Microbiology and Biotechnology Letters (한국미생물·생명공학회지)

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Lower Airway Microbiota and Lung Cancer

  • Sanchez-Hellin, Victoria (Section of Microbiology, Hospital General Universitario de Elche) ;
  • Galiana, Antonio (Section of Microbiology, Hospital General Universitario de Elche) ;
  • Zamora-Molina, Lucia (Section of Respiratory Medicine, Hospital General Universitario de Elche) ;
  • Soler-Sempere, Maria J. (Section of Respiratory Medicine, Hospital General Universitario de Elche) ;
  • Grau-Delgado, Justo (Section of Respiratory Medicine, Hospital General Universitario de Elche) ;
  • Barbera, Victor M. (Molecular Genetics Unit, Hospital General Universitario de Elche) ;
  • Padilla-Navas, Isabel (Section of Respiratory Medicine, Hospital General Universitario de Elche) ;
  • Garcia-Pachon, Eduardo (Section of Respiratory Medicine, Hospital General Universitario de Elche)
  • Received : 2018.11.20
  • Accepted : 2018.12.24
  • Published : 2019.09.28
Download PDF
⟨ Previous Next ⟩

Abstract

This study was aimed at identifying the lower airway microbiota in patients with lung cancer (LC) using protected brush sampling. We enrolled 37 patients undergoing diagnostic bronchoscopy for suspected LC, 26 with LC and 11 with benign diseases. Protected brush specimens were obtained from the contralateral lung and the side of the tumor; these specimens were analyzed by 16S rRNA-based-next-generation sequencing. The results indicated that the biodiversity was not different between groups, and there were no significant differences between the proportion of microorganisms in the tumor and in the contralateral side of patients with LC. In patients with LC, there was a higher abundance of several microorganisms including Capnocytophaga, Haemophilus, Enterococcus, and Streptococcus; whereas, in individuals without LC, Bacteroides, Lactobacillus, or Methylobacterium were more abundant. Malignancy could be determined with an accuracy of 70% by isolating Enterococcus, Capnocytophaga, or Actinomyces. Microbispora indicated benignity with a sensitivity of 55%, specificity of 88%, and accuracy of 78%. Lower airway microbiota in patients with LC is fairly similar in both the tumor and contralateral sites. Endobronchial microbiota is different in patients with and without LC, and these differences may have a potential clinical value as diagnostic or prognostic biomarkers.

Keywords

References

  1. Lynch SV, Pedersen O. 2016. The human intestinal microbiome in health and disease. N. Engl. J. Med. 375: 2369-2379. https://doi.org/10.1056/NEJMra1600266
  2. Pevsner-Fischer M, Tuganbaev T, Meijer M, Zhang SH, Zeng ZR, Chen MH, et al. 2016. Role of the microbiome in non-gastrointestinal cancers. World J. Clin. Oncol. 7: 200-213. https://doi.org/10.5306/wjco.v7.i2.200
  3. Vogtmann E, Goedert JJ. 2016. Epidemiologic studies of the human microbiome and cancer. Br. J. Cancer 114: 237-242. https://doi.org/10.1038/bjc.2015.465
  4. Schwabe RF, Jobin C. 2013. The microbiome and cancer. Nat. Rev. Cancer 13: 800-812. https://doi.org/10.1038/nrc3610
  5. Nugent JL, McCoy AN, Addamo CJ, Jia W, Sandler RS, Keku TO. 2014. Altered tissue metabolites correlate with microbial dysbiosis in colorectal adenomas. J. Proteome Res. 13: 1921-1929. https://doi.org/10.1021/pr4009783
  6. Brenner DR, McLaughlin JR, Hung RJ. 2011. Previous lung diseases and lung cancer risk: a systematic review and meta-analysis. PLoS One 6: e17479. https://doi.org/10.1371/journal.pone.0017479
  7. Zhan P, Suo LJ, Qian Q, Shen XK, Qiu LX, Yu LK, et al. 2011. Chlamydia pneumoniae infection and lung cancer risk: a meta-analysis. Eur. J. Cancer. 47: 742-747. https://doi.org/10.1016/j.ejca.2010.11.003
  8. Cameron SJS, Lewis KE, Huws SA, Hegarty MJ, Lewis PD, Pachebat JA, et al. 2017. A pilot study using metagenomic sequencing of the sputum microbiome suggests potential bacterial biomarkers for lung cancer. PLoS One 12: e0177062. https://doi.org/10.1371/journal.pone.0177062
  9. Cheng M, Qian L, Shen G, Bian G, Xu T, Xu W, et al. 2014. Microbiota modulate tumoral immune surveillance in lung through a ${\gamma}{\delta}T17$ immune cell-dependent mechanism. Cancer Res. 74: 4030-4041. https://doi.org/10.1158/0008-5472.CAN-13-2462
  10. Gui QF, Lu HF, Zhang CX, Xu ZR, Yang YH. 2015. Well-balanced commensal microbiota contributes to anti-cancer response in al lung cancer mouse model. Genet. Mol. Res. 14: 5642-5651. https://doi.org/10.4238/2015.May.25.16
  11. Hosgood HD, Sapkota AR, Rothan N, Rohan T, Hu W, Xu J, et al. 2014. The potential role of lung microbiota in lung cancer attributed to household coal burning exposure. Environ. Mol. Mutagen. 55: 643-651. https://doi.org/10.1002/em.21878
  12. Yan X, Yan M, Liu J, Gao R, Hu J, Li J, et al. 2015. Discovery and validation of potential bacterial biomarkers for lung cancer. Am. J. Cancer Res. 5: 3111-3122.
  13. Lee SH, Sung JY, Yong D, Chun J, Kim SY, Song JH, et al. 2016. Characterization of microbiome in bronchoalveolar lavage fluid of patients with lung cancer comparing with benign mass like lesions. Lung Cancer 102: 89-95. https://doi.org/10.1016/j.lungcan.2016.10.016
  14. Yu G, Gall MH, Consonni D, Carugno M, Humphys M, Pesatori AC, et al. 2016. Characterizing human lung tissue microbiota and its relationship to epidemiological and clinical features. Genome Biology 17: 163. https://doi.org/10.1186/s13059-016-1021-1
  15. Liu HX, Tao LL, Zhang J, Zhu YG, Zheng Y, Liu D, et al. 2018. Difference of lower airway microbiome in bilateral protected specimen brush between lung cancer patients with unilateral lobar masses and control subjects. Int. J. Cancer 142: 769-778. https://doi.org/10.1002/ijc.31098
  16. Berger G, Wunderink RG. 2013. Lung microbiota: genuine or artefact? Isr. Med. Assoc. J. 15: 731-733.
  17. Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, et al. 2013. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 41: e1. doi: 10.1093/nar/gks808.
  18. Schmieder R, Edwards R. 2011. Quality control and preprocessing of metagenomic datasets. Bioinformatics 27: 863-864. https://doi.org/10.1093/bioinformatics/btr026
  19. Aronesty E. 2011. Ea-tools: Command-line tools for processing biological sequencing data. Available from: https://github.com/ExpressionAnalysis/ea-utils. Accessed July 21, 2018.
  20. Edgar RC. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460-2461. https://doi.org/10.1093/bioinformatics/btq461
  21. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, et al. 2009. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 37(Database issue): D141-5. https://doi.org/10.1093/nar/gkn879
  22. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7: 335-336. https://doi.org/10.1038/nmeth.f.303
  23. Cole JR, Wang Q, Fish JA, Chai B, McGarrell DM, Sun Y, et al. 2014. Ribosomal Database Project: data and tools for highthroughput rRNA analysis. Nucleic Acids Res. 42(Database issue): D633-D642. https://doi.org/10.1093/nar/gkt1244
  24. Kim BR, Shin J, Guevarra R, Lee JH, Kim DW, Seol KH, et al. 2017. Deciphering diversity indices for a better understanding of microbial communities. J. Microbiol. Biotechnol. 27: 2089-2093. https://doi.org/10.4014/jmb.1709.09027
  25. Gronseth R, Drengenes C, Wiker HG, Tangedal S, Xue Y, Husebo GR, et al. 2017. Protected sampling is preferable in bronchoscopic studies of the airway microbiome. ERJ Open Res. 3: 0019-2017.
  26. Burns MB, Lynch J, Starr TK, Knights D, Blekhman R. 2015. Virulence genes are a signature of the microbiome in the colorectal tumor microenvironment. Genome Med. 7: 55. https://doi.org/10.1186/s13073-015-0177-8
  27. Hieken TJ, Chen J, Hoskin TL, Walther-Antonio M, Johnson S, Ramaker S, et al. 2016. The microbiome of aseptically collected human breast tissue in benign and malignant disease. Sci. Rep. 6: 30751. https://doi.org/10.1038/srep30751
  28. Laroumagne S, Lepage B, Hermant C, Plat G, Phelippeau M, Bigay-Game L, et al. 2013. Bronchial colonization in patients with lung cancer: a prospective study. Eur. Respir. J. 42: 220-229. https://doi.org/10.1183/09031936.00062212
  29. Mao Q, Jiang F, Yin R, Wang J, Xia W, Dong G, et al. 2018. Interplay between the lung microbiome and lung cancer. Cancer Lett. 415: 40-48. https://doi.org/10.1016/j.canlet.2017.11.036
  30. Tsay JJ, Wu BG, Badri MH, Clemente JC, Shen N, Meyn P, et al. 2018. Airway microbiota is associated with up-regulation of the PI3K pathway in lung cancer. Am. J. Respir. Crit. Care Med. 98: 1188-1198.
  31. Gustafson AM, Soldi R, Anderlind C, Scholand MB, Qian J, Zhang X, et al. 2010. Airway PI3K pathway activation is an early and reversible event in lung cancer development. Sci. Transl. Med. 2: 26ra25. https://doi.org/10.1126/scitranslmed.3000251
  32. Yan L, Cai Q, Xu Y. 2013. The ubiquitin-CXCR4 axis plays an important role in acute lung infection-enhanced lung tumor metastasis. Clin. Cancer Res. 19: 4706-4716. https://doi.org/10.1158/1078-0432.CCR-13-0011

Cited by

  1. Host-Microbiome Interaction in Lung Cancer vol.12, 2019, https://doi.org/10.3389/fimmu.2021.679829