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Selection for stress-induced analgesia affects the mouse hippocampal transcriptome

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Abstract

Stress responsiveness, including pain sensitivity and stress-induced analgesia (SIA), depends on genotype and, partially, is mediated by hippocampus. The present study examined differences in constitutive gene expression in hippocampus in lines of mice bred for high (HA) and low (LA) swim SIA. Between the lines, we found 1.5-fold or greater differences in expression of 205 genes in the hippocampus in nonstressed animals. The identity of these genes indicates that selective breeding for swim SIA affected many aspects of hippocampal neurons physiology, including metabolism, structural changes, and cellular signaling. Genes involved in calcium signaling pathway, including Slc8a1, Slc8a2, Prkcc, and Ptk2b, were upregulated in LA mice. In HA mice, robust upregulation of genes coding some transcription factors (Klf5) or receptors for neurotensin (Ntsr2) and GABA (Gabard) suggests the genetic basis for a novel mechanism of the non-opioid type of SIA in HA animals. Additional groups of differentially expressed genes represented functional networks involved in carbohydrate metabolism, gene expression regulation, and molecular transport. Our data indicate that selection for a single and very specific stress response trait, swim SIA, alters hippocampal gene expression. The results suggest that individual stress responsiveness may be associated with characteristics of the constitutive hippocampal transcriptome.

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Abbreviations

cDNA:

complementary DNA

cRNA:

complementary RNA

E:

real-time PCR efficiency

EASE:

expression analysis systemic explorer

GABA:

γ-Aminobutyric acid

GABAA/B:

γ-Aminobutyric acid receptors

HA:

line of mice selected for high swim stress-induced analgesia

IEGs:

immediate early genes

IPA:

ingenuity pathway analysis

KLF5:

Krueppel-like factor 5

LA:

line of mice selected for low swim stress-induced analgesia

MAP:

mitogen-activated protein

NF:

normalization factor

NMDA:

N-metylo-d-asparaginian

NT:

neurotensin

qRT:

quantitative real time

R:

relative expression ratio

SIA:

stress-induced analgesia

TF:

transcription factor

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Acknowledgments

The authors would like to thank the European Commission Framework 6 Integrated Project NEWMOOD (LSHMCT-2004-503474); Intramural Statutory Funds S.VI-2 and 4, and the Polish Scientific Committee Grant N N311 604938.

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Authors and Affiliations

  1. Department of Molecular Biology, Institute of Genetics and Animal Breeding, Polish Academy of Sciences, Jastrzebiec, Poland

    Pawel Lisowski & Lech Zwierzchowski

  2. Department of Animal Behavior, Institute of Genetics and Animal Breeding, Polish Academy of Sciences, Jastrzebiec, Poland

    Adrian M. Stankiewicz & Artur H. Swiergiel

  3. Department of Software Engineering, Faculty of Computer Science, Bialystok University of Technology, Bialystok, Poland

    Joanna Goscik

  4. Department of Neurophysiology, University of Lodz, Lodz, Poland

    Marek Wieczorek

  5. Department of Animal Physiology, University of Gdansk, Gdansk, Poland

    Artur H. Swiergiel

  6. Department of Pharmacology, Toxicology and Neuroscience, Louisiana State University Health Science Center, Shreveport, LA, USA

    Artur H. Swiergiel

  7. Centre for Experimental Medicine, Medical University of Bialystok, Bialystok, Poland

    Joanna Goscik

Authors
  1. Pawel Lisowski
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  2. Adrian M. Stankiewicz
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  5. Lech Zwierzchowski
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  6. Artur H. Swiergiel
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Correspondence to Pawel Lisowski.

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Supplementary Figure S1

Gene network graphical representation. Gene networks represent molecular relationships between genes or the genes’ products: a carbohydrate metabolism, small molecule biochemistry and energy production gene network; b gene expression and cell death gene network; c molecular transport gene network; d cellular function and maintenance gene network. Genes or gene products are represented as nodes, and the biological relationship between two nodes is represented as an edge (line). All edges are supported by at least one reference from the literature, from a textbook, or from canonical information stored in the Ingenuity® knowledge database. Human, mouse, and rat orthologs of a gene are stored as separate objects in Ingenuity® knowledge database, but are represented as a single node in the network. The intensity of the node color indicates the degree of downregulation (red) in high analgesia mice (HA) or upregulation (green) in HA. Nodes are displayed using various shapes that represent the functional class of gene product (JPEG 125 kb)

Supplementary Figure S1A

JPEG 206 kb

Supplementary Figure S1B

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Supplementary Figure S1C

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Supplementary Figure S1D

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Supplementary Table S1

XLS 148 kb

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Lisowski, P., Stankiewicz, A.M., Goscik, J. et al. Selection for stress-induced analgesia affects the mouse hippocampal transcriptome. J Mol Neurosci 47, 101–112 (2012). https://doi.org/10.1007/s12031-011-9692-2

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  • DOI: https://doi.org/10.1007/s12031-011-9692-2

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