Prospero-related homeobox 1 (Prox1) functions as a novel modulator of retinoic acid-related orphan receptors α- and γ-mediated transactivation

Nucleic Acids Research

Volumn 41, Issue 14, 2013, Pages 6992-7008

  Takeda, Yukimasa ^a   Jetten, Anton M ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRYPTOCHROME 1; DNA; HISTONE; HOMEODOMAIN PROTEIN; NEURONAL PAS DOMAIN PROTEIN 2; PROSPERO RELATED HOMEOBOX 1; PROTEIN BMAL1; RECEPTOR BLOCKING AGENT; RETINOID RELATED ORPHAN RECEPTOR ALPHA; RETINOID RELATED ORPHAN RECEPTOR GAMMA; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR CLOCK; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA RESPONSIVE ELEMENT; FEEDBACK SYSTEM; GENE TARGETING; HEPATOMA CELL; HISTONE ACETYLATION; HUMAN; HUMAN CELL; LIVER PARENCHYMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN TRANSPORT; RNA INTERFERENCE; SEQUENCE ANALYSIS; TRANSACTIVATION; TRANSCRIPTION REGULATION;

ANIMALS; CELL LINE, TUMOR; CELL NUCLEUS; CIRCADIAN CLOCKS; HEK293 CELLS; HOMEODOMAIN PROTEINS; HUMANS; LIVER; MICE; MICE, NEUROLOGIC MUTANTS; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP F, MEMBER 1; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP F, MEMBER 3; PROTEIN INTERACTION DOMAINS AND MOTIFS; REPRESSOR PROTEINS; TRANSCRIPTIONAL ACTIVATION; TUMOR SUPPRESSOR PROTEINS;

EID: 84881488679     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt447     Document Type: Article

References (67)

1. Kallen J.A., Schlaeppi J.M., Bitsch F., Geisse S., Geiser M., Delhon I. and Fournier B. (2002) X-ray structure of the hRORalpha LBD at 1.63 A: Structural and functional data that cholesterol or a cholesterol derivative is the natural ligand of RORalpha. Structure, 10, 1697-1707
2. Jetten A.M. (2011) Immunology: A helping hand against autoimmunity. Nature, 472, 421-422
3. Solt L.A., Wang Y., Banerjee S., Hughes T., Kojetin D.J., Lundasen T., Shin Y., Liu J., Cameron M.D., Noel R. et al. (2012) Regulation of circadian behaviour and metabolism by synthetic REV-ERB agonists. Nature, 485, 62-68
4. Jetten A.M. (2009) Retinoid-related orphan receptors (RORs): Critical roles in development, immunity, circadian rhythm, and cellular metabolism. Nucl. Recept. Signal., 7, e003
5. Huh J.R. and Littman D.R. (2012) Small molecule inhibitors of RORgammat: Targeting Th17 cells and other applications. Eur. J. Immunol., 42, 2232-2237
6. Sato T.K., Panda S., Miraglia L.J., Reyes T.M., Rudic R.D., McNamara P., Naik K.A., FitzGerald G.A., Kay S.A. and Hogenesch J.B. (2004) A functional genomics strategy reveals Rora as a component of the mammalian circadian clock. Neuron, 43, 527-537
7. Ueda H.R., Hayashi S., Chen W., Sano M., Machida M., Shigeyoshi Y., Iino M. and Hashimoto S. (2005) System-level identification of transcriptional circuits underlying mammalian circadian clocks. Nat. Genet., 37, 187-192
8. Duez H. and Staels B. (2010) Nuclear receptors linking circadian rhythms and cardiometabolic control. Arterioscler. Thromb. Vac. Biol., 30, 1529-1534
9. Takeda Y., Kang H.S., Angers M. and Jetten A.M. (2011) Retinoic acid-related orphan receptor gamma directly regulates neuronal PAS domain protein 2 transcription in vivo. Nucleic Acids Res., 39, 4769-4782
10. Takeda Y., Jothi R., Birault V. and Jetten A.M. (2012) RORgamma directly regulates the circadian expression of clock genes and downstream targets in vivo. Nucleic Acids Res., 40, 8519-8535
11. Akashi M. and Takumi T. (2005) The orphan nuclear receptor RORalpha regulates circadian transcription of the mammalian core-clock Bmal1. Nat. Struct. Mol. Biol., 12, 441-448
12. Crumbley C., Wang Y., Kojetin D.J. and Burris T.P. (2010) Characterization of the core mammalian clock component, NPAS2, as a REV-ERBalpha/RORalpha target gene. J. Biol. Chem., 285, 35386-35392
13. Guillaumond F., Dardente H., Giguere V. and Cermakian N. (2005) Differential control of Bmal1 circadian transcription by REV-ERB and ROR nuclear receptors. J. Biol. Rhythms, 20, 391-403
14. Muhlbauer E., Bazwinsky-Wutschke I., Wolgast S., Labucay K. and Peschke E. (2013) Differential and day-Time dependent expression of nuclear receptors RORalpha, RORbeta, RORgamma and RXRalpha in the rodent pancreas and islet. Mol. Cell. Endocrinol., 365, 129-138
15. Kang H.S., Angers M., Beak J.Y., Wu X., Gimble J.M., Wada T., Xie W., Collins J.B., Grissom S.F. and Jetten A.M. (2007) Gene expression profiling reveals a regulatory role for ROR alpha and ROR gamma in phase I and phase II metabolism. Physiol. Genomics, 31, 281-294
16. Wada T., Kang H.S., Angers M., Gong H., Bhatia S., Khadem S., Ren S., Ellis E., Strom S.C., Jetten A.M. et al. (2008) Identification of oxysterol 7alpha-hydroxylase (Cyp7b1) as a novel retinoid-related orphan receptor alpha (RORalpha) (NR1F1) target gene and a functional cross-Talk between RORalpha and liver X receptor (NR1H3). Mol. Pharmacol., 73, 891-899
17. Kang H.S., Okamoto K., Takeda Y., Beak J.Y., Gerrish K., Bortner C.D., DeGraff L.M., Wada T., Xie W. and Jetten A.M. (2011) Transcriptional profiling reveals a role for RORalpha in regulating gene expression in obesity-Associated inflammation and hepatic steatosis. Physiol. Genomics, 43, 818-828
18. Lau P., Fitzsimmons R.L., Raichur S., Wang S.C., Lechtken A. and Muscat G.E. (2008) The orphan nuclear receptor, RORalpha, regulates gene expression that controls lipid metabolism: Staggerer (SG/SG) mice are resistant to diet-induced obesity. J. Biol. Chem., 283, 18411-18421
19. Fitzsimmons R.L., Lau P. and Muscat G.E. (2012) Retinoidrelated orphan receptor alpha and the regulation of lipid homeostasis. J. Steroid Biochem. Mol. Biol., 130, 159-168
20. Jetten A.M., Kang H.S. and Takeda Y. (2013) Retinoic acidrelated orphan receptors alpha and gamma: Key regulators of lipid/glucose metabolism, inflammation, and insulin sensitivity. Front. Endocrinol., 4, 1-8
21. Meissburger B., Ukropec J., Roeder E., Beaton N., Geiger M., Teupser D., Civan B., Langhans W., Nawroth P.P., Gasperikova D. et al. (2011) Adipogenesis and insulin sensitivity in obesity are regulated by retinoid-related orphan receptor gamma. EMBO Mol. Med., 3, 637-651
22. Tinahones F.J., Moreno-Santos I., Vendrell J., Chacon M.R., Garrido-Sanchez L., Garcia-Fuentes E. and Macias-Gonzalez M. (2012) The retinoic acid receptor-related orphan nuclear receptor gamma1 (RORgamma1): A novel player determinant of insulin sensitivity in morbid obesity. Obesity, 20, 488-497
23. Le-Niculescu H., Patel S.D., Bhat M., Kuczenski R., Faraone S.V., Tsuang M.T., McMahon F.J., Schork N.J., Nurnberger J.I. Jr and Niculescu A.B. (2009) Convergent functional genomics of genomewide association data for bipolar disorder: Comprehensive identification of candidate genes, pathways and mechanisms. Am. J. Med. Genet. B Neuropsychiatr. Genet., 150B, 155-181
24. Medrano L.M., Garcia-Magarinos M., Dema B., Espino L., Maluenda C., Polanco I., Figueredo M.A., Fernandez-Arquero M. and Nunez C. (2012) Th17-related genes and celiac disease susceptibility. PLoS One, 7, e31244
25. Ramasamy A., Kuokkanen M., Vedantam S., Gajdos Z.K., Couto Alves A., Lyon H.N., Ferreira M.A., Strachan D.P., Zhao J.H., Abramson M.J. et al. (2012) Genome-wide association studies of asthma in population-based cohorts confirm known and suggested loci and identify an additional association near HLA. PLoS One, 7, e44008
26. Gamboa-Melendez M.A., Huerta-Chagoya A., Moreno-Macias H., Vazquez-Cardenas P., Ordonez-Sanchez M.L., Rodriguez-Guillen R., Riba L., Rodriguez-Torres M., Guerra-Garcia M.T., Guillen-Pineda L.E. et al. (2012) Contribution of common genetic variation to the risk of type 2 diabetes in the Mexican Mestizo population. Diabetes, 61, 3314-3321
27. Albers M., Kranz H., Kober I., Kaiser C., Klink M., Suckow J., Kern R. and Koegl M. (2005) Automated yeast two-hybrid screening for nuclear receptor-interacting proteins. Mol. Cell. Proteomics, 4, 205-213
28. Kurebayashi S., Nakajima T., Kim S.C., Chang C.Y., McDonnell D.P., Renaud J.P. and Jetten A.M. (2004) Selective LXXLL peptides antagonize transcriptional activation by the retinoid-related orphan receptor RORgamma. Biochem. Biophys. Res. Commun., 315, 919-927
29. Liu C., Li S., Liu T., Borjigin J. and Lin J.D. (2007) Transcriptional coactivator PGC-1alpha integrates the mammalian clock and energy metabolism. Nature, 447, 477-481
30. Elsir T., Smits A., Lindstrom M.S. and Nister M. (2012) Transcription factor PROX1: Its role in development and cancer. Cancer Metastasis Rev., 31, 795-805
31. Nishijima I. and Ohtoshi A. (2006) Characterization of a novel prospero-related homeobox gene, Prox2. Mol. Genet. Genomics, 275, 471-478
32. Bi X., Kajava A.V., Jones T., Demidenko Z.N. and Mortin M.A. (2003) The carboxy terminus of Prospero regulates its subcellular localization. Mol. Cell. Biol., 23, 1014-1024
33. Demidenko Z., Badenhorst P., Jones T., Bi X. and Mortin M.A. (2001) Regulated nuclear export of the homeodomain transcription factor Prospero. Development, 128, 1359-1367
34. Ryter J.M., Doe C.Q. and Matthews B.W. (2002) Structure of the DNA binding region of prospero reveals a novel homeo-prospero domain. Structure, 10, 1541-1549
35. Yousef M.S. and Matthews B.W. (2005) Structural basis of Prospero-DNA interaction: Implications for transcription regulation in developing cells. Structure, 13, 601-607
36. Song K.H., Li T. and Chiang J.Y. (2006) A Prospero-related homeodomain protein is a novel co-regulator of hepatocyte nuclear factor 4alpha that regulates the cholesterol 7alphahydroxylase gene. J. Biol. Chem., 281, 10081-10088
37. Steffensen K.R., Holter E., Bavner A., Nilsson M., Pelto-Huikko M., Tomarev S. and Treuter E. (2004) Functional conservation of interactions between a homeodomain cofactor and a mammalian FTZ-F1 homologue. EMBO Rep., 5, 613-619
38. Yoshimatsu Y., Yamazaki T., Mihira H., Itoh T., Suehiro J., Yuki K., Harada K., Morikawa M., Iwata C., Minami T. et al. (2011) Ets family members induce lymphangiogenesis through physical and functional interaction with Prox1. J. Cell Sci., 124, 2753-2762
39. Francois M., Harvey N.L. and Hogan B.M. (2011) The transcriptional control of lymphatic vascular development. Physiology, 26, 146-155
40. Karalay O., Doberauer K., Vadodaria K.C., Knobloch M., Berti L., Miquelajauregui A., Schwark M., Jagasia R., Taketo M.M., Tarabykin V. et al. (2011) Prospero-related homeobox 1 gene (Prox1) is regulated by canonical Wnt signaling and has a stage-specific role in adult hippocampal neurogenesis. Proc. Natl Acad. Sci. USA, 108, 5807-5812
41. Sosa-Pineda B., Wigle J.T. and Oliver G. (2000) Hepatocyte migration during liver development requires Prox1. Nat. Genet., 25, 254-255
42. Westmoreland J.J., Kilic G., Sartain C., Sirma S., Blain J., Rehg J., Harvey N. and Sosa-Pineda B. (2011) Pancreas-specific deletion of Prox1 affects development and disrupts homeostasis of the exocrine pancreas. Gastroenterology, 142, 999-1009
43. Wang J., Kilic G., Aydin M., Burke Z., Oliver G. and Sosa-Pineda B. (2005) Prox1 activity controls pancreas morphogenesis and participates in the production of ''secondary transition'' pancreatic endocrine cells. Dev. Biol., 286, 182-194
44. Petrova T.V., Nykanen A., Norrmen C., Ivanov K.I., Andersson L.C., Haglund C., Puolakkainen P., Wempe F., von Melchner H., Gradwohl G. et al. (2008) Transcription factor PROX1 induces colon cancer progression by promoting the transition from benign to highly dysplastic phenotype. Cancer Cell, 13, 407-419
45. Dupuis J., Langenberg C., Prokopenko I., Saxena R., Soranzo N., Jackson A.U., Wheeler E., Glazer N.L., Bouatia-Naji N., Gloyn A.L. et al. (2010) New genetic loci implicated in fasting glucose homeostasis and their impact on type 2 diabetes risk. Nat. Genet., 42, 105-116
46. Ohshige T., Iwata M., Omori S., Tanaka Y., Hirose H., Kaku K., Maegawa H., Watada H., Kashiwagi A., Kawamori R. et al. (2011) Association of new loci identified in European genomewide association studies with susceptibility to type 2 diabetes in the Japanese. PLoS One, 6, e26911
47. Lecompte S., Pasquetti G., Hermant X., Grenier-Boley B., Gonzalez-Gross M., De Henauw S., Molnar D., Stehle P., Beghin L., Moreno L.A. et al. (2013) Genetic and molecular insights into the role of PROX1 in glucose metabolism. Diabetes, 62, 1738-1745
48. Dussault I., Fawcett D., Matthyssen A., Bader J.A. and Giguere V. (1998) Orphan nuclear receptor ROR alpha-deficient mice display the cerebellar defects of staggerer. Mech. Dev., 70, 147-153
49. Kurebayashi S., Ueda E., Sakaue M., Patel D.D., Medvedev A., Zhang F. and Jetten A.M. (2000) Retinoid-related orphan receptor gamma (RORgamma) is essential for lymphoid organogenesis and controls apoptosis during thymopoiesis. Proc. Natl Acad. Sci. USA, 97, 10132-10137
50. Nakajima T., Fujino S., Nakanishi G., Kim Y.S. and Jetten A.M. (2004) TIP27: A novel repressor of the nuclear orphan receptor TAK1/TR4. Nucleic Acids Res, 32, 4194-4204
51. Kumar N., Solt L.A., Conkright J.J., Wang Y., Istrate M.A., Busby S.A., Garcia-Ordonez R.D., Burris T.P. and Griffin P.R. (2010) The benzenesulfoamide T0901317 [N-(2,2,2-Trifluoroethyl)-N-[4-[2,2,2-Trifluoro-1-hydroxy-1- (trifluoromethyl)ethyl] phenyl]-benzenesulfonamide] is a novel retinoic acid receptor-related orphan receptor-Alpha/gamma inverse agonist. Mol. Pharmacol., 77, 228-236
52. Xu T., Wang X., Zhong B., Nurieva R.I., Ding S. and Dong C. (2011) Ursolic acid suppresses interleukin-17 (IL-17) production by selectively antagonizing the function of RORgamma t protein. J. Biol. Chem., 286, 22707-22710
53. McInerney E.M., Rose D.W., Flynn S.E., Westin S., Mullen T.M., Krones A., Inostroza J., Torchia J., Nolte R.T., Assa-Munt N. et al. (1998) Determinants of coactivator LXXLL motif specificity in nuclear receptor transcriptional activation. Genes Dev., 12, 3357-3368
54. Heery D.M., Hoare S., Hussain S., Parker M.G. and Sheppard H. (2001) Core LXXLL motif sequences in CREB-binding protein, SRC1, and RIP140 define affinity and selectivity for steroid and retinoid receptors. J. Biol. Chem., 276, 6695-6702
55. Shin J.W., Min M., Larrieu-Lahargue F., Canron X., Kunstfeld R., Nguyen L., Henderson J.E., Bikfalvi A., Detmar M. and Hong Y.K. (2006) Prox1 promotes lineage-specific expression of fibroblast growth factor (FGF) receptor-3 in lymphatic endothelium: A role for FGF signaling in lymphangiogenesis. Mol. Biol. Cell, 17, 576-584
56. Charest-Marcotte A., Dufour C.R., Wilson B.J., Tremblay A.M., Eichner L.J., Arlow D.H., Mootha V.K. and Giguere V. (2010) The homeobox protein Prox1 is a negative modulator of ERR{alpha}/PGC-1{alpha} bioenergetic functions. Genes Dev., 24, 537-542
57. Zinovieva R.D., Duncan M.K., Johnson T.R., Torres R., Polymeropoulos M.H. and Tomarev S.I. (1996) Structure and chromosomal localization of the human homeobox gene Prox 1. Genomics, 35, 517-522
58. Giresi P.G., Kim J., McDaniell R.M., Iyer V.R. and Lieb J.D. (2007) FAIRE (Formaldehyde-Assisted Isolation of Regulatory Elements) isolates active regulatory elements from human chromatin. Genome Res., 17, 877-885
59. Dufour C.R., Levasseur M.P., Pham N.H., Eichner L.J., Wilson B.J., Charest-Marcotte A., Duguay D., Poirier-Heon J.F., Cermakian N. and Giguere V. (2011) Genomic convergence among ERRalpha, PROX1, and BMAL1 in the control of metabolic clock outputs. PLoS Genet., 7, e1002143
60. Heery D.M., Kalkhoven E., Hoare S. and Parker M.G. (1997) A signature motif in transcriptional co-Activators mediates binding to nuclear receptors. Nature, 387, 733-736
61. Azuma K., Urano T., Watabe T., Ouchi Y. and Inoue S. (2011) PROX1 suppresses vitamin K-induced transcriptional activity of Steroid and Xenobiotic Receptor. Genes Cell, 16, 1063-1070
62. Baxter S.A., Cheung D.Y., Bocangel P., Kim H.K., Herbert K., Douville J.M., Jangamreddy J.R., Zhang S., Eisenstat D.D. and Wigle J.T. (2011) Regulation of the lymphatic endothelial cell cycle by the PROX1 homeodomain protein. Biochim. Biophys. Acta, 1813, 201-212
63. Pan M.R., Chang T.M., Chang H.C., Su J.L., Wang H.W. and Hung W.C. (2009) Sumoylation of Prox1 controls its ability to induce VEGFR3 expression and lymphatic phenotypes in endothelial cells. J. Cell Sci., 122, 3358-3364
64. Risebro C.A., Petchey L.K., Smart N., Gomes J., Clark J., Viera J.M., Yanni J., Dobrzynski H., Davidson S., Zuberi Z. et al. (2012) Epistatic rescue of Nkx2.5 adult cardiac conduction disease phenotypes by Prospero-related homeobox protein 1 and HDAC3. Circ. Res., 111, e19-e31
65. Solt L.A., Kojetin D.J. and Burris T.P. (2011) The REV-ERBs and RORs: Molecular links between circadian rhythms and lipid homeostasis. Future Med. Chem., 3, 623-638
66. Asher G. and Schibler U. (2011) Crosstalk between components of circadian and metabolic cycles in mammals. Cell Metab., 13, 125-137
67. Bass J. and Takahashi J.S. (2010) Circadian integration of metabolism and energetics. Science, 330, 1349-1354