Circuit-wide Transcriptional Profiling Reveals Brain Region-Specific Gene Networks Regulating Depression Susceptibility

Neuron

Volumn 90, Issue 5, 2016, Pages 969-983

  Bagot, Rosemary C ^a   Cates, Hannah M ^a   Purushothaman, Immanuel ^a   Lorsch, Zachary S ^a   Walker, Deena M ^a   Wang, Junshi ^b   Huang, Xiaojie ^b   Schlüter, Oliver M ^b   Maze, Ian ^a   Peña, Catherine J ^a   Heller, Elizabeth A ^a,c   Issler, Orna ^a   Wang, Minghui ^a   Song, Won min ^a   Stein, Jason  L ^d,e   Liu, Xiaochuan ^a   Doyle, Marie A ^a   Scobie, Kimberly N ^a   Sun, Hao Sheng ^a   Neve, Rachael L ^f   Geschwind, Daniel ^e   Dong, Yan ^b   Shen, Li ^a   Zhang, Bin ^a   Nestler, Eric J ^a   more..

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BIOINFORMATICS; BRAIN REGION; BRAIN SLICE; CONTROLLED STUDY; DEPRESSION; DISEASE PREDISPOSITION; DISEASE RESISTANCE; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE IDENTIFICATION; GENE OVEREXPRESSION; GENE REGULATORY NETWORK; GENETIC SUSCEPTIBILITY; GENETIC TRANSCRIPTION; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RNA SEQUENCE; SOCIAL STRESS; STEREOTAXIC SURGERY; SYNAPSE; VALIDATION STUDY; ANIMAL; BRAIN; EXCITATORY POSTSYNAPTIC POTENTIAL; GENETIC PREDISPOSITION; GENETICS; HIPPOCAMPUS; METABOLISM; NERVE TRACT; PHYSIOLOGY; SOCIAL BEHAVIOR;

TRANSCRIPTOME;

ANIMALS; BRAIN; DEPRESSION; EXCITATORY POSTSYNAPTIC POTENTIALS; GENE REGULATORY NETWORKS; GENETIC PREDISPOSITION TO DISEASE; HIPPOCAMPUS; MICE; NEURAL PATHWAYS; SOCIAL BEHAVIOR; TRANSCRIPTOME;

EID: 84966622155     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2016.04.015     Document Type: Article

References (66)

1. Admon, R., Holsen, L.M., Aizley, H., Remington, A., Whitfield-Gabrieli, S., Goldstein, J.M., Pizzagalli, D.A., Striatal hypersensitivity during stress in remitted individuals with recurrent depression. Biol. Psychiatry 78 (2015), 67–76.
2. Arloth, J., Bogdan, R., Weber, P., Frishman, G., Menke, A., Wagner, K.V., Balsevich, G., Schmidt, M.V., Karbalai, N., Czamara, D., et al. Major Depressive Disorder Working Group of the Psychiatric Genomics Consortium (PGC), Major Depressive Disorder Working Group of the Psychiatric Genomics Consortium PGC. Genetic differences in the immediate transcriptome response to stress predict risk-related brain function and psychiatric disorders. Neuron 86 (2015), 1189–1202.
3. Bagot, R.C., Parise, E.M., Peña, C.J., Zhang, H.X., Maze, I., Chaudhury, D., Persaud, B., Cachope, R., Bolaños-Guzmán, C.A., Cheer, J.F., et al. Ventral hippocampal afferents to the nucleus accumbens regulate susceptibility to depression. Nat. Commun., 6, 2015, 7062.
4. Berton, O., McClung, C.A., Dileone, R.J., Krishnan, V., Renthal, W., Russo, S.J., Graham, D., Tsankova, N.M., Bolanos, C.A., Rios, M., et al. Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 311 (2006), 864–868.
5. Block, S.G., Nemeroff, C.B., Emerging antidepressants to treat major depressive disorder. Asian J. Psychiatr. 12 (2014), 7–16.
6. Buijs, R.M., Van Eden, C.G., The integration of stress by the hypothalamus, amygdala and prefrontal cortex: balance between the autonomic nervous system and the neuroendocrine system. Prog. Brain Res. 126 (2000), 117–132.
7. Chang, L.C., Jamain, S., Lin, C.W., Rujescu, D., Tseng, G.C., Sibille, E., A conserved BDNF, glutamate- and GABA-enriched gene module related to human depression identified by coexpression meta-analysis and DNA variant genome-wide association studies. PLoS ONE, 9, 2014, e90980.
8. Chen, Z.Q., Du, M.Y., Zhao, Y.J., Huang, X.Q., Li, J., Lui, S., Hu, J.M., Sun, H.Q., Liu, J., Kemp, G.J., et al. Voxel-wise meta-analyses of brain blood flow and local synchrony abnormalities in medication-free patients with major depressive disorder. J. Psychiatry Neurosci., 40, 2015, 140119.
9. Christoffel, D.J., Golden, S.A., Walsh, J.J., Guise, K.G., Heshmati, M., Friedman, A.K., Dey, A., Smith, M., Rebusi, N., Pfau, M., et al. Excitatory transmission at thalamo-striatal synapses mediates susceptibility to social stress. Nat. Neurosci. 18 (2015), 962–964.
10. Cooper, D.C., Moore, S.J., Staff, N.P., Spruston, N., Psychostimulant-induced plasticity of intrinsic neuronal excitability in ventral subiculum. J. Neurosci. 23 (2003), 9937–9946.
11. Covington, H.E. 3rd, Lobo, M.K., Maze, I., Vialou, V., Hyman, J.M., Zaman, S., LaPlant, Q., Mouzon, E., Ghose, S., Tamminga, C.A., et al. Antidepressant effect of optogenetic stimulation of the medial prefrontal cortex. J. Neurosci. 30 (2010), 16082–16090.
12. Dias, C., Feng, J., Sun, H., Shao, N.Y., Mazei-Robison, M.S., Damez-Werno, D., Scobie, K., Bagot, R., LaBonté, B., Ribeiro, E., et al. β-catenin mediates stress resilience through Dicer1/microRNA regulation. Nature 516 (2014), 51–55.
13. Ding, Y., Chang, L.C., Wang, X., Guilloux, J.P., Parrish, J., Oh, H., French, B.J., Lewis, D.A., Tseng, G.C., Sibille, E., Molecular and genetic characterization of depression: overlap with other psychiatric disorders and aging. Mol. Neuropsychiatry 1 (2015), 1–12.
14. Epstein, J., Pan, H., Kocsis, J.H., Yang, Y., Butler, T., Chusid, J., Hochberg, H., Murrough, J., Strohmayer, E., Stern, E., Silbersweig, D.A., Lack of ventral striatal response to positive stimuli in depressed versus normal subjects. Am. J. Psychiatry 163 (2006), 1784–1790.
15. Fabbri, C., Serretti, A., Pharmacogenetics of major depressive disorder: top genes and pathways toward clinical applications. Curr. Psychiatry Rep., 17, 2015, 50.
16. Friedman, A.K., Walsh, J.J., Juarez, B., Ku, S.M., Chaudhury, D., Wang, J., Li, X., Dietz, D.M., Pan, N., Vialou, V.F., et al. Enhancing depression mechanisms in midbrain dopamine neurons achieves homeostatic resilience. Science 344 (2014), 313–319.
17. Gaiteri, C., Sibille, E., Differentially expressed genes in major depression reside on the periphery of resilient gene coexpression networks. Front. Neurosci., 5, 2011, 95.
18. Gaiteri, C., Guilloux, J.P., Lewis, D.A., Sibille, E., Altered gene synchrony suggests a combined hormone-mediated dysregulated state in major depression. PLoS ONE, 5, 2010, e9970.
19. Gaiteri, C., Ding, Y., French, B., Tseng, G.C., Sibille, E., Beyond modules and hubs: the potential of gene coexpression networks for investigating molecular mechanisms of complex brain disorders. Genes Brain Behav. 13 (2014), 13–24.
20. Goto, Y., Grace, A.A., Limbic and cortical information processing in the nucleus accumbens. Trends Neurosci. 31 (2008), 552–558.
21. Greenberg, P.E., Fournier, A.A., Sisitsky, T., Pike, C.T., Kessler, R.C., The economic burden of adults with major depressive disorder in the United States (2005 and 2010). J. Clin. Psychiatry 76 (2015), 155–162.
22. Groenewegen, H.J., Vermeulen-Van der Zee, E., te Kortschot, A., Witter, M.P., Organization of the projections from the subiculum to the ventral striatum in the rat. A study using anterograde transport of Phaseolus vulgaris leucoagglutinin. Neuroscience 23 (1987), 103–120.
23. Guilloux, J.P., Douillard-Guilloux, G., Kota, R., Wang, X., Gardier, A.M., Martinowich, K., Tseng, G.C., Lewis, D.A., Sibille, E., Molecular evidence for BDNF- and GABA-related dysfunctions in the amygdala of female subjects with major depression. Mol. Psychiatry 17 (2012), 1130–1142.
24. Heller, E.A., Cates, H.M., Peña, C.J., Sun, H., Shao, N., Feng, J., Golden, S.A., Herman, J.P., Walsh, J.J., Mazei-Robison, M., et al. Locus-specific epigenetic remodeling controls addiction- and depression-related behaviors. Nat. Neurosci. 17 (2014), 1720–1727.
25. Hooley, J.M., Gruber, S.A., Parker, H.A., Guillaumot, J., Rogowska, J., Yurgelun-Todd, D.A., Cortico-limbic response to personally challenging emotional stimuli after complete recovery from depression. Psychiatry Res. 172 (2009), 83–91.
26. Insel, N., Pilkiw, M., Nobrega, J.N., Hutchison, W.D., Takehara-Nishiuchi, K., Hamani, C., Chronic deep brain stimulation of the rat ventral medial prefrontal cortex disrupts hippocampal-prefrontal coherence. Exp. Neurol. 269 (2015), 1–7.
27. Jaworska, N., Yang, X.R., Knott, V., Macqueen, G., A review of fMRI studies during visual emotive processing in major depressive disorder. World J. Biol. Psychiatry 16 (2014), 448–471.
28. Kang, H.J., Voleti, B., Hajszan, T., Rajkowska, G., Stockmeier, C.A., Licznerski, P., Lepack, A., Majik, M.S., Jeong, L.S., Banasr, M., et al. Decreased expression of synapse-related genes and loss of synapses in major depressive disorder. Nat. Med. 18 (2012), 1413–1417.
29. Kennedy, S.H., Evans, K.R., Krüger, S., Mayberg, H.S., Meyer, J.H., McCann, S., Arifuzzman, A.I., Houle, S., Vaccarino, F.J., Changes in regional brain glucose metabolism measured with positron emission tomography after paroxetine treatment of major depression. Am. J. Psychiatry 158 (2001), 899–905.
30. Krishnan, V., Han, M.H., Graham, D.L., Berton, O., Renthal, W., Russo, S.J., Laplant, Q., Graham, A., Lutter, M., Lagace, D.C., et al. Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell 131 (2007), 391–404.
31. Langfelder, P., Zhang, B., Horvath, S., Defining clusters from a hierarchical cluster tree: the Dynamic Tree Cut package for R. Bioinformatics 24 (2008), 719–720.
32. Malki, K., Tosto, M.G., Jumabhoy, I., Lourdusamy, A., Sluyter, F., Craig, I., Uher, R., McGuffin, P., Schalkwyk, L.C., Integrative mouse and human mRNA studies using WGCNA nominates novel candidate genes involved in the pathogenesis of major depressive disorder. Pharmacogenomics 14 (2013), 1979–1990.
33. Malki, K., Mineur, Y.S., Tosto, M.G., Campbell, J., Karia, P., Jumabhoy, I., Sluyter, F., Crusio, W.E., Schalkwyk, L.C., Pervasive and opposing effects of Unpredictable Chronic Mild Stress (UCMS) on hippocampal gene expression in BALB/cJ and C57BL/6J mouse strains. BMC Genomics, 16, 2015, 262.
34. Margolin, A.A., Nemenman, I., Basso, K., Wiggins, C., Stolovitzky, G., Dalla Favera, R., Califano, A., ARACNE: an algorithm for the reconstruction of gene regulatory networks in a mammalian cellular context. BMC Bioinformatics, 7(Suppl 1), 2006, S7.
35. Maschietto, M., Tahira, A.C., Puga, R., Lima, L., Mariani, D., Paulsen, Bda.S., Belmonte-de-Abreu, P., Vieira, H., Krepischi, A.C., Carraro, D.M., et al. Co-expression network of neural-differentiation genes shows specific pattern in schizophrenia. BMC Med. Genomics, 8, 2015, 23.
36. Mayberg, H.S., Brannan, S.K., Tekell, J.L., Silva, J.A., Mahurin, R.K., McGinnis, S., Jerabek, P.A., Regional metabolic effects of fluoxetine in major depression: serial changes and relationship to clinical response. Biol. Psychiatry 48 (2000), 830–843.
37. Messmer, K., Shen, W.B., Remington, M., Fishman, P.S., Induction of neural differentiation by the transcription factor neuroD2. Int. J. Dev. Neurosci. 30 (2012), 105–112.
38. Miller, J.A., Woltjer, R.L., Goodenbour, J.M., Horvath, S., Geschwind, D.H., Genes and pathways underlying regional and cell type changes in Alzheimer's disease. Genome Med., 5, 2013, 48.
39. Nestler, E.J., Carlezon, W.A. Jr., The mesolimbic dopamine reward circuit in depression. Biol. Psychiatry 59 (2006), 1151–1159.
40. Network and Pathway Analysis Subgroup of Psychiatric Genomics Consortium. Psychiatric genome-wide association study analyses implicate neuronal, immune and histone pathways. Nat. Neurosci. 18 (2015), 199–209.
41. Oliva, C.A., Vargas, J.Y., Inestrosa, N.C., Wnts in adult brain: from synaptic plasticity to cognitive deficiencies. Front. Cell. Neurosci., 7, 2013, 224.
42. Olson, J.M., Asakura, A., Snider, L., Hawkes, R., Strand, A., Stoeck, J., Hallahan, A., Pritchard, J., Tapscott, S.J., NeuroD2 is necessary for development and survival of central nervous system neurons. Dev. Biol. 234 (2001), 174–187.
43. Parikshak, N.N., Luo, R., Zhang, A., Won, H., Lowe, J.K., Chandran, V., Horvath, S., Geschwind, D.H., Integrative functional genomic analyses implicate specific molecular pathways and circuits in autism. Cell 155 (2013), 1008–1021.
44. Philip, N.S., Carpenter, L.L., Tyrka, A.R., Price, L.H., Nicotinic acetylcholine receptors and depression: a review of the preclinical and clinical literature. Psychopharmacology (Berl.) 212 (2010), 1–12.
45. Plaisier, S.B., Taschereau, R., Wong, J.A., Graeber, T.G., Rank-rank hypergeometric overlap: identification of statistically significant overlap between gene-expression signatures. Nucleic Acids Res., 38, 2010, e169.
46. Posner, J., Hellerstein, D.J., Gat, I., Mechling, A., Klahr, K., Wang, Z., McGrath, P.J., Stewart, J.W., Peterson, B.S., Antidepressants normalize the default mode network in patients with dysthymia. J. Am. Med. Assoc. Psychiatry 70 (2013), 373–382.
47. 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.
48. Schlaepfer, T.E., Cohen, M.X., Frick, C., Kosel, M., Brodesser, D., Axmacher, N., Joe, A.Y., Kreft, M., Lenartz, D., Sturm, V., Deep brain stimulation to reward circuitry alleviates anhedonia in refractory major depression. Neuropsychopharmacology 33 (2008), 368–377.
49. Schrattenholz, A., Soskić, V., What does systems biology mean for drug development?. Curr. Med. Chem. 15 (2008), 1520–1528.
50. Schrattenholz, A., Groebe, K., Soskić, V., Systems biology approaches and tools for analysis of interactomes and multi-target drugs. Methods Mol. Biol. 662 (2010), 29–58.
51. Scobie, K.N., Damez-Werno, D., Sun, H., Shao, N., Gancarz, A., Panganiban, C.H., Dias, C., Koo, J., Caiafa, P., Kaufman, L., et al. Essential role of poly(ADP-ribosyl)ation in cocaine action. Proc. Natl. Acad. Sci. USA 111 (2014), 2005–2010.
52. Sequeira, A., Mamdani, F., Ernst, C., Vawter, M.P., Bunney, W.E., Lebel, V., Rehal, S., Klempan, T., Gratton, A., Benkelfat, C., et al. Global brain gene expression analysis links glutamatergic and GABAergic alterations to suicide and major depression. PLoS ONE, 4, 2009, e6585.
53. Sibbe, M., Jarowyj, J., Region-specific expression of Dickkopf-like1 in the adult brain. Abbreviated title: Dkkl1 in the adult brain. Neurosci. Lett. 535 (2013), 84–89.
54. Steel, Z., Marnane, C., Iranpour, C., Chey, T., Jackson, J.W., Patel, V., Silove, D., The global prevalence of common mental disorders: a systematic review and meta-analysis 1980-2013. Int. J. Epidemiol. 43 (2014), 476–493.
55. Stein, J.L., de la Torre-Ubieta, L., Tian, Y., Parikshak, N.N., Hernández, I.A., Marchetto, M.C., Baker, D.K., Lu, D., Hinman, C.R., Lowe, J.K., et al. A quantitative framework to evaluate modeling of cortical development by neural stem cells. Neuron 83 (2014), 69–86.
56. Tham, M.W., Woon, P.S., Sum, M.Y., Lee, T.S., Sim, K., White matter abnormalities in major depression: evidence from post-mortem, neuroimaging and genetic studies. J. Affect. Disord. 132 (2011), 26–36.
57. Trapnell, C., Roberts, A., Goff, L., Pertea, G., Kim, D., Kelley, D.R., Pimentel, H., Salzberg, S.L., Rinn, J.L., Pachter, L., Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7 (2012), 562–578.
58. Vanderlinden, L.A., Saba, L.M., Kechris, K., Miles, M.F., Hoffman, P.L., Tabakoff, B., Whole brain and brain regional coexpression network interactions associated with predisposition to alcohol consumption. PLoS ONE, 8, 2013, e68878.
59. Vialou, V., Bagot, R.C., Cahill, M.E., Ferguson, D., Robison, A.J., Dietz, D.M., Fallon, B., Mazei-Robison, M., Ku, S.M., Harrigan, E., et al. Prefrontal cortical circuit for depression- and anxiety-related behaviors mediated by cholecystokinin: role of ΔFosB. J. Neurosci. 34 (2014), 3878–3887.
60. Wilke, S.A., Hall, B.J., Antonios, J.K., Denardo, L.A., Otto, S., Yuan, B., Chen, F., Robbins, E.M., Tiglio, K., Williams, M.E., et al. NeuroD2 regulates the development of hippocampal mossy fiber synapses. Neural Dev., 7, 2012, 9.
61. Wilkinson, M.B., Xiao, G., Kumar, A., LaPlant, Q., Renthal, W., Sikder, D., Kodadek, T.J., Nestler, E.J., Imipramine treatment and resiliency exhibit similar chromatin regulation in the mouse nucleus accumbens in depression models. J. Neurosci. 29 (2009), 7820–7832.
62. Yamagata, M., Sanes, J.R., Dscam and Sidekick proteins direct lamina-specific synaptic connections in vertebrate retina. Nature 451 (2008), 465–469.
63. Yamagata, M., Weiner, J.A., Sanes, J.R., Sidekicks: synaptic adhesion molecules that promote lamina-specific connectivity in the retina. Cell 110 (2002), 649–660.
64. Zhang, B., Horvath, S., A general framework for weighted gene co-expression network analysis. Stat. Appl. Genet. Mol. Biol., 4, 2005 Article 17.
65. Zhang, B., Gaiteri, C., Bodea, L.G., Wang, Z., McElwee, J., Podtelezhnikov, A.A., Zhang, C., Xie, T., Tran, L., Dobrin, R., et al. Integrated systems approach identifies genetic nodes and networks in late-onset Alzheimer's disease. Cell 153 (2013), 707–720.
66. Zhang, Y., Chen, K., Sloan, S.A., Bennett, M.L., Scholze, A.R., O'Keeffe, S., Phatnani, H.P., Guarnieri, P., Caneda, C., Ruderisch, N., et al. An RNA-sequencing transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex. J. Neurosci. 34 (2014), 11929–11947.