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Protein side-chain resonance assignment and NOE assignment using RDC-defined backbones without TOCSY data

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Abstract

One bottleneck in NMR structure determination lies in the laborious and time-consuming process of side-chain resonance and NOE assignments. Compared to the well-studied backbone resonance assignment problem, automated side-chain resonance and NOE assignments are relatively less explored. Most NOE assignment algorithms require nearly complete side-chain resonance assignments from a series of through-bond experiments such as HCCH-TOCSY or HCCCONH. Unfortunately, these TOCSY experiments perform poorly on large proteins. To overcome this deficiency, we present a novel algorithm, called Nasca (NOE Assignment and Side-Chain Assignment), to automate both side-chain resonance and NOE assignments and to perform high-resolution protein structure determination in the absence of any explicit through-bond experiment to facilitate side-chain resonance assignment, such as HCCH-TOCSY. After casting the assignment problem into a Markov Random Field (MRF), Nasca extends and applies combinatorial protein design algorithms to compute optimal assignments that best interpret the NMR data. The MRF captures the contact map information of the protein derived from NOESY spectra, exploits the backbone structural information determined by RDCs, and considers all possible side-chain rotamers. The complexity of the combinatorial search is reduced by using a dead-end elimination (DEE) algorithm, which prunes side-chain resonance assignments that are provably not part of the optimal solution. Then an A* search algorithm is employed to find a set of optimal side-chain resonance assignments that best fit the NMR data. These side-chain resonance assignments are then used to resolve the NOE assignment ambiguity and compute high-resolution protein structures. Tests on five proteins show that Nasca assigns resonances for more than 90% of side-chain protons, and achieves about 80% correct assignments. The final structures computed using the NOE distance restraints assigned by Nasca have backbone RMSD 0.8–1.5 Å from the reference structures determined by traditional NMR approaches.

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Abbreviations

NMR:

Nuclear magnetic resonance

ppm:

Parts per million

RMSD:

Root mean square deviation

HSQC:

Heteronuclear single quantum coherence spectroscopy

NOE:

Nuclear Overhauser effect

NOESY:

Nuclear Overhauser and exchange spectroscopy

TOCSY:

Total correlation spectroscopy

TROSY:

Transverse relaxation-optimized spectroscopy

RDC:

Residual dipolar coupling

PDB:

Protein Data Bank

BMRB:

Biological Magnetic Resonance Bank

pol η UBZ:

Ubiquitin-binding zinc finger domain of the human Y-family DNA polymerase Eta

hSRI:

Human Set2-Rpb1 interacting domain

FF2:

FF Domain 2 of human transcription elongation factor CA150

GB1:

B1 domain of Protein G

CH:

Cα−Hα

SSE:

Secondary structure element

\(\hbox{C}^{\prime}\) :

Carbonyl carbon

MRF:

Markov Random Field

DEE:

Dead-end elimination

GMEC:

Global minimum energy conformation

SA:

Simulated annealing

MD:

Molecular dynamics

\({\mathbb{R}}^3\) :

3-Dimensional Euclidean space

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Acknowledgements

We thank Dr. C. Bailey-Kellogg, Dr. M.S. Apaydin and Mr. J. Martin for reading our draft and providing us with valuable comments. We thank all members of the Donald and Zhou Labs for helpful discussions and comments. We are grateful to Ms. M. Bomar for helping us with pol η UBZ NMR data. We thank Dr. J. Liu for helping us check the side-chain resonance assignments of FF2. We thank the anonymous reviewers for their helpful comments and suggestions. This work is supported by the following grants from National Institutes of Health: R01 GM-65982 and R01 GM-78031 to B.R.D. and R01 GM-079376 to P.Z

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  1. Department of Computer Science, Duke University, Durham, NC, 27708, USA

    Jianyang Zeng & Bruce Randall Donald

  2. Department of Biochemistry, Duke University Medical Center, Durham, NC, 27710, USA

    Pei Zhou & Bruce Randall Donald

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  1. Jianyang Zeng
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Correspondence to Bruce Randall Donald.

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Zeng, J., Zhou, P. & Donald, B.R. Protein side-chain resonance assignment and NOE assignment using RDC-defined backbones without TOCSY data. J Biomol NMR 50, 371–395 (2011). https://doi.org/10.1007/s10858-011-9522-4

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