877
Views
66
CrossRef citations to date
0
Altmetric
Review

Selective histone deacetylase small molecule inhibitors: recent progress and perspectives

, &
Pages 621-636 | Received 28 Jun 2016, Accepted 19 Dec 2016, Published online: 29 Dec 2016

References

  • Jenuwein T, Allis CD. Translating the histone code. Science. 2001;293:1074–1080.
  • Glozak MA, Sengupta N, Zhang XH, et al. Acetylation and deacetylation of non-histone proteins. Gene. 2005;363:15–23.
  • Minucci S, Pelicci PG. Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer. Nat Rev Cancer. 2006;6:38–51.
  • Mai A, Massa S, Rotili D, et al. Histone deacetylation in epigenetics: an attractive target for anticancer therapy. Med Res Rev. 2005;25:261–309.
  • Paris M, Porcelloni M, Binaschi M, et al. Histone deacetylase inhibitors: from bench to clinic. J Med Chem. 2008;51:1505–1529.
  • Marks P, Rifkind RA, Richon VM, et al. Histone deacetylases and cancer: causes and therapies. Nat Rev Cancer. 2001;1:194–202.
  • Gregoretti IV, Lee YM, Goodson HV. Molecular evolution of the histone deacetylase family: functional implications of phylogenetic analysis. J Mol Biol. 2004;338:17–31.
  • Blander G, Guarente L. The Sir2 family of protein deacetylases. Annu Rev Biochem. 2004;73:417–435.
  • De Ruijter AJ, Van Gennip AH, Caron HN, et al. Histone deacetylases (HDACs): characterization of the classical HDAC family. J Biochem. 2003;370:737–749.
  • Zupkovitz G, Tischler J, Posch M, et al. Negative and positive regulation of gene expression by mouse histone deacetylase 1. Mol Cell Biol. 2006;26:7913–7928.
  • Lagger G, O’Carrol D, Rembold M, et al. Essential function of histone deacetylase 1 in proliferation control and CDK inhibitor repression. Embo J. 2002;21:2672–2681.
  • Montgomery RL, Davis CA, Potthoff MJ, et al. Histone deacetylases 1 and 2 redundantly regulate cardiac morphogenesis, growth, and contractility. Genes Dev. 2007;21:1790–1802.
  • Zhang CL, McKinsey TA, Chang S, et al. Class II histone deacetylases act assignal-responsive repressors of cardiac hypertrophy. Cell. 2002;110:479–488.
  • Bolger TA, Yao TP. Intracellular trafficking of histone deacetylase 4 regulates neuronal cell death. J Neurosci. 2005;25:9544–9553.
  • Outeiro TF, Kontopoulos E, Altman S, et al. Sirtuin 2 inhibitors rescue α-synuclein-mediated toxicity in models of Parkinson’s disease. Science. 2007;317:516–519.
  • Ota H, Tokunaga E, Chang K, et al. Sirt1 inhibitor, Sirtinol, induces senescence-like growth arrest with attenuated Ras-MAPK signaling in human cancer cells. Oncogene. 2006;25:176–185.
  • Grant S, Easley C, Kirkpatrick P. Vorinostat. Nat Rev Drug Discov. 2007;6:21–22.
  • Nakajima H, Kim YB, Terano H, et al. FR901228, a potent antitumorantibiotic, is a novel histonedeacetylase inhibitor. Exp Cell Res. 1998;241:126–133.
  • Piekarz RL, Frye R, Turner M, et al. Phase II multiinstitutionaltrial of the histone deacetylase inhibitor romidepsin asmonotherapy for patients with cutaneous T-cell lymphoma. J Clin Oncol. 2009;27:5410–5417.
  • Bates SE, Zhan Z, Steadman K, et al. Laboratory correlates for a phase II trial of romidepsin in cutaneous and peripheral T-celllymphoma. Br J Haematol. 2010;148:256–267.
  • Foss F, Advani R, Duvic M, et al. APhase II trial of Belinostat (PXD101) in patients with relapsed orrefractory peripheral or cutaneous T-cell lymphoma. Br J Haematol. 2015;168:811–819.
  • Dong M, Ning ZQ, Xing PY, et al. Phase I study of chidamide(CS055/HBI-8000), a new histone deacetylase inhibitor, in patientswith advanced solid tumors and lymphomas. Cancer Chemother Pharmacol. 2012;69:1413–1422.
  • DeAngelo DJ, Spencer A, Bhalla KN, et al. Phase Ia/II, two-arm, openlabel,dose-escalation study of oral panobinostat administered via two dosing schedules in patients with advanced hematologic malignancies. Leukemia. 2013;27:1628–1636.
  • Avalos JL, Bever KM, Wolberger C. Mechanism of sirtuin inhibition by nicotinamide: altering the NAD+cosubstrate specificity of a Sir2 enzyme. Mol Cell. 2005;17:855–868.
  • Best JD, Carey N. Epigenetic therapies for non-oncology indications. Drug Discovery Today. 2010;15:1008–1014.
  • Bowers AA, Greshock TJ, West N, et al. Synthesis and conformation activity relationships of the peptide isosteres of FK228 and largazole. J Am Chem Soc. 2009;131:2900–2905.
  • Taori K, Paul VJ, Luesch H. Structure and activity of largazole, a potent antiproliferative agent from the Floridian marine cyanobacterium Symploca sp. J Am Chem Soc. 2008;130:1806–1807.
  • Campas-Moya C. Romidepsin for the treatment of cutaneous T-cell lymphoma. Drugs Today. 2009;45:787–795.
  • Bhansali P, Hanigan CL, Casero RA, et al. Largazole and analogues with modified metal-binding motifs targeting histone deacetylases: synthesis and biological evaluation. J Med Chem. 2011;54:7453–7463.
  • Souto JA, Vaz E, Lepore I, et al. Synthesis and biological characterization of the histone deacetylase inhibitor largazole and C7-modified analogues. J Med Chem. 2010;53:4654–4667.
  • Li X, Tu Z, Li H, et al. Biological evaluation of new largazole analogues: alteration of macrocyclic scaffold with click chemistry. ACS Med Chem Lett. 2013;4:132–136.
  • Nanjing Yoko Biomedical R&D LTD. Histone deacetylase inhibitors and synthetic method thereof and use thereof in manufacture of medicaments. US20140243501. 2014.
  • The Regents of the University of Colorado. Macrocyclic compounds useful as inhibitors of histone deacetylase. US20150010541. 2015.
  • Benelkebir H, Marie S, Hayden AL, et al. Total synthesis of largazole and analogues: HDAC inhibition, antiproliferative activity and metabolic stability. Bioorg Med Chem. 2011;19:3650–3658.
  • Chen F, Gao AH, Li J, et al. Synthesis and biological evaluation of C7-demethyl largazole analogues. ChemMedChem. 2009;4:1269–1272.
  • Georgia Tech Research Corporation. Non-Peptide macrocyclic histone deacetylase (HDAC) inhibitors and methods of making and using thereof. US20120329741. 2012.
  • Bernstein BE, Tong JK, Schreiber SL. Genomewide studies of histone deacetylase function in yeast. Proc Nat Acad Sci USA. 2000;97:13708–13713.
  • De Ruijter AJM, Van Gennip AH, Caron HN, et al. Histone deacetylases (HDACs): characterization of the classical HDAC family. Biochem J. 2003;370:737–749.
  • Lee JH, Yao Y, Mahendran A, et al. Creation of a histone deacetylase 6 inhibitor and its biological effects. Proc Natl Acad Sci USA. 2015;112:12005–12010.
  • Duvi M, Talpur R, Ni X, et al. Phase 2 trial of oral vorinostat (suberoylanilidehydroxamic acid, SAHA) for refractory cutaneous T-cell lymphoma (CTCL). Blood. 2007;109:31–39.
  • Butler LM, Zhou X, Xu WS, et al. The histone deacetylase inhibitor SAHA arrests cancer cell growth, up-regulates thioredoxin-binding protein-2, and down-regulates thioredoxin. Proc Natl Acad Sci USA. 2002;99:11700–11705.
  • Atadja P. Development of the pan-HDAC inhibitor panobinostat (LBH589): successes and challenges. Cancer Lett. 2009;280:233–241.
  • Sawas A, Radeski D, O’Connor OA. Belinostat in patients with refractory or relapsed peripheral T-cell lymphoma: a perspective reviews. Ther Adv Hematol. 2015;6:202–208.
  • Wong JC, Hong R, Schreiber SL. Structural biasing elements for in-cell histone deacetylase paralog selectivity. J Am Chem Soc. 2003;125:5586–5587.
  • Santo L, Hideshima T, Kung AL, et al. Preclinical activity, pharmacodynamic, and pharmacokinetic properties of a selective HDAC6 inhibitor, ACY-1215, in combination with bortezomib in multiple myeloma. Blood. 2012;119:2579–2589.
  • The General Hospital Corporation. Histone deacetylase 6 selective inhibitors for the treatment of bone disease. US20140378385. 2014.
  • Butler KV, Kalin J, Brochier C, et al. Rational design and simple chemistry yield a superior, neuroprotective HDAC6 inhibitor, tubastatin A. J Am Chem Soc. 2010;132:10842–10846.
  • Kalin JH, Butler KV, Akimova T, et al. Second-generation histone deacetylase 6 inhibitors enhance the immunosuppressive effects of foxp3+ T-regulatory cells. J Med Chem. 2012;55:639–651.
  • Ikerchem SL Histone deacetylase inhibitors based on derivatives of tricycle polyhydroacridine and analogs possessing fused saturated five-and seven-member rings. WO2014180984. 2014.
  • Lin X, Chen W, Qiu Z, et al. Design and Synthesis of orally bioavailable aminopyrrolidinone histone deacetylase 6 inhibitors. J Med Chem. 2015;58:2809–2820.
  • Dana-Farber Cancer Institute. Selective inhibitors for histone deacetylase 6 and method thereof. US20150197497. 2015.
  • The Trustees of Columbia University in The City of New York. Novel molecules that selectivity inhibit histone deacetylase 6 relative to histone deacetylase 1. WO2013052110. 2013.
  • Chdi Foudation. Inc. Histone deacetylase 6 inhibitors and compositions and method of thereof. WO20160031863. 2016.
  • Topo Target UK Limited. Pharmaceutical formulations of HDAC inhibitors. US20150031770. 2015.
  • Hackanson B, Rimmele L, Benkisser M, et al. HDAC6 as a target for antileukemic drugs in acute myeloid leukemia. Leuk Res. 2012;36:1055–1062.
  • Yu CW, Chang PT, Hsin LW, et al. Quinazolin-4-one derivatives as delective histone deacetylase 6 inhibitors for the treatment of Alzheimer’s disease. J Med Chem. 2013;56:6775–6791.
  • The BoardInstitute Inc. Cycloalkenyl hydroxamic acid derivatives and their use as histone deacetylase inhibitors. WO20150368221. 2015.
  • Orchid Research Laboratories Ltd. Histone deacetylase inhibitors. WO2012117421. 2012.
  • Bergman JA, Woan K, Perez-Villarroel P, et al. Selective histone deacetylase 6 inhibitors bearing substituted urea linkers inhibit melanoma cell growth. J Med Chem. 2012;55:9891–9899.
  • Tapadar S, He R, Luchini DN, et al. Isoxazole moiety in the linker region of HDAC inhibitors adjacent to the Zn-chelating group: effects on HDAC biology and antiproliferative activity. Bioorg Med Chem Lett. 2009;19:3023–3026.
  • Senger J, Melesina J, Marek M, et al. Synthesis and biological investigation of oxazole hydroxamates as highly selective histone deacetylase 6 (HDAC6) inhibitors. J Med Chem. 2016;59:1545–1555.
  • Ontoria JM, Altamura S, Di Marco A, et al. Identification of novel, selective, and stable inhibitors of class II histone deacetylases. J Med Chem. 2009;52:6782–6789.
  • Oyelere KV, Chen PC, Guerrant W, et al. Non-peptide macrocyclic histone deacetylase inhibitors. J Med Chem. 2008;52:456–458.
  • Feng T, Wang H, Su H, et al. Design, synthesis and biological evaluation of novel N-hydroxybenzamide based HDAC inhibitors. Bioorg Med Chem. 2013;1:5339–5354.
  • The General Hospital Corporation. Histone deacetylase inhibitors. WO 2016018795. 2016.
  • Orchid Research Laboratories Ltd. Novel bridged cyclic compounds as histone deacetylase inhibitors. US20110212943. 2011.
  • Orchid Research Laboratories Ltd. Histone deacetylase inhibitors for the treatment of fungal infections. WO2011058582. 2011.
  • Balasubramanian S, Ramos J, Luo W, et al. A novel histone deacetylase 8 (HDAC8)-specific inhibitor PCI-34051 induces apoptosis in T-cell lymphomas. Leukemia. 2008;22:1026–1034.
  • Pharmacyclics Inc. Uses of selective inhibitors of HDAC8 and treatment of inflammatory conditions. US20150038542. 2015.
  • Pharmacyclics Inc. Selective inhibitors of histone deacetylase. US20150320758. 2015.
  • Huang WJ, Wang YC, Chao SW, et al. Epigenetic regulation of inflammation: progressing from broad acting histone deacetylase (HDAC) inhibitors to targeting specific HDACs. Chem Med Chem. 2012;7:1815–1824.
  • Tang W, Luo T, Greenberg EF, et al. Discovery of histone deacetylase 8 selective inhibitors. Bioorg Med Chem Lett. 2011;21:2601–2605.
  • Thaler F, Colombo C, Mai C, et al. Synthesis and biological evaluation of N-hydroxyphenylacrylamides and N-hydroxypyridin-2-ylacrylamides as novel histone deacetylase inhibitors. J Med Chem. 2010;53:822–829.
  • Suzuki T, Ota Y, Ri M, et al. Rapid discovery of highly potent and selective inhibitors of histone deacetylase 8 using click chemistry to generate candidate libraries. J Med Chem. 2012;55:9562–9575.
  • Trustees of Boston University. Selective histone deacetylase 8 inhibitors. US20150352079. 2015.
  • Adegboyega Oyelere. Histone deacetylase (HDAC) inhibitors targeting prostate tumors and method of making and using thereof. US20130289085. 2013.
  • ShouguangFukang Pharmaceuticals LTD. Preparative method and use of ZYJ-D08A and its epimers as histone deacetylase inhibitors. WO2012174730. 2012.
  • Shandong University. Tyrosine derivatives as histone deacetylase inhibitors and using thereof. CN101723896. 2010.
  • Zhang Y, Feng J, Liu C, et al. Design, synthesis and preliminary activity assay of 1,2,3,4-tetrahydroisoquinoline-3-carboxylic acid derivatives as novel histone deacetylases (HDACs) inhibitors. Bioorg Med Chem. 2010;18:1761–1772.
  • Zhang Y, Feng J, Jia Y, et al. Development of tetrahydroisoquinoline-based hydroxamic acid derivatives: potent histone deacetylase inhibitors with marked in vitro and in vivo antitumor activities. J Med Chem. 2011;54:2823–2838.
  • Janssen Pharmceutica NV Histone deacetylase inhibitors in combination with proteasome inhibitors and dexamethasone. WO2013021032. 2013.
  • Acetylon PharmceuticalInc. Pyrimidine hydroxyamide compounds ashistone deacetylase inhibitors. WO2015054474 2015.
  • Chen Y, Wang X, Xiang W, et al. Development of purine-based hydroxamic acid derivatives: potent histone deacetylase inhibitors with marked in vitro and in vivo antitumor activities. J Med Chem. 2016;59:5488–5504.
  • Duan W, Li J, Inks ES, et al. Design, synthesis, and antitumor evaluation of novel histone deacetylase inhibitors equipped with a phenylsulfonylfuroxan module as a nitric oxide donor. J Med Chem. 2015;58:4325–4338.
  • Li X, Inks ES, Li X, et al. Discovery of the first N-hydroxycinnamamide-based histone deacetylase 1/3 dual inhibitors with potent oral antitumor activity. J Med Chem. 2014;57:3324–3341.
  • Zhang L, Zhang Y, Chou CJ, et al. Histone deacetylase inhibitors with enhanced enzymatic inhibition effects and potent in vitro and in vivo antitumor activities. ChemMedChem. 2014;9:638–648.
  • Chid Foundation Inc. Histone deacetylase inhibitors and compositions and methods of use thereof. US20160031863. 2016.
  • Chid Foundation Inc. Histone deacetylase inhibitors and compositions and methods of use thereof. US20160039745. 2016.
  • Lee HZ, Kwitkowski VE, Del Valle PL, et al. Belinostat for the treatment of patients with relapsed or refractory peripheral T-cell lymphoma. Clin Cancer Res. 2015;21:2666–2670.
  • Richardson PG, Laubach JP, Lonial S, et al. Panobinostat: a novel pan-deacetylase inhibitor for the treatment of relapsed or relapsed and refractory multiple myeloma. Expert Rev Anticancer Ther. 2015;15:737–748.
  • Zhou N, Moradei O, Raeppel S, et al. Discovery of N-(2-aminophenyl)-4-[(4-pyridin-3-ylpyrimidin-2-ylamino)methyl]benzamide (MGCD0103), an orally active histone deacetylase inhibitor. J Med Chem. 2008;51:4072–4075.
  • Garcia-Manero G, Minden M, Estrov Z, et al. Clinical activity and safety of the histone deacetylase inhibitor MGCD0103: results of a phase I study in patients with leukemia or myelodysplastic syndromes (MDS). J Clin Oncol. 2006;24:37S.
  • Saito A, Yamashita T, Mariko Y, et al. A synthetic inhibitor of histone deacetylase, MS-275, with marked in vivo antitumor activity against human tumors. Proc Natl Acad Sci USA. 1999;96:4592–4597.
  • Knipstein J, Gore L. Entinostat for treatment of solid tumors and hematologic malignancies. Expert Opin Invest Drugs. 2011;20:1455–1467.
  • Chou CJ, Herman D, Gottesfeld JM. Pimelic diphenylamide 106 is a slow, tight-binding inhibitor of class I histone deacetylases. J Biol Chem. 2008;283:35402–35409.
  • Bonfils C, Kalita A, Dubay M, et al. Evaluation of the pharmacodynamic effects of MGCD0103 from preclinical models to human using a novel HDAC enzyme assay. Clin Cancer Res. 2008;14:3441–3449.
  • Dedes KJ, Dedes I, Imesch P, et al. Acquired vorinostat resistance shows partial cross-resistance to ’second-generation’ HDAC inhibitors and correlates with loss of histone acetylation and apoptosis but not with altered HDAC and HAT activities. Anti-Cancer Drugs. 2009;20:321–333.
  • Matsuyama A, Shimazu T, Sumida Y, et al. In vivo destabilization of dynamic microtubules by HDAC6-mediated deacetylation. Embo J. 2002;21:6820–6831.
  • Hildmann C, Wegener D, Riester D, et al. Substrate and inhibitor specificity of class 1 and class 2 histone deacetylases. J Biotechnol. 2006;124:258–270.
  • Khan N, Jeffers M, Kumar S, et al. Determination of the class and isoform selectivity of small-molecule histone deacetylase inhibitors. Biochem J. 2008;409:581–589.
  • Qiao Z, Ren S, Li W, et al. Chidamide, a novel histone deacetylase inhibitor, synergistically enhances gemcitabine cytotoxicity in pancreatic cancer cells. Biochem Biophys Res Commun. 2013;34:95–101.
  • Shenzhen Chipscreen Biosciences Ltd. Histone deacetylase inhibitors of novel benzamide derivatives with potent differentiation and anti-proliferation activity. EP2860174. 2013.
  • The General Hospital Corporation d/b/a Massachusetts General Hospital. Inhibitors of histone deacetylase. US20150191427. 2015.
  • Repligen Corporation. Histone deacetylase inhibitor. US20140051680. 2014.
  • Jia H, Pallos J, Jacques V, et al. Histone deacetylase (HDAC) inhibitors targeting HDAC3 and HDAC1 ameliorate polyglutamine-elicited phenotypes in model systems of Huntington’s disease. Neurobiol Dis. 2012;46:351–361.
  • Plasterer HL, Deutsch EC, Belmonte M, et al. Development of frataxin gene expression measures for the evaluation of experimental treatments in Friedreich’s ataxia. PLoS One. 2013;8:e63958.
  • IRBM-Science Park SPA. Compounds for use in the treatment of parasitic disease. US20150299163. 2015.
  • Wells CE, Bhaskara S, Stengel KR, et al. Inhibition of histone deacetylase 3 causes replication stress in cutaneous T cell lymphoma. PLoS One. 2013;8:e68915.
  • Melissa M, McQuown SC, Roggea GA, et al. HDAC3-selective inhibitor enhances extinction of cocaine-seeking behavior in a persistent manner. Proc Natl Acad Sci USA. 2013;110:2647–2652.
  • Cancer Research Technology Ltd. N-(2-aminophenyl)benzamide derivatives as histone deacetylase inhibitors. US20140135327. 2014.
  • Marson M, Matthews CJ, Atkinson SJ, et al. Potent and selective inhibitors of histone deacetylase‑3 containing chiral oxazoline capping groups and a N-(2-Aminophenyl)-benzamide binding unit. J Med Chem. 2015;58:6803–6818.
  • Pavlik CM, Wong CYB, Ononye S, et al. Santacruzamate A, a potent and selective histone deacetylase inhibitor from the panamanian marine cyanobacterium cf. Symplocasp. J Nat Prod. 2013;76:2026–2033.
  • University of Connecticut. Santacruzamate A composition and analogs and methods of use. W02014018913. 2014.
  • Harrington P. 4-carboxy-benzylamino derivatives as histone deacetylase inhibitors. US20130137690. 2013.
  • Rivieccio MA, Brochier C, Willis DE, et al. HDAC6 is a target for protection and regeneration following injury in the nervous system. Proc Natl Acad Sci USA. 2009;106:19599–19604.
  • Kalin JH, Zhang H, Gaudrel-Grosay S, et al. Chiral mercaptoacetamides display enantioselective inhibition of histone deacetylase 6 and exhibit neuroprotection in cortical neuron models of oxidative stress. Chem Med Chem. 2012;7:425–439.
  • Inks ES, Josey BJ, Jesinkey SR, et al. A novel class of small molecule inhibitors of HDAC6. ACS Chem Biol. 2012;7:331–339.
  • Feldman JL, Dittenhafer-Reed KE, Denu JM. Sirtuin catalysis and regulation. J Biol Chem. 2012;287:42419–42427.
  • Bruzzone S, Del Rio A, Nencioni A. Biosynthesis and signaling of NAD+ as an emerging area for new therapeutic agents. Curr Top Med Chem. 2013;13:2905–2906.
  • The Trustees of Princeton University. Sirtuin modulators as virus production modulators. WO2012106509. 2012.
  • Zhao X, Allison D, Condon B, et al. The 2.5 Å Crystal structure of the SIRT1 catalytic domain bound toNicotinamide adenine dinucleotide (NAD+) and an indole (EX527Analogue) reveals a novel mechanism of histone deacetylase inhibition. J Med Chem. 2013;56:963–969.
  • The Regents of the University of California. Method for increasing muscle growth by blocking sirtuin activity. WO2014110399. 2014.
  • Max-Planck-Gesellschaft zur Förderung. Foam cell specific liver X receptor (LXR) alpha agonist, SIRT1 inhibitors as well as p300 inhibitors as pharmaceutically active agents. EP2759295. 2014.
  • The University of Sydney. Prenylated hydroxystilbenes. WO2012149608. 2012.
  • GlaxoSmithKline LLC. Thieno [3,2-d]pyrimidine-6-carboxamides and analogues as sirtuin modulators. WO2014138562. 2014.
  • Disch JS, Evindar G, Chiu CH, et al. Discovery of thieno[3,2-d]pyrimidine-6-carboxamides as potent Inhibitors of SIRT1, SIRT2, and SIRT3. J Med Chem. 2013;56:3666–3679.
  • Rumpf T, Schiedel M, Karaman B, et al. Selective Sirt2 inhibition by ligand-induced rearrangement of the active site. Nat Commun. 2015;6:6263.
  • Gojo I, Tan M, Fang H, et al. Translational Phase I trial of vorinostat (suberoylanilidehydroxamic acid) combined with cytarabine and etoposidein patients with relapsed, refractory, or high-risk acutemyeloid leukemia. Clin Cancer Res. 2013;19:1838–1851.
  • Glozak MA, Sengupta N, Zhang X, et al. Acetylation and deacetylation of non-histone proteins. Gene. 2005;363:15–23.
  • Miller TA, Witter DJ, Belvedere S. Histone deacetylase inhibitors. J Med Chem. 2003;46:5097–5116.

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.