Tailoring the CRISPR system to transactivate coagulation gene promoters in normal and mutated contexts

Biochim Biophys Acta Gene Regul Mech. 2019 Jun;1862(6):619-624. doi: 10.1016/j.bbagrm.2019.04.002. Epub 2019 Apr 18.

Abstract

Engineered transcription factors (TF) have expanded our ability to modulate gene expression and hold great promise as bio-therapeutics. The first-generation TF, based on Zinc Fingers or Transcription-Activator-like Effectors (TALE), required complex and time-consuming assembly protocols, and were indeed replaced in recent years by the CRISPR activation (CRISPRa) technology. Here, with coagulation F7/F8 gene promoters as models, we exploited a CRISPRa system based on deactivated (d)Cas9, fused with a transcriptional activator (VPR), which is driven to its target by a single guide (sg)RNA. Reporter gene assays in hepatoma cells identified a sgRNA (sgRNAF7.5) triggering a ~35-fold increase in the activity of F7 promoter, either wild-type, or defective due to the c.-61T>G mutation. The effect was higher (~15-fold) than that of an engineered TALE-TF (TF4) targeting the same promoter region. Noticeably, when challenged on the endogenous F7 gene, the dCas9-VPR/sgRNAF7.5 combination was more efficient (~6.5-fold) in promoting factor VII (FVII) protein secretion/activity than TF4 (~3.8-fold). The approach was translated to the promoter of F8, whose reduced expression causes hemophilia A. Reporter gene assays in hepatic and endothelial cells identified sgRNAs that, respectively, appreciably increased F8 promoter activity (sgRNAF8.1, ~8-fold and 3-fold; sgRNAF8.2, ~19-fold and 2-fold) with synergistic effects (~38-fold and 2.7-fold). Since modest increases in F7/F8 expression would ameliorate patients' phenotype, the CRISPRa-mediated transactivation extent might approach the low therapeutic threshold. Through this pioneer study we demonstrated that the CRISPRa system is easily tailorable to increase expression, or rescue disease-causing mutations, of different promoters, with potential intriguing implications for human disease models.

Keywords: CRISPR activation; Engineered transcription factors; Promoter mutations; TALE-TF.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Binding Sites
  • Biomarkers, Tumor / genetics
  • CRISPR-Cas Systems*
  • Carcinoma, Hepatocellular
  • Endothelial Cells
  • Factor VII
  • Factor VIII / genetics
  • Gene Expression
  • Genes, Reporter
  • Hep G2 Cells
  • Hepatocyte Nuclear Factor 4 / genetics
  • Humans
  • Mutation
  • Promoter Regions, Genetic / genetics*
  • RNA, Guide, CRISPR-Cas Systems
  • Receptors, Immunologic / genetics
  • Transcription Factors / genetics*
  • Transcriptional Activation / genetics*

Substances

  • Biomarkers, Tumor
  • Hepatocyte Nuclear Factor 4
  • RNA, Guide, CRISPR-Cas Systems
  • Receptors, Immunologic
  • Transcription Factors
  • trophoblastic beta 1-glycoprotein receptor, human
  • F8 protein, human
  • Factor VII
  • Factor VIII