Characterization of hibernating ribosomes in mammalian cells

Cell Cycle

Volumn 10, Issue 16, 2011, Pages 2691-2702

  Krokowski, Dawid ^a,e   Gaccioli, Francesca ^a,f   Majumder, Mithu ^a   Mullins, Michael R ^b   Yuan, Celvie L ^a   Papadopoulou, Barbara ^d   Merrick, William C ^b   Komar, Anton A ^c   Taylor, Derek ^b   Hatzoglou, Maria ^a  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c CLEVELAND STATE UNIVERSITY   (United States)

^d LAVAL UNIVERSITY   (Canada)

^e MARIA CURIE SK ODOWSKA UNIVERSITY   (Poland)

^f Mays Cancer Center at UT Health San Antonio   (United States)

Author keywords

Polysome; Ribosome; Starvation; Stress; Translation

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL INTERACTION; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; EUKARYOTIC CELL; HIBERNATING RIBOSOME; HUMAN; HUMAN CELL; MAMMAL CELL; MOUSE; NONHUMAN; NUTRIENT; POLYSOME; RAT; RIBOSOME; STARVATION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; EUKARYOTA; MAMMALIA; PROKARYOTA; RATTUS;

EID: 80051771740     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.10.16.16844     Document Type: Article

References (74)

1. Schmeing T.M., Ramakrishnan V What recent ribosome structures have revealed about the mechanism of translation Nature 2009; 461:1234-42; PMID: 19838167; DOI: 10.1038/nature08403.
2. Rabl J., Leibundgut M., Ataide S.F., Haag A., Ban N Crystal structure of the eukaryotic 40S ribosomal subunit in complex with initiation factor 1 Science 2011; 331:730-6; PMID: 21205638; DOI: 10.1126/ science.1198308.
3. Ben-Shem A., Jenner L., Yusupova G., Yusupov M Crystal structure of the eukaryotic ribosome Science 2010; 330:1203-9; PMID: 21109664; DOI: 10.1126/ science.1194294.
4. Taylor D.J., Devkota B., Huang A.D., Topf M., Narayanan E., Sali A., et al. Comprehensive molecular structure of the eukaryotic ribosome. Structure 2009; 17:1591-604; PMID: 20004163; DOI: 10.1016/j.str.2009.09.015.
5. Korostelev A., Ermolenko D.N., Noller HF Structural dynamics of the ribosome Curr Opin Chem Biol 2008; 12:674-83; PMID: 18848900; DOI: 10.1016/j. cbpa.2008.08.037.
6. Spahn C.M., Gomez-Lorenzo M.G., Grassucci R.A., Jorgensen R., Andersen G.R., Beckmann R., et al. Domain movements of elongation factor eEF2 and the eukaryotic 80S ribosome facilitate tRNA translocation. EMBO J 2004; 23:1008-19; PMID: 14976550; DOI: 10.1038/sj.emboj.7600102.
7. Gao H., Zhou Z., Rawat U., Huang C., Bouakaz L., Wang C., et al. RF3 induces ribosomal conformational changes responsible for dissociation of class I release factors. Cell 2007; 129:929-41; PMID: 17540173; DOI: 10.1016/j.cell.2007.03.050.
8. Ramakrishnan V The ribosome: some hard facts about its structure and hot air about its evolution Cold Spring Harb Symp Quant Biol 2009; 74:25-33; PMID: 19955257; DOI: 10.1101/sqb.2009.74.032.
9. Lecocq R.E., Cantraine F., Keyhani E., Claude A., Delcroix C., Dumont JE Quantitative evaluation of polysomes and ribosomes by density gradient centrifugation and electron microscopy Anal Biochem 1971; 43:71-9; PMID: 5130413; DOI: 10.1016/0003- 2697(71)90109-6.
10. Pisarev A.V., Skabkin M.A., Pisareva V.P., Skabkina O.V., Rakotondrafara A.M., Hentze M.W., et al. The role of ABCE1 in eukaryotic posttermination ribosomal recycling. Mol Cell 2010; 37:196-210; PMID: 20122402; DOI: 10.1016/j.molcel.2009.12.034.
11. Gaccioliy F., Huang C.C., Wang C., Bevilacqua E., Franchi-Gazzola R., Gazzola G.C., et al. Amino acid starvation induces the SNAT2 neutral amino acid transporter by a mechanism that involves eukaryotic initiation factor 2alpha phosphorylation and cap-independent translation. J Biol Chem 2006; 281:17929-40; PMID: 16621798; DOI: 10.1074/jbc.M600341200.
12. Bevilacqua E., Wang X., Majumder M., Gaccioli F., Yuan C.L., Wang C., et al. eIF2alpha phosphorylation tips the balance to apoptosis during osmotic stress. J Biol Chem 2010; 285:17098-111; PMID: 20338999; DOI: 10.1074/jbc.M110.109439.
13. Sells B.H., Ennis H.L. Polysome stability in relaxed and stringent strain of Escherichia coli during amino acid starvation. J Bacteriol 1970; 102:666-671; PMID: 4914072.
14. Cataldo L., Mastrangelo M.A., Kleene KC A quantitative sucrose gradient analysis of the translational activity of 18 mRNA species in testes from adult mice Mol Hum Reprod 1999; 5:206-13; PMID: 10333353; DOI: 10.1093/molehr/5.3.206.
15. Kraft C., Deplazes A., Sohrmann M., Peter M Mature ribosomes are selectively degraded upon starvation by an autophagy pathway requiring the Ubp3p/Bre5p ubiquitin protease Nat Cell Biol 2008; 10:602-10; PMID: 18391941; DOI: 10.1038/ncb1723.
16. Wada A., Igarashi K., Yoshimura S., Aimoto S., Ishihama A Ribosome modulation factor: stationary growth phase-specific inhibitor of ribosome functions from Escherichia coli Biochem Biophys Res Commun 1995; 214:410-7; PMID: 7677746; DOI: 10.1006/ bbrc.1995.2302.
17. Yoshida H., Maki Y., Kato H., Fujisawa H., Izutsu K., Wada C., et al. The ribosome modulation factor (RMF) binding site on the 100S ribosome of Escherichia coli. J Biochem 2002; 132:983-989; PMID: 12473202.
18. Yamagishi M., Matsushima H., Wada A., Sakagami M., Fujita N., Ishihama A. Regulation of the Escherichia coli rmf gene encoding the ribosome modulation factor: growth phase- and growth rate-dependent control. EMBO J 1993; 12:625-630; PMID: 8440252.
19. Izutsu K., Wada A., Wada C Expression of ribosome modulation factor (RMF) in Escherichia coli requires ppGpp Genes Cells 2001; 6:665-76; PMID: 11532026; DOI: 10.1046/j.1365-2443.2001.00457.x.
20. Yoshida H., Yamamoto H., Uchiumi T., Wada A RMF inactivates ribosomes by covering the peptidyl transferase centre and entrance of peptide exit tunnel Genes Cells 2004; 9:271-8; PMID: 15066119; DOI: 10.1111/j.1356-9597.2004.00723. x.
21. Ueta M., Yoshida H., Wada C., Baba T., Mori H., Wada A Ribosome binding proteins YhbH and YfiA have opposite functions during 100S formation in the stationary phase of Escherichia coli Genes Cells 2005; 10:1103-12; PMID: 16324148; DOI: 10.1111/j.1365- 2443.2005.00903.x.
22. Yoshida H., Ueta M., Maki Y., Sakai A., Wada A Activities of Escherichia coli ribosomes in IF3 and RMF change to prepare 100S ribosome formation on entering the stationary growth phase Genes Cells 2009; 14:271-80; PMID: 19170772; DOI: 10.1111/j.1365- 2443.2008.01272.x.
23. Agafonov D.E., Kolb V.A., Spirin A.S. Ribosomeassociated protein that inhibits translation at the aminoacyl-tRNA binding stage. EMBO Rep 2001; 2:399-402; PMID: 11375931.
24. Maki Y., Yoshida H., Wada A Two proteins, YfiA and YhbH, associated with resting ribosomes in stationary phase Escherichia coli Genes Cells 2000; 5:965-74; PMID: 11168583; DOI: 10.1046/j.1365- 2443.2000.00389.x.
25. Agafonov D.E., Kolb V.A., Nazimov I.V., Spirin AS A protein residing at the subunit interface of the bacterial ribosome Proc Natl Acad Sci USA 1999; 96:12345-9; PMID: 10535924; DOI: 10.1073/pnas.96.22.12345.
26. Vila-Sanjurjo A., Schuwirth B.S., Hau C.W., Cate JH Structural basis for the control of translation initiation during stress Nat Struct Mol Biol 2004; 11:1054-9; PMID: 15502846; DOI: 10.1038/nsmb850.
27. Wada A Growth phase coupled modulation of Escherichia coli ribosomes Genes Cells 1998; 3:203-8; PMID: 9663655; DOI: 10.1046/j.1365- 2443.1998.00187.x.
28. Kato T., Yoshida H., Miyata T., Maki Y., Wada A., Namba K Structure of the 100S ribosome in the hibernation stage revealed by electron cryomicroscopy Structure 2010; 18:719-24; PMID: 20541509; DOI: 10.1016/j. str.2010.02.017.
29. Ortiz JO, Brandt F, Matias VR, Sennels L, Rappsilber J, Scheres SH, et al. Structure of hibernating ribosomes studied by cryoelectron tomography in vitro and in situ. J Cell Biol 2010; 190:613-21; PMID: 20733057; DOI: 10.1083/jcb.201005007.
30. 2+ uptake by OmpC (cation-selective porin) deficiency in ribosome modulation factor-deficient mutant. Biochem Biophys Res Commun 1998; 251:482-7; PMID: 9792800; DOI: 10.1006/bbrc.1998.9494.
31. Ueta M., Ohniwa R.L., Yoshida H., Maki Y., Wada C., Wada A Role of HPF (hibernation promoting factor) in translational activity in Escherichia coli J Biochem 2008; 143:425-33; PMID: 18174192; DOI: 10.1093/ jb/mvm243.
32. Ueta M., Wada C., Wada A Formation of 100S ribosomes in Staphylococcus aureus by the hibernation promoting factor homolog SaHPF Genes Cells 2010; 15:43-58; PMID: 20015224; DOI: 10.1111/j.1365- 2443.2009.01364.x.
33. Martin T.E., Rolleston F.S., Low R.B., Wool IG Dissociation and reassociation of skeletal muscle ribosomes J Mol Biol 1969; 43:135-49; PMID: 4980475; DOI: 10.1016/0022-2836(69)90084-9.
34. Reader R.W., Stanners CP On the significance of ribosome dimers in extracts of animal cells J Mol Biol 1967; 28:211-23; PMID: 6052638; DOI: 10.1016/ S0022-2836(67)80004-4.
35. Eliceiri G.L. The RNA of a dimerized ribosomal structure from hamster cells. Biochim Biophys Acta 1972; 269:450-452; PMID: 5064715.
36. Zhang P., McGrath B.C., Reinert J., Olsen D.S., Lei L., Gill S., et al. The GCN2 eIF2alpha kinase is required for adaptation to amino acid deprivation in mice. Mol Cell Biol 2002; 22:6681-8; PMID: 12215525; DOI: 10.1128/MCB.22.19.6681-8.2002.
37. Bordeleau M.E., Mori A., Oberer M., Lindqvist L., Chard L.S., Higa T., et al. Functional characterization of IRESes by an inhibitor of the RNA helicase eIF4A. Nat Chem Biol 2006; 2:213-20; PMID: 16532013; DOI: 10.1038/nchembio776.
38. Bertolotti A., Zhang Y., Hendershot L.M., Harding H.P., Ron D Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response Nat Cell Biol 2000; 2:326-32; PMID: 10854322; DOI: 10.1038/35014014.
39. Stark H GraFix: stabilization of fragile macromolecular complexes for single particle cryo-EM Methods Enzymol 2010; 481:109-26; PMID: 20887855; DOI: 10.1016/S0076-6879(10)81005-5.
40. Penczek P.A., Grassucci R.A., Frank J The ribosome at improved resolution: new techniques for merging and orientation refinement in 3D cryo-electron microscopy of biological particles Ultramicroscopy 1994; 53:251-70; PMID: 8160308; DOI: 10.1016/0304-3991(94)90038-8.
41. Spahn C.M., Jan E., Mulder A., Grassucci R.A., Sarnow P., Frank J Cryo-EM visualization of a viral internal ribosome entry site bound to human ribosomes: the IRES functions as an RNA-based translation factor Cell 2004; 118:465-75; PMID: 15315759; DOI: 10.1016/j.cell.2004.08.001.
42. Shaikh T.R., Trujillo R., LeBarron J.S., Baxter W.T., Frank J Particle-verification for single-particle, referencebased reconstruction using multivariate data analysis and classification J Struct Biol 2008; 164:41-8; PMID: 18619547; DOI: 10.1016/j.jsb.2008.06.006.
43. Cornish P.V., Ermolenko D.N., Staple D.W., Hoang L., Hickerson R.P., Noller H.F., et al. Following movement of the L1 stalk between three functional states in single ribosomes. Proc Natl Acad Sci USA 2009; 106:2571-6; PMID: 19190181; DOI: 10.1073/pnas.0813180106.
44. Grela P., Bernado P., Svergun D., Kwiatowski J., Abramczyk D., Grankowski N., et al. Structural relationships among the ribosomal stalk proteins from the three domains of life. J Mol Evol 2008; 67:154-67; PMID: 18612675; DOI: 10.1007/s00239-008-9132-2
45. Tchórzewski M. The acidic ribosomal P proteins. Int J Biochem Cell Biol 2002; 34:911-5; PMID: 12007628; DOI: 10.1016/S1357-2725(02)00012-2.
46. Gonzalo P., Lavergne J.P., Reboud JP Pivotal role of the P1 N-terminal domain in the assembly of the mammalian ribosomal stalk and in the proteosynthetic activity J Biol Chem 2001; 276:19762-9; PMID: 11274186; DOI: 10.1074/jbc.M101398200.
47. Helgstrand M., Mandava C.S., Mulder F.A., Liljas A., Sanyal S., Akke M The ribosomal stalk binds to translation factors IF2, EF-Tu, EF-G and RF3 via a conserved region of the L12 C-terminal domain J Mol Biol 2007; 365:468-79; PMID: 17070545; DOI: 10.1016/j.jmb.2006.10.025.
48. Jiang H.Y., Wek S.A., McGrath B.C., Scheuner D., Kaufman R.J., Cavener D.R., et al. Phosphorylation of the alpha subunit of eukaryotic initiation factor 2 is required for activation of NFkappaB in response to diverse cellular stresses. Mol Cell Biol 2003; 23:5651-63; PMID: 12897138; DOI: 10.1128/ MCB.23.16.5651-63.2003.
49. Buchan J.R., Parker R Eukaryotic stress granules: the ins and outs of translation Mol Cell 2009; 36:932-41; PMID: 20064460; DOI: 10.1016/j.molcel. 2009.11.020.
50. Masuda K., Marasa B., Martindale J.L., Halushka M.K., Gorospe M. Tissue- and age-dependent expression of RNA-binding proteins that influence mRNA turnover and translation. Aging (Albany NY) 2009; 1:681-698; PMID: 20157551.
51. Gallouzi I.E. Could stress granules be involved in agerelated diseases? Aging (Albany NY) 2009; 1:753-757; PMID: 20157563.
52. Kedersha N.L., Gupta M., Li W., Miller I., Anderson P RNA-binding proteins TIA-1 and TIAR link the phosphorylation of eIF-2alpha to the assembly of mammalian stress granules J Cell Biol 1999; 147:1431-42; PMID: 10613902; DOI: 10.1083/jcb.147.7.1431.
53. El-Sharoud WM Ribosome inactivation for preservation: concepts and reservations Sci Prog 2004; 87:137-52; PMID: 15884656; DOI: 10.3184/ 003685004783238517.
54. Jackson R.J., Hellen C.U., Pestova TV The mechanism of eukaryotic translation initiation and principles of its regulation Nat Rev Mol Cell Biol 2010; 11:113-27; PMID: 20094052; DOI: 10.1038/nrm2838.
55. Komar A.A., Hatzoglou M Cellular IRES-mediated translation: the war of ITAFs in pathophysiological states Cell Cycle 2011; 10:229-40; PMID: 21220943; DOI: 10.4161/cc.10.2.14472.
56. Wek R.C., Jiang H.Y., Anthony TG Coping with stress: eIF2 kinases and translational control Biochem Soc Trans 2006; 34:7-11; PMID: 16246168; DOI: 10.1042/BST0340007.
57. Holz M.K., Blenis J Identification of S6 kinase 1 as a novel mammalian target of rapamycin (mTOR)-phosphorylating kinase J Biol Chem 2005; 280:26089-93; PMID: 15905173; DOI: 10.1074/jbc.M504045200.
58. Panieri E., Toietta G., Mele M., Labate V., Ranieri S.C., Fusco S., et al. Nutrient withdrawal rescues growth factor-deprived cells from mTOR-dependent damage. Aging (Albany NY) 2010; 2:487-503; PMID: 20739737.
59. Hands S.L., Proud C.G., Wyttenbach A. mTOR's role in ageing: protein synthesis or autophagy? Aging (Albany NY) 2009; 1:586-597; PMID: 20157541.
60. Pause A., Belsham G.J., Gingras A.C., Donze O., Lin T.A., Lawrence J.C. Jr, et al. Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5'-cap function. Nature 1994; 371:762-7; PMID: 7935836; DOI: 10.1038/371762a0.
61. Eliceiri GL The ribosomal RNA of hamster-mouse hybrid cells J Cell Biol 1972; 53:177-84; PMID: 5062528; DOI: 10.1083/jcb.53.1.177.
62. Lilja H.S., Longnecker D.S., Curphey T.J., Daniel D.S., Adams WE Studies of DNA damage in rat pancreas and liver by 6-diazo-5-oxo-L-norleucine, ethyl diazoacetate and azaserine Cancer Lett 1981; 12:139-46; PMID: 7272997; DOI: 10.1016/0304-3835(81)90049-5.
63. Genot A., Dazord A Transitory increase of run-off single ribosomes in rat adrenocortical cells, following ACTH administration, in vivo Biochem Biophys Res Commun 1982; 109:1172-9; PMID: 6301428; DOI: 10.1016/0006-291X(82)91900-3.
64. McGown E., Richardson A.G., Henderson L.M., Swan P.B. Effect of amino acids on ribosome aggregation and protein synthesis in perfused rat liver. J Nutr 1973; 103:109-116; PMID: 4682444.
65. Volchuk A., Ron D The endoplasmic reticulum stress response in the pancreatic beta-cell Diabetes Obes Metab 2010; 12:48-57; PMID: 21029300; DOI: 10.1111/j.1463-326.2010.01271.x.
66. Hartley T., Siva M., Lai E., Teodoro T., Zhang L., Volchuk A Endoplasmic reticulum stress response in an INS-1 pancreatic beta-cell line with inducible expression of a folding-deficient proinsulin BMC Cell Biol 2010; 11:59; PMID: 20659334; DOI: 10.1186/1471-2121- 11-59.
67. Garay-Arroyo A., Colmenero-Flores J.M., Garciarrubio A., Covarrubias AA Highly hydrophilic proteins in prokaryotes and eukaryotes are common during conditions of water deficit J Biol Chem 2000; 275:5668-74; PMID: 10681550; DOI: 10.1074/jbc.275.8.5668.
68. Niven GW Ribosome modulation factor protects Escherichia coli during heat stress, but this may not be dependent on ribosome dimerisation. Arch Microbiol 2004; 182:60-6; PMID: 15278243; DOI: 10.1007/ s00203-004-0698-9.
69. Bürk J., Weiche B., Wenk M., Boy D., Nestel S., Heimrich B., et al. Depletion of the signal recognition particle receptor inactivates ribosomes in Escherichia coli. J Bacteriol 2009; 191:7017-26; PMID: 19749044; DOI: 10.1128/JB.00208-09.
70. El-Sharoud W.M., Niven GW The influence of ribosome modulation factor on the survival of stationaryphase Escherichia coli during acid stress Microbiology 2007; 153:247-53; PMID: 17185553; DOI: 10.1099/ mic.0.2006/001552-0.
71. Zeenko V.V., Wang C., Majumder M., Komar A.A., Snider M.D., Merrick W.C., et al. An efficient in vitro translation system from mammalian cells lacking the translational inhibition caused by eIF2 phosphorylation. RNA 2008; 14:593-602; PMID: 18230759; DOI: 10.1261/rna.825008.
72. Frank J., Radermacher M., Penczek P., Zhu J., Li Y., Ladjadj M., et al. SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J Struct Biol 1996; 116:190-9; PMID: 8742743; DOI: 10.1006/jsbi.1996.0030.
73. Majumder M., Yaman I., Gaccioli F., Zeenko V.V., Wang C., Caprara M.G., et al. The hnRNA-binding proteins hnRNP L and PTB are required for efficient translation of the Cat-1 arginine/lysine transporter mRNA during amino acid starvation. Mol Cell Biol 2009; 29:2899- 912; PMID: 19273590; DOI: 10.1128/MCB.01774- 08.
74. Li Y., Bevilacqua E., Chiribau C.B., Majumder M., Wang C., Croniger C.M., et al. Differential control of the CCAAT/enhancer-binding protein beta (C/EBPbeta) products liver-enriched transcriptional activating protein (LAP) and liver-enriched transcriptional inhibitory protein (LIP) and the regulation of gene expression during the response to endoplasmic reticulum stress. J Biol Chem 2008; 283:22443-56; PMID: 18550528; DOI: 10.1074/jbc.M801046200.