Pancreatic Amylase Is an Environmental Signal for Regulation of Biofilm Formation and Host Interaction in Campylobacter jejuni

Jowiya, Waheed; Brunner, K. T.; Abouelhadid, Sherif; Hussain, Haitham; Nair, Sean P.; Sadiq, Sohaib; Williams, Lisa; Trantham, Emma K.; Stephenson, Holly; Wren, Brendan W.; Bajaj-Elliott, Mona; Cogan, Tristan A; Laws, Andrew P.; Wade, Jim; Dorrell, Nick; Allan, Elaine

doi:10.1128/iai.01064-15

Cited by 10 publications

(8 citation statements)

References 67 publications

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“…jejuni and inactivation of each has been linked to the attenuation of C . jejuni physiology, virulence, and/or immunogenicity (Brondsted et al, ; Jowiya et al, ; Karlyshev et al, ). The enhanced proteolytic activity of 11168H ST‐OMVs indirectly indicates a more pathogenic C .…”

Section: Discussionmentioning

confidence: 99%

“…*, p < .05. ST = sodium taurocholate; PBS = phosphate buffered saline; OMVs = outer membrane vesicles linked to the attenuation of C. jejuni physiology, virulence, and/or immunogenicity(Brondsted et al, 2005;Jowiya et al, 2015;Karlyshev et al, 2014). The enhanced proteolytic activity of 11168H ST-OMVs indirectly indicates a more pathogenic C. jejuni response during colonisation of a host after the bacteria senses bile salts.…”

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confidence: 99%

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The bile salt sodium taurocholate inducesCampylobacter jejuniouter membrane vesicle production and increases OMV-associated proteolytic activity

Elmi

Dorey

Watson

et al. 2017

Cellular Microbiology

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Campylobacter jejuni, the leading cause of bacterial acute gastroenteritis worldwide, secretes an arsenal of virulence-associated proteins within outer membrane vesicles (OMVs). C. jejuni OMVs contain three serine proteases (HtrA, Cj0511, and Cj1365c) that cleave the intestinal epithelial cell (IEC) tight and adherens junction proteins occludin and E-cadherin, promoting enhanced C. jejuni adhesion to and invasion of IECs. C. jejuni OMVs also induce IECs innate immune responses. The bile salt sodium taurocholate (ST) is sensed as a host signal to coordinate the activation of virulence-associated genes in the enteric pathogen Vibrio cholerae. In this study, the effect of ST on C. jejuni OMVs was investigated. Physiological concentrations of ST do not have an inhibitory effect on C. jejuni growth until the early stationary phase. Coculture of C. jejuni with 0.1% or 0.2% (w/v) ST stimulates OMV production, increasing both lipid and protein concentrations. C. jejuni ST-OMVs possess increased proteolytic activity and exhibit a different protein profile compared to OMVs isolated in the absence of ST. ST-OMVs exhibit enhanced cytotoxicity and immunogenicity to T84 IECs and enhanced killing of Galleria mellonella larvae. ST increases the level of mRNA transcripts of the OMVs-associated serine protease genes and the cdtABC operon that encodes the cytolethal distending toxin. Coculture with ST significantly enhances the OMVs-induced cleavage of E-cadherin and occludin. C. jejuni OMVs also cleave the major endoplasmic reticulum chaperone protein BiP/GRP78 and this activity is associated with the Cj1365c protease. These data suggest that C. jejuni responds to the presence of physiological concentrations of the bile salt ST that increases OMV production and the synthesis of virulence-associated factors that are secreted within the OMVs. We propose that these events contribute to pathogenesis.

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

The bile salt sodium taurocholate inducesCampylobacter jejuniouter membrane vesicle production and increases OMV-associated proteolytic activity

Elmi

Dorey

Watson

et al. 2017

Cellular Microbiology

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“…Host signals also play a role; a recent study showed that C. jejuni 11168 can produce a glucan biofilm composed of α-dextran as a specific response to the presence of host pancreatic amylase (Jowiya et al, 2015). In contrast to the clear stimulatory effect of glucose on biofilm formation we found here, the only other sugar known to be metabolized by campylobacters, L -fucose, was very recently shown to reduce biofilm formation in the C. jejuni NCTC 11168 strain (Dwivedi et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

Glucose Metabolism via the Entner-Doudoroff Pathway in Campylobacter: A Rare Trait that Enhances Survival and Promotes Biofilm Formation in Some Isolates

et al. 2016

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Isolates of the zoonotic pathogen Campylobacter are generally considered to be unable to metabolize glucose due to lack of key glycolytic enzymes. However, the Entner-Doudoroff (ED) pathway has been identified in Campylobacter jejuni subsp. doylei and a few C. coli isolates. A systematic search for ED pathway genes in a wide range of Campylobacter isolates and in the C. jejuni/coli PubMLST database revealed that 1.7% of >6,000 genomes encoded a complete ED pathway, including both C. jejuni and C. coli from diverse clinical, environmental and animal sources. In rich media, glucose significantly enhanced stationary phase survival of a set of ED-positive C. coli isolates. Unexpectedly, glucose massively promoted floating biofilm formation in some of these ED-positive isolates. Metabolic profiling by gas chromatography–mass spectrometry revealed distinct responses to glucose in a low biofilm strain (CV1257) compared to a high biofilm strain (B13117), consistent with preferential diversion of hexose-6-phosphate to polysaccharide in B13117. We conclude that while the ED pathway is rare amongst Campylobacter isolates causing human disease (the majority of which would be of agricultural origin), some glucose-utilizing isolates exhibit specific fitness advantages, including stationary-phase survival and biofilm production, highlighting key physiological benefits of this pathway in addition to energy conservation.

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“…Although the formation of C . jejuni biofilms is not fully understood, as with many other bacteria they contain DNA [ 7 , 12 ] and polysaccharide [ 13 ].…”

Section: Introductionmentioning

confidence: 99%

Campylobacter jejuni CsrA Regulates Metabolic and Virulence Associated Proteins and Is Necessary for Mouse Colonization

Fields

Gulbronson

et al. 2016

PLoS ONE

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Campylobacter jejuni infection is a leading bacterial cause of gastroenteritis and a common antecedent leading to Gullian-Barré syndrome. Our previous data suggested that the RNA-binding protein CsrA plays an important role in regulating several important phenotypes including motility, biofilm formation, and oxidative stress resistance. In this study, we compared the proteomes of wild type, csrA mutant, and complemented csrA mutant C. jejuni strains in an effort to elucidate the mechanisms by which CsrA affects virulence phenotypes. The putative CsrA regulon was more pronounced at stationary phase (111 regulated proteins) than at mid-log phase (25 regulated proteins). Proteins displaying altered expression in the csrA mutant included diverse metabolic functions, with roles in amino acid metabolism, TCA cycle, acetate metabolism, and various other cell processes, as well as pathogenesis-associated characteristics such as motility, chemotaxis, oxidative stress resistance, and fibronectin binding. The csrA mutant strain also showed altered autoagglutination kinetics when compared to the wild type. CsrA specifically bound the 5’ end of flaA mRNA, and we demonstrated that CsrA is a growth-phase dependent repressor of FlaA expression. Finally, the csrA mutant exhibited reduced ability to colonize in a mouse model when in competition with the wild type, further underscoring the role of CsrA in C. jejuni colonization and pathogenesis.

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Pancreatic Amylase Is an Environmental Signal for Regulation of Biofilm Formation and Host Interaction in Campylobacter jejuni

Cited by 10 publications

References 67 publications

The bile salt sodium taurocholate inducesCampylobacter jejuniouter membrane vesicle production and increases OMV-associated proteolytic activity

The bile salt sodium taurocholate inducesCampylobacter jejuniouter membrane vesicle production and increases OMV-associated proteolytic activity

Glucose Metabolism via the Entner-Doudoroff Pathway in Campylobacter: A Rare Trait that Enhances Survival and Promotes Biofilm Formation in Some Isolates

Campylobacter jejuni CsrA Regulates Metabolic and Virulence Associated Proteins and Is Necessary for Mouse Colonization

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