Rotavirus rewires host cell metabolic pathways toward glutamine catabolism for effective virus infection

Gut Microbes. 2024 Jan-Dec;16(1):2428425. doi: 10.1080/19490976.2024.2428425. Epub 2024 Nov 20.

Abstract

Rotavirus (RV) accounts for 19.11% of global diarrheal deaths. Though GAVI assisted vaccine introduction has curtailed RV induced mortality, factors like RV strain diversity, differential infantile gut microbiome, malnutrition, interference from maternal antibodies and other administered vaccines, etc. often compromise vaccine efficacy. Herein emerges the need of antivirals which can be administered adjunct to vaccination to curb the socio-economic burden stemming from frequent RV infection. Cognisance of pathogen-perturbed host cellular physiology has revolutionized translational research and aided precision-based therapy, particularly for viruses, with no metabolic machinery of their own. To date there has been limited exploration of the host cellular metabolome in context of RV infection. In this study, we explored the endometabolomic landscape of human intestinal epithelial cells (HT-29) on RV-SA11 infection. Significant alteration of host cellular metabolic pathways like the nucleotide biosynthesis pathway, alanine, aspartate and glutamate metabolism pathway, the host citric acid cycle was observed in RV-SA11 infection scenario. Detailed study further revealed that RV replication is exclusively dependent on glutamine metabolism for their propagation in host cells. Glutamine metabolism generates glutamate, aspartate, and asparagine which facilitates virus infection. Abrogation of aspartate biogenesis from glutamine by use of Aminooxyacetic acid (AOAA), significantly curbed RV-SA11 infection in-vitro and in-vivo. Overall, the study improves our understanding of host-rotavirus interactome and recognizes host glutamine metabolism pathway as a suitable target for effective therapeutic intervention against RV infection.

Keywords: Rotavirus; antiviral; aspartate aminotransferase; glutamine metabolism; metabolomics.

MeSH terms

  • Animals
  • Epithelial Cells / metabolism
  • Epithelial Cells / virology
  • Gastrointestinal Microbiome
  • Glutamine* / metabolism
  • HT29 Cells
  • Host-Pathogen Interactions
  • Humans
  • Metabolic Networks and Pathways*
  • Mice
  • Rotavirus Infections* / metabolism
  • Rotavirus Infections* / virology
  • Rotavirus* / metabolism
  • Virus Replication*

Substances

  • Glutamine

Grants and funding

Authors would like to thank the Human Resources Department, Department of Health Research for providing grant and fellowship for this study to Ms. Suvrotoa Mitra under the ICMR-DHR Young Scientist Scheme (No. R.12014/14/2021-HR) and the Japan Initiative for Global Research Network on Infectious Diseases (J-GRID) from the Ministry of Education, Culture, Sports, Science and Technology in Japan (MEXT) and Japan Agency for Medical Research and Development (AMED) (grant no.: JP24wm0125004).