The Biological Chemistry of Iron

A Look at the Metabolism of Iron

and Its Subsequent Uses in Living Organisms

Proceedings of the NATO Advanced Study Institute held at Edmonton, Alberta, Canada, August 23 - September 4,1981

edited by

H.BRIAN DUNFORD Dept. of Chemistry, University of Alberta, Edmonton, Canada

DAVID DOLPHIN Dept. of Chemistry, University of British Columbia, Vancouver, Canada

KENNETH N. RAYMOND Dept. of Chemistry, University of California, Berkeley, U.S.A. and

LARRY SIEKER Dept. of Molecular Structure, University of Washington, Seattle, U.S.A.

D. Reidel Publishing Company

Dordrecht Holland / Boston .U.S.A. / London England

Published in cooperation with NATO Scientific Affairs Division

PREFACE

The results of a NATO Advanced Study Institute (ASI) entitled "Coordination Chemistry Environments in Iron-Containing Proteins and Enzymes - Including Smaller Molecules and Model Systems" are summarized in this book. The ASI was held in the Province of Alberta, Canada, from August 23 to September 4, 1981. The first half of the conference was held on the campus of the University of Alberta, Edmonton, and the second half at the Overlander Lodge, Hinton.

Two other conferences had the greatest impact upon the planning for this ASI. One was a NATO ASI held in Tomar, Portugal in September of 1979, entitled "Metal Ions in Biology". Among the organizers for that conference were Allen Hill and Antonio Xavier; we are happy to acknowledge their beneficial influence on our subsequent conference. The other most influential conference was one organized by Ralph Wilkins and Dennis Darnell entitled "Methods for Determining Metal Ion Environments in Proteins" which was held in Las Cruces, New Mexico, U.S.A., January 10-12, 1979. The Las Cruces conference invited lectures were published as Volume 2 of "Advances in Inorganic Biochemistry", G. Eichhorn and L. Marzilli, editors. Most of the physical techniques used to probe metal ion environments are eloquently described in the latter volume. The undersigned organizers for the Alberta ASI made two decisions which shaped its format: first, to narrow the scope of "Metal Ions in Biology" to iron-containing systems. Second, to emphasize a description of the results obtained by investigation of the biological systems, and not the physical techniques used to probe the systems. One exception is Mossbauer spectroscopy, a technique not described in the proceedings of the Las Cruces conference, which is uniquely suited to iron-containing systems. This volume contains an excellent description of both the technique and the type of results which can be obtained from it.

The title of this book "The Biological Chemistry of Iron" is simplicity itself. It also is misleading, because justice to the title would require a monumental multivolume series. Nevertheless, we have used it for the sake of brevity. To the best of our knowledge this volume is the first to attempt to describe in some detail both sides of the story of the biology of iron. One side is the gathering of iron, its storage and transport, in other words the metabolism of iron. The other is the utilization of the iron by living systems. Most animal systems use most of their iron to transport or store oxygen. Myoglobin and hemoglobin immediately come to mind. However, these molecules have been intensively studied and well described elsewhere (see for example "Hemoglobin and Myoglobin in their Reactions with Ligands" by E. Antonini and M. Brunori, North-Holland, Amsterdam - a book which is still of great value although it was published in 1971. We do not mean to imply that research on these molecules is anywhere near complete.) There are many references to hemoglobin in this volume, but we describe in detail a less well-known oxygen transport molecule, hemerythrin. Another well known heme protein, cytochrome o is discussed briefly, but we have concentrated more on the remarkable four-heme molecule cytochrome £3. With these types of decisions the conference was held to a viable two week format.

Most of our interest centered on iron-containing enzymes and model systems, as essential for aerobic life as oxygen transport. It would appear that we may be approaching the point where we have enough structural and mechanistic information to elucidate completely the mechanism of an enzyme reaction. One may judge for oneself how well the criteria of complete mechanistic information as defined by biologists, chemists and/or physicists are being met for the enzymes discussed in this volume. Many important iron enzymes are not discussed; it was our concern to obtain some depth for which we paid a price in breadth of coverage.

The participants at the conference ranged from graduate students to senior investigators, from theoretical chemists to medical doctors, from microbiologists to physicists. The mix of participants was truly interdisciplinary providing an accurate match to the types of research required to push back the research frontier on the biological chemistry of iron.

This book is organized in sections which we describe briefly. Speakers (as distinct from coauthors) are also listed. Section A, the introduction, contains the keynote lecture by Allen Hill. It also contains two lectures which were organized as an "inorganic chemistry teach-in" to review the basic principles of inorganic and physical chemistry which must apply equally to non-biological and biological iron. The first, by Ralph Wilkins, describes ligand reaction dynamics. The second, by Chris Reed, discusses the influence of structure, spin state, ligand equilibria, coordination number, redox potential and oxidation state. The remainder of the book might be summarized as follows. It is concerned with the elucidation of ways in which the biological

environment and the iron (or in a few cases, copper or molybdenum) influence each other according to the basic principles of physics and chemistry. Iron metabolism is summarized in Section B. Robert Crichton describes the iron storage protein, ferritin. The iron transport protein, transferrin, is the topic of Philip Aisen. Ken Raymond and Gunther Winkelmann discuss those unique iron-grabbers for microorganisms, the siderophores, as well as the chemistry of analogous molecules. And last, but not least, Rowe Byers describes iron uptake and distribution in cultured beating heart muscle cells.

Section C is for cytochromes, particularly as viewed using NMR spectroscopy. These are the topic of Antonio Xavier. In Section D, the topic is the oxygen transport molecule, heme-rythrin; the dynamics and mechanisms of its reactions (Ralph Wilkins) and its three-dimensional structure (Larry Sieker and Ron Stenkamp).

The topic of Section E is iron-sulfur centers, clusters and enzymes. We are indebted to Jose Moura for coordinating this section. Jose also gave the introductory talk. Hydro-genases and nitrogenases are described in detail: hydrogenases by Hans Grande and Jean LeGall and nitrogenases by Gees Veeger and Vincent Huynh. In the latter talk, Mossbauer spectroscopy is described.

Section F is for ferrous and ferric hemes. Heme model studies are documented. Magnetic complexities in hemes (Robert Scheldt), resonance energies (Philip George), models for peroxidases and cytochrome P-450 (David Dolphin), theoretical calculations on model cytochrome P-450 (Gilda Loew) and hemes of hydroporphyrins (Chris Chang) provide an excellent background for a look at the heme-containing enzymes themselves.

In the final part, Section G, heme enzymes are the topic. An introduction to the peroxidases is provided by Brian Dunford, Rick Rutter, Ron Wever and Nils Ellfolk. The nature of the ligand in the fifth coordination position of the heme iron of horseradish peroxidase is scrutinized intensively by Gerd LaMar and Teizo Kitagawa, as is Compound I of horseradish and yeast cytochrome o peroxidases by Brian Hoffman. Cytochrome P-450 is the topic for Gerald Wagner and Volker Ullrich. With increasing enzyme complexity, catalase is introduced by Peter Jones. The three-dimensional structure of beef liver catalase is outlined by Nobuo Tanaka and Thomas Reid III. Finally the pi.'ece de resistance of heme enzymes, cytochrome o oxidase is reached. Its subunits (Howard Mason) and EXAFS structural results on its copper (Robert Scott) are the aspects treated here.

Philip George was honorary chairman for the conference. He was the hardest working honorary chairman any of us have seen. Not only did he act as chairman for events, both scientific and social, but he is a contributor to this volume. Our hats are off to you, Philip. The only criticism we can make of your pioneering research is that it was ahead of its time.

Acknowledgements are in order to the following organizations and persons: to the University of Alberta and the Overlander Lodge for providing first-rate conference facilities. In particular we thank Therese Roberts and her helpers at Lister Hall; Stockwell Day, his family and his staff at the Overlander Lodge. The grant from NATO Scientific Affairs Division made the conference possible. In addition, the financial help of the Alberta Heritage Foundation for Medical Research is gratefully acknowledged as well as that from the Natural Sciences and Engineering Research Council of Canada, an anonymous donor and Smith-Klein Pharmaceutical. Social events sponsored by the City of Edmonton Business Development Office, (thank you Al Bleiken and Paul Ouimet) and a hospitality grant from the Province of Alberta contributed in a large way to the success of the conference. A large fraction of this volume was typed in camera-ready form by Lavine Shupenia and Jacki Jorgensen; they now will have an audience of appropriate size to view their handiwork. Special thanks go to Jacki Jorgensen and Dee Dunford who looked after many of the local arrangements.

The Editors: Brian Dunford, Edmonton, Alberta David Dolphin, Vancouver, British Columbia Kenneth Raymond, Berkeley, California Larry Sieker, Seattle, Washington

Ahr, H.J. 413

Aisen, P. 63

Araiso, T. 337

Boelens, R. 337

Braaksma, A. 223

Byers, B.R. 117

Castle, L. 413

Chang, C.K. 313

Chacko, V.P. 357

Cox, P. 117

Crichton, R.R. 45

deRopp, J.S. 357

Dolphin, D. 283

Dunford, H.B. 337

Dunham, W.R. 193

Ellfolk, N. 337

George, P. 273

Grande, H.J. 193,223

Gunsalus, I.C. 405

Haaker, H. 223

Hager, L.P. 337

Harrington, P.C. 145

Hill, H.A.O. 3

Hoffman, B.M. 391

Huynh, B.H. 241

Jensen, L.H. 161

Job, D. 337

Jones, P. 427

Kast, W.M. 337

Kitagawa, T. 375

Kuthan, H. 413

Laane, C. 223

LaMar, G.N. 357

LeGall, J. 207

Loew, G. 295

Mason, H.S. 459

Moura, I. 127,179

Moura, J.J.G. 127,179

Mu'nck, E. 241

Murthy, M.R.N. 439

Nastainczyk, W. 413

Orme-Johnson, W.H. 241

Peck, H.D., Jr. 207

Pudzianowski, A. 295

Raymond, K.N. 85

Reed, C.A. 25

Reid, T.J., III 439

Ricard, J. 337

Robinson, P. 117

Ronnberg, M. 337

Rossmann, M.G. 439

Ruf, H.H. 413

Rutter, R. 337

Santos, M.H. 127

Scheldt, W.R. 261

Sciortino, C.V. 117

Scott, R.A. 475

Sicignano, A. 439

Sieker, L.C. 161

Spangler, D. 295

Stenkamp, R.E. 161

Tanaka, N. 439

Teraoka, J. 375

Tufano, T.P. 85

Ullrich, V. 413

van Dijk, C. 193

Veeger, C. 193,223

Villalain, J. 127

Wagner, G. C 405

Wever, R. 337

Wilkins, R. G. 13, 145

Winkelmann, G. 107

Xavier, A.V. 127

SUBJECT INDEX

apoferritin, analogies with lactate

dehydrogenase 54 electron microscopy

of 53 structure of 48

apoprotein formation 18 aqueous chemistry of iron 63 aromatic nitrogen hetero-

cycles 276 aromaticity of porphyrin

ring 339 Asoomyoetes fungi 107 assembly of cytochrome o

oxidase 459 associative mechanism 14 ATP production,

chemiosmotic model for 65 autoxidation, of

Fe(II) 64 in Thiobaoillus fevvi-

oxidans 65 hemerythrin 152 A. vinelandii ferreoxin 185,189 A. vinelandii nitro-

genase 223 axial ligands, 36

of cytochrome P-450 407 in heme complexes 261 strong field 262

axial ligation, of heme iron 377 influence on Raman

frequencies 381 P and s bonds in 377

azurin, reduction of cytochrome o perox- idase with 351

Ab initio calculations, of resonance energies 278

aconitase, 3Fe-3S centers in 187

active site, of peroxidases, ionizable

groups in 341,348 aerobactin 94,122 aerobic life, key to 459 agrobactin 117,121 alcohols,

from cellulose degrada- tion 208

amino acid sequence, of ferritin 48 of transferrin 69

amino acid substitutions, in cytochromes 134

ammonia, as inhibitor of N2 fixa- tion 227

analytical gel electro- phoresis ,

of cytochrome c oxidase 469 Swank-Munkres procedure for 469

anemia, 46 (see also Cooleys1 anemia)

antiferromagnetic coupling, 27 between metal ions 39

antimicrobial activity, of myeloperoxidase 347

antitumor activity, of bleomycin 66

2A1u and 2A2u orbitals, of porphyrins 385 in chloroperoxidase 334

rate, constants for binding by hemes 318 titration, of cyto- chrome c peroxidase 350

carbonmonoxyhemoglobin 27 carbon tetrachloride

reaction with cyto- chrome P-450 416

carbonyl compound of iron in (-11) oxidation

state 26 catecholate,

iron exchange rates with 103 reaction with ferric ion 86 siderophores 86

cation radical (see also TT

cation radical) in peroxidase compound I 29

catalase, 284 biliverdin complex in 440 catalatic activity of 440 compound I of 428,432 crystal structure of 428,439 description of molecule 441 electron density map for 452 erythrocyte 440 general properties of 430 heavy atom derivatives of 448 heme environment 449

essential residues in 453 heme pocket in 454 hydrogen bonding in 442 iron-porphyrin models for 427,433 kinetics of action of 431 organization of molecule 441 from V e n i o i t t i y m v i t a t e 441,447 peroxidatic activity of 440 proximal phenoxide in 286 quaternary structure in 449 reaction with hydrogen

peroxide 391,427 role of iron coordination

environment in 427 role of protein in 435 secondary structure in 444 subunits of 440 tyrosyl l igand in 439

bacterial ferredoxin 33 bacterial growth, regulation

in oral cavity 347 B as id i o my oe t es fungi 107 beef liver catalase (see also

catalase) structure of 439

binding constants, of CO by hemes 318 of iron by siderophores 94,102

binuclear iron complex in hemerythrin 161,165

bioenergetics of proton pumping 475

biological probes, chromic siderophores as 88

biosynthesis of cytochrome o oxidase 459

bleomycin, antitumor activity of 66

blood transfusion, excess iron from 46

bond lengths, iron-sulfur, in cyto- chromes 133 bonellin,

structure of 314 B . p o l y m i x a ferredoxin 188 bromination reactions of

chloroperoxidase 34>

calcium ions, in horseradish peroxi- dase 339 C a l da r i o my o es fumago,

chloroperoxidase from 343 camphor monoxygenase

cytochrome P-450 as 405 carbanions and carbenes,

from cytochrome P-450 reactions 413

carbon monoxide, binding constants by

hemes 318 binding by hydro-

porphyrins 317 complex, of reduced

cytochrome P-450 406

catalatic action of iron(III) porphyrin

models 433 of catalases 427,440 of chloroperoxidase 343,440

influence of iron coordina- tion on 429 CD spectra (see circular

dichroism spectra) cellular iron metabolism,

model systems for 118 cellulose degradation 207 ceruloplasmin 65 chain reactions catalyzed

by ferrous ion 429 Chang cells,

iron metabolism in 118 chelating agents, 18

for iron overload 85 effect on iron uptake and distribution 121 chelation therapy,

for iron overload 103 chemiosmotic model,

for ATP production 65 chlorination reactions,

of chloroperoxidase 343 chlorins,

iron 313 redox potentials of 325

chloroperoxidase, Ai u and A2 U orbitals in 334 bromination reactions of 343 from C a l d av i o my c es

f i ma go 343 catalatic reaction of 343,440 chlorination reactions of 343 compound I,

comparison to horse- radish peroxidase 334 EPR spectrum of 345 Mossbauer spectrum of 345 coordination reactions

of 343 organic substrate halo- genation by 343 similarities to cyto- chrome P-450 344

C h r o m a t i u m HiPIP 187 chromic,

desferriferrichrome 92 desferriferrichyrin 92 enterobactin 93

ion substitution, in ferrichrome 92 in siderophores 88 circular dichroism spectra,

of cy tochrome c peroxidase 350 citrate,

as iron chelator 107 CO complexes (see carbon

monoxide complexes) cobalt-substitution,

in cytochrome o 134 in cytochrome P-450 406,409

composition of cytochrome c oxidase 460

compound I, of catalase 428,432 chloroperoxidase 334 cytochrome o peroxidase 391 ferryl species in 29 hemoproteins 391 horseradish peroxidase 29,

334,367,391 formation 340 peroxidases 26

compound II, of horseradish peroxidase 29,368 peroxidases 291

conalbumin (see ovotransferrin) conformational changes

of hemerythrin 157 constraint mechanisms for

hemoglobin 39 contact shift in proton

NMR 359 Cooleys1 anemia 86,118 cooperativity,

in hemoglobin 35 coordination chemistry, of

siderophores 85 transition metal ions 25

coordination environment of iron, influence on

catalatic mechanism 429

sequence data and NMR spectra 135

redox potentials of 128 X-ray structures of 128 cytochrome a 32 in cytochrome a oxidase 459,475 cytochrome ay in cytochrome o oxidase 459,475 cytochrome b 9 32,283 heme in 128

in methanogenic bacteria 210 in Desulfovibrio 210

cytochrome £5, 128 deprotonated imidazole

in 357 Raman spectrum of 377

cytochrome &562 > 128 sixth ligand in 132

cytochrome O 9 26,283 cysteinyl residues in 128 in Desulfovibrio 210 electron transfer in 132 ferri- 34 from mammals 134 from Pseudomonas

aeruginosa 131 Raman spectrum of 377 structure 128

cytochrome c2 in Rhodospirillum rubrum 133

cytochrome c 3

from Desulfovibrio species 136,138,211

heme ligands in 132 ligands of iron in 128 redox titration of 136 titration w ith ferredoxin 140

cytochrome c 551 , from Pseudomonas

aeruginosa 131,133 from Pseudomonas

perfeotomarinus 129 redox potentials of 139 reduction of cytochrome

0 peroxidase by 350

copper, atoms in cytochrome a

oxidase 460 chemistry of 12 location in cytochrome o

oxidase 465 natural abundance of 25 I/II redox couple 12

sites, X-ray absorption spectra of 475 copper A and B,

in cytochrome o oxidase 475,483

EXAFS data on 483 coprogen and coprogen B 1.09 core expansion,

in porphyrins 380 core size indicators

in Raman spectra 380 C pastorianum

hydrogenase 214 nitrogenase 224

cosmic abundance, of the elements 4

cross reactions, Marcus theory for 21

crystal field parameters of hemes 32 9

crystal field theory 35 crystal forms,

of cytochrome P-450cam 408 crystal structures, (see also X-ray structures) of catalase 428 of octameric metheme- rythrin 161 cultured heart cells, rat 117 Curie law in rubredoxins 181 C. vinosum nitrogenase 223 CYCAMS 94 cysteinate ligatio n

in ferre doxins 28 in cytochrome P-450 28

cysteinyl residues bound to cytochrome o 128 in cytochrome P-450 408

cytochromes, 30,32 amino acid substitutions

in 134

cytochrome c oxidase, 11 analytical gel electro- phoresis of 469 assembly 459 biosynthesis of 459 catalytic core of 468 composition 460 copper A and B in 483 copper atoms in 460 copper locations in 465 cytochromes a and

in 459 definition of 460 electron transfer by 459 electrophoresis of 466 elution of subunits 469 EPR detectable Cu in

spectra of subunit 1 471 EXAFS of copper sites in 475 and four-electron reduction

of O2 to water 283 heme a in 460,465 heme a3 in 34 and mitochondrial inner

membrane 460 molecular weight 460 multiplicity of subunits 463 photoreduction of 477,481 preparation of native

subunits 467 prosthetic groups in 461 proton pumping by 459 reduction of oxygen by

330,459 sulfur ligands of copper

A in 473 spectra of subunits I

and II 469 subunits of, 459,463

visible spectra of 467,468 nomenclature 465

XAS of copper sites in 476 X-ray absorption edge

spectra of copper sites in 475

cytochrome c peroxidase (see also Pseudomonas cytochrome Q peroxidase and yeast cytochrome a peroxidase) compound I of 340

cytochrome oxidase (see cytochrome o oxidase) cytochrome P-420, Raman spectrum of 338 cytochrome P-450, 26,28,34 from aorta,

comparison to prosta- glandin synthase 423 axial ligands in 407 carbanions and carbenes

from 413 carbonmonoxide complex

of 289,406 cobalt substituted 406,409 cysteinate ligation in 28,408 ENDOR spectrum of 409 enzymatic activity of 299 expoxidation by 287 EPR spectrum of

intermediate species 410 reactive intermediates 416

ferric peroxide complex in 288

hydroxylation by 2 92 isotopic labelling of Fe,

S, N in 406 ligand field parameters

for 419 mammalian, membrane bound 288 mechanism of hydroxylation

by 300 mercaptide axial ligand

in 407 models, 283

mechanism of oxidation by 295

spectra and structure for 299 theoretical calculation on 295

optical spectra of deriva- tives 289

oxene donors, as models for 422

as an oxene transferase 413 oxenoid complex of 421 oxy-form and oxymyo-

globin 289 oxidation of C-H bonds by 287

of Dieldrin by 291

D, sulfurioans Norway 4 and ATCC 7757,

hydrogenase from 212 D . vulgaris

hydrogenase from 193,203,212 dead end adduct 21 deazoflavin F 4 2 O in

methanogenic bacteria 2 10 deferoxamine (see Desferal) definition of

cytochrome 0 oxidase 460 ENDOR 395 formal charge 27 oxidation state 26 redox potentials 30

deoxyhemerythrin, oxygenation of 147

deoxyhemoglobin, 37 R and T states,

Raman spectra of 379,381 deoxymyoglobin

from sperm whale 362 deferoxamine (see Desferal) deprotonated imidazole,

in hemoproteins 358 Desferal 121,122 desferrichrome 94 desferrioxamine 57,94 desulforedoxin

from D. gigas 183 in Desulfovibrio 210

Desulfotomaculum genera as sulfate-reducing bacteria 210 Desulfovibrio gigas,

cytochrome c 3 in 136,138 Desulfovibrio species,

cytochrome C3 in 132 electron carriers in 210 as sulfate-reducing

bacteria 210 hydrogenases 211

deuteroheme, dimerization in 434

substitution in peroxidase 287 Dieldrin,

oxidation by cytochrome P-450 291

cytochrome P-450 (cont.) oxidized states, Fe(IV) in 411 peroxide shunt in 407 primary structure of 407 in prostaglandin bio- synthesis 413 from Pseudomonas putida 32 Raman spectrum of 408 reaction cycle of 406 mechanism 414 with peroxides 414 with prostaglandin endoperoxidase 422 reduced, Raman spectrum of 377 reduction, of polyhalo- genated hydrocarbons by 413 role of thiolate anion

in 290 similarities to chloro-

peroxidase 344 spectra of states 407 structure of 404 thiolate ligand in 28,413 transient intermediates

of 299 two-electron activation

of O2 by 405 X-ray study of 407 cytochrome P-450 cam (see also cytochrome P-450) 288 dissociation of 405 cytoplasmic membrane, proton motive force across 227 cytosol, ferritin in 120,123

d5 ferric ion, in siderophores 88

d orbitals, energy splitting of 35 symmetry properties of 7

D 4h symmetry, in porphyrins 377

D. gigas, 3Fe-3S centers in 185 ferredoxin II 189

2,3-dihydroxybenzoyl deriva- tives ,

as iron chelators 122 2,3-dihydroxybenzoylserine, from hydrolytic degrada- tion of enterobactin 93 dimerization of ferric

hemes 434 dioxygen reduction 10 displacement reaction of Fe-S centers with o-xylydithiol 189 disproportionation reactions

of hemerythrin 155 dissociative mechanism 14 distinguishability,

of transferrin sites 76 dynamic stability

of horseradish peroxi- dase 367

e g symmetry 8 E O , E 0 ’ scales 30 EDTA, as competitor with enterobactin 93 effective nuclear charge 5 electrochemical oxidations

of metalloporphyrins 284 electron carriers

in Desulfovibrio 210 in methanogenic bacteria

210 electron density map,

for catalase 452 electron exchange

mechanisms in cytochromes 135

electron microscopy of apoferritin 53

electron nuclear double resonance (s ee ENDOR)

electron spin resonance (see EPR)

electron transfer, in cytochromes 136 in cytochrome o 132 in cytochrome c oxidase 459 in hemerythrin 145

to nitrogenase 224 reactions, of iron 20 reactions Marcus theory

for 21 vectorial, across membrane 214,219 electronic quadruple inter- action in Mossbauer spectra 244 electronic spectra for model cytochrome P-450 299 electronic spectroscopy for rate measurements on hemerythrin 146 electronic structure, of the heme of cyto- chromes 131 for model cytochrome P-450 299 electrons, low potential, and nitogenase 226 electrophoresis

of cytochrome c oxidase 466 endocytosis 58 ENDOR,

definition 395 description of techniques 395 of nitrogenase 253 of porphyrin ir-cation

radical 286 of cytochorme P-450 409 of horseradish peroxidase

compound I 345,396 of peroxidase compounds

I 391 energy splitting,

of d orbital energies 35 enteric bacteria,

enterobactin as growth factor for 93

enterobactin, 94,117,122 affinity for ferric ion 103 chronic 93 as competitor with EDTA 93 as growth factor 93 hydrolytic degradation of 93 as iron(III) selector 7

on molybdenum of nitro- genase 253

synchrotron radiation for 476 excess iron,

by blood transfusion 46 exchangeable proton

in imidazole 362 5- ex o -hyd r oxy c amp ho r from cytochrome P-450 reaction 405 extended Hiickel calculation

on hemes 327 extended X-ray absorption

fine structure (see EXAFS) extrusion,

of Fe-S centers 189

fatty acids, from cellulose degrada- tion 208 Fe(-It)

oxidation state 26 Fe(I) oxidation state,

in porphyrins 28 Fe(II), 9 autoxidation of 64 complexes 15,22 hydrolysis 66 one-electron energy levels of 8 Fe(III), 9

biliverdin complex in catalase 440

chelators 57 hydrolysis 66 low and high spin 18 one-electron energy

levels of 8 protoporphyrin IX, in

catalase 440 substitution reactions of 17 Fe(IV), in oxidized peroxidases 339 in cytochrome P-450 oxidized states 411 Fe(VI),

in ferrate ion 26

enthalpy of ionization, of iron 6

EPR detectable copper in cytochrome c oxidase 462

EPR spectra, of chloroperoxidase

compound I 345 of cytochrome o oxidase

subunit I 468 of cytochrome P-450

407,410,416 of hemerythrin 146 of hemes 327 of hemin nitr ites 324 of hydrogenases 193 Kramers1 doublet and 247 of nitrogenase 232,241 of perchlorato iron(III)

complexes 263 of peroxidase compounds

I and II 394 of TT-cation radical 325 of Pseudomonas cytochrome

o peroxidase 350 of semi-met anion adducts

of hemerythrin 149 of transferrin using

Cu(II) 70 epoxidation,

of aliphatic hydrocarbons by cytochrome P-450 2 99

by cytochrome P-450 287 erythrocyte catalase 440 erythrocytes,

iron metabolism in 118 eukaryotic

cytochrome O 9 NMR spectra of 131

cytochrome P-450 405 EXAFS,

of copper sites in cytochrome c oxidase 475

of copper A and B 483 of a cytochrome o oxidase 462 fluorescence excitation of 476 Fourier transforms of

data 481 K-absorption edges in 482 of iron core of ferretin 51

Fe-S centers, extrusion and displace-

ment 189 reactions of 180 role in redox processes 180

2Fe-2S (or Fe 2 -S 2 ) centers, 40,179 models for 185 spectral studies of 184

3Fe-3S centers, 179 in aconitase 187 In ferredoxin II 185 in Me t h an os a rc i n a b a rk e r i

ferredoxin 187 in T h e r mus t he r m op h i l i c s ferredoxin 187 4Fe-4S (or Fez r S^

centers 39, 179 4Fe-4S clusters, 34

in hydrogenase 193 Fenton1 S reagent 66 ferrate ion,

oxidation state of 26 ferredoxins, 26

from A . V i ne la nd i i 3 189 from B . p o l y m ix a 188 bacterial 33 cysteinate ligation in 28 in D e s u l f o v i b r i o 210 3Fe-3« centers, 187

in methanogenic bacteria 210 four-iron 30,40 from M. I a e t y l i t i o u s 201 multiple, in De su l f ov i b r i o 217 role in electron transfer

to nitrogenase 224 thiolate binding in 28 as titrant of cytochrome e 3 140

two-iron 30,40 ferredoxin II from D . g i g as 189 3Fe-3S centers in 185 m.c.d. of 186 ferric (see also Fe(III)) fusarinine 90 hemes, 37

coordination environment in 430

dimerization of 434 in peroxidases 338 hydroxide 85 ion, reaction with catecholates and hydroxamates 86 ion, reaction with thio-

hydroxamates 86 low spin complexes, of cytochromes b 5 and c 377 octaethylporphyrin,

Raman spectrum of 37 9 -oxene complex,

in cytochrome P-450 290 oxyhydroxide,

in ferritin 46 -peroxide complex,

in cytochrome P-450 288 tetraphenylporphinato

complexes 262 geometries of 268

tris benzhydroxamato complexes 90

ferrichrome, 85,90 chromic ion substitution

in 92 iron uptake kinetics of 113

ferrichrome A 90,98 ferrichrome A and C 108 ferrichrysin 90,108 ferricrocin 108 ferricytochrome c ,

NMR spectrum of 129,133 ferrihaems (see ferric hemes,

hemes) ferrimycobactin 90 ferrioxamine B, 86

iron removal from 98 ferrioxamine E 90 ferr!protoporphyrin IX,

in peroxidases 338 ferrirhodin 1099 ferrirubin 108 ferritin,

amino acid sequence of 48 in cytosol 120,123 distribution, role in iron metabolism 46

ferritin, (cont.) ferric oxyhydroxide in 46 function of 45 in hepatocytes 47 from horse spleen 46 iron core,

Mossbauer spectrum of 51 role of phosphate in 53 structure of 51

iron, deposition in 54 mobilization from 56 oxidation in 55

magnetic susceptibility of 51

in mucosal cells 46 non-mammalian 46 production 117 structure 45,48 ferrocytochrome O 9

NMR spectrum of 129,133 ferroxidase activity, of iron-binding proteins 64 ferrous (see also Fe(II)) ion and chain reactions 429 low spin complexes of

myoglobin and hemoglobin 377

ferroxidase, 65 activity of iron-binding proteins 64 ferryl species,

in peroxidase compound I 29 five-coordinate

Fe(III) species 262 high spin ferrous porphyrins 361

flavodoxins, in Desulfovibrio 210

role in electron transfer to nitrogenase 224 flavodoxin hydroquinone,

from A. vinelandii 231 as electron donor to

nitrogenase 225 formation 227 oxidation by nitro-

genase 231

flavoprotein, FAD containing, in cyto- chrome P-450 system 405 Fletcher and Huehns

hypothesis 77 fluorescence excitation

of EXAFS spectra 476 force constants, for Urey-Bradley force field 376 formal charge,

definition 27 formation constants,

of iron siderophores 88 four-electron reduction by

cytochrome o oxidase 283 Fourier transforms,

of EXAFS data 481 free radical

of compound I 391 functions of ferritin 45,54 fungi,

iron chelating agents in 107 and iron supply 107

fungicidal activity of myeloperoxidase 347

fusarinin (see fusigen) Fusarium strain,

siderophores from 109 fusigen 109,122

geometrical isomers 89 gingival fluid

of oral cavity 347 ground states

of porphyrins 285

Haber-Weiss reaction 65 haem (see heme) haemoglobin (see hemoglobin) haemosiderin (see hemosiderin) halogenation

by chloroperoxidase 343 heart cells, cultured rat, iron uptake by 117 heavy atom derivatives

of catalase 448

heme complexes axial ligands in 261 with imidazolate 385 of cytochrome c 128 environment, in catalase, 449 essential residues in 453 of cytochrome c peroxidase 393 of hydroporphyrins 313 iron,

axial ligation of 377 ligands,

in cytochrome 132 -linked ionization

in horseradish peroxi- dase 382

distal, in plant peroxidases 375

structural implications of 383 modification,

of cytochrome P-450 406 pocket, in catalase 454 redox potentials, in

cytochromes 132 synthesis,

in reticulocytes 58 of yeast cytochrome c

peroxidase 392 heme a

in cytochrome c oxidase 60 location 465

heme a 3 of cytochrome c oxidase 34

heme c in Pseudmonas cytochrome

c peroxidase 350 hemerythrin,

autoxidation, inf luence of anions on 152

binuclear iron complex in 161 crystal structure of 161 disproportionation reactions

of 155 electron transfer in 145 EPR spectrum of 146 magnetic susceptibility of 162

net redox reactions of 150 oxy- 39 oxygen transport by 161 Raman spectrum of 376 rate measurements on 146 rates of redox reactions 151 spectroscopic studies on 162 substitution reactions

in 145 semi-met adducts of 149 from Thermiste zosterioola

145 hemochromes,

hexacoordinated 322 hemoglobin, 26

carbonmonoxy - 27 constraint mechanisms for 39 cooperativity 10 deoxy-, 37 T and R states, Raman spectrum of 379 ferrous low spin complexes

of 377 heme substituted,

O2 binding by 321 met-, fluoride complex of 37 oxy- 27 Perutz-Hoard trigger

mechanism for 38 synthesis, by reticuloendo- thelial cells 47 tension theory of cooperativity in 35 hemoproteins, action of 357 compounds I in 391 deprotonated imidazole in 358 Raman spectra of 376 hemosiderin 47 hepatic ferritin

in parenchymal cells 47 high potential iron protein (see HiPIP) high spin complexes, Fe(II) 15 Fe(III), 18

protoporphyrin IX in catalase 440 ferrous model compounds 361 octahedral, of Fe(II) 15

high spin complexes, (cont.) rubredoxins 32

HiPIP, 33 from C h r o ma t i u m 187 oxidized 186 role in hydrogenase mechanism 193,205 super-reduced 193,205 homozygous 3-thalassemia

(see Cooleyt S anemia) hormone control, in plants 342 horseradish peroxidase, calcium ions in 339 compound I 2 9,367,391 compared to chloro-

peroxidase 334 compared to cytochrome

o peroxidase 340 ENDOR of 345,396 EPR spectrum of 394 mechanism of formation 340 Mossbauer spectrum of 394 spectra of 340 stoichiometric EPR signal of 397 compound II 29,368 EPR spectra of 394 Raman spectrum of 377 Mossbauer spectrum of 394 dynamic stability of 367 ferrous, Raman spectrum of 384 heme-linked io nization in 382 isoenzymes A and C,

Raman spectra of 382 hydrogen bonding of proximal

imidazole 357 indolepropionic acid as

substrate for 366 labile protons in 367 low-spin cyanide complex

of 368 primary structure of 339 proton NMR spectra of 357 proximal histidine ligand in 382 reduced, proton NMR of 366 resting state of 366 Soret spectrum of 340

horseradish peroxidase (cont.) state of protonation, of proximal histidine in 357

horse spleen ferritin 46 Hiickel calculations, on ferric hemes 263 in hemes 327 hydrogenases

from D. v u l g a r i s 193,203 in D e s u l f o v i b r i o 210 EPR spectra of 199 from M. e l s d en i i 193,203 in methane-forming

bacteria 207 soluble, from Me t ha no -

s a r o i na ba rk e r i 218 in sulfate-reducing bacteria 207 hydrogen bonding, in catalase 442 of proximal imidazole in horseradish peroxidase 357 hydrogen peroxide, reaction, with catalase 391,427 with peroxidases 339 role in TT-cation radical formation 283 hydrogen production, from

hydrogenases 193 hydrodynamic properties

of transferrin 69 hydrolysis, of Fe(II) and Fe(III) 66 hydroporphyrins, hemes from 313 ligand binding by 317 hydroxamate iron exchange rates 103 reaction with ferric ion 86 siderophores 87 hydroxyl radical, 65 role in destruction of invading organisms and xenobiotics 283 hydroxyIation,

mechanism of, by cyto- chrome P-450 299

hyperfine shifts, in proton NMR spectra 359

hypothiocyanite, production in oral cavity 347

imidazolate, as an iron ligand 370 -heme complexes 385

imidazole binding by hydroporphyrins 317 deprotonated, in hemo-

proteins 358 exchangeable proton of 362

immunoprecipitation of radioiron 120

INDO program, for cytochrome P-450 models 299 indole-3-acetate, in plants 343 indolepropionic acid as

peroxidase substrate 366 inhibition

of iron deposition, by transition metals ions 56

of methanogenesis by sulfides 209 inner membrane

and cytochrome o oxidase 460 inner sphere, redox

reactions 19 interchange, associative and

dissociative mechanism 14 intermolecular electron exchange, in cytochromes 136,139 intracellular iron metabol- ism 117 intramolecular electron

transfer, in multiheme cyto- chromes 136 iodination reactions,

of chloroperoxidase 343 iodosyl benzene,

reaction with porphyrins 290 ionizable groups, in active sites of peroxidases 341,348 ionophores,

role in changing membrane potential 227

invading organisms, and polymorphonuclear leukocytes 283 ionization potentials of first row transition elements 5 iron (see also Fe, ferric, ferrous) 3 (I) porphyrins 28 (II)/(III) potentials 30

binding to entero- bactin 7

spin states 262 six-coordinate

species 262 low spin porphyrin

complexes 370 porphyrin models, for

catalase 433 III/IV potential 30,34 (IV) , oxo-complex in

compound I 29 absorption, in humans 117 aqueous chemistry of 63 binding proteins 64

by transferrin 73 chelating agents, of

fungi 107 chelation, 122 by citrate 107 chelators, effect,

on intracellular iron distribution 117 on iron uptake in heart cells 117 chlorins, synthesis of 313 competition for, by siderophores 111 coordination, in catalase 427 core structure, of

ferritin 51 deficiency 46 deposition, i n ferritin 54 distribution, effect

of chelators on 117,121 enthalpy of ionization 6

redox potentials of 25 properties of 63

reduction in ferritin 56 release from transferrin 73 removal from ferrioxamine

B 98 by EDTA 98

role in pathogenicity of bacterial infections 86 sequestering agents for 94 spin states of 25 sublimation energy of 6 -sulfur bond lengths, in cytochromes 133

centers (see Fe-S centers) clusters, in reductases 330 proteins 30,179

Raman spectra of 376 in P-450 system 405 supply, in fungi 107 toxicity, in humans 86

therapeutic agents for 93 transport, in microbial cells 88 in N e u ros po ra o r as s a 113 in P e n i o i l l i i m pa rv i u m 113 -tyrosyl, class of proteins 70 uptake, effect of chelators on 121

in cultured rat heart cells 117

by microorganisms 107 specificity in fungi 107 isobacteriochlorins,

synthesis of 313 isodesmic reactions 275 isomer shift, in Mossbauer

spectra 245 isomorphous replacement,

in catalase 448 isotopic labell ing,

of cytochrome P-450 406 of octaethylporphyrin Ni complex 376

iron (cont.) excess, from blood trans-

fusion 46 exchange, between ferritin

and transferrin 58 in mammals 46 between siderophores 85 kinetics, between

siderophores 96 rates, for catecho- lates and hydroxa- mates 103

of heme in hemoproteins 261 -histidine stretching

frequency 375 -imidazole bonding 361 -Iigand stretching

frequency 381 magnetic anisotropy of 359 metabolism

in Chang cells 118 in erythrocytes 118 intracellular 117 model systems for 118 role of ferritin in 46

mobilization, from ferritin 56 natural abundance of 25 non-biological, oxidation

states in 26 in non-ferritin cytosol

fraction 120,123 overload, 118

chelating agents for 85 chelation therapy for 103 chronic 86 in humans 117,121 syndrome, therapeutic agents for 93

oxidation, in ferritin 55 oxidation states of 25

from (-11) to (VI) 26 and the periodic table 3

pool, intermediate 118 -porphyrin model systems

for catalase 427 Poubaix diagram for 7 radioactive, immunoprecipita-

tion of 120 rates of electron transfer in

reactions of 20

kinetic model, for lacto- and myeloperoxi- dase oxidation of thio- cyanate 347 kinetics, of

catalase action 431 horseradish peroxidase compound I formation 341 iron deposition, in ferri- tin 56 iron exchange between siderophores 96

iron siderophore complexes 88 K-absorption edge,

in EXAFS data 482 Kekule structure, for porphine 273 KramerT s theorem 246 Kupfer cells, in liver 47

labile protons, in horseradish peroxidase 367

lactate, from cellulose degradation 208

lactate dehydrogenase, analogies with apoferritin 54

lactoferrin 68,75 lactotranferrin 68 l^ctoperoxidase,

ionizable groups in active site of 348

in peroxidation of thio- cyanate 347 laser photolysis

of oxyhemerythrin 148 LFSE (see ligand field

stabilization energy) LICAMS, 94,101,122

55Fe-Iabelled 99 ligand binding,

by iron hydroporphyrins 317 dynamics 25

ligand field 31 parameters, of cytochrome

P-450 complexes 419 stabilization energy 31 strength 36

ligand substitution mechanisms, associate, dissociative and interchange 14 ligands,

of iron, in cytochrome o ^ 128 in low spin cytochrome o 128 soft/hard, characteristics of 31

low spin cyanide complex, of horseradish peroxidase 368 cytochromes, NMR studies on 127 cytochromes O 9 l igands of

iron in 128 Fe(II) 15 Fe(III) 18

ferric iron, in porphyrins 361 model porphyrin complexes of Fe(III) 370 low potential electrons, and nitrogenase 226

M. e l s d en i i f lavodoxin hydroquinone oxidation by nitro- genase 231 hydrogenase 193,203,214 magnetic hyperfine inter- action ,

in Mossbauer spectra 243 properties, of porphinato iron(III) complexes 261 magnetic susceptibility,

of ferritin iron core 51 of hemerythrin 162 of cytochrome P-450 407

mammalian cytochromes o 134 peroxidases 337

polymorphonuclear leukocytes 283 Marcus theory, for electron

transfer reactions 21 marker lines,

for axial l igation 379 for core expansion 379 extreme values for 377 for Raman spectra 376

Methanobaotevium bryantii 217 thermoautobrophicum 218 methanogenic bacteria,

electron carriers in 210 methenogenesis, inhibition by sulfide 209 Methanosaroina 215 barkeri ferredoxin 187 hydrogenase 214 soluble hydrogenase from 218 methemerythrin,

-azide, photochemical reduction of 155 crystal structure of 161 photochemical reduction of 153 reduction of anion adducts

154 methemoglobin,

fluoride complex 37 methydroxyhemerythrin,

structure of complex 166 5-methyl-imidazole, as

iron ligand 370 methyl viologen semiquinone,

oxidation by nitrogen ase 231 metmyoglobin,

cyanide complex 368 microbial

cells, in transport in 88 growth factors, sidero-

phores as 86 iron transport compounds (see siderophores) Miorooooous lactylitious

ferredoxin 201 mitochondrial inner membrane

and cytochrome e oxidase 460 proton transfer acro ss 46 0

mitochondrial structure, and cytochrome c oxidase 459

mixing of spin states 38 model compounds of

2Fe-2S centers 184 cytochrome P-450 295 siderophores 26 catalase 427

marine invertebrate phyla, hemerythrin in 161

MECAM 122 MECAMS, 94,101 potentiometric titration of 95 mechanism of

active oxidizing agent of cytochrome P-450 291

cytochrome P-450 414 electron exchange in

cytochromes 135 horseradish peroxidase

compound I formation 341 interspecies hydrogen

transfer 209 iron binding to trans- ferrin 73 iron release from trans- ferrin 73 oxidation by model cyto- chrome P-450 295 cytochrome P-450 hydroxyla- tion 292 membrane organization, of catalytic core of cyto- chrome e oxidase 468 membrane potential,

cytoplasmic 227 mercaptide-CO complex of protoheme 288 mercaptide ligand, in cyto- chrome P-450 407 mesoporphyrin, in cytochrome c

128 metabolism, of ethanol and CO2 209 of iron 46,117 metalloporphyrins,

electrochemical oxidation of 284

metazidehemerythrin, structure of complex 166

methane formation, from bacteria 207 by cellulose degradation 207

Methanobacillus Omelianski3

metabolism of ethanol and CO2 by 209

model systems for cellular iron meta- bolism 118 models,

for peroxidase and cyto- chrome P-450 283

synthetic, for porphyrins 315 MoFe protein (see nitrogenase) molecular weight, of cytochrome

c oxidase 460 molybdenum-iron protein (see

nitrogenase) monomeric species, of heme-

rythrin 151 monoxygenase, cytochrome P-450

as a 405 Mossbauer spectra,

of chloroperoxidase compound I 345

correlation with EPR spectra 246

of cytochrome P-450 states 407 of ferritin iron core 51 Kramers doublet and 247 of nitrogenase 241 paramagnetic components of

nitrogenase 248 of perchlorato iron(III)

complexes 263 of peroxidase compound I 29 of peroxidase compounds I

and II 394 quadrupole doublets from

nitrogenase 248 of rubredoxin 183 theory for 242

multidentate ligands, substitution by 18

multielectron reductions 330 multiheme cytochromes,

redox equilibria in 136 multiplicity of subunits,

in cytochrome c oxidase 463 myeloperoxidase,

antimicrobial activity of 347 fungicidal activity of 347 ionizable groups in active

site of 348 in leucocytes 283

in neutrophils 347 in peroxidation of thio- cyanate 347 myocytes, cultured rat 117

radioiron uptake in 119 myoglobin, 10

ferrous low spin complexes of 377

heme substituted, O2 binding by 321

reconstituted 322

N,N’,N"-tris(2,3-dihydroxy- 5-sulfobenzoyl)- 1,5,9-cyclotriazatridecane (see CYCAMS) 1,5,10-triazadecane (see

LICAMS) 1,3,5-triaminomethylbenzene (see MECAMS) natural abundance, of Cu and Fe 25 Nernst equations, for multi- heme cytochromes 138 neutrophils,

myeloperoxidase in 347 Neurospora Crassa3

iron transport studies with 113

siderophores from 108 nitric oxide, binding by

hydroporphyrins 317 nitrite ion binding,

by hydroporphyrins 317 nitrite reductases 314,329 nitrogen fixation 224 nitrogenase, 241

from A . vinlandii 250 from C pasteurianum 248 ENDOR study of 253 electron transfer to 224 -enzyme complex components of 242 iron protein (component I)

242 Mo-Fe protein (component II)

242 EPR spectra of 232,241,248

nitrogenase (cont.) EXAFS study of 253

inhibition 229 low-potential reducing equivalent in 223

Mossbauer spectrum of 241 quadrupole doublets of 248 paramagnetic spectrum 248

P-clusters in 253 NMR spectra,

of cobalt-substituted cyto- chrome c 134

correlated with sequence data in cytochromes 135

of cytochrome P-450 states 407 of cytochromes 129 of eukaryotic cytochromes a

131 of ferricytochrome o 129 of ferrocytochrome c 133 of low spin cytochromes 127 proton, of horseradish peroxidase 357 NOE (see nuclear Overhauser effect) non-biological iron, oxidation

states in 26 non-heme iron

dioxygenases, Raman spectra of 376

proteins in D e s u l f ov i bv i o 210 non-mammalian ferritin 46 nuclear charge, effective,

of transition metals 5 nuclear Overhauser effect, 131

in cytochromes 132

O2 binding, by substituted myo- globin and hemoglobin 321

O17 labelling, of horseradish peroxidase compound I 399

octaethylporphinato Ni complex, isotope labelling of 376

octahedral, complexes, of iron 15,22 symmetry 8

octameric species, of hemerythrin 151

one-electron energy levels, of Fe(II) and Fe(III) 8

optical isomers, 89 of tris(hydroxamato) metal complexes 89 optical spectra, of cytochrome P-450 derivatives 289 oral cavity, bacterial growth regula- tion in 347 organic substrate halogena-

tion, by chloroperoxidase 343 outer sphere reactions 19 ovotransferrin 68,75 oxene

donors, as models for cytochrome P-450 422

transfer, in prostacyclin biosynthesis 413 transferase, cytochrome P-450 as 413 oxenoid complex, of cyto- chrome P-450 421 oxidation,

of C-H bonds by cytochrome P-450 287

of Dieldrin, by cytochrome P-450 291 by model cytochrome P-450 295 of tetradeuteronorbornane by P-450 model 291 oxidation-reduction (see redox) oxidation states, definition 26 of ferrate ion 26 and formal charge 27 of iron, 25

from (-II) to (VI) 26 markers, in Raman spectroscopy 376

of non-biological iron 26 oxidized HiPIP 186 oxo-complex, of Fe(IV) in compound I 29 oxy-ferryl nature of compound I 391

oxygen, redox chemistry of 283 singlet 283 transport,

by hemerythrin 161 and respiration 161

oxygenation, of deoxyheme- rythrin 147

oxyhemocyanin, peroxide ion in 27

oxyhemerythrin, 39 laser photolysis of 149

oxyhemoglobin, 27 superoxide ion in 27

oxymyoglobin, and oxy-P-450 279

paramagnetism, in hemoprotein 359

P-cluster, in nitrogenase 253 P e n i c l l i u m p a rv u r r i j iron transport in 113 strain, siderophores from 108 V t t a l e i catalase from 441 peptide mapping, of turnip peroxidases 341 perchlorato iron(III) complexes,

EPR spectra of 263 periodic table, and iron 3 peroxidase, (see also peroxidases) peroxidase compound I Mossbauer spectrum 29 oxyferryl and free radical nature of 391 compounds I and II, descrip- tion of 394 compound II 391 model for 283 proximal imidazole in 286 chloroperoxidase, cytochrome o peroxidase, peroxidases (see also horse- radish peroxidase, lacto- peroxidase, myeloperoxidase, plant peroxidases, P s e ud o mo nas cytochrome o peroxidase, turnip peroxidase, yeast cyto- chrome o peroxidase)

peroxidases, 11,26,337 compound I of 26 Fe(IV) in 339 in mammals 337

peroxidatic activity, of catalase 428,440 of peroxidase 337

peroxidation, of thiocyanate by peroxidases 347 peroxide ion, in oxyheme- rythrin 27 peroxides,

peroxygenase shunt in P-450, induced by 407

reactions with cytochrome P-450 414 Perutz-Hoard trigger

mechanism, for hemog lobin 39 P h aso o l ops i s g o u l d i i ,

hemerythrin from 163 phosphate, role in ferritin

iron core 53 photochemical reduction,

of methemerythrin 153 of methemerythrin-azide

adduct 155 of cytochrome o oxidase 477

physiology, of transferrins 63 Ti-bonding 36 TT-bonds, in axial ligation

of heme iron 377 TT-cation radical,

EPR spectrum of 325 in oxidized peroxidases 283 in peroxidase compound I 29 in porphyrins 283,396

TT-spin density, in porphyrins 359

picket fence porphyrin 39 ping-pong kinetics,

modified, of peroxidases 338 plant hormone control 342 plant peroxidases, 339,341

Raman spectra of 375 plasma copper protein (see

ceruloplasmin) pM values, of ferric sidero-

phores 94,102

polyhalogenated hydrocarbons,

reduction by P-450 413

polymeric iron hydroxides 107

polymers, of iron 51

porphine,

compared to [18] annulene 279

Kekule structure for 273

resonance energies for 273

porphinato (III) complexes,

magnetic complexities in 261

structure of 261

porphyrin

complexes, low-spin Fe (III)

370

ligands 9

p-cation radicals 283,396

in peroxidase compound

I 29

p-spin density 359

porphyrin, picket fence 39

reaction with iodosyl

benzene 290

ring, resonance energy of 339

a spin density 361

porphyrins, (see also porphine)

core expansion in 380

containing iron (I) 28

potentiometric titration, of

MECAMS 95

Poubaix diagram, for iron 7,8

precursor complex 18

primary structure,

of cytochrome P-450 cam 407

of horseradish peroxidase 339

prokaryotic cytochrome P-450 405

prostacyclin,

biosynthesis involving

P-450 413

synthesis, in arterial

walls 422

prostacyclin synthase,

comparison to aorta P-450 423

prostaglandin endoperoxide,

reaction with cytochrome

P-450 422

prosthetic groups, of cytochrome

c oxidase 461

of Pseudomonas cytochrome c peroxidase 350

protein, role in catalase

catalysis 434

protoheme-mercaptide-CO

complex 288

proton motive force,

across cytoplasmic

membrane 227

proton NMR, (see also NMR)

contact shift in 359

hyperfine shifts in 359

of reduced horseradish

peroxidase 366

proton pump,

bioenergetics of 475

proton transfer,

across mitochondrial

membrane 460

protoporphyrin IX

in cytochrome b 128

proximal histidyl residue,

in horseradish peroxi-

dase 357,382

Pseudomonas aeruginosa cytochrome o in 131

cytochrome £551 in 131,133,

139

cytochrome 0 peroxidase

from 349

Pseudomonas cytochrome 0 oxidase, hemes in 313

Pseudomonas cytochrome c peroxidase, 349

circular dichroism spectrum

of 350

CO titration of 350

prostheticgroups in 350

reduction by azurin 351

reduction with cytochrome

C 5 5 1 350

Soret spectrum of 350

resonance Raman spectrum

of 350

Pseudomonas perfeotomarinus cytochrome £551 in 130

Pseudomonas putida3

cytochrome P-450 from 405

putidaredoxin, 32

in cytochrome P-450

systems 405

quadrupole doublets, in

Mőssbauer spectra 248

quantum mechanical mixing

in porphyrin ground

states 287

quaternary structure, in

catalase 449

radioiron uptake, by rat

myocytes 119

Raman scattering 375

Raman spectra,

accurate measurement of

small frequency shifts

in 378

core size indicators in 380

of cytochrome P-420 378

of cytochrome P-450 408

of deoxyhemoglobin, T and

R states 379 of ferric octaethylpor-

phyrin 379

of ferrous horseradish

peroxidase 384

of hemerythrin 376

of hemoproteins 376

of horseradish peroxidases

A and C 382

of horseradish peroxidase

compound II 377

influence of axial ligation

on 381

of iron-sulfur proteins 376

marker lines, 376

for axial l igation 379

for core expansion 379

of myoglobin and hemoglobin,

low spin 377

of non-heme iron dioxy-

genases 376

of Pseudomonas cytochrome o peroxidase 350

of plant peroxidases 375

of reduced cytochrome

P-450 377

of transferrin 376

rat myocardial cells,

iron uptake by 119

rate constants,

for CO binding by hemes 319

for electron transfer

reactions of iron 20

rates, of net redox reactions

of hemerythrin 151

reaction cycle,

of cytochrome P-450 406,414

of horseradish peroxidase 337

reactions, of Fe-S centers 180

reconstitution,

of cytochrome P-450, with

modified hemes 406

redox chemistry, of oxygen 283

redox equilibria, in

multiheme cytochromes 136

redox potentials,

of chlorins 325

of Cu(II)/Cu(I) 12

of cytochromes 128

of cytochrome £55^ 139

definition 30

of dithionite/sulfite

complex 229

of Fe(II)/Fe(III) 30

of Fe(III)/Fe(IV) 30

influence of pH on 31

of iron 31

of transition metals 5

redox properties, of iron 63

redox reactions, net,

of hemerythrin 150

redox titration,

of cytochrome £3 136

reduced pyridine nucleotides,

possible role in N2

fixation 224

reductases,

for nitrite 314

reduction,

of methemerythrin-anion

adducts 154

of O2 to water by cytochrome

0 oxidase 459

of protons 207

of sulfate 207

reduction potentials (see

redox potentials)

siderophores, 7 catecholate 87 chromic ion substitution in 88 competition between for

iron 111 complexes, kinetics of 88 coordination chemistry

of 85 d5 ferric ion in 88 formation constants for 88 from different bacterial

strains 108 hydroxamate 87 iron exchange between, 85

kinetics of 86 iron transport by 110 as microbial growth

factors 86 model compounds for 26 pM values for 94,102 specificity of 107 and specificity of iron

uptake by fungi 107 stereoselectivity of

uptake by 113 synthetic analogs for 85 transport system 110

s -bonding 36 s -non bonding 36 s -bonds, in axial ligation

of heme ir on 377 s spin density, in

porphyrins 361 singlet oxygen 283 siroheme, structure of 314 six-coordinate Fe(III)

species 261 sixth ligand, in cytochrome

b 5 6 2 132 soft/hard ligand character-

istics 31 Soret spectra, of

peroxidase compounds 340 of Pseudomorias cytochrome 0 peroxidase 350

specificity, of sidero- phores 107

spectra, of model cytochrome P-450 295

resonance energies, of [18] annulene 273 of benzene 273 of porphine 273 of porphyrin ring 339

resonance Raman spectra (see Raman spectra)

respiration, and oxygen transport in marine invertibrates 161 reticulocyte heme synthesis 58 reticuloendothelial system,

and hemoglobin synthesis 47 Rhodospirillum Tubrum3

cytochrome 02 in 133 Rhodotorula pilimanae,

rhodotorulic acid in 89 Rhodotorula strain

rhodotorulic acid from 109 rhodotorulic acid 57,89,94,109,

122 rubredoxin, 36

and desulforedoxin, compari- son of 183

from C. pasterurianum 181 from D. vulgaris 181 in Desulfovibrio 210 EPR spectrum of 181 high spin 32 Mossbauer spectrum of

ferrous 183 structure of 179 X-ray studies of 181

S 3 / 2 / S 5 / 2 mixing of states 38 saturation kinetics 15 schizokinen 122 secondary structure, of

catalase 444 sequence data, of

cytochromes 135 sequestering agents, for

iron 94 serum transferrin 72 sideramines (see sidero-

phores) siderochromes (see

siderophores)

spectral studies, on 2Fe-2S centers 184

spectroscopic studies, on hemerythrin 162

spin-lattice relaxation times, in cytochromes 135

spin state mixing 38 spin states, of iron 25 splitting, of d orbital

energies 35 stabilization energies,

of ligand fields 31 resonance 273

standard reduction potentials (see redox potentials)

stereochemical probes, chromic siderophores as 89

stereoselectivity, of sidero- phofe uptake 113

stretching frequency, of iron-histidine bond 375 of iron ligand bond 381

structure, of apoferritin 48 beef liver catalase 439 binuclear complex of

hemerythrin 165 bonellin 314 cytochrome o 128 cytochrome P-450 405 ferritin 45,48 ferritin iron core 51 model cytochrome P-450 295 porphinato iron(III)

complexes 261 siroheme 314

yeast cytochrome c peroxidase 392 structural control,

of heme redox potentials 132 structural studies, by NMR

of cy tochromes c 133 sublimation energy, of

iron 6 substitution, mechanism 13

by multidentate ligands 18 reactions of Fe(II) 16 reactions of Fe(III) 17 of hemerythrin 145,147

subunit nomenclature, in cy tochrome c oxidase 4 65

subunits, of beef liver catalase 440 of cytochrome c oxidase

459,463 native, of cytochrome o oxidase, preparation of 467 successor complex 18 sulfate reducing bacteria, from Desulfovibrio genera 209 from Desulfotonaculum genera 209 sulfate reduction, by bacteria 207 and relation to proton reduction 207 sulfide inhibition,

of methanogenesis 209 sulfite reductase, 329

prosthetic group in 314 sulfur ligands, of CuA in cytochrome a oxidase 475 superoxide dismutase 11 superoxide ion, in chain reactions 429 in oxyhemerythrin 27 Swank-Munkres procedure, for analytical gel electrophoresis 469 symmetry, D4h, in porphyrins 377 of octahedral orbitals 8 properties, of d orbitals 7 synchrotron radiation,

for EXAFS st udies 476 synthesis, of porphyrin models 315 synthetic analogs, for siderophores 85

t2g symmetry 8 tetradeuteronorbornane oxidation by cytochrome P-450 291

-ferritin iron exchange 58 Fletcher and Huehns

hypothesis for 77 hydrodynamic properties

of 69 interaction with cells 73 mechanism of

iron binding by 73 iron release from 73

Raman spectrum of 376 structure of 75 two-domain hypothesis

for 75 transient intermediates,

in cytochrome P-450 reactions 299

transition elements, ioniza- tion potentials of 5

transition metal ions, inhibition of iron deposition by 56

transition metals, redox potentials of 5

triacetylfusarinin (see triacetylfusigen)

triacetylfusigen 109 tricatechoylamide sequester-

ing agents, 101 for iron 94

tris (tricatecholato)- chromium(III), as model for enterbactin 92

tris(hydroxamato) metal complexes y isomers of 89

trigger mechanism, for hemoglobin 39

turnip peroxidases, 341 compound I formation in 342 peptide mapping in 341 role in controlling indole-3-acetate 342

two-domain hypothesis, of transferrin structure 35

two-electron activation of O2 by cytochrome P-450 405

tyrosine, as proximal ligand in catalase 439

tetraphenylporphyrins, 29,38,40

tension theory, of cooperativity in hemo- globin 35 T h e mi s t e d y Q c v i t w f i 5

octameric hemerythrin in 163 theoretical calculations,

on cytochrome P-450 models 295 of spectra and structure of P-450 models 299 therapeutic agents,

for acute iron toxicity 93 for iron overload syndrome 93

T h ev m is t e Z os t ev i c o l a i

hemerythrin in 145 T h ev mus t h evm o ph i l us 3

ferredoxin from 187 T h i ob ao i l l us f evv i ox i dans 3

autotoxidation of Fe(II) in 65

thiocyanate peroxidation, by lacto- and myelo- peroxidase 347 thioether linkages,

to iron of cytochrome o 128 thiohydroxamates, reaction

with ferric ion 86 thiolate anion, role in

cytochrome P-450 2 90 thiolate binding,

in cytochrome P-450 28,143 in ferredoxins 28

three-dimensional model, of crystal structure of octameric hemerythrin 161 three-dimensional structure,

(see also structure) of beef liver catalase 439

titration of cytochrome c 3

with ferredoxin 140 TPP (see tetraphenylporphyrins) transferrin, 18,46,57,67,118

amino acid composition and sequence in 69

chemistry and physiology of 63

distinguishability of the sites in 76

EPR spectrum of 70

Urey-Bradley field, force constants for 376

Us t i Za go strain, sidero- phores from 108

vibrational frequencies, of ground electronic states

376 visible spectra,

of cytochrome o oxidase subunits 467,468

of rubredoxin 183

XAS, of copper in cytochrome o oxidase 476

xenobiotics, and mammalian polymorpho- nuclear leukocytes 283 X-ray absorption edge

spectroscopy, of cyto- chrome o oxidase 461

of copper sites in cyto- chrome o oxidase 475 X-ray absorption spectro- scopy (see XAS) X-ray diffraction study,

of cytochrome P-450 cam 407 X-ray structure, of (see also

structure) A . v i n e l a n d i i ferredoxin 189 catalase 428 beef livep catalase 439 cytochrome c peroxidase 392 cytochromes 128 porphinato iron(III)

complexes 264 rubredoxin centers 181

yeast cytochrome c peroxidase, 10

compound I in, 391 ENDOR and EPR of 400 EPR and Mossbauer of 395 and metmyoglobin, compari- son of 393 heme of 392 properties of 392