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J Biol Chem, Vol. 275, Issue 14, 10331-10341, April 7, 2000

Chitinases of the Avian Malaria Parasite Plasmodium gallinaceum, a Class of Enzymes Necessary for Parasite Invasion of the Mosquito Midgut*

Joseph M. VinetzDagger §, Jesus G. Valenzuela, Charles A. Specht||**, L. AravindDagger Dagger , Rebecca C. LangerDagger , Jose M. C. Ribeiro, and David C. Kaslow

From the Dagger  World Health Organization Collaborating Center for Tropical Diseases, Department of Pathology, the University of Texas Medical Branch, Galveston, Texas 77615, the  Laboratory of Parasitic Diseases, NIAID, National Institutes of Health, Bethesda, Maryland 20892, the || Department of Molecular and Cell Biology, Goldman School of Dental Medicine, Boston University, Boston, Massachusetts 02118, and the Dagger Dagger  National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, Maryland 20892

The Plasmodium ookinete produces chitinolytic activity that allows the parasite to penetrate the chitin-containing peritrophic matrix surrounding the blood meal in the mosquito midgut. Since the peritrophic matrix is a physical barrier that the parasite must cross to invade the mosquito, and the presence of allosamidin, a chitinase inhibitor, in a blood meal prevents the parasite from invading the midgut epithelium, chitinases (3.2.1.14) are potential targets of malaria parasite transmission-blocking interventions. We have purified a chitinase of the avian malaria parasite Plasmodium gallinaceum and cloned the gene, PgCHT1, encoding it. PgCHT1 encodes catalytic and substrate-binding sites characteristic of family 18 glycohydrolases. Expressed in Escherichia coli strain AD494 (DE3), recombinant PgCHT1 was found to hydrolyze polymeric chitin, native chitin oligosaccharides, and 4-methylumbelliferone derivatives of chitin oligosaccharides. Allosamidin inhibited recombinant PgCHT1 with an IC50 of 7 µM and differentially inhibited two chromatographically separable P. gallinaceum ookinete-produced chitinase activities with IC50 values of 7 and 12 µM, respectively. These two chitinase activities also had different pH activity profiles. These data suggest that the P. gallinaceum ookinete uses products of more than one chitinase gene to initiate mosquito midgut invasion.

* The costs of publication of this article were defrayed in part by the payment of page charges. The 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 GenBankTM/EMBL Data Bank with accession number(s) AF064079 and AF072442.

§ Physician Postdoctoral Fellow of the Howard Hughes Medical Institute. Recipient of a Medical Sciences scholarship from the Charles E. Culpeper Foundation and supported by the World Health Organization Collaborating Center for Tropical Diseases at the University of Texas Medical Branch at Galveston, TX. To whom correspondence should be addressed: WHO Center for Tropical Diseases, Dept. of Pathology, University of Texas Medical Branch, Keiller 2.138, 301 University Blvd., Galveston, TX 77615-0609. Tel.: 409-747-2962; Fax: 409-747-2437; E-mail: jovinetz@utmb.edu.

** Supported by Grants GM-54380 and GM-31318 from the National Institutes of Health.

Copyright © 2000 by The American Society for Biochemistry and Molecular Biology, Inc.
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