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The LOTUS domain is a conserved DEAD-box RNA helicase regulator essential for the recruitment of Vasa to the germ plasm and nuage.

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Jeske M, Müller CW, Ephrussi A
OpenAccess logo Genes Dev 31 939-952 (2017)
Cited: 39 times
EuropePMC logo PMID: 28536148

Abstract

DEAD-box RNA helicases play important roles in a wide range of metabolic processes. Regulatory proteins can stimulate or block the activity of DEAD-box helicases. Here, we show that LOTUS (Limkain, Oskar, and Tudor containing proteins 5 and 7) domains present in the germline proteins Oskar, TDRD5 (Tudor domain-containing 5), and TDRD7 bind and stimulate the germline-specific DEAD-box RNA helicase Vasa. Our crystal structure of the LOTUS domain of Oskar in complex with the C-terminal RecA-like domain of Vasa reveals that the LOTUS domain occupies a surface on a DEAD-box helicase not implicated previously in the regulation of the enzyme's activity. We show that, in vivo, the localization of Drosophila Vasa to the nuage and germ plasm depends on its interaction with LOTUS domain proteins. The binding and stimulation of Vasa DEAD-box helicases by LOTUS domains are widely conserved.

Articles - 5nt7 mentioned but not cited (4)

  1. The LOTUS domain is a conserved DEAD-box RNA helicase regulator essential for the recruitment of Vasa to the germ plasm and nuage. Jeske M, Müller CW, Ephrussi A. Genes Dev 31 939-952 (2017)
  2. Novel LOTUS-domain proteins are organizational hubs that recruit C. elegans Vasa to germ granules. Cipriani PG, Bay O, Zinno J, Gutwein M, Gan HH, Mayya VK, Chung G, Chen JX, Fahs H, Guan Y, Duchaine TF, Selbach M, Piano F, Gunsalus KC. Elife 10 e60833 (2021)
  3. The Caenorhabditis elegans TDRD5/7-like protein, LOTR-1, interacts with the helicase ZNFX-1 to balance epigenetic signals in the germline. Marnik EA, Almeida MV, Cipriani PG, Chung G, Caspani E, Karaulanov E, Gan HH, Zinno J, Isolehto IJ, Kielisch F, Butter F, Sharp CS, Flanagan RM, Bonnet FX, Piano F, Ketting RF, Gunsalus KC, Updike DL. PLoS Genet 18 e1010245 (2022)
  4. Evolution of a Cytoplasmic Determinant: Evidence for the Biochemical Basis of Functional Evolution of the Novel Germ Line Regulator Oskar. Blondel L, Besse S, Rivard EL, Ylla G, Extavour CG. Mol Biol Evol 38 5491-5513 (2021)


Reviews citing this publication (7)

  1. Germ granules in Drosophila. Trcek T, Lehmann R. Traffic 20 650-660 (2019)
  2. RNA-binding proteins and post-transcriptional regulation in lens biology and cataract: Mediating spatiotemporal expression of key factors that control the cell cycle, transcription, cytoskeleton and transparency. Lachke SA. Exp Eye Res 214 108889 (2022)
  3. Building RNA-protein germ granules: insights from the multifaceted functions of DEAD-box helicase Vasa/Ddx4 in germline development. Xu C, Cao Y, Bao J. Cell Mol Life Sci 79 4 (2021)
  4. Patterning the Drosophila embryo: A paradigm for RNA-based developmental genetic regulation. Lasko P. Wiley Interdiscip Rev RNA 11 e1610 (2020)
  5. Structural and functional organization of germ plasm condensates. Chiappetta A, Liao J, Tian S, Trcek T. Biochem J 479 2477-2495 (2022)
  6. Evolution of germ plasm assembly and function among the insects. Kemph A, Lynch JA. Curr Opin Insect Sci 50 100883 (2022)
  7. RNA Helicase Vasa as a Multifunctional Conservative Regulator of Gametogenesis in Eukaryotes. Adashev VE, Kotov AA, Olenina LV. Curr Issues Mol Biol 45 5677-5705 (2023)

Articles citing this publication (28)

  1. Phase transitioned nuclear Oskar promotes cell division of Drosophila primordial germ cells. Kistler KE, Trcek T, Hurd TR, Chen R, Liang FX, Sall J, Kato M, Lehmann R. Elife 7 e37949 (2018)
  2. Stochastic Seeding Coupled with mRNA Self-Recruitment Generates Heterogeneous Drosophila Germ Granules. Niepielko MG, Eagle WVI, Gavis ER. Curr Biol 28 1872-1881.e3 (2018)
  3. TDRD5 binds piRNA precursors and selectively enhances pachytene piRNA processing in mice. Ding D, Liu J, Midic U, Wu Y, Dong K, Melnick A, Latham KE, Chen C. Nat Commun 9 127 (2018)
  4. The Tudor-domain protein TDRD7, mutated in congenital cataract, controls the heat shock protein HSPB1 (HSP27) and lens fiber cell morphology. Barnum CE, Al Saai S, Patel SD, Cheng C, Anand D, Xu X, Dash S, Siddam AD, Glazewski L, Paglione E, Polson SW, Chuma S, Mason RW, Wei S, Batish M, Fowler VM, Lachke SA. Hum Mol Genet 29 2076-2097 (2020)
  5. Ribonuclease activity of MARF1 controls oocyte RNA homeostasis and genome integrity in mice. Yao Q, Cao G, Li M, Wu B, Zhang X, Zhang T, Guo J, Yin H, Shi L, Chen J, Yu X, Zheng L, Ma J, Su YQ. Proc Natl Acad Sci U S A 115 11250-11255 (2018)
  6. Aggregation, segregation, and dispersal of homotypic germ plasm RNPs in the early zebrafish embryo. Eno C, Hansen CL, Pelegri F. Dev Dyn 248 306-318 (2019)
  7. Functional equivalence of germ plasm organizers. Krishnakumar P, Riemer S, Perera R, Lingner T, Goloborodko A, Khalifa H, Bontems F, Kaufholz F, El-Brolosy MA, Dosch R. PLoS Genet 14 e1007696 (2018)
  8. LOTUS domain protein MARF1 binds CCR4-NOT deadenylase complex to post-transcriptionally regulate gene expression in oocytes. Zhu L, Kandasamy SK, Liao SE, Fukunaga R. Nat Commun 9 4031 (2018)
  9. Bacterial contribution to genesis of the novel germ line determinant oskar. Blondel L, Jones TE, Extavour CG. Elife 9 e45539 (2020)
  10. LOTUS domain is a novel class of G-rich and G-quadruplex RNA binding domain. Ding D, Wei C, Dong K, Liu J, Stanton A, Xu C, Min J, Hu J, Chen C. Nucleic Acids Res 48 9262-9272 (2020)
  11. Comparative Proteomics Reveal Me31B's Interactome Dynamics, Expression Regulation, and Assembly Mechanism into Germ Granules during Drosophila Germline Development. McCambridge A, Solanki D, Olchawa N, Govani N, Trinidad JC, Gao M. Sci Rep 10 564 (2020)
  12. Germ Cell Lineage Homeostasis in Drosophila Requires the Vasa RNA Helicase. Durdevic Z, Ephrussi A. Genetics 213 911-922 (2019)
  13. Human MARF1 is an endoribonuclease that interacts with the DCP1:2 decapping complex and degrades target mRNAs. Nishimura T, Fakim H, Brandmann T, Youn JY, Gingras AC, Jinek M, Fabian MR. Nucleic Acids Res 46 12008-12021 (2018)
  14. Genome-Wide Analysis of Differentially Expressed miRNAs and Their Associated Regulatory Networks in Lenses Deficient for the Congenital Cataract-Linked Tudor Domain Containing Protein TDRD7. Anand D, Al Saai S, Shrestha SK, Barnum CE, Chuma S, Lachke SA. Front Cell Dev Biol 9 615761 (2021)
  15. Letter An in vivo proteomic analysis of the Me31B interactome in Drosophila germ granules. DeHaan H, McCambridge A, Armstrong B, Cruse C, Solanki D, Trinidad JC, Arkov AL, Gao M. FEBS Lett 591 3536-3547 (2017)
  16. Phylogenetic Analysis of the Dengue Virus Strains Causing the 2019 Dengue Fever Outbreak in Hainan, China. Du J, Zhang L, Hu X, Peng R, Wang G, Huang Y, Wang W, Wu K, Wang Q, Su H, Yang F, Zhang Y, Tang C, Cui X, Niu L, Lu G, Xiao M, Du Y, Yin F. Virol Sin 36 636-643 (2021)
  17. A non-canonical role for the EDC4 decapping factor in regulating MARF1-mediated mRNA decay. Brothers WR, Hebert S, Kleinman CL, Fabian MR. Elife 9 e54995 (2020)
  18. Drosophila MARF1 ensures proper oocyte maturation by regulating nanos expression. Kawaguchi S, Ueki M, Kai T. PLoS One 15 e0231114 (2020)
  19. Oogenesis of Hematophagous Midge Forcipomyia taiwana (Diptera: Ceratopogonidae) and Nuage Localization of Vasa in Germline Cells. Wang SC, Ching YH, Krishnaraj P, Chen GY, Radhakrishnan AS, Lee HM, Tu WC, Lin MD. Insects 11 E106 (2020)
  20. Proximity labeling identifies LOTUS domain proteins that promote the formation of perinuclear germ granules in C. elegans. Price IF, Hertz HL, Pastore B, Wagner J, Tang W. Elife 10 e72276 (2021)
  21. Receptor-mediated yolk uptake is required for oskar mRNA localization and cortical anchorage of germ plasm components in the Drosophila oocyte. Tanaka T, Tani N, Nakamura A. PLoS Biol 19 e3001183 (2021)
  22. Proteins rather than mRNAs regulate nucleation and persistence of Oskar germ granules in Drosophila. Curnutte HA, Lan X, Sargen M, Ao Ieong SM, Campbell D, Kim H, Liao Y, Lazar SB, Trcek T. Cell Rep 42 112723 (2023)
  23. Bucky Ball Is a Novel Zebrafish Vasa ATPase Activator. Perera RP, Shaikhqasem A, Rostam N, Dickmanns A, Ficner R, Tittmann K, Dosch R. Biomolecules 11 1507 (2021)
  24. Early germline differentiation in bivalves: TDRD7 as a candidate investigational unit for Ruditapes philippinarum germ granule assembly. Filanti B, Piccinini G, Bettini S, Lazzari M, Franceschini V, Maurizii MG, Milani L. Histochem Cell Biol 156 19-34 (2021)
  25. Highly Overexpressed AtC3H18 Impairs Microgametogenesis via Promoting the Continuous Assembly of mRNP Granules. Xu L, Liu T, Xiong X, Shen X, Huang L, Yu Y, Cao J. Front Plant Sci 13 932793 (2022)
  26. TDRD5 Is Required for Spermatogenesis and Oogenesis in Locusta migratoria. Deng S, Wang J, Ma E, Zhang J, Xing S. Insects 13 227 (2022)
  27. Structural basis for binding of Drosophila Smaug to the GPCR Smoothened and to the germline inducer Oskar. Kubíková J, Ubartaitė G, Metz J, Jeske M. Proc Natl Acad Sci U S A 120 e2304385120 (2023)
  28. Tejas functions as a core component in nuage assembly and precursor processing in Drosophila piRNA biogenesis. Lin Y, Suyama R, Kawaguchi S, Iki T, Kai T. J Cell Biol 222 e202303125 (2023)


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