592
Views
38
CrossRef citations to date
0
Altmetric
Review

Enhancing the therapeutic potential of peptide toxins

Pages 611-623 | Received 14 Dec 2016, Accepted 05 Apr 2017, Published online: 20 Apr 2017

References

  • Gongora-Benitez M, Tulla-Puche J, Albericio F. Multifaceted roles of disulfide bonds. Peptides as therapeutics. Chem Rev. 2014;114(2):901–926. .
  • Pineda SS, Undheim EA, Rupasinghe DB, et al. Spider venomics: implications for drug discovery. Future Med Chem. 2014;6(15):1699–1714.
  • Prashanth JR, Brust A, Jin AH, et al. Cone snail venomics: from novel biology to novel therapeutics. Future Med Chem. 2014;6(15):1659–1675.
  • Verdes A, Anand P, Gorson J, et al. From mollusks to medicine: a venomics approach for the discovery and characterization of therapeutics from terebridae peptide toxins. Toxins (Basel). 2016;8(4):117.
  • Durek T, Craik DJ. Therapeutic conotoxins: a US patent literature survey. Expert Opin Ther Pat. 2015;25:1159–1173.
  • Rao SS, Quigley EM, Shiff SJ, et al. Effect of linaclotide on severe abdominal symptoms in patients with irritable bowel syndrome with constipation. Clin Gastroenterol Hepatol. 2014;12(4):616–623.
  • King GF. Venoms as a platform for human drugs: translating toxins into therapeutics. Expert Opin Biol Ther. 2011;11(11):1469–1484.
  • Schmidtko A, Lotsch J, Freynhagen R, et al. Ziconotide for treatment of severe chronic pain. Lancet. 2010;375:1569–1577.
  • Zambelli VO, Pasqualoto KF, Picolo G, et al. Harnessing the knowledge of animal toxins to generate drugs. Pharmacol Res. 2016;112:30–36.
  • Chi V, Pennington MW, Norton RS, et al. Development of a sea anemone toxin as an immunomodulator for therapy of autoimmune diseases. Toxicon. 2012;59:529–546.
  • Mahato RI, Narang AS, Thoma L, et al. Emerging trends in oral delivery of peptide and protein drugs. Crit Rev Ther Drug Carrier Syst. 2003;20(2–3):153–214.
  • Kuyucak S, Norton RS. Computational approaches for designing potent and selective analogs of peptide toxins as novel therapeutics. Future Med Chem. 2014;6(15):1645–1658.
  • Rashid MH, Huq R, Tanner MR, et al. A potent and Kv1.3-selective analogue of the scorpion toxin HsTX1 as a potential therapeutic for autoimmune diseases. Sci Rep. 2014;4:4509.
  • Rashid MH, Heinzelmann G, Huq R, et al. A potent and selective peptide blocker of the Kv1.3 channel: prediction from free-energy simulations and experimental confirmation. Plos One. 2013;8(11):e78712.
  • Chang SC, Huq R, Chhabra S, et al. N-Terminally extended analogues of the K+ channel toxin from Stichodactyla helianthus as potent and selective blockers of the voltage-gated potassium channel Kv1.3. Febs J. 2015;282(12):2247–2259.
  • Shcherbatko A, Rossi A, Foletti D, et al. Engineering highly potent and selective microproteins against NaV1.7 sodium channel for treatment of pain. J Biol Chem. 2016;291(27):13974–13986.
  • Flinspach M, Xu Q, Piekarz AD, et al. Insensitivity to pain induced by a potent selective closed-state Nav1.7 inhibitor. Sci Rep. 2017;7:39662.
  • Murray JK, Qian YX, Liu B, et al. Pharmaceutical optimization of peptide toxins for ion channel targets: potent, selective, and long-lived antagonists of Kv1.3. J Med Chem. 2015;58(17):6784–6802.
  • Pallaghy PK, Nielsen KJ, Craik DJ, et al. A common structural motif incorporating a cystine knot and a triple-stranded β-sheet in toxic and inhibitory polypeptides. Protein Sci. 1994;3(10):1833–1839.
  • Moore SJ, Cochran JR. Engineering knottins as novel binding agents. Methods Enzymol. 2012;503:223–251.
  • Silverman AP, Levin AM, Lahti JL, et al. Engineered cystine-knot peptides that bind αvβ3 integrin with antibody-like affinities. J Mol Biol. 2009;385(4):1064–1075.
  • Bhardwaj G, Mulligan VK, Bahl CD, et al. Accurate de novo design of hyperstable constrained peptides. Nature. 2016;538(7625):329–335.
  • Khoo KK, Norton RS. Role of disulfide bonds in peptide and protein conformation. In: Hughes AB, ed.. Amino acids, peptides and proteins in organic chemistry. Weinheim, Germany:Wiley-VCH; 2010.
  • Robinson SD, Chhabra S, Belgi A, et al. A naturally occurring peptide with an elementary single disulfide-directed β-hairpin fold. Structure. 2016;24(2):293–299.
  • Kuang Z, Zhang MM, Gupta K, et al. Mammalian neuronal sodium channel blocker μ-conotoxin BuIIIB has a structured N-terminus that influences potency. ACS Chem Biol. 2013;8:1344−51.
  • Green BR, Zhang MM, Chhabra S, et al. Interactions of disulfide-deficient selenocysteine analogs of μ-conotoxin BuIIIB with the a-subunit of the voltage-gated sodium channel subtype 1.3. Febs J. 2014;281(13):2885–2898.
  • Okumura M, Shimamoto S, Hidaka Y. A chemical method for investigating disulfide-coupled peptide and protein folding. Febs J. 2012;279(13):2283–2295.
  • Armishaw CJ, Daly NL, Nevin ST, et al. α-selenoconotoxins, a new class of potent α7 neuronal nicotinic receptor antagonists. J Biol Chem. 2006;281(20):14136–14143.
  • Muttenthaler M, Nevin ST, Grishin AA, et al. Solving the α-conotoxin folding problem: efficient selenium-directed on-resin generation of more potent and stable nicotinic acetylcholine receptor antagonists. J Am Chem Soc. 2010;132(10):3514–3522.
  • Menting JG, Gajewiak J, MacRaild CA, et al. A minimized human insulin-receptor-binding motif revealed in a Conus geographus venom insulin. Nat Struct Mol Biol. 2016;23(10):916–920.
  • Vassilevski AA, Sachkova MY, Ignatova AA, et al. Spider toxins comprising disulfide-rich and linear amphipathic domains: a new class of molecules identified in the lynx spider Oxyopes takobius. Febs J. 2013;280(23):6247–6261.
  • Klint JK, Senff S, Saez NJ, et al. Production of recombinant disulfide-rich venom peptides for structural and functional analysis via expression in the periplasm of E. coli. Plos One. 2013;8(5):e63865.
  • Huo X, Liu Y, Wang X, et al. Co-expression of human protein disulfide isomerase (hPDI) enhances secretion of bovine follicle-stimulating hormone (bFSH) in Pichia pastoris. Protein Expr Purif. 2007;54(2):234–239.
  • Lobstein J, Emrich CA, Jeans C, et al. SHuffle, a novel Escherichia coli protein expression strain capable of correctly folding disulfide bonded proteins in its cytoplasm. Microb Cell Fact. 2012;11:56.
  • Ueda T, Akuta T, Kikuchi-Ueda T, et al. Improving the soluble expression and purification of recombinant human stem cell factor (SCF) in endotoxin-free Escherichia coli by disulfide shuffling with persulfide. Protein Expr Purif. 2016;120:99–105.
  • Sequeira AF, Turchetto J, Saez NJ, et al. Gene design, fusion technology and TEV cleavage conditions influence the purification of oxidized disulphide-rich venom peptides in Escherichia coli. Microb Cell Fact. 2017;16(1):4.
  • Turchetto J, Sequeira AF, Ramond L, et al. High-throughput expression of animal venom toxins in Escherichia coli to generate a large library of oxidized disulphide-reticulated peptides for drug discovery. Microb Cell Fact. 2017;16(1):6.
  • Gowd KH, Yarotskyy V, Elmslie KS, et al. Site-specific effects of diselenide bridges on the oxidative folding of a cystine knot peptide, ω-selenoconotoxin GVIA. Biochemistry. 2010;49(12):2741–2752.
  • Van Lierop BJ, Robinson SD, Kompella SN, et al. Dicarba α-conotoxin Vc1.1 analogues with differential selectivity for nicotinic acetylcholine and GABAB receptors. ACS Chem Biol. 2013;8(8):1815–1821.
  • Chhabra S, Belgi A, Bartels P, et al. Dicarba analogues of α-conotoxin RgIA, Structure, stability, and activity at potential pain targets. J Med Chem. 2014;57(23):9933–9944.
  • Clark RJ, Fischer H, Nevin ST, et al. The synthesis, structural characterization, and receptor specificity of the α-conotoxin Vc1.1. J Biol Chem. 2006;281(32):23254–23263.
  • Ellison M, Feng ZP, Park AJ, et al. α-RgIA, a novel conotoxin that blocks the α9α10 nAChR: structure and identification of key receptor-binding residues. J Mol Biol. 2008;377(4):1216–1227.
  • Halai R, Callaghan B, Daly NL, et al. Effects of cyclization on stability, structure, and activity of α-conotoxin RgIA at the α9α10 nicotinic acetylcholine receptor and GABAB receptor. J Med Chem. 2011;54(19):6984–6992.
  • Dekan Z, Vetter I, Daly NL, et al. α-Conotoxin ImI incorporating stable cystathionine bridges maintains full potency and identical three-dimensional structure. J Am Chem Soc. 2011;133(40):15866–15869.
  • Yap BK, Harjani JR, Leung EW, et al. Redox-stable cyclic peptide inhibitors of the SPSB2-iNOS interaction. FEBS Lett. 2016;590(6):696–704.
  • Tabor AB. The challenge of the lantibiotics: synthetic approaches to thioether-bridged peptides. Org Biomol Chem. 2011;9(22):7606–7628.
  • MacRaild CA, Illesinghe J, Van Lierop BJ, et al. Structure and activity of (2,8)-dicarba-(3,12)-cystino α-ImI, an α-conotoxin containing a nonreducible cystine analogue. J Med Chem. 2009;52(3):755–762.
  • Gleeson EC, Wang ZJ, Robinson SD, et al. Stereoselective synthesis and structural elucidation of dicarba peptides. Chem Commun (Camb). 2016;52(24):4446–4449.
  • Hu Q, Van Gaal EV, Brundel P, et al. A novel approach for the intravenous delivery of leuprolide using core-cross-linked polymeric micelles. J Control Release. 2015;205:98–108.
  • Schwendeman SP, Shah RB, Bailey BA, et al. Injectable controlled release depots for large molecules. J Control Release. 2014;190:240–253.
  • Gori A, Wang CI, Harvey PJ, et al. Stabilization of the cysteine-rich conotoxin MrIA by using a 1,2,3-triazole as a disulfide bond mimetic. Angew Chem Int Ed Engl. 2015;54(4):1361–1364.
  • Dutton JL, Bansal PS, Hogg RC, et al. A new level of conotoxin diversity, a non-native disulfide bond connectivity in α-conotoxin AuIB reduces structural definition but increases biological activity. J Biol Chem. 2002;277(50):48849–48857.
  • Grishin AA, Wang CI, Muttenthaler M, et al. α-conotoxin AuIB isomers exhibit distinct inhibitory mechanisms and differential sensitivity to stoichiometry of α3β4 nicotinic acetylcholine receptors. J Biol Chem. 2010;285(29):22254–22263.
  • Khoo KK, Gupta K, Green BR, et al. Distinct disulfide isomers of μ-conotoxins KIIIA and KIIIB block voltage-gated sodium channels. Biochemistry. 2012;51:9826–9835.
  • Norton RS, Olivera BM. Conotoxins down under. Toxicon. 2006;48(7):780–798.
  • Tietze AA, Tietze D, Ohlenschlager O, et al. Structurally diverse μ-conotoxin PIIIA isomers block sodium channel Nav1.4. Angew Chem Int Ed Engl. 2012;51(17):4058–4061.
  • Zhu Q, Liang S, Martin L, et al. Role of disulfide bonds in folding and activity of leiurotoxin I: just two disulfides suffice. Biochemistry. 2002;41(38):11488–11494.
  • Seronay RA, Fedosov AE, Astilla MA, et al. Accessing novel conoidean venoms: biodiverse lumun-lumun marine communities, an untapped biological and toxinological resource. Toxicon. 2010;56(7):1257–1266.
  • Yao S, Zhang MM, Yoshikami D, et al. Structure, dynamics, and selectivity of the sodium channel blocker μ-conotoxin SIIIA. Biochemistry. 2008;47(41):10940–10949.
  • Sher I, Chang SC, Li Y, et al. Conformational flexibility in the binding surface of the potassium channel blocker ShK. Chem Bio Chem. 2014;15(16):2402–2410.
  • Meirovitch E, Tchaicheeyan O, Sher I, et al. Structural dynamics of the potassium channel blocker ShK: SRLS analysis of 15N relaxation. J Phys Chem B. 2015;119(49):15130–15137.
  • Pennington MW, Chang SC, Chauhan S, et al. Development of highly selective Kv1.3-blocking peptides based on the sea anemone peptide ShKs. Mar Drug. 2015;13(1):529–542.
  • Pennington MW, Beeton C, Galea CA, et al. Engineering a stable and selective peptide blocker of the Kv1.3 channel in T lymphocytes. Mol Pharmacol. 2009;75(4):762–773.
  • Norton RS, Pennington MW, Beeton C. Case study 2: transforming a toxin into a therapeutic: the sea anemone potassium channel blocker ShK toxin for treatment of autoimmune diseases. In: King GF, ed. Venoms to drugs: venom as a source for the development of human therapeutics. Cambridge, UK:Royal Society of Chemistry; 2015:255–274. .
  • Tudor JE, Pallaghy PK, Pennington MW, et al. Solution structure of ShK toxin, a novel potassium channel inhibitor from a sea anemone. Nat Struct Biol. 1996;3(4):317–320.
  • White AM, Craik DJ. Discovery and optimization of peptide macrocycles. Expert Opin Drug Discov. 2016;11(12):1151–1163.
  • Hruby VJ. Design of cyclic peptides with biological activities from biologically active peptides: the case of peptide modulators of melanocortin receptors. Biopolymers. 2016;106(6):884–888.
  • Carstens BB, Clark RJ, Daly NL, et al. Engineering of conotoxins for the treatment of pain. Curr Pharm Des. 2011;17(38):4242–4253.
  • Wang CK, Craik DJ. Cyclic peptide oral bioavailability: lessons from the past. Biopolymers. 2016;106(6):901–909.
  • Santos GB, Ganesan A, Emery FS. Oral administration of peptide-based drugs: beyond Lipinski’s rule. Chem Med Chem. 2016;11(20):2245–2251.
  • Satkunanathan N, Livett B, Gayler K, et al. α-conotoxin Vc1.1 alleviates neuropathic pain and accelerates functional recovery of injured neurones. Brain Res. 2005;1059(2):149–158.
  • Clark RJ, Jensen J, Nevin ST, et al. The engineering of an orally active conotoxin for the treatment of neuropathic pain. Angew Chem Int Ed Engl. 2010;49(37):6545–6548.
  • Castro J, Harrington AM, Garcia-Caraballo S, et al. α-Conotoxin Vc1.1 inhibits human dorsal root ganglion neuroexcitability and mouse colonic nociception via GABAB receptors. Gut. 2016. PMID: 26887818.
  • Romero HK, Christensen SB, Di Cesare Mannelli L, et al. Inhibition of α9α10 nicotinic acetylcholine receptors prevents chemotherapy-induced neuropathic pain. Proc Natl Acad Sci U S A. 2017;114(10):E1825–E1832.
  • Beeton C, Wulff H, Standifer NE, et al. Kv1.3 channels are a therapeutic target for T cell-mediated autoimmune diseases. Proc Natl Acad Sci U S A. 2006;103(46):17414–17419.
  • Sullivan JK, Miranda LP, Gegg CV, et al. Selective and potent peptide inhibitors of Kv1.3. World Intellectual Property Organization 2010: WO 2010/108154 A2.
  • Marshall KM, Laval M, Sims I, et al. Retro-inverso forms of gastrin5-12 are as biologically active as glycine-extended gastrin in vitro but not in vivo. Peptides. 2015;74:16–22.
  • De La Fuente-Nunez C, Reffuveille F, Mansour SC, et al. D-enantiomeric peptides that eradicate wild-type and multidrug-resistant biofilms and protect against lethal Pseudomonas aeruginosa infections. Chem Biol. 2015;22(2):196–205.
  • Green BR, Catlin P, Zhang MM, et al. Conotoxins containing nonnatural backbone spacers: cladistic-based design, chemical synthesis, and improved analgesic activity. Chem Biol. 2007;14(4):399–407.
  • Stevens M, Peigneur S, Dyubankova N, et al. Design of bioactive peptides from naturally occurring μ-conotoxin structures. J Biol Chem. 2012;287(37):31382–31392.
  • Khoo KK, Feng ZP, Smith BJ, et al. Structure of the analgesic μ-conotoxin KIIIA and effects on the structure and function of disulfide deletion. Biochemistry. 2009;48(6):1210–1219.
  • Khoo KK, Wilson MJ, Smith BJ, et al. Lactam-stabilized helical analogues of the analgesic μ-conotoxin KIIIA. J Med Chem. 2011;54(21):7558–7566.
  • Brady RM, Baell JB, Norton RS. Strategies for the development of conotoxins as new therapeutic leads. Mar Drugs. 2013;11(7):2293–2313.
  • Fiedler B, Zhang MM, Buczek O, et al. Specificity, affinity and efficacy of ι-conotoxin RXIA, an agonist of voltage-gated sodium channels NaV1.2, 1.6 and 1.7. Biochem Pharmacol. 2008;75(12):2334–2344.
  • Aguirre TA, Teijeiro-Osorio D, Rosa M, et al. Current status of selected oral peptide technologies in advanced preclinical development and in clinical trials. Adv Drug Deliv Rev. 2016;106(Pt B):223–241.
  • Tomlinson B, Hu M, Zhang Y, et al. Investigational glucagon-like peptide-1 agonists for the treatment of obesity. Expert Opin Investig Drugs. 2016;25(10):1167–1179.
  • Caon T, Jin L, Simoes CM, et al. Enhancing the buccal mucosal delivery of peptide and protein therapeutics. Pharm Res. 2015;32(1):1–21.
  • Jin L, Boyd BJ, White PJ, et al. Buccal mucosal delivery of a potent peptide leads to therapeutically-relevant plasma concentrations for the treatment of autoimmune diseases. J Control Release. 2015;199:37–44.
  • Jin L, Boyd BJ, Larson IC, et al. Enabling noninvasive systemic delivery of the Kv1.3-blocking peptide HsTX1[R14A] via the buccal mucosa. J Pharm Sci. 2016;105(7):2173–2179.
  • Castaneda O, Sotolongo V, Amor AM, et al. Characterization of a potassium channel toxin from the Caribbean Sea anemone Stichodactyla helianthus. Toxicon. 1995;33(5):603–613.
  • Jin L, Zhou QT, Chan HK, et al. Pulmonary delivery of the Kv1.3-blocking peptide HsTX1[R14A] for the treatment of autoimmune diseases. J Pharm Sci. 2016;105(2):650–656.
  • Thwala LN, Preat V, Csaba NS. Emerging delivery platforms for mucosal administration of biopharmaceuticals: a critical update on nasal, pulmonary and oral routes. Expert Opin Drug Deliv. 2017;14(1):23–36.
  • Patton JS, Byron PR. Inhaling medicines: delivering drugs to the body through the lungs. Nat Rev Drug Discov. 2007;6(1):67–74.
  • Pagels RF, Prud’homme RK. Polymeric nanoparticles and microparticles for the delivery of peptides, biologics, and soluble therapeutics. J Control Release. 2015;219:519–535.
  • Okada H. One- and three-month release injectable microspheres of the LH-RH superagonist leuprorelin acetate. Adv Drug Deliv Rev. 1997;28(1):43–70.
  • Zhang L, Bulaj G. Converting peptides into drug leads by lipidation. Curr Med Chem. 2012;19(11):1602–1618.
  • Varamini P, Toth I. Lipid- and sugar-modified endomorphins: novel targets for the treatment of neuropathic pain. Front Pharmacol. 2013;4:155.
  • Van Witteloostuijn SB, Mannerstedt K, Wismann P, et al. Neoglycolipids for prolonging the effects of peptides: self-assembling glucagon-like peptide 1 analogues with albumin binding properties and potent in vivo efficacy. Mol Pharm. 2017;14(1):193–205.
  • Green BR, Smith M, White KL, et al. Analgesic neuropeptide W suppresses seizures in the brain revealed by rational repositioning and peptide engineering. ACS Chem Neurosci. 2011;2(1):51–56.
  • Zhan C, Li C, Wei X, et al. Toxins and derivatives in molecular pharmaceutics: drug delivery and targeted therapy. Adv Drug Deliv Rev. 2015;90:101–118.
  • Harris JM, Chess RB. Effect of PEGylation on pharmaceuticals. Nat Rev Drug Discov. 2003;2(3):214–221.
  • Kim TH, Jiang HH, Lim SM, et al. Site-specific PEGylated Exendin-4 modified with a high molecular weight trimeric PEG reduces steric hindrance and increases type 2 antidiabetic therapeutic effects. Bioconjug Chem. 2012;23(11):2214–2220.
  • Turecek PL, Bossard MJ, Schoetens F, et al. PEGylation of biopharmaceuticals: a review of chemistry and nonclinical safety information of approved drugs. J Pharm Sci. 2016;105(2):460–475.
  • Tanner MR, Tahiya RB, Huq R, et al. Prolonged immunomodulation in inflammatory arthritis using the selective Kv1.3 channel blocker HsTX1[R14A] and its PEGylated analog. Clin Immunol. 2017. PMID: 28389388.
  • Edwards W, Fung-Leung WP, Huang C, et al. Targeting the ion channel Kv1.3 with scorpion venom peptides engineered for potency, selectivity, and half-life. J Biol Chem. 2014;289(33):22704–22714.
  • Beeton C, Pennington MW, Wulff H, et al. Targeting effector memory T cells with a selective peptide inhibitor of Kv1.3 channels for therapy of autoimmune diseases. Mol Pharmacol. 2005;67(4):1369–1381.
  • Boswell CA, Tesar DB, Mukhyala K, et al. Effects of charge on antibody tissue distribution and pharmacokinetics. Bioconjug Chem. 2010;21(12):2153–2163.
  • Tarcha EJ, Chi V, Munoz-Elias EJ, et al. Durable pharmacological responses from the peptide drug ShK-186, a specific Kv1.3 channel inhibitor that suppresses T cell mediators of autoimmune disease. J Pharmacol Exp Ther. 2012;342(3):642–653.
  • Bergmann R, Kubeil M, Zarschler K, et al. Distribution and kinetics of the Kv1.3-blocking peptide HsTX1[R14A] in experimental rats. Sci Rep. 2017. accepted.
  • Osborne R. Fresh from the biotech pipeline–2012. Nat Biotechnol. 2013;31(2):100–103.
  • Fda U 2016 [ cited; Available from: http://www.fda.gov/Drugs/DevelopmentApprovalProcess/DrugInnovation/ucm430302.htm
  • Harvey AL. Toxins and drug discovery. Toxicon. 2014;92C:193–200.
  • Safavi-Hemami H, Gajewiak J, Karanth S, et al. Specialized insulin is used for chemical warfare by fish-hunting cone snails. Proc Natl Acad Sci U S A. 2015;112(6):1743–1748.
  • Robinson SD, Norton RS. Conotoxin gene superfamilies. Mar Drugs. 2014;12(12):6058–6101.
  • Prashanth JR, Lewis RJ. An efficient transcriptome analysis pipeline to accelerate venom peptide discovery and characterisation. Toxicon. 2015;107(Pt B):282–289.
  • Fautin DG 2013 [ cited; Available from: http://hercules.kgs.ku.edu/hexacoral/anemone2/documentation/stats.cfm
  • Miljanich GP. Ziconotide: neuronal calcium channel blocker for treating severe chronic pain. Curr Med Chem. 2004;11(23):3029–3040.
  • Brookes ME, Eldabe S, Batterham A. Ziconotide monotherapy: a systematic review of randomised controlled trials. Curr Neuropharmacol. 2017;15(2):217–231.
  • Russo P, Kisialiou A, Lamonaca P, et al. New drugs from marine organisms in Alzheimer’s disease. Mar Drugs. 2015;14(1):5.
  • Osteen JD, Herzig V, Gilchrist J, et al. Selective spider toxins reveal a role for the Nav1.1 channel in mechanical pain. Nature. 2016;534(7608):494–499.

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.