37
Views
84
CrossRef citations to date
0
Altmetric
Cell Growth and Development

The Oncogenic Potential of the Pax3-FKHR Fusion Protein Requires the Pax3 Homeodomain Recognition Helix but Not the Pax3 Paired-Box DNA Binding Domain

, , &
Pages 594-601 | Received 04 Feb 1998, Accepted 01 Oct 1998, Published online: 28 Mar 2023

Keep up to date with the latest research on this topic with citation updates for this article.

Read on this site (4)

Mary E Olanich & Frederic G Barr. (2013) A call to ARMS: targeting the PAX3-FOXO1 gene in alveolar rhabdomyosarcoma. Expert Opinion on Therapeutic Targets 17:5, pages 607-623.
Read now
Irina Lagutina, Simon J. Conway, Jack Sublett & Gerard C. Grosveld. (2002) Pax3-FKHR Knock-In Mice Show Developmental Aberrations but Do Not Develop Tumors. Molecular and Cellular Biology 22:20, pages 7204-7216.
Read now
Arjan Buijs, Luc van Rompaey, Anco C. Molijn, J. Nathan Davis, Alfred C. O. Vertegaal, Mark D. Potter, Constantin Adams, Sjozèf van Baal, Ellen C. Zwarthoff, Martine F. Roussel & Gerard C. Grosveld. (2000) The MN1-TEL Fusion Protein, Encoded by the Translocation (12;22)(p13;q11) in Myeloid Leukemia, Is a Transcription Factor with Transforming Activity. Molecular and Cellular Biology 20:24, pages 9281-9293.
Read now

Articles from other publishers (80)

Naomi TERAMOTO, Masanari IKEDA, Hidetoshi SUGIHARA, Takanori SHIGA, Takashi MATSUWAKI, Masugi NISHIHARA, Kazuyuki UCHIDA & Keitaro YAMANOUCHI. (2021) Loss of p16/Ink4a drives high frequency of rhabdomyosarcoma in a rat model of Duchenne muscular dystrophy. Journal of Veterinary Medical Science 83:9, pages 1416-1424.
Crossref
Gloria Gonzalez Curto, Audrey Der Vartanian, Youcef El-Mokhtar Frarma, Line Manceau, Lorenzo Baldi, Selene Prisco, Nabila Elarouci, Frédéric Causeret, Daniil Korenkov, Muriel Rigolet, Frédéric Aurade, Aurélien De Reynies, Vincent Contremoulins, Frédéric Relaix, Orestis Faklaris, James Briscoe, Pascale Gilardi-Hebenstreit & Vanessa Ribes. (2020) The PAX-FOXO1s trigger fast trans-differentiation of chick embryonic neural cells into alveolar rhabdomyosarcoma with tissue invasive properties limited by S phase entry inhibition. PLOS Genetics 16:11, pages e1009164.
Crossref
Ross A. Okimoto, Wei Wu, Shigeki Nanjo, Victor Olivas, Yone K. Lin, Rovingaile Kriska Ponce, Rieko Oyama, Tadashi Kondo & Trever G. Bivona. (2019) CIC-DUX4 oncoprotein drives sarcoma metastasis and tumorigenesis via distinct regulatory programs. Journal of Clinical Investigation 129:8, pages 3401-3406.
Crossref
Stephen X. Skapek, Andrea Ferrari, Abha A. Gupta, Philip J. Lupo, Erin Butler, Janet Shipley, Frederic G. Barr & Douglas S. Hawkins. (2019) Rhabdomyosarcoma. Nature Reviews Disease Primers 5:1.
Crossref
Ashok Arasu, Sengottuvelan Murugan, Musthafa Mohamed Essa, Thirunavukkarasu Velusamy & Gilles J. Guillemin. (2018) PAX3: A Molecule with Oncogenic or Tumor Suppressor Function Is Involved in Cancer. BioMed Research International 2018, pages 1-12.
Crossref
Salah Boudjadi, Bishwanath Chatterjee, Wenyue Sun, Prasantha Vemu & Frederic G. Barr. (2018) The expression and function of PAX3 in development and disease. Gene 666, pages 145-157.
Crossref
Mohammad Alimohammadi, Mohamed Hassen Lahiani, Diamond McGehee & Mariya Khodakovskaya. (2017) Polyphenolic extract of InsP 5-ptase expressing tomato plants reduce the proliferation of MCF-7 breast cancer cells. PLOS ONE 12:4, pages e0175778.
Crossref
Puspa R Pandey, Bishwanath Chatterjee, Mary E Olanich, Javed Khan, Markku M Miettinen, Stephen M Hewitt & Frederic G Barr. (2017) PAX3-FOXO1 is essential for tumour initiation and maintenance but not recurrence in a human myoblast model of rhabdomyosarcoma. The Journal of Pathology 241:5, pages 626-637.
Crossref
Jacob M. Loupe, Patrick J. Miller, Benjamin P. Bonner, Elaine C. Maggi, Jyothi Vijayaraghavan, Jovanny Zabaleta, Christopher M. Taylor, Fern Tsien, Judy S. Crabtree & Andrew D. Hollenbach. (2016) Acquisition of an oncogenic fusion protein serves as an initial driving mutation by inducing aneuploidy and overriding proliferative defects. Oncotarget 7:39, pages 62814-62835.
Crossref
J M Loupe, P J Miller, B P Bonner, E C Maggi, J Vijayaraghavan, J S Crabtree, C M Taylor, J Zabaleta & A D Hollenbach. (2016) Comparative transcriptomic analysis reveals the oncogenic fusion protein PAX3-FOXO1 globally alters mRNA and miRNA to enhance myoblast invasion. Oncogenesis 5:7, pages e246-e246.
Crossref
J M Loupe, P J Miller, D R Ruffin, M W Stark & A D Hollenbach. (2015) Inhibiting phosphorylation of the oncogenic PAX3-FOXO1 reduces alveolar rhabdomyosarcoma phenotypes identifying novel therapy options. Oncogenesis 4:3, pages e145-e145.
Crossref
Irina V. Lagutina, Virginia Valentine, Fabrizio Picchione, Frank Harwood, Marcus B. Valentine, Barbara Villarejo-Balcells, Jaime J. Carvajal & Gerard C. Grosveld. (2015) Modeling of the Human Alveolar Rhabdomyosarcoma Pax3-Foxo1 Chromosome Translocation in Mouse Myoblasts Using CRISPR-Cas9 Nuclease. PLOS Genetics 11:2, pages e1004951.
Crossref
F.G. Barr. 2015. Reference Module in Biomedical Sciences. Reference Module in Biomedical Sciences.
H Yoshida, M Miyachi, K Sakamoto, K Ouchi, S Yagyu, K Kikuchi, Y Kuwahara, K Tsuchiya, T Imamura, T Iehara, N Kakazu, H Hojo & H Hosoi. (2013) PAX3-NCOA2 fusion gene has a dual role in promoting the proliferation and inhibiting the myogenic differentiation of rhabdomyosarcoma cells. Oncogene 33:49, pages 5601-5608.
Crossref
Charles Keller & Denis C. Guttridge. (2013) Mechanisms of impaired differentiation in rhabdomyosarcoma. FEBS Journal 280:17, pages 4323-4334.
Crossref
Amy D. Marshall, Fabrizio Picchione, Ramon I. Klein Geltink & Gerard C. Grosveld. (2013) PAX3-FOXO1 Induces Up-Regulation of Noxa Sensitizing Alveolar Rhabdomyosarcoma Cells to Apoptosis. Neoplasia 15:7, pages 738-IN15.
Crossref
Qiande Hu, Yewen Yuan & Chiayeng Wang. (2013) Structural and Functional Studies of FKHR-PAX3, a Reciprocal Fusion Gene of the t(2;13) Chromosomal Translocation in Alveolar Rhabdomyosarcoma. PLoS ONE 8:6, pages e68065.
Crossref
Amy D. Marshall, Martijn A. van der Ent & Gerard C. Grosveld. (2012) PAX3-FOXO1 and FGFR4 in alveolar rhabdomyosarcoma. Molecular Carcinogenesis 51:10, pages 807-815.
Crossref
C. Wang. (2011) Childhood Rhabdomyosarcoma. Journal of Dental Research 91:4, pages 341-350.
Crossref
Amy D. Marshall, Irina Lagutina & Gerard C. Grosveld. (2011) PAX3-FOXO1 Induces Cannabinoid Receptor 1 to Enhance Cell Invasion and Metastasis. Cancer Research 71:24, pages 7471-7480.
Crossref
Stefania Rossi, Pietro Luigi Poliani, Cristina Missale, Eugenio Monti & Alessandro Fanzani. (2011) Caveolins in rhabdomyosarcoma. Journal of Cellular and Molecular Medicine 15:12, pages 2553-2568.
Crossref
Guri Tzivion, Melissa Dobson & Gopalakrishnan Ramakrishnan. (2011) FoxO transcription factors; Regulation by AKT and 14-3-3 proteins. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research 1813:11, pages 1938-1945.
Crossref
Y Zhang & C Wang. (2011) Nephroblastoma overexpressed (NOV/CCN3) gene: a paired-domain-specific PAX3-FKHR transcription target that promotes survival and motility in alveolar rhabdomyosarcoma cells. Oncogene 30:32, pages 3549-3562.
Crossref
Yue Xiao, Lingling Zhang, Kuanjun He, Xiang Gao, Lun Yang, Lin He, Gang Ma & Xizhi Guo. (2011) Characterization of a novel missense mutation on murine Pax3 through ENU mutagenesis. Journal of Genetics and Genomics 38:8, pages 333-339.
Crossref
Kevin N. Dietz, Patrick J. Miller, Aditi S. Iyengar, Jacob M. Loupe & Andrew D. Hollenbach. (2011) Identification of serines 201 and 209 as sites of Pax3 phosphorylation and the altered phosphorylation status of Pax3-FOXO1 during early myogenic differentiation. The International Journal of Biochemistry & Cell Biology 43:6, pages 936-945.
Crossref
Fabrizio Picchione, Colin Pritchard, Irina Lagutina, Laura Janke & Gerard C. Grosveld. (2011) IRIZIO : a novel gene cooperating with PAX3-FOXO1 in alveolar rhabdomyosarcoma (ARMS). Carcinogenesis 32:4, pages 452-461.
Crossref
Gianni Bisogno & John Anderson. 2010. Pediatric Hematology and Oncology. Pediatric Hematology and Oncology 216 233 .
Jerzy Lasota. 2011. Modern Soft Tissue Pathology. Modern Soft Tissue Pathology 127 180 .
Kevin N. Dietz, Patrick J. Miller & Andrew D. Hollenbach. (2009) Phosphorylation of Serine 205 by the Protein Kinase CK2 Persists on Pax3-FOXO1, but Not Pax3, throughout Early Myogenic Differentiation. Biochemistry 48:49, pages 11786-11795.
Crossref
Shujuan J. Xia, Dara D. Holder, Bruce R. Pawel, Chune Zhang & Frederic G. Barr. (2009) High Expression of the PAX3-FKHR Oncoprotein Is Required to Promote Tumorigenesis of Human Myoblasts. The American Journal of Pathology 175:6, pages 2600-2608.
Crossref
Carla De Giovanni, Lorena Landuzzi, Giordano Nicoletti, Pier-Luigi LolliniPatrizia Nanni. (2009) Molecular and cellular biology of rhabdomyosarcoma. Future Oncology 5:9, pages 1449-1475.
Crossref
Frederic G. Barr & Richard B. Womer. 2009. Oncology of Infancy and Childhood. Oncology of Infancy and Childhood 743 781 .
Qiuyu Wang, Wen-Hui Fang, Jerzy Krupinski, Shant Kumar, Mark Slevin & Patricia Kumar. (2008) Pax genes in embryogenesis and oncogenesis . Journal of Cellular and Molecular Medicine 12:6a, pages 2281-2294.
Crossref
Patrick J. Miller, Kevin N. Dietz & Andrew D. Hollenbach. (2008) Identification of serine 205 as a site of phosphorylation on Pax3 in proliferating but not differentiating primary myoblasts. Protein Science 17:11, pages 1979-1986.
Crossref
Corinne M. Linardic. (2008) PAX3–FOXO1 fusion gene in rhabdomyosarcoma. Cancer Letters 270:1, pages 10-18.
Crossref
David M. Loeb, Katherine Thornton & Ori Shokek. (2008) Pediatric Soft Tissue Sarcomas. Surgical Clinics of North America 88:3, pages 615-627.
Crossref
F Graf Finckenstein, V Shahbazian, E Davicioni, Y-X Ren & M J Anderson. (2007) PAX-FKHR function as pangenes by simultaneously inducing and inhibiting myogenesis. Oncogene 27:14, pages 2004-2014.
Crossref
M Ebauer, M Wachtel, F K Niggli & B W Schäfer. (2007) Comparative expression profiling identifies an in vivo target gene signature with TFAP2B as a mediator of the survival function of PAX3/FKHR. Oncogene 26:51, pages 7267-7281.
Crossref
Patrick J. Miller & Andrew D. Hollenbach. (2007) The oncogenic fusion protein Pax3–FKHR has a greater post-translational stability relative to Pax3 during early myogenesis. Biochimica et Biophysica Acta (BBA) - General Subjects 1770:10, pages 1450-1458.
Crossref
Hong Gui Li, Qiuyu Wang, Hong Mei Li, Shant Kumar, Craig Parker, Mark Slevin & Patricia Kumar. (2007) PAX3 and PAX3-FKHR promote rhabdomyosarcoma cell survival through downregulation of PTEN. Cancer Letters 253:2, pages 215-223.
Crossref
Claudio Scuoppo, Ilan Riess, Michel Schmitt-Ney, Paola Allegra, Paolo E. Forni, Francesca Bersani, Riccardo Taulli, Paolo Accornero, Tiziana Crepaldi & Carola Ponzetto. (2007) The oncogenic transcription factor PAX3-FKHR can convert fibroblasts into contractile myotubes. Experimental Cell Research 313:11, pages 2308-2317.
Crossref
Shujuan J Xia, Prerna Rajput, Donna M Strzelecki & Frederic G Barr. (2007) Analysis of genetic events that modulate the oncogenic and growth suppressive activities of the PAX3-FKHR fusion oncoprotein. Laboratory Investigation 87:4, pages 318-325.
Crossref
L Zhang & C Wang. (2006) Identification of a new class of PAX3-FKHR target promoters: a role of the Pax3 paired box DNA binding domain. Oncogene 26:11, pages 1595-1605.
Crossref
Friedrich Graf Finckenstein, Elai Davicioni, Kent G. Osborn, Webster K. Cavenee, Karen C. Arden & Michael J. Anderson. (2006) Transgenic mice expressing PAX3-FKHR have multiple defects in muscle development, including ectopic skeletal myogenesis in the developing neural tube. Transgenic Research 15:5, pages 595-614.
Crossref
Qiuyu Wang, Shant Kumar, Mark Slevin & Patricia Kumar. (2006) Functional Analysis of Alternative Isoforms of the Transcription Factor PAX3 in Melanocytes In vitro . Cancer Research 66:17, pages 8574-8580.
Crossref
Alberto Pappo, Fred G. Barr & Suzanne L. Wolden. 2006. Pediatric Bone and Soft Tissue Sarcomas. Pediatric Bone and Soft Tissue Sarcomas 103 132 .
Stephen Nabarro, Nourredine Himoudi, Antigoni Papanastasiou, Kimberly Gilmour, Sian Gibson, Neil Sebire, Adrian Thrasher, Michael P. Blundell, Mike Hubank, Glenda Canderan & John Anderson. (2005) Coordinated oncogenic transformation and inhibition of host immune responses by the PAX3-FKHR fusion oncoprotein. Journal of Experimental Medicine 202:10, pages 1399-1410.
Crossref
Shujuan J. Xia & Frederic G. Barr. (2005) Chromosome translocations in sarcomas and the emergence of oncogenic transcription factors. European Journal of Cancer 41:16, pages 2513-2527.
Crossref
Philippe R.J. Bois, Kamel Izeradjene, Peter J. Houghton, John L. Cleveland, Janet A. Houghton & Gerard C. Grosveld. (2005) FOXO1a acts as a selective tumor suppressor in alveolar rhabdomyosarcoma. Journal of Cell Biology 170:6, pages 903-912.
Crossref
Shouying Du, Eric J. Lawrence, Donna Strzelecki, Prerna Rajput, Shujuan J. Xia, Dina M. Gottesman & Frederic G. Barr. (2005) Co-expression of alternatively spliced forms of PAX3, PAX7, PAX3-FKHR and PAX7-FKHR with distinct DNA binding and transactivation properties in rhabdomyosarcoma. International Journal of Cancer 115:1, pages 85-92.
Crossref
Salma Begum, Nashmil Emani, Albert Cheung, Olivia Wilkins, Sandy Der & Paul A Hamel. (2005) Cell-type-specific regulation of distinct sets of gene targets by Pax3 and Pax3/FKHR. Oncogene 24:11, pages 1860-1872.
Crossref
Decheng Cai, Richard M. McCarron & John Hallenbeck. (2004) Cloning and characterization of a forkhead transcription factor gene, FoxO1a, from thirteen-lined ground squirrel. Gene 343:1, pages 203-209.
Crossref
Shujuan J Xia & Frederic G Barr. (2004) Analysis of the transforming and growth suppressive activities of the PAX3-FKHR oncoprotein. Oncogene 23:41, pages 6864-6871.
Crossref
Oana Tomescu, Shujuan J Xia, Donna Strezlecki, Jeannette L Bennicelli, Jill Ginsberg, Bruce Pawel & Frederic G Barr. (2004) Inducible short-term and stable long-term cell culture systems reveal that the PAX3-FKHR fusion oncoprotein regulates CXCR4, PAX3, and PAX7 expression. Laboratory Investigation 84:8, pages 1060-1070.
Crossref
Craig J. Parker, Susan G. Shawcross, Honggui Li, Qui-Yu Wang, C. Simon Herrington, Shant Kumar, Rhona M. MacKie, Wendy Prime, Ian G. Rennie, Karen Sisley & Patricia Kumar. (2004) Expression ofPAX 3 alternatively spliced transcripts and identification of two new isoforms in human tumors of neural crest origin. International Journal of Cancer 108:2, pages 314-320.
Crossref
Hien TranAnne BrunetEric C. GriffithMichael E. Greenberg. (2003) The Many Forks in FOXO's Road. Science's STKE 2003:172.
Crossref
Marcin Kortylewski, Florian Feld, Klaus-Dieter Krüger, Gregor Bahrenberg, Richard A. Roth, Hans-Georg Joost, Peter C. Heinrich, Iris Behrmann & Andreas Barthel. (2003) Akt Modulates STAT3-mediated Gene Expression through a FKHR (FOXO1a)-dependent Mechanism. Journal of Biological Chemistry 278:7, pages 5242-5249.
Crossref
Colin Pritchard, Gerard Grosveld & Andrew D Hollenbach. (2003) Alternative splicing of Pax3 produces a transcriptionally inactive protein. Gene 305:1, pages 61-69.
Crossref
Chi Wai SoMichael L. Cleary. (2003) Common mechanism for oncogenic activation of MLL by forkhead family proteins. Blood 101:2, pages 633-639.
Crossref
Lei Zhang & Chiayeng Wang. (2003) PAX3-FKHR Transformation Increases 26 S Proteasome-dependent Degradation of p27Kip1, a Potential Role for Elevated Skp2 Expression. Journal of Biological Chemistry 278:1, pages 27-36.
Crossref
Cory Abate-Shen. (2002) Deregulated homeobox gene expression in cancer: cause or consequence?. Nature Reviews Cancer 2:10, pages 777-785.
Crossref
Andrew D. Hollenbach, Craig J. McPherson, Edwin J. Mientjes, Rekha Iyengar & Gerard Grosveld. (2002) Daxx and histone deacetylase II associate with chromatin through an interaction with core histones and the chromatin-associated protein Dek. Journal of Cell Science 115:16, pages 3319-3330.
Crossref
Josef-Karl Gerber, Thomas Richter, Elisabeth Kremmer, Jerzy Adamski, Heinz Höfler, Rudi Balling & Heiko Peters. (2002) Progressive loss of PAX9 expression correlates with increasing malignancy of dysplastic and cancerous epithelium of the human oesophagus. The Journal of Pathology 197:3, pages 293-297.
Crossref
Andrew D. Hollenbach, Craig J. McPherson, Irina Lagutina & Gerard Grosveld. (2002) The EF-hand calcium-binding protein calmyrin inhibits the transcriptional and DNA-binding activity of Pax3. Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression 1574:3, pages 321-328.
Crossref
C.S.K. Mayanil, David George, Laura Freilich, Erik J. Miljan, Barbara Mania-Farnell, David G. McLone & Eric G. Bremer. (2001) Microarray Analysis Detects Novel Pax3 Downstream Target Genes. Journal of Biological Chemistry 276:52, pages 49299-49309.
Crossref
D. Ayalon, T. Glaser & H. Werner. (2001) Transcriptional regulation of IGF-I receptor gene expression by the PAX3–FKHR oncoprotein. Growth Hormone & IGF Research 11:5, pages 289-297.
Crossref
Frederic G Barr. (2001) Gene fusions involving PAX and FOX family members in alveolar rhabdomyosarcoma. Oncogene 20:40, pages 5736-5746.
Crossref
Nathalie Planque, Laurence Leconte, Frédéric M. Coquelle, Patrick Martin & Simon Saule. (2001) Specific Pax-6/Microphthalmia Transcription Factor Interactions Involve Their DNA-binding Domains and Inhibit Transcriptional Properties of Both Proteins. Journal of Biological Chemistry 276:31, pages 29330-29337.
Crossref
R J Olsen & S H Hinrichs. (2001) Phosphorylation of the EWS IQ domain regulates transcriptional activity of the EWS/ATF1 and EWS/FLI1 fusion proteins. Oncogene 20:14, pages 1756-1764.
Crossref
D Alan Underhill. (2000) Genetic and biochemical diversity in the Pax gene family . Biochemistry and Cell Biology 78:5, pages 629-638.
Crossref
Christiane M Margue, Michele Bernasconi, Frederic G Barr & Beat W Schäfer. (2000) Transcriptional modulation of the anti-apoptotic protein BCL-XL by the paired box transcription factors PAX3 and PAX3/FKHR. Oncogene 19:25, pages 2921-2929.
Crossref
Yun Cao & Chiayeng Wang. (2000) The COOH-terminal Transactivation Domain Plays a Key Role in Regulating the in Vitro and in Vivo Function of Pax3 Homeodomain. Journal of Biological Chemistry 275:13, pages 9854-9862.
Crossref
Luis del Peso, Víctor M González, Rubén Hernández, Frederic G Barr & Gabriel Núñez. (1999) Regulation of the forkhead transcription factor FKHR, but not the PAX3-FKHR fusion protein, by the serine/threonine kinase Akt. Oncogene 18:51, pages 7328-7333.
Crossref
Joseph M. Bosilevac, Randall J. Olsen, Julia A. Bridge & Steven H. Hinrichs. (1999) Tumor Cell Viability in Clear Cell Sarcoma Requires DNA Binding Activity of the EWS/ATF1 Fusion Protein. Journal of Biological Chemistry 274:49, pages 34811-34818.
Crossref
John Anderson, Anthony Gordon, Kathy Pritchard-Jones & Janet Shipley. (1999) Genes, chromosomes, and rhabdomyosarcoma. Genes, Chromosomes and Cancer 26:4, pages 275-285.
Crossref
Javed Khan, Michael L. Bittner, Lao H. Saal, Ulrike Teichmann, David O. Azorsa, Gerald C. Gooden, William J. Pavan, Jeffrey M. Trent & Paul S. Meltzer. (1999) cDNA microarrays detect activation of a myogenic transcription program by the PAX3-FKHR fusion oncogene . Proceedings of the National Academy of Sciences 96:23, pages 13264-13269.
Crossref
S Jaishankar, J Zhang, M F Roussel & S J Baker. (1999) Transforming activity of EWS/FLI is not strictly dependent upon DNA-binding activity. Oncogene 18:40, pages 5592-5597.
Crossref
Glenn Merlino & Lee J Helman. (1999) Rhabdomyosarcoma – working out the pathways. Oncogene 18:38, pages 5340-5348.
Crossref
Marie-Dominique Galibert, Timothy J. Dexter, Colin R. Goding & Ugur Yavuzer. (1999) Pax3 and Regulation of the Melanocyte-specific Tyrosinase-related Protein-1 Promoter. Journal of Biological Chemistry 274:38, pages 26894-26900.
Crossref
Jeannette L. Bennicelli & Frederic G. Barr. (1999) Genetics and the biologic basis of sarcomas. Current Opinion in Oncology 11:4, pages 267.
Crossref

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.