Angiogenin loss-of-function mutations in amyotrophic lateral sclerosis

Ann Neurol. 2007 Dec;62(6):609-17. doi: 10.1002/ana.21221.

Abstract

Objective: Heterozygous missense mutations in the coding region of angiogenin (ANG), an angiogenic ribonuclease, have been reported in amyotrophic lateral sclerosis (ALS) patients. However, the role of ANG in motor neuron physiology and the functional consequences of these mutations are unknown. We searched for new mutations and sought to define the functional consequences of these mutations.

Methods: We sequenced the coding region of ANG in an independent cohort of North American ALS patients. Identified ANG mutations were then characterized using functional assays of angiogenesis, ribonucleolysis, and nuclear translocation. We also examined expression of ANG in normal human fetal and adult spinal cords.

Results: We identified four mutations in the coding region of ANG from 298 ALS patients. Three of these mutations are present in the mature protein. Among the four mutations, P(-4)S, S28N, and P112L are novel, and K17I has been reported previously. Functional assays show that these ANG mutations result in complete loss of function. The mutant ANG proteins are unable to induce angiogenesis because of a deficiency in ribonuclease activity, nuclear translocation, or both. As a correlate, we demonstrate strong ANG expression in both endothelial cells and motor neurons of normal human spinal cords from the developing fetus and adult.

Interpretation: We provide the first evidence that ANG mutations, identified in ALS patients, are associated with functional loss of ANG activity. Moreover, strong ANG expression, in normal human fetal and adult spinal cord neurons and endothelial cells, confirms the plausibility of ANG dysfunction being relevant to the pathogenesis of ALS.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Active Transport, Cell Nucleus
  • Adult
  • Aged, 80 and over
  • Amyotrophic Lateral Sclerosis / genetics
  • Amyotrophic Lateral Sclerosis / metabolism
  • Amyotrophic Lateral Sclerosis / physiopathology*
  • Cell Nucleus / metabolism
  • Cohort Studies
  • Endothelial Cells / metabolism
  • Female
  • Fetus / metabolism
  • Heterozygote
  • Humans
  • Male
  • Middle Aged
  • Motor Neurons / metabolism
  • Mutation*
  • Mutation, Missense
  • Neovascularization, Physiologic
  • Ribonuclease, Pancreatic / deficiency
  • Ribonuclease, Pancreatic / genetics*
  • Ribonuclease, Pancreatic / metabolism
  • Ribonucleases / deficiency
  • Spinal Cord / embryology
  • Spinal Cord / growth & development
  • Spinal Cord / metabolism

Substances

  • Ribonucleases
  • angiogenin
  • Ribonuclease, Pancreatic