Overexpression of SREBP1 (sterol regulatory element binding protein 1) promotes de novo fatty acid synthesis and triacylglycerol accumulation in goat mammary epithelial cells

Journal of Dairy Science

Volumn 99, Issue 1, 2016, Pages 783-795

  Xu, H F ^a   Luo, J ^a   Zhao, W S ^a   Yang, Y C ^a   Tian, H B ^a   Shi, H B ^a   Bionaz, M ^b  

^a NORTHWEST A F UNIVERSITY   (China)

^b OREGON STATE UNIVERSITY   (United States)

Author keywords

Adenovirus; Goat; Milk fat synthesis; Sterol regulatory element binding protein 1 (SREBP1)

Indexed keywords

ACYL COENZYME A DESATURASE; COENZYME A LIGASE; FATTY ACID; FATTY ACID BINDING PROTEIN; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; TRIACYLGLYCEROL;

ADIPOGENESIS; ANIMAL; BIOSYNTHESIS; EPITHELIUM CELL; FEMALE; GENE EXPRESSION REGULATION; GENETICS; GOAT; HEK293 CELL LINE; HUMAN; METABOLISM; UDDER;

ADIPOGENESIS; ANIMALS; COENZYME A LIGASES; EPITHELIAL CELLS; FATTY ACID-BINDING PROTEINS; FATTY ACIDS; FEMALE; GENE EXPRESSION REGULATION; GOATS; HEK293 CELLS; HUMANS; MAMMARY GLANDS, ANIMAL; STEAROYL-COA DESATURASE; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; TRIGLYCERIDES;

EID: 84952716814     PISSN: 00220302     EISSN: 15253198     Source Type: Journal    
DOI: 10.3168/jds.2015-9736     Document Type: Article

References (62)

1. Amemiya-Kudo M., Shimano H., Yoshikawa T., Yahagi N., Hasty A.H., Okazaki H., Tamura Y., Shionoiri F., Iizuka Y., Ohashi K., Osuga J., Harada K., Gotoda T., Sato R., Kimura S., Ishibashi S., Yamada N. Promoter analysis of the mouse sterol regulatory element-binding protein-1c gene. J. Biol. Chem. 2000, 275:31078-31085.
2. Barber M.C., Vallance A.J., Kennedy H.T., Travers M.T. Induction of transcripts derived from promoter III of the acetyl-CoA carboxylase-alpha gene in mammary gland is associated with recruitment of SREBP-1 to a region of the proximal promoter defined by a DNase I hypersensitive site. Biochem. J. 2003, 375:489-501.
3. Bauman D.E., Mather I.H., Wall R.J., Lock A.L. Major advances associated with the biosynthesis of milk. J. Dairy Sci. 2006, 89:1235-1243.
4. Bauman D.E., Perfield J.W., Harvatine K.J., Baumgard L.H. Regulation of fat synthesis by conjugated linoleic acid: Lactation and the ruminant model. J. Nutr. 2008, 138:403-409.
5. Bionaz M., Chen S., Khan M.J., Loor J.J. Functional role of PPARs in ruminants: Potential targets for fine-tuning metabolism during growth and lactation. PPAR Res. 2013, 2013:684159.
6. Bionaz M., Loor J.J. Identification of reference genes for quantitative real-time PCR in the bovine mammary gland during the lactation cycle. Physiol. Genomics 2007, 29:312-319.
7. Bionaz M., Loor J.J. ACSL1, AGPAT6, FABP3, LPIN1, and SLC27A6 are the most abundant isoforms in bovine mammary tissue and their expression is affected by stage of lactation. J. Nutr. 2008, 138:1019-1024. a.
8. Bionaz M., Loor J.J. Gene networks driving bovine milk fat synthesis during the lactation cycle. BMC Genomics 2008, 9:366. b.
9. Bionaz M., Thering B.J., Loor J.J. Fine metabolic regulation in ruminants via nutrient-gene interactions: Saturated long-chain fatty acids increase expression of genes involved in lipid metabolism and immune response partly through PPAR-alpha activation. Br. J. Nutr. 2012, 107:179-191.
10. Briggs M.R., Yokoyama C., Wang X., Brown M.S., Goldstein J.L. Nuclear protein that binds sterol regulatory element of low density lipoprotein receptor promoter. I. Identification of the protein and delineation of its target nucleotide sequence. J. Biol. Chem. 1993, 268:14490-14496.
11. Brown M.S., Goldstein J.L. The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell 1997, 89:331-340.
12. Carcangiu V., Mura M.C., Daga C., Luridiana S., Bodano S., Sanna G.A., Diaz M.L., Cosso G. Association between SREBP-1 gene expression in mammary gland and milk fat yield in Sarda breed sheep. Meta Gene 2013, 1:43-49.
13. Chen I.B., Rathi V.K., DeAndrade D.S., Jay P.Y. Association of genes with physiological functions by comparative analysis of pooled expression microarray data. Physiol. Genomics 2013, 45:69-78.
14. Chypre M., Zaidi N., Smans K. ATP-citrate lyase: A mini-review. Biochem. Biophys. Res. Commun. 2012, 422:1-4.
15. Clegg R.A., Barber M.C., Pooley L., Ernens I., Larondelle Y., Travers M.T. Milk fat synthesis and secretion: molecular and cellular aspects. Livest. Prod. Sci. 2001, 70:3-14.
16. Desvergne B., Michalik L., Wahli W. Transcriptional regulation of metabolism. Physiol. Rev. 2006, 86:465-514.
17. Eberlé D., Hegarty B., Bossard P., Ferre P., Foufelle F. SREBP transcription factors: Master regulators of lipid homeostasis. Biochimie 2004, 86:839-848.
18. Espenshade P.J. SREBPs: Sterol-regulated transcription factors. J. Cell Sci. 2006, 119:973-976.
19. Hardwick D.C. The fate of acetyl groups derived from glucose in the isolated perfused goat udder. Biochem. J. 1966, 99:228-231.
20. Harvatine K.J., Bauman D.E. 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. 2006, 136:2468-2474.
21. Harvatine K.J., Boisclair Y.R., Bauman D.E. Recent advances in the regulation of milk fat synthesis. Animal 2009, 3:40-54.
22. Hatzivassiliou G., Zhao F., Bauer D.E., Andreadis C., Shaw A.N., Dhanak D., Hingorani S.R., Tuveson D.A., Thompson C.B. ATP citrate lyase inhibition can suppress tumor cell growth. Cancer Cell 2005, 8:311-321.
23. He T.C., Zhou S., da Costa L.T., Yu J., Kinzler K.W., Vogelstein B. A simplified system for generating recombinant adenoviruses. Proc. Natl. Acad. Sci. USA 1998, 95:2509-2514.
24. Horton J.D. Sterol regulatory element-binding proteins: Transcriptional activators of lipid synthesis. Biochem. Soc. Trans. 2002, 30:1091-1095.
25. Horton J.D., Shah N.A., Warrington J.A., Anderson N.N., Park S.W., Brown M.S., Goldstein J.L. Combined analysis of oligonucleotide microarray data from transgenic and knockout mice identifies direct SREBP target genes. Proc. Natl. Acad. Sci. USA 2003, 100:12027-12032.
26. Ishimoto K., Nakamura H., Tachibana K., Yamasaki D., Ota A., Hirano K., Tanaka T., Hamakubo T., Sakai J., Kodama T., Doi T. Sterol-mediated regulation of human lipin 1 gene expression in hepatoblastoma cells. J. Biol. Chem. 2009, 284:22195-22205.
27. Jakobsson A., Westerberg R., Jacobsson A. Fatty acid elongases in mammals: Their regulation and roles in metabolism. Prog. Lipid Res. 2006, 45:237-249.
28. Kadegowda A.K., Bionaz M., Piperova L.S., Erdman R.A., Loor J.J. Peroxisome proliferator-activated receptor-gamma activation and long-chain fatty acids alter lipogenic gene networks in bovine mammary epithelial cells to various extents. J. Dairy Sci. 2009, 92:4276-4289.
29. Lee C., Huang C.H. LASAGNA: A novel algorithm for transcription factor binding site alignment. BMC Bioinformatics 2013, 14:108.
30. Lengi A.J., Corl B.A. Short communication: Identification of the bovine sterol regulatory element binding protein-1c promoter and its activation by liver X receptor. J. Dairy Sci. 2010, 93:5831-5836.
31. Li J., Luo J., Xu H., Wang M., Zhu J., Shi H., Haile A.B., Wang H., Sun Y. Fatty acid synthase promoter: Characterization, and transcriptional regulation by sterol regulatory element binding protein-1 in goat mammary epithelial cells. Gene 2015, 561:157-164.
32. Li N., Zhao F., Wei C., Liang M., Zhang N., Wang C., Li Q.Z., Gao X.J. Function of SREBP1 in the milk fat synthesis of dairy cow mammary epithelial cells. Int. J. Mol. Sci. 2014, 15:16998-17013. a.
33. Li X., Li Y., Yang W., Xiao C., Fu S., Deng Q., Ding H., Wang Z., Liu G., Li X. SREBP-1c overexpression induces triglycerides accumulation through increasing lipid synthesis and decreasing lipid oxidation and VLDL assembly in bovine hepatocytes. J. Steroid Biochem. Mol. Biol. 2014, 143:174-182. b.
34. Lin X.Z., Luo J., Zhang L.P., Wang W., Shi H.B., Zhu J.J. MiR-27a suppresses triglyceride accumulation and affects gene mRNA expression associated with fat metabolism in dairy goat mammary gland epithelial cells. Gene 2013, 521:15-23.
35. Luong A., Hannah V.C., Brown M.S., Goldstein J.L. Molecular characterization of human acetyl-CoA synthetase, an enzyme regulated by sterol regulatory element-binding proteins. J. Biol. Chem. 2000, 275:26458-26466.
36. Ma L., Corl B.A. Transcriptional regulation of lipid synthesis in bovine mammary epithelial cells by sterol regulatory element binding protein-1. J. Dairy Sci. 2012, 95:3743-3755.
37. Mashima T., Seimiya H., Tsuruo T. De novo fatty-acid synthesis and related pathways as molecular targets for cancer therapy. Br. J. Cancer 2009, 100:1369-1372.
38. Matsuda M., Korn B.S., Hammer R.E., Moon Y.A., Komuro R., Horton J.D., Goldstein J.L., Brown M.S., Shimomura I. SREBP cleavage-activating protein (SCAP) is required for increased lipid synthesis in liver induced by cholesterol deprivation and insulin elevation. Genes Dev. 2001, 15:1206-1216.
39. Maxwell K.N., Soccio R.E., Duncan E.M., Sehayek E., Breslow J.L. Novel putative SREBP and LXR target genes identified by microarray analysis in liver of cholesterol-fed mice. J. Lipid Res. 2003, 44:2109-2119.
40. McFadden J.W., Corl B.A. Activation of liver X receptor (LXR) enhances de novo fatty acid synthesis in bovine mammary epithelial cells. J. Dairy Sci. 2010, 93:4651-4658.
41. Moore J.H., Christie W.W. Lipid metabolism in the mammary gland of ruminant animals. Prog. Lipid Res. 1979, 17:347-395.
42. Nohturfft A., Brown M.S., Goldstein J.L. Topology of SREBP cleavage-activating protein, a polytopic membrane protein with a sterol-sensing domain. J. Biol. Chem. 1998, 273:17243-17250.
43. Oppi-Williams C., Suagee J.K., Corl B.A. Regulation of lipid synthesis by liver X receptor alpha and sterol regulatory element-binding protein 1 in mammary epithelial cells. J. Dairy Sci. 2013, 96:112-121.
44. Peterson D.G., Matitashvili E.A., Bauman D.E. The inhibitory effect of trans-10, cis-12 CLA on lipid synthesis in bovine mammary epithelial cells involves reduced proteolytic activation of the transcription factor SREBP-1. J. Nutr. 2004, 134:2523-2527.
45. Peterson T.R., Sengupta S.S., Harris T.E., Carmack A.E., Kang S.A., Balderas E., Guertin D.A., Madden K.L., Carpenter A.E., Finck B.N., Sabatini D.M. mTOR complex 1 regulates lipin 1 localization to control the SREBP pathway. Cell 2011, 146:408-420.
46. Radhakrishnan A., Ikeda Y., Kwon H.J., Brown M.S., Goldstein J.L. Sterol-regulated transport of SREBPs from endoplasmic reticulum to Golgi: Oxysterols block transport by binding to Insig. Proc. Natl. Acad. Sci. USA 2007, 104:6511-6518.
47. Ramakers C., Ruijter J.M., Deprez R.H.L., Moorman A.F.M. Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci. Lett. 2003, 339:62-66.
48. Rudolph M.C., Monks J., Burns V., Phistry M., Marians R., Foote M.R., Bauman D.E., Anderson S.M., Neville M.C. Sterol regulatory element binding protein and dietary lipid regulation of fatty acid synthesis in the mammary epithelium. Am. J. Physiol. Endocrinol. Metab. 2010, 299:E918-E927.
49. Sato R. Sterol metabolism and SREBP activation. Arch. Biochem. Biophys. 2010, 501:177-181.
50. Shi H., Luo J., Zhu J., Li J., Sun Y., Lin X., Zhang L., Yao D., Shi H. PPAR gamma regulates genes involved in triacylglycerol synthesis and secretion in mammary gland epithelial cells of dairy goats. PPAR Res. 2013, 2013:310948. a.
51. Shi H.B., Luo J., Yao D.W., Zhu J.J., Xu H.F., Shi H.P., Loor J.J. Peroxisome proliferator-activated receptor-gamma stimulates the synthesis of monounsaturated fatty acids in dairy goat mammary epithelial cells via the control of stearoyl-coenzyme A desaturase. J. Dairy Sci. 2013, 96:7844-7853. b.
52. Shi H.B., Zhao W.S., Luo J., Yao D.W., Sun Y.T., Li J., Shi H.P., Loor J.J. Peroxisome proliferator-activated receptor gamma1 and gamma2 isoforms alter lipogenic gene networks in goat mammary epithelial cells to different extents. J. Dairy Sci. 2014, 97:5437-5447.
53. Tontonoz P., Kim J.B., Graves R.A., Spiegelman B.M. ADD1: A novel helix-loop-helix transcription factor associated with adipocyte determination and differentiation. Mol. Cell. Biol. 1993, 13:4753-4759.
54. van Dorland H.A., Richter S., Morel I., Doherr M.G., Castro N., Bruckmaier R.M. Variation in hepatic regulation of metabolism during the dry period and in early lactation in dairy cows. J. Dairy Sci. 2009, 92:1924-1940.
55. Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A., Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002, 3. RESEARCH0034.
56. Wang W., Luo J., Zhong Y., Lin X.Z., Shi H.B., Zhu J.J., Li J., Sun Y.T., Zhao W.S. Goat liver X receptor alpha, molecular cloning, functional characterization and regulating fatty acid synthesis in epithelial cells of goat mammary glands. Gene 2012, 505:114-120.
57. Wang X., Briggs M.R., Hua X., Yokoyama C., Goldstein J.L., Brown M.S. Nuclear protein that binds sterol regulatory element of low density lipoprotein receptor promoter. II. Purification and characterization. J. Biol. Chem. 1993, 268:14497-14504.
58. Wang Y., Botolin D., Xu J., Christian B., Mitchell E., Jayaprakasam B., Nair M.G., Peters J.M., Busik J.V., Olson L.K., Jump D.B. Regulation of hepatic fatty acid elongase and desaturase expression in diabetes and obesity. J. Lipid Res. 2006, 47:2028-2041.
59. Yang T., Espenshade P.J., Wright M.E., Yabe D., Gong Y., Aebersold R., Goldstein J.L., Brown M.S. Crucial step in cholesterol homeostasis: Sterols promote binding of SCAP to INSIG-1, a membrane protein that facilitates retention of SREBPs in ER. Cell 2002, 110:489-500.
60. Yokoyama C., Wang X.D., Briggs M.R., Admon A., Wu J., Hua X.X., Goldstein J.L., Brown M.S. Srebp-1, a basic-helix-loop-helix-leucine zipper protein that controls transcription of the low density lipoprotein receptor gene. Cell 1993, 75:187-197.
61. Yoshii Y., Furukawa T., Yoshii H., Mori T., Kiyono Y., Waki A., Kobayashi M., Tsujikawa T., Kudo T., Okazawa H., Yonekura Y., Fujibayashi Y. Cytosolic acetyl-CoA synthetase affected tumor cell survival under hypoxia: The possible function in tumor acetyl-CoA/acetate metabolism. Cancer Sci. 2009, 100:821-827.
62. Zhao W., Bionaz M., Luo J., Hosseini A., Loor J.J. Long chain fatty acids alter expression of genes involved in lipid metabolism in goat mammary epithelial cells partly through PPAR-gamma. J. Dairy Sci. 2014, 97(E-Suppl. 1):321. (Abstr.).