The mitochondrial SDHD gene is required for early embryogenesis, and its partial deficiency results in persistent carotid body glomus cell activation with full responsiveness to hypoxia

Mol Cell Biol. 2004 Dec;24(24):10933-40. doi: 10.1128/MCB.24.24.10933-10940.2004.

Abstract

The SDHD gene encodes one of the two membrane-anchoring proteins of the succinate dehydrogenase (complex II) of the mitochondrial electron transport chain. This gene has recently been proposed to be involved in oxygen sensing because mutations that cause loss of its function produce hereditary familiar paraganglioma, a tumor of the carotid body (CB), the main arterial chemoreceptor that senses oxygen levels in the blood. Here, we report the generation of a SDHD knockout mouse, which to our knowledge is the first mammalian model lacking a protein of the electron transport chain. Homozygous SDHD(-/-) animals die at early embryonic stages. Heterozygous SDHD(+/-) mice show a general, noncompensated deficiency of succinate dehydrogenase activity without alterations in body weight or major physiological dysfunction. The responsiveness to hypoxia of CBs from SDHD(+/-) mice remains intact, although the loss of an SDHD allele results in abnormal enhancement of resting CB activity due to a decrease of K(+) conductance and persistent Ca(2+) influx into glomus cells. This CB overactivity is linked to a subtle glomus cell hypertrophy and hyperplasia. These observations indicate that constitutive activation of SDHD(+/-) glomus cells precedes CB tumor transformation. They also suggest that, contrary to previous beliefs, mitochondrial complex II is not directly involved in CB oxygen sensing.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alleles
  • Animals
  • Calcium / metabolism
  • Carotid Body / metabolism
  • Carotid Body Tumor / genetics*
  • Carotid Body Tumor / metabolism
  • Cell Hypoxia / physiology*
  • DNA Mutational Analysis
  • Electron Transport Complex II / chemistry
  • Electron Transport Complex II / genetics*
  • Electron Transport Complex II / metabolism
  • Embryonic Development*
  • Gene Targeting
  • Heterozygote
  • Immunohistochemistry
  • Membrane Proteins / chemistry
  • Membrane Proteins / genetics*
  • Membrane Proteins / metabolism
  • Mice
  • Mice, Knockout
  • Mitochondria / metabolism
  • Mutation
  • Paraganglioma / genetics*
  • Patch-Clamp Techniques
  • Potassium / metabolism
  • RNA, Messenger / metabolism
  • Recombination, Genetic
  • Succinate Dehydrogenase / chemistry
  • Succinate Dehydrogenase / genetics*
  • Succinate Dehydrogenase / metabolism

Substances

  • Membrane Proteins
  • RNA, Messenger
  • Electron Transport Complex II
  • SDHD protein, mouse
  • Succinate Dehydrogenase
  • Potassium
  • Calcium