Genome Engineering of Primary and Pluripotent Stem Cell-Derived Hepatocytes for Modeling Liver Tumor Formation

Authors:
Lulu Zhang , Xunting Wang , Xuelian Yang , Yijia Chi , Yihang Chu , Yi Zhang , Yufan Gong , Fei Wang , Qian Zhao , Dongxin Zhao 
In:
Source: Open Biology
Publication Date: (2024)
Issue: 13: 9
Research Area:
Gastroenterology
Stem Cells
Toxicology
Drug Discovery
Cells used in publication:
Hepatocyte, mouse
Species: mouse
Tissue Origin: liver
Culture Media:
Platform:
4D-Nucleofector® X-Unit
Experiment

2.2. Primary Mouse Hepatocytes Isolation

The primary hepatocyte maintenance media were as follows: Williams’ Medium E with supplements (WEM), Williams’ medium E containing 1× B27, 1× Glutamax, and 1× penicillin-streptomycin; 5C condition (5C): WEM supplemented with Forskolin (20 µM), SB431542 (10 µM), IWP2 (0.5 µM), DAPT (5 µM), and LDN193189 (0.1 µM); Hepatocyte Culture Medium (HCM): manufactured by Lonza (CC3198); Proliferation human hepatocytes condition (ProliHH): Advanced DMEM/F12 supplemented with 1 mM N-acetylcysteine, 1× B27 (minus vitamin A), 1× N2 supplement, 10 nM gastrin I, 25 µg/mL recombinant Human Wnt-3a Protein, 50 ng/mL EGF, 2 ng/mL FGF10, 25 ng/mL recombinant human HGF, 25 ng/mL human recombinant bFGF, 5 µM A83-01, 10 µM Y-27632, 1% penicillin-streptomycin, and 1% fetal bovine serum.


2.6. Electroporation

Electroporation was performed using a P3 Primary Cell 4D-Nucleofector™ X Kit (Lonza, Basel, Switzerland). According to the manufacturer’s instructions, 600,000 freshly isolated mouse hepatocytes were resuspended in 100 µL of Lonza electroporation buffer P3 (82 µL Nucleofector Solution and 18 µL Supplement) containing 5 µg of DNA. The cell suspension was then transferred into NucelocuvetteTM vessels and electroporated using a Lonza 4D-NucleofectorTM core unit with the DS-150 program. After electroporation, the cells were resuspended in plating medium and seeded onto collagen I-coated plates for at least 3 h. The plating medium was then replaced with pre-warmed HCM. After 72 h, images were captured using an Olympus IX73 fluorescence microscope and the transfection efficiency was quantified using Image J software (version 1.53e).
Abstract

Genome editing has demonstrated its utility in generating isogenic cell-based disease models, enabling the precise introduction of genetic alterations into wild-type cells to mimic disease phenotypes and explore underlying mechanisms. However, its application in liver-related diseases has been limited by challenges in genetic modification of mature hepatocytes in a dish. Here, we conducted a systematic comparison of various methods for primary hepatocyte culture and gene delivery to achieve robust genome editing of hepatocytes ex vivo. Our efforts yielded editing efficiencies of up to 80% in primary murine hepatocytes cultured in monolayer and 20% in organoids. To model human hepatic tumorigenesis, we utilized hepatocytes differentiated from human pluripotent stem cells (hPSCs) as an alternative human hepatocyte source. We developed a series of cellular models by introducing various single or combined oncogenic alterations into hPSC-derived hepatocytes. Our findings demonstrated that distinct mutational patterns led to phenotypic variances, affecting both overgrowth and transcriptional profiles. Notably, we discovered that the PI3KCA E542K mutant, whether alone or in combination with exogenous c-MYC, significantly impaired hepatocyte functions and facilitated cancer metabolic reprogramming, highlighting the critical roles of these frequently mutated genes in driving liver neoplasia. In conclusion, our study demonstrates genome-engineered hepatocytes as valuable cellular models of hepatocarcinoma, providing insights into early tumorigenesis mechanisms.