The role of estrogen signaling in a mouse model of inflammatory bowel disease: A helicobacter hepaticus model

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Cook, Lydia C ^a   Hillhouse, Andrew E ^a,b,d   Myles, Matthew H ^a,c   Lubahn, Dennis B ^b   Bryda, Elizabeth C ^a   Davis, J Wade ^a   Franklin, Craig L ^a  

^a UNIVERSITY OF MISSOURI   (United States)

^b University of Missouri   (United States)

^c IDEXX LABORATORIES   (United States)

^d TEXAS A M COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,3,5 TRIS(4 HYDROXYPHENYL) 4 PROPYLPYRAZOLE; BUPRENORPHINE; CXCL9 CHEMOKINE; DIARYLPROPIONITRILE; ESTRADIOL; ESTROGEN; INTERLEUKIN 10; INTERLEUKIN 12P40; INTERLEUKIN 17; INTERLEUKIN 17F; INTERLEUKIN 23P19; INTERLEUKIN 4; PLACEBO; SEX HORMONE; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIUM CULTURE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE COURSE; DISEASE SEVERITY; FEMALE; HELICOBACTER HEPATICUS; HISTOPATHOLOGY; INFLAMMATORY BOWEL DISEASE; INTESTINE FLORA; MOUSE; NONHUMAN; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; ANIMAL; DEFICIENCY; DISEASE MODEL; GENE INACTIVATION; GENETICS; HELICOBACTER; METABOLISM; MICROBIOLOGY; PATHOLOGY; PHYSIOLOGY;

ANIMALS; DISEASE MODELS, ANIMAL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; ESTROGENS; FEMALE; GENE KNOCKOUT TECHNIQUES; HELICOBACTER; INFLAMMATORY BOWEL DISEASES; MICE; SIGNAL TRANSDUCTION;

EID: 84899414826     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0094209     Document Type: Article

References (50)

1. Xavier RJ, Podolsky DK (2007) Unravelling the pathogenesis of inflammatory bowel disease. Nature 448: 427-434. (Pubitemid 47123518)
2. Bousvaros A, Sylvester F, Kugathasan S, Szigethy E, Fiocchi C, et al. (2006) Challenges in pediatric inflammatory bowel disease. Inflamm Bowel Dis 12: 885-913. (Pubitemid 44352716)
3. Kuiper GG, Carlsson B, Grandien K, Enmark E, Haggblad J, et al. (1997) Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology 138: 863-870. (Pubitemid 27089735)
4. Whitacre CC (2001) Sex differences in autoimmune disease. Nat Immunol 2: 777-780.
5. McCarthy M (2000) The "gender gap" in autoimmune disease. Lancet 356: 1088.
6. Gleicher N, Barad DH (2007) Gender as risk factor for autoimmune diseases. J Autoimmun 28: 1-6. (Pubitemid 46274179)
7. Beagley KW, Gockel CM (2003) Regulation of innate and adaptive immunity by the female sex hormones oestradiol and progesterone. FEMS Immunol Med Microbiol 38: 13-22. (Pubitemid 37297438)
8. Campbell-Thompson M, Lynch IJ, Bhardwaj B (2001) Expression of estrogen receptor (ER) subtypes and ERbeta isoforms in colon cancer. Cancer Res 61: 632-640. (Pubitemid 32128626)
9. Williams JJ, Kaplan GG, Makhija S, Urbanski SJ, Dupre M, et al. (2008) Microscopic colitis-defining incidence rates and risk factors: a population-based study. Clin Gastroenterol Hepatol 6: 35-40. (Pubitemid 350309538)
10. Kao KT, Pedraza BA, McClune AC, Rios DA, Mao YQ, et al. (2009) Microscopic colitis: a large retrospective analysis from a health maintenance organization experience. World J Gastroenterol 15: 3122-3127.
11. Godet PG, May GR, Sutherland LR (1995) Meta-analysis of the role of oral contraceptive agents in inflammatory bowel disease. Gut 37: 668-673.
12. Khalili H, Higuchi LM, Ananthakrishnan AN, Richter JM, Feskanich D, et al. (2012) Oral contraceptives, reproductive factors and risk of inflammatory bowel disease. Gut.
13. Cornish JA, Tan E, Simillis C, Clark SK, Teare J, et al. (2008) The risk of oral contraceptives in the etiology of inflammatory bowel disease: a meta-analysis. Am J Gastroenterol 103: 2394-2400.
14. Villafruela Cives M (2009) Re: "The risk of oral contraceptives in the etiology of inflammatory bowel disease: a meta-analysis". Response to Cornish, et al. Am J Gastroenterol 104: 534-535.
15. Riis L, Vind I, Politi P, Wolters F, Vermeire S, et al. (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. (Pubitemid 43982551)
16. Kane SV, Reddy D (2008) Hormonal replacement therapy after menopause is protective of disease activity in women with inflammatory bowel disease. Am J Gastroenterol 103: 1193-1196. (Pubitemid 351677960)
17. Harnish DC, Albert LM, Leathurby Y, Eckert AM, Ciarletta A, et al. (2004) Beneficial effects of estrogen treatment in the HLA-B27 transgenic rat model of inflammatory bowel disease. Am J Physiol Gastrointest Liver Physiol 286: G118-125. (Pubitemid 38055845)
18. Harris HA, Albert LM, Leathurby Y, Malamas MS, Mewshaw RE, et al. (2003) Evaluation of an estrogen receptor-beta agonist in animal models of human disease. Endocrinology 144: 4241-4249. (Pubitemid 37204818)
19. Chadwick CC, Chippari S, Matelan E, Borges-Marcucci L, Eckert AM, et al. (2005) Identification of pathway-selective estrogen receptor ligands that inhibit NF-kappaB transcriptional activity. Proc Natl Acad Sci U S A 102: 2543-2548. (Pubitemid 40279413)
20. Mewshaw RE, Edsall RJ, Jr., Yang C, Manas ES, Xu ZB, et al. (2005) ERbeta ligands. 3. Exploiting two binding orientations of the 2-phenylnaphthalene scaffold to achieve ERbeta selectivity. J Med Chem 48: 3953-3979. (Pubitemid 40800606)
21. Verdu EF, Deng Y, Bercik P, Collins SM (2002) Modulatory effects of estrogen in two murine models of experimental colitis. Am J Physiol Gastrointest Liver Physiol 283: G27-36. (Pubitemid 34666159)
22. Gunal O, Oktar BK, Ozcinar E, Sungur M, Arbak S, et al. (2003) Estradiol treatment ameliorates acetic acid-induced gastric and colonic injuries in rats. Inflammation 27: 351-359. (Pubitemid 38028617)
23. Saleiro D, Murillo G, Benya RV, Bissonnette M, Hart J, et al. (2012) Estrogen receptor-beta protects against colitis-associated neoplasia in mice. Int J Cancer 131: 2553-2561.
24. Myles MH, Dieckgraefe BK, Criley JM, Franklin CL (2007) Characterization of cecal gene expression in a differentially susceptible mouse model of bacterial-induced inflammatory bowel disease. Inflamm Bowel Dis 13: 822-836. (Pubitemid 47203860)
25. Maggio-Price L, Bielefeldt-Ohmann H, Treuting P, Iritani BM, Zeng W, et al. (2005) Dual infection with Helicobacter bilis and Helicobacter hepaticus in p-glycoprotein-deficient mdr1a-/- mice results in colitis that progresses to dysplasia. Am J Pathol 166: 1793-1806. (Pubitemid 40734402)
26. Maggio-Price L, Shows D, Waggie K, Burich A, Zeng W, et al. (2002) Helicobacter bilis infection accelerates and H. hepaticus infection delays the development of colitis in multiple drug resistance-deficient (mdr1a-/-) mice. American Journal of Pathology 160: 739-751. (Pubitemid 34160352)
27. Maggio-Price L, Treuting P, Zeng W, Tsang M, Bielefeldt-Ohmann H, et al. (2006) Helicobacter infection is required for inflammation and colon cancer in SMAD3-deficient mice. Cancer Res 66: 828-838. (Pubitemid 43165948)
28. Cahill RJ, Foltz CJ, Fox JG, Dangler CA, Powrie F, et al. (1997) Inflammatory bowel disease: an immunity-mediated condition triggered by bacterial infection with Helicobacter hepaticus. Infection & Immunity 65: 3126-3131. (Pubitemid 27342388)
29. Livingston RS, Myles MH, Livingston BA, Criley JM, Franklin CL (2004) Sex influence on chronic intestinal inflammation in Helicobacter hepaticus-infected A/JCr mice. Comp Med 54: 301-308. (Pubitemid 38856991)
30. Whary MT, Morgan TJ, Dangler CA, Gaudes KJ, Taylor NS, et al. (1998) Chronic active hepatitis induced by Helicobacter hepaticus in the A/JCr mouse is associated with a Th1 cell-mediated immune response. Infect Immun 66: 3142-3148. (Pubitemid 28303109)
31. Myles MH, Livingston RS, Livingston BA, Criley JM, Franklin CL (2003) Analysis of gene expression in ceca of Helicobacter hepaticus-infected A/JCr mice before and after development of typhlitis. Infect Immun 71: 3885-3893. (Pubitemid 36753711)
32. Lubahn DB, Moyer JS, Golding TS, Couse JF, Korach KS, et al. (1993) Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc Natl Acad Sci U S A 90: 11162-11166. (Pubitemid 23354389)
33. Krege JH, Hodgin JB, Couse JF, Enmark E, Warner M, et al. (1998) Generation and reproductive phenotypes of mice lacking estrogen receptor beta. Proc Natl Acad Sci U S A 95: 15677-15682. (Pubitemid 29018759)
34. Riley LK, Franklin CL, Hook RR, Jr., Besch-Williford C (1996) Identification of murine helicobacters by PCR and restriction enzyme analyses. J Clin Microbiol 34: 942-946. (Pubitemid 26091512)
35. Mohammadi M, Redline R, Nedrud J, Czinn S (1996) Role of the host in pathogenesis of Helicobacter-associated gastritis: H. felis infection of inbred and congenic mouse strains. Infect Immun 64: 238-245. (Pubitemid 26009879)
36. Dunn OJ (1964) Multiple comparisons using rank sums. Technometrics 6: 241-252.
37. Jansson L, Holmdahl R (1998) Estrogen-mediated immunosuppression in autoimmune diseases. Inflamm Res 47: 290-301. (Pubitemid 28379309)
38. Bebo BF, Jr., Fyfe-Johnson A, Adlard K, Beam AG, Vandenbark AA, et al. (2001) Low-dose estrogen therapy ameliorates experimental autoimmune encephalomyelitis in two different inbred mouse strains. J Immunol 166: 2080-2089. (Pubitemid 32114698)
39. Subramanian S, Matejuk A, Zamora A, Vandenbark AA, Offner H (2003) Oral feeding with ethinyl estradiol suppresses and treats experimental autoimmune encephalomyelitis in SJL mice and inhibits the recruitment of inflammatory cells into the central nervous system. J Immunol 170: 1548-1555. (Pubitemid 36139527)
40. Liu HY, Buenafe AC, Matejuk A, Ito A, Zamora A, et al. (2002) Estrogen inhibition of EAE involves effects on dendritic cell function. J Neurosci Res 70: 238-248.
41. Subramanian S, Tovey M, Afentoulis M, Krogstad A, Vandenbark AA, et al. (2005) Ethinyl estradiol treats collagen-induced arthritis in DBA/1LacJ mice by inhibiting the production of TNF-alpha and IL-1beta. Clin Immunol 115: 162-172. (Pubitemid 40693086)
42. Brant SR, Nguyen GC (2008) Is there a gender difference in the prevalence of Crohn's disease or ulcerative colitis? Inflamm Bowel Dis 14 Suppl 2: S2-3.
43. Ferguson CB, Mahsud-Dornan S, Patterson RN (2008) Inflammatory bowel disease in pregnancy. BMJ 337: a427.
44. Looijer-van Langen M, Hotte N, Dieleman LA, Albert E, Mulder C, et al. (2011) Estrogen receptor-beta signaling modulates epithelial barrier function. Am J Physiol Gastrointest Liver Physiol 300: G621-626.
45. Wada-Hiraike O, Imamov O, Hiraike H, Hultenby K, Schwend T, et al. (2006) Role of estrogen receptor beta in colonic epithelium. Proc Natl Acad Sci U S A 103: 2959-2964.
46. Wada-Hiraike O, Warner M, Gustafsson JA (2006) New developments in oestrogen signalling in colonic epithelium. Biochem Soc Trans 34: 1114-1116. (Pubitemid 46772912)
47. Phiel KL, Henderson RA, Adelman SJ, Elloso MM (2005) Differential estrogen receptor gene expression in human peripheral blood mononuclear cell populations. Immunol Lett 97: 107-113. (Pubitemid 40038861)
48. Mao A, Paharkova-Vatchkova V, Hardy J, Miller MM, Kovats S (2005) Estrogen selectively promotes the differentiation of dendritic cells with characteristics of Langerhans cells. J Immunol 175: 5146-5151. (Pubitemid 41456398)
49. Nalbandian G, Kovats S (2005) Understanding sex biases in immunity: effects of estrogen on the differentiation and function of antigen-presenting cells. Immunol Res 31: 91-106. (Pubitemid 40631381)
50. Siracusa MC, Overstreet MG, Housseau F, Scott AL, Klein SL (2008) 17beta-estradiol alters the activity of conventional and IFN-producing killer dendritic cells. J Immunol 180: 1423-1431.