Electron Transfer in Biology and the Solid State - American Chemical

4 Directional Electron Transfer

Downloaded by IOWA STATE UNIV on September 27, 2013 | http://pubs.acs.org Publication Date: May 5, 1989 | doi: 10.1021/ba-1990-0226.ch004

in Ruthenium-Modified Cytochrome c Stephan S. Isied Department of Chemistry, Rutgers, The State University of New Jersey, New Brunswick, N J 08903

Studies of intramolecular oxidation and reduction in cytochrome c complexes covalently modified at the His-33 residue with a variety of ruthenium amine and ruthenium polypyridine complexes are presented. The redox potential of the ruthenium complexes vary over a potential range above and below the redox potential of the native cytochrome c. These studies show that the reduction of cytochrome c with these ruthenium complexes proceeds with a rate-limiting electron-transfer step that changes with the driving force of the reaction, as expected. Oxidation of cytochrome c proceeds with rates significantly lower than those expected on the basis of the driving force of the reaction. A mechanism to interpret the directional electron-transfer behavior of these ruthenium cytochrome c complexes on the basis of conformational changes of the reduced cytochrome c is described.

RAPID ELECTRON TRANSFER CAN BE OBSERVED OVER LONG DISTANCES (~ 1 0 - 2 0 A) (1-11), as s h o w n b y studies o n e l e c t r o n transfer w i t h organic a n d inorganic d o n o r - a c c e p t o r complexes. T h e factors that c o n t r o l t h e rate of e l e c t r o n transfer i n these systems are d r i v i n g force, reorganization e n e r g y , a n d distance a n d orientation.

Polypeptide Donor-Acceptor Complexes I n a n attempt to gain further insight into these factors, w e have s y n t h e s i z e d a n d s t u d i e d a series o f b r i d g e d p o l y p r o l i n e

complexes (12) o f t h e t y p e

[ ( N H 3 ) O s - L - R u ( N H ) 5 ] , w h e r e L (the ligand) is i s n ( P r o ) , i s n is t h e i s o 5

3

5 +

n

n i c o t i n y l g r o u p , a n d n = 0, 1, 2, 3, o r 4 (Table I). 0065-2393/90/0226-0091$06.00/0 © 1990 American Chemical Society

In Electron Transfer in Biology and the Solid State; Johnson, M., et al.; Advances in Chemistry; American Chemical Society: Washington, DC, 1989.

92

E L E C T R O N TRANSFER IN BIOLOGY A N D T H E SOLID STATE

Table I. Rates and Distances of Intramolecular Electron Transfer in [ ( N H ) O s - L - R u ( N H ) ] 3


Complex

5

3

5

5+

Rate Constant, s'

1

Os-Ru Distance, A

N O T E : L is isn(Pro)„, isn is isonicotinyl group, and n — 0, 1, 2, 3, or 4. T h e C - a n d N - t e r m i n a l residues i n T a b l e I are d e r i v a t i z e d w i t h [ ( N H ) R u - ] a n d [ ( N H ) O s i s n - ] , respectively. T h e redox potentials o f the O s ( I I - I I I ) couple a n d the R u ( I I - I I I ) c o u p l e are such that e l e c t r o n transfer i n this series o f complexes occurs from Os(II) —> Ru(III) w i t h a d r i v i n g force of—150 m V (13). I n this series of complexes, the d r i v i n g force (the difference i n redox p o t e n t i a l b e t w e e n t h e R u ( I I - I I I ) a n d the O s ( I I - I I I ) couple) a n d the i n n e r - s p h e r e reorganization energy are k e p t constant, w h i l e the distance b e t w e e n the O s a n d R u centers increases b y 3.2 A p e r p r o l i n e . U n d e r the conditions used to carry out these e x p e r i m e n t s (~0.1 M C F C O O H ) , the p r o l i n e oligomers are p r e d o m i n a n t l y i n the ell-trans configuration a n d t h e r e fore act as a r i g i d spacer separating the m e t a l ions (12). 3

5

n

3

5

n

3

T h e rate of i n t r a m o l e c u l a r electron transfer i n this series of m o l e c u l e s decreases b y m o r e t h a n 8 orders o f m a g n i t u d e as p r o l i n e residues are i n t r o d u c e d . A n a l y s i s o f the t e m p e r a t u r e d e p e n d e n c e o f these rate constants showed that the decrease i n rate w i t h distance i n these m o l e c u l e s is a t t r i b u t e d to b o t h the increase i n outer-sphere reorganization w i t h distance a n d the decrease i n electronic c o u p l i n g b e t w e e n the d o n o r a n d acceptor as p r o l i n e residues are i n t r o d u c e d (12, 13).


4.

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93

Ruthenium-Modified Cytochrome c

Intramolecular e l e c t r o n transfer for the tetraproline c o m p l e x occurs w i t h a rate constant —50 s" at a m e t a l - t o - m e t a l distance o f —21 A (12,14). R a p i d electron transfer at these l o n g distances is o b s e r v e d at v e r y l o w d r i v i n g forces. H e n c e , increasing t h e d r i v i n g force o r decreasing t h e outer-sphere reorganization energy is expected to y i e l d r a p i d i n t r a m o l e c u l a r e l e c t r o n transfer rates at e v e n longer distances. E x t r a p o l a t i o n o f these results i n d i cates that i n t r a m o l e c u l a r electron transfer w i l l b e observable at m e t a l - m e t a l separations o f 3 0 - 4 0 A i n t h e m i l l i s e c o n d t i m e scale. W e are c u r r e n t l y p u r s u i n g this goal b y s y n t h e s i z i n g molecules that have 6 - 1 0 p r o l i n e s sep arating t h e d o n o r a n d acceptor m e t a l ions. Downloaded by IOWA STATE UNIV on September 27, 2013 | http://pubs.acs.org Publication Date: May 5, 1989 | doi: 10.1021/ba-1990-0226.ch004

1

Protein Donor-Acceptor Complexes O n e of the techniques that has l e d to a n e w u n d e r s t a n d i n g of the m e c h a n i s m of e l e c t r o n transfer i n electron-transfer proteins is t h e use o f the p r o t e i n as a d o n o r - a c c e p t o r c o m p l e x b y covalently attaching to these proteins a w e l l d e f i n e d transition m e t a l c o m p l e x that b i n d s to a specific a m i n o a c i d site. A l t h o u g h this t e c h n i q u e h a d b e e n u s e d to m o d i f y ribonuclease (15, 16), t h e synthetic b r e a k t h r o u g h i n m o d i f y i n g c y t o c h r o m e c o c c u r r e d w h e n t h e r e action o f [ ( N H ) R u ( O H ) ] w i t h c y t c was c a r r i e d o u t at h i g h p r o t e i n concentrations w i t h h i g h m e t a l - t o - p r o t e i n m o l a r ratios (17). E x h a u s t i v e c h a r acterization o f this m o d i f i e d p r o t e i n s h o w e d that the r u t h e n i u m is covalently b o u n d to the H i s 33 side c h a i n o f cyt c a n d that the p r o t e i n d i d n o t u n d e r g o any measurable p e r t u r b a t i o n as a result o f the modification (18-20). 3

5

2

2 +

W h e n the m o d i f i e d p r o t e i n is p r e p a r e d i n the Ru(III)cyt c(III) oxidation state a n d t h e n r e d u c e d w i t h a variety of radicals generated b y p u l s e radiolysis techniques (21, 22), i n t r a m o l e c u l a r e l e c t r o n transfer from the r u t h e n i u m site to the h e m e site occurs w i t h a rate constant k = 5 3 s (reduction p o t e n t i a l , E°, for cyt c = 0.26 V a n d E° for [ ( N H 3 ) R u - ( H i s ) ] = 0.10 V s . N H E ) (23, 24). T h e t e m p e r a t u r e d e p e n d e n c e , concentration d e p e n d e n c e , a n d p H d e p e n d e n c e o f this electron-transfer reaction w e r e investigated. T h e results o f this investigation s h o w e d that t h e rate o f e l e c t r o n transfer is i n d e p e n d e n t of concentration a n d m o d e r a t e l y sensitive to t e m p e r a t u r e (enthalpy change A H * — 3.5 k c a l M a n d e n t r o p y change A S * — - 3 9 eu). T h e e l e c t r o n transfer reaction is i n d e p e n d e n t o f p H b e t w e e n p H 5 a n d 9, a n d t h e n increases b e l o w p H 5 as t h e native conformation o f the c y t c changes (23). 1

5

n

n i

1

T h e observation o f i n t r a m o l e c u l a r e l e c t r o n transfer b e t w e e n t h e r u t h e n i u m site a n d t h e h e m e site o c c u r r i n g at distances of 1 2 - 1 5 A ( F i g u r e 1) is e x t r e m e l y significant, because i t represents t h e first observation o f an i n t r a m o l e c u l a r electron-transfer reaction w i t h i n a r u t h e n i u m - m o d i f i e d elec tron-transfer p r o t e i n . T h e m a g n i t u d e o f the rate constant (53 s" ) is s i m i l a r to t h e rate constants for o t h e r d y n a m i c a l processes that are k n o w n to occur w i t h i n t h e native c y t c p r o t e i n . T h i s finding l e d us to question w h e t h e r the u n i m o l e c u l a r rate o b s e r v e d is rate l i m i t i n g i n electron transfer (as i n e q u a 1



94


Ru(NH ) L 3

4

Ru(bpy) L 2

Figure 1. Ruthenium-modified cytochrome c, showing the relative position of the heme and the ruthenium sites. t i o n 1) or i n a protein-associated conformational change (as i n equations 2a and 2b). R n u

where k

ET

c y t c

in J E *

R

u

m

c

y

t

c

i i

(!)

is the rate constant for i n t r a m o l e c u l a r e l e c t r o n transfer. Ru»cyt c Ru *cyt c n

m

111

- H Ru»*cyt c"

1

R u c y t c " (fast) n l

(2a) (2b)

where k is the rate constant for a p r o t e i n conformational change. To answer this question, w e designed a series of r e l a t e d r u t h e n i u m molecules that are m o r e o x i d i z i n g than cyt c a n d w o u l d therefore a l l o w us cc


4.

95


ISIED

to reverse the d i r e c t i o n of electron transfer i n the modified cyt c. T h u s , w e c o u l d change the h e m e of cyt c from an electron acceptor to an electron donor. T h e rationale b e h i n d these experiments is rather s i m p l e . If the u n i molecular rate o b s e r v e d is rate l i m i t i n g i n electron transfer, t h e n oxidation as w e l l as r e d u c t i o n s h o u l d be o b s e r v e d w i t h i n these r u t h e n i u m - m o d i f i e d proteins. T h e r e m a i n i n g part of this chapter describes the results of these e x p e r i m e n t s a n d proposes a k i n e t i c scheme for the electron-transfer reactions of


r u t h e n i u m - m o d i f i e d c y t o c h r o m e c.

Results T h e r u t h e n i u m - m o d i f i e d proteins l i s t e d i n Table II w e r e p r e p a r e d a n d p u rified b y procedures similar to those p u b l i s h e d earlier (19, 23, 25). T h e complexes w e r e characterized b y difference v i s i b l e spectra, c i r c u l a r d i c h r o i s m , t r y p t i c digestion, R u - F e analysis, c y c l i c v o l t a m m e t r y , a n d differential p u l s e polarography. Results of these characterization studies clearly s h o w e d that a l l the r u t h e n i u m complexes w e r e b o u n d to the H i s 33 site a n d that there was no measurable difference i n the conformation of the m o d i f i e d a n d the native proteins. Table II lists the r e d u c t i o n p o t e n t i a l of the r u t h e n i u m a m m i n e site i n the r u t h e n i u m - m o d i f i e d proteins. F o r the b i p y r i d i n e series, the r e d u c t i o n potentials have b e e n obtained o n l y for the c o r r e s p o n d i n g r u t h e n i u m complexes. F i g u r e 1 shows the structure of cyt c a n d the relative positions of the h e m e to the r u t h e n i u m - m o d i f i e d sites. Table I I summarizes the rates of

Table H . Rates of Intramolecular Electron Transfer and Reduction Potential of Ruthenium-Cytochrome c Complexes

Ruthenium-Modified cyt c Native H H cytochrome c c-[(NH )4Ru(OH)]-(II/III) [(NH )5Ru]-(II/III) c-[(NH ) Ru(py)]-(II/III) t-[(NH ) Ru(py)]-(II/III) c-[(NH ) Ru(isn)]-(II/III) t-[(NH ) Ru(isn)]-(II/III) c-[(NH ) Ru(Mepz)]-(II/I) c-[(NH ) Ru(Mepz)]-(II/III) [Ru(bpy) (py)]-(II/I) [Ru(bpy) (im)]-(II/I) [Ru(bpy) (py)]-(II/III) [Ru(bpy) (im]-(II/III) 3

3

3

3

3

3

4

4

4

4

3

4

3

4

2

2

2

2

E°, V 0.26 -0.01 0.13 0.36 0.37 0.44 0.44 -0.02 0.72 -1.3 -1.3 1.1 1.0

Rate Constant, Intramolecular ET, k, s' 1

Direction ofET

—

—

5 x 10 55 2.0 1.5 heme Heme —» Ru Heme —> Ru Ru —» heme Heme —> Ru Ru —» heme Ru - » heme Heme —» Ru Heme - » Ru

N O T E : E° was taken versus the normal hydrogen electrode. E T is electron transfer.


96


i n t r a m o l e c u l a r electron transfer for the r e d u c t i o n a n d the oxidation of cyt c b y these r u t h e n i u m reagents. C h a r t I shows the ligands i n the r u t h e n i u m reagents.


Discussion Table I I shows that the rate of r e d u c t i o n of cyt c can be c h a n g e d b y m o r e than 5 orders of m a g n i t u d e , d e p e n d i n g o n the redox p o t e n t i a l a n d the r e organization energy of the r u t h e n i u m - m o d i f i e d p r o t e i n . T w o types of c o m plexes coordinated to H i s 33 of c y t o c h r o m e c can b e i d e n t i f i e d . I n the the first t y p e , electron transfer takes place f r o m (or to) a r u t h e n i u m t - t y p e orbital. T h i s c o n d i t i o n is t r u e for a l l the oxidation reactions of c y t o c h r o m e c b y the different r u t h e n i u m complexes. 2g

F o r the i n t r a m o l e c u l a r r e d u c t i o n o f c y t o c h r o m e c, the r e d u c i n g agent can be e i t h e r a r u t h e n i u m t m e t a l - c e n t e r e d electron as i n the [ ( N H ) R u L ] ( L is cis o r trans O H " , N H , p y , isn) complexes o r a l i g a n d - c e n t e r e d IT* o r b i t a l as i n the c i s - [ ( N H ) R u ( M e p z ) ] a n d the [ ( b p y ) R u - L ] ( L is p y o r im) complexes. T h e role of the ruthenium(II) attached to the c y t o c h r o m e c is e i t h e r as a r e d u c i n g agent or as a covalent l i n k e r to h o l d the M e p z a n d b p y l i g a n d i n the p r o x i m i t y of the H i s 33 site. T h u s , the distance for electron transfer from these organic radicals to the c y t o c h r o m e closely resembles the distances for r e d u c t i o n from the r u t h e n i u m orbitals. T h e reorganization e n ergy for electron transfer for the l i g a n d - c e n t e r e d reductions c o u l d b e dif ferent from the reorganization energy from the r u t h e n i u m - c e n t e r e d orbitals. T h i s difference s h o u l d be taken i n t o account w h e n c o m p a r i n g rates of r e d u c t i o n of c y t o c h r o m e c from r u t h e n i u m - c e n t e r e d orbitals vs. l i g a n d - c e n t e r e d orbitals. 2 g

3

4

n

3

3

O

4

n

0 ~ Q

\=/

\

py: pyridine

—

N

=

-

O — S

bpy: 2,2'-bipyridine

\ = /

n

2

NH

2

Isn: isonlcotlnamlde

\==/

Mepz: methylpyrazlnlum

N = /

Im: Imidazole

Chart I. Ligands in ruthenium reagents.


4.

97


ISIED

T h e o x i d i z e d ruthenium(III) f o r m of the [ ( N H ) R u - M e p z ] a n d the [(bpy) Ru-L] are i n t r a m o l e c u l a r l y r e d u c e d b y c y t o c h r o m e c to the c o r r e s p o n d i n g ruthenium(II) species (a m e t a l - c e n t e r e d orbital). I n these cases, reorganizational energies of the r u t h e n i u m c e n t e r are associated w i t h the rate of electron transfer. 3

3 +

4

3 +

2

T h e n o v e l p r o p e r t y of the second t y p e , the [ ( N H ) R u - M e p z ] a n d the 3

2


4

n

[ ( b p y ) R u - L ] c y t o c h r o m e c species, is that oxidation to the ruthenium(III) center can be o b s e r v e d , as w e l l as r e d u c t i o n from the l i g a n d - c e n t e r e d r a d icals. T h u s b o t h the oxidation a n d r e d u c t i o n of c y t o c h r o m e c can b e o b s e r v e d from the same inorganic modifier, e v e n t h o u g h it is m e t a l - c e n t e r e d i n one d i r e c t i o n a n d l i g a n d - c e n t e r e d i n the other. C o r r e c t i o n for the r e o r g a n i z a tional energies b e t w e e n the m e t a l center a n d the l i g a n d center allows a d i r e c t comparison of oxidation a n d r e d u c t i o n at these s i m i l a r distances. n

B i n u c l e a r r u t h e n i u m complexes of the b r i d g i n g p y r a z i n e a n d b i p y r i d i n e type can be u s e d to observe m e t a l - c e n t e r e d oxidation a n d r e d u c t i o n . C o m plexes of the type [ ( N H ) O s - L L - R u ( N H ) - L - ( O H ) ] (where L L is p y r azine a n d L is 4,4'bpy) have m u l t i p l e o x i d a t i o n - r e d u c t i o n properties that w i l l a l l o w the oxidation a n d r e d u c t i o n of c y t o c h r o m e c to m e t a l - c e n t e r e d orbitals. I n these cases, c o r r e c t i o n for reorganizational energies because of the o r i g i n of the o r b i t a l for the electron-transfer reaction w i l l not b e necessary. 3

5

3

4

2

4 / 5 +

"One-Direction" Electron Transfer T a b l e I I shows that the rates of oxidation a n d r e d u c t i o n of c y t o c h r o m e c b y these covalently m o d i f i e d r u t h e n i u m complexes do not p r o c e e d i n a s i m p l e r e v e r s i b l e e l e m e n t a r y step. T h e fact that the rate of i n t r a m o l e c u l a r oxidation of cis- a n d J r a n s - [ ( N H ) R u - L ] ( L is isn) b y c y t o c h r o m e c is m u c h slower than the r e d u c t i o n o f c y t o c h r o m e c w i t h [ ( N H ) R u - ] indicates that m o r e c o m p l e x c h e m i s t r y is associated w i t h e l e c t r o n transfer i n the p r o t e i n . A s sociation of this c o m p l e x i t y w i t h the p r o t e i n rather t h a n w i t h the r u t h e n i u m l a b e l is i n f e r r e d from the variety of r u t h e n i u m complexes that e x h i b i t the same behavior. W e i n t e r p r e t e d this i n 1986 as " d i r e c t i o n a l e l e c t r o n transfer", w h e r e p r o t e i n conformational states play a role i n the i n t r a m o l e c u l a r e l e c tron-transfer reaction (24). 3

4

n

3

5

n

S u b s e q u e n t to o u r w o r k , a paper o n "gated electron-transfer reactions" b y H o f l m a n et a l . (26) was p u b l i s h e d to i n t e r p r e t a r e l a t e d observation i n t h e i r w o r k o n p h o t o i n d u c e d e l e c t r o n transfer i n p r o t e i n electron-transfer complexes. S u t i n et al. (27, i n this volume) w o r k e d out the general t h e o r e t i c a l formalisms for the m a n y possible types of " d i r e c t i o n a l e l e c t r o n transfer". T h i s theoretical w o r k opens u p m o r e avenues for d e s i g n i n g n e w types of d o n o r - a c c e p t o r complexes that exhibit d i r e c t i o n a l electron transfer. T h e c h e m i s t r y of c y t o c h r o m e c can be u s e d to a i d i n the i n t e r p r e t a t i o n of this d i r e c t i o n a l electron transfer i n r u t h e n i u m - m o d i f i e d c y t o c h r o m e c.


98


T h e r e d u c t i o n o f c y t o c h r o m e c w i t h r u t h e n i u m reagents c o v a l e n t l y attached to H i s 33 is d e p e n d e n t o n t h e d r i v i n g force o f t h e reaction. T a b l e I I shows that this rate c a n b e v a r i e d o v e r 5 orders o f m a g n i t u d e b y changes i n t h e r u t h e n i u m complexes. O n t h e other h a n d , t h e i n t r a m o l e c u l a r oxidation o f c y t o c h r o m e c is 4 - 5 orders o f m a g n i t u d e slower than its r e d u c t i o n after correction for d r i v i n g force a n d reorganizational energy. A m e c h a n i s m to i n t e r p r e t these results is s h o w n i n S c h e m e I . T h u s c y t o c h r o m e c is r e d u c e d to a n activated i n t e r m e d i a t e , c y t c* , w h i c h undergoes a conformational change to t h e stable form o f c y t c . T h e r e f o r e , i n t h e r e d u c t i o n o f c y t c w e measure the rate o f formation o f this activated i n t e r m e d i a t e , k . F o r t h e oxidation o f c y t o c h r o m e c, t h e p r e - e q u i l i b r i u m to f o r m t h e same activated i n t e r m e d i a t e is r e q u i r e d first. T h i s r e q u i r e m e n t depresses t h e o b s e r v e d rate of i n t r a m o l e c u l a r oxidation to k_ /K , a n d therefore w e observe a s i g n i f i cantly decreased i n t r a m o l e c u l a r rate o f oxidation for t h e c y t o c h r o m e c. T h i s m e c h a n i s m is o n e of m a n y that can b e u s e d to i n t e r p r e t t h e o b s e r v e d results. T h e attractiveness o f this m e c h a n i s m is its s i m p l i c i t y . O t h e r m e c h a n i s m s i n v o l v i n g m o r e intermediates a n d associated rate constants c a n also b e u s e d to i n t e r p r e t t h e results. n i

11

11


x

x

eq

A n o t h e r attractive feature o f this m e c h a n i s m is that i t is v e r y s i m i l a r to the mechanisms p r o p o s e d for e l e c t r o n transfer at s o l i d electrodes. I n t h e language o f e l e c t r o c h e m i s t r y , t h e m e c h a n i s m (Scheme I) is r e f e r r e d to as the E C m e c h a n i s m (i.e., a c h e m i c a l reaction [an e q u i l i b r i u m o r c o n f o r m a tional change, etc.] f o l l o w i n g t h e electron-transfer step i n t h e r e d u c t i o n process). F i n a l l y , i t is o f interest to define t h e m o l e c u l a r event that leads to this conformational change. F u r t h e r w o r k from N M R a n d t i m e - d e p e n d e n t r e s -

Ru

cytc

Ru cytc

^ — • Ru cytc

Forward reaction k

obs

=k

Reverse reaction

Scheme I. Directional electron-transfer mechanism.


4.

ISIED


99


onance R a m a n spectroscopy m i g h t shed l i g h t o n these m o l e c u l a r events. T h e other i m p o r t a n t question that s h o u l d b e addressed is w h e t h e r " o n e d i r e c t i o n e l e c t r o n transfer" can b e o b s e r v e d from different sites of the p r o t e i n surface to the h e m e a n d v i c e versa. C h e m i c a l modification o f c y t o c h r o m e c a n d s i t e - d i r e c t e d mutagenesis experiments are r e q u i r e d to generate specific b i n d i n g sites i n different regions o f the c y t o c h r o m e c so that e x p e r i m e n t s s i m i l a r to the ones o u t l i n e d i n this chapter c a n b e c a r r i e d o u t . C o m p a r i son o f t h e i n t r a m o l e c u l a r oxidation a n d r e d u c t i o n p r o p e r t i e s o f t h e h e m e site from different regions o f t h e p r o t e i n s h o u l d p r o v i d e answers to these questions.

Acknowledgments I a m i n d e b t e d to m a n y collaborators w h o c o n t r i b u t e d significantly to this research: H a r o l d S c h w a r z a n d James W i s h a r t (Brookhaven N a t i o n a l L a b o ratories) for t h e i r collaboration o n the pulse radiolysis w o r k , a n d A . Vassilian, M a r y G a r d i n e e r , R o l f B e c h t o l d , C . K u e h n , a n d M . C h o , from t h e R u t g e r s group. I w o u l d also l i k e to acknowledge h e l p f u l discussions w i t h H . T a u b e , N.

Sutin, C . Creutz, and B . Brunschwig.

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Electron Transfer in Biology and the Solid State - American Chemical

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