J. Exp. Med., Volume 189, Number 4, February 15, 1999 615-625

Endotoxin-tolerant Mice Have Mutations in Toll-like Receptor 4 (Tlr4)

By Salman T. Qureshi,^* Line Larivière, Gary Leveque, Sophie Clermont, Karen J. Moore,^¶ Philippe Gros, and Danielle Malo^*§

From the ^* Department of Medicine,  Department of Biochemistry, and ^§ Department of Human Genetics, McGill University, Montreal, Quebec, Canada H3G 1A4; the  Centre for the Study of Host Resistance, Montreal General Hospital, Montreal, Quebec, Canada H3G 1A4; and ^¶ Millennium Pharmaceuticals, Inc., Cambridge, Massachusetts 02139

Bacterial lipopolysaccharide (LPS) provokes a vigorous, generalized proinflammatory state in the infected host. Genetic regulation of this response has been localized to the Lps locus on mouse chromosome 4, through study of the C3H/HeJ and C57BL/10ScCr inbred strains. Both C3H/HeJ and C57BL/10ScCr mice are homozygous for a mutant Lps allele (Lps^d/d) that confers hyporesponsiveness to LPS challenge, and therefore exhibit natural tolerance to its lethal effects. Genetic and physical mapping of 1,345 backcross progeny segregating this mutant phenotype confined Lps to a 0.9-cM interval spanning 1.7 Mb. Three transcription units were identified within the candidate interval, including Toll-like receptor 4 (Tlr4), part of a protein family with members that have been implicated in LPS-induced cell signaling. C3H/HeJ mice have a point mutation within the coding region of the Tlr4 gene, resulting in a nonconservative substitution of a highly conserved proline by histidine at codon 712, whereas C57BL/ 10ScCr mice exhibit a deletion of Tlr4. Identification of distinct mutations involving the same gene at the Lps locus in two different hyporesponsive inbred mouse strains strongly supports the hypothesis that altered Tlr4 function is responsible for endotoxin tolerance.

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• Matsumoto, S., Matsumoto, M., Umemori, K., Ozeki, Y., Furugen, M., Tatsuo, T., Hirayama, Y., Yamamoto, S., Yamada, T., Kobayashi, K. (2005). DNA Augments Antigenicity of Mycobacterial DNA-Binding Protein 1 and Confers Protection against Mycobacterium tuberculosis Infection in Mice. J. Immunol. 175: 441-449 [Abstract] [Full Text]  
• Toshchakov, V. U., Basu, S., Fenton, M. J., Vogel, S. N. (2005). Differential Involvement of BB Loops of Toll-IL-1 Resistance (TIR) Domain-Containing Adapter Proteins in TLR4- versus TLR2-Mediated Signal Transduction. J. Immunol. 175: 494-500 [Abstract] [Full Text]  
• Bluml, S., Kirchberger, S., Bochkov, V. N., Kronke, G., Stuhlmeier, K., Majdic, O., Zlabinger, G. J., Knapp, W., Binder, B. R., Stockl, J., Leitinger, N. (2005). Oxidized Phospholipids Negatively Regulate Dendritic Cell Maturation Induced by TLRs and CD40. J. Immunol. 175: 501-508 [Abstract] [Full Text]  
• Cho, H.-Y., Jedlicka, A. E., Clarke, R., Kleeberger, S. R. (2005). Role of Toll-like receptor-4 in genetic susceptibility to lung injury induced by residual oil fly ash. Physiol. Genomics 22: 108-117 [Abstract] [Full Text]  
• Mancek Keber, M., Gradisar, H., Jerala, R. (2005). MD-2 and Der p 2 -- a tale of two cousins or distant relatives?. Innate Immunity 11: 186-192 [Abstract]  
• Saha, S., Engstrom, L., Mackerlova, L., Jakobsson, P.-J., Blomqvist, A. (2005). Impaired febrile responses to immune challenge in mice deficient in microsomal prostaglandin E synthase-1. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288: R1100-R1107 [Abstract] [Full Text]  
• Kaiser, W. J., Offermann, M. K. (2005). Apoptosis Induced by the Toll-Like Receptor Adaptor TRIF Is Dependent on Its Receptor Interacting Protein Homotypic Interaction Motif. J. Immunol. 174: 4942-4952 [Abstract] [Full Text]  
• Hollingsworth, J. W., Chen, B. J., Brass, D. M., Berman, K., Gunn, M. D., Cook, D. N., Schwartz, D. A. (2005). The Critical Role of Hematopoietic Cells in Lipopolysaccharide-induced Airway Inflammation. Am. J. Respir. Crit. Care Med. 171: 806-813 [Abstract] [Full Text]  
• Morris, G. E., Whyte, M. K. B., Martin, G. F., Jose, P. J., Dower, S. K., Sabroe, I. (2005). Agonists of Toll-like Receptors 2 and 4 Activate Airway Smooth Muscle via Mononuclear Leukocytes. Am. J. Respir. Crit. Care Med. 171: 814-822 [Abstract] [Full Text]  
• Iqbal, M., Philbin, V. J., Withanage, G. S. K., Wigley, P., Beal, R. K., Goodchild, M. J., Barrow, P., McConnell, I., Maskell, D. J., Young, J., Bumstead, N., Boyd, Y., Smith, A. L. (2005). Identification and Functional Characterization of Chicken Toll-Like Receptor 5 Reveals a Fundamental Role in the Biology of Infection with Salmonella enterica Serovar Typhimurium. Infect. Immun. 73: 2344-2350 [Abstract] [Full Text]  
• Hirsch, E., Wang, H. (2005). The Molecular Pathophysiology of Bacterially Induced Preterm Labor: Insights From the Murine Model. Reproductive Sciences 12: 145-155 [Abstract]  
• Lentschat, A., Karahashi, H., Michelsen, K. S., Thomas, L. S., Zhang, W., Vogel, S. N., Arditi, M. (2005). Mastoparan, a G Protein Agonist Peptide, Differentially Modulates TLR4- and TLR2-Mediated Signaling in Human Endothelial Cells and Murine Macrophages. J. Immunol. 174: 4252-4261 [Abstract] [Full Text]  
• Kim, J.-I., Lee, C. J., Jin, M. S., Lee, C.-H., Paik, S.-G., Lee, H., Lee, J.-O. (2005). Crystal Structure of CD14 and Its Implications for Lipopolysaccharide Signaling. J. Biol. Chem. 280: 11347-11351 [Abstract] [Full Text]  
• Singleton, T. E., Massari, P., Wetzler, L. M. (2005). Neisserial Porin-Induced Dendritic Cell Activation Is MyD88 and TLR2 Dependent. J. Immunol. 174: 3545-3550 [Abstract] [Full Text]  
• De Creus, A., Abe, M., Lau, A. H., Hackstein, H., Raimondi, G., Thomson, A. W. (2005). Low TLR4 Expression by Liver Dendritic Cells Correlates with Reduced Capacity to Activate Allogeneic T Cells in Response to Endotoxin. J. Immunol. 174: 2037-2045 [Abstract] [Full Text]  
• Kobayashi, K. S., Chamaillard, M., Ogura, Y., Henegariu, O., Inohara, N., Nunez, G., Flavell, R. A. (2005). Nod2-Dependent Regulation of Innate and Adaptive Immunity in the Intestinal Tract. Science 307: 731-734 [Abstract] [Full Text]  

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