The Journal of Experimental Medicine
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© The Rockefeller University Press, 0022-1007/1998/11/1941/ $5.00
The Journal of Experimental Medicine, Volume 188, Number 10, November 16, 1998 1941-1953

Articles

Development of a Natural Model of Cutaneous Leishmaniasis: Powerful Effects of Vector Saliva and Saliva Preexposure on the Long-Term Outcome of Leishmania major Infection in the Mouse Ear Dermis

Yasmine Belkaid*, Shaden Kamhawi*, Govind Modi*, Jesus Valenzuela*, Nancy Noben-Trauth{ddagger}, Edgar Rowton§, José Ribeiro*, and David L. Sacks*

From the * Laboratory of Parasitic Diseases and the {ddagger} Laboratory of Immunology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland 20892; and the § Department of Entomology, Walter Reed Army Institute of Research, Washington DC 20307

We have developed a model of cutaneous leishmaniasis due to Leishmania major that seeks to mimic the natural conditions of infection. 1,000 metacyclic promastigotes were coinoculated with a salivary gland sonicate (SGS) obtained from a natural vector, Phlebotomus papatasii, into the ear dermis of naive mice or of mice preexposed to SGS. The studies reveal a dramatic exacerbating effect of SGS on lesion development in the dermal site, and a complete abrogation of this effect in mice preexposed to salivary components. In both BALB/c and C57Bl/6 (B/6) mice, the dermal lesions appeared earlier, were more destructive, and contained greater numbers of parasites after infection in the presence of SGS. Furthermore, coinoculation of SGS converted B/6 mice into a nonhealing phenotype. No effect of SGS was seen in either IL-4– deficient or in SCID mice. Disease exacerbation in both BALB/c and B/6 mice was associated with an early (6 h) increase in the frequency of epidermal cells producing type 2 cytokines. SGS did not elicit type 2 cytokines in the epidermis of mice previously injected with SGS. These mice made antisaliva antibodies that were able to neutralize the ability of SGS to enhance infection and to elicit IL-4 and IL-5 responses in the epidermis. These results are the first to suggest that for individuals at risk of vector-borne infections, history of exposure to vector saliva might influence the outcome of exposure to transmitted parasites.

Key Words: Leishmania major • sand flies • saliva • skin • cytokines

Address correspondence to Dr. David L. Sacks, NIAID, Laboratory of Parasitic Diseases, Bldg. 4, Rm. 126, Center Dr., MSC 0425, Bethesda, MD 20892-0425. Phone: 301-496-0577; Fax: 301-480-3708; E-mail: dsacks{at}nih.gov

Abbreviations used: DETC, dendritic epidermal T cells; DTH, delayed type hypersensitivity; SGS, salivary gland sonicate; SLA, soluble L. major antigen.


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