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Infection and Immunity, March 2004, p. 1240-1247, Vol. 72, No. 3
0019-9567/04/$08.00+0     DOI: 10.1128/IAI.72.3.1240-1247.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

Sand Fly Saliva Enhances Leishmania amazonensis Infection by Modulating Interleukin-10 Production

Nilufer B. Norsworthy,1 Jiaren Sun,1 Dia Elnaiem,2 Gregory Lanzaro,2 and Lynn Soong1,3*

Departments of Microbiology and Immunology,1 of Pathology, Center for Biodefense and Emerging Infectious Diseases, Sealy Center for Vaccine Development, University of Texas Medical Branch at Galveston, Galveston, Texas 77555-1070,3 Department of Entomology, University of California, Davis, California 956162

Received 3 September 2003/ Returned for modification 26 October 2003/ Accepted 10 December 2003

After transmission through the bite of female sand flies, Leishmania spp. can cause a broad spectrum of disease manifestations collectively known as leishmaniases. L. amazonensis is endemic in South America, where it causes cutaneous, diffuse cutaneous, and visceral leishmaniasis. In this study, we have provided evidence that salivary gland extracts (SGE) of Lutzomyia longipalpis enhances L. amazonensis infection. BALB/c mice infected intradermally in the ear with 105 metacyclic promastigotes of L. amazonensis together with SGE (equivalent to 0.5 gland) showed an early onset of disease and larger lesions that contained ~3-log-units more parasites than did controls. To determine the potential mechanism underlying this enhancement, we assessed cytokine production via reverse transcriptase PCR and enzyme-linked immunosorbent assay. Mice coinjected with parasites and SGE displayed higher levels of interleukin-10 (IL-10) mRNA in the ear tissues, as well as higher levels of IL-10 in supernatants of restimulated draining lymph node (LN) cells, than did controls. Flow cytometric analysis revealed high frequencies of IL-10-producing CD4+ and CD8+ T cells in the draining LN of mice coinjected with the parasite and SGE. In addition, we examined bone marrow derived-macrophage cultures and detected increased IL-10 but decreased nitric oxide (NO) production in cells exposed to SGE prior to infection with L. amazonensis. Together, these results imply that the sand fly saliva facilitates Leishmania evasion of the host immune system by modulating IL-10 production.

* Corresponding author. Mailing address: Department of Microbiology and Immunology, University of Texas Medical Branch, Medical Research Building 3.132, 301 University Blvd., Galveston, TX 77555-1019. Phone: (409)772-8149. Fax: (409)747-6869. E-mail: lysoong{at}utmb.edu.

Editor: W. A. Petri, Jr.

Infection and Immunity, March 2004, p. 1240-1247, Vol. 72, No. 3
0019-9567/04/$08.00+0     DOI: 10.1128/IAI.72.3.1240-1247.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.



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