5mrf › Citations

The structure of the yeast mitochondrial ribosome.

Desai N, Brown A, Amunts A, Ramakrishnan V
Science 355 528-531 (2017)
Related entries: 5mrc, 5mre

Cited: 89 times
EuropePMC logo PMID: 28154081

Abstract

Mitochondria have specialized ribosomes (mitoribosomes) dedicated to the expression of the genetic information encoded by their genomes. Here, using electron cryomicroscopy, we have determined the structure of the 75-component yeast mitoribosome to an overall resolution of 3.3 angstroms. The mitoribosomal small subunit has been built de novo and includes 15S ribosomal RNA (rRNA) and 34 proteins, including 14 without homologs in the evolutionarily related bacterial ribosome. Yeast-specific rRNA and protein elements, including the acquisition of a putatively active enzyme, give the mitoribosome a distinct architecture compared to the mammalian mitoribosome. At an expanded messenger RNA channel exit, there is a binding platform for translational activators that regulate translation in yeast but not mammalian mitochondria. The structure provides insights into the evolution and species-specific specialization of mitochondrial translation.

Articles - 5mrf mentioned but not cited (3)

  1. The structure of the yeast mitochondrial ribosome. Desai N, Brown A, Amunts A, Ramakrishnan V. Science 355 528-531 (2017)
  2. Measurement of atom resolvability in cryo-EM maps with Q-scores. Pintilie G, Zhang K, Su Z, Li S, Schmid MF, Chiu W. Nat Methods 17 328-334 (2020)
  3. Residue-wise local quality estimation for protein models from cryo-EM maps. Terashi G, Wang X, Maddhuri Venkata Subramaniya SR, Tesmer JJG, Kihara D. Nat Methods 19 1116-1125 (2022)


Reviews citing this publication (20)

  1. Does functional specialization of ribosomes really exist? Ferretti MB, Karbstein K. RNA 25 521-538 (2019)
  2. Structural and evolutionary insights into ribosomal RNA methylation. Sergiev PV, Aleksashin NA, Chugunova AA, Polikanov YS, Dontsova OA. Nat. Chem. Biol. 14 226-235 (2018)
  3. The Diseased Mitoribosome. Ferrari A, Del'Olio S, Barrientos A. FEBS Lett 595 1025-1061 (2021)
  4. Translation initiation in mammalian mitochondria- a prokaryotic perspective. Ayyub SA, Varshney U. RNA Biol 17 165-175 (2020)
  5. Emerging Roles of Mitochondrial Ribosomal Proteins in Plant Development. Robles P, Quesada V. Int J Mol Sci 18 (2017)
  6. Developments, applications, and prospects of cryo-electron microscopy. Benjin X, Ling L. Protein Sci 29 872-882 (2020)
  7. Epitranscriptomics of Mammalian Mitochondrial Ribosomal RNA. Laptev I, Dontsova O, Sergiev P. Cells 9 E2181 (2020)
  8. Structural Heterogeneities of the Ribosome: New Frontiers and Opportunities for Cryo-EM. Poitevin F, Kushner A, Li X, Dao Duc K. Molecules 25 E4262 (2020)
  9. Structure determination of group II introns. Wiryaman T, Toor N. Methods 125 10-15 (2017)
  10. Translational regulation in mycobacteria and its implications for pathogenicity. Sawyer EB, Grabowska AD, Cortes T. Nucleic Acids Res. 46 6950-6961 (2018)
  11. Activation of Yeast Mitochondrial Translation: Who Is in Charge? Derbikova KS, Levitsky SA, Chicherin IV, Vinogradova EN, Kamenski PA. Biochemistry Mosc. 83 87-97 (2018)
  12. An Update on Mitochondrial Ribosome Biology: The Plant Mitoribosome in the Spotlight. Tomal A, Kwasniak-Owczarek M, Janska H. Cells 8 (2019)
  13. High resolution single particle Cryo-EM refinement using JSPR. Sun C, Gonzalez B, Vago FS, Jiang W. Prog Biophys Mol Biol 160 37-42 (2021)
  14. Pathways to balance mitochondrial translation and protein import. Priesnitz C, Becker T. Genes Dev. 32 1285-1296 (2018)
  15. Ribosomal proteins: insight into molecular roles and functions in hepatocellular carcinoma. Xie X, Guo P, Yu H, Wang Y, Chen G. Oncogene 37 277-285 (2018)
  16. Constructive Neutral Evolution 20 Years Later. Muñoz-Gómez SA, Bilolikar G, Wideman JG, Geiler-Samerotte K. J Mol Evol (2021)
  17. Mechanisms and regulation of protein synthesis in mitochondria. Kummer E, Ban N. Nat Rev Mol Cell Biol (2021)
  18. Mechanisms of ribosome recycling in bacteria and mitochondria: a structural perspective. Seely SM, Gagnon MG. RNA Biol 19 662-677 (2022)
  19. Ribosome Specialization in Protozoa Parasites. Rodríguez-Almonacid CC, Kellogg MK, Karamyshev AL, Karamysheva ZN. Int J Mol Sci 24 7484 (2023)
  20. Types and Functions of Mitoribosome-Specific Ribosomal Proteins across Eukaryotes. Scaltsoyiannes V, Corre N, Waltz F, Giegé P. Int J Mol Sci 23 3474 (2022)

Articles citing this publication (66)

  1. Analysis of translating mitoribosome reveals functional characteristics of translation in mitochondria of fungi. Itoh Y, Naschberger A, Mortezaei N, Herrmann JM, Amunts A. Nat Commun 11 5187 (2020)
  2. Kinetics and Mechanism of Mammalian Mitochondrial Ribosome Assembly. Bogenhagen DF, Ostermeyer-Fay AG, Haley JD, Garcia-Diaz M. Cell Rep 22 1935-1944 (2018)
  3. The DEAD-box helicase Mss116 plays distinct roles in mitochondrial ribogenesis and mRNA-specific translation. De Silva D, Poliquin S, Zeng R, Zamudio-Ochoa A, Marrero N, Perez-Martinez X, Fontanesi F, Barrientos A. Nucleic Acids Res. 45 6628-6643 (2017)
  4. Complexome Profiling Reveals Association of PPR Proteins with Ribosomes in the Mitochondria of Plants. Rugen N, Straube H, Franken LE, Braun HP, Eubel H. Mol Cell Proteomics 18 1345-1362 (2019)
  5. Structural insights into species-specific features of the ribosome from the human pathogen Mycobacterium tuberculosis. Yang K, Chang JY, Cui Z, Li X, Meng R, Duan L, Thongchol J, Jakana J, Huwe CM, Sacchettini JC, Zhang J. Nucleic Acids Res. 45 10884-10894 (2017)
  6. Revising the Structural Diversity of Ribosomal Proteins Across the Three Domains of Life. Melnikov S, Manakongtreecheep K, Söll D. Mol. Biol. Evol. 35 1588-1598 (2018)
  7. Yeast Mitoribosome Large Subunit Assembly Proceeds by Hierarchical Incorporation of Protein Clusters and Modules on the Inner Membrane. Zeng R, Smith E, Barrientos A. Cell Metab. 27 645-656.e7 (2018)
  8. Cryo-EM structures of the 80S ribosomes from human parasites Trichomonas vaginalis and Toxoplasma gondii. Li Z, Guo Q, Zheng L, Ji Y, Xie YT, Lai DH, Lun ZR, Suo X, Gao N. Cell Res. 27 1275-1288 (2017)
  9. Integrating Rio1 activities discloses its nutrient-activated network in Saccharomyces cerevisiae. Iacovella MG, Bremang M, Basha O, Giacò L, Carotenuto W, Golfieri C, Szakal B, Dal Maschio M, Infantino V, Beznoussenko GV, Joseph CR, Visintin C, Mironov AA, Visintin R, Branzei D, Ferreira-Cerca S, Yeger-Lotem E, De Wulf P. Nucleic Acids Res. 46 7586-7611 (2018)
  10. A Case of Gene Fragmentation in Plant Mitochondria Fixed by the Selection of a Compensatory Restorer of Fertility-Like PPR Gene. Nguyen TT, Planchard N, Dahan J, Arnal N, Balzergue S, Benamar A, Bertin P, Brunaud V, Dargel-Graffin C, Macherel D, Martin-Magniette ML, Quadrado M, Namy O, Mireau H. Mol Biol Evol 38 3445-3458 (2021)
  11. An Unexpectedly Complex Mitoribosome in Andalucia godoyi, a Protist with the Most Bacteria-like Mitochondrial Genome. Valach M, Gonzalez Alcazar JA, Sarrasin M, Lang BF, Gray MW, Burger G. Mol Biol Evol 38 788-804 (2021)
  12. Ciliate mitoribosome illuminates evolutionary steps of mitochondrial translation. Tobiasson V, Amunts A. Elife 9 (2020)
  13. Evolutionary shift toward protein-based architecture in trypanosomal mitochondrial ribosomes. Ramrath DJF, Niemann M, Leibundgut M, Bieri P, Prange C, Horn EK, Leitner A, Boehringer D, Schneider A, Ban N. Science 362 (2018)
  14. OXPHOS deficiency activates global adaptation pathways to maintain mitochondrial membrane potential. Liu S, Liu S, He B, Li L, Li L, Wang J, Cai T, Chen S, Jiang H. EMBO Rep 22 e51606 (2021)
  15. Ribosome engineering reveals the importance of 5S rRNA autonomy for ribosome assembly. Huang S, Aleksashin NA, Loveland AB, Klepacki D, Reier K, Kefi A, Szal T, Remme J, Jaeger L, Vázquez-Laslop N, Korostelev AA, Mankin AS. Nat Commun 11 2900 (2020)
  16. Structures of Mycobacterium smegmatis 70S ribosomes in complex with HPF, tmRNA, and P-tRNA. Mishra S, Ahmed T, Tyagi A, Shi J, Bhushan S. Sci Rep 8 13587 (2018)
  17. TopMatch-web: pairwise matching of large assemblies of protein and nucleic acid chains in 3D. Wiederstein M, Sippl MJ. Nucleic Acids Res 48 W31-W35 (2020)
  18. Chromosome-level genome assembly and structural variant analysis of two laboratory yeast strains from the Peterhof Genetic Collection lineage. Barbitoff YA, Matveenko AG, Matiiv AB, Maksiutenko EM, Moskalenko SE, Drozdova PB, Polev DE, Beliavskaia AY, Danilov LG, Predeus AV, Zhouravleva GA. G3 (Bethesda) 11 jkab029 (2021)
  19. Elongational stalling activates mitoribosome-associated quality control. Desai N, Yang H, Chandrasekaran V, Kazi R, Minczuk M, Ramakrishnan V. Science 370 1105-1110 (2020)
  20. Genetic ablation of the mitoribosome in the malaria parasite Plasmodium falciparum sensitizes it to antimalarials that target mitochondrial functions. Ling L, Mulaka M, Munro J, Dass S, Mather MW, Riscoe MK, Llinás M, Zhou J, Ke H. J Biol Chem 295 7235-7248 (2020)
  21. How to build a ribosome from RNA fragments in Chlamydomonas mitochondria. Waltz F, Salinas-Giegé T, Englmeier R, Meichel H, Soufari H, Kuhn L, Pfeffer S, Förster F, Engel BD, Giegé P, Drouard L, Hashem Y. Nat Commun 12 7176 (2021)
  22. Mitochondrial dysfunction rapidly modulates the abundance and thermal stability of cellular proteins. Groh C, Haberkant P, Stein F, Filbeck S, Pfeffer S, Savitski MM, Boos F, Herrmann JM. Life Sci Alliance 6 e202201805 (2023)
  23. Mitochondrial ribosome bL34 mutants present diminished translation of cytochrome c oxidase subunits. Guedes-Monteiro RF, Ferreira-Junior JR, Bleicher L, Nóbrega FG, Barrientos A, Barros MH. Cell Biol. Int. 42 630-642 (2018)
  24. Mitoribosomal small subunit maturation involves formation of initiation-like complexes. Lenarčič T, Niemann M, Ramrath DJF, Calderaro S, Flügel T, Saurer M, Leibundgut M, Boehringer D, Prange C, Horn EK, Schneider A, Ban N. Proc Natl Acad Sci U S A 119 e2114710118 (2022)
  25. MrpL35, a mitospecific component of mitoribosomes, plays a key role in cytochrome c oxidase assembly. Box JM, Kaur J, Stuart RA. Mol. Biol. Cell 28 3489-3499 (2017)
  26. Small is big in Arabidopsis mitochondrial ribosome. Waltz F, Nguyen TT, Arrivé M, Bochler A, Chicher J, Hammann P, Kuhn L, Quadrado M, Mireau H, Hashem Y, Giegé P. Nat Plants 5 106-117 (2019)
  27. Structure of the mature kinetoplastids mitoribosome and insights into its large subunit biogenesis. Soufari H, Waltz F, Parrot C, Durrieu-Gaillard S, Bochler A, Kuhn L, Sissler M, Hashem Y. Proc Natl Acad Sci U S A 117 29851-29861 (2020)
  28. Structures of the human mitochondrial ribosome bound to EF-G1 reveal distinct features of mitochondrial translation elongation. Koripella RK, Sharma MR, Bhargava K, Datta PP, Kaushal PS, Keshavan P, Spremulli LL, Banavali NK, Agrawal RK. Nat Commun 11 3830 (2020)
  29. The draft nuclear genome sequence and predicted mitochondrial proteome of Andalucia godoyi, a protist with the most gene-rich and bacteria-like mitochondrial genome. Gray MW, Burger G, Derelle R, Klimeš V, Leger MM, Sarrasin M, Vlček Č, Roger AJ, Eliáš M, Lang BF. BMC Biol 18 22 (2020)
  30. The mitoribosome-specific protein mS38 is preferentially required for synthesis of cytochrome c oxidase subunits. Mays JN, Camacho-Villasana Y, Garcia-Villegas R, Perez-Martinez X, Barrientos A, Fontanesi F. Nucleic Acids Res. 47 5746-5760 (2019)
  31. The translational landscape of Arabidopsis mitochondria. Planchard N, Bertin P, Quadrado M, Dargel-Graffin C, Hatin I, Namy O, Mireau H. Nucleic Acids Res. 46 6218-6228 (2018)
  32. The yeast protein Mam33 functions in the assembly of the mitochondrial ribosome. Hillman GA, Henry MF. J Biol Chem 294 9813-9829 (2019)
  33. MRX8, the conserved mitochondrial YihA GTPase family member, is required for de novo Cox1 synthesis at suboptimal temperatures in Saccharomyces cerevisiae. Verma Y, Mehra U, Pandey DK, Kar J, Pérez-Martinez X, Jana SS, Datta K. Mol Biol Cell 32 ar16 (2021)
  34. A Transcriptomic Analysis of Saccharomyces cerevisiae Under the Stress of 2-Phenylethanol. Jin D, Gu B, Xiong D, Huang G, Huang X, Liu L, Xiao J. Curr. Microbiol. 75 1068-1076 (2018)
  35. A unified dinucleotide alphabet describing both RNA and DNA structures. Černý J, Božíková P, Svoboda J, Schneider B. Nucleic Acids Res 48 6367-6381 (2020)
  36. Biological and Evolutionary Significance of Terminal Extensions of Mitochondrial Translation Initiation Factor 3. Derbikova K, Kuzmenko A, Levitskii S, Klimontova M, Chicherin I, Baleva MV, Krasheninnikov IA, Kamenski P. Int J Mol Sci 19 (2018)
  37. Cryo-EM structure of the highly atypical cytoplasmic ribosome of Euglena gracilis. Matzov D, Taoka M, Nobe Y, Yamauchi Y, Halfon Y, Asis N, Zimermann E, Rozenberg H, Bashan A, Bhushan S, Isobe T, Gray MW, Yonath A, Shalev-Benami M. Nucleic Acids Res 48 11750-11761 (2020)
  38. DPC29 promotes post-initiation mitochondrial translation in Saccharomyces cerevisiae. Hubble KA, Henry MF. Nucleic Acids Res 51 1260-1276 (2023)
  39. DSSR-enabled innovative schematics of 3D nucleic acid structures with PyMOL. Lu XJ. Nucleic Acids Res 48 e74 (2020)
  40. Evolutionary Trajectories are Contingent on Mitonuclear Interactions. Biot-Pelletier D, Bettinazzi S, Gagnon-Arsenault I, Dubé AK, Bédard C, Nguyen THM, Fiumera HL, Breton S, Landry CR. Mol Biol Evol 40 msad061 (2023)
  41. Expression and analysis of the SAM-dependent RNA methyltransferase Rsm22 from Saccharomyces cerevisiae. Alam J, Rahman FT, Sah-Teli SK, Venkatesan R, Koski MK, Autio KJ, Hiltunen JK, Kastaniotis AJ. Acta Crystallogr D Struct Biol 77 840-853 (2021)
  42. Functional analyses of mitoribosome 54S subunit devoid of mitochondria-specific protein sequences. Santos B, Zeng R, Jorge SF, Ferreira-Junior JR, Barrientos A, Barros MH. Yeast 39 208-229 (2022)
  43. GTPBP8 is required for mitoribosomal biogenesis and mitochondrial translation. Wang L, Hilander T, Liu X, Tsang HY, Eriksson O, Jackson CB, Varjosalo M, Zhao H. Cell Mol Life Sci 80 361 (2023)
  44. Identification and Validation of Toxoplasma gondii Mitoribosomal Large Subunit Components. Shikha S, Silva MF, Sheiner L. Microorganisms 10 863 (2022)
  45. Identification of the Toxoplasma gondii mitochondrial ribosome, and characterisation of a protein essential for mitochondrial translation. Lacombe A, Maclean AE, Ovciarikova J, Tottey J, Mühleip A, Fernandes P, Sheiner L. Mol. Microbiol. 112 1235-1252 (2019)
  46. Introns provide a platform for intergenic regulatory feedback of RPL22 paralogs in yeast. Abrhámová K, Nemčko F, Libus J, Převorovský M, Hálová M, Půta F, Folk P. PLoS ONE 13 e0190685 (2018)
  47. Mammalian HEMK1 methylates glutamine residue of the GGQ motif of mitochondrial release factors. Fang Q, Kimura Y, Shimazu T, Suzuki T, Yamada A, Dohmae N, Iwasaki S, Shinkai Y. Sci Rep 12 4104 (2022)
  48. Methods to Study the Biogenesis of Mitoribosomal Proteins in Yeast. Bertgen L, Flohr T, Herrmann JM. Methods Mol Biol 2661 143-161 (2023)
  49. Miniature RNAs are embedded in an exceptionally protein-rich mitoribosome via an elaborate assembly pathway. Valach M, Benz C, Aguilar LC, Gahura O, Faktorová D, Zíková A, Oeffinger M, Burger G, Gray MW, Lukeš J. Nucleic Acids Res 51 6443-6460 (2023)
  50. Mitoribosome Biogenesis. Conor Moran J, Del'Olio S, Choi A, Zhong H, Barrientos A. Methods Mol Biol 2661 23-51 (2023)
  51. Overexpression of MRX9 impairs processing of RNAs encoding mitochondrial oxidative phosphorylation factors COB and COX1 in yeast. Chagas JAC, Kfouri Martins Soares MA, Ribeiro Franco LV, Barros MH. J Biol Chem 298 102214 (2022)
  52. Principles of mitoribosomal small subunit assembly in eukaryotes. Harper NJ, Burnside C, Klinge S. Nature 614 175-181 (2023)
  53. Purification of Mitochondrial Ribosomal Complexes from Trypanosoma cruzi and Leishmania tarentolae for Cryo-EM Analysis. Durrieu-Gaillard S, Sissler M, Hashem Y. Bio Protoc 12 e4425 (2022)
  54. Rapid Cryopurification of the Yeast Mitochondrial Ribosome. Pang HW, Barrientos A. Methods Mol Biol 2661 133-141 (2023)
  55. Stress signaling and cellular proliferation reverse the effects of mitochondrial mistranslation. Ferreira N, Perks KL, Rossetti G, Rudler DL, Hughes LA, Ermer JA, Scott LH, Kuznetsova I, Richman TR, Narayana VK, Abudulai LN, Shearwood AJ, Cserne Szappanos H, Tull D, Yeoh GC, Hool LC, Filipovska A, Rackham O. EMBO J. 38 e102155 (2019)
  56. Structural Patching Fosters Divergence of Mitochondrial Ribosomes. Petrov AS, Wood EC, Bernier CR, Norris AM, Brown A, Amunts A. Mol. Biol. Evol. 36 207-219 (2019)
  57. Structural basis for the interaction of the chaperone Cbp3 with newly synthesized cytochrome b during mitochondrial respiratory chain assembly. Ndi M, Masuyer G, Dawitz H, Carlström A, Michel M, Elofsson A, Rapp M, Stenmark P, Ott M. J. Biol. Chem. 294 16663-16671 (2019)
  58. Structural insights into the binding of bS1 to the ribosome. D'Urso G, Chat S, Gillet R, Giudice E. Nucleic Acids Res 51 3410-3419 (2023)
  59. Supramolecular Double Helices from Small C3-Symmetrical Molecules Aggregated in Water. Lafleur RPM, Herziger S, Schoenmakers SMC, Keizer ADA, Jahzerah J, Thota BNS, Su L, Bomans PHH, Sommerdijk NAJM, Palmans ARA, Haag R, Friedrich H, Böttcher C, Meijer EW. J Am Chem Soc 142 17644-17652 (2020)
  60. Systematic Analysis of Assembly Intermediates in Yeast to Decipher the Mitoribosome Assembly Pathway. Del'Olio S, Barrientos A. Methods Mol Biol 2661 163-191 (2023)
  61. The mitospecific domain of Mrp7 (bL27) supports mitochondrial translation during fermentation and is required for effective adaptation to respiration. Anderson JM, Box JM, Stuart RA. Mol Biol Cell 33 ar7 (2022)
  62. The translational activator Sov1 coordinates mitochondrial gene expression with mitoribosome biogenesis. Seshadri SR, Banarjee C, Barros MH, Fontanesi F. Nucleic Acids Res 48 6759-6774 (2020)
  63. Translational activators and mitoribosomal isoforms cooperate to mediate mRNA-specific translation in Schizosaccharomyces pombe mitochondria. Herbert CJ, Labarre-Mariotte S, Cornu D, Sophie C, Panozzo C, Michel T, Dujardin G, Bonnefoy N. Nucleic Acids Res 49 11145-11166 (2021)
  64. Widespread use of unconventional targeting signals in mitochondrial ribosome proteins. Bykov YS, Flohr T, Boos F, Zung N, Herrmann JM, Schuldiner M. EMBO J 41 e109519 (2022)
  65. Yeast Mitochondrial Translation Initiation Factor 3 Interacts with Pet111p to Promote COX2 mRNA Translation. Chicherin I, Levitskii S, Baleva MV, Krasheninnikov IA, Patrushev MV, Kamenski P. Int J Mol Sci 21 (2020)
  66. Yeast pentatricopeptide protein Dmr1 (Ccm1) binds a repetitive AU-rich motif in the small subunit mitochondrial ribosomal RNA. Piątkowski J, Golik P. RNA 26 1268-1282 (2020)


Quick links