A novel adipose-specific gene deletion model demonstrates potential pitfalls of existing methods

Molecular Endocrinology

Volumn 27, Issue 1, 2013, Pages 127-134

  Mullican, Shannon E ^a   Tomaru, Takuya ^a   Gaddis, Christine A ^a   Peed, Lindsey C ^a   Sundaram, Anand ^a   Lazar, Mitchell A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; HISTONE DEACETYLASE 3;

ADIPOSE TISSUE; ANIMAL TISSUE; ARTICLE; GENE DELETION; GENE EXPRESSION; GENE TARGETING; IN VIVO STUDY; MORTALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION;

ADIPOSE TISSUE; ANIMALS; DISEASE MODELS, ANIMAL; EPIDIDYMIS; FATTY ACID-BINDING PROTEINS; GENE DELETION; GENES, LETHAL; GENETIC ENGINEERING; HISTONE DEACETYLASES; MALE; MICE; MICE, TRANSGENIC; OBESITY; ORGAN SPECIFICITY; PHENOTYPE;

MUS;

EID: 84871750212     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2012-1267     Document Type: Article

References (47)

1. Wang X 2009 Cre transgenic mouse lines. Methods Mol Biol 561: 265-273
2. He W, Barak Y, Hevener A, Olson P, Liao D, Le J, Nelson M, Ong E, Olefsky JM, Evans RM 2003 Adipose-specific peroxisome pro-liferator-activated receptor y knockout causes insulin resistance in fat and liver but not in muscle. Proc Natl Acad Sci USA 100:15712-15717
3. Abel ED, Peroni O, Kim JK, Kim YB, Boss O, Hadro E, Minnemann T, Shulman GI, Kahn BB 2001 Adipose-selective targeting of the GLUT4 gene impairs insulin action in muscle and liver. Nature 409:729-733
4. Barlow C, Schroeder M, Lekstrom-Himes J, Kylefjord H, Deng CX, Wynshaw-Boris A, Spiegelman BM, Xanthopoulos KG 1997 Targeted expression of Cre recombinase to adipose tissue of transgenic mice directs adipose-specific excision of loxP-flanked gene segments. Nucleic Acids Res 25:2543-2545
5. Mao J, Yang T, Gu Z, Heird WC, Finegold MJ, Lee B, Wakil SJ 2009 aP2-Cre-mediated inactivation of acetyl-CoA carboxylase 1 causes growth retardation and reduced lipid accumulation in adipose tissues. Proc Natl Acad Sci USA 106:17576-17581
6. Ellis JM, Li LO, Wu PC, Koves TR, Ilkayeva O, Stevens RD, Wat-kins SM, Muoio DM, Coleman RA 2010 Adipose acyl-CoA syn-thetase-1 (ACSL1) directs fatty acids towards /3-oxidation and is required for cold thermogenesis. Cell Metab 12:53-64
7. Singh R, Xiang Y, Wang Y, Baikati K, Cuervo AM, Luu YK, Tang Y, Pessin JE, Schwartz GJ, Czaja MJ 2009 Autophagy regulates adipose mass and differentiation in mice. J Clin Invest 119:3329-3339
8. Pan D, Fujimoto M, Lopes A, Wang YX 2009 Twist-1 is a PPARA-inducible, negative-feedback regulator of PGC-1a in brown fat metabolism. Cell 137:73-86
9. Yu IC, Lin HY, Liu NC, Wang RS, Sparks JD, Yeh S, Chang C 2008 Hyperleptinemia without obesity in male mice lacking androgen receptor in adipose tissue. Endocrinology 149:2361-2368
10. Hommel A, Hesse D, Völker W, Jaschke A, Moser M, Engel T, Blüher M, Zahn C, Chadt A, Ruschke K, Vogel H, Kluge R, Ro-benek H, Joost HG, Schürmann A 2010 The ARF-like GTPase ARFRP1 is essential for lipid droplet growth and is involved in the regulation of lipolysis. Mol Cell Biol 30:1231-1242
11. Dusaulcy R, Rancoule C, Grès S, Wanecq E, Colom A, Guigné C, van Meeteren LA, Moolenaar WH, Valet P, Saulnier-Blache JS 2011 Adipose-specific disruption of autotaxin enhances nutritional fattening and reduces plasma lysophosphatidic acid. J Lipid Res 52:1247-1255
12. Wueest S, Rapold RA, Schumann DM, Rytka JM, Schildknecht A, Nov O, Chervonsky AV, Rudich A, Schoenle EJ, Donath MY, Kon-rad D 2010 Deletion of Fas in adipocytes relieves adipose tissue inflammation and hepatic manifestations of obesity in mice. J Clin Invest 120:191-202
13. Hofmann SM, Zhou L, Perez-Tilve D, Greer T, Grant E, Wancata L, Thomas A, Pfluger PT, Basford JE, Gilham D, Herz J, Tschöp MH, Hui DY 2007 Adipocyte LDL receptor-related protein-1 expression modulates postprandial lipid transport and glucose homeostasis in mice. J Clin Invest 117:3271-3282
14. Sabio G, Das M, Mora A, Zhang Z, Jun JY, Ko HJ, Barrett T, Kim JK, Davis RJ 2008 A stress signaling pathway in adipose tissue regulates hepatic insulin resistance. Science 322:1539-1543
15. Li P, Fan W, Xu J, Lu M, Yamamoto H, Auwerx J, Sears DD, Talukdar S, Oh D, Chen A, Bandyopadhyay G, Scadeng M, Ofrecio JM, Nalbandian S, Olefsky JM 2011 Adipocyte NCoR knockout decreases PPAR7 phosphorylation and enhances PPAR7 activity and insulin sensitivity. Cell 147:815-826
16. Ahmadian M, Abbott MJ, Tang T, Hudak CS, Kim Y, Bruss M, Hellerstein MK, Lee HY, Samuel VT, Shulman GI, Wang Y, Duncan RE, Kang C, Sul HS 2011 Desnutrin/ATGL is regulated by AMPK and is required for a brown adipose phenotype. Cell Metab 13:739-748
17. Wu JW, Wang SP, Casavant S, Moreau A, Yang GS, Mitchell GA 2012 Fasting energy homeostasis in mice with adipose deficiency of desnutrin/adipose triglyceride lipase. Endocrinology 153:2198-2207
18. Pardo R, Enguix N, Lasheras J, Feliu JE, Kralli A, Villena JA2011 Rosiglitazone-induced mitochondrial biogenesis in white adipose tissue is independent of peroxisome proliferator-activated receptor y coactivator-1a. PLoS One 6:e26989
19. Polak P, Cybulski N, Feige JN, Auwerx J, Rüegg MA, Hall MN 2008 Adipose-specific knockout of raptor results in lean mice with enhanced mitochondrial respiration. Cell Metab 8:399-410
20. Cybulski N, Polak P, Auwerx J, Rüegg MA, Hall MN 2009 mTOR complex 2 in adipose tissue negatively controls whole-body growth. Proc Natl Acad Sci USA 106:9902-9907
21. Kumar A, Lawrence Jr JC, Jung DY, Ko HJ, Keller SR, Kim JK, Magnuson MA, Harris TE 2010 Fat cell-specific ablation of rictor in mice impairs insulin-regulated fat cell and whole-body glucose and lipid metabolism. Diabetes 59:1397-1406
22. Lenz LS, Marx J, Chamulitrat W, Kaiser I, Gröne HJ, Liebisch G, Schmitz G, Elsing C, Straub BK, Füllekrug J, Stremmel W, Herrmann T 2011 Adipocyte-specific inactivation of Acyl-CoA synthetase fatty acid transport protein 4 (Fatp4) in mice causes adipose hypertrophy and alterations in metabolism of complex lipids under high fat diet. J Biol Chem 286:35578-35587
23. Urs S, Venkatesh D, Tang Y, Henderson T, Yang X, Friesel RE, Rosen CJ, Liaw L 2010 Sprouty1 is a critical regulatory switch of mesenchymal stem cell lineage allocation. FASEB J 24:3264-3273
24. Cernkovich ER, Deng J, Bond MC, Combs TP, Harp JB 2008 Adipose-specific disruption of signal transducer and activator of transcription 3 increases body weight and adiposity. Endocrinology 149:1581-1590
25. Pospisilik JA, Schramek D, Schnidar H, Cronin SJ, Nehme NT, Zhang X, Knauf C, Cani PD, Aumayr K, Todoric J, Bayer M, Haschemi A, Puviindran V, Tar K, Orthofer M, Neely GG, Dietzl G, Manoukian A, Funovics M, Prager G, Wagner O, Ferrandon D, Aberger F, Hui CC, Esterbauer H, Pennniger JM 2010 Drosophila genome-wide obesity screen reveals hedgehog as a determinant of brown versus white adipose cell fate. Cell 140:148-160
26. Minamino T, Orimo M, Shimizu I, Kunieda T, Yokoyama M, Ito T, Nojima A, Nabetani A, Oike Y, Matsubara H, Ishikawa F, Komuro I 2009 A crucial role for adipose tissue p53 in the regulation of insulin resistance. Nat Med 15:1082-1087
27. Shimizu I, Yoshida Y, Katsuno T, Tateno K, Okada S, Moriya J, Yokoyama M, Nojima A, Ito T, Zechner R, Komuro I, Kobayashi Y, Minamino T 2012 p53-Induced adipose tissue inflammation is critically involved in the development of insulin resistance in heart failure. Cell Metab 15:51-64
28. Feng D, Liu T, Sun Z, Bugge A, Mullican SE, Alenghat T, Liu XS, Lazar MA 2011 A circadian rhythm orchestrated by histone deacetylase 3 controls hepatic lipid metabolism. Science 331:1315-1319
29. Mullican SE, Gaddis CA, Alenghat T, Nair MG, Giacomin PR, Everett LJ, Feng D, Steger DJ, Schug J, Artis D, Lazar MA 2011 Histone deacetylase 3 is an epigenomic brake in macrophage alternative activation. Genes Dev 25:2480-2488
30. Sun Z, Miller RA, Patel RT, Chen J, Dhir R, Wang H, Zhang D, Graham MJ, Unterman TG, Shulman GI, Sztalryd C, Bennett MJ, Ahima RS, Birnbaum MJ, Lazar MA 2012 Hepatic Hdac3 promotes gluconeogenesis by repressing lipid synthesis and sequestration. Nat Med 18:934-942
31. Sun Z, Singh N, Mullican SE, Everett LJ, Li L, Yuan L, Liu X, Epstein JA, Lazar MA 2011 Diet-induced lethality due to deletion of the Hdac3 gene in heart and skeletal muscle. J Biol Chem 286: 33301-33309
32. Gong S, Yang XW, Li C, Heintz N 2002 Highly efficient modification of bacterial artificial chromosomes (BACs) using novel shuttle vectors containing the R6K7 origin of replication. Genome Res 12:1992-1998
33. Liu P, Jenkins NA, Copeland NG 2003 A highly efficient recom-bineering-based method for generating conditional knockout mutations. Genome Res 13:476-484
34. Jones JR, Barrick C, Kim KA, Lindner J, Blondeau B, Fujimoto Y, Shiota M, Kesterson RA, Kahn BB, Magnuson MA 2005 Deletion of PPAR7 in adipose tissues of mice protects against high fat diet-induced obesity and insulin resistance. Proc Natl Acad Sci USA 102:6207-6212
35. Moitra J, Mason MM, Olive M, Krylov D, Gavrilova O, Marcus-Samuels B, Feigenbaum L, Lee E, Aoyama T, Eckhaus M, Reitman ML, Vinson C 1998 Life without white fat: a transgenic mouse. Genes Dev 12:3168-3181
36. Ross SR, Graves RA, Spiegelman BM 1993 Targeted expression of a toxin gene to adipose tissue: transgenic mice resistant to obesity. Genes Dev 7:1318-1324
37. Péterfy M, Phan J, Xu P, Reue K 2001 Lipodystrophy in the fld mouse results from mutation of a new gene encoding a nuclear protein, lipin. Nat Genet 27:121-124
38. Shimomura I, Hammer RE, Richardson JA, Ikemoto S, Bashmakov Y, Goldstein JL, Brown MS 1998 Insulin resistance and diabetes mellitus in transgenic mice expressing nuclear SREBP-1c in adipose tissue: model for congenital generalized lipodystrophy. Genes Dev 12:3182-3194
39. Urs S, Harrington A, Liaw L, Small D 2006 Selective expression of an aP2/fatty acid binding protein 4-Cre transgene in non-adipo-genic tissues during embryonic development. Transgenic Res 15: 647-653
40. Martens K, Bottelbergs A, Baes M 2010 Ectopic recombination in the central and peripheral nervous system by aP2/FABP4-Cre mice: implications for metabolism research. FEBS Lett 584:1054-1058
41. Zhang J, Wang Y, Gao Z, Yun Z, Ye J 2012 Hypoxia-inducible factor 1 activation from adipose protein 2-cre mediated knockout of von Hippel-Lindau gene leads to embryonic lethality. Clin Exp Pharmacol Physiol 39:145-150
42. Steppan CM, Bailey ST, Bhat S, Brown EJ, Banerjee RR, Wright CM, Patel HR, Ahima RS, Lazar MA 2001 The hormone resistin links obesity to diabetes. Nature 409:307-312
43. Tomaru T, Steger DJ, Lefterova MI, Schupp M, Lazar MA 2009 Adipocyte-specific expression of murine resistin is mediated by synergism between peroxisome proliferator-activated receptor y and CCAAT/enhancer-binding proteins. J Biol Chem 284:6116-6125
44. Soriano P 1999 Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 21:70-71
45. Eguchi J, Wang X, Yu S, Kershaw EE, Chiu PC, Dushay J, Estall JL, Klein U, Maratos-Flier E, Rosen ED 2011 Transcriptional control of adipose lipid handling by IRF4. Cell Metab 13:249-259
46. Cinti S 2005 The adipose organ. Prostaglandins Leukot Essent Fatty Acids 73:9-15
47. Wang ZV, Deng Y, Wang QA, Sun K, Scherer PE 2010 Identification and characterization of a promoter cassette conferring adipocyte-specific gene expression. Endocrinology 151:2933-2939