title: Independent and coordinate trafficking of single Drosophila germ plasm mRNAs.
abstract: Messenger RNA localization is a conserved mechanism for spatial control of protein synthesis, with key roles in generating cellular and developmental asymmetry. Whereas different transcripts may be targeted to the same subcellular domain, the extent to which their localization is coordinated is unclear. Using quantitative single-molecule imaging, we analysed the assembly of Drosophila germ plasm mRNA granules inherited by nascent germ cells. We find that the germ-cell-destined transcripts nanos, cyclin B and polar granule component travel within the oocyte as ribonucleoprotein particles containing single mRNA molecules but co-assemble into multi-copy heterogeneous granules selectively at the posterior of the oocyte. The stoichiometry and dynamics of assembly indicate a defined stepwise sequence. Our data suggest that co-packaging of these transcripts ensures their effective segregation to germ cells. In contrast, compartmentalization of the germline determinant oskar mRNA into different granules limits its entry into germ cells. This exclusion is required for proper germline development.
authors.affiliation: 1] Department of Molecular Biology, Princeton University, Princeton, New Jersey 08544, USA [2] Howard Hughes Medical Institute, Princeton University, Princeton, New Jersey 08544, USA.
authors.forename: Shawn C
authors.initials: SC
authors.lastname: Little
authors.affiliation: Department of Molecular Biology, Princeton University, Princeton, New Jersey 08544, USA.
authors.forename: Kristina S
authors.initials: KS
authors.lastname: Sinsimer
authors.affiliation: Department of Molecular Biology, Princeton University, Princeton, New Jersey 08544, USA.
authors.forename: Jack J
authors.initials: JJ
authors.lastname: Lee
authors.affiliation: 1] Department of Molecular Biology, Princeton University, Princeton, New Jersey 08544, USA [2] Howard Hughes Medical Institute, Princeton University, Princeton, New Jersey 08544, USA.
authors.forename: Eric F
authors.initials: EF
authors.lastname: Wieschaus
authors.affiliation: Department of Molecular Biology, Princeton University, Princeton, New Jersey 08544, USA.
authors.forename: Elizabeth R
authors.initials: ER
authors.lastname: Gavis
mesh_terms: D021581:Active Transport, Cell Nucleus; D000818:Animals; D002467:Cell Nucleus / Q000378:metabolism; D019926:Cyclin B / Q000235:genetics; D003594:Cytoplasmic Granules / Q000378:metabolism; D029721:Drosophila Proteins / Q000235:genetics*; D004331:Drosophila melanogaster / Q000166:cytology / Q000235:genetics* / Q000378:metabolism*; D018715:Microscopy, Video; D009865:Oocytes / Q000378:metabolism*; D042925:Positive Transcriptional Elongation Factor B / Q000235:genetics; D012333:RNA, Messenger / Q000235:genetics* / Q000378:metabolism*; D016601:RNA-Binding Proteins / Q000235:genetics; D014158:Transcription, Genetic
chemical_list: C503698:CycB protein, Drosophila; D019926:Cyclin B; D029721:Drosophila Proteins; D012333:RNA, Messenger; D016601:RNA-Binding Proteins; C091675:osk protein, Drosophila; C527201:pgc protein, Drosophila; C070574:nos protein, Drosophila; D042925:Positive Transcriptional Elongation Factor B
references.citation: EMBO J. 2000 Mar 15;19(6):1366-77
references.pmid: 10716936
references.citation: Int Rev Cytol. 2001;203:187-213
references.pmid: 11131516
references.citation: Development. 2002 Aug;129(15):3705-14
references.pmid: 12117819
references.citation: Curr Biol. 2003 Jul 15;13(14):1159-68
references.pmid: 12867026
references.citation: Development. 2003 Sep;130(17):4201-15
references.pmid: 12874138
references.citation: Development. 1992 Aug;115(4):989-97
references.pmid: 1451670
references.citation: Nature. 2004 Apr 29;428(6986):959-63
references.pmid: 15118729
references.citation: Cell. 1992 Sep 4;70(5):849-59
references.pmid: 1516136
references.citation: Development. 2004 Sep;131(17):4167-78
references.pmid: 15280213
references.citation: Dev Biol. 2005 Jun 1;282(1):207-17
references.pmid: 15936341
references.citation: Nature. 1992 Jul 30;358(6385):387-92
references.pmid: 1641021
references.citation: Cell. 2006 Feb 10;124(3):521-33
references.pmid: 16469699
references.citation: Dev Cell. 2006 May;10(5):601-13
references.pmid: 16678775
references.citation: Development. 2007 Feb;134(4):703-12
references.pmid: 17215303
references.citation: Differentiation. 2007 Mar;75(3):246-55
references.pmid: 17359300
references.citation: Cell. 2007 Oct 5;131(1):174-87
references.pmid: 17923096
references.citation: Cell. 2008 Feb 22;132(4):559-62
references.pmid: 18295574
references.citation: Curr Biol. 2008 May 20;18(10):745-750
references.pmid: 18472422
references.citation: Traffic. 2008 Aug;9(8):1256-67
references.pmid: 18485054
references.citation: Cell. 2008 Sep 5;134(5):843-53
references.pmid: 18775316
references.citation: Nat Methods. 2008 Oct;5(10):877-9
references.pmid: 18806792
references.citation: Development. 2008 Dec;135(23):3817-27
references.pmid: 18997110
references.citation: Cell. 1991 Aug 23;66(4):637-47
references.pmid: 1908748
references.citation: Curr Biol. 2009 Jan 13;19(1):72-7
references.pmid: 19110432
references.citation: Genes Dev. 2009 Jan 15;23(2):195-207
references.pmid: 19131435
references.citation: Development. 1991 Jul;112(3):679-91
references.pmid: 1935684
references.citation: Science. 2009 Jun 26;324(5935):1729-32
references.pmid: 19460965
references.citation: Development. 2009 Aug;136(15):2493-503
references.pmid: 19592573
references.citation: J Neurosci. 2010 Mar 17;30(11):4160-70
references.pmid: 20237286
references.citation: J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2010 May;196(5):321-34
references.pmid: 20237785
references.citation: Nat Protoc. 2010 Apr;5(4):678-87
references.pmid: 20360763
references.citation: Cell. 1991 Jul 12;66(1):37-50
references.pmid: 2070417
references.citation: Curr Biol. 2011 Mar 22;21(6):439-48
references.pmid: 21376599
references.citation: PLoS Biol. 2011 Mar;9(3):e1000596
references.pmid: 21390295
references.citation: Development. 2011 Aug;138(16):3431-40
references.pmid: 21752933
references.citation: RNA. 2011 Dec;17(12):2049-57
references.pmid: 22028360
references.citation: Curr Opin Cell Biol. 2012 Apr;24(2):202-10
references.pmid: 22278045
references.citation: Nat Cell Biol. 2012 Feb 26;14(4):416-23
references.pmid: 22366687
references.citation: Proc Natl Acad Sci U S A. 2012 Mar 20;109(12):4645-50
references.pmid: 22392993
references.citation: Nat Struct Mol Biol. 2012 Mar 18;19(4):441-9
references.pmid: 22426546
references.citation: Curr Opin Cell Biol. 2013 Feb;25(1):99-106
references.pmid: 23200723
references.citation: Cell. 2013 Aug 15;154(4):789-800
references.pmid: 23953111
references.citation: Cell Rep. 2013 Dec 12;5(5):1169-77
references.pmid: 24290763
references.citation: Curr Biol. 2014 Jun 2;24(11):1283-8
references.pmid: 24856210
references.citation: Roux Arch Dev Biol. 1986 Jul;195(5):302-317
references.pmid: 28306055
references.citation: J Theor Biol. 1966 Nov;12(2):276-90
references.pmid: 5972197
references.citation: Dev Dyn. 1994 Feb;199(2):103-15
references.pmid: 7515724
references.citation: Development. 1995 Sep;121(9):2737-46
references.pmid: 7555702
references.citation: Dev Biol. 1996 May 25;176(1):36-50
references.pmid: 8654893
references.citation: Science. 1996 Dec 20;274(5295):2075-9
references.pmid: 8953037
references.citation: Curr Biol. 1997 May 1;7(5):326-37
references.pmid: 9115398
references.citation: Development. 1999 Feb;126(4):659-69
references.pmid: 9895314