Skip to main content

Advertisement

Log in

Peripheral regulation of T cells by dendritic cells during infection

  • IMMUNOLOGY AT THE UNIVERSITY OF IOWA
  • Published:
Immunologic Research Aims and scope Submit manuscript

Abstract

It is well accepted that T cell responses are integral in providing protection during pathogenic infections. In numerous tissues, T cell responses are generated to combat infection. Typically, these T cell responses are primed in draining lymph nodes (LN) by dendritic cells (DC) that have migrated from the infected tissue. Previously, it was thought that after the initial encounter between DC and T cells in the LN, the T cells underwent a programmed response. However, it has become increasingly clear that direct interactions between DCs and T cells in infected, peripheral tissues can modulate the activation, effector function, tissue residence, and memory responses of these T cells. This review will highlight the contribution of local, direct DC: T cell interactions to the regulation of T cell responses in various tissues during inflammation and infection .

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Banchereau J, Briere F, Caux C, Davoust J, Lebecque S, Liu YJ, et al. Immunobiology of dendritic cells. Annu Rev Immunol. 2000;18:767–811. doi:10.1146/annurev.immunol.18.1.767.

    Article  CAS  PubMed  Google Scholar 

  2. Guermonprez P, Valladeau J, Zitvogel L, Thery C, Amigorena S. Antigen presentation and T cell stimulation by dendritic cells. Annu Rev Immunol. 2002;20:621–67. doi:10.1146/annurev.immunol.20.100301.064828.

    Article  CAS  PubMed  Google Scholar 

  3. Lambrecht BN, Hammad H. Lung dendritic cells in respiratory viral infection and asthma: from protection to immunopathology. Annu Rev Immunol. 2012;30:243–70. doi:10.1146/annurev-immunol-020711-075021.

    Article  CAS  PubMed  Google Scholar 

  4. Smith-Garvin JE, Koretzky GA, Jordan MS. T cell activation. Annu Rev Immunol. 2009;27:591–619. doi:10.1146/annurev.immunol.021908.132706.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  5. Curtsinger JM, Mescher MF. Inflammatory cytokines as a third signal for T cell activation. Curr Opin Immunol. 2010;22(3):333–40. doi:10.1016/j.coi.2010.02.013.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  6. Bertram EM, Dawicki W, Watts TH. Role of T cell costimulation in anti-viral immunity. Semin Immunol. 2004;16(3):185–96. doi:10.1016/j.smim.2004.02.006.

    Article  CAS  PubMed  Google Scholar 

  7. Welten SP, Melief CJ, Arens R. The distinct role of T cell costimulation in antiviral immunity. Curr Opin Virol. 2013;3(4):475–82. doi:10.1016/j.coviro.2013.06.012.

    Article  CAS  PubMed  Google Scholar 

  8. Kaech SM, Ahmed R. Memory CD8+ T cell differentiation: initial antigen encounter triggers a developmental program in naive cells. Nat Immunol. 2001;2(5):415–22. doi:10.1038/87720.

    PubMed Central  CAS  PubMed  Google Scholar 

  9. van Stipdonk MJ, Hardenberg G, Bijker MS, Lemmens EE, Droin NM, Green DR, et al. Dynamic programming of CD8+ T lymphocyte responses. Nat Immunol. 2003;4(4):361–5. doi:10.1038/ni912.

    Article  PubMed  Google Scholar 

  10. van Stipdonk MJ, Lemmens EE, Schoenberger SP. Naive CTLs require a single brief period of antigenic stimulation for clonal expansion and differentiation. Nat Immunol. 2001;2(5):423–9. doi:10.1038/87730.

    PubMed  Google Scholar 

  11. Bedoui S, Gebhardt T. Interaction between dendritic cells and T cells during peripheral virus infections: a role for antigen presentation beyond lymphoid organs? Curr Opin Immunol. 2011;23(1):124–30. doi:10.1016/j.coi.2010.11.001.

    Article  CAS  PubMed  Google Scholar 

  12. Bennett CL, Chakraverty R. Dendritic cells in tissues: in situ stimulation of immunity and immunopathology. Trends Immunol. 2012;33(1):8–13. doi:10.1016/j.it.2011.09.008.

    Article  CAS  PubMed  Google Scholar 

  13. Carragher DM, Rangel-Moreno J, Randall TD. Ectopic lymphoid tissues and local immunity. Semin Immunol. 2008;20(1):26–42. doi:10.1016/j.smim.2007.12.004.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  14. Neyt K, Perros F, GeurtsvanKessel CH, Hammad H, Lambrecht BN. Tertiary lymphoid organs in infection and autoimmunity. Trends Immunol. 2012;33(6):297–305. doi:10.1016/j.it.2012.04.006.

    Article  CAS  PubMed  Google Scholar 

  15. Chiavolini D, Rangel-Moreno J, Berg G, Christian K, Oliveira-Nascimento L, Weir S, et al. Bronchus-associated lymphoid tissue (BALT) and survival in a vaccine mouse model of tularemia. PLoS One. 2010;5(6):e11156. doi:10.1371/journal.pone.0011156.

    Article  PubMed Central  PubMed  Google Scholar 

  16. Holt PG. Development of bronchus associated lymphoid tissue (BALT) in human lung disease: a normal host defence mechanism awaiting therapeutic exploitation? Thorax. 1993;48(11):1097–8.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  17. Moyron-Quiroz JE, Rangel-Moreno J, Kusser K, Hartson L, Sprague F, Goodrich S, et al. Role of inducible bronchus associated lymphoid tissue (iBALT) in respiratory immunity. Nat Med. 2004;10(9):927–34. doi:10.1038/nm1091.

    Article  CAS  PubMed  Google Scholar 

  18. Tschernig T, Pabst R. Bronchus-associated lymphoid tissue (BALT) is not present in the normal adult lung but in different diseases. Pathobiology. 2000;68(1):1–8.

    Article  CAS  PubMed  Google Scholar 

  19. Moyron-Quiroz J, Rangel-Moreno J, Carragher DM, Randall TD. The function of local lymphoid tissues in pulmonary immune responses. Adv Exp Med Biol. 2007;590:55–68. doi:10.1007/978-0-387-34814-8_4.

    Article  PubMed  Google Scholar 

  20. GeurtsvanKessel CH, Willart MA, Bergen IM, van Rijt LS, Muskens F, Elewaut D, et al. Dendritic cells are crucial for maintenance of tertiary lymphoid structures in the lung of influenza virus-infected mice. J Exp Med. 2009;206(11):2339–49. doi:10.1084/jem.20090410.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  21. Belz GT, Smith CM, Kleinert L, Reading P, Brooks A, Shortman K, et al. Distinct migrating and nonmigrating dendritic cell populations are involved in MHC class I-restricted antigen presentation after lung infection with virus. Proc Natl Acad Sci USA. 2004;101(23):8670–5. doi:10.1073/pnas.0402644101.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  22. Brincks EL, Katewa A, Kucaba TA, Griffith TS, Legge KL. CD8 T cells utilize TRAIL to control influenza virus infection. J Immunol. 2008;181(7):4918–25.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  23. GeurtsvanKessel CH, Willart MA, van Rijt LS, Muskens F, Kool M, Baas C, et al. Clearance of influenza virus from the lung depends on migratory langerin+ CD11b- but not plasmacytoid dendritic cells. J Exp Med. 2008;205(7):1621–34. doi:10.1084/jem.20071365.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  24. Kim TS, Braciale TJ. Respiratory dendritic cell subsets differ in their capacity to support the induction of virus-specific cytotoxic CD8+ T cell responses. PLoS One. 2009;4(1):e4204. doi:10.1371/journal.pone.0004204.

    Article  PubMed Central  PubMed  Google Scholar 

  25. Legge KL, Braciale TJ. Accelerated migration of respiratory dendritic cells to the regional lymph nodes is limited to the early phase of pulmonary infection. Immunity. 2003;18(2):265–77.

    Article  CAS  PubMed  Google Scholar 

  26. McGill J, Legge KL. Cutting edge: contribution of lung-resident T cell proliferation to the overall magnitude of the antigen-specific CD8 T cell response in the lungs following murine influenza virus infection. J Immunol. 2009;183(7):4177–81. doi:10.4049/jimmunol.0901109.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  27. McGill J, Van Rooijen N, Legge KL. Protective influenza-specific CD8 T cell responses require interactions with dendritic cells in the lungs. J Exp Med. 2008;205(7):1635–46. doi:10.1084/jem.20080314.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  28. McGill J, Van Rooijen N, Legge KL. IL-15 trans-presentation by pulmonary dendritic cells promotes effector CD8 T cell survival during influenza virus infection. J Exp Med. 2010;207(3):521–34. doi:10.1084/jem.20091711.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  29. Halle S, Dujardin HC, Bakocevic N, Fleige H, Danzer H, Willenzon S, et al. Induced bronchus-associated lymphoid tissue serves as a general priming site for T cells and is maintained by dendritic cells. J Exp Med. 2009;206(12):2593–601. doi:10.1084/jem.20091472.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  30. Marshall DR, Turner SJ, Belz GT, Wingo S, Andreansky S, Sangster MY, et al. Measuring the diaspora for virus-specific CD8+ T cells. Proc Natl Acad Sci USA. 2001;98(11):6313–8. doi:10.1073/pnas.101132698.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  31. Kohlmeier JE, Miller SC, Woodland DL. Cutting edge: antigen is not required for the activation and maintenance of virus-specific memory CD8+ T cells in the lung airways. J Immunol. 2007;178(8):4721–5.

    Article  CAS  PubMed  Google Scholar 

  32. Hogan RJ, Usherwood EJ, Zhong W, Roberts AA, Dutton RW, Harmsen AG, et al. Activated antigen-specific CD8+ T cells persist in the lungs following recovery from respiratory virus infections. J Immunol. 2001;166(3):1813–22.

    Article  CAS  PubMed  Google Scholar 

  33. Roberts AD, Woodland DL. Cutting edge: effector memory CD8+ T cells play a prominent role in recall responses to secondary viral infection in the lung. J Immunol. 2004;172(11):6533–7.

    Article  CAS  PubMed  Google Scholar 

  34. Sallusto F, Lenig D, Forster R, Lipp M, Lanzavecchia A. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature. 1999;401(6754):708–12. doi:10.1038/44385.

    Article  CAS  PubMed  Google Scholar 

  35. Wherry EJ, Teichgraber V, Becker TC, Masopust D, Kaech SM, Antia R, et al. Lineage relationship and protective immunity of memory CD8 T cell subsets. Nat Immunol. 2003;4(3):225–34. doi:10.1038/ni889.

    Article  CAS  PubMed  Google Scholar 

  36. Topham DJ, Castrucci MR, Wingo FS, Belz GT, Doherty PC. The role of antigen in the localization of naive, acutely activated, and memory CD8(+) T cells to the lung during influenza pneumonia. J Immunol. 2001;167(12):6983–90.

    Article  CAS  PubMed  Google Scholar 

  37. Yewdell JW, Bennink JR. Immunodominance in major histocompatibility complex class I-restricted T lymphocyte responses. Annu Rev Immunol. 1999;17:51–88. doi:10.1146/annurev.immunol.17.1.51.

    Article  CAS  PubMed  Google Scholar 

  38. Piet B, de Bree GJ, Smids-Dierdorp BS, van der Loos CM, Remmerswaal EB, von der Thusen JH, et al. CD8(+) T cells with an intraepithelial phenotype upregulate cytotoxic function upon influenza infection in human lung. J Clin Investig. 2011;121(6):2254–63. doi:10.1172/JCI44675.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  39. Moyron-Quiroz JE, Rangel-Moreno J, Hartson L, Kusser K, Tighe MP, Klonowski KD, et al. Persistence and responsiveness of immunologic memory in the absence of secondary lymphoid organs. Immunity. 2006;25(4):643–54. doi:10.1016/j.immuni.2006.08.022.

    Article  CAS  PubMed  Google Scholar 

  40. Kim TS, Hufford MM, Sun J, Fu YX, Braciale TJ. Antigen persistence and the control of local T cell memory by migrant respiratory dendritic cells after acute virus infection. J Exp Med. 2010;207(6):1161–72. doi:10.1084/jem.20092017.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  41. Inman CF, Singha S, Lewis M, Bradley B, Stokes C, Bailey M. Dendritic cells interact with CD4 T cells in intestinal mucosa. J Leukoc Biol. 2010;88(3):571–8. doi:10.1189/jlb.0310161.

    Article  CAS  PubMed  Google Scholar 

  42. Johansson-Lindbom B, Svensson M, Wurbel MA, Malissen B, Marquez G, Agace W. Selective generation of gut tropic T cells in gut-associated lymphoid tissue (GALT): requirement for GALT dendritic cells and adjuvant. J Exp Med. 2003;198(6):963–9. doi:10.1084/jem.20031244.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  43. Mora JR, Cheng G, Picarella D, Briskin M, Buchanan N, von Andrian UH. Reciprocal and dynamic control of CD8 T cell homing by dendritic cells from skin- and gut-associated lymphoid tissues. J Exp Med. 2005;201(2):303–16. doi:10.1084/jem.20041645.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  44. Klonowski KD, Marzo AL, Williams KJ, Lee SJ, Pham QM, Lefrancois L. CD8 T cell recall responses are regulated by the tissue tropism of the memory cell and pathogen. J Immunol. 2006;177(10):6738–46.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  45. Iijima N, Mattei LM, Iwasaki A. Recruited inflammatory monocytes stimulate antiviral Th1 immunity in infected tissue. Proc Natl Acad Sci USA. 2011;108(1):284–9. doi:10.1073/pnas.1005201108.

    Article  PubMed Central  PubMed  Google Scholar 

  46. Lehner T, Panagiotidi C, Bergmeier LA, Tao L, Brookes R, Gearing A, et al. Genital-associated lymphoid tissue in female non-human primates. Adv Exp Med Biol. 1995;371A:357–65.

    Article  CAS  PubMed  Google Scholar 

  47. Zhu J, Koelle DM, Cao J, Vazquez J, Huang ML, Hladik F, et al. Virus-specific CD8+ T cells accumulate near sensory nerve endings in genital skin during subclinical HSV-2 reactivation. J Exp Med. 2007;204(3):595–603. doi:10.1084/jem.20061792.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  48. Streilein JW. Lymphocyte traffic, T-cell malignancies and the skin. J Invest Dermatol. 1978;71(3):167–71.

    Article  CAS  PubMed  Google Scholar 

  49. Streilein JW. Skin-associated lymphoid tissues (SALT): origins and functions. J Invest Dermatol. 1983;80(Suppl):12s–6s.

    Article  PubMed  Google Scholar 

  50. Streilein JW. Circuits and signals of the skin-associated lymphoid tissues (SALT). J Invest Dermatol. 1985;85(1 Suppl):10s–3s.

    Article  CAS  PubMed  Google Scholar 

  51. Ginhoux F, Liu K, Helft J, Bogunovic M, Greter M, Hashimoto D, et al. The origin and development of nonlymphoid tissue CD103+ DCs. J Exp Med. 2009;206(13):3115–30. doi:10.1084/jem.20091756.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  52. Heath WR, Carbone FR. Dendritic cell subsets in primary and secondary T cell responses at body surfaces. Nat Immunol. 2009;10(12):1237–44. doi:10.1038/ni.1822.

    Article  CAS  PubMed  Google Scholar 

  53. Miller JC, Brown BD, Shay T, Gautier EL, Jojic V, Cohain A, et al. Deciphering the transcriptional network of the dendritic cell lineage. Nat Immunol. 2012;13(9):888–99. doi:10.1038/ni.2370.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  54. Toews GB, Bergstresser PR, Streilein JW. Langerhans cells: sentinels of skin associated lymphoid tissue. J Invest Dermatol. 1980;75(1):78–82.

    Article  CAS  PubMed  Google Scholar 

  55. Bedoui S, Whitney PG, Waithman J, Eidsmo L, Wakim L, Caminschi I, et al. Cross-presentation of viral and self antigens by skin-derived CD103+ dendritic cells. Nat Immunol. 2009;10(5):488–95. doi:10.1038/ni.1724.

    Article  CAS  PubMed  Google Scholar 

  56. McLachlan JB, Catron DM, Moon JJ, Jenkins MK. Dendritic cell antigen presentation drives simultaneous cytokine production by effector and regulatory T cells in inflamed skin. Immunity. 2009;30(2):277–88. doi:10.1016/j.immuni.2008.11.013.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  57. Seneschal J, Clark RA, Gehad A, Baecher-Allan CM, Kupper TS. Human epidermal Langerhans cells maintain immune homeostasis in skin by activating skin resident regulatory T cells. Immunity. 2012;36(5):873–84. doi:10.1016/j.immuni.2012.03.018.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  58. Bennett CL, Fallah-Arani F, Conlan T, Trouillet C, Goold H, Chorro L, et al. Langerhans cells regulate cutaneous injury by licensing CD8 effector cells recruited to the skin. Blood. 2011;117(26):7063–9. doi:10.1182/blood-2011-01-329185.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  59. Gebhardt T, Whitney PG, Zaid A, Mackay LK, Brooks AG, Heath WR, et al. Different patterns of peripheral migration by memory CD4+ and CD8+ T cells. Nature. 2011;477(7363):216–9. doi:10.1038/nature10339.

    Article  CAS  PubMed  Google Scholar 

  60. Heath WR, Carbone FR. The skin-resident and migratory immune system in steady state and memory: innate lymphocytes, dendritic cells and T cells. Nat Immunol. 2013;14(10):978–85. doi:10.1038/ni.2680.

    Article  CAS  PubMed  Google Scholar 

  61. Mackay LK, Stock AT, Ma JZ, Jones CM, Kent SJ, Mueller SN, et al. Long-lived epithelial immunity by tissue-resident memory T (TRM) cells in the absence of persisting local antigen presentation. Proc Natl Acad Sci USA. 2012;109(18):7037–42. doi:10.1073/pnas.1202288109.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  62. Hino K, Okuda M, Konishi T, Yamashita A, Kayano K, Kubota M, et al. Analysis of lymphoid follicles in liver of patients with chronic hepatitis C. Liver. 1992;12(6):387–91.

    Article  CAS  PubMed  Google Scholar 

  63. Shomer NH, Fox JG, Juedes AE, Ruddle NH. Helicobacter-induced chronic active lymphoid aggregates have characteristics of tertiary lymphoid tissue. Infect Immun. 2003;71(6):3572–7.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  64. Yoneyama H, Matsuno K, Zhang Y, Murai M, Itakura M, Ishikawa S, et al. Regulation by chemokines of circulating dendritic cell precursors, and the formation of portal tract-associated lymphoid tissue, in a granulomatous liver disease. J Exp Med. 2001;193(1):35–49.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  65. Crispe IN. The liver as a lymphoid organ. Annu Rev Immunol. 2009;27:147–63. doi:10.1146/annurev.immunol.021908.132629.

    Article  CAS  PubMed  Google Scholar 

  66. Huang LR, Wohlleber D, Reisinger F, Jenne CN, Cheng RL, Abdullah Z, et al. Intrahepatic myeloid-cell aggregates enable local proliferation of CD8(+) T cells and successful immunotherapy against chronic viral liver infection. Nat Immunol. 2013;14(6):574–83. doi:10.1038/ni.2573.

    Article  CAS  PubMed  Google Scholar 

  67. Lauer GM. Hepatitis C virus-specific CD8+ T cells restricted by donor HLA alleles following liver transplantation. Liver Transpl. 2005;11(7):848–50. doi:10.1002/lt.20423.

    Article  PubMed  Google Scholar 

  68. Bowen DG, Zen M, Holz L, Davis T, McCaughan GW, Bertolino P. The site of primary T cell activation is a determinant of the balance between intrahepatic tolerance and immunity. J Clin Invest. 2004;114(5):701–12. doi:10.1172/JCI21593.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  69. Klein I, Crispe IN. Complete differentiation of CD8+ T cells activated locally within the transplanted liver. J Exp Med. 2006;203(2):437–47. doi:10.1084/jem.20051775.

    Article  PubMed Central  PubMed  Google Scholar 

  70. Klonowski KD, Williams KJ, Marzo AL, Blair DA, Lingenheld EG, Lefrancois L. Dynamics of blood-borne CD8 memory T cell migration in vivo. Immunity. 2004;20(5):551–62.

    Article  CAS  PubMed  Google Scholar 

  71. Wakim LM, Woodward-Davis A, Bevan MJ. Memory T cells persisting within the brain after local infection show functional adaptations to their tissue of residence. Proc Natl Acad Sci USA. 2010;107(42):17872–9. doi:10.1073/pnas.1010201107.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  72. Wakim LM, Waithman J, van Rooijen N, Heath WR, Carbone FR. Dendritic cell-induced memory T cell activation in nonlymphoid tissues. Science. 2008;319(5860):198–202. doi:10.1126/science.1151869.

    Article  CAS  PubMed  Google Scholar 

  73. Bartholomaus I, Kawakami N, Odoardi F, Schlager C, Miljkovic D, Ellwart JW, et al. Effector T cell interactions with meningeal vascular structures in nascent autoimmune CNS lesions. Nature. 2009;462(7269):94–8. doi:10.1038/nature08478.

    Article  PubMed  Google Scholar 

  74. Bulloch K, Miller MM, Gal-Toth J, Milner TA, Gottfried-Blackmore A, Waters EM, et al. CD11c/EYFP transgene illuminates a discrete network of dendritic cells within the embryonic, neonatal, adult, and injured mouse brain. J Comp Neurol. 2008;508(5):687–710. doi:10.1002/cne.21668.

    Article  PubMed  Google Scholar 

  75. Reboldi A, Coisne C, Baumjohann D, Benvenuto F, Bottinelli D, Lira S, et al. C–C chemokine receptor 6-regulated entry of TH-17 cells into the CNS through the choroid plexus is required for the initiation of EAE. Nat Immunol. 2009;10(5):514–23. doi:10.1038/ni.1716.

    Article  CAS  PubMed  Google Scholar 

  76. Anandasabapathy N, Victora GD, Meredith M, Feder R, Dong B, Kluger C, et al. Flt3L controls the development of radiosensitive dendritic cells in the meninges and choroid plexus of the steady-state mouse brain. J Exp Med. 2011;208(8):1695–705. doi:10.1084/jem.20102657.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  77. Milo I, Sapoznikov A, Kalchenko V, Tal O, Krauthgamer R, van Rooijen N, et al. Dynamic imaging reveals promiscuous cross presentation of blood-borne antigens to naive CD8+ T cells in the bone marrow. Blood. 2013;122(2):193–208. doi:10.1182/blood-2012-01-401265.

    Article  CAS  PubMed  Google Scholar 

  78. Muniz LR, Pacer ME, Lira SA, Furtado GC. A critical role for dendritic cells in the formation of lymphatic vessels within tertiary lymphoid structures. J Immunol. 2011;187(2):828–34. doi:10.4049/jimmunol.1004233.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  79. Rangel-Moreno J, Moyron-Quiroz JE, Carragher DM, Kusser K, Hartson L, Moquin A, et al. Omental milky spots develop in the absence of lymphoid tissue-inducer cells and support B and T cell responses to peritoneal antigens. Immunity. 2009;30(5):731–43. doi:10.1016/j.immuni.2009.03.014.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Emma E. Hornick for her critical reading of this manuscript. This work was supported by National Institutes of Health awards AI071085 (to K.L.L.), T32 AI007533 (to E.A.H.), and T32 AI007485 (to E.A.H.).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kevin L. Legge.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hemann, E.A., Legge, K.L. Peripheral regulation of T cells by dendritic cells during infection. Immunol Res 59, 66–72 (2014). https://doi.org/10.1007/s12026-014-8530-3

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12026-014-8530-3

Keywords

Navigation