Publikationsserver der Universitätsbibliothek Marburg

Titel:Small RNA-guided processes in the hyperthermophilic methanogen Methanopyrus kandleri
Autor:Su, Andreas A. H.
Weitere Beteiligte: Randau, Lennart (Dr.)
URN: urn:nbn:de:hebis:04-z2014-04826
DDC: Biowissenschaften, Biologie
Titel (trans.):Von kleinen RNAs geleitete Prozesse im hyperthermophilen Methanogen Mathanopyrus kandleri


CRISPR-Cas, kleine RNAs, kleine RNAs, CRISPR-Cas

In this thesis, a combination of RNAseq, computational and biochemical methods was applied to analyze processes that use small RNAs (sRNAs) as guide molecules at extreme temperatures. Here, the hyperthermophilic archaeon Methanopyrus kandleri, which grows at temperatures of up to 110°C, was used as a model organism. The genome of M. kandleri harbors two CRISPR-Cas systems that use CRISPR RNA (crRNA) as guide molecules to target foreign nucleic acids. RNAseq analysis revealed a high abundance and processing of crRNAs in M. kandleri that indicated that CRISPR-Cas systems are highly active at extreme temperatures. Furthermore, the crystal structure of the CRISPR-associated protein Csm3 was solved in collaboration with Prof. Dr. Elena Conti (MPI Martinsried). Csm3 was found to bind crRNAs and was shown to function as the crRNA-binding backbone protein in type III-A CRISPR-Cas interference complexes. A recently discovered nucleic acid-guided mechanism uses prokaryotic Argonaute (pAgo) proteins. In M. kandleri, a pAgo protein was found to be encoded within a potential operon of CRISPR-associated genes and the analysis of recombinant pAgo protein production revealed a high toxicity in Escherichia coli that might correlate with its potential defense function against plasmid DNA. Methylation of rRNA is regulated by a different sRNA-guided mechanism that utilizes C/D box sRNAs to target a ribonucleoprotein complex to the rRNA methylation site. In M. kandleri, a record number of 126 C/D box sRNAs were detected by RNAseq analysis and indicate an increased potential for rRNA methylation reactions. Furthermore, most of the C/D box sRNAs were detected as circular molecules. Taken together, the circularization of C/D box sRNAs and the high requirement for rRNA methylation are suggested to be adaptations to the hyperthermophilic lifestyle of M. kandleri. Finally, RNAseq analyses were used to identify tRNA precursors in M. kandleri that feature a unique C-to-U editing reaction of base 8. The occurrence of this editing event was used to deduce the order of tRNA processing steps in a non-compartmentalized cell, indicating that termini truncation precedes intron removal and editing.

Bibliographie / References

  1. Siomi, M. C., Sato, K., Pezic, D., Aravin, A. A. (2011). PIWI-interacting small RNAs: the vanguard of genome defence. Nature Reviews. Molecular Cell Biology, 12, 246-58.
  2. Palmer, J. R., Baltrus, T., Reeve, J. N., Daniels, C. J. (1992). Transfer RNA genes from the hyperthermophilic Archaeon, Methanopyrus kandleri. Biochimica et Biophysica Acta, 1132, 315-8.
  3. Zhu, X., Ye, K. (2012). Crystal structure of Cmr2 suggests a nucleotide cyclase-related enzyme in type III CRISPR-Cas systems. FEBS Letters, 586, 939-45.
  4. Osawa, T., Inanaga, H., Numata, T. (2013). Crystal structure of the Cmr2-Cmr3 subcomplex in the CRISPR-Cas RNA silencing effector complex. Journal of Molecular Biology, 425, 3811-23.
  5. Yuan, Y.-R., Pei, Y., Ma, J.-B., Kuryavyi, V., Zhadina, M., Meister, G., Patel, D. J. (2005). Crystal structure of A. aeolicus argonaute, a site-specific DNA-guided endoribonuclease, provides insights into RISC-mediated mRNA cleavage. Molecular Cell, 19, 405-19.
  6. Wiedenheft, B., Zhou, K., Jinek, M., Coyle, S. M., Ma, W., Doudna, J. A. (2009). Structural basis for DNase activity of a conserved protein implicated in CRISPR-mediated genome defense. Structure, 17, 904-12.
  7. Forterre, P. (2006). DNA topoisomerase V: a new fold of mysterious origin. Trends in Biotechnology, 24, 245-7.
  8. Kowalak, J. A., Dalluge, J. J., Mccloskey, J. A., Stetters, K. (1994). The Role of Posttranscriptional Modification in Stabilization of Transfer RNA from Hyperthermophiles. Biochemistry, 33, 7869-76.
  9. Meister, G. (2013). Argonaute proteins: functional insights and emerging roles. Nature Reviews. Genetics, 14, 447-59.
  10. Samson, J. E., Magadán, A. H., Sabri, M., Moineau, S. (2013). Revenge of the phages: defeating bacterial defences. Nature Reviews. Microbiology, 11, 675-87.
  11. Van der Oost, J., Westra, E. R., Jackson, R. N., Wiedenheft, B. (2014). Unraveling the structural and mechanistic basis of CRISPR-Cas systems. Nature Reviews. Microbiology, 12, 479-92.
  12. Sheng, G., Zhao, H., Wang, J., Rao, Y., Tian, W., Swarts, D. C., van der Oost, J. (2014). Structure- based cleavage mechanism of Thermus thermophilus Argonaute DNA guide strand-mediated DNA target cleavage. Proceedings of the National Academy of Sciences of the United States of America, 111, 652-7.
  13. Rashid, U. J., Paterok, D., Koglin, A., Gohlke, H., Piehler, J., Chen, J. C. H. (2007). Structure of Aquifex aeolicus argonaute highlights conformational flexibility of the PAZ domain as a potential regulator of RNA-induced silencing complex function. The Journal of Biological Chemistry, 282, 13824-32.
  14. Van Duijn, E., Barbu, I. M., Barendregt, A., Jore, M. M., Wiedenheft, B., Lundgren, M., Heck, A. J. R. (2012). Native tandem and ion mobility mass spectrometry highlight structural and modular similarities in clustered-regularly-interspaced shot-palindromic-repeats (CRISPR)-associated protein complexes from Escherichia coli and Pseudomonas aeruginosa. Molecular & Cellular Proteomics, 11, 1430-41.
  15. Kehr, S., Bartschat, S., Stadler, P. F., Tafer, H. (2011). PLEXY: efficient target prediction for box C/D snoRNAs. Bioinformatics, 27, 279-80.
  16. Lowe, T.M., Eddy, S.R. (1997). tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Research, 25, 955-64.
  17. Rozhdestvensky, T. S. (2003). Binding of L7Ae protein to the K-turn of archaeal snoRNAs: a shared RNA binding motif for C/D and H/ACA box snoRNAs in Archaea. Nucleic Acids Research, 31, 869-77.
  18. Grissa, I., Vergnaud, G., Pourcel, C. (2007). CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Research, 35, 52-7.
  19. Chan, P. P., Lowe, T. M. (2009). GtRNAdb: a database of transfer RNA genes detected in genomic sequence. Nucleic Acids Research, 37, 93-7.
  20. Carbonell, A., Flores, R., Gago, S. (2011). Trans-cleaving hammerhead ribozymes with tertiary stabilizing motifs: in vitro and in vivo activity against a structured viroid RNA. Nucleic Acids Research, 39, 2432-44.
  21. Danan, M., Schwartz, S., Edelheit, S., Sorek, R. (2012). Transcriptome-wide discovery of circular RNAs in Archaea. Nucleic Acids Research, 40, 3131-42.
  22. Richter, H., Zoephel, J., Schermuly, J., Maticzka, D., Backofen, R., Randau, L. (2012). Characterization of CRISPR RNA processing in Clostridium thermocellum and Methanococcus maripaludis. Nucleic Acids Research, 40, 9887-96.
  23. Makarova, K. S., Wolf, Y. I., Koonin, E. V. (2013). Comparative genomics of defense systems in archaea and bacteria. Nucleic Acids Research, 41, 4360-77.
  24. Su, A. A. H., Tripp, V., Randau, L. (2013). RNA-Seq analyses reveal the order of tRNA processing events and the maturation of C/D box and CRISPR RNAs in the hyperthermophile Methanopyrus kandleri. Nucleic Acids Research, 41, 6250-8.
  25. Carte, J., Wang, R., Li, H., Terns, R. M., Terns, M. P. (2008). Cas6 is an endoribonuclease that generates guide RNAs for invader defense in prokaryotes. Genes & Development, 22, 3489-96.
  26. Marblestone, J. G., Edavettal, S. C., Lim, Y., Lim, P., Zuo, X. U. N., Butt, T. R. (2006). Comparison of SUMO fusion technology with traditional gene fusion systems : Enhanced expression and solubility with SUMO. Protein Science, 15, 182-9.
  27. Juranek, S., Eban, T., Altuvia, Y., Brown, M., Morozov, P., Tuschl, T., Margalit, H. (2012). A genome-wide view of the expression and processing patterns of Thermus thermophilus HB8 CRISPR RNAs. RNA, 18, 783-94.
  28. Garside, E. L., Schellenberg, M. J., Gesner, E. M., Bonanno, J. B., Sauder, J. M., Burley, S. K., MacMillan, A. M. (2012). Cas5d processes pre-crRNA and is a member of a larger family of CRISPR RNA endonucleases. RNA, 18, 2020-8.
  29. Jore, M. M., Lundgren, M., van Duijn, E., Bultema, J. B., Westra, E. R., Waghmare, S. P., Brouns, S. J. J. (2011). Structural basis for CRISPR RNA-guided DNA recognition by Cascade. Nature Structural & Molecular Biology, 18, 529-36.
  30. Swarts, D. C., Jore, M. M., Westra, E. R., Zhu, Y., Janssen, J. H., Snijders, A. P., van der Oost, J. (2014). DNA-guided DNA interference by a prokaryotic Argonaute. Nature, 507, 258-61.
  31. Mole, L. D. B., Sabatier, P. (2001). Small nucleolar RNA-guided post-transcriptional modification of cellular RNAs. The EMBO Journal, 20, 3617-22.
  32. Wagner, M., Berkner, S., Ajon, M., Driessen, A. J. M., Lipps, G., Albers, S.-V. (2009). Expanding and understanding the genetic toolbox of the hyperthermophilic genus Sulfolobus. Biochemical Society Transactions, 37, 97-101.
  33. Randau, L. (2012). RNA processing in the minimal organism Nanoarchaeum equitans. Genome Biology, 13, 63.
  34. Song, J. J., Smith, S. K., Hannon, G. J., Joshua-Tor, L. (2004). Crystal structure of Argonaute and its implications for RISC slicer activity. Science, 305, 1434-7.
  35. Liu, J., Carmell, M. A, Rivas, F. V, Marsden, C. G., Thomson, J. M., Song, J. J., Hannon, G. J. (2004). Argonaute2 is the catalytic engine of mammalian RNAi. Science, 305, 1437-41.
  36. Rivas, F. V, Tolia, N. H., Song, J. J., Aragon, J. P., Liu, J., Hannon, G. J., Joshua-Tor, L. (2005). Purified Argonaute2 and an siRNA form recombinant human RISC. Nature Structural & Molecular Biology, 12, 340-9.
  37. Hutvagner, G., Simard, M. J. (2008). Argonaute proteins: key players in RNA silencing. Nature Reviews Molecular Cell Biology, 9, 22-32.
  38. Peters, L., Meister, G. (2007). Argonaute proteins: mediators of RNA silencing. Molecular Cell, 26, 611-23.
  39. Ma, J. B., Yuan, Y. R., Meister, G., Pei, Y., Tuschl, T., Patel, D. J. (2005). Structural basis for 5'-end- specific recognition of guide RNA by the A. fulgidus Piwi protein. Nature, 434, 666-70.
  40. Maris, C., Dominguez, C., Allain, F. H. T. (2005). The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression. The FEBS Journal, 272, 2118-31.
  41. Shima, S., Hérault, D. A., Berkessel, A., Thauer, R. K. (1998). Activation and thermostabilization effects of cyclic 2,3-diphosphoglycerate on enzymes from the hyperthermophilic Methanopyrus kandleri. Archaeal Microbiology, 170, 469-72.
  42. Mojica, F. J. M., Díez-Villaseñor, C., García-Martínez, J., Soria, E. (2005). Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. Journal of Molecular Evolution, 60, 174-82.
  43. Huber, R., Kurr, M., Jannasch, H. W., Stetter, K. O. (1989). A novel group of abyssal methanogenic archaebacteria (Methanopyrus) growing at 110°C. Nature, 342, 833-4.
  44. Fribourg, S., Gatfield, D., Izaurralde, E., Conti, E. (2003). A novel mode of RBD-protein recognition in the Y14-Mago complex. Nature Structural Biology, 10, 433-9.
  45. Makarova, K. S., Grishin, N. V, Shabalina, S. A, Wolf, Y. I., Koonin, E. V. (2006). A putative RNA- interference-based immune system in prokaryotes: computational analysis of the predicted enzymatic machinery, functional analogies with eukaryotic RNAi, and hypothetical mechanisms of action. Biology Direct, 1, 7.
  46. Jinek, M., Doudna, J. A. (2009). A three-dimensional view of the molecular machinery of RNA interference. Nature, 457, 405-12.
  47. Olovnikov, I., Chan, K., Sachidanandam, R., Newman, D., Aravin, A. (2013). Bacterial Argonaute Samples the Transcriptome to Identify Foreign DNA. Molecular Cell, 51, 594-605.
  48. Labrie, S. J., Samson, J. E., Moineau, S. (2010). Bacteriophage resistance mechanisms. Nature Reviews. Microbiology, 8, 317-27.
  49. Mojica FJ, Díez-Villaseñor C, Soria E, Juez G. (2000). Biological significance of a family of regularly spaced repeats in the genomes of Archaea, Bacteria and mitochondria. Molecular Microbiology, 36, 244-6.
  50. Nuñez, J. K., Kranzusch, P. J., Noeske, J., Wright, A. V, Davies, C. W., Doudna, J. A. (2014). Cas1- Cas2 complex formation mediates spacer acquisition during CRISPR-Cas adaptive immunity. Nature Structural & Molecular Biology, 21, 528-34.
  51. Hochstrasser, M. L., Taylor, D. W., Bhat, P., Guegler, C. K., Sternberg, S. H., Nogales, E., Doudna, J. A. (2014). CasA mediates Cas3-catalyzed target degradation during CRISPR RNA-guided interference. Proceedings of the National Academy of Sciences of the United States of America, 111, 6618-23.
  52. Takai, K., Nakamura, K., Toki, T., Tsunogai, U., Miyazaki, M., Miyazaki, J., Horikoshi, K. (2008). Cell proliferation at 122°C and isotopically heavy CH 4 production by a hyperthermophilic methanogen under high-pressure cultivation. Proceedings of the National Academy of Sciences of the United States of America, 105, 10949-54.
  53. Koonin, E. V, Makarova, K. S. (2013). CRISPR-Cas: evolution of an RNA-based adaptive immunity system in prokaryotes. RNA Biology, 10, 679-86.
  54. Nowotny, M., Gaidamakov, S. A, Crouch, R. J., Yang, W. (2005). Crystal structures of RNase H bound to an RNA/DNA hybrid: substrate specificity and metal-dependent catalysis. Cell, 121, 1005-16.
  55. Slesarev A. I., Stetter K. O., Lake J. A., Gellert M., Krah R., Kozyavkin S. A. (1993). DNA topoisomerase V is a relative of eukaryotic topoisomerase I from a hyperthermophilic prokaryote. Nature, 364, 735-7.
  56. Puttaraju, M., Been, M. D. (1995). Generation of nuclease resistant circular RNA decoys for HIV- Tat and HIV-Rev by autocatalytic splicing. Nucleic Acids Symposium Series, 1995, 49-51.
  57. Haas, E. S., Daniels, C. J., Reeve, J. N. (1989). Genes encoding 5s rRNA and tRNAs in the extremely thermophilic thermus fewidus archaebacterium. Gene, 77, 253-63.
  58. Hatoum-Aslan, A., Maniv, I., Samai, P., Marraffini, L. A. (2014). Genetic characterization of antiplasmid immunity through a type III-A CRISPR-Cas system. Journal of Bacteriology, 196, 310-7.
  59. Plagens, A., Tripp, V., Daume, M., Sharma, K., Klingl, A., Hrle, A., Conti, E., Urlaub,H., Randau, L. (2014). In vitro assembly and activity of an archaeal CRISPR-Cas type I-A Cascade interference complex. Nucleic Acids Research, 42, 5125-38.
  60. Suttle, C. A. (2007). Marine viruses, major players in the global ecosystem. Nature Reviews. Microbiology, 5, 801-12.
  61. Burggraf, S., Stetter, K. O., Rouviere, P., Woese, C. R. (1991). Methanopyrus kandleri: an archaeal methanogen unrelated to all other known methanogens. Systematic and Applied Microbiology, 14, 346-51.
  62. Sauerwald, A., Sitaramaiah, D., McCloskey, J. A, Söll, D., Crain, P. F. (2005). N6-Acetyladenosine: a new modified nucleoside from Methanopyrus kandleri tRNA. FEBS Letters, 579, 2807-10.
  63. Wiedenheft, B., Sternberg, S. H., Doudna, J. A. (2012). RNA-guided genetic silencing systems in bacteria and archaea. Nature, 482, 331-8.
  64. Hale, C. R., Zhao, P., Olson, S., Duff, M. O., Graveley, B. R., Wells, L., Terns, M. P. (2009). RNA- guided RNA cleavage by a CRISPR RNA-Cas protein complex. Cell, 139, 945-56.
  65. Lintner, N. G., Kerou, M., Brumfield, S. K., Graham, S., Liu, H., Naismith, J. H., Lawrence, C. M. (2011). Structural and functional characterization of an archaeal clustered regularly interspaced short palindromic repeat (CRISPR)-associated complex for antiviral defense (CASCADE). The Journal of Biological Chemistry, 286, 21643-56.
  66. Staals, R. H. J., Agari, Y., Maki-Yonekura, S., Zhu, Y., Taylor, D. W., van Duijn, E., Shinkai, A. (2013). Structure and activity of the RNA-targeting Type III-B CRISPR-Cas complex of Thermus thermophilus. Molecular Cell, 52, 135-45.
  67. Spilman, M., Cocozaki, A., Hale, C., Shao, Y., Ramia, N., Terns, R., Stagg, S. (2013). Structure of an RNA silencing complex of the CRISPR-Cas immune system. Molecular Cell, 52, 146-52.
  68. Cocozaki, A. I., Ramia, N. F., Shao, Y., Hale, C. R., Terns, R. M., Terns, M. P., Li, H. (2012). Structure of the Cmr2 subunit of the CRISPR-Cas RNA silencing complex. Structure, 20, 545-53.
  69. Wang, Y., Sheng, G., Juranek, S., Tuschl, T., Patel, D. J. (2008). Structure of the guide-strand- containing argonaute silencing complex. Nature, 456, 209-13.
  70. Wiedenheft, B., Lander, G. C., Zhou, K., Jore, M. M., Brouns, S. J. J., van der Oost, J., Nogales, E. (2011). Structures of the RNA-guided surveillance complex from a bacterial immune system. Nature, 477, 486-9.
  71. Mat, W. K., Xue, H., Wong, J. T. (2008) The genomics of LUCA. Frontiers in Bioscience, 13, 5605-13.
  72. Raabe, C. a, Hoe, C. H., Randau, G., Brosius, J., Tang, T. H., Rozhdestvensky, T. S. (2011). The rocks and shallows of deep RNA sequencing: Examples in the Vibrio cholerae RNome. RNA, 17, 1357-66.
  73. Sapranauskas, R., Gasiunas, G., Fremaux, C., Barrangou, R., Horvath, P., Siksnys, V. (2011). The Streptococcus thermophilus CRISPR/Cas system provides immunity in Escherichia coli. Nucleic Acids Research, 39, 9275-82.
  74. Jansen, R., Embden, J. D. A. Van, Gaastra, W., Schouls, L. M. (2002). Identification of genes that are associated with DNA repeats in prokaryotes. Molecular Microbiology, 43, 1565-75.
  75. Fechter, P., The, A., Giege, R. (2000). Identity of tRNA for Yeast Tyrosyl-tRNA Synthetase : Tyrosylation Is More Sensitive to Identity Nucleotides than to Structural Features. Biochemistry, 39, 1725-33.
  76. Marck, C., Grosjean, H. (2003). Identification of BHB splicing motifs in intron-containing tRNAs from 18 archaea : evolutionary implications Identification of BHB splicing motifs in intron- containing tRNAs from 18 archaea : evolutionary implications. RNA, 9, 1516-31.
  77. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., Read, R. J. (2007). Phaser crystallographic software. Journal of Applied Crystallography, 40, 658 -74.
  78. Emsley, P., Cowtan, K. (2002). Coot: model-building tools for molecular graphics. Acta Crystallographica, 60, 2126-32.
  79. Yamaguchi, Y., Park, J.-H., Inouye, M. (2011). Toxin-antitoxin systems in bacteria and archaea. Annual Review of Genetics, 45, 61-79.
  80. Makarova, K. S., Wolf, Y. I., van der Oost, J., Koonin, E. V. (2009). Prokaryotic homologs of Argonaute proteins are predicted to function as key components of a novel system of defense against mobile genetic elements. Biology Direct, 4, 29.
  81. Makarova, K. S., Aravin, L., Wolf, Y. I., Koonin, E. V. (2011). Unification of Cas protein families and a simple scenario for the origin and evolution of CRISPR-Cas systems. Biology Direct, 6, 38.
  82. Grissa, I., Vergnaud, G., Pourcel, C. (2007). The CRISPRdb database and tools to display CRISPRs and to generate dictionaries of spacers and repeats. BMC Bioinformatics, 8, 172.
  83. Scholz, J., Besir, H., Strasser, C., Suppmann, S. (2013). A new method to customize protein expression vectors for fast, efficient and background free parallel cloning. BMC Biotechnology, 13, 12.
  84. Findeiss, S., Langenberger, D., Stadler, P. F., Hoffmann, S. (2011). Traces of post-transcriptional RNA modifications in deep sequencing data. The Journal of Biological Chemistry, 392, 305-13.
  85. Mulepati, S., Bailey, S. (2011). Structural and biochemical analysis of nuclease domain of clustered regularly interspaced short palindromic repeat (CRISPR)-associated protein 3 (Cas3). The Journal of Biological Chemistry, 286, 31896-903.
  86. Kadlec, J., Izaurralde, E., Cusack, S. (2004). The structural basis for the interaction between nonsense-mediated mRNA decay factors UPF2 and UPF3. Nature Structural & Molecular Biology, 11, 330-7.
  87. Hatoum-Aslan, A., Samai, P., Maniv, I., Jiang, W., Marraffini, L. A. (2013). A ruler protein in a complex for antiviral defense determines the length of small interfering CRISPR RNAs. The Journal of Biological Chemistry, 288, 27888-97.
  88. Slesarev, A. I., Mezhevaya, K. V, Makarova, K. S., Polushin, N. N., Shcherbinina, O. V, Shakhova, V. V, Kozyavkin, S. A. (2002). The complete genome of hyperthermophile Methanopyrus kandleri AV19 and monophyly of archaeal methanogens. Proceedings of the National Academy of Sciences of the United States of America, 99, 4644-9.
  89. Klein, D. J., Schmeing, T. M., Moore, P. B., Steitz, T. A. (2001). The kink-turn : a new RNA secondary structure motif. The EMBO Journal, 20, 4214-21.
  90. Yoshihisa, T., Yunoki-esaki, K., Ohshima, C., Tanaka, N., Endo, T. (2003). Possibility of cytoplasmic pre-tRNA splicing : the yeast tRNA splicing endonuclease mainly localizes on the mitochondria. Molecular Biology of the Cell, 14, 3266-79.
  91. Randau, L., Söll, D. (2008). Transfer RNA genes in pieces. EMBO Reports, 9, 623-8.
  92. Marraffini, L. A., Sontheimer, E. J. (2008). CRISPR Interference Limits Horizontal Targeting DNA, Science, 322, 1843-5.
  93. Shen, A., Lupardus, P. J., Morell, M., Ponder, E. L., Sadaghiani, A. M., Garcia, K. C., Bogyo, M. (2009). Simplified, enhanced protein purification using an inducible, autoprocessing enzyme tag. PloS One, 4, e8119.
  94. Randau, L., Stanley, B. J., Kohlway, A., Mechta, S., Xiong, Y., Söll, D. (2009). A cytidine deaminase edits C to U in transfer RNAs in Archaea. Science, 324, 657-9.
  95. Marraffini, L. A., Sontheimer, E. J. (2010). CRISPR interference: RNA-directed adaptive immunity in bacteria and archaea. Nature Reviews. Genetics, 11, 181-90.
  96. Parker, J. S., Roe, S. M., Barford, D. (2005). Structural insights into mRNA recognition from a PIWI domain-siRNA guide complex. Nature Letters, 434, 663-6.
  97. Deltcheva, E., Chylinski, K., Sharma, C. M., Gonzales, K., Chao, Y., Pirzada, Z. A, Charpentier, E. (2011). CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature, 471, 602-7.
  98. RNA-guided complex from a bacterial immune system enhances target recognition through seed sequence interactions. Proceedings of the National Academy of Sciences, 108, 15010.
  99. Wang, R., Preamplume, G., Terns, M. P., Terns, R. M., Li, H. (2011). Interaction of the Cas6 riboendonuclease with CRISPR RNAs: recognition and cleavage. Structure, 19, 257-64.
  100. Joshua-Tor, L., Hannon, G. J. (2011). Ancestral roles of small RNAs: an Ago-centric perspective. Cold Spring Harbor Perspectives in Biology, 3, 3772.
  101. Hatoum-Aslan, A., Maniv, I., Marraffini, L. A. (2011). Mature clustered, regularly interspaced, short palindromic repeats RNA (crRNA) length is measured by a ruler mechanism anchored at the precursor processing site. Proceedings of the National Academy of Sciences of the United States of America, 108, 21218-22.
  102. Salzman, J., Gawad, C., Wang, P. L., Lacayo, N., Brown, P. O. (2012). Circular RNAs are the predominant transcript isoform from hundreds of human genes in diverse cell types. PloS One, 7, e30733.
  103. Hale, C. R., Majumdar, S., Elmore, J., Pfister, N., Compton, M., Olson, S., Terns, M. P. (2012). Essential features and rational design of CRISPR RNAs that function with the Cas RAMP module complex to cleave RNAs. Molecular Cell, 45, 292-302.
  104. Makarova, K. S., Haft, D. H., Barrangou, R., Brouns, S. J. J., Charpentier, E., Horvath, P., Koonin, E. V. (2011). Evolution and classification of the CRISPR-Cas systems. Nature Reviews. Microbiology, 9, 467-77.
  105. Zhang, J., Rouillon, C., Kerou, M., Reeks, J., Brugger, K., Graham, S., White, M. F. (2012). Structure and mechanism of the CMR complex for CRISPR-mediated antiviral immunity. Molecular Cell, 45, 303-13.
  106. Elkayam, E., Kuhn, C.-D., Tocilj, A., Haase, A. D., Greene, E. M., Hannon, G. J., Joshua-Tor, L. (2012). The structure of human argonaute-2 in complex with miR-20a. Cell, 150, 100-10.
  107. Nam, K. H., Haitjema, C., Liu, X., Ding, F., Wang, H., DeLisa, M. P., Ke, A. (2012). Cas5d protein processes pre-crRNA and assembles into a cascade-like interference complex in subtype I- C/Dvulg CRISPR-Cas system. Structure, 20, 1574-84.
  108. Reeks, J., Naismith, J. H., White, M. F. (2013). CRISPR interference: a structural perspective. The Biochemical Journal, 453, 155-66.
  109. Rouillon, C., Zhou, M., Zhang, J., Politis, A., Beilsten-Edmands, V., Cannone, G., White, M. F. (2013). Structure of the CRISPR interference complex CSM reveals key similarities with cascade. Molecular Cell, 52, 124-34.
  110. Nakanishi, K., Weinberg, D. E., Bartel, D. P., Patel, D. J. (2012). Structure of yeast Argonaute with guide RNA. Nature, 486, 368-74.
  111. Hrle, A., Su, A. A. H., Ebert, J., Benda, C., Randau, L., Conti, E. (2013). Structure and RNA-binding properties of the type III-A CRISPR-associated protein Csm3. RNA Biology, 10, 1670-8.
  112. Zander, A., Holzmeister, P., Klose, D., Tinnefeld, P., Grohmann, D. (2014). Single-molecule FRET supports the two-state model of Argonaute action. RNA Biology, 11, 45-56.
  113. Krah, R., Kozyavkin, S. A., Slesarevt, A. I., Gellert, M. (1996). A two-subunit type I DNA topoisomerase (reverse gyrase) from an extreme hyperthermophile, Proceedings of the National Academy of Sciences of the United States of America, 93, 106-10.
  114. Hur, J. K., Olovnikov, I., Aravin, A. A. (2014). Prokaryotic Argonautes defend genomes against invasive DNA. Trends in Biochemical Sciences, 39, 257-9.
  115. Starostina, N. G., Marshburn, S., Johnson, L. S., Eddy, S. R., Terns, R. M., Terns, M. P. (2004). Circular box C/D RNAs in Pyrococcus furiosus. Proceedings of the National Academy of Sciences of the United States of America, 101, 14097-101.
  116. Lowe, T. M. (1999). A Computational Screen for Methylation Guide snoRNAs in Yeast. Science, 283, 1168-71.
  117. Omer, A. D. (2000). Homologs of Small Nucleolar RNAs in Archaea. Science, 288, 517-22.
  118. Haurwitz, R. E., Jinek, M., Wiedenheft, B., Zhou, K., Doudna, J. A. (2010). Sequence-and structure- specific RNA processing by a CRISPR endonuclease. Science, 329, 1355-8.
  119. Giacalone, M., Gentile, A., Lovitt, B., Berkley, N., Gunderson, C., Surber, M. (2006). Toxic protein expression in Escherichia coli using a rhamnose-based tightly regulated and tunable promoter system. BioTechniques, 40, 355-64.
  120. Yip, W. S. V., Vincent, N. G., Baserga, S. J. (2013). Ribonucleoproteins in archaeal pre-rRNA processing and modification. Archaea, 2013, 614735.
  121. Malakhov, M. P., Mattern, M. R., Malakhova, O. A, Drinker, M., Weeks, S. D., Butt, T. R. (2004). SUMO fusions and SUMO-specific protease for efficient expression and purification of proteins. Journal of Structural and Functional Genomics, 5, 75-86.
  122. Sharma, C. M., Hoffmann, S., Darfeuille, F., Reignier, J., Findeiss, S., Sittka, A., Vogel, J. (2010). The primary transcriptome of the major human pathogen Helicobacter pylori. Nature, 464, 250-5.
  123. Ketting, R. F. (2011). The many faces of RNAi. Developmental Cell, 20, 148-61.

* Das Dokument ist im Internet frei zugänglich - Hinweise zu den Nutzungsrechten