J. Exp. Med., Volume 189, Number 2, January 18, 1999 341-346

Targeted Disruption of Migration Inhibitory Factor Gene Reveals Its Critical Role in Sepsis

By Marcelo Bozza,^* Abhay R. Satoskar,^* Guosheng Lin,^* Bao Lu, Alison A. Humbles, Craig Gerard, and John R. David^*

From the ^* Department of Immunology and Infectious Diseases, Harvard School of Public Health, and the  Ina Sue Perlmutter Laboratory, Children's Hospital, Harvard Medical School, Boston, Massachusetts 02115

To study the biologic role of migration inhibitory factor (MIF), a pleiotropic cytokine, we generated a mouse strain lacking MIF by gene targeting in embryonic stem cells. Analysis of the role of MIF during sepsis showed that MIF^/ mice were resistant to the lethal effects of high dose bacterial lipopolysaccharide (LPS), or Staphylococcus aureus enterotoxin B (SEB) with D-galactosamine and had lower plasma levels of tumor necrosis factor  (TNF-) than did wild-type mice, but normal levels of interleukin (IL)-6 and IL-10. When stimulated with LPS and interferon , macrophages from MIF^/ mice showed diminished production of TNF-, normal IL-6 and IL-12, and increased production of nitric oxide. MIF^/ animals cleared gram-negative bacteria Pseudomonas aeruginosa instilled into the trachea better than did wild-type mice and had diminished neutrophil accumulation in their bronchoalveolar fluid compared to the wild-type mice. Thioglycollate elicited peritoneal exudates in uninfected MIF^/ mice, but showed normal neutrophil accumulation. Finally, the findings of enhanced resistance to P. aeruginosa and resistance to endotoxin-induced lethal shock suggest that the counteraction or neutralization of MIF may serve as an adjunct therapy in sepsis.

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• Senter, P. D., Al-Abed, Y., Metz, C. N., Benigni, F., Mitchell, R. A., Chesney, J., Han, J., Gartner, C. G., Nelson, S. D., Todaro, G. J., Bucala, R. (2002). Inhibition of macrophage migration inhibitory factor (MIF) tautomerase and biological activities by acetaminophen metabolites. Proc. Natl. Acad. Sci. USA 10.1073/pnas.011569399v1 [Abstract] [Full Text]  
• Mitchell, R. A., Liao, H., Chesney, J., Fingerle-Rowson, G., Baugh, J., David, J., Bucala, R. (2001). Macrophage migration inhibitory factor (MIF) sustains macrophage proinflammatory function by inhibiting p53: Regulatory role in the innate immune response. Proc. Natl. Acad. Sci. USA 10.1073/pnas.012511599v1 [Abstract] [Full Text]  
• Roger, T., Glauser, M. P., Calandra, T. (2001). Macrophage migration inhibitory factor (MIF) modulates innate immune responses induced by endotoxin and Gram-negative bacteria. Innate Immunity 7: 456-460 [Abstract]  
• WANG, H., YANG, H., CZURA, C. J., SAMA, A. E., TRACEY, K. J. (2001). HMGB1 as a Late Mediator of Lethal Systemic Inflammation. Am. J. Respir. Crit. Care Med. 164: 1768-1773 [Full Text]  
• Alexander, C., Rietschel, E. Th. (2001). Invited review: Bacterial lipopolysaccharides and innate immunity. Innate Immunity 7: 167-202 [Abstract]  
• Beishuizen, A., Thijs, L. G., Haanen, C., Vermes, I. (2001). Macrophage Migration Inhibitory Factor and Hypothalamo-Pituitary-Adrenal Function during Critical Illness. J. Clin. Endocrinol. Metab. 86: 2811-2816 [Abstract] [Full Text]  
• Satoskar, A. R., Bozza, M., Rodriguez Sosa, M., Lin, G., David, J. R. (2001). Migration-Inhibitory Factor Gene-Deficient Mice Are Susceptible to Cutaneous Leishmania major Infection. Infect. Immun. 69: 906-911 [Abstract] [Full Text]  
• Greenberg, P. L., Gordeuk, V., Issaragrisil, S., Siritanaratkul, N., Fucharoen, S., Ribeiro, R. C. (2001). Major Hematologic Diseases in the Developing World-- New Aspects of Diagnosis and Management of Thalassemia, Malarial Anemia, and Acute Leukemia. ASH Education Book 2001: 479-498 [Abstract] [Full Text]  
• Lin, S.-G., Yu, X.-Y., Chen, Y.-X., Huang, X. R., Metz, C., Bucala, R., Lau, C.-P., Lan, H. Y. (2000). De Novo Expression of Macrophage Migration Inhibitory Factor in Atherogenesis in Rabbits. Circ. Res. 87: 1202-1208 [Abstract] [Full Text]  
• Daun, J. M., Cannon, J. G. (2000). Macrophage migration inhibitory factor antagonizes hydrocortisone-induced increases in cytosolic Ikappa Balpha. Am. J. Physiol. Regul. Integr. Comp. Physiol. 279: R1043-R1049 [Abstract] [Full Text]  
• Wennemuth, G., Aumüller, G., Bacher, M., Meinhardt, A. (2000). Macrophage Migration Inhibitory Factor-Induced Ca2+ Response in Rat Testicular Peritubular Cells. Biol. Reprod. 62: 1632-1639 [Abstract] [Full Text]  
• Chvatchko, Y., Hoogewerf, A. J., Meyer, A., Alouani, S., Juillard, P., Buser, R., Conquet, F., Proudfoot, A. E.I., Wells, T. N.C., Power, C. A. (2000). A Key Role for CC Chemokine Receptor 4 in Lipopolysaccharide-induced Endotoxic Shock. JEM 191: 1755-1764 [Abstract] [Full Text]  
• Grohmann, U., Van Snick, J., Campanile, F., Silla, S., Giampietri, A., Vacca, C., Renauld, J.-C., Fioretti, M. C., Puccetti, P. (2000). IL-9 Protects Mice from Gram-Negative Bacterial Shock: Suppression of TNF-{alpha}, IL-12, and IFN-{gamma}, and Induction of IL-10. J. Immunol. 164: 4197-4203 [Abstract] [Full Text]  
• Senter, P. D., Al-Abed, Y., Metz, C. N., Benigni, F., Mitchell, R. A., Chesney, J., Han, J., Gartner, C. G., Nelson, S. D., Todaro, G. J., Bucala, R. (2002). Inhibition of macrophage migration inhibitory factor (MIF) tautomerase and biological activities by acetaminophen metabolites. Proc. Natl. Acad. Sci. USA 99: 144-149 [Abstract] [Full Text]  
• Mitchell, R. A., Liao, H., Chesney, J., Fingerle-Rowson, G., Baugh, J., David, J., Bucala, R. (2002). Macrophage migration inhibitory factor (MIF) sustains macrophage proinflammatory function by inhibiting p53: Regulatory role in the innate immune response. Proc. Natl. Acad. Sci. USA 99: 345-350 [Abstract] [Full Text]  

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