Ultrafast energy relaxation dynamics of amide I vibrations coupled with protein-bound water molecules

Tan, Ji; Zhang, Jiahui; Li, Chuanzhao; Luo, Yi; Ye, Shuji

doi:10.1038/s41467-019-08899-3

Cited by 50 publications

(54 citation statements)

References 67 publications

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“…There is a consensus that dynamic nanoscopic heterogeneities are involved in signal transduction in biological membranes (65). Recently, it was shown that the collective picosecond dynamics of interfacial water (with the energy range of 2 to 5 meV) can serve as a relaxation pathway for protein backbones (66,67). Therefore, it is intriguing that the ultrafast dynamics of functional lipid pairs (the energy of the optical modes) operate at the same timescales as relaxation processes of the transmembrane proteins (66).…”

Section: Discussionmentioning

confidence: 99%

Functional lipid pairs as building blocks of phase-separated membranes

Soloviov

Cai

Bolmatov

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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Biological membranes exhibit a great deal of compositional and phase heterogeneity due to hundreds of chemically distinct components. As a result, phase separation processes in cell membranes are extremely difficult to study, especially at the molecular level. It is currently believed that the lateral membrane heterogeneity and the formation of domains, or rafts, are driven by lipid–lipid and lipid–protein interactions. Nevertheless, the underlying mechanisms regulating membrane heterogeneity remain poorly understood. In the present work, we combine inelastic X-ray scattering with molecular dynamics simulations to provide direct evidence for the existence of strongly coupled transient lipid pairs. These lipid pairs manifest themselves experimentally through optical vibrational (a.k.a. phononic) modes observed in binary (1,2-dipalmitoyl-sn-glycero-3-phosphocholine [DPPC]–cholesterol) and ternary (DPPC–1,2-dioleoyl-sn-glycero-3-phosphocholine/1-palmitoyl-2-oleoyl-glycero-3-phosphocholine [DOPC/POPC]–cholesterol) systems. The existence of a phononic gap in these vibrational modes is a direct result of the finite size of patches formed by these lipid pairs. The observation of lipid pairs provides a spatial (subnanometer) and temporal (subnanosecond) window into the lipid–lipid interactions in complex mixtures of saturated/unsaturated lipids and cholesterol. Our findings represent a step toward understanding the lateral organization and dynamics of membrane domains using a well-validated probe with a high spatial and temporal resolution.

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Section: Discussionmentioning

confidence: 99%

Functional lipid pairs as building blocks of phase-separated membranes

Soloviov

Cai

Bolmatov

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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“…294 The Ye group investigated the impact of hydration water on the vibrational energy relaxation in an interfacial protein. 247 Tan et al probed the vibrational dynamics of the amide-I mode of the KALP23 peptide at the H 2 O and D 2 O interface. The vibrational relaxation times showed a strong solvent dependence that the authors attributed to resonant vibrational energy transfer from the amide-I mode to water bending modes.…”

Section: Chemical Reviewsmentioning

confidence: 99%

Structure and Dynamics of Interfacial Peptides and Proteins from Vibrational Sum-Frequency Generation Spectroscopy

et al. 2020

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Proteins at interfaces play important roles in cell biology, immunology, bioengineering, and biomimetic material design. Many biological processes are based on interfacial protein action, ranging from cellular communication to immune responses and the protein-driven mineralization of bone. Despite the importance of interfacial proteins, comparatively little is known about their structure. The standard methods for studying crystalline or solution-phase proteins (X-ray diffraction and NMR spectroscopy) are not well-suited for studying proteins at interfaces, and for these proteins we still lack a corresponding technique that can provide the same level of structural resolution. This is not surprising in view of the challenges involved in probing the structure of proteins within monomolecular films assembled at a very thin interface in situ. Vibrational sumfrequency generation (SFG) spectroscopy has the potential to overcome this challenge and investigate the structure and dynamics of proteins at interfaces at the molecular level with subpicosecond time resolution. While SFG studies were initially limited to simple model peptides, the past decade has seen a dramatic advancement of experimental techniques and data analysis methods that has made it possible to also study interfacial proteins and their folding, binding, orientation, hydration, and dynamics. In this review, we first explain the principles of SFG spectroscopy and the experimental and theoretical methods to measure and analyze protein SFG spectra. Then we give an extensive overview of the interfacial proteins studied to date with SFG. We highlight representative examples to demonstrate recent advances in probing the structure of proteins at the interfaces of liquids, membranes, minerals, and synthetic materials.

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“…Here, the main purpose of the switch is to activate the molecules [ 27 ] which experience the relaxation time as a response to the continuous wave (CW) on the femtosecond timescale. [ 28 ] Here, we report for the first time the time‐dependent absorption of the NMA molecules. Time‐dependent absorption of other molecules is known and was reported for instance in ref.…”

Section: Introductionmentioning

confidence: 99%