Glycosylation not only impacts the functions of glycoproteins but can also improve glycoprotein stability and folding efficiency-characteristics that are desirable for protein engineering and therapeutic design. To further elucidate the effects of N-glycosylation on protein structure and to provide principles useful for the rational design of α-helical glycopeptides, we investigate stabilizing protein-sugar interactions in α-helical glycosylation sites using an integrated structural bioinformatics analysis and molecular dynamics simulation approach. We identify two glycan conformations with an Asn χ1 of 180° or 300° that are amenable to α-helical structure in natural α-helical glycosylation sites in the Protein Data Bank. A combination of sterics and favorable intraglycopeptide enthalpy explains the existence of only these two conformations. Furthermore, we catalog all known protein-sugar interactions that utilize these conformational modes. The most common interactions involve either a Glu residue at the -4 position interacting with the GlcNAc whose Asn has χ1 = 300° or a Glu residue at the +4 position interacting with the GlcNAc whose Asn has χ1 = 180°. Via metadynamics simulations of model α-helical glycopeptides with each of these two interactions, we find that both interactions are stabilizing as a result of favorable electrostatic intraglycopeptide interactions. Thus, we suggest that incorporating a Glu at either the -4 or +4 position relative to an N-linked glycan may be a useful strategy for engineering stable α-helical glycoproteins.