TLR2 agonist PSK activates human NK cells and enhances the antitumor effect of HER2-targeted monoclonal antibody therapy

Clinical Cancer Research

Volumn 17, Issue 21, 2011, Pages 6742-6753

  Lu, Hailing ^a   Yang, Yi ^a   Gad, Ekram ^a   Inatsuka, Carol ^a   Wenner, Cynthia A ^b   Disis, Mary L ^a   Standish, Leanna J ^b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b BASTYR UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR ANTIBODY; GAMMA INTERFERON; INTERLEUKIN 12; KRESTIN; MONOCLONAL ANTIBODY 7.16.4; TOLL LIKE RECEPTOR 2; TRASTUZUMAB; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CANCER; CANCER CELL; CELL ACTIVATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG MECHANISM; DRUG POTENTIATION; HUMAN; HUMAN CELL; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; TUMOR CELL DESTRUCTION;

ANIMALS; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; ANTIGENS, CD56; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; BREAST NEOPLASMS; CYTOKINES; DRUG SYNERGISM; FEMALE; HUMANS; INTERFERON-GAMMA; INTERLEUKIN-2; KILLER CELLS, NATURAL; LEUKOCYTES, MONONUCLEAR; MICE; MICE, TRANSGENIC; MOLECULAR TARGETED THERAPY; PROTEOGLYCANS; RECEPTOR, ERBB-2; TOLL-LIKE RECEPTOR 2; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 80455144500     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-11-1142     Document Type: Article

References (49)

1. Hudis CA. Drug therapy: trastuzumab - mechanism of action and use in clinical practice. N Engl J Med 2007;357:39-51. (Pubitemid 47026733)
2. Baselga J, Perez EA, Pienkowski T, Bell R. Adjuvant trastuzumab: a milestone in the treatment of HER-2-positive early breast cancer. Oncologist 2006;11:4-12.
3. Clynes RA, Towers TL, Presta LG, Ravetch JV. Inhibitory Fc receptors modulate in vivo cytoxicity against tumor targets. Nat Med 2000;6:443-6. (Pubitemid 30208162)
4. Varchetta S, Gibelli N, Oliviero B, Nardini E, Gennari R, Gatti G, et al. Elements related to heterogeneity of antibody-dependent cell cytotoxicity in patients under trastuzumab therapy for primary operable breast cancer overexpressing Her2. Cancer Res 2007;67:11991-9.
5. Arnould L, Gelly M, Penault-Llorca F, Benoit L, Bonnetain F, Migeon C, et al. Trastuzumab-based treatment of HER2-positive breast cancer: an antibody-dependent cellular cytotoxicity mechanism? Br J Cancer 2006;94:259-67. (Pubitemid 43151545)
6. Musolino A, Naldi N, Bortesi B, Pezzuolo D, Capelletti M, Missale G, et al. Immunoglobulin G fragment C receptor polymorphisms and clinical efficacy of trastuzumab-based therapy in patients with HER-2/neu-positive metastatic breast cancer. J Clin Oncol 2008;26:1789-96.
7. Zamai L, Ponti C, Mirandola P, Gobbi G, Papa S, Galeotti L, et al. NK cells and cancer. J Immunol 2007;178:4011-6. (Pubitemid 46492347)
8. Ferris RL, Jaffee EM, Ferrone S. Tumor antigen-targeted, monoclonal antibody-based immunotherapy: clinical response, cellular immunity, and immunoescape. J Clin Oncol 2010;28:4390-9.
9. Lee JC, Lee KM, Kim DW, Heo DS. Elevated TGF-beta1 secretion and down-modulation of NKG2D underlies impaired NK cytotoxicity in cancer patients. J Immunol 2004;172:7335-40. (Pubitemid 38747593)
10. Varker KA, Terrell CE, Welt M, Suleiman S, Thornton L, Andersen BL, et al. Impaired natural killer cell lysis in breast cancer patients with high levels of psychological stress is associated with altered expression of killer immunoglobin-like receptors. J Surg Res 2007;139:36-44. (Pubitemid 46482568)
11. Kono K, Takahashi A, Ichihara F, Sugai H, Fujii H, Matsumoto Y. Impaired antibody-dependent cellular cytotoxicity mediated by herceptin in patients with gastric cancer. Cancer Res 2002;62:5813-7. (Pubitemid 35204740)
12. Garner WL, Minton JP, James AG, Hoffmann CC. Human breast cancer and impaired NK cell function. J Surg Oncol 1983;24:64-6. (Pubitemid 13004154)
13. Lanier LL. NK cell recognition. Annu Rev Immunol 2005;23:225-74. (Pubitemid 40563170)
14. Cooper MA, Fehniger TA, Turner SC, Chen KS, Ghaheri BA, Ghayur T, et al. Human natural killer cells: a unique innate immunoregulatory role for the CD56(bright) subset. Blood 2001;97:3146-51.
15. Gorski KS, Waller EL, Bjornton-Severson J, Hanten JA, Riter CL, Kieper WC, et al. Distinct indirect pathways govern human NK-cell activation by TLR-7 and TLR-8 agonists. Int Immunol 2006;18:1115-26. (Pubitemid 43923429)
16. Schmidt KN, Leung B, Kwong M, Zarember KA, Satyal S, Navas TA, et al. APC-independent activation ofNKcells by the Toll-like receptor 3 agonist double-stranded RNA. J Immunol 2004;172:138-43. (Pubitemid 38020465)
17. Roda JM, Parihar R, Carson WE III. CpG-containing oligodeoxynucleotides act through TLR9 to enhance the NK cell cytokine response to antibody-coated tumor cells. J Immunol 2005;175:1619-27. (Pubitemid 41023064)
18. Hart OM, Athie-Morales V, O'Connor GM, Gardiner CM. TLR7/8-mediated activation of human NK cells results in accessory cell-dependent IFN-gamma production. J Immunol 2005;175:1636-42. (Pubitemid 41023066)
19. Ebihara T, Azuma M, Oshiumi H, Kasamatsu J, Iwabuchi K, Matsumoto K, et al. Identification of a polyI:C-inducible membrane protein that participates in dendritic cell-mediated natural killer cell activation. J Exp Med 2010;207:2675-87.
20. Friedberg JW, Kelly JL, Neuberg D, Peterson DR, Kutok JL, Salloum R, et al. Phase II study of a TLR-9 agonist (1018 ISS) with rituximab in patients with relapsed or refractory follicular lymphoma. Br J Haematol 2009;146:282-91.
21. Martinez J, Huang X, Yang Y. Direct TLR2 signaling is critical for NK cell activation and function in response to vaccinia viral infection. PLoS Pathog 2010;6:e1000811.
22. Marcenaro E, Ferranti B, Falco M, Moretta L, Moretta A. Human NK cells directly recognize Mycobacterium bovis via TLR2 and acquire the ability to kill monocyte-derived DC. Int Immunol 2008;20:1155-67.
23. Azuma M, Sawahata R, Akao Y, Ebihara T, Yamazaki S, Matsumoto M, et al. The peptide sequence of diacyl lipopeptides determines dendritic cell TLR2-mediated NK activation. PLoS One 2010;5:e12550.
24. Moreno M, Mol BM, von Mensdorff-Pouilly S, Verheijen RH, von Blomberg BM, van den Eertwegh AJ, et al. Toll-like receptor agonists and invariant natural killer T-cells enhance antibody-dependent cell-mediated cytotoxicity (ADCC). Cancer Lett 2008;272:70-6.
25. Lu H, Yang Y, Gad E, Wenner CA, Chang A, Larson ER, et al. Polysaccharide krestin is a novel TLR2 agonist that mediates inhibition of tumor growth via stimulation of CD8 T cells and NK cells. Clin Cancer Res 2011;17:67-76.
26. Fisher M, Yang LX. Anticancer effects and mechanisms of polysaccharide-K (PSK): implications of cancer immunotherapy. Anticancer Res 2002;22:1737-54. (Pubitemid 34839190)
27. Oba K, Teramukai S, Kobayashi M, Matsui T, Kodera Y, Sakamoto J. Efficacy of adjuvant immunochemotherapy with polysaccharide K for patients with curative resections of gastric cancer. Cancer Immunol Immunother 2007;56:905-11. (Pubitemid 46729147)
28. Ohwada S, Ikeya T, Yokomori T, Kusaba T, Roppongi T, Takahashi T, et al. Adjuvant immunochemotherapy with oral Tegafur/uracil plus PSK in patients with stage II or III colorectal cancer: a randomised controlled study. Br J Cancer 2004;90:1003-10. (Pubitemid 38495819)
29. Sakamoto J, Morita S, Oba K, Matsui T, Kobayashi M, Nakazato H, et al. Efficacy of adjuvant immunochemotherapy with polysaccharide K for patients with curatively resected colorectal cancer: a meta-analysis of centrally randomized controlled clinical trials. Cancer Immunol Immunother 2006;55:404-11. (Pubitemid 43076892)
30. Lu H, Knutson KL, Gad E, Disis ML. The tumor antigen repertoire identified in tumor-bearing Neu transgenic mice predicts human tumor antigens. Cancer Res 2006;66:9754-61. (Pubitemid 44623677)
31. Gong JH, Maki G, Klingemann HG. Characterization of a human cell line (NK-92) with phenotypical and functional characteristics of activated natural killer cells. Leukemia 1994;8:652-8. (Pubitemid 24133034)
32. Papadopoulos NG, Dedoussis GV, Spanakos G, Gritzapis AD, Baxevanis CN, Papamichail M. An improved fluorescence assay for the determination of lymphocyte-mediated cytotoxicity using flow cytometry. J Immunol Methods 1994;177:101-11.
33. Knutson KL, Lu H, Stone B, Reiman JM, Behrens MD, Prosperi CM, et al. Immunoediting of cancers may lead to epithelial to mesenchymal transition. J Immunol 2006;177:1526-33.
34. Lu H, Wagner WM, Gad E, Yang Y, Duan H, Amon LM, et al. Treatment failure of a TLR-7 agonist occurs due to self-regulation of acute inflammation and can be overcome by IL-10 blockade. J Immunol 2010;184:5360-7.
35. Alter G, Malenfant JM, Altfeld M. CD107a as a functional marker for the identification of natural killer cell activity. J Immunol Methods 2004;294:15-22. (Pubitemid 39626587)
36. Knutson KL, Almand B, Dang Y, Disis ML. Neu antigen-negative variants can be generated after neu-specific antibody therapy in neu transgenic mice. Cancer Res 2004;64:1146-51. (Pubitemid 38176922)
37. Stagg J, Loi S, Divisekera U, Ngiow SF, Duret H, Yagita H, et al. Anti-ErbB-2 mAb therapy requires type I and II interferons and synergizes with anti-PD-1 or anti-CD137 mAb therapy. Proc Natl Acad Sci U S A 2011;108:7142-7.
38. Roda JM, Joshi T, Butchar JP, McAlees JW, Lehman A, Tridandapani S, et al. The activation of natural killer cell effector functions by cetuximab-coated, epidermal growth factor receptor positive tumor cells is enhanced by cytokines. Clin Cancer Res 2007;13:6419-28. (Pubitemid 350075032)
39. Roda JM, Parihar R, Lehman A, Mani A, Tridandapani S, Carson WE III. Interleukin-21 enhances NK cell activation in response to antibody-coated targets. J Immunol 2006;177:120-9. (Pubitemid 43939123)
40. Moga E, Alvarez E, Canto E, Vidal S, Rodriguez-Sanchez JL, Sierra J, et al. NK cells stimulated with IL-15 or CpG ODN enhance rituximab-dependent cellular cytotoxicity against B-cell lymphoma. Exp Hematol 2008;36:69-77. (Pubitemid 350266964)
41. Parihar R, Dierksheide J, Hu Y, Carson WE. IL-12 enhances the natural killer cell cytokine response to Ab-coated tumor cells. J Clin Invest 2002;110:983-92.
42. Jaime-Ramirez AC, Mundy-Bosse BL, Kondadasula S, Jones NB, Roda JM, Mani A, et al. IL-12 enhances the antitumor actions of trastuzumab via NK cell IFN-{gamma} production. J Immunol 2011;186:3401-9.
43. 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 U S A 2004;101:10116-21. (Pubitemid 38891204)
44. Butchar JP, Mehta P, Justiniano SE, Guenterberg KD, Kondadasula SV, Mo X, et al. Reciprocal regulation of activating and inhibitory Fc {gamma} receptors by TLR7/8 activation: implications for tumor immunotherapy. Clin Cancer Res 2010;16:2065-75.
45. Kariya Y, Inoue N, Kihara T, Okamoto N, Sugie K, Mori T, et al. Activation of human natural killer cells by the protein-bound polysaccharide PSK independently of interferon and interleukin 2. Immunol Lett 1992;31:241-5.
46. Caligiuri MA. Human natural killer cells. Blood 2008;112:461-9.
47. Nakazato H, Koike A, Saji S, Ogawa N, Sakamoto J. Efficacy of immunochemotherapy as adjuvant treatment after curative resection of gastric cancer. Study group of immunochemotherapy with PSK for gastric cancer. Lancet 1994;343:1122-6. (Pubitemid 24142032)
48. Hayakawa K, Mitsuhashi N, Saito Y, Takahashi M, Katano S, Shiojima K, et al. Effect of krestin (PSK) as adjuvant treatment on the prognosis after radical radiotherapy in patients with non-small cell lung cancer. Anticancer Res 1993;13:1815-20.
49. Misch EA, Hawn TR. Toll-like receptor polymorphisms and susceptibility to human disease. Clin Sci (Lond) 2008;114:347-60. (Pubitemid 351397384)