Stress response and virulence-associated proteins in
Abstract
Listeria monocytogenes is a foodborne pathogen, which causes listeriosis disease among humans and other animal species. Infections in humans mainly occur in immunocompromised individuals and are caused by the consumption of ready-to-eat and raw food products contaminated with the pathogen. To ensure survival in nature, L. monocytogenes easily adapts to different environmental conditions, and that justifies the hurdles to prevent bacterial growth inside the food chain. Exposure to a single or multiple sublethal stresses, as those impaired by food processing, food matrices, and the gastrointestinal tract, can enhance tolerance of L. monocytogenes to stresses and increase its survival and pathogenesis. This chapter summarizes the current information on the adaptive response of L. monocytogenes to different stresses, namely (1) cold stress, (2) acid stress, (3) osmotic stress, (4) desiccation stress, and (5) high hydrostatic pressure, and the impact of these stresses on L. monocytogenes virulence. The objective is to provide the background information that is necessary for the development of scientifically sound control strategies to improve food safety and to reduce the uncertainty of microbial risk assessments, associated to limited knowledge on the behavior of cells capable to adapt and survive stresses.
Keywords
- Listeria monocytogenes
- stress response
- virulence
1. Introduction
Listeriosis is an atypical disease with multiple routes of infection, including aerial, cutaneous, transplacental, nosocomial, direct contact, or digestive tract. However, surveillance studies and investigation of recent outbreaks have demonstrated that the most associated transmission pathway to humans is the intake of contaminated food (digestive tract). Ready-to-eat foods, particularly refrigerated foodstuffs, such as milk and dairy products, meat and meat products, raw vegetables, and fruits, have been related to recent outbreaks [3, 4].
The food industry relies on a variety of processing and preservation methods to produce safe and healthy products with adequate shelf life and that are appreciated by consumers. These methods inactivate or inhibit the growth of pathogenic microorganisms such as
This review focuses on key issues such as the molecular mechanisms underlying
2. Cold stress response
Cold stress adaptation is a fundamental characteristic of
2.1. Listerial mechanisms of low-temperature resistance
Changes in temperature also lead to an alteration in the membrane lipid composition to maintain the ideal membrane fluidity required for proper enzyme activity and transport of solutes [12].
3. Acid stress response
Being a neutrophile (optimum pH 6 or 7),
3.1. Listerial mechanisms of acid resistance
Cellular exposure to pH stress induces the modulation of fatty acid profiles in
Under high acidic environments, two chaperonins (DnaK and GroES) and a serine protease (HtrA) have been identified and characterized in
Additional mechanisms of acid resistance such as the F0-ATPase complex, arginine deiminase system (ADI), and the glutamate decarboxylase (GAD) have been elucidated.
3.1.1. F0F1-ATPase complex
F0F1-ATPase is an enzyme organized in two distinct although physically linked domains. The catalytic part (F1) is cytoplasmic while the integral membrane domain (F0) acts as a membrane channel for proton translocation. Cytoplasmic domain may either catalyze the synthesis of adenosine triphosphate (ATP) when the protons pass into the cytoplasm through the membrane-bound domain, or hydrolyze ATP when the protons move outside of the cell. Thus, the F0F1-ATPase complex is responsible for the aerobic synthesis of ATP, as a result of protons moving into the cell, and generates a proton motive force anaerobically by expelling protons. As a consequence of the latter mechanism, F0F1-ATPase is thought to increase intracellular pH in acidic situations [25].
3.1.2. Arginine deiminase system
This system comprises three enzymes: arginine deiminase (encoded by
Arginine is transported into the cell in exchange for an ornithine molecule that is moved outside through the transporter encoded by
3.1.3. Glutamate decarboxylase system
The GAD enzyme, generally encoded by
The GAD system is crucial for
4. Osmotic stress response
Osmotic stress defines the osmotic strength variation of an organism environment, which results from desiccation or from a high content of osmotically active compounds (salt or sugars) in the environment, lowering its water activity (aw). Since the bacterial cytoplasmic membrane is permeable to water but not to most other metabolites, hyper- or hypo-osmotic shock causes an efflux or influx of water, accompanied by a concomitant decrease or an increase in intracellular volume, respectively. In general, the internal osmotic pressure is higher than that of the surrounding medium, generating turgor, the driving force for cell extension, growth, and division. Therefore, the bacterial maintenance of pressure turgor is critical to survival in osmotic stress conditions.
The maximum NaCl concentration that permits
4.1. Listerial mechanisms of osmotic resistance
Compatible solute osmoadaptation is a biphasic response in which elevated levels of potassium cation K+ (and glutamate, its counter-ion) represent a primary response, succeeded by a significant increase in cytoplasmic concentration of compatible solutes. Cells absorb osmolytes from the external environment to restore osmotic balance within cells. The solute-mediated osmoprotection stimulates the growth of cells subjected to high salt concentrations. Deletions of these osmolyte transporters reduce the growth of
In response to osmotic stress, two genes involved in cell envelope modification have been identified:
A further mechanism of osmotic adaptation is the modification of genetic expression leading to an increased or a decreased synthesis of several proteins. Salt-shock proteins are rapidly induced and overexpressed for a short time period, being similar to those induced in cold-shock response (CSPs and CAPs). Among CSPs induced in
5. Desiccation stress response
Desiccation tolerance defines the bacteria’s aptitude to survive for extended periods on a surface, deficient of nutrients and water. As so,
6. High hydrostatic pressure
A high hydrostatic pressure (HHP) represents the application of pressure in the range of 50–1000 MPa, though the inactivation of vegetative cells of bacterial species is typically reached from 300 to 700 MPa, and bacterial spores inactivation demands higher pressure levels up to 1000 MPa [48]. However, depending on the pressure level, HHP treatments can fully inactivate bacteria or impose sublethal injuries. For pressures up to 400 MPa, the integrity of Gram-positive bacterial cells and metabolic activity are maintained, with very limited cell destruction [49]. Over the last years, it has been stated that
To date, little research has been conducted regarding the mechanisms of bacterial adaptation and resistance to high pressure. Wemekamp-Kamphuis et al. [54] demonstrated that one of the responses that enable
Several pressure-induced proteins have been increasingly synthesized when compared to the synthesis of other control proteins at atmospheric pressure [55].
Several genes associated with cell formation and shape, as well as synthesis or reassembly of cell-wall constituents, in particular peptidoglycan and fatty acids, were observed to have an increased expression. Because of this, genes involved in such functions can be considered as very central in the response to high pressure. It is presumed that
Cell membranes damage by HPP may possibly be a main cause of inactivation or death in Gram-negative bacteria, but it is fallacious to admit that in Gram-positive bacteria. Cell membrane and wall stabilization in the stationary growth phase do provide a protective effect against HPP, being a major factor for the survival of HPP-induced damage [60]. Beyond cell envelope damage, HPP interferes within the nascent septal ring formation along with other associated cell-wall formation and chromosome segregation processes [59].
7. Stress impact on L. monocytogenes virulence
PrfA-dependent virulence gene cluster or LIPI-1 (
Following the complete genome sequencing of several
Involvement | Proteins/function | Ref. |
---|---|---|
Regulation | [68] | |
[69] | ||
[70] | ||
[71] | ||
Attachment and invasion | [65] | |
[72] | ||
Lysis of vacuoles | [73] | |
[74] | ||
[75] | ||
Intracellular multiplication | [76] | |
Cell-to-cell spread | [77] | |
Environmental stress response and virulence | [78] | |
[79] | ||
[80] | ||
[81] | ||
[22] | ||
[23] | ||
[29] | ||
[82] | ||
[15] | ||
[83] |
In addition to other factors, the infectious potential of
Low pH and high salt content are common factors often found in foods contaminated with
Conte et al. [31, 89] demonstrated that short-term exposure (1 h) of
Garner et al. [93] reported an intensified invasiveness of
Complementary studies demonstrate that
A further prerequisite for
Over the last years, novel trends in food production tend to preserve the natural flavor and texture of products using minimal processing. Non-thermal food preservation usually allows a significant microbial reduction, and mounting evidence also demonstrates that the conditions applied by alternative technologies may influence bacterial virulence [102]. The application of HHP has been shown not to induce mutations in the internal genes,
8. Conclusions
Exposure of
Although significant advances in our understanding on stress response and virulence potential have been achieved in the last years, there is still a need to fulfill knowledge gaps on molecular mechanisms behind
Acknowledgments
This work was supported by National Funds from FCT—Fundação para a Ciência e a Tecnologia through project UID/Multi/50016/2013. Publication in open access was co-financed by the project NORTE-01-0246-FEDER-000011, supported by Norte Portugal Regional Operational Programme (NORTE 2020), under the PORTUGAL 2020 Partnership Agreement, through the European Regional Development Fund (ERDF). Financial support for author Sofia Pereira was provided by ESF—European Social Fund, under the PORTUGAL 2020 Partnership Agreement, through doctoral fellowship NORTE-08-5369-FSE-000007_BD_1.
References
- 1.
Saavedra L, Bellomio A, Hebert EM, Minahk C, Suarez N, Sesma F. Listeria: Epidemiology, pathogenesis and novel potential treatments. In: Romano A, Giordano CF, editors. Listeria Infections: Epidemiology, Pathogenesis and Treatment. New York: Nova Science Publishers, Incorporated; 2012. pp. 67-98 - 2.
EFSA. The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2016. EFSA Journal. 2017; 15 (12):56-78 - 3.
Magalhães R, Almeida G, Ferreira V, Santos I, Silva J, Mendes MM, Pita J, Mariano G, Mâncio I, Sousa MM, Farber J, Pagotto F, Teixeira P. Cheese-related listeriosis outbreak, Portugal, March 2009 to February 2012. Euro Surveillaince. 2015; 20 (17):pii=21104 - 4.
Callejón RM, Rodríguez-Naranjo MI, Ubeda C, Hornedo-Ortega R, Garcia-Parrilla MC, Troncoso AM. Reported foodborne outbreaks due to fresh produce in the United States and European Union: Trends and causes. Foodborne Pathogens and Disease. 2015 Jan; 12 (1):32-38 - 5.
Lou Y, Yousef AE. Adaptation to sublethal environmental stresses protects Listeria monocytogenes against lethal preservation factors. Applied and Environmental Microbiology. 1997;63 (4):1252-1255 - 6.
Junttila JR, Niemelä SI, Hirn J. Minimum growth temperatures of Listeria monocytogenes and non-haemolytic Listeria. The Journal of Applied Bacteriology. 1988 Oct;65 (4):321-327 - 7.
Walker SJ, Archer P, Banks JG. Growth of Listeria monocytogenes at refrigeration temperatures. The Journal of Applied Bacteriology. 1990 Feb;68 (2):157-162 - 8.
Seeliger HPR, Jones D. Listeria. In: Sneath PHA, Mair NS, Sharpe NE, Holt JG, editors. Bergey’s Manual of Systematic Bacteriology. Vol 2. Baltimore: Williams and Wilkins; 1986. pp. 1235-1245 - 9.
Bayles DO, Annous BA, Wilkinson BJ. Cold stress proteins induced in Listeria monocytogenes in response to temperature downshock and growth at low temperatures. Applied and Environmental Microbiology. 1996 Mar;62 (3):1116-9 - 10.
Schmid B, Klumpp J, Raimann E, Loessner MJ, Stephan R, Tasara T. Role of cold shock proteins in growth of Listeria monocytogenes under cold and osmotic stress conditions. Applied and Environmental Microbiology. 2009 Mar;75 (6):1621-1627 - 11.
Liu S, Graham JE, Bigelow L, Ii PDM, Wilkinson BJ. Identification of Listeria monocytogenes genes expressed in response to growth at low temperature. Applied and Environmental Microbiology. 2002;68 (4):1697-1705 - 12.
Mansilla MC, Cybulski LE, Albanesi D, de Mendoza D. Control of membrane lipid fluidity by molecular thermosensors. Journal of Bacteriology. 2004 Oct; 186 (20):6681-6688 - 13.
Annous BA, Becker LA, Bayles DO, Labeda DP, Wilkinson BJ. Critical role of anteiso-C15:0 fatty acid in the growth of Listeria monocytogenes at low temperatures. Applied and Environmental Microbiology. 1997 Oct;63 (10):3887-3894 - 14.
Angelidis AS, Smith GM. Role of the glycine betaine and carnitine transporters in adaptation of Listeria monocytogenes to chill stress in defined medium. Applied and Environmental Microbiology. 2003 Dec;69 (12):7492-7498 - 15.
Lou MM, Smith LT. Gbu glycine betaine porter and carnitine uptake in osmotically stressed Listeria monocytogenes cells. Applied and Environmental Microbiology. 2002 Nov;68 (11):5647-5655 - 16.
Bayles DO, Wilkinson BJ. Osmoprotectants and cryoprotectants for Listeria monocytogenes . Letters in Applied Microbiology. 2000 Jan;30 (1):23-27 - 17.
Wemekamp-Kamphuis HH, Wouters JA, Sleator RD, Gahan CGM, Hill C, Abee T. Multiple deletions of the osmolyte transporters BetL, Gbu, and OpuC of Listeria monocytogenes affect virulence and growth at high osmolarity. Applied and Environmental Microbiology. 2002 Oct;68 (10):4710-4716 - 18.
Bearson S, Bearson B, Foster JW. Acid stress responses in enterobacteria. FEMS Microbiology Letters. 1997 Feb; 147 (2):173-180 - 19.
Fozo EM, Quivey RG. The fabM gene product of streptococcus mutans is responsible for the synthesis of monounsaturated fatty acids and is necessary for survival at low pH. Journal of Bacteriology. 2004; 186 (13):4152-4158 - 20.
van Schaik W, Gahan CG, Hill C. Acid-adapted Listeria monocytogenes displays enhanced tolerance against the lantibiotics nisin and lacticin 3147. Journal of Food Protection. 1999 May;62 (5):536-539 - 21.
Ryan S, Hill C, Gahan CGM. Acid stress responses in Listeria monocytogenes . Advances in Applied Microbiology. 2008;65 :67-91 - 22.
Hanawa T, Fukuda M, Kawakami H, Hirano H, Kamiya S, Yamamoto T. The Listeria monocytogenes DnaK chaperone is required for stress tolerance and efficient phagocytosis with macrophages. Cell Stress Chaperones. 1999 Jun;4 (2):118-128 - 23.
Gahan CGM, O’Mahony J, Hill C. Characterization of the groESL operon in Listeria monocytogenes : Utilization of two reporter systems (gfp and hly) for evaluating in vivo expression. Infection and Immunity. 2001 Jun;69 (6):3924-3932 - 24.
Wilson RL, Brown LL, Kirkwood-Watts D, Warren TK, Lund SA, King DS, et al. Listeria monocytogenes 10403S HtrA is necessary for resistance to cellular stress and virulence. Infection and Immunity. 2006 Jan;74 (1):765-768 - 25.
Cotter PD, Gahan CG, Hill C. Analysis of the role of the listeria monocytogenes F0F1-AtPase operon in the acid tolerance response. International Journal of Food Microbiology. 2000 Sep;60 (2-3):137-146 - 26.
Ryan S, Begley M, Gahan CGM, Hill C. Molecular characterization of the arginine deiminase system in Listeria monocytogenes : Regulation and role in acid tolerance. Environmental Microbiology. 2009 Feb;11 (2):432-445 - 27.
Lucas PM, Blancato VS, Claisse O, Magni C, Lolkema JS, Lonvaud-Funel A. Agmatine deiminase pathway genes in lactobacillus brevis are linked to the tyrosine decarboxylation operon in a putative acid resistance locus. Microbiology. 2007 Jul; 153 (7):2221-2230 - 28.
Karatzas K-AG, Suur L, O’Byrne CP. Characterization of the intracellular glutamate decarboxylase system: Analysis of its function, transcription, and role in the acid resistance of various strains of Listeria monocytogenes . Applied and Environmental Microbiology. 2012 May;78 (10):3571-3579 - 29.
Cotter PD, Gahan CG, Hill C. A glutamate decarboxylase system protects Listeria monocytogenes in gastric fluid. Molecular Microbiology. 2001 Apr;40 (2):465-475 - 30.
Gandhi M, Chikindas ML. Listeria: A foodborne pathogen that knows how to survive. International Journal of Food Microbiology. 2007 Jan; 113 (1):1-15 - 31.
Conte MP, Petrone G, Di Biase AM, Longhi C, Penta M, Tinari A, et al. Effect of acid adaptation on the fate of Listeria monocytogenes in THP-1 human macrophages activated by gamma interferon. Infection and Immunity. 2002 Aug;70 (8):4369-4378 - 32.
Jydegaard-Axelsen A-M, Hoiby PE, Holmstrom K, Russell N, Knochel S. CO2- and anaerobiosis-induced changes in physiology and gene expression of different Listeria monocytogenes strains. Applied and Environmental Microbiology. 2004 Jul;70 (7):4111-4117 - 33.
Lado BH, Yousef AE. Characteristics of Listeria monocytogenes important to food processors. In: Ryser T, Marth EH, editors. Listeria, Listeriosis and Food Safety. Boca Raton, FL: CRC Press; 2007. pp. 157-214 - 34.
Hill C, Cotter PD, Sleator RD, Gahan CGM. Bacterial stress response in Listeria monocytogenes: Jumping the hurdles imposed by minimal processing. International Dairy Journal. 2002; 12 :273-283 - 35.
Wemekamp-kamphuis HH, Sleator RD, Wouters JA, Hill C, Abee T. Molecular and physiological analysis of the role of osmolyte transporters BetL, Gbu, and OpuC in growth of Listeria monocytogenes at low temperatures. Applied and Environmental Microbiology. 2004;70 (5):2912-2918 - 36.
Sleator RD, Hill C. Bacterial osmoadaptation: The role of osmolytes in bacterial stress and virulence. FEMS Microbiology Reviews. 2002 Mar; 26 (1):49-71 - 37.
Utratna M, Shaw I, Starr E, O’Byrne CP. Rapid, transient, and proportional activation of σ(B) in response to osmotic stress in Listeria monocytogenes . Applied and Environmental Microbiology. 2011 Nov;77 (21):7841-7845 - 38.
Duché O, Trémoulet F, Glaser P, Labadie J. Salt stress proteins induced in Listeria monocytogenes . Applied and Environmental Microbiology. 2002 Apr;68 (4):1491-1498 - 39.
Wonderling LD, Wilkinson BJ, Bayles DO. The htrA (degP) gene of Listeria monocytogenes 10403S is essential for optimal growth under stress conditions. Applied and Environmental Microbiology. 2004 Apr;70 (4):1935-1943 - 40.
Vogel BF, Hansen LT, Mordhorst H, Gram L. The survival of Listeria monocytogenes during long term desiccation is facilitated by sodium chloride and organic material. International Journal of Food Microbiology. 2010 Jun 15;140 (2-3):192-200 - 41.
Amezaga M, Davidson I, McLaggan D, Verheul A, Abee T, Booth I. The role of peptide metabolism in the growth of Listeria monocytogenes ATCC 23074 at high osmolarity. Microbiology. 1995 Jan;141 (1):41-49 - 42.
Nolan DA, Chamblin DC, Troller JA. Minimal water activity levels for growth and survival of Listeria monocytogenes andListeria innocua . International Journal of Food Microbiology. 1992 Aug;16 (4):323-335 - 43.
Zoz F, Iaconelli C, Lang E, Iddir H, Guyot S, Grandvalet C, et al. Control of relative air humidity as a potential means to improve hygiene on surfaces: A preliminary approach with Listeria monocytogenes . Almeida A, editor. PLoS One. 2016 Feb;11 (2):e0148418 - 44.
Overney A, Chassaing D, Carpentier B, Guillier L, Firmesse O. Development of synthetic media mimicking food soils to study the behaviour of listeria monocytogenes on stainless steel surfaces. International Journal of Food Microbiology. 2016 Dec;238 :7-14 - 45.
Hingston PA, Piercey MJ, Hansen LT. Genes associated with desiccation and osmotic stress in Listeria monocytogenes as revealed by insertional mutagenesis. Applied and Environmental Microbiology. 2015 Aug;81 (16):5350-5362 - 46.
Hansen LT, Vogel BF. Desiccation of adhering and biofilm Listeria monocytogenes on stainless steel: Survival and transfer to salmon products. International Journal of Food Microbiology. 2011 Mar;146 (1):88-93 - 47.
Hingston P, Chen J, Dhillon BK, Laing C, Bertelli C, Gannon V, et al. Genotypes associated with Listeria monocytogenes isolates displaying impaired or enhanced tolerances to cold, salt, acid, or desiccation stress. Frontiers in Microbiology. 2017 Mar;8 :369 - 48.
Smelt JPP. Recent advances in the microbiology of high pressure processing. Trends in Food Science & Technology. 1998 Apr; 9 (4):152-158 - 49.
Ritz M, Pilet MF, Jugiau F, Rama F, Federighi M. Inactivation of salmonella Typhimurium and listeria monocytogenes using high-pressure treatments: Destruction or sublethal stress? Letters in Applied Microbiology. 2006;42 (4):357-362 - 50.
Jantzen MM, Navas J, de Paz M, Rodriguez B, da Silva WP, Nunez M, et al. Evaluation of ALOA plating medium for its suitability to recover high pressure-injured Listeria monocytogenes from ground chicken meat. Letters in Applied Microbiology. 2006 Sep;43 (3):313-317 - 51.
Bozoglu F, Alpas H, Kaletunç G. Injury recovery of foodborne pathogens in high hydrostatic pressure treated milk during storage. FEMS Immunology and Medical Microbiology. 2004 Apr; 40 (3):243-247 - 52.
Bull MK, Hayman MM, Stewart CM, Szabo EA, Knabel SJ. Effect of prior growth temperature, type of enrichment medium, and temperature and time of storage on recovery of Listeria monocytogenes following high pressure processing of milk. International Journal of Food Microbiology. 2005;101 (1):53-61 - 53.
Kilimann K, Hartmann C, Delgado A, Vogel R, Ganzle M. A fuzzy logic-based model for the multistage high-pressure inactivation of ssp. MG 1363. International Journal of Food Microbiology. 2005 Jan; 98 (1):89-105 - 54.
Wemekamp-Kamphuis HH, Wouters JA, de Leeuw PPLA, Hain T, Chakraborty T, Abee T. Identification of sigma factor B-controlled genes and their impact on acid stress, high hydrostatic pressure, and freeze survival in Listeria monocytogenes EGD-e. Applied and Environmental Microbiology. 2004 Jun;70 (6):3457-3466 - 55.
Welch TJ, Farewell A, Neidhardt FC, Bartlett DH. Stress response of Escherichia coli to elevated hydrostatic pressure. Journal of Bacteriology. 1993 Nov;175 (22):7170-7177 - 56.
Liu Y, Ream A. Gene expression profiling of Listeria monocytogenes strain F2365 during growth in ultrahigh-temperature-processed skim milk. Applied and Environmental Microbiology. 2008 Nov;74 (22):6859-6866 - 57.
Malone AS, Chung Y-K, Yousef AE. Genes of Escherichia coli O157:H7 that are involved in high-pressure resistance. Applied and Environmental Microbiology. 2006 Apr;72 (4):2661-2671 - 58.
Scortti M, Monzó HJ, Lacharme-Lora L, Lewis DA, Vázquez-Boland JA. The PrfA virulence regulon. Microbes and Infection. 2007 Aug; 9 (10):1196-1207 - 59.
Bowman JP, Bittencourt CR, Ross T. Differential gene expression of Listeria monocytogenes during high hydrostatic pressure processing. Microbiology. 2008;154 (2):462-475 - 60.
Mañas P, Mackey BM. Morphological and physiological changes induced by high hydrostatic pressure in exponential- and stationary-phase cells of Escherichia coli: Relationship with cell death. Applied and Environmental Microbiology. 2004 Mar; 70 (3):1545-1554 - 61.
Freitag NE, Port GC, Miner MD. Listeria monocytogenes —From saprophyte to intracellular pathogen. Nature Reviews. Microbiology. 2009 Sep;7 (9):623-628 - 62.
Kazmierczak MJ, Mithoe SC, Boor KJ, Wiedmann M. Listeria monocytogenes sigma B regulates stress response and virulence functions. Journal of Bacteriology. 2003 Oct;185 (19):5722-5734 - 63.
Nadon CA, Bowen BM, Wiedmann M, Boor KJ. Sigma B contributes to PrfA-mediated virulence in Listeria monocytogenes . Infection and Immunity. 2002;70 (7):3948 - 64.
Leimeister-Wächter M, Haffner C, Domann E, Goebel W, Chakraborty T. Identification of a gene that positively regulates expression of listeriolysin, the major virulence factor of listeria monocytogenes . Proceedings of the National Academy of Sciences of the United States of America. 1990;87 (21):8336 - 65.
Gaillard JL, Berche P, Frehel C, Gouln E, Cossart P, Gouin E, et al. Entry of L. monocytogenes into cells is mediated by internalin, a repeat protein reminiscent of surface antigens from gram-positive cocci. Cell. 1991 Jun;65 (7):1127-1141 - 66.
Kuhn M, Goebel W. Internalization of listeria monocytogenes by nonprofessional and professional phagocytes. In: Oelschlaeger TA, Hacker JH, editors. Bacterial Invasion into Eukaryotic Cells Subcellular Biochemistry. Vol. 33. Boston, MA: Springer; 2000. pp. 411-436 - 67.
Roche SM, Velge P, Liu D. Virulence determination, section II identification and detection. In: Liu D, editor. Handbook of Listeria monocytogenes . Boca Raton: CRC Press, Taylor & Francis Group; 2008. pp. 241-270 - 68.
Kreft J, Vázquez-Boland JA. Regulation of virulence genes in Listeria. International Journal of Medical Microbiology. 2001; 291 :145-157 - 69.
Wiedmann M, Arvik TJ, Hurley RJ, Boor KJ. General stress transcription factor sigmaB and its role in acid tolerance and virulence of Listeria monocytogenes . Journal of Bacteriology. 1998 Jul;180 (14):3650-3656 - 70.
Karatzas KAG, Wouters JA, Gahan CGM, Hill C, Abee T, Bennik MHJ. The CtsR regulator of Listeria monocytogenes contains a variant glycine repeat region that affects piezotolerance, stress resistance, motility and virulence. Molecular Microbiology. 2003 Sep;49 (5):1227-1238 - 71.
van der Veen S, Abee T. HrcA and DnaK are important for static and continuous-flow biofilm formation and disinfectant resistance in listeria monocytogenes . Microbiology. 2010 Dec;156 (12):3782-3790 - 72.
Bierne H, Cossart P. InlB, a surface protein of Listeria monocytogenes that behaves as an invasin and a growth factor. Journal of Cell Science. 2002 Sep;115 (Pt 17):3357-3367 - 73.
Cossart P, Vicente MF, Mengaud J, Baquero F, Perez-Diaz JC, Berche P. Listeriolysin O is essential for virulence of listeria monocytogenes : Direct evidence obtained by gene complementation. Infection and Immunity. 1989 Nov;57 (11):3629-3636 - 74.
Marquis H, Doshi V, Portnoy DA. The broad-range phospholipase C and a metalloprotease mediate listeriolysin O-independent escape of Listeria monocytogenes from a primary vacuole in human epithelial cells. Infection and Immunity. 1995 Nov;63 (11):4531-4534 - 75.
Poyart C, Abachin E, Razafimanantsoa I, Berche P. The zinc metalloprotease of Listeria monocytogenes is required for maturation of phosphatidylcholine phospholipase C: Direct evidence obtained by gene complementation. Infection and Immunity. 1993 Apr;61 (4):1576-1580 - 76.
Chico-Calero I, Suarez M, Gonzalez-Zorn B, Scortti M, Slaghuis J, Goebel W, et al. Hpt, a bacterial homolog of the microsomal glucose-6-phosphate translocase, mediates rapid intracellular proliferation in Listeria. Proceedings of the National Academy of Sciences. 2002 Jan; 99 (1):431-436 - 77.
Kocks C, Gouin E, Tabouret M, Berche P, Ohayon H, Cossart P. L. monocytogenes -induced actin assembly requires the actA gene product, a surface protein. Cell. 1992 Feb;68 (3):521-531 - 78.
Stack HM, Sleator RD, Bowers M, Hill C, Gahan CGM. Role for HtrA in stress induction and virulence potential in Listeria monocytogenes . Applied and Environmental Microbiology. 2005 Aug;71 (8):4241-4247 - 79.
Dussurget O, Cabanes D, Dehoux P, Lecuit M, Buchrieser C, Glaser P, et al. Listeria monocytogenes bile salt hydrolase is a PrfA-regulated virulence factor involved in the intestinal and hepatic phases of listeriosis. Molecular Microbiology. 2002 Aug;45 (4):1095-1106 - 80.
Rouquette C, de Chastellier C, Nair S, Berche P. The ClpC ATPase of Listeria monocytogenes is a general stress protein required for virulence and promoting early bacterial escape from the phagosome of macrophages. Molecular Microbiology. 1998 Mar;27 (6):1235-1245 - 81.
Gaillot O, Pellegrini E, Bregenholt S, Nair S, Berche P. The ClpP serine protease is essential for the intracellular parasitism and virulence of Listeria monocytogenes . Molecular Microbiology. 2000 Mar;35 (6):1286-1294 - 82.
Sleator RD, Gahan CG, Abee T, Hill C. Identification and disruption of BetL, a secondary glycine betaine transport system linked to the salt tolerance of Listeria monocytogenes LO28. Applied and Environmental Microbiology. 1999 May;65 (5):2078-2083 - 83.
Angelidis AS, Smith LT, Hoffman LM, Smith GM. Identification of opuC as a chill-activated and osmotically activated carnitine transporter in Listeria monocytogenes . Applied and Environmental Microbiology. 2002 Jun;68 (6):2644-2650 - 84.
Roche SM, Gracieux P, Milohanic E, Albert I, Virlogeux-Payant I, Temoin S, et al. Investigation of specific substitutions in virulence genes characterizing phenotypic groups of low-virulence field strains of Listeria monocytogenes . Applied and Environmental Microbiology. 2005 Oct;71 (10):6039-6048 - 85.
Johansson J, Mandin P, Renzoni A, Chiaruttini C, Springer M, Cossart P. An RNA thermosensor controls expression of virulence genes in Listeria monocytogenes . Cell. 2002 Sep;110 (5):551-561 - 86.
Loh E, Dussurget O, Gripenland J, Vaitkevicius K, Tiensuu T, Mandin P, et al. A trans-acting Riboswitch controls expression of the virulence regulator PrfA in Listeria monocytogenes . Cell. 2009 Nov;139 (4):770-779 - 87.
Buncic S, Avery SM, Rogers AR. Listeriolysin O production and pathogenicity of non-growing Listeria monocytogenes stored at refrigeration temperature. International Journal of Food Microbiology. 1996 Aug;31 (1-3):133-147 - 88.
Cole MB, Jones MV, Holyoak C. The effect of pH, salt concentration and temperature on the survival and growth of Listeria monocytogenes . The Journal of Applied Bacteriology. 1990 Jul;69 (1):63-72 - 89.
Conte M, Petrone G, Di Biase A, Ammendolia M, Superti F, Seganti L. Acid tolerance in Listeria monocytogenes influences invasiveness of enterocyte-like cells and macrophage-like cells. Microbial Pathogenesis. 2000 Sep;29 (3):137-144 - 90.
Sue D, Fink D, Wiedmann M, Boor KJ. Sigma B-dependent gene induction and expression in Listeria monocytogenes during osmotic and acid stress conditions simulating the intestinal environment. Microbiology. 2004 Nov;150 (11):3843-3855 - 91.
Rieu A, Guzzo J, Piveteau P. Sensitivity to acetic acid, ability to colonize abiotic surfaces and virulence potential of Listeria monocytogenes EGD-e after incubation on parsley leaves. Journal of Applied Microbiology. 2010 Feb;108 (2):560-570 - 92.
Kouassi Y, Shelef LA. Listeriolysin O secretion by Listeria monocytogenes in broth containing salts of organic acids. Journal of Food Protection. 1995;58 (12):1314-1319 - 93.
Garner MR, James KE, Callahan MC, Wiedmann M, Boor KJ. Exposure to salt and organic acids increases the ability of Listeria monocytogenes to invade Caco-2 cells but decreases its ability to survive gastric stress. Applied and Environmental Microbiology. 2006;72 (8):5384-5395 - 94.
Kim H, Boor KJ, Marquis H. Listeria monocytogenes B contributes to invasion of human intestinal epithelial cells. Infection and Immunity. 2004 Dec;72 (12):7374-7378 - 95.
Kim H, Marquis H, Boor KJ. B contributes to Listeria monocytogenes invasion by controlling expression of inlA and inlB. Microbiology. 2005 Oct;151 (10):3215-3222 - 96.
Dramsi S, Kocks C, Forestier C, Cossart P. Internalin-mediated invasion of epithelial cells by Listeria monocytogenes is regulated by the bacterial growth state, temperature and the pleiotropic activator prfA. Molecular Microbiology. 1993 Sep;9 (5):931-941 - 97.
O’Driscoll B, Gahan CG, Hill C. Adaptive acid tolerance response in Listeria monocytogenes : Isolation of an acid-tolerant mutant which demonstrates increased virulence. Applied and Environmental Microbiology. 1996 May;62 (5):1693-1698 - 98.
Cotter PD, Emerson N, Gahan CG, Hill C. Identification and disruption of lisRK, a genetic locus encoding a two-component signal transduction system involved in stress tolerance and virulence in Listeria monocytogenes . Journal of Bacteriology. 1999 Nov;181 (21):6840-6843 - 99.
Sleator RD, Francis GA, O’Beirne D, Gahan CGM, Hill C. Betaine and carnitine uptake systems in Listeria monocytogenes affect growth and survival in foods and during infection. Journal of Applied Microbiology. 2003;95 (4):839-846 - 100.
Sleator RD, Gahan CGM, O’Driscoll B, Hill C. Analysis of the role of betL in contributing to the growth and survival of Listeria monocytogenes LO28. International Journal of Food Microbiology. 2000 Sep;60 (2-3):261-268 - 101.
Joseph B, Przybilla K, Stuhler C, Schauer K, Slaghuis J, Fuchs TM, et al. Identification of Listeria monocytogenes genes contributing to intracellular replication by expression profiling and mutant screening. Journal of Bacteriology. 2006 Jan;188 (2):556-568 - 102.
van Schaik W, Abee T. The role of σB in the stress response of Gram-positive bacteria—Targets for food preservation and safety. Current Opinion in Biotechnology. 2005 Apr; 16 (2):218-224 - 103.
Van Boeijen IKH, Casey PG, Hill C, Moezelaar R, Zwietering MH, Gahan CGM, et al. Virulence aspects of Listeria monocytogenes LO28 high pressure-resistant variants. Microbial Pathogenesis. 2013 Jun;59-60 :48-51