Hole Hopping Across a Protein-Protein Interface

0501880 - ÚFCH JH 2020 RIV US eng J - Journal Article
Takematsu, K. - Pospíšil, Petr - Pižl, Martin - Towrie, M. - Heyda, Jan - Záliš, Stanislav - Kaiser, J. T. - Winkler, J. R. - Gray, H. B. - Vlček, Antonín
Hole Hopping Across a Protein-Protein Interface.
Journal of Physical Chemistry B. Roč. 123, č. 7 (2019), s. 1578-1591. ISSN 1520-6106. E-ISSN 1520-5207
R&D Projects: GA ČR GA17-01137S; GA MŠMT(CZ) LTAUSA18026
Grant - others:Ga MŠk(CZ) LM2015070
Institutional support: RVO:61388955
Keywords : INTRAMOLECULAR ELECTRON-TRANSFER * RESOLVED INFRARED-SPECTROSCOPY * DENSITY-FUNCTIONAL THEORY
OECD category: Physical chemistry
Impact factor: 2.857, year: 2019
Method of publishing: Limited access

We have investigated photoinduced hole hopping in a Pseudomonas aeruginosa azurin mutant Re126WWCu I , where two adjacent tryptophan residues (W124 and W122) are inserted between the Cu I center and a Re photosensitizer coordinated to a H126 imidazole (Re = Re I (H126)(CO) 3 (dmp) + , dmp = 4,7-dimethyl-1,10-phenanthroline). Optical excitation of this mutant in aqueous media (≤40 μM) triggers 70 ns electron transport over 23 Å, yielding a long-lived (120 μs) Re I (H126)(CO) 3 (dmp •- )WWCu II product. The Re126FWCu I mutant (F124, W122) is not redox-active under these conditions. Upon increasing the concentration to 0.2-2 mM, {Re126WWCu I } 2 and {Re126FWCu I } 2 are formed with the dmp ligand of the Re photooxidant of one molecule in close contact (3.8 Å) with the W122′ indole on the neighboring chain. In addition, {Re126WWCu I } 2 contains an interfacial tryptophan quadruplex of four indoles (3.3-3.7 Å apart). In both mutants, dimerization opens an intermolecular W122′ → //∗Re ET channel (// denotes the protein interface,∗Re is the optically excited sensitizer). Excited-state relaxation and ET occur together in two steps (time constants of ∼600 ps and ∼8 ns) that lead to a charge-separated state containing a Re(H126)(CO) 3 (dmp •- )//(W122 •+ )′ unit. Then (Cu I )′ is oxidized intramolecularly (60-90 ns) by (W122 •+ )′, forming Re I (H126)(CO) 3 (dmp •- )WWCu I //(Cu II )′. The photocycle is closed by ∼1.6 μs Re I (H126)(CO) 3 (dmp •- ) → //(Cu II )′ back ET that occurs over 12 Å, in contrast to the 23 Å, 120 μs step in Re126WWCu I . Importantly, dimerization makes Re126FWCu I photoreactive and, as in the case of {Re126WWCu I } 2 , channels the photoproduced ´´hole´´ to the molecule that was not initially photoexcited, thereby shortening the lifetime of Re I (H126)(CO) 3 (dmp •- )//Cu II . Although two adjacent W124 and W122 indoles dramatically enhance Cu I →RogersRe intramolecular multistep ET, the tryptophan quadruplex in {Re126WWCu I } 2 does not accelerate intermolecular electron transport, instead, it acts as a hole storage and crossover unit between inter- and intramolecular ET pathways. Irradiation of {Re126WWCu II } 2 or {Re126FWCu II } 2 also triggers intermolecular W122′ → //∗Re ET, and the Re(H126)(CO) 3 (dmp •- )//(W122 •+ )′ charge-separated state decays to the ground state by ∼50 ns Re I (H126)(CO) 3 (dmp •- ) + → //(W122 •+ )′ intermolecular charge recombination. Our findings shed light on the factors that control interfacial hole/electron hopping in protein complexes and on the role of aromatic amino acids in accelerating long-range electron transport.
Permanent Link: http://hdl.handle.net/11104/0293862