Clinical or ATPase domain mutations in ABCD4 disrupt the interaction between the vitamin B12-trafficking proteins ABCD4 and LMBD1

J Biol Chem. 2017 Jul 14;292(28):11980-11991. doi: 10.1074/jbc.M117.784819. Epub 2017 Jun 1.

Abstract

Vitamin B12 (cobalamin (Cbl)), in the cofactor forms methyl-Cbl and adenosyl-Cbl, is required for the function of the essential enzymes methionine synthase and methylmalonyl-CoA mutase, respectively. Cbl enters mammalian cells by receptor-mediated endocytosis of protein-bound Cbl followed by lysosomal export of free Cbl to the cytosol and further processing to these cofactor forms. The integral membrane proteins LMBD1 and ABCD4 are required for lysosomal release of Cbl, and mutations in the genes LMBRD1 and ABCD4 result in the cobalamin metabolism disorders cblF and cblJ. We report a new (fifth) patient with the cblJ disorder who presented at 7 days of age with poor feeding, hypotonia, methylmalonic aciduria, and elevated plasma homocysteine and harbored the mutations c.1667_1668delAG [p.Glu556Glyfs*27] and c.1295G>A [p.Arg432Gln] in the ABCD4 gene. Cbl cofactor forms are decreased in fibroblasts from this patient but could be rescued by overexpression of either ABCD4 or, unexpectedly, LMBD1. Using a sensitive live-cell FRET assay, we demonstrated selective interaction between ABCD4 and LMBD1 and decreased interaction when ABCD4 harbored the patient mutations p.Arg432Gln or p.Asn141Lys or when artificial mutations disrupted the ATPase domain. Finally, we showed that ABCD4 lysosomal targeting depends on co-expression of, and interaction with, LMBD1. These data broaden the patient and mutation spectrum of cblJ deficiency, establish a sensitive live-cell assay to detect the LMBD1-ABCD4 interaction, and confirm the importance of this interaction for proper intracellular targeting of ABCD4 and cobalamin cofactor synthesis.

Keywords: ABC transporter; ABCD4; LMBD1; cblF; cblJ; fluorescence resonance energy transfer (FRET); homology modeling; inborn error of metabolism; protein-protein interaction; vitamin B12.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ATP-Binding Cassette Transporters / chemistry
  • ATP-Binding Cassette Transporters / deficiency
  • ATP-Binding Cassette Transporters / genetics*
  • ATP-Binding Cassette Transporters / metabolism
  • Amino Acid Metabolism, Inborn Errors / genetics*
  • Amino Acid Metabolism, Inborn Errors / metabolism
  • Amino Acid Metabolism, Inborn Errors / pathology
  • Amino Acid Substitution
  • Catalytic Domain
  • Cell Line, Transformed
  • Cells, Cultured
  • HeLa Cells
  • Humans
  • Luminescent Proteins / genetics
  • Luminescent Proteins / metabolism
  • Lysosomes / enzymology
  • Lysosomes / metabolism*
  • Lysosomes / pathology
  • Metabolism, Inborn Errors / genetics*
  • Metabolism, Inborn Errors / metabolism
  • Metabolism, Inborn Errors / pathology
  • Models, Molecular*
  • Molecular Docking Simulation
  • Mutation*
  • Nucleocytoplasmic Transport Proteins / chemistry
  • Nucleocytoplasmic Transport Proteins / deficiency
  • Nucleocytoplasmic Transport Proteins / genetics*
  • Nucleocytoplasmic Transport Proteins / metabolism
  • Protein Conformation
  • Protein Interaction Domains and Motifs
  • Protein Multimerization
  • Protein Transport
  • Recombinant Fusion Proteins / chemistry
  • Recombinant Fusion Proteins / metabolism
  • Structural Homology, Protein
  • Vitamin B 12 / metabolism

Substances

  • ABCD4 protein, human
  • ATP-Binding Cassette Transporters
  • LMBRD1 protein, human
  • Luminescent Proteins
  • Nucleocytoplasmic Transport Proteins
  • Recombinant Fusion Proteins
  • Vitamin B 12

Supplementary concepts

  • Methylmalonic Aciduria and Homocystinuria, CblF Type

Associated data

  • PDB/2D62
  • PDB/4RY2