Skip to main content
SpringerLink
Log in

In vivo recording of colonic motility in conscious rats with deficiency of interstitial cells of Cajal, with special reference to the effects of nitric oxide on colonic motility

  • Published:
Journal of Gastroenterology Aims and scope Submit manuscript

Abstract

Background

We recorded in vivo colonic motility in rats with a deficiency of interstitial cells of Cajal (ICC) (Ws/Ws rats) and in wild-type rats (+/+ rats), with special reference to the effects of nitric oxide (NO) on colonic motility in both types of rats, in order to ascertain the role of ICC in colonic motility, and the relationship between NO and ICC in regard to colonic motility.

Methods

Miniature strain-gauge force transducers were sutured on the surface of the ascending and sigmoid colon of Ws/Ws rats and +/+ rats as controls. After 1 week and a fasting period of 24 h, colonic motility in +/+ and Ws/Ws rats was recorded. We also studied the effect of NO on colonic motility in both types of rats, by means of the administration of N-nitro-l-arginine methyl ester (l-NAME) or l-arginine.

Results

In +/+ rats, there were contractions with high amplitude and long duration in both the ascending and sigmoid colon. The number, amplitude, and duration of contractions in the ascending colon were 9.9/20 min, 6.1 g, and 22.7 s, respectively. These findings in the sigmoid colon were 5.2/20 min, 5.2 g, and 23.0 s, respectively. The number of contractions in the ascending and sigmoid colon in Ws/Ws rats (2.3 and 1.0/20 min) was significantly lower than that in +/+ rats (P < 0.05). The number of contractions in the ascending and sigmoid colon in +/+ rats (9.7 and 5.1/20 min before treatment) was significantly increased by l-NAME administration (28.7 and 13.9/40–60 min after treatment; P < 0.05), but that in Ws/Ws rats was not influenced. The number of contractions in the ascending and sigmoid colon in +/+ rats (10.2 and 5.2/20 min before treatment) was significantly decreased by l-arginine administration (3.6 and 2.1/40–60 min after treatment; P < 0.05), but that in Ws/Ws rats was not influenced.

Conclusions

ICC must be related to the occurrence of a normal number of colonic contractions. NO may be involved in the inhibitory regulation of colonic motility, and the effect of NO on the occurrence of contractions appears to be mediated by ICC.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. SM Ward KM Sanders (1990) ArticleTitlePacemaker activity in septal structures of canine colonic circular muscle Am J Physiol 259 G264–73 Occurrence Handle2382725 Occurrence Handle1:STN:280:DyaK3czkt1yksA%3D%3D

    PubMed  CAS  Google Scholar 

  2. H Maeda A Yamagata S Nishikawa K Yoshinaga S Kobayashi K Nishi et al. (1992) ArticleTitleRequirement of c-kit for development of intestinal pacemaker system Development 116 369–75 Occurrence Handle1283735 Occurrence Handle1:CAS:528:DyaK3sXls12msw%3D%3D

    PubMed  CAS  Google Scholar 

  3. S Torihashi SM Ward S Nishikawa K Nishi S Kobayashi KM Sanders (1995) ArticleTitleC-kit-dependent development of interstitial cells and electrical activity in the murine gastrointestinal tract Cell Tissue Res 280 97–111 Occurrence Handle7538451 Occurrence Handle1:CAS:528:DyaK2MXlt1eisrg%3D

    PubMed  CAS  Google Scholar 

  4. SM Ward AJ Burns S Torihashi KM Sanders (1994) ArticleTitleMutation of the protooncogene c-kit blocks development of intestinal cells and electrical rhythmicity in murine intestine J Physiol (Lond) 480 91–7 Occurrence Handle1:CAS:528:DyaK2cXmslOqt78%3D

    CAS  Google Scholar 

  5. JD Huizinga L Thuneberg M Kluppel J Malysz HB Mikkelsen A Bernstein (1995) ArticleTitleW/kit gene required for interstitial cells of Cajal and for intestinal pacemaker activity Nature 373 347–9 Occurrence Handle7530333 Occurrence Handle1:CAS:528:DyaK2MXjtlygur0%3D

    PubMed  CAS  Google Scholar 

  6. SM Ward AJ Burns S Torihashi SC Harney K Sandes (1995) ArticleTitleImpaired development of interstitial cells and intestinal electrical rhythmicity in steel mutants Am J Physiol Cell Physiol 269 C1577–85 Occurrence Handle1:CAS:528:DyaK28XjslOjsQ%3D%3D

    CAS  Google Scholar 

  7. KM Sanders T Ordog SD Koh S Torihashi SM Ward (1999) ArticleTitleDevelopment and plasticity of interstitial cells of Cajal Neurogastroenterol Mot 11 311–38 Occurrence Handle1:STN:280:DyaK1MvltFCjtQ%3D%3D Occurrence Handle10.1046/j.1365-2982.1999.00164.x

    Article  CAS  Google Scholar 

  8. SD Koh TW Kim JY Jun NJ Glasgow SM Ward KM Sanders (2000) ArticleTitleRegulation of pacemaker currents in interstitial cells of Cajal from murine small intestine by cyclic nucleotides J Physiol 527.1 149–62

    Google Scholar 

  9. K Isozaki S Hirota A Nakama J Miyagawa Y Shinomura Z Xu et al. (1995) ArticleTitleDisturbed intestinal movement, bile reflux to the stomach, and deficiency of c-kit-expressing cells in Ws/Ws mutant rats Gastroenterology 109 456–64 Occurrence Handle7542218 Occurrence Handle1:CAS:528:DyaK2MXntlCgtLo%3D Occurrence Handle10.1016/0016-5085(95)90333-X

    Article  PubMed  CAS  Google Scholar 

  10. A Nakama S Hirota T Okazaki K Nagano S Kawano M Hori et al. (1998) ArticleTitleDisturbed pyloric motility in Ws/Ws mutant rats due to deficiency of c-kit-expressing interstitial cells of Cajal Pathol Int 48 843–9 Occurrence Handle9832052 Occurrence Handle1:CAS:528:DyaK1cXns1Kis78%3D

    PubMed  CAS  Google Scholar 

  11. I Takayama E Seto H Zai S Ohno H Tezuka Y Daigo et al. (2000) ArticleTitleChanges of in vivo gastrointestinal motor pattern in pacemaker-deficient (WsRC-Ws/Ws) rats Dig Dis Sci 45 1901–6 Occurrence Handle11117558 Occurrence Handle1:STN:280:DC%2BD3M%2FntVWrsA%3D%3D Occurrence Handle10.1023/A:1005612109863

    Article  PubMed  CAS  Google Scholar 

  12. T Tomomasa A Takahashi M Tabata H Kaneko T Watanabe T Kobayashi et al. (2000) ArticleTitleIn vivo recording of gastrointestinal motility in Ws/Ws mutant rats (abstract) Gastroenterology 118 A635 Occurrence Handle10.1016/S0016-5085(00)80638-1

    Article  Google Scholar 

  13. T Tomomasa A Takahashi H Kaneko T Watanabe M Tabata M Kato et al. (1999) ArticleTitleY-27632 inhibits gastric motility in conscious rats Life Sci 66 PL29–34 Occurrence Handle10.1016/S0024-3205(99)00577-9

    Article  Google Scholar 

  14. H Kaneko T Tomomasa T Watanabe A Takahashi M Tabata S Hussein et al. (2001) ArticleTitleEffect of vincristine on gastric motility in conscious rats Dig Dis Sci 46 952–9 Occurrence Handle11341664 Occurrence Handle1:CAS:528:DC%2BD3MXjvVCgs7Y%3D Occurrence Handle10.1023/A:1010785206315

    Article  PubMed  CAS  Google Scholar 

  15. A Takahashi T Tomomasa H Kaneko T Watanabe M Tabata H Morikawa et al. (2001) ArticleTitleIntestinal motility in an in vivo rat model of intestinal ischemia-reperfusion with special reference to the effects of nitric oxide on the motility changes J Pediatr Gastroenterol Nutr 33 283–8 Occurrence Handle11593123 Occurrence Handle1:CAS:528:DC%2BD3MXnvFOksLY%3D

    PubMed  CAS  Google Scholar 

  16. Z Itoh T Sekiguchi (1983) ArticleTitleInterdigestive motor activity in health and disease Scand J Gastroenterol 18 121–34

    Google Scholar 

  17. Z Itoh M Nakaya T Suzuki H Arai K Wakabayashi (1984) ArticleTitleErythromycin mimics exogenous motilin in gastrointestinal contractile activity in the dog Am J Physiol Gastrointest Liver Physiol 247 G688–94 Occurrence Handle1:CAS:528:DyaL2MXnt1Cluw%3D%3D

    CAS  Google Scholar 

  18. KM Sanders (1996) ArticleTitleA case for interstitial cells of Cajal as pacemakers and mediators of neurotransmission in the gastrointestinal tract Gastroenterology 111 492–515 Occurrence Handle8690216 Occurrence Handle1:STN:280:DyaK28zgsFWiuw%3D%3D Occurrence Handle10.1053/gast.1996.v111.pm8690216

    Article  PubMed  CAS  Google Scholar 

  19. S Yoneda M Kadowaki S Sugimori F Sekiguchi S Sunada H Fukui et al. (2001) ArticleTitleRhythmic spontaneous contractions in the rat proximal colon Jpn J Physiol 51 717–23 Occurrence Handle11846963 Occurrence Handle1:STN:280:DC%2BD387kvVWitA%3D%3D

    PubMed  CAS  Google Scholar 

  20. SM Ward HH Dalziel KD Thornbury DP Westfall KM Sanders (1992) ArticleTitleNonadrenergic, noncholinergic inhibition and rebound excitation in canine colon depend on nitric oxide Am J Physiol Gastrointest Liver Physiol 262 G237–43 Occurrence Handle1:CAS:528:DyaK38Xhs1Kqsr4%3D

    CAS  Google Scholar 

  21. K Venkova J Krier (1994) ArticleTitleA nitric oxide and prostaglandin-dependent component of NANC off-contractions in cat colon Am J Physiol Gastrointest Liver Physiol 266 G40–7 Occurrence Handle1:CAS:528:DyaK2cXhsFCltLk%3D

    CAS  Google Scholar 

  22. RA Lefebvre (1995) ArticleTitleNitric oxide in the peripheral nervous system Ann Med 27 379–88 Occurrence Handle7546628 Occurrence Handle1:CAS:528:DyaK2MXpt12nsb8%3D Occurrence Handle10.3109/07853899509002591

    Article  PubMed  CAS  Google Scholar 

  23. MG Vannucchi L Corsani D Bani MS Faussone-Pellegrini (2002) ArticleTitleMyenteric neurons and interstitial cells of Cajal of mouse colon express several nitric oxide synthase isoforms Neurosci Lett 326 191–5 Occurrence Handle12095654 Occurrence Handle1:CAS:528:DC%2BD38XkvFykuro%3D Occurrence Handle10.1016/S0304-3940(02)00338-5

    Article  PubMed  CAS  Google Scholar 

  24. X-Y Wang KM Sanders SM Ward (2000) ArticleTitleRelationship between interstitial cells of Cajal and enteric motor neurons in the murine proximal colon Cell Tissue Res 302 331–42 Occurrence Handle11151445 Occurrence Handle1:CAS:528:DC%2BD3cXoslKltr4%3D Occurrence Handle10.1007/s004410000272

    Article  PubMed  CAS  Google Scholar 

  25. NG Publicover EM Hammond KM Sanders (1993) ArticleTitleAmplification of nitric oxide signaling by interstitial cells isolated from canine colon Proc Natl Acad Sci USA 90 2087–91 Occurrence Handle8446634 Occurrence Handle1:CAS:528:DyaK3sXhs1Wls78%3D

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of General Surgical Science (Surgery I), Gunma University, Graduate School of Medicine, 3-39-15 Showa-machi, Maebashi, 371-8511, Japan

    Atsushi Takahashi, Makoto Suzuki, Erito Mochiki & Hiroyuki Kuwano

  2. Department of Pediatrics and Developmental Medicine, Gunma University, Graduate School of Medicine, Gunma, Japan

    Takeshi Tomomasa, Hiroaki Kaneko, Reiko Hatori, Takashi Ishige & Akihiro Morikawa

Authors
  1. Atsushi Takahashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Takeshi Tomomasa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hiroaki Kaneko
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Reiko Hatori
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Takashi Ishige
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Makoto Suzuki
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Erito Mochiki
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Akihiro Morikawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Hiroyuki Kuwano
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Takahashi, A., Tomomasa, T., Kaneko, H. et al. In vivo recording of colonic motility in conscious rats with deficiency of interstitial cells of Cajal, with special reference to the effects of nitric oxide on colonic motility. J Gastroenterol 40, 1043–1048 (2005). https://doi.org/10.1007/s00535-005-1688-7

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00535-005-1688-7

Key words

Search

Navigation