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An evolutionarily conserved pacemaker role for HCN ion channels in smooth muscle.

Lei Yang1, Rodolfo J Ricart Arbona2, Carl S Smith3

  • 1Department of Physiology and Biophysics, Weill Medical College of Cornell University, New York, NY, USA.

The Journal of Physiology
|March 17, 2023
PubMed
Summary

Hyperpolarization-activated cation (HCN) channels are confirmed as key pacemakers in smooth muscle, driving peristalsis in the upper urinary tract. This discovery clarifies their conserved role beyond the heart and suggests channelopathies as causes of smooth muscle disorders.

Keywords:
HCN channelsIh funny currentPDGFR-αpacemakersperistalsisrenal pelvissmooth muscle

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Area of Science:

  • Physiology
  • Ion Channel Biology
  • Smooth Muscle Physiology

Background:

  • Hyperpolarization-activated cation (HCN) ion channels are established cardiac pacemakers, but their function in smooth muscle remains debated.
  • Renal pelvic smooth muscle (RPSM) cells in the murine upper urinary tract contain HCN channels and are crucial for peristalsis.
  • Previous studies failed to detect the HCN (Ih) current in RPSM cells, questioning their pacemaker identity and the mechanisms in multicalyceal upper urinary tracts.

Purpose of the Study:

  • To investigate the role of HCN channels in renal pelvic smooth muscle (RPSM) pacemaker activity.
  • To identify the specific cell types responsible for pacemaker activity in the upper urinary tract.
  • To determine if HCN channels are conserved in the multicalyceal upper urinary tracts of humans and pigs.

Main Methods:

  • Immunopanning purification of HCN-expressing cells from murine renal pelvic smooth muscle.
  • Single-molecule super-resolution microscopy (STORM) and whole-tissue imaging.
  • Translational studies using homologous human and porcine upper urinary tracts.

Main Results:

  • 96% of purified HCN+ cells exhibited the Ih current, confirming their pacemaker potential.
  • HCN+ cells were found to integrate into the smooth muscle syncytium and express HCN channels on their plasma membrane.
  • Translational studies in humans and pigs confirmed HCN+ cells in calyceal RPSM, with HCN channel block abolishing pacemaker activity and peristalsis.

Conclusions:

  • HCN ion channels play a conserved pacemaker role in both cardiac and smooth muscle organs.
  • HCN+ cells are the bona fide pacemakers in the renal pelvic smooth muscle of the upper urinary tract.
  • Channelopathies affecting HCN channels are potential causes of smooth muscle dysfunction.