Brain tumor is a sequence-specific RNA-binding protein that directs maternal mRNA clearance during the Drosophila maternal-to-zygotic transition

Genome Biology

Volumn 16, Issue 1, 2015, Pages

  Laver, John D ^a   Li, Xiao ^a   Ray, Debashish ^a   Cook, Kate B ^a   Hahn, Noah A ^a   Nabeel Shah, Syed ^a   Kekis, Mariana ^a   Luo, Hua ^a   Marsolais, Alexander J ^a   Fung, Karen YY ^a   Hughes, Timothy R ^a   Westwood, J Timothy ^b   Sidhu, Sachdev S ^a   Morris, Quaid ^a,b   Lipshitz, Howard D ^a   Smibert, Craig A ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; RNA BINDING PROTEIN; BRAT PROTEIN, DROSOPHILA; DNA BINDING PROTEIN; DROSOPHILA PROTEIN; PUMILIO PROTEIN, DROSOPHILA; TRANSCRIPTION FACTOR; ZELDA PROTEIN, DROSOPHILA;

ANIMAL TISSUE; ARTICLE; BINDING SITE; BIOLOGICAL PHENOMENA AND FUNCTIONS CONCERNING ORGAN SYSTEMS; BRAIN TUMOR; CONTROLLED STUDY; DROSOPHILA; EMBRYO; FEMALE; GENE IDENTIFICATION; GENETIC TRANSCRIPTION; IN VITRO STUDY; IN VIVO STUDY; MATERNAL TO ZYGOTIC TRANSITION; NONHUMAN; RNA SEQUENCE; RNA STABILITY; RNA STRUCTURE; RNA TRANSLATION; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS; ANIMAL; BRAIN NEOPLASMS; EMBRYOLOGY; EPIGENETIC REPRESSION; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION STUDY; GENETICS; METABOLISM; MUTATION; TISSUE CULTURE TECHNIQUE;

METAZOA;

ANIMALS; BINDING SITES; BRAIN NEOPLASMS; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; EPIGENETIC REPRESSION; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC ASSOCIATION STUDIES; MUTATION; RNA, MESSENGER, STORED; RNA-BINDING PROTEINS; TISSUE CULTURE TECHNIQUES; TRANSCRIPTION FACTORS;

EID: 84939141051     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/s13059-015-0659-4     Document Type: Article

References (75)

1. Tadros W, Lipshitz HD. The maternal-to-zygotic transition: a play in two acts. Development. 2009;136:3033-42.
2. Walser CB, Lipshitz HD. Transcript clearance during the maternal-to-zygotic transition. Curr Opin Genet Dev. 2011;21:431-43.
3. Sonoda J, Wharton RP. Drosophila Brain Tumor is a translational repressor. Genes Dev. 2001;15:762-73.
4. Lehmann R, Nusslein-Volhard C. Involvement of the pumilio gene in the transport of an abdominal signal in the Drosophila embryo. Nature. 1987;329:167-70.
5. Murata Y, Wharton RP. Binding of pumilio to maternal hunchback mRNA is required for posterior patterning in Drosophila embryos. Cell. 1995;80:747-56.
6. Irish V, Lehmann R, Akam M. The Drosophila posterior-group gene nanos functions by repressing hunchback activity. Nature. 1989;338:646-8.
7. Hulskamp M, Schroder C, Pfeifle C, Jackle H, Tautz D. Posterior segmentation of the Drosophila embryo in the absence of a maternal posterior organizer gene. Nature. 1989;338:629-32.
8. Struhl G. Differing strategies for organizing anterior and posterior body pattern in Drosophila embryos. Nature. 1989;338:741-4.
9. Petrera F, Meroni G. TRIM proteins in development. Adv Exp Med Biol. 2012;770:131-41.
10. Loedige I, Filipowicz W. TRIM-NHL proteins take on miRNA regulation. Cell. 2009;136:818-20.
11. Worringer KA, Rand TA, Hayashi Y, Sami S, Takahashi K, Tanabe K, et al. The let-7/LIN-41 pathway regulates reprogramming to human induced pluripotent stem cells by controlling expression of prodifferentiation genes. Cell Stem Cell. 2014;14:40-52.
12. Loedige I, Gaidatzis D, Sack R, Meister G, Filipowicz W. The mammalian TRIM-NHL protein TRIM71/LIN-41 is a repressor of mRNA function. Nucleic Acids Res. 2013;41:518-32.
13. Wharton RP, Struhl G. RNA regulatory elements mediate control of Drosophila body pattern by the posterior morphogen nanos. Cell. 1991;67:955-67.
14. Sonoda J, Wharton RP. Recruitment of Nanos to hunchback mRNA by Pumilio. Genes Dev. 1999;13:2704-12.
15. Zamore PD, Williamson JR, Lehmann R. The Pumilio protein binds RNA through a conserved domain that defines a new class of RNA-binding proteins. RNA. 1997;3:1421-33.
16. Wharton RP, Sonoda J, Lee T, Patterson M, Murata Y. The Pumilio RNA-binding domain is also a translational regulator. Mol Cell. 1998;1:863-72.
17. Loedige I, Stotz M, Qamar S, Kramer K, Hennig J, Schubert T, et al. The NHL domain of BRAT is an RNA-binding domain that directly contacts the hunchback mRNA for regulation. Genes Dev. 2014;28:749-64.
18. Castello A, Fischer B, Eichelbaum K, Horos R, Beckmann BM, Strein C, et al. Insights into RNA biology from an atlas of mammalian mRNA-binding proteins. Cell. 2012;149:1393-406.
19. Kwon SC, Yi H, Eichelbaum K, Fohr S, Fischer B, You KT, et al. The RNA-binding protein repertoire of embryonic stem cells. Nat Struct Mol Biol. 2013;20:1122-30.
20. Muraro NI, Weston AJ, Gerber AP, Luschnig S, Moffat KG, Baines RA. Pumilio binds para mRNA and requires Nanos and Brat to regulate sodium current in Drosophila motoneurons. J Neurosci. 2008;28:2099-109.
21. Olesnicky EC, Bhogal B, Gavis ER. Combinatorial use of translational co-factors for cell type-specific regulation during neuronal morphogenesis in Drosophila. Dev Biol. 2012;365:208-18.
22. Harris RE, Pargett M, Sutcliffe C, Umulis D, Ashe HL. Brat promotes stem cell differentiation via control of a bistable switch that restricts BMP signaling. Dev Cell. 2011;20:72-83.
23. Asaoka-Taguchi M, Yamada M, Nakamura A, Hanyu K, Kobayashi S. Maternal Pumilio acts together with Nanos in germline development in Drosophila embryos. Nat Cell Biol. 1999;1:431-7.
24. Kadyrova LY, Habara Y, Lee TH, Wharton RP. Translational control of maternal Cyclin B mRNA by Nanos in the Drosophila germline. Development. 2007;134:1519-27.
25. Weidmann CA, Goldstrohm AC. Drosophila Pumilio protein contains multiple autonomous repression domains that regulate mRNAs independently of Nanos and brain tumor. Mol Cell Biol. 2012;32:527-40.
26. Bowman SK, Rolland V, Betschinger J, Kinsey KA, Emery G, Knoblich JA. The tumor suppressors Brat and Numb regulate transit-amplifying neuroblast lineages in Drosophila. Dev Cell. 2008;14:535-46.
27. Arama E, Dickman D, Kimchie Z, Shearn A, Lev Z. Mutations in the beta-propeller domain of the Drosophila brain tumor (brat) protein induce neoplasm in the larval brain. Oncogene. 2000;19:3706-16.
28. Lee CY, Wilkinson BD, Siegrist SE, Wharton RP, Doe CQ. Brat is a Miranda cargo protein that promotes neuronal differentiation and inhibits neuroblast self-renewal. Dev Cell. 2006;10:441-9.
29. Bello B, Reichert H, Hirth F. The brain tumor gene negatively regulates neural progenitor cell proliferation in the larval central brain of Drosophila. Development. 2006;133:2639-48.
30. Betschinger J, Mechtler K, Knoblich JA. Asymmetric segregation of the tumor suppressor brat regulates self-renewal in Drosophila neural stem cells. Cell. 2006;124:1241-53.
31. Woodhouse E, Hersperger E, Shearn A. Growth, metastasis, and invasiveness of Drosophila tumors caused by mutations in specific tumor suppressor genes. Dev Genes Evol. 1998;207:542-50.
32. Laver JD, Ancevicius K, Sollazzo P, Westwood JT, Sidhu SS, Lipshitz HD, et al. Synthetic antibodies as tools to probe RNA-binding protein function. Mol Biosyst. 2012;8:1650-7.
33. Laver JD, Li X, Ancevicius K, Westwood JT, Smibert CA, Morris QD, et al. Genome-wide analysis of Staufen-associated mRNAs identifies secondary structures that confer target specificity. Nucleic Acids Res. 2013;41:9438-60.
34. Gamberi C, Peterson DS, He L, Gottlieb E. An anterior function for the Drosophila posterior determinant Pumilio. Development. 2002;129:2699-710.
35. Vardy L, Orr-Weaver TL. The Drosophila PNG kinase complex regulates the translation of cyclin B. Dev Cell. 2007;12:157-66.
36. Shi W, Chen Y, Gan G, Wang D, Ren J, Wang Q, et al. Brain tumor regulates neuromuscular synapse growth and endocytosis in Drosophila by suppressing mad expression. J Neurosci. 2013;33:12352-63.
37. Gerber AP, Luschnig S, Krasnow MA, Brown PO, Herschlag D. Genome-wide identification of mRNAs associated with the translational regulator PUMILIO in Drosophila melanogaster. Proc Natl Acad Sci U S A. 2006;103:4487-92.
38. Li X, Quon G, Lipshitz HD, Morris Q. Predicting in vivo binding sites of RNA-binding proteins using mRNA secondary structure. RNA. 2010;16:1096-107.
39. Ray D, Kazan H, Cook KB, Weirauch MT, Najafabadi HS, Li X, et al. A compendium of RNA-binding motifs for decoding gene regulation. Nature. 2013;499:172-7.
40. Miller MA, Olivas WM. Roles of Puf proteins in mRNA degradation and translation. Wiley Interdiscip Rev RNA. 2011;2:471-92.
41. Ray D, Kazan H, Chan ET, Pena Castillo L, Chaudhry S, Talukder S, et al. Rapid and systematic analysis of the RNA recognition specificities of RNA-binding proteins. Nat Biotechnol. 2009;27:667-70.
42. da Huang W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4:44-57.
43. da Huang W, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 2009;37:1-13.
44. Chen L, Dumelie JG, Li X, Cheng MH, Yang Z, Laver JD, et al. Global regulation of mRNA translation and stability in the early Drosophila embryo by the Smaug RNA-binding protein. Genome Biol. 2014;15:R4.
45. Barker DD, Wang C, Moore J, Dickinson LK, Lehmann R. Pumilio is essential for function but not for distribution of the Drosophila abdominal determinant Nanos. Genes Dev. 1992;6:2312-26.
46. Forbes A, Lehmann R. Nanos and Pumilio have critical roles in the development and function of Drosophila germline stem cells. Development. 1998;125:679-90.
47. Macdonald PM. The Drosophila pumilio gene: an unusually long transcription unit and an unusual protein. Development. 1992;114:221-32.
48. Siddiqui NU, Li X, Luo H, Karaiskakis A, Hou H, Kislinger T, et al. Genome-wide analysis of the maternal-to-zygotic transition in Drosophila primordial germ cells. Genome Biol. 2012;13:R11.
49. Ye B, Petritsch C, Clark IE, Gavis ER, Jan LY, Jan YN. Nanos and Pumilio are essential for dendrite morphogenesis in Drosophila peripheral neurons. Curr Biol. 2004;14:314-21.
50. Parisi M, Lin H. The Drosophila pumilio gene encodes two functional protein isoforms that play multiple roles in germline development, gonadogenesis, oogenesis and embryogenesis. Genetics. 1999;153:235-50.
51. Kim SY, Kim JY, Malik S, Son W, Kwon KS, Kim C. Negative regulation of EGFR/MAPK pathway by Pumilio in Drosophila melanogaster. PLoS One. 2012;7:e34016.
52. Harrison MM, Li XY, Kaplan T, Botchan MR, Eisen MB. Zelda binding in the early Drosophila melanogaster embryo marks regions subsequently activated at the maternal-to-zygotic transition. PLoS Genet. 2011;7:e1002266.
53. Liang HL, Nien CY, Liu HY, Metzstein MM, Kirov N, Rushlow C. The zinc-finger protein Zelda is a key activator of the early zygotic genome in Drosophila. Nature. 2008;456:400-3.
54. Xu Z, Chen H, Ling J, Yu D, Struffi P, Small S. Impacts of the ubiquitous factor Zelda on Bicoid-dependent DNA binding and transcription in Drosophila. Genes Dev. 2014;28:608-21.
55. Lecuyer E, Yoshida H, Parthasarathy N, Alm C, Babak T, Cerovina T, et al. Global analysis of mRNA localization reveals a prominent role in organizing cellular architecture and function. Cell. 2007;131:174-87.
56. Fly-FISH: A database of Drosophila embryo mRNA localization patterns. [ http://fly-fish.ccbr.utoronto.ca/ ].
57. Qin X, Ahn S, Speed TP, Rubin GM. Global analyses of mRNA translational control during early Drosophila embryogenesis. Genome Biol. 2007;8:R63.
58. De Renzis S, Elemento O, Tavazoie S, Wieschaus EF. Unmasking activation of the zygotic genome using chromosomal deletions in the Drosophila embryo. PLoS Biol. 2007;5:e117.
59. Thomsen S, Anders S, Janga SC, Huber W, Alonso CR. Genome-wide analysis of mRNA decay patterns during early Drosophila development. Genome Biol. 2010;11:R93.
60. Tadros W, Goldman AL, Babak T, Menzies F, Vardy L, Orr-Weaver T, et al. SMAUG is a major regulator of maternal mRNA destabilization in Drosophila and its translation is activated by the PAN GU kinase. Dev Cell. 2007;12:143-55.
61. Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, et al. TM4: a free, open-source system for microarray data management and analysis. Biotechniques. 2003;34:374-8.
62. Saeed AI, Bhagabati NK, Braisted JC, Liang W, Sharov V, Howe EA, et al. TM4 microarray software suite. Methods Enzymol. 2006;411:134-93.
63. Foo SM, Sun Y, Lim B, Ziukaite R, O'Brien K, Nien CY, et al. Zelda potentiates morphogen activity by increasing chromatin accessibility. Curr Biol. 2014;24:1341-6.
64. ten Bosch JR, Benavides JA, Cline TW. The TAGteam DNA motif controls the timing of Drosophila pre-blastoderm transcription. Development. 2006;133:1967-77.
65. Bushati N, Stark A, Brennecke J, Cohen SM. Temporal reciprocity of miRNAs and their targets during the maternal-to-zygotic transition in Drosophila. Curr Biol. 2008;18:501-6.
66. Benoit B, He CH, Zhang F, Votruba SM, Tadros W, Westwood JT, et al. An essential role for the RNA-binding protein Smaug during the Drosophila maternal-to-zygotic transition. Development. 2009;136:923-32.
67. Temme C, Zhang L, Kremmer E, Ihling C, Chartier A, Sinz A, et al. Subunits of the Drosophila CCR4-NOT complex and their roles in mRNA deadenylation. RNA. 2010;16:1356-70.
68. Semotok JL, Cooperstock RL, Pinder BD, Vari HK, Lipshitz HD, Smibert CA. Smaug recruits the CCR4/POP2/NOT deadenylase complex to trigger maternal transcript localization in the early Drosophila embryo. Curr Biol. 2005;15:284-94.
69. Schupbach T, Wieschaus E. Female sterile mutations on the second chromosome of Drosophila melanogaster, II. Mutations blocking oogenesis or altering egg morphology. Genetics. 1991;129:1119-36.
70. Stathakis DG, Pentz ES, Freeman ME, Kullman J, Hankins GR, Pearlson NJ, et al. The genetic and molecular organization of the Dopa decarboxylase gene cluster of Drosophila melanogaster. Genetics. 1995;141:629-55.
71. Persson H, Ye W, Wernimont A, Adams JJ, Koide A, Koide S, et al. CDR-H3 diversity is not required for antigen recognition by synthetic antibodies. J Mol Biol. 2013;425:803-11.
72. Fellouse FA, Sidhu SS. Making antibodies in bacteria. In: Howard GC, Kaser MR, editors. Making and Using Antibodies. Boca Raton, FL: CRC Press; 2007. p. 157-80.
73. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A. 2001;98:5116-21.
74. Bunch TA, Grinblat Y, Goldstein LS. Characterization and use of the Drosophila metallothionein promoter in cultured Drosophila melanogaster cells. Nucleic Acids Res. 1988;16:1043-61.
75. BioMart. [http://www.biomart.org/]