Advanced search
Publication Cover
Emerging Therapeutic Targets Volume 5, 2001 - Issue 2
Journal homepage
41
Views
11
CrossRef citations to date
0
Altmetric
Review

Sec, drugs and rock’n’roll: antibiotic targeting of bacterial protein translocation

Anastassios Economou Institute of Molecular Biology and Biotechnology, FORTH and Department of, Biology, University of Crete, PO Box 1527, GR-711 10 Iraklio, Crete, Greece. [email protected]
Pages 141-153 | Published online: 25 Feb 2005

  • GERSTEIN M, LIN J, HEGYI H: Protein folds in the wormgenome. Pac. Symp. Biocomput. (200030–41.
  • KIHARA D, KANEHISA M: Tandem clusters ofmembrane proteins in complete genome sequences. Genome Res. (2000) 1O(6):731–743.
  • TJALSMA H, BOLHUIS A, JONGBLOED JD, BRON S, VAN DIJL JM: Signal peptide-dependent protein transport in Bacillus subtilis: a gen ome-based survey of the secretome. Microbiol. Mol. Biol. Rev. (2000) 64(3):515–547.
  • DANESE PN, SILHAVY TJ: Targeting and assembly of periplasmic and outer-membrane proteins in Escheri-chia coli. Ann. Rev. Genet. (1998) 32:59–94.
  • POHLSCHRODER M, PRINZ WA, HARTMANN E,BECKWITH J: Protein translocation in the three domains of life: variations on a theme. Cell (1997) 91 (5):563–566.
  • GRIBALDO S, CAMMARANO P: The root of the universal tree of life inferred from anciently duplicated genes encoding components of the protein-targeting machinery. j Mol. Evol. (1998) 47(5):508–516.
  • ECONOMOU A: Bacterial pre-protein translocase, mechanism and conformational dynamics of a proces-sive enzyme. Mol. Microbiol. (1998) 27(3):511–518.
  • ECONOMOU A: Following the leader: bacterial protein export through the Sec pathway. Trends Microbiol. (1999) 7 (8):315–320.
  • ECONOMOU A: Bacterial protein translocase: a unique molecular machine with an army of substrates. FEBS Lett. (2000) 476(1-2):18–21.
  • MANTING EH, DRIESSEN AJ: Escherichia coli translo-case: the unravelling of a molecular machine. Mol. Microbiol (2000) 379(2):226–238.
  • STROHL WR (Ed.): Biotechnology of antibiotics. Marcel Dekker, New York, NY (1997).
  • SWANEY SM, AOKI H, GANOZA MC, SHINABARGER DL: The oxazolidinone linezolid inhibits initiation of protein synthesis in bacteria. Antimicrob. Agents Chemother. (1998) 42(12):3251–3255.
  • NOVAK R, HENRIQUES B, CHARPENTIER E, NORMARK S, TUOMANEN E: Emergence of vancomycin tolerance in Streptococcus pneumoniae. Nature (1999) 399(6736)590–593.
  • BREITHAUPT H: The new antibiotics. Nature Biotech-nology (1999) 17:1165–1169.
  • PERSIDIS A: Antibacterial and antifungal drug discovery. Nat. Biotechnol. (1999) 17(11):1141–1142.
  • HELLINGER WC: Confronting the problem of increasing antibiotic resistance. South Med. J. (2000) 93 (9):842–848.
  • WALSH C: Molecular mechanisms that confer antibac-terial drug resistance. Nature (2000) 406 (6797):775–781.
  • TAN YT, TILLETT DJ, MCKAY IA: Molecular strategies for overcoming antibiotic resistance in bacteria. Mol. Med. Today (2000) 6(8):309–314.
  • DEDECKER BS: Allosteric drugs: thinking outside the active-site box. Chem. Biol. (2000) 7(5):R103–107.
  • ROSAMOND J, ALLSOP A: Harnessing the power of the genome in the search for new antibiotics. Science (2000) 287 (54601973–1976.
  • SEIWERT SD, STINES NAHREINI T, AIGNER S, AHN NG,UHLENBECK OC: RNA aptamers as pathway-specific MAPkinase inhibitors. Chem. Biol. (2000) 7 (10 :833–843.
  • STATHOPOULOS C, HENDRIXSON DR, THANASSI DG et al.: Secretion of virulence determinants by the general secretory pathway in Gram-negative pathogens: an evolving story. Microbes Infect. (2000) 2 (9):1061–1072.
  • STEPHENS C, SHAPIRO L: Bacterial protein secretion - a target for new antibiotics? Chem. Mol. (1997) 4 (9):637–641.
  • OLIVER DB, CABELLI RJ, DOLAN KM, JAROSIK GP: Azide-resistant mutants of Escherichia coli alter the SecA protein, an azide-sensitive component of the protein export machinery. Proc. Natl. Acad. Sci. USA (1990) 87(20:8227–82231.
  • •Identification of the first known inhibitor of SecA.
  • HALEGOUA, S, INOUYE M: Translocation and assembly of outer membrance proteins of Escherichia coli. Selective accumulation of precursors and novel assembly intermediates caused by phenethyl alcohol. Mol. Biol. (1979) 130(0:39–61.
  • SALEH FA, FREER JH: Inhibition of secretion of staphy-lococcal alpha toxin by cerulenin. J. Med. Microbiol. (1984) 18(2):205–216.
  • ALKSNE LE, BURGIO P, HU W et al.: Identification and analysis of bacterial protein secretion inhibitors utilizing a SecA-LacZ reporter fusion system. Antimi-crob. Agents Chemother. (2000) 44(6):1418–1427.
  • •First published HTS effort for Sec pathway inhibitors.
  • PAETZEL M, DALBEY RE, STRYNADKA NC: Crystal structure of a bacterial signal peptidase in complex with a beta-lactam inhibitor. Nature (1998) 396 (6707):186–190.
  • ••One of the first high resolution structures of essential Secpathway components. Signal peptidase I is the first Sec pathway enzyme to be extensively targeted for antibiotic development. The high resolution data will open new possibilities for lead optimisation.
  • HERSKOVITS AA, BOCHKAREVA ES, BIBI E: New prospects in studying the bacterial signal recognition particle pathway. Mol. Microbiol. (2000) 38 (5):927–939.
  • XU Z, KNAFELS JD, YOSHINO K: Crystal structure of the bacterial protein export chaperone SecB. Nat. Struct. Biol. (2000) 7(12):1172–1177.
  • LILL R, DOWHAN W, WICKNER W: The ATPase activity of SecA is regulated by acidic phospholipids, SecY and the leader and mature domains of precursor proteins. Cell (1990) 60(2):271–280.
  • SCHIEBEL E, DRIESSEN AJM, HARTL F-U, WICKNER W: DmH± and ATP function at different steps of the catalytic cycle of preprotein translocase. Cell (1991) 64(5): 927–939.
  • ••An elaborate dissection of the energetics of bacterial proteintranslocation that laid the foundation for much of the subsequent work.
  • MANTING EH, VAN DER DOES C, REMIGY H, ENGEL A, DRIESSEN AJ: Se cYEG assembles into a tetramer to form the active protein translocation channel. EMBO (2000) 19(5) :852–861.
  • •In-depth study of the oligomerisation state of bacterial translocase.
  • MEYER TH, MENETRET JF, BREITLING R, MILLER KR, AKEY CW, RAPOPORT TA: The bacterial SecY/E translo-cation complex forms channel-like structures similar to those of the eukaryotic Sec61p complex. j Ma Biol. (1999) 285 (4):1789–1800.
  • DUONG F, WICKNER W: Distinct catalytic roles of the SecYE, SecG and SecDFyajC subunits of preprotein translocase holoenzyme. EMBO J. (1997) 16 (10):2756–2768.
  • DUONG F, WICKNER W: The SecDFyajC domain of preprotein translocase controls preprotein movement by regulating SecA membrane cycling. EMBO J. (1997) 16(16):4871–4879.
  • SAMUELSON JC, CHEN M, JIANG F et al: YidC mediates membrane protein insertion in bacteria. Nature (2000) 406 (6796):637–641.
  • HARTL FU, LECKER S, SCHIEBEL E, HENDRICK JP, WICKNER W: The binding cascade of SecB to SecA to SecY/E mediates preprotein targeting to the E. coli plasma membrane. Cell (1990) 63(2):269–279.
  • ••Seminal paper determining the physical order of bindingaffinities that determines targeting of SecA, SecB and substrates to the translocase.
  • ECONOMOU A, WICKNER W: SecApromotes preprotein translocation by undergoing ATP-driven cycles of membrane insertion and deinsertion. Cell (1994) 78 (5):835–843.
  • •First demonstration that SecA undergoes ATP-driven confor-mational cycles into the membrane during protein transloca-tion catalysis.
  • ECONOMOU A, POGLIANO JP, BECKWITH J, OLIVER DB, WICKNER W: SecA membrane cycling at SecYEG is driven by distinct ATP binding and hydrolysis events and is regulated by SecD and SecF. Cell (1995) 83(7)1171–1181.
  • CHEN X, XU H, TAI PC: A significant fraction of functional SecA is permanently embedded in the membrane. SecA cycling on and off the membrane is not essential during protein translocation. J Chem. (1996) 271 (47):29698–29706.
  • MCGOVERN K, EHRMANN M, BECKWITH J: Decoding signals for membrane protein assembly using alkaline phosphatase fusions. EMBO J. (1991) 10(102773–2782.
  • MARGOLIN W: Green Fluorescent Protein as a Reporter for Macromolecular Localization in Bacterial Cells. METHODS (2000) 20 (1):62–72.
  • HORNEF MW, ROGGENKAMP A, GEIGER AM, HOGARDT M, JACOBI CA, HEESEMANN J: Triggering the ExoS reg-ulon of pseudomonas aeruginosa: A GFP-reporter analysis of exoenzyme (Exo) S, ExoT and ExoU synthesis. Microb. Pathog. (2000) 2 9 (6):329–343.
  • THOMAS JD, DANIEL RA, ERRINGTON J, ROBINSON C: Export of active green fluorescent protein to the periplasm by the twin-arginine translocase (Tat) pathway in Escherichia con Mol. Microbic)]. (2001) 39 (1):47–53.
  • FEILMEIER BJ, ISEMINGER G, SCHROEDER D, WEBBER H,PHILLIPS GJ: Green fluorescent protein functions as a reporter for protein localization in Escherichia coli. Bacteriol. (2000) 182 (14) :4068–4076.
  • •First report of green fluorescent protein as a marker for bacterial Sec-dependent trafficking. After further optimisa-tion, this approach holds high potential for future use in HTS.
  • WU MM, LLOPIS J, ADAMS SR et al.: Studying organellephysiology with fusion protein-targeted avidin and fluorescent biotin conjugates. Methods Enzymol. (2000) 327:546–564.
  • JANDER G, CRONAN JE JR., BECKWITH J:Biotinylation invivo as a sensitive indicator of protein secretion and membrane protein insertion. J. Bacteria (1996) 178 (1 1) 3049–3058.
  • AKIMARU J, MATSUYAMA S, TOKUDA H, MIZUSHIMA S: Reconstitution of a protein translocation system containing purified SecY, SecEand SecA from Escheri-chia coli. Proc. Natl. Acad. Sci. USA (1 9 9 1) 88 (15):6545–6549.
  • ULBRANDT ND, LONDON E, OLIVER DB: Deep penetra-tion of a portion of Escherichia coli SecA protein into model membranes is promoted by anionic phospholipids and by partial unfolding. J. Biol. Chem. (1992) 267(20:15184–15192.
  • DEN BLAAUWEN T, FEKKES P, DE WIT JG, KUIPER W,DRIESSEN AJ: Domain interactions of the peripheral preprotein Translocase subunit SecA. Biochem. (1996) 35 (37) :11994–12004.
  • BIERI C, ERNST OP, HEYSE S, HOFMANN KP, VOGEL H:Micropatterned immobilization of a G protein-coupled receptor and direct detection of G protein activation. Nat. Biotechnol (1999)17 (11):1105–1108.
  • •Powerful implementation of a surface plasmon resonance optical biosensor for the study of binding and release of a protein to its membrane-embedded receptor.
  • KARAMANOU S, VRONTOU E, SIANIDIS G et al.: A molecular switch in SecA protein couples ATP hydrolysis to protein translocation. Mol. Microbiol. (1999) 34 (5) :1133–1145.
  • DEN BLAAUWEN T, DE WIT JG, GOSKER H et al.: Inhibi-tion of preprotein translocation and reversion of the membrane inserted state of SecA by a carboxyl terminus binding mAb. Biochem. (1997) 36(309159–9168.
  • SIANIDIS G, KARAMANOU S, VRONTOU E et al.: Cross-talk between catalytic and regulatory elements in a DEAD motor domain is essential for SecA function. (2001) EMBO J 20(5):961–970.
  • •The N-domain of SecA is shown to possess essential function DEAD family motifs. The enzymological features of the ATPase cycle are attributed to defined domains of the enzyme.
  • SHIMIZU H, NISHIYAMA K, TOKUDA H: Expression of gpsA encoding biosynthetic sn-glycerol 3-phosphate dehydrogenase suppresses both the LB-phenotype of a secB null mutant and the cold-sensitive phenotype of a secG null mutant. Mol. Microbiol. (1997) 26(5):1013–1021.
  • OTVOS L JR, O I, ROGERS ME, CONSOLVO PJ et al: Interaction between heat shock proteins and antimi-crobial peptides. Biochem. (2000) 39 (46):14150–14159.
  • •Peptide antibiotics acting directly on a chaperone protein are distinct form the peptide antibiotics that disrupt bacterial membranes and may be also applicable to the Sec-system.
  • FEWELL SW, DAY BW, BRODSKY JL: Identification of anInhibitor of hsc70-mediated protein translocation and ATP hydrolysis. J. Biol. Chem. (2001) 276(2):910–914.
  • WALTER P, KEENAN R, SCHMITZ U: SRP-where the RNAand membrane worlds meet. Science (2000) 287 (5456):1212–1213.
  • SHILTON B, SVERGUN DI, VOLKOV W, KOCH MHJ, CUSACK S, ECONOMOU A: Escherichia coli SecA shape and dimensions. FEBS Lett. (1998) 436(2).277–282.
  • VAN RAAIJ MJ, ABRAHAMS JP, LESLIE AG, WALKER JE: Thestructure of bovine F1-ATPase complexed with the antibiotic inhibitor aurovertin B. Proc. Natl. Acad. ScL USA (1996) 93(14):6913–6917.
  • WEBER J, SENIOR AE: Effects of the inhibitors azide, dicyclohexylcarbodiimide and aurovertin on nucleo-tide binding to the three F1-ATPase catalytic sites measured using specific tryptophan probes. J Chem. (1998) 273(50):33210–33215.
  • TONG L, PAV S, WHITE DM et al: A highly specific inhibitor of human p38 MAP kinase binds in the ATP pocket. Nat. Struct. Biol. (1997) 4 (4) :311–316.
  • WALKER JE, SARASTE M, RUNSWICK MJ, GAY NJ: Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleo-tide binding fold. EMBO J (1982) 1 (8):945–951.
  • MCNICHOLAS P, SALAVATI R, OLIVER D: Dual regulation of Escherichia coli secA translation by distinct upstream elements. j Mot. Biol. (1997) 265 (2):128–141.
  • HERBORT M, KLEIN M, MANTING EH, DRIESSEN AJ, FREUDL R: Temporal expression of the Bacillus subtilis secA gene, encoding a central component of the preprotein translocase. J. Bacteriol. (1999) 181 (2) :493–500.
  • KOONIN EV, GORBALENYA AE: Autogenous translation regulation by Escherichia coli ATPase SecA may be mediated by an intrinsic RNA helicase activity of this protein. FEBS Lett. (1992) 298 (1):6–8.
  • PARK SK, KIM DW, CHOE J, KIM H: RNA helicase activity of Escherichia coliSecA protein. Biochem. Biophys. Res. Commun. (1997) 235(3)593–597.
  • •Demonstration of the RNA helicase activity of SecA, an enzymatic activity that can be targeted.
  • KWONG AD, KIM JL, LIN C: Structure and function of hepatitis C virus NS3 helicase. Curr. Top Microbiol. Immunol. (2000) 242:171–196.
  • YAO N, WEBER PC: Helicase, a target for novel inhibi-tors of hepatitis C virus. Antivir. Ther. (1998) 3 (Suppl. 3) 93–97.
  • DYMOCK BW, JONES PS, WILSON FX: Novel approaches to the treatment of hepatitis C virus infection. Antivir. Chem. Chemother. (2000) 11 (2) :79–96.
  • BOROWSKI P, KUEHL R, MUELLER O, HWANG LH, SCHULZE ZUR WIESCH J, SCHMITZ H: Biochemical properties of a minimal functional domain with ATP-binding activity of the NTPase/helicase of hepatitis C virus. Eur.j Biochem. (1999) 266 (3) :715–723.
  • DEAN DA: Peptide nucleic acids: versatile tools forgene therapy strategies. Adv. Drug Deliv. Rev. (2000) 44 (2-3) :81–95.
  • BASTIDE L, BOEHMER PE, VILLANI G, LEBLEU B: Inhibi-tion of a DNA-helicase by peptide nucleic acids. Nucleic Acids Res. (1999) 27(2):551–554.
  • GOOD L, NIELSEN PE: Antisense inhibition of geneexpression in bacteria by PNA targeted to mRNA. Nat. Biotechnol. (1998) 1 6 (4) :355–358.
  • GOOD L, SANDBERG R, LARSSON O, NIELSEN PE, WAHLESTEDT C: Antisense PNA effects in Escherichia coli are limited by the outer-membrane LPS layer. Microbiology (2000) 1 46 (10) :2665–2670.
  • MCCAFFERTY DG, CUDIC P, YU MK, BEHENNA DC, KRUGER R: Synergy and duality in peptide antibiotic mechanisms. Curr. Opin. Chem. Biol. (1999) 3 (6) :672–680.
  • MILLER A, WANG L, KENDALL DA: Synthetic signalpeptides specifically recognize SecA and stimulate ATPase activity in the absence of preprotein. J Chem. (1998) 273(19):11409–11412.
  • •Demonstaration of functional signal peptide binding on SecA in the absence of any other auxhilliary factors.
  • KIMURA E, AKITA M, MATSUYAMA S, MIZUSHIMA S: Determination of a region in SecA that interacts with presecretory proteins in Escherichia con J. Biol. Chem. (1991) 266(106600–6606.
  • DRIESSEN AJ: SecA, the peripheral subunit of theEscherichia coli precursor protein translocase, is functional as a dimer. Biochem. (1993) 32 (48):13190–13197.
  • HIRANO M, MATSUYAMA S, TOKUDA H: The carboxyl-terminal region is essential for Sec-A dimerization. Biochem. Biophys. Res. Commun. (1996) 229(0:90–95.
  • MCMILLAN K, ADLER M, AULD DS et al: Allosteric inhibi-tors of inducible nitric oxide synthase dimerization discovered via combinatorial chemistry. Proc. Natl. Acad. ScL USA (2000) 97 (4) :1506–1511.
  • GHOSH I, ISSAC R, CHMIELEWSKI J: Structure-function relationship in a beta-sheet peptide inhibitor of E47 dimerization and DNA binding. Bioorg. Med. Chem. (1999) 7(0:61–66.
  • ZUTSHI R, CHMIELEWSKI J: Targeting the dimerization interface for irreversible inhibition of HIV-1 protease. Bioorg. Med. Chem. Lett. (2000) 1 0 (17):1901–1903.
  • ELKIN CD, ZUCCOLA H, JOGLE JM, JOSEPH-MCCARTHY D: Computational design of D-peptide inhibitors of hepatitis delta antigen dimerization. j Comput. Aided Mol. Des. (2000) 14(8):705–718.
  • COCHRAN AG: Antagonists of protein-protein interac-tions. Chem. Biol. (2000) 7(4):R85–94.
  • ZUTSHI R, BRICKNER M, CHMIELEWSKI J: Inhibiting theassembly of protein-protein interfaces. Curr. Opin. Chem. Biol. (1998) 2(0:62–66.
  • NORMAN TC, SMITH DL, SORGER PK et al.: Geneticselection of peptide inhibitors of biological pathways. Science (1999) 285 (5427):591–595.
  • STIGERS KD, SOTH MJ, NOWICK JS: Designed moleculesthat fold to mimic protein secondary structures. Curr. Opin. Chem. Biol. (1999) 3(6):714–23.
  • WAY JC: Covalent modification as a strategy to blockprotein-protein interactions with small-molecule drugs. Curr. Opin. Chem. Biol. (2000) 4(0:40–46.
  • JOHNSON AE, VAN WAES MA: The translocon: a dynamic gateway at the ER membrane. Ann. Rev. Cell Dev. Biol. (1999) 15:799–842.
  • FLOWER AM, HINES LL, PFENNIG PL: SecGis an auxiliarycomponent of the protein export apparatus of Escherichia coli. Mol. Gen. Genet. (2000) 263 (0:131–136.
  • SUZUKI H, NISHIYAMA K, TOKUDA H: Coupled structure changes of SecA and SecG revealed by the synthetic lethality of the secAcsR11 and AsecG::kan double mutant. Mol. Mkrobiol. (1998) 29 (1):331–341.
  • POGLIANO JA, BECKWITH J: SecD and SecF facilitateprotein export in Escherichia con EMBO J. (1994) 13 (3):554–561.
  • MATSUYAMA S, FUJITA Y, MIZUSHIMA S: SecD isinvolved in the release of translocated secretory proteins from the cytoplasmic membrane of Escheri-chia coli. EMBO J (1993) 12(1):265–270.
  • •Demonstration that the periplasmic SecD domains are essential for translcoase function.
  • DEV IK, HARVEY RJ, RAY PH: Inhibition of prolipopro-tein signal peptidase by globomycin. J. Biol. Chem. (1985) 260(10):5891–5894.
  • BLACK MT, BRUTON G: Inhibitors of bacterial signalpeptidases. Curr. Pharm. Des. (1998) 4(2):133–154.
  • PAETZEL M, DALBEY RE, STRYNADKA NC: The structureand mechanism of bacterial Type I signal peptidases. A novel antibiotic target. Pharmacol. Ther. (2000) 87 (1):27–49.
  • SALAVATI R, OLIVER D: Identification of elements on Gen eX-se cA RNA of Escherichia coli r equir ed for SecA binding and secA auto-regulation. j Mol. Biol. (1997) 265 (2):142–152.
  • MITCHELL C, OLIVER D: Two distinct ATP-binding domains are needed to promote protein export by Escherichia coli SecA ATPase. Mol Microbiol (1993) 10 (3):483–497.
  • BREUKINK E, DEMEL RA, DE KORTE-KOOL G, DE KRUIJFF B: SecA insertion into phospholipids is stimulated by negatively charged lipids and inhibited by ATP: a monolayer study. Biochem. (1992) 31 (4) :1119–1124.
  • BOCHKAREVA ES, SOLOVIEVA ME, GIRSHOVICH AS: Targeting of GroEL to SecA on the cytoplasmic membrane of Escherichia coil Proc. Natl. Acad. ScL USA (1998) 95 (2):478–483.
  • MULLER JP, OZEGOWSKI J, VETTERMANN S, SWAVING J, VAN WELY KH, DRIESSENInteraction of Bacillussubtilis CsaA with SecA and precursor proteins. Biochem. j (2000) 348 (2) :367–73.
  • SCOTTI PA, URBANUS ML, BRUNNER J et al: YidC, the Escherichia coll'homolog-ue of mitochondrial Oxa1p, is a component of the Sec translocase. EMBO (2000) 19 (4):542–549.
  • http://wit.integratedgenomics.com/IGwitl Kyrpides NC, Integrated Genomics, Inc.: GOLD: Genomes on-line database. (2001).
  • www.ribotargets.com/science/ribodock_body.html Ribotargets Ltd: Research programmes and technology. (2001).
  • www.vpharm.com/NonEnhanced/AntiviralNonE.html Vertex Pharmaceuticals, Inc.: Products and Programs. (2001).
  • www.schering-plough.com/news/research/ 191999/10-28-99. html Schering-Plough, Inc.: Research news. (1999).
  • www.roche-discovery.co.uk/science/hcv.html Roche Discovery Welwyn: Science-Virology. (2000).

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:

Order Reprints Request Corporate Permissions

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:

Request Academic Permissions

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.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.