Repression of GSK3 restores NK cell cytotoxicity in AML patients

Nature Communications

Volumn 7, Issue , 2016, Pages

  Parameswaran, Reshmi ^a   Ramakrishnan, Parameswaran ^a   Moreton, Stephen A ^a,b   Xia, Zhiqiang ^b   Hou, Yongchun ^a   Lee, Dean A ^c   Gupta, Kalpana ^a   Delima, Marcos ^d   Beck, Rose C ^d   Wald, David N ^a,d  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Invenio Therapeutics   (United States)

^c UNIVERSITY OF TEXAS   (United States)

^d UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; TUMOR NECROSIS FACTOR ALPHA; 3-(3-CHLORO-4-HYDROXYPHENYLAMINO)-4-(4-NITROPHENYL)-1H-PYRROLE-2,5-DIONE; 3-(9-FLUORO-2-(PIPERIDIN-1-YLCARBONYL)-1,2,3,4-TETRAHYDRO(1,4)DIAZEPINO(6,7,1-HI)INDOL-7-YL)-4-IMIDAZO(1,2-A)PYRIDIN-3-YL-1H-PYRROLE-2,5-DIONE; 4 BENZYL 2 METHYL 1,2,4 THIAZOLIDINE 3,5 DIONE; AMINOPHENOL DERIVATIVE; FUSED HETEROCYCLIC RINGS; GLYCOGEN SYNTHASE KINASE 3BETA; GSK3B PROTEIN, HUMAN; GSK3B PROTEIN, MOUSE; MALEIMIDE DERIVATIVE; THIADIAZOLE DERIVATIVE; TUMOR NECROSIS FACTOR;

CELLS AND CELL COMPONENTS; CYTOGENETICS; EXPERIMENTAL STUDY; GENE EXPRESSION; GENOTOXICITY; INHIBITION; RODENT;

ACUTE MYELOBLASTIC LEUKEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER PATIENT; CONJUGATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXICITY; ENZYME REPRESSION; HUMAN; HUMAN CELL; LEUKEMIA CELL; MOUSE; NATURAL KILLER CELL; NONHUMAN; PROTEIN EXPRESSION; UPREGULATION; ACUTE MYELOID LEUKEMIA; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMISTRY; IMMUNOLOGY; IMMUNOTHERAPY; METABOLISM; TUMOR MICROENVIRONMENT;

AMINOPHENOLS; ANIMALS; CELLULAR MICROENVIRONMENT; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; HETEROCYCLIC COMPOUNDS, 3-RING; IMMUNOTHERAPY; INTERCELLULAR ADHESION MOLECULE-1; KILLER CELLS, NATURAL; LEUKEMIA, MYELOID, ACUTE; MALEIMIDES; MICE; NF-KAPPA B; THIADIAZOLES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84962734942     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms11154     Document Type: Article

References (56)

1. Cheng, M., Chen, Y., Xiao, W., Sun, R. & Tian, Z. NK cell-based immunotherapy for malignant diseases. Cell. Mol. Immunol. 10, 230-252 (2013).
2. Miller, J. S. et al. Successful adoptive transfer and in vivo expansion of human haploidentical NK cells in patients with cancer. Blood 105, 3051-3057 (2005).
3. Ruggeri, L. et al. Natural killer cell alloreactivity for leukemia therapy. J. Immunother. 28, 175-182 (2005).
4. Bachanova, V. et al. Clearance of acute myeloid leukemia by haploidentical natural killer cells is improved using IL-2 diphtheria toxin fusion protein. Blood 123, 3855-3863 (2014).
5. Pegram, H. J., Andrews, D. M., Smyth, M. J., Darcy, P. K. & Kershaw, M. H. Activating and inhibitory receptors of natural killer cells. Immunol. Cell Biol. 89, 216-224 (2011).
6. Fauriat, C., Long, E. O., Ljunggren, H. G. & Bryceson, Y. T. Regulation of human NK-cell cytokine and chemokine production by target cell recognition. Blood 115, 2167-2176 (2010).
7. Mace, E. M. et al. Cell biological steps and checkpoints in accessing NK cell cytotoxicity. Immunol. Cell Biol. 92, 245-255 (2014).
8. Wang, R., Jaw, J. J., Stutzman, N. C., Zou, Z. & Sun, P. D. Natural killer cell-produced IFN-gamma and TNF-alpha induce target cell cytolysis through up-regulation of ICAM-1. J. Leukoc. Biol. 91, 299-309 (2012).
9. Lichtenegger, F. S. et al. Impaired NK cells and increased T regulatory cell numbers during cytotoxic maintenance therapy in AML. Leuk. Res. 38, 964-969 (2014).
10. Fauriat, C. et al. Deficient expression of NCR in NK cells from acute myeloid leukemia: Evolution during leukemia treatment and impact of leukemia cells in NCRdull phenotype induction. Blood 109, 323-330 (2007).
11. Costello, R. T. et al. Defective expression and function of natural killer cell-triggering receptors in patients with acute myeloid leukemia. Blood 99, 3661-3667 (2002).
12. Khaznadar, Z. et al. Acute myeloid leukemia impairs natural killer cells through the formation of a deficient cytotoxic immunological synapse. Eur. J. Immunol. 44, 3068-3080 (2014).
13. Doble, B. W. & Woodgett, J. R. GSK-3: tricks of the trade for a multi-tasking kinase. J. Cell Sci. 116, 1175-1186 (2003).
14. Gupta, K. et al. GSK3 is a regulator of RAR-mediated differentiation. Leukemia 26, 1277-1285 (2012).
15. Wang, Z. et al. Glycogen synthase kinase 3 in MLL leukemia maintenance and targeted therapy. Nature 455, 1205-1209 (2008).
16. Beurel, E., Michalek, S. M. & Jope, R. S. Innate and adaptive immune responses regulated by glycogen synthase kinase-3 (GSK3). Trends Immunol. 31, 24-31 (2010).
17. Aoukaty, A. & Tan, R. Role for glycogen synthase kinase-3 in NK cell cytotoxicity and X-linked lymphoproliferative disease. J. Immunol. 174, 4551-4558 (2005).
18. Ogbomo, H. et al. The anti-tumoral drug enzastaurin inhibits natural killer cell cytotoxicity via activation of glycogen synthase kinase-3b. Biochem. Pharmacol. 81, 251-258 (2011).
19. Luo, J. Glycogen synthase kinase 3beta (GSK3beta) in tumorigenesis and cancer chemotherapy. Cancer Lett. 273, 194-200 (2009).
20. Liu, Z. C. et al. AKT/GSK-3beta regulates stability and transcription of snail which is crucial for bFGF-induced epithelial-mesenchymal transition of prostate cancer cells. Biochim. Biophys. Acta 1840, 3096-3105 (2014).
21. Naito, S. et al. Glycogen synthase kinase-3beta: a prognostic marker and a potential therapeutic target in human bladder cancer. Clin. Cancer Res. 16, 5124-5132 (2010).
22. Ougolkov, A. V., Bone, N. D., Fernandez-Zapico, M. E., Kay, N. E. & Billadeau, D. D. Inhibition of glycogen synthase kinase-3 activity leads to epigenetic silencing of nuclear factor kappaB target genes and induction of apoptosis in chronic lymphocytic leukemia B cells. Blood 110, 735-742 (2007).
23. Ougolkov, A. V., Fernandez-Zapico, M. E., Savoy, D. N., Urrutia, R. A. & Billadeau, D. D. Glycogen synthase kinase-3beta participates in nuclear factor kappaB-mediated gene transcription and cell survival in pancreatic cancer cells. Cancer Res. 65, 2076-2081 (2005).
24. Shao, J. et al. COP1 and GSK3beta cooperate to promote c-Jun degradation and inhibit breast cancer cell tumorigenesis. Neoplasia 15, 1075-1085 (2013).
25. Sun, A. et al. Lithium suppresses cell proliferation by interrupting E2F-DNA interaction and subsequently reducing S-phase gene expression in prostate cancer. Prostate 67, 976-988 (2007).
26. Shakoori, A. et al. Deregulated GSK3beta activity in colorectal cancer: its association with tumor cell survival and proliferation. Biochem. Biophys. Res. Commun. 334, 1365-1373 (2005).
27. Klemfuss, H. Rhythms and the pharmacology of lithium. Pharmacol. Ther. 56, 53-78 (1992).
28. Perussia, B. The cytokine profile of resting and activated NK cells. Methods 9, 370-378 (1996).
29. Mehrotra, P. T. et al. Production of IL-10 by human natural killer cells stimulated with IL-2 and/or IL-12. J. Immunol. 160, 2637-2644 (1998).
30. Kuprash, D. V. et al. Similarities and differences between human and murine TNF promoters in their response to lipopolysaccharide. J. Immunol. 162, 4045-4052 (1999).
31. Orange, J. S. Formation and function of the lytic NK-cell immunological synapse. Nat. Rev. Immunol. 8, 713-725 (2008).
32. Roberts, M. S., Woods, A. J., Dale, T. C., Van Der Sluijs, P. & Norman, J. C. Protein kinase B/Akt acts via glycogen synthase kinase 3 to regulate recycling of alpha v beta 3 and alpha 5 beta 1 integrins. Mol. Cell. Biol. 24, 1505-1515 (2004).
33. Waldhauer, I. & Steinle, A. NK cells and cancer immunosurveillance. Oncogene 27, 5932-5943 (2008).
34. Jewett, A. & Tseng, H. C. Tumor induced inactivation of natural killer cell cytotoxic function; implication in growth, expansion and differentiation of cancer stem cells. J. Cancer 2, 443-457 (2011).
35. Barber, D. F., Faure, M. & Long, E. O. LFA-1 contributes an early signal for NK cell cytotoxicity. J. Immunol. 173, 3653-3659 (2004).
36. Bernot, D., Peiretti, F., Canault, M., Juhan-Vague, I. & Nalbone, G. Upregulation of TNF-alpha-induced ICAM-1 surface expression by adenylate cyclase-dependent pathway in human endothelial cells. J. Cell. Physiol. 202, 434-441 (2005).
37. Myers, C. L., Wertheimer, S. J., Schembri-King, J., Parks, T. & Wallace, R. W. Induction of ICAM-1 by TNF-alpha, IL-1 beta, and LPS in human endothelial cells after downregulation of PKC. Am. J. Physiol. 263, C767-C772 (1992).
38. Sun, D. et al. Effects of TNF-alpha on ICAM-1 and LFA-1 expression in peripheral blood mononuclear cells of children with febrile seizures. Zhongguo Dang Dai Er Ke Za Zhi 13, 285-287 (2011).
39. Catharina, C. et al. Tethering of ICAM on target cells is required for LFA-1-dependent NK cell adhesion and granule polarization. J. Immunol. 185, 2918-2926 (2010).
40. Kim, H. et al. TNF-alpha-induced up-regulation of intercellular adhesion molecule-1 is regulated by a Rac-ROS-dependent cascade in human airway epithelial cells. Exp. Mol. Med. 40, 167-175 (2008).
41. Rushworth, S. A. 1 & MacEwan, D. J. HO-1 underlies resistance of AML cells to TNF-induced apoptosis. Blood 111, 3793-3801 (2008).
42. Holmes, T. et al. Glycogen synthase kinase-3beta inhibition preserves hematopoietic stem cell activity and inhibits leukemic cell growth. Stem Cells 26, 1288-1297 (2008).
43. Gotschel, F. et al. Inhibition of GSK3 differentially modulates NF-kappaB, CREB, AP-1 and beta-catenin signaling in hepatocytes, but fails to promote TNF-alpha-induced apoptosis. Exp. Cell Res. 314, 1351-1366 (2008).
44. Graham, J. R., Tullai, J. W. & Cooper, G. M. GSK-3 represses growth factor-inducible genes by inhibiting NF-kappaB in quiescent cells. J. Biol. Chem. 285, 4472-4480 (2010).
45. Nemeth, Z. H. et al. Lithium induces NF-kappa B activation and interleukin-8 production in human intestinal epithelial cells. J. Biol. Chem. 277, 7713-7719 (2002).
46. Arena, A. et al. In vitro effects of lithium chloride on TNF alpha and IL-6 production by monocytes from breast cancer patients. J. Chemother. 9, 219-226 (1997).
47. Ruggeri, L. et al. Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science 295, 2097-2100 (2002).
48. Fionda, C. et al. Inhibition of glycogen synthase kinase-3 increases NKG2D ligand MICA expression and sensitivity to NK cell-mediated cytotoxicity in multiple myeloma cells: role of STAT3. J. Immunol. 190, 6662-6672 (2013).
49. Somanchi, S. S., Senyukov, V. V., Denman, C. J. & Lee, D. A. Expansion, purification, and functional assessment of human peripheral blood NK cells. J. Vis. Exp. 48, 2540 (2011).
50. Patel, S. et al. Tissue-specific role of glycogen synthase kinase 3beta in glucose homeostasis and insulin action. Mol. Cell. Biol. 28, 6314-6328 (2008).
51. Georgiades, P. et al. VavCre transgenic mice: a tool for mutagenesis in hematopoietic and endothelial lineages. Genesis 34, 251-256 (2002).
52. Lin, C. et al. Practical synthesis of N-substituted cyanamides via tiemann rearrangement of amidoximes. Org. Lett. 16, 892-895 (2014).
53. Gobis, K. et al. Synthesis and tuberculostatic activity of novel diverse heterocyclic compounds derived from heterocyclic carbohydrazides and methyl 2-heteroaroylhydrazinecarbodithioates. Heterocycles 85, 871-885 (2012).
54. Ramakrishnan, P., Kahn, D. A. & Baltimore, D. Anti-apoptotic effect of hyperglycemia can allow survival of potentially autoreactive T cells. Cell Death Differ. 18, 690-699 (2011).
55. Ramakrishnan, P. et al. Activation of the transcriptional function of the NF-kappaB protein c-Rel by O-GlcNAc glycosylation. Sci. Signal. 6, ra75 (2013).
56. Tai, Y. T. et al. Anti-CS1 humanized monoclonal antibody HuLuc63 inhibits myeloma cell adhesion and induces antibody-dependent cellular cytotoxicity in the bone marrow milieu. Blood 112, 1329-1337 (2008).