Activation of pedunculopontine tegmental protein kinase A: A mechanism for rapid eye movement sleep generation in the freely moving rat

Journal of Neuroscience

Volumn 26, Issue 35, 2006, Pages 8931-8942

  Bandyopadhya, Ram S ^a   Datta, Subimal ^a   Saha, Subhash ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Anterior hypothalamus; Medial pontine reticular formation; Medial prefrontal cortex; Pedunculopontine tegmentum; REM sleep; Signal transduction

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; PROTEIN KINASE C ALPHA; PROTEIN KINASE R; PROTEIN KINASE R1; PROTEIN KINASE R2A; PROTEIN KINASE R2B; UNCLASSIFIED DRUG;

ANATOMICAL VARIATION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTERIOR HYPOTHALAMUS; ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVATION; MALE; NONHUMAN; PEDUNCULOPONTINE TEGMENTAL NUCLEUS; PONS RETICULAR FORMATION; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REM SLEEP; SLEEP DEPRIVATION; SLEEP PATTERN; SLEEP WAKING CYCLE;

ANIMALS; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENZYME ACTIVATION; HYPOTHALAMUS, ANTERIOR; ISOENZYMES; MICROINJECTIONS; PEDUNCULOPONTINE TEGMENTAL NUCLEUS; PONS; PREFRONTAL CORTEX; PROTEIN KINASE INHIBITORS; RATS; RETICULAR FORMATION; SLEEP DEPRIVATION; SLEEP STAGES; SLEEP, REM; THIONUCLEOTIDES; TISSUE DISTRIBUTION; WAKEFULNESS;

EID: 33748269472     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2173-06.2006     Document Type: Article

References (63)

1. Ahnaou A, Basille M, Gonzalez B, Vaudry H, Hamon M, Adrien J, Bourgin P (1999) Long-term enhancement of REM sleep by the pituitary adenylyl cyclase-activating polypeptide (PACAP) in the pontine reticular formation of rat. Eur J Neurosci 11:4051-4058.
2. Borrelli E, Montmayeur JP, Foulkes NS, Sassone-Corsi P (1992) Signal transduction and gene control: the cAMP pathway. Crit Rev Oncog 3:321-338.
3. Bradford M (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 72:248-254.
4. Capece ML, Lydic R (1997) cAMP and protein kinase A modulate cholinergic rapid eye movement sleep generation. Am J Physiol 273:R1430-R1440.
5. Cook SA, Welch SP, Lichtman AH, Martin BR (1995) Evaluation of cAMP involvement in cannabinoid-induced antinociception. Life Sci 56:2049-2056.
6. Couve A, Moss SJ, Pangalos MN (2000) GABA-B receptors: a new paradigm in G protein signaling. Mol Cell Neurosci 16:296-312.
7. Dalley JW, Cardinal RN, Robbins TW (2004) Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates. Neurosci Biobehav Rev 28:771-784.
8. Datta S (1995) Neuronal activity in the peribrachial area: relationship to behavioral state control. Neurosci Biobehav Rev 19:67-84.
9. Datta S (2000) Avoidance task training potentiates phasic pontine-wave density in the rat: a mechanism for sleep-dependent plasticity. J Neurosci 20:8607-8613.
10. Datta S (2002) Evidence that REM sleep is controlled by the activation of brainstem pedunculopontine tegmental kainate receptor. J Neurophysiol 87:1790-1798.
11. Datta S, Patterson EH (2003) Activation of phasic pontine-wave (P-wave): a mechanism of learning and memory processing. In: Sleep and brain plasticity (Maquet P, Smith C, Stickgold R, eds), pp 135-156. New York: Oxford UP.
12. Datta S, Prutzman SL (2005) Novel role of brain stem pedunculopontine tegmental adenylyl cyclase in the regulation of spontaneous REM sleep in the freely moving rat. J Neurophysiol 94:1928-1937.
13. Datta S, Siwek DF (2002) Single cell activity patterns of pedunculopontine tegmentum neurons across the sleep-wake cycle in the freely moving rats. J Neurosci Res 70:611-621.
14. Datta S, Kumar VM, Chhina GS, Singh B (1988) Interrelationship of thermal and sleep-wakefulness changes elicited from the medial preoptic area in rats. Exp Neurol 100:40-50.
15. Datta S, Spoley EE, Patterson EH (2001) Microinjection of glutamate into the pedunculopontine tegmentum induces REM sleep and wakefulness in the rat. Am J Physiol 280:R752-R759.
16. Datta S, Spoley EE, Mavanji VK, Patterson EH (2002) A novel action of pedunculopontine tegmental kainate receptors: a mechanism of REM sleep generation in the rat. Neuroscience 114:157-164.
17. Datta S, Mavanji V, Ulloor J, Patterson EH (2004) Activation of phasic pontine-wave generator prevents rapid eye movement sleep deprivation-induced learning impairment in the rat: a mechanism for sleep-dependent plasticity. J Neurosci 24:1416-1427.
18. El-Mansari M, Sakai K, Jouvet M (1989) Unitary characteristics of presumptive cholinergic tegmental neurons during the sleep-waking cycle in freely moving cats. Exp Brain Res 76:519-529.
19. Ford B, Holmes CJ, Mainville L, Jones BE (1995) GABAergic neurons in the rat pontomesencephalic tegmentum: codistribution with cholinergic and other tegmental neurons projecting to the posterior lateral hypothalamus. J Comp Neurol 363:177-196.
20. Garcia-Rill E, Skinner RD, Miyazato H, Homma Y (2001) Pedunculopontine stimulation induces prolonged activation of pontine reticular neurons. Neuroscience 104:455-465.
21. Gilman AG (1987) G proteins: transducers of receptor-generated signals. Annu Rev Biochem 56:615-649.
22. Goldman-Rakic PS (1987) Circuitry of the primate prefrontal cortex and the regulation of behavior by representational memory. In: Handbook of physiology, the nervous system, higher functions of the brain (Plum F, ed), pp 373-417. Bethesda, MD: American Physiological Society.
23. Goueli S, Larson B, Hsiao K, Worzella T, Gallagher A, Mathews E (2004) High-throughput kinase screening using a universal luminescent kinase assay. Cell Notes 10:20-23.
24. Hobson JA, Pace-Schott EF (2002) The cognitive neuroscience of sleep: neuronal systems, consciousness and learning. Nat Rev Neurosci 3:679-693.
25. Jones BE (2004) Paradoxical REM sleep promoting and permitting neuronal networks. Arch Ital Biol 142:379-396.
26. Kaitin KI (1984) Preoptic area unit activity during sleep and wakefulness in the cat. Exp Neurol 83:347-357.
27. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
28. Lohmann SM, Walter U (1984) Regulation of the cellular and subcellular concentrations and distribution of nucleotide-dependent protein kinases. Adv Cyclic Nucleotide Protein Phosphorylation Res 18:63-102.
29. Maquet P, Dive D, Salmon E, Sadzot B, Franco G, Poirrier R, von Frenckell R, Franck G (1990) Cerebral glucose utilization during sleep-wake cycle in man determined by positron emission tomography and [18F]2-fluoro-2-deoxy-D-glucose method. Brain Res 513:136-143.
30. Maquet P, Peters JM, Aerts J, Delfiore G, Degueldre C, Luxen A, Franck G (1996) Functional neuroanatomy of human rapid eye movement sleep and dreaming. Nature 383:163-166.
31. Marinissen MJ, Gutkind JS (2001) G-protein coupled receptors and signaling networks: emerging paradigms. Trends Pharmacol Sci 22:368-376.
32. Marks GA, Birabil CG (2000) Infusion of adenylyl cyclase inhibitor SQ22,536 into the medial pontine reticular formation of rats enhances rapid eye movement sleep. Neuroscience 98:311-315.
33. McCarley RW (2004) Mechanisms and models of REM sleep control. Arch Ital Biol 142:429-467.
34. Meinkoth JL, Ji Y, Taylor SS, Feramisco JR (1990) Dynamics of the distribution of cyclic AMP-dependent protein kinase in living cells. Proc Natl Acad Sci USA 87:9595-9599.
35. Mesulam MM, Mufson EJ, Wainer BH, Levey AI (1983) Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience 10:1185-1201.
36. Montplaisir J, Petit D, Gauthier S, Gaudreau H, Decary A (1998) Sleep disturbances and EEG slowing in Alzheimer's disease. Sleep Res Online 1:147-151.
37. Nauta WJH (1946) Hypothalamic regulation of sleep in rats: an experimental study. J Neurophysiol 1:455-473.
38. Nestler EJ, Greengard P (1994) Protein phosphorylation and the regulation of neuronal function. In: Basic neurochemistry: molecular, cellular, and medical aspects (Siegel GS, Agranoff BW, Albers RW, Molinoff PB, eds), pp 449-474. Boston: Little Brown.
39. Pace-Schott EF, Hobson JA (2002) The neurobiology of sleep: genetics, cellular physiology and subcortical networks. Nat Rev Neurosci 3:591-605.
40. Paxinos G, Watson C (1997) The rat brain in stereotaxic coordinates. San Diego: Academic.
41. Prinz PN, Peskind ER, Vitaliano PP, Raskind MA, Eisdorfer C, Zemcuznikov N, Gerber CJ (1982) Sleep, EEG, and mental function changes in senile dementia of the Alzheimer's type. Neurobiol Aging 3:361-370.
42. Punch LJ, Self DW, Nestler EJ, Taylor JR (1997) Opposite modulation of opiate withdrawal behaviors on microinjection of a protein kinase A inhibitor versus activator into the locus coeruleus or periaqueductal gray. J Neurosci 17:8520-8527.
43. Ramos BP, Birnbaum SG, Lindenmayer I, Newton SS, Dumon RS, Arnsten AFT (2003) Dysregulation of protein kinase A signaling in the aged prefrontal cortex: new strategy for treating age-related cognitive decline. Neuron 40:835-845.
44. Rye DB, Saper CB, Lee HJ, Wainer BH (1987) Pedunculopontine tegmental nucleus of the rat: cytoarchitecture, cytochemistry, and some extrapyramidal connections of the mesopontine tegmentum. J Comp Neurol 259:483-528.
45. Sahir N, Mas C, Bourgeois F, Simonneau M, Evrard P, Gressens P (2001) Caffeine-induced telencephalic vesicle evagination in early post-implantation mouse embryos involves cAMP-dependent protein kinase (PKA) inhibition. Cereb Cortex 11:343-349.
46. Schafe GE, LeDoux JE (2000) Memory consolidation of auditory pavlovian fear conditioning requires protein synthesis and protein kinase A in the amygdala. J Neurosci 20:RC96(1-5).
47. Self DW, Nestler EJ (1995) Molecular mechanisms of drug reinforcement and addiction. Annu Rev Neurosci 18:463-495.
48. Self DW, Genova LM, Hope BT, Barnhart WJ, Spencer JJ, Nestler EJ (1998) Involvement of cAMP-dependent protein kinase in the nucleus accumbens in cocaine self-administration and relapse of cocaine-seeking behavior. J Neurosci 18:1848-1859.
49. Shi W-X, Bunney BS (1992) Roles of intracellular cAMP and protein kinase A in the actions of dopamine and neurotensin on midbrain dopamine neurons. J Neurosci 12:2433-2438.
50. Sivilotti L, Nistri A (1991) GABA receptor mechanisms in the central nervous system. Prog Neurobiol 36:35-92.
51. Smith C (1995) Sleep states and memory processes. Behav Brain Res 69:137-145.
52. Spaulding SW (1993) The ways in which hormones change cAMP-dependent protein kinase subunits, and how such changes affect cell behavior. Endocr Rev 14:632-650.
53. Steriade M, McCarley RW (1990) Brainstem control of wakefulness and sleep. New York: Plenum.
54. Steriade M, Datta S, Pare D, Oakson G, CurroDossi R (1990) Neuronal activities in brain-stem cholinergic nuclei related to tonic activation processes in thalamocortical systems. J Neurosci 10:2541-2559.
55. Taylor SS, Buechler JA, Yonemoto W (1990) cAMP-dependent protein kinase: framework for a diverse family of regulatory enzymes. Annu Rev Biochem 59:971-1005.
56. Thomas M, Sing H, Belenky G, Holcomb H, Mayberg H, Dannals R, Wagner Jr H, Thorne D, Popp K, Rowland L, Welsh A, Balwinski S, Redmond D (2000) Neural basis of alertness and cognitive performance impairments during sleepiness. I. Effects of 24 h of sleep deprivation on waking human regional brain activity. J Sleep Res 9:335-352.
57. Ulloor J, Mavanji V, Saha S, Siwek DF, Datta S (2004) Spontaneous REM sleep is modulated by the activation of the pedunculopontine tegmental GABA-B receptors in the freely moving rat. J Neurophysiol 91:1822-1831.
58. Van Haastert PJ, Van Driel R, Jastorff B, Baraniak J, Stec WJ, De Wit RJ (1984) Competitive cAMP antagonists for cAMP-receptor proteins. J Biol Chem 259:10020-10024.
59. Wang L-Y, Salter MW, MacDonald JF (1991) Regulation of kainate receptors by cAMP-dependent protein kinase and phosphatases. Science 253:1132-1135.
60. Wang L-Y, Taverna FA, Huang X-P, MacDonald JF, Hampson DR (1993) Phosphorylation and modulation of a kainate receptor (GluR6) by cAMP-dependent protein kainase. Science 259:1173-1175.
61. Weber W, Hilz H (1986) cAMP-dependent protein kinase I and II: divergent turnover of subunits. Biochemistry 25:5661-5667.
62. White D, Shultz J (1992) A novel method for non-radioactive assays of specific protein kinases. Promega Notes 35:11-17.
63. Zhang B, Veasey SC, Wood MA, Leng LZ, Kaminski C, Leight S, Abel T, Lee VM, Trojanowski JQ (2005) Impaired rapid eye movement sleep in the Tg2576 APP murine model of Alzheimer's disease with injury to pedunculopontine cholinergic neurons. Am J Pathol 167:1361-1369.