SREBP-2-deficient and hypomorphic mice reveal roles for SREBP-2 in embryonic development and SREBP-1c expression

Journal of Lipid Research

Volumn 57, Issue 3, 2016, Pages 410-421

  Vergnes, Laurent ^a   Chin, Robert G ^a   De Vallim, Thomas Aguiar ^b   Fong, Loren G ^b   Osborne, Timothy F ^c   Young, Stephen G ^a,b   Reue, Karen ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c BURNHAM INSTITUTE   (United States)

Author keywords

Cholesterol synthesis; Gene regulation; Sterol regulatory element binding protein 1c; Sterol regulatory element binding protein 2

Indexed keywords

CHOLESTEROL; MESSENGER RNA; STEROL REGULATORY ELEMENT BINDING PROTEIN 1A; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; STEROL REGULATORY ELEMENT BINDING PROTEIN 2; STEROL REGULATORY ELEMENT BINDING PROTEIN 1;

ADIPOSE TISSUE; ADULT; ALLELE; ALOPECIA; ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CAUSE OF DEATH; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; DEVELOPMENTAL STAGE; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; GENE EXPRESSION; GENE INACTIVATION; GENE MUTATION; GENE TARGETING; HISTOLOGY; HOMEOSTASIS; HYPOMORPHIC MOUSE; LIMB DEVELOPMENT; LIPID LIVER LEVEL; LIPID STORAGE; LIVER; MALE; MORPHOGENESIS; MOUSE; MOUSE MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SREBP 2 DEFICIENT MOUSE; SURVIVAL TIME; WEIGHT REDUCTION; ANIMAL; CELL LINE; DEFICIENCY; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; LIMB; LIPID METABOLISM; METABOLISM; MUTATION; OBESITY; SEXUAL DEVELOPMENT; TISSUE SURVIVAL;

ADIPOSE TISSUE; ADIPOSITY; ALLELES; ANIMALS; CELL LINE; EMBRYONIC DEVELOPMENT; EXTREMITIES; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEOSTASIS; LIPID METABOLISM; LIVER; MALE; MICE; MUTATION; SEX CHARACTERISTICS; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; STEROL REGULATORY ELEMENT BINDING PROTEIN 2; TISSUE SURVIVAL;

EID: 84964460015     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M064022     Document Type: Article

References (48)

1. Lingwood , D. , and K. Simons . 2010 . Lipid rafts as a membraneorganizing principle. Science . 327 : 46 - 50 .
2. Maxfield , F. R. , and G. van Meer . 2010 . Cholesterol, the central lipid of mammalian cells. Curr. Opin. Cell Biol. 22 : 422 - 429 .
3. Horton , J. D. , J. L. Goldstein , and M. S. Brown . 2002 . SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J. Clin. Invest. 109 : 1125 - 1131 .
4. Jeon , T-I. , and T. F. Osborne . 2012 . SREBPs: metabolic integrators in physiology and metabolism. Trends Endocrinol. Metab. 23 : 65 - 72 .
5. Ye , J. , and R. A. DeBose-Boyd . 2011 . Regulation of cholesterol and fatty acid synthesis. Cold Spring Harb. Perspect. Biol. 3 : a004754 .
6. Pai , J. T. , O. Guryev , M. S. Brown , and J. L. Goldstein . 1998 . Differential stimulation of cholesterol and unsaturated fatty acid biosynthesis in cells expressing individual nuclear sterol regulatory element-binding proteins. J. Biol. Chem. 273 : 26138 - 26148 .
7. Horton , J. D. , N. A. Shah , J. A. Warrington , N. N. Anderson , S. W. Park , M. S. Brown , and J. L. Goldstein . 2003 . Combined analysis of oligonucleotide microarray data from transgenic and knockout mice identifies direct SREBP target genes. Proc. Natl. Acad. Sci. USA . 100 : 12027 - 12032 .
8. McPherson , R. , and A. Gauthier . 2004 . Molecular regulation of SREBP function: the Insig-SCAP connection and isoform-specific modulation of lipid synthesis. Biochem. Cell Biol. 82 : 201 - 211 .
9. Shimano , H. , J. D. Horton , I. Shimomura , R. E. Hammer , M. S. Brown , and J. L. Goldstein . 1997 . Isoform 1c of sterol regulatory element binding protein is less active than isoform 1a in livers of transgenic mice and in cultured cells. J. Clin. Invest. 99 : 846 - 854 .
10. Goldstein , J. L. , R. A. DeBose-Boyd , and M. S. Brown . 2006 . Protein sensors for membrane sterols. Cell . 124 : 35 - 46 .
11. Goldstein , J. L. , and M. S. Brown . 2015 . A century of cholesterol and coronaries: from plaques to genes to statins. Cell . 161 : 161 - 172 .
12. Horton J.D. , ShimomuraI. , BrownM.S. , HammerR.E. , GoldsteinJ.L. , H. Shimano1998 . Activation of cholesterol synthesis in preference to fatty acid synthesis in liver and adipose tissue of transgenic mice overproducing sterol regulatory element-binding protein-2J. Clin. Invest.101 : 2331-2339
13. Shimano , H. , J. D. Horton , R. E. Hammer , I. Shimomura , M. S. Brown , and J. L. Goldstein . 1996 . Overproduction of cholesterol and fatty acids causes massive liver enlargement in transgenic mice expressing truncated SREBP-1a. J. Clin. Invest. 98 : 1575 - 1584 .
14. Shimano , H. , I. Shimomura , R. E. Hammer , J. Herz , J. L. Goldstein , M. S. Brown , and J. D. Horton . 1997 . Elevated levels of SREBP-2 and cholesterol synthesis in livers of mice homozygous for a targeted disruption of the SREBP-1 gene. J. Clin. Invest. 100 : 2115 - 2124 .
15. Yang , J. , J. L. Goldstein , R. E. Hammer , Y. A. Moon , M. S. Brown , and J. D. Horton . 2001 . Decreased lipid synthesis in livers of mice with disrupted Site-1 protease gene. Proc. Natl. Acad. Sci. USA . 98 : 13607 - 13612 .
16. Matsuda , M. , B. S. Korn , R. E. Hammer , Y. A. Moon , R. Komuro , J. D. Horton , J. L. Goldstein , M. S. Brown , and I. Shimomura . 2001 . 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 .
17. Chevy F. , IllienF. , WolfC. , C. Roux .2002 . Limb malformations of rat fetuses exposed to a distal inhibitor of cholesterol biosynthesisJ. Lipid Res.43 : 1192-1200
18. Gofflot , F. , C. Hars , F. Illien , F. Chevy , C. Wolf , J. J. Picard , and C. Roux . 2003 . Molecular mechanisms underlying limb anomalies associated with cholesterol deficiency during gestation: implications of Hedgehog signaling. Hum. Mol. Genet. 12 : 1187 - 1198 .
19. Porter , J. A. , K. E. Young , and P. A. Beachy . 1996 . Cholesterol modification of hedgehog signaling proteins in animal development. Science . 274 : 255 - 259 .
20. Kanungo , S. , N. Soares , M. He , and R. D. Steiner . 2013 . Sterol metabolism disorders and neurodevelopment-an update. Dev. Disabil. Res. Rev. 17 : 197 - 210 .
21. Nord , A. S. , P. J. Chang , B. R. Conklin , A. V. Cox , C. A. Harper , G. G. Hicks , C. C. Huang , S. J. Johns , M. Kawamoto , S. Liu , et al . 2006 . The International Gene Trap Consortium Website: a portal to all publicly available gene trap cell lines in mouse. Nucleic Acids Res. 34 : D642 - D648 .
22. Stryke , D. , M. Kawamoto , C. C. Huang , S. J. Johns , L. A. King , C. A. Harper , E. C. Meng , R. E. Lee , A. Yee , L. L'Italien , et al . 2003 . BayGenomics: a resource of insertional mutations in mouse embryonic stem cells. Nucleic Acids Res. 31 : 278 - 281 .
23. Tang , S-H. E. , F. J. Silva , W. M. K. Tsark , and J. R. Mann . 2002 . A Cre/loxP-deleter transgenic line in mouse strain 129S1/SvImJ. Genesis . 32 : 199 - 202 .
24. Vergnes L. , BeigneuxA.P. , DavisR. , WatkinsS.M. , YoungS.G. , K. Reue .2006 . Agpat6 deficiency causes subdermal lipodystrophy and resistance to obesityJ. Lipid Res.47 : 745-754
25. BeigneuxA.P. VergnesL. QiaoX. QuatelaS. DavisR. WatkinsS.M. ColemanR.A. WalzemR.L. PhilipsM. ReueK.et al.2006Agpat6-a novel lipid biosynthetic gene required for triacylglycerol production in mammary epitheliumJ. Lipid Res.47734-744
26. Zakin , L. , and E. M. De Robertis . 2004 . Inactivation of mouse Twisted gastrulation reveals its role in promoting Bmp4 activity during forebrain development. Development . 131 : 413 - 424 .
27. Zakin , L. , B. Reversade , H. Kuroda , K. M. Lyons , and E. M. De Robertis . 2005 . Sirenomelia in Bmp7 and Tsg compound mutant mice: requirement for Bmp signaling in the development of ventral posterior mesoderm. Development . 132 : 2489 - 2499 .
28. Solloway , M. J. , A. T. Dudley , E. K. Bikoff , K. M. Lyons , B. L. Hogan , and E. J. Robertson . 1998 . Mice lacking Bmp6 function. Dev. Genet. 22 : 321 - 339 .
29. Seo , Y-K. , T-I. Jeon , H. K. Chong , J. Biesinger , X. Xie , and T. F. Osborne . 2011 . Genome-wide localization of SREBP-2 in hepatic chromatin predicts a role in autophagy. Cell Metab. 13 : 367 - 375 .
30. Capdevila , J. , and J. C. Izpisúa Belmonte . 2001 . Patterning mechanisms controlling vertebrate limb development. Annu. Rev. Cell Dev. Biol. 17 : 87 - 132 .
31. Bénazet , J-D. , and R. Zeller . 2009 . Vertebrate limb development: moving from classical morphogen gradients to an integrated 4-dimensional patterning system. Cold Spring Harb. Perspect. Biol. 1 : a001339 .
32. Cohen , M. M. 2003 . The hedgehog signaling network. Am. J. Med. Genet. A. 123A : 5 - 28 .
33. McGlinn , E. , and C. J. Tabin . 2006 . Mechanistic insight into how Shh patterns the vertebrate limb. Curr. Opin. Genet. Dev. 16 : 426 - 432 .
34. Zúñiga , A. , A. P. Haramis , A. P. McMahon , and R. Zeller . 1999 . Signal relay by BMP antagonism controls the SHH/FGF4 feedback loop in vertebrate limb buds. Nature . 401 : 598 - 602 .
35. Verheyden , J. M. , and X. Sun . 2008 . An Fgf/Gremlin inhibitory feedback loop triggers termination of limb bud outgrowth. Nature . 454 : 638 - 641 .
36. Bastida , M. F. , R. Sheth , and M. A. Ros . 2009 . A BMP-Shh negativefeedback loop restricts Shh expression during limb development. Development . 136 : 3779 - 3789 .
37. SatoR. InoueJ. KawabeY. KodamaT. TakanoT. M. Maeda1996Sterol-dependent transcriptional regulation of sterol regulatory element-binding protein-2J. Biol. Chem.27126461-26464
38. Amemiya-KudoM. ShimanoH. YoshikawaT. YahagiN. HastyA.H. OkazakiH. TamuraY. ShionoiriF. IizukaY. OhashiK.et al.2000Promoter analysis of the mouse sterol regulatory element-binding protein-1c geneJ. Biol. Chem.27531078-31085
39. Merath , K. M. , B. Chang , R. Dubielzig , R. Jeannotte , and D. J. Sidjanin . 2011 . A spontaneous mutation in Srebf2 leads to cataracts and persistent skin wounds in the lens opacity 13 (lop13) mouse. Mamm. Genome . 22 : 661 - 673 .
40. Laubner , D. , R. Breitling , and J. Adamski . 2003 . Embryonic expression of cholesterogenic genes is restricted to distinct domains and colocalizes with apoptotic regions in mice. Brain Res. Mol. Brain Res. 115 : 87 - 92 .
41. Rahnama , F. , R. Toftgård , and P. G. Zaphiropoulos . 2004 . Distinct roles of PTCH2 splice variants in Hedgehog signalling. Biochem. J. 378 : 325 - 334 .
42. Marquart , T. J. , R. M. Allen , D. S. Ory , and A. Baldán . 2010 . miR-33 links SREBP-2 induction to repression of sterol transporters. Proc. Natl. Acad. Sci. USA . 107 : 12228 - 12232 .
43. Rayner , K. J. , Y. Suárez , A. Dávalos , S. Parathath , M. L. Fitzgerald , N. Tamehiro , E. A. Fisher , K. J. Moore , and C. Fernández-Hernando . 2010 . MiR-33 contributes to the regulation of cholesterol homeostasis. Science . 328 : 1570 - 1573 .
44. Najafi-Shoushtari , S. H. , F. Kristo , Y. Li , T. Shioda , D. E. Cohen , R. E. Gerszten , and A. M. Näär . 2010 . MicroRNA-33 and the SREBP host genes cooperate to control cholesterol homeostasis. Science . 328 : 1566 - 1569 .
45. Tarling , E. J. , H. Ahn , and T. Q. de Aguiar Vallim . 2015 . The nuclear receptor FXR uncouples the actions of miR-33 from SREBP-2. Arterioscler. Thromb. Vasc. Biol. 35 : 787 - 795 .
46. RaynerK.J. SheedyF.J. EsauC.C. HussainF.N. TemelR.E. ParathathS. GilsJ.M.V. RaynerA.J. ChangA.N. SuarezY.et al.2011Antagonism of miR-33 in mice promotes reverse cholesterol transport and regression of atherosclerosisJ. Clin. Invest.1212921-2931
47. Horie T. , BabaO. , KuwabaraY. , ChujoY. , WatanabeS. , KinoshitaM. , HoriguchiM. , NakamuraT. , ChonabayashiK. , HishizawaM. , et al. . 2012 . MicroRNA-33 deficiency reduces the progression of atherosclerotic plaque in ApoE - / - miceJ. Am. Heart Assoc.1 : e003376
48. Horie , T. , T. Nishino , O. Baba , Y. Kuwabara , T. Nakao , M. Nishiga , S. Usami , M. Izuhara , N. Sowa , N. Yahagi , et al . 2013 . MicroRNA-33 regulates sterol regulatory element-binding protein 1 expression in mice. Nat. Commun. 4 : 2883 .