Cigarette smoke promotes colorectal cancer through modulation of gut microbiota and related metabolites

ObjectiveCigarette smoking is a major risk factor for colorectal cancer (CRC). We aimed to investigate whether cigarette smoke promotes CRC by altering the gut microbiota and related metabolites.DesignAzoxymethane-treated C57BL/6 mice were exposed to cigarette smoke or clean air 2 hours per day for...

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Vydáno v:	Gut Ročník 71; číslo 12; s. 2439 - 2450
Hlavní autoři:	Bai, Xiaowu, Wei, Hong, Liu, Weixin, Coker, Olabisi Oluwabukola, Gou, Hongyan, Liu, Changan, Zhao, Liuyang, Li, Chuangen, Zhou, Yunfei, Wang, Guoping, Kang, Wei, Ng, Enders Kwok-wai, Yu, Jun
Médium:	Journal Article
Jazyk:	angličtina
Vydáno:	London BMJ Publishing Group Ltd and British Society of Gastroenterology 01.12.2022 BMJ Publishing Group LTD BMJ Publishing Group
Témata:	Air cleanliness Animal models Azoxymethane BACTERIAL PATHOGENESIS BILE ACID METABOLISM Cigarette smoke Cigarette smoking Cigarettes COLORECTAL CANCER Colorectal carcinoma Dysbacteriosis Epithelium Extracellular signal-regulated kinase Germfree Gut Microbiome Gut microbiota Intestinal microflora Kinases Laboratory animals Liquid chromatography MAP kinase Mass spectroscopy Metabolic pathways Metabolites Metabolomics Metagenomics Microbiota Protein kinase Proteins Risk factors Signal transduction Smoking Taurodeoxycholic acid Tumors United States > US China
ISSN:	0017-5749, 1468-3288, 1468-3288
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Abstract	ObjectiveCigarette smoking is a major risk factor for colorectal cancer (CRC). We aimed to investigate whether cigarette smoke promotes CRC by altering the gut microbiota and related metabolites.DesignAzoxymethane-treated C57BL/6 mice were exposed to cigarette smoke or clean air 2 hours per day for 28 weeks. Shotgun metagenomic sequencing and liquid chromatography mass spectrometry were parallelly performed on mice stools to investigate alterations in microbiota and metabolites. Germ-free mice were transplanted with stools from smoke-exposed and smoke-free control mice.ResultsMice exposed to cigarette smoke had significantly increased tumour incidence and cellular proliferation compared with smoke-free control mice. Gut microbial dysbiosis was observed in smoke-exposed mice with significant differential abundance of bacterial species including the enrichment of Eggerthella lenta and depletion of Parabacteroides distasonis and Lactobacillus spp. Metabolomic analysis showed increased bile acid metabolites, especially taurodeoxycholic acid (TDCA) in the colon of smoke-exposed mice. We found that E. lenta had the most positive correlation with TDCA in smoke-exposed mice. Moreover, smoke-exposed mice manifested enhanced oncogenic MAPK/ERK (mitogen-activated protein kinase/extracellular signal‑regulated protein kinase 1/2) signalling (a downstream target of TDCA) and impaired gut barrier function. Furthermore, germ-free mice transplanted with stools from smoke-exposed mice (GF-AOMS) had increased colonocyte proliferation. Similarly, GF-AOMS showed increased abundances of gut E. lenta and TDCA, activated MAPK/ERK pathway and impaired gut barrier in colonic epithelium.ConclusionThe gut microbiota dysbiosis induced by cigarette smoke plays a protumourigenic role in CRC. The smoke-induced gut microbiota dysbiosis altered gut metabolites and impaired gut barrier function, which could activate oncogenic MAPK/ERK signalling in colonic epithelium.
AbstractList	Cigarette smoking is a major risk factor for colorectal cancer (CRC). We aimed to investigate whether cigarette smoke promotes CRC by altering the gut microbiota and related metabolites.OBJECTIVECigarette smoking is a major risk factor for colorectal cancer (CRC). We aimed to investigate whether cigarette smoke promotes CRC by altering the gut microbiota and related metabolites.Azoxymethane-treated C57BL/6 mice were exposed to cigarette smoke or clean air 2 hours per day for 28 weeks. Shotgun metagenomic sequencing and liquid chromatography mass spectrometry were parallelly performed on mice stools to investigate alterations in microbiota and metabolites. Germ-free mice were transplanted with stools from smoke-exposed and smoke-free control mice.DESIGNAzoxymethane-treated C57BL/6 mice were exposed to cigarette smoke or clean air 2 hours per day for 28 weeks. Shotgun metagenomic sequencing and liquid chromatography mass spectrometry were parallelly performed on mice stools to investigate alterations in microbiota and metabolites. Germ-free mice were transplanted with stools from smoke-exposed and smoke-free control mice.Mice exposed to cigarette smoke had significantly increased tumour incidence and cellular proliferation compared with smoke-free control mice. Gut microbial dysbiosis was observed in smoke-exposed mice with significant differential abundance of bacterial species including the enrichment of Eggerthella lenta and depletion of Parabacteroides distasonis and Lactobacillus spp. Metabolomic analysis showed increased bile acid metabolites, especially taurodeoxycholic acid (TDCA) in the colon of smoke-exposed mice. We found that E. lenta had the most positive correlation with TDCA in smoke-exposed mice. Moreover, smoke-exposed mice manifested enhanced oncogenic MAPK/ERK (mitogen-activated protein kinase/extracellular signal‑regulated protein kinase 1/2) signalling (a downstream target of TDCA) and impaired gut barrier function. Furthermore, germ-free mice transplanted with stools from smoke-exposed mice (GF-AOMS) had increased colonocyte proliferation. Similarly, GF-AOMS showed increased abundances of gut E. lenta and TDCA, activated MAPK/ERK pathway and impaired gut barrier in colonic epithelium.RESULTSMice exposed to cigarette smoke had significantly increased tumour incidence and cellular proliferation compared with smoke-free control mice. Gut microbial dysbiosis was observed in smoke-exposed mice with significant differential abundance of bacterial species including the enrichment of Eggerthella lenta and depletion of Parabacteroides distasonis and Lactobacillus spp. Metabolomic analysis showed increased bile acid metabolites, especially taurodeoxycholic acid (TDCA) in the colon of smoke-exposed mice. We found that E. lenta had the most positive correlation with TDCA in smoke-exposed mice. Moreover, smoke-exposed mice manifested enhanced oncogenic MAPK/ERK (mitogen-activated protein kinase/extracellular signal‑regulated protein kinase 1/2) signalling (a downstream target of TDCA) and impaired gut barrier function. Furthermore, germ-free mice transplanted with stools from smoke-exposed mice (GF-AOMS) had increased colonocyte proliferation. Similarly, GF-AOMS showed increased abundances of gut E. lenta and TDCA, activated MAPK/ERK pathway and impaired gut barrier in colonic epithelium.The gut microbiota dysbiosis induced by cigarette smoke plays a protumourigenic role in CRC. The smoke-induced gut microbiota dysbiosis altered gut metabolites and impaired gut barrier function, which could activate oncogenic MAPK/ERK signalling in colonic epithelium.CONCLUSIONThe gut microbiota dysbiosis induced by cigarette smoke plays a protumourigenic role in CRC. The smoke-induced gut microbiota dysbiosis altered gut metabolites and impaired gut barrier function, which could activate oncogenic MAPK/ERK signalling in colonic epithelium. ObjectiveCigarette smoking is a major risk factor for colorectal cancer (CRC). We aimed to investigate whether cigarette smoke promotes CRC by altering the gut microbiota and related metabolites.DesignAzoxymethane-treated C57BL/6 mice were exposed to cigarette smoke or clean air 2 hours per day for 28 weeks. Shotgun metagenomic sequencing and liquid chromatography mass spectrometry were parallelly performed on mice stools to investigate alterations in microbiota and metabolites. Germ-free mice were transplanted with stools from smoke-exposed and smoke-free control mice.ResultsMice exposed to cigarette smoke had significantly increased tumour incidence and cellular proliferation compared with smoke-free control mice. Gut microbial dysbiosis was observed in smoke-exposed mice with significant differential abundance of bacterial species including the enrichment of Eggerthella lenta and depletion of Parabacteroides distasonis and Lactobacillus spp. Metabolomic analysis showed increased bile acid metabolites, especially taurodeoxycholic acid (TDCA) in the colon of smoke-exposed mice. We found that E. lenta had the most positive correlation with TDCA in smoke-exposed mice. Moreover, smoke-exposed mice manifested enhanced oncogenic MAPK/ERK (mitogen-activated protein kinase/extracellular signal‑regulated protein kinase 1/2) signalling (a downstream target of TDCA) and impaired gut barrier function. Furthermore, germ-free mice transplanted with stools from smoke-exposed mice (GF-AOMS) had increased colonocyte proliferation. Similarly, GF-AOMS showed increased abundances of gut E. lenta and TDCA, activated MAPK/ERK pathway and impaired gut barrier in colonic epithelium.ConclusionThe gut microbiota dysbiosis induced by cigarette smoke plays a protumourigenic role in CRC. The smoke-induced gut microbiota dysbiosis altered gut metabolites and impaired gut barrier function, which could activate oncogenic MAPK/ERK signalling in colonic epithelium.
Author	Ng, Enders Kwok-wai Li, Chuangen Bai, Xiaowu Wei, Hong Coker, Olabisi Oluwabukola Liu, Changan Liu, Weixin Kang, Wei Gou, Hongyan Zhao, Liuyang Zhou, Yunfei Yu, Jun Wang, Guoping
AuthorAffiliation	1 Institute of Digestive Disease and The Department of Medicine and Therapeutics, State Key Laboratory of Digestive Disease, Li Ka Shing Institute of Health Sciences, CUHK Shenzhen Research Institute , The Chinese University of Hong Kong , Hong Kong , China 2 Department of Surgery , The Chinese University of Hong Kong , Hong Kong , China 4 Department of Anatomical and Cellular Pathology , The Chinese University of Hong Kong , Hong Kong , China 3 Department of Precision Medicine, The First Affiliated Hospital , Sun Yat-Sen University , Guangzhou , Guangdong , China
AuthorAffiliation_xml	– name: 1 Institute of Digestive Disease and The Department of Medicine and Therapeutics, State Key Laboratory of Digestive Disease, Li Ka Shing Institute of Health Sciences, CUHK Shenzhen Research Institute , The Chinese University of Hong Kong , Hong Kong , China – name: 3 Department of Precision Medicine, The First Affiliated Hospital , Sun Yat-Sen University , Guangzhou , Guangdong , China – name: 2 Department of Surgery , The Chinese University of Hong Kong , Hong Kong , China – name: 4 Department of Anatomical and Cellular Pathology , The Chinese University of Hong Kong , Hong Kong , China
Author_xml	– sequence: 1 givenname: Xiaowu surname: Bai fullname: Bai, Xiaowu organization: Department of Surgery, The Chinese University of Hong Kong, Hong Kong, China – sequence: 2 givenname: Hong surname: Wei fullname: Wei, Hong organization: Department of Precision Medicine, The First Affiliated Hospital, Sun Yat-Sen University, Guangzhou, Guangdong, China – sequence: 3 givenname: Weixin surname: Liu fullname: Liu, Weixin organization: Institute of Digestive Disease and The Department of Medicine and Therapeutics, State Key Laboratory of Digestive Disease, Li Ka Shing Institute of Health Sciences, CUHK Shenzhen Research Institute, The Chinese University of Hong Kong, Hong Kong, China – sequence: 4 givenname: Olabisi Oluwabukola surname: Coker fullname: Coker, Olabisi Oluwabukola organization: Institute of Digestive Disease and The Department of Medicine and Therapeutics, State Key Laboratory of Digestive Disease, Li Ka Shing Institute of Health Sciences, CUHK Shenzhen Research Institute, The Chinese University of Hong Kong, Hong Kong, China – sequence: 5 givenname: Hongyan surname: Gou fullname: Gou, Hongyan organization: Institute of Digestive Disease and The Department of Medicine and Therapeutics, State Key Laboratory of Digestive Disease, Li Ka Shing Institute of Health Sciences, CUHK Shenzhen Research Institute, The Chinese University of Hong Kong, Hong Kong, China – sequence: 6 givenname: Changan surname: Liu fullname: Liu, Changan organization: Institute of Digestive Disease and The Department of Medicine and Therapeutics, State Key Laboratory of Digestive Disease, Li Ka Shing Institute of Health Sciences, CUHK Shenzhen Research Institute, The Chinese University of Hong Kong, Hong Kong, China – sequence: 7 givenname: Liuyang surname: Zhao fullname: Zhao, Liuyang organization: Institute of Digestive Disease and The Department of Medicine and Therapeutics, State Key Laboratory of Digestive Disease, Li Ka Shing Institute of Health Sciences, CUHK Shenzhen Research Institute, The Chinese University of Hong Kong, Hong Kong, China – sequence: 8 givenname: Chuangen surname: Li fullname: Li, Chuangen organization: Institute of Digestive Disease and The Department of Medicine and Therapeutics, State Key Laboratory of Digestive Disease, Li Ka Shing Institute of Health Sciences, CUHK Shenzhen Research Institute, The Chinese University of Hong Kong, Hong Kong, China – sequence: 9 givenname: Yunfei surname: Zhou fullname: Zhou, Yunfei organization: Institute of Digestive Disease and The Department of Medicine and Therapeutics, State Key Laboratory of Digestive Disease, Li Ka Shing Institute of Health Sciences, CUHK Shenzhen Research Institute, The Chinese University of Hong Kong, Hong Kong, China – sequence: 10 givenname: Guoping surname: Wang fullname: Wang, Guoping organization: Institute of Digestive Disease and The Department of Medicine and Therapeutics, State Key Laboratory of Digestive Disease, Li Ka Shing Institute of Health Sciences, CUHK Shenzhen Research Institute, The Chinese University of Hong Kong, Hong Kong, China – sequence: 11 givenname: Wei orcidid: 0000-0002-4651-677X surname: Kang fullname: Kang, Wei organization: Department of Anatomical and Cellular Pathology, The Chinese University of Hong Kong, Hong Kong, China – sequence: 12 givenname: Enders Kwok-wai surname: Ng fullname: Ng, Enders Kwok-wai organization: Department of Surgery, The Chinese University of Hong Kong, Hong Kong, China – sequence: 13 givenname: Jun orcidid: 0000-0001-5008-2153 surname: Yu fullname: Yu, Jun email: junyu@cuhk.edu.hk organization: Institute of Digestive Disease and The Department of Medicine and Therapeutics, State Key Laboratory of Digestive Disease, Li Ka Shing Institute of Health Sciences, CUHK Shenzhen Research Institute, The Chinese University of Hong Kong, Hong Kong, China
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Snippet	ObjectiveCigarette smoking is a major risk factor for colorectal cancer (CRC). We aimed to investigate whether cigarette smoke promotes CRC by altering the gut... Cigarette smoking is a major risk factor for colorectal cancer (CRC). We aimed to investigate whether cigarette smoke promotes CRC by altering the gut...
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SubjectTerms	Air cleanliness Animal models Azoxymethane BACTERIAL PATHOGENESIS BILE ACID METABOLISM Cigarette smoke Cigarette smoking Cigarettes COLORECTAL CANCER Colorectal carcinoma Dysbacteriosis Epithelium Extracellular signal-regulated kinase Germfree Gut Microbiome Gut microbiota Intestinal microflora Kinases Laboratory animals Liquid chromatography MAP kinase Mass spectroscopy Metabolic pathways Metabolites Metabolomics Metagenomics Microbiota Protein kinase Proteins Risk factors Signal transduction Smoking Taurodeoxycholic acid Tumors
Title	Cigarette smoke promotes colorectal cancer through modulation of gut microbiota and related metabolites
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