The role of substance P in the maintenance of colonic hypermotility induced by repeated stress in rats
Abstract
Background The mechanism underlying chronic stress-induced gastrointestinal (GI) dysmotility has not been fully elucidated and GI hormones have been indicated playing a role in mediating stress-induced changes in GI motor function.Aims Our objective was to study the possible role of substance P (SP) in the colonic hypermotility induced by repeated water avoidance stress (WAS) which mimics irritable bowel syndrome.Methods Male Wistar rats were submitted to WAS or sham WAS (SWAS) (1h/day) for up to 10 consecutive days. Enzyme Immunoassay Kit was used to detect the serum level of SP. The expression of neurokinin-1 receptor (NK1R) was investigated by Immunohistochemistry and Western blotting. The spontaneous contraction of muscle strip was studied in an organ bath system. L-type calcium channel currents (ICa,L) of smooth muscle cells (SMCs) were recorded by whole-cell patch-clamp technique.Results Fecal pellet expulsion and spontaneous contraction of proximal colon in rats were increased after repeated WAS. The serum level of SP was elevated following WAS. Immunohistochemistry proved the expression of NK1R in mucosa, muscularis and myenteric plexus. Western blotting demonstrated stress-induced up-regulation of NK1R in colon devoid of mucosa and submucosa. Repeated WAS increased the contractile activities of longitudinal muscle and circular muscle strips induced by SP and this effect was reversed by a selective NK1R antagonist. The ICa,L of SMCs in the WAS rats were drastically increased compared to controls after addition of SP.Conclusions Increased serum SP level and up-regulated NK1R in colon may contribute to stress-induced colonic hypermotility. And L-type calcium channels play a potentially important role in the process of WAS-induced dysmotility.
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Increased local production of estrogen and proinflammatory cytokines may induce NK1R in myometrium, causing uterine hyperactivity and subsequently pain.
“This may suggest that increased local production of estrogen and proinflammatory cytokines may induce NK1R in myometrium, causing uterine hyperactivity and, subsequently, pain, as in colon72,73.”
From Neuropeptides Substance P and Calcitonin Gene Related Peptide Accelerate the Development and Fibrogenesis of Endometriosis (2019) · cites this paper as [73]
NK1R antagonism reduces anxiety and emotional arousal circuit response to noxious visceral distension in women with irritable bowel syndrome.
“Moreover, NK1R antagonism has been shown to reduce anxiety and emotional arousal circuit response to noxious visceral distension in women with irritable bowel syndrome107, which is likely attributable, at least in part, to increased colonic hypermotility induced by SP and NK1R activation72,73.”
From Neuropeptides Substance P and Calcitonin Gene Related Peptide Accelerate the Development and Fibrogenesis of Endometriosis (2019) · cites this paper as [73]
Water avoidance stress (WAS)-induced colonic hypermotility is probably dependent on the upregulation of the neurokinin-1 receptor (NK1R) in the colon and increased serum SP levels, suggesting a potential mechanism for diarrhea in IBD patients with anxiety or depression.
“Another study revealed that water avoidance stress (WAS)-induced colonic hypermotility is probably dependent on the upregulation of the neurokinin-1 receptor (NK1R) in the colon and increased serum SP levels, suggesting a potential mechanism for diarrhea in IBD patients with anxiety or depression (41).”
From Stress triggers flare of inflammatory bowel disease in children and adults (2019) · cites this paper as [41]
Cites
Neurotransmitter functions of mammalian tachykinins.
Otsuka, M., & Yoshioka, K. (1993) · Physiological Reviews · doi:10.1152/physrev.1993.73.2.229 · Cited by 1,091 · see citing works
Severini, C., Improta, G., Falconieri-Erspamer, G., Salvadori, S., & Erspamer, V. (2002) · Pharmacological Reviews · doi:10.1124/pr.54.2.285 · Cited by 638 · see citing works
Tachykinins and tachykinin receptors: a growing family
Pennefather, J. N., Lecci, A., Candenas, L., Patak, E., Pinto, F. M., & Maggi, C. A. (2003) · Life Sciences · doi:10.1016/j.lfs.2003.09.039 · Cited by 473 · see citing works
Coutinho, S. V., Plotsky, P. M., Sablad, M., Miller, J. C., Zhou, H., Bayati, A. I., McRoberts, J. A., & Mayer, E. A. (2002) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00240.2001 · Cited by 456 · see citing works
V. Stress and irritable bowel syndrome
Mayer, E. A., Naliboff, B. D., Chang, L., & Coutinho, S. V. (2001) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.2001.280.4.g519 · Cited by 413 · cited 1× · see citing works
“Different types of psychological and environmental stressors are known to play an important role in the development (Coutinho et al., 2002), maintenance, and exacerbation of irritable bowel syndrome (IBS) symptoms (Mayer et al., 2001).”
Söderholm, J. D., Yang, P., Ceponis, P., Vohra, A., Riddell, R., Sherman, P. M., & Perdue, M. H. (2002) · Gastroenterology · doi:10.1053/gast.2002.36019 · Cited by 362 · see citing works
Tachykinins in the gut. Part I. Expression, release and motor function
Holzer, P. D., & Holzer‐Petsche, U. (1997) · Pharmacology & Therapeutics · doi:10.1016/s0163-7258(96)00195-7 · Cited by 312 · see citing works
Repeated exposure to water avoidance stress in rats: a new model for sustained visceral hyperalgesia
Bradesi, S., Schwetz, I., Ennes, H. S., Lamy, C. M., Ohning, G., Fanselow, M. S., Pothoulakis, C., McRoberts, J. A., & Mayer, E. A. (2005) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00500.2004 · Cited by 307 · see citing works
Grady, E. F., Bałuk, P., Böhm, S. K., Gamp, P. D., Wong, H. C., Payan, D. G., Ansel, J. C., Portbury, A. L., Furness, J. B., McDonald, D. M., et al. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-21-06975.1996 · Cited by 201 · see citing works
The Effect of Stress on Colon Motor and Electrical Activity in Irritable Bowel Syndrome
Welgan, P. R., Meshkinpour, H., & Hoehler, F. K. (1985) · Psychosomatic Medicine · doi:10.1097/00006842-198503000-00005 · Cited by 147 · see citing works
Tachykinins and their functions in the gastrointestinal tract
Shimizu, Y., Matsuyama, H., Shiina, T., Takewaki, T., & Furness, J. B. (2007) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-007-7148-1 · Cited by 133 · see citing works
Immunomodulatory Properties of Substance P
Koon, H. W., & Pothoulakis, C. (2006) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1366.024 · Cited by 126 · see citing works
Ren, T., Wu, J. C., Yew, D. T.-W., Ziea, E. T.-C., Lao, L., Leung, W. K., Berman, B., Hu, P., & Sung, J. J. �. (2006) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00400.2006 · Cited by 125 · see citing works
The Enteric Nervous System II: Gastrointestinal Functions
Hansen, M. B. (2003) · Pharmacology & Toxicology · doi:10.1034/j.1600-0773.2003.920601.x · Cited by 117 · see citing works
Cold-restraint stress increases rat fecal pellet output and colonic transit
Barone, F. C., Deegan, J. F., Price, W. J., Fowler, P. J., Fondacaro, J. D., & Ormsbee, H. S. (1990) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.1990.258.3.g329 · Cited by 106 · see citing works
Gazzieri, D., Trevisani, M., Springer, J., Harrison, S., Cottrell, G. S., Andrè, E., Nicoletti, P., Massi, D., Zecchi, S., Nosi, D., et al. (2007) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2007.05.018 · Cited by 99 · see citing works
Tachykinins and tachykinin receptors in the gut, with special reference to NK2 receptors in human
Lecci, A., Capriati, A., Altamura, M., & Maggi, C. A. (2006) · Autonomic Neuroscience · doi:10.1016/j.autneu.2006.02.014 · Cited by 91 · see citing works
Bischoff, S. C., Schwengberg, S., Lorentz, A., Manns, M. P., Bektaş, H., Sann, H., Levi‐Schaffer, F., Shanahan, F., & Schemann, M. (2004) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2004.00502.x · Cited by 73 · see citing works
Control of intestinal motility by the Cav1.2 L‐type calcium channel in mice
Wegener, J. W., Schulla, V., Koller, A., et al. (2006) · The FASEB Journal · doi:10.1096/fj.05-5292fje · Cited by 56 · see citing works
Bradesi, S., Kokkotou, E. G., Simeonidis, S., Patierno, S., Ennes, H. S., Mittal, Y., McRoberts, J. A., Ohning, G., McLean, P. G., Marvizón, J. C. G., et al. (2006) · Gastroenterology · doi:10.1053/j.gastro.2006.01.037 · Cited by 54 · see citing works
zhang, M., Leung, F., Huang, Y., & Bian, Z. (2010) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2009.01467.x · Cited by 47 · see citing works
Involvement of Tachykinins in Intestinal Inflammation
Evangelista, B. S. P. S. (2001) · Current Pharmaceutical Design · doi:10.2174/1381612013398446 · Cited by 41 · see citing works
Chen, F.-X., Yu, Y., Yuan, X., et al. (2012) · Regulatory Peptides · doi:10.1016/j.regpep.2012.07.001 · Cited by 40 · see citing works
Quan, X., Luo, H., Liu, Y., Xia, H., Chen, W., & Tang, Q. (2015) · PLoS ONE · doi:10.1371/journal.pone.0121331 · Cited by 40 · see citing works
Self-citationA One-Hour Active Coping Stressor Reduces Small Bowel Transit Time in Healthy Young Adults
Ditto, B., Miller, S. B., & Barr, R. G. (1998) · Psychosomatic Medicine · doi:10.1097/00006842-199801000-00002 · Cited by 39 · see citing works
Plasma Hormones Facilitated the Hypermotility of the Colon in a Chronic Stress Rat Model
Liang, C., Luo, H., Liu, Y., Cao, J., & Xia, H. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031774 · Cited by 29 · see citing works
Self-citationPotent NK1antagonism by SR-140333 reduces rat colonic secretory response to immunocyte activation
Moriarty, D. C., Selve, N., Baird, A. W., et al. (2001) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.2001.280.4.c852 · Cited by 28 · see citing works
Scheurer, U., Drack, E., & Halter, F. (1994) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)22717-3 · Cited by 28 · see citing works
Substance P and the neurokinin-1 receptor in relation to eosinophilia in ulcerative colitis
Jönsson, M. E., Norrgård, Ö., & Forsgren, S. (2005) · Peptides · doi:10.1016/j.peptides.2004.12.018 · Cited by 25 · see citing works
Jaafari, N., Khomitch‐Baud, A., Christen, M., et al. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21359 · Cited by 24 · see citing works
Liu, Y., Luo, H., Liang, C.-B., Xia, H., Xu, W., Chen, J., & Chen, M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0055853 · Cited by 23 · see citing works
Self-citationBayguinov, O. P., Hagen, B. M., & Sanders, K. M. (2003) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0705139 · Cited by 22 · see citing works
La, J. (2005) · World Journal of Gastroenterology · doi:10.3748/wjg.v11.i2.237 · Cited by 21 · see citing works
Kojima, S., Ueda, S., Ikeda, M., et al. (2004) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0705624 · Cited by 20 · see citing works
Liu, L., Shang, F., Morgan, M. J., et al. (2009) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.108.148148 · Cited by 20 · see citing works
Beglinger, C., & Degen, L. P. (2002) · Gut · doi:10.1136/gut.51.suppl_1.i45 · Cited by 20 · see citing works
Expression of the neurokinin type 1 receptor in the human colon
Boutaghou‐Cherid, H., Porcher, C., Liberge, M., et al. (2005) · Autonomic Neuroscience · doi:10.1016/j.autneu.2005.10.002 · Cited by 18 · see citing works
Modulation of colonic motility by substance P, cholecystokinin and neuropeptide Y
Mangel, A. W., Fitz, J. G., & Taylor, I. L. (1991) · Peptides · doi:10.1016/0196-9781(91)90061-s · Cited by 15 · see citing works
Kong, Z., Han, M. S., Yang, W., et al. (2009) · Neuropeptides · doi:10.1016/j.npep.2009.03.004 · Cited by 6 · see citing works
Contractile effect of tachykinins on Suncus murinus (house musk shrew) isolated ileum
Cheng, F. H. M., Chan, S. W., & Rudd, J. A. (2008) · Neuropeptides · doi:10.1016/j.npep.2008.05.002 · Cited by 6 · see citing works
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Stress triggers flare of inflammatory bowel disease in children and adults
Sun, Y., Li, L., Xie, R., Wang, B., Jiang, K., & Cao, H. (2019) · Frontiers in Pediatrics · doi:10.3389/fped.2019.00432 · Cited by 171 · see citing works
Yan, D., Liu, X., & Guo, S.-W. (2019) · Scientific Reports · doi:10.1038/s41598-019-39170-w · Cited by 82 · see citing works
- Authors
- Lu, P., Luo, H., Quan, X., Fan, H., Tang, Q., Yu, G., Chen, W., & Xia, H.
- Affiliations
- Renmin Hospital of Wuhan University (CN)
- Corresponding author
- Luo, Hesheng
- Venue
- Neuropeptides
- Publisher
- Elsevier BV
- Published
- 2016-04
- Volume
- 56
- Pages
- 75-82
- ISSN
- 0143-4179 (ISSN-L)
- OpenAlex
- W2268600191
- Cited by
- 11
- References
- 40
- Citations by year
- 2024: 1 · 2023: 3 · 2022: 1 · 2020: 1 · 2019: 2 · 2018: 1 · 2017: 1 · 2016: 1
- FWCI
- 1.81
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuropeptides (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Natural Science Foundation of Hubei Province (2013CFA128)
- Topics
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Health Sciences › Medicine › Surgery › Congenital gastrointestinal and neural anomalies
- Keywords
- substance P, chronic stress, water avoidance stress, irritable bowel syndrome, neurokinin-1 receptor, L-type calcium channels, smooth muscle contraction, gastrointestinal motility disorders, NK1 receptor antagonists, myenteric plexus
- MeSH terms
- Animals, Colon, Gastrointestinal Motility, Male, Muscle, Smooth, Myenteric Plexus, Stress, Psychological, Substance P, Rats, Wistar, Receptors, Neurokinin-1, Receptors, Neurokinin-2, Calcium Channels, L-Type, Rats
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