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J. Biol. Chem., Vol. 283, Issue 37, 25316-25323, September 12, 2008

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Molecular Control of Phenoloxidase-induced Melanin Synthesis in an Insect^*

Hongnan Kan, Chan-Hee Kim, Hyun-Mi Kwon, Ji-Won Park, Kyung-Baeg Roh, Hanna Lee, Bum-Joon Park^¶, Rong Zhang, Jinghai Zhang, Kenneth Söderhäll^||, Nam-Chul Ha, and Bok Luel Lee¹

From the National Research Laboratory of Defense Proteins, College of Pharmacy, and the ^¶Department of Molecular Biology, College of Natural Science, Pusan National University, Busan 609-735, Korea, the School of Life Science and Biopharmaceutics, Shenyang Pharmaceutical University, Shenyang 110016, China, and the ^||Department of Comparative Physiology, Evolutionary Biology Center, Uppsala University, Norbyvägen 18A, SE-752 36 Uppsala, Sweden

The melanization reaction induced by activated phenoloxidase in arthropods must be tightly controlled because of excessive formation of quinones and excessive systemic melanization damage to the hosts. However, the molecular mechanism by which phenoloxidase-induced melanin synthesis is regulated in vivo is largely unknown. It is known that the Spätzle-processing enzyme is a key enzyme in the production of cleaved Spätzle from pro-Spätzle in the Drosophila Toll pathway. Here, we provide biochemical evidence that the Tenebrio molitor Spätzle-processing enzyme converts both the 79-kDa Tenebrio prophenoloxidase and Tenebrio clip-domain SPH1 zymogen to an active melanization complex. This complex, consisting of the 76-kDa Tenebrio phenoloxidase and an active form of Tenebrio clip-domain SPH1, efficiently produces melanin on the surface of bacteria, and this activity has a strong bactericidal effect. Interestingly, we found the phenoloxidase-induced melanization reaction to be tightly regulated by Tenebrio prophenoloxidase, which functions as a competitive inhibitor of melanization complex formation. These results demonstrate that the Tenebrio Toll pathway and the melanization reaction share a common serine protease for the regulation of these two major innate immune responses.

Received for publication, June 6, 2008

^* This work was supported by programs of the National Research Laboratory (Grant M10400000028-04J0000-02) of the Ministry of Science and Technology/Korea Science and Engineering Foundation and in part by the BK21 Program and a 2007 Pusan National University postdoctoral fellowship grant (to C.-H. K.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains supplemental "Experimental Procedures," Fig. 1, and additional references.

This article was selected as a Paper of the Week.

¹ To whom correspondence should be addressed: National Research Lab. of Defense Proteins, College of Pharmacy, Pusan National University, Jangjeon Dong, Kumjeong Ku, Busan 609-735, Korea. Tel.: 82-51-510-2809; Fax: 82-51-513-2801; E-mail: brlee{at}pusan.ac.kr.

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