Lennarz W.J., Lane M.D. (eds.) Encyclopedia of Biological Chemistry. Four-Volume Set . V. 4

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Award of the American Diabetes Association, Fellow of

the American Association for the Advancement of

Science and election to membership in the National

Academy of Sciences.

Paul Modrich

Duke University Medical Center, Durham, NC, USA

Section: Molecular Biology

PAUL MODRICH is an Investigator of the Howard

Hughes Medical Institute and James B. Duke Professor

of Biochemistry at Duke University Medical Center. He

received his undergraduate degree from M.I.T. and his

Ph.D. in Biochemistry from Stanford University. His

current research addresses the mechanisms of DNA

repair. He has served on the editorial boards of the

Journal of Biological Chemistry, Biochemistry, Proceed-

ings of the National Academy of Sciences, and DNA

Repair. His honors include election to National Acad-

emy of Sciences and the Institute of Medicine, the Pﬁzer

Award in Enzyme Chemistry, the General Motors Mott

Prize in Cancer Research, and the Pasarow Foundation

Award in Cancer Research.

ASSOCIATE EDITORS iii

Preface

Biological Chemistry is deﬁned as the chemistry of the

compounds and processesthatconstitute living organisms.

The ultimate goal, of course, is to understand and deﬁne

biology at a mechanistic level. This was aptly stated in an

historical treatise on the founding of the Journal of

Biological Chemistry, where John Edsall quoted a state-

ment in a letter from J. L. Loeb (in Berkeley), “The future

of biology lies with those who attack its problems from a

chemical point of view.” What was an emerging ﬁeld in

1900 with its origins in physiology, nutrition and

chemistry has broadened and expanded to include

numerous other ﬁelds including mechanistic enzymology,

molecular biology, structural biology, cell biology, geno-

mics, proteomics, bioinformatics, metabolomics and

others, that were not deﬁned as discrete ﬁelds at that time.

Modern biochemistry (biological chemistry) began

with the accidental discovery by Eduard Buchner in

1897 that a cell-free yeast extract could carry out

fermentation of glucose to alcohol and CO

in the

absence of intact cells. He named the dissolved

substance responsible for this process zymase, the

substance(s) we now refer to as enzymes. Importantly,

Buchner recognized the signiﬁcance of his discovery.

This ended the dogma of the time, perpetuated by

Pasteur, the concept of vitalism; i.e., that fermentation

(and presumably other complex biological phenomena)

required the action of intact cells. Thus, serendipity and

a prepared mind ushered in a new era of discovery. Now

it became possible to dissect complex physiological

processes and to study them with preparations free of

the constraints of intact cells. Once a metabolic

pathway/process was established, it became possible to

purify the enzymes, cofactors and substrates involved,

to reconstitute the process with puriﬁed components and

to characterize the components chemically. What

followed was an information explosion in the ﬁeld of

biochemistry and progression through a series of trends,

each “in vogue” in its time. The identiﬁcation of the

dietary essentials, the hunt for the vitamins/cofactors,

the hormones, identiﬁcation of metabolic pathways and

the enzymes involved, oxidative phosphorylation, pro-

tein synthesis, molecular biology—each developed as a

primary focus.

The need to associate chemistry with function came

early and was evident in the naming of departments and

journals. Over time names changed from Agricultural

Chemistry to Physiological Chemistry to Biochemistry to

Biological Chemistry. An example is the Department of

Biochemistry at the University of Wisconsin, which began

in 1883 as the Department of Agricultural Chemistry.

Where are we headed? We have reached the point

where the borders of these areas have become blurred.

What constitutes cell biology, molecular biology/

genetics, developmental biology, physiology, immuno-

logy—ultimately reduces to chemistry. To understand

these processes we must know what the molecules are

and understand how they interact, i.e. the basic

chemistry. That is what this encyclopedia is about.

The breadth of content of this encyclopedia aims to

cover major topics of modern biochemistry, each

authored by an expert in the area. We feel that the

coverage is broad and we have been inclusive in choice

of topics. The encyclopedia is a reference work encom-

passing four volumes containing over 500 articles with

more than 750 authors or coauthors. Each article/topic

covers an important area of the ﬁeld which reﬂects the

point of view of the authors. Together the articles cover

virtually every aspect of biology for which we have

“mechanistic” information. For those who wish to

probe more deeply into a topic, references to further

readings are included at the end of each article. The

editorial board that made decisions on coverage consists

of seven members, each an expert representing a major

area in the ﬁeld of biochemistry. A dedicated effort was

made to provide coverage that is as complete as possible.

The content is presented at a level that we hope will be

interpretable to interested individuals with some back-

ground in chemistry and biology. It is intended for such

individuals rather than specialists with extensive scien-

tiﬁc backgrounds in speciﬁc areas. It is aimed at the

generalist as opposed to the specialist.

Finally, we would like to single out Gail Rice and

Dr. Noelle Gracy for their enormous contribution in

putting this encyclopedia together. They, in fact, were a

driving force that brought this major work to

completion.

lxxv

Notes on the Subject Index

Abbreviations used in subentries without explanation:

CoA coenzyme A

DAG diacylglycerol

ELISA enzyme-linked immunosorbent assay

ERK extracellular-signal regulated kinase

GlcNAC N-Acetylglucosamine

HPLC high-pressure liquid chromatography

inositol 1,4,5-triphosphate

MAP mitogen-activated protein

MMP matrix metalloproteinase

mtDNA mitochondrial DNA

NADPH nicotinamide-adenine dinucleotide

phosphate

PFK-2/

FBPase-2

6-phosphofructo-2-kinase/fructose-

2,6-bisphosphatase

PI3K phosphatidylinositol 3-kinase

PIP

phosphatidylinositol 4,5-bisphosphate

PIP

phosphatidylinositol-3,4,5-triphosphate

PPAR peroxisome proliferator-activated receptor

RPLC reversed-phase high-performance

liquid chromatography

Volume 1

ABC Transporters, Pages 1-5, Andre Goffeau, Benoit De Hertogh and

Philippe V. Baret

Abscisic Acid (ABA), Pages 6-11, Ramanjulu Sunkar and Jian-Kang

Zhu

Actin Assembly/Disassembly, Pages 12-18, Henry N. Higgs

Actin-Capping and -Severing Proteins, Pages 19-26, Sankar Maiti

and James R. Bamburg

Actin-Related Proteins, Pages 27-33, R. Dyche Mullins

Adenosine Receptors, Pages 34-39, Lauren J. Murphree and Joel

Linden

Adenylyl Cyclases, Pages 40-45, Ronald Taussig

Adrenergic Receptors, Pages 46-50, David B. Bylund

Affinity Chromatography, Pages 51-56, Pedro Cuatrecasas and Meir

Wilchek

Affinity Tags for Protein Purification, Pages 57-63, Joseph J.

Falke and John A. Corbin

A-Kinase Anchoring Proteins, Pages 64-67, Lorene K. Langeberg and

John D. Scott

Allosteric Regulation, Pages 68-73, Barry S. Cooperman

Alternative Splicing: Regulation of Fibroblast Growth Factor

Receptor (FGFR), Pages 74-77, Mariano A. Garcia-Blanco

Alternative Splicing: Regulation of Sex Determination in

Drosophila melanogaster, Pages 78-84, Jill K. M. Penn, Patricia

Graham and Paul Schedl

Amine Oxidases, Pages 85-89, Giovanni Floris and Alessandro

Finazzi Agro

Amino Acid Metabolism, Pages 90-95, Luc Cynober

Aminopeptidases, Pages 96-98, Ralph A. Bradshaw

Amyloid, Pages 99-104, Ronald Wetzel

Anaplerosis, Pages 105-110, Raymond R. Russell, III and Heinrich

Taegtmeyer

Angiotensin Receptors, Pages 111-115, Tadashi Inagami

ara Operon, Pages 116-119, Robert F. Schleif

ARF Family, Pages 120-122, Gustavo Pacheco-Rodriguez, Joel Moss

and Martha Vaughan

Aspartic Proteases, Pages 123-127, Ben M. Dunn

ATP Synthesis in Plant Mitochondria: Substrates, Inhibitors,

Uncouplers, Pages 128-132, Kathleen L. Soole and R. Ian Menz

ATP Synthesis: Mitochondrial Cyanide-Resistant Terminal Oxidases,

Pages 133-137, James N. Siedow

Autophagy in Fungi and Mammals, Pages 138-143, Daniel J. Klionsky

and Ju Guan

B12-Containing Enzymes, Pages 145-151, Vahe Bandarian and Rowena

G. Matthews

Bax and Bcl2 Cell Death Enhancers and Inhibitors, Pages 152-154,

David L. Vaux

B-Cell Antigen Receptor, Pages 155-158, Thomas M. Yankee and

Edward A. Clark

Bile Salts and their Metabolism, Pages 159-163, Ulrich Beuers and

Thomas Pusl

Biliary Cirrhosis, Primary, Pages 164-169, Marshall M. Kaplan

Bioenergetics: General Definition of Principles, Pages 170-173,

David G. Nicholls

Biotin, Pages 174-178, Steven W. Polyak and Anne Chapman-Smith

Biotinylation of Proteins, Pages 179-181, Ronald A. Kohanski

Bradykinin Receptors, Pages 182-185, Ronald M. Burch

Branched-Chain -Ketoacids, Pages 186-191, David T. Chuang

Brassinosteroids, Pages 192-197, Steven D. Clouse

Cadherin Signaling, Pages 199-204, David B. Sacks and Jonathan M.

G. Higgins

Cadherin-Mediated Cell-Cell Adhesion, Pages 205-211, Frauke Drees

and W. James Nelson

Calcitonin Gene-Related Peptide and Adrenomedullin Receptors,

Pages 212-216, Debbie L. Hay, Alex C. Conner and David R. Poyner

Calcitonin Receptor, Pages 217-220, Samia I. Girgis, Niloufar

Moradi-Bidhendi, Lucia Mancini and Iain MacIntyre

Calcium Buffering Proteins: Calbindin, Pages 221-225, Willi

Hunziker and Igor Bendik

Calcium Buffering Proteins: ER Luminal Proteins, Pages 226-230,

Jody Groenendyk and Marek Michalak

Calcium Oscillations, Pages 231-234, Marisa Brini

Calcium Sensing Receptor, Pages 235-240, Jacob Tfelt-Hansen and

Edward M. Brown

Calcium Signaling: Calmodulin-Dependent Phosphatase, Pages 241-

245, Claude Klee, Hao Ren and Shipeng Li

Calcium Signaling: Cell Cycle, Pages 246-249, Luigia Santella

Calcium Signaling: Motility (Actomyosin-Troponin System), Pages

250-255, Takeyuki Wakabayashi and Setsuro Ebashi

Calcium Signaling: NO Synthase, Pages 256-260, Zhi-Qiang Wang and

Dennis J. Stuehr

Calcium Transport in Mitochondria, Pages 261-266, Rosario Rizzuto

and Marisa Brini

Calcium Waves, Pages 267-269, Lionel F. Jaffe

Calcium, Biological Fitness of, Pages 270-273, Robert J. P.

Williams

Calcium/Calmodulin-Dependent Protein Kinase II, Pages 274-280,

Andy Hudmon and Howard Schulman

Calcium/Calmodulin-Dependent Protein Kinases, Pages 281-286, J.

Robison and Roger J. Colbran

Calcium-Binding Proteins: Cytosolic (Annexins, Gelsolins, C2-

Domain Proteins) , Pages 287-293, Joachim Krebs

Calcium-Modulated Proteins (EF-Hand), Pages 294-299, Robert H.

Kretsinger

Calpain, Pages 300-306, Hiroyuki Sorimachi and Yasuko Ono

Carbohydrate Chains: Enzymatic and Chemical Synthesis, Pages 307-

313, Thomas J. Tolbert and Chi-Huey Wong

Carnitine and -Oxidation, Pages 314-318, Janos Kerner and Charles

L. Hoppel

Caspases and Cell Death, Pages 319-327, Don W. Nicholson,

Pierluigi Nicotera and Gerry Melino

Cell Cycle Controls in G1 and G0, Pages 328-331, WengeShi and

Steven F. Dowdy

Cell Cycle: Control of Entry and Progression Through S Phase,

Pages 332-337, Susan L. Forsburg

Cell Cycle: DNA Damage Checkpoints, Pages 338-344, Jean Y. J. Wang

Cell Cycle: Mitotic Checkpoint, Pages 345-351, Tim J. Yen

Cell Death by Apoptosis and Necrosis, Pages 352-355, Pierluigi

Nicotera

Cell Migration, Pages 356-361, J. Victor Small and Emmanuel Vignal

Cell-Matrix Interactions, Pages 362-366, Janet A. Askari and

Martin J. Humphries

Centromeres, Pages 367-371, Beth A. Sullivan

Centrosomes and Microtubule Nucleation, Pages 372-376, Reiko

Nakajima, Ming-Ying Tsai and Yixian Zheng

c-fes Proto-Oncogene, Pages 377-382, Thomas E. Smithgall and

Robert I. Glazer

Chaperones for Metalloproteins, Pages 383-386, Valeria C. Culotta

and Edward Luk

Chaperones, Molecular, Pages 387-392, Sue Wickner and Joel R.

Hoskins

Chaperonins, Pages 393-398, Arthur L. Horwich, Wayne A. Fenton and

George W. Farr

Chemiluminescence and Bioluminescence, Pages 399-404, Thomas O.

Baldwin

Chemiosmotic Theory, Pages 405-412, Keith D. Garlid

Chemokine Receptors, Pages 413-418, Ann Richmond and Guo-Huang Fan

Chemolithotrophy, Pages 419-424, Alan B. Hooper

Chemotactic Peptide/Complement Receptors, Pages 425-429, Eric R.

Prossnitz and Larry A. Sklar

Chlorophylls and Carotenoids, Pages 430-437, Hugo Scheer

Chloroplast Redox Poise and Signaling, Pages 438-445, John F.

Allen

Chloroplasts, Pages 446-450, Nicoletta Rascio

Cholesterol Synthesis, Pages 451-455, Peter A. Edwards

Chromatin Remodeling, Pages 456-463, Eric Kallin and Yi Zhang

Chromatin: Physical Organization, Pages 464-468, Christopher L.

Woodcock

Chromosome Organization and Structure, Overview, Pages 469-474,

Elena Gracheva and Sarah C. R. Elgin

Coenzyme A, Pages 475-477, M. Daniel Lane

Collagenases, Pages 478-481, Kenn Holmbeck and Henning Birkedal-

Hansen

Collagens, Pages 482-487, Darwin J. Prockop

Cyclic AMP Receptors of Dictyostelium, Pages 488-493, Dale Hereld

and Peter N. Devreotes

Cyclic GMP Phosphodiesterases, Pages 494-500, Sharron H. Francis

and Jackie D. Corbin

Cyclic Nucleotide Phosphodiesterases, Pages 501-505, Vincent C.

Manganiello and Eva Degerman

Cyclic Nucleotide-Dependent Protein Kinases, Pages 506-511,

Sharron H. Francis and Jackie D. Corbin

Cyclic Nucleotide-Regulated Cation Channels, Pages 512-515, Martin

Biel and Franz Hofmann

Cysteine Proteases, Pages 516-520, David J. Buttle and John S.

Mort

Cytochrome b6f Complex, Pages 521-527, Gunter A. Hauska and Thomas

Schodl

Cytochrome bc1 Complex (Respiratory Chain Complex III), Pages 528-

534, Bernard L. Trumpower

Cytochrome c, Pages 535-538, Hans Tuppy and Gunther Kreil

Cytochrome Oxidases, Bacterial, Pages 539-543, Peter Brzezinski

and Pia Adelroth

Cytochrome P-450, Pages 544-549, Rita Bernhardt

Cytokines, Pages 550-555, Andrea L. Wurster and Michael J. Grusby

Cytokinesis, Pages 556-561, Masanori Mishima and Michael Glotzer

Cytokinin, Pages 562-567, Thomas Schmulling

Desmosomes and Hemidesmosomes, Pages 569-576, Rachel L. Dusek,

Jonathan C. R. Jones and Kathleen J. Green

Detergent Properties, Pages 577-581, Darrell R. McCaslin

Diabetes, Pages 582-592, David W. Cooke

Diacylglycerol Kinases and Phosphatidic Acid Phosphatases, Pages

593-597, Stephen M. Prescott and Matthew K. Topham

Disulfide Bond Formation, Pages 598-602, Hiram F. Gilbert

DNA Base Excision Repair, Pages 603-608, Hilde Nilsen and Tomas

Lindahl

DNA Damage: Alkylation, Pages 609-613, Anton B. Guliaev and B.

Singer

DNA Glycosylases: Mechanisms, Pages 614-617, Daniel J. Krosky and

James T. Stivers

DNA Helicases: Dimeric Enzyme Action, Pages 618-623, Timothy M.

Lohman

DNA Helicases: HexamericEnzyme Action, Pages 624-631, Smita S.

Patel

DNA Ligases: Mechanism and Functions, Pages 632-636, Alan E.

Tomkinson and John B. Leppard

DNA Ligases: Structures, Pages 637-643, C. Kiong Ho, Mark Odell

and Dimitar B. Nikolov

DNA Methyltransferases, Bacterial, Pages 644-651, Albert Jeltsch

and Richard I. Gumport

DNA Methyltransferases, Structural Themes, Pages 652-659, Sanjay

Kumar

DNA Methyltransferases: Eubacterial GATC, Pages 660-664, Martin G.

Marinus

DNA Mismatch Repair and Homologous Recombination, Pages 665-670,

Ivan Matic and Miroslav Radman

DNA Mismatch Repair and the DNA Damage Response, Pages 671-674,

Guo-Min Li and Steven R. Presnell

DNA Mismatch Repair Defects and Cancer, Pages 675-681, Richard D.

Kolodner

DNA Mismatch Repair in Bacteria, Pages 682-686, A-Lien Lu

DNA Mismatch Repair in Mammals, Pages 687-690, James T. Drummond

DNA Mismatch Repair: E. coli Vsr and Eukaryotic G-T Systems, Pages

691-693, Margaret Lieb

DNA Oxidation, Pages 694-697, Arthur P. Grollman and Dmitry O.

Zharkov

DNA Photolyase, Pages 698-702, Carrie L. Partch and Aziz Sancar

DNA Polymerase, Eukaryotic α, Pages 703-707, Teresa S. -F. Wang

DNA Polymerase, Eukaryotic β, Pages 708-712, William A. Beard and

Samuel H. Wilson

DNA Polymerase, Eukaryotic δ, Pages 713-715, Antero G. So and

Kathleen M. Downey

DNA Polymerase, Eukaryotic ε, Pages 716-719, Yasuo Kawasaki and

Akio Sugino

DNA Polymerase I, Bacterial, Pages 720-725, Catherine M. Joyce