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Electrophysiological and Mechanical Characteristics in Human Ileal Motility: Recordings of Slow Waves Conductions and Contractions, In vitro

  • Ryoo, Seung-Bum (Department of Surgery, Seoul National University College of Medicine) ;
  • Oh, Heung-Kwon (Department of Surgery, Seoul National University College of Medicine) ;
  • Moon, Sang Hui (Department of Surgery, Seoul National University College of Medicine) ;
  • Choe, Eun Kyung (Department of Surgery, Seoul National University College of Medicine) ;
  • Yu, Sung A (Department of Surgery, Seoul National University College of Medicine) ;
  • Park, Sung-Hye (Department of Pathology, Seoul National University College of Medicine) ;
  • Park, Kyu Joo (Department of Surgery, Seoul National University College of Medicine)
  • Received : 2015.07.02
  • Accepted : 2015.08.14
  • Published : 2015.11.01

Abstract

Little human tissue data are available for slow waves and migrating motor complexes, which are the main components of small bowel motility. We investigated the electrophysiological and mechanical characteristics of human ileal motility, in vitro. Ileum was obtained from patients undergoing bowel resection. Electrophysiological microelectrode recordings for membrane potential changes and mechanical tension recordings for contraction from smooth muscle strips and ileal segments were performed. Drugs affecting the enteric nervous system were applied to measure the changes in activity. Slow waves were detected with a frequency of 9~10/min. There were no cross-sectional differences in resting membrane potential (RMP), amplitude or frequency between outer and inner circular muscle (CM), suggesting that electrical activities could be effectively transmitted from outer to inner CM. The presence of the interstitial cell of Cajal (ICC) at the linia septa was verified by immunohistochemistry. Contractions of strips and segments occurred at a frequency of 3~4/min and 1~2/min, respectively. The frequency, amplitude and area under the curve were similar between CM and LM. In segments, contractions of CM were associated with LM, but propagation varied with antegrade and retrograde directions. Atropine, $N^W$-oxide-L-arginine, and sodium nitroprusside exhibited different effects on RMP and contractions. There were no cross-sectional differences with regard to the characteristics of slow waves in CM. The frequency of contractions in smooth muscle strips and ileal segments was lower than slow waves. The directions of propagation were diverse, indicating both mixing and transport functions of the ileum.

Keywords

References

  1. Sanders KM. A case for interstitial cells of Cajal as pacemakers and mediators of neurotransmission in the gastrointestinal tract. Gastroenterology. 1996;111:492-515. https://doi.org/10.1053/gast.1996.v111.pm8690216
  2. Wingate DL. Backwards and forwards with the migrating complex. Dig Dis Sci. 1981;26:641-666. https://doi.org/10.1007/BF01367678
  3. Thuneberg L. Interstitial cells of Cajal: intestinal pacemaker cells? Adv Anat Embryol Cell Biol. 1982;71:1-130. https://doi.org/10.1007/978-3-642-68417-3_1
  4. Koh SD, Sanders KM. Stretch-dependent potassium channels in murine colonic smooth muscle cells. J Physiol. 2001;533: 155-163. https://doi.org/10.1111/j.1469-7793.2001.0155b.x
  5. Spencer NJ. Control of migrating motor activity in the colon. Curr Opin Pharmacol. 2001;1:604-610. https://doi.org/10.1016/S1471-4892(01)00103-5
  6. Spencer NJ, Sanders KM, Smith TK. Migrating motor complexes do not require electrical slow waves in the mouse small intestine. J Physiol. 2003;553:881-893. https://doi.org/10.1113/jphysiol.2003.049700
  7. Fida R, Lyster DJ, Bywater RA, Taylor GS. Colonic migrating motor complexes (CMMCs) in the isolated mouse colon. Neurogastroenterol Motil. 1997;9:99-107. https://doi.org/10.1046/j.1365-2982.1997.d01-25.x
  8. Bush TG, Spencer NJ, Watters N, Sanders KM, Smith TK. Spontaneous migrating motor complexes occur in both the terminal ileum and colon of the C57BL/6 mouse in vitro. Auton Neurosci. 2000;84:162-168. https://doi.org/10.1016/S1566-0702(00)00201-0
  9. Hara Y, Kubota M, Szurszewski JH. Electrophysiology of smooth muscle of the small intestine of some mammals. J Physiol. 1986;372:501-520. https://doi.org/10.1113/jphysiol.1986.sp016022
  10. Bauer AJ, Sarr MG, Szurszewski JH. Opioids inhibit neuromuscular transmission in circular muscle of human and baboon jejunum. Gastroenterology. 1991;101:970-976. https://doi.org/10.1016/0016-5085(91)90723-X
  11. Stark ME, Bauer AJ, Sarr MG, Szurszewski JH. Nitric oxide mediates inhibitory nerve input in human and canine jejunum. Gastroenterology. 1993;104:398-409. https://doi.org/10.1016/0016-5085(93)90407-4
  12. Farrelly AM, Ro S, Callaghan BP, Khoyi MA, Fleming N, Horowitz B, Sanders KM, Keef KD. Expression and function of KCNH2 (HERG) in the human jejunum. Am J Physiol Gastrointest Liver Physiol. 2003;284:G883-895. https://doi.org/10.1152/ajpgi.00394.2002
  13. Ryoo SB, Oh HK, Yu SA, Moon SH, Choe EK, Oh TY, Park KJ. The effects of eupatilin ($stillen^{(R)}$) on motility of human lower gastrointestinal tracts. Korean J Physiol Pharmacol. 2014;18:383-390. https://doi.org/10.4196/kjpp.2014.18.5.383
  14. Lee HT, Hennig GW, Fleming NW, Keef KD, Spencer NJ, Ward SM, Sanders KM, Smith TK. The mechanism and spread of pacemaker activity through myenteric interstitial cells of Cajal in human small intestine. Gastroenterology. 2007;132:1852-1865. https://doi.org/10.1053/j.gastro.2007.02.049
  15. Lee HT, Hennig GW, Fleming NW, Keef KD, Spencer NJ, Ward SM, Sanders KM, Smith TK. Septal interstitial cells of Cajal conduct pacemaker activity to excite muscle bundles in human jejunum. Gastroenterology. 2007;133:907-917. https://doi.org/10.1053/j.gastro.2007.06.024
  16. Sanders KM, Koh SD, Ro S, Ward SM. Regulation of gastrointestinal motility--insights from smooth muscle biology. Nat Rev Gastroenterol Hepatol. 2012;9:633-645. https://doi.org/10.1038/nrgastro.2012.168
  17. Lee HK, Sanders KM. Comparison of ionic currents from interstitial cells and smooth muscle cells of canine colon. J Physiol. 1993;460:135-152. https://doi.org/10.1113/jphysiol.1993.sp019463
  18. Ward SM, Ordog T, Koh SD, Baker SA, Jun JY, Amberg G, Monaghan K, Sanders KM. Pacemaking in interstitial cells of Cajal depends upon calcium handling by endoplasmic reticulum and mitochondria. J Physiol. 2000;525 Pt 2:355-361. https://doi.org/10.1111/j.1469-7793.2000.t01-1-00355.x
  19. Kim YC, Koh SD, Sanders KM. Voltage-dependent inward currents of interstitial cells of Cajal from murine colon and small intestine. J Physiol. 2002;541:797-810. https://doi.org/10.1113/jphysiol.2002.018796
  20. Park KJ, Hennig GW, Lee HT, Spencer NJ, Ward SM, Smith TK, Sanders KM. Spatial and temporal mapping of pacemaker activity in interstitial cells of Cajal in mouse ileum in situ. Am J Physiol Cell Physiol. 2006;290:C1411-1427. https://doi.org/10.1152/ajpcell.00447.2005
  21. Kito Y, Suzuki H. Properties of pacemaker potentials recorded from myenteric interstitial cells of Cajal distributed in the mouse small intestine. J Physiol. 2003;553:803-818. https://doi.org/10.1113/jphysiol.2003.051334
  22. Koh SD, Ward SM, Sanders KM. Ionic conductances regulating the excitability of colonic smooth muscles. Neurogastroenterol Motil. 2012;24:705-718. https://doi.org/10.1111/j.1365-2982.2012.01956.x
  23. Hennig GW, Hirst GD, Park KJ, Smith CB, Sanders KM, Ward SM, Smith TK. Propagation of pacemaker activity in the guineapig antrum. J Physiol. 2004;556:585-599. https://doi.org/10.1113/jphysiol.2003.059055
  24. Ward SM, Sanders KM. Pacemaker activity in septal structures of canine colonic circular muscle. Am J Physiol. 1990;259:G264-273.
  25. Horiguchi K, Semple GS, Sanders KM, Ward SM. Distribution of pacemaker function through the tunica muscularis of the canine gastric antrum. J Physiol. 2001;537:237-250. https://doi.org/10.1111/j.1469-7793.2001.0237k.x
  26. Sanders KM, Koh SD, Ward SM. Interstitial cells of cajal as pacemakers in the gastrointestinal tract. Annu Rev Physiol. 2006;68:307-343. https://doi.org/10.1146/annurev.physiol.68.040504.094718
  27. Hara Y, Szurszewski JH. Effect of potassium and acetylcholine on canine intestinal smooth muscle. J Physiol. 1986;372:521-537. https://doi.org/10.1113/jphysiol.1986.sp016023
  28. Iino S, Horiguchi K. Interstitial cells of cajal are involved in neurotransmission in the gastrointestinal tract. Acta Histochem Cytochem. 2006;39:145-153. https://doi.org/10.1267/ahc.06023
  29. Stark ME, Bauer AJ, Szurszewski JH. Effect of nitric oxide on circular muscle of the canine small intestine. J Physiol. 1991; 444:743-761. https://doi.org/10.1113/jphysiol.1991.sp018904
  30. Boeckxstaens GE, Pelckmans PA, Bult H, De Man JG, Herman AG, Van Maercke YM. Non-adrenergic non-cholinergic relaxation mediated by nitric oxide in the canine ileocolonic junction. Eur J Pharmacol. 1990;190:239-246. https://doi.org/10.1016/0014-2999(90)94132-H
  31. Park KJ, Baker SA, Cho SY, Sanders KM, Koh SD. Sulfurcontaining amino acids block stretch-dependent K+ channels and nitrergic responses in the murine colon. Br J Pharmacol. 2005;144:1126-1137. https://doi.org/10.1038/sj.bjp.0706154
  32. Powell AK, Fida R, Bywater RA. Motility in the isolated mouse colon: migrating motor complexes, myoelectric complexes and pressure waves. Neurogastroenterol Motil. 2003;15:257-266. https://doi.org/10.1046/j.1365-2982.2003.00412.x
  33. Huizinga JD, Stern HS, Chow E, Diamant NE, El-Sharkawy TY. Electrophysiologic control of motility in the human colon. Gastroenterology. 1985;88:500-511. https://doi.org/10.1016/0016-5085(85)90513-X
  34. Rae MG, Fleming N, McGregor DB, Sanders KM, Keef KD. Control of motility patterns in the human colonic circular muscle layer by pacemaker activity. J Physiol. 1998;510:309-320. https://doi.org/10.1111/j.1469-7793.1998.309bz.x
  35. Smith TK, Reed JB, Sanders KM. Interaction of two electrical pacemakers in muscularis of canine proximal colon. Am J Physiol. 1987;252:C290-299. https://doi.org/10.1152/ajpcell.1987.252.3.C290
  36. Choe EK, Moon JS, Moon SB, So IS, Park KJ. Electromechanical characteristics of the human colon in vitro: is there any difference between the right and left colon? Int J Colorectal Dis. 2010;25:1117-1126. https://doi.org/10.1007/s00384-010-0966-x
  37. 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;18:393-403. https://doi.org/10.1016/S0165-6147(97)90668-4

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