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Molecular and Cellular Biology, October 2008, p. 6196-6207, Vol. 28, No. 20
0270-7306/08/$08.00+0     doi:10.1128/MCB.00553-08
Copyright © 2008, American Society for Microbiology. All Rights Reserved.

Distinct Malaria Parasite Sporozoites Reveal Transcriptional Changes That Cause Differential Tissue Infection Competence in the Mosquito Vector and Mammalian Host{triangledown}

Sebastian A. Mikolajczak,1 Hilda Silva-Rivera,1 Xinxia Peng,1 Alice S. Tarun,1 Nelly Camargo,1 Vanessa Jacobs-Lorena,1 Thomas M. Daly,2 Lawrence W. Bergman,2 Patricia de la Vega,3 Jack Williams,3 Ahmed S. I. Aly,1 and Stefan H. I. Kappe1,4*

Seattle Biomedical Research Institute, Seattle, Washington 98109,1 Division of Molecular Parasitology, Department of Microbiology & Immunology, Drexel University College of Medicine, Philadelphia, Pennsylvania 19129,2 Walter Reed Army Institute for Research, Silver Spring, Maryland 20910,3 Department of Global Health, University of Washington, Seattle, Washington 981954

Received 5 April 2008/ Returned for modification 6 May 2008/ Accepted 31 July 2008

The malaria parasite sporozoite transmission stage develops and differentiates within parasite oocysts on the Anopheles mosquito midgut. Successful inoculation of the parasite into a mammalian host is critically dependent on the sporozoite's ability to first infect the mosquito salivary glands. Remarkable changes in tissue infection competence are observed as the sporozoites transit from the midgut oocysts to the salivary glands. Our microarray analysis shows that compared to oocyst sporozoites, salivary gland sporozoites upregulate expression of at least 124 unique genes. Conversely, oocyst sporozoites show upregulation of at least 47 genes (upregulated in oocyst sporozoites [UOS genes]) before they infect the salivary glands. Targeted gene deletion of UOS3, encoding a putative transmembrane protein with a thrombospondin repeat that localizes to the sporozoite secretory organelles, rendered oocyst sporozoites unable to infect the mosquito salivary glands but maintained the parasites' liver infection competence. This phenotype demonstrates the significance of differential UOS expression. Thus, the UIS-UOS gene classification provides a framework to elucidate the infectivity and transmission success of Plasmodium sporozoites on a whole-genome scale. Genes identified herein might represent targets for vector-based transmission blocking strategies (UOS genes), as well as strategies that prevent mammalian host infection (UIS genes).

* Corresponding author. Mailing address: Seattle Biomedical Research Institute, 307 Westlake Avenue North, Suite 500, Seattle, WA 98109-5219. Phone: (206) 256-7205. Fax: (206) 256-7229. E-mail: stefan.kappe{at}sbri.org

{triangledown} Published ahead of print on 18 August 2008.

Molecular and Cellular Biology, October 2008, p. 6196-6207, Vol. 28, No. 20
0270-7306/08/$08.00+0     doi:10.1128/MCB.00553-08
Copyright © 2008, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Sarda, V., Kaslow, D. C., Williamson, K. C. (2009). Approaches to Malaria Vaccine Development Using the Retrospectroscope. Infect. Immun. 77: 3130-3140 [Full Text]  


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