Advertisement

Narcolepsy pp 93-104 | Cite as

Prostaglandin D2: An Endogenous Somnogen

Chapter

Abstract

The humoral theory of sleep regulation, the concept that sleep and wakefulness are induced and regulated by a hormone-like chemical substance rather than by a neural network, was initially proposed by Kuniomi Ishimori of Nagoya, Japan, in 1909 and independently and concurrently, by a French neuroscientist, Henri Piéron of Paris, in 1913. They took samples of the brain and cerebrospinal fluid (CSF) from sleep-deprived dogs and infused them into the brains of normal dogs.

Keywords

Prostaglandines Prostaglandine D synthase Adenosine Narcolepsy Ventrolateral preoptic area 

Notes

Acknowledgments

Studies conducted in our laboratory were supported in part by the Program for Promotion of Basic Research Activities for Innovative Biosciences (PROBRAIN); the Program for Promotion of Fundamental Studies in Health Sciences of the National Institute of Biomedical Innovation (NIBIO); a Health and Labor Science Research Grant from the Ministry of Health, Labor, and Welfare, Japan; and by research grants from Takeda Science Foundation, Takeda Pharmaceutical Co. Ltd., Ono Pharmaceutical Co. Ltd., and Osaka city.

References

  1. 1.
    Narumiya S, Ogorochi T, Nakao K, et al. Prostaglandin D2 in rat brain, spinal cord and pituitary: basal level and regional distribution. Life Sci. 1982;31:2093–103.PubMedCrossRefGoogle Scholar
  2. 2.
    Ogorochi T, Narumiya S, Mizuno N, et al. Regional distribution of prostaglandins D2, E2, and F2 alpha and related enzymes in postmortem human brain. J Neurochem. 1984;43:71–82.PubMedCrossRefGoogle Scholar
  3. 3.
    Ueno R, Ishikawa Y, Nakayama T, et al. Prostaglandin D2 induces sleep when microinjected into the preoptic area of conscious rats. Biochem Biophys Res Commun. 1982;109:576–82.PubMedCrossRefGoogle Scholar
  4. 4.
    Ueno R, Honda K, Inoue S, et al. Prostaglandin D2, a cerebral sleep-inducing substance in rats. Proc Natl Acad Sci U S A. 1983;80:1735–7.PubMedCrossRefGoogle Scholar
  5. 5.
    Onoe H, Ueno R, Fujita I, et al. Prostaglandin D2, a cerebral sleep-inducing substance in monkeys. Proc Natl Acad Sci U S A. 1988;85:4082–6.PubMedCrossRefGoogle Scholar
  6. 6.
    Pandey HP, Ram A, Matsumura H, et al. Concentration of prostaglandin D2 in cerebrospinal fluid exhibits a circadian alteration in conscious rats. Biochem Mol Biol Int. 1995;37:431–7.PubMedGoogle Scholar
  7. 7.
    Ram A, Pandey HP, Matsumura H, et al. CSF levels of prostaglandins, especially the level of prostaglandin D2, are correlated with increasing propensity towards sleep in rats. Brain Res. 1997;751:81–9.PubMedCrossRefGoogle Scholar
  8. 8.
    Roberts 2nd LJ, Sweetman BJ, Lewis RA, et al. Increased production of prostaglandin D2 in patients with systemic mastocytosis. N Engl J Med. 1980;303:1400–4.PubMedCrossRefGoogle Scholar
  9. 9.
    Pentreath VW, Rees K, Owolabi OA, et al. The somnogenic T lymphocyte suppressor prostaglandin D2 is selectively elevated in cerebrospinal fluid of advanced sleeping sickness patients. Trans R Soc Trop Med Hyg. 1990;84:795–9.PubMedCrossRefGoogle Scholar
  10. 10.
    Urade Y, Fujimoto N, Hayaishi O. Purification and characterization of rat brain prostaglandin D synthetase. J Biol Chem. 1985;260:12410–5.PubMedGoogle Scholar
  11. 11.
    Christ-Hazelhof E, Nugteren DH. Purification and characterisation of prostaglandin endoperoxide D-isomerase, a cytoplasmic, glutathione-requiring enzyme. Biochim Biophys Acta. 1979;572:43–51.PubMedCrossRefGoogle Scholar
  12. 12.
    Urade Y, Fujimoto N, Ujihara M, et al. Biochemical and immunological characterization of rat spleen prostaglandin D synthetase. J Biol Chem. 1987;262:3820–5.PubMedGoogle Scholar
  13. 13.
    Urade Y, Eguchi N. Lipocalin-type and hematopoietic prostaglandin D synthases as a novel example of functional convergence. Prostaglandins Other Lipid Mediat. 2002;68–69:375–82.PubMedCrossRefGoogle Scholar
  14. 14.
    Urade Y, Hayaishi O. Biochemical, structural, genetic, physiological, and pathophysiological features of lipocalin-type prostaglandin D synthase. Biochim Biophys Acta. 2000;1482:259–71.PubMedCrossRefGoogle Scholar
  15. 15.
    Hirata M, Kakizuka A, Aizawa M, et al. Molecular characterization of a mouse prostaglandin D receptor and functional expression of the cloned gene. Proc Natl Acad Sci U S A. 1994;91:11192–6.PubMedCrossRefGoogle Scholar
  16. 16.
    Hirai H, Tanaka K, Yoshie O, et al. Prostaglandin D2 selectively induces chemotaxis in T helper type 2 cells, eosinophils, and basophils via seven-transmembrane receptor CRTH2. J Exp Med. 2001;193:255–61.PubMedCrossRefGoogle Scholar
  17. 17.
    Irikura D, Aritake K, Nagata N, et al. Biochemical, functional, and pharmacological characterization of AT-56, an orally active and selective inhibitor of lipocalin-type prostaglandin D synthase. J Biol Chem. 2009;284:7623–30.PubMedCrossRefGoogle Scholar
  18. 18.
    Aritake K, Kado Y, Inoue T, et al. Structural and functional characterization of HQL-79, an orally selective inhibitor of human hematopoietic prostaglandin D synthase. J Biol Chem. 2006;281:15277–86.PubMedCrossRefGoogle Scholar
  19. 19.
    Mohri I, Eguchi N, Suzuki K, et al. Hematopoietic prostaglandin D synthase is expressed in microglia in the developing postnatal mouse brain. Glia. 2003;42:263–74.PubMedCrossRefGoogle Scholar
  20. 20.
    Beuckmann CT, Lazarus M, Gerashchenko D, et al. Cellular localization of lipocalin-type prostaglandin D synthase (beta-trace) in the central nervous system of the adult rat. J Comp Neurol. 2000;428:62–78.PubMedCrossRefGoogle Scholar
  21. 21.
    Urade Y, Kitahama K, Ohishi H, et al. Dominant expression of mRNA for prostaglandin D synthase in leptomeninges, choroid plexus, and oligodendrocytes of the adult rat brain. Proc Natl Acad Sci U S A. 1993;90:9070–4.PubMedCrossRefGoogle Scholar
  22. 22.
    Mizoguchi A, Eguchi N, Kimura K, et al. Dominant localization of prostaglandin D receptors on arachnoid trabecular cells in mouse basal forebrain and their involvement in the regulation of non-rapid eye movement sleep. Proc Natl Acad Sci U S A. 2001;98:11674–9.PubMedCrossRefGoogle Scholar
  23. 23.
    Urade Y, Eguchi N, Hayaishi O. Lipocalin-type prostaglandin D synthase as an enzymic lipocalin. Georgetown, TX: Landes Bioscience/Eurekah.com; 2006.Google Scholar
  24. 24.
    Urade Y, Hayaishi O. Prostaglandin D synthase: structure and function. Vitam Horm. 2000;58:89–120.PubMedCrossRefGoogle Scholar
  25. 25.
    Shimamoto S, Yoshida T, Inui T, et al. NMR solution structure of lipocalin-type prostaglandin D synthase: evidence for partial overlapping of catalytic pocket and retinoic acid-binding pocket within the central cavity. J Biol Chem. 2007;282:31373–9.PubMedCrossRefGoogle Scholar
  26. 26.
    Kumasaka T, Aritake K, Ago H, et al. Structural basis of the catalytic mechanism operating in open-closed conformers of lipocalin type prostaglandin D synthase. J Biol Chem. 2009;284:22344–52.PubMedCrossRefGoogle Scholar
  27. 27.
    Hoffmann A, Conradt HS, Gross G. Purification and chemical characterization of beta-trace protein from human cerebrospinal fluid: its identification as prostaglandin D synthase. J Neurochem. 1993;61:451–6.PubMedCrossRefGoogle Scholar
  28. 28.
    Watanabe K, Urade Y, Mader M, et al. Identification of beta-trace as prostaglandin D synthase. Biochem Biophys Res Commun. 1994;203:1110–6.PubMedCrossRefGoogle Scholar
  29. 29.
    Clausen J. Proteins in normal cerebrospinal fluid not found in serum. Proc Soc Exp Biol Med. 1961;107:170–2.PubMedGoogle Scholar
  30. 30.
    Jordan W, Tumani H, Cohrs S, et al. Prostaglandin D synthase (beta-trace) in healthy human sleep. Sleep. 2004;27:867–74.PubMedGoogle Scholar
  31. 31.
    Kohtoh S, Taguchi Y, Matsumoto N, et al. Algorithm for sleep scoring in experimental animals based on fast Fourier transform power spectrum analysis of the electroencephalogram. Sleep Biol Rhythm. 2008;6:163–71.CrossRefGoogle Scholar
  32. 32.
    Urade Y, Eguchi N, Qu WM, et al. Sleep regulation in adenosine A2A receptor-deficient mice. Neurology. 2003;61:S94–6.PubMedCrossRefGoogle Scholar
  33. 33.
    Satoh S, Matsumura H, Koike N, et al. Region-dependent difference in the sleep-promoting potency of an adenosine A2A receptor agonist. Eur J Neurosci. 1999;11:1587–97.PubMedCrossRefGoogle Scholar
  34. 34.
    Scammell T, Gerashchenko D, Urade Y, et al. Activation of ventrolateral preoptic neurons by the somnogen prostaglandin D2. Proc Natl Acad Sci U S A. 1998;95:7754–9.PubMedCrossRefGoogle Scholar
  35. 35.
    Sherin JE, Elmquist JK, Torrealba F, et al. Innervation of histaminergic tuberomammillary neurons by GABAergic and galaninergic neurons in the ventrolateral preoptic nucleus of the rat. J Neurosci. 1998;18:4705–21.PubMedGoogle Scholar
  36. 36.
    Gallopin T, Luppi PH, Cauli B, et al. The endogenous somnogen adenosine excites a subset of sleep-­promoting neurons via A2A receptors in the ventrolateral preoptic nucleus. Neuroscience. 2005;134:1377–90.PubMedCrossRefGoogle Scholar
  37. 37.
    Hong ZY, Huang ZL, Qu WM, et al. An adenosine A2A receptor agonist induces sleep by increasing GABA release in the tuberomammillary nucleus to inhibit histaminergic systems in rats. J Neurochem. 2005;92:1542–9.PubMedCrossRefGoogle Scholar
  38. 38.
    Saper CB, Chou TC, Scammell TE. The sleep switch: hypothalamic control of sleep and wakefulness. Trends Neurosci. 2001;24:726–31.PubMedCrossRefGoogle Scholar
  39. 39.
    Saper CB, Scammell TE, Lu J. Hypothalamic regulation of sleep and circadian rhythms. Nature. 2005;437:1257–63.PubMedCrossRefGoogle Scholar
  40. 40.
    Chu M, Huang ZL, Qu WM, et al. Extracellular histamine level in the frontal cortex is positively correlated with the amount of wakefulness in rats. Neurosci Res. 2004;49:417–20.PubMedCrossRefGoogle Scholar
  41. 41.
    Huang ZL, Sato Y, Mochizuki T, et al. Prostaglandin E2 activates the histaminergic system via the EP4 receptor to induce wakefulness in rats. J Neurosci. 2003;23:5975–83.PubMedGoogle Scholar
  42. 42.
    Huang ZL, Qu WM, Li WD, et al. Arousal effect of orexin A depends on activation of the histaminergic system. Proc Natl Acad Sci U S A. 2001;98:9965–70.PubMedCrossRefGoogle Scholar
  43. 43.
    Oishi Y, Huang ZL, Fredholm BB, et al. Adenosine in the tuberomammillary nucleus inhibits the histaminergic system via A1 receptors and promotes non-rapid eye movement sleep. Proc Natl Acad Sci U S A. 2008;105:19992–7.PubMedCrossRefGoogle Scholar
  44. 44.
    Eguchi N, Minami T, Shirafuji N, et al. Lack of tactile pain (allodynia) in lipocalin-type prostaglandin D synthase-deficient mice. Proc Natl Acad Sci U S A. 1999;96:726–30.PubMedCrossRefGoogle Scholar
  45. 45.
    Hayaishi O, Urade Y, Eguchi N, et al. Genes for prostaglandin D synthase and receptor as well as adenosine A2A receptor are involved in the homeostatic regulation of NREM sleep. Arch Ital Biol. 2004;142:533–9.PubMedGoogle Scholar
  46. 46.
    Pinzar E, Kanaoka Y, Inui T, et al. Prostaglandin D synthase gene is involved in the regulation of non-rapid eye movement sleep. Proc Natl Acad Sci U S A. 2000;97:4903–7.PubMedCrossRefGoogle Scholar
  47. 47.
    Huang ZL, Mochizuki T, Qu WM, et al. Altered sleep-wake characteristics and lack of arousal response to H3 receptor antagonist in histamine H1 receptor knockout mice. Proc Natl Acad Sci U S A. 2006;103:4687–92.PubMedCrossRefGoogle Scholar
  48. 48.
    Qu WM, Huang ZL, Xu XH, et al. Lipocalin-type prostaglandin D synthase produces prostaglandin D2 involved in regulation of physiological sleep. Proc Natl Acad Sci U S A. 2006;103:17949–54.PubMedCrossRefGoogle Scholar
  49. 49.
    Islam F, Watanabe Y, Morii H, et al. Inhibition of rat brain prostaglandin D synthase by inorganic selenocompounds. Arch Biochem Biophys. 1991;289:161–6.PubMedCrossRefGoogle Scholar
  50. 50.
    Huang ZL, Qu WM, Eguchi N, et al. Adenosine A2A, but not A1, receptors mediate the arousal effect of caffeine. Nat Neurosci. 2005;8:858–9.PubMedCrossRefGoogle Scholar
  51. 51.
    Jordan W, Tumani H, Cohrs S, et al. Narcolepsy increased L-PGDS (β-trace) levels correlate with excessive daytime s;leepiness but not with cataplexy. J Neurol. 2005;252:1372–8.PubMedCrossRefGoogle Scholar
  52. 52.
    Bassetti CL, Hersberger M, Baumann CR. CSF prostaglandin D synthase is reduced in excessive daytime sleepiness. J Neurol. 2006;253:1030–3.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  1. 1.Department of Molecular Behavioral BiologyOsaka Bioscience InstituteSuita-shiJapan

Personalised recommendations