Cited by 43Cholesterol and Lipid MetabolismSteroid Chemistry and BiochemistrySphingolipid Metabolism and Signaling

Nuclear receptors, cholesterol homeostasis and the immune system

Open access
Shahoei, Sayyed Hamed, Nelson, Erik R.·2019·The Journal of Steroid Biochemistry and Molecular Biology

Abstract

Cholesterol is essential for maintaining membrane fluidity in eukaryotes. Additionally, the synthetic cascade of cholesterol results in precursor molecules important for cellular function such as lipid raft formation and protein prenylation. As such, cholesterol homeostasis is tightly regulated. Interestingly, it is now known that some cholesterol precursors and many metabolites serve as active signaling molecules, binding to different classes of receptors including the nuclear receptors. Furthermore, many cholesterol metabolites or their nuclear receptors have been implicated in the regulation of the immune system in normal physiology and disease. Therefore, in this focused review, cholesterol homeostasis and nuclear receptors involved in this regulation will be discussed, with particular emphasis on how these cascades influence the immune system.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.jsbmb.2019.04.013

Cites

11 of 11 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 103

  1. [2]Dawaliby R, Trubbia C, Delporte C, Noyon C, Ruysschaert J-M, Van Antwerpen P, Govaerts C, Phosphatidylethanolamine Is a Key Regulator of Membrane Fluidity in Eukaryotic Cells, Journal of Biological Chemistry, 291 (2016) 3658– 3667. 26663081 PMC4751403
  2. [3]Ricci JN, Coleman ML, Welander PV, Sessions AL, Summons RE, Spear JR, Newman DK, Diverse capacity for 2-methylhopanoid production correlates with a specific ecological niche, The Isme Journal, 8 (2013) 675. 24152713 PMC3930323
  3. [4]Huang X, Warren JT, Gilbert LI, New players in the regulation of ecdysone biosynthesis, Journal of Genetics and Genomics, 35 (2008) 1– 10. 18222403
  4. [5]Motola DL, Cummins CL, Rottiers V, Sharma KK, Li T, Li Y, Suino-Powell K, Xu HE, Auchus RJ, Antebi A, Mangelsdorf DJ, Identification of Ligands for DAF-12 that Govern Dauer Formation and Reproduction in C. elegans, Cell, 124 (2006) 1209– 1223. 16529801
  5. [6]Hofmann AF, Hagey LR, Krasowski MD, Bile salts of vertebrates: structural variation and possible evolutionary significance, 51 (2010) 226– 246. PMC2803226 19638645
  6. [8]Nelson ER, Habibi HR, Estrogen receptor function and regulation in fish and other vertebrates, Gen Comp Endocrinol, 192 (2013) 15– 24. 23583769
  7. [9]Mangelsdorf DJ, Thummel C, Beato M, Herrlich P, Schutz G, Umesono K, Blumberg B, Kastner P, Mark M, Chambon P, Evans RM, The nuclear receptor superfamily: the second decade, Cell, 83 (1995) 835– 839. 8521507 PMC6159888
  8. [10]Nelson ER, Wardell SE, McDonnell DP, The molecular mechanisms underlying the pharmacological actions of estrogens, SERMs and oxysterols: implications for the treatment and prevention of osteoporosis, Bone, 53 (2013) 42– 50. 23168292 PMC3552054
  9. [11]Goldstein JL, Brown MS, Regulation of the mevalonate pathway, Nature, 343 (1990) 425. 1967820
  10. [12]Sharpe LJ, Brown AJ, Controlling cholesterol synthesis beyond 3-hydroxy-3-methylglutaryl-CoA reductase (HMGCR), The Journal of biological chemistry, 288 (2013) 18707– 18715. 23696639 PMC3696645
  11. [13]Olson RE, Discovery of the Lipoproteins, Their Role in Fat Transport and Their Significance as Risk Factors, The Journal of Nutrition, 128 (1998) 439S– 443S. 9478044
  12. [14]Julve J, Martín-Campos JM, Escolà-Gil JC, Blanco-Vaca F, Chylomicrons: Advances in biology, pathology, laboratory testing, and therapeutics, Clinica Chimica Acta, 455 (2016) 134– 148. 26868089
  13. [15]Russell DW, The Enzymes, Regulation, and Genetics of Bile Acid Synthesis, 72 (2003) 137– 174. 12543708
  14. [16]Andersson S, Davis DL, Dahlbäck H, Jörnvall H, Russell DW, Cloning, structure, and expression of the mitochondrial cytochrome P-450 sterol 26-hydroxylase, a bile acid biosynthetic enzyme, 264 (1989) 8222– 8229. 2722778
  15. [17]He S, Nelson ER, 27-Hydroxycholesterol, an endogenous selective estrogen receptor modulator, Maturitas, 104 (2017) 29– 35. 28923174 PMC5657610
  16. [19]Nevius E, Pinho F, Dhodapkar M, Jin H, Nadrah K, Horowitz MC, Kikuta J, Ishii M, Pereira JP, Oxysterols and EBI2 promote osteoclast precursor migration to bone surfaces and regulate bone mass homeostasis, 212 (2015) 1931– 1946. PMC4612084 26438360
  17. [20]Nelson ER, DuSell CD, Wang X, Howe MK, Evans G, Michalek RD, Umetani M, Rathmell JC, Khosla S, Gesty-Palmer D, McDonnell DP, The oxysterol, 27-hydroxycholesterol, links cholesterol metabolism to bone homeostasis through its actions on the estrogen and liver X receptors, Endocrinology, 152 (2011) 4691– 4705. 21933863 PMC3230052
  18. [21]Zimmer S, Grebe A, Bakke SS, Bode N, Halvorsen B, Ulas T, Skjelland M, De Nardo D, Labzin LI, Kerksiek A, Hempel C, Heneka MT, Hawxhurst V, Fitzgerald ML, Trebicka J, Björkhem I, Gustafsson J-Å, Westerterp M, Tall AR, Wright SD, Espevik T, Schultze JL, Nickenig G, Lütjohann D, Latz E, Cyclodextrin promotes atherosclerosis regression via macrophage reprogramming, Science translational medicine, 8 (2016) 333ra350– 333ra350. PMC4878149 27053774
  19. [22]Moore KJ, Sheedy FJ, Fisher EA, Macrophages in atherosclerosis: a dynamic balance, Nature Reviews Immunology, 13 (2013) 709. PMC4357520 23995626
  20. [23]Ma L, Nelson ER, Oxysterols and nuclear receptors, Molecular and cellular endocrinology, Published Online on 18 1, 2019 (in press). 30660701
  21. [24]Brown MS, Goldstein JL, The SREBP Pathway: Regulation of Cholesterol Metabolism by Proteolysis of a Membrane-Bound Transcription Factor, Cell, 89 (1997) 331– 340. 9150132
  22. [25]Hua X, Nohturfft A, Goldstein JL, Brown MS, Sterol Resistance in CHO Cells Traced to Point Mutation in SREBP Cleavage–Activating Protein, Cell, 87 (1996) 415– 426. 8898195
  23. [26]Ioannou GN, The Role of Cholesterol in the Pathogenesis of NASH, Trends in Endocrinology & Metabolism, 27 (2016) 84– 95. 26703097
  24. [27]Janowski BA, Willy PJ, Devi TR, Falck JR, Mangelsdorf DJ, An oxysterol signalling pathway mediated by the nuclear receptor LXRα, Nature, 383 (1996) 728. 8878485
  25. [28]Nitta M, Ku S, Brown C, Okamoto AY, Shan B, CPF: an orphan nuclear receptor that regulates liver-specific expression of the human cholesterol 7alpha-hydroxylase gene, Proceedings of the National Academy of Sciences of the United States of America, 96 (1999) 6660– 6665. 10359768 PMC21971
  26. [29]Kerr TA, Saeki S, Schneider M, Schaefer K, Berdy S, Redder T, Shan B, Russell DW, Schwarz M, Loss of nuclear receptor SHP impairs but does not eliminate negative feedback regulation of bile acid synthesis, Developmental cell, 2 (2002) 713– 720. 12062084 PMC4010195
  27. [30]Wang L, Lee Y-K, Bundman D, Han Y, Thevananther S, Kim C-S, Chua SS, Wei P, Heyman RA, Karin M, Moore DD, Redundant Pathways for Negative Feedback Regulation of Bile Acid Production, Developmental Cell, 2 (2002) 721– 731. 12062085
  28. [31]Goodwin B, Jones SA, Price RR, Watson MA, McKee DD, Moore LB, Galardi C, Wilson JG, Lewis MC, Roth ME, Maloney PR, Willson TM, Kliewer SA, A Regulatory Cascade of the Nuclear Receptors FXR, SHP-1, and LRH-1 Represses Bile Acid Biosynthesis, Molecular Cell, 6 (2000) 517– 526. 11030332
  29. [32]Lu TT, Makishima M, Repa JJ, Schoonjans K, Kerr TA, Auwerx J, Mangelsdorf DJ, Molecular Basis for Feedback Regulation of Bile Acid Synthesis by Nuclear Receptors, Molecular Cell, 6 (2000) 507– 515. 11030331
  30. [33]Barish GD, Downes M, Alaynick WA, Yu RT, Ocampo CB, Bookout AL, Mangelsdorf DJ, Evans RM, A Nuclear Receptor Atlas: Macrophage Activation, Molecular Endocrinology, 19 (2005) 2466– 2477. 16051664
  31. [34]van Beek ER, Cohen LH, Leroy IM, Ebetino FH, Löwik CWGM, Papapoulos SE, Differentiating the mechanisms of antiresorptive action of nitrogen containing bisphosphonates, Bone, 33 (2003) 805– 811. 14623056
  32. [35]Newton RH, Shrestha S, Sullivan JM, Yates KB, Compeer EB, Ron-Harel N, Blazar BR, Bensinger SJ, Haining WN, Dustin ML, Campbell DJ, Chi H, Turka LA, Maintenance of CD4 T cell fitness through regulation of Foxo1, Nature immunology, 19 (2018) 838– 848. 29988091 PMC6289177
  33. [36]Zhao W, Prijic S, Urban BC, Tisza MJ, Zuo Y, Li L, Tan Z, Chen X, Mani SA, Chang JT, Candidate Antimetastasis Drugs Suppress the Metastatic Capacity of Breast Cancer Cells by Reducing Membrane Fluidity, 76 (2016) 2037– 2049. PMC8491548 26825169
  34. [37]Fessler MB, The Intracellular Cholesterol Landscape: Dynamic Integrator of the Immune Response, Trends Immunol, 37 (2016) 819– 830. 27692616 PMC5135597
  35. [38]Reboldi A, Dang E, Cholesterol metabolism in innate and adaptive response, F1000Res, 7 (2018). PMC6192436 30364153
  36. [39]Anuka E, Gal M, Stocco DM, Orly J, Expression and roles of steroidogenic acute regulatory (StAR) protein in ‘non-classical’, extra-adrenal and extra-gonadal cells and tissues, Molecular and Cellular Endocrinology, 371 (2013) 47– 61. 23415713
  37. [40]Gottfried-Blackmore A, Sierra A, Jellinck PH, McEwen BS, Bulloch K, Brain microglia express steroid-converting enzymes in the mouse, The Journal of steroid biochemistry and molecular biology, 109 (2008) 96– 107. 18329265 PMC2423427
  38. [41]Berstein L, Larionov A, Poroshina T, Zimarina T, Leenman E, Aromatase (CYP19) expression in tumor-infiltrating lymphocytes and blood mononuclears, Journal of Cancer Research and Clinical Oncology, 128 (2002) 173– 176. 11935306 PMC12164450
  39. [43]Forero-Pena DA, Gutierrez FR, Statins as modulators of regulatory T-cell biology, Mediators Inflamm, 2013 (2013) 167086. 24222935 PMC3816059
  40. [44]Zeiser R, Immune modulatory effects of statins, Immunology, 154 (2018) 69– 75. 29392731 PMC5904709
  41. [45]Koch CA, Krabbe S, Hehmke B, Statins, metformin, proprotein-convertase-subtilisin-kexin type-9 (PCSK9) inhibitors and sex hormones: Immunomodulatory properties?, Rev Endocr Metab Disord, 19 (2018) 363– 395. 30673921
  42. [46]Filomenko R, Fourgeux C, Bretillon L, Gambert-Nicot S, Oxysterols: Influence on plasma membrane rafts microdomains and development of ocular diseases, Steroids, 99 (2015) 259– 265. 25683893
  43. [47]Raccosta L, Fontana R, Maggioni D, Lanterna C, Villablanca EJ, Paniccia A, Musumeci A, Chiricozzi E, Trincavelli ML, Daniele S, Martini C, Gustafsson J-A, Doglioni C, Feo SG, Leiva A, Ciampa MG, Mauri L, Sensi C, Prinetti A, Eberini I, Mora JR, Bordignon C, Steffensen KR, Sonnino S, Sozzani S, Traversari C, Russo V, The oxysterol–CXCR2 axis plays a key role in the recruitment of tumor-promoting neutrophils, The Journal of Experimental Medicine, 210 (2013) 1711. 23897983 PMC3754872
  44. [48]Ma L, Nelson ER, Oxysterols and nuclear receptors, Molecular and cellular endocrinology, (2019). 30660701
  45. [49]Villey I, de Chasseval R, de Villartay J-P, RORγT, a thymus-specific isoform of the orphan nuclear receptor RORγ / TOR, is up-regulated by signaling through the pre-T cell receptor and binds to the TEA promoter, 29 (1999) 4072– 4080. 10602018
  46. [50]Ivanov II, McKenzie BS, Zhou L, Tadokoro CE, Lepelley A, Lafaille JJ, Cua DJ, Littman DR, The Orphan Nuclear Receptor RORγt Directs the Differentiation Program of Proinflammatory IL-17+ T Helper Cells, Cell, 126 (2006) 1121– 1133. 16990136
  47. [51]Sun Z, Unutmaz D, Zou Y-R, Sunshine MJ, Pierani A, Brenner-Morton S, Mebius RE, Littman DR, Requirement for RORγ in Thymocyte Survival and Lymphoid Organ Development, 288 (2000) 2369– 2373. 10875923
  48. [52]Yang BH, Hagemann S, Mamareli P, Lauer U, Hoffmann U, Beckstette M, Föhse L, Prinz I, Pezoldt J, Suerbaum S, Sparwasser T, Hamann A, Floess S, Huehn J, Lochner M, Foxp3+ T cells expressing RORγt represent a stable regulatory T-cell effector lineage with enhanced suppressive capacity during intestinal inflammation, Mucosal Immunology, 9 (2015) 444. 26307665
  49. [53]Burris TP, Busby SA, Griffin PR, Targeting orphan nuclear receptors for treatment of metabolic diseases and autoimmunity, Chemistry & biology, 19 (2012) 51– 59. 22284354 PMC3269034
  50. [54]Solt LA, Burris TP, Action of RORs and their ligands in (patho)physiology, Trends in Endocrinology & Metabolism, 23 (2012) 619– 627. 22789990 PMC3500583
  51. [55]Wang Y, Kumar N, Crumbley C, Griffin PR, Burris TP, A second class of nuclear receptors for oxysterols: Regulation of RORalpha and RORgamma activity by 24S-hydroxycholesterol (cerebrosterol), Biochimica et biophysica acta, 1801 (2010) 917– 923. 20211758 PMC2886165
  52. [56]Jin L, Martynowski D, Zheng S, Wada T, Xie W, Li Y, Structural basis for hydroxycholesterols as natural ligands of orphan nuclear receptor RORgamma, Molecular endocrinology (Baltimore, Md.), 24 (2010) 923– 929. PMC2870936 20203100
  53. [57]Hu X, Wang Y, Hao L-Y, Liu X, Lesch CA, Sanchez BM, Wendling JM, Morgan RW, Aicher TD, Carter LL, Toogood PL, Glick GD, Sterol metabolism controls TH17 differentiation by generating endogenous RORγ agonists, Nature chemical biology, 11 (2015) 141. 25558972
  54. [58]Xue X, Soroosh P, De Leon-Tabaldo A, Luna-Roman R, Sablad M, Rozenkrants N, Yu J, Castro G, Banie H, Fung-Leung W-P, Santamaria-Babi L, Schlueter T, Albers M, Leonard K, Budelsky AL, Fourie AM, Pharmacologic modulation of RORγt translates to efficacy in preclinical and translational models of psoriasis and inflammatory arthritis, Scientific Reports, 6 (2016) 37977. 27905482 PMC5131364
  55. [59]and JJR, Mangelsdorf DJ, The Role of Orphan Nuclear Receptors in the Regulation of Cholesterol Homeostasis, 16 (2000) 459– 481. 11031244
  56. [60]Joseph SB, Bradley MN, Castrillo A, Bruhn KW, Mak PA, Pei L, Hogenesch J, O’Connell RM, Cheng G, Saez E, Miller JF, Tontonoz P, LXR-Dependent Gene Expression Is Important for Macrophage Survival and the Innate Immune Response, Cell, 119 (2004) 299– 309. 15479645
  57. [61]Hong C, Bradley MN, Rong X, Wang X, Wagner A, Grijalva V, Castellani LW, Salazar J, Realegeno S, Boyadjian R, Fogelman AM, Van Lenten BJ, Reddy ST, Lusis AJ, Tangirala RK, Tontonoz P, LXRα is uniquely required for maximal reverse cholesterol transport and atheroprotection in ApoE-deficient mice, Journal of lipid research, 53 (2012) 1126– 1133. 22454476 PMC3351819
  58. [62]Li P, Spann NJ, Kaikkonen MU, Lu M, Oh DY, Fox JN, Bandyopadhyay G, Talukdar S, Xu J, Lagakos WS, Patsouris D, Armando A, Quehenberger O, Dennis EA, Watkins SM, Auwerx J, Glass CK, Olefsky JM, NCoR repression of LXRs restricts macrophage biosynthesis of insulin-sensitizing omega 3 fatty acids, Cell, 155 (2013) 200– 214. 24074869 PMC4131699
  59. [64]Rong X, Albert Carolyn J., Hong C, Duerr Mark A., Chamberlain Brian T., Tarling Elizabeth J., Ito A, Gao J, Wang B, Edwards Peter A., Jung Michael E., Ford David A., Tontonoz P, LXRs Regulate ER Stress and Inflammation through Dynamic Modulation of Membrane Phospholipid Composition, Cell Metabolism, 18 (2013) 685– 697. 24206663 PMC3889491
  60. [65]Solt LA, Kamenecka TM, Burris TP, LXR-Mediated Inhibition of CD4+ T Helper Cells, PLOS ONE, 7 (2012) e46615. 23029557 PMC3460920
  61. [66]Herold M, Breuer J, Hucke S, Knolle P, Schwab N, Wiendl H, Klotz L, Liver X receptor activation promotes differentiation of regulatory T cells, PLOS ONE, 12 (2017) e0184985. 28926619 PMC5604992
  62. [67]Bensinger SJ, Bradley MN, Joseph SB, Zelcer N, Janssen EM, Hausner MA, Shih R, Parks JS, Edwards PA, Jamieson BD, Tontonoz P, LXR signaling couples sterol metabolism to proliferation in the acquired immune response, Cell, 134 (2008) 97– 111. 18614014 PMC2626438
  63. [68]Spann Nathanael J., Garmire Lana X., McDonald Jeffrey G., Myers David S., Milne Stephen B., Shibata N, Reichart D, Fox Jesse N., Shaked I, Heudobler D, Raetz Christian R.H., Wang Elaine W., Kelly Samuel L., Sullards MC, Murphy Robert C., Merrill Alfred H. Jr., Brown HA, Dennis Edward A., Li Andrew C., Ley K, Tsimikas S, Fahy E, Subramaniam S, Quehenberger O, Russell David W., Glass Christopher K., Regulated Accumulation of Desmosterol Integrates Macrophage Lipid Metabolism and Inflammatory Responses, Cell, 151 (2012) 138– 152. 23021221 PMC3464914
  64. [69]Makishima M, Okamoto AY, Repa JJ, Tu H, Learned RM, Luk A, Hull MV, Lustig KD, Mangelsdorf DJ, Shan B, Identification of a Nuclear Receptor for Bile Acids, Science, 284 (1999) 1362. 10334992
  65. [72]Fiorucci S, Biagioli M, Zampella A, Distrutti E, Bile Acids Activated Receptors Regulate Innate Immunity, 9 (2018). PMC6099188 30150987
  66. [74]Renga B, Mencarelli A, Cipriani S, D’Amore C, Carino A, Bruno A, Francisci D, Zampella A, Distrutti E, Fiorucci S, The bile acid sensor FXR is required for immune-regulatory activities of TLR-9 in intestinal inflammation, PLoS One, 8 (2013) e54472. 23372731 PMC3555871
  67. [75]Yuk JM, Shin DM, Lee HM, Kim JJ, Kim SW, Jin HS, Yang CS, Park KA, Chanda D, Kim DK, Huang SM, Lee SK, Lee CH, Kim JM, Song CH, Lee SY, Hur GM, Moore DD, Choi HS, Jo EK, The orphan nuclear receptor SHP acts as a negative regulator in inflammatory signaling triggered by Toll-like receptors, Nature immunology, 12 (2011) 742– 751. 21725320
  68. [76]Yang CS, Kim JJ, Kim TS, Lee PY, Kim SY, Lee HM, Shin DM, Nguyen LT, Lee MS, Jin HS, Kim KK, Lee CH, Kim MH, Park SG, Kim JM, Choi HS, Jo EK, Small heterodimer partner interacts with NLRP3 and negatively regulates activation of the NLRP3 inflammasome, Nat Commun, 6 (2015) 6115. 25655831 PMC4347017
  69. [77]Noh J-R, Kim Y-H, Kim D-K, Hwang JH, Kim K-S, Choi D-H, Lee S-J, Lee HG, Lee TG, Weng H-L, Dooley S, Choi H-S, Lee C-H, Small heterodimer partner negatively regulates C-X-C motif chemokine ligand 2 in hepatocytes during liver inflammation, Scientific Reports, 8 (2018) 15222. 30323351 PMC6189097
  70. [78]Hall JM, McDonnell DP, The Estrogen Receptor β-Isoform (ERβ) of the Human Estrogen Receptor Modulates ERα Transcriptional Activity and Is a Key Regulator of the Cellular Response to Estrogens and Antiestrogens1, Endocrinology, 140 (1999) 5566– 5578. 10579320
  71. [79]Pettersson K, Grandien K, Kuiper GGJM, Gustafsson J.-A.k., Mouse Estrogen Receptor β Forms Estrogen Response Element-Binding Heterodimers with Estrogen Receptor α, Molecular Endocrinology, 11 (1997) 1486– 1496. 9280064
  72. [80]Svoronos N, Perales-Puchalt A, Allegrezza MJ, Rutkowski MR, Payne KK, Tesone AJ, Nguyen JM, Curiel TJ, Cadungog MG, Singhal S, Eruslanov EB, Zhang P, Tchou J, Zhang R, Conejo-Garcia JR, Tumor Cell-Independent Estrogen Signaling Drives Disease Progression through Mobilization of Myeloid-Derived Suppressor Cells, Cancer Discov, 7 (2017) 72– 85. 27694385 PMC5222699
  73. [81]Svoronos N, Perales-Puchalt A, Allegrezza MJ, Rutkowski MR, Payne KK, Tesone AJ, Nguyen JM, Curiel TJ, Cadungog MG, Singhal S, Eruslanov EB, Zhang P, Tchou J, Zhang R, Conejo-Garcia JR, Tumor Cell–Independent Estrogen Signaling Drives Disease Progression through Mobilization of Myeloid-Derived Suppressor Cells, 7 (2017) 72– 85. PMC5222699 27694385
  74. [82]Saijo K, Collier Jana G., Li Andrew C., Katzenellenbogen John A., Glass Christopher K., An ADIOL-ERβ-CtBP Transrepression Pathway Negatively Regulates Microglia-Mediated Inflammation, Cell, 145 (2011) 584– 595. 21565615 PMC3433492
  75. [84]Offner H, Adlard K, Zamora A, Vandenbark AA, Estrogen potentiates treatment with T-cell receptor protein of female mice with experimental encephalomyelitis, The Journal of clinical investigation, 105 (2000) 1465– 1472. 10811854 PMC315468
  76. [85]Lélu K, Laffont S, Delpy L, Paulet P-E, Périnat T, Tschanz SA, Pelletier L, Engelhardt B, Guéry J-C, Estrogen Receptor α Signaling in T Lymphocytes Is Required for Estradiol-Mediated Inhibition of Th1 and Th17 Cell Differentiation and Protection against Experimental Autoimmune Encephalomyelitis, (2011) 1101578. 21810607
  77. [86]Gourdy P, Araujo LM, Zhu R, Garmy-Susini B, Diem S, Laurell H, Leite-de-Moraes M, Dy M, Arnal JF, Bayard F, Herbelin A, Relevance of sexual dimorphism to regulatory T cells: estradiol promotes IFN-γ production by invariant natural killer T cells, 105 (2005) 2415– 2420. 15383462
  78. [87]Mohammad I, Starskaia I, Nagy T, Guo J, Yatkin E, Väänänen K, Watford WT, Chen Z, Estrogen receptor α contributes to T cell–mediated autoimmune inflammation by promoting T cell activation and proliferation, 11 (2018) eaap9415. 29666308
  79. [88]Bernardi AI, Andersson A, Stubelius A, Grahnemo L, Carlsten H, Islander U, Selective estrogen receptor modulators in T cell development and T cell dependent inflammation, Immunobiology, 220 (2015) 1122– 1128. 26044996
  80. [89]DuSell CD, Umetani M, Shaul PW, Mangelsdorf DJ, McDonnell DP, 27-hydroxycholesterol is an endogenous selective estrogen receptor modulator, Mol Endocrinol, 22 (2008) 65– 77. 17872378 PMC2194632
  81. [90]Umetani M, Domoto H, Gormley AK, Yuhanna IS, Cummins CL, Javitt NB, Korach KS, Shaul PW, Mangelsdorf DJ, 27-Hydroxycholesterol is an endogenous SERM that inhibits the cardiovascular effects of estrogen, Nat Med, 13 (2007) 1185– 1192. 17873880
  82. [91]Nelson ER, Wardell SE, Jasper JS, Park S, Suchindran S, Howe MK, Carver NJ, Pillai RV, Sullivan PM, Sondhi V, Umetani M, Geradts J, McDonnell DP, 27-Hydroxycholesterol links hypercholesterolemia and breast cancer pathophysiology, Science, 342 (2013) 1094– 1098. 24288332 PMC3899689
  83. [92]Wu Q, Ishikawa T, Sirianni R, Tang H, McDonald JG, Yuhanna IS, Thompson B, Girard L, Mineo C, Brekken RA, Umetani M, Euhus DM, Xie Y, Shaul PW, 27-Hydroxycholesterol promotes cell-autonomous, ER-positive breast cancer growth, Cell reports, 5 (2013) 637– 645. 24210818 PMC3950897
  84. [93]Baek AE, Yu YA, He S, Wardell SE, Chang CY, Kwon S, Pillai RV, McDowell HB, Thompson JW, Dubois LG, Sullivan PM, Kemper JK, Gunn MD, McDonnell DP, Nelson ER, The cholesterol metabolite 27 hydroxycholesterol facilitates breast cancer metastasis through its actions on immune cells, Nat Commun, 8 (2017) 864. 29021522 PMC5636879
  85. [95]Baek AE, Nelson ER, The Contribution of Cholesterol and Its Metabolites to the Pathophysiology of Breast Cancer, Horm Cancer, 7 (2016) 219– 228. 27020054 PMC4930376
  86. [96]Fu X, Menke JG, Chen Y, Zhou G, MacNaul KL, Wright SD, Sparrow CP, Lund EG, 27-hydroxycholesterol is an endogenous ligand for liver X receptor in cholesterol-loaded cells, J Biol Chem, 276 (2001) 38378– 38387. 11504730
  87. [97]Raccosta L, Fontana R, Maggioni D, Lanterna C, Villablanca EJ, Paniccia A, Musumeci A, Chiricozzi E, Trincavelli ML, Daniele S, Martini C, Gustafsson JA, Doglioni C, Feo SG, Leiva A, Ciampa MG, Mauri L, Sensi C, Prinetti A, Eberini I, Mora JR, Bordignon C, Steffensen KR, Sonnino S, Sozzani S, Traversari C, Russo V, The oxysterol-CXCR2 axis plays a key role in the recruitment of tumor-promoting neutrophils, J Exp Med, 210 (2013) 1711– 1728. 23897983 PMC3754872
  88. [98]Nissen RM, Yamamoto KR, The glucocorticoid receptor inhibits NFκB by interfering with serine-2 phosphorylation of the RNA polymerase II carboxy-terminal domain, 14 (2000) 2314– 2329. PMC316928 10995388
  89. [99]Voisin M, de Medina P, Mallinger A, Dalenc F, Huc-Claustre E, Leignadier J, Serhan N, Soules R, Ségala G, Mougel A, Noguer E, Mhamdi L, Bacquié E, Iuliano L, Zerbinati C, Lacroix-Triki M, Chaltiel L, Filleron T, Cavaillès V, Al Saati T, Rochaix P, Duprez-Paumier R, Franchet C, Ligat L, Lopez F, Record M, Poirot M, Silvente-Poirot S, Identification of a tumor-promoter cholesterol metabolite in human breast cancers acting through the glucocorticoid receptor, 114 (2017) E9346– E9355. PMC5676900 29078321
  90. [100]Ricote M, Li AC, Willson TM, Kelly CJ, Glass CK, The peroxisome proliferator-activated receptor-γ is a negative regulator of macrophage activation, Nature, 391 (1998) 79. 9422508
  91. [101]Hall JM, McDonnell DP, The Molecular Mechanisms Underlying the Proinflammatory Actions of Thiazolidinediones in Human Macrophages, Molecular Endocrinology, 21 (2007) 1756– 1768. 17488971
  92. [102]Jones JR, Barrick C, Kim K-A, Lindner J, Blondeau B, Fujimoto Y, Shiota M, Kesterson RA, Kahn BB, Magnuson MA, Deletion of PPARγ in adipose tissues of mice protects against high fat diet-induced obesity and insulin resistance, 102 (2005) 6207– 6212. PMC556131 15833818
  93. [103]Lehrke M, Lazar MA, The Many Faces of PPARγ, Cell, 123 (2005) 993– 999. 16360030
  94. [104]Ricote M, Glass CK, New roles for PPARs in cholesterol homeostasis, Trends in Pharmacological Sciences, 22 (2001) 441– 443. 11543857
  95. [106]Baker AD, Malur A, Barna BP, Kavuru MS, Malur AG, Thomassen MJ, PPARγ regulates the expression of cholesterol metabolism genes in alveolar macrophages, Biochemical and Biophysical Research Communications, 393 (2010) 682– 687. 20170635
  96. [107]Giguère V, Transcriptional Control of Energy Homeostasis by the Estrogen-Related Receptors, Endocrine Reviews, 29 (2008) 677– 696. 18664618
  97. [108]Sonoda J, Laganière J, Mehl IR, Barish GD, Chong L-W, Li X, Scheffler IE, Mock DC, Bataille AR, Robert F, Lee C-H, Giguère V, Evans RM, Nuclear receptor ERR alpha and coactivator PGC-1 beta are effectors of IFN-gamma-induced host defense, Genes & development, 21 (2007) 1909– 1920. 17671090 PMC1935029
  98. [109]Yuk J-M, Kim Tae S., Kim Soo Y., Lee H-M, Han J, Dufour Catherine R., Kim Jin K., Jin Hyo S., Yang C-S, Park K-S, Lee C-H, Kim J-M, Kweon Gi R., Choi H-S, Vanacker J-M, Moore David D., Giguère V, Jo E-K, Orphan Nuclear Receptor ERRα Controls Macrophage Metabolic Signaling and A20 Expression to Negatively Regulate TLR-Induced Inflammation, Immunity, 43 (2015) 80– 91. 26200012
  99. [110]Michalek RD, Gerriets VA, Nichols AG, Inoue M, Kazmin D, Chang C-Y, Dwyer MA, Nelson ER, Pollizzi KN, Ilkayeva O, Giguere V, Zuercher WJ, Powell JD, Shinohara ML, McDonnell DP, Rathmell JC, Estrogen-related receptor-α is a metabolic regulator of effector T-cell activation and differentiation, Proceedings of the National Academy of Sciences of the United States of America, 108 (2011) 18348– 18353. 22042850 PMC3215012
  100. [111]Wei W, Schwaid Adam G., Wang X, Wang X, Chen S, Chu Q, Saghatelian A, Wan Y, Ligand Activation of ERRα by Cholesterol Mediates Statin and Bisphosphonate Effects, Cell Metabolism, 23 (2016) 479– 491. 26777690 PMC4785078
  101. [112]Chisamore MJ, Cunningham ME, Flores O, Wilkinson HA, Chen JD, Characterization of a novel small molecule subtype specific estrogen-related receptor alpha antagonist in MCF-7 breast cancer cells, PLoS One, 4 (2009) e5624. 19462000 PMC2680043
  102. [113]Wu F, Wang J, Wang Y, Kwok TT, Kong SK, Wong C, Estrogen-related receptor alpha (ERRalpha) inverse agonist XCT-790 induces cell death in chemotherapeutic resistant cancer cells, Chem Biol Interact, 181 (2009) 236– 242. 19464277
  103. [114]de Medina P, Paillasse MR, Segala G, Voisin M, Mhamdi L, Dalenc F, Lacroix-Triki M, Filleron T, Pont F, Saati TA, Morisseau C, Hammock BD, Silvente-Poirot S, Poirot M, Dendrogenin A arises from cholesterol and histamine metabolism and shows cell differentiation and anti-tumour properties, Nature Communications, 4 (2013) 1840. PMC3674249 23673625

Cited by

Sorted by citations

Authors
Shahoei, S. H., & Nelson, E. R.
Affiliations
University of Illinois Urbana-Champaign (US)
Corresponding author
Nelson, Erik R.
Venue
The Journal of Steroid Biochemistry and Molecular Biology
Publisher
Elsevier BV
Published
2019-07
Volume
191
Pages
105364
ISSN
0960-0760 (ISSN-L)
OpenAlex
W2936573240
Cited by
43
References
11
Citations by year
2026: 4 · 2025: 4 · 2024: 4 · 2023: 11 · 2022: 7 · 2021: 5 · 2020: 7 · 2019: 1
FWCI
1.03
Type
journal article
Language
en
Open access
Locations
  • The Journal of Steroid Biochemistry and Molecular Biology (acceptedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • U.S. Department of Defense
  • National Institutes of Health
Topics
  • Health Sciences › Medicine › Surgery › Cholesterol and Lipid Metabolism
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Steroid Chemistry and Biochemistry
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sphingolipid Metabolism and Signaling
Keywords
nuclear receptors, cholesterol homeostasis, bile acid homeostasis, cholesterol metabolites, immune regulation, membrane fluidity, lipid rafts, protein prenylation, signaling molecules
MeSH terms
Animals, Cholesterol, Homeostasis, Humans, Immune System, Immunity, Receptors, Cytoplasmic and Nuclear

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review