Skip to main content
Top
Published in: Inflammation 5/2015

01-10-2015

Sex Differences in Experimentally Induced Colitis in Mice: a Role for Estrogens

Authors: Janka Bábíčková, Ľubomíra Tóthová, Eva Lengyelová, Anastázie Bartoňová, Július Hodosy, Roman Gardlík, Peter Celec

Published in: Inflammation | Issue 5/2015

Login to get access

Abstract

Sex differences have been found in the incidence and progression of inflammatory bowel diseases (IBD) such as ulcerative colitis and Crohn’s disease. The reported differences in observational studies are controversial, and the effects of sex hormones on the pathogenesis of IBD are not clear. The aim of this study was to analyze sex differences in the progression of experimentally induced colitis. Experimental colitis was induced in adult mice by adding 2 % dextran sodium sulfate (DSS) into drinking water. Male and female mice were used as intact, gonadectomized, and supplemented with either estradiol or testosterone. In comparison to males, female mice with induced colitis had significantly longer colon (p < 0.05), lower decrease in body weight (p < 0.001), and lower stool consistency score (p < 0.05). Histopathological analysis showed less inflammatory infiltrates (p < 0.001) and crypt damage (p < 0.001) in female mice. Female mice with colitis had also lower concentration of TNF-α in colon homogenates (p < 0.01). Supplementation with estradiol in ovariectomized mice ameliorated the severity of colitis. Female mice are partially protected against chemically induced colitis. This protection seems to be mediated by estradiol.
Literature
1.
go back to reference Cosnes, J., C. Gower-Rousseau, P. Seksik, and A. Cortot. 2011. Epidemiology and natural history of inflammatory bowel diseases. Gastroenterology 140: 1785–1794.CrossRefPubMed Cosnes, J., C. Gower-Rousseau, P. Seksik, and A. Cortot. 2011. Epidemiology and natural history of inflammatory bowel diseases. Gastroenterology 140: 1785–1794.CrossRefPubMed
2.
go back to reference Molodecky, N.A., I.S. Soon, D.M. Rabi, W.A. Ghali, M. Ferris, G. Chernoff, E.I. Benchimol, R. Panaccione, S. Ghosh, H.W. Barkema, and G.G. Kaplan. 2012. Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology 142: 46–54.CrossRefPubMed Molodecky, N.A., I.S. Soon, D.M. Rabi, W.A. Ghali, M. Ferris, G. Chernoff, E.I. Benchimol, R. Panaccione, S. Ghosh, H.W. Barkema, and G.G. Kaplan. 2012. Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology 142: 46–54.CrossRefPubMed
3.
go back to reference Sartor, R.B. 2006. Mechanisms of disease: pathogenesis of Crohn’s disease and ulcerative colitis. Nat Clin Pract Gastroenterol Hepatol 3: 390–407.CrossRefPubMed Sartor, R.B. 2006. Mechanisms of disease: pathogenesis of Crohn’s disease and ulcerative colitis. Nat Clin Pract Gastroenterol Hepatol 3: 390–407.CrossRefPubMed
4.
go back to reference Herrinton, L.J., L. Liu, J.D. Lewis, P.M. Griffin, and J. Allison. 2008. Incidence and prevalence of inflammatory bowel disease in a Northern California managed care organization, 1996–2002. Am J Gastroenterol 103: 1998–2006.CrossRefPubMed Herrinton, L.J., L. Liu, J.D. Lewis, P.M. Griffin, and J. Allison. 2008. Incidence and prevalence of inflammatory bowel disease in a Northern California managed care organization, 1996–2002. Am J Gastroenterol 103: 1998–2006.CrossRefPubMed
5.
go back to reference Jacobsen, B.A., J. Fallingborg, H.H. Rasmussen, K.R. Nielsen, A.M. Drewes, E. Puho, G.L. Nielsen, and H.T. Sorensen. 2006. Increase in incidence and prevalence of inflammatory bowel disease in northern Denmark: a population-based study, 1978–2002. Eur J Gastroenterol Hepatol 18: 601–606.CrossRefPubMed Jacobsen, B.A., J. Fallingborg, H.H. Rasmussen, K.R. Nielsen, A.M. Drewes, E. Puho, G.L. Nielsen, and H.T. Sorensen. 2006. Increase in incidence and prevalence of inflammatory bowel disease in northern Denmark: a population-based study, 1978–2002. Eur J Gastroenterol Hepatol 18: 601–606.CrossRefPubMed
6.
go back to reference Molinie, F., C. Gower-Rousseau, T. Yzet, V. Merle, B. Grandbastien, R. Marti, E. Lerebours, J.L. Dupas, J.F. Colombel, J.L. Salomez, and A. Cortot. 2004. Opposite evolution in incidence of Crohn’s disease and ulcerative colitis in Northern France (1988–1999). Gut 53: 843–848.PubMedCentralCrossRefPubMed Molinie, F., C. Gower-Rousseau, T. Yzet, V. Merle, B. Grandbastien, R. Marti, E. Lerebours, J.L. Dupas, J.F. Colombel, J.L. Salomez, and A. Cortot. 2004. Opposite evolution in incidence of Crohn’s disease and ulcerative colitis in Northern France (1988–1999). Gut 53: 843–848.PubMedCentralCrossRefPubMed
7.
go back to reference Lok, K.H., H.G. Hung, C.H. Ng, K.K. Li, K.F. Li, and M.L. Szeto. 2007. The epidemiology and clinical characteristics of Crohn’s disease in the Hong Kong Chinese population: experiences from a regional hospital. Hong Kong Med J 13: 436–441.PubMed Lok, K.H., H.G. Hung, C.H. Ng, K.K. Li, K.F. Li, and M.L. Szeto. 2007. The epidemiology and clinical characteristics of Crohn’s disease in the Hong Kong Chinese population: experiences from a regional hospital. Hong Kong Med J 13: 436–441.PubMed
8.
go back to reference Lopez-Serrano, P., J.L. Perez-Calle, E. Carrera-Alonso, T. Perez-Fernandez, G. Rodriguez-Caravaca, D. Boixeda-de-Miguel, and C.M. Fernandez-Rodriguez. 2009. Epidemiologic study on the current incidence of inflammatory bowel disease in Madrid. Rev Esp Enferm Dig 101: 768–772.CrossRefPubMed Lopez-Serrano, P., J.L. Perez-Calle, E. Carrera-Alonso, T. Perez-Fernandez, G. Rodriguez-Caravaca, D. Boixeda-de-Miguel, and C.M. Fernandez-Rodriguez. 2009. Epidemiologic study on the current incidence of inflammatory bowel disease in Madrid. Rev Esp Enferm Dig 101: 768–772.CrossRefPubMed
9.
go back to reference Tsianos, E.V., K.H. Katsanos, D. Christodoulou, I. Dimoliatis, A. Kogevinas, and R.F. Logan. 2003. Northwest Greece inflammatory bowel disease study: continuing low incidence of Crohn’s disease in Northwest Greece. Dig Liver Dis 35: 99–103.CrossRefPubMed Tsianos, E.V., K.H. Katsanos, D. Christodoulou, I. Dimoliatis, A. Kogevinas, and R.F. Logan. 2003. Northwest Greece inflammatory bowel disease study: continuing low incidence of Crohn’s disease in Northwest Greece. Dig Liver Dis 35: 99–103.CrossRefPubMed
10.
go back to reference Wagtmans, M.J., H.W. Verspaget, C. Lamers, and R.A. van Hogezand. 2001. Gender-related differences in the clinical course of Crohn’s disease. Am J Gastroenterol 96: 1541–1546.CrossRefPubMed Wagtmans, M.J., H.W. Verspaget, C. Lamers, and R.A. van Hogezand. 2001. Gender-related differences in the clinical course of Crohn’s disease. Am J Gastroenterol 96: 1541–1546.CrossRefPubMed
11.
go back to reference Blumenstein, I., E. Herrmann, N. Filmann, C. Zosel, W. Tacke, H. Bock, A. Dignass, F. Hartmann, S. Zeuzem, J. Stein, and O. Schroder. 2011. Female patients suffering from inflammatory bowel diseases are treated less frequently with immunosuppressive medication and have a higher disease activity: a subgroup analysis of a large multi-centre, prospective, internet-based study. J Crohns Colitis 5: 203–210.CrossRefPubMed Blumenstein, I., E. Herrmann, N. Filmann, C. Zosel, W. Tacke, H. Bock, A. Dignass, F. Hartmann, S. Zeuzem, J. Stein, and O. Schroder. 2011. Female patients suffering from inflammatory bowel diseases are treated less frequently with immunosuppressive medication and have a higher disease activity: a subgroup analysis of a large multi-centre, prospective, internet-based study. J Crohns Colitis 5: 203–210.CrossRefPubMed
12.
go back to reference Zelinkova, Z., E. Bultman, L. Vogelaar, C. Bouziane, E.J. Kuipers, and C.J. van der Woude. 2012. Sex-dimorphic adverse drug reactions to immune suppressive agents in inflammatory bowel disease. World J Gastroenterol 18: 6967–6973.PubMedCentralCrossRefPubMed Zelinkova, Z., E. Bultman, L. Vogelaar, C. Bouziane, E.J. Kuipers, and C.J. van der Woude. 2012. Sex-dimorphic adverse drug reactions to immune suppressive agents in inflammatory bowel disease. World J Gastroenterol 18: 6967–6973.PubMedCentralCrossRefPubMed
13.
go back to reference Allison, J., L.J. Herrinton, L. Liu, J. Yu, and J. Lowder. 2008. Natural history of severe ulcerative colitis in a community-based health plan. Clin Gastroenterol Hepatol 6: 999–1003.CrossRefPubMed Allison, J., L.J. Herrinton, L. Liu, J. Yu, and J. Lowder. 2008. Natural history of severe ulcerative colitis in a community-based health plan. Clin Gastroenterol Hepatol 6: 999–1003.CrossRefPubMed
14.
15.
go back to reference Hofer, B., T. Bottger, T. Hernandez-Richter, J.K. Seifert, and T. Junginger. 2001. The impact of clinical types of disease manifestation on the risk of early postoperative recurrence in Crohn’s disease. Hepatogastroenterology 48: 152–155.PubMed Hofer, B., T. Bottger, T. Hernandez-Richter, J.K. Seifert, and T. Junginger. 2001. The impact of clinical types of disease manifestation on the risk of early postoperative recurrence in Crohn’s disease. Hepatogastroenterology 48: 152–155.PubMed
16.
go back to reference Jess, T., E.V. Loftus, W.S. Harmsen, A.R. Zinsmeister, W.J. Tremaine, L.J. Melton, P. Munkholm, and W.J. Sandborn. 2006. Survival and cause specific mortality in patients with inflammatory bowel disease: a long term outcome study in Olmsted County, Minnesota, 1940–2004. Gut 55: 1248–1254.PubMedCentralCrossRefPubMed Jess, T., E.V. Loftus, W.S. Harmsen, A.R. Zinsmeister, W.J. Tremaine, L.J. Melton, P. Munkholm, and W.J. Sandborn. 2006. Survival and cause specific mortality in patients with inflammatory bowel disease: a long term outcome study in Olmsted County, Minnesota, 1940–2004. Gut 55: 1248–1254.PubMedCentralCrossRefPubMed
17.
go back to reference Binder, V. 2004. Epidemiology of IBD during the twentieth century: an integrated view. Best Pract Res Clin Gastroenterol 18: 463–479.CrossRefPubMed Binder, V. 2004. Epidemiology of IBD during the twentieth century: an integrated view. Best Pract Res Clin Gastroenterol 18: 463–479.CrossRefPubMed
18.
go back to reference Jess, T., K.V. Winther, P. Munkholm, E. Langholz, and V. Binder. 2002. Mortality and causes of death in Crohn’s disease: follow-up of a population-based cohort in Copenhagen County, Denmark. Gastroenterology 122: 1808–1814.CrossRefPubMed Jess, T., K.V. Winther, P. Munkholm, E. Langholz, and V. Binder. 2002. Mortality and causes of death in Crohn’s disease: follow-up of a population-based cohort in Copenhagen County, Denmark. Gastroenterology 122: 1808–1814.CrossRefPubMed
19.
go back to reference Godet, P.G., G.R. May, and L.R. Sutherland. 1995. Meta-analysis of the role of oral contraceptive agents in inflammatory bowel disease. Gut 37: 668–673.PubMedCentralCrossRefPubMed Godet, P.G., G.R. May, and L.R. Sutherland. 1995. Meta-analysis of the role of oral contraceptive agents in inflammatory bowel disease. Gut 37: 668–673.PubMedCentralCrossRefPubMed
20.
go back to reference Khalili, H., L.M. Higuchi, A.N. Ananthakrishnan, J.M. Richter, D. Feskanich, C.S. Fuchs, and A.T. Chan. 2013. Oral contraceptives, reproductive factors and risk of inflammatory bowel disease. Gut 62: 1153–1159.PubMedCentralCrossRefPubMed Khalili, H., L.M. Higuchi, A.N. Ananthakrishnan, J.M. Richter, D. Feskanich, C.S. Fuchs, and A.T. Chan. 2013. Oral contraceptives, reproductive factors and risk of inflammatory bowel disease. Gut 62: 1153–1159.PubMedCentralCrossRefPubMed
21.
go back to reference Riis, L., I. Vind, P. Politi, F. Wolters, S. Vermeire, E. Tsianos, J. Freitas, I. Mouzas, V.R. Ochoa, C. O’Morain, S. Odes, V. Binder, B. Moum, R. Stockbrugger, E. Langholz, P. Munkholm, and I.B.D. Ec. 2006. Does pregnancy change the disease course? A study in a European cohort of patients with inflammatory bowel disease. Am J Gastroenterol 101: 1539–1545.CrossRefPubMed Riis, L., I. Vind, P. Politi, F. Wolters, S. Vermeire, E. Tsianos, J. Freitas, I. Mouzas, V.R. Ochoa, C. O’Morain, S. Odes, V. Binder, B. Moum, R. Stockbrugger, E. Langholz, P. Munkholm, and I.B.D. Ec. 2006. Does pregnancy change the disease course? A study in a European cohort of patients with inflammatory bowel disease. Am J Gastroenterol 101: 1539–1545.CrossRefPubMed
22.
go back to reference Kane, S.V., and D. Reddy. 2008. Hormonal replacement therapy after menopause is protective of disease activity in women with inflammatory bowel disease. Am J Gastroenterol 103: 1193–1196.CrossRefPubMed Kane, S.V., and D. Reddy. 2008. Hormonal replacement therapy after menopause is protective of disease activity in women with inflammatory bowel disease. Am J Gastroenterol 103: 1193–1196.CrossRefPubMed
23.
go back to reference Ballinger, A.B..., M.O. Savage, and I.R. Sanderson. 2003. Delayed puberty associated with inflammatory bowel disease. Pediatr Res 53: 205–210.CrossRefPubMed Ballinger, A.B..., M.O. Savage, and I.R. Sanderson. 2003. Delayed puberty associated with inflammatory bowel disease. Pediatr Res 53: 205–210.CrossRefPubMed
24.
go back to reference Mason, A., S.C. Wong, P. McGrogan, and S.F. Ahmed. 2011. Effect of testosterone therapy for delayed growth and puberty in boys with inflammatory bowel disease. Horm Res Paediatr 75: 8–13.CrossRefPubMed Mason, A., S.C. Wong, P. McGrogan, and S.F. Ahmed. 2011. Effect of testosterone therapy for delayed growth and puberty in boys with inflammatory bowel disease. Horm Res Paediatr 75: 8–13.CrossRefPubMed
25.
go back to reference Azooz, O.G., M.J. Farthing, M.O. Savage, and A.B... Ballinger. 2001. Delayed puberty and response to testosterone in a rat model of colitis. Am J Physiol Regul Integr Comp Physiol 281: 1483–1491. Azooz, O.G., M.J. Farthing, M.O. Savage, and A.B... Ballinger. 2001. Delayed puberty and response to testosterone in a rat model of colitis. Am J Physiol Regul Integr Comp Physiol 281: 1483–1491.
26.
go back to reference Deboer, M.D., and Y.L. Li. 2011. Puberty is delayed in male mice with dextran sodium sulfate colitis out of proportion to changes in food intake, body weight, and serum levels of leptin. Pediatr Res 69: 34–39.PubMedCentralCrossRefPubMed Deboer, M.D., and Y.L. Li. 2011. Puberty is delayed in male mice with dextran sodium sulfate colitis out of proportion to changes in food intake, body weight, and serum levels of leptin. Pediatr Res 69: 34–39.PubMedCentralCrossRefPubMed
27.
go back to reference Resta-Lenert, S., J. Smitham, and K.E. Barrett. 2005. Epithelial dysfunction associated with the development of colitis in conventionally housed mdr1a−/− mice. Am J Physiol Gastrointest Liver Physiol 289: 153–162.CrossRef Resta-Lenert, S., J. Smitham, and K.E. Barrett. 2005. Epithelial dysfunction associated with the development of colitis in conventionally housed mdr1a−/− mice. Am J Physiol Gastrointest Liver Physiol 289: 153–162.CrossRef
28.
go back to reference Mahler, M., I.J. Bristol, E.H. Leiter, A.E. Workman, E.H. Birkenmeier, C.O. Elson, and J.P. Sundberg. 1998. Differential susceptibility of inbred mouse strains to dextran sulfate sodium-induced colitis. Am J Physiol 274: 544–551. Mahler, M., I.J. Bristol, E.H. Leiter, A.E. Workman, E.H. Birkenmeier, C.O. Elson, and J.P. Sundberg. 1998. Differential susceptibility of inbred mouse strains to dextran sulfate sodium-induced colitis. Am J Physiol 274: 544–551.
29.
go back to reference Verdu, E.F., Y. Deng, P. Bercik, and S.M. Collins. 2002. Modulatory effects of estrogen in two murine models of experimental colitis. Am J Physiol Gastrointest Liver Physiol 283: 27–36.CrossRef Verdu, E.F., Y. Deng, P. Bercik, and S.M. Collins. 2002. Modulatory effects of estrogen in two murine models of experimental colitis. Am J Physiol Gastrointest Liver Physiol 283: 27–36.CrossRef
30.
go back to reference Harnish, D.C., L.M. Albert, Y. Leathurby, A.M. Eckert, A. Ciarletta, M. Kasaian, and J.C. Keith Jr. 2004. Beneficial effects of estrogen treatment in the HLA-B27 transgenic rat model of inflammatory bowel disease. Am J Physiol Gastrointest Liver Physiol 286: 118–125.CrossRef Harnish, D.C., L.M. Albert, Y. Leathurby, A.M. Eckert, A. Ciarletta, M. Kasaian, and J.C. Keith Jr. 2004. Beneficial effects of estrogen treatment in the HLA-B27 transgenic rat model of inflammatory bowel disease. Am J Physiol Gastrointest Liver Physiol 286: 118–125.CrossRef
31.
go back to reference Gunal, O., B.K. Oktar, E. Ozcinar, M. Sungur, S. Arbak, and B. Yegen. 2003. Estradiol treatment ameliorates acetic acid-induced gastric and colonic injuries in rats. Inflammation 27: 351–359.CrossRefPubMed Gunal, O., B.K. Oktar, E. Ozcinar, M. Sungur, S. Arbak, and B. Yegen. 2003. Estradiol treatment ameliorates acetic acid-induced gastric and colonic injuries in rats. Inflammation 27: 351–359.CrossRefPubMed
32.
go back to reference Heijmans, J., M.C. Wielenga, S.L. Rosekrans, J. Roelofs, P. Groothuis, A. Ederveen, E.S. de Jonge-Muller, I. Biemond, J.C. Hardwick, G. D’Haens, D.W. Hommes, V. Muncan, G.R. van den Brink, and J.F. van Lidth de Jeude. 2014. Oestrogens promote tumorigenesis in a mouse model for colitis-associated cancer. Gut 63: 310–316.PubMed Heijmans, J., M.C. Wielenga, S.L. Rosekrans, J. Roelofs, P. Groothuis, A. Ederveen, E.S. de Jonge-Muller, I. Biemond, J.C. Hardwick, G. D’Haens, D.W. Hommes, V. Muncan, G.R. van den Brink, and J.F. van Lidth de Jeude. 2014. Oestrogens promote tumorigenesis in a mouse model for colitis-associated cancer. Gut 63: 310–316.PubMed
33.
go back to reference Cook, L.C., A.E. Hillhouse, M.H. Myles, D.B. Lubahn, E.C. Bryda, J.W. Davis, and C.L. Franklin. 2014. The role of estrogen signaling in a mouse model of inflammatory bowel disease: a Helicobacter hepaticus model. PLoS ONE 9: e94209.PubMedCentralCrossRefPubMed Cook, L.C., A.E. Hillhouse, M.H. Myles, D.B. Lubahn, E.C. Bryda, J.W. Davis, and C.L. Franklin. 2014. The role of estrogen signaling in a mouse model of inflammatory bowel disease: a Helicobacter hepaticus model. PLoS ONE 9: e94209.PubMedCentralCrossRefPubMed
34.
go back to reference Harris, H.A., L.M. Albert, Y. Leathurby, M.S. Malamas, R.E. Mewshaw, C.P. Miller, Y.P. Kharode, J. Marzolf, B.S. Komm, R.C. Winneker, D.E. Frail, R.A. Henderson, Y. Zhu, and J.C. Keith Jr. 2003. Evaluation of an estrogen receptor-beta agonist in animal models of human disease. Endocrinology 144: 4241–4249.CrossRefPubMed Harris, H.A., L.M. Albert, Y. Leathurby, M.S. Malamas, R.E. Mewshaw, C.P. Miller, Y.P. Kharode, J. Marzolf, B.S. Komm, R.C. Winneker, D.E. Frail, R.A. Henderson, Y. Zhu, and J.C. Keith Jr. 2003. Evaluation of an estrogen receptor-beta agonist in animal models of human disease. Endocrinology 144: 4241–4249.CrossRefPubMed
35.
go back to reference Palffy, R., R. Gardlik, M. Behuliak, P. Jani, D. Balakova, L. Kadasi, J. Turna, and P. Celec. 2011. Salmonella-mediated gene therapy in experimental colitis in mice. Exp Biol Med (Maywood) 236: 177–183.CrossRef Palffy, R., R. Gardlik, M. Behuliak, P. Jani, D. Balakova, L. Kadasi, J. Turna, and P. Celec. 2011. Salmonella-mediated gene therapy in experimental colitis in mice. Exp Biol Med (Maywood) 236: 177–183.CrossRef
36.
go back to reference Dieleman LA, Palmen M, Akol H, Bloemena E, Pena AS, Meuwissen SGM, and van Rees EP Chronic experimental colitis induced by dextran sulphate sodium (DSS) is characterized by Th1 and Th2 cytokines. Clin Exp Immunol 114: 385–391 Dieleman LA, Palmen M, Akol H, Bloemena E, Pena AS, Meuwissen SGM, and van Rees EP Chronic experimental colitis induced by dextran sulphate sodium (DSS) is characterized by Th1 and Th2 cytokines. Clin Exp Immunol 114: 385–391
37.
go back to reference Kim, J.J., M.S. Shajib, M.M. Manocha, and W.I. Khan. 2012. Investigating intestinal inflammation in DSS-induced model of IBD. J Vis Exp 60: e3678. Kim, J.J., M.S. Shajib, M.M. Manocha, and W.I. Khan. 2012. Investigating intestinal inflammation in DSS-induced model of IBD. J Vis Exp 60: e3678.
38.
go back to reference Ambrosini, R., A. Barchiesi, V. Di Mizio, M. Di Terlizzi, L. Leo, A. Filippone, L. Canalis, R. Fossaceca, and A. Carriero. 2007. Inflammatory chronic disease of the colon: how to image. Eur J Radiol 61: 442–448.CrossRefPubMed Ambrosini, R., A. Barchiesi, V. Di Mizio, M. Di Terlizzi, L. Leo, A. Filippone, L. Canalis, R. Fossaceca, and A. Carriero. 2007. Inflammatory chronic disease of the colon: how to image. Eur J Radiol 61: 442–448.CrossRefPubMed
39.
go back to reference Saleiro D, Murillo G, Benya RV, Bissonnette M, Hart J and Mehta RG Estrogen receptor-ss protects against colitis-associated neoplasia in mice. Int J Cancer 131: 2553–2561 Saleiro D, Murillo G, Benya RV, Bissonnette M, Hart J and Mehta RG Estrogen receptor-ss protects against colitis-associated neoplasia in mice. Int J Cancer 131: 2553–2561
40.
go back to reference Geerling, B.J., W.D.V. Lichtenbelt, R.W. Stockbrugger, and R.J.M. Brummer. 1999. Gender specific alterations of body composition in patients with inflammatory bowel disease compared with controls. Eur J Clin Nutr 53: 479–485.CrossRefPubMed Geerling, B.J., W.D.V. Lichtenbelt, R.W. Stockbrugger, and R.J.M. Brummer. 1999. Gender specific alterations of body composition in patients with inflammatory bowel disease compared with controls. Eur J Clin Nutr 53: 479–485.CrossRefPubMed
41.
go back to reference Jahnsen, J., J.A. Falch, P. Mowinckel, and E. Aadland. 2003. Body composition in patients with inflammatory bowel disease: a population-based study. Am J Gastroenterol 98: 1556–1562.CrossRefPubMed Jahnsen, J., J.A. Falch, P. Mowinckel, and E. Aadland. 2003. Body composition in patients with inflammatory bowel disease: a population-based study. Am J Gastroenterol 98: 1556–1562.CrossRefPubMed
42.
go back to reference Oh, J.E., Y.W. Kim, S.Y. Park, and J.Y. Kim. 2013. Estrogen rather than progesterone cause constipation in both female and male mice. Korean J Physiol Pharmacol 17: 423–426.PubMedCentralCrossRefPubMed Oh, J.E., Y.W. Kim, S.Y. Park, and J.Y. Kim. 2013. Estrogen rather than progesterone cause constipation in both female and male mice. Korean J Physiol Pharmacol 17: 423–426.PubMedCentralCrossRefPubMed
43.
go back to reference Looijer-van Langen, M., N. Hotte, L.A. Dieleman, E. Albert, C. Mulder, and K.L. Madsen. 2011. Estrogen receptor-beta signaling modulates epithelial barrier function. Am J Physiol Gastrointest Liver Physiol 300: 621–626.CrossRef Looijer-van Langen, M., N. Hotte, L.A. Dieleman, E. Albert, C. Mulder, and K.L. Madsen. 2011. Estrogen receptor-beta signaling modulates epithelial barrier function. Am J Physiol Gastrointest Liver Physiol 300: 621–626.CrossRef
44.
Metadata
Title
Sex Differences in Experimentally Induced Colitis in Mice: a Role for Estrogens
Authors
Janka Bábíčková
Ľubomíra Tóthová
Eva Lengyelová
Anastázie Bartoňová
Július Hodosy
Roman Gardlík
Peter Celec
Publication date
01-10-2015
Publisher
Springer US
Published in
Inflammation / Issue 5/2015
Print ISSN: 0360-3997
Electronic ISSN: 1573-2576
DOI
https://doi.org/10.1007/s10753-015-0180-7

Other articles of this Issue 5/2015

Inflammation 5/2015 Go to the issue