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Research Paper

The effects of Aurora Kinase inhibition on thyroid cancer growth and sensitivity to MAPK-directed therapies

ORCID Icon, , , ORCID Icon & ORCID Icon
Article: 2332000 | Received 24 Apr 2023, Accepted 14 Mar 2024, Published online: 23 Mar 2024

References

  • Li M, Dal Maso L, Vaccarella S. Global trends in thyroid cancer incidence and the impact of overdiagnosis. Lancet Diabetes Endocrinol. 2020;8(6):468–10. doi:10.1016/S2213-8587(20)30115-7.
  • Molinaro E, Romei C, Biagini A, Sabini E, Agate L, Mazzeo S, Materazzi G, Sellari-Franceschini S, Ribechini A, Torregrossa L, et al. Anaplastic thyroid carcinoma: from clinicopathology to genetics and advanced therapies. Nat Rev Endocrinol. 2017;13(11):644–660. doi:10.1038/nrendo.2017.76.
  • Smallridge RC, Marlow LA, Copland JA. Anaplastic thyroid cancer: molecular pathogenesis and emerging therapies. Endocr Relat Cancer. 2009;16(1):17–44. doi:10.1677/ERC-08-0154.
  • Tumino D, Frasca F, Newbold K. Updates on the management of advanced, metastatic, and radioiodine refractory differentiated thyroid cancer. Front Endocrinol (Lausanne). 2017;8:312. doi:10.3389/fendo.2017.00312.
  • Bernet V, Smallridge R. New therapeutic options for advanced forms of thyroid cancer. Expert Opin Emerg Drugs. 2014;19(2):225–241. doi:10.1517/14728214.2014.894017.
  • Hundahl SA, Fleming ID, Fremgen AM, Menck HR. A national cancer data base report on 53,856 cases of thyroid carcinoma treated in the U.S., 1985-1995 [see commetns]. Cancer. 1998;83(12):2638–2648. doi:10.1002/(SICI)1097-0142(19981215)83:12<2638:AID-CNCR31>3.0.CO;2-1.
  • Fagin JA, Wells SA Jr., Longo DL. Biologic and clinical perspectives on thyroid cancer. N Engl J Med. 2016;375(11):1054–1067. doi:10.1056/NEJMc1613118.
  • Pfister DG, Fagin JA. Refractory thyroid cancer: a paradigm shift in treatment is not far off. J Clin Oncol. 2008;26(29):4701–4704. doi:10.1200/JCO.2008.17.3682.
  • Xing M. Molecular pathogenesis and mechanisms of thyroid cancer. Nat Rev Cancer. 2013;13(3):184–199. doi:10.1038/nrc3431.
  • Chapman PB, Hauschild A, Robert C, Haanen JB, Ascierto P, Larkin J, Dummer R, Garbe C, Testori A, Maio M, et al. Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N Engl J Med. 2011;364(26):2507–2516. doi:10.1056/NEJMoa1103782.
  • Brose MS, Cabanillas ME, Cohen EEW, Wirth LJ, Riehl T, Yue H, Sherman SI, Sherman EJ. Vemurafenib in patients with BRAF(V600E)-positive metastatic or unresectable papillary thyroid cancer refractory to radioactive iodine: a non-randomised, multicentre, open-label, phase 2 trial. Lancet Oncol. 2016;17(9):1272–1282. doi:10.1016/S1470-2045(16)30166-8.
  • Hayes DN, Lucas AS, Tanvetyanon T, Krzyzanowska MK, Chung CH, Murphy BA, Gilbert J, Mehra R, Moore DT, Sheikh A, et al. Phase II efficacy and pharmacogenomic study of selumetinib (AZD6244; ARRY-142886) in iodine-131 refractory papillary thyroid carcinoma with or without follicular elements. Clin Cancer Res. 2012;18(7):2056–2065. doi:10.1158/1078-0432.CCR-11-0563.
  • Iyer PC, Dadu R, Ferrarotto R, Busaidy NL, Habra MA, Zafereo M, Gross N, Hess KR, Gule-Monroe M, Williams MD, et al. Real-world experience with targeted therapy for the treatment of anaplastic thyroid carcinoma. Thyroid. 2018;28(1):79–87. doi:10.1089/thy.2017.0285.
  • Subbiah V, Kreitman RJ, Wainberg ZA, Cho JY, Schellens JHM, Soria JC, Wen PY, Zielinski C, Cabanillas ME, Urbanowitz G, et al. Dabrafenib and trametinib treatment in patients with locally advanced or metastatic BRAF V600–mutant anaplastic thyroid cancer. J Clin Oncol. 2018;36(1):7–13. doi:10.1200/JCO.2017.73.6785.
  • Johannessen CM, Boehm JS, Kim SY, Thomas SR, Wardwell L, Johnson LA, Emery CM, Stransky N, Cogdill AP, Barretina J, et al. COT drives resistance to RAF inhibition through MAP kinase pathway reactivation. Nature. 2010;468(7326):968–972. doi:10.1038/nature09627.
  • Poulikakos PI, Persaud Y, Janakiraman M, Kong X, Ng C, Moriceau G, Shi H, Atefi M, Titz B, Gabay MT, et al. RAF inhibitor resistance is mediated by dimerization of aberrantly spliced BRAF(V600E). Nature. 2011;480(7377):387–390. doi:10.1038/nature10662.
  • Shi H, Hugo W, Kong X, Hong A, Koya RC, Moriceau G, Chodon T, Guo R, Johnson DB, Dahlman KB, et al. Acquired resistance and clonal evolution in melanoma during BRAF inhibitor therapy. Cancer Discov. 2014;4(1):80–93. doi:10.1158/2159-8290.CD-13-0642.
  • Trunzer K, Pavlick AC, Schuchter L, Gonzalez R, McArthur GA, Hutson TE, Moschos SJ, Flaherty KT, Kim KB, Weber JS, et al. Pharmacodynamic effects and mechanisms of resistance to vemurafenib in patients with metastatic melanoma. J Clin Oncol. 2013;31(14):1767–1774. doi:10.1200/JCO.2012.44.7888.
  • Villanueva J, Vultur A, Lee JT, Somasundaram R, Fukunaga-Kalabis M, Cipolla AK, Wubbenhorst B, Xu X, Gimotty PA, Kee D, et al. Acquired resistance to BRAF inhibitors mediated by a RAF kinase switch in melanoma can be overcome by cotargeting MEK and IGF-1R/PI3K. Cancer Cell. 2010;18(6):683–695. doi:10.1016/j.ccr.2010.11.023.
  • Ascierto PA, McArthur GA, Dréno B, Atkinson V, Liszkay G, Di Giacomo AM, Mandalà M, Demidov L, Stroyakovskiy D, Thomas L, et al. Cobimetinib combined with vemurafenib in advanced BRAF(V600)-mutant melanoma (coBRIM): updated efficacy results from a randomised, double-blind, phase 3 trial. Lancet Oncol. 2016;17(9):1248–1260. doi:10.1016/S1470-2045(16)30122-X.
  • Long GV, Stroyakovskiy D, Gogas H, Levchenko E, de Braud F, Larkin J, Garbe C, Jouary T, Hauschild A, Grob J-J, et al. Dabrafenib and trametinib versus dabrafenib and placebo for Val600 BRAF-mutant melanoma: a multicentre, double-blind, phase 3 randomised controlled trial. Lancet. 2015;386(9992):444–451. doi:10.1016/S0140-6736(15)60898-4.
  • Robert C, Karaszewska B, Schachter J, Rutkowski P, Mackiewicz A, Stroiakovski D, Lichinitser M, Dummer R, Grange F, Mortier L, et al. Improved overall survival in melanoma with combined dabrafenib and trametinib. N Engl J Med. 2015;372(1):30–39. doi:10.1056/NEJMoa1412690.
  • Subbiah V, Kreitman RJ, Wainberg ZA, Cho JY, Schellens JHM, Soria JC, Wen PY, Zielinski CC, Cabanillas ME, Boran A, et al. Dabrafenib plus trametinib in patients with BRAF V600E-mutant anaplastic thyroid cancer: updated analysis from the phase II ROAR basket study. Ann Oncol. 2022;33(4):406–415. doi:10.1016/j.annonc.2021.12.014.
  • Shah MH, Wei L, Wirth LJ, Daniels GA, De Souza JA, Timmers CD, Sexton JL, Beshara M, Nichols D, Snyder N, et al. Results of randomized phase II trial of dabrafenib versus dabrafenib plus trametinib in BRAF-mutated papillary thyroid carcinoma. J Clin Oncol. 2017;35(15_suppl):6022–6022. doi:10.1200/JCO.2017.35.15_suppl.6022.
  • Vader G, Medema RH, Lens SM. The chromosomal passenger complex: guiding aurora-B through mitosis. J Cell Biol. 2006;173(6):833–837. doi:10.1083/jcb.200604032.
  • Tang A, Gao K, Chu L, Zhang R, Yang J, Zheng J. Aurora kinases: novel therapy targets in cancers. Oncotarget. 2017;8(14):23937–23954. doi:10.18632/oncotarget.14893.
  • Zhao ZW, Wang H, Kang N, Wang Z, Hou X, Hu L, Qie S, Guo J, Wei S, Ruan X et al. Aurora kinase a promotes the progression of papillary thyroid carcinoma by activating the mTORC2-AKT signalling pathway. Cell Biosci 12 (2022):ARTN 19510.1186/s13578-022-00934-z
  • Schweppe RE, Pozdeyev N, Pike LA, Korch C, Zhou Q, Sams SB, Sharma V, Pugazhenthi U, Raeburn C, Albuja-Cruz MB, et al. Establishment and Characterization of four Novel Thyroid cancer Cell Lines and PDX models expressing the RET/PTC1 rearrangement, BRAFV600E, or RASQ61R as drivers. Mol Cancer Res. 2019;17(5):1036–1048. doi:10.1158/1541-7786.MCR-18-1026.
  • Landa I, Pozdeyev N, Korch C, Marlow LA, Smallridge RC, Copland JA, Henderson YC, Lai SY, Clayman GL, Onoda N, et al. Comprehensive genetic characterization of human thyroid cancer cell lines: a validated panel for preclinical studies. Clin Cancer Res. 2019;25(10):3141–3151. doi:10.1158/1078-0432.CCR-18-2953.
  • Schweppe RE, Klopper JP, Korch C, Pugazhenthi U, Benezra M, Knauf JA, Fagin JA, Marlow LA, Copland JA, Smallridge RC, et al. Deoxyribonucleic acid profiling analysis of 40 human thyroid cancer cell lines reveals cross-contamination resulting in cell line redundancy and misidentification. J Clin Endocrinol Metab. 2008;93(11):4331–4341. doi:10.1210/jc.2008-1102.
  • Hicks HM, McKenna LR, Espinoza VL, Pozdeyev N, Pike LA, Sams SB, LaBarbera D, Reigan P, Raeburn CD, Schweppe ER, et al. Inhibition of BRAF and ERK1/2 has synergistic effects on thyroid cancer growth in vitro and in vivo. Mol Carcinog. 2021;60(3):201–212. doi:10.1002/mc.23284.
  • Chou TC, Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul. 1984;22:27–55. doi:10.1016/0065-2571(84)90007-4.
  • Milella M, Konopleva M, Precupanu CM, Tabe Y, Ricciardi MR, Gregorj C, Collins SJ, Carter BZ, D’Angelo C, Petrucci MT, et al. MEK blockade converts AML differentiating response to retinoids into extensive apoptosis. Blood. 2007;109(5):2121–2129. doi:10.1182/blood-2006-05-024679.
  • Byeon HK, Na HJ, Yang YJ, Ko S, Yoon SO, Ku M, Yang J, Kim JW, Ban MJ, Kim J-H, et al. Acquired resistance to BRAF inhibition induces epithelial-to-mesenchymal transition in BRAF (V600E) mutant thyroid cancer by c-met-mediated AKT activation. Oncotarget. 2017;8(1):596–609. doi:10.18632/oncotarget.13480.
  • Byeon HK, Na HJ, Yang YJ, Kwon HJ, Chang JW, Ban MJ, Kim WS, Shin DY, Lee EJ, Koh YW, et al. C-met-mediated reactivation of PI3K/AKT signaling contributes to insensitivity of BRAF(V600E) mutant thyroid cancer to BRAF inhibition. Mol Carcinog. 2016;55(11):1678–1687. doi:10.1002/mc.22418.
  • Jin N, Jiang T, Rosen DM, Nelkin BD, Ball DW. Dual inhibition of mitogen-activated protein kinase kinase and mammalian target of rapamycin in differentiated and anaplastic thyroid cancer. J Clin Endocrinol Metab. 2009;94(10):4107–4112. doi:10.1210/jc.2009-0662.
  • Torre D, Lachmann A, Ma’ayan A. BioJupies: automated generation of Interactive Notebooks for RNA-Seq Data Analysis in the cloud. Cell Syst. 2018;7(5):556–561.e3. doi:10.1016/j.cels.2018.10.007.
  • Morris EJ, Jha S, Restaino CR, Dayananth P, Zhu H, Cooper A, Carr D, Deng Y, Jin W, Black S, et al. Discovery of a novel ERK inhibitor with activity in models of acquired resistance to BRAF and MEK inhibitors. Cancer Discov. 2013;3(7):742–750. doi:10.1158/2159-8290.CD-13-0070.
  • Hatzivassiliou G, Liu B, O’Brien C, Spoerke JM, Hoeflich KP, Haverty PM, Soriano R, Forrest WF, Heldens S, Chen H, et al. ERK inhibition overcomes acquired resistance to MEK inhibitors. Mol Cancer Ther. 2012;11(5):1143–1154. doi:10.1158/1535-7163.MCT-11-1010.
  • Li Y, Li X, Pu J, Yang Q, Guan H, Ji M, Shi B, Chen M, Hou P. C-myc is a Major determinant for antitumor activity of Aurora a kinase inhibitor MLN8237 in thyroid cancer. Thyroid. 2018;28(12):1642–1654. doi:10.1089/thy.2018.0183.
  • Zhang W, Pear WS. MYC degradation via AURKB inhibition: a new brake in the path to T-ALL. Blood Sci. 2020;2(2):68–69. doi:10.1097/BS9.0000000000000046.
  • Brockmann M, Poon E, Berry T, Carstensen A, Deubzer HE, Rycak L, Jamin Y, Thway K, Robinson SP, Roels F, et al. Small molecule inhibitors of aurora-A induce proteasomal degradation of N-Myc in childhood neuroblastoma. Cancer Cell. 2016;30(2):357–358. doi:10.1016/j.ccell.2016.07.002.
  • Lake D, Correa SA, Muller J. Negative feedback regulation of the ERK1/2 MAPK pathway. Cell Mol Life Sci. 2016;73(23):4397–4413. doi:10.1007/s00018-016-2297-8.
  • Johannessen CM, Boehm JS, Kim SY, Thomas SR, Wardwell L, Johnson LA, Emery CM, Stransky N, Cogdill AP, Barretina J, et al. COT drives resistance to RAF inhibition through MAP kinase pathway reactivation. Nature. 2010;468(7326):968–U370. doi:10.1038/nature09627.
  • Liu F, Yang X, Geng M, Huang M. Targeting ERK, an Achilles’ heel of the MAPK pathway, in cancer therapy. Acta Pharmaceutica Sinica B. 2018;8(4):552–562. doi:10.1016/j.apsb.2018.01.008.
  • Jiang J, Wang J, Yue M, Cai X, Wang T, Wu C, Su H, Wang Y, Han M, Zhang Y, et al. Direct phosphorylation and stabilization of MYC by aurora B kinase promote T-cell leukemogenesis. Cancer Cell. 2020;37(2):200–215.e5. doi:10.1016/j.ccell.2020.01.001.
  • Bavetsias V, Linardopoulos S. Aurora Kinase Inhibitors: Current Status and Outlook. Front Oncol. 2015;5:278. doi:10.3389/fonc.2015.00278.
  • Zhang M, Zhang L, Hei R, Li X, Cai H, Wu X, Zheng Q, Cai C. CDK inhibitors in cancer therapy, an overview of recent development. Am J Cancer Res. 2021;11(5):1913–1935.
  • Zeidan AM, Ridinger M, Lin TL, Becker PS, Schiller GJ, Patel PA, Spira AI, Tsai ML, Samuëlsz E, Silberman SL, et al. A phase ib study of Onvansertib, a Novel Oral PLK1 Inhibitor, in combination therapy for patients with relapsed or refractory acute myeloid leukemia. Clin Cancer Res. 2020;26(23):6132–6140. doi:10.1158/1078-0432.CCR-20-2586.
  • Triscott J, Lee C, Hu K, Fotovati A, Berns R, Pambid M, Luk M, Kast RE, Kong E, Toyota E, et al. Disulfiram, a drug widely used to control alcoholism, suppresses the self-renewal of glioblastoma and over-rides resistance to temozolomide. Oncotarget. 2012;3(10):1112–1123. doi:10.18632/oncotarget.604.
  • Rapino F, Naumann I, Fulda S. Bortezomib antagonizes microtubule-interfering drug-induced apoptosis by inhibiting G2/M transition and MCL-1 degradation. Cell Death Disease. 2013;4(11):e925. doi:10.1038/cddis.2013.440.
  • Lin SF, Lin J-D, Yeh C-N, Huang Y-T, Chou T-C, Wong RJ. Targeting PLKs as a therapeutic approach to well-differentiated thyroid cancer. Endocr-Relat Cancer. 2019;26(8):727–738. doi:10.1530/ERC-18-0555.
  • Roskoski R Jr. ERK1/2 MAP kinases: structure, function, and regulation. Pharmacol Res. 2012;66(2):105–143. doi:10.1016/j.phrs.2012.04.005.
  • Lachmann A, Xu H, Krishnan J, Berger SI, Mazloom AR, Ma’ayan A. ChEA: transcription factor regulation inferred from integrating genome-wide ChIP-X experiments. Bioinformatics. 2010;26(19):2438–2444. doi:10.1093/bioinformatics/btq466.
  • Hicks HM, Pozdeyev N, Sams SB, Pugazhenthi U, Bales ES, Hofmann M-C, McKenna LR, Schweppe RE. Fibronectin contributes to a BRAF Inhibitor–driven invasive phenotype in thyroid cancer through EGR1, which can Be blocked by inhibition of ERK1/2. Mol Cancer Res. 2023;21(9):867–880. doi:10.1158/1541-7786.MCR-22-1031.
  • Gully CP, Velazquez-Torres G, Shin J-H, Fuentes-Mattei E, Wang E, Carlock C, Chen J, Rothenberg D, Adams HP, Choi HH, et al. Aurora B kinase phosphorylates and instigates degradation of p53. Proc Natl Acad Sci U S A. 2012;109(24):E1513–1522. doi:10.1073/pnas.1110287109.
  • Rose MM, Espinoza VL, Hoff KJ, Pike LA, Sharma V, Hofmann M-C, Tan AC, Pozdeyev N, Schweppe RE. BCL2L11 induction mediates sensitivity to src and MEK1/2 inhibition in thyroid cancer. Cancers Basel. 2023;15(2):378. doi:10.3390/cancers15020378.