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J. Biol. Chem., Vol. 279, Issue 33, 34101-34106, August 13, 2004

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A Pattern Recognition Serine Proteinase Triggers the Prophenoloxidase Activation Cascade in the Tobacco Hornworm, Manduca sexta^*

Chuanyi Ji, Yang Wang, Xiaoping Guo, Steve Hartson¶, and Haobo Jiang||

From the Department of Entomology and Plant Pathology, Oklahoma State University, Stillwater, Oklahoma 74078 and the ^¶Department of Biochemistry and Molecular Biology, Oklahoma State University, Stillwater, Oklahoma 74078

A serine proteinase cascade in insect hemolymph mediates prophenoloxidase activation, a defense mechanism against pathogen or parasite infection. Little is known regarding its initiating proteinase or how this enzyme is activated in response to invading microorganisms. We have isolated from the tobacco hornworm, Manduca sexta, a cDNA encoding a modular protein designated hemolymph proteinase 14 (HP14). It contains five low density lipoprotein receptor class A repeats, a Sushi domain, a unique Cys-rich region, and a proteinase-catalytic domain. The HP14 mRNA exists in fat body and hemocytes of the naive larvae, and its level increases significantly at 24 h after a bacterial challenge. We expressed proHP14 with a carboxyl-terminal hexahistidine tag in a baculovirus/insect cell system and detected the recombinant protein in two forms. The 87-kDa protein was primarily intracellular, whereas the 75-kDa form was present in the medium. Interaction with peptidoglycan resulted in proteolytic processing of the purified zymogen and generation of an amidase activity. Supplementation of hemolymph with proHP14 greatly enhanced prophenoloxidase activation in response to Micrococcus luteus. These data suggest that proHP14 is a pattern recognition protein that binds to bacteria and autoactivates and triggers the prophenoloxidase activation system in the hemolymph of M. sexta.

Received for publication, April 26, 2004 , and in revised form, June 7, 2004.

^* This work was supported by the National Institutes of Health Grant GM58634 (to H. J.). 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 GenBank^TM/EBI Data Bank with accession number(s) AY380790.

Both authors contributed equally to this work.

^|| To whom correspondence should be addressed: Dept. of Entomology and Plant Pathology, Oklahoma State University, Stillwater, OK 74078, Tel.: 405-744-9400; Fax: 405-744-6039; E-mail: haobo{at}okstate.edu.

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