Active Sites of Binuclear IronâOxo Proteins - ACS Symposium Series

Chapter 8

Active Sites of Binuclear Iron—Oxo Proteins

Downloaded by CORNELL UNIV on October 16, 2016 | http://pubs.acs.org Publication Date: June 21, 1988 | doi: 10.1021/bk-1988-0372.ch008

Lawrence Que, Jr., and Robert C. Scarrow Department of Chemistry, University of Minnesota, Minneapolis, MN 55455 The binuclear iron unit consisting of a (μ-oxo(or hydroxo))bis(μcarboxylato)diiron core is a potential common structural feature of the active sites of hemerythrin, ribonucleotide reductase, and the purple acid phosphatases. Synthetic complexes having such a binuclear core have recently been prepared; their characterization has greatly facilitated the comparison of the active sites of the various proteins. The extent of structural analogy among the different forms of the proteins is discussed in light of their spectroscopic and magnetic properties. It is clear that this binuclear core represents yet another structural motif with the versatility to participate in different protein functions.

A binuclear iron unit has recently emerged as a potential common structural feature of the active sites of several binuclear iron proteins, namely, hemerythrin (1), ribonucleotide reductase (2), and the purple acid phosphatases (3). Such proteins are characterized by strong antiferromagnetic coupling (-J > 100 c m for H = -2 JS] S2) between the iron centers in their Fe(III)-Fe(III) forms and EPR signals with gav values « 1.7-1.8 in the mixed-valence • Fe(II)-Fe(III) forms (Figure 1). The ^ ^ binuclear iron unit consists of a (|i-oxo(or ? • ? hydroxo))bis()Li-carboxylato)diiron core and | o- **o^ | can be distinguished from other iron * x. ' prosthetic groups such as hemes and ironoô ^ o ^ ' cTô sulfur clusters. The binuclear unit is ' c I c' ' readily recognized as a wedge of the basic IR ^ *o^F'eô" S r ' ferric acetate structure (4) which consists of R ' ° \ y i ' \ a |i3-oxo-triiron core with carboxylates o L o bridging between pairs of iron atoms. -1

R

c

L

F e

% F e

7

c

0097-6156/88/0372-0152$07.75/0 1988 American Chemical Society

Que; Metal Clusters in Proteins ACS Symposium Series; American Chemical Society: Washington, DC, 1988.

8. QUE AND SCARROW

Active Sites of Iron-Oxo Proteins

153


1.72

1.66

1.69

1.92

Figure 1. Characteristic EPR signals of Fe(II)Fe(III) sites in semimethemerythrin (a), semimethemerythrin (b), reduced uteroferrin (c), reduced uteroferrin-molybdate complex (d), reduced bovine spleen purple acid phosphatase (e), reduced component A of methane monooxygenase (f). (Reproduced with permission from ref. 26. Copyright 1987 Elsevier.) R

0


154

M E T A L CLUSTERS IN PROTEINS

Synthetic Analogues The thermodynamic stability of such a binuclear unit has been recently demonstrated by the spontaneous self assembly of the core structure with a number of trigonal face-capping ligands. Complexes of the type [(LFe )20(OAc)2l have been crystallized with ligands such as HBpZ3 (1) (5), tacn (2) (6), and Me3tacn (3) (7,8). With a hexadentate ligand such as 4, a tetranuclear complex is formed with Fe20(OAc)2 units connecting N3 faces of different ligands (9). Relevant structural parameters are compared in Table I. ra


H

1,HBpz

2, tacn (R=H) 3, M e t a c n (R=Me)

3

4,

tpbn

3

Table I. Comparison of Structural and Spectroscopic Parameters of Binuclear Iron Complexes Complex

iFe-u-0(R)

Fe(III)-Fe(III) [(HBpz Fe) 0(OAc)2] (HBpz Fe) 0(02CH)2] [(tacnFe) 0(OAc) ] [(Me3tacnFe)20(OAc)2] [tbpnFe2

Uf Pi 0

The reduced uteroferrin-phosphate complex (Uf Pi) forms immediately and reversibly and becomes oxidized over a period of hours (90). The reversibility of its formation would be consistent with the competitive inhibition, and a ratedetermining oxidation to U f P i would be consistent with the slow loss of enzyme activity. The postulated U f P i would thus be purple and EPR silent. Though the purple color is characteristic of the oxidized form, Antanaitis and Aisen have shown that color and oxidation state in uteroferrin are not necessarily coupled (84). The loss of the EPR signal is more surprising, since a mixed valence state is normally expected to be EPR active. The Mossbauer spectrum of U f P i at 55 K (Figure 6) exhibits two quadrupole doublets with parameters consistent with a high spin Fe(IQ) and high spin Fe(II) formulation (90). The 4.2 K spectrum shows magnetic hyperfine broadening characteristic of a half-integer spin state. These observations r

0

r

r



172

METAL CLUSTERS IN PROTEINS

J

.

J

,

I

"

I

.

I

- 5 - 3 - 1 I 3 Velocity (mm/s)

.

I

L

5

7

Figure 6. Mossbauer spectra of the reduced uteroferrin phosphate complex at 55K (a) and 4.2K (b) and the oxidized uteroferrin-phosphate complex at 4.2K (c). (Reproduced with permission from ref. 90. Copyright 1986 American Society for Biological Chemists.)


8. QUE AND SCARROW

173


demonstrate that the purple and EPR silent complex obtained immediately after addition of phosphate to reduced uteroferrin is indeed U f P i . The EPR silence of this mixed valence complex is still not understood, but a recendy synthesized mixed valence complex has also been found to be EPR silent (22,23). Observations on the interaction of phosphate with the bovine enzyme are somewhat different (89). In the bovine case, the oxidation of the enzyme in the presence of phosphate is slow like that observed for uteroferrin (k = 0.07 mhr ); however, the color change and loss of EPR also follow kinetics similar to the loss of enzyme actvity. A comparison of the Mossbauer parameters of reduced uteroferrin and its phosphate complex shows that phosphate binding perturbs the ferrous center only slightly but significandy affects the ferric center, suggesting that it coordinates to the ferric site (90,92). However, the potentiation of phosphatase oxidation by phosphate has led to the suggestion that phosphate can bind at the Fe(II) site to alter the Fe(III)/Fe(II) redox potential (73,89). In U f P i , the Mossbauer parameters of both iron sites differ significandy from those of oxidized uteroferrin, suggesting that the phosphate may bridge the iron centers in this form. A scheme which accommodates these observations is as follows: ut r


1

0

Fe(,0' Vefll,

r

a

p

i

d

_ ....

....

s

l

o

w

_ . . ^ U . ^ ^

^ ^ s

F

9

W

O OH

It is clear from the foregoing discussion that the terminal ligands in the phosphatases differ somewhat from those found in hemerythrin, but to what extent is the triply bridged diiron unit retained? The analyses of the second-shell E X A F S spectra of bovine (93) and porcine (94) oxidized phosphate complexes have identified Fe-Fe and Fe-P components (Table II). For the bovine enzyme, these scatterers are found at ca. 3 A; for the porcine enzyme, they are found at 3.210.1 A. The Fe-P distances of 3.1 - 3.2 A are consistent with a bridging phosphate ligand. The short Fe-Fe distances observed indicate the participation of at least one single atom bridge. Indeed the distance found for the porcine enzyme is comparable to those observed for metHrN3 and RRB2, suggesting the presence of a triply bridged core structure. Variable temperature magnetic susceptibility experiments on the oxidized phosphate complex from bovine spleen confirm the antiferromagnetic coupling between the iron centers and -J is estimated to be > 150 cm"l (73). Studies on oxidized uteroferrin suggest that -J is at least 40 cm" (77,81). The strong antiferromagnetic coupling found in the oxidized enzymes would argue for an oxo bridge between the metal centers, since only single atom bridges thus far have been shown to give rise to such a strong interaction between iron(III) centers. (A sulfido bridge could mediate such strong coupling, as in |i-sulfidomethemerythrin (35,95), but, unlike ^-sulfidomethemerythrin, the purple acid phosphatases exhibit neither multiple S -»Fe(III) charge transfer transitions in their visible spectra nor Fe-S-Fe vibrations in their Raman spectra that would be expected of a sulfide bridge.) For hemerythrin and ribonucleotide reductase, resonance Raman and E X A F S spectroscopy provide clear evidence for an oxo bridge (31-33,43,45, 62,63,65-67). Surprisingly, such evidence is lacking for the oxidized acid phosphatases. The VFe-O-Fe feature expected at ca. 500 c m has not been observed 1

2_

-1


174


by resonance Raman experiments, despite efforts to find it (73). Its absence can be rationalized by the results from model compound studies which show that the intensity of the VFe-O-Fe feature depends on the nature of the terminal ligands (see Chapter 3 for an in depth discussion). The terminal ligand arrangement in the purple acid phosphatases could conceivably be such as to render only weak enhancement of the VFe-O-Fe feature. EXAFS studies of the bovine (93) and porcine (94) oxidized phosphate complexes also do not provide definitive evidence for an oxo bridge (Table II). The first shell E X A F S spectrum of U f P i (Figure 3) clearly differs from those of metHrN3 and RRB2 in the lack of significant destructive interference at low k values due to a short Fe-0 bond (33). Twocomponent fits of the first shell EXAFS of the bovine and the porcine complexes show a shell at 1.95-1.98 A and another shell at 2.10-2.13 A. The presence of short (1.9 A) Fe-O(tyrosine) bonds may cause sufficient interference to obscure the even shorter Fe-oxo bond (93); perhaps more likely is the participation of hydrogen bonding to the postulated oxo bridge which may lengthen the Fe-oxo bond (94). The resolution of these inconsistencies await further data. The magnetic interactions in the reduced porcine and bovine enzymes are considerably weaker than in the oxidized forms. The temperature dependences of the intensity of the EPR signals afford an estimate of -7 and -5.5 ± 1 c m for the J values of the reduced porcine and bovine enzymes, respectively (73,81). The large shifts observed in the N M R spectra of both enzymes also indicate that the coupling is weak; from the temperature dependence of the isotropic shifts, J is estimated to be ca. -10 c u r for reduced uteroferrin (81). By analogy to the proposed structure for semimetHrN3, the reduced enzymes would have a hydroxo bridge.


0

-1

1

Overview Hemerythrin in its met and oxy forms has been characterized crystallographically to have a (|i-oxo)bis(^-carboxylato)diiron(III) core. From a comparison of spectroscopic and magnetic data, it is clear that the B2 subunit of ribonucleotide reductase has an active site which closely resembles that found in methemerythrin. The purple acid phosphatases may have a similar active site core structure, but one that is modified in some respects. Their active site picture will evolve with further experiments. Other proteins that are likely to contain such an active site include the recendy isolated rubrerythrin (96) and methane monooxygenase (97). Rubrerythrin has been recendy purified from Desulfovibrio gigas and found to have two mononuclear iron sites resembling that of rubredoxin and a binuclear site similar to that of methemerythrin. The binuclear site in rubrerythrin consists of antiferromagnetically coupled high spin ferric centers with large quadrupole splittings. Its biological functional has yet to be determined. The hydroxylase component of methane monooxygenase from Methanobacterium capsulatas Bath is a nearly colorless protein which contains two iron atoms (97). As isolated, it is EPR silent, but yields signals with gav of 1.7-1.8 upon treatment with N A D H (98). The resemblance of these signals to those found for semimethemerythrins and reduced purple acid phosphatases suggests the possibility of a similar triply-bridged diiron unit in methane monooxygenase. With an appropriate modification of the active site, methane monooxygenase may utilize the dioxygen binding chemistry of hemerythrin to effect hydroxylation, by analogy to hemocyanin and tyrosinase which have similar active sites but differing functions (99).


8. QUE AND SCARROW


Acknowledgments This work has been supported by grants from the National Institutes of Health and the National Science Foundation. Robert C. Scarrow is grateful for a postdoctoral fellowship from the American Cancer Society.


References and Notes 1. Klotz, I. M.; Kurtz, D. M., Jr. Accts. Chem. Res. 1984, 17, 16-22 and references therein. 2. Reichard, P.; Ehrenberg, A . Science (Washington, D. C.) 1983, 221, 514519. 3. Antanaitis, B . C.; Aisen, P. Adv. Inorg. Biochem. 1983, 5, 111-136. 4. Cotton, F. A.; Wilkinson, G . Advanced Inorganic Chemistry (4th ed) Wiley:1980; pp. 154-155. 5. Armstrong, W. H.; Spool, A.; Papaefthymiou, G. C.; Frankel, R. B.; Lippard, S. J. J. Am Chem. Soc. 1984, 106, 3653-3667. 6. Wieghardt, K . ; Pohl, K.; Gebert, W. Angew. Chem. Intl. Ed. Engl. 1983, 22, 727. 7. Chaudhuri, P.; Wieghardt, K.; Nuber, B.; Weiss, J. Angew. Chem. Intl. Ed. Engl. 1985, 24, 778-779. 8. Hartman, J. R.; Rardin, R. L.; Chaudhuri, P.; Pohl, K.; Wieghardt, K . ; Nuber, B.; Weiss, J.; Papaefthymiou, G. C.; Frankel, R. B.; Lippard, S. J. J. Am Chem. Soc. 1987. 9. Toftlund, H.; Murray, K . S.; Zwack, P. R.; Taylor, L . F.; Anderson, O. P. J. Chem. Soc. Chem. Commun. 1986, 191-193. 10. Spool, A.; Williams, I. D.; Lippard, S. J. Inorg. Chem. 1985, 24, 21562162. 11. Czernuszewicz, R. S.; Sheats, J. E.; Spiro, T. G . Inorg. Chem. 1987, 26, 2063-2067. 12. O'Connor, C. J. Prog. Inorg. Chem. 1982, 29, 204-283. 13. Armstrong, W. H . ; Lippard, S. J. J. Am Chem. Soc. 1985, 107, 37303731. 14. Murray, K . S. Coord. Chem. Rev. 1974, 12, 1-35. 15. Bertini, I.; Luchinat, C. NMR of Paramagnetic Molecules in Biological Systems, Benjamin/Cummings: Menlo Park, 1986; Chapter 2. 16. Que, L., Jr.; Maroney, M . J. Metal Ions Biol. Syst. 1987, 21, 87-120. 17. Gerloch, M.; McKenzie, E. D.; Towl, A . D. C. J. Chem. Soc. A 1969, 71-. 18. Armstrong, W. H . ; Lippard, S. J. J. Am. Chem. Soc. 1984, 106, 46324633. 19. Murch, B . P.; Bradley, F. C.; Que, L., Jr. J. Am. Chem. Soc. 1986, 108, 5027-5028. 20. Gorun, S. M.; Lippard, S. J. Rec. Trav. Chim. Pays-Bas 1987, 106, 417. 21. Gibson, J. F.; Hall, D. O.; Thornby, J. H . M.; Whatley, F. R. Proc. Natl. Acad. Sci. U. S. A. 1966, 56, 987-. 22 Borovik, A . S.; Que, L., Jr. submitted. 23 Borovik, A . S.; Murch, B . P.; Que, L., Jr.; Papaefthymiou, V.; Münck, E. J. Am. Chem. Soc. 1987, 109, 7190-7191.


175

176



24. 25. 26. 27. 28.

Suzuki, M.; Uehara, A . Inorg. Chim. Acta 1986, 123, L9-L10. Klotz, I. M.; Kurtz, D. M., Jr. Acc. Chem. Res. 1984, 17, 16-22. Wilkins, P. C.; Wilkins, R. G.; Coord. Chem. Rev. 1987, 79, 195-214. Sanders-Loehr, J.; Loehr, T. M. Adv. Inorg. Biochem. 1979, 1, 235-252. a) Stenkamp, R. E.; Sieker, L . C.; Jensen, L . H. J. Am. Chem. Soc 1984, 106, 618-622. b) Stenkamp, R. E.; Sieker, L. C.; Jensen, L . H . Acta Crystallogr. Sect. B 1983, B39, 697-703. 29. Stenkamp, R. E.; Sieker, L. C.; Jensen, L . H.; McCallum, J. D.; SandersLoehr, J. Proc. Natl. Acad. Sci. U.S.A. 1985, 82, 713-716. 30 Sheriff, S.; Hendrickson, W . A.; Smith, J. L . J. Mol. Biol.,1987, 197, 273-296. 31. Hendrickson, W. A.; Co, M. S.; Smith, J. L.; Hodgson, K . O.; Klippenstein, G . L . Proc. Natl. Acad. Sci. U.S.A. 1982, 79, 6255-6259. Hedman, B.; Co, M. S.; Armstrong, W . H.; Hodgson, K . O.; Lippard, S. J. Inorg. Chem. 1986, 25, 3708-3711. 32. Elam, W . T.; Stern, E. A.; McCallum, J. D.; Sanders-Loehr, J. J. Am. Chem. Soc 1982, 104, 6369-6373. 33. Scarrow, R. C.; Maroney, M. J.; Palmer, S. M . ; Que, L., Jr.; Roe, A . L.; Salowe, S. P.; Stubbe, J. J. Am. Chem. Soc 1987, 109, 7857-7864. 34. Dawson, J. W.; Gray, H . B.; Hoenig, H . E.; Rossman, G . R.; Shredder, J. M . ; Wang, R.-H. Biochemistry 1972, 11, 461-465. 35. Maroney, M. J.; Lauffer, R. B.; Que, L., Jr.; Kurtz, D. M., Jr. J. Am. Chem. Soc 1984, 106, 6445-6446. 36. Maroney, M. J.; Kurtz, D. M., Jr.; Nocek, J. M.; Pearce, L . L.; Que, L., Jr. J. Am. Chem. Soc 1986, 108, 6871-6879. 37. Okamura, M. Y . ; Klotz, I. M.; Johnson, C. E.; Winter, M. R. C.; Williams, R. J. P. Biochemistry 1969, 8, 1951-1959. 38. Garbett, K.; Darnall, D. W.; Klotz, I. M.; Williams, R. J. P. Arch. Biochem. Biophys. 1969, 135, 419-434. 39. Clark, P. E.; Webb, J Biochemistry 1981, 20, 4628-4632. 40. Loehr, J. S.; Loehr, T. M.; Mauk, A . G.; Gray, H . B. J. Am. Chem. Soc 1980, 102, 6992-6996. 41. Dunn, J. B . R.; Shriver, D. F.; Klotz, I. M. Biochemistry 1975, 14, 26892694. 42. Kurtz, D. M. Jr.; Shriver, D . F.; Klotz, I. M. J. Am. Chem. Soc 1976, 98, 5033-5035. 43. Shiemke, A . K.; Loehr, T. M.; Sanders-Loehr, J. J. Am. Chem. Soc 1984 106, 4951-4956. 44. Freier, S. M.; Duff, L. L ; Shriver, D. F.; Klotz, I. M . Arch. Biochem. Biophys. 1980, 205, 449-463. 45. Shiemke, A . K.; Loehr, T. M.; Sanders-Loehr, J. J. Am. Chem. Soc 1986 108, 2437-2443. 46. Reem, R. C.; Solomon, E. I. J. Am. Chem. Soc 1984, 106, 8323-8325. 47. Reem, R. C.; Solomon, E . I. J. Am. Chem. Soc 1987, 109, 1216-1226. 48. Elam, W . T.; Stern, E. A.; McCallum, J. D.; Sanders-Loehr, J. J. Am. Chem. Soc 1983, 105, 1919-1923. 49. Babcock, L. M.; Bradic, Z.; Harrington, P. C.; Wilkins, R. G.; Yoneda, G . S. J. Am. Chem. Soc 1980, 102, 2849-2850. 50. Muhoberac, B . B.; Wharton, D. C.; Babcock, L. M . ; Harrington, P. C.; Wilkins, R. G . Biochem. Biophys. Acta 1980, 626, 337-345.


8. QUE AND SCARROW 51. 52. 53. 54. 55. 56. 57. 58. 59.


60. 61. 62. 63. 64.


Wilkins, R. G.; Harrington, P. C. Adv. Inorg. Biochem. 1983, 5, 52-85. Sjöberg, B . - M . ; Gräslund, A . Adv. Inorg. Biochem. 1983, 5, 87-110. Lammers, M.; Follmann, H . Struct. Bonding (Berlin) 1983, 54, 27-91. Stubbe, J.; Ator, M.; Krenitsky, T. J. Biol. Chem. 1983, 258, 1625-1630. Ator, M. A.; Stubbe, J.; Spector, T. J. Biol. Chem. 1986, 261, 3595-3599. Sjöberg, B . - M . ; J. Biol. Chem. 1986, 261, 5658-5662. Sjöberg, B . - M . ; Hahne, S.; Karlsson, M . ; Jörnvall, H.; Göransson, M . ; Uhlin, B.-E. J. Biol. Chem. 1986, 261, 5658-5662. Salowe, S. P.; Stubbe, J. J. Bacteriol. 1986, 165, 363-366. Joelson, T.; Uhlin, U . ; Eklund, H.; Sjöberg, B . - M . ; Hahne, S.; Karlsson, M J. Biol. Chem. 1984, 259, 9076-9077. Peterson, L.; Gräslund, A.; Ehrenberg, A.; Sjöberg, B . - M . ; Reichard, P. J. Biol. Chem. 1980, 255, 6706-6712. Land, E. J.; Porter, G.; Strachan, E . Trans. Faraday Soc. 1961, 57, 18851893. Scarrow, R. C.; Maroney, M. J.; Palmer, S. M.; Que, L., Jr.; Salowe, S. P.; Stubbe, J. J. Am. Chem. Soc. 1986, 108, 6832-6834. Bunker, G.; Petersson, L.; Sjöberg, B . - M . ; Sahlin, M.; Chance, M.; Chance, B.; Ehrenberg, A . Biochemistry 1987, 26, 4708-4716. In μ-oxo dimers where the Fe-O-Fe angle is greater than 150°, multiple scattering along the Fe-O-Fe bonds contributes more to the E X A F S spectrum than does single scattering along the Fe-Fe vector. In such cases, the observed Fe-Fe distance (neglecting multiple scattering) is between 3.34 and 3.36 Å, which is twice the Fe-O bond length minus a phase shift factor of 0.22 Ådue to the scattering from the oxygen atoms. Thus we dispute the claim that the determined Fe-Fe distance of 3.26 Åcould be an artifact of multiple scattering. Co, M. S.; Hendrickson, W. A.; Hodgson, K . O.; Doniach, S. J. Am. Chem. Soc 1983, 105, 1144-1150. Sjöberg, B . - M . ; Loehr, T. M.; Sanders-Loehr, J. Biochemistry 1982, 21, 96-102. Sjöberg, B . - M . ; Sanders-Loehr, J.; Loehr, T. M. Biochemistry 1987, 26, 4242-4247. Sahlin, M.; Ehrenberg, A.; Gräslund, A.; Sjöberg, B . - M . J. Biol. Chem. 1986, 267, 2778-2780. Atkin, C. L.; Thelander, L.; Reichard, P.. Lang, G. J. Biol. Chem. 1973, 248, 7464-7472. Barlow, T.; Eliasson, R.; Platz, A.; Reichard, P.; Sjöberg, B . - M . Proc. Natl. Acad. Sci. U.S.A. 1983, 80, 1492-1495. Eliasson, R.; Jörnvall, H.; Reichard, P. Proc. Natl. Acad. Sci. U.S.A. 1986, 83, 2373-2377. Antanaitis, B . C.; Aisen, P.; Lilienthal, H . R. J. Biol. Chem. 1983, 258, 3166-3172. Averill, B. A.; Davis, J. C.; Burman, S.; Zirino, T.; Sanders-Loehr, J.; Loehr, T. M.; Sage, J. T., Debrunner, P. G . J. Am Chem. Soc. 1987, 109, 3760-3767. Hara, A.; Sawada, H.; Kato, T.; Nakayama, T.; Yamamoto, H.; Matsumoto, Y . J. Biochem. (Tokyo) 1984, 95, 67-74. 65

63

65. 66. 67. 68. 69. 70. 71. 72. 73.

74.


111


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75. Ketcham, C. M.; Baumbach, G. A.; Bazer, F. W.; Roberts, R. M. J. Biol. Chem. 1985, 260, 5768-5776. 76. Hunt, D. F.; Yates, J. R., III; Shabanowitz, J.; Zhu, N.-Z.; Zirino, T.; Averill, B. A.; Daurat-Larroque, S. T.; Shewale, J. G.; Roberts, R. M.; Brew, K . Biochem. Biophys. Res. Comm. 1987,144, 1154-1160. 77. Sinn, E.; O'Connor, C. J.; de Jersey, J.; Zerner, B . Inorg. Chim. Acta 1983, 78, L13-L15. 78. Antanaitis, B . C.; Aisen, P. J. Biol. Chem. 1982, 257, 5330-5332. 79. For example: Hefler, S. K.; Averill, B. A . Biochem. Biophys. Res. Comm. 1987, 146, 1173-1177. Sugiura, Y . ; Kawabe, H.; Tanaka, H.; Fujimoto, S.; Ohara, A . J. Biol. Chem. 1981, 256, 10664-10670. Uehara, K . ; Fujimoto, S.; Taniguchi, T. J. Biochem. (Tokyo) 75, 627-638. Uehara, K . ; Fujimoto, S.; Taniguchi, T.; Nakai, K . J. Biochem. (Tokyo) 1974, 75, 639-649. Fujimoto, S.; Nakagawa, T.; Ohara, A . Chem. Pharm. Bull. 1977, 25, 3282-3288. 80. Gaber, B . P.; Sheridan, J. P.; Bazer, F. W.; Roberts, R. M. J. Biol. Chem. 1979, 254, 8340-8342. Antanaitis, B . C.; Strekas, T.; Aisen, P. J. Biol. Chem. 1982, 257, 3766-3770. 81. Lauffer, R. B.; Antanaitis, B . C.; Aisen, P.; Que, L., Jr. J. Biol. Chem. 1983, 258, 14212-14218. 82. Scarrow, R. C.; Que, L., Jr., unpublished observations 83. Antanaitis, B . C.; Peisach, J.; Mims, W. B.; Aisen, P. J. Biol. Chem. 1985, 260, 4572-4574. 84. Antanaitis, B . C.; Aisen, P. J. Biol. Chem. 1985, 260, 751-756. 85. Pyrz, J. W. Ph. D. thesis, Cornell University, 1986. 86. Doi, K.; Gupta, R.; Aisen, P. Rec. Trav. Chim. Pays-Bas 1987, 106, 251. 87. Keough, D. T.; Dionysius, D. A.; de Jersey, J.; Zerner, B . Biochem. Biophys. Res. Comm. 1982, 108, 1643-1648. 88. Antanaitis, B . C.; Aisen, P. J. Biol. Chem. 1984, 259, 2066-2069. 89. Burman, S.; Davis, J. C.; Weber, M. J.; Averill, B . A. Biochem. Biophys. Res. Comm. 1986, 136, 490-497. 90. Pyrz, J. W.; Sage, J. T.; Debrunner, P. G.; Que, L., Jr. J. Biol. Chem. 1986, 261, 11015-11020. 91. Doi, K.; Gupta, R.; Aisen, P. J. Biol. Chem. 1987, 262, 6892-6895. 92. Debrunner, P. G.; Hendrich, M. P.; DeJersey, J.; Keough, D . T.; Sage, J. T.; Zerner, B . Biochim. Biophys. Acta 1983, 745, 103-106. 93. Kauzlarich, S. M.; Teo, B . K.; Zirino, T.; Burman, S.; Davis, J. C.; Averill, B . A . Inorg. Chem. 1986, 25, 2781-2785. 94. Scarrow, R. C.; Que, L., Jr., manuscript in preparation 95. Lukat, G. S.; Kurtz, D. M., Jr.; Shiemke, A . K.; Loehr, T. M.; SandersLoehr, J. Biochemistry 1984, 23, 6416-6422. 96. Huynh, B . H.; Prickril, B., C.; Moura, I.; Moura, J. J. G.; LeGall, J. Rec. Trav. Chim. Pays-Bas 1987, 106, 233. 97. Woodland, M. P.; Dalton, H . J. Biol. Chem. 1984, 259, 53-59. 98. Woodland, M. P.; Patil, D. S.; Cammack, R.; Dalton, H Biochim. Biophys. Acta 1986, 873, 237-242. 99. Himmelwright, R. S.; Eickman, N . C.; Solomon, E. I. J. Am. Chem. Soc. 1979, 101, 1576-1586. Himmelwright, R. S.; Eickman, N. C.; LuBien, C. D.; Lerch, K.; Solomon, E. I. J. Am. Chem. Soc. 1980, 102, 7339-7344. RECEIVED December 18, 1987


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