Lack of macrophage migration inhibitory factor suppresses innate immune response in murine dextran sulfate sodium-induced colitis

Scandinavian Journal of Gastroenterology

Volumn 43, Issue 12, 2008, Pages 1497-1504

  Ohkawara, Tatsuya ^a,c   Mitsuyama, Keiichi ^b   Takeda, Hiroshi ^c   Asaka, Masahiro ^c   Fujiyama, Yoshihide ^d   Nishihira, Jun ^a  

^a HOKKAIDO INFORMATION UNIVERSITY   (Japan)

^b KURUME UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d SHIGA UNIVERSITY OF MEDICAL SCIENCE   (Japan)

Author keywords

Chemokine; Colitis; Innate immunity; Macrophage migration inhibitory factor

Indexed keywords

CHEMOKINE; COMPLEMENTARY DNA; DEXTRAN SULFATE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; MACROPHAGE MIGRATION INHIBITION FACTOR; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; MYELOPEROXIDASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INFILTRATION; COLITIS; DISEASE ACTIVITY; DISEASE SEVERITY; ENTERITIS; ENZYME ACTIVITY; IMMUNOHISTOCHEMISTRY; INNATE IMMUNITY; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RECEPTOR UPREGULATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; SURVIVAL RATE;

ANIMALS; COLITIS; DEXTRAN SULFATE; IMMUNITY, INNATE; INTRAMOLECULAR OXIDOREDUCTASES; MACROPHAGE MIGRATION-INHIBITORY FACTORS; MALE; MICE; MICE, INBRED BALB C; MODELS, ANIMAL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 56749170706     PISSN: 00365521     EISSN: 15027708     Source Type: Journal    
DOI: 10.1080/00365520802273017     Document Type: Article

References (48)

1. Bloom BR, Bennett B. Mechanism of a reaction in vitro associated with delayed-type hypersensitivity. Science 1966;153:80-2.
2. David JR. Delayed hypersensitivity in vitro: its mediation by cell-free substances formed by lymphoid cell-antigen interaction. Proc Natl Acad Sci USA 1966;56:72-7.
3. Bucala R. MIF re-discovered: pituitary hormone and glucocorticoid-induced regulator of cytokine production. FASEB J 1996;7:19-24.
4. Donn RP, Shelley E, Ollier WE, Thompson W. A novel 5′-flanking region polymorphism of macrophage migration inhibitory factor is associated with systemic-onset juvenile idiopathic arthritis. Arthritis Rheum 2001;44:1782-5.
5. Donn R, Alourfi Z, De Benedetti F, Meazza C, Zeggini E, Lunt M, et al. Mutation screening of the macrophage migration inhibitory factor gene: positive association of a functional polymorphism of macrophage migration inhibitory factor with juvenile idiopathic arthritis. Arthritis Rheum 2002;46:2402-9.
6. Calandra T, Bernhagen J, Mitchell RA, Bucala R. The macrophage is an important and previously unrecognized source of macrophage migration inhibitory factor. J Exp Med 1994;179:1895-902.
7. Bacher M, Meinhardt A, Lan HY, Mu W, Metz CN, Chesney JA, et al. Migration inhibitory factor expression in experimentally induced endotoxemia. Am J Pathol 1997;150:235-46.
8. Bernhagen J, Calandra T, Mitchell RA, Martin SB, Tracey KJ, Voelter W, et al. MIF is a pituitary-derived cytokine that potentiates lethal endotoxaemia. Nature 1993;365:756-9.
9. Bacher M, Metz CN, Calandra T, Mayer K, Chesney J, Lohoff M, et al. An essential regulatory role for macrophage migration inhibitory factor in T-cell activation. Proc Natl Acad Sci USA 1996;93:7849-54.
10. Nishihira J. Macrophage migration inhibitory factor (MIF): its essential role in the immune system and cell growth. J Interferon Cytokine Res 2000;20:751-62.
11. Podolsky DK. Inflammatory bowel disease. N Engl J Med 2002;347:417-29.
12. Sartor RB. Pathogenesis and immune mechanisms of chronic inflammatory bowel diseases. Am J Gastroenterology 1997;92:5S-11S.
13. Papadakis KA, Targan SR. Role of cytokines in the pathogenesis of inflammatory bowel disease. Annu Rev Med 2000;51:289-98.
14. de Jong YP, Abadia-Molina AC, Satoskar AR, Clarke K, Rietdijk ST, Faubion WA, et al. Development of chronic colitis is dependent on the cytokine MIF. Nat Immunol 2001;2:1061-6.
15. Ohkawara T, Nishihira J, Takeda H, Hige S, Kato M, Sugiyama T, et al. Amelioration of dextran sulfate sodium-induced colitis by anti-macrophage migration inhibitory factor antibody in mice. Gastroenterology 2002;123:256-70.
16. Murakami H, Akbar SM, Matsui H, 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 2001;31:337-43.
17. Ohkawara T, Miyashita K, Nishihira J, Mitsuyama K, Takeda H, Kato M, et al. Transgenic overexpression of macrophage migration inhibitory factor renders mice markedly more susceptible to experimental colitis. Clin Exp Immunol 2005;140:241-8.
18. Elson CO, Sartor RB, Tennyson GS, Riddell RH. Experimental models of inflammatory bowel disease. Gastroenterology 1995;109:1344-67.
19. Okayasu I, Hatakeyama S, Yamada M, Ohkusa T, Inagaki Y, Nakaya R. A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology 1990;98:694-702.
20. Honma N, Koseki H, Akasaka T, Nakayama T, Taniguchi M, Serizawa I, et al. Deficiency of the macrophage migration inhibitory factor gene has no significant effect on endotoxaemia. Immunology 2000;100:84-90.
21. Cooper HS, Murthy SN, Shah RS, Sedergran DJ. Clinico-pathologic study of dextran sulfate sodium experimental murine colitis. Lab Invest 1993;69:238-49.
22. Bozza M, Satoskar AR, Lin G, Lu B, Humbles AA, Gerard C, et al. Targeted disruption of migration inhibitory factor gene reveals its critical role in sepsis. J Exp Med 1999;189:341-6.
23. Donnelly SC, Haslett C, Reid PT, Grant IS, Wallace WA, Metz CN, et al. Regulatory role for macrophage migration inhibitory factor in acute respiratory distress syndrome. Nat Med 1997;3:320-3.
24. Onodera S, Kaneda K, Mizue Y, Koyama Y, Fujinaga M, Nishihira J. Macrophage migration inhibitory factor up-regulates expression of matrix metalloproteinases in synovial fibroblasts of rheumatoid arthritis. J Biol Chem 2000;275:444-50.
25. Shimizu T, Abe R, Ohkawara A, Nishihira J. Ultraviolet B radiation up-regulates the production of macrophage migration inhibitory factor (MIF) in human epidermal keratinocytes. J Invest Dermatol 1999;112:210-5.
26. Fukuzawa J, Nishihira J, Hasebe N, Haneda T, Osaki J, Saito T, et al. Contribution of macrophage migration inhibitory factor to extracellular signal-regulated kinase activation by oxidative stress in cardiomyocytes. J Biol Chem 2002;277:24889-95.
27. Ohkawara T, Nishihira J, Ishiguro Y, Otsubo E, Nagai K, Takeda H, et al. Resistance to experimental colitis depends on cytoprotective heat shock proteins in macrophage migration inhibitory factor null mice. Immunol Lett 2006;107:148-54.
28. Makita H, Nishimura M, Miyamoto K, Nakano T, Tanino Y, Hirokawa J, et al. Effect of anti-macrophage migration inhibitory factor antibody on lipopolysaccharide-induced pulmonary neutrophil accumulation. Am J Respir Crit Care Med 1998;158:573-9.
29. Krawisz JE, Sharon P, Stenson WF. Quantitative assay for acute intestinal inflammation based on myeloperoxidase activity. Assessment of inflammation in rat and hamster models. Gastroenterology 1984;87:1344-50.
30. Kobayashi S, Nishihira J, Watanabe S, Todo S. Prevention of lethal acute hepatic failure by anti-macrophage migration inhibitory factor antibody in mice treated with bacille Calmette-Guerin and lipopolysaccharide. Hepatology 1999;29:1752-9.
31. Dieleman LA, Ridwan BU, Tennyson GS, Beagley KW, Bucy RP, Elson CO. Dextran sulfate sodium-induced colitis occurs in severe combined immunodeficient mice. Gastroenterology 1994;107:1643-52.
32. Banks C, Bateman A, Payne R, Johnson P, Sheron N. Chemokine expression in IBD. Mucosal chemokine expression is unselectively increased in both ulcerative colitis and Crohn's disease. J Pathol 2003;199:28-35.
33. Gijsbers K, Van Assche G, Joossens S, Struyf S, Proost P, Rutgeerts P, et al. CXCR1-binding chemokines in inflammatory bowel diseases: down-regulated IL-8/CXCL8 production by leukocytes in Crohn's disease and selective GCP/CXCL6 expression in inflamed intestinal tissue. Eur J Immunol 2004;34:1992-2000.
34. Reinecker HC, Loh EY, Ringer DJ, Mehta A, Rombeau JL, MacDermott RP, et al. Monocyte-chemoattractant protein 1 gene expression in intestinal epithelial cells and inflammatory bowel disease mucosa. Gastroenterology 1995;108:40-50.
35. MacDermott RP, Sanderson IR, Reinecker HC. The central role of chemokines (chemotactic cytokines) in the immunopathogenesis of ulcerative colitis and Crohn's disease. Inflamm Bowel Dis 1998;4:54-67.
36. McCormack G, Moriarty D, O'Donoghue DP, McCormick PA, Sheahan K, Baird AW. Tissue cytokine and chemokine expression in inflammatory bowel disease. Inflamm Res 2001;50:491-5.
37. Uguccioni M, Gionchetti P, Robbiani DF, Rizzello F, Peruzzo S, Campieri M, et al. Increased expression of IP-10, IL-8, MCP-1, MCP-3 in ulcerative colitis. Am J Pathol 1999;155:331-6.
38. Sasaki S, Yoneyama H, Suzuki K, Suriki H, Aiba T, Watanabe S, et al. Blockade of CXCL10 protects mice from acute colitis and enhances crypt cell survival. Eur J Immunol 2002;32:3197-205.
39. -/- mice. J Immunol 2003;171:1401-6.
40. Ohtsuka Y, Sanderson IR. Dextran sulfate sodium-induced inflammation is enhanced by intestinal epithelial cell chemokine expression in mice. Pediatr Res 2003;53:143-7.
41. Yoshimura T, Robinson EA, Tanaka S, Appella E, Kuratsu J, Leonard EJ. Purification and amino acid analysis of two human glioma-derived monocyte chemoattractants. J Exp Med 1989;169:1449-59.
42. Matsushima K, Larsen CG, DuBois GC, Oppenheim JJ. Purification and characterization of a novel monocyte chemotactic and activating factor produced by a human myelomonocytic cell line. J Exp Med 1989;169:1485-90.
43. Allavena P, Bianchi G, Zhou D, van Damme J, Jilek P, Sozzani S, et al. Induction of natural killer cell migration by monocyte chemotactic protein-1, -2 and -3. Eur J Immunol 1994;24:3233-6.
44. Carr MW, Roth SJ, Luther E, Rose SS, Springer TA. Monocyte chemoattractant protein 1 acts as a T-lymphocyte chemoattractant. Proc Natl Acad Sci USA 1994;91:3652-6.
45. + lymphocyte-associated Th-2-type immune response in the intestine. J Immunol 2000;164:6303-12.
46. Onodera S, Nishihira J, Koyama Y, Majima T, Aoki Y, Ichiyama H, et al. Macrophage migration inhibitory factor up-regulates the expression of interleukin-8 messenger RNA in synovial fibroblasts of rheumatoid arthritis patients: common transcriptional regulatory mechanism between interleukin-8 and interleukin-1beta. Arthritis Rheum 2004;50:1437-47.
47. Ichiyama H, Onodera S, Nishihira J, Ishibashi T, Nakayama T, Minami A, et al. Inhibition of joint inflammation and destruction induced by anti-type II collagen antibody/lipopolysaccharide (LPS)-induced arthritis in mice due to deletion of macrophage migration inhibitory factor (MIF). Cytokine 2004;26:187-94.
48. Tanino Y, Makita H, Miyamoto K, Betsuyaku T, Ohtsuka Y, Nishihira J, et al. Role of macrophage migration inhibitory factor in bleomycin-induced lung injury and fibrosis in mice. Am J Physiol Lung Cell Mol Physiol 2002;283:L156-62.