Mapping cell types in the tumor microenvironment from tissue images via deep learning trained by spatial transcriptomics of lung adenocarcinoma

Profiling heterogeneous cell types in the tumor microenvironment (TME) is important for cancer immunotherapy. Here, we propose a method and validate in independent samples for mapping cell types in the TME from only hematoxylin and eosin (H&E)-stained tumor tissue images using spatial transcriptomic data of lung adenocarcinoma. We obtained spatial transcriptomic data of lung adenocarcinoma from 22 samples. The cell types of each spot were estimated using cell type inference based on a domain adaptation algorithm with single-cell RNA-sequencing data. They were used to train a convolutional neural network with a corresponding H&E image patch as an input. Consequently, the five predicted cell types estimated from the H&E images were significantly correlated with those derived from the RNA-sequencing data. We validated our model using immunohistochemical staining results with marker proteins from independent lung adenocarcinoma samples. Our resource of spatial transcriptomics of lung adenocarcinoma and proposed method with independent validation can provide an annotation-free and precise profiling method of tumor microenvironment using H&E images.

[1]  P. Laurent-Puig,et al.  Tertiary lymphoid structures generate and propagate anti-tumor antibody-producing plasma cells in renal cell cancer. , 2022, Immunity.

[2]  M. Mino‐Kenudson,et al.  Three subtypes of lung cancer fibroblasts define distinct therapeutic paradigms. , 2021, Cancer cell.

[3]  D. Lin,et al.  Artificial intelligence-assisted system for precision diagnosis of PD-L1 expression in non-small cell lung cancer , 2021, Modern Pathology.

[4]  Gustavo S. França,et al.  Exploring tissue architecture using spatial transcriptomics , 2021, Nature.

[5]  Jun Liu,et al.  Tertiary Lymphoid Structures in Cancer: The Double-Edged Sword Role in Antitumor Immunity and Potential Therapeutic Induction Strategies , 2021, Frontiers in Immunology.

[6]  Z. Shao,et al.  Spatial architecture of the immune microenvironment orchestrates tumor immunity and therapeutic response , 2021, Journal of Hematology & Oncology.

[7]  N. Almog,et al.  Conserved pan-cancer microenvironment subtypes predict response to immunotherapy. , 2021, Cancer cell.

[8]  D. S. Lee,et al.  CellDART: cell type inference by domain adaptation of single-cell and spatial transcriptomic data , 2021, bioRxiv.

[9]  T. Mak,et al.  Beyond immune checkpoint blockade: emerging immunological strategies , 2021, Nature Reviews Drug Discovery.

[10]  Juan Fang,et al.  Prognostic value of tertiary lymphoid structure and tumour infiltrating lymphocytes in oral squamous cell carcinoma , 2020, International journal of oral science.

[11]  J. Galon,et al.  The immune contexture and Immunoscore in cancer prognosis and therapeutic efficacy , 2020, Nature Reviews Cancer.

[12]  G. Barceló-Coblijn,et al.  Immune Landscape in Tumor Microenvironment: Implications for Biomarker Development and Immunotherapy , 2020, International journal of molecular sciences.

[13]  J. Lundeberg,et al.  Seamless integration of image and molecular analysis for spatial transcriptomics workflows , 2020, BMC Genomics.

[14]  D. Lee,et al.  Discovery of molecular features underlying the morphological landscape by integrating spatial transcriptomic data with deep features of tissue images , 2020, bioRxiv.

[15]  T. Mok,et al.  Deep-learning analysis of H&E images to define three immune phenotypes to reveal loss-of-target in excluded immune cells as a novel resistance mechanism of immune checkpoint inhibitor in non-small cell lung cancer. , 2020 .

[16]  Jung-Il Lee,et al.  Single-cell RNA sequencing demonstrates the molecular and cellular reprogramming of metastatic lung adenocarcinoma , 2020, Nature Communications.

[17]  C. Sautès-Fridman,et al.  The Tumor Microenvironment in the Response to Immune Checkpoint Blockade Therapies , 2020, Frontiers in Immunology.

[18]  Jeffrey E. Lee,et al.  B cells and tertiary lymphoid structures promote immunotherapy response , 2020, Nature.

[19]  Neofytos Dimitriou,et al.  Deep Learning for Whole Slide Image Analysis: An Overview , 2019, Front. Med..

[20]  M. Smyth,et al.  Myeloid immunosuppression and immune checkpoints in the tumor microenvironment , 2019, Cellular & Molecular Immunology.

[21]  A. Ribas,et al.  Tumour-intrinsic resistance to immune checkpoint blockade , 2019, Nature Reviews Immunology.

[22]  L. Shevde,et al.  The Tumor Microenvironment Innately Modulates Cancer Progression. , 2019, Cancer research.

[23]  John D. Minna,et al.  Computational staining of pathology images to study tumor microenvironment in lung cancer , 2019, bioRxiv.

[24]  P. Spellman,et al.  Human Tumor-Associated Macrophage and Monocyte Transcriptional Landscapes Reveal Cancer-Specific Reprogramming, Biomarkers, and Therapeutic Targets , 2019, Cancer cell.

[25]  Denise Lau,et al.  RNA Sequencing of the Tumor Microenvironment in Precision Cancer Immunotherapy. , 2019, Trends in cancer.

[26]  X. Liu,et al.  Signatures of T cell dysfunction and exclusion predict cancer immunotherapy response , 2018, Nature Medicine.

[27]  Rajarsi R. Gupta,et al.  Spatial Organization and Molecular Correlation of Tumor-Infiltrating Lymphocytes Using Deep Learning on Pathology Images. , 2018, Cell reports.

[28]  R. Weinberg,et al.  Understanding the tumor immune microenvironment (TIME) for effective therapy , 2018, Nature Medicine.

[29]  Fabian J Theis,et al.  SCANPY: large-scale single-cell gene expression data analysis , 2018, Genome Biology.

[30]  Adel Hafiane,et al.  Integrating segmentation with deep learning for enhanced classification of epithelial and stromal tissues in H&E images , 2017, Pattern Recognit. Lett..

[31]  F. Hodi,et al.  Monitoring immune-checkpoint blockade: response evaluation and biomarker development , 2017, Nature Reviews Clinical Oncology.

[32]  A. Butte,et al.  xCell: digitally portraying the tissue cellular heterogeneity landscape , 2017, bioRxiv.

[33]  P. Laurent-Puig,et al.  Estimating the population abundance of tissue-infiltrating immune and stromal cell populations using gene expression , 2016, Genome Biology.

[34]  R. Kalluri The biology and function of fibroblasts in cancer , 2016, Nature Reviews Cancer.

[35]  C. Rudin,et al.  Nivolumab versus Docetaxel in Advanced Nonsquamous Non-Small-Cell Lung Cancer. , 2015, The New England journal of medicine.

[36]  J. Lunceford,et al.  Pembrolizumab for the treatment of non-small-cell lung cancer. , 2015, The New England journal of medicine.

[37]  E. Mansfield,et al.  FDA Perspective on Companion Diagnostics: An Evolving Paradigm , 2014, Clinical Cancer Research.

[38]  D. Quail,et al.  Microenvironmental regulation of tumor progression and metastasis , 2014 .

[39]  Douglas Hanahan,et al.  Accessories to the Crime: Functions of Cells Recruited to the Tumor Microenvironment Prospects and Obstacles for Therapeutic Targeting of Function-enabling Stromal Cell Types , 2022 .

[40]  Brian B. Avants,et al.  Symmetric diffeomorphic image registration with cross-correlation: Evaluating automated labeling of elderly and neurodegenerative brain , 2008, Medical Image Anal..

[41]  L. Coussens,et al.  The tumor microenvironment: a critical determinant of neoplastic evolution. , 2003, European journal of cell biology.