Atlastin GTPases are required for Golgi apparatus and ER morphogenesis

Hum Mol Genet. 2008 Jun 1;17(11):1591-604. doi: 10.1093/hmg/ddn046. Epub 2008 Feb 12.

Abstract

The hereditary spastic paraplegias (SPG1-33) comprise a cluster of inherited neurological disorders characterized principally by lower extremity spasticity and weakness due to a length-dependent, retrograde axonopathy of corticospinal motor neurons. Mutations in the gene encoding the large oligomeric GTPase atlastin-1 are responsible for SPG3A, a common autosomal dominant hereditary spastic paraplegia. Here we describe a family of human GTPases, atlastin-2 and -3 that are closely related to atlastin-1. Interestingly, while atlastin-1 is predominantly localized to vesicular tubular complexes and cis-Golgi cisternae, mostly in brain, atlastin-2 and -3 are localized to the endoplasmic reticulum (ER) and are most enriched in other tissues. Knockdown of atlastin-2 and -3 levels in HeLa cells using siRNA (small interfering RNA) causes disruption of Golgi morphology, and these Golgi structures remain sensitive to brefeldin A treatment. Interestingly, expression of SPG3A mutant or dominant-negative atlastin proteins lacking GTPase activity causes prominent inhibition of ER reticularization, suggesting a role for atlastin GTPases in the formation of three-way junctions in the ER. However, secretory pathway trafficking as assessed using vesicular stomatitis virus G protein fused to green fluorescent protein (VSVG-GFP) as a reporter was essentially normal in both knockdown and dominant-negative overexpression conditions for all atlastins. Thus, the atlastin family of GTPases functions prominently in both ER and Golgi morphogenesis, but they do not appear to be required generally for anterograde ER-to-Golgi trafficking. Abnormal morphogenesis of the ER and Golgi resulting from mutations in atlastin-1 may ultimately underlie SPG3A by interfering with proper membrane distribution or polarity of the long corticospinal motor neurons.

Publication types

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

MeSH terms

  • Adenosine Triphosphatases / metabolism
  • Animals
  • Brefeldin A / pharmacology
  • Endoplasmic Reticulum / enzymology*
  • Endoplasmic Reticulum / ultrastructure*
  • GTP Phosphohydrolases / classification
  • GTP Phosphohydrolases / genetics
  • GTP Phosphohydrolases / metabolism*
  • GTP-Binding Proteins
  • Golgi Apparatus / drug effects
  • Golgi Apparatus / enzymology*
  • Golgi Apparatus / ultrastructure*
  • Humans
  • Membrane Proteins
  • Mice
  • Microtubules / enzymology
  • Microtubules / ultrastructure
  • Phylogeny
  • Protein Synthesis Inhibitors / pharmacology
  • Protein Transport / genetics
  • Rats
  • Spastin

Substances

  • Membrane Proteins
  • Protein Synthesis Inhibitors
  • Brefeldin A
  • ATL1 protein, human
  • ATL2 protein, human
  • Adenosine Triphosphatases
  • GTP Phosphohydrolases
  • GTP-Binding Proteins
  • Spastin
  • ATL3 protein, human
  • SPAST protein, human