Single-Cell Transcriptome Analysis Uncovers Intratumoral Heterogeneity and Underlying Mechanisms for Drug Resistance in Hepatobiliary Tumor Organoids

Adv Sci (Weinh). 2021 Jun;8(11):e2003897. doi: 10.1002/advs.202003897. Epub 2021 Mar 23.

Abstract

Molecular heterogeneity of hepatobiliary tumor including intertumoral and intratumoral disparity always leads to drug resistance. Here, seven hepatobiliary tumor organoids are generated to explore heterogeneity and evolution via single-cell RNA sequencing. HCC272 with high status of epithelia-mesenchymal transition proves broad-spectrum drug resistance. By examining the expression pattern of cancer stem cells markers (e.g., PROM1, CD44, and EPCAM), it is found that CD44 positive population may render drug resistance in HCC272. UMAP and pseudo-time analysis identify the intratumoral heterogeneity and distinct evolutionary trajectories, of which catenin beta-1 (CTNNB1), glyceraldehyde-3-phosphate dehydrogenase (GAPDH), and nuclear paraspeckle assembly transcript 1 (NEAT1) advantage expression clusters are commonly shared across hepatobiliary organoids. CellphoneDB analysis further implies that metabolism advantage organoids with enrichment of hypoxia signal upregulate NEAT1 expression in CD44 subgroup and mediate drug resistance that relies on Jak-STAT pathway. Moreover, metabolism advantage clusters shared in several organoids have similar characteristic genes (GAPDH, NDRG1 (N-Myc downstream regulated 1), ALDOA, and CA9). The combination of GAPDH and NDRG1 is an independent risk factor and predictor for patient survival. This study delineates heterogeneity of hepatobiliary tumor organoids and proposes that the collaboration of intratumoral heterogenic subpopulations renders malignant phenotypes and drug resistance.

Keywords: drug resistance; hepatobiliary tumor organoid; single-cell analysis; tumor ecosystem; tumor heterogeneity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antigens, Neoplasm / genetics
  • Carbonic Anhydrase IX / genetics
  • Cell Cycle Proteins / genetics
  • Digestive System Diseases / drug therapy
  • Digestive System Diseases / genetics*
  • Digestive System Diseases / pathology
  • Drug Resistance, Neoplasm / genetics
  • Epithelial-Mesenchymal Transition / genetics
  • Fructose-Bisphosphate Aldolase / genetics
  • Gastrointestinal Neoplasms / drug therapy
  • Gastrointestinal Neoplasms / genetics*
  • Gastrointestinal Neoplasms / pathology
  • Gene Expression Regulation, Neoplastic / genetics
  • Glyceraldehyde-3-Phosphate Dehydrogenase (Phosphorylating) / genetics*
  • Humans
  • Hyaluronan Receptors / genetics
  • Intracellular Signaling Peptides and Proteins / genetics
  • Janus Kinases / genetics
  • Neoplastic Stem Cells / metabolism
  • Neoplastic Stem Cells / pathology
  • Organoids / drug effects
  • Organoids / metabolism
  • Organoids / pathology
  • RNA, Long Noncoding / genetics*
  • RNA-Seq
  • STAT Transcription Factors / genetics
  • Single-Cell Analysis
  • Transcriptome / genetics
  • beta Catenin / genetics*

Substances

  • Antigens, Neoplasm
  • CTNNB1 protein, human
  • Cell Cycle Proteins
  • Hyaluronan Receptors
  • Intracellular Signaling Peptides and Proteins
  • N-myc downstream-regulated gene 1 protein
  • NEAT1 long non-coding RNA, human
  • RNA, Long Noncoding
  • STAT Transcription Factors
  • beta Catenin
  • GAPDH protein, human
  • Glyceraldehyde-3-Phosphate Dehydrogenase (Phosphorylating)
  • Janus Kinases
  • ALDOA protein, human
  • Fructose-Bisphosphate Aldolase
  • CA9 protein, human
  • Carbonic Anhydrase IX