Mutation for survival

Current Opinion in Genetics and Development

Volumn 7, Issue 6, 1997, Pages 829-834

  Rosenberg, Susan M ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PLASMID DNA;

ANIMAL CELL; DNA SYNTHESIS; GENE MUTATION; GENETIC RECOMBINATION; GENETIC SELECTION; GENOME; HERITABILITY; HUMAN; HUMAN CELL; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; REVIEW; STRESS;

EID: 0031446430     PISSN: 0959437X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-437X(97)80047-0     Document Type: Article

References (50)

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22. Prival M, Cebula T. Adaptive mutation and slow growing revertants of an Escherichia coli lacZ amber mutant. of special interest Genetics. 144:1996;1337-1341 The authors find that the apparently post-selection reversions of an E. coli lac amber mutation originally described by Cairns [1] are mostly suppressor mutations that cause slow growth in the presence of an excess of non-mutant cells such as those that are present on the selective lactose plates. Thus, these can be accounted for as mutations that formed prior to selection. Cairns [1] had shown that their mutants were not slow-growing on lactose but had done so in the absence of an excess of non-mutant competitors. A similar test of revertants of Cairns's and Foster's lac frameshift strain reveals no such slow growth artifact (G McKenzie, M-J Lombardo, SM Rosenberg, unpublished data).
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30. Taddei F, Halliday JA, Matic I, Radman M. Genetic analysis of mutagenesis in aging E. coli colonies. of special interest Mol Gen Genet. 256:1997;277-281 The authors of this paper report stationary-phase mutations the genetic requirements of which are strikingly similar to recombination-dependent stationary-phase mutations discussed here. It is a good bet that the same or a similar mechanism is at work.
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33. of outstanding interest Foster PL, Trimarchi JM, Maurer RA. Two enzymes, both of which process recombination intermediates, have opposite effects on adaptive mutation in Escherichia coli. of special interest Genetics. 142:1996;25-37 This paper, along with that of Harris [34], shows that proteins required for resolution of strand-exchange recombination intrmediates are required for adaptive Lac reversion. This implies that strand-exchange intermediates are also intermediates in recombination-dependent mutation. Of further interest, these authors report that overexpression of MutS plus MutL inhibited growth-dependent as well as stationary-phase Lac reversion - apparently disagreeing with the finding of Harris [49], that only stationary-phase, not growth-dependent, mutation is inhibited by excess MutL (with or without MutS). In that paper, Harris show that the apparent depression in growth-dependent mutation is caused by scoring mutants without taking into consideration the slow-growth of colonies of the overexpressing strains.
34. Harris RS, Ross KJ, Rosenberg SM. Opposing roles of the Holliday junction processing systems of Escherichia coli in recombination-dependent adaptive mutation. of special interest Genetics. 142:1996;681-691 This paper demonstrates opposite roles for the two strand-exchange intermediate resolution systems in recombination-dependent stationary-phase Lac mutation. The RuvABC system is required whereas RecG protein inhibits mutation. Thus recombination intermediates are also intermediates in rec-dependent mutation and are processed differently by the two systems, as also reported by Foster [33]. Additionally, a transient lack of both systems causes hypermutation, indicating that the intermediates are mutagenic. However, those intermediates must be resolved ultimately for viable mutant colonies to be obtained. Note that a direct physical demonstration that the recombination intermediate occurs in the region mutated has not been made (see Figure 1 legend).
35. Foster PL, Trimarchi JM. Adaptive reversion of a frameshift mutation in Escherichia coli by simple base deletions in homopolymeric runs. Science. 265:1994;407-409.
36. Rosenberg SM, Longerich S, Gee P, Harris RS. Adaptive mutation by deletions in small mononucleotide repeats. Science. 265:1994;405-407.
37. Foster PL, Gudmundsson G, Trimarchi JM, Cai H, Goodman MF. Proofreading-defective DNA polymerase II increases adaptive mutative in Escherichia coli. Proc Natl Acad Sci USA. 92:1995;7951-7955.
38. Harris RS, Bull HJ, Rosenberg SM. A direct role for DNA polymerase III in adaptive reversion of a frameshift mutation in Escherichia coli. Mutat Res. 375:1997;19-24.
39. Longerich S, Galloway AM, Harris RS, Wong C, Rosenberg SM. Adaptive mutation sequences reproduced by mismatch repair deficiency. Proc Natl Acad Sci USA. 92:1995;12017-12020.
40. Benson S. Adaptive mutation: a general phenomenon or a special case? Bioessays. 19:1997;9-11.
41. + and the unselected mutation are not independent events because the same DSBs, recombination events, and possibly the same DNA synthesis events that lead to mutation in one gene may cause the mutations in the other.
42. Torkelson J, Harris RS, Lombardo M-J, Nagendran J, Thulin C, Rosenberg SM. Genome-wide hypermutation in a subpopulation of stationary-phase cells underlies recombination-dependent adaptive mutation. of outstanding interest EMBO J. 16:1997;3303-3311 This paper puts to rest the two most contentious issues in the field of adaptive mutation and includes the discovery of two more important points. First, the data demonstrate that the recombination-dependent adaptive mutation mechanism can occur in genes other than the selected gene (also shown by [41]). Thus these adaptive mutations are not directed, á la Lamarck. Second, the mutagenesis is not sex plasmid specific, as many had contended it would be [7-9, 40]. All replicons in the cell including the bacterial chromosome experience the mutagenesis. The most widely cited reason for discounting the general applicability of results from this mutation assay system was the worry that these mutations were sex plasmid specific. Third, a small hypermutable subpopulation of the stressed cells is shown to give rise to the stationary-phase mutants. Fourth, the chromosome is shown to have hot and cold places for the stationary-phase mutations, perhaps explaining the few cold sites described previously, and in other systems (discussed in main text).
43. Hall BG. Spontaneous point mutations that occur more often when advantageous than when neutral. Genetics. 126:1990;5-16.
44. of outstanding interest Michel B, Ehrlich SD, Uzest M. DNA double-strand breaks caused by replication arrest. of special interest EMBO J. 16:1997;430-438 Arrest of replication forks produces physically-detectable DSBs in the bacterial chromosome. Though not discussed by these authors, this could be a source of the DSBs that promote chromosomal mutations of Torkelson [42].
45. Bridges BA. Hypermutation under stress. of special interest Nature. 387:1997;557-558 This article reviews aspects of work described in [41] and [42]. The authors suggest that the oxidative damage may cause the DSBs that provoke recombination-dependent mutation. Oxidative damage is a good candidate for the source of DSBs in recombination-dependent stationary-phase mutation.
46. Modrich P. Mismatch repair, genetic stability, and cancer. Science. 266:1994;1959-1960.
47. Radman M, Matic I, Halliday JA, Taddei F. Editing DNA replication and recombination by mismatch repair: from bacterial genetics to mechanisms of predisposition to cancer in humans. Phil Trans R Soc London. 347:1995;97-103.
48. Feng G, Tsui H-CT, Winkler ME. Depletion of the cellular amounts of the MutS and MutH methyl-directed mismatch repair proteins in stationary-phase Escherichia coli K-12 cells. J Bacteriol. 178:1996;2388-2396.
49. Harris RS, Feng G, Thulin C, Ross KJ, Sidhu R, Longerich S, Szigety SK, Winkler ME, Rosenberg SM. Mismatch repair protein MutL becomes limiting during stationary-phase mutation. of outstanding interest Genes Dev. 11:1997;2426-2437 This is the first report for any organism that the post-replicative MMR repair system is not constitutively active but can be modulated. The MMR protein MutL is shown to become limiting for MMR function during stationary-phase mutation and is not limiting during growth. Profound consequences in cancer, development, and evolution follow from this discovery, and an important regulatory component, MutL, is identified.
50. Razavy H, Szigety SK, Rosenberg SM. Evidence for both 3′ and 5′ single-strand DNA ends in intermediates in Chi stimulated recombination in vivo. of special interest Genetics. 142:1996;333-339 A recombination paper that both presents new and reviews old evidence supporting 3′ and 5′ single-strand DNA ends as substrates used for recombinational strand-invasion in the RecBCD DSB-repair system of E. coli. The consequences of these conclusions bear on the choice of 3′ polarities only in mutation and both polarities in recombination as discussed by Harris [34]. See also Figure 1.