleoside transport by new analogues of 4-nitrobenzylthionosine: Replacement of the ribose moiety by substituted benzyl groups. Journal of Medical Chemistry 47 (2004) 5441-5450
83. Van Calker D., Muller M., and Hamprecht B. Adenosine regulates via two different types of receptors the accumulation of cyclic AMP in cultured brain cells. Journal of Neurochemistry 33 (1979) 99-1005
84. Weaver D.R. A2a adenosine receptor gene expression in developing rat brain. Molecular Brain Research 20 (1993) 313-327
85. Weiss J.M., Goodman P.A., Losito B.G., Corrigan S., Charry J.M., and Bailey W.H. Behavioral depression produced by an uncontrollable stressor: Relationship to norepinephrine, dopamine, and serotonin in various regions of rat brain. Brain Research Reviews 3 (1981) 167-205
86. Weiss J.M., and Simson P.E. Mechanisms underlying stress-induced behavioral depression. In: Field T., McCabe P., and Schneiderman N. (Eds). Stress and coping (1985), Lawrence-Erlbaum Associates, Hillsdale 99-116
87. Weiss J.M., and Simson P.E. Neurochemical and electrophysiological events underlying stress-induced depression in an animal model. Advances in Experimental Medicine and Biology 245 (1988) 425-440
88. Winder D.G., and Conn P.J. Activation of metabotropic glutamate receptors increases cAMP accumulation in hippocampus by potentiating responses to endogenous adenosine. Journal of Neuroscience 13 (1993) 38-44
89. Woodson J.C., Minor T.R., and Job R.F. 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 112 (1998) 399-409