A protein • protein interaction platform involved in recruitment of GLD-3 to the FBF ×fem-3 mRNA complex

Journal of Molecular Biology

Volumn 425, Issue 4, 2013, Pages 738-754

  Wu, Joann ^a   Campbell, Zachary T ^b   Menichelli, Elena ^a   Wickens, Marvin ^b   Williamson, James R ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

fem 3; germline development; PUF protein; RNA protein interactions; RNA binding proteins

Indexed keywords

AMINO ACID; FAMILY MEMBER FEM 3 BINDING FACTOR; GERMLINE DEVELOPMENT DEFECTIVE 3; MESSENGER RNA; PROTEIN; UNCLASSIFIED DRUG; CAENORHABDITIS ELEGANS PROTEIN; FEM 3 BINDING PROTEIN, C ELEGANS; FEM 3 PROTEIN, C ELEGANS; FEM-3 PROTEIN, C ELEGANS; FEM-3-BINDING PROTEIN, C ELEGANS; GLD 3 PROTEIN, C ELEGANS; GLD-3 PROTEIN, C ELEGANS; HELMINTH RNA; RNA BINDING PROTEIN;

3' UNTRANSLATED REGION; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; POINT MUTATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RNA BINDING; SPERMATOGENESIS; ANIMAL; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; GEL MOBILITY SHIFT ASSAY; GENETICS; METABOLISM; METHODOLOGY; MOLECULAR GENETICS; MUTATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN ANALYSIS; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY; TWO HYBRID SYSTEM;

CAENORHABDITIS ELEGANS; EUKARYOTA;

AMINO ACID SEQUENCE; AMINO ACIDS; ANIMALS; BINDING SITES; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ELECTROPHORETIC MOBILITY SHIFT ASSAY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN STRUCTURE, TERTIARY; REPETITIVE SEQUENCES, AMINO ACID; RNA, HELMINTH; RNA, MESSENGER; RNA-BINDING PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; TWO-HYBRID SYSTEM TECHNIQUES;

MLCS; MLOWN;

EID: 84873413339     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2012.11.013     Document Type: Article

References (51)

1. P. Lasko Gene regulation at the RNA layer: RNA binding proteins in intercellular signaling networks Sci. STKE 2003 RE6
2. B.M. Lunde, C. Moore, and G. Varani RNA-binding proteins: modular design for efficient function Nat. Rev. Mol. Cell Biol. 8 2007 479 490
3. T. Glisovic, J.L. Bachorik, J. Yong, and G. Dreyfuss RNA-binding proteins and post-transcriptional gene regulation FEBS Lett. 582 2008 1977 1986
4. J. Kimble Molecular regulation of the mitosis/meiosis decision in multicellular organisms Cold Spring Harbor Perspect. Biol. 3 2011 a002683
5. J.P. Gudikote, and M.F. Wilkinson RNA-Binding Proteins: Regulation of mRNA Splicing, Export and Decay eLS 2001 John Wiley & Sons, Ltd
6. S. Kuersten, and E.B. Goodwin The power of the 3′ UTR: translational control and development Nat. Rev. Genet. 4 2003 626 637
7. B. Thompson, M. Wickens, and J. Kimble Translational control in development M.B. Mathews, N. Sonenberg, J.W.B. Hershey, Translational Control in Biology and Medicine 2007 Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY 507 544
8. J. Kimble, and S.L. Crittenden Controls of germline stem cells, entry into meiosis, and the sperm/oocyte decision in Caenorhabditis elegans Annu. Rev. Cell Dev. Biol. 23 2007 405 433
9. E. Kaymak, L.M. Wee, and S.P. Ryder Structure and function of nematode RNA-binding proteins Curr. Opin. Struct. Biol. 20 2010 305 312
10. P.E. Kuwabara, and M.D. Perry It ain't over till it's ova: germline sex determination in C. elegans BioEssays 23 2001 596 604
11. A. Puoti, P. Pugnale, M. Belfiore, A.C. Schlappi, and Z. Saudan RNA and sex determination in Caenorhabditis elegans. Post-transcriptional regulation of the sex-determining tra-2 and fem-3 mRNAs in the Caenorhabditis elegans hermaphrodite EMBO Rep. 2 2001 899 904
12. E.B. Goodwin, and R.E. Ellis Turning clustering loops: sex determination in Caenorhabditis elegans Curr. Biol. 12 2002 R111 R120
13. B. Zhang, M. Gallegos, A. Puoti, E. Durkin, S. Fields, J. Kimble, and M.P. Wickens A conserved RNA-binding protein that regulates sexual fates in the C. elegans hermaphrodite germ line Nature 390 1997 477 484
14. S.L. Crittenden, D.S. Bernstein, J.L. Bachorik, B.E. Thompson, M. Gallegos, and A.G. Petcherski A conserved RNA-binding protein controls germline stem cells in Caenorhabditis elegans Nature 417 2002 660 663
15. L.B. Lamont, S.L. Crittenden, D. Bernstein, M. Wickens, and J. Kimble FBF-1 and FBF-2 regulate the size of the mitotic region in the C. elegans germline Dev. Cell 7 2004 697 707
16. N. Suh, S.L. Crittenden, A. Goldstrohm, B. Hook, B. Thompson, M. Wickens, and J. Kimble FBF and its dual control of gld-1 expression in the Caenorhabditis elegans germline Genetics 181 2009 1249 1260
17. B. Kraemer, S. Crittenden, M. Gallegos, G. Moulder, R. Barstead, J. Kimble, and M. Wickens NANOS-3 and FBF proteins physically interact to control the sperm-oocyte switch in Caenorhabditis elegans Curr. Biol. 9 1999 1009 1018
18. C. Luitjens, M. Gallegos, B. Kraemer, J. Kimble, and M. Wickens CPEB proteins control two key steps in spermatogenesis in C. elegans Genes Dev. 14 2000 2596 2609
19. C.R. Eckmann, B. Kraemer, M. Wickens, and J. Kimble GLD-3, a bicaudal-C homolog that inhibits FBF to control germline sex determination in C. elegans Dev. Cell 3 2002 697 710
20. K. Friend, Z.T. Campbell, A. Cooke, P. Kroll-Conner, M.P. Wickens, and J. Kimble A conserved PUF-Ago-eEF1A complex attenuates translation elongation Nat. Struct. Mol. Biol. 19 2012 176 183
21. U. Tran, L.M. Pickney, B.D. Ozpolat, and O. Wessely Xenopus Bicaudal-C is required for the differentiation of the amphibian pronephros Dev. Biol. 307 2007 152 164
22. C. Maisonneuve, I. Guilleret, P. Vick, T. Weber, P. Andre, and T. Beyer Bicaudal C, a novel regulator of Dvl signaling abutting RNA-processing bodies, controls cilia orientation and leftward flow Development 136 2009 3019 3030
23. U. Tran, L. Zakin, A. Schweickert, R. Agrawal, R. Doger, and M. Blum The RNA-binding protein bicaudal C regulates polycystin 2 in the kidney by antagonizing miR-17 activity Development 137 2010 1107 1116
24. D.J. Bouvrette, V. Sittaramane, J.R. Heidel, A. Chandrasekhar, and E.C. Bryda Knockdown of bicaudal C in zebrafish (Danio rerio) causes cystic kidneys: a nonmammalian model of polycystic kidney disease Comp. Med. 60 2010 96 106
25. L. Wang, C.R. Eckmann, L.C. Kadyk, M. Wickens, and J. Kimble A regulatory cytoplasmic poly(A) polymerase in Caenorhabditis elegans Nature 419 2002 312 316
26. J.E. Kwak, L. Wang, S. Ballantyne, J. Kimble, and M. Wickens Mammalian GLD-2 homologs are poly(A) polymerases Proc. Natl Acad. Sci. USA 101 2004 4407 4412
27. L. Rouhana, L. Wang, N. Buter, J.E. Kwak, C.A. Schiltz, and T. Gonzalez Vertebrate GLD2 poly(A) polymerases in the germline and the brain RNA 11 2005 1117 1130
28. J.E. Kwak, E. Drier, S.A. Barbee, M. Ramaswami, J.C. Yin, and M. Wickens GLD2 poly(A) polymerase is required for long-term memory Proc. Natl Acad. Sci. USA 105 2008 14644 14649
29. D.M. Burns, A. D'Ambrogio, S. Nottrott, and J.D. Richter CPEB and two poly(A) polymerases control miR-122 stability and p53 mRNA translation Nature 473 2011 105 108
30. I.M. Alexandrov, M. Ivshina, D.Y. Jung, R. Friedline, H.J. Ko, and M. Xu Cytoplasmic polyadenylation element binding protein deficiency stimulates PTEN and Stat3 mRNA translation and induces hepatic insulin resistance PLoS Genet. 8 2012 e1002457
31. Y. Wang, L. Opperman, M. Wickens, and T.M. Hall Structural basis for specific recognition of multiple mRNA targets by a PUF regulatory protein Proc. Natl Acad. Sci. USA 106 2009 20186 20191
32. P.D. Zamore, J.R. Williamson, and R. Lehmann The Pumilio protein binds RNA through a conserved domain that defines a new class of RNA-binding proteins RNA 3 1997 1421 1433
33. P.D. Zamore, D.P. Bartel, R. Lehmann, and J.R. Williamson The PUMILIO-RNA interaction: a single RNA-binding domain monomer recognizes a bipartite target sequence Biochemistry 38 1999 596 604
34. X. Wang, P.D. Zamore, and T.M. Hall Crystal structure of a Pumilio homology domain Mol. Cell 7 2001 855 865
35. T.A. Edwards, S.E. Pyle, R.P. Wharton, and A.K. Aggarwal Structure of Pumilio reveals similarity between RNA and peptide binding motifs Cell 105 2001 281 289
36. X. Wang, J. McLachlan, P.D. Zamore, and T.M. Hall Modular recognition of RNA by a human pumilio-homology domain Cell 110 2002 501 512
37. L. Opperman, B. Hook, M. DeFino, D.S. Bernstein, and M. Wickens A single spacer nucleotide determines the specificities of two mRNA regulatory proteins Nat. Struct. Mol. Biol. 12 2005 945 951
38. C.G. Cheong, and T.M. Hall Engineering RNA sequence specificity of Pumilio repeats Proc. Natl Acad. Sci. USA 103 2006 13635 13639
39. M.T. Miller, J.J. Higgin, and T.M. Hall Basis of altered RNA-binding specificity by PUF proteins revealed by crystal structures of yeast Puf4p Nat. Struct. Mol. Biol. 15 2008 397 402
40. D. Zhu, C.R. Stumpf, J.M. Krahn, M. Wickens, and T.M. Hall A 5′ cytosine binding pocket in Puf3p specifies regulation of mitochondrial mRNAs Proc. Natl Acad. Sci. USA 106 2009 20192 20197
41. D. Bernstein, B. Hook, A. Hajarnavis, L. Opperman, and M. Wickens Binding specificity and mRNA targets of a C. elegans PUF protein, FBF-1 RNA 11 2005 447 458
42. Y.Y. Koh, Y. Wang, C. Qiu, L. Opperman, L. Gross, T.M. Tanaka Hall, and M. Wickens Stacking interactions in PUF-RNA complexes RNA 17 2011 718 727
43. C.R. Eckmann, S.L. Crittenden, N. Suh, and J. Kimble GLD-3 and control of the mitosis/meiosis decision in the germline of Caenorhabditis elegans Genetics 168 2004 147 160
44. Z.T. Campbell, E. Menichelli, K. Friend, J. Wu, J. Kimble, J.R. Williamson, and M. Wickens A conserved interface between PUF and CPEB proteins J Biol Chem 287 2012 18854 18862
45. Menichelli, E., Wu, J., Campbell, Z. T., Wickens, M. & Williamson, J. R. Biochemical characterization of the Caenorhabditis elegans FBF × CPB-1 translational regulation complex identifies conserved protein interaction hotspots. Submitted.
46. M.A. Miller, and W.M. Olivas Roles of Puf proteins in mRNA degradation and translation Wiley Interdiscip. Rev.: RNA 2 2011 471 492
47. J. Sonoda, and R.P. Wharton Recruitment of Nanos to hunchback mRNA by Pumilio Genes Dev. 13 1999 2704 2712
48. T.A. Edwards, B.D. Wilkinson, R.P. Wharton, and A.K. Aggarwal Model of the brain tumor-Pumilio translation repressor complex Genes Dev. 17 2003 2508 2513
49. A. Rybarska, M. Harterink, B. Jedamzik, A.P. Kupinski, M. Schmid, and C.R. Eckmann GLS-1, a novel P granule component, modulates a network of conserved RNA regulators to influence germ cell fate decisions PLoS Genet. 5 2009 e1000494
50. S.P. Ryder, and J.R. Williamson Specificity of the STAR/GSG domain protein Qk1: implications for the regulation of myelination RNA 10 2004 1449 1458
51. S.P. Ryder, L.A. Frater, D.L. Abramovitz, E.B. Goodwin, and J.R. Williamson RNA target specificity of the STAR/GSG domain post-transcriptional regulatory protein GLD-1 Nat. Struct. Mol. Biol. 11 2004 20 28