Transcriptome analysis of genes and gene networks involved in aggressive behavior in mouse and zebrafish
Open accessAbstract
Despite moderate heritability estimates, the molecular architecture of aggressive behavior remains poorly characterized. This study compared gene expression profiles from a genetic mouse model of aggression with zebrafish, an animal model traditionally used to study aggression. A meta‐analytic, cross‐species approach was used to identify genomic variants associated with aggressive behavior. The Rankprod algorithm was used to evaluated mRNA differences from prefrontal cortex tissues of three sets of mouse lines (N = 18) selectively bred for low and high aggressive behavior (SAL/LAL, TA/TNA, and NC900/NC100). The same approach was used to evaluate mRNA differences in zebrafish (N = 12) exposed to aggressive or non‐aggressive social encounters. Results were compared to uncover genes consistently implicated in aggression across both studies. Seventy‐six genes were differentially expressed (PFP < 0.05) in aggressive compared to non‐aggressive mice. Seventy genes were differentially expressed in zebrafish exposed to a fight encounter compared to isolated zebrafish. Seven genes (Fos, Dusp1, Hdac4, Ier2, Bdnf, Btg2, and Nr4a1) were differentially expressed across both species 5 of which belonging to a gene‐network centred on the c‐Fos gene hub. Network analysis revealed an association with the MAPK signaling cascade. In human studies HDAC4 haploinsufficiency is a key genetic mechanism associated with brachydactyly mental retardation syndrome (BDMR), which is associated with aggressive behaviors. Moreover, the HDAC4 receptor is a drug target for valproic acid, which is being employed as an effective pharmacological treatment for aggressive behavior in geriatric, psychiatric, and brain‐injury patients. © 2016 Wiley Periodicals, Inc.
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Exploration, normalization, and summaries of high density oligonucleotide array probe level data
Irizarry, R. A. (2003) · Biostatistics · doi:10.1093/biostatistics/4.2.249 · Cited by 10,603 · see citing works
Adjusting batch effects in microarray expression data using empirical Bayes methods
Johnson, W. E., Li, C., & Rabinovic, A. (2007) · Biostatistics · doi:10.1093/biostatistics/kxj037 · Cited by 8,658 · see citing works
AP-1 as a regulator of cell life and death
Shaulian, E., & Karin, M. (2002) · Nature Cell Biology · doi:10.1038/ncb0502-e131 · Cited by 2,961 · cited 1× · see citing works
“Ap-1 regulates major physiological processes including cell proliferation, differentiation, and response to stress [Shaulian and Karin, 2002].”
BackgroundSerious mental disorder in 23 000 prisoners: a systematic review of 62 surveys
Fazel, S., & Danesh, J. (2002) · The Lancet · doi:10.1016/s0140-6736(02)07740-1 · Cited by 2,201 · see citing works
Animal models of human disease: zebrafish swim into view
Lieschke, G. J., & Currie, P. D. (2007) · Nature Reviews Genetics · doi:10.1038/nrg2091 · Cited by 2,162 · see citing works
Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells
Göttlicher, M., Minucci, S., Zhu, P., Krämer, O. H., Schimpf, A., Giavara, S., Sleeman, J. P., Coco, F. L., Nervi, C., Pelicci, P. G., et al. (2001) · The EMBO Journal · doi:10.1093/emboj/20.24.6969 · Cited by 1,889 · see citing works
Abnormal behavior associated with a point mutation in the structural gene for monoamine oxidase A
Brunner, H. G., Nelen, M., Breakefield, X. O., Ropers, H. H., & van Oost, B. A. (1993) · Science · doi:10.1126/science.8211186 · Cited by 1,644 · see citing works
Rainer Breitling, A., Armengaud, P., Anna Amtmann, A., & Herzyk, P. (2004) · FEBS Letters · doi:10.1016/j.febslet.2004.07.055 · Cited by 1,478 · see citing works
Aggressive Behavior and Altered Amounts of Brain Serotonin and Norepinephrine in Mice Lacking MAOA
Cases, O., Seif, I., Grimsby, J. S., Gaspar, P., Chen, K., Vandormael‐Pournin, S., Müller, U., Aguet, M., Babinet, C., Shih, J. C., et al. (1995) · Science · doi:10.1126/science.7792602 · Cited by 1,225 · see citing works
The behaviour and ecology of the zebrafish, Danio rerio
Spence, R., Gerlach, G., Lawrence, C., & Smith, C. (2007) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/j.1469-185x.2007.00030.x · Cited by 1,130 · see citing works
Lyons, W. E., Mamounas, L. A., Ricaurte, G. A., Coppola, V., Reid, S. W., Bora, S. H., Wihler, C., Koliatsos, V. E., & Tessarollo, L. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.26.15239 · Cited by 862 · see citing works
Enhanced Aggressive Behavior in Mice Lacking 5-HT 1B Receptor
Saudou, F., Amara, D. A., Dierich, A., LeMeur, M., Ramboz, S., Ségu, L., Buhot, M.-C., & Hen, R. (1994) · Science · doi:10.1126/science.8091214 · Cited by 839 · see citing works
Modulation of aggressive behaviour by fighting experience: mechanisms and contest outcomes
Hsu, Y., Earley, R. L., & Wolf, L. L. (2005) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1017/s146479310500686x · Cited by 766 · see citing works
RankProd: a bioconductor package for detecting differentially expressed genes in meta-analysis
Hong, F., Breitling, R., McEntee, C., Wittner, B. S., Nemhauser, J. L., & Chory, J. (2006) · Bioinformatics · doi:10.1093/bioinformatics/btl476 · Cited by 741 · see citing works
The Syntenic Relationship of the Zebrafish and Human GenomesPreprint
Barbazuk, W. B., Korf, I. F., Kadavi, C., Heyen, J. W., Tate, S., Wun, E., Bedell, J. A., McPherson, J. D., & Johnson, S. L. (2000) · Genome Research · doi:10.1101/gr.144700 · Cited by 650 · see citing works
Neurotrophin signalling in health and disease
Chao, M. V., Rajagopal, R., & Lee, F. S. (2006) · Clinical Science · doi:10.1042/cs20050163 · Cited by 619 · see citing works
The histone deacetylase inhibitor valproic acid selectively induces proteasomal degradation of HDAC2
Krämer, O. H., Zhu, P., Ostendorff, H. P., Golebiewski, M., Tiefenbach, J., Peters, M. A., Brill, B., Groner, B., Bach, I., Heinzel, T., et al. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg315 · Cited by 523 · see citing works
Seo, D., Patrick, C. J., & Kennealy, P. J. (2008) · Aggression and Violent Behavior · doi:10.1016/j.avb.2008.06.003 · Cited by 520 · see citing works
Tyler, W. J., & Pozzo‐Miller, L. D. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-12-04249.2001 · Cited by 520 · see citing works
Behavioral effects of estrogen receptor gene disruption in male mice
Ogawa, S., Lubahn, D. B., Korach, K. S., & Pfaff, D. W. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.4.1476 · Cited by 498 · see citing works
Genetic and environmental architecture on human aggression.
Miles, D. R., & Carey, G. (1997) · Journal of Personality and Social Psychology · doi:10.1037//0022-3514.72.1.207 · Cited by 490 · see citing works
Panula, P., Chen, Y.-C., Priyadarshini, M., Kudo, H., Semenova, S. A., Sundvik, M., & Sallinen, V. J. (2010) · Neurobiology of Disease · doi:10.1016/j.nbd.2010.05.010 · Cited by 454 · see citing works
Genetic and environmental architecture on human aggression.
Miles, D. R., & Carey, G. (1997) · Journal of Personality and Social Psychology · doi:10.1037/0022-3514.72.1.207 · Cited by 414 · see citing works
A Comparative Map of the Zebrafish GenomePreprint
Woods, I. G. (2000) · Genome Research · doi:10.1101/gr.10.12.1903 · Cited by 399 · see citing works
Lasky-Su, J. A., Neale, B. M., Franke, B., Anney, R., Zhou, K., Maller, J., Vásquez, A. A., Chen, W., Asherson, P. J., Buitelaar, J. K., et al. (2008) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.30867 · Cited by 388 · see citing works
Self-citationAggression and vasotocin are associated with dominant–subordinate relationships in zebrafish
Larson, E. T., O’Malley, D. M., & Melloni, R. H. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.08.020 · Cited by 290 · see citing works
Regulation of T cell activation, anxiety, and male aggression by RGS2
Oliveira-dos-Santos, A., Matsumoto, G., Snow, B. E., Bai, D., Houston, F. P., Whishaw, I. Q., Mariathasan, S., Sasaki, T., Wakeham, A. C., Ohashi, P. S., et al. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.220414397 · Cited by 290 · see citing works
Genome-wide Association Scan of Attention Deficit Hyperactivity Disorder
Neale, B., Su, J., Anney, R., Franke, B., Zhou, K., Maller, J., Vásquez, A., Asherson, P., Chen, W., Banaschewski, T., et al. (2008) · American Journal of Medical Genetics Part B: Neuropsychiatric Genetics · doi:10.1002/ajmg.b.30866 · Cited by 288 · see citing works
Self-citationDivalproex in the Treatment of Impulsive Aggression: Efficacy in Cluster B Personality Disorders
Hollander, E., Tracy, K. A., Swann, A. C., Coccaro, E. F., McElroy, S. L., Wozniak, P., Sommerville, K. W., & Nemeroff, C. B. (2003) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300153 · Cited by 279 · see citing works
Donovan, S. J., Stewart, J. W., Nunes, E. V., Quitkin, F. M., Parides, M., Daniel, W., Susser, E., & Klein, D. F. (2000) · American Journal of Psychiatry · doi:10.1176/appi.ajp.157.5.818 · Cited by 273 · cited 1× · see citing works
“…effective in controlling disruptive behavior in adolescents with conduct disorder and adjunctive therapy to reduce aggression in children with ADHD [Donovan et al., 2000; Wozniak, 2005; MacMillan et al., 2006; Blader et al., 2009]. c-Fos also interacts directly with the Bdnf (Brain-derived…”
BackgroundArtificial selection for short and long attack latencies in wildMus musculus domesticus
van Oortmerssen, G. A., & Bakker, T. C. M. (1981) · Behavior Genetics · doi:10.1007/bf01065622 · Cited by 263 · see citing works
Li, H., Radford, J. C., Ragusa, M. J., Shea, K. L., McKercher, S. R., Zaremba, J. D., Soussou, W., Nie, Z., Kang, Y., Nakanishi, N., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0802876105 · Cited by 254 · see citing works
A review of effective interventions for reducing aggression and violence
McGuire, J. (2008) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2008.0035 · Cited by 234 · see citing works
Vassos, E., Collier, D. A., & Fazel, S. (2014) · Molecular Psychiatry · doi:10.1038/mp.2013.31 · Cited by 234 · cited 1× · see citing works
“However, these findings often show small effect sizes and fail to replicate [Vassos et al., 2014].”
ResultTirone, F. (2001) · Journal of Cellular Physiology · doi:10.1002/jcp.1062 · Cited by 213 · see citing works
Fighting Zebrafish: Characterization of Aggressive Behavior and Winner–Loser Effects
Oliveira, R. F., Silva, J. F., & Simões, J. M. (2011) · Zebrafish · doi:10.1089/zeb.2011.0690 · Cited by 208 · see citing works
Etiology of the impulsivity/aggression relationship: Genes or environment?
Seroczynski, A. D., Bergeman, C. S., & Coccaro, E. F. (1999) · Psychiatry Research · doi:10.1016/s0165-1781(99)00013-x · Cited by 195 · see citing works
Kovács, K. A., Steullet, P., Steinmann, M., Kim, Q., Magistretti, P. J., Halfon, O., & Cardinaux, J. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0607524104 · Cited by 179 · see citing works
What can animal aggression research tell us about human aggression?
Blanchard, D. C., & Blanchard, R. J. (2003) · Hormones and Behavior · doi:10.1016/s0018-506x(03)00133-8 · Cited by 172 · see citing works
Mielcarek, M., Landles, C., Weiss, A., Bradaia, A., Seredenina, T., Inuabasi, L., Osborne, G. F., Wadel, K., Touller, C., Butler, R., et al. (2013) · PLoS Biology · doi:10.1371/journal.pbio.1001717 · Cited by 172 · see citing works
Controlling the Proportion of False Positives in Multiple Dependent Tests
Fernando, R. L., Nettleton, D. S., Southey, B. R., Dekkers, J. C. M., Rothschild, M. F., & Soller, M. (2004) · Genetics · doi:10.1534/genetics.166.1.611 · Cited by 165 · see citing works
Colman, J. R., Baldwin, D. H., Johnson, L. L., & Scholz, N. L. (2008) · Aquatic Toxicology · doi:10.1016/j.aquatox.2008.12.001 · Cited by 161 · see citing works
Coccaro, E., Kavoussi, R., Berman, M., & Lish, J. D. (1998) · Comprehensive Psychiatry · doi:10.1016/s0010-440x(98)90050-5 · Cited by 156 · see citing works
Norton, W., Stumpenhorst, K., Faus-Keßler, T., Folchert, A., Rohner, N., Harris, M. P., Callebert, J., & Bally‐Cuif, L. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.2892-11.2011 · Cited by 154 · see citing works
Blader, J. C., Schooler, N. R., Jensen, P. S., Pliszka, S. R., & Kafantaris, V. (2009) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2009.09020233 · Cited by 149 · cited 7× · see citing works
“geriatrics and in patients with acquired brain-injury [Horne and Lindley, 1995; Wilcox, 1994; Wroblewski et al., 1997; Ruedrich et al., 1999; Hollander et al., 2003; DelBello et al., 2004; Barzman et al., 2005; Barzman et al., 2006; Blader et al., 2009; Bidzan et al., 2012].”
BackgroundInfluentialHaller, J., Tóth, M., Halász, J., & de Boer, S. F. (2006) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.03.030 · Cited by 148 · see citing works
Genetics of aggressive behavior: An overview
Veroude, K., Zhang‐James, Y., Fernàndez‐Castillo, N., Bakker, M. J., Cormand, B., & Faraone, S. V. (2016) · American Journal of Medical Genetics Part B: Neuropsychiatric Genetics · doi:10.1002/ajmg.b.32364 · Cited by 147 · see citing works
Histamine in Neurotransmission and Brain Diseases
Nuutinen, S., & Panula, P. (2010) · Advances in experimental medicine and biology · doi:10.1007/978-1-4419-8056-4_10 · Cited by 141 · see citing works
cFOS and pCREB activation and maternal aggression in mice
Gammie, S. C., & Nelson, R. J. (2001) · Brain Research · doi:10.1016/s0006-8993(01)02189-8 · Cited by 131 · see citing works
Examination of behavioral deficits triggered by targeting BDNF in fetal or postnatal brains of mice
Chan, J., Unger, T. J., BYRNES, J. J., & Rios, M. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.06.002 · Cited by 125 · see citing works
Kent, L., Green, E., Hawi, Z., Kirley, A., Dudbridge, F., Lowe, N., Raybould, R., Langley, K., Bray, N., Fitzgerald, M., et al. (2005) · Molecular Psychiatry · doi:10.1038/sj.mp.4001696 · Cited by 125 · see citing works
Wroblewski, B. A., Joseph, A. B., Kupfer, J., & KALLIEL, K. (1997) · Brain Injury · doi:10.1080/026990597123791 · Cited by 118 · see citing works
Taylor, D. M., Moser, R., Régulier, E., Breuillaud, L., Dixon, M. A., Beesen, A. A., Elliston, L., Santos, M. D. F. S., Kim, J., Jones, L., et al. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.4965-11.2013 · Cited by 116 · see citing works
Oliveira, R. F., Simões, J. M., Teles, M. C., Oliveira, C. R., Becker, J. D., & Lopes, J. S. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1514292113 · Cited by 113 · see citing works
Trainor, B. C., Greiwe, K. M., & Nelson, R. J. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.04.002 · Cited by 106 · see citing works
Breuillaud, L., Rossetti, C., Meylan, E. M., Mérinat, C., Halfon, O., Magistretti, P. J., & Cardinaux, J. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.04.011 · Cited by 98 · see citing works
Forero, D. A., Arboleda, G., Vásquez, R., & Arboleda, H. (2009) · Journal of Psychiatry and Neuroscience · doi:10.1139/jpn.0947 · Cited by 89 · see citing works
BDNF restricted knockout mice as an animal model for aggression
Ito, W., Chehab, M., Thakur, S., Li, J., & Morozov, A. (2011) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2010.00676.x · Cited by 87 · see citing works
Unraveling the Genetic Etiology of Adult Antisocial Behavior: A Genome-Wide Association Study
Tielbeek, J. J., Medland, S. E., Benyamin, B., Byrne, E. M., Heath, A. C., Madden, P. A. F., Martin, N. G., Wray, N. R., & Verweij, K. J. H. (2012) · PLoS ONE · doi:10.1371/journal.pone.0045086 · Cited by 86 · see citing works
Davidge, K. M., Atkinson, L., Douglas, L., Lee, V., Shapiro, S., Kennedy, J. L., & Beitchman, J. H. (2004) · Psychiatric Genetics · doi:10.1097/00041444-200409000-00004 · Cited by 84 · see citing works
Davis, E. S., & Marler, C. A. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.05.034 · Cited by 81 · see citing works
Aggression in male mice lacking functional estrogen receptor alpha.
Scordalakes, E. M., & Rissman, E. (2003) · Behavioral Neuroscience · doi:10.1037/0735-7044.117.1.38 · Cited by 80 · see citing works
Monoamine oxidase A gene is associated with borderline personality disorder
Ni, X., Sicard, T., Bulgin, N., Bismil, R., Chan, K., McMain, S., & Kennedy, J. L. (2007) · Psychiatric Genetics · doi:10.1097/ypg.0b013e328016831c · Cited by 79 · see citing works
Aggression in male mice lacking functional estrogen receptor alpha.
Scordalakes, E. M., & Rissman, E. F. (2003) · Behavioral Neuroscience · doi:10.1037//0735-7044.117.1.38 · Cited by 76 · see citing works
Barzman, D. H., DelBello, M. P., Adler, C. M., Stanford, K. E., & Strakowski, S. M. (2006) · Journal of Child and Adolescent Psychopharmacology · doi:10.1089/cap.2006.16.665 · Cited by 74 · see citing works
Sandnabba, N. K. (1996) · Behavior Genetics · doi:10.1007/bf02359752 · Cited by 74 · see citing works
BDNF Val66Met polymorphism is associated with aggressive behavior in schizophrenia
Spalletta, G., Morris, D. W., Angelucci, F., Rubino, I. A., Spoletini, I., Bria, P., Martinotti, G., Siracusano, A., Bonaviri, G., Bernardini, S., et al. (2010) · European Psychiatry · doi:10.1016/j.eurpsy.2009.10.008 · Cited by 72 · see citing works
Ruedrich, S., Swales, T. P., Fossaceca, C., Toliver, J., & Rutkowski, A. (1999) · Journal of Intellectual Disability Research · doi:10.1046/j.1365-2788.1999.00193.x · Cited by 71 · see citing works
Negative cross-talk between the human orphan nuclear receptor Nur77/NAK-1/TR3 and nuclear factor- B
Harant, H. (2004) · Nucleic Acids Research · doi:10.1093/nar/gkh856 · Cited by 69 · see citing works
Monuteaux, M. C., Biederman, J., Doyle, A. E., Mick, E. O., & Faraone, S. V. (2009) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/chi.0b013e3181a5661b · Cited by 69 · see citing works
A developmental-genetic analysis of aggressive behavior in mice. II. Cross-sex inheritance
Hood, K., & Cairns, R. B. (1988) · Behavior Genetics · doi:10.1007/bf01082312 · Cited by 67 · see citing works
Paruthiyil, S., Čvoro, A., Tagliaferri, M. A., Cohen, I. V., Shtivelman, E., & Leitman, D. C. (2010) · Breast Cancer Research and Treatment · doi:10.1007/s10549-010-1273-5 · Cited by 66 · see citing works
Sánchez‐Mora, C., Ribasés, M., Ramos‐Quiroga, J. A., Casas, M., Bosch, R., Boreatti‐Hümmer, A., Heine, M., Jacob, C., Lesch, K., Fasmer, O. B., et al. (2009) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.31008 · Cited by 66 · see citing works
Self-citationJones, L. J., & Norton, W. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.05.055 · Cited by 65 · see citing works
GENETIC AND SOCIAL CAUSES OF AGGRESSIVE BEHAVIOUR IN MICE
Lagerspetz, K. (1961) · Scandinavian Journal of Psychology · doi:10.1111/j.1467-9450.1961.tb01237.x · Cited by 63 · see citing works
Malki, K., Tosto, M. G., Jumabhoy, I., Lourdusamy, A., Sluyter, F., Craig, I., Uher, R., McGuffin, P., & Schalkwyk, L. C. (2013) · Pharmacogenomics · doi:10.2217/pgs.13.154 · Cited by 55 · see citing works
Self-citationSakata, K., & Duke, S. M. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.12.013 · Cited by 54 · see citing works
Horne, M. K., & Lindley, S. E. (1995) · PubMed · Cited by 53 · see citing works
Malki, K., Pain, O., Tosto, M. G., Rietz, E. D., Carboni, L., & Schalkwyk, L. C. (2015) · Translational Psychiatry · doi:10.1038/tp.2015.15 · Cited by 53 · see citing works
Self-citationLanktree, M. B., Squassina, A., Krinsky, M., Strauss, J., Jain, U., Macciardi, F. M., Kennedy, J. L., & Muglia, P. (2008) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.30723 · Cited by 53 · see citing works
Divalproex Sodium in the Treatment of Aggressive Behavior
WILCOX, J. A. (1994) · Annals of Clinical Psychiatry · doi:10.3109/10401239409148834 · Cited by 48 · see citing works
Aggression in non‐human vertebrates: Genetic mechanisms and molecular pathways
Freudenberg, F., Gutiérrez, H. C., Post, A. M., Reif, A., & Norton, W. (2015) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.32358 · Cited by 44 · see citing works
Kabelik, D., Kelly, A. M., & Goodson, J. L. (2009) · Neuropharmacology · doi:10.1016/j.neuropharm.2009.06.009 · Cited by 38 · see citing works
A Comparison of Divalproex and Oxcarbazepine in Aggressive Youth with Bipolar Disorder
MACMILLAN, C. M., KORNDÖRFER, S. R., Rao, S., Fleisher, C., Mezzacappa, E., & Gonzalez–Heydrich, J. (2006) · Journal of Psychiatric Practice · doi:10.1097/00131746-200607000-00003 · Cited by 36 · see citing works
Genes and Gene Networks Implicated in Aggression Related Behaviour
Malki, K., Pain, O., Du Rietz, E., Tosto, M. G., Paya-Cano, J., Sandnabba, K. N., de Boer, S., Schalkwyk, L. C., & Sluyter, F. (2014) · neurogenetics · doi:10.1007/s10048-014-0417-x · Cited by 33 · see citing works
Self-citationAndrogen response to social competition in a shoaling fish
Teles, M. C., & Oliveira, R. F. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.10.009 · Cited by 33 · see citing works
A Positive Feedback Mechanism That Regulates Expression of miR-9 during Neurogenesis
Davila, J., Goff, L. A., Ricupero, C. L., Camarillo, C., Oni, E. N., Swerdel, M. R., Toro-Ramos, A. J., Li, J., & Hart, R. P. (2014) · PLoS ONE · doi:10.1371/journal.pone.0094348 · Cited by 32 · see citing works
Divalproex for the Treatment of Aggression Associated with Adolescent Mania
DelBello, M. P., Adler, C. M., & Strakowski, S. M. (2004) · Journal of Child and Adolescent Psychopharmacology · doi:10.1089/1044546041649101 · Cited by 31 · see citing works
Karmakar, S., Foster, E. A., & Smith, C. L. (2008) · International Journal of Cancer · doi:10.1002/ijc.24133 · Cited by 30 · see citing works
NR4A1 enhances neural survival following oxygen and glucose deprivation: An in vitro study
Xiao, G., Sun, T., Songming, C., & Cao, Y. (2013) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2013.04.010 · Cited by 25 · see citing works
Barzman, D. H., McConville, B. J., Masterson, B. J., McElroy, S. L., Sethuraman, G., Moore, K., Kahwaty, A.-M., & Nelson, D. (2005) · Journal of Affective Disorders · doi:10.1016/j.jad.2005.08.006 · Cited by 22 · see citing works
Female-Specific Hypertension Loci on Rat Chromosome 13
Hoffman, M. J., Flister, M. J., Núñez, L., Xiao, B., Greene, A. S., Jacob, H. J., & Moreno, C. (2013) · Hypertension · doi:10.1161/hypertensionaha.113.01708 · Cited by 20 · see citing works
Irritable assault and variation in the COMT gene
Flory, J. D., Xu, K., New, A. S., Finch, T., Goldman, D. A., & Siever, L. J. (2007) · Psychiatric Genetics · doi:10.1097/ypg.0b013e3281c8f126 · Cited by 16 · see citing works
Comparative mRNA analysis of behavioral and genetic mouse models of aggression
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Self-citationBidzan, L., Grabowski, J., Dutczak, B., & Bidzan, M. (2012) · PubMed · Cited by 8 · see citing works
Wozniak, J. R. (2005) · Evidence-Based Mental Health · doi:10.1136/ebmh.8.3.78 · Cited by 2 · see citing works
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Zhang, Y., Tao, H., Shen, Y., Chen, Q., & Liu, Z. (2025) · Frontiers in Marine Science · doi:10.3389/fmars.2025.1578762 · Cited by 1 · see citing works
Romero‐Diaz, C., Xu, C., Campos, S. M., Herrmann, M. A., Kusumi, K., Hews, D. K., & Martins, E. P. (2021) · Genes Brain & Behavior · doi:10.1111/gbb.12753 · Cited by 1 · see citing works
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Haller, J. (2020) · Springer eBooks · doi:10.1007/978-3-030-46331-1_2 · Cited by 1 · see citing works
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Poleev, A. (2016) · PhilPapers (PhilPapers Foundation) · doi:10.5281/zenodo.664775
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Poleev, A. (2016) · SSRN Electronic Journal · doi:10.2139/ssrn.2857935
James, N. (2019) · Illinois Digital Environment for Access to Learning and Scholarship (University of Illinois at Urbana-Champaign)
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Reichmann, F., Pilic, J., Trajanoski, S., & Norton, W. (2022) · Figshare · doi:10.6084/m9.figshare.19696044
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- Authors
- Malki, K., Du Rietz, E., Crusio, W. E., Pain, O., Paya‐Cano, J., Karadaghi, R. L., Sluyter, F., de Boer, S. F., Sandnabba, K., Schalkwyk, L. C., Asherson, P., & Tosto, M. G.
- Affiliations
- King's College London (GB)
- King's College London Social, Genetic and Developmental Psychiatry Centre (MRC), Institute of Psychiatry, Psychology and Neuroscience United Kingdom
- Centre National de la Recherche Scientifique (FR)
- University of London (GB)
- Groningen Institute for Evolutionary LifeSciences (GELIFES) University of Groningen Groningen The Netherlands
- Åbo Akademi University (FI)
- University of Essex (GB)
- Corresponding author
- Malki, Karim
- Venue
- American Journal of Medical Genetics Part B: Neuropsychiatric Genetics
- Publisher
- Wiley
- Published
- 2016-04-19
- Volume
- 171
- Issue
- 6
- Pages
- 827-838
- ISSN
- 1552-4841 (ISSN-L)
- 1552-485X
- OpenAlex
- W2337364142
- Cited by
- 52
- References
- 96
- Citations by year
- 2026: 4 · 2025: 4 · 2024: 2 · 2022: 10 · 2021: 4 · 2020: 7 · 2019: 6 · 2018: 5 · 2017: 7 · 2016: 3
- FWCI
- 3.94
- Type
- journal article
- Language
- en
- Open access
- green
- research.rug.nl
- Licence
- Locations
- American Journal of Medical Genetics Part B Neuropsychiatric Genetics (publishedVersion)
- PubMed (publishedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (publishedVersion, other-oa)
- Open Access at Essex (University of Essex) (acceptedVersion)
- BIROn (Birkbeck, University of London) (submittedVersion)
- Research Portal (King's College London) (submittedVersion)
- Åbo Akademi University Research Portal (submittedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion, other-oa)
- Funders
- MRC Centre Grant (G9817803)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Zebrafish Biomedical Research Applications
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Keywords
- aggression, gene expression, cross-species comparison, prefrontal cortex, differentially expressed genes, gene networks, c-fos, MAPK signaling, HDAC4, valproic acid, brain-derived neurotrophic factor, FOS, MKP-1
- MeSH terms
- Aggression, Animals, Behavior, Animal, Disease Models, Animal, Social Behavior, Zebrafish, Genes, fos, Gene Expression Profiling, Mice, Gene Regulatory Networks, Transcriptome
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