Proteolipid protein modulates preservation of peripheral axons and premature death when myelin protein zero is lacking

Glia. 2016 Jan;64(1):155-74. doi: 10.1002/glia.22922. Epub 2015 Sep 22.

Abstract

Protein zero (P0) is the major structural component of peripheral myelin. Lack of this adhesion protein from Schwann cells causes a severe dysmyelinating neuropathy with secondary axonal degeneration in humans with the neuropathy Dejerine-Sottas syndrome (DSS) and in the corresponding mouse model (P0(null)-mice). In the mammalian CNS, the tetraspan-membrane protein PLP is the major structural myelin constituent and required for the long-term preservation of myelinated axons, which fails in hereditary spastic paraplegia (SPG type-2) and the relevant mouse model (Plp(null)-mice). The Plp-gene is also expressed in Schwann cells but PLP is of very low abundance in normal peripheral myelin; its function has thus remained enigmatic. Here we show that the abundance of PLP but not of other tetraspan myelin proteins is strongly increased in compact peripheral myelin of P0(null)-mice. To determine the functional relevance of PLP expression in the absence of P0, we generated P0(null)*Plp(null)-double-mutant mice. Compared with either single-mutant, P0(null)*Plp(null)-mice display impaired nerve conduction, reduced motor functions, and premature death. At the morphological level, axonal segments were frequently non-myelinated but in a one-to-one relationship with a hypertrophic Schwann cell. Importantly, axonal numbers were reduced in the vital phrenic nerve of P0(null)*Plp(null)-mice. In the absence of P0, thus, PLP also contributes to myelination by Schwann cells and to the preservation of peripheral axons. These data provide a link between the Schwann cell-dependent support of peripheral axons and the oligodendrocyte-dependent support of central axons.

Keywords: Charcot-Marie-tooth disease; Dejerine-Sottas syndrome; Schwann cell; glia-axonal support; hereditary spastic paraplegia (SPG-2); myelin; neurodegeneration; neuropathy; oligodendrocyte.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Axons / metabolism*
  • Axons / pathology
  • Brain / metabolism
  • Brain / pathology
  • Female
  • Kaplan-Meier Estimate
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mortality, Premature
  • Motor Activity / physiology
  • Myelin P0 Protein / genetics
  • Myelin P0 Protein / metabolism*
  • Myelin Proteolipid Protein / genetics
  • Myelin Proteolipid Protein / metabolism*
  • Myelin Sheath / metabolism
  • Myelin Sheath / pathology
  • Myelin-Associated Glycoprotein / metabolism
  • Neural Conduction / physiology
  • Optic Nerve / metabolism
  • Optic Nerve / pathology
  • Phrenic Nerve / metabolism*
  • Phrenic Nerve / pathology
  • Sciatic Nerve / metabolism*
  • Sciatic Nerve / pathology

Substances

  • Mag protein, mouse
  • Mpz protein, mouse
  • Myelin P0 Protein
  • Myelin Proteolipid Protein
  • Myelin-Associated Glycoprotein
  • Plp1 protein, mouse