Analysis of two domains with novel RNA-processing activities throws light on the complex evolution of ribosomal RNA biogenesis

Frontiers in Genetics

Volumn 5, Issue NOV, 2014, Pages

  Burroughs, A Maxwell ^a   Aravind, L ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CHAPERONE; DTWD1; DTWD2; RIBONUCLEASE; RIBOSOME RNA; RNA 18S; TRANSFER RNA; TSR3; UNCLASSIFIED DRUG;

ARABIDOPSIS THALIANA; ARTICLE; BIOGENESIS; CHLAMYDIACEAE; ENZYME ACTIVITY; GENE FUSION; GENE SEQUENCE; GENETIC ASSOCIATION; GIARDIA; MATURATION; NONHUMAN; NOSEMA BOMBYCIS; OSTREOCOCCUS; OSTREOCOCCUS TAURUS; PLANCTOMYCETES; PROTEIN ANALYSIS; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEOBACTERIA; PROTOCHLAMYDIA AMOEBOPHILA; RNA PROCESSING; SPIROCHETE; VERRUCOMICROBIA;

BACTERIA (MICROORGANISMS); EUKARYOTA;

EID: 84917696052     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2014.00424     Document Type: Article

References (90)

1. Mullineux ST, Lafontaine DL: Mapping the cleavage sites on mammalian pre-rRNAs: where do we stand? Biochimie 2012, 94:1521-1532.
2. Deutscher MP: Maturation and degradation of ribosomal RNA in bacteria. Progress in molecular biology and translational science 2009, 85:369-391.
3. Yip WS, Vincent NG, Baserga SJ: Ribonucleoproteins in archaeal pre-rRNA processing and modification. Archaea 2013, 2013:614735.
4. Kressler D, Hurt E, Bassler J: Driving ribosome assembly. Biochimica et biophysica acta 2010, 1803:673-683.
5. Panse VG, Johnson AW: Maturation of eukaryotic ribosomes: acquisition of functionality. Trends in biochemical sciences 2010, 35:260-266.
6. Lafontaine DL, Tollervey D: The function and synthesis of ribosomes. Nature reviews Molecular cell biology 2001, 2:514-520.
7. Fromont-Racine M, Senger B, Saveanu C, Fasiolo F: Ribosome assembly in eukaryotes. Gene 2003, 313:17-42.
8. Bellemer C, Chabosseau P, Gallardo F, Gleizes PE, Stahl G: Genetic interactions show the importance of rRNA modification machinery for the role of Rps15p during ribosome biogenesis in S. cerevisiae. PloS one 2010, 5:e10472.
9. Li Z, Lee I, Moradi E, Hung NJ, Johnson AW, Marcotte EM: Rational extension of the ribosome biogenesis pathway using network-guided genetics. PLoS biology 2009, 7:e1000213.
10. Lamanna AC, Karbstein K: Nob1 binds the single-stranded cleavage site D at the 3'-end of 18S rRNA with its PIN domain. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:14259-14264.
11. Stevens A, Hsu CL, Isham KR, Larimer FW: Fragments of the internal transcribed spacer 1 of pre-rRNA accumulate in Saccharomyces cerevisiae lacking 5'----3' exoribonuclease 1. Journal of bacteriology 1991, 173:7024-7028.
12. Wang M, Pestov DG: 5'-end surveillance by Xrn2 acts as a shared mechanism for mammalian pre-rRNA maturation and decay. Nucleic acids research 2011, 39:1811-1822.
13. Lindahl L, Bommankanti A, Li X, Hayden L, Jones A, Khan M, Oni T, Zengel JM: RNase MRP is required for entry of 35S precursor rRNA into the canonical processing pathway. RNA 2009, 15:1407-1416.
14. Morello LG, Hesling C, Coltri PP, Castilho BA, Rimokh R, Zanchin NI: The NIP7 protein is required for accurate pre-rRNA processing in human cells. Nucleic acids research 2011, 39:648-665.
15. Carron C, O'Donohue MF, Choesmel V, Faubladier M, Gleizes PE: Analysis of two human pre-ribosomal factors, bystin and hTsr1, highlights differences in evolution of ribosome biogenesis between yeast and mammals. Nucleic acids research 2011, 39:280-291.
16. Zemp I, Wandrey F, Rao S, Ashiono C, Wyler E, Montellese C, Kutay U: CK1delta and CK1epsilon are components of human 40S subunit precursors required for cytoplasmic 40S maturation. Journal of cell science 2014, 127:1242-1253.
17. Widmann B, Wandrey F, Badertscher L, Wyler E, Pfannstiel J, Zemp I, Kutay U: The kinase activity of human Rio1 is required for final steps of cytoplasmic maturation of 40S subunits. Molecular biology of the cell 2012, 23:22-35.
18. Lafontaine D, Vandenhaute J, Tollervey D: The 18S rRNA dimethylase Dim1p is required for pre-ribosomal RNA processing in yeast. Genes & development 1995, 9:2470-2481.
19. Loc'h J, Blaud M, Rety S, Lebaron S, Deschamps P, Bareille J, Jombart J, Robert-Paganin J, Delbos L, Chardon F, et al: RNA mimicry by the fap7 adenylate kinase in ribosome biogenesis. PLoS biology 2014, 12:e1001860.
20. Gelperin D, Horton L, Beckman J, Hensold J, Lemmon SK: Bms1p, a novel GTP-binding protein, and the related Tsr1p are required for distinct steps of 40S ribosome biogenesis in yeast. RNA 2001, 7:1268-1283.
21. Armengaud J, Dedieu A, Solques O, Pellequer JL, Quemeneur E: Deciphering structure and topology of conserved COG2042 orphan proteins. BMC structural biology 2005, 5:3.
22. Owens GP, Hahn WE, Cohen JJ: Identification of mRNAs associated with programmed cell death in immature thymocytes. Molecular and cellular biology 1991, 11:4177-4188.
23. Baron BW, Hyjek E, Gladstone B, Thirman MJ, Baron JM: PDCD2, a protein whose expression is repressed by BCL6, induces apoptosis in human cells by activation of the caspase cascade. Blood cells, molecules & diseases 2010, 45:169-175.
24. Ni Nyoman AD, Luder CG: Apoptosis-like cell death pathways in the unicellular parasite Toxoplasma gondii following treatment with apoptosis inducers and chemotherapeutic agents: a proof-of-concept study. Apoptosis: an international journal on programmed cell death 2013, 18:664-680.
25. Barboza N, Minakhina S, Medina DJ, Balsara B, Greenwood S, Huzzy L, Rabson AB, Steward R, Schaar DG: PDCD2 functions in cancer cell proliferation and predicts relapsed leukemia. Cancer biology & therapy 2013, 14:546-555.
26. Baron BW, Zeleznik-Le N, Baron MJ, Theisler C, Huo D, Krasowski MD, Thirman MJ, Baron RM, Baron JM: Repression of the PDCD2 gene by BCL6 and the implications for the pathogenesis of human B and T cell lymphomas. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:7449-7454.
27. Chen Q, Yan C, Yan Q, Feng L, Chen J, Qian K: The novel MGC13096 protein is correlated with proliferation. Cell biochemistry and function 2008, 26:141-145.
28. Minakhina S, Druzhinina M, Steward R: Zfrp8, the Drosophila ortholog of PDCD2, functions in lymph gland development and controls cell proliferation. Development 2007, 134:2387-2396.
29. Kokorina NA, Granier CJ, Zakharkin SO, Davis S, Rabson AB, Sabaawy HE: PDCD2 knockdown inhibits erythroid but not megakaryocytic lineage differentiation of human hematopoietic stem/progenitor cells. Experimental hematology 2012, 40:1028-1042 e1023.
30. Mu W, Munroe RJ, Barker AK, Schimenti JC: PDCD2 is essential for inner cell mass development and embryonic stem cell maintenance. Developmental biology 2010, 347:279-288.
31. Kramer J, Granier CJ, Davis S, Piso K, Hand J, Rabson AB, Sabaawy HE: PDCD2 controls hematopoietic stem cell differentiation during development. Stem cells and development 2013, 22:58-72.
32. Minakhina S, Changela N, Steward R: Zfrp8/PDCD2 is required in ovarian stem cells and interacts with the piRNA pathway machinery. Development 2014, 141:259-268.
33. Chen Q, Yan CQ, Liu FJ, Tong J, Miao SL, Chen JP: Overexpression of the PDCD2-like gene results in inhibited TNF-alpha production in activated Daudi cells. Human immunology 2008, 69:259-265.
34. Fukae J, Sato S, Shiba K, Sato K, Mori H, Sharp PA, Mizuno Y, Hattori N: Programmed cell death-2 isoform1 is ubiquitinated by parkin and increased in the substantia nigra of patients with autosomal recessive Parkinson's disease. FEBS letters 2009, 583:521-525.
35. Zhang L, Gough J, Christmas D, Mattey DL, Richards SC, Main J, Enlander D, Honeybourne D, Ayres JG, Nutt DJ, Kerr JR: Microbial infections in eight genomic subtypes of chronic fatigue syndrome/myalgic encephalomyelitis. Journal of clinical pathology 2010, 63:156-164.
36. Kaushik N, Fear D, Richards SC, McDermott CR, Nuwaysir EF, Kellam P, Harrison TJ, Wilkinson RJ, Tyrrell DA, Holgate ST, Kerr JR: Gene expression in peripheral blood mononuclear cells from patients with chronic fatigue syndrome. Journal of clinical pathology 2005, 58:826-832.
37. Wagner M, Horn M: The Planctomycetes, Verrucomicrobia, Chlamydiae and sister phyla comprise a superphylum with biotechnological and medical relevance. Current opinion in biotechnology 2006, 17:241-249.
38. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, et al: The Pfam protein families database. Nucleic acids research 2012, 40:D290-301.
39. Bisbal C, Martinand C, Silhol M, Lebleu B, Salehzada T: Cloning and characterization of a RNAse L inhibitor. A new component of the interferon-regulated 2-5A pathway. The Journal of biological chemistry 1995, 270:13308-13317.
40. Karcher A, Schele A, Hopfner KP: X-ray structure of the complete ABC enzyme ABCE1 from Pyrococcus abyssi. The Journal of biological chemistry 2008, 283:7962-7971.
41. Becker T, Franckenberg S, Wickles S, Shoemaker CJ, Anger AM, Armache JP, Sieber H, Ungewickell C, Berninghausen O, Daberkow I, et al: Structural basis of highly conserved ribosome recycling in eukaryotes and archaea. Nature 2012, 482:501-506.
42. Aravind L: Guilt by association: contextual information in genome analysis. Genome research 2000, 10:1074-1077.
43. Huynen M, Snel B, Lathe W, 3rd, Bork P: Predicting protein function by genomic context: quantitative evaluation and qualitative inferences. Genome research 2000, 10:1204-1210.
44. Wolf YI, Rogozin IB, Kondrashov AS, Koonin EV: Genome alignment, evolution of prokaryotic genome organization, and prediction of gene function using genomic context. Genome research 2001, 11:356-372.
45. Godin KS, Varani G: How arginine-rich domains coordinate mRNA maturation events. RNA biology 2007, 4:69-75.
46. Rajyaguru P, Parker R: RGG motif proteins: modulators of mRNA functional states. Cell Cycle 2012, 11:2594-2599.
47. Milkereit P, Gadal O, Podtelejnikov A, Trumtel S, Gas N, Petfalski E, Tollervey D, Mann M, Hurt E, Tschochner H: Maturation and intranuclear transport of pre-ribosomes requires Noc proteins. Cell 2001, 105:499-509.
48. Nissan TA, Bassler J, Petfalski E, Tollervey D, Hurt E: 60S pre-ribosome formation viewed from assembly in the nucleolus until export to the cytoplasm. The EMBO journal 2002, 21:5539-5547.
49. Edskes HK, Ohtake Y, Wickner RB: Mak21p of Saccharomyces cerevisiae, a homolog of human CAATT-binding protein, is essential for 60 S ribosomal subunit biogenesis. The Journal of biological chemistry 1998, 273:28912-28920.
50. Hierlmeier T, Merl J, Sauert M, Perez-Fernandez J, Schultz P, Bruckmann A, Hamperl S, Ohmayer U, Rachel R, Jacob A, et al: Rrp5p, Noc1p and Noc2p form a protein module which is part of early large ribosomal subunit precursors in S. cerevisiae. Nucleic acids research 2013, 41:1191-1210.
51. Du H, Rosbash M: The U1 snRNP protein U1C recognizes the 5' splice site in the absence of base pairing. Nature 2002, 419:86-90.
52. del Sol A, Fujihashi H, Amoros D, Nussinov R: Residue centrality, functionally important residues, and active site shape: analysis of enzyme and non-enzyme families. Protein science: a publication of the Protein Society 2006, 15:2120-2128.
53. Anantharaman V, Koonin EV, Aravind L: Comparative genomics and evolution of proteins involved in RNA metabolism. Nucleic acids research 2002, 30:1427-1464.
54. Montelione GT: The Protein Structure Initiative: achievements and visions for the future. F1000 biology reports 2012, 4:7.
55. Ramalho-Santos M, Yoon S, Matsuzaki Y, Mulligan RC, Melton DA: "Stemness": transcriptional profiling of embryonic and adult stem cells. Science 2002, 298:597-600.
56. Scarr RB, Sharp PA: PDCD2 is a negative regulator of HCF-1 (C1). Oncogene 2002, 21:5245-5254.
57. Burroughs AM, Iyer LM, Aravind L: Functional diversification of the RING finger and other binuclear treble clef domains in prokaryotes and the early evolution of the ubiquitin system. Molecular bioSystems 2011, 7:2261-2277.
58. Liu Y, Chen W, Gaudet J, Cheney MD, Roudaia L, Cierpicki T, Klet RC, Hartman K, Laue TM, Speck NA, Bushweller JH: Structural basis for recognition of SMRT/N-CoR by the MYND domain and its contribution to AML1/ETO's activity. Cancer cell 2007, 11:483-497.
59. Matthews JM, Bhati M, Lehtomaki E, Mansfield RE, Cubeddu L, Mackay JP: It takes two to tango: the structure and function of LIM, RING, PHD and MYND domains. Current pharmaceutical design 2009, 15:3681-3696.
60. Perederina A, Svetlov V, Vassylyeva MN, Tahirov TH, Yokoyama S, Artsimovitch I, Vassylyev DG: Regulation through the secondary channel--structural framework for ppGpp- DksA synergism during transcription. Cell 2004, 118:297-309.
61. Tehranchi AK, Blankschien MD, Zhang Y, Halliday JA, Srivatsan A, Peng J, Herman C, Wang JD: The transcription factor DksA prevents conflicts between DNA replication and transcription machinery. Cell 2010, 141:595-605.
62. Paul BJ, Barker MM, Ross W, Schneider DA, Webb C, Foster JW, Gourse RL: DksA: a critical component of the transcription initiation machinery that potentiates the regulation of rRNA promoters by ppGpp and the initiating NTP. Cell 2004, 118:311-322.
63. Blankschien MD, Potrykus K, Grace E, Choudhary A, Vinella D, Cashel M, Herman C: TraR, a homolog of a RNAP secondary channel interactor, modulates transcription. PLoS genetics 2009, 5:e1000345.
64. Satory D, Halliday JA, Sivaramakrishnan P, Lua RC, Herman C: Characterization of a novel RNA polymerase mutant that alters DksA activity. Journal of bacteriology 2013, 195:4187-4194.
65. Kedzierski L, Montgomery J, Curtis J, Handman E: Leucine-rich repeats in host-pathogen interactions. Archivum immunologiae et therapiae experimentalis 2004, 52:104-112.
66. Kobe B, Kajava AV: The leucine-rich repeat as a protein recognition motif. Current opinion in structural biology 2001, 11:725-732.
67. Zhang D, de Souza RF, Anantharaman V, Iyer LM, Aravind L: Polymorphic toxin systems: Comprehensive characterization of trafficking modes, processing, mechanisms of action, immunity and ecology using comparative genomics. Biology direct 2012, 7:18.
68. Zelensky AN, Gready JE: The C-type lectin-like domain superfamily. The FEBS journal 2005, 272:6179-6217.
69. Carlson BL, Ballister ER, Skordalakes E, King DS, Breidenbach MA, Gilmore SA, Berger JM, Bertozzi CR: Function and structure of a prokaryotic formylglycine-generating enzyme. The Journal of biological chemistry 2008, 283:20117-20125.
70. Iyer LM, Abhiman S, Maxwell Burroughs A, Aravind L: Amidoligases with ATP-grasp, glutamine synthetase-like and acetyltransferase-like domains: synthesis of novel metabolites and peptide modifications of proteins. Molecular bioSystems 2009, 5:1636-1660.
71. Mosavi LK, Cammett TJ, Desrosiers DC, Peng ZY: The ankyrin repeat as molecular architecture for protein recognition. Protein science: a publication of the Protein Society 2004, 13:1435-1448.
72. Gerloff DL, Woods NT, Farago AA, Monteiro AN: BRCT domains: A little more than kin, and less than kind. FEBS letters 2012, 586:2711-2716.
73. Leung CC, Glover JN: BRCT domains: easy as one, two, three. Cell Cycle 2011, 10:2461-2470.
74. Hassa PO, Haenni SS, Elser M, Hottiger MO: Nuclear ADP-ribosylation reactions in mammalian cells: where are we today and where are we going? Microbiology and molecular biology reviews: MMBR 2006, 70:789-829.
75. Citarelli M, Teotia S, Lamb RS: Evolutionary history of the poly(ADP-ribose) polymerase gene family in eukaryotes. BMC evolutionary biology 2010, 10:308.
76. Anantharaman V, Aravind L: The SHS2 module is a common structural theme in functionally diverse protein groups, like Rpb7p, FtsA, GyrI, and MTH1598/TM1083 superfamilies. Proteins 2004, 56:795-807.
77. Desai KK, Cheng CL, Bingman CA, Phillips GN, Jr., Raines RT: A tRNA splicing operon: Archease endows RtcB with dual GTP/ATP cofactor specificity and accelerates RNA ligation. Nucleic acids research 2014, 42:3931-3942.
78. Auxilien S, El Khadali F, Rasmussen A, Douthwaite S, Grosjean H: Archease from Pyrococcus abyssi improves substrate specificity and solubility of a tRNA m5C methyltransferase. The Journal of biological chemistry 2007, 282:18711-18721.
79. Fatica A, Tollervey D, Dlakic M: PIN domain of Nob1p is required for D-site cleavage in 20S pre-rRNA. RNA 2004, 10:1698-1701.
80. Schmitt ME, Clayton DA: Nuclear RNase MRP is required for correct processing of pre-5.8S rRNA in Saccharomyces cerevisiae. Molecular and cellular biology 1993, 13:7935-7941.
81. Oeffinger M, Zenklusen D, Ferguson A, Wei KE, El Hage A, Tollervey D, Chait BT, Singer RH, Rout MP: Rrp17p is a eukaryotic exonuclease required for 5' end processing of Pre-60S ribosomal RNA. Molecular cell 2009, 36:768-781.
82. Henry Y, Wood H, Morrissey JP, Petfalski E, Kearsey S, Tollervey D: The 5' end of yeast 5.8S rRNA is generated by exonucleases from an upstream cleavage site. The EMBO journal 1994, 13:2452-2463.
83. Rolland T, Neuveglise C, Sacerdot C, Dujon B: Insertion of horizontally transferred genes within conserved syntenic regions of yeast genomes. PloS one 2009, 4:e6515.
84. Jekely G: Origin of the nucleus and Ran-dependent transport to safeguard ribosome biogenesis in a chimeric cell. Biology direct 2008, 3:31.
85. Johnson AW, Lund E, Dahlberg J: Nuclear export of ribosomal subunits. Trends in biochemical sciences 2002, 27:580-585.
86. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic acids research 1997, 25:3389-3402.
87. Soding J, Biegert A, Lupas AN: The HHpred interactive server for protein homology detection and structure prediction. Nucleic acids research 2005, 33:W244-248.
88. Edgar RC: MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC bioinformatics 2004, 5:113.
89. Cuff JA, Clamp ME, Siddiqui AS, Finlay M, Barton GJ: JPred: a consensus secondary structure prediction server. Bioinformatics 1998, 14:892-893.
90. Holm L, Kaariainen S, Rosenstrom P, Schenkel A: Searching protein structure databases with DaliLite v.3. Bioinformatics 2008, 24:2780-2781.