Nuclear receptors as regulators of stem cell and cancer stem cell metabolism

Seminars in Cell and Developmental Biology

Volumn 24, Issue 10-12, 2013, Pages 716-723

  Simandi, Zoltan ^a   Cuaranta Monroy, Ixchelt ^a   Nagy, Laszlo ^a,b  

^a UNIVERSITY OF DEBRECEN   (Hungary)

^b UNIVERSITY OF DEBRECEN   (Hungary)

Author keywords

Cancer stem cells; Embryonic stem cells; Metabolism; Nuclear receptors; Pluripotency

Indexed keywords

6 PHOSPHOFRUCTOKINASE; CARBAMOYL PHOSPHATE SYNTHASE; CELL NUCLEUS RECEPTOR; FRUCTOSE BISPHOSPHATE ALDOLASE; GLUCOSE 6 PHOSPHATE ISOMERASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; HYPOXIA INDUCIBLE FACTOR; LIVER RECEPTOR HOMOLOG 1; LIVER X RECEPTOR; NUCLEAR RECEPTOR DAX 1; PHOSPHOGLYCERATE KINASE; PYRIMIDINE NUCLEOTIDE; PYRUVATE DEHYDROGENASE; PYRUVATE DEHYDROGENASE COMPLEX; PYRUVATE DEHYDROGENASE KINASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; RETINOIC ACID; RETINOID X RECEPTOR; RIBOSEPHOSPHATE PYROPHOSPHOKINASE; TRIOSEPHOSPHATE ISOMERASE;

AMINO ACID METABOLISM; BILE ACID METABOLISM; BINDING SITE; BROWN ADIPOSE TISSUE; CANCER STEM CELL; CARBOHYDRATE METABOLISM; CELL METABOLISM; CELL PROLIFERATION; CHOLESTEROL METABOLISM; DNA SEQUENCE; EMBRYO DEVELOPMENT; EMBRYONAL CARCINOMA STEM CELL; EMBRYONIC STEM CELL; ENDOMETRIUM CANCER; FATTY ACID OXIDATION; FATTY ACID SYNTHESIS; GENE DISRUPTION; GENE EXPRESSION; GLUCONEOGENESIS; GLUCOSE METABOLISM; GLUCOSE OXIDATION; GLYCOLYSIS; GONAD DEVELOPMENT; HUMAN; LIPID METABOLISM; LIPOGENESIS; MITOCHONDRION; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXYGEN TENSION; PENTOSE PHOSPHATE CYCLE; PLURIPOTENT STEM CELL; PROTEIN LOCALIZATION; PROTEIN TARGETING; REGULATORY DNA SEQUENCE; REVIEW; SIGNAL TRANSDUCTION; STEM CELL; UPREGULATION;

CANCER STEM CELLS; EMBRYONIC STEM CELLS; METABOLISM; NUCLEAR RECEPTORS; PLURIPOTENCY;

ANIMALS; HUMANS; MODELS, BIOLOGICAL; NEOPLASTIC STEM CELLS; PLURIPOTENT STEM CELLS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; STEM CELLS;

EID: 84888341755     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2013.10.002     Document Type: Review

References (84)

1. Lu C., Thompson C.B. Metabolic regulation of epigenetics. Cell Metab 2012, 16:9-17.
2. Chung S., Dzeja P.P., Faustino R.S., Perez-Terzic C., Behfar A., Terzic A. Mitochondrial oxidative metabolism is required for the cardiac differentiation of stem cells. Nat Clin Pract Cardiovasc Med 2007, 4(Suppl. 1):S60-S67.
3. Cho Y.M., Kwon S., Pak Y.K., Seol H.W., Choi Y.M., Park do J., et al. Dynamic changes in mitochondrial biogenesis and antioxidant enzymes during the spontaneous differentiation of human embryonic stem cells. Biochem Biophys Res Commun 2006, 348:1472-1478.
4. Wang J., Alexander P., Wu L., Hammer R., Cleaver O., McKnight S.L. Dependence of mouse embryonic stem cells on threonine catabolism. Science 2009, 325:435-439.
5. Evans M.J., Kaufman M.H. Establishment in culture of pluripotential cells from mouse embryos. Nature 1981, 292:154-156.
6. Folmes C.D., Dzeja P.P., Nelson T.J., Terzic A. Metabolic plasticity in stem cell homeostasis and differentiation. Cell Stem Cell 2012, 11:596-606.
7. 2 tensions and the prevention of differentiation of hES cells. Proc Natl Acad Sci USA 2005, 102:4783-4788.
8. Westfall S.D., Sachdev S., Das P., Hearne L.B., Hannink M., Roberts R.M., et al. Identification of oxygen-sensitive transcriptional programs in human embryonic stem cells. Stem Cells Dev 2008, 17:869-881.
9. Yoshida Y., Takahashi K., Okita K., Ichisaka T., Yamanaka S. Hypoxia enhances the generation of induced pluripotent stem cells. Cell Stem Cell 2009, 5:237-241.
10. Covello K.L., Kehler J., Yu H., Gordan J.D., Arsham A.M., Hu C.J., et al. HIF-2alpha regulates Oct-4: effects of hypoxia on stem cell function, embryonic development, and tumor growth. Genes Dev 2006, 20:557-570.
11. Kim J.W., Tchernyshyov I., Semenza G.L., Dang C.V. HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab 2006, 3:177-185.
12. Forristal C.E., Christensen D.R., Chinnery F.E., Petruzzelli R., Parry K.L., Sanchez-Elsner T., et al. Environmental oxygen tension regulates the energy metabolism and self-renewal of human embryonic stem cells. PLoS ONE 2013, 8:e62507.
13. Yanes O., Clark J., Wong D.M., Patti G.J., Sanchez-Ruiz A., Benton H.P., et al. Metabolic oxidation regulates embryonic stem cell differentiation. Nat Chem Biol 2010, 6:411-417.
14. Knobloch M., Braun S.M., Zurkirchen L., von Schoultz C., Zamboni N., Arauzo-Bravo M.J., et al. Metabolic control of adult neural stem cell activity by Fasn-dependent lipogenesis. Nature 2013, 493:226-230.
15. Shyh-Chang N., Locasale J.W., Lyssiotis C.A., Zheng Y., Teo R.Y., Ratanasirintrawoot S., et al. Influence of threonine metabolism on S-adenosylmethionine and histone methylation. Science 2013, 339:222-226.
16. Sonoda J., Pei L., Evans R.M. Nuclear receptors: decoding metabolic disease. FEBS Lett 2008, 582:2-9.
17. Wagner R.T., Cooney A.J. Minireview: the diverse roles of nuclear receptors in the regulation of embryonic stem cell pluripotency. Mol Endocrinol 2013, 27:864-878.
18. Xie C.Q., Jeong Y., Fu M., Bookout A.L., Garcia-Barrio M.T., Sun T., et al. Expression profiling of nuclear receptors in human and mouse embryonic stem cells. Mol Endocrinol 2009, 23:724-733.
19. Simandi Z., Balint B.L., Poliska S., Ruhl R., Nagy L. Activation of retinoic acid receptor signaling coordinates lineage commitment of spontaneously differentiating mouse embryonic stem cells in embryoid bodies. FEBS Lett 2010, 584:3123-3130.
20. Sablin E.P., Woods A., Krylova I.N., Hwang P., Ingraham H.A., Fletterick R.J. The structure of corepressor Dax-1 bound to its target nuclear receptor LRH-1. Proc Natl Acad Sci USA 2008, 105:18390-18395.
21. Guo W., Burris T.P., McCabe E.R. Expression of DAX-1, the gene responsible for X-linked adrenal hypoplasia congenita and hypogonadotropic hypogonadism, in the hypothalamic-pituitary-adrenal/gonadal axis. Biochem Mol Med 1995, 56:8-13.
22. Iyer A.K., McCabe E.R. Molecular mechanisms of DAX1 action. Mol Genet Metab 2004, 83:60-73.
23. Achermann J.C., Meeks J.J., Jameson J.L. Phenotypic spectrum of mutations in DAX-1 and SF-1. Mol Cell Endocrinol 2001, 185:17-25.
24. Khalfallah O., Rouleau M., Barbry P., Bardoni B., Lalli E. Dax-1 knockdown in mouse embryonic stem cells induces loss of pluripotency and multilineage differentiation. Stem Cells 2009, 27:1529-1537.
25. Kim J., Chu J., Shen X., Wang J., Orkin S.H. An extended transcriptional network for pluripotency of embryonic stem cells. Cell 2008, 132:1049-1061.
26. Pare J.F., Malenfant D., Courtemanche C., Jacob-Wagner M., Roy S., Allard D., et al. The fetoprotein transcription factor (FTF) gene is essential to embryogenesis and cholesterol homeostasis and is regulated by a DR4 element. J Biol Chem 2004, 279:21206-21216.
27. Fayard E., Auwerx J., Schoonjans K. LRH-1: an orphan nuclear receptor involved in development, metabolism and steroidogenesis. Trends Cell Biol 2004, 14:250-260.
28. Oosterveer M.H., Mataki C., Yamamoto H., Harach T., Moullan N., van Dijk T.H., et al. LRH-1-dependent glucose sensing determines intermediary metabolism in liver. J Clin Invest 2012, 122:2817-2826.
29. Labelle-Dumais C., Jacob-Wagner M., Pare J.F., Belanger L., Dufort D. Nuclear receptor NR5A2 is required for proper primitive streak morphogenesis. Dev Dyn 2006, 235:3359-3369.
30. Wang W., Yang J., Liu H., Lu D., Chen X., Zenonos Z., et al. Rapid and efficient reprogramming of somatic cells to induced pluripotent stem cells by retinoic acid receptor gamma and liver receptor homolog 1. Proc Natl Acad Sci USA 2011, 108:18283-18288.
31. Heng J.C., Feng B., Han J., Jiang J., Kraus P., Ng J.H., et al. The nuclear receptor Nr5a2 can replace Oct4 in the reprogramming of murine somatic cells to pluripotent cells. Cell Stem Cell 2009, 6:167-174.
32. Busby S., Nuhant P., Cameron M., Mercer B.A., Hodder P., Roush W.R., et al. Discovery of Inverse Agonists for the Liver Receptor Homologue-1 (LRH1; NR5A2) 2010.
33. Giguere V., Yang N., Segui P., Evans R.M. Identification of a new class of steroid hormone receptors. Nature 1988, 331:91-94.
34. Poidatz D., Dos Santos E., Brule A., De Mazancourt P., Dieudonne M.N. Estrogen-related receptor gamma modulates energy metabolism target genes in human trophoblast. Placenta 2012, 33:688-695.
35. Kim D.K., Ryu D., Koh M., Lee M.W., Lim D., Kim M.J., et al. Orphan nuclear receptor estrogen-related receptor gamma (ERRgamma) is key regulator of hepatic gluconeogenesis. J Biol Chem 2012, 287:21628-21639.
36. Martello G., Sugimoto T., Diamanti E., Joshi A., Hannah R., Ohtsuka S., et al. Esrrb is a pivotal target of the Gsk3/Tcf3 axis regulating embryonic stem cell self-renewal. Cell Stem Cell 2012, 11:491-504.
37. Festuccia N., Osorno R., Halbritter F., Karwacki-Neisius V., Navarro P., Colby D., et al. Esrrb is a direct Nanog target gene that can substitute for Nanog function in pluripotent cells. Cell Stem Cell 2012, 11:477-490.
38. Feng B., Jiang J., Kraus P., Ng J.H., Heng J.C., Chan Y.S., et al. Reprogramming of fibroblasts into induced pluripotent stem cells with orphan nuclear receptor Esrrb. Nat Cell Biol 2009, 11:197-203.
39. Chen X., Xu H., Yuan P., Fang F., Huss M., Vega V.B., et al. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 2008, 133:1106-1117.
40. Sem D.S., Casimiro D.R., Kliewer S.A., Provencal J., Evans R.M., Wright P.E. NMR spectroscopic studies of the DNA-binding domain of the monomer-binding nuclear orphan receptor, human estrogen related receptor-2. The carboxyl-terminal extension to the zinc-finger region is unstructured in the free form of the protein. J Biol Chem 1997, 272:18038-18043.
41. Tang Q., Chen Y., Meyer C., Geistlinger T., Lupien M., Wang Q., et al. A comprehensive view of nuclear receptor cancer cistromes. Cancer Res 2011, 71:6940-6947.
42. Shyr C.R., Kang H.Y., Tsai M.Y., Liu N.C., Ku P.Y., Huang K.E., et al. Roles of testicular orphan nuclear receptors 2 and 4 in early embryonic development and embryonic stem cells. Endocrinology 2009, 150:2454-2462.
43. Collins L.L., Lee Y.F., Heinlein C.A., Liu N.C., Chen Y.T., Shyr C.R., et al. Growth retardation and abnormal maternal behavior in mice lacking testicular orphan nuclear receptor 4. Proc Natl Acad Sci USA 2004, 101:15058-15063.
44. Kim E., Xie S., Yeh S.D., Lee Y.F., Collins L.L., Hu Y.C., et al. Disruption of TR4 orphan nuclear receptor reduces the expression of liver apolipoprotein E/C-I/C-II gene cluster. J Biol Chem 2003, 278:46919-46926.
45. Yan Z.H., Karam W.G., Staudinger J.L., Medvedev A., Ghanayem B.I., Jetten A.M. Regulation of peroxisome proliferator-activated receptor alpha-induced transactivation by the nuclear orphan receptor TAK1/TR4. J Biol Chem 1998, 273:10948-10957.
46. Liu N.C., Lin W.J., Kim E., Collins L.L., Lin H.Y., Yu I.C., et al. Loss of TR4 orphan nuclear receptor reduces phosphoenolpyruvate carboxykinase-mediated gluconeogenesis. Diabetes 2007, 56:2901-2909.
47. O'Geen H., Lin Y.H., Xu X., Echipare L., Komashko V.M., He D., et al. Genome-wide binding of the orphan nuclear receptor TR4 suggests its general role in fundamental biological processes. BMC Genomics 2010, 11:689.
48. Flaig R., Greschik H., Peluso-Iltis C., Moras D. Structural basis for the cell-specific activities of the NGFI-B and the Nurr1 ligand-binding domain. J Biol Chem 2005, 280:19250-19258.
49. Chao L.C., Wroblewski K., Zhang Z., Pei L., Vergnes L., Ilkayeva O.R., et al. Insulin resistance and altered systemic glucose metabolism in mice lacking Nur77. Diabetes 2009, 58:2788-2796.
50. Zhang P., Hu Y., Yang J., Zheng L., Wang Q. The orphan nuclear receptor Nur77 regulates hepatic cholesterol metabolism through the suppression of LDLR and HMGCR expression. Mol Med Rep 2012, 5:1541-1547.
51. Soprano D.R., Teets B.W., Soprano K.J. Role of retinoic acid in the differentiation of embryonal carcinoma and embryonic stem cells. Vitam Horm 2007, 75:69-95.
52. Lane M.A., Chen A.C., Roman S.D., Derguini F., Gudas L.J. Removal of LIF (leukemia inhibitory factor) results in increased vitamin A (retinol) metabolism to 4-oxoretinol in embryonic stem cells. Proc Natl Acad Sci USA 1999, 96:13524-13529.
53. Weston A.D., Blumberg B., Underhill T.M. Active repression by unliganded retinoid receptors in development: less is sometimes more. J Cell Biol 2003, 161:223-228.
54. Delacroix L., Moutier E., Altobelli G., Legras S., Poch O., Choukrallah M.A., et al. Cell-specific interaction of retinoic acid receptors with target genes in mouse embryonic fibroblasts and embryonic stem cells. Mol Cell Biol 2010, 30:231-244.
55. Willy P.J., Umesono K., Ong E.S., Evans R.M., Heyman R.A., Mangelsdorf D.J. LXR, a nuclear receptor that defines a distinct retinoid response pathway. Genes Dev 1995, 9:1033-1045.
56. Calkin A.C., Tontonoz P. Transcriptional integration of metabolism by the nuclear sterol-activated receptors LXR and FXR. Nat Rev Mol Cell Biol 2012, 13:213-224.
57. Annicotte J.S., Schoonjans K., Auwerx J. Expression of the liver X receptor alpha and beta in embryonic and adult mice. Anat Rec A Discov Mol Cell Evol Biol 2004, 277:312-316.
58. Alberti S., Schuster G., Parini P., Feltkamp D., Diczfalusy U., Rudling M., et al. Hepatic cholesterol metabolism and resistance to dietary cholesterol in LXRbeta-deficient mice. J Clin Invest 2001, 107:565-573.
59. Steffensen K.R., Robertson K., Gustafsson J.A., Andersen C.Y. Reduced fertility and inability of oocytes to resume meiosis in mice deficient of the Lxr genes. Mol Cell Endocrinol 2006, 256:9-16.
60. Laffitte B.A., Chao L.C., Li J., Walczak R., Hummasti S., Joseph S.B., et al. Activation of liver X receptor improves glucose tolerance through coordinate regulation of glucose metabolism in liver and adipose tissue. Proc Natl Acad Sci USA 2003, 100:5419-5424.
61. Boergesen M., Pedersen T.A., Gross B., van Heeringen S.J., Hagenbeek D., Bindesboll C., et al. Genome-wide profiling of liver X receptor, retinoid X receptor, and peroxisome proliferator-activated receptor alpha in mouse liver reveals extensive sharing of binding sites. Mol Cell Biol 2011, 32:852-867.
62. Huq M.D., Tsai N.P., Gupta P., Wei L.N. Regulation of retinal dehydrogenases and retinoic acid synthesis by cholesterol metabolites. EMBO J 2006, 25:3203-3213.
63. Wang X., Penzes P., Napoli J.L. Cloning of a cDNA encoding an aldehyde dehydrogenase and its expression in Escherichia coli. Recognition of retinal as substrate. J Biol Chem 1996, 271:16288-16293.
64. Clevers H. The cancer stem cell: premises, promises and challenges. Nat Med 2011, 17:313-319.
65. Jordan C.T., Guzman M.L., Noble M. Cancer stem cells. N Engl J Med 2006, 355:1253-1261.
66. Magee J.A., Piskounova E., Morrison S.J. Cancer stem cells: impact, heterogeneity, and uncertainty. Cancer Cell 2012, 21:283-296.
67. Quail D.F., Taylor M.J., Postovit L.M. Microenvironmental regulation of cancer stem cell phenotypes. Curr Stem Cell Res Ther 2012, 7:197-216.
68. Warburg O. On the origin of cancer cells. Science 1956, 123:309-314.
69. Gonzalez I.R., Moreno-Manzano V., Rodriguez-Jimenez F.J., Sepulveda P., Sanchez-Puelles J.M. The biology of HIFalpha proteins in cell differentiation and disease. Vitam Horm 2011, 87:367-379.
70. Visvader J.E., Lindeman G.J. Cancer stem cells: current status and evolving complexities. Cell Stem Cell 2012, 10:717-728.
71. Chand A.L., Herridge K.A., Thompson E.W., Clyne C.D. The orphan nuclear receptor LRH-1 promotes breast cancer motility and invasion. Endocr Relat Cancer 2010, 17:965-975.
72. Dube C., Bergeron F., Vaillant M.J., Robert N.M., Brousseau C., Tremblay J.J. The nuclear receptors SF1 and LRH1 are expressed in endometrial cancer cells and regulate steroidogenic gene transcription by cooperating with AP-1 factors. Cancer Lett 2009, 275:127-138.
73. Benod C., Vinogradova M.V., Jouravel N., Kim G.E., Fletterick R.J., Sablin E.P. Nuclear receptor liver receptor homologue 1 (LRH-1) regulates pancreatic cancer cell growth and proliferation. Proc Natl Acad Sci USA 2011, 108:16927-16931.
74. Lalli E., Alonso J. Targeting DAX-1 in embryonic stem cells and cancer. Expert Opin Ther Targets 2010, 14:169-177.
75. Hah N., Kraus W.L. Hormone-regulated transcriptomes: lessons learned from estrogen signaling pathways in breast cancer cells. Mol Cell Endocrinol 2013 Jun 28, pii: S0303-7207(13)00268-2. doi:10.1016/j.mce.2013.06.021 [Epub ahead of print].
76. de Weille J., Fabre C., Bakalara N. Oxysterols in cancer cell proliferation and death. Biochem Pharmacol 2013, 86:154-160.
77. Guo D., Reinitz F., Youssef M., Hong C., Nathanson D., Akhavan D., et al. An LXR agonist promotes glioblastoma cell death through inhibition of an EGFR/AKT/SREBP-1/LDLR-dependent pathway. Cancer Discov 2011, 1:442-456.
78. Moschetta A. Nuclear receptor LXR as a novel therapeutic antitumoral target in glioblastoma. Cancer Discov 2011, 1:381-382.
79. Papi A., Guarnieri T., Storci G., Santini D., Ceccarelli C., Taffurelli M., et al. Nuclear receptors agonists exert opposing effects on the inflammation dependent survival of breast cancer stem cells. Cell Death Differ 2012, 19:1208-1219.
80. Nguyen-Vu T., Vedin L.L., Liu K., Jonsson P., Lin J.Z., Candelaria N.R., et al. Liver X receptor ligands disrupt breast cancer cell proliferation through an E2F-mediated mechanism. Breast Cancer Res 2013, 15:R51.
81. Lapidot T., Sirard C., Vormoor J., Murdoch B., Hoang T., Caceres-Cortes J., et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 1994, 367:645-648.
82. Bonnet D., Dick J.E. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 1997, 3:730-737.
83. Hope K.J., Jin L., Dick J.E. Acute myeloid leukemia originates from a hierarchy of leukemic stem cell classes that differ in self-renewal capacity. Nat Immunol 2004, 5:738-743.
84. Alcalay M., Meani N., Gelmetti V., Fantozzi A., Fagioli M., Orleth A., et al. Acute myeloid leukemia fusion proteins deregulate genes involved in stem cell maintenance and DNA repair. J Clin Investig 2003, 112:1751-1761.