Cited by 81

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SUMOylation-Dependent LRH-1/PROX1 Interaction Promotes Atherosclerosis by Decreasing Hepatic Reverse Cholesterol Transport

Stein, Sokrates, Oosterveer, Maaike H., Mataki, Chikage, Xu, Pan, Lemos, Vera, Havinga, Rick, Dittner, Claudia, Ryu, Dongryeol, Menzies, Keir J., Wang, Xu, Perino, Alessia, Houten, Sander M., Melchior, Frauke, Schoonjans, Kristina·2014·Cell Metabolism

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Crossref · 10.1016/j.cmet.2014.07.023

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  • SUMOylation promotes LRH-1 to interact with co-repressor Prox1, leading to reduced transcription of reverse cholesterol transport genes.

    “SUMOylation is also reported to promote the nuclear receptor liver receptor homolog 1 to interact with its co-repressor prosperso homeobox protein 1, leading to reduced transcription of the target genes involved in reverse cholesterol transport (25).”

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Research works printed but not linked: 38

  1. Bernier-Villamor, 2002, Structural basis for E2-mediated SUMO conjugation revealed by a complex between ubiquitin-conjugating enzyme Ubc9 and RanGAP1, Cell, 108, 345, 10.1016/S0092-8674(02)00630-X · DOI
  2. Botrugno, 2004, Synergy between LRH-1 and beta-catenin induces G1 cyclin-mediated cell proliferation, Mol. Cell, 15, 499, 10.1016/j.molcel.2004.07.009 · DOI
  3. Chalkiadaki, 2005, SUMO-dependent compartmentalization in promyelocytic leukemia protein nuclear bodies prevents the access of LRH-1 to chromatin, Mol. Cell. Biol., 25, 5095, 10.1128/MCB.25.12.5095-5105.2005 · DOI
  4. Coste, 2007, LRH-1-mediated glucocorticoid synthesis in enterocytes protects against inflammatory bowel disease, Proc. Natl. Acad. Sci. USA, 104, 13098, 10.1073/pnas.0702440104 · DOI
  5. Duggavathi, 2008, Liver receptor homolog 1 is essential for ovulation, Genes Dev., 22, 1871, 10.1101/gad.472008 · DOI
  6. Fayard, 2003, Liver receptor homolog 1 controls the expression of carboxyl ester lipase, J. Biol. Chem., 278, 35725, 10.1074/jbc.M302370200 · DOI
  7. Fayard, 2004, LRH-1: an orphan nuclear receptor involved in development, metabolism and steroidogenesis, Trends Cell Biol., 14, 250, 10.1016/j.tcb.2004.03.008 · DOI
  8. Fernandez-Marcos, 2011, Emerging actions of the nuclear receptor LRH-1 in the gut, Biochim. Biophys. Acta, 1812, 947, 10.1016/j.bbadis.2010.12.010 · DOI
  9. Freeman, 2004, The orphan nuclear receptor LRH-1 activates the ABCG5/ABCG8 intergenic promoter, J. Lipid Res., 45, 1197, 10.1194/jlr.C400002-JLR200 · DOI
  10. Geiss-Friedlander, 2007, Concepts in sumoylation: a decade on, Nat. Rev. Mol. Cell Biol., 8, 947, 10.1038/nrm2293 · DOI
  11. Goodwin, 2000, A regulatory cascade of the nuclear receptors FXR, SHP-1, and LRH-1 represses bile acid biosynthesis, Mol. Cell, 6, 517, 10.1016/S1097-2765(00)00051-4 · DOI · Paper page
  12. Hwang, 2009, SUMOylation of RORalpha potentiates transcriptional activation function, Biochem. Biophys. Res. Commun., 378, 513, 10.1016/j.bbrc.2008.11.072 · DOI
  13. Ingraham, 2005, Orphan nuclear receptors adopted by crystallography, Curr. Opin. Struct. Biol., 15, 708, 10.1016/j.sbi.2005.10.009 · DOI
  14. Jentsch, 2013, Control of nuclear activities by substrate-selective and protein-group SUMOylation, Annu. Rev. Genet., 47, 167, 10.1146/annurev-genet-111212-133453 · DOI
  15. Krasowski, 2008, Intrinsic disorder in nuclear hormone receptors, J. Proteome Res., 7, 4359, 10.1021/pr8003024 · DOI
  16. Kruit, 2005, Increased fecal neutral sterol loss upon liver X receptor activation is independent of biliary sterol secretion in mice, Gastroenterology, 128, 147, 10.1053/j.gastro.2004.10.006 · DOI
  17. Lee, 2002, Dual mechanisms for repression of the monomeric orphan receptor liver receptor homologous protein-1 by the orphan small heterodimer partner, J. Biol. Chem., 277, 2463, 10.1074/jbc.M105161200 · DOI
  18. Lee, 2008, Liver receptor homolog-1, an emerging metabolic modulator, Front. Biosci., 13, 5950, 10.2741/3128 · DOI
  19. Lee, 2005, The DEAD-box protein DP103 (Ddx20 or Gemin-3) represses orphan nuclear receptor activity via SUMO modification, Mol. Cell. Biol., 25, 1879, 10.1128/MCB.25.5.1879-1890.2005 · DOI
  20. Lee, 2011, Eliminating SF-1 (NR5A1) sumoylation in vivo results in ectopic hedgehog signaling and disruption of endocrine development, Dev. Cell, 21, 315, 10.1016/j.devcel.2011.06.028 · DOI
  21. Lee, 2011, A nuclear-receptor-dependent phosphatidylcholine pathway with antidiabetic effects, Nature, 474, 506, 10.1038/nature10111 · DOI
  22. Lu, 2000, Molecular basis for feedback regulation of bile acid synthesis by nuclear receptors, Mol. Cell, 6, 507, 10.1016/S1097-2765(00)00050-2 · DOI · Paper page
  23. Marciano, 2014, The therapeutic potential of nuclear receptor modulators for treatment of metabolic disorders: PPARγ, RORs, and Rev-erbs, Cell Metab., 19, 193, 10.1016/j.cmet.2013.12.009 · DOI
  24. Mataki, 2007, Compromised intestinal lipid absorption in mice with a liver-specific deficiency of liver receptor homolog 1, Mol. Cell. Biol., 27, 8330, 10.1128/MCB.00852-07 · DOI
  25. Meissner, 2010, Voluntary exercise increases cholesterol efflux but not macrophage reverse cholesterol transport in vivo in mice, Nutr. Metab. (Lond), 7, 54, 10.1186/1743-7075-7-54 · DOI
  26. Oosterveer, 2012, LRH-1-dependent glucose sensing determines intermediary metabolism in liver, J. Clin. Invest., 122, 2817, 10.1172/JCI62368 · DOI
  27. Out, 2011, Liver receptor homolog-1 is critical for adequate up-regulation of Cyp7a1 gene transcription and bile salt synthesis during bile salt sequestration, Hepatology, 53, 2075, 10.1002/hep.24286 · DOI
  28. Qin, 2004, Prospero-related homeobox (Prox1) is a corepressor of human liver receptor homolog-1 and suppresses the transcription of the cholesterol 7-alpha-hydroxylase gene, Mol. Endocrinol., 18, 2424, 10.1210/me.2004-0009 · DOI
  29. Ryu, 2011, Endoplasmic reticulum stress promotes LIPIN2-dependent hepatic insulin resistance, Diabetes, 60, 1072, 10.2337/db10-1046 · DOI
  30. Schoonjans, 2002, Liver receptor homolog 1 controls the expression of the scavenger receptor class B type I, EMBO Rep., 3, 1181, 10.1093/embo-reports/kvf238 · DOI
  31. Stein, 2010, SIRT1 decreases Lox-1-mediated foam cell formation in atherogenesis, Eur. Heart J., 31, 2301, 10.1093/eurheartj/ehq107 · DOI · Paper page
  32. Talamillo, 2013, Scavenger receptors mediate the role of SUMO and Ftz-f1 in Drosophila steroidogenesis, PLoS Genet., 9, e1003473, 10.1371/journal.pgen.1003473 · DOI
  33. Treuter, 2011, Transcriptional control of metabolic and inflammatory pathways by nuclear receptor SUMOylation, Biochim. Biophys. Acta, 1812, 909, 10.1016/j.bbadis.2010.12.008 · DOI
  34. Venteclef, 2008, Regulation of anti-atherogenic apolipoprotein M gene expression by the orphan nuclear receptor LRH-1, J. Biol. Chem., 283, 3694, 10.1074/jbc.M706382200 · DOI
  35. Venteclef, 2010, GPS2-dependent corepressor/SUMO pathways govern anti-inflammatory actions of LRH-1 and LXRbeta in the hepatic acute phase response, Genes Dev., 24, 381, 10.1101/gad.545110 · DOI · Paper page
  36. Ward, 2013, Sumoylated NHR-25/NR5A regulates cell fate during C. elegans vulval development, PLoS Genet., 9, e1003992, 10.1371/journal.pgen.1003992 · DOI
  37. Weber, 2011, Atherosclerosis: current pathogenesis and therapeutic options, Nat. Med., 17, 1410, 10.1038/nm.2538 · DOI · Paper page
  38. Yang, 2009, Liver receptor homolog-1 localization in the nuclear body is regulated by sumoylation and cAMP signaling in rat granulosa cells, FEBS J., 276, 425, 10.1111/j.1742-4658.2008.06785.x · DOI

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Metadata

Authors
Stein, S., Oosterveer, M. H., Mataki, C., Xu, P., Lemos, V., Havinga, R., Dittner, C., Ryu, D., Menzies, K. J., Wang, X., Perino, A., Houten, S. M., Melchior, F., & Schoonjans, K.
Venue
Cell Metabolism
Publisher
Elsevier BV
Published
2014-10
Volume
20
Issue
4
Pages
603-613
ISSN
1550-4131
Cited by
81
References
2
Language
en
Funders
  • Schweizerische Herzstiftung
  • École Polytechnique Fédérale de Lausanne
  • Krebsliga Schweiz (KLS-2809-08-2011)

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