A computational model of the ionic currents, ca2+ dynamics and action potentials underlying contraction of isolated uterine smooth muscle

PLoS ONE

Volumn 6, Issue 4, 2011, Pages

  Tong, Wing Chiu ^a,b   Choi, Cecilia Y ^b   Karche, Sanjay ^b   Holden, Arun V ^c   Zhang, Henggui ^b   Taggart, Michael J ^a,b  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); CALCIUM ACTIVATED POTASSIUM CHANNEL; CALCIUM CHANNEL L TYPE; CALCIUM CHANNEL T TYPE; CALCIUM ION; CATION CHANNEL; CHLORIDE CHANNEL; CHLORIDE ION; ESTRADIOL; POTASSIUM ION; SODIUM CALCIUM EXCHANGE PROTEIN; SODIUM ION; VOLTAGE GATED POTASSIUM CHANNEL; CALCIUM; CALCIUM CHANNEL; POTASSIUM; SODIUM;

ARTICLE; CALCIUM CELL LEVEL; CALCIUM CURRENT; CALCIUM TRANSPORT; CONTROLLED STUDY; ELECTRIC POTENTIAL; ELECTROPHYSIOLOGY; EXCITATION CONTRACTION COUPLING; HYPERPOLARIZATION; ION CURRENT; MATHEMATICAL MODEL; MUSCLE ACTION POTENTIAL; MUSCLE FIBER MEMBRANE CONDUCTANCE; MYOMETRIUM; POTASSIUM CURRENT; SMOOTH MUSCLE CONTRACTION; SODIUM CURRENT; VALIDATION STUDY; VOLTAGE CLAMP; ACTION POTENTIAL; BIOLOGY; BIOPHYSICS; CELL MEMBRANE POTENTIAL; CHEMISTRY; FEMALE; HUMAN; METHODOLOGY; PATHOLOGY; PHYSIOLOGY; PREGNANCY; THEORETICAL MODEL; UTERUS CONTRACTION;

ACTION POTENTIALS; BIOPHYSICS; CALCIUM; CALCIUM CHANNELS; COMPUTATIONAL BIOLOGY; FEMALE; HUMANS; MEMBRANE POTENTIALS; MODELS, THEORETICAL; MYOMETRIUM; POTASSIUM; PREGNANCY; SODIUM; UTERINE CONTRACTION;

EID: 79955722767     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0018685     Document Type: Article

References (113)

1. Landa J, West TC, (1956) Transmembrane potentials and contractility in the pregnant rat uterus. Am J Physiol 187: 333-337.
2. Landa JF, West TC, Thiersch JB, (1959) Relationships between contraction and membrane electrical activity in the isolated uterus of the pregnant rat. Am J Physiol 196: 905-909.
3. Csapo IA, Kuriyama HA, (1963) Effects of ions and drugs on cell membrane activity and tension in the postpartum rat myometrium. J Physiol 165: 575-592.
4. Garfield RE, Maner WL, (2007) Physiology and electrical activity of uterine contractions. Semin Cell Dev Biol 18: 289-295.
5. Taggart MJ, Morgan KG, (2007) Regulation of the uterine contractile apparatus and cytoskeleton. Semin Cell Dev Biol 18: 296-304.
6. Goldenberg RL, Culhane JF, Iams JD, Romero R, (2008) Epidemiology and causes of preterm birth. Lancet 371: 75-84.
7. Bugg GJ, Stanley E, Baker PN, Taggart MJ, Johnston TA, (2006) Outcomes of labours augmented with oxytocin. Eur J Obstet Gynecol Reprod Biol 124: 37-41.
8. Parkington HC, Tonta MA, Davies NK, Brennecke SP, Coleman HA, (1999) Hyperpolarization and slowing of the rate of contraction in human uterus in pregnancy by prostaglandins E2 and F2α: Involvement of the Na+ pump. J Physiol 514 (Pt 1): 229-243.
9. Taggart MJ, Tribe RM, (2007) Cellular ionic mechanisms controlling uterine smooth muscle contraction: effects of gestational state. In: Savinneau JP, editors. New Frontiers in Smooth Muscle Biology and Physiology India Research Signpost pp. 523-549 ISBN: 9788178952956.
10. Wilde DW, Marshall JM, (1988) Effects of tetraethylammonium and 4-aminopyridine on the plateau potential of circular myometrium from the pregnant rat. Biol Reprod 38: 836-845.
11. Inoue Y, Okabe K, Soeda H, (1999) Augmentation and suppression of action potentials by estradiol in the myometrium of pregnant rat. Can J Physiol Pharmacol 77: 447-453.
12. Shmigol AV, Eisner DA, Wray S, (1998) Properties of voltage-activated [Ca2+]i transients in, single smooth muscle cells isolated from pregnant rat uterus. J Physiol 511: 803-811.
13. Blanks AM, Zhao ZH, Shmygol A, Bru-Mercier G, Astle S, et al. (2007) Characterization of the molecular and electrophysiological properties of the T-type calcium channel in human myometrium. J Physiol 581: 915-926.
14. Sperelakis N, Inoue Y, Ohya Y, (1992) Fast Na+ channels and slow Ca2+ current in smooth muscle from pregnant rat uterus. Mol Cell Biochem 114: 79-89.
15. Jones K, Shmygol A, Kupittayanant S, Wray S, (2004) Electrophysiological characterization and functional importance of calcium-activated chloride channel in rat uterine myocytes. Pflugers Arch 448: 36-43.
16. Khan RN, Smith SK, Morrison JJ, Ashford ML, (1993) Properties of large-conductance K+ channels in human myometrium during pregnancy and labour. Proc Biol Sci 251: 9-15.
17. Wang SY, Yoshino M, Sui JL, Wakui M, Kao PN, et al. (1998) Potassium currents in freshly dissociated uterine myocytes from nonpregnant and late-pregnant rats. J Gen Physiol 112: 737-756.
18. Knock GA, Aaronson PI, (1999) Calcium antagonistic properties of the cyclooxygenase-2 inhibitor nimesulide in human myometrial myocytes. Br J Pharmacol 127: 1470-1478.
19. Knock GA, Smirnov SV, Aaronson PI, (1999) Voltage-gated K+ currents in freshly isolated myocytes of, the pregnant human myometrium. J Physiol 518: 769-781.
20. Noble K, Floyd R, Shmygol A, Shmygol A, Mobasheri A, et al. (2010) Distribution, expression and functional effects of small conductance Ca-activated potassium (SK) channels in rat myometrium. Cell Calcium 47: 47-54.
21. Floyd RV, Wray S, Quenby S, Martin-Vasallo P, Mobasheri A, (2010) Expression and distribution of Na, K-ATPase isoforms in the human uterus. Reprod Sci 17: 366-376.
22. Grover AK, Kwan CY, Daniel EE, (1981) Na-Ca exchange in rat myometrium membrane vesicles highly enriched in plasma membranes. Am J Physiol 240: C175-82.
23. Taggart MJ, Blanks A, Kharche S, Holden A, Wang B, et al. (2007) Towards understanding the myometrial physiome: approaches for the construction of a virtual physiological uterus. BMC Pregnancy Childbirth 7 (Suppl 1): S3.
24. Bursztyn L, Eytan O, Jaffa AJ, Elad D, (2007) Mathematical model of excitation-contraction in a uterine smooth muscle cell. Am J Physiol cell Physiol 292: 1816-1829.
25. Rihana S, Terrien J, Germain G, Marque C, (2009) Mathematical modeling of electrical activity of uterine muscle cells. Med Biol Eng Comput 47: 665-675.
26. Jmari K, Mironneau C, Mironneau J, (1986) Inactivation of calcium channel current in rat uterine smooth muscle: evidence for calcium- and voltage-mediated mechanisms. J Physiol 380: 111-126.
27. Miyoshi H, Urabe T, Fujiwara A, (1991) Electrophysiological properties of membrane currents in single myometrial, cells isolated from pregnant rats. Pflugers Arch 419: 386-393.
28. Young RC, Smith LH, McLaren MD, (1993) T-type and L-type calcium currents in freshly dispersed human uterine smooth muscle cells. Am J Obstet Gynecol 169: 785-792.
29. Amedee T, Mironneau C, Mironneau J, (1987) The calcium channel current of pregnant rat single myometrial cells, in short-term primary culture. J Physiol 392: 253-272.
30. Yamamoto T, (1995) Effects of estrogens on Ca channels in myometrial cells isolated from pregnant rats. Am J Physiol 268: C64-9.
31. Mcdonald TF, Pelzer S, Trautwein W, Pelzer DJ, (1994) Regulation and modulation of calcium channels in cardiac, skeletal, and smooth muscle cells. Physiol Rev 74: 365-507.
32. Okabe K, Inoue Y, Soeda H, (1999) Estradiol inhibits Ca2+ and K+ channels in smooth muscle cells from pregnant rat myometrium. Eur J Pharmacol 376: 101-108.
33. Yoshino M, Wang SY, Kao CY, (1997) Sodium and calcium inward currents in freshly dissociated smooth myocytes of rat uterus. J Gen Physiol 110: 565-577.
34. Inoue Y, Sperelakis N, (1991) Gestational change in Na+ and Ca2+ channel current densities, in rat myometrial smooth muscle cells. Am J Physiol 260: C658-63.
35. Kusaka M, Sperelakis N, (1995) Inhibition of L-type calcium current by genistein, a tyrosine kinase inhibitor, in pregnant rat myometrial cells. Biochim Biophys Acta 1240: 196-200.
36. Greenwood IA, Large WA, (1996) Analysis of the time course of calcium-activated chloride 'tail' currents in rabbit portal vein smooth muscle cells. Pflugers Arch 432: 970-979.
37. Parkington HC, Coleman HA, (2001) Excitability in uterine smooth muscle. Front Horm Res 27: 179-200.
38. Mershon JL, Mikala G, Schwartz A, (1994) Changes in the expression of the L-type voltage-dependent calcium channel during pregnancy and parturition in the rat. Biol Reprod 51: 993-1002.
39. Tezuka N, Ali M, Chwalisz K, Garfield RE, (1995) Changes in transcripts encoding calcium channel subunits of rat myometrium during pregnancy. Am J Physiol 269: C1008-17.
40. Ohkubo T, Kawarabayashi T, Inoue Y, Kitamura K, (2005) Differential expression of L- and T-type calcium channels between, longitudinal and circular muscles of the rat myometrium during pregnancy. Gynecol Obstet Invest 59: 80-85.
41. Helguera G, Olcese R, Song M, Toro L, Stefani E, (2002) Tissue-specific regulation of Ca2+ channel protein expression by sex hormones. Biochim Biophys Acta 1569: 59-66.
42. Ohya Y, Sperelakis N, (1989) Fast Na+ and slow Ca2+ channels in single uterine muscle cells from pregnant rats. Am J Physiol 257: C408-12.
43. Serrano JR, Perez-Reyes E, Jones SW, (1999) State-dependent inactivation of the alpha1G T-type calcium channel. J Gen Physiol 114: 185-201.
44. Hering J, Feltz A, Lambert RC, (2003) Slow inactivation of the Cav3.1 isotype of T-type calcium channels. J Physiol 555: 331-344.
45. Asokan KT, Sarkar SN, Mishra SK, Raviprakash V, (2002) Effects of mibefradil on uterine contractility. Eur J Pharmacol 455: 65-71.
46. Lee SE, Ahn DS, Lee YH, (2009) Role of T-type Ca channels in the spontaneous phasic contraction of pregnant rat uterine smooth muscle. Korean J Physiol Pharmacol 13: 241-249.
47. Inoue Y, Nakao K, Okabe K, Izumi H, Kanda S, et al. (1990) Some electrical properties of human pregnant myometrium. Am J Obstet Gynecol 162: 1090-1098.
48. Satoh H, (1995) Identification of a hyperpolarization-activated inward current in uterine smooth muscle cells during pregnancy. Gen Pharmacol 26: 1335-1338.
49. Okabe K, Inoue Y, Kawarabayashi T, Kajiya H, Okamoto F, et al. (1999) Physiological significance of hyperpolarization-activated inward currents (ih) in smooth muscle cells from the circular layers of pregnant rat myometrium. Pflugers Arch 439: 76-85.
50. Shannon TR, Wang F, Puglisi J, Weber C, Bers DM, (2004) A mathematical treatment of integrated Ca dynamics within the ventricular myocyte. Biophys J 87: 3351-3371.
51. Knock GA, Tribe RM, Hassoni AA, Aaronson PI, (2001) Modulation of potassium current characteristics in human myometrial smooth muscle by 17beta-estradiol and progesterone. Biol Reprod 64: 1526-1534.
52. Erulkar SD, Rendt J, Nori RD, Ger B, (1994) The influence of 17 beta-oestradiol on K+ currents in smooth muscle cells isolated from immature rat uterus. Proc Biol Sci 256: 59-65.
53. Piedras-Renteria E, Stefani E, Toro L, (1991) Potassium currents in freshly dispersed myometrial cells. Am J Physiol 261: C278-84.
54. Anwer K, Toro L, Oberti C, Stefani E, Sanborn BM, (1992) Ca2+-activated K+ channels in pregnant rat myometrium: modulation by a beta-adrenergic agent. Am J Physiol 263: C1049-56.
55. Anwer K, Oberti C, Perez GJ, Perez-Reyes N, Mcdougall JK, et al. (1993) Calcium-activated K+ channels as modulators of human myometrial contractile activity. Am J Physiol 265: C976-85.
56. Perez GJ, Toro L, Erulkar SD, Stefani E, (1993) Characterization of large-conductance, calcium-activated potassium channels from human myometrium. Am J Obstet Gynecol 168: 652-660.
57. Song M, Zhu N, Olcese R, Barila B, Toro L, et al. (1999) Hormonal control of protein expression and mRNA levels of the MaxiK channel alpha subunit in myometrium. FEBS Lett 460: 427-432.
58. Zhou XB, Wang GX, Ruth P, Huneke B, Korth M, (2000) BK(Ca) channel activation by membrane-associated cGMP kinase may contribute to uterine quiescence in pregnancy. Am J Physiol Cell Physiol 279: C1751-9.
59. Matharoo-Ball B, Ashford MLJ, Arulkumaran S, Khan RN, (2003) Down-regulation of the alpha- and beta-subunits of the calcium-activated potassium channel in human myometrium with parturition. Biol Reprod 68: 2135-2141.
60. Curley M, Morrison JJ, Smith TJ, (2004) Analysis of maxi-K alpha subunit splice variants in human myometrium. Reprod Biol Endocrinol 2: 67.
61. Khan RN, Smith SK, Ashford ML, (1998) Contribution of calcium-sensitive potassium channels to NS1619-induced relaxation in human pregnant myometrium. Hum Reprod 13: 208-213.
62. Khan RN, Matharoo-Ball B, Arulkumaran S, Ashford ML, (2001) Potassium channels in the human myometrium. Exp Physiol 86: 255-264.
63. Bao L, Cox DH, (2005) Gating and ionic currents reveal how the BK(Ca) channel's Ca2+ sensitivity is enhanced by its beta1 subunit. J Gen Physiol 12: 393-412.
64. Orio P, Torres Y, Rojas P, Carvacho I, Garcia ML, et al. (2006) Structural determinants for functional coupling between the beta and alpha subunits in the Ca2+-activated K+ (BK) channel. J Gen Physiol 127: 191-204.
65. Benkusky NA, Fergus DJ, Zucchero TM, England SK, (2000) Regulation of the Ca2+-sensitive domains of the maxi-K channel in the mouse myometrium during gestation. J Biol Chem 275: 27712-27719.
66. Zhou XB, Wang GX, Huneke B, Wieland T, Korth M, (2000) Pregnancy switches adrenergic signal transduction in rat and human uterine myocytes as probed by BKCa channel activity. J Physiol 524: 339-352.
67. Shmigol A, Eisner DA, Wray S, (1998) Carboxyeosin decreases the rate of decay of the [Ca2+]i, transient in uterine smooth muscle cells isolated from pregnant rats. Pflugers Arch 437: 158-160.
68. Brown A, Cornwell T, Korniyenko I, Solodushko V, Bond CT, et al. (2007) Myometrial expression of small conductance Ca2+-activated K+ channels depresses phasic uterine contraction. Am J Physiol Cell Physiol 292: C832-C840.
69. Smith RC, McClure MC, Smith MA, Abel PW, Bradley ME, (2007) The role of voltage-gated potassium channels in the regulation of mouse uterine contractility. Reprod Biol Endocrinol 5: 41.
70. Pierce SL, Kresowik JDK, Lamping KG, England SK, (2008) Overexpression of SK3 channels dampens uterine contractility to prevent preterm labor in mice. Biol Reprod 78: 1058-1063.
71. McCallum LA, Pierce SL, England SK, Greenwood IA, Tribe RM, (2011) The contribution of Kv7 channels to pregnant mouse and human myometrial contractility. J Cell Mol Med 15: 577-86.
72. Coleman HA, Parkington HC, (1987) Single channel Cl- and K+ currents from cells of uterus not treated with enzymes. Pflugers Arch 410: 560-562.
73. Mironneau J, Arnaudeau S, Macrez-Lepretre N, Boittin FX, (1996) Ca2+ sparks and Ca2+ waves activate different Ca2+-dependent ion channels in single myocytes from rat portal vein. Cell Calcium 20: 153-160.
74. Young RC, Bemis A, (2009) Calcium-activated chloride currents prolongs the duration of contractions in pregnant rat myometrial tissue. Reprod Sci 16: 734-739.
75. Jeong JW, Lee KY, Lydon JP, DeMayo FJ, (2006) Steroid hormone regulation of Clca3 expression in the murine uterus. J Endocrinol 189: 473-484.
76. Song J, Zhang X, Qi Z, Sun G, Chi S, et al. (2009) Cloning and characterization of a calcium-activated chloride channel in rat uterus. Biol Reprod 80: 788-794.
77. Arreola J, Melvin JE, Begenisich T, (1996) Activation of calcium-dependent chloride channels in rat parotid acinar cells. J Gen Physiol 108: 35-47.
78. Angermann JE, Sanguinetti AR, Kenyon JL, Leblanc N, Greenwood IA, (2006) Mechanism of the inhibition of Ca2+-activated Cl- currents by phosphorylation in pulmonary arterial smooth muscle cells. J Gen Physiol 128: 73-87.
79. Miyoshi H, Yamaoka K, Garfield RE, Ohama K, (2004) Identification of a non-selective cation channel current in myometrial cells isolated from pregnant rats. Pflugers Arch 447: 457-464.
80. Chang DC, (1983) Dependence of cellular potential on ionic concentrations. data supporting a modification of the constant field equation. Biophys J 43: 149-156.
81. Manabe K, Takano M, Noma A, (1995) Non-selective cation current of guinea-pig endocardial endothelial cells. J Physiol 487: 407-419.
82. Taylor GS, Paton DM, Daniel EE, (1969) Evidence for an electrogenic sodium pump in smooth muscle. Life Sci 8: 769-773.
83. Taylor GS, Paton DM, Daniel EE, (1970) Characteristics of electrogenic sodium pumping in rat myometrium. J Gen Physiol 56: 360-375.
84. Turi A, Marcsek Z, Mullner N, Kucsera M, Bori Z, (1992) The activity of Na+/K+-ATPase and abundance of its mRNA are regulated in rat myometrium during pregnancy. Biochem Biophys Res Commun 188: 1191-1198.
85. Esplin MS, Fausett MB, Faux DS, Graves SW, (2003) Changes in the isoforms of the sodium pump in the placenta and myometrium of women in labor. Am J Obstet Gynecol 188: 759-764.
86. Vance CJ, Esplin MS, Hamblin S, Graves SW, (2006) Alterations in uterine sodium pump abundance may contribute to the onset and progression of term and preterm labor in mice. Am J Obstet Gynecol 195: 1407-1414.
87. Nakao M, Gadsby DC, (1989) [Na] and [K] dependence of the Na/K pump current-voltage relationship in guinea pig ventricular myocytes. J Gen Physiol 94: 539-565.
88. Nakamura Y, Ohya Y, Abe I, Fujishima M, (1999) Sodium-potassium pump current in smooth muscle cells from mesenteric resistance arteries of the guinea-pig. J Physiol 519: 203-212.
89. Taggart MJ, Wray S, (1997) Agonist mobilization of sarcoplasmic reticular calcium in smooth muscle: Functional coupling to the plasmalemmal Na+/Ca2+ exchanger? Cell Calcium 22: 333-341.
90. Shmigol AV, Eisner DA, Wray S, (1999) The role of the sarcoplasmic reticulum as a Ca2+ sink in rat uterine smooth muscle cells. J Physiol 520 Pt 1: 153-163.
91. Weber CR, Ginsburg KS, Philipson KD, Shannon TR, Bers DM, (2001) Allosteric regulation of Na/Ca exchange current by cytosolic Ca in intact cardiac myocytes. J Gen Physiol 117: 119-131.
92. Abe Y, (1971) Effects of changing the ionic environment on passive and active membrane properties of pregnant rat uterus. J Physiol 214: 173-190.
93. Quednau BD, Nicoll DA, Philipson KD, (1997) Tissue specificity and alternative splicing of the Na+/Ca2+ exchanger isoforms NCX1, NCX2, and NCX3 in rat. Am J Physiol Cell Physiol 272: C1250-1261.
94. Levitsky DO, (2007) Three types of muscles express three sodium-calcium exchanger isoforms. Ann NY Acad Sci 1099: 221-225.
95. Li Z, Matsuoka S, Hryshko LV, Nicoll DA, Bersohn MM, et al. (1994) Cloning of the NCX2 isoform of the plasma membrane Na+-Ca2+ exchanger. J Biol Chem 269: 17434-17439.
96. Iwamoto T, Shigekawa M, (1998) Differential inhibition of Na+/Ca2+ exchanger isoforms by divalent cations and isothiourea derivative. Am J Physiol 275: C423-30.
97. Linck B, Qiu Z, He Z, Tong Q, Hilgemann DW, et al. (1998) Functional comparison of the three isoforms of the Na+/Ca2+ exchanger (NCX1, NCX2, NCX3). Am J Physiol 274: C415-23.
98. Campbell DL, Giles WR, Robinson K, Shibata EF, (1988) Studies of the sodium-calcium exchanger in bull-frog atrial myocytes. J Physiol 403: 317-340.
99. Vigne P, Breittmayer JP, Duval D, Frelin C, Lazdunski M, (1988) The Na+/Ca2+ antiporter in aortic smooth muscle cells. J Biol Chem 263: 8078-8083.
100. Mollard P, Mironneau J, Amedee T, Mironneau C, (1986) Electrophysiological characterization of single pregnant rat myometrial cells in short-term primary culture. Am J Physiol 250: C47-54.
101. Bengtsson B, Chow EM, Marshall JM, (1984) Activity of circular muscle of rat uterus at different times in pregnancy. Am J Physiol 246: C216-23.
102. Meisheri KD, Mcneill JH, Marshall JM, (1979) Effect of isoproterenol on the isolated pregnant rat myometrium. Eur J Pharmacol 60: 1-6.
103. Burdyga T, Wray S, Noble K, (2007) In situ calcium signaling. no calcium sparks detected in rat myometrium. Ann N Y Acad Sci 1101: 85-96.
104. Burdyga T, Borisova L, Burdyga AT, Wray S, (2009) Temporal and spatial variations in spontaneous Ca events and mechanical activity in pregnant rat myometrium. Eur J Obstet Gynecol Reprod Biol 144 (Suppl 1): S25-S32.
105. Kawarabayashi T, (1994) Electrophysiology of the human myometrium. In: Chard T, Grudzinskas JG, editors. The Uterus Cambridge, UK Cambridge University Press, Cambridge Reviews in Human Reproduction, chapter 7 pp. 148-172.
106. Mankouri HW, Burdyga T, Taggart MJ, Wray S, (1998) Simultaneous measurements of electrical activity, intracellular calcium and contraction in smooth muscle. J Physiol 509.P: 2P-3P.
107. Zhang J, Taggart M, Thornton S, Shmygol A, Blanks AM, (2010) The pregnancy dependent expression profile of the genomic complement of K channels in human myometrial smooth muscle and vasculature. Reprod Sci 17: 78A.
108. Lammers WJEP, Mirghani H, Stephen B, Dhanasekaran S, Wahab A, et al. (2008) Patterns of electrical propagation in the intact pregnant guinea pig uterus. Am J Physiol Regul Integr Comp Physiol 294: R919-R928.
109. Mitchell BF, Taggart MJ, (2009) Are animal models relevant to key aspects of human parturition? Am J Physiol Regul Integr Comp Physiol 297: R525-R545.
110. Kamishima T, Mccarron JG, (1996) Depolarization-evoked increases in cytosolic calcium concentration in isolated smooth muscle cells of rat portal vein. J Physiol 492 (Pt 1): 61-74.
111. Standen NB, Stanfield PR, (1982) A binding-site model for calcium channel inactivation that depends on calcium entry. Proc R Soc Lond B Biol Sci 217: 101-110.
112. Crichton CA, Taggart MJ, Wray S, Smith GL, (1993) Effects of pH and inorganic phosphate on force production in alpha-toxin-permeabilized isolated rat uterine smooth muscle. J Physiol 465: 629-645.
113. Ermentrout GB, (2002) Simulating, analyzing, and animating dynamical systems: a guide to XPPAUT for researchers and students Philadelphia, US Society for Industrial and Applied Mathematics.