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. 1995 Jul 15;486(Pt 2):373–384. doi: 10.1113/jphysiol.1995.sp020819

Stretch-induced enhancement of contractions in uterine smooth muscle of rats.

Y Kasai 1, O Tsutsumi 1, Y Taketani 1, M Endo 1, M Iino 1
PMCID: PMC1156528  PMID: 7473204

Abstract

1. We studied the effect of servo-controlled stretch of smooth muscle strips from rat uterus on tension and intracellular Ca2+ concentration ([Ca2+]i, using fura-2 as an indicator) at 30 degrees C. 2. When quiescent uterine muscle strips were stretched at a ramp time of 0.5 s by multiples of 5% of the resting muscle length (L0) up to 40%, forty-two out of sixty muscle strips responded with a transient active contraction and a [Ca2+]i increase. The minimum excursion of stretch required for contraction was 26.3 +/- 7.5% of L0 (mean +/- S.D.). The peak response had an all-or-none property and was almost independent of the duration of stretch. 3. Stretches of 30 or 35% of L0 induced contraction in most cases when rapidly applied in 0.2-0.5 s, but slowly applied stretch (ramp duration of 5-10 s) rarely induced contraction. 4. The stretch-induced response was inhibited by the removal of extracellular Ca2+ or by the addition of 10 nM nicardipine. However, it was unaffected by 1 microM tetrodotoxin, 1 microM atropine or by 10 microM cyclopiazonic acid, an inhibitor of Ca2+-ATPase in intracellular Ca2+ stores. 5. When a stretch of 15-35% of L0 was applied during the relaxation phase of 10 nM oxytocin-induced rhythmic contractions, the first contraction after the stretch occurred earlier than that expected from the control rhythm. However, the frequency of the subsequent rhythm returned to almost the control level even during continued application of stretch, although the half-width of rhythmic contractions was increased during stretch. 6. The present study demonstrates that stretch of uterine muscle induces a transient contraction due to Ca2+ influx, which is myogenic and dependent on the excursion and velocity of stretch. The all-or-none property of the stretch-induced contractions suggests initiation of Ca2+ spikes. Furthermore, stretch modulates the oxytocin-induced rhythmic contractions.

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Selected References

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  1. BULBRING E. Correlation between membrane potential, spike discharge and tension in smooth muscle. J Physiol. 1955 Apr 28;128(1):200–221. doi: 10.1113/jphysiol.1955.sp005299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. BURNSTOCK G., HOLMAN M. E., PROSSER C. L. Electrophysiology of smooth muscle. Physiol Rev. 1963 Jul;43:482–527. doi: 10.1152/physrev.1963.43.3.482. [DOI] [PubMed] [Google Scholar]
  3. BURNSTOCK G., PROSSER C. L. Responses of smooth muscles to quick stretch: relation of stretch to conduction. Am J Physiol. 1960 May;198:921–925. doi: 10.1152/ajplegacy.1960.198.5.921. [DOI] [PubMed] [Google Scholar]
  4. Berrier C., Coulombe A., Szabo I., Zoratti M., Ghazi A. Gadolinium ion inhibits loss of metabolites induced by osmotic shock and large stretch-activated channels in bacteria. Eur J Biochem. 1992 Jun 1;206(2):559–565. doi: 10.1111/j.1432-1033.1992.tb16960.x. [DOI] [PubMed] [Google Scholar]
  5. Clapp L. H., Vivaudou M. B., Walsh J. V., Jr, Singer J. J. Acetylcholine increases voltage-activated Ca2+ current in freshly dissociated smooth muscle cells. Proc Natl Acad Sci U S A. 1987 Apr;84(7):2092–2096. doi: 10.1073/pnas.84.7.2092. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cooper K. E., Tang J. M., Rae J. L., Eisenberg R. S. A cation channel in frog lens epithelia responsive to pressure and calcium. J Membr Biol. 1986;93(3):259–269. doi: 10.1007/BF01871180. [DOI] [PubMed] [Google Scholar]
  7. Csabina S., Bárány M., Bárány K. Stretch-induced myosin light chain phosphorylation in rat uterus. Arch Biochem Biophys. 1986 Sep;249(2):374–381. doi: 10.1016/0003-9861(86)90013-5. [DOI] [PubMed] [Google Scholar]
  8. Davis M. J., Donovitz J. A., Hood J. D. Stretch-activated single-channel and whole cell currents in vascular smooth muscle cells. Am J Physiol. 1992 Apr;262(4 Pt 1):C1083–C1088. doi: 10.1152/ajpcell.1992.262.4.C1083. [DOI] [PubMed] [Google Scholar]
  9. Guharay F., Sachs F. Stretch-activated single ion channel currents in tissue-cultured embryonic chick skeletal muscle. J Physiol. 1984 Jul;352:685–701. doi: 10.1113/jphysiol.1984.sp015317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hamill O. P., Lane J. W., McBride D. W., Jr Amiloride: a molecular probe for mechanosensitive channels. Trends Pharmacol Sci. 1992 Oct;13(10):373–376. doi: 10.1016/0165-6147(92)90115-m. [DOI] [PubMed] [Google Scholar]
  11. Hamill O. P., McBride D. W., Jr Rapid adaptation of single mechanosensitive channels in Xenopus oocytes. Proc Natl Acad Sci U S A. 1992 Aug 15;89(16):7462–7466. doi: 10.1073/pnas.89.16.7462. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hisada T., Ordway R. W., Kirber M. T., Singer J. J., Walsh J. V., Jr Hyperpolarization-activated cationic channels in smooth muscle cells are stretch sensitive. Pflugers Arch. 1991 Jan;417(5):493–499. doi: 10.1007/BF00370945. [DOI] [PubMed] [Google Scholar]
  13. Hudspeth A. J. The cellular basis of hearing: the biophysics of hair cells. Science. 1985 Nov 15;230(4727):745–752. doi: 10.1126/science.2414845. [DOI] [PubMed] [Google Scholar]
  14. Iino M. Tension responses of chemically skinned fibre bundles of the guinea-pig taenia caeci under varied ionic environments. J Physiol. 1981 Nov;320:449–467. doi: 10.1113/jphysiol.1981.sp013961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kasai Y., Iino M., Tsutsumi O., Taketani Y., Endo M. Effects of cyclopiazonic acid on rhythmic contractions in uterine smooth muscle bundles of the rat. Br J Pharmacol. 1994 Aug;112(4):1132–1136. doi: 10.1111/j.1476-5381.1994.tb13201.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kirber M. T., Walsh J. V., Jr, Singer J. J. Stretch-activated ion channels in smooth muscle: a mechanism for the initiation of stretch-induced contraction. Pflugers Arch. 1988 Sep;412(4):339–345. doi: 10.1007/BF01907549. [DOI] [PubMed] [Google Scholar]
  17. Kleinhaus A. L., Kao C. Y. Electrophysiological actions of oxytocin on the rabbit myometrium. J Gen Physiol. 1969 Jun;53(6):758–780. doi: 10.1085/jgp.53.6.758. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lacampagne A., Gannier F., Argibay J., Garnier D., Le Guennec J. Y. The stretch-activated ion channel blocker gadolinium also blocks L-type calcium channels in isolated ventricular myocytes of the guinea-pig. Biochim Biophys Acta. 1994 Apr 20;1191(1):205–208. doi: 10.1016/0005-2736(94)90250-x. [DOI] [PubMed] [Google Scholar]
  19. Langton P. D. Calcium channel currents recorded from isolated myocytes of rat basilar artery are stretch sensitive. J Physiol. 1993 Nov;471:1–11. doi: 10.1113/jphysiol.1993.sp019887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Meininger G. A., Davis M. J. Cellular mechanisms involved in the vascular myogenic response. Am J Physiol. 1992 Sep;263(3 Pt 2):H647–H659. doi: 10.1152/ajpheart.1992.263.3.H647. [DOI] [PubMed] [Google Scholar]
  21. Nakayama K., Tanaka Y. Stretch-induced contraction and Ca2+ mobilization in vascular smooth muscle. Biol Signals. 1993 Sep-Oct;2(5):241–252. doi: 10.1159/000109505. [DOI] [PubMed] [Google Scholar]
  22. Ohmori H. Mechanoelectrical transducer has discrete conductances in the chick vestibular hair cell. Proc Natl Acad Sci U S A. 1984 Mar;81(6):1888–1891. doi: 10.1073/pnas.81.6.1888. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Vivaudou M. B., Clapp L. H., Walsh J. V., Jr, Singer J. J. Regulation of one type of Ca2+ current in smooth muscle cells by diacylglycerol and acetylcholine. FASEB J. 1988 Jun;2(9):2497–2504. doi: 10.1096/fasebj.2.9.2453389. [DOI] [PubMed] [Google Scholar]
  24. Walsh J. V., Jr, Singer J. J. Calcium action potentials in single freshly isolated smooth muscle cells. Am J Physiol. 1980 Nov;239(5):C162–C174. doi: 10.1152/ajpcell.1980.239.5.C162. [DOI] [PubMed] [Google Scholar]
  25. Wellner M. C., Isenberg G. Properties of stretch-activated channels in myocytes from the guinea-pig urinary bladder. J Physiol. 1993 Jul;466:213–227. [PMC free article] [PubMed] [Google Scholar]
  26. Wellner M. C., Isenberg G. Stretch effects on whole-cell currents of guinea-pig urinary bladder myocytes. J Physiol. 1994 Nov 1;480(Pt 3):439–448. doi: 10.1113/jphysiol.1994.sp020373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Wray S. The effect of pregnancy and lactation on the mesometrium of the rat. J Physiol. 1983 Jul;340:525–533. doi: 10.1113/jphysiol.1983.sp014778. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Wray S. The role of mechanical and hormonal stimuli on uterine involution in the rat. J Physiol. 1982 Jul;328:1–9. doi: 10.1113/jphysiol.1982.sp014249. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Wray S. Uterine contraction and physiological mechanisms of modulation. Am J Physiol. 1993 Jan;264(1 Pt 1):C1–18. doi: 10.1152/ajpcell.1993.264.1.C1. [DOI] [PubMed] [Google Scholar]
  30. Yang X. C., Sachs F. Block of stretch-activated ion channels in Xenopus oocytes by gadolinium and calcium ions. Science. 1989 Feb 24;243(4894 Pt 1):1068–1071. doi: 10.1126/science.2466333. [DOI] [PubMed] [Google Scholar]

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