Phenotype Matters: Identification of Light-Responsive Cells in the Mouse Suprachiasmatic Nucleus

Journal of Neuroscience

Volumn 24, Issue 1, 2004, Pages 68-75

  Karatsoreos, Ilia N ^a   Yan, Lily ^a   LeSauter, Joseph ^b   Silver, Rae ^a,b,c  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b Barnard College of Columbia University   (United States)

^c MC5501 ^*  (United States)

Author keywords

Circadian rhythms; Clock gene; GFP reporter; GRP; mPer1; SCN; Transgenic

Indexed keywords

CALBINDIN; GASTRIN RELEASING PEPTIDE; GREEN FLUORESCENT PROTEIN; MESSENGER RNA; PROTEIN FOS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL ARTIFICIAL CHROMOSOME; BRAIN CELL; CELL COMMUNICATION; CELL SECRETION; CELL TYPE; CIRCADIAN RHYTHM; CONTROLLED STUDY; GENE; GENE EXPRESSION; GENE INDUCTION; GENE INSERTION; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; LIGHT; MOUSE; NONHUMAN; PERIOD 1 GENE; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; REPORTER GENE; STRAIN DIFFERENCE; SUPRACHIASMATIC NUCLEUS; TRANSGENE;

ANIMALS; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CELL CYCLE PROTEINS; CIRCADIAN RHYTHM; GASTRIN-RELEASING PEPTIDE; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; LIGHT; LUMINESCENT PROTEINS; MICE; MICE, TRANSGENIC; NUCLEAR PROTEINS; PHENOTYPE; PROMOTER REGIONS (GENETICS); RNA, MESSENGER; SUPRACHIASMATIC NUCLEUS;

EID: 0842301344     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1666-03.2004     Document Type: Article

References (60)

1. Abercrombie M (1946) Estimation of nuclear populations from microtome sections. Anat Rec 94:239-247.
2. Abrahamson EE, Moore RY (2001) Suprachiasmatic nucleus in the mouse: retinal innervation, intrinsic organization and efferent projections. Brain Res 916:172-191.
3. Aggelopoulos NC, Meissl H (2000) Responses of neurones of the rat suprachiasmatic nucleus to retinal illumination under photopic and scotopic conditions. J Physiol (Lond) 523:211-222.
4. Aida R, Moriya T, Araki M, Akiyama M, Wada K, Wada E, Shibata S (2002) Gastrin-releasing peptide mediates photic entrainable signals to dorsal subsets of suprachiasmatic nucleus via induction of period gene in mice. Mol Pharmacol 61:26-34.
5. Aioun J, Chambille I, Peytevin J, Martinet L (1998) Neurons containing gastrin-releasing peptide and vasoactive intestinal polypeptide are involved in the reception of the photic signal in the suprachiasmatic nucleus of the Syrian hamster: an immunocytochemical ultrastructural study. Cell Tissue Res 291:239-253.
6. Albers HE, Gillespie CF, Babagbemi TO, Huhman KL (1995) Analysis of the phase shifting effects of gastrin releasing peptide when microinjected into the suprachiasmatic region. Neurosci Lett 191:63-66.
7. Antle MC, Foley DK, Foley NC, Silver R (2003) Gates and oscillators: a network model of the brain clock. J Biol Rhythms 18:339-350.
8. Arvanitogiannis A, Robinson B, Beaule C, Amir S (2000) Calbindin-D28k immunoreactivity in the suprachiasmatic nucleus and the circadian response to constant light in the rat. Neuroscience 99:397-401.
9. Best JD, Maywood ES, Smith KL, Hastings MH (1999) Rapid resetting of the mammalian circadian clock. J Neurosci 19:828-835.
10. Card JP, Moore RY (1984) The suprachiasmatic nucleus of the golden hamster: immunohistochemical analysis of cell and fiber distribution. Neuroscience 13:415-431.
11. Castel M, Belenky M, Cohen S, Wagner S, Schwartz WJ (1997) Light-induced c-Fos expression in the mouse suprachiasmatic nucleus: immunoelectron microscopy reveals co-localization in multiple cell types. Eur J Neurosci 9:1950-1960.
12. Cui LN, Dyball RE (1996) Synaptic input from the retina to the suprachiasmatic nucleus changes with the light-dark cycle in the Syrian hamster. J Physiol (Lond) 497:483-493.
13. DiLeone RJ, Marcus GA, Johnson MD, Kingsley DM (2000) Efficient studies of long-distance Bmp5 gene regulation using bacterial artificial chromosomes. Proc Natl Acad Sci USA 97:1612-1617.
14. Earnest DJ, DiGiorgio S, Olschowka JA (1993) Light induces expression of fos-related proteins within gastrin-releasing peptide neurons in the rat suprachiasmatic nucleus. Brain Res 627:205-209.
15. Eskin A (1979) Identification and physiology of circadian pacemakers. Introduction. Fed Proc 38:2570-2572.
16. Field MD, Maywood ES, O'Brien JA, Weaver DR, Reppert SM, Hastings MH (2000) Analysis of clock proteins in mouse SCN demonstrates phylogenetic divergence of the circadian clockwork and resetting mechanisms. Neuron 25:437-447.
17. Groos GA, Mason R (1980) The visual properties of rat and cat suprachiasmatic neurones. J Comp Neurol 349-356.
18. Hamada T, LeSauter J, Venuti JM, Silver R (2001) Expression of period genes: rhythmic and nonrhythmic compartments of the suprachiasmatic nucleus pacemaker. J Neurosci 21:7742-7750.
19. Jobst EE, Allen CN (2002) Calbindin neurons in the hamster suprachiasmatic nucleus do not exhibit a circadian variation in spontaneous firing rate. Eur J Neurosci 16:2469-2474.
20. Johnson RF, Morin LP, Moore RY (1988) Retinohypothalamic projections in the hamster and rat demonstrated using cholera toxin. Brain Res 462:301-312.
21. Klien D, Moore R, Reppert S (1991) Suprachiasmatic nucleus: the mind's clock. Oxford: Oxford UP.
22. Kuhlman SJ, Quintero JE, McMahon DG (2000) GFP fluorescence reports period 1 circadian gene regulation in the mammalian biological clock. NeuroReport 11:1479-1482.
23. Kuhlman SJ, Silver R, Le Sauter J, Bult-Ito A, McMahon DG (2003) Phase resetting light pulses induce Per1 and persistent spike activity in a subpopulation of biological clock neurons. J Neurosci 23:1441-1450.
24. LeSauter J, Silver R (1999) Localization of asuprachiasmatic nucleus subregion regulating locomotor rhythmicity. J Neurosci 19:5574-5585.
25. LeSauter J, Yan L, Vishnubhotla B, Quintero JE, Kuhlman SJ, McMahon DG, Silver R (2003) A short half-life GFP mouse model for analysis of suprachiasmatic nucleus organization. Brain Res 964:279-287.
26. Lowrey PL, Takahashi JS (2000) Genetics of the mammalian circadian system: photic entrainment, circadian pacemaker mechanisms, and posttranslational regulation. Annu Rev Genet 34:533-562.
27. McArthur AJ, Coogan AN, Ajpru S, Sugden D, Biello SM, Piggins HD (2000) Gastrin-releasing peptide phase-shifts suprachiasmatic nuclei neuronal rhythms in vitro. J Neurosci 20:5496-5502.
28. Meijer JH, Groos GA, Rusak B (1986) Luminance coding in a circadian pacemaker: the suprachiasmatic nucleus of the rat and the hamster. Brain Res 382:109-118.
29. Mikkelsen JD, Larsen PJ, Sorensen GG, Woldbye D, Bolwig TG, Hastings MH, Ebling FJ (1994) A dual-immunocytochemical method to localize c-fos protein in specific neurons based on their content of neuropeptides and connectivity. Histochemistry 101:245-251.
30. Moore RY (1992) The fourth C.U. Ariens Kappers lecture. The organization of the human circadian timing system. Prog Brain Res 93:99-115.
31. Moore RY (1996) Entrainment pathways and the functional organization of the circadian system. Prog Brain Res 111:103-119.
32. Moore RY, Silver R (1998) Suprachiasmatic nucleus organization. Chronobiol Int 15:475-487.
33. Moore RY, Speh JC, Leal, RK (2002) Suprachiasmatic nucleus organization. Cell Tissue Res 309:89-98.
34. Morin LP (1994) The circadian visual system. Brain Res Brain Res Rev 19:102-127.
35. Nakamura W, Honma S, Shirakawa T, Honma K (2001) Regional pacemakers composed of multiple oscillator neurons in the rat suprachiasmatic nucleus. Eur J Neurosci 14:666-674.
36. Panda S, Provencio I, Tu DC, Pires SS, Rollag MD, Castrucci AM, Pletcher MT, Sato TK, Wiltshire T, Andahazy M, Kay SA, Van Gelder RN, Hogenesch JB (2003) Melanopsin is required for non-image-forming photic responses in blind mice. Science 301:525-527.
37. Piggins HD, Rusak B (1993) Electrophysiological effects of pressure-ejected bombesin-like peptides on hamster suprachiasmatic nucleus neurons in vitro. J Neuroendocrinol 5:575-581.
38. Piggins HD, Cutler DJ, Rusak B (1994) Effects of ionophoretically applied bombesin-like peptides on hamster suprachiasmatic nucleus neurons in vitro. Eur J Pharmacol 271:413-419.
39. Piggins HD, Antle MC, Rusak B (1995) Neuropeptides phase shift the mammalian circadian pacemaker. J Neurosci 15:5612-5622.
40. Reppert SM, Weaver DR (2001) Molecular analysis of mammalian circadian rhythms. Annu Rev Physiol 63:647-676.
41. Reppert SM, Weaver DR (2002) Coordination of circadian timing in mammals. Nature 418:935-941.
42. Romijn HJ, Sluiter AA, Pool CW, Wortel J, Buijs RM (1996) 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 372:1-8.
43. Sawaki Y (1979) Suprachiasmatic nucleus neurones: excitation and inhibition mediated by the direct retino-hypothalamic projection in female rats. Exp Brain Res 37:127-138.
44. Shearman LP, Sriram S, Weaver DR, Maywood ES, Chaves I, Zheng B, Kume K, Lee CC, van der Horst GT, Hastings MH, Reppert SM (2000) Interacting molecular loops in the mammalian circadian clock. Science 288:1013-1019.
45. Shibata S, Liou S, Ueki S, Oomura Y (1984) Influence of environmental light-dark cycle and enucleation on activity of suprachiasmatic neurons in slice preparations. Brain Res 302:75-81.
46. Shigeyoshi Y, Taguchi K, Yamamoto S, Takekida S, Yan L, Tei H, Moriya T, Shibata S, Loros JJ, Dunlap JC, Okamura H (1997) Light-induced resetting of a mammalian circadian clock is associated with rapid induction of the mPer1 transcript. Cell 91:1043-1053.
47. 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.
48. Silver R, Romero MT, Besmer HR, Leak R, Nunez JM, LeSauter J (1996) Calbindin-D28K cells in the hamster SCN express light-induced Fos. NeuroReport 7:1224-1228.
49. Silver R, Sookhoo 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.
50. Tanaka M, Ichitani Y, Okamura H, Tanaka Y, Ibata Y (1993) The direct retinal projection to VIP neuronal elements in the rat SCN. Brain Res Bull 31:637-640.
51. Tanaka M, Hayashi S, Tamada Y, Ikeda T, Hisa Y, Takamatsu T, Ibata Y (1997) Direct retinal projections to GRP neurons in the suprachiasmatic nucleus of the rat. NeuroReport 8:2187-2191.
52. Van den Pol AN (1980) The hypothalamic suprachiasmatic nucleus of rat: intrinsic anatomy. J Comp Neurol 191:661-702.
53. Van den Pol AN, Tsujimoto KL (1985) Neurotransmitters of the hypothalamic suprachiasmatic nucleus: immunocytochemical analysis of 25 neuronal antigens. Neuroscience 15:1049-1086.
54. Watanabe K, Deboer T, Meijer JH (2001) Light-induced resetting of the circadian pacemaker: quantitative analysis of transient versus steady-state phase shifts. J Biol Rhythms 16:564-573.
55. 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.
56. Witkovsky P, Veisenberger E, LeSauter J, Yan L, Johnson M, Zhang DQ, McMahon D, Silver R (2003) Cellular location and circadian rhythm of expression of the biological clock gene Period 1 in the mouse retina. J Neurosci 23:7670-7676.
57. Yan L, Okamura H (2002) Gradients in the circadian expression of Per1 and Per2 genes in the rat suprachiasmatic nucleus. Eur J Neurosci 15:1153-1162.
58. Yan L, Silver R (2002) Differential induction and localization of mPer1 and mPer2 during advancing and delaying phase shifts. Eur J Neurosci 16:1531-1540.
59. Yang XW, Model P, Heintz N (1997) Homologous recombination based modification in Escherichia coli and germline transmission in transgenic mice of a bacterial artificial chromosome. Nat Biotechnol 15:859-865.
60. Young MW, Kay SA (2001) Time zones: a comparative genetics of circadian clocks. Nat Rev Genet 2:702-715.