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13.01.2022 | Original Article

Alterations to microbial secretome by estrogen may contribute to sex bias in irritable bowel syndrome

verfasst von: Lesha Pretorius, Anton du Preez Van Staden, Johannes J. Van der Merwe, Natasha Henning, Carine Smith

Erschienen in: Inflammopharmacology | Ausgabe 1/2022

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Abstract

Introduction

Irritable bowel syndrome (IBS) is a female predominant functional gastrointestinal disorder, underpinned by microbial dysbiosis and microinflammation. We suggest that changes in trace amine (TA) load and metabolism may link together diet, inflammation and sex in this context.

Methods

The effect of E2 treatment on microbial growth and TA generation was assessed using liquid chromatography and tandem mass spectrometry methodology. To investigate the effects of TAs on the gut, WST-1, prostaglandin E2 and tight junction protein dynamics were investigated in TA treated (HT-29) colon epithelial monolayer cultures.

Results

Differential E2-dependent alterations of the TA production capabilities of microbes were observed. Significantly, E2 treatment resulted in a 50% increase in tryptamine secretion from a probiotic microbe (p < 0.0001). Moreover, in vitro experiments indicated that TA treatment exerted type-specific effects in the gut, e.g., reducing mitochondrial functionality, even at low doses of tryptamine (p < 0.0001) and ρ-tyramine (p < 0.001). Additionally, prostaglandin E2 levels were significantly increased following ρ-tyramine and agmatine treatment (p < 0.05). In terms of functionality, all investigated TAs resulted in occludin redistribution and loss of zona occludens-1 and occludin co-localization.

Conclusion

Increases in the gastrointestinal TA load may contribute to a relatively pro-inflammatory outcome in the intestine, along with tight junction protein disruption. Additionally, fluctuating levels of endogenous E2 may modulate microbially-derived TA levels, potentially explaining exaggerating gastrointestinal symptomology in females during low E2 phases. Thus, current data warrants subsequent investigations in appropriate in vivo models to fully elucidate the role of the trace aminergic system in the sex bias observed in IBS.
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Literatur
Zurück zum Zitat Alonso C, Guilarte M, Vicario M, Ramos L, Ramadan Z, Antolin M, Martinez C, Rezzi S, Saperas E, Kochhar S, Santos J, Malagelada JR (2008) Maladaptive intestinal epithelial responses to life stress may predispose healthy women to gut mucosal inflammation. Gastroenterology 135:163–172PubMedCrossRef Alonso C, Guilarte M, Vicario M, Ramos L, Ramadan Z, Antolin M, Martinez C, Rezzi S, Saperas E, Kochhar S, Santos J, Malagelada JR (2008) Maladaptive intestinal epithelial responses to life stress may predispose healthy women to gut mucosal inflammation. Gastroenterology 135:163–172PubMedCrossRef
Zurück zum Zitat Alonso C, Guilarte M, Vicario M, Ramos L, Rezzi S, Martinez C, Lobo B, Martin FP, Pigrau M, Gonzalez-Castro AM, Gallart M, Malagelada JR, Azpiroz F, Kochhar S, Santos J (2012) Acute experimental stress evokes a differential gender-determined increase in human intestinal macromolecular permeability. Neurogastroenterol Motil 24(740–6):E348–E349 Alonso C, Guilarte M, Vicario M, Ramos L, Rezzi S, Martinez C, Lobo B, Martin FP, Pigrau M, Gonzalez-Castro AM, Gallart M, Malagelada JR, Azpiroz F, Kochhar S, Santos J (2012) Acute experimental stress evokes a differential gender-determined increase in human intestinal macromolecular permeability. Neurogastroenterol Motil 24(740–6):E348–E349
Zurück zum Zitat Altemus M, Sarvaiya N, Neill Epperson C (2014) Sex differences in anxiety and depression clinical perspectives. Front Neuroendocrinol 35:320–330PubMedPubMedCentralCrossRef Altemus M, Sarvaiya N, Neill Epperson C (2014) Sex differences in anxiety and depression clinical perspectives. Front Neuroendocrinol 35:320–330PubMedPubMedCentralCrossRef
Zurück zum Zitat Arai N, Strom A, Rafter JJ, Gustafsson JA (2000) Estrogen receptor beta mrna in colon cancer cells: growth effects of estrogen and genistein. Biochem Biophys Res Commun 270:425–431PubMedCrossRef Arai N, Strom A, Rafter JJ, Gustafsson JA (2000) Estrogen receptor beta mrna in colon cancer cells: growth effects of estrogen and genistein. Biochem Biophys Res Commun 270:425–431PubMedCrossRef
Zurück zum Zitat Babusyte A, Kotthoff M, Fiedler J, Krautwurst D (2013) Biogenic amines activate blood leukocytes via trace amine-associated receptors taar1 and taar2. J Leukoc Biol 93:387–394PubMedCrossRef Babusyte A, Kotthoff M, Fiedler J, Krautwurst D (2013) Biogenic amines activate blood leukocytes via trace amine-associated receptors taar1 and taar2. J Leukoc Biol 93:387–394PubMedCrossRef
Zurück zum Zitat Baker JM, Al-Nakkash L, Herbst-Kralovetz MM (2017) Estrogen-gut microbiome axis: physiological and clinical implications. Maturitas 103:45–53PubMedCrossRef Baker JM, Al-Nakkash L, Herbst-Kralovetz MM (2017) Estrogen-gut microbiome axis: physiological and clinical implications. Maturitas 103:45–53PubMedCrossRef
Zurück zum Zitat Barbieri F, Montanari C, Gardini F, Tabanelli G (2019) Biogenic amine production by lactic acid bacteria: a review. Foods 8(1):7CrossRef Barbieri F, Montanari C, Gardini F, Tabanelli G (2019) Biogenic amine production by lactic acid bacteria: a review. Foods 8(1):7CrossRef
Zurück zum Zitat Bertiaux-Vandaele N, Youmba SB, Belmonte L, Lecleire S, Antonietti M, Gourcerol G, Leroi AM, Dechelotte P, Menard JF, Ducrotte P, Coeffier M (2011) The expression and the cellular distribution of the tight junction proteins are altered in irritable bowel syndrome patients with differences according to the disease subtype. Am J Gastroenterol 106:2165–2173PubMedCrossRef Bertiaux-Vandaele N, Youmba SB, Belmonte L, Lecleire S, Antonietti M, Gourcerol G, Leroi AM, Dechelotte P, Menard JF, Ducrotte P, Coeffier M (2011) The expression and the cellular distribution of the tight junction proteins are altered in irritable bowel syndrome patients with differences according to the disease subtype. Am J Gastroenterol 106:2165–2173PubMedCrossRef
Zurück zum Zitat Bharadwaj S, Barber MD, Graff LA, Shen B (2015) Symptomatology of irritable bowel syndrome and inflammatory bowel disease during the menstrual cycle. Gastroenterol Rep 3:185–193CrossRef Bharadwaj S, Barber MD, Graff LA, Shen B (2015) Symptomatology of irritable bowel syndrome and inflammatory bowel disease during the menstrual cycle. Gastroenterol Rep 3:185–193CrossRef
Zurück zum Zitat Bohn L, Storsrud S, Tornblom H, Bengtsson U, Simren M (2013) Self-reported food-related gastrointestinal symptoms in IBS are common and associated with more severe symptoms and reduced quality of life. Am J Gastroenterol 108:634–641PubMedCrossRef Bohn L, Storsrud S, Tornblom H, Bengtsson U, Simren M (2013) Self-reported food-related gastrointestinal symptoms in IBS are common and associated with more severe symptoms and reduced quality of life. Am J Gastroenterol 108:634–641PubMedCrossRef
Zurück zum Zitat Braniste V, Leveque M, Buisson-Brenac C, Bueno L, Fioramonti J, Houdeau E (2009) Oestradiol decreases colonic permeability through oestrogen receptor beta-mediated up-regulation of occludin and junctional adhesion molecule-a in epithelial cells. J Physiol 587:3317–3328PubMedPubMedCentralCrossRef Braniste V, Leveque M, Buisson-Brenac C, Bueno L, Fioramonti J, Houdeau E (2009) Oestradiol decreases colonic permeability through oestrogen receptor beta-mediated up-regulation of occludin and junctional adhesion molecule-a in epithelial cells. J Physiol 587:3317–3328PubMedPubMedCentralCrossRef
Zurück zum Zitat Bustos V, Nolan AM, Harvey H, Parker A, Poulsom R, Mcbryan J, Thomas W, Silver A, Harvey BJ (2017) Gper mediates differential effects of estrogen on colon cancer cell proliferation and migration under normoxic and hypoxic conditions. Oncotarget 8:84258–84275PubMedPubMedCentralCrossRef Bustos V, Nolan AM, Harvey H, Parker A, Poulsom R, Mcbryan J, Thomas W, Silver A, Harvey BJ (2017) Gper mediates differential effects of estrogen on colon cancer cell proliferation and migration under normoxic and hypoxic conditions. Oncotarget 8:84258–84275PubMedPubMedCentralCrossRef
Zurück zum Zitat Campbell-Thompson M, Lynch J, Bhardwaj B (2001) Expression of estrogen receptor (Er) subtypes in colon cancer cell lines. Can Res 61:632–640 Campbell-Thompson M, Lynch J, Bhardwaj B (2001) Expression of estrogen receptor (Er) subtypes in colon cancer cell lines. Can Res 61:632–640
Zurück zum Zitat Casimir GJ, Lefevre N, Corazza F, Duchateau J, Chamekh M (2018) The acid-base balance and gender in inflammation: a mini-review. Front Immunol 9:475PubMedPubMedCentralCrossRef Casimir GJ, Lefevre N, Corazza F, Duchateau J, Chamekh M (2018) The acid-base balance and gender in inflammation: a mini-review. Front Immunol 9:475PubMedPubMedCentralCrossRef
Zurück zum Zitat Chatila R, Merhi M, Hariri E, Sabbah N, Deeb ME (2017) Irritable bowel syndrome: prevalence, risk factors in an adult lebanese population. BMC Gastroenterol 17:137–142PubMedPubMedCentralCrossRef Chatila R, Merhi M, Hariri E, Sabbah N, Deeb ME (2017) Irritable bowel syndrome: prevalence, risk factors in an adult lebanese population. BMC Gastroenterol 17:137–142PubMedPubMedCentralCrossRef
Zurück zum Zitat Chatzinikolaou G, Nikitovic D, Stathopoulos EN, Velegrakis GA, Karamanos NK, Tzanakakis GN (2007) Protein tyrosine kinase and estrogen receptor-dependent pathways regulate the synthesis and distribution of glycosaminoglycans: proteoglycans produced by two human colon cancer cell lines. Anticancer Res 27:4101–4106PubMed Chatzinikolaou G, Nikitovic D, Stathopoulos EN, Velegrakis GA, Karamanos NK, Tzanakakis GN (2007) Protein tyrosine kinase and estrogen receptor-dependent pathways regulate the synthesis and distribution of glycosaminoglycans: proteoglycans produced by two human colon cancer cell lines. Anticancer Res 27:4101–4106PubMed
Zurück zum Zitat Chong PP, Chin VK, Looi CY, Wong WF, Madhavan P, Yong VC (2019) The microbiome and irritable bowel syndrome - a review on the pathophysiology, current research and future therapy. Front Microbiol 10:1136PubMedPubMedCentralCrossRef Chong PP, Chin VK, Looi CY, Wong WF, Madhavan P, Yong VC (2019) The microbiome and irritable bowel syndrome - a review on the pathophysiology, current research and future therapy. Front Microbiol 10:1136PubMedPubMedCentralCrossRef
Zurück zum Zitat Coeffier M, Gloro R, Boukhettala N, Aziz M, Lecleire S, Vandaele N, Antonietti M, Savoye G, Bole-Feysot C, Dechelotte P, Reimund JM, Ducrotte P (2010) Increased proteasome-mediated degradation of occludin in irritable bowel syndrome. Am J Gastroenterol 105:1181–1188PubMedCrossRef Coeffier M, Gloro R, Boukhettala N, Aziz M, Lecleire S, Vandaele N, Antonietti M, Savoye G, Bole-Feysot C, Dechelotte P, Reimund JM, Ducrotte P (2010) Increased proteasome-mediated degradation of occludin in irritable bowel syndrome. Am J Gastroenterol 105:1181–1188PubMedCrossRef
Zurück zum Zitat Cuomo R, Andreozzi P, Zito FP, Passananti V, De Carlo G, Sarnelli G (2014) Irritable bowel syndrome and food interaction. World J Gastroenterol 20:8837–8845PubMedPubMedCentral Cuomo R, Andreozzi P, Zito FP, Passananti V, De Carlo G, Sarnelli G (2014) Irritable bowel syndrome and food interaction. World J Gastroenterol 20:8837–8845PubMedPubMedCentral
Zurück zum Zitat D’amato M (2013) Genes and functional gi disorders: from casual to causal relationship. Neurogastroenterol Motil 25:638–649PubMedCrossRef D’amato M (2013) Genes and functional gi disorders: from casual to causal relationship. Neurogastroenterol Motil 25:638–649PubMedCrossRef
Zurück zum Zitat Demady RD, Jianmongkol S, Vuletich JL, Bender AT, Osawa Y (2001) Agmatine enhances the nadph oxidase activity of neuronal no synthase and leads to oxidative inactivation of the enzyme. Mol Pharmacol 59:24–29PubMedCrossRef Demady RD, Jianmongkol S, Vuletich JL, Bender AT, Osawa Y (2001) Agmatine enhances the nadph oxidase activity of neuronal no synthase and leads to oxidative inactivation of the enzyme. Mol Pharmacol 59:24–29PubMedCrossRef
Zurück zum Zitat Ek WE, Reznichenko A, Ripke S, Niesler B, Zucchelli M, Rivera NV, Schmidt PT, Pedersen NL, Magnusson P, Talley NJ, Holliday EG, Houghton L, Gazouli M, Karamanolis G, Rappold G, Burwinkel B, Surowy H, Rafter J, Assadi G, Li L, Papadaki E, Gambaccini D, Marchi S, Colucci R, Blandizzi C, Barbaro R, Karling P, Walter S, Ohlsson B, Tornblom H, Bresso F, Andreasson A, Dlugosz A, Simren M, Agreus L, Lindberg G, Boeckxstaens G, Bellini M, Stanghellini V, Barbara G, Daly MJ, Camilleri M, Wouters MM, D’amato M (2015) Exploring the genetics of irritable bowel syndrome: a gwa study in the general population and replication in multinational case-control cohorts. Gut 64:1774–1782PubMedCrossRef Ek WE, Reznichenko A, Ripke S, Niesler B, Zucchelli M, Rivera NV, Schmidt PT, Pedersen NL, Magnusson P, Talley NJ, Holliday EG, Houghton L, Gazouli M, Karamanolis G, Rappold G, Burwinkel B, Surowy H, Rafter J, Assadi G, Li L, Papadaki E, Gambaccini D, Marchi S, Colucci R, Blandizzi C, Barbaro R, Karling P, Walter S, Ohlsson B, Tornblom H, Bresso F, Andreasson A, Dlugosz A, Simren M, Agreus L, Lindberg G, Boeckxstaens G, Bellini M, Stanghellini V, Barbara G, Daly MJ, Camilleri M, Wouters MM, D’amato M (2015) Exploring the genetics of irritable bowel syndrome: a gwa study in the general population and replication in multinational case-control cohorts. Gut 64:1774–1782PubMedCrossRef
Zurück zum Zitat Enck P, Aziz Q, Barbara G, Farmer AD, Fukudo S, Mayer EA, Niesler B, Quigley EM, Rajilic-Stojanovic M, Schemann M, Schwille-Kiuntke J, Simren M, Zipfel S, Spiller RC (2016) Irritable bowel syndrome. Nat Rev Dis Primers 2:16014PubMedPubMedCentralCrossRef Enck P, Aziz Q, Barbara G, Farmer AD, Fukudo S, Mayer EA, Niesler B, Quigley EM, Rajilic-Stojanovic M, Schemann M, Schwille-Kiuntke J, Simren M, Zipfel S, Spiller RC (2016) Irritable bowel syndrome. Nat Rev Dis Primers 2:16014PubMedPubMedCentralCrossRef
Zurück zum Zitat Ervin SM, Li H, Lim L, Roberts LR, Liang X, Mani S, Redinbo MR (2019) Gut microbial beta-glucuronidases reactivate estrogens as components of the estrobolome that reactivate estrogens. J Biol Chem 294:18586–18599PubMedPubMedCentralCrossRef Ervin SM, Li H, Lim L, Roberts LR, Liang X, Mani S, Redinbo MR (2019) Gut microbial beta-glucuronidases reactivate estrogens as components of the estrobolome that reactivate estrogens. J Biol Chem 294:18586–18599PubMedPubMedCentralCrossRef
Zurück zum Zitat Fernandez M, Linares DM, Rodriguez A, Alvarez MA (2007) Factors affecting tyramine production in enterococcus durans Ipla 655. Appl Microbiol Biotechnol 73:1400–1406PubMedCrossRef Fernandez M, Linares DM, Rodriguez A, Alvarez MA (2007) Factors affecting tyramine production in enterococcus durans Ipla 655. Appl Microbiol Biotechnol 73:1400–1406PubMedCrossRef
Zurück zum Zitat Gadkari TV, Cortes N, Madrasi K, Tsoukias NM, Joshi MS (2013) Agmatine induced no dependent rat mesenteric artery relaxation and its impairment in salt-sensitive hypertension. Nitric Oxide 35:65–71PubMedCrossRef Gadkari TV, Cortes N, Madrasi K, Tsoukias NM, Joshi MS (2013) Agmatine induced no dependent rat mesenteric artery relaxation and its impairment in salt-sensitive hypertension. Nitric Oxide 35:65–71PubMedCrossRef
Zurück zum Zitat Gilad LA, Bresler T, Gnainsky J, Smirnoff P, Schwartz B (2005) Regulation of vitamin d receptor expression via estrogen-induced activation of the Erk 1/2 signaling pathway in colon and breast cancer cells. J Endocrinol 185:577–592PubMedCrossRef Gilad LA, Bresler T, Gnainsky J, Smirnoff P, Schwartz B (2005) Regulation of vitamin d receptor expression via estrogen-induced activation of the Erk 1/2 signaling pathway in colon and breast cancer cells. J Endocrinol 185:577–592PubMedCrossRef
Zurück zum Zitat Gilligan LC, Gondal A, Tang V, Hussain MT, Arvaniti A, Hewitt AM, Foster PA (2017) Estrone sulfate transport and steroid sulfatase activity in colorectal cancer: implications for hormone replacement therapy. Front Pharmacol 8:103PubMedPubMedCentralCrossRef Gilligan LC, Gondal A, Tang V, Hussain MT, Arvaniti A, Hewitt AM, Foster PA (2017) Estrone sulfate transport and steroid sulfatase activity in colorectal cancer: implications for hormone replacement therapy. Front Pharmacol 8:103PubMedPubMedCentralCrossRef
Zurück zum Zitat Guo X, Rao JN, Liu L, Zou T, Keledjian KM, Boneva D, Marasa BS, Wang JY (2005) Polyamines are necessary for synthesis and stability of occludin protein in intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 288:G1159–G1169PubMedCrossRef Guo X, Rao JN, Liu L, Zou T, Keledjian KM, Boneva D, Marasa BS, Wang JY (2005) Polyamines are necessary for synthesis and stability of occludin protein in intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 288:G1159–G1169PubMedCrossRef
Zurück zum Zitat Gwilt KB, Gonzalez DP, Olliffe N, Oller H, Hoffing R, Puzan M, El Aidy S, Miller GM (2020) Actions of trace amines in the brain-gut-microbiome axis via trace amine-associated receptor-1 (Taar1). Cell Mol Neurobiol 40:191–201CrossRef Gwilt KB, Gonzalez DP, Olliffe N, Oller H, Hoffing R, Puzan M, El Aidy S, Miller GM (2020) Actions of trace amines in the brain-gut-microbiome axis via trace amine-associated receptor-1 (Taar1). Cell Mol Neurobiol 40:191–201CrossRef
Zurück zum Zitat Hanning N, Edwinson AL, Ceuleers H, Peters SA, De Man JG, Hassett LC, De Winter BY, Grover M (2021) Intestinal barrier dysfunction in irritable bowel syndrome: a systematic review. Therap Adv Gastroenterol 14:1756284821993586PubMedPubMedCentralCrossRef Hanning N, Edwinson AL, Ceuleers H, Peters SA, De Man JG, Hassett LC, De Winter BY, Grover M (2021) Intestinal barrier dysfunction in irritable bowel syndrome: a systematic review. Therap Adv Gastroenterol 14:1756284821993586PubMedPubMedCentralCrossRef
Zurück zum Zitat Heitkemper M, Jarrett M (2008) Irritable bowel syndrome: does gender matter? J Psychosom Res 64:583–587PubMedCrossRef Heitkemper M, Jarrett M (2008) Irritable bowel syndrome: does gender matter? J Psychosom Res 64:583–587PubMedCrossRef
Zurück zum Zitat Heitkemper M, Cain KC, Jarrett ME, Burr RL, Hertig V, Bond EF (2003) Symptoms across the menstrual cycle in women with irritable bowel syndrome. Am J Gastroenterol 98:420–430PubMedCrossRef Heitkemper M, Cain KC, Jarrett ME, Burr RL, Hertig V, Bond EF (2003) Symptoms across the menstrual cycle in women with irritable bowel syndrome. Am J Gastroenterol 98:420–430PubMedCrossRef
Zurück zum Zitat Honda J, Iijima K, Asanuma K, Ara N, Shiroki T, Kondo Y, Hatta W, Uno K, Asano N, Koike T, Shimosegawa T (2016) Estrogen enhances esophageal barrier function by potentiating occludin expression. Dig Dis Sci 61:1028–1038PubMedCrossRef Honda J, Iijima K, Asanuma K, Ara N, Shiroki T, Kondo Y, Hatta W, Uno K, Asano N, Koike T, Shimosegawa T (2016) Estrogen enhances esophageal barrier function by potentiating occludin expression. Dig Dis Sci 61:1028–1038PubMedCrossRef
Zurück zum Zitat Horvath A, Dziechciarz P, Szajewska H (2011) Meta-analysis: lactobacillus rhamnosus Gg for abdominal pain-related functional gastrointestinal disorders in childhood. Aliment Pharmacol Ther 33:1302–1310PubMedCrossRef Horvath A, Dziechciarz P, Szajewska H (2011) Meta-analysis: lactobacillus rhamnosus Gg for abdominal pain-related functional gastrointestinal disorders in childhood. Aliment Pharmacol Ther 33:1302–1310PubMedCrossRef
Zurück zum Zitat Jane ZY, Chang CC, Lin HK, Liu YC, Chen WL (2011) The association between the exacerbation of irritable bowel syndrome and menstrual symptoms in young taiwanese women. Gastroenterol Nurs 34:277–286PubMedCrossRef Jane ZY, Chang CC, Lin HK, Liu YC, Chen WL (2011) The association between the exacerbation of irritable bowel syndrome and menstrual symptoms in young taiwanese women. Gastroenterol Nurs 34:277–286PubMedCrossRef
Zurück zum Zitat Kennedy PJ, Cryan JF, Dinan TG, Clarke G (2014) Irritable bowel syndrome: a microbiome-gut-brain axis disorder? World J Gastroenterol 20:14105–14125PubMedPubMedCentralCrossRef Kennedy PJ, Cryan JF, Dinan TG, Clarke G (2014) Irritable bowel syndrome: a microbiome-gut-brain axis disorder? World J Gastroenterol 20:14105–14125PubMedPubMedCentralCrossRef
Zurück zum Zitat Kim HJ, Vazquez Roque MI, Camilleri M, Stephens D, Burton DD, Baxter K, Thomforde G, Zinsmeister AR (2005) A randomized controlled trial of a probiotic combination Vsl# 3 and placebo in irritable bowel syndrome with bloating. Neurogastroenterol Motil 17:687–696PubMedCrossRef Kim HJ, Vazquez Roque MI, Camilleri M, Stephens D, Burton DD, Baxter K, Thomforde G, Zinsmeister AR (2005) A randomized controlled trial of a probiotic combination Vsl# 3 and placebo in irritable bowel syndrome with bloating. Neurogastroenterol Motil 17:687–696PubMedCrossRef
Zurück zum Zitat Kuo WT, Shen L, Zuo L, Shashikanth N, Ong M, Wu L, Zha J, Edelblum KL, Wang Y, Wang Y, Nilsen SP, Turner JR (2019) Inflammation-induced occludin downregulation limits epithelial apoptosis by suppressing caspase-3 expression. Gastroenterology 157:1323–1337PubMedCrossRef Kuo WT, Shen L, Zuo L, Shashikanth N, Ong M, Wu L, Zha J, Edelblum KL, Wang Y, Wang Y, Nilsen SP, Turner JR (2019) Inflammation-induced occludin downregulation limits epithelial apoptosis by suppressing caspase-3 expression. Gastroenterology 157:1323–1337PubMedCrossRef
Zurück zum Zitat Lazaridis N, Germanidis G (2018) Current insights into the innate immune system dysfunction in irritable bowel syndrome. Ann Gastroenterol 31:171–187PubMedPubMedCentral Lazaridis N, Germanidis G (2018) Current insights into the innate immune system dysfunction in irritable bowel syndrome. Ann Gastroenterol 31:171–187PubMedPubMedCentral
Zurück zum Zitat Lee H, Park JH, Park DI, Kim HJ, Cho YK, Sohn CI, Jeon WK, Kim BI, Chae SW (2013) Mucosal mast cell count is associated with intestinal permeability in patients with diarrhea predominant irritable bowel syndrome. J Neurogastroenterol Motil 19:244–250PubMedPubMedCentralCrossRef Lee H, Park JH, Park DI, Kim HJ, Cho YK, Sohn CI, Jeon WK, Kim BI, Chae SW (2013) Mucosal mast cell count is associated with intestinal permeability in patients with diarrhea predominant irritable bowel syndrome. J Neurogastroenterol Motil 19:244–250PubMedPubMedCentralCrossRef
Zurück zum Zitat Lee JY, Kim N, Park JH, Nam RH, Lee SM, Song CH, Kim G, Na HY, Choi YJ, Kim JJ, Lee DH (2020) Expression of neurotrophic factors, tight junction proteins, and cytokines according to the irritable bowel syndrome subtype and sex. J Neurogastroenterol Motil 26:106–116PubMedPubMedCentralCrossRef Lee JY, Kim N, Park JH, Nam RH, Lee SM, Song CH, Kim G, Na HY, Choi YJ, Kim JJ, Lee DH (2020) Expression of neurotrophic factors, tight junction proteins, and cytokines according to the irritable bowel syndrome subtype and sex. J Neurogastroenterol Motil 26:106–116PubMedPubMedCentralCrossRef
Zurück zum Zitat Liberles SD, Buck LB (2006) A second class of chemosensory receptors in the olfactory epithelium. Nature 442:645–650PubMedCrossRef Liberles SD, Buck LB (2006) A second class of chemosensory receptors in the olfactory epithelium. Nature 442:645–650PubMedCrossRef
Zurück zum Zitat Lindemann L, Hoener MC (2005) A renaissance in trace amines inspired by a novel Gpcr family. Trends Pharmacol Sci 26:274–281PubMedCrossRef Lindemann L, Hoener MC (2005) A renaissance in trace amines inspired by a novel Gpcr family. Trends Pharmacol Sci 26:274–281PubMedCrossRef
Zurück zum Zitat Looijer-Van Langen M, Hotte N, Dieleman LA, Albert E, Mulder C, Madsen KL (2011) Estrogen receptor-beta signaling modulates epithelial barrier function. Am J Physiol Gastrointest Liver Physiol 300:G621–G626PubMedCrossRef Looijer-Van Langen M, Hotte N, Dieleman LA, Albert E, Mulder C, Madsen KL (2011) Estrogen receptor-beta signaling modulates epithelial barrier function. Am J Physiol Gastrointest Liver Physiol 300:G621–G626PubMedCrossRef
Zurück zum Zitat Lorencová E, Buňková L, Matoulková D, Dráb V, Pleva P, Kubáň V, Buňka F (2012) Production of biogenic amines by lactic acid bacteria and bifidobacteria isolated from dairy products and beer. Int J Food Sci Technol 47:2086–2091CrossRef Lorencová E, Buňková L, Matoulková D, Dráb V, Pleva P, Kubáň V, Buňka F (2012) Production of biogenic amines by lactic acid bacteria and bifidobacteria isolated from dairy products and beer. Int J Food Sci Technol 47:2086–2091CrossRef
Zurück zum Zitat Luqman A, Nega M, Nguyen MT, Ebner P, Gotz F (2018) Sada-expressing staphylococci in the human gut show increased cell adherence and internalization. Cell Rep 22:535–545PubMedCrossRef Luqman A, Nega M, Nguyen MT, Ebner P, Gotz F (2018) Sada-expressing staphylococci in the human gut show increased cell adherence and internalization. Cell Rep 22:535–545PubMedCrossRef
Zurück zum Zitat Mahurkar S, Polytarchou C, Iliopoulos D, Pothoulakis C, Mayer EA, Chang L (2016) Genome-wide dna methylation profiling of peripheral blood mononuclear cells in irritable bowel syndrome. Neurogastroenterol Motil 28:410–422PubMedCrossRef Mahurkar S, Polytarchou C, Iliopoulos D, Pothoulakis C, Mayer EA, Chang L (2016) Genome-wide dna methylation profiling of peripheral blood mononuclear cells in irritable bowel syndrome. Neurogastroenterol Motil 28:410–422PubMedCrossRef
Zurück zum Zitat Mayeur C, Veuillet G, Michaud M, Raul F, Blottiere HM, Blachier F (2005) Effects of agmatine accumulation in human colon carcinoma cells on polyamine metabolism, dna synthesis and the cell cycle. Biochim Biophys Acta 1745:111–123PubMedCrossRef Mayeur C, Veuillet G, Michaud M, Raul F, Blottiere HM, Blachier F (2005) Effects of agmatine accumulation in human colon carcinoma cells on polyamine metabolism, dna synthesis and the cell cycle. Biochim Biophys Acta 1745:111–123PubMedCrossRef
Zurück zum Zitat Moracanin SV, Stefanovic S, Radicevic T, Borovic B, Djukic D (2015) Production of biogenic amines by lactic acid bacteria isolated from uzicka sausages. Proc Food Sci 5:308–311CrossRef Moracanin SV, Stefanovic S, Radicevic T, Borovic B, Djukic D (2015) Production of biogenic amines by lactic acid bacteria isolated from uzicka sausages. Proc Food Sci 5:308–311CrossRef
Zurück zum Zitat Mujagic Z, Ludidi S, Keszthelyi D, Hesselink MA, Kruimel JW, Lenaerts K, Hanssen NM, Conchillo JM, Jonkers DM, Masclee AA (2014) Small intestinal permeability is increased in diarrhoea predominant Ibs, while alterations in gastroduodenal permeability In All ibs subtypes are largely attributable to confounders. Aliment Pharmacol Ther 40:288–297PubMedCrossRef Mujagic Z, Ludidi S, Keszthelyi D, Hesselink MA, Kruimel JW, Lenaerts K, Hanssen NM, Conchillo JM, Jonkers DM, Masclee AA (2014) Small intestinal permeability is increased in diarrhoea predominant Ibs, while alterations in gastroduodenal permeability In All ibs subtypes are largely attributable to confounders. Aliment Pharmacol Ther 40:288–297PubMedCrossRef
Zurück zum Zitat Ohman L, Simren M (2010) Pathogenesis of ibs: role of inflammation, immunity and neuroimmune interactions. Nat Rev Gastroenterol Hepatol 7:163–173PubMedCrossRef Ohman L, Simren M (2010) Pathogenesis of ibs: role of inflammation, immunity and neuroimmune interactions. Nat Rev Gastroenterol Hepatol 7:163–173PubMedCrossRef
Zurück zum Zitat Oliphant K, Allen-Vercoe E (2019) Macronutrient metabolism by the human gut microbiome: major fermentation by-products and their impact on host health. Microbiome 7:91PubMedPubMedCentralCrossRef Oliphant K, Allen-Vercoe E (2019) Macronutrient metabolism by the human gut microbiome: major fermentation by-products and their impact on host health. Microbiome 7:91PubMedPubMedCentralCrossRef
Zurück zum Zitat Peerapen P, Thongboonkerd V (2011) Effects of calcium oxalate monohydrate crystals on expression and function of tight junction of renal tubular epithelial cells. Lab Invest 91:97–105PubMedCrossRef Peerapen P, Thongboonkerd V (2011) Effects of calcium oxalate monohydrate crystals on expression and function of tight junction of renal tubular epithelial cells. Lab Invest 91:97–105PubMedCrossRef
Zurück zum Zitat Petecchia L, Sabatini F, Usai C, Caci E, Varesio L, Rossi GA (2012) Cytokines induce tight junction disassembly in airway cells via An Egfr-dependent Mapk/Erk1/2-pathway. Lab Invest 92:1140–1148PubMedCrossRef Petecchia L, Sabatini F, Usai C, Caci E, Varesio L, Rossi GA (2012) Cytokines induce tight junction disassembly in airway cells via An Egfr-dependent Mapk/Erk1/2-pathway. Lab Invest 92:1140–1148PubMedCrossRef
Zurück zum Zitat Piche T (2014) Tight junctions and Ibs-the link between epithelial permeability, low-grade inflammation, and symptom generation? Neurogastroenterol Motil 26:296–302PubMedCrossRef Piche T (2014) Tight junctions and Ibs-the link between epithelial permeability, low-grade inflammation, and symptom generation? Neurogastroenterol Motil 26:296–302PubMedCrossRef
Zurück zum Zitat Piche T, Barbara G, Aubert P, Bruley Des VS, Dainese R, Nano JL, Cremon C, Stanghellini V, De Giorgio R, Galmiche JP, Neunlist M (2009) Impaired intestinal barrier integrity in the colon of patients with irritable bowel syndrome: involvement of soluble mediators. Gut 58:196–201PubMedCrossRef Piche T, Barbara G, Aubert P, Bruley Des VS, Dainese R, Nano JL, Cremon C, Stanghellini V, De Giorgio R, Galmiche JP, Neunlist M (2009) Impaired intestinal barrier integrity in the colon of patients with irritable bowel syndrome: involvement of soluble mediators. Gut 58:196–201PubMedCrossRef
Zurück zum Zitat Price DB, Ackland ML, Burks W, Knight MI, Suphioglu C (2014) Peanut allergens alter intestinal barrier permeability and tight junction localisation in Caco-2 Cell cultures. Cell Physiol Biochem 33:1758–1777PubMedCrossRef Price DB, Ackland ML, Burks W, Knight MI, Suphioglu C (2014) Peanut allergens alter intestinal barrier permeability and tight junction localisation in Caco-2 Cell cultures. Cell Physiol Biochem 33:1758–1777PubMedCrossRef
Zurück zum Zitat Pugin B, Barcik W, Westermann P, Heider A, Wawrzyniak M, Hellings P, Akdis CA (2017) A wide diversity of bacteria from the human gut produces and degrades biogenic amines. Microb Ecol Health Dis 28:1353881PubMedPubMedCentral Pugin B, Barcik W, Westermann P, Heider A, Wawrzyniak M, Hellings P, Akdis CA (2017) A wide diversity of bacteria from the human gut produces and degrades biogenic amines. Microb Ecol Health Dis 28:1353881PubMedPubMedCentral
Zurück zum Zitat Rao JN, Rathor N, Zhuang R, Zou T, Liu L, Xiao L, Turner DJ, Wang JY (2012) Polyamines regulate intestinal epithelial restitution through Trpc1-mediated Ca(2)+ signaling by differentially modulating Stim1 and Stim2. Am J Physiol Cell Physiol 303:C308–C317PubMedPubMedCentralCrossRef Rao JN, Rathor N, Zhuang R, Zou T, Liu L, Xiao L, Turner DJ, Wang JY (2012) Polyamines regulate intestinal epithelial restitution through Trpc1-mediated Ca(2)+ signaling by differentially modulating Stim1 and Stim2. Am J Physiol Cell Physiol 303:C308–C317PubMedPubMedCentralCrossRef
Zurück zum Zitat Roshchina VV (2010) Evolutionary considerations of neurotransmitters in microbial, plant, and animal cells. Microbial Endocrinol Roshchina VV (2010) Evolutionary considerations of neurotransmitters in microbial, plant, and animal cells. Microbial Endocrinol
Zurück zum Zitat Salvemini D, Kim SF, Mollace V (2013) Reciprocal regulation of the nitric oxide and cyclooxygenase pathway in pathophysiology: relevance and clinical implications. Am J Physiol Regul Integr Comp Physiol 304:R473–R487PubMedPubMedCentralCrossRef Salvemini D, Kim SF, Mollace V (2013) Reciprocal regulation of the nitric oxide and cyclooxygenase pathway in pathophysiology: relevance and clinical implications. Am J Physiol Regul Integr Comp Physiol 304:R473–R487PubMedPubMedCentralCrossRef
Zurück zum Zitat Seregi A, Hertting G (1984) Changes in cyclooxygenase activity and prostaglandin profiles during monoamine metabolism in rat bain homogenates. Prostagl Leukot Med 14:113–121CrossRef Seregi A, Hertting G (1984) Changes in cyclooxygenase activity and prostaglandin profiles during monoamine metabolism in rat bain homogenates. Prostagl Leukot Med 14:113–121CrossRef
Zurück zum Zitat Thackray VG (2019) Sex, microbes, and polycystic ovary syndrome. Trends Endocrinol Metab 30:54–65PubMedCrossRef Thackray VG (2019) Sex, microbes, and polycystic ovary syndrome. Trends Endocrinol Metab 30:54–65PubMedCrossRef
Zurück zum Zitat Vannucchi MG, Evangelista S (2018) Experimental models of irritable bowel syndrome and the role of the enteric neurotransmission. J Clin Med 7(1):4PubMedCentralCrossRef Vannucchi MG, Evangelista S (2018) Experimental models of irritable bowel syndrome and the role of the enteric neurotransmission. J Clin Med 7(1):4PubMedCentralCrossRef
Zurück zum Zitat Wilkins T, Pepitone C, Alex B, Schade RR (2012) Diagnosis and management of Ibs in adults. Am Fam Phys 86:419–426 Wilkins T, Pepitone C, Alex B, Schade RR (2012) Diagnosis and management of Ibs in adults. Am Fam Phys 86:419–426
Zurück zum Zitat Williams BB, Van Benschoten AH, Cimermancic P, Donia MS, Zimmermann M, Taketani M, Ishihara A, Kashyap PC, Fraser JS, Fischbach MA (2014) Discovery and characterization of gut microbiota decarboxylases that can produce the neurotransmitter tryptamine. Cell Host Microbe 16:495–503PubMedPubMedCentralCrossRef Williams BB, Van Benschoten AH, Cimermancic P, Donia MS, Zimmermann M, Taketani M, Ishihara A, Kashyap PC, Fraser JS, Fischbach MA (2014) Discovery and characterization of gut microbiota decarboxylases that can produce the neurotransmitter tryptamine. Cell Host Microbe 16:495–503PubMedPubMedCentralCrossRef
Zurück zum Zitat Yano JM, Yu K, Donaldson GP, Shastri GG, Ann P, Ma L, Nagler CR, Ismagilov RF, Mazmanian SK, Hsiao EY (2015) Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis. Cell 161:264–276PubMedPubMedCentralCrossRef Yano JM, Yu K, Donaldson GP, Shastri GG, Ann P, Ma L, Nagler CR, Ismagilov RF, Mazmanian SK, Hsiao EY (2015) Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis. Cell 161:264–276PubMedPubMedCentralCrossRef
Zurück zum Zitat Zeng R, Li X, Gorodeski GI (2004) Estrogen abrogates transcervical tight junctional resistance by acceleration of occludin modulation. J Clin Endocrinol Metab 89:5145–5155PubMedCrossRef Zeng R, Li X, Gorodeski GI (2004) Estrogen abrogates transcervical tight junctional resistance by acceleration of occludin modulation. J Clin Endocrinol Metab 89:5145–5155PubMedCrossRef
Zurück zum Zitat Zhou Z, Zhang L, Ding M, Luo Z, Yuan S, Bansal MB, Gilkeson G, Lang R, Jiang W (2017) Estrogen decreases tight junction protein zo-1 expression in human primary gut tissues. Clin Immunol 183:174–180PubMedPubMedCentralCrossRef Zhou Z, Zhang L, Ding M, Luo Z, Yuan S, Bansal MB, Gilkeson G, Lang R, Jiang W (2017) Estrogen decreases tight junction protein zo-1 expression in human primary gut tissues. Clin Immunol 183:174–180PubMedPubMedCentralCrossRef
Metadaten
Titel
Alterations to microbial secretome by estrogen may contribute to sex bias in irritable bowel syndrome
verfasst von
Lesha Pretorius
Anton du Preez Van Staden
Johannes J. Van der Merwe
Natasha Henning
Carine Smith
Publikationsdatum
13.01.2022
Verlag
Springer International Publishing
Erschienen in
Inflammopharmacology / Ausgabe 1/2022
Print ISSN: 0925-4692
Elektronische ISSN: 1568-5608
DOI
https://doi.org/10.1007/s10787-021-00906-8