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Physiology of myometrial function: intercellular coupling and its role in uterine contractility

Published online by Cambridge University Press:  10 October 2008

TN Tabb
Affiliation:
University of Texas Medical Branch, Galveston, Texas, USA
RE Garfield*
Affiliation:
University of Texas Medical Branch, Galveston, Texas, USA
G Thilander
Affiliation:
University of Texas Medical Branch, Galveston, Texas, USA
*
Dr Robert E Garfield, Department of Obstetrics and Gynecology, University of Texas Medical Branch, Galveston, Texas 77555, USA.

Extract

The mammalian uterus is composed of a preponderance of small smooth muscle cells usually aligned in two layers. The number of muscle cells in the human uterus at term is estimated at 200 billion, each minute fusiform cell measuring about 5–10μm in diameter and about 200μm in length. The main function of the uterus is to harbour the developing fetus during pregnancy and then to contract vigorously during labour to expel the products of conception. In order for the uterus to contract rhythmically and forcefully, a mechanism must exist to allow interaction between muscle cells in order to achieve synchronous activity. Phasic or cyclical patterns of contractile activity of the uterus cannot be accounted for by stimulation or inhibition from the nervous or endocrine systems. Since myometrial cells are dependent upon action potentials for their contractile processes, some system must be present between the muscle cells for the propagation of action potentials between them. The observation that gap junctions occur in large numbers between myometrial cells during parturition is thought to be significant in this regard and they are considered to play an essential role in parturition and in the control and co-ordination of uterine contractility. In this brief review, we will discuss the role of gap junctions in the modulation of myometrial contractility and the mechanisms that regulate their synthesis and permeability.

Type
Articles
Copyright
Copyright © Cambridge University Press 1991

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References

1Garfield, RE. Myometrial ultrastructure and uterine contractility. In: Bottari, S, Thomas, JP, Vokaer, A, Vokaer, R eds. Uterine contractility. New York: Masson Publishing, 1984: 81109.Google Scholar
2Csapo, AI. Force of labor. In: Iffy, L, Kamientzky, HA eds. Principles and practice of obstetrics and perinatology. New York: John Wiley and Sons, 1981: 761–99.Google Scholar
3Garfield, RE, Beier, S. Increased myometrial responsiveness to oxytocin during term and preterm labor. Am J Obstet Gynec 1989; 161: 454–61.CrossRefGoogle ScholarPubMed
4Marshall, JM. Regulation of activity in uterine smooth muscle. Physiol Rev 1962; 42: 213–27.Google Scholar
5Marshall, JM. The physiology of the uterus. In: Norris, HJ, Hertig, AT, Abell, MR eds. The uterus. Baltimore: Williams and Wilkins, 1973: 89109.Google Scholar
6Kao, CY. Electrophysiological properties of uterine smooth muscle. In: Wynn, RM, Jollie, WP eds. Biology of the uterus, second edition. New York: Plenum Publishing, 1989: 403–54.CrossRefGoogle Scholar
7Kuriyama, H. Recent studies on the electrophysiology of the uterus. In: Ciba Foundation Study Group. Progesterone and the defence mechanism of pregnancy, volume 9. Boston: Little, Brown, 1961: 5170.Google Scholar
8Kuriyama, H. Excitation-contraction coupling in various visceral smooth muscles. In: Bulbring, E, Brading, AF, Jones, AW, Tomita, T eds. Smooth muscle: an assessment of current knowledge. London: Edward Arnold, 1981: 171–97.Google Scholar
9Abe, Y. The hormonal control and the effects of drugs and ions on the electrical and mechanical activity of the uterus. In: Bulbring, E, Brading, AF, Jones, AW, Tomita, T eds. Smooth muscle: an assessment of current knowledge. London: Edward Arnold, 1970: 396417.Google Scholar
10Bozler, E. Electrical stimulation and conduction of excitation in smooth muscle. Am J Physiol 1938; 122: 616–23.CrossRefGoogle Scholar
11Bozler, E. Influence of estrone on the electric characteristics and motility of uterine muscle. Endocrinology 1941; 29: 225–27.CrossRefGoogle Scholar
12Marshall, JM. Effects of estrogen and progesterone on single uterine muscle fibres in the rat. Am J Physiol 1959; 197: 935–42.CrossRefGoogle ScholarPubMed
13Csapo, AI. Defence mechanism of pregnancy. In: Ciba Foundation Study Group. Progesterone and the defence mechanism of pregnancy, Volume 9. Boston: Little, Brown, 1961: 127.Google Scholar
14Carsten, ME. Regulation of myometrial composition, growth and activity. In: Assali, NS ed. Biology of the uterus, Volume 1. New York: Academic Press, 1968: 355423.Google Scholar
15Csapo, AI, Kuriyama, H. Effects of ions and drugs on cell membrane activity and tension in the postpartum rat myometrium. J Physiol (Lond) 1963; 165: 575–92.CrossRefGoogle ScholarPubMed
16Mironneau, J. Relationship between contraction and transmembrane ionic current in voltage-clamped uterine smooth muscle. In: Bulbring, E, Shuba, MF eds. Physiology of smooth muscle. New York: Raven Press, 1976: 175–83.Google ScholarPubMed
17Mironneau, J, Savineau, J-P. Effects of calcium ions on outward membrane currents in rat uterine smooth muscle. J Physiol (Lond) 1980; 302: 411–25.CrossRefGoogle ScholarPubMed
18Osa, T. An interaction between the electrical activities of longitudinal and circular smooth muscles of pregnant mouse uterus. Jpn J Physiol 1974; 24: 189203.CrossRefGoogle ScholarPubMed
19Osa, T, Ogasawara, T, Kato, S. Effects of magnesium, oxytocin and prostaglandin F on the generation and propagation of excitation in the longitudinal muscle of rat myometrium during late pregnancy. Jpn J Physiol 1983; 33: 5167.CrossRefGoogle Scholar
20Saldivar, JT, Melton, CE. Effects in vivo and in vitro of sex steroids on rat myometrium. Am J Physiol 1966; 211: 835–43.CrossRefGoogle ScholarPubMed
21Furshpan, EJ, Potter, DD. Transmission at the giant motor synapses of the crayfish. J Physiol (Lond) 1959; 145: 289325.CrossRefGoogle ScholarPubMed
22Revel, J-P, Karnovsky, M. Hexagonal array of subunits in intercellular junctions of the mouse heart and liver. J Cell Biol 1967; 33: C712.CrossRefGoogle ScholarPubMed
23Hooper, ML, Subak-Sharpe, JH. Metabolic cooperation between cells. Int Rev Cytol 1981; 69: 45104.CrossRefGoogle ScholarPubMed
24Larsen, WJ. Biological implications of gap junction structure, distribution and composition: a review. Tissue Cell 1983; 15: 645–71.CrossRefGoogle ScholarPubMed
25McNutt, NS, Weinstein, RS. The ultrastructure of the nexus. A correlated thin section and freeze-cleave study. J Cell Biol 1970; 47: 666–88.CrossRefGoogle Scholar
26Peracchia, C. Structural correlates of gap junction permeation. Int Rev Cytol 1980; 66: 81146.CrossRefGoogle ScholarPubMed
27Pitts, JD, Finbow, ME. The gap junction. J Cell Sci [Suppl] 1986; 4: 239–66.CrossRefGoogle ScholarPubMed
28Revel, J-P, Nicholson, BJ, Yancey, SB. Chemistry of gap junctions. Ann Rev Physiol 1985; 47: 263–79.CrossRefGoogle ScholarPubMed
29Spray, DC, Bennett, MVL. Physiology and pharmacology of gap junctions. Am J Physiol 1985; 47: 281303.Google ScholarPubMed
30Meda, P, Merrelet, A, Orci, L. Increase of gap junctions between pancreatic B-cells during stimulation of insulin secretion. J Cell Biol 1979; 82: 441–48.CrossRefGoogle ScholarPubMed
31Fallon, RF, Goodenough, DA. Five hour half-life of mouse liver gap junction protein. J Cell Biol 1981; 90: 521–26.CrossRefGoogle ScholarPubMed
32Saez, JC, Connor, JA, Spray, DC, Bennett, MVL. Hepatocyte gap junctions are permeable to the second messenger, inositol 1,4,5-trisphosphate, and to calcium ions. Proc Natl Acad Sci USA 1988; 86: 2708–12.CrossRefGoogle Scholar
33Kam, E, Melville, L, Pitts, JD. Patterns of junctional communication in skin. J Invest Dermatol 1986; 87: 748–63.CrossRefGoogle ScholarPubMed
34Garfield, RE, Sims, S, Daniel, EE. Gap junctions: their presence and necessity in myometrium during gestation. Science 1977; 198: 958–60.CrossRefGoogle Scholar
35Garfield, RE, Sims, SM, Kannan, MS, Daniel, EE. Possible role of gap junctions in activation of myometrium during parturition. Am J Physiol 1978; 235: C16879.CrossRefGoogle ScholarPubMed
36Garfield, RE, Merrett, D, Grover, AK. Gap junction formation and regulation in myometrium. Am J Physiol 1980; 239: C21728.CrossRefGoogle ScholarPubMed
37Garfield, RE, Hayashi, RH. Appearance of gap junctions in the myometrium of women during labor. Am J Obstet Gynecol 1981; 140: 254–60.CrossRefGoogle ScholarPubMed
38Garfield, RE, Puri, CP, Csapo, AI. Endocrine, structural and functional changes in the uterus during premature labor. Am J Obstet Gynecol 1982; 142: 2127.CrossRefGoogle ScholarPubMed
39Garfield, RE, Baulieu, EE. The antiprogesterone steroid RU486: a short pharmacological and clinical review with emphasis on the interruption of pregnancy. Baillieres Clin Endocrinol Metab 1987; 1: 207–21.CrossRefGoogle Scholar
40Cole, WC, Garfield, RE, Kirkaldy, JS. Gap junctions and direct intercellular communication between rat uterine smooth muscle cells. Am J Physiol 1985; 249: C2031.CrossRefGoogle ScholarPubMed
41Cole, WC, Garfield, RE. Evidence for physiological regulation of gap junction permeability. Am J Physiol 1986; 251: C41120.CrossRefGoogle ScholarPubMed
42Demianczuk, N, Towell, M, Garfield, RE. Myometrial electrophysiologic activity and gap junctions in the pregnant rabbit. Am J Obstet Gynecol 1984; 149: 485–91.CrossRefGoogle ScholarPubMed
43Garfield, RE, Blennerhassett, MG, Miller, SM. Control of myometrial contractility: role and regulation of gap junctions. Oxf Rev Report Biol 1988; 10: 436–90.Google ScholarPubMed
44Puri, CP, Garfield, RE. Changes in hormone levels and gap junctions in the rat uterus during pregnancy and parturition. Biol Reprod 1982; 27: 967–75.Google ScholarPubMed
45Sims, SM, Daniel, EE, Garfield, RG. Improved electrical coupling in uterine smooth muscle is associated with increased gap junctions at parturition. J Gen Physiol 1982; 80: 353–75.CrossRefGoogle ScholarPubMed
46Miller, SM, Garfield, RE, Daniel, EE. Improved propagation in myometrium associated with gap junctions during parturition. Am J Physiol 1989; 256: C13041.CrossRefGoogle ScholarPubMed
47Garfield, RE. Effects of antiprogesterone compounds on uterine contractility. Proceedings of the symposium on hormone antagonists for fertility regulation. Bombay Indian Society for the Study of Reproduction and Fertility and the World Health Organization’s Special Programme of Research, Development and Research Training in Human Reproduction, 1988: 6385.Google Scholar
48Fuchs, A-R. Hormonal control of myometrial function during pregnancy and parturition. Acta Endocrinol [Suppl] (Copenh) 1978; 221: 170.Google ScholarPubMed
49Challis, JRG, Lye, SJ. Parturition. In: Clarke, JR ed. Oxf Rev Reprod Biol 1986; 8: 61129.Google Scholar
50Casey, ML, MacDonald, PC. Initiation of labor in women. In: Huszar, G ed. The physiology and biochemistry of the uterus in pregnancy and labor. Boca Raton: CRC Press Inc, 1986: 155–61.Google Scholar
51Grody, WW, Schrader, WT, O’Malley, BW. Activation, transformation, and subunit structure of steroid hormone receptors. Endocr Rev 1982; 3: 141–63.CrossRefGoogle ScholarPubMed
52Dahl, G, Azarina, R, Werner, R. De novo construction of cell-to-cell channels. In Vitro Cell Dev Biol 1980; 16: 1068–75.Google ScholarPubMed
53Gorski, J, Gannon, F. Current models of steroid hormone action: a critique. Ann Rev Physiol 1976; 38: 425–50.CrossRefGoogle Scholar
54MacKenzie, LW, Garfield, RE. Hormonal control of gap junctions in the myometrium. Am J Physiol 1985; 248: C296308.CrossRefGoogle ScholarPubMed
55MacKenzie, LW, Puri, CP, Garfield, RE. Effect of estradiol-17β and prostaglandins on rat myometrial gap junctions. Prostaglandins 1983; 26: 925–41.CrossRefGoogle ScholarPubMed
56Garfield, RE, Kannan, MS, Daniel, EE. Gap junction formation in myometrium: control by estrogens, progesterone and prostaglandins. Am J Physiol 1980; 238: C8189.CrossRefGoogle ScholarPubMed
57Paul, DL. Molecular cloning of cDNA for rat liver gap junction protein. J Cell Biol 1986; 103: 123–34.CrossRefGoogle ScholarPubMed
58Beyer, EC, Paul, DL, Goodenough, DA. Connexin 43: a protein from rat heart homologous to a gap junction protein from liver. J Cell Biol 1987; 105: 2621–29.CrossRefGoogle Scholar
59Beyer, EC, Kistler, J, Paul, DL, Goodenough, DA. Antisera directed against connexin 43 peptides react with a 43-dk protein localized to gap junctions in myocardium and other tissues. J Cell Biol 1989; 108: 595605.CrossRefGoogle Scholar
60Garfield, RE, Hertzberg, E. Cell-to-cell coupling in the myometrium: Emil Bozher’s Prediction. In: Sperelakis, N, Wood, JD eds. Frontiers in smooth muscle research. Alan R Liss: New York, 1990: 673–81.Google Scholar
61Risek, B, Guthrie, S, Kumar, N, Gilula, NB. Modulation of gap junction transcript and protein expression during pregnancy in the rat. J Cell Biol 1990; 110: 269–82.CrossRefGoogle ScholarPubMed
62Crow, DS, Beyer, EC, Paul, DL, Kobe, SS, Lau, AF. Phosphorylation of connexin 43 gap junction protein in un-infected and Rous Sarcoma Virus-transformed mammalian fibroblasts. Mol Cell Biol 1990; 10: 1754–63.Google Scholar
63Laird, DW, Puranam, KL, Revel, J-P. Turnover and phosphorylation dynamics of connexin 43 gap junction protein in cultured cardiac myocytes. Biochem J 1991; 273: 6772.CrossRefGoogle Scholar
64Musil, LS, Beyer, EC, Goodenough, DA. Expression of the gap junction protein in embryonic chick lens: molecular cloning, ultrastructural localization and post-transitional phosphorylation. J Membr Biol 1991; 116: 163–75.CrossRefGoogle Scholar
65Garfield, RE, Cole, WC, Blennerhassett, MG. Gap junctions in uterine smooth muscle. In: Sperelakis, N, Cole, WC eds. Cell interactions and gap junctions. Boca Raton: CRC Press Inc, 1989; 239–66.Google Scholar
66Edwards, E, Good, DM, Granger, SE et al. The spasmogenic action of oxytocin in the rat uterus – comparison with other agonists. Br J Pharmacol 1986; 88: 899908.CrossRefGoogle ScholarPubMed