1,455
Views
3
CrossRef citations to date
0
Altmetric
REVIEW

Eukaryote-specific extensions in ribosomal proteins of the small subunit: Structure and function

&
Article: e999576 | Received 16 Oct 2014, Accepted 12 Dec 2014, Published online: 05 Feb 2015

References

  • Ramakrishnan V. Ribosome structure and the mechanism of translation. Cell 2002; 108:557-2; PMID:11909526; http://dx.doi.org/10.1016/S0092-8674(02)00619-0
  • Schmeing TM, Ramakrishnan V. What recent ribosome structures have revealed about the mechanism of translation. Nature 2009; 461:1234-1242; PMID:19838167; http://dx.doi.org/10.1038/nature08403
  • Dinman JD. The eukaryotic ribosome: current status and challenges. J Biol Chem 2009; 284(18):11761-5; PMID:19117941; http://dx.doi.org/10.1074/jbc.R800074200
  • Budkevich TV, El'skaya AV, Nierhaus, KH. Features of 80S mammalian ribosome and its subunits. Nucleic Acids Res 2008; 36(14):4736-4744. PMID:18632761; http://dx.doi.org/10.1093/nar/gkn424
  • Ben-Shem A, Jenner L, Yusupova G, Yusupov M. Crystal structure of the eukaryotic ribosome. Science 2010; 330(6008):1203-9; PMID:21109664; http://dx.doi.org/10.1126/science.1194294
  • Ben-Shem A, Garreau de Loubresse N, Melnikov S, Jenner L, Yusupova G, Yusupov M. The structure of the eukaryotic ribosome at 3.0 Å resolution. Science 2011; 334(6062):1524-9; PMID:22096102; http://dx.doi.org/10.1126/science.1212642
  • Ban N, Nissen P, Hansen J, Moore PB, Steitz TA. The complete atomic structure of the large ribosomal subunit at 2.4 A resolution. Science 2000; 289(5481):905-920; PMID:10937989; http://dx.doi.org/10.1126/science.289.5481.905
  • Zhang W, Dunkle JA, Cate JH. Structures of the ribosome in intermediate states of ratcheting. Science 2009; 325(5943):1014-7; PMID:19696352. http://dx.doi.org/ 10.1126/science.1175275
  • Klinge S, Voigts-Hoffmann F, Leibundgut M, Ban N. Atomic structures of the eukaryotic ribosome. Trends Biochem Sci 2012; 37(5):189-98; PMID:22436288; http://dx.doi.org/10.1016/j.tibs.2012.02.007
  • Ramakrishnan V. Molecular biology. The eukaryotic ribosome. Science 2011; 331(6018):681-2; PMID:21310988; http://dx.doi.org/10.1126/science.1202093
  • Anger AM, Armache JP, Berninghausen O, Habeck M, Subklewe M, Wilson DN, Beckmann R. Structures of the human and Drosophila 80S ribosome. Nature 2013; 497(7447):80-5; PMID:23636399; http://dx.doi.org/10.1038/nature12104
  • Melnikov S, Ben-Shem A, Garreau de Loubresse N, Jenner L, Yusupova G, Yusupov M. One core, two shells: bacterial and eukaryotic ribosomes. Nat Struct Mol Biol 2012; 19(6):560-7; PMID:22664983; http://dx.doi.org/10.1038/nsmb.2313
  • Rodnina MV, Wintermeyer W. Recent mechanistic insights into eukaryotic ribosomes. Curr Opin Cell Biol 2009; 21(3):435-43; PMID:19243929; http://dx.doi.org/10.1016/j.ceb.2009.01.023
  • Jackson RJ, Hellen CU, Pestova TV. The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol 2010; 11(2):113-27; PMID:20094052; http://dx.doi.org/10.1038/nrm2838
  • Voigts-Hoffmann F, Klinge S, Ban N. Structural insights into eukaryotic ribosomes and the initiation of translation. Curr Opin Struct Biol 2012; 22(6):768-77; PMID:22889726; http://dx.doi.org/10.1016/j.sbi.2012.07.010
  • Milon P, Konevega AL, Gualerzi CO, Rodnina MV. Kinetic checkpoint at a late step in translation initiation. Mol Cell 2008; 30(6):712-20; PMID:18570874; http://dx.doi.org/10.1016/j.molcel.2008.04.014
  • Grigoriadou C, Marzi S, Kirillov S, Gualerzi CO, Cooperman BS. A quantitative kinetic scheme for 70 S translation initiation complex formation. J Mol Biol 2007; 373(3):562-72; PMID:17868692; http://dx.doi.org/10.1016/j.jmb.2007.07.032
  • Pisarev AV, Hellen CU, Pestova TV. Recycling of eukaryotic post termination ribosomal complexes. Cell 2007; 131(2):286-99; PMID:17956730; http://dx.doi.org/10.1016/j.cell.2007.08.041
  • Pisarev AV, Skabkin MA, Pisareva VP, Skabkina OV, Rakotondrafara AM, Hentze MW, Hellen CU, Pestova TV. The role of ABCE1 in eukaryotic post termination ribosomal recycling. Mol Cell 2010; 37(2):196-210; PMID:20122402; http://dx.doi.org/10.1016/j.molcel.2009.12.034
  • Gross JD, Moerke NJ, von der Haar T, Lugovskoy AA, Sachs AB, McCarthy JE, Wagner G. Ribosome loading onto the mRNA cap is driven by conformational coupling between eIF4G and eIF4E. Cell 2003; 115(6):739-50; PMID:14675538; http://dx.doi.org/10.1016/S0092-8674(03)00975-9
  • LeFebvre AK, Korneeva NL, Trutschl M, Cvek U, Duzan RD, Bradley CA, Hershey JW, Rhoads RE. Translation initiation factor eIF4G-1 binds to eIF3 through the eIF3e subunit. J Biol Chem 2006; 281(32):22917-32; PMID:16766523; http://dx.doi.org/10.1074/jbc.M605418200
  • Asano K, Clayton J, Shalev A, Hinnebusch AG. A multifactor complex of eukaryotic initiation factors, eIF1, eIF2, eIF3, eIF5, and initiator tRNA(Met) is an important translation initiation intermediate in vivo. Genes Dev 2000; 14(19): 2534-46; PMID:11018020; http://dx.doi.org/10.1101/gad.831800
  • Asano K, Phan L, Valásek L, Schoenfeld LW, Shalev A, Clayton J, Nielsen K, Donahue TF, Hinnebusch AG. Multifactor complex of eIF1, eIF2, eIF3, eIF5, and tRNA(i)Met promotes initiation complex assembly and couples GTP hydrolysis to AUG recognition. Cold Spring Harb Symp Quant Biol 2001; 66:403-15; PMID:12762043; http://dx.doi.org/10.1101/sqb.2001.66.403
  • Asano K, Shalev A, Phan L, Nielsen K, Clayton J, Valásek L, Donahue TF, Hinnebusch AG. Multiple roles for the C-terminal domain of eIF5 in translation initiation complex assembly and GTPase activation. EMBO J 2001; 20(9):2326-37; PMID:11331597; http://dx.doi.org/10.1093/emboj/20.9.2326
  • Hinnebusch AG. eIF3: a versatile scaffold for translation initiation complexes. Trends Biochem Sci 2006; 31(10):553-62; PMID:16920360; http://dx.doi.org/10.1016/j.tibs.2006.08.005
  • Passmore LA, Schmeing TM, Maag D, Applefield DJ, Acker MG, Algire MA, Lorsch JR, Ramakrishnan V. The eukaryotic translation initiation factors eIF1 and eIF1A induce an open conformation of the 40S ribosome. Mol Cell 2007; 26(1):41-50; PMID:17434125; http://dx.doi.org/10.1016/j.molcel.2007.03.018
  • Hinnebusch AG, Lorsch JR. The mechanism of eukaryotic translation initiation: new insights and challenges. Cold Spring Harb Perspect Biol 2012; 4(10): pii: a011544; PMID:22815232; http://dx.doi.org/10.1101/cshperspect.a011544
  • Hinnebusch AG. The scanning mechanism of eukaryotic translation initiation. Annu Rev Biochem 2014; 83:779-812; PMID:24499181; http://dx.doi.org/10.1146/annurev-biochem-060713-035802
  • Algire MA, Maag D, Lorsch JR. Pi release from eIF2, not GTP hydrolysis, is the step controlled by start-site selection during eukaryotic translation initiation. Mol Cell 2005; 20(2):251-62; PMID:16246727; http://dx.doi.org/10.1016/j.molcel.2005.09.008
  • Hashem Y, des Georges A, Dhote V, Langlois R, Liao HY, Grassucci RA, Hellen CU, Pestova TV, Frank J. Structure of the mammalian ribosomal 43S preinitiation complex bound to the scanning factor DHX29. Cell 2013; 153(5):1108-19; PMID:23706745; http://dx.doi.org/10.1016/j.cell.2013.04.036
  • Lomakin IB, Steitz TA. The initiation of mammalian protein synthesis and mRNA scanning mechanism. Nature 2013; 500(7462):307-11; PMID:23873042; http://dx.doi.org/10.1038/nature12355
  • Dresios J, Panopoulos P, Synetos D. Eukaryotic ribosomal proteins lacking a eubacterial counterpart: important players in ribosomal function. Mol Microbiol 2006; 59(6):1651-63; PMID:16553873; http://dx.doi.org/10.1111/j.1365-2958.2006.05054.x
  • Valásek LS. ‘Ribozoomin’-translation initiation from the perspective of the ribosome-bound eukaryotic initiation factors (eIFs). Curr Protein Pept Sci 2012; 13(4):305; PMID:22708493; http://dx.doi.org/10.2174/138920312801619385
  • Ardini E, Pesole G, Tagliabue E, Magnifico A, Castronovo V, Sobel ME, Colnaghi MI, Ménard S. The 67-kDa laminin receptor originated from a ribosomal protein that acquired a dual function during evolution. Mol Biol Evol 1998; 15(8):1017-25; PMID:9718729
  • Nelson J, McFerran NV, Pivato G, Chambers E, Doherty C, Steele D, Timson DJ. The 67 kDa laminin receptor: structure, function and role in disease. Biosci Rep 2008; 28(1):33-48; PMID:18269348; http://dx.doi.org/10.1042/BSR20070004
  • Castronovo V. Laminin receptors and laminin-binding proteins during tumor invasion and metastasis. Invasion Metastasis 1993;13(1):1-30; PMID:8407208
  • Martignone S, Ménard S, Bufalino R, Cascinelli N, Pellegrini R, Tagliabue E, Andreola S, Rilke F, Colnaghi MI. Prognostic significance of the 67-kilodalton laminin receptor expression in human breast carcinomas. J Natl Cancer Inst 1993;85(5):398-402; PMID:8433393; http://dx.doi.org/10.1093/jnci/85.5.398
  • Berno V, Porrini D, Castiglioni F, Campiglio M, Casalini P, Pupa SM, Balsari A, Ménard S, Tagliabue E. The 67 kDa laminin receptor increases tumor aggressiveness by remodeling laminin-1. Endocr Relat Cancer 2005;12(2):393-406; PMID:15947111; http://dx.doi.org/10.1677/erc.1.00870
  • Wang KS, Kuhn RJ, Strauss EG, Ou S, Strauss JH. High-affinity laminin receptor is a receptor for Sindbis virus in mammalian cells. J Virol. 1992; 66(8):4992-5001; PMID:1385835
  • Phan L, Zhang X, Asano K, Anderson J, Vornlocher HP, Greenberg JR, Qin J, Hinnebusch AG. Identification of a translation initiation factor 3 (eIF3) core complex, conserved in yeast and mammals, that interacts with eIF5. Mol Cell Biol 1998; 18(8):4935-46; PMID:9671501
  • Valásek L, Phan L, Schoenfeld LW, Valásková V, Hinnebusch AG. Related eIF3 subunits TIF32 and HCR1 interact with an RNA recognition motif in PRT1 required for eIF3 integrity and ribosome binding. EMBO J 2001; 20(4):891-904; PMID:11179233; http://dx.doi.org/10.1093/emboj/20.4.891
  • Chaudhuri J, Chowdhury D, Maitra U. Distinct functions of eukaryotic translation initiation factors eIF1A and eIF3 in the formation of the 40S ribosomal preinitiation complex. J Biol Chem 1999; 274(25):17975-80; PMID:10364246; http://dx.doi.org/10.1074/jbc.274.25.17975
  • Kolupaeva VG, Unbehaun A, Lomakin IB, Hellen CU, Pestova TV. Binding of eukaryotic initiation factor 3 to ribosomal 40S subunits and its role in ribosomal dissociation and anti-association. RNA 2005; 11(4):470-86; PMID:15703437; http://dx.doi.org/10.1261/rna.7215305
  • Phan L, Schoenfeld LW, Valásek L, Nielsen KH, Hinnebusch AG. A subcomplex of three eIF3 subunits binds eIF1 and eIF5 and stimulates ribosome binding of mRNA and tRNA(i)Met. EMBO J 2001; 20(11):2954-65; PMID:11387228; http://dx.doi.org/10.1093/emboj/20.11.2954
  • Valásek L, Mathew AA, Shin BS, Nielsen KH, Szamecz B, Hinnebusch AG. The yeast eIF3 subunits TIF32/a, NIP1/c, and eIF5 make critical connections with the 40S ribosome in vivo. Genes Dev 2003; 17(6), 786-99; PMID:12651896; http://dx.doi.org/10.1101/gad.1065403
  • Valásek L, Nielsen KH, Zhang F, Fekete CA, Hinnebusch AG. Interactions of eukaryotic translation initiation factor 3 (eIF3) subunit NIP1/c with eIF1 and eIF5 promote preinitiation complex assembly and regulate start codon selection. Mol Cell Biol 2004; 24(21):9437-55; PMID:15485912; http://dx.doi.org/10.1128/MCB.24.21.9437-9455.2004
  • Siridechadilok B, Fraser CS, Hall RJ, Doudna JA, Nogales E. Structural roles for human translation factor eIF3 in initiation of protein synthesis. Science 2005; 310(5753):1513-5; PMID:16322461; http://dx.doi.org/10.1126/science.1118977
  • Sun C, Querol-Audí J, Mortimer SA, Arias-Palomo E, Doudna JA, Nogales E, Cate JH. Two RNA-binding motifs in eIF3 direct HCV IRES-dependent translation. Nucleic Acids Res 2013; 41(15):7512-21; PMID:23766293; http://dx.doi.org/10.1093/nar/gkt510
  • Ban N, Beckmann R, Cate JH, Dinman JD, Dragon F, Ellis SR, Lafontaine DL, Lindahl L, Liljas A, Lipton JM, et al. A new system for naming ribosomal proteins. Curr Opin Struct Biol 2014; 24:165-69; PMID:24524803; http://dx.doi.org/10.1016/j.sbi.2014.01.002
  • Kouba T, Dányi I, Gunišová S, Munzarová V, Vlčková V, Cuchalová L, Neueder A, Milkereit P, Valásek LS. Small ribosomal protein RPS0 stimulates translation initiation by mediating 40S-binding of eIF3 via its direct contact with the eIF3a/TIF32 subunit. PLoS One 2012; 7(7):e40464; PMID:22792338; http://dx.doi.org/10.1371/journal.pone.0040464
  • Chiu WL, Wagner S, Herrmannová A, Burela L, Zhang F, Saini AK, Valásek L, Hinnebusch AG. The C-terminal region of eukaryotic translation initiation factor 3a (eIF3a) promotes mRNA recruitment, scanning, and, together with eIF3j and the eIF3b RNA recognition motif, selection of AUG start codons. Mol Cell Biol 2010; 30(18):4415-34; PMID:20584985; http://dx.doi.org/10.1128/MCB.00280-10
  • Nielsen KH, Szamecz B, Valásek L, Jivotovskaya A, Shin BS, Hinnebusch AG. Functions of eIF3 downstream of 48S assembly impact AUG recognition and GCN4 translational control. EMBO J 2004; 23(5):1166-77; PMID:14976554; http://dx.doi.org/10.1038/sj.emboj.7600116
  • Munzarová V, Pánek J, Gunišová S, Dányi I, Szamecz B, Valášek LS. Translation reinitiation relies on the interaction between eIF3a/TIF32 and progressively folded cis-acting mRNA elements preceding short uORFs. PLoS Genet 2011; 7(7), e1002137; PMID:21750682; http://dx.doi.org/10.1371/journal.pgen.1002137
  • Szamecz B, Rutkai E, Cuchalová L, Munzarová V, Herrmannová A, Nielsen KH, Burela L, Hinnebusch AG, Valásek L. eIF3a cooperates with sequences 5' of uORF1 to promote resumption of scanning by post-termination ribosomes for reinitiation on GCN4 mRNA. Genes Dev 2008; 22(17):2414-25; PMID:18765792; http://dx.doi.org/10.1101/gad.480508
  • Cuchalová L, Kouba T, Herrmannová A, Dányi I, Chiu WL, Valásek L. The RNA recognition motif of eukaryotic translation initiation factor 3g (eIF3g) is required for resumption of scanning of posttermination ribosomes for reinitiation on GCN4 and together with eIF3i stimulates linear scanning. Mol Cell Biol 2010; 30(19):4671-86; PMID:20679478; http://dx.doi.org/10.1128/MCB.00430-10
  • Elantak L, Wagner S, Herrmannová A, Karásková M, Rutkai E, Lukavsky PJ, Valásek L. The indispensable N-terminal half of eIF3j/HCR1 cooperates with its structurally conserved binding partner eIF3b/PRT1-RRM and with eIF1A in stringent AUG selection. J Mol Biol 2010; 396(4):1097-116; PMID:20060839; http://dx.doi.org/10.1016/j.jmb.2009.12.047
  • Lumsden T, Bentley AA, Beutler W, Ghosh A, Galkin O, Komar AA. Yeast strains with N-terminally truncated ribosomal protein S5: implications for the evolution, structure and function of the Rps5/Rps7 proteins. Nucleic Acids Res 2010; 38(4):1261-72; PMID:19969550; http://dx.doi.org/10.1093/nar/gkp1113
  • Erzberger JP, Stengel F, Pellarin R, Zhang S, Schaefer T, Aylett CHS, Cimermančič P, Boehringer D, Sali A, Aebersold R, Ban N. Molecular Architecture of the 40S,eIF1,eIF3 Translation Initiation Complex. Cell 2014; 158(5):1123-35; PMID:25171412; http://dx.doi.org/10.1016/j.cell.2014.07.044
  • Shin BS, Kim JR, Walker SE, Dong J, Lorsch JR, Dever TE. Initiation factor eIF2γ promotes eIF2-GTP-Met-tRNAi(Met) ternary complex binding to the 40S ribosome. Nat Struct Mol Biol 2011; 18(11):1227-34; PMID:22002225; http://dx.doi.org/10.1038/nsmb.2133
  • Sharifulin D, Babaylova E, Kossinova O, Bartuli Y, Graifer D, Karpova G. Ribosomal Protein S5e is Implicated in Translation Initiation through its Interaction with the N-Terminal Domain of Initiation Factor eIF2α. Chembiochem 2013; 14(16):2136-43; PMID:24106102; http://dx.doi.org/10.1002/cbic.201300318
  • Hinnebusch AG. Molecular mechanism of scanning and start codon selection in eukaryotes. Microbiol Mol Biol Rev 2011; 75(3):434-67; PMID:21885680; http://dx.doi.org/10.1128/MMBR.00008-11
  • Lomakin IB, Kolupaeva VG, Marintchev A, Wagner G, Pestova TV. Position of eukaryotic initiation factor eIF1 on the 40S ribosomal subunit determined by directed hydroxyl radical probing. Genes Dev 2003; 17(22):2786-97; PMID:14600024; http://dx.doi.org/10.1101/gad.1141803
  • Fringer JM, Acker MG, Fekete CA, Lorsch JR, Dever TE. Coupled release of eukaryotic translation initiation factors 5B and 1A from 80S ribosomes following subunit joining. Mol Cell Biol 2007; 27(6):2384-97; PMID:17242201; http://dx.doi.org/10.1128/MCB.02254-06
  • Nanda JS, Saini AK, Muñoz AM, Hinnebusch AG, Lorsch JR. Coordinated movements of eukaryotic translation initiation factors eIF1, eIF1A, and eIF5 trigger phosphate release from eIF2 in response to start codon recognition by the ribosomal preinitiation complex. J Biol Chem 2013; 288(8):5316-29; PMID:23293029; http://dx.doi.org/10.1074/jbc.M112.440693
  • Yu Y, Marintchev A, Kolupaeva VG, Unbehaun A, Veryasova T, Lai SC, Hong P, Wagner G, Hellen CU, Pestova TV. Position of eukaryotic translation initiation factor eIF1A on the 40S ribosomal subunit mapped by directed hydroxyl radical probing. Nucleic Acids Res 2009; 37(15):5167-82; PMID:19561193; http://dx.doi.org/10.1093/nar/gkp519
  • Pestova TV, Lomakin IB, Lee JH, Choi SK, Dever TE, Hellen CU. The joining of ribosomal subunits in eukaryotes requires eIF5B. Nature 2000; 403(6767):332-5; PMID:10659855; http://dx.doi.org/10.1038/35002118
  • Choi SK, Lee JH, Zoll WL, Merrick WC, Dever TE. Promotion of met-tRNAiMet binding to ribosomes by yIF2, a bacterial IF2 homolog in yeast. Science 1998; 280(5370):1757-60; PMID:9624054; http://dx.doi.org/10.1126/science.280.5370.1757
  • Kuhle B, Ficner R. eIF5B employs a novel domain release mechanism to catalyze ribosomal subunit joining. EMBO J 2014; 33(10):1177-1191; PMID:24686316; http://dx.doi.org/10.1002/embj.201387344
  • Fernández IS, Bai XC, Hussain T, Kelley AC, Lorsch JR, Ramakrishnan V, Scheres SH. Molecular architecture of a eukaryotic translational initiation complex. Science 2013; 342(6160):1240585; PMID:24200810; http://dx.doi.org/10.1126/science.1240585
  • Triana-Alonso FJ, Chakraburtty K, Nierhaus KH. The elongation factor 3 unique in higher fungi and essential for protein biosynthesis is an E site factor. J Biol Chem 1995; 270(35):20473-8; PMID:7657623; http://dx.doi.org/10.1074/jbc.270.35.20473
  • Andersen CB, Becker T, Blau M, Anand M, Halic M, Balar B, Mielke T, Boesen T, Pedersen JS, Spahn CM, et al. Structure of eEF3 and the mechanism of transfer RNA release from the E-site. Nature 2006; 443(7112):663-8; PMID:16929303; http://dx.doi.org/10.1038/nature05126
  • Galkin O, Bentley AA, Gupta S, Compton BA, Mazumder B, Kinzy TG, Merrick WC, Hatzoglou M, Pestova TV, Hellen CU, et al. Roles of the negatively charged N-terminal extension of Saccharomyces cerevisiae ribosomal protein S5 revealed by characterization of a yeast strain containing human ribosomal protein S5. RNA 2007; 13(12):2116-28; PMID:17901157; http://dx.doi.org/10.1261/rna.688207
  • Sengupta J, Nilsson J, Gursky R, Spahn CM, Nissen P, Frank J. Identification of the versatile scaffold protein RACK1 on the eukaryotic ribosome by cryo-EM. Nat Struct Mol Biol 2004; 11(10):957-62; PMID:15334071; http://dx.doi.org/10.1038/nsmb822
  • Nilsson J, Sengupta J, Frank J, Nissen P. Regulation of eukaryotic translation by the RACK1 protein: a platform for signalling molecules on the ribosome. EMBO Rep 2004; 5(12):1137-41; PMID:15577927; http://dx.doi.org/10.1038/sj.embor.7400291
  • Ghosh A, Jindal S, Bentley AA, Hinnebusch AG, Komar AA. Rps5-Rps16 communication is essential for efficient translation initiation in yeast S. cerevisiae. Nucleic Acids Res 2014; 42(13):8537-55. [epub ahead of print]; PMID:24948608; http://dx.doi.org/10.1093/nar/gku550
  • Armache JP, Jarasch A, Anger AM, Villa E, Becker T, Bhushan S, Jossinet F, Habeck M, Dindar G, Franckenberg S, et al. Cryo-EM structure and rRNA model of a translating eukaryotic 80S ribosome at 5.5-A resolution. Proc Natl Acad Sci U S A 2010; 107(46):19748-53; PMID:20980660; http://dx.doi.org/10.1073/pnas.1009999107
  • Seidelt B, Innis CA, Wilson DN, Gartmann M, Armache JP, Villa E, Trabuco LG, Becker T, Mielke T, Schulten K, et al. Structural insight into nascent polypeptide chain-mediated translational stalling. Science 2009; 326(5958):1412-5; PMID:19933110; http://dx.doi.org/10.1126/science.1177662

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.