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Differences in Gamma Interferon Production Induced by Listeriolysin O and Ivanolysin O Result in Different Levels of Protective Immunity in Mice Infected with Listeria monocytogenes and Listeria ivanovii

Terumi Kimoto, Ikuo Kawamura,^* Chikara Kohda, Takamasa Nomura, Kohsuke Tsuchiya, Yutaka Ito, Isao Watanabe, Taijin Kaku, Endang Setianingrum, and Masao Mitsuyama

Department of Microbiology, Kyoto University Graduate School of Medicine, Kyoto 606-8501, Japan

Received 18 October 2002/ Returned for modification 10 December 2002/ Accepted 14 February 2003

Two pathogenic species in the genus Listeria, Listeria monocytogenes and Listeria ivanovii, are characterized by the production of hemolysins belonging to cholesterol-dependent cytolysins, listeriolysin O (LLO) and ivanolysin O (ILO), respectively. LLO, produced by L. monocytogenes, is able to induce gamma interferon (IFN-) production and contributes to the generation of Th1-dependent protective immunity. On the other hand, nothing is known about the role of ILO, produced by L. ivanovii, in this regard. In this study, we immunized mice with 0.1 50% lethal dose (LD₅₀) of L. monocytogenes and L. ivanovii. Protective immunity against a challenge with 10 LD₅₀ was generated in mice infected with L. monocytogenes, whereas L. ivanovii infection did not induce protection. After immunization, the level of IFN- in serum samples was increased in mice given L. monocytogenes but not in those given L. ivanovii. To determine the IFN--inducing activity of cytolysins, recombinant protein was constructed. Recombinant ILO exhibited significantly lower IFN--inducing activity than LLO. By comparing the IFN--inducing activity of a chimera incorporating LLO and ILO, it was found that domains 1 to 3 of LLO were critical for IFN--inducing activity while the counterpart in ILO was unable to induce cytokine production. These results suggested that the weak ability of ILO to induce IFN- production is responsible for the failure of L. ivanovii to generate effective protective immunity.

Editor: W. A. Petri, Jr.

Department of Bacteriology, Showa University School of Medicine, 1-5-8 Hatanodai, Shinagawa, Tokyo 142-8555, Japan.

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