Sterol regulatory element binding protein and dietary lipid regulation of fatty acid synthesis in the mammary epithelium

American Journal of Physiology - Endocrinology and Metabolism

Volumn 299, Issue 6, 2010, Pages

  Rudolph, Michael C ^a   Monks, Jenifer ^a   Burns, Valerie ^a   Phistry, Meridee ^a   Marians, Russell ^a   Foote, Monica R ^b   Bauman, Dale E ^b   Anderson, Steven M ^a   Neville, Margaret C ^a  

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

^b Department of Molecular Biology and Genetics   (United States)

Author keywords

Lactation; Milk triglyceride; Sterol regulatory element binding transcription factor 1 cleavage activating protein

Indexed keywords

ACYL COENZYME A DESATURASE; ACYL COENZYME A DESATURASE 2; ADENOSINE TRIPHOSPHATE CITRATE LYASE; FATTY ACID; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MESSENGER RNA; STEROL REGULATORY ELEMENT BINDING PROTEIN; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; STEROL REGULATORY ELEMENT BINDING PROTEIN 1A; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BREAST EPITHELIUM; FATTY ACID SYNTHESIS; FEMALE; GENE; INSULIN INDUCED GENE 1; LACTATION; LIPID DIET; LIPOGENESIS; MOUSE; NONHUMAN; PHOSPHOLIPID SYNTHESIS; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION;

ANIMALS; BLOTTING, WESTERN; DIETARY FATS; FATTY ACIDS; FEMALE; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LACTATION; LIPOGENESIS; MAMMARY GLANDS, ANIMAL; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MILK; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STEROL REGULATORY ELEMENT BINDING PROTEIN 1;

EID: 78649643401     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00376.2010     Document Type: Article

References (46)

1. Abraham S, Chaikoff IL. Glycolytic pathways and lipogenesis in mammary glands of lactating and nonlactating normal rats. J Biol Chem 234: 2246-2253, 1959.
2. Anderson SM, Rudolph MC, McManaman JL, Neville MC. 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, 2007.
3. Avril-Sassen S, Goldstein LD, Stingl J, Blenkiron C, Le Quesne J, Spiteri I, Karagavriilidou K, Watson CJ, Tavare S, Miska EA, Caldas C. Characterisation of microRNA expression in post-natal mouse mammary gland development. BMC Genomics 10: 548, 2009.
4. Bauman DE, Davis CL. Biosynthesis of milk fat. In: Lactation, edited by Larson B. New York: Academic, 1974, p. 32-75.
5. Brown MS, Goldstein JL. The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell 89: 331-340, 1997.
6. Damiano F, Gnoni GV, Siculella L. Functional analysis of rat liver citrate carrier promoter: differential responsiveness to polyunsaturated fatty acids. Biochem J 417: 561-571, 2009.
7. Daniel S, Kim KH. Sp1 mediates glucose activation of the acetyl-CoA carboxylase promoter. J Biol Chem 271: 1385-1392, 1996. (Pubitemid 26028620)
8. Esau C, Davis S, Murray SF, Yu XX, Pandey SK, Pear M, Watts L, Booten SL, Graham M, McKay R, Subramaniam A, Propp S, Lollo BA, Freier S, Bennett CF, Bhanot S, Monia BP. miR-122 regulation of lipid metabolism revealed by in vivo antisense targeting. Cell Metab 3: 87-98, 2006.
9. Foretz M, Guichard C, Ferré P, Foufelle F. Sterol regulatory element binding protein-1c is a major mediator of insulin action on the hepatic expression of glucokinase and lipogenesis-related genes. Proc Natl Acad Sci USA 96: 12727-12742, 2002.
10. Fukuda H, Noguchi T, Iritani N. Transcriptional regulation of fatty acid synthase gene and ATP citrate-lyase gene by Sp1 and Sp3 in rat hepatocytes. FEBS Lett 464: 113-117, 1999.
11. Goldstein JL, DeBose-Boyd RA, Brown MS. Protein sensors for membrane sterols. Cell 124: 35-46, 2006.
12. Griffin MJ, Sul HS. Insulin regulation of fatty acid synthase gene transcription: roles of USF and SREBP-1c. IUBMB Life 56: 595-600, 2004.
13. Hadsell DL, Bonnette S, George J, Torres D, Klementidis Y, Gao S, Haney PM, Summy-Long J, Soloff MS, Parlow AF, Sirito M, Sawadogo M. Diminished milk synthesis in upstream stimulatory factor 2 null mice is associated with decreased circulating oxytocin and decreased mammary gland expression of eukaryotic initiation factors 4E and 4G. Mol Endocrinol 17: 2251-2267, 2003.
14. Hara A, Radin NS. Lipid extraction of tissues with a low-toxicity solvent. Anal Biochem 90: 420-426, 1978.
15. Harvatine KJ, Bauman DE. SREBP1 and thyroid hormone responsive Spot 14 (S14) are involved in the regulation of bovine mammary lipid synthesis during diet-induced milk fat depression and treatment with CLA. J Nutr 136: 2468-2474, 2006.
16. Horton JD, Goldstein JL, Brown MS. SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J Clin Invest 109: 1125-1135, 2002.
17. Horton JD, Shah NA, Warrington JA, Anderson NN, Park SW, Brown MS, Goldstein JL. Combined analysis of oligonucleotide microarray data from transgenic and knockout mice identifies direct SREBP target genes. Proc Natl Acad Sci USA 100: 12027-12032, 2003.
18. Jump DB. N-3 polyunsaturated fatty acid regulation of hepatic gene transcription. Curr Opin Lipidol 19: 242-247, 2008.
19. Kim CW, Moon YA, Park SW, Cheng D, Kwon HJ, Horton JD. Induced polymerization of mammalian acetyl-CoA carboxylase by MIG12 provides a tertiary level of regulation of fatty acid synthesis. Proc Natl Acad Sci USA 107: 9626-9631, 2010.
20. Knight CH, Maltz E, Docherty AH. Milk yield and composition in mice: effects of litter size and lactation number. Comp Biochem Physiol 84: 127-133, 1986.
21. Libertini LJ, Smith S. Purification and properties of a thioesterase from lactating rat mammary gland which modifies the product specificity of fatty acid synthetase. J Biol Chem 253: 1393-1401, 1978.
22. Lin J, Yang R, Tarr PT, Wu PH, Handschin C, Li S, Yang W, Pei L, Uldry M, Tontonoz P, Newgard CB, Spiegelman BM. Hyperlipidemic effects of dietary saturated fats mediated through PGC-1β coactivation of SREBP. Cell 120: 261-273, 2005.
23. Matsuda M, Korn BS, Hammer RE, Moon YA, Komuro R, Horton JD, Goldstein JL, Brown MS, Shimomura I. SREBP cleavage-activating protein (SCAP) is required for increased lipid synthesis in liver induced by cholesterol deprivation and insulin elevation. Genes Dev 15: 1206-1216, 2001.
24. Monks J, Smith-Steinhart C, Kruk ER, Fadok VA, Henson PM. Epithelial cells remove apoptotic epithelial cells during post-lactation involution of the mouse mammary gland. Biol Reprod 78: 586-594, 2008. (Pubitemid 351469341)
25. Munday MR, Williamson DH. Insulin activation of lipogenesis in isolated mammary acini from lactating rats fed a high-fat diet: evidence that acetyl-CoA carboxylase is a site of action. Biochem J 242: 905-911, 1987.
26. Nagai J, Sarkar NK. Relationship between milk yield and mammary gland development in mice. J Dairy Sci 61: 733-739, 1978.
27. Nakajima T, Hamakubo T, Kodama T, Inazawa J, Emi M. Genomic structure and chromosomal mapping of the human sterol regulatory element binding protein (SREBP) cleavage-activating protein (SCAP) gene. J Hum Genet 44: 402-407, 1999.
28. Ntambi JM, Miyazaki M. Regulation of stearoyl-CoA desaturases and role in metabolism. Prog Lipid Res 43: 91-104, 2004.
29. Ordovas L, Roy R, Pampin S, Zaragoza P, Osta R, Rodriguez-Rey JC, Rodellar C. The g.763G>C SNP of the bovine FASN gene affects its promoter activity via Sp-mediated regulation: implications for the bovine lactating mammary gland. Physiol Genomics 34: 144-148, 2008.
30. Osborne TF. Creating a SCAP-less liver keeps SREBPs pinned in the ER membrane and prevents increased lipid synthesis in response to low cholesterol and high insulin. Genes Dev 15: 1873-1878, 2001.
31. 9-desaturase index in dairy cows. J Dairy Sci 89: 2559-2566, 2006.
32. Rudolph M, McManaman JL, Phang T, Russell T, Kominsky DM, Serkova N, Anderson SM, Neville MC. Metabolic regulation in the lactating mammary gland: a lipid synthesizing machine. Physiol Genomics 28: 323-336, 2007.
33. Rudolph MC, McManaman JL, Hunter L, Phang T, Neville MC. 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, 2003.
34. Rudolph MC, Wellberg EA, Anderson SM. Adipose-depleted mammary epithelial cells and organoids. J Mammary Gland Biol Neoplasia 14: 381-386, 2009.
35. Schwertfeger KL, McManaman JL, Palmer CA, Neville MC, Anderson SM. Expression of constitutively activated Akt in the mammary gland leads to excess lipid synthesis during pregnancy and lactation. J Lipid Res 44: 1100-1112, 2003.
36. Sdassi N, Silveri L, Laubier J, Tilly G, Costa J, Layani S, Vilotte JL, Le Provost F. Identification and characterization of new miRNAs cloned from normal mouse mammary gland. BMC Genomics 10: 149, 2009.
37. Sekiya M, Yahagi N, Matsuzaka T, Takeuchi Y, Nakagawa Y, Takahashi H, Okazaki H, Iizuka Y, Ohashi K, Gotoda T, Ishibashi S, Nagai R, Yamazaki T, Kadowaki T, Yamada N, Osuga J, Shimano H. SREBP-1-independent regulation of lipogenic gene expression in adipocytes. J Lipid Res 48: 1581-1591, 2007.
38. Selbert S, Bentley DJ, Melton DW, Rannie D, Lourenco P, Watson CJ, Clarke AR. Efficient BLG-Cre mediated gene deletion in the mammary gland. Transgenic Res 7: 387-396, 1998.
39. Smith S. Mechanism of chain length determination in biosynthesis of milk fatty acids. J Dairy Sci 63: 337-352, 1980.
40. Smith S, Dils R. Factors affecting the chain length of fatty acids synthesized by lactating-rabbit mammary glands. Biochim Biophys Acta 116: 23-40, 1966.
41. Smith S, Gagne HT, Pitelka DR, Abraham S. The effect of dietary fat on lipogenesis in mammary gland and liver from lactating and virgin mice. Biochem J 115: 807-815, 1969.
42. Stein T, Morris JS, Davies CR, Weber-Hall SJ, Duffy M, Heath VJ, Bell AK, Ferrier RK, Sandilands GP, Gusterson B. Involution of the mouse mammary gland is associated with an immune cascade and an acute-phase response, involving LBP, CD14 and STAT3. Breast Cancer Res 6: 75-91, 2004.
43. Teran-Garcia M, Adamson AW, Yu G, Rufo C, Suchankova G, Dreesen TD, Tekle M, Clarke SD, Gettys TW. Polyunsaturated fatty acid suppression of fatty acid synthase (FASN): evidence for dietary modulation of NF-Y binding to the Fasn promoter by SREBP-1c. Biochem J 402: 591-600, 2007.
44. Uyeda K, Yamashita H, Kawaguchi A. Carbohydrate responsive element-binding protein (ChREBP), a key regulator of glucose metabolism and fat storage. Biochem Pharmacol 63: 2075-2080, 2002.
45. Wakil SJ, Abu-Elheiga LA. Fatty acid metabolism: target for metabolic syndrome. J Lipid Res 50 Suppl: S138-S143, 2009.
46. Zhu A, Anderson GW, Mucha GT, Parks EJ, Metkowski JK, Mariash CN. The Spot 14 protein is required for de novo lipid synthesis in the lactating mammary gland. Endocrinology 146: 3343-3350, 2005.