The role of Clock in the developmental expression of neuropeptides in the suprachiasmatic nucleus

Journal of Comparative Neurology

Volumn 424, Issue 1, 2000, Pages 86-98

  Herzog, Erik D ^a,d   Grace, Michael S ^a,b   Harrer, Christine ^a   Williamson, John ^a   Shinohara, Kazuyuki ^a,c   Block, Gene D ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b Florida Institute of Technology   (United States)

^c YOKOHAMA CITY UNIVERSITY   (Japan)

^d WASHINGTON UNIVERSITY   (United States)

Author keywords

Circadian; Mouse; Pacemaker; Suprachiasmatic nucleus; Vasoactive intestinal polypeptide; Vasopressin

Indexed keywords

VASOACTIVE INTESTINAL POLYPEPTIDE; VASOPRESSIN;

ADOLESCENT; AGE; ANIMAL TISSUE; ARTICLE; BRAIN MATURATION; CIRCADIAN RHYTHM; CONTROLLED STUDY; GENE FUNCTION; GENE MUTATION; HORMONE SYNTHESIS; MALE; MOUSE; NEUROENDOCRINOLOGY; NEWBORN; NONHUMAN; ONTOGENY; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; STRAIN DIFFERENCE; SUPRACHIASMATIC NUCLEUS; TISSUE DISTRIBUTION;

AGING; ANIMALS; ANIMALS, NEWBORN; ARGININE VASOPRESSIN; FEMALE; MALE; MICE; MICE, INBRED STRAINS; NEURONS; NEUROPEPTIDES; SUPRACHIASMATIC NUCLEUS; THALAMUS; TISSUE DISTRIBUTION; TRANS-ACTIVATORS; VASOACTIVE INTESTINAL PEPTIDE;

EID: 0034648333     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/1096-9861(20000814)424:1<86::AID-CNE7>3.0.CO;2-W     Document Type: Article

References (80)

1. Aguilar-Roblero R, Salazar-Juarez A, Rojas-Castaneda J, Escobar C, Cintra L. 1997. Organization of circadian rhythmicity and suprachiasmatic nuclei in malnourished rats. Am J Physiol 273:R1321-R1331.
2. Albers HE, Minamitani N, Stopa E, Ferns CF. 1987. Light selectively alters vasoactive intestinal peptide and peptide histidine isoleucine immunoreactivity within the rat suprachiasmatic nucleus. Brain Res 437:189-192.
3. Albers HE, Liou SY, Stopa EG, Zoeller RT. 1991. Interaction of colocalized neuropeptides: functional significance in the circadian timing system. J Neurosci 11:846-851.
4. Altman J, Bayer SA. 1978. Development of the diencephalon in the rat. I. Autoradiographic study of the time of origin and settling patterns of neurons of the hypothalamus. J Comp Neurol 182:945-971.
5. Antoch MP, Song EJ, Chang AM, Vitaterna MH, Zhao Y, Wilsbacher LD, Sangoram AM, King DP, Pinto LH, Takahashi JS. 1997. Functional identification of the mouse circadian Clock gene by transgenic BAC rescue. Cell 89:655-667.
6. Ban Y, Shigeyoshi Y, Okamura H. 1997. Development of vasoactive intestinal peptide mRNA rhythm in the rat suprachiasmatic nucleus. J Neurosci 17:3920-3931.
7. Bosler O, Beaudet A. 1985. VIP neurons as prime synaptic targets for serotonin afferents in rat suprachiasmatic nucleus: a combined radioautographic and immunocytochemical study. J Neurocytol 14:749-763.
8. Brown MH, Nunez AA. 1989. Vasopressin-deficient rats show a reduced amplitude of the circadian sleep rhythm. Physiol Behav 46:759-762.
9. Buijs RM, Hermes MH, Kalsbeek A. 1998. The suprachiasmatic nucleus-paraventricular nucleus interactions: a bridge to the neuroendocrine and autonomic nervous system. Progr Brain Res 119:365-382.
10. Bult A, Hiestand L, Van der Zee EA, Lynch CB. 1993. Circadian rhythms differ between selected mouse lines: a model to study the role of vasopressin neurons in the suprachiasmatic nuclei. Brain Res Bull 32:623-627.
11. Carter DA, Murphy D. 1990. Vasopressin mRNA in parvocellular neurons of the rat suprachiasmatic nucleus exhibits increased poly (A) tail length following water deprivation. Neurosci Lett 109:180-185.
12. Cassone VM, Speh JC, Card JP, Moore RY. 1988 Comparative anatomy of the mammalian hypothalamic suprachiasmatic nucleus. J Biol Rhythms 3:71-91.
13. Castel M, Morris JF. 1988. The neurophysin-containing innervation of the forebrain of the mouse. Neuroscience 24:937-966.
14. Castel M, Feinstein N, Cohen S, Harari N. 1990. Vasopressinergic innervation of the mouse suprachiasmatic nucleus: an immune-electron microscopic analysis. J Comp Neurol 298:172-187.
15. Davis FC, Boada R, LeDeaux J. 1990.Neurogenesis of the hamster suprachiasmatic nucleus. Brain Res 519:192-199.
16. Duncan MJ, Banister MJ, Reppert SM. 1986. Developmental appearance of light-dark entrainment in the rat. Brain Res 369:326-330.
17. Freedman MS, Lucas RJ, Soni B, von Schantz MR, Munoz M, David-Gray Z, Foster R. 1999. Regulation of mammalian circadian behavior by non-rod, non-cone, ocular photo receptors. Science 284:502-504.
18. Fukuhara C, Nishiwaki T, Cagampang FR, Inouye ST. 1994. Emergence of VIP rhythmicity following somatostatin depletion in the rat suprachiasmatic nucleus. Brain Res 645:343-346.
19. Gekakis N, Staknis D, Nguyen HB, Davis FC, Wilsbacher LD, King DP, Takahashi JS, Weitz CJ. 1998. Role of the CLOCK protein in the mammalian circadian mechanism. Science 280:1564-1569.
20. Glazer R. Gozes I. 1994. Diurnal oscillation in vasoactive intestinal peptide gene expression independent of environmental light entraining. Brain Res 644:164-167.
21. Groblewski TA, Nunez AA, Gold RM. 1981. Circadian rhythms in vasopressin deficient rats. Brain Res Bull 6:125-130.
22. Harney JP, Scarbrough K, Rosewell KL, Wise PM. 1996. In vivo antisense antagonism of vasoactive intestinal peptide in the suprachiasmatic nuclei causes aging-like changes in the estradiol-induced luteinizing hormone and prolactin surges. Endocrinology 137:3696-3701.
23. Heimer L, Harlan RE, Alheid GF, Garcia MM, de Olmos J. 1997. Substantia innominata: a notion which impedes clinical-anatomical correlations in neuropsychiatric disorders. Neuroscience 76:957-1006.
24. Herzog ED, Geusz ME, Khalsa SB, Straume M, Block GD. 1997. Circadian rhythms in mouse suprachiasmatic nucleus explants on multimicroelectrode plates. Brain Res 757:285-290.
25. Herzog ED, Takahashi JS, Block GD. 1998. Clock controls circadian period in isolated suprachiasmatic nucleus neurons. Nature Neurosci 1:708-713.
26. Hisano S, Chikamori-Aoyama M, Katoh S, Kagotani Y, Daikoku S, Chihara K. 1988. 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 88:145-150.
27. Honma S, Hiroshige T. 1977. Pubertal manifestation of sex difference in circadian rhythm of corticotrophin-releasing activity in the rat hypothalamus. Acta Endocrinol 86:225-234.
28. Honma S, Shirakawa T, Katsuno Y, Namihira M, Honma K. 1998. Circadian periods of single suprachiasmatic neurons in rats. Neurosci Lett 250:157-160.
29. Hyodo S, Yamada C, Takezawa T, Urano A. 1992. Expression of provasopressin gene during ontogeny in the hypothalamus of developing mice. Neuroscience 46:241-250.
30. Ibata Y, Takahashi Y, Okamura H, Kawakami F, Terubayashi H, Kubo T, Yanaihara N. 1989. Vasoactive intestinal peptide (VIP)-like immunoreactive neurons located in the rat suprachiasmatic nucleus receive a direct retinal projection. Neurosci Lett 97:1-5.
31. Ifft JD. 1972. An autoradiographic study of the time of final division of neurons in rat hypothalamic nuclei. J Comp Neurol 144:193-204.
32. Ingram CD, Snowball RK, Mihai R. 1996. Circadian rhythm of neuronal activity in suprachiasmatic nucleus slices from the vasopressin-deficient Brattleboro rat. Neuroscience 75:635-641.
33. Iwasaki Y, Oiso Y, Saito H, Majzoub JA. 1997. Positive and negative regulation of the rat vasopressin gene promoter. Endocrinology 138: 5266-5274.
34. Jin X, Shearman LP, Weaver DR, Zylka MJ, De Vries GJ, Reppert SM. 1999. A molecular mechanism regulating rhythmic output from the suprachiasmatic circadian clock. Cell 96:57-68.
35. Kalsbeek A, Buijs RM, van Heerikhuize JJ, Arts M, van der Woude TP. 1992. Vasopressin-containing neurons of the suprachiasmatic nuclei inhibit corticosterone release. Brain Res 580:62-67.
36. Kalsbeek A, van Heerikbuize JJ, Wortel J, Buijs RM. 1996a. A diurnal rhythm of stimulatory input to the hypothalamo-pituitary-adrenal system as revealed by timed intrahypothalamic administration of the vasopressin VI antagonist. J Neurosci 16:5555-5565.
37. Kalsbeek A, Van D, Buijs RM. 1996b. Decrease of endogenous vasopressin release necessary for expression of the circadian rise in plasma corticosterone: a reverse microdialysis study. J Neuroendocrinol 8:299-307.
38. King DP, Zhao Y, Sangoram AM, Wilsbacher LD, Tanaka M, Antoch MP, Steeves TD, Vitaterna MH, Kornhauser JM, Lowrey PL, Turek FW, Takahashi JS. 1997. Positional cloning of the mouse circadian clock gene. Cell 89:641-653.
39. Kiss J, Leranth C, Halasz B. 1984. Serotoninergic 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 44:119-124.
40. Klein DC. 1991. Suprachiasmatic nucleus: the mind's clock. New York: Oxford University Press.
41. Krajnak K, Kashon ML, Rosewell KL, Wise PM. 1998. Aging alters the rhythmic expression of vasoactive intestinal polypeptide mRNA but not arginine vasopressin mRNA in the suprachiasmatic nuclei of female rats. J Neurosci 18:4767-4774.
42. Liou SY, Albers HE. 1989. Single unit response of suprachiasmatic neurons to arginine vasopressin (AVP) is mediated by a V1-like receptor in the hamster. Brain Res 477:336-343.
43. Liu C, Weaver DR, Jin X, Shearman LP, Pieschl RL, Gribkoff VK, Reppert SM. 1997. Molecular dissection of two distinct actions of melatonin on the suprachiasmatic circadian clock. Neuron 19:91-102.
44. Lucas RJ, Cagampang FR, Loudon AS, Stirland JA, Coen CW. 1998 Expression of vasoactive intestinal peptide mRNA in the suprachiasmatic nuclei of the circadian tau mutant hamster. Neurosci Lett 249:147-150.
45. Mihai R, Juss TS, Ingram CD. 1994a. Suppression of suprachiasmatic nucleus neurone activity with a vasopressin receptor antagonist: possible role for endogenous vasopressin in circadian activity cycles in vitro. Neurosci Lett 179:95-99.
46. 8]vasotocin on the firing rate of suprachiasmatic neurons in vitro. Neuroscience 62:783-792.
47. Moore RY, Bernstein ME. 1989. Synaptogenesis in the rat suprachiasmatic nucleus demonstrated by electron microscopy and synapsin I immunoreactivity. J Neurosci 9:2151-2162.
48. Moore RY, Silver R. 1998. Suprachiasmatic nucleus organization. Chronobiol Int 15:475-487.
49. Moore RY, Speh JC. 1993. GABA is the principal neurotransmitter of the circadian system. Neurosci Lett 150:112-116.
50. Okamoto S, Okamura H, Miyake M, Takahashi Y, Takagi S, Akagi Y, Fukui K, Okamoto H, Ibata Y. 1991. A diurnal variation of vasoactive intestinal peptide (VIP) mRNA under a daily light-dark cycle in the rat suprachiasmatic nucleus. Histochem 95:525-528.
51. Peters RV, Zoeller RT, Hennessey AC, Stopa EG, Anderson G, Albers HE. 1994. The control of circadian rhythms and the levels of vasoactive intestinal peptide mRNA in the suprachiasmatic nucleus are altered in spontaneously hypertensive rats. Brain Res 639:217-227.
52. Petit JM, Luppi PH, Peyron C, Rampon C, Jouvet M. 1995. VIP-like immunoreactive projections from the dorsal raphe and caudal linear raphe nuclei to the bed nucleus of the stria terminalis demonstrated by a double immunohistochemical method in the rat. Neurosci Lett 193: 77-80.
53. Pickard GE, Sollars PJ, Rinchik EM, Nolan PM, Bucan M. 1995. Mutagenesis and behavioral screening for altered circadian activity identifies the mouse mutant, Wheels. Brain Res 705:255-266.
54. Piggins HD, Antle MC, Rusak B. 1995. Neuropeptides phase shift the mammalian circadian pacemaker. J Neurosci 15:5612-5622.
55. Reghunandanan V, Reghunandanan R, Marya RK. 1991. Vasopressin: its possible role in circadian time keeping. Chronobiologia 18:39-47.
56. Reppert SM, Schwartz WJ. 1984. The suprachiasmatic nuclei of the fetal rat: characterization of a functional circadian clock using 14C-labeled deoxyglucose. J Neurosci 4:1677-1682.
57. Reuss S. 1996. Components and connections of the circadian timing system in mammals. Cell Tissue Res 285:353-378.
58. Romero MT, Silver R. 1990. Time course of peptidergic expression in fetal suprachiasmatic nucleus transplanted into adult hamster. Brain Res Dev Brain Res 57:1-6.
59. Romijn HJ, Sluiter AA, Wortel J, Van Uum JF, Buijs RM. 1998. Immunocytochemical evidence for a diurnal rhythm of neurons showing colocalization of VIP with GRP in the rat suprachiasmatic nucleus. J Comp Neurol 391:397-405.
60. Scarbrough K, Turek FVV. 1996. Quantitative differences in the circadian rhythm of locomotor activity and vasopressin and vasoactive intestinal peptide gene expression in the suprachiasmatic nucleus of tau mutant compared to wildtype hamsters. Brain Res 736:251-259.
61. Shen H, Watanabe M, Tomasiewicz H, Rutishauser U, Magnuson T, Glass JD. 1997. Role of neural cell adhesion molecule and polysialic acid in mouse circadian clock function. J Neurosci 17:5221-5229.
62. Shibata S, Ono M, Tominaga K, Hamada T, Watanabe A, Watanabe S. 1994. Involvement of vasoactive intestinal polypeptide in NMDA-induced phase delay of firing activity rhythm in the suprachiasmatic nucleus in vitro. Neurosci Biobehav Rev 18:591-595.
63. Shinohara K, Tominaga K, Isobe Y, Inouye ST. 1993. Photic regulation of peptides located in the ventrolateral subdivision of the suprachiasmatic nucleus of the rat: daily variations of vasoactive intestinal polypeptide, gastrin-releasing peptide, and neuropeptide Y. J Neurosci 13:793-800.
64. Shinohara K, Honma S, Katsuno Y, Abe H, Honma K. 1995. Two distinct oscillators in the rat suprachiasmatic nucleus in vitro. Proc Natl Acad Sci USA 92:7396-7400.
65. Shinohara K, Tominaga K, Inouye ST. 1998. Luminance-dependent decrease in vasoactive intestinal polypeptide in the rat suprachiasmatic nucleus. Neurosci Lett 251:21-24.
66. Silver R, Sookoo AI, LeSauter J, Stevens P, Jansen HT, Lehman MN. 1999. Multiple regulatory elements result in regional specificity in circadian rhythms of neuropeptide expression in mouse SCN. Neuroreport 10: 3165-3174.
67. Sims KB, Hoffman DL, Said SI, Zimmerman EA. 1980. Vasoactive intestinal polypeptide (VIP) in mouse and rat brain: an immunocytochemical study. Brain Res 186:165-183.
68. Sofroniew MV, Weindl A. 1980. Identification of parvocellular vasopressin and neurophysin neurons in the suprachiasmatic nucleus of a variety of mammals including primates. J Comp Neurol 193:659-675.
69. Sterio DC. 1984. The unbiased estimation of number and sizes of arbitrary particles using the disector. J Microsc 134:127-136.
70. Swanson LW. 1998. Brain maps: structure of the rat brain. New York: Elsevier.
71. Takahashi Y, Okamura H, Yanaihara N, Hamada S, Fujita S, Ibata Y. 1989. Vasoactive intestinal peptide immunoreactive neurons in the rat suprachiasmatic nucleus demonstrate diurnal variation. Brain Res 497:374-377.
72. Tosini G, Menaker M. 1996. Circadian rhythms in cultured mammalian retina. Science 272:419-421.
73. van den Pol AN, Tsujimoto KL. 1985. Neurotransmitters of the hypothalamic suprachiasmatic nucleus: immunocytochemical analysis of 25 neuronal antigens. Neuroscience 15:1049-1086.
74. van der Beek EM, Horvath TL, Wiegant VM, van den Hurk R, Buijs RM. 1997. 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 384:569-579.
75. van der Horst GTJ, Muijtjens M, Kobayashi K, Takano R, Kanno S, Takao M, de Wit J, Verkerk A, Eker APM, van Leenen D, Buijs R, Bootsma D, Hoeijmakers JHJ, Yasui A. m1999. Mammalian Cry1 and Cry2 are essential for maintenance of circadian rhythms. Nature 398:627-630.
76. Van der Zee EA, Jansen K, Gerkema MP. 1999. Severe loss of vasopressin-immunoreactive cells in the suprachiasmatic nucleus of aging voles coincides with reduced circadian organization of running wheel activity. Brain Res 816:572-579.
77. Vitaterna MH, King DP, Chang AM, Kornhauser JM, Lowrey PL, McDonald JD, Dove WF, Pinto LH, Turek FW, Takahashi JS. 1994. Mutagenesis and mapping of a mouse gene, Clock, essential for circadian behavior. Science 264:719-725.
78. Vitaterna MH, Selby CP, Todo T, Niwa H, Thompson C, Fruechte EM, Hitomi K, Thresher RJ, Ishikawa T, Miyazki J, Takahashi JS, Sancar A. 1999. Differential regulation of mammalian Period genes and circadian rhythmicity by cryptochromes 1 and 2. Proc Natl Acad Sci USA 96:12114-12119.
79. Watts AG, Swanson LW. 1987. Efferent projections of the suprachiasmatic nucleus. II. Studies using retrograde transport of fluorescent dyes and simultaneous peptide immunohistochemistry in the rat. J Comp Neurol 258:230-252.
80. Welsh DK, Logothetis DE, Meister M, Reppert SM. 1995. Individual neurons dissociated from rat suprachiasmatic nucleus express independently phased circadian firing rhythms. Neuron 14:697-706.