Electrical slow waves in the mouse oviduct are dependent on extracellular and intracellular calcium sources

Rose Ellen Dickson, Fiona C. Britton, Salah A. Baker, Grant W. Hennig, Christina M. Rollings, Kenton M. Sanders, Sean M. Ward

Research output: Contribution to journalArticle

12 Citations (Scopus)

Abstract

Spontaneous contractions of the myosalpinx are critical for oocyte transport along the oviduct. Slow waves, the electrical events that underlie myosalpinx contractions, are generated by a specialized network of pacemaker cells called oviduct interstitial cells of Cajal (ICC-OVI). The ionic basis of oviduct pacemaker activity is unknown. Intracellular recordings and Ca 2+ imaging were performed to examine the role of extracellular and intracellular Ca 2+ sources in slow wave generation. RT-PCR was performed to determine the transcriptional expression of Ca 2+ channels. Molecular studies revealed most isoforms of L- and T-type calcium channels (Cav1.2,1.3,1.4,3.1,3.2,3.3) were expressed in myosalpinx. Reduction of extracellular Ca 2+ concentration ([Ca 2+]o) resulted in the abolition of slow waves and myosalpinx contractions without significantly affecting resting membrane potential (RMP). Spontaneous Ca 2+ waves spread through ICC-OVI cells at a similar frequency to slow waves and were inhibited by reduced [Ca 2+] o. Nifedipine depolarized RMP and inhibited slow waves; however, pacemaker activity returned when the membrane was repolarized with reduced extracellular K + concentration ([K +] o). Ni 2+ also depolarized RMP but failed to block slow waves. The importance of ryanodine and inositol 1,4,5 trisphosphate-sensitive stores were examined using ryanodine, tetracaine, caffeine, and 2-aminoethyl diphenylborinate. Results suggest that although both stores are involved in regulation of slow wave frequency, neither are exclusively essential. The sarco/endoplasmic reticulum Ca 2+-ATPase (SERCA) pump inhibitor cyclopiazonic acid inhibited pacemaker activity and Ca 2+ waves suggesting that a functional SERCA pump is necessary for pacemaker activity. In conclusion, results from this study suggest that slow wave generation in the oviduct is voltage dependent, occurs in a membrane potential window, and is dependent on extracellular calcium and functional SERCA pumps.

Original languageEnglish (US)
JournalAmerican Journal of Physiology - Cell Physiology
Volume301
Issue number6
DOIs
StatePublished - Dec 2011
Externally publishedYes

Fingerprint

Oviducts
Membrane Potentials
Endoplasmic Reticulum
Calcium
Adenosine Triphosphatases
Ryanodine
T-Type Calcium Channels
Interstitial Cells of Cajal
Tetracaine
L-Type Calcium Channels
Inositol 1,4,5-Trisphosphate
Nifedipine
Caffeine
Oocytes
Protein Isoforms
Polymerase Chain Reaction
Membranes

Keywords

  • Interstitial cells of cajal
  • Oocyte transport
  • Smooth muscle

ASJC Scopus subject areas

  • Cell Biology
  • Physiology

Cite this

Electrical slow waves in the mouse oviduct are dependent on extracellular and intracellular calcium sources. / Dickson, Rose Ellen; Britton, Fiona C.; Baker, Salah A.; Hennig, Grant W.; Rollings, Christina M.; Sanders, Kenton M.; Ward, Sean M.

In: American Journal of Physiology - Cell Physiology, Vol. 301, No. 6, 12.2011.

Research output: Contribution to journalArticle

Dickson, Rose Ellen ; Britton, Fiona C. ; Baker, Salah A. ; Hennig, Grant W. ; Rollings, Christina M. ; Sanders, Kenton M. ; Ward, Sean M. / Electrical slow waves in the mouse oviduct are dependent on extracellular and intracellular calcium sources. In: American Journal of Physiology - Cell Physiology. 2011 ; Vol. 301, No. 6.
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AU - Rollings, Christina M.

AU - Sanders, Kenton M.

AU - Ward, Sean M.

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AB - Spontaneous contractions of the myosalpinx are critical for oocyte transport along the oviduct. Slow waves, the electrical events that underlie myosalpinx contractions, are generated by a specialized network of pacemaker cells called oviduct interstitial cells of Cajal (ICC-OVI). The ionic basis of oviduct pacemaker activity is unknown. Intracellular recordings and Ca 2+ imaging were performed to examine the role of extracellular and intracellular Ca 2+ sources in slow wave generation. RT-PCR was performed to determine the transcriptional expression of Ca 2+ channels. Molecular studies revealed most isoforms of L- and T-type calcium channels (Cav1.2,1.3,1.4,3.1,3.2,3.3) were expressed in myosalpinx. Reduction of extracellular Ca 2+ concentration ([Ca 2+]o) resulted in the abolition of slow waves and myosalpinx contractions without significantly affecting resting membrane potential (RMP). Spontaneous Ca 2+ waves spread through ICC-OVI cells at a similar frequency to slow waves and were inhibited by reduced [Ca 2+] o. Nifedipine depolarized RMP and inhibited slow waves; however, pacemaker activity returned when the membrane was repolarized with reduced extracellular K + concentration ([K +] o). Ni 2+ also depolarized RMP but failed to block slow waves. The importance of ryanodine and inositol 1,4,5 trisphosphate-sensitive stores were examined using ryanodine, tetracaine, caffeine, and 2-aminoethyl diphenylborinate. Results suggest that although both stores are involved in regulation of slow wave frequency, neither are exclusively essential. The sarco/endoplasmic reticulum Ca 2+-ATPase (SERCA) pump inhibitor cyclopiazonic acid inhibited pacemaker activity and Ca 2+ waves suggesting that a functional SERCA pump is necessary for pacemaker activity. In conclusion, results from this study suggest that slow wave generation in the oviduct is voltage dependent, occurs in a membrane potential window, and is dependent on extracellular calcium and functional SERCA pumps.

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