Lymphocyte activation gene 3: A novel therapeutic target in chronic lymphocytic leukemia

Haematologica

Volumn 102, Issue 5, 2017, Pages 874-882

  Shapiro, Mika ^a   Herishanu, Yair ^a,b   Ben Zion katz, ^a,b   Dezorella, Nili ^a,b   Sun, Clare ^c   Kay, Sigi ^a   Polliack, Aaron ^d   Avivi, Irit ^a,b   Wiestner, Adrian ^c   Perry, Chava ^a  

^a TEL AVIV SOURASKY MEDICAL CENTER   (Israel)

^b TEL AVIV UNIVERSITY   (Israel)

^c NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^d HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; CD69 ANTIGEN; CD86 ANTIGEN; FOSTAMATINIB; GILVETMAB; IBRUTINIB; IMMUNE CHECKPOINT RECEPTOR; LYMPHOCYTE ACTIVATION GENE 3; LYMPHOCYTE ANTIGEN RECEPTOR; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN MCL 1; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; BLOCKING ANTIBODY; CD223 ANTIGEN; HLA ANTIGEN CLASS 2; LEUKOCYTE ANTIGEN; PROTEIN BINDING;

APOPTOSIS; ARTICLE; CELL STIMULATION; CELL SURVIVAL; CELL VIABILITY; CHRONIC LYMPHATIC LEUKEMIA; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC ANALYSIS; HUMAN; HUMAN CELL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; TUMOR MICROENVIRONMENT; UPREGULATION; WESTERN BLOTTING; ANTIGEN PRESENTING CELL; DRUG EFFECTS; GENETICS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MOLECULARLY TARGETED THERAPY; PROCEDURES; T LYMPHOCYTE;

ANTIBODIES, BLOCKING; ANTIGEN-PRESENTING CELLS; ANTIGENS, CD; APOPTOSIS; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; LYMPHOCYTE ACTIVATION; MOLECULAR TARGETED THERAPY; PROTEIN BINDING; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 85018991663     PISSN: 03906078     EISSN: 15928721     Source Type: Journal    
DOI: 10.3324/haematol.2016.148965     Document Type: Article

References (31)

1. Caligaris-Cappio F, Hamblin TJ. B-cell chronic lymphocytic leukemia: a bird of a different feather. J Clin Oncol. 1999; 17(1):399-408.
2. Moreno C, Villamor N, Colomer D, et al. Allogeneic stem-cell transplantation may overcome the adverse prognosis of unmutated VH gene in patients with chronic lymphocytic leukemia. J Clin Oncol. 2005 20;23(15):3433-3438.
3. Gladstone DE, Fuchs E. Hematopoietic stem cell transplantation for chronic lymphocytic leukemia. Curr Opin Oncol. 2012; 24(2):176-181.
4. Lanham S, Hamblin T, Oscier D, Ibbotson R, Stevenson F, Packham G. Differential signaling via surface IgM is associated with VH gene mutational status and CD38 expression in chronic lymphocytic leukemia. Blood. 2003; 101(3):1087-1093.
5. Stevenson FK, Krysov S, Davies AJ, Steele AJ, Packham G. B-cell receptor signaling in chronic lymphocytic leukemia. Blood. 2011;118(16):4313-4320.
6. Herishanu Y, Perez-Galan P, Liu D, et al. The lymph node microenvironment promotes B-cell receptor signaling, NF-kappaB activation, and tumor proliferation in chronic lymphocytic leukemia. Blood. 2011;117(2):563-574.
7. Valujskikh A, Li XC. Memory T cells and their exhaustive differentiation in allograft tolerance and rejection. Curr Opin organ Transplant. 2012;17(1):15-19.
8. Matsuzaki J, Gnjatic S, Mhawech-Fauceglia P, et al. Tumor-infiltrating NY-ESO-1-spe-cific CD8+ T cells are negatively regulated by LAG-3 and PD-1 in human ovarian cancer. Proc Natl Acad Sci USA. 2010; 107(17):7875-7880.
9. Fourcade J, Sun Z, Benallaoua M, et al. Upregulation of Tim-3 and PD-1 expression is associated with tumor antigen-specific CD8+ T cell dysfunction in melanoma patients. J Exp Med. 2010;207(10):2175-2186.
10. Norde WJ, Hobo W, van der Voort R, Dolstra H. Coinhibitory molecules in hematologic malignancies: targets for therapeutic intervention. Blood. 2012; 120(4): 728-736.
11. Woo SR, Turnis ME, Goldberg MV, et al. Immune inhibitory molecules LAG-3 and PD-1 synergistically regulate T-cell function to promote tumoral immune escape. Cancer Res. 2012;72(4):917-927.
12. Grosso JF, Kelleher CC, Harris TJ, et al. LAG-3 regulates CD8+ T cell accumulation and effector function in murine self- and tumor-tolerance systems. J Clin Invest. 2007;117(11):3383-3392.
13. Triebel F. LAG-3: a regulator of T-cell and DC responses and its use in therapeutic vaccination. Trends Immunol. 2003; 24(12):619-622.
14. Romano E, Michielin O, Voelter V, et al. MART-1 peptide vaccination plus IMP321 (LAG-3Ig fusion protein) in patients receiving autologous PBMCs after lymphodeple-tion: results of a Phase I trial. J Transl Med. 2014;12:97.
15. Hemon P, Jean-Louis F, Ramgolam K, et al. MHC class II engagement by its ligand LAG-3 (CD223) contributes to melanoma resistance to apoptosis. J Immunol. 2011; 186(9):5173-5183.
16. Kotaskova J, Tichy B, Trbusek M, et al. High expression of lymphocyte-activation gene 3 (LAG3) in chronic lymphocytic leukemia cells is associated with unmutated immunoglobulin variable heavy chain region (IGHV) gene and reduced treatment-free survival. J Mol Diagn. 2010;12(3):328-334.
17. Hallek M, Cheson BD, Catovsky D, et al. Guidelines for the diagnosis and treatment of chronic lymphocytic leukemia: a report from the International Workshop on Chronic Lymphocytic Leukemia updating the National Cancer Institute-Working Group 1996 guidelines. Blood. 2008; 111(12):5446-5456.
18. Wiestner A, Rosenwald A, Barry TS, et al. ZAP-70 expression identifies a chronic lymphocytic leukemia subtype with unmutated immunoglobulin genes, inferior clinical outcome, and distinct gene expression profile. Blood. 2003;101(12):4944-4951.
19. Guy K, Meehan RR, Dewar AE, Larhammar D. Expression of MHC class II antigens in human B-cell leukaemia, and increased levels of class II antigens and DR-specific mRNA after stimulation with 12-O-tetradecanoyl phorbol-13-acetate. Immunology. 1986;57(2):181-188.
20. Baixeras E, Huard B, Miossec C, et al. Characterization of the lymphocyte activation gene 3-encoded protein. A new ligand for human leukocyte antigen class II antigens. J Exp Med. 1992; 176(2):327-337.
21. Huard B, Mastrangeli R, Prigent P, et al. Characterization of the major histocompatibility complex class II binding site on LAG-3 protein. Proc Natl Acad Sci USA. 1997; 94(11):5744-5749.
22. Ranheim EA, Kipps TJ. Activated T cells induce expression of B7/BB1 on normal or leukemic B cells through a CD40-dependent signal. J Exp Med. 1993; 177(4):925-935.
23. Scholl PR, Geha RS. MHC class-II signaling in B-cell activation. Immunol Today. 1994; 15(9):418-422.
24. Triebel F, Hacene K, Pichon MF. A soluble lymphocyte activation gene-3 (sLAG-3) protein as a prognostic factor in human breast cancer expressing estrogen or progesterone receptors. Cancer Lett. 2006; 235(1):147-153.
25. Nashar TO, Hirst TR, Williams NA. Modulation of B-cell activation by the B subunit of Escherichia coli enterotoxin: receptor interaction up-regulates MHC class II, B7, CD40, CD25 and ICAM-1. Immunology. 1997;91(4):572-578.
26. Gassner FJ, Zaborsky N, Catakovic K, et al. Chronic lymphocytic leukaemia induces an exhausted T cell phenotype in the TCL1 transgenic mouse model. Br J Haematol. 2015;170(4):515-522.
27. Demeure CE, Wolfers J, Martin-Garcia N, Gaulard P, Triebel F. T Lymphocytes infiltrating various tumour types express the MHC class II ligand lymphocyte activation gene-3 (LAG-3): role of LAG-3/MHC class II interactions in cell-cell contacts. Eur J Cancer. 2001;37(13):1709-1718.
28. Turnis ME, Korman AJ, Drake CG, Vignali DA. Combinatorial Immunotherapy: PD-1 may not be LAG-ing behind any more. Oncoimmunology. 2012; 1(7):1172-1174.
29. Grosso JF, Goldberg MV, Getnet D, et al. Functionally distinct LAG-3 and PD-1 subsets on activated and chronically stimulated CD8 T cells. J Immunol. 2009;182(11): 6659-6669.
30. Baitsch L, Legat A, Barba L, et al. Extended co-expression of inhibitory receptors by human CD8 T-cells depending on differentiation, antigen-specificity and anatomical localization. PLoS One. 2012;7(2):e30852.
31. Wei Ding, Jennifer Le-Rademacher, Timothy G. Call, et al. PD-1 blockade with pembrolizumab in relapsed CLL including Richter’s transformation: an updated report from a phase 2 trial (MC1485). Blood. 2016; 128(22):4392.