Contextual control of skin immunity and inflammation by Corynebacterium

Journal of Experimental Medicine

Volumn 215, Issue 3, 2018, Pages 785-799

  Ridaura, Vanessa K ^a,g   Bouladoux, Nicolas ^a,b   Claesen, Jan ^d,f   Erin Chen, Y ^d   Byrd, Allyson L ^a,c,e   Constantinides, Michael G ^a   Merrill, Eric D ^a   Tamoutounour, Samira ^a   Fischbach, Michael A ^d   Belkaid, Yasmine ^a,b  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^d Stanford University   (United States)

^e BOSTON UNIVERSITY   (United States)

^f LERNER RESEARCH INSTITUTE   (United States)

^g VERILY LIFE SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 17; INTERLEUKIN 23; MYCOLIC ACID; LYMPHOCYTE ANTIGEN RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTATION; ARTICLE; BACTERIAL CELL WALL; CELL PROLIFERATION; CELL SUSPENSION; COCULTURE; COLONY FORMING UNIT; COMPARATIVE STUDY; CONTROLLED STUDY; CORYNEBACTERIUM; CORYNEBACTERIUM ACCOLENS; CORYNEBACTERIUM INFECTION; CYTOKINE PRODUCTION; DENDRITIC CELL; DERMATITIS; DNA EXTRACTION; FLOW CYTOMETRY; GAMMA DELTA T LYMPHOCYTE; GENE EXPRESSION; GENETIC ANALYSIS; HISTOCOMPATIBILITY; HUMAN; HUMAN TISSUE; IMMUNITY; IN VITRO STUDY; IN VIVO STUDY; KERATINOCYTE; LIPID DIET; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PSORIASIS; SKIN; SKIN FLORA; SKINFOLD THICKNESS; STEADY STATE; UPREGULATION; ANIMAL; C57BL MOUSE; CELL MEMBRANE; IMMUNOLOGY; INFLAMMATION; LYMPHOCYTE ACTIVATION; METABOLISM; MICROBIOLOGY; PHYLOGENY; PHYSIOLOGY; T LYMPHOCYTE;

ANIMALS; CELL MEMBRANE; CELL PROLIFERATION; CORYNEBACTERIUM; HUMANS; IMMUNITY; INFLAMMATION; INTERLEUKIN-17; INTERLEUKIN-23; LYMPHOCYTE ACTIVATION; MICE, INBRED C57BL; PHYLOGENY; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; SKIN; T-LYMPHOCYTES;

EID: 85042876586     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20171079     Document Type: Article

References (45)

1. Alekseyenko, A.V., G.I. Perez-Perez, A. De Souza, B. Strober, Z. Gao, M. Bihan, K. Li, B.A. Methé, and M.J. Blaser. 2013. Community differentiation of the cutaneous microbiota in psoriasis. Microbiome. 1:31. https ://doi .org /10 .1186 /2049-2618-1-31
2. Awasthi, A., L. Riol-Blanco, A. Jäger, T. Korn, C. Pot, G. Galileos, E. Bettelli, V.K. Kuchroo, and M. Oukka. 2009. Cutting edge: IL-23 receptor gfp reporter mice reveal distinct populations of IL-17-producing cells. J. Immunol. 182:5904-5908. https ://doi .org /10 .4049 /jimmunol .0900732
3. Barreau, C., F. Bimet, M. Kiredjian, N. Rouillon, and C. Bizet. 1993. Comparative chemotaxonomic studies of mycolic acid-free coryneform bacteria of human origin. J. Clin. Microbiol. 31:2085-2090
4. Belheouane, M., Y. Gupta, S. Künzel, S. Ibrahim, and J.F. Baines. 2017. Improved detection of gene-microbe interactions in the mouse skin microbiota using high-resolution QTL mapping of 16S rRNA transcripts. Microbiome. 5:59. https ://doi .org /10 .1186 /s40168-017-0275-5
5. Belkaid, Y., and J.A. Segre. 2014. Dialogue between skin microbiota and immunity. Science. 346:954-959. https ://doi .org /10 .1126 /science .1260144
6. Bou Raad, R., X. Méniche, C. de Sousa-d'Auria, M. Chami, C. Salmeron, M. Tropis, C. Labarre, M. Daffé, C. Houssin, and N. Bayan. 2010. A deficiency in arabinogalactan biosynthesis affects Corynebacterium glutamicum mycolate outer membrane stability. J. Bacteriol. 192:2691-2700. https :// doi .org /10 .1128 /JB .00009-10
7. Burkovski, A. 2013. Cell envelope of corynebacteria: Structure and influence on pathogenicity. ISRN Microbiol. 2013:935736. https ://doi .org /10 .1155 /2013 /935736
8. Cai, Y., X. Shen, C. Ding, C. Qi, K. Li, X. Li, V.R. Jala, H.G. Zhang, T. Wang, J. Zheng, and J. Yan. 2011. Pivotal role of dermal IL-17-producing d T cells in skin inflammation. Immunity. 35:596-610. https ://doi .org /10 .1016 /j .immuni .2011 .08 .001
9. Conlan, S., L.A. Mijares, J. Becker, R.W. Blakesley, G.G. Bouffard, S. Brooks, H. Coleman, J. Gupta, N. Gurson, M. Park, et al. NISC Comparative Sequencing Program. 2012. Staphylococcus epidermidis pan-genome sequence analysis reveals diversity of skin commensal and hospital infection-associated isolates. Genome Biol. 13:R64. https ://doi .org /10 .1186 /gb-2012-13-7-r64
10. Converse, S.E., and J.S. Cox. 2005. A protein secretion pathway critical for Mycobacterium tuberculosis virulence is conserved and functional in Mycobacterium smegmatis. J. Bacteriol. 187:1238-1245. https ://doi .org /10 .1128 /JB .187 .4 .1238-1245 .2005
11. Dörner, U., B. Schiffler, M.A. Lanéelle, M. Daffé, and R. Benz. 2009. Identification of a cell-wall channel in the corynemycolic acid-free Gram-positive bacterium Corynebacterium amycolatum. Int. Microbiol. 12:29-38
12. Eggeling, L., and M. Bott. 2005. Handbook of Corynebacterium glutamicum. Taylor & Francis, Boca Raton, FL. 616 pp
13. Gande, R., K.J. Gibson, A.K. Brown, K. Krumbach, L.G. Dover, H. Sahm, S. Shioyama, T. Oikawa, G.S. Besra, and L. Eggeling. 2004. Acyl-CoA carboxylases (accD2 and accD3), together with a unique polyketide synthase (Cg-pks), are key to mycolic acid biosynthesis in Corynebacterianeae such as Corynebacterium glutamicum and Mycobacterium tuberculosis. J. Biol. Chem. 279:44847-44857. https :// doi .org /10 .1074 /jbc .M408648200
14. Gao, Z., C.H. Tseng, B.E. Strober, Z. Pei, and M.J. Blaser. 2008. Substantial alterations of the cutaneous bacterial biota in psoriatic lesions. PLoS One. 3:e2719. https ://doi .org /10 .1371 /journal .pone .0002719
15. Gray, E.E., F. Ramírez-Valle, Y. Xu, S. Wu, Z. Wu, K.E. Karjalainen, and J.G. Cyster. 2013. Deficiency in IL-17-committed Vγ4(+) γΔ T cells in a spontaneous Sox13-mutant CD45.1(+) congenic mouse substrain provides protection from dermatitis. Nat. Immunol. 14:584-592. https :// doi .org /10 .1038 /ni .2585
16. Grice, E.A., and J.A. Segre. 2011. The skin microbiome. Nat. Rev. Microbiol. 9:244-253. https ://doi .org /10 .1038 /nrmicro2537
17. Grice, E.A., H.H. Kong, S. Conlan, C.B. Deming, J. Davis, A.C. Young, G.G. Bouffard, R.W. Blakesley, P.R. Murray, E.D. Green, et al. 2009. Topographical and temporal diversity of the human skin microbiome. Science. 324:1190-1192. https ://doi .org /10 .1126 /science .1171700
18. Grice, E.A., E.S. Snitkin, L.J. Yockey, D.M. Bermudez, K.W. Liechty, J.A. Segre; NISC Comparative Sequencing Program. 2010. Longitudinal shift in diabetic wound microbiota correlates with prolonged skin defense response. Proc. Natl. Acad. Sci. USA. 107:14799-14804. https :// doi .org /10 .1073 /pnas .1004204107
19. Ha, H.L., H. Wang, P. Pisitkun, J.C. Kim, I. Tassi, W. Tang, M.I. Morasso, M.C. Udey, and U. Siebenlist. 2014. IL-17 drives psoriatic inflammation via distinct, target cell-specific mechanisms. Proc. Natl. Acad. Sci. USA. 111:E3422-E3431. https ://doi .org /10 .1073 /pnas .1400513111
20. Heilig, J.S., and S. Tonegawa. 1986. Diversity of murine gamma genes and expression in fetal and adult T lymphocytes. Nature. 322:836-840. https ://doi .org /10 .1038 /322836a0
21. Holderness, J., J.F. Hedges, A. Ramstead, and M.A. Jutila. 2013. Comparative biology of γΔ T cell function in humans, mice, and domestic animals. Annu. Rev. Anim. Biosci. 1:99-124. https ://doi .org /10 .1146 /annurev-animal-031412-103639
22. Hsu, Y.M., Y. Zhang, Y. You, D. Wang, H. Li, O. Duramad, X.F. Qin, C. Dong, and X. Lin. 2007. The adaptor protein CARD9 is required for innate immune responses to intracellular pathogens. Nat. Immunol. 8:198-205. https ://doi .org /10 .1038 /ni1426
23. Kobayashi, T., M. Glatz, K. Horiuchi, H. Kawasaki, H. Akiyama, D.H. Kaplan, H.H. Kong, M. Amagai, and K. Nagao. 2015. Dysbiosis and Staphylococcus aureus colonization drives inflammation in atopic dermatitis. Immunity. 42:756-766. https ://doi .org /10 .1016 /j .immuni .2015 .03 .014
24. Korf, J., A. Stoltz, J. Verschoor, P. De Baetselier, and J. Grooten. 2005. The Mycobacterium tuberculosis cell wall component mycolic acid elicits pathogen-associated host innate immune responses. Eur. J. Immunol. 35:890-900. https ://doi .org /10 .1002 /eji .200425332
25. Kuleshov, M.V., M.R. Jones, A.D. Rouillard, N.F. Fernandez, Q. Duan, Z. Wang, S. Koplev, S.L. Jenkins, K.M. Jagodnik, A. Lachmann, et al. 2016. Enrichr: A comprehensive gene set enrichment analysis web server 2016 update. Nucleic Acids Res. 44(W1):W90-W97. https ://doi .org /10 .1093 /nar /gkw377
26. Lai, Y., A. Di Nardo, T. Nakatsuji, A. Leichtle, Y. Yang, A.L. Cogen, Z.R. Wu, L.V. Hooper, R.R. Schmidt, S. von Aulock, et al. 2009. Commensal bacteria regulate Toll-like receptor 3-dependent inflammation after skin injury. Nat. Med. 15:1377-1382. https ://doi .org /10 .1038 /nm .2062
27. Langowski, J.L., X. Zhang, L. Wu, J.D. Mattson, T. Chen, K. Smith, B. Basham, T. McClanahan, R.A. Kastelein, and M. Oft. 2006. IL-23 promotes tumour incidence and growth. Nature. 442:461-465. https ://doi .org /10 .1038 /nature04808
28. Liang, D., A. Zuo, H. Shao, W.K. Born, R.L. O'Brien, H.J. Kaplan, and D. Sun. 2013. IL-23 receptor expression on γΔ T cells correlates with their enhancing or suppressive effects on autoreactive T cells in experimental autoimmune uveitis. J. Immunol. 191:1118-1125. https ://doi .org /10 .4049 /jimmunol .1300626
29. Matsunaga, I., and D.B. Moody. 2009. Mincle is a long sought receptor for mycobacterial cord factor. J. Exp. Med. 206:2865-2868. https ://doi .org /10 .1084 /jem .20092533
30. Minnikin, D.E., I.G. Hutchinson, and A.B. Caldicott. 1980. Thin-layer chromatography of methanolysates of mycolic acid-containing bacteria. J. Chromatogr. A. 188:221-233. https ://doi .org /10 .1016 /S0021-9673(00)88433-2
31. Mishra, A.K., L.J. Alderwick, D. Rittmann, C. Wang, A. Bhatt, W.R. Jacobs Jr., K. Takayama, L. Eggeling, and G.S. Besra. 2008. Identification of a novel alpha(1->6) mannopyranosyltransferase MptB from Corynebacterium glutamicum by deletion of a conserved gene, NCgl1505, affords a lipomannan-and lipoarabinomannan-deficient mutant. Mol. Microbiol. 68:1595-1613. https ://doi .org /10 .1111 /j .1365-2958 .2008 .06265 .x
32. Naik, S., N. Bouladoux, C. Wilhelm, M.J. Molloy, R. Salcedo, W. Kastenmuller, C. Deming, M. Quinones, L. Koo, S. Conlan, et al. 2012. Compartmentalized control of skin immunity by resident commensals. Science. 337:1115-1119. https ://doi .org /10 .1126 /science .1225152
33. Naik, S., N. Bouladoux, J.L. Linehan, S.J. Han, O.J. Harrison, C. Wilhelm, S. Conlan, S. Himmelfarb, A.L. Byrd, C. Deming, et al. 2015. Commensaldendritic-cell interaction specifies a unique protective skin immune signature. Nature. 520:104-108. https ://doi .org /10 .1038 /nature14052
34. Padhi, T., and Garima. 2013. Metabolic syndrome and skin: psoriasis and beyond. Indian J. Dermatol. 58:299-305. https ://doi .org /10 .4103 /0019-5154 .113950
35. Puig, L. 2017. The role of IL 23 in the treatment of psoriasis. Expert Rev. Clin. Immunol. 13:525-534. https ://doi .org /10 .1080 /1744666X .2017 .1292137
36. Quan, J., and J. Tian. 2011. Circular polymerase extension cloning for highthroughput cloning of complex and combinatorial DNA libraries. Nat. Protoc. 6:242-251. https ://doi .org /10 .1038 /nprot .2010 .181
37. Ramírez-Valle, F., E.E. Gray, and J.G. Cyster. 2015. Inflammation induces dermal Vγ4+ γΔT17 memory-like cells that travel to distant skin and accelerate secondary IL-17-driven responses. Proc. Natl. Acad. Sci. USA. 112:8046-8051. https ://doi .org /10 .1073 /pnas .1508990112
38. Riol-Blanco, L., V. Lazarevic, A. Awasthi, M. Mitsdoerffer, B.S. Wilson, A. Croxford, A. Waisman, V.K. Kuchroo, L.H. Glimcher, and M. Oukka. 2010. IL-23 receptor regulates unconventional IL-17-producing T cells that control bacterial infections. J. Immunol. 184:1710-1720. https ://doi .org /10 .4049 /jimmunol .0902796
39. Riol-Blanco, L., J. Ordovas-Montanes, M. Perro, E. Naval, A. Thiriot, D. Alvarez, S. Paust, J.N. Wood, and U.H. von Andrian. 2014. Nociceptive sensory neurons drive interleukin-23-mediated psoriasiform skin inflammation. Nature. 510:157-161. https ://doi .org /10 .1038 /nature13199
40. Scharschmidt, T.C., and M.A. Fischbach. 2013. What lives on our skin: Ecology, genomics and therapeutic opportunities of the skin microbiome. Drug Discov. Today Dis. Mech. 10:e83-89. https ://doi .org /10 .1016 /j .ddmec .2012 .12 .003
41. Sutton, C.E., S.J. Lalor, C.M. Sweeney, C.F. Brereton, E.C. Lavelle, and K.H. Mills. 2009. Interleukin-1 and IL-23 induce innate IL-17 production from gammadelta T cells, amplifying Th17 responses and autoimmunity. Immunity. 31:331-341. https ://doi .org /10 .1016 /j .immuni .2009 .08 .001
42. Vantourout, P., and A. Hayday. 2013. Six-of-the-best: Unique contributions of γΔ T cells to immunology. Nat. Rev. Immunol. 13:88-100. https ://doi .org /10 .1038 /nri3384
43. Wang, K., and M. Karin. 2015. The IL-23 to IL-17 cascade inflammation-related cancers. Clin. Exp. Rheumatol. 33(4, Suppl 92):S87-S90
44. Yamasaki, S., M. Matsumoto, O. Takeuchi, T. Matsuzawa, E. Ishikawa, M. Sakuma, H. Tateno, J. Uno, J. Hirabayashi, Y. Mikami, et al. 2009. C-type lectin Mincle is an activating receptor for pathogenic fungus, Malassezia. Proc. Natl. Acad. Sci. USA. 106:1897-1902. https ://doi .org /10 .1073 / pnas .0805177106
45. Zhang, Y., Q. Li, E. Rao, Y. Sun, M.E. Grossmann, R.J. Morris, M.P. Cleary, and B. Li. 2015. Epidermal fatty acid binding protein promotes skin inflammation induced by high-fat diet. Immunity. 42:953-964. https :// doi .org /10 .1016 /j .immuni .2015 .04 .016