The NHL domain of BRAT is an RNA-binding domain that directly contacts the hunchback mRNA for regulation

Genes and Development

Volumn 28, Issue 7, 2014, Pages 749-764

  Loedige, Inga ^a   Stotz, Mathias ^a   Qamar, Saadia ^b,c   Kramer, Katharina ^b,c   Hennig, Janosch ^d,e   Schubert, Thomas ^a   Löffler, Patrick ^a   Längst, Gernot ^a   Merkl, Rainer ^a   Urlaub, Henning ^b,c   Meister, Gunter ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

^b MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^c UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^d INSTITUTE OF EPIDEMIOLOGY   (Germany)

^e Munich Center for Integrated Protein Science   (Germany)

Author keywords

BRAT; Gene regulation; Hunchback; RNA binding; Translational repression; TRIM NHL

Indexed keywords

DROSOPHILA PROTEIN; MESSENGER RNA; RNA BINDING PROTEIN;

3' UNTRANSLATED REGION; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; ELECTROPHORETIC MOBILITY; GENE CONTROL; HUNCHBACK; IN VITRO STUDY; IN VIVO STUDY; MASS SPECTROMETRY; NHL DOMAIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN RNA BINDING; REGULATORY MECHANISM; RNA BINDING; RNA SEQUENCE; RNA TRANSLATION; SPINE DISEASE; STOICHIOMETRY;

BRAT; GENE REGULATION; HUNCHBACK; RNA BINDING; TRANSLATIONAL REPRESSION; TRIM-NHL;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BINDING SITES; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INSECT PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; RNA, MESSENGER; RNA-BINDING PROTEINS; SEQUENCE ALIGNMENT; TRANSCRIPTION FACTORS;

EID: 84898867787     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.236513.113     Document Type: Article

References (55)

1. Arama E., Dickman D, Kimchie Z, Shearn A, Lev Z. 2000. Mutations in the β-propeller domain of the Drosophila brain tumor (brat) protein induce neoplasm in the larval brain. Oncogene 19: 3706-3716.
2. Asaoka-Taguchi M, Yamada M, Nakamura A, Hanyu K, Kobayashi S. 1999. Maternal Pumilio acts together with Nanos in germline development in Drosophila embryos. Nat Cell Biol 1: 431-437.
3. Baker R. T, Catanzariti AM, Karunasekara Y, Soboleva TA, Sharwood R, Whitney S, Board PG. 2005. Using deubiquitylating enzymes as research tools. Methods Enzymol 398: 540-554.
4. Baltz A. G, Munschauer M, Schwanhausser B, Vasile A, Murakawa Y, Schueler M., Youngs N, Penfold-Brown D, Drew K, Milek M, et al. 2012. The mRNA-bound proteome and its global occupancy profile on protein-coding transcripts. Mol Cell 46: 674-690.
5. Betschinger J., Mechtler K, Knoblich JA. 2006. Asymmetric segregation of the tumor suppressor brat regulates self-renewal in Drosophila neural stem cells. Cell 124: 1241-1253.
6. Castello A., Fischer B, Eichelbaum K, Horos R, Beckmann BM, Strein C., Davey NE, Humphreys DT, Preiss T, Steinmetz LM, et al. 2012. Insights into RNA biology from an atlas of mammalian mRNA-binding proteins. Cell 149: 1393-1406.
7. Catanzariti A. M, Soboleva TA, Jans DA, Board PG, Baker RT. 2004. An efficient system for high-level expression and easy purification of authentic recombinant proteins. Protein Sci 13: 1331-1339.
8. Chang H. M, Martinez NJ, Thornton JE, Hagan JP, Nguyen KD, Gregory R.I. 2012. Trim71 cooperates with microRNAs to repress Cdkn1a expression and promote embryonic stem cell proliferation. Nat Commun 3: 923.
9. Chekulaeva M., Filipowicz W, Parker R. 2009. Multiple independent domains of dGW182 function in miRNA-mediated repression in Drosophila. RNA 15: 794-803.
10. Cherbas L., Willingham A, Zhang D, Yang L, Zou Y, Eads BD, Carlson J. W, Landolin JM, Kapranov P, Dumais J, et al. 2011. The transcriptional diversity of 25 Drosophila cell lines. Genome Res 21: 301-314.
11. Cho P. F, Gamberi C, Cho-Park YA, Cho-Park IB, Lasko P, Sonenberg N. 2006. Cap-dependent translational inhibition establishes two opposing morphogen gradients in Drosophila embryos. Curr Biol 16: 2035-2041.
12. Chufan E. E, De M, Eipper BA, Mains RE, Amzel LM. 2009. Amidation of bioactive peptides: the structure of the lyase domain of the amidating enzyme. Structure 17: 965-973.
13. Curtis D., Lehmann R, Zamore PD. 1995. Translational regulation in development. Cell 81: 171-178.
14. Duchaine T. F, Wohlschlegel JA, Kennedy S, Bei Y, Conte D Jr, Pang K., Brownell DR, Harding S, Mitani S, Ruvkun G, et al. 2006. Functional proteomics reveals the biochemical niche of C. elegans DCR-1 in multiple small-RNA-mediated pathways. Cell 124: 343-354.
15. Edwards T. A, Wilkinson BD, Wharton RP, Aggarwal AK. 2003. Model of the brain tumor-Pumilio translation repressor complex. Genes Dev 17: 2508-2513.
16. Frank D. J, Edgar BA, Roth MB. 2002. The Drosophila melanogaster gene brain tumor negatively regulates cell growth and ribosomal RNA synthesis. Development 129: 399-407.
17. Gerber A. P, Luschnig S, Krasnow MA, Brown PO, Herschlag D. 2006. Genome-wide identification of mRNAs associated with the translational regulator PUMILIO in Drosophila melanogaster. Proc Natl Acad Sci 103: 4487-4492.
18. Good M. C, Greenstein AE, Young TA, Ng HL, Alber T. 2004. Sensor domain of the Mycobacterium tuberculosis receptor Ser/Thr protein kinase, PknD, forms a highly symmetric β propeller. J Mol Biol 339: 459-469.
19. Hammell C. M, Lubin I, Boag PR, Blackwell TK, Ambros V. 2009. nhl-2 modulates microRNA activity in Caenorhabditis elegans. Cell 136: 926-938.
20. Harris R. E, Pargett M, Sutcliffe C, Umulis D, Ashe HL. 2011. Brat promotes stem cell differentiation via control of a bistable switch that restricts BMP signaling. Dev Cell 20: 72-83.
21. Hulskamp M., Pfeifle C, 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.
22. Jerabek-Willemsen M, Wienken CJ, Braun D, Baaske P, Duhr S. 2011. Molecular interaction studies using microscale thermophoresis. Assay Drug Dev Technol 9: 342-353.
23. Kanai Y., Dohmae N, Hirokawa N. 2004. Kinesin transports RNA: isolation and characterization of an RNA-transporting granule. Neuron 43: 513-525.
24. Kramer K., Hummel P, Hsiao H-H, Luo X, Wahl M, Urlaub H. 2011. Mass-spectrometric analysis of proteins cross-linked to 4-thio-uracil-and 5-bromo-uracil-substituted RNA. Int J Mass Spectrom 304: 184-194.
25. Kwon S. C, Yi H, Eichelbaum K, Fohr S, Fischer B, You KT, Castello A., Krijgsveld J, Hentze MW, Kim VN. 2013. The RNA-binding protein repertoire of embryonic stem cells. Nat Struct Mol Biol 20: 1122-1130.
26. Lau C. K, Bachorik JL, Dreyfuss G. 2009. Gemin5-snRNA interaction reveals an RNA binding function for WD repeat domains. Nat Struct Mol Biol 16: 486-491.
27. Lee C. Y, Wilkinson BD, Siegrist SE, Wharton RP, Doe CQ. 2006. Brat is a Miranda cargo protein that promotes neuronal differentiation and inhibits neuroblast self-renewal. Dev Cell 10: 441-449.
28. Li Y., Maines JZ, Tastan OY, McKearin DM, Buszczak M. 2012. Mei-P26 regulates the maintenance of ovarian germline stem cells by promoting BMP signaling. Development 139: 1547-1556.
29. Li Y., Zhang Q, Carreira-Rosario A, Maines JZ, McKearin DM, Buszczak M. 2013. Mei-p26 cooperates with Bam, Bgcn and Sxl to promote early germline development in the Drosophila ovary. PLoS ONE 8: e58301.
30. Loedige I., Gaidatzis D, Sack R, Meister G, Filipowicz W. 2013. The mammalian TRIM-NHL protein TRIM71/LIN-41 is a repressor of mRNA function. Nucleic Acids Res 41: 518-532.
31. Luo X., Hsiao HH, Bubunenko M, Weber G, Court DL, Gottesman ME, Urlaub H, Wahl MC. 2008. Structural and functional analysis of the E. coli NusB-S10 transcription antitermination complex. Mol Cell 32: 791-802.
32. Muraro N. I, Weston AJ, Gerber AP, Luschnig S, Moffat KG, Baines R.A. 2008. Pumilio binds para mRNA and requires Nanos and Brat to regulate sodium current in Drosophila motoneurons. J Neurosci 28: 2099-2109.
33. Murata Y., Wharton RP. 1995. Binding of pumilio to maternal hunchback mRNA is required for posterior patterning in Drosophila embryos. Cell 80: 747-756.
34. Neumuller R. A, Betschinger J, Fischer A, Bushati N, Poernbacher I, Mechtler K., Cohen SM, Knoblich JA. 2008. Mei-P26 regulates microRNAs and cell growth in the Drosophila ovarian stem cell lineage. Nature 454: 241-245.
35. Nusslein-Volhard C, Frohnhofer HG, Lehmann R. 1987. Determination of anteroposterior polarity in Drosophila. Science 238: 1675-1681.
36. Reymond A., Meroni G, Fantozzi A, Merla G, Cairo S, Luzi L, Riganelli D., Zanaria E, Messali S, Cainarca S, et al. 2001. The tripartite motif family identifies cell compartments. EMBO J 20: 2140-2151.
37. Rybak A., Fuchs H, Hadian K, Smirnova L, Wulczyn EA, Michel G, Nitsch R, Krappmann D, Wulczyn FG. 2009. The let-7 target gene mouse lin-41 is a stem cell specific E3 ubiquitin ligase for the miRNA pathway protein Ago2. Nat Cell Biol 11: 1411-1420.
38. Sardiello M., Cairo S, Fontanella B, Ballabio A, Meroni G. 2008. Genomic analysis of the TRIM family reveals two groups of genes with distinct evolutionary properties. BMC Evol Biol 8: 225.
39. Schwamborn J. C, Berezikov E, Knoblich JA. 2009. The TRIMNHL protein TRIM32 activates microRNAs and prevents self-renewal in mouse neural progenitors. Cell 136: 913-925.
40. Scrima A., Konickova R, Czyzewski BK, Kawasaki Y, Jeffrey PD, Groisman R., Nakatani Y, Iwai S, Pavletich NP, Thoma NH. 2008. Structural basis of UV DNA-damage recognition by the DDB1-DDB2 complex. Cell 135: 1213-1223.
41. Shi W., Chen Y, Gan G, Wang D, Ren J, Wang Q, Xu Z, Xie W, Zhang Y.Q. 2013. Brain tumor regulates neuromuscular synapse growth and endocytosis in Drosophila by suppressing mad expression. J Neurosci 33: 12352-12363.
42. Slack F. J, Ruvkun G. 1998. A novel repeat domain that is often associated with RING finger and B-box motifs. Trends Biochem Sci 23: 474-475.
43. Slack F. J, Basson M, Liu Z, Ambros V, Horvitz HR, Ruvkun G. 2000. The lin-41 RBCC gene acts in the C. elegans heterochronic pathway between the let-7 regulatory RNA and the LIN-29 transcription factor. Mol Cell 5: 659-669.
44. Sonoda J., Wharton RP. 1999. Recruitment of Nanos to hunchback mRNA by Pumilio. Genes Dev 13: 2704-2712.
45. Sonoda J., Wharton RP. 2001. Drosophila brain tumor is a translational repressor. Genes Dev 15: 762-773.
46. Stirnimann C. U, Petsalaki E, Russell RB, Müller CW. 2010. WD40 proteins propel cellular networks. Trends Biochem Sci 35: 565-574.
47. Tautz D., 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.
48. Wang X., McLachlan J, Zamore PD, Hall TM. 2002. Modular recognition of RNA by a human pumilio-homology domain. Cell 110: 501-512.
49. Weidmann C. A, Goldstrohm AC. 2012. Drosophila Pumilio protein contains multiple autonomous repression domains that regulate mRNAs independently of Nanos and brain tumor. Mol Cell Biol 32: 527-540.
50. Wharton R. P, Struhl G. 1991. RNA regulatory elements mediate control of Drosophila body pattern by the posterior morphogen nanos. Cell 67: 955-967.
51. Worringer K. A, Rand TA, Hayashi Y, Sami S, Takahashi K, Tanabe K., Narita M, Srivastava D, Yamanaka S. 2014. The let-7/LIN-41 pathway regulates reprogramming to human induced pluripotent stem cells by controlling expression of prodifferentiation genes. Cell Stem Cell 14: 40-52.
52. Zamore P. D, Williamson JR, Lehmann R. 1997. The Pumilio protein binds RNA through a conserved domain that defines a new class of RNA-binding proteins. RNA 3: 1421-1433.
53. Zamore P. D, Bartel DP, Lehmann R, Williamson JR. 1999. The PUMILIO-RNA interaction: a single RNA-binding domain monomer recognizes a bipartite target sequence. Biochemistry 38: 596-604.
54. Zheng L., Baumann U, Reymond JL. 2004. An efficient one-step site-directed and site-saturation mutagenesis protocol. Nucleic Acids Res 32: e115.
55. Zillner K., Jerabek-Willemsen M, Duhr S, Braun D, Langst G, Baaske P. 2012. Microscale thermophoresis as a sensitive method to quantify protein: nucleic acid interactions in solution. Methods Mol Biol 815: 241-252.