Brain-gut axis: From the conditioned reflex to the microbiota-gut-brain communication system

Klara Gyires

doi:10.33910/2687-1270-2020-1-4-266-276

Авторы

Klara Gyires Department of Pharmacology and Pharmacotherapy, Semmelweis University

DOI:

https://doi.org/10.33910/2687-1270-2020-1-4-266-276

Ключевые слова:

brain-gut, gut-brain axis, microbiomes, stress, mental disorders, gastric ulceration, inflammatory bowel disease (IBD)

Аннотация

Communication between the central nervous system (CNS) and the gastrointestinal tract is called the brain-gut axis. This communication network includes the CNS, hypothalamic-pituitary-adrenal axis, the autonomic nervous system (sympathetic and parasympathetic), the enteric nervous system and the gut microbiota. From the conditioned reflex activity in gastric acid secretion discovered by Pavlov to the recognition of the role of CNS in stress-induced gastric ulcer and exacerbation of intestinal inflammation, all these facts confirm the significance of brain-gut axis. Moreover, mental illnesses and depression also result in high risk for developing subsequent gastrointestinal mucosal injury. The brain-gut axis is bidirectional; therefore, not only the CNS affects the gastrointestinal functions, but the gut information is also forwarded to the CNS, which may modify its activity. Several observations suggested that changes in microbiome composition can be manifested in alterations of behavior and cognition; and a strong correlation between dysbiosis and psychiatric disorders has been observed. These observations substantially contributed to the establishment of the concept of the microbiota-gut-brain axis. The present work aims to overview the mutual role of brain-gut-microbiota and microbiota-gut-brain axis in the development of gastrointestinal and mental disorders as well as their mechanisms.

Библиографические ссылки

Abdel-Salam, O. M. E., Czimmer, J., Drebreceni, A. et al. (2001) Gastric mucosal integrity: Gastric mucosal blood flow and microcirculation. An overview. Journal of Physiology-Paris, vol. 95, no. 1-6, pp. 105–127. DOI: 10.1016/S0928-4257(01)00015-8 (In English)

Ambrosini, Y. M., Borcherding, D., Kanthasamy, A. et al. (2019) The gut-brain axis in neurodegenerative diseases and relevance of the canine model: A review. Frontiers in Aging Neuroscience, vol. 11, article 130. DOI: 10.3389/fnagi.2019.00130 (In English)

Banks, W. A., Erickson, M. A. (2010) The blood-brain barrier and immune function and dysfunction. Neurobiology of Disease, vol. 37, no. 1, pp. 26–32. DOI: 10.1016/j.nbd.2009.07.031 (In English)

Banks, W. A. (2005) Blood-brain barrier transport of cytokines: A mechanism for neuropathology. Current Pharmaceutical Design, vol. 11, no. 8, pp. 973–984. DOI: 10.2174/1381612053381684 (In English)

Beynon, S. B., Walker, F. R. (2012) Microglial activation in the injured and healthy brain: What are we really talking about? Practical and theoretical issues associated with the measurement of changes in microglial morphology. Neuroscience, vol. 225, pp. 162–171. DOI: 10.1016/j.neuroscience.2012.07.029 (In English)

Bonaz, B., Bazin, T., Pellissier, S. (2018) The vagus nerve at the interface of the microbiota-gut-brain Axis. Frontiers in Neuroscience, vol. 12, article 49. DOI: 10.3389/fnins.2018.00049 (In English)

Bonaz, B. L., Bernstein, C. N. (2013) Brain-gut interactions in inflammatory bowel disease. Gastroenterology, vol. 144, no. 1, pp. 36–49. DOI: 10.1053/j.gastro.2012.10.003 (In English)

Brzozowski, B., Mazur-Bialy, A., Pajdo, R. et al. (2016) Mechanisms by which stress affects the experimental and clinical inflammatory bowel disease (IBD): Role of brain-gut axis. Current Neuropharmacology, vol. 14, no. 8, pp. 892–900. DOI: 10.2174/1570159x14666160404124127 (In English)

Byrne, G., Rosenfeld, G., Leung, Y. et al. (2017) Prevalence of anxiety and depression in patients with inflammatory bowel disease. Canadian Journal of Gastroenterology and Hepatology, vol. 2017, article 6496727. DOI: 10.1155/2017/6496727 (In English)

Carabotti, M., Scirocco, A., Maselli, M. A. et al. (2015) The gut-brain axis: Interactions between enteric microbiota, central and enteric nervous systems. Annals of Gastroenterology, vol. 28, no. 2, pp. 203–209. PMID: 25830558. (In English)

Chen, C., Brown, D. R., Xie, Y. et al. (2003) Catecholamines modulate Escherichia coli O157:H7 adherence to murine cecal mucosa. Shock, vol. 20, no. 2, pp. 183–188. DOI: 10.1097/01.shk.0000073867.66587.e0 (In English)

Collins, S. M. (2020) Interrogating the gut-brain axis in the context of inflammatory bowel disease: A translational approach. Inflammatory Bowel Diseases, vol. 26, no. 4, pp. 493–501. DOI: 10.1093/ibd/izaa004 (In English)

Cushing, H. (1932) Peptic ulcers and the interbrain. Surgery, Gynecology and Obstetrics, vol. 55, pp. 1–34. (In English)

Dantzer, R. (2009) Cytokine, sickness behavior, and depression. Immunology and Allergy Clinics of North America, vol. 29, no. 2, pp. 247–264. DOI: 10.1016/j.iac.2009.02.002 (In English)

Eckburg, P. B., Bik, E. M., Bernstein, C. M. et al. (2005) Diversity of the human intestinal microbial flora. Science, vol. 308, no. 5728, pp. 1635–1638. DOI: 10.1126/science.1110591 (In English)

Emanuele, E., Orsi, P., Boso, M. et al. (2010) Low-grade endotoxemia in patients with severe autism. Neuroscience Letters, vol. 471, no. 3, pp. 162–165. DOI: 10.1016/j.neulet.2010.01.033 (In English)

Eisenstein, M. (2016) Microbiome: Bacterial broadband. Nature, vol. 533, no. 7603, pp. S104–S106. DOI: 10.1038/533S104a (In English)

Fan, W., Zhang, S., Hu, J. et al. (2019) Aberrant brain function in active-stage ulcerative colitis patients: A resting-state functional MRI study. Frontiers in Human Neuroscience, vol. 13, article 107. DOI: 10.3389/fnhum.2019.00107 (In English)

Filaretova, L., Bagaeva, T. (2016) The realization of the brain-gut interactions with corticotropin-releasing factor and glucocorticoids. Current Neuropharmacology, vol. 14, no. 8, pp. 876–881. DOI: 10.2174/1570159x14666160614094234 (In English)

Filipovic, B. R., Filipovic, B. F. (2014) Psychiatric comorbidity in the treatment of patients with inflammatory bowel disease. World Journal of Gastroenterology, vol. 20, no. 13, pp. 3552–3563. DOI: 10.3748/wjg.v20.i13.3552 (In English)

Galley, J. D., Nelson, M. C., Yu, Z. et al. (2014) Exposure to a social stressor disrupts the community structure of the colonic mucosa-associated microbiota. BMC Microbiology, vol. 14, article 189. DOI: 10.1186/1471-2180-14-189 (In English)

Ghia, J.-E., Blennerhassett, P., Collins, S. M. (2008) Impaired parasympathetic function increases susceptibility to inflammatory bowel disease in a mouse model of depression. Journal of Clinical Investigation, vol. 118, no. 6, pp. 2209–2218. DOI: 10.1172/jci32849 (In English)

Ghia, J.-E., Blennerhassett, P., Kumar-Ondiveeran, H. et al. (2006) The vagus nerve: A tonic inhibitory influence associated with inflammatory bowel disease in a murine model. Gastroenterology, vol. 131, no. 4, pp. 1122–1130. DOI: 10.1053/j.gastro.2006.08.016 (In English)

Ghia, J.-E., Park, A. J., Blennerhassett, P. et al. (2011) Adoptive transfer of macrophage from mice with depression-like behavior enhances susceptibility to colitis. Inflammatory Bowel Diseases, vol. 17, no. 7, pp. 1474–1489. DOI: 10.1002/ibd.21531 (In English)

Goodwin, R. D., Talley, N. J., Hotopf, M. et al. (2013) A link between physician-diagnosed ulcer and anxiety disorders among adults. Annals of Epidemiology, vol. 23, no. 4, pp. 189–192. DOI: 10.1016/j.annepidem.2013.01.003 (In English)

Gyires, K., Németh, J., Zádori, Z. S. (2013) Gastric mucosal protection and central nervous system. Current Pharmaceutical Design, vol. 19, no. 1, pp. 34–39. DOI: 10.2174/13816128130107 (In English)

Gyires, K., Rónai, A. Z. (2001) Supraspinal delta- and mu-opioid receptors mediate gastric mucosal protection in the rat. Journal of Pharmacology and Experimental Therapeutics, vol. 297, no. 3, pp. 1010–1015. PMID: 11356923. (In English)

Gyires, K., Zádori, Z. S. (2014) Brain neuropeptides in gastric mucosal protection. Current Opinion in Pharmacology, vol. 19, pp. 24–30. DOI: 10.1016/j.coph.2014.06.002 (In English)

Holzer, P., Farzi, A. (2014). Neuropeptides and the microbiota-gut-brain axis. Advances in Experimental Medicine and Biology, vol. 817, pp. 195–219. DOI: 10.1007/978-1-4939-0897-4_9 (In English)

Holzer, P., Hassan, A. M., Jain, P. et al. (2015) Neuroimmune pharmacological approaches. Current Opinion in Pharmacology, vol. 25, pp. 13–22. DOI: 10.1016/j.coph.2015.09.003 (In English)

Holzer, P., Pabst, M. A., Lippe, I. T. et al. (1990) Afferent nerve-mediated protection against deep mucosal damage in the rat stomach. Gastroenterology, vol. 98, no. 4, pp. 838–848. DOI: 10.1016/0016-5085(90)90005-l (In English)

Kim, K.-A., Gu, W., Lee, I.-A. et al. (2012) High fat diet-induced gut microbiota exacerbates inflammation and obesity in mice via the TLR4 signaling pathway. PLoS One, vol. 7, no. 10, article e47713. DOI: 10.1371/journal. pone.0047713 (In English)

Konturek, S. J., Konturek, P. C., Brzozowski, T. et al. (2005) From nerves and hormones to bacteria in the stomach; Nobel prize for achievements in gastrology during last century. Journal of Physiology and Pharmacology, vol. 56, no. 4, pp. 507–530. PMID: 16391411. (In English)

Koob, G. F. (1999) Corticotropin-releasing factor, norepinephrine, and stress. Biological Psychiatry, vol. 46, no. 9, pp. 1167–1180. DOI: 10.1016/s0006-3223(99)00164-x (In English)

Kurina, L. M., Goldacre, M. J., Yeates, D., Gill, L. E. (2001) Depression and anxiety in people with inflammatory bowel disease. Journal of Epidemiology and Community Health, vol. 55, no. 10, pp. 716–720. DOI: 10.1136/jech.55.10.716 (In English)

Lyte, M. (2013) Microbial endocrinology in the microbiome-gut-brain axis: How bacterial production and utilization of neurochemicals influence behavior. PLoS Pathogens, vol. 9, no. 11, article e1003726. DOI: 10.1371/journal.ppat.1003726 (In English)

Mangiola, F., Ianiro, G., Franceschi, F. et al. (2016) Gut microbiota in autism and mood disorders. World Journal of Gastroenterology, vol. 22, no. 1, pp. 361–368. DOI: 10.3748/wjg.v22.i1.361 (In English)

Mao, Y.-K., Kasper, D. L., Wang, B. et al. (2013) Bacteroides fragilis polysaccharide A is necessary and sufficient for acute activation of intestinal sensory neurons. Nature Communications, vol. 4, article 1465. DOI: 10.1038/ncomms2478 (In English)

Matteoli, G., Boeckxstaens, G. E. (2013) The vagal innervation of the gut and immune homeostasis. Gut, vol. 62, no. 8, pp. 1214–1222. DOI: 10.1136/gutjnl-2012-302550 (In English)

Mawdsley, J. E., Rampton, D. S. (2006) The role of psychological stress in inflammatory bowel disease. Neuroimmunomodulation, vol. 13, no. 5-6, pp. 327–336. DOI: 10.1159/000104861 (In English)

Monnig, A. A., Prittie, J. E. (2011) A review of stress-related mucosal disease. Journal of Veterinary Emergency and Critical Care (San Antonio), vol. 21, no. 5, pp. 484–495. DOI: 10.1111/j.1476-4431.2011.00680.x (In English)

Mueller, N. T., Bakacs, E., Combellick, J. et al. (2015) The infant microbiome development: Mom matters. Trends in Molecular Medicine, vol. 21, no. 2, pp. 109–117. DOI: 10.1016/j.molmed.2014.12.002 (In English)

Nikolaus, S., Bauditz, J., Gionchetti, P. et al. (1998) Increased secretion of pro-inflammatory cytokines by circulating polymorphonuclear neutrophils and regulation by interleukin 10 during intestinal inflammation. Gut, vol. 42, no. 4, pp. 470–476. DOI: 10.1136/gut.42.4.470 (In English)

Nyuyki, K. D., Cluny, N. L., Swain, M. G. et al. (2018) Altered brain excitability and increased anxiety in mice with experimental colitis: Consideration of hyperalgesia and sex differences. Frontiers in Behavioral Neuroscience, vol. 12, article 58. DOI: 10.3389/fnbeh.2018.00058 (In English)

Ozdemir, V., Jamal, M. M., Osapay, K. et al. (2007) Cosegregation of gastrointestinal ulcers and schizophrenia in a large national inpatient discharge database: Revisiting the “brain-gut axis” hypothesis in ulcer pathogenesis. Journal of Investigative Medicine, vol. 55, no. 6, pp. 315–320. DOI: 10.2310/6650.2007.00014 (In English)

Parracho, H. M., Bingham, M. O., Gibson, G. R., McCartney, A. L. (2005) Differences between the gut microflora of children with autistic spectrum disorders and that of healthy children. Journal of Medical Microbiology, vol. 54, no. 10, pp. 987–991. DOI: 10.1099/jmm.0.46101-0 (In English)

Pavlov, I. P., Thompson, W. H. (1902) The work of the digestive glands: Lectures by Professor J. P. Pawlow. London: Charles Griffin & Co. Ltd, 196 p. DOI: 10.5962/bhl.title.3784 (In English)

Pawlik, M. W., Obuchowicz, R., Biernat, J. et al. (2011) Effects of peripherally and centrally applied ghrelin in the pathogenesis of ischemia-reperfusion induced injury of the small intestine. Journal of Physiology and Pharmacology, vol. 62, no. 4, pp. 429–439. PMID: 22100844. (In English)

Persoons, P., Vermeire, S., Demyttenaere, K. et al. (2005) The impact of major depressive disorder on the short- and long-term outcome of Crohn’s disease treatment with infliximab. Alimentary Pharmacology Therapeutics, vol. 22, no. 2, pp. 101–110. DOI: 10.1111/j.1365-2036.2005.02535.x (In English)

Polidori, C., Massi, M., Guerrini, R. et al. (2005) Peripheral mechanisms involved in gastric mucosal protection by intracerebroventricular and intraperitoneal nociceptin in rats. Endocrinology, vol. 146, no. 9, pp. 3861–3867. DOI: 10.1210/en.2005-0397 (In English)

Qin, L., Wu, X., Block, M. L. et al. (2007) Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia, vol. 55, no. 5, pp. 453–462. DOI: 10.1002/glia.20467 (In English)

Reichmann, F., Hassan, A. M., Farzi, A. et al. (2015) Dextran sulfate sodium-induced colitis alters stress-associated behaviour and neuropeptide gene expression in the amygdala-hippocampus network of mice. Scientific Reports, vol. 5, article 9970. DOI: 10.1038/srep09970 (In English)

Saper, C. B., Romanovsky, A. A., Scammell, T. E. (2012) Neural circuitry engaged by prostaglandins during the sickness syndrome. Nature Neuroscience, vol. 15, no. 8, pp. 1088–1095. DOI: 10.1038/nn.3159 (In English)

Schiltz, J. C., Sawchenko, P. E. (2002) Distinct brain vascular cell types manifest inducible cyclooxygenase expression as a function of the strength and nature of immune insults. Journal of Neuroscience, vol. 22, no. 13, pp. 5606–5618. DOI: 10.1523/jneurosci.22-13-05606.2002 (In English)

Schuligoi, R., Jocic, M., Heinemann, A. (1998) Gastric acid-evoked c-fos messenger RNA expression in rat brainstem is signaled by capsaicin-resistant vagal afferents. Gastroenterology, vol. 115, no. 3, pp. 649–660. DOI: 10.1016/s0016-5085(98)70144-1 (In English)

Selye, H. (1936) A syndrome produced by diverse nocuous agents. Nature, vol. 138, no. 3479, p. 32. DOI: 10.1038/138032a0 (In English)

Selye, H. (1943) Perforated peptic ulcer during air-raid. The Lancet, vol. 241, no. 6234, p. 252. DOI: 10.1016/S0140-6736(00)42250-6 (In English)

Smith, G. P. (2000) Pavlov and integrative physiology. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, vol. 279, no. 3, pp. R743–R755. DOI: 10.1152/ajpregu.2000.279.3.R743 (In English)

Stilling, R. M., Dinan, T. G., Cryan, J. F. (2014) Microbial genes, brain & behaviour — epigenetic regulation of the gut-brain axis. Genes, Brain and Behavior, vol. 13, no. 1, pp. 69–86. DOI: 10.1111/gbb.12109 (In English)

Straub, R. H., Dhabhar, F. S., Bijlsma, J. W., Cutolo, M. (2005) How psychological stress via hormones and nerve fibers may exacerbate rheumatoid arthritis. Arthritis & Rheumatology, vol. 52, no. 1, pp. 16–26. DOI: 10.1002/art.20747 (In English)

Szabo, S., Tache, Y., Somogyi, A. (2012) The legacy of Hans Selye and the origins of stress research: A retrospective 75 years after his landmark “letter” in Nature. Stress, vol. 15, no. 5, pp. 472–478. DOI: 10.3109/10253890.2012.710919 (In English)

Tache, Y. (2012) Brainstem neuropeptides and vagal protection of the gastric mucosal against injury: Role of prostaglandins, nitric oxide and calcitonin-gene related peptide in capsaicin afferents. Current Medicinal Chemistry, vol. 19, no. 1, pp. 35–42. DOI: 10.2174/092986712803414097 (In English)

Tuglu, C., Kara, S. H., Caliyurt, O. et al. (2003) Increased serum tumor necrosis factor-alpha levels and treatment response in major depressive disorder. Psychopharmacology, vol. 170, no. 4, pp. 429–433. DOI: 10.1007/s00213-003-1566-z (In English)

Wang, L., Cardin, S., Martínez, V., Taché, Y. (1996) Intracerebroventricular CRF inhibits cold restraint-induced c-fos expression in the dorsal motor nucleus of the vagus and gastric erosions in rats. Brain Research, vol. 736, no. 1–2, pp. 44–53. DOI: 10.1016/0006-8993(96)00726-3 (In English)

Wang, Y., Kasper, L. H. (2014) The role of microbiome in central nervous system disorders. Brain, Behavior and Immunity, vol. 38, pp. 1–12. DOI: 10.1016/j.bbi.2013.12.015 (In English)

Xu, M, Wang, C., Krolick, K. N. et al. (2020) Difference in post-stress recovery of the gut microbiome and its altered metabolism after chronic adolescent stress in rats. Scientific Reports, vol. 10, no. 1, article 3950. DOI: 10.1038/s41598-020-60862-1 (In English)

Zadina, J. E., Hackler, L., Ge, L. J., Kastin, A. B. (1997) A potent and selective endogenous agonist for the mu-opiate receptor. Nature, vol. 386, no. 6624, pp. 499–502. DOI: 10.1038/386499a0 (In English)

Zhang, Y. M., Wei, E. Q., Hu, X. et al. (2008) Administration of angiotensin II in the paraventricular nucleus protects gastric mucosa from ischemia-reperfusion injury. Brain Research, vol. 1212, pp. 25–34. DOI: 10.1016/j. brainres.2008.03.028 (In English)

Zheng, G., Fon, G. V., Meixner, W. (2017) Chronic stress and intestinal barrier dysfunction: Glucocorticoid receptor and transcription repressor HES1 regulate tight junction protein Claudin-1 promoter. Scientific Reports, vol. 7, no. 1, article 4502. DOI: 10.1038/s41598-017-04755-w (In English)

Brain-gut axis: From the conditioned reflex to the microbiota-gut-brain communication system

Авторы

DOI:

Ключевые слова:

Аннотация

Библиографические ссылки

Загрузки

Опубликован

Выпуск

Раздел

Лицензия

Информация

Отправить материал

Язык

organizations

Политика

Индексация