Depiction of tumor stemlike features and underlying relationships with hazard immune infiltrations based on large prostate cancer cohorts

Prostate cancer stemness (PCS) cells have been reported to drive tumor progression, recurrence and drug resistance. However, there is lacking systematical assessment of stemlike indices and associations with immunological properties in prostate adenocarcinoma (PRAD). We thus collected 7 PRAD cohorts with 1465 men and calculated the stemlike indices for each sample using one-class logistic regression machine learning algorithm. We selected the mRNAsi to quantify the stemlike indices that correlated significantly with prognosis and accordingly identified 21 PCS-related CpG loci and 13 pivotal signature. The 13-gene based PCS model possessed high predictive significance for progression-free survival (PFS) that was trained and validated in 7 independent cohorts. Meanwhile, we conducted consensus clustering and classified the total cohorts into 5 PCS clusters with distinct outcomes. Samples in PCScluster5 possessed the highest stemness fractions and suffered from the worst prognosis. Additionally, we implemented the CIBERSORT algorithm to infer the differential abundance across 5 PCS clusters. The activated immune cells (CD8+ T cell and dendritic cells) infiltrated significantly less in PCScluster5 than other clusters, supporting the negative regulations between stemlike indices and anticancer immunity. High mRNAsi was also found to be associated with up-regulation of immunosuppressive checkpoints, like PDL1. Lastly, we used the Connectivity Map (CMap) resource to screen potential compounds for targeting PRAD stemness, including the top hits of cell cycle inhibitor and FOXM1 inhibitor. Taken together, our study comprehensively evaluated the PRAD stemlike indices based on large cohorts and established a 13-gene based classifier for predicting prognosis or potential strategies for stemness treatment.

[1]  Allen W. Zhang,et al.  Cancer stemness, intratumoral heterogeneity, and immune response across cancers , 2019, Proceedings of the National Academy of Sciences.

[2]  W. Mao,et al.  Integrative analysis of gene expression and DNA methylation through one‐class logistic regression machine learning identifies stemness features in medulloblastoma , 2019, Molecular oncology.

[3]  F. Montorsi,et al.  The Microbiome of the Prostate Tumor Microenvironment. , 2017, European Urology.

[4]  Günter P. Wagner,et al.  Measurement of mRNA abundance using RNA-seq data: RPKM measure is inconsistent among samples , 2012, Theory in Biosciences.

[5]  Genevieve L. Stein-O’Brien,et al.  Aging-like Spontaneous Epigenetic Silencing Facilitates Wnt Activation, Stemness, and BrafV600E-Induced Tumorigenesis. , 2019, Cancer cell.

[6]  Mariano J. Alvarez,et al.  Cross-species regulatory network analysis identifies a synergistic interaction between FOXM1 and CENPF that drives prostate cancer malignancy. , 2014, Cancer cell.

[7]  Pan Du,et al.  lumi: a pipeline for processing Illumina microarray , 2008, Bioinform..

[8]  Steven J. M. Jones,et al.  Pan-cancer analysis of whole genomes , 2020, Nature.

[9]  S. Tomlins,et al.  Translational and clinical implications of the genetic landscape of prostate cancer , 2016, Nature Reviews Clinical Oncology.

[10]  Angela N. Brooks,et al.  A Next Generation Connectivity Map: L1000 Platform and the First 1,000,000 Profiles , 2017, Cell.

[11]  Daniela Matei,et al.  Targeting Cancer Stemness in the Clinic: From Hype to Hope. , 2019, Cell stem cell.

[12]  The Icgctcga Pan-Cancer Analysis of Whole Genomes Consortium Pan-cancer analysis of whole genomes , 2020 .

[13]  Benjamin M. Bolstad,et al.  affy - analysis of Affymetrix GeneChip data at the probe level , 2004, Bioinform..

[14]  W. Nelson,et al.  The inflammatory microenvironment and microbiome in prostate cancer development , 2018, Nature Reviews Urology.

[15]  M. Gleave,et al.  siRNA Lipid Nanoparticle Potently Silences Clusterin and Delays Progression When Combined with Androgen Receptor Cotargeting in Enzalutamide-Resistant Prostate Cancer , 2015, Clinical Cancer Research.

[16]  Artem Sokolov,et al.  One-Class Detection of Cell States in Tumor Subtypes , 2016, PSB.

[17]  Paul A Clemons,et al.  The Connectivity Map: Using Gene-Expression Signatures to Connect Small Molecules, Genes, and Disease , 2006, Science.

[18]  Hua Yu,et al.  Erratum: JAK/STAT3-Regulated Fatty Acid β-Oxidation Is Critical for Breast Cancer Stem Cell Self-Renewal and Chemoresistance (Cell Metabolism (2018) 27(1) (136–150.e5)(S1550413117306691)(10.1016/j.cmet.2017.11.001)) , 2018 .

[19]  F. Saad,et al.  Metastatic Prostate Cancer and the Bone: Significance and Therapeutic Options. , 2015, European urology.

[20]  A. Jemal,et al.  Colorectal cancer statistics, 2020 , 2020, CA: a cancer journal for clinicians.

[21]  M. Cooperberg,et al.  The Immune Landscape of Prostate Cancer and Nomination of PD-L2 as a Potential Therapeutic Target , 2018, Journal of the National Cancer Institute.

[22]  Zhan Ye,et al.  Misuse of RPKM or TPM normalization when comparing across samples and sequencing protocols , 2020, RNA.

[23]  D. Cheresh,et al.  Integrins and cancer: regulators of cancer stemness, metastasis, and drug resistance. , 2015, Trends in cell biology.

[24]  Gary D Bader,et al.  Erratum: The Mitochondrial Transacylase, Tafazzin, Regulates AML Stemness by Modulating Intracellular Levels of Phospholipids (Cell Stem Cell (2019) 24(4) (621–636.e16), (S1934590919300724), (10.1016/j.stem.2019.02.020)) , 2019 .

[25]  Broad Genomics Platform,et al.  Exome sequencing of 20,791 cases of type 2 diabetes and 24,440 controls , 2019 .

[26]  Erik N. Bergstrom,et al.  The repertoire of mutational signatures in human cancer , 2018, bioRxiv.

[27]  Jan Paul Medema,et al.  Intra-tumor heterogeneity from a cancer stem cell perspective , 2017, Molecular Cancer.

[28]  Mark S. Litwin,et al.  The Diagnosis and Treatment of Prostate Cancer: A Review , 2017, JAMA.

[29]  M. Rubin,et al.  SOX2 promotes lineage plasticity and antiandrogen resistance in TP53- and RB1-deficient prostate cancer , 2017, Science.

[30]  Sendurai A Mani,et al.  EMT, stemness and tumor plasticity in aggressive variant neuroendocrine prostate cancers. , 2018, Biochimica et biophysica acta. Reviews on cancer.

[31]  L. Holmberg,et al.  Radical Prostatectomy or Watchful Waiting in Prostate Cancer — 29‐Year Follow‐up , 2018, The New England journal of medicine.

[32]  J. Inal,et al.  A novel role for peptidylarginine deiminases in microvesicle release reveals therapeutic potential of PAD inhibition in sensitizing prostate cancer cells to chemotherapy , 2015, Journal of extracellular vesicles.

[33]  Joshua M. Stuart,et al.  A basal stem cell signature identifies aggressive prostate cancer phenotypes , 2015, Proceedings of the National Academy of Sciences.

[34]  Q. Hu,et al.  MUC1-C regulates lineage plasticity driving progression to neuroendocrine prostate cancer , 2020, Nature Communications.

[35]  Ash A. Alizadeh,et al.  Abstract PR09: The prognostic landscape of genes and infiltrating immune cells across human cancers , 2015 .

[36]  Joshua M. Stuart,et al.  Machine Learning Identifies Stemness Features Associated with Oncogenic Dedifferentiation. , 2018, Cell.

[37]  H. Scher,et al.  The Polycomb Repressor Complex 1 Drives Double-Negative Prostate Cancer Metastasis by Coordinating Stemness and Immune Suppression. , 2019, Cancer cell.

[38]  Y. Liao,et al.  Tumor Microenvironment Characterization in Gastric Cancer Identifies Prognostic and Immunotherapeutically Relevant Gene Signatures , 2019, Cancer Immunology Research.

[39]  I. Melero,et al.  Combined immunotherapy encompassing intratumoral poly-ICLC, dendritic-cell vaccination and radiotherapy in advanced cancer patients , 2017, Annals of oncology : official journal of the European Society for Medical Oncology.

[40]  Jia-geng Zhu,et al.  FOXM1 contributes to docetaxel resistance in castration-resistant prostate cancer by inducing AMPK/mTOR-mediated autophagy. , 2019, Cancer letters.

[41]  Ash A. Alizadeh,et al.  Robust enumeration of cell subsets from tissue expression profiles , 2015, Nature Methods.