Impact of Cancer Evolution on Immune Surveillance and Checkpoint Inhibitor Response

Overview

Journal Semin Cancer Biol

Specialty Oncology

Date 2021 Feb 25

PMID 33631295

Citations 18

Authors

Yin Wu

Dhruva Biswas

Charles Swanton

Affiliations

Soon will be listed here.

Abstract

Intratumour heterogeneity (ITH) is pervasive across all cancers studied and may provide the evolving tumour multiple routes to escape immune surveillance. Immune checkpoint inhibitors (CPIs) are rapidly becoming standard of care for many cancers. Here, we discuss recent work investigating the influence of ITH on patient response to immune checkpoint inhibitor (CPI) therapy. At its simplest, ITH may confound the diagnostic accuracy of predictive biomarkers used to stratify patients for CPI therapy. Furthermore, ITH is fuelled by mechanisms of genetic instability that can both engage immune surveillance and drive immune evasion. A greater appreciation of the interplay between ITH and the immune system may hold the key to increasing the proportion of patients experiencing durable responses from CPI therapy.

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References

Campbell P, Yachida S, Mudie L, Stephens P, Pleasance E, Stebbings L . The patterns and dynamics of genomic instability in metastatic pancreatic cancer. Nature. 2010; 467(7319):1109-13. PMC: 3137369. DOI: 10.1038/nature09460. View

Witkowska M, Smolewski P . Immune Checkpoint Inhibitors to Treat Malignant Lymphomas. J Immunol Res. 2018; 2018:1982423. PMC: 5925139. DOI: 10.1155/2018/1982423. View

Salgado R, Denkert C, Demaria S, Sirtaine N, Klauschen F, Pruneri G . The evaluation of tumor-infiltrating lymphocytes (TILs) in breast cancer: recommendations by an International TILs Working Group 2014. Ann Oncol. 2014; 26(2):259-71. PMC: 6267863. DOI: 10.1093/annonc/mdu450. View

Gerstung M, Jolly C, Leshchiner I, Dentro S, Gonzalez S, Rosebrock D . The evolutionary history of 2,658 cancers. Nature. 2020; 578(7793):122-128. PMC: 7054212. DOI: 10.1038/s41586-019-1907-7. View

Lawrence M, Stojanov P, Polak P, Kryukov G, Cibulskis K, Sivachenko A . Mutational heterogeneity in cancer and the search for new cancer-associated genes. Nature. 2013; 499(7457):214-218. PMC: 3919509. DOI: 10.1038/nature12213. View

Stich H, FLORIAN S, Emson H . The DNA content of tumor cells. 1. Polyps and adenocarcinomas of the intestine of man. J Natl Cancer Inst. 1960; 24:471-82. View

Reuben A, Zhang J, Chiou S, Gittelman R, Li J, Lee W . Comprehensive T cell repertoire characterization of non-small cell lung cancer. Nat Commun. 2020; 11(1):603. PMC: 6992630. DOI: 10.1038/s41467-019-14273-0. View

Zhang Q, Luo J, Wu S, Si H, Gao C, Xu W . Prognostic and Predictive Impact of Circulating Tumor DNA in Patients with Advanced Cancers Treated with Immune Checkpoint Blockade. Cancer Discov. 2020; 10(12):1842-1853. PMC: 8358981. DOI: 10.1158/2159-8290.CD-20-0047. View

Snyder A, Makarov V, Merghoub T, Yuan J, Zaretsky J, Desrichard A . Genetic basis for clinical response to CTLA-4 blockade in melanoma. N Engl J Med. 2014; 371(23):2189-2199. PMC: 4315319. DOI: 10.1056/NEJMoa1406498. View

10.

McGranahan N, Rosenthal R, Hiley C, Rowan A, Watkins T, Wilson G . Allele-Specific HLA Loss and Immune Escape in Lung Cancer Evolution. Cell. 2017; 171(6):1259-1271.e11. PMC: 5720478. DOI: 10.1016/j.cell.2017.10.001. View

11.

Brattain M, Fine W, Khaled F, Thompson J, Brattain D . Heterogeneity of malignant cells from a human colonic carcinoma. Cancer Res. 1981; 41(5):1751-6. View

12.

Gubin M, Zhang X, Schuster H, Caron E, Ward J, Noguchi T . Checkpoint blockade cancer immunotherapy targets tumour-specific mutant antigens. Nature. 2014; 515(7528):577-81. PMC: 4279952. DOI: 10.1038/nature13988. View

13.

Kazdal D, Endris V, Allgauer M, Kriegsmann M, Leichsenring J, Volckmar A . Spatial and Temporal Heterogeneity of Panel-Based Tumor Mutational Burden in Pulmonary Adenocarcinoma: Separating Biology From Technical Artifacts. J Thorac Oncol. 2019; 14(11):1935-1947. DOI: 10.1016/j.jtho.2019.07.006. View

14.

DAngelo S, Russell J, Lebbe C, Chmielowski B, Gambichler T, Grob J . Efficacy and Safety of First-line Avelumab Treatment in Patients With Stage IV Metastatic Merkel Cell Carcinoma: A Preplanned Interim Analysis of a Clinical Trial. JAMA Oncol. 2018; 4(9):e180077. PMC: 5885245. DOI: 10.1001/jamaoncol.2018.0077. View

15.

Riaz N, Havel J, Makarov V, Desrichard A, Urba W, Sims J . Tumor and Microenvironment Evolution during Immunotherapy with Nivolumab. Cell. 2017; 171(4):934-949.e16. PMC: 5685550. DOI: 10.1016/j.cell.2017.09.028. View

16.

Madore J, Vilain R, Menzies A, Kakavand H, Wilmott J, Hyman J . PD-L1 expression in melanoma shows marked heterogeneity within and between patients: implications for anti-PD-1/PD-L1 clinical trials. Pigment Cell Melanoma Res. 2014; 28(3):245-53. DOI: 10.1111/pcmr.12340. View

17.

Chen Z, Zhong W, Zhang X, Su J, Yang X, Chen Z . EGFR mutation heterogeneity and the mixed response to EGFR tyrosine kinase inhibitors of lung adenocarcinomas. Oncologist. 2012; 17(7):978-85. PMC: 3399655. DOI: 10.1634/theoncologist.2011-0385. View

18.

Ayers M, Lunceford J, Nebozhyn M, Murphy E, Loboda A, Kaufman D . IFN-γ-related mRNA profile predicts clinical response to PD-1 blockade. J Clin Invest. 2017; 127(8):2930-2940. PMC: 5531419. DOI: 10.1172/JCI91190. View

19.

Greaves M . Evolutionary determinants of cancer. Cancer Discov. 2015; 5(8):806-20. PMC: 4539576. DOI: 10.1158/2159-8290.CD-15-0439. View

20.

Rizvi N, Hellmann M, Snyder A, Kvistborg P, Makarov V, Havel J . Cancer immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science. 2015; 348(6230):124-8. PMC: 4993154. DOI: 10.1126/science.aaa1348. View