Targeted mutation of the calbindin D28k gene selectively alters nonvisual photosensitivity

European Journal of Neuroscience

Volumn 33, Issue 12, 2011, Pages 2299-2307

  Butler, Matthew P ^a   Lesauter, Joseph ^b   Sichel, Amarynth N ^b   Silver, Rae ^a,b,c  

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

^b Program on US Russia Relations at Columbia s Harriman Institute   (United States)

^c Department of Medicine   (United States)

Author keywords

Circadian rhythms; Entrainment; Masking; Mouse; Pupillary reflex

Indexed keywords

ATROPINE; CALBINDIN; CARBACHOL;

ANATOMICAL VARIATION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CILIARY GANGLION; CONTROLLED STUDY; EDINGER WESTPHAL NUCLEUS; GENE MUTATION; LIGHT INTENSITY; MALE; MOUSE; NONHUMAN; OLIVARY NUCLEUS; PHOTOSENSITIVITY; PHOTOSTIMULATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PUPIL REFLEX; VISUAL SYSTEM; WILD TYPE;

ANIMALS; ATROPINE; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CARBACHOL; CIRCADIAN RHYTHM; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOTOR ACTIVITY; NEURAL PATHWAYS; PHOTIC STIMULATION; PHOTOPERIOD; REFLEX, PUPILLARY; VISION, OCULAR; VISUAL PERCEPTION;

EID: 79959363810     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2011.07689.x     Document Type: Article

References (59)

1. 28k gene. Proc. Natl. Acad. Sci. USA, 94, 1488-1493.
2. Aschoff, J. (1960) Exogenous and endogenous components in circadian rhythms. Cold Spring Harb. Symp. Quant. Biol., 25, 11-28.
3. Baumgardt, E. (1972) Threshold quantal problems. In Jameson, D. & Hurvich, L.M. (Eds), Handbook of Sensory Physiology. Springer-Verlag, New York, pp. 29-55.
4. Berson, D.M. (2003) Strange vision: ganglion cells as circadian photoreceptors. Trends Neurosci., 26, 314-320.
5. Bowes, C., Li, T., Danciger, M., Baxter, L.C., Applebury, M.L. & Farber, D.B. (1990) Retinal degeneration in the rd mouse is caused by a defect in the β subunit of rod cGMP-phosphodiesterase. Nature, 347, 677-680.
6. Butler, M.P. & Silver, R. (2011) Divergent photic thresholds in the non-image-forming visual system: entrainment, masking and pupillary light reflex. Proc. R. Soc. B., 278, 745-750.
7. 28K protein cells in a primate suprachiasmatic nucleus: localization, daily rhythm and age-related changes. Eur. J. Neurosci., 26, 2025-2032.
8. Ciarleglio, C.M., Axley, J.C., Strauss, B.R., Gamble, K.L. & McMahon, D.G. (2011) Perinatal photoperiod imprints the circadian clock. Nat. Neurosci., 14, 25-27.
9. Dkhissi-Benyahya, O., Sicard, B. & Cooper, H.M. (2000) Effects of irradiance and stimulus duration on early gene expression (Fos) in the suprachiasmatic nucleus: temporal summation and reciprocity. J. Neurosci., 20, 7790-7797.
10. Do, M.T., Kang, S.H., Xue, T., Zhong, H., Liao, H.W., Bergles, D.E. & Yau, K.W. (2009) Photon capture and signalling by melanopsin retinal ganglion cells. Nature, 457, 281-287.
11. Doyle, S.E., Yoshikawa, T., Hillson, H. & Menaker, M. (2008) Retinal pathways influence temporal niche. Proc. Natl. Acad. Sci. USA, 105, 13133-13138.
12. Drouyer, E., LeSauter, J., Hernandez, A.L. & Silver, R. (2010) Specializations of gastrin-releasing peptide cells of the mouse suprachiasmatic nucleus. J. Comp. Neurol., 518, 1249-1263.
13. Ecker, J.L., Dumitrescu, O.N., Wong, K.Y., Alam, N.M., Chen, S.K., LeGates, T., Renna, J.M., Prusky, G.T., Berson, D.M. & Hattar, S. (2010) Melanopsin-expressing retinal ganglion-cell photoreceptors: cellular diversity and role in pattern vision. Neuron, 67, 49-60.
14. Govardovskii, V.I., Fyhrquist, N., Reuter, T., Kuzmin, D.G. & Donner, K. (2000) In search of the visual pigment template. Vis. Neurosci., 17, 509-528.
15. Grubb, M.S. & Thompson, I.D. (2004) Biochemical and anatomical subdivision of the dorsal lateral geniculate nucleus in normal mice and in mice lacking the β2 subunit of the nicotinic acetylcholine receptor. Vision Res., 44, 3365-3376.
16. Güler, A.D., Ecker, J.L., Lall, G.S., Haq, S., Altimus, C.M., Liao, H.W., Barnard, A.R., Cahill, H., Badea, T.C., Zhao, H., Hankins, M.W., Berson, D.M., Lucas, R.J., Yau, K.W. & Hattar, S. (2008) Melanopsin cells are the principal conduits for rod-cone input to non-image-forming vision. Nature, 453, 102-105.
17. Hamada, T., LeSauter, J., Lokshin, M., Romero, M.T., Yan, L., Venuti, J.M. & Silver, R. (2003) Calbindin influences response to photic input in suprachiasmatic nucleus. J. Neurosci., 23, 8820-8826.
18. Harrington, M.E. & Rusak, B. (1991) Luminance coding properties of intergeniculate leaflet neurons in the golden hamster and the effects of chronic clorgyline. Brain Res., 554, 95-104.
19. Hatori, M., Le, H., Vollmers, C., Keding, S.R., Tanaka, N., Buch, T., Waisman, A., Schmedt, C., Jegla, T. & Panda, S. (2008) Inducible ablation of melanopsin-expressing retinal ganglion cells reveals their central role in non-image forming visual responses. PLoS ONE, 3, e2451.
20. Hattar, S., Lucas, R.J., Mrosovsky, N., Thompson, S., Douglas, R.H., Hankins, M.W., Lem, J., Biel, M., Hofmann, F., Foster, R.G. & Yau, K.W. (2003) Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice. Nature, 424, 76-81.
21. Haverkamp, S. & Wässle, H. (2000) Immunocytochemical analysis of the mouse retina. J. Comp. Neurol., 424, 1-23.
22. 28k and calretinin expression in the mouse suprachiasmatic nucleus. Eur. J. Neurosci., 17, 1111-1118.
23. Kim, H.J. & Harrington, M.E. (2008) Neuropeptide Y-deficient mice show altered circadian response to simulated natural photoperiod. Brain Res., 1246, 96-100.
24. Kozicz, T. (2003) Neurons colocalizing urocortin and cocaine and amphetamine-regulated transcript immunoreactivities are induced by acute lipopolysaccharide stress in the Edinger-Westphal nucleus in the rat. Neuroscience, 116, 315-320.
25. Kriegsfeld, L.J., LeSauter, J. & Silver, R. (2004) Targeted microlesions reveal novel organization of the hamster suprachiasmatic nucleus. J. Neurosci., 24, 2449-2457.
26. 28K gene disrupts circadian rhythmicity and entrainment. Eur. J. Neurosci., 27, 2907-2921.
27. Kuder, T. (1986) The ciliary ganglion in mouse. Folia Morphol. (Warsz)., 45, 80-85.
28. Lall, G.S., Revell, V.L., Momiji, H., Al Enezi, J., Altimus, C.M., Guler, A.D., Aguilar, C., Cameron, M.A., Allender, S., Hankins, M.W. & Lucas, R.J. (2010) Distinct contributions of rod, cone, and melanopsin photoreceptors to encoding irradiance. Neuron, 66, 417-428.
29. LeSauter, J. & Silver, R. (1999) Localization of a suprachiasmatic nucleus subregion regulating locomotor rhythmicity. J. Neurosci., 19, 5574-5585.
30. Li, X., Gilbert, J. & Davis, F.C. (2005) Disruption of masking by hypothalamic lesions in Syrian hamsters. J. Comp. Physiol. [A], 191, 23-30.
31. Lucas, R.J., Douglas, R.H. & Foster, R.G. (2001) Characterization of an ocular photopigment capable of driving pupillary constriction in mice. Nat. Neurosci., 4, 621-626.
32. Lucas, R.J., Hattar, S., Takao, M., Berson, D.M., Foster, R.G. & Yau, K.W. (2003) Diminished pupillary light reflex at high irradiances in melanopsin-knockout mice. Science, 299, 245-247.
33. Mahoney, M.M., Nunez, A.A. & Smale, L. (2000) Calbindin and Fos within the suprachiasmatic nucleus and the adjacent hypothalamus of Arvicanthis niloticus and Rattus norvegicus. Neuroscience, 99, 565-575.
34. Mai, J.K., Kedziora, O., Teckhaus, L. & Sofroniew, M.V. (1991) Evidence for subdivisions in the human suprachiasmatic nucleus. J. Comp. Neurol., 305, 508-525.
35. Morin, L.P. & Allen, C.N. (2006) The circadian visual system, 2005. Brain. Res. Rev., 51, 1-60.
36. Mrosovsky, N. (1999) Masking: history, definitions, and measurement. Chronobiol. Int., 16, 415-429.
37. Mrosovsky, N. & Hattar, S. (2003) Impaired masking responses to light in melanopsin-knockout mice. Chronobiol. Int., 20, 989-999.
38. Mrosovsky, N., Foster, R.G. & Salmon, P.A. (1999) Thresholds for masking responses to light in three strains of retinally degenerate mice. J. Comp. Physiol. A., 184, 423-428.
39. Mure, L.S., Rieux, C., Hattar, S. & Cooper, H.M. (2007) Melanopsin-dependent nonvisual responses: evidence for photopigment bistability in vivo. J. Biol. Rhythms, 22, 411-424.
40. Nelson, D.E. & Takahashi, J.S. (1991) Sensitivity and integration in a visual pathway for circadian entrainment in the hamster (Mesocricetus auratus). J. Physiol., 439, 115-145.
41. Nelson, D.E. & Takahashi, J.S. (1999) Integration and saturation within the circadian photic entrainment pathway of hamsters. Am. J. Physiol., 277, R1351-R1361.
42. Panda, S., Nayak, S.K., Campo, B., Walker, J.R., Hogenesch, J.B. & Jegla, T. (2005) Illumination of the melanopsin signaling pathway. Science, 307, 600-604.
43. Pasteels, B., Rogers, J., Blachier, F. & Pochet, R. (1990) Calbindin and calretinin localization in retina from different species. Vis. Neurosci., 5, 1-16.
44. Pohl, H. (1976) Proportional effect of light on entrained circadian-rhythms of birds and mammals. J. Comp. Physiol., 112, 103-108.
45. van den Pol, A.N., Cao, V. & Heller, H.C. (1998) Circadian system of mice integrates brief light stimuli. Am. J. Physiol., 275, R654-R657.
46. Redlin, U., Vrang, N. & Mrosovsky, N. (1999) Enhanced masking response to light in hamsters with IGL lesions. J. Comp. Physiol. [A], 184, 449-456.
47. Rintoul, G.L., Raymond, L.A. & Baimbridge, K.G. (2001) Calcium buffering and protection from excitotoxic cell death by exogenous calbindin-D28k in HEK 293 cells. Cell Calcium., 29, 277-287.
48. 28k. J. Physiol., 551, 13-32.
49. Sekaran, S., Lupi, D., Jones, S.L., Sheely, C.J., Hattar, S., Yau, K.W., Lucas, R.J., Foster, R.G. & Hankins, M.W. (2005) Melanopsin-dependent photoreception provides earliest light detection in the mammalian retina. Curr. Biol., 15, 1099-1107.
50. Silver, R., LeSauter, J., Tresco, P.A. & Lehman, M.N. (1996) A diffusible coupling signal from the transplanted suprachiasmatic nucleus controlling circadian locomotor rhythms. Nature, 382, 810-813.
51. Silver, R., Sookhoo, A.I., LeSauter, J., Stevens, P., Jansen, H.T. & Lehman, M.N. (1999) Multiple regulatory elements result in regional specificity in circadian rhythms of neuropeptide expression in mouse SCN. Neuroreport, 10, 3165-3174.
52. 28k alters response of the murine circadian clock to light. Chronobiol. Int., 27, 68-82.
53. Stephan, F.K. & Zucker, I. (1972) Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions. Proc. Natl. Acad. Sci. USA, 69, 1583-1586.
54. Sun, H., Macke, J.P. & Nathans, J. (1997) Mechanisms of spectral tuning in the mouse green cone pigment. Proc. Natl. Acad. Sci. USA, 94, 8860-8865.
55. Takahashi, J.S., DeCoursey, P.J., Bauman, L. & Menaker, M. (1984) Spectral sensitivity of a novel photoreceptive system mediating entrainment of mammalian circadian rhythms. Nature, 308, 186-188.
56. Thompson, S., Foster, R.G., Stone, E.M., Sheffield, V.C. & Mrosovsky, N. (2008) Classical and melanopsin photoreception in irradiance detection: negative masking of locomotor activity by light. Eur. J. Neurosci., 27, 1973-1979.
57. Wright, K.P. Jr, Gronfier, C., Duffy, J.F. & Czeisler, C.A. (2005) Intrinsic period and light intensity determine the phase relationship between melatonin and sleep in humans. J. Biol. Rhythms, 20, 168-177.
58. Yamazaki, S., Alones, V. & Menaker, M. (2002) Interaction of the retina with suprachiasmatic pacemakers in the control of circadian behavior. J. Biol. Rhythms, 17, 315-329.
59. Zhu, Y., Tu, D.C., Denner, D., Shane, T., Fitzgerald, C.M. & Van Gelder, R.N. (2007) Melanopsin-dependent persistence and photopotentiation of murine pupillary light responses. Invest. Ophthalmol. Vis. Sci., 48, 1268-1275.