Impaired circadian photosensitivity in mice lacking glutamate transmission from retinal melanopsin cells

Journal of Biological Rhythms

Volumn 30, Issue 1, 2015, Pages 35-41

  Gompf, Heinrich S ^a   Fuller, Patrick M ^a   Hattar, Samer ^b,c   Saper, Clifford B ^a   Lu, Jun ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

light entrainment; masking; melanopsin; retina; suprachiasmatic nucleus (SCN); vesicular glutamate transporter 2 (VGLUT2)

Indexed keywords

ANIMALIA; MUS;

GLUTAMIC ACID; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; MELANOPSIN; SCOTOPSIN;

ANIMAL; CHEMISTRY; CIRCADIAN RHYTHM; KNOCKOUT MOUSE; LIGHT; METABOLISM; MOUSE; NERVE CELL; PHYSIOLOGY; RETINA GANGLION CELL; SUPRACHIASMATIC NUCLEUS; SYNAPTIC TRANSMISSION;

ANIMALS; CIRCADIAN RHYTHM; GLUTAMIC ACID; LIGHT; MICE; MICE, KNOCKOUT; NEURONS; PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE; RETINAL GANGLION CELLS; ROD OPSINS; SUPRACHIASMATIC NUCLEUS; SYNAPTIC TRANSMISSION;

EID: 84922342154     PISSN: 07487304     EISSN: 15524531     Source Type: Journal    
DOI: 10.1177/0748730414561545     Document Type: Article

References (28)

1. Abrahamson EE and Moore RY (2001) Suprachiasmatic nucleus in the mouse: retinal innervation, intrinsic organization and efferent projections. Brain Res 916:172-191.
2. Berson DM, Dunn FA, and Takao M (2002) Phototransduction by retinal ganglion cells that set the circadian clock. Science 295:1070-1073.
3. Cahill GM and Menaker M (1989) Effects of excitatory amino acid receptor antagonists and agonists on suprachiasmatic nucleus responses to retinohypothalamic tract volleys. Brain Res 479:76-82.
4. Castel M, Belenky M, Cohen S, Ottersen OP, and Storm-Mathisen J (1993) Glutamate-like immunoreactivity in retinal terminals of the mouse suprachiasmatic nucleus. Eur J Neurosci 5:368-381.
5. Colwell CS and Menaker M (1992) NMDA as well as non-NMDA receptor antagonists can prevent the phaseshifting effects of light on the circadian system of the golden hamster. J Biol Rhythms 7:125-136.
6. de Vries MJ, Nunes Cardozo B, van der Want J, de Wolf A, and Meijer JH (1993) Glutamate immunoreactivity in terminals of the retinohypothalamic tract of the brown Norwegian rat. Brain Res 612:231-237.
7. Delwig A, Majumdar S, Ahern K, LaVail MM, Edwards R, Hnasko TS, and Copenhagen DR (2013) Glutamatergic neurotransmission from melanopsin retinal ganglion cells is required for neonatal photoaversion but not adult pupillary light reflex. PLoS One 8:e83974.
8. Ecker JL, Dumitrescu ON, Wong KY, Alam NM, Chen SK, LeGates T, Renna J, Prusky GT, Berson DM, and Hattar S (2010) Melanopsin-expressing retinal ganglion-cell photoreceptors: cellular diversity and role in pattern vision. Neuron 67:49-60.
9. Fujiyama F, Hioki H, Tomioka R, Taki K, Tamamaki N, Nomura S, Okamoto K, and Kaneko T (2003) Changes of immunocytochemical localization of vesicular glutamate transporters in the rat visual system after the retinofugal denervation. J Comp Neurol 465:234-249.
10. Fyk-Kolodziej B, Dzhagaryan A, Qin P, and Pourcho RG (2004) Immunocytochemical localization of three vesicular glutamate transporters in the cat retina. J Comp Neurol 475:518-530.
11. Gooley JJ, Lu J, Chou TC, Scammell TE, and Saper CB (2001) Melanopsin in cells of origin of the retinohypothalamic tract. Nat Neurosci 4:1165.
12. Guillery RW (2002) On counting and counting errors. J Comp Neurol 447:1-7.
13. Guler AD, Ecker JL, Lall GS, Haq S, Altimus CM, Liao HW, Barnard AR, Cahil H, Badea TC, Zhao H, Hankins MW, et al. (2008) Melanopsin cells are the principal conduits for rod-cone input to non-image-forming vision. Nature 453:102-105.
14. Hannibal J, Hindersson P, Knudsen SM, Georg B, and Fahrenkrug J (2002) The photopigment melanopsin is exclusively present in pituitary adenylate cyclase-activating polypeptide-containing retinal ganglion cells of the retinohypothalamic tract. J Neurosci 22:RC191.
15. Hattar S, Liao HW, Takao M, Berson DM, and Yau KW (2002) Melanopsin-containing retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. Science 295:1065-1070.
16. Johnson J, Fremeau RT Jr, Duncan JL, Renteria RC, Yang H, Hua Z, Liu X, LaVail MM, Edwards RH, and Copenhagen DR (2007) Vesicular glutamate transporter 1 is required for photoreceptor synaptic signaling but not for intrinsic visual functions. J Neurosci 27:7245-7255.
17. Kim YI and Dudek FE (1991) Intracellular electrophysiological study of suprachiasmatic nucleus neurons in rodents: excitatory synaptic mechanisms. J Physiol 444:269-287.
18. Krout KE, Kawano J, Mettenleiter TC, Loewy AD (2002) CNS inputs to the suprachiasmatic nucleus of the rat. Neurosci 110:73-92.
19. Moffett J.R, Williamson L, Palkovits M, and Namboodiri M.A (1990) N-acetylaspartylglutamate: a transmitter candidate for the retinohypothalamic tract. Proc Natl Acad Sci USA 87:8065-8069.
20. Moore R., Speh JC, and Card JP (1995) The retinohypothalamic tract originates from a distinct subset of retinal ganglion cells. J Comp Neurol 352:351-366.
21. Morin LP and Allen CN (2006) The circadian visual system, 2005. Brain Res Rev 51:1-60.
22. Ohi K, Takashima M, Nishikawa T, and Takahashi K (1991) N-methyl-D-aspartate receptor participates in neuronal transmission of photic information through the retinohypothalamic tract. Neuroendocrinology 53:344-348.
23. Pickard GE, Smeraski CA, Tomlinson CC, Banfield BW, Kaufman J, Wilcox CL, Enquist LW, and Sollars PJ (2002) Intravitreal injection of the attenuated pseudorabies virus PRV Bartha results in infection of the hamster suprachiasmatic nucleus only by retrograde transsynaptic transport via autonomic circuits. J Neurosci 22:2701-2710.
24. Purrier N, Engeland WC, and Kofuji P (2014) Mice deficient of glutamatergic signaling from intrinsically photosensitive retinal ganglion cells exhibit abnormal circadian photoentrainment. PLoS One 9:e111449.
25. Shibata S, Watanabe A, Hamada T, Ono M, and Watanabe S (1994) N-methyl-D-aspartate induces phase shifts in circadian rhythm of neuronal activity of rat SCN in vitro. Am J Physiol 267:R360-364.
26. Tong Q, Ye C, McCrimmon RJ, Dhillon H, Choi B, Kramer MD, Yu J, Yang Z, Christiansen LM, Lee CE, et al. (2007) Synaptic glutamate release by ventromedial hypothalamic neurons is part of the neurocircuitry that prevents hypoglycemia. Cell Metab 5:383-393.
27. van den Pol AN (1991) Glutamate and aspartate immunoreactivity in hypothalamic presynaptic axons. J Neurosci 11:2087-2101.
28. Wassle H, Regus-Leidig H, and Haverkamp S (2006) Expression of the vesicular glutamate transporter vGluT2 in a subset of cones of the mouse retina. J Comp Neurol 496:544-555.