Temporal patterns of light-induced immediate-early gene expression in the suprachiasmatic nucleus

Exposing an animal to light during the normal dark period of its daily cycle induces shifts in the animal's circadian rhythm of activity. These shifts are preceded by an increase in the expression of an array of immediate early genes in the suprachiasmatic nucleus, the location of the primary circadian clock in the brain. For most of these genes, little is known about the physiological significance of their expression in the SCN. In order to characterize the expression of these genes, laser capture microscopy, and real-time PCR were used to measure the time course of expression of immediate-early genes in the SCN after a 30-min light pulse during the early portion of the night. Most of the measured genes show peak expression shortly after the end of the stimulus and then decline back to baseline after 2h. However, a few genes, including Rrad, Egr3, and Jun, show a more sustained elevation in expression. Analysis of the function of light-induced genes in other cellular systems suggests a possible role for these genes in reducing the SCN to subsequent photic stimuli and in protecting the SCN from excitotoxicity.

[1]  M. Ciotti,et al.  Dual Control of Neurogenesis by PC3 through Cell Cycle Inhibition and Induction of Math1 , 2004, The Journal of Neuroscience.

[2]  Lin Chen,et al.  Structure, mapping, and expression of erp, a growth factor-inducible gene encoding a nontransmembrane protein tyrosine phosphatase, and effect of ERP on cell growth , 1993, Molecular and cellular biology.

[3]  C. Kahn,et al.  Rad and Rad-related GTPases Interact with Calmodulin and Calmodulin-dependent Protein Kinase II* , 1997, The Journal of Biological Chemistry.

[4]  Brigitte Schulz-Klaus.  Neurotoxic lesion of the rostral perirhinal cortex blocks stress-induced exploratory behavioral changes in male rats , 2009, Stress.

[5]  M. Levine,et al.  Glutamate receptor-induced toxicity in neostriatal cells , 1996, Brain Research.

[6]  A. Puisieux,et al.  BTG2TIS21/PC3 induces neuronal differentiation and prevents apoptosis of terminally differentiated PC12 cells , 2002, Oncogene.

[7]  S. Keyse,et al.  Protein phosphatases and the regulation of mitogen-activated protein kinase signalling. , 2000, Current opinion in cell biology.

[8]  R. Schwarcz,et al.  Dopamine receptor activation reveals a novel, kynurenate-sensitive component of striatal N-methyl-d-aspartate neurotoxicity , 2007, Neuroscience.

[9]  K. Tsuneyama,et al.  Proto‐oncogene, Pim‐3 with serine/threonine kinase activity, is aberrantly expressed in human colon cancer cells and can prevent Bad‐mediated apoptosis , 2007, Cancer science.

[10]  E. Challet,et al.  Minireview: Entrainment of the suprachiasmatic clockwork in diurnal and nocturnal mammals. , 2007, Endocrinology.

[11]  K. Kaestner,et al.  Krüppel-like factor 4 exhibits antiapoptotic activity following gamma-radiation-induced DNA damage. , 2007, Oncogene.

[12]  A. B. Reddy,et al.  Genetic and molecular analysis of the central and peripheral circadian clockwork of mice. , 2007, Cold Spring Harbor symposia on quantitative biology.

[13]  D. Welsh,et al.  Exploring spatiotemporal organization of SCN circuits. , 2007, Cold Spring Harbor symposia on quantitative biology.

[14]  D. Andres,et al.  Regulation of voltage-gated calcium channel activity by the Rem and Rad GTPases , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[15]  C. Allen,et al.  Calcium Response to Retinohypothalamic Tract Synaptic Transmission in Suprachiasmatic Nucleus Neurons , 2007, The Journal of Neuroscience.

[16]  Gregor Eichele,et al.  A Differential Response of Two Putative Mammalian Circadian Regulators, mper1 and mper2, to Light , 1997, Cell.

[17]  K. Obrietan,et al.  PACAP potentiates L-type calcium channel conductance in suprachiasmatic nucleus neurons by activating the MAPK pathway. , 2002, Journal of neurophysiology.

[18]  P. Sassone-Corsi,et al.  Light-Inducible and Clock-Controlled Expression of MAP Kinase Phosphatase 1 in Mouse Central Pacemaker Neurons , 2007, Journal of biological rhythms.

[19]  C. Grimm,et al.  Light-induced cell death of retinal photoreceptors in the absence of p53. , 1998, Investigative ophthalmology & visual science.

[20]  K. Kaestner,et al.  Krüppel-like factor 4 exhibits antiapoptotic activity following γ-radiation-induced DNA damage , 2007, Oncogene.

[21]  Greg Q. Butcher,et al.  The p42/44 Mitogen-activated Protein Kinase Pathway Couples Photic Input to Circadian Clock Entrainment* , 2002, The Journal of Biological Chemistry.

[22]  Greg Q. Butcher,et al.  The ERK/MAP kinase pathway couples light to immediate‐early gene expression in the suprachiasmatic nucleus , 2003, The European journal of neuroscience.

[23]  Rae Silver,et al.  Orchestrating time: arrangements of the brain circadian clock , 2005, Trends in Neurosciences.

[24]  N. Billestrup,et al.  Growth arrest- and DNA-damage-inducible 45β gene inhibits c-Jun N-terminal kinase and extracellular signal-regulated kinase and decreases IL-1β-induced apoptosis in insulin-producing INS-1E cells , 2006, Diabetologia.

[25]  C. Marvel,et al.  Activation of NMDA Receptors in the Suprachiasmatic Nucleus Produces Light-Like Phase Shifts of the Circadian Clock In Vivo , 1999, The Journal of Neuroscience.

[26]  Glaucoma in the brain: a piece of the puzzle. , 2006, Canadian journal of ophthalmology. Journal canadien d'ophtalmologie.

[27]  Hiroshi Ishikura,et al.  Pim-3, a proto-oncogene with serine/threonine kinase activity, is aberrantly expressed in human pancreatic cancer and phosphorylates bad to block bad-mediated apoptosis in human pancreatic cancer cell lines. , 2006, Cancer research.

[28]  M. Gillette,et al.  Response Element-binding Protein ( CREB )-dependent Activation of Per 1 Is Required for Light-induced Signaling in the Suprachiasmatic Nucleus Circadian Clock , 2002 .

[29]  I. Lim,et al.  TIS21/BTG2/PC3 as a link between ageing and cancer: cell cycle regulator and endogenous cell death molecule , 2006, Journal of Cancer Research and Clinical Oncology.

[30]  Mark J. Zylka,et al.  Two period Homologs: Circadian Expression and Photic Regulation in the Suprachiasmatic Nuclei , 1997, Neuron.

[31]  W. Huttner,et al.  Expression of the antiproliferative gene TIS21 at the onset of neurogenesis identifies single neuroepithelial cells that switch from proliferative to neuron-generating division. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[32]  Erik D Herzog,et al.  Clock Genes, Oscillators, and Cellular Networks in the Suprachiasmatic Nuclei , 2004, Journal of biological rhythms.

[33]  Serge Daan,et al.  A functional analysis of circadian pacemakers in nocturnal rodents , 1976, Journal of comparative physiology.

[34]  D. Guardavaccaro,et al.  PC3 potentiates NGF-induced differentiation and protects neurons from apoptosis , 2002, Neuroreport.

[35]  M. Camps,et al.  Dual specificity phosphatases: a gene family for control of MAP kinase function , 2000, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[36]  D. Storm,et al.  Light and circadian rhythmicity regulate MAP kinase activation in the suprachiasmatic nuclei , 1998, Nature Neuroscience.

[37]  J. Kornhauser,et al.  Regulation of jun-B messenger RNA and AP-1 activity by light and a circadian clock. , 1992, Science.

[38]  Jun Lu,et al.  The hypothalamic integrator for circadian rhythms , 2005, Trends in Neurosciences.

[39]  Yuichiro Yamada,et al.  Nuclear sequestration of beta-subunits by Rad and Rem is controlled by 14-3-3 and calmodulin and reveals a novel mechanism for Ca2+ channel regulation. , 2006, Journal of molecular biology.

[40]  Thomas D. Schmittgen,et al.  Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. , 2001, Methods.

[41]  D. Peeper,et al.  KLF4, p21 and context-dependent opposing forces in cancer , 2006, Nature Reviews Cancer.

[42]  Hong Sun,et al.  MKP-1 (3CH134), an immediate early gene product, is a dual specificity phosphatase that dephosphorylates MAP kinase in vivo , 1993, Cell.

[43]  F. Ebling.  The role of glutamate in the photic regulation of the suprachiasmatic nucleus , 1996, Progress in Neurobiology.

[44]  Helen Piontkivska,et al.  Identification of novel light-induced genes in the suprachiasmatic nucleus , 2007, BMC Neuroscience.