Sex Steroid Regulation of Macrophage Migration Inhibitory Factor in Normal and Inflamed Colon in the Female Rat

Gastroenterology

Volumn 132, Issue 3, 2007, Pages 982-993

  Houdeau, Eric ^a   Moriez, Raphael ^a   Leveque, Mathilde ^a   Salvador Cartier, Christel ^a   Waget, Aurelie ^a   Leng, Lin ^b   Bueno, Lionel ^a   Bucala, Richard ^b   Fioramonti, Jean ^a  

^a CEMAGREF   (France)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CORTICOSTERONE; CORTODOXONE; CYTOKINE; DEXTRAN SULFATE; ESTRADIOL; ESTRADIOL BENZOATE; INTERLEUKIN 1BETA; MACROPHAGE MIGRATION INHIBITION FACTOR; MYELOPEROXIDASE; PROGESTERONE; SEX HORMONE; TRINITROBENZENESULFONIC ACID; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COLITIS; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; CYTOKINE PRODUCTION; DISEASE PREDISPOSITION; ENZYME ACTIVITY; ESTRUS CYCLE; FEMALE; HORMONE SUBSTITUTION; IMMUNOHISTOCHEMISTRY; METESTRUS; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM; UPREGULATION;

EID: 33947310770     PISSN: 00165085     EISSN: None     Source Type: Journal    
DOI: 10.1053/j.gastro.2006.12.028     Document Type: Article

References (61)

1. Weber A.M., Ziegler C., Belinson J.L., Mitchinson A.R., Widrich T., and Fazio V. Gynecologic history of women with inflammatory bowel disease. Obstet Gynecol 86 (1995) 843-847
2. Kane S.V., Sable K., and Hanauer S.B. The menstrual cycle and its effect on inflammatory bowel disease and irritable bowel syndrome: a prevalence study. Am J Gastroenterol 93 (1998) 1867-1872
3. Maunder R., Toner B., de Rooy E., and Moskovitz D. Influence of sex and disease on illness-related concerns in inflammatory bowel disease. Can J Gastroenterol 13 (1999) 728-732
4. Bernklev T., Jahnsen J., Aadland E., Sauar J., Schulz T., Lygren I., Henriksen M., Stray N., Kjellevold O., Vatn M., and Moum B. Health-related quality of life in patients with inflammatory bowel disease five years after the initial diagnosis. Scand J Gastroenterol 39 (2004) 365-373
5. Bernstein C.N., Wajda A., Svenson L.W., MacKenzie A., Koehoorn M., Jackson M., Fedorak R., Israel D., and Blanchard J.F. The epidemiology of inflammatory bowel disease in Canada: a population-based study. Am J Gastroenterol 101 (2006) 1559-1568
6. Gurbuz A.K., Gurbuz B., Salas L., Rosenshein N.B., Donowitz M., and Giardiello F.M. Premarin-induced ischemic colitis. J Clin Gastroenterol 19 (1994) 108-111
7. Garcia Rodriguez L.A., Gonzalez-Perez A., Johansson S., and Wallander M.A. Risk factors for inflammatory bowel disease in the general population. Aliment Pharmacol Ther 22 (2005) 309-315
8. Gunal O., Oktar B.K., Ozcinar E., Sungur M., Arbak S., and Yegen B. Estradiol treatment ameliorates acetic acid-induced gastric and colonic injuries in rats. Inflammation 27 (2003) 351-359
9. Harnish D.C., Albert L.M., Leathurby Y., Eckert A.M., Ciarletta A., Kasaian M., and Keith J.C. Beneficial effects of estrogen treatment in the HLA-B27 transgenic rat model of inflammatory bowel disease. Am J Physiol Gastrointest Liver Physiol 286 (2004) 118-125
10. Verdu E.F., Deng Y., Bercik P., and Collins S.M. Modulatory effects of estrogen in two murine models of experimental colitis. Am J Physiol Gastrointest Liver Physiol 283 (2002) G27-G36
11. Smith M.S., Freeman M.E., and Neill J.D. The control of progesterone secretion during the estrous cycle and early pseudopregnancy in the rat: prolactin, gonadotropin and steroid levels associated with rescue of the corpus luteum of pseudopregnancy. Endocrinology 96 (1975) 219-226
12. Faas M.M., Bakker W.W., Valkhof N., van der Horst M.C., and Schuiling G.A. Reproductive condition and the low-dose endotoxin-induced inflammatory response in rats. Glomerular influx of inflammatory cells and expression of adhesion molecules. Biol Reprod 56 (1997) 1400-1406
13. Hellings P.W., Vandekerckhove P., Claeys R., Billen J., Kasran A., and Ceuppens J.L. Progesterone increases airway eosinophilia and hyper-responsiveness in a murine model of allergic asthma. Clin Exp Allergy 33 (2003) 1457-1463
14. Jain S.K., Kannan K., Prouty L., and Jain S.K. Progesterone, but not 17β-estradiol, increases TNF-α secretion in U937 monocytes. Cytokine 26 (2004) 102-105
15. Gillgrass A.E., Fernandez S.A., Rosenthal K.L., and Kaushic C. Estradiol regulates susceptibility following primary exposure to genital herpes simplex virus type 2, while progesterone induces inflammation. J Virol 79 (2005) 3107-3116
16. Maaser C., Eckmann L., Paesold G., Kim H.S., and Kagnoff M.F. Ubiquitous distribution of macrophage migration inhibitory factor by human gastric and intestinal epithelium. Gastroenterology 122 (2002) 667-680
17. Calandra T., and Roger T. Macrophage migration inhibitory factor: a regulator of innate immunity. Nat Rev Immunol 3 (2003) 791-800
18. de Jong Y.P., Abadia-Molina A.C., Satoskar A.R., Clarke K., Rietdijk S.T., Faubion W.A., Mizoguchi E., Metz C.N., Al Sahli M., ten Hove T., Keates A.C., Lubetsky J.B., Farrell R.J., Michetti P., van Deventer S.J., Lolis E., David J.R., Bhan A.K., and Terhorst C. Development of chronic colitis is dependent on the cytokine MIF. Nat Immunol 2 (2001) 1061-1066
19. Murakami H., Akbar S.M.F., Matsui H., and Onji M. Macrophage migration inhibitory factor in the sera and at the colonic mucosa in patients with ulcerative colitis: clinical implications and pathogenic significance. Eur J Clin Invest 31 (2001) 337-343
20. Murakami H., Akbar S.M.F., Matsui H., Horiike N., and Onji M. Macrophage migration inhibitory factor activates antigen-presenting dendritic cells and induces inflammatory cytokines in ulcerative colitis. Clin Exp Immunol 128 (2002) 504-510
21. Ohkawara T., Nishihira J., Takeda H., Hige S., Kato M., Sugiyama T., Iwagana T., Nakamura H., Mizue Y., and Asaka M. Amelioration of dextran sulfate sodium-induced colitis by anti-macrophage migration inhibitory factor antibody in mice. Gastroenterology 123 (2002) 256-270
22. Ohkawara T., Miyashita K., Nishihira J., Mitsuyama K., Takeda H., Kato M., Kondo N., Yamasaki Y., Sata M., Yoshiki T., Sugiyama T., and Asaka M. Transgenic over-expression of macrophage migration inhibitory factor renders mice markedly more susceptible to experimental colitis. Clin Exp Immunol 140 (2005) 241-248
23. Calandra T., Bernhagen J., Mitchell R.A., and Bucala R. The macrophage is an important and previously unrecognized source of macrophage migration inhibitory factor. J Exp Med 78 (1994) 1895-1902
24. Bouman A., Moes H., Heineman M.J., de Leij L.F., and Faas M.M. The immune response during the luteal phase of the ovarian cycle: increasing sensitivity of human monocytes to endotoxin. Fertil Steril 76 (2001) 555-559
25. He J., Evans C.O., Hoffman S.W., Oyesiku N.M., and Stein D.G. Progesterone and allopregnanolone reduce inflammatory cytokines after traumatic brain injury. Exp Neurol 189 (2004) 404-412
26. Speyer C.L., Rancilio N.J., McClintock S.D., Crawford J.D., Gao H., Sarma J.V., and Ward P.A. Regulatory effects of estrogen on acute lung inflammation in mice. Am J Physiol Cell Physiol 288 (2005) C881-C890
27. Ashcroft G.S., Mills S.J., Lei K., Gibbons L., Jeong M.J., Taniguchi M., Burow M., Horan M.A., Wahl S.M., and Nakayama T. Estrogen modulates cutaneous wound healing by downregulating macrophage migration inhibitory factor. J Clin Invest 111 (2003) 1309-1318
28. Hardman M.J., Waite A., Zeef L., Burow M., Nakayama T., and Ashcroft G.S. Macrophage migration inhibitory factor: a central regulator of wound healing. Am J Pathol 167 (2005) 1561-1574
29. Makita H., Nishimura M., Miyamoto K., Nakano T., Tanino Y., Hirokawa J., Nishihira J., and Kawakami Y. Effect of anti-macrophage migration inhibitory factor antibody on lipopolysaccharide-induced pulmonary neutrophil accumulation. Am J Respir Crit Care Med 158 (1998) 573-579
30. Houdeau E., Larauche M., Monnerie R., Bueno L., and Fioramonti J. Uterine motor alterations and estrous cycle disturbances associated with colonic inflammation in the rat. Am J Physiol Regul Integr Comp Physiol 288 (2005) R630-R637
31. Krawisz J.E., Sharon P., and Stenson W.F. Quantitative assay for acute intestinal inflammation based on myeloperoxidase activity. Assessment of inflammation in rat and hamster models. Gastroenterology 87 (1984) 1344-1350
32. Appleyard C.B., and Wallace J.L. Reactivation of hapten-induced colitis and its prevention by anti-inflammatory drugs. Am J Physiol 269 (1995) G119-G125
33. Vongher J.M., and Frye C.A. Progesterone in conjunction with estradiol has neuroprotective effects in an animal model of neurodegeneration. Pharmacol Biochem Behav 64 (1999) 777-785
34. Mazelin L., Theodorou V., Fioramonti J., and Bueno L. Vagally dependent protective action of calcitonin gene-related peptide on colitis. Peptides 20 (1999) 1367-1374
35. Improta G., Carpino F., Petrozza V., Guglietta A., Tabacco A., and Broccardo M. Central effects of selective NK1 and NK3 tachykinin receptor agonists on two models of experimentally-induced colitis in rats. Peptides 24 (2003) 903-911
36. Kats R., Al-Akoum M., Guay S., Metz C., and Akoum A. Cycle-dependent expression of macrophage migration inhibitory factor in the human endometrium. Hum Reprod 20 (2005) 3518-3525
37. Mazlam M.Z., and Hodgson H.J. Peripheral blood monocyte cytokine production and acute phase response in inflammatory bowel disease. Gut 33 (1992) 773-778
38. McAlindon M.E., Hawkey C.J., and Mahida Y.R. Expression of interleukin 1 beta and interleukin 1 beta converting enzyme by intestinal macrophages in health and inflammatory bowel disease. Gut 42 (1998) 214-219
39. Rojas-Cartagena C., Flores I., and Appleyard C.B. Role of tumor necrosis factor receptors in an animal model of acute colitis. Cytokine 32 (2005) 85-93
40. Aloisi A.M., Pari G., Ceccarelli I., Vecchi I., Ietta F., Lodi L., and Paulesu L. Gender-related effects of chronic non-malignant pain and opioid therapy on plasma levels of macrophage migration inhibitory factor (MIF). Pain 115 (2005) 142-151
41. Vera P.L., and Meyer-Siegler K.L. Anatomical location of macrophage migration inhibitory factor in urogenital tissues, peripheral ganglia and lumbosacral spinal cord of the rat. BMC Neurosci 4 (2003) 17-26
42. Chalimoniuk M., King-Pospisil K., Metz C.N., and Toborek M. Macrophage migration inhibitory factor induces cell death and decreases neuronal nitric oxide expression in spinal cord neurons. Neuroscience 139 (2006) 1117-1128
43. Konstantinopoulos P.A., Kominea A., Vandoros G., Sykiotis G.P., Andricopoulos P., Varakis I., Sotiropoulou-Bonikou G., and Papavassiliou A.G. Oestrogen receptor beta (ERbeta) is abundantly expressed in normal colonic mucosa, but declines in colon adenocarcinoma paralleling the tumour's dedifferentiation. Eur J Cancer 39 (2003) 1251-1258
44. Oshima C.T., Wonraht D.R., Catarino R.M., Mattos D., and Forones N.M. Estrogen and progesterone receptors in gastric and colorectal cancer. Hepatogastroenterology 46 (1999) 3155-3158
45. Wada-Hiraike O., Imamov O., Hiraike H., Hultenby K., Schwend T., Omoto Y., Warner M., and Gustafsson J.A. Role of estrogen receptor beta in colonic epithelium. Proc Natl Acad Sci U S A 103 (2006) 2959-2964
46. Wilson J.M., Coletta P.L., Cuthbert R.J., Scott N., MacLennan K., Hawcroft G., Leng L., Lubetsky J.B., Jin K.K., Lolis E., Medina F., Brieva J.A., Poulsom R., Markham A.F., Bucala R., and Hull M.A. Macrophage migration inhibitory factor promotes intestinal tumorigenesis. Gastroenterology 129 (2005) 1485-1503
47. Nanda K., Bastian L.A., Hasselblad V., and Simel D.L. Hormone replacement therapy and the risk of colorectal cancer: a meta-analysis. Obstet Gynecol 93 (1999) 880-888
48. Salzman A.L., Linn S.C., and Szabo C. Progesterone inhibits inducible nitric oxide synthase mRNA expression in human intestinal epithelial cells. Int J Mol Med 6 (2000) 209-216
49. Khan K.N., Masuzaki H., Fujishita A., Kitajima M., Sekine I., Matsuyama T., and Ishimaru T. Estrogen and progesterone receptor expression in macrophages and regulation of hepatocyte growth factor by ovarian steroids in women with endometriosis. Hum Reprod 20 (2005) 2004-2013
50. Mahida Y.R. The key role of macrophages in the immunopathogenesis of inflammatory bowel disease. Inflamm Bowel Dis 6 (2000) 21-33
51. Arai Y., Takanashi H., Kitagawa H., and Okayasu I. Involvement of interleukin-1 in the development of ulcerative colitis induced by dextran sulfate sodium in mice. Cytokine 10 (1998) 890-896
52. Schreiber S., Nikolaus S., Hampe J., Hamling J., Koop I., Groessner B., Lochs H., and Raedler A. Tumor necrosis factor α and interleukin 1β in relapse of Crohn's disease. Lancet 353 (1999) 459-461
53. Cominelli F., Nast C.C., Clark B.D., Schindler R., Lierena R., Eysselein V.E., Thompson R.C., and Dinarello C.A. Interleukin 1 (IL-1) gene expression, synthesis, and effect of specific IL-1 receptor blockade in rabbit immune complex colitis. J Clin Invest 86 (1990) 972-980
54. Reinecker H.C., Steffen M., Witthoeft T., Pflueger I., Schreiber S., MacDermott R.P., and Raedler A. Enhanced secretion of tumour necrosis factor-alpha, IL-6, and IL-1 beta by isolated lamina propria mononuclear cells from patients with ulcerative colitis and Crohn's disease. Clin Exp Immunol 94 (1993) 174-181
55. Nikolaus S., Raedler A., Kuhbacker T., Sfikas N., Folsch U.R., and Schreiber S. Mechanisms in failure of infliximab for Crohn's disease. Lancet 356 (2000) 1475-1479
56. Rutgeerts P., D'Haens G., Targan S., Vasiliauskas E., Hanauer S.B., Present D.H., Mayer L., Van Hogezand R.A., Braakman T., DeWoody K.L., Schaible T.F., and Van Deventer S.J. Efficacy and safety of retreatment with anti-tumor necrosis factor antibody (infliximab) to maintain remission in Crohn's disease. Gastroenterology 117 (1999) 761-769
57. Huang X.R., Chun Hui C.W., Chen Y.X., Wong B.C., Fung P.C., Metz C., Cho C.H., Hui W.M., Bucala R., Lam S.K., and Lan H.Y. Macrophage migration inhibitory factor is an important mediator in the pathogenesis of gastric inflammation in rats. Gastroenterology 121 (2001) 619-630
58. Roger T., Chanson A.L., Knaup-Reymond M., and Calandra T. Macrophage migration inhibitory factor promotes innate immune responses by suppressing glucocorticoid-induced expression of mitogen-activated protein kinase phosphatase-1. Eur J Immunol 35 (2005) 3405-3413
59. Koebernick H., Grode L., David J.R., Rohde W., Rolph M.S., Mittrucker H.W., and Kaufmann S.H. Macrophage migration inhibitory factor (MIF) plays a pivotal role in immunity against Salmonella typhimurium. Proc Natl Acad Sci U S A 99 (2002) 13681-13686
60. Powell N.D., Papenfuss T.L., McClain M.A., Gienapp I.E., Shawler T.M., Satoskar A.R., and Whitacre C.C. Cutting edge: macrophage migration inhibitory factor is necessary for progression of experimental autoimmune encephalomyelitis. J Immunol 175 (2005) 5611-5614
61. Yang N., Nikolic-Paterson D.J., Ng Y.Y., Mu W., Metz C., Bacher M., Meinhardt A., Bucala R., Atkins R.C., and Lan H.Y. Reversal of established rat crescentic glomerulonephritis by blockade of macrophage migration inhibitory factor (MIF): potential role of MIF in regulating glucocorticoid production. Mol Med 4 (1998) 413-424