Relationship of Other Cytoplasmic Ribonucleoprotein Bodies (cRNPB) to GW/P Bodies

Chapter
Part of the Advances in Experimental Medicine and Biology book series (volume 768)

Abstract

GW/P body components are involved in the post-transcriptional ­processing of messenger RNA (mRNA) through the RNA interference and 5′ → 3′ mRNA degradation pathways, as well as functioning in mRNA transport and stabilization. It is currently thought that the relevant mRNA silencing and degrading factors are partitioned to these cytoplasmic microdomains thus effecting post-transcriptional regulation and the prevention of accidental degradation of functional mRNA. Although much attention has focused on GW/P bodies, a variety of other cytoplasmic RNP bodies (cRNPB) also have highly specialized functions and have been shown to interact or co-localize with components of GW/P bodies. These cRNPB include neuronal transport RNP granules, stress granules, RNP-rich cytoplasmic germline granules or chromatoid bodies, sponge bodies, cytoplasmic prion protein-induced RNP granules, U bodies and TAM bodies. Of clinical relevance, autoantibodies directed against protein and miRNA components of GW/P bodies have been associated with autoimmune diseases, neurological diseases and cancer. Understanding the molecular function of GW/P bodies and their interactions with other cRNPB may provide clues to the etiology or pathogenesis of diseases associated with autoantibodies directed to these structures. This chapter will focus on the similarities and differences of the various cRNPB as an approach to understanding their functional relationships to GW/P bodies.

References

  1. Aguzzi A, Polymenidou M (2004) Mammalian prion biology: one century of evolving concepts. Cell 116:313–327PubMedCrossRefGoogle Scholar
  2. Aizer A, Brody Y, Ler LW, Sonenberg N, Singer RH, Shav-Tal Y (2008) The dynamics of mammalian P body transport, assembly and disassembly in vivo. Mol Biol Cell 19:4154–4166PubMedCrossRefGoogle Scholar
  3. Anderson P, Kedersha N (2006) RNA granules. J Cell Biol 172:803–808PubMedCrossRefGoogle Scholar
  4. Anderson P, Kedersha N (2008) Stress granules: the Tao of RNA triage. Trends Biochem Sci 33:141–150PubMedCrossRefGoogle Scholar
  5. Anderson P, Kedersha N (2009a) RNA granules: post-transcriptional and epigenetic modulators of gene expression. Nat Rev Mol Cell Biol 10:430–436PubMedCrossRefGoogle Scholar
  6. Anderson P, Kedersha N (2009b) Stress granules. Curr Biol 19:R397–R398PubMedCrossRefGoogle Scholar
  7. Andrei MA, Ingelfinger D, Heintzmann R, Achsel T, Rivera-Pomar R, Luhrmann R (2005) A role for eIF4E and eIF4E-transporter in targeting mRNPs to mammalian processing bodies. RNA 11:717–727PubMedCrossRefGoogle Scholar
  8. Antar LN, Dictenberg JB, Plociniak M, Afroz R, Bassell GJ (2005) Localization of FMRP-associated mRNA granules and requirement of microtubules for activity-dependent trafficking in hippocampal neurons. Genes Brain Behav 4:350–359PubMedCrossRefGoogle Scholar
  9. Ares M Jr, Proudfoot NJ (2005) The Spanish connection: transcription and mRNA processing get even closer. Cell 120:163–166PubMedGoogle Scholar
  10. Ashraf SI, Kunes S (2006) A trace of silence: memory and microRNA at the synapse. Curr Opin Neurobiol 16:535–539PubMedCrossRefGoogle Scholar
  11. Baillat D, Shiekhattar R (2009) Functional dissection of the human TNRC6 (GW182-related) family of proteins. Mol Cell Biol 29:4144–4155PubMedCrossRefGoogle Scholar
  12. Barbee SA, Estes PS, Cziko AM, Hillebrand J, Luedeman RA, Coller JM, Johnson N, Howlett IC, Geng C, Ueda R, Brand AH, Newbury SF, Wilhelm JE, Levine RB, Nakamura A, Parker R, Ramaswami M (2006) Staufen- and FMRP-containing neuronal RNPs are structurally and functionally related to somatic P bodies. Neuron 52:997–1009PubMedCrossRefGoogle Scholar
  13. Bashkirov VI, Scherthan H, Solinger JA, Buerstedde JM, Heyer WD (1997) A mouse cytoplasmic exoribonuclease (mXRN1p) with preference for G4 tetraplex substrates. J Cell Biol 136:761–773PubMedCrossRefGoogle Scholar
  14. Beaudoin S, Goggin K, Bissonnette C, Grenier C, Roucou X (2008) Aggresomes do not represent a general cellular response to protein misfolding in mammalian cells. BMC Cell Biol 9:59PubMedCrossRefGoogle Scholar
  15. Behm-Ansmant I, Rehwinkel J, Doerks T, Stark A, Bork P, Izaurralde E (2006) mRNA degradation by miRNAs and GW182 requires both CCR4:NOT deadenylase and DCP1:DCP2 decapping complexes. Genes Dev 20:1885–1898PubMedCrossRefGoogle Scholar
  16. Berleth T, Burri M, Thoma G, Bopp D, Richstein S, Frigerio G, Noll M, Nusslein-Volhard C (1988) The role of localization of bicoid RNA in organizing the anterior pattern of the Drosophila embryo. EMBO J 7:1749–1756PubMedGoogle Scholar
  17. Bertrand E, Bordonne R (2004) Assembly and traffic of small nuclear RNPs. Prog Mol Subcell Biol 35:79–97PubMedCrossRefGoogle Scholar
  18. Bhanji R, Eystathioy T, Chan EKL, Bloch DB, Fritzler MJ (2007) Clinical and serological features of patients with autoantibodies to GW/P bodies. Clin Immunol 123:247–256CrossRefGoogle Scholar
  19. Biggiogera M, Fakan S, Leser G, Martin TE, Gordon J (1990) Immunoelectron microscopical visualization of ribonucleoproteins in the chromatoid body of mouse spermatids. Mol Reprod Dev 26:150–158PubMedCrossRefGoogle Scholar
  20. Bloch DB, Yu JH, Yang WH, Graeme-Cook F, Lindor KD, Viswanathan A, Bloch KD, Nakajima A (2005) The cytoplasmic dot staining pattern is detected in a subgroup of patients with primary biliary cirrhosis. J Rheumatol 32:477–483PubMedGoogle Scholar
  21. Bolognani F, Perrone-Bizzozero NI (2008) RNA-protein interactions and control of mRNA stability in neurons. J Neurosci Res 86:481–489PubMedCrossRefGoogle Scholar
  22. Brengues M, Teixeira D, Parker R (2005) Movement of eukaryotic mRNAs between polysomes and cytoplasmic processing bodies. Science 310:486–489PubMedCrossRefGoogle Scholar
  23. Buchan JR, Muhlrad D, Parker R (2008) P bodies promote stress granule assembly in Saccharomyces cerevisiae. J Cell Biol 183:441–455PubMedCrossRefGoogle Scholar
  24. Carmo-Fonseca M, Tollervey D, Pepperkok R, Barabino WML, Merdes A, Brunner C, Zamore PD, Green MR, Hurt E, Lamond AI (1991) Mammalian nuclei contain foci which are highly enriched in components of the pre-mRNA splicing machinery. EMBO J 10:196–206Google Scholar
  25. Cauchi RJ, Sanchez-Pulido L, Liu JL (2010) Drosophila SMN complex proteins Gemin2, Gemin3, and Gemin5 are components of U bodies. Exp Cell Res 316:2354–2364PubMedCrossRefGoogle Scholar
  26. Chu CY, Rana TM (2006) Translation repression in human cells by microRNA-induced gene silencing requires RCK/p54. PLoS Biol 4:e210PubMedCrossRefGoogle Scholar
  27. Chuma S, Hosokawa M, Kitamura K, Kasai S, Fujioka M, Hiyoshi M, Takamune K, Noce T, Nakatsuji N (2006) 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 103:15894–15899PubMedCrossRefGoogle Scholar
  28. Chuma S, Hosokawa M, Tanaka T, Nakatsuji N (2009) Ultrastructural characterization of spermatogenesis and its evolutionary conservation in the germline: germinal granules in mammals. Mol Cell Endocrinol 306:17–23PubMedCrossRefGoogle Scholar
  29. Collinge J (2001) Prion diseases of humans and animals: their causes and molecular basis. Annu Rev Neurosci 24:519–550PubMedCrossRefGoogle Scholar
  30. Cougot N, Babajko S, Seraphin B (2004) Cytoplasmic foci are sites of mRNA decay in human cells. J Cell Biol 165:31–40PubMedCrossRefGoogle Scholar
  31. Cougot N, Bhattacharyya SN, Tapia-Arancibia L, Bordonne R, Filipowicz W, Bertrand E, Rage F (2008) Dendrites of mammalian neurons contain specialized P-body-like structures that respond to neuronal activation. J Neurosci 28:13793–13804PubMedCrossRefGoogle Scholar
  32. Ding L, Spencer A, Morita K, Han M (2005) The developmental timing regulator AIN-1 interacts with miRISCs and may target the argonaute protein ALG-1 to cytoplasmic P bodies in C. elegans. Mol Cell 19:437–447PubMedCrossRefGoogle Scholar
  33. Ecroyd H, Sarradin P, Dacheux JL, Gatti JL (2004) Compartmentalization of prion isoforms within the reproductive tract of the ram. Biol Reprod 71:993–1001PubMedCrossRefGoogle Scholar
  34. Eddy EM (1975) Germ plasm and the differentiation of the germ cell line. Int Rev Cytol 43:229–280PubMedCrossRefGoogle Scholar
  35. Eulalio A, Behm-Ansmant I, Izaurralde E (2007) P bodies: at the crossroads of post-transcriptional pathways. Nat Rev Mol Cell Biol 8:9–22PubMedCrossRefGoogle Scholar
  36. Eulalio A, Huntzinger E, Izaurralde E (2008) GW182 interaction with Argonaute is essential for miRNA-mediated translational repression and mRNA decay. Nat Struct Mol Biol 15:346–353PubMedCrossRefGoogle Scholar
  37. Eulalio A, Helms S, Fritzsch C, Fauser M, Izaurralde E (2009a) A C-terminal silencing domain in GW182 is essential for miRNA function. RNA 15:1067–1077PubMedCrossRefGoogle Scholar
  38. Eulalio A, Huntzinger E, Nishihara T, Rehwinkel J, Fauser M, Izaurralde E (2009b) Deadenylation is a widespread effect of miRNA regulation. RNA 15:21–32PubMedCrossRefGoogle Scholar
  39. Eulalio A, Tritschler F, Buttner R, Weichenrieder O, Izaurralde E, Truffault V (2009c) The RRM domain in GW182 proteins contributes to miRNA-mediated gene silencing. Nucleic Acids Res 37:2974–2983PubMedCrossRefGoogle Scholar
  40. Eulalio A, Tritschler F, Izaurralde E (2009d) The GW182 protein family in animal cells: new insights into domains required for miRNA-mediated gene silencing. RNA 15:1433–1442PubMedCrossRefGoogle Scholar
  41. Eystathioy T, Chan EKL, Tenenbaum SA, Keene JD, Griffith KJ, Fritzler MJ (2002a) A ­phosphorylated cytoplasmic autoantigen, GW182, associates with a unique population of human mRNAs within novel cytoplasmic speckles. Mol Biol Cell 13:1338–1351PubMedCrossRefGoogle Scholar
  42. Eystathioy T, Peebles C, Hamel JC, Vaughan JH, Chan EKL (2002b) Autoantibody to hLSm4 and the hepatameric LSm complex in anti-Sm sera. Arthritis Rheum 46:726–734PubMedCrossRefGoogle Scholar
  43. Eystathioy T, Chan EKL, Yang Z, Takeuchi K, Mahler M, Luft LM, Zochodne DW, Fritzler MJ (2003a) Clinical and serological associations of autoantibodies to a novel cytoplasmic autoantigen, GW182 and GW bodies. J Mol Med 81:811–818PubMedCrossRefGoogle Scholar
  44. Eystathioy T, Jakymiw A, Chan EKL, Séraphin B, Cougot N, Fritzler MJ (2003b) The GW182 protein co-localizes with mRNA degradation associated proteins hDcp1 and hLSm4 in cytoplasmic GW bodies. RNA 9:1171–1173PubMedCrossRefGoogle Scholar
  45. Fenger-Gron M, Fillman C, Norrild B, Lykke-Andersen J (2005) Multiple processing body factors and the ARE binding protein TTP activate mRNA decapping. Mol Cell 20:905–915PubMedCrossRefGoogle Scholar
  46. Fierro-Monti I, Mohammed S, Matthiesen R, Santoro R, Burns JS, Williams DJ, Proud CG, Kassem M, Jensen ON, Roepstorff P (2006) Quantitative proteomics identifies Gemin5, a scaffolding protein involved in ribonucleoprotein assembly, as a novel partner for eukaryotic initiation factor 4E. J Proteome Res 5:1367–1378PubMedCrossRefGoogle Scholar
  47. Figueroa J, Burzio LO (1998) Polysome-like structures in the chromatoid body of rat spermatids. Cell Tissue Res 291:575–579PubMedCrossRefGoogle Scholar
  48. Friedman RC, Farh KK, Burge CB, Bartel DP (2009) Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19:92–105PubMedCrossRefGoogle Scholar
  49. Fritzler MJ (1996) Clinical relevance of autoantibodies in systemic rheumatic diseases. Mol Biol Rep 23:133–145PubMedCrossRefGoogle Scholar
  50. Fujiwara Y, Komiya T, Kawabata H, Sato M, Fujimoto H, Furusawa M, Noce T (1994) Isolation of a DEAD-family protein gene that encodes a murine homolog of Drosophila vasa and its specific expression in germ cell lineage. Proc Natl Acad Sci U S A 91:12258–12262PubMedCrossRefGoogle Scholar
  51. Gall JG (2000) Cajal bodies: the first 100 years. Annu Rev Cell Dev Biol 16:273–300PubMedCrossRefGoogle Scholar
  52. Gallo CM, Munro E, Rasoloson D, Merritt C, Seydoux G (2008) Processing bodies and germ granules are distinct RNA granules that interact in C. elegans embryos. Dev Biol 323(1):76–87PubMedCrossRefGoogle Scholar
  53. Gallois-Montbrun S, Kramer B, Swanson CM, Byers H, Lynham S, Ward M, Malim MH (2007) Antiviral protein APOBEC3G localizes to ribonucleoprotein complexes found in P bodies and stress granules. J Virol 81:2165–2178PubMedCrossRefGoogle Scholar
  54. Gallouzi IE, Brennan CM, Stenberg MG, Swanson MS, Eversole A, Maizels N, Steitz JA (2000) HuR binding to cytoplasmic mRNA is perturbed by heat shock. Proc Natl Acad Sci U S A 97:3073–3078PubMedCrossRefGoogle Scholar
  55. Gibbings DJ, Ciaudo C, Erhardt M, Voinnet O (2009) Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat Cell Biol 11:1143–1149PubMedCrossRefGoogle Scholar
  56. Gilks N, Kedersha N, Ayodele M, Shen L, Stoecklin G, Dember LM, Anderson P (2004) Stress granule assembly is mediated by prion-like aggregation of TIA-1. Mol Biol Cell 15:5383–5398PubMedCrossRefGoogle Scholar
  57. Gill T, Aulds J, Schmitt ME (2006) A specialized processing body that is temporally and asymmetrically regulated during the cell cycle in Saccharomyces cerevisiae. J Cell Biol 173:35–45PubMedCrossRefGoogle Scholar
  58. Gold HA, Topper JN, Clayton DA, Craft J (1989) The RNA processing enzyme RNase MRP is identical to the Th RNP and related to RNase P. Science 245:1377–1380PubMedCrossRefGoogle Scholar
  59. Gregory RI, Chendrimada TP, Cooch N, Shiekhattar R (2005) Human RISC couples microRNA biogenesis and posttranscriptional gene silencing. Cell 123:631–640PubMedCrossRefGoogle Scholar
  60. Haraguchi CM, Mabuchi T, Hirata S, Shoda T, Hoshi K, Akasaki K, Yokota S (2005) Chromatoid bodies: aggresome-like characteristics and degradation sites for organelles of spermiogenic cells. J Histochem Cytochem 53:455–465PubMedCrossRefGoogle Scholar
  61. Hegde RS, Mastrianni JA, Scott MR, DeFea KA, Tremblay P, Torchia M, DeArmond SJ, Prusiner SB, Lingappa VR (1998) A transmembrane form of the prion protein in neurodegenerative disease. Science 279:827–834PubMedCrossRefGoogle Scholar
  62. Hess RA, Miller LA, Kirby JD, Margoliash E, Goldberg E (1993) Immunoelectron microscopic localization of testicular and somatic cytochromes c in the seminiferous epithelium of the rat. Biol Reprod 48:1299–1308PubMedCrossRefGoogle Scholar
  63. Hillebrand J, Barbee SA, Ramaswami M (2007) P-body components, microRNA regulation, and synaptic plasticity. ScientificWorldJournal 7:178–190PubMedCrossRefGoogle Scholar
  64. Hirokawa N (2006) mRNA transport in dendrites: RNA granules, motors, and tracks. J Neurosci 26:7139–7142PubMedCrossRefGoogle Scholar
  65. Hosokawa M, Shoji M, Kitamura K, Tanaka T, Noce T, Chuma S, Nakatsuji N (2007) Tudor-related proteins TDRD1/MTR-1, TDRD6 and TDRD7/TRAP: domain composition, intracellular localization, and function in male germ cells in mice. Dev Biol 301:38–52PubMedCrossRefGoogle Scholar
  66. Hoyle NP, Castelli LM, Campbell SG, Holmes LE, Ashe MP (2007) Stress-dependent relocalization of translationally primed mRNPs to cytoplasmic granules that are kinetically and spatially distinct from P-bodies. J Cell Biol 179:65–74PubMedCrossRefGoogle Scholar
  67. Huang S, Spector DL (1992) U1 and U2 small nuclear RNAs are present in nuclear speckles. Proc Natl Acad Sci U S A 89:305–308PubMedCrossRefGoogle Scholar
  68. Ingelfinger D, Arndt-Jovin DJ, Luhrmann R, Achsel T (2002) The human LSm1-7 proteins colocalize with the mRNA-degrading enzymes Dcp1/2 and Xrnl in distinct cytoplasmic foci. RNA 8:1489–1501PubMedGoogle Scholar
  69. Ivanov PA, Chudinova EM, Nadezhdina ES (2003) Disruption of microtubules inhibits cytoplasmic ribonucleoprotein stress granule formation. Exp Cell Res 290:227–233PubMedCrossRefGoogle Scholar
  70. Jakymiw A, Eystathioy T, Satoh M, Hamel JC, Fritzler MJ, Chan EKL (2005) Disruption of GW bodies impairs mammalian mRNA interference. Nat Cell Biol 7:1167–1174CrossRefGoogle Scholar
  71. Jakymiw A, Ikeda K, Fritzler MJ, Reeves WH, Satoh M, Chan EKL (2006) Autoimmune targeting of key components of RNA interference. Arthritis Res Ther 8:R87PubMedCrossRefGoogle Scholar
  72. Jakymiw A, Pauley KM, Li S, Ikeda K, Lian S, Eystathioy T, Satoh M, Fritzler MJ, Chan EKL (2007) The role of GW/P bodies in RNA processing and silencing. J Cell Sci 120:1317–1323PubMedCrossRefGoogle Scholar
  73. Karwan RM (1998) Further characterization of human RNase MRP RNase P and related autoantibodies. Mol Biol Rep 25:95–101PubMedCrossRefGoogle Scholar
  74. Kedersha N, Anderson P (2002) Stress granules: sites of mRNA triage that regulate mRNA stability and translatability. Biochem Soc Trans 30:963–969PubMedCrossRefGoogle Scholar
  75. Kedersha N, Anderson P (2007) Mammalian stress granules and processing bodies. Methods Enzymol 431:61–81PubMedCrossRefGoogle Scholar
  76. Kedersha NL, Gupta M, Li W, Miller I, Anderson P (1999) RNA-binding proteins TIA-1 and TIAR link the phosphorylation of eIF-2 alpha to the assembly of mammalian stress granules. J Cell Biol 147:1431–1442PubMedCrossRefGoogle Scholar
  77. Kedersha N, Stoecklin G, Ayodele M, Yacono P, Lykke-Andersen J, Fritzler MJ, Scheuner D, Kaufman RJ, Golan DE, Anderson P (2005) Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J Cell Biol 169:871–884PubMedCrossRefGoogle Scholar
  78. Kiebler MA, Bassell GJ (2006) Neuronal RNA granules: movers and makers. Neuron 51:685–690PubMedCrossRefGoogle Scholar
  79. Kikuchi Y, Kakeya T, Nakajima O, Sakai A, Ikeda K, Yamaguchi N, Yamazaki T, Tanamoto K, Matsuda H, Sawada J, Takatori K (2008) Hypoxia induces expression of a GPI-anchorless splice variant of the prion protein. FEBS J 275:2965–2976PubMedCrossRefGoogle Scholar
  80. Kloc M, Dougherty MT, Bilinski S, Chan AP, Brey E, King ML, Patrick CW, Etkin LD (2002) Three-dimensional ultrastructural analysis of RNA distribution within germinal granules of xenopus. Dev Biol 241:79–93PubMedCrossRefGoogle Scholar
  81. Kotaja N, Bhattacharyya SN, Jaskiewicz L, Kimmins S, Parvinen M, Filipowicz W, Sassone-Corsi P (2006) 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 103:2647–2652PubMedCrossRefGoogle Scholar
  82. Kozak SL, Marin M, Rose KM, Bystrom C, Kabat D (2006) The anti-HIV-1 editing enzyme APOBEC3G binds HIV-1 RNA and messenger RNAs that shuttle between polysomes and stress granules. J Biol Chem 281:29105–29119PubMedCrossRefGoogle Scholar
  83. Krichevsky AM, Kosik KS (2001) Neuronal RNA granules: a link between RNA localization and stimulation-dependent translation. Neuron 32:683–696PubMedCrossRefGoogle Scholar
  84. Kuwana M, Kimura K, Hirakata M, Kawakami Y, Ikeda Y (2002) Differences in autoantibody response to Th/To between systemic sclerosis and other autoimmune diseases. Ann Rheum Dis 61:842–846PubMedCrossRefGoogle Scholar
  85. Laurino CFC, Fritzler MJ, Mortara RA, Silva NP, Almeida IC, Andrade LEC (2006) Human autoantibodies to diacyl-phosphatidylethanolamine recognize a specific set of discrete cytoplasmic domains. Clin Exp Immunol 143:572–584PubMedCrossRefGoogle Scholar
  86. Lazzaretti D, Tournier I, Izaurralde E (2009) The C-terminal domains of human TNRC6A, TNRC6B, and TNRC6C silence bound transcripts independently of Argonaute proteins. RNA 15:1059–1066PubMedCrossRefGoogle Scholar
  87. Leatherman JL, Jongens TA (2003) Transcriptional silencing and translational control: key features of early germline development. Bioessays 25:326–335PubMedCrossRefGoogle Scholar
  88. Lee L, Davies SE, Liu JL (2009a) The spinal muscular atrophy protein SMN affects drosophila germline nuclear organization through the U-body-P-body pathway. Dev Biol 332:142–155PubMedCrossRefGoogle Scholar
  89. Lee YS, Pressman S, Andress AP, Kim K, White JL, Cassidy JJ, Li X, Lubell K, Lim DH, Cho IS, Nakahara K, Preall JB, Bellare P, Sontheimer EJ, Carthew RW (2009b) Silencing by small RNAs is linked to endosomal trafficking. Nat Cell Biol 11:1150–1156PubMedCrossRefGoogle Scholar
  90. Leung AK, Sharp PA (2007) microRNAs: a safeguard against turmoil? Cell 130:581–585PubMedCrossRefGoogle Scholar
  91. Leung AK, Calabrese JM, Sharp PA (2006) Quantitative analysis of Argonaute protein reveals microRNA-dependent localization to stress granules. Proc Natl Acad Sci U S A 103:18125–18130PubMedCrossRefGoogle Scholar
  92. Li S, Lian SL, Moser JJ, Fritzler ML, Fritzler MJ, Satoh M, Chan EKL (2008) Identification of GW182 and its novel isoform TNGW1 as translational repressors in Ago-2-mediated silencing. J Cell Sci 121:4134–4144PubMedCrossRefGoogle Scholar
  93. Lian S, Jakymiw A, Eystathioy T, Hamel JC, Fritzler MJ, Chan EKL (2006) GW bodies, MicroRNAs and the cell cycle. Cell Cycle 5:242–245PubMedCrossRefGoogle Scholar
  94. Lin MD, Fan SJ, Hsu WS, Chou TB (2006) Drosophila decapping protein 1, dDcp1, is a component of the oskar mRNP complex and directs its posterior localization in the oocyte. Dev Cell 10:601–613PubMedCrossRefGoogle Scholar
  95. Lin MD, Jiao X, Grima D, Newbury SF, Kiledjian M, Chou TB (2008) Drosophila processing bodies in oogenesis. Dev Biol 322:276–288PubMedCrossRefGoogle Scholar
  96. Liu JL, Gall JG (2007) U bodies are cytoplasmic structures that contain uridine-rich small nuclear ribonucleoproteins and associate with P bodies. Proc Natl Acad Sci U S A 104:11655–11659PubMedCrossRefGoogle Scholar
  97. Liu J, Carmell MA, Rivas FV, Marsden CG, Thomson JM, Song JJ, Hammond SM, Joshua-Tor L, Hannon GJ (2004) Argonaute2 is the catalytic engine of mammalian RNAi. Science 305:1437–1441PubMedCrossRefGoogle Scholar
  98. Liu J, Rivas FV, Wohlschlegel J, Yates JR III, Parker R, Hannon GJ (2005a) A role for the P-body component GW182 in microRNA function. Nat Cell Biol 7:1161–1166CrossRefGoogle Scholar
  99. Liu J, Valencia-Sanchez MA, Hannon GJ, Parker R (2005b) MicroRNA-dependent localization of targeted mRNAs to mammalian P-bodies. Nat Cell Biol 7:719–723PubMedCrossRefGoogle Scholar
  100. Liu JL, Buszczak M, Gall JG (2006) Nuclear bodies in the Drosophila germinal vesicle. Chromosome Res 14:465–475PubMedCrossRefGoogle Scholar
  101. Luft LM (2005) Thesis Dissertation: Characterization of GWBs in Breast Cancer. University of CalgaryGoogle Scholar
  102. Lugli G, Larson J, Martone ME, Jones Y, Smalheiser NR (2005) Dicer and eIF2c are enriched at postsynaptic densities in adult mouse brain and are modified by neuronal activity in a calpain-dependent manner. J Neurochem 94:896–905PubMedCrossRefGoogle Scholar
  103. Lugli G, Torvik VI, Larson J, Smalheiser NR (2008) Expression of microRNAs and their precursors in synaptic fractions of adult mouse forebrain. J Neurochem 106:650–661PubMedCrossRefGoogle Scholar
  104. Mansfield KD, Keene JD (2009) The ribonome: a dominant force in co-ordinating gene expression. Biol Cell 101:169–181PubMedCrossRefGoogle Scholar
  105. Marnef A, Sommerville J, Ladomery MR (2009) RAP55: insights into an evolutionarily conserved protein family. Int J Biochem Cell Biol 41:977–981PubMedCrossRefGoogle Scholar
  106. Martin AN, Li Y (2007) RNase MRP RNA and human genetic diseases. Cell Res 17:219–226PubMedGoogle Scholar
  107. Matranga C, Tomari Y, Shin C, Bartel DP, Zamore PD (2005) Passenger-strand cleavage facilitates assembly of siRNA into Ago2-containing RNAi enzyme complexes. Cell 123:607–620PubMedCrossRefGoogle Scholar
  108. Mazroui R, Huot ME, Tremblay S, Filion C, Labelle Y, Khandjian EW (2002) Trapping of messenger RNA by Fragile X Mental Retardation protein into cytoplasmic granules induces translation repression. Hum Mol Genet 11:3007–3017PubMedCrossRefGoogle Scholar
  109. McLellan A (2009) Exosome release by primary B cells. Crit Rev Immunol 29:203–217PubMedCrossRefGoogle Scholar
  110. Meister G, Tuschl T (2004) Mechanisms of gene silencing by double-stranded RNA. Nature 431:343–349PubMedCrossRefGoogle Scholar
  111. Meister G, Landthaler M, Peters L, Chen PY, Urlaub H, Luhrmann R, Tuschl T (2005) Identification of novel Argonaute-associated proteins. Curr Biol 15:2149–2155PubMedCrossRefGoogle Scholar
  112. Mironov A Jr, Latawiec D, Wille H, Bouzamondo-Bernstein E, Legname G, Williamson RA, Burton D, DeArmond SJ, Prusiner SB, Peters PJ (2003) Cytosolic prion protein in neurons. J Neurosci 23:7183–7193PubMedGoogle Scholar
  113. Misteli T, Caceres JF, Spector DL (1997) The dynamics of a pre-mRNA splicing factor in living cells. Nature 387:523–527PubMedCrossRefGoogle Scholar
  114. Miyoshi K, Okada TN, Siomi H, Siomi MC (2009) Characterization of the miRNA-RISC loading complex and miRNA-RISC formed in the Drosophila miRNA pathway. RNA 15:1282–1291PubMedCrossRefGoogle Scholar
  115. Mollet S, Cougot N, Wilczynska A, Dautry F, Kress M, Bertrand E, Weil D (2008) Translationally repressed mRNA transiently cycles through stress granules during stress. Mol Biol Cell 19:4469–4479PubMedCrossRefGoogle Scholar
  116. Moser JJ, Fritzler MJ (2010) Cytoplasmic ribonucleoprotein (RNP) bodies and their relationship to GW/P bodies. Int J Biochem Cell Biol 42:828–843PubMedCrossRefGoogle Scholar
  117. Moser JJ, Eystathioy T, Chan EKL, Fritzler MJ (2007) Markers of mRNA stabilization and degradation, and RNAi within astrocytoma GW bodies. J Neurosci Res 85:3619–3631PubMedCrossRefGoogle Scholar
  118. Moser JJ, Chan EKL, Fritzler MJ (2009) Optimization of immunoprecipitation-western blot analysis in detecting GW182-associated components of GW/P bodies. Nat Protoc 4:674–685PubMedCrossRefGoogle Scholar
  119. Moser JJ, Fritzler MJ, Rattner JB (2011) Repression of GW/P body components and the RNAi microprocessor impacts primary ciliogenesis in human astrocytes. BMC Cell Biol 12:37PubMedCrossRefGoogle Scholar
  120. Moussa F, Oko R, Hermo L (1994) The immunolocalization of small nuclear ribonucleoprotein particles in testicular cells during the cycle of the seminiferous epithelium of the adult rat. Cell Tissue Res 278:363–378PubMedCrossRefGoogle Scholar
  121. Musunuru K, Darnell RB (2001) Paraneoplastic neurologic disease antigens: RNA-binding proteins and signaling proteins in neuronal degeneration. Annu Rev Neurosci 24:239–262PubMedCrossRefGoogle Scholar
  122. Nagamori I, Sassone-Corsi P (2008) The chromatoid body of male germ cells: epigenetic control and miRNA pathway. Cell Cycle 7:3503–3508PubMedCrossRefGoogle Scholar
  123. Nakamura A, Amikura R, Hanyu K, Kobayashi S (2001) Me31B silences translation of oocyte-localizing RNAs through the formation of cytoplasmic RNP complex during Drosophila oogenesis. Development 128:3233–3242PubMedGoogle Scholar
  124. Narayanan U, Achsel T, Luhrmann R, Matera AG (2004) Coupled in vitro import of U snRNPs and SMN, the spinal muscular atrophy protein. Mol Cell 16:223–234PubMedCrossRefGoogle Scholar
  125. Nissan T, Parker R (2008) Analyzing P-bodies in Saccharomyces cerevisiae. Methods Enzymol 448:507–520PubMedCrossRefGoogle Scholar
  126. Pare JM, Tahbaz N, Lopez-Orozco J, Lapointe P, Lasko P, Hobman TC (2009) Hsp90 regulates the function of Argonaute 2 and its recruitment to stress granules and P-bodies. Mol Biol Cell 20:3273–3284PubMedCrossRefGoogle Scholar
  127. Parker R, Sheth U (2007) P bodies and the control of mRNA translation and degradation. Mol Cell 25:635–646PubMedCrossRefGoogle Scholar
  128. Parvinen M (2005) The chromatoid body in spermatogenesis. Int J Androl 28:189–201PubMedCrossRefGoogle Scholar
  129. Pauley KM, Eystathioy T, Jakymiw A, Hamel JC, Fritzler MJ, Chan EKL (2006) Formation of GW bodies is a consequence of microRNA genesis. EMBO Rep 7:904–910PubMedCrossRefGoogle Scholar
  130. Perl A (2009) Emerging new pathways of pathogenesis and targets for treatment in systemic lupus erythematosus and Sjogren’s syndrome. Curr Opin Rheumatol 21:443–447PubMedCrossRefGoogle Scholar
  131. Pillai RS, Bhattacharyya SN, Artus CG, Zoller T, Cougot N, Basyuk E, Bertrand E, Filipowicz W (2005) Inhibition of translational initiation by Let-7 microRNA in human cells. Science 309:1573–1576PubMedCrossRefGoogle Scholar
  132. Prusiner SB (1998) Prions. Proc Natl Acad Sci U S A 95:13363–13383PubMedCrossRefGoogle Scholar
  133. Quaresma AJ, Bressan GC, Gava LM, Lanza DC, Ramos CH, Kobarg J (2009) Human HnRNP Q re-localizes to cytoplasmic granules upon PMA, thapsigargin, Arsenite and heat-shock treatments. Exp Cell Res 315:968–980PubMedCrossRefGoogle Scholar
  134. Rabinowits G, Gercel-Taylor C, Day JM, Taylor DD, Kloecker GH (2009) Exosomal microRNA: a diagnostic marker for lung cancer. Clin Lung Cancer 10:42–46PubMedCrossRefGoogle Scholar
  135. Rana TM (2007) Illuminating the silence: understanding the structure and function of small RNAs. Nat Rev Mol Cell Biol 8:23–36PubMedCrossRefGoogle Scholar
  136. Rehwinkel J, Behm-Ansmant I, Gatfield D, Izaurralde E (2005) A crucial role for GW182 and the DCP1:DCP2 decapping complex in miRNA-mediated gene silencing. RNA 11:1640–1647PubMedCrossRefGoogle Scholar
  137. Rosen A, Casciola-Rosen L (2009) Autoantigens in systemic autoimmunity: critical partner in pathogenesis. J Intern Med 265:625–631PubMedCrossRefGoogle Scholar
  138. Roucou X (2009) Prion protein and RNA: a view from the cytoplasm. Front Biosci 14:5157–5164PubMedCrossRefGoogle Scholar
  139. Scheller N, Resa-Infante P, de la Luna S, Galao RP, Albrecht M, Kaestner L, Lipp P, Lengauer T, Meyerhans A, Diez J (2007) Identification of PatL1, a human homolog to yeast P body component Pat1. Biochim Biophys Acta 1773:1786–1792PubMedCrossRefGoogle Scholar
  140. Schisa JA, Pitt JN, Priess JR (2001) Analysis of RNA associated with P granules in germ cells of C. elegans adults. Development 128:1287–1298PubMedGoogle Scholar
  141. Schneider MD, Najand N, Chaker S, Pare JM, Haskins J, Hughes SC, Hobman TC, Locke J, Simmonds AJ (2006) Gawky is a component of cytoplasmic mRNA processing bodies required for early Drosophila development. J Cell Biol 174:349–358PubMedCrossRefGoogle Scholar
  142. Schratt GM, Tuebing F, Nigh EA, Kane CG, Sabatini ME, Kiebler M, Greenberg ME (2006) A brain-specific microRNA regulates dendritic spine development. Nature 439:283–289PubMedCrossRefGoogle Scholar
  143. Schumperli D, Pillai RS (2004) The special Sm core structure of the U7 snRNP: far-reaching significance of a small nuclear ribonucleoprotein. Cell Mol Life Sci 61:2560–2570PubMedCrossRefGoogle Scholar
  144. Sen GL, Blau HM (2005) Argonaute 2/RISC resides in sites of mammalian mRNA decay known as cytoplasmic bodies. Nat Cell Biol 7:633–636PubMedCrossRefGoogle Scholar
  145. Serman A, LeRoy F, Aigueperse C, Kress M, Dautry F, Weil D (2007) GW body disassembly triggered by siRNAs independently of their silencing activity. Nucleic Acids Res 35:4715–4727PubMedCrossRefGoogle Scholar
  146. Sheth U, Parker R (2003) Decapping and decay of messenger RNA occur in cytoplasmic processing bodies. Science 300:805–808PubMedCrossRefGoogle Scholar
  147. Sheth U, Parker R (2006) Targeting of aberrant mRNAs to cytoplasmic processing bodies. Cell 125:1095–1109PubMedCrossRefGoogle Scholar
  148. Simpson RJ, Lim JW, Moritz RL, Mathivanan S (2009) Exosomes: proteomic insights and diagnostic potential. Expert Rev Proteomics 6:267–283PubMedCrossRefGoogle Scholar
  149. Snee MJ, Macdonald PM (2009) Dynamic organization and plasticity of sponge bodies. Dev Dyn 238:918–930PubMedCrossRefGoogle Scholar
  150. Sossin WS, DesGroseillers L (2006) Intracellular trafficking of RNA in neurons. Traffic 7:1581–1589PubMedCrossRefGoogle Scholar
  151. Souquere S, Mollet S, Kress M, Dautry F, Pierron G, Weil D (2009) Unravelling the ultrastructure of stress granules and associated P-bodies in human cells. J Cell Sci 122:3619–3626PubMedCrossRefGoogle Scholar
  152. St Johnston D (2005) Moving messages: the intracellular localization of mRNAs. Nat Rev Mol Cell Biol 6:363–375PubMedCrossRefGoogle Scholar
  153. St JD, Driever W, Berleth T, Richstein S, Nusslein-Volhard C (1989) Multiple steps in the localization of bicoid RNA to the anterior pole of the Drosophila oocyte. Development 107(Suppl):13–19Google Scholar
  154. Stinton LM, Eystathioy T, Selak S, Chan EKL, Fritzler MJ (2004) Autoantibodies to protein transport and messenger RNA processing pathways: endosomes, lysosomes, Golgi complex, proteasomes, assemblyosomes, exosomes and GW Bodies. Clin Immunol 110:30–44PubMedCrossRefGoogle Scholar
  155. Strom A, Wang GS, Reimer R, Finegood DT, Scott FW (2007) Pronounced cytosolic aggregation of cellular prion protein in pancreatic beta-cells in response to hyperglycemia. Lab Invest 87:139–149PubMedCrossRefGoogle Scholar
  156. Sutton MA, Schuman EM (2006) Dendritic protein synthesis, synaptic plasticity, and memory. Cell 127:49–58PubMedCrossRefGoogle Scholar
  157. Tan EM (1991) Autoantibodies in pathology and cell biology. Cell 67:841–842PubMedCrossRefGoogle Scholar
  158. Tarn WY, Steitz JA (1997) Pre-mRNA splicing: the discovery of a new spliceosome doubles the challenge. Trends Biochem Sci 22:132–137PubMedCrossRefGoogle Scholar
  159. Teixeira D, Sheth U, Valencia-Sanchez MA, Brengues M, Parker R (2005) Processing bodies require RNA for assembly and contain nontranslating mRNAs. RNA 11:371–382PubMedCrossRefGoogle Scholar
  160. Thomas MG, Tosar LJM, Loschi M, Pasquini JM, Correale J, Kindler S, Boccaccio GL (2005) Staufen recruitment into stress granules does not affect early mRNA transport in oligodendrocytes. Mol Biol Cell 16:405–420PubMedCrossRefGoogle Scholar
  161. Tourriere H, Gallouzi IE, Chebli K, Capony JP, Mouaikel J, Van der Geer P, Tazi J (2001) RasGAP-associated endoribonuclease G3Bp: selective RNA degradation and phosphorylation-dependent localization. Mol Cell Biol 21:7747–7760PubMedCrossRefGoogle Scholar
  162. Tourrière H, Chebli K, Zekri L, Courselaud B, Blanchard JM, Bertrand E, Tazi J (2003) The RasGAP-associated endoribonuclease G3BP assembles stress granules. J Cell Biol 160:823–831PubMedCrossRefGoogle Scholar
  163. Toyooka Y, Tsunekawa N, Takahashi Y, Matsui Y, Satoh M, Noce T (2000) Expression and intracellular localization of mouse Vasa-homologue protein during germ cell development. Mech Dev 93:139–149PubMedCrossRefGoogle Scholar
  164. Tsai-Morris CH, Sheng Y, Lee E, Lei KJ, Dufau ML (2004) Gonadotropin-regulated testicular RNA helicase (GRTH/Ddx25) is essential for spermatid development and completion of spermatogenesis. Proc Natl Acad Sci U S A 101:6373–6378PubMedCrossRefGoogle Scholar
  165. van Dijk E, Cougot N, Meyer S, Babajko S, Wahle E, Séraphin B (2002) Human Dcp2: a catalytically active mRNA decapping enzyme located in specific cytoplasmic structures. EMBO J 21:6915–6924PubMedCrossRefGoogle Scholar
  166. van Eenennaam H, Vogelzangs JHP, Lugtenberg D, van den Hoogen FHJ, Van Venrooij WJ, Pruijn GJM (2002) Identity of the RNase MRP- and RNase P-associated Th/To autoantigen. Arthritis Rheum 46:3266–3272PubMedCrossRefGoogle Scholar
  167. Vey M, Pilkuhn S, Wille H, Nixon R, DeArmond SJ, Smart EJ, Anderson RG, Taraboulos A, Prusiner SB (1996) Subcellular colocalization of the cellular and scrapie prion proteins in caveolae-like membranous domains. Proc Natl Acad Sci U S A 93:14945–14949PubMedCrossRefGoogle Scholar
  168. Werner G, Werner K (1995) Immunocytochemical localization of histone H4 in the chromatoid body of rat spermatids. J Submicrosc Cytol Pathol 27:325–330PubMedGoogle Scholar
  169. Wilczynska A, Aigueperse C, Kress M, Dautry F, Weil D (2005) The translational regulator CPEB1 provides a link between dcp1 bodies and stress granules. J Cell Sci 118:981–992PubMedCrossRefGoogle Scholar
  170. Wilhelm JE, Mansfield J, Hom-Booher N, Wang S, Turck CW, Hazelrigg T, Vale RD (2000) Isolation of a ribonucleoprotein complex involved in mRNA localization in Drosophila oocytes. J Cell Biol 148:427–440PubMedCrossRefGoogle Scholar
  171. Will CL, Luhrmann R (2001) Spliceosomal UsnRNP biogenesis, structure and function. Curr Opin Cell Biol 13:290–301PubMedCrossRefGoogle Scholar
  172. Wilsch-Brauninger M, Schwarz H, Nusslein-Volhard C (1997) A sponge-like structure involved in the association and transport of maternal products during Drosophila oogenesis. J Cell Biol 139:817–829PubMedCrossRefGoogle Scholar
  173. Yamane K, Ihn H, Kubo M, Kuwana M, Asano Y, Yazawa N, Tamaki K (2001) Antibodies to Th/To ribonucleoprotein in patients with localized scleroderma. Rheumatology 40:683–686PubMedCrossRefGoogle Scholar
  174. Yamochi T, Ohnuma K, Hosono O, Tanaka H, Kanai Y, Morimoto C (2008) SSA/Ro52 autoantigen interacts with Dcp2 to enhance its decapping activity. Biochem Biophys Res Commun 370:195–199PubMedCrossRefGoogle Scholar
  175. Yang Z, Jakymiw A, Wood MR, Eystathioy T, Rubin RL, Fritzler MJ, Chan EKL (2004) GW182 is critical for the stability of GW bodies expressed during the cell cycle and cell proliferation. J Cell Sci 117:5567–5578PubMedCrossRefGoogle Scholar
  176. Yang WH, Yu JH, Gulick T, Bloch KD, Bloch DB (2006) RNA-associated protein 55 (RAP55) localizes to mRNA processing bodies and stress granules. RNA 12:547–554PubMedCrossRefGoogle Scholar
  177. Yu JH, Yang WH, Gulick T, Bloch KD, Bloch DB (2005) Ge-1 is a central component of the mammalian cytoplasmic mRNA processing body. RNA 11:1795–1802PubMedCrossRefGoogle Scholar
  178. Zee JM, Shideler KK, Eystathioy T, Bruecks AK, Fritzler MJ, Mydlarski PR (2008) GW bodies: cytoplasmic compartments in normal human skin. J Invest Dermatol 128:2902–2912CrossRefGoogle Scholar
  179. Zeitelhofer M, Karra D, Macchi P, Tolino M, Thomas S, Schwarz M, Kiebler M, Dahm R (2008) Dynamic interaction between P-bodies and transport ribonucleoprotein particles in dendrites of mature hippocampal neurons. J Neurosci 28:7555–7562PubMedCrossRefGoogle Scholar
  180. Zeng Y, Sankala H, Zhang X, Graves PR (2008) Phosphorylation of Argonaute 2 at serine-387 facilitates its localization to processing bodies. Biochem J 413:429–436PubMedCrossRefGoogle Scholar
  181. Zhang L, Ding L, Cheung TH, Dong MQ, Chen J, Sewell AK, Liu X, Yates JR III, Han M (2007) Systematic identification of C. elegans miRISC proteins, miRNAs, and mRNA targets by their interactions with GW182 proteins AIN-1 and AIN-2. Mol Cell 28:598–613PubMedCrossRefGoogle Scholar
  182. Zipprich JT, Bhattacharyya S, Mathys H, Filipowicz W (2009) Importance of the C-terminal domain of the human GW182 protein TNRC6C for translational repression. RNA 20:781–793CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Department of Biochemistry and Molecular BiologyUniversity of CalgaryCalgaryCanada

Personalised recommendations