Antigen delivery to dendritic cells shapes human CD4+and CD8+T cell memory responses to Staphylococcus aureus

PLoS Pathogens

Volumn 13, Issue 5, 2017, Pages

  Uebele, Julia ^a,b   Stein, Christoph ^a,b   Nguyen, Minh Thu ^c   Schneider, Anja ^a   Kleinert, Franziska ^b   Tichá, Olga ^a   Bierbaum, Gabriele ^b   Götz, Friedrich ^c   Bekeredjian Ding, Isabelle ^a,b  

^a PAUL EHRLICH INSTITUT   (Germany)

^b UNIVERSITY HOSPITAL BONN   (Germany)

^c UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOTOXIN; GAMMA INTERFERON; GRANULOCYTE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5; MESSENGER RNA; PROTEIN; SITC PROTEIN; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; BACTERIAL ANTIGEN; CYTOKINE; IL10 PROTEIN, HUMAN;

ANTIGEN PRESENTATION; ARTICLE; ASSAY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ISOLATION; CELL STIMULATION; CELLULAR IMMUNITY; COCULTURE; CONTROLLED STUDY; DENDRITIC CELL; DNA ISOLATION; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME LINKED IMMUNOSPOT ASSAY; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; FLUOROSPOT ASSAY; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; HEK293 CELL LINE; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; IN VITRO STUDY; LUCIFERASE ASSAY; MEMORY T LYMPHOCYTE; MONOCYTE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; POLYMERASE CHAIN REACTION; PROTEIN PURIFICATION; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION; TH1 CELL; TH2 CELL; WESTERN BLOTTING; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; MICROBIOLOGY; REGULATORY T LYMPHOCYTE;

ANTIGEN PRESENTATION; ANTIGENS, BACTERIAL; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CYTOKINES; DENDRITIC CELLS; GRANULOCYTE COLONY-STIMULATING FACTOR; HUMANS; IMMUNE TOLERANCE; INTERLEUKIN-10; INTERLEUKIN-2; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; T-LYMPHOCYTES, REGULATORY; TH2 CELLS;

EID: 85020217711     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1006387     Document Type: Article

References (75)

1. Eiff C von, Becker K, Machka K, Stammer H, Peters G, (2001) Nasal carriage as a source of Staphylococcus aureus bacteremia. Study Group. The New England journal of medicine344 (1): 11–16. doi: 10.1056/NEJM200101043440102 11136954
2. Foster TJ, (2005) Immune evasion by staphylococci. Nature reviews. Microbiology3 (12): 948–958. doi: 10.1038/nrmicro1289 16322743
3. Daum RS, Spellberg B, (2012) Progress toward a Staphylococcus aureus vaccine. Clinical infectious diseases: an official publication of the Infectious Diseases Society of America54 (4): 560–567.
4. Botelho-Nevers E, Verhoeven P, Paul S, Grattard F, Pozzetto B, et al. (2013) Staphylococcal vaccine development: review of past failures and plea for a future evaluation of vaccine efficacy not only on staphylococcal infections but also on mucosal carriage. Expert review of vaccines12 (11): 1249–1259. doi: 10.1586/14760584.2013.840091 24111513
5. Fowler VG, Proctor RA, (2014) Where does a Staphylococcus aureus vaccine stand. Clinical microbiology and infection: the official publication of the European Society of Clinical Microbiology and Infectious Diseases20Suppl 5: 66–75.
6. Pletz MW, Uebele J, Gotz K, Hagel S, Bekeredjian-Ding I, (2016) Vaccines against major ICU pathogens: where do we stand. Current Opinion in Critical Care22 (5): 470–476. doi: 10.1097/MCC.0000000000000338 27583587
7. Archer NK, Harro JM, Shirtliff ME, (2013) Clearance of Staphylococcus aureus Nasal Carriage Is T Cell Dependent and Mediated through Interleukin-17A Expression and Neutrophil Influx. Infect. Immun. 81 (6): 2070–2075. Available: http://iai.asm.org/content/81/6/2070.full. doi: 10.1128/IAI.00084-13 23529621
8. Mancini F, Monaci E, Lofano G, Torre A, Bacconi M, et al. (2016) One Dose of Staphylococcus aureus 4C-Staph Vaccine Formulated with a Novel TLR7-Dependent Adjuvant Rapidly Protects Mice through Antibodies, Effector CD4+ T Cells, and IL-17A. PloS one11 (1): e0147767. doi: 10.1371/journal.pone.0147767 26812180
9. Montgomery CP, Daniels M, Zhao F, Alegre M-L, Chong AS, et al. (2014) Protective immunity against recurrent Staphylococcus aureus skin infection requires antibody and interleukin-17A. Infection and immunity82 (5): 2125–2134. doi: 10.1128/IAI.01491-14 24614654
10. Miller LS, Cho JS, (2011) Immunity against Staphylococcus aureus cutaneous infections. Nature reviews. Immunology11 (8): 505–518. doi: 10.1038/nri3010 21720387
11. Lin L, Ibrahim AS, Xu X, Farber JM, Avanesian V, et al. (2009) Th1-Th17 Cells Mediate Protective Adaptive Immunity against Staphylococcus aureus and Candida albicans Infection in Mice. PLOS Pathog5 (12): e1000703. doi: 10.1371/journal.ppat.1000703 20041174
12. Choi SJ, Kim M-H, Jeon J, Kim OY, Choi Y, et al. (2015) Active Immunization with Extracellular Vesicles Derived from Staphylococcus aureus Effectively Protects against Staphylococcal Lung Infections, Mainly via Th1 Cell-Mediated Immunity. PloS one10 (9): e0136021. doi: 10.1371/journal.pone.0136021 26333035
13. Zielinski CE, Mele F, Aschenbrenner D, Jarrossay D, Ronchi F, et al. (2012) Pathogen-induced human TH17 cells produce IFN-γ or IL-10 and are regulated by IL-1β. Nature484 (7395): 514–518. doi: 10.1038/nature10957 22466287
14. Murphy AG, O'Keeffe KM, Lalor SJ, Maher BM, Mills Kingston H G, et al. (2014) Staphylococcus aureus infection of mice expands a population of memory γδ T cells that are protective against subsequent infection. Journal of immunology (Baltimore, Md.: 1950)192 (8): 3697–3708.
15. Brown AF, Murphy AG, Lalor SJ, Leech JM, O'Keeffe KM, et al. (2015) Memory Th1 Cells Are Protective in Invasive Staphylococcus aureus Infection. PLoS pathogens11 (11): e1005226. doi: 10.1371/journal.ppat.1005226 26539822
16. Kolata JB, Kühbandner I, Link C, Normann N, Vu CH, et al. (2015) The Fall of a Dogma? Unexpected High T-Cell Memory Response to Staphylococcus aureus in Humans. The Journal of infectious diseases.
17. Zautner AE, Krause M, Stropahl G, Holtfreter S, Frickmann H, et al. (2010) Intracellular Persisting Staphylococcus aureus Is the Major Pathogen in Recurrent Tonsillitis. PloS one5 (3).
18. Sachse F, Becker K, Eiff C von, Metze D, Rudack C, (2010) Staphylococcus aureus invades the epithelium in nasal polyposis and induces IL-6 in nasal epithelial cells in vitro. Allergy65 (11): 1430–1437. doi: 10.1111/j.1398-9995.2010.02381.x 20456313
19. Boczkowski D, Nair SK, Nam JH, Lyerly HK, Gilboa E, (2000) Induction of tumor immunity and cytotoxic T lymphocyte responses using dendritic cells transfected with messenger RNA amplified from tumor cells. Cancer research60 (4): 1028–1034. 10706120
20. Fotin-Mleczek M, Zanzinger K, Heidenreich R, Lorenz C, Thess A, et al. (2012) Highly potent mRNA based cancer vaccines represent an attractive platform for combination therapies supporting an improved therapeutic effect. The journal of gene medicine14 (6): 428–439. doi: 10.1002/jgm.2605 22262664
21. Gilboa E, Vieweg J, (2004) Cancer immunotherapy with mRNA-transfected dendritic cells. Immunological reviews199: 251–263. doi: 10.1111/j.0105-2896.2004.00139.x 15233739
22. Rejman J, Tavernier G, Bavarsad N, Demeester J, De Smedt Stefaan C, (2010) mRNA transfection of cervical carcinoma and mesenchymal stem cells mediated by cationic carriers. Journal of controlled release: official journal of the Controlled Release Society147 (3): 385–391.
23. Li J, Sun Y, Jia T, Zhang R, Zhang K, et al. (2014) Messenger RNA vaccine based on recombinant MS2 virus-like particles against prostate cancer. International journal of cancer. Journal international du cancer134 (7): 1683–1694. doi: 10.1002/ijc.28482 24105486
24. Wong S-S, Webby RJ, (2012) An mRNA vaccine for influenza. Nature biotechnology30 (12): 1202–1204. doi: 10.1038/nbt.2439 23222788
25. Weissman D, Ni H, Scales D, Dude A, Capodici J, et al. (2000) HIV Gag mRNA Transfection of Dendritic Cells (DC) Delivers Encoded Antigen to MHC Class I and II Molecules, Causes DC Maturation, and Induces a Potent Human In Vitro Primary Immune Response. The Journal of Immunology165 (8): 4710–4717. Available: http://www.jimmunol.org/content/165/8/4710.full.pdf#page=1&view=FitH. Accessed 10 September 2015. 11035115
26. Thornburg C, Boczkowski D, Gilboa E, Nair SK, (2000) Induction of cytotoxic T lymphocytes with dendritic cells transfected with human papillomavirus E6 and E7 RNA: implications for cervical cancer immunotherapy. Journal of immunotherapy (Hagerstown, Md.: 1997)23 (4): 412–418.
27. Müller P, Müller-Anstett M, Wagener J, Gao Q, Kaesler S, et al. (2010) The Staphylococcus aureus lipoprotein SitC colocalizes with Toll-like receptor 2 (TLR2) in murine keratinocytes and elicits intracellular TLR2 accumulation. Infection and immunity78 (10): 4243–4250. doi: 10.1128/IAI.00538-10 20679445
28. Stoll H, Dengjel J, Nerz C, Gotz F, (2005) Staphylococcus aureus deficient in lipidation of prelipoproteins is attenuated in growth and immune activation. Infection and immunity73 (4): 2411–2423. doi: 10.1128/IAI.73.4.2411-2423.2005 15784587
29. Holtfreter S, Grumann D, Schmudde M, Nguyen HTT, Eichler P, et al. (2007) Clonal distribution of superantigen genes in clinical Staphylococcus aureus isolates. Journal of clinical microbiology45 (8): 2669–2680. doi: 10.1128/JCM.00204-07 17537946
30. Katayama Y, Ito T, Hiramatsu K, (2000) A New Class of Genetic Element, Staphylococcus Cassette Chromosome mec, Encodes Methicillin Resistance in Staphylococcus aureus. Antimicrobial agents and chemotherapy44 (6): 1549–1555. 10817707
31. Rowe J, Macaubas C, Monger TM, Holt BJ, Harvey J, et al. (2000) Antigen-specific responses to diphtheria-tetanus-acellular pertussis vaccine in human infants are initially Th2 polarized. Infection and immunity68 (7): 3873–3877. 10858197
32. Scheel B, Braedel S, Probst J, Carralot J-P, Wagner H, et al. (2004) Immunostimulating capacities of stabilized RNA molecules. European journal of immunology34 (2): 537–547. doi: 10.1002/eji.200324198 14768059
33. Hornung V, Ellegast J, Kim S, Brzózka K, Jung A, et al. (2006) 5'-Triphosphate RNA is the ligand for RIG-I. Science (New York, N.Y.)314 (5801): 994–997.
34. Yu P, Lee Y, Liu W, Chin RK, Wang J, et al. (2004) Priming of naive T cells inside tumors leads to eradication of established tumors. Nature immunology5 (2): 141–149. doi: 10.1038/ni1029 14704792
35. Archer NK, Adappa ND, Palmer JN, Cohen NA, Harro JM, et al. (2016) IL-17A and IL-17F are critical for antimicrobial peptide production and clearance of Staphylococcus aureus nasal colonization. Infection and immunity. Accessed 3 November 2016.
36. Chau TA, McCully ML, Brintnell W, An G, Kasper KJ, et al. (2009) Toll-like receptor 2 ligands on the staphylococcal cell wall downregulate superantigen-induced T cell activation and prevent toxic shock syndrome. Nature medicine15 (6): 641–648. doi: 10.1038/nm.1965 19465927
37. Rossetti M, Gregori S, Roncarolo MG, (2010) Granulocyte-colony stimulating factor drives the in vitro differentiation of human dendritic cells that induce anergy in naïve T cells. European journal of immunology40 (11): 3097–3106. doi: 10.1002/eji.201040659 20957751
38. Rutella S, Zavala F, Danese S, Kared H, Leone G, (2005) Granulocyte Colony-Stimulating Factor: A Novel Mediator of T Cell Tolerance. The Journal of Immunology175 (11): 7085–7091. 16301609
39. McNeely TB, Shah NA, Fridman A, Joshi A, Hartzel JS, et al. (2014) Mortality among recipients of the Merck V710 Staphylococcus aureus vaccine after postoperative S. aureus infections: an analysis of possible contributing host factors. Human vaccines & immunotherapeutics10 (12): 3513–3516.
40. Bercovici N, Duffour M-T, Agrawal S, Salcedo M, Abastado J-P, (2000) New Methods for Assessing T-Cell Responses. Clinical and diagnostic laboratory immunology7 (6): 859–864. 11063487
41. Todryk SM, Pathan AA, Keating S, Porter DW, Berthoud T, et al. (2009) The relationship between human effector and memory T cells measured by ex vivo and cultured ELISPOT following recent and distal priming. Immunology128 (1): 83–91. Accessed 24 April 2017. doi: 10.1111/j.1365-2567.2009.03073.x 19689738
42. Veiga-Fernandes H, Walter U, Bourgeois C, McLean A, Rocha B, (2000) Response of naive and memory CD8+ T cells to antigen stimulation in vivo. Nature immunology1 (1): 47–53. doi: 10.1038/76907 10881174
43. Vu CH, Kolata J, Stentzel S, Beyer A, Salazar MG, et al. (2016) Adaptive immune response to lipoproteins of Staphylococcus aureus in healthy subjects. Proteomics.
44. Stentzel S, Teufelberger A, Nordengrün M, Kolata J, Schmidt F, et al. (2017) Staphylococcal serine protease–like proteins are pacemakers of allergic airway reactions to Staphylococcus aureus. Journal of Allergy and Clinical Immunology139 (2): 492–500.e8. Available: http://www.jacionline.org/article/S009167491630272X/fulltext. doi: 10.1016/j.jaci.2016.03.045 27315768
45. Mueller SN, Zaid A, Carbone FR, (2014) Tissue-Resident T Cells: Dynamic Players in Skin Immunity. Front. Immunol. 5: 332. doi: 10.3389/fimmu.2014.00332 25076947
46. Zhao YX, Tarkowski A, (1995) Impact of interferon-gamma receptor deficiency on experimental Staphylococcus aureus septicemia and arthritis. Journal of immunology (Baltimore, Md.: 1950)155 (12): 5736–5742.
47. Kosor Krnic E, Gagro A, Drazenovic V, Kuzman I, Jeren T, et al. (2008) Enumeration of haemagglutinin-specific CD8+ T cells after influenza vaccination using MHC class I peptide tetramers. Scandinavian journal of immunology67 (1): 86–94. doi: 10.1111/j.1365-3083.2007.02042.x 18052968
48. Foreman A, Holtappels G, Psaltis AJ, Jervis-Bardy J, Field J, et al. (2011) Adaptive immune responses in Staphylococcus aureus biofilm-associated chronic rhinosinusitis. Allergy66 (11): 1449–1456. doi: 10.1111/j.1398-9995.2011.02678.x 21834937
49. Kirsche H, Niederführ A, Deutschle T, Fuchs C, Riechelmann H, (2010) Ratio of myeloid and plasmacytoid dendritic cells and TH2 skew in CRS with nasal polyps. Allergy65 (1): 24–31. doi: 10.1111/j.1398-9995.2009.02174.x 19793060
50. Netea MG, Kullberg BJ, van der Meer J W M, (2005) Severely impaired IL-12/IL-18/IFNgamma axis in patients with hyper IgE syndrome. European journal of clinical investigation35 (11): 718–721. doi: 10.1111/j.1365-2362.2005.01564.x 16269022
51. Niebuhr M, Baumert K, Heratizadeh A, Satzger I, Werfel T, (2014) Impaired NLRP3 inflammasome expression and function in atopic dermatitis due to Th2 milieu. Allergy69 (8): 1058–1067. doi: 10.1111/all.12428 24894535
52. Warner JA, McGirt LY, Beck LA, (2009) Biomarkers of Th2 polarity are predictive of staphylococcal colonization in subjects with atopic dermatitis. The British journal of dermatology160 (1): 183–185. doi: 10.1111/j.1365-2133.2008.08905.x 19016695
53. Huber JP, Farrar JD, (2011) Regulation of effector and memory T-cell functions by type I interferon. Immunology132 (4): 466–474. doi: 10.1111/j.1365-2567.2011.03412.x 21320124
54. Kolumam GA, Thomas S, Thompson LJ, Sprent J, Murali-Krishna K, (2005) Type I interferons act directly on CD8 T cells to allow clonal expansion and memory formation in response to viral infection. The Journal of experimental medicine202 (5): 637–650. doi: 10.1084/jem.20050821 16129706
55. Bendriss-Vermare N, Burg S, Kanzler H, Chaperot L, Duhen T, et al. (2005) Virus overrides the propensity of human CD40L-activated plasmacytoid dendritic cells to produce Th2 mediators through synergistic induction of IFN-{gamma} and Th1 chemokine production. Journal of leukocyte biology78 (4): 954–966. doi: 10.1189/jlb.0704383 16081597
56. Parcina M, Miranda-Garcia MA, Durlanik S, Ziegler S, Over B, et al. (2013) Pathogen-triggered activation of plasmacytoid dendritic cells induces IL-10-producing B cells in response to Staphylococcus aureus. Journal of immunology (Baltimore, Md.: 1950)190 (4): 1591–1602.
57. Parcina M, Wendt C, Goetz F, Zawatzky R, Zahringer U, et al. (2008) Staphylococcus aureus-Induced Plasmacytoid Dendritic Cell Activation Is Based on an IgG-Mediated Memory Response. The Journal of Immunology181 (6): 3823–3833. 18768836
58. Bekeredjian-Ding I, Greil J, Ammann S, Parcina M, (2014) Plasmacytoid Dendritic Cells: Neglected Regulators of the Immune Response to Staphylococcus aureus. Frontiers in immunology5: 238. doi: 10.3389/fimmu.2014.00238 24904586
59. Sander LE, Davis MJ, Boekschoten MV, Amsen D, Dascher CC, et al. (2011) Detection of prokaryotic mRNA signifies microbial viability and promotes immunity. Nature474 (7351): 385–389. doi: 10.1038/nature10072 21602824
60. Bachmann MF, Oxenius A, (2007) Interleukin 2: from immunostimulation to immunoregulation and back again. EMBO Reports8 (12): 1142–1148. doi: 10.1038/sj.embor.7401099 18059313
61. Brubaker AL, Kovacs EJ, (2013) G-CSF enhances resolution of Staphylococcus aureus wound infection in an age-dependent manner. Shock (Augusta, Ga.)40 (4): 327–333.
62. Söderquist B, Danielsson D, Holmberg H, Vikerfors T, (1995) Granulocyte colony-stimulating factor (G-CSF) and interleukin (IL)-8 in sera from patients with Staphylococcus aureus septicemia. Clinical Microbiology and Infection1 (2): 101–109. 11866736
63. Karzai W, Specht BU von, Parent C, Haberstroh J, Wollersen K, et al. (1999) G-CSF during Escherichia coli versus Staphylococcus aureus pneumonia in rats has fundamentally different and opposite effects. American journal of respiratory and critical care medicine159 (5 Pt 1): 1377–1382.
64. Heim CE, Vidlak D, Scherr TD, Hartman CW, Garvin KL, et al. (2015) IL-12 promotes myeloid-derived suppressor cell recruitment and bacterial persistence during Staphylococcus aureus orthopedic implant infection. Journal of immunology (Baltimore, Md.: 1950)194 (8): 3861–3872.
65. Yang J-Z, Zhang J-Q, Sun L-X, (2015) Mechanisms for T cell tolerance induced with granulocyte colony-stimulating factor. Molecular immunology70: 56–62. doi: 10.1016/j.molimm.2015.12.006 26703218
66. Franzke A, Piao W, Lauber J, Gatzlaff P, Konecke C, et al. (2003) G-CSF as immune regulator in T cells expressing the G-CSF receptor: implications for transplantation and autoimmune diseases. Blood102 (2): 734–739. doi: 10.1182/blood-2002-04-1200 12676791
67. Bacher P, Heinrich F, Stervbo U, Nienen M, Vahldieck M, et al. (2016) Regulatory T Cell Specificity Directs Tolerance versus Allergy against Aeroantigens in Humans. Cell167 (4): 1067–1078.e16. doi: 10.1016/j.cell.2016.09.050 27773482
68. Kim HK, Cheng AG, Kim H-Y, Missiakas DM, Schneewind O, (2010) Nontoxigenic protein A vaccine for methicillin-resistant Staphylococcus aureus infections in mice. The Journal of experimental medicine207 (9): 1863–1870. doi: 10.1084/jem.20092514 20713595
69. McCormack G, O'Donoghue D, Baird A, (2001) In-vitro cyclosporin sensitivity of proliferating lymphocytes is predictive of in-vivo therapeutic response in ulcerative colitis. Alimentary pharmacology & therapeutics15 (5): 665–668.
70. Forsgren A, (1969) Protein A from Staphylococcus aureus. 8. Production of protein A by bacterial and L-forms of S. aureus. Acta pathologica et microbiologica Scandinavica75 (3): 481–490. 4979379
71. Schneewind O, Fowler A, Faull K, (1995) Structure of the cell wall anchor of surface proteins in Staphylococcus aureus. Science268 (5207): 103–106. 7701329
72. STAPLETON PD, TAYLOR PW, (2002) Methicillin resistance in Staphylococcus aureus: mechanisms and modulation. Science progress85 (Pt 1): 57–72. 11969119
73. Nguyen MT, Götz F, (2016) Lipoproteins of Gram-Positive Bacteria: Key Players in the Immune Response and Virulence. Microbiol. Mol. Biol. Rev. 80 (3): 891–903. Available: http://mmbr.asm.org/content/80/3/891.full. doi: 10.1128/MMBR.00028-16 27512100
74. Gómez MI, Lee A, Reddy B, Muir A, Soong G, et al. (2004) Staphylococcus aureus protein A induces airway epithelial inflammatory responses by activating TNFR1. Nature medicine10 (8): 842–848. doi: 10.1038/nm1079 15247912
75. Sedger LM, McDermott MF, (2014) TNF and TNF-receptors. From mediators of cell death and inflammation to therapeutic giants—past, present and future. Cytokine & growth factor reviews25 (4): 453–472.