A flagellin-derived toll-like receptor 5 agonist stimulates cytotoxic lymphocyte-mediated tumor immunity

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Leigh, Nicholas D ^a   Bian, Guanglin ^a   Ding, Xilai ^a   Liu, Hong ^a   Aygun Sunar, Semra ^a   Burdelya, Lyudmila G ^a   Gudkov, Andrei V ^a   Cao, Xuefang ^a  

^a ROSWELL PARK CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; ENTOLIMOD; FLAGELLIN; GLYCOPROTEIN P 15095; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PERFORIN; TOLL LIKE RECEPTOR 5;

ACCESSORY CELL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B CELL LYMPHOMA; BAGG ALBINO MOUSE; C57BL 6 MOUSE; CANCER CELL CULTURE; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CELL NUCLEUS; CELL STRAIN RMAS; CELLULAR IMMUNITY; CYTOTOXIC LYMPHOCYTE; DRUG EFFECT; FLOW CYTOMETRY; IMMUNOSTIMULATION; MOUSE; NATURAL KILLER CELL; NONHUMAN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SALMONELLA ENTERICA; T CELL LYMPHOMA; T LYMPHOCYTE ACTIVATION; TREATMENT RESPONSE; TUMOR GROWTH; TUMOR IMMUNITY; TUMOR MODEL;

ADAPTIVE IMMUNITY; ADJUVANTS, IMMUNOLOGIC; ANIMALS; CELL LINE, TUMOR; CYTOKINES; FLAGELLIN; IMMUNITY, INNATE; LYMPHOCYTES; LYMPHOMA, T-CELL; MICE; PEPTIDES; PERFORIN; TOLL-LIKE RECEPTOR 5; UP-REGULATION;

EID: 84898010578     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0085587     Document Type: Article

References (46)

1. Akira S, Takeda K, Kaisho T (2001) Toll-like receptors: critical proteins linking innate and acquired immunity. Nat Immunol 2: 675-680. (Pubitemid 32747155)
2. Matzinger P (1994) Tolerance, danger, and the extended family. Annu Rev Immunol 12: 991-1045.
3. Yu L, Wang L, Chen S (2010) Endogenous toll-like receptor ligands and their biological significance. J Cell Mol Med 14: 2592-2603.
4. Lonsdorf AS, Kuekrek H, Stern BV, Boehm BO, Lehmann PV, et al. (2003) Intratumor CpG-oligodeoxynucleotide injection induces protective antitumor T cell immunity. J Immunol 171: 3941-3946. (Pubitemid 37238666)
5. Chicoine MR, Zahner M, Won EK, Kalra RR, Kitamura T, et al. (2007) The in vivo antitumoral effects of lipopolysaccharide against glioblastoma multiforme are mediated in part by Toll-like receptor 4. Neurosurgery 60: 372-380; discussion 381.
6. Scheel B, Aulwurm S, Probst J, Stitz L, Hoerr I, et al. (2006) Therapeutic antitumor immunity triggered by injections of immunostimulating single-stranded RNA. Eur J Immunol 36: 2807-2816. (Pubitemid 44608463)
7. Hayashi F, Smith KD, Ozinsky A, Hawn TR, Yi EC, et al. (2001) The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410: 1099-1103. (Pubitemid 32391041)
8. Eaves-Pyles T, Murthy K, Liaudet L, Virag L, Ross G, et al. (2001) Flagellin, a novel mediator of Salmonella-induced epithelial activation and systemic inflammation: I kappa B alpha degradation, induction of nitric oxide synthase, induction of proinflammatory mediators, and cardiovascular dysfunction. J Immunol 166: 1248-1260. (Pubitemid 32060286)
9. Honko AN, Sriranganathan N, Lees CJ, Mizel SB (2006) Flagellin is an effective adjuvant for immunization against lethal respiratory challenge with Yersinia pestis. Infect Immun 74: 1113-1120. (Pubitemid 43185549)
10. McSorley SJ, Ehst BD, Yu Y, Gewirtz AT (2002) Bacterial flagellin is an effective adjuvant for CD4+ T cells in vivo. J Immunol 169: 3914-3919.
11. Sfondrini L, Rossini A, Besusso D, Merlo A, Tagliabue E, et al. (2006) Antitumor activity of the TLR-5 ligand flagellin in mouse models of cancer. J Immunol 176: 6624-6630. (Pubitemid 43787845)
12. Bohnhorst J, Rasmussen T, Moen SH, Flottum M, Knudsen L, et al. (2006) Toll-like receptors mediate proliferation and survival of multiple myeloma cells. Leukemia 20: 1138-1144. (Pubitemid 43797309)
13. Cai Z, Sanchez A, Shi Z, Zhang T, Liu M, et al. (2011) Activation of Toll-like receptor 5 on breast cancer cells by flagellin suppresses cell proliferation and tumor growth. Cancer Res 71: 2466-2475.
14. Burdelya LG, Krivokrysenko VI, Tallant TC, Strom E, Gleiberman AS, et al. (2008) An agonist of toll-like receptor 5 has radioprotective activity in mouse and primate models. Science 320: 226-230. (Pubitemid 351521417)
15. Ding X, Bian G, Leigh ND, Qiu J, McCarthy PL, et al. (2012) A TLR5 agonist enhances CD8(+) T cell-mediated graft-versus-tumor effect without exacerbating graft-versus-host disease. J Immunol 189: 4719-4727.
16. Fehniger TA, Cai SF, Cao X, Bredemeyer AJ, Presti RM, et al. (2007) Acquisition of murine NK cell cytotoxicity requires the translation of a preexisting pool of granzyme B and perforin mRNAs. Immunity 26: 798-811. (Pubitemid 46907665)
17. Cao X, Cai SF, Fehniger TA, Song J, Collins LI, et al. (2007) Granzyme B and perforin are important for regulatory T cell-mediated suppression of tumor clearance. Immunity 27: 635-646. (Pubitemid 47628832)
18. Gross S, Piwnica-Worms D (2005) Real-time imaging of ligand-induced IKK activation in intact cells and in living mice. Nat Methods 2: 607-614. (Pubitemid 41086852)
19. Burdelya LG, Gleiberman AS, Toshkov I, Aygun-Sunar S, Bapardekar M, et al. (2012) Toll-like receptor 5 agonist protects mice from dermatitis and oral mucositis caused by local radiation: implications for head-and-neck cancer radiotherapy. Int J Radiat Oncol Biol Phys 83: 228-234.
20. Maguire O, Collins C, O'Loughlin K, Miecznikowski J, Minderman H (2011) Quantifying nuclear p65 as a parameter for NF-kappaB activation: Correlation between ImageStream cytometry, microscopy, and Western blot. Cytometry A 79: 461-469.
21. George TC, Fanning SL, Fitzgerald-Bocarsly P, Medeiros RB, Highfill S, et al. (2006) Quantitative measurement of nuclear translocation events using similarity analysis of multispectral cellular images obtained in flow. J Immunol Methods 311: 117-129.
22. Kaufman DS, Schoon RA, Leibson PJ (1993) MHC class I expression on tumor targets inhibits natural killer cell-mediated cytotoxicity without interfering with target recognition. J Immunol 150: 1429-1436. (Pubitemid 23127433)
23. Nishikado H, Mukai K, Kawano Y, Minegishi Y, Karasuyama H (2011) NK cell-depleting anti-asialo GM1 antibody exhibits a lethal off-target effect on basophils in vivo. J Immunol 186: 5766-5771.
24. Smyth MJ, Kelly JM, Baxter AG, Korner H, Sedgwick JD (1998) An essential role for tumor necrosis factor in natural killer cell-mediated tumor rejection in the peritoneum. J Exp Med 188: 1611-1619. (Pubitemid 28516106)
25. Kim S, Iizuka K, Aguila HL, Weissman IL, Yokoyama WM (2000) In vivo natural killer cell activities revealed by natural killer cell-deficient mice. Proc Natl Acad Sci U S A 97: 2731-2736. (Pubitemid 30159240)
26. Sun JC, Lanier LL (2011) NK cell development, homeostasis and function: parallels with CD8(+) T cells. Nat Rev Immunol 11: 645-657.
27. Glimcher LH, Kim KJ, Green I, Paul WE (1982) Ia antigen-bearing B cell tumor lines can present protein antigen and alloantigen in a major histocompatibility complex-restricted fashion to antigen-reactive T cells. J Exp Med 155: 445-459. (Pubitemid 12171290)
28. Uematsu S, Jang MH, Chevrier N, Guo Z, Kumagai Y, et al. (2006) Detection of pathogenic intestinal bacteria by Toll-like receptor 5 on intestinal CD11c+ lamina propria cells. Nat Immunol 7: 868-874. (Pubitemid 44084094)
29. Zarember KA, Godowski PJ (2002) 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 168: 554-561. (Pubitemid 34049553)
30. Schwarz K, Storni T, Manolova V, Didierlaurent A, Sirard JC, et al. (2003) Role of Toll-like receptors in costimulating cytotoxic T cell responses. Eur J Immunol 33: 1465-1470. (Pubitemid 36790406)
31. Lyakh LA, Koski GK, Telford W, Gress RE, Cohen PA, et al. (2000) Bacterial lipopolysaccharide, TNF-alpha, and calcium ionophore under serum-free conditions promote rapid dendritic cell-like differentiation in CD14+ monocytes through distinct pathways that activate NK-kappa B. J Immunol 165: 3647-3655. (Pubitemid 32057269)
32. Barr TA, Brown S, Ryan G, Zhao J, Gray D (2007) TLR-mediated stimulation of APC: Distinct cytokine responses of B cells and dendritic cells. Eur J Immunol 37: 3040-3053. (Pubitemid 350131284)
33. Mescher MF, Curtsinger JM, Agarwal P, Casey KA, Gerner M, et al. (2006) Signals required for programming effector and memory development by CD8+ T cells. Immunol Rev 211: 81-92. (Pubitemid 43882963)
34. Dienz O, Rincon M (2009) The effects of IL-6 on CD4 T cell responses. Clin Immunol 130: 27-33.
35. Rakoff-Nahoum S, Medzhitov R (2009) Toll-like receptors and cancer. Nat Rev Cancer 9: 57-63.
36. El Andaloussi A, Sonabend AM, Han Y, Lesniak MS (2006) Stimulation of TLR9 with CpG ODN enhances apoptosis of glioma and prolongs the survival of mice with experimental brain tumors. Glia 54: 526-535. (Pubitemid 44449333)
37. Whitmore MM, DeVeer MJ, Edling A, Oates RK, Simons B, et al. (2004) Synergistic activation of innate immunity by double-stranded RNA and CpG DNA promotes enhanced antitumor activity. Cancer Res 64: 5850-5860. (Pubitemid 39095586)
38. Tsujimoto H, Uchida T, Efron PA, Scumpia PO, Verma A, et al. (2005) Flagellin enhances NK cell proliferation and activation directly and through dendritic cell-NK cell interactions. J Leukoc Biol 78: 888-897. (Pubitemid 41384405)
39. Salazar-Gonzalez RM, Srinivasan A, Griffin A, Muralimohan G, Ertelt JM, et al. (2007) Salmonella flagellin induces bystander activation of splenic dendritic cells and hinders bacterial replication in vivo. J Immunol 179: 6169-6175.
40. Didierlaurent A, Ferrero I, Otten LA, Dubois B, Reinhardt M, et al. (2004) Flagellin promotes myeloid differentiation factor 88-dependent development of Th2-type response. J Immunol 172: 6922-6930. (Pubitemid 38669131)
41. Burdelya LG, Brackett CM, Kojouharov B, Gitlin, II, Leonova KI, et al. (2013) Central role of liver in anticancer and radioprotective activities of Toll-like receptor 5 agonist. Proc Natl Acad Sci U S A 110: E1857-E1866.
42. Kim KJ, Kanellopoulos-Langevin C, Merwin RM, Sachs DH, Asofsky R (1979) Establishment and characterization of BALB/c lymphoma lines with B cell properties. J Immunol 122: 549-554. (Pubitemid 9089211)
43. Faham A, Altin JG (2010) Antigen-containing liposomes engrafted with flagellin-related peptides are effective vaccines that can induce potent antitumor immunity and immunotherapeutic effect. J Immunol 185: 1744-1754.
44. Garaude J, Kent A, van Rooijen N, Blander JM (2012) Simultaneous targeting of toll- and nod-like receptors induces effective tumor-specific immune responses. Sci Transl Med 4: 120ra116.
45. Bates JT, Graff AH, Phipps JP, Grayson JM, Mizel SB (2011) Enhanced antigen processing of flagellin fusion proteins promotes the antigen-specific CD8+ T cell response independently of TLR5 and MyD88. J Immunol 186: 6255-6262.
46. Hawn TR, Verbon A, Lettinga KD, Zhao LP, Li SS, et al. (2003) A common dominant TLR5 stop codon polymorphism abolishes flagellin signaling and is associated with susceptibility to legionnaires' disease. J Exp Med 198: 1563-1572. (Pubitemid 37467170)