55
Views
22
CrossRef citations to date
0
Altmetric
REVIEW

Development of Farnesyltransferase Inhibitors for Clinical Cancer Therapy: Focus on Hematologic Malignancies

, M.D. & , M.D.
Pages 484-494 | Published online: 11 Jun 2009

REFERENCES

  • End D. W. Farnesyl protein transferase inhibitors and other therapies targeting the Ras signal transduction pathway. Invest. New Drugs 1999; 17: 241–258
  • Rowinsky E. K., Windle J. J., Von Hoff D. D. Ras protein Farnesyltransferase: a strategic target for anticancer therapeutic development. J. Clin. Oncol. 1999; 17: 3631–365
  • Sebti S. M., Der C. J. Searching for the elusive targets of Farnesyltransferase inhibitors. Nature Rev. Cancer 2003; 3: 945–951
  • Johnston S. R.D., Hickish T., Ellis P., Houston S., Kelland L., Dowsett M., et al. Phase II study of the efficacy and tolerability of two dosing regimens of the Farnesyltransferase inhibitor, R115777, in advanced breast cancer. J. Clin. Oncol. 2003; 21: 2492–2499
  • Adjei A. A., Mauer A., Bruzek L., Marks R. S., Hillman S., et al. Phase II study of the Farnesyltransferase inhibitor R115777 in patients with advanced non-small cell lung cancer. J. Clin. Oncol. 2003; 21: 1760–1766
  • Patnaik A., Eckhardt S. G., Izbicka E., Tolcher A. A., Hammond L. A., et al. A Phase I, pharmacokinetic, and biological study of the Farnesyltransferase inhibitor Tipifarnib in combination with gemcitabine in patients with advanced malignancies. Clin. Cancer Res. 2003; 9: 4761–4741
  • Siegel-Lakhai W. S., Crul M., Zhang S., Sparidans R. W., Pluim D., et al. Phase I and pharmacological study of the Farnesyltransferase inhibitor tipifarnib (Zarnestra, R115777) in combination with gemcitabine and cisplatin in patients with advanced solid tumours. Br. J. Cancer 2005; 93: 1222–1229
  • Dy G. K., Bruzek L. M., Croghan G. A., Mandrekar S., Ehrlichman C., et al. A phase I trials of the novel Farnesyltransferase inhibitor, BMS-214662, in combination with paclitaxel and carboplatin in patients with advanced cancer. Clin. Cancer Res. 2005; 11: 1877–1883
  • Khuri F. R., Glisson B. S., Kim E. S., Statkevich P., Thall P. E., et al. Phase I study of the Farnesyltransferase inhibitor lonafarnib with paclitaxel in solid tumors. Clin. Cancer Res. 2004; 10: 2968–2976
  • Boguski M. S., McCormick F. Proteins regulating Ras and its relatives. Nature 1993; 366: 643–654
  • Lowy D. R., Willumsen B. M. Function and regulation of ras. Annu. Rev. Biochem. 1993; 62: 851–591
  • Khosvari-Far R., Cox AD., Cato K., Der CJ. Protein prenylation: key to ras function and cancer intervention?. Cell Growth Differ. 1992; 3: 461–469
  • Lancet J. E., Karp J. E. Farnesyltransferase inhibitors in hematologic malignancies: new horizons in therapy. Blood 2003; 102: 3880–3889
  • Reuter C. W.M., Morgan M. A., Bergmann L. Targeting the Ras signaling pathway: a rational, mechanism-based treatment for hematologic malignancies?. Blood 2000; 96: 1655–1669
  • Ridley A. J., Hall A. The small GTP-binding protein Rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 1992; 70: 389–399
  • Armstrong S. A., Hannah V. C., Goldstein J. L., Brown M. S. CAAX geranylgeranyl transferase transfers farnesyl as efficiently as geranylgeranyl tp RhoB. J. Biol. Chem. 1995; 270: 7864–7868
  • Adamson P., Marshall C. J., Hall A., Tilbrook P. A. Post-translational modifications of p21rho proteins. J. Biol. Chem. 1992; 267: 20033–20038
  • Prendergast C. G., Khosravifar R., Solski P. A., Kurzawa H., Lebowitz P., Der C. J. Critical role of Rho in cell transformation by oncogenic Ras. Oncogene 1995; 10: 2289–2296
  • Du W., Lebowitz P. F., Prendergast C. G. Cell growth inhibition by farnesyltransferase inhibitors is mediated by a gain of geranylgeranylated RhoB. Mol. Cell Biol. 1999; 19: 1831–1840
  • Lebowitz P. F., Casey P. J., Prendergast C. G., Thissen J. A. Farnesyltransferase inhibitors alter the prenylation and growth-stimulating function of RhoB. J. Biol. Chem. 1997; 272: 15591–15594
  • Lebowitz P. F., Sakamuor D., Prendergast C. G. Farnesyl transferase inhibitors induce apoptosis of Ras-transformed cells denied substratum attachement. Cancer Res. 1997; 57: 708–713
  • Chen Z., Sun J., Pradines A., Favre G., Adnane J., Sebti S. M. Both farnesylated and geranylgeranylated RhoB inhibit malignant transformation and suppress human tumor growth in nude mice. J. Biol. Chem. 2000; 275: 17974–17978
  • Raponi M., Lowenberg B., Lancet J. E., Harosseau JL., Stone R., et al. Identification of molecular predictors of response to Zarnestra (tipifarnib, R115777) in relapsed and refractory acute myeloid leukemia. Blood 2004; 104: 246a
  • Lackner M. R., Kindt R. M., Carroll P. M., Brown K., Cancilla M. R., et al. Chemical genetics identifies Rab geranylgeranyltransferase as an apoptotic target of Farnesyltransferase inhibitors. Cancer Cell 2005; 7: 325–336
  • Basso A. D., Mirza A., Liu G., Long B. J., Bishop W. R., Kirschmeier P. The Farnesyltransferase inhibitor (FTI) SCH66336 (lonafarnib) inhibits Rheb farnesylation and mTor signaling. J. Biol. Chem. 2005; 280: 31101–31108
  • Ashar H. R., James L., Gray K., Carr D., Black S., et al. Farnesyl transferase inhibitors block the farnesylation of CENP-E and CENP-F and alter the association of CENP-E with the microtubules. J. Biol. Chem. 2000; 275: 30451–30457
  • Ashar H. R., James L., Gray K., Carr D., McGuirk M., et al. The farnesyltransferase inhibitor SCH66336 induces a G2 → M or G1 pause in sensitive human tumor cell lines. Exper. Cell Res. 2001; 262: 17–27
  • Crespo N. C., Ohkanda J., Yen T. J., Hamilton A. D., Sebti S. M. The farnesyltransferase inhibitor FTI-2153 blocks bipolar spindle formation and chromosome alignment and causes prometaphase accumulation accumulation during mitosis of human lung cancer cells. J. Biol. Chem. 2001; 276: 16161–16167
  • Feldkamp M. M., Lau N., Guha A. Growth inhibition of astrocytoma cells by farnesyl transferase inhibitors is mediated by a combination of anti-proliferative, pro-apoptotic and anti-angiogenic effects. Oncogene 1999; 18: 7514–7526
  • Gu W. Z., Tahir S. K., Wang Y. C., Zhang H. C., Cherian S. P., et al. Effect of novel CAAX peptidomimetic farnesyl transferase inhibitor on angiogenesis in vitro and in vivo. Eur. J. Cancer 1999; 35: 1394–1401
  • Peters D. G., Hoover R. R., Gerlach M. J., Koh E. Y., Zhang H., et al. Activity of the farnesyl protein transferase inhibitor SCH66336 against BCR/ABL-induced murine leukemia and primary cells from patients with chronic myeloid leukemia. Blood 2001; 97: 1404–1412
  • Reichert A., Heisterkamp N., Daley G. Q., Groffen J. Treatment of Bcr-ABl positive acute lymphoblastic leukemia in P190 transgenic mice with the Farnesyltransferase inhibitor SCH66336. Blood 2001; 97: 1399–1403
  • Zhu K., Gerbino E., Beaupre D. M., Mackley P. A., Muro-Cacho C., et al. Farnsyltransferase inhibitor R115777 (Zarnestra, Tipifarnib) synergizes with paclitaxel to induce apoptosis and mitotic arrest and to inhibit tumor growth of multiple myeloma cells. Blood 2005; 105: 4759–4766
  • Burgering B. M., Coffer P. J. Protein kinase B (c-AKT) in phosphatidylinositol-3-OH kinase signal transduction. Nature 1995; 376: 599–602
  • Downward J. Mechanisms and consequences of activation of protein kinase B/Akt. Curr. Opin. Cell Biol. 1998; 10: 262–272
  • Klippel A., Escobedo M. A., Wachowicz M. S., Aoell G., Brown T. W., et al. Activation of phosphatidylinositol-3 kinase is sufficient for cell cycle entry and promotes cellular changes characteristic of oncogenic transformation. Mol. Cell Biol. 1998; 18: 5699–5711
  • Grandage V. L., Gale R. E., Linch D. C., Khwaja A. PI3-kinase is constitutively active in primary acute myeloid leukaemia cells and regulates survival and chemoresistance via NF-kB, MAPkinase and p53 pathways. Leukemia 2005; 19: 586–594
  • Jiang K., Coppola D., Crespo N. C., Nicosia S. V., Hamilton A. D., Sebti S. M., Cheng J. Q. The phosphoinositide 3-OH/AKT2 pathway as a critical target for farnesyltransferase inhibitor-induced apoptosis. Mol. Cell Biol. 2000; 20: 139–148
  • Carloni V., Vizzutti F., Pantaleo P. Farnesyltransferase inhibitor ABT-100 is a potent liver cancer chemopreventive agent. Clin. Cancer Res. 2005; 11: 4266–4274
  • Delmas C., End D., Rochaix P., Favre G., Toulas C., Cohen-Jonathan E. The Farnesyltransferase inhibitor R115777 reduces hypoxia and matrix metalloproteinase 2 expression in human glioma xenograft. Clin. Cancer Res. 2003; 9: 6062–6068
  • Delmas C., Heliez C., Cohen-Jonathan E., et al. Farnesyltransferase inhibitor, R115777, reverses the resistance of human glioma cell lines to ionizing radiation. Int. J. Cancer 2002; 100: 43–48
  • Oh S. H., Kim W. Y., Kim J. H., Younes M. N., El-Naggar A. K., et al. Identification of insulin-like growth factor binding protein-3 as a Farnesyltransferase inhibitor SCH66336-induced negative regulator of angiogenesis in head and neck squamous cell carcinoma. Clin. Cancer Res. 2006; 12: 653–661
  • Gu W. Z., Jospeh I., Wang Y. C., Frost D., Sullivan G. M., et al. A highly potent and selective Farnesyltransferase inhibitor ABT-100 in preclinical studies. Anticancer Drugs 2005; 16: 1059–1069
  • Lancet J. E., Willman C. L., Bennett J. M. Acute myelogenous and aging: clinical interactions. Hematol. Oncol. North. Am. 2000; 14: 251–267
  • Stone R. M., Berg D. T., George S. L., Dodge R. K., Paciucci P. A., et al. Postremission therapy in older patients with de novo acute myeloid leukemia: a randomized trial comparing mitoxantrone and intermediate-dose cytarabine with standard-dose cytarabine. Blood 2001; 98: 548–553
  • Bolanos-Meade J., Guo C., Gojo I., Karp J. E. A phase II study of timed sequential therapy of acute myelogenous leukemia (AML) for patients over age 60: two cycle timed sequential therapy with topotecan, ara-C and mitoxantrone in adults with poor-risk AML. Leuk. Res. 2004; 28: 571–577
  • Grimwade D., Walker H., Harrison G., Oliver F., Chatters S., et al. The predictive value of hierarchical cytogenetic classification in older adults with acute myeloid leukemia (AML): analysis of 1065 patients entered into the United Kingdom Medical Research Council AML 11 trial. Blood 2001; 98: 1312–1320
  • Leith C. P., Kopecky K. J., Chen I. M., Eijdems L., Slovak M. L., et al. Frequency and clinical significance of the expression of the multidrug resistance proteins MDR1/P-glycoprotein, MRP1, and LRP in acute myeloid leukemia: a Southwest Oncology Group study. Blood 1999; 94: 1086–1099
  • Karp J. E., Lancet J. E., Kaufmann S. H., End D. W., Wright J. J., et al. Clinical and biological activity in the Farnesyltransferase inhibitor R115777 in adults with refractory and relapsed acute leukemias: a Phase I clinical-correlative trial. Blood 2001; 97: 3361–3369
  • Lancet J. E., Gojo I., Gotlib J., Feldman E. J., Greer J., et al. A phase II study of the Farnesyltransferase inhibitor Tipifarnib in elderly patients with previously untreated poor-risk acute myelogenous leukemia. Blood 2007; 109: 1387–1394
  • Harousseau J. L., Reiffers J., Lowenberg B., Thomas X., Huguet F., et al. Zarnestra (R115777) in patients with relapsed and refractory acute myelogenous leukemia (AML): results of a multicenter phase 2 study. Blood 2003; 102: 176a
  • Cortes J., Faderl S., Estey E., Kurzrock R., Thomas D., et al. Phase I study of BMS-214662, a farnesyl transferase inhibitor in patients with acute leukemias and high-risk myelodysplastic syndromes. J. Clin. Oncol. 2005; 23: 2805–2812
  • Kurzrock R., Albitar M., Cortes J. E., Estey E. H., Faderl S. H., et al. Phase II study of R115777, a farnesyl transferase inhibitor, in myelodysplastic syndrome. J. Clin. Oncol. 2004; 22: 1287–1292
  • Kurzrock R., Kantarjian H. M., Cortes J. E., Singhania N., Thomas D. A., et al. Farnesyltransferase inhibitor R115777 in myelodysplastic syndrome: clinical and biologic activities in the Phase 1 setting. Blood 2003; 102: 4527–4534
  • Kurzrock R., Fenaux P., Raza A., Mufti G., Aul C., et al. High-risk myelodysplastic syndrome (MDS): first results of international Phase 2 study with oral farnesyltransferase inhibitor R115777 (ZARNESTRA). Blood 2004; 104: 23a
  • Kurzrock R., Verstovsek S., Wright J. J., Pilat S. R., Cortes J. E., et al. Alternate week administration of the farnesyltransferase inhibitor Tipifarnib (Zarnestra, R115777) in patients with myelodysplastic syndrome: results of a Phase I study. Blood 2005; 106: 7082, (Abstr. 2521)
  • Feldman E. J., Cortes J., Holyoake T. L., Simonsson B., DeAngelo D. J., et al. Continuous oral lonafarnib (Sarasar) for the treatment of patients with myelodysplastic syndrome. Blood 2003; 102: 421a
  • Cortes J., Albitar M., Thomas D., Giles F., Kurzrock R., et al. Efficacy of the farnesyl transferase inhibitor R115777 in chronic myeloid leukemia and other hematologic malignancies. Blood 2003; 101: 1692–1697
  • Cortes J. E., Daley G., Talpaz M., O'Brien S., Garcia-Manero G., et al. Pilot study of SCH66336(lonafarnib), a farnesyl transferase inhibitor (FTI), in patients with chronic myeloid leukemia (CML) in chronic or accelerated phase resistant or refractory to Imatinib. Blood 2002; 100: 164a
  • Mesa R. A., Tefferi A., Gray L. A., Reeder T., Schroeder G., Kaufmann S. H. In vitro antiproliferative activity of the farnesyltransferase inhibitor R115777 in hematopoietic progenitors from patients with myelofibrosis with myeloid metaplasia. Leukemia 2003; 17: 849–855
  • Mesa R. A., Camoriano J. K., Geyer S. M., Kaufmann S. H., Rivera C. E., Ehrlichmann C., Tefferi A. A Phase 2 consortium (P2C) trial of R115777 (Tipifarnib) in myelofibrosis with myeloid metaplasia. Blood 2004; 104: 422a
  • Bollag G., Clapp D. W., Shih S., Adler F., Zhang Y. Y., et al. Loss of NF1 results in activation of the Ras signaling pathway and leads to aberrant growth in haematopoietic cells. Nature Genetics 1996; 12: 144–148
  • Schubbert S., Lieuw K., Rowe S. L., Lee C. M., Li X. X., et al. Functional analysis of leukemia-associated PTPN11 mutations in primary hematopoietic cells. Blood 2005; 106: 311–317
  • Side L. E., Emanuel P. D., Taylor B., Franklin J., Thompson P., Castleberry R. P., Shannon K. M. Mutations of the NF1 gene in children with juvenile myelomonocytic leukemia without clinical evidence of neurofibromatosis, type 1. Blood 1998; 92: 267–272
  • Castleman R. P., Loh M., Jayaprakash N., Peterson A., Casey V., et al. Phase II window study of the Farnesyltransferase inhibitor R115777 (Zarnestra) in untreated juvenile myelomonocytic leukemia (JMML): a Children's Oncology Group study. Blood 2005; 106: 727a, (Abstr. 2587)
  • Gotlib J., Loh M., Lancet J. E., Vattikuti S., Quesada S., et al. Phase I/II study of farnesyltransferase inhibitor R115777 (Zarnestra) in patients with myeloproliferative disorders (MPDs): interim results. Blood 2003; 102: 3425a
  • Buresh A., Perentesis J., Rimsza L., Kurtin S., Heaton R., Sugrue M., List A. F. Hyperleukocytosis complicating lonafarnib treatment in patients with chronic myelomonocytic leukemia. Leukemia 2005; 19: 308–310
  • List A. F., Tache-Tallmadge C., Tate W., Glinsmann-Gibson B., Brown D., et al. Farnesyltransferase inhibitors (FTI) modulate beta-integrin affinity to promote homotypic and heterotypic adhesion of chronic myelomonocytic leukemia (CMML) cells. Blood 2003; 102: 427a
  • Beaupre D. M., Cepero E., Obeng E. A., Boise L. H., Lichtenheld M. G. R115777 induces Ras-independent apoptosis of myeloma cells via multiple intrinsic pathways. Mol. Cancer Ther. 2004; 3: 179–186
  • Bolick S. C.E., Landowski T. H., Boulware D., Oshiro M. M., Ohkanda J., et al. The farnesyl transferase inhibitor, FTI-277, inhibits growth and induces apoptosis in drug-resistance myeloma cells. Leukemia 2003; 17: 451–457
  • Gomez-Benito M., Marzo I., Anel A., Naval J. Farnesyltransferase inhibitor BMS-214662 induces apoptosis in myeloma cells through PUMA up-regulation, Bax and Bak activation, and Mcl-1 elimination. Mol. Pharmacol. 2005; 67: 1991–1998
  • Le Gouill S., Pellat-Deceunynck C., Harousseau J. L., Rapp M. J., Robillard N., Bataille R., Amiot M. Farnesyl transferase inhibitor R115777 induces apoptosis in human myeloma cells. Leukemia 2002; 16: 1664–1667
  • Shi Y., Gera J., Hsu J., Van Ness B., Lichtenstein A. Cytoreductive effects of farnesyl transferase inhibitors on multiple myeloma tumor cells. Mol. Cell Ther. 2003; 2: 563–572
  • Alsina M., Fonseca R., Wilson E. F., Belle A. N., Gerbino E., et al. Farnesyltransferase inhibitor tipifarnib is well tolerated, induces stabilization of disease, and inhibits farnesylation and oncogenic/tumor survival pathways in patients with advanced multiple myeloma. Blood 2004; 103: 3271–3277
  • Ravandi-Kashani F., Kantarjian H., Garcia-Manero G., O'Brien S., Verstovsek S., et al. Tipifarnib in combination with idarubicin and cytarabine in patients with newly diagnosed acute myeloid leukemia (AML) or high risk myelodysplastic syndrome (MDS). Proc. Am. Soc. Clin. Oncol. 2006; 24: 351s
  • Marcus A. I., Zhou J., O'Brate A., Hamel E., Wong J., et al. The synergistic cominbation of the Farnesyltransferase inhibitor lonafarnib and paclitaxel enhances tubulin acetylation and requires functional tubulin deacetylase. Cancer Res. 2005; 65: 3883–3893
  • Cortes J., Garcia-Manero G., O'Brien S., Hernandez I., Rackoff W., et al. A Phase I study of tipifarnib in combination with imatinib mesylate (IM) for patients with chronic myeloid leukemia in chronic phase (CP) who failed IM therapy. Blood 2004; 104: 289a
  • Cortes J., O'Brien S., Verstovek S., Daley G., Koller C., et al. Phase I study of lonafarnib (SCH66336) in combination with imatinib for patients with chronic myeloid leukemia after failure to imatinib. Blood 2004; 104: 288a
  • Hu L., Shi Y., Hsu J., Gera J., Van Ness B., Lichtenstein A. Downstream effectors of oncogenic ras in multiple myeloma cells. Blood 2003; 101: 3126–3135
  • Yanamandra N., Colaco N. M., Parquet N. A., Buzzeo R. W., Boulware D., et al. Tipifarnib and bortezomib are synergistic and overcome cell adhesion-mediated drug resistance in multiple myeloma and acute myeloid leukemia. Clin. Cancer Res. 2006; 12: 591–599
  • David E., Sun S. Y., Waller E. K., Chen J., Khuri F. R., Lonial S. The combination of the farnesyl transferase inhibitor lonafarnib and the proteasome inhibitor bortezomib induces synergistic apoptosis in human myeloma cells that is associated with down-regulation of p-AKT. Blood 2005; 106: 4322–4329
  • Buzzeo R., Enkemann S., Nimmanapalli R., Alsina M., Lichtenheld M. G., Dalton W. S., Beaupre D. M. Characterization of a R115777-resistant human multiple myeloma cell line with cross-resistance to PS-341. Clin. Cancer Res. 2005; 11: 6057–6064
  • Prendergast G. C., Davide J. P., Lebowitz P. F., Wechsler-Reya R., Kohl N. E. Resistance of a variant ras-transformed cell line to phenotypic reversion by farnesyltransferase inhibitors. Cancer Res. 1996; 56: 2626–2632
  • Smith V., Rowlands MG., Barrie E., Workman P., Kelland LR. Establishment and characterization of acquired resistance to farnesyl protein transferase inhibitor R115777 in a human colon cancer cell line. Clin. Cancer Res. 2002; 8: 2002–2009
  • Zhang B., Groffen J., Heisterkamp N. Resistance to farnesyltransferase inhibitors in Bcr/Abl-positive lymphoblastic leukemia by increased expression of a novel ABC transporter homolog ATP11a. Blood 2005; 106: 1355–1361
  • Del Villar K., Urano J., Guo L., Tamanoi F. A mutant form of protein Farnesyltransferase exhibits increase resistance to farnesyltransferase inhibitors. J. Biol. Chem. 1999; 27010–27017
  • Raz T., Mohammad A., Daley G. Q. Resistance to the farnesyl transferase inhibitor SCH66336 (Lonafarnib) caused by mutations in the target protein farnesyl transferase beta. Blood 2004; 104: 133a
  • Goemans B. F., Zwaan C. M., Harlow A., Loonen A. H., Gibson B. E.S., et al. In vitro profiling of the sensitivity of pediatric leukemia cells to tipifarnib: identification of T-cell ALL and FAB M5 AML as the most sensitive subsets. Blood 2005; 106: 3532–3537
  • Raponi M., Belly R. T., Karp J. E., Lancet J. E., Atkins D., Wang Y. Microarray analysis reveals genetic pathways modulated by tipifarnib in acute myeloid leukemia. BMC Cancer 2004; 4: 56, doi; 10.1186/1471-2407-4-56
  • Toksoz D., Williams DA. Novel human oncogene lbc detected by transfection with distinct homology regions to signal transduction proteins. Oncogene 1994; 9: 621–628
  • Zheng Y., Olson M. F., Hall A., Cerione R. A., Toksoz D. Direct involvement of the small GTP-binding protein Rho in lbc oncogene function. J. Biol. Chem. 1995; 270: 9031–9034
  • Foisner R., Traub P., Wiche G. Protein kinase A- and protein kinase C-regulated interaction of plectin with lamin B and vimentin. Proc Natl Acad Sci USA 1991; 88: 3812–3816
  • Tsai M. Y., Wang S., Heidinger J. M., Shumaker D. K., Adam S. A., Goldman R. D., Zheng Y. A mitotic lamin B matrix induced by RanGTP required for spindle assembly. Science 2006; 311: 1887–1893
  • Raponi M., Zhang Y., Jatkoe T., Yu J., Lee G., et al. Gene expression profiling predictive of Tipifarnib (ZARNESTRA, R115777) response in patients with newly diagnosed acute myeloid leukemia. Blood 2005; 106: 781a
  • Fong L. G., Frost D., Meta M., Qiao X., Yang S. H., Coffinier C., Young S. G. A protein Farnesyltransferase inhibitor ameliorates disease in a mouse model of progeria. Science 2006; 311: 1621–1623

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.