Expression of CD1c enhances human invariant NKT cell activation by α-GalCer

Cancer Immunity

Volumn 13, Issue 2, 2013, Pages

  Fox, Lisa M ^a   Miksanek, Jennifer ^a   May, Nathan A ^b   Scharf, Louise ^c   Lockridge, Jennifer L ^a   Veerapen, Natacha ^d   Besra, Gurdyal S ^d   Adams, Erin J ^c   Hudson, Amy W ^b   Gumperz, Jenny E ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b MEDICAL COLLEGE OF WISCONSIN   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

^d UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

GalCer; CD1 molecules; Human; iNKT cells

Indexed keywords

ALPHA GALACTOSYLCERAMIDE; CD1C ANTIGEN; CD1D ANTIGEN; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 13; INTERLEUKIN 2; ALPHA-GALACTOSYLCERAMIDE; CD1 ANTIGEN; CD1C PROTEIN, HUMAN; GALACTOSYLCERAMIDE; GLYCOPROTEIN; PROTEIN BINDING;

ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ARTICLE; B LYMPHOCYTE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CROSS REACTION; CYTOKINE RELEASE; DENDRITIC CELL; DRUG PROTEIN BINDING; DRUG TARGETING; HUMAN; HUMAN CELL; IMMUNOGENICITY; IMMUNOSTIMULATION; NATURAL KILLER T CELL; PROTEIN LOCALIZATION; T LYMPHOCYTE ACTIVATION; AMINO ACID SEQUENCE; ANIMAL; BIOSYNTHESIS; CHEMICAL STRUCTURE; HELA CELL LINE; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MOLECULAR GENETICS; MOUSE; Α-GALCER; CD1 MOLECULES; HELA CELL; INKT CELLS; PROTEIN BINDING;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD1; DENDRITIC CELLS; GALACTOSYLCERAMIDES; GLYCOPROTEINS; HELA CELLS; HUMANS; LYMPHOCYTE ACTIVATION; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NATURAL KILLER T-CELLS; PROTEIN BINDING;

Α-GALCER; CD1 MOLECULES; HUMAN; INKT CELLS;

EID: 84879033899     PISSN: 14249634     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (49)

1. Terabe M, Berzofsky JA. The role of NKT cells in tumor immunity. Adv Cancer Res 2008; 101: 277-348. (PMID: 19055947)
2. Cui J, Shin T, Kawano T, Sato H, Kondo E, Toura I, Kaneko Y, Koseki H, Kanno M, Taniguchi M. Requirement for Valpha14 NKT cells in IL-12- mediated rejection of tumors. Science 1997; 278: 1623-1626. (PMID: 9374462)
3. Kitamura H, Iwakabe K, Yahata T, Nishimura S, Ohta A, Ohmi Y, Sato M, Takeda K, Okumura K, Van Kaer L, Kawano T, Taniguchi M, Nishimura T. The natural killer T (NKT) cell ligand alphagalactosylceramide demonstrates its immunopotentiating effect by inducing interleukin (IL)-12 production by dendritic cells and IL-12 receptor expression on NKT cells. J Exp Med 1999; 189: 1121-1128. (PMID: 10190903)
4. 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: 661-668. (PMID: 10684858)
5. Smyth MJ, Crowe NY, Pellicci DG, Kyparissoudis K, Kelly JM, Takeda K, Yagita H, Godfrey DI. Sequential production of interferon-gamma by NK1.1(+) T cells and natural killer cells is essential for the antimetastatic effect of alpha-galactosylceramide. Blood 2002; 99: 1259-1266. (PMID: 11830474)
6. Ishihara S, Nieda M, Kitayama J, Osada T, Yabe T, Kikuchi A, Koezuka Y, Porcelli SA, Tadokoro K, Nagawa H, Juji T. Alpha-glycosylceramides enhance the antitumor cytotoxicity of hepatic lymphocytes obtained from cancer patients by activating CD3-CD56+ NK cells in vitro. J Immunol 2000; 165: 1659-1664. (PMID: 10903777)
7. Fujii S, Shimizu K, Smith C, Bonifaz L, Steinman RM. 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 2003; 198: 267-279. (PMID: 12874260)
8. Silk JD, Hermans IF, Gileadi U, Chong TW, Shepherd D, Salio M, Mathew B, Schmidt RR, Lunt SJ, Williams KJ, Stratford IJ, Harris AL, Cerundolo V. Utilizing the adjuvant properties of CD1d-dependent NK T cells in T cell-mediated immunotherapy. J Clin Invest 2004; 114: 1800-1811. (PMID: 15599405)
9. Chung Y, Qin H, Kang CY, Kim S, Kwak LW, Dong C. An NKT-mediated autologous vaccine generates CD4 T-cell dependent potent antilymphoma immunity. Blood 2007; 110: 2013-2019. (PMID: 17581919)
10. Kawano T, Cui J, Koezuka Y, Toura I, Kaneko Y, Motoki K, Ueno H, Nakagawa R, Sato H, Kondo E, Koseki H, Taniguchi M. CD1drestricted and TCR-mediated activation of valpha14 NKT cells by glycosylceramides. Science 1997; 278: 1626-1629. (PMID: 9374463)
11. Burdin N, Brossay L, Kronenberg M. Immunization with alphagalactosylceramide polarizes CD1-reactive NK T cells towards Th2 cytokine synthesis. Eur J Immunol 1999; 29: 2014-2025. (PMID: 10382765)
12. Carnaud C, Lee D, Donnars O, Park SH, Beavis A, Koezuka Y, Bendelac A. Cutting edge: Cross-talk between cells of the innate immune system: NKT cells rapidly activate NK cells. J Immunol 1999; 163: 4647-4650. (PMID: 10528160)
13. Nieda M, Okai M, Tazbirkova A, Lin H, Yamaura A, Ide K, Abraham R, Juji T, Macfarlane DJ, Nicol AJ. Therapeutic activation of Valpha24+Vbeta11+ NKT cells in human subjects results in highly coordinated secondary activation of acquired and innate immunity. Blood 2004; 103: 383-389. (PMID: 14512316)
14. Chang DH, Osman K, Connolly J, Kukreja A, Krasovsky J, Pack M, Hutchinson A, Geller M, Liu N, Annable R, Shay J, Kirchhoff K, Nishi N, Ando Y, Hayashi K, Hassoun H, Steinman RM, Dhodapkar MV. Sustained expansion of NKT cells and antigen-specific T cells after injection of alpha-galactosyl-ceramide loaded mature dendritic cells in cancer patients. J Exp Med 2005; 201: 1503-1517. (PMID: 15867097)
15. Chang DH, Liu N, Klimek V, Hassoun H, Mazumder A, Nimer SD, Jagannath S, Dhodapkar MV. Enhancement of ligand-dependent activation of human natural killer T cells by lenalidomide: therapeutic implications. Blood 2006; 108: 618-621. (PMID: 16569772)
16. Motohashi S, Nakayama T. Clinical applications of natural killer T cell-based immunotherapy for cancer. Cancer Sci 2008; 99: 638-645. (PMID: 18294290)
17. Schneiders FL, Scheper RJ, von Blomberg BM, Woltman AM, Janssen HL, van den Eertwegh AJ, Verheul HM, de Gruijl TD, van der Vliet HJ. Clinical experience with alpha-galactosylceramide (KRN7000) in patients with advanced cancer and chronic hepatitis B/C infection. Clin Immunol 2011; 140: 130-141. (PMID: 21169066)
18. Taniguchi M, Tashiro T, Dashtsoodol N, Hongo N, Watarai H. The specialized iNKT cell system recognizes glycolipid antigens and bridges the innate and acquired immune systems with potential applications for cancer therapy. Int Immunol 2010; 22: 1-6. (PMID: 19858073)
19. Dhodapkar MV. Harnessing human CD1d restricted T cells for tumor immunity: progress and challenges. Front Biosci 2009; 14: 796-807. (PMID: 19273100)
20. Cerundolo V, Silk JD, Masri SH, Salio M. Harnessing invariant NKT cells in vaccination strategies. Nat Rev Immunol 2009; 9: 28-38. (PMID: 19079136)
21. Martin LH, Calabi F, Milstein C. Isolation of CD1 genes: a family of major histocompatibility complex-related differentiation antigens. Proc Natl Acad Sci U S A 1986; 83: 9154-9158. (PMID: 3097645)
22. Kasmar A, Van Rhijn I, Moody DB. The evolved functions of CD1 during infection. Curr Opin Immunol 2009; 21: 397-403. (PMID: 19541469)
23. Cohen NR, Garg S, Brenner MB. Antigen presentation by CD1 lipids, T cells, and NKT cells in microbial immunity. Adv Immunol 2009; 102: 1-94. (PMID: 19477319)
24. Salio M, Silk JD, Cerundolo V. Recent advances in processing and presentation of CD1 bound lipid antigens. Curr Opin Immunol 2010; 22: 81-88. (PMID: 20080041)
25. Shamshiev A, Gober HJ, Donda A, Mazorra Z, Mori L, De Libero G. Presentation of the same glycolipid by different CD1 molecules. J Exp Med 2002; 195: 1013-1021. (PMID: 11956292)
26. Exley M, Garcia J, Wilson SB, Spada F, Gerdes D, Tahir SM, Patton KT, Blumberg RS, Porcelli S, Chott A, Balk SP. CD1d structure and regulation on human thymocytes, peripheral blood T cells, B cells and monocytes. Immunology 2000; 100: 37-47. (PMID: 10809957)
27. Gumperz JE. The ins and outs of CD1 molecules: bringing lipids under immunological surveillance. Traffic 2006; 7: 2-13. (PMID: 16445682)
28. Zhou D, Cantu C, 3rd, Sagiv Y, Schrantz N, Kulkarni AB, Qi X, Mahuran DJ, Morales CR, Grabowski GA, Benlagha K, Savage P, Bendelac A, Teyton L. Editing of CD1d-bound lipid antigens by endosomal lipid transfer proteins. Science 2004; 303: 523-527. (PMID: 14684827)
29. Kang SJ, Cresswell P. Saposins facilitate CD1d-restricted presentation of an exogenous lipid antigen to T cells. Nat Immunol 2004; 5: 175-181. (PMID: 14716312)
30. Fox LM, Cox DG, Lockridge JL, Wang X, Chen X, Scharf L, Trott DL, Ndonye RM, Veerapen N, Besra GS, Howell AR, Cook ME, Adams EJ, Hildebrand WH, Gumperz JE. Recognition of lyso-phospholipids by human natural killer T lymphocytes. PLoS Biol 2009; 7: e1000228. (PMID: 19859526)
31. Pellicci DG, Patel O, Kjer-Nielsen L, Pang SS, Sullivan LC, Kyparissoudis K, Brooks AG, Reid HH, Gras S, Lucet IS, Koh R, Smyth MJ, Mallevaey T, Matsuda JL, Gapin L, McCluskey J, Godfrey DI, Rossjohn J. Differential recognition of CD1d-alphagalactosyl ceramide by the V beta 8.2 and V beta 7 semi-invariant NKT T cell receptors. Immunity 2009; 31: 47-59. (PMID: 19592275)
32. Scharf L, Li NS, Hawk AJ, Garzon D, Zhang T, Fox LM, Kazen AR, Shah S, Haddadian EJ, Gumperz JE, Saghatelian A, Faraldo-Gomez JD, Meredith SC, Piccirilli JA, Adams EJ. The 2.5 a structure of CD1c in complex with a mycobacterial lipid reveals an open groove ideally suited for diverse antigen presentation. Immunity 2010; 33: 853-862. (PMID: 21167756)
33. Wun KS, Borg NA, Kjer-Nielsen L, Beddoe T, Koh R, Richardson SK, Thakur M, Howell AR, Scott-Browne JP, Gapin L, Godfrey DI, McCluskey J, Rossjohn J. A minimal binding footprint on CD1dglycolipid is a basis for selection of the unique human NKT TCR. J Exp Med 2008; 205: 939-949. (PMID: 18378792)
34. Wang X, Chen X, Rodenkirch L, Simonson W, Wernimont S, Ndonye RM, Veerapen N, Gibson D, Howell AR, Besra GS, Painter GF, Huttenlocher A, Gumperz JE. Natural killer T-cell autoreactivity leads to a specialized activation state. Blood 2008; 112: 4128-4138. (PMID: 18779390)
35. Wulfing C, Sumen C, Sjaastad MD, Wu LC, Dustin ML, Davis MM. Costimulation and endogenous MHC ligands contribute to T cell recognition. Nat Immunol 2002; 3: 42-47. (PMID: 11731799)
36. Krogsgaard M, Li QJ, Sumen C, Huppa JB, Huse M, Davis MM. Agonist/endogenous peptide-MHC heterodimers drive T cell activation and sensitivity. Nature 2005; 434: 238-243. (PMID: 15724150)
37. Krogsgaard M, Juang J, Davis MM. A role for "self " in T-cell activation. Sem Immunol 2007; 19: 236-244. (PMID: 17548210)
38. Allan LL, Stax AM, Zheng DJ, Chung BK, Kozak FK, Tan R, van den Elzen P. CD1d and CD1c expression in human B cells is regulated by activation and retinoic acid receptor signaling. J Immunol 2011; 186: 5261-5272. (PMID: 21451111)
39. Blair PA, Norena LY, Flores-Borja F, Rawlings DJ, Isenberg DA, Ehrenstein MR, Mauri C. CD19(+)CD24(hi)CD38(hi) B cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic Lupus Erythematosus patients. Immunity 2010; 32: 129-140. (PMID: 20079667)
40. Leslie DS, Dascher CC, Cembrola K, Townes MA, Hava DL, Hugendubler LC, Mueller E, Fox L, Roura-Mir C, Moody DB, Vincent MS, Gumperz JE, Illarionov PA, Besra GS, Reynolds CG, Brenner MB. Serum lipids regulate dendritic cell CD1 expression and function. Immunology 2008; 125: 289-301. (PMID: 18445008)
41. Szatmari I, Pap A, Ruhl R, Ma JX, Illarionov PA, Besra GS, Rajnavolgyi E, Dezso B, Nagy L. PPARgamma controls CD1d expression by turning on retinoic acid synthesis in developing human dendritic cells. J Exp Med 2006; 203: 2351-2362. (PMID: 16982809)
42. Mostoslavsky G, Fabian AJ, Rooney S, Alt FW, Mulligan RC. Complete correction of murine Artemis immunodeficiency by lentiviral vector-mediated gene transfer. Proc Natl Acad Sci U S A 2006; 103: 16406-11641. (PMID: 17062750)
43. 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: 625-636. (PMID: 11877485)
44. Cantu C 3rd, Benlagha K, Savage PB, Bendelac A, Teyton L. The paradox of immune molecular recognition of alpha-galactosylceramide: low affinity, low specificity for CD1d, high affinity for alpha beta TCRs. J Immunol 2003; 170: 4673-4682. (PMID: 12707346)
45. Brigl M, van den Elzen P, Chen X, Meyers JH, Wu D, Wong CH, Reddington F, Illarianov PA, Besra GS, Brenner MB, Gumperz JE. Conserved and heterogeneous lipid antigen specificities of CD1drestricted NKT cell receptors. J Immunol 2006; 176: 3625-3634. (PMID: 16517731)
46. Yu KO, Im JS, Molano A, Dutronc Y, Illarionov PA, Forestier C, Fujiwara N, Arias I, Miyake S, Yamamura T, Chang YT, Besra GS, Porcelli SA. Modulation of CD1d-restricted NKT cell responses by using N-acyl variants of alpha-galactosylceramides. Proc Natl Acad Sci U S A 2005; 102: 3383-3388. (PMID: 15722411)
47. Veerapen N, Leadbetter EA, Brenner MB, Cox LR, Besra GS. Synthesis of a novel alpha-galactosyl ceramide haptenated-lipid antigen, a useful tool in demonstrating the involvement of iNKT cells in the production of antilipid antibodies. Bioconjug Chem 2010; 21: 741-747. (PMID: 20345125)
48. Gumperz JE. Generation of HLA class I transfected target cell lines. Methods Mol Biol 2000; 121: 49-60. (PMID: 10818716)
49. Chen X, Wang X, Keaton JM, Reddington F, Illarionov PA, Besra GS, Gumperz JE. Distinct endosomal trafficking requirements for presentation of autoantigens and exogenous lipids by human CD1d molecules. J Immunol 2007; 178: 6181-6190. (PMID: 17475845)