227
Views
0
CrossRef citations to date
0
Altmetric
Review Article

Amino acid arginine and adducts: autoimmune activity

References

  • Rose, W. C.; Haines, W. J.; Warner, D. T. The Amino Acid Requirements of Man. V. The Rôle of Lysine, Arginine, and Tryptophan. J. Biol. Chem. 1954, 206, 421–430.
  • Ha, Y. H.; Milner, J. A.; Corbin, J. E. Arginine Requirements in Immature Dogs. J. Nutr. 1978, 108, 203–210. DOI: 10.1093/jn/108.2.203.
  • Barbul, A.; Arginine: Biochemistry, Physiology, and Therapeutic Implications. J. Parenter. Enteral. Nutr. 1986, 10, 227–238. DOI: 10.1177/0148607186010002227.
  • Heird, W. C.; Amino Acids in Pediatric and Neonatal Nutrition. Curr. Opin. Clin. Nutr. Metab Care. 1998, 1, 73–78.
  • Pieper, G. M.; Dondlinger, L. A. Plasma and Vascular Tissue Arginine are Decreased in Diabetes: Acute Arginine Supplementation Restores Endothelium-Dependent Relaxation by Augmenting cGMP Production. J. Pharmacol. Exp. Ther. 1997, 283, 684–691.
  • Tangphao, O.; Chalon, S.; Coulston, A. M.; Moreno, H., Jr; Chan, J. R.; Cooke, J. P.; Hoffman, B. B.; Blaschke, T. F. L-Arginine and Nitric Oxide-Related Compounds in Plasma: Comparison of Normal and Arginine-Free Diets in a 24-H Crossover Study. Vasc. Med. 1999, 4, 27–32. DOI: 10.1177/1358836X9900400105.
  • Tangphao, O.; Grossmann, M.; Chalon, S.; Hoffman, B. B.; Blaschke, T. F. Pharmacokinetics of Intravenous and Oral L-Arginine in Normal Volunteers. Br. J. Clin. Pharmacol. 1999, 47, 261–266.
  • Morris, C. R.; Poljakovic, M.; Lavrisha, L.; Machado, L.; Kuypers, F. A.; Morris, S. M., Jr. Decreased Arginine Bioavailability and Increased Serum Arginase Activity in Asthma. Am. J. Respir. Crit. Care Med. 2004, 170, 148–153. DOI: 10.1164/rccm.200309-1304OC.
  • Castillo, L.; Sanchez, M.; Vogt, J.; Chapman, T. E.; DeRojas-Walker, T. C.; Tannenbaum, S. R.; Ajami, A. M.; Young, V. R. Plasma Arginine, Citrulline, and Ornithine Kinetics in Adults, with Observations on Nitric Oxide Synthesis. Am. J. Physiol. Endocrinol. Metab. 1995, 268, E360–E367. DOI: 10.1152/ajpendo.1995.268.2.E360.
  • Dejong, C. H.; Welters, C. F.; Deutz, N. E.; Heineman, E.; Soeters, P. B. Renal Arginine Metabolism in Fasted Rats with Subacute Short Bowel Syndrome. Clin. Sci. 1998, 95, 409–418. DOI: 10.1042/cs0950409.
  • Dhanakoti, S. N.; Brosnan, J. T.; Herzberg, G. R.; Brosnan, M. E. Renal Arginine Synthesis: Studies in Vitro and in Vivo. Am. J. Physiol. Endocrinol. Metab. 1990, 259, E437–E442. DOI: 10.1152/ajpendo.1990.259.3.E437.
  • Dioguardi, F. S.;. To Give or Not to Give? Lessons from the Arginine Paradox. J. Nutrigenet. Nutrigenomics. 2011, 4, 90–98. DOI: 10.1159/000327777.
  • Domenico, R.;. Pharmacology of Nitric Oxide: Molecular Mechanisms and Therapeutic Strategies. Curr. Pharm. Des. 2004, 10, 1667–1676. DOI: 10.2174/1381612043384709.
  • Featherston, W. R.; Rogers, Q. R.; Freedland, R. A. Relative Importance of Kidney and Liver in Synthesis of Arginine by the Rat. Am. J. Physiol. 1973, 224, 127–129.
  • Luiking, Y. C.; Gabriella, A. M.; Have, T.; Wolfe, R. R.; Nicolaas, E.; Deutz, P. Arginine De Novo and Nitric Oxide Production in Disease States. Am. J. Physiol. Endocrinol. Metab. 2012, 303, E1177–E1189. DOI: 10.1152/ajpendo.00284.2012.
  • Eagle, H.;. Amino Acid Metabolism in Mammalian Cell Cultures. Science. 1959, 130, 432–437. DOI: 10.1126/science.130.3373.432.
  • Jackson, M. J.; Beaudet, A. L.; O’Brien, W. E. Mammalian Urea Cycle Enzymes. Ann. Rev. Genet. 1986, 20, 431–464. DOI: 10.1146/annurev.ge.20.120186.002243.
  • Morris, S. M., Jr.;. Arginine Synthesis, Metabolism, and Transport: Regulators of Nitric Oxide Synthesis. In Cellular and Molecular Biology of Nitric Oxide; Laskin, J. D., Laskin, D. L., Eds.; Marcel Dekker, Inc.: New York, 1999; pp 57–85.
  • Windmueller, H. G.; Spaeth, A. E. Source and Fate of Circulating Citrulline. Am. J. Physiol. 1981, 241, E473–E80. DOI: 10.1152/ajpregu.1981.241.1.R36.
  • Ryall, J.; Nguyen, M.; Bendayan, M.; Shore, G. C. Expression of Nuclear Genes Encoding the Urea Cycle Enzymes, Carbamoyl-Phosphate Synthetase I and Ornithine Carbamoyl Transferase, in Rat Liver and Intestinal Mucosa. Eur. J. Biochem. 1985, 152, 287–292.
  • Levillain, O.; Hus-Citharel, A.; Morel, F.; Bankir, L. Localization of Arginine Synthesis along Rat Nephron. Am. J. Physiol. 1990, 259, F916–F23.
  • Morris, R. M.;. Arginine Metabolism: Boundaries of Our Knowledge. J. Nutr. 2007, 137, 1602s–1609s. DOI: 10.1093/jn/137.6.1602S.
  • Abumrad, N. N.; Barbul, A. The Use of Arginine in Clinical Practice. In Metabolic and Therapeutic Aspects of Amino Acids in Clinical Nutrition; Cynober, L. A., Ed.; CRC Press: Boca Raton, 2004; pp 595–611.
  • Castillo, L.; Chapman, T. E.; Sanchez, M.; Yu, Y. M.; Burke, J. F.; Ajami, A. M.; Vogt, J.; Young, V. R. Plasma Arginine and Citrulline Kinetics in Adults Given Adequate and Arginine-Free Diets. Proc. Natl. Acad. Sci. USA. 1993, 90, 7749–7753. DOI: 10.1073/pnas.90.16.7749.
  • Costa, B. P.; Martins, P.; Veríssimo, C.; Simões, M.; Tomé, M.; Grazina, M.; Pimentel, J.; Castro-Sousa, F. Argininemia and Plasma Arginine Bioavailability – Predictive Factors of Mortality in the Severe Trauma Patients? Nutr Metab. 2016, 13(1), 60. DOI: 10.1186/s12986-016-0093-y.
  • Rao, P. V. L. N. S.; Bitla, A. R. Simultaneous Determination of Arginine, Citrulline, and Asymmetric Dimethylarginine in Plasma by Reverse-Phase High-Performance Liquid Chromatography. J. Lab. Physicians. 2017, 9(4), 243–248. DOI: 10.4103/JLP.JLP_70_16.
  • Schou-Pedersen, A. M. V.; Lykkesfeldt, J. Comparison of Three Sample Preparation Procedures for the Quantification of L-Arginine, Asymmetric Dimethylarginine, and Symmetric Dimethylarginine in Human Plasma Using HPLC-FLD. J. Anal. Methods Chem. 2018, 2018, 6148515. DOI: 10.1155/2018/6148515.
  • Brown, C. M.; Becker, J. O.; Wise, P. M.; Hoofnagle, A. N. Simultaneous Determination of 6 L-Arginine Metabolites in Human and Mouse Plasma by Using Hydrophilic-Interaction Chromatography and Electrospray Tandem Mass Spectrometry. Clin. Chem. May 2011, 57(5), 701–709. DOI: 10.1373/clinchem.2010.155895.
  • Deves, R.; Boyd, C. A. R. Transporters for Cationic Amino Acids in Animal Cells: Discovery, Structure, and Function. Physiol. Rev. 1998, 78, 487–545. DOI: 10.1152/physrev.1998.78.2.487.
  • Closs, E. I.; Simon, A.; Vekony, N.; Rotmann, A. Plasma membrane transporters for arginine. J. Nutr. 2004, 134, 2752S–9S. DOI: 10.1093/jn/134.10.2752S.
  • Closs, E. I.;. Expression, Regulation and Function of Carrier Proteins for Cationic Amino Acids. Curr. Opin. Nephrol. Hypertens. 2002, 11, 99–107. DOI: 10.1097/00041552-200201000-00015.
  • Manner, C. K.; Nicholson, B.; MacLeod, C. L. CAT2 Arginine Transporter Deficiency Significantly Reduces iNOS-mediated NO Production in Astrocytes. J. Neurochem. 2003, 85, 476–482. DOI: 10.1046/j.1471-4159.2003.01695.x.
  • Nicholson, B.; Manner, C. K.; Kleeman, J.; MacLeod, C. L. Sustained Nitric Oxide Production in Macrophages Requires the Arginine Transporter CAT2. J. Biol. Chem. 2001, 276, 15881–15885. DOI: 10.1074/jbc.M010030200.
  • Nicholson, B.; Manner, C. K.; MacLeod, C. L. Cat2 L-Arginine Transporter Deficient Fibroblasts Can Sustain Nitric Oxide Production. Nitric Oxide. 2002, 7, 236–243. DOI: 10.1016/S1089-8603(02)00116-7.
  • Rothenberg, M. E.; Doepker, M. P.; Lewkowich, I. P.; Chiaramonte, M. G.; Stringer, K. F.; Finkelman, F. D.; MacLeod, C. L.; Ellies, L. G.; Zimmermann, N. Cationic Amino Acid Transporter 2 Regulates Inflammatory Homeostasis in the Lung. Proc. Natl. Acad. Sci. USA. 2006, 103, 14895–14900. DOI: 10.1073/pnas.0605478103.
  • Rath, M.; Müller, I.; Kropf, P.; Closs, E. I.; Munder, M. Metabolism via Arginase or Nitric Oxide Synthase: Two Competing Arginine Pathways in Macrophages. Front. Imm. 2014, 5, 532. DOI: 10.3389/fimmu.2014.00532.
  • Windmueller, H. G.; Spaeth, A. E. Source and Fate of Circulating Citrulline. Am. J. Physiol. Endocrinol. Metab. 1981, 241, E473–E480. DOI: 10.1152/ajpendo.1981.241.6.E473.
  • Furchgott, R. F.;. Studies on Relaxation of Rabbit Aorta by Sodium Nitrite: The Basis for the Proposal that the Acid-Activatable Inhibitory Factor from Retractor Penis Is Inorganic Nitrite and the Endothelium-Derived Relaxing Factor Is Nitric Oxide. In Vasodilatation: Vascular Smooth Muscle, Peptides, Autonomic Nerves and Endothelium; Vanhoutte, P. M., Ed.; Raven Press: New York, 1988; pp 401–414.
  • Moncada, S.; Higgs, E. A. The Discovery of Nitric Oxide and Its Role in Vascular Biology. Br. J. Pharmacol. 2006, 147(Suppl 1), S193–S201. DOI: 10.1038/sj.bjp.0706458.
  • Rabelink, A. J.;. Nobel Prize in Medicine and Physiology 1998 for the Discovery of the Role of Nitric Oxide as a Signalling Molecule. Ned. Tijdschr. Geneeskd. 1998, 142(52), 2828–2830.
  • Wu, G.; Bazer, F. W.; Davis, T. A.; Kim, S. W.; Li, P.; Marc Rhoads, J.; Carey Satterfield, M.; Smith, S. B.; Spencer, T. E.; Yin, Y. Arginine Metabolism and Nutrition in Growth, Health and Disease. Amino Acids. 2009, 37(1), 153–168. DOI: 10.1007/s00726-008-0210-y.
  • Xiong, L.; Teng, J. L.; Botelho, M. G.; Lo, R. C.; Lau, S. K.; Woo, P. C. Arginine Metabolism in Bacterial Pathogenesis and Cancer Therapy. Int J. Mol. Sci. Mar 11, 2016, 17(3), 363. DOI: 10.3390/ijms17030363.
  • Caldwell, R. B.; Toque, H. A.; Narayanan, S. P.; Caldwell, R. W. Arginase: An Old Enzyme with New Tricks. Trends Pharmacol. Sci. 2015, 36(6), 395–405. DOI: 10.1016/j.tips.2015.03.006.
  • Voloshin, I.; Hahn-Obercyger, M.; Anavi, S.; Tirosh, O. L-Arginine Conjugates of Bile Acids-A Possible Treatment for Non-Alcoholic Fatty Liver Disease. Lipids Health Dis. 2014, 13, 69. DOI: 10.1186/1476-511X-13-69.
  • Hristina, K.; Langerholc, T.; Trapecar, M. Novel Metabolic Roles of L-Arginine in Body Energy Metabolism and Possible Clinical Applications. J. Nutr. Health Aging. 2014, 18(2), 213–218. DOI: 10.1007/s12603-014-0015-5.
  • Martens, C. R.; Kuczmarski, J. M.; Lennon-Edwards, S.; Edwards, D. G. Impaired L-Arginine Uptake but Not Arginase Contributes to Endothelial Dysfunction in Rats with Chronic Kidney Disease. J. Cardiovasc. Pharmacol. 2014, 63(1), 40–48. DOI: 10.1097/FJC.0000000000000022.
  • Ralph, A. P.; Yeo, T. W.; Salome, C. M.; Waramori, G.; Pontororing, G. J.; Kenangalem, E.; Sandjaja, T. E.; Lumb, R.; Maguire, G. P.; Price, R. N.; et al. Impaired Pulmonary Nitric Oxide Bioavailability in Pulmonary Tuberculosis: Association with Disease Severity and Delayed Mycobacterial Clearance with Treatment. J. Infect. Dis. 2013, 208(4), 616–626. DOI: 10.1093/infdis/jit248.
  • Zhu, X.; Pribis, J. P.; Rodriguez, P. C.; Morris, S. M.; Vodovotz, Y.; Billiar, T. R.; Ochoa, J. B. The Central Role of Arginine Catabolism in T-Cell Dysfunction and Increased Susceptibility to Infection after Physical Injury. Ann. Surg. 2014, 259(1), 171–178. DOI: 10.1097/SLA.0b013e31828611f8.
  • Reis, O. T.; Raini, J. C.; Coradi, S. T.; Constantino, D. H. Effect of L-Arginine and L-NAME Treatments on Polymorphonuclear Leukocytes and Mononuclear Cells Influx during Tumor Growth. Acta Cir. Bras. 2009, 24(2), 107–111.
  • Aletta, J. M.; Hu, J. C. Protein Arginine Methylation in Health and Disease. Biotechnol. Annu. Rev. 2008, 14, 203–224. DOI: 10.1016/S1387-2656(08)00008-2.
  • Furchgott, R. F.; Zawadzki, J. V. The Obligatory Role of Endothelial Cells in the Relaxation of Arterial Smooth Muscle by Acetylcholine. Nature. 1980, 288, 373–376. DOI: 10.1038/288373a0.
  • Furchgott, R. F.; Cherry, P. D.; Zawadzki, J. V.; Jothianandan, D. Endothelial Cells as Mediators of Vasodilation of arteries.J. Cardiovasc. Pharmacol. 1984, 6, S336–S343. DOI: 10.1097/00005344-198406002-00008.
  • Furchgott, R. F.;. The Role of Endothelium in the Responses of Vascular Smooth Muscle to Drugs. Annu. Rev. Pharmacol. Toxicol. 1984, 24, 175–197. DOI: 10.1146/annurev.pa.24.040184.001135.
  • Stuehr, D. J.; Marletta, M. A. Mammalian Nitrate Biosynthesis: Mouse Macrophages Produce Nitrite and Nitrate in Response to Escherichia Coli Lipopolysaccharide. Proc. Natl. Acad. Sci. USA. 1985, 82, 7738–7742. DOI: 10.1073/pnas.82.22.7738.
  • Stuehr, D. J.; Marletta, M. A. Induction of Nitrite/Nitrate Synthesis in Murine Macrophages by BCG Infection, Lymphokines, or interferon-gamma. J. Immunol. 1987, 139, 518–525.
  • Bredt, D. S.; Hwang, P. M.; Glatt, C. E.; Lowenstein, C.; Reed, R. R.; Snyder, S. H. Cloned and Expressed Nitric Oxide Synthase Structurally Resembles Cytochrome P-450 Reductase. Nature. 1991, 351, 714–718. DOI: 10.1038/351714a0.
  • Lyons, C. R.; Orloff, G. J.; Cunningham, J. M. Molecular Cloning and Functional Expression of an Inducible Nitric Oxide Synthase from a Murine Macrophage Cell Line. J. Biol. Chem. 1992, 267, 6370–6374.
  • Xie, QW.; Cho, HJ.; Calaycay, J.; Mumford, R.A.; Swiderek, K.M; Lee, T.D; Ding, A.; Troso, T.; Nathan, C. Cloning and Characterization of Inducible Nitric Oxide Synthase from Mouse Macrophages. Science. 1992, 256, 225–228. DOI: 10.1126/science.1373522.
  • Michel, T.; Lamas, S. Molecular Cloning of Constitutive Endothelial Nitric Oxide Synthase: Evidence for a Family of Related Genes. J. Cardiovasc. Pharmacol. 1992, 20, S45–9. DOI: 10.1097/00005344-199204002-00014.
  • Ahmad, R.; Rasheed, Z.; Kaushal, E.; Singh, D.; Ahsan, H. Biochemical Evaluation of Human DNA-lysine Photoadduct Treated with Peroxynitrite. Toxicol. Mech. Method. 2008, 18, 589–595. DOI: 10.1080/15376510802205676.
  • Ahmad, R.; Yadav, N.; Chaudhary, K.; Heming, T.; Ahsan, H. Analysis of Human DNA-arginine Photoadduct Modified with Peroxynitrite. Nucleosides Nucleotides Nucleic Acids. 2012, 31, 377–387. DOI: 10.1080/15257770.2012.662610.
  • Ahmad, R.; Ahsan, H. Contribution of Peroxynitrite, a Reactive Nitrogen Species, in the Pathogenesis of Autoimmunity. In Autoimmune Disorders-Pathogenetic Aspects; Mavragani, C. P. Ed.; Intech Open Access Publishers: Croatia, 2011 141–196.
  • Islam, N.; Ali, R. Formation of Thymine-Lysine and Cytosine-Lysine Adducts in DNA-lysine Photoconjugate. J. Photochem. Photobiol. B. 1995, 27(2), 109–115. DOI: 10.1016/1011-1344(94)07062-S.
  • Ahsan, H.; Abdi, S.; Ali, A. Recognition of DNA-arginine Photoadduct by anti-DNA Autoantibodies in Systemic Lupus Erythematosus. Ind. J. Med. Res. 2002, 115, 201–211.
  • Dixit, K.; Ahsan, H.; Ali, A. Polydeoxyribonucleotide C Photoconjugated with Lysine or Arginine Present Unique Epitopes for Human anti-DNA Autoantibodies. Hum. Immunol. 2003, 64(9), 880–886. DOI: 10.1016/S0198-8859(03)00144-7.
  • Stollar, B. D.; Zon, G.; Pastor, R. W. A Recognition Site on Synthetic Helical Oligonucleotides for Monoclonal Antinative DNA Autoantibody. Proc. Natl. Acad. Sci. USA. 1986, 83, 4469. DOI: 10.1073/pnas.83.12.4469.
  • Stollar, B. D.;. Antibodies to DNA. CRC Crit. Rev. Biochem. 1986, 20, 1. DOI: 10.3109/10409238609115899.
  • Habib, S.; Moinuddin, Ali, R. Acquired Antigenicity of DNA after Modification with Peroxynitrite. Int. J. Biol. Macromol. 2005, 35(3–4), 221–225. DOI: 10.1016/j.ijbiomac.2005.02.005.
  • Habib, S.; Moinuddin, Ali, R. Peroxynitrite Modified DNA: A Better Antigen for Systemic Lupus Erythematosus anti-DNA Autoantibodies. Biotechnol. Appl. Biochem. 2006, 43(2), 65–70. DOI: 10.1042/BA20050156.
  • Ahmad, R.; Ahsan, H. Role of Peroxynitrite-Modified Biomolecules in the Etiopathogenesis of Systemic Lupus Erythematosus. Clin. Exp. Med. 2014, 14, 1–11. DOI: 10.1007/s10238-012-0222-5.
  • Ahmad, R.; Rasheed, Z.; Ahsan, H. Biochemical and Cellular Toxicology of Peroxynitrite: Implications in Cell Death and Autoimmune Phenomenon. Immunopharmacol. Immunotoxicol. 2009, 31(3), 388–396. DOI: 10.1080/08923970802709197.
  • Islam, N.; Ali, R. Immunological Studies on DNA-lysine Photoadduct. Biochem. Mol. Biol. Int. 1998, 45(3), 453–464.
  • Pfeifer, G. P.; You, Y. H.; Besaratinia, A. Mutations Induced by Ultraviolet Light. Mutat. Res. 2005, 571(1–2), 19–31. DOI: 10.1016/j.mrfmmm.2004.06.057.
  • Ahsan, H.;. Selfie: Autoimmunity, Boon or Bane. J. Immunoassay. Immunochem. 2017, 38(3), 235–246. DOI: 10.1080/15321819.2017.1319861.
  • Liehr, J. G.; Gladek, A.; Macatee, T.; Randerath, E.; Randerath, K. DNA Adduct Formation in Liver and Kidney of Male Syrian Hamsters Treated with Estrogen And/Or Alpha-Naphthoflavone. Carcinogenesis. 1991, 12(3), 385–389. DOI: 10.1093/carcin/12.3.385.
  • Pisetsky, D. S.; Grudier, J. P.; Gilkeson, G. S. A Role for Immunogenic DNA in the Pathogenesis of Systemic Lupus Erythematosus. Arth. Rheum. 1990, 33, 153. DOI: 10.1002/art.1780330202.
  • Hardin, J. A.;. The Lupus Autoantigens and the Pathogenesis of Systemic Lupus Erythematosus. Arth. Rheum. 1986, 29, 457–460. DOI: 10.1002/art.1780290401.
  • Klinman, D. M.; Steinberg, A. D. Inquiry into Murine and Human Lupus. Immunol. Rev. 1995, 144, 157. DOI: 10.1111/j.1600-065X.1995.tb00069.x.
  • Emlen, W.; Neibur, J.; Kadera, R. Accelerated in Vitro Apoptosis of Lymphocytes from Patients with Systemic Lupus Erythematosus. J. Immunol. 1994, 152(7), 3685–3692.
  • Vlahakos, D. V.; Foster, M. H.; Adams, S.; Katz, M.; Ucci, A. A.; Banett, K. J.; Datta, S. K.; Madaio, M. P. Anti-DNA Antibodies from Immune Deposits at Distinct Glomerular and Vascular Sites. Kidney Int. 1992, 41, 1690.
  • Ahsan, H.;. DNA–L-Arginine Adducts and Implications in Disease. In L-Arginine in Clinical Nutrition, Nutrition and Health; V.B. Patel., V.R. Preedy., R. Rajendram (Eds.) ; Springer International Publishing: Switzerland, 2017; pp. 201–212.
  • Raz, E.; Brezis, M.; Rosenmann, E. Eilat D: Anti-DNA Antibodies Bind Directly to Renal Antigens and Induce Kidney Dysfunction in the Isolated Perfused Rat Kidney. J. Immunol. 1989, 142, 3076.
  • Zamansky, G. D.;. Sunlight-Induced Pathogenesis in Systemic Lupus Erythematosus. J. Invest. Dermatol. 1985, 85, 198. DOI: 10.1111/1523-1747.ep12276644.
  • Vermeer, B. J.; Hurks, M. The Clinical Relevance of Immunosuppression by UV Irradiation. J. Photochem. Photobiol. B. 1994, 24, 149–154.
  • Arjumand, S.; Moinuddin, Ali, A. Binding Characteristics of SLE anti-DNA Autoantibodies to Modified DNA Analogs. Biochem. Mol. Biol. Int. 1997, 43, 643–653.
  • Moinuddin, Ali, A.;. SLE Autoantibodies Recognize Spermine Induced Z-Conformation of Native Calf Thymus DNA. Biochem. Mol. Biol. Int. 1996, 40, 787–797.

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.