Neurons identified by NeuN/Fox-3 immunoreactivity have a novel distribution in the hamster and mouse suprachiasmatic nucleus

Brain Research

Volumn 1421, Issue , 2011, Pages 44-51

  Morin, Lawrence P ^a,b   Hefton, Sara ^c   Studholme, Keith M ^a  

^a STONY BROOK UNIVERSITY MEDICAL CENTER   (United States)

^b Graduate Program in Neuroscience   (United States)

^c STONY BROOK UNIVERSITY   (United States)

Author keywords

Anatomy; Circadian; Hamster; Mouse; SCN

Indexed keywords

CHOLECYSTOKININ; MONOCLONAL ANTIBODY; NEURON SPECIFIC NUCLEAR PROTEIN; VASOACTIVE INTESTINAL POLYPEPTIDE; VASOPRESSIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CELLULAR DISTRIBUTION; HAMSTER; IMMUNOREACTIVITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; SUPRACHIASMATIC NUCLEUS; VENTROMEDIAL PREFRONTAL CORTEX;

ANIMALS; CRICETINAE; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED C57BL; NERVE TISSUE PROTEINS; NEURONS; NUCLEAR PROTEINS; SUPRACHIASMATIC NUCLEUS;

CRICETINAE;

EID: 80054975060     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2011.09.015     Document Type: Article

References (59)

1. E.E. Abrahamson, and R.Y. Moore Suprachiasmatic nucleus in the mouse: retinal innervation, intrinsic organization and efferent projections Brain Res. 916 2001 172 191 (Pubitemid 32971919)
2. M.C. Antle, L.J. Kriegsfeld, and R. Silver Signaling within the master clock of the brain: localized activation of mitogen-activated protein kinase by gastrin-releasing peptide J. Neurosci. 25 2005 2447 2454 (Pubitemid 40365154)
3. M.A. Belenky, C.A. Smeraski, I. Provencio, P.J. Sollars, and G.E. Pickard Melanopsin retinal ganglion cells receive bipolar and amacrine cell synapses J. Comp. Neurol. 460 2003 380 393 (Pubitemid 36514616)
4. G.I. Botchkina, and L.P. Morin Ontogeny of radial glia, astrocytes and vasoactive intestinal peptide immunoreactive neurons in hamster suprachiasmatic nucleus Dev. Brain Res. 86 1995 48 56
5. J.P. Card, and R.Y. Moore The suprachiasmatic nucleus of the golden hamster: immunohistochemical analysis of cell and fiber distribution Neuroscience 13 1984 390 396
6. V.M. Cassone, J.C. Speh, and J.P. Card Comparative anatomy of the mammalian hypothalamic suprachiasmatic nucleus J. Biol. Rhythm. 3 1988 71 91
7. E. Drouyer, C. Rieux, R.A. Hut, and H.M. Cooper Responses of suprachiasmatic nucleus neurons to light and dark adaptation: relative contributions of melanopsin and rod-cone inputs J. Neurosci. 27 2007 9623 9631 (Pubitemid 47492183)
8. K. Edelstein, H.O. De la Iglesia, and N. Mrosovsky Period gene expression in the suprachiasmatic nucleus of behaviorally decoupled hamsters Brain Res. Mol. Brain Res. 114 2003 40 45 (Pubitemid 36627994)
9. A. Gdalyahu, I. Ghosh, T. Levy, T. Sapir, S. Sapoznik, Y. Fishler, D. Azoulai, and O. Reiner DCX, a new mediator of the JNK pathway EMBO J. 23 2004 823 832 (Pubitemid 38418749)
10. D. Geoghegan, and D.A. Carter A novel site of adult doublecortin expression: neuropeptide neurons within the suprachiasmatic nucleus circadian clock BMC Neurosci. 9 2008 2
11. J.D. Glass, M. Watanabe, L. Fedorkova, H. Shen, G. Ungers, and U. Rutishauser Dynamic regulation of polysialylated neural cell adhesion molecule in the suprachiasmatic nucleus Neuroscience 117 2003 203 211 (Pubitemid 36246517)
12. J.J. Gooley, J. Lu, T.C. Chou, T.E. Scammell, and C.B. Saper Melanopsin in cells of origin of the retinohypothalamic tract Nat. Neurosci. 4 2001 1165 (Pubitemid 33135616)
13. T. Hamada, M.C. Antle, and R. Silver Temporal and spatial expression patterns of canonical clock genes and clock-controlled genes in the suprachiasmatic nucleus Eur. J. Neurosci. 19 2004 1741 1748 (Pubitemid 38482562)
14. S. Hattar, M. Kumar, A. Park, P. Tong, J. Tung, K.W. Yau, and D.M. Berson Central projections of melanopsin-expressing retinal ganglion cells in the mouse J. Comp. Neurol. 497 2006 326 349 (Pubitemid 43865789)
15. C.A. Hundahl, J. Hannibal, J. Fahrenkrug, S. Dewilde, and A. Hay-Schmidt Neuroglobin expression in the rat suprachiasmatic nucleus: colocalization, innervation, and response to light J. Comp. Neurol. 518 2010 1556 1569
16. I.N. Karatsoreos, M.P. Butler, J. LeSauter, and R. Silver Androgens modulate structure and function of the suprachiasmatic nucleus brain clock Endocrinology 152 2011 1970 1978
17. K.K. Kim, R.S. Adelstein, and S. Kawamoto Identification of neuronal nuclei (NeuN) as Fox-3, a new member of the Fox-1 gene family of splicing factors J. Biol. Chem. 284 2009 31052 31061
18. K.K. Kim, Y.C. Kim, R.S. Adelstein, and S. Kawamoto Fox-3 and PSF interact to activate neural cell-specific alternative splicing Nucleic Acids Res. 39 2011 3064 3078
19. S.V. Kozlov, J.W. Bogenpohl, M.P. Howell, R. Wevrick, S. Panda, J.B. Hogenesch, L.J. Muglia, R.N. Van Gelder, E.D. Herzog, and C.L. Stewart The imprinted gene Magel2 regulates normal circadian output Nat. Genet. 39 2007 1266 1272 (Pubitemid 47482682)
20. L.J. Kriegsfeld, R.K. Leak, C.B. Yackulic, J. LeSauter, and R. Silver Organization of suprachiasmatic nucleus projections in Syrian hamsters (Mesocricetus auratus): an anterograde and retrograde analysis J. Comp. Neurol. 468 2004 361 379 (Pubitemid 37549656)
21. S.S. Kumar, and P.S. Buckmaster Neuron-specific nuclear antigen NeuN is not detectable in gerbil subtantia nigra pars reticulata Brain Res. 1142 2007 54 60 (Pubitemid 46413186)
22. H.S. Lee, J.L. Nelms, M. Nguyen, R. Silver, and M.N. Lehman The eye is necessary for a circadian rhythm in the suprachiasmatic nucleus Nat. Neurosci. 6 2003 111 112 (Pubitemid 36182776)
23. M.L. Lee, B.E. Swanson, and H.O. De la Iglesia Circadian timing of REM sleep is coupled to an oscillator within the dorsomedial suprachiasmatic nucleus Curr. Biol. 19 2009 848 852
24. J. LeSauter, L.J. Kriegsfeld, J. Hon, and R. Silver Calbindin-D 28K cells selectively contact intra-SCN neurons Neuroscience 111 2002 575 585 (Pubitemid 34521896)
25. D. Lind, S. Franken, J. Kappler, J. Jankowski, and K. Schilling Characterization of the neuronal marker NeuN as a multiply phophorylated antigen with discrete subcellular localization J. Neurosci. Res. 79 2005 295 302 (Pubitemid 40278343)
26. J. Lindley, S. Deurveilher, B. Rusak, and K. Semba Transforming growth factor-alpha and glial fibrillary acidic protein in the hamster circadian system: daily profile and cellular localization Brain Res. 1197 2008 94 105
27. A.C. Liu, D.K. Welsh, C.H. Ko, H.G. Tran, E.E. Zhang, A.A. Priest, E.D. Buhr, O. Singer, K. Meeker, I.M. Verma, F.J. Doyle III, J.S. Takahashi, and S.A. Kay Intercellular coupling confers robustness against mutations in the SCN circadian clock network Cell 129 2007 605 616 (Pubitemid 46660967)
28. E.G. Marchant, and L.P. Morin The hamster circadian rhythm system includes nuclei of the subcortical visual shell J. Neurosci. 19 1999 10482 10493 (Pubitemid 30228054)
29. E.L. Meyer-Bernstein, and L.P. Morin Differential serotonergic innervation of the suprachiasmatic nucleus and the intergeniculate leaflet and its role in circadian rhythm modulation J. Neurosci. 16 1996 2097 2111 (Pubitemid 26144022)
30. J.D. Mikkelsen, P.J. Larsen, M.M.T. O'Hare, and S.J. Wiegand Gastrin releasing peptide in the rat suprachiasmatic nucleus: an immunohistochemical, chromatographic and radioimmunological study Neuroscience 40 1991 55 66
31. R.Y. Moore, J.C. Speh, and R.K. Leak Suprachiasmatic nucleus organization Cell Tissue Res. 309 2002 89 98 (Pubitemid 34744031)
32. C.A. Moores, M. Perderiset, C. Kappeler, S. Kain, D. Drummond, S.J. Perkins, J. Chelly, R. Cross, A. Houdusse, and F. Francis Distinct roles of doublecortin modulating the microtubule cytoskeleton EMBO J. 25 2006 4448 4457 (Pubitemid 44498119)
33. L.P. Morin SCN organization reconsidered J. Biol. Rhythms. 33 2007 3 13 (Pubitemid 46041608)
34. L.P. Morin, and C.N. Allen The circadian visual system, 2005 Brain Res. Rev. 51 2006 1 60 (Pubitemid 44218910)
35. L.P. Morin, and J.H. Blanchard Organization of the hamster paraventricular hypothalamic nucleus J. Comp. Neurol. 332 1993 341 357 (Pubitemid 23163334)
36. L.P. Morin, and J.H. Blanchard Neuromodulator content of hamster intergeniculate leaflet neurons and their projection to the suprachiasmatic nucleus or visual midbrain J. Comp. Neurol. 437 2001 79 90 (Pubitemid 32691495)
37. L.P. Morin, J.H. Blanchard, and R.Y. Moore Intergeniculate leaflet and suprachiasmatic nucleus organization and connections in the hamster Vis. Neurosci. 8 1992 219 230
38. L.P. Morin, J.H. Blanchard, and I. Provencio Retinal ganglion cell projections to the hamster suprachiasmatic nucleus, intergeniculate leaflet and visual midbrain: bifurcation and melanopsin immunoreactivity J. Comp. Neurol. 465 2003 401 416 (Pubitemid 37174204)
39. L.P. Morin, K.Y. Shivers, J.H. Blanchard, and L. Muscat Complex organization of mouse and rat suprachiasmatic nucleus Neuroscience 137 2006 1285 1297 (Pubitemid 43133153)
40. R.J. Mullen, C.R. Buck, and A.M. Smith NeuN, a neuronal specific nuclear protein in vertebrates Development 116 1992 201 211
41. L. Muscat, A.D. Huberman, C.L. Jordan, and L.P. Morin Crossed and uncrossed retinal projections to the hamster circadian system J. Comp. Neurol. 466 2003 513 524 (Pubitemid 37305995)
42. G.M. Peterson, and R.Y. Moore Selective effects of kainic acid on diencephalic neurons Brain Res. 202 1980 165 182 (Pubitemid 10010981)
43. M.R. Ralph, R.G. Foster, F.C. Davis, and M. Menaker Transplanted suprachiasmatic nucleus determines circadian period Science 247 1990 975 978
44. J. Schilling, and F. Nurnberger Dynamic changes in the immunoreactivity of neuropeptide systems of the suprachiasmatic nuclei in golden hamsters during the sleep-wake cycle Cell Tissue Res. 294 1998 233 241 (Pubitemid 28486399)
45. M.D. Schwartz, C. Wotus, T. Liu, W.O. Friesen, J. Borjigin, G.A. Oda, and H.O. De la Iglesia Dissociation of circadian and light inhibition of melatonin release through forced desynchronization in the rat Proc. Natl. Acad. Sci. U. S. A. 106 2009 17540 17545
46. Y. Shigeyoshi, K. Taguchi, S. Yamamoto, S. Takekida, L. Yan, H. Tei, T. Moriya, S. Shibata, J.J. Loros, J.C. Dunlap, and H. Okamura Light-induced resetting of a mammalian circadian clock is associated with rapid induction of the mPer1 transcript Cell 91 1997 1043 1053 (Pubitemid 28027836)
47. R. Silver, J. LeSauter, P.A. Tresco, and M.N. Lehman A diffusible coupling signal from the transplanted suprachiasmatic nucleus controlling circadian locomotor rhythms Nature 382 1996 810 813 (Pubitemid 26299564)
48. R. Silver, M.T. Romero, H.R. Besmer, R.K. Leak, J.M. Nunez, and J. LeSauter Calbindin-D28K cells in the hamster SCN express light-induced Fos Neuroreport 7 1996 1224 1228 (Pubitemid 26230081)
49. R. Silver, A.I. Sookhoo, J. LeSauter, P. Stevens, H.T. Jansen, and M.N. Lehman Multiple regulatory elements result in regional specificity in circadian rhythms of neuropeptide expression in mouse SCN Neuroreport 10 1999 3165 3174 (Pubitemid 29498415)
50. L. Smale, and J. Boverhof The suprachiasmatic nucleus and intergeniculate leaflet of Arvicanthis niloticus, a diurnal murid rodent from East Africa J. Comp. Neurol. 403 1999 190 208
51. L. Smale, J.H. Blanchard, R.Y. Moore, and L.P. Morin Immunocytochemical characterization of the suprachiasmatic nucleus and the intergeniculate leaflet in the diurnal ground squirrel, Spermophilus lateralis Brain Res. 563 1991 77 86
52. M. Tanaka, S. Hayashi, Y. Tamada, T. Ikeda, Y. Hisa, T. Takamatsu, and Y. Ibata Direct retinal projections to GRP neurons in the suprachiasmatic nucleus of the rat Neuroreport 8 1997 2187 2191 (Pubitemid 27319670)
53. I. Unal-Cevik, M. Kilinc, Y. Gursoy-Ozdemir, G. Gurer, and T. Dalkara Loss of NeuN immunoreactivity after cerebral ischemia does not indicate neuronal cell loss: a cautionary note Brain Res. 1015 2004 169 174 (Pubitemid 38829751)
54. A.N. van den Pol, and K.L. Tsujimoto Neurotransmitters of the hypothalamic suprachiasmatic nucleus: immunocytochemical analysis of 25 neuronal antigens Neuroscience 15 1985 1049 1086 (Pubitemid 15226670)
55. T. Watanabe, E. Naito, N. Nakao, H. Tei, T. Yoshimura, and S. Ebihara Bimodal clock gene expression in mouse suprachiasmatic nucleus and peripheral tissues under a 7-hour light and 5-hour dark condition J. Biol. Rhythms 22 2006 58 68 (Pubitemid 46041613)
56. D.K. Welsh, J.S. Takahashi, and S.A. Kay Suprachiasmatic nucleus: cell autonomy and network properties Annu. Rev. Physiol. 72 2010 551 577
57. A. Weyer, and K. Schilling Developmental and cell type-specific expression of the neuronal marker NeuN in the murine cerebellum J. Neurosci. Res. 73 2003 400 409 (Pubitemid 36918103)
58. L. Yan, S. Takekida, Y. Shigeyoshi, and H. Okamura Per1 and Per2 gene expression in the rat suprachiasmatic nucleus: circadian profile and the compartment-specific response to light Neuroscience 94 1999 141 150 (Pubitemid 29457604)
59. L. Yan, R. Silver, and M. Gorman Reorganization of suprachiasmatic nucleus networks under 24-h LDLD conditions J. Biol. Rhythms 25 2010 19 27