Early-Life Antibiotic Exposure Causes Intestinal Dysbiosis and Exacerbates Skin and Lung Pathology in Experimental Systemic Sclerosis

Journal of Investigative Dermatology

Volumn 137, Issue 11, 2017, Pages 2316-2325

  Mehta, Heena ^a   Goulet, Philippe Olivier ^a   Mashiko, Shunya ^a   Desjardins, Jade ^a   Pérez, Gemma ^a   Koenig, Martial ^a   Senécal, Jean Luc ^a   Constante, Marco ^a   Santos, Manuela M ^a   Sarfati, Marika ^a  

^a CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DNA TOPOISOMERASE; INTERLEUKIN 13; STREPTOMYCIN; BACTERIAL DNA;

ADULTHOOD; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTEROIDETES; CELL INFILTRATION; COL1A1 GENE; CONTROLLED STUDY; DENDRITIC CELL; DISEASE EXACERBATION; DYSBIOSIS; FIRMICUTES; GENE EXPRESSION; HOUSEKEEPING GENE; INFLAMMATORY CELL; LUNG FIBROSIS; LUNG PARENCHYMA; MAST CELL; MONONUCLEAR PHAGOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SERPINE1 GENE; SKIN; SKIN FIBROSIS; SYSTEMIC SCLEROSIS; AGE; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; DISEASE MODEL; DRUG EFFECTS; FEMALE; GENETICS; HUMAN; IMMUNOLOGY; INTESTINE FLORA; MALE; MICROBIOLOGY; NONPARAMETRIC TEST; PATHOLOGY; PROCEDURES; RANDOMIZATION; REAL TIME POLYMERASE CHAIN REACTION; RISK FACTOR; TRANSGENIC MOUSE;

AGE FACTORS; ANIMALS; CELLS, CULTURED; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; DNA, BACTERIAL; DYSBIOSIS; FEMALE; GASTROINTESTINAL MICROBIOME; HUMANS; MALE; MICE; MICE, INBRED BALB C; MICE, TRANSGENIC; PULMONARY FIBROSIS; RANDOM ALLOCATION; REAL-TIME POLYMERASE CHAIN REACTION; RISK FACTORS; SCLERODERMA, SYSTEMIC; STATISTICS, NONPARAMETRIC; STREPTOMYCIN;

EID: 85032017630     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1016/j.jid.2017.06.019     Document Type: Article

References (55)

1. Abrahamsson, T.R., Jakobsson, H.E., Andersson, A.F., Bjorksten, B., Engstrand, L., Jenmalm, M.C., Low diversity of the gut microbiota in infants with atopic eczema. J Allergy Clin Immunol 129 (2012), 434–440 40.e1–2.
2. Allakhverdi, Z., Comeau, M.R., Delespesse, G., Dexamethasone regulation of thymic stromal lymphopoietin receptor expression on mast cells and their precursors. J Allergy Clin Immunol 127 (2011), 523–524.e1–2.
3. Allakhverdi, Z., Comeau, M.R., Smith, D.E., Toy, D., Endam, L.M., Desrosiers, M., et al. CD34+ hemopoietic progenitor cells are potent effectors of allergic inflammation. J Allergy Clin Immunol 123 (2009), 472–478.
4. Arron, S.T., Dimon, M.T., Li, Z., Johnson, M.E., A Wood, T., Feeney, L., et al. High Rhodotorula sequences in skin transcriptome of patients with diffuse systemic sclerosis. J Invest Dermatol 134 (2014), 2138–2145.
5. Barfod, K.K., Vrankx, K., Mirsepasi-Lauridsen, H.C., Hansen, J.S., Hougaard, K.S., Larsen, S.T., et al. The murine lung microbiome changes during lung inflammation and intranasal vancomycin treatment. Open Microbiol J 9 (2015), 167–179.
6. Bazett, M., Bergeron, M.E., Haston, C.K., Streptomycin treatment alters the intestinal microbiome, pulmonary T cell profile and airway hyperresponsiveness in a cystic fibrosis mouse model. Sci Rep, 6, 2016, 19189.
7. Brembilla, N.C., Chizzolini, C., T cell abnormalities in systemic sclerosis with a focus on Th17 cells. Eur Cytokine Netw 23 (2012), 128–139.
8. Candon, S., Perez-Arroyo, A., Marquet, C., Valette, F., Foray, A.P., Pelletier, B., et al. Antibiotics in early life alter the gut microbiome and increase disease incidence in a spontaneous mouse model of autoimmune insulin-dependent diabetes. PLoS One, 10, 2015, e0125448.
9. Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7 (2010), 335–336.
10. Christmann, R.B., Mathes, A., Affandi, A.J., Padilla, C., Nazari, B., Bujor, A.M., et al. Thymic stromal lymphopoietin is up-regulated in the skin of patients with systemic sclerosis and induces profibrotic genes and intracellular signaling that overlap with those induced by interleukin-13 and transforming growth factor beta. Arthritis Rheum 65 (2013), 1335–1346.
11. Fujimura, K.E., Sitarik, A.R., Havstad, S., Lin, D.L., Levan, S., Fadrosh, D., et al. Neonatal gut microbiota associates with childhood multisensitized atopy and T cell differentiation. Nat Med 22 (2016), 1187–1191.
12. Giacomelli, R., Matucci-Cerinic, M., Cipriani, P., Ghersetich, I., Lattanzio, R., Pavan, A., et al. Circulating Vdelta1+ T cells are activated and accumulate in the skin of systemic sclerosis patients. Arthritis Rheum 41 (1998), 327–334.
13. Granel, B., Allanore, Y., Chevillard, C., Arnaud, V., Marquet, S., Weiller, P.J., et al. IL13RA2 gene polymorphisms are associated with systemic sclerosis. J Rheumatol 33 (2006), 2015–2019.
14. Granel, B., Chevillard, C., Allanore, Y., Arnaud, V., Cabantous, S., Marquet, S., et al. Evaluation of interleukin 13 polymorphisms in systemic sclerosis. Immunogenetics 58 (2006), 693–699.
15. Greenblatt, M.B., Sargent, J.L., Farina, G., Tsang, K., Lafyatis, R., Glimcher, L.H., et al. Interspecies comparison of human and murine scleroderma reveals IL-13 and CCL2 as disease subset-specific targets. Am J Pathol 180 (2012), 1080–1094.
16. Gruschwitz, M.S., Vieth, G., Up-regulation of class II major histocompatibility complex and intercellular adhesion molecule 1 expression on scleroderma fibroblasts and endothelial cells by interferon-γ and tumor necrosis factor α in the early disease stage. Arthritis Rheum 40 (1997), 540–550.
17. Hansen, C.H., Krych, L., Nielsen, D.S., Vogensen, F.K., Hansen, L.H., Sorensen, S.J., et al. Early life treatment with vancomycin propagates Akkermansia muciniphila and reduces diabetes incidence in the NOD mouse. Diabetologia 55 (2012), 2285–2294.
18. Hevia, A., Milani, C., Lopez, P., Cuervo, A., Arboleya, S., Duranti, S., et al. Intestinal dysbiosis associated with systemic lupus erythematosus. mBio, 5, 2014 e01548–14.
19. Hu, Y., Jin, P., Peng, J., Zhang, X., Wong, F.S., Wen, L., Different immunological responses to early-life antibiotic exposure affecting autoimmune diabetes development in NOD mice. J Autoimmun 72 (2016), 47–56.
20. Hu, Y., Peng, J., Tai, N., Hu, C., Zhang, X., Wong, F.S., et al. Maternal antibiotic treatment protects offspring from diabetes development in nonobese diabetic mice by generation of tolerogenic APCs. J Immunol 195 (2015), 4176–4184.
21. Johnson, B.M., Gaudreau, M.C., Al-Gadban, M.M., Gudi, R., Vasu, C., Impact of dietary deviation on disease progression and gut microbiome composition in lupus-prone SNF1 mice. Clin Exp Immunol 181 (2015), 323–337.
22. Knip, M., Siljander, H., The role of the intestinal microbiota in type 1 diabetes mellitus. Nat Rev Endocrinol 12 (2016), 154–167.
23. Lemaire, R., Burwell, T., Sun, H., Delaney, T., Bakken, J., Cheng, L., et al. Resolution of skin fibrosis by neutralization of the antifibrinolytic function of plasminogen activator inhibitor 1. Arthritis Rheumatol 68 (2016), 473–483.
24. Matsushita, M., Yamamoto, T., Nishioka, K., Upregulation of interleukin-13 and its receptor in a murine model of bleomycin-induced scleroderma. Int Arch Allergy Immunol 135 (2004), 348–356.
25. McMurdie, P.J., Holmes, S., Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One, 8, 2013, e61217.
26. Mehta, H., Goulet, P.O., Nguyen, V., Perez, G., Koenig, M., Senecal, J.L., et al. Topoisomerase I peptide-loaded dendritic cells induce autoantibody response as well as skin and lung fibrosis. Autoimmunity 49 (2016), 1–11.
27. Mehta, H., Mashiko, S., Goulet, P.O., Desjardins, J., Perez, G., Koenig, M., et al. Dabigatran aggravates topoisomerase I peptide-loaded dendritic cells-induced lung and skin fibrosis. Clin Exp Rheumatol, 2017.
28. Naik, S., Bouladoux, N., Wilhelm, C., Molloy, M.J., Salcedo, R., Kastenmuller, W., et al. Compartmentalized control of skin immunity by resident commensals. Science 337 (2012), 1115–1119.
29. Nieuwenhuis, E.E.S., Visser, M.R., Kavelaars, A., Cobelens, P.M., Fleer, A., Harmsen, W., et al. Oral antibiotics as a novel therapy for arthritis: evidence for a beneficial effect of intestinal Escherichia coli. Arthritis Rheum 43 (2000), 2583–2589.
30. Ochoa-Reparaz, J., Mielcarz, D.W., Ditrio, L.E., Burroughs, A.R., Foureau, D.M., Haque-Begum, S., et al. Role of gut commensal microflora in the development of experimental autoimmune encephalomyelitis. J Immunol 183 (2009), 6041–6050.
31. Okamoto, Y., Hasegawa, M., Matsushita, T., Hamaguchi, Y., Huu, D.L., Iwakura, Y., et al. Potential roles of interleukin-17A in the development of skin fibrosis in mice. Arthritis Rheum 64 (2012), 3726–3735.
32. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O'Hara RB, et al. vegan: Community Ecology Package. R package version 2.3-2. http://CRAN.R-project.org/package=vegan; 2015. Accessed 18 July 2016.
33. Olszak, T., An, D., Zeissig, S., Vera, M.P., Richter, J., Franke, A., et al. Microbial exposure during early life has persistent effects on natural killer T cell function. Science 336 (2012), 489–493.
34. Pattanaik, D., Brown, M., Postlethwaite, B.C., Postlethwaite, A.E., Pathogenesis of systemic sclerosis. Front Immunol, 6, 2015, 272.
35. Penders, J., Gerhold, K., Stobberingh, E.E., Thijs, C., Zimmermann, K., Lau, S., et al. Establishment of the intestinal microbiota and its role for atopic dermatitis in early childhood. J Allergy Clin Immunol 132 (2013), 601–607.e8.
36. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/; 2015. Accessed 18 July 2016.
37. Ruane, D., Chorny, A., Lee, H., Faith, J., Pandey, G., Shan, M., et al. Microbiota regulate the ability of lung dendritic cells to induce IgA class-switch recombination and generate protective gastrointestinal immune responses. J Exp Med 213 (2016), 53–73.
38. Russell, S.L., Gold, M.J., Hartmann, M., Willing, B.P., Thorson, L., Wlodarska, M., et al. Early life antibiotic-driven changes in microbiota enhance susceptibility to allergic asthma. EMBO Rep 13 (2012), 440–447.
39. Russell, S.L., Gold, M.J., Reynolds, L.A., Willing, B.P., Dimitriu, P., Thorson, L., et al. Perinatal antibiotic-induced shifts in gut microbiota have differential effects on inflammatory lung diseases. J Allergy Clin Immunol 135 (2015), 100–109.
40. Russell, S.L., Gold, M.J., Willing, B.P., Thorson, L., McNagny, K.M., Finlay, B.B., Perinatal antibiotic treatment affects murine microbiota, immune responses and allergic asthma. Gut Microbes 4 (2013), 158–164.
41. Samuelson, D.R., Welsh, D.A., Shellito, J.E., Regulation of lung immunity and host defense by the intestinal microbiota. Front Microbiol, 6, 2015, 1085.
42. Sargent, J.L., Li, Z., Aliprantis, A.O., Greenblatt, M., Lemaire, R., Wu, M.H., et al. Identification of optimal mouse models of systemic sclerosis by interspecies comparative genomics. Arthritis Rheumatol 68 (2016), 2003–2015.
43. Segawa, S., Goto, D., Horikoshi, M., Kondo, Y., Umeda, N., Hagiwara, S., et al. Involvement of CD161+ Vdelta1+ gammadelta T cells in systemic sclerosis: association with interstitial pneumonia. Rheumatology 53 (2014), 2259–2269.
44. Truchetet, M.-E., Brembilla, N.-C., Montanari, E., Lonati, P., Raschi, E., Zeni, S., et al. Interleukin-17A+ cell counts are increased in systemic sclerosis skin and their number is inversely correlated with the extent of skin involvement. Arthritis Rheum 65 (2013), 1347–1356.
45. Truchetet, M.E., Demoures, B., Eduardo Guimaraes, J., Bertrand, A., Laurent, P., Jolivel, V., et al. Platelets induce thymic stromal lymphopoietin production by endothelial cells: contribution to human systemic sclerosis fibrosis. Arthritis Rheumatol 68 (2016), 2784–2794.
46. Ueda-Hayakawa, I., Hasegawa, M., Hamaguchi, Y., Takehara, K., Fujimoto, M., Circulating gamma/delta T cells in systemic sclerosis exhibit activated phenotype and enhance gene expression of proalpha2(I) collagen of fibroblasts. J Dermatol Sci 69 (2013), 54–60.
47. Usategui, A., Criado, G., Izquierdo, E., Del Rey, M.J., Carreira, P.E., Ortiz, P., et al. A profibrotic role for thymic stromal lymphopoietin in systemic sclerosis. Ann Rheum Dis 72 (2013), 2018–2023.
48. Volkmann, E.R., Chang, Y.L., Barroso, N., Furst, D.E., Clements, P.J., Gorn, A.H., et al. Association of systemic sclerosis with a unique colonic microbial consortium. Arthritis Rheumatol 68 (2016), 1483–1492.
49. Wick, G., Grundtman, C., Mayerl, C., Wimpissinger, T.F., Feichtinger, J., Zelger, B., et al. The immunology of fibrosis. Ann Rev Immunol 31 (2013), 107–135.
50. Yang, X., Yang, J., Xing, X., Wan, L., Li, M., Increased frequency of Th17 cells in systemic sclerosis is related to disease activity and collagen overproduction. Arthritis Res Ther, 16, 2014, R4.
51. Yockey, L.J., Demehri, S., Turkoz, M., Turkoz, A., Ahern, P.P., Jassim, O., et al. The absence of a microbiota enhances TSLP expression in mice with defective skin barrier but does not affect the severity of their allergic inflammation. J Invest Dermatol 133 (2013), 2714–2721.
52. Yokote, H., Miyake, S., Croxford, J.L., Oki, S., Mizusawa, H., Yamamura, T., NKT cell-dependent amelioration of a mouse model of multiple sclerosis by altering gut flora. Am J Pathol 173 (2008), 1714–1723.
53. Yurkovetskiy, L.A., Pickard, J.M., Chervonsky, A.V., Microbiota and autoimmunity: exploring new avenues. Cell Host Microbe 17 (2015), 548–552.
54. Zanvit, P., Konkel, J.E., Jiao, X., Kasagi, S., Zhang, D., Wu, R., et al. Antibiotics in neonatal life increase murine susceptibility to experimental psoriasis. Nat Commun, 6, 2015, 8424.
55. Zhang, J., Kobert, K., Flouri, T., Stamatakis, A., PEAR: a fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics 30 (2014), 614–620.