RNA-dependent genome processing during nuclear differentiation: The model systems of stichotrichous ciliates

Epigenomics

Volumn 5, Issue 2, 2013, Pages 229-236

  Fuhrmann, Gloria ^a   Swart, Estienne ^b   Nowacki, Mariusz ^b   Lipps, Hans J ^a  

^a Institute of Virology and Microbiology   (Germany)

^b UNIVERSITY OF BERN   (Switzerland)

Author keywords

ciliated protozoa; gene amplification; gene processing; nuclear differentiation

Indexed keywords

RIBOSOME RNA; SMALL NUCLEAR RNA; UNTRANSLATED RNA;

ARTICLE; BIOLOGICAL MODEL; CELL DIFFERENTIATION; DNA SEQUENCE; GENE AMPLIFICATION; GENE DOSAGE; GENE REARRANGEMENT; GENOME ANALYSIS; HISTONE MODIFICATION; MACRONUCLEUS; MICRONUCLEUS; NONHUMAN; OXYTRICHA; POLYTENE CHROMOSOME; PRIORITY JOURNAL; REGULATORY MECHANISM; REPRODUCTION; STICHOTRICHIA; STYLONYCHIA;

CELL NUCLEUS; CILIOPHORA; EPIGENESIS, GENETIC; GENE AMPLIFICATION; GENE DOSAGE; GENOMIC IMPRINTING; MACRONUCLEUS; MODELS, BIOLOGICAL; OXYTRICHA; RNA, SMALL NUCLEOLAR;

CILIOPHORA; MYXOZOA; OXYTRICHA; STYLONYCHIA;

EID: 84876136283     PISSN: 17501911     EISSN: 1750192X     Source Type: Journal    
DOI: 10.2217/epi.13.15     Document Type: Article

References (54)

1. Farazi TA, Juranek SA, Tuschl T. The growing catalog of small RNAs and their association with distinct Argonaute/Piwi family members. Development 135(7), 1201-1214 (2008). (Pubitemid 351622465)
2. Magistri M, Faghihi MA, St Laurent G 3rd, Wahlestedt C. Regulation of chromatin structure by long noncoding RNAs: focus on natural antisense transcripts. Trends Genet. 28(8), 389-396 (2012).
3. Wang KC, Chang HY. Molecular mechanisms of long noncoding RNAs. Mol. Cell 43(6), 904-914 (2011).
4. Swart EC, Bracht JR, Magrini V et al. The Oxytricha trifallax macronuclear genome: a complex eukaryotic genome with 16,000 tiny chromosomes. PLoS Biology 11(1), e1001473 (2013).
5. Prescott DM. The DNA of ciliated protozoa. Microbiol. Rev. 58(2), 233-267 (1994).
6. Heyse G, Jonsson F, Chang WJ, Lipps HJ. RNA-dependent control of gene amplification. Proc. Natl Acad. Sci. USA 107(51), 22134-22139 (2010).
7. Tausta SL, Turner LR, Buckley LK, Klobutcher LA. High fidelity developmental excision of Tec1 transposons and internal eliminated sequences in Euplotes crassus. Nucleic Acids Res. 19(12), 3229-3236 (1991). (Pubitemid 21912674)
8. Mollenbeck M, Zhou Y, Cavalcanti AR et al. The pathway to detangle a scrambled gene. PloS One 3(6), e2330 (2008).
9. Nowacki M, Haye JE, Fang W, Vijayan V, Landweber LF. RNA-mediated epigenetic regulation of DNA copy number. Proc. Natl Acad. Sci. USA 107(51), 22140-22144 (2010).
10. Denovan-Wright EM, Sankoff D, Spencer DF, Lee RW. Evolution of fragmented mitochondrial ribosomal RNA genes in Chlamydomonas. J. Mol. Evol. 42(4), 382-391 (1996). (Pubitemid 26154315)
11. Gillespie DE, Salazar NA, Rehkopf DH, Feagin JE. The fragmented mitochondrial ribosomal RNAs of Plasmodium falciparum have short A tails. Nucleic Acids Res. 27(11), 2416-2422 (1999). (Pubitemid 29245663)
12. Kairo A, Fairlamb AH, Gobright E, Nene V. A 7.1 kb linear DNA molecule of Theileria parva has scrambled rDNA sequences and open reading frames for mitochondrially encoded proteins. EMBO J. 13(4), 898-905 (1994). (Pubitemid 24057521)
13. Pavlakis GN, Jordan BR, Wurst RM, Vournakis JN. Sequence and secondary structure of Drosophila melanogaster 5.8S and 2S rRNAs and of the processing site between them. Nucleic Acids Res. 7(8), 2213-2238 (1979).
14. Spencer DF, Gray MW. Ribosomal RNA genes in Euglena gracilis mitochondrial DNA: fragmented genes in a seemingly fragmented genome. Mol. Genet. Genomics 285(1), 19-31 (2011).
15. Landweber LF. Genetics. Why genomes in pieces? Science 318(5849), 405-407 (2007).
16. Soma A, Onodera A, Sugahara J et al. Permuted tRNA genes expressed via a circular RNA intermediate in Cyanidioschyzon merolae. Science 318(5849), 450-453 (2007). (Pubitemid 47614530)
17. Robertson HM, Navik JA, Walden KK, Honegger HW. The bursicon gene in mosquitoes: an unusual example of mRNA trans-splicing. Genetics 176(2), 1351-1353 (2007). (Pubitemid 46961127)
18. Marande W, Burger G. Mitochondrial DNA as a genomic jigsaw puzzle. Science 318(5849), 415 (2007). (Pubitemid 47614519)
19. Manis JP, Tian M, Alt FW. Mechanism and control of class-switch recombination. Trends Immunol. 23(1), 31-39 (2002). (Pubitemid 34098959)
20. Bertoni L, Zoli W, Mucciolo E et al. Different genome organization in two new cell lines established from human gastric carcinoma. Cancer Genet. Cytogenet. 105(2), 152-159 (1998). (Pubitemid 28381630)
21. Bignell GR, Santarius T, Pole JC et al. Architectures of somatic genomic rearrangement in human cancer amplicons at sequence-level resolution. Genome Res. 17(9), 1296-1303 (2007). (Pubitemid 47360904)
22. Campbell PJ, Stephens PJ, Pleasance ED et al. Identification of somatically acquired rearrangements in cancer using genome-wide massively parallel paired-end sequencing. Nat. Genet. 40(6), 722-729 (2008). (Pubitemid 351748860)
23. Edwards SL, Brough R, Lord CJ et al. Resistance to therapy caused by intragenic deletion in BRCA2. Nature 451(7182), 1111-1115 (2008). (Pubitemid 351317441)
24. Li H, Wang J, Mor G, Sklar J. A neoplastic gene fusion mimics trans-splicing of RNAs in normal human cells. Science 321(5894), 1357-1361 (2008).
25. Lucito R, West J, Reiner A et al. Detecting gene copy number fluctuations in tumor cells by microarray analysis of genomic representations. Genome Res. 10(11), 1726-1736 (2000).
26. Stephens PJ, Greenman CD, Fu B et al. Massive genomic rearrangement acquired in a single catastrophic event during cancer development. Cell 144(1), 27-40 (2011).
27. Mochizuki K, Fine NA, Fujisawa T, Gorovsky MA. Analysis of a piwi-related gene implicates small RNAs in genome rearrangement in tetrahymena. Cell 110(6), 689-699 (2002). (Pubitemid 35283959)
28. Mochizuki K. DNA rearrangements directed by non-coding RNAs in ciliates. Wiley Interdiscip. Rev. RNA 1(3), 376-387 (2010).
29. Duharcourt S, Lepere G, Meyer E. Developmental genome rearrangements in ciliates: a natural genomic subtraction mediated by non-coding transcripts. Trends Genet. 25(8), 344-350 (2009).
30. Fang W, Wang X, Bracht JR, Nowacki M, Landweber LF. Piwi-interacting RNAs protect DNA against loss during Oxytricha genome rearrangement. Cell 151(6), 1243-1255 (2012).
31. Jonsson F, Postberg J, Lipps HJ. The unusual way to make a genetically active nucleus. DNA Cell Biol. 28(2), 71-78 (2009).
32. Zahler AM, Neeb ZT, Lin A, Katzman S. Mating of the stichotrichous ciliate Oxytricha trifallax induces production of a class of 27 nt small RNAs derived from the parental macronucleus. PloS One 7(8), e42371 (2012).
33. Juranek SA, Rupprecht S, Postberg J, Lipps HJ. snRNA and heterochromatin formation are involved in DNA excision during macronuclear development in stichotrichous ciliates. Eukaryot. Cell 4(11), 1934-1941 (2005). (Pubitemid 41636885)
34. Postberg J, Heyse K, Cremer M, Cremer T, Lipps HJ. Spatial and temporal plasticity of chromatin during programmed DNA-reorganization in Stylonychia macronuclear development. Epigenetics Chromatin 1(1), 3 (2008).
35. Meyer GF, Lipps HJ. Chromatin elimination in the hypotrichous ciliate Stylonychia mytilus. Chromosoma 77(3), 285-297 (1980). (Pubitemid 10132165)
36. Bracht JR, Perlman DH, Landweber LF. Cytosine methylation and hydroxymethylation mark DNA for elimination in Oxytricha trifallax. Genome Biol. 13(10), R99 (2012).
37. Juranek S, Wieden HJ, Lipps HJ. De novo cytosine methylation in the differentiating macronucleus of the stichotrichous ciliate Stylonychia lemnae. Nucleic Acids Res. 31(5), 1387-1391 (2003). (Pubitemid 36304899)
38. Prescott DM, Ehrenfeucht A, Rozenberg G. Template-guided recombination for IES elimination and unscrambling of genes in stichotrichous ciliates. J. Theor. Biol. 222(3), 323-330 (2003). (Pubitemid 36542824)
39. Nowacki M, Shetty K, Landweber LF. RNA-mediated epigenetic programming of genome rearrangements. Annu. Rev. Genomics Hum. Genet. 12, 367-389 (2011).
40. Nowacki M, Vijayan V, Zhou Y, Schotanus K, Doak TG, Landweber LF. RNA-mediated epigenetic programming of a genome-rearrangement pathway. Nature 451(7175), 153-158 (2008).
41. Tower J. Developmental gene amplification and origin regulation. Annu. Rev. Genet. 38, 273-304 (2004). (Pubitemid 40013730)
42. Heck MM, Spradling AC. Multiple replication origins are used during Drosophila chorion gene amplification. J. Cell Biol. 110(4), 903-914 (1990).
43. Hourcade D, Dressler D, Wolfson J. The amplification of ribosomal RNA genes involves a rolling circle intermediate. Proc. Natl Acad. Sci. USA 70(10), 2926-2930 (1973).
44. Trask BJ, Hamlin JL. Early dihydrofolate reductase gene amplification events in CHO cells usually occur on the same chromosome arm as the original locus. Genes Dev. 3(12A), 1913-1925 (1989). (Pubitemid 20023217)
45. Mohammad MM, Donti TR, Sebastian Yakisich J, Smith AG, Kapler GM. Tetrahymena ORC contains a ribosomal RNA fragment that participates in rDNA origin recognition. EMBO J. 26(24), 5048-5060 (2007). (Pubitemid 350261282)
46. Tanaka H, Yao MC. Palindromic gene amplification - an evolutionarily conserved role for DNA inverted repeats in the genome. Nat. Rev. Cancer 9(3), 216-224 (2009).
47. Xu K, Doak TG, Lipps HJ, Wang J, Swart EC, Chang WJ. Copy number variations of 11 macronuclear chromosomes and their gene expression in Oxytricha trifallax. Gene 505(1), 75-80 (2012).
48. Baird SE, Klobutcher LA. Differential DNA amplification and copy number control in the hypotrichous ciliate Euplotes crassus. J. Protozoology 38(2), 136-140 (1991).
49. Harper DS, Song K, Jahn CL. Overamplification of macronuclear linear DNA molecules during prolonged vegetative growth of Oxytricha nova. Gene 99(1), 55-61 (1991).
50. Duerr HP, Eichner M, Ammermann D. Modeling senescence in hypotrichous ciliates. Protist 155(1), 45-52 (2004). (Pubitemid 38503624)
51. Ammermann D, Steinbruck G, Von Berger L, Hennig W. The development of the macronucleus in the ciliated protozoan Stylonychia mytilus. Chromosoma 45(4), 401-429 (1974).
52. Mollenbeck M, Cavalcanti AR, Jonsson F, Lipps HJ, Landweber LF. Interconversion of germline-limited and somatic DNA in a scrambled gene. J. Mol. Evol. 63(1), 69-73 (2006). (Pubitemid 43992005)
53. Landweber LF, Kuo TC, Curtis EA. Evolution and assembly of an extremely scrambled gene. Proc. Natl Acad. Sci. USA 97(7), 3298-3303 (2000). (Pubitemid 30183296)
54. Mitcham JL, Prescott DM, Miller MK. The micronuclear gene encoding beta-telomere binding protein in Oxytricha nova. J. Eukaryot. Microbiol. 41(5), 478-480 (1994).