Nerve growth factor R221W responsible for insensitivity to pain is defectively processed and accumulates as proNGF

Neurobiol Dis. 2009 Feb;33(2):221-8. doi: 10.1016/j.nbd.2008.10.012. Epub 2008 Nov 8.

Abstract

We have previously identified a homozygous missense (R221W) mutation in the NGFB gene in patients with loss of deep pain perception. NGF is important not only for the survival of sensory neurons but also for the sympathetic neurons and cholinergic neurons of the basal forebrain; however, it is the sensory neurons that are mainly affected in patients with mutant NGFB. In this report, we describe the effects of the mutation on the function of NGF protein and the molecular mechanisms that may underlie the pain insensitivity phenotype in these patients. We show that the mutant NGF has lost its ability to mediate differentiation of PC12 cells into a neuron-like phenotype. We also show that the inability of PC12 cells to differentiate is due to a markedly reduced secretion of mature R221W NGF. The R221W NGF is found mainly as proNGF, in contrast to wild-type NGF which is predominantly in the mature form in both undifferentiated and differentiated PC12 cells. The reduction in numbers of sensory fibers observed in the patients is therefore probably due to loss of trophic support as a result of drastically reduced secretion of NGF from the target organs. Taken together, these data show a clear decrease in the availability of mutant mature NGF and also an accumulation of proNGF in both neuronal and non-neuronal cells. The differential loss of NGF-dependent neurons in these patients, mainly affecting sensory neurons, may depend on differences in the roles of mature NGF and proNGF in different cells and tissues.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • COS Cells
  • Chlorocebus aethiops
  • Endoplasmic Reticulum / metabolism
  • Endoplasmic Reticulum Chaperone BiP
  • Fibrinolysin / metabolism
  • Furin / metabolism
  • Heat-Shock Proteins / metabolism
  • Humans
  • Molecular Chaperones / metabolism
  • Mutation, Missense
  • Nerve Growth Factor / genetics*
  • Nerve Growth Factor / metabolism*
  • Neurogenesis*
  • Neurons / metabolism
  • PC12 Cells
  • Pain / genetics
  • Protein Precursors / metabolism*
  • Rats
  • Receptor, trkA / metabolism

Substances

  • Endoplasmic Reticulum Chaperone BiP
  • Heat-Shock Proteins
  • Molecular Chaperones
  • NGF protein, human
  • Protein Precursors
  • pro-nerve growth factor, human
  • Nerve Growth Factor
  • Receptor, trkA
  • Fibrinolysin
  • Furin