Beta-glucosylceramide administration (i.p.) activates natural killer T cells in vivo and prevents tumor metastasis in mice

Lipids

Volumn 47, Issue 6, 2012, Pages 581-591

  Inafuku, Masashi ^a   Li, Changchun ^a   Kanda, Yasuhiro ^b   Kawamura, Toshihiko ^b   Takeda, Kazuyoshi ^c   Oku, Hirosuke ^a   Watanabe, Hisami ^a  

^a UNIVERSITY OF THE RYUKYUS   (Japan)

^b NIIGATA UNIVERSITY   (Japan)

^c JUNTENDO UNIVERSITY   (Japan)

Author keywords

Glucosylceramide; Ja18 and CD1d; Natural killer T cells; NKT cell based immunotherapies; Tumor metastasis

Indexed keywords

1 O (ALPHA GALACTOPYRANOSYL) 2 HEXACOSANOYLAMINO 1,3,4 OCTADECANETRIOL; ANTIMETASTATIC AGENT; ANTINEOPLASTIC AGENT; BETA GALACTOSYLCERAMIDE; BETA GLUCOSYLCERAMIDE; GAMMA INTERFERON; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG CYTOTOXICITY; DRUG EFFECT; DRUG EFFICACY; DRUG STRUCTURE; IN VIVO STUDY; LIVER METASTASIS; METASTASIS INHIBITION; MOUSE; NATURAL KILLER T CELL; NONHUMAN; PROTEIN LOCALIZATION; T LYMPHOCYTE ACTIVATION; TUMOR IMMUNITY;

ALANINE TRANSAMINASE; ANIMALS; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; ANTINEOPLASTIC AGENTS; ASPARTATE AMINOTRANSFERASES; CELL LINE, TUMOR; CYTOTOXICITY, IMMUNOLOGIC; GENE EXPRESSION; GLUCOSYLCERAMIDES; IMMUNOLOGIC FACTORS; IMMUNOTHERAPY; INJECTIONS, INTRAPERITONEAL; INTERFERON-GAMMA; LECTINS, C-TYPE; LIVER; LIVER NEOPLASMS; LYMPHOMA; MICE; MICE, INBRED C57BL; NATURAL KILLER T-CELLS; TUMOR BURDEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

MUS;

EID: 84863474287     PISSN: 00244201     EISSN: 15589307     Source Type: Journal    
DOI: 10.1007/s11745-012-3666-1     Document Type: Article

References (38)

1. Futerman AH, Hannun YA (2004) The complex life of simple sphingolipids. EMBO Rep 5(8):777-782. doi:10.1038/sj.embor. 7400208 (Pubitemid 39199166)
2. Ogretmen B, Hannun YA (2004) Biologically active sphingolipids in cancer pathogenesis and treatment. Nat Rev Cancer 4(8):604-616. doi:10.1038/nrc1411 (Pubitemid 39025055)
3. Oku H, Li C, Shimatani M, Iwasaki H, Toda T, Okabe T, Watanabe H (2009) Tumor specific cytotoxicity of beta-glucosylceramide: structure-cytotoxicity relationship and anti-tumor activity in vivo. Cancer Chemother Pharmacol 64(3):485-496. doi:10.1007/s00280-008-0896-2
4. Cerundolo V, Silk JD, Masri SH, Salio M (2009) Harnessing invariant NKT cells in vaccination strategies. Nat Rev Immunol 9(1):28-38. doi:10.1038/nri2451
5. Kobayashi E, Motoki K, Uchida T, Fukushima H, Koezuka Y (1995) KRN7000, a novel immunomodulator, and its antitumor activities. Oncol Res 7(10-11):529-534 (Pubitemid 26077987)
6. Molling JW, Moreno M, van der Vliet HJ, van den Eertwegh AJ, Scheper RJ, von Blomberg BM, Bontkes HJ (2008) Invariant natural killer T cells and immunotherapy of cancer. Clin Immunol 129(2):182-194. doi:10.1016/j.clim.2008. 07.025
7. Kronenberg M, Gapin L (2002) The unconventional lifestyle of NKT cells. Nat Rev Immunol 2(8):557-568. doi:10.1038/nri854 (Pubitemid 37328731)
8. Bendelac A, Rivera MN, Park SH, Roark JH (1997) Mouse CD1-specific NK1 T cells: development, specificity, and function. Annu Rev Immunol 15:535-562. doi:10.1146/annurev. immunol. 15.1.535 (Pubitemid 27169416)
9. Bendelac A, Savage PB, Teyton L (2007) The biology of NKT cells. Annu Rev Immunol 25:297-336. doi:10.1146/annurev. immunol.25.022106.141711 (Pubitemid 46697911)
10. Jahng A, Maricic I, Aguilera C, Cardell S, Halder RC, Kumar V (2004) Prevention of autoimmunity by targeting a distinct, noninvariant CD1d-reactive T cell population reactive to sulfatide. J Exp Med 199(7):947-957. doi:10.1084/jem.20031389 (Pubitemid 38481086)
11. Arrenberg P, Halder R, Kumar V (2009) Cross-regulation between distinct natural killer T cell subsets influences immune response to self and foreign antigens. J Cell Physiol 218(2):246-250. doi:10.1002/jcp. 21597
12. Kawano T, Cui J, Koezuka Y, Toura I, Kaneko Y, Motoki K, Ueno H, Nakagawa R, Sato H, Kondo E, Koseki H, Taniguchi M (1997) CD1d-restricted and TCR-mediated activation of valpha14 NKT cells by glycosylceramides. Science 278(5343):1626-1629 (Pubitemid 27516282)
13. Taniguchi M, Harada M, Kojo S, Nakayama T, Wakao H (2003) The regulatory role of Valpha14 NKT cells in innate and acquired immune response. Annu Rev Immunol 21:483-513. doi: 10.1146/annurev. immunol.21.120601.141057 (Pubitemid 37174539)
14. Wilson MT, Johansson C, Olivares-Villagomez D, Singh AK, Stanic AK, Wang CR, Joyce S, Wick MJ, Van Kaer L (2003) The response of natural killer T cells to glycolipid antigens is characterized by surface receptor down-modulation and expansion. Proc Natl Acad Sci USA 100(19):10913-10918. doi:10.1073/pnas. 1833166100 (Pubitemid 37140127)
15. Harada M, Seino K, Wakao H, Sakata S, Ishizuka Y, Ito T, Kojo S, Nakayama T, Taniguchi M (2004) Down-regulation of the invariant Valpha14 antigen receptor in NKT cells upon activation. Int Immunol 16(2):241-247 (Pubitemid 38195654)
16. Schmieg J, Yang G, Franck RW, Tsuji M (2003) Superior protection against malaria and melanoma metastases by a C-glycoside analogue of the natural killer T cell ligand alpha-Galactosylceramide. J Exp Med 198(11):1631-1641. doi: 10.1084/jem.20031192 (Pubitemid 37494156)
17. Nakagawa R, Serizawa I, Motoki K, Sato M, Ueno H, Iijima R, Nakamura H, Shimosaka A, Koezuka Y (2000) Antitumor activity of alpha-galactosylceramide, KRN7000, in mice with the melanoma B16 hepatic metastasis and immunohistological study of tumor infiltrating cells. Oncol Res 12(2):51-58
18. Nakagawa R, Nagafune I, Tazunoki Y, Ehara H, Tomura H, Iijima R, Motoki K, Kamishohara M, Seki S (2001) Mechanisms of the antimetastatic effect in the liver and of the hepatocyte injury induced by alpha-galactosylceramide in mice. J Immunol 166(11):6578-6584 (Pubitemid 32467197)
19. Osada T, Nagawa H, Shibata Y (2004) Tumor-infiltrating effector cells of alpha-galactosylceramide-induced antitumor immunity in metastatic liver tumor. J Immune Based Ther Vaccines 2(1):7. doi:10.1186/1476-8518-2-7 (Pubitemid 39112054)
20. Fujii H, Seki S, Kobayashi S, Kitada T, Kawakita N, Adachi K, Tsutsui H, Nakanishi K, Fujiwara H, Ikarashi Y, Taniguchi M, Kronenberg M, Ikemoto M, Nakajima Y, Arakawa T, Kaneda K (2005) A murine model of NKT cell-mediated liver injury induced by alpha-galactosylceramide/d-galactosamine. Virchows Arch 446(6):663-673. doi:10.1007/s00428-005-1265-8 (Pubitemid 40922273)
21. Biburger M, Tiegs G (2005) Alpha-galactosylceramide-induced liver injury in mice is mediated by TNF-alpha but independent of Kupffer cells. J Immunol 175(3):1540-1550 (pii: 175/3/1540) (Pubitemid 41023055)
22. Hannun YA, Luberto C, Argraves KM (2001) Enzymes of sphingolipid metabolism: from modular to integrative signaling. Biochemistry 40(16):4893-4903 (pii: bi002836k) (Pubitemid 32332534)
23. Brutkiewicz RR (2006) CD1d ligands: the good, the bad, and the ugly. J Immunol 177(2):769-775 (pii: 177/2/769) (Pubitemid 44036575)
24. Zajonc DM, Cantu C 3rd, Mattner J, Zhou D, Savage PB, Bendelac A, Wilson IA, Teyton L (2005) Structure and function of a potent agonist for the semi-invariant natural killer T cell receptor. Nat Immunol 6(8):810-818. doi:10.1038/ni1224 (Pubitemid 43090467)
25. Margalit M, Ghazala SA, Alper R, Elinav E, Klein A, Doviner V, Sherman Y, Thalenfeld B, Engelhardt D, Rabbani E, Ilan Y (2005) Glucocerebroside treatment ameliorates ConA hepatitis by inhibition of NKT lymphocytes. Am J Physiol Gastrointest Liver Physiol 289(5):G917-G925. doi:10.1152/ajpgi.00105.2005 (Pubitemid 41532585)
26. Safadi R, Zigmond E, Pappo O, Shalev Z, Ilan Y (2007) Amelioration of hepatic fibrosis via beta-glucosylceramide-mediated immune modulation is associated with altered CD8 and NKT lymphocyte distribution. Int Immunol 19(8):1021-1029. doi: 10.1093/intimm/dxm069 (Pubitemid 47386927)
27. Zigmond E, Preston S, Pappo O, Lalazar G, Margalit M, Shalev Z, Zolotarov L, Friedman D, Alper R, Ilan Y (2007) Betaglucosylceramide: a novel method for enhancement of natural killer T lymphoycte plasticity in murine models of immunemediated disorders. Gut 56(1):82-89. doi:10.1136/gut.2006. 095497 (Pubitemid 46044892)
28. Horani A, Shoseyov D, Doron S, Mruwat R, Amer J, Kerem E, Safadi R (2011) Immune modulation of ovalbumin-induced lung injury in mice using beta-glucosylceramide and a potential role of the liver. Immunobiology 216(5):548-557. doi:10.1016/j.imbio. 2010.10.002
29. Zigmond E, Zangen SW, Pappo O, Sklair-Levy M, Lalazar G, Zolotaryova L, Raz I, Ilan Y (2009) Beta-glycosphingolipids improve glucose intolerance and hepatic steatosis of the Cohen diabetic rat. Am J Physiol Endocrinol Metab 296(1):E72-E78. doi:10.1152/ajpendo.90634.2008
30. Lalazar G, Ben Ya'acov A, Livovsky DM, El Haj M, Pappo O, Preston S, Zolotarov L, Ilan Y (2009) Beta-glycoglycosphingolipidinduced alterations of the STAT signaling pathways are dependent on CD1d and the lipid raft protein flotillin-2. Am J Pathol 174(4):1390-1399. doi:10.2353/ajpath.2009.080841
31. Zhou D, Mattner J, Cantu C 3rd, Schrantz N, Yin N, Gao Y, Sagiv Y, Hudspeth K, Wu YP, Yamashita T, Teneberg S, Wang D, Proia RL, Levery SB, Savage PB, Teyton L, Bendelac A (2004) Lysosomal glycosphingolipid recognition by NKT cells. Science 306(5702):1786-1789. doi:10.1126/science.1103440 (Pubitemid 39601398)
32. Xia C, Yao Q, Schumann J, Rossy E, Chen W, Zhu L, Zhang W, De Libero G, Wang PG (2006) Synthesis and biological evaluation of alpha-galactosylceramide (KRN7000) and isoglobotrihexosylceramide (iGb3). Bioorg Med Chem Lett 16(8):2195-2199. doi:10.1016/j.bmcl.2006.01.040 (Pubitemid 43351077)
33. Porubsky S, Speak AO, Luckow B, Cerundolo V, Platt FM, Grone HJ (2007) Normal development and function of invariant natural killer T cells in mice with isoglobotrihexosylceramide (iGb3) deficiency. Proc Natl Acad Sci USA 104(14):5977-5982. doi:10.1073/pnas.0611139104 (Pubitemid 47175644)
34. Stanic AK, De Silva AD, Park JJ, Sriram V, Ichikawa S, Hirabyashi Y, Hayakawa K, Van Kaer L, Brutkiewicz RR, Joyce S (2003) Defective presentation of the CD1d1-restricted natural Va14Ja18 NKT lymphocyte antigen caused by beta-D-glucosylceramide synthase deficiency. Proc Natl Acad Sci USA 100(4):1849-1854. doi:10.1073/pnas.0430327100 (Pubitemid 36254537)
35. Zigmond E, Shalev Z, Pappo O, Alper R, Zolotarov L, Ilan Y (2008) NKT lymphocyte polarization determined by microenvironment signaling: a role for CD8? lymphocytes and betaglycosphingolipids. J Autoimmun 31(2):188-195. doi:10.1016/j.jaut.2008.07.003
36. Oku H, Wongtangtintharn S, Iwasaki H, Inafuku M, Shimatani M, Toda T (2007) Tumor specific cytotoxicity of glucosylceramide. Cancer Chemother Pharmacol 60(6):767-775. doi: 10.1007/s00280-007-0422-y (Pubitemid 47389382)
37. Miyamoto K, Miyake S, Yamamura T (2001) A synthetic glycolipid prevents autoimmune encephalomyelitis by inducing TH2 bias of natural killer T cells. Nature 413(6855):531-534. doi: 10.1038/35097097 (Pubitemid 32938752)
38. Kobayashi E, Motoki K, Yamaguchi Y, Uchida T, Fukushima H, Koezuka Y (1996) Enhancing effects of alpha-, beta-monoglycosylceramides on natural killer cell activity. Bioorg Med Chem 4(4):615-619. (pii: 0968089696000491)