Residual photosensitivity in mice lacking both rod opsin and cone photoreceptor cyclic nucleotide gated channel 3 α subunit

Visual Neuroscience

Volumn 21, Issue 5, 2004, Pages 675-683

  Barnard, Alun R ^a,g   Appleford, Joanne M ^a   Sekaran, Sumathi ^a   Chinthapalli, Krishna ^a   Jenkins, Aaron ^a   Seeliger, Matheas ^b   Biel, Martin ^c   Humphries, Peter ^d   Douglas, Ron H ^e   Wenzel, Andreas ^f   Foster, Russell G ^a   Hankins, Mark W ^a   Lucas, Robert J ^a,g  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^c UNIVERSITY OF MUNICH   (Germany)

^d TRINITY COLLEGE DUBLIN   (Ireland)

^e CITY UNIVERSITY   (United Kingdom)

^f Laboratory for Retinal Cell Biology   (Switzerland)

^g UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Circadian entrainment; Heart rate; Light; Melanopsin; Retinal degeneration

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; ELECTRORETINOGRAPHY; FLUORESCENCE; GENE INDUCTION; HEART RATE; IMAGING SYSTEM; IMMEDIATE EARLY GENE; IMMUNOHISTOCHEMISTRY; INFORMATION PROCESSING; LIGHT EXPOSURE; LOCOMOTION; MOUSE; MOUSE STRAIN; NONHUMAN; ONCOGENE C FOS; PHOTORECEPTOR; PHOTOSENSITIVITY; PHOTOSTIMULATION; PHOTOTRANSDUCTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PUPIL REFLEX; PUPILLOMETRY; RETINA CONE; RETINA GANGLION CELL; RETINA INNER PLEXIFORM LAYER; RETINA ROD; SUPRACHIASMATIC NUCLEUS; WILD TYPE;

ANIMALS; CALCIUM; CIRCADIAN RHYTHM; CONES (RETINA); ELECTRORETINOGRAPHY; FURA-2; GENE DELETION; HEART RATE; ION CHANNELS; LIGHT; MICE; MICE, INBRED C3H; MICE, KNOCKOUT; MODELS, ANIMAL; MOTOR ACTIVITY; OPSIN; PHOTORECEPTORS, VERTEBRATE; PHOTOTRANSDUCTION; PROTO-ONCOGENE PROTEINS C-FOS; REFLEX, PUPILLARY; RETINAL GANGLION CELLS; RHODOPSIN; RODS (RETINA);

EID: 19944426972     PISSN: 09525238     EISSN: None     Source Type: Journal    
DOI: 10.1017/S0952523804215024     Document Type: Article

References (50)

1. ALBRECHT, U. & FOSTER, R.G. (2002). Placing ocular mutants into a functional context: A chronobiological approach. Methods 28, 465-477.
2. BELENKY, M.A., SMERASKI, C.A., PROVENCIO, I., SOLLARS, P.J. & PICKARD, G.E. (2003). Melanopsin retinal ganglion cells receive bipolar and amacrine cell synapses. Journal of Comparative Neurology 460, 380-393.
3. BENCA, R.M., GILLILAND, M.A. & OBERMEYER, W.H. (1998). Effects of lighting conditions on sleep and wakefulness in albino lewis and pigmented brown norway rats. Sleep 21, 451-460.
4. BERSON, D., DUNN, F. & TAKAO, M. (2002). Phototransduction by retinal ganglion cells that set the circadian clock. Science 295, 1070-1073.
5. BIEL, M., SEELIGER, M., PFEIFER, A., KOHLER, K., GERSTNER, A., LUDWIG, A., JAISSLE, G., FAUSER, S., ZRENNER, E. & HOFMANN, F. (1999). Selective loss of cone function in mice lacking the cyclic nucleotidegated channel cng3. Proceedings of the National Academy Sciences of the U.S.A. 96, 7553-7557.
6. 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 beta subunit of rod cGMP-phosphodiesterase. Nature 347, 677-680.
7. CAJOCHEN, C., ZEITZER, J.M., CZEISLER, C.A. & DUK, D.-J. (2000). Dose-response relationship for light intensity and ocular and electroencephalographic correlates of human alertness. Behavioral Brain Research 115, 75-83.
8. CARTER-DAWSON, L.D., LAVAIL, M.M. & SIDMAN, R.L. (1978). Differential effect of the rd mutation on rods and cones in the mouse retina. Investigative Ophthalmology and Visual Sciences 17, 489-498.
9. CZEISLER, C.A., SHANAHAN, T.L., KLERMAN, E.B., MARTENS, H., BROTMAN, D.J., EMENS, J.S., KLEIN, T. & RIZZO, J.F. (1995). Suppression of melatonin secretion in some blind patients by exposure to bright light. New England Journal of Medicine 332, 6-11.
10. EBIHARA, S. & TSUJI, K. (1980). Entrainment of the circadian activity rhythm to the light cycle: Effective light intensity for a zeitgeber in the retinal degenerate c3h mouse and the normal c57b1 mouse. Physiology & Behavior 24, 523-527.
11. FOSTER, R.G., PROVENCIO, I., HUDSON, D., FISKE, S., DE GRIP, W. & MENAKER, M. (1991). Circadian photoreception in the retinally degenerate mouse (rd/rd). Journal of Comparative Physiology (A) 169, 39-50.
12. FREEDMAN, M.S., LUCAS, R.J., SONI, B., VON SCHANTZ, M., MUNOZ, M., DAVID-GRAY, Z. & FOSTER, R.G. (1999). Regulation of mammalian circadian behavior by non-rod, non-cone, ocular photoreceptors. Science 284, 502-504.
13. GOOLEY, J.J., Lu, J., CHOU, T.C., SCAMMELL, T.E. & SAPER, C.B. (2001). Melanopsin in cells of origin of the retinohypothalamic tract. Nature Neuroscience 4, 1165.
14. GOOLEY, J.J., LU, J., FISCHER, D. & SAPER, C.B. (2003). A broad role for melanopsin in nonvisual photoreception. Journal of Neuroscience 23, 7093-7106.
15. HANKINS, M.W. & LUCAS, R.J. (2002). The primary visual pathway in humans is regulated according to long-term light exposure through the action of a nonclassical photopigment. Current Biology 12, 191-198.
16. HANNIBAL, J., HINDERSSON, P., KNUDSEN, S.M., GEORG, B. & FAHRENKRUG, J. (2002). The photopigment melanopsin is exclusively present in pituitary adenylate cyclase-activating polypeptide-containing retinal ganglion cells of the retinohypothalamic tract. Journal Neuroscience 22, RC191.
17. HATTAR, S., LIAO, H.-W., TAKAO, M., BERSON, D. & YAU, K.-W. (2002). Melanopsin-containing retinal ganglion cells: Architecture, projections, and intrinsic photosensitivity. Science 295, 1065-1070.
18. 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, 75-81.
19. HAVERKAMP, S., CLAES, F., HUMPHRIES, P., BIEL, M. & SEELIGER, M. (2003). Morphological alterations in the retina of cng3-/- / rho-/- double mutant mice. Investigative Ophthalmology Visual Science 44, Abstract 2830.
20. HUERTA, J.J., LLAMOSAS, M.M., CERNUDA-CERNUDA, R. & GARCIA-FERNANDEZ, J.M. (1997). Fos expression in the retina of rd/rd mice during the light/dark cycle. Neuroscience Letters 232, 143-146.
21. HUMPHRIES, M., RANCOURT, D., FARRAR, G., KENNA, P., HAZEL, M., BUSH, R., SIEVING, P., SHEILS, D., MCNALLY, N., CREIGHTON, P., ERVEN, A., BOROS, A., GULYA, K., CAPECCHI, M. & HUMPHRIES, P.H. (1997). Retinopathy induced in mice by targeted disruption of the rhodopsin gene. Nature Genetics 15, 216-219.
22. KLERMAN, E., SHANAHAN, T., BROTMAN, D., RIMMER, D., EMENS, J., RIZZO, J. & CZEISLER, C. (2002). Photic resetting of the human circadian pacemaker in the absence of conscious vision. Journal of Biological Rhythms 17, 548-555.
23. LOCKLEY, S.W., SKENE, D.J., ARENDT, J., TABANDEH, H., BIRD, J.C. & DEFRANCE, R. (1997). Relationship between melatonin rhythms and visual loss in the blind. Journal of Clinical Endocrinology and Metabolism 82, 3763-3770.
24. LUCAS, R., DOUGLAS, R. & FOSTER, R. (2001). Characterization of an ocular photopigment capable of driving pupillary constriction in mice. Nature Neuroscience 4, 621-626.
25. LUCAS, R.J., FREEDMAN, M.S., MUNOZ, M., GARCIA-FERNANDEZ, J.M. & FOSTER, R.G. (1999). Regulation of the mammalian pineal by non-rod, non-cone, ocular photoreceptors. Science 284, 505-507.
26. 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.
27. LUPI, D., COOPER, H., FROEHLICH, A., STANDFORD, L., MCCALL, M. & FOSTER, R. (1999). Transgenic ablation of rod photoreceptors alters the circadian phenotype of mice. Neuroscience 89, 363-374.
28. MORIN, L., BLANCHARD, J. & PROVENCIO, I. (2003). Retinal ganglion cell projections to the hamster suprachiasmatic nucleus, intergeniculate leaflet and visual midbrain: Bifurcation and melanopsin immunoreactivity. Journal of Comparative Neurology 465, 401-416.
29. MROSOVSKY, N. (1994). In praise of masking: Behavioural responses of retinally degenerate mice to dim light. Chronobiology International 11, 343-348.
30. MROSOVSKY, N. & SALMON, P.A. (2002). Learned arbitrary responses to light in mice without rods or cones. Naturwissenschaften 89, 525-527.
31. MROSOVSKY, N., FOSTER, R.G. & SALMON, P.A. (1999). Thresholds for masking responses to light in three strains of retinally degenerate mice. Journal of Comparative Physiology A 184, 423-428.
32. MROSOVSKY, N., LUCAS, R. & FOSTER, R. (2001). Persistence of masking responses to light in mice lacking rods and cones. Journal of Biological Rhythms 16, 585-587.
33. MROSOVSKY, N. & HATTAR, S. (2003). Impaired masking responses to light in melanopsin-knockout mice. Chronobiology International 20, 989-999.
34. MUTOH, T., SHIBATA, S., KORF, H.W. & OKAMURA, H. (2003). Melatonin modulates the light-induced sympathoexcitation and vagal suppression with participation of the suprachiasmatic nucleus in mice. Journal of Physiology 547, 317-332.
35. PANDA, S., SATO, T.K., CASTRUCCI, A.M., ROLLAG, M.D., DEGRIP, W.J., HOGENESCH, J.B., PROVENCIO, I. & KAY, S.A. (2002). Melanopsin (opn4) requirement for normal light-induced circadian phase shifting. Science 301, 2213-2216.
36. PANDA, S., PROVENCIO, I., TU, D.C., PIRES, S.S., ROLLAG, M.D., CASTRUCCI, A.M., PLETCHER, M.T., SATO, T.K., WILTSHIRE, T., ANDAHAZY, M., KAY, S.A., VAN GELDER, R.N. & HOGENESCH, J.B. (2003). Melanopsin is required for non-image-forming photic responses in blind mice. Science 301, 525-527.
37. PROVENCIO, I. & FOSTER, R. (1995). Circadian rhythms in mice can be regulated by photoreceptors with cone-like characteristics. Brain Research 694, 183-190.
38. PROVENCIO, I., ROLLAG, M. & CASTRUCCI, A. (2002). Photoreceptive net in the mammalian retina. Nature 415, 493.
39. RIEUX, C., CARNEY, R., LUPI, D., DKHISSI-BENYAHYA, O., JANSEN, K., CHOUNLAMOUNTRI, N., FOSTER, R.G. & COOPER, H.M. (2002). Analysis of immunohistochemical label of fos protein in the suprachiasmatic nucleus: Comparison of different methods of quantification. Journal of Biological Rhythms 17, 121-136.
40. RUBY, N.F., BRENNAN, T.J., XIE, X., CAO, V., FRANKEN, P., HELLER, H.C. & O'HARA, B.F. (2002). Role of melanopsin in circadian responses to light. Science 298, 2211-2213.
41. SCHEER, F.A., VAN DOORNEN, L.J. & BUJIS, R.M. (1999). Light and diurnal cycle affect human heart rate: Possible role for the circadian pacemaker. Journal of Biological Rhythms 14, 202-212.
42. SCHEER, F.A., TER HORST, G.J., VAN DER VLIET, J. & BUIJS, R.M. (2001). Physiological and anatomic evidence for regulation of the heart by suprachiasmatic nucleus in rats. American Journal of Physiology: Heart and Circulatory Physiology 280, H1391-H1399.
43. SEELIGER, M.W., GRIMM, C., STAHLBERG, F., FRIEDBURG, C., JAISSLE, G., ZRENNER, E., GUO, H., REME, C.E., HUMPHRIES, P., HOFMANN, F., BIEL, M., FARISS, R.N., REDMOND, T.M. & WENZEL, A. (2001). New views on RPE65 deficiency: The rod system is the source of vision in a mouse model of Leber congenital amaurosis. Nature Genetics 29, 70-74.
44. SEKARAN, S., FOSTER, R.G., LUCAS, R.J. & HANKINS, M.W. (2003). Calcium imaging reveals a network of intrinsically light sensitive inner retinal neurones. Current Biology 13, 1290-1298.
45. SEMO, M., LUPI, D., PEIRSON, S.N., BUTLER, J.N. & FOSTER, R.G. (2003). Light-induced c-fos in melanopsin retinal ganglion cells of young and aged rodless/coneless (rd/rd c1) mice. European Journal of Neuroscience 18, 3007-3017.
46. Soucy, E., WANG, Y., NIRENBERG, S., NATHANS, J. & MEISTER, M. (1998). A novel signaling pathway from rod photoreceptors to ganglion cells in mammalian retina. Neuron 21, 481-493.
47. STRETTOI, E., PORCIATTI, V., FALSINI, B., PIGNATELLI, V. & ROSSI, C. (2002). Morphological and functional abnormalities in the inner retina of the rd/rd mouse. Journal of Neuroscience 22, 5492-5504.
48. TREJO, L.J. & CICERONE, C.M. (1982). Retinal sensitivity measured by the pupillary light reflex in rcs and albino rats. Vision Research 22, 1163-1171.
49. WARREN, E.J., ALLEN, C.N., BROWN, R.L. & ROBINSON, D.W. (2003). Intrinsic light responses of retinal ganglion cells projecting to the circadian system. European Journal Neuroscience 17, 1727-1735.
50. YOSHIMURA, T. & EBIHARA, S. (1996). Spectral sensitivity of photoreceptors mediating phase-shifts of circadian rhythms in retinally degenerate cba/j (rd/rd) and normal cba/n (+/+) mice. Journal of Comparative Physiology (A) 178, 797-802.