Aldehyde dehydrogenase 3A1 activation prevents radiation-induced xerostomia by protecting salivary stem cells from toxic aldehydes

Proc Natl Acad Sci U S A. 2018 Jun 12;115(24):6279-6284. doi: 10.1073/pnas.1802184115. Epub 2018 May 24.

Abstract

Xerostomia (dry mouth) is the most common side effect of radiation therapy in patients with head and neck cancer and causes difficulty speaking and swallowing. Since aldehyde dehydrogenase 3A1 (ALDH3A1) is highly expressed in mouse salivary stem/progenitor cells (SSPCs), we sought to determine the role of ALDH3A1 in SSPCs using genetic loss-of-function and pharmacologic gain-of-function studies. Using DarkZone dye to measure intracellular aldehydes, we observed higher aldehyde accumulation in irradiated Aldh3a1-/- adult murine salisphere cells and in situ in whole murine embryonic salivary glands enriched in SSPCs compared with wild-type glands. To identify a safe ALDH3A1 activator for potential clinical testing, we screened a traditional Chinese medicine library and isolated d-limonene, commonly used as a food-flavoring agent, as a single constituent activator. ALDH3A1 activation by d-limonene significantly reduced aldehyde accumulation in SSPCs and whole embryonic glands, increased sphere-forming ability, decreased apoptosis, and improved submandibular gland structure and function in vivo after radiation. A phase 0 study in patients with salivary gland tumors showed effective delivery of d-limonene into human salivary glands following daily oral dosing. Given its safety and bioavailability, d-limonene may be a good clinical candidate for mitigating xerostomia in patients with head and neck cancer receiving radiation therapy.

Keywords: ALDH3A1; aldehyde dehydrogenase; dry mouth; radiation; xerostomia.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Aldehyde Dehydrogenase / metabolism*
  • Aldehydes / metabolism*
  • Animals
  • Apoptosis / drug effects
  • Cyclohexenes / pharmacology*
  • Female
  • Head and Neck Neoplasms / metabolism
  • Head and Neck Neoplasms / radiotherapy
  • Limonene
  • Medicine, Chinese Traditional / methods
  • Mice
  • Mice, Inbred C57BL
  • Protective Agents / pharmacology
  • Radiotherapy / adverse effects*
  • Salivary Glands / drug effects
  • Salivary Glands / metabolism*
  • Salivary Glands / radiation effects
  • Stem Cells / drug effects
  • Stem Cells / metabolism
  • Submandibular Gland / drug effects
  • Submandibular Gland / metabolism
  • Terpenes / pharmacology*
  • Xerostomia / drug therapy
  • Xerostomia / metabolism*

Substances

  • Aldehydes
  • Cyclohexenes
  • Protective Agents
  • Terpenes
  • Limonene
  • Aldehyde Dehydrogenase
  • Aldh3a1protein, mouse