Functional and structural basis of the nuclear localization signal in the ZIC3 zinc finger domain

Human Molecular Genetics

Volumn 17, Issue 22, 2008, Pages 3459-3473

  Hatayama, Minoru ^a   Tomizawa, Tadashi ^b   Sakai Kato, Kumiko ^c   Bouvagnet, Patrice ^d   Kose, Shingo ^e   Imamoto, Naoko ^e   Yokoyama, Shigeyuki ^b,f   Utsunomiya Tate, Naoko ^c   Mikoshiba, Katsuhiko ^a   Kigawa, Takanori ^b,g   Aruga, Jun ^a  

^a RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^b RIKEN YOKOHAMA INSTITUTE   (Japan)

^c MUSASHINO UNIVERSITY   (Japan)

^d INSERM   (France)

^e Japan Science and Technology Agency   (Japan)

^f UNIVERSITY OF TOKYO   (Japan)

^g TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; FUNGAL PROTEIN; KARYOPHERIN; KARYOPHERIN ALPHA; NUCLEAR PROTEIN; TRYPTOPHAN;

ARTICLE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CHELATION; CONTROLLED STUDY; GENE DISRUPTION; HETEROTAXY SYNDROME; HUMAN; HUMAN CELL; MISSENSE MUTATION; MOLECULAR INTERACTION; NUCLEAR LOCALIZATION SIGNAL; NUCLEAR MAGNETIC RESONANCE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN TRANSPORT; STRUCTURE ANALYSIS; ZINC FINGER MOTIF;

ALPHA KARYOPHERINS; AMINO ACID SEQUENCE; ANIMALS; ARGININE; CELL NUCLEUS; CIRCULAR DICHROISM; HOMEODOMAIN PROTEINS; HUMANS; KARYOPHERINS; LYSINE; MAGNETIC RESONANCE IMAGING; MICE; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEAR LOCALIZATION SIGNALS; PEPTIDE MAPPING; PROTEIN STRUCTURE, SECONDARY; RNA INTERFERENCE; TRANSCRIPTION FACTORS; ZINC FINGERS;

MYOXUS;

EID: 54949147968     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddn239     Document Type: Article

References (72)

1. Aruga, J., Kamiya, A., Takahashi, H., Fujimi, T.J., Shimizu, Y., Ohkawa, K., Yazawa, S., Umesono, Y., Noguchi, H., Shimizu, T. et al. (2006) A wide-range phylogenetic analysis of Zic proteins: Implications for correlations between protein structure conservation and body plan complexity. Genomics, 87, 783-792.
2. Aruga, J. (2004) The role of Zic genes in neural development. Mol. Cell. Neurosci., 26, 205-221.
3. Herman, G.E. and El-Hodiri, H.M. (2002) The role of ZIC3 in vertebrate development. Cytogenet. Genome Res., 99, 229-235.
4. Grinberg, I. and Millen, K.J. (2005) The ZIC gene family in development and disease. Clin. Genet., 67, 290-296.
5. Grebbia, M., Ferrero, G.B., Pilia, G., Bassi, M.T, Aylsworth, A., Penman-Splitt, M., Bird, L.M., Bamforth, J.S., Burn, J., Schlessinger, D. et al. (1997) X-linked situs abnormalities result from mutations in ZIC3, Nat. Genet., 17, 305-308.
6. Ware, S.M., Peng, J., Zhu, L., Fernbach, S., Colicos, S., Casey, B., Towbin, J. and Belmont. J.W. (2004) Identification and functional analysis of ZIC3 mutations in heterotaxy and related congenital heart defects. Am. J. Hum. Genet., 74, 93-105.
7. Aruga, J., Nagai, T., Tokuyama, T., Hayashizaki, Y., Okazaki, Y., Chapman, V.M. and Mikoshiba, K. (1996) The mouse zic gene family. Homologues of the Drosophila pair-rule gene odd-paired. J. Biol. Chem., 271, 1043-1047.
8. Mizugishi, K., Aruga, J., Nakata, K. and Mikoshiba, K. (2001) Molecular properties of Zic proteins as transcriptional regulators and their relationship to GLI proteins. J. Biol. Chem., 276, 2180-2188.
9. Carrel, T., Purandare, S.M., Harrison, W., Elder, F., Fox, T., Casey, B. and Herman, G.E. (2000) The X-linked mouse mutation Bent tail is associated with a deletion of the Zic3 locus. Hum. Mol. Genet., 9, 1937-1942.
10. Klootwijk, R., Franke, B., van der Zee, C.E., de Boer, R.T., Wilms, W., Hol, F.A. and Mariman, E.C. (2000) A deletion encompassing Zic3 in bent tail, a mouse model for X-linked neural tube defects. Hum. Mol. Genet., 9, 1615-1622.
11. Purandare, S.M., Ware, S.M., Kwan, K.M., Gebbia, M., Bassi, M.T., Deng, J.M., Vogel, H., Behringer, R.R., Belmont, J.W. and Casey, B. (2002) A complex syndrome of left-right axis, central nervous system and axial skeleton defects in Zic3 mutant mice. Development, 129, 2293-2302.
12. Aruga, J., Ogura, H., Shutoh, F., Ogawa, M., Franke, B., Nagao, S. and Mikoshiba, K. (2004) Locomotor and oculomotor impairment associated with cerebellar dysgenesis in Zic3-deficient (Bent tail) mutant mice. Eur. J. Neurosci., 20, 2159-2167.
13. Nakata, K., Nagai, T., Aruga, J. and Mikoshiba, K. (1997) Xenopus Zic3, a primary regulator both in neural and nettral crest development. Proc. Natl. Acad. Sci. USA, 94, 11980-11985.
14. Kitaguchi, T., Nagai, T., Nakata, K., Aruga, J. and Mikoshiha, K. (2000) Zic3 is involved in the left-right specification of the Xenopus embryo. Development, 127, 4787-4795.
15. Chhin, B., Hatayama, M., Bozon, D., Ogawa, M., Schon, P., Tohmonda, T., Sassolas, F., Aruga, J., Valard, A.G., Chen, S.C. et al. (20-07) Elucidation of penetrance variability of a ZIC3 mutation in a family with complex heart defects and functional analysis of ZIC3 mutations in the first zinc finger domain. Hum. Mutat., 28, 563-570.
16. Gorlich, D. and Mattaj, I.W. (1996) Nucleocytoplasmic transport. Science, 271, 1513-1518.
17. Goldfarb, D.S., Corbett, A.H., Mason, D.A., Harreman, M.T. and Adam, S.A, (2004) Importin alpha: A multipurpose nuclear-transport receptor. Trends Cell Biol., 14, 505-514.
18. Hogarth, C.A., Calanni, S., Jans, D.A. and Loveland, K.L. (2006) Importin alpha mRNAs have distinct expression profiles during spermatogenesis. Dev. Dyn., 235, 253-162.
19. Yasuhara, N., Shibazaki, N., Tanaka, S., Nagai, M., Kamikawa, Y., Oe, S.. Asally. M., Kamachi, Y., Kondoh, H. and Yoneda, Y. (2007) Triggering neural differentiation of ES cells by subtype switching of importin-alpha. Nat. Cell Biol., 9, 72-79.
20. Pelton, J.T. and McLean, L.R. (2000) Spectroscopic methods for analysis of protein secondary structure. Anal. Biochem., 277, 167-176.
21. Kelly, S.M. and Price, N.C. (2000) The use of circular dichroism in the investigation of protein structure and function. Curr. Protein Pept. Sci., 1, 349-384.
22. Plafker, K. and Macara, I.G. (2000) Facilitated nucleocytoplasmic shuttling of the Ran binding protein RanBP1. Mol. Cell. Biol., 20, 3510-3521.
23. Sheng, T., Chi, S., Zhang, X. and Xie, J. (2006) Regulation of Glil localization by the cAMP/protein kinase A signaling axis through a site near the nuclear localization signal. J. Biol. Chem., 281, 9-11
24. Wang, Q.T. and Holmgren, R.A. (1999) The subcellular localization and activity of Drosophila cubitus interruptus are regulated at multiple levels. Development, 126, 5097-5106.
25. Bedard, J.E., Purnell, J.D. and Ware, S.M. (2007) Nuclear import and export signals are essential for proper cellular trafficking and function of ZIC3. Hum. Mol. Genet., 16, 187-198.
26. Laskowski, R.A., Rullmannn, J.A., MacArthur, M.W., Kaptein, R. and Thornton, J.M. (1996) AQUA and PROCHECK-NMR: Programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR, 8 477-486.
27. Pavletich, N.P. and Pabo, C.O. (1993) Crytal structure of a five-finger GLI-DNA complex: New perspectives on zinc fingers. Science, 261 1701-1707.
28. Pavletich, N.P. and Pabo, C.O. (1991) Zinc finger-DNA recognition: crystal structure of a Zif268-DNA complex at 2.1 A. Science, 252, 809-817.
29. Beak, J.Y., Kang, H.S., Kim, Y.S. and Jetten. A.M. (2008) Functional analysis of the zinc finger and activation domain of Glis3 and mutant Glis3(NDH1). Nucleic Acids Res., 36, 1690-1702.
30. Dingwall, C. and Laskey, R.A. (1991) Nuclear targeting sequences-a. consensus? Trends Biochem. Sci., 16, 478-481.
31. Jans, D.A., Xiao, C.Y. and Lam, M.H. (2000) Nuclear targeting signal recognition: A key control point in nuclear transport? Bioessays, 22, 532-544.
32. Pandya, K. and Townes, T.M. (2002) Basic residues within the Kruppel zinc finger DNA binding domains are the critical nuclear localization determinants of EKLF/KLF-1. J. Biol. Chem. 277, 16304-16312.
33. Yang, M., May, W.S. and Ito, T. (1999) JAZ requires the double-stranded RNA-binding zinc finger motifs for nuclear localization. J. Biol. Chem., 274, 27399-27406.
34. Huang, S.M., Huang, S.P., Wang, S.L. and Liu, P.Y. (2007) Importin alpha1 is involved in the nuclear localization of Zac1 and the induction of p21WAF1/CIP1 by Zac1. Biochem. J., 402, 359-366.
35. Quadrini. K.J. and Bieker, J.J. (2002) Krüppel-like zinc fingers bind to nuclear import proteins and are required for efficient nuclear localization of erythroid Krüppel-like factor. J. Biol. Chem., 277, 32243-32252.
36. Conti, E., Uy, M., Leighton, L., Blobel, G. and Kuriyan, J. (1998) Crystallographic analysis of the recognition of a nuclear localization signal by the nuclear import factor karyopherin alpha. Cell, 94 193-204.
37. Cutress, M.L., Whitaker, H.C., Mills, I.G., Stewart, M. and Neal, D.E. (2008) Structural basis for the nuclear import of the human androgen receptor. J. Cell Sci., 121, 957-968.
38. Fontes, M.R., Teh, T. and Kobe, B. (2000) Structural basis of recognition f monopartite and bipartite nuclear localization sequences by mammalian mportin-alpha. J. Mol. Biol., 297, 1183-1194.
39. Conti, E. and Kuriyan, J. (2000) Crystallographic analysis of the specific yet versatile recognition of distinct nuclear localization signals by karyopherin alpha. Structure, 8, 329-338.
40. Tarendeau, F., Boudet, J., Guilligay, D., Mas, P.J., Bougault, C.M., Boulo, S., Baudin, F., Ruigrok, R.W., Daigle, N., Ellenberg, J. et al. (2007) Structure and nuclear import function of the C-terminal domain of influenza virus polymerase PB2 subunit. Nat. Struct. Mol. Biol., 14, 229-233.
41. Fontes, M.R., Teh, T., Jans, D., Brinkworth, R.I. and Kobe, B. (2003) Structural basis for the specificity of bipartite nuclear localization sequence binding by importin-alpha. J. Biol. Chem., 278, 27981-27987.
42. Espeso, E.A., Tilburn, J., Sanchez-Pulido, L., Brown, C.V., Valencia, A., Arst, H.N. Jr and Penalva, M.A. (1997) Specific DNA recognition by the Aspergillus nidulans three zinc finger transcription factor PacC. J. Mol. Biol., 274, 466-480.
43. Wang, Z., Feng, L.S., Matskevich, V., Venkataraman, K., Parasuram, P. and Laity, J.H. (2006) Solution structure of a Zap1 zinc-responsive domain provides insights into metalloregulatory transcriptional repression in Saccharomyces cerevisiae, J. Mol. Biol. 357, 1167-1183.
44. Sakai-Kato, K., Ishiguro, A., Mikoshiba, K., Aruga, J. and Utsunomiya-Tate, N. (2008) CD spectra show the relational style between Zic-, Gli-, Glis-zinc finger protein and DNA. Biochim. Biophys. Acta 1784, 1011-1019.
45. 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 singie-finger domain of yeast ADR1. Science, 241, 1489-1492.
46. Nomura, A. and Sugiura, Y. (2002) Contribution of individual zinc ligands to metal binding and peptide folding of zinc finger peptides. Inorg. Chem., 41, 3693-3698.
47. Frankel, A.D., Berg, J.M. and Pabo, C.O. (1987) Metal-dependent folding of a single zinc finger from transcription factor IIIA. Proc. Natl. Acad. Sci. USA, 84, 4841-4845.
48. Hard, F.U. and Hayer-Hartl, M. (2002) Molecular chaperones in the cytosol: From nascent chain to folded protein. Science, 295, 1852-1858.
49. Spiess, C., Meyer, A.S., Reissmann, S. and Frydman, J. (2004) Mechanism of the eukaryotic chaperonin: Protein folding in the chamber of secrets. Trends Cell Biol., 14, 598-604.
50. Turner, D.L. and Weintraub., H. (1994) Expression of achaete-scute homolog 3 in Xenopus embryos converts ectodermal cells to a neural fate. Genes Dev., 8, 1434-1447.
51. Kinzler. K.W. and Vogelstein. B. (1990) The GL1 gene encodes a nuclear protein which binds specific sequences in the human genome. Mol. Cell. Biol., 10, 634-642.
52. Carninci, P., Kasukawa, T., Katayama, S., Gough, J., Frith, M.C., Maeda, N., Oyama, R., Ravasi, T., Lenhard, B., Wells, C. et al. (2005) The transcriptional landscape of the mammalian genome. Science, 309, 1559-1563.
53. Kamitori, K., Machide, M., Tomita, K., Nakafuku, M. and Kohsaka, S. (2002) Cell-type-specific expression of protein tyrosine kinase-telated receptor RYK in the central nervous system of the rat. Brain Res. Mol. Brain Res., 104, 255-266.
54. Galigniana, M.D., Scruggs, J.L., Herrington, J., Welsh, M.J., Carter-Su, C., Housley, P.R. and Pratt, W.B. (1998) Heat shock protein 90-dependent (geldanamycin-inhibited) movement of the glucocorticoid receptor through the cytoplasm to the nucleus requires intact cytoskeleton. Mol. Endocrinol., 12, 1903-1913.
55. Koyabu, Y., Nakata, K., Mizugishi, K., Aruga, J. and Mikoshiba, K. (2001) Physical and functional interactions between Zic and Gli proteins. J. Biol. Chem., 276, 6889-6892.
56. Kigawa, T., Yabuki, T., Yoshida, Y., Tsutsui, M., Ito, Y., Shibata, T. and Yokoyama, S. (1999) Cell-free production and stable-isotope labeling of milligram quantities of proteins. FEBS Lett., 442, 15-19.
57. Matsuda, T., Koshiba, S., Tochio, N., Seki, E., Iwasaki, N., Yabuki, T., Inoue, M., Yokoyama, S. and Kigawa, T. (2007) Improving cell-free protein synthesis for stable-isotope labeling. J. Biomol. NMR, 37, 225-229.
58. Tochio, N., Umehara, T., Koshiba, S., Inoue. M., Yabuki. T., Aoki, M., Seki, E., Watanabe, S., Tomo, Y., Hanada, M. et al. (2006) Solution structure of the SWIRM domain of human historic demethylase LSD1. Structure, 14, 457-468.
59. Cavanagh, J., Fairbrother, J.W., Palmer, G.A. and Skelton, J.N. (1996) Protein NMR Spectroscopy, Principles and Practice. Academic Press, Inc, San Diego.
60. Ikura, M., Kay, L.E. and Bax, A. (1990) A novel approach for sequential assignment of 1H, 13C, and 15N spectra of proteins: Heteronuclear triple-resonance three-dimensional NMR spectroscopy. Application to calmodulin. Biochemistry, 29, 4659-4667.
61. Bax, A., Vuister, G.W., Grzesick, S., Delaglio, F., Wang, A.C., Tschudin, R. and Zhu, G. (1994) Measurement of homo- and heteronuclear J couplings from quantitative J correlation. Methods Enzymol., 239, 79-105.
62. Kay, L.E. (1997) NMR methods for the study of protein structure and dynamics. Biochem. Cell Biol., 75, 1-15.
63. Sattler, M., Schleucher, J. and Griesinger, C. (1999) Heteronuclear multidimensional NMR experiments for the structure determination of proteins in solution employing pulsed field gradients. Prog. NMR Spectrosc., 24, 93-158.
64. Delaglio, F., Grzesiek, S., Vuister, G.W., Zhu, G., Pfeifer, J. and Bax, A. 1995) NMRPipe: A multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR, 6, 277-293.
65. Kobayashi, N., Iwahara, J., Koshiba, S., Tomizawa, T., Tochio, N., Güntert, P., Kigawa, T. and Yokoyama, S. (2007) KUJIRA, a package of integrated modules for systematic and interactive analysis of NMR data directed to high-throughput NMR structure studies. J. Biomol. NMR, 39, 31-52.
66. Johnson, A.B. and Blevins, R. (1994) NMRView: A computer program for the visualization and analysis of NMR data. J. Biomol. NMR, 4, 603-614.
67. Johnson, B.A. (2004) Using NMR View to visualize and analyze the NMR spectra of macromolecules. Methods Mol. Biol., 278, 313-352.
68. Güntert, P., Mumenthaler, C. and Wuthrich, K. (1997) Torsion angle dynamics for NMR structure calculation with the new program DYANA. J. Mol. Biol., 273, 283-298.
69. Herrmann, T., Güntert, P. and Wuthrich, K. (2002) Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J. Mol. Biol., 319, 209-227.
70. Jee, J. and Gütert, P. (2003) Influence of the completeness of chemical shift assignments on NMR structures obtained with automated NOE assignment. J. Struct. Funct. Genomics, 4, 179-189.
71. Güntert, P. (2004) Automated NMR structure calculation with CYANA. Methods Mol. Biol., 278, 353-378.
72. Kelly, K.F., Otchere, A.A., Graham, M. and Daniel, J.M. (2004) Nuclear import of the BTB/POZ transcriptional regulator Kaiso. J. Cell Sci. 117, 6143-6152.