A CCHC metal-binding domain in Nanos is essential for translational regulation

EMBO Journal

Volumn 16, Issue 4, 1997, Pages 834-843

  Curtis, Daniel ^a,b   Treiber, Daniel K ^d   Tao, Feng ^d   Zamore, Phillip D ^a   Williamson, James R ^d   Lehmann, Ruth ^a,c  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b EXELIXIS INC   (United States)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d NONE

Author keywords

CCHC; Hunchback; Nanos; Translation; Zinc

Indexed keywords

BINDING PROTEIN; MESSENGER RNA; RIBONUCLEOPROTEIN; ZINC;

ABSORPTION SPECTROSCOPY; AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ANTERIOR POSTERIOR AXIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; DROSOPHILA; EMBRYO; GENETIC CONSERVATION; METAL BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN RNA BINDING; REPRESSOR GENE; RNA TRANSLATION; TRANSLATION REGULATION;

AMINO ACID SEQUENCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CONSERVED SEQUENCE; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INSECT HORMONES; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; RECOMBINANT FUSION PROTEINS; RNA-BINDING PROTEINS; ZINC;

EID: 0031046736     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.4.834     Document Type: Article

References (47)

1. Barker, D.D., Wang, C., Moore, J., Dickinson, L.K. and Lehmann, R. (1992) Pumilio is essential for function but not for distribution of the Drosophila abdominal determinant nanos. Genes Dev., 6, 2312-2326.
2. 4 domain by 1H-nuclear magnetic resonance spectroscopy. J. Mol. Biol., 237, 201-211.
3. Bartel, D.P., Zapp, M.L., Green, M.R. and Szostak, J.W. (1991) HIV-1 Rev regulation involves recognition of non-Watson-Crick base pairs in viral RNA. Cell, 67, 529-536.
4. Berg, J.M. (1990) Zinc finger domains: hypothesis and current knowledge. Annu. Rev. Biophys. Biophys. Chem., 19, 405-421.
5. Berg, J.M. and Shi, Y. (1996) The galvanization of biology: a growing appreciation for the roles of zinc. Science, 271, 1081-1085.
6. Clemens, K.R., Wolf, V., McBryant, S.J., Zhang, P., Liao, X., Wright, P.E. and Gottesfeld, J.M. (1993) Molecular basis for specific recognition of both RNA and DNA by a zinc finger protein. Science, 260, 530-533.
7. Curtis, D., Apfeld, J. and Lehmann, R. (1995a) nanos is an evolutionarily conserved organizer of anterior-posterior polarity. Development, 121, 1899-1910.
8. Curtis, D., Lehmann, R. and Zamore, P.D. (1995b) Translational regulation in development. Cell, 81, 171-178.
9. Darlix, J.-L., Lapadat-Tapolsky, M., de Rocquigny, H. and Roques, B.P. (1995) First glimpses of structure-function relationships of the nucleocapsid protein of retroviruses. J. Mol. Biol., 254, 523-537.
10. Feuerstein, R., Wang, X., Song, D., Cooke, N.E. and Liebhaber, S.A. (1994) The LIM/double zinc-finger motif functions as a protein dimerization domain. Proc. Natl Acad. Sci. USA, 91, 10655-10659.
11. Freyd, G., Kim, S.K. and Horvitz, R.H. (1990) Novel cysteine-rich motif and homeodomain in the product of the Caenorhabditis elegans cell lineage gene lin-11. Nature, 344, 876-879.
12. Gavis, E.R. and Lehmann, R. (1992) Localization of nanos RNA controls embryonic polarity. Cell, 71, 301-313.
13. Gill, S.C. and von Hippel, P.H. (1989) Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem., 182, 319-326.
14. 4-Cys peptide binds metal ions: spectroscopic studies and a proposed three-dimensional structure. Proc. Natl Acad. Sci. USA, 86, 4047-4051.
15. Higuchi, R. (1990) Recombinant PCR. In Innis, M.A., Gelfand, D.H., Sninsky, J.J. and White, T.J. (eds), PCR Protocols: A Guide to Methods and Approaches. Academic Press, New York, pp. 177-183.
16. Hommel, U., Zurini, M. and Luyten, M. (1994) Solution structure of a cysteine rich domain of rat protein kinase C. Nature Struct. Biol., 1, 383-387.
17. Hulskamp, M., Schroder, C., Pfeifle, C., Jackle, H. and Tautz, D. (1990) A morphogenetic gradient of hunchback protein organizes the expression of the gap genes Kruppel and knirps in the early Drosophila embryo. Nature, 346, 577-580.
18. Karlsson, O., Thor, S., Norberg, T., Ohlsson, H. and Edlund, T. (1990) Insulin gene enhancer binding protein ISI-1 is a member of a novel class of proteins containing both a homeo-and a Cys-His domain. Nature, 344, 879-882.
19. Klug, A. and Schwabe, J.W.R. (1995) Zinc fingers. FASEB J., 9, 597-604.
20. Krizek, B.A., Amann, B.T., Kilfoil, V.J., Merkle, D.L. and Berg, J.M. (1991) A consensus zinc finger peptide: design, high affinity metal binding, a pH-dependent structure, and a His to Cys sequence variant. J. Am. Chem. Soc., 113, 4518-4523.
21. Lee, M.S., Cavannagh, J. and Wright, P.E. (1989) Complete assignment of the 1H NMR spectrum of a synthetic zinc finger from Xfin. Sequential resonance assignments and secondary structure. FEBS Lett., 254, 159-164.
22. Lehmann, R. and Nusslein-Volhard, C. (1991) The maternal gene nanos has a central role in pattern formation of the Drosophila embryo. Development, 112, 679-691.
23. Lim, W.A., Sauer, R.T. and Lander, A.D. (1991) Analysis of DNA-protein interactions by affinity coelectrophoresis. Methods Enzymol., 208, 196-210.
24. Lippard, S.J. and Berg, J.M. (1994) Principles of Bioinorganic Chemistry. University Science Books, Mill Valley, CA, USA.
25. Macdonald, P.M. (1992) The Drosophila pumilio gene: an unusually long transcription unit and an unusual protein. Development, 114, 221-232.
26. Michelsen, J.W., Schmeichel, K.L., Beckerle, M.C. and Winge, D.R. (1993) The LIM motif defines a specific zinc-binding protein domain. Proc. Natl Acad. Sci. USA, 90, 4404-4408.
27. Michelsen, J.W., Sewell, A.K., Louis, H.A., Olsen, J.I., Davis, D.R., Winge, D.R. and Beckerle, M.C. (1994) Mutational analysis of the metal sites in an LIM domain. J. Biol. Chem., 269, 11108-11113.
28. Mosquera, L., Forristall, C., Zhou, Y. and King, M.L. (1993) A mRNA localized to the vegetal cortex of Xenopus oocytes encodes a protein with a nanos-like zinc finger domain. Development, 117, 377-386.
29. Murata, Y. and Wharton, R.P. (1995) Binding of pumilio to maternal hunchback mRNA is required for posterior patterning in Drosophila embryos. Cell, 80, 747-756.
30. Ono, Y., Fujii, T., Igarashi, K., Kuno, T., Tanaka, C., Kikkawa, U. and Nishizuka, Y. (1989) Phorbol ester binding to protein kinase C requires a cysteine-rich zinc-finger-like sequence. Proc. Natl Acad. Sci. USA, 86, 4868-4871.
31. Parraga, G., Horvath, S.J., Eisen, A., Taylor, W.E., Hood, L., Young, E.T. and Klevit, R.E. (1988) Zinc-dependent structure of a single-finger domain of yeast ADR1. Science, 241, 1489-1492.
32. Parraga, G., Horvath, S., Hood, L., Young, E.T. and Klevit, R.E. (1990) Spectroscopic studies of wild-type and mutant 'zinc finger' peptides: determinants of domain folding and structure. Proc. Natl Acad. Sci. USA, 87, 137-141.
33. Perez-Alvarado, G.C., Miles, C., Michelsen, J.W., Louis, H.A., Winge, D.R., Beckerle, M.C. and Summers, M.F. (1994) Structure of the carboxy-terminal LIM domain from the cysteine rich protein CRP. Nature Struct. Biol., 1, 388-398.
34. Quest, A.F.G., Bardes, E.S.C. and Bell, R.M. (1994) A phorbol ester binding domain of protein kinase C gamma. J. Biol. Chem., 269, 2961-2970.
35. Rajavashisth, T.B., Taylor, A.K., Andalibi, A., Svenson, K.L. and Lusis, A.J. (1989) Identification of a zinc finger protein that binds to the sterol regulatory element. Science, 245, 640-643.
36. Schmeichel, K.L. and Beckerle, M.C. (1994) The LIM domain is a modular protein-binding interface. Cell, 79, 211-219.
37. Schwabe, J.W.R. and Klug, A. (1994) Zinc mining for protein domains. Nature Struct. Biol., 1, 345-349.
38. Schwabe, J.W.R., Chapman, J., Finch, J.T. and Rhodes, D. (1993) The crystal structure of the estrogen receptor DNA-binding domain bound to DNA: how receptors discriminate between their response elements. Cell, 75, 567-578.
39. Shamoo, Y. Webster, K.R., Williams, K.R. and Konigsberg, W.H. (1991) A retrovirus-like zinc domain is essential for translational repression of bacteriophage T4 Gene 32. J. Biol. Chem., 266, 7967-7970.
40. Shi, Y., Beger, R.D. and Berg, J.M. (1993) Metal binding properties of single amino acid deletion mutants of zinc finger peptides: studies using cobalt(II) as a spectroscopic probe. Biophys. J., 64, 749-753.
41. 113Cd NMR studies of a 1:1 Cd adduct with an 18-residue finger peptide from HIV-1 nucleic acid binding protein. J. Am. Chem. Soc., 111, 395-396.
42. Tautz, D. and Pfeifle, C. (1989) A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma, 98, 81-85.
43. Theurkauf, W.E., Baum, H., Bo, J. and Wensink, P.C. (1986) Tissue-specific and constitutive α-tubulin genes of Drosophila melanogaster code for structurally distinct proteins. Proc. Natl Acad. Sci. USA, 83, 8477-8481.
44. Tzfati, Y., Abeliovich, H., Avrahami, D. and Shlomai, J. (1995) Universal minicircle sequence binding protein, a CCHC-type zinc finger protein that binds the universal minicircle sequence of trypanosoatids. J. Biol. Chem., 270, 21339-21345.
45. Wang, C. and Lehmann, R. (1991) Nanos is the localized posterior determinant in Drosophila. Cell, 66, 637-648.
46. Wang, C., Dickinson, L.K. and Lehmann, R. (1994) Genetics of nanos localization in Drosophila. Dev. Dyn., 199, 113-115.
47. Wharton, R.P. and Struhl, G. (1991) RNA regulatory elements mediate control of Drosophila body pattern by the posterior morphogen nanos. Cell, 67, 955-967.