Nitric oxide regulates polarity of guinea pig distal colon pellet propagation and circular muscle motor response

Irena Gribovskaja-Rupp, Jung-Myun Kwak, Toku Takahashi, Kirk Ludwig

Research output: Contribution to journalArticle

Abstract

Background: Peristaltic reflex does not fully explain the polarity of peristalsis. In the distal colon, we propose that the balance of circular muscle contraction proximal and distal to the pellet is a local reflex that predicts polarity of peristalsis. Methods: Guinea pig distal colon segments were harvested, and fecal pellet transit was measured. Photographs of fecal pellet propagation were taken, colonic radius proximal and distal to the moving pellet was measured, and the ratio of radius proximal to pellet to radius distal to pellet was measured. Isometric transducers were attached 1 cm proximal and distal to a fixed intraluminal balloon, and circular muscle (CM) response to balloon distension was recorded. N G-Nitro-l-arginine methyl ester hydrochloride (L-NAME) was used to elicit an effect in experimental preparations and compared to controls. Results: Fecal pellet transit was delayed after L-NAME treatment (163 ± 23.9 vs. 41.5 ± 1.9 s in control, n = 6, p < 0.001). Photo-analysis revealed a ratio of proximal/distal colonic radius in control colon to be 0.72 ± 0.02 (n = 17) and in L-NAME treated colon 1.0 ± 0.02 (n = 10, p < 0.01). The dominant CM response pattern was a large contraction proximal to the inflated balloon and a smaller contraction distal to the balloon. In the presence of L-NAME, distal contraction was larger than the proximal contraction in 66 % of the experiments. Conclusions: Pellet propulsion in the guinea pig's distal colon depends on nitric oxide to provide appropriate balance of force between proximal and distal contraction, resulting in pellet propagation toward the anus. CM contracts both proximal and distal to the pellet, and the polarity of pellet progression depends on the balance of the two forces.

Original languageEnglish
Pages (from-to)835-842
Number of pages8
JournalJournal of Gastroenterology
Volume49
Issue number5
DOIs
Publication statusPublished - 2014 Jan 1
Externally publishedYes

Fingerprint

NG-Nitroarginine Methyl Ester
Nitric Oxide
Guinea Pigs
Colon
Muscles
Peristalsis
Reflex
Anal Canal
Contracts
Muscle Contraction
Transducers
Therapeutics

Keywords

  • Balloon distension
  • Peristaltic reflex
  • Polarity

ASJC Scopus subject areas

  • Gastroenterology

Cite this

Nitric oxide regulates polarity of guinea pig distal colon pellet propagation and circular muscle motor response. / Gribovskaja-Rupp, Irena; Kwak, Jung-Myun; Takahashi, Toku; Ludwig, Kirk.

In: Journal of Gastroenterology, Vol. 49, No. 5, 01.01.2014, p. 835-842.

Research output: Contribution to journalArticle

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abstract = "Background: Peristaltic reflex does not fully explain the polarity of peristalsis. In the distal colon, we propose that the balance of circular muscle contraction proximal and distal to the pellet is a local reflex that predicts polarity of peristalsis. Methods: Guinea pig distal colon segments were harvested, and fecal pellet transit was measured. Photographs of fecal pellet propagation were taken, colonic radius proximal and distal to the moving pellet was measured, and the ratio of radius proximal to pellet to radius distal to pellet was measured. Isometric transducers were attached 1 cm proximal and distal to a fixed intraluminal balloon, and circular muscle (CM) response to balloon distension was recorded. N G-Nitro-l-arginine methyl ester hydrochloride (L-NAME) was used to elicit an effect in experimental preparations and compared to controls. Results: Fecal pellet transit was delayed after L-NAME treatment (163 ± 23.9 vs. 41.5 ± 1.9 s in control, n = 6, p < 0.001). Photo-analysis revealed a ratio of proximal/distal colonic radius in control colon to be 0.72 ± 0.02 (n = 17) and in L-NAME treated colon 1.0 ± 0.02 (n = 10, p < 0.01). The dominant CM response pattern was a large contraction proximal to the inflated balloon and a smaller contraction distal to the balloon. In the presence of L-NAME, distal contraction was larger than the proximal contraction in 66 {\%} of the experiments. Conclusions: Pellet propulsion in the guinea pig's distal colon depends on nitric oxide to provide appropriate balance of force between proximal and distal contraction, resulting in pellet propagation toward the anus. CM contracts both proximal and distal to the pellet, and the polarity of pellet progression depends on the balance of the two forces.",
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N2 - Background: Peristaltic reflex does not fully explain the polarity of peristalsis. In the distal colon, we propose that the balance of circular muscle contraction proximal and distal to the pellet is a local reflex that predicts polarity of peristalsis. Methods: Guinea pig distal colon segments were harvested, and fecal pellet transit was measured. Photographs of fecal pellet propagation were taken, colonic radius proximal and distal to the moving pellet was measured, and the ratio of radius proximal to pellet to radius distal to pellet was measured. Isometric transducers were attached 1 cm proximal and distal to a fixed intraluminal balloon, and circular muscle (CM) response to balloon distension was recorded. N G-Nitro-l-arginine methyl ester hydrochloride (L-NAME) was used to elicit an effect in experimental preparations and compared to controls. Results: Fecal pellet transit was delayed after L-NAME treatment (163 ± 23.9 vs. 41.5 ± 1.9 s in control, n = 6, p < 0.001). Photo-analysis revealed a ratio of proximal/distal colonic radius in control colon to be 0.72 ± 0.02 (n = 17) and in L-NAME treated colon 1.0 ± 0.02 (n = 10, p < 0.01). The dominant CM response pattern was a large contraction proximal to the inflated balloon and a smaller contraction distal to the balloon. In the presence of L-NAME, distal contraction was larger than the proximal contraction in 66 % of the experiments. Conclusions: Pellet propulsion in the guinea pig's distal colon depends on nitric oxide to provide appropriate balance of force between proximal and distal contraction, resulting in pellet propagation toward the anus. CM contracts both proximal and distal to the pellet, and the polarity of pellet progression depends on the balance of the two forces.

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