Triggering of toll-like receptor signaling pathways in T cells contributes to the anti-tumor efficacy of T cell responses

Immunology Letters

Volumn 137, Issue 1-2, 2011, Pages 9-14

  Salem, Mohamed Labib ^a  

^a Tanta University   (Egypt)

Author keywords

T cells; TLR; TLR agonists; TLR expression; TLR ligands; Toll like Receptors; Vaccination

Indexed keywords

CYTOKINE; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 5; TOLL LIKE RECEPTOR 6; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; TOLL LIKE RECEPTOR 9; TOLL LIKE RECEPTOR AGONIST; TUMOR VACCINE;

ADAPTIVE IMMUNITY; CANCER IMMUNIZATION; CANCER IMMUNOTHERAPY; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL THERAPY; CELLULAR IMMUNITY; EFFECTOR CELL; HUMAN; IMMUNOMODULATION; IMMUNOSTIMULATION; INNATE IMMUNITY; LYMPHOCYTE FUNCTION; MELANOMA; MEMORY T LYMPHOCYTE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; REVIEW; SIGNAL TRANSDUCTION; SOLID TUMOR; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TREATMENT RESPONSE; TUMOR; TUMOR IMMUNITY;

ANIMALS; ANTIGENS, NEOPLASM; ANTINEOPLASTIC AGENTS; CANCER VACCINES; HUMANS; IMMUNOMODULATION; IMMUNOTHERAPY, ADOPTIVE; LYMPHOCYTE ACTIVATION; RECEPTOR CROSS-TALK; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TOLL-LIKE RECEPTORS;

EID: 79954414905     PISSN: 01652478     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.imlet.2011.02.019     Document Type: Review

References (79)

1. Uematsu S., Jang M.H., Chevrier N., Guo Z., Kumagai Y., Yamamoto M., et al. Detection of pathogenic intestinal bacteria by toll-like receptor 5 on intestinal CD11c(+) lamina propria cells. Nat Immunol 2006, 7:868-874.
2. Wesch D., Beetz S., Oberg H.H., Marget M., Krengel K., Kabelitz D. Direct costimulatory effect of TLR3 ligand poly(I:C) on human gamma delta T lymphocytes. J Immunol 2006, 176:1348-1354.
3. Salem M.L., Diaz-Montero C.M., El-Naggar S.A., Chen Y., Moussa O., Cole D.J. The TLR3 agonist poly(I:C) targets CD8+ T cells and augments their antigen-specific responses upon their adoptive transfer into naive recipient mice. Vaccine 2009, 27:549-557.
4. Cottalorda A., Verschelde C., Marcais A., Tomkowiak M., Musette P., Uematsu S., et al. TLR2 engagement on CD8 T cells lowers the threshold for optimal antigen-induced T cell activation. Eur J Immunol 2006, 36:1684-1693.
5. Schwarz K., Storni T., Manolova V., Didierlaurent A., Sirard J.C., Rothlisberger P., et al. Role of toll-like receptors in costimulating cytotoxic T cell responses. Eur J Immunol 2003, 33:1465-1470.
6. Marsland B.J., Nembrini C., Grun K., Reissmann R., Kurrer M., Leipner C., et al. TLR ligands act directly upon T cells to restore proliferation in the absence of protein kinase C-theta signaling and promote autoimmune myocarditis. J Immunol 2007, 178:3466-3473.
7. Gelman A.E., LaRosa D.F., Zhang J., Walsh P.T., Choi Y., Sunyer J.O., et al. The adaptor molecule MyD88 activates PI-3 kinase signaling in CD4+ T cells and enables CpG oligodeoxynucleotide-mediated costimulation. Immunity 2006, 25:783-793.
8. Gelman A.E., Zhang J., Choi Y., Turka L.A. Toll-like receptor ligands directly promote activated CD4+ T cell survival. J Immunol 2004, 172:6065-6073.
9. Caron G., Duluc D., Fremaux I., Jeannin P., David C., Gascan H., et al. Direct stimulation of human T cells via TLR5 and TLR7/8: flagellin and R-848 up-regulate proliferation and IFN-gamma production by memory CD4+ T cells. J Immunol 2005, 175:1551-1557.
10. Tomita T., Kanai T., Fujii T., Nemoto Y., Okamoto R., Tsuchiya K., et al. MyD88-dependent pathway in T cells directly modulates the expansion of colitogenic CD4+ T cells in chronic colitis. J Immunol 2008, 180:5291-5299.
11. Komai-Koma M., Jones L., Ogg G.S., Xu D., Liew F.Y. TLR2 is expressed on activated T cells as a costimulatory receptor. Proc Natl Acad Sci USA 2004, 101:3029-3034.
12. Asprodites N., Zheng L., Geng D., Velasco-Gonzalez C., Sanchez-Perez L., Davila E. Engagement of toll-like receptor-2 on cytotoxic T-lymphocytes occurs in vivo and augments antitumor activity. FASEB J 2008, 22:3628-3637.
13. Tabiasco J., Devevre E., Rufer N., Salaun B., Cerottini J.C., Speiser D., et al. Human effector CD8+ T lymphocytes express TLR3 as a functional coreceptor. J Immunol 2006, 177:8708-8713.
14. Mercier B.C., Cottalorda A., Coupet C.A., Marvel J., Bonnefoy-Berard N. TLR2 engagement on CD8 T cells enables generation of functional memory cells in response to a suboptimal TCR signal. J Immunol 2009, 182:1860-1867.
15. Quigley M., Martinez J., Huang X., Yang Y. A critical role for direct TLR2-MyD88 signaling in CD8 T cell clonal expansion and memory formation following vaccinia viral infection. Blood 2009, 113:2256-2264.
16. Hornung V., Rothenfusser S., Britsch S., Krug A., Jahrsdorfer B., Giese T., et al. Quantitative expression of toll-like receptor 1-10 mRNA in cellular subsets of human peripheral blood mononuclear cells and sensitivity to CpG oligodeoxynucleotides. J Immunol 2002, 168:4531-4537.
17. Seya T., Akazawa T., Tsujita T., Matsumoto M. Role of toll-like receptors in adjuvant-augmented immune therapies. Evid Based Complement Alternat Med 2006, 3:31-38. (discussion 133-137).
18. Bowie A., O'Neill L.A. The interleukin-1 receptor/toll-like receptor superfamily: signal generators for pro-inflammatory interleukins and microbial products. J Leukoc Biol 2000, 67:508-514.
19. Kawai T., Akira S. TLR signaling. Semin Immunol 2007, 19:24-32.
20. Salem M.L., Diaz-Montero C.M., Al-Khami A.A., El-Naggar S.A., Naga O., Montero A.J., et al. Recovery from cyclophosphamide-induced lymphopenia results in expansion of immature dendritic cells which can mediate enhanced prime-boost vaccination antitumor responses in vivo when stimulated with the TLR3 agonist poly(I:C). J Immunol 2009, 182:2030-2040.
21. Salem M.L., El-Naggar S.A., Kadima A., Gillanders W.E., Cole D.J. The adjuvant effects of the toll-like receptor 3 ligand polyinosinic-cytidylic acid poly (I:C) on antigen-specific CD8+ T cell responses are partially dependent on NK cells with the induction of a beneficial cytokine milieu. Vaccine 2006, 24:5119-5132.
22. Salem M.L., Kadima A.N., Cole D.J., Gillanders W.E. Defining the antigen-specific T-cell response to vaccination and poly(I:C)/TLR3 signaling: evidence of enhanced primary and memory CD8 T-cell responses and antitumor immunity. J Immunother 2005, 28:220-228.
23. Salem M.L., Kadima A.N., El-Naggar S.A., Rubinstein M.P., Chen Y., Gillanders W.E., et al. Defining the ability of cyclophosphamide preconditioning to enhance the antigen-specific CD8+ T-cell response to peptide vaccination: creation of a beneficial host microenvironment involving type I IFNs and myeloid cells. J Immunother 2007, 30:40-53.
24. Lore K., Betts M.R., Brenchley J.M., Kuruppu J., Khojasteh S., Perfetto S., et al. Toll-like receptor ligands modulate dendritic cells to augment cytomegalovirus- and HIV-1-specific T cell responses. J Immunol 2003, 171:4320-4328.
25. Sivori S., Falco M., Della Chiesa M., Carlomagno S., Vitale M., Moretta L., et al. CpG and double-stranded RNA trigger human NK cells by toll-like receptors: induction of cytokine release and cytotoxicity against tumors and dendritic cells. Proc Natl Acad Sci USA 2004, 101:10116-10121.
26. Thompson K.A., Strayer D.R., Salvato P.D., Thompson C.E., Klimas N., Molavi A., et al. Results of a double-blind placebo-controlled study of the double-stranded RNA drug polyI:polyC12U in the treatment of HIV infection. Eur J Clin Microbiol Infect Dis 1996, 15:580-587.
27. Ahonen C.L., Doxsee C.L., McGurran S.M., Riter T.R., Wade W.F., Barth R.J., et al. Combined TLR and CD40 triggering induces potent CD8+ T cell expansion with variable dependence on type I IFN. J Exp Med 2004, 199:775-784.
28. Ahonen C.L., Wasiuk A., Fuse S., Turk M.J., Ernstoff M.S., Suriawinata A.A., et al. Enhanced efficacy and reduced toxicity of multifactorial adjuvants compared with unitary adjuvants as cancer vaccines. Blood 2008, 111:3116-3125.
29. Guillot L., Le Goffic R., Bloch S., Escriou N., Akira S., Chignard M., et al. Involvement of toll-like receptor 3 in the immune response of lung epithelial cells to double-stranded RNA and influenza A virus. J Biol Chem 2005, 280:5571-5580.
30. Applequist S.E., Wallin R.P., Ljunggren H.G. Variable expression of toll-like receptor in murine innate and adaptive immune cell lines. Int Immunol 2002, 14:1065-1074.
31. Zarember K.A., Godowski P.J. Tissue expression of human toll-like receptors and differential regulation of toll-like receptor mRNAs in leukocytes in response to microbes, their products, and cytokines. J Immunol 2002, 168:554-561.
32. Xu D., Komai-Koma M., Liew F.Y. Expression and function of toll-like receptor on T cells. Cell Immunol 2005, 233:85-89.
33. Brentano F., Kyburz D., Schorr O., Gay R., Gay S. The role of toll-like receptor signalling in the pathogenesis of arthritis. Cell Immunol 2005, 233:90-96.
34. Ignacio G., Nordone S., Howard K.E., Dean G.A. Toll-like receptor expression in feline lymphoid tissues. Vet Immunol Immunopathol 2005, 106:229-237.
35. Mansson A., Adner M., Hockerfelt U., Cardell L.O. A distinct toll-like receptor repertoire in human tonsillar B cells, directly activated by PamCSK, R-837 and CpG-2006 stimulation. Immunology 2006, 118:539-548.
36. Liew F.Y., Komai-Koma M., Xu D. A toll for T cell costimulation. Ann Rheum Dis 2004, 63(Suppl. 2):ii76-ii78.
37. McKay A., Komai-Koma M., MacLeod K.J., Campbell C.C., Kitson S.M., Chaudhuri R., et al. Interleukin-18 levels in induced sputum are reduced in asthmatic and normal smokers. Clin Exp Allergy 2004, 34:904-910.
38. Xu D., Liu H., Komai-Koma M. Direct and indirect role of toll-like receptors in T cell mediated immunity. Cell Mol Immunol 2004, 1:239-246.
39. Cottalorda A., Mercier B.C., Mbitikon-Kobo F.M., Arpin C., Teoh D.Y., McMichael A., et al. TLR2 engagement on memory CD8(+) T cells improves their cytokine-mediated proliferation and IFN-gamma secretion in the absence of Ag. Eur J Immunol 2009, 39:2673-2681.
40. Babu S., Blauvelt C.P., Kumaraswami V., Nutman T.B. Diminished expression and function of TLR in lymphatic filariasis: a novel mechanism of immune dysregulation. J Immunol 2005, 175:1170-1176.
41. Caramalho I., Lopes-Carvalho T., Ostler D., Zelenay S., Haury M., Demengeot J. Regulatory T cells selectively express toll-like receptors and are activated by lipopolysaccharide. J Exp Med 2003, 197:403-411.
42. Sobek V., Birkner N., Falk I., Wurch A., Kirschning C.J., Wagner H., et al. Direct toll-like receptor 2 mediated co-stimulation of T cells in the mouse system as a basis for chronic inflammatory joint disease. Arthritis Res Ther 2004, 6:R433-446.
43. Cairns B., Maile R., Barnes C.M., Frelinger J.A., Meyer A.A. Increased toll-like receptor 4 expression on T cells may be a mechanism for enhanced T cell response late after burn injury. J Trauma 2006, 61:293-298. (discussion 298-299).
44. Liu G., Zhang L., Zhao Y. Modulation of immune responses through direct activation of toll-like receptors to T cells. Clin Exp Immunol 2010, 160:168-175.
45. Rahman A.H., Taylor D.K., Turka L.A. The contribution of direct TLR signaling to T cell responses. Immunol Res 2009, 45:25-36.
46. Kolumam G.A., Thomas S., Thompson L.J., Sprent J., Murali-Krishna K. Type I interferons act directly on CD8 T cells to allow clonal expansion and memory formation in response to viral infection. J Exp Med 2005, 202:637-650.
47. Kabelitz D. Expression and function of toll-like receptors in T lymphocytes. Curr Opin Immunol 2007, 19:39-45.
48. Dai J., Liu B., Li Z. Regulatory T cells and toll-like receptors: what is the missing link?. Int Immunopharmacol 2009, 9:528-533.
49. Nyirenda M.H., O'Brien K., Sanvito L., Constantinescu C.S., Gran B. Modulation of regulatory T cells in health and disease: role of toll-like receptors. Inflamm Allergy Drug Targets 2009, 8:124-129.
50. Chiffoleau E., Heslan J.M., Heslan M., Louvet C., Condamine T., Cuturi M.C. TLR9 ligand enhances proliferation of rat CD4+ T cell and modulates suppressive activity mediated by CD4+ CD25+ T cell. Int Immunol 2007, 19:193-201.
51. LaRosa D.F., Gelman A.E., Rahman A.H., Zhang J., Turka L.A., Walsh P.T. CpG DNA inhibits CD4+CD25+ Treg suppression through direct MyD88-dependent costimulation of effector CD4+ T cells. Immunol Lett 2007, 108:183-188.
52. Sutmuller R.P., den Brok M.H., Kramer M., Bennink E.J., Toonen L.W., Kullberg B.J., et al. Toll-like receptor 2 controls expansion and function of regulatory T cells. J Clin Invest 2006, 116:485-494.
53. Peng G., Guo Z., Kiniwa Y., Voo K.S., Peng W., Fu T., et al. Toll-like receptor 8-mediated reversal of CD4+ regulatory T cell function. Science 2005, 309:1380-1384.
54. Crellin N.K., Garcia R.V., Hadisfar O., Allan S.E., Steiner T.S., Levings M.K. Human CD4+ T cells express TLR5 and its ligand flagellin enhances the suppressive capacity and expression of FOXP3 in CD4+CD25+ T regulatory cells. J Immunol 2005, 175:8051-8059.
55. Okugawa S., Yanagimoto S., Tsukada K., Kitazawa T., Koike K., Kimura S., et al. Bacterial flagellin inhibits T cell receptor-mediated activation of T cells by inducing suppressor of cytokine signalling-1 (SOCS-1). Cell Microbiol 2006, 8:1571-1580.
56. Klebanoff C.A., Gattinoni L., Restifo N.P. CD8+ T-cell memory in tumor immunology and immunotherapy. Immunol Rev 2006, 211:214-224.
57. Rosenberg S.A., Restifo N.P., Yang J.C., Morgan R.A., Dudley M.E. Adoptive cell transfer: a clinical path to effective cancer immunotherapy. Nat Rev Cancer 2008, 8:299-308.
58. Dudley M.E., Rosenberg S.A. Adoptive cell transfer therapy. Semin Oncol 2007, 34:524-531.
59. Dudley M.E., Yang J.C., Sherry R., Hughes M.S., Royal R., Kammula U., et al. Adoptive cell therapy for patients with metastatic melanoma: evaluation of intensive myeloablative chemoradiation preparative regimens. J Clin Oncol 2008, 26:5233-5239.
60. Macgregor J.N., Li Q., Chang A.E., Braun T.M., Hughes D.P., McDonagh K.T. Ex vivo culture with interleukin (IL)-12 improves CD8(+) T-cell adoptive immunotherapy for murine leukemia independent of IL-18 or IFN-gamma but requires perforin. Cancer Res 2006, 66:4913-4921.
61. Dudley M.E., Wunderlich J.R., Yang J.C., Sherry R.M., Topalian S.L., Restifo N.P., et al. Adoptive cell transfer therapy following non-myeloablative but lymphodepleting chemotherapy for the treatment of patients with refractory metastatic melanoma. J Clin Oncol 2005, 23:2346-2357.
62. Dudley M.E., Wunderlich J.R., Yang J.C., Hwu P., Schwartzentruber D.J., Topalian S.L., et al. A phase I study of nonmyeloablative chemotherapy and adoptive transfer of autologous tumor antigen-specific T lymphocytes in patients with metastatic melanoma. J Immunother 2002, 25:243-251.
63. Schumacher T.N. T-cell-receptor gene therapy. Nat Rev Immunol 2002, 2:512-519.
64. Huang J., Kerstann K.W., Ahmadzadeh M., Li Y.F., El-Gamil M., Rosenberg S.A., et al. Modulation by IL-2 of CD70 and CD27 expression on CD8+ T cells: importance for the therapeutic effectiveness of cell transfer immunotherapy. J Immunol 2006, 176:7726-7735.
65. Morgan S.M., Hodges E., Mitchell T.J., Harris S., Whittaker S.J., Smith J.L. Molecular analysis of T-cell receptor beta genes in cutaneous T-cell lymphoma reveals Jbeta1 bias. J Invest Dermatol 2006, 126:1893-1899.
66. Morgan R.A., Dudley M.E., Yu Y.Y., Zheng Z., Robbins P.F., Theoret M.R., et al. High efficiency TCR gene transfer into primary human lymphocytes affords avid recognition of melanoma tumor antigen glycoprotein 100 and does not alter the recognition of autologous melanoma antigens. J Immunol 2003, 171:3287-3295.
67. Abad J.D., Wrzensinski C., Overwijk W., De Witte M.A., Jorritsma A., Hsu C., et al. T-cell receptor gene therapy of established tumors in a murine melanoma model. J Immunother 2008, 31:1-6.
68. Shen X., Zhou J., Hathcock K.S., Robbins P., Powell D.J., Rosenberg S.A., et al. Persistence of tumor infiltrating lymphocytes in adoptive immunotherapy correlates with telomere length. J Immunother 2007, 30:123-129.
69. Diaz-Montero C.M., El Naggar S., Al Khami A., El Naggar R., Montero A.J., Cole D.J., et al. Priming of naive CD8+ T cells in the presence of IL-12 selectively enhances the survival of CD8+CD62Lhi cells and results in superior anti-tumor activity in a tolerogenic murine model. Cancer Immunol Immunother 2008, 57:563-572.
70. Rubinstein M.P., Kadima A.N., Salem M.L., Nguyen C.L., Gillanders W.E., Nishimura M.I., et al. Transfer of TCR genes into mature T cells is accompanied by the maintenance of parental T cell avidity. J Immunol 2003, 170:1209-1217.
71. Rubinstein M.P., Salem M.L., Kadima A.N., Nguyen C.L., Gillanders W.E., Nishimura M.I., et al. Loss of T cell-mediated antitumor immunity after construct-specific downregulation of retrovirally encoded T-cell receptor expression in vivo. Cancer Gene Ther 2009, 16:171-183.
72. Nguyen C.L., Salem M.L., Rubinstein M.P., Demcheva M., Vournakis J.N., Cole D.J., et al. Mechanisms of enhanced antigen-specific T cell response following vaccination with a novel peptide-based cancer vaccine and systemic interleukin-2 (IL-2). Vaccine 2003, 21:2318-2328.
73. Salem M.L., Kadima A.N., Zhou Y., Nguyen C.L., Rubinstein M.P., Demcheva M., et al. Paracrine release of IL-12 stimulates IFN-gamma production and dramatically enhances the antigen-specific T cell response after vaccination with a novel peptide-based cancer vaccine. J Immunol 2004, 172:5159-5167.
74. Rubinstein M.P., Kadima A.N., Salem M.L., Nguyen C.L., Gillanders W.E., Cole D.J. Systemic administration of IL-15 augments the antigen-specific primary CD8+ T cell response following vaccination with peptide-pulsed dendritic cells. J Immunol 2002, 169:4928-4935.
75. Klebanoff C.A., Gattinoni L., Torabi-Parizi P., Kerstann K., Cardones A.R., Finkelstein S.E., et al. Central memory self/tumor-reactive CD8+ T cells confer superior antitumor immunity compared with effector memory T cells. Proc Natl Acad Sci USA 2005, 102:9571-9576.
76. Gattinoni L., Ranganathan A., Surman D.R., Palmer D.C., Antony P.A., Theoret M.R., et al. CTLA-4 dysregulation of self/tumor-reactive CD8+ T-cell function is CD4+ T-cell dependent. Blood 2006, 108:3818-3823.
77. Bendigs S., Salzer U., Lipford G.B., Wagner H., Heeg K. CpG-oligodeoxynucleotides co-stimulate primary T cells in the absence of antigen-presenting cells. Eur J Immunol 1999, 29:1209-1218.
78. Hinrichs C.S., Spolski R., Paulos C.M., Gattinoni L., Kerstann K.W., Palmer D.C., et al. IL-2 and IL-21 confer opposing differentiation programs to CD8+ T cells for adoptive immunotherapy. Blood 2008, 111:5326-5333.
79. Zhang Y., Luo F., Cai Y., Liu N., Wang L., Xu D., et al. TLR1/TLR2 agonist induces tumor regression by reciprocal modulation of effector and regulatory T Cells. J Immunol 2011, 186:1963-1969.