Deletion of L4 domains reveals insights into the importance of ribosomal protein extensions in eukaryotic ribosome assembly

RNA

Volumn 20, Issue 11, 2014, Pages 1725-1731

  Gamalinda, Michael ^a,b   Woolford, John L ^a  

^a CARNEGIE MELLON UNIVERSITY   (United States)

^b MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

Author keywords

Ribosomal protein extensions; Ribosomal protein L4; Ribosome; Ribosome assembly

Indexed keywords

ERYTHROMYCIN; PROTEIN; PROTEIN L4; RIBOSOME PROTEIN; RNA 18S; UNCLASSIFIED DRUG; RIBOSOMAL PROTEIN L4; SACCHAROMYCES CEREVISIAE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BIOGENESIS; CELL FUNCTION; CELL VIABILITY; CENTROMERE; DELETION MUTANT; ESCHERICHIA COLI; EUKARYOTE; EUKARYOTIC RIBOSOME ASSEMBLY; FRACTIONATION; LARGE RIBOSOMAL SUBUNIT; NONHUMAN; NORTHERN BLOTTING; POLYACRYLAMIDE GEL ELECTROPHORESIS; POLYSOME; PROTEIN DOMAIN; RIBOSOME; RIBOSOME SUBUNIT; SILVER STAINING; SUCROSE GRADIENT; WESTERN BLOTTING; YEAST; CHEMICAL STRUCTURE; GENE DELETION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NUCLEOTIDE SEQUENCE; PROTEIN CONFORMATION; PROTEIN SECONDARY STRUCTURE; SACCHAROMYCES CEREVISIAE;

BASE SEQUENCE; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; RIBOSOMAL PROTEINS; RIBOSOMES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE DELETION;

EID: 84908138347     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.046649.114     Document Type: Article

References (50)

1. Ban N, Nissen P, Hansen J, Moore PB, Steitz TA. 2000. The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution. Science 289: 905-920.
2. 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.
3. Blaha GM, Polikanov YS, Steitz TA. 2012. Elements of ribosomal drug resistance and specificity. Curr Opin Struct Biol 22: 750-758.
4. Bussiere C, Hashem Y, Arora S, Frank J, Johnson AW. 2012. Integrity of the P-site is probed during maturation of the 60S ribosomal subunit. J Cell Biol 197: 747-759.
5. Calidas D, Culver GM. 2010. Interdependencies govern multidomain architecture in ribosomal small subunit assembly. RNA 17: 263-277.
6. Calidas D, Lyon H, Culver GM. 2014. The N-terminal extension of S12 influences small ribosomal subunit assembly in Escherichia coli. RNA 20: 321-330.
7. Chittum HS, Champney WS. 1994. Ribosomal protein gene sequence changes in erythromycin-resistant mutants of Escherichia coli. J Bacteriol 176: 6192-6198.
8. De Keersmaecker K, Atak ZK, Li N, Vicente C, Patchett S, Girardi T, Gianfelici V, Geerdens E, Clappier E, Porcu M, et al. 2012. Exome sequencing identifies mutation in CNOT3 and ribosomal genes RPL5 and RPL10 in T-cell acute lymphoblastic leukemia. Nat Genet 45: 186-190.
9. Fulle S, Gohlke H. 2009. Statics of the ribosomal exit tunnel: Implications for cotranslational peptide folding, elongation regulation, and antibiotics binding. J Mol Biol 387: 502-517.
10. Gabashvili IS, Gregory ST, Valle M, Grassucci R, Worbs M, Wahl MC, Dahlberg AE, Frank J. 2001. The polypeptide tunnel system in the ribosome and its gating in erythromycin resistance mutants of L4 and L22. Mol Cell 8: 181-188.
11. Gamalinda M, Jakovljevic J, Babiano R, Talkish J, de la Cruz J, Woolford JL Jr. 2013. Yeast polypeptide exit tunnel ribosomal proteins L17, L35 and L37 are necessary to recruit late-assembling factors required for 27SB pre-rRNA processing. Nucleic Acids Res 41: 1965-1983.
12. Gamalinda M, Ohmayer U, Jakovljevic J, Kumcuoglu B, Woolford J, Mbom B, Lin L, Woolford JL Jr. 2014. A hierarchical model for assembly of eukaryotic 60S ribosomal subunit domains. Genes Dev 28: 198-210.
13. Garcia-Gomez JJ, Fernandez-Pevida A, Lebaron S, Rosado IV, Tollervey D, Kressler D, de la Cruz J. 2014. Final pre-40S maturation depends on the functional integrity of the 60S subunit ribosomal protein L3. PLoS Genet 10: E1004205.
14. Gazda HT, Sheen MR, Vlachos A, Choesmel V, O'Donohue MF, Schneider H, Darras N, Hasman C, Sieff CA, Newburger PE, et al. 2008. Ribosomal protein L5 and L11 mutations are associated with cleft palate and abnormal thumbs in Diamond-Blackfan anemia patients. Am J Hum Genet 83: 769-780.
15. Guillier M, Allemand F, Graffe M, Raibaud S, Dardel F, Springer M, Chiaruttini C. 2005. The N-terminal extension of Escherichia coli ribosomal protein L20 is important for ribosome assembly, but dispensable for translational feedback control. RNA 11: 728-738.
16. Holmes KL, Culver GM. 2005. Analysis of conformational changes in 16 S rRNA during the course of 30 S subunit assembly. J Mol Biol 354: 340-357.
17. Jakovljevic J, de Mayolo PA, Miles TD, Nguyen TM, Leger-Silvestre I, Gas N, Woolford JL Jr. 2004. The carboxy-terminal extension of yeast ribosomal protein S14 is necessary for maturation of 43S preribosomes. Mol Cell 14: 331-342.
18. Jakovljevic J, Ohmayer U, Gamalinda M, Talkish J, Alexander L, Linnemann J, Milkereit P, Woolford JL Jr. 2012. Ribosomal proteins L7 and L8 function in concert with six A3 assembly factors to propagate assembly of domains I and II of 25S rRNA in yeast 60S ribosomal subunits. RNA 18: 1805-1822.
19. 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.
20. Kannan K, Mankin AS. 2011. Macrolide antibiotics in the ribosome exit tunnel: Species-specific binding and action. Ann N Y Acad Sci 1241: 33-47.
21. Karbstein K. 2011. Inside the 40S ribosome assembly machinery. Curr Opin Chem Biol 15: 657-663.
22. Karbstein K. 2013. Quality control mechanisms during ribosome maturation. Trends Cell Biol 23: 242-250.
23. Klein DJ, Moore PB, Steitz TA. 2004. The roles of ribosomal proteins in the structure assembly, and evolution of the large ribosomal subunit. J Mol Biol 340: 141-177.
24. Kressler D, Hurt E, Bergler H, Bassler J. 2012. The power of AAAATPases on the road of pre-60S ribosome maturation-molecular machines that strip pre-ribosomal particles. Biochim Biophys Acta 1823: 92-100.
25. Maxwell ES, Fournier MJ. 1995. The small nucleolar RNAs. Annu Rev Biochem 64: 897-934.
26. Mayerle M, Woodson SA. 2013. Specific contacts between protein S4 and ribosomal RNA are required at multiple stages of ribosome assembly. RNA 19: 574-585.
27. Melnikov S, Ben-Shem A, Garreau de Loubresse N, Jenner L, Yusupova G, Yusupov M. 2012. One core, two shells: bacterial and eukaryotic ribosomes. Nat Struct Mol Biol 19: 560-567.
28. Nissen P, Hansen J, Ban N, Moore PB, Steitz TA. 2000. The structural basis of ribosome activity in peptide bond synthesis. Science 289: 920-930.
29. Ohmayer U, Gamalinda M, Sauert M, Ossowski J, Poll G, Linnemann J, Hierlmeier T, Perez-Fernandez J, Kumcuoglu B, Leger-Silvestre I, et al. 2013. Studies on the assembly characteristics of large subunit ribosomal proteins in S. cerevisae. PLoS One 8: E68412.
30. Peng Z, Oldfield CJ, Xue B, Mizianty MJ, Dunker AK, Kurgan L, Uversky VN. 2014. A creature with a hundred waggly tails: Intrinsically disordered proteins in the ribosome. Cell Mol Life Sci 71: 1477-1504.
31. Poll G, Braun T, Jakovljevic J, Neueder A, Jakob S, Woolford JL Jr, Tschochner H, Milkereit P. 2009. rRNA maturation in yeast cells depleted of large ribosomal subunit proteins. PLoS One 4: E8249.
32. Ramaswamy P, Woodson SA. 2009a. Global stabilization of rRNA structure by ribosomal proteins S4, S17, and S20. J Mol Biol 392: 666-677.
33. Ramaswamy P, Woodson SA. 2009b. S16 throws a conformational switch during assembly of 30S 5′ domain. Nat Struct Mol Biol 16: 438-445.
34. Recht MI, Williamson JR. 2004. RNA tertiary structure and cooperative assembly of a large ribonucleoprotein complex. J Mol Biol 344: 395-407.
35. Rohl R, Nierhaus KH. 1982. Assembly map of the large subunit (50S) of Escherichia coli ribosomes. Proc Natl Acad Sci 79: 729-733.
36. Sahasranaman A, Dembowski J, Strahler J, Andrews P, Maddock J, Woolford JL Jr. 2011. Assembly of Saccharomyces cerevisiae 60S ribosomal subunits: role of factors required for 27S pre-rRNA processing. EMBO J 30: 4020-4032.
37. Schuwirth BS, Borovinskaya MA, Hau CW, Zhang W, Vila-Sanjurjo A, Holton JM, Cate JH. 2005. Structures of the bacterial ribosome at 3.5 Å resolution. Science 310: 827-834.
38. Strunk BS, Novak MN, Young CL, Karbstein K. 2012. A translation-like cycle is a quality control checkpoint for maturing 40S ribosome subunits. Cell 150: 111-121.
39. Timsit Y, Acosta Z, Allemand F, Chiaruttini C, Springer M. 2009. The role of disordered ribosomal protein extensions in the early steps of eubacterial 50 S ribosomal subunit assembly. Int J Mol Sci 10: 817-834.
40. Watkins-Chow DE, Cooke J, Pidsley R, Edwards A, Slotkin R, Leeds KE, Mullen R, Baxter LL, Campbell TG, Salzer MC, et al. 2013. Mutation of the Diamond-Blackfan anemia gene Rps7 in mouse results in morphological and neuroanatomical phenotypes. PLoS Genet 9: E1003094.
41. Wilson DN, Nierhaus KH. 2005. Ribosomal proteins in the spotlight. Crit Rev Biochem Mol Biol 40: 243-267.
42. Wimberly BT, Brodersen DE, Clemons WM Jr, Morgan-Warren RJ, Carter AP, Vonrhein C, Hartsch T, Ramakrishnan V. 2000. Structure of the 30S ribosomal subunit. Nature 407: 327-339.
43. Woolford JL Jr, Baserga SJ. 2013. Ribosome biogenesis in the yeast Saccharomyces cerevisiae. Genetics 195: 643-681.
44. Woolstenhulme CJ, Hill WE. 2009. The genesis of ribosome structure: How a protein generates RNA structure in real time. J Mol Biol 392: 645-656.
45. Worbs M, Huber R, Wahl MC. 2000. Crystal structure of ribosomal protein L4 shows RNA-binding sites for ribosome incorporation and feedback control of the S10 operon. EMBO J 19: 807-818.
46. Yonath A. 2005. Antibiotics targeting ribosomes: resistance, selectivity, synergism and cellular regulation. Annu Rev Biochem 74: 649-679.
47. Yusupov MM, Yusupova GZ, Baucom A, Lieberman K, Earnest TN, Cate JH, Noller HF. 2001. Crystal structure of the ribosome at 5.5 Å resolution. Science 292: 883-896.
48. Yusupova G, Yusupov M. 2014. High-resolution structure of the eukaryotic 80S ribosome. Annu Rev Biochem 83: 467-486.
49. Zaman S, Fitzpatrick M, Lindahl L, Zengel J. 2007. Novel mutations in ribosomal proteins L4 and L22 that confer erythromycin resistance in Escherichia coli. Mol Microbiol 66: 1039-1050.
50. Zengel JM, Jerauld A, Walker A, WahlMC, Lindahl L. 2003. The extended loops of ribosomal proteins L4 and L22 are not required for ribosome assembly or L4-mediated autogenous control. RNA 9: 1188-1197.