Oxidative Stress Responses in Escherichia Coli and Salmonella Typhimurium

Oxidative Stress Responses in Escherichia Coli and Salmonella Typhimurium

MICROBIOLOGICAL REVIEWS, Dec. 1991, p. 561-585 Vol. 55, No. 4 0146-07 49/91/040561-25$02. 00/0 Copyright © 1991, American Society for Microbiology Oxidative Stress Responses in Escherichia coli and Salmonella typhimurium SPENCER B. FARR1* AND TOKIO KOGOMA2 Department of Molecular and Cellular Toxicology, Harvard School of Public Health, Boston, Massachusetts 02115, 1 and Departments ofCell Biology and Microbiology, University of New Mexico Medical Center, Albuquerque, New Mexico 87131 2 INTRODUCTION AND SCOPE OF REVIEW ............................................................................ 561 OXIDATIVE STRESS RESPONSES .........................................................................................562 Active Oxygen Species ......................................................................................................... 562 Reactivities .....••••.•.......................•............................•.........•.......................................... 562 Sources ......................................•................•.......•.•.•..................................••...••....•.......563 Oxidative Stress and Cellular Responses .........................................................•.......•..•••••....•...563 Peroxide stress response •................•.......•.............................................................•...........564 Su peroxide stress response ...............•..........•.•........•....••....••.....................••.•••••...••.•..•..•..•.564 The two oxidative stress responses are distinct .......................................................................564 OXIDATIVE STRESS-INDUCIBLE PROTEINS .........................................................................564 Peroxide Stress Proteins ..........••..•..................................•......................................••.....•......565 0 2 - Stress Proteins ............................................................................................................ 566 Overlaps with Other Stress Responses .................................................................................... 566 Heat shock response ........................................................................................................ 566 Carbon starvation response .......................•.•.•...................•..•............••......•.•.....•...............567 SOS response ................................................................................................................. 567 REGULATION OF CELLULAR RESPONSES TO OXIDATIVE STRESS ....................................... 567 OxyR Regulon .•..•••...........................•.•.•.......................•.......•..••................•..................•.... 567 Positive regulatory protein, OxyR .......................................................................................567 Direct activation of OxyR by oxidative stress ........................................................................568 SoxRS Regulon ................................•.............•.•.•.....................................•...•.........•........•..568 Isolation of Sox(Con) mutants ............................................................................................568 The soxR locus encodes two proteins ................................................................................... 568 Pleiotropic effects of soxR(Con) mutations ............................................................................569 Other Factors Involved in Regulation of SoxRS Regulon Genes ....................................................569 Multilayered Regulation of SodA Expression ............................................................................ 569 KatF (RpoS) Regulon ..........................................................................................................569 AppppN, Heat Shock, and Oxidative Stress .............................................................................570 Summary ......................................................................................................................... 570 PHYSIOLOGICAL ROLE OF RESPONSES IN OXIDATIVE STRESS ........................................... 571 Prevention of Oxidative Damage ...................................•...•............................••..•...................571 Oxidative Damage and Repair ...•.•........................................•.............................•..•..•••.......•.572 DNA damage .................................................................................................................. 572 Mutagenicity ....................•••.................................•.•..•.............•..............•.•••...................574 DNA damage and transcription ..........................................................................................575 Membrane damage ..........................................................................................................576 Protein damage ...............................................................................................................576 Role of the Peroxide Stress Response ...................................................................................... 577 Role of the Superoxide Stress Response ................................................................................... 577 Possible Role of the Stringent Response .................................................................................. 578 Other Genes Involved in Protection against Oxidative Stress ....................................................... 578 CONCLUSIONS ................................................................................................................... 578 Comparison and Extrapolation to Eukaryotes .......................................................................... 578 ACKNOWLEDGMENTS ........................................................................................................ 579 REFERENCES .....................................................................................................................579 INTRODUCTION AND SCOPE OF REVIEW been shown to cause damage to DNA, RNA, protein, and lipids. Active oxygen species are produced as an ines­ Oxidative stress can be functionally defined as an excess capable by-product of normal aerobic metabolism, and their of prooxidants in the cell. Active oxygen molecules have production is further enhanced by exposure to certain envi­ ronments or by dietary or disease conditions. Oxygen tox­ icity results when the degree of oxidative stress exceeds the * Corresponding author. capacity of the cell defense systems. Oxidative stress is 561 562 FARR AND KOGOMA MICROBIOL. REV. strongly implicated in a number of diseases such as rheuma­ three electrons to form, respectively, a superoxide radical toid arthritis, inflammatory bowel disorders, and atheroscle­ (02-), hydrogen peroxide (H20 2), and hydroxyl radicals rosis (102, 104). It is also emerging as one of the most (OH"), or when it undergoes a spin flip to become singlet important causative agents of mutagenesis, tumorigenesis, oxygen (1Ig 0 2) (76, 112). The overall four-electron reduc­ and aging (1, 3-5, 40, 75). Virtually all aerobic organisms tion of molecular oxygen to water is shown below. have evolved complex defense and repair mechanisms to e-,2H+ e-,H+ e-,H+ mitigate the damaging effects of active oxygen (160, 161). Because of the powerful genetic techniques available for 02~ 02- ~ H202 ~ OH"~ H20 manipulations in bacteria, tremendous progress has been ! (pKa 4.8) made toward understanding the genetic and physiological HOO" responses to oxidative stress in bacteria. Many aerobic bacteria tested to date appear to encode multigene responses Under more acidic conditions, 0 2- can be protonated to to oxidative stress (for example, see reference 25). In this form HOO" (hydroperoxyl radical) (19). article, we will summarize what has been learned to date Reactivities. 0 2- will oxidize thiols, ascorbate, toco­ about cellular responses to oxidative stress, primarily in pherol, and catecholamines (78, 112, 156). Proteins contain­ Escherichia coli and Salmonella typhimurium. We will ing (Fe-S)4 clusters are highly sensitive to attack by 0 2- briefly describe the reactivities of active species of oxygen, (80). Probably the most important reactions of 0 2- are its detail the genetics and molecular biology of oxidative stress spontaneous dismutation to H20 2 + 0 2 and its ability to responses, and discuss the physiological role of the re­ reduce transition metals and metal complexes. Spontaneous sponses in oxidative stress. More recently, responses anal­ dismutation of 0 2- in aqueous neutral pH environments ogous to those first characterized in bacteria have been produces H20 2 (78). As mentioned above, when 0 2- is found in mammalian cells (e.g., 55a, 131, 185a). We will protonated, the hydroperoxyl radical (HOO") is produced conclude by briefly reviewing the similarities and differences (02- + H+ - HOO"). The Hoo· radical is much more between oxidative stress responses in bacteria and eukary­ reactive than 0 2- because the negative charge has been otic organisms. neutralized. The pKa of this species is 4.8. Thus, at physio­ This review is intended to be comprehensive and self­ logical pH, the ratio of 0 2- to its protonated form would be contained so that most readers will obtain a current picture about 100:1. When the pH of the cell (or mitochondria) of the field without frequent consultation with references. decreases,

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