Advertisement

Venous Vasomotion

  • Dirk F. van HeldenEmail author
  • Mohammad S. Imtiaz
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1124)

Abstract

Veins exhibit spontaneous contractile activity, a phenomenon generally termed vasomotion. This is mediated by spontaneous rhythmical contractions of mural cells (i.e. smooth muscle cells (SMCs) or pericytes) in the wall of the vessel. Vasomotion occurs through interconnected oscillators within and between mural cells, entraining their cycles. Pharmacological studies indicate that a key oscillator underlying vasomotion is the rhythmical calcium ion (Ca2+) release-refill cycle of Ca2+ stores. This occurs through opening of inositol 1,4,5-trisphosphate receptor (IP3R)- and/or ryanodine receptor (RyR)-operated Ca2+ release channels in the sarcoplasmic/endoplasmic (SR/ER) reticulum and refilling by the SR/ER reticulum Ca2+ATPase (SERCA). Released Ca2+ from stores near the plasma membrane diffuse through the cytosol to open Ca2+-activated chloride (Cl) channels, this generating inward current through an efflux of Cl. The resultant depolarisation leads to the opening of voltage-dependent Ca2+ channels and possibly increased production of IP3, which through Ca2+-induced Ca2+ release (CICR) of IP3Rs and/or RyRs and IP3R-mediated Ca2+ release provide a means by which store oscillators entrain their activity. Intercellular entrainment normally involves current flow through gap junctions that interconnect mural cells and in many cases this is aided by additional connectivity through the endothelium. Once entrainment has occurred the substantial Ca2+ entry that results from the near-synchronous depolarisations leads to rhythmical contractions of the mural cells, this often leading to vessel constriction. The basis for venous/venular vasomotion has yet to be fully delineated but could improve both venous drainage and capillary/venular absorption of blood plasma-associated fluids.

Keywords

Veins Smooth muscle Vasomotion Cellular rhythms Coupled oscillator-based entrainment Ca2+ stores Inositol 1,4,5-trisphosphate receptors Ryanodine receptors Cardiac muscle Pericytes 

References

  1. 1.
    dela Paz NG, D’Amore PA. Arterial versus venous endothelial cells. Cell Tissue Res. 2009;335(1):5–16.CrossRefGoogle Scholar
  2. 2.
    Reed KE, Westphale EM, Larson DM, Wang HZ, Veenstra RD, Beyer EC. Molecular cloning and functional expression of human connexin37, an endothelial cell gap junction protein. J Clin Invest. 1993;91(3):997–1004.PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Bruzzone R, Haefliger JA, Gimlich RL, Paul DL. Connexin40, a component of gap junctions in vascular endothelium, is restricted in its ability to interact with other connexins. Mol Biol Cell. 1993;4(1):7–20.PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Pepper MS, Montesano R, el Aoumari A, Gros D, Orci L, Meda P. Coupling and connexin 43 expression in microvascular and large vessel endothelial cells. Am J Phys. 1992;262(5 Pt 1):C1246–57.CrossRefGoogle Scholar
  5. 5.
    Hill CE, Rummery N, Hickey H, Sandow SL. Heterogeneity in the distribution of vascular gap junctions and connexins: implications for function. Clin Exp Pharmacol Physiol. 2002;29(7):620–5.PubMedCrossRefPubMedCentralGoogle Scholar
  6. 6.
    Haddock RE, Hill CE. Rhythmicity in arterial smooth muscle. J Physiol. 2005;566(Pt 3):645–56.PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Hashitani H, Mitsui R, Shimizu Y, Higashi R, Nakamura K. Functional and morphological properties of pericytes in suburothelial venules of the mouse bladder. Br J Pharmacol. 2012;167(8):1723–36.PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Franklin KT. The physiology and pharmacology of veins. Physiol Rev. 1928;8:346–66.CrossRefGoogle Scholar
  9. 9.
    Liu R, Feng H-Z, Jin J-P. Physiological contractility of cardiomyocytes in the wall of mouse and rat azygos vein. Am J Physiol Cell Physiol. 2014;306(7):C697–704.PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Yoffey JM, Coutice C. Lymphatics, lymph and the lymphomyeloid complex. New York: Academic Press; 1970.Google Scholar
  11. 11.
    Barrowman JA. Physiology of the gastro-intestinal lymphatic system. Cambridge: Cambridge University Press; 1978.Google Scholar
  12. 12.
    Jones TW. Discovery that the veins of the bat’s wing (which are furnished with valves) are endowed with rhythmical contractility, and that the onward flow of blood is accelerated by each contraction. Phil Trans R Soc Lond. 1852;142:131–46.  https://doi.org/10.1098/rstl.1852.0011.CrossRefGoogle Scholar
  13. 13.
    Florey HW. Observations on the contractility of lacteals. Part I. J Physiol (Lond). 1927;62:267–72.CrossRefGoogle Scholar
  14. 14.
    Mislin H. Active contractility of the lymphangion and coordination of lymphangion chains. Experientia. 1976;32(7):820–2.PubMedCrossRefPubMedCentralGoogle Scholar
  15. 15.
    Crowe MJ, von der Weid PY, Brock JA, van Helden DF. Co-ordination of contractile activity in guinea-pig mesenteric lymphatics. J Physiol (Lond). 1997;500(Pt 1):235–44.CrossRefGoogle Scholar
  16. 16.
    Caggiati A, Phillips M, Lametschwandtner A, Allegra C. Valves in small veins and venules. Eur J Vasc Endovasc Surg. 2006;32(4):447–52.PubMedCrossRefPubMedCentralGoogle Scholar
  17. 17.
    Funaki S, Bohr DF. Electrical and mechanical activity of isolated vascular smooth muscle of the rat. Nature. 1964;203:192–4.PubMedCrossRefPubMedCentralGoogle Scholar
  18. 18.
    Cuthbert AW, Sutter MC. Electrical activity of a mammalian vein. Nature. 1964;202:95.PubMedCrossRefPubMedCentralGoogle Scholar
  19. 19.
    Axelsson J, Wahlstrom B, Johansson B, Jonsson O. Influence of the ionic environment on spontaneous electrical and mechanical activity of the rat portal vein. Circ Res. 1967;21(5):609–18.PubMedCrossRefPubMedCentralGoogle Scholar
  20. 20.
    Holman ME, Kasby CB, Suthers MB, Wilson JA. Some properties of the smooth muscle of rabbit portal vein. J Physiol. 1968;196(1):111–32.PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Gunn JA, Chavasse FB. The action of adrenin on veins. Proc R Soc B. 1913;86(586):192–7.CrossRefGoogle Scholar
  22. 22.
    Mitsui R, Miyamoto S, Takano H, Hashitani H. Properties of submucosal venules in the rat distal colon. Br J Pharmacol. 2013;170(5):968–77.PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Mitsui R, Hashitani H. Functional properties of submucosal venules in the rat stomach. Pflugers Arch. 2015;467(6):1327–42.PubMedCrossRefPubMedCentralGoogle Scholar
  24. 24.
    Mitsui R, Hashitani H. Mechanisms underlying spontaneous constrictions of postcapillary venules in the rat stomach. Pflugers Arch. 2016;468(2):279–91.PubMedCrossRefPubMedCentralGoogle Scholar
  25. 25.
    Ito Y, Kuriyama H. Membrane properties of the smooth-muscle fibres of the guinea-pig portal vein. J Physiol. 1971;214(3):427–41.PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Suzuki H. Effects of endogenous and exogenous noradrenaline on the smooth muscle of guinea-pig mesenteric vein. J Physiol. 1981;321:495–512.PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Van Helden DF. Spontaneous and noradrenaline-induced transient depolarizations in the smooth muscle of guinea-pig mesenteric vein. J Physiol. 1991;437:511–41.PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Benham CD, Bolton TB. Spontaneous transient outward currents in single visceral and vascular smooth muscle cells of the rabbit. J Physiol. 1986;381:385–406.PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Berridge MJ. Inositol trisphosphate and diacylglycerol as second messengers. Biochem J. 1984;220(2):345–60.PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Berridge MJ, Irvine RF. Inositol trisphosphate, a novel second messenger in cellular signal transduction. Nature. 1984;312(5992):315–21.PubMedCrossRefPubMedCentralGoogle Scholar
  31. 31.
    Van Helden DF, von der Weid P-Y, Crowe MJ. Electrophysiology of lymphatic smooth muscle. In: Reed RK, McHale NG, Bert JL, Winlove CP, Laine GA, editors. Interstitium, connective tissue and lymphatics. London: Portland Press; 1995. p. 221–36.Google Scholar
  32. 32.
    Van Helden DF. Electrophysiology of neuromuscular transmission in guinea-pig mesenteric veins. J Physiol (Lond). 1988;401:469–88.CrossRefGoogle Scholar
  33. 33.
    Van Helden DF. An alpha-adrenoceptor-mediated chloride conductance in mesenteric veins of the guinea-pig. J Physiol (Lond). 1988;401:489–501.CrossRefGoogle Scholar
  34. 34.
    Wang Q, Hogg RC, Large WA. Properties of spontaneous inward currents recorded in smooth muscle cells isolated from the rabbit portal vein. J Physiol. 1992;451:525–37.PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Pacaud P, Loirand G. Release of Ca2+ by noradrenaline and ATP from the same Ca2+ store sensitive to both InsP3 and Ca2+ in rat portal vein myocytes. J Physiol. 1995;484(Pt 3):549–55.PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Gordienko DV, Bolton TB. Crosstalk between ryanodine receptors and IP(3) receptors as a factor shaping spontaneous Ca(2+)-release events in rabbit portal vein myocytes. J Physiol. 2002;542(Pt 3):743–62.PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Nagasaki K, Fleischer S. Ryanodine sensitivity of the calcium release channel of sarcoplasmic reticulum. Cell Calcium. 1988;9(1):1–7.PubMedCrossRefPubMedCentralGoogle Scholar
  38. 38.
    Van Helden DF. Spontaneous activity in the smooth muscle of lymphatic vessels of the guinea-pig mesentery. Proc Int Union Physiol Sci. 1989;XVII:4386.Google Scholar
  39. 39.
    Van Helden DF. Pacemaker potentials in lymphatic smooth muscle of the guinea-pig mesentery. J Physiol. 1993;471:465–79.PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Burt RP. Phasic contractions of the rat portal vein depend on intracellular Ca2+ release stimulated by depolarization. Am J Physiol Heart Circ Physiol. 2003;284(5):H1808–17.PubMedCrossRefPubMedCentralGoogle Scholar
  41. 41.
    Spencer NJ, Greenwood IA. Characterization of properties underlying rhythmicity in mouse portal vein. Auton Neurosci. 2003;104(2):73–82.PubMedCrossRefPubMedCentralGoogle Scholar
  42. 42.
    Griffith TM, Edwards DH. Fractal analysis of role of smooth muscle Ca2+ fluxes in genesis of chaotic arterial pressure oscillations. Am J Phys. 1994;266(5 Pt 2):H1801–11.Google Scholar
  43. 43.
    Edwards DH, Griffith TM. Entrained ion transport systems generate the membrane component of chaotic agonist-induced vasomotion. Am J Phys. 1997;273(2 Pt 2):H909–20.Google Scholar
  44. 44.
    Noble D. The surprising heart: a review of recent progress in cardiac electrophysiology. J Physiol. 1984;353:1–50.PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Bogdanov KY, Vinogradova TM, Lakatta EG. Sinoatrial nodal cell ryanodine receptor and Na(+)-Ca(2+) exchanger: molecular partners in pacemaker regulation. Circ Res. 2001;88(12):1254–8.PubMedCrossRefPubMedCentralGoogle Scholar
  46. 46.
    Vinogradova TM, Zhou YY, Maltsev V, Lyashkov A, Stern M, Lakatta EG. Rhythmic ryanodine receptor Ca2+ releases during diastolic depolarization of sinoatrial pacemaker cells do not require membrane depolarization. Circ Res. 2004;94(6):802–9.PubMedCrossRefPubMedCentralGoogle Scholar
  47. 47.
    Lakatta EG, Maltsev VA, Vinogradova TM. A coupled SYSTEM of intracellular Ca2+ clocks and surface membrane voltage clocks controls the timekeeping mechanism of the heart’s pacemaker. Circ Res. 2010;106(4):659–73.PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Parker I, Yao Y. Regenerative release of calcium from functionally discrete subcellular stores by inositol trisphosphate. Proc Biol Sci. 1991;246(1317):269–74.PubMedCrossRefPubMedCentralGoogle Scholar
  49. 49.
    Parker I, Choi J, Yao Y. Elementary events of InsP3-induced Ca2+ liberation in Xenopus oocytes: hot spots, puffs and blips. Cell Calcium. 1996;20(2):105–21.PubMedCrossRefPubMedCentralGoogle Scholar
  50. 50.
    Cheng H, Lederer WJ, Cannell MB. Calcium sparks: elementary events underlying excitation-contraction coupling in heart muscle. Science. 1993;262(5134):740–4.PubMedCrossRefPubMedCentralGoogle Scholar
  51. 51.
    Strogatz SH, Stewart I. Coupled oscillators and biological synchronization. Sci Am. 1993;269(6):102–9.PubMedCrossRefPubMedCentralGoogle Scholar
  52. 52.
    van der Pol B, van der Mark J. The heartbeat considered as a relaxation oscillation, and an electrical model of the heart. Phil Magn. 1926;6(Suppl):763–75.Google Scholar
  53. 53.
    Woods NM, Cuthbertson KS, Cobbold PH. Repetitive transient rises in cytoplasmic free calcium in hormone-stimulated hepatocytes. Nature. 1986;319(6054):600–2.PubMedCrossRefPubMedCentralGoogle Scholar
  54. 54.
    Jacob R, Merritt JE, Hallam TJ, Rink TJ. Repetitive spikes in cytoplasmic calcium evoked by histamine in human endothelial cells. Nature. 1988;335(6185):40–5.PubMedCrossRefPubMedCentralGoogle Scholar
  55. 55.
    Wakui M, Potter BV, Petersen OH. Pulsatile intracellular calcium release does not depend on fluctuations in inositol trisphosphate concentration. Nature. 1989;339(6222):317–20.PubMedCrossRefPubMedCentralGoogle Scholar
  56. 56.
    Berridge MJ. Inositol trisphosphate and calcium signalling. Nature. 1993;361(6410):315–25.PubMedCrossRefPubMedCentralGoogle Scholar
  57. 57.
    Nelsen TS, Becker JC. Simulation of the electrical and mechanical gradient of the small intestine. Am J Phys. 1968;214(4):749–57.CrossRefGoogle Scholar
  58. 58.
    Diamant NE, Rose PK, Davison EJ. Computer simulation of intestinal slow-wave frequency gradient. Am J Phys. 1970;219(6):1684–90.CrossRefGoogle Scholar
  59. 59.
    Sarna SK, Daniel EE. Electrical stimulation of small intestinal electrical control activity. Gastroenterology. 1975;69(3):660–7.PubMedCrossRefPubMedCentralGoogle Scholar
  60. 60.
    Bortoff A. Myogenic control of intestinal motility. Physiol Rev. 1976;56(2):418–34.PubMedCrossRefPubMedCentralGoogle Scholar
  61. 61.
    Daniel EE, Sarna S. The generation and conduction of activity in smooth muscle. Annu Rev Pharmacol Toxicol. 1978;18:145–66.PubMedCrossRefPubMedCentralGoogle Scholar
  62. 62.
    Daniel EE, Bardakjian BL, Huizinga JD, Diamant NE. Relaxation oscillator and core conductor models are needed for understanding of GI electrical activities. Am J Physiol. 1994;266(3 Pt 1):G339–49.PubMedPubMedCentralGoogle Scholar
  63. 63.
    Sanders KM. A case for Interstitial cells of Cajal as pacemakers and mediators of neurotransmission in the gastrointestinal tract. Gastroenterology. 1996;111:492–515.PubMedCrossRefPubMedCentralGoogle Scholar
  64. 64.
    Publicover NG. Generation and propagation of rhythmicity in gastrointestinal smooth muscle. In: Huizinga JD, editor. Pacemaker activity and intercellular communication. Ann Arbor, MI: CRC; 1995. p. 175–90.Google Scholar
  65. 65.
    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.PubMedCrossRefPubMedCentralGoogle Scholar
  66. 66.
    Lammers WJ, Stephen B. Origin and propagation of individual slow waves along the intact feline small intestine. Exp Physiol. 2008;93(3):334–46.PubMedCrossRefPubMedCentralGoogle Scholar
  67. 67.
    Huizinga JD, Chen JH, Zhu YF, Pawelka A, McGinn RJ, Bardakjian BL, et al. The origin of segmentation motor activity in the intestine. Nat Commun. 2014;5:3326.PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Parsons SP, Huizinga JD. Effects of gap junction inhibition on contraction waves in the murine small intestine in relation to coupled oscillator theory. Am J Physiol Gastrointest Liver Physiol. 2015;308(4):G287–97.PubMedCrossRefPubMedCentralGoogle Scholar
  69. 69.
    Liu LW, Thuneberg L, Huizinga JD. Cyclopiazonic acid, inhibiting the endoplasmic reticulum calcium pump, reduces the canine colonic pacemaker frequency. J Pharmacol Exp Therap. 1995;275(2):1058–68.Google Scholar
  70. 70.
    Suzuki H, Hirst GD. Regenerative potentials evoked in circular smooth muscle of the antral region of guinea-pig stomach. J Physiol (Lond). 1999;517(Pt 2):563–73.CrossRefGoogle Scholar
  71. 71.
    Edwards FR, Hirst GD, Suzuki H. Unitary nature of regenerative potentials recorded from circular smooth muscle of guinea-pig antrum. J Physiol (Lond). 1999;519(Pt 1):235–50.CrossRefGoogle Scholar
  72. 72.
    Van Helden DF, Imtiaz MS, Nurgaliyeva K, von der Weid P, Dosen PJ. Role of calcium stores and membrane voltage in the generation of slow wave action potentials in guinea-pig gastric pylorus. J Physiol. 2000;524(Pt 1):245–65.PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    Zhu MH, Kim TW, Ro S, Yan W, Ward SM, Koh SD, et al. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Van Helden DF, Zhao J. Lymphatic vasomotion. Clin Exp Physiol Pharmacol. 2000;27:1014–8.CrossRefGoogle Scholar
  75. 75.
    Allbritton NL, Meyer T, Stryer L. Range of messenger action of calcium ion and inositol 1,4,5-trisphosphate. Science. 1992;258(5089):1812–5.PubMedCrossRefPubMedCentralGoogle Scholar
  76. 76.
    van Helden DF, Imtiaz MS. Ca2+ phase waves: a basis for cellular pacemaking and long-range synchronicity in the guinea-pig gastric pylorus. J Physiol. 2003;548(1):271–96.PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Itoh T, Seki N, Suzuki S, Ito S, Kajikuri J, Kuriyama H. Membrane hyperpolarization inhibits agonist-induced synthesis of inositol 1,4,5-trisphosphate in rabbit mesenteric artery. J Physiol. 1992;451:307–28.PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  79. 79.
    Peng H, Matchkov V, Ivarsen A, Aalkjaer C, Nilsson H. Hypothesis for the initiation of vasomotion. Circ Res. 2001;88(8):810–5.CrossRefGoogle Scholar
  80. 80.
    Lee HK, Sanders KM. Comparison of ionic currents from interstitial cells and smooth muscle cells of canine colon. J Physiol. 1993;460:135–52.PubMedPubMedCentralCrossRefGoogle Scholar
  81. 81.
    Kim YC, Koh SD, Sanders KM. Voltage-dependent inward currents of interstitial cells of Cajal from murine colon and small intestine. J Physiol. 2002;541(Pt 3):797–810.PubMedPubMedCentralGoogle Scholar
  82. 82.
    Kito Y, Fukuta H, Suzuki H. Components of pacemaker potentials recorded from the guinea pig stomach antrum. Pflugers Arch. 2002;445(2):202–17.CrossRefGoogle Scholar
  83. 83.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Kito Y, Ward SM, Sanders KM. Pacemaker potentials generated by interstitial cells of Cajal in the murine intestine. Am J Physiol Cell Physiol. 2005;288(3):C710–20.PubMedCrossRefPubMedCentralGoogle Scholar
  85. 85.
    Edwards FR, Hirst GD. An electrical description of the generation of slow waves in the antrum of the guinea-pig. J Physiol. 2005;564(Pt 1):213–32.PubMedCrossRefPubMedCentralGoogle Scholar
  86. 86.
    Zheng H, Park KS, Koh SD, Sanders KM. Expression and function of a T-type Ca2+ conductance in interstitial cells of Cajal of the murine small intestine. Am J Physiol Cell Physiol. 2014;306(7):C705–13.PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Zhu MH, Sung TS, O’Driscoll K, Koh SD, Sanders KM. Intracellular Ca(2+) release from endoplasmic reticulum regulates slow wave currents and pacemaker activity of interstitial cells of Cajal. Am J Physiol Cell Physiol. 2015;308(8):C608–20.PubMedPubMedCentralCrossRefGoogle Scholar
  88. 88.
    Wei R, Parsons SP, Huizinga JD. Network properties of interstitial cells of Cajal affect intestinal pacemaker activity and motor patterns, according to a mathematical model of weakly coupled oscillators. Exp Physiol. 2017;102(3):329–46.PubMedCrossRefPubMedCentralGoogle Scholar
  89. 89.
    Lakatta EG, Vinogradova T, Lyashkov A, Sirenko S, Zhu W, Ruknudin A, et al. The integration of spontaneous intracellular Ca2+ cycling and surface membrane ion channel activation entrains normal automaticity in cells of the heart’s pacemaker. Ann N Y Acad Sci. 2006;1080:178–206.PubMedCrossRefPubMedCentralGoogle Scholar
  90. 90.
    Maltsev VA, Lakatta EG. Synergism of coupled subsarcolemmal Ca2+ clocks and sarcolemmal voltage clocks confers robust and flexible pacemaker function in a novel pacemaker cell model. Am J Physiol Heart Circ Physiol. 2009;296(3):H594–615.PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Faussone Pellegrini MS, Cortesini C, Romagnoli P. [Ultrastructure of the tunica muscularis of the cardial portion of the human esophagus and stomach, with special reference to the so-called Cajal’s interstitial cells]. Arch Ital Anat Embriol. 1977;82(2):157–77.Google Scholar
  92. 92.
    Thuneberg L. Interstitial cells of Cajal: intestinal pacemaker cells? Adv Anat Embryol Cell Biol. 1982;71:1–130.CrossRefGoogle Scholar
  93. 93.
    Ward SM, Burns AJ, Torihashi S, Sanders KM. Mutation of the proto-oncogene c-kit blocks development of interstitial cells and electrical rhythmicity in murine intestine. J Physiol. 1994;480(Pt 1):91–7.PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Huizinga JD, Thuneberg L, Kluppel M, Malysz J, Mikkelsen HB, Bernstein A. W/kit gene required for interstitial cells of Cajal and for intestinal pacemaker activity. Nature. 1995;373(6512):347–9.PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Komuro T, Seki K, Horiguchi K. Ultrastructural characterization of the interstitial cells of Cajal. Arch Histol Cytol. 1999;62(4):295–316.CrossRefGoogle Scholar
  96. 96.
    Sergeant GP, Hollywood MA, McCloskey KD, Thornbury KD, McHale NG. Specialised pacemaking cells in the rabbit urethra. J Physiol. 2000;526(Pt 2):359–66.PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Lang RJ, Hashitani H. Role of prostatic interstitial cells in prostate motility. J Smooth Muscle Res. 2017;53(0):57–72.PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    Hashitani H, Edwards FR. Spontaneous and neurally activated depolarizations in smooth muscle cells of the guinea-pig urethra. J Physiol. 1999;514(Pt 2):459–70.PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Shigemasa Y, Lam M, Mitsui R, Hashitani H. Voltage dependence of slow wave frequency in the guinea pig prostate. J Urol. 2014;192(4):1286–92.CrossRefGoogle Scholar
  101. 101.
    Meyling HA. Structure and significance of the peripheral extension of the autonomic nervous system. J Comp Neurol. 1953;99(3):495–543.PubMedCrossRefPubMedCentralGoogle Scholar
  102. 102.
    Dahl E, Nelson E. Electron microscopic observations on human intracranial arteries. II. Innervation. Arch Neurol. 1964;10:158–64.PubMedCrossRefPubMedCentralGoogle Scholar
  103. 103.
    McCloskey KD, Hollywood MA, Thornbury KD, Ward SM, McHale NG. Kit-like immunopositive cells in sheep mesenteric lymphatic vessels. Cell Tissue Res. 2002;310(1):77–84.PubMedCrossRefPubMedCentralGoogle Scholar
  104. 104.
    Bolton TB, Gordienko DV, Povstyan OV, Harhun MI, Pucovsky V. Smooth muscle cells and interstitial cells of blood vessels. Cell Calcium. 2004;35(6):643–57.PubMedCrossRefPubMedCentralGoogle Scholar
  105. 105.
    Pucovsky V, Moss RF, Bolton TB. Non-contractile cells with thin processes resembling interstitial cells of Cajal found in the wall of guinea-pig mesenteric arteries. J Physiol. 2003;552(Pt 1):119–33.PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    Ghose D, Jose L, Manjunatha S, Rao MS, Rao JP. Inherent rhythmicity and interstitial cells of Cajal in a frog vein. J Biosci. 2008;33(5):755–9.PubMedCrossRefPubMedCentralGoogle Scholar
  107. 107.
    Morel E, Meyronet D, Thivolet-Bejuy F, Chevalier P. Identification and distribution of interstitial Cajal cells in human pulmonary veins. Heart Rhythm. 2008;5(7):1063–7.PubMedCrossRefPubMedCentralGoogle Scholar
  108. 108.
    Komuro T, Burnstock G. The fine structure of smooth muscle cells and their relationship to connective tissue in the rabbit portal vein. Cell Tissue Res. 1980;210(2):257–67.PubMedCrossRefPubMedCentralGoogle Scholar
  109. 109.
    Povstyan OV, Gordienko DV, Harhun MI, Bolton TB. Identification of interstitial cells of Cajal in the rabbit portal vein. Cell Calcium. 2003;33(4):223–39.PubMedCrossRefPubMedCentralGoogle Scholar
  110. 110.
    Hermsmeyer K. Multiple pacemaker sites in spontaneously active vascular muscle. Circ Res. 1973;33(2):244–51.PubMedCrossRefPubMedCentralGoogle Scholar
  111. 111.
    Harhun MI, Gordienko DV, Povstyan OV, Moss RF, Bolton TB. Function of interstitial cells of Cajal in the rabbit portal vein. Circ Res. 2004;95(6):619–26.PubMedCrossRefPubMedCentralGoogle Scholar
  112. 112.
    Heberlein KR, Straub AC, Isakson BE. The myoendothelial junction: breaking through the matrix? Microcirculation. 2009;16(4):307–22.PubMedPubMedCentralCrossRefGoogle Scholar
  113. 113.
    von der Weid PY, Van Helden DF. Functional electrical properties of the endothelium in lymphatic vessels of the guinea-pig mesentery. J Physiol. 1997;504(Pt 2):439–51.PubMedPubMedCentralCrossRefGoogle Scholar
  114. 114.
    Roizes S, von der Weid P-Y. Oubain blocks EDNO-mediated relaxation in mesenteric veins and EDHF-mediated relaxation in mesenteric arteries of the guinea pig. In: Vanhoutte PM, editor. EDHF 2002. Boca Raton, FL: CRC Press; 2005. p. 297–306.Google Scholar
  115. 115.
    Yokoyama S, Ohhashi T. Effects of acetylcholine on spontaneous contractions in isolated bovine mesenteric lymphatics. Am J Phys. 1993;264(5 Pt 2):H1460–4.Google Scholar
  116. 116.
    Reeder LB, Yang LH, Ferguson MK. Modulation of lymphatic spontaneous contractions by EDRF. J Surg Res. 1994;56(6):620–5.PubMedCrossRefPubMedCentralGoogle Scholar
  117. 117.
    von der Weid PY, Crowe MJ, Van Helden DF. Endothelium-dependent modulation of pacemaking in lymphatic vessels of the guinea-pig mesentery. J Physiol. 1996;493(Pt 2):563–75.PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    Ignarro LJ, Gold ME, Buga GM, Byrns RE, Wood KS, Chaudhuri G, et al. Basic polyamino acids rich in arginine, lysine, or ornithine cause both enhancement of and refractoriness to formation of endothelium-derived nitric oxide in pulmonary artery and vein. Circ Res. 1989;64(2):315–29.PubMedCrossRefPubMedCentralGoogle Scholar
  119. 119.
    Gao Y, Zhou H, Raj JU. Endothelium-derived nitric oxide plays a larger role in pulmonary veins than in arteries of newborn lambs. Circ Res. 1995;76(4):559–65.PubMedCrossRefPubMedCentralGoogle Scholar
  120. 120.
    Gao Y, Raj JU. Role of veins in regulation of pulmonary circulation. Am J Physiol Lung Cell Mol Physiol. 2005;288(2):L213–26.PubMedCrossRefPubMedCentralGoogle Scholar
  121. 121.
    Shimokawa H. 2014 Williams Harvey Lecture: importance of coronary vasomotion abnormalities-from bench to bedside. Eur Heart J. 2014;35(45):3180–93.PubMedCrossRefPubMedCentralGoogle Scholar
  122. 122.
    Dunham EW, Haddox MK, Goldberg ND. Alteration of vein cyclic 3′:5′ nucleotide concentrations during changes in contractility. Proc Natl Acad Sci U S A. 1974;71(3):815–9.PubMedPubMedCentralCrossRefGoogle Scholar
  123. 123.
    Morgan SJ, Deshpande DA, Tiegs BC, Misior AM, Yan H, Hershfeld AV, et al. β-Agonist-mediated relaxation of airway smooth muscle is protein kinase A-dependent. J Biol Chem. 2014;289(33):23065–74.PubMedPubMedCentralCrossRefGoogle Scholar
  124. 124.
    von der Weid PY, Van Helden DF. Beta-adrenoceptor-mediated hyperpolarization in lymphatic smooth muscle of guinea pig mesentery. Am J Phys. 1996;270(5 Pt 2):H1687–95.Google Scholar
  125. 125.
    Chan AK, von der Weid PY. 5-HT decreases contractile and electrical activities in lymphatic vessels of the guinea-pig mesentery: role of 5-HT 7-receptors. Br J Pharmacol. 2003;139(2):243–54.PubMedPubMedCentralCrossRefGoogle Scholar
  126. 126.
    Hosaka K, Rayner SE, von der Weid PY, Zhao J, Imtiaz MS, van Helden DF. Calcitonin gene-related peptide activates different signaling pathways in mesenteric lymphatics of guinea pigs. Am J Physiol Heart Circ Physiol. 2006;290(2):H813–22.PubMedCrossRefGoogle Scholar
  127. 127.
    Norel X. Prostanoid receptors in the human vascular wall. ScientificWorldJournal. 2007;7:1359–74.PubMedPubMedCentralCrossRefGoogle Scholar
  128. 128.
    Foudi N, Kotelevets L, Louedec L, Leseche G, Henin D, Chastre E, et al. Vasorelaxation induced by prostaglandin E2 in human pulmonary vein: role of the EP4 receptor subtype. Br J Pharmacol. 2008;154(8):1631–9.PubMedPubMedCentralCrossRefGoogle Scholar
  129. 129.
    Mironneau J, Martin C, Arnaudeau S, Jmari K, Rakotoarisoa L, Sayet I, et al. High-affinity binding sites for [3H]saxitoxin are associated with voltage-dependent sodium channels in portal vein smooth muscle. Eur J Pharmacol. 1990;184(2–3):315–9.PubMedCrossRefPubMedCentralGoogle Scholar
  130. 130.
    Cuthbert AW, Sutter MC. The effects of drugs on the relation between the action potential discharge and tension in a mammalian vein. Br J Pharmacol Chemother. 1965;25(3):592–601.PubMedPubMedCentralCrossRefGoogle Scholar
  131. 131.
    Yatani A, Seidel CL, Allen J, Brown AM. Whole-cell and single-channel calcium currents of isolated smooth muscle cells from saphenous vein. Circ Res. 1987;60(4):523–33.PubMedCrossRefPubMedCentralGoogle Scholar
  132. 132.
    Loirand G, Mironneau C, Mironneau J, Pacaud P. Two types of calcium currents in single smooth muscle cells from rat portal vein. J Physiol. 1989;412:333–49.PubMedPubMedCentralCrossRefGoogle Scholar
  133. 133.
    Arnaudeau S, Boittin FX, Macrez N, Lavie JL, Mironneau C, Mironneau J. L-type and Ca2+ release channel-dependent hierarchical Ca2+ signalling in rat portal vein myocytes. Cell Calcium. 1997;22(5):399–411.PubMedCrossRefPubMedCentralGoogle Scholar
  134. 134.
    Saleh SN, Greenwood IA. Activation of chloride currents in murine portal vein smooth muscle cells by membrane depolarization involves intracellular calcium release. Am J Physiol Cell Physiol. 2005;288(1):C122–31.PubMedCrossRefPubMedCentralGoogle Scholar
  135. 135.
    Wareing M, Bai X, Seghier F, Turner CM, Greenwood SL, Baker PN, et al. Expression and function of potassium channels in the human placental vasculature. Am J Physiol Regul Integr Comp Physiol. 2006;291(2):R437–46.PubMedCrossRefPubMedCentralGoogle Scholar
  136. 136.
    Mauricio MD, Serna E, Cortina B, Novella S, Segarra G, Aldasoro M, et al. Role of Ca2+-activated K+ channels on adrenergic responses of human saphenous vein. Am J Hypertens. 2007;20(1):78–82.PubMedCrossRefPubMedCentralGoogle Scholar
  137. 137.
    Brayden JE. Functional roles of KATP channels in vascular smooth muscle. Clin Exp Pharmacol Physiol. 2002;29(4):312–6.PubMedCrossRefPubMedCentralGoogle Scholar
  138. 138.
    Kajioka S, Kitamura K, Kuriyama H. Guanosine diphosphate activates an adenosine 5′-triphosphate-sensitive K+ channel in the rabbit portal vein. J Physiol. 1991;444:397–418.PubMedPubMedCentralCrossRefGoogle Scholar
  139. 139.
    Noack T, Edwards G, Deitmer P, Weston AH. Potassium channel modulation in rat portal vein by ATP depletion: a comparison with the effects of levcromakalim (BRL 38227). Br J Pharmacol. 1992;107(4):945–55.PubMedPubMedCentralCrossRefGoogle Scholar
  140. 140.
    Kamouchi M, Kitamura K. Regulation of ATP-sensitive K+ channels by ATP and nucleotide diphosphate in rabbit portal vein. Am J Phys. 1994;266(5 Pt 2):H1687–98.Google Scholar
  141. 141.
    Zhang HL, Bolton TB. Two types of ATP-sensitive potassium channels in rat portal vein smooth muscle cells. Br J Pharmacol. 1996;118(1):105–14.PubMedPubMedCentralCrossRefGoogle Scholar
  142. 142.
    Yamamoto T, Takahara K, Inai T, Node K, Teramoto N. Molecular analysis of ATP-sensitive K(+) channel subunits expressed in mouse portal vein. Vasc Pharmacol. 2015;75:29–39.CrossRefGoogle Scholar
  143. 143.
    Sakurai T, Terui N. Effects of sympathetically induced vasomotion on tissue-capillary fluid exchange. Am J Physiol Heart Circ Physiol. 2006;291(4):H1761–7.PubMedCrossRefPubMedCentralGoogle Scholar
  144. 144.
    Nilsson H, Aalkjaer C. Vasomotion: mechanisms and physiological importance. Mol Interv. 2003;3(2):79–89, 51.PubMedPubMedCentralCrossRefGoogle Scholar
  145. 145.
    Koenigsberger M, Sauser R, Seppey D, Beny JL, Meister JJ. Calcium dynamics and vasomotion in arteries subject to isometric, isobaric, and isotonic conditions. Biophys J. 2008;95(6):2728–38.PubMedPubMedCentralCrossRefGoogle Scholar
  146. 146.
    van Helden DF, Imtiaz MS. Ca2+ phase waves emerge. Physiol News. 2003;52:7–11.Google Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  1. 1.Faculty of Health and Medicine, School of Biomedical Sciences and PharmacyUniversity of NewcastleNewcastleAustralia
  2. 2.Department of Electrical and Computer EngineeringBradley UniversityPeoriaUSA

Personalised recommendations