Voltage-dependent $Ca^{2+}$ Current Identified in Freshly Isolated Interstitial Cells of Cajal (ICC) of Guinea-pig Stomach

  • Kim, Young-Chul (Department of Physiology, Chungbuk National University, College of Medicine) ;
  • Suzuki, Hikaru (Department of Physiology, Nagoya City University Medical School) ;
  • Xu, Wen-Xie (Department of Physiology, College of Medicine, Shanghai Jiaotong University) ;
  • Hashitani, Hikaru (Department of Physiology, Nagoya City University Medical School) ;
  • Choi, Woong (Department of Pharmacology, Chungbuk National University, College of Medicine) ;
  • Yun, Hyo-Yung (Department of Surgery, Chungbuk National University, College of Medicine) ;
  • Park, Seon-Mee (Department of Internal Medicine, Chungbuk National University, College of Medicine) ;
  • Youn, Sei-Jin (Department of Internal Medicine, Chungbuk National University, College of Medicine) ;
  • Lee, Sang-Jeon (Department of Surgery, Chungbuk National University, College of Medicine) ;
  • Lee, Sang-Jin (Department of Physiology, Chungbuk National University, College of Medicine)
  • Published : 2008.12.31

Abstract

The properties of voltage dependent $Ca^{2+}$ current (VDCC) were investigated in interstitial cells of Cajal (ICC) distributed in the myenteric layer (ICC-MY) of guinea-pig antrum. In tissue, ICC-MY showed c-Kit positive reactions and produced driving potentials with the amplitude and frequency of about 62 mV and 2 times $min^{-1}$ respectively, in the presence of $1{\mu}M$ nifedipine. Single ICC-MY isolated by enzyme treatment also showed c-Kit immunohistochemical reactivity. These cells were also identified by generation of spontaneous inward current under $K^+$ -rich pipette solution. The voltage clamp experiments revealed the amplitude of - 329 pA inward current at irregular frequency. With $Cs^+$-rich pipette solution at $V_h=-80\;mV$, ICC-MY produced voltage-dependent inward currents (VDIC), and nifedipine ($1{\mu}M$) blocked VDIC. Therefore, we successfully isolated c-Kit positive single ICC from guinea-pig stomach, and found that ICC-MY potently produced dihydropiridine sensitive L-type voltage-dependent $Ca^{2+}$ currents ($VDCC_L$).

Keywords

References

  1. Beckett EAH, Ro S, Bayquinov Y, Sanders KM, Ward SM. Kit signaling is essential for development and maintenance of interstitial cells of Cajal and electrical rhythmicity in the embryonic and gastrointestinal tract. Dev Dyn 236: 60-72, 2007 https://doi.org/10.1002/dvdy.20929
  2. Cayabyab FS, DeBruin H, Jimenez M, Daniel EE. Ca^{2+}$ role in myogenic and neurogenic activities of canine ileum circular muscle. Am J Physiol 271: G1053-G1066, 1996
  3. Dickens EJ, Edward FR, Hirst GDS. Selective knockout of intramuscular interstitial cell reveals their role in the generation of slow waves in mouse stomach. J Physiol 531: 827-833, 2001 https://doi.org/10.1111/j.1469-7793.2001.0827h.x
  4. Goto K, Matsuoka S, Noma A. Two types of spontaneous depolarizations in the interstitial cells freshly prepared from the murine small intestine. J Physiol 559: 409-420, 2004
  5. Dickens EJ, Hirst GDS, Tomita T. Identification of rhythmically active cells in guinea-pig stomach. J Physiol 514: 515-531, 1999 https://doi.org/10.1111/j.1469-7793.1999.515ae.x
  6. Hamil OP, Marty A, Neher E, Sakamnn B, Sigworth FJ. Improved patch-clamp technique for high resolution current from cells ands cell-free membrane patches. Pflügers Arch 391: 85-100, 1981 https://doi.org/10.1007/BF00656997
  7. Hennig GW, Hirst GD, Park KJ, Smith CB, Sanders KM, Ward SM, Smith TK. Propagation of pacemaker activity in the guinea-pig antrum. J Physiol 556: 585-599, 2004 https://doi.org/10.1113/jphysiol.2003.059055
  8. Hirst GD, Edward FR. Generation of slow waves in the antral region of guinea-pig stomach - a stochastic process. J Physiol 535: 165-180, 2001 https://doi.org/10.1111/j.1469-7793.2001.00165.x
  9. Hirst GDS, Ward SM. Interstitial cells: involvement in rhythmicity and neural control of gut smooth muscle. J Physiol 550: 337-346, 2003 https://doi.org/10.1113/jphysiol.2003.043299
  10. 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 373: 347-349, 1995 https://doi.org/10.1038/373347a0
  11. Kim YC, Koh SD, Sanders KM. Voltage-dependent inward currents of interstitial cells of Cajal from murine colon and small intestine. J Physiol 541: 797-810, 2002 https://doi.org/10.1113/jphysiol.2002.018796
  12. Kito Y, Suzuki H. Pacemaker frequency is increased by sodium nitroprusside in the guinea pig gastric antrum. J Physiol 546: 191-205, 2003 https://doi.org/10.1113/jphysiol.2002.027607
  13. Kito Y, Ward SM, Sanders KM. Pacemaker potential generated by interstitial cells of Cajal in the murine intestine. J Physiol 288: C710-C720, 2005
  14. Kluppel M, Huizinga JD, Malysz J, Bernstein A. Developmental origin and Kit- dependent development of the interstitial cells of Cajal in the mammalian small intestine. Dev Dyn 211: 60-71, 1998 https://doi.org/10.1002/(SICI)1097-0177(199801)211:1<60::AID-AJA6>3.0.CO;2-5
  15. Koh SD, Jun JY, Kim TW, Sanders KM. A Ca^{2+}-inhibited$ non-selective cation conductance contributes to pacemaker currents in mouse interstitial cells of Cajal. J Physiol 540: 803-814, 2002 https://doi.org/10.1113/jphysiol.2001.014639
  16. Koh SD, Monaghhan K, RoS, Mason HS, Kenyon JL, Sanders KM. Novel voltage-dependent non-selective cation conductance in murine colonic myocytes. J Physiol 533: 341-355, 2001 https://doi.org/10.1111/j.1469-7793.2001.0341a.x
  17. Koh SD, Sanders KM, Ward SM. Spontaneous electrical rhythmicity in cultured interstitial cells of Cajal from the murine small intestine. J Physiol 513: 203-213, 1998 https://doi.org/10.1111/j.1469-7793.1998.203by.x
  18. Komuro T, Tokui K, Zhou DS. Identification of interstitial cells of Cajal. Histol Histopathol 11: 769-786, 1996
  19. Kubota M, Kanda E, Ida K, Sakakihara Y, Hayashi M. Severe gastrointestinal dysmotility in a patient with congenital myopathy: causal relationship to decrease of interstitial cells of Cajal. Brain Develop 27: 447-450, 2005 https://doi.org/10.1016/j.braindev.2004.10.006
  20. Lammers WJ, Stephen B, Adeghate E, Ponery S, Pozzan O. The slow wave does not propagate across the gastroduodenal junction in the isolated feline preparation. Neurogastroenterol Motil 10: 339-349, 1998 https://doi.org/10.1046/j.1365-2982.1998.00113.x
  21. Langton P, Ward SM, Carl A, Norell MA, Sanders KM. Spontaneous electrical activity of interstitial cells of Cajal isolated from canine proximal colon. Proc Natl Acad Sci 86: 7280-7284, 1989
  22. Lee HK, Sanders KM. Comparision of ionic currents from interstitial cells and smooth muscle cells of canine colon. J Physiol 460: 135-152, 1993 https://doi.org/10.1113/jphysiol.1993.sp019463
  23. Lee JI, Park HJ, Kamm MA, Talbot IC. Decreased density of interstitial cells of Cajal and neuronal cells in patients with slow-transit constipation and acquired megacolon. J Gastroenterol Hepatol 20: 1292-1298, 2005 https://doi.org/10.1111/j.1440-1746.2005.03809.x
  24. Malysz J, Richaedson D, Farraway L, Christen MOM, Huizinga JD. Generaion of slow wave type action potentials in the mouse small intestine involves a non-L-type calsium channel. Can J Physiol Pharmacol 73: 1502-1511, 1995 https://doi.org/10.1139/y95-208
  25. Ordog T, Redelman D, Miller LJ, Horvath VJ, Zhong Q, Almeida-Porada G, Zanjani ED, Horowitz B, Sanders KM. Purification of interstitial cells of Cajal by fluorescence-activated cell sorting. Am J Physiol 286: C448-C456, 2004 https://doi.org/10.1152/ajpcell.00273.2003
  26. Oue T, Puri P. Smooth muscle cell hypertrophy versus hyperplasia in infantile hypertrophic pyloric stenosis. Pediatric Res 45: 853-857, 1999 https://doi.org/10.1203/00006450-199906000-00012
  27. Pucovsky V, Moss Ray, Bolton TB. Non-contractile cells with thin processes resembling interstitial cells of Cajal found in the wall of guinea-pig mesenteric arteries. J Physiol 552: 119-133, 2003 https://doi.org/10.1113/jphysiol.2003.046243
  28. Sanders KM. A case for interstitial cells of Cajal as pacemakers and mediators of neurotransmission in the gastrointestinal tract. Gastroenterology 111: 492-515, 1996 https://doi.org/10.1053/gast.1996.v111.pm8690216
  29. Sergeant GP, Hollywood MA, McCloskey KD, Thornbury KD, McHale NG. Specialized pacemaking cells in the rabbit urethra. J Physiol 526: 359-366, 2000 https://doi.org/10.1111/j.1469-7793.2000.t01-2-00359.x
  30. Thomsen L, Robinson TL, Lee JCF, Farraway LA, Hughes MJG, Andrew DW, Huizinga JD. Interstitial cells of Cajal generate a rhythmic pacemaker current. Nat Med 4: 848-851, 1998 https://doi.org/10.1038/nm0798-848
  31. Torihashi S, Ward SM, Nishikawa S, Kobayashi S, Sanders KM. c-Kit-dependent development of interstitial cells and electrical activity in the murine gastrointestinal tract. Cell Tissue Res 280: 97-111, 1995
  32. Torihashi S, Ward SM, Sanders KM. Development of c-Kit-positive cells and the onset of electrical rhythmicity in murine small intestine. Gastroenterology 112: 144-155, 1997 https://doi.org/10.1016/S0016-5085(97)70229-4
  33. Wang B, Kunze WA, Zhu Y, Huizinga JD. In situ recording from gut pacemaker cells. Pflugers Arch 457: 243-251, 2008 https://doi.org/10.1007/s00424-008-0513-6
  34. Wang XY, Lammers WJEP, Bercik P, Huizinga JD. Lack of pyloric interstitial cells of Cajal explains distinct peristalsis motor patterns in stomach and small intestine. Am J Physiol 289: G539-G549, 2005
  35. Wang XY, Paterson C, Huizinga JD. Cholineregic and nitrergic innervation of ICC-DMP and ICC-IM in the human small intestine. Neurogastroenterol Motil 15: 531-543, 2003 https://doi.org/10.1046/j.1365-2982.2003.00429.x
  36. 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 480: 91-97, 1994 https://doi.org/10.1113/jphysiol.1994.sp020343
  37. Ward SM, Dixon RE, Faoite A, Sanders KM. Voltage-dependent calcium entry underlies propagation of slow waves in canine gastric antrum. J Physiol 561: 793-810, 2004 https://doi.org/10.1113/jphysiol.2004.076067
  38. Ward SM, Sanders KM. Upstroke potential of electrical slow waves in canine colonic smooth muscle due to nifedipine-resistant calcium current. J Physiol 455: 321-337, 1992 https://doi.org/10.1113/jphysiol.1992.sp019304
  39. Xu WX, Kim SJ, Kim SJ, So I, Kang TM, Rhee JC, Kim KW. Effect of stretch on calcium channel currents recorded from the antral myocytes of guinea-pig stomach. Pflugers Arch 432: 159-164, 1996 https://doi.org/10.1007/s004240050119