Relay of Herpes Simplex Virus between Langerhans Cells and Dermal Dendritic Cells in Human Skin

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Herpes Simplex Virus (HSV) is a highly prevalent virus that causes cold sores and genital herpes but also increases the chance of contracting HIV by several folds. In fact, most new cases of HIV in Africa occur in people infected with HSV. Thus, a protective HSV vaccine would have a large impact on public health. Currently, the process by which immunity to HSV is generated is incompletely understood. Paradoxically, the first immune cells to become infected, Langerhans cells in the epidermis, are not the cells that initiate the immune response, while the dermal dendritic cells thought to be responsible for initiating the immune response are not likely to be infected. Here, we have shown, in human skin models and genital herpes lesion biopsies, an interaction between these dendritic cells that could relay HSV to the lymph node. HSV is taken up by the epidermal Langerhans cells that then migrate into the dermis, die and are taken up by another subset of dermal dendritic cells—the homologs of those in mice which stimulate HSV-specific T cells in the lymph node. Thus, a mucosal or intradermal vaccine targeting these two dendritic cells may be required.

Vyšlo v časopise: Relay of Herpes Simplex Virus between Langerhans Cells and Dermal Dendritic Cells in Human Skin. PLoS Pathog 11(4): e32767. doi:10.1371/journal.ppat.1004812
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004812

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Zdroje

1. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature. 1998;392(6673):245–52. 9521319

2. Cunningham AL, Diefenbach RJ, Miranda-Saksena M, Bosnjak L, Kim M, Jones C, et al. The cycle of human herpes simplex virus infection: virus transport and immune control. J Infect Dis. 2006;194 Suppl 1:S11–8. 16921466

3. Su SJ, Wu HH, Lin YH, Lin HY. Comparative studies of types 1 and 2 herpes simplex virus infection of cultured normal keratinocytes. J Clin Pathol. 1995;48(1):75–9. 7706526

4. Yoshida Y, Li Z, Kurokawa M, Kawana T, Imakita M, Shiraki K. Growth of herpes simplex virus in epidermal keratinocytes determines cutaneous pathogenicity in mice. J Med Virol. 2005;75(3):421–6. 15648069

5. Puttur FK, Fernandez MA, White R, Roediger B, Cunningham AL, Weninger W, et al. Herpes simplex virus infects skin gamma delta T cells before Langerhans cells and impedes migration of infected Langerhans cells by inducing apoptosis and blocking E-cadherin downregulation. J Immunol. 2010;185(1):477–87. doi: 10.4049/jimmunol.0904106 20519652

6. Koelle DM, Corey L. Recent progress in herpes simplex virus immunobiology and vaccine research. Clin Microbiol Rev. 2003;16(1):96–113. 12525427

7. Ashley R, Mertz GJ, Corey L. Detection of asymptomatic herpes simplex virus infections after vaccination. J Virol. 1987;61(2):264–8. 3806788

8. Reeves WC, Corey L, Adams HG, Vontver LA, Holmes KK. Risk of recurrence after first episodes of genital herpes. Relation to HSV type and antibody response. N Engl J Med. 1981;305(6):315–9. 6264300

9. Harrison CJ, Miller RL, Bernstein DI. Posttherapy suppression of genital herpes simplex virus (HSV) recurrences and enhancement of HSV-specific T-cell memory by imiquimod in guinea pigs. Antimicrob Agents Chemother. 1994;38(9):2059–64. 7811019

10. Manickan E, Rouse BT. Roles of different T-cell subsets in control of herpes simplex virus infection determined by using T-cell-deficient mouse-models. J Virol. 1995;69(12):8178–9. 7494346

11. Cunningham AL, Turner RR, Miller AC, Para MF, Merigan TC. Evolution of recurrent herpes simplex lesions. An immunohistologic study. J Clin Invest. 1985;75(1):226–33. 3880773

12. Koelle DM, Liu Z, McClurkan CM, Topp MS, Riddell SR, Pamer EG, et al. Expression of cutaneous lymphocyte-associated antigen by CD8(+) T cells specific for a skin-tropic virus. J Clin Invest. 2002;110(4):537–48. 12189248

13. 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 21841802

14. 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. 17325200

15. Sprecher E, Becker Y. Skin Langerhans cells play an essential role in the defense against HSV-1 infection. Arch Virol. 1986;91(3–4):341–9. 3778212

16. Zhao X, Deak E, Soderberg K, Linehan M, Spezzano D, Zhu J, et al. Vaginal submucosal dendritic cells, but not Langerhans cells, induce protective Th1 responses to herpes simplex virus-2. J Exp Med. 2003;197(2):153–62. 12538655

17. Bachem A, Guttler S, Hartung E, Ebstein F, Schaefer M, Tannert A, et al. Superior antigen cross-presentation and XCR1 expression define human CD11c+CD141+ cells as homologues of mouse CD8+ dendritic cells. J Exp Med. 2010;207(6):1273–81. doi: 10.1084/jem.20100348 20479115

18. 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 19349986

19. Allan RS, Smith CM, Belz GT, van Lint AL, Wakim LM, Heath WR, et al. Epidermal viral immunity induced by CD8alpha+ dendritic cells but not by Langerhans cells. Science. 2003;301(5641):1925–8. 14512632

20. Poulin LF, Salio M, Griessinger E, Anjos-Afonso F, Craciun L, Chen JL, et al. Characterization of human DNGR-1+ BDCA3+ leukocytes as putative equivalents of mouse CD8alpha+ dendritic cells. J Exp Med. 2010;207(6):1261–71. doi: 10.1084/jem.20092618 20479117

21. Haniffa M, Shin A, Bigley V, McGovern N, Teo P, See P, et al. Human tissues contain CD141hi cross-presenting dendritic cells with functional homology to mouse CD103+ nonlymphoid dendritic cells. Immunity. 2012;37(1):60–73. doi: 10.1016/j.immuni.2012.04.012 22795876

22. Schlitzer A, Ginhoux F. Organization of the mouse and human DC network. Curr Opin Immunol. 2014;26:90–9. doi: 10.1016/j.coi.2013.11.002 24556405

23. Edelson BT, Kc W, Juang R, Kohyama M, Benoit LA, Klekotka PA, et al. Peripheral CD103+ dendritic cells form a unified subset developmentally related to CD8alpha+ conventional dendritic cells. J Exp Med. 2010;207(4):823–36. doi: 10.1084/jem.20091627 20351058

24. 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 20008528

25. Segura E, Durand M, Amigorena S. Similar antigen cross-presentation capacity and phagocytic functions in all freshly isolated human lymphoid organ-resident dendritic cells. J Exp Med. 2013;210(5):1035–47. doi: 10.1084/jem.20121103 23569327

26. Engering A, Geijtenbeek TB, van Vliet SJ, Wijers M, van Liempt E, Demaurex N, et al. The dendritic cell-specific adhesion receptor DC-SIGN internalizes antigen for presentation to T cells. J Immunol. 2002;168(5):2118–26. 11859097

27. McGovern N, Schlitzer A, Gunawan M, Jardine L, Shin A, Poyner E, et al. Human Dermal CD14(+) Cells Are a Transient Population of Monocyte-Derived Macrophages. Immunity. 2014;41(3):465–77. doi: 10.1016/j.immuni.2014.08.006 25200712

28. Saksena MM, Wakisaka H, Tijono B, Boadle RA, Rixon F, Takahashi H, et al. Herpes simplex virus type 1 accumulation, envelopment, and exit in growth cones and varicosities in mid-distal regions of axons. J Virol. 2006;80(7):3592–606. 16537627

29. Kim M, Osborne NR, Zeng W, Donaghy H, McKinnon K, Jackson DC, et al. Herpes simplex virus antigens directly activate NK cells via TLR2, thus facilitating their presentation to CD4 T lymphocytes. J Immunol. 2012;188(9):4158–70. doi: 10.4049/jimmunol.1103450 22467654

30. Nasr N, Lai J, Botting RA, Mercier SK, Harman AN, Kim M, et al. Inhibition of Two Temporal Phases of HIV-1 Transfer from Primary Langerhans Cells to T Cells: The Role of Langerin. J Immunol. 2014;193(5):2554–64. doi: 10.4049/jimmunol.1400630 25070850

31. Fontaine-Rodriguez EC, Knipe DM. Herpes simplex virus ICP27 increases translation of a subset of viral late mRNAs. J Virol. 2008;82(7):3538–45. doi: 10.1128/JVI.02395-07 18216091

32. O'Toole EA. Extracellular matrix and keratinocyte migration. Clin Exp Dermatol. 2001;26(6):525–30. 11678882

33. Tokumaru S, Sayama K, Shirakata Y, Komatsuzawa H, Ouhara K, Hanakawa Y, et al. Induction of keratinocyte migration via transactivation of the epidermal growth factor receptor by the antimicrobial peptide LL-37. J Immunol. 2005;175(7):4662–8. 16177113

34. Eidsmo L, Allan R, Caminschi I, van Rooijen N, Heath WR, Carbone FR. Differential migration of epidermal and dermal dendritic cells during skin infection. J Immunol. 2009;182(5):3165–72. doi: 10.4049/jimmunol.0802950 19234214

35. Bosnjak L, Miranda-Saksena M, Koelle DM, Boadle RA, Jones CA, Cunningham AL. Herpes simplex virus infection of human dendritic cells induces apoptosis and allows cross-presentation via uninfected dendritic cells. J Immunol. 2005;174(4):2220–7. 15699155

36. Peng Y, Martin DA, Kenkel J, Zhang K, Ogden CA, Elkon KB. Innate and adaptive immune response to apoptotic cells. J Autoimmun. 2007;29(4):303–9. 17888627

37. Huysamen C, Willment JA, Dennehy KM, Brown GD. CLEC9A is a novel activation C-type lectin-like receptor expressed on BDCA3+ dendritic cells and a subset of monocytes. J Biol Chem. 2008;283(24):16693–701. doi: 10.1074/jbc.M709923200 18408006

38. Caminschi I, Proietto AI, Ahmet F, Kitsoulis S, Shin Teh J, Lo JC, et al. The dendritic cell subtype-restricted C-type lectin Clec9A is a target for vaccine enhancement. Blood. 2008;112(8):3264–73. doi: 10.1182/blood-2008-05-155176 18669894

39. Zhang JG, Czabotar PE, Policheni AN, Caminschi I, Wan SS, Kitsoulis S, et al. The dendritic cell receptor Clec9A binds damaged cells via exposed actin filaments. Immunity. 2012;36(4):646–57. doi: 10.1016/j.immuni.2012.03.009 22483802

40. Harman AN, Bye CR, Nasr N, Sandgren KJ, Kim M, Mercier SK, et al. Identification of lineage relationships and novel markers of blood and skin human dendritic cells. J Immunol. 2013;190(1):66–79. doi: 10.4049/jimmunol.1200779 23183897