A Metabolic Checkpoint for the Yeast-to-Hyphae Developmental Switch Regulated by Endogenous Nitric Oxide Signaling

Cell Rep. 2018 Nov 20;25(8):2244-2258.e7. doi: 10.1016/j.celrep.2018.10.080.

Abstract

The yeast Candida albicans colonizes several sites in the human body and responds to metabolic signals in commensal and pathogenic states. The yeast-to-hyphae transition correlates with virulence, but how metabolic status is integrated with this transition is incompletely understood. We used the putative mitochondrial fission inhibitor mdivi-1 to probe the crosstalk between hyphal signaling and metabolism. Mdivi-1 repressed C. albicans hyphal morphogenesis, but the mechanism was independent of its presumed target, the mitochondrial fission GTPase Dnm1. Instead, mdivi-1 triggered extensive metabolic reprogramming, consistent with metabolic stress, and reduced endogenous nitric oxide (NO) levels. Limiting endogenous NO stabilized the transcriptional repressor Nrg1 and inhibited the yeast-to-hyphae transition. We establish a role for endogenous NO signaling in C. albicans hyphal morphogenesis and suggest that NO regulates a metabolic checkpoint for hyphal growth. Furthermore, identifying NO signaling as an mdivi-1 target could inform its therapeutic applications in human diseases.

Keywords: Candida albicans; fungal pathogenesis; hyphae; mdivi-1; metabolism; mitochondria; morphogenesis; mycology; nitric oxide.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Caenorhabditis elegans
  • Candida albicans / drug effects
  • Candida albicans / genetics
  • Candida albicans / growth & development*
  • Candida albicans / metabolism*
  • Cyclic AMP-Dependent Protein Kinases / metabolism
  • Electron Transport Complex I / metabolism
  • Fungal Proteins / metabolism
  • Gene Expression Regulation, Fungal / drug effects
  • Hyphae / drug effects
  • Hyphae / growth & development*
  • Hyphae / metabolism*
  • Macrophages / drug effects
  • Macrophages / microbiology
  • Mice, Inbred C57BL
  • Mitochondrial Dynamics / drug effects
  • Models, Biological
  • Morphogenesis / drug effects
  • Nitric Oxide / metabolism*
  • Quinazolinones / pharmacology
  • Repressor Proteins / metabolism
  • Saccharomyces cerevisiae / drug effects
  • Saccharomyces cerevisiae / metabolism
  • Signal Transduction*
  • ras Proteins / metabolism

Substances

  • 3-(2,4-dichloro-5-methoxyphenyl)-2-sulfanyl-4(3H)-quinazolinone
  • Fungal Proteins
  • Quinazolinones
  • Repressor Proteins
  • Nitric Oxide
  • Cyclic AMP-Dependent Protein Kinases
  • ras Proteins
  • Electron Transport Complex I