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Effect of charged amino acid side chain length on lateral cross-strand interactions between carboxylate- and guanidinium-containing residues in a β-hairpin

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Abstract

β-Sheet is one of the major protein secondary structures. Oppositely charged residues are frequently observed across neighboring strands in antiparallel sheets, suggesting the importance of cross-strand ion pairing interactions. The charged amino acids Asp, Glu, Arg, and Lys have different numbers of hydrophobic methylenes linking the charged functionality to the backbone. To investigate the effect of side chain length of guanidinium- and carboxylate-containing residues on lateral cross-strand ion pairing interactions at non-hydrogen-bonded positions, β-hairpin peptides containing Zbb-Agx (Zbb = Asp, Glu, Aad in increasing length; Agx = Agh, Arg, Agb, Agp in decreasing length) sequence patterns were studied by NMR methods. The fraction folded population and folding energy were derived from the chemical shift deviation data. Peptides with high fraction folded populations involved charged residue side chain lengths that supported high strand propensity. Double mutant cycle analysis was used to determine the interaction energy for the potential lateral ion pairs. Minimal interaction was observed between residues with short side chains, most likely due to the diffused positive charge on the guanidinium group, which weakened cross-strand electrostatic interactions with the carboxylate side chain. Only the Aad-Arg/Agh interactions with long side chains clearly exhibited stabilizing energetics, possibly relying on hydrophobics. A survey of a non-redundant protein structure database revealed that the statistical sheet pair propensity followed the trend Asp-Arg < Glu-Arg, implying the need for matching long side chains. This suggested the need for long side chains on both guanidinium-bearing and carboxylate-bearing residues to stabilize the β-hairpin motif.

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Abbreviations

Aad:

(S)-Aminoadipate

Agb:

(S)-2-Amino-4-guanidinobutyric acid

Agh:

(S)-2-Amino-6-guanidinohexanoic acid

Agp:

(S)-2-Amino-3-guanidinopropionic acid

Ala:

Alanine

Arg:

Arginine

Asp:

Aspartate

DQF-COSY:

Double-quantum filtered-correlated spectroscopy

Fmoc:

N α-Fluorenylmethyloxycarbonyl

Glu:

Glutamate

Lys:

Lysine

MALDI-TOF:

Matrix-assisted laser desorption ionization time-of-flight

NMR:

Nuclear magnetic resonance spectroscopy

NOESY:

Nuclear overhauser effect spectroscopy

Orn:

Ornithine

ROESY:

Rotating-frame nuclear Overhauser effect spectroscopy

TOCSY:

Total correlation spectroscopy

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Acknowledgments

This work was supported by National Taiwan University (R.P.C., NTU-ERP-103R891302) and the Ministry of Science and Technology in Taiwan (former National Science Council; S. J. H., 100-2731-M-002-002-MY2; R.P.C., 99-2113-M-002-002-MY2, 101-2113-M-002-006-MY2, 103-2113-M-002-018-MY3). The authors would like to thank the Computer and Information Networking Center at National Taiwan University for the support of the high-performance computing facilities.

Conflict of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Department of Chemistry, National Taiwan University, Taipei, 10617, Taiwan

    Hsiou-Ting Kuo, Shing-Lung Liu, Wen-Chieh Chiu, Chun-Jen Fang, Hsien-Chen Chang, Wei-Ren Wang, Po-An Yang, Jhe-Hao Li & Richard P. Cheng

  2. Instrument Center at National Taiwan University, National Taiwan University, Taipei, 10617, Taiwan

    Shing-Jong Huang & Shou-Ling Huang

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  1. Hsiou-Ting Kuo
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Kuo, HT., Liu, SL., Chiu, WC. et al. Effect of charged amino acid side chain length on lateral cross-strand interactions between carboxylate- and guanidinium-containing residues in a β-hairpin. Amino Acids 47, 885–898 (2015). https://doi.org/10.1007/s00726-015-1916-2

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