Enhanced TCR footprint by a novel glycolipid increases NKT-dependent tumor protection

Journal of Immunology

Volumn 191, Issue 6, 2013, Pages 2917-2925

  Aspeslagh, Sandrine ^a   Nemcovic, Marek ^b   Pauwels, Nora ^a   Venken, Koen ^a   Wang, Jing ^b   Van Calenbergh, Serge ^a   Zajonc, Dirk M ^b   Elewaut, Dirk ^a  

^a GHENT UNIVERSITY   (Belgium)

^b LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA GALACTOSYLCERAMIDE; ALPHA GALACTOSYLCERAMIDE 6'' (1 NAPHTHYL)UREA; ALPHA GALACTOSYLCERAMIDE 6'' (4 CHLOROPHENYL)CARBAMATE; ALPHA GALACTOSYLCERAMIDE 6'' (PYRIDIN 4 YL)CARBAMATE; AROMATIC COMPOUND; CARBAMIC ACID DERIVATIVE; CD1D ANTIGEN; GAMMA INTERFERON; GLYCOLIPID; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 4; NEW DRUG; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG; UREA DERIVATIVE; ALPHA-GALACTOSYLCERAMIDE; GALACTOSYLCERAMIDE; LYMPHOCYTE ANTIGEN RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BINDING AFFINITY; BINDING KINETICS; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DRUG POTENCY; DRUG STABILITY; DRUG STRUCTURE; DRUG SYNTHESIS; DRUG TARGETING; HUMAN; HUMAN CELL; MOLECULAR STABILITY; MOUSE; NATURAL KILLER T CELL; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FOOTPRINTING; PROTEIN LIPID INTERACTION; PROTEIN PROTEIN INTERACTION; STRUCTURE ACTIVITY RELATION; TH1 CELL; ANIMAL; C57BL MOUSE; CHEMISTRY; EXPERIMENTAL NEOPLASM; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; SURFACE PLASMON RESONANCE;

ANIMALS; GALACTOSYLCERAMIDES; GLYCOLIPIDS; HUMANS; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; NATURAL KILLER T-CELLS; NEOPLASMS, EXPERIMENTAL; RECEPTORS, ANTIGEN, T-CELL; STRUCTURE-ACTIVITY RELATIONSHIP; SURFACE PLASMON RESONANCE;

EID: 85045153238     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1203134     Document Type: Article

References (52)

1. Wu, L., and L. Van Kaer. 2011. Natural killer T cells in health and disease. Front Biosci (Schol Ed) 3: 236-251 (Schol Ed).
2. Fujii, S., K. Shimizu, H. Hemmi, M. Fukui, A. J. Bonito, G. Chen, R. W. Franck, M. Tsuji, and R. M. Steinman. 2006. Glycolipid alpha-C- galactosylceramide is a distinct inducer of dendritic cell function during innate and adaptive immune responses of mice. Proc. Natl. Acad. Sci. USA 103: 11252-11257.
3. Im, J. S., P. Arora, G. Bricard, A. Molano, M. M. Venkataswamy, I. Baine, E. S. Jerud, M. F. Goldberg, A. Baena, K. O. Yu, et al. 2009. Kinetics and cellular site of glycolipid loading control the outcome of natural killer T cell activation. Immunity 30: 888-898.
4. Bai, L., Y. Sagiv, Y. Liu, S. Freigang, K. O. Yu, L. Teyton, S. A. Porcelli, P. B. Savage, and A. Bendelac. 2009. Lysosomal recycling terminates CD1dmediated presentation of short and polyunsaturated variants of the NKT cell lipid antigen alphaGalCer. Proc. Natl. Acad. Sci. USA 106: 10254-10259.
5. Sullivan, B. A., N. A. Nagarajan, G. Wingender, J. Wang, I. Scott, M. Tsuji, R. W. Franck, S. A. Porcelli, D. M. Zajonc, and M. Kronenberg. 2010. Mechanisms for glycolipid antigen-driven cytokine polarization by Valpha14i NKT cells. J. Immunol. 184: 141-153.
6. Tyznik, A. J., E. Farber, E. Girardi, A. Birkholz, Y. Li, S. Chitale, R. So, P. Arora, A. Khurana, J. Wang, et al. 2011. Glycolipids that elicit IFN-g-biased responses from natural killer T cells. Chem. Biol. 18: 1620-1630.
7. Aspeslagh, S., Y. Li, E. D. Yu, N. Pauwels, M. Trappeniers, E. Girardi, T. Decruy, K. Van Beneden, K. Venken, M. Drennan, et al. 2011. Galactosemodified iNKT cell agonists stabilized by an induced fit of CD1d prevent tumour metastasis. EMBO J. 30: 2294-2305.
8. Venkataswamy, M. M., and S. A. Porcelli. 2010. Lipid and glycolipid antigens of CD1d-restricted natural killer T cells. Semin. Immunol. 22: 68-78.
9. Joyce, S., E. Girardi, and D. M. Zajonc. 2011. NKT cell ligand recognition logic: molecular basis for a synaptic duet and transmission of inflammatory effectors. J. Immunol. 187: 1081-1089.
10. Scott-Browne, J. P., J. L. Matsuda, T. Mallevaey, J. White, N. A. Borg, J. McCluskey, J. Rossjohn, J. Kappler, P. Marrack, and L. Gapin. 2007. Germline-encoded recognition of diverse glycolipids by natural killer T cells. Nat. Immunol. 8: 1105-1113.
11. Fujio, M., D.Wu, R. Garcia-Navarro, D. D. Ho, M. Tsuji, and C. H. Wong. 2006. Structure-based discovery of glycolipids for CD1d-mediated NKT cell activation: tuning the adjuvant versus immunosuppression activity. J. Am. Chem. Soc. 128: 9022-9023.
12. Liang, P. H., M. Imamura, X. Li, D. Wu, M. Fujio, R. T. Guy, B. C. Wu, M. Tsuji, and C. H. Wong. 2008. Quantitative microarray analysis of intact glycolipid-CD1d interaction and correlation with cell-based cytokine production. J. Am. Chem. Soc. 130: 12348-12354.
13. Wu, T. N., K. H. Lin, Y. J. Chang, J. R. Huang, J. Y. Cheng, A. L. Yu, and C. H. Wong. 2011. Avidity of CD1d-ligand-receptor ternary complex contributes to T-helper 1 (Th1) polarization and anticancer efficacy. Proc. Natl. Acad. Sci. USA 108: 17275-17280.
14. Wun, K. S., G. Cameron, O. Patel, S. S. Pang, D. G. Pellicci, L. C. Sullivan, S. Keshipeddy, M. H. Young, A. P. Uldrich, M. S. Thakur, et al. 2011. A molecular basis for the exquisite CD1d-restricted antigen specificity and functional responses of natural killer T cells. Immunity 34: 327-339.
15. Girardi, E., E. D. Yu, Y. Li, N. Tarumoto, B. Pei, J. Wang, P. Illarionov, Y. Kinjo, M. Kronenberg, and D. M. Zajonc. 2011. Unique interplay between sugar and lipid in determining the antigenic potency of bacterial antigens for NKT cells. PLoS Biol. 9: e1001189.
16. Li, Y., E. Girardi, J. Wang, E. D. Yu, G. F. Painter, M. Kronenberg, and D. M. Zajonc. 2010. The V{alpha}14 invariant natural killer T cell TCR forces microbial glycolipids and CD1d into a conserved binding mode. J. Exp. Med. 207: 2383-2393.
17. Yu, E. D., E. Girardi, J. Wang, and D. M. Zajonc. 2011. Cutting edge: structural basis for the recognition of b-linked glycolipid antigens by invariant NKT cells. J. Immunol. 187: 2079-2083.
18. Pellicci, D. G., A. J. Clarke, O. Patel, T. Mallevaey, T. Beddoe, J. Le Nours, A. P. Uldrich, J. McCluskey, G. S. Besra, S. A. Porcelli, et al. 2011. Recognition of b-linked self glycolipids mediated by natural killer T cell antigen receptors. Nat. Immunol. 12: 827-833.
19. Trappeniers, M., K. Van Beneden, T. Decruy, U. Hillaert, B. Linclau, D. Elewaut, and S. Van Calenbergh. 2008. 69-Derivatised alpha-GalCer analogues capable of inducing strong CD1d-mediated Th1-biased NKT cell responses in mice. J. Am. Chem. Soc. 130: 16468-16469.
20. Burdin, N., L. Brossay, Y. Koezuka, S. T. Smiley, M. J. Grusby, M. Gui, M. Taniguchi, K. Hayakawa, and M. Kronenberg. 1998. Selective ability of mouse CD1 to present glycolipids: alpha-galactosylceramide specifically stimulates V alpha 14+ NK T lymphocytes. J. Immunol. 161: 3271-3281.
21. Lutz, M. B., N. Kukutsch, A. L. Ogilvie, S. Rössner, F. Koch, N. Romani, and G. Schuler. 1999. An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J. Immunol. Methods 223: 77-92.
22. Cui, J., T. Shin, T. Kawano, H. Sato, E. Kondo, I. Toura, Y. Kaneko, H. Koseki, M. Kanno, and M. Taniguchi. 1997. Requirement for Valpha14 NKT cells in IL-12-mediated rejection of tumors. Science 278: 1623-1626.
23. Franki, A. S., K. Van Beneden, P. Dewint, K. J. Hammond, S. Lambrecht, G. Leclercq, M. Kronenberg, D. Deforce, and D. Elewaut. 2006. A unique lymphotoxin alphabeta-dependent pathway regulates thymic emigration of Valpha14 invariant natural killer T cells. Proc. Natl. Acad. Sci. USA 103: 9160-9165.
24. Wang, J., Y. Li, Y. Kinjo, T. T. Mac, D. Gibson, G. F. Painter, M. Kronenberg, and D. M. Zajonc. 2010. Lipid binding orientation within CD1d affects recognition of Borrelia burgorferi antigens by NKT cells. Proc. Natl. Acad. Sci. USA 107: 1535-1540.
25. Otwinowski, Z. M. W. 1997. Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276: 307-326.
26. Battye, T. G., L. Kontogiannis, O. Johnson, H. R. Powell, and A. G. Leslie. 2011. iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr. D Biol. Crystallogr. 67: 271-281.
27. Vagin, A. A., and A. Teplyakov. 1997. MOLREP: an automated program for molecular replacement. J. Appl. Crystallogr. 30: 1022-1025.
28. Winn, M. D., C. C. Ballard, K. D. Cowtan, E. J. Dodson, P. Emsley, P. R. Evans, R. M. Keegan, E. B. Krissinel, A. G. Leslie, A. McCoy, et al. 2011. Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67: 235-242.
29. Schüttelkopf, A. W., and D. M. van Aalten. 2004. PRODRG: a tool for highthroughput crystallography of protein-ligand complexes. Acta Crystallogr. D Biol. Crystallogr. 60: 1355-1363.
30. Emsley, P., and K. Cowtan. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60: 2126-2132.
31. Vagin, A. A., R. A. Steiner, A. A. Lebedev, L. Potterton, S. McNicholas, F. Long, and G. N. Murshudov. 2004. REFMAC5 dictionary: organization of prior chemical knowledge and guidelines for its use. Acta Crystallogr. D Biol. Crystallogr. 60: 2184-2195.
32. Chen, V. B., W. B. Arendall, III, J. J. Headd, D. A. Keedy, R. M. Immormino, G. J. Kapral, L. W. Murray, J. S. Richardson, and D. C. Richardson. 2010. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66: 12-21.
33. Pauwels, N., S. Aspeslagh, G. Vanhoenacker, K. Sandra, E. D. Yu, D. M. Zajonc, D. Elewaut, B. Linclau, and S. Van Calenbergh. 2011. Divergent synthetic approach to 60-modified a-GalCer analogues. Org. Biomol. Chem. 9: 8413-8421.
34. Smyth, M. J., N. Y. Crowe, D. G. Pellicci, K. Kyparissoudis, J. M. Kelly, K. Takeda, H. Yagita, and D. I. Godfrey. 2002. Sequential production of interferon-gamma by NK1.1(+) T cells and natural killer cells is essential for the antimetastatic effect of alpha-galactosylceramide. Blood 99: 1259-1266.
35. Wesley, J. D., S. H. Robbins, S. Sidobre, M. Kronenberg, S. Terrizzi, and L. Brossay. 2005. Cutting edge: IFN-gamma signaling to macrophages is required for optimal Valpha14i NK T/NK cell cross-talk. J. Immunol. 174: 3864-3868.
36. Vincent, M. S., D. S. Leslie, J. E. Gumperz, X. Xiong, E. P. Grant, and M. B. Brenner. 2002. CD1-dependent dendritic cell instruction. Nat. Immunol. 3: 1163-1168.
37. Fujii, S., K. Shimizu, C. Smith, L. Bonifaz, and R. M. Steinman. 2003. Activation of natural killer T cells by alpha-galactosylceramide rapidly induces the full maturation of dendritic cells in vivo and thereby acts as an adjuvant for combined CD4 and CD8 T cell immunity to a coadministered protein. J. Exp. Med. 198: 267-279.
38. Zaini, J., S. Andarini, M. Tahara, Y. Saijo, N. Ishii, K. Kawakami, M. Taniguchi, K. Sugamura, T. Nukiwa, and T. Kikuchi. 2007. OX40 ligand expressed by DCs costimulates NKT and CD4+ Th cell antitumor immunity in mice. J. Clin. Invest. 117: 3330-3338.
39. Zietara, N., M. Lyszkiewicz, A. Krueger, and S. Weiss. 2011. ICOS-dependent stimulation of NKT cells by marginal zone B cells. Eur. J. Immunol. 41: 3125-3134.
40. Akbari, O., P. Stock, E. H. Meyer, G. J. Freeman, A. H. Sharpe, D. T. Umetsu, and R. H. DeKruyff. 2008. ICOS/ICOSL interaction is required for CD4+ invariant NKT cell function and homeostatic survival. J. Immunol. 180: 5448-5456.
41. Hayakawa, Y., K. Takeda, H. Yagita, L. Van Kaer, I. Saiki, and K. Okumura. 2001. Differential regulation of Th1 and Th2 functions of NKT cells by CD28 and CD40 costimulatory pathways. J. Immunol. 166: 6012-6018.
42. Bezbradica, J. S., A. K. Stanic, N. Matsuki, H. Bour-Jordan, J. A. Bluestone, J. W. Thomas, D. Unutmaz, L. Van Kaer, and S. Joyce. 2005. Distinct roles of dendritic cells and B cells in Va14Ja18 natural T cell activation in vivo. J. Immunol. 174: 4696-4705.
43. Bai, L., M. G. Constantinides, S. Y. Thomas, R. Reboulet, F. Meng, F. Koentgen, L. Teyton, P. B. Savage, and A. Bendelac. 2012. Distinct APCs explain the cytokine bias of a-galactosylceramide variants in vivo. J. Immunol. 188: 3053-3061.
44. Sidobre, S., O. V. Naidenko, B. C. Sim, N. R. Gascoigne, K. C. Garcia, and M. Kronenberg. 2002. The V alpha 14 NKT cell TCR exhibits high-affinity binding to a glycolipid/CD1d complex. J. Immunol. 169: 1340-1348.
45. Granucci, F., C. Vizzardelli, N. Pavelka, S. Feau, M. Persico, E. Virzi, M. Rescigno, G. Moro, and P. Ricciardi-Castagnoli. 2001. Inducible IL-2 production by dendritic cells revealed by global gene expression analysis. Nat. Immunol. 2: 882-888.
46. Wilson, M. T., C. Johansson, D. Olivares-Villagómez, A. K. Singh, A. K. Stanic, C. R. Wang, S. Joyce, M. J. Wick, and L. Van Kaer. 2003. The response of natural killer T cells to glycolipid antigens is characterized by surface receptor downmodulation and expansion. Proc. Natl. Acad. Sci. USA 100: 10913-10918.
47. Li, X., M. Fujio, M. Imamura, D. Wu, S. Vasan, C. H. Wong, D. D. Ho, and M. Tsuji. 2010. Design of a potent CD1d-binding NKT cell ligand as a vaccine adjuvant. Proc. Natl. Acad. Sci. USA 107: 13010-13015.
48. Schiefner, A., M. Fujio, D. Wu, C. H. Wong, and I. A. Wilson. 2009. Structural evaluation of potent NKT cell agonists: implications for design of novel stimulatory ligands. J. Mol. Biol. 394: 71-82.
49. Matsuda, J. L., L. Gapin, J. L. Baron, S. Sidobre, D. B. Stetson, M. Mohrs, R. M. Locksley, and M. Kronenberg. 2003. Mouse V alpha 14i natural killer T cells are resistant to cytokine polarization in vivo. Proc. Natl. Acad. Sci. USA 100: 8395-8400.
50. Wesley, J. D., M. S. Tessmer, D. Chaukos, and L. Brossay. 2008. NK cell-like behavior of Valpha14i NK T cells during MCMV infection. PLoS Pathog. 4: e1000106.
51. van den Heuvel, M. J., N. Garg, L. Van Kaer, and S. M. Haeryfar. 2011. NKT cell costimulation: experimental progress and therapeutic promise. Trends Mol. Med. 17: 65-77.
52. Yu, K. O., J. S. Im, A. Molano, Y. Dutronc, P. A. Illarionov, C. Forestier, N. Fujiwara, I. Arias, S. Miyake, T. Yamamura, et al. 2005. Modulation of CD1d-restricted NKT cell responses by using N-acyl variants of alpha-galactosylceramides. Proc. Natl. Acad. Sci. USA 102: 3383-3388.