Mechanistic Bioinorganic Chemistry - American Chemical Society

18 Donor-Acceptor Electronic Coupling in Ruthenium-Modified Heme Proteins 1

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Danilo R. Casimiro , David N . Beratan , José Nelson Onuchic , Jay R. Winkler , and Harry B. Gray

Downloaded by FUDAN UNIV on November 18, 2016 | http://pubs.acs.org Publication Date: May 5, 1996 | doi: 10.1021/ba-1995-0246.ch018

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1

1

Beckman Institute, California Institute of Technology, Pasadena, C A 91125

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Department of Chemistry, University of Pittsburgh, Pittsburgh, PA 15260

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Department of Physics, University of California, San Diego, L a Jolla, C A 92093

The rates of electron transfer (ET) in six Ru-modified cytochrome c derivatives were analyzed in terms of four theoretical models describing donor-acceptor electronic coupling. The simplest model, which treats the protein as a homogeneous medium, fails to describe the variations in ET rates with changes in donor-acceptor separation. The three other models explicitly account for the inhomogeneity of the polypeptide matrix and are more successful in describing the electronic couplings. Calculations of relative coupling strengths give results within an order of magnitude of experimentally determined values for cytochrome c. The homogeneous-medium model is more successful in describing ET in Ru-modified myoglobin, and two of the inhomogeneous-medium models suggest that multiple pathways are important in mediating the electronic coupling.

A N Y B I O E N E R G E T I C A N D B I O S Y N T H E T I C PROCESSES i n v o l v e e l e c t r o n -

t r a n s f e r ( E T ) steps i n w h i c h a n e l e c t r o n t u n n e l s s e v e r a l a n g s t r o m s f r o m donor to acceptor through protein (J). T h e problem o f understanding t h e d e t a i l e d m e c h a n i s m s o f t h e s e p r o c e s s e s is b e i n g a d d r e s s e d e x p e r i m e n t a l l y t h r o u g h s t u d i e s o f E T i n s y n t h e t i c m o d e l c o m p l e x e s (2-4), c h e m i c a l l y m o d i f i e d m e t a l l o p r o t e i n s (5), a n d p r o t e i n c o m p l e x e s (6-8). T h e o r e t i c a l efforts a r e a i m e d at d e s c r i b i n g t h e e l e c t r o n i c c o u p l i n g b e t w e e n d i s t a n t r e d o x sites (9-21) a n d c l a r i f y i n g t h e i m p o r t a n c e o f p r o t e i n c o n f o r m a t i o n a l d y n a m i c s i n r e g u l a t i n g E T (22). A p a r t i c u l a r e m p h a s i s 0065-2393/95/0246-0471$08.00/0 © 1995 American Chemical Society

Thorp and Pecoraro; Mechanistic Bioinorganic Chemistry Advances in Chemistry; American Chemical Society: Washington, DC, 1996.

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o f o u r w o r k is t o i d e n t i f y t h e r o l e o f t h e p r o t e i n m a t r i x i n m e d i a t i n g biological electron transfer. T h e weak electronic c o u p l i n g b e t w e e n distant donor and acceptor sites l e a d s t o l o n g - r a n g e E T r a t e s (fc ) t h a t a r e w e l l - d e s c r i b e d b y a n o n a d i a b a t i c f o r m u l a t i o n (23): ET

2

|T | (FC)

(1)

DA

T h e r a t e is p r o p o r t i o n a l t o a n e l e c t r o n i c c o u p l i n g f a c t o r , | T | , a n d a F r a n c k - C o n d o n f a c t o r , F C , t h a t arises f r o m n u c l e a r m o t i o n c o u p l e d t o the E T process. T h e F C factor describes t h e trade-off b e t w e e n reaction free energy a n d t h e nuclear r e o r g a n i z a t i o n energy. A t t h e o p t i m u m d r i v i n g f o r c e , F C is u n i t y , a n d rates r e a c h a m a x i m u m v a l u e (k ), l i m i t e d by I T | . T h e simplest description o f T treats t h e m e d i u m b e t w e e n d o n o r a n d a c c e p t o r as a o n e - d i m e n s i o n a l s q u a r e t u n n e l i n g b a r r i e r ( 1 D S B ) . A s s u c h , t h e r a t e is p r e d i c t e d t o d r o p e x p o n e n t i a l l y w i t h R - R , t h e t u n n e l i n g d i s t a n c e (24, 2 5 ) :


D A

2

max

D A

2

D

A

0

2\TH93 186

4^^^

E85

^

^

^

V

^

Figure 6. Comparison of dominant tunneling pathways (left) and residues identified in EH searches (right) of Ru(NH ) (HisX)-modified Zn-substituted Mb [X = 70 (A), 48 (B), and 83 (C)\. 3

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MECHANISTIC BIOINORGANIC CHEMISTRY

Acknowledgments We thank A. Kuki and R. A. Marcus for preprints of references 13 and 43, respectively. This research was supported by the National Science Foundation, the National Institutes of Health, the Department of Energy, and the Arnold and Mabel Beckman Foundation.


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RECEIVED for review July 19, 1993. ACCEPTED revised manuscript December 10, 1993.


Mechanistic Bioinorganic Chemistry - American Chemical Society

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