Defective NKT cell activation by CD1d+ TRAMP prostate tumor cells is corrected by interleukin-12 with alpha-galactosylceramide

PLoS ONE

Volumn 5, Issue 6, 2010, Pages

  Nowak, Michael ^a,b   Arredouani, Mohammed S ^a   Tun Kyi, Adrian ^a   Schmidt Wolf, Ingo ^b   Sanda, Martin G ^a   Balk, Steven P ^a   Exley, Mark A ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF BONN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA GALACTOSYLCERAMIDE; CD1D ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 12 RECEPTOR; INTERLEUKIN 2 RECEPTOR ALPHA; MACROPHAGE DERIVED CHEMOKINE; PROGRAMMED DEATH 1 RECEPTOR; RANTES; STAT4 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CELL ACTIVATION; CELL DAMAGE; CELL INFILTRATION; CELL INTERACTION; CELL MIGRATION; CONTROLLED STUDY; CYTOKINE RELEASE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NATURAL KILLER T CELL; NONHUMAN; PROSTATE TUMOR; PROTEIN PHOSPHORYLATION; RECEPTOR BINDING; SIGNAL TRANSDUCTION; TUMOR CELL; UPREGULATION;

ANIMALS; ANTIGENS, CD1D; BLOTTING, WESTERN; CELL LINE, TUMOR; CELL SEPARATION; CYTOKINES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GALACTOSYLCERAMIDES; INTERLEUKIN-12; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, INBRED C57BL; PROSTATIC NEOPLASMS;

MURINAE;

EID: 77955321049     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0011311     Document Type: Article

References (46)

1. Bendelac A, Savage PB, Teyton L (2007) The biology of NKT cells. Annu Rev Immunol 25: 297-336.
2. Nowak M, Stein-Streilein J (2007) Invariant NKT cells and tolerance. Int Rev Immunol 26: 95-119.
3. Parekh VV, Wilson MT, Van Kaer L (2005) INKT-cell responses to glycolipids. Crit Rev Immunol 25: 183-213.
4. Matsuda JL, Mallevaey T, Scott-Browne J, Gapin L (2008) CD1d-restricted iNKT cells, the 'Swiss-Army knife' of the immune system. Curr Opin Immunol 20: 358-368.
5. Bellone M, Ceccon M, Grioni M, Jachetti E, Calcinotto A, et al. (2010) INKT cells control mouse spontaneous carcinoma independently of tumor-specific cytotoxic T cells. PLoS One 5: e8646.
6. Tahir SM, Cheng O, Shaulov A, Koezuka Y, Bubley GJ, et al. (2001) Loss of IFN-gamma production by invariant NK T cells in advanced cancer. J Immunol 167: 4046-4050.
7. Dhodapkar MV, Geller MD, Chang DH, Shimizu K, Fujii S, et al. (2003) A reversible defect in natural killer T cell function characterizes the progression of premalignant to malignant multiple myeloma. J Exp Med 197: 1667-1676.
8. van der Vliet HJ, Molling JW, Nishi N, Masterson AJ, Kolgen W, et al. (2003) Polarization of Valpha24+Vbeta11+ natural killer T cells of healthy volunteers and cancer patients using alpha-galactosylceramide-loaded and environmentally instructed dendritic cells. Cancer Res 53: 4101-4106.
9. Molling JW, Kolgen W, van der Vliet HJ, Boomsma MF, Kruizenga H, et al. (2005) Peripheral blood IFN-gamma-secreting Valpha24+Vbeta11+ NKT cell numbers are decreased in cancer patients independent of tumor type or tumor load. Int J Cancer 116: 87-93.
10. Cui J, Shin T, Kawano T, Sato H, Kondo E, et al. (1997) Requirement for Valpha14 NKT cells in IL-12-mediated rejection of tumors. Science 278: 1623-1626.
11. Motohashi S, Nakayama T (2008) Clinical applications of natural killer T cellbased immunotherapy for cancer. Cancer Sci 99: 638-645.
12. Fujii S, Shimizu K, Kronenberg M, Steinman RM (2002) Prolonged IFNgamma producing NKT response induced with alphagalactosylceramideloaded DCs. Nat Immunol 3: 867-874.
13. Moodycliffe AM, Nghiem D, Clydesdale G, Ullrich SE (2000) Immune suppression and skin cancer development: regulation by NKT cells. Nat Immunol 1: 521-525.
14. Kitamura H, Iwakabe K, Yahata T, Nishimura S, Ohta A, et al. (1999) The natural killer T (NKT) cell ligand alpha-galactosylceramide demonstrates its immunopotentiating effect by inducing interleukin (IL)- 12 production by dendritic cells and IL-12 receptor expression on NKT cells. J Exp Med 189: 1121-1128.
15. Hayakawa Y, Takeda K, Yagita H, Van Kaer L, Saiki I, et al. (2001) Differential regulation of Th1 and Th2 functions of NKT cells by CD28 and CD40 costimulatory pathways. J Immunol 166: 6012-6018.
16. Manetti R, Parronchi P, Giudizi MG, Piccinni MP, Maggi E, et al. (1993) Natural killer cell stimulatory factor (interleukin 12 [IL-12]) induces T helper type 1 (Th1)-specific immune responses and inhibits the development of IL-4-producing Th cells. J Exp Med 177: 1199-1204.
17. Cocco C, Pistoia V, Airoldi I (2009) New perspectives for melanoma immunotherapy: role of IL-12. Curr Mol Med 9: 459-469.
18. Greenberg NM, DeMayo F, Finegold MJ, Medina D, Tilley WD, et al. (1995) Prostate cancer in a transgenic mouse. Proc Natl Acad Sci U S A 92: 3439-3443.
19. Inaba K, Inaba M, Romani N, Aya H, Deguchi M, et al. (1992) Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J Exp Med 176: 1693-1702.
20. Beldi G, Wu Y, Banz Y, Nowak M, Miller L, et al. (2008) Natural killer T cell dysfunction in CD39-null mice protects against concanavalin A-induced hepatitis. Hepatology 48: 841-852.
21. Sidobre S, Kronenberg M (2002) CD1 tetramers: a powerful tool for the analysis of glycolipid-reactive T cells. J Immunol Methods 268: 107-121.
22. Shi M, Bi X, Xu S, He Y, Guo X, et al. (2005) Increased susceptibility of tumorigenicity and decreased anti-tumor effect of DC vaccination in aged mice are potentially associated with increased number of NK1.1+CD3+ NKT cells. Exp Oncol 27: 125-129.
23. Kim CH, Johnston B, Butcher EC (2002) Trafficking machinery of NKT cells: shared and differential chemokine receptor expression among Valpha24+Vbeta11+ NKT cell subsets with distinct cytokine-producing capacity. Blood 100: 11-16.
24. Thomas SY, Hou R, Boyson JE, Means TK, Hess C, et al. (2003) CD1drestricted NKT cells express a chemokine receptor profile indicative of Th1-type inflammatory homing cells. J Immunol 171: 2571-2580.
25. Lu Y, Cai Z, Galson DL, Xiao G, Liu Y, et al. (2006) Monocyte chemotactic protein-1 (MCP-1) acts as a paracrine and autocrine factor for prostate cancer growth and invasion. Prostate 66: 1311-1318.
26. Mazzucchelli L, Loetscher P, Kappeler A, Uguccioni M, Baggiolini M, et al. (1996) Monocyte chemoattractant protein-1 gene expression in prostatic hyperplasia and prostate adenocarcinoma. Am J Pathol 149: 501-509.
27. Luther SA, Cyster JG (2001) Chemokines as regulators of T cell differentiation. Nat Immunol 2: 102-107.
28. Metelitsa LS, Wu HW, Wang H, Yang Y, Warsi Z, et al. (2004) Natural killer T cells infiltrate neuroblastomas expressing the chemokine CCL2. J Exp Med 199: 1213-1221.
29. Park SH, Roark JH, Bendelac A (1998) Tissue-specific recognition of mouse CD1 molecules. J Immunol 160: 3128-3134.
30. Roark JH, Park SH, Jayawardena J, Kavita U, Shannon M, et al. (1998) CD1.1 expression by mouse antigen-presenting cells and marginal zone B cells. J Immunol 160: 3121-3127.
31. Bleicher PA, Balk SP, Hagen SJ, Blumberg RS, Flotte TJ, et al. (1990) Expression of murine CD1 on gastrointestinal epithelium. Science 250: 679-682.
32. Mandal M, Chen XR, Alegre ML, Chiu NM, Chen YH, et al. (1998) Tissue distribution, regulation and intracellular localization of murine CD1 molecules. Mol Immunol 35: 525-536.
33. Metelitsa LS, Weinberg KI, Emanuel PD, Seeger RC (2003) Expression of CD1d by myelomonocytic leukemias provides a target for cytotoxic NKT cells. Leukemia 17: 1068-1077.
34. Fais F, Morabito F, Stelitano C, Callea V, Zanardi S, et al. (2004) CD1d is expressed on B-chronic lymphocytic leukemia cells and mediates alphagalactosylceramide presentation to natural killer T lymphocytes. Int J Cancer 109: 402-411.
35. Brutkiewicz RR, Bennink JR, Yewdell JW, Bendelac A (1995) TAPindependent, beta 2-microglobulin-dependent surface expression of functional mouse CD1.1. J Exp Med 182: 1913-1919.
36. Watford WT, Moriguchi M, Morinobu A, O'Shea JJ (2003) The biology of IL-12: coordinating innate and adaptive immune responses. Cytokine Growth Factor Rev 14: 361-368.
37. Reddy M, Wong J, Davis C, Prabhakar U (2005) Co-expression of IL-12 receptors along with CXCR3 and CD25 on activated peripheral blood T lymphocytes. Cell Immunol 236: 123-130.
38. Parekh VV, Lalani S, Kim S, Halder R, Azuma M, et al. (2009) PD-1/PD-L blockade prevents anergy induction and enhances the anti-tumor activities of glycolipid-activated invariant NKT cells. J Immunol 182: 2816-2826.
39. Chang WS, Kim JY, Kim YJ, Kim YS, Lee JM, et al. (2008) Cutting edge: Programmed death-1/programmed death ligand 1 interaction regulates the induction and maintenance of invariant NKT cell anergy. J Immunol 181: 6707-6710.
40. Darnell JE, Jr., Kerr IM, Stark GR (1994) Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 264: 1415-1421.
41. Yang YF, Tomura M, Ono S, Hamaoka T, Fujiwara H (2000) Requirement for IFN-gamma in IL-12 production induced by collaboration between Valpha14+NKT cells and antigen-presenting cells. Int Immunol 12: 1669-1675.
42. Brigl M, Bry L, Kent SC, Gumperz JE, Brenner MB (2003) Mechanism of CD1d-restricted natural killer T cell activation during microbial infection. Nat Immunol 4: 1230-1237.
43. Ortaldo JR, Young HA (2005) Mouse Ly49 NK receptors: balancing activation and inhibition. Mol Immunol 42: 445-450.
44. Fasso M, Waitz R, Hou Y, Rim T, Greenberg NM, et al. (2008) SPAS-1 (stimulator of prostatic adenocarcinoma-specific T cells)/SH3GLB2: A prostate tumor antigen identified by CTLA-4 blockade. Proc Natl Acad Sci U S A 105: 3509-3514.
45. van der Vliet HJ, Wang R, Yue SC, Koon HB, Balk SP, et al. (2008) Circulating myeloid dendritic cells of advanced cancer patients result in reduced activation and a biased cytokine profile in invariant NKT cells. J Immunol 180: 7287-7293.
46. Matsuda JL, Gapin L, Baron JL, Sidobre S, Stetson DB, et al. (2003) Mouse V alpha 14i natural killer T cells are resistant to cytokine polarization in vivo. Proc Natl Acad Sci U S A 100: 8395-8400.