Streptomycin treatment alters the intestinal microbiome, pulmonary T cell profile and airway hyperresponsiveness in a cystic fibrosis mouse model

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Bazett, Mark ^a   Bergeron, Marie Eve ^a   Haston, Christina K ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; STREPTOMYCIN;

ANIMAL; BACTERIAL LOAD; BAGG ALBINO MOUSE; BONE; COMPLICATION; CYSTIC FIBROSIS; DISEASE MODEL; DRUG EFFECTS; FEMALE; IMMUNOLOGY; IMMUNOMODULATION; IMMUNOPHENOTYPING; INTESTINE FLORA; METABOLISM; METAGENOME; METAGENOMICS; MORTALITY; MOUSE; PATHOLOGY; PHENOTYPE; RESPIRATORY HYPERSENSITIVITY; T LYMPHOCYTE SUBPOPULATION; TRANSGENIC MOUSE;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIAL LOAD; BONE AND BONES; CYSTIC FIBROSIS; DISEASE MODELS, ANIMAL; FEMALE; GASTROINTESTINAL MICROBIOME; IMMUNOMODULATION; IMMUNOPHENOTYPING; METAGENOME; METAGENOMICS; MICE; MICE, INBRED BALB C; MICE, TRANSGENIC; PHENOTYPE; RESPIRATORY HYPERSENSITIVITY; STREPTOMYCIN; T-LYMPHOCYTE SUBSETS;

EID: 84954460126     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep19189     Document Type: Article

References (82)

1. O'Sullivan, B. P. & Freedman, S. D. Cystic fibrosis. Lancet 373, 1891-1904, (2009).
2. Brand, P. L. Bronchodilators in cystic fibrosis. J. R. Soc. Med. 93 Suppl 38, 37-39, (2000).
3. Balfour-Lynn, I. M. & Elborn, J. S. "CF asthma": what is it and what do we do about it? Thorax 57, 742-748, (2002).
4. Kent, B. D. et al. Asthma and cystic fibrosis: a tangled web. Pediatr. Pulmonol. 49, 205-213, (2014).
5. Mitchell, I., Corey, M., Woenne, R., Krastins, I. R. & Levison, H. Bronchial hyperreactivity in cystic fibrosis and asthma. J. Pediatr. 93, 744-748, (1978).
6. Eggleston, P. A., Rosenstein, B. J., Stackhouse, C. M. & Alexander, M. F. Airway hyperreactivity in cystic fibrosis. Clinical correlates and possible effects on the course of the disease. Chest 94, 360-365, (1988).
7. van der Doef, H. P., Kokke, F. T., van der Ent, C. K. & Houwen, R. H. Intestinal obstruction syndromes in cystic fibrosis: meconium ileus, distal intestinal obstruction syndrome, and constipation. Curr. Gastroenterol. Rep. 13, 265-270, (2011).
8. Lisowska, A., Wojtowicz, J. & Walkowiak, J. Small intestine bacterial overgrowth is frequent in cystic fibrosis: combined hydrogen and methane measurements are required for its detection. Acta. Biochim. Pol. 56, 631-634, (2009).
9. Bruzzese, E. et al. Disrupted intestinal microbiota and intestinal inflammation in children with cystic fibrosis and its restoration with Lactobacillus GG: a randomised clinical trial. PLoS One 9, e87796, (2014).
10. Hoffman, L. R. et al. Escherichia coli dysbiosis correlates with gastrointestinal dysfunction in children with cystic fibrosis. Clin. Infect. Dis. 58, 396-399, (2014).
11. Scanlan, P. D. et al. Gut dysbiosis in cystic fibrosis. J. Cyst. Fibros. 11, 454-455, (2012).
12. Duytschaever, G. et al. Cross-sectional and longitudinal comparisons of the predominant fecal microbiota compositions of a group of pediatric patients with cystic fibrosis and their healthy siblings. Appl. Environ. Microbiol. 77, 8015-8024, (2011).
13. Duytschaever, G. et al. Dysbiosis of bifidobacteria and Clostridium cluster XIVa in the cystic fibrosis fecal microbiota. J. Cyst. Fibros. 12, 206-215, (2013).
14. Stalvey, M. S. & Clines, G. A. Cystic fibrosis-related bone disease: insights into a growing problem. Curr. Opin. Endocrinol. Diabetes Obes. 20, 547-552, (2013).
15. Putman, M. S. et al. Compromised bone microarchitecture and estimated bone strength in young adults with cystic fibrosis. J. Clin. Endocrinol. Metab. 99, 3399-3407, (2014).
16. De Lisle, R. C. & Borowitz, D. The cystic fibrosis intestine. Cold Spring Harb. Perspect. Med. 3, a009753, (2013).
17. Bazett, M., Stefanov, A. N., Paun, A., Paradis, J. & Haston, C. K. Strain-dependent airway hyperresponsiveness and a chromosome 7 locus of elevated lymphocyte numbers in cystic fibrosis transmembrane conductance regulator-deficient mice. J. Immunol. 188, 2297-2304, (2012).
18. Bazett, M. & Haston, C. K. Airway hyperresponsiveness in FVB/N delta F508 cystic fibrosis transmembrane conductance regulator mice. J. Cyst. Fibros. 13, 378-383, (2014).
19. Haston, C. K., Li, W., Li, A., Lafleur, M. & Henderson, J. E. Persistent osteopenia in adult cystic fibrosis transmembrane conductance regulator-deficient mice. Am. J. Respir. Crit. Care Med. 177, 309-315, (2008).
20. Wilke, M. et al. Mouse models of cystic fibrosis: phenotypic analysis and research applications. J. Cyst. Fibros. 10 Suppl 2, S152-171, (2011).
21. Bazett, M. et al. Cystic fibrosis mouse model-dependent intestinal structure and gut microbiome. Mamm. Genome 26, 222-234, (2015).
22. Bazett, M., Paun, A. & Haston, C. K. Micro RNA profiling of cystic fibrosis intestinal disease in mice. Mol. Genet. Metab. 103, 38-43, (2011).
23. Canale-Zambrano, J. C., Auger, M. L. & Haston, C. K. Toll-like receptor-4 genotype influences the survival of cystic fibrosis mice. Am. J. Physiol. Gastrointest. Liver. Physiol. 299, G381-390, (2010).
24. Durie, P. R., Kent, G., Phillips, M. J. & Ackerley, C. A. Characteristic multiorgan pathology of cystic fibrosis in a long-living cystic fibrosis transmembrane regulator knockout murine model. Am. J. Pathol. 164, 1481-1493, (2004).
25. Kent, G. et al. Phenotypic abnormalities in long-term surviving cystic fibrosis mice. Pediatr. Res. 40, 233-241, (1996).
26. Canale-Zambrano, J. C. & Haston, C. K. IGF binding protein-3 treatment alters intestinal cell proliferation but not body weight of adult cystic fibrosis transmembrane conductance regulator deficient mice. Pediatr. Res. 69, 129-134, (2011).
27. Norkina, O., Burnett, T. G. & De Lisle, R. C. Bacterial overgrowth in the cystic fibrosis transmembrane conductance regulator null mouse small intestine. Infect. Immun. 72, 6040-6049, (2004).
28. Lynch, S. V. et al. Cystic fibrosis transmembrane conductance regulator knockout mice exhibit aberrant gastrointestinal microbiota. Gut Microbes. 4, 41-47, (2013).
29. Ivanov, I. I. et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139, 485-498, (2009).
30. Olszak, T. et al. Microbial exposure during early life has persistent effects on natural killer T cell function. Science 336, 489-493, (2012).
31. Preidis, G. A. et al. Probiotics stimulate enterocyte migration and microbial diversity in the neonatal mouse intestine. FASEB J. 26, 1960-1969, (2012).
32. Russell, S. L. et al. Early life antibiotic-driven changes in microbiota enhance susceptibility to allergic asthma. EMBO Rep. 13, 440-447, (2012).
33. Ichinohe, T. et al. Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc. Natl. Acad. Sci. USA 108, 5354-5359, (2011).
34. Trompette, A. et al. Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nat. Med. 20, 159-166, (2014).
35. Sjogren, K. et al. The gut microbiota regulates bone mass in mice. J. Bone Miner. Res. 27, 1357-1367, (2012).
36. Fujimura, K. E. et al. House dust exposure mediates gut microbiome Lactobacillus enrichment and airway immune defense against allergens and virus infection. Proc. Natl. Acad. Sci. USA 111, 805-810, (2014).
37. Herbst, T. et al. Dysregulation of allergic airway inflammation in the absence of microbial colonization. Am. J. Respir. Crit. Care. Med. 184, 198-205, (2011).
38. Hill, D. A. et al. Commensal bacteria-derived signals regulate basophil hematopoiesis and allergic inflammation. Nat. Med. 18, 538-546, (2012).
39. Russell, S. L. et al. Perinatal antibiotic-induced shifts in gut microbiota have differential effects on inflammatory lung diseases. J. Allergy Clin. Immunol. 135, 100-109, (2015).
40. Bernard, H. et al. Dietary pectin-derived acidic oligosaccharides improve the pulmonary bacterial clearance of Pseudomonas aeruginosa lung infection in mice by modulating intestinal microbiota and immunity. J. Infect. Dis. 211, 156-165, (2015).
41. Buggs, C. W. et al. The Absorption, Distribution, and Excretion of Streptomycin in Man. J. Clin. Invest. 25, 94-102, (1946).
42. Haston, C. K., Humes, D. G. & Lafleur, M. X chromosome transmission ratio distortion in CFTR +/- intercross-derived mice. BMC Genet. 8, 23, (2007).
43. Haston, C. K., Corey, M. & Tsui, L. C. Mapping of genetic factors influencing the weight of cystic fibrosis knockout mice. Mamm. Genome 13, 614-618, (2002).
44. Lambrecht, B. N. & Hammad, H. The immunology of asthma. Nat. Immunol. 16, 45-56, (2015).
45. Hoen, A. G. et al. Associations between Gut Microbial Colonization in Early Life and Respiratory Outcomes in Cystic Fibrosis. J. Pediatr. 167, 138-47, (2015).
46. Bruzzese, E. et al. Effect of Lactobacillus GG supplementation on pulmonary exacerbations in patients with cystic fibrosis: a pilot study. Clin. Nutr. 26, 322-328, (2007).
47. Di Nardo, G. et al. Lactobacillus reuteri ATCC55730 in cystic fibrosis. J. Pediatr. Gastroenterol. Nutr. 58, 81-86, (2014).
48. Weiss, B. et al. Probiotic supplementation affects pulmonary exacerbations in patients with cystic fibrosis: a pilot study. Pediatr. Pulmonol. 45, 536-540, (2010).
49. Hubeau, C. et al. Quantitative analysis of inflammatory cells infiltrating the cystic fibrosis airway mucosa. Clin. Exp. Immunol. 124, 69-76, (2001).
50. Regamey, N. et al. Distinct patterns of inflammation in the airway lumen and bronchial mucosa of children with cystic fibrosis. Thorax 67, 164-170, (2012).
51. Chan, Y. R. et al. Patients with cystic fibrosis have inducible IL-17+ IL-22+ memory cells in lung draining lymph nodes. J. Allergy. Clin. Immunol. 131, 1117-1129, 1129 e1111-1115, (2013).
52. Tiringer, K. et al. A Th17- and Th2-skewed cytokine profile in cystic fibrosis lungs represents a potential risk factor for Pseudomonas aeruginosa infection. Am. J. Respir. Crit. Care. Med. 187, 621-629, (2013).
53. Hartl, D. et al. Pulmonary T(H)2 response in Pseudomonas aeruginosa-infected patients with cystic fibrosis. J. Allergy Clin. Immunol. 117, 204-211, (2006).
54. Cheng, M. et al. Microbiota modulate tumoral immune surveillance in lung through a gammadelta T17 immune cell-dependent mechanism. Cancer Res. 74, 4030-4041, (2014).
55. Matsubara, S. et al. Vgamma1+ T cells and tumor necrosis factor-alpha in ozone-induced airway hyperresponsiveness. Am. J. Respir. Cell. Mol. Biol. 40, 454-463, (2009).
56. Hahn, Y. S. et al. V gamma 4+ gamma delta T cells regulate airway hyperreactivity to methacholine in ovalbumin-sensitized and challenged mice. J. Immunol. 171, 3170-3178, (2003).
57. Lahn, M. et al. MHC class I-dependent Vgamma4+ pulmonary T cells regulate alpha beta T cell-independent airway responsiveness. Proc. Natl. Acad. Sci. USA 99, 8850-8855, (2002).
58. Hahn, Y. S. et al. Different potentials of gamma delta T cell subsets in regulating airway responsiveness: V gamma 1+ cells, but not V gamma 4+ cells, promote airway hyperreactivity, Th2 cytokines, and airway inflammation. J. Immunol. 172, 2894-2902, (2004).
59. Decraene, A. et al. Elevated expression of both mRNA and protein levels of IL-17A in sputum of stable Cystic Fibrosis patients. Respir. Res. 11, 177, (2010).
60. McAllister, F. et al. Role of IL-17A, IL-17F, and the IL-17 receptor in regulating growth-related oncogene-alpha and granulocyte colony-stimulating factor in bronchial epithelium: implications for airway inflammation in cystic fibrosis. J. Immunol. 175, 404-412, (2005).
61. Tan, H. L. et al. The Th17 pathway in cystic fibrosis lung disease. Am. J. Respir. Crit. Care. Med. 184, 252-258, (2011).
62. Duan, J., Chung, H., Troy, E. & Kasper, D. L. Microbial colonization drives expansion of IL-1 receptor 1-expressing and IL-17-producing gamma/delta T cells. Cell Host Microbe 7, 140-150, (2010).
63. Noverr, M. C., Falkowski, N. R., McDonald, R. A., McKenzie, A. N. & Huffnagle, G. B. Development of allergic airway disease in mice following antibiotic therapy and fungal microbiota increase: role of host genetics, antigen, and interleukin-13. Infect. Immun. 73, 30-38, (2005).
64. Kaur, S., Norkina, O., Ziemer, D., Samuelson, L. C. & De Lisle, R. C. Acidic duodenal pH alters gene expression in the cystic fibrosis mouse pancreas. Am. J. Physiol. Gastrointest. Liver. Physiol. 287, G480-490, (2004).
65. Wlodarska, M. et al. Antibiotic treatment alters the colonic mucus layer and predisposes the host to exacerbated Citrobacter rodentium-induced colitis. Infect. Immun. 79, 1536-1545, (2011).
66. Tang, C. et al. Inhibition of Dectin-1 Signaling Ameliorates Colitis by Inducing Lactobacillus-Mediated Regulatory T Cell Expansion in the Intestine. Cell Host Microbe 18, 183-97, (2015).
67. Liu, Y., Tran, D. Q., Fatheree, N. Y. & Marc Rhoads, J. Lactobacillus reuteri DSM 17938 differentially modulates effector memory T cells and Foxp3+ regulatory T cells in a mouse model of necrotizing enterocolitis. Am. J. Physiol. Gastrointest. Liver Physiol. 307, G177-86, (2014).
68. Sadarangani, S. P., Estes, L. L. & Steckelberg, J. M. Non-anti-infective effects of antimicrobials and their clinical applications: a review. Mayo Clin. Proc. 90, 109-27, (2015).
69. Haston, C. K., Cory, S., Lafontaine, L., Dorion, G. & Hallett, M. T. Strain-dependent pulmonary gene expression profiles of a cystic fibrosis mouse model. Physiol. Genomics 25, 336-345, (2006).
70. Clarke, L. L., Gawenis, L. R., Franklin, C. L. & Harline, M. C. Increased survival of CFTR knockout mice with an oral osmotic laxative. Lab. Anim. Sci. 46, 612-618, (1996).
71. Smyth, A. R. et al. European Cystic Fibrosis Society Standards of Care: Best Practice guidelines. J. Cyst. Fibros. 13 Suppl 1, S23-42 (2014).
72. Ott, S. J., Musfeldt, M., Ullmann, U., Hampe, J. & Schreiber, S. Quantification of intestinal bacterial populations by real-time PCR with a universal primer set and minor groove binder probes: a global approach to the enteric flora. J. Clin. Microbiol. 42, 2566-2572, (2004).
73. Yu, Z. & Morrison, M. Improved extraction of PCR-quality community DNA from digesta and fecal samples. Biotechniques 36, 808-812, (2004).
74. Dowd, S. E. et al. Polymicrobial nature of chronic diabetic foot ulcer biofilm infections determined using bacterial tag encoded FLX amplicon pyrosequencing (bTEFAP). PLoS One 3, e3326, (2008).
75. Schloss, P. D. et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537-7541, (2009).
76. Schloss, P. D., Gevers, D. & Westcott, S. L. Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One 6, e27310, (2011).
77. Wang, Q., Garrity, G. M., Tiedje, J. M. & Cole, J. R. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73, 5261-5267, (2007).
78. Paradis, J., Wilke, M. & Haston, C. K. Osteopenia in CFTR-deltaF508 mice. J. Cyst. Fibros. 9, 239-245, (2010).
79. Misharin, A. V., Morales-Nebreda, L., Mutlu, G. M., Budinger, G. R. & Perlman, H. Flow cytometric analysis of macrophages and dendritic cell subsets in the mouse lung. Am. J. Respir. Cell. Mol. Biol. 49, 503-510, (2013).
80. Evans, J., Sheneman, L. & Foster, J. Relaxed neighbor joining: a fast distance-based phylogenetic tree construction method. J. Mol. Evol. 62, 785-792, (2006).
81. Shannon, C. E. & Weaver, W. A mathematic theory of communication. Bell Syst. Tech. J. 27, 379-423 and 623-656, (1948).
82. White, J. R., Nagarajan, N. & Pop, M. Statistical methods for detecting differentially abundant features in clinical metagenomic samples. PLoS Comput. Biol. 5, e1000352, (2009).