pubmed.ncbi.nlm.nih.gov

Plasma hormones facilitated the hypermotility of the colon in a chronic stress rat model - PubMed

Plasma hormones facilitated the hypermotility of the colon in a chronic stress rat model

Chengbai Liang et al. PLoS One. 2012.

Abstract

Objective: To study the relationship between brain-gut peptides, gastrointestinal hormones and altered motility in a rat model of repetitive water avoidance stress (WAS), which mimics the irritable bowel syndrome (IBS).

Methods: Male Wistar rats were submitted daily to 1-h of water avoidance stress (WAS) or sham WAS (SWAS) for 10 consecutive days. Plasma hormones were determined using Enzyme Immunoassay Kits. Proximal colonic smooth muscle (PCSM) contractions were studied in an organ bath system. PCSM cells were isolated by enzymatic digestion and IKv and IBKca were recorded by the patch-clamp technique.

Results: The number of fecal pellets during 1 h of acute restraint stress and the plasma hormones levels of substance P (SP), thyrotropin-releasing hormone (TRH), motilin (MTL), and cholecystokinin (CCK) in WAS rats were significantly increased compared with SWAS rats, whereas vasoactive intestinal peptide (VIP), calcitonin gene-related peptide (CGRP) and corticotropin releasing hormone (CRH) in WAS rats were not significantly changed and peptide YY (PYY) in WAS rats was significantly decreased. Likewise, the amplitudes of spontaneous contractions of PCSM in WAS rats were significantly increased comparing with SWAS rats. The plasma of WAS rats (100 µl) decreased the amplitude of spontaneous contractions of controls. The IKv and IBKCa of PCSMs were significantly decreased in WAS rats compared with SWAS rats and the plasma of WAS rats (100 µl) increased the amplitude of IKv and IBKCa in normal rats.

Conclusion: These results suggest that WAS leads to changes of plasma hormones levels and to disordered myogenic colonic motility in the short term, but that the colon rapidly establishes a new equilibrium to maintain the normal baseline functioning.

PubMed Disclaimer

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Number of fecal pellets.

Number of the fecal pellets in water avoidance stress (WAS) and sham water avoidance stress (SWAS) rats at the first five days (FFD) or the last five days (LFD) and at the base state (BASE) or acute stress state (AS) on the eleventh day. Data are expressed as mean ± SEM (n = 10). Statistical significance of difference between fecal pellet counts in WAS and SWAS rats at FFD or LFD and BASE or AS was evaluated by using unpaired Student's t-test. **P<0.01, * P<0.05 compared between WAS and SWAS.

Figure 2
Figure 2. WAS increased spontaneous contractile amplitude of proximal colonic smooth muscle (PCSM) strips.

A, C: Representative traces of the effect of WAS or SWAS on the spontaneous contractile amplitude of longitudinal smooth muscle (LM) and circular smooth muscle (CM) strips. WAS increased the mean contractile amplitude of CM and LM strips in the absence and presence of 100 nm TTX. B, D: Summarized results of the LM (B) and CM (D) spontaneous contractions in WAS and SWAS rats. Data are expressed as mean ± SEM (n = 12). Significant difference is indicated by * (P<0.05 compared to SWAS or SWAS-TTX groups, respectively, according to the unpaired Student's t-test).

Figure 3
Figure 3. WAS plasma decreased spontaneous contractile amplitude of proximal colonic smooth muscle (PCSM) strips.

A, C: Representative traces of the effect of WAS rat plasma (WP) or SWAS rat plasma (SWP) on the spontaneous contractile amplitude of longitudinal smooth muscle (LM) and circular smooth muscle (CM) strips. WP decreased the mean contractile amplitude of CM and LM strips in the presence of 100 nm TTX. B, D: Summarized results showing the effect of WP or SWP on LM (B) and CM (D) spontaneous contractions in normal rats. Data are expressed as mean ± SEM (n = 8). Significant difference is indicated by * (P<0.05 compared to normal (Nor) or Nor-SWP group according to the ANOVA analysis).

Figure 4
Figure 4. WAS reduced the whole-cell IKv of PCSMC.

A: Current tracings elicited by +20 mV depolarizing steps from a constant holding potential of −80 mV to +60 mv; the basal IKv was reduced in PCSMCs from WAS rats compared with SWAS rats. B: Current-voltage relationships comparing IKv current density between PCSMCs from WAS and SWAS rats. C: Summarized data showing the density of the currents at 60 mV in WAS and SWAS PCSMCs. **: P<0.01 vs. SWAS PCSMCs.

Figure 5
Figure 5. WAS reduced the whole-cell IBKca of PCSMC.

A: Current tracings elicited by +20 mV depolarizing steps from a constant holding potential of −60 mV to +80 mv; the basal IBKca current was reduced in PCSMCs from WAS rats compared with SWAS rats. B: Current-voltage relationships comparing IBKca density between PCSMCs from WAS and SWAS rats. C: Summarized data showing the density of the currents at 80 mV in WAS and SWAS PCSMCs. **: P<0.01 vs. SWAS PCSMCs.

Figure 6
Figure 6. Excitation of IKv in rat PCSMCs by WAS rat plasma (WP).

A: Representative record of IK in the absence and presence of WP or SWP. B: I–V relationships of IK in the absence and presence of WP or SWP. C: Summarized data showing the density of the currents at 80 mv in WAS and SWAS PCSMCs. **: P<0.01 vs. SWAS PCSMCs according to the ANOVA analysis.

Figure 7
Figure 7. Excitation of IBKca in rat PCSMCs by WAS rat plasma.

A: Representative records of IK in the absence and presence of WP or SWP (50 ul/2 ml). B: I–V relationships of IBKca in the absence and presence of WP OR SWP. C: Summarized data showing the density of the currents at 80 mV in WAS and SWAS PCSMCs. **: P<0.01 vs. SWAS PCSMCs according to the ANOVA analysis.

Similar articles

Cited by

References

    1. Lee OY. Asian motility studies in irritable bowel syndrome. J Neurogastroenterol Motil. 2010;16:120–130. - PMC - PubMed
    1. Ren TH, Wu J, Yew D, Ziea E, Lao L, et al. Effects of neonatal maternal separation on neurochemical and sensory response to colonic distension in a rat model of irritable bowel syndrome. Am J Physiol Gastrointest Liver Physiol. 2007;292:G849–856. - PubMed
    1. Ait-Belgnaoui A, Bradesi S, Fioramonti J, Theodorou V, Bueno L. Acute stress-induced hypersensitivity to colonic distension depends upon increase in paracellular permeability: role of myosin light chain kinase. Pain. 2005;113:141–147. - PubMed
    1. Kellow JE, Eckersley CM, Jones MP. Enhanced perception of physiological intestinal motility in the irritable bowel syndrome. Gastroenterology. 1991;101:1621–1627. - PubMed
    1. Bradette M, Delvaux M, Staumont G, Fioramonti J, Bueno L, et al. Evaluation of colonic sensory thresholds in IBS patients using a barostat. Definition of optimal conditions and comparison with healthy subjects. Dig Dis Sci. 1994;39:449–457. - PubMed

Publication types

MeSH terms

Substances