An anomalous abundance of tryptophan residues in ceramide synthases based on analysis of all membrane proteins in the Swiss-Prot database

J Biol Chem. 2024 Dec 7:108053. doi: 10.1016/j.jbc.2024.108053. Online ahead of print.

Abstract

The relationship between membrane proteins and the lipid constituents of the membrane bilayer depends on finely-tuned atomic interactions, which itself depends on the precise distribution of amino acids within the 3D structure of the protein. In this regard, tryptophan (Trp), one of the least abundant amino acids, is found at higher levels in transmembrane proteins where it likely plays a role in helping anchor them to the membrane. We now re-evaluate Trp distribution in membrane proteins using all known proteins in the Swiss-Prot database and confirm that it is somewhat higher (∼1.7%) than in soluble proteins (∼1.0%), but not as high as in a well-quoted study (∼3.1%). However, the resident endoplasmic reticulum membrane protein, ceramide synthase (CerS), contains a higher abundance of Trp (3.4%). In the case of CerS which contain a Hox-like domain, the Trp residues are asymmetrically distributed throughout the protein with a bias towards the lumenal side of the endoplasmic reticulum membrane. Mutation of these residues, even to other hydrophobic amino acids, leads to loss of activity, expression and/or N-glycosylation. Moreover, 5 of the 10 most conserved amino acids in the CerS are Trp, and site-directed mutagenesis of numerous conserved Trp residues to alanine had distinct effects. Our data is consistent with other studies suggesting that Trp plays critical roles not only in membrane anchoring of transmembrane proteins but also in their activity and function.

Keywords: Sphingolipids; ceramide; ceramide synthase; lipid synthesis; membrane proteins; tryptophan.