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Journal of Lipid Research, Vol. 48, 1463-1475, July 2007
Copyright © 2007 by American Society for Biochemistry and Molecular Biology

Cytoplasmic lipid droplet accumulation in developing mammary epithelial cells: roles of adipophilin and lipid metabolism

Tanya D. Russell^1,*,, Carol A. Palmer^1,, David J. Orlicky^**, Andreas Fischer, Michael C. Rudolph, Margaret C. Neville^,, and James L. McManaman^2,*,,,

^* Graduate Programs in Molecular Biology, University of Colorado Health Sciences Center, Aurora, CO
Cell and Developmental Biology, University of Colorado Health Sciences Center, Aurora, CO
Division of Basic Reproductive Science, Department of Obstetrics and Gynecology, University of Colorado Health Sciences Center, Aurora, CO
Departments of Physiology and Biophysics, University of Colorado Health Sciences Center, Aurora, CO
^** Department of Pathology, University of Colorado Health Sciences Center, Aurora, CO
Department of Pharmacology and Toxicology, Charité-University Medicine, Berlin, Germany

Published, JLR Papers in Press, April 23, 2007.

¹ T. D. Russell and C. A. Palmer contributed equally to these studies.

² To whom correspondence should be addressed. e-mail: jim.mcmanaman{at}uchsc.edu

PAT proteins (perilipin, adipophilin, and TIP47) are hypothesized to be critical regulators of lipid accumulation in eukaryotic cells. We investigated the developmental relationships between the expression of these proteins and cytoplasmic lipid droplet (CLD) accumulation in differentiating secretory epithelial cells in mouse mammary glands. Adipophilin (ADPH) specifically localized to CLD in differentiating and lactating mammary glands and was found exclusively in the secreted lipid droplet fraction of mouse milk. ADPH transcripts were selectively detected in secretory epithelial cells, and steady-state levels of both ADPH mRNA and protein increased during secretory differentiation in patterns consistent with functional linkage to CLD accumulation. TIP47 also was detected in secretory epithelial cells; however, it had a diffuse punctate appearance, and its mRNA and protein expression patterns did not correlate with CLD accumulation. Perilipin-positive adipose cells and steady-state levels of perilipin mRNA and protein decreased during mammary gland differentiation, suggesting a progressive loss of adipose lipid storage during this process. Collectively, these data demonstrate that increased ADPH expression is a specialized property of differentiated secretory epithelial cells and provide developmental evidence specifically linking increased ADPH expression to increased CLD accumulation. In addition, evidence is presented that the epithelial and adipose compartments of the mammary gland undergo concerted, developmentally regulated shifts in lipid metabolism that increase the availability of fatty acids necessary for lipid synthesis by milk-secreting cells.

Supplementary key words perilipin • mammary gland • adipose • fatty acid • cytoplasmic lipid droplet • differentiation • triglyceride

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