Slow-wave activity in colon: role of network of submucosal interstitial cells of Cajal

1991 ◽  
Vol 260 (4) ◽  
pp. G636-G645 ◽  
Author(s):  
R. Serio ◽  
C. Barajas-Lopez ◽  
E. E. Daniel ◽  
I. Berezin ◽  
J. D. Huizinga
Keyword(s):  
Smooth Muscle ◽  
Slow Wave ◽  
Interstitial Cells Of Cajal ◽  
Circular Muscle ◽  
Interstitial Cells ◽  
Wave Activity ◽  
Slow Waves ◽  
Slow Wave Activity ◽  
Plateau Potentials ◽  
Cells Of Cajal

The present study compares the electrophysiological properties of two preparations dissected from the canine colon circular muscle layer: first, containing the submucosal network of interstitial cells of Cajal (ICC) with two to four associated smooth muscle cell layers, and second, a circular muscle preparation devoid of the submucosal ICC network. In the ICC-rich preparations, consistent slow-wave activity was observed with prolonged plateau potentials of approximately 10-s duration. The plateau potentials were sensitive to D 600. In approximately 45% of circular muscle preparations devoid of the submucosal ICC network (confirmed using electron microscopy) slow waves, of different waveshape, were recorded at frequencies identical to those in whole circular muscle preparations. These slow waves did not show a plateau potential. Compared with ICC-rich preparations with a resting membrane potential of about -80 mV, circular muscle preparations had lower membrane potentials, about -70 mV when active, and about -60 mV when quiescent. Heptanol (1 mM) electrically uncoupled cells, since it abolished electrotonic current spread and allowed measurement of the input resistance by intracellular current injection. Heptanol also affected ionic conductances. Heptanol abolished slow waves; the underlying mechanism needs further investigation. In the presence of heptanol, cells in the isolated ICC network and in circular smooth muscle preparations showed spontaneous hyperpolarizing potential fluctuations at a frequency of four to six per second. These oscillations were abolished by current-induced hyperpolarization and TEA (30 mM) and are therefore likely due to spontaneously active K+ conductance.

Selective lesioning of interstitial cells of Cajal by methylene blue and light leads to loss of slow waves

1994 ◽  
Vol 266 (3) ◽  
pp. G485-G496 ◽  
Author(s):  
L. W. Liu ◽  
L. Thuneberg ◽  
J. D. Huizinga
Keyword(s):  
Methylene Blue ◽  
Smooth Muscle ◽  
Smooth Muscle Cells ◽  
Electrical Activity ◽  
Slow Wave ◽  
Interstitial Cells Of Cajal ◽  
Wave Activity ◽  
Slow Waves ◽  
Slow Wave Activity ◽  
Cells Of Cajal

Incubation with 50 microM methylene blue (MB) and subsequent intense illumination resulted in abolition of the slow-wave activity in the submuscular interstitial cells of Cajal-circular muscle (ICC-CM) preparations of canine colon. This was often accompanied by a decrease in resting membrane potential. Repolarization of cells back to -70 mV did not restore the slow-wave activity, indicating that MB plus light directly interrupted the generation mechanism of slow waves. After MB incubation, a 2-min illumination consistently changed the mitochondrial conformation in ICCs from very condensed to orthodox, without inducing any obvious changes in smooth muscle cells. After 4- to 10-min illumination, ICCs became progressively more damaged with swollen and ruptured mitochondria, loss of cytoplasmic contrast and detail, loss of caveolae, and rupture of the plasma membrane. No damage was seen in smooth muscle cells or nerves. Gap junctional ultrastructure was preserved. Intense illumination without preincubation with MB left the slow waves and the ultrastructure of ICC-CM preparations unaffected. In CM preparations, without the submuscular ICC-smooth-muscle network, MB plus light induced no changes in electrical activity. We conclude that the correlation between selective damage to the submuscular ICCs (relative to smooth muscle) and selective loss of the slow-wave activity (relative to other electrical activity of the CM) strongly indicates that the ICCs play an essential role in the generation of slow waves.

Pacemaker activity recorded in interstitial cells of Cajal of the gastrointestinal tract

1989 ◽  
Vol 257 (4) ◽  
pp. C830-C835 ◽  
Author(s):  
C. Barajas-Lopez ◽  
I. Berezin ◽  
E. E. Daniel ◽  
J. D. Huizinga
Keyword(s):  
Methylene Blue ◽  
Slow Wave ◽  
Interstitial Cells Of Cajal ◽  
Circular Muscle ◽  
Interstitial Cells ◽  
Wave Activity ◽  
Slow Wave Activity ◽  
Resting Membrane Potential ◽  
Pacemaker Activity ◽  
Cells Of Cajal

The hypothesis was tested that interstitial cells of Cajal can generate slow wave activity. Intracellular recordings were performed only in the most superficial cells at the submucosal surface of the canine colonic circular muscle layer. An omnipresent and characteristic slow wave activity was present in all cells with a mean amplitude of 37 +/- 3 mV, a frequency of 4.6 +/- 0.1 counts/min (cpm), and a duration of 5.6 +/- 0.5 s; the average resting membrane potential was -70 +/- 1 mV. To determine the type of cell from which these recordings were obtained, methylene blue was injected by microiontophoresis. The strips were immediately fixed while the microelectrode was kept in the cell. A small segment of the tissue containing this cell was then processed for electron microscopy and serially sectioned. Electron-microscopic evidence showed that the microelectrode tip was positioned in an interstitial cell of Cajal (ICC): 1) several sections were observed with round cytoplasmic lesions of decreasing diameter followed by sections from the same cell without the lesion and 2) electron-dense material was observed in these sections due to the injected methylene blue. These cells were identified as part of the ICC network present at the muscle-submucosa interface of the circular muscle and were positively identified as ICC by the presence of cell processes. This is the first report giving direct evidence for the occurrence of electrical slow waves in ICC. It is essential support for the hypothesis that ICC are the actual pacemaker cells of the gut musculature.

Quantitative cellular description of gastric slow wave activity

2008 ◽  
Vol 294 (4) ◽  
pp. G989-G995 ◽  
Author(s):  
Alberto Corrias ◽  
Martin L. Buist
Keyword(s):  
Slow Wave ◽  
Interstitial Cells Of Cajal ◽  
Quantitative Description ◽  
Wave Activity ◽  
Slow Waves ◽  
Slow Wave Activity ◽  
Good Correspondence ◽  
Gastric Slow Wave ◽  
Intracellular Ca ◽  
Cells Of Cajal

Interstitial cells of Cajal (ICC) are responsible for the spontaneous and omnipresent electrical activity in the stomach. A quantitative description of the intracellular processes whose coordinated activity is believed to generate electrical slow waves has been developed and is presented here. In line with recent experimental evidence, the model describes how the interplay between the mitochondria and the endoplasmic reticulum in cycling intracellular Ca2+ provides the primary regulatory signal for the initiation of the slow wave. The major ion channels that have been identified as influencing slow wave activity have been modeled according to data obtained from isolated ICC. The model has been validated by comparing the simulated profile of the slow waves with experimental recordings and shows good correspondence in terms of frequency, amplitude, and shape in both control and pharmacologically altered conditions.

Are interstitial cells of Cajal plurifunction cells in the gut?

2008 ◽  
Vol 294 (2) ◽  
pp. G372-G390 ◽  
Author(s):  
Sushil K. Sarna
Keyword(s):  
Smooth Muscle ◽  
Smooth Muscle Cells ◽  
Interstitial Cells Of Cajal ◽  
Circular Muscle ◽  
Muscle Cells ◽  
Interstitial Cells ◽  
Slow Waves ◽  
Enteric Neurons ◽  
Motility Disorders ◽  
Cells Of Cajal

The proposed functions of the interstitial cells of Cajal (ICC) are to 1) pace the slow waves and regulate their propagation, 2) mediate enteric neuronal signals to smooth muscle cells, and 3) act as mechanosensors. In addition, impairments of ICC have been implicated in diverse motility disorders. This review critically examines the available evidence for these roles and offers alternate explanations. This review suggests the following: 1) The ICC may not pace the slow waves or help in their propagation. Instead, they may help in maintaining the gradient of resting membrane potential (RMP) through the thickness of the circular muscle layer, which stabilizes the slow waves and enhances their propagation. The impairment of ICC destabilizes the slow waves, resulting in attenuation of their amplitude and impaired propagation. 2) The one-way communication between the enteric neuronal varicosities and the smooth muscle cells occurs by volume transmission, rather than by wired transmission via the ICC. 3) There are fundamental limitations for the ICC to act as mechanosensors. 4) The ICC impair in numerous motility disorders. However, a cause-and-effect relationship between ICC impairment and motility dysfunction is not established. The ICC impair readily and transform to other cell types in response to alterations in their microenvironment, which have limited effects on motility function. Concurrent investigations of the alterations in slow-wave characteristics, excitation-contraction and excitation-inhibition couplings in smooth muscle cells, neurotransmitter synthesis and release in enteric neurons, and the impairment of the ICC are required to understand the etiologies of clinical motility disorders.

scholarly journals Expression of anoctamin 1/TMEM16A by interstitial cells of Cajal is fundamental for slow wave activity in gastrointestinal muscles

2009 ◽  
Vol 587 (20) ◽  
pp. 4887-4904 ◽  
Author(s):  
Sung Jin Hwang ◽  
Peter J. A. Blair ◽  
Fiona C. Britton ◽  
Kate E. O’Driscoll ◽  
Grant Hennig ◽  
...  
Keyword(s):  
Slow Wave ◽  
Interstitial Cells Of Cajal ◽  
Interstitial Cells ◽  
Wave Activity ◽  
Slow Wave Activity ◽  
Anoctamin 1 ◽  
Cells Of Cajal

Role of gap junctions in structural arrangements of interstitial cells of Cajal and canine ileal smooth muscle

1998 ◽  
Vol 274 (6) ◽  
pp. G1125-G1141 ◽  
Author(s):  
Edwin E. Daniel ◽  
Yu-Fang Wang ◽  
Francisco S. Cayabyab
Keyword(s):  
Smooth Muscle ◽  
Smooth Muscle Cells ◽  
Gap Junctions ◽  
Interstitial Cells Of Cajal ◽  
Circular Muscle ◽  
Muscle Cells ◽  
Interstitial Cells ◽  
Slow Waves ◽  
Circular Smooth Muscle ◽  
Cells Of Cajal

We examined the structural and functional basis for pacemaking by interstitial cells of Cajal (ICC) in circular smooth muscle of the canine ileum. Gap junctions were found between ICC of myenteric plexus (MyP), occasionally between MyP ICC and outer circular smooth muscle cells, between individual outer circular smooth muscle cells, between them and ICC of the deep muscular plexus (DMP), and between DMP ICC. No visible gap junctions connected MyP ICC to longitudinal muscle cells or inner circular muscle cells. Occasionally contacts occurred between the two muscle layers. No special structures were found to connect MyP and DMP ICC networks. Octanol concentration dependently reduced the amplitude and frequency of, but did not abolish, slow waves in circular muscle in isolated ileum recorded near the MyP or the DMP. Slow waves triggered from MyP ICC by a current pulse also persisted. Contractile activity was abolished, cells were depolarized, and fast inhibitory junction potentials were reduced by octanol. We conclude that ICC pacemakers of the MyP and DMP utilize gap junctional conductances for pacemaking function but may not require them. Coupling between the two ICC networks may utilize the circular muscle syncytium.

Excitability of canine colon circular muscle disconnected from the network of interstitial cells of Cajal

1992 ◽  
Vol 70 (2) ◽  
pp. 289-295 ◽  
Author(s):  
Louis W. C. Liu ◽  
Edwin E. Daniel ◽  
Jan D. Huizinga
Keyword(s):  
Slow Wave ◽  
Interstitial Cells Of Cajal ◽  
Potassium Conductance ◽  
Circular Muscle ◽  
Interstitial Cells ◽  
Slow Waves ◽  
Oscillatory Activity ◽  
Krebs Solution ◽  
Ionic Mechanisms ◽  
Cells Of Cajal

The 6 cpm omnipresent slow waves recorded in the circular muscle (CM) layer of canine colon are generated at the submucosal surface of the CM layer. After removal of the submucosal network of interstitial cells of Cajal (ICC), 66% of the CM preparations (25 of 38) were quiescent in Krebs solution. In the presence of carbachol, seven of nine of these spontaneously quiescent CM preparations demonstrated slow wave-like activity with mean frequency, duration and amplitude of 5.9 ± 0.4 cpm, 2.8 ± 0.5 s, and 0.8 ± 0.2 mV, respectively. Similar slow wave-like activities were induced by TEA (seven out of eight quiescent CM preparations) with frequency, duration and amplitude of 6.1 ± 0.2 cpm, 2.7 ± 0.5 s, and 1.0 ± 0.2 mV, respectively, and by BaCl2 (eight of eight quiescent CM preparations) with frequency, duration, and amplitude of 6.3 ± 0.3 cpm, 1.8 ± 0.2 s, and 0.5 ± 0.1 mV, respectively. All the induced activities were abolished in the presence of 1 μM D600. CM preparations with the submucosal ICC network intact (ICC–CM) showed slow wave activity in Krebs solution at a frequency of 6.2 ± 0.2 cpm, a duration of 3.6 ± 0.2 s, and an amplitude of 1.0 ± 0.1 mV (n = 22). When ICC–CM preparations were stimulated by BaCl2, carbachol, or TEA, the slow wave frequency did not change significantly, but the duration increased as well as the amplitude. In the presence of D600, the upstroke of slow waves remained and the frequency was not affected. The ability to generate slow wave-like activity after potassium conductance blockade in spontaneously quiescent CM disconnected from the ICC network suggested that circular muscle cells have ionic mechanisms for intrinsic oscillatory activity and are capable of actively participating in the conduction and generation of slow waves.Key words: colon, smooth muscle, interstitial cells of Cajal, canine, slow waves, excitability.

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