Innate immune responses to herpes simplex virus type 2 influence skin homing molecule expression by memory CD4+ lymphocytes

Journal of Virology

Volumn 80, Issue 6, 2006, Pages 2863-2872

  Koelle, David M ^a,b,c,d   Huang, Jay ^a   Hensel, Michael T ^a   McClurkan, Christopher L ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b USA   (United States)

^c BENAROYA RESEARCH INSTITUTE   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN; CUTANEOUS LYMPHOCYTE ASSOCIATED ANTIGEN; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; HOMING RECEPTOR; INTERFERON; INTERLEUKIN 12; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; VIRUS ANTIGEN;

ARTICLE; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; HERPES SIMPLEX VIRUS 2; HUMAN; IN VITRO STUDY; INNATE IMMUNITY; LIGAND BINDING; MEMORY T LYMPHOCYTE; MONOCYTE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRUS REPLICATION;

ANTIGENS, NEOPLASM; ANTIGENS, VIRAL; CD4-POSITIVE T-LYMPHOCYTES; DENDRITIC CELLS; HERPESVIRUS 2, HUMAN; HUMANS; IMMUNITY, NATURAL; IMMUNOLOGIC MEMORY; LYMPHOCYTE ACTIVATION; MEMBRANE GLYCOPROTEINS; RECEPTORS, LYMPHOCYTE HOMING; SKIN;

HUMAN HERPESVIRUS 2; SIMPLEXVIRUS;

EID: 33644761955     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.80.6.2863-2872.2006     Document Type: Article

References (64)

1. Alcami, A., J. A. Symons, and G. L. Smith. 2000. The vaccinia virus soluble alpha/beta interferon (IFN) receptor binds to the cell surface and protects cells from the antiviral effects of IFN. J. Virol. 74:11230-11239.
2. Allan, R. S., C. M. Smith, G. T. Belz, A. L. van Lint, L. M. Wakim, W. R. Heath, and F. R. Carbone. 2003. Epidermal viral immunity induced by CD8alpha+ dendritic cells but not by Langerhans cells. Science 301:1925-1928.
3. Ankel, H., D. F. Westra, S. Welling-Wester, and P. Lebon. 1998. Induction of interferon-alpha by glycoprotein D of herpes simplex virus: a possible role of chemokine receptors. Virology 251:317-326.
4. Armerding, D., and T. S. Kupper. 1999. Functional cutaneous lymphocyte antigen can be induced in essentially all peripheral blood T lymphocytes. Int. Arch. Allergy Immunol. 119:212-222.
5. Bangert, C., J. Friedl, G. Stary, G. Stingl, and T. Kopp. 2003. Immunopathologic features of allergic contact dermatitis in humans: participation of plasmacytoid dendritic cells in the pathogenesis of the disease? J. Investig. Dermatol. 121:1409-1418.
6. Barcy, S., M. L. Huang, L. Corey, and D. M. Koelle. 2005. Longitudinal analysis of herpes simplex virus-specific CD4+ cell clonotypes in infected tissues and blood. J. Infect. Dis. 191:2012-2021.
7. Barry, S. M., D. G. Zisoulis, J. W. Neal, N. A. Clipstone, and G. S. Kansas. 2003. Induction of FucT-VII by the Ras/MAP kinase cascade in Jurkat T cells. Blood 102:1771-1778.
8. Campbell, D. J., C. H. Kim, and E. C. Butcher. 2003. Chemokines in the systemic organization of immunity. Immunol. Rev. 195:58-71.
9. Chehimi, J., D. E. Campbell, L. Azzoni, D. Bachelier, E. Papasawas, G. Jerandi, K. Mounzer, J. Kostman, G. Trinchieri, and L. J. Montaner. 2002. Persistent decreases in blood plasmacytoid dendritic cell number and function despite effective highly active antiretroviral therapy and increased blood myeloid dendritic cells in HIV-infected individuals. J. Immunol. 168:4796-4801.
10. Colantonio, L., B. Rossi, G. Constantin, and D. D'Ambrosio. 2004. Integration and independent acquisition of specialized skin- versus gut-homing and Th1 versus Th2 cytokine synthesis phenotypes in human CD4(+) T cells. Eur. J. Immunol. 34:2419-2429.
11. Cunningham, A. L., R. R. Turner, A. C. Miller, M. F. Para, and T. C. Merigan. 1985. Evolution of recurrent herpes simplex lesions: an immunohistologic study. J. Clin. Investig. 75:226-233.
12. Dai, J., N. J. Megjugorac, S. B. Amrute, and P. Fitzgerald-Bocarsly. 2004. Regulation of IFN regulatory factor-7 and IFN-alpha production by enveloped virus and lipopolysaccharide in human plasmacytoid dendritic cells. J. Immunol. 173:1535-1548.
13. Danke, N. A., D. M. Koelle, and W. W. Kwok. 2005. Persistence of HSV-2 VP16-specific CD4 T-cells. Hum. Immunol. 66:777-787.
14. Fieschi, C., and J. L. Casanova. 2003. The role of interleukin-12 in human infectious diseases: only a faint signature. Eur. J. Immunol. 33:1461-1464.
15. Fitzgerald-Bocarsly, P. 2002. Natural interferon-alpha producing cells: the plasmacytoid dendritic cells. BioTechniques 2002(Suppl.):16-20, 22, 24-29.
16. Fuhlbrigge, R. C., J. D. Kieffer, D. Armerding, and T. S. Kupper. 1997. Cutaneous lymphocyte antigen is a specialized form of PSGL-1 expressed on skin-homing T cells. Nature 389:978-981.
17. Gonzalez, J. C., W. W. Kwok, A. Wald, C. L. McClurkan, and D. M. Koelle. 2005. Programmed expression of cutaneous lymphocyte-associated antigen amongst circulating memory T-cells specific for HSV-2. J. Infect. Dis. 191: 243-254.
18. Hochrein, H., B. Schlatter, M. O'Keeffe, C. Wagner, F. Schmitz, M. Schiemann, S. Bauer, M. Suter, and H. Wagner. 2004. Herpes simplex virus type-1 induces IFN-alpha production via Toll-like receptor 9-dependent and -independent pathways. Proc. Natl. Acad. Sci. USA 101:11416-11421.
19. Ito, T., R. Amakawa, M. Inaba, S. Ikehara, K. Inaba, and S. Fukuhara. 2001. Differential regulation of human blood dendritic cell subsets by IFNs. J. Immunol. 166:2961-2969.
20. Iwata, M., A. Hirakiyama, Y. Eshima, H. Kagechika, C. Kate, and S.-Y. Song. 2004. Retinoic acid imprints gut-homing specificity on T cells. Immunity 21:527-538.
21. Kansas, G. S. 2004. Control of FucT-VII expression in CD4+ T cells. Ernst Schering Res. Found. Workshop 2004:95-107.
22. Koelle, D. M., H. Abbo, A. Peck, K. Ziegweid, and L. Corey. 1994. Direct recovery of HSV-specific T lymphocyte clones from human recurrent HSV-2 lesions. J. Infect. Dis. 169:956-961.
23. Koelle, D. M., L. Corey, R. L. Burke, R. J. Eisenberg, G. H. Cohen, R. Pichyangkura, and S. J. Triezenberg. 1994. Antigenic specificities of human CD4+ T cell clones recovered from recurrent genital HSV-2 lesions. J. Virol. 68:2803-2810.
24. Koelle, D. M., and L. Corey. 2003. Recent progress in herpes simplex virus immunobiology and vaccine research. Clin. Microbiol. Rev. 16:96-113.
25. Koelle, D. M., C. M. Posavad, G. R. Barnum, M. L. Johnson, J. M. Frank, and L. Corey. 1998. Clearance of HSV-2 from recurrent genital lesions correlates with infiltration of HSV-specific cytotoxic T lymphocytes. J. Clin. Investig. 101:1500-1508.
26. Koelle, D. M., Z. Liu, C. M. McClurkan, M. Topp, S. R. Riddell, E. G. Pamer, A. S. Johnson, A. Wald, and L. Corey. 2002. Expression of cutaneous lymphocyte-associated antigen by CD8+ T-cells specific for a skin-tropic virus. J. Clin. Investig. 110:537-548.
27. Koelle, D. M., J. C. Gonzalez, and A. S. Johnson. 2005. Homing in on the cellular immune response to HSV-2 in humans. Am. J. Reprod. Immunol. 53:172-181.
28. Koelle, D. M., J. Benedetti, A. Langenberg, and L. Corey. 1992. Asymptomatic reactivation of herpes simplex virus in women after the first episode of genital infection. Ann. Intern. Med. 116:433-437.
29. Kohrgruber, N., N. Halanek, M. Groger, D. Winter, K. Rappersberger, M. Schmitt-Egenolf, G. Stingl, and D. Maurer. 1999. Survival, maturation, and function of CD11c- and CD11c+ peripheral Wood dendritic cells are differentially regulated by cytokines. J. Immunol. 163:3250-3259.
30. Krug, A., G. D. Luker, W. Barchet, D. A. Leib, S. Akira, and M. Colonna. 2004. Herpes simplex virus type 1 activates murine natural interferon-producing cells through Toll-like receptor 9. Blood 103:1433-1437.
31. Kurt-Jones, E. A., M. Chan, S. Zhou, J. Wang, G. Reed, R. Bronson, M. M. Arnold, D. M. Knipe, and R. W. Finberg. 2004. Herpes simplex virus 1 interaction with Toll-like receptor 2 contributes to lethal encephalitis. Proc. Natl. Acad. Sci. USA 101:1315-1320.
32. Kwok, W. W., J. A. Gebe, A. Liu, S. Agar, N. Ptacek, J. Hammer, D. M. Koelle, and G. T. Nepom. 2001. Rapid epitope identification from complex class II-restricted T-cell antigens. Trends Immunol. 22:583-588.
33. Kwok, W. W., A. W. Liu, E. J. Novak, J. A. Gebe, S. N. Reymond, R. A. Ettinger, G. T. Nepom, and D. M. Koelle. 2000. HLA-DQ tetramers identify epitope-specific T-cells in peripheral blood of herpes simplex virus-2-infected individuals: direct detection of immunodominant antigen responsive cells. J. Immunol. 164:4244-4249.
34. Leung, D. Y., M. Gately, A. Trumble, B. Ferguson-Darnell, P. M. Schlievert, and L. J. Picker. 1995. Bacterial superantigens induce T cell expression of the skin-selective homing receptor, the cutaneous lymphocyte-associated antigen, via stimulation of interleukin 12 production. J. Exp. Med. 181:747-753.
35. Liu, Y. J. 2005. IPC: professional type 1 interferon-producing cells and plasmacytoid dendritic cell precursors. Annu. Rev. Immunol. 23:275-306.
36. Lund, J., A. Sato, S. Akira, R. Medzhitov, and H. Iwasaki. 2003. Toll-like receptor 9-mediated recognition of herpes simplex virus-2 by plasmacytoid dendritic cells. J. Exp. Med. 198:513-520.
37. Malmgaard, L., S. R. Paludan, S. C. Mogensen, and S. Ellerman-Eriksen. 2000. Herpes simplex virus type 2 induces secretion of IL-12 by macrophages through a mechanism involving NF-kappaB. J. Gen. Virol. 81:3011-3020.
38. Maly, P., A. Thall, B. Petryniak, C. E. Rogers, P. L. Smith, R. M. Marks, R. J. Kelly, K. M. Gersten, G. Cheng, T. L. Saunders, S. A. Camper, R. T. Camphausen, F. X. Sullivan, Y. Isogai, O. Hindsgaul, U. H. von Andrian, and J. B. Lowe. 1996. The alpha(1,3)fucosyltransferase Fuc-TVII controls leukocyte trafficking through an essential role in L-, E-, and P-selectin ligand biosynthesis. Cell 86:643-653.
39. Mendez-Samperio, P., M. Hernandez, and H. E. Ayala. 2000. Induction of transforming growth factor-beta 1 production in human cells by herpes simplex virus. J. Interferon Cytokine Res. 20:273-280.
40. Mora, J. R., G. Cheng, D. Picarella, M. Briskin, N. Buchanan, and U. H. von Andrian. 2005. Reciprocal and dynamic control of CD8 T cell homing by dendritic cells from skin- and gut-associated lymphoid tissues. J. Exp. Med. 201:303-316.
41. Morrison, L. A. 2004. The Toll of herpes simplex virus infection. Trends Microbiol. 12:353-356.
42. Nakayama, F., Y. Teraki, T. Kudo, A. Togayachi, H. Iwasaki, T. Tamatani, S. Nishihara, T. Mizukawa, T. Shiohara, and H. Narimatsu. 2000. Expression of cutaneous lymphocyte-associated antigen regulated by a set of glycosyltransferases in human T cells: involvement of alpha1,3-fucosyl transferase VII and beta1,4-galactosyltransferase I. J. Investig. Dermatol. 115:299-306.
43. Novak, E. J., A. W. Liu, J. A. Gebe, B. A. Falk, G. T. Nepom, D. M. Koelle, and W. W. Kwok. 2001. Tetramer-guided epitope mapping: rapid identification and characterization of immunodominant CD4+ T cell epitopes from complex antigens. J. Immunol. 166:6665-6670.
44. Otero, M., G. Nunnari, D. Leto, J. Sullivan, F. X. Wang, I. Frank, Y. Xu, C. Patel, G. Dornadula, J. Kulkosky, and R. J. Pomerantz. 2003. Peripheral blood dendritic cells are not a major reservoir for HIV type 1 in infected individuals on virally suppressive HAART. AIDS Res. Hum. Retrovir. 19: 1097-1103.
45. Picker, L. J., J. R. Treer, B. Ferguson-Darnell, P. A. Collins, P. R. Bergstresser, and L. W. M. M. Terstappen. 1993. Control of lymphocyte recirculation in man. II. Differential regulation of the cutaneous lymphocyte-associated antigen, a tissue-selective homing receptor for skin-homing T cells. J. Immunol. 150:1122-1136.
46. Pollara, G., M. Jones, M. E. Handley, M. Rajpopat, A. Kwan, R. S. Coffin, G. Foster, B. Chain, and D. R. Katz. 2004. Herpes simplex virus type-1-induced activation of myeloid dendritic cells: the roles of virus cell interaction and paracrine type I IFN secretion. J. Immunol. 173:4108-4119.
47. Posavad, C. M., S. Barcy, M. L. Huang, D. M. Koelle, S. J. Polyak, and L. Corey. 2000. Long-term persistence of herpes simplex virus-specific CD8+ CTL clones derived from genital lesions. J. Immunol. 165:1146-1152.
48. Salio, M., M. Cella, W. Vermi, F. Facchetti, M. J. Palmowski, C. L. Smith, D. Shepherd, M. Colonna, and V. Cerundolo. 2003. Plasmacytoid dendritic cells prime IFN-gamma-secreting melanoma-specific CD8 lymphocytes and are found in primary melanoma lesions. Eur. J. Immunol. 33:1052-1062.
49. Schaerli, P., L. Ebert, K. Willimann, A. Blaser, R. S. Roos, P. Loetscher, and B. Moser. 2004. A skin-selective homing mechanism for human immune surveillance T cells. J. Exp. Med. 199:1265-1275.
50. Schmitt, C., H. Fohrer, S. Beaudet, P. Palmer, M. J. Alpha, B. Canque, J. C. Gluckman, and A. H. Dalloul. 2000. Identification of mature and immature human thymic dendritic cells that differentially express HLA-DR and interleukin-3 receptor in vivo. J. Leukoc. Biol. 68:836-844.
51. Schneider, K., K. G. Potter, and C. F. Ware. 2004. Lymphotoxin and LIGHT signaling pathways and target genes. Immunol. Rev. 202:49-66.
52. Seneviratne, S. L., L. Jones, A. S. Bailey, R. V. Samuel, A. P. Black, and G. S. Ogg. 2005. Interleukin-4 induced down-regulation of skin homing receptor expression by human viral-specific CD8+ T cells may contribute to atopic risk of cutaneous infection. Clin. Exp. Immunol. 141:107-115.
53. Siegal, F. P., N. Kadowaki, M. Shodell, P. A. Fitzgerald-Bocarsly, K. Shah, S. Ho, S. Antonenko, and Y.-J. Liu. 1999. The nature of the principle type 1 interferon-producing cells in human blood. Science 284:1835-1837.
54. Sigmundsdottir, H., J. E. Gudjonsson, and H. Valdimarsson. 2003. Interleukin-12 alone cannot enhance the expression of the cutaneous lymphocyte associated antigen (CLA) by superantigen-stimulated T lymphocytes. Clin. Exp. Immunol. 132:430-435.
55. Swetter, S. M., E. L. Hill, E. L. Kern, D. M. Koelle, C. M. Posavad, and S. Safrin. 1998. Chronic vulvar ulceration in an immunocompetent woman due to acyclovir-resistant, thymidine-kinase-deficient herpes simplex virus. J. Infect. Dis. 177:543-550.
56. Syrbe, U., S. Jennrich, A. Schottelius, A. Richter, A. Radbruch, and A. Hamann. 2004. Differential regulation of P-selectin ligand expression in naive versus memory CD4+ T cells: evidence for epigenetic regulation of involved glycosyltransferase genes. Blood 104:3243-3248.
57. Takahashi, R., Y. Mizukawa, Y. Yamazaki, K. Hayakawa, J. Hayakawa, A. Kudo, and T. Shiohara. 2003. In vitro differentiation from naive to mature E-selectin binding CD4 T cells: acquisition of skin-homing properties occurs independently of cutaneous lymphocyte antigen expression. J. Immunol. 171:5769-5777.
58. + herpes simplex virus-specific cytotoxic T lymphocyte clones recognize diverse virion protein antigens. J. Virol. 66:1622-1634.
59. Wagers, A. J., and G. S. Kansas. 2000. Potent induction of alpha(1,3)-fucosyltransferase VII in activated CD4+ T cells by TGF-beta 1 through a p38 mitogen-activated protein kinase-dependent pathway. J. Immunol. 165: 5011-5016.
60. Wald, A., J. Zeh, S. Selke, T. Warren, A. Ryncarz, R. Ashley, J. N. Krieger, and L. Corey. 2000. Reactivation of genital herpes type 2 infection in asymptomatic seropositive persons. N. Engl. J. Med. 342:844-850.
61. White, S. J., G. H. Underhill, M. H. Kaplan, and G. S. Kansas. 2001. Cutting edge: differential requirements for stat4 in expression of glycosyltransferases responsible for selectin ligand formation in Th1 cells. J. Immunol. 167:628-631.
62. Wickham, S., B. Lu, J. Ash, and D. J. Carr. 2005. Chemokine receptor deficiency is associated with increased chemokine expression in the peripheral and central nervous systems and increased resistance to herpetic encephalitis. J. Neuroimmunol. 162:51-59.
63. Wollenberg, A., M. Wagner, S. Gunther, A. Towarowski, E. Tuma, M. Moderer, S. Rothenfusser, S. Wetzel, S. Endres, and G. Hartmann. 2002. Plasmacytoid dendritic cells: a new cutaneous dendritic cell subset with distinct role in inflammatory skin diseases. J. Investig. Dermatol. 119:1096-1102.
64. Zhao, X., E. Deak, K. Soderberg, M. Linehan, D. Spezzano, J. Zhu, D. M. Knipe, and A. Iwasaki. 2003. Vaginal submucosal dendritic cells, but not Langerhans cells, induce protective Th1 responses to herpes simplex virus-2. J. Exp. Med. 197:153-162.