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Research Paper

p18INK4C and BRCA1 inhibit follicular cell proliferation and dedifferentiation in thyroid cancer

, , , , , & ORCID Icon show all
Pages 1637-1653 | Received 09 Sep 2022, Accepted 09 Jun 2023, Published online: 22 Jun 2023

References

  • Du L, Zhao Z, Zheng R, et al. Epidemiology of Thyroid Cancer: incidence and Mortality in China, 2015. Front Oncol. 2020;10:1702. doi:10.3389/fonc.2020.01702
  • Lim H, Devesa SS, Sosa JA, et al. Trends in thyroid cancer incidence and mortality in the United States, 1974-2013. JAMA. 2017;317(13):1338–1348. DOI:10.1001/jama.2017.2719
  • Kondo T, Ezzat S, Asa SL. Pathogenetic mechanisms in thyroid follicular-cell neoplasia. Nat Rev Cancer. 2006;6(4):292–306. doi:10.1038/nrc1836.
  • Taccaliti A, Silvetti F, Palmonella G, et al. Anaplastic thyroid carcinoma. Front Endocrinol. 2012;3:84. doi:10.3389/fendo.2012.00084
  • Zane M, Scavo E, Catalano V, et al. Normal vs cancer thyroid stem cells: the road to transformation. Oncogene. 2016;35(7):805–815. DOI:10.1038/onc.2015.138
  • Bhaijee F, Nikiforov YE. Molecular analysis of thyroid tumors. Endocr Pathol. 2011;22(3):126–133. doi:10.1007/s12022-011-9170-y.
  • Agrawal N, Akbani R, Aksoy B&, et al. Integrated genomic characterization of papillary thyroid carcinoma. Cell. 2014;159(3):676–690. DOI:10.1016/j.cell.2014.09.050
  • Ron E, Lubin JH, Shore RE, et al. Thyroid cancer after exposure to external radiation: a pooled analysis of seven studies. Radiat Res. 1995;141(3):259–277. DOI:10.2307/3579003
  • Daniels GH. Follicular variant of papillary thyroid carcinoma: hybrid or mixture? Thyroid: Offic J Am Thyroid Association. 2016;26(7):872–874. doi:10.1089/thy.2016.0244.
  • Shih HA, Nathanson KL, Seal S, et al. BRCA1 and BRCA2 mutations in breast cancer families with multiple primary cancers. Clin Cancer Res. 2000;6(11):4259–4264.
  • Xu L, Doan PC, Wei Q, et al. Association of BRCA1 functional single nucleotide polymorphisms with risk of differentiated thyroid carcinoma. Thyroid: Offic J Am Thyroid Association. 2012;22(1):35–43. DOI:10.1089/thy.2011.0117
  • Streff H, Profato J, Ye Y, et al. Cancer incidence in first- and second-degree relatives of BRCA1 and BRCA2 mutation carriers. Oncology. 2016;21(7):869–874. DOI:10.1634/theoncologist.2015-0354
  • Hincza K, Kowalik A, Kowalska A. Current knowledge of germline genetic risk factors for the development of non-medullary thyroid cancer. Genes (Basel). 2019;10(7):482. doi:10.3390/genes10070482.
  • Wojcicka A, Czetwertynska M, Swierniak M, et al. Variants in the ATM-CHEK2-BRCA1 axis determine genetic predisposition and clinical presentation of papillary thyroid carcinoma. Genes Chromosomes Cancer. 2014;53(6):516–523. DOI:10.1002/gcc.22162
  • Galetzka D, Hansmann T, El Hajj N, et al. Monozygotic twins discordant for constitutive BRCA1 promoter methylation, childhood cancer and secondary cancer. Epigenetics. 2012;7(1):47–54. DOI:10.4161/epi.7.1.18814
  • Penha RCC, Lima SCS, Boroni M, et al. Intrinsic LINE-1 hypomethylation and decreased Brca1 expression are associated with DNA repair delay in irradiated thyroid cells. Radiat Res. 2017;188(2):144–155. DOI:10.1667/RR14532.1
  • Bai F, Chan HL, Scott A, et al. BRCA1 suppresses epithelial-to-mesenchymal transition and stem cell dedifferentiation during mammary and tumor development. Cancer Res. 2014;74(21):6161–6172. DOI:10.1158/0008-5472.CAN-14-1119
  • Pei XH, Xiong Y. Biochemical and cellular mechanisms of mammalian CDK inhibitors: a few unresolved issues. Oncogene. 2005;24(17):2787–2795. doi:10.1038/sj.onc.1208611.
  • Kunstman JW, Juhlin CC, Goh G, et al. Characterization of the mutational landscape of anaplastic thyroid cancer via whole-exome sequencing. Hum Mol Genet. 2015;24(8):2318–2329. DOI:10.1093/hmg/ddu749
  • Grubbs EG, Williams MD, Scheet P, et al. Role of CDKN2C copy number in sporadic medullary thyroid carcinoma. Thyroid: Offic J Am Thyroid Association. 2016;26(11):1553–1562. DOI:10.1089/thy.2016.0224
  • Pita JM, Figueiredo IF, Moura MM, et al. Cell cycle deregulation and TP53 and RAS mutations are major events in poorly differentiated and undifferentiated thyroid carcinomas. J Clin Endocrinol Metab. 2014;99(3):E497–507. DOI:10.1210/jc.2013-1512
  • Neta G, Brenner AV, Sturgis EM, et al. Common genetic variants related to genomic integrity and risk of papillary thyroid cancer. Carcinogenesis. 2011;32(8):1231–1237. DOI:10.1093/carcin/bgr100
  • van Veelen W, Klompmaker R, Gloerich M, et al. P18 is a tumor suppressor gene involved in human medullary thyroid carcinoma and pheochromocytoma development. Int J Cancer. 2009;124(2):339–345. DOI:10.1002/ijc.23977
  • Maxwell JE, Gule-Monroe MK, Subbiah V, et al. Novel use of a Clinical Laboratory Improvements Amendments (CLIA)-certified Cyclin-Dependent Kinase N2C (CDKN2C) loss assay in sporadic medullary thyroid carcinoma. Surgery. 2020;167(1):80–86. DOI:10.1016/j.surg.2019.03.041
  • Franklin DS, Godfrey VL, O’Brien DA, et al. Functional collaboration between different cyclin-dependent kinase inhibitors suppresses tumor growth with distinct tissue specificity. Mol Cell Biol. 2000;20(16):6147–6158. DOI:10.1128/MCB.20.16.6147-6158.2000
  • Bai F, Pei XH, Nishikawa T, et al. P18ink4c, but not p27Kip1, collaborates with Men1 to suppress neuroendocrine organ tumors. Mol Cell Biol. 2007;27(4):1495–1504. doi:10.1128/MCB.01764-06.
  • Bai F, Pei XH, Pandolfi PP, et al. P18 Ink4c and Pten constrain a positive regulatory loop between cell growth and cell cycle control. Mol Cell Biol. 2006;26(12):4564–4576. doi:10.1128/MCB.00266-06.
  • Nikitin AY, Juarez-Perez MI, Li S, et al. RB-mediated suppression of spontaneous multiple neuroendocrine neoplasia and lung metastases in Rb± mice. Proc Natl Acad Sci U S A. 1999;96(7):3916–3921. doi:10.1073/pnas.96.7.3916.
  • Williams BO, Remington L, Albert DM, et al. Cooperative tumorigenic effects of germline mitations in Rb and p53. Nature Genet. 1994;7:480–484. doi: 10.1038/ng0894-480
  • Loffler KA, Biondi CA, Gartside MG, et al. Lack of augmentation of tumor spectrum or severity in dual heterozygous Men1 and Rb1 knockout mice. Oncogene. 2007;26(27):4009–4017. DOI:10.1038/sj.onc.1210163
  • Sharpless NE, Bardeesy N, Lee KH, et al. Loss of p16Ink4a with retention of p19Arf predisposes mice to tumorigenesis. Nature. 2001;413(6851):86–91. DOI:10.1038/35092592
  • Bai F, Chan HL, Smith MD, et al. P19ink4d is a tumor suppressor and controls pituitary anterior lobe cell proliferation. Mol Cell Biol. 2014;34(12):2121–2134. doi:10.1128/MCB.01363-13.
  • Sherr CJ, McCormick F. The RB and p53 pathways in cancer. Cancer Cell. 2002;2(2):103–112. doi:10.1016/S1535-6108(02)00102-2.
  • Cranston AN, Ponder BA. Modulation of medullary thyroid carcinoma penetrance suggests the presence of modifier genes in a RET transgenic mouse model. Cancer Res. 2003;63(16):4777–4780.
  • Tiozzo C, Danopoulos S, Lavarreda-Pearce M, et al. Embryonic epithelial Pten deletion through Nkx2.1-cre leads to thyroid tumorigenesis in a strain-dependent manner. Endocr Relat Cancer. 2012;19(2):111–122. DOI:10.1530/ERC-10-0327
  • Frith CH, Heath JE. Morphological classification and incidence of thyroid tumors in untreated aged mice. J Gerontol. 1984;39(1):7–10. doi:10.1093/geronj/39.1.7.
  • Freeman D, Lesche R, Kertesz N, et al. Genetic background controls tumor development in PTEN-deficient mice. Cancer Res. 2006;66(13):6492–6496. DOI:10.1158/0008-5472.CAN-05-4143
  • Bai F, Smith MD, Chan HL, et al. Germline mutation of Brca1 alters the fate of mammary luminal cells and causes luminal-to-basal mammary tumor transformation. Oncogene. 2013;32(22):2715–2725. DOI:10.1038/onc.2012.293
  • Scott A, Bai F, Chan HL, et al. P16ink4a suppresses BRCA1-deficient mammary tumorigenesis. Oncotarget. 2016;7(51):84496–84507. DOI:10.18632/oncotarget.13015
  • Sedic M, Skibinski A, Brown N, et al. Haploinsufficiency for BRCA1 leads to cell-type-specific genomic instability and premature senescence. Nat Commun. 2015;6(1):7505. DOI:10.1038/ncomms8505
  • Franklin DS, Godfrey VL, Lee H, et al. CDK inhibitors p18(INK4c) and p27(Kip1) mediate two separate pathways to collaboratively suppress pituitary tumorigenesis. Genes Dev. 1998;12(18):2899–2911. DOI:10.1101/gad.12.18.2899
  • Pei XH, Bai F, Smith MD, et al. CDK inhibitor p18(INK4c) is a downstream target of GATA3 and restrains mammary luminal progenitor cell proliferation and tumorigenesis. Cancer Cell. 2009;15(5):389–401. DOI:10.1016/j.ccr.2009.03.004
  • Bai F, Wang C, Liu X, et al. Loss of function of BRCA1 promotes EMT in mammary tumors through activation of TGFbetaR2 signaling pathway. Cell Death Dis. 2022;13(3):195. DOI:10.1038/s41419-022-04646-7
  • Bai F, Zhang LH, Liu X, et al. GATA3 functions downstream of BRCA1 to suppress EMT in breast cancer. Theranostics. 2021;11(17):8218–8233. DOI:10.7150/thno.59280
  • Tang Z, Li C, Kang B, et al. GEPIA: a web server for cancer and normal gene expression profiling and interactive analyses. Nucleic Acids Res. 2017;45(W1):W98–w102. DOI:10.1093/nar/gkx247
  • TCGAR N. Integrated genomic characterization of papillary thyroid carcinoma. Cell. 2014;159(3):676–690. doi:10.1016/j.cell.2014.09.050.
  • Cerami E, Gao J, Dogrusoz U, et al. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov. 2012;2(5):401–404. DOI:10.1158/2159-8290.CD-12-0095
  • Bai F, Liu S, Liu X, et al. Pdgfrbeta is an essential therapeutic target for BRCA1-deficient mammary tumors. Breast Cancer Res. 2021;23(1):10. DOI:10.1186/s13058-021-01387-x
  • Pozdeyev N, Gay LM, Sokol ES, et al. Genetic analysis of 779 advanced differentiated and anaplastic thyroid cancers. Clin Cancer Res. 2018;24(13):3059–3068. DOI:10.1158/1078-0432.CCR-18-0373
  • Yoo SK, Song YS, Lee EK, et al. Integrative analysis of genomic and transcriptomic characteristics associated with progression of aggressive thyroid cancer. Nat Commun. 2019;10. doi:10.1038/s41467-019-10680-5.
  • Zou MJ, Shi YF, Farid NR, et al. Inverse association between cyclin D1 overexpression and retinoblastoma gene mutation in thyroid carcinomas. Endocrine. 1998;8(1):61–64. doi:10.1385/ENDO:8:1:61.
  • Kim JH, Jeong JY, Seo AN, et al. Genomic profiling of aggressive thyroid cancer in association with its clinicopathological characteristics. In Vivo. 2022;36(1):111–120. doi:10.21873/invivo.12682.
  • Lee HJ, Lee WK, Kang CW, et al. A selective cyclin-dependent kinase 4, 6 dual inhibitor, Ribociclib (LEE011) inhibits cell proliferation and induces apoptosis in aggressive thyroid cancer. Cancer Lett. 2018;417:131–140. doi:10.1016/j.canlet.2017.12.037
  • Sotillo R, Dubus P, Martin J, et al. Wide spectrum of tumors in knock-in mice carrying a Cdk4 protein insensitive to INK4 inhibitors. Embo J. 2001;20(23):6637–6647. DOI:10.1093/emboj/20.23.6637
  • Schagdarsurengin U, Gimm O, Hoang-Vu C, et al. Frequent epigenetic silencing of the CpG island promoter of RASSF1A in thyroid carcinoma. Cancer Res. 2002;62(13):3698–3701.
  • Ragazzi M, Torricelli F, Donati B, et al. Coexisting well-differentiated and anaplastic thyroid carcinoma in the same primary resection specimen: immunophenotypic and genetic comparison of the two components in a consecutive series of 13 cases and a review of the literature. Virchows Arch. 2021;478(2):265–281. DOI:10.1007/s00428-020-02891-9
  • Volante M, Lam AK, Papotti M, et al. Molecular pathology of poorly differentiated and anaplastic thyroid cancer: what do pathologists need to know. Endocr Pathol. 2021;32(1):63–76. doi:10.1007/s12022-021-09665-2.
  • McFadden DG, Vernon A, Santiago PM, et al. P53 constrains progression to anaplastic thyroid carcinoma in a Braf-mutant mouse model of papillary thyroid cancer. P Natl Acad Sci USA. 2014;111(16):E1600–E9. DOI:10.1073/pnas.1404357111
  • Powell DJ, Russell JP, Li GQ, et al. Altered gene expression in immunogenic poorly differentiated thyroid carcinomas from RET/PTC3p53 mice. Oncogene. 2001;20(25):3235–3246. DOI:10.1038/sj.onc.1204425
  • Proia TA, Keller PJ, Gupta PB, et al. Genetic predisposition directs breast cancer phenotype by dictating progenitor cell fate. Cell Stem Cell. 2011;8(2):149–163. DOI:10.1016/j.stem.2010.12.007
  • Tkocz D, Crawford NT, Buckley NE, et al. BRCA1 and GATA3 corepress FOXC1 to inhibit the pathogenesis of basal-like breast cancers. Oncogene. 2011;31(32):3667–3678. DOI:10.1038/onc.2011.531
  • Tam WL, Lu H, Buikhuisen J, et al. Protein kinase C alpha is a central signaling node and therapeutic target for breast cancer stem cells. Cancer Cell. 2013;24(3):347–364. DOI:10.1016/j.ccr.2013.08.005

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