The Balbiani Ring Story: Synthesis, Assembly, Processing, and Transport of Specific Messenger RNA–Protein Complexes

Literature Cited

1. Pan T, Sosnick T. 1.  2006. RNA folding during transcription. Annu. Rev. Biophys. Biomol. Struct. 35:161–75 [Google Scholar]
2. Lai D, Proctor JR, Meyer IM. 2.  2013. On the importance of cotranscriptional RNA structure formation. RNA 19:1461–73 [Google Scholar]
3. Hopfield JJ. 3.  1974. Kinetic proofreading: a new mechanism for reducing errors in biosynthetic processes requiring high specificity. PNAS 71:4135–39 [Google Scholar]
4. Dreyfuss G, Kim VN, Kataoka N. 4.  2002. Messenger-RNA-binding proteins and the messages they carry. Nat. Rev. 3:195–205 [Google Scholar]
5. Müller-McNicoll M, Neugebauer KM. 5.  2013. How cells get the message: dynamic assembly and function of mRNA–protein complexes. Nat. Rev. Genet. 14:275–87 [Google Scholar]
6. Wahle E, Rüegsegger U. 6.  1999. 3′-end processing of pre-mRNA in eukaryotes. FEMS Microbiol. Rev. 23:277–95 [Google Scholar]
7. Will CL, Lührmann R. 7.  2011. Spliceosome structure and function. Cold Spring Harb. Perspect. Biol. 1:3 [Google Scholar]
8. Blackburn E, Gall J. 8.  1978. A tandemly repeated sequence at the termini of the extrachromosomal ribosomal RNA genes in Tetrahymena. J. Mol. Biol. 120:33–53 [Google Scholar]
9. Balbiani EG. 9.  1881. Sur la structure du noyau de cellules salivaires chez les larves de Chironomus. Zool. Anz. 4:637–41662–66 [Google Scholar]
10. Beermann W. 10.  1962. Riesenchromosomen. Protoplasmologia 6:1–61 [Google Scholar]
11. Daneholt B, Edström JE. 11.  1967. The content of deoxyribonucleic acid in individual polytene chromosomes of Chironomus tentans. Cytogenetics 6:350–56 [Google Scholar]
12. Macgreggor HC. 12.  2012. Chromomeres revisited. Chromosome Res. 20:911–24 [Google Scholar]
13. Fakan S, van Driel R. 13.  2007. The perichromatin region: a functional compartment in the nucleus that determines large-scale chromatin folding. Semin. Cell Dev. Biol. 18:676–81 [Google Scholar]
14. Wu N, Lianf C, DiBartolomeis SM, Smith HS, Gerbi SA. 14.  1993. Developmental progression of DNA puffs in Sciara coprophila: amplification and transcription. Dev. Biol. 160:73–84 [Google Scholar]
15. Beermann W. 15.  1952. Chromomerenkonstanz und spezifische Modifikationen der Chromosomenstruktur in der Entwicklung und Organdifferenzierung von Chironomus tentans. Chromosoma 5:139–98 [Google Scholar]
16. Beermann W. 16.  1961. Ein Balbiani-ring als Locus einer Speicheldrüsen-Mutation.. Chromosoma 12:1–25 [Google Scholar]
17. Beermann W. 17.  1973. Directed changes in the pattern of Balbiani ring puffing in Chironomus: effects of a sugar treatment. Chromosoma 41:297–326 [Google Scholar]
18. Botella LM, Edström JE. 18.  1991. The Balbiani ring 6 induction in Chironomus. Biol. Cell 71:11–16 [Google Scholar]
19. Case ST, Wieslander L. 19.  1992. Secretory proteins of Chironomus salivary glands: structural motifs and assembly characteristics of a novel biopolymer. Results Probl. Cell Differ 19:187–226 [Google Scholar]
20. Wieslander L. 20.  1994. The Balbiani ring multigene family: coding repetitive sequences and evolution of a tissue-specific cell function. Prog. Nucleic Acids Res. Mol. Biol. 48:275–313 [Google Scholar]
21. Sümegi J, Wieslander L, Daneholt B. 21.  1982. A hierarchic arrangement of the repetitive sequences in the Balbiani ring 2 gene of Chironomus tentans. Cell 30:579–87 [Google Scholar]
22. Jäckle H, Almeida JC, Galler R, Kluding H, Lehrach H, Edström JE. 22.  1982. Constant and variable parts of Balbiani ring 2 repeat unit and the translation termination region. EMBO J. 1:883–88 [Google Scholar]
23. Case ST, Byers MR. 23.  1983. Repeated nucleotide sequence arrays in Balbiani ring 1 of Chironomus tentans contain internally nonrepeating and subrepeating elements. J. Biol. Chem. 258:7793–99 [Google Scholar]
24. Pustell J, Kafatos FC, Wobus U, Bäumlein H. 24.  1984. Balbiani ring DNA: sequence comparisons and evolutionary history of a family of hierarchically repetitive protein-coding sequences. J. Mol. Evol. 20:281–85 [Google Scholar]
25. Paulsson G, Wieslander L. 25.  1992. Sequence organization of the Balbiani ring 2.1 gene in Chironomus tentans. PNAS 89:4578–82 [Google Scholar]
26. Paulsson G, Lendahl U, Galli J, Ericsson C, Wieslander L. 26.  1990. The Balbiani ring 3 gene in Chironomus tentans has a diverged repetitive structure split by many introns. J. Mol. Biol. 211:331–49 [Google Scholar]
27. Kutsenko A, Svensson T, Nystedt B, Lundeberg J, Björk P. 27.  et al. 2014. The Chironomus tentans genome sequence and the organization of the Balbiani ring genes. BMC Genomics 15:819–30 [Google Scholar]
28. Derksen J, Wieslander L, van der Ploeg M, Daneholt B. 28.  1980. Identification of the Balbiani ring 2 chromomere and determination of the content and compaction of its DNA. Chromosoma 81:65–84 [Google Scholar]
29. Lamb MM, Daneholt B. 29.  1979. Characterization of active transcription units in Balbiani rings of Chironomus tentans. Cell 17:835–48 [Google Scholar]
30. Nelson LG, Daneholt B. 30.  1981. Modulation of 75S RNA synthesis in the Balbiani rings of Chironomus tentans with galactose treatment. Chromosoma 83:645–59 [Google Scholar]
31. Andersson K, Björkroth B, Daneholt B. 31.  1980. The in situ structure of the active 75S RNA genes in Balbiani rings of Chironomus tentans. Exp. Cell Res. 130:313–26 [Google Scholar]
32. Belikov S, Paulsson G, Wieslander L. 32.  1998. Promoter regions of four Balbiani ring genes in Chironomus tentans exhibit a common salivary gland–specific chromatin organization, which is independent of the rate of transcriptional initiation. Mol. Gen. Genet. 258:420–26 [Google Scholar]
33. Andersson K, Björkroth B, Daneholt B. 33.  1984. Packing of a specific gene into higher order structures following repression of RNA synthesis. J. Cell Biol. 98:1296–303 [Google Scholar]
34. Ericsson C, Mehlin H, Björkroth B, Lamb MM, Daneholt B. 34.  1989. The ultrastructure of upstream and downstream regions of an active Balbiani ring gene. Cell 56:631–39 [Google Scholar]
35. Baurén G, Belikov S, Wieslander L. 35.  1998. Transcriptional termination in the Balbiani ring 1 gene is closely coupled to the 3′-end formation and excision of the 3′-terminal intron. Genes Dev. 12:2759–69 [Google Scholar]
36. Egyhazi E. 36.  1975. Inhibition of Balbiani ring RNA synthesis at the initiation level. PNAS 72:947–50 [Google Scholar]
37. Edström JE, Ericsson E, Lindgren S, Lönn U, Rydlander L. 37.  1978. Fate of Balbiani ring RNA in vivo. Cold Spring Harb. Symp. Quant. Biol. 42:877–84 [Google Scholar]
38. Edström JE, Lindgren S, Lönn U, Rydlander L. 38.  1978. Balbiani ring RNA content and half-life in nucleus and cytoplasm. Chromosoma 66:33–44 [Google Scholar]
39. Edström JE, Beermann W. 39.  1962. The base composition of nucleic acids in chromosomes, puffs, nucleoli and cytoplasm in Chironomus tentans salivary gland cells. J. Mol. Biol. 28:331–43 [Google Scholar]
40. Papantonis A, Cook PR. 40.  2013. Transcription factories: genome organization and gene regulation. Chem. Rev. 113:8683–705 [Google Scholar]
41. Wetterberg I, Baurén G, Wieslander L. 41.  1996. The intranuclear site of excision of each intron in Balbiani ring 3 pre-mRNA is influenced by the time remaining to transcription termination and different excision efficiencies for the various introns. RNA 2:641–51 [Google Scholar]
42. Wetterberg I, Zhao J, Masich S, Wieslander L, Skoglund U. 42.  2001. In situ transcription and splicing in the Balbiani ring 3 gene. EMBO J. 20:2564–74 [Google Scholar]
43. Skoglund U, Andersson K, Björkroth B, Lamb MM, Daneholt B. 43.  1983. Visualization of the formation and transport of a specific hnRNP particle. Cell 34:847–55 [Google Scholar]
44. Lönnroth A, Alexciev K, Mehlin H, Wurtz T, Skoglund U, Daneholt B. 44.  1992. Demonstration of a 7-nm RNP fiber as the basic structural element in a premessenger RNP particle. Exp. Cell Res. 199:292–96 [Google Scholar]
45. Kiseleva J, Wurtz T, Visa N, Daneholt B. 45.  1994. Assembly and disassembly of spliceosomes along a specific pre-messenger RNP fiber. EMBO J. 13:6052–61 [Google Scholar]
46. Singh G, Kucukaral A, Cenik C, Leszyk JD, Shaffer SA. 46.  et al. 2012. The cellular EJC interactome reveals higher-order mRNP structure and an EJC–SR protein nexus. Cell 151:750–64 [Google Scholar]
47. Batisse J, Batisse C, Budd A, Böttcher B, Hurt E. 47.  2009. Purification of nuclear poly(A)-binding protein Nab2 reveals association with the yeast transcriptome and a messenger ribonucleoprotein core structure. J. Biol. Chem. 284:34911–17 [Google Scholar]
48. Mor A, Suliman S, Ben-Yishay R, Ynger S, Brody Y, Shav-Tal Y. 48.  2010. Dynamics of single mRNP nucleocytoplasmic transport and export through the nuclear pore in living cells. Nat. Cell Biol. 12:543–54 [Google Scholar]
49. Percipalle P, Fomproix N, Kylberg K, Miralles F, Björkroth B. 49.  et al. 2003. An actin–ribonucleoprotein interaction is involved in transcription by RNA polymerase II. PNAS 100:6475–80 [Google Scholar]
50. Sjölinder M, Björk P, Sjöberg E, Sabri N, Östlund-Farrants AK, Visa N. 50.  2005. The growing pre-mRNA recruits actin and chromatin-modifying factors to transcriptionally active genes. Genes Dev. 19:1871–84 [Google Scholar]
51. Eberle AB, Hessle V, Helbig R, Dantoft W, Gimber N, Visa N. 51.  2010. Splice-site mutations cause Rrp6-mediated nuclear retention of the unspliced RNAs and transcriptional down-regulation of the splicing-defective genes. PLOS ONE 5e11540
52. Hessle V, von Euler A, González de Valdivia E, Visa N. 52.  2012. Rrp6 is recruited to transcribed genes and accompanies the spliced mRNA to the nuclear pore. RNA 18:1466–74 [Google Scholar]
53. Hessle V, Björk P, Sokolowski M, González de Valdivia E, Silverstein R. 53.  et al. 2009. The exosome associates cotranscriptionally with the nascent pre-mRNP through interactions with heterogeneous nuclear ribonucleoproteins. Mol. Biol. Cell 20:3459–70 [Google Scholar]
54. Baurén G, Wieslander L. 54.  1994. Splicing of Balbiani ring 1 gene pre-mRNA occurs simultaneously with transcription. Cell 76:183–92 [Google Scholar]
55. Visa N, Izaurralde E, Ferreira J, Daneholt B, Mattaj IW. 55.  1996. A nuclear cap-binding complex binds Balbiani ring pre-mRNA cotranscriptionally and accompanies the ribonucleoprotein particle during nuclear export. J. Cell Biol. 133:5–14 [Google Scholar]
56. Beyer AL, Osheim Y. 56.  1988. Splice site selection, rate of splicing and alternative splicing on nascent transcripts. Genes Dev. 2:754–65 [Google Scholar]
57. Baurén G, Jiang WQ, Bernholm K, Gu F, Wieslander L. 57.  1996. Demonstration of a dynamic, transcription-dependent organization of pre-mRNA splicing factors in polytene nuclei. J. Cell Biol. 133:929–41 [Google Scholar]
58. Misteli T, Cáceres JF, Clement JQ, Krainer AR, Wilkinson MF, Spector DL. 58.  1998. Serine phosphorylation of SR proteins is required for their recruitment to sites of transcription in vivo. J. Cell Biol. 143:297–307 [Google Scholar]
59. Brugiolo M, Herzel L, Neugebauer KM. 59.  2013. Counting on co-transcriptional splicing. F1000Prime Rep. 5:9 [Google Scholar]
60. Sass H, Pederson T. 60.  1984. Transcription-dependent localization of U1 and U2 small nuclear ribonucleoproteins at major sites of gene activity in polytene chromosomes. J. Mol. Biol. 180:911–26 [Google Scholar]
61. Bear DG, Fomproix N, Soop T, Björkroth B, Masich S, Daneholt B. 61.  2003. Nuclear poly(A)-binding protein PABPN1 is associated with RNA polymerase II during transcription and accompanies the released transcript to the nuclear pore. Exp. Cell Res. 286:332–44 [Google Scholar]
62. Singh OP, Björkroth B, Masich S, Wieslander L, Daneholt B. 62.  1999. The intranuclear movement of Balbiani ring premessenger ribonucleoprotein particles. Exp. Cell Res. 251:135–46 [Google Scholar]
63. Stevens BJ, Swift H. 63.  1966. RNA transport from nucleus to cytoplasm in Chironomus salivary glands. J. Cell Biol. 31:55–77 [Google Scholar]
64. Skoglund U, Andersson K, Strandberg B, Daneholt B. 64.  1986. Three-dimensional structure of a specific RNP particle established by electron microscope tomography. Nature 319:560–64 [Google Scholar]
65. Alexciev K, Wurtz T, Lönnroth A, Daneholt B. 65.  1993. The elementary RNP fiber—not the higher order structure—determines the all-or-none disintegration behaviour of Balbiani ring pre-messenger RNP particles upon RNase A treatment. Biol. Cell 77:165–72 [Google Scholar]
66. Siebrasse JP, Veith R, Dobay A, Leonhardt H, Daneholt B, Kubitscheck U. 66.  2008. Discontinuous movement of mRNP particles in nucleoplasmic regions devoid of chromatin. PNAS 105:20291–96 [Google Scholar]
67. Veith R, Sorkalla T, Baumgart E, Anzt J, Häberlein H. 67.  et al. 2010. Balbiani ring mRNPs diffuse through and bind to clusters of large intranuclear molecular structures. Biophys. J. 99:2676–85 [Google Scholar]
68. Miralles F, Öfverstedt LG, Sabri N, Aissouni Y, Hellman U. 68.  et al. 2000. Electron tomography reveals posttranscriptional binding of pre-mRNPs to specific fibers in the nucleoplasm. J. Cell Biol. 148:271–82 [Google Scholar]
69. Wurtz T, Lönnroth A, Ovchinnikov L, Skoglund U, Daneholt B. 69.  1990. Isolation and initial characterization of a specific premessenger ribonucleoprotein particle. PNAS 87:831–35 [Google Scholar]
70. Björk P, Jin SB, Singh OP, Persson JO, Hellman U, Wieslander L. 70.  2009. Specific combinations of SR proteins associate with single pre-messenger RNAs in vivo and contribute different functions. J. Cell Biol. 184:555–68 [Google Scholar]
71. Cheng H, Dufu K, Hsu JL, Dias A, Reed R. 71.  2006. Human mRNA export machinery recruited to the 5′-end of mRNA. Cell 127:899–905 [Google Scholar]
72. Siebrasse JP, Kaminsky T, Kubitscheck U. 72.  2012. Nuclear export of single native mRNA molecules observed by light sheet fluorescence microscopy. PNAS 109:9426–31 [Google Scholar]
73. Ma J, Liu Z, Michelotti N, Pitchiaya S, Veerapeneni R. 73.  et al. 2013. High-resolution three-dimensional mapping of mRNA export through the nuclear pore. Nat. Commun. 4:2414 [Google Scholar]
74. Kiseleva E, Goldberg MW, Daneholt B, Allen TD. 74.  1996. RNP export is mediated by structural reorganization of the nuclear pore basket. J. Mol. Biol. 260:304–11 [Google Scholar]
75. Soop T, Ivarsson B, Björkroth B, Fomproix N, Masich S. 75.  et al. 2005. Nup153 affects entry of messenger and ribosomal ribonucleoproteins into the nuclear basket during export. Mol. Biol. Cell 16:5610–20 [Google Scholar]
76. Mehlin H, Daneholt B, Skoglund U. 76.  1995. Structural interaction between the nuclear pore complex and a specific translocating RNP particle. J. Cell Biol. 129:1205–16 [Google Scholar]
77. Dworetzky SI, Feldherr CM. 77.  1988. Translocation of RNA-coated gold particles through the nuclear pores of oocytes. J. Cell Biol. 106:575–84 [Google Scholar]
78. Kiseleva E, Goldberg MW, Allen TD, Akey CW. 78.  1998. Active nuclear pore complexes in Chironomus: visualization of transporter configurations related to mRNP export. J. Cell Sci. 111:223–36 [Google Scholar]
79. Daneholt B. 79.  2001. Packaging and delivery of a genetic message. Chromosoma 110:173–85 [Google Scholar]
80. Björk P, Baurén G, Gelius B, Wrange Ö, Wieslander L. 80.  2003. The Chironomus tentans translation initiation factor eIF4H is present in the nucleus but does not bind to mRNA until the mRNA reaches the cytoplasmic perinuclear region. J. Cell Sci. 116:4521–32 [Google Scholar]
81. Lönn U. 81.  1978. Delayed flow-through cytoplasm of newly synthesized Balbiani ring 75S RNA. Cell 13:727–33 [Google Scholar]
82. Francke C, Edström JE, McDowall AW, Miller OL Jr. 82.  1983. Electron microscopic visualization of a discrete class of giant translation units in salivary gland cells of Chironomus tentans. EMBO J. 1:59–62 [Google Scholar]
83. Percipalle P, Zhao J, Pope B, Weeds A, Lindberg U, Daneholt B. 83.  2001. Actin bound to the heterogeneous nuclear ribonucleoprotein hrp36 is associated with Balbiani ring mRNA from the gene to polysomes. J. Cell Biol. 153:229–36 [Google Scholar]
84. Botelho SC, Tyagi A, Hessle W, Farrants AK, Visa N. 84.  2008. The association of Brahma with the Balbiani ring 1 gene of Chironomus tentans studied by immunoelectron microscopy and chromatin immunoprecipitation. Insect Mol. Biol. 5:505–13 [Google Scholar]
85. Tyagi A, Ryme J, Brodin D, Östlund-Farrants AK, Visa N. 85.  2009. SWI/SNF associates with nascent pre-mRNPs and regulates alternative pre-mRNA processing. PLOS Genet. 5:e1000470 [Google Scholar]
86. Alzhanova-Ericsson AT, Sun X, Visa N, Kiseleva E, Wurtz T, Daneholt B. 86.  1996. A protein of the SR family of splicing factors binds extensively to exonic Balbiani ring pre-mRNA and accompanies the RNA from the gene to the nuclear pore. Genes Dev. 10:2881–93 [Google Scholar]
87. Björk P, Wetterberg-Strandh I, Baurén G, Wieslander L. 87.  2006. Chironomus tentans–repressor splicing factor represses SR protein function locally on pre-mRNA exons and is displaced at correct splice sites. Mol. Biol. Cell 1:32–42 [Google Scholar]
88. Sun X, Alzhanova-Ericsson AT, Visa N, Aissouni Y, Zhao J, Daneholt B. 88.  1998. The hrp23 protein in the Balbiani ring pre-mRNP particles is released just before or at the binding of the particles to the nuclear pore complex. J. Cell Biol. 142:1181–93 [Google Scholar]
89. Visa N, Alzhanova-Ericsson AT, Sun X, Kiseleva E, Björkroth B. 89.  et al. 1996. A pre-mRNA-binding protein accompanies the RNA from the gene through the nuclear pores and into polysomes. Cell 84:253–64 [Google Scholar]
90. Kiesler E, Miralles F, Visa N. 90.  2002. HEL/UAP56 binds cotranscriptionally to the Balbiani ring pre-mRNA in an intron-independent manner and accompanies the BR mRNP to the nuclear pore. Curr. Biol. 12:859–62 [Google Scholar]
91. Kiesler E, Hase ME, Brodin D, Visa N. 91.  2005. Hrp59, an hnRNP M protein in Chironomus and Drosophila, binds to exonic splicing enhancers and is required for expression of a subset of mRNAs. J. Cell Biol. 168:1013–25 [Google Scholar]
92. Zhao J, Jin SB, Björkroth B, Wieslander L, Daneholt B. 92.  2002. The mRNA export factor Dbp5 is associated with Balbiani ring mRNP from gene to cytoplasm. EMBO J. 21:1177–87 [Google Scholar]
93. Zhao J, Jin SB, Wieslander L. 93.  2004. CRM1 and Ran are present but a NES–CRM1–RanGTP complex is not required in Balbiani ring mRNP particles from the gene to the cytoplasm. J. Cell Sci. 117:1553–66 [Google Scholar]
94. Sabri N, Visa N. 94.  2000. The Ct-RAE1 protein interacts with Balbiani ring RNP particles at the nuclear pore. RNA 6:1597–609 [Google Scholar]
95. Nashchekin D, Zhao J, Visa N, Daneholt B. 95.  2006. A novel Ded1-like RNA helicase interacts with the Y-box protein CtYB-1 in nuclear mRNP particles and in polysomes. J. Biol. Chem. 281:14263–72 [Google Scholar]
96. Soop T, Nashchekin D, Zhao J, Sun X, Alzhanova-Ericsson AT. 96.  et al. 2003. A p50-like Y-box protein with a putative translational role becomes associated with pre-mRNA concomitant with transcription. J. Cell Sci. 116:1493–503 [Google Scholar]
97. Nashchekin D, Masich S, Soop T, Kukalev A, Kovrigina E. 97.  et al. 2007. Two splicing isoforms of the Y-box protein ctYB-1 appear on the same mRNA molecule. FEBS J. 274:202–11 [Google Scholar]
98. Sun X, Zhao J, Kylberg K, Soop T, Palka K. 98.  et al. 2004. Conspicuous accumulation of transcription elongation repressor hrp130/CA150 on the intron-rich Balbiani ring 3 gene. Chromosoma 113:244–57 [Google Scholar]
99. Mehlin H, Daneholt B, Skoglund U. 99.  1992. Translocation of a specific premessenger ribonucleoprotein particle through the nuclear pore studied with electron microscope tomography. Cell 69:605–13 [Google Scholar]