Expression of trefoil factor 1 in the developing and adult rat ventral mesencephalon

PLoS One. 2013 Oct 7;8(10):e76592. doi: 10.1371/journal.pone.0076592. eCollection 2013.

Abstract

Trefoil factor 1 (TFF1) belongs to a family of secreted peptides with a characteristic tree-looped trefoil structure. TFFs are mainly expressed in the gastrointestinal tract where they play a critical role in the function of the mucosal barrier. TFF1 has been suggested as a neuropeptide, but not much is known about its expression and function in the central nervous system. We investigated the expression of TFF1 in the developing and adult rat midbrain. In the adult ventral mesencephalon, TFF1-immunoreactive (-ir) cells were predominantly found in the substantia nigra pars compacta (SNc), the ventral tegmental area (VTA) and in periaqueductal areas. While around 90% of the TFF1-ir cells in the SNc co-expressed tyrosine hydroxylase (TH), only a subpopulation of the TH-ir neurons expressed TFF1. Some TFF1-ir cells in the SNc co-expressed the calcium-binding proteins calbindin or calretinin and nearly all were NeuN-ir confirming a neuronal phenotype, which was supported by lack of co-localization with the astroglial marker glial fibrillary acidic protein (GFAP). Interestingly, at postnatal (P) day 7 and P14, a significantly higher proportion of TH-ir neurons in the SNc co-expressed TFF1 as compared to P21. In contrast, the proportion of TFF1-ir cells expressing TH remained unchanged during postnatal development. Furthermore, significantly more TH-ir neurons expressed TFF1 in the SNc, compared to the VTA at all four time-points investigated. Injection of the tracer fluorogold into the striatum of adult rats resulted in retrograde labeling of several TFF1 expressing cells in the SNc showing that a significant fraction of the TFF1-ir cells were projection neurons. This was also reflected by unilateral loss of TFF1-ir cells in SNc of 6-hydroxylase-lesioned hemiparkinsonian rats. In conclusion, we show for the first time that distinct subpopulations of midbrain dopaminergic neurons express TFF1, and that this expression pattern is altered in a rat model of Parkinson's disease.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Female
  • Immunohistochemistry
  • Mesencephalon / cytology
  • Mesencephalon / growth & development
  • Mesencephalon / metabolism*
  • Microscopy, Fluorescence
  • Peptides / metabolism*
  • Rats
  • Rats, Wistar
  • Substantia Nigra / cytology
  • Substantia Nigra / growth & development
  • Substantia Nigra / metabolism
  • Time Factors
  • Trefoil Factor-1
  • Tyrosine 3-Monooxygenase / metabolism
  • Ventral Tegmental Area / cytology
  • Ventral Tegmental Area / growth & development
  • Ventral Tegmental Area / metabolism

Substances

  • Peptides
  • Tff1 protein, mouse
  • Trefoil Factor-1
  • Tyrosine 3-Monooxygenase

Grants and funding

This research was supported by the Danish Parkinson Association, the Danish Medical Research Council (J. No. 271-07-0582), the Danish Centre for Stem Cell Research (www.dasc.dk), Hørslev Fonden, IMK Almene Fond, Familien Hede Nielsens Fond, Augustinus Fonden, Fonden til Lægevidenskabens Fremme, Lægeforeningens Forskningsfond and the Swiss National Science Foundation (Contract No. 3100A0-112529 and 31003A_135565). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.