The Secretion of Toxins and Other Exoproteins of Cronobacter: Role in Virulence, Adaption, and Persistence

Hyein Jang; Gopal R. Gopinath; Athmanya Eshwar; Shabarinath Srikumar; Scott Nguyen; Jayanthi Gangiredla; Isha R. Patel; Samantha B. Finkelstein; Flavia Negrete; Jung Ha Woo; You Young Lee; Séamus Fanning; Roger Stephan; Ben D. Tall; Angelika Lehner

doi:10.3390/microorganisms8020229

The Secretion of Toxins and Other Exoproteins of Cronobacter: Role in Virulence, Adaption, and Persistence

Hyein Jang, Gopal R. Gopinath, Athmanya Eshwar, Shabarinath Srikumar, Scott Nguyen, Jayanthi Gangiredla, Isha R. Patel, Samantha B. Finkelstein, Flavia Negrete, Jung Ha Woo, You Young Lee, Séamus Fanning, Roger Stephan, Ben D. Tall^*, Angelika Lehner

^*Corresponding author for this work

Research output: Contribution to journal › Review article › peer-review

31 Citations (Scopus)

49 Downloads (Pure)

Abstract

Cronobacter species are considered an opportunistic group of foodborne pathogenic bacteria capable of causing both intestinal and systemic human disease. This review describes common virulence themes shared among the seven Cronobacter species and describes multiple exoproteins secreted by Cronobacter, many of which are bacterial toxins that may play a role in human disease. The review will particularly concentrate on the virulence factors secreted by C. sakazakii, C. malonaticus, and C. turicensis, which are the primary human pathogens of interest. It has been discovered that various species-specific virulence factors adversely affect a wide range of eukaryotic cell processes including protein synthesis, cell division, and ion secretion. Many of these factors are toxins which have been shown to also modulate the host immune response. These factors are encoded on a variety of mobile genetic elements such as plasmids and transposons; this genomic plasticity implies ongoing re-assortment of virulence factor genes which has complicated our efforts to categorize Cronobacter into sharply defined genomic pathotypes.

Original language	English
Article number	229
Journal	Microorganisms
Volume	8
Issue number	2
DOIs	https://doi.org/10.3390/microorganisms8020229
Publication status	Published - 08 Feb 2020
Externally published	Yes

Bibliographical note

Funding Information:
This research was internally funded through U.S. FDA appropriations, and in part by the University of Maryland JIFSAN Program through a cooperative agreement with the FDA (no. FDU001418). Acknowledgments: We thank the student internship programs sponsored by the Office of International Affairs of Gachon University, Gyeonggi, Republic of Korea for supporting student interns, JungHa Woo and YouYoung Lee. We thank the University of Maryland, Joint Institute for Food Safety and Applied Nutrition (JIFSAN) for supporting JIFSAN interns, Samantha Finkelstein and Flavia Negrete. We also thank the Oak Ridge Institute for Science and Education, Oak Ridge, Tennessee for sponsoring research fellow Hyein Jang.

Publisher Copyright:
© 2020 by the authors. Licensee MDPI, Basel, Switzerland.

Keywords

Adherence factors
Efflux pumps
Iron transport
Osmotic stress response
Outer membrane proteins
Plasmids
Protein secretion systems
Quorum sensing systems
Virulence factors

ASJC Scopus subject areas

Microbiology
Microbiology (medical)
Virology

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.3390/microorganisms8020229Licence: CC BY

The Secretion of Toxins and Other Exoproteins of Cronobacter: Role in Virulence, Adaption, and Persistence
Copyright 2020 the authors. This is an open access article published under a Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution and reproduction in any medium, provided the author and source are cited.
Final published version, 1.26 MBLicence: CC BY

Cite this

Jang, H., Gopinath, G. R., Eshwar, A., Srikumar, S., Nguyen, S., Gangiredla, J., Patel, I. R., Finkelstein, S. B., Negrete, F., Woo, J. H., Lee, Y. Y., Fanning, S., Stephan, R., Tall, B. D., & Lehner, A. (2020). The Secretion of Toxins and Other Exoproteins of Cronobacter: Role in Virulence, Adaption, and Persistence. Microorganisms, 8(2), Article 229. https://doi.org/10.3390/microorganisms8020229

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title = "The Secretion of Toxins and Other Exoproteins of Cronobacter: Role in Virulence, Adaption, and Persistence",

abstract = "Cronobacter species are considered an opportunistic group of foodborne pathogenic bacteria capable of causing both intestinal and systemic human disease. This review describes common virulence themes shared among the seven Cronobacter species and describes multiple exoproteins secreted by Cronobacter, many of which are bacterial toxins that may play a role in human disease. The review will particularly concentrate on the virulence factors secreted by C. sakazakii, C. malonaticus, and C. turicensis, which are the primary human pathogens of interest. It has been discovered that various species-specific virulence factors adversely affect a wide range of eukaryotic cell processes including protein synthesis, cell division, and ion secretion. Many of these factors are toxins which have been shown to also modulate the host immune response. These factors are encoded on a variety of mobile genetic elements such as plasmids and transposons; this genomic plasticity implies ongoing re-assortment of virulence factor genes which has complicated our efforts to categorize Cronobacter into sharply defined genomic pathotypes.",

keywords = "Adherence factors, Efflux pumps, Iron transport, Osmotic stress response, Outer membrane proteins, Plasmids, Protein secretion systems, Quorum sensing systems, Virulence factors",

author = "Hyein Jang and Gopinath, {Gopal R.} and Athmanya Eshwar and Shabarinath Srikumar and Scott Nguyen and Jayanthi Gangiredla and Patel, {Isha R.} and Finkelstein, {Samantha B.} and Flavia Negrete and Woo, {Jung Ha} and Lee, {You Young} and S{\'e}amus Fanning and Roger Stephan and Tall, {Ben D.} and Angelika Lehner",

note = "Funding Information: This research was internally funded through U.S. FDA appropriations, and in part by the University of Maryland JIFSAN Program through a cooperative agreement with the FDA (no. FDU001418). Acknowledgments: We thank the student internship programs sponsored by the Office of International Affairs of Gachon University, Gyeonggi, Republic of Korea for supporting student interns, JungHa Woo and YouYoung Lee. We thank the University of Maryland, Joint Institute for Food Safety and Applied Nutrition (JIFSAN) for supporting JIFSAN interns, Samantha Finkelstein and Flavia Negrete. We also thank the Oak Ridge Institute for Science and Education, Oak Ridge, Tennessee for sponsoring research fellow Hyein Jang. Publisher Copyright: {\textcopyright} 2020 by the authors. Licensee MDPI, Basel, Switzerland.",

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Jang, H, Gopinath, GR, Eshwar, A, Srikumar, S, Nguyen, S, Gangiredla, J, Patel, IR, Finkelstein, SB, Negrete, F, Woo, JH, Lee, YY, Fanning, S, Stephan, R, Tall, BD & Lehner, A 2020, 'The Secretion of Toxins and Other Exoproteins of Cronobacter: Role in Virulence, Adaption, and Persistence', Microorganisms, vol. 8, no. 2, 229. https://doi.org/10.3390/microorganisms8020229

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T1 - The Secretion of Toxins and Other Exoproteins of Cronobacter: Role in Virulence, Adaption, and Persistence

AU - Jang, Hyein

AU - Gopinath, Gopal R.

AU - Eshwar, Athmanya

AU - Srikumar, Shabarinath

AU - Nguyen, Scott

AU - Gangiredla, Jayanthi

AU - Patel, Isha R.

AU - Finkelstein, Samantha B.

AU - Negrete, Flavia

AU - Woo, Jung Ha

AU - Lee, You Young

AU - Fanning, Séamus

AU - Stephan, Roger

AU - Tall, Ben D.

AU - Lehner, Angelika

N1 - Funding Information: This research was internally funded through U.S. FDA appropriations, and in part by the University of Maryland JIFSAN Program through a cooperative agreement with the FDA (no. FDU001418). Acknowledgments: We thank the student internship programs sponsored by the Office of International Affairs of Gachon University, Gyeonggi, Republic of Korea for supporting student interns, JungHa Woo and YouYoung Lee. We thank the University of Maryland, Joint Institute for Food Safety and Applied Nutrition (JIFSAN) for supporting JIFSAN interns, Samantha Finkelstein and Flavia Negrete. We also thank the Oak Ridge Institute for Science and Education, Oak Ridge, Tennessee for sponsoring research fellow Hyein Jang. Publisher Copyright: © 2020 by the authors. Licensee MDPI, Basel, Switzerland.

PY - 2020/2/8

Y1 - 2020/2/8

N2 - Cronobacter species are considered an opportunistic group of foodborne pathogenic bacteria capable of causing both intestinal and systemic human disease. This review describes common virulence themes shared among the seven Cronobacter species and describes multiple exoproteins secreted by Cronobacter, many of which are bacterial toxins that may play a role in human disease. The review will particularly concentrate on the virulence factors secreted by C. sakazakii, C. malonaticus, and C. turicensis, which are the primary human pathogens of interest. It has been discovered that various species-specific virulence factors adversely affect a wide range of eukaryotic cell processes including protein synthesis, cell division, and ion secretion. Many of these factors are toxins which have been shown to also modulate the host immune response. These factors are encoded on a variety of mobile genetic elements such as plasmids and transposons; this genomic plasticity implies ongoing re-assortment of virulence factor genes which has complicated our efforts to categorize Cronobacter into sharply defined genomic pathotypes.

AB - Cronobacter species are considered an opportunistic group of foodborne pathogenic bacteria capable of causing both intestinal and systemic human disease. This review describes common virulence themes shared among the seven Cronobacter species and describes multiple exoproteins secreted by Cronobacter, many of which are bacterial toxins that may play a role in human disease. The review will particularly concentrate on the virulence factors secreted by C. sakazakii, C. malonaticus, and C. turicensis, which are the primary human pathogens of interest. It has been discovered that various species-specific virulence factors adversely affect a wide range of eukaryotic cell processes including protein synthesis, cell division, and ion secretion. Many of these factors are toxins which have been shown to also modulate the host immune response. These factors are encoded on a variety of mobile genetic elements such as plasmids and transposons; this genomic plasticity implies ongoing re-assortment of virulence factor genes which has complicated our efforts to categorize Cronobacter into sharply defined genomic pathotypes.

KW - Adherence factors

KW - Efflux pumps

KW - Iron transport

KW - Osmotic stress response

KW - Outer membrane proteins

KW - Plasmids

KW - Protein secretion systems

KW - Quorum sensing systems

KW - Virulence factors

U2 - 10.3390/microorganisms8020229

DO - 10.3390/microorganisms8020229

M3 - Review article

AN - SCOPUS:85079481079

SN - 2076-2607

VL - 8

JO - Microorganisms

JF - Microorganisms

IS - 2

M1 - 229

ER -

The Secretion of Toxins and Other Exoproteins of Cronobacter: Role in Virulence, Adaption, and Persistence

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

UN SDGs

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