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Title: From Protein Design to the Energy Landscape of a Cold Unfolding Protein

Abstract

Understanding protein folding is crucial for protein sciences. The conformational spaces and energy landscapes of cold (unfolded) protein states, as well as the associated transitions, are hardly explored. Furthermore, it is not known how structure relates to the cooperativity of cold transitions, if cold and heat unfolded states are thermodynamically similar, and if cold states play important roles for protein function. We created the cold unfolding 4-helix bundle DCUB1 with a de novo designed bipartite hydrophilic/hydrophobic core featuring a hydrogen bond network which extends across the bundle in order to study the relative importance of hydrophobic versus hydrophilic protein–water interactions for cold unfolding. Structural and thermodynamic characterization resulted in the discovery of a complex energy landscape for cold transitions, while the heat unfolded state is a random coil. Below ~0 °C, the core of DCUB1 disintegrates in a largely cooperative manner, while a near-native helical content is retained. The resulting cold core-unfolded state is compact and features extensive internal dynamics. Below -5 °C, two additional cold transitions are seen, that is, (i) the formation of a water-mediated, compact, and highly dynamic dimer, and (ii) the onset of cold helix unfolding decoupled from cold core unfolding. Our results suggest that coldmore » unfolding is initiated by the intrusion of water into the hydrophilic core network and that cooperativity can be tuned by varying the number of core hydrogen bond networks. Protein design has proven to be invaluable to explore the energy landscapes of cold states and to robustly test related theories.« less

Authors:
 [1];  [2];  [3];  [4];  [5];  [6];  [7]; ORCiD logo [8]; ORCiD logo [9];  [10]; ORCiD logo [11]; ORCiD logo [6]; ORCiD logo [1]
+ Show Author Affiliations
  1. State Univ. of New York (SUNY), Buffalo, NY (United States)
  2. Univ. of North Carolina, Chapel Hill, NC (United States); Menten AI Inc., Palo Alto, CA (United States)
  3. State Univ. of New York at Buffalo, NY (United States)
  4. Univ. of North Carolina, Chapel Hill, NC (United States); Univ. of the Pacific, Stockton, CA (United States)
  5. State Univ. of New York at Buffalo, NY (United States); Astrix Software Technology Inc., Red Bank, NJ (United States)
  6. Univ. of North Carolina, Chapel Hill, NC (United States)
  7. Malvern Panalytical Inc, Northhampton, MA (United States)
  8. Rensselaer Polytechnic Inst., Troy, NY (United States)
  9. Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
  10. Stanford Univ., CA (United States)
  11. Hauptman-Woodward Medical Research Inst. (HWI), Buffalo, NY (United States); State Univ. of New York at Buffalo, NY (United States)
Publication Date:
Research Org.:
Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Sponsoring Org.:
USDOE Laboratory Directed Research and Development (LDRD) Program; National Science Foundation (NSF); National Institutes of Health (NIH)
OSTI Identifier:
1865037
Report Number(s):
LA-UR-21-32367
Journal ID: ISSN 1520-6106
Grant/Contract Number:  
89233218CNA000001; AC02-76SF00515; MCB-1615570; MCB-180104; GM131923; P30GM133894; S10OD021512; 1S10OD012254; 1231306
Resource Type:
Accepted Manuscript
Journal Name:
Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry
Additional Journal Information:
Journal Volume: 126; Journal Issue: 6; Journal ID: ISSN 1520-6106
Publisher:
American Chemical Society
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; cold denaturation; protein design; NMR; simulation; alkyls; molecular structure; molecules; noncovalent interactions; x-rays

Citation Formats

Pulavarti, Surya V.S.R.K., Maguire, Jack B., Yuen, Shirley, Harrison, Joseph S., Griffin, Jermel, Premkumar, Lakshmanane, Esposito, Edward A., Makhatadze, George I., Garcia, Angel E., Weiss, Thomas M., Snell, Edward H., Kuhlman, Brian, and Szyperski, Thomas. From Protein Design to the Energy Landscape of a Cold Unfolding Protein. United States: N. p., 2022. Web. doi:10.1021/acs.jpcb.1c10750.
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Pulavarti, Surya V.S.R.K., Maguire, Jack B., Yuen, Shirley, Harrison, Joseph S., Griffin, Jermel, Premkumar, Lakshmanane, Esposito, Edward A., Makhatadze, George I., Garcia, Angel E., Weiss, Thomas M., Snell, Edward H., Kuhlman, Brian, & Szyperski, Thomas. From Protein Design to the Energy Landscape of a Cold Unfolding Protein. United States. https://doi.org/10.1021/acs.jpcb.1c10750
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Pulavarti, Surya V.S.R.K., Maguire, Jack B., Yuen, Shirley, Harrison, Joseph S., Griffin, Jermel, Premkumar, Lakshmanane, Esposito, Edward A., Makhatadze, George I., Garcia, Angel E., Weiss, Thomas M., Snell, Edward H., Kuhlman, Brian, and Szyperski, Thomas. Mon . "From Protein Design to the Energy Landscape of a Cold Unfolding Protein". United States. https://doi.org/10.1021/acs.jpcb.1c10750. https://www.osti.gov/servlets/purl/1865037.
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@article{osti_1865037,
title = {From Protein Design to the Energy Landscape of a Cold Unfolding Protein},
author = {Pulavarti, Surya V.S.R.K. and Maguire, Jack B. and Yuen, Shirley and Harrison, Joseph S. and Griffin, Jermel and Premkumar, Lakshmanane and Esposito, Edward A. and Makhatadze, George I. and Garcia, Angel E. and Weiss, Thomas M. and Snell, Edward H. and Kuhlman, Brian and Szyperski, Thomas},
abstractNote = {Understanding protein folding is crucial for protein sciences. The conformational spaces and energy landscapes of cold (unfolded) protein states, as well as the associated transitions, are hardly explored. Furthermore, it is not known how structure relates to the cooperativity of cold transitions, if cold and heat unfolded states are thermodynamically similar, and if cold states play important roles for protein function. We created the cold unfolding 4-helix bundle DCUB1 with a de novo designed bipartite hydrophilic/hydrophobic core featuring a hydrogen bond network which extends across the bundle in order to study the relative importance of hydrophobic versus hydrophilic protein–water interactions for cold unfolding. Structural and thermodynamic characterization resulted in the discovery of a complex energy landscape for cold transitions, while the heat unfolded state is a random coil. Below ~0 °C, the core of DCUB1 disintegrates in a largely cooperative manner, while a near-native helical content is retained. The resulting cold core-unfolded state is compact and features extensive internal dynamics. Below -5 °C, two additional cold transitions are seen, that is, (i) the formation of a water-mediated, compact, and highly dynamic dimer, and (ii) the onset of cold helix unfolding decoupled from cold core unfolding. Our results suggest that cold unfolding is initiated by the intrusion of water into the hydrophilic core network and that cooperativity can be tuned by varying the number of core hydrogen bond networks. Protein design has proven to be invaluable to explore the energy landscapes of cold states and to robustly test related theories.},
doi = {10.1021/acs.jpcb.1c10750},
journal = {Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry},
number = 6,
volume = 126,
place = {United States},
year = {Mon Feb 07 00:00:00 EST 2022},
month = {Mon Feb 07 00:00:00 EST 2022}
}
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https://doi.org/10.1021/acs.jpcb.1c10750
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