Multiomics profiling of primary lung cancers and distant metastases reveals immunosuppression as a common characteristic of tumor cells with metastatic plasticity

Won Chul Lee, Alexandre Reuben, Xin Hu, Nicholas McGranahan, Runzhe Chen, Ali Jalali, Marcelo V. Negrao, Shawna M. Hubert, Chad Tang, Chia Chin Wu, Anthony San Lucas, Whijae Roh, Kenichi Suda, Jihye Kim, Aik Choon Tan, David H. Peng, Wei Lu, Ximing Tang, Chi Wan Chow, Junya FujimotoCarmen Behrens, Neda Kalhor, Kazutaka Fukumura, Marcus Coyle, Rebecca Thornton, Curtis Gumbs, Jun Li, Chang Jiun Wu, Latasha Little, Emily Roarty, Xingzhi Song, J. Jack Lee, Erik P. Sulman, Ganesh Rao, Stephen Swisher, Lixia Diao, Jing Wang, John V. Heymach, Jason T. Huse, Paul Scheet, Ignacio I. Wistuba, Don L. Gibbons, P. Andrew Futreal, Jianhua Zhang, Daniel Gomez, Jianjun Zhang

Research output: Contribution to journalArticlepeer-review

32 Scopus citations

Abstract

Background: Metastasis is the primary cause of cancer mortality accounting for 90% of cancer deaths. Our understanding of the molecular mechanisms driving metastasis is rudimentary. Results: We perform whole exome sequencing (WES), RNA sequencing, methylation microarray, and immunohistochemistry (IHC) on 8 pairs of non-small cell lung cancer (NSCLC) primary tumors and matched distant metastases. Furthermore, we analyze published WES data from 35 primary NSCLC and metastasis pairs, and transcriptomic data from 4 autopsy cases with metastatic NSCLC and one metastatic lung cancer mouse model. The majority of somatic mutations are shared between primary tumors and paired distant metastases although mutational signatures suggest different mutagenesis processes in play before and after metastatic spread. Subclonal analysis reveals evidence of monoclonal seeding in 41 of 42 patients. Pathway analysis of transcriptomic data reveals that downregulated pathways in metastases are mainly immune-related. Further deconvolution analysis reveals significantly lower infiltration of various immune cell types in metastases with the exception of CD4+ T cells and M2 macrophages. These results are in line with lower densities of immune cells and higher CD4/CD8 ratios in metastases shown by IHC. Analysis of transcriptomic data from autopsy cases and animal models confirms that immunosuppression is also present in extracranial metastases. Significantly higher somatic copy number aberration and allelic imbalance burdens are identified in metastases. Conclusions: Metastasis is a molecularly late event, and immunosuppression driven by different molecular events, including somatic copy number aberration, may be a common characteristic of tumors with metastatic plasticity.

Original languageEnglish (US)
Article number271
JournalGenome biology
Volume21
Issue number1
DOIs
StatePublished - Dec 1 2020

Keywords

  • DNA methylation
  • Gene expression
  • Genomics
  • Immune profiling
  • Lung cancer
  • Metastasis
  • Multiomics

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Genetics
  • Cell Biology

MD Anderson CCSG core facilities

  • Tissue Biospecimen and Pathology Resource
  • Biostatistics Resource Group
  • Bioinformatics Shared Resource

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