Transcriptional regulation of brain gene expression in response to a territorial intrusion.

Yibayiri O Sanogo, Mark Band, Charles Blatti, Saurabh Sinha, Alison M Bell
Author Information
  1. Yibayiri O Sanogo: Integrative Biology, University of Illinois, Urbana-Champaign, IL, USA.

Abstract

aggressive behaviour associated with territorial defence is widespread and has fitness consequences. However, excess aggression can interfere with other important biological functions such as immunity and energy homeostasis. How the expression of complex behaviours such as aggression is regulated in the brain has long intrigued ethologists, but has only recently become amenable for molecular dissection in non-model organisms. We investigated the transcriptomic response to territorial intrusion in four brain regions in breeding male threespined sticklebacks using expression microarrays and quantitative polymerase chain reaction (qPCR). Each region of the brain had a distinct genomic response to a territorial challenge. We identified a set of genes that were upregulated in the diencephalon and downregulated in the cerebellum and the brain stem. Cis-regulatory network analysis suggested transcription factors that regulated or co-regulated genes that were consistently regulated in all brain regions and others that regulated gene expression in opposing directions across brain regions. Our results support the hypothesis that territorial animals respond to social challenges via transcriptional regulation of genes in different brain regions. Finally, we found a remarkably close association between gene expression and aggressive behaviour at the individual level. This study sheds light on the molecular mechanisms in the brain that underlie the response to social challenges.

References

  1. Invert Neurosci. 2004 Oct;5(2):77-83 [PMID: 15378392]
  2. BMC Neurosci. 2011 Jan 26;12:15 [PMID: 21269499]
  3. News Physiol Sci. 1999 Dec;14:223-231 [PMID: 11390856]
  4. Horm Behav. 2012 Jan;61(1):140-6 [PMID: 22155114]
  5. Curr Biol. 2010 Dec 7;20(23):2124-30 [PMID: 21093265]
  6. Proc Biol Sci. 2008 Feb 22;275(1633):393-402 [PMID: 18055387]
  7. Neuroendocrinology. 2009;89(1):27-37 [PMID: 18758154]
  8. J Mol Biol. 1990 Apr 20;212(4):563-78 [PMID: 2329577]
  9. Breast Cancer Res Treat. 2010 Nov;124(2):585-91 [PMID: 20623181]
  10. Nat Neurosci. 2011 Jun;14(6):677-83 [PMID: 21613996]
  11. Mol Ecol. 2007 Nov;16(21):4419-21 [PMID: 17883391]
  12. Proc Natl Acad Sci U S A. 2011 Nov 1;108(44):18020-5 [PMID: 21960440]
  13. Eur J Pharmacol. 2011 Jun 11;660(1):181-7 [PMID: 21211522]
  14. Bioinformatics. 2003;19 Suppl 1:i292-301 [PMID: 12855472]
  15. Endocrinology. 2011 Feb;152(2):568-80 [PMID: 21123436]
  16. Proc Biol Sci. 2005 Aug 22;272(1573):1655-62 [PMID: 16087419]
  17. Integr Comp Biol. 2009 Oct;49(4):423-40 [PMID: 21665831]
  18. Science. 2009 Jan 23;323(5913):498-501 [PMID: 19164747]
  19. Neuroscience. 2006;137(1):37-49 [PMID: 16289586]
  20. PLoS One. 2011 Apr 05;6(4):e18181 [PMID: 21483679]
  21. BMC Bioinformatics. 2010 Jan 22;11:45 [PMID: 20096121]
  22. Ann N Y Acad Sci. 1999 Jun 29;877:242-57 [PMID: 10415653]
  23. J Neurosci. 2007 Mar 21;27(12):3295-304 [PMID: 17376990]
  24. J Exp Biol. 2008 Sep;211(Pt 18):3041-56 [PMID: 18775941]
  25. Proc Natl Acad Sci U S A. 2005 Apr 5;102(14):4935 [PMID: 15809445]
  26. PLoS Biol. 2005 Nov;3(11):e363 [PMID: 16216088]
  27. Nat Genet. 2006 Sep;38(9):1023-31 [PMID: 16906161]
  28. Endocrinology. 2012 Mar;153(3):1341-51 [PMID: 22166981]
  29. BMC Vet Res. 2010 Jun 16;6:34 [PMID: 20553618]
  30. Annu Rev Cell Dev Biol. 2010;26:581-603 [PMID: 19575671]
  31. Proc Natl Acad Sci U S A. 2012 Jun 26;109(26):E1801-10 [PMID: 22691501]
  32. Cell. 2010 Mar 5;140(5):744-52 [PMID: 20211142]
  33. Trends Ecol Evol. 2004 Jul;19(7):372-8 [PMID: 16701288]
  34. PLoS One. 2009 Dec 04;4(12):e8182 [PMID: 19997634]
  35. BMC Genomics. 2010 Sep 16;11:498 [PMID: 20846403]
  36. Mol Cell Biol. 1997 Nov;17(11):6673-82 [PMID: 9343431]
  37. Proc Biol Sci. 2008 Oct 22;275(1649):2393-402 [PMID: 18628117]
  38. Physiol Behav. 2007 May 16;91(1):15-25 [PMID: 17321556]
  39. Brain Behav Evol. 2011;77(4):270-85 [PMID: 21677424]
  40. J Neurosci Res. 2003 Dec 1;74(5):701-16 [PMID: 14635221]
  41. Science. 2011 Jul 15;333(6040):357-60 [PMID: 21764751]
  42. Horm Behav. 2005 Jun;48(1):11-22 [PMID: 15885690]
  43. PLoS Genet. 2006 Sep 15;2(9):e154 [PMID: 17044737]
  44. Bioinformatics. 2005 Aug 15;21(16):3439-40 [PMID: 16082012]
  45. Proc Natl Acad Sci U S A. 2006 Oct 31;103(44):16352-7 [PMID: 17065326]
  46. FEBS Lett. 2004 Aug 27;573(1-3):83-92 [PMID: 15327980]
  47. Neurobiol Learn Mem. 2000 Nov;74(3):185-216 [PMID: 11031127]
  48. Proc Natl Acad Sci U S A. 2009 Sep 8;106(36):15400-5 [PMID: 19706434]
  49. Genetics. 2011 Jan;187(1):157-69 [PMID: 20980240]
  50. Science. 2000 Jul 28;289(5479):586-90 [PMID: 10915614]
  51. J Comp Neurol. 2010 Aug 15;518(16):3302-26 [PMID: 20575061]

Grants

  1. R01 GM082937/NIGMS NIH HHS

MeSH Term

Animals
Brain
Gene Expression Profiling
Gene Expression Regulation
Gene Regulatory Networks
Male
Oligonucleotide Array Sequence Analysis
Smegmamorpha
Territoriality
Tissue Distribution
Transcription, Genetic

Word Cloud

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