Repetitive non-typhoidal Salmonella exposure is an environmental risk factor for colon cancer and tumor growth

Daphne M van Elsland; Janneke W Duijster; Jilei Zhang; Virginie Stévenin; Yongguo Zhang; Lang Zha; Yinglin Xia; Eelco Franz; Jun Sun; Lapo Mughini-Gras; Jacques Neefjes

doi:10.1016/j.xcrm.2022.100852

Repetitive non-typhoidal Salmonella exposure is an environmental risk factor for colon cancer and tumor growth

Daphne M van Elsland
, Janneke W Duijster
, Jilei Zhang
, Virginie Stévenin
, Yongguo Zhang
, Lang Zha
, Yinglin Xia
, Eelco Franz
, Jun Sun^*
, Lapo Mughini-Gras^*
, Jacques Neefjes^*

^*Corresponding author for this work

IRAS OH Epidemiology Microbial Agents

Research output: Contribution to journal › Article › Academic › peer-review

Abstract

During infection, Salmonella hijacks essential host signaling pathways. These molecular manipulations disrupt cellular integrity and may induce oncogenic transformation. Systemic S. Typhi infections are linked to gallbladder cancer, whereas severe non-typhoidal Salmonella (NTS) infections are associated with colon cancer (CC). These diagnosed infections, however, represent only a small fraction of all NTS infections as many infections are mild and go unnoticed. To assess the overall impact of NTS infections, we performed a retrospective serological study on NTS exposure in patients with CC. The magnitude of exposure to NTS, as measured by serum antibody titer, is significantly positively associated with CC. Repetitively infecting mice with low NTS exposure showed similar accelerated tumor growth to that observed after high NTS exposure. At the cellular level, NTS preferably infects (pre-)transformed cells, and each infection round exponentially increases the rate of transformed cells. Thus, repetitive exposure to NTS associates with CC risk and accelerates tumor growth.

Original language	English
Article number	100852
Pages (from-to)	1-18
Journal	Cell reports. Medicine
Volume	3
Issue number	12
DOIs	https://doi.org/10.1016/j.xcrm.2022.100852
Publication status	Published - 20 Dec 2022

Bibliographical note

Funding Information:
We would like to thank Rong Lu and Shari Garrett for helping with the animal studies, Karen A. Krogfelt for help with the epidemiological study, and Marlieke Jongsma for help with the graphical abstract. This work was supported by KWF grant “Bacterial food poisoning and colon cancer; a cell biological and epidemiological study” (2017-1-11001) (to J.N. and L.M.-G.), an ERC Advanced grant ERCOPE (to J.N.), and the Netherlands Organisation for Health Research and Development ( ZonMw ) (to J.N. and L.M.-G.) (grant number 522004001 ). Mouse experiments were supported by the Oncode program from Oncode member J.N. and the UIC Cancer Center Fund for J.S. V.S. was supported by the LUMC MSCA-IF Seal of Excellence program.

Publisher Copyright:
© 2022 The Author(s)

Keywords

Salmonella
colon cancer
environmental risk factor
seroincidence

UN SDGs

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

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10.1016/j.xcrm.2022.100852Licence: CC BY

1-s2.0-S2666379122004165-mainFinal published version, 3.36 MBLicence: CC BY

Cite this

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title = "Repetitive non-typhoidal Salmonella exposure is an environmental risk factor for colon cancer and tumor growth",

abstract = "During infection, Salmonella hijacks essential host signaling pathways. These molecular manipulations disrupt cellular integrity and may induce oncogenic transformation. Systemic S. Typhi infections are linked to gallbladder cancer, whereas severe non-typhoidal Salmonella (NTS) infections are associated with colon cancer (CC). These diagnosed infections, however, represent only a small fraction of all NTS infections as many infections are mild and go unnoticed. To assess the overall impact of NTS infections, we performed a retrospective serological study on NTS exposure in patients with CC. The magnitude of exposure to NTS, as measured by serum antibody titer, is significantly positively associated with CC. Repetitively infecting mice with low NTS exposure showed similar accelerated tumor growth to that observed after high NTS exposure. At the cellular level, NTS preferably infects (pre-)transformed cells, and each infection round exponentially increases the rate of transformed cells. Thus, repetitive exposure to NTS associates with CC risk and accelerates tumor growth.",

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note = "Funding Information: We would like to thank Rong Lu and Shari Garrett for helping with the animal studies, Karen A. Krogfelt for help with the epidemiological study, and Marlieke Jongsma for help with the graphical abstract. This work was supported by KWF grant “Bacterial food poisoning and colon cancer; a cell biological and epidemiological study” (2017-1-11001) (to J.N. and L.M.-G.), an ERC Advanced grant ERCOPE (to J.N.), and the Netherlands Organisation for Health Research and Development ( ZonMw ) (to J.N. and L.M.-G.) (grant number 522004001 ). Mouse experiments were supported by the Oncode program from Oncode member J.N. and the UIC Cancer Center Fund for J.S. V.S. was supported by the LUMC MSCA-IF Seal of Excellence program. Publisher Copyright: {\textcopyright} 2022 The Author(s)",

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T1 - Repetitive non-typhoidal Salmonella exposure is an environmental risk factor for colon cancer and tumor growth

AU - van Elsland, Daphne M

AU - Duijster, Janneke W

AU - Zhang, Jilei

AU - Stévenin, Virginie

AU - Zhang, Yongguo

AU - Zha, Lang

AU - Xia, Yinglin

AU - Franz, Eelco

AU - Sun, Jun

AU - Mughini-Gras, Lapo

AU - Neefjes, Jacques

N1 - Funding Information: We would like to thank Rong Lu and Shari Garrett for helping with the animal studies, Karen A. Krogfelt for help with the epidemiological study, and Marlieke Jongsma for help with the graphical abstract. This work was supported by KWF grant “Bacterial food poisoning and colon cancer; a cell biological and epidemiological study” (2017-1-11001) (to J.N. and L.M.-G.), an ERC Advanced grant ERCOPE (to J.N.), and the Netherlands Organisation for Health Research and Development ( ZonMw ) (to J.N. and L.M.-G.) (grant number 522004001 ). Mouse experiments were supported by the Oncode program from Oncode member J.N. and the UIC Cancer Center Fund for J.S. V.S. was supported by the LUMC MSCA-IF Seal of Excellence program. Publisher Copyright: © 2022 The Author(s)

PY - 2022/12/20

Y1 - 2022/12/20

N2 - During infection, Salmonella hijacks essential host signaling pathways. These molecular manipulations disrupt cellular integrity and may induce oncogenic transformation. Systemic S. Typhi infections are linked to gallbladder cancer, whereas severe non-typhoidal Salmonella (NTS) infections are associated with colon cancer (CC). These diagnosed infections, however, represent only a small fraction of all NTS infections as many infections are mild and go unnoticed. To assess the overall impact of NTS infections, we performed a retrospective serological study on NTS exposure in patients with CC. The magnitude of exposure to NTS, as measured by serum antibody titer, is significantly positively associated with CC. Repetitively infecting mice with low NTS exposure showed similar accelerated tumor growth to that observed after high NTS exposure. At the cellular level, NTS preferably infects (pre-)transformed cells, and each infection round exponentially increases the rate of transformed cells. Thus, repetitive exposure to NTS associates with CC risk and accelerates tumor growth.

AB - During infection, Salmonella hijacks essential host signaling pathways. These molecular manipulations disrupt cellular integrity and may induce oncogenic transformation. Systemic S. Typhi infections are linked to gallbladder cancer, whereas severe non-typhoidal Salmonella (NTS) infections are associated with colon cancer (CC). These diagnosed infections, however, represent only a small fraction of all NTS infections as many infections are mild and go unnoticed. To assess the overall impact of NTS infections, we performed a retrospective serological study on NTS exposure in patients with CC. The magnitude of exposure to NTS, as measured by serum antibody titer, is significantly positively associated with CC. Repetitively infecting mice with low NTS exposure showed similar accelerated tumor growth to that observed after high NTS exposure. At the cellular level, NTS preferably infects (pre-)transformed cells, and each infection round exponentially increases the rate of transformed cells. Thus, repetitive exposure to NTS associates with CC risk and accelerates tumor growth.

KW - Salmonella

KW - colon cancer

KW - environmental risk factor

KW - seroincidence

UR - https://www.scopus.com/pages/publications/85144400919

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DO - 10.1016/j.xcrm.2022.100852

M3 - Article

C2 - 36543099

SN - 2666-3791

VL - 3

SP - 1

EP - 18

JO - Cell reports. Medicine

JF - Cell reports. Medicine

IS - 12

M1 - 100852

ER -

Repetitive non-typhoidal Salmonella exposure is an environmental risk factor for colon cancer and tumor growth

Abstract

Bibliographical note

Keywords

UN SDGs

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