The KRAB zinc finger protein RSL1 modulates sex-biased gene expression in liver and adipose tissue to maintain metabolic homeostasis

Molecular and Cellular Biology

Volumn 34, Issue 2, 2014, Pages 221-232

  Krebs, Christopher J ^a   Zhang, Deqiang ^a   Yin, Lei ^a   Robins, Diane M ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACYL COENZYME A DESATURASE 1; MESSENGER RNA; PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP); PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP) 1; REGULATOR OF SEX LIMITATION 1 PROTEIN; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY MASS; CONTROLLED STUDY; DIET RESTRICTION; DIETARY INTAKE; FEMALE; GENE CONTROL; GENE EXPRESSION; GENE MUTATION; GENETIC VARIABILITY; HOMEOSTASIS; LIPID DIET; MALE; METABOLIC PARAMETERS; METABOLIC STRESS; METABOLISM; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OBESITY; PRIORITY JOURNAL; PROTEIN FUNCTION; SEX DIFFERENCE; WEIGHT GAIN; WHITE ADIPOSE TISSUE; WILD TYPE;

EID: 84891428738     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00875-13     Document Type: Article

References (62)

1. Desvergne B, Michalik L, Wahli W. 2006. Transcriptional regulation of metabolism. Physiol. Rev. 86:465-514. http://dx.doi.org/10.1152/physrev.00025.2005.
2. Krebs CJ, Khan S, MacDonald JW, Sorenson M, Robins DM. 2009. Regulator of sex-limitation KRAB zinc finger proteins modulate sexdependent and -independent liver metabolism. Physiol. Genomics 38:16-28. http://dx.doi.org/10.1152/physiolgenomics.90391.2008.
3. Krebs CJ, Schultz DC, Robins DM. 2012. The KRAB zinc finger protein RSL1 regulates sex- and tissue-specific promoter methylation and dynamic hormone-responsive chromatin configuration. Mol. Cell. Biol. 32: 3732-3742. http://dx.doi.org/10.1128/MCB.00615-12.
4. Nowick K, Fields C, Gernat T, Caetano-Anolles D, Kholina N, Stubbs L. 2011. Gain, loss and divergence in primate zinc-finger genes: a rich resource for evolution of gene regulatory differences between species. PLoS One 6:e21553. http://dx.doi.org/10.1371/journal.pone.0021553.
5. Mackay DJ, Callaway JL, Marks SM, White HE, Acerini CL, Boonen SE, Dayanikli P, Firth HV, Goodship JA, Haemers AP, Hahnemann JM, Kordonouri O, Masoud AF, Oestergaard E, Storr J, Ellard S, Hattersley AT, Robinson DO, Temple IK. 2008. Hypomethylation of multiple imprinted loci in individuals with transient neonatal diabetes is associated with mutations in ZFP57. Nat. Genet. 40:949-951. http://dx.doi.org/10.1038/ng.187.
6. Hamilton AT, Huntley S, Kim J, Branscomb E, Stubbs L. 2003. Lineagespecific expansion of KRAB zinc-finger transcription factor genes: implications for the evolution of vertebrate regulatory networks. Cold Spring Harbor Symp. Quant. Biol. 68:131-140. http://dx.doi.org/10.1101/sqb.2003.68.131.
7. Krebs CJ, Larkins LK, Khan SM, Robins DM. 2005. Expansion and diversification of KRAB zinc-finger genes within a cluster including Regulator of sex-limitation 1 and 2. Genomics 85:752-761. http://dx.doi.org/10.1016/j.ygeno.2005.03.004.
8. Hamilton AT, Huntley S, Tran-GyamfiM, Baggott DM, Gordon L, Stubbs L. 2006. Evolutionary expansion and divergence in the ZNF91 subfamily of primate-specific zinc finger genes. Genome Res. 16:584-594. http://dx.doi.org/10.1101/gr.4843906.
9. Tadepally HD, Burger G, Aubry M. 2008. Evolution of C2H2-zinc finger genes and subfamilies in mammals: species-specific duplication and loss of clusters, genes and effector domains. BMC Evol. Biol. 8:176. http://dx.doi.org/10.1186/1471-2148-8-176.
10. Bellefroid EJ, Poncelet DA, Lecocq PJ, Revelant O, Martial JA. 1991. The evolutionarily conserved Kruppel-associated box domain defines a subfamily of eukaryotic multifingered proteins. Proc. Natl. Acad. Sci. U. S. A. 88:3608-3612. http://dx.doi.org/10.1073/pnas.88.9.3608.
11. Schultz DC, Friedman JR, Rauscher FJ, 3rd. 2001. Targeting histone deacetylase complexes via KRAB-zinc finger proteins: the PHD and bromodomains of KAP-1 form a cooperative unit that recruits a novel isoform of the Mi-2alpha subunit of NuRD. Genes Dev. 15:428-443. http://dx.doi.org/10.1101/gad.869501.
12. Schultz DC, Ayyanathan K, Negorev D, Maul GG, Rauscher FJ, 3rd. 2002. SETDB1: a novel KAP-1-associated histone H3, lysine 9-specific methyltransferase that contributes to HP1-mediated silencing of euchromatic genes by KRAB zinc-finger proteins. Genes Dev. 16:919-932. http://dx.doi.org/10.1101/gad.973302.
13. Ayyanathan K, Lechner MS, Bell P, Maul GG, Schultz DC, Yamada Y, Tanaka K, Torigoe K, Rauscher FJ, 3rd. 2003. Regulated recruitment of HP1 to a euchromatic gene induces mitotically heritable, epigenetic gene silencing: a mammalian cell culture model of gene variegation. Genes Dev. 17:1855-1869. http://dx.doi.org/10.1101/gad.1102803.
14. Zuo X, Sheng J, Lau HT, McDonald CM, Andrade M, Cullen DE, Bell FT, Iacovino M, Kyba M, Xu G, Li X. 2012. Zinc finger protein ZFP57 requires its co-factor to recruit DNA methyltransferases and maintains DNA methylation imprint in embryonic stem cells via its transcriptional repression domain. J. Biol. Chem. 287:2107-2118. http://dx.doi.org/10.1074/jbc. M111.322644.
15. Wolf D, GoffSP. 2007. TRIM28 mediates primer binding site-targeted silencing of murine leukemia virus in embryonic cells. Cell 131:46-57. http://dx.doi.org/10.1016/j.cell.2007.07.026.
16. Rowe HM, Jakobsson J, Mesnard D, Rougemont J, Reynard S, Aktas T, Maillard PV, Layard-Liesching H, Verp S, Marquis J, Spitz F, Constam DB, Trono D. 2010. KAP1 controls endogenous retroviruses in embryonic stem cells. Nature 463:237-240. http://dx.doi.org/10.1038/nature08674.
17. Li X, Ito M, Zhou F, Youngson N, Zuo X, Leder P, Ferguson-Smith AC. 2008. A maternal-zygotic effect gene, Zfp57, maintains both maternal and paternal imprints. Dev. Cell 15:547-557. http://dx.doi.org/10.1016/j.devcel.2008.08.014.
18. Scherneck S, Nestler M, Vogel H, Bluher M, Block MD, Berriel Diaz M, Herzig S, Schulz N, Teichert M, Tischer S, Al-Hasani H, Kluge R, Schurmann A, Joost HG. 2009. Positional cloning of zinc finger domain transcription factor Zfp69, a candidate gene for obesity-associated diabetes contributed by mouse locus Nidd/SJL. PLoS Genet. 5:e1000541. http://dx.doi.org/10.1371/journal.pgen.1000541.
19. Shibata M, Blauvelt KE, Liem KF, Jr, Garcia-Garcia MJ. 2011. TRIM28 is required by the mouse KRAB domain protein ZFP568 to control convergent extension and morphogenesis of extra-embryonic tissues. Development 138:5333-5343. http://dx.doi.org/10.1242/dev.072546.
20. Shin JH, Ko HS, Kang H, Lee Y, Lee YI, Pletinkova O, Troconso JC, Dawson VL, Dawson TM. 2011. PARIS (ZNF746) repression of PGC-1alpha contributes to neurodegeneration in Parkinson's disease. Cell 144: 689-702. http://dx.doi.org/10.1016/j.cell.2011.02.010.
21. Tullis KM, Krebs CJ, Leung JY, Robins DM. 2003. The regulator of sex-limitation gene, rsl, enforces male-specific liver gene expression by negative regulation. Endocrinology 144:1854-1860. http://dx.doi.org/10.1210/en.2002-0190.
22. Krebs CJ, Larkins LK, Price R, Tullis KM, Miller RD, Robins DM. 2003. Regulator of sex-limitation (Rsl) encodes a pair of KRAB zinc-finger genes that control sexually dimorphic liver gene expression. Genes Dev. 17: 2664-2674. http://dx.doi.org/10.1101/gad.1135703.
23. Udy GB, Towers RP, Snell RG, Wilkins RJ, Park SH, Ram PA, Waxman DJ, Davey HW. 1997. Requirement of STAT5b for sexual dimorphism of body growth rates and liver gene expression. Proc. Natl. Acad. Sci. U. S. A. 94:7239-7244. http://dx.doi.org/10.1073/pnas.94.14.7239.
24. Zhang Y, Klein K, Sugathan A, Nassery N, Dombkowski A, Zanger UM, Waxman DJ. 2011. Transcriptional profiling of human liver identifies sex-biased genes associated with polygenic dyslipidemia and coronary artery disease. PLoS One 6:e23506. http://dx.doi.org/10.1371/journal.pone.0023506.
25. Rinn JL, Snyder M. 2005. Sexual dimorphism in mammalian gene expression. Trends Genet. 21:298-305. http://dx.doi.org/10.1016/j.tig.2005.03.005.
26. Yang X, Schadt EE, Wang S, Wang H, Arnold AP, Ingram-Drake L, Drake TA, Lusis AJ. 2006. Tissue-specific expression and regulation of sexually dimorphic genes in mice. Genome Res. 16:995-1004. http://dx.doi.org/10.1101/gr.5217506.
27. Jiang PP, Frederick K, Hansen TH, Miller RD. 1996. Localization of the mouse gene releasing sex-limited expression of Slp. Proc. Natl. Acad. Sci. U. S. A. 93:913-917. http://dx.doi.org/10.1073/pnas.93.2.913.
28. Zhang R, Dhillon H, Yin H, Yoshimura A, Lowell BB, Maratos-Flier E, Flier JS. 2008. Selective inactivation of Socs3 in SF1 neurons improves glucose homeostasis without affecting body weight. Endocrinology 149: 5654-5661. http://dx.doi.org/10.1210/en.2008-0805.
29. Krebs CJ, Robins DM. 2010. A pair of mouse KRAB zinc finger proteins modulates multiple indicators of female reproduction. Biol. Reprod. 82: 662-668. http://dx.doi.org/10.1095/biolreprod.109.080846.
30. PfafflMW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45. http://dx.doi.org/10.1093/nar/29.9.e45.
31. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP. 2003. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4:249-264. http://dx.doi.org/10.1093/biostatistics/4.2.249.
32. Bojkowska K, Aloisio F, Cassano M, Kapopoulou A, Santoni de Sio F, Zangger N, Offner S, Cartoni C, Thomas C, Quenneville S, Johnsson K, Trono D. 2012. Liver-specific ablation of Kruppel-associated boxassociated protein 1 in mice leads to male-predominant hepatosteatosis and development of liver adenoma. Hepatology 56:1279-1290. http://dx.doi.org/10.1002/hep.25767.
33. Wahli W, Michalik L. 2012. PPARs at the crossroads of lipid signaling and inflammation. Trends Endocrinol. Metab. 23:351-363. http://dx.doi.org/10.1016/j.tem.2012.05.001.
34. Zadravec D, Brolinson A, Fisher RM, Carneheim C, Csikasz RI, Bertrand-Michel J, Boren J, Guillou H, Rudling M, Jacobsson A. 2010. Ablation of the very-long-chain fatty acid elongase ELOVL3 in mice leads to constrained lipid storage and resistance to diet-induced obesity. FASEB J. 24:4366-4377. http://dx.doi.org/10.1096/fj.09-152298.
35. Zhou Y, Jiang L, Rui L. 2009. Identification of MUP1 as a regulator for glucose and lipid metabolism in mice. J. Biol. Chem. 284:11152-11159. http://dx.doi.org/10.1074/jbc. M900754200.
36. Jakobsson A, Westerberg R, Jacobsson A. 2006. Fatty acid elongases in mammals: their regulation and roles in metabolism. Prog. Lipid Res. 45: 237-249. http://dx.doi.org/10.1016/j.plipres.2006.01.004.
37. Sun K, Kusminski CM, Scherer PE. 2011. Adipose tissue remodeling and obesity. J. Clin. Invest. 121:2094-2101. http://dx.doi.org/10.1172/JCI45887.
38. Costet P, Legendre C, More J, Edgar A, Galtier P, Pineau T. 1998. Peroxisome proliferator-activated receptor alpha-isoform deficiency leads to progressive dyslipidemia with sexually dimorphic obesity and steatosis. J. Biol. Chem. 273:29577-29585. http://dx.doi.org/10.1074/jbc.273.45.29577.
39. Perez-Sieira S, Martinez G, Porteiro B, Lopez M, Vidal A, Nogueiras R, Dieguez C. 2013. Female Nur77-deficient mice show increased susceptibility to diet-induced obesity. PLoS One 8:e53836. http://dx.doi.org/10.1371/journal.pone.0053836.
40. Holloway MG, Miles GD, Dombkowski AA, Waxman DJ. 2008. Liverspecific hepatocyte nuclear factor-4alpha deficiency: greater impact on gene expression in male than in female mouse liver. Mol. Endocrinol. 22:1274-1286. http://dx.doi.org/10.1210/me.2007-0564.
41. Leuenberger N, Pradervand S, Wahli W. 2009. Sumoylated PPARalpha mediates sex-specific gene repression and protects the liver from estrogeninduced toxicity in mice. J. Clin. Invest. 119:3138-3148. http://dx.doi.org/10.1172/JCI39019.
42. Meyer RD, Laz EV, Su T, Waxman DJ. 2009. Male-specific hepatic Bcl6: growth hormone-induced block of transcription elongation in females and binding to target genes inversely coordinated with STAT5. Mol. Endocrinol. 23:1914-1926. http://dx.doi.org/10.1210/me.2009-0242.
43. Whitelaw NC, Chong S, Morgan DK, Nestor C, Bruxner TJ, Ashe A, Lambley E, Meehan R, Whitelaw E. 2010. Reduced levels of two modifiers of epigenetic gene silencing, Dnmt3a and Trim28, cause increased phenotypic noise. Genome Biol. 11:R111. http://dx.doi.org/10.1186/gb -2010-11-11-r111.
44. Messerschmidt DM, de Vries W, Ito M, Solter D, Ferguson-Smith A, Knowles BB. 2012. Trim28 is required for epigenetic stability during mouse oocyte to embryo transition. Science 335:1499-1502. http://dx.doi.org/10.1126/science.1216154.
45. O'Geen H, Squazzo SL, Iyengar S, Blahnik K, Rinn JL, Chang HY, Green R, Farnham PJ. 2007. Genome-wide analysis of KAP1 binding suggests autoregulation of KRAB-ZNFs. PLoS Genet. 3:e89. http://dx.doi.org/10.1371/journal.pgen.0030089.
46. Flower DR. 1996. The lipocalin protein family: structure and function. Biochem. J. 318:1-14.
47. Sharrow SD, Vaughn JL, Zidek L, Novotny MV, Stone MJ. 2002. Pheromone binding by polymorphic mouse major urinary proteins. Protein Sci. 11:2247-2256. http://dx.doi.org/10.1110/ps.0204202.
48. Yang Q, Graham TE, Mody N, Preitner F, Peroni OD, Zabolotny JM, Kotani K, Quadro L, Kahn BB. 2005. Serum retinol binding protein 4 contributes to insulin resistance in obesity and type 2 diabetes. Nature 436:356-362. http://dx.doi.org/10.1038/nature03711.
49. Zhang J, Wu Y, Zhang Y, Leroith D, Bernlohr DA, Chen X. 2008. The role of lipocalin 2 in the regulation of inflammation in adipocytes and macrophages. Mol. Endocrinol. 22:1416-1426. http://dx.doi.org/10.1210/me.2007-0420.
50. Yan QW, Yang Q, Mody N, Graham TE, Hsu CH, Xu Z, Houstis NE, Kahn BB, Rosen ED. 2007. The adipokine lipocalin 2 is regulated by obesity and promotes insulin resistance. Diabetes 56:2533-2540. http://dx.doi.org/10.2337/db07-0007.
51. Guo H, Jin D, Zhang Y, Wright W, Bazuine M, Brockman DA, Bernlohr DA, Chen X. 2010. Lipocalin-2 deficiency impairs thermogenesis and potentiates diet-induced insulin resistance in mice. Diabetes 59: 1376-1385. http://dx.doi.org/10.2337/db09-1735.
52. Macotela Y, Boucher J, Tran TT, Kahn CR. 2009. Sex and depot differences in adipocyte insulin sensitivity and glucose metabolism. Diabetes 58:803-812. http://dx.doi.org/10.2337/db08-1054.
53. Grove KL, Fried SK, Greenberg AS, Xiao XQ, Clegg DJ. 2010. A microarray analysis of sexual dimorphism of adipose tissues in high-fatdiet-induced obese mice. Int. J. Obes. (Lond.) 34:989-1000. http://dx.doi.org/10.1038/ijo.2010.12.
54. Shi H, Seeley RJ, Clegg DJ. 2009. Sexual differences in the control of energy homeostasis. Front. Neuroendocrinol. 30:396-404. http://dx.doi.org/10.1016/j.yfrne.2009.03.004.
55. Ochsner SA, Watkins CM, McOwiti A, Xu X, Darlington YF, Dehart MD, Cooney AJ, Steffen DL, Becnel LB, McKenna NJ. 2012. Transcriptomine, a web resource for nuclear receptor signaling transcriptomes. Physiol. Genomics 44:853-863. http://dx.doi.org/10.1152/physiolgenomics.00033.2012.
56. Heine PA, Taylor JA, Iwamoto GA, Lubahn DB, Cooke PS. 2000. Increased adipose tissue in male and female estrogen receptor-alpha knockout mice. Proc. Natl. Acad. Sci. U. S. A. 97:12729-12734. http://dx.doi.org/10.1073/pnas.97.23.12729.
57. Garcia-Garcia MJ, Shibata M, Anderson KV. 2008. Chato, a KRAB zinc-finger protein, regulates convergent extension in the mouse embryo. Development 135:3053-3062. http://dx.doi.org/10.1242/dev.022897.
58. Cheng Y, Geng H, Cheng SH, Liang P, Bai Y, Li J, Srivastava G, Ng MH, Fukagawa T, Wu X, Chan AT, Tao Q. 2010. KRAB zinc finger protein ZNF382 is a proapoptotic tumor suppressor that represses multiple oncogenes and is commonly silenced in multiple carcinomas. Cancer Res. 70: 6516-6526. http://dx.doi.org/10.1158/0008-5472.CAN-09-4566.
59. Lin LF, Chuang CH, Li CF, Liao CC, Cheng CP, Cheng TL, Shen MR, Tseng JT, Chang WC, Lee WH, Wang JM. 2010. ZBRK1 acts as a metastatic suppressor by directly regulating MMP9 in cervical cancer. Cancer Res. 70:192-201. http://dx.doi.org/10.1158/0008-5472.CAN-09-2641.
60. Emerson RO, Thomas JH. 2009. Adaptive evolution in zinc finger transcription factors. PLoS Genet. 5:e1000325. http://dx.doi.org/10.1371/journal.pgen.1000325.
61. Wang S, Yehya N, Schadt EE, Wang H, Drake TA, Lusis AJ. 2006. Genetic and genomic analysis of a fat mass trait with complex inheritance reveals marked sex specificity. PLoS Genet. 2:e15. http://dx.doi.org/10.1371/journal.pgen.0020015.
62. Huntley S, Baggott DM, Hamilton AT, Tran-GyamfiM, Yang S, Kim J, Gordon L, Branscomb E, Stubbs L. 2006. A comprehensive catalog of human KRAB-associated zinc finger genes: insights into the evolutionary history of a large family of transcriptional repressors. Genome Res. 16: 669-677. http://dx.doi.org/10.1101/gr.4842106.