Natural killer T cell activation overcomes immunosuppression to enhance clearance of postsurgical breast cancer metastasis in mice

OncoImmunology

Volumn 4, Issue 3, 2015, Pages 1-11

  Gebremeskel, Simon ^a,b   Clattenburg, Daniel R ^a,b   Slauenwhite, Drew ^a   Lobert, Lynnea ^a,b   Johnston, Brent ^a,b  

^a DALHOUSIE UNIVERSITY   (Canada)

^b Beatrice Hunter Cancer Research Institute   (Canada)

Author keywords

Dendritic cells; Metastatic breast cancer; Myeloid derived suppressor cells; Natural killer T cells; Tumor immunotherapy

Indexed keywords

(2,3,4) 1 (ALPHA D GALACTIPYRANOSYL) 2 TETRACOSANOYLAMINONONAN 3,4 DIOL; (2,3,4) 1 CH2 (ALPHA D GALACTIPYRANOSYL) 2 (N HEXACOSANOYLAMINO) 1,3,4 OCTADECANETRIOL; (2,3,4) 1 O (ALPHA D GALACTIPYRANOSYL) 2 (N HEXACOSANOYLAMINO) 1,3,4 OCTADECANETRIOL; CD11B ANTIGEN; CELL THERAPY AGENT; GAMMA INTERFERON; GLYCOLIPID; INTERLEUKIN 4; UNCLASSIFIED DRUG;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; CANCER IMMUNOTHERAPY; CELL ACTIVATION; CELL ISOLATION; CELL PROLIFERATION; COLONY FORMING UNIT; CONTROLLED STUDY; DENDRITIC CELL; DRUG DOSE COMPARISON; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; METASTASIS; MORTALITY; MOUSE; NATURAL KILLER T CELL; NONHUMAN; OVERALL SURVIVAL; POSTOPERATIVE CARE; SUPPRESSOR CELL;

EID: 84934348359     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.1080/2162402X.2014.995562     Document Type: Article

References (62)

1. Brennan PJ, Brigl M, Brenner MB. Invariant natural killer T cells: an innate activation scheme linked to diverse effector functions. Nat Rev Immunol 2013; 13:101-17; PMID:23334244; http://dx.doi.org/10.1038/nri3369
2. Van Kaer L, Parekh VV, Wu L. Invariant natural killer T cells: bridging innate and adaptive immunity. Cell Tissue Res 2011; 343:43-55; PMID:20734065; http://dx.doi.org/10.1007/s00441-010-1023-3
3. Lantz O, Bendelac A. An invariant T cell receptor a chain is used by a unique subset of major histocompatibility complex class I-specific CD4+ and CD4-8- T cells in mice and humans. J Exp Med 1994; 180:1097-106; PMID:7520467; http://dx.doi.org/10.1084/jem.180.3.1097
4. Kawano T, Cui J, Koezuka Y, Toura I, Kaneko Y, Motoki K, Ueno H, Nakagawa R, Sato H, Kondo E et al. CD1d-restricted and TCR-mediated activation of Va14 NKT cells by glycosylceramides. Science 1997; 278:1626-9; PMID:9374463; http://dx.doi.org/10.1126/science.278.5343.1626
5. Gumperz JE, Miyake S, Yamamura T, Brenner MB. Functionally distinct subsets of CD1d-restricted natural killer T cells revealed by CD1d tetramer staining. J Exp Med 2002; 195:625-36; PMID:11877485; http://dx.doi.org/10.1084/jem.20011786
6. Coquet JM, Chakravarti S, Kyparissoudis K, McNab FW, Pitt LA, McKenzie BS, Berzins SP, Smyth MJ, Godfrey DI. Diverse cytokine production by NKT cell subsets and identification of an IL-17-producing CD4-NK1.1- NKT cell population. Proc Natl Acad Sci U S A 2008; 105:11287-92; PMID:18685112; http://dx.doi.org/10.1073/pnas.0801631105
7. Cullen R, Germanov E, Shimaoka T, Johnston B. Enhanced tumor metastasis in response to blockade of the chemokine receptor CXCR6 is overcome by NKT cell activation. J Immunol 2009; 183:5807-15; PMID:19812206; http://dx.doi.org/10.4049/jimmunol.0803520
8. Smyth MJ, Thia KY, Street SE, Cretney E, Trapani JA, Taniguchi M, Kawano T, Pelikan SB, Crowe NY, Godfrey DI. Differential tumor surveillance by natural killer (NK) and NKT cells. J Exp Med 2000; 191:661-8; PMID:10684858; http://dx.doi.org/10.1084/jem.191.4.661
9. Swann JB, Uldrich AP, van Dommelen S, Sharkey J, Murray WK, Godfrey DI, Smyth MJ. Type I natural killer T cells suppress tumors caused by p53 loss in mice. Blood 2009; 113:6382-5; PMID:19234138; http://dx.doi.org/10.1182/blood-2009-01-198564
10. Wu DY, Segal NH, Sidobre S, Kronenberg M, Chapman PB. Cross-presentation of disialoganglioside GD3 to natural killer T cells. J Exp Med 2003; 198:173-81; PMID:12847141; http://dx.doi.org/10.1084/jem.20030446
11. Zhou D, Mattner J, Cantu 3rd C, Schrantz N, Yin N, Gao Y, Sagiv Y, Hudspeth K, Wu YP, Yamashita T et al. Lysosomal glycosphingolipid recognition by NKT cells. Science 2004; 306:1786-9; PMID: 15539565; http://dx.doi.org/10.1126/science.1103440
12. Mattner J, Debord KL, Ismail N, Goff RD, Cantu 3rd C, Zhou D, Saint-Mezard P, Wang V, Gao Y, Yin N et al. Exogenous and endogenous glycolipid antigens activate NKT cells during microbial infections. Nature 2005; 434:525-9; PMID:15791258; http://dx.doi.org/10.1038/nature03408
13. Leite-de-Moraes MC, Hameg A, Arnould A, Machavoine F, Koezuka Y, Schneider E, Herbelin A, Dy M. A distinct IL-18-induced pathway to fully activate NK T lymphocytes independently from TCR engagement. J Immunol 1999; 163:5871-6; PMID:10570271
14. Brigl M, Tatituri RV V, Watts GFM, Bhowruth V, Leadbetter EA, Barton N, Cohen NR, Hsu F-F, Besra GS, Brenner MB. Innate and cytokine-driven signals, rather than microbial antigens, dominate in natural killer T cell activation during microbial infection. J Exp Med 2011; 208:1163-77; PMID: 21555485; http://dx.doi.org/10.1084/jem.20102555
15. Fujii S-I, Shimizu K, Okamoto Y, Kunii N, Nakayama T, Motohashi S, Taniguchi M. NKT cells as an ideal antitumor immunotherapeutic. Front Immunol 2013; 4:409; PMID:24348476; http://dx.doi.org/10.3389/fimmu.2013.00409
16. Kawano T, Cui J, Koezuka Y, Toura I, Kaneko Y, Sato H, Kondo E, Harada M, Koseki H, Nakayama T et al. Natural killer-like nonspecific tumor cell lysis mediated by specific ligand-activated Va14 NKT cells. Proc Natl Acad Sci USA 1998; 95:5690-3; PMID:9576945; http://dx.doi.org/10.1073/pnas.95.10.5690
17. Motohashi S, Ishikawa A, Ishikawa E, Otsuji M, Iizasa T, Hanaoka H, Shimizu N, Horiguchi S, Okamoto Y, Fujii S et al. A phase I study of in vitro expanded natural killer T cells in patients with advanced and recurrent non-small cell lung cancer. Clin Cancer Res 2006; 12:6079-86; PMID:17028247; http://dx.doi.org/10.1158/1078-0432.CCR-06-0114
18. Ishikawa A, Motohashi S, Ishikawa E, Fuchida H, Higashino K, Otsuji M, Iizasa T, Nakayama T, Taniguchi M, Fujisawa T. A phase I study of a-galactosylceramide (KRN7000)-pulsed dendritic cells in patients with advanced and recurrent non-small cell lung cancer. Clin Cancer Res 2005; 11:1910-7; PMID:15756017; http://dx.doi.org/10.1158/1078-0432.CCR-04-1453
19. Kunii N, Horiguchi S, Motohashi S, Yamamoto H, Ueno N, Yamamoto S, Sakurai D, Taniguchi M, Nakayama T, Okamoto Y. Combination therapy of in vitro-expanded natural killer T cells and a-galactosylceramide- pulsed antigen-presenting cells in patients with recurrent head and neck carcinoma. Cancer Sci 2009; 100:1092-8; PMID:19302288; http://dx.doi.org/10.1111/j.1349-7006.2009.01135.x
20. Motohashi S, Nagato K, Kunii N, Yamamoto H, Yamasaki K, Okita K, Hanaoka H, Shimizu N, Suzuki M, Yoshino I et al. A phase I-II study of a-galactosylceramide- pulsed IL-2/GM-CSF-cultured peripheral blood mononuclear cells in patients with advanced and recurrent non-small cell lung cancer. J Immunol 2009; 182:2492-501; PMID:19201905; http://dx.doi.org/10.4049/jimmunol.0800126
21. Teng MWL, Westwood JA, Darcy PK, Sharkey J, Tsuji M, Franck RW, Porcelli SA, Besra GS, Takeda K, Yagita H et al. Combined natural killer T-cell based immunotherapy eradicates established tumors in mice. Cancer Res 2007; 67:7495-504; PMID:17671220; http://dx.doi.org/10.1158/0008-5472.CAN-07-0941
22. Hayakawa Y, Rovero S, Forni G, Smyth MJ. α-galactosylceramide (KRN7000) suppression of chemical- and oncogene-dependent carcinogenesis. Proc Natl Acad Sci U S A 2003; 100:9464-9; PMID:12867593; http://dx.doi.org/10.1073/pnas.1630663100
23. Gabrilovich DI, Ostrand-Rosenberg S, Bronte V. Coordinated regulation of myeloid cells by tumours. Nat Rev 2012; 12:253-68; PMID:22437938; http://dx.doi.org/10.1038/nri3175
24. Almand B, Clark JI, Nikitina E, van Beynen J, English NR, Knight SC, Carbone DP, Gabrilovich DI. Increased production of immature myeloid cells in cancer patients: a mechanism of immunosuppression in cancer. J Immunol 2001; 166:678-89; PMID:11123353; http://dx.doi.org/10.4049/jimmunol.166.1.678
25. Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev 2009; 9:162-74; PMID:19197294; http://dx.doi.org/10.1038/nri2506
26. Mundy-Bosse BL, Lesinski GB, Jaime-Ramirez AC, Benninger K, Khan M, Kuppusamy P, Guenterberg K, Kondadasula SV, Chaudhury AR, La Perle KM et al. Myeloid-derived suppressor cell inhibition of the IFN response in tumor-bearing mice. Cancer Res 2011; 71:5101-10; PMID:21680779; http://dx.doi.org/10.1158/0008-5472.CAN-10-2670
27. Wesolowski R, Markowitz J, Carson WE. Myeloid derived suppressor cells—a new therapeutic target in the treatment of cancer. J Immunother Cancer 2013; 1:10; PMID:24829747; http://dx.doi.org/10.1186/2051-1426-1-10
28. Alizadeh D, Larmonier N. Chemotherapeutic targeting of cancer-induced immunosuppressive cells. Cancer Res 2014; 74:2663-8; PMID:24778417; http://dx.doi.org/10.1158/0008-5472.CAN-14-0301
29. De Santo C, Salio M, Masri SH, Lee LY-H, Dong T, Speak AO, Porubsky S, Booth S, Veerapen N, Besra GS et al. Invariant NKT cells reduce the immunosuppressive activity of influenza A virus-induced myeloidderived suppressor cells in mice and humans. J Clin Invest 2008; 118:4036-48; PMID:19033672; http://dx.doi.org/10.1172/JCI36264
30. Nakagawa R, Motoki K, Ueno H. Treatment of hepatic metastasis of the Colon26 adenocarcinoma with an a-Galactosylceramide, KRN7000. Cancer Res 1998; 58:1202-7; PMID:9515806
31. Schmieg J, Yang G, Franck RW, Tsuji M. Superior protection against malaria and melanoma metastases by a C-glycoside analogue of the natural killer T cell ligand a-Galactosylceramide. J Exp Med 2003; 198:1631-41; PMID:14657217; http://dx.doi.org/10.1084/jem.20031192
32. Miyamoto K, Miyake S, Yamamura T. A synthetic glycolipid prevents autoimmune encephalomyelitis by inducing TH2 bias of natural killer T cells. Nature 2001; 413:531-4; PMID:11586362; http://dx.doi.org/10.1038/35097097
33. Smyth MJ, Crowe NY, Pellicci DG, Kyparissoudis K, Kelly JM, Takeda K, Yagita H, Godfrey DI. Sequential production of interferon-g by NK1.1+ T cells and natural killer cells is essential for the antimetastatic effect of a-galactosylceramide. Blood 2002; 99:1259-66; PMID:11830474; http://dx.doi.org/10.1182/blood.V99.4.1259
34. Nishimura T, Nakui M, Sato M, Iwakabe K, Kitamura H, Sekimoto M, Ohta A, Koda T, Nishimura S. The critical role of Th1-dominant immunity in tumor immunology. Cancer Chemother Pharmacol 2000; 46 Suppl: 52-61; PMID:10950149; http://dx.doi.org/10.1007/PL00014051
35. Motohashi S, Okamoto Y, Yoshino I, Nakayama T. Anti-tumor immune responses induced by iNKT cellbased immunotherapy for lung cancer and head and neck cancer. Clin Immunol 2011; 140:167-76; PMID:21349771; http://dx.doi.org/10.1016/j.clim. 2011.01.009
36. Parekh VV, Wilson MT, Olivares-Villagomez D, Singh AK, Wu L, Wang CR, Joyce S, Van Kaer L. Glycolipid antigen induces long-term natural killer T cell anergy in mice. J Clin Invest 2005; 115:2572-83; PMID:16138194; http://dx.doi.org/10.1172/JCI24762
37. Huang J-R, Tsai Y-C, Chang Y-J, Wu J-C, Hung J-T, Lin K-H, Wong C-H, Yu AL. α-Galactosylceramide but not phenyl-glycolipids induced NKT cell anergy and IL-33-mediated myeloid-derived suppressor cell accumulation via upregulation of egr2/3. J Immunol 2014; 192:1972-81; PMID:24465013; http://dx.doi.org/10.4049/jimmunol.1302623
38. Fujii S, Shimizu K, Kronenberg M, Steinman RM. Prolonged IFN-γ-producing NKT response induced with α-galactosylceramide-loaded DCs. Nat Immunol 2002; 3:867-74; PMID:12154358; http://dx.doi.org/10.1038/ni827
39. Nakagawa R, Nagafune I, Tazunoki Y, Ehara H, Tomura H, Iijima R, Motoki K, Kamishohara M, Seki S. Mechanisms of the antimetastatic effect in the liver and of the hepatocyte injury induced by α-galactosylceramide in mice. J Immunol 2001; 166:6578-84; PMID:11359810; http://dx.doi.org/10.4049/jimmunol.166.11.6578
40. Tahir SM, Cheng O, Shaulov A, Koezuka Y, Bubley GJ, Wilson SB, Balk SP, Exley MA. Loss of IFN-γ production by invariant NK T cells in advanced cancer. J Immunol 2001; 167:4046-50; PMID:11564825; http://dx.doi.org/10.4049/jimmunol.167.7.4046
41. Molling JW, Kolgen W, van der Vliet HJ, Boomsma MF, Kruizenga H, Smorenburg CH, Molenkamp BG, Langendijk JA, Leemans CR, von Blomberg BM et al. Peripheral blood IFN-g-secreting Va24+ Vb11+ NKT cell numbers are decreased in cancer patients independent of tumor type or tumor load. Int J Cancer 2005; 116:87-93; PMID:15756674; http://dx.doi.org/10.1002/ijc.20998
42. Diaz-Montero CM, Salem ML, Nishimura MI, Garrett-Mayer E, Cole DJ, Montero AJ. Increased circulating myeloid-derived suppressor cells correlate with clinical cancer stage, metastatic tumor burden, and doxorubicincyclophosphamide chemotherapy. Cancer Immunol Immunother 2009; 58:49-59; PMID:18446337; http://dx.doi.org/10.1007/s00262-008-0523-4
43. Sinha P, Clements VK, Bunt SK, Albelda SM, Ostrand-Rosenberg S. Cross-talk between myeloidderived suppressor cells and macrophages subverts tumor immunity toward a type 2 response. J Immunol 2007; 179:977-83; PMID:17617589; http://dx.doi.org/10.4049/jimmunol.179.2.977
44. Parekh VV, Wu L, Olivares-Villagόmez D, Wilson KT, Van Kaer L. Activated invariant NKT cells control central nervous system autoimmunity in a mechanism that involves myeloid-derived suppressor cells. J Immunol 2013; 190:1948-60; PMID:23345328; http://dx.doi.org/10.4049/jimmunol.1201718
45. Kmieciak M, Basu D, Payne KK, Toor A, Yacoub A, Wang X-Y, Smith L, Bear HD, Manjili MH. Activated NKT cells and NK cells render T cells resistant to myeloid-derived suppressor cells and result in an effective adoptive cellular therapy against breast cancer in the FVBN202 transgenic mouse. J Immunol 2011; 187:708-17; PMID:21670315; http://dx.doi.org/10.4049/jimmunol.1100502
46. Ko H-J, Lee J-M, Kim Y-JY-S, Lee K-A, Kang C-Y. Immunosuppressive myeloid-derived suppressor cells can be converted into immunogenic APCs with the help of activated NKT cells: an alternative cell-based antitumor vaccine. J Immunol 2009; 182:1818-28; PMID:19201833; http://dx.doi.org/10.4049/jimmunol.0802430
47. Ghochikyan A, Davtyan A, Hovakimyan A, Davtyan H, Poghosyan A, Bagaev A, Ataullakhanov RI, Nelson EL, Agadjanyan MG. Primary 4T1 tumor resection provides critical “window of opportunity” for immunotherapy. Clin Exp Metastasis 2014; 31:185-98; PMID:24096737; http://dx.doi.org/10.1007/s10585-013-9619-0
48. Sinha P, Clements VK, Ostrand-Rosenberg S. Reduction of myeloid-derived suppressor cells and induction of M1 macrophages facilitate the rejection of established metastatic disease. J Immunol 2005; 174:636-45; PMID:15634881; http://dx.doi.org/10.4049/jimmunol.174.2.636
49. Predina JD, Kapoor V, Judy BF, Cheng G, Fridlender ZG, Albelda SM, Singhal S. Cytoreduction surgery reduces systemic myeloid suppressor cell populations and restores intratumoral immunotherapy effectiveness. J Hematol Oncol 2012; 5:34; PMID:22742411; http://dx.doi.org/10.1186/1756-8722-5-34
50. Weigelt B, Peterse JL, van ’t Veer LJ. Breast cancer metastasis: markers and models. Nat Rev Cancer 2005; 5:591-602; PMID:16056258; http://dx.doi.org/10.1038/nrc1670
51. Terabe M, Swann J, Ambrosino E, Sinha P, Takaku S, Hayakawa Y, Godfrey DI, Ostrand-Rosenberg S, Smyth MJ, Berzofsky JA. A nonclassical non-Va14Ja18 CD1drestricted (type II) NKT cell is sufficient for down-regulation of tumor immunosurveillance. J Exp Med 2005; 202:1627-33; PMID:16365146; http://dx.doi.org/10.1084/jem.20051381
52. Pilones KA, Kawashima N, Yang AM, Babb JS, Formenti SC, Demaria S. Invariant natural killer T cells regulate breast cancer response to radiation and CTLA-4 blockade. Clin Cancer Res 2009; 15:597-606; PMID:19147765; http://dx.doi.org/10.1158/1078-0432.CCR-08-1277
53. Chen Q, Ross AC. All-trans-retinoic acid and the glycolipid a-galactosylceramide combined reduce breast tumor growth and lung metastasis in a 4T1 murine breast tumor model. Nutr Cancer 2012; 64:1219-27; PMID:23163850; http://dx.doi.org/10.1080/01635581.2012.718404
54. Webb TJ, Li X, Giuntoli RL, Lopez PHH, Heuser C, Schnaar RL, Tsuji M, Kurts C, Oelke M, Schneck JP. Molecular identification of GD3 as a suppressor of the innate immune response in ovarian cancer. Cancer Res 2012; 72:3744-52; PMID:22649190; http://dx.doi.org/10.1158/0008-5472.CAN-11-2695
55. Bezbradica JS, Stanic AK, Matsuki N, Bour-Jordan H, Bluestone JA., Thomas JW, Unutmaz D, Van Kaer L, Joyce S. Distinct roles of dendritic cells and B cells in Va14Ja18 natural T cell activation in vivo. J Immunol 2005; 174:4696-705; PMID:15814694; http://dx.doi.org/10.4049/jimmunol.174.8.4696
56. Yamasaki K, Horiguchi S, Kurosaki M, Kunii N, Nagato K, Hanaoka H, Shimizu N, Ueno N, Yamamoto S, Taniguchi M et al. Induction of NKT cell-specific immune responses in cancer tissues after NKT celltargeted adoptive immunotherapy. Clin Immunol 2011; 138:255-65; PMID:21185787; http://dx.doi.org/10.1016/j.clim.2010.11.014
57. Kim Y-S, Kim Y-J, Lee J-M, Kim E-K, Park Y-J, Choe S-K, Ko H-J, Kang C-Y. Functional changes in myeloid-derived suppressor cells (MDSCs) during tumor growth: FKBP51 contributes to the regulation of the immunosuppressive function of MDSCs. J Immunol 2012; 188:4226-34; PMID:22474024; http://dx.doi.org/10.4049/jimmunol.1103040
58. Payne KK, Zoon CK, Wan W, Marlar K, Keim RC, Kenari MN, Kazim AL, Bear HD, Manjili MH. Peripheral blood mononuclear cells of patients with breast cancer can be reprogrammed to enhance anti-HER-2/neu reactivity and overcome myeloid-derived suppressor cells. Breast Cancer Res Treat 2013; 142:45-57; PMID:24197563; http://dx.doi.org/10.1007/s10549-013-2733-5
59. Song L, Asgharzadeh S, Salo J, Engell K, Wu HW, Sposto R, Ara T, Silverman AM, DeClerck YA, Seeger RC et al. Va24-invariant NKT cells mediate antitumor activity via killing of tumor-associated macrophages. J Clin Invest 2009; 119:1524-36; PMID:19411762; http://dx.doi.org/10.1172/JCI37869
60. Metelitsa LS, Weinberg KI, Emanuel PD, Seeger RC. Expression of CD1d by myelomonocytic leukemias provides a target for cytotoxic NKT cells. Leukemia 2003; 17:1068-77; PMID:12764370; http://dx.doi.org/10.1038/sj.leu.2402943
61. Nieda M, Nicol A, Koezuka Y, Kikuchi A, Lapteva N, Tanaka Y, Tokunaga K, Suzuki K, Kayagaki N, Yagita H et al. TRAIL expression by activated human CD4+ Va24 NKT cells induces in vitro and in vivo apoptosis of human acute myeloid leukemia cells. Blood 2001; 97:2067-74; PMID:11264173; http://dx.doi.org/10.1182/blood.V97.7.2067
62. Gebremeskel S, LeVatte T, Liwski RS, Johnston B, Bezuhly M. The reversible P2Y12 inhibitor ticagrelor inhibits metastasis and improves survival in mouse models of cancer. Int J Cancer 2015; 136:234-40; PMID:24798403; http://dx.doi.org/10.1002/ijc.28947