5,981
Views
22
CrossRef citations to date
0
Altmetric
Original Research

Characterization of immune landscape in papillary thyroid cancer reveals distinct tumor immunogenicity and implications for immunotherapy

, , , , , , , , , , ORCID Icon & show all
Article: 1964189 | Received 23 Apr 2021, Accepted 30 Jul 2021, Published online: 07 Sep 2021

References

  • Siegel RL, Miller KD, Jemal A. Cancer statistics, 2020. CA Cancer J Clin. 2020;70(1):7–14. doi:10.3322/caac.21590.
  • McQueen AS, Bhatia KS. Thyroid nodule ultrasound: technical advances and future horizons. Insights Imaging. 2015;6(2):173–188. doi:10.1007/s13244-015-0398-9.
  • Cabanillas ME, McFadden DG, Durante C. Thyroid cancer. Lancet. 2016;388(10061):2783–2795. doi:10.1016/S0140-6736(16)30172-6.
  • Haugen BR, Alexander EK, Bible KC, Doherty GM, Mandel SJ, Nikiforov YE, et al. 2015 American Thyroid Association management guidelines for adult patients with thyroid nodules and differentiated thyroid cancer: the american thyroid association guidelines task force on thyroid nodules and differentiated thyroid cancer. Thyroid. 2016;26(1):1–133. doi:10.1089/thy.2015.0020.
  • Sipos JA, Mazzaferri EL. Thyroid cancer epidemiology and prognostic variables. Clin Oncol (R Coll Radiol). 2010;22(6):395–404. doi:10.1016/j.clon.2010.05.004.
  • Ito Y, Miyauchi A, Kihara M, Fukushima M, Higashiyama T, Miya A. Overall survival of papillary thyroid carcinoma patients: a single-institution long-term follow-up of 5897 patients. World J Surg. 2018;42(3):615–622. doi:10.1007/s00268-018-4479-z.
  • Junttila MR, de Sauvage FJ. Influence of tumour micro-environment heterogeneity on therapeutic response. Nature. 2013;501(7467):346–354. doi:10.1038/nature12626.
  • Gonzalez H, Hagerling C, Werb Z. Roles of the immune system in cancer: from tumor initiation to metastatic progression. Genes Dev. 2018;32(19–20):1267–1284. doi:10.1101/gad.314617.118.
  • Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: integrating immunity’s roles in cancer suppression and promotion. Science. 2011;331(6024):1565–1570. doi:10.1126/science.1203486.
  • Dunn GP, Old LJ, Schreiber RD. The immunobiology of cancer immunosurveillance and immunoediting. Immunity. 2004;21(2):137–148. doi:10.1016/j.immuni.2004.07.017.
  • Dunn GP, Bruce AT, Ikeda H, Old LJ, Schreiber RD. Cancer immunoediting: from immunosurveillance to tumor escape. Nat Immunol. 2002;3(11):991–998. doi:10.1038/ni1102-991.
  • Mellman I, Coukos G, Dranoff G. Cancer immunotherapy comes of age. Nature. 2011;480(7378):480–489. doi:10.1038/nature10673.
  • Hodi FS, O’Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med. 2010;363(8):711–723. doi:10.1056/NEJMoa1003466.
  • Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med. 2012;366(26):2443–2454. doi:10.1056/NEJMoa1200690.
  • Choueiri TK, Escudier B, Powles T, Mainwaring PN, Rini BI, Donskov F, et al. Cabozantinib versus everolimus in advanced renal-cell carcinoma. N Engl J Med. 2015;373(19):1814–1823. doi:10.1056/NEJMoa1510016.
  • Gunda V, Gigliotti B, Ndishabandi D, Ashry T, McCarthy M, Zhou Z, et al. Combinations of BRAF inhibitor and anti-PD-1/PD-L1 antibody improve survival and tumour immunity in an immunocompetent model of orthotopic murine anaplastic thyroid cancer. Br J Cancer. 2018;119(10):1223–1232. doi:10.1038/s41416-018-0296-2.
  • Gunda V, Gigliotti B, Ashry T, Ndishabandi D, McCarthy M, Zhou Z, et al. Anti-PD-1/PD-L1 therapy augments lenvatinib’s efficacy by favorably altering the immune microenvironment of murine anaplastic thyroid cancer. Int J Cancer. 2019;144(9):2266–2278. doi:10.1002/ijc.32041.
  • French JD. Immunotherapy for advanced thyroid cancers - rationale, current advances and future strategies. Nat Rev Endocrinol. 2020;16(11):629–641. doi:10.1038/s41574-020-0398-9.
  • Moretti S, Menicali E, Nucci N, Guzzetti M, Morelli S, Puxeddu E. THERAPY OF ENDOCRINE DISEASE Immunotherapy of advanced thyroid cancer: from bench to bedside. Eur J Endocrinol. 2020;183(2):R41–R55. doi:10.1530/EJE-20-0283.
  • Bhattacharya S, Andorf S, Gomes L, Dunn P, Schaefer H, Pontius J, et al. ImmPort: disseminating data to the public for the future of immunology. Immunol Res. 2014;58(2–3):234–239. doi:10.1007/s12026-014-8516-1.
  • Tomas G, Tarabichi M, Gacquer D, Hebrant A, Dom G, Dumont JE, et al. A general method to derive robust organ-specific gene expression-based differentiation indices: application to thyroid cancer diagnostic. Oncogene. 2012;31(41):4490–4498. doi:10.1038/onc.2011.626.
  • Tarabichi M, Saiselet M, Tresallet C, Hoang C, Larsimont D, Andry G, et al. Revisiting the transcriptional analysis of primary tumours and associated nodal metastases with enhanced biological and statistical controls: application to thyroid cancer. Br J Cancer. 2015;112(10):1665–1674. doi:10.1038/bjc.2014.665.
  • He H, Jazdzewski K, Li W, Liyanarachchi S, Nagy R, Volinia S, et al. The role of microRNA genes in papillary thyroid carcinoma. Proc Natl Acad Sci U S A. 2005;102(52):19075–19080. doi:10.1073/pnas.0509603102.
  • Giordano TJ, Kuick R, Thomas DG, Misek DE, Vinco M, Sanders D, et al. Molecular classification of papillary thyroid carcinoma: distinct BRAF, RAS, and RET/PTC mutation-specific gene expression profiles discovered by DNA microarray analysis. Oncogene. 2005;24(44):6646–6656. doi:10.1038/sj.onc.1208822.
  • Cancer Genome Atlas Research N. Integrated genomic characterization of papillary thyroid carcinoma. Cell. 2014;159(3):676–690. doi:10.1016/j.cell.2014.09.050.
  • Consortium GT. The genotype-tissue expression (GTEx) project. Nat Genet. 2013;45(6):580–585. doi:10.1038/ng.2653.
  • Shi R, Bao X, Sun J, Lu S, Belka C, Li M. Tumor microenvironment characterization in head and neck squamous carcinoma reveals distinct genomic alterations and clinical outcomes. Clin Transl Med. 2020;10(5):e187. doi:10.1002/ctm2.187.
  • Shi R, Bao X, Unger K, Sun J, Lu S, Manapov F, et al. Identification and validation of hypoxia-derived gene signatures to predict clinical outcomes and therapeutic responses in stage I lung adenocarcinoma patients. Theranostics. 2021;11(10):5061–5076. doi:10.7150/thno.56202.
  • Sun J, Zhao T, Zhao D, Qi X, Bao X, Shi R, et al. Development and validation of a hypoxia-related gene signature to predict overall survival in early-stage lung adenocarcinoma patients. Ther Adv Med Oncol. 2020;12:1758835920937904. doi:10.1177/1758835920937904.
  • Chalmers ZR, Connelly CF, Fabrizio D, Gay L, Ali SM, Ennis R, et al. Analysis of 100,000 human cancer genomes reveals the landscape of tumor mutational burden. Genome Med. 2017;9(1):34. doi:10.1186/s13073-017-0424-2.
  • Aran D, Hu Z, Butte AJ. xCell: digitally portraying the tissue cellular heterogeneity landscape. Genome Biol. 2017;18(1):220. doi:10.1186/s13059-017-1349-1.
  • Yoshihara K, Shahmoradgoli M, Martinez E, Vegesna R, Kim H, Torres-Garcia W, et al. Inferring tumour purity and stromal and immune cell admixture from expression data. Nat Commun. 2013;4:2612. doi:10.1038/ncomms3612.
  • Chen B, Khodadoust MS, Liu CL, Newman AM, Alizadeh AA. Profiling tumor infiltrating immune cells with CIBERSORT. Methods Mol Biol. 2018;1711:243–259. doi:10.1007/978-1-4939-7493-1_12.
  • Rooney MS, Shukla SA, Wu CJ, Getz G, Hacohen N. Molecular and genetic properties of tumors associated with local immune cytolytic activity. Cell. 2015;160(1–2):48–61. doi:10.1016/j.cell.2014.12.033.
  • Langfelder P, Horvath S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinform. 2008;9:559. doi:10.1186/1471-2105-9-559.
  • Liberzon A, Birger C, Thorvaldsdottir H, Ghandi M, Mesirov JP, Tamayo P. The molecular signatures database (MSigDB) hallmark gene set collection. Cell Syst. 2015;1(6):417–425. doi:10.1016/j.cels.2015.12.004.
  • Jiang P, Gu S, Pan D, Fu J, Sahu A, Hu X, et al. Signatures of T cell dysfunction and exclusion predict cancer immunotherapy response. Nat Med. 2018;24(10):1550–1558. doi:10.1038/s41591-018-0136-1.
  • Zhou Y, Zhou B, Pache L, Chang M, Khodabakhshi AH, Tanaseichuk O, et al. Metascape provides a biologist-oriented resource for the analysis of systems-level datasets. Nat Commun. 2019;10(1):1523. doi:10.1038/s41467-019-09234-6.
  • Subramanian A, Narayan R, Corsello SM, Peck DD, Natoli TE, Lu X, et al. A next generation connectivity map: L1000 platform and the first 1,000,000 profiles. Cell. 2017;171(6):1437–1452 e1417. doi:10.1016/j.cell.2017.10.049.
  • Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646–674. doi:10.1016/j.cell.2011.02.013.
  • Wang Y, Chen C, Wang X, Jin F, Liu Y, Liu H, et al. Lower DSC1 expression is related to the poor differentiation and prognosis of head and neck squamous cell carcinoma (HNSCC). J Cancer Res Clin Oncol. 2016;142(12):2461–2468. doi:10.1007/s00432-016-2233-1.
  • Myklebust MP, Fluge O, Immervoll H, Skarstein A, Balteskard L, Bruland O, et al. Expression of DSG1 and DSC1 are prognostic markers in anal carcinoma patients. Br J Cancer. 2012;106(4):756–762. doi:10.1038/bjc.2011.548.
  • Katsuta E, Maawy AA, Yan L, Takabe K. High expression of bone morphogenetic protein (BMP) 6 and BMP7 are associated with higher immune cell infiltration and better survival in estrogen receptorpositive breast cancer. Oncol Rep. 2019;42(4):1413–1421. doi:10.3892/or.2019.7275.
  • Moossavi M, Parsamanesh N, Bahrami A, Atkin SL, Sahebkar A. Role of the NLRP3 inflammasome in cancer. Mol Cancer. 2018;17(1):158. doi:10.1186/s12943-018-0900-3.
  • Fernandez-Nogueira P, Noguera-Castells A, Fuster G, Recalde-Percaz L, Moragas N, Lopez-Plana A, et al. Histamine receptor 1 inhibition enhances antitumor therapeutic responses through extracellular signal-regulated kinase (ERK) activation in breast cancer. Cancer Lett. 2018;424:70–83. doi:10.1016/j.canlet.2018.03.014.
  • Shi Z, Fultz RS, Engevik MA, Gao C, Hall A, Major A, et al. Distinct roles of histamine H1- and H2-receptor signaling pathways in inflammation-associated colonic tumorigenesis. Am J Physiol Gastrointest Liver Physiol. 2019;316(1):G205–G216. doi:10.1152/ajpgi.00212.2018.
  • Na KJ, Choi H. Immune landscape of papillary thyroid cancer and immunotherapeutic implications. Endocr Relat Cancer. 2018;25(5):523–531. doi:10.1530/ERC-17-0532.
  • Walle T, Martinez Monge R, Cerwenka A, Ajona D, Melero I, Lecanda F. Radiation effects on antitumor immune responses: current perspectives and challenges. Ther Adv Med Oncol. 2018;10:1758834017742575. doi:10.1177/1758834017742575.
  • Al-Abdallah A, Jahanbani I, Mehdawi H, Ali RH, Al-Brahim N, Mojiminiyi O, et al. Down-regulation of the human major histocompatibility complex class I chain-related gene A (MICA) and its receptor is mediated by microRNA-146b-5p and is a potential mechanism of immunoediting in papillary thyroid carcinoma. Exp Mol Pathol. 2020;113:104379. doi:10.1016/j.yexmp.2020.104379.
  • Stenman A, Backman S, Johansson K, Paulsson JO, Stalberg P, Zedenius J, et al. Pan-genomic characterization of high-risk pediatric papillary thyroid carcinoma. Endocr Relat Cancer. 2021;28(5):337–351. doi:10.1530/ERC-20-0464.