A Circadian Genomic Signature Common to Ketamine and Sleep Deprivation in the Anterior Cingulate Cortex

Biological Psychiatry

Volumn 82, Issue 5, 2017, Pages 351-360

  Orozco Solis, Ricardo ^a   Montellier, Emilie ^a   Aguilar Arnal, Lorena ^a   Sato, Shogo ^a   Vawter, Marquis P ^a   Bunney, Blynn G ^a   Bunney, William E ^a   Sassone Corsi, Paolo ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Anterior cingulate cortex; Circadian clock; Depression; Ketamine; Sleep deprivation; Transcriptome

Indexed keywords

CIART PROTEIN; COMPLEMENTARY DNA; DBP PROTEIN; KETAMINE; NPAS4 PROTEIN; PER2 PROTEIN; PROTEIN; RETINOID RELATED ORPHAN RECEPTOR BETA; SODIUM CHLORIDE; TRANSCRIPTOME; UNCLASSIFIED DRUG; ANTIDEPRESSANT AGENT; CIRCADIAN RHYTHM SIGNALING PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTERIOR CINGULATE; ANTIDEPRESSANT ACTIVITY; ARTICLE; BEHAVIOR CHANGE; CIRCADIAN RHYTHM; COMPARATIVE STUDY; CONTROLLED STUDY; DOWN REGULATION; FORCED SWIM TEST; GENE EXPRESSION; GENE IDENTIFICATION; GENOME ANALYSIS; MAJOR DEPRESSION; MALE; MICROARRAY ANALYSIS; MOLECULAR CLOCK; MOUSE; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SLEEP DEPRIVATION; TRANSCRIPTOMICS; ANIMAL; BIOLOGY; C57BL MOUSE; CINGULATE GYRUS; DEPRESSION; DISEASE MODEL; DRUG EFFECT; METABOLISM; PHYSIOLOGY;

ANIMALS; ANTIDEPRESSIVE AGENTS; CIRCADIAN RHYTHM SIGNALING PEPTIDES AND PROTEINS; COMPUTATIONAL BIOLOGY; DEPRESSIVE DISORDER; DISEASE MODELS, ANIMAL; GENE EXPRESSION; GYRUS CINGULI; KETAMINE; MALE; MICE, INBRED C57BL; MICROARRAY ANALYSIS; SLEEP DEPRIVATION; TRANSCRIPTOME;

EID: 85017114504     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2017.02.1176     Document Type: Article

References (82)

1. NIMH, Major depression among adults, 2014 http://www.nimh.nih.gov/health/statistics/prevalence/major-depression-among-adults.shtml Accessed September 18, 2016.
2. Berman, R.M., Cappiello, A., Anand, A., Oren, D.A., Heninger, G.R., Charney, D.S., Krystal, J.H., Antidepressant effects of ketamine in depressed patients. Biol Psychiatry 47 (2000), 351–354.
3. Bunney, B.G., Bunney, W.E., Rapid-acting antidepressant strategies: mechanisms of action. Int J Neuropsychopharmacol 15 (2012), 695–713.
4. DiazGranados, N., Ibrahim, L.A., Brutsche, N.E., Ameli, R., Henter, I.D., Luckenbaugh, D.A., et al. Rapid resolution of suicidal ideation after a single infusion of an N-methyl-D-aspartate antagonist in patients with treatment-resistant major depressive disorder. J Clin Psychiatry 71 (2010), 1605–1611.
5. Larkin, G.L., Beautrais, A.L., A preliminary naturalistic study of low-dose ketamine for depression and suicide ideation in the emergency department. Int J Neuropsychopharmacol 14 (2011), 1127–1131.
6. Price, R.B., Nock, M.K., Charney, D.S., Mathew, S.J., Effects of intravenous ketamine on explicit and implicit measures of suicidality in treatment-resistant depression. Biol Psychiatry 66 (2009), 522–526.
7. Murrough, J.W., Soleimani, L., DeWilde, K.E., Collins, K.A., Lapidus, K.A., Iacoviello, B.M., et al. Ketamine for rapid reduction of suicidal ideation: A randomized controlled trial. Psychol Med 45 (2015), 3571–3580.
8. Zarate, C.A. Jr., Brutsche, N.E., Ibrahim, L., Franco-Chaves, J., Diazgranados, N., Cravchik, A., et al. Replication of ketamine׳s antidepressant efficacy in bipolar depression: A randomized controlled add-on trial. Biol Psychiatry 71 (2012), 939–946.
9. Price, R.B., Iosifescu, D.V., Murrough, J.W., Chang, L.C., Al Jurdi, R.K., Iqbal, S.Z., et al. Effects of ketamine on explicit and implicit suicidal cognition: A randomized controlled trial in treatment-resistant depression. Depress Anxiety 31 (2014), 335–343.
10. Dallaspezia, S., Suzuki, M., Benedetti, F., Chronobiological therapy for mood disorders. Curr Psychiatry Rep, 17, 2015, 95.
11. Masri, S., Sassone-Corsi, P., The circadian clock: A framework linking metabolism, epigenetics and neuronal function. Nat Rev Neurosci 14 (2013), 69–75.
12. Bunney, B.G., Li, J.Z., Walsh, D.M., Stein, R., Vawter, M.P., Cartagena, P., et al. Circadian dysregulation of clock genes: Clues to rapid treatments in major depressive disorder. Mol Psychiatry 20 (2015), 48–55.
13. Hasler, B.P., Buysse, D.J., Kupfer, D.J., Germain, A., Phase relationships between core body temperature, melatonin, and sleep are associated with depression severity: Further evidence for circadian misalignment in non-seasonal depression. Psychiatry Res 178 (2010), 205–207.
14. Troxel, W.M., Kupfer, D.J., Reynolds, C.F. 3rd, Frank, E., Thase, M.E., Miewald, J.M., et al. Insomnia and objectively measured sleep disturbances predict treatment outcome in depressed patients treated with psychotherapy or psychotherapy-pharmacotherapy combinations. J Clin Psychiatry 73 (2012), 478–485.
15. Avery, D.H., Shah, S.H., Eder, D.N., Wildschiodtz, G., Nocturnal sweating and temperature in depression. Acta Psychiatr Scand 100 (1999), 295–301.
16. Souetre, E., Salvati, E., Wehr, T.A., Sack, D.A., Krebs, B., Darcourt, G., Twenty-four-hour profiles of body temperature and plasma TSH in bipolar patients during depression and during remission and in normal control subjects. Am J Psychiatry 145 (1988), 1133–1137.
17. Bunney, B.G., Bunney, W.E., Mechanisms of rapid antidepressant effects of sleep deprivation therapy: Clock genes and circadian rhythms. Biol Psychiatry 73 (2013), 1164–1171.
18. Bunney, W.E., Bunney, B.G., Molecular clock genes in man and lower animals: Possible implications for circadian abnormalities in depression. Neuropsychopharmacology 22 (2000), 335–345.
19. Wu, J.C., Kelsoe, J.R., Schachat, C., Bunney, B.G., DeModena, A., Golshan, S., et al. Rapid and sustained antidepressant response with sleep deprivation and chronotherapy in bipolar disorder. Biol Psychiatry 66 (2009), 298–301.
20. Wisor, J.P., O׳Hara, B.F., Terao, A., Selby, C.P., Kilduff, T.S., Sancar, A., et al. A role for cryptochromes in sleep regulation. BMC Neurosci, 3, 2002, 20.
21. Wisor, J.P., Pasumarthi, R.K., Gerashchenko, D., Thompson, C.L., Pathak, S., Sancar, A., et al. Sleep deprivation effects on circadian clock gene expression in the cerebral cortex parallel electroencephalographic differences among mouse strains. J Neurosci 28 (2008), 7193–7201.
22. Thompson, C.L., Wisor, J.P., Lee, C.K., Pathak, S.D., Gerashchenko, D., Smith, K.A., et al. Molecular and anatomical signatures of sleep deprivation in the mouse brain. Front Neurosci, 4, 2010, 165.
23. Balsalobre, A., Damiola, F., Schibler, U., A serum shock induces circadian gene expression in mammalian tissue culture cells. Cell 93 (1998), 929–937.
24. Maret, S., Dorsaz, S., Gurcel, L., Pradervand, S., Petit, B., Pfister, C., et al. Homer1a is a core brain molecular correlate of sleep loss. Proc Natl Acad Sci U S A 104 (2007), 20090–20095.
25. Bellet, M.M., Vawter, M.P., Bunney, B.G., Bunney, W.E., Sassone-Corsi, P., Ketamine influences CLOCK:BMAL1 function leading to altered circadian gene expression. PLoS One, 6, 2011, e23982.
26. Li, J.Z., Bunney, B.G., Meng, F., Hagenauer, M.H., Walsh, D.M., Vawter, M.P., et al. Circadian patterns of gene expression in the human brain and disruption in major depressive disorder. Proc Natl Acad Sci U S A 110 (2013), 9950–9955.
27. Drevets, W.C., Savitz, J., Trimble, M., The subgenual anterior cingulate cortex in mood disorders. CNS Spectr 13 (2008), 663–681.
28. Salvadore, G., Cornwell, B.R., Colon-Rosario, V., Coppola, R., Grillon, C., Zarate, C.A. Jr., Manji, H.K., Increased anterior cingulate cortical activity in response to fearful faces: A neurophysiological biomarker that predicts rapid antidepressant response to ketamine. Biol Psychiatry 65 (2009), 289–295.
29. Mulert, C., Juckel, G., Brunnmeier, M., Karch, S., Leicht, G., Mergl, R., et al. Prediction of treatment response in major depression: Integration of concepts. J Affect Disord 98 (2007), 215–225.
30. Hines, D.J., Schmitt, L.I., Hines, R.M., Moss, S.J., Haydon, P.G., Antidepressant effects of sleep deprivation require astrocyte-dependent adenosine mediated signaling. Transl Psychiatry, 3, 2013, e212.
31. Can, A., Dao, D.T., Arad, M., Terrillion, C.E., Piantadosi, S.C., Gould, T.D., The mouse forced swim test. J Vis Exp, 59, 2012, e3638.
32. Orozco-Solis, R., Ramadori, G., Coppari, R., Sassone-Corsi, P., SIRT1 relays nutritional inputs to the circadian clock through the Sf1 neurons of the ventromedial hypothalamus. Endocrinology 156 (2015), 2174–2184.
33. Surget, A., Wang, Y., Leman, S., Ibarguen-Vargas, Y., Edgar, N., Griebel, G., et al. Corticolimbic transcriptome changes are state-dependent and region-specific in a rodent model of depression and of antidepressant reversal. Neuropsychopharmacology 34 (2008), 1363–1380.
34. Berton, O., McClung, C.A., Dileone, R.J., Krishnan, V., Renthal, W., Russo, S.J., et al. Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 311 (2006), 864–868.
35. Eisen, M.B., Spellman, P.T., Brown, P.O., Botstein, D., Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95 (1998), 14863–14868.
36. Tabas-Madrid, D., Nogales-Cadenas, R., Pascual-Montano, A., GeneCodis3: A non-redundant and modular enrichment analysis tool for functional genomics. Nucleic Acids Res 40 (2012), W478–W483.
37. Lopez-Rodriguez, F., Kim, J., Poland, R.E., Total sleep deprivation decreases immobility in the forced-swim test. Neuropsychopharmacology 29 (2004), 1105–1111.
38. Scheuing, L., Chiu, C.T., Liao, H.M., Chuang, D.M., Antidepressant mechanism of ketamine: Perspective from preclinical studies. Front Neurosci, 9, 2015, 249.
39. Autry, A.E., Adachi, M., Nosyreva, E., Na, E.S., Los, M.F., Cheng, P.F., et al. NMDA receptor blockade at rest triggers rapid behavioural antidepressant responses. Nature 475 (2011), 91–95.
40. Fillinger, C., Yalcin, I., Barrot, M., Veinante, P., Afferents to anterior cingulate areas 24a and 24b and midcingulate areas 24a׳ and 24b׳ in the mouse. Brain Struct Funct 222 (2017), 1509–1532.
41. Annayev, Y., Adar, S., Chiou, Y.Y., Lieb, J.D., Sancar, A., Ye, R., Gene model 129 (Gm129) encodes a novel transcriptional repressor that modulates circadian gene expression. J Biol Chem 289 (2014), 5013–5024.
42. Goriki, A., Hatanaka, F., Myung, J., Kim, J.K., Yoritaka, T., Tanoue, S., et al. A novel protein, CHRONO, functions as a core component of the mammalian circadian clock. PLoS Biol, 12, 2014, e1001839.
43. Petryszak, R., Keays, M., Tang, Y.A., Fonseca, N.A., Barrera, E., Burdett, T., et al. Expression Atlas update—An integrated database of gene and protein expression in humans, animals and plants. Nucleic Acids Res 44 (2016), D746–D752.
44. Orozco-Solis, R., Sassone-Corsi, P., Epigenetic control and the circadian clock: Linking metabolism to neuronal responses. Neuroscience 264 (2014), 76–87.
45. Janich, P., Pascual, G., Merlos-Suárez, A., Batlle, E., Ripperger, J., Albrecht, U., et al. The circadian molecular clock creates epidermal stem cell heterogeneity. Nature 480 (2011), 209–214.
46. Karpowicz, P., Zhang, Y., Hogenesch, J.B., Emery, P., Perrimon, N., The circadian clock gates the intestinal stem cell regenerative state. Cell Reports 3 (2013), 996–1004.
47. Akashi, M., Nishida, E., Involvement of the MAP kinase cascade in resetting of the mammalian circadian clock. Genes Dev 14 (2000), 645–649.
48. Gerstner, J.R., Yin, J.C.P., Circadian rhythms and memory formation. Nat Rev Neurosci 11 (2010), 577–588.
49. Ficek, J., Zygmunt, M., Piechota, M., Hoinkis, D., Rodriguez, Parkitna J., Przewlocki, R., Korostynski, M., Molecular profile of dissociative drug ketamine in relation to its rapid antidepressant action. BMC Genomics, 17, 2016, 362.
50. Mongrain, V., La Spada, F., Curie, T., Franken, P., Sleep loss reduces the DNA-binding of BMAL1, CLOCK, and NPAS2 to specific clock genes in the mouse cerebral cortex. PLoS One, 6, 2011, e26622.
51. Curie, T., Mongrain, V., Dorsaz, S., Mang, G.M., Emmenegger, Y., Franken, P., Homeostatic and circadian contribution to EEG and molecular state variables of sleep regulation. Sleep 36 (2013), 311–323.
52. Garcia, L.S., Comim, C.M., Valvassori, S.S., Reus, G.Z., Barbosa, L.M., Andreazza, A.C., et al. Acute administration of ketamine induces antidepressant-like effects in the forced swimming test and increases BDNF levels in the rat hippocampus. Prog Neuropsychopharmacol Biol Psychiatry 32 (2008), 140–144.
53. Weckmann, K., Labermaier, C., Asara, J.M., Muller, M.B., Turck, C.W., Time-dependent metabolomic profiling of Ketamine drug action reveals hippocampal pathway alterations and biomarker candidates. Transl Psychiatry, 4, 2014, e481.
54. Gene Ontology Consortium. Gene Ontology Consortium: Going forward. Nucleic Acids Res 43 (2015), D1049–D1056.
55. Kanehisa, M., Sato, Y., Kawashima, M., Furumichi, M., Tanabe, M., KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res 44 (2016), D457–D462.
56. Abdallah, C.G., Adams, T.G., Kelmendi, B., Esterlis, I., Sanacora, G., Krystal, J.H., Ketamine׳s mechanism of action: A path to rapid-acting antidepressants. Depress Anxiety 33 (2016), 689–697.
57. Beurel, E., Song, L., Jope, R.S., Inhibition of glycogen synthase kinase-3 is necessary for the rapid antidepressant effect of ketamine in mice. Mol Psychiatry 16 (2011), 1068–1070.
58. Liu, R.J., Fuchikami, M., Dwyer, J.M., Lepack, A.E., Duman, R.S., Aghajanian, G.K., GSK-3 inhibition potentiates the synaptogenic and antidepressant-like effects of subthreshold doses of ketamine. Neuropsychopharmacology 38 (2013), 2268–2277.
59. Mathews, D.C., Zarate, C.A. Jr., Current status of ketamine and related compounds for depression. J Clin Psychiatry 74 (2013), 516–517.
60. Kavalali, E.T., Monteggia, L.M., Synaptic mechanisms underlying rapid antidepressant action of ketamine. Am J Psychiatry 169 (2012), 1150–1156.
61. Antle, M.C., Tse, F., Koke, S.J., Sterniczuk, R., Hagel, K., Non-photic phase shifting of the circadian clock: Role of the extracellular signal-responsive kinases I/II/mitogen-activated protein kinase pathway. Eur J Neurosci 28 (2008), 2511–2518.
62. Duman, C.H., Schlesinger, L., Kodama, M., Russell, D.S., Duman, R.S., A role for MAP kinase signaling in behavioral models of depression and antidepressant treatment. Biol Psychiatry 61 (2007), 661–670.
63. Reus, G.Z., Vieira, F.G., Abelaira, H.M., Michels, M., Tomaz, D.B., dos Santos, M.A., et al. MAPK signaling correlates with the antidepressant effects of ketamine. J Psychiatr Res 55 (2014), 15–21.
64. Thomas, G.M., Huganir, R.L., MAPK cascade signalling and synaptic plasticity. Nat Rev Neurosci 5 (2004), 173–183.
65. Nilsson, E.K., Bostrom, A.E., Mwinyi, J., Schioth, H.B., Epigenomics of total acute sleep deprivation in relation to genome-wide DNA methylation profiles and RNA expression. OMICS 20 (2016), 334–342.
66. Cedernaes, J., Osler, M.E., Voisin, S., Broman, J.E., Vogel, H., Dickson, S.L., et al. Acute sleep loss induces tissue-specific epigenetic and transcriptional alterations to circadian clock genes in men. J Clin Endocrinol Metab 100 (2015), E1255–E1261.
67. Yoon, K., Gaiano, N., Notch signaling in the mammalian central nervous system: Insights from mouse mutants. Nat Neurosci 8 (2005), 709–715.
68. Chiba, S., Notch signaling in stem cell systems. Stem Cells 24 (2006), 2437–2447.
69. Ables, J.L., Breunig, J.J., Eisch, A.J., Rakic, P., Not(ch) just development: Notch signalling in the adult brain. Nat Rev Neurosci 12 (2011), 269–283.
70. Alberi, L., Liu, S., Wang, Y., Badie, R., Smith-Hicks, C., Wu, J., et al. Activity-induced Notch signaling in neurons requires Arc/Arg3.1 and is essential for synaptic plasticity in hippocampal networks. Neuron 69 (2011), 437–444.
71. Bagot, R.C., Cates, H.M., Purushothaman, I., Vialou, V., Heller, E.A., Yieh, L., et al. Ketamine and imipramine reverse transcriptional signatures of susceptibility and induce resilience-specific gene expression profiles. Biol Psychiatry 81 (2017), 285–295.
72. Papadopoulou, A., Siamatras, T., Delgado-Morales, R., Amin, N.D., Shukla, V., Zheng, Y.L., et al. Acute and chronic stress differentially regulate cyclin-dependent kinase 5 in mouse brain: Implications to glucocorticoid actions and major depression. Transl Psychiatry, 5, 2015, e578.
73. Duman, R.S., Aghajanian, G.K., Synaptic dysfunction in depression: Potential therapeutic targets. Science 338 (2012), 68–72.
74. Mei, L., Xiong, W.C., Neuregulin 1 in neural development, synaptic plasticity and schizophrenia. Nat Rev Neurosci 9 (2008), 437–452.
75. Karatsoreos, I.N., Bhagat, S., Bloss, E.B., Morrison, J.H., McEwen, B.S., Disruption of circadian clocks has ramifications for metabolism, brain, and behavior. Proc Natl Acad Sci U S A 108 (2011), 1657–1662.
76. Maret, S., Faraguna, U., Nelson, A.B., Cirelli, C., Tononi, G., Sleep and waking modulate spine turnover in the adolescent mouse cortex. Nat Neurosci 14 (2011), 1418–1420.
77. Mineur, Y.S., Obayemi, A., Wigestrand, M.B., Fote, G.M., Calarco, C.A., Li, A.M., Picciotto, M.R., Cholinergic signaling in the hippocampus regulates social stress resilience and anxiety- and depression-like behavior. Proc Natl Acad Sci U S A 110 (2013), 3573–3578.
78. Berger, M., Riemann, D., Höchli, D., Spiegel, R., The cholinergic rapid eye movement sleep induction test with rs-86: State or trait marker of depression?. Arch Gen Psychiatry 46 (1989), 421–428.
79. Benedetti, F., Dallaspezia, S., Lorenzi, C., Pirovano, A., Radaelli, D., Locatelli, C., et al. Gene-gene interaction of glycogen synthase kinase 3-β and serotonin transporter on human antidepressant response to sleep deprivation. J Affect Disord 136 (2012), 514–519.
80. Ressler, K.J., Mayberg, H.S., Targeting abnormal neural circuits in mood and anxiety disorders: From the laboratory to the clinic. Nat Neurosci 10 (2007), 1116–1124.
81. Nestler, E.J., Hyman, S.E., Animal models of neuropsychiatric disorders. Nat Neurosci 13 (2010), 1161–1169.
82. Serchov, T., Clement, H.W., Schwarz, M.K., Iasevoli, F., Tosh, D.K., Idzko, M., et al. Increased signaling via adenosine A1 receptors, sleep deprivation, imipramine, and ketamine inhibit depressive-like behavior via induction of Homer1a. Neuron 87 (2015), 549–562.