Folia Biologica
Journal of Cellular and Molecular Biology, Charles University 

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Fol. Biol. 2007, 53, 85-96

https://doi.org/10.14712/fb2007053030085

Supplementary Nuclear Receptor NHR-60 is Required for Normal Embryonic and Early Larval Development of Caenorhabditis elegans

K. Šimečková1, E. Brožová1, J. Vohánka1, M. Pohludka2, Z. Kostrouch2,3, M. W. Krause4, J. E. Rall3, Marta Kostrouchová1,3

1Laboratory of Molecular Biology and Genetics, Institute of Inherited Metabolic Disorders, 1st Faculty of Medicine, Charles University, Prague, Czech Republic
2Laboratory of Molecular Pathology, Institute of Inherited Metabolic Disorders, 1st Faculty of Medicine, Charles University, Prague, Czech Republic
3Clinical Endocrinology Branch, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, MD., United States of America
4Laboratory of Molecular Biology, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, MD., United States of America

Received April 4, 2007
Accepted May 3, 2007

References

1. Aggelidou, E., Iordanidou, P., Tsantili, P., Papadopoulos, G., Hadzopoulou-Cladaras, M. (2004) Critical role of residues defining the ligand binding pocket in hepatocyte nuclear factor-4α. J. Biol. Chem. 279, 30680-30688. <https://doi.org/10.1074/jbc.M401120200>
2. Antebi, A. (2006) Nuclear hormone receptors in C. elegans (January 03, 2006), ed. The C. elegans Research Community, WormBook, doi/10.1895/wormbook.1.64.1 http://www.wormbook.org.
3. Barettino, D., Vivanco Ruiz, M. M., Stunnenberg, H. G. (1994) Characterization of the ligand-dependent transactivation domain of thyroid hormone receptor. EMBO J. 13, 3039-3049. <https://doi.org/10.1002/j.1460-2075.1994.tb06603.x>
4. Blumenthal, T., Spieth, J. (1996) Gene structure and organization in Caenorhabditis elegans. Curr. Opin. Genet. Dev. 6, 692-698. <https://doi.org/10.1016/S0959-437X(96)80022-0>
5. Bogan, A. A., Dallas-Yang, Q., Ruse, M. D., Jr., Maeda, Y., Jiang, G., Nepomuceno, L., Scanlan, T. S., Cohen, F. E., Sladek, F. M. (2000) Analysis of protein dimerization and ligand binding of orphan receptor HNF4α. J. Mol. Biol. 302, 831-851. <https://doi.org/10.1006/jmbi.2000.4099>
6. Brenner, S. (1974) The genetics of Caenorhabditis elegans. Genetics 77, 71-94. <https://doi.org/10.1093/genetics/77.1.71>
7. Brozova, E., Simeckova, K., Kostrouch, Z., Rall, J. E., Kostrouchova, M. (2006) NHR-40, a Caenorhabditis elegans supplementary nuclear receptor, regulates embryonic and early larval development. Mech. Dev. 123, 689-701. <https://doi.org/10.1016/j.mod.2006.06.006>
8. Chawla, A., Repa, J. J., Evans, R. M., Mangelsdorf, D. J. (2001) Nuclear receptors and lipid physiology: opening the X-files. Science 294, 1866-1870. <https://doi.org/10.1126/science.294.5548.1866>
9. Chen, W. S., Manova, K., Weinstein, D. C., Duncan, S. A., Plump, A. S., Prezioso, V. R., Bachvarova, R. F., Darnell, J. E., Jr. (1994) Disruption of the HNF-4 gene, expressed in visceral endoderm, leads to cell death in embryonic ectoderm and impaired gastrulation of mouse embryos. Genes Dev. 8, 2466-2477. <https://doi.org/10.1101/gad.8.20.2466>
10. Dhe-Paganon, S., Duda, K., Iwamoto, M., Chi, Y. I., Shoelson, S. E. (2002) Crystal structure of the HNF4 α ligand binding domain in complex with endogenous fatty acid ligand. J. Biol. Chem. 277, 37973-37976. <https://doi.org/10.1074/jbc.C200420200>
11. Duncan, S. A., Nagy, A., Chan, W. (1997) Murine gastrulation requires HNF-4 regulated gene expression in the visceral endoderm: tetraploid rescue of Hnf-4(-/-) embryos. Development 124, 279-287. <https://doi.org/10.1242/dev.124.2.279>
12. Enmark, E., Gustafsson, J. A. (2001) Comparing nuclear receptors in worms, flies and humans. Trends Pharmacol. Sci. 22, 611-615. <https://doi.org/10.1016/S0165-6147(00)01859-9>
13. Fire, A., Albertson, D., Harrison, S. W., Moerman, D. G. (1991) Production of antisense RNA leads to effective and specific inhibition of gene expression in C. elegans muscle. Development 113, 503-514. <https://doi.org/10.1242/dev.113.2.503>
14. Gissendanner, C. R., Crossgrove, K., Kraus, K. A., Maina, C. V., Sluder, A. E. (2004) Expression and function of conserved nuclear receptor genes in Caenorhabditis elegans. Dev. Biol. 266, 399-416. <https://doi.org/10.1016/j.ydbio.2003.10.014>
15. Gruenbaum, Y., Goldman, R. D., Meyuhas, R., Mills, E., Margalit, A., Fridkin, A., Dayani, Y., Prokocimer, M., Enosh, A. (2003) The nuclear lamina and its functions in the nucleus. Int. Rev. Cytol. 226, 1-62. <https://doi.org/10.1016/S0074-7696(03)01001-5>
16. Hager, G. L., Lim, C. S., Elbi, C., Baumann, C. T. (2000) Trafficking of nuclear receptors in living cells. J. Steroid. Biochem. Mol. Biol. 74, 249-254. <https://doi.org/10.1016/S0960-0760(00)00100-X>
17. Hayhurst, G. P., Lee, Y. H., Lambert, G., Ward, J. M., Gonzalez, F. J. (2001) Hepatocyte nuclear factor 4α (nuclear receptor 2A1) is essential for maintenance of hepatic gene expression and lipid homeostasis. Mol. Cell. Biol. 21, 1393-1403. <https://doi.org/10.1128/MCB.21.4.1393-1403.2001>
18. Hertz, R., Magenheim, J., Berman, I., Bar-Tana, J. (1998) Fatty acyl-CoA thioesters are ligands of hepatic nuclear factor-4α. Nature 392, 512-516. <https://doi.org/10.1038/33185>
19. Iordanidou, P., Aggelidou, E., Demetriades, C., Hadzopoulou-Cladaras, M. (2005) Distinct amino acid residues may be involved in coactivator and ligand interactions in hepatocyte nuclear factor-4α. J. Biol. Chem. 280, 21810-21819. <https://doi.org/10.1074/jbc.M501221200>
20. Johnson, B. S., Chandraratna, R. A., Heyman, R. A., Allegretto, E. A., Mueller, L., Collins, S. J. (1999) Retinoid X receptor (RXR) agonist-induced activation of dominant-negative RXR-retinoic acid receptor α403 heterodimers is developmentally regulated during myeloid differentiation. Mol. Cell. Biol. 19, 3372-3382. <https://doi.org/10.1128/MCB.19.5.3372>
21. Johnstone, I. L., Barry, J. D. (1996) Temporal reiteration of a precise gene expression pattern during nematode development. EMBO J. 15, 3633-3639. <https://doi.org/10.1002/j.1460-2075.1996.tb00732.x>
22. King-Jones, K., Thummel, C. S. (2005) Nuclear receptors - a perspective from Drosophila. Nat. Rev. Genet. 6, 311-323. <https://doi.org/10.1038/nrg1581>
23. Kostrouchova, M., Krause, M., Kostrouch, Z., Rall, J. (1998) CHR3: a Caenorhabditis elegans orphan nuclear hormone receptor required for proper epidermal development and molting. Development 125, 1617-1626. <https://doi.org/10.1242/dev.125.9.1617>
24. Kostrouchova, M., Krause, M., Kostrouch, Z., Rall, J. E. (2001) Nuclear hormone receptor CHR3 is a critical regulator of all four larval molts of the nematode Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 98, 7360-7365. <https://doi.org/10.1073/pnas.131171898>
25. Krause, M., Harrison, S. W., Xu, S. Q., Chen, L., Fire, A. (1994) Elements regulating cell- and stage-specific expression of the C. elegans MyoD family homolog hlh-1. Dev. Biol. 166, 133-148. <https://doi.org/10.1006/dbio.1994.1302>
26. Krause, M., Hirsh, D. (1987) A trans-spliced leader sequence on actin mRNA in C. elegans. Cell 49, 753-761. <https://doi.org/10.1016/0092-8674(87)90613-1>
27. Ktistaki, E., Ktistakis, N. T., Papadogeorgaki, E., Talianidis, I. (1995) Recruitment of hepatocyte nuclear factor 4 into specific intranuclear compartments depends on tyrosine phosphorylation that affects its DNA-binding and transactivation potential. Proc. Natl. Acad. Sci. USA 92, 9876-9880. <https://doi.org/10.1073/pnas.92.21.9876>
28. Li, J., Ning, G., Duncan, S. A. (2000) Mammalian hepatocyte differentiation requires the transcription factor HNF-4α. Genes Dev. 14, 464-474. <https://doi.org/10.1101/gad.14.4.464>
29. Libý, P., Kostrouchová, M., Pohludka, M., Yilma, P., Hrabal, P., Sikora, J., Brožová, E., Kostrouchová, M., Rall, J. E., Kostrouch, Z. (2006) Elevated and deregulated expression of HDAC3 in human astrocytic glial tumors. Folia Biol. (Praha) 52, 21-33.
30. Liu, J., Ben-Shahar, T. R., Riemer, D., Treinin, M., Spann, P., Weber, K., Fire, A., Gruenbaum, Y. (2000) Essential roles for Caenorhabditis elegans lamin gene in nuclear organization, cell cycle progression, and spatial organization of nuclear pore complexes. Mol. Biol. Cell. 11, 3937-3947. <https://doi.org/10.1091/mbc.11.11.3937>
31. Liu, Y. Y., Tachiki, K. H., Brent, G. A. (2002) A targeted thyroid hormone receptor α gene dominant-negative mutation (P398H) selectively impairs gene expression in differentiated embryonic stem cells. Endocrinology 143, 2664-2672. <https://doi.org/10.1210/endo.143.7.8906>
32. Maglich, J. M., Sluder, A., Guan, X., Shi, Y., McKee, D. D., Carrick, K., Kamdar, K., Willson, T. M., Moore, J. T. (2001) Comparison of complete nuclear receptor sets from the human, Caenorhabditis elegans and Drosophila genomes. RESEARCH0029. Epub 2001 Jul 0024.
33. Mangelsdorf, D. J., Evans, R. M. (1995) The RXR heterodimers and orphan receptors. Cell 83, 841-850. <https://doi.org/10.1016/0092-8674(95)90200-7>
34. Mangelsdorf, D. J., Thummel, C., Beato, M., Herrlich, P., Schultz, G., Umesono, K., Blumberg, B., Kastner, P., Mark, M., Chambon, P. (1995) The nuclear receptor superfamily: the second decade. Cell 83, 835-839. <https://doi.org/10.1016/0092-8674(95)90199-X>
35. Maruvada, P., Baumann, C. T., Hager, G. L., Yen, P. M. (2003) Dynamic shuttling and intranuclear mobility of nuclear hormone receptors. J. Biol. Chem. 278, 12425-12432. <https://doi.org/10.1074/jbc.M202752200>
36. Mello, C., Fire, A. (1995) DNA transformation. In: Caenorhabditis elegans: Modern Biological Analysis of an Organism, eds. Epstein, H. F., Shakes, D. C., pp. 451-482 Academic Press, New York.
37. Miyabayashi, T., Palfreyman, M. T., Sluder, A. E., Slack, F., Sengupta, P. (1999) Expression and function of members of a divergent nuclear receptor family in Caenorhabditis elegans. Dev. Biol. 215, 314-331. <https://doi.org/10.1006/dbio.1999.9470>
38. Mohler, W. A., Simske, J. S., Williams-Masson, E. M., Hardin, J. D., White, J. G. (1998) Dynamics and ultrastructure of developmental cell fusions in the Caenorhabditis elegans hypodermis. Curr. Biol. 8, 1087-1090. <https://doi.org/10.1016/S0960-9822(98)70447-6>
39. Park, Y., Freedman, B. D., Lee, E. J., Park, S., Jameson, J. L. (2003) A dominant negative PPARγ mutant shows altered cofactor recruitment and inhibits adipogenesis in 3T3-L1 cells. Diabetologia 46, 365-377. <https://doi.org/10.1007/s00125-003-1037-4>
40. Pemrick, S. M., Lucas, D. A., Grippo, J. F. (1994) The retinoid receptors. Leukemia 8, S1-10.
41. Petrescu, A. D., Hertz, R., Bar-Tana, J., Schroeder, F., Kier, A. B. (2005) Role of regulatory F-domain in hepatocyte nuclear factor-4α ligand specificity. J. Biol. Chem. 280, 16714-16727. <https://doi.org/10.1074/jbc.M405906200>
42. Robinson-Rechavi, M., Escriva Garcia, H., Laudet, V. (2003) The nuclear receptor superfamily. J. Cell. Sci. 116, 585-586. <https://doi.org/10.1242/jcs.00247>
43. Robinson-Rechavi, M., Maina, C. V., Gissendanner, C. R., Laudet, V., Sluder, A. (2005) Explosive lineage-specific expansion of the orphan nuclear receptor HNF4 in nematodes. J. Mol. Evol. 60, 577-586. <https://doi.org/10.1007/s00239-004-0175-8>
44. Ruau, D., Duarte, J., Ourjdal, T., Perriere, G., Laudet, V., Robinson-Rechavi, M., Escriva Garcia, H. (2004) Update of NUREBASE: nuclear hormone receptor functional genomics. The nuclear receptor superfamily. Nucleic Acids Res. 32, D165-167. <https://doi.org/10.1093/nar/gkh062>
45. Ruse, M. D., Jr., Privalsky, M. L., Sladek, F. M. (2002) Competitive cofactor recruitment by orphan receptor hepatocyte nuclear factor 4α1: modulation by the F domain. Mol. Cell. Biol. 22, 1626-1638. <https://doi.org/10.1128/MCB.22.6.1626-1638.2002>
46. Sengupta, P., Colbert, H. A., Bargmann, C. I. (1994) The C. elegans gene odr-7 encodes an olfactory-specific member of the nuclear receptor superfamily. Cell 79, 971-980. <https://doi.org/10.1016/0092-8674(94)90028-0>
47. Silhankova, M., Jindra, M., Asahina, M. (2005) Nuclear receptor NHR-25 is required for cell-shape dynamics during epidermal differentiation in Caenorhabditis elegans. J. Cell Sci. 118, 223-232. <https://doi.org/10.1242/jcs.01609>
48. Sluder, A. E., Maina, C. V. (2001) Nuclear receptors in nematodes: themes and variations. Trends Genet. 17, 206-213. <https://doi.org/10.1016/S0168-9525(01)02242-9>
49. Stegmann, A., Hansen, M., Wang, Y., Larsen, J. B., Lund, L. R., Ritie, L., Nicholson, J. K., Quistorff, B., Simon-Assmann, P., Troelsen, J. T., Olsen, J. (2006) Metabolome, transcriptome, and bioinformatic cis-element analyses point to HNF-4 as a central regulator of gene expression during enterocyte differentiation. Physiol. Genomics 27, 141-155. <https://doi.org/10.1152/physiolgenomics.00314.2005>
50. Sulston, J. E., Horvitz, H. R. (1977) Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev. Biol. 56, 110-156. <https://doi.org/10.1016/0012-1606(77)90158-0>
51. Sun, Y., Polishchuk, E. A., Radoja, U., Cullen, W. R. (2004) Identification and quantification of arsC genes in environmental samples by using real-time PCR. J. Microbiol. Methods 58, 335-349. <https://doi.org/10.1016/j.mimet.2004.04.015>
52. Timmons, L., Fire, A. (1998) Specific interference by ingested dsRNA [letter]. Nature 395, 854. <https://doi.org/10.1038/27579>
53. Van Gilst, M. R., Gissendanner, C. R., Sluder, A. E. (2002) Diversity and function of orphan nuclear receptors in nematodes. Crit. Rev. Eukaryot. Gene Expr. 12, 65-88.
54. Van Gilst, M. R., Hadjivassiliou, H., Yamamoto, K. R. (2005a) A Caenorhabditis elegans nutrient response system partially dependent on nuclear receptor NHR-49. Proc. Natl. Acad. Sci. USA 102, 13496-13501. <https://doi.org/10.1073/pnas.0506234102>
55. Van Gilst, M. R., Hadjivassiliou, H., Jolly, A., Yamamoto, K. R. (2005b) Nuclear hormone receptor NHR-49 controls fat consumption and fatty acid composition in C. elegans. PLoS Biol. 3, e53. <https://doi.org/10.1371/journal.pbio.0030053>
56. Watt, A. J., Garrison, W. D., Duncan, S. A. (2003) HNF4: a central regulator of hepatocyte differentiation and function. Hepatology 37, 1249-1253. <https://doi.org/10.1053/jhep.2003.50273>
57. Zhu, X. G., Hanover, J. A., Hager, G. L., Cheng, S. Y. (1998) Hormone-induced translocation of thyroid hormone receptors in living cells visualized using a receptor green fluorescent protein chimera. J. Biol. Chem. 273, 27058-27063. <https://doi.org/10.1074/jbc.273.42.27058>
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