905
Views
17
CrossRef citations to date
0
Altmetric
Review Article

Advances in directed molecular evolution of reporter genes

, , , , &
Pages 133-142 | Received 10 Dec 2010, Accepted 31 May 2011, Published online: 21 Jul 2011

References

  • Abbyad P, Childs W, Shi X, Boxer SG. (2007). Dynamic Stokes shift in green fluorescent protein variants. Proc Natl Acad Sci USA, 104, 20189–20194.
  • Ai HW, Henderson JN, Remington SJ, Campbell RE. (2006). Directed evolution of a monomeric, bright and photostable version of Clavularia cyan fluorescent protein: structural characterization and applications in fluorescence imaging. Biochem J, 400, 531–540.
  • Alwen A, Moreno RMB, Vicente O, Heberle-Bors E. (1992). Plant endogenous activity: how to avoid interference with the use of E.coli β-glucuronidase as a reporter gene in transgenic plants. Transgenic Res, 1, 63–70.
  • Ang EL, Obbard JP, Zhao H. (2009). Directed evolution of aniline dioxygenase for enhanced bioremediation of aromatic amines. Appl Microbiol Biotechnol, 81, 1063–1070.
  • Baird GS, Zacharias DA, Tsien RY. (2000). Biochemistry, mutagenesis, and oligomerization of DsRed, a red fluorescent protein from coral. Proc Natl Acad Sci USA, 97, 11984–11989.
  • Bekkaoui F, Pilon M, Laine E, Raju DSS, Crosby WL, Dunstan DI. (1988). Transient gene expression in electroporated Picea glauca protoplasts. Plant Cell Rep, 7, 481–484.
  • Bevis BJ, Glick BS. (2002). Rapidly maturing variants of the Discosoma red fluorescent protein (DsRed). Nat Biotechnol, 20, 83–87.
  • Callanan MJ, Russell WM, Klaenhammer TR. (2007). Modification of Lactobacillus beta-glucuronidase activity by random mutagenesis. Gene, 389, 122–127.
  • Campbell RE, Tour O, Palmer AE, Steinbach PA, Baird GS, Zacharias DA, Tsien RY. (2002). A monomeric red fluorescent protein. Proc Natl Acad Sci USA, 99, 7877–7882.
  • Castle LA, Siehl DL, Gorton R, Patten PA, Chen YH, Bertain S, Cho HJ, Duck N, Wong J, Liu D, Lassner MW. (2004). Discovery and directed evolution of a glyphosate tolerance gene. Science, 304, 1151–1154.
  • Chalfie M, Tu Y, Euskirchen G, Ward WW, Prasher DC. (1994). Green fluorescent protein as a marker for gene expression. Science, 263, 802–805.
  • Christians FC, Scapozza L, Crameri A, Folkers G, Stemmer WP. (1999). Directed evolution of thymidine kinase for AZT phosphorylation using DNA family shuffling. Nat Biotechnol, 17, 259–264.
  • Cormack BP, Valdivia RH, Falkow S. (1996). FACS-optimized mutants of the green fluorescent protein (GFP). Gene, 173, 33–38.
  • Crameri A, Whitehorn EA, Tate E, Stemmer WP. (1996). Improved green fluorescent protein by molecular evolution using DNA shuffling. Nat Biotechnol, 14, 315–319.
  • Craveiro KI, Gomes Jú,nior JE, Silva MC, Macedo LL, Lucena WA, Silva MS, de Souza Jú,nior JD, Oliveira GR, de Magalhães MT, Santiago AD, Grossi-de-Sa MF. (2010). Variant Cry1Ia toxins generated by DNA shuffling are active against sugarcane giant borer. J Biotechnol, 145, 215–221.
  • Dixon DP, McEwen AG, Lapthorn AJ, Edwards R. (2003). Forced evolution of a herbicide detoxifying glutathione transferase. J Biol Chem, 278, 23930–23935.
  • Dupuy LC, Locher CP, Paidhungat M, Richards MJ, Lind CM, Bakken R, Parker MD, Whalen RG, Schmaljohn CS. (2009). Directed molecular evolution improves the immunogenicity and protective efficacy of a Venezuelan equine encephalitis virus DNA vaccine. Vaccine, 27, 4152–4160.
  • Endow SA. (2001). Green fluorescent protein as a tag for molecular motor proteins. Methods Mol Biol, 164, 123–131.
  • Fior S, Vianelli A, Gerola PD. (2009a). A novel method for fluorometric continuous measurement of β-glucuronidase (GUS) activity using 4-methyl-umbelliferyl- β-D-glucuronide (MUG) as substrate. Plant Sci, 176, 130–135.
  • Fior S, Gerola PD. (2009b). Impact of ubiquitous inhibitors on the GUS gene reporter system: evidence from the model plants Arabidopsis, tobacco and rice and correction methods for quantitative assays of transgenic and endogenous GUS. Plant Methods, 5, 19.
  • Flores H, Ellington AD. (2002). Increasing the thermal stability of an oligomeric protein, beta-glucuronidase. J Mol Biol, 315, 325–327.
  • Fradkov AF, Chen Y, Ding L, Barsova EV, Matz MV, Lukyanov SA. (2000). Novel fluorescent protein from Discosoma coral and its mutants possesses a unique far-red fluorescence. FEBS Lett, 479, 127–130.
  • Geddie ML, Matsumura I. (2004). Rapid evolution of beta-glucuronidase specificity by saturation mutagenesis of an active site loop. J Biol Chem, 279, 26462–26468.
  • Gilissen LJ, Metz PL, Stiekema WJ, Nap JP. (1998). Biosafety of E. coli beta-glucuronidase (GUS) in plants. Transgenic Res, 7, 157–163.
  • Griesbeck O, Baird GS, Campbell RE, Zacharias DA, Tsien RY. (2001). Reducing the environmental sensitivity of yellow fluorescent protein. Mechanism and applications. J Biol Chem, 276, 29188–29194.
  • Gross LA, Baird GS, Hoffman RC, Baldridge KK, Tsien RY. (2000). The structure of the chromophore within DsRed, a red fluorescent protein from coral. Proc Natl Acad Sci USA, 97, 11990–11995.
  • Gurskaya NG, Fradkov AF, Terskikh A, Matz MV, Labas YA, Martynov VI, Yanushevich YG, Lukyanov KA, Lukyanov SA. (2001). GFP-like chromoproteins as a source of far-red fluorescent proteins. FEBS Lett, 507, 16–20.
  • Gurskaya NG, Verkhusha VV, Shcheglov AS, Staroverov DB, Chepurnykh TV, Fradkov AF, Lukyanov S, Lukyanov KA. (2006). Engineering of a monomeric green-to-red photoactivatable fluorescent protein induced by blue light. Nat Biotechnol, 24, 461–465.
  • Harper BK, Mabon SA, Leffel SM, Halfhill MD, Richards HA, Moyer KA, Stewart CN Jr. (1999). Green fluorescent protein as a marker for expression of a second gene in transgenic plants. Nat Biotechnol, 17, 1125–1129.
  • Haseloff J, Siemering KR. (2006). The uses of green fluorescent protein in plants. Methods Biochem Anal, 47, 259–284.
  • Heikal AA, Hess ST, Baird GS, Tsien RY, Webb WW. (2000). Molecular spectroscopy and dynamics of intrinsically fluorescent proteins: coral red (dsRed) and yellow (Citrine). Proc Natl Acad Sci USA, 97, 11996–12001.
  • Heim R, Prasher DC, Tsien RY. (1994). Wavelength mutations and posttranslational autoxidation of green fluorescent protein. Proc Natl Acad Sci USA, 91, 12501–12504.
  • Heim R, Tsien RY. (1996). Engineering green fluorescent protein for improved brightness, longer wavelengths and fluorescence resonance energy transfer. Curr Biol, 6, 178–182.
  • Hodal L, Bochardt A, Neilson JE, Mattson O, Okkels FT. (1992). Detection, expression and specific eliminaton of endogenous β-glucuronidase activity in transgenic and non-transgenic plants. Plant Sci, 87, 115–122.
  • Hu C, Chee PP, Robert H., Chesney, James H., Zhou JH, Miller PD, O’Brien WT. (1990). Intrinsic GUS-like activities in seed plants. Plant Cell Rep, 9, 1–5.
  • Jefferson RA, Burgess SM, Hirsh D. (1986). Beta-Glucuronidase from Escherichia coli as a gene-fusion marker. Proc Natl Acad Sci USA, 83, 8447–8451.
  • Jefferson RA, Kavanagh TA, Bevan MW. (1987a). GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J, 6, 3901–7390.
  • Jefferson RA, Bevan M, Kavanagh T. (1987b). The use of the Escherichia coli beta- glucuronidase as a gene fusion marker for studies of gene expression in higher plants. Biochem Soc Trans, 15, 17–18.
  • Jefferson RA. (1989). The GUS reporter gene system. Nature, 342, 837–838.
  • Jin XF, Zhu B, Peng RH, Meng XR, Chen JM, Jiang HH, Yao QH, Xiong AS. (2010). Optimizing the binding activity of the AP2/ERF transcription factor with the GCC box element from Brassica napus by directed evolution. BMB Rep, 43, 567–572.
  • Kaur J, Sharma R. (2006). Directed evolution: an approach to engineer enzymes. Crit Rev Biotechnol, 26, 165–199.
  • Kim MS, Lei XG. (2008). Enhancing thermostability of Escherichia coli phytase AppA2 by error-prone PCR. Appl Microbiol Biotechnol, 79, 69–75.
  • Knop M, Barr F, Riedel CG, Heckel T, Reichel C. (2002). Improved version of the red fluorescent protein (drFP583/DsRed/RFP). Biotechniques, 33, 592–602.
  • Kremers GJ, Piston DW. (2008). Turning fluorescent proteins into energy-saving light bulbs. Nat Methods, 5, 472–473.
  • Kosugi S, Ohashi Y, Nakajima K, Arai Y. (1990). An improved assay for β-glucuronidase in transformed cells: Methanol almost completely suppresses a putative endogenous β-glucuronidase activity. Plant Sci, 70, 133–140.
  • Labrou NE. (2010). Random mutagenesis methods for in vitro directed enzyme evolution. Curr Protein Pept Sci, 11, 91–100.
  • Lassner M, Bedbrook J. (2001). Directed molecular evolution in plant improvement. Curr Opin Plant Biol, 4, 152–156.
  • Lassner MW, McElroy D. (2002). Directed molecular evolution: bridging the gap between genomics leads and commercial products. OMICS, 6, 153–162.
  • Locher CP, Soong NW, Whalen RG, Punnonen J. (2004). Development of novel vaccines using DNA shuffling and screening strategies. Curr Opin Mol Ther 6, 34–39.
  • Locher CP, Paidhungat M, Whalen RG, Punnonen J. (2005). DNA shuffling and screening strategies for improving vaccine efficacy. DNA Cell Biol, 24, 256–263.
  • Lukyanov KA, Fradkov AF, Gurskaya NG, Matz MV, Labas YA, Savitsky AP, Markelov ML, Zaraisky AG, Zhao X, Fang Y, Tan W, Lukyanov SA. (2000). Natural animal coloration can be determined by a nonfluorescent green fluorescent protein homolog. J Biol Chem, 275, 25879–25882.
  • Luo WX, Cheng T, Guan BQ, Li SW, Miao J, Zhang J, Xia NS. (2006). Variants of green fluorescent protein GFPxm. Mar Biotechnol (NY), 8, 560–566.
  • March JC, Rao G, Bentley WE. (2003). Biotechnological applications of green fluorescent protein. Appl Microbiol Biotechnol, 62, 303–315.
  • Martin T, Scmidt R, Altman T, Frommer WB. (1990). Non-destructive assay system for detection of β-glucuronidase activity in higher plants. Plant Mol Biol Rep, 10, 37–46.
  • Matsumura I, Wallingford JB, Surana NK, Vize PD, Ellington AD. (1999). Directed evolution of the surface chemistry of the reporter enzyme beta-glucuronidase. Nat Biotechnol, 17, 696–701.
  • Matsumura I, Ellington AD. (2001). In vitro evolution of beta-glucuronidase into a beta-galactosidase proceeds through nonspecific intermediates. J Mol Biol, 305, 331–339.
  • Matthews BW. (2005). The structure of E. coli beta-galactosidase. C R Biol, 328, 549–556.
  • Matz MV, Fradkov AF, Labas YA, Savitsky AP, Zaraisky AG, Markelov ML, Lukyanov SA. (1999). Fluorescent proteins from nonbioluminescent Anthozoa species. Nat Biotechnol, 17, 969–973.
  • Megason S, Amsterdam A, Hopkins N, Lin S. (2006). Uses of GFP in transgenic vertebrates. Methods Biochem Anal, 47, 285–303.
  • Miki B., McHugh S. (2004). Selectable marker genes in transgenic plants: applications, alternatives and biosafety. J Biotechnol, 107, 193–232.
  • Morin JG, Hastings JW. (1971). Energy transfer in a bioluminescent system. J Cell Physiol, 77, 313–318.
  • Nagai T, Ibata K, Park ES, Kubota M, Mikoshiba K, Miyawaki A. (2002). A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat Biotechnol, 20, 87–90.
  • Nam SH, Oh KH, Kim GJ, Kim HS. (2003). Functional tuning of a salvaged green fluorescent protein variant with a new sequence space by directed evolution. Protein Eng, 16, 1099–1105.
  • Ormö M, Cubitt AB, Kallio K, Gross LA, Tsien RY, Remington SJ. (1996). Crystal structure of the Aequorea victoria green fluorescent protein. Science, 273, 1392–1395.
  • Otten LG, Quax WJ. (2005). Directed evolution: selecting today’s biocatalysts. Biomol Eng, 22, 1–9.
  • Parikh MR, Matsumura I. (2005). Site-saturation mutagenesis is more efficient than DNA shuffling for the directed evolution of beta-fucosidase from beta-galactosidase. J Mol Biol, 352, 621–628.
  • Patten PA, Howard RJ, Stemmer WP. (1997). Applications of DNA shuffling to pharmaceuticals and vaccines. Curr Opin Biotechnol, 8, 724–733.
  • Patterson GH. (2004). A new harvest of fluorescent proteins. Nat Biotechnol, 22, 1524–1525.
  • Prasher DC, Eckenrode VK, Ward WW, Prendergast FG, Cormier MJ. (1992). Primary structure of the Aequorea victoria green fluorescent protein. Gene, 111, 229–233.
  • Prendergast F, Mann K. (1978). Chemical and physical properties of aequorin and the green fluorescent protein isolated from Aequorea forskålea. Biochemistry, 17, 3448–3453.
  • Rasila TS, Pajunen MI, Savilahti H. (2009). Critical evaluation of random mutagenesis by error-prone PCR protocols, Escherichia coli mutator strain and hydroxylamine treatment. Anal Biochem, 388, 71–80.
  • Rizzo MA, Springer GH, Granada B, Piston DW. (2004). An improved cyan fluorescent protein variant useful for FRET. Nat Biotechnol, 22, 445–449.
  • Roda A. (2010). Discovery and development of the green fluorescent protein, GFP: the 2008 Nobel Prize. Anal Bioanal Chem, 396, 1619–1622.
  • Rowe LA, Geddie ML, Alexander OB, Matsumura I. (2003). A comparison of directed evolution approaches using the beta-glucuronidase model system. Mol Biol, 332, 851–860.
  • Russell WM, Klaenhammer TR. (2001). Identification and cloning of gusA, encoding a new beta-glucuronidase from Lactobacillus gasseri ADH. Appl Environ Microbiol, 67, 1253–1261.
  • Sawano A, Miyawaki A. (2000). Directed evolution of green fluorescent protein by a new versatile PCR strategy for site-directed and semi-random mutagenesis. Nucleic Acids Res, 28, e78.
  • Shaner NC, Campbell RE, Steinbach PA, Giepmans BN, Palmer AE, Tsien RY. (2004). Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol, 22, 1567–1572.
  • Shaner NC, Patterson GH, Davidson MW. (2007). Advances in fluorescent protein technology. J Cell Sci, 120, 4247–4260.
  • Shaner NC, Lin MZ, McKeown MR, Steinbach PA, Hazelwood KL, Davidson MW, Tsien RY. (2008). Improving the photostability of bright monomeric orange and red fluorescent proteins. Nat Methods, 5, 545–551.
  • Scholz O, Thiel A, Hillen W, Niederweis M. (2000). Quantitative analysis of gene expression with an improved green fluorescent protein. Eur J Biochem, 267, 1565–1570.
  • Shimomura O, Johnson FH, Saiga Y. (1962). Extraction, purification and properties of aequorin, a bioluminescent protein from the luminous hydromedusan, Aequorea. J Cell Comp Physiol, 59, 223–229.
  • Shimomura O. (2005). The discovery of aequorin and green fluorescent protein. J Microsc, 217, 1–15.
  • Shkrob MA, Yanushevich YG, Chudakov DM, Gurskaya NG, Labas YA, Poponov SY, Mudrik NN, Lukyanov S, Lukyanov KA. (2005). Far-red fluorescent proteins evolved from a blue chromoprotein from Actinia equina. Biochem J, 392, 649–654.
  • Shu X, Wang L, Colip L, Kallio K, Remington SJ. (2009). Unique interactions between the chromophore and glutamate 16 lead to far-red emission in a red fluorescent protein. Protein Sci, 18, 460–466.
  • Stefan A, Radeghieri A, Gonzalez Vara y Rodriguez A, Hochkoeppler A. (2001). Directed evolution of beta-galactosidase from Escherichia coli by mutator strains defective in the 3′–>5′ exonuclease activity of DNA polymerase III. FEBS Lett, 493, 139–143.
  • Stemmer WP. (1994a). DNA shuffling by random fragmentation and reassembly: in vitro recombination for molecular evolution. Proc Natl Acad Sci USA, 91, 10747–10751.
  • Stemmer WP. (1994b). Rapid evolution of a protein in vitro by DNA shuffling. Nature, 370, 389–391.
  • Stephens DE, Singh S, Permaul K. (2009). Error-prone PCR of a fungal xylanase for improvement of its alkaline and thermal stability. FEMS Microbiol Lett, 293, 42–47.
  • Stewart CN. (2001). The utility of green fluorescent protein in transgenic plants. Plant Cell Rep, 20, 376–382.
  • Sudan C, Prakash S, Bhomkar P, Jain S, Bhalla-Sarin N. (2006). Ubiquitous presence of β-glucuronidase (GUS) in plants and its regulation in some model plants. Planta, 224, 853–864.
  • Taylor CB. (1997). Promoter fusion analysis: an insufficient measure of gene expression. Plant Cell, 9, 273–275.
  • Tsien RY. (1998). The green fluorescent protein. Annu Rev Biochem, 67, 509–544.
  • Tian YS, Peng RH, Xu J, Zhao W, Gao F, Fu XY, Xiong AS, Yao QH. (2010a). Mutations in two amino acids in phyI1s from Aspergillus niger 113 improve its phytase activity. World J Microbiol Biotechnol, 26, 903–907.
  • Tian YS, Peng RH, Xu J, Zhao W, Gao F, Fu XY, Xiong AS, Yao QH. (2010b). Semi-rational site-directed mutagenesis of phyI1s from Aspergillus niger 113 at two residue to improve its phytase activity. Mol Biol Rep.
  • Turner NJ. (2003). Directed evolution of enzymes for applied biocatalysis. Trends Biotechnol, 21, 474–478.
  • Turner NJ. (2009). Directed evolution drives the next generation of biocatalysts. Nat Chem Biol, 5, 567–573.
  • Wang L, Jackson W, Steinbach P, Tsien R. (2004). Evolution of new nonantibody proteins via iterative somatic hypermutation. Proc Natl Acad Sci USA, 101, 16745–16749.
  • Whalen RG, Kaiwar R, Soong NW, Punnonen J. (2001). DNA shuffling and vaccines. Curr Opin Mol Ther, 3, 31–36.
  • Woznaik CA, Owens LD. (1994). Native β-glucuronidase activity in sugarbeet (Beta vulgaris). Physiol Plant, 90, 763–771.
  • Xia NS, Luo WX, Zhang J, Xie XY, Yang HJ, Li SW, Chen M, Ng MH. (2002). Bioluminescence of Aequorea macrodactyla, a common jellyfish species found in the east China sea. Mar Biotechnol, 4, 155–162.
  • Xie Z, Li H, Chen J, Zhang HB, Wang YY, Chen Q, Zhao ZZ, Cheng C, Zhang H, Yang Y, Wang HN, Gao R. (2007). Shuffling of pig interleukin-2 gene and its enhancing of immunity in mice to Pasteurella multocida vaccine. Vaccine, 25, 8163–8171.
  • Xiong AS, Yao QH, Peng RH, Chen JM, Li X, Fan HQ. (2002).Molecular evolution of beta-glucuronidase in vitro: obtaining thermotolerant GUS gene. Yi Chuan Xue Bao, 29, 1034–1040.
  • Xiong AS, Yao QH, Peng RH, Li X, Fan HQ, Cheng ZM, Li Y. (2004). A simple, rapid, high-fidelity and cost-effective PCR-based two-step DNA synthesis method for long gene sequences. Nucleic Acids Res, 32, e98.
  • Xiong AS, Yao QH, Peng RH, Duan H, Li X, Fan HQ, Cheng ZM, Li Y. (2006). PCR-based accurate synthesis of long DNA sequences. Nat Protoc, 1, 791–797.
  • Xiong AS, Peng RH, Liu JG, Zhuang J, Qiao YS, Xu F, Cai B, Zhang Z, Chen JM, Yao QH. (2007a). High efficiency and throughput system in directed evolution in vitro of reporter gene. Appl Microbiol Biotechnol, 74, 160–168.
  • Xiong AS, Peng RH, Cheng ZM, Li Y, Liu JG, Zhuang J, Gao F, Xu F, Qiao YS, Zhang Z, Chen JM, Yao QH. (2007b). Concurrent mutations in six amino acids in beta-glucuronidase improve its thermostability. Protein Eng Des Sel, 20, 319–325.
  • Xiong AS, Peng RH, Zhuang J, Liu JG, Gao F, Xu F, Cai B, Yao QH. (2007c). A semi-rational design strategy of directed evolution combined with chemical synthesis of DNA sequences. Biol Chem, 388, 1291–1300.
  • Xiong AS, Peng RH, Zhuang J, Liu JG, Xu F, Cai B, Guo ZK, Qiao YS, Chen JM, Zhang Z, Yao QH. (2007d). Directed evolution of beta-galactosidase from Escherichia coli into beta-glucuronidase. J Biochem Mol Biol, 40, 419–425.
  • Xiong AS, Peng RH, Zhuang J, Li X, Xue Y, Liu JG, Gao F, Cai B, Chen JM, Yao QH. (2007e). Directed evolution of a beta-galactosidase from Pyrococcus woesei resulting in increased thermostable beta-glucuronidase activity. Appl Microbiol Biotechnol, 77, 569–578.
  • Xiong AS, Yao QH, Peng RH, Cheng ZM. (2010). Directed in vitro evolution of reporter genes based on semi-rational design and high throughput screening. In: Methods in Molecular Biology. Vol. 634. In Vitro Mutagenesis Protocols. 3rd edition. Braman J, Ed. Totowa, NJ: Springer, Humana Press, 239–256.
  • Yang TT, Cheng L, Kain SR. (1996). Optimized codon usage and chromophore mutations provide enhanced sensitivity with the green fluorescent protein. Nucleic Acids Res, 24, 4592–4593.
  • Yoo TH, Link AJ, Tirrell DA. (2007). Evolution of a fluorinated green fluorescent protein. Proc Natl Acad Sci USA, 104, 13887–13890.
  • Yu H, Li J, Zhang D, Yang Y, Jiang W, Yang S. (2009). Improving the thermostability of N-carbamyl-D-amino acid amidohydrolase by error-prone PCR. Appl Microbiol Biotechnol, 82, 279–285.
  • Zhang JH, Dawes G, Stemmer WP. (1997). Directed evolution of a fucosidase from a galactosidase by DNA shuffling and screening. Proc Natl Acad Sci USA, 94, 4504–4509.
  • Zhang YX, Perry K, Vinci VA, Powell K, Stemmer WP, del Cardayré SB. (2002). Genome shuffling leads to rapid phenotypic improvement in bacteria. Nature, 415, 644–646.
  • Zhou M, Xu H, Wei X, Ye Z, Wei L, Gong W, Wang Y, Zhu Z. (2006). Identification of a glyphosate-resistant mutant of rice 5-enolpyruvylshikimate 3-phosphate synthase using a directed evolution strategy. Plant Physiol, 40, 184–195.

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.