Tumor Microbiome Diversity and Composition Influence Pancreatic Cancer Outcomes

Most patients diagnosed with resected pancreatic adenocarcinoma (PDAC) survive less than 5 years, but a minor subset survives longer. Here, we dissect the role of the tumor microbiota and the immune system in influencing long-term survival. Using 16S rRNA gene sequencing, we analyzed the tumor micro...

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Vydané v:	Cell Ročník 178; číslo 4; s. 795
Hlavní autori:	Riquelme, Erick, Zhang, Yu, Zhang, Liangliang, Montiel, Maria, Zoltan, Michelle, Dong, Wenli, Quesada, Pompeyo, Sahin, Ismet, Chandra, Vidhi, San Lucas, Anthony, Scheet, Paul, Xu, Hanwen, Hanash, Samir M, Feng, Lei, Burks, Jared K, Do, Kim-Anh, Peterson, Christine B, Nejman, Deborah, Tzeng, Ching-Wei D, Kim, Michael P, Sears, Cynthia L, Ajami, Nadim, Petrosino, Joseph, Wood, Laura D, Maitra, Anirban, Straussman, Ravid, Katz, Matthew, White, James Robert, Jenq, Robert, Wargo, Jennifer, McAllister, Florencia
Médium:	Journal Article
Jazyk:	English
Vydavateľské údaje:	United States 08.08.2019
Predmet:	Adult Aged Animals Bacteria - classification Carcinoma, Pancreatic Ductal - microbiology Carcinoma, Pancreatic Ductal - mortality Cell Line, Tumor Cohort Studies Fecal Microbiota Transplantation Feces - microbiology Female Gastrointestinal Microbiome Humans Male Mice Mice, Inbred C57BL Middle Aged Pancreatic Neoplasms - microbiology Pancreatic Neoplasms - mortality RNA, Ribosomal, 16S - genetics Sequence Analysis, RNA Survival Rate microbiota pancreatic cancer PDAC cancer survivors fecal microbial transplants CD8 immunoactivation antibiotics tumor microbiome
ISSN:	1097-4172, 1097-4172
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Abstract	Most patients diagnosed with resected pancreatic adenocarcinoma (PDAC) survive less than 5 years, but a minor subset survives longer. Here, we dissect the role of the tumor microbiota and the immune system in influencing long-term survival. Using 16S rRNA gene sequencing, we analyzed the tumor microbiome composition in PDAC patients with short-term survival (STS) and long-term survival (LTS). We found higher alpha-diversity in the tumor microbiome of LTS patients and identified an intra-tumoral microbiome signature (Pseudoxanthomonas-Streptomyces-Saccharopolyspora-Bacillus clausii) highly predictive of long-term survivorship in both discovery and validation cohorts. Through human-into-mice fecal microbiota transplantation (FMT) experiments from STS, LTS, or control donors, we were able to differentially modulate the tumor microbiome and affect tumor growth as well as tumor immune infiltration. Our study demonstrates that PDAC microbiome composition, which cross-talks to the gut microbiome, influences the host immune response and natural history of the disease.
AbstractList	Most patients diagnosed with resected pancreatic adenocarcinoma (PDAC) survive less than 5 years, but a minor subset survives longer. Here, we dissect the role of the tumor microbiota and the immune system in influencing long-term survival. Using 16S rRNA gene sequencing, we analyzed the tumor microbiome composition in PDAC patients with short-term survival (STS) and long-term survival (LTS). We found higher alpha-diversity in the tumor microbiome of LTS patients and identified an intra-tumoral microbiome signature (Pseudoxanthomonas-Streptomyces-Saccharopolyspora-Bacillus clausii) highly predictive of long-term survivorship in both discovery and validation cohorts. Through human-into-mice fecal microbiota transplantation (FMT) experiments from STS, LTS, or control donors, we were able to differentially modulate the tumor microbiome and affect tumor growth as well as tumor immune infiltration. Our study demonstrates that PDAC microbiome composition, which cross-talks to the gut microbiome, influences the host immune response and natural history of the disease. Most patients diagnosed with resected pancreatic adenocarcinoma (PDAC) survive less than 5 years, but a minor subset survives longer. Here, we dissect the role of the tumor microbiota and the immune system in influencing long-term survival. Using 16S rRNA gene sequencing, we analyzed the tumor microbiome composition in PDAC patients with short-term survival (STS) and long-term survival (LTS). We found higher alpha-diversity in the tumor microbiome of LTS patients and identified an intra-tumoral microbiome signature (Pseudoxanthomonas-Streptomyces-Saccharopolyspora-Bacillus clausii) highly predictive of long-term survivorship in both discovery and validation cohorts. Through human-into-mice fecal microbiota transplantation (FMT) experiments from STS, LTS, or control donors, we were able to differentially modulate the tumor microbiome and affect tumor growth as well as tumor immune infiltration. Our study demonstrates that PDAC microbiome composition, which cross-talks to the gut microbiome, influences the host immune response and natural history of the disease.Most patients diagnosed with resected pancreatic adenocarcinoma (PDAC) survive less than 5 years, but a minor subset survives longer. Here, we dissect the role of the tumor microbiota and the immune system in influencing long-term survival. Using 16S rRNA gene sequencing, we analyzed the tumor microbiome composition in PDAC patients with short-term survival (STS) and long-term survival (LTS). We found higher alpha-diversity in the tumor microbiome of LTS patients and identified an intra-tumoral microbiome signature (Pseudoxanthomonas-Streptomyces-Saccharopolyspora-Bacillus clausii) highly predictive of long-term survivorship in both discovery and validation cohorts. Through human-into-mice fecal microbiota transplantation (FMT) experiments from STS, LTS, or control donors, we were able to differentially modulate the tumor microbiome and affect tumor growth as well as tumor immune infiltration. Our study demonstrates that PDAC microbiome composition, which cross-talks to the gut microbiome, influences the host immune response and natural history of the disease.
Author	Zhang, Liangliang San Lucas, Anthony Sears, Cynthia L Zhang, Yu Ajami, Nadim Chandra, Vidhi Sahin, Ismet Straussman, Ravid Riquelme, Erick Hanash, Samir M Maitra, Anirban McAllister, Florencia Dong, Wenli Burks, Jared K Feng, Lei Zoltan, Michelle Kim, Michael P Tzeng, Ching-Wei D Quesada, Pompeyo Wood, Laura D Nejman, Deborah Montiel, Maria Do, Kim-Anh Katz, Matthew Wargo, Jennifer Xu, Hanwen Peterson, Christine B White, James Robert Petrosino, Joseph Jenq, Robert Scheet, Paul
Author_xml	– sequence: 1 givenname: Erick surname: Riquelme fullname: Riquelme, Erick organization: Department of Clinical Cancer Prevention, The University of Texas MD Anderson Cancer Center, Houston, TX, USA; Center for Integrative Biology, Faculty of Science, Universidad Mayor, Santiago, Chile – sequence: 2 givenname: Yu surname: Zhang fullname: Zhang, Yu organization: Department of Clinical Cancer Prevention, The University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 3 givenname: Liangliang surname: Zhang fullname: Zhang, Liangliang organization: Department of Biostatistics, The University of Texas MD Anderson Cancer Center, Houston, TX, USA; Department of Genomic Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 4 givenname: Maria surname: Montiel fullname: Montiel, Maria organization: Department of Clinical Cancer Prevention, The University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 5 givenname: Michelle surname: Zoltan fullname: Zoltan, Michelle organization: Department of Clinical Cancer Prevention, The University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 6 givenname: Wenli surname: Dong fullname: Dong, Wenli organization: Department of Biostatistics, The University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 7 givenname: Pompeyo surname: Quesada fullname: Quesada, Pompeyo organization: Department of Clinical Cancer Prevention, The University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 8 givenname: Ismet surname: Sahin fullname: Sahin, Ismet organization: Department of Engineering, Texas Southern University, Houston, TX, USA – sequence: 9 givenname: Vidhi surname: Chandra fullname: Chandra, Vidhi organization: Department of Clinical Cancer Prevention, The University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 10 givenname: Anthony surname: San Lucas fullname: San Lucas, Anthony organization: Department of Epidemiology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 11 givenname: Paul surname: Scheet fullname: Scheet, Paul organization: Department of Epidemiology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 12 givenname: Hanwen surname: Xu fullname: Xu, Hanwen organization: Department of Clinical Cancer Prevention, The University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 13 givenname: Samir M surname: Hanash fullname: Hanash, Samir M organization: Department of Clinical Cancer Prevention, The University of Texas MD Anderson Cancer Center, Houston, TX, USA; McCombs Institute for the Early Detection and Treatment of Cancer, The University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 14 givenname: Lei surname: Feng fullname: Feng, Lei organization: Department of Biostatistics, The University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 15 givenname: Jared K surname: Burks fullname: Burks, Jared K organization: Department of Leukemia, The University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 16 givenname: Kim-Anh surname: Do fullname: Do, Kim-Anh organization: Department of Biostatistics, The University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 17 givenname: Christine B surname: Peterson fullname: Peterson, Christine B organization: Department of Biostatistics, The University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 18 givenname: Deborah surname: Nejman fullname: Nejman, Deborah organization: Department of Molecular Cell Biology, Weizmann Institute of Science, Rehovot, Israel – sequence: 19 givenname: Ching-Wei D surname: Tzeng fullname: Tzeng, Ching-Wei D organization: Department of Surgical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 20 givenname: Michael P surname: Kim fullname: Kim, Michael P organization: Department of Surgical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 21 givenname: Cynthia L surname: Sears fullname: Sears, Cynthia L organization: Departments of Medicine, Oncology and Molecular Microbiology & Immunology, Johns Hopkins University School of Medicine and the Bloomberg School of Public Health, Baltimore, MD, USA – sequence: 22 givenname: Nadim surname: Ajami fullname: Ajami, Nadim organization: Department of Molecular Virology and Microbiology, Baylor College of Medicine, Houston, TX, USA – sequence: 23 givenname: Joseph surname: Petrosino fullname: Petrosino, Joseph organization: Department of Molecular Virology and Microbiology, Baylor College of Medicine, Houston, TX, USA – sequence: 24 givenname: Laura D surname: Wood fullname: Wood, Laura D organization: Department of Pathology and The Sol Goldman Pancreatic Cancer Research Center, Johns Hopkins University School of Medicine, Baltimore, MD, USA – sequence: 25 givenname: Anirban surname: Maitra fullname: Maitra, Anirban organization: Sheikh Ahmed Pancreatic Cancer Research Center, The University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 26 givenname: Ravid surname: Straussman fullname: Straussman, Ravid organization: Department of Molecular Cell Biology, Weizmann Institute of Science, Rehovot, Israel – sequence: 27 givenname: Matthew surname: Katz fullname: Katz, Matthew organization: Department of Surgical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 28 givenname: James Robert surname: White fullname: White, James Robert organization: Resphera Biosciences, Baltimore, MD, USA – sequence: 29 givenname: Robert surname: Jenq fullname: Jenq, Robert organization: Department of Genomic Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 30 givenname: Jennifer surname: Wargo fullname: Wargo, Jennifer organization: Department of Genomic Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX, USA; Department of Surgical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA – sequence: 31 givenname: Florencia surname: McAllister fullname: McAllister, Florencia email: fmcallister@mdanderson.org organization: Department of Clinical Cancer Prevention, The University of Texas MD Anderson Cancer Center, Houston, TX, USA; Department of Gastrointestinal Medical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA; Clinical Cancer Genetics Program, The University of Texas MD Anderson Cancer Center, Houston, TX, USA. Electronic address: fmcallister@mdanderson.org
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/31398337$$D View this record in MEDLINE/PubMed
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Keywords	microbiota pancreatic cancer PDAC cancer survivors fecal microbial transplants CD8 immunoactivation antibiotics tumor microbiome
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PublicationYear	2019
References	31477872 - Nat Rev Gastroenterol Hepatol. 2019 Nov;16(11):649 31530941 - Nat Rev Clin Oncol. 2019 Nov;16(11):665-666 31471581 - Nat Rev Cancer. 2019 Oct;19(10):545
References_xml	– reference: 31477872 - Nat Rev Gastroenterol Hepatol. 2019 Nov;16(11):649 – reference: 31530941 - Nat Rev Clin Oncol. 2019 Nov;16(11):665-666 – reference: 31471581 - Nat Rev Cancer. 2019 Oct;19(10):545
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Snippet	Most patients diagnosed with resected pancreatic adenocarcinoma (PDAC) survive less than 5 years, but a minor subset survives longer. Here, we dissect the role...
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SubjectTerms	Adult Aged Animals Bacteria - classification Carcinoma, Pancreatic Ductal - microbiology Carcinoma, Pancreatic Ductal - mortality Cell Line, Tumor Cohort Studies Fecal Microbiota Transplantation Feces - microbiology Female Gastrointestinal Microbiome Humans Male Mice Mice, Inbred C57BL Middle Aged Pancreatic Neoplasms - microbiology Pancreatic Neoplasms - mortality RNA, Ribosomal, 16S - genetics Sequence Analysis, RNA Survival Rate
Title	Tumor Microbiome Diversity and Composition Influence Pancreatic Cancer Outcomes
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