Non-classical Immunity Controls Microbiota Impact on Skin Immunity and Tissue Repair

Cell

Volumn 172, Issue 4, 2018, Pages 784-796.e18

  Linehan, Jonathan L ^a   Harrison, Oliver J ^a   Han, Seong Ji ^a   Byrd, Allyson L ^a,b,c   Vujkovic Cvijin, Ivan ^a   Villarino, Alejandro V ^d   Sen, Shurjo K ^e   Shaik, Jahangheer ^a   Smelkinson, Margery ^a   Tamoutounour, Samira ^a   Collins, Nicholas ^a   Bouladoux, Nicolas ^a   Dzutsev, Amiran ^e   Rosshart, Stephan P ^f   Arbuckle, Jesse H ^a   Wang, Chyung Ru ^g   Kristie, Thomas M ^a   Rehermann, Barbara ^f   Trinchieri, Giorgio ^e   Brenchley, Jason M ^a   O'Shea, John J ^d   Belkaid, Yasmine ^a   more..

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

^b NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^c BOSTON UNIVERSITY   (United States)

^d NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

^e NATIONAL CANCER INSTITUTE   (United States)

^f NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^g NORTHWESTERN UNIVERSITY   (United States)

Author keywords

H2 M3; MHCIb; microbiota; non classical MHC class I; skin immunity; Staphylococcus epidermidis; tissue repair

Indexed keywords

FORMYLMETHIONINE; INTERLEUKIN 17; LIGAND; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; HLA ANTIGEN CLASS 1;

A2780-TC1 CELL LINE; ADAPTIVE IMMUNITY; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL IMMUNITY; CD8+ T LYMPHOCYTE; CELL ISOLATION; COMMENSAL; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CORRELATIONAL STUDY; CYTOTOXIC T LYMPHOCYTE; DERMATITIS; EFFECTOR CELL; EPIFLUORESCENCE MICROSCOPY; FEMALE; GENE EXPRESSION; HERPES VIRUS INFECTION; HOMEOSTASIS; HUMAN; HUMAN ALPHAHERPESVIRUS 1; IMMUNE RESPONSE; IMMUNOFLUORESCENCE; IMMUNOREGULATION; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; LEISHMANIA MAJOR; LEISHMANIASIS; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; MOUSE; NONHUMAN; PATHOGENESIS; PHYSIOLOGY; PLEIOTROPY; PRIORITY JOURNAL; RNA EXTRACTION; RNA SEQUENCE; SKIN FLORA; SKIN INJURY; SKIN PROTECTION; STAPHYLOCOCCUS EPIDERMIDIS; TISSUE REPAIR; WOUND CLOSURE; WOUND HEALING; ANIMAL; BACTERIUM; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; MICROFLORA; SKIN; T LYMPHOCYTE; TRANSGENIC MOUSE;

ADAPTIVE IMMUNITY; ANIMALS; BACTERIA; GENE EXPRESSION REGULATION; HISTOCOMPATIBILITY ANTIGENS CLASS I; MICE; MICE, TRANSGENIC; MICROBIOTA; SKIN; T-LYMPHOCYTES;

EID: 85041116653     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2017.12.033     Document Type: Article

References (53)

1. Adams, E.J., Luoma, A.M., The adaptable major histocompatibility complex (MHC) fold: structure and function of nonclassical and MHC class I-like molecules. Annu. Rev. Immunol. 31 (2013), 529–561.
2. An, D., Oh, S.F., Olszak, T., Neves, J.F., Avci, F.Y., Erturk-Hasdemir, D., Lu, X., Zeissig, S., Blumberg, R.S., Kasper, D.L., Sphingolipids from a symbiotic microbe regulate homeostasis of host intestinal natural killer T cells. Cell 156 (2014), 123–133.
3. Anders, S., Huber, W., Differential expression analysis for sequence count data. Genome Biol., 11, 2010, R106.
4. Belkaid, Y., Hand, T.W., Role of the microbiota in immunity and inflammation. Cell 157 (2014), 121–141.
5. Belkaid, Y., Segre, J.A., Dialogue between skin microbiota and immunity. Science 346 (2014), 954–959.
6. Belkaid, Y., Tamoutounour, S., The influence of skin microorganisms on cutaneous immunity. Nat. Rev. Immunol. 16 (2016), 353–366.
7. Belkaid, Y., Von Stebut, E., Mendez, S., Lira, R., Caler, E., Bertholet, S., Udey, M.C., Sacks, D., CD8+ T cells are required for primary immunity in C57BL/6 mice following low-dose, intradermal challenge with Leishmania major. J. Immunol. 168 (2002), 3992–4000.
8. Beura, L.K., Hamilton, S.E., Bi, K., Schenkel, J.M., Odumade, O.A., Casey, K.A., Thompson, E.A., Fraser, K.A., Rosato, P.C., Filali-Mouhim, A., et al. Normalizing the environment recapitulates adult human immune traits in laboratory mice. Nature 532 (2016), 512–516.
9. Bolger, A.M., Lohse, M., Usadel, B., Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30 (2014), 2114–2120.
10. Byrd, A.L., Deming, C., Cassidy, K.B., Harrison, O.J., Conlan, S., Belkaid, Y., Segre, J.A., Kong, H.H., NISC Comparative Sequencing Program. Staphylococcus aureus and S. epidermidis strain diversity underlying human atopic dermatitis. Sci. Transl. Med., 9, 2017 pii: eaal465.
11. Cho, H., Bediako, Y., Xu, H., Choi, H.J., Wang, C.R., Positive selecting cell type determines the phenotype of MHC class Ib-restricted CD8+ T cells. Proc. Natl. Acad. Sci. USA 108 (2011), 13241–13246.
12. Chun, T., Serbina, N.V., Nolt, D., Wang, B., Chiu, N.M., Flynn, J.L., Wang, C.R., Induction of M3-restricted cytotoxic T lymphocyte responses by N-formylated peptides derived from Mycobacterium tuberculosis. J. Exp. Med. 193 (2001), 1213–1220.
13. Cong, Y., Feng, T., Fujihashi, K., Schoeb, T.R., Elson, C.O., A dominant, coordinated T regulatory cell-IgA response to the intestinal microbiota. Proc. Natl. Acad. Sci. USA 106 (2009), 19256–19261.
14. Conlan, S., Mijares, L.A., Becker, J., Blakesley, R.W., Bouffard, G.G., Brooks, S., Coleman, H., Gupta, J., Gurson, N., Park, M., et al., NISC Comparative Sequencing Program. Staphylococcus epidermidis pan-genome sequence analysis reveals diversity of skin commensal and hospital infection-associated isolates. Genome Biol., 13, 2012, R64.
15. Dobin, A., Davis, C.A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M., Gingeras, T.R., STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29 (2013), 15–21.
16. Doyle, C.K., Davis, B.K., Cook, R.G., Rich, R.R., Rodgers, J.R., Hyperconservation of the N-formyl peptide binding site of M3: evidence that M3 is an old eutherian molecule with conserved recognition of a pathogen-associated molecular pattern. J. Immunol. 171 (2003), 836–844.
17. Eming, S.A., Martin, P., Tomic-Canic, M., Wound repair and regeneration: mechanisms, signaling, and translation. Sci. Transl. Med., 6, 2014, 265sr6.
18. Ewels, P., Magnusson, M., Lundin, S., Käller, M., MultiQC: summarize analysis results for multiple tools and samples in a single report. Bioinformatics 32 (2016), 3047–3048.
19. Fan, X., Rudensky, A.Y., Hallmarks of Tissue-Resident Lymphocytes. Cell 164 (2016), 1198–1211.
20. Gebhardt, T., Wakim, L.M., Eidsmo, L., Reading, P.C., Heath, W.R., Carbone, F.R., Memory T cells in nonlymphoid tissue that provide enhanced local immunity during infection with herpes simplex virus. Nat. Immunol. 10 (2009), 524–530.
21. Gensollen, T., Iyer, S.S., Kasper, D.L., Blumberg, R.S., How colonization by microbiota in early life shapes the immune system. Science 352 (2016), 539–544.
22. Godfrey, D.I., Uldrich, A.P., McCluskey, J., Rossjohn, J., Moody, D.B., The burgeoning family of unconventional T cells. Nat. Immunol. 16 (2015), 1114–1123.
23. Hand, T.W., Dos Santos, L.M., Bouladoux, N., Molloy, M.J., Pagán, A.J., Pepper, M., Maynard, C.L., Elson, C.O. 3rd, Belkaid, Y., Acute gastrointestinal infection induces long-lived microbiota-specific T cell responses. Science 337 (2012), 1553–1556.
24. Honda, K., Littman, D.R., The microbiota in adaptive immune homeostasis and disease. Nature 535 (2016), 75–84.
25. Ivanov, I.I., Atarashi, K., Manel, N., Brodie, E.L., Shima, T., Karaoz, U., Wei, D., Goldfarb, K.C., Santee, C.A., Lynch, S.V., et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139 (2009), 485–498.
26. Jameson, J., Ugarte, K., Chen, N., Yachi, P., Fuchs, E., Boismenu, R., Havran, W.L., A role for skin gammadelta T cells in wound repair. Science 296 (2002), 747–749.
27. Kawano, M., Komi-Kuramochi, A., Asada, M., Suzuki, M., Oki, J., Jiang, J., Imamura, T., Comprehensive analysis of FGF and FGFR expression in skin: FGF18 is highly expressed in hair follicles and capable of inducing anagen from telogen stage hair follicles. J. Invest. Dermatol. 124 (2005), 877–885.
28. Kerksiek, K.M., Busch, D.H., Pamer, E.G., Variable immunodominance hierarchies for H2-M3-restricted N-formyl peptides following bacterial infection. J. Immunol. 166 (2001), 1132–1140.
29. Keyes, B.E., Liu, S., Asare, A., Naik, S., Levorse, J., Polak, L., Lu, C.P., Nikolova, M., Pasolli, H.A., Fuchs, E., Impaired epidermal to dendritic T cell signaling slows wound repair in aged skin. Cell 167 (2016), 1323–1338.e14.
30. Lai, Y., Di Nardo, A., Nakatsuji, T., Leichtle, A., Yang, Y., Cogen, A.L., Wu, Z.R., Hooper, L.V., Schmidt, R.R., von Aulock, S., et al. Commensal bacteria regulate Toll-like receptor 3-dependent inflammation after skin injury. Nat. Med. 15 (2009), 1377–1382.
31. Lai, Y., Cogen, A.L., Radek, K.A., Park, H.J., Macleod, D.T., Leichtle, A., Ryan, A.F., Di Nardo, A., Gallo, R.L., Activation of TLR2 by a small molecule produced by Staphylococcus epidermidis increases antimicrobial defense against bacterial skin infections. J. Invest. Dermatol. 130 (2010), 2211–2221.
32. Li, B., Dewey, C.N., RSEM: accurate transcript quantification from RNA-seq data with or without a reference genome. BMC Bioinformatics, 12, 2011, 323.
33. Lindahl, K.F., Byers, D.E., Dabhi, V.M., Hovik, R., Jones, E.P., Smith, G.P., Wang, C.R., Xiao, H., Yoshino, M., H2-M3, a full-service class Ib histocompatibility antigen. Annu. Rev. Immunol. 15 (1997), 851–879.
34. Moon, J.J., Chu, H.H., Pepper, M., McSorley, S.J., Jameson, S.C., Kedl, R.M., Jenkins, M.K., Naive CD4(+) T cell frequency varies for different epitopes and predicts repertoire diversity and response magnitude. Immunity 27 (2007), 203–213.
35. Naik, S., Bouladoux, N., Wilhelm, C., Molloy, M.J., Salcedo, R., Kastenmuller, W., Deming, C., Quinones, M., Koo, L., Conlan, S., et al. Compartmentalized control of skin immunity by resident commensals. Science 337 (2012), 1115–1119.
36. Naik, S., Bouladoux, N., Linehan, J.L., Han, S.J., Harrison, O.J., Wilhelm, C., Conlan, S., Himmelfarb, S., Byrd, A.L., Deming, C., et al. Commensal-dendritic-cell interaction specifies a unique protective skin immune signature. Nature 520 (2015), 104–108.
37. Nielsen, M.M., Witherden, D.A., Havran, W.L., γδ T cells in homeostasis and host defence of epithelial barrier tissues. Nat. Rev. Immunol. 17 (2017), 733–745.
38. Obar, J.J., Khanna, K.M., Lefrançois, L., Endogenous naive CD8+ T cell precursor frequency regulates primary and memory responses to infection. Immunity 28 (2008), 859–869.
39. Pamer, E.G., Resurrecting the intestinal microbiota to combat antibiotic-resistant pathogens. Science 352 (2016), 535–538.
40. Ploss, A., Lauvau, G., Contos, B., Kerksiek, K.M., Guirnalda, P.D., Leiner, I., Lenz, L.L., Bevan, M.J., Pamer, E.G., Promiscuity of MHC class Ib-restricted T cell responses. J. Immunol. 171 (2003), 5948–5955.
41. Rakoff-Nahoum, S., Paglino, J., Eslami-Varzaneh, F., Edberg, S., Medzhitov, R., Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118 (2004), 229–241.
42. Rodgers, J.R., Cook, R.G., MHC class Ib molecules bridge innate and acquired immunity. Nat. Rev. Immunol. 5 (2005), 459–471.
43. Scharschmidt, T.C., Vasquez, K.S., Truong, H.A., Gearty, S.V., Pauli, M.L., Nosbaum, A., Gratz, I.K., Otto, M., Moon, J.J., Liese, J., et al. A wave of regulatory T cells into neonatal skin mediates tolerance to commensal microbes. Immunity 43 (2015), 1011–1021.
44. Schenkel, J.M., Masopust, D., Tissue-resident memory T cells. Immunity 41 (2014), 886–897.
45. Seaman, M.S., Wang, C.R., Forman, J., MHC class Ib-restricted CTL provide protection against primary and secondary Listeria monocytogenes infection. J. Immunol. 165 (2000), 5192–5201.
46. Shang, S., Siddiqui, S., Bian, Y., Zhao, J., Wang, C.R., Nonclassical MHC Ib-restricted CD8+ T cells recognize mycobacterium tuberculosis-derived protein antigens and contribute to protection against infection. PLoS Pathog., 12, 2016, e1005688.
47. Torkamani, N., Rufaut, N., Jones, L., Sinclair, R., The arrector pili muscle, the bridge between the follicular stem cell niche and the interfollicular epidermis. Anat. Sci. Int. 92 (2017), 151–158.
48. van der Fits, L., Mourits, S., Voerman, J.S., Kant, M., Boon, L., Laman, J.D., Cornelissen, F., Mus, A.M., Florencia, E., Prens, E.P., Lubberts, E., Imiquimod-induced psoriasis-like skin inflammation in mice is mediated via the IL-23/IL-17 axis. J. Immunol. 182 (2009), 5836–5845.
49. van Lint, A., Ayers, M., Brooks, A.G., Coles, R.M., Heath, W.R., Carbone, F.R., Herpes simplex virus-specific CD8+ T cells can clear established lytic infections from skin and nerves and can partially limit the early spread of virus after cutaneous inoculation. J. Immunol. 172 (2004), 392–397.
50. Van Rhijn, I., Godfrey, D.I., Rossjohn, J., Moody, D.B., Lipid and small-molecule display by CD1 and MR1. Nat. Rev. Immunol. 15 (2015), 643–654.
51. Vugmeyster, Y., Glas, R., Pérarnau, B., Lemonnier, F.A., Eisen, H., Ploegh, H., Major histocompatibility complex (MHC) class I KbDb -/- deficient mice possess functional CD8+ T cells and natural killer cells. Proc. Natl. Acad. Sci. USA 95 (1998), 12492–12497.
52. Werner, S., Grose, R., Regulation of wound healing by growth factors and cytokines. Physiol. Rev. 83 (2003), 835–870.
53. Yang, Y., Torchinsky, M.B., Gobert, M., Xiong, H., Xu, M., Linehan, J.L., Alonzo, F., Ng, C., Chen, A., Lin, X., et al. Focused specificity of intestinal TH17 cells towards commensal bacterial antigens. Nature 510 (2014), 152–156.