Intradermal Immunization pp 1-24

Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 351) | Cite as

Understanding the Murine Cutaneous Dendritic Cell Network to Improve Intradermal Vaccination Strategies

Chapter

Abstract

Dendritic cells (DCs) form a heterogeneous group of antigen presenting cells that play different roles in tissue immunity. Recent studies have revealed the presence of distinct DC populations in murine skin, highlighting the complexity of the cutaneous DC network. In this review, we will define the major DC subsets that populate the different layers of the skin, focusing on their origin and the mechanisms controlling their homeostasis. We will also review recent evidence underlining the functional specialization of dermal DC subsets and its relevance in the design of novel vaccine approaches.

References

  1. Allan RS, Smith CM, Belz GT, van Lint AL, Wakim LM, Heath WR, Carbone FR (2003) Epidermal viral immunity induced by CD8alpha+ dendritic cells but not by Langerhans cells. Science 301:1925–1928PubMedCrossRefGoogle Scholar
  2. Baca-Estrada ME, Ewen C, Mahony D, Babiuk LA, Wilkie D, Foldvari M (2002) The haemopoietic growth factor, Flt3L, alters the immune response induced by transcutaneous immunization. Immunology 107:69–76PubMedCrossRefGoogle Scholar
  3. Banchereau J, Briere F, Caux C, Davoust J, Lebecque S, Liu YJ, Pulendran B, Palucka K (2000) Immunobiology of dendritic cells. Annu Rev Immunol 18:767–811PubMedCrossRefGoogle Scholar
  4. Bedoui S, Davey GM, Lew AM, Heath WR (2009a) Equivalent stimulation of naive and memory CD8 T cells by DNA vaccination: a dendritic cell-dependent process. Immunol Cell Biol 87:255–259PubMedCrossRefGoogle Scholar
  5. Bedoui S, Whitney PG, Waithman J, Eidsmo L, Wakim L, Caminschi I, Allan RS, Wojtasiak M, Shortman K, Carbone FR, Brooks AG, Heath WR (2009b) Cross-presentation of viral and self antigens by skin-derived CD103+ dendritic cells. Nat Immunol 10:488–495PubMedCrossRefGoogle Scholar
  6. Belyakov IM, Hammond SA, Ahlers JD, Glenn GM, Berzofsky JA (2004) Transcutaneous immunization induces mucosal CTLs and protective immunity by migration of primed skin dendritic cells. J Clin Invest 113:998–1007PubMedGoogle Scholar
  7. Bennett CL, van Rijn E, Jung S, Inaba K, Steinman RM, Kapsenberg ML, Clausen BE (2005) Inducible ablation of mouse Langerhans cells diminishes but fails to abrogate contact hypersensitivity. J Cell Biol 169:569–576PubMedCrossRefGoogle Scholar
  8. Bogunovic M, Ginhoux F, Wagers A, Loubeau M, Isola LM, Lubrano L, Najfeld V, Phelps RG, Grosskreutz C, Scigliano E, Frenette PS, Merad M (2006) Identification of a radio-resistant and cycling dermal dendritic cell population in mice and men. J Exp Med 203:2627–2638PubMedCrossRefGoogle Scholar
  9. Bonifaz L, Bonnyay D, Mahnke K, Rivera M, Nussenzweig MC, Steinman RM (2002) Efficient targeting of protein antigen to the dendritic cell receptor DEC-205 in the steady state leads to antigen presentation on major histocompatibility complex class I products and peripheral CD8+ T cell tolerance. J Exp Med 196:1627–1638PubMedCrossRefGoogle Scholar
  10. Bonifaz LC, Bonnyay DP, Charalambous A, Darguste DI, Fujii S, Soares H, Brimnes MK, Moltedo B, Moran TM, Steinman RM (2004) In vivo targeting of antigens to maturing dendritic cells via the DEC-205 receptor improves T cell vaccination. J Exp Med 199:815–824PubMedCrossRefGoogle Scholar
  11. Borkowski TA, Letterio JJ, Farr AG, Udey MC (1996a) A role for endogenous transforming growth factor beta 1 in Langerhans cell biology: the skin of transforming growth factor beta 1 null mice is devoid of epidermal Langerhans cells. J Exp Med 184:2417–2422PubMedCrossRefGoogle Scholar
  12. Borkowski TA, Nelson AJ, Farr AG, Udey MC (1996b) Expression of gp40, the murine homologue of human epithelial cell adhesion molecule (Ep-CAM), by murine dendritic cells. Eur J Immunol 26:110–114PubMedCrossRefGoogle Scholar
  13. Borkowski TA, Letterio JJ, Mackall CL, Saitoh A, Wang XJ, Roop DR, Gress RE, Udey MC (1997) A role for TGFbeta1 in Langerhans cell biology. Further characterization of the epidermal Langerhans cell defect in TGFbeta1 null mice. J Clin Invest 100:575–581PubMedCrossRefGoogle Scholar
  14. Bougneres L, Helft J, Tiwari S, Vargas P, Chang BH, Chan L, Campisi L, Lauvau G, Hugues S, Kumar P, Kamphorst AO, Dumenil AM, Nussenzweig M, MacMicking JD, Amigorena S, Guermonprez P (2009) A role for lipid bodies in the cross-presentation of phagocytosed antigens by MHC class I in dendritic cells. Immunity 31:232–244PubMedCrossRefGoogle Scholar
  15. Bozzacco L, Trumpfheller C, Huang Y, Longhi MP, Shimeliovich I, Schauer JD, Park CG, Steinman RM (2010) HIV gag protein is efficiently cross-presented when targeted with an antibody towards the DEC-205 receptor in Flt3 ligand-mobilized murine DC. Eur J Immunol 40:36–46PubMedCrossRefGoogle Scholar
  16. Brewig N, Kissenpfennig A, Malissen B, Veit A, Bickert T, Fleischer B, Mostbock S, Ritter U (2009) Priming of CD8+ and CD4+ T cells in experimental leishmaniasis is initiated by different dendritic cell subtypes. J Immunol 182:774–783PubMedGoogle Scholar
  17. Burnett SH, Kershen EJ, Zhang J, Zeng L, Straley SC, Kaplan AM, Cohen DA (2004) Conditional macrophage ablation in transgenic mice expressing a Fas-based suicide gene. J Leukoc Biol 75:612–623PubMedCrossRefGoogle Scholar
  18. Bursch LS, Wang L, Igyarto B, Kissenpfennig A, Malissen B, Kaplan DH, Hogquist KA (2007) Identification of a novel population of Langerin+ dendritic cells. J Exp Med 204:3147–3156PubMedCrossRefGoogle Scholar
  19. Caminschi I, Proietto AI, Ahmet F, Kitsoulis S, Shin Teh J, Lo JC, Rizzitelli A, Wu L, Vremec D, van Dommelen SL, Campbell IK, Maraskovsky E, Braley H, Davey GM, Mottram P, van de Velde N, Jensen K, Lew AM, Wright MD, Heath WR, Shortman K, Lahoud MH (2008) The dendritic cell subtype-restricted C-type lectin Clec9A is a target for vaccine enhancement. Blood 112:3264–3273PubMedCrossRefGoogle Scholar
  20. Caux C, Dezutter-Dambuyant C, Schmitt D, Banchereau J (1992) GM-CSF and TNF-alpha cooperate in the generation of dendritic Langerhans cells. Nature 360:258–261PubMedCrossRefGoogle Scholar
  21. Cepek KL, Shaw SK, Parker CM, Russell GJ, Morrow JS, Rimm DL, Brenner MB (1994) Adhesion between epithelial cells and T lymphocytes mediated by E-cadherin and the alpha E beta 7 integrin. Nature 372:190–193PubMedCrossRefGoogle Scholar
  22. Chorro L, Sarde A, Li M, Woollard KJ, Chambon P, Malissen B, Kissenpfennig A, Barbaroux JB, Groves R, Geissmann F (2009) Langerhans cell (LC) proliferation mediates neonatal development, homeostasis, and inflammation-associated expansion of the epidermal LC network. J Exp Med 206:3089–3100PubMedCrossRefGoogle Scholar
  23. Condon C, Watkins SC, Celluzzi CM, Thompson K, Falo LD Jr (1996) DNA-based immunization by in vivo transfection of dendritic cells. Nat Med 2:1122–1128PubMedCrossRefGoogle Scholar
  24. Dai XM, Ryan GR, Hapel AJ, Dominguez MG, Russell RG, Kapp S, Sylvestre V, Stanley ER (2002) Targeted disruption of the mouse colony-stimulating factor 1 receptor gene results in osteopetrosis, mononuclear phagocyte deficiency, increased primitive progenitor cell frequencies, and reproductive defects. Blood 99:111–120PubMedCrossRefGoogle Scholar
  25. Del Rio ML, Rodriguez-Barbosa JI, Kremmer E, Forster R (2007) CD103 and CD103+ bronchial lymph node dendritic cells are specialized in presenting and cross-presenting innocuous antigen to CD4+ and CD8+ T cells. J Immunol 178:6861–6866PubMedGoogle Scholar
  26. Demangel C, Zhou J, Choo AB, Shoebridge G, Halliday GM, Britton WJ (2005) Single chain antibody fragments for the selective targeting of antigens to dendritic cells. Mol Immunol 42:979–985PubMedCrossRefGoogle Scholar
  27. Den Haan JM, Lehar SM, Bevan MJ (2000) CD8(+) but not CD8(−) dendritic cells cross-prime cytotoxic T cells in vivo. J Exp Med 192:1685–1696CrossRefGoogle Scholar
  28. Dranoff G, Jaffee E, Lazenby A, Golumbek P, Levitsky H, Brose K, Jackson V, Hamada H, Pardoll D, Mulligan RC (1993) Vaccination with irradiated tumor cells engineered to secrete murine granulocyte-macrophage colony-stimulating factor stimulates potent, specific, and long-lasting anti-tumor immunity. Proc Natl Acad Sci USA 90:3539–3543PubMedCrossRefGoogle Scholar
  29. Drexhage HA, Mullink H, de Groot J, Clarke J, Balfour BM (1979) A study of cells present in peripheral lymph of pigs with special reference to a type of cell resembling the Langerhans cell. Cell Tissue Res 202:407–430PubMedCrossRefGoogle Scholar
  30. 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 315:107–111PubMedCrossRefGoogle Scholar
  31. Edwards AD, Chaussabel D, Tomlinson S, Schulz O, Sher A, Reis e Sousa C (2003) Relationships among murine CD11c(high) dendritic cell subsets as revealed by baseline gene expression patterns. J Immunol 171:47–60PubMedGoogle Scholar
  32. Eidsmo L, Allan R, Caminschi I, van Rooijen N, Heath WR, Carbone FR (2009) Differential migration of epidermal and dermal dendritic cells during skin infection. J Immunol 182:3165–3172PubMedCrossRefGoogle Scholar
  33. Fan H, Lin Q, Morrissey GR, Khavari PA (1999) Immunization via hair follicles by topical application of naked DNA to normal skin. Nat Biotechnol 17:870–872PubMedCrossRefGoogle Scholar
  34. Flacher V, Sparber F, Tripp CH, Romani N, Stoitzner P (2009) Targeting of epidermal Langerhans cells with antigenic proteins: attempts to harness their properties for immunotherapy. Cancer Immunol Immunother 58:1137–1147PubMedCrossRefGoogle Scholar
  35. Flacher V, Tripp CH, Stoitzner P, Haid B, Ebner S, Del Frari B, Koch F, Park CG, Steinman RM, Idoyaga J, Romani N (2010) Epidermal Langerhans cells rapidly capture and present antigens from C-type lectin-targeting antibodies deposited in the dermis. J Invest Dermatol 130:755–762PubMedCrossRefGoogle Scholar
  36. Forster R, Schubel A, Breitfeld D, Kremmer E, Renner-Muller I, Wolf E, Lipp M (1999) CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell 99:23–33PubMedCrossRefGoogle Scholar
  37. Garg S, Oran A, Wajchman J, Sasaki S, Maris CH, Kapp JA, Jacob J (2003) Genetic tagging shows increased frequency and longevity of antigen-presenting, skin-derived dendritic cells in vivo. Nat Immunol 4:907–912PubMedCrossRefGoogle Scholar
  38. Geissmann F, Auffray C, Palframan R, Wirrig C, Ciocca A, Campisi L, Narni-Mancinelli E, Lauvau G (2008) Blood monocytes: distinct subsets, how they relate to dendritic cells, and their possible roles in the regulation of T-cell responses. Immunol Cell Biol 86:398–408PubMedCrossRefGoogle Scholar
  39. Geissmann F, Manz MG, Jung S, Sieweke MH, Merad M, Ley K (2010) Development of monocytes, macrophages, and dendritic cells. Science 327:656–661PubMedCrossRefGoogle Scholar
  40. Ginhoux F, Tacke F, Angeli V, Bogunovic M, Loubeau M, Dai XM, Stanley ER, Randolph GJ, Merad M (2006) Langerhans cells arise from monocytes in vivo. Nat Immunol 7:265–273PubMedCrossRefGoogle Scholar
  41. Ginhoux F, Collin MP, Bogunovic M, Abel M, Leboeuf M, Helft J, Ochando J, Kissenpfennig A, Malissen B, Grisotto M, Snoeck H, Randolph G, Merad M (2007) Blood-derived dermal langerin+ dendritic cells survey the skin in the steady state. J Exp Med 204:3133–3146PubMedCrossRefGoogle Scholar
  42. 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 206:3115–3130PubMedCrossRefGoogle Scholar
  43. Glenn GM, Rao M, Matyas GR, Alving CR (1998a) Skin immunization made possible by cholera toxin. Nature 391:851PubMedCrossRefGoogle Scholar
  44. Glenn GM, Scharton-Kersten T, Vassell R, Mallett CP, Hale TL, Alving CR (1998b) Transcutaneous immunization with cholera toxin protects mice against lethal mucosal toxin challenge. J Immunol 161:3211–3214PubMedGoogle Scholar
  45. Glenn GM, Taylor DN, Li X, Frankel S, Montemarano A, Alving CR (2000) Transcutaneous immunization: a human vaccine delivery strategy using a patch. Nat Med 6:1403–1406PubMedCrossRefGoogle Scholar
  46. Hamilton JA (2008) Colony-stimulating factors in inflammation and autoimmunity. Nat Rev Immunol 8:533–544PubMedCrossRefGoogle Scholar
  47. Haniffa M, Ginhoux F, Wang XN, Bigley V, Abel M, Dimmick I, Bullock S, Grisotto M, Booth T, Taub P, Hilkens C, Merad M, Collin M (2009) Differential rates of replacement of human dermal dendritic cells and macrophages during hematopoietic stem cell transplantation. J Exp Med 206:371–385PubMedCrossRefGoogle Scholar
  48. Hawiger D, Inaba K, Dorsett Y, Guo M, Mahnke K, Rivera M, Ravetch JV, Steinman RM, Nussenzweig MC (2001) Dendritic cells induce peripheral T cell unresponsiveness under steady state conditions in vivo. J Exp Med 194:769–779PubMedCrossRefGoogle Scholar
  49. He Y, Falo LD Jr (2007) Lentivirus as a potent and mechanistically distinct vector for genetic immunization. Curr Opin Mol Ther 9:439–446PubMedGoogle Scholar
  50. He Y, Zhang J, Donahue C, Falo LD Jr (2006) Skin-derived dendritic cells induce potent CD8(+) T cell immunity in recombinant lentivector-mediated genetic immunization. Immunity 24:643–656PubMedCrossRefGoogle Scholar
  51. Helft J, Ginhoux F, Bogunovic M, Merad M (2010) Origin and functional heterogeneity of non-lymphoid tissue dendritic cells in mice. Immunol Rev 234:55–75PubMedCrossRefGoogle Scholar
  52. Hemmi H, Yoshino M, Yamazaki H, Naito M, Iyoda T, Omatsu Y, Shimoyama S, Letterio JJ, Nakabayashi T, Tagaya H, Yamane T, Ogawa M, Nishikawa S, Ryoke K, Inaba K, Hayashi S, Kunisada T (2001) Skin antigens in the steady state are trafficked to regional lymph nodes by transforming growth factor-beta1-dependent cells. Int Immunol 13:695–704PubMedCrossRefGoogle Scholar
  53. Henri S, Poulin LF, Tamoutounour S, Ardouin L, Guilliams M, de Bovis B, Devilard E, Viret C, Azukizawa H, Kissenpfennig A, Malissen B (2009) CD207+ CD103+ dermal dendritic cells cross-present keratinocyte-derived antigens irrespective of the presence of Langerhans cells. J Exp Med 207(1):189–206PubMedCrossRefGoogle Scholar
  54. Hickey DK, Bao S, Ikeda LT, Carey AJ, Beagley KW (2005) Induction of anti-chlamydial mucosal immunity by transcutaneous immunization is enhanced by topical application of GM-CSF. Curr Mol Med 5:599–605PubMedCrossRefGoogle Scholar
  55. 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 322:1097–1100PubMedCrossRefGoogle Scholar
  56. Inaba K, Inaba M, Romani N, Aya H, Deguchi M, Ikehara S, Muramatsu S, Steinman RM (1992) Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J Exp Med 176:1693–1702PubMedCrossRefGoogle Scholar
  57. Inaba K, Swiggard WJ, Inaba M, Meltzer J, Mirza A, Sasagawa T, Nussenzweig MC, Steinman RM (1995) Tissue distribution of the DEC-205 protein that is detected by the monoclonal antibody NLDC-145. I. Expression on dendritic cells and other subsets of mouse leukocytes. Cell Immunol 163:148–156PubMedCrossRefGoogle Scholar
  58. Iyoda T, Shimoyama S, Liu K, Omatsu Y, Akiyama Y, Maeda Y, Takahara K, Steinman RM, Inaba K (2002) The CD8+ dendritic cell subset selectively endocytoses dying cells in culture and in vivo. J Exp Med 195:1289–1302PubMedCrossRefGoogle Scholar
  59. Jakubzick C, Bogunovic M, Bonito AJ, Kuan EL, Merad M, Randolph GJ (2008) Lymph-migrating, tissue-derived dendritic cells are minor constituents within steady-state lymph nodes. J Exp Med 205:2839–2850PubMedCrossRefGoogle Scholar
  60. Jiang W, Swiggard WJ, Heufler C, Peng M, Mirza A, Steinman RM, Nussenzweig MC (1995) The receptor DEC-205 expressed by dendritic cells and thymic epithelial cells is involved in antigen processing. Nature 375:151–155PubMedCrossRefGoogle Scholar
  61. Julia V, Hessel EM, Malherbe L, Glaichenhaus N, O’Garra A, Coffman RL (2002) A restricted subset of dendritic cells captures airborne antigens and remains able to activate specific T cells long after antigen exposure. Immunity 16:271–283PubMedCrossRefGoogle Scholar
  62. Jung S, Aliberti J, Graemmel P, Sunshine MJ, Kreutzberg GW, Sher A, Littman DR (2000) Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol Cell Biol 20:4106–4114PubMedCrossRefGoogle Scholar
  63. Kabashima K, Banks TA, Ansel KM, Lu TT, Ware CF, Cyster JG (2005) Intrinsic lymphotoxin-beta receptor requirement for homeostasis of lymphoid tissue dendritic cells. Immunity 22:439–450PubMedCrossRefGoogle Scholar
  64. Kaplan DH, Jenison MC, Saeland S, Shlomchik WD, Shlomchik MJ (2005) Epidermal Langerhans cell-deficient mice develop enhanced contact hypersensitivity. Immunity 23:611–620PubMedCrossRefGoogle Scholar
  65. Kaplan DH, Li MO, Jenison MC, Shlomchik WD, Flavell RA, Shlomchik MJ (2007) Autocrine/paracrine TGFbeta1 is required for the development of epidermal Langerhans cells. J Exp Med 204:2545–2552PubMedCrossRefGoogle Scholar
  66. Kelly RH, Balfour BM, Armstrong JA, Griffiths S (1978) Functional anatomy of lymph nodes. II. Peripheral lymph-borne mononuclear cells. Anat Rec 190:5–21PubMedCrossRefGoogle Scholar
  67. Kenney RT, Frech SA, Muenz LR, Villar CP, Glenn GM (2004) Dose sparing with intradermal injection of influenza vaccine. N Engl J Med 351:2295–2301PubMedCrossRefGoogle Scholar
  68. Kim TS, Braciale TJ (2009) Respiratory dendritic cell subsets differ in their capacity to support the induction of virus-specific cytotoxic CD8+ T cell responses. PLoS One 4:e4204PubMedCrossRefGoogle Scholar
  69. Kim YC, Jarrahian C, Zehrung D, Mitragotri S, Prausnitz MR (2011) Delivery systems for intradermal vaccination. Curr Top Microbiol Immunol 351:77–112CrossRefGoogle Scholar
  70. Kingston D, Schmid MA, Onai N, Obata-Onai A, Baumjohann D, Manz MG (2009) The concerted action of GM-CSF and Flt3-ligand on in vivo dendritic cell homeostasis. Blood 114:835–843PubMedCrossRefGoogle Scholar
  71. Kissenpfennig A, Henri S, Dubois B, Laplace-Builhe C, Perrin P, Romani N, Tripp CH, Douillard P, Leserman L, Kaiserlian D, Saeland S, Davoust J, Malissen B (2005) Dynamics and function of Langerhans cells in vivo: dermal dendritic cells colonize lymph node areas distinct from slower migrating Langerhans cells. Immunity 22:643–654PubMedCrossRefGoogle Scholar
  72. Kubo A, Nagao K, Yokouchi M, Sasaki H, Amagai M (2009) External antigen uptake by Langerhans cells with reorganization of epidermal tight junction barriers. J Exp Med 206:2937–2946PubMedCrossRefGoogle Scholar
  73. Lahoud MH, Proietto AI, Ahmet F, Kitsoulis S, Eidsmo L, Wu L, Sathe P, Pietersz S, Chang HW, Walker ID, Maraskovsky E, Braley H, Lew AM, Wright MD, Heath WR, Shortman K, Caminschi I (2009) The C-type lectin Clec12A present on mouse and human dendritic cells can serve as a target for antigen delivery and enhancement of antibody responses. J Immunol 182:7587–7594PubMedCrossRefGoogle Scholar
  74. Le Borgne M, Etchart N, Goubier A, Lira SA, Sirard JC, van Rooijen N, Caux C, Ait-Yahia S, Vicari A, Kaiserlian D, Dubois B (2006) Dendritic cells rapidly recruited into epithelial tissues via CCR6/CCL20 are responsible for CD8+ T cell crosspriming in vivo. Immunity 24:191–201PubMedCrossRefGoogle Scholar
  75. Leon B, Ardavin C (2008) Monocyte-derived dendritic cells in innate and adaptive immunity. Immunol Cell Biol 86:320–324PubMedCrossRefGoogle Scholar
  76. Leon B, Lopez-Bravo M, Ardavin C (2007) Monocyte-derived dendritic cells formed at the infection site control the induction of protective T helper 1 responses against Leishmania. Immunity 26:519–531PubMedCrossRefGoogle Scholar
  77. Lindquist RL, Shakhar G, Dudziak D, Wardemann H, Eisenreich T, Dustin ML, Nussenzweig MC (2004) Visualizing dendritic cell networks in vivo. Nat Immunol 5:1243–1250PubMedCrossRefGoogle Scholar
  78. Liu YJ (2005) IPC: professional type 1 interferon-producing cells and plasmacytoid dendritic cell precursors. Annu Rev Immunol 23:275–306PubMedCrossRefGoogle Scholar
  79. 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 8:578–583PubMedCrossRefGoogle Scholar
  80. Liu K, Victora GD, Schwickert TA, Guermonprez P, Meredith MM, Yao K, Chu FF, Randolph GJ, Rudensky AY, Nussenzweig M (2009) In vivo analysis of dendritic cell development and homeostasis. Science 324(5925):392–397PubMedGoogle Scholar
  81. Lyman SD, Jacobsen SE (1998) c-kit ligand and Flt3 ligand: stem/progenitor cell factors with overlapping yet distinct activities. Blood 91:1101–1134PubMedGoogle Scholar
  82. Lyman SD, James L, Escobar S, Downey H, de Vries P, Brasel K, Stocking K, Beckmann MP, Copeland NG, Cleveland LS et al. (1995) Identification of soluble and membrane-bound isoforms of the murine flt3 ligand generated by alternative splicing of mRNAs. Oncogene 10:149–157PubMedGoogle Scholar
  83. Macdonald KP, Rowe V, Bofinger HM, Thomas R, Sasmono T, Hume DA, Hill GR (2005) The colony-stimulating factor 1 receptor is expressed on dendritic cells during differentiation and regulates their expansion. J Immunol 175:1399–1405PubMedGoogle Scholar
  84. Maraskovsky E, Brasel K, Teepe M, Roux ER, Lyman SD, Shortman K, McKenna HJ (1996) Dramatic increase in the numbers of functionally mature dendritic cells in Flt3 ligand-treated mice: multiple dendritic cell subpopulations identified. J Exp Med 184:1953–1962PubMedCrossRefGoogle Scholar
  85. McKenna HJ, Stocking KL, Miller RE, Brasel K, De Smedt T, Maraskovsky E, Maliszewski CR, Lynch DH, Smith J, Pulendran B, Roux ER, Teepe M, Lyman SD, Peschon JJ (2000) Mice lacking flt3 ligand have deficient hematopoiesis affecting hematopoietic progenitor cells, dendritic cells, and natural killer cells. Blood 95:3489–3497PubMedGoogle Scholar
  86. McLachlan JB, Catron DM, Moon JJ, Jenkins MK (2009) Dendritic cell antigen presentation drives simultaneous cytokine production by effector and regulatory T cells in inflamed skin. Immunity 30:277–288PubMedCrossRefGoogle Scholar
  87. Merad M, Manz MG, Karsunky H, Wagers A, Peters W, Charo I, Weissman IL, Cyster JG, Engleman EG (2002) Langerhans cells renew in the skin throughout life under steady-state conditions. Nat Immunol 3:1135–1141PubMedCrossRefGoogle Scholar
  88. Merad M, Hoffmann P, Ranheim E, Slaymaker S, Manz MG, Lira SA, Charo I, Cook DN, Weissman IL, Strober S, Engleman EG (2004) Depletion of host Langerhans cells before transplantation of donor alloreactive T cells prevents skin graft-versus-host disease. Nat Med 10:510–517PubMedCrossRefGoogle Scholar
  89. Merad M, Ginhoux F, Collin M (2008) Origin, homeostasis and function of Langerhans cells and other langerin-expressing dendritic cells. Nat Rev Immunol 8:935–947PubMedCrossRefGoogle Scholar
  90. Nagao K, Ginhoux F, Leitner WW, Motegi S, Bennett CL, Clausen BE, Merad M, Udey MC (2009) Murine epidermal Langerhans cells and langerin-expressing dermal dendritic cells are unrelated and exhibit distinct functions. Proc Natl Acad Sci USA 106:3312–3317PubMedCrossRefGoogle Scholar
  91. Naik SH, Metcalf D, van Nieuwenhuijze A, Wicks I, Wu L, O’Keeffe M, Shortman K (2006) Intrasplenic steady-state dendritic cell precursors that are distinct from monocytes. Nat Immunol 7(6):663–671PubMedCrossRefGoogle Scholar
  92. Nchinda G, Kuroiwa J, Oks M, Trumpfheller C, Park CG, Huang Y, Hannaman D, Schlesinger SJ, Mizenina O, Nussenzweig MC, Uberla K, Steinman RM (2008) The efficacy of DNA vaccination is enhanced in mice by targeting the encoded protein to dendritic cells. J Clin Invest 118:1427–1436PubMedCrossRefGoogle Scholar
  93. Nestle FO, Di Meglio P, Qin JZ, Nickoloff BJ (2009) Skin immune sentinels in health and disease. Nat Rev Immunol 9:679–691PubMedGoogle Scholar
  94. Ng LG, Mrass P, Kinjyo I, Reiner SL, Weninger W (2008) Two-photon imaging of effector T-cell behavior: lessons from a tumor model. Immunol Rev 221:147–162PubMedCrossRefGoogle Scholar
  95. Nishibu A, Ward BR, Jester JV, Ploegh HL, Boes M, Takashima A (2006) Behavioral responses of epidermal Langerhans cells in situ to local pathological stimuli. J Invest Dermatol 126:787–796PubMedCrossRefGoogle Scholar
  96. Ohl L, Mohaupt M, Czeloth N, Hintzen G, Kiafard Z, Zwirner J, Blankenstein T, Henning G, Forster R (2004) CCR7 governs skin dendritic cell migration under inflammatory and steady-state conditions. Immunity 21:279–288PubMedCrossRefGoogle Scholar
  97. Porgador A, Irvine KR, Iwasaki A, Barber BH, Restifo NP, Germain RN (1998) Predominant role for directly transfected dendritic cells in antigen presentation to CD8+ T cells after gene gun immunization. J Exp Med 188:1075–1082PubMedCrossRefGoogle Scholar
  98. Poulin LF, Henri S, de Bovis B, Devilard E, Kissenpfennig A, Malissen B (2007) The dermis contains langerin+ dendritic cells that develop and function independently of epidermal Langerhans cells. J Exp Med 204:3119–3131PubMedCrossRefGoogle Scholar
  99. Randolph GJ, Ochando J, Partida-Sanchez S (2008) Migration of dendritic cell subsets and their precursors. Annu Rev Immunol 26:293–316PubMedCrossRefGoogle Scholar
  100. Roediger B, Ng LG, Smith AL, Fazekas de St Groth B, Weninger W (2008) Visualizing dendritic cell migration within the skin. Histochem Cell Biol 130:1131–1146PubMedCrossRefGoogle Scholar
  101. Sallusto F, Lanzavecchia A (1994) Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J Exp Med 179:1109–1118PubMedCrossRefGoogle Scholar
  102. Sancho D, Joffre OP, Keller AM, Rogers NC, Martinez D, Hernanz-Falcon P, Rosewell I, Reis e Sousa C (2009) Identification of a dendritic cell receptor that couples sensing of necrosis to immunity. Nature 458:899–903PubMedCrossRefGoogle Scholar
  103. Savina A, Peres A, Cebrian I, Carmo N, Moita C, Hacohen N, Moita LF, Amigorena S (2009) The small GTPase Rac2 controls phagosomal alkalinization and antigen crosspresentation selectively in CD8(+) dendritic cells. Immunity 30:544–555PubMedCrossRefGoogle Scholar
  104. Shklovskaya E, Roediger B, Fazekas de St Groth B (2008) Epidermal and dermal dendritic cells display differential activation and migratory behavior while sharing the ability to stimulate CD4+ T cell proliferation in vivo. J Immunol 181:418–430PubMedGoogle Scholar
  105. Shortman K, Naik SH (2007) Steady-state and inflammatory dendritic-cell development. Nat Rev Immunol 7:19–30PubMedCrossRefGoogle Scholar
  106. Simons JW, Mikhak B, Chang JF, DeMarzo AM, Carducci MA, Lim M, Weber CE, Baccala AA, Goemann MA, Clift SM, Ando DG, Levitsky HI, Cohen LK, Sanda MG, Mulligan RC, Partin AW, Carter HB, Piantadosi S, Marshall FF, Nelson WG (1999) Induction of immunity to prostate cancer antigens: results of a clinical trial of vaccination with irradiated autologous prostate tumor cells engineered to secrete granulocyte-macrophage colony-stimulating factor using ex vivo gene transfer. Cancer Res 59:5160–5168PubMedGoogle Scholar
  107. Song JH, Kim JI, Kwon HJ, Shim DH, Parajuli N, Cuburu N, Czerkinsky C, Kweon MN (2009) CCR7-CCL19/CCL21-regulated dendritic cells are responsible for effectiveness of sublingual vaccination. J Immunol 182:6851–6860PubMedCrossRefGoogle Scholar
  108. Steinman RM, Hawiger D, Nussenzweig MC (2003) Tolerogenic dendritic cells. Annu Rev Immunol 21:685–711PubMedCrossRefGoogle Scholar
  109. Stoecklinger A, Grieshuber I, Scheiblhofer S, Weiss R, Ritter U, Kissenpfennig A, Malissen B, Romani N, Koch F, Ferreira F, Thalhamer J, Hammerl P (2007) Epidermal Langerhans cells are dispensable for humoral and cell-mediated immunity elicited by gene gun immunization. J Immunol 179:886–893PubMedGoogle Scholar
  110. Stutte S, Jux B, Esser C, Forster I (2008) CD24a expression levels discriminate Langerhans cells from dermal dendritic cells in murine skin and lymph nodes. J Invest Dermatol 128:1470–1475PubMedCrossRefGoogle Scholar
  111. Sung SS, Fu SM, Rose CE Jr, Gaskin F, Ju ST, Beaty SR (2006) A major lung CD103 (alphaE)-beta7 integrin-positive epithelial dendritic cell population expressing Langerin and tight junction proteins. J Immunol 176:2161–2172PubMedGoogle Scholar
  112. Takahara K, Omatsu Y, Yashima Y, Maeda Y, Tanaka S, Iyoda T, Clausen BE, Matsubara K, Letterio J, Steinman RM, Matsuda Y, Inaba K (2002) Identification and expression of mouse Langerin (CD207) in dendritic cells. Int Immunol 14:433–444PubMedCrossRefGoogle Scholar
  113. Takahashi K, Naito M, Shultz LD, Hayashi S, Nishikawa S (1993) Differentiation of dendritic cell populations in macrophage colony-stimulating factor-deficient mice homozygous for the osteopetrosis (op) mutation. J Leukoc Biol 53:19–28PubMedGoogle Scholar
  114. Tang A, Amagai M, Granger LG, Stanley JR, Udey MC (1993) Adhesion of epidermal Langerhans cells to keratinocytes mediated by E-cadherin. Nature 361:82–85PubMedCrossRefGoogle Scholar
  115. Trumpfheller C, Finke JS, Lopez CB, Moran TM, Moltedo B, Soares H, Huang Y, Schlesinger SJ, Park CG, Nussenzweig MC, Granelli-Piperno A, Steinman RM (2006) Intensified and protective CD4+ T cell immunity in mice with anti-dendritic cell HIV gag fusion antibody vaccine. J Exp Med 203:607–617PubMedCrossRefGoogle Scholar
  116. Valladeau J, Saeland S (2005) Cutaneous dendritic cells. Semin Immunol 17:273–283PubMedCrossRefGoogle Scholar
  117. Vremec D, Lieschke GJ, Dunn AR, Robb L, Metcalf D, Shortman K (1997) The influence of granulocyte/macrophage colony-stimulating factor on dendritic cell levels in mouse lymphoid organs. Eur J Immunol 27:40–44PubMedCrossRefGoogle Scholar
  118. Wakim LM, Waithman J, van Rooijen N, Heath WR, Carbone FR (2008) Dendritic cell-induced memory T cell activation in nonlymphoid tissues. Science 319:198–202PubMedCrossRefGoogle Scholar
  119. Waskow C, Liu K, Darrasse-Jeze G, Guermonprez P, Ginhoux F, Merad M, Shengelia T, Yao K, Nussenzweig M (2008) The receptor tyrosine kinase Flt3 is required for dendritic cell development in peripheral lymphoid tissues. Nat Immunol 9:676–683PubMedCrossRefGoogle Scholar
  120. Williams RS, Johnston SA, Riedy M, DeVit MJ, McElligott SG, Sanford JC (1991) Introduction of foreign genes into tissues of living mice by DNA-coated microprojectiles. Proc Natl Acad Sci USA 88:2726–2730PubMedCrossRefGoogle Scholar
  121. Witmer-Pack MD, Hughes DA, Schuler G, Lawson L, McWilliam A, Inaba K, Steinman RM, Gordon S (1993) Identification of macrophages and dendritic cells in the osteopetrotic (op/op) mouse. J Cell Sci 104(Pt 4):1021–1029PubMedGoogle Scholar
  122. Wright DE, Wagers AJ, Gulati AP, Johnson FL, Weissman IL (2001) Physiological migration of hematopoietic stem and progenitor cells. Science 294:1933–1936PubMedCrossRefGoogle Scholar
  123. Xiang Z, Ertl HC (1995) Manipulation of the immune response to a plasmid-encoded viral antigen by coinoculation with plasmids expressing cytokines. Immunity 2:129–135PubMedCrossRefGoogle Scholar
  124. Yoshida H, Hayashi S, Kunisada T, Ogawa M, Nishikawa S, Okamura H, Sudo T, Shultz LD (1990) The murine mutation osteopetrosis is in the coding region of the macrophage colony stimulating factor gene. Nature 345:442–444PubMedCrossRefGoogle Scholar
  125. Zhao X, Deak E, Soderberg K, Linehan M, Spezzano D, Zhu J, Knipe DM, Iwasaki A (2003) Vaginal submucosal dendritic cells, but not Langerhans cells, induce protective Th1 responses to herpes simplex virus-2. J Exp Med 197:153–162PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2010

Authors and Affiliations

  1. 1.Singapore Immunology Network (SIgN), Agency for Science, Technology and Research (A*STAR)SingaporeSingapore
  2. 2.Department of Gene and Cell Medicine and the Immunology InstituteMount Sinai School of MedicineNew YorkUSA

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