Regulation of Sexual Dimorphism: Mutational and Chemogenetic Analysis of the Doublesex DM Domain

REFERENCES

• Ahmad, S. M., and B. S. Baker. 2002. Sex-specific deployment of FGF signaling in Drosophila recruits mesodermal cells into the male genital imaginal disc. Cell 109:651–661.
   PubMedGoogle Scholar
• An, W., S. Cho, H. Ishii, and P. C. Wensink. 1996. Sex-specific and non-sex-specific oligomerization domains in both of the doublesex transcription factors from Drosophila melanogaster. Mol. Cell. Biol. 16:3106–3111.
   PubMedGoogle Scholar
• An, W., and P. C. Wensink. 1995. Integrating sex- and tissue-specific regulation within a single Drosophila enhancer. Genes Dev. 9:256–266.
   PubMedGoogle Scholar
• An, W., and P. C. Wensink. 1995. Three protein binding sites form an enhancer that regulates sex- and fat body-specific transcription of Drosophila yolk protein genes. EMBO J. 14:1221–1230.
   PubMedGoogle Scholar
• Bayrer, J. R., W. Zhang, and M. A. Weiss. 2005. Dimerization of doublesex is mediated by a cryptic UBA-domain fold. Implications for sex-specific gene regulation. J. Biol. Chem. 280:32989–32996.
   PubMedGoogle Scholar
• Bennett, C. P., Z. Docherty, S. A. Robb, P. Ramani, J. R. Hawkins, and D. Grant. 1993. Deletion 9p and sex reversal. J. Med. Genet. 30:518–520.
   PubMedGoogle Scholar
• Berta, P., J. R. Hawkins, A. H. Sinclair, A. Taylor, B. L. Griffiths, P. N. Goodfellow, and M. Fellous. 1990. Genetic evidence equating SRY and the testis-determining factor. Nature 348:448–450.
   PubMed Web of Science ®Google Scholar
• Bewley, C. A., A. M. Gronenborn, and G. M. Clore. 1998. Minor groove-binding architectural proteins: structure, function, and DNA recognition. Annu. Rev. Biophys. Biomol. Struct. 27:105–131.
   PubMedGoogle Scholar
• Bopp, D. 2001. Merging sex and position. Bioessays 23:304–306.
   PubMedGoogle Scholar
• Botfield, M. C., and M. A. Weiss. 1994. Bipartite DNA recognition by the human Oct-2 POU domain: POUs-specific phosphate contacts are analogous to those of bacteriophage λ repressor. Biochemistry 33:2349–2355.
   PubMedGoogle Scholar
• Bowie, J. U., J. F. Reidhaar-Olson, W. A. Lim, and R. T. Sauer. 1990. Deciphering the message in protein sciences: tolerance to amino acid substitutions. Science 247:1306–1310.
   PubMed Web of Science ®Google Scholar
• Burtis, K. C. 2002. Doublesex in the middle. Science 297:1135–1136.
   PubMedGoogle Scholar
• Burtis, K. C., K. T. Coschigano, B. S. Baker, and P. C. Wensink. 1991. The doublesex proteins of Drosophila melanogaster bind directly to a sex-specific yolk protein gene enhancer. EMBO J. 10:2577–2582.
   PubMed Web of Science ®Google Scholar
• Bushman, F. D., J. E. Anderson, S. C. Harrison, and M. Ptashne. 1985. Ethylation interference and X-ray crystallography identify similar interactions between 434 repressor and operator. Nature 316:651–653.
   PubMedGoogle Scholar
• Cho, S., and P. C. Wensink. 1997. DNA binding by the male and female doublesex proteins of Drosophila melanogaster. J. Biol. Chem. 272:3185–3189.
   PubMedGoogle Scholar
• Cho, S., and P. C. Wensink. 1998. Linkage between oligomerization and DNA binding in Drosophila doublesex proteins. Biochemistry 37:11301–11308.
   PubMedGoogle Scholar
• Cho, S., and P. C. Wensink. 1996. Purification and physical properties of the male and female double sex proteins of Drosophila. Proc. Natl. Acad. Sci. USA 93:2043–2047.
   PubMedGoogle Scholar
• Cline, T. W., and B. J. Meyer. 1996. Vive la difference: males vs females in flies vs worms. Annu. Rev. Genet. 30:637–702.
   PubMed Web of Science ®Google Scholar
• Dawes, H. E., D. S. Berlin, D. M. Lapidus, C. Nusbaum, T. L. Davis, and B. J. Meyer. 1999. Dosage compensation proteins targeted to X chromosomes by a determinant of hermaphrodite fate. Science 284:1800–1804.
   PubMedGoogle Scholar
• Dawson, P. E., T. W. Muir, I. Clark-Lewis, and S. B. Kent. 1994. Synthesis of proteins by native chemical ligation. Science 266:776–779.
   PubMed Web of Science ®Google Scholar
• Ebright, R. H., P. Cossart, B. Gicquel-Sanzey, and J. Beckwith. 1984. Mutations that alter the DNA sequence specificity of the catabolite gene activator protein of E. coli. Nature 311:232–235.
   PubMed Web of Science ®Google Scholar
• Ebright, R. H., A. Kolb, H. Buc, T. A. Kunkel, J. S. Krakow, and J. Beckwith. 1987. Role of glutamic acid-181 in DNA-sequence recognition by the catabolite gene activator protein (CAP) of Escherichia coli: Altered DNA-sequence-recognition properties of [Val181]CAP and [Leu181]CAP. Proc. Natl. Acad. Sci. USA 84:6083–6087.
   PubMedGoogle Scholar
• Ellenberger, T. E., C. J. Brandl, K. Struhl, and S. C. Harrison. 1992. The GCN4 basic region leucine zipper binds DNA as a dimer of uninterrupted alpha helices: crystal structure of the protein-DNA complex. Cell 71:1223–1237.
   PubMed Web of Science ®Google Scholar
• Elrod-Erickson, M., and C. O. Paco. 1999. Binding studies with mutants of Zif268. Contribution of individual side chains to binding affinity and specificity in the Zif268 zinc finger-DNA complex. J. Biol. Chem. 274:19281–19285.
   PubMedGoogle Scholar
• Erdman, S. E., and K. C. Burtis. 1993. The Drosophila doublesex proteins share a novel zinc finger related DNA binding domain. EMBO J. 12:527–535.
   PubMedGoogle Scholar
• Erdman, S. E., H. J. Chen, and K. C. Burtis. 1996. Functional and genetic characterization of the oligomerization and DNA binding properties of the Drosophila doublesex proteins. Genetics 144:1639–1652.
   PubMedGoogle Scholar
• Flejter, W. L., J. Fergestad, J. Gorski, T. Varvill, and S. Chandrasekharappa. 1998. A gene involved in XY sex reversal is located on chromosome 9, distal to marker D9S1779. Am. J. Hum. Genet. 63:794–802.
   PubMed Web of Science ®Google Scholar
• Giese, K., J. Cox, and R. Grosschedl. 1992. The HMG domain of lymphoid enhancer factor 1 bends DNA and facilitates assembly of functional nucleoprotein structures. Cell 69:185–195.
   PubMed Web of Science ®Google Scholar
• Graham, P., J. K. M. Penn, and P. Schedl. 2002. Masters change, slaves remain. Bioessays 25:1–4.
   Google Scholar
• Gubbay, J., J. Collignon, P. Koopman, B. Capel, A. Economou, A. Munsterberg, N. Vivian, P. Goodfellow, and R. Lovell-Badge. 1990. A gene mapping to the sex-determining region of the mouse Y chromosome is a member of a novel family of embryonically expressed genes. Nature 346:245–250.
   PubMed Web of Science ®Google Scholar
• Guioli, S., K. Schmitt, R. Critcher, M. Bouzyk, N. K. Spurr, T. Ogata, J. J. Hoo, L. Pinsky, G. Gimelli, L. Pasztor, and P. N. Goodfellow. 1998. Molecular analysis of 9p deletions associated with XY sex reversal: refining the localization of a sex-determining gene to the tip of the chromosome. Am. J. Hum. Genet. 63:905–908.
   PubMedGoogle Scholar
• Han, F., W. Watt, D. J. Duchamp, L. Callahan, F. J. Kezdy, and K. Agarwal. 1990. Molecular structure of deoxycytidyl-3′-methylphosphonate (RP) 5′-deoxyguanidine, d[Cp(CH3)G]. A neutral dinucleotide with Watson-Crick base pairing and a right handed helical twist. Nucleic Acids Res. 18:2759–2767.
   PubMed Web of Science ®Google Scholar
• Hecht, M. H., H. C. M. Nelson, and R. T. Sauer. 1983. Mutation in λ repressor's amino-terminal domain: implication for protein stability and DNA binding. Proc. Natl. Acad. Sci. USA 80:2676–2680.
   PubMed Web of Science ®Google Scholar
• Hochschild, A., and M. Ptashne. 1986. Homologous interactions of λ repressor and λ Cro with the λ operator. Cell 44:925–933.
   PubMedGoogle Scholar
• Hodgkin, J. 2002. The remarkable ubiquity of DM domain factors as regulator of sexual phenotype: ancestry or aptitude? Gene Dev. 16:2322–2326.
   PubMedGoogle Scholar
• Johnson, A. D., B. J. Meyer, and M. Ptashne. 1979. Interactions between DNA-bound repressors govern regulation by the λ phage repressor. Proc. Natl. Acad. Sci. USA 76:5061–5065.
   PubMed Web of Science ®Google Scholar
• Johnson, A. D., A. R. Poteete, G. Lauer, R. T. Sauer, G. K. Ackers, and M. Ptashne. 1981. λ Repressor and cro—components of an efficient molecular switch. Nature 294:217–223.
   PubMed Web of Science ®Google Scholar
• Keisman, E. L., and B. S. Baker. 2001. The Drosophila sex determination hierarchy modulates wingless and decapentaplegic signaling to deploy dachshund sex-specifically in the genital imaginal disc. Development 128:1643–1656.
   PubMed Web of Science ®Google Scholar
• Keisman, E. L., A. E. Christiansen, and B. S. Baker. 2001. The sex determination gene doublesex regulates the A/P organizer to direct sex-specific patterns of growth in the Drosophila genital imaginal disc. Dev. Cell. 1:215–225.
   PubMed Web of Science ®Google Scholar
• Kissinger, C. R., B. S. Liu, E. Martin-Blanco, T. B. Kornberg, and C. O. Pabo. 1990. Crystal structure of an engrailed homeodomain-DNA complex at 2.8 A resolution: a framework for understanding homeodomain-DNA interactions. Cell 63:579–590.
   PubMed Web of Science ®Google Scholar
• Koopman, P., J. Gubbay, N. Vivian, P. Goodfellow, and R. Lovell-Badge. 1991. Male development of chromosomally female mice transgenic for Sry. Nature 351:117–121.
   PubMed Web of Science ®Google Scholar
• Koopman, P., A. Munsterberg, B. Capel, N. Vivian, and R. Lovell-Badge. 1990. Expression of a candidate sex-determining gene during mouse testis differentiation. Nature 348:450–452.
   PubMed Web of Science ®Google Scholar
• Kopp, A., I. Duncan, and S. B. Carroll. 2000. Genetic control and evolution of sexually dimorphic characters in Drosophila. Nature 408:553–559.
   PubMedGoogle Scholar
• Labeots, L. A., and M. A. Weiss. 1997. Electrostatics and hydration at the homeodomain-DNA interface: chemical probes of an interfacial water cavity. J. Mol. Biol. 269:113–128.
   PubMedGoogle Scholar
• Lachenmann, M. J., J. E. Ladbury, N. B. Phillips, N. Narayana, X. Qian, and M. A. Weiss. 2002. The hidden thermodynamics of a zinc finger. J. Mol. Biol. 316:969–989.
   PubMedGoogle Scholar
• Lee, M. S., R. J. Mortishire-Smith, and P. E. Wright. 1992. The zinc finger motif. Conservation of chemical shifts and correlation with structure. FEBS Lett. 309:29–32.
   PubMed Web of Science ®Google Scholar
• Li, J. J., and I. Herskowitz. 1993. Isolation of ORC6, a component of the yeast origin recognition complex by a one-hybrid system. Science 262:1870–1874.
   PubMed Web of Science ®Google Scholar
• Ling, M., F. Merante, and B. H. Robinson. 1995. A rapid and relible DNA preparation mechod for screening a large number of yeast clones by polymerase chain reaction. Nucleic Acids Res. 23:4924–4925.
   PubMed Web of Science ®Google Scholar
• McDonald, M. T., W. Flejter, S. Sheldon, M. J. Putzi, and J. L. Gorski. 1997. XY sex reversal and gonadal dysgenesis due to 9p24 monosomy. Am. J. Med. Genet. 73:321–326.
   PubMedGoogle Scholar
• Meyer, B. J. 1988. Primary events in C. elegans sex determination and dosage compensation. Trends Genet. 12:337–342.
   Google Scholar
• Murphy, E. C., V. B. Zhurkin, J. M. Louis, G. Cornilescu, and G. M. Clore. 2001. Structural basis for SRY-dependent 46-X, Y sex reversal: modulation of DNA bending by a naturally occurring point mutation. J. Mol. Biol. 312:481–499.
   PubMedGoogle Scholar
• Narendra, U., L. Zhu, B. Li, J. Wilken, and M. A. Weiss. 2002. Sex-specific gene regulation: the doublesex DM motif is a bipartite DNA-binding domain. J. Biol. Chem. 277:43463–43473.
   PubMed Web of Science ®Google Scholar
• Noble, S. A., E. F. Fisher, and M. H. Caruthers. 1984. Methylphosphonates as probes of protein-nucleic acid interactions. Nucleic Acids Res. 12:3387–3404.
   PubMed Web of Science ®Google Scholar
• Oh, D. B., Y. G. Kim, and A. Rich. 2002. Z-DNA-binding proteins can act as potent effectors of gene expression in vivo. Proc. Natl. Acad. Sci. USA 99:16666–16671.
   PubMed Web of Science ®Google Scholar
• Ounap, K., O. Uibo, R. Zordania, L. Kiho, T. Ilus, E. Oiglane-Shlik, and O. Bartsch. 2004. Three patients with 9P deletions including DMRT1 and DMRT2: a girl with XY complement, bilateral ovotestes, and extreme growth retardation, and two two females with normal pubertal development. Am. J. Med. Genet. 130A:415–423.
   PubMedGoogle Scholar
• Pabo, C. O., and R. T. Sauer. 1992. Transcription factors: structural families and principles of DNA recognition. Annu. Rev. Biochem. 61:1053–1095.
   PubMed Web of Science ®Google Scholar
• Pavletich, N. P., and C. O. Pabo. 1991. Zinc finger-DNA recognition: crystal structure of a Zif268-DNA complex at 2.1 A. Science 252:809–817.
   PubMed Web of Science ®Google Scholar
• Phillips, N. B., A. Jancso-Radek, V. Ittah, R. Singh, G. Chan, N. Narayana, E. Haas, and M. A. Weiss. SRY and human sex determination: the basic tail of the HMG box functions as a kinetic clamp to augment DNA bending. Submitted for publication.
   Google Scholar
• Raymond, C. S., C. E. Shamu, M. M. Shen, K. J. Seifert, B. Hirsch, J. Hodgkin, and D. Zarkower. 1998. Evidence for evolutionary conservation of sex-determining genes. Nature 391:691–695.
   PubMed Web of Science ®Google Scholar
• Sigler, P. B. 1994. Chemogenetics. Nat. Struct. Biol. 1:3–4.
   PubMedGoogle Scholar
• Simpson, R. J. Y., E. D. Cram, R. Czolij, J. M. Matthews, M. Crossley, and J. P. Mackay. 2003. CCHX zinc finger derivatives retain the ability to bind Zn(II) and mediate protein-DNA interactions. J. Biol. Chem. 278:28011–28018.
   PubMedGoogle Scholar
• Tan, R., L. Chen, J. Buettner, D. Hudson, and A. D. Frankel. 1993. RNA recognition by an isolated α helix. Cell 73:1031–1040.
   PubMedGoogle Scholar
• Veitia, R. A., M. Nunes, L. Quintana-Murci, R. Rappaport, E. Thibaud, F. Jaubert, M. Fellous, K. McElreavey, J. Goncalves, M. Silva, J. C. Rodrigues, M. Caspurro, F. Boieiro, R. Marques, and J. Lavinha. 1998. Swyer syndrome and 46, XY partial gonadal dysgenesis associated with 9p deletions in the absence of monosomy-9p syndrome. Am. J. Hum. Genet. 63:901–905.
   PubMedGoogle Scholar
• Weiss, M. A., and N. Narayana. 1998. RNA recognition by arginine-rich peptide motifs. Biopolymers 48:167–180.
   PubMed Web of Science ®Google Scholar
• Wilkins, A. S. 1995. Moving up the hierarchy: a hypothesis onthe evolution of a genetic sex-determination pathway. Bioessays 17:71–77.
   PubMedGoogle Scholar
• Wolf, U. 1999. Reorganization of sex-determining pathway with the evolution of placentation. Hum. Genet. 105:288–292.
   PubMedGoogle Scholar
• Zarkower, D. 2001. Establishing sexual dimorphism: conservation amidst diversity? Nat. Rev. Genet. 2:175–185.
   PubMed Web of Science ®Google Scholar
• Zhu, L., J. Wilken, N. B. Phillips, U. Narendra, G. Chan, S. M. Stratton, S. B. Kent, and M. A. Weiss. 2000. Sexual dimorphism in diverse metazoans is regulated by a novel class of intertwined zinc fingers. Genes Dev. 14:1750–1764.
   PubMed Web of Science ®Google Scholar