American Association for Cancer Research (AACR)

Cancer Discovery

, volume 11 , issue 2 , pages 293-307

Lower Airway Dysbiosis Affects Lung Cancer Progression

Jun-Chieh J. Tsay ^{1, 2}

Benjamin G. Wu ^{1, 2}

Imran Sulaiman ¹

Katherine Gershner ³

Rosemary Schluger ¹

Yonghua Li ¹

Ting-An Yie ¹

Peter Meyn ⁴

Evan Olsen ¹

Luisannay Perez ¹

Brendan Franca ¹

Joseph Carpenito ¹

Tadasu Iizumi ¹

Mariam El-Ashmawy ⁵

Michelle Badri ⁶

James T Morton ⁷

Nan Shen ⁸

Linchen He ⁹

Gaetane Michaud ¹

Samaan Rafeq ¹

Jamie L. Bessich ¹

Robert L. Smith ²

Harald Sauthoff ²

Kevin Felner ²

Ray Pillai ¹

Anastasia Maria Zavitsanou ¹⁰

Sergei B. Koralov ¹⁰

Valeria Mezzano ¹⁰

Cynthia A. Loomis ¹⁰

Andre L. Moreira ¹⁰

William Moore ¹¹

Aristotelis Tsirigos ¹⁰

Adriana Heguy ^{4, 10}

William N. Rom ¹

Daniel H. Sterman ¹

Harvey I. Pass ¹²

Jose C. Clemente ⁸

Huilin Li ⁹

Richard Bonneau ^{6, 7, 13}

Kwok-Kin Wong ¹⁴

Thales Papagiannakopoulos ¹⁰

Leopoldo N Segal ¹

Hide authors affiliations Show authors affiliations: 14 affiliations

1Division of Pulmonary and Critical Care Medicine, New York University School of Medicine, New York, New York. |

2Division of Pulmonary and Critical Care Medicine, VA New York Harbor Healthcare System, New York, New York. |

3Section of Pulmonary, Critical Care, Allergy and Immunology, Wake Forest School of Medicine, Winston-Salem, North Carolina. |

⁴

4NYU Langone Genomic Technology Center, New York University School of Medicine, New York, New York. |

⁵

5Department of Medicine, New York University School of Medicine, New York, New York. |

⁶

6Department of Biology, New York University, New York, New York. |

⁷

7Center for Computational Biology, Flatiron Institute, Simons Foundation, New York, New York. |

⁸

8Department of Genetics and Genomic Sciences and Immunology Institute, Icahn School of Medicine at Mount Sinai, New York, New York. |

⁹

9Department of Population Health, New York University School of Medicine, New York, New York. |

¹⁰

10Department of Pathology, New York University School of Medicine, New York, New York. |

¹¹

11Department of Radiology, New York University School of Medicine, New York, New York. |

¹²

12Department of Cardiothoracic Surgery, New York University School of Medicine, New York, New York. |

¹³

13Center for Data Science, New York University School of Medicine, New York, New York. |

¹⁴

14Division of Hematology and Oncology, New York University School of Medicine, New York, New York. |

Publication type: Journal Article

Publication date: 2021-02-01

American Association for Cancer Research (AACR)

Cancer Discovery

scimago Q1

wos Q1

SJR: 7.283

CiteScore: 24.8

Impact factor: 33.3

ISSN: 21598274, 21598290

DOI: 10.1158/2159-8290.cd-20-0263

Copy DOI

PubMed ID: 33177060

Oncology

Abstract

In lung cancer, enrichment of the lower airway microbiota with oral commensals commonly occurs, and ex vivo models support that some of these bacteria can trigger host transcriptomic signatures associated with carcinogenesis. Here, we show that this lower airway dysbiotic signature was more prevalent in the stage IIIB–IV tumor–node–metastasis lung cancer group and is associated with poor prognosis, as shown by decreased survival among subjects with early-stage disease (I–IIIA) and worse tumor progression as measured by RECIST scores among subjects with stage IIIB–IV disease. In addition, this lower airway microbiota signature was associated with upregulation of the IL17, PI3K, MAPK, and ERK pathways in airway transcriptome, and we identified Veillonella parvula as the most abundant taxon driving this association. In a KP lung cancer model, lower airway dysbiosis with V. parvula led to decreased survival, increased tumor burden, IL17 inflammatory phenotype, and activation of checkpoint inhibitor markers.

Significance:

Multiple lines of investigation have shown that the gut microbiota affects host immune response to immunotherapy in cancer. Here, we support that the local airway microbiota modulates the host immune tone in lung cancer, affecting tumor progression and prognosis.

See related commentary by Zitvogel and Kroemer, p. 224.

This article is highlighted in the In This Issue feature, p. 211

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243

Cite this

GOST |

Cite this

GOST Copy

Tsay J. J. et al. Lower Airway Dysbiosis Affects Lung Cancer Progression // Cancer Discovery. 2021. Vol. 11. No. 2. pp. 293-307.

GOST all authors (up to 50) Copy

Tsay J. J., Wu B. G., Sulaiman I., Gershner K., Schluger R., Li Y., Yie T., Meyn P., Olsen E., Perez L., Franca B., Carpenito J., Iizumi T., El-Ashmawy M., Badri M., Morton J. T., Shen N., He L., Michaud G., Rafeq S., Bessich J. L., Smith R. L., Sauthoff H., Felner K., Pillai R., Zavitsanou A. M., Koralov S. B., Mezzano V., Loomis C. A., Moreira A. L., Moore W., Tsirigos A., Heguy A., Rom W. N., Sterman D. H., Pass H. I., Clemente J. C., Li H., Bonneau R., Wong K., Papagiannakopoulos T., Segal L. N. Lower Airway Dysbiosis Affects Lung Cancer Progression // Cancer Discovery. 2021. Vol. 11. No. 2. pp. 293-307.

RIS |

Cite this

RIS Copy

TY - JOUR

DO - 10.1158/2159-8290.cd-20-0263

UR - https://doi.org/10.1158/2159-8290.cd-20-0263

TI - Lower Airway Dysbiosis Affects Lung Cancer Progression

T2 - Cancer Discovery

AU - Tsay, Jun-Chieh J.

AU - Wu, Benjamin G.

AU - Sulaiman, Imran

AU - Gershner, Katherine

AU - Schluger, Rosemary

AU - Li, Yonghua

AU - Yie, Ting-An

AU - Meyn, Peter

AU - Olsen, Evan

AU - Perez, Luisannay

AU - Franca, Brendan

AU - Carpenito, Joseph

AU - Iizumi, Tadasu

AU - El-Ashmawy, Mariam

AU - Badri, Michelle

AU - Morton, James T

AU - Shen, Nan

AU - He, Linchen

AU - Michaud, Gaetane

AU - Rafeq, Samaan

AU - Bessich, Jamie L.

AU - Smith, Robert L.

AU - Sauthoff, Harald

AU - Felner, Kevin

AU - Pillai, Ray

AU - Zavitsanou, Anastasia Maria

AU - Koralov, Sergei B.

AU - Mezzano, Valeria

AU - Loomis, Cynthia A.

AU - Moreira, Andre L.

AU - Moore, William

AU - Tsirigos, Aristotelis

AU - Heguy, Adriana

AU - Rom, William N.

AU - Sterman, Daniel H.

AU - Pass, Harvey I.

AU - Clemente, Jose C.

AU - Li, Huilin

AU - Bonneau, Richard

AU - Wong, Kwok-Kin

AU - Papagiannakopoulos, Thales

AU - Segal, Leopoldo N

PY - 2021

DA - 2021/02/01

PB - American Association for Cancer Research (AACR)

SP - 293-307

IS - 2

VL - 11

PMID - 33177060

SN - 2159-8274

SN - 2159-8290

ER -

BibTex |

Cite this

BibTex (up to 50 authors) Copy

@article{2021_Tsay,

author = {Jun-Chieh J. Tsay and Benjamin G. Wu and Imran Sulaiman and Katherine Gershner and Rosemary Schluger and Yonghua Li and Ting-An Yie and Peter Meyn and Evan Olsen and Luisannay Perez and Brendan Franca and Joseph Carpenito and Tadasu Iizumi and Mariam El-Ashmawy and Michelle Badri and James T Morton and Nan Shen and Linchen He and Gaetane Michaud and Samaan Rafeq and Jamie L. Bessich and Robert L. Smith and Harald Sauthoff and Kevin Felner and Ray Pillai and Anastasia Maria Zavitsanou and Sergei B. Koralov and Valeria Mezzano and Cynthia A. Loomis and Andre L. Moreira and William Moore and Aristotelis Tsirigos and Adriana Heguy and William N. Rom and Daniel H. Sterman and Harvey I. Pass and Jose C. Clemente and Huilin Li and Richard Bonneau and Kwok-Kin Wong and Thales Papagiannakopoulos and Leopoldo N Segal},

title = {Lower Airway Dysbiosis Affects Lung Cancer Progression},

journal = {Cancer Discovery},

year = {2021},

volume = {11},

publisher = {American Association for Cancer Research (AACR)},

month = {feb},

url = {https://doi.org/10.1158/2159-8290.cd-20-0263},

number = {2},

pages = {293--307},

doi = {10.1158/2159-8290.cd-20-0263}

}

MLA

Cite this

MLA Copy

Tsay, Jun-Chieh J., et al. “Lower Airway Dysbiosis Affects Lung Cancer Progression.” Cancer Discovery, vol. 11, no. 2, Feb. 2021, pp. 293-307. https://doi.org/10.1158/2159-8290.cd-20-0263.

Publisher

American Association for Cancer Research (AACR)

Journal

Cancer Discovery

scimago Q1

wos Q1

SJR

7.283

CiteScore

24.8

Impact factor

33.3

ISSN

21598274 (Print)

21598290 (Electronic)