Differences in the expression of transient receptor potential channel V1, transient receptor potential channel A1 and mechanosensitive two pore-domain K+ channels between the lumbar splanchnic and pelvic nerve innervations of mouse urinary bladder and colon

Neuroscience. 2011 Jul 14:186:179-87. doi: 10.1016/j.neuroscience.2011.04.049. Epub 2011 Apr 30.

Abstract

The bladder and distal colon are innervated by lumbar splanchnic (LSN) and pelvic nerves (PN) whose axons arise from dorsal root ganglia (DRG) neurons at thoracolumbar (TL) and lumbosacral (LS) spinal levels, respectively. In an attempt to understand the molecular basis of differences between LSN and PN mechanosensitive afferents, we analyzed the gene expression of two potentially counteracting ion channel groups involved in mechanosensation, transient receptor potential channels (TRPV1 and TRPA1) and mechanosensitive two pore-domain K(+) (K(2P)) channels (TREK-1, TREK-2 and TRAAK), in TL and LS DRG neurons innervating mouse bladder or distal colon. The proportion of TRPV1-expressing cells (41∼61%) did not differ between TL and LS neurons innervating bladder or colon. TRPA1 was seldom detected in bladder LS neurons whereas it was expressed in 64∼66% of bladder TL, colon TL and colon LS neurons. Coexpression of TRPV1 and TRPA1 was frequent. TREK-1-expressing cells were more prevalent in LS than TL ganglia in both bladder- and colon-DRG neurons. All three K(2P) channels were detected more frequently in TRPV1-positive neurons in TL ganglia. More than half of TL neurons expressing only TRPA1 were devoid of any of the three K(2P) channels, whereas all TL neurons expressing both TRPA1 and TRPV1 expressed at least one of the K(2P) channels. These results reveal clear differences between LSN and PN sensory pathways in TRPA1 and TREK-1 gene expression and in the gene expression of K(2P) channels in TRPV1-expressing neurons. This study further documents heterogeneity of visceral afferents based on combinations of the five channels examined.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Cells, Cultured
  • Colon / cytology
  • Colon / innervation*
  • Colon / metabolism
  • Hypogastric Plexus / cytology
  • Hypogastric Plexus / physiology*
  • Male
  • Mechanoreceptors / cytology
  • Mechanoreceptors / physiology*
  • Mechanotransduction, Cellular / physiology
  • Mice
  • Mice, Inbred C57BL
  • Neural Pathways / physiology
  • Potassium Channels, Tandem Pore Domain / biosynthesis*
  • Potassium Channels, Tandem Pore Domain / physiology
  • Splanchnic Nerves / cytology
  • Splanchnic Nerves / physiology*
  • TRPA1 Cation Channel
  • TRPV Cation Channels / biosynthesis*
  • TRPV Cation Channels / physiology
  • Transient Receptor Potential Channels / biosynthesis*
  • Transient Receptor Potential Channels / physiology
  • Urinary Bladder / cytology
  • Urinary Bladder / innervation*
  • Urinary Bladder / metabolism

Substances

  • Potassium Channels, Tandem Pore Domain
  • TRPA1 Cation Channel
  • TRPV Cation Channels
  • TRPV1 protein, mouse
  • Transient Receptor Potential Channels
  • Trpa1 protein, mouse