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J. Biol. Chem., Vol. 279, Issue 51, 53475-53482, December 17, 2004

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Inducible Peroxidases Mediate Nitration of Anopheles Midgut Cells Undergoing Apoptosis in Response to Plasmodium Invasion^*

Sanjeev Kumar, Lalita Gupta, Yeon Soo Han¶, and Carolina Barillas-Mury||

From the Department of Microbiology, Immunology, and Pathology, Colorado State University, Fort Collins, Colorado 80523 and Laboratory of Malaria and Vector Research, NIAID, National Institutes of Health, Rockville, Maryland 20852

Plasmodium berghei invasion of Anopheles stephensi midgut cells causes severe damage, induces expression of nitric-oxide synthase, and leads to apoptosis. The present study indicates that invasion results in tyrosine nitration, catalyzed as a two-step reaction in which nitric-oxide synthase induction is followed by increased peroxidase activity. Ookinete invasion induced localized expression of peroxidase enzymes, which catalyzed protein nitration in vitro in the presence of nitrite and H₂O₂. Histochemical stainings revealed that when a parasite migrates laterally and invades more than one cell, the pattern of induced peroxidase activity is similar to that observed for tyrosine nitration. In Anopheles gambiae, ookinete invasion elicited similar responses; it induced expression of 5 of the 16 peroxidase genes predicted by the genome sequence and decreased mRNA levels of one of them. One of these inducible peroxidases has a C-terminal oxidase domain homologous to the catalytic moiety of phagocyte NADPH oxidase and could provide high local levels of superoxide anion (), that when dismutated would generate the local increase in H₂O₂ required for nitration. Chemically induced apoptosis of midgut cells also activated expression of four ookinete-induced peroxidase genes, suggesting their involvement in general apoptotic responses. The two-step nitration reaction provides a mechanism to precisely localize and circumscribe the toxic products generated by defense reactions involving nitration. The present study furthers our understanding of the biochemistry of midgut defense reactions to parasite invasion and how these may influence the efficiency of malaria transmission by anopheline mosquitoes.

Received for publication, August 30, 2004 , and in revised form, September 27, 2004.

^* The initial part of this work at Colorado State University was funded by Grant R01AI45573 from the National Institutes of Health. 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 Table 1.

^¶ Present address: College of Agriculture and Life Science, Chonnam National University, 300 Yongbong-Dong, Puk-Gu, Gwangju, Korea.

^|| To whom correspondence should be addressed: Laboratory of Malaria and Vector Research, National Institutes of Health, 12735 Twinbrook Parkway, Rockville, MD 20852. Tel.: 301-496-3066; Fax: 301-480-1337; E-mail: cbarillas{at}niaid.nih.gov.

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