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US 2008/0279894 A1 Savage Et Al US 200802798.94A1 (19) United States (12) Patent Application Publication (10) Pub. No.: US 2008/0279894 A1 Savage et al. (43) Pub. Date: Nov. 13, 2008 (54) BACTERIAL GLYCOLIPIDACTIVATION OF (86). PCT No.: PCT/US2O06/OO2781 CD1D-RESTRICTED NKT CELLS S371 (c)(1), (75) Inventors: Paul B. Savage, Mapleton, UT (2), (4) Date: Apr. 11, 2008 (US); Albert Bendelac, Chicago, IL Related U.S. Application Data (US); Luc Teyton, Del Mar, CA (60) Provisional application No. 60/648,153, filed on Jan. (US) 28, 2005. Publication Classification Correspondence Address: MICHAEL BEST & FRIEDRCH LLP (51) Int. Cl. ONE SOUTH PINCKNEY STREET, PO BOX A6139/02 (2006.01) 1806 CI2N 5/06 (2006.01) MADISON, WI 53701 (US) A6139/00 (2006.01) (52) U.S. Cl. .................... 424/234.1: 435/375; 424/184.1 (73) Assignees: BRIGHAMYOUNG (57) ABSTRACT UNIVERSITY, Provo, UT (US); Disclosed are methods for activating an NKT cell, methods of THE UNIVERSITY OF stimulating an immune response in a subject, methods of CHICAGO, Chicago, IL (US); improving vaccine efficacy, and methods of treating an infec THE SCRIPPS RESEARCH tion. Also disclosed are methods of promoting tumor rejec INSTITUTE, La Jolla, CA (US) tion, treating cancer, modulating autoimmunity and inhibit ing allergen-induced hypersensitivity in Subjects. The methods include contacting an NKT cell with a bacterial (21) Appl. No.: 11/814,103 glycolipid complexed with a CD1 molecule to activate the NKT cell. The bacterial glycolipid may be derived from a (22) PCT Filed: Jan. 26, 2006 member of the Class Alphaproteobacteria. A Mouse DC + NKT Human DC + NKT B Spleen 2.03 6 5.34 8 NS 1. CD1 al igG aGalCer S. 5 co-i- DoCD1d d 6 O Sphingomonas s O Salmonella S. 2 4 - 1 N1 2. 2 1 S 2 O O O c O 2 4 6 wes x^e S was ve S days of stimulation s o es &s 9 3° 9 o & &o c g S e s Salmonella OGalCer Patent Application Publication Nov. 13, 2008 Sheet 2 of 7 US 2008/02798.94 A1 +1,88GÁIN)sOCl --88CIÁINDIsoq OCHLXAN+ US 2008/02798.94 A1 0ULee-pCO Jeuee-pico Patent Application Publication Nov. 13, 2008 Sheet 4 of 7 US 2008/02798.94 A1 to Lo w to em to v 009 0 ensSI) ue.Bued no 06o HOWS OOO'O fSeidoo eluolulug L Patent Application Publication Nov. 13, 2008 Sheet 5 of 7 US 2008/02798.94 A1 Patent Application Publication Nov. 13, 2008 Sheet 6 of 7 US 2008/02798.94 A1 ('\u00)G'91-' Patent Application Publication Nov. 13, 2008 Sheet 7 of 7 US 2008/02798.94 A1 HO US 2008/02798.94 A1 Nov. 13, 2008 BACTERAL, GLYCOLPIDACTIVATION OF 0009. In yet another aspect, the invention provides a CD1D-RESTRICTED NKT CELLS method of stimulating an immune response in a Subject com prising administering to the Subject an effective amount of CROSS-REFERENCE TO RELATED NKT cells activated by contacting a T-cell receptor of the APPLICATIONS NKT cells with a bacterial glycolipid complexed with a CD1d 0001. This application claims the benefit of U.S. provi molecule. sional application 60/648,153 filed on Jan. 28, 2005. The 0010 Infurther aspects, the invention provides methods of provisional application is incorporated herein by reference. improving vaccine efficacy, promoting tumor rejection, modulating autoimmunity, inhibiting allergen-induced STATEMENT REGARDING FEDERALLY hypersensitivity, and treating an infection in a Subject by SPONSORED RESEARCH administration of an effective amount of a bacterial glycolipid derived from a member of the Class Alphaproteobacteria. 0002 This invention was made with United States govern ment support awarded by the National Institutes of Health, National Institute of Allergy and Infectious Disease (Grant BRIEF DESCRIPTION OF THE DRAWINGS No. A 1053725). The United States government has certain (0011 FIG. 1A depicts CD1d-dependent IFN-y secretion rights in this invention. by mouse and human NKT cells stimulated with heat-killed bacteria or C.Gal-Cer. Mean and standard deviation of 3 INTRODUCTION experiments. 0003. The CD1d molecule is a member of the CD1 family (0012 FIG. 1B depicts NKT cell proliferation in a spleen of 32 microglobulin-associated molecules. In contrast to cell culture stimulated with heat-killed bacteria or OGal-Cer. class I and II major histocompatibility complex (MHC) mol Data points show means and standard deviations from 3 sepa ecules that present protein antigens to CD8+ and CD4+ T rate experiments. cells, respectively, CD1 molecules have evolved to capture (0013 FIG. 1C depicts NKT cell proliferation in response and process both foreign and selflipid antigens for display to to bacterial stimuli or C.Gal-Cer. Upper row, CD1d-C.Gal-Cerf T cells. CD1a, -b, and -c molecules have been shown to B220 staining of spleen cells with NKT cell gate and percent present foreign microbial antigens to human TCRO.BT cells. age as indicated. Lower row, CFSE dilution profile of 5x10 In contrast, CD1d-restricted T cells, or NKT cells, are a gated NKT cells. population of innate-like memory/effector cells expressing (0014 FIG. 2A depicts IFN-Y released by whole spleen both NK receptors and a conserved, semi-invariant TCR cells cultured with heat killed Salmonella typhimurium, Sph (VC.14-JC.18/VB8 in mice and Vol.24-Jo. 18/VB11 inhumans). ingomonas capsulata, and Ehrlichia muris for 48 hours. Left Like NK cells, NKT cells constitutively express mRNA but panel, data shown as percentage of wild type control. Right not protein for IFN-y, evidencing their poised effector stage. panel, data shown as mean and standard deviation of two to NKT cells have been implicated in suppression of autoimmu three separate experiments. nity and graft rejection, promotion of resistance to pathogens, (0015 FIG. 2B depicts the blockade of human NKT cell and promotion of tumor immunity. responses to DC plus antigen by lectin IB4. Similar data 0004 While NKT cells are known to respond to C-Galac obtained in two experiments. tosylCeramide (C,Gal-Cer), a Surrogate ligand derived from a marine sponge, lack of knowledge of their natural antigens (0016 FIG. 2C depicts stimulation of mouse NKT cell has previously precluded understanding of the mechanisms responses to bacterial antigen presented by Hexb" or of their peripheral activation and recruitment, as well as their Hexb DC. Similar data obtained in two experiments. thymic development. 0017 FIG. 3A depicts structures of synthetic Sphingomo 0005. The inventors have previously identified a natural nas cell wall antigens. PBS 50 is a control f-glucuronosylce endogenous antigen, isoglobotrihexosylceramide (iGb3), ramide. which is presented to NKT cells by LPS-activated dendritic (0018 FIG. 3B depicts the IFN-Y response of a human cells. This work Suggests that iGb3 is a primary ligand for Vo24-Jo.18 NKT line and fresh purified mouse NKT cells NKT cells. However, the partial diversity of the B-chain of the stimulated by synthetic lipid antigens and DC. Data shown TCR suggests that multiple natural antigen specificity may be are the mean and standard deviation of two separate experi possible. mentS. 0019 FIG. 3C depicts CD1d tetramer staining of human SUMMARY NKT (upper row) and mouse spleen cells (lower row) with 0006. Described herein is the inventors surprising discov synthetic glycolipids. NKT cell gate and percentages are as ery that glycolipids derived from members of the Class indicated. Alphaproteobacteria also act as natural ligands of CD1d mol (0020 FIG. 4A depicts in vivo activation of NKT cells 24 ecules to activate NKT cells. hours after intravenous infection with Sphingomonas 0007. In one aspect, the invention provides a method of (1x107), Ehrlichia (1x10) and Salmonella (1x10). Similar activating an NKT cell comprising contacting the NKT cell results were obtained in 2 experiments. with a bacterial glycolipid complexed with a CD1d molecule. (0021 FIG. 4B depicts IFN-y production by NKT cells in In some embodiments, the bacterial glycolipid may be response to Salmonella. The difference between Hexb" and derived from a member of the class Alphaproteobacteria. Hexb was significant for Salmonella (p=0.001). Three 0008. In another aspect, the invention provides a method mice per group were analyzed and similar results obtained in of inducing cytokine expression by an NKT cell comprising 2 independent experiments. contacting a T-cell receptor of the NKT cell with a bacterial 0022 FIG. 4C depicts bacterial burden in the lungs of glycolipid complexed with a CD1d molecule. CD1d" and CD1d mice after infection with the indicated US 2008/02798.94 A1 Nov. 13, 2008 CFU of Sphingomonas (each bar represents 4 to 5 mice). Fold NKT cells comprises contacting an NKT cell with a bacterial increase and p values are indicated. Two representative glycolipid derived from a member of the Class Alphaproteo experiments are shown. bacteria. A T cell receptor of an NKT cell,” as the term is 0023 FIG. 4D depicts acute lethality in mice after inocu used herein, refers to the conserved, semi-invariant TCR of lation of a high dose of 5x10 Sphingomonas capsulata. NKT cells comprising, e.g., VC.14-JC18/VB8 in mice and Separate experiments comparing CD1d" and CD1d VC.24-JC.18/VB11 in humans. “Contacting, as used herein, (n=24 each, p<0.0001) and Jo. 18" and Jo.18 (n=12 each, refers to the in vitro addition of bacterial glycolipid in solu p=0.034) are shown. tion to immobilized, soluble, or insoluble CD1d molecules, or 0024 FIG. 4E depicts acute serum release of IFN-Y and to the in vivo administration of bacterial glycolipid to a sub IL-12p40 in heterozygous and homozygous CD1d and Jo. 18 ject having antigen presenting cells which express cell Sur mutant mice and littermate controls after infection with face CD1d molecules.
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