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Journal of Oncology
Volume 2017, Article ID 5035371, 15 pages
https://doi.org/10.1155/2017/5035371
Review Article

Desired Turbulence? Gut-Lung Axis, Immunity, and Lung Cancer

1University of Clermont-Auvergne, UMR 1019 INRA-UCA, Human Nutrition Unit (UNH), ECREIN Team, 63000 Clermont-Ferrand, France
2Jean Perrin Comprehensive Cancer Centre, Thoracic Surgery Unit, 63011 Clermont-Ferrand, France
3University of Clermont-Auvergne, Jean Perrin Comprehensive Cancer Centre, Department of Pathology, INSERM U1240 Molecular Imaging and Theranostic Strategies, 63000 Clermont-Ferrand, France
4Greentech SA, Biopôle Clermont-Limagne, 63360 Saint-Beauzire, France
5INRA, UR454 Microbiology Unit, Clermont-Ferrand/Theix Research Centre, 63122 Saint-Genès-Champanelle, France
6Jean Perrin Comprehensive Cancer Centre, CHU Gabriel-Montpied, Human Nutrition Unit (UNH), CRNH Auvergne, 63000 Clermont-Ferrand, France
7CIAMS, University Paris-Sud, University Paris-Saclay, 91405 Orsay Cedex, France
8CIAMS, University of Orléans, 45067 Orléans, France

Correspondence should be addressed to Edith Filaire; rf.snaelro-vinu@erialif.htide

Received 8 March 2017; Revised 30 June 2017; Accepted 3 August 2017; Published 17 September 2017

Academic Editor: James L. Mulshine

Copyright © 2017 Rea Bingula et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. B. J. Marsland, A. Trompette, and E. S. Gollwitzer, “The gut-lung axis in respiratory disease,” Annals of the American Thoracic Society, vol. 12, Suppl 2, pp. S150–S156, 2015. View at Publisher · View at Google Scholar · View at Scopus
  2. A. M. Brownawell, W. Caers, G. R. Gibson et al., “Prebiotics and the health benefits of fiber: Current regulatory status, future research, and goals,” Journal of Nutrition, vol. 142, no. 5, pp. 962–974, 2012. View at Publisher · View at Google Scholar · View at Scopus
  3. Y. Belkaid and T. W. Hand, “Role of the microbiota in immunity and inflammation,” Cell, vol. 157, no. 1, pp. 121–141, 2014. View at Publisher · View at Google Scholar · View at Scopus
  4. S. Carding, K. Verbeke, D. T. Vipond, B. M. Corfe, and L. J. Owen, “Dysbiosis of the gut microbiota in disease,” Microbial Ecology in Health & Disease, vol. 26, no. 1, 2015. View at Publisher · View at Google Scholar
  5. P. Forsythe, W. Kunze, and J. Bienenstock, “Moody microbes or fecal phrenology: What do we know about the microbiota-gut-brain axis?” BMC Medicine, vol. 14, no. 1, article no. 58, 2016. View at Publisher · View at Google Scholar · View at Scopus
  6. T. J. Schuijt, J. M. Lankelma, B. P. Scicluna et al., “The gut microbiota plays a protective role in the host defence against pneumococcal pneumonia,” Gut, vol. 65, no. 4, pp. 575–583, 2016. View at Publisher · View at Google Scholar · View at Scopus
  7. M. Hilty, C. Burke, H. Pedro et al., “Disordered microbial communities in asthmatic airways,” PLoS ONE, vol. 5, no. 1, Article ID e8578, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. H. Wang, J.-S. Liu, S.-H. Peng et al., “Gut-lung crosstalk in pulmonary involvement with inflammatory bowel diseases,” World Journal of Gastroenterology, vol. 19, no. 40, pp. 6794–6804, 2013. View at Publisher · View at Google Scholar · View at Scopus
  9. T. Jess, E. Horváth-Puhó, J. Fallingborg, H. H. Rasmussen, and B. A. Jacobsen, “Cancer risk in inflammatory bowel disease according to patient phenotype and treatment: a danish population-based cohort study,” American Journal of Gastroenterology, vol. 108, no. 12, pp. 1869–1876, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. S. Keely, N. J. Talley, and P. M. Hansbro, “Pulmonary-intestinal cross-talk in mucosal inflammatory disease,” Mucosal Immunology, vol. 5, no. 1, pp. 7–18, 2012. View at Publisher · View at Google Scholar · View at Scopus
  11. J. Tap, S. Mondot, F. Levenez et al., “Towards the human intestinal microbiota phylogenetic core,” Environmental Microbiology, vol. 11, no. 10, pp. 2574–2584, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. V. Lazarevic, K. Whiteson, S. Huse et al., “Metagenomic study of the oral microbiota by Illumina high-throughput sequencing,” Journal of Microbiological Methods, vol. 79, no. 3, pp. 266–271, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. K. P. Lemon, V. Klepac-Ceraj, H. K. Schiffer, E. L. Brodie, S. V. Lynch, and R. Kolter, “Comparative analyses of the Bacterial microbiota of the human nostril and oropharynx,” mBio, vol. 1, no. 3, 2010. View at Publisher · View at Google Scholar · View at Scopus
  14. E. S. Charlson, K. Bittinger, A. R. Haas et al., “Topographical continuity of bacterial populations in the healthy human respiratory tract,” The American Journal of Respiratory and Critical Care Medicine, vol. 184, no. 8, pp. 957–963, 2011. View at Publisher · View at Google Scholar · View at Scopus
  15. Z. Pei, E. J. Bini, L. Yang, M. Zhou, F. Francois, and M. J. Blaser, “Bacterial biota in the human distal esophagus,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 12, pp. 4250–4255, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. A. A. Pragman, H. B. Kim, C. S. Reilly, C. Wendt, and R. E. Isaacson, “The Lung Microbiome in Moderate and Severe Chronic Obstructive Pulmonary Disease,” PLoS ONE, vol. 7, no. 10, Article ID e47305, 2012. View at Publisher · View at Google Scholar · View at Scopus
  17. J. R. Erb-Downward, D. L. Thompson, M. K. Han et al., “Analysis of the lung microbiome in the ‘healthy’ smoker and in COPD,” PLoS ONE, vol. 6, no. 2, Article ID e16384, 2011. View at Publisher · View at Google Scholar · View at Scopus
  18. M. Garcia-Nuñez, L. Millares, X. Pomares et al., “Severity-related changes of bronchial microbiome in chronic obstructive pulmonary disease,” Journal of Clinical Microbiology, vol. 52, no. 12, pp. 4217–4223, 2014. View at Publisher · View at Google Scholar · View at Scopus
  19. M. A. Sze, P. A. Dimitriu, S. Hayashi et al., “The lung tissue microbiome in chronic obstructive pulmonary disease,” American Journal of Respiratory and Critical Care Medicine, vol. 185, no. 10, pp. 1073–1080, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. D. Wu, C. Hou, Y. Li et al., “Analysis of the bacterial community in chronic obstructive pulmonary disease sputum samples by denaturing gradient gel electrophoresis and real-time PCR,” BMC Pulmonary Medicine, vol. 14, no. 1, article no. 179, 2014. View at Publisher · View at Google Scholar · View at Scopus
  21. X. Yan, M. Yang, J. Liu et al., “Discovery and validation of potential bacterial biomarkers for lung cancer,” American Journal of Cancer Research, vol. 5, pp. 3111–3122, 2015. View at Google Scholar
  22. P. Rybojad, R. Los, M. Sawicki, J. Tabarkiewicz, and A. Malm, “Anaerobic bacteria colonizing the lower airways in lung cancer patients,” Folia Histochemica et Cytobiologica, vol. 49, no. 2, pp. 263–266, 2011. View at Publisher · View at Google Scholar · View at Scopus
  23. M. T. Abreu, “Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function,” Nature Reviews Immunology, vol. 10, no. 2, pp. 131–144, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. G. D. Wu, J. Chen, C. Hoffmann et al., “Linking long-term dietary patterns with gut microbial enterotypes,” Science, vol. 334, no. 6052, pp. 105–108, 2011. View at Publisher · View at Google Scholar · View at Scopus
  25. M. Arumugam, J. Raes, E. Pelletier et al., “Enterotypes of the human gut microbiome,” Nature, vol. 12, pp. 174–180, 2011. View at Google Scholar
  26. D. R. Samuelson, D. A. Welsh, and J. E. Shellito, “Regulation of lung immunity and host defense by the intestinal microbiota,” Frontiers in Microbiology, vol. 6, article no. 1085, 2015. View at Publisher · View at Google Scholar · View at Scopus
  27. I. I. Ivanov and K. Honda, “Intestinal commensal microbes as immune modulators,” Cell Host & Microbe, vol. 12, no. 4, pp. 496–508, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. A. Hakansson and G. Molin, “Gut microbiota and inflammation,” Nutrients, vol. 3, no. 6, pp. 637–682, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. B. Kelsall, “Recent progress in understanding the phenotype and function of intestinal dendritic cells and macrophages,” Mucosal Immunology, vol. 1, no. 6, pp. 460–469, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. T. Nakajima, V. Palchevsky, D. L. Perkins, J. A. Belperio, and P. W. Finn, “Lung transplantation: Infection, inflammation, and the microbiome,” Seminars in Immunopathology, vol. 33, no. 2, pp. 135–156, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. A. J. Macpherson and T. Uhr, “Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science,” Science, vol. 303, no. 5664, pp. 1662–1665, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. H. Tezuka, Y. Abe, J. Asano et al., “Prominent Role for Plasmacytoid Dendritic Cells in Mucosal T Cell-Independent IgA Induction,” Immunity, vol. 34, no. 2, pp. 247–257, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. E. Castigli, S. A. Wilson, S. Scott et al., “TACI and BAFF-R mediate isotype switching in B cells,” Journal of Experimental Medicine, vol. 201, no. 1, pp. 35–39, 2005. View at Publisher · View at Google Scholar · View at Scopus
  34. N. Kamada, S.-U. Seo, G. Y. Chen, and G. Núñez, “Role of the gut microbiota in immunity and inflammatory disease,” Nature Reviews Immunology, vol. 13, no. 5, pp. 321–335, 2013. View at Publisher · View at Google Scholar · View at Scopus
  35. P. López, M. Gueimonde, A. Margolles, and A. Suárez, “Distinct Bifidobacterium strains drive different immune responses in vitro,” International Journal of Food Microbiology, vol. 138, no. 1-2, pp. 157–165, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. H. S. Gill, K. J. Rutherfurd, M. L. Cross, and P. K. Gopal, “Enhancement of immunity in the elderly by dietary supplementation with the probiotic Bifidobactedum lactis HN019,” American Journal of Clinical Nutrition, vol. 74, no. 6, pp. 833–839, 2001. View at Google Scholar · View at Scopus
  37. G. T. Macfarlane and S. Macfarlane, “Bacteria, colonic fermentation, and gastrointestinal health,” Journal of AOAC International, vol. 95, no. 1, pp. 50–60, 2012. View at Publisher · View at Google Scholar · View at Scopus
  38. D. L. Topping and P. M. Clifton, “Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides,” Physiological Reviews, vol. 81, no. 3, pp. 1031–1064, 2001. View at Google Scholar · View at Scopus
  39. G. T. Macfarlane and S. Macfarlane, “Fermentation in the human large intestine: Its physiologic consequences and the potential contribution of prebiotics,” Journal of Clinical Gastroenterology, vol. 45, no. 3, pp. S120–S127, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. E. le Poul, C. Loison, S. Struyf et al., “Functional characterization of human receptors for short chain fatty acids and their role in polymorphonuclear cell activation,” The Journal of Biological Chemistry, vol. 278, no. 28, pp. 25481–25489, 2003. View at Publisher · View at Google Scholar · View at Scopus
  41. N. Singh, A. Gurav, S. Sivaprakasam et al., “Activation of Gpr109a, receptor for niacin and the commensal metabolite butyrate, suppresses colonic inflammation and carcinogenesis,” Immunity, vol. 40, no. 1, pp. 128–139, 2014. View at Publisher · View at Google Scholar · View at Scopus
  42. N. I. McNeil, “The contribution of the large intestine to energy supplies in man,” The American Journal of Clinical Nutrition, vol. 39, no. 3, pp. 338–342, 1981. View at Google Scholar
  43. S. Krishnan, N. Alden, and K. Lee, “Pathways and functions of gut microbiota metabolism impacting host physiology,” Current Opinion in Biotechnology, vol. 36, pp. 137–145, 2015. View at Publisher · View at Google Scholar · View at Scopus
  44. Y. Furusawa, Y. Obata, S. Fukuda et al., “Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells,” Nature, vol. 504, no. 7480, pp. 446–450, 2013. View at Publisher · View at Google Scholar · View at Scopus
  45. L. Chen, W. Fischle, E. Verdin, and W. C. Greene, “Duration of nuclear NF-κB action regulated by reversible acetylation,” Science, vol. 293, no. 5535, pp. 1653–1657, 2001. View at Publisher · View at Google Scholar · View at Scopus
  46. Z.-L. Yuan, Y.-J. Guan, D. Chatterjee, and Y. E. Chin, “Stat3 dimerization regulated by reversible acetylation of a single lysine residue,” Science, vol. 307, no. 5707, pp. 269–273, 2005. View at Publisher · View at Google Scholar · View at Scopus
  47. S. Viaud, R. Daillère, I. G. Boneca et al., “Gut microbiome and anticancer immune response: really hot Sh*t!,” Cell Death and Differentiation, 2014. View at Publisher · View at Google Scholar · View at Scopus
  48. H. M. Hamer, D. Jonkers, K. Venema, S. Vanhoutvin, F. J. Troost, and R.-J. Brummer, “Review article: the role of butyrate on colonic function,” Alimentary Pharmacology and Therapeutics, vol. 27, no. 2, pp. 104–119, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. E. Cario, “Microbiota and innate immunity in intestinal inflammation and neoplasia,” Current Opinion in Gastroenterology, vol. 29, no. 1, pp. 85–91, 2013. View at Publisher · View at Google Scholar · View at Scopus
  50. S. Dulal and T. O. Keku, “Gut microbiome and colorectal adenomas,” Cancer Journal (United States), vol. 20, no. 3, pp. 225–231, 2014. View at Publisher · View at Google Scholar · View at Scopus
  51. L. V. Hooper, D. R. Littman, and A. J. Macpherson, “Interactions between the microbiota and the immune system,” Science, vol. 336, no. 6086, pp. 1268–1273, 2012. View at Publisher · View at Google Scholar · View at Scopus
  52. C. T. Fagundes, F. A. Amaral, A. T. Vieira et al., “Transient TLR activation restores inflammatory response and ability to control pulmonary bacterial infection in germfree mice,” The Journal of Immunology, vol. 188, no. 3, pp. 1411–1420, 2012. View at Publisher · View at Google Scholar · View at Scopus
  53. I. C. Allen, E. M. Tekippe, R.-M. T. Woodford et al., “The NLRP3 inflammasome functions as a negative regulator of tumorigenesis during colitis-associated cancer,” Journal of Experimental Medicine, vol. 207, no. 5, pp. 1045–1056, 2010. View at Publisher · View at Google Scholar · View at Scopus
  54. M. A. Sze, M. Tsuruta, S.-W. J. Yang et al., “Changes in the bacterial microbiota in gut, blood, and lungs following acute LPS instillation into mice lungs,” PLoS ONE, vol. 9, no. 10, Article ID e111228, 2014. View at Publisher · View at Google Scholar · View at Scopus
  55. M. A. Sze, P. A. Dimitriu, M. Suzuki et al., “Host response to the lung microbiome in chronic obstructive pulmonary disease,” American Journal of Respiratory and Critical Care Medicine, vol. 192, no. 4, pp. 438–445, 2015. View at Publisher · View at Google Scholar · View at Scopus
  56. A. F. Goddard, B. J. Staudinger, S. E. Dowd et al., “Direct sampling of cystic fibrosis lungs indicates that DNA-based analyses of upper-airway specimens can misrepresent lung microbiota,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 34, pp. 13769–13774, 2012. View at Publisher · View at Google Scholar · View at Scopus
  57. R. P. Dickson, J. R. Erb-Downward, and G. B. Huffnagle, “Towards an ecology of the lung: New conceptual models of pulmonary microbiology and pneumonia pathogenesis,” The Lancet Respiratory Medicine, vol. 2, no. 3, pp. 238–246, 2014. View at Publisher · View at Google Scholar · View at Scopus
  58. R. P. Dickson, F. J. Martinez, and G. B. Huffnagle, “The role of the microbiome in exacerbations of chronic lung diseases,” The Lancet, vol. 384, no. 9944, pp. 691–702, 2014. View at Publisher · View at Google Scholar · View at Scopus
  59. A. Venkataraman, C. M. Bassis, J. M. Beck et al., “Application of a neutral community model to assess structuring of the human lung microbiome,” mBio, vol. 6, no. 1, Article ID e02284, 2015. View at Publisher · View at Google Scholar · View at Scopus
  60. E. R. Shanahan, L. Zhong, N. J. Talley, M. Morrison, and G. Holtmann, “Characterisation of the gastrointestinal mucosa-associated microbiota: a novel technique to prevent cross-contamination during endoscopic procedures,” Alimentary Pharmacology and Therapeutics, vol. 43, no. 11, pp. 1186–1196, 2016. View at Publisher · View at Google Scholar · View at Scopus
  61. S. Raviv, K. A. Hawkins, M. M. DeCamp Jr., and R. Kalhan, “Lung cancer in chronic obstructive pulmonary disease: Enhancing surgical options and outcomes,” American Journal of Respiratory and Critical Care Medicine, vol. 183, no. 9, pp. 1138–1146, 2011. View at Publisher · View at Google Scholar · View at Scopus
  62. A. El-Telbany and P. C. Ma, “Cancer genes in lung cancer: racial disparities: are there any?” Genes and Cancer, vol. 3, no. 7-8, pp. 467–480, 2012. View at Publisher · View at Google Scholar · View at Scopus
  63. R. A. Stockley, “Measurement of soluble proteins in lung secretion,” Thorax, vol. 39, no. 4, pp. 241–247, 1984. View at Publisher · View at Google Scholar · View at Scopus
  64. I. Fillion, N. Ouellet, M. Simard, Y. Bergeron, S. Sato, and M. G. Bergeron, “Role of chemokines and formyl peptides in pneumococcal pneumonia-induced monocyte/macrophage recruitment,” The Journal of Immunology, vol. 166, no. 12, pp. 7353–7361, 2001. View at Publisher · View at Google Scholar · View at Scopus
  65. L.-F. Lee, R. P. Hellendall, Y. Wang et al., “IL-8 reduced tumorigenicity of human ovarian cancer in vivo due to neutrophil infiltration,” Journal of Immunology, vol. 164, no. 5, pp. 2769–2775, 2000. View at Publisher · View at Google Scholar · View at Scopus
  66. P. J. Barnes, “Chronic obstructive pulmonary disease,” The New England Journal of Medicine, vol. 343, no. 4, pp. 269–280, 2000. View at Publisher · View at Google Scholar · View at Scopus
  67. S. Sethi, “Bacterial Infection and the Pathogenesis of COPD,” Chest, vol. 117, no. 5, pp. 286S–291S, 2000. View at Publisher · View at Google Scholar
  68. P. S. Hiemstra, S. Van Watering, and J. Stolk, “Neutrophil serine proteinases and defensins in chronic obstructive pulmonary disease: Effects on pulmonary epithelium,” European Respiratory Journal, vol. 12, no. 5, pp. 1200–1208, 1998. View at Publisher · View at Google Scholar · View at Scopus
  69. D. Worlitzsch, R. Tarran, M. Ulrich et al., “Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients,” The Journal of Clinical Investigation, vol. 109, no. 3, pp. 317–325, 2002. View at Publisher · View at Google Scholar · View at Scopus
  70. A. Schmidt, A. Belaaouaj, R. Bissinger et al., “Neutrophil elastase-mediated increase in airway temperature during inflammation,” Journal of Cystic Fibrosis, vol. 13, no. 6, pp. 623–631, 2014. View at Publisher · View at Google Scholar · View at Scopus
  71. P. P. Freestone, R. A. Hirst, S. M. Sandrini et al., “Pseudomonas aeruginosa-catecholamine inotrope interactions: A contributory factor in the development of ventilator-associated pneumonia?” Chest, vol. 142, no. 5, pp. 1200–1210, 2012. View at Publisher · View at Google Scholar · View at Scopus
  72. A. T. Hill, E. J. Campbell, S. L. Hill, D. L. Bayley, and R. A. Stockley, “Association between airway bacterial load and markers of airway inflammation in patients with stable chronic bronchitis,” American Journal of Medicine, vol. 109, no. 4, pp. 288–295, 2000. View at Publisher · View at Google Scholar · View at Scopus
  73. T. M. A. Wilkinson, I. S. Patel, M. Wilks, G. C. Donaldson, and J. A. Wedzicha, “Airway bacterial load and FEV1 decline in patients with chronic obstructive pulmonary disease,” American Journal of Respiratory and Critical Care Medicine, vol. 167, no. 8, pp. 1090–1095, 2003. View at Publisher · View at Google Scholar · View at Scopus
  74. W. Lin and M. Karin, “A cytokine-mediated link between innate immunity, inflammation, and cancer,” Journal of Clinical Investigation, vol. 117, no. 5, pp. 1175–1183, 2007. View at Publisher · View at Google Scholar · View at Scopus
  75. A. R. Davalos, J.-P. Coppe, J. Campisi, and P.-Y. Desprez, “Senescent cells as a source of inflammatory factors for tumor progression,” Cancer and Metastasis Reviews, vol. 29, no. 2, pp. 273–283, 2010. View at Publisher · View at Google Scholar · View at Scopus
  76. H. Takamori, Z. G. Oades, R. C. Hoch, M. Burger, and I. U. Schraufstatter, “Autocrine growth effect of IL-8 and GROalpha on a human pancreatic cancer cell line, Capan-1,” Pancreas, vol. 21, no. 1, pp. 52–56, 2000. View at Publisher · View at Google Scholar · View at Scopus
  77. K. Lang, B. Niggemann, K. S. Zanker, and F. Entschladen, “Signal processing in migrating T24 human bladder carcinoma cells: Role of the autocrine interleukin-8 loop,” International Journal of Cancer, vol. 99, no. 5, pp. 673–680, 2002. View at Publisher · View at Google Scholar · View at Scopus
  78. N. Mukaida, “Pathophysiological roles of interleukin-8/CXCL8 in pulmonary diseases,” The American Journal of Physiology—Lung Cellular and Molecular Physiology, vol. 284, no. 4, pp. L566–L577, 2003. View at Publisher · View at Google Scholar · View at Scopus
  79. S. R. Pine, L. E. Mechanic, L. Enewold et al., “Increased levels of circulating interleukin 6, interleukin 8, C-reactive protein, and risk of lung cancer,” Journal of the National Cancer Institute, vol. 103, no. 14, pp. 1112–1122, 2011. View at Publisher · View at Google Scholar · View at Scopus
  80. K. F. Budden, S. L. Gellatly, D. L. A. Wood et al., “Emerging pathogenic links between microbiota and the gut-lung axis,” Nature Reviews Microbiology, vol. 15, no. 1, pp. 55–63, 2017. View at Publisher · View at Google Scholar · View at Scopus
  81. G. B. Huffnagle, “The microbiota and allergies/asthma,” PLoS Pathogens, vol. 6, no. 5, Article ID e1000549, pp. 1–3, 2010. View at Publisher · View at Google Scholar · View at Scopus
  82. M. F. Neurath, S. Finotto, and L. H. Glimcher, “The role of TH1/TH2 polarization in mucosal immunity,” Nature Medicine, vol. 8, no. 6, pp. 567–573, 2002. View at Publisher · View at Google Scholar · View at Scopus
  83. T. B. Clarke, K. M. Davis, E. S. Lysenko, A. Y. Zhou, Y. Yu, and J. N. Weiser, “Recognition of peptidoglycan from the microbiota by NOD1 enhances systemic innate immunity,” Nature Medicine, vol. 16, no. 2, pp. 228–231, 2010. View at Publisher · View at Google Scholar · View at Scopus
  84. Z. Mikhak, J. P. Strassner, and A. D. Luster, “Lung dendritic cells imprint T cell lung homing and promote lung immunity through the chemokine receptor CCR4,” Journal of Experimental Medicine, vol. 210, no. 9, pp. 1855–1869, 2013. View at Publisher · View at Google Scholar · View at Scopus
  85. D. Ruane, L. Brane, B. S. Reis et al., “Lung dendritic cells induce migration of protective T cells to the gastrointestinal tract,” Journal of Experimental Medicine, vol. 210, no. 9, pp. 1871–1888, 2013. View at Publisher · View at Google Scholar · View at Scopus
  86. Y. Yun, G. Srinivas, S. Kuenzel et al., “Environmentally determined differences in the murine lung microbiota and their relation to alveolar architecture,” PLoS ONE, vol. 9, no. 12, Article ID 0113466, 2014. View at Publisher · View at Google Scholar · View at Scopus
  87. T.-B. Tsay, M.-C. Yang, P.-H. Chen, C.-M. Hsu, and L.-W. Chen, “Gut flora enhance bacterial clearance in lung through toll-like receptors 4,” Journal of Biomedical Science, vol. 18, no. 1, article 68, 2011. View at Publisher · View at Google Scholar · View at Scopus
  88. T. Ichinohe, I. K. Pang, Y. Kumamoto et al., “Microbiota regulates immune defense against respiratory tract influenza a virus infection,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 13, pp. 5354–5359, 2011. View at Publisher · View at Google Scholar · View at Scopus
  89. B. Boursi, R. Mamtani, K. Haynes, and Y.-X. Yang, “Recurrent antibiotic exposure may promote cancer formation-Another step in understanding the role of the human microbiota?” European Journal of Cancer, vol. 51, no. 17, pp. 2655–2664, 2015. View at Publisher · View at Google Scholar · View at Scopus
  90. K. Yoda, F. He, K. Miyazawa, M. Kawase, A. Kubota, and M. Hiramatsu, “Orally administered heat-killed Lactobacillus gasseri TMC0356 alters respiratory immune responses and intestinal microbiota of diet-induced obese mice,” Journal of Applied Microbiology, vol. 113, no. 1, pp. 155–162, 2012. View at Publisher · View at Google Scholar · View at Scopus
  91. J. C. Madan, D. C. Koestle, B. A. Stanton et al., “Serial analysis of the gut and respiratory microbiome in cystic fibrosis in infancy: Interaction between intestinal and respiratory tracts and impact of nutritional exposures,” mBio, vol. 3, no. 4, 2012. View at Publisher · View at Google Scholar · View at Scopus
  92. A. Trompette, E. S. Gollwitzer, K. Yadava et al., “Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis,” Nature Medicine, vol. 20, no. 2, pp. 159–166, 2014. View at Publisher · View at Google Scholar · View at Scopus
  93. D. S. Southam, M. Dolovich, P. M. O'Byrne, and M. D. Inman, “Distribution of intranasal instillations in mice: Effects of volume, time, body position, and anesthesia,” American Journal of Physiology - Lung Cellular and Molecular Physiology, vol. 282, no. 4, pp. L833–L839, 2002. View at Publisher · View at Google Scholar · View at Scopus
  94. D. S. Chen and I. Mellman, “Oncology meets immunology: the cancer-immunity cycle,” Immunity, vol. 39, no. 1, pp. 1–10, 2013. View at Publisher · View at Google Scholar · View at Scopus
  95. T. W. Hand, L. M. Dos Santos, N. Bouladoux et al., “Acute gastrointestinal infection induces long-lived microbiota-specific T cell responses,” Science, vol. 337, no. 6101, pp. 1553–1556, 2012. View at Publisher · View at Google Scholar · View at Scopus
  96. E. Slack, S. Hapfelmeier, B. Stecher et al., “Innate and adaptive immunity cooperate flexibly to maintain host-microbiota mutualism,” Science, vol. 325, no. 5940, pp. 617–620, 2009. View at Publisher · View at Google Scholar · View at Scopus
  97. N. Iida, A. Dzutsev, C. A. Stewart et al., “Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment,” Science, vol. 342, no. 6161, pp. 967–970, 2013. View at Publisher · View at Google Scholar · View at Scopus
  98. S. Viaud, F. Saccheri, G. Mignot et al., “The intestinal microbiota modulates the anticancer immune effects of cyclophosphamide,” Science, vol. 342, no. 6161, pp. 971–976, 2013. View at Publisher · View at Google Scholar · View at Scopus
  99. L. Zitvogel, M. Ayyoub, B. Routy, and G. Kroemer, “Microbiome and Anticancer Immunosurveillance,” Cell, vol. 165, no. 2, pp. 276–287, 2016. View at Publisher · View at Google Scholar · View at Scopus
  100. FAO/WHO, “Guidelines for the Evaluation of Probiotics,” 2002.
  101. A. Vásquez, G. Molin, B. Pettersson, M. Antonsson, and S. Ahrné, “DNA-based classification and sequence heterogeneities in the 16S rRNA genes of Lactobacillus casei/paracasei and related species,” Systematic and Applied Microbiology, vol. 28, no. 5, pp. 430–441, 2005. View at Publisher · View at Google Scholar · View at Scopus
  102. T. Matsuzaki, T. Yokokura, and I. Azuma, “Anti-tumour activity of Lactobacillus casei on lewis lung carcinoma and line-10 hepatoma in syngeneic mice and guinea pigs,” Cancer Immunology Immunotherapy, vol. 20, no. 1, pp. 18–22, 1985. View at Publisher · View at Google Scholar · View at Scopus
  103. K. Kelly, J. Crowley, J. Bunn P.A. et al., “Randomized phase III trial of paclitaxel plus carboplatin versus vinorelbine plus cisplatin in the treatment of patients with advanced non—small-cell lung cancer: a Southwest Oncology Group trial,” Journal of Clinical Oncology: Official Journal of the American Society of Clinical Oncology, vol. 19, no. 13, pp. 3210–3218, 2001. View at Publisher · View at Google Scholar · View at Scopus
  104. A. Sistigu, S. Viaud, N. Chaput, L. Bracci, E. Proietti, and L. Zitvogel, “Immunomodulatory effects of cyclophosphamide and implementations for vaccine design,” Seminars in Immunopathology, pp. 1–15, 2011. View at Publisher · View at Google Scholar · View at Scopus
  105. Q.-F. Gui, H.-F. Lu, C.-X. Zhang, Z.-R. Xu, and Y.-M. Yang, “Well-balanced commensal microbiota contributes to anti-cancer response in a lung cancer mouse model,” Genetics and Molecular Research, vol. 14, no. 2, pp. 5642–5651, 2015. View at Publisher · View at Google Scholar · View at Scopus
  106. A. Sivan, L. Corrales, and N. Hubert, “Commensal Bifidobacterium promotes antitumor immunity and facilitates anti PD-L1 efficacy,” Science, vol. 350, pp. 1084–1089, 2015. View at Publisher · View at Google Scholar
  107. M. Vétizou, J. M. Pitt, R. Daillère et al., “Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota,” Science, vol. 350, no. 6264, pp. 1079–1084, 2015. View at Publisher · View at Google Scholar · View at Scopus
  108. R. Daillère, M. Vétizou, N. Waldschmitt et al., “Enterococcus hirae and Barnesiella intestinihominis Facilitate Cyclophosphamide-Induced Therapeutic Immunomodulatory Effects,” Immunity, vol. 45, no. 4, pp. 931–943, 2016. View at Publisher · View at Google Scholar · View at Scopus