Hippocampal Sirtuin 1 Signaling Mediates Depression-like Behavior

Biological Psychiatry

Volumn 80, Issue 11, 2016, Pages 815-826

  Abe Higuchi, Naoko ^a   Uchida, Shusaku ^a,b   Yamagata, Hirotaka ^a,b   Higuchi, Fumihiro ^a,b   Hobara, Teruyuki ^a   Hara, Kumiko ^a   Kobayashi, Ayumi ^a   Watanabe, Yoshifumi ^a  

^a YAMAGUCHI UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Anxiety; Chronic stress; Dendritic atrophy; Depression; Hippocampus; Sirtuin

Indexed keywords

MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; SIRTUIN 1; SMALL INTERFERING RNA; BENZAMIDE DERIVATIVE; ENZYME INHIBITOR; FUSED HETEROCYCLIC RINGS; IMIPRAMINE; NAPHTHOL DERIVATIVE; RESVERATROL; SIRT1 PROTEIN, MOUSE; SIRTINOL; SRT2104; STILBENE DERIVATIVE; TRICYCLIC ANTIDEPRESSANT AGENT;

ADULT; AMYGDALA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIDEPRESSANT ACTIVITY; ARTICLE; BRAIN ATROPHY; CHRONIC STRESS; CONTROLLED STUDY; DENDRITIC SPINE; DENTATE GYRUS; DEPRESSION; GENE OVEREXPRESSION; GENE TRANSFER; HIPPOCAMPUS; INTRACELLULAR SIGNALING; LATENT PERIOD; MALE; MEDIAL PREFRONTAL CORTEX; MOUSE; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS INHIBITION; SOCIAL INTERACTION; WILD TYPE; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; C57BL MOUSE; DENDRITE; DISEASE MODEL; MENTAL STRESS; METABOLISM; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; ANTIDEPRESSIVE AGENTS, TRICYCLIC; BENZAMIDES; DENDRITES; DENTATE GYRUS; DEPRESSION; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; HETEROCYCLIC COMPOUNDS, 2-RING; HIPPOCAMPUS; IMIPRAMINE; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; NAPHTHOLS; SIGNAL TRANSDUCTION; SIRTUIN 1; STILBENES; STRESS, PSYCHOLOGICAL;

EID: 84962587892     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2016.01.009     Document Type: Article

References (80)

1. 1 Krishnan, V, Nestler, EJ, The molecular neurobiology of depression. Nature 455 (2008), 894–902.
2. 2 Duman, RS, Aghajanian, GK, Synaptic dysfunction in depression: Potential therapeutic targets. Science 338 (2012), 68–72.
3. 3 Malykhin, NV, Coupland, NJ, Hippocampal neuroplasticity in major depressive disorder. Neuroscience 309 (2015), 200–213.
4. 4 McEwen, BS, Eiland, L, Hunter, RG, Miller, MM, Stress and anxiety: Structural plasticity and epigenetic regulation as a consequence of stress. Neuropharmacology 62 (2012), 3–12.
5. 5 Price, JL, Drevets, WC, Neurocircuitry of mood disorders. Neuropsychopharmacology 35 (2010), 192–216.
6. 6 Imai, S, Armstrong, CM, Kaeberlein, M, Guarente, L, Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature 403 (2000), 795–800.
7. 7 Brunet, A, Sweeney, LB, Sturgill, JF, Chua, KF, Greer, PL, Lin, Y, et al. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 303 (2004), 2011–2015.
8. 8 Kim, S, Benguria, A, Lai, CY, Jazwinski, SM, Modulation of life-span by histone deacetylase genes in Saccharomyces cerevisiae. Mol Biol Cell 10 (1999), 3125–3136.
9. 9 Landry, J, Sutton, A, Tafrov, ST, Heller, RC, Stebbins, J, Pillus, L, Sternglanz, R, The silencing protein SIR2 and its homologs are NAD-dependent protein deacetylases. Proc Natl Acad Sci U S A 97 (2000), 5807–5811.
10. 10 Smith, JS, Brachmann, CB, Celic, I, Kenna, MA, Muhammad, S, Starai, VJ, et al. A phylogenetically conserved NAD+-dependent protein deacetylase activity in the Sir2 protein family. Proc Natl Acad Sci U S A 97 (2000), 6658–6663.
11. 11 Asher, G, Gatfield, D, Stratmann, M, Reinke, H, Dibner, C, Kreppel, F, et al. SIRT1 regulates circadian clock gene expression through PER2 deacetylation. Cell 134 (2008), 317–328.
12. 12 Chang, HC, Guarente, L, SIRT1 mediates central circadian control in the SCN by a mechanism that decays with aging. Cell 153 (2013), 1448–1460.
13. 13 Nakahata, Y, Sahar, S, Astarita, G, Kaluzova, M, Sassone-Corsi, P, Circadian control of the NAD+ salvage pathway by CLOCK-SIRT1. Science 324 (2009), 654–657.
14. 14 Cohen, DE, Supinski, AM, Bonkowski, MS, Donmez, G, Guarente, LP, Neuronal SIRT1 regulates endocrine and behavioral responses to calorie restriction. Genes Dev 23 (2009), 2812–2817.
15. 15 Ramadori, G, Fujikawa, T, Anderson, J, Berglund, ED, Frazao, R, Michan, S, et al. SIRT1 deacetylase in SF1 neurons protects against metabolic imbalance. Cell Metab 14 (2011), 301–312.
16. 16 Sasaki, T, Kim, HJ, Kobayashi, M, Kitamura, YI, Yokota-Hashimoto, H, Shiuchi, T, et al. Induction of hypothalamic Sirt1 leads to cessation of feeding via agouti-related peptide. Endocrinology 151 (2010), 2556–2566.
17. 17 Satoh, A, Brace, CS, Ben-Josef, G, West, T, Wozniak, DF, Holtzman, DM, et al. SIRT1 promotes the central adaptive response to diet restriction through activation of the dorsomedial and lateral nuclei of the hypothalamus. J Neurosci 30 (2010), 10220–10232.
18. 18 Gao, J, Wang, WY, Mao, YW, Graff, J, Guan, JS, Pan, L, et al. A novel pathway regulates memory and plasticity via SIRT1 and miR-134. Nature 466 (2010), 1105–1109.
19. 19 Michan, S, Li, Y, Chou, MM, Parrella, E, Ge, H, Long, JM, et al. SIRT1 is essential for normal cognitive function and synaptic plasticity. J Neurosci 30 (2010), 9695–9707.
20. 20 Ferguson, D, Koo, JW, Feng, J, Heller, E, Rabkin, J, Heshmati, M, et al. Essential role of SIRT1 signaling in the nucleus accumbens in cocaine and morphine action. J Neurosci 33 (2013), 16088–16098.
21. 21 Renthal, W, Kumar, A, Xiao, G, Wilkinson, M, Covington, HE 3rd, Maze, I, et al. Genome-wide analysis of chromatin regulation by cocaine reveals a role for sirtuins. Neuron 62 (2009), 335–348.
22. 22 Herskovits, AZ, Guarente, L, SIRT1 in neurodevelopment and brain senescence. Neuron 81 (2014), 471–483.
23. 23 Kishi, T, Yoshimura, R, Kitajima, T, Okochi, T, Okumura, T, Tsunoka, T, et al. SIRT1 gene is associated with major depressive disorder in the Japanese population. J Affect Disord 126 (2010), 167–173.
24. 24 Libert, S, Pointer, K, Bell, EL, Das, A, Cohen, DE, Asara, JM, et al. SIRT1 activates MAO-A in the brain to mediate anxiety and exploratory drive. Cell 147 (2011), 1459–1472.
25. 25 CONVERGE Consortium. Sparse whole-genome sequencing identifies two loci for major depressive disorder. Nature 523 (2015), 588–591.
26. 26 Abe, N, Uchida, S, Otsuki, K, Hobara, T, Yamagata, H, Higuchi, F, et al. Altered sirtuin deacetylase gene expression in patients with a mood disorder. J Psychiatr Res 45 (2011), 1106–1112.
27. 27 Watanabe, S, Ageta-Ishihara, N, Nagatsu, S, Takao, K, Komine, O, Endo, F, et al. SIRT1 overexpression ameliorates a mouse model of SOD1-linked amyotrophic lateral sclerosis via HSF1/HSP70i chaperone system. Mol Brain, 7, 2014, 62.
28. 28 Ferland, CL, Hawley, WR, Puckett, RE, Wineberg, K, Lubin, FD, Dohanich, GP, Schrader, LA, Sirtuin activity in dentate gyrus contributes to chronic stress-induced behavior and extracellular signal-regulated protein kinases 1 and 2 cascade changes in the hippocampus. Biol Psychiatry 74 (2013), 927–935.
29. 29 Ferland, CL, Schrader, LA, Regulation of histone acetylation in the hippocampus of chronically stressed rats: A potential role of sirtuins. Neuroscience 174 (2011), 104–114.
30. 30 Liu, D, Xie, K, Yang, X, Gu, J, Ge, L, Wang, X, Wang, Z, Resveratrol reverses the effects of chronic unpredictable mild stress on behavior, serum corticosterone levels and BDNF expression in rats. Behav Brain Res 264 (2014), 9–16.
31. 31 Hurley, LL, Akinfiresoye, L, Kalejaiye, O, Tizabi, Y, Antidepressant effects of resveratrol in an animal model of depression. Behav Brain Res 268 (2014), 1–7.
32. 32 Ge, JF, Peng, L, Cheng, JQ, Pan, CX, Tang, J, Chen, FH, Li, J, Antidepressant-like effect of resveratrol: Involvement of antioxidant effect and peripheral regulation on HPA axis. Pharmacol Biochem Behav 114–115 (2013), 64–69.
33. 33 Uchida, S, Hara, K, Kobayashi, A, Otsuki, K, Yamagata, H, Hobara, T, et al. Epigenetic status of Gdnf in the ventral striatum determines susceptibility and adaptation to daily stressful events. Neuron 69 (2011), 359–372.
34. 34 Uchida, S, Hara, K, Kobayashi, A, Funato, H, Hobara, T, Otsuki, K, et al. Early life stress enhances behavioral vulnerability to stress through the activation of REST4-mediated gene transcription in the medial prefrontal cortex of rodents. J Neurosci 30 (2010), 15007–15018.
35. 35 David, DJ, Samuels, BA, Rainer, Q, Wang, JW, Marsteller, D, Mendez, I, et al. Neurogenesis-dependent and -independent effects of fluoxetine in an animal model of anxiety/depression. Neuron 62 (2009), 479–493.
36. 36 Holick, KA, Lee, DC, Hen, R, Dulawa, SC, Behavioral effects of chronic fluoxetine in BALB/cJ mice do not require adult hippocampal neurogenesis or the serotonin 1A receptor. Neuropsychopharmacology 33 (2008), 406–417.
37. 37 Uchida, S, Martel, G, Pavlowsky, A, Takizawa, S, Hevi, C, Watanabe, Y, et al. Learning-induced and stathmin-dependent changes in microtubule stability are critical for memory and disrupted in ageing. Nat Commun, 5, 2014, 4389.
38. 38 Uchida, S, Nishida, A, Hara, K, Kamemoto, T, Suetsugi, M, Fujimoto, M, et al. Characterization of the vulnerability to repeated stress in Fischer 344 rats: Possible involvement of microRNA-mediated down-regulation of the glucocorticoid receptor. Eur J Neurosci 27 (2008), 2250–2261.
39. 39 Uchida, S, Hara, K, Kobayashi, A, Fujimoto, M, Otsuki, K, Yamagata, H, et al. Impaired hippocampal spinogenesis and neurogenesis and altered affective behavior in mice lacking heat shock factor 1. Proc Natl Acad Sci U S A 108 (2011), 1681–1686.
40. 40 Franklin, KBJ, Paxinos, G, The Mouse Brain in Stereotaxic Coordinates. 2007, Elsevier Academic Press, San Diego.
41. 41 Gunduz-Cinar, O, Hill, MN, McEwen, BS, Holmes, A, Amygdala FAAH and anandamide: Mediating protection and recovery from stress. Trends Pharmacol Sci 34 (2013), 637–644.
42. 42 Holmes, A, Wellman, CL, Stress-induced prefrontal reorganization and executive dysfunction in rodents. Neurosci Biobehav Rev 33 (2009), 773–783.
43. 43 Licznerski, P, Duman, RS, Remodeling of axo-spinous synapses in the pathophysiology and treatment of depression. Neuroscience 251 (2013), 33–50.
44. 44 McEwen, BS, Morrison, JH, The brain on stress: Vulnerability and plasticity of the prefrontal cortex over the life course. Neuron 79 (2013), 16–29.
45. 45 Berton, O, McClung, CA, Dileone, RJ, Krishnan, V, Renthal, W, Russo, SJ, et al. Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 311 (2006), 864–868.
46. 46 File, SE, Seth, P, A review of 25 years of the social interaction test. Eur J Pharmacol 463 (2003), 35–53.
47. 47 Porsolt, RD, Bertin, A, Jalfre, M, Behavioral despair in mice: A primary screening test for antidepressants. Arch Int Pharmacodyn Ther 229 (1977), 327–336.
48. 48 Solomon, JM, Pasupuleti, R, Xu, L, McDonagh, T, Curtis, R, DiStefano, PS, Huber, LJ, Inhibition of SIRT1 catalytic activity increases p53 acetylation but does not alter cell survival following DNA damage. Mol Cell Biol 26 (2006), 28–38.
49. 49 Hisahara, S, Chiba, S, Matsumoto, H, Tanno, M, Yagi, H, Shimohama, S, et al. Histone deacetylase SIRT1 modulates neuronal differentiation by its nuclear translocation. Proc Natl Acad Sci U S A 105 (2008), 15599–15604.
50. 50 Gray, JD, Milner, TA, McEwen, BS, Dynamic plasticity: The role of glucocorticoids, brain-derived neurotrophic factor and other trophic factors. Neuroscience 239 (2013), 214–227.
51. 51 Pittenger, C, Duman, RS, Stress, depression, and neuroplasticity: A convergence of mechanisms. Neuropsychopharmacology 33 (2008), 88–109.
52. 52 Watanabe, Y, Gould, E, McEwen, BS, Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res 588 (1992), 341–345.
53. 53 Tsai, SY, Hayashi, T, Harvey, BK, Wang, Y, Wu, WW, Shen, RF, et al. Sigma-1 receptors regulate hippocampal dendritic spine formation via a free radical-sensitive mechanism involving Rac1xGTP pathway. Proc Natl Acad Sci U S A 106 (2009), 22468–22473.
54. 54 Alfonso, J, Fernandez, ME, Cooper, B, Flugge, G, Frasch, AC, The stress-regulated protein M6a is a key modulator for neurite outgrowth and filopodium/spine formation. Proc Natl Acad Sci U S A 102 (2005), 17196–17201.
55. 55 Dehmelt, L, Smart, FM, Ozer, RS, Halpain, S, The role of microtubule-associated protein 2c in the reorganization of microtubules and lamellipodia during neurite initiation. J Neurosci 23 (2003), 9479–9490.
56. 56 Ma׳ayan, A, Jenkins, SL, Barash, A, Iyengar, R, Neuro2A differentiation by Galphai/o pathway. Sci Signal 2:cm1., 2009.
57. 57 Li, Y, Xu, W, McBurney, MW, Longo, VD, SirT1 inhibition reduces IGF-I/IRS-2/Ras/ERK1/2 signaling and protects neurons. Cell Metab 8 (2008), 38–48.
58. 58 Iniguez, SD, Vialou, V, Warren, BL, Cao, JL, Alcantara, LF, Davis, LC, et al. Extracellular signal-regulated kinase-2 within the ventral tegmental area regulates responses to stress. J Neurosci 30 (2010), 7652–7663.
59. 59 Duman, CH, Schlesinger, L, Kodama, M, Russell, DS, Duman, RS, A role for MAP kinase signaling in behavioral models of depression and antidepressant treatment. Biol Psychiatry 61 (2007), 661–670.
60. 60 Dwivedi, Y, Rizavi, HS, Roberts, RC, Conley, RC, Tamminga, CA, Pandey, GN, Reduced activation and expression of ERK1/2 MAP kinase in the post-mortem brain of depressed suicide subjects. J Neurochem 77 (2001), 916–928.
61. 61 Duric, V, Banasr, M, Licznerski, P, Schmidt, HD, Stockmeier, CA, Simen, AA, et al. A negative regulator of MAP kinase causes depressive behavior. Nat Med 16 (2010), 1328–1332.
62. 62 Alonso, M, Melani, M, Converso, D, Jaitovich, A, Paz, C, Carreras, MC, et al. Mitochondrial extracellular signal-regulated kinases 1/2 (ERK1/2) are modulated during brain development. J Neurochem 89 (2004), 248–256.
63. 63 Winder, DG, Martin, KC, Muzzio, IA, Rohrer, D, Chruscinski, A, Kobilka, B, Kandel, ER, ERK plays a regulatory role in induction of LTP by theta frequency stimulation and its modulation by beta-adrenergic receptors. Neuron 24 (1999), 715–726.
64. 64 Impey, S, Obrietan, K, Storm, DR, Making new connections: Role of ERK/MAP kinase signaling in neuronal plasticity. Neuron 23 (1999), 11–14.
65. 65 Bordone, L, Cohen, D, Robinson, A, Motta, MC, van Veen, E, Czopik, A, et al. SIRT1 transgenic mice show phenotypes resembling calorie restriction. Aging Cell 6 (2007), 759–767.
66. 66 McBurney, MW, Yang, X, Jardine, K, Hixon, M, Boekelheide, K, Webb, JR, et al. The mammalian SIR2alpha protein has a role in embryogenesis and gametogenesis. Mol Cell Biol 23 (2003), 38–54.
67. 67 Wolfer, DP, Crusio, WE, Lipp, HP, Knockout mice: Simple solutions to the problems of genetic background and flanking genes. Trends Neurosci 25 (2002), 336–340.
68. 68 Crusio, WE, Flanking gene and genetic background problems in genetically manipulated mice. Biol Psychiatry 56 (2004), 381–385.
69. 69 Francis, DD, Szegda, K, Campbell, G, Martin, WD, Insel, TR, Epigenetic sources of behavioral differences in mice. Nat Neurosci 6 (2003), 445–446.
70. 70 Hovatta, I, Tennant, RS, Helton, R, Marr, RA, Singer, O, Redwine, JM, et al. Glyoxalase 1 and glutathione reductase 1 regulate anxiety in mice. Nature 438 (2005), 662–666.
71. 71 Mozhui, K, Karlsson, RM, Kash, TL, Ihne, J, Norcross, M, Patel, S, et al. Strain differences in stress responsivity are associated with divergent amygdala gene expression and glutamate-mediated neuronal excitability. J Neurosci 30 (2010), 5357–5367.
72. 72 Fanselow, MS, Dong, HW, Are the dorsal and ventral hippocampus functionally distinct structures?. Neuron 65 (2010), 7–19.
73. 73 Bannerman, DM, Rawlins, JN, McHugh, SB, Deacon, RM, Yee, BK, Bast, T, et al. Regional dissociations within the hippocampus–memory and anxiety. Neurosci Biobehav Rev 28 (2004), 273–283.
74. 74 Guo, W, Qian, L, Zhang, J, Zhang, W, Morrison, A, Hayes, P, et al. Sirt1 overexpression in neurons promotes neurite outgrowth and cell survival through inhibition of the mTOR signaling. J Neurosci Res 89 (2011), 1723–1736.
75. 75 Codocedo, JF, Allard, C, Godoy, JA, Varela-Nallar, L, Inestrosa, NC, SIRT1 regulates dendritic development in hippocampal neurons. PLoS One, 7, 2012, e47073.
76. 76 Sugino, T, Maruyama, M, Tanno, M, Kuno, A, Houkin, K, Horio, Y, Protein deacetylase SIRT1 in the cytoplasm promotes nerve growth factor-induced neurite outgrowth in PC12 cells. FEBS Lett 584 (2010), 2821–2826.
77. 77 Kim, MJ, Ahn, K, Park, SH, Kang, HJ, Jang, BG, Oh, SJ, et al. SIRT1 regulates tyrosine hydroxylase expression and differentiation of neuroblastoma cells via FOXO3a. FEBS Lett 583 (2009), 1183–1188.
78. 78 Dasgupta, B, Milbrandt, J, Resveratrol stimulates AMP kinase activity in neurons. Proc Natl Acad Sci U S A 104 (2007), 7217–7222.
79. 79 Michan, S, Sinclair, D, Sirtuins in mammals: Insights into their biological function. Biochem J 404 (2007), 1–13.
80. 80 Westerheide, SD, Anckar, J, Stevens, SM Jr, Sistonen, L, Morimoto, RI, Stress-inducible regulation of heat shock factor 1 by the deacetylase SIRT1. Science 323 (2009), 1063–1066.