Adaptation of stress-induced mucosal pathophysiology in rat colon involves opioid pathways
Abstract
Acute stress increases ion secretion and permeability of rat colonic epithelium. However, it is not known if stress-induced mucosal changes are subject to adaptation. Wistar-Kyoto rats were exposed to either continuous water-avoidance stress (CS) for 60 min or intermittent stress (IS) for three 20-min periods. Distal colonic segments were mounted in Ussing Chambers, and ion-transport [short-circuit current ( I sc)] and permeability [conductance and flux of horseradish peroxidase (HRP)] parameters were measured. CS significantly increased I sc, conductance, and HRP flux compared with control values. In contrast, in IS rats these variables were similar to those in nonstressed controls. To study the pathways involved in IS-induced adaptation, rats were pretreated intraperitoneally with the opioid antagonists naloxone or methylnaloxone. Opioid antagonists had no effect on values in control or CS rats. However, in the IS group, naloxone and methylnaloxone reversed the adaptive responses, and all variables increased to CS values. We conclude that stress-induced colonic mucosal pathophysiology is subject to rapid adaptation, which involves opioid pathways.
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Stressful stimuli can enhance the permeability of the intestinal epithelium, which allows bacterial antigens to penetrate the gut epithelium and triggers an immune response in the intestinal mucosa.
“For example, several studies have demonstrated that stressful stimuli can enhance the permeability of the intestinal epithelium, which allows bacterial antigens to penetrate the gut epithelium and triggers an immune response in the intestinal mucosa.23-27”
From Principles and clinical implications of the brain-gut-enteric microbiota axis (2009) · cites this paper as [25]
Cites
II. Stress and intestinal barrier function
Söderholm, J. D., & Perdue, M. H. (2001) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.2001.280.1.g7 · Cited by 467 · see citing works
Self-citationStress and Exacerbation in Ulcerative Colitis: A Prospective Study of Patients Enrolled in Remission
Levenstein, S., Prantera, C., Varvo, V., Scribano, M. L., Andreoli, A., Luzi, C., Arcà, M., Berto, E., Milite, G., & Marcheggiano, A. (2000) · American Journal of Gastroenterology · doi:10.1111/j.1572-0241.2000.02012.x · Cited by 451 · see citing works
Level of chronic life stress predicts clinical outcome in irritable bowel syndrome
Bennett, E. J., Tennant, C. C., Piesse, C., Badcock, C.-A., & Kellow, J. E. (1998) · Gut · doi:10.1136/gut.43.2.256 · Cited by 405 · cited 1× · see citing works
“CLINICAL DATA IMPLICATE psychological stress as an important determinant in the reactivation of inflammatory bowel disease (1, 20), as well as a contributing factor in irritable bowel syndrome, gastric ulcers, and gastric hemorrhage (4, 13).”
BackgroundGastrointestinal Illness and the Biopsychosocial Model
Drossman, D. A. (1998) · Psychosomatic Medicine · doi:10.1097/00006842-199805000-00007 · Cited by 388 · see citing works
Qiu, B., Vallance, B. A., Blennerhassett, P. A., & Collins, S. M. (1999) · Nature Medicine · doi:10.1038/13503 · Cited by 252 · see citing works
Castagliuolo, I., LaMont, J. T., Qiu, B., Fleming, S. M., Bhaskar, K. R., Nikulásson, S. Þ., Kornetsky, C. H., & Pothoulakis, C. (1996) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.1996.271.5.g884 · Cited by 251 · see citing works
Corticotropin-releasing hormone mimics stress-induced colonic epithelial pathophysiology in the rat
Santos, J., Saunders, P. R., Hanssen, N. P. M., Yang, P., Yates, D. A., Groot, J. A., & Perdue, M. H. (1999) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.1999.277.2.g391 · Cited by 251 · see citing works
Self-citationRelease of mast cell mediators into the jejunum by cold pain stress in humans
Santos, J., Saperas, E., Nogueiras, C., Mourelle, M., Antolín, M., Cadahia, A., & Malagelada, J. (1998) · Gastroenterology · doi:10.1016/s0016-5085(98)70577-3 · Cited by 237 · see citing works
Self-citationStress stimulates transepithelial macromolecular uptake in rat jejunum
Kiliaan, A. J., Saunders, P. R., Bijlsma, P. B., Berin, M. C., Taminiau, J. A., Groot, J. A., & Perdue, M. H. (1998) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.1998.275.5.g1037 · Cited by 223 · see citing works
Self-citationAcute stressors stimulate ion secretion and increase epithelial permeability in rat intestine
Saunders, P. R., Kosecka, U., McKay, D. M., & Perdue, M. H. (1994) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.1994.267.5.g794 · Cited by 215 · see citing works
Self-citationRole of CRF in Stress‐Related Alterations of Gastric and Colonic Motor Functiona
Taché, Y., Mönnikes, H., Bonaz, B. L., & Rivier, J. (1993) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1993.tb49936.x · Cited by 206 · see citing works
Chronic stress impairs rat growth and jejunal epithelial barrier function: role of mast cells
Santos, J., Benjamin, M. A., Yang, P., Prior, T., & Perdue, M. H. (2000) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.2000.278.6.g847 · Cited by 205 · see citing works
Self-citationHuether, G. (1996) · Progress in Neurobiology · doi:10.1016/0301-0082(96)00003-2 · Cited by 155 · see citing works
Adeno-associated virus 2 co-receptors?
Qiu, J., Mizukami, H., & Brown, K. E. (1999) · Nature Medicine · doi:10.1038/8328 · Cited by 135 · see citing works
Stress-induced behavioral responses and multiple opioid systems in the brain
Yamada, K., & Nabeshima, T. (1995) · Behavioural Brain Research · doi:10.1016/0166-4328(94)00150-e · Cited by 134 · see citing works
Control of guinea pig intestinal electrolyte secretion by a delta-opiate receptor.
Kachur, J. F., Miller, R. J., & Field, M. (1980) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.77.5.2753 · Cited by 121 · see citing works
Cholinergic nerves mediate stress-induced intestinal transport abnormalities in Wistar-Kyoto rats
Saunders, P. R., Hanssen, N. P. M., & Perdue, M. H. (1997) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.1997.273.2.g486 · Cited by 118 · see citing works
Self-citationCorticotropin-releasing factor in antinociception and inflammation
Schäfer, M., Mousa, S. A., & Stein, C. (1997) · European Journal of Pharmacology · doi:10.1016/s0014-2999(97)00057-5 · Cited by 109 · see citing works
Effect of psychological stress on salt and water transport in the human jejunum
Barclay, G. R., & Turnberg, L. A. (1987) · Gastroenterology · doi:10.1016/0016-5085(87)90319-2 · Cited by 109 · see citing works
Colonic mucin release in response to immobilization stress is mast cell dependent
Castagliuolo, I., Wershil, B. K., Karalis, K. P., Pasha, A., Nikulásson, S. Þ., & Pothoulakis, C. (1998) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.1998.274.6.g1094 · Cited by 102 · see citing works
Stress and intestinal barrier function
Wang, H. (2002) · Parenteral & Enteral Nutrition · Cited by 97 · see citing works
Škultétyová, I., Tokarev, D., & Ježová, D. (1998) · Brain Research Bulletin · doi:10.1016/s0361-9230(97)00335-3 · Cited by 87 · see citing works
Blood‐brain barrier permeability and immobilization stress
Belova, T. I., & JONSSON, G. (1982) · Acta Physiologica Scandinavica · doi:10.1111/j.1748-1716.1982.tb10594.x · Cited by 79 · see citing works
Opioid receptors on guinea‐pig intestinal crypt epithelial cells.
Lang, M., Davison, J. S., Bates, S., & Meddings, J. B. (1996) · The Journal of Physiology · doi:10.1113/jphysiol.1996.sp021757 · Cited by 60 · see citing works
Opioid regulation of mucosal ion transport in the mouse isolated jejunum.
Sheldon, R. J., Rivière, P. J.-M., Malarchik, M. E., Moseberg, H. I., Burks, T. F., & Porreca, F. (1990) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)12435-x · Cited by 54 · see citing works
Stress and mind-body impact on the course of inflammatory bowel diseases.
Anton, P. A. (1999) · PubMed · Cited by 52 · see citing works
Role of Opioid Ligands in the Irritable Bowel Syndrome
Corazziari, E. S. (1999) · Canadian Journal of Gastroenterology and Hepatology · doi:10.1155/1999/598659 · Cited by 47 · see citing works
Calogero, A. E., Scaccianoce, S., Burrello, N., Nicolai, R., Muscolo, L. A. A., Kling, M. A., Angelucci, L., & D’Agata, R. (1996) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1996.tb00691.x · Cited by 44 · see citing works
George, T. P. (2000) · Neuropsychopharmacology · doi:10.1016/s0893-133x(99)00165-7 · Cited by 30 · see citing works
Delta-Opioid Receptor mRNA Expression and Immunohistochemical Localization in Porcine Ileum
Brown, D. R., Poonyachoti, S., Osinski, M. A., Kowalski, T. R., Pampusch, M. S., Elde, R. P., & Murtaugh, M. P. (1998) · Digestive Diseases and Sciences · doi:10.1023/a:1018877823534 · Cited by 27 · see citing works
Opiate binding sites in mucosa of pig small intestine
Quito, F. L., Seybold, V. S., & Brown, D. R. (1991) · Life Sciences · doi:10.1016/0024-3205(91)90297-o · Cited by 19 · see citing works
Coping styles, opioid blockade, and cardiovascular response to stress
Bruehl, S. P., McCubbin, J. A., Wilson, J. F., Montgomery, T. B., Ibarra, P., & Carlson, C. R. (1994) · Journal of Behavioral Medicine · doi:10.1007/bf01856880 · Cited by 19 · see citing works
Naloxone Exacerbates Intestinal and Systemic Anaphylaxis in the Rat
Djuric, V., Wang, L., Bienenstock, J., & Perdue, M. H. (1995) · Brain Behavior and Immunity · doi:10.1006/brbi.1995.1010 · Cited by 11 · see citing works
Self-citationNaloxone and Experimental Spinal Cord Injury: Effect of Varying Dose and Intensity of Injury
BLACK, P., Markowitz, R. S., GILLESPIE, J. A., & Finkelstein, S. D. (1991) · Journal of Neurotrauma · doi:10.1089/neu.1991.8.157 · Cited by 8 · see citing works
Postnatal naltrindole treatments induce behavioural modifications in preweanling rats
Martín‐Fernández, B., Romero, E., Kitchen, I., & Viveros, M. (2000) · Neuroscience Letters · doi:10.1016/s0304-3940(00)00918-6 · Cited by 5 · see citing works
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Mayer, E. A., Tillisch, K., & Gupta, A. (2015) · Journal of Clinical Investigation · doi:10.1172/jci76304 · Cited by 1,503 · see citing works
Principles and clinical implications of the brain-gut-enteric microbiota axis
Rhee, S. H., Pothoulakis, C., & Mayer, E. A. (2009) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2009.35 · Cited by 1,342 · see citing works
Brain gut microbiome interactions and functional bowel disorders
Mayer, E. A., Savidge, T., & Shulman, R. J. (2014) · Gastroenterology · doi:10.1053/j.gastro.2014.02.037 · Cited by 496 · see citing works
The Gut-Brain Axis: Influence of Microbiota on Mood and Mental Health.
Appleton, J. (2018) · Europe PMC (PubMed Central) · Cited by 337 · see citing works
Söderholm, J. D., Yates, D. A., Gareau, M. G., Yang, P.-C., MacQueen, G., & Perdue, M. H. (2002) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00314.2002 · Cited by 243 · see citing works
Self-citationCellular and Molecular Basis of Intestinal Barrier Dysfunction in the Irritable Bowel Syndrome
Martínez, C., González-Castro, A. M., Vicario, M., & Santos, J. (2012) · Gut and Liver · doi:10.5009/gnl.2012.6.3.305 · Cited by 115 · see citing works
Self-citationTreatment of opioid-induced gut dysfunction
Holzer, P. D. (2007) · Expert Opinion on Investigational Drugs · doi:10.1517/13543784.16.2.181 · Cited by 109 · see citing works
Preclinical studies of opioids and opioid antagonists on gastrointestinal function
Meerveld, B. G., Gardner, C. J., Little, P., Hicks, G. A., & DeHaven‐Hudkins, D. L. (2004) · Neurogastroenterology & Motility · doi:10.1111/j.1743-3150.2004.00555.x · Cited by 101 · see citing works
Gui, X. S., Carraway, R. E., & Dobner, P. R. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.04.034 · Cited by 53 · see citing works
Pharmacological investigations on adaptation in rats subjected to cold water immersion stress
Agrawal, A., Jaggi, A. S., & Singh, N. (2011) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.02.014 · Cited by 52 · see citing works
Hyland, N. P., O’Mahony, S. M., O’Malley, D., O'Mahony, C. M., Dinan, T. G., & Cryan, J. F. (2014) · Neurogastroenterology & Motility · doi:10.1111/nmo.12486 · Cited by 44 · see citing works
Zhang, L., Gong, J. T., Zhang, H. Q., Song, Q. H., Xu, G., Cai, L., Tang, X. D., Zhang, H. F., Liu, F., Jia, Z., et al. (2014) · Journal of Neurogastroenterology and Motility · doi:10.5056/jnm14119 · Cited by 41 · see citing works
Sanger, G. J., & Tuladhar, B. R. (2004) · Neurogastroenterology & Motility · doi:10.1111/j.1743-3150.2004.00556.x · Cited by 39 · see citing works
Endogenous opiates and behavior: 2001
Bodnar, R. J., & Hadjimarkou, M. M. (2002) · Peptides · doi:10.1016/s0196-9781(02)00306-6 · Cited by 36 · see citing works
Zou, N., Lv, H., Li, J., Yang, N., Xue, H., Zhu, J., & Qian, J. (2008) · Translational research · doi:10.1016/j.trsl.2008.10.002 · Cited by 38 · see citing works
Bajka, B. H., M., G. C., Steeb, C. B., Read, L. C., & Howarth, G. S. (2003) · Scandinavian Journal of Gastroenterology · doi:10.1080/00365520310003101 · Cited by 35 · see citing works
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Bao, Z., Zhang, Z., Zhou, G., Zhang, A., Shao, A., & Zhou, F. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.871720 · Cited by 22 · see citing works
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Gernone, F., Uva, A., Silvestrino, M., Cavalera, M. A., & Zatelli, A. (2022) · Biology · doi:10.3390/biology11091290 · Cited by 13 · see citing works
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Petrella, C., Agostini, S., Guerrini, R., Calò, G., Giaquinto, A., Nuccio, C. D., Improta, G., & Broccardo, M. (2011) · Pharmacological Research · doi:10.1016/j.phrs.2011.06.007 · Cited by 13 · see citing works
Aschenbach, J. R., Ahrens, F., Schwelberger, H. G., Fürll, B., Roesler, U. H., Hensel, A., & Gäbel, G. (2006) · Scandinavian Journal of Gastroenterology · doi:10.1080/00365520601053297 · Cited by 13 · see citing works
Bouritius, H., van Hoorn, D. E. C., Oosting, A., van Middelaar‐Voskuilen, M. C., van Limpt, C. J. P., Lamb, K. J., van Leeuwen, P. A. M., Vriesema, A. J. M., & van Norren, K. (2008) · Journal of Parenteral and Enteral Nutrition · doi:10.1177/0148607108316191 · Cited by 12 · see citing works
Xiao-zhi, X., Zhao, Z., Qi, D., & Wang, Z.-M. (2006) · World Journal of Gastroenterology · doi:10.3748/wjg.v12.i14.2288 · Cited by 11 · see citing works
Yang, P., Tu, Y., Perdue, M. H., Oluwole, C., & Struiksma, S. (2009) · Europe PMC (PubMed Central) · Cited by 11 · see citing works
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Söderholm, J. D., & Perdue, M. H. (2006) · Elsevier eBooks · doi:10.1016/b978-012088394-3/50031-3 · Cited by 5 · see citing works
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Wójcik, M., Boreński, G., Poleszak, J., Szabat, M., Złakowska, P., & Milanowska, J. (2019) · World Scientific News · Cited by 1 · see citing works
Inflammation, Microflora, Motility, and Visceral Sensitivity
Michail, S. K., & Ng, M.-W. (2012) · Humana Press eBooks · doi:10.1007/978-1-60761-709-9_5
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Nilsson, M. (2015) · Aalborg University Library · doi:10.5278/vbn.phd.med.00040
- Authors
- Yates, D. A., Santos, J., Söderholm, J. D., & Perdue, M. H.
- Affiliations
- McMaster University (CA)
- Venue
- American Journal of Physiology-Gastrointestinal and Liver Physiology
- Publisher
- American Physiological Society
- Published
- 2001-07-01
- Volume
- 281
- Issue
- 1
- Pages
- G124-G128
- ISSN
- 0193-1857 (ISSN-L)
- 1522-1547
- OpenAlex
- W1870487270
- Cited by
- 32
- References
- 35
- Citations by year
- 2022: 2 · 2019: 1 · 2018: 1 · 2015: 2 · 2014: 3 · 2012: 4
- FWCI
- 1.90
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- American Journal of Physiology-Gastrointestinal and Liver Physiology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- acute stress, colonic mucosa, stress adaptation, opioid pathway, naloxone, ion secretion, epithelial permeability, short-circuit current, water avoidance stress, colonic epithelium
- MeSH terms
- Adaptation, Physiological, Analgesics, Opioid, Animals, Colon, Feces, Gastrointestinal Motility, Intestinal Absorption, Intestinal Mucosa, Male, Naloxone, Narcotic Antagonists, Oxymorphone, Rats, Inbred WKY, Stress, Physiological, Opioid Peptides, Rats, In Vitro Techniques
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