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JOURNAL ARTICLES
CHR3: a Caenorhabditis elegans orphan nuclear hormone receptor required for proper epidermal development and molting
M. Kostrouchova, M. Krause, Z. Kostrouch, J.E. Rall
Development 1998 125: 1617-1626;

Summary

CHR3 is a Caenorhabditis elegans orphan nuclear hormone receptor highly homologous to Drosophila DHR3, an ecdysone-inducible gene product involved in metamorphosis. Related vertebrate factors include RORalpha/RZRalpha, RZRbeta and RevErb. Gel-shift studies show that CHR3 can bind the DR5-type hormone response sequence. CHR3 is a nuclear protein present in all blastomeres during early embryogenesis. During morphogenesis, both CHR3 protein and zygotically active reporter genes are detectable in epidermal cells and their precursors. Inhibition of the gene encoding CHR3 results in several larval defects associated with abnormal epidermal cell function, including molting and body size regulation, suggesting that CHR3 is an essential epidermal factor required for proper postembryonic development.

REFERENCES

    1. Ambros V.,
    2. Horvitz H. R.
    (1984) Heterochronic mutants of the nematode Caenorhabditis elegans. Science 226, 409–416
    OpenUrlAbstract/FREE Full Text
    1. Azzaria M.,
    2. Goszczynski B.,
    3. Chung M.A.,
    4. Kalb J.M.,
    5. McGhee J.D.
    (1996) A fork head /HNF-3 homolog expressed in the pharynx and intestine of the Caenorhabditis elegans embryo. Dev. Biol 178, 289–303
    OpenUrlCrossRefPubMedWeb of Science
    1. Becker-Andre M.,
    2. Andre E.,
    3. DeLamarter J. F.
    (1993) Identification of nuclear receptor mRNAs by RT-PCR amplification of conserved zinc-finger motif sequences. Biochem. Biophys. Res. Commun 194, 1371–1379
    OpenUrlCrossRefPubMedWeb of Science
    1. Carlberg C.,
    2. Hooft,
    3. van Huijsduijnen R.,
    4. Staple J. K.,
    5. DeLamarter J. F.,
    6. Becker A. M.
    (1994) RZRs, a new family of retinoid-related orphan receptors that function as both monomers and homodimers. Mol. Endocrinol 8, 757–770
    OpenUrlCrossRefPubMedWeb of Science
    1. Carney G. E.,
    2. Wade A. A.,
    3. Sapra R.,
    4. Goldstein E. S.,
    5. Bender M.
    (1997) DHR3, an ecdysone-inducible early-late gene encoding a Drosophila nuclear receptor, is required for embryogenesis. Proc. Natl. Acad. Sci. USA 94, 12024–12029
    OpenUrlAbstract/FREE Full Text
    1. Chawla A.,
    2. Lazar M. A.
    (1993) Induction of Rev-ErbA alpha, an orphan receptor encoded on the opposite strand of the alpha-thyroid hormone receptor gene, during adipocyte differentiation. J. Biol. Chem 268, 16265–16269
    OpenUrlAbstract/FREE Full Text
    1. Cox G. N.,
    2. Kramer J. M.,
    3. Hirsh D.
    (1984) Number and organization of collagen genes in Caenorhabditis elegans. Mol. Cell. Biol 4, 2389–2395
    OpenUrlAbstract/FREE Full Text
    1. Cox G. N.,
    2. Fields C.,
    3. Kramer J. M.,
    4. Rosenzweig B.,
    5. Hirsh D.
    (1989) Sequence comparison of developmentally regulated collagen genes of Caenorhabditis elegans. Gene 76, 331–344
    OpenUrlCrossRefPubMed
    1. Downes M.,
    2. Carozzi A. J.,
    3. Muscat G. E.
    (1995) Constitutive expression of the orphan receptor, Rev-erbA alpha, inhibits muscle differentiation and abrogates the expression of the MyoD gene family. Mol. Endocrinol 9, 1666–1678
    OpenUrlCrossRefPubMedWeb of Science
    1. Enmark E.,
    2. Gustafsson J. A.
    (1996) Orphan nuclear receptors--the first eight years. Mol. Endocrinol 10, 1293–1307
    OpenUrlCrossRefPubMedWeb of Science
    1. Finney M.,
    2. Ruvkun G.
    (1990) The unc - 86 gene product couples cell lineage and cell identity in C. elegans. Cell 63, 895–905
    OpenUrlCrossRefPubMedWeb of Science
    1. Fire A.,
    2. Harrison S. W.,
    3. Dixon D.
    (1990) A modular set of lacZ fusion vectors for studying gene expression in Caenorhabditis elegans. Gene 93, 189–198
    OpenUrlCrossRefPubMedWeb of Science
    1. Fire A.,
    2. Xu S.,
    3. Montgomery M.K.,
    4. Driver S.A.,
    5. Mello C.C.
    (1998) Potent and specific genetic interference by double stranded RNA in C. elegans. Nature 391, 806–811
    OpenUrlCrossRefPubMedWeb of Science
    1. Forman B. M.,
    2. Chen J.,
    3. Blumberg B.,
    4. Kliewer S. A.,
    5. Henshaw R.,
    6. Ong E. S.,
    7. Evans R. M.
    (1994) Cross-talk among ROR alpha 1 and the Rev-erb family of orphan nuclear receptors. Mol. Endocrinol 8, 1253–1261
    OpenUrlCrossRefPubMedWeb of Science
    1. Francis G. R.,
    2. Waterston R. H.
    (1985) Muscle organization in Caenorhabditis elegans: localization of proteins implicated in thin filament attachment and I-band organization. J. Cell Biol 101, 1532–1549
    OpenUrlAbstract/FREE Full Text
    1. Freedman L. P.
    (1992) Anatomy of the steroid receptor zinc finger region. Endocr. Rev 13, 129–145
    OpenUrlCrossRefPubMedWeb of Science
    1. Giguere V.,
    2. Tini M.,
    3. Flock G.,
    4. Ong E.,
    5. Evans R. M.,
    6. Otulakowski G.
    (1994) Isoform-specific amino-terminal domains dictate DNA-binding properties of ROR alpha, a novel family of orphan hormone nuclear receptors. Genes Dev 8, 538–553
    OpenUrlAbstract/FREE Full Text
    1. Giguere V.,
    2. McBroom L. D.,
    3. Flock G.
    (1995) Determinants of target gene specificity for ROR alpha 1: monomeric DNA binding by an orphan nuclear receptor. Mol. Cell. Biol 15, 2517–2526
    OpenUrlAbstract/FREE Full Text
    1. Gilleard J. S.,
    2. Barry J. D.,
    3. Johnstone I. L.
    (1997) cis-Regulatory requirements for hypodermal cell-specific expression of the Caenorhabditis elegans cuticle collagen gene dpy - 7. Mol. Cell. Biol 17, 2301–2311
    OpenUrlAbstract/FREE Full Text
    1. Greiner E. F.,
    2. Kirfel J.,
    3. Greschik H.,
    4. Dörflinger U.,
    5. Becker P.,
    6. Mercep A.,
    7. Schule R.
    (1996) Functional analysis of retinoid Z receptor, a brain-specific nuclear orphan receptor. Proc. Natl Acad. Sci. USA 93, 10105–10110
    OpenUrlAbstract/FREE Full Text
    1. Guo S.,
    2. Kemphues K. J.
    (1995) par-1, a gene required for establishing polarity in C. elegans embryos, encodes a putative Ser/Thr kinase that is asymmetrically distributed. Cell 81, 611–620
    OpenUrlCrossRefPubMedWeb of Science
    1. Guo S.,
    2. Kemphues K. J.
    (1996) A non-muscle myosin required for embryonic polarity in Caenorhabditis elegans. Nature 382, 455–458
    OpenUrlCrossRefPubMed
    1. Hamilton B. A.,
    2. Frankel W. N.,
    3. Kerrebrock A. W.,
    4. Hawkins T. L.,
    5. FitzHugh W.,
    6. Kusumi K.,
    7. Russell L. B.,
    8. Mueller K. L.,
    9. van B. V.,
    10. Birren B. W.,
    11. Kruglyak L.,
    12. Lander E. S.
    (1996) Disruption of the nuclear hormone receptor RORalpha in staggerer mice. Nature 379, 736–739
    OpenUrlCrossRefPubMedWeb of Science
    1. Harfe B. D.,
    2. Fire A.
    (1998) Muscle and nerve-specific regulation of a novel NK-2 class homeodomain factor in C. elegans. Development 125, 421–429
    OpenUrlAbstract
    1. Herskowitz I.
    (1987) Functional inactivation of genes by dominant negative mutations. Nature 329, 219–222
    OpenUrlCrossRefPubMed
    1. Horner M. A.,
    2. Chen T.,
    3. Thummel C. S.
    (1995) Ecdysteroid regulation and DNA binding properties of Drosophila nuclear hormone receptor superfamily members. Dev. Biol 168, 490–502
    OpenUrlCrossRefPubMedWeb of Science
    1. Johnstone I. L.
    (1994) The cuticle of the nematode Caenorhabditis elegans: a complex collagen structure. BioEssays 16, 171–178
    OpenUrlCrossRefPubMedWeb of Science
    1. Kato S.,
    2. Sasaki H.,
    3. Suzawa M.,
    4. Masushige S.,
    5. Tora L.,
    6. Chambon P.,
    7. Gronemeyer H.
    (1995) Widely spaced, directly repeated PuGGTCA elements act as promiscuous enhancers for different classes of nuclear receptors. Mol. Cell. Biol 15, 5858–5867
    OpenUrlAbstract/FREE Full Text
    1. Koelle M. R.,
    2. Talbot W. S.,
    3. Segraves W. A.,
    4. Bender M. T.,
    5. Cherbas P.,
    6. Hogness D. S.
    (1991) The Drosophila EcR gene encodes an ecdysone receptor, a new member of the steroid receptor superfamily. Cell 67, 59–77
    OpenUrlCrossRefPubMedWeb of Science
    1. Koelle M. R.,
    2. Segraves W. A.,
    3. Hogness D. S.
    (1992) DHR3: a Drosophila steroid receptor homolog. Proc. Natl. Acad. Sci. USA 89, 6167–6171
    OpenUrlAbstract/FREE Full Text
    1. Kostrouch Z.,
    2. Kostrouchova M.,
    3. Rall J. E.
    (1995) Steroid/thyroid hormone receptor genes in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 92, 156–159
    OpenUrlAbstract/FREE Full Text
    1. Kramer J. M.
    (1994) Structures and functions of collagens in Caenorhabditis elegans. FASEB J 8, 329–336
    OpenUrlAbstract
    1. Krause M.,
    2. Harrison S. W.,
    3. Xu S. Q.,
    4. Chen L.,
    5. Fire A.
    (1994) Elements regulating cell-and stage-specific expression of the C. elegans MyoD family homolog hlh-1. Dev. Biol 166, 133–148
    OpenUrlCrossRefPubMedWeb of Science
    1. Krause M.,
    2. Hirsh D.
    (1987) A trans-spliced leader sequence on actin mRNA in C. elegans. Cell 49, 753–761
    OpenUrlCrossRefPubMedWeb of Science
    1. Krause M.,
    2. Park M.,
    3. Zhang J. M.,
    4. Yuan J.,
    5. Harfe B.,
    6. Xu S. Q.,
    7. Greenwald I.,
    8. Cole M.,
    9. Paterson B.,
    10. Fire A.
    (1997) A C. elegans E/Daughterless bHLH protein marks neuronal but not striated muscle development. Development 124, 2179–2189
    OpenUrlAbstract
    1. Lam G. T.,
    2. Jiang C.,
    3. Thummel C. S.
    (1997) Coordination of larval and prepupal gene expression by the DHR3 orphan receptor during Drosophila metamorphosis. Development 124, 1757–1769
    OpenUrlAbstract
    1. Laudet V.,
    2. Adelmant G.
    (1995) Nuclear receptors. Lonesome orphans. Curr. Biol 5, 124–127
    OpenUrlCrossRefPubMed
    1. Laudet V.,
    2. Hanni C.,
    3. Coll J.,
    4. Catzeflis F.,
    5. Stehelin D.
    (1992) Evolution of the nuclear receptor gene superfamily. EMBO J 11, 1003–1013
    OpenUrlPubMedWeb of Science
    1. Levy A. D.,
    2. Yang J.,
    3. Kramer J. M.
    (1993) Molecular and genetic analyses of the Caenorhabditis elegans dpy - 2 and dpy - 10 collagen genes: a variety of molecular alterations affect organismal morphology. Mol. Biol. Cell 4, 803–817
    OpenUrlAbstract/FREE Full Text
    1. Lin R.,
    2. Thompson S.,
    3. Priess J. R.
    (1995) pop - 1 encodes an HMG box protein required for the specification of a mesoderm precursor in early C. elegans embryos. Cell 83, 599–609
    OpenUrlCrossRefPubMedWeb of Science
    1. Liu Z.,
    2. Kirch S.,
    3. Ambros V.
    (1995) The Caenorhabditis elegans heterochronic gene pathway controls stage-specific transcription of collagen genes. Development 121, 2471–2478
    OpenUrlAbstract
    1. Mangelsdorf D. J.,
    2. Evans R. M.
    (1995) The RXR heterodimers and orphan receptors. Cell 83, 841–850
    OpenUrlCrossRefPubMedWeb of Science
    1. Mangelsdorf D. J.,
    2. Thummel C.,
    3. Beato M.,
    4. Herrlich P.,
    5. Schultz G.,
    6. Umesono K.,
    7. Blumberg B.,
    8. Kastner P.,
    9. Mark M.,
    10. Chambon P.,
    11. Evans R.M.
    (1995) The nuclear receptor superfamily: the second decade. Cell 83, 835–839
    OpenUrlCrossRefPubMedWeb of Science
    1. O'Malley B. W.,
    2. Conneely O. M.
    (1992) Orphan receptors: in search of a unifying hypothesis for activation. Mol. Endocrinol 6, 1359–1361
    OpenUrlCrossRefPubMedWeb of Science
    1. Palli S. R.,
    2. Hiruma K.,
    3. Riddiford L. M.
    (1992) An ecdysteroid-inducible Manduca gene similar to the Drosophila DHR3 gene, a member of the steroid hormone receptor superfamily. Dev. Biol 150, 306–318
    OpenUrlCrossRefPubMedWeb of Science
    1. Rocheleau C. E.,
    2. Downs W. D.,
    3. Lin R.,
    4. Wittman C.,
    5. Bei Y.,
    6. Cha Y.-H.,
    7. Ali M.,
    8. Priess J. R.,
    9. Mello C. C.
    (1997) Wnt signaling and an APC-related gene specify endoderm in early C. elegans embryos. Cell 90, 707–716
    OpenUrlCrossRefPubMedWeb of Science
    1. Schräder M.,
    2. Danielsson C.,
    3. Wiesenberg I.,
    4. Carlberg C.
    (1996) Identification of natural monomeric response elements fo the nuclear receptor RZR/ROR. J. Biol. Chem 271, 19732–19736
    OpenUrlAbstract/FREE Full Text
    1. Sengupta P.,
    2. Colbert H. A.,
    3. Bargmann C. I.
    (1994) The C. elegans gene odr - 7 encodes an olfactory-specific member of the nuclear receptor superfamily. Cell 79, 971–980
    OpenUrlCrossRefPubMedWeb of Science
    1. Sluder A. E.,
    2. Lindblom T.,
    3. Ruvkun G.
    (1997) The Caenorhabditis elegans orphan nuclear hormone receptor gene nhr - 2 functions in early embryonic development. Dev. Biol 184, 303–319
    OpenUrlCrossRefPubMedWeb of Science
    1. Stringham E. G.,
    2. Dixon D. K.,
    3. Jones D.,
    4. Candido E. P.
    (1992) Temporal and spatial expression patterns of the small heat shock (hsp16) genes in transgenic Caenorhabditis elegans. Mol. Biol. Cell 3, 221–233
    OpenUrlAbstract/FREE Full Text
    1. Sulston J. E.,
    2. Schierenberg E.,
    3. White J. G.,
    4. Thomson J. N.
    (1983) The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol 100, 64–119
    OpenUrlCrossRefPubMedWeb of Science
    1. Tabara H.,
    2. Motohashi T.,
    3. Kohara Y.
    (1996) A multi-well version of in situ hybridization on whole mount embryos of Caenorhabditis elegans. Nucleic Acids Res 24, 2119–2124
    OpenUrlAbstract/FREE Full Text
    1. Thummel C. S.
    (1995) From embryogenesis to metamorphosis: the regulation and function of Drosophila nuclear receptor superfamily members. Cell 83, 871–877
    OpenUrlCrossRefPubMedWeb of Science
    1. Thummel C. S.
    (1996) Files on steroids-- Drosophila metamorphosis and the mechanisms of steroid hormone action. Trends Genet 12, 306–310
    OpenUrlCrossRefPubMedWeb of Science
    1. Tsai M. J.,
    2. O'Malley B. W.
    (1994) Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Annu. Rev. Biochem 63, 451–486
    OpenUrlCrossRefPubMedWeb of Science
    1. von Mende N.,
    2. Bird D. M.,
    3. Albert P. S.,
    4. Riddle D. L.
    (1988) dpy - 13: a nematode collagen gene that affects body shape. Cell 55, 567–76
    OpenUrlCrossRefPubMedWeb of Science
    1. Waterston R.,
    2. Martin C.,
    3. Craxton M.,
    4. Hyunh C.,
    5. Coulson A.,
    6. Hillier L.,
    7. Durbin R.,
    8. Green P.,
    9. Shownkeen R.,
    10. Halloran N.,
    11. Metzstein M.,
    12. Hawkins T.,
    13. Wilson R.,
    14. Berks M.,
    15. Du Z.,
    16. Thomas K.,
    17. Thierry-Mieg J.,
    18. Sulston J.
    (1992) A survey of expressed genes in Caenorhabditis elegans. Nature Genetics 1, 114–123
    OpenUrlCrossRefPubMedWeb of Science
    1. Waterston R.,
    2. Sulston J.
    (1995) The genome of Caenorhabditis elegans. Proc. Nat. Acad. Sci. USA 92, 10836–10840
    OpenUrlAbstract/FREE Full Text
    1. Wang B. B.,
    2. Muller I. M.,
    3. Austin J.,
    4. Robinson N. T.,
    5. Chisholm A.,
    6. Kenyon C.
    (1993) A homeotic gene cluster patterns the anteroposterior body axis of C. elegans. Cell 74, 29–42
    OpenUrlCrossRefPubMedWeb of Science
    1. White K. P.,
    2. Hurban P.,
    3. Watanabe T.,
    4. Hogness D. S.
    (1997) Coordination of Drosophila metamorphosis by two ecdysone-induced nuclear receptors. Science 276, 114–117
    OpenUrlAbstract/FREE Full Text
    1. Williams M. E.,
    2. Malik A. N.,
    3. Hardin J.
    (1997) An actin-mediated two-step mechanism is required for ventral enclosure of the C. elegans hypodermis. Development 124, 2889–2901
    OpenUrlAbstract
    1. Yao T. P.,
    2. Segraves W. A.,
    3. Oro A. E.,
    4. McKeown M.,
    5. Evans R. M.
    (1992) Drosophila ultraspiracle modulates ecdysone receptor function via heterodimer formation. Cell 71, 63–72
    OpenUrlCrossRefPubMedWeb of Science
    1. Yao T. P.,
    2. Forman B. M.,
    3. Jiang Z.,
    4. Cherbas L.,
    5. Chen J. D.,
    6. McKeown M.,
    7. Cherbas P.,
    8. Evans R. M.
    (1993) Functional ecdysone receptor is the product of EcR and Ultraspiracle genes. Nature 366, 476–479
    OpenUrlCrossRefPubMedWeb of Science
    1. Zwaal R. R.,
    2. Broeks A.,
    3. van M. J.,
    4. Groenen J. T.,
    5. Plasterk R. H.
    (1993) Target-selected gene inactivation in Caenorhabditis elegans by using a frozen transposon insertion mutant bank. Proc. Natl. Acad. Sci. USA 90, 7431–7435
    OpenUrlAbstract/FREE Full Text
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JOURNAL ARTICLES
CHR3: a Caenorhabditis elegans orphan nuclear hormone receptor required for proper epidermal development and molting
M. Kostrouchova, M. Krause, Z. Kostrouch, J.E. Rall
Development 1998 125: 1617-1626;
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