Retinoic acid as a vaccine adjuvant enhances CD8+ T cell response and mucosal protection from viral challenge

Journal of Virology

Volumn 85, Issue 16, 2011, Pages 8316-8327

  Tan, Xuefang ^a   Sande, Jamie L ^a   Pufnock, Jeffrey S ^b   Blattman, Joseph N ^a,b   Greenberg, Philip D ^a,b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b Fred Hutchinson Cancer Research Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; CHEMOKINE RECEPTOR CCR9; LYMPHOCYTIC CHORIOMENINGITIS VIRUS GLYCOPROTEIN; MODIFIED VACCINIA VIRUS ANKARA 5T4 VACCINE; RETINOIC ACID; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN;

ADJUVANT THERAPY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; DRUG MECHANISM; DRUG POTENTIATION; DRUG SPECIFICITY; EFFECTOR CELL; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INTESTINE MUCOSA; LYMPHOCYTE COUNT; LYMPHOCYTE PROLIFERATION; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MEMORY T LYMPHOCYTE; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; SYSTEMIC THERAPY; T LYMPHOCYTE ACTIVATION; VACCINATION; VACCINIA VIRUS; VAGINA MUCOSA; VIRUS EXPRESSION; VIRUS RECOMBINANT; VIRUS REPLICATION; VIRUS RESISTANCE;

ADENOVIRIDAE; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MUS; VACCINIA VIRUS; VACCINIA VIRUS ANKARA;

EID: 79961181485     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00781-11     Document Type: Article

References (64)

1. Agace, W. W. 2006. Tissue-tropic effector T cells: generation and targeting opportunities. Nat. Rev. Immunol. 6:682-692.
2. Belyakov, I. M., and J. A. Berzofsky. 2004. Immunobiology of mucosal HIV infection and the basis for development of a new generation of mucosal AIDS vaccines. Immunity 20:247-253.
3. Belyakov, I. M., et al. 2006. Impact of vaccine-induced mucosal high-avidity CD8+ CTLs in delay of AIDS viral dissemination from mucosa. Blood 107:3258-3264.
4. Benson, M. J., K. Pino-Lagos, M. Rosemblatt, and R. J. Noelle. 2007. Alltrans retinoic acid mediates enhanced Treg cell growth, differentiation, and gut homing in the face of high levels of co-stimulation. J. Exp. Med. 204: 1765-1774.
5. Berger, R., et al. 2007. Tretinoin gel microspheres 0.04% versus 0.1% in adolescents and adults with mild to moderate acne vulgaris: a 12-week, multicenter, randomized, double-blind, parallel-group, phase IV trial. Clin. Ther. 29:1086-1097.
6. Berlin, C., et al. 1995. Alpha 4 integrins mediate lymphocyte attachment and rolling under physiologic flow. Cell 80:413-422.
7. Campbell, D. J., and E. C. Butcher. 2002. Intestinal attraction: CCL25 functions in effector lymphocyte recruitment to the small intestine. J. Clin. Invest. 110:1079-1081.
8. Cepek, K. L., et al. 1994. Adhesion between epithelial cells and T lymphocytes mediated by E-cadherin and the alpha E beta 7 integrin. Nature 372:190-193.
9. Chiba, K. 2005. FTY720, a new class of immunomodulator, inhibits lymphocyte egress from secondary lymphoid tissues and thymus by agonistic activity at sphingosine 1-phosphate receptors. Pharmacol. Ther. 108:308-319.
10. Coombes, J. L., et al. 2007. A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism. J. Exp. Med. 204:1757-1764.
11. Eksteen, B., et al. 2009. Gut homing receptors on CD8 T cells are retinoic acid dependent and not maintained by liver dendritic or stellate cells. Gastroenterology 137:320-329.
12. Engedal, N., T. Gjevik, R. Blomhoff, and H. K. Blomhoff. 2006. All-trans retinoic acid stimulates IL-2-mediated proliferation of human T lymphocytes: early induction of cyclin D3. J. Immunol. 177:2851-2861.
13. Geissmann, F., et al. 2003. Retinoids regulate survival and antigen presentation by immature dendritic cells. J. Exp. Med. 198:623-634.
14. Genescà, M., et al. 2008. Protective attenuated lentivirus immunization induces SIV-specific T cells in the genital tract of rhesus monkeys. Mucosal Immunol. 1:219-228.
15. Gollnick, H., et al. 2003. Management of acne: a report from a global alliance to improve outcomes in acne. J. Am. Acad. Dermatol. 49:S1-37.
16. Goodsell, A., et al. 2008. Beta7-integrin-independent enhancement of mucosal and systemic anti-HIV antibody responses following combined mucosal and systemic gene delivery. Immunology 123:378-389.
17. Hammerschmidt, S. I., et al. 2008. Stromal mesenteric lymph node cells are essential for the generation of gut-homing T cells in vivo. J. Exp. Med. 205:2483-2490.
18. Heyday, A., E. Theodoridis, E. Ramsburg, and J. Shires. 2001. Intraepithelial lymphocytes: exploring the third way in immunology. Nat. Immunol. 2:997-1003.
19. Hikono, H., et al. 2006. T-cell memory and recall responses to respiratory virus infections. Immunol. Rev. 211:119-132.
20. Hladik, F., G. Lentz, E. Delpit, A. McElroy, and M. J. McElrath. 1999. Coexpression of CCR5 and IL-2 in human genital but not blood T cells: implications for the ontogeny of the CCR5+ Th1 phenotype. J. Immunol. 163:2306-2313.
21. Ho, W. Y., H. N. Nguyen, M. Wolfl, J. Kuball, and P. D. Greenberg. 2006. In vitro methods for generating CD8+ T-cell clones for immunotherapy from the naïve repertoire. J. Immunol. Methods 310:40-52.
22. Holmgren, J., and C. Czerkinsky. 2005. Mucosal immunity and vaccines. Nat. Med. 11:S45-53.
23. Holmgren, J., A. M. Harandi, and C. Czerkinsky. 2005. Mucosal adjuvants and anti-infection and anti-immunopathology vaccines based on cholera toxin, cholera toxin B subunit and CpG DNA. Immunol. Lett. 97:181-188.
24. Iwata, M. 2009. Retinoic acid production by intestinal dendritic cells and its role in T-cell trafficking. Semin. Immunol. 21:8-13.
25. Iwata, M., et al. 2004. Retinoic acid imprints gut-homing specificity on T cells. Immunity 21:527-538.
26. Johansson-Lindbom, B., and W. W. Agace. 2004. Vitamin A helps gut T cells find their way in the dark. Nat. Med. 10:1300-1301.
27. Johansson-Lindbom, B., et al. 2005. Functional specialization of gut CD103+ dendritic cells in the regulation of tissue-selective T cell homing. J. Exp. Med. 202:1063-1073.
28. Johansson-Lindbom, B., et al. 2003. Selective generation of gut tropic T cells in gut-associated lymphoid tissue (GALT): requirement for GALT dendritic cells and adjuvant. J. Exp. Med. 198:963-969.
29. Kelly, K. A., and R. G. Rank. 1997. Identification of homing receptors that mediate the recruitment of CD4 T cells to the genital tract following intravaginal infection with Chlamydia trachomatis. Infect. Immun. 65:5198-5208.
30. Krautheim, M., and H. P. M. Gollnick. 2004. Acne: topical treatment. Clin. Dermatol. 22:398-407.
31. Lefrançois, L., and A. L. Marzo. 2006. The descent of memory T-cell subsets. Nat. Rev. Immunol. 6:618-623.
32. Lefrancois, L., et al. 1999. The role of β integrins in CD8 T cell trafficking during an antiviral immune response. J. Exp. Med. 189:1631-1638.
33. Li, Q., et al. 2009. Visualizing antigen-specific and infected cells in situ predicts outcomes in early viral infection. Science 323:1726-1729.
34. Manicassamy, S., and B. Pulendran. 2009. Retinoic acid-dependent regulation of immune responses by dendritic cells and macrophages. Semin. Immunol. 21:22-27.
35. Martin, M. P. et al. 2010. Adjuvanted influenza vaccine administered intradermally elicits robust long-term immune responses that confer protection from lethal challenge. PLoS One 5:e10897.
36. Masopust, D., et al. 2010. Dynamic T cell migration program provides resident memory within intestinal epithelium. J. Exp. Med. 207:553-564.
37. Masopust, D., V. Vezys, A. L. Marzo, and L. Lefrançois. 2001. Preferential localization of effector memory cells in nonlymphoid tissue. Science 291: 2413-2417.
38. Mohty, M., et al. 2003. All-trans retinoic acid skews monocyte differentiation into interleukin-12-secreting dendritic-like cells. Br. J. Haematol. 122:829-836.
39. Mora, J. R., et al. 2006. Generation of gut-homing IgA-secreting B cells by intestinal dendritic cells. Science 314:1157-1160.
40. Mora, J. R., et al. 2003. Selective imprinting of gut-homing T cells by Peyer's patch dendritic cells. Nature 424:88-93.
41. Mucida, D., et al. 2007. Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid. Science 317:256-260.
42. Neutra, M. R., and P. A. Kozlowski. 2006. Mucosal vaccines: the promise and the challenge. Nat. Rev. Immunol. 6:148-158.
43. Pinschewer, D. D., et al. 2000. FTY720 immunosuppression impairs effector T cell peripheral homing without affecting induction, expansion, and memory. J. Immunol. 164:5761-5770.
44. Pizza, M., et al. 2001. Mucosal vaccines: non toxic derivatives of LT and CT as mucosal adjuvants. Vaccine 19:2534-2541.
45. Pudney, J., and D. J. Anderson. 1995. Immunobiology of the human penile urethra. Am. J. Pathol. 147:155-165.
46. Sallusto, F., D. Lenig, R. Förster, M. Lipp, and A. Lanzavecchia. 1999. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401:708-712.
47. Sallusto, F., J. Geginat, and A. Lanzavecchia. 2004. Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu. Rev. Immunol. 22:745-763.
48. Saurer, L., K. C. McCullough, and A. Summerfield. 2007. In vitro induction of mucosa-type dendritic cells by all-trans retinoic acid. J. Immunol. 79:3504-3514.
49. Schon, M. P., et al. 1999. Mucosal T lymphocyte numbers are selectively reduced in integrin αE (CD103)-deficient mice. J. Immunol. 162:6641-6649.
50. Shattock, R. J., et al. 2008. Improving defenses at the portal of HIV entry: mucosal and innate immunity. PLoS Med. 5:e81.
51. Smyth, L. J. C., J. A. Kirby, and A. C. Cunningham. 2007. Role of the mucosal integrin αE(CD103)-7 in tissue-restricted cytotoxicity. Clin. Exp. Immunol. 149:162-170.
52. Soderberg, K. A., M. M. Linehan, N. H. Ruddle, and A. Iwasaki. 2004. MAdCAM-1 expressing sacral lymph node in the lymphotoxin beta-deficient mouse provides a site for immune generation following vaginal herpes simplex virus-2 infection. J. Immunol. 173:1908-1913.
53. Stenstad, H., et al. 2006. Gut-associated lymphoid tissue-primed CD4+ T cells display CCR9-dependent and -independent homing to the small intestine. Blood 107:3447-3454.
54. Sun, C. M., et al. 2007. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J. Exp. Med. 204:1775-1785.
55. Suvas, P. K., H. M. Dech, F. Sambira, J. Zeng, and T. M. Onami. 2007. Systemic and mucosal infection program protective memory CD8 T cells in the vaginal mucosa. J. Immunol. 179:8122-8127.
56. Suvas, S., U. Kumaraguru, C. D. Pack, S. Lee, and B. T. Rouse. 2003. CD4+CD25+T cells regulate virus-specific primary and memory CD8+ T cell responses. J. Exp. Med. 198:889-901.
57. Svensson, M., et al. 2008. Retinoic acid receptor signaling levels and antigen dose regulate gut homing receptor expression on CD8+ T cells. Mucosal Immunol. 1:38-48.
58. Svensson, M., et al. 2002. CCL25 mediates the localization of recently activated CD8alphabeta(+) lymphocytes to the small-intestinal mucosa. J. Clin. Invest. 110:1113-1121.
59. Uematsu, S., et al. 2008. Regulation of humoral and cellular gut immunity by lamina propria dendritic cells expressing Toll-like receptor 5. Nat. Immunol. 9:769-776.
60. Wakim, L. M., J. Waithman, N. van Rooijen, W. R. Heath, and F. R. Carbone. 2008. Dendritic cell-induced memory T cell activation in nonlymphoid tissues. Science 319:198-202.
61. Wakim, L. M., T. Gebhardt, W. R. Heath, and F. R. Carbone. 2008. Local recall responses by memory T cells newly recruited to peripheral nonlymphoid tissues. J. Immunol. 181:5837-5841.
62. Wang, Z. Y., and Z. Chen. 2008. Acute promyelocytic leukemia: from highly fatal to highly curable. Blood 111:2505-2515.
63. Woodland, D. L., and J. E. Kohlmeier. 2009. Migration, maintenance and recall of memory T cells in peripheral tissues. Nat. Rev. Immunol. 9:153-161.
64. + regulatory T cells and inhibits development of Th17 cells by enhancing TGF-(-driven smad3 signaling and inhibiting IL-6 and IL-23 receptor expression. J. Immunol. 181: 2277-2284.