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Helicobacter and Salmonella Persistent Infection Strategies Downloaded from http://perspectivesinmedicine.cshlp.org/ on September 25, 2021 - Published by Cold Spring Harbor Laboratory Press Helicobacter and Salmonella Persistent Infection Strategies Denise M. Monack Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, California 94305 Correspondence: [email protected] Some host-adapted bacterial pathogens are capable of causing persistent infections in humans. For example, Helicobacter pylori inhabits the human gastric mucosa and persis- tence can be lifelong. Salmonella enterica serovar Typhi causes systemic infections that involve colonization of the reticuloendothelial system and some individuals become lifelong carriers. In this review, I compare and contrast the different lifestyles of Helicobacter and Salmonella within the host and the strategies they have evolved to persist in mammalian hosts. Persistently infected carriers serve as the reservoirs for these pathogens, and the carrier state is an essential feature that is required for survival of the bacteria within a restricted host population. Therefore, investigating the chronic carrier state should provide insight into bacterial survival strategies, as well as new therapeutic approaches for treatments. n infection with a pathogenic microorgan- the absence of clinical symptoms, infection Oism, the host usually responds by activat- poses some risk to the host. For example, H. py- ing the innate and adaptive immune responses. lori induce gastritis with varying degrees of se- If the host survives the initial battle, the adaptive verity. In addition, individuals who are chroni- immune response usually clears the foreign in- cally infectedwithS.Typhihaveanincreasedrisk vader. However, some pathogens have evolved of developing hepatobiliary cancer. Although a the capacity to survive the initial robust im- deeper understanding of the mechanisms of pa- mune response and persist. The persistent phase thology and disease caused by chronic Helico- www.perspectivesinmedicine.org of infection usually involves a complex balance bacter and Salmonella infections is important, of protective immunity and immunopathology. this work focuses on the mechanisms of persis- The interactions between the host and pathogen tent colonization and transmission. are very complex and likely reflect the coevolu- tion and fine tuning of bacterial virulence PERSISTENT H. PYLORI INFECTIONS mechanisms and host immune responses. Persistent colonizationwith the human-spe- H. pylori infection is an important example of a cific bacterial pathogens Helicobacter pylori and persistent bacterial pathogen that is usually ac- Salmonella enterica serovar Typhi (S. Typhi) are quired in early childhood and lasts for a lifetime. usually not clinically apparent. However, even in The majority of those infected (80%–90%) will Editors: Pascale Cossart and Stanley Maloy Additional Perspectives on Bacterial Pathogenesis available at www.perspectivesinmedicine.org Copyright # 2013 Cold Spring Harbor Laboratory Press; all rights reserved; doi: 10.1101/cshperspect.a010348 Cite this article as Cold Spring Harb Perspect Med 2013;3:a010348 1 Downloaded from http://perspectivesinmedicine.cshlp.org/ on September 25, 2021 - Published by Cold Spring Harbor Laboratory Press D.M. Monack carry and transmit H. pylori without any symp- et al. 2011). For example, CheW, CheA, CheY, toms of disease (Hunt 1996; Amieva and El- and ChePep H. pylori mutants are defective for Omar 2008). In some ways, H. pylori behave colonizing the mouse stomach when in compe- like commensal bacteria and not pathogens. tition with wild-type H. pylori (Terry et al. 2005; However, this bacterium has evolved to success- Williams et al. 2007; Howitt et al. 2011). Recent fully colonize the hostile environment of the hu- results with the ChePep-deficient H. pylori mu- man stomach in the face of a constant innate and tant in a mouse model suggest that chemotaxis adaptive immune response. Although most in- is essential for colonizing the glands of the an- fected people do not develop disease, three main trum of stomachs (Fig. 1). Both wild-type and gastric phenotypes have been identified. The DChePep strains colonize the mucus layer over- most common, a “benign gastritis” phenotype, lying the stomach surface. In contrast, the is seen in asymptomatic subjects, who on the DChePep mutant is not found in the glandular whole do not develop serious gastrointestinal region (Howitt et al. 2011). Taken together, disease. The second, a “duodenal ulcer” pheno- these results indicate that chemotaxis is impor- type, accounts for up to 15% of infected sub- tant in allowing the bacteria to colonize a spe- jects. The third, a “gastric cancer” phenotype, cialized niche and in locating or persisting with- is more serious and affects 1% of infected sub- in the mid-glands. This tropism for the mid- jects as a result of a chronic inflammation in- glandular zone is intriguing because the gastric duced by the infection and increases the risk of progenitor cells are known to reside in this re- gastric cancer (Hunt 1996; Amieva and El-Omar gion and a direct association with H. pylori and 2008). Most basic research focuses on the diseas- gastric progenitor cells could be related to the esthat are caused by H. pylori, the host factors for increased gastric cancerassociated with H. pylori disease, and the bacterial virulence determi- infection (Uemura et al. 2001; Qiao et al. 2007). nants. Here, we focus on the bacterial and host factors that contribute to the ability of this path- Life on the Surface of Gastric ogen to persist. Epithelial Cells Once the bacteria reach the microenvironment Chemotaxis Is Required for Persistence of the epithelial lining, they survive as two major H. pylori colonize the harsh environment of the populations: one that is free-swimming in the human stomach. To survive their journey mucus gel and a second population (20%) through the acidic stomach, H. pylori generate found directly adhered to the epithelial surface large quantities of cytosolic and cell surface-as- via multiple adhesins (Hessey et al. 1990; Ilver www.perspectivesinmedicine.org sociated urease. Urease is an enzyme that breaks et al. 1998; Mahdavi et al. 2002). The more vir- down urea to generate ammonia and carbon ulent strains of H. pylori have contact-depen- dioxide and transiently buffers the acidic envi- dent mechanisms to interact with and modify ronment (Merrell et al. 2003; Pflock et al. 2006). epithelial cells, including a type IV secretion sys- Rather than persisting in the lumen of the stom- tem that injects the virulence factor CagA into ach, H. pylori have evolved mechanisms to reach host cells (Segal et al. 1999; Asahi et al. 2000; and colonize a very narrow anatomical niche Backert et al. 2000; Odenbreit et al. 2000; Stein (25–30 mm) near the surface of the epithelial et al. 2000). CagA has multiple effects on epi- cells (Schreiber et al. 2004). The ability to reach thelial cells, including the ability to modify api- this niche is dependent on sensing pH gradients cal junctions and perturb cell polarity (Amieva and chemotaxis away from low pH (Ottemann et al. 2003; Bagnoli et al. 2005; Murata-Kamiya and Lowenthal 2002; Schreiber et al. 2004, 2005; et al. 2007; Saadat et al. 2007; Zeaiteret al. 2008). Croxen et al. 2006). Mutant H. pylori that are CagA affects multiple host cell signaling path- defective for sensing low pH and chemotaxis are ways, which are the subject of many reviews. defective in their ability to colonize the stom- However, the functions of CagA that benefit achs of mice (Howitt et al. 2011; Lertsethtakarn the bacteria have only recently been described 2 Cite this article as Cold Spring Harb Perspect Med 2013;3:a010348 Downloaded from http://perspectivesinmedicine.cshlp.org/ on September 25, 2021 - Published by Cold Spring Harbor Laboratory Press Helicobacter/Salmonella: Infection Strategies A 7 D 6 5 4 3 Log CFU/g 2 1 wt ΔChePeP ΔChePeP B 7 6 5 4 3 Log CFU/g 2 1 wt Wt ΔChePeP C 1000 P < 0.0001 EF G 100 10 1 in glands/section Hp wt ΔChePeP Figure 1. Chemotaxis is essential for H. pylori colonization of the antral gastric glands and colonization of the mouse stomach. (A) Colony-forming units (CFU) of H. pylori in the stomachs of mice colonized with either the wild-type or DChePep mutant for 2 weeks. Each marker represents an individual mouse. (B) CFU counts from the mice coinfected with both the wild-type and DChePep mutant in a 1:1 ratio for 2 weeks. The dashed line indicates the limit of detection. P , 0.0001. (C) Volumetric analysis of bacteria colonizing the antral glands calculated from 100-mm-thick sections imaged by three-dimensional (3D) confocal microscopy from single infections of either the wild-type or DChePep mutant. (D) 3D confocal microscopy of murine stomachs infected with either wild-type or DChePep mutant. F-actin is stained with phalloidin (red) and nuclei (blue), and H. pylori cells (green) are immunolabeled. Asterisks indicate H. pylori cells in the surface mucus of the stomach, whereas a box highlights bacterial colonies in mid-glands. (E) Magnified view of the area boxed in panel D.(F) Scanning electron microscopy (SEM) of wild-type infected gland. (G) Magnified view of area boxed in panel F. www.perspectivesinmedicine.org Scale bars, 100 mm(D), 10 mm(E) and (F), and 2 mm(G). Hp, Helicobacter pylori; wt, wild type. (Hatakeyama 2004; Peek 2005; Suzuki et al. larity of the transferrin/transferrin receptor 2006; Handa et al. 2007; Hatakeyama 2008; iron uptake system by a mechanism that de- Backert et al. 2010, 2011; Murata-Kamiya pends on CagA and another major virulence 2011). Using a polarized epithelium model sys- factor, VacA (Tanet al. 2011). CagA is important tem, CagA was found to play an important role in promoting iron acquisition in vivo. This was in enabling H. pylori colonization of the epithe- shown in a Mongolian gerbil model by compar- lium (Tan et al. 2009).
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