BDCA1-positive dendritic cells (DCs) represent a unique human myeloid DC subset that induces innate and adaptive immune responses to Staphylococcus aureus infection

Infection and Immunity

Volumn 82, Issue 11, 2014, Pages 4466-4476

  Jin, Jun O ^a   Zhang, Wei ^a   Du, Jiang yuan ^a   Yu, Qing ^a,b  

^a FUDAN UNIVERSITY   (China)

^b FORSYTH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 12P40; INTERLEUKIN 12P70; INTERLEUKIN 6; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MESSENGER RNA; MYELOID DIFFERENTIATION FACTOR 88; SCAVENGER RECEPTOR A; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; ANTIBODY; CD1 ANTIGEN; CD1C PROTEIN, HUMAN; GLYCOPROTEIN; TLR2 PROTEIN, HUMAN;

ADAPTIVE IMMUNITY; ARTICLE; BACTERIAL IMMUNITY; BDCA1+ MYELOID DENDRITIC CELL; BDCA3+ MYELOID DENDRITIC CELL; CD16+ MYELOID DENDRITIC CELL; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL PHAGOCYTOSIS; CELLULAR DISTRIBUTION; CYTOKINE PRODUCTION; CYTOPLASM; HUMAN; HUMAN CELL; INNATE IMMUNITY; LYMPHOCYTE PROLIFERATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MYELOID DENDRITIC CELL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION; T LYMPHOCYTE ACTIVATION; UPREGULATION; ADULT; CELL CULTURE; CLASSIFICATION; DENDRITIC CELL; DRUG EFFECTS; FEMALE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; MALE; METABOLISM; PHYSIOLOGY; YOUNG ADULT;

ADAPTIVE IMMUNITY; ADULT; ANTIBODIES; ANTIGENS, CD1; CELLS, CULTURED; DENDRITIC CELLS; FEMALE; GENE EXPRESSION REGULATION; GLYCOPROTEINS; HUMANS; IMMUNITY, INNATE; MALE; SCAVENGER RECEPTORS, CLASS A; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS; TOLL-LIKE RECEPTOR 2; YOUNG ADULT;

EID: 84907960586     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01851-14     Document Type: Article

References (48)

1. Laupland KB. 2013. Incidence of bloodstream infection: a review of population-based studies. Clin. Microbiol. Infect. 19:492-500. http://dx.doi.org/10.1111/1469-0691.12144.
2. Lowy FD. 1998. Staphylococcus aureus infections. N. Engl. J. Med. 339:520-532. http://dx.doi.org/10.1056/NEJM199808203390806.
3. Kern WV. 2010. Management of Staphylococcus aureus bacteremia and endocarditis: progresses and challenges. Curr. Opin. Infect. Dis. 23:346-358. http://dx.doi.org/10.1097/QCO.0b013e32833bcc8a.
4. Thwaites GE, Edgeworth JD, Gkrania-Klotsas E, Kirby A, Tilley R, Torok ME, Walker S, Wertheim HF, Wilson P, Llewelyn MJ, UK Clinical Infection Research Group. 2011. Clinical management of Staphylococcus aureus bacteraemia. Lancet Infect. Dis. 11:208-222. http://dx.doi.org/10.1016/S1473-3099(10)70285-1.
5. Garzoni C, Vergidis P, AST Infectious Diseases Community of Practice. 2013. Methicillin-resistant, vancomycin-intermediate and vancomycinresistant Staphylococcus aureus infections in solid organ transplantation.Am. J. Transplant. 13(Suppl 4):50-58. http://dx.doi.org/10.1111/ajt.12098.
6. Furuno JP, Johnson JK, Schweizer ML, Uche A, Stine OC, Shurland SM, Forrest GN. 2011. Community-associated methicillin-resistant Staphylococcus aureus bacteremia and endocarditis among HIV patients: a cohort study. BMC Infect. Dis. 11:298. http://dx.doi.org/10.1186/1471-2334-11-298.
7. Levy MM, Fink MP, Marshall JC, Abraham E, Angus D, Cook D, Cohen J, Opal SM, Vincent JL, Ramsay G, SCCM/ESICM/ACCP/ATS/SIS. 2003. 2001 SCCM/ESICM/ACCP/ATS/SIS International Sepsis Definitions Conference. Crit. Care Med. 31:1250-1256. http://dx.doi.org/10.1097/01.CCM.0000050454.01978.3B.
8. Rasmussen RV, Fowler VG, Jr, Skov R, Bruun NE. 2011. Future challenges and treatment of Staphylococcus aureus bacteremia with emphasis on MRSA. Future Microbiol. 6:43-56. http://dx.doi.org/10.2217/fmb.10.155.
9. Banchereau J, Steinman RM. 1998. Dendritic cells and the control of immunity. Nature 392:245-252. http://dx.doi.org/10.1038/32588.
10. Banchereau J, Palucka AK. 2005. Dendritic cells as therapeutic vaccines against cancer. Nat. Rev. Immunol. 5:296-306. http://dx.doi.org/10.1038/nri1592.
11. Hart DN. 1997. Dendritic cells: unique leukocyte populations which control the primary immune response. Blood 90:3245-3287.
12. MacDonald KP, Munster DJ, Clark GJ, Dzionek A, Schmitz J, Hart DN. 2002. Characterization of human blood dendritic cell subsets. Blood 100:4512-4520. http://dx.doi.org/10.1182/blood-2001-11-0097.
13. Vulink A, Radford KJ, Melief C, Hart DN. 2008. Dendritic cells in cancer immunotherapy. Adv. Cancer Res. 99:363-407. http://dx.doi.org/10.1016/S0065-230X(07)99006-5.
14. Garcia F, Climent N, Assoumou L, Gil C, Gonzalez N, Alcami J, Leon A, Romeu J, Dalmau J, Martinez-Picado J, Lifson J, Autran B, Costagliola D, Clotet B, Gatell JM, Plana M, Gallart T, DCV2/MANON07 AIDS Vaccine Research Objective Study Group. 2011. A therapeutic dendritic cell-based vaccine for HIV-1 infection. J. Infect. Dis. 203:473-478. http://dx.doi.org/10.1093/infdis/jiq077.
15. Schindler D, Gutierrez MG, Beineke A, Rauter Y, Rohde M, Foster S, Goldmann O, Medina E. 2012. Dendritic cells are central coordinators of the host immune response to Staphylococcus aureus bloodstream infection. Am. J. Pathol. 181:1327-1337. http://dx.doi.org/10.1016/j.ajpath.2012.06.039.
16. Kassianos AJ, Jongbloed SL, Hart DN, Radford KJ. 2010. Isolation of human blood DC subtypes. Methods Mol. Biol. 595:45-54. http://dx.doi.org/10.1007/978-1-60761-421-0_3.
17. Bachem A, Guttler S, Hartung E, Ebstein F, Schaefer M, Tannert A, Salama A, Movassaghi K, Opitz C, Mages HW, Henn V, Kloetzel PM, Gurka S, Kroczek RA. 2010. Superior antigen cross-presentation and XCR1 expression define human CD11c+CD141+cells as homologues of mouse CD8+ dendritic cells. J. Exp. Med. 207:1273-1281. http://dx.doi.org/10.1084/jem.20100348.
18. Jongbloed SL, Kassianos AJ, McDonald KJ, Clark GJ, Ju X, Angel CE, Chen CJ, Dunbar PR, Wadley RB, Jeet V, Vulink AJ, Hart DN, Radford KJ. 2010. Human CD141+(BDCA-3)+dendritic cells (DCs) represent a unique myeloid DC subset that cross-presents necrotic cell antigens. J. Exp. Med. 207:1247-1260. http://dx.doi.org/10.1084/jem.20092140.
19. Poulin LF, Salio M, Griessinger E, Anjos-Afonso F, Craciun L, Chen JL, Keller AM, Joffre O, Zelenay S, Nye E, Le Moine A, Faure F, Donckier V, Sancho D, Cerundolo V, Bonnet D, Reis e Sousa C. 2010. Characterization of human DNGR-1+ BDCA3+ leukocytes as putative equivalents of mouse CD8alpha+ dendritic cells. J. Exp. Med. 207:1261-1271. http://dx.doi.org/10.1084/jem.20092618.
20. Jin JO, Park HY, Xu Q, Park JI, Zvyagintseva T, Stonik VA, Kwak JY. 2009. Ligand of scavenger receptor class A indirectly induces maturation of human blood dendritic cells via production of tumor necrosis factoralpha. Blood 113:5839-5847. http://dx.doi.org/10.1182/blood-2008-10-184796.
21. Takeda K, Akira S. 2004. TLR signaling pathways. Semin. Immunol. 16:3-9. http://dx.doi.org/10.1016/j.smim.2003.10.003.
22. Schmaler M, Jann NJ, Ferracin F, Landmann R. 2011. T and B cells are not required for clearing Staphylococcus aureus in systemic infection despite a strong TLR2-MyD88-dependent T cell activation. J. Immunol. 186:443-452. http://dx.doi.org/10.4049/jimmunol.1001407.
23. Ip WK, Sokolovska A, Charriere GM, Boyer L, Dejardin S, Cappillino MP, Yantosca LM, Takahashi K, Moore KJ, Lacy-Hulbert A, Stuart LM. 2010. Phagocytosis and phagosome acidification are required for pathogen processing and MyD88-dependent responses to Staphylococcus aureus. J. Immunol. 184:7071-7081. http://dx.doi.org/10.4049/jimmunol.1000110.
24. Vremec D, Pooley J, Hochrein H, Wu L, Shortman K. 2000. CD4 and CD8 expression by dendritic cell subtypes in mouse thymus and spleen. J. Immunol. 164:2978-2986. http://dx.doi.org/10.4049/jimmunol.164.6.2978.
25. Villadangos JA, Schnorrer P. 2007. Intrinsic and cooperative antigenpresenting functions of dendritic-cell subsets in vivo. Nat. Rev. Immunol. 7:543-555. http://dx.doi.org/10.1038/nri2103.
26. Nizzoli G, Krietsch J, Weick A, Steinfelder S, Facciotti F, Gruarin P, Bianco A, Steckel B, Moro M, Crosti M, Romagnani C, Stolzel K, Torretta S, Pignataro L, Scheibenbogen C, Neddermann P, De Francesco R, Abrignani S, Geginat J. 2013. Human CD1c+ dendritic cells secrete high levels of IL-12 and potently prime cytotoxic T-cell responses. Blood 122:932-942. http://dx.doi.org/10.1182/blood-2013-04-495424.
27. Segura E, Durand M, Amigorena S. 2013. Similar antigen crosspresentation capacity and phagocytic functions in all freshly isolated human lymphoid organ-resident dendritic cells. J. Exp. Med. 210:1035-1047. http://dx.doi.org/10.1084/jem.20121103.
28. Burgdorf S, Kurts C. 2008. Endocytosis mechanisms and the cell biology of antigen presentation. Curr. Opin. Immunol. 20:89-95. http://dx.doi.org/10.1016/j.coi.2007.12.002.
29. Parker D, Prince A. 2012. Staphylococcus aureus induces type I IFN signaling in dendritic cells via TLR9. J. Immunol. 189:4040-4046. http://dx.doi.org/10.4049/jimmunol.1201055.
30. Carrion J, Scisci E, Miles B, Sabino GJ, Zeituni AE, Gu Y, Bear A, Genco CA, Brown DL, Cutler CW. 2012. Microbial carriage state of peripheral blood dendritic cells (DCs) in chronic periodontitis influences DC differentiation, atherogenic potential. J. Immunol. 189:3178-3187. http://dx.doi.org/10.4049/jimmunol.1201053.
31. Gordon S. 2002. Pattern recognition receptors: doubling up for the innate immune response. Cell 111:927-930. http://dx.doi.org/10.1016/S0092-8674(02)01201-1.
32. Villadangos JA, Shortman K. 2010. Found in translation: the human equivalent of mouse CD8+ dendritic cells. J. Exp. Med. 207:1131-1134. http://dx.doi.org/10.1084/jem.20100985.
33. Yimin Kohanawa M, Zhao S, Ozaki M, Haga S, Nan G, Kuge Y, Tamaki N. 2013. Contribution of Toll-like receptor 2 to the innate response against Staphylococcus aureus infection in mice. PLoS One 8:e74287. http://dx.doi.org/10.1371/journal.pone.0074287.
34. Takeuchi O, Hoshino K, Akira S. 2000. Cutting edge: TLR2-deficient and MyD88-deficient mice are highly susceptible to Staphylococcus aureus infection. J. Immunol. 165:5392-5396. http://dx.doi.org/10.4049/jimmunol.165.10.5392.
35. Blander JM, Medzhitov R. 2004. Regulation of phagosome maturation by signals from Toll-like receptors. Science 304:1014-1018. http://dx.doi.org/10.1126/science.1096158.
36. Mullaly SC, Kubes P. 2006. The role of TLR2 in vivo following challenge with Staphylococcus aureus and prototypic ligands. J. Immunol. 177:8154-8163. http://dx.doi.org/10.4049/jimmunol.177.11.8154.
37. Amiel E, Alonso A, Uematsu S, Akira S, Poynter ME, Berwin B. 2009. Pivotal advance: Toll-like receptor regulation of scavenger receptor-A-mediated phagocytosis. J. Leukoc. Biol. 85:595-605. http://dx.doi.org/10.1189/jlb.1008631.
38. Amiel E, Nicholson-Dykstra S, Walters JJ, Higgs H, Berwin B. 2007. Scavenger receptor-A functions in phagocytosis of E. coli by bone marrow dendritic cells. Exp. Cell Res. 313:1438-1448. http://dx.doi.org/10.1016/j.yexcr.2007.02.011.
39. Blanchet C, Jouvion G, Fitting C, Cavaillon JM, Adib-Conquy M. 2014. Protective or deleterious role of scavenger receptors SR-A and CD36 on host resistance to Staphylococcus aureus depends on the site of infection. PLoS One 9:e87927. http://dx.doi.org/10.1371/journal.pone.0087927.
40. Peiser L, Gough PJ, Kodama T, Gordon S. 2000. Macrophage class A scavenger receptor-mediated phagocytosis of Escherichia coli: role of cell heterogeneity, microbial strain, and culture conditions in vitro. Infect. Immun. 68:1953-1963. http://dx.doi.org/10.1128/IAI.68.4.1953-1963.2000.
41. Sever-Chroneos Z, Krupa A, Davis J, Hasan M, Yang CH, Szeliga J, Herrmann M, Hussain M, Geisbrecht BV, Kobzik L, Chroneos ZC. 2011. Surfactant protein A (SP-A)-mediated clearance of Staphylococcus aureus involves binding of SP-A to the staphylococcal adhesin eap and the macrophage receptors SP-A receptor 210 and scavenger receptor class A. J. Biol. Chem. 286:4854-4870. http://dx.doi.org/10.1074/jbc.M110.125567.
42. Xu WY, Wang L, Wang HM, Wang YQ, Liang YF, Zhao TT, Wu YZ. 2007. TLR2 and TLR4 agonists synergistically up-regulate SR-A in RAW264.7 through p38. Mol. Immunol. 44:2315-2323. http://dx.doi.org/10.1016/j.molimm.2006.11.013.
43. Hoebe K, Georgel P, Rutschmann S, Du X, Mudd S, Crozat K, Sovath S, Shamel L, Hartung T, Zahringer U, Beutler B. 2005. CD36 is a sensor of diacylglycerides. Nature 433:523-527. http://dx.doi.org/10.1038/nature03253.
44. Shiratsuchi A, Mori T, Sakurai K, Nagaosa K, Sekimizu K, Lee BL, Nakanishi Y. 2012. Independent recognition of Staphylococcus aureus by two receptors for phagocytosis in Drosophila. J. Biol. Chem. 287:21663-21672. http://dx.doi.org/10.1074/jbc.M111.333807.
45. Gomez MI, Lee A, Reddy B, Muir A, Soong G, Pitt A, Cheung A, Prince A. 2004. Staphylococcus aureus protein A induces airway epithelial inflammatory responses by activating TNFR1. Nat. Med. 10:842-848. http://dx.doi.org/10.1038/nm1079.
46. Fournier B, Philpott DJ. 2005. Recognition of Staphylococcus aureus by the innate immune system. Clin. Microbiol. Rev. 18:521-540. http://dx.doi.org/10.1128/CMR.18.3.521-540.2005.
47. Azuma K, Ishihara T, Nakamoto H, Amaha T, Osaki T, Tsuka T, Imagawa T, Minami S, Takashima O, Ifuku S, Morimoto M, Saimoto H, Kawamoto H, Okamoto Y. 2012. Effects of oral administration of fucoidan extracted from Cladosiphon okamuranus on tumor growth and survival time in a tumor-bearing mouse model. Mar. Drugs 10:2337-2348. http://dx.doi.org/10.3390/md10102337.
48. Geiger-Maor A, Levi I, Even-Ram S, Smith Y, Bowdish DM, Nussbaum G, Rachmilewitz J. 2012. Cells exposed to sublethal oxidative stress selectively attract monocytes/macrophages via scavenger receptors and MyD88-mediated signaling. J. Immunol. 188:1234-1244. http://dx.doi.org/10.4049/jimmunol.1101740.