Advertisement

Review of Mouse and Human Dendritic Cell Subsets

  • Elodie Segura
Protocol
Part of the Methods in Molecular Biology book series (MIMB, volume 1423)

Abstract

Dendritic cells are specialized antigen-presenting cells that initiate and orient immune responses. Numerous studies in mice and humans have shown that dendritic cells are heterogeneous and comprise several subsets that can be distinguished by their surface phenotype, ontogeny, and molecular signature. This review gives an overview of mouse and human dendritic cell subsets and their defining features and summarizes the current knowledge of dendritic cell subsets’ functional specialization in terms of antigen presentation.

Key words

Dendritic cells Subsets Human Mouse Antigen presentation 

Notes

Acknowledgments

This work is supported by INSERM, the European Research Council, LabEx DCBiol, and Ligue contre le Cancer .

References

  1. 1.
    Steinman RM, Nussenzweig MC (1980) Dendritic cells: features and functions. Immunol Rev 53:127–147CrossRefPubMedGoogle Scholar
  2. 2.
    Merad M, Sathe P, Helft J, Miller J, Mortha A (2013) The dendritic cell lineage: ontogeny and function of dendritic cells and their subsets in the steady state and the inflamed setting. Annu Rev Immunol 31:563–604CrossRefPubMedGoogle Scholar
  3. 3.
    Wilson NS, El-Sukkari D, Belz GT, Smith CM, Steptoe RJ, Heath WR, Shortman K, Villadangos JA (2003) Most lymphoid organ dendritic cell types are phenotypically and functionally immature. Blood 102(6):2187–2194CrossRefPubMedGoogle Scholar
  4. 4.
    Wilson NS, Young LJ, Kupresanin F, Naik SH, Vremec D, Heath WR, Akira S, Shortman K, Boyle J, Maraskovsky E, Belz GT, Villadangos JA (2008) Normal proportion and expression of maturation markers in migratory dendritic cells in the absence of germs or Toll-like receptor signaling. Immunol Cell Biol 86(2):200–205CrossRefPubMedGoogle Scholar
  5. 5.
    Reizis B, Bunin A, Ghosh HS, Lewis KL, Sisirak V (2011) Plasmacytoid dendritic cells: recent progress and open questions. Annu Rev Immunol 29:163–183CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Naik SH, Sathe P, Park HY, Metcalf D, Proietto AI, Dakic A, Carotta S, O’Keeffe M, Bahlo M, Papenfuss A, Kwak JY, Wu L, Shortman K (2007) Development of plasmacytoid and conventional dendritic cell subtypes from single precursor cells derived in vitro and in vivo. Nat Immunol 8(11):1217–1226CrossRefPubMedGoogle Scholar
  7. 7.
    Onai N, Obata-Onai A, Schmid MA, Ohteki T, Jarrossay D, Manz MG (2007) Identification of clonogenic common Flt3+M-CSFR+ plasmacytoid and conventional dendritic cell progenitors in mouse bone marrow. Nat Immunol 8(11):1207–1216CrossRefPubMedGoogle Scholar
  8. 8.
    Cisse B, Caton ML, Lehner M, Maeda T, Scheu S, Locksley R, Holmberg D, Zweier C, den Hollander NS, Kant SG, Holter W, Rauch A, Zhuang Y, Reizis B (2008) Transcription factor E2-2 is an essential and specific regulator of plasmacytoid dendritic cell development. Cell 135(1):37–48CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Ippolito GC, Dekker JD, Wang YH, Lee BK, Shaffer AL III, Lin J, Wall JK, Lee BS, Staudt LM, Liu YJ, Iyer VR, Tucker HO (2014) Dendritic cell fate is determined by BCL11A. Proc Natl Acad Sci U S A 111(11):E998–E1006CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Gilliet M, Cao W, Liu YJ (2008) Plasmacytoid dendritic cells: sensing nucleic acids in viral infection and autoimmune diseases. Nat Rev Immunol 8(8):594–606CrossRefPubMedGoogle Scholar
  11. 11.
    Lund JM, Linehan MM, Iijima N, Iwasaki A (2006) Cutting edge: plasmacytoid dendritic cells provide innate immune protection against mucosal viral infection in situ. J Immunol 177(11):7510–7514CrossRefPubMedGoogle Scholar
  12. 12.
    GeurtsvanKessel CH, Willart MA, van Rijt LS, Muskens F, Kool M, Baas C, Thielemans K, Bennett C, Clausen BE, Hoogsteden HC, Osterhaus AD, Rimmelzwaan GF, Lambrecht BN (2008) Clearance of influenza virus from the lung depends on migratory langerin+ CD11b− but not plasmacytoid dendritic cells. J Exp Med 205(7):1621–1634CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Swiecki M, Gilfillan S, Vermi W, Wang Y, Colonna M (2010) Plasmacytoid dendritic cell ablation impacts early interferon responses and antiviral NK and CD8(+) T cell accrual. Immunity 33(6):955–966CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Cervantes-Barragan L, Lewis KL, Firner S, Thiel V, Hugues S, Reith W, Ludewig B, Reizis B (2012) Plasmacytoid dendritic cells control T-cell response to chronic viral infection. Proc Natl Acad Sci U S A 109(8):3012–3017CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Liu K, Waskow C, Liu X, Yao K, Hoh J, Nussenzweig M (2007) Origin of dendritic cells in peripheral lymphoid organs of mice. Nat Immunol 8(6):578–583CrossRefPubMedGoogle Scholar
  16. 16.
    Miller JC, Brown BD, Shay T, Gautier EL, Jojic V, Cohain A, Pandey G, Leboeuf M, Elpek KG, Helft J, Hashimoto D, Chow A, Price J, Greter M, Bogunovic M, Bellemare-Pelletier A, Frenette PS, Randolph GJ, Turley SJ, Merad M, Gautier EL, Jakubzick C, Randolph GJ, Best AJ, Knell J, Goldrath A, Miller J, Brown B, Merad M, Jojic V, Koller D, Cohen N, Brennan P, Brenner M, Shay T, Regev A, Fletcher A, Elpek K, Bellemare-Pelletier A, Malhotra D, Turley S, Jianu R, Laidlaw D, Collins J, Narayan K, Sylvia K, Kang J, Gazit R, Rossi DJ, Kim F, Rao TN, Wagers A, Shinton SA, Hardy RR, Monach P, Bezman NA, Sun JC, Kim CC, Lanier LL, Heng T, Kreslavsky T, Painter M, Ericson J, Davis S, Mathis D, Benoist C (2012) Deciphering the transcriptional network of the dendritic cell lineage. Nat Immunol 13(9):888–899CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Satpathy AT, Kc W, Albring JC, Edelson BT, Kretzer NM, Bhattacharya D, Murphy TL, Murphy KM (2012) Zbtb46 expression distinguishes classical dendritic cells and their committed progenitors from other immune lineages. J Exp Med 209(6):1135–1152CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Meredith MM, Liu K, Darrasse-Jeze G, Kamphorst AO, Schreiber HA, Guermonprez P, Idoyaga J, Cheong C, Yao KH, Niec RE, Nussenzweig MC (2012) Expression of the zinc finger transcription factor zDC (Zbtb46, Btbd4) defines the classical dendritic cell lineage. J Exp Med 209(6):1153–1165CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Schraml BU, van Blijswijk J, Zelenay S, Whitney PG, Filby A, Acton SE, Rogers NC, Moncaut N, Carvajal JJ, Reis e Sousa C (2013) Genetic tracing via DNGR-1 expression history defines dendritic cells as a hematopoietic lineage. Cell 154(4):843–858CrossRefPubMedGoogle Scholar
  20. 20.
    Ginhoux F, Liu K, Helft J, Bogunovic M, Greter M, Hashimoto D, Price J, Yin N, Bromberg J, Lira SA, Stanley ER, Nussenzweig M, Merad M (2009) The origin and development of nonlymphoid tissue CD103+ DCs. J Exp Med 206(13):3115–3130CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Hildner K, Edelson BT, Purtha WE, Diamond M, Matsushita H, Kohyama M, Calderon B, Schraml BU, Unanue ER, Diamond MS, Schreiber RD, Murphy TL, Murphy KM (2008) Batf3 deficiency reveals a critical role for CD8alpha+ dendritic cells in cytotoxic T cell immunity. Science 322(5904):1097–1100CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Edelson BT, Kc W, Juang R, Kohyama M, Benoit LA, Klekotka PA, Moon C, Albring JC, Ise W, Michael DG, Bhattacharya D, Stappenbeck TS, Holtzman MJ, Sung SS, Murphy TL, Hildner K, Murphy KM (2010) Peripheral CD103+ dendritic cells form a unified subset developmentally related to CD8alpha+ conventional dendritic cells. J Exp Med 207(4):823–836CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Joffre OP, Segura E, Savina A, Amigorena S (2012) Cross-presentation by dendritic cells. Nat Rev Immunol 12(8):557–569CrossRefPubMedGoogle Scholar
  24. 24.
    Desch AN, Randolph GJ, Murphy K, Gautier EL, Kedl RM, Lahoud MH, Caminschi I, Shortman K, Henson PM, Jakubzick CV (2011) CD103+ pulmonary dendritic cells preferentially acquire and present apoptotic cell-associated antigen. J Exp Med 208(9):1789–1797CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Kashiwada M, Pham NL, Pewe LL, Harty JT, Rothman PB (2011) NFIL3/E4BP4 is a key transcription factor for CD8alpha(+) dendritic cell development. Blood 117(23):6193–6197CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Yamazaki C, Sugiyama M, Ohta T, Hemmi H, Hamada E, Sasaki I, Fukuda Y, Yano T, Nobuoka M, Hirashima T, Iizuka A, Sato K, Tanaka T, Hoshino K, Kaisho T (2013) Critical roles of a dendritic cell subset expressing a chemokine receptor, XCR1. J Immunol 190(12):6071–6082CrossRefPubMedGoogle Scholar
  27. 27.
    Igyarto BZ, Haley K, Ortner D, Bobr A, Gerami-Nejad M, Edelson BT, Zurawski SM, Malissen B, Zurawski G, Berman J, Kaplan DH (2011) Skin-resident murine dendritic cell subsets promote distinct and opposing antigen-specific T helper cell responses. Immunity 35(2):260–272CrossRefPubMedGoogle Scholar
  28. 28.
    Helft J, Manicassamy B, Guermonprez P, Hashimoto D, Silvin A, Agudo J, Brown BD, Schmolke M, Miller JC, Leboeuf M, Murphy KM, Garcia-Sastre A, Merad M (2012) Cross-presenting CD103+ dendritic cells are protected from influenza virus infection. J Clin Invest 122(11):4037–4047CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Wu L, D’Amico A, Winkel KD, Suter M, Lo D, Shortman K (1998) RelB is essential for the development of myeloid-related CD8alpha− dendritic cells but not of lymphoid-related CD8alpha+ dendritic cells. Immunity 9(6):839–847CrossRefPubMedGoogle Scholar
  30. 30.
    Suzuki S, Honma K, Matsuyama T, Suzuki K, Toriyama K, Akitoyo I, Yamamoto K, Suematsu T, Nakamura M, Yui K, Kumatori A (2004) Critical roles of interferon regulatory factor 4 in CD11bhighCD8alpha− dendritic cell development. Proc Natl Acad Sci U S A 101(24):8981–8986CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Schlitzer A, McGovern N, Teo P, Zelante T, Atarashi K, Low D, Ho AW, See P, Shin A, Wasan PS, Hoeffel G, Malleret B, Heiseke A, Chew S, Jardine L, Purvis HA, Hilkens CM, Tam J, Poidinger M, Stanley ER, Krug AB, Renia L, Sivasankar B, Ng LG, Collin M, Ricciardi-Castagnoli P, Honda K, Haniffa M, Ginhoux F (2013) IRF4 transcription factor-dependent CD11b+ dendritic cells in human and mouse control mucosal IL-17 cytokine responses. Immunity 38(5):970–983CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Dudziak D, Kamphorst AO, Heidkamp GF, Buchholz VR, Trumpfheller C, Yamazaki S, Cheong C, Liu K, Lee HW, Park CG, Steinman RM, Nussenzweig MC (2007) Differential antigen processing by dendritic cell subsets in vivo. Science 315(5808):107–111CrossRefPubMedGoogle Scholar
  33. 33.
    Vander Lugt B, Khan AA, Hackney JA, Agrawal S, Lesch J, Zhou M, Lee WP, Park S, Xu M, DeVoss J, Spooner CJ, Chalouni C, Delamarre L, Mellman I, Singh H (2014) Transcriptional programming of dendritic cells for enhanced MHC class II antigen presentation. Nat Immunol 15(2):161–167CrossRefPubMedGoogle Scholar
  34. 34.
    Persson EK, Uronen-Hansson H, Semmrich M, Rivollier A, Hagerbrand K, Marsal J, Gudjonsson S, Hakansson U, Reizis B, Kotarsky K, Agace WW (2013) IRF4 transcription-factor-dependent CD103(+)CD11b(+) dendritic cells drive mucosal T helper 17 cell differentiation. Immunity 38(5):958–969CrossRefPubMedGoogle Scholar
  35. 35.
    Gao Y, Nish SA, Jiang R, Hou L, Licona-Limon P, Weinstein JS, Zhao H, Medzhitov R (2013) Control of T helper 2 responses by transcription factor IRF4-dependent dendritic cells. Immunity 39(4):722–732CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Plantinga M, Guilliams M, Vanheerswynghels M, Deswarte K, Branco-Madeira F, Toussaint W, Vanhoutte L, Neyt K, Killeen N, Malissen B, Hammad H, Lambrecht BN (2013) Conventional and monocyte-derived CD11b(+) dendritic cells initiate and maintain T helper 2 cell-mediated immunity to house dust mite allergen. Immunity 38(2):322–335CrossRefPubMedGoogle Scholar
  37. 37.
    Williams JW, Tjota MY, Clay BS, Vander Lugt B, Bandukwala HS, Hrusch CL, Decker DC, Blaine KM, Fixsen BR, Singh H, Sciammas R, Sperling AI (2013) Transcription factor IRF4 drives dendritic cells to promote Th2 differentiation. Nat Commun 4:2990PubMedPubMedCentralGoogle Scholar
  38. 38.
    Hoeffel G, Wang Y, Greter M, See P, Teo P, Malleret B, Leboeuf M, Low D, Oller G, Almeida F, Choy SH, Grisotto M, Renia L, Conway SJ, Stanley ER, Chan JK, Ng LG, Samokhvalov IM, Merad M, Ginhoux F (2012) Adult Langerhans cells derive predominantly from embryonic fetal liver monocytes with a minor contribution of yolk sac-derived macrophages. J Exp Med 209(6):1167–1181CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Wang Y, Szretter KJ, Vermi W, Gilfillan S, Rossini C, Cella M, Barrow AD, Diamond MS, Colonna M (2012) IL-34 is a tissue-restricted ligand of CSF1R required for the development of Langerhans cells and microglia. Nat Immunol 13(8):753–760CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Greter M, Lelios I, Pelczar P, Hoeffel G, Price J, Leboeuf M, Kundig TM, Frei K, Ginhoux F, Merad M, Becher B (2012) Stroma-derived interleukin-34 controls the development and maintenance of Langerhans cells and the maintenance of microglia. Immunity 37(6):1050–1060CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Guilliams M, Ginhoux F, Jakubzick C, Naik SH, Onai N, Schraml BU, Segura E, Tussiwand R, Yona S (2014) Dendritic cells, monocytes and macrophages: a unified nomenclature based on ontogeny. Nat Rev Immunol 14(8):571–578CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Nakajima S, Igyarto BZ, Honda T, Egawa G, Otsuka A, Hara-Chikuma M, Watanabe N, Ziegler SF, Tomura M, Inaba K, Miyachi Y, Kaplan DH, Kabashima K (2012) Langerhans cells are critical in epicutaneous sensitization with protein antigen via thymic stromal lymphopoietin receptor signaling. J Allergy Clin Immunol 129(4):1048–1055, e1046CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Bursch LS, Rich BE, Hogquist KA (2009) Langerhans cells are not required for the CD8 T cell response to epidermal self-antigens. J Immunol 182(8):4657–4664CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Seneschal J, Jiang X, Kupper TS (2014) Langerin+ dermal DC, but not Langerhans cells, are required for effective CD8-mediated immune responses after skin scarification with vaccinia virus. J Invest Dermatol 134(3):686–694CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Segura E, Amigorena S (2013) Inflammatory dendritic cells in mice and humans. Trends Immunol 34(9):440–445CrossRefPubMedGoogle Scholar
  46. 46.
    Greter M, Helft J, Chow A, Hashimoto D, Mortha A, Agudo-Cantero J, Bogunovic M, Gautier EL, Miller J, Leboeuf M, Lu G, Aloman C, Brown BD, Pollard JW, Xiong H, Randolph GJ, Chipuk JE, Frenette PS, Merad M (2012) GM-CSF controls nonlymphoid tissue dendritic cell homeostasis but is dispensable for the differentiation of inflammatory dendritic cells. Immunity 36(6):1031–1046CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Bogunovic M, Ginhoux F, Helft J, Shang L, Hashimoto D, Greter M, Liu K, Jakubzick C, Ingersoll MA, Leboeuf M, Stanley ER, Nussenzweig M, Lira SA, Randolph GJ, Merad M (2009) Origin of the lamina propria dendritic cell network. Immunity 31(3):513–525CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Varol C, Vallon-Eberhard A, Elinav E, Aychek T, Shapira Y, Luche H, Fehling HJ, Hardt WD, Shakhar G, Jung S (2009) Intestinal lamina propria dendritic cell subsets have different origin and functions. Immunity 31(3):502–512CrossRefPubMedGoogle Scholar
  49. 49.
    Langlet C, Tamoutounour S, Henri S, Luche H, Ardouin L, Gregoire C, Malissen B, Guilliams M (2012) CD64 expression distinguishes monocyte-derived and conventional dendritic cells and reveals their distinct role during intramuscular immunization. J Immunol 188(4):1751–1760CrossRefPubMedGoogle Scholar
  50. 50.
    Tamoutounour S, Guilliams M, Montanana Sanchis F, Liu H, Terhorst D, Malosse C, Pollet E, Ardouin L, Luche H, Sanchez C, Dalod M, Malissen B, Henri S (2013) Origins and functional specialization of macrophages and of conventional and monocyte-derived dendritic cells in mouse skin. Immunity 39(5):925–938CrossRefPubMedGoogle Scholar
  51. 51.
    Zigmond E, Varol C, Farache J, Elmaliah E, Satpathy AT, Friedlander G, Mack M, Shpigel N, Boneca IG, Murphy KM, Shakhar G, Halpern Z, Jung S (2012) Ly6C(hi) monocytes in the inflamed colon give rise to proinflammatory effector cells and migratory antigen-presenting cells. Immunity 37(6):1076–1090CrossRefPubMedGoogle Scholar
  52. 52.
    Chakarov S, Fazilleau N (2014) Monocyte-derived dendritic cells promote T follicular helper cell differentiation. EMBO Mol Med 6(5):590–603PubMedPubMedCentralGoogle Scholar
  53. 53.
    Wakim LM, Waithman J, van Rooijen N, Heath WR, Carbone FR (2008) Dendritic cell-induced memory T cell activation in nonlymphoid tissues. Science 319(5860):198–202CrossRefPubMedGoogle Scholar
  54. 54.
    Iijima N, Mattei LM, Iwasaki A (2011) Recruited inflammatory monocytes stimulate antiviral Th1 immunity in infected tissue. Proc Natl Acad Sci U S A 108(1):284–289CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Aldridge JR Jr, Moseley CE, Boltz DA, Negovetich NJ, Reynolds C, Franks J, Brown SA, Doherty PC, Webster RG, Thomas PG (2009) TNF/iNOS-producing dendritic cells are the necessary evil of lethal influenza virus infection. Proc Natl Acad Sci U S A 106(13):5306–5311CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Ziegler-Heitbrock L, Ancuta P, Crowe S, Dalod M, Grau V, Hart DN, Leenen PJ, Liu YJ, MacPherson G, Randolph GJ, Scherberich J, Schmitz J, Shortman K, Sozzani S, Strobl H, Zembala M, Austyn JM, Lutz MB (2010) Nomenclature of monocytes and dendritic cells in blood. Blood 116(16):e74–e80CrossRefPubMedGoogle Scholar
  57. 57.
    Segura E, Valladeau-Guilemond J, Donnadieu MH, Sastre-Garau X, Soumelis V, Amigorena S (2012) Characterization of resident and migratory dendritic cells in human lymph nodes. J Exp Med 209(4):653–660CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Nizzoli G, Krietsch J, Weick A, Steinfelder S, Facciotti F, Gruarin P, Bianco A, Steckel B, Moro M, Crosti MC, Romagnani C, Stolzel K, Torretta S, Pignataro L, Scheibenbogen C, Neddermann P, Defrancesco 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(6):932–942CrossRefPubMedGoogle Scholar
  59. 59.
    Segura E, Durand M, Amigorena S (2013) Similar antigen cross-presentation capacity and phagocytic functions in all freshly isolated human lymphoid organ-resident dendritic cells. J Exp Med 210(5):1035–1047CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Martinez-Cingolani C, Grandclaudon M, Jeanmougin M, Jouve M, Zollinger R, Soumelis V (2014) Human blood BDCA-1 dendritic cells differentiate into Langerhans-like cells with thymic stromal lymphopoietin and TGF-beta. Blood 124(15):2411–2420CrossRefPubMedGoogle Scholar
  61. 61.
    Haniffa M, Shin A, Bigley V, McGovern N, Teo P, See P, Wasan PS, Wang XN, Malinarich F, Malleret B, Larbi A, Tan P, Zhao H, Poidinger M, Pagan S, Cookson S, Dickinson R, Dimmick I, Jarrett RF, Renia L, Tam J, Song C, Connolly J, Chan JK, Gehring A, Bertoletti A, Collin M, Ginhoux F (2012) Human tissues contain CD141(hi) cross-presenting dendritic cells with functional homology to mouse CD103(+) nonlymphoid dendritic cells. Immunity 37(1):60–73CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Morandi B, Bonaccorsi I, Mesiti M, Conte R, Carrega P, Costa G, Iemmo R, Martini S, Ferrone S, Cantoni C, Mingari MC, Moretta L, Ferlazzo G (2013) Characterization of human afferent lymph dendritic cells from seroma fluids. J Immunol 191(9):4858–4866CrossRefPubMedGoogle Scholar
  63. 63.
    Cella M, Jarrossay D, Facchetti F, Alebardi O, Nakajima H, Lanzavecchia A, Colonna M (1999) Plasmacytoid monocytes migrate to inflamed lymph nodes and produce large amounts of type I interferon. Nat Med 5(8):919–923CrossRefPubMedGoogle Scholar
  64. 64.
    Pulendran B, Banchereau J, Burkeholder S, Kraus E, Guinet E, Chalouni C, Caron D, Maliszewski C, Davoust J, Fay J, Palucka K (2000) Flt3-ligand and granulocyte colony-stimulating factor mobilize distinct human dendritic cell subsets in vivo. J Immunol 165(1):566–572CrossRefPubMedGoogle Scholar
  65. 65.
    Nagasawa M, Schmidlin H, Hazekamp MG, Schotte R, Blom B (2008) Development of human plasmacytoid dendritic cells depends on the combined action of the basic helix-loop-helix factor E2-2 and the Ets factor Spi-B. Eur J Immunol 38(9):2389–2400CrossRefPubMedGoogle Scholar
  66. 66.
    Cella M, Facchetti F, Lanzavecchia A, Colonna M (2000) Plasmacytoid dendritic cells activated by influenza virus and CD40L drive a potent TH1 polarization. Nat Immunol 1(4):305–310CrossRefPubMedGoogle Scholar
  67. 67.
    Manches O, Munn D, Fallahi A, Lifson J, Chaperot L, Plumas J, Bhardwaj N (2008) HIV-activated human plasmacytoid DCs induce Tregs through an indoleamine 2,3-dioxygenase-dependent mechanism. J Clin Invest 118(10):3431–3439CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Palomares O, Ruckert B, Jartti T, Kucuksezer UC, Puhakka T, Gomez E, Fahrner HB, Speiser A, Jung A, Kwok WW, Kalogjera L, Akdis M, Akdis CA (2012) Induction and maintenance of allergen-specific FOXP3+ Treg cells in human tonsils as potential first-line organs of oral tolerance. J Allergy Clin Immunol 129(2):510–520, 520 e511–519CrossRefPubMedGoogle Scholar
  69. 69.
    Mittag D, Proietto AI, Loudovaris T, Mannering SI, Vremec D, Shortman K, Wu L, Harrison LC (2011) Human dendritic cell subsets from spleen and blood are similar in phenotype and function but modified by donor health status. J Immunol 186(11):6207–6217CrossRefPubMedGoogle Scholar
  70. 70.
    Tel J, Schreibelt G, Sittig SP, Mathan TS, Buschow SI, Cruz LJ, Lambeck AJ, Figdor CG, de Vries IJ (2013) Human plasmacytoid dendritic cells efficiently cross-present exogenous Ags to CD8+ T cells despite lower Ag uptake than myeloid dendritic cell subsets. Blood 121(3):459–467CrossRefPubMedGoogle Scholar
  71. 71.
    Hoeffel G, Ripoche AC, Matheoud D, Nascimbeni M, Escriou N, Lebon P, Heshmati F, Guillet JG, Gannage M, Caillat-Zucman S, Casartelli N, Schwartz O, De la Salle H, Hanau D, Hosmalin A, Maranon C (2007) Antigen crosspresentation by human plasmacytoid dendritic cells. Immunity 27(3):481–492CrossRefPubMedGoogle Scholar
  72. 72.
    Di Pucchio T, Chatterjee B, Smed-Sorensen A, Clayton S, Palazzo A, Montes M, Xue Y, Mellman I, Banchereau J, Connolly JE (2008) Direct proteasome-independent cross-presentation of viral antigen by plasmacytoid dendritic cells on major histocompatibility complex class I. Nat Immunol 9(5):551–557CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Lui G, Manches O, Angel J, Molens JP, Chaperot L, Plumas J (2009) Plasmacytoid dendritic cells capture and cross-present viral antigens from influenza-virus exposed cells. PLoS One 4(9):e7111CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Dzionek A, Fuchs A, Schmidt P, Cremer S, Zysk M, Miltenyi S, Buck DW, Schmitz J (2000) BDCA-2, BDCA-3, and BDCA-4: three markers for distinct subsets of dendritic cells in human peripheral blood. J Immunol 165(11):6037–6046CrossRefPubMedGoogle Scholar
  75. 75.
    Summers KL, Hock BD, McKenzie JL, Hart DN (2001) Phenotypic characterization of five dendritic cell subsets in human tonsils. Am J Pathol 159(1):285–295CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    McIlroy D, Troadec C, Grassi F, Samri A, Barrou B, Autran B, Debre P, Feuillard J, Hosmalin A (2001) Investigation of human spleen dendritic cell phenotype and distribution reveals evidence of in vivo activation in a subset of organ donors. Blood 97(11):3470–3477CrossRefPubMedGoogle Scholar
  77. 77.
    Yu CI, Becker C, Wang Y, Marches F, Helft J, Leboeuf M, Anguiano E, Pourpe S, Goller K, Pascual V, Banchereau J, Merad M, Palucka K (2013) Human CD1c(+) dendritic cells drive the differentiation of CD103(+) CD8(+) mucosal effector T cells via the cytokine TGF-beta. Immunity 38(4):818–830CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Watchmaker PB, Lahl K, Lee M, Baumjohann D, Morton J, Kim SJ, Zeng R, Dent A, Ansel KM, Diamond B, Hadeiba H, Butcher EC (2014) Comparative transcriptional and functional profiling defines conserved programs of intestinal DC differentiation in humans and mice. Nat Immunol 15(1):98–108CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Robbins SH, Walzer T, Dembele D, Thibault C, Defays A, Bessou G, Xu H, Vivier E, Sellars M, Pierre P, Sharp FR, Chan S, Kastner P, Dalod M (2008) Novel insights into the relationships between dendritic cell subsets in human and mouse revealed by genome-wide expression profiling. Genome Biol 9(1):R17CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Crozat K, Guiton R, Contreras V, Feuillet V, Dutertre CA, Ventre E, Vu Manh TP, Baranek T, Storset AK, Marvel J, Boudinot P, Hosmalin A, Schwartz-Cornil I, Dalod M (2010) The XC chemokine receptor 1 is a conserved selective marker of mammalian cells homologous to mouse CD8alpha+ dendritic cells. J Exp Med 207(6):1283–1292CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Poulin LF, Reyal Y, Uronen-Hansson H, Schraml B, Sancho D, Murphy KM, Hakansson UK, Moita LF, Agace WW, Bonnet D, Reis ESC (2012) DNGR-1 is a specific and universal marker of mouse and human Batf3-dependent dendritic cells in lymphoid and non-lymphoid tissues. Blood 119(25):6052–6062CrossRefPubMedGoogle Scholar
  82. 82.
    Hambleton S, Salem S, Bustamante J, Bigley V, Boisson-Dupuis S, Azevedo J, Fortin A, Haniffa M, Ceron-Gutierrez L, Bacon CM, Menon G, Trouillet C, McDonald D, Carey P, Ginhoux F, Alsina L, Zumwalt TJ, Kong XF, Kumararatne D, Butler K, Hubeau M, Feinberg J, Al-Muhsen S, Cant A, Abel L, Chaussabel D, Doffinger R, Talesnik E, Grumach A, Duarte A, Abarca K, Moraes-Vasconcelos D, Burk D, Berghuis A, Geissmann F, Collin M, Casanova JL, Gros P (2011) IRF8 mutations and human dendritic-cell immunodeficiency. N Engl J Med 365(2):127–138CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Duluc D, Gannevat J, Anguiano E, Zurawski S, Carley M, Boreham M, Stecher J, Dullaers M, Banchereau J, Oh S (2013) Functional diversity of human vaginal APC subsets in directing T-cell responses. Mucosal Immunol 6(3):626–638CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Klechevsky E, Morita R, Liu M, Cao Y, Coquery S, Thompson-Snipes L, Briere F, Chaussabel D, Zurawski G, Palucka AK, Reiter Y, Banchereau J, Ueno H (2008) Functional specializations of human epidermal Langerhans cells and CD14+ dermal dendritic cells. Immunity 29(3):497–510CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Nestle FO, Zheng XG, Thompson CB, Turka LA, Nickoloff BJ (1993) Characterization of dermal dendritic cells obtained from normal human skin reveals phenotypic and functionally distinctive subsets. J Immunol 151(11):6535–6545PubMedGoogle Scholar
  86. 86.
    Bigley V, Haniffa M, Doulatov S, Wang XN, Dickinson R, McGovern N, Jardine L, Pagan S, Dimmick I, Chua I, Wallis J, Lordan J, Morgan C, Kumararatne DS, Doffinger R, van der Burg M, van Dongen J, Cant A, Dick JE, Hambleton S, Collin M (2011) The human syndrome of dendritic cell, monocyte, B and NK lymphoid deficiency. J Exp Med 208(2):227–234CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Polak ME, Newell L, Taraban VY, Pickard C, Healy E, Friedmann PS, Al-Shamkhani A, Ardern-Jones MR (2012) CD70-CD27 interaction augments CD8+ T-cell activation by human epidermal Langerhans cells. J Invest Dermatol 132(6):1636–1644CrossRefPubMedGoogle Scholar
  88. 88.
    Banchereau J, Thompson-Snipes L, Zurawski S, Blanck JP, Cao Y, Clayton S, Gorvel JP, Zurawski G, Klechevsky E (2012) The differential production of cytokines by human Langerhans cells and dermal CD14(+) DCs controls CTL priming. Blood 119(24):5742–5749CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Wollenberg A, Mommaas M, Oppel T, Schottdorf EM, Gunther S, Moderer M (2002) Expression and function of the mannose receptor CD206 on epidermal dendritic cells in inflammatory skin diseases. J Invest Dermatol 118(2):327–334CrossRefPubMedGoogle Scholar
  90. 90.
    Segura E, Touzot M, Bohineust A, Cappuccio A, Chiocchia G, Hosmalin A, Dalod M, Soumelis V, Amigorena S (2013) Human inflammatory dendritic cells induce Th17 cell differentiation. Immunity 38(2):336–348CrossRefPubMedGoogle Scholar
  91. 91.
    Guttman-Yassky E, Lowes MA, Fuentes-Duculan J, Whynot J, Novitskaya I, Cardinale I, Haider A, Khatcherian A, Carucci JA, Bergman R, Krueger JG (2007) Major differences in inflammatory dendritic cells and their products distinguish atopic dermatitis from psoriasis. J Allergy Clin Immunol 119(5):1210–1217CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  1. 1.Institut CurieParis Cedex 05France
  2. 2.INSERM U932Paris Cedex 05France

Personalised recommendations