Distinct transport selectivity of two structural subclasses of the nodulin-like intrinsic protein family of plant aquaglyceroporin channels

Biochemistry. 2005 Dec 27;44(51):16826-34. doi: 10.1021/bi0511888.

Abstract

Major intrinsic proteins (MIPs) are a diverse class of integral membrane proteins that facilitate the transport of water and some small solutes across cellular membranes. X-ray structures of MIPs indicate that a tetrad of residues (the ar/R region) form a narrow pore constriction that constitutes the selectivity filter. In comparison with mammalian and microbial species, plants have a greater number and diversity of MIPs with greater than 30 genes encoding four phylogenetic subfamilies with eight different classes of ar/R sequences. The nodulin 26-like intrinsic protein (NIP) subfamily in Arabidopsis can be subdivided into two ar/R subgroups: the NIP subgroup I, which resembles the archetype of the family, soybean nodulin 26, and the NIP subgroup II, which is represented by the Arabidopsis protein AtNIP6;1. These two NIPs differ principally by the substitution of a conserved alanine (NIP subgroup II) for a conserved tryptophan (NIP subgroup I) in the helix 2 position (H2) of the ar/R filter. A comparison of the water and solute tranport properties of the two proteins was performed by expression in Xenopus laevis oocytes. Nodulin 26 is an aquaglyceroporin with a modest osmotic water permeability (P(f)) and the ability to transport uncharged solutes such as glycerol and formamide. In constrast, AtNIP6;1 showed no measurable water permeability but transported glycerol, formamide, as well as larger solutes that were impermeable to nodulin 26. By site-directed mutagenesis, we show that the H2 position is the crucial determinant that confers these transport behaviors. A comparison of the NIPs and tonoplast-intrinsic proteins (TIP) shows that the H2 residue can predict the transport profile for water and glycerol with histidine found in TIP-like aquaporins, tryptophan found in aquaglyceroporins (NIP I), and alanine found in water-impermeable glyceroporins (AtNIP6;1).

Publication types

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

MeSH terms

  • Amino Acid Sequence
  • Amino Acid Substitution
  • Animals
  • Aquaglyceroporins / chemistry
  • Aquaglyceroporins / genetics
  • Aquaglyceroporins / physiology*
  • Aquaporins / chemistry
  • Aquaporins / genetics
  • Aquaporins / physiology
  • Arabidopsis Proteins / chemistry
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / physiology*
  • Biological Transport
  • Female
  • Formamides / metabolism
  • Glycerol / metabolism
  • Membrane Proteins / chemistry
  • Membrane Proteins / genetics
  • Membrane Proteins / physiology*
  • Molecular Sequence Data
  • Mutation / genetics
  • Oocytes / metabolism
  • Phylogeny
  • Plant Proteins / chemistry
  • Plant Proteins / genetics
  • Plant Proteins / physiology*
  • RNA, Complementary / genetics
  • Sequence Homology, Amino Acid
  • Urea / metabolism
  • Water / metabolism
  • Xenopus laevis

Substances

  • Aquaglyceroporins
  • Aquaporins
  • Arabidopsis Proteins
  • Formamides
  • Membrane Proteins
  • Plant Proteins
  • RNA, Complementary
  • major intrinsic protein, plant
  • nodulin
  • Water
  • formamide
  • Urea
  • Glycerol