78
Views
158
CrossRef citations to date
0
Altmetric
Cell Growth and Development

Molecular Mechanism of Insulin-Induced Degradation of Insulin Receptor Substrate 1

, , &
Pages 1016-1026 | Received 16 Aug 2001, Accepted 13 Nov 2001, Published online: 28 Mar 2023

REFERENCES

  • Anai, M., M. Funaki, T. Ogihara, J. Terasaki, K. Inukai, H. Katagiri, Y. Fukushima, Y. Yazaki, M. Kikuchi, Y. Oka, and T. Asano. 1998. Altered expression levels and impaired steps in the pathway to phosphatidylinositol 3-kinase activation via insulin receptor substrates 1 and 2 in Zucker fatty rats. Diabetes 47: 13–23.
  • Aoki, M., E. Blazek, and P. K. Vogt. 2001. A role of the kinase mTOR in cellular transformation induced by the oncoproteins P3k and Akt. Proc. Natl. Acad. Sci. USA 98: 136–141.
  • Araki, E., M. A. Lipes, M. E. Patti, J. C. Bruning, B. Haag, 3rd, R. S. Johnson, and C. R. Kahn. 1994. Alternative pathway of insulin signalling in mice with targeted disruption of the IRS-1 gene. Nature 372: 186–190.
  • Backer, J. M., M. G. Myers, Jr., S. E. Shoelson, D. J. Chin, X. J. Sun, M. Miralpeix, P. Hu, B. Margolis, E. Y. Skolnik, J. Schlessinger, and M. F. White. 1992. Phosphatidylinositol 3"-kinase is activated by association with IRS-1 during insulin stimulation. EMBO J. 11: 3469–3479.
  • Backer, J. M., M. G. Myers, Jr., X. J. Sun, D. J. Chin, S. E. Shoelson, M. Miralpeix, and M. F. White. 1993. Association of IRS-1 with the insulin receptor and the phosphatidylinositol 3"-kinase. Formation of binary and ternary signaling complexes in intact cells. J. Biol. Chem. 268: 8204–8212.
  • Bruning, J. C., J. Winnay, S. Bonner-Weir, S. I. Taylor, D. Accili, and C. R. Kahn. 1997. Development of a novel polygenic model of NIDDM in mice heterozygous for IR and IRS-1 null alleles. Cell 88: 561–572.
  • Burgering, B. M., and P. J. Coffer. 1995. Protein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal transduction. Nature 376: 599–602.
  • Chung, J., T. C. Grammer, K. P. Lemon, A. Kazlauskas, and J. Blenis. 1994. PDGF- and insulin-dependent pp70S6k activation mediated by phosphatidylinositol-3-OH kinase. Nature 370: 71–75.
  • Ciechanover, A. 1994. The ubiquitin-proteasome proteolytic pathway. Cell 79: 13–21.
  • Ciechanover, A. 1998. The ubiquitin-proteasome pathway: on protein death and cell life. EMBO J. 17: 7151–7160.
  • Cross, D. A. E., D. R. Alessi, P. Cohen, M. Andjelkovich, and B. A. Hemmings. 1995. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378: 785–789.
  • Datta, S. R., H. Dudek, X. Tao, S. Masters, H. Fu, Y. Gotoh, and M. E. Greenberg. 1997. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91: 231–241.
  • del Peso, L., M. Gonzalez-Garcia, C. Page, R. Herrera, and G. Nunez. 1997. Interleukin-3-induced phosphorylation of BAD through the protein kinase Akt. Science 278: 687–689.
  • Del Prato, S., F. Leonetti, D. C. Simonson, P. Sheehan, M. Matsuda, and R. A. DeFronzo. 1994. Effect of sustained physiologic hyperinsulinaemia and hyperglycaemia on insulin secretion and insulin sensitivity in man. Diabetologia 37: 1025–1035.
  • Dhand, R., I. Hiles, G. Panayotou, S. Roche, M. J. Fry, I. Gout, N. F. Totty, O. Truong, P. Vicendo, K. Yonezawa, M. Kasuga, S. A. Courtneidge, and M. D. Waterfield. 1994. PI-3-kinase is a dual specificity enzyme -- autoregulation by an intrinsic protein-serine kinase activity. EMBO J. 13: 522–533.
  • Egawa, K., N. Nakashima, P. M. Sharma, H. Maegawa, Y. Nagai, A. Kashiwagi, R. Kikkawa, and J. M. Olefsky. 2000. Persistent activation of phosphatidylinositol 3-kinase causes insulin resistance due to accelerated insulin-induced insulin receptor substrate-1 degradation in 3T3-L1 adipocytes. Endocrinology 141: 1930–1935.
  • Egawa, K., P. M. Sharma, N. Nakashima, Y. Huang, E. Huver, G. R. Boss, and J. M. Olefsky. 1999. Membrane-targeted phosphatidylinositol 3-kinase mimics insulin actions and induces a state of cellular insulin resistance. J. Biol. Chem. 274: 14306–14314.
  • Feldman, R. M., C. C. Correll, K. B. Kaplan, and R. J. Deshaies. 1997. A complex of Cdc4p, Skp1p, and Cdc53p/cullin catalyzes ubiquitination of the phosphorylated CDK inhibitor Sic1p. Cell 91: 221–230.
  • Gilliland, G., S. Perrin, and H. F. Bunn. 1990. Competitive PCR for quantitation of mRNA, p. 60–75. In M. A. Innis, D. H. Geland, J. J. Sninsky, and T. J. White (ed.), PCR protocols, a guide to methods and applications. Academic Press, Inc., San Diego, Calif.
  • Gustafson, T. A., W. He, A. Craparo, C. D. Schaub, and T. J. O'Neill. 1995. Phosphotyrosine-dependent interaction of Shc and IRS-1 with the NPEY motif of the insulin receptor via a novel non-SH2 domain. Mol. Cell. Biol. 15: 2500–2508.
  • Hamel, F. G., R. G. Bennett, K. S. Harmon, and W. C. Duckworth. 1997. Insulin inhibition of proteasome activity in intact cells. Biochem. Biophys. Res. Commun. 234: 671–674.
  • Handley-Gearhart, P. M., J. S. Trausch-Azar, A. Ciechanover, and A. L. Schwartz. 1994. Rescue of the complex temperature-sensitive phenotype of Chinese hamster ovary E36ts20 cells by expression of the human ubiquitin-activating enzyme cDNA. Biochem. J. 304: 1015–1020.
  • Haruta, T., T. Uno, J. Kawahara, A. Takano, K. Egawa, P. M. Sharma, J. M. Olefsky, and M. Kobayashi. 2001. A rapamycin-sensitive pathway down-regulates insulin signaling via phosphorylation and proteasomal degradation of insulin receptor substrate-1. Mol. Endocrinol. 14: 783–794.
  • He, W., T. J. O'Neill, and T. A. Gustafson. 1995. Distinct modes of interaction of SHC and insulin receptor substrate-1 with the insulin receptor NPEY region via non-SH2 domains. J. Biol. Chem. 270: 23258–23262.
  • Iozzo, P., T. Pratipanawatr, H. Pijl, C. Vogt, V. Kumar, R. Pipek, M. Matsuda, L. J. Mandarino, K. J. Cusi, and R. A. DeFronzo. 2001. Physiological hyperinsulinemia impairs insulin-stimulated glycogen synthase activity and glycogen synthesis. Am. J. Physiol. Endocrinol. Metab. 280: E712–E719.
  • Jiang, Z. Y., Y. W. Lin, A. Clemont, E. P. Feener, K. D. Hein, M. Igarashi, T. Yamauchi, M. F. White, and G. L. King. 1999. Characterization of selective resistance to insulin signaling in the vasculature of obese Zucker (fa/fa) rats. J. Clin. Investig. 104: 447–457.
  • Kaburagi, Y., K. Momomura, R. Yamamoto-Honda, K. Tobe, Y. Tamori, H. Sakura, Y. Akanuma, Y. Yazaki, and T. Kadowaki. 1993. Site-directed mutatgenesis of the juxtamembrane domain of the human insulin receptor. J. Biol. Chem. 268: 16610–16622.
  • Kaplan, K. B., A. A. Hyman, and P. K. Sorger. 1997. Regulating the yeast kinetochore by ubiquitin-dependent degradation and Skp1p-mediated phosphorylation. Cell 91: 491–500.
  • Kerouz, N. J., D. Horsch, S. Pons, and C. R. Kahn. 1997. Differential regulation of insulin receptor substrates-1 and -2 (IRS-1 and IRS-2) and phosphatidylinositol 3-kinase isoforms in liver and muscle of the obese diabetic (ob/ob) mouse. J. Clin. Investig. 100: 3164–3172.
  • Kettelhut, I. C., S. S. Wing, and A. L. Goldberg. 1988. Endocrine regulation of protein breakdown in skeletal muscle. Diabetes Metab. Rev. 4: 751–772.
  • Kitagawa, M., S. Hatakeyama, M. Shirane, M. Matsumoto, N. Ishida, K. Hattori, I. Nakamichi, A. Kikuchi, and K. Nakayama. 1999. An F-box protein, FWD1, mediates ubiquitin-dependent proteolysis of beta-catenin. EMBO J. 18: 2401–2410.
  • Koopmans, S. J., L. Ohman, J. R. Haywood, L. J. Mandarino, and R. A. DeFronzo. 1997. Seven days of euglycemic hyperinsulinemia induces insulin resistance for glucose metabolism but not hypertension, elevated catecholamine levels, or increased sodium retention in conscious normal rats. Diabetes 46: 1572–1578.
  • Kornitzer, D., and A. Ciechanover. 2001. Modes of regulation of ubiquitin-mediated protein degradation. J. Cell Physiol. 182: 1–11.
  • Kulka, R. G., B. Raboy, R. Schuster, H. A. Parag, G. Diamond, A. Ciechanover, and M. Marcus. 1988. A Chinese hamster cell cycle mutant arrested at G2 phase has a temperature-sensitive ubiquitin-activating enzyme, E1. J. Biol. Chem. 263: 15726–15731.
  • Lee, A. V., J. L. Gooch, S. Oesterreich, R. L. Guler, and D. Yee. 2000. Insulin-like growth factor I-induced degradation of insulin receptor substrate 1 is mediated by the 26S proteasome and blocked by phosphatidylinositol 3"-kinase inhibition. Mol. Cell. Biol. 20: 1489–1496.
  • Maniatis, T. 1999. A ubiquitin ligase complex essential for the NF-kappaB, Wnt/Wingless, and Hedgehog signaling pathways. Genes Dev. 13: 505–510.
  • Meerovitch, K., S. Wing, and D. Goltzman. 1998. Proparathyroid hormone-related protein is associated with the chaperone protein BiP and undergoes proteasome-mediated degradation. J. Biol. Chem. 273: 21025–21030.
  • Meng, L., R. Mohan, B. H. Kwok, M. Elofsson, N. Sin, and C. M. Crews. 1999. Epoxomicin, a potent and selective proteasome inhibitor, exhibits in vivo antiinflammatory activity. Proc. Natl. Acad. Sci. USA 96: 10403–10408.
  • Miles, P. D., S. Li, M. Hart, O. Romeo, J. Cheng, A. Cohen, K. Raafat, A. R. Moossa, and J. M. Olefsky. 1998. Mechanisms of insulin resistance in experimental hyperinsulinemic dogs. J. Clin. Investig. 101: 202–211.
  • Myers, M. G., Jr., J. M. Backer, X. J. Sun, S. E. Shoelson, P. Hu, J. Schlessinger, M. Yoakim, B. Schaffhausen, and M. F. White. 1992. IRS-1 activates phosphatidylinositol 3"-kinase by associating with src homology 2 domains of p85. Proc. Natl. Acad. Sci. USA 89: 10350–10354.
  • Myers, M. G., Jr., Y. Zhang, G. A. Aldaz, T. Grammer, E. M. Glasheen, L. Yenush, L. M. Wang, X. J. Sun, J. Blenis, J. H. Pierce, and M. F. White. 1996. YMXM motifs and signaling by an insulin receptor substrate 1 molecule without tyrosine phosphorylation sites. Mol. Cell. Biol. 16: 4147–4155.
  • Nave, B. T., R. J. Haigh, A. C. Hayward, K. Siddle, and P. R. Shepherd. 1996. Compartment-specific regulation of phosphoinositide 3-kinase by platelet-derived growth factor and insulin in 3T3-L1 adipocytes. Biochem. J. 318: 55–60.
  • O'Neill, T. J., A. Craparo, and T. A. Gustafson. 1994. Characterization of an interaction between insulin receptor substrate-1 and the insulin receptor by using the two-hybrid system. Mol. Cell. Biol. 14: 6433–6442.
  • Ozes, O. N., H. Akca, L. D. Mayo, J. A. Gustin, T. Maehama, J. E. Dixon, and D. B. Donner. 2001. A phosphatidylinositol 3-kinase/Akt/mTOR pathway mediates and PTEN antagonizes tumor necrosis factor inhibition of insulin signaling through insulin receptor substrate-1. Proc. Natl. Acad. Sci. USA 98: 4640–4645.
  • Pagano, M. 1997. Cell cycle regulation by the ubiquitin pathway. FASEB J. 11: 1067–1075.
  • Palombella, V. J., O. J. Rando, A. L. Goldberg, and T. Maniatis. 1994. The ubiquitin-proteasome pathway is required for processing the NF-kappa B1 precursor protein and the activation of NF-kappa B. Cell 78: 773–785.
  • Patti, M. E., A. Virkamaki, E. J. Landaker, C. R. Kahn, and H. Yki-Jarvinen. 1999. Activation of the hexosamine pathway by glucosamine in vivo induces insulin resistance of early postreceptor insulin signaling events in skeletal muscle. Diabetes 48: 1562–1571.
  • Pederson, T. M., D. L. Kramer, and C. M. Rondinone. 2001. Serine/threonine phosphorylation of IRS-1 triggers its degradation: possible regulation by tyrosine phosphorylation. Diabetes 50: 24–31.
  • Rice, K. M., M. A. Turnbow, and C. W. Garner. 1993. Insulin stimulates the degradation of IRS-1 in 3T3-L1 adipocytes. Biochem. Biophys. Res. Commun. 190: 961–967.
  • Ricort, J. M., J. F. Tanti, E. Van Obberghen, and Y. Le Marchand-Brustel. 1995. Alterations in insulin signalling pathway induced by prolonged insulin treatment of 3T3-L1 adipocytes. Diabetologia 38: 1148–1156.
  • Ricort, J. M., J. F. Tanti, E. Van Obberghen, and Y. Le Marchand-Brustel. 1996. Different effects of insulin and platelet-derived growth factor on phosphatidylinositol 3-kinase at the subcellular level in 3T3-L1 adipocytes. A possible explanation for their specific effects on glucose transport. Eur. J. Biochem. 239: 17–22.
  • Rommel, C., B. A. Clarke, S. Zimmermann, L. Nunez, R. Rossman, K. Reid, K. Moelling, G. D. Yancopoulos, and D. J. Glass. 1999. Differentiation stage-specific inhibition of the Raf-MEK-ERK pathway by Akt. Science 286: 1738–1741.
  • Rondinone, C. M., L. M. Wang, P. Lonnroth, C. Wesslau, J. H. Pierce, and U. Smith. 1997. Insulin receptor substrate (IRS) 1 is reduced and IRS-2 is the main docking protein for phosphatidylinositol 3-kinase in adipocytes from subjects with non-insulin-dependent diabetes mellitus. Proc. Natl. Acad. Sci. USA 94: 4171–4175.
  • Rordorf-Nikolic, T., D. J. Van Horn, D. Chen, M. F. White, and J. M. Backer. 1995. Regulation of phosphatidylinositol 3-kinase by tyrosyl phosphoproteins. Full activation requires occupancy of both SH2 domains in the 85 kDa regulatory subunit. J. Biol. Chem. 270: 3662–3666.
  • Saad, M. J., E. Araki, M. Miralpeix, P. L. Rothenberg, M. F. White, and C. R. Kahn. 1992. Regulation of insulin receptor substrate-1 in liver and muscle of animal models of insulin resistance. J. Clin. Investig. 90: 1839–1849.
  • Saad, M. J., F. Folli, and C. R. Kahn. 1995. Insulin and dexamethasone regulate insulin receptors, insulin receptor substrate-1, and phosphatidylinositol 3-kinase in Fao hepatoma cells. Endocrinology 136: 1579–1588.
  • Sabatini, D. M., H. Erdjument-Bromage, M. Lui, P. Tempst, and S. H. Snyder. 1994. RAFT1: A mammalian protein that binds to FKBP12 in a rapamycin-dependent fashion and is homologous to yeast TORs. Cell 78: 35–43.
  • Schmelzle, T., and M. N. Hall. 2001. TOR, a central controller of cell growth. Cell 103: 253–262.
  • Singh, T. J. 1993. Insulin receptor serine kinase activation by casein kinase 2 and a membrane tyrosine kinase. Mol. Cell. Biochem. 121: 167–174.
  • Skowyra, D., K. L. Craig, M. Tyers, S. J. Elledge, and J. W. Harper. 1997. F-box proteins are receptors that recruit phosphorylated substrates to the SCF ubiquitin-ligase complex. Cell 91: 209–219.
  • Smith, L. K., M. Bradshaw, D. E. Croall, and C. W. Garner. 1993. The insulin receptor substrate (IRS-1) is a PEST protein that is susceptible to calpain degradation in vitro. Biochem. Biophys. Res. Commun. 196: 767–772.
  • Smith, L. K., K. M. Rice, and C. W. Garner. 1996. The insulin-induced down-regulation of IRS-1 in 3T3-L1 adipocytes is mediated by a calcium-dependent thiol protease. Mol. Cell. Endocrinol. 122: 81–92.
  • Smith, L. K., C. J. Vlahos, K. K. Reddy, J. R. Falck, and C. W. Garner. 1995. Wortmannin and LY294002 inhibit the insulin-induced down-regulation of IRS-1 in 3T3-L1 adipocytes. Mol. Cell. Endocrinol. 113: 73–81.
  • Spencer, E., J. Jiang, and Z. J. Chen. 1999. Signal-induced ubiquitination of IkappaBalpha by the F-box protein Slimb/beta-TrCP. Genes Dev. 13: 284–294.
  • Stephens, J. M., J. Lee, and P. F. Pilch. 1997. Tumor necrosis factor-alpha-induced insulin resistance in 3T3-L1 adipocytes is accompanied by a loss of insulin receptor substrate-1 and GLUT4 expression without a loss of insulin receptor-mediated signal transduction. J. Biol. Chem. 272: 971–976.
  • Stephens, L., K. Anderson, D. Stokoe, H. Erdjument-Bromage, G. F. Painter, A. B. Holmes, P. R. J. Gaffney, C. B. Reese, F. McCormick, P. Tempst, J. Coadwell, P. T. Hawkins, and P. R. Gaffney. 1998. Protein kinase B kinases that mediate phosphatidylinositol 3,4,5-trisphosphate-dependent activation of protein kinase B. Science 279: 710–714.
  • Stokoe, D., L. R. Stephens, T. Copeland, P. R. Gaffney, C. B. Reese, G. F. Painter, A. B. Holmes, F. McCormick, and P. T. Hawkins. 1997. Dual role of phosphatidylinositol-3,4,5-trisphosphate in the activation of protein kinase B. Science 277: 567–570.
  • Sun, X. J., J. L. Goldberg, L. Y. Qiao, and J. J. Mitchell. 1999. Insulin-induced insulin receptor substrate-1 degradation is mediated by the proteasome degradation pathway. Diabetes 48: 1359–1364.
  • Sun, X. J., M. Miralpeix, M. G. Myers, Jr., E. M. Glasheen, J. M. Backer, C. R. Kahn, and M. F. White. 1992. The expression and function of IRS-1 in insulin signal transmission. J. Biol. Chem. 267: 22662–22672.
  • Sun, X. J., S. Pons, L.-M. Wang, Y. Zhang, L. Yenush, D. Burks, M. G. Myers, Jr., E. M. Glasheen, N. G. Copeland, N. A. Jenkins, J. H. Pierce, and M. F. White. 1997. The IRS-2 gene on murine chromosome 8 encodes a unique signaling adapter for insulin and cytokine action. Mol. Endocrinol. 11: 251–262.
  • Sun, X. J., L. M. Wang, Y. Zhang, L. Yenush, M. G. Myers, Jr., E. Glasheen, W. S. Lane, J. H. Pierce, and M. F. White. 1995. Role of IRS-2 in insulin and cytokine signalling. Nature 377: 173–177.
  • Takano, A., I. Usui, T. Haruta, J. Kawahara, T. Uno, M. Iwata, and M. Kobayashi. 2001. Mammalian target of rapamycin pathway regulates insulin signaling via subcellular redistribution of insulin receptor substrate 1 and integrates nutritional signals and metabolic signals of insulin. Mol. Cell. Biol. 21: 5050–5062.
  • Tamemoto, H., T. Kadowaki, K. Tobe, T. Yagi, H. Sakura, T. Hayakawa, Y. Terauchi, K. Ueki, Y. Kaburagi, S. Satoh, H. Sekihara, S. Yoshioka, H. Horikoshi, Y. Furuta, Y. Ikawa, M. Kasuga, Y. Yazaki, and S. Aizawa. 1994. Insulin resistance and growth retardation in mice lacking insulin receptor substrate-1. Nature 372: 182–186.
  • Tanti, J. F., T. Gremeaux, E. Van Obberghen, and Y. Le Marchand-Brustel. 1994. Insulin receptor substrate 1 is phosphorylated by the serine kinase activity of phosphatidylinositol 3-kinase. Biochem. J. 304: 17–21.
  • Vanhaesebroeck, B., K. Higashi, C. Raven, M. Welham, S. Anderson, P. Brennan, S. G. Ward, and M. D. Waterfield. 1999. Autophosphorylation of p110delta phosphoinositide 3-kinase: a new paradigm for the regulation of lipid kinases in vitro and in vivo. EMBO J. 18: 1292–1302.
  • Verma, R., R. S. Annan, M. J. Huddleston, S. A. Carr, G. Reynard, and R. J. Deshaies. 1997. Phosphorylation of Sic1p by G1 Cdk required for its degradation and entry into S phase. Science 278: 455–460.
  • Virkamaki, A., K. Ueki, and C. R. Kahn. 1999. Protein-protein interaction in insulin signaling and the molecular mechanisms of insulin resistance. J. Clin. Investig. 103: 931–943.
  • White, M. F. 1996. The IRS-signalling system in insulin and cytokine action. Phil. Trans. R. Soc. Lond. Ser. B Biol. Sci. 351: 181–189.
  • White, M. F. 1997. The insulin signalling system and the IRS proteins. Diabetologia 40(Suppl. 2): S2–S17.
  • White, M. F. 1998. The IRS-signaling system: a network of docking proteins that mediate insulin and cytokine action. Recent Prog. Hormone Res. 53: 119–138.
  • White, M. F., J. N. Livingston, J. M. Backer, V. Lauris, T. J. Dull, A. Ullrich, and C. R. Kahn. 1988. Mutation of the insulin receptor at tyrosine 960 inhibits signal transmission but does not affect its tyrosine kinase activity. Cell 54: 641–649.
  • Wiese, R. J., C. C. Mastick, D. F. Lazar, and A. R. Saltiel. 1995. Activation of mitogen-activated protein kinase and phosphatidylinositol 3"-kinase is not sufficient for the hormonal stimulation of glucose uptake, lipogenesis, or glycogen synthesis in 3T3-L1 adipocytes. J. Biol. Chem. 270: 3442–3446.
  • Withers, D. J., D. J. Burks, H. H. Towery, S. L. Altamuro, C. L. Flint, and M. F. White. 1999. Irs-2 coordinates Igf-1 receptor-mediated beta-cell development and peripheral insulin signalling. Nat. Genet. 23: 32–40.
  • Withers, D. J., J. S. Gutierrez, H. Towery, D. J. Burks, J. M. Ren, S. Previs, Y. Zhang, D. Bernal, S. Pons, G. I. Shulman, S. Bonner-Weir, and M. F. White. 1998. Disruption of IRS-2 causes type 2 diabetes in mice. Nature 391: 900–904.
  • Zhang, H., H. Hoff, and C. Sell. 2000. Insulin-like growth factor 1-mediated degradation of insulin receptor substrate-1 is inhibited by epidermal growth factor (EGF) in prostate epithelial cells. J. Biol. Chem. 275: 22558–22562.
  • Zimmermann, S., and K. Moelling. 1999. Phosphorylation and regulation of Raf by Akt (protein kinase B). Science 286: 1741–1744.

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.