Adipophilin regulates maturation of cytoplasmic lipid droplets and alveolae in differentiating mammary glands

Journal of Cell Science

Volumn 124, Issue 19, 2011, Pages 3247-3253

  Russell, Tanya D ^a,b   Schaack, Jerome ^a   Orlicky, David J ^b   Palmer, Carol ^a,b   Chang, Benny Hung Junn ^c   Chan, Lawrence ^c   McManaman, James L ^a,b  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Adenovirus; Adipophilin; Adipose triglyceride lipase; Differentiation; Lipid droplet; Mammary gland

Indexed keywords

ADIPOPHILIN; FAT DROPLET; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL TISSUE; ARTICLE; BREAST DEVELOPMENT; CONTROLLED STUDY; LIPID ANALYSIS; LIPOLYSIS; MAMMARY GLAND; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; TISSUE DIFFERENTIATION;

ANIMALS; CASEINS; CYTOPLASM; FEMALE; GREEN FLUORESCENT PROTEINS; LACTATION; LIPASE; LIPID METABOLISM; MAMMARY GLANDS, ANIMAL; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; PROTEIN BINDING; RECOMBINANT FUSION PROTEINS;

ADENOVIRIDAE; MUS;

EID: 80054020618     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.082974     Document Type: Article

References (39)

1. Allen, J. C., Keller, R. P., Archer, P. C. and Neville, M. C. (1991). Studies in human lactation: 6. Milk composition and daily secretion rates of macronutrients in the first year of lactation. Am. J. Clin. Nutr. 54, 69-80.
2. Anderson, S. M., Rudolph, M. C., McManaman, J. L. and Neville, M. C. (2007). Key stages in mammary gland development. Secretory activation in the mammary gland: it's not just about milk protein synthesis! Breast Cancer Res. 9, 204.
3. Brasaemle, D. L. (2007a). The perilipin family of structural lipid droplet proteins: stabilization of lipid droplets and control of lipolysis. J. Lipid Res. 48, 2547-2549.
4. Brasaemle, D. L. (2007b). Thematic review series: adipocyte biology. The perilipin family of structural lipid droplet proteins: stabilization of lipid droplets and control of lipolysis. J. Lipid Res. 48, 2547-2559.
5. Brasaemle, D. L., Subramanian, V., Garcia, A., Marcinkiewicz, A. and Rothenberg, A. (2009). Perilipin A and the control of triacylglycerol metabolism. Mol. Cell. Biochem. 326, 15-21.
6. Browning, J. D. and Horton, J. D. (2004). Molecular mediators of hepatic steatosis and liver injury. J. Clin. Invest. 114, 147-152.
7. Cases, S., Zhou, P., Shillingford, J. M., Wiseman, B. S., Fish, J. D., Angle, C. S., Hennighausen, L., Werb, Z. and Farese, R. V., Jr (2004). Development of the mammary gland requires DGAT1 expression in stromal and epithelial tissues. Development 131, 3047-3055.
8. Chang, B. H., Li, L., Paul, A., Taniguchi, S., Nannegari, V., Heird, W. C. and Chan, L. (2006). Protection against fatty liver but normal adipogenesis in mice lacking adipose differentiation-related protein. Mol. Cell. Biol. 26, 1063-1076.
9. Chong, B. M., Russell, T. D., Schaack, J., Orlicky, D. J., Reigan, P., Ladinsky, M. and McManaman, J. L. (2011). The adipophilin C-terminus is a self-folding membrane binding domain that is important for milk lipid secretion. J. Biol. Chem. 286, 23254-23265.
10. Ducharme, N. A. and Bickel, P. E. (2008). Lipid droplets in lipogenesis and lipolysis. Endocrinology 149, 942-949.
11. Evans, R. K., Nawrocki, D. K., Isopi, L. A., Williams, D. M., Casimiro, D. R., Chin, S., Chen, M., Zhu, D. M., Shiver, J. W. and Volkin, D. B. (2004). Development of stable liquid formulations for adenovirus-based vaccines. J. Pharm. Sci. 93, 2458-2475.
12. 2+ entry. J. Biol. Chem. 275, 40187-40194.
13. Granneman, J. G., Moore, H. P., Granneman, R. L., Greenberg, A. S., Obin, M. S. and Zhu, Z. (2007). Analysis of lipolytic protein trafficking and interactions in adipocytes. J. Biol. Chem. 282, 5726-5735.
14. He, T. C., Zhou, S., da Costa, L. T., Yu, J., Kinzler, K. W. and Vogelstein, B. (1998). A simplified system for generating recombinant adenoviruses. Proc. Natl. Acad. Sci. USA 95, 2509-2514.
15. Hollmann, K. H. (1974). Cytology and fine structure of the mammary gland. In Lactation, Vol. 1 (ed. B. L. Larson and V. R. Smith), pp. 3-95. New York: Academic Press.
16. Imai, Y., Varela, G. M., Jackson, M. B., Graham, M. J., Crooke, R. M. and Ahima, R. S. (2007). Reduction of hepatosteatosis and lipid levels by an adipose differentiation-related protein antisense oligonucleotide. Gastroenterology 132, 1947-1954.
17. Jensen, D. R., Gavigan, S., Sawicki, V., Witsell, D., Eckel, R. H. and Neville, M. C. (1994). Regulation of lipoprotein lipase activity in the mammary gland of the lactating mouse. Biochem. J. 298, 321-327.
18. Listenberger, L. L., Han, X., Lewis, S. E., Cases, S., Farese, R. V., Jr, Ory, D. S. and Schaffer, J. E. (2003). Triglyceride accumulation protects against fatty acid-induced lipotoxicity. Proc. Natl. Acad. Sci. USA 100, 3077-3082.
19. Listenberger, L. L., Ostermeyer-Fay, A. G., Goldberg, E. B., Brown, W. J. and Brown, D. A. (2007). Adipocyte differentiation-related protein reduces lipid droplet association of adipose triglyceride lipase and slows triacylglycerol turnover. J. Lipid Res. 48, 2751-2761.
20. Martinez-Botas, J., Anderson, J. B., Tessier, D., Lapillonne, A., Chang, B. H., Quast, M. J., Gorenstein, D., Chen, K. H. and Chan, L. (2000). Absence of perilipin results in leanness and reverses obesity in Lepr(db/db) mice. Nat. Genet. 26, 474-479.
21. McManaman, J. L. (2009). Formation of milk lipids: a molecular perspective. Clin. Lipidol. 4, 391-401.
22. McManaman, J. L., Palmer, C. A., Wright, R. M. and Neville, M. C. (2002). Functional regulation of xanthine oxidoreductase expression and localization in the mouse mammary gland: evidence of a role in lipid secretion. J. Physiol. 545, 567-579.
23. Miller, N., Delbecchi, L., Petitclerc, D., Wagner, G. F., Talbot, B. G. and Lacasse, P. (2006). Effect of stage of lactation and parity on mammary gland cell renewal. J. Dairy Sci. 89, 4669-4677.
24. Murphy, D. J. (2001). The biogenesis and functions of lipid bodies in animals, plants and microorganisms. Prog. Lipid Res. 40, 325-438.
25. Natali, F., Siculella, L., Salvati, S. and Gnoni, G. V. (2007). Oleic acid is a potent inhibitor of fatty acid and cholesterol synthesis in C6 glioma cells. J. Lipid Res. 48, 1966-1975.
26. Orlicky, D. J. and Schaack, J. (2001). Adenovirus transduction of 3T3-L1 cells. J. Lipid Res. 42, 460-466.
27. Orlicky, D. J., Degala, G., Greenwood, C., Bales, E. S., Russell, T. D. and McManaman, J. L. (2008). Multiple functions encoded by the N-terminal PAT domain of adipophilin. J. Cell Sci. 121, 2921-2929.
28. Robinson, G. W., McKnight, R. A., Smith, G. H. and Hennighausen, L. (1995). Mammary epithelial cells undergo secretory differentiation in cycling virgins but require pregnancy for the establishment of terminal differentiation. Development 121, 2079-2090.
29. Rudolph, M. C., McManaman, J. L., Hunter, L., Phang, T. and Neville, M. C. (2003). Functional development of the mammary gland: use of expression profiling and trajectory clustering to reveal changes in gene expression during pregnancy, lactation, and involution. J. Mammary Gland Biol. Neoplasia 8, 287-307.
30. Rudolph, M. C., Neville, M. C. and Anderson, S. M. (2007). Lipid synthesis in lactation: diet and the fatty acid switch. J. Mammary Gland Biol. Neoplasia 12, 269-281.
31. Russell, T. D., Fischer, A., Beeman, N. E., Freed, E. F., Neville, M. C. and Schaack, J. (2003). Transduction of the mammary epithelium with adenovirus vectors in vivo. 77, 5801-5809.
32. Russell, T. D., Palmer, C. A., Orlicky, D. J., Fischer, A., Rudolph, M. C., Neville, M. C. and McManaman, J. L. (2007). Cytoplasmic lipid droplet accumulation in developing mammary epithelial cells: roles of adipophilin and lipid metabolism. J. Lipid Res. 48, 1463-1475.
33. Russell, T. D., Palmer, C. A., Orlicky, D. J., Bales, E. S., Chang, B. H., Chan, L. and McManaman, J. L. (2008). Mammary glands of adipophilin-null mice produce an amino-terminally truncated form of adipophilin that mediates milk lipid droplet formation and secretion. J. Lipid Res. 49, 206-216.
34. Schwertfeger, K. L., McManaman, J. L., Palmer, C. A., Neville, M. C. and Anderson, S. M. (2003). Expression of constitutively activated Akt in the mammary gland leads to excess lipid synthesis during pregnancy and lactation. J. Lipid Res. 44, 1100-1112.
35. Smirnova, E., Goldberg, E. B., Makarova, K. S., Lin, L., Brown, W. J. and Jackson, C. L. (2006). ATGL has a key role in lipid droplet/adiposome degradation in mammalian cells. EMBO Rep. 7, 106-113.
36. Tansey, J. T., Sztalryd, C., Gruia-Gray, J., Roush, D. L., Zee, J. V., Gavrilova, O., Reitman, M. L., Deng, C. X., Li, C., Kimmel, A. R. et al. (2001). Perilipin ablation results in a lean mouse with aberrant adipocyte lipolysis, enhanced leptin production, and resistance to diet-induced obesity. Proc. Natl. Acad. Sci. USA 98, 6494-6499.
37. Wagner, K. U., Boulanger, C. A., Henry, M. D., Sgagias, M., Hennighausen, L. and Smith, G. H. (2002). An adjunct mammary epithelial cell population in parous females: its role in functional adaptation and tissue renewal. Development 129, 1377-1386.
38. Zechner, R., Kienesberger, P. C., Haemmerle, G., Zimmermann, R. and Lass, A. (2009). Adipose triglyceride lipase and the lipolytic catabolism of cellular fat stores. J. Lipid Res. 50, 3-21.
39. Zimmermann, R., Lass, A., Haemmerle, G. and Zechner, R. (2009). Fate of fat: the role of adipose triglyceride lipase in lipolysis. Biochim. Biophys. Acta 1791, 494-500.