Herpes Simplex Virus 1 Infection of Human Brain Organoids and Pancreatic Stem Cell-Islets Drives Organoid-Specific Transcripts Associated with Alzheimer's Disease and Autoimmune Diseases

Cells. 2024 Nov 29;13(23):1978. doi: 10.3390/cells13231978.

Abstract

Viral infections leading to inflammation have been implicated in several common diseases, such as Alzheimer's disease (AD) and type 1 diabetes (T1D). Of note, herpes simplex virus 1 (HSV-1) has been reported to be associated with AD. We sought to identify the transcriptomic changes due to HSV-1 infection and anti-viral drug (acyclovir, ACV) treatment of HSV-1 infection in dissociated cells from human cerebral organoids (dcOrgs) versus stem cell-derived pancreatic islets (sc-islets) to gain potential biological insights into the relevance of HSV-1-induced inflammation in AD and T1D. We observed that differentially expressed genes (DEGs) in HSV-1-infected sc-islets were enriched for genes associated with several autoimmune diseases, most significantly, T1D, but also rheumatoid arthritis, psoriasis, Crohn's disease, and multiple sclerosis, whereas DEGs in HSV-1-infected dcOrgs were exclusively enriched for genes associated with AD. The ACV treatment of sc-islets was not as effective in rescuing transcript perturbations of autoimmune disease-associated genes. Finally, we identified gene ontology categories that were enriched for DEGs that were in common across, or unique to, viral treatment of dcOrgs and sc-islets, such as categories involved in the transferase complex, mitochondrial, and autophagy function. In addition, we compared transcriptomic signatures from HSV-1-infected sc-islets with sc-islets that were infected with the coxsackie B virus (CVB) that had been associated with T1D pathogenesis. Collectively, this study provides tissue-specific insights into the molecular effects of inflammation in AD and T1D.

Keywords: Alzheimer’s disease; acyclovir; autoimmune diseases; cerebral organoids; herpes simplex virus 1; innate immune; neurodegenerative diseases; stem cell islets; type 1 diabetes.

MeSH terms

  • Alzheimer Disease* / genetics
  • Alzheimer Disease* / pathology
  • Alzheimer Disease* / virology
  • Autoimmune Diseases / genetics
  • Autoimmune Diseases / virology
  • Brain* / metabolism
  • Brain* / pathology
  • Brain* / virology
  • Diabetes Mellitus, Type 1 / genetics
  • Diabetes Mellitus, Type 1 / pathology
  • Diabetes Mellitus, Type 1 / virology
  • Herpes Simplex / genetics
  • Herpes Simplex / virology
  • Herpesvirus 1, Human* / genetics
  • Herpesvirus 1, Human* / physiology
  • Humans
  • Islets of Langerhans / metabolism
  • Islets of Langerhans / pathology
  • Islets of Langerhans / virology
  • Organoids* / metabolism
  • Organoids* / virology
  • Stem Cells / metabolism
  • Stem Cells / virology
  • Transcriptome / genetics