Electron Transfer in Inorganic, Organic, and Biological Systems

12 Long-Range Electron Transfer

Downloaded by COLUMBIA UNIV on March 20, 2013 | http://pubs.acs.org Publication Date: May 5, 1991 | doi: 10.1021/ba-1991-0228.ch012

in Heme Proteins Porphyrin-Ruthenium Electronic Couplings in Three Ru(His)Cytochromes c Michael J. Therien , Bruce E. Bowler , Mary A. Selman , Harry B. Gray , I-Jy Chang , and Jay R. Winkler 1

2

1

2

1

1

1

2

Arthur Amos Noyes Laboratory of Chemical Physics, California Institute of Technology, Pasadena, C A 91125 Chemistry Department, Brookhaven National Laboratory, Upton, NY 11973

The kinetics of long-range electron transfer (ET) have been measured in Ru(NH ) L(His 39) derivatives (L is NH , pyridine, or isonicotinamide) of Zn-substituted C a n d i d a k r u s e i cytochrome c and Ru(NH ) L(His 62) derivatives (L is NH or pyridine) of Zn-substituted Saccharomyces cerevisiae cytochrome c. The rates of both excited-state electron transfer and thermal recombination are approximately 3 times greater in Ru(His 39)cytochrome c (Zn) than the rates of the corresponding reactions in Ru(His 33)cytochrome c (Zn), but analogous ET reactions in Ru(His 62)cytochrome c (Zn) are roughly 2 orders of magnitude slower than in the His 33-modified protein. Analysis of driving-force dependences establishes that the large variations in the ET rates are due to differences in donor-acceptor electronic couplings. Examination of potential ET pathways indicates that hydrogen bonds could be responsible for the enhanced electronic couplings in the Ru(His 39) and Ru(His 33) proteins. 3 4

3 4

3

3

E L E C T R O N T R A N S F E R (ET) C A N T A K E P L A C E at a p p r e c i a b l e rates o v e r l o n g distances ( > 1 0 Â) i n organic a n d i n o r g a n i c m o l e c u l e s (1-6)

and i n proteins

(6-15). I n n o n p r o t e i n systems, the e v i d e n c e suggests that E T rates d e p e n d 0065-2393/91/0228-0191$06.00/0 © 1991 American Chemical Society

In Electron Transfer in Inorganic, Organic, and Biological Systems; Bolton, J., et al.; Advances in Chemistry; American Chemical Society: Washington, DC, 1991.


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E T IN INORGANIC, ORGANIC, A N D BIOLOGICAL SYSTEMS

u p o n the n u m b e r of covalent b o n d s separating the d o n o r a n d the acceptor, rather t h a n u p o n t h e i r d i r e c t separation distance ( J , 2). T h e r e are m a n y p o t e n t i a l E T pathways i n proteins (16-19); the t h r o u g h - p e p t i d e routes g e n erally i n v o l v e so m a n y b o n d s that t h e y cannot possibly account for the o b s e r v e d rates (20, 21). Pathways that i n c l u d e i o n i c contacts (e.g., h y d r o g e n bonds) or s m a l l through-space j u m p s often can be f o u n d , a n d it has b e e n postulated that such shortcuts greatly enhance the d o n o r - a c c e p t o r e l e c t r o n i c c o u p l i n g (16, 22). O u r w o r k o n r u t h e n i u m - m o d i f i e d cytochromes c is focused i n part o n u n d e r s t a n d i n g h o w variations i n e l e c t r o n - t u n n e l i n g pathways affect long-range d o n o r - a c c e p t o r e l e c t r o n i c couplings (17, 21, 23-25). H e r e w e examine three m o d i f i e d proteins: horse heart R u ( H i s 33)cytochrome c (Zn) (21), Candida krusei R u ( H i s 39)cytochrome c (Zn) (23), a n d Saccharomyces cerevisiae R u ( H i s 62)cytochrome c (Zn) (24). R u t h e n i u m [ R u ( N H ) L ( H i s 3 3 ; H i s 39) w i t h L as N H , p y r i d i n e , o r i s o n i c o t i n a m i d e , a n d R u ( N H ) L ( H i s 62) w i t h L as N H or p y r i d i n e ] d e r i v atives of Z n - s u b s t i t u t e d cyt c [ R u ( H i s X ) Z n cyt c] w e r e p r e p a r e d b y standard procedures (9, 23-26). I n t r a m o l e c u l a r E T can be i n i t i a t e d i n these p r o t e i n derivatives b y photoexcitation of the Z n - p o r p h y r i n (ZnP) to its strongly r e d u c i n g t r i p l e t excited state (21). I n a d d i t i o n to its i n t r i n s i c radiative a n d n o n r a d i a t i v e decay pathways, this t r i p l e t can decay b y E T to a h i s t i d i n e b o u n d R u ( I I I ) - a m m i n e c o m p l e x ( E T * ) . T h e metastable p r o d u c t of the E T * reaction, R u ( I I ) - Z n P , relaxes v i a a t h e r m a l E T process ( E T ) to reform the ground-state c o m p l e x , R u ( I I I ) - Z n P . 3

4

3

3

4

3

+

b

Kinetics of Electron-Transfer Reactions T h e k i n e t i c s of the E T reactions of the R u ( H i s 33)Zn cyt c (21), R u ( H i s 39)Zn cyt c (23), a n d R u ( H i s 62)Zn cyt c (24) derivatives have b e e n m e a s u r e d b y laser flash photolysis (9). E T rates a n d activation parameters are set out i n T a b l e I. A l t h o u g h the E T rates i n R u ( H i s 39)Zn cyt c a n d R u ( H i s 33)Zn cyt c are not v e r y different, i t is s t r i k i n g that E T i n R u ( H i s 62)Zn cyt c is r o u g h l y 2 orders of m a g n i t u d e slower t h a n i n the H i s 3 3 - m o d i f i e d p r o t e i n . Semiclassical theories describe E T rates as the p r o d u c t of three factors: n u c l e a r f r e q u e n c y , electronic c o u p l i n g , a n d nuclear r e o r i e n t a t i o n . A n o n a diabatic expression (eq 1) is appropriate for long-range E T i n d e r i v a t i z e d proteins (27).

(1)

T h e p a r a m e t e r Η i n e q 1 is the e l e c t r o n i c c o u p l i n g m a t r i x e l e m e n t for the E T r e a c t i o n , h is Planck's constant, AG is the reaction free energy, k is the B o l t z m a n n constant, Τ is absolute t e m p e r a t u r e , a n d X is the n u c l e a r r e o r φ

0


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Electron Transfer in Heme Proteins

Table I. Rate Constants and Activation Parameters Reaction

-AG°(eV)

kfr (

s

1

ΔΗ* (kcal mol- )

)

1

AS* (eu)

Ru(His 33)Zn cyt c

a

Rua (isn)(His) ZnP ZnP* Rua (His) Rua (py)(His) ZnP Z n P * -H> Rua (py)(His) Rua5(His) -> Z n P ZnP* Rua (isn)(His) 2+

4

2+

4

+

3+

5

+

3+

4

2+

+

3+

4

0.66 0.70 0.74 0.97 1.01 1.05

2.0 7.7 3.5 3.3 1.6 2.9

Χ x x x x Χ

10 10 10 10 10 10

Rua (isn)(His) 2+

4

+

3+

2+

4

+

3+

4

2 +

u a 5

+

3+

4

0.66 0.70 0.74 0.97 1.01 1.05

6.5 1.5 1.5 8.9 5.7 1.0

x 10 x 10 x 10 x 10 x 10 x 10

5 6 6 6 6 7

Ru(His 62)Zn cyt c

c

Z n P * - » Rua (His) Rua (py)(His) -> Z n P Z n P * -> Rua (py)(His) R u a 5 ( H i s ) -> Z n P 3+

5

2+

4

+

3+

4

2+

+

0.70 0.74 0.97 1.01

6.5 8.1 3.6 2.0

x 10 x 10 x 10 x 10

3 3 4 4

—

NOTE: a is N H , py is pyridine, isn is isonicotinamide, Δ Η * is the activation enthalpy, and aS* is the activation entropy. "Data are from ref. 21. Data are from ref. 23. Data are from ref. 24. 3

fe c

ganization e n e r g y , w h i c h comprises i n n e r - s p h e r e (X ) a n d o u t e r - s p h e r e ( X ) in

out

c o n t r i b u t i o n s . Plots of the R u ( H i s 33)Zn cyt c, R u ( H i s 39)Zn cyt c, a n d R u ( H i s 62)Zn cyt c data, a l o n g w i t h the c o r r e s p o n d i n g fits to e q 1, are s h o w n i n F i g u r e 1. A l t h o u g h the reorganization e n e r g y is n e a r l y the same for the E T reactions i n the three proteins (—1.2 e V ) , the Η

v a l u e for R u ( H i s 39)Zn

φ

cyt c (0.21 c m ) (23) is almost t w i c e as large as that for R u ( H i s 33)Zn cyt c - 1

(0.12 c m " ) (21) a n d over 20 times larger t h a n the Η 1

ψ

c (0.01 c m ) 1

for R u ( H i s 62)Zn cyt

(24).

B o t h the e l e c t r o n i c c o u p l i n g m a t r i x e l e m e n t a n d the o u t e r - s p h e r e c o m p o n e n t of t h e n u c l e a r reorganization energy are t h o u g h t to v a r y w i t h d o nor-acceptor

separation a n d o r i e n t a t i o n (27,

28).

Studies of O s -

and

R u - a m m i n e s b r i d g e d b y p o l y p r o l i n e spacers show that the distance d e p e n d e n c e of λ can e v e n b e greater t h a n that o f Η

φ

m o d e l s o f solvent reorganization p r e d i c t that X

(4). D i e l e c t r i c c o n t i n u u m o u t

w i l l increase w i t h

do

n o r - a c c e p t o r separation ( r ) . M o d e l s that describe charge transfer w i t h i n D A

l o w - d i e l e c t r i c spheres or ellipsoids e m b e d d e d i n d i e l e c t r i c c o n t i n u a e x h i b i t


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E T IN INORGANIC, ORGANIC, A N D BIOLOGICAL SYSTEMS

14+

9+ in

l%

J

T


-1

-6

-0.2

0.1

0.4

0.7

1.0

1.3

-AG° (eV) Figure 1. Plots of In k r vs. -AG for the Ru(His X)cytochrome c ET reactions (Table I). Boxes (His 39), circles (His 33), and triangles (His 62) represent the experimental data (ET* and ET ). Solid lines are the best fits to eq 1: λ = 1.21, Η = 0.21 (His 39); λ = 1.20, Η = 0.12 (His 33); λ = 1.20 eV, Urp = 0.01 cm- (His 62). 0

E

h

φ

φ

1

a dependence upon r as w e l l as u p o n the positions of the redox sites i n s i d e the sphere or e l l i p s o i d (29). M o d e l i n g the R u - Z n - c y t c systems as single spheres suggests, h o w e v e r , that variations i n X for the R u ( H i s 33)Zn cyt c, R u ( H i s 39)Zn cyt c, a n d R u ( H i s 62)Zn cyt c E T reactions w i l l not b e significant (0.57, 0.60, a n d 0.63 eV, respectively). I n the calculations o f X , the cyt c m o l e c u l e was r e p r e s e n t e d as a 34Â sphere e n c l o s i n g 9 0 - 9 5 % of the n o n h y d r o g e n atoms i n the p r o t e i n . T h e R u - a m m i n e g r o u p was taken as a 6-Â sphere. T h e s e two i n t e r p e n e t r a t i n g spheres w e r e e n c l o s e d b y a t h i r d sphere of radius 17.1 Â for R u ( H i s 3 3 ) Z n cyt c, 18.0 Â for R u ( H i s 39)Zn cyt c, a n d 17.9 Â for R u ( H i s 62)Zn cyt c. T h e Z n a n d R u redox centers w e r e p l a c e d 5.8 a n d 14.1 A f r o m the c e n t e r o f the sphere, r e s p e c t i v e l y , a n d separated f r o m one another b y 17.6 A i n R u ( H i s 33)Zn cyt c. T h e c o r r e s p o n d i n g distances w e r e 6.2, 15.0, a n d 19.9 Â for the R u ( H i s 39)Zn cyt c m o d e l , a n d 7.0, 14.9, a n d 21.8 Â for the R u ( H i s 62)Zn cyt c m o d e l . T h e d i e l e c t r i c constant of the sphere was taken as 1.8; the solvent was assigned a static d i e l e c t r i c constant of 78.54 a n d an o p t i c a l d i e l e c t r i c constant of 1.78. D A

o u t

o u t

Models of Electron Transfer I n an extension o f these calculations, w e e x a m i n e d the m a x i m u m v a r i a t i o n in X

o u t

p r e d i c t e d b y the single-sphere c o n t i n u u m m o d e l (34-Â-radius sphere


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Long-Range Electron Transfer in Heme Proteins

195

for cyt c, w i t h its m e t a l c e n t e r 5.8 Â f r o m the origin). T h e R u - a m m i n e c o m p l e x was t a k e n as a 6-Â sphere c e n t e r e d o n the R u atom that was a s s u m e d to b e fixed 16 Â from the c e n t e r of the cyt c sphere. T h e s m a l l sphere can o c c u p y any p o s i t i o n o n the large sphere, w i t h values o f r v a r y i n g from 10.2 to 21.8 Â. A t h i r d sphere t h e n encloses the two other spheres, a n d \ for e l e c t r o n transfer b e t w e e n the two metals was calculated b y t r e a t i n g the solvent as a d i e l e c t r i c c o n t i n u u m . T h e v a l u e of X varies from 0.38 to 0.63 e V almost l i n e a r l y as f*D increases from 10.2 to 21.8 A . T h e total variation o f 0.25 e V is o n l y s l i g h t l y larger t h a n the u n c e r t a i n t y range i n o u r estimates of λ ( ± 0 . 1 eV). T h e invariance of λ f o u n d a m o n g the different E T reactions is, therefore, consistent w i t h theoretical considerations. D A

o u t

o u t


A

T h e differences i n E T rates a m o n g the R u ( H i s 33), R u ( H i s 39), a n d R u ( H i s 62) derivatives arise f r o m variations i n d o n o r - a c c e p t o r e l e c t r o n i c c o u p l i n g . T h e shortest d i r e c t distances b e t w e e n the p o r p h y r i n a n d i m i d a z o l e c a r b o n atoms o f H i s 33 (13.2 A ) , H i s 39 (13.0 Â), a n d H i s 62 (15.5 Â) are m u c h too l o n g for any d i r e c t d o n o r - a c c e p t o r i n t e r a c t i o n (16, 30). Because v i r t u a l l y the same d o n o r a n d acceptor e l e c t r o n i c states are f o u n d i n the t h r e e p r o t e i n s , the differences i n H^, m u s t arise from the m a n n e r i n w h i c h the i n t e r v e n i n g atoms c o u p l e the two states. I f a h o m o g e n e o u s m e d i u m o f c o n stant t u n n e l i n g - b a r r i e r h e i g h t separated the d o n o r a n d the acceptor i n the t h r e e systems, t h e n Η w o u l d d e p e n d p r i m a r i l y o n r . It w o u l d b e n e a r l y the same for R u ( H i s 33)Zn cyt c a n d R u ( H i s 39)Zn cyt c a n d decrease o n l y slightly for R u ( H i s 62)Zn cyt c relative to R u ( H i s 39)Zn c y t c. T h i s p r e d i c t i o n c l e a r l y is not i n accord w i t h e x p e r i m e n t , so i t is logical to c o n c l u d e that the inhomogeneous nature of the polypeptide m e d i u m separating the R u - a m m i n e a n d m e t a l l o p o r p h y r i n sites is responsible for the differential e l e c t r o n i c c o u p l i n g i n these r u t h e n i u m - m o d i f i e d Z n cyt c d e r i v a t i v e s . φ

D A

Bridge-Mediated Electron Transfer B r i d g e - m e d i a t e d E T involves a superexchange m e c h a n i s m i n w h i c h e l e c t r o n i c states of the i n t e r v e n i n g m e d i u m m i x w i t h l o c a l i z e d d o n o r states to p r o d u c e a n o n z e r o H ^(31, 32). B e r a t a n a n d co-workers (16, 33) d e v e l o p e d a s i m p l e m o d e l to describe the c o n t r i b u t i o n of the p o l y p e p t i d e b r i d g e to the electronic c o u p l i n g i n long-range E T i n p r o t e i n systems. T h e essence of the m o d e l is that Η decreases from its m a x i m a l v a l u e (at v a n d e r Waals contact of d o n o r a n d acceptor) b y a constant factor for each covalent b o n d i n the E T pathway. I o n i c contacts ( H b o n d s a n d salt bridges) a n d t h r o u g h space j u m p s decrease Η b y somewhat larger factors. F o r R u ( H i s X ) c y t c, e v e r y p o t e n t i a l t u n n e l i n g pathway is t a k e n to originate at a c a r b o n a t o m of the relevant h i s t i d i n e a n d d e f i n e d to t e r m i n a t e at the first p o i n t o f contact w i t h the p o r p h y r i n . T h e o p t i m u m pathway is that w i t h the c o m b i n a t i o n of t h r o u g h - b o n d , i o n i c , a n d through-space contacts that y i e l d s the smallest diminution of Η . φ

φ

φ



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ET IN INORGANIC, ORGANIC, A N D BIOLOGICAL SYSTEMS

His

33

Figure 2. Possible ET pathways from His 33 and His 39 to the heme in cytochrome c (33). Edge-edge distances are as follows: His 39 to the heme, 13.0 A; His 33 to His 18, 11.7 A; His 33 to the heme, 13.2 Â. Calculations of distances were made by using Biograf/IH version 1.34 (Biodesign, Inc.). The structures of Candida krusei and horse heart cytochromes were generated from the structure of the tuna protein by standard methods (23). In both Candida krusei and horse heart proteins, an imidazole carbon on His 33 is 11.7 Â from an imidazole carbon of His 18, an axial ligand of the metalloporphyrin. This value has been used as the edge-to-edge distance in previous studies (9, 21). His 18 is not likely to be as strongly coupled to the porphyrinlocalized donor and acceptor states as are carbon atoms of the porphyrin ring. Hence, in comparing donor—acceptor coupling in Ru(His 33)Zn cyt c and Ru(His 39)Zn cyt c, distances to porphyrin carbon atoms have been used.

T h e E T pathways i n R u ( H i s 33)Zn cyt c a n d R u ( H i s 39)Zn cyt c generated (33) b y a p p l y i n g the B e r a t a n - O n u c h i c c r i t e r i a (16) are s h o w n i n F i g u r e 2. T h e best pathway from H i s 33 to the m e t a l l o p o r p h y r i n is a 15-bond route to the Z n atom t h r o u g h H i s 18 that i n c l u d e s a 1.85-Â h y d r o g e n b o n d b e t w e e n the P r o 30 c a r b o x y l oxygen a n d the p r o t o n o n the H i s 18 n i t r o g e n . T h e shortest p a t h w a y from H i s 39 is a 12-bond route that i n c l u d e s a 2 . 4 - A H b o n d b e t w e e n the α-amino h y d r o g e n atom o f G l y 41 a n d the c a r b o x y l o x y g e n of a p r o p i o n a t e side c h a i n o n the p o r p h y r i n . T h e k e y difference b e t w e e n these t w o pathways is that the H i s 39 pathway is b u i l t f r o m 11 covalent bonds a n d 1 H b o n d ; the H i s 33 pathway i n c l u d e s 14 covalent bonds a n d 1 H b o n d (30). H e n c e , the e x p e r i m e n t a l observation that the e l e c t r o n i c c o u p l i n g is stronger i n the H i s 39 d e r i v a t i v e t h a n i n the H i s 3 3 - m o d i f i e d p r o t e i n (even t h o u g h the e d g e - e d g e distances i n the t w o m o d i f i e d p r o t e i n s are r o u g h l y the same) is consistent w i t h the B e r a t a n - O n u c h i c pathway a n a l ysis.



12.

T H E R I E N ET AL.


197

Figure 3. Possible ET pathways from His 62 to the heme in cytochrome c (30). The His 62-heme edge-edge distance is 15.5 À (see Figure 2 legend).

Tunneling Pathways T h e analysis suggests that there are two comparable t u n n e l i n g pathways for R u ( H i s 62)Zn cyt c ( F i g u r e 3). O n e is a 17-bond route w i t h 14 covalent b o n d s a n d 3 H bonds (the t h i r d of w h i c h connects the T r p 59 n i t r o g e n a t o m to the c a r b o n y l oxygen of the h e m e propionate side chain); the o t h e r is a 1 3 - b o n d route w i t h 12 covalent bonds a n d a through-space i n t e r a c t i o n b e t w e e n the sulfur atom of M e t 64 a n d the h e m e edge (30). T h e s h a r p l y l o w e r e l e c t r o n i c c o u p l i n g i n the H i s 62 p r o t e i n relative to b o t h the H i s 33 a n d H i s 39 systems indicates that n e i t h e r the 17-bond n o r the 13-bond p a t h w a y is v e r y good. T h e 13-bond p a t h w a y is the most d i r e c t route, a finding that suggests that the M e t 6 4 - h e m e through-space i n t e r a c t i o n is a p o o r shortcut. A n a m i n o a c i d w i t h an aromatic g r o u p or a sulfur atom i n the p a t h w a y does not n e c essarily enhance the d o n o r - a c c e p t o r e l e c t r o n i c c o u p l i n g . A l t h o u g h the decay of a t u n n e l i n g e l e c t r o n wave f u n c t i o n m i g h t be slow across an aromatic g r o u p , m i x i n g of the wave f u n c t i o n onto a n d off of this group m a y i n fact b e q u i t e unfavorable (30). E x p e r i m e n t s w i t h systematic variations i n t u n n e l i n g pathways a n d t u n n e l i n g m e d i u m energetics s h o u l d f u r t h e r clarify the possible roles that through-space interactions a n d h y d r o g e n bonds play i n b i o l o g i c a l E T reactions.


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Acknowledgments


W e thank D a v i d B e r a t a n for h e l p f u l discussions. B o t h M . J . T h e r i e n ( N a t i o n a l Institutes o f H e a l t h ) a n d Β. E . B o w l e r ( M e d i c a l R e s e a r c h C o u n c i l of Canada) a c k n o w l e d g e postdoctoral fellowships. Research at the C a l i f o r n i a Institute of T e c h n o l o g y was s u p p o r t e d b y the N a t i o n a l S c i e n c e F o u n d a t i o n ( C H E 8 8 - 2 2 9 8 8 ) a n d the N a t i o n a l Institutes of H e a l t h ( D K 1 9 0 3 8 ) . R e s e a r c h p e r f o r m e d at B r o o k h a v e n N a t i o n a l L a b o r a t o r y was c a r r i e d out u n d e r C o n tract D E - A C 0 2 - C H 0 0 0 1 6 w i t h the U . S . D e p a r t m e n t of E n e r g y a n d s u p p o r t e d b y its D i v i s i o n of C h e m i c a l Sciences, Office of Basic E n e r g y Sciences.

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