ZBP1 recognition of β-actin zipcode induces RNA looping

Genes and Development

Volumn 24, Issue 2, 2010, Pages 148-158

  Chao, Jeffrey A ^a   Patskovsky, Yury ^a   Patel, Vivek ^a   Levy, Matthew ^a   Almo, Steven C ^a   Singer, Robert H ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

KH domain; RNA localization; RNA binding protein; ZBP1

Indexed keywords

BETA ACTIN; BINDING PROTEIN; NUCLEOTIDE; UNCLASSIFIED DRUG; ZIPCODE BINDING PROTEIN 1;

ANIMAL CELL; ARTICLE; BINDING SITE; CONTROLLED STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; RNA BINDING; RNA SEQUENCE; SEQUENCE HOMOLOGY; X RAY CRYSTALLOGRAPHY;

ACTINS; ANIMALS; BASE SEQUENCE; CONSERVED SEQUENCE; DNA-BINDING PROTEINS; HUMANS; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RNA; RNA-BINDING PROTEINS; XENOPUS LAEVIS;

EID: 75149177311     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1862910     Document Type: Article

References (56)

1. Adams PD, Grosse-Kunstleve RW, Hung LW, Ioerger TR, McCoy AJ, Moriarty NW, Read RJ, Sacchettini JC, Sauter NK, Terwilliger TC. 2002. PHENIX: Building new software for automated crystallographic structure determination. Acta Crystallogr D Biol Crystallogr 58: 1948-1954.
2. Atlas R, Behar L, Elliott E, Ginzburg I. 2004. The insulin-like growth factor mRNA binding-protein IMP-1 and the Ras-regulatory protein G3BP associate with tau mRNA and HuD protein in differentiated P19 neuronal cells. J Neurochem 89: 613-626.
3. Atlas R, Behar L, Sapoznik S, Ginzburg I. 2007. Dynamic association with polysomes during P19 neuronal differentiation and an untranslated-region- dependent translation regulation of the tau mRNA by the tau mRNA-associated proteins IMP1, HuD, and G3BP1. J Neurosci Res 85: 173-183.
4. Auweter SD, Oberstrass FC, Allain FH. 2006. Sequence-specific binding of single-stranded RNA: Is there a code for recognition? Nucleic Acids Res 34: 4943-4959.
5. Backe PH, Messias AC, Ravelli RB, Sattler M, Cusack S. 2005. X-ray crystallographic and NMR studies of the third KH domain of hnRNP K in complex with single-stranded nucleic acids. Structure 13: 1055-1067.
6. Braddock DT, Louis JM, Baber JL, Levens D, Clore GM. 2002. Structure and dynamics of KH domains from FBP bound to single-stranded DNA. Nature 415: 1051-1056.
7. Chao JA, Lee JH, Chapados BR, Debler EW, Schneemann A, Williamson JR. 2005. Dual modes of RNA-silencing suppression by Flock House virus protein B2. Nat Struct Mol Biol 12: 952-957.
8. Collaborative Computational Project, Number 4. 1994. The CCP4 suite: Programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50: 760-763.
9. Davis IW, Leaver-Fay A, Chen VB, Block JN, Kapral GJ, Wang X, Murray LW, Arendall WB III, Snoeyink J, Richardson JS, et al. 2007. MolProbity: All-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res 35: W375-W383. doi: 10.1093/nar/gkm216.
10. Deshler JO, Highett MI, Abramson T, Schnapp BJ. 1998. A highly conserved RNA-binding protein for cytoplasmic mRNA localization in vertebrates. Curr Biol 8: 489-496.
11. Dimitriadis E, Trangas T, Milatos S, Foukas PG, Gioulbasanis I, Courtis N, Nielsen FC, Pandis N, Dafni U, Bardi G, et al. 2007. Expression of oncofetal RNA-binding protein CRD-BP/IMP1 predicts clinical outcome in colon cancer. Int J Cancer 121: 486-494.
12. Doyle GA, Betz NA, Leeds PF, Fleisig AJ, Prokipcak RD, Ross J. 1998. The c-myc coding region determinant-binding protein: A member of a family of KH domain RNA-binding proteins. Nucleic Acids Res 26: 5036-5044.
13. Du Z, Lee JK, Tjhen R, Li S, Pan H, Stroud RM, James TL. 2005. Crystal structure of the first KH domain of human poly(C)-binding protein-2 in complex with a C-rich strand of human telomeric DNA at 1.7 A. J Biol Chem 280: 38823-38830.
14. Du Z, Lee JK, Fenn S, Tjhen R, Stroud RM, James TL. 2007. X-ray crystallographic and NMR studies of protein-protein and protein-nucleic acid interactions involving the KH domains from human poly(C)-binding protein-2. RNA 13: 1043-1051.
15. Du Z, Fenn S, Tjhen R, James TL. 2008. Structure of a construct of a human poly(C)-binding protein containing the first and second KH domains reveals insights into its regulatory mechanisms. J Biol Chem 283: 28757-28766.
16. Elcheva I, Goswami S, Noubissi FK, Spiegelman VS. 2009. CRD-BP protects the coding region of βTrCP1 mRNA from miR-183-mediated degradation. Mol Cell 35: 240-246.
17. Emsley P, Cowtan K. 2004. Coot: Model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
18. Farina KL, Huttelmaier S, Musunuru K, Darnell R, Singer RH. 2003. Two ZBP1 KH domains facilitate β-actin mRNA localization, granule formation, and cytoskeletal attachment. J Cell Biol 160: 77-87.
19. Fusco D, Accornero N, Lavoie B, Shenoy SM, Blanchard JM, Singer RH, Bertrand E. 2003. Single mRNA molecules demonstrate probabilistic movement in living mammalian cells. Curr Biol 13: 161-167.
20. Garcia-Mayoral MF, Hollingworth D, Masino L, Diaz-Moreno I, Kelly G, Gherzi R, Chou CF, Chen CY, Ramos A. 2007. The structure of the C-terminal KH domains of KSRP reveals a noncanonical motif important for mRNA degradation. Structure 15: 485-498.
21. Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A. 2005. Protein identification and analysis tools on the ExPASy server. In The proteomics protocols handbook (ed. JM Walker), pp. 571-607. Humana Press, Totawa, NJ.
22. Git A, Standart N. 2002. The KH domains of Xenopus Vg1RBP mediate RNA binding and self-association. RNA 8: 1319-1333.
23. Hammer NA, Hansen TO, Byskov AG, Rajpert-De Meyts E, Grondahl ML, Bredkjaer HE, Wewer UM, Christiansen J, Nielsen FC. 2005. Expression of IGF-II mRNA-binding proteins (IMPs) in gonads and testicular cancer. Reproduction 130: 203-212.
24. Havin L, Git A, Elisha Z, Oberman F, Yaniv K, Schwartz SP, Standart N, Yisraeli JK. 1998. RNA-binding protein conserved in both microtubule- and microfilament-based RNA localization. Genes & Dev 12: 1593-1598.
25. Jiang Z, Lohse CM, Chu PG, Wu CL, Woda BA, Rock KL, Kwon ED. 2008. Oncofetal protein IMP3: A novel molecular marker that predicts metastasis of papillary and chromophobe renal cell carcinomas. Cancer 112: 2676-2682.
26. Jonson L, Vikesaa J, Krogh A, Nielsen LK, Hansen T, Borup R, Johnsen AH, Christiansen J, Nielsen FC. 2007. Molecular composition of IMP1 ribonucleoprotein granules. Mol Cell Proteomics 6: 798-811.
27. Kislauskis EH, Zhu X, Singer RH. 1994. Sequences responsible for intracellular localization of β-actin messenger RNA also affect cell phenotype. J Cell Biol 127: 441-451.
28. Kobel M, Xu H, Bourne PA, Spaulding BO, Shih Ie M, Mao TL, Soslow RA, Ewanowich CA, Kalloger SE, Mehl E, et al. 2009. IGF2BP3 (IMP3) expression is a marker of unfavorable prognosis in ovarian carcinoma of clear cell subtype. Mod Pathol 22: 469-475.
29. Krissinel E, Henrick K. 2007. Inference of macromolecular assemblies from crystalline state. J Mol Biol 372: 774-797.
30. Latham VM Jr, Kislauskis EH, Singer RH, Ross AF. 1994. β-Actin mRNA localization is regulated by signal transduction mechanisms. J Cell Biol 126: 1211-1219.
31. Lawrence JB, Singer RH. 1986. Intracellular localization of messenger RNAs for cytoskeletal proteins. Cell 45: 407-415.
32. Lecuyer E, Yoshida H, Parthasarathy N, Alm C, Babak T, Cerovina T, Hughes TR, Tomancak P, Krause HM. 2007. Global analysis of mRNA localization reveals a prominent role in organizing cellular architecture and function. Cell 131: 174-187.
33. Leung KM, van Horck FP, Lin AC, Allison R, Standart N, Holt CE. 2006. Asymmetrical β-actin mRNA translation in growth cones mediates attractive turning to netrin-1. Nat Neurosci 9: 1247-1256.
34. Lewis HA, Chen H, Edo C, Buckanovich RJ, Yang YY, Musunuru K, Zhong R, Darnell RB, Burley SK. 1999. Crystal structures of Nova-1 and Nova-2 K-homology RNA-binding domains. Structure 7: 191-203.
35. Lewis HA, Musunuru K, Jensen KB, Edo C, Chen H, Darnell RB, Burley SK. 2000. Sequence-specific RNA binding by a Nova KH domain: Implications for paraneoplastic disease and the fragile X syndrome. Cell 100: 323-332.
36. Martin KC, Ephrussi A. 2009. mRNA localization: Gene expression in the spatial dimension. Cell 136: 719-730.
37. Mili S, Moissoglu K, Macara IG. 2008. Genome-wide screen reveals APC-associated RNAs enriched in cell protrusions. Nature 453: 115-119.
38. Nielsen J, Christiansen J, Lykke-Andersen J, Johnsen AH, Wewer UM, Nielsen FC. 1999. A family of insulin-like growth factor II mRNA-binding proteins represses translation in late development. Mol Cell Biol 19: 1262-1270.
39. Nielsen FC, Nielsen J, Kristensen MA, Koch G, Christiansen J. 2002. Cytoplasmic trafficking of IGF-II mRNA-binding protein by conserved KH domains. J Cell Sci 115: 2087-2097.
40. Nielsen J, Kristensen MA, Willemoes M, Nielsen FC, Christiansen J. 2004. Sequential dimerization of human zipcode-binding protein IMP1 on RNA: A cooperative mechanism providing RNP stability. Nucleic Acids Res 32: 4368-4376.
41. Oberman F, Rand K, Maizels Y, Rubinstein AM, Yisraeli JK. 2007. VICKZ proteins mediate cell migration via their RNA binding activity. RNA 13: 1558-1569.
42. Oberstrass FC, Auweter SD, Erat M, Hargous Y, Henning A, Wenter P, Reymond L, Amir-Ahmady B, Pitsch S, Black DL, et al. 2005. Structure of PTB bound to RNA: Specific binding and implications for splicing regulation. Science 309: 2054-2057.
43. Oleynikov Y, Singer RH. 2003. Real-time visualization of ZBP1 association with β-actin mRNA during transcription and localization. Curr Biol 13: 199-207.
44. Pagano JM, Farley BM, McCoig LM, Ryder SP. 2007. Molecular basis of RNA recognition by the embryonic polarity determinant MEX-5. J Biol Chem 282: 8883-8894.
45. Patel GP, Bag J. 2006. IMP1 interacts with poly(A)-binding protein (PABP) and the autoregulatory translational control element of PABP-mRNA through the KH III-IV domain. FEBS J 273: 5678-5690.
46. Rambo RP, Doudna JA. 2004. Assembly of an active group II intron-maturase complex by protein dimerization. Biochemistry 43: 6486-6497.
47. Read RJ. 2001. Pushing the boundaries of molecular replacement with maximum likelihood. Acta Crystallogr D Biol Crystallogr 57: 1373-1382.
48. Ross AF, Oleynikov Y, Kislauskis EH, Taneja KL, Singer RH. 1997. Characterization of a β-actin mRNA zipcode-binding protein. Mol Cell Biol 17: 2158-2165.
49. Runge S, Nielsen FC, Nielsen J, Lykke-Andersen J, Wewer UM, Christiansen J. 2000. H19 RNA binds four molecules of insulin-like growth factor II mRNA-binding protein. J Biol Chem 275: 29562-29569.
50. Ryder SP, Recht MI, Williamson JR. 2008. Quantitative analysis of protein-RNA interactions by gel mobility shift. Methods Mol Biol 488: 99-115.
51. Valverde R, Pozdnyakova I, Kajander T, Venkatraman J, Regan L. 2007. Fragile X mental retardation syndrome: Structure of the KH1-KH2 domains of fragile X mental retardation protein. Structure 15: 1090-1098.
52. Valverde R, Edwards L, Regan L. 2008. Structure and function of KH domains. FEBS J 275: 2712-2726.
53. Vikesaa J, Hansen TV, Jonson L, Borup R, Wewer UM, Christiansen J, Nielsen FC. 2006. RNA-binding IMPs promote cell adhesion and invadopodia formation. EMBO J 25: 1456-1468.
54. Weidensdorfer D, Stohr N, Baude A, Lederer M, Kohn M, Schierhorn A, Buchmeier S, Wahle E, Huttelmaier S. 2009. Control of c-myc mRNA stability by IGF2BP1-associated cytoplasmic RNPs. RNA 15: 104-115.
55. 2+-dependent growth cone guidance. Nat Neurosci 9: 1265-1273.
56. Yisraeli JK. 2005. VICKZ proteins: A multi-talented family of regulatory RNA-binding proteins. Biol Cell 97: 87-96.