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J. Biol. Chem., Vol. 281, Issue 52, 40283-40291, December 29, 2006

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Combined Leptin Actions on Adipose Tissue and Hypothalamus Are Required to Deplete Adipocyte Fat in Lean Rats

IMPLICATIONS FOR OBESITY TREATMENT^*

Byung-Hyun Park¹, May-Yun Wang¹, Young Lee, Xinxin Yu, Mariella Ravazzola, Lelio Orci, and Roger H. Unger^¶2

From the Gifford Laboratories of the Touchstone Center for Diabetes Research, University of Texas Southwestern Medical Center, Dallas, Texas 75390-8854, ^¶Veterans Affairs Medical Center, Dallas, Texas 75216, and Department of Cell Physiology and Metabolism, University Medical Center, 1 Rue Michel Servet, 1211 Geneva 4, Switzerland

Intense hyperleptinemia completely depletes adipocyte fat of normal rats within 14 days. To determine the mechanism, epididymal fat pads from normal wild-type (+/+) and obese (fa/fa) Zucker Diabetic Fatty (ZDF) donor rats were transplanted into normal +/+ and fa/fa ZDF recipients. Hyperleptinemia induced by adenovirus-leptin administration depleted all fat from native fat pads and from fat transplants from +/+ donors but not from transplants from ZDF^fa/fa donors with defective leptin receptors. In both native and transplanted +/+ fat pads, large numbers of mitochondria were apparent, and genes involved in fatty acid oxidation were up-regulated. However, +/+ fat pads transplanted into fa/fa recipients did not respond to hyperleptinemia, suggesting lack of an essential leptin-stimulated cohormone(s). In +/+ but not in fa/fa rats, plasma catecholamine levels rose, and both P-STAT3 and P-CREB increased in adipose tissue, suggesting that both direct and indirect (hypothalamic) leptin receptor-mediated actions of hyperleptinemia are involved in depletion of adipocyte fat.

Received for publication, August 8, 2006 , and in revised form, September 19, 2006.

^* This work was supported by grants from the NIDDK, National Institutes of Health, the Department of Veterans Affairs Merit Review, the Juvenile Diabetes Research Foundation, Takeda Pharmaceuticals (to R. H. U.), and by the Swiss National Science Foundation (to L. O.). 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.

¹ Both authors contributed equally to this work.

² To whom correspondence should be addressed: Touchstone Center for Diabetes Research, University of Texas Southwestern Medical Center, 5323 Harry Hines Blvd., Dallas, TX 75390-8854. Tel.: 214-648-6742; Fax: 214-648-9191; E-mail: roger.unger{at}utsouthwestern.edu.

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