by THz spectroscopy. Proc Natl Acad Sci U S
A 103:12301–12306
151. Heyden M, Bru ¨ndermann E, Heugen U,
Niehues G, Leitner DM, Havenith M
(2008) The long range influence of carbohydrates on the solvation dynamics of water—
answers from THz spectroscopic measurements and molecular modelling simulations.
J Am Chem Soc 130:5773–5779
152. Heyden M, Havenith M (2010) Combining
THz spectroscopy and MD simulations to
study protein-hydration coupling. Methods
52:74–83
153. Leitner DM, Gruebele M, Havenith M
(2008) Solvation dynamics of biomolecules:
modeling and terahertz experiments. HFSP J
32:314–323
154. Luong TQ, Xu Y, Bru ¨ndermann E, Leitner
DM, Havenith M (2016) Hydrophobic collapse induces changes in the collective protein
and hydration low frequency modes. Chem
Phys Lett 651:1–7
155. Xu Y, Gnanasekaran R, Leitner DM (2012)
Analysis of water and hydrogen bond dynamics at the surface of an antifreeze protein. J At
Mol Opt Phys 2012:125071–125076
156. Meister K, Duman JG, Xu Y, DeVries AL,
Leitner DM, Havenith M (2014) The role of
sulfates on antifreeze protein activity. J Phys
Chem B 118:7920–7924
157. Schmidt DA, Birer O ¨ , Funkner S, Born B,
Gnanasekaran R, Schwaab G, Leitner DM,
Havenith M (2009) Rattling in the cage:
ions as probes of sub-picosecond water network dynamics. J Am Chem Soc
131:18512–18517
158. Xu Y, B€ aumer A, Meister K, Bischak C, DeVries AL, Leitner DM, Havenith M (2016)
Protein-water dynamics in antifreeze protein
III activity. Chem Phys Lett 647:1–6
159. Acbas G, Niessen KA, Snell EH, Markelz AG
(2014) Optical measurements of long-range
protein vibrations. Nat Commun 5:3076
160. Knab JR, Chen J-Y, Markelz AG (2006)
Hydration dependence of conformational
dielectric relaxation of lysozyme. Biophys J
90:2576–2581
161. Yu X, Park J, Leitner DM (2003) Thermodynamics of protein hydration computed by
molecular dynamics and normal modes. J
Phys Chem B 107:12820–12829
162. Pandey HD, Leitner DM (2017) Thermodynamics of hydration water around an antifreeze protein: a molecular simulation study.
J Phys Chem B 121:9498–9507
163. LeBard DN, Matyushov DV (2010) Ferroelectric hydration shells around proteins: electrostatics of the protein-water interface. J
Phys Chem B 114:9246–9258
164. Martin DR, Matyushov DV (2012)
Non-Gaussian statistics and nanosecond
dynamics of electrostatic fluctuations affecting optical transitions in proteins. J Phys
Chem B 116:10294–10300
165. Martin DR, Matyushov DV (2015) Dipolar
nanodomains in protein hydration shells. J
Phys Chem Lett 6:407–412
166. Matyushov DV (2010) Terahertz response of
dipolar impurities in polar liquids: on anomalous dielectric absorption of protein solutions.
Phys Rev E 81:021914
167. Heyden M, Tobias DJ (2013) Spatial dependence of protein-water collective hydrogen
bond dynamics. Phys Rev Lett 111:218101
168. Laage D, Elsaesser T, Hynes JT (2017) Water
dynamics in the hydration shells of biomolecules. Chem Rev 117:10694–10725
169. Xu Y, Havenith M (2015) Perspective: watching low-frequency vibrations of water in biomolecules by THz spectroscopy. J Chem Phys
143:170901
170. Wirtz H, Sch€ afer S, Hoberg C, Reid KM,
Leitner DM, Havenith M (2018) Hydrophobic collapse of ubiquitin generates rapid
protein-water
motions.
Biochemistry
57:3650–3657
171. Wellig S, Hamm P (2018) Solvation layer of
antifreeze proteins analyzed with a Markov
state
model.
J
Phys
Chem
B
122:11014–11022.
https://doi.org/10.
1021/acs.jpcb.8b04491
172. Leitner DM, Pandey HD, Reid KM (2019)
Energy transport across interfaces in biomolecular systems. J Phys Chem B
123:9507–9524
173. Reid KM, Yamato T, Leitner DM (2020) Variation of energy transfer rates across proteinwater contacts with equilibrium structural
fluctuations of a homodimeric hemoglobin. J
Phys Chem B 124:1148–1159
174. Leitner DM, Yamato T (2020) Recent developments in the computational study of protein structural and vibrational energy
dynamics. Biophysical Reviews 12:317–322
175. Leitner DM, Hyeon C, Reid KM (2020)
Water-mediated biomolecular dynamics and
allostery. J Chem Phys 152:240901
Locating and Navigating Energy Transport Networks in Proteins
59
A 103:12301–12306
151. Heyden M, Bru ¨ndermann E, Heugen U,
Niehues G, Leitner DM, Havenith M
(2008) The long range influence of carbohydrates on the solvation dynamics of water—
answers from THz spectroscopic measurements and molecular modelling simulations.
J Am Chem Soc 130:5773–5779
152. Heyden M, Havenith M (2010) Combining
THz spectroscopy and MD simulations to
study protein-hydration coupling. Methods
52:74–83
153. Leitner DM, Gruebele M, Havenith M
(2008) Solvation dynamics of biomolecules:
modeling and terahertz experiments. HFSP J
32:314–323
154. Luong TQ, Xu Y, Bru ¨ndermann E, Leitner
DM, Havenith M (2016) Hydrophobic collapse induces changes in the collective protein
and hydration low frequency modes. Chem
Phys Lett 651:1–7
155. Xu Y, Gnanasekaran R, Leitner DM (2012)
Analysis of water and hydrogen bond dynamics at the surface of an antifreeze protein. J At
Mol Opt Phys 2012:125071–125076
156. Meister K, Duman JG, Xu Y, DeVries AL,
Leitner DM, Havenith M (2014) The role of
sulfates on antifreeze protein activity. J Phys
Chem B 118:7920–7924
157. Schmidt DA, Birer O ¨ , Funkner S, Born B,
Gnanasekaran R, Schwaab G, Leitner DM,
Havenith M (2009) Rattling in the cage:
ions as probes of sub-picosecond water network dynamics. J Am Chem Soc
131:18512–18517
158. Xu Y, B€ aumer A, Meister K, Bischak C, DeVries AL, Leitner DM, Havenith M (2016)
Protein-water dynamics in antifreeze protein
III activity. Chem Phys Lett 647:1–6
159. Acbas G, Niessen KA, Snell EH, Markelz AG
(2014) Optical measurements of long-range
protein vibrations. Nat Commun 5:3076
160. Knab JR, Chen J-Y, Markelz AG (2006)
Hydration dependence of conformational
dielectric relaxation of lysozyme. Biophys J
90:2576–2581
161. Yu X, Park J, Leitner DM (2003) Thermodynamics of protein hydration computed by
molecular dynamics and normal modes. J
Phys Chem B 107:12820–12829
162. Pandey HD, Leitner DM (2017) Thermodynamics of hydration water around an antifreeze protein: a molecular simulation study.
J Phys Chem B 121:9498–9507
163. LeBard DN, Matyushov DV (2010) Ferroelectric hydration shells around proteins: electrostatics of the protein-water interface. J
Phys Chem B 114:9246–9258
164. Martin DR, Matyushov DV (2012)
Non-Gaussian statistics and nanosecond
dynamics of electrostatic fluctuations affecting optical transitions in proteins. J Phys
Chem B 116:10294–10300
165. Martin DR, Matyushov DV (2015) Dipolar
nanodomains in protein hydration shells. J
Phys Chem Lett 6:407–412
166. Matyushov DV (2010) Terahertz response of
dipolar impurities in polar liquids: on anomalous dielectric absorption of protein solutions.
Phys Rev E 81:021914
167. Heyden M, Tobias DJ (2013) Spatial dependence of protein-water collective hydrogen
bond dynamics. Phys Rev Lett 111:218101
168. Laage D, Elsaesser T, Hynes JT (2017) Water
dynamics in the hydration shells of biomolecules. Chem Rev 117:10694–10725
169. Xu Y, Havenith M (2015) Perspective: watching low-frequency vibrations of water in biomolecules by THz spectroscopy. J Chem Phys
143:170901
170. Wirtz H, Sch€ afer S, Hoberg C, Reid KM,
Leitner DM, Havenith M (2018) Hydrophobic collapse of ubiquitin generates rapid
protein-water
motions.
Biochemistry
57:3650–3657
171. Wellig S, Hamm P (2018) Solvation layer of
antifreeze proteins analyzed with a Markov
state
model.
J
Phys
Chem
B
122:11014–11022.
https://doi.org/10.
1021/acs.jpcb.8b04491
172. Leitner DM, Pandey HD, Reid KM (2019)
Energy transport across interfaces in biomolecular systems. J Phys Chem B
123:9507–9524
173. Reid KM, Yamato T, Leitner DM (2020) Variation of energy transfer rates across proteinwater contacts with equilibrium structural
fluctuations of a homodimeric hemoglobin. J
Phys Chem B 124:1148–1159
174. Leitner DM, Yamato T (2020) Recent developments in the computational study of protein structural and vibrational energy
dynamics. Biophysical Reviews 12:317–322
175. Leitner DM, Hyeon C, Reid KM (2020)
Water-mediated biomolecular dynamics and
allostery. J Chem Phys 152:240901
Locating and Navigating Energy Transport Networks in Proteins
59