Intestinal microbiota of mice influences resistance to Staphylococcus aureus pneumonia

Infection and Immunity

Volumn 83, Issue 10, 2015, Pages 4003-4014

  Gauguet, Stefanie ^a,b   D'Ortona, Samantha ^a   Ahnger Pier, Kathryn ^a   Duan, Biyan ^a   Surana, Neeraj K ^b   Lu, Roger ^a   Cywes Bentley, Colette ^a   Gadjeva, Mihaela ^a   Shan, Qiang ^a   Priebe, Gregory P ^a,b   Pier, Gerald B ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD3 ANTIGEN; INTERLEUKIN 17; INTERLEUKIN 22; INTERLEUKIN 6; T LYMPHOCYTE RECEPTOR BETA CHAIN; INTERLEUKIN DERIVATIVE; INTERLEUKIN-22;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL COUNT; BACTERIAL LOAD; BACTERIUM; CONTROLLED STUDY; INFECTION RESISTANCE; INFECTION SENSITIVITY; INTESTINE FLORA; LUNG LAVAGE; LYMPHOID CELL; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; SEGMENTED FILAMENTOUS BACTERIA; STAPHYLOCOCCAL PNEUMONIA; TH17 CELL; TH22 CELL; ANIMAL; C57BL MOUSE; FEMALE; HUMAN; IMMUNOLOGY; INTESTINE; LUNG; MALE; MICROBIOLOGY; PHYSIOLOGY; STAPHYLOCOCCUS AUREUS;

ANIMALS; FEMALE; GASTROINTESTINAL MICROBIOME; HUMANS; INTERLEUKINS; INTESTINES; LUNG; MALE; MICE; MICE, INBRED C57BL; PNEUMONIA, STAPHYLOCOCCAL; STAPHYLOCOCCUS AUREUS;

EID: 84944472849     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00037-15     Document Type: Article

References (47)

1. Dantes R, Mu Y, Belflower R, Aragon D, Dumyati G, Harrison LH, Lessa FC, Lynfield R, Nadle J, Petit S, Ray SM, Schaffner W, Townes J, Fridkin S, Emerging Infections Program-Active Bacterial Core Surveillance MRSA Surveillance Investigators. 2013. National burden of invasive methicillin-resistant Staphylococcus aureus infections, United States, 2011. JAMA Intern Med 173:1970-1978. http://dx.doi.org/10.1001/jamainternmed.2013.10423.
2. Rubinstein E, Kollef MH, Nathwani D. 2008. Pneumonia caused by methicillin-resistant Staphylococcus aureus. Clin Infect Dis 46(Suppl 5):S378-S385. http://dx.doi.org/10.1086/533594.
3. Vardakas KZ, Matthaiou DK, Falagas ME. 2009. Incidence, characteristics and outcomes of patients with severe community acquired- MRSA pneumonia. Eur Respir J 34:1148-1158. http://dx.doi.org/10.1183/09031936.00041009.
4. Klevens RM, Morrison MA, Nadle J, Petit S, Gershman K, Ray S, Harrison LH, Lynfield R, Dumyati G, Townes JM, Craig AS, Zell ER, Fosheim GE, McDougal LK, Carey RB, Fridkin SK, Active Bacterial Core Surveillance MRSA Investigators. 2007. Invasive methicillinresistant Staphylococcus aureus infections in the United States. JAMA 298:1763-1771. http://dx.doi.org/10.1001/jama.298.15.1763.
5. Tsai HC, Velichko S, Hung LY, Wu R. 2013. IL-17A and Th17 cells in lung inflammation: an update on the role of Th17 cell differentiation and IL-17R signaling in host defense against infection. Clin Dev Immunol 2013:267971. http://dx.doi.org/10.1155/2013/267971.
6. de Beaucoudrey L, Puel A, Filipe-Santos O, Cobat A, Ghandil P, Chrabieh M, Feinberg J, von Bernuth H, Samarina A, Janniere L, Fieschi C, Stephan JL, Boileau C, Lyonnet S, Jondeau G, Cormier-Daire V, Le Merrer M, Hoarau C, Lebranchu Y, Lortholary O, Chandesris MO, Tron F, Gambineri E, Bianchi L, Rodriguez-Gallego C, Zitnik SE, Vasconcelos J, Guedes M, Vitor AB, Marodi L, Chapel H, Reid B, Roifman C, Nadal D, Reichenbach J, Caragol I, Garty BZ, Dogu F, Camcioglu Y, Gulle S, Sanal O, Fischer A, Abel L, Stockinger B, Picard C, Casanova JL. 2008. Mutations in STAT3 and IL12RB1 impair the development of human IL-17-producing T cells. J Exp Med 205:1543-1550. http://dx.doi.org/10.1084/jem.20080321.
7. Minegishi Y, Saito M, Nagasawa M, Takada H, Hara T, Tsuchiya S, Agematsu K, Yamada M, Kawamura N, Ariga T, Tsuge I, Karasuyama H. 2009. Molecular explanation for the contradiction between systemic Th17 defect and localized bacterial infection in hyper-IgE syndrome. J Exp Med 206:1291-1301. http://dx.doi.org/10.1084/jem.20082767.
8. Aujla SJ, Chan YR, Zheng M, Fei M, Askew DJ, Pociask DA, Reinhart TA, McAllister F, Edeal J, Gaus K, Husain S, Kreindler JL, Dubin PJ, Pilewski JM, Myerburg MM, Mason CA, Iwakura Y, Kolls JK. 2008. IL-22 mediates mucosal host defense against Gram-negative bacterial pneumonia. Nat Med 14:275-281. http://dx.doi.org/10.1038/nm1710.
9. Choi SM, McAleer JP, Zheng M, Pociask DA, Kaplan MH, Qin S, Reinhart TA, Kolls JK. 2013. Innate Stat3-mediated induction of the antimicrobial protein Reg3gamma is required for host defense against MRSA pneumonia. J Exp Med 210:551-561. http://dx.doi.org/10.1084/jem.20120260.
10. Kudva A, Scheller EV, Robinson KM, Crowe CR, Choi SM, Slight SR, Khader SA, Dubin PJ, Enelow RI, Kolls JK, Alcorn JF. 2011. Influenza A inhibits Th17-mediated host defense against bacterial pneumonia in mice. J Immunol 186:1666-1674. http://dx.doi.org/10.4049/jimmunol.1002194.
11. Robinson KM, McHugh KJ, Mandalapu S, Clay ME, Lee B, Scheller EV, Enelow RI, Chan YR, Kolls JK, Alcorn JF. 2014. Influenza A virus exacerbates Staphylococcus aureus pneumonia in mice by attenuating antimicrobial peptide production. J Infect Dis 209:865-875. http://dx.doi.org/10.1093/infdis/jit527.
12. Priebe GP, Walsh RL, Cederroth TA, Kamei A, Coutinho-Sledge YS, Goldberg JB, Pier GB. 2008. IL-17 is a critical component of vaccineinduced protection against lung infection by lipopolysaccharideheterologous strains of Pseudomonas aeruginosa. J Immunol 181:4965-4975. http://dx.doi.org/10.4049/jimmunol.181.7.4965.
13. Gopal R, Rangel-Moreno J, Slight S, Lin Y, Nawar HF, Fallert Junecko BA, Reinhart TA, Kolls J, Randall TD, Connell TD, Khader SA. 2013. Interleukin-17-dependent CXCL13 mediates mucosal vaccine-induced immunity against tuberculosis. Mucosal Immunol 6:972-984. http://dx.doi.org/10.1038/mi.2012.135.
14. Wu W, Huang J, Duan B, Traficante DC, Hong H, Risech M, Lory S, Priebe GP. 2012. Th17-stimulating protein vaccines confer protection against Pseudomonas aeruginosa pneumonia. Am J Respir Crit Care Med 186:420-427. http://dx.doi.org/10.1164/rccm.201202-0182OC.
15. Chewning JH, Weaver CT. 2014. Development and survival of Th17 cells within the intestines: the influence of microbiome- and diet-derived signals. J Immunol 193:4769-4777. http://dx.doi.org/10.4049/jimmunol.1401835.
16. Clarke TB. 2014. Early innate immunity to bacterial infection in the lung is regulated systemically by the commensal microbiota via Nod-like receptor ligands. Infect Immun 82:4596-4606. http://dx.doi.org/10.1128/IAI.02212-14.
17. Ivanov II, Atarashi K, Manel N, Brodie EL, Shima T, Karaoz U, Wei D, Goldfarb KC, Santee CA, Lynch SV, Tanoue T, Imaoka A, Itoh K, Takeda K, Umesaki Y, Honda K, Littman DR. 2009. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139:485-498. http://dx.doi.org/10.1016/j.cell.2009.09.033.
18. Ivanov II, Frutos RL, Manel N, Yoshinaga K, Rifkin DB, Sartor RB, Finlay BB, Littman DR. 2008. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 4:337-349. http://dx.doi.org/10.1016/j.chom.2008.09.009.
19. Ivanov II, Littman DR. 2010. Segmented filamentous bacteria take the stage. Mucosal Immunol 3:209-212. http://dx.doi.org/10.1038/mi.2010.3.
20. Cooke KR, Hill GR, Gerbitz A, Kobzik L, Martin TR, Crawford JM, Brewer JP, Ferrara JL. 2000. Hyporesponsiveness of donor cells to lipopolysaccharide stimulation reduces the severity of experimental idiopathic pneumonia syndrome: potential role for a gut-lung axis of inflammation. J Immunol 165:6612-6619. http://dx.doi.org/10.4049/jimmunol.165.11.6612.
21. Chen LW, Chen PH, Hsu CM. 2011. Commensal microflora contribute to host defense against Escherichia coli pneumonia through Toll-like receptors. Shock 36:67-75. http://dx.doi.org/10.1097/SHK.0b013e3182184ee7.
22. Fox AC, McConnell KW, Yoseph BP, Breed E, Liang Z, Clark AT, O'Donnell D, Zee-Cheng B, Jung E, Dominguez JA, Dunne WM, Burd EM, Coopersmith CM. 2012. The endogenous bacteria alter gut epithelial apoptosis and decrease mortality following Pseudomonas aeruginosa pneumonia. Shock 38:508-514. http://dx.doi.org/10.1097/SHK.0b013e31826e47e8.
23. Umesaki Y, Okada Y, Matsumoto S, Imaoka A, Setoyama H. 1995. Segmented filamentous bacteria are indigenous intestinal bacteria that activate intraepithelial lymphocytes and induce MHC class II molecules and fucosyl asialoGM1glycolipids on the small intestinal epithelial cells in the ex-germ-free mouse. Microbiol Immunol 39:555-562. http://dx.doi.org/10.1111/j.1348-0421.1995.tb02242.x.
24. Li L, Shi QG, Lin F, Liang YG, Sun LJ, Mu JS, Wang YG, Su HB, Xu B, Ji CC, Huang HH, Li K, Wang HF. 2014. Cytokine IL-6 is required in Citrobacter rodentium infection-induced intestinal Th17 responses and promotes IL-22 expression in inflammatory bowel disease. Mol Med Rep 9:831-836. http://dx.doi.org/10.3892/mmr.2014.1898.
25. Ye P, Rodriguez FH, Kanaly S, Stocking KL, Schurr J, Schwarzenberger P, Oliver P, Huang W, Zhang P, Zhang J, Shellito JE, Bagby GJ, Nelson S, Charrier K, Peschon JJ, Kolls JK. 2001. Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colonystimulating factor expression, neutrophil recruitment, and host defense. J Exp Med 194:519-527. http://dx.doi.org/10.1084/jem.194.4.519.
26. Cheng P, Liu T, Zhou WY, Zhuang Y, Peng LS, Zhang JY, Yin ZN, Mao XH, Guo G, Shi Y, Zou QM. 2012. Role of gamma-delta T cells in host response against Staphylococcus aureus-induced pneumonia. BMC Immunol 13:38. http://dx.doi.org/10.1186/1471-2172-13-38.
27. Simon MM, Greenaway S, White JK, Fuchs H, Gailus-Durner V, Wells S, Sorg T, Wong K, Bedu E, Cartwright EJ, Dacquin R, Djebali S, Estabel J, Graw J, Ingham NJ, Jackson IJ, Lengeling A, Mandillo S, Marvel J, Meziane H, Preitner F, Puk O, Roux M, Adams DJ, Atkins S, Ayadi A, Becker L, Blake A, Brooker D, Cater H, Champy MF, Combe R, Danecek P, di Fenza A, Gates H, Gerdin AK, Golini E, Hancock JM, Hans W, Holter SM, Hough T, Jurdic P, Keane TM, Morgan H, Muller W, NeffF, Nicholson G, Pasche B, Roberson LA, Rozman J, Sanderson M, Santos L, Selloum M, Shannon C, Southwell A, Tocchini-Valentini GP, Vancollie VE, Westerberg H, Wurst W, Zi M, Yalcin B, Ramirez- Solis R, Steel KP, Mallon AM, de Angelis MH, Herault Y, Brown SD. 2013. A comparative phenotypic and genomic analysis of C57BL/6J and C57BL/6N mouse strains. Genome Biol 14:R82. http://dx.doi.org/10.1186/gb-2013-14-7-r82.
28. Fagundes CT, Amaral FA, Vieira AT, Soares AC, Pinho V, Nicoli JR, Vieira LQ, Teixeira MM, Souza DG. 2012. Transient TLR activation restores inflammatory response and ability to control pulmonary bacterial infection in germfree mice. J Immunol 188:1411-1420. http://dx.doi.org/10.4049/jimmunol.1101682.
29. Wu S, Jiang ZY, Sun YF, Yu B, Chen J, Dai CQ, Wu XL, Tang XL, Chen XY. 2013. Microbiota regulates the TLR7 signaling pathway against respiratory tract influenza A virus infection. Curr Microbiol 67:414-422. http://dx.doi.org/10.1007/s00284-013-0380-z.
30. Ichinohe T, Pang IK, Kumamoto Y, Peaper DR, Ho JH, Murray TS, Iwasaki A. 2011. Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc Natl Acad Sci U S A 108:5354-5359. http://dx.doi.org/10.1073/pnas.1019378108.
31. Cheng M, Qian L, Shen G, Bian G, Xu T, Xu W, Shen G, Hu S. 2014. Microbiota modulate tumoral immune surveillance in lung through a gammadeltaT17 immune cell-dependent mechanism. Cancer Res 74:4030-4041. http://dx.doi.org/10.1158/0008-5472.CAN-13-2462.
32. Liu J, Feng Y, Yang K, Li Q, Ye L, Han L, Wan H. 2011. Early production of IL-17 protects against acute pulmonary Pseudomonas aeruginosa infection in mice. FEMS Immunol Med Microbiol 61:179-188. http://dx.doi.org/10.1111/j.1574-695X.2010.00764.x.
33. Wolf K, Plano GV, Fields KA. 2009. A protein secreted by the respiratory pathogen Chlamydia pneumoniae impairs IL-17 signalling via interaction with human Act1. Cell Microbiol 11:769-779. http://dx.doi.org/10.1111/j.1462-5822.2009.01290.x.
34. Zhou X, Chen Q, Moore J, Kolls JK, Halperin S, Wang J. 2009. Critical role of the interleukin-17/interleukin-17 receptor axis in regulating host susceptibility to respiratory infection with Chlamydia species. Infect Immun 77:5059-5070. http://dx.doi.org/10.1128/IAI.00403-09.
35. Wu Q, Martin RJ, Rino JG, Breed R, Torres RM, Chu HW. 2007. IL-23-dependent IL-17 production is essential in neutrophil recruitment and activity in mouse lung defense against respiratory Mycoplasma pneumoniae infection. Microbes Infect 9:78-86. http://dx.doi.org/10.1016/j.micinf.2006.10.012.
36. Lockhart E, Green AM, Flynn JL. 2006. IL-17 production is dominated by gammadelta T cells rather than CD4 T cells during Mycobacterium tuberculosis infection. J Immunol 177:4662-4669. http://dx.doi.org/10.4049/jimmunol.177.7.4662.
37. Frank KM, Zhou T, Moreno-Vinasco L, Hollett B, Garcia JG, Bubeck Wardenburg J. 2012. Host response signature to Staphylococcus aureus alpha-hemolysin implicates pulmonary Th17 response. Infect Immun 80:3161-3169. http://dx.doi.org/10.1128/IAI.00191-12.
38. Zenewicz LA, Flavell RA. 2011. Recent advances in IL-22 biology. Int Immunol 23:159-163. http://dx.doi.org/10.1093/intimm/dxr001.
39. Raffatellu M, George MD, Akiyama Y, Hornsby MJ, Nuccio SP, Paixao TA, Butler BP, Chu H, Santos RL, Berger T, Mak TW, Tsolis RM, Bevins CL, Solnick JV, Dandekar S, Baumler AJ. 2009. Lipocalin-2 resistance confers an advantage to Salmonella enterica serotype Typhimurium for growth and survival in the inflamed intestine. Cell Host Microbe 5:476-486. http://dx.doi.org/10.1016/j.chom.2009.03.011.
40. Wolk K, Kunz S, Witte E, Friedrich M, Asadullah K, Sabat R. 2004. IL-22 increases the innate immunity of tissues. Immunity 21:241-254. http://dx.doi.org/10.1016/j.immuni.2004.07.007.
41. Zheng Y, Valdez PA, Danilenko DM, Hu Y, Sa SM, Gong Q, Abbas AR, Modrusan Z, Ghilardi N, de Sauvage FJ, Ouyang W. 2008. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat Med 14:282-289. http://dx.doi.org/10.1038/nm1720.
42. Simonian PL, Wehrmann F, Roark CL, Born WK, O'Brien RL, Fontenot AP. 2010. Gammadelta T cells protect against lung fibrosis via IL-22. J Exp Med 207:2239-2253. http://dx.doi.org/10.1084/jem.20100061.
43. Eyerich S, Eyerich K, Pennino D, Carbone T, Nasorri F, Pallotta S, Cianfarani F, Odorisio T, Traidl-Hoffmann C, Behrendt H, Durham SR, Schmidt-Weber CB, Cavani A. 2009. Th22 cells represent a distinct human T cell subset involved in epidermal immunity and remodeling. J Clin Invest 119:3573-3585. http://dx.doi.org/10.1172/JCI40202.
44. Van Maele L, Carnoy C, Cayet D, Ivanov S, Porte R, Deruy E, Chabalgoity JA, Renauld JC, Eberl G, Benecke AG, Trottein F, Faveeuw C, Sirard JC. 2014. Activation of type 3 innate lymphoid cells and interleukin 22 secretion in the lungs during Streptococcus pneumoniae infection. J Infect Dis 210:493-503. http://dx.doi.org/10.1093/infdis/jiu106.
45. Zielinski CE, Mele F, Aschenbrenner D, Jarrossay D, Ronchi F, Gattorno M, Monticelli S, Lanzavecchia A, Sallusto F. 2012. Pathogen- induced human TH17 cells produce IFN-gamma or IL-10 and are regulated by IL-1beta. Nature 484:514-518. http://dx.doi.org/10.1038/nature10957.
46. Camporeale A, Poli V. 2012. IL-6, IL-17 and STAT3: a holy trinity in auto-immunity? Front Biosci 17:2306-2326. http://dx.doi.org/10.2741/4054.
47. van der Poll T, Keogh CV, Guirao X, Buurman WA, Kopf M, Lowry SF. 1997. Interleukin-6 gene-deficient mice show impaired defense against pneumococcal pneumonia. J Infect Dis 176:439-444. http://dx.doi.org/10.1086/514062.