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Myosalpinx Contractions Are Essential for Egg Transport Along the Oviduct and Are Disrupted in Reproductive Tract Diseases

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Smooth Muscle Spontaneous Activity

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1124))

Abstract

Oviducts (also called fallopian tubes) are smooth muscle-lined tubular organs that at one end extend in a trumpet bell-like fashion to surround the ovary, and at the other connect to the uterus. Contractions of the oviduct smooth muscle (myosalpinx) and the wafting motion of the ciliated epithelium that lines these tubes facilitate bidirectional transport of gametes so that newly released ovum(s) are transported in one direction (pro-uterus) while spermatozoa are transported in the opposite direction (pro-ovary). These transport processes must be temporally coordinated so that the ovum and spermatozoa meet in the ampulla, the site of fertilization. Once fertilized, the early embryo begins another precisely timed journey towards the uterus for implantation. Myosalpinx contractions facilitate this journey too, while luminal secretions from secretory epithelial cells aid early embryo maturation.

The previous paradigm was that oviduct transport processes were primarily controlled by fluid currents generated by the incessant beat of the ciliated epithelium towards the uterus. More recently, video imaging and spatiotemporal mapping have suggested a novel paradigm in which ovum/embryo transport is highly dependent upon phasic and propulsive contractions of the myosalpinx. A specialized population of pacemaker cells, termed oviduct interstitial cells of Cajal (ICC-OVI), generate the electrical activity that drives these contractions. The ionic mechanisms underlying this pacemaker activity are dependent upon the calcium-activated chloride conductance, Ano1.

This chapter discusses the basis of oviduct pacemaker activity, its hormonal regulation, and the underlying mechanisms and repercussions when this activity becomes disrupted during inflammatory responses to bacterial infections, such as Chlamydia.

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Notes

  1. 1.

    As an aside point, the term “salpinx” which is often used to refer to the oviducts is derived from the name of a Greek trumpetlike instrument with a shape strongly resembling that of a human oviduct.

References

  1. Cook MJ. The anatomy of the laboratory mouse, vol. 143. London: Academic Press; 1965.

    Google Scholar 

  2. Nilsson O, Reinius S. Light and electron microscopic structure of the oviduct. In: Hafez ESE, Blandau RJ, Washington State University, editors. The mammalian oviduct comparative biology and methodology. Chicago, IL: University of Chicago Press; 1969. p. 57–83.

    Google Scholar 

  3. Eddy CA, Pauerstein CJ. Anatomy and physiology of the fallopian tube. Clin Obstet Gynecol. 1980;23(4):1177–93.

    Article  CAS  PubMed  Google Scholar 

  4. Blandau RJ. Gamete transport—comparative aspects. In: Hafez ESE, Blandau RJ, Washington State University, editors. The mammalian oviduct comparative biology and methodology. Chicago, IL: University of Chicago Press; 1969. p. 129–62.

    Google Scholar 

  5. Paton DM, Widdicombe JH, Rheaume DE, Johns A. The role of the adrenergic innervation of the oviduct in the regulation of mammalian ovum transport. Pharmacol Rev. 1977;29(2):67–102.

    CAS  PubMed  Google Scholar 

  6. Croxatto HB. Physiology of gamete and embryo transport through the fallopian tube. Reprod Biomed Online. 2002;4(2):160–9.

    Article  CAS  PubMed  Google Scholar 

  7. Hafez ESE, Black DL. The mammalian uterotubal junction. In: Hafez ESE, Blandau RJ, Washington State University, editors. The mammalian oviduct comparative biology and methodology. Chicago, IL: University of Chicago Press; 1969. p. 105–6.

    Google Scholar 

  8. Foster HL, Small JD, Fox JG. The mouse in biomedical research, American College of Laboratory Animal Medicine series, vol. 4. New York: Academic Press; 1981.

    Google Scholar 

  9. Ezzati M, Djahanbakhch O, Arian S, Carr BR. Tubal transport of gametes and embryos: a review of physiology and pathophysiology. J Assist Reprod Genet. 2014;31(10):1337–47. https://doi.org/10.1007/s10815-014-0309-x.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Faussone-Pellegrini MS, Bani G. The muscle coat morphology of the mouse oviduct during the estrous cycle. Arch Histol Cytol. 1990;53(2):167–78.

    Article  CAS  PubMed  Google Scholar 

  11. Abe H. The mammalian oviductal epithelium: regional variations in cytological and functional aspects of the oviductal secretory cells. Histol Histopathol. 1996;11(3):743–68.

    CAS  PubMed  Google Scholar 

  12. Lyons RA, Saridogan E, Djahanbakhch O. The reproductive significance of human Fallopian tube cilia. Hum Reprod Update. 2006;12(4):363–72.

    Article  CAS  PubMed  Google Scholar 

  13. Amso NN, Crow J, Lewin J, Shaw RW. A comparative morphological and ultrastructural study of endometrial gland and fallopian tube epithelia at different stages of the menstrual cycle and the menopause. Hum Reprod. 1994;9(12):2234–41.

    Article  CAS  PubMed  Google Scholar 

  14. Crow J, Amso NN, Lewin J, Shaw RW. Morphology and ultrastructure of fallopian tube epithelium at different stages of the menstrual cycle and menopause. Hum Reprod. 1994;9(12):2224–33.

    Article  CAS  PubMed  Google Scholar 

  15. Dirksen ER, Satir P. Ciliary activity in the mouse oviduct as studied by transmission and scanning electron microscopy. Tissue Cell. 1972;4(3):389–403.

    Article  CAS  PubMed  Google Scholar 

  16. Patek E. The epithelium of the human Fallopian tube. A surface ultrastructural and cytochemical study. Acta Obstet Gynecol Scand Suppl. 1974;31:1–28.

    CAS  PubMed  Google Scholar 

  17. Croxatto HB, Villalon M. Oocyte transport. In: Grudzinskas JG, Yovich J, editors. Gametes the oocyte. Cambridge reviews in human reproduction. Cambridge: Cambridge University Press; 1995. p. 253–76.

    Google Scholar 

  18. Leese HJ, Tay JI, Reischl J, Downing SJ. Formation of Fallopian tubal fluid: role of a neglected epithelium. Reproduction. 2001;121(3):339–46.

    Article  CAS  PubMed  Google Scholar 

  19. Paltieli Y, Eibschitz I, Ziskind G, Ohel G, Silbermann M, Weichselbaum A. High progesterone levels and ciliary dysfunction—a possible cause of ectopic pregnancy. J Assist Reprod Genet. 2000;17(2):103–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Mahmood T, Saridogan E, Smutna S, Habib AM, Djahanbakhch O. The effect of ovarian steroids on epithelial ciliary beat frequency in the human Fallopian tube. Hum Reprod. 1998;13(11):2991–4.

    Article  CAS  PubMed  Google Scholar 

  21. Nishimura A, Sakuma K, Shimamoto C, Ito S, Nakano T, Daikoku E, Ohmichi M, Ushiroyama T, Ueki M, Kuwabara H, Mori H, Nakahari T. Ciliary beat frequency controlled by oestradiol and progesterone during ovarian cycle in guinea-pig Fallopian tube. Exp Physiol. 2010;95(7):819–28. https://doi.org/10.1113/expphysiol.2010.052555.

    Article  CAS  PubMed  Google Scholar 

  22. Talbot P, Geiske C, Knoll M. Oocyte pickup by the mammalian oviduct. Mol Biol Cell. 1999;10(1):5–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Zhuo L, Kimata K. Cumulus oophorus extracellular matrix: its construction and regulation. Cell Struct Funct. 2001;26(4):189–96.

    Article  CAS  PubMed  Google Scholar 

  24. Pauerstein CJ, Eddy CA. The role of the oviduct in reproduction; our knowledge and our ignorance. J Reprod Fertil. 1979;55(1):223–9.

    Article  CAS  PubMed  Google Scholar 

  25. Norwood JT, Hein CE, Halbert SA, Anderson RG. Polycationic macromolecules inhibit cilia-mediated ovum transport in the rabbit oviduct. Proc Natl Acad Sci USA. 1978;75(9):4413–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Halbert SA, Becker DR, Szal SE. Ovum transport in the rat oviductal ampulla in the absence of muscle contractility. Biol Reprod. 1989;40(6):1131–6.

    Article  CAS  PubMed  Google Scholar 

  27. Halbert SA, Tam PY, Blandau RJ. Egg transport in the rabbit oviduct: the roles of cilia and muscle. Science. 1976;191(4231):1052–3.

    Article  CAS  PubMed  Google Scholar 

  28. Dixon RE, Hwang SJ, Hennig GW, Ramsey KH, Schripsema JH, Sanders KM, Ward SM. Chlamydia infection causes loss of pacemaker cells and inhibits oocyte transport in the mouse oviduct. Biol Reprod. 2009;80(4):665–73. https://doi.org/10.1095/biolreprod.108.073833.

    Article  CAS  PubMed  Google Scholar 

  29. Griffin J, Emery BR, Huang I, Peterson CM, Carrell DT. Comparative analysis of follicle morphology and oocyte diameter in four mammalian species (mouse, hamster, pig, and human). J Exp Clin Assist Reprod. 2006;3:2.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Fitzharris G, Baltz JM. Granulosa cells regulate intracellular pH of the murine growing oocyte via gap junctions: development of independent homeostasis during oocyte growth. Development. 2006;133(4):591–9.

    Article  CAS  PubMed  Google Scholar 

  31. Hodgson BJ, Talo A, Pauerstein CJ. Oviductal ovum surrogate movement: interrelation with muscular activity. Biol Reprod. 1977;16(3):394–6.

    Article  CAS  PubMed  Google Scholar 

  32. Eddy CA, Flores JJ, Archer DR, Pauerstein CJ. The role of cilia in fertility: an evaluation by selective microsurgical modification of the rabbit oviduct. Am J Obstet Gynecol. 1978;132(7):814–21.

    Article  CAS  PubMed  Google Scholar 

  33. Afzelius BA, Camner P, Mossberg B. On the function of cilia in the female reproductive tract. Fertil Steril. 1978;29(1):72–4.

    Article  CAS  PubMed  Google Scholar 

  34. Raidt J, Werner C, Menchen T, Dougherty GW, Olbrich H, Loges NT, Schmitz R, Pennekamp P, Omran H. Ciliary function and motor protein composition of human fallopian tubes. Hum Reprod. 2015;30(12):2871–80. https://doi.org/10.1093/humrep/dev227.

    Article  CAS  PubMed  Google Scholar 

  35. Overstreet JW, Cooper GW. Sperm transport in the reproductive tract of the female rabbit: I. The rapid transit phase of transport. Biol Reprod. 1978;19(1):101–14.

    Article  CAS  PubMed  Google Scholar 

  36. Suarez SS, Pacey AA. Sperm transport in the female reproductive tract. Hum Reprod Update. 2006;12(1):23–37.

    Article  CAS  PubMed  Google Scholar 

  37. Suarez SS. Regulation of sperm storage and movement in the mammalian oviduct. Int J Dev Biol. 2008;52(5–6):455–62.

    Article  PubMed  Google Scholar 

  38. Suarez SS. Sperm transport and motility in the mouse oviduct: observations in situ. Biol Reprod. 1987;36(1):203–10.

    Article  CAS  PubMed  Google Scholar 

  39. Okabe M. Mechanisms of fertilization elucidated by gene-manipulated animals. Asian J Androl. 2015;17(4):646–52. https://doi.org/10.4103/1008-682X.153299.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Muro Y, Hasuwa H, Isotani A, Miyata H, Yamagata K, Ikawa M, Yanagimachi R, Okabe M. Behavior of mouse spermatozoa in the female reproductive tract from soon after mating to the beginning of fertilization. Biol Reprod. 2016;94(4):80. https://doi.org/10.1095/biolreprod.115.135368.

    Article  CAS  PubMed  Google Scholar 

  41. Blandau RJ, Gaddum-Rosse P. Mechanism of sperm transport in pig oviducts. Fertil Steril. 1974;25(1):61–7.

    Article  CAS  PubMed  Google Scholar 

  42. Battalia DE, Yanagimachi R. Enhanced and co-ordinated movement of the hamster oviduct during the periovulatory period. J Reprod Fertil. 1979;56(2):515–20.

    Article  CAS  PubMed  Google Scholar 

  43. Chang H, Suarez SS. Unexpected flagellar movement patterns and epithelial binding behavior of mouse sperm in the oviduct. Biol Reprod. 2012;86(5):140, 141–8. https://doi.org/10.1095/biolreprod.111.096578.

    Article  CAS  Google Scholar 

  44. Yanagimachi R, Chang MC. Sperm ascent through the oviduct of the hamster and rabbit in relation to the time of ovulation. J Reprod Fertil. 1963;6:413–20.

    Article  CAS  PubMed  Google Scholar 

  45. Overstreet JW, Cooper GW. Sperm transport in the reproductive tract of the female rabbit: II. The sustained phase of transport. Biol Reprod. 1978;19(1):115–32.

    Article  CAS  PubMed  Google Scholar 

  46. Wilcox AJ, Weinberg CR, Baird DD. Timing of sexual intercourse in relation to ovulation. Effects on the probability of conception, survival of the pregnancy, and sex of the baby. N Engl J Med. 1995;333(23):1517–21.

    Article  CAS  PubMed  Google Scholar 

  47. Kervancioglu ME, Djahanbakhch O, Aitken RJ. Epithelial cell coculture and the induction of sperm capacitation. Fertil Steril. 1994;61(6):1103–8.

    Article  CAS  PubMed  Google Scholar 

  48. Rodriguez-Martinez H. Role of the oviduct in sperm capacitation. Theriogenology. 2007;68(Suppl 1):S138–46.

    Article  CAS  PubMed  Google Scholar 

  49. Demott RP, Suarez SS. Hyperactivated sperm progress in the mouse oviduct. Biol Reprod. 1992;46(5):779–85.

    Article  CAS  PubMed  Google Scholar 

  50. Morales P, Palma V, Salgado AM, Villalon M. Sperm interaction with human oviductal cells in vitro. Hum Reprod. 1996;11(7):1504–9.

    Article  CAS  PubMed  Google Scholar 

  51. Pauerstein CJ. Pathophysiology of the Fallopian tube. Clin Obstet Gynecol. 1974;17(2):89–119.

    Article  CAS  PubMed  Google Scholar 

  52. Killian GJ. Evidence for the role of oviduct secretions in sperm function, fertilization and embryo development. Anim Reprod Sci. 2004;82-83:141–53.

    Article  CAS  PubMed  Google Scholar 

  53. Nishimura T, Nakajima A, Hayashi T. The basic pattern of electrical activities in the rabbit fallopian tube. Acta Obstet Gynaecol Jpn. 1969;16(2):97–103.

    CAS  PubMed  Google Scholar 

  54. Brundin J, Talo A. The effects of estrogen and progesterone on the electric activity and intraluminal pressure of the castrated rabbit oviduct. Biol Reprod. 1972;7(3):417–24.

    Article  CAS  PubMed  Google Scholar 

  55. Talo A. Electric and mechanical activity of the rabbit oviduct in vitro before and after ovulation. Biol Reprod. 1974;11(3):335–45.

    Article  CAS  PubMed  Google Scholar 

  56. Talo A, Brundin J. Muscular activity in the rabbit oviduct: a combination of electric and mechanic recordings. Biol Reprod. 1971;5(1):67–77.

    Article  CAS  PubMed  Google Scholar 

  57. Talo A, Hodgson BJ. Spike bursts in rabbit oviduct. I. Effect of ovulation. Am J Physiol. 1978;234(4):E430–8.

    CAS  PubMed  Google Scholar 

  58. Tomita T, Watanabe H. Factors controlling myogenic activity in smooth muscle. Philos Trans R Soc Lond B Biol Sci. 1973;265(867):73–85.

    Article  CAS  PubMed  Google Scholar 

  59. Dixon RE, Britton FC, Baker SA, Hennig GW, Rollings CM, Sanders KM, Ward SM. Electrical slow waves in the mouse oviduct are dependent on extracellular and intracellular calcium sources. Am J Physiol Cell Physiol. 2011;301(6):C1458–69. https://doi.org/10.1152/ajpcell.00293.2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Dixon RE, Hennig GW, Baker SA, Britton FC, Harfe BD, Rock JR, Sanders KM, Ward SM. Electrical slow waves in the mouse oviduct are dependent upon a calcium activated chloride conductance encoded by Tmem16a. Biol Reprod. 2012;86(1):1–7. https://doi.org/10.1095/biolreprod.111.095554.

    Article  CAS  PubMed  Google Scholar 

  61. Dixon RE, Ramsey KH, Schripsema JH, Sanders KM, Ward SM. Time-dependent disruption of oviduct pacemaker cells by Chlamydia infection in mice. Biol Reprod. 2010;83(2):244–53. https://doi.org/10.1095/biolreprod.110.083808.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Johns A, Coons LW. Physiological and pharmacological characteristics of the baboon (Papio anubis) oviduct. Biol Reprod. 1981;25(1):120–7.

    Article  CAS  PubMed  Google Scholar 

  63. Zasztowt O. [Studies on the bioelectrical phenomena of the cell membrane of the muscle of oviducts]. Ginekol Pol. 1969;40(4):371–6.

    Google Scholar 

  64. Kishikawa T, Kuriyama H. Electrical and mechanical activities recorded from smooth muscle cells of the human fallopian tube. Jpn J Physiol. 1981;31(3):417–22.

    Article  CAS  PubMed  Google Scholar 

  65. Lindblom B, Wikland M. Simultaneous recording of electrical and mechanical activity in isolated smooth muscle of the human oviduct. Biol Reprod. 1982;27(2):393–8.

    Article  CAS  PubMed  Google Scholar 

  66. Parkington HC. Intracellularly recorded electrical activity of smooth muscle of guinea pig oviduct. Am J Physiol. 1983;245(5 Pt 1):C357–64.

    Article  CAS  PubMed  Google Scholar 

  67. Holman ME. Membrane potentials recorded with high-resistance micro-electrodes; and the effects of changes in ionic environment on the electrical and mechanical activity of the smooth muscle of the taenia coli of the guinea pig. J Physiol. 1958;141(3):464–88.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Talo A, Hodgson BJ. Electrical slow waves in oviductal smooth muscle of the guinea-pig, mouse and the immature baboon. Experientia. 1978;34(2):198–200.

    Article  CAS  PubMed  Google Scholar 

  69. Bayguinov O, Hennig GW, Sanders KM. Movement based artifacts may contaminate extracellular electrical recordings from GI muscles. Neurogastroenterol Motil. 2011;23(11):1029–42, e1498. https://doi.org/10.1111/j.1365-2982.2011.01784.x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Ozaki H, Stevens RJ, Blondfield DP, Publicover NG, Sanders KM. Simultaneous measurement of membrane potential, cytosolic Ca2+, and tension in intact smooth muscles. Am J Physiol. 1991;260(5 Pt 1):C917–25.

    Article  CAS  PubMed  Google Scholar 

  71. Forrest AS, Ordog T, Sanders KM. Neural regulation of slow-wave frequency in the murine gastric antrum. Am J Physiol Gastrointest Liver Physiol. 2006;290(3):G486–95. https://doi.org/10.1152/ajpgi.00349.2005.

    Article  CAS  PubMed  Google Scholar 

  72. Hirst GD, Bramich NJ, Teramoto N, Suzuki H, Edwards FR. Regenerative component of slow waves in the guinea-pig gastric antrum involves a delayed increase in [Ca(2+)](i) and Cl(−) channels. J Physiol. 2002;540(Pt 3):907–19.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Burke EP, Gerthoffer WT, Sanders KM, Publicover NG. Wortmannin inhibits contraction without altering electrical activity in canine gastric smooth muscle. Am J Phys. 1996;270(5 Pt 1):C1405–12. https://doi.org/10.1152/ajpcell.1996.270.5.C1405.

    Article  CAS  Google Scholar 

  74. Sanders KM, Ward SM, Hennig GW. Problems with extracellular recording of electrical activity in gastrointestinal muscle. Nat Rev Gastroenterol Hepatol. 2016;13(12):731–41. https://doi.org/10.1038/nrgastro.2016.161.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Du P, Calder S, Angeli TR, Sathar S, Paskaranandavadivel N, O’Grady G, Cheng LK. Progress in mathematical modeling of gastrointestinal slow wave abnormalities. Front Physiol. 2017;8:1136. https://doi.org/10.3389/fphys.2017.01136.

    Article  PubMed  Google Scholar 

  76. O’Grady G, Paskaranandavadivel N, Du P, Angeli T, Erickson JC, Cheng LK. Correct techniques for extracellular recordings of electrical activity in gastrointestinal muscle. Nat Rev Gastroenterol Hepatol. 2017;14(6):372. https://doi.org/10.1038/nrgastro.2017.15.

    Article  PubMed  Google Scholar 

  77. Sanders KM, Ward SM, Hennig GW. Extracellular gastrointestinal electrical recordings: movement not electrophysiology. Nat Rev Gastroenterol Hepatol. 2017;14(6):372. https://doi.org/10.1038/nrgastro.2017.39.

    Article  PubMed  Google Scholar 

  78. Hodgson BJ, Talo A. Spike bursts in rabbit oviduct. II. Effects of estrogen and progesterone. Am J Physiol. 1978;234(4):E439–43.

    CAS  PubMed  Google Scholar 

  79. Popescu LM, Ciontea SM, Cretoiu D, Hinescu ME, Radu E, Ionescu N, Ceausu M, Gherghiceanu M, Braga RI, Vasilescu F, Zagrean L, Ardeleanu C. Novel type of interstitial cell (Cajal-like) in human fallopian tube. J Cell Mol Med. 2005;9(2):479–523.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Shafik A, Shafik AA, El Sibai O, Shafik IA. Specialized pacemaking cells in the human Fallopian tube. Mol Hum Reprod. 2005;11(7):503–5.

    Article  CAS  PubMed  Google Scholar 

  81. Ordog T, Redelman D, Horvath VJ, Miller LJ, Horowitz B, Sanders KM. Quantitative analysis by flow cytometry of interstitial cells of Cajal, pacemakers, and mediators of neurotransmission in the gastrointestinal tract. Cytometry A. 2004;62(2):139–49.

    Article  PubMed  CAS  Google Scholar 

  82. Christensen J. A commentary on the morphological identification of interstitial cells of Cajal in the gut. J Auton Nerv Syst. 1992;37(2):75–88.

    Article  CAS  PubMed  Google Scholar 

  83. Huizinga JD, Thuneberg L, Vanderwinden JM, Rumessen JJ. Interstitial cells of Cajal as targets for pharmacological intervention in gastrointestinal motor disorders. Trends Pharmacol Sci. 1997;18(10):393–403.

    Article  CAS  PubMed  Google Scholar 

  84. Sanders KM. A case for interstitial cells of Cajal as pacemakers and mediators of neurotransmission in the gastrointestinal tract. Gastroenterology. 1996;111(2):492–515.

    Article  CAS  PubMed  Google Scholar 

  85. Torihashi S, Ward SM, Nishikawa S, Nishi K, Kobayashi S, Sanders KM. c-Kit-dependent development of interstitial cells and electrical activity in the murine gastrointestinal tract. Cell Tissue Res. 1995;280(1):97–111.

    CAS  PubMed  Google Scholar 

  86. Beckett EA, Ro S, Bayguinov Y, Sanders KM, Ward SM. Kit signaling is essential for development and maintenance of interstitial cells of Cajal and electrical rhythmicity in the embryonic gastrointestinal tract. Dev Dyn. 2007;236(1):60–72.

    Article  CAS  PubMed  Google Scholar 

  87. Maeda H, Yamagata A, Nishikawa S, Yoshinaga K, Kobayashi S, Nishi K, Nishikawa S. Requirement of c-kit for development of intestinal pacemaker system. Development. 1992;116(2):369–75.

    CAS  PubMed  Google Scholar 

  88. Sanders KM. Regulation of smooth muscle excitation and contraction. Neurogastroenterol Motil. 2008;20(Suppl 1):39–53.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Hashitani H, van Helden DF, Suzuki H. Properties of spontaneous depolarizations in circular smooth muscle cells of rabbit urethra. Br J Pharmacol. 1996;118(7):1627–32.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Kito Y, Fukuta H, Suzuki H. Components of pacemaker potentials recorded from the guinea pig stomach antrum. Pflugers Arch. 2002;445(2):202–17.

    Article  CAS  PubMed  Google Scholar 

  91. von der Weid PY, Rahman M, Imtiaz MS, van Helden DF. Spontaneous transient depolarizations in lymphatic vessels of the guinea pig mesentery: pharmacology and implication for spontaneous contractility. Am J Physiol Heart Circ Physiol. 2008;295(5):H1989–2000.

    Article  PubMed  CAS  Google Scholar 

  92. Cobine CA, Hannah EE, Zhu MH, Lyle HE, Rock JR, Sanders KM, Ward SM, Keef KD. ANO1 in intramuscular interstitial cells of Cajal plays a key role in the generation of slow waves and tone in the internal anal sphincter. J Physiol. 2017;595(6):2021–41. https://doi.org/10.1113/JP273618.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Zhu MH, Kim TW, Ro S, Yan W, Ward SM, Koh SD, Sanders KM. A Ca(2+)-activated Cl(−) conductance in interstitial cells of Cajal linked to slow wave currents and pacemaker activity. J Physiol. 2009;587(Pt 20):4905–18. https://doi.org/10.1113/jphysiol.2009.176206.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Huang F, Zhang H, Wu M, Yang H, Kudo M, Peters CJ, Woodruff PG, Solberg OD, Donne ML, Huang X, Sheppard D, Fahy JV, Wolters PJ, Hogan BL, Finkbeiner WE, Li M, Jan YN, Jan LY, Rock JR. Calcium-activated chloride channel TMEM16A modulates mucin secretion and airway smooth muscle contraction. Proc Natl Acad Sci U S A. 2012;109(40):16354–9. https://doi.org/10.1073/pnas.1214596109.

    Article  PubMed  PubMed Central  Google Scholar 

  95. Hwang SJ, Blair PJ, Britton FC, O’Driscoll KE, Hennig G, Bayguinov YR, Rock JR, Harfe BD, Sanders KM, Ward SM. Expression of anoctamin 1/TMEM16A by interstitial cells of Cajal is fundamental for slow wave activity in gastrointestinal muscles. J Physiol. 2009;587(Pt 20):4887–904. https://doi.org/10.1113/jphysiol.2009.176198.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Hwang SJ, Basma N, Sanders KM, Ward SM. Effects of new-generation inhibitors of the calcium-activated chloride channel anoctamin 1 on slow waves in the gastrointestinal tract. Br J Pharmacol. 2016;173(8):1339–49. https://doi.org/10.1111/bph.13431.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Sanders KM, Zhu MH, Britton F, Koh SD, Ward SM. Anoctamins and gastrointestinal smooth muscle excitability. Exp Physiol. 2012;97(2):200–6. https://doi.org/10.1113/expphysiol.2011.058248.

    Article  CAS  PubMed  Google Scholar 

  98. Singh RD, Gibbons SJ, Saravanaperumal SA, Du P, Hennig GW, Eisenman ST, Mazzone A, Hayashi Y, Cao C, Stoltz GJ, Ordog T, Rock JR, Harfe BD, Szurszewski JH, Farrugia G. Ano1, a Ca2+-activated Cl− channel, coordinates contractility in mouse intestine by Ca2+ transient coordination between interstitial cells of Cajal. J Physiol. 2014;592(18):4051–68. https://doi.org/10.1113/jphysiol.2014.277152.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. El-Sharkawy TY, Daniel EE. Ionic mechanisms of intestinal electrical control activity. Am J Physiol. 1975;229(5):1287–98.

    Article  CAS  Google Scholar 

  100. El-Sharkawy TY, Szurszewski JH. Modulation of canine antral circular smooth muscle by acetylcholine, noradrenaline and pentagastrin. J Physiol. 1978;279:309–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Dahms V, Prosser CL, Suzuki N. Two types of ‘slow waves’ in intestinal smooth muscle of cat. J Physiol. 1987;392:51–69.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Huizinga JD, Farraway L, Den Hertog A. Generation of slow-wave-type action potentials in canine colon smooth muscle involves a non-L-type Ca2+ conductance. J Physiol. 1991;442:15–29.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Ward SM, Sanders KM. Dependence of electrical slow waves of canine colonic smooth muscle on calcium gradient. J Physiol. 1992;455:307–19.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Ward SM, Sanders KM. Upstroke component of electrical slow waves in canine colonic smooth muscle due to nifedipine-resistant calcium current. J Physiol. 1992;455:321–37.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Kito Y, Suzuki H. Properties of pacemaker potentials recorded from myenteric interstitial cells of Cajal distributed in the mouse small intestine. J Physiol. 2003;553(Pt 3):803–18.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Ward SM, Dixon RE, de Faoite A, Sanders KM. Voltage-dependent calcium entry underlies propagation of slow waves in canine gastric antrum. J Physiol. 2004;561(Pt 3):793–810.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Bayguinov O, Ward SM, Kenyon JL, Sanders KM. Voltage-gated Ca2+ currents are necessary for slow-wave propagation in the canine gastric antrum. Am J Physiol Cell Physiol. 2007;293(5):C1645–59.

    Article  CAS  PubMed  Google Scholar 

  108. Drumm BT, Hennig GW, Battersby MJ, Cunningham EK, Sung TS, Ward SM, Sanders KM, Baker SA. Clustering of Ca(2+) transients in interstitial cells of Cajal defines slow wave duration. J Gen Physiol. 2017;149(7):703–25. https://doi.org/10.1085/jgp.201711771.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Berridge MJ. Smooth muscle cell calcium activation mechanisms. J Physiol. 2008;586(Pt 21):5047–61.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Feske S, Gwack Y, Prakriya M, Srikanth S, Puppel SH, Tanasa B, Hogan PG, Lewis RS, Daly M, Rao A. A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature. 2006;441(7090):179–85. https://doi.org/10.1038/nature04702.

    Article  CAS  PubMed  Google Scholar 

  111. Prakriya M, Lewis RS. Store-operated calcium channels. Physiol Rev. 2015;95(4):1383–436. https://doi.org/10.1152/physrev.00020.2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Putney JWJ. Capacitative calcium entry revisited. Cell Calcium. 1990;11(10):611–24.

    Article  CAS  PubMed  Google Scholar 

  113. Berridge MJ. Inositol trisphosphate and calcium signalling. Nature. 1993;361(6410):315–25.

    Article  CAS  PubMed  Google Scholar 

  114. Dixon R, Hwang S, Britton F, Sanders K, Ward S. Inhibitory effect of caffeine on pacemaker activity in the oviduct is mediated by cAMP-regulated conductances. Br J Pharmacol. 2011;163(4):745–54. https://doi.org/10.1111/j.1476-5381.2011.01266.x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Johnston L, Sergeant GP, Hollywood MA, Thornbury KD, McHale NG. Calcium oscillations in interstitial cells of the rabbit urethra. J Physiol. 2005;565(Pt 2):449–61.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Aickin CC, Brading AF. Measurement of intracellular chloride in guinea-pig vas deferens by ion analysis, 36chloride efflux and micro-electrodes. J Physiol. 1982;326:139–54.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Greenwood IA, Leblanc N. Overlapping pharmacology of Ca2+-activated Cl− and K+ channels. Trends Pharmacol Sci. 2007;28(1):1–5.

    Article  CAS  PubMed  Google Scholar 

  118. Ohba M, Sakamoto Y, Tomita T. The slow wave in the circular muscle of the guinea-pig stomach. J Physiol. 1975;253(2):505–16.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Rock JR, Harfe BD. Expression of TMEM16 paralogs during murine embryogenesis. Dev Dyn. 2008;237(9):2566–74.

    Article  CAS  PubMed  Google Scholar 

  120. Huang F, Rock JR, Harfe BD, Cheng T, Huang X, Jan YN, Jan LY. Studies on expression and function of the TMEM16A calcium-activated chloride channel. Proc Natl Acad Sci U S A. 2009;106(50):21413–8. https://doi.org/10.1073/pnas.0911935106.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Gomez-Pinilla PJ, Gibbons SJ, Bardsley MR, Lorincz A, Pozo MJ, Pasricha PJ, de Rijn MV, West RB, Sarr MG, Kendrick ML, Cima RR, Dozois EJ, Larson DW, Ordog T, Farrugia G. Ano1 is a selective marker of interstitial cells of Cajal in the human and mouse gastrointestinal tract. Am J Physiol Gastrointest Liver Physiol. 2009;296(6):G1370–81.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Xiao Q, Yu K, Perez-Cornejo P, Cui Y, Arreola J, Hartzell HC. Voltage- and calcium-dependent gating of TMEM16A/Ano1 chloride channels are physically coupled by the first intracellular loop. Proc Natl Acad Sci U S A. 2011;108(21):8891–6. https://doi.org/10.1073/pnas.1102147108.

    Article  PubMed  PubMed Central  Google Scholar 

  123. Szurszewski JH. Electrical basis for gastrointestinal motility. In: Johnson LR, editor. Physiology of the gastrointestinal tract. 2nd ed. New York: Raven Press; 1987. p. 1435.

    Google Scholar 

  124. Diamant NE, Bortoff A. Nature of the intestinal slow-wave frequency gradient. Am J Physiol. 1969;216(2):301–7.

    Article  CAS  PubMed  Google Scholar 

  125. Szurszewski JH, Elveback LR, Code CF. Configuration and frequency gradient of electric slow wave over canine small bowel. Am J Phys. 1970;218(5):1468–73. https://doi.org/10.1152/ajplegacy.1970.218.5.1468.

    Article  CAS  Google Scholar 

  126. Siegle ML, Buhner S, Schemann M, Schmid HR, Ehrlein HJ. Propagation velocities and frequencies of contractions along canine small intestine. Am J Physiol. 1990;258(5 Pt 1):G738–44.

    CAS  PubMed  Google Scholar 

  127. Traurig HH, Papka RE. Autonomic efferent and visceral sensory innervation of the female reproductive system: special reference to the functional roles of nerves in reproductive organs. In: Maggi CA, editor. Nervous control of the urogenital system, The autonomic nervous system, vol. 3. Chur: Harwood Academic Publishers; 1993. p. 103–41.

    Google Scholar 

  128. Nance DM, Burns J, Klein CM, Burden HW. Afferent fibers in the reproductive system and pelvic viscera of female rats: anterograde tracing and immunocytochemical studies. Brain Res Bull. 1988;21(4):701–9.

    Article  CAS  PubMed  Google Scholar 

  129. Papka RE, Traurig HH. Autonomic efferent and visceral sensory innervation of the female reproductive tract: special reference to neurochemical markers in nerves and ganglionic connections. In: Maggi CA, editor. Nervous control of the urogenital system, The autonomic nervous system, vol. 3. Chur: Harwood Academic Publishers; 1993. p. 423–66.

    Google Scholar 

  130. Jankovic SM, Protic BA, Jankovic SV. Contractile effect of acetylcholine on isolated isthmic segment of fallopian tubes. Methods Find Exp Clin Pharmacol. 2004;26(2):87–91.

    Article  CAS  PubMed  Google Scholar 

  131. Jankovic SM, Protic BA, Jankovic SV. Contractile effect of acetylcholine on isolated ampullar segment of Fallopian tubes. Pharmacol Res. 2004;49(1):31–5.

    Article  CAS  PubMed  Google Scholar 

  132. Helm GH, Hakanson R, Leander S, Owman C, Sjoberg NO, Sporrong B. Neurogenic relaxation mediated by vasoactive intestinal polypeptide (VIP) in the isthmus of the human fallopian tube. Regul Pept. 1982;3(2):145–53.

    Article  CAS  PubMed  Google Scholar 

  133. Grozdanovic Z, Mayer B, Baumgarten HG, Bruning G. Nitric oxide synthase-containing nerve fibers and neurons in the genital tract of the female mouse. Cell Tissue Res. 1994;275(2):355–60.

    Article  CAS  PubMed  Google Scholar 

  134. Ekerhovd E, Brannstrom M, Weijdegard B, Norstrom A. Localization of nitric oxide synthase and effects of nitric oxide donors on the human Fallopian tube. Mol Hum Reprod. 1999;5(11):1040–7.

    Article  CAS  PubMed  Google Scholar 

  135. Lapointe J, Roy M, St-Pierre I, Kimmins S, Gauvreau D, MacLaren LA, Bilodeau JF. Hormonal and spatial regulation of nitric oxide synthases (NOS) (neuronal NOS, inducible NOS, and endothelial NOS) in the oviducts. Endocrinology. 2006;147(12):5600–10.

    Article  CAS  PubMed  Google Scholar 

  136. Ortiz ME, Villalon M, Croxatto HB. Ovum transport and fertility following postovulatory treatment with estradiol in rats. Biol Reprod. 1979;21(5):1163–7.

    Article  CAS  PubMed  Google Scholar 

  137. Rios M, Hermoso M, Sanchez TM, Croxatto HB, Villalon MJ. Effect of oestradiol and progesterone on the instant and directional velocity of microsphere movements in the rat oviduct: gap junctions mediate the kinetic effect of oestradiol. Reprod Fertil Dev. 2007;19(5):634–40.

    Article  CAS  PubMed  Google Scholar 

  138. Norwitz ER, Schust DJ, Fisher SJ. Implantation and the survival of early pregnancy. N Engl J Med. 2001;345(19):1400–8. https://doi.org/10.1056/NEJMra000763.

    Article  CAS  PubMed  Google Scholar 

  139. Wilcox AJ, Weinberg CR, O’Connor JF, Baird DD, Schlatterer JP, Canfield RE, Armstrong EG, Nisula BC. Incidence of early loss of pregnancy. N Engl J Med. 1988;319(4):189–94. https://doi.org/10.1056/NEJM198807283190401.

    Article  CAS  PubMed  Google Scholar 

  140. Pisarska MD, Carson SA. Incidence and risk factors for ectopic pregnancy. Clin Obstet Gynecol. 1999;42(1):2–8; quiz 55–56

    Article  CAS  PubMed  Google Scholar 

  141. From the Centers for Disease Control and Prevention. Ectopic pregnancy—United States, 1990–1992. JAMA. 1995;273(7):533.

    Article  Google Scholar 

  142. Talbot P, Riveles K. Smoking and reproduction: the oviduct as a target of cigarette smoke. Reprod Biol Endocrinol. 2005;3:52. https://doi.org/10.1186/1477-7827-3-52.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Saraiya M, Berg CJ, Kendrick JS, Strauss LT, Atrash HK, Ahn YW. Cigarette smoking as a risk factor for ectopic pregnancy. Am J Obstet Gynecol. 1998;178(3):493–8.

    Article  CAS  PubMed  Google Scholar 

  144. Yoshinaga K, Rice C, Krenn J, Pilot RL. Effects of nicotine on early pregnancy in the rat. Biol Reprod. 1979;20(2):294–303.

    Article  CAS  PubMed  Google Scholar 

  145. Jensen TK, Henriksen TB, Hjollund NH, Scheike T, Kolstad H, Giwercman A, Ernst E, Bonde JP, Skakkebaek NE, Olsen J. Caffeine intake and fecundability: a follow-up study among 430 Danish couples planning their first pregnancy. Reprod Toxicol. 1998;12(3):289–95.

    Article  CAS  PubMed  Google Scholar 

  146. United Nations Office on Drugs and Crime. World drug report.

    Google Scholar 

  147. Feng T. Substance abuse in pregnancy. Curr Opin Obstet Gynecol. 1993;5(1):16–23.

    Article  CAS  PubMed  Google Scholar 

  148. Young-Wolff KC, Tucker LY, Alexeeff S, Armstrong MA, Conway A, Weisner C, Goler N. Trends in self-reported and biochemically tested Marijuana use among pregnant females in California from 2009–2016. JAMA. 2017;318(24):2490–1. https://doi.org/10.1001/jama.2017.17225.

    Article  PubMed  PubMed Central  Google Scholar 

  149. Maykut MO. Health consequences of acute and chronic marihuana use. Prog Neuropsychopharmacol Biol Psychiatry. 1985;9(3):209–38.

    Article  CAS  PubMed  Google Scholar 

  150. Mueller BA, Daling JR, Weiss NS, Moore DE. Recreational drug use and the risk of primary infertility. Epidemiology. 1990;1(3):195–200.

    Article  CAS  PubMed  Google Scholar 

  151. Klonoff-Cohen HS, Natarajan L, Chen RV. A prospective study of the effects of female and male marijuana use on in vitro fertilization (IVF) and gamete intrafallopian transfer (GIFT) outcomes. Am J Obstet Gynecol. 2006;194(2):369–76. https://doi.org/10.1016/j.ajog.2005.08.020.

    Article  CAS  PubMed  Google Scholar 

  152. Horne AW, Phillips JA 3rd, Kane N, Lourenco PC, McDonald SE, Williams AR, Simon C, Dey SK, Critchley HO. CB1 expression is attenuated in Fallopian tube and decidua of women with ectopic pregnancy. PLoS One. 2008;3(12):e3969. https://doi.org/10.1371/journal.pone.0003969.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Wang H, Guo Y, Wang D, Kingsley PJ, Marnett LJ, Das SK, DuBois RN, Dey SK. Aberrant cannabinoid signaling impairs oviductal transport of embryos. Nat Med. 2004;10(10):1074–80. https://doi.org/10.1038/nm1104.

    Article  CAS  PubMed  Google Scholar 

  154. Maccarrone M, Valensise H, Bari M, Lazzarin N, Romanini C, Finazzi-Agro A. Relation between decreased anandamide hydrolase concentrations in human lymphocytes and miscarriage. Lancet. 2000;355(9212):1326–9. https://doi.org/10.1016/S0140-6736(00)02115-2.

    Article  CAS  PubMed  Google Scholar 

  155. Matsuda LA, Lolait SJ, Brownstein MJ, Young AC, Bonner TI. Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature. 1990;346(6284):561–4. https://doi.org/10.1038/346561a0.

    Article  CAS  PubMed  Google Scholar 

  156. Munro S, Thomas KL, Abu-Shaar M. Molecular characterization of a peripheral receptor for cannabinoids. Nature. 1993;365(6441):61–5. https://doi.org/10.1038/365061a0.

    Article  CAS  PubMed  Google Scholar 

  157. Sugiura T, Kodaka T, Nakane S, Miyashita T, Kondo S, Suhara Y, Takayama H, Waku K, Seki C, Baba N, Ishima Y. Evidence that the cannabinoid CB1 receptor is a 2-arachidonoylglycerol receptor. Structure-activity relationship of 2-arachidonoylglycerol, ether-linked analogues, and related compounds. J Biol Chem. 1999;274(5):2794–801.

    Article  CAS  PubMed  Google Scholar 

  158. Sugiura T, Kondo S, Sukagawa A, Nakane S, Shinoda A, Itoh K, Yamashita A, Waku K. 2-Arachidonoylglycerol: a possible endogenous cannabinoid receptor ligand in brain. Biochem Biophys Res Commun. 1995;215(1):89–97.

    Article  CAS  PubMed  Google Scholar 

  159. Mechoulam R, Ben-Shabat S, Hanus L, Ligumsky M, Kaminski NE, Schatz AR, Gopher A, Almog S, Martin BR, Compton DR, et al. Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochem Pharmacol. 1995;50(1):83–90.

    Article  CAS  PubMed  Google Scholar 

  160. Maccarrone M, Finazzi-Agro A. Endocannabinoids and their actions. Vitam Horm. 2002;65:225–55.

    Article  CAS  PubMed  Google Scholar 

  161. Piomelli D. The molecular logic of endocannabinoid signalling. Nat Rev Neurosci. 2003;4(11):873–84. https://doi.org/10.1038/nrn1247.

    Article  CAS  PubMed  Google Scholar 

  162. De Petrocellis L, Cascio MG, Di Marzo V. The endocannabinoid system: a general view and latest additions. Br J Pharmacol. 2004;141(5):765–74. https://doi.org/10.1038/sj.bjp.0705666.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  163. Paria BC, Das SK, Dey SK. The preimplantation mouse embryo is a target for cannabinoid ligand-receptor signaling. Proc Natl Acad Sci U S A. 1995;92(21):9460–4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  164. Paria BC, Song H, Wang X, Schmid PC, Krebsbach RJ, Schmid HH, Bonner TI, Zimmer A, Dey SK. Dysregulated cannabinoid signaling disrupts uterine receptivity for embryo implantation. J Biol Chem. 2001;276(23):20523–8. https://doi.org/10.1074/jbc.M100679200.

    Article  CAS  PubMed  Google Scholar 

  165. Schmid PC, Paria BC, Krebsbach RJ, Schmid HH, Dey SK. Changes in anandamide levels in mouse uterus are associated with uterine receptivity for embryo implantation. Proc Natl Acad Sci U S A. 1997;94(8):4188–92.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  166. Wang H, Matsumoto H, Guo Y, Paria BC, Roberts RL, Dey SK. Differential G protein-coupled cannabinoid receptor signaling by anandamide directs blastocyst activation for implantation. Proc Natl Acad Sci U S A. 2003;100(25):14914–9. https://doi.org/10.1073/pnas.2436379100.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  167. Nawrot P, Jordan S, Eastwood J, Rotstein J, Hugenholtz A, Feeley M. Effects of caffeine on human health. Food Addit Contam. 2003;20(1):1–30. https://doi.org/10.1080/0265203021000007840.

    Article  CAS  PubMed  Google Scholar 

  168. Stanton CK, Gray RH. Effects of caffeine consumption on delayed conception. Am J Epidemiol. 1995;142(12):1322–9.

    Article  CAS  PubMed  Google Scholar 

  169. Bolumar F, Olsen J, Rebagliato M, Bisanti L. Caffeine intake and delayed conception: a European multicenter study on infertility and subfecundity. European Study Group on Infertility Subfecundity. Am J Epidemiol. 1997;145(4):324–34.

    Article  CAS  PubMed  Google Scholar 

  170. Florack EI, Zielhuis GA, Rolland R. Cigarette smoking, alcohol consumption, and caffeine intake and fecundability. Prev Med. 1994;23(2):175–80. https://doi.org/10.1006/pmed.1994.1024.

    Article  CAS  PubMed  Google Scholar 

  171. Hatch EE, Bracken MB. Association of delayed conception with caffeine consumption. Am J Epidemiol. 1993;138(12):1082–92.

    Article  CAS  PubMed  Google Scholar 

  172. Parker I, Ivorra I. Caffeine inhibits inositol trisphosphate-mediated liberation of intracellular calcium in Xenopus oocytes. J Physiol. 1991;433:229–40.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  173. Butcher RW, Sutherland EW. Adenosine 3′,5′-phosphate in biological materials. I. Purification and properties of cyclic 3′,5′-nucleotide phosphodiesterase and use of this enzyme to characterize adenosine 3′,5′-phosphate in human urine. J Biol Chem. 1962;237:1244–50.

    CAS  PubMed  Google Scholar 

  174. Beavo JA. Cyclic nucleotide phosphodiesterases: functional implications of multiple isoforms. Physiol Rev. 1995;75(4):725–48.

    Article  CAS  PubMed  Google Scholar 

  175. Kim M, Cho SY, Han IS, Koh SD, Perrino BA. CaM kinase II and phospholamban contribute to caffeine-induced relaxation of murine gastric fundus smooth muscle. Am J Physiol Cell Physiol. 2005;288(6):C1202–10.

    Article  CAS  PubMed  Google Scholar 

  176. Kim M, Hennig GW, Smith TK, Perrino BA. Phospholamban knockout increases CaM kinase II activity and intracellular Ca2+ wave activity and alters contractile responses of murine gastric antrum. Am J Physiol Cell Physiol. 2008;294(2):C432–41. https://doi.org/10.1152/ajpcell.00418.2007.

    Article  CAS  PubMed  Google Scholar 

  177. Nobe K, Sutliff RL, Kranias EG, Paul RJ. Phospholamban regulation of bladder contractility: evidence from gene-altered mouse models. J Physiol. 2001;535(Pt 3):867–78.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  178. Eggermont JA, Vrolix M, Wuytack F, Raeymaekers L, Casteels R. The (Ca2+-Mg2+)-ATPases of the plasma membrane and of the endoplasmic reticulum in smooth muscle cells and their regulation. J Cardiovasc Pharmacol. 1988;12(Suppl 5):S51–5.

    Article  CAS  PubMed  Google Scholar 

  179. Meera P, Anwer K, Monga M, Oberti C, Stefani E, Toro L, Sanborn BM. Relaxin stimulates myometrial calcium-activated potassium channel activity via protein kinase A. Am J Physiol. 1995;269(2 Pt 1):C312–7.

    Article  CAS  PubMed  Google Scholar 

  180. Sanborn BM, Yue C, Wang W, Dodge KL. G protein signalling pathways in myometrium: affecting the balance between contraction and relaxation. Rev Reprod. 1998;3(3):196–205.

    Article  CAS  PubMed  Google Scholar 

  181. Price SA, Bernal AL. Uterine quiescence: the role of cyclic AMP. Exp Physiol. 2001;86(2):265–72.

    Article  CAS  PubMed  Google Scholar 

  182. Quayle JM, Bonev AD, Brayden JE, Nelson MT. Calcitonin gene-related peptide activated ATP-sensitive K+ currents in rabbit arterial smooth muscle via protein kinase A. J Physiol. 1994;475(1):9–13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  183. Wellman GC, Quayle JM, Standen NB. ATP-sensitive K+ channel activation by calcitonin gene-related peptide and protein kinase A in pig coronary arterial smooth muscle. J Physiol. 1998;507(Pt 1):117–29.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  184. Quinn KV, Giblin JP, Tinker A. Multisite phosphorylation mechanism for protein kinase A activation of the smooth muscle ATP-sensitive K+ channel. Circ Res. 2004;94(10):1359–66.

    Article  CAS  PubMed  Google Scholar 

  185. Shi Y, Wu Z, Cui N, Shi W, Yang Y, Zhang X, Rojas A, Ha BT, Jiang C. PKA phosphorylation of SUR2B subunit underscores vascular KATP channel activation by beta-adrenergic receptors. Am J Physiol Regul Integr Comp Physiol. 2007;293(3):R1205–14.

    Article  CAS  PubMed  Google Scholar 

  186. Shi Y, Chen X, Wu Z, Shi W, Yang Y, Cui N, Jiang C, Harrison RW. cAMP-dependent protein kinase phosphorylation produces interdomain movement in SUR2B leading to activation of the vascular KATP channel. J Biol Chem. 2008;283(12):7523–30.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  187. Burg AW. Physiological disposition of caffeine. Drug Metab Rev. 1975;4(2):199–228. https://doi.org/10.3109/03602537508993756.

    Article  CAS  PubMed  Google Scholar 

  188. White JR Jr, Padowski JM, Zhong Y, Chen G, Luo S, Lazarus P, Layton ME, McPherson S. Pharmacokinetic analysis and comparison of caffeine administered rapidly or slowly in coffee chilled or hot versus chilled energy drink in healthy young adults. Clin Toxicol (Phila). 2016;54(4):308–12. https://doi.org/10.3109/15563650.2016.1146740.

    Article  Google Scholar 

  189. Adderley-Kelly B, Stephens EM. Chlamydia: a major health threat to adolescents and young adults. ABNF J. 2005;16(3):52–5.

    PubMed  Google Scholar 

  190. Stamm WE. Chlamydia screening: expanding the scope. Ann Intern Med. 2004;141(7):570–2.

    Article  PubMed  Google Scholar 

  191. World Health Organization. Global prevalence and incidence of selected curable sexually transmitted infections overview and estimates. Geneva: WHO; 2001.

    Google Scholar 

  192. Entrican G, Wattegedera S, Rocchi M, Fleming DC, Kelly RW, Wathne G, Magdalenic V, Howie SE. Induction of inflammatory host immune responses by organisms belonging to the genera Chlamydia/Chlamydophila. Vet Immunol Immunopathol. 2004;100(3–4):179–86.

    Article  CAS  PubMed  Google Scholar 

  193. World Health Organization. Global strategy for the prevention and control of sexually transmitted infections: 2006–2015: breaking the chain of transmission. Geneva: WHO; 2007.

    Google Scholar 

  194. Read TD, Brunham RC, Shen C, Gill SR, Heidelberg JF, White O, Hickey EK, Peterson J, Utterback T, Berry K, Bass S, Linher K, Weidman J, Khouri H, Craven B, Bowman C, Dodson R, Gwinn M, Nelson W, DeBoy R, Kolonay J, McClarty G, Salzberg SL, Eisen J, Fraser CM. Genome sequences of Chlamydia trachomatis MoPn and Chlamydia pneumoniae AR39. Nucleic Acids Res. 2000;28(6):1397–406.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  195. Brunham RC, Rey-Ladino J. Immunology of Chlamydia infection: implications for a Chlamydia trachomatis vaccine. Nat Rev Immunol. 2005;5(2):149–61.

    Article  CAS  PubMed  Google Scholar 

  196. Shah AA, Schripsema JH, Imtiaz MT, Sigar IM, Kasimos J, Matos PG, Inouye S, Ramsey KH. Histopathologic changes related to fibrotic oviduct occlusion after genital tract infection of mice with Chlamydia muridarum. Sex Transm Dis. 2005;32(1):49–56.

    Article  PubMed  Google Scholar 

  197. Eskandari MK, Kalff JC, Billiar TR, Lee KK, Bauer AJ. LPS-induced muscularis macrophage nitric oxide suppresses rat jejunal circular muscle activity. Am J Physiol. 1999;277(2 Pt 1):G478–86.

    CAS  PubMed  Google Scholar 

  198. Kalff JC, Schraut WH, Billiar TR, Simmons RL, Bauer AJ. Role of inducible nitric oxide synthase in postoperative intestinal smooth muscle dysfunction in rodents. Gastroenterology. 2000;118(2):316–27.

    Article  CAS  PubMed  Google Scholar 

  199. Yanagida H, Sanders KM, Ward SM. Inactivation of inducible nitric oxide synthase protects intestinal pacemaker cells from postoperative damage. J Physiol. 2007;582(Pt 2):755–65.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  200. Xin HB, Deng KY, Rishniw M, Ji G, Kotlikoff MI. Smooth muscle expression of Cre recombinase and eGFP in transgenic mice. Physiol Genomics. 2002;10(3):211–5.

    Article  CAS  PubMed  Google Scholar 

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Dixon, R.E., Hwang, S.J., Kim, B.H., Sanders, K.M., Ward, S.M. (2019). Myosalpinx Contractions Are Essential for Egg Transport Along the Oviduct and Are Disrupted in Reproductive Tract Diseases. In: Hashitani, H., Lang, R. (eds) Smooth Muscle Spontaneous Activity. Advances in Experimental Medicine and Biology, vol 1124. Springer, Singapore. https://doi.org/10.1007/978-981-13-5895-1_11

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