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Restriction Enzymes: A History

By Wil A.M. Loenen, Leiden University Medical Center
April 2019 · 346 pages, illustrated (38 color and 26 B&W)
ISBN 978-1-621821-05-2

<<  Appendix B   —   Author  >>

References

Page references followed by f denote figures, those followed by t denote tables.

A

AAA+ ATPases, 155

AbaSI, 246

Acinetobacter baumanii, 246

ACNs (anticodon nucleases), 230

AcuI, 129, 130t, 322

Adamczyk-Poplawska, Monika, 252

Adenosine triphosphate. See ATP

Adenovirus, split genes in, 49

AFM. See Atomic force microscopy (AFM)

Agarose slab gel electrophoresis, 52, 66

AgeI, 194t

Aggarwal, Aneel, 79, 128, 134, 138, 205, 236, 238, 241

AhdI, 130t

control by C proteins, 213

recent studies, 294t

recognition sequence, 294t

Alkyladenine glycosylase, 243f

Allelism, of R-M genes, 21–23

AloI, 195

Ames test, 13

Anderson, John, 96

Anticodon nucleases (ACNs), 230

Antirestriction, 230–232, 234–235

Anti-restriction-modification (anti-RM) systems, 230, 235

Antisense RNA, 214

ApeKI, 322

Apoptotic mutual exclusion, 214

Applications of restriction enzymes, modern-day, 317–306

Apyrimidine lyase, 319

Arber, Werner, 228

Arber-Dussoix papers, 17–19

Bertani and, 14

DNA modification, 20–21

E. coli B REase, 20

Edouard Kellenberger and, 35

Hamilton Smith and, 39

host-controlled variation, 1, 6, 8, 15, 17–19

journal club seminar on Watson and Crick model of DNA, 15–17

models for hyphenated and/or palendromic recognition sites, 22–23

Nobel Prize, 1, 6, 33, 35, 40

PhD thesis, 16f, 17

photograph, 16f, 50f, 199f

Thomas Bickle and, 42

transduction by lambda, 12–13

Archaea, 125

ArdA, 223–224, 231–232

effectiveness of inhibition of Type I R-M systems, 234–235

structure, 233, 234f

ArdB, 231–232

effectiveness of inhibition of Type I R-M systems, 234–235

structure, 233–234, 234f

Argonaute proteins, 325

AS1 (Aggravated Sludge 1) bacterial strain, 88

AspBHI, 247

AspCNI

catalytic domains, 193

recent studies, 294t

recognition sequence, 294t

ATAC-seq, 324–325

Atomic force microscopy (AFM), 158

Type I restriction enzymes, 216, 224

Type IIE restriction enzymes, 196, 198

ATP

DNA translocation and, 155–156, 158–159, 227, 253

EcoKI DNA cleavage and, 108

restriction enzyme requirement for, 30–32, 34, 43, 78, 104

Type III enzymes and, 111, 236, 238, 240–241, 253, 307

AvaI, 43

Avery, Oswald, 16

B

Bacillus

B. amloliquefaciens, 134

B. stearothermophiles, 142

B. subtilis

restriction enzymes, 43

subsp. globigii, 134

BspLU11III, 202

m4C modification, 187

Balendiran, Ganesaratinam, 213

BamHI

altering specificity, 127

BamHI–DNA complex, 135, 136f

cloning of, 55, 134

control of restriction, 211, 213

crystal structure, 96–97, 96f

DNA binding, 91, 92

DNA cleavage, 71

DNA interactions, 132

recognition sequence, 53, 53f, 205

restriction folds, 146f

specificity, 138

BamHI (Continued )

stable DNA–protein complexes in absence of Mg2+, 91

structure, 103, 127–128, 134–135, 136f, 146, 186

Barrier to infection, discovery of, 5–8

Base analogs, affect on DNA cleavage of, 100

Base flipping, 3, 128, 186

by MspJI, 246

by PabI, 207

Bases, modified, 186–187

BbsI, 319

BbvCI, 207

recent studies, 294t

recognition sequence, 188, 294t

BcgI, 42–43, 88, 90, 129, 130t

DNA cleavage, 195

recent studies, 294t

recognition sequence, 195, 294t

structure, 129

BcnI

DNA cleavage mechanism, 204

recent studies, 294t

recognition sequence, 204, 294t

subunit/domain composition and cleavage mechanisms, 200

B-DNA, 132, 186, 240

Beadle, George, 17

Benner, Jack, 56

Berg, Paul, 19, 87

Bertani, Elizabeth, 10, 14, 17

Bertani, Giuseppe (Joe)

Arber and, 15, 17

host controlled variation, 5–8, 6f, 10–12, 14

letter to Noreen Murray, 10–13

obituary, 13–14

phage P1 and, 17–18, 77

BfiI, 150

catalytic domain, 191, 193

reaction mechanism, 147

recent studies, 294t

recognition sequence, 294t

BglI, 127, 129, 130t, 147

BglII

cloning of, 55, 134

control by C proteins, 213

DNA interactions, 136f, 137

recognition sequence, 205

specificity, 138

structure, 127–128, 134, 136f, 137

Bickle, Thomas, 42, 231

genetic selection operating at population level, 112, 149

Type I restriction enzymes, 75

Type III restriction enzymes, 79

BioBrick, 318, 319

BisI

recent studies, 295t

recognition sequence, 204, 295t

Bitinaite, Jurate, 57f

BlpI, 188

Blumenthal, Bob, 187, 211

Bordetella pertussis, 231, 233

Boyd, Chris, 88

Boyer, Herbert, 311f

EcoBI purification, 24

EcoRI discovery, 21, 36, 40–41

PhD thesis, 40–41

Bpu10I, 129, 130t, 188

BpuSI, 228, 229f

methylation, 202

recent studies, 295t

recognition sequence, 196, 203, 295t

subunit/domain composition and cleavage mechanisms, 203

Brammar, William, 52

Chris Boyd and, 88

EcoKI genes, cloning of, 54

Brooks, Joan, 55

Brown, Nigel, 69

BsaI, 319, 320f

BsaI-HF v2, 319, 320f

BsaWI, 194t

BsaXI

recent studies, 295t

recognition sequence, 195, 295t

subdomains, 195–196

Bse634I, 142, 143f, 144

CCGG family of restriction enzymes, 194t

recent studies, 295t

recognition sequence, 200, 295t

subunit/domain composition and cleavage mechanisms, 200

BseRI, 202

BslI, 129, 130t

BsmBI, 319

BsmFI, 321

BsoBI, 127

BspD6I

recent studies, 295t

recognition sequence, 295t

BspI, 71

BspLU11III, 202

BspMI, 159

recent studies, 295t

recognition sequence, 295t

BspRI

recent studies, 295t

recognition sequence, 295t

BssHII, 323

Bst DNA polymerase, 323–324

BstNI, 138–139

BstYI

recent studies, 295t

recognition sequence, 205, 295t

structure, 205

Bsu36I, 188

BsuRI

molecular weight, 91

recognition sequence, 188

Bucci, Pat, 40

Bujnicki, Janusz, 128

Bullas, Len, 104

Burns, Ken, 39f

Butkus, Viktoras, 57f

C

3C (chromosome conformation capture)-based technologies, 324

C (control) proteins, 187, 212–214, 212f, 307

Ca2+, 191

CalI, 71

Campbell, Allan, 12

Campylobacter jejuni, 249

Cas9 fusions, 209

Catenane assays, 140, 141f, 142

CCGG family of restriction enzymes, 193, 194t

CCGG group photo, 198f

CCR5, 152

Cfr9I, 91, 93

Cfr10I

CCGG family of restriction enzymes, 194, 194t

recent studies, 295t

recognition sequence, 186, 194, 194t, 200, 295t

restriction folds, 146f

structural localization of active site residues, 145f

structure and biochemistry, 141–142, 143f, 144

Cfr42I, 201

CglI

recent studies, 296t

recognition sequence, 296t

Chan, Siuhong, 317

Chandrasegaran, Srinivasan, 152, 208

Chargaff, Erwin, 16

Chimeric restriction enzymes, 127, 151–152

ChIP-based sequencing, 322

Chromatin

mapping of open chromatin regions, 324–325

spatial structure, study of, 324

Chromosome conformation capture (3C)-based technologies, 324

Circular permutations, 3, 129, 215

Citrobacter freundii, 103, 142

CjeI, 195

Clamp loader, 240

Clark, John, 31

Cleavage. See DNA cleavage

Cloning vectors, EcoRI, 41

ClpXP

proteolysis mediated by, 230, 307

restriction alleviation, 161, 161f

Co2+, 188, 191

Codon usage in R-M systems, 125

Coevolution, 153

Collision model for DNA breakage, 108–109, 109f, 158–160, 160f, 307

Comb, Don, 53

Commercially available restriction enzymes in 1970s, 65, 66f

Control of restriction, 187, 211–215, 212f, 307

Control (C) proteins, 187, 212–214, 212f, 307

Convergent evolution, 188, 201

CpG islands, demethylation of, 232

CRISPR, 152, 252, 306, 325

Crossing-over, evolution of DNA specificity of Type I enzymes by unequal, 105, 307

Crystallography of Type II restriction enzymes, 95–99, 131, 188

Csp231I, 214

Cu2+, 188, 205

CUTTER, 53

Cuvier, Georges, 43

Cys4-Zn2+, 191

Cytosine epigenetic markers, mapping, 323

D

Dam methyltransferase, 67–68, 72, 251

Danna, Kathleen, 321

Dcm, 244

DdeI, cloning of, 55

DEAD box motif, 155–157

DeepSAGE, 321

Delbrück, Max, 6, 13–15

Demerec, Milislav, 13

Desulfococcus oleovorans, 215

Dickerson, Richardson, 69

Divergent evolution, 188

DNA assembly technologies, in vitro, 318

DNA binding by Type II restriction enzymes, 91–93, 92f, 93f

DNA cleavage. See also specific enzymes

BamHI, 135

diversity in, 126

metal ions and, 150–151

models for Type I restriction enzymes, 108–109

phosphorothioates, affect of, 100–101

restriction enzymes needing two copies of recognition sequence, 126, 129

as two-step process

Type II restriction enzymes, 70–71, 93–94

Type III restriction enzymes, 111–112

DNA fingerprinting, 255, 255f

DNA glycosylase, 207

DNA helicases, 155

DNA inactivation by restriction, 17–19

DNA libraries, 321–322

DNA ligase, 54, 95, 317, 321, 322f

DNA looping, 126, 140, 141f, 142, 226f, 237–238

DNA mapping, 44, 321

DNA methylation. See Methylation

DNA modification. See also Methylation

Arber-Dussoix paper, 19

discovery of, 186

mapping epigenetic modification, 323

role of methionine in, 20–21

Type IV restriction enzyme dependence on, 186, 241–247

DNA recognition functions of Type II restriction enzymes, 99–101

DNA replication, semiconservative nature of, 16

DNA sequencing, restriction enzyme use in, 44

DNA specificity. See Specificity

DnaB, 229

DnaE, 229

DNA–protein interfaces of Type II restriction enzymes, 99

DNase I-based sequencing methods, 324–325

DNase-Seq, 324–325

Doermann, Gus, 13

Double digests, 57

DpnI, 129, 130t

methyltransferase, 89

recent studies, 296t

recognition sequence, 204, 296t

subunit/domain composition and cleavage mechanisms, 204

DpnII

3C-based methods and, 324

methyltransferase, 89

recognition sequence, 204

Drug resistance, 28, 41

Dryden, David, 220, 226, 235

Dussoix, Daisy. See Roullan-Dussoix, Daisy

E

EagI, 323

Ecl18kI, 199

CCGG family of restriction enzymes, 194t

recent studies, 296t

recognition sequence, 199, 296t

EcoAI, 161

circular permutation of HsdS, 215

methylation, 110

EcoBI (EcoB), 103, 305

classification as Type IA enzyme, 104

DNA cleavage, 108

methylation, 110

purification, 24–25

reaction mechanism, 77

recognition sequence, 76

EcoBI methyltransferase (MTase), 25

EcoDXXI, 107

Eco57I, 88, 129, 130t

recent studies, 296t

recognition sequence, 196, 202, 296t

subunit/domain composition and cleavage mechanisms, 202

Eco72I, 213

Eco29kI

GIY-YIG motif, 191

recent studies, 296t

recognition sequence, 191, 296t

EcoKI (EcoK), 18–19, 305

ATP as allosteric effector, 253

classification as Type IA enzyme, 104

cloning of genes encoding, 54, 55

DNA cleavage, 108–109

DNA translocation, 155–156, 157f, 158–159, 216–217

enzyme structure and mechanisms, 108

HsdM protein, 153, 154f

HsdR protein, 153, 154f, 225f, 226–228

HsdS protein, 153, 154f

M·EcoKI (M2S1) complex, 217–220, 218f–219f

methylation, 110, 309

methyltransferases, 217, 218f, 255–256

modeling DNA recognition complex of EcoKI trimeric complex, 153–155, 154f

nomenclature, 103

purification, 23–24, 24–25, 29–34

reaction mechanisms, 76–77

recent studies, 302t

recognition sequence, 76, 302t

R2M2S1 complexes, 220–228

S-adenosylmethionine (SAM) and, 153, 255

single-molecule studies, 216–217

structure, 154, 221f, 224, 225f, 307

subunits of, 108

translocation, 307

EcoP1I (EcoP1), 5, 18, 77–78, 110

genetics of, 78

mod gene, 111

purification, 78

reaction mechanism, 111

recognition sequence, 78, 111

res gene, 111

EcoP15I (EcoP15), 77, 110, 236–241

DNA cleavage, 112

DNA recognition by, 238

genetics of, 78

Huntington's disease and, 206

mod gene, 111

reaction mechanism, 111

recent studies, 303t

recognition sequence, 78, 111, 303t

res gene, 111

restriction by, 240–241

structure, 237–241, 239f, 253, 307

structure of EcoP15I/DNA/AMP complex, 238, 239f

in SuperSAGE and DeepSAGE, 321

translocation, 253

EcoprrI system, 230

EcoRI, 129, 130t, 305

action of, 88

altering specificity, 127

biochemistry of, 68, 132

3C and, 324

dimer, 143f

discovery of, 21, 36, 40–41, 65

DNA binding, 91–93

DNA cleavage, 99, 204, 205

DNA interactions of, 73–74, 132

DNA recognition, 99–101

DNA–protein interfaces, 99

fidelity of, 71

genes

cloning of, 54

DNA sequence of, 68

organization, 91

homodimer, 68

lambda mutants with variation in number of EcoRI sites, 69–70, 70f

operon, regulation of, 205

organization, genes and, 91

purification, 68–70

recent studies, 296t

recognition sequence, 41, 88–89, 144, 185, 188, 296t

restriction folds, 146f

RNA–DNA hybrids, cleavage of, 72

RsrI similarity to, 188

specificity, 95, 101, 132

stable DNA–protein complexes in absence of Mg2+, 91

star (*) activity, 95, 205

structural localization of active site residues, 145f

structure, 95–99, 96f, 103, 131–132, 143f, 145–147, 145f

target site location, 93

transcriptional control of restriction, 214

as Type IIP restriction enzyme, 43

water role in recognition, 149

EcoR124I (EcoR124), 104–105, 106f, 107, 161, 251–252

DNA translocation, 226f

HsdM protein, 224, 225f–226f

HsdR protein, 222–224, 222f, 225f–226f

HsdS protein, 108, 224, 225f–226f

recent studies, 302t

recognition sequence, 302t

R2M2S1 complexes, 220–228

R1M2S1 form of, 228

single-molecule studies, 216–217

structure, 221f, 224, 225f

EcoRI methyltransferase, 68

DNA contacts made by, 74

monomeric, 68

EcoRI–DNA enzyme complex, structure of, 97–99, 98f

EcoRII, 41, 88, 129, 130t

activation in trans, 138–139, 139f

CCGG family of restriction enzymes, 193–194, 194t

cloning of genes encoding, 54

DNA cleavage, 94

genes and organization, 91

PD…(D/E)XK motif, 149

recent studies, 297t

recognition sequence, 65, 90, 138, 142, 193–194, 194t, 297t

refractory sites, 128

satellite DNA cleavage, 45

stable DNA–protein complexes in absence of Mg2+, 91

subunit/domain composition and cleavage mechanisms, 196, 197f, 198–200

translocation along DNA, 199

EcoR124II (EcoR124/3), 105, 106f, 107, 251–252

EcoRII-C, 199

EcoR124I-Ocr complex, 223

EcoRV, 65, 87, 127, 129

action of, 88

altering specificity, 127

cloning of genes encoding, 54

control by C proteins, 213

crystal structure, 96–99, 96f

DNA binding, 91–93, 92f

DNA cleavage, 94, 99, 132, 204

DNA interactions, 134

DNA recognition, 100–101

DNA–protein interfaces, 99

metal cofactors, 150–151

recent studies, 297t

recognition sequence, 297t

restriction folds, 146f

sliding along DNA, 204–205

specificity, 95

stable DNA–protein complexes in absence of Mg2+, 91

structure, 103, 132–134, 133f, 145–147, 186

EcoRV–DNA enzyme complex, structure of, 97–99

Eisenstark, Abe, 6f

Endonuclease R, purification of, 49

Endonuclease structural domains, 191–193

Endonuclease Z, 49

Endonucleases, homing, 191, 208, 210f, 325

EndoR. See HindII

Enterococcus faecalis, 231, 233

“Epigenetic identity,” 214

Epigenetic modification, mapping, 323

Epigenetics, 21, 186

Escherichia coli

CFT073, 231, 233

CT596, 241

Type I enzymes from, 103

Esp3I, 89, 319

Esp1396I, 212f, 213

Eubacteria, 125

Evolution, 54, 190

antirestriction, 231

convergent, 188, 201

divergent, 188

DNA specificity of Type I restriction enzymes, 104–107, 106f, 307

by homologous recombination within the hsdS gene, 104–105, 106f

by transposition within the hsdS gene, 107

by unequal crossing-over within the hsdS gene, 105, 106f, 107

independent by most restriction enzymes, 91

neutral drift, 188

PD…(D/E)XK motif family of restriction enzymes, 145–147, 185

relationship between restriction enzymes, 148–149, 148f

slipped-strand mispairing (SSM), 247

Type I R-M systems, 153, 307

Type IIF restriction enzymes, 144

Type IIG enzymes from Type I enzyme, 228, 229f

Evolutionary trees, 2, 128

Exonuclease-based DNA assembly methods, 320–321, 322f

EXPAR, 323

F

FastDigest buffer, 57

Fd phage, 20

Fe2+, 188

Fermentas, 56–57, 57f, 128

Fidelity

methyltransferases, 71–72

Type II restriction enzymes, 71–72

Fiers, Walter, 50

Flavobacterium okeanokoites, 151

FokI, 88, 89, 129, 130t, 147, 149

chimeric restriction enzymes, 151–152

cloning, 151

engineering to obtain hybrid restriction enzymes, 90

fusions proteins, 208–209, 306

recent studies, 297t

recognition sequence, 206, 297t

restriction folds, 146f

serial analysis of gene expression (SAGE) and, 321

structure, 127, 129

subunit/domain composition and cleavage mechanism, 206–207

FspEI, 323

Fusions proteins, 208–209, 210f, 306

G

Gel-shift assays, 91–92, 92f, 94, 133

GenBank, 58

Gene targeting tools, 208–211, 210f

fusions, 208–209, 210f

nickases (nicking enzymes), 209, 211

Generalized transduction, 5

Genes

cloning of genes encoding restriction enzymes, 54–57

first R-M systems, 54

at New England Biolabs, 54–56

in Vilnius, Lithuania, 56–57, 57f

codon usage in R-M systems, 125

isolation of, 45

methyltransferase gene locations adjacent to restriction genes, 3

Genetic engineering, 41, 44–46, 305

Genetic selection operating at population level, 112

Genome editing, 252, 306, 325

ghm5C, 241, 246

Gibson, Daniel G., 320

Gibson Assembly, 318, 320–321, 322f

GIY-YIG motif, 191, 306

Glover, Stuart, 22, 104, 237

gmrD, 241, 246

gmrS, 241, 246

GmrSD, 246

Golden Gate Assembly, 318, 319–320, 320f

Greene, Patricia, 69

GsuI, 130t

Gutfreund, Herbert Frederick, 69

H

HaeII, 49, 72

HaeII methyltransferase, 72

HaeIII, 43, 49

mechanisms of base pair recognition, 74–75

recognition sequence, 188

RNA–DNA hybrids, cleavage of, 72

HaeIII methyltransferase, 72

HaeIV, 130t

Haemophilus influenzae, 237

nontypeable Haemophilus influenzae (NTHi), 2, 249, 250f

phase variation, 247, 249–252, 250f

Hairpin adaptor ligation, 322

Halford, Stephen, 68–70

crystal structures of EcoRI and EcoRV, 97

retirement party, 198f

HaloPlex enrichment, 322

Heitman, Joe, 56, 100

Helicobacter pylori, 207, 247–249

Helix-turn-helix. See HTH (helix-turn-helix) motif

Hershey, Alfred, 19

Hershey & Chase experiment, 8, 12, 16

HgaI, 89–90

HhaI methyltransferase, 128, 153

HhaII, 244

cloning of, 54, 55

RNA–DNA hybrids, cleavage of, 72

Hi-C, 324

Higa, Akiko, 21

HincII, 127

HindfII, 78

HindI, 75, 251

HindII, 305

recognition sequence, 38–39, 40f

recognition sequences in SV40, 39–40

HindIII, 43

3C and, 324

DNA cleavage, 71

RNA–DNA hybrids, cleavage of, 72

HinfIII, 77, 110, 111

HinP1I

recent studies, 298t

recognition sequence, 298t

History of Restriction Enzymes (October 19-21, 2013) meeting program, 199f, 311–316, 311f

hm5C, 42, 186, 241, 244, 246

HNH motifs, 191, 244, 306

Hoffmann-Berling, Hartmut, 20

Homing endonucleases, 191, 208, 210f, 325

Homologous recombination, 307

within hsdS gene of Type I restriction enzymes, 104–105, 106f

stimulated by fusion proteins, 208, 210f

Horecker, Bernie, 31

Horizontal transfer, 125, 230, 249, 307

Host-controlled modification, 21

Host-controlled variation, 1, 305

Bertani and, 5–8, 10–12, 14

discovery of, 5–8, 10, 14

general scheme of adaptive host-induced modification, Luria's, 9t

Jean Weigle and, 5–8, 10–12, 14

Salvador Luria and, 8, 9t, 11–12

HpaI, 43, 49, 74

DNA cleavage, 71

recognition of ssDNA, 72

HpaI methyltransferase, 68

HpaII, 43, 49, 67

DNA cleavage, 71

mechanisms of base pair recognition, 74–75

methylation-sensitive amplification polymorphism (MSAP), 323

HpaII methyltransferase, 68

Hph1

recent studies, 299t

recognition sequence, 299t

Hpy99I

HNH motif, 191

recognition sequence, 191

Hpy188I

GIY-YIG motif, 191

recent studies, 299t

recognition sequence, 191, 299t

HrpA, 229

hsdM gene(s), 22, 25, 34, 75, 103–104, 215, 251

HsdM protein

EcoKI, 153, 154f

EcoR124I, 224, 225f–226f

M·EcoKI (M2S1) complex, 217, 218f

hsdR gene(s), 22, 25, 75, 103–104, 215

HsdR protein

ATP dependence of motors, 216

DNA translocation, 153, 155–161

EcoKI, 153, 154f, 225f, 226–228

EcoR124I, 222–224, 222f, 225f–226f

phosphorylation of, 229–230

Res compared, 157

hsdS gene(s), 22, 25, 75, 215

cotranscription with hsdM gene, 103

evolution of DNA specificity of Type I enzymes

by homologous recombination within the hsdS gene if Type I restriction enzymes, 104–105, 106f

transposition within the hsdS gene, 107

by unequal crossing-over within the hsdS gene, 105, 106f, 107

phase variation, 251, 252

shuffling in Mycoplasma, 215

HsdS protein

circular permutation of EcoAI, 215

EcoKI, 153, 154f

EcoR124I, 224, 225f–226f

M·EcoKI (M2S1) complex, 217, 218f–219f, 219

repeats in, 251

similarities and differences between Type I families, 215

HTH (helix-turn-helix) motif, 129

Hubácek, Josef, 22

Human, Mary, 8, 11–12

Hungarian trick, 55

Huntington's disease, 206

Hutchison, Clyde, 49

Hybrid restriction enzymes, engineering FokI to obtain, 90

Hydroxymethylcytosine (hm5C), 42, 186, 241, 244, 246

I

iGEM (International Genetically Engineered Machines) competition, 319

Immune system

evasion, 247

primitive bacterial, 153, 248

In vitro DNA assembly technologies, 318

IncI plasmid, 231

Indels (insertions/deletions), 321

In-fusion, 321

Insertions/deletions (indels), 321

International Genetically Engineered Machines (iGEM) competition, 319

Isoschizomers, 43

defined, 67

differential strand preference for DNA duplexes, 71

differentially sensitive to methylation, 67

EMBO Workshop in Ghent (1974), 50, 50f

neoschizomers, 67

Type II restriction enzymes, 66–67

Type IIS restriction enzymes, 89

usefulness of, 67

J

Jacob, François, 29

Janulaitis, Arvydas, 56, 57f

Jeffreys, Alec, 255, 255f, 305

Jeltsch, Albert, 128

Jen-Jacobson, Linda, 72

Jennings, Michael, 247

K

Kellenberger, Edouard, 15, 16f, 35

Kellenberger-Gujer, Grete, 17, 18, 35

Kelly, Tom, 39, 39f, 311f

Kinetic studies on DNA cleavage, 94

KlcA, 231, 233, 235

Kneale, Geoff, 187, 213

Knock-in, 325

Knockout, 325

Kobayashi, Ichizo, 128, 161, 205, 214, 230

kor operon, 233

KpnAI, 104

KpnBI, 104

KpnI

HNH motifs, 191

recent studies, 299t

recognition sequence, 191, 299t

Kpn2I, 194t

Krüger, Detlev, 128, 231

Kühnlein, Urs, 33

L

Lactococcus lactis, 235

Lambda, 305

Arber and, 15, 17

dgal, 17

EcoKI action on, 23–24

efficiency of plating variants on different host strains, 17–19, 18t

gene control, 213

host controlled variation and, 5–8, 17–19

methylation, 20

mutants with variation in number of EcoRI sites, 69–70, 70f

Ral protein, 110, 230, 255, 309

restriction of DNA, 41

transduction by, 12–13

Lar protein, 110, 230

Lateral domain movement within genes, 230

LB medium, 13

Lederberg, Esther, 5, 17, 35

Lederberg, Joshua, 17

Lederberg, Seymour, 30

Lehman, Robert, 69

Lenhof, Ed, 31

Lindahl, Tomas, 69

Linn, Stuart, 19–20, 30, 33, 39, 311f

EcoBI purification, 24–25

models for hyphenated and/or palendromic recognition sites, 22–23

Noreen Murray and, 70

LlaBIII, 235–236

LlaGI, 235–236

LongSAGE, 321

Looping. See DNA looping

LoxP-Cre recombination system, 5

LpnPI, 323

Lubys, Arvydas, 57f

Lunnen, Keith, 56

Luria, Salvador

barrier to infection, 8

Bertani and, 13–14

Hamilton Smith and, 39

host controlled variation, 8, 9t, 11–12

Joe Bertani and, 5

A Slot Machine, a Broken Test Tube, 11, 15

T* phages, 8, 21

Lysogeny, 5, 8, 10–12

M

m6A, 204, 206, 235, 238, 244

Macelis, Dana, 50

Mandel, Morton, 21

Mapping, restriction enzyme use in, 44, 321

Mapping epigenetic modification, 323

Markauskas, Algimantas, 57f

Maternal inheritance of mitochondria, discovery of, 44

MboI, 67

3C-based methods and, 324

methyltransferase, 89

recognition site, 194

m4C, 187, 202

m5C, 42, 186–187, 202, 206, 241–242, 244, 246

Mcr restriction system, 8, 15, 42, 56

mcrA gene, 186

McrA protein, 241

mcrBC gene, 186

McrBC protein, 129, 131, 241, 244, 245f

McrB-N, 243f

recent studies, 302t

recognition sequence, 302t

MDEs (modification-dependent restriction enzymes). See Type IV restriction enzymes

M·EcoKI (M2S1) complex, 217–220, 218f–219f

M·EcoKI-Ocr complex, 220

Meganucleases, 208, 210f

Merozygotes, 22

Meselson, Matthew, 16–17, 311f

e-mails with Noreen Murray, 29–34

purification EcoKI, 23–24

Metal cofactors, 127, 188

BamHI, 135

positioning of, 126

role in Type II restriction enzymes, 150–151

Methanocaldococcus jannaschii, 219

Methicillin-resistant Staphylococcus aureus (MRSA), 230

Methionine, role in DNA modification, 20–21

Methylase-selection method, 55

Methylation

discovery of, 186

host specificity and, 22

maintenance versus de novo methylation by Type I enzymes, 110, 309

mapping epigenetic modification, 323

methionine role in DNA modification, 20–21

methylome, 18, 308

Ral-independent novo methylation in EcoKI M* mutants, 110, 309

RNA, 238

sensitivity of isoschizomers to, 67

SMRT sequencing to locate sites of, 58

Type I systems, 76

Type II systems, 71

Type III systems, 78, 111–112, 236

Type IIS systems, 89–90

Methylation-sensitive amplification polymorphism (MSAP), 323

Methylome, 18, 308

Methylophilus methylotrophus, 88

Methyltransferases (MTases)

base flipping, 128

circular permutations, 3, 129

common amino acid sequence motifs, 58, 58f

common architecture of, 91

control of restriction and, 212–213, 215

Dam, 67–68, 72, 251

dimeric, 237–238

EcoKI, 217, 218f, 255–256

EcoKI and EcoR124I (R2M2S1) complex, 220–228

EcoRI, 89

fidelity of, 71–72

genes, cloning, 55

identification of, 58–59

methylome, 18, 308

modeling DNA recognition complex of EcoKI trimeric complex, 153–155, 154f

monomeric, 71

monomers, 68, 89, 91

phase variation, 248, 250f

RNA, 238

Type II systems, 71

Type IIA restriction enzymes, 194

Type IIG restriction enzymes, 202–203

Type IIH restriction enzymes, 204

Type III systems, 238

Type IIP restriction enzymes, 204

Type IIS restriction enzymes, 206–207

Mg2+, 205

DNA binding by Type II restriction enzymes in absence of, 93

EcoRV DNA cleavage and, 101

HNH motif, 191

restriction enzyme requirement for, 41, 42, 68, 89, 91

Microbiome, 308

Mismatch repair, strand-directed DNA, 69

Mitochondria, discovery of maternal inheritance in, 44

MluCI, 188

MmeI, 88, 130t, 188, 228, 229f

LongSAGE, 321

recent studies, 299t

recognition sequence, 196, 202, 299t

specificity alteration, 203

subunit/domain composition and cleavage mechanisms, 202–203

Mn2+, 188, 191

MnlI

recent studies, 299t

recognition sequence, 299t

mod genes, 22, 78, 110–111

Neisseria gonorrhoeae, 250–251

phase variation, 249–252, 250f

Mod subunits of EcoP15I, 159, 236–238, 239f, 240

Model, Peter, 56, 100

Modification-dependent restriction enzymes (MDEs). See Type IV restriction enzymes

Modified cytosine restriction. See mcr restriction system

Modified single burst technique, 13

Modrich, Paul, 68–69

Molecular cloning, 317–318, 318f

Molecular motors, 127, 152, 155–160, 157f, 160f, 216, 220, 227–228, 240–241, 253, 307

Molecular switching, 240

Molecular weight of restriction enzymes, 68, 91

Montagnier, Luc, 36

Morgan, Richard, 88, 203

Mori, Hirotada, 228

Morse, Larry, 17

Mosaicism, 188

Motors. See Molecular motors

Moxon, Richard, 247

Mrr (modified DNA rejection and restriction), 56, 244

MRSA (methicillin-resistant Staphylococcus aureus), 230

Mruk, Iwona, 214

MspI, 67

methylation-sensitive amplification polymorphism (MSAP), 323

RNA–DNA hybrids, cleavage of, 72, 73

MspJI, 244, 246–247

mapping cytosine epigenetic markers, 323

recent studies, 303t

recognition sequence, 303t

MunI

recognition sequence, 144, 188

structure, 127

Murray, Kenneth, 70

Murray, Noreen, 161

Bertani letter to, 5, 10–13

EcoKI genes, cloning of, 54

e-mails with Matt Meselson, 29–34

lambda phages with variation in EcoRI sites, 69–70

photograph, 199f

Ral-independent EcoKI M* mutants, 110, 309

Type I restriction enzymes, 75

MUTATE, 53

MutH, 145, 146f, 149, 200

MvaI, 139–140, 200

Mva269I, 207

recent studies, 299t

recognition sequence, 299t

Mycobacterium, 246

Mycoplasma, 215

Myers, Phyllis, 69

N

NaeI, 88, 129, 130t

activation in trans, 139

DNA cleavage, 94

DNA interaction, 140

recent studies, 299t

recognition sequence, 299t

structure, 140

subunit/domain composition and cleavage mechanisms, 196, 197f

“Turbo NaeI,” 139

“Nanoballs,” DNA, 322

NarI

recent studies, 299t

recognition sequence, 299t

Nathans, Daniel, 321

Hind II restriction sites in SV40, 39–40

Nobel Prize, 1, 6, 35, 40

photograph, 39f

restriction of SV40 DNA by endonuclease R, 49

NEAR, 323

NEB. See New England Biolabs (NEB)

NEBcutter, 53

NEBuilder Hi-Fi DNA Assembly, 318, 321, 322f

Neisseria, 237, 247, 250–252

Neisseria gonorrhoeae, 142, 250–252

Neoschizomers, 67

NESA, 323

Neutral drift, 188

New England Biolabs (NEB), 91, 128

catalog, 51f, 53

cloning genes encoding restriction enzymes, 54–56

founding of, 53

meetings (1988–2015), 254f

Next-generation sequencing, 58

NgoAV, 251, 252

NgoAXP, 250

NgoMIV, 129, 135

CCGG family of restriction enzymes, 193–194, 194t

PD…(D/E)XK motif, 149

recognition sequence, 142, 185, 193–194, 194t, 200

structural localization of active site residues, 145f

structure and biochemistry, 127, 141–142, 143f, 144

Ni2+, 188, 191

NicE-seq (nicking enzyme-assisted sequencing), 324–325

Nickases (nicking enzymes), 209, 211, 323–324

Nocardia aerocolonigenes, 139

Nonhomologous enjoining (NHEJ), 211

Nontypeable Haemophilus influenzae (NTHi), 2

NotI

recent studies, 300t

recognition sequence, 188, 300t

restriction landmark genome scanning (RLGS), 323

Nt.CviPII, 324

Nuc endonuclease, 193

NucA, 147

Nucleotide excision repair, 232

O

Ocr, 109, 219–220, 223, 231

effectiveness of inhibition of Type I R-M systems, 234–235

structure, 232–235, 232f, 234f

OkrAI, 205

Oligo(dT) tailing, 45

Open chromatin regions, 324–325

Ostwald viscometer, 37, 38f

P

P1 phage

Bertani and, 17–18, 77

host-controlled variation and, 18

restriction enzymes, 5, 42

P2 phage

Bertani and, 12–14

host range variation, 6–8, 7f

restriction and modification, 10–12

PabI

DNA glycosylase, 207

recent studies, 300t

recognition sequence, 300t

PacI

HNH motif, 191

recent studies, 300t

recognition sequence, 191, 205, 300t

subunit/domain composition and cleavage mechanisms, 205–205

PaeR7I, 54

Partial diploids, 22

Pasteurella haemolytica, 251

Pathogenic bacteria, restriction systems in, 2, 308

pBR322, 317

PD fold. See PD…(D/E)XK motif

PDB (Protein Data Base), 188, 189f, 190

PD…(D/E)XK motif, 145–147, 145f, 147f, 185, 190–191, 306

Pettersson, Ulf, 50f

PfoI, 194t, 199

Phage selection, use in cloning restriction enzymes,54, 55

Phase variation, 187–188, 247–252, 250f, 308

pathogen use, 230

Type I systems, 251–252

Type II systems, 248–249

Type III systems, 237, 249–251

Phosphorothioates, 100–101, 244

Phylogenetic trees, 148, 148f

Piekarowicz, Andrzej, 237, 247

Pin domain, 240–241

Pingoud, Alfred, 87–88, 97, 126, 128, 193, 253, 305

Plasmid vectors, 317–318, 318f

PLD catalytic domain, 191, 193

PluTI, 201

Point-of-care DNA amplification and detection, 323–324

Pollock, Mila, 311f

Pósfai, Janos, 58

PpiI, 195

PpuMI, 130t

Programmed cell death, 214

Protein Data Base (PDB), 188, 189f, 190

Proteus vulgaris, 211, 246

PrrC, 230

pSC101, 317

PspGI, 144

CCGG family of restriction enzymes, 194, 194t

PD…(D/E)XK motif, 149

recent studies, 300t

recognition sequence, 194, 194t, 199, 300t

PstI, 244

cloning of, 55

E. coli strain overexpressing, 55

PstII, 55

Ptashne, Mark, 30

Purification of restriction enzymes, 49

PvuII

cloning of genes encoding, 54

control of restriction, 211–213, 212f

fusion proteins, 208–209, 210f

metal cofactors, 151

molecular weight, 91, 103

restriction folds, 146f

structure, 96–97, 102–103, 102f, 146, 186

PVUII–DNA complex, structure of, 102–103, 102f

PvuRts1I, 246

recent studies, 302t

recognition sequence, 302t

PyrG, 229

Pyrococcus abyssi, 207

Q

Q-tip helix motif, 157

R

Radzeviciene, Egle, 57f

Ral (restriction alleviation) protein of lambda, 110, 230, 255, 309

Raleigh, Elizabeth, 56, 57f

Rao, D.N., 199f

Rau, Donald, 149

Reaction mechanisms

Type I restriction enzymes, 76–77

Type III restriction enzymes, 78–79

REBASE database, 50, 52f, 125–126, 126t, 215, 305

REBpredictor, 53

RecA domains, of EcoP15I, 240–241

Recognition sequence. See also specific restriction enzymes

Arber and Linn models for hyphenated and/or palendromic recognition sites, 22–23

BamHI determination by 2D electrophoresis, 53, 53f

Hind II, 38–39, 40f

Type III restriction enzymes, 78

Recombinant DNA, Type II restriction enzyme use in, 44–46

gene isolation, 45

mapping, 44

repeat DNA sequences, 45

sequencing, 44–45

REMAP, 53

Repetitive DNA sequences, analysis of, 45

res gene, 22, 78, 110–111

Res protein

DNA translocation, 155–160

EcoP15I, 155–156, 237–238, 240

HsdR compared, 157

sequence subtypes, 157–158

Resistance transfer factors (RTFs), 21, 29, 41

Resolvase, 141f

Restriction alleviation, 160–162, 161f

Restriction enzymes

classification of, 41–43

growth in number of, 49, 51f, 52, 126

in mid-1970s, 43–44

Restriction fragment length polymorphisms (RFLPs), 255

Restriction genes, methyltransferase gene locations adjacent to, 3

Restriction landmark genome scanning (RLGS), 323

Restriction sites, of selected enzymes studied in recent years, 294t–303t

Restriction-modification (R-M) genes

allelism of, 21–23

location of, 21–23

Restriction-modification (R-M) systems. See also Host-controlled variation

Arber-Dussoix papers, 19

cloning, 54–57

codon usage, 125

control of restriction, 211–213, 212f

horizontal transfer, 125

identification using MTase motifs, 58

nomenclature, 40

shuffling protein domains, 149

Reuter, Monika, 128

RFLPS (restriction fragment length polymorphisms), 255

Rgl1, 42

Rgl2, 42

rglA, 186

rglB, 186

Rich, Alexander, 69

Richardson, Charles, 38, 69

RLGS (restriction landmark genome scanning), 323

R-M systems. See Restriction-modification (R-M) systems

RNA methylation, 238

RNA targeting, 325

RNA-based innate immunity system, 230

RNA–DNA hybrids, Type II restriction enzyme recognition of, 72–73

Roberts, Richard, 23, 44, 311f

classification of Type II restriction enzymes, 129

crystal structures of EcoRI and EcoRV, 97

Nobel Prize, 49

photograph, 50f, 57f

restriction enzyme list, 50, 51f, 305

restriction enzymes, 49–53

Rolling circle amplification, 323

Rosenberg, John, 68–69, 96, 131–132, 311f

Roullan-Dussoix, Daisy

Arber-Dussoix papers, 17–19

EcoBI purification, 24

EcoRI purification, 41

host-controlled variation, 17–19

malaria, 36

PhD work, 35

photograph, 18f

postdoctoral work, 36

scientific career, 35–36

RsrI

DNA binding, 91, 92

EcoRI similarity to, 188

recognition sequence, 188

stable DNA–protein complexes in absence of Mg2+, 91

RsuI methyltransferase, 68

RTFs (resistance transfer factors), 21, 29, 41

S

S-adenosylmethionine (SAM)

EcoKI, 153, 255

methylation of DNA, 20

requirement in restriction enzyme purification, 31, 34

restriction enzyme requirement for, 24, 41–42, 43, 90, 104

Type I restriction enzymes reaction mechanisms, 76

Type III enzymes and, 78, 111–112

“Safety catch,” 201

SAGE (serial analysis of gene expression), 321

SalI, 71, 94

Salmonella

S. potsdam, 104

S. typhimurium, 147

Nuc endonuclease, 193

Type I restriction enzymes, 75–76

StyLTI system, 110–111

Type I enzymes from, 103–105

Sancar, Aziz, 69

Sanger, Fred, 52, 69

Satellite repeats, analysis of, 45

Sau3AI, 67

3C-based methods and, 324

cutting of RNA–DNA hybrids, 73

DNA interaction, 149

SauI, 230

SauUSI, 245–246

Schell, Josef, 50

ScoA3McrA, 244

SDA, 323

Self versus nonself, 307

Selfishness, 127–128, 161–162

Sequence discrimination, mechanisms of, 128

Sequence homologies within and between families of Type I enzymes, 104

Sequencing

DNase I–based sequencing methods, 324–325

NicE-seq (nicking enzyme-assisted sequencing), 324–325

restriction enzyme use in, 44–45

single-molecule (SMRT), 58–59, 187, 216

whole-genome, 230, 307–308

SeqWare, 58

Serial analysis of gene expression (SAGE), 321

SF1 (superfamily 1) proteins, 159

SF2 (superfamily 2) proteins, 154f, 156, 216, 232, 241, 253, 306

SfiI, 129, 130t

DNA excision, 149

recent studies, 300t

recognition sequence, 201, 300t

structure and biochemistry, 141–142, 145, 201

SgrAI, 130t, 139

CCGG family of restriction enzymes, 194t

recent studies, 301t

recognition sequence, 201, 301t

structure, 201, 201f

Sgr20I, 90

Sharp, Phillip, 49

Shuttle vectors, 2

Sidorova, Nina, 149

Šikšnys, Virginijus, 128, 142, 185, 194t

Single-molecule (SMRT) sequencing, 58–59, 187, 216

Single-molecule studies

FokI, 207

Type I restriction enzymes, 216–217, 307

Type IIE restriction enzymes, 196, 198

Type III restriction enzymes, 240–241

Single-nucleotide polymorphisms (SNPs), 321

Single-stranded DNA (ssDNA), Type II restriction enzyme recognition of, 72–73

Slab gel electrophoresis, 52, 66

Slipped-strand mispairing (SSM), 247

A Slot Machine, a Broken Test Tube (Luria), 11, 15

SmaI

cleavage site, 67

control by C proteins, 213

Smith, Hamilton, 311f

HhaII cloning, 54

Hind II discovery, 37–40

Nobel Prize, 1, 6, 35, 40

photograph, 39f

Rich Roberts and, 49

Smith, John, 20, 33

SMRT sequencing method, 58–59, 187, 216

SNPs (single-nucleotide polymorphisms), 321

Solfolobus solfataricus, 223, 241

SOS response, 56, 100

Southern blot, 45, 75

Specificity

altered, 127, 203

evolution of Type I restriction enzymes, 104–107, 106f, 307

by homologous recombination within the hsdS gene, 104–105, 106f

by transposition within the hsdS gene, 107

by unequal crossing-over within the hsdS gene, 105, 106f, 107

Type II restriction enzymes, 66–67, 87, 88–89, 95

Type IIS restriction enzymes, 89

water role in recognition by Type II restriction enzymes, 149

Spi phenotype, 6

Split genes in adenovirus, 49

ssDNA (single-stranded DNA), Type II restriction enzyme recognition of, 72–73

SSM (slipped-strand mispairing), 247

SsoI

CCGG family of restriction enzymes, 193–194

recognition site, 193–194

SsoII, 144

PD…(D/E)XK motif, 149

recent studies, 301t

recognition sequence, 142, 199, 301t

Stahl, Franklin, 16

Staphylococcus aureus

MRSA (methicillin-resistant Staphylococcus aureus), 230

SauUSI, 245–246

Star (*) activity, 95, 188, 205

Stent, Gunther, 19, 20, 33

Sticky ends

EcoRI, 2, 41

recombinant DNA applications, 45

Stillman, Bruce, 311f

Strain typing, 230

Strand-directed DNA mismatch repair, 69

Streptomyces coelicolor A3, 244

Strominger, Jack, 49

Structural evolution of Type IIG enzymes from Type I enzyme, 228, 229f

StsI, 89, 207

Studier, Bill, 109, 158, 231, 307

StyBLI, 104

StyD4I, 142

StyLTI, 110, 244

mod gene, 111

recognition sequence, 111

res gene, 111

StyLTIII, 106f

StyR124I, 104

StySB1, 105

StySJ, 106f

StySJIb, 105

StySP1, 105, 106f

StySQ, 104–105, 106f

StySQ1, 105

SuperSAGE, 321

SUVH5, 243f

SV40, 39–40, 321

SwaI

recent studies, 301t

recognition sequence, 205, 301t

subunit/domain composition and cleavage mechanisms, 205–205

SWI2/SNF2 chromatin remodeling translocase, 223

Synthetic biology, 318

Szczelkun, Mark, 156

Szybalski, Waclaw, 6f, 206

T

T3 phage

antirestriction, 231

resistance to EcoRII, 138

T4 phage, as dodger of host restriction, 231, 241

T7 phage

antirestriction, 231

Ocr, 109, 219–220, 223, 232–235, 232f, 234f

resistance to EcoKI cleavage, 109

resistance to EcoP15I, 112

resistance to EcoRII, 138

T* phages, 21, 186

barrier to infection by, 8

Type IV restriction enzymes, 42

T4 polynucleotide kinase, 38

TALE nucleases (TALENs), 209, 210f, 306, 325

TALE (transcription activator-like effector) proteins, 208–209, 210f

TaqI

DNA binding, 91, 93

stable DNA–protein complexes in absence of Mg2+, 91

Target site location, scheme for, 93, 93f

Tet (ten-eleven translocation) proteins, 187

Tetranucleotide hypothesis, Levene's, 16

TFO (triple-helix-forming oligonucleotide)-linked nucleases, 210f

ThermoFisher Scientific, 57

Thomas, René, 10

Tn5, 107, 324

Tn916, 233

Tn7 transposase, 149

TnsA, 145, 146f

Tracking, by restriction enzymes, 140, 141f

Transcription activator-like effector (TALE) proteins, 208–209, 210f

Transcriptional control, 214

Transcriptional regulation of R genes of Type II restriction enzymes by control (C) proteins and antisense promoters, 55

Transduction

Bertani and, 14

generalized, 5

lambda, 12–13

Translocation, 152–153, 155–160, 157f, 160f, 190, 199, 216–217, 220, 224, 307

ATP and, 155–156, 158–159, 227

EcoKI, 155–156, 157f, 158–159, 216–217, 307

EcoP15I, 237–238, 253

EcoR124I, 226f

Transposition, evolution of Type I enzyme DNA specificity by, 107

Triple-helix-forming oligonucleotide (TFO)-linked nucleases, 210f

TseI

Huntington's disease and, 206

recent studies, 301t

recognition sequence, 301t

TspGWI

recent studies, 301t

recognition sequence, 301t

TstI

recent studies, 301t

recognition sequence, 301t

2D electrophoresis, 53, 53f

Type I restriction enzymes, 75–77, 103–110, 152–162, 305–308

Type I restriction enzymes (Continued )

antagonists of, 230–232

atomic structure, 217–228

EcoKI and EcoR124I (R2M2S1) complex, 220–228, 221f–222f, 225f–226f

M·EcoKI (M2S1) complex, 217–220, 218f–219f

ATP use, 152, 216

cleavage models for, 108–109

DNA translocation, 152, 155–156, 158–159, 216–217, 226f

ecoprrI system, 230

evolution of DNA specificity, 104–107, 106f, 307

by homologous recombination within the hsdS gene, 104–105, 106f

by transposition within the hsdS gene, 107

by unequal crossing-over within the hsdS gene, 105, 106f, 107

families and diversity of, 215–216

genes and proteins of, 75–76

history

1982–1993, 103–110

1993–2004, 152–162

2004–2016, 215–236

1970s and early 1980s, 75–77

identification, 58–59

maintenance versus de novo methylation by Type I enzymes, 110

molecular motors, 155–160, 157f, 160f

phase variation, 251–252

reaction mechanisms of, 76–77

in REBASE (2004), 126t

recognition sequences, 76

restriction alleviation, 160–162, 161f

roles of, 88, 228–230

sequence homologies within and between families, 104

SMRT sequencing, 216

structural evolution of Type IIG enzymes from Type I enzyme, 228, 229f

structural genes and family relationships of, 103–104

structures and mechanisms of, 107–110

Type II enzymes compared, 43, 307

Type I single protein (Type ISP), 235–236

Type IA restriction enzymes, 76, 104, 153

methylation, 110

methyltransferase switch, 255–256

Type IB restriction enzymes, 76, 104, 110, 153

Type IC restriction enzymes, 104, 153

HsdS protein variation, 251

methylation, 110

Type ID restriction enzymes, 104, 153

Type IE restriction enzymes, 104

Type II restriction enzymes, 66–75, 129–152, 305–308

amino acid similarities, 188

biochemistry of, 67–68

catalytic domains, 190–193

chimeric, 151–152

control of restriction, 211–215

by C proteins, 211–214, 212f

transcriptional control, 214

crystallography, 95–99

determination of cleavage sites for, 90–91

dimers, 91, 126

discovery of, 1, 2

DNA binding, 91–93, 92f, 93f

DNA cleavage, 70–71, 93–94

DNA recognition functions, 99–101

DNA–protein interfaces, 99

fidelity of, 71–72

gene targeting tools, 208–211, 210f

fusions, 208–209, 210f

nickases (nicking enzymes), 209, 211

generation of new specificities, 88

genes and organization, 91

growth in number of, 52, 59, 67, 188

history

1982–1993, 88–103

1993–2004, 129–152

2004–2016, 188–215

1970s, 37–46

1970s and early 1980s, 66–75

identification using MTase motifs, 58–59

isoschizomers, 66–67

metal cofactors, role of, 150–151

PD…(D/E)XK motif, 145–147, 145f, 147f, 306

percentage of bacteria carrying, 87

phase variation, 248–249

readout types, 131

in REBASE (2004), 126t

recognition of RNA–DNA hybrids, 72–73

recognition of ssDNA, 72–73

recombinant DNA uses, 44–46

selected enzymes studied in recent years, table of, 294t–303t

specific versus nonspecific enzyme–DNA interactions, 73–74

specificities, 66–67, 87, 88–89, 95, 305

structures, 127, 306

subtypes, 42–43, 128, 129–131, 130t, 185, 193–207, 305

subunit/domain composition and cleavage mechanism, 192f

transcriptional regulation of R genes by control (C) proteins and antisense promoters, 55

Type I restriction enzymes compared, 43, 307

water role in recognition, 149

Type IIA restriction enzymes, 130t

DNA cleavage, 194

methyltransferases, 194

subunit/domain composition and cleavage mechanisms, 194–195

Type IIB restriction enzymes, 43, 129, 130t, 228

cloning of, 57

DNA cleavage, 195

subunit/domain composition and cleavage mechanism, 192f, 195–196

Type I enzymes compared, 307

Type IIC restriction enzymes, 43, 90, 130t

DNA cleavage, 196

subunit/domain composition and cleavage mechanism, 192f

Type IIE restriction enzymes, 90, 129, 130t

structure and biochemistry, 138–141

subunit/domain composition and cleavage mechanism, 196–200, 197f

Type IIF restriction enzymes, 90, 129, 130t, 141–145

Type IIG restriction enzymes, 54, 129, 130t, 228

methyltransferases, 202–203

phase variation, 249

structural evolution of Type IIG enzymes from Type I enzyme, 228, 229f

subunit/domain composition and cleavage mechanism, 192f, 202–203

Type I enzymes compared, 307–308

Type IIH restriction enzymes, 90, 130t

methyltransferases, 204

subunit structure, 204

Type IIL restriction enzymes, 202, 235

Type IIM restriction enzymes, 129, 130t, 204

Type IIP restriction enzymes, 43, 89, 129, 130t

cloning of, 57

methyltransferases, 204

structure and biochemistry, 131–138

subunit/domain composition and cleavage mechanism, 192f, 204–206

Type IIS restriction enzymes, 129, 130t, 247

cloning of, 57

Golden Gate Assembly method, 319–320, 320f

isoschizomers, 89

methyltransferases, 206–207

serial analysis of gene expression (SAGE) and, 321

specificities, 89

subunit/domain composition and cleavage mechanism, 192f, 206–207

Type IIT restriction enzymes, 129, 130t, 192f, 207

Type III restriction enzymes, 77–79, 110–112, 152–162, 305–308

ATP and, 111, 236, 238, 240–241, 253, 307

characteristics of, 42

DNA cleavage, 111–112

DNA recognition and cleavage sequences of, 78

enzyme mechanisms, 111–112

genetics of, 78

history

1982–1993, 110–112

1993–2004, 155–160

2004–2016, 236–241

1970s and early 1980s, 77–79

identification, 58–59

molecular motors, 155–160, 157f, 160f

occurrence and genetics, 110–111

phase variation, 249–251

reaction mechanisms of, 78–79

in REBASE (2004), 126t

subclasses, 42–43

Type II enzymes compared, 43

Type IIS enzymes compared, 89

Type IV restriction enzymes, 305, 308

discovery of, 42, 186, 308

diversity of, 308

history (2004–2016), 241–247

modification dependence, 186, 241–247

in REBASE (2004), 126t

Type II enzymes compared, 43

U

UbaLAI

CCGG family of restriction enzymes, 194t

subunit/domain composition and cleavage mechanisms, 196, 197f

UHRF1, 243f

Uracil DNA glycosylase, 319

USER (Uracil-Specific Excision Reagent) Enzyme, 318, 319

V

Van Montagu, Marc, 50

Varmus, Harold E., 36

Venetianer, Pál, 55

Vibrio, 220

Viscometric assay for restriction enzymes, 37, 38f

von Hippel, Peter, 72, 87

Vsr endonuclease, 145, 146f

W

Wada, Chieko, 228

Walker A and B boxes, 156

Watanabe, Tsutomu

drug resistance, 21, 29, 41

scientific career, 28–29

Water, role in recognition by restriction enzymes, 149

Watson, James, 5, 52–53

Weigle, Jean

Edouard Kellenberger and, 35

host controlled variation, 5–8, 10–12, 14

photograph, 16f

Weiserova, Marie, 229

Weiss, Bernard, 38, 39f

Whole-genome sequencing, 230, 307–308

Wilcox, Kent, 37

Wilson, Geoffrey, 54–56, 91, 203

Winkler, Fritz, 132–134

Witkin, Evelyn, 5

Wood, William, 19, 30, 31, 33–34

X

Xeroderma pigmentosum, 232, 308

XmaI, 67

Y

Yoshimori, Robert, 21, 36, 41

Yuan, Robert, 31

EcoKI purification, 23–24

Thomas Bickle and, 42

Type I restriction enzymes, 75

Z

Zabeau, Marc, 69

Zavil'gel'skii, G.B., 231, 235

Zinc fingers, 127, 152, 208, 306

Zinc-finger nucleases, 208, 210f, 325

Zn2+, 188, 191

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