Ribosome-omics of the human ribosome

RNA

Volumn 20, Issue 7, 2014, Pages 1004-1013

  Gupta, Varun ^a   Warner, Jonathan R ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Alternative splicing; Pseudogene; Ribosomal protein; Ribosome; RNA seq

Indexed keywords

MESSENGER RNA; RIBOSOME PROTEIN; RNA; TRANSCRIPTOME;

AMBIGUITY; CONTROLLED STUDY; GENE MAPPING; HUMAN; HUMAN CELL; INTRON; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PSEUDOGENE; REVIEW; RIBOSOME; RNA ANALYSIS; RNA METABOLISM; RNA SEQUENCE; RNA SPLICING; RNA SYNTHESIS; STOICHIOMETRY; TISSUE SPECIFICITY; TURNOVER TIME;

ALTERNATIVE SPLICING; PSEUDOGENE; RIBOSOMAL PROTEIN; RIBOSOME; RNA-SEQ;

AMINO ACID SEQUENCE; CHROMOSOME MAPPING; GENOMICS; HUMANS; MOLECULAR SEQUENCE DATA; PROTEOME; RIBOSOMAL PROTEINS; RIBOSOMES; RNA SPLICING; RNA, MESSENGER; SEQUENCE ANALYSIS, RNA; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84902654766     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.043653.113     Document Type: Review

References (66)

1. Anger AM, Armache JP, Berninghausen O, Habeck M, Subklewe M, Wilson DN, Beckmann R. 2013. Structures of the human and Drosophila 80S ribosome. Nature 497: 80-85.
2. Babiano R, Badis G, Saveanu C, Namane A, Doyen A, Díaz-Quintana A, JacquierA, Fromont-Racine M,de la CruzJ.2013.Yeast ribosomal protein L7 and its homologue Rlp7 are simultaneously present at distinct sites on pre-60S ribosomal particles. Nucleic Acids Res 41: 9461-9470.
3. Balasubramanian S, Zheng D, Liu YJ, Fang G, Frankish A, Carriero N, Robilotto R, Cayting P, Gerstein M. 2009. Comparative analysis of processed ribosomal protein pseudogenes in four mammalian genomes. Genome Biol 10: R2.
4. Beck M, Schmidt A, Malmstroem J, Claassen M, Ori A, Szymborska A, Herzog F, Rinner O, Ellenberg J, Aebersold R. 2011. The quantitative proteome of a human cell line. Mol Syst Biol 7: 549.
5. Ben-Shem A, Garreau de Loubresse N, Melnikov S, Jenner L, Yusupova G, Yusupov M. 2011. The structure of the eukaryotic ribosome at 3.0 Å resolution. Science 334: 1524-1529.
6. Bolze A, Mahlaoui N, Byun M, Turner B, Trede N, Ellis SR, Abhyankar A, Itan Y, Patin E, Brebner S, et al. 2013. Ribosomal protein SA haploinsufficiency in humans with isolated congenital asplenia. Science 340: 976-978.
7. Brawand D, Soumillon M, Necsulea A, Julien P, Csárdi G, Harrigan P, Weier M, Liechti A, Aximu-Petri A, Kircher M, et al. 2011. The evolution of gene expression levels in mammalian organs. Nature 478: 343-348.
8. Charneski CA, Hurst LD. 2013. Positively charged residues are the major determinants of ribosomal velocity. PLoS Biol 11: e1001508.
9. Chen R, Mias GI, Li-Pook-Than J, Jiang L, Lam HY, Chen R, Miriami E, Karczewski KJ, Hariharan M, Dewey FE, et al. 2012. Personal omics profiling reveals dynamic molecular and medical phenotypes. Cell 148: 1293-1307.
10. Cuccurese M, Russo G, Russo A, Pietropaolo C. 2005. Alternative splicing and nonsense-mediated mRNA decay regulate mammalian ribosomal gene expression. Nucleic Acids Res 33: 5965-5977.
11. Djebali S, Davis CA, Merkel A, Dobin A, Lassmann T, Mortazavi A, Tanzer A, Lagarde J, Lin W, Schlesinger F, et al. 2012. Landscape of transcription in human cells. Nature 489: 101-108.
12. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR. 2013. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29: 15-21.
13. Draptchinskaia N, Gustavsson P, Andersson B, Pettersson M, Willig TN, Dianzani I, Ball S, Tchernia G, Klar J, Matsson H, et al. 1999. The gene encoding ribosomal protein S19 is mutated in Diamond-Blackfan anaemia. Nat Genet 21: 169-175.
14. Dunbar DA, Dragon F, Lee SJ, Baserga SJ. 2000. A nucleolar protein related to ribosomal protein L7 is required for an early step in large ribosomal subunit biogenesis. Proc Natl Acad Sci 97: 13027-13032.
15. - syndrome gene by RNA interference screen. Nature 451: 335-339.
16. The ENCODE Project Consortium. 2011. A user's guide to the encyclopedia of DNA elements (ENCODE). PLoS Biol 9: e1001046.
17. Farrar JE, Vlachos A, Atsidaftos E, Carlson-Donohoe H, Markello TC, Arceci RJ, Ellis SR, Lipton JM, Bodine DM. 2011. Ribosomal protein gene deletions in Diamond-Blackfan anemia. Blood 118: 6943-6951.
18. Geiger T, Wehner A, Schaab C, Cox J, Mann M. 2012. Comparative proteomic analysis of eleven common cell lines reveals ubiquitous but varying expression of most proteins. Mol Cell Proteomics 11: M111.014050.
19. Gonzalo P, Reboud JP. 2003. The puzzling lateral flexible stalk of the ribosome. Biol Cell 95: 179-193.
20. Gu W, Zhou T, Wilke CO. 2010. A universal trend of reduced mRNA stability near the translation-initiation site in prokaryotes and eukaryotes. PLoS Comput Biol 6: e1000664.
21. Hinnebusch AG, Lorsch JR. 2012. The mechanism of eukaryotic translation initiation: new insights and challenges. Cold Spring Harb Perspect Biol 4: a011544.
22. Hsieh AC, Liu Y, Edlind MP, Ingolia NT, Janes MR, Sher A, Shi EY, Stumpf CR, Christensen C, Bonham MJ, et al. 2012. The translational landscape of mTOR signalling steers cancer initiation and metastasis. Nature 485: 55-61.
23. Jenner L, Melnikov S, Garreau de Loubresse N, Ben-Shem A, Iskakova M, Urzhumtsev A, Meskauskas A, Dinman J, Yusupova G, Yusupov M. 2012. Crystal structure of the 80S yeast ribosome. Curr Opin Struct Biol 22: 759-767.
24. Jouffe C, Cretenet G, Symul L, Martin E, Atger F, Naef F, Gachon F. 2013. The circadian clock coordinates ribosome biogenesis. PLoS Biol 11: e1001455.
25. Kappel L, Loibl M, Zisser G, Klein I, Fruhmann G, Gruber C, Unterweger S, Rechberger G, Pertschy B, Bergler H. 2012. Rlp24 activates the AAA-ATPase Drg1 to initiate cytoplasmic pre-60S maturation. J Cell Biol 199: 771-782.
26. Kondrashov N, Pusic A, Stumpf CR, Shimizu K, Hsieh AC, Xue S, Ishijima J, Shiroishi T, Barna M. 2011. Ribosome-mediated specificity in Hox mRNA translation and vertebrate tissue patterning. Cell 145: 383-397.
27. Lam YW, Lamond AI, Mann M, Andersen JS. 2007. Analysis of nucleolar protein dynamics reveals the nuclear degradation of ribosomal proteins. Curr Biol 17: 749-760.
28. Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods 9: 357-359.
29. Lee AS, Burdeinick-Kerr R, Whelan SP. 2013. A ribosome-specialized translation initiation pathway is required for cap-dependent translation of vesicular stomatitis virus mRNAs. Proc Natl Acad Sci 110: 324-329.
30. Li W, Yang W, Wang XJ. 2013. Pseudogenes: pseudo or real functional elements? J Genet Genomics 40: 171-177.
31. Lianoglou S, Garg V, Yang JL, Leslie CS, Mayr C. 2013. Ubiquitously transcribed genes use alternative polyadenylation to achieve tissuespecific expression. Genes Dev 27: 2380-2396.
32. Llorian M, Smith CW. 2011. Decoding muscle alternative splicing. Curr Opin Genet Dev 21: 380-387.
33. Loayza-Puch F, Drost J, Rooijers K, Lopes R, Elkon R, Agami R. 2013. p53 induces transcriptional and translational programs to suppress cell proliferation and growth. Genome Biol 14: R32.
34. Lopes AM, Miguel RN, Sargent CA, Ellis PJ, Amorim A, Affara NA. 2010. The human RPS4 paralogue on Yq11.223 encodes a structurally conserved ribosomal protein and is preferentially expressed during spermatogenesis. BMC Mol Biol 11: 33.
35. Mahoney SJ, Dempsey JM, Blenis J. 2009. Cell signaling in protein synthesis ribosome biogenesis and translation initiation and elongation. Prog Mol Biol Transl Sci 90: 53-107.
36. McIlwain DR, Pan Q, Reilly PT, Elia AJ, McCracken S, Wakeham AC, Itie-Youten A, Blencowe BJ, Mak TW. 2010. Smg1 is required for embryogenesis and regulates diverse genes via alternative splicing coupled to nonsense-mediated mRNA decay. Proc Natl Acad Sci 107: 12186-12191.
37. Meyuhas O, Dreazen A. 2009. Ribosomal protein S6 kinase from TOP mRNAs to cell size. Prog Mol Biol Transl Sci 90: 109-153.
38. Muro EM, Mah N, Andrade-Navarro MA. 2011. Functional evidence of post-transcriptional regulation by pseudogenes. Biochimie 93: 1916-1921.
39. Nagaraj N, Wisniewski JR, Geiger T, Cox J, Kircher M, Kelso J, Paabo S, Mann M. 2011. Deep proteome and transcriptome mapping of a human cancer cell line. Mol Syst Biol 7: 548.
40. Nakao A, Yoshihama M, Kenmochi N. 2004. RPG: the Ribosomal Protein Gene database. Nucleic Acids Res 32: D168-D170.
41. O'Leary MN, Schreiber KH, Zhang Y, Duc AC, Rao S, Hale JS, Academia EC, Shah SR, Morton JF, Holstein CA, et al. 2013. The ribosomal protein Rpl22 controls ribosome composition by directly repressing expression of its own paralog, Rpl22l1. PLoS Genet 9: e1003708.
42. Pan Q, Shai O, Lee LJ, Frey BJ, Blencowe BJ. 2008. Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat Genet 40: 1413-1415.
43. Raiser DM, Narla A, Ebert BL. 2014. The emerging importance of ribosomal dysfunction in the pathogenesis of hematologic disorders. Leuk Lymphoma 55: 491-500.
44. Seila AC, Core LJ, Lis JT, Sharp PA. 2009. Divergent transcription: a new feature of active promoters. Cell Cycle 8: 2557-2564.
45. Stadanlick JE, Zhang Z, Lee SY, Hemann M, Biery M, Carleton MO, Zambetti GP, Anderson SJ, Oravecz T, Wiest DL. 2011. Developmental arrest of T cells in Rpl22-deficient mice is dependent upon multiple p53 effectors. J Immunol 187: 664-675.
46. Steffen KK, McCormick MA, Pham KM, MacKay VL, Delaney JR, Murakami CJ, Kaeberlein M, Kennedy BK. 2012. Ribosome deficiency protects against ER stress in Saccharomyces cerevisiae. Genetics 191: 107-118.
47. Stumpf CR, Moreno MV, Olshen AB, Taylor BS, Ruggero D. 2013. The translational landscape of the mammalian cell cycle. Mol Cell 52: 574-582.
48. Sugihara Y, Honda H, Iida T, Morinaga T, Hino S, Okajima T, Matsuda T, Nadano D. 2010. Proteomic analysis of rodent ribosomes revealed heterogeneity including ribosomal proteins L10-like, L22-like 1, and L39-like. J Proteome Res 9: 1351-1366.
49. Sun Z, Asmann YW, Kalari KR, Bot B, Eckel-Passow JE, Baker TR, Carr JM, Khrebtukova I, Luo S, Zhang L, et al. 2011. Integrated analysis of gene expression, CpG island methylation, and gene copy number in breast cancer cells by deep sequencing. PLoS One 6:e17490.
50. Tafforeau L, Zorbas C, Langhendries JL, Mullineux ST, Stamatopoulou V, Mullier R, Wacheul L, Lafontaine DL. 2013. The complexity of human ribosome biogenesis revealed by systematic nucleolar screening of pre-rRNA processing factors. Mol Cell 51: 539-551.
51. Thomson E, Ferreira-Cerca S, Hurt E. 2013. Eukaryotic ribosome biogenesis at a glance. J Cell Sci 126: 4815-4821.
52. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. 2010. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28: 511-515.
53. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L. 2012. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7: 562-578.
54. Uechi T, Tanaka T, Kenmochi N. 2001. A complete map of the human ribosomal protein genes: assignment of 80 genes to the cytogenetic map and implications for human disorders. Genomics 72: 223-230.
55. Vallot C, Huret C, Lesecque Y, Resch A, Oudrhiri N, Bennaceur-Griscelli A, Duret L, Rougeulle C. 2013. XACT, a long noncoding transcript coating the active X chromosome in human pluripotent cells. Nat Genet 45: 239-241.
56. Vlatković N, Boyd MT, Rubbi CP. 2014. Nucleolar control of p53: a cellular Achilles' heel and a target for cancer therapy. Cell Mol Life Sci 71: 771-791.
57. Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, Mayr C, Kingsmore SF, Schroth GP, Burge CB. 2008. Alternative isoform regulation in human tissue transcriptomes. Nature 456: 470-476.
58. Warner JR, McIntosh KB. 2009. How common are extra-ribosomal functions of ribosomal proteins? Mol Cell 34: 3-11.
59. Weischenfeldt J, Waage J, Tian G, Zhao J, Damgaard I, Jakobsen JS, Kristiansen K, Krogh A, Wang J, Porse BT. 2012. Mammalian tissues defective in nonsense-mediated mRNA decay display highly aberrant splicing patterns. Genome Biol 13: R35.
60. Woolford JL Jr, Baserga SJ. 2013. Ribosome biogenesis in the yeast Saccharomyces cerevisiae. Genetics 195: 643-681.
61. Wu TD, Nacu S. 2010. Fast and SNP-tolerant detection of complex variants and splicing in short reads. Bioinformatics 26: 873-881.
62. Wu X, Sharp PA. 2013. Divergent transcription: a driving force for new gene origination? Cell 155: 990-996.
63. Xue S, Barna M. 2012. Specialized ribosomes: a new frontier in gene regulation and organismal biology. Nat Rev Mol Cell Biol 13: 355-369.
64. Yu X,Warner JR. 2001. Expression of a micro-protein. J Biol Chem 276: 33821-33825.
65. Zhang Y, Duc AC, Rao S, Sun XL, Bilbee AN, Rhodes M, Li Q, Kappes DJ, Rhodes J, Wiest DL. 2013. Control of hematopoietic stem cell emergence by antagonistic functions of ribosomal protein paralogs. Dev Cell 24: 411-425.
66. Zheng D, Frankish A, Baertsch R, Kapranov P, Reymond A, Choo SW, Lu Y, Denoeud F, Antonarakis SE, Snyder M, et al. 2007. Pseudogenes in the ENCODE regions: consensus annotation, analysis of transcription, and evolution. Genome Res 17: 839-851.