Excitation-Contraction Coupling in Ureteric Smooth Muscle: Mechanisms Driving Ureteric Peristalsis

  • Theodor BurdygaEmail author
  • Richard J. Lang
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1124)


The ureter acts as a functional syncytium and is controlled by a propagating plateau-type action potential (AP) which gives rise to a wave of contraction (ureteral peristalsis) via a process called excitation-contraction (E-C)coupling. The second messenger Ca2+ activates Ca2+/calmodulin-dependent myosin light chain kinase-dependent phosphorylation of 20-kDa regulatory light chains of myosin which leads to ureteric contraction. Ca2+ entry from the extracellular space via voltage-gated L-type Ca2+ channels (VGCCs) provides the major source of activator Ca2+, responsible for generation of both the AP and a Ca2+ transient that appears as an intercellular Ca2+ wave. The AP, inward Ca2+ current, Ca2+ transient and twitch contraction are all fully blocked by the selective L-type Ca2+ channel blocker nifedipine. Ca2+ entry via VGCCs, coupled to activation of Ca2+-sensitive K+ (KCa) or Cl (ClCa) channels, acts as a negative or positive feedback mechanism, respectively, to control excitability and the amplitude and duration of the plateau component of the AP, Ca2+ transient and twitch contraction. The ureter, isolated from the pelvis, is not spontaneously active. However, spontaneous activity can be initiated in the proximal and distal ureter by a variety of biological effectors such as neurotransmitters, paracrine, endocrine and inflammatory factors. Applied agonists depolarise ureteric smooth muscles cells to threshold of AP activation, initiating propagating intercellular AP-mediated Ca2+ waves to produce antegrade and/or retrograde ureteric peristalsis. Several mechanisms have been proposed to describe agonist-induced depolarization of ureteric smooth muscle, which include suppression of K+ channels, stimulation of ClCa current and activation of non-selective cation receptor/store operated channels.


Ureteric peristalsis Smooth muscle cells Contraction Calcium Ion channels Action potentials Calcium imaging 

Supplementary material

Supplementary Video 4.1

Propagating intercellular Ca2+ waves in the upper and lower segments of the guinea pig ureter. See Fig. 4.4 and text for details (MPG 2270 kb)

Supplementary Video 4.2

Effects of low concentration of Caffeine (1 mM) on Ca2+ signalling of isolated guinea pig ureteric myocytes. See Fig. 4.5 and text for details (MPG 728 kb)


  1. 1.
    Notley RG. The musculature of the human ureter. Br J Urol. 1970;42:124–7.Google Scholar
  2. 2.
    Uehara Y, Burnstock G. Demonstration of gap junctions between smooth muscle cells. J Cell Biol. 1970;44:215–7.PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Dixon JS, Gosling JA. The musculature of the human renal calices, pelvis and upper ureter. J Anat. 1982;135:129–37.PubMedPubMedCentralGoogle Scholar
  4. 4.
    Tachibana S, Takeuchi M, Uehara Y. The architecture of the musculature of the guinea-pig ureter as examined by scanning electron microscopy. J Urol. 1985;134:582–6.PubMedCrossRefGoogle Scholar
  5. 5.
    Aragona F, Artibani W, de Caro R, Pizzarella M, Passerini G. The morphological basis of ureteral peristalsis. An ultra structural study of the rat ureter. Int Urol Nephrol. 1988;20:239–50.PubMedCrossRefGoogle Scholar
  6. 6.
    Tahara H. The three-dimensional structure of the musculature and the nerve in the rabbit ureter. J Anat. 1990;170:183–91.PubMedPubMedCentralGoogle Scholar
  7. 7.
    Floyd RV, Borisova L, Bakran A, Hart A, Wray S, Burdyga T. Morphology, calcium signalling and mechanical activity in human ureter. J Urol. 2008;180:398–405.PubMedCrossRefGoogle Scholar
  8. 8.
    Wakahara T, Mori S, Ide C. Ultrastructural study of the ureter smooth muscle of the cat. Nihon Heikatsukin Gakkai Zasshi. 1986;22:63–72.PubMedCrossRefGoogle Scholar
  9. 9.
    Borysova L, Wray S, Eisner DA Burdyga T. How calcium signals in myocytes and pericytes are integrated across in situ microvascular networks and control microvascular tone. Cell Calcium. 2013;54:163–74.PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Bush KT, Vaughn DA, Li X, Rosenfield MG, Rose DW, Mendoza SA, Sanjay K, et al. Development and differentiation of the ureteric bud into the ureter in the absence of a kidney collecting system. Dev Biol. 2006;298:571–84.PubMedCrossRefGoogle Scholar
  11. 11.
    Langhorst H, Jutter R, Groneberg D, Mohtashamdolatshahi A, Pelz L, Purfürst B, et al. The IgCAM CLMP is required for intestinal and ureteral smooth muscle contraction by regulating Connexin 43 and 45 expression in mice. Dis Model Mech. 2018;11:dmm.032128. Scholar
  12. 12.
    Sleator W, Butcher HR. Action potentials and pressure changes in ureteral peristaltic waves. Am J Phys. 1955;180:261–76.CrossRefGoogle Scholar
  13. 13.
    Kondo A. The contraction of the ureter. Observations in normal human and dog ureters. Nagoya J Med Sci. 1969;32:387–94.Google Scholar
  14. 14.
    Tindall AR. Preliminary observations on the mechanical and electrical activity of the rat ureter. J Physiol. 1972;223:633–475.PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Ohhashi T, Miyazawa T, Azuma T. Conduction velocity of peristaltic waves in the in vivo ureter: application of a new diameter guage. Experientia. 1981;37:377–8.PubMedCrossRefGoogle Scholar
  16. 16.
    Tsuchiya T, Takei N. Pressure responses and conduction of peristaltic wave in guinea-pig ureter. Jpn J Physiol. 1990;40:139–49.PubMedCrossRefGoogle Scholar
  17. 17.
    Prosser CL, Smith CE, Melton CE. Conduction of action potentials in the ureter of the rat. Am J Phys. 1955;180:651–60.CrossRefGoogle Scholar
  18. 18.
    Kobayashi M. Conduction velocity in various regions of the ureter. Tohoku J Exp Med. 1964;83:220–4.PubMedCrossRefGoogle Scholar
  19. 19.
    Hammad FT, Lammers WJ, Stephen B, Lubbad L. Propagation characteristics of the electrical impulse the normal and obstructed ureter as determined at high electrophysiological resolution. Br J Urol. 2011;108:E36–42.CrossRefGoogle Scholar
  20. 20.
    Ishikawa S, Ikeda O. Recovery curve and conduction of action potentials in the ureter of guinea pig. Jpn J Physiol. 1996;10:1–12.CrossRefGoogle Scholar
  21. 21.
    Tscholl R, Osypka P, Goetlin J, Zingg E. Measurement of the velocity and rate of ureteral contractions with a video-integrator in a model, in animals, and in humans, peroperatively and with intact body surface. Investig Urol. 1974;12:224–32.Google Scholar
  22. 22.
    Kuriyama H, Osa T, Toida N. Membrane properties of the smooth muscle of guinea-pig ureter. J Physiol. 1967;191:225–38.PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Lang RJ, Zoltkowski BZ, Hammer JM, Meeker WF, Wendt I. Electrical characterization of interstitial cells of Cajal-like cells and smooth muscle cells isolated from the mouse ureteropelvic junction. J Urol. 2007;177:1573–80.PubMedCrossRefPubMedCentralGoogle Scholar
  24. 24.
    Hashitani H, Nguyen MJ, Noda H, Mitsui R, Higashi R, Ohta K, et al. Interstitial cell modulation of pyeloureteric peristalsis in the mouse renal pelvis examined using FIBSEM tomography and calcium indicators. Pflugers Arch. 2017;469:797–813.PubMedCrossRefGoogle Scholar
  25. 25.
    Santicioli P, Maggi CA. Effect of 18β-glycyrrhetinic acid on electromechanical coupling in the guinea-pig renal pelvis and ureter. Br J Pharmacol. 2000;129:163–9.PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Kobayashi M. Relationship between membrane potential and spike configuration recorded by sucrose gap method in the ureter smooth muscle. Comp Biochem Physiol. 1971;38A:301–8.CrossRefGoogle Scholar
  27. 27.
    Vereecken RL, Hendrickx H, Casteels R. The influence of calcium on the electrical and mechanical activity of the guinea pig ureter. Urol Res. 1975;3:149–53.PubMedCrossRefGoogle Scholar
  28. 28.
    Hendrickx H, Vereecken RL, Casteels R. The influence of sodium on the electrical and mechanical activity of the ureter. Urol Res. 1975;3:159–63.PubMedGoogle Scholar
  29. 29.
    Shuba MF. The effect of sodium-free and potassium-free solutions, ionic current inhibitors and ouabain on electrophysiological properties of smooth muscle of guinea-pig ureter. J Physiol. 1977;264:837–85.PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Imaizumi Y, Muraki K, Watanabe M. Ionic currents in single smooth muscle cells from the ureter of the guinea-pig. J Physiol. 1989;411:131–59.PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Lang RJ. Identification of the major membrane currents in freshly dispersed single smooth muscle cells of guinea-pig ureter. J Physiol. 1989;412:375–95.PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Sui JL, Kao CY. Roles of Ca2+ and Na+ in the inward current and action potential of guinea pig ureteral myocytes. Am J Phys. 1997;41:C535–42.CrossRefGoogle Scholar
  33. 33.
    Burdyga T, Wray S. Simultaneous measurements of electrical activity, intracellular [Ca2+] and force in intact smooth muscle. Pflugers Arch. 1997;435:182–4.PubMedCrossRefPubMedCentralGoogle Scholar
  34. 34.
    Patacchini R, Santicioli P, Zagorodnyuk V, Lazzeri M, Turini D, Maggi CA. Excitatory motor and electrical effects produced by tachykinins in the human and guinea-pig isolated ureter and guinea-pig renal pelvis. Br J Pharmacol. 1998;125:987–96.PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Bennett MR, Burnstock G, Holman ME, Walker JW. The effect of Ca2+ on plateau-type action potentials in smooth muscle. J Physiol. 1962;161:47–8.Google Scholar
  36. 36.
    Cole RS, Fry CH, Shuttleworth KE. The action of the prostaglandins on isolated human ureteric smooth muscle. Br J Urol. 1988;61:19–26.PubMedCrossRefGoogle Scholar
  37. 37.
    Aickin CC, Brading AF, Burdyga TV. Evidence for sodium-calcium exchange in the guinea-pig ureter. J Physiol. 1984;347:411–30.PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Aickin CC. Investigation of factors affecting the intracellular sodium activity in the smooth muscle of guinea-pig ureter. J Physiol. 1987;385:483–505.PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Kuriyama H, Tomita T. The action potential in the smooth muscle of the guinea pig taenia coli and ureter studied by the double sucrose-gap method. J Gen Physiol. 1970;55:147–62.PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Brading AF, Burdyga TV, Scripnyuk ZD. The effects of papaverine on the electrical and mechanical activity of the guinea-pig ureter. J Physiol. 1983;34:79–89.CrossRefGoogle Scholar
  41. 41.
    Lamont C, Burdyga T, Wray S. Intracellular Na+ measurements in guinea-pig ureteric smooth muscle using SBFI. Pflugers Arch. 1998;435:523–7.PubMedCrossRefGoogle Scholar
  42. 42.
    Aaronson PI, Benham CD. Alterations in [Ca2+]i mediated by sodium-calcium exchange in smooth muscle cells isolated from the guinea-pig ureter. J Physiol. 1989;416:1–18.PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Borisova L, Shmygol A, Wray S, Burdyga T. Evidence that Ca2+ sparks/STOCs coupling mechanism is responsible for the inhibitory effect of caffeine on the electro-mechanical coupling in guinea pig ureter smooth muscle. Cell Calcium. 2007;42:303–11.PubMedCrossRefPubMedCentralGoogle Scholar
  44. 44.
    Hertle L, Nawrath H. Stimulation of voltage-dependent contractions by calcium channel activator Bay K 8644 in the human upper urinary tract in vitro. J Urol. 1989;41:1014–8.CrossRefGoogle Scholar
  45. 45.
    Maggi CA, Giuliani S, Santicioli P. Effect of BayK 8644 and ryanodine on the refractory period, action potential and mechanical response of the guinea-pig ureter to electrical stimulation. Naunyn Schmiedeberg’s Arch Pharmacol. 1994;349:510–22.CrossRefGoogle Scholar
  46. 46.
    Shabir S, Borisova L, Wray S, Burdyga T. Rho-kinase inhibition and electromechanical coupling in rat and guinea pig ureter smooth muscle: Ca2+-dependent and -independent mechanisms. J Physiol. 2004;560:839–55.PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Shuba MF. The mechanism of the excitatory action of catecholamines and histamine on the smooth muscle of guinea-pig ureter. J Physiol. 1977;264:853–64.PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Muraki K, Imaizumi Y, Watanabe M. Effects of noradrenaline on membrane currents and action potential shape in smooth muscle cells from guinea-pig ureter. J Physiol. 1994;481:617–27.PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Burdyga T, Wray S. The relationship between the action potential, intracellular calcium and force in intact phasic guinea-pig uretic smooth muscle. J Physiol. 1999;520:867–83.PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Lang RJ. The whole-cell Ca2+channel current in single smooth muscle cells of the guinea-pig ureter. J Physiol. 1990;423:453–73.PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Imaizumi Y, Muraki K, Watanabe M. Characteristics of transient outward currents in single smooth muscle cells from the ureter of the guinea-pig. J Physiol. 1990;4(27):301–24.CrossRefGoogle Scholar
  52. 52.
    Sui JL, Kao CY. Properties of inward calcium current in guinea pig ureteral myocytes. Am J Phys. 1997;41:C543–9.CrossRefGoogle Scholar
  53. 53.
    Sui JL, Kao CY. Roles of outward potassium currents in the action potential of guinea pig ureteral myocytes. Am J Phys. 1997;273:C962–72.CrossRefGoogle Scholar
  54. 54.
    Burdyga T, Wray S. Action potential refractory period in ureter smooth muscle is set by Ca2+ sparks and BK channels. Nature. 2005;28:559–62.CrossRefGoogle Scholar
  55. 55.
    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
  56. 56.
    Burdyga T, Wray S. On the mechanisms whereby temperature affects excitation-contraction coupling in smooth muscle. J Gen Physiol. 2002;19:93–104.CrossRefGoogle Scholar
  57. 57.
    Smith RD, Borisova L, Wray S, Burdyga T. Characterisation of the ionic currents in freshly isolated rat ureter smooth muscle cells: evidence for species-dependent currents. Pflugers Arch. 2002;445:444–53.PubMedCrossRefGoogle Scholar
  58. 58.
    Borysova L, Shabir S, Walsh MP, Burdyga T. The importance of Rho-associated kinase-induced Ca2+ sensitization as a component of electromechanical and pharmacomechanical coupling in rat ureteric smooth muscle. Cell Calcium. 2011;50:393–405.PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Burdyga T, Wray S. The effect of cyclopiazonic acid on excitation-contraction coupling in guinea-pig ureteric smooth muscle. J Physiol. 1999;517:855–66.PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Maggi CA, Giuliani S, Santicioli P. Effect of the Ca2+-ATPase inhibitor, cyclopiazonic acid, on electromechanical coupling in the guinea-pig ureter. Br J Pharmacol. 1995;114:127–37.PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    Burdyga T, Wray S. Sarcoplasmic reticulum function and contractile consequences in ureteric smooth muscles. Novartis Found Symp. 2002;246:208–17.PubMedGoogle Scholar
  62. 62.
    Burdyga T, Wray S. Sarcoplasmic reticulum function in smooth muscle. Physiol Rev. 2010;90:113–78.PubMedCrossRefGoogle Scholar
  63. 63.
    Burdyga T, Taggart MJ, Crichton C, Smith G, Wray S. The mechanism of Ca2+ release from the SR of permeabilised guinea pig and rat ureteric smooth muscle. Biochim Biophys Acta. 1998;1402:109–14.PubMedCrossRefGoogle Scholar
  64. 64.
    Boittin FX, Coussin F, Morel JL, Halet G, Macrez N, Mirroneau J. Ca2+ signals mediated by Ins(1,4,5)P(3)-gated channels in rat ureteric myocytes. Biochem J. 2000;349:323–32.PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Nelson MT, Cheng H, Rubart M, Sanatana LF, Bonev AD, Knot HJ, Ledere WJ. Relaxation of arterial smooth muscle by calcium sparks. Science. 1995;270:633–7.PubMedCrossRefGoogle Scholar
  66. 66.
    Lang RJ, Zhang Y. The effects of K+ channel blockers on the spontaneous electrical and contractile activity in the proximal renal pelvis of the guinea pig. J Urol. 1996;155:332–6.PubMedCrossRefGoogle Scholar
  67. 67.
    Berridge MJ, Bootman MD, Roderick HL. Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol. 2003;4:517–29.PubMedCrossRefGoogle Scholar
  68. 68.
    Berridge MJ. Inositol triphosphate and diacylglycerol as second messengers. Biochem J. 1984;220:345–60.PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Casteels R, Hendrickx H, Vereecken R, Bulbring E. Effects of catecholamines on the electrical and mechanical activity of the guinea-pig ureter. Br J Pharmacol. 1971;43:429P.PubMedPubMedCentralGoogle Scholar
  70. 70.
    Hannappel J, Golenhofen K. The effect of catecholamines on ureteral peristalsis in different species (dog, guinea-pigs and rat). Pflugers Arch. 1974;350:55–68.PubMedCrossRefGoogle Scholar
  71. 71.
    Hertle L, Nawrath H. Calcium channel blockade in smooth muscle of the human upper urinary tract: II—effects on norepinephrine-induced activation. J Urol. 1984;132:1270–4.PubMedCrossRefGoogle Scholar
  72. 72.
    Catacutan-Labay P, Boyarski S. Bradykinin: effect on ureteral peristalsis. Science. 1996;151:78–9.CrossRefGoogle Scholar
  73. 73.
    Arrighi N, Bodel S, Zani D, Peroni A, Simeone C Mirabella G, et al. Alpha 1adrenoreceptors in human urinary tract: expression, distribution and clinical implications. Urologia. 2007;74:53–60.PubMedGoogle Scholar
  74. 74.
    Maggi CA, Parlani M, Astolfi M, Santicioli P, Rovero P, Abelli V, et al. Neurokinin receptors in the rat lower urinary tract. J Pharmacol Exp Ther. 1988;246:308–15.PubMedGoogle Scholar
  75. 75.
    Maggi CA, Santicioli P, Del Bianco E, Guiliani S. Local motor responses to bradykinin and bacterial chemotactic peptide formyl-methionyl-leucyl-phenylalanine (FMLP) in the guinea-pig isolated renal pelvis and ureter. J Urol. 1992;148:1944–50.PubMedCrossRefGoogle Scholar
  76. 76.
    Maggi CA, Santicioli P, Guiliani S, Albelli L, Melli A. The motor effect of the capsaicin sensitive inhibitory innervation of the rat ureter. Eur J Pharmacol. 1986;126:333–6.PubMedCrossRefGoogle Scholar
  77. 77.
    Eggerecks D, Raspe E, Bertrand D, Vassart G, Parmentier M. Molecular cloning, functional expression and pharmacological characterization of human bradykinin B2 receptor gene. Biochem Biophys Res Commun. 1992;187:1306–13.CrossRefGoogle Scholar
  78. 78.
    Ribeiro ASF, Fernandes VS, Martiınez MP, Lopez-Oliva ME, Barahona MV, Recio P, et al. Pre- and post-junctional bradykinin B2 receptors regulate smooth muscle tension to the pig intravesical ureter. Neurourol Urodyn. 2016;35:115–21.PubMedCrossRefGoogle Scholar
  79. 79.
    Laird JM, Roza C, Cervero F. Effects of artificial calculosis on rat ureter motility: peripheral contribution to the pain of ureteric colic. Am J Phys. 1997;272:R1409–16.Google Scholar
  80. 80.
    Streb H, Irvine RF, Berridge MJ, Schulz I. Release of Ca2+ from a non- mitochondrial store in pancreatic acinar cell by inositol 1,4,5-triphosphate. Nature. 1983;306:67–9.PubMedCrossRefGoogle Scholar
  81. 81.
    Nishizuka Y. The role of protein kinase C in cell surface signal transduction and tumor production. Nature. 1984;308:693–8.PubMedCrossRefGoogle Scholar
  82. 82.
    Weiss RM, Bassett AL, Hoffman BF. Adrenergic innervation of the ureter. Investig Urol. 1978;16:123–7.Google Scholar
  83. 83.
    Del Tacca M. Acetylcholine content of and release from isolated pelviureteral tract. Naunyn Schmiedeberg’s Arch Pharmacol. 1978;302:293–7.CrossRefGoogle Scholar
  84. 84.
    Malin JM, Deane RF, Boyarsky S. Characterisation of adrenergic receptors in human ureter. Br J Urol. 1979;42:171–4.CrossRefGoogle Scholar
  85. 85.
    Sigala S, Dellabella M, Milanese G, Formari S, Faccoli S, Palazzolo F, et al. Evidence for the presence of alpha 1 adrenoreceptorssubtypes in the human ureter. Neurourol Urodyn. 2005;24:142–8.PubMedCrossRefGoogle Scholar
  86. 86.
    Morita T, Wada I, Suzuki T, Tsuchida S. Characterization of alpha-adrenoceptor subtypes involved in regulation of ureteral fluid transport. Tohoku J Exp Med. 1987;152:111–8.PubMedCrossRefGoogle Scholar
  87. 87.
    Sakamoto K, Suri D, Rajasekaran M. Characterization of muscarinic receptor subtypes in human ureter. J Endourol. 2006;20:939–42.PubMedCrossRefGoogle Scholar
  88. 88.
    Hernandez M, Simonsen U, Prieto D, Rivera L, Garcia P, Ordaz E, et al. Different muscarinic receptor subtypes mediating the phasic activity and basal tone of pig isolated intravesical ureter. Br J Pharmacol. 1993;110:141–55.Google Scholar
  89. 89.
    Yoshida S, Kuga T. Effects of field stimulation on cholinergic fibers of the pelvic region in the isolated guinea pig ureter. Jpn J Physiol. 1980;30:415.PubMedCrossRefGoogle Scholar
  90. 90.
    Roshani H, Dabhoiwala NF, Dijkhuis T, Pfaffendorf M, Boon TA, Lamers WH. Pharmacological modulation of ureteral peristalsis in a chronically instrumented conscious pig model. I: effect of cholinergic stimulation and inhibition. J Urol. 2003;170:264–7.PubMedCrossRefGoogle Scholar
  91. 91.
    Hua XY, Saria A, Gamse R, Theodorsson-Norheim E, Brodin E, Lunberg JM. Capsaicin-induced release of multiple tachykinins (SP, neurokinin A and eledoisin-like material from guinea-pig spinal cord and ureter). Neuroscience. 1986;19:313–9.PubMedCrossRefGoogle Scholar
  92. 92.
    Hua XY, Theodorsson-Norheim E, Lundberg JM, Kinn AC, Hokfelt T, Cuello AC. Co-localization of tachykinins and CGRP in capsaicin-sensitive afferents in relation to motility effects in the human ureter in vitro. Neuroscience. 1987;23:693–703.PubMedCrossRefPubMedCentralGoogle Scholar
  93. 93.
    Jerde TJ, Saban R, Bjorling DE, et al. Distribution of neuropeptides, histamine content, and inflammatory cells in the ureter. Urology. 2000;56:173–8.PubMedCrossRefGoogle Scholar
  94. 94.
    Santicioli P, Maggi CA. Myogenic and neurogenic factors in the control of pyeloureteral motility and ureteral peristalsis. Pharmacol Rev. 1998;50:683–722.PubMedPubMedCentralGoogle Scholar
  95. 95.
    Menon M, Resnick MI. Urinary lithiasis: etiology, diagnosis, and medical management. In: Walsh PC, Retik AB, Vaughan ED, et al., editors. Campbell’s urology, vol. 4. Philadelphia: Saunders; 2002. p. 3227–92.Google Scholar
  96. 96.
    Golias C, Charalabopoulos A, Stagikas D, Charalabopoulos K, Batistatou A. The kinin system-bradykinin: biological effects and clinical implications. Multiple role of the kinin system–bradykinin. Hippokratia. 2007;11:124–8.PubMedPubMedCentralGoogle Scholar
  97. 97.
    Stoller ML, Bolton DM. Urinary stone disease. In: Tanagho EA, McAninch JW, editors. Smith’s urology. San Francisco: Lange Medical Book/McGraw-Hill; 2000. p. 291–320.Google Scholar
  98. 98.
    Yalcin S, Ertunc M, Ardicli B, Kabakus IM, Tas TS Sara Y, et al. Ureterovesical junction obstruction causes increment insmooth muscle contractility, and cholinergic and adrenergic activity in distal ureter of rabbits. J Pediatr Surg. 2013;48:1954–61.PubMedCrossRefGoogle Scholar
  99. 99.
    Canda AE, Turna B, Cinar GM, Nazli O. Physiology and pharmacology of the human ureter: basis for current and future treatments. Urol Int. 2007;78:289–98.PubMedCrossRefGoogle Scholar
  100. 100.
    Ziemba JB, Matlaga BR. Guideline of guidelines: kidney stones. Br J Urol. 2015;116:184–9.CrossRefGoogle Scholar
  101. 101.
    Mak RH, Kuo HJ. Primary ureteral reflux: emerging insights from molecular and genetic studies. Curr Opin Pediatr. 2003;15:181–5.PubMedCrossRefGoogle Scholar
  102. 102.
    Grana L, Donnellan WL, Swenson O. Effects of gram-negative bacteria on ureteral structure and function. J Urol. 1968;99:539–50.PubMedCrossRefGoogle Scholar
  103. 103.
    Teague N, Boyarsky S. Further effects of coliform bacteria on on ureteral peristalsis. J Urol. 1968;99:720–4.PubMedCrossRefGoogle Scholar
  104. 104.
    King WW, Cox CE. Bacterial inhibition of ureteral smooth muscle contractility. I. The effect of common urinary pathogens and endotoxin in an in vitro system. J Urol. 1972;108:700–5.PubMedCrossRefGoogle Scholar
  105. 105.
    Floyd RV, Winstanley C, Bakran A, Wray S, Burdyga TV. Modulation of ureteric Ca signaling and contractility in humans and rats by uropathogenic E. coli. Am J Physiol Ren Physiol. 2010;298:F900–8.CrossRefGoogle Scholar
  106. 106.
    Floyd RV, Upton M, Hultgren S, Wray S, Burdyga TV, Winstanley C. Escherichia coli-mediated impairment of ureteric contractility is uropathogenic E. coli specific. J Infect Dis. 2012;206:1589–96.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  1. 1.Department of Cellular and Molecular Physiology, Institute of Translational MedicineUniversity of LiverpoolLiverpoolUK
  2. 2.School of Biomedical Sciences, Faculty of Medicine, Nursing and Health SciencesMonash UniversityClaytonAustralia

Personalised recommendations