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J. Biol. Chem., Vol. 280, Issue 25, 24085-24094, June 24, 2005

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The Adipocyte as an Important Target Cell for Trypanosoma cruzi Infection^*

Terry P. Combs, Nagajyothi¶, Shankar Mukherjee¶, Cecilia J. G. de Almeida||, Linda A. Jelicks**, William Schubert||, Ying Lin, David S. Jayabalan, Dazhi Zhao¶, Vicki L. Braunstein¶, Shira Landskroner-Eiger, Aisha Cordero, Stephen M. Factor¶, Louis M. Weiss¶, Michael P. Lisanti||, Herbert B. Tanowitz¶, and Philipp E. Scherer

From the Departments of Cell Biology, ^¶Pathology, ^||Molecular Pharmacology, ^**Physiology and Biophysics, and Medicine, Albert Einstein College of Medicine, Bronx, New York 10461

Adipose tissue plays an active role in normal metabolic homeostasis as well as in the development of human disease. Beyond its obvious role as a depot for triglycerides, adipose tissue controls energy expenditure through secretion of several factors. Little attention has been given to the role of adipocytes in the pathogenesis of Chagas disease and the associated metabolic alterations. Our previous studies have indicated that hyperglycemia significantly increases parasitemia and mortality in mice infected with Trypanosoma cruzi. We determined the consequences of adipocyte infection in vitro and in vivo. Cultured 3T3-L1 adipocytes can be infected with high efficiency. Electron micrographs of infected cells revealed a large number of intracellular parasites that cluster around lipid droplets. Furthermore, infected adipocytes exhibited changes in expression levels of a number of different adipocyte-specific or adipocyte-enriched proteins. The adipocyte is therefore an important target cell during acute Chagas disease. Infection of adipocytes by T. cruzi profoundly influences the pattern of adipokines. During chronic infection, adipocytes may represent an important long-term reservoir for parasites from which relapse of infection can occur. We have demonstrated that acute infection has a unique metabolic profile with a high degree of local inflammation in adipose tissue, hypoadiponectinemia, hypoglycemia, and hypoinsulinemia but with relatively normal glucose disposal during an oral glucose tolerance test.

Received for publication, November 12, 2004 , and in revised form, March 31, 2005.

^* This work was supported by National Institutes of Health National Research Service Award DK61228 (to T. P. C.) and National Institutes of Health Grants AI-52739, D43TW007129 (FIC-NIH), and AI-12770 (to H. B. T.), R01-HL073163-01 (to L. A. J. and P. E. S.), AI-062730 (to L. A. J.), and R01-DK55758 and R03 EY014935-01 (to P. E. S.). 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.

Present address: Dept. of Nutrition, University of North Carolina at Chapel Hill, McGavran-Greenberg Hall, CB7461, Chapel Hill, NC 27599-7461.

Recipient of an Irma T. Hirschl Career Scientist award. To whom correspondence should be addressed: Dept. of Cell Biology, Albert Einstein College of Medicine, 1300 Morris Park Ave., Bronx, NY 10461. Tel.: 718-430-2928; Fax: 718-430-8574; E-mail: scherer{at}aecom.yu.edu.

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