Gli Protein Nuclear Localization Signal

Vitamins and Hormones

Volumn 88, Issue , 2012, Pages 73-89

  Hatayama, Minoru ^a   Aruga, Jun ^a,b  

^a RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^b SAITAMA UNIVERSITY   (Japan)

Author keywords

Bipartite NLS; Ci; Gli; Importin ; Nuclear export signal; Nuclear transport; Structure modeling

Indexed keywords

EID: 84857769595     PISSN: 00836729     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-394622-5.00004-3     Document Type: Chapter

References (60)

1. Aza-Blanc P., Ramirez-Weber F.A., Laget M.P., Schwartz C., Kornberg T.B. Proteolysis that is inhibited by hedgehog targets Cubitus interruptus protein to the nucleus and converts it to a repressor. Cell 1997, 89:1043-1053.
2. Barnfield P.C., Zhang X., Thanabalasingham V., Yoshida M., Hui C.C. Negative regulation of Gli1 and Gli2 activator function by suppressor of fused through multiple mechanisms. Differentiation 2005, 73:397-405.
3. Beak J.Y., Kang H.S., Kim Y.S., Jetten A.M. Functional analysis of the zinc finger and activation domains of Glis3 and mutant Glis3(NDH1). Nucleic Acids Res. 2008, 36:1690-1702.
4. Bedard J.E., Purnell J.D., Ware S.M. Nuclear import and export signals are essential for proper cellular trafficking and function of ZIC3. Hum. Mol. Genet. 2007, 16:187-198.
5. Brewster R., Lee J., Ruiz i Altaba A. Gli/Zic factors pattern the neural plate by defining domains of cell differentiation. Nature 1998, 393:579-583.
6. Chan D.W., Liu V.W., Leung L.Y., Yao K.M., Chan K.K., Cheung A.N., Ngan H.Y. Zic2 synergistically enhances Hedgehog signalling through nuclear retention of Gli1 in cervical cancer cells. J. Pathol. 2011, 225:525-534.
7. Chen C.H., von Kessler D.P., Park W., Wang B., Ma Y., Beachy P.A. Nuclear trafficking of Cubitus interruptus in the transcriptional regulation of Hedgehog target gene expression. Cell 1999, 98:305-316.
8. Conti E., Kuriyan J. Crystallographic analysis of the specific yet versatile recognition of distinct nuclear localization signals by karyopherin alpha. Structure 2000, 8:329-338.
9. Conti E., Uy M., Leighton L., Blobel G., Kuriyan J. Crystallographic analysis of the recognition of a nuclear localization signal by the nuclear import factor karyopherin alpha. Cell 1998, 94:193-204.
10. Ding Q., Fukami S., Meng X., Nishizaki Y., Zhang X., Sasaki H., Dlugosz A., Nakafuku M., Hui C. Mouse suppressor of fused is a negative regulator of sonic hedgehog signaling and alters the subcellular distribution of Gli1. Curr. Biol. 1999, 9:1119-1122.
11. Dingwall C., Laskey R.A. Nuclear targeting sequences-A consensus?. Trends Biochem. Sci. 1991, 16:478-481.
12. Eswar N., Webb B., Marti-Renom M.A., Madhusudhan M.S., Eramian D., Shen M.Y., Pieper U., Sali A. Comparative protein structure modeling using Modeller. Curr. Protoc. Bioinform. 2006, Chapter 5, Unit 5 6.
13. Fontes M.R., Teh T., Kobe B. Structural basis of recognition of monopartite and bipartite nuclear localization sequences by mammalian importin-alpha. J. Mol. Biol. 2000, 297:1183-1194.
14. Fontes M.R., Teh T., Jans D., Brinkworth R.I., Kobe B. Structural basis for the specificity of bipartite nuclear localization sequence binding by importin-alpha. J. Biol. Chem. 2003, 278:27981-27987.
15. Formstecher E., Aresta S., Collura V., Hamburger A., Meil A., Trehin A., Reverdy C., Betin V., Maire S., Brun C., Jacq B., Arpin M., et al. Protein interaction mapping: A Drosophila case study. Genome Res. 2005, 15:376-384.
16. Goldfarb D.S., Corbett A.H., Mason D.A., Harreman M.T., Adam S.A. Importin alpha: A multipurpose nuclear-transport receptor. Trends Cell Biol. 2004, 14:505-514.
17. Gorlich D., Mattaj I.W. Nucleocytoplasmic transport. Science 1996, 271:1513-1518.
18. Harreman M.T., Kline T.M., Milford H.G., Harben M.B., Hodel A.E., Corbett A.H. Regulation of nuclear import by phosphorylation adjacent to nuclear localization signals. J. Biol. Chem. 2004, 279:20613-20621.
19. Hatayama M., Aruga J. Characterization of the tandem CWCH2 sequence motif: A hallmark of inter-zinc finger interactions. BMC Evol. Biol. 2010, 10:53.
20. Hatayama M., Tomizawa T., Sakai-Kato K., Bouvagnet P., Kose S., Imamoto N., Yokoyama S., Utsunomiya-Tate N., Mikoshiba K., Kigawa T., Aruga J. Functional and structural basis of the nuclear localization signal in the ZIC3 zinc finger domain. Hum. Mol. Genet. 2008, 17:3459-3473.
21. Hepker J., Wang Q.T., Motzny C.K., Holmgren R., Orenic T.V. Drosophila cubitus interruptus forms a negative feedback loop with patched and regulates expression of Hedgehog target genes. Development 1997, 124:549-558.
22. Huangfu D., Anderson K.V. Signaling from Smo to Ci/Gli: Conservation and divergence of Hedgehog pathways from Drosophila to vertebrates. Development 2006, 133:3-14.
23. Ingham P.W., Nakano Y., Seger C. Mechanisms and functions of Hedgehog signalling across the metazoa. Nat. Rev. Genet. 2011, 12:393-406.
24. Ito T., Azumano M., Uwatoko C., Itoh K., Kuwahara J. Role of zinc finger structure in nuclear localization of transcription factor Sp1. Biochem. Biophys. Res. Commun. 2009, 380:28-32.
25. Jiang J., Hui C.C. Hedgehog signaling in development and cancer. Dev. Cell 2008, 15:801-812.
26. Kent D., Bush E.W., Hooper J.E. Roadkill attenuates Hedgehog responses through degradation of Cubitus interruptus. Development 2006, 133:2001-2010.
27. Kinzler K.W., Vogelstein B. The GLI gene encodes a nuclear protein which binds specific sequences in the human genome. Mol. Cell. Biol. 1990, 10:634-642.
28. Kogerman P., Grimm T., Kogerman L., Krause D., Unden A.B., Sandstedt B., Toftgard R., Zaphiropoulos P.G. Mammalian suppressor-of-fused modulates nuclear-cytoplasmic shuttling of Gli-1. Nat. Cell Biol. 1999, 1:312-319.
29. Koyabu Y., Nakata K., Mizugishi K., Aruga J., Mikoshiba K. Physical and functional interactions between Zic and Gli proteins. J. Biol. Chem. 2001, 276:6889-6892.
30. Lange A., Mills R.E., Lange C.J., Stewart M., Devine S.E., Corbett A.H. Classical nuclear localization signals: Definition, function, and interaction with importin alpha. J. Biol. Chem. 2007, 282:5101-5105.
31. Layden M.J., Meyer N.P., Pang K., Seaver E.C., Martindale M.Q. Expression and phylogenetic analysis of the zic gene family in the evolution and development of metazoans. Evodevo 2010, 1:12.
32. Lum L., Beachy P.A. The Hedgehog response network: Sensors, switches, and routers. Science 2004, 304:1755-1759.
33. Marfori M., Mynott A., Ellis J.J., Mehdi A.M., Saunders N.F., Curmi P.M., Forwood J.K., Boden M., Kobe B. Molecular basis for specificity of nuclear import and prediction of nuclear localization. Biochim. Biophys. Acta 2010.
34. Mason D.A., Stage D.E., Goldfarb D.S. Evolution of the metazoan-specific importin alpha gene family. J. Mol. Evol. 2009, 68:351-365.
35. Maurus D., Harris W.A. Zic-associated holoprosencephaly: Zebrafish Zic1 controls midline formation and forebrain patterning by regulating Nodal, Hedgehog, and retinoic acid signaling. Genes Dev. 2009, 23:1461-1473.
36. Merchant M., Vajdos F.F., Ultsch M., Maun H.R., Wendt U., Cannon J., Desmarais W., Lazarus R.A., de Vos A.M., de Sauvage F.J. Suppressor of fused regulates Gli activity through a dual binding mechanism. Mol. Cell. Biol. 2004, 24:8627-8641.
37. Methot N., Basler K. Suppressor of fused opposes hedgehog signal transduction by impeding nuclear accumulation of the activator form of Cubitus interruptus. Development 2000, 127:4001-4010.
38. Mingot J.M., Vega S., Maestro B., Sanz J.M., Nieto M.A. Characterization of Snail nuclear import pathways as representatives of C2H2 zinc finger transcription factors. J. Cell Sci. 2009, 122:1452-1460.
39. Mizugishi K., Aruga J., Nakata K., Mikoshiba K. Molecular properties of Zic proteins as transcriptional regulators and their relationship to GLI proteins. J. Biol. Chem. 2001, 276:2180-2188.
40. Monnier V., Dussillol F., Alves G., Lamour-Isnard C., Plessis A. Suppressor of fused links fused and Cubitus interruptus on the hedgehog signalling pathway. Curr. Biol. 1998, 8:583-586.
41. Motzny C.K., Holmgren R. The Drosophila cubitus interruptus protein and its role in the wingless and hedgehog signal transduction pathways. Mech. Dev. 1995, 52:137-150.
42. Nguyen V., Chokas A.L., Stecca B., Ruiz i Altaba A. Cooperative requirement of the Gli proteins in neurogenesis. Development 2005, 132:3267-3279.
43. Ohlmeyer J.T., Kalderon D. Hedgehog stimulates maturation of Cubitus interruptus into a labile transcriptional activator. Nature 1998, 396:749-753.
44. Pan Y., Bai C.B., Joyner A.L., Wang B. Sonic hedgehog signaling regulates Gli2 transcriptional activity by suppressing its processing and degradation. Mol. Cell. Biol. 2006, 26:3365-3377.
45. Pan Y., Wang C., Wang B. Phosphorylation of Gli2 by protein kinase A is required for Gli2 processing and degradation and the Sonic Hedgehog-regulated mouse development. Dev. Biol. 2009, 326:177-189.
46. Pavletich N.P., Pabo C.O. Crystal structure of a five-finger GLI-DNA complex: New perspectives on zinc fingers. Science 1993, 261:1701-1707.
47. Ruiz i Altaba A. Gli proteins encode context-dependent positive and negative functions: Implications for development and disease. Development 1999, 126:3205-3216.
48. Sasaki H., Nishizaki Y., Hui C., Nakafuku M., Kondoh H. Regulation of Gli2 and Gli3 activities by an amino-terminal repression domain: Implication of Gli2 and Gli3 as primary mediators of Shh signaling. Development 1999, 126:3915-3924.
49. Seong K.H., Akimaru H., Dai P., Nomura T., Okada M., Ishii S. Inhibition of the nuclear import of cubitus interruptus by Roadkill in the presence of strong hedgehog signal. PLoS One 2010, 5:e15365.
50. Sheng T., Chi S., Zhang X., Xie J. Regulation of Gli1 localization by the cAMP/protein kinase A signaling axis through a site near the nuclear localization signal. J. Biol. Chem. 2006, 281:9-12.
51. Shin S.H., Kogerman P., Lindstrom E., Toftgard R., Biesecker L.G. GLI3 mutations in human disorders mimic Drosophila cubitus interruptus protein functions and localization. Proc. Natl. Acad. Sci. USA 1999, 96:2880-2884.
52. Sisson B.E., Ziegenhorn S.L., Holmgren R.A. Regulation of Ci and Su(fu) nuclear import in Drosophila. Dev. Biol. 2006, 294:258-270.
53. Srivastava M., Simakov O., Chapman J., Fahey B., Gauthier M.E., Mitros T., Richards G.S., Conaco C., Dacre M., Hellsten U., Larroux C., Putnam N.H., et al. The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 2010, 466:720-726.
54. Stecca B., Ruiz i Altaba A. Context-dependent regulation of the GLI code in cancer by Hedgehog and non-Hedgehog signals. J. Mol. Cell Biol. 2010, 2:84-95.
55. Vasanth S., ZeRuth G., Kang H.S., Jetten A.M. Identification of nuclear localization, DNA binding, and transactivating mechanisms of Kruppel-like zinc finger protein Gli-similar 2 (Glis2). J. Biol. Chem. 2011, 286:4749-4759.
56. Wang Q.T., Holmgren R.A. The subcellular localization and activity of Drosophila cubitus interruptus are regulated at multiple levels. Development 1999, 126:5097-5106.
57. Wang G., Jiang J. Multiple Cos2/Ci interactions regulate Ci subcellular localization through microtubule dependent and independent mechanisms. Dev. Biol. 2004, 268:493-505.
58. Wang B., Fallon J.F., Beachy P.A. Hedgehog-regulated processing of Gli3 produces an anterior/posterior repressor gradient in the developing vertebrate limb. Cell 2000, 100:423-434.
59. Yamasaki H., Sekimoto T., Ohkubo T., Douchi T., Nagata Y., Ozawa M., Yoneda Y. Zinc finger domain of Snail functions as a nuclear localization signal for importin beta-mediated nuclear import pathway. Genes Cells 2005, 10:455-464.
60. Zhang Q., Zhang L., Wang B., Ou C.Y., Chien C.T., Jiang J. A hedgehog-induced BTB protein modulates hedgehog signaling by degrading Ci/Gli transcription factor. Dev. Cell 2006, 10:719-729.