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J. Biol. Chem., Vol. 279, Issue 5, 3218-3227, January 30, 2004

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Peptidoglycan Recognition Proteins Involved in 1,3--D-Glucan-dependent Prophenoloxidase Activation System of Insect^*

Mi Hee Lee, Tsukasa Osaki¶, Joo Young Lee, Min Ji Baek, Rong Zhang, Ji Won Park, Shun-ichiro Kawabata¶, Kenneth Söderhäll||, and Bok Luel Lee**

From the College of Pharmacy, Pusan National University, Jangjeon Dong, Kumjeong Ku, Busan 609-735, Korea, the ^¶Department of Biology, Faculty of Sciences, Kyushu University, Fukuoka 812-8581, Japan, and the ^||Department of Comparative Physiology, Evolutionary Biology Center, Uppsala University, Norbyvägen 18A, SE-752 36 Uppsala, Sweden

The prophenoloxidase (proPO) cascade is a major innate immune response in invertebrates, which is triggered into its active form by elicitors, such as lipopolysaccharide, peptidoglycan, and 1,3--D-glucan. A key question of the proPO system is how pattern recognition proteins recognize pathogenic microbes and subsequently activate the system. To investigate the biological function of 1,3--D-glucan pattern recognition protein in the proPO cascade system, we isolated eight different 1,3--D-glucan-binding proteins from the hemolymph of large beetle (Holotrichia diomphalia) larvae by using 1,3--D-glucan immobilized column. Among them, a 20- and 17-kDa protein (referred to as Hd-PGRP-1 and Hd-PGRP-2) show high sequence identity with the short forms of peptidoglycan recognition proteins (PGRPs-S) from human and Drosophila melanogaster. To be able to characterize the biochemical properties of these two proteins, we expressed them in Drosophila S2 cells. Hd-PGRP-1 and Hd-PGRP-2 were found to specifically bind both 1,3--D-glucan and peptidoglycan. By BIAcore analysis, the minimal 1,3--D-glucan structure required for binding to Hd-PGRP-1 was found to be laminaritetraose. Hd-PGRP-1 increased serine protease activity upon binding to 1,3--D-glucan and subsequently induced the phenoloxidase activity in the presence of both 1,3--D-glucan and Ca²⁺, but no phenoloxidase activity was elicited under the same conditions in the presence of peptidoglycan and Ca²⁺. These results demonstrate that Hd-PGRP-1 can serve as a receptor for 1,3--D-glucan in the insect proPO activation system.

Received for publication, September 4, 2003 , and in revised form, October 27, 2003.

^* This work was supported by Korean Research Foundation Grant KRF-2002-042-C00203 (to B. L. L.), a grant from the Swedish Foundation for International Cooperation in Research and Higher Education (to K. S. and B. L. L.), and by a 2003 Pusan National University research grant (to B. L. L.). 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 nucleotide sequence(s) reported in this paper has been submitted to the DDBJ/GenBank^TM/EBI Data Bank with accession number(s) AB115774, AB115775, and AB115776 (for Hd-PGRP-1, Hd-PGRP-2, and Hd-PGRP-3, respectively).

These authors contributed equally to this work.

^** To whom all correspondence should be addressed. Tel.: 82-51-510-2809; Fax: 82-51-513-6754; E-mail: brlee{at}pusan.ac.kr.

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