Targeting myeloid-derived suppressor cells using a novel adenosine monophosphate-activated protein kinase (AMPK) activator

OncoImmunology

Volumn 5, Issue 9, 2016, Pages

  Trikha, Prashant ^a   Plews, Robert L ^a   Stiff, Andrew ^a   Gautam, Shalini ^a   Hsu, Vincent ^a   Abood, David ^a   Wesolowski, Robert ^a   Landi, Ian ^a   Mo, Xiaokui ^b   Phay, John ^a   Chen, Ching Shih ^b   Byrd, John ^a   Caligiuri, Michael ^a   Tridandapani, Susheela ^a   Carson, William ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

AMPK; Immunotherapy; iNOS; MDSC; OSU 53

Indexed keywords

2,4 THIAZOLIDINEDIONE DERIVATIVE; ADENOSINE PHOSPHATE; BETA ACTIN; CYTOKINE; DIMETHYL SULFOXIDE; GAMMA INTERFERON; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 2; INTERLEUKIN 6; LIPOCORTIN 5; NITRIC OXIDE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA AGONIST; PROTEIN SERINE THREONINE KINASE; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL LINE; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; IMMUNOBLOTTING; MELANOMA; MITOCHONDRIAL BIOGENESIS; MOUSE; MYELOID DERIVED SUPPRESSOR CELL; NEOPLASM; NONHUMAN; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SUPPRESSOR CELL; TUMOR GROWTH;

EID: 84986313468     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.1080/2162402X.2016.1214787     Document Type: Article

References (46)

1. M.J.Bissell, W.C.Hines. Why don't we get more cancer? A proposed role of the microenvironment in restraining cancer progression. Nat Med 2011; 17:320-9; PMID:21383745; http://dx.doi.org/10.1038/nm.2328
2. D.Lindau, P.Gielen, M.Kroesen, P.Wesseling, G.J.Adema. The immunosuppressive tumour network:myeloid-derived suppressor cells, regulatory T cells and natural killer T cells. Immunology 2013; 138:105-15; PMID:23216602; http://dx.doi.org/10.1111/imm.12036
3. S.Solito, I.Marigo, L.Pinton, V.Damuzzo, S.Mandruzzato, V.Bronte. Myeloid-derived suppressor cell heterogeneity in human cancers. Ann N Y Acad Sci 2014; 1319:47-65; PMID:24965257; http://dx.doi.org/10.1111/nyas.12469
4. D.I.Gabrilovich, S.Nagaraj. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 2009; 9:162-74; PMID:19197294; http://dx.doi.org/10.1038/nri2506
5. P.Trikha, W.E.Carson. Signaling pathways involved in MDSC regulation. Biochim Biophys Acta 2014 Aug; 1846(1):55-65; PMID:24727385; http://dx.doi.org/10.1016/j.bbcan.2014.04.003
6. J.I.Youn, S.Nagaraj, M.Collazo, D.I.Gabrilovich. Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J Immunol 2008; 181:5791-802; PMID:18832739; http://dx.doi.org/10.4049/jimmunol.181.8.5791
7. + T cell tolerance in cancer. Nat Med 2007; 13:828-35; PMID:17603493; http://dx.doi.org/10.1038/nm1609
8. T.Condamine, D.I.Gabrilovich. Molecular mechanisms regulating myeloid-derived suppressor cell differentiation and function. Trends Immunol 2011; 32:19-25; PMID:21067974; http://dx.doi.org/10.1016/j.it.2010.10.002
9. + T cells from patients with GI malignancy. Cancer Immunol Immunother 2011; 60:1269-79; PMID:21604071; http://dx.doi.org/10.1007/s00262-011-1029-z
10. J.Vincent, G.Mignot, F.Chalmin, S.Ladoire, M.Bruchard, A.Chevriaux, F.Martin, L.Apetoh, C.Rébé, F.Ghiringhelli. 5-Fluorouracil selectively kills tumor-associated myeloid-derived suppressor cells resulting in enhanced T cell-dependent antitumor immunity. Cancer Res 2010; 70:3052-61; PMID:20388795; http://dx.doi.org/10.1158/0008-5472.CAN-09-3690
11. R.Wesolowski, J.Markowitz, W.E.Carson. Myeloid derived suppressor cells - a new therapeutic target in the treatment of cancer. J Immunother Cancer 2013; 1:10; PMID:24829747; http://dx.doi.org/10.1186/2051-1426-1-10
12. D.G.Hardie, F.A.Ross, S.A.Hawley. AMPK:a nutrient and energy sensor that maintains energy homeostasis. Nat Rev Mol Cell Biol 2012; 13:251-62; PMID:22436748; http://dx.doi.org/10.1038/nrm3311
13. C.Cantó, Z.Gerhart-Hines, J.N.Feige, M.Lagouge, L.Noriega, J.C.Milne, P.J.Elliott, P.Puigserver, J.Auwerx. AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity. Nature 2009; 458:1056-60; PMID:19262508; http://dx.doi.org/10.1038/nature07813
14. N.Henin, M.F.Vincent, H.E.Gruber, G.Van den Berghe. Inhibition of fatty acid and cholesterol synthesis by stimulation of AMP-activated protein kinase. FASEB J 1995; 9:541-6; PMID:7737463
15. K.Inoki, T.Zhu, K.L.Guan. TSC2 mediates cellular energy response to control cell growth and survival. Cell 2003; 115:577-90; PMID:14651849; http://dx.doi.org/10.1016/S0092-8674(03)00929-2
16. N.Nath, S.Giri, R.Prasad, M.L.Salem, A.K.Singh, I.Singh. 5-aminoimidazole-4-carboxamide ribonucleoside:a novel immunomodulator with therapeutic efficacy in experimental autoimmune encephalomyelitis. J Immunol 2005; 175:566-74; PMID:15972693; http://dx.doi.org/10.4049/jimmunol.175.1.566
17. P.J.Goodwin, J.A.Ligibel, V.Stambolic. Metformin in breast cancer:time for action. J Clin Oncol 2009; 27:3271-3; PMID:19487373; http://dx.doi.org/10.1200/JCO.2009.22.1630
18. P.J.Goodwin, V.Stambolic, J.Lemieux, B.E.Chen, W.R.Parulekar, K.A.Gelmon, D.L.Hershman, T.J.Hobday, J.A.Ligibel, I.A.Mayer et al. Evaluation of metformin in early breast cancer:a modification of the traditional paradigm for clinical testing of anti-cancer agents. Breast Cancer Res Treat 2011; 126:215-20; PMID:20976543; http://dx.doi.org/10.1007/s10549-010-1224-1
19. Y.K.Chae, A.Arya, M.K.Malecek, D.S.Shin, B.Carneiro, S.Chandra, J.Kaplan, A.Kalyan, J.K.Altman, L.Platanias et al. Repurposing metformin for cancer treatment:current clinical studies. Oncotarget 2016 Mar 19; PMID:27004404; http://dx.doi.org/10.18632/oncotarget.8194.
20. K.H.Lee, E.C.Hsu, J.H.Guh, H.C.Yang, D.Wang, S.K.Kulp, C.L.Shapiro, C.S.Chen. Targeting energy metabolic and oncogenic signaling pathways in triple-negative breast cancer by a novel adenosine monophosphate-activated protein kinase (AMPK) activator. J Biol Chem 2011 Nov 11; 286(45):39247-58; PMID:21917926; http://dx.doi.org/10.1074/jbc.M111.264598
21. D.Guo, I.J.Hildebrandt, R.M.Prins, H.Soto, M.M.Mazzotta, J.Dang, J.Czernin, J.Y.Shyy, A.D.Watson, M.Phelps et al. The AMPK agonist AICAR inhibits the growth of EGFRvIII-expressing glioblastomas by inhibiting lipogenesis. Proc Natl Acad Sci U S A 2009; 106:12932-7; PMID:19625624; http://dx.doi.org/10.1073/pnas.0906606106
22. R.R.Landgraf, D.Goswami, F.Rajamohan, M.S.Harris, M.F.Calabrese, L.R.Hoth, R.Magyar, B.D.Pascal, M.J.Chalmers, S.A.Busby et al. Activation of AMP-activated protein kinase revealed by hydrogen/deuterium exchange mass spectrometry. Structure 2013; 21:1942-53; PMID:24076403; http://dx.doi.org/10.1016/j.str.2013.08.023
23. J.H.Guh, W.L.Chang, J.Yang, S.L.Lee, S.Wei, D.Wang, S.K.Kulp, C.S.Chen. Development of novel adenosine monophosphate-activated protein kinase activators. J Med Chem 2010; 53:2552-61; PMID:20170185; http://dx.doi.org/10.1021/jm901773d
24. G.Pilon, P.Dallaire, A.Marette. Inhibition of inducible nitric-oxide synthase by activators of AMP-activated protein kinase:a new mechanism of action of insulin-sensitizing drugs. J Biol Chem 2004; 279:20767-74; PMID:14985344; http://dx.doi.org/10.1074/jbc.M401390200
25. C.C.Chou, K.H.Lee, I.L.Lai, D.Wang, X.Mo, S.K.Kulp, C.L.Shapiro, C.S.Chen. AMPK reverses the mesenchymal phenotype of cancer cells by targeting the Akt-MDM2-Foxo3a signaling axis. Cancer Res 2014; 74:4783-95; PMID:24994714; http://dx.doi.org/10.1158/0008-5472.CAN-14-0135
26. R.L.Plews, A.Mohd Yusof, C.Wang, M.Saji, X.Zhang, C.S.Chen, M.D.Ringel, J.E.Phay. A novel dual AMPK activator/mTOR inhibitor inhibits thyroid cancer cell growth. J Clin Endocrinol Metab 2015; 100:E748-56; PMID:25710562; http://dx.doi.org/10.1210/jc.2014-1777
27. A.Stiff, P.Trikha, R.Wesolowski, K.Kendra, V.Hsu, S.Uppati, E.L.McMichael, M.Duggan, A.Campbell, K.Keller et al. Myeloid-derived suppressor cells express Bruton's tyrosine kinase and can be depleted in tumor bearing hosts by ibrutinib treatment. Cancer Res 2016 Apr 15; 76(8):2125-36; PMID:26880800; http://dx.doi.org/10.1158/0008-5472.CAN-15-1490
28. N.Obermajer, R.Muthuswamy, K.Odunsi, R.P.Edwards, P.Kalinski. PGE(2)-induced CXCL12 production and CXCR4 expression controls the accumulation of human MDSCs in ovarian cancer environment. Cancer Res 2011; 71:7463-70; PMID:22025564; http://dx.doi.org/10.1158/0008-5472.CAN-11-2449
29. P.C.Rodriguez, C.P.Hernandez, D.Quiceno, S.M.Dubinett, J.Zabaleta, J.B.Ochoa, J.Gilbert, A.C.Ochoa. Arginase I in myeloid suppressor cells is induced by COX-2 in lung carcinoma. J Exp Med 2005; 202:931-9; PMID:16186186; http://dx.doi.org/10.1084/jem.20050715
30. P.Serafini, I.Borrello, V.Bronte. Myeloid suppressor cells in cancer:recruitment, phenotype, properties, and mechanisms of immune suppression. Semin Cancer Biol 2006; 16:53-65; PMID:16168663; http://dx.doi.org/10.1016/j.semcancer.2005.07.005
31. C.W.Lee, L.L.Wong, E.Y.Tse, H.F.Liu, V.Y.Leong, J.M.Lee, D.G.Hardie, I.O.Ng, Y.P.Ching. AMPK promotes p53 acetylation via phosphorylation and inactivation of SIRT1 in liver cancer cells. Cancer Res 2012; 72:4394-404; PMID:22728651; http://dx.doi.org/10.1158/0008-5472.CAN-12-0429
32. S.Matsumoto, R.Iwakawa, K.Takahashi, T.Kohno, Y.Nakanishi, Y.Matsuno, K.Suzuki, M.Nakamoto, E.Shimizu, J.D.Minna et al. Prevalence and specificity of LKB1 genetic alterations in lung cancers. Oncogene 2007; 26:5911-8; PMID:17384680; http://dx.doi.org/10.1038/sj.onc.1210418
33. C.T.Pineda, S.Ramanathan, K.Fon Tacer, J.L.Weon, M.B.Potts, Y.H.Ou, M.A.White, P.R.Potts. Degradation of AMPK by a cancer-specific ubiquitin ligase. Cell 2015; 160:715-28; PMID:25679763; http://dx.doi.org/10.1016/j.cell.2015.01.034
34. J.Ouyang, R.A.Parakhia, R.S.Ochs. Metformin activates AMP kinase through inhibition of AMP deaminase. J Biol Chem 2011; 286:1-11; PMID:21059655; http://dx.doi.org/10.1074/jbc.M110.121806
35. T.Schneider, A.Sevko, C.P.Heussel, L.Umansky, P.Beckhove, H.Dienemann, S.Safi, J.Utikal, H.Hoffmann, V.Umansky. Serum inflammatory factors and circulating immunosuppressive cells are predictive markers for efficacy of radiofrequency ablation in non-small-cell lung cancer. Clin Exp Immunol 2015; 180:467-74; PMID:25644608; http://dx.doi.org/10.1111/cei.12596
36. Y.Yan, O.Tsukamoto, A.Nakano, H.Kato, H.Kioka, N.Ito, S.Higo, S.Yamazaki, Y.Shintani, K.Matsuoka et al. Augmented AMPK activity inhibits cell migration by phosphorylating the novel substrate Pdlim5. Nat Commun 2015; 6:6137; PMID:25635515; http://dx.doi.org/10.1038/ncomms7137
37. G.R.Stark, J.E.Darnell. The JAK-STAT pathway at twenty. Immunity 2012; 36:503-14; PMID:22520844; http://dx.doi.org/10.1016/j.immuni.2012.03.013
38. P.Sinha, V.K.Clements, S.Ostrand-Rosenberg. Reduction of myeloid-derived suppressor cells and induction of M1 macrophages facilitate the rejection of established metastatic disease. J Immunol 2005; 174:636-45; PMID:15634881; http://dx.doi.org/10.4049/jimmunol.174.2.636
39. V.Bronte, P.Serafini, C.De Santo, I.Marigo, V.Tosello, A.Mazzoni, D.M.Segal, C.Staib, M.Lowel, G.Sutter et al. IL-4-induced arginase 1 suppresses alloreactive T cells in tumor-bearing mice. J Immunol 2003; 170:270-8; PMID:12496409; http://dx.doi.org/10.4049/jimmunol.170.1.270
40. X.Yu, R.H.Kennedy, S.J.Liu. JAK2/STAT3, not ERK1/2, mediates interleukin-6-induced activation of inducible nitric-oxide synthase and decrease in contractility of adult ventricular myocytes. J Biol Chem 2003; 278:16304-9; PMID:12595539; http://dx.doi.org/10.1074/jbc.M212321200
41. Q.W.Xie, R.Whisnant, C.Nathan. Promoter of the mouse gene encoding calcium-independent nitric oxide synthase confers inducibility by interferon gamma and bacterial lipopolysaccharide. J Exp Med 1993; 177:1779-84; PMID:7684434; http://dx.doi.org/10.1084/jem.177.6.1779
42. S.Horman, G.Browne, U.Krause, J.Patel, D.Vertommen, L.Bertrand, A.Lavoinne, L.Hue, C.Proud, M.Rider. Activation of AMP-activated protein kinase leads to the phosphorylation of elongation factor 2 and an inhibition of protein synthesis. Curr Biol 2002; 12:1419-23; PMID:12194824; http://dx.doi.org/10.1016/S0960-9822(02)01077-1
43. J.Blanchette, M.Jaramillo, M.Olivier. Signalling events involved in interferon-gamma-inducible macrophage nitric oxide generation. Immunology 2003; 108:513-22; PMID:12667213; http://dx.doi.org/10.1046/j.1365-2567.2003.01620.x
44. J.S.Welch, M.Ricote, T.E.Akiyama, F.J.Gonzalez, C.K.Glass. PPARgamma and PPARdelta negatively regulate specific subsets of lipopolysaccharide and IFN-gamma target genes in macrophages. Proc Natl Acad Sci U S A 2003; 100:6712-7; PMID:12740443; http://dx.doi.org/10.1073/pnas.1031789100
45. B.J.Quinn, H.Kitagawa, R.M.Memmott, J.J.Gills, P.A.Dennis. Repositioning metformin for cancer prevention and treatment. Trends Endocrinol Metab 2013; 24:469-80; PMID:23773243; http://dx.doi.org/10.1016/j.tem.2013.05.004
46. K.A.Varker, S.V.Kondadasula, M.R.Go, G.B.Lesinski, R.Ghosh-Berkebile, A.Lehman, J.P.Monk, T.Olencki, K.Kendra, W.E.Carson. Multiparametric flow cytometric analysis of signal transducer and activator of transcription 5 phosphorylation in immune cell subsets in vitro and following interleukin-2 immunotherapy. Clin Cancer Res 2006; 12:5850-8; PMID:17020993; http://dx.doi.org/10.1158/1078-0432.CCR-06-1159