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