User menu

Accès à distance ? S'identifier sur le proxy UCLouvain

Interleukin-22 regulates antimicrobial peptide expression and keratinocyte differentiation to control Staphylococcus aureus colonization of the nasal mucosa.

Primary tabs

download
  • Open access
  • PDF
  • 1.41 M
Mulcahy, M E Leech, J M Renauld, Jean-Christophe [UCL] Mills, K Hg McLoughlin, R M

The local immune response occurring during Staphylococcus aureus nasal colonization remains ill-defined. Studies have highlighted the importance of T-cell immunity in controlling S. aureus colonization of the nasal mucosa. We extend these observations, identifying a critical role for interleukin (IL)-22 in this process. IL-22 is basally expressed within the nasal mucosa and is induced upon S. aureus colonization. IL-22 is produced by CD4+ and CD8+ T lymphocytes at this site, with innate-like lymphocytes also contributing. IL-22(-/-) mice demonstrate significantly elevated levels of S. aureus nasal colonization as compared with wild-type (WT) mice. This was associated with reduced expression of antimicrobial peptides (AMPs) in the nose. Furthermore, expression of staphylococcal ligands loricrin and cytokeratin 10 was higher in the noses of IL-22(-/-) as compared with WT mice. IL-17 has been shown to regulate S. aureus nasal colonization by controlling local neutrophil responses; however, IL-17 expression and neutrophil responses were comparable in the noses of IL-22(-/-) and WT mice during S. aureus colonization. We conclude that IL-22 has an important role in controlling S. aureus nasal colonization through distinct mechanisms, with IL-22 mediating its effect exclusively by inducing AMP expression and controlling availability of staphylococcal ligands.

Document type Article de périodique (Journal article) – Article de recherche
Access type Accès libre
Publication date 2016
Language Anglais
Journal information "Mucosal Immunology" - Vol. 9, no.6, p. 1429-1441 (2016)
Peer reviewed yes
Publisher Nature Publishing Group (New York)
issn 1933-0219
e-issn 1935-3456
Publication status Publié
Affiliation UCL - SSS/DDUV - Institut de Duve
Links
  1. van Belkum Alex, Verkaik Nelianne J., de Vogel Corné P., Boelens Hélène A., Verveer Jeroen, Nouwen Jan L., Verbrugh Henri A., Wertheim Heiman F. L., Reclassification ofStaphylococcus aureusNasal Carriage Types, 10.1086/599119
  2. Mermel L. A., Cartony J. M., Covington P., Maxey G., Morse D., Methicillin-Resistant Staphylococcus aureus Colonization at Different Body Sites: a Prospective, Quantitative Analysis, 10.1128/jcm.02601-10
  3. Wertheim Heiman FL, Vos Margreet C, Ott Alewijn, van Belkum Alex, Voss Andreas, Kluytmans Jan AJW, van Keulen Peter HJ, Vandenbroucke-Grauls Christina MJE, Meester Marlene HM, Verbrugh Henri A, Risk and outcome of nosocomial Staphylococcus aureus bacteraemia in nasal carriers versus non-carriers, 10.1016/s0140-6736(04)16897-9
  4. Cookson B. D., Mupirocin resistance in staphylococci, 10.1093/jac/25.4.497
  5. Baur Stefanie, Rautenberg Maren, Faulstich Manuela, Grau Timo, Severin Yannik, Unger Clemens, Hoffmann Wolfgang H., Rudel Thomas, Autenrieth Ingo B., Weidenmaier Christopher, A Nasal Epithelial Receptor for Staphylococcus aureus WTA Governs Adhesion to Epithelial Cells and Modulates Nasal Colonization, 10.1371/journal.ppat.1004089
  6. Mulcahy Michelle E., Geoghegan Joan A., Monk Ian R., O'Keeffe Kate M., Walsh Evelyn J., Foster Timothy J., McLoughlin Rachel M., Nasal Colonisation by Staphylococcus aureus Depends upon Clumping Factor B Binding to the Squamous Epithelial Cell Envelope Protein Loricrin, 10.1371/journal.ppat.1003092
  7. Cole A. M., Tahk S., Oren A., Yoshioka D., Kim Y.-H., Park A., Ganz T., Determinants of Staphylococcusaureus Nasal Carriage, 10.1128/cdli.8.6.1064-1069.2001
  8. Nakamura M. M., McAdam A. J., Sandora T. J., Moreira K. R., Lee G. M., Higher Prevalence of Pharyngeal than Nasal Staphylococcus aureus Carriage in Pediatric Intensive Care Units, 10.1128/jcm.00547-10
  9. Emonts Marieke, Uitterlinden André G., Nouwen Jan L., Kardys Isabella, Maat Moniek P. M. de, Melles Damian C., Witteman Jacqueline, Jong Paulus T. V. M. de, Verbrugh Henri A., Hofman Albert, Hermans Peter W. M., Belkum Alex van, Host Polymorphisms in Interleukin 4, Complement Factor H, and C‐Reactive Protein Associated with Nasal Carriage ofStaphylococcus aureusand Occurrence of Boils, 10.1086/533501
  10. Nurjadi Dennis, Herrmann Elena, Hinderberger Isabel, Zanger Philipp, Impaired β-Defensin Expression in Human Skin Links DEFB1 Promoter Polymorphisms With Persistent Staphylococcus aureus Nasal Carriage, 10.1093/infdis/jis735
  11. van Belkum Alex, Emonts Marieke, Wertheim Heiman, de Jongh Christa, Nouwen Jan, Bartels Hans, Cole Alexander, Cole Amy, Hermans Peter, Boelens Hélène, Toom Nicole Lemmens-den, Snijders Susan, Verbrugh Henri, van Leeuwen Willem, The role of human innate immune factors in nasal colonization by Staphylococcus aureus, 10.1016/j.micinf.2007.08.003
  12. Zanger P., Nurjadi D., Vath B., Kremsner P. G., Persistent Nasal Carriage of Staphylococcus aureus Is Associated with Deficient Induction of Human  -Defensin 3 after Sterile Wounding of Healthy Skin In Vivo, 10.1128/iai.00101-11
  13. Verkaik N.J., Lebon A., de Vogel C.P., Hooijkaas H., Verbrugh H.A., Jaddoe V.W.V., Hofman A., Moll H.A., van Belkum A., van Wamel W.J.B., Induction of antibodies by Staphylococcus aureus nasal colonization in young children, 10.1111/j.1469-0691.2009.03073.x
  14. Padoveze Maria Clara, de Jesus Pedro Rogério, Blum-Menezes Dulcinéa, Bratfich Orlando José, Moretti Maria Luiza, Staphylococcus aureus nasal colonization in HIV outpatients: Persistent or transient?, 10.1016/j.ajic.2007.05.012
  15. Archer N. K., Harro J. M., Shirtliff M. E., Clearance of Staphylococcus aureus Nasal Carriage Is T Cell Dependent and Mediated through Interleukin-17A Expression and Neutrophil Influx, 10.1128/iai.00084-13
  16. Zheng Yan, Valdez Patricia A, Danilenko Dimitry M, Hu Yan, Sa Susan M, Gong Qian, Abbas Alexander R, Modrusan Zora, Ghilardi Nico, de Sauvage Frederic J, Ouyang Wenjun, Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens, 10.1038/nm1720
  17. Sonnenberg Gregory F, Fouser Lynette A, Artis David, Border patrol: regulation of immunity, inflammation and tissue homeostasis at barrier surfaces by IL-22, 10.1038/ni.2025
  18. Liang Spencer C., Tan Xiang-Yang, Luxenberg Deborah P., Karim Riyez, Dunussi-Joannopoulos Kyriaki, Collins Mary, Fouser Lynette A., Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides, 10.1084/jem.20061308
  19. Aujla Shean J, Chan Yvonne R, Zheng Mingquan, Fei Mingjian, Askew David J, Pociask Derek A, Reinhart Todd A, McAllister Florencia, Edeal Jennifer, Gaus Kristi, Husain Shahid, Kreindler James L, Dubin Patricia J, Pilewski Joseph M, Myerburg Mike M, Mason Carol A, Iwakura Yoichiro, Kolls Jay K, IL-22 mediates mucosal host defense against Gram-negative bacterial pneumonia, 10.1038/nm1710
  20. Wolk Kerstin, Kunz Stefanie, Witte Ellen, Friedrich Markus, Asadullah Khusru, Sabat Robert, IL-22 Increases the Innate Immunity of Tissues, 10.1016/j.immuni.2004.07.007
  21. Boniface K., Bernard F.-X., Garcia M., Gurney A. L., Lecron J.-C., Morel F., IL-22 Inhibits Epidermal Differentiation and Induces Proinflammatory Gene Expression and Migration of Human Keratinocytes, 10.4049/jimmunol.174.6.3695
  22. Wolk Kerstin, Witte Ellen, Wallace Elizabeth, Döcke Wolf-Dietrich, Kunz Stefanie, Asadullah Khusru, Volk Hans-Dieter, Sterry Wolfram, Sabat Robert, IL-22 regulates the expression of genes responsible for antimicrobial defense, cellular differentiation, and mobility in keratinocytes: a potential role in psoriasis, 10.1002/eji.200535503
  23. Ahlfors Helena, Morrison Peter J., Duarte João H., Li Ying, Biro Judit, Tolaini Mauro, Di Meglio Paola, Potocnik Alexandre J., Stockinger Brigitta, IL-22 Fate Reporter Reveals Origin and Control of IL-22 Production in Homeostasis and Infection, 10.4049/jimmunol.1401244
  24. Duhen Thomas, Geiger Rebekka, Jarrossay David, Lanzavecchia Antonio, Sallusto Federica, Production of interleukin 22 but not interleukin 17 by a subset of human skin-homing memory T cells, 10.1038/ni.1767
  25. Nomura Takashi, Kabashima Kenji, Miyachi Yoshiki, The panoply of αβT cells in the skin, 10.1016/j.jdermsci.2014.07.010
  26. Cella Marina, Fuchs Anja, Vermi William, Facchetti Fabio, Otero Karel, Lennerz Jochen K. M., Doherty Jason M., Mills Jason C., Colonna Marco, A human natural killer cell subset provides an innate source of IL-22 for mucosal immunity, 10.1038/nature07537
  27. Satoh-Takayama Naoko, Vosshenrich Christian A.J., Lesjean-Pottier Sarah, Sawa Shinichiro, Lochner Matthias, Rattis Frederique, Mention Jean-Jacques, Thiam Kader, Cerf-Bensussan Nadine, Mandelboim Ofer, Eberl Gerard, Di Santo James P., Microbial Flora Drives Interleukin 22 Production in Intestinal NKp46+ Cells that Provide Innate Mucosal Immune Defense, 10.1016/j.immuni.2008.11.001
  28. Van Maele Laurye, Carnoy Christophe, Cayet Delphine, Ivanov Stoyan, Porte Rémi, Deruy Emeric, Chabalgoity José A., Renauld Jean-Christophe, Eberl Gérard, Benecke Arndt G., Trottein François, Faveeuw Christelle, Sirard Jean-Claude, Activation of Type 3 Innate Lymphoid Cells and Interleukin 22 Secretion in the Lungs During Streptococcus pneumoniae Infection, 10.1093/infdis/jiu106
  29. Simonian Philip L., Wehrmann Fabian, Roark Christina L., Born Willi K., O'Brien Rebecca L., Fontenot Andrew P., γδ T cells protect against lung fibrosis via IL-22, 10.1084/jem.20100061
  30. Mielke Lisa A., Jones Sarah A., Raverdeau Mathilde, Higgs Rowan, Stefanska Anna, Groom Joanna R., Misiak Alicja, Dungan Lara S., Sutton Caroline E., Streubel Gundula, Bracken Adrian P., Mills Kingston H.G., Retinoic acid expression associates with enhanced IL-22 production by γδ T cells and innate lymphoid cells and attenuation of intestinal inflammation, 10.1084/jem.20121588
  31. de Repentigny Louis, Goupil Mathieu, Jolicoeur Paul, Oropharyngeal Candidiasis in HIV Infection: Analysis of Impaired Mucosal Immune Response to Candida albicans in Mice Expressing the HIV-1 Transgene, 10.3390/pathogens4020406
  32. Gauguet Stefanie, D'Ortona Samantha, Ahnger-Pier Kathryn, Duan Biyan, Surana Neeraj K., Lu Roger, Cywes-Bentley Colette, Gadjeva Mihaela, Shan Qiang, Priebe Gregory P., Pier Gerald B., Intestinal Microbiota of Mice Influences Resistance to Staphylococcus aureus Pneumonia, 10.1128/iai.00037-15
  33. Ivanov Ivaylo I., Frutos Rosa de Llanos, Manel Nicolas, Yoshinaga Keiji, Rifkin Daniel B., Sartor R. Balfour, Finlay B. Brett, Littman Dan R., Specific Microbiota Direct the Differentiation of IL-17-Producing T-Helper Cells in the Mucosa of the Small Intestine, 10.1016/j.chom.2008.09.009
  34. Sanos Stephanie L, Bui Viet L, Mortha Arthur, Oberle Karin, Heners Charlotte, Johner Caroline, Diefenbach Andreas, RORγt and commensal microflora are required for the differentiation of mucosal interleukin 22–producing NKp46+ cells, 10.1038/ni.1684
  35. Cho M.-L., Kang J.-W., Moon Y.-M., Nam H.-J., Jhun J.-Y., Heo S.-B., Jin H.-T., Min S.-Y., Ju J.-H., Park K.-S., Cho Y.-G., Yoon C.-H., Park S.-H., Sung Y.-C., Kim H.-Y., STAT3 and NF- B Signal Pathway Is Required for IL-23-Mediated IL-17 Production in Spontaneous Arthritis Animal Model IL-1 Receptor Antagonist-Deficient Mice, 10.4049/jimmunol.176.9.5652
  36. Maher Belinda M., Mulcahy Michelle E., Murphy Alison G., Wilk Mieszko, O'Keeffe Kate M., Geoghegan Joan A., Lavelle Ed C., McLoughlin Rachel M., Nlrp-3-Driven Interleukin 17 Production by γδT Cells Controls Infection Outcomes during Staphylococcus aureus Surgical Site Infection, 10.1128/iai.01026-13
  37. O'Brien Louise M., Walsh Evelyn J., Massey Ruth C., Peacock Sharon J., Foster Timothy J., Staphylococcus aureusclumping factor B (ClfB) promotes adherence to human type I cytokeratin 10: implications for nasal colonization, 10.1046/j.1462-5822.2002.00231.x
  38. Zhang Z., J. Clin. Invest., 119, 1899 (2009)
  39. Nograles Kristine E., Zaba Lisa C., Shemer Avner, Fuentes-Duculan Judilyn, Cardinale Irma, Kikuchi Toyoko, Ramon Michal, Bergman Reuven, Krueger James G., Guttman-Yassky Emma, IL-22–producing “T22” T cells account for upregulated IL-22 in atopic dermatitis despite reduced IL-17–producing TH17 T cells, 10.1016/j.jaci.2009.03.041
  40. Ishigame Harumichi, Kakuta Shigeru, Nagai Takeshi, Kadoki Motohiko, Nambu Aya, Komiyama Yutaka, Fujikado Noriyuki, Tanahashi Yuko, Akitsu Aoi, Kotaki Hayato, Sudo Katsuko, Nakae Susumu, Sasakawa Chihiro, Iwakura Yoichiro, Differential Roles of Interleukin-17A and -17F in Host Defense against Mucoepithelial Bacterial Infection and Allergic Responses, 10.1016/j.immuni.2008.11.009
  41. Midorikawa K., Ouhara K., Komatsuzawa H., Kawai T., Yamada S., Fujiwara T., Yamazaki K., Sayama K., Taubman M. A., Kurihara H., Hashimoto K., Sugai M., Staphylococcus aureus Susceptibility to Innate Antimicrobial Peptides,  -Defensins and CAP18, Expressed by Human Keratinocytes, 10.1128/iai.71.7.3730-3739.2003
  42. Cash H. L., Symbiotic Bacteria Direct Expression of an Intestinal Bactericidal Lectin, 10.1126/science.1127119
  43. Sestito R., Madonna S., Scarponi C., Cianfarani F., Failla C. M., Cavani A., Girolomoni G., Albanesi C., STAT3-dependent effects of IL-22 in human keratinocytes are counterregulated by sirtuin 1 through a direct inhibition of STAT3 acetylation, 10.1096/fj.10-172288
  44. Choi Sun-Mi, McAleer Jeremy P., Zheng Mingquan, Pociask Derek A., Kaplan Mark H., Qin Shulin, Reinhart Todd A., Kolls Jay K., Innate Stat3-mediated induction of the antimicrobial protein Reg3γ is required for host defense against MRSA pneumonia, 10.1084/jem.20120260
  45. Son Eui Dong, Kim Hyoung-June, Park Taehun, Shin Kyeho, Bae Il-Hong, Lim Kyung-Min, Cho Eun-Gyung, Lee Tae Ryong, Staphylococcus aureus inhibits terminal differentiation of normal human keratinocytes by stimulating interleukin-6 secretion, 10.1016/j.jdermsci.2013.12.004
  46. Nograles K.E., Br. J. Dermatol., 159, 1092 (2008)
  47. Wolk K., Warszawska K., Hoeflich C., Witte E., Schneider-Burrus S., Witte K., Kunz S., Buss A., Roewert H. J., Krause M., Lukowsky A., Volk H.-D., Sterry W., Sabat R., Deficiency of IL-22 Contributes to a Chronic Inflammatory Disease: Pathogenetic Mechanisms in Acne Inversa, 10.4049/jimmunol.0903907
  48. Kreymborg K., Etzensperger R., Dumoutier L., Haak S., Rebollo A., Buch T., Heppner F. L., Renauld J.-C., Becher B., IL-22 Is Expressed by Th17 Cells in an IL-23-Dependent Fashion, but Not Required for the Development of Autoimmune Encephalomyelitis, 10.4049/jimmunol.179.12.8098
  49. Kryczek Ilona, Lin Yanwei, Nagarsheth Nisha, Peng Dongjun, Zhao Lili, Zhao Ende, Vatan Linda, Szeliga Wojciech, Dou Yali, Owens Scott, Zgodzinski Witold, Majewski Marek, Wallner Grzegorz, Fang Jingyuan, Huang Emina, Zou Weiping, IL-22+CD4+ T Cells Promote Colorectal Cancer Stemness via STAT3 Transcription Factor Activation and Induction of the Methyltransferase DOT1L, 10.1016/j.immuni.2014.03.010
  50. Asanuma Hideki, Hodson Thompson Amy, Iwasaki Takuya, Sato Yuko, Inaba Yuji, Aizawa Chikara, Kurata Takeshi, Tamura Shin-ichi, Isolation and characterization of mouse nasal-associated lymphoid tissue, 10.1016/s0022-1759(96)00243-8
Bibliographic reference Mulcahy, M E ; Leech, J M ; Renauld, Jean-Christophe ; Mills, K Hg ; McLoughlin, R M. Interleukin-22 regulates antimicrobial peptide expression and keratinocyte differentiation to control Staphylococcus aureus colonization of the nasal mucosa.. In: Mucosal Immunology, Vol. 9, no.6, p. 1429-1441 (2016)
Permanent URL http://hdl.handle.net/2078.1/184350