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PMID: 21768607 Published · epublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Review

RNA granules in germ cells.

Cold Spring Harbor perspectives in biology ·Vol. 3 ·No. 12 ·2011-12-01

Voronina E, Seydoux G, Sassone-Corsi P, Nagamori I

Abstract

"Germ granules" are cytoplasmic, nonmembrane-bound organelles unique to germline. Germ granules share components with the P bodies and stress granules of somatic cells, but also contain proteins and RNAs uniquely required for germ cell development. In this review, we focus on recent advances in our understanding of germ granule assembly, dynamics, and function. One hypothesis is that germ granules operate as hubs for the posttranscriptional control of gene expression, a function at the core of the germ cell differentiation program.

MeSH Terms
Animals Caenorhabditis elegans/cytology,genetics,ultrastructure Cell Differentiation Chromatin/metabolism Cytoplasmic Granules/genetics,physiology,ultrastructure Drosophila/cytology,genetics,ultrastructure Germ Cells/ultrastructure Mitosis Protein Structure, Tertiary RNA/metabolism,physiology RNA Stability
Chemicals
Chromatin RNA
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Voronina Ekaterina
Department of Molecular Biology and Genetics and Howard Hughes Medical Institute, Center for Cell Dynamics, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA. evoronina@jhmi.edu
Seydoux Geraldine
Sassone-Corsi Paolo
Nagamori Ippei
References (256)
256 references, click to expand
  1. Mitochondrial small ribosomal RNA is present on polar granules in early cleavage embryos of Drosophila melanogaster.
    Dev Growth Differ. 1999 Aug;41(4):495-502 PMID: 10466937
  2. Unique germ-line organelle, nuage, functions to repress selfish genetic elements in Drosophila melanogaster.
    Proc Natl Acad Sci U S A. 2007 Apr 17;104(16):6714-9 PMID: 17428915
  3. Human Dcp2: a catalytically active mRNA decapping enzyme located in specific cytoplasmic structures.
    EMBO J. 2002 Dec 16;21(24):6915-24 PMID: 12486012
  4. Potential structural role of non-coding and coding RNAs in the organization of the cytoskeleton at the vegetal cortex of Xenopus oocytes.
    Development. 2005 Aug;132(15):3445-57 PMID: 16000384
  5. NANOS3 function in human germ cell development.
    Hum Mol Genet. 2011 Jun 1;20(11):2238-50 PMID: 21421998
  6. Expression and intracellular localization of mouse Vasa-homologue protein during germ cell development.
    Mech Dev. 2000 May;93(1-2):139-49 PMID: 10781947
  7. The kinesin KIF17b and RNA-binding protein TB-RBP transport specific cAMP-responsive element modulator-regulated mRNAs in male germ cells.
    Proc Natl Acad Sci U S A. 2003 Dec 23;100(26):15566-71 PMID: 14673085
  8. Developmentally regulated piRNA clusters implicate MILI in transposon control.
    Science. 2007 May 4;316(5825):744-7 PMID: 17446352
  9. A cytochemical study of the Golgi apparatus of the spermatid during spermiogenesis in the rat.
    Am J Anat. 1982 Apr;163(4):283-94 PMID: 6124118
  10. Elective affinities: a Tudor-Aubergine tale of germline partnership.
    Genes Dev. 2010 Sep 15;24(18):1963-6 PMID: 20844011
  11. Intercellular organelle traffic through cytoplasmic bridges in early spermatids of the rat: mechanisms of haploid gene product sharing.
    Mol Biol Cell. 2003 Jul;14(7):2768-80 PMID: 12857863
  12. P granules extend the nuclear pore complex environment in the C. elegans germ line.
    J Cell Biol. 2011 Mar 21;192(6):939-48 PMID: 21402789
  13. A novel function for the Sm proteins in germ granule localization during C. elegans embryogenesis.
    Curr Biol. 2002 Sep 3;12(17):1502-6 PMID: 12225665
  14. The mouse homolog of HEN1 is a potential methylase for Piwi-interacting RNAs.
    RNA. 2007 Sep;13(9):1397-401 PMID: 17652135
  15. Cytoplasmic partitioning of P granule components is not required to specify the germline in C. elegans.
    Science. 2010 Dec 17;330(6011):1685-9 PMID: 21127218
  16. Cytological approach to morphogenesis in the planarian blastema. II. The effect of neuropeptides.
    J Submicrosc Cytol Pathol. 1997 Jan;29(1):91-7 PMID: 9066147
  17. Arginine methylation as a molecular signature of the Piwi small RNA pathway.
    Cell Cycle. 2009 Dec 15;8(24):4003-4 PMID: 19949292
  18. Argonautes ALG-3 and ALG-4 are required for spermatogenesis-specific 26G-RNAs and thermotolerant sperm in Caenorhabditis elegans.
    Proc Natl Acad Sci U S A. 2010 Feb 23;107(8):3588-93 PMID: 20133686
  19. Processing bodies and germ granules are distinct RNA granules that interact in C. elegans embryos.
    Dev Biol. 2008 Nov 1;323(1):76-87 PMID: 18692039
  20. GASZ is essential for male meiosis and suppression of retrotransposon expression in the male germline.
    PLoS Genet. 2009 Sep;5(9):e1000635 PMID: 19730684
  21. A conserved germline multipotency program.
    Development. 2010 Dec;137(24):4113-26 PMID: 21098563
  22. Immunoelectron microscopic localization of testicular and somatic cytochromes c in the seminiferous epithelium of the rat.
    Biol Reprod. 1993 Jun;48(6):1299-308 PMID: 8391332
  23. Flexible gates: dynamic topologies and functions for FG nucleoporins in nucleocytoplasmic transport.
    Eukaryot Cell. 2009 Dec;8(12):1814-27 PMID: 19801417
  24. Non-coding RNAs enter mitosis: functions, conservation and implications.
    Cell Div. 2011 Feb 28;6:6 PMID: 21356070
  25. MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline.
    Dev Cell. 2007 Apr;12(4):503-14 PMID: 17395546
  26. Multiple potential germ-line helicases are components of the germ-line-specific P granules of Caenorhabditis elegans.
    Proc Natl Acad Sci U S A. 1996 Nov 26;93(24):13837-42 PMID: 8943022
  27. Structural analysis of the nuclear pore complex by integrated approaches.
    Curr Opin Struct Biol. 2009 Apr;19(2):226-32 PMID: 19327984
  28. The Argonaute CSR-1 and its 22G-RNA cofactors are required for holocentric chromosome segregation.
    Cell. 2009 Oct 2;139(1):123-34 PMID: 19804758
  29. Bucky ball functions in Balbiani body assembly and animal-vegetal polarity in the oocyte and follicle cell layer in zebrafish.
    Dev Biol. 2008 Sep 1;321(1):40-50 PMID: 18582455
  30. CBP-independent activation of CREM and CREB by the LIM-only protein ACT.
    Nature. 1999 Mar 11;398(6723):165-9 PMID: 10086359
  31. Protection of specific maternal messenger RNAs by the P body protein CGH-1 (Dhh1/RCK) during Caenorhabditis elegans oogenesis.
    J Cell Biol. 2008 Aug 11;182(3):543-57 PMID: 18695045
  32. Ultrastructural characterization of spermatogenesis and its evolutionary conservation in the germline: germinal granules in mammals.
    Mol Cell Endocrinol. 2009 Jul 10;306(1-2):17-23 PMID: 19063939
  33. nos-1 and nos-2, two genes related to Drosophila nanos, regulate primordial germ cell development and survival in Caenorhabditis elegans.
    Development. 1999 Nov;126(21):4861-71 PMID: 10518502
  34. Posterior localization of vasa protein correlates with, but is not sufficient for, pole cell development.
    Genes Dev. 1990 Jun;4(6):905-21 PMID: 2384213
  35. EGO-1, a C. elegans RdRP, modulates gene expression via production of mRNA-templated short antisense RNAs.
    Curr Biol. 2011 Mar 22;21(6):449-59 PMID: 21396820
  36. Zebrafish vasa RNA but not its protein is a component of the germ plasm and segregates asymmetrically before germline specification.
    J Cell Biol. 2000 May 15;149(4):875-88 PMID: 10811828
  37. A large ribonucleoprotein particle induced by cytoplasmic PrP shares striking similarities with the chromatoid body, an RNA granule predicted to function in posttranscriptional gene regulation.
    Biochim Biophys Acta. 2009 Feb;1793(2):335-45 PMID: 19014979
  38. Segregation of germ granules in living Caenorhabditis elegans embryos: cell-type-specific mechanisms for cytoplasmic localisation.
    Development. 1996 Apr;122(4):1303-12 PMID: 8620857
  39. synMuv B proteins antagonize germline fate in the intestine and ensure C. elegans survival.
    Development. 2011 Mar;138(6):1069-79 PMID: 21343362
  40. Mouse RanBPM is a partner gene to a germline specific RNA helicase, mouse vasa homolog protein.
    Mol Reprod Dev. 2004 Jan;67(1):1-7 PMID: 14648869
  41. Symmetry breaking in C. elegans: another gift from the sperm.
    Dev Cell. 2006 Sep;11(3):273-4 PMID: 16950117
  42. Morphological evidence for calcium storage in the chromatoid body of rat spermatids.
    Experientia. 1989 Apr 15;45(4):377-8 PMID: 2468518
  43. RNA granules: post-transcriptional and epigenetic modulators of gene expression.
    Nat Rev Mol Cell Biol. 2009 Jun;10(6):430-6 PMID: 19461665
  44. Polar granules of Drosophila. 3. The continuity of polar granules during the life cycle of Drosophila.
    J Exp Zool. 1971 Mar;176(3):329-43 PMID: 5548873
  45. U bodies are cytoplasmic structures that contain uridine-rich small nuclear ribonucleoproteins and associate with P bodies.
    Proc Natl Acad Sci U S A. 2007 Jul 10;104(28):11655-9 PMID: 17595295
  46. A complex containing the Sm protein CAR-1 and the RNA helicase CGH-1 is required for embryonic cytokinesis in Caenorhabditis elegans.
    J Cell Biol. 2005 Oct 24;171(2):267-79 PMID: 16247027
  47. Localization of vasa protein to the Drosophila pole plasm is independent of its RNA-binding and helicase activities.
    Development. 1994 May;120(5):1201-11 PMID: 8026330
  48. An eIF4E-binding protein regulates katanin protein levels in C. elegans embryos.
    J Cell Biol. 2009 Oct 5;187(1):33-42 PMID: 19786575
  49. Ectopic expression of germline genes drives malignant brain tumor growth in Drosophila.
    Science. 2010 Dec 24;330(6012):1824-7 PMID: 21205669
  50. Piwi and piRNAs act upstream of an endogenous siRNA pathway to suppress Tc3 transposon mobility in the Caenorhabditis elegans germline.
    Mol Cell. 2008 Jul 11;31(1):79-90 PMID: 18571451
  51. Lighting up mRNA localization in Drosophila oogenesis.
    Development. 2009 Aug;136(15):2493-503 PMID: 19592573
  52. Spatiotemporal localization of germ plasm RNAs during zebrafish oogenesis.
    Mech Dev. 2007 Apr;124(4):279-89 PMID: 17293094
  53. Dynamic organization and plasticity of sponge bodies.
    Dev Dyn. 2009 Apr;238(4):918-30 PMID: 19301391
  54. A role for vasa in regulating mitotic chromosome condensation in Drosophila.
    Curr Biol. 2011 Jan 11;21(1):39-44 PMID: 21185189
  55. Maelstrom, a Drosophila spindle-class gene, encodes a protein that colocalizes with Vasa and RDE1/AGO1 homolog, Aubergine, in nuage.
    Development. 2003 Mar;130(5):859-71 PMID: 12538514
  56. Critical roles for Dicer in the female germline.
    Genes Dev. 2007 Mar 15;21(6):682-93 PMID: 17369401
  57. The endocytic pathway acts downstream of Oskar in Drosophila germ plasm assembly.
    Development. 2008 Mar;135(6):1107-17 PMID: 18272590
  58. C. elegans Dicer interacts with the P-granule component GLH-1 and both regulate germline RNPs.
    Dev Biol. 2011 Feb 15;350(2):370-81 PMID: 21146518
  59. Valois, a component of the nuage and pole plasm, is involved in assembly of these structures, and binds to Tudor and the methyltransferase Capsuléen.
    Development. 2005 May;132(9):2167-77 PMID: 15800004
  60. Maternal control of vertebrate development before the midblastula transition: mutants from the zebrafish I.
    Dev Cell. 2004 Jun;6(6):771-80 PMID: 15177026
  61. The role of a "germinal plasm" in the formation of primordial germ cells in Rana pipiens.
    Dev Biol. 1966 Oct;14(2):330-47 PMID: 6008350
  62. A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice.
    Mol Cell. 2008 Sep 26;31(6):785-99 PMID: 18922463
  63. Translational regulation of oskar mRNA by bruno, an ovarian RNA-binding protein, is essential.
    Cell. 1995 May 5;81(3):403-12 PMID: 7736592
  64. Organization of cytokeratin cytoskeleton and germ plasm in the vegetal cortex of Xenopus laevis oocytes depends on coding and non-coding RNAs: three-dimensional and ultrastructural analysis.
    Exp Cell Res. 2007 May 1;313(8):1639-51 PMID: 17376434
  65. Cup is an eIF4E binding protein required for both the translational repression of oskar and the recruitment of Barentsz.
    J Cell Biol. 2003 Dec 22;163(6):1197-204 PMID: 14691132
  66. Smaug assembles an ATP-dependent stable complex repressing nanos mRNA translation at multiple levels.
    EMBO J. 2011 Jan 5;30(1):90-103 PMID: 21081899
  67. Oskar protein interaction with Vasa represents an essential step in polar granule assembly.
    Genes Dev. 1996 Sep 1;10(17):2179-88 PMID: 8804312
  68. Hrp48, a Drosophila hnRNPA/B homolog, binds and regulates translation of oskar mRNA.
    Dev Cell. 2004 May;6(5):637-48 PMID: 15130489
  69. Vasa promotes Drosophila germline stem cell differentiation by activating mei-P26 translation by directly interacting with a (U)-rich motif in its 3' UTR.
    Genes Dev. 2009 Dec 1;23(23):2742-52 PMID: 19952109
  70. Distinct argonaute-mediated 22G-RNA pathways direct genome surveillance in the C. elegans germline.
    Mol Cell. 2009 Oct 23;36(2):231-44 PMID: 19800275
  71. Immunocytochemical localization of histone H4 in the chromatoid body of rat spermatids.
    J Submicrosc Cytol Pathol. 1995 Jul;27(3):325-30 PMID: 7671213
  72. Three-dimensional ultrastructural analysis of RNA distribution within germinal granules of Xenopus.
    Dev Biol. 2002 Jan 1;241(1):79-93 PMID: 11784096
  73. Gonadotropin-regulated testicular RNA helicase (GRTH/Ddx25) is essential for spermatid development and completion of spermatogenesis.
    Proc Natl Acad Sci U S A. 2004 Apr 27;101(17):6373-8 PMID: 15096601
  74. Germ-plasm specification and germline development in the parthenogenetic pea aphid Acyrthosiphon pisum: Vasa and Nanos as markers.
    Int J Dev Biol. 2006;50(4):413-21 PMID: 16525937
  75. Control over the morphology and segregation of Zebrafish germ cell granules during embryonic development.
    BMC Dev Biol. 2008 May 28;8:58 PMID: 18507824
  76. P granule assembly and function in Caenorhabditis elegans germ cells.
    J Androl. 2010 Jan-Feb;31(1):53-60 PMID: 19875490
  77. nanos function is essential for development and regeneration of planarian germ cells.
    Proc Natl Acad Sci U S A. 2007 Apr 3;104(14):5901-6 PMID: 17376870
  78. Polar granules of Drosophila. II. Ultrastructural changes during early embryogenesis.
    J Exp Zool. 1968 Feb;167(2):237-61 PMID: 5676182
  79. Sm proteins, the constituents of the spliceosome, are components of nuage and mitochondrial cement in Xenopus oocytes.
    Exp Cell Res. 2004 Sep 10;299(1):171-8 PMID: 15302584
  80. A novel class of small RNAs bind to MILI protein in mouse testes.
    Nature. 2006 Jul 13;442(7099):203-7 PMID: 16751777
  81. piRNA-associated germline nuage formation and spermatogenesis require MitoPLD profusogenic mitochondrial-surface lipid signaling.
    Dev Cell. 2011 Mar 15;20(3):376-87 PMID: 21397848
  82. The Balbiani body and germ cell determinants: 150 years later.
    Curr Top Dev Biol. 2004;59:1-36 PMID: 14975245
  83. Interplay of PIWI/Argonaute protein MIWI and kinesin KIF17b in chromatoid bodies of male germ cells.
    J Cell Sci. 2006 Jul 1;119(Pt 13):2819-25 PMID: 16787948
  84. Meiosis and retrotransposon silencing during germ cell development in mice.
    Differentiation. 2010 Mar;79(3):147-58 PMID: 20227008
  85. Arginine methylation of Piwi proteins catalysed by dPRMT5 is required for Ago3 and Aub stability.
    Nat Cell Biol. 2009 May;11(5):652-8 PMID: 19377467
  86. P granules in the germ cells of Caenorhabditis elegans adults are associated with clusters of nuclear pores and contain RNA.
    Dev Biol. 2000 Mar 15;219(2):315-33 PMID: 10694425
  87. Essential role of the posterior morphogen nanos for germline development in Drosophila.
    Nature. 1996 Apr 25;380(6576):708-11 PMID: 8614464
  88. Fine structural observations on the origin and associations of primordial germ cells of the mouse.
    Dev Biol. 1975 Nov;47(1):136-55 PMID: 173592
  89. Multiple controls over the efficiency of translation of the mRNAs encoding transition proteins, protamines, and the mitochondrial capsule selenoprotein in late spermatids in mice.
    Dev Biol. 1993 Oct;159(2):720-31 PMID: 8405691
  90. MILI, a PIWI-interacting RNA-binding protein, is required for germ line stem cell self-renewal and appears to positively regulate translation.
    J Biol Chem. 2009 Mar 6;284(10):6507-19 PMID: 19114715
  91. Gene silencing mechanisms mediated by Aubergine piRNA complexes in Drosophila male gonad.
    RNA. 2007 Nov;13(11):1911-22 PMID: 17872506
  92. Germ plasm and the differentiation of the germ cell line.
    Int Rev Cytol. 1975;43:229-80 PMID: 770367
  93. Mouse Piwi interactome identifies binding mechanism of Tdrkh Tudor domain to arginine methylated Miwi.
    Proc Natl Acad Sci U S A. 2009 Dec 1;106(48):20336-41 PMID: 19918066
  94. Associations between PIWI proteins and TDRD1/MTR-1 are critical for integrated subcellular localization in murine male germ cells.
    Genes Cells. 2009 Oct;14(10):1155-65 PMID: 19735482
  95. Assembly of the Drosophila germ plasm.
    Int Rev Cytol. 2001;203:187-213 PMID: 11131516
  96. The chromatoid body of male germ cells: similarity with processing bodies and presence of Dicer and microRNA pathway components.
    Proc Natl Acad Sci U S A. 2006 Feb 21;103(8):2647-52 PMID: 16477042
  97. piRNAs mediate posttranscriptional retroelement silencing and localization to pi-bodies in the Drosophila germline.
    J Cell Biol. 2009 Aug 10;186(3):333-42 PMID: 19651888
  98. Proteomic analysis of murine Piwi proteins reveals a role for arginine methylation in specifying interaction with Tudor family members.
    Genes Dev. 2009 Aug 1;23(15):1749-62 PMID: 19584108
  99. Prion protein and RNA: a view from the cytoplasm.
    Front Biosci (Landmark Ed). 2009 Jun 01;14:5157-64 PMID: 19482610
  100. Arginine methylation of vasa protein is conserved across phyla.
    J Biol Chem. 2010 Mar 12;285(11):8148-54 PMID: 20080973
  101. Induction of germ cell formation by oskar.
    Nature. 1992 Jul 30;358(6385):387-92 PMID: 1641021
  102. Arginine methyltransferase Capsuleen is essential for methylation of spliceosomal Sm proteins and germ cell formation in Drosophila.
    Development. 2007 Jan;134(1):137-46 PMID: 17164419
  103. Stress granule assembly is mediated by prion-like aggregation of TIA-1.
    Mol Biol Cell. 2004 Dec;15(12):5383-98 PMID: 15371533
  104. Germline P granules are liquid droplets that localize by controlled dissolution/condensation.
    Science. 2009 Jun 26;324(5935):1729-32 PMID: 19460965
  105. Chromatoid bodies in somatic cells of the planarian: observations on their behavior during mitosis.
    Anat Rec. 1974 Nov;180(3):533-45 PMID: 4371241
  106. Mouse oocytes within germ cell cysts and primordial follicles contain a Balbiani body.
    Proc Natl Acad Sci U S A. 2007 Jan 2;104(1):187-92 PMID: 17189423
  107. Perinuclear P granules are the principal sites of mRNA export in adult C. elegans germ cells.
    Development. 2010 Apr;137(8):1305-14 PMID: 20223759
  108. Germline autonomy of maternal-effect mutations altering the embryonic body pattern of Drosophila.
    Dev Biol. 1986 Feb;113(2):443-8 PMID: 3081391
  109. Oskar organizes the germ plasm and directs localization of the posterior determinant nanos.
    Cell. 1991 Jul 12;66(1):37-50 PMID: 2070417
  110. Contribution of the Golgi apparatus components to the formation of the acrosomic system and chromatoid body in rat spermatids.
    Anat Rec. 1988 Jun;221(2):591-8 PMID: 2843065
  111. Somatic misexpression of germline P granules and enhanced RNA interference in retinoblastoma pathway mutants.
    Nature. 2005 Jul 28;436(7050):593-7 PMID: 16049496
  112. The Xdsg protein in presumptive primordial germ cells (pPGCs) is essential to their differentiation into PGCs in Xenopus.
    Dev Biol. 2006 Sep 15;297(2):483-92 PMID: 16806152
  113. Pimet, the Drosophila homolog of HEN1, mediates 2'-O-methylation of Piwi- interacting RNAs at their 3' ends.
    Genes Dev. 2007 Jul 1;21(13):1603-8 PMID: 17606638
  114. Delocalization of Vg1 mRNA from the vegetal cortex in Xenopus oocytes after destruction of Xlsirt RNA.
    Science. 1994 Aug 19;265(5175):1101-3 PMID: 7520603
  115. A sponge-like structure involved in the association and transport of maternal products during Drosophila oogenesis.
    J Cell Biol. 1997 Nov 3;139(3):817-29 PMID: 9348297
  116. CAR-1, a protein that localizes with the mRNA decapping component DCAP-1, is required for cytokinesis and ER organization in Caenorhabditis elegans embryos.
    Mol Biol Cell. 2006 Jan;17(1):336-44 PMID: 16267265
  117. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila.
    Cell. 2007 Mar 23;128(6):1089-103 PMID: 17346786
  118. Genetic analysis of the Caenorhabditis elegans GLH family of P-granule proteins.
    Genetics. 2008 Apr;178(4):1973-87 PMID: 18430929
  119. Live imaging of nuage and polar granules: evidence against a precursor-product relationship and a novel role for Oskar in stabilization of polar granule components.
    J Cell Sci. 2004 Apr 15;117(Pt 10):2109-20 PMID: 15090597
  120. Drosophila decapping protein 1, dDcp1, is a component of the oskar mRNP complex and directs its posterior localization in the oocyte.
    Dev Cell. 2006 May;10(5):601-13 PMID: 16678775
  121. Recent advances in the morphology, cytochemistry, and function of Balbiani's vitelline body in animal oocytes.
    Int Rev Cytol. 1979;59:249-321 PMID: 385545
  122. PRG-1 and 21U-RNAs interact to form the piRNA complex required for fertility in C. elegans.
    Mol Cell. 2008 Jul 11;31(1):67-78 PMID: 18571452
  123. Ultrastructural detection of calcium and magnesium in the chromatoid body of mouse spermatids by electron spectroscopic imaging and electron energy loss spectroscopy.
    J Histochem Cytochem. 1993 Aug;41(8):1155-62 PMID: 8331281
  124. SEPA-1 mediates the specific recognition and degradation of P granule components by autophagy in C. elegans.
    Cell. 2009 Jan 23;136(2):308-21 PMID: 19167332
  125. Bucky ball organizes germ plasm assembly in zebrafish.
    Curr Biol. 2009 Mar 10;19(5):414-22 PMID: 19249209
  126. MEP-1 and a homolog of the NURD complex component Mi-2 act together to maintain germline-soma distinctions in C. elegans.
    Cell. 2002 Dec 27;111(7):991-1002 PMID: 12507426
  127. The Drosophila RNA methyltransferase, DmHen1, modifies germline piRNAs and single-stranded siRNAs in RISC.
    Curr Biol. 2007 Jul 17;17(14):1265-72 PMID: 17604629
  128. Regulated synthesis, transport and assembly of the Drosophila germ plasm.
    Trends Genet. 1996 Mar;12(3):102-9 PMID: 8868348
  129. Presence of polysaccharides and proteins in the chromatoid body of mouse spermatids.
    Cell Biol Int Rep. 1980 Mar;4(3):265-70 PMID: 7379136
  130. Germ plasm assembly and germ cell migration in Drosophila.
    Cold Spring Harb Symp Quant Biol. 1997;62:1-11 PMID: 9598330
  131. Loss of the Mili-interacting Tudor domain-containing protein-1 activates transposons and alters the Mili-associated small RNA profile.
    Nat Struct Mol Biol. 2009 Jun;16(6):639-46 PMID: 19465913
  132. The mouse homolog of Drosophila Vasa is required for the development of male germ cells.
    Genes Dev. 2000 Apr 1;14(7):841-53 PMID: 10766740
  133. Separate pathways of RNA recruitment lead to the compartmentalization of the zebrafish germ plasm.
    Dev Biol. 2006 Apr 1;292(1):129-41 PMID: 16457796
  134. Bruno acts as a dual repressor of oskar translation, promoting mRNA oligomerization and formation of silencing particles.
    Cell. 2006 Feb 10;124(3):521-33 PMID: 16469699
  135. cgh-1, a conserved predicted RNA helicase required for gametogenesis and protection from physiological germline apoptosis in C. elegans.
    Development. 2001 Sep;128(17):3221-32 PMID: 11546739
  136. Arginine methylation of Aubergine mediates Tudor binding and germ plasm localization.
    RNA. 2010 Jan;16(1):70-8 PMID: 19926723
  137. Targeting and anchoring Tudor in the pole plasm of the Drosophila oocyte.
    PLoS One. 2010 Dec 15;5(12):e14362 PMID: 21179512
  138. Observations on the origin of the 'germinal cytoplasm' in Xenopus laevis.
    J Embryol Exp Morphol. 1969 Sep;22(2):229-51 PMID: 5391303
  139. Temporally regulated traffic of HuR and its associated ARE-containing mRNAs from the chromatoid body to polysomes during mouse spermatogenesis.
    PLoS One. 2009;4(3):e4900 PMID: 19333380
  140. 4E-BP1, a repressor of mRNA translation, is phosphorylated and inactivated by the Akt(PKB) signaling pathway.
    Genes Dev. 1998 Feb 15;12(4):502-13 PMID: 9472019
  141. Immunoelectron microscopical visualization of ribonucleoproteins in the chromatoid body of mouse spermatids.
    Mol Reprod Dev. 1990 Jun;26(2):150-8 PMID: 2142601
  142. Collapse of germline piRNAs in the absence of Argonaute3 reveals somatic piRNAs in flies.
    Cell. 2009 May 1;137(3):509-21 PMID: 19395009
  143. The role of PIWI and the miRNA machinery in Drosophila germline determination.
    Curr Biol. 2006 Oct 10;16(19):1884-94 PMID: 16949822
  144. A Balbiani body and the fusome mediate mitochondrial inheritance during Drosophila oogenesis.
    Development. 2003 Apr;130(8):1579-90 PMID: 12620983
  145. The RNA interference proteins and vasa locus are involved in the silencing of retrotransposons in the female germline of Drosophila melanogaster.
    RNA Biol. 2004 May;1(1):54-8 PMID: 17194939
  146. Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes.
    Nature. 2008 May 22;453(7194):534-8 PMID: 18404147
  147. Repression of retroelements in Drosophila germline via piRNA pathway by the Tudor domain protein Tejas.
    Curr Biol. 2010 Apr 27;20(8):724-30 PMID: 20362446
  148. Hen1 is required for oocyte development and piRNA stability in zebrafish.
    EMBO J. 2010 Nov 3;29(21):3688-700 PMID: 20859253
  149. Cytoplasmic compartmentalization of the fetal piRNA pathway in mice.
    PLoS Genet. 2009 Dec;5(12):e1000764 PMID: 20011505
  150. The human VASA gene is specifically expressed in the germ cell lineage.
    Proc Natl Acad Sci U S A. 2000 Aug 15;97(17):9585-90 PMID: 10920202
  151. Rtnl1 is enriched in a specialized germline ER that associates with ribonucleoprotein granule components.
    J Cell Sci. 2007 Mar 15;120(Pt 6):1081-92 PMID: 17327273
  152. Mouse Tudor Repeat-1 (MTR-1) is a novel component of chromatoid bodies/nuages in male germ cells and forms a complex with snRNPs.
    Mech Dev. 2003 Sep;120(9):979-90 PMID: 14550528
  153. Maternal mRNAs are regulated by diverse P body-related mRNP granules during early Caenorhabditis elegans development.
    J Cell Biol. 2008 Aug 11;182(3):559-72 PMID: 18695046
  154. Tdrd6 is required for spermiogenesis, chromatoid body architecture, and regulation of miRNA expression.
    Curr Biol. 2009 Apr 28;19(8):630-9 PMID: 19345099
  155. The piRNA pathway: a fly's perspective on the guardian of the genome.
    Trends Genet. 2010 Dec;26(12):499-509 PMID: 20934772
  156. TDRD5 is required for retrotransposon silencing, chromatoid body assembly, and spermiogenesis in mice.
    J Cell Biol. 2011 Mar 7;192(5):781-95 PMID: 21383078
  157. A distinct small RNA pathway silences selfish genetic elements in the germline.
    Science. 2006 Jul 21;313(5785):320-4 PMID: 16809489
  158. Tudor-related proteins TDRD1/MTR-1, TDRD6 and TDRD7/TRAP: domain composition, intracellular localization, and function in male germ cells in mice.
    Dev Biol. 2007 Jan 1;301(1):38-52 PMID: 17141210
  159. Pathway to totipotency: lessons from germ cells.
    Cell. 2006 Dec 1;127(5):891-904 PMID: 17129777
  160. Localization of mitochondrial ribosomal RNA on the chromatoid bodies of marine planarian polyclad embryos.
    Dev Growth Differ. 2001 Apr;43(2):107-14 PMID: 11284961
  161. The biogenesis and function of PIWI proteins and piRNAs: progress and prospect.
    Annu Rev Cell Dev Biol. 2009;25:355-76 PMID: 19575643
  162. oskar mRNA is localized to the posterior pole of the Drosophila oocyte.
    Cell. 1991 Jul 12;66(1):23-35 PMID: 2070416
  163. MIWI associates with translational machinery and PIWI-interacting RNAs (piRNAs) in regulating spermatogenesis.
    Proc Natl Acad Sci U S A. 2006 Sep 5;103(36):13415-20 PMID: 16938833
  164. Aubergine is a component of a nanos mRNA localization complex.
    Dev Biol. 2011 Jan 1;349(1):46-52 PMID: 20937269
  165. A mRNA localized to the vegetal cortex of Xenopus oocytes encodes a protein with a nanos-like zinc finger domain.
    Development. 1993 Jan;117(1):377-86 PMID: 8223259
  166. Nanos is the localized posterior determinant in Drosophila.
    Cell. 1991 Aug 23;66(4):637-47 PMID: 1908748
  167. RNAi-mediated targeting of heterochromatin by the RITS complex.
    Science. 2004 Jan 30;303(5658):672-6 PMID: 14704433
  168. The TDRD9-MIWI2 complex is essential for piRNA-mediated retrotransposon silencing in the mouse male germline.
    Dev Cell. 2009 Dec;17(6):775-87 PMID: 20059948
  169. Multiple mechanisms collaborate to repress nanos translation in the Drosophila ovary and embryo.
    RNA. 2011 May;17(5):967-77 PMID: 21460235
  170. miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis.
    Dev Cell. 2002 Jun;2(6):819-30 PMID: 12062093
  171. Germ-line mitochondria exhibit suppressed respiratory activity to support their accurate transmission to the next generation.
    Dev Biol. 2011 Jan 15;349(2):462-9 PMID: 21112323
  172. Genetics of nanos localization in Drosophila.
    Dev Dyn. 1994 Feb;199(2):103-15 PMID: 7515724
  173. Mouse maelstrom, a component of nuage, is essential for spermatogenesis and transposon repression in meiosis.
    Dev Cell. 2008 Aug;15(2):285-97 PMID: 18694567
  174. Nuage morphogenesis becomes more complex: two translocation pathways and two forms of nuage coexist in Drosophila germline syncytia.
    Cell Tissue Res. 2011 Apr;344(1):169-81 PMID: 21365220
  175. An epigenetic role for maternally inherited piRNAs in transposon silencing.
    Science. 2008 Nov 28;322(5906):1387-92 PMID: 19039138
  176. Sending RNAs into the future: RNA localization and germ cell fate.
    IUBMB Life. 2004 Jan;56(1):19-27 PMID: 14992376
  177. The C. elegans homolog of nucleoporin Nup98 is required for the integrity and function of germline P granules.
    Development. 2010 May;137(9):1441-50 PMID: 20335358
  178. Oskar allows nanos mRNA translation in Drosophila embryos by preventing its deadenylation by Smaug/CCR4.
    Development. 2006 Nov;133(22):4573-83 PMID: 17050620
  179. Germ cell-specific DNA and RNA binding proteins p48/52 are expressed at specific stages of male germ cell development and are present in the chromatoid body.
    Mol Reprod Dev. 1996 May;44(1):1-13 PMID: 8722687
  180. The chromatoid body in spermatogenesis.
    Int J Androl. 2005 Aug;28(4):189-201 PMID: 16048630
  181. Functional redundancy among Nanos proteins and a distinct role of Nanos2 during male germ cell development.
    Development. 2007 Jan;134(1):77-83 PMID: 17138666
  182. Structural basis for methylarginine-dependent recognition of Aubergine by Tudor.
    Genes Dev. 2010 Sep 1;24(17):1876-81 PMID: 20713507
  183. The DEAD-box RNA helicase Vasa functions in embryonic mitotic progression in the sea urchin.
    Development. 2011 Jun;138(11):2217-22 PMID: 21525076
  184. Transport of germ plasm on astral microtubules directs germ cell development in Drosophila.
    Curr Biol. 2011 Mar 22;21(6):439-48 PMID: 21376599
  185. Interaction with eIF5B is essential for Vasa function during development.
    Development. 2004 Sep;131(17):4167-78 PMID: 15280213
  186. Presence of mitochondria-type ribosomes outside mitochondria in germ plasm of Drosophila embryos.
    Proc Natl Acad Sci U S A. 2001 Jul 31;98(16):9133-8 PMID: 11470924
  187. A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in Zebrafish.
    Cell. 2007 Apr 6;129(1):69-82 PMID: 17418787
  188. Polysomes, P bodies and stress granules: states and fates of eukaryotic mRNAs.
    Curr Opin Cell Biol. 2009 Jun;21(3):403-8 PMID: 19394210
  189. Dcp1-bodies in mouse oocytes.
    Mol Biol Cell. 2009 Dec;20(23):4951-61 PMID: 19812249
  190. Oskar anchoring restricts pole plasm formation to the posterior of the Drosophila oocyte.
    Development. 2002 Aug;129(15):3705-14 PMID: 12117819
  191. A genomewide RNAi screen for genes that affect the stability, distribution and function of P granules in Caenorhabditis elegans.
    Genetics. 2009 Dec;183(4):1397-419 PMID: 19805813
  192. Amyloid-like interactions within nucleoporin FG hydrogels.
    Proc Natl Acad Sci U S A. 2010 Apr 6;107(14):6281-5 PMID: 20304795
  193. Mice deficient for testis-brain RNA-binding protein exhibit a coordinate loss of TRAX, reduced fertility, altered gene expression in the brain, and behavioral changes.
    Mol Cell Biol. 2003 Sep;23(18):6419-34 PMID: 12944470
  194. Aubergine encodes a Drosophila polar granule component required for pole cell formation and related to eIF2C.
    Development. 2001 Jul;128(14):2823-32 PMID: 11526087
  195. MVH in piRNA processing and gene silencing of retrotransposons.
    Genes Dev. 2010 May;24(9):887-92 PMID: 20439430
  196. Temporal and spatial control of germ-plasm RNAs.
    Curr Biol. 2009 Jan 13;19(1):72-7 PMID: 19110432
  197. Association of Golgi vesicles containing acid phosphatase with the chromatoid body of rat spermatids.
    Experientia. 1983 Apr 15;39(4):393-4 PMID: 6832320
  198. Mouse MAELSTROM: the link between meiotic silencing of unsynapsed chromatin and microRNA pathway?
    Hum Mol Genet. 2006 Aug 1;15(15):2324-34 PMID: 16787967
  199. The 3' termini of mouse Piwi-interacting RNAs are 2'-O-methylated.
    Nat Struct Mol Biol. 2007 Apr;14(4):349-50 PMID: 17384646
  200. Tdrd1/Mtr-1, a tudor-related gene, is essential for male germ-cell differentiation and nuage/germinal granule formation in mice.
    Proc Natl Acad Sci U S A. 2006 Oct 24;103(43):15894-9 PMID: 17038506
  201. An overview on the diversity of cellular organelles during the germ cell cycle.
    Histol Histopathol. 2010 Feb;25(2):267-76 PMID: 20017112
  202. Functional involvement of Tudor and dPRMT5 in the piRNA processing pathway in Drosophila germlines.
    EMBO J. 2009 Dec 16;28(24):3820-31 PMID: 19959991
  203. An isoform of eIF4E is a component of germ granules and is required for spermatogenesis in C. elegans.
    Development. 2001 Oct;128(20):3899-912 PMID: 11641215
  204. Reaction of the chromatoid body with a monoclonal antibody to a rat histocompatibility antigen.
    Biol Reprod. 1985 Nov;33(4):1001-8 PMID: 3910120
  205. Isolation of new polar granule components in Drosophila reveals P body and ER associated proteins.
    Mech Dev. 2008 Sep-Oct;125(9-10):865-73 PMID: 18590813
  206. Mili, a mammalian member of piwi family gene, is essential for spermatogenesis.
    Development. 2004 Feb;131(4):839-49 PMID: 14736746
  207. Caenorhabditis elegans decapping proteins: localization and functional analysis of Dcp1, Dcp2, and DcpS during embryogenesis.
    Mol Biol Cell. 2005 Dec;16(12):5880-90 PMID: 16207815
  208. A novel group of pumilio mutations affects the asymmetric division of germline stem cells in the Drosophila ovary.
    Development. 1997 Jun;124(12):2463-76 PMID: 9199372
  209. Brief cytochalasin-induced disruption of microfilaments during a critical interval in 1-cell C. elegans embryos alters the partitioning of developmental instructions to the 2-cell embryo.
    Development. 1990 Jan;108(1):159-72 PMID: 2190787
  210. A light- and electron-microscopic study of primordial germ cells in the early mouse embryo.
    J Embryol Exp Morphol. 1973 Aug;30(1):97-118 PMID: 4729955
  211. Generation of asymmetry and segregation of germ-line granules in early C. elegans embryos.
    Cell. 1983 Nov;35(1):15-25 PMID: 6684994
  212. Actin and RNA are components of the chromatoid bodies in spermatids of the rat.
    Cell Tissue Res. 1984;236(2):487-90 PMID: 6203647
  213. Chromatoid bodies: aggresome-like characteristics and degradation sites for organelles of spermiogenic cells.
    J Histochem Cytochem. 2005 Apr;53(4):455-65 PMID: 15805420
  214. Combinatorial RNA interference indicates GLH-4 can compensate for GLH-1; these two P granule components are critical for fertility in C. elegans.
    Development. 2000 Jul;127(13):2907-16 PMID: 10851135
  215. Transformation of the germ line into muscle in mes-1 mutant embryos of C. elegans.
    Development. 1995 Sep;121(9):2961-72 PMID: 7555722
  216. Zili is required for germ cell differentiation and meiosis in zebrafish.
    EMBO J. 2008 Oct 22;27(20):2702-11 PMID: 18833190
  217. PGL proteins self associate and bind RNPs to mediate germ granule assembly in C. elegans.
    J Cell Biol. 2011 Mar 21;192(6):929-37 PMID: 21402787
  218. A conserved RNA-protein complex component involved in physiological germline apoptosis regulation in C. elegans.
    Development. 2005 Nov;132(22):4975-86 PMID: 16221731
  219. The chromatoid body: a germ-cell-specific RNA-processing centre.
    Nat Rev Mol Cell Biol. 2007 Jan;8(1):85-90 PMID: 17183363
  220. Incorporation of (3H)uridine by the chromatoid body during rat spermatogenesis.
    J Cell Biol. 1976 Jul;70(1):239-46 PMID: 932099
  221. Distribution of tudor protein in the Drosophila embryo suggests separation of functions based on site of localization.
    Development. 1993 Sep;119(1):207-19 PMID: 8275857
  222. Assembly of RNP granules in stressed and aging oocytes requires nucleoporins and is coordinated with nuclear membrane blebbing.
    Dev Biol. 2011 May 15;353(2):173-85 PMID: 21382369
  223. RNF17, a component of the mammalian germ cell nuage, is essential for spermiogenesis.
    Development. 2005 Sep;132(18):4029-39 PMID: 16093322
  224. A zebrafish nanos-related gene is essential for the development of primordial germ cells.
    Genes Dev. 2001 Nov 1;15(21):2877-85 PMID: 11691838
  225. Accumulation of piRNAs in the chromatoid bodies purified by a novel isolation protocol.
    Exp Cell Res. 2010 May 15;316(9):1567-75 PMID: 20219458
  226. vasa is required for GURKEN accumulation in the oocyte, and is involved in oocyte differentiation and germline cyst development.
    Development. 1998 May;125(9):1569-78 PMID: 9521895
  227. Mouse Piwi-interacting RNAs are 2'-O-methylated at their 3' termini.
    Nat Struct Mol Biol. 2007 Apr;14(4):347-8 PMID: 17384647
  228. The Sm-protein methyltransferase, dart5, is essential for germ-cell specification and maintenance.
    Curr Biol. 2006 Jun 6;16(11):1077-89 PMID: 16753561
  229. Milton controls the early acquisition of mitochondria by Drosophila oocytes.
    Development. 2006 Sep;133(17):3371-7 PMID: 16887820
  230. Conserved role of nanos proteins in germ cell development.
    Science. 2003 Aug 29;301(5637):1239-41 PMID: 12947200
  231. Drosophila cup is an eIF4E binding protein that associates with Bruno and regulates oskar mRNA translation in oogenesis.
    Dev Cell. 2004 Jan;6(1):69-78 PMID: 14723848
  232. PAPI, a novel TUDOR-domain protein, complexes with AGO3, ME31B and TRAL in the nuage to silence transposition.
    Development. 2011 May;138(9):1863-73 PMID: 21447556
  233. Efficient protein trafficking requires trailer hitch, a component of a ribonucleoprotein complex localized to the ER in Drosophila.
    Dev Cell. 2005 Nov;9(5):675-85 PMID: 16256742
  234. Mitochondrial small ribosomal RNA is a component of germinal granules in Xenopus embryos.
    Mech Dev. 2001 Mar;101(1-2):71-7 PMID: 11231060
  235. Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes.
    Nature. 2008 May 22;453(7194):539-43 PMID: 18404146
  236. The immunolocalization of small nuclear ribonucleoprotein particles in testicular cells during the cycle of the seminiferous epithelium of the adult rat.
    Cell Tissue Res. 1994 Nov;278(2):363-78 PMID: 8001088
  237. Effect of actinomycin D on the structure of the chromatoid body in the rat spermatids.
    Cell Tissue Res. 1977 Nov 7;184(3):411-21 PMID: 922881
  238. A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell self-renewal.
    Genes Dev. 1998 Dec 1;12(23):3715-27 PMID: 9851978
  239. Isolation of a ribonucleoprotein complex involved in mRNA localization in Drosophila oocytes.
    J Cell Biol. 2000 Feb 7;148(3):427-40 PMID: 10662770
  240. The role of Tudor domains in germline development and polar granule architecture.
    Development. 2006 Oct;133(20):4053-62 PMID: 16971472
  241. VASA mediates translation through interaction with a Drosophila yIF2 homolog.
    Mol Cell. 2000 Jan;5(1):181-7 PMID: 10678180
  242. Sm proteins specify germ cell fate by facilitating oskar mRNA localization.
    Development. 2010 Jul;137(14):2341-51 PMID: 20570937
  243. Involvement of the protein of Xenopus vasa homolog (Xenopus vasa-like gene 1, XVLG1) in the differentiation of primordial germ cells.
    Dev Growth Differ. 1997 Oct;39(5):625-33 PMID: 9338598
  244. MITOPLD is a mitochondrial protein essential for nuage formation and piRNA biogenesis in the mouse germline.
    Dev Cell. 2011 Mar 15;20(3):364-75 PMID: 21397847
  245. A protein component of Drosophila polar granules is encoded by vasa and has extensive sequence similarity to ATP-dependent helicases.
    Cell. 1988 Nov 18;55(4):577-87 PMID: 3052853
  246. Live imaging of endogenous RNA reveals a diffusion and entrapment mechanism for nanos mRNA localization in Drosophila.
    Curr Biol. 2003 Jul 15;13(14):1159-68 PMID: 12867026
  247. Presence of ribonucleoproteins and basic proteins in the nuage and intermitochondrial bars of human spermatogonia.
    J Anat. 1985 Dec;143:201-6 PMID: 3870728
  248. Mili interacts with tudor domain-containing protein 1 in regulating spermatogenesis.
    Curr Biol. 2009 Apr 28;19(8):640-4 PMID: 19345100
  249. Translational control of oskar generates short OSK, the isoform that induces pole plasma assembly.
    Development. 1995 Nov;121(11):3723-32 PMID: 8582284
  250. Large P body-like RNPs form in C. elegans oocytes in response to arrested ovulation, heat shock, osmotic stress, and anoxia and are regulated by the major sperm protein pathway.
    Dev Biol. 2008 Jun 1;318(1):38-51 PMID: 18439994
  251. Immunofluorescence visualization of germ-line-specific cytoplasmic granules in embryos, larvae, and adults of Caenorhabditis elegans.
    Proc Natl Acad Sci U S A. 1982 Mar;79(5):1558-62 PMID: 7041123
  252. Building RNA-protein granules: insight from the germline.
    Trends Cell Biol. 2010 Aug;20(8):482-90 PMID: 20541937
  253. Observations on the fine structure and relationships of the chromatoid body in mammalian spermatogenesis.
    Biol Reprod. 1970 Feb;2(1):129-53 PMID: 4106274
  254. Me31B silences translation of oocyte-localizing RNAs through the formation of cytoplasmic RNP complex during Drosophila oogenesis.
    Development. 2001 Sep;128(17):3233-42 PMID: 11546740
  255. Delivery of germinal granules and localized RNAs via the messenger transport organizer pathway to the vegetal cortex of Xenopus oocytes occurs through directional expansion of the mitochondrial cloud.
    Int J Dev Biol. 2005;49(1):17-21 PMID: 15744663
  256. Transplantation of posterior polar plasm in Drosophila. Induction of germ cells at the anterior pole of the egg.
    Proc Natl Acad Sci U S A. 1974 Apr;71(4):1016-20 PMID: 4208545
Article Info
Journal
Cold Spring Harbor perspectives in biology
Abbr.
Cold Spring Harb Perspect Biol
ISSN
1943-0264
DOI
10.1101/cshperspect.a002774
Email
evoronina@jhmi.edu
Published
2011-12-01
Epub
2011-00-01
Language
English
Region
United States
NLM ID
101513680
PMCID
PMC3225947
Subset
IM
Grants
NICHD NIH HHS · R01 HD037047 · United States
Howard Hughes Medical Institute · United States
NIGMS NIH HHS · 5F32GM080923 · United States
NICHD NIH HHS · R37 HD037047 · United States
NIGMS NIH HHS · R01 GM081634 · United States
NIGMS NIH HHS · GM081634 · United States
NIGMS NIH HHS · F32 GM080923 · United States
NICHD NIH HHS · HD37047 · United States
External Links
PubMed source DOI: 10.1101/cshperspect.a002774 PMC Full Text View journal details
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