Functional morphology of the suprachiasmatic nucleus

Frontiers in Neuroendocrinology

Volumn 20, Issue 3, 1999, Pages 241-268

  Ibata, Yasuhiko ^a   Okamura, Hitoshi ^b   Tanaka, Masaki ^a   Tamada, Yoshitaka ^a   Hayashi, Seiji ^a   Iijima, Norio ^a   Matsuda, Tomoyuki ^a   Munekawa, Katsuhiko ^a   Takamatsu, Tetsuro ^a   Hisa, Yasuo ^a   Shigeyoshi, Yasufumi ^b   Amaya, Fumimasa ^a  

^a KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

^b KOBE UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Biological clock; Clock genes; Melatonin; mRNA; Peptides; Suprachiasmatic nucleus

Indexed keywords

BIOLOGICAL RHYTHM; CIRCADIAN RHYTHM; GLIA CELL; HORMONE RELEASE; IMMEDIATE EARLY GENE; MOLECULAR INTERACTION; MORPHOLOGY; POLYSYNAPTIC REFLEX; PRIORITY JOURNAL; REVIEW; SLEEP WAKING CYCLE; SUPRACHIASMATIC NUCLEUS; SYNAPTIC TRANSMISSION;

EID: 0032801508     PISSN: 00913022     EISSN: None     Source Type: Journal    
DOI: 10.1006/frne.1999.0180     Document Type: Article

References (102)

1. Albers H E, Stopa E G, Zoeller R T, Kauer J S, King J C, Fink J S, Mobfaker H, Wolfe H. Day-night variation in prepro vasoactive intestinal peptide/peptide histidine isoleucine mRNA within the rat suprachiasmatic nucleus. Mol Brain Res. 7:1990;85-89.
2. Albrecht U, Sun Z S, Eichele G, Lee C C. A differential response of two putative mammalian circadian regulators, mper1 and mper2, to light. Cell. 91:1997;1055-1064.
3. Aronson B, Johnson K, Loros J J, Dunlap J C. Negative feedback defining a circadian clock: Autoregulation in the clock gene frequency. Science. 263:1994;1578-1584.
4. Ban Y, Shigeyoshi Y, Okamura H. Development of vasoactive intestinal peptide mRNA rhythm in the rat suprachiasmatic nucleus. J Neurosci. 17:1997;3920-3931.
5. Barbour B, Sqarkowski M, Ingledew N, Atturell D. Arachidonic acid induces a prolonged inhibition of glutamate uptake into glia cells. Nature. 342:1989;918-920.
6. Bennett M R, Aronin N, Schwartz W J. In vitro stimulation of c-fos protein expression in the suprachiasmatic nucleus of hypothalamus slices. Mol Brain Res. 42:1996;140-144.
7. Bennett M R, Schwartz W J. Are glia among the cells that express immunoreactive c-Fos in the suprachiasmatic nucleus. NeuroReport. 5:1994;1737-1740.
8. Castel M, Belenky M, Cohen S, Wagner S, Schwartz W J. Light-induced c-Fos expression in the mouse suprachiasmatic nucleus: Immunoelectron microscopy reveals co-localization in maltiple cell types. Eur J Neurosci. 9:1997;1950-1960.
9. Castel M, Morris J, Belenky M. Non-synaptic and dendritic exocytosis from dense-cored vescles in the suprachiasmatic nucleus. NeuroReport. 7:1996;543-547.
10. Darlington T K, Wager-Smith K, Ceriani M F, Staknis D, Gekakis N, Steeves T DL, Weitz C J, Takahashi J S, Kay S A. Closing the circadian loop: CLOCK-induced transcription of its own inhibitors per and tim. Science. 280:1998;1599-1603.
11. Ding J M, Buchanan G F, Tischkau S A, Chen D, Kuriashkina L, Falman L E, Alster J M, Mcpherson P S, Campbell K P, Gillelte M U. A neuronal ryanodine receptor mediates light-induced phase delay of the circadian clock. Nature. 394:1998;381-384.
12. Ding J M, Chen D, Weber E T, Faiman L E, Rea M A, Gillett M U. Resetting the biological clock: Mediation of nocturnal circadian shifts by glutamate and NO. Science. 266:1994;1713-1717.
13. Dunlap J C. Common threads in eukaryotic circadian systems. Curr Opin Genet Dev. 8:1998;400-406.
14. Foulkes N S, Borjigen J, Snyder S H, Sasson-Corsi P. Rhythmic transcription: The molecular basic of circadian melatonin synthesis. Trends Neurosci. 20:1997;487-493.
15. Fukuhara C, Shinohara K, Tominaga K, Otori Y, Inoue S T. Endogenous circadian rhythmicity of somatostatin like-immunoreactivity in the rat suprachiasmatic nucleus. Brain Res. 606:1993;28-35.
16. Gekakis N, Staknis D, Nguyen H B, Davis F C, Wilsbacher L D, King D P, Tahahashi J S, Weitz C J. Role of the CLOCK protein in the mammalian circadian mechanism. Science. 280:1998;1564-1569.
17. Glüdner F H, Bahr E, Young C A, Ingham C A. Structural plasticity of optic synapses in the rat suprachiasmatic nucleus: Adaptation to long-term influence of light and darkness. Cell Tissue Res. 287:1997;43-60.
18. 2 receptor. NeuroReport. 7:1996;1315-1319.
19. Hannibal J, Ding J M, Chen D, Fahrenkrug J, Larsen J, Larsen P J, Gillette M U, Mikkelsen J D. Pituitary adenylate cyclase-activating peptide (PACAP) in the retinohypothalamic tract: A potential daytime regulator of the biological clock. J Neurosci. 17:1997;2637-2644.
20. Hardin P E, Hall J C, Rosbash M. Feedback of the Drosophila period gene product on circadian cycling of its messenger RNA levels. Nature. 343:1990;536-540.
21. Herzog H D, Takahashi J S, Block G D. Clock controls circadian period in isolated suprachiasmatic nucleus neurons. Nature Neurosci. 1:1998;708-713.
22. Hisano S, Chikamori-Aoyama M, Katoh S, Kagotani Y, Daikoku S, Chihara K. Suprachiasmatic nucleus neurons immunoreactive for vasoactive intestinal polypeptide have synaptic contacts with axons immunoreactive for neuropeptide Y: An immunoelectron microscopic study in the rat. Neurosci Lett. 1988;145-150.
23. Honma K, Honma S. Non-SCN rhythm in the circadian domain. Touitou Y. Biological Clocks: Mechanisms and Applications. 1998;33-40 Elsevier, Amsterdam.
24. 2 receptor. NeuroReport. 7:1996;1249-1252.
25. Hunt S P, Pini A, Evans G. Induction of c-fos like protein in spinal cord neurons following sensory stimulation. Nature. 328:1987;632-634.
26. Ibata Y, Takahashi Y, Okamura H, Kawakami F, Terubayashi H, Kubo T, Yanaihara N. Vasoactive intestinal peptide (VIP)-like immunoreactive neurons located in the rat suprachiasmatic nucleus receive a direct retinal projection. Neurosci Lett. 97:1989;1-5.
27. Ibata Y, Tanaka M, Ichitani Y, Takahashi Y, Okamura H. Neuronal interaction between VIP and vasopressin neurons in the rat suprachiasmatic nucleus. NeuroReport. 4:1993;128-130.
28. Ibata Y, Tanaka M, Tamada Y, Hayashi S, Kawakami F, Takamatsu T, Hisa Y, Okamura H. The suprachiasmatic nucleus: A circadian oscillator. The Neuroscientist. 3:1997;215-225.
29. Ibuka N, Kawamura H. Loss of circadian sleep-wakefulness cycle in the rat by suprachiasmatic nucleus lesion. Brain Res. 96:1975;76-81.
30. Jacomy H J, Burlet A, Bosler O. Vasoactive intestinal peptide neurons as synaptic targets for vasopressin neurons in the suprachiasmatic nucleus. Double-label immunocytochemical demonstration in the rat. Neuroscience. 88:1999;859-870.
31. Jiang Z G, Yang Y Q, Allen C N. Tracer and electrical coupling of rat suprachiasmatic nucleus neurons. Neuroscience. 77:1997;1059-1066.
32. Kawakami F, Okamura H, Tamada Y, Nakajima T, Ibata Y. Changes in vasoactive intestinal peptide mRNA levels in the rat suprachiasmatic nucleus following p-chlorophenylalanine (PCPA) treatment under light/dark conditions. Neurosci Lett. 200:1995;171-174.
33. King D P, Zhao Y, Sangoram A M, Wilsbacher L D, Tanaka M, Antoch P, Steeves D LT, Vitaterna M H, Kohnhauser J M, Lowrey P L, Turek F M, Takahashi J S. Positional cloning of the mouse circadian clock gene. Cell. 89:1997;641-653.
34. Kiss J, Leranth C S, Halasq B. Serotonergic endings on VIP-neurons in the suprachiasmatic nucleus and on ACTH-neurons in the arcuate nucleus of the rat hypothalamus. A combination of high resolution autoradiography and electron microscopic immunocytochemistry. Neurosci Lett. 44:1984;119-124.
35. Klein D C, Weller J L. Indole metabolism in the pineal gland: A circadian rhythm in N-acetyl-transferase. Science. 169:1970;1093-1095.
36. Lehman M N, Silver R, Gladstone W R, Kahn R M, Gibson M, Bittman E L. Circadian rhythmicity restored by neuronal transplant. Immunocytochemical characterization of the graft and its integration with the host brain. J Neurosci. 7:1987;1626-1638.
37. McArthur A J, Hunt A E, Gillette M U. Melatonin action and signal transduction in the rat suprachiasmatic circadian clock: Activation of protein keinase C at dusk and dawn. Endocrinology. 138:1997;627-634.
38. Moore R Y, Bernstein M E. Synaptogenesis in the rat suprachiasmatic nucleus demonstrated by electron microscopy and synapsin I immunoreactivity. J Neurosci. 9:1989;2151-2162.
39. Moore R Y, Eichler V B. Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesion in the rat. Brain Res. 42:1972;201-206.
40. Moore R Y, Klein D C. Visual pathways and the central neuronal control of a circadian rhythm in pineal serotonin N-acetyl-transferase activity. Brain Res. 71:1974;17-33.
41. Moore R Y, Lenn N J. A retinohypothalamic projection in the rat. J Comp Neurol. 146:1972;1-14.
42. Morin L P, Johnson R F, Moore R Y. Two brain nuclei controlling circadian rhythm are identified by GFAP immunoreactivity in hamster and rat. Neurosci Lett. 99:1989;55-60.
43. Neumann-Haefelin T, Wiessner C, Vogel P, Back T, Hossmann K A. Differential expression of immediate early genes c-fos, c-jun, jun-B and NGFI-B in the rat brain following transient forebrain ischemia. J Cereb Blood Flow Metab. 14:1994;206-216.
44. Nishiwaki T, Okamura H, Kanemasa K, Inatomi T, Ibata Y, Fukuhara C, Inoue S T. Differences of somatostatin mRNA in the rat suprachiasmatic nucleus under light-dark and constant dark conditions: An analysis by in situ hybridization. Neurosci Lett. 197:1995;231-234.
45. Obrietan K, Impey S, Storm D R. Light and circadian rhythmicity regulate MAP kainase activation in the suprachiasmatic nuclei. Nature Neurosci. 1:1998;693-700.
46. Okamoto S, Okamura H, Miyake M, Takahashi Y, Takagi S, Akagi Y, Fukui K, Okamoto H, Ibata Y. A diurnal variation of vasoactive intestinal peptide (VIP) mRNA under a day light-dark cycle in the rat suprachiasmatic nucleus. Histochemistry. 95:1991;525-528.
47. Okamura H, Abitbol M, Julien J-F, Dumas S, Bérod A, Geffard M, Kitahama K, Bobillier P, Mallet J, Wiklund I. Neurons containing messenger RNA encording glutamic acid decarboxylase (GAD) in rat hypothalamus demonstrated by in situ hybridization, with special emphasis on cell groups in medial preoptic area and dorsomedial hypothalamus nucleus. Neuroscience. 39:1990;675-699.
48. Okamura H, Tominaga K, Ban Y, Fukuhara C, Yanaihara N, Ibata Y, Inoue S T. Morphological survey of the suprachiasmatic nucleus in slice culture using roller tube method. 2. Peptidergic neurons. Acta Histochem Cytochem. 27:1994;171-179.
49. Okamura H, Tominaga K, Ban Y, Tanaka M, Tamada Y, Inoue S T, Ibata Y. Morphological survey of the suprachiasmatic nucleus in slice culture using roller tube method. 1. Architecture of the suprachiasmatic nucleus in vitro. Acta Histochem Cytochem. 27:1994;159-169.
50. Palm L, Blennow G, Wetterberg L. Correction of non-24 hour sleep/wake cycle by melatonin in a blind retarded boy. Ann Neurol. 29:1991;336-339.
51. Pennartz C MA, Jeu M TG, Geurtsen A MS, Sluiter A A, Hermes M LHJ. Electrophysiological and morphological heterogeneity of neurons in slice of rat suprachiasmatic nucleus. J Physiol. 506:1998;775-793.
52. Peters R V, Aronin N, Schwartz W G. C-fos expression in the rat intergeniculate leaflet: Photic regulation, co-localization. Brain Res. 728:1996;231-241.
53. Petrie K, Conaglen J V, Thompson L, Chamberlain K. Effect of melatonin on jet lag after long haul flights. BMJ. 298:1989;705-707.
54. Ralph M R, Foster R G, Davis F C, Menaker M. Transplanted suprachiasmatic nucleus determines circadian period. Science. 247:1990;975-978.
55. Reppert S M, Weaver D R, Ebisawa T. Cloning and characterization of mammalian melatonin receptor that mediates reproductive and circadian response. Neuron. 13:1994;1177-1185.
56. Romijn H J, Sluiter A A, Pool C W, Wortel J, Buijs R M. Differences in colocalization between Fos and PHI, GRP, VIP and VP in neurons of the rat suprachiasmatic nucleus after a light stimulus during the phase delay versus the phase advance period of the night. J Comp Neurol. 372:1996;1-8.
57. Romijn H J, Sluiter A A, Pool C W, Wortel J, Buijs R M. Evidence from confocal fluorescence microscopy for a dense, reciprocal innervation between AVP-, somatostatin-, VIP/PHI-, GRP- and VIP/PHI/GRP-immunoreactive neurons in the rat suprachiasmatic nucleus. Eur J Neurosci. 9:1997;2613-2623.
58. Rosbash M, Allada R, Dembinska M, Guo W Q, Le M, Marrus S, Qian Z, Rutila J, Yaglom J, Zeng H. A Drosophila circadian clock. Cold Spring Harbor Symp Quant Biol. 61:1996;265-278.
59. Rusak B, Robertson H A, Wisden W, Hunt S P. Light pulses that shift rhythms induce gene expression in the suprachiasmatic nucleus. Science. 248:1990;1237-1240.
60. Sangoram A M, Saez L, Antoch M P, Nicholas Gekakis N, Staknis D, Whiteley A, Fruechte E M, Vitaterna M H, Shimomura K, King D P, Young M W, Weitz C J, Takahashi J S. Mammalian circadian autoregulatory loop: A Timeless ortholog and mPer1 interact and negatively regulate CLOCK-BMAL1-induced transcription. Neuron. 21:1998;1101-1103.
61. Sawaki Y, Nihonmatsu I, Kawamura H. Transplantation of the neonatal suprachiasmatic nucleus into rats with complate bilateral suprachiasmatic lesion. Neurosci Res. 1:1984;67-72.
62. Schmahl C, Bohmer G. Effects of exitatory amino acids and neuropeptide Y on the discharge activity of suprachiasmatic neurons in rat brain slices. Brain Res. 746:1997;151-163.
63. Schwartz W G, Aronin N, Takeuchi J, Bennett M R, Peter R V. Towards a molecular biology of the suprachiasmatic nucleus: Photic and temporal regulation of c-fos gene expression. Semin Neurosci. 7:1995;53-60.
64. Shearman L P, Zylka M J, Weaver D R, Kolakowski J LF, Reppert S M. Two period homologs: Circadian expression and photic regulation in the suprachiasmatic nuclei. Neuron. 19:1997;1261-1269.
65. Shen H, Watanabe M, Tomasiewicz H, Rutishauser U, Magnuson T, Glass J D. Role of cell adhesion molecule and polysialic acid in mouse circadian clock function. J Neurosci. 17:1997;5221-5229.
66. Shigeyoshi Y, Taguchi K, Yamamoto S, Takeda S, Yan L, Tei H, Moriya T, Shibata S, Loros J G, Dunlap J C, Okamura H. Light-induced resetting of a mammalian circadian clock is associated with rapid induction of the mPer1 transport. Cell. 91:1997;1043-1053.
67. Shinohara K, Honma S, Katsuno Y, Abe H, Honma K. Two distinct oscillators in the rat suprachiasmatic nucleus. Proc Natl Acad Sci USA. 92:1995;7396-7400.
68. Sontheirmer H, Waxman S G. Expression of voltage-activated ion channels by astrocytes and oligodendrocytes in the hippocampal slice. J Neurophysiol. 70:1993;1863-1873.
69. Sun Z S, Alsbrecht U, Zhuchenko O, Bailey J, Eichele G, Lee C C. RIGUI, a putative mammalian orthology of the Drosophila period gene. Cell. 90:1997;1003-1011.
70. Sutin E L, Kilduff T S. Circadian and light induced expression of immediate early gene mRNA in the rat suprachiasmatic nucleus. Mol Brain Res. 15:1992;281-290.
71. Takatsuji K, Miguel-Hidalgo J G, Tohyama M. Substance P-immunoreactive innervation from the retina to the suprachiasmatic nucleus in the rat. Brain Res. 568:1991;223-229.
72. Takeuchi Y, Takashima M, Katoh Y, Nishikawa T, Takahashi K. N-Methyl-d-asparate, quisqualate and kainate receptors are all involved in transmission of photic stimulation in the suprachiasmatic nucleus in rats. Brain Res. 563:1991;127-131.
73. Takumi T, Matsubara C, Shigeyoshi Y, Taguchi K, Yagita K, Maebayashi Y, Sakakida Y, Okumura K, Takashima N, Okamura H. A new mammalian period gene predominantly expressed in the suprachiasmatic nucleus. Genes Cells. 3:1998;167-176.
74. Takumi T, Nagamine Y, Miyake S, Matsubara C, Taguchi K, Takekida S, Sakakida Y, Nishikawa K, Kishimoto T, Niwa S, Okumura K, Okamura H. A mammalian ortholog of Drosophila timeless, highly expressed in SCN and retina, forms a complex with mPER1. Genes Cells. 4:1999;67-75.
75. Takumi T, Taguchi K, Miyake S, Sakakida Y, Takashima N, Matsubara C, Maebayashi Y, Okumura K, Takekida S, Yamamoto S, Yagita K, Yan L, Young M L, Okamura H. A light-independent oscillatory gene mPer3 in mouse SCN and OVLT. EMBO J. 17:1998;4753-4759.
76. Tamada Y, Tanaka M, Munekawa K, Hayashi S, Okamura H, Kubo T, Hisa Y, Ibata Y. Neuron-glia interaction in the suprachiasmatic nucleus: A double labeling light and electron microscopic immunocytochemical study in the rat. Brain Res Bull. 45:1998;281-287.
77. Tanaka M, Amaya F, Tamada Y, Okamura H, Hisa Y, Ibata Y. Induction of NGFI-A gene expression in the rat suprachiasmatic nucleus by photic stimulation. Brain Res. 756:1997;305-310.
78. Tanaka M, Matsuda T, Shigeyoshi Y, Ibata Y, Okamura H. Peptide expression in GABAergic neurons in the rat suprachiasmatic nucleus in comparison with other forebrain structure: A double labeling in situ hybridization study. J Histochem Cytochem. 45:1997;1231-1237.
79. Tanaka M, Ichitani Y, Okamura H, Tanaka Y, Ibata Y. The direct retinal projection to VIP neuronal elements in the rat SCN. Brain Res Bull. 31:1993;637-640.
80. Tanaka M, Okamura H, Matsuda T, Shigeyoshi Y, Hisa Y, Chihara K, Ibata Y. Somatostatin neurons from a distinct peptidergic neuronal group in the rat suprachiasmatic nucleus: A double labeling in situ hybridization study. Neurosci Lett. 215:1996;119-122.
81. Takahashi Y, Okamura H, Yanaihara N, Hamada S, Fujita S, Ibata Y. Vasoactive intestinal peptide immunoreactive neurons in the rat suprachiasmatic nucleus demonstrate diurnal variation. Brain Res. 497:1989;374-377.
82. Teclemarian-Mesbah R, Kalsbeek A, Pevet P, Buijs R M. Direct vasoactive intestinal polypeptide-containing projection from the suprachiasmatic nucleus to spinal projecting hypothalamic paraventricular neurons. Brain Res. 748:1997;71-76.
83. Tei H, Okamura H, Shigeyoshi Y, Fukuhara C, Ozawa R, Hirose M, Sakaki Y. Circadian oscillation of a mammalian homologue of the Drosophila period gene. Nature. 389:1997;512-516.
84. Tosini G, Menaker M. Circadian rhythms in cultured mammalian retina. Science. 272:1996;419-421.
85. Uhl G R, Reppert S M. Suprachiasmatic nucleus vasopressin messenger RNA: Circadian variation in normal and Brattleboro rats. Science. 232:1986;390-393.
86. van den Pol A N. The hypothalamic suprachiasmatic nucleus of rat: Intrinsic anatomy. J Comp Neurol. 191:1980;661-702.
87. van den Pol A N, Finkbeiner S T, Cornell-Bell A H. Calcium excitability and oscillation in suprachiasmatic nucleus neurons and glia in vitro. J Neurosci. 12:1992;2648-2664.
88. van den Pol A N, Tsujimoto K L. Neurotransmitters of the hypothalamic suprachiasmatic nucleus: Immunocytochemical analysis of 25 neuronal antigens. Neuroscience. 15:1985;1049-1086.
89. van der Beek E M, Horvath T L, Wiegant V M, van den Hurk R, Buijs R M. Evidence for a direct neuronal pathway from the suprachiasmatic nucleus to the gonadotropin-releasing hormone system: Combined tracing and light and electron microscopic immunocytochemical studies. J Comp Neurol. 384:1997;569-579.
90. van der Beek E M, Wiegant V M, van der Donk H A, van den Hunk R, Buijs R M. Lesion of the suprachiasmatic nucleus indicate the presence of a direct vasoactive intestinal polypeptide-containing projection to gonadotropin-releasing hormone neurons in the female rat. J Neuroendocrinol. 5:1993;137-144.
91. Vrang N, Larsen P J, Mikkelsen J D. Direct projection from the suprachiasmatic nucleus to hypophysiotrophic corticotrophin-releasing factor immunoreactive cells in the paraventricular nucleus of the hypothalamus demonstrated by means of phaseolus vulgaris-leucoagglutinin tract tracing. Brain Res. 684:1995;61-69.
92. Vrang N, Mikkelsen J D, Lansen P J. Direct link from the suprachiasmatic nucleus to hypothalamic neurons projecting to the spinal cord: A combined tracing study using cholera toxin subunit B and phaseolus vulgaris-leucoagglutinin. Brain Res Bull. 44:1997;671-680.
93. Wagner S, Castel M, Gainer H, Yarom Y. GABA in the mammalian suprachiasmatic nucleus and its role in diurnal rhythmicity. Nature. 387:1997;598-603.
94. Wang H, Morris J F. Presence of neuronal nitric oxide synthase in the suprachiasmatic nuclei of mouse and rat. Neuroscience. 74:1996;1059-1068.
95. Watts A G, Swanson L M. Efferent projections of the suprachiasmatic nucleus. II. Studies using retrograde transport of fluorescent dyes and simultaneous peptide immunohistochemistry in the rat. J Comp Neurol. 258:1987;230-252.
96. Watts A G, Swanson L W, Sanchez-Watts G. Efferent projections of the suprachiasmatic nucleus: I. Studies using anterograde transport of phaseolus vulgaris leucoaggulatinin in the rat. J Comp Neurol. 258:1987;204-229.
97. Welsh D K, Logothetis D E, Meister M, Reppert S M. Individual neurons dissociated from rat suprachiasmatic nucleus express independently phased circadian firing rhythms. Neuron. 14:1995;697-706.
98. Wollnik F, Brtsch W, Uhlmann E, Gillardon F, Bravo R, Zimmermann M, Schlingensiepen K H, Herdegen T. Block of c-fos and Jun B expression by antisense oligonucleotides inhibits light-induced phase shifts of the mammalian circadian clock. Eur J Neurosci. 7:1995;388-393.
99. Young M W. The molecular control of circadian behavioral rhythms and their entrainment in Drosophila. Annu Rev Biochem. 67:1998;135-152.
100. Young M W, Weitz C J, Takahashi J S. Mammalian circadian regulate CLOCK-BMAL1-induced transcription. Neuron. 21:1998;1101-1103.
101. Zylka M J, Shearman L P, Weaver D R, Reppert S M. Three period homolog in mammals: differential light responses in the suprachiasmatic circadian clock and oscillating transcripts outside of brain. Neuron. 20:1998;1103-1110.
102. Zylka M J, Shearman L P, Levine J D, Jin X, Weaver D R, Reppert S M. Molecular analysis of mammalian Timeless. Neuron. 21:1998;1115-1122.