Resveratrol sensitized leukemia stem cell-like KG-1a cells to cytokine-induced killer cells-mediated cytolysis through NKG2D ligands and TRAIL receptors

Cancer Biology and Therapy

Volumn 13, Issue 7, 2012, Pages 516-526

  Hu, Liangshan ^a   Cao, Donglin ^b   Li, Yuhua ^a   He, Yanjie ^a   Guo, Kunyuan ^a  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

^b GUANGDONG SECOND PROVINCIAL GENERAL HOSPITAL   (China)

Author keywords

Cytokine induced killer cells; Cytolysis; KG 1a cells; NKG2D ligands; Resveratrol; Susceptibility; TRAIL receptors

Indexed keywords

BINDING PROTEIN; DEATH RECEPTOR 4; GAMMA INTERFERON; INTERLEUKIN 15; INTERLEUKIN 2; LIGAND; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1 CHAIN RELATED PROTEIN A; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1 CHAIN RELATED PROTEIN B; NATURAL KILLER CELL RECEPTOR NKG2D; RESVERATROL; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND RECEPTOR; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND RECEPTOR 3; UL16 BINDING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL LINE; CHEMOSENSITIZATION; CONTROLLED STUDY; CYTOKINE INDUCED KILLER CELL; CYTOLYSIS; DRUG EFFECT; DRUG MECHANISM; GROWTH INHIBITION; HUMAN; HUMAN CELL; HUMAN PROMYELOBLASTIC LEUKEMIA KG 1A CELL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR INTRINSIC ACTIVITY; T LYMPHOCYTE;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; CELL LINE, TUMOR; CELL MEMBRANE; CELL PROLIFERATION; CYTOKINE-INDUCED KILLER CELLS; CYTOTOXICITY, IMMUNOLOGIC; GENE EXPRESSION REGULATION, LEUKEMIC; GPI-LINKED PROTEINS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; INTERLEUKIN-15; INTERLEUKIN-2; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LEUKEMIA, PROMYELOCYTIC, ACUTE; LEUKOCYTES, MONONUCLEAR; LIGANDS; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY K; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; STILBENES; TUMOR NECROSIS FACTOR DECOY RECEPTORS;

EID: 84861152103     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.4161/cbt.19601     Document Type: Article

References (49)

1. Konopleva MY, Jordan CT. Leukemia stem cells and microenvironment: biology and therapeutic targeting. J Clin Oncol 2011; 29:591-9; PMID:21220598; http://dx.doi.org/10.1200/JCO.2010.31.0904.
2. Schreiber RD, Old LJ, Smyth MJ.Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science 2011; 331:1565-70; PMID:21436444; http://dx.doi.org/10.1126/science. 1203486.
3. O'Sullivan T, Dunn GP, Lacoursiere DY, Schreiber RD, Bui JD. Cancer immunoediting of the NK group 2D ligand H60a. J Immunol 2011; 187:3538-45; PMID:21876033; http://dx.doi.org/10.4049/jimmunol. 1100413.
4. Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 1997; 3:730-7; PMID:9212098; http://dx.doi.org/10.1038/nm0797-730.
5. Fuchs D, Daniel V, Sadeghi M, Opelz G, Naujokat C. Salinomycin overcomes ABC transporter-mediated multidrug and apoptosis resistance in human leukemia stem cell-like KG-1a cells. Biochem Biophys Res Commun 2010; 394:1098-104; PMID:20350531; http://dx.doi.org/10.1016/j.bbrc.2010.03.138.
6. Ringdén O, Karlsson H, Olsson R, Omazic B, Uhlin M. The allogeneic graft-versus-cancer effect. Br J Haematol 2009; 147:614-33; PMID:19735262; http://dx.doi.org/10.1111/j.1365-2141.2009.07886.x.
7. Linn YC, Niam M, Chu S, Choong A, Yong HX, Heng KK, et al. The anti-tumour activity of allogeneic cytokine-induced killer cells in patients who relapse after allogeneic transplant for haematological malignancies. Bone Marrow Transplant 2011; PMID:21986635; http://dx.doi.org/10.1038/bmt.2011.202.
8. Rettinger E, Kuçi S, Naumann I, Becker P, Kreyenberg H, Anzaghe M, et al. The cytotoxic potential of interleukin-15-stimulated cytokine-induced killer cells against leukemia cells. Cytotherapy 2012; 14:91-103; PMID:21973023; http://dx.doi.org/10.3109/1465324 9.2011.613931.
9. Tan AC, Konczak I, Sze DM, Ramzan I. Molecular pathways for cancer chemoprevention by dietary phytochemicals. Nutr Cancer 2011; 63:495-505; PMID:21500099; http://dx.doi.org/10.1080/016355 81.2011.538953.
10. Vanamala J, Reddivari L, Radhakrishnan S, Tarver C. Resveratrol suppresses IGF-1 induced human colon cancer cell proliferation and elevates apoptosis via suppression of IGF-1R/Wnt and activation of p53 signaling pathways. BMC Cancer 2010; 10:238; PMID:20504360; http://dx.doi.org/10.1186/ 1471-2407-10-238.
11. He X, Wang Y, Zhu J, Orloff M, Eng C. Resveratrol enhances the antitumor activity of the mTOR inhibitor rapamycin in multiple breast cancer cell lines mainly by suppressing rapamycin-induced AKT signaling. Cancer Lett 2011; 301:168-76; PMID:21168265; http://dx.doi.org/10.1016/j.canlet.2010.11.012.
12. Roccaro AM, Leleu X, Sacco A, Moreau AS, Hatjiharissi E, Jia X, et al. Resveratrol exerts anti-proliferative activity and induces apoptosis in Waldenström'smacroglobulinemia. Clin Cancer Res 2008; 14:1849-58; PMID:18347188; http://dx.doi. org/10.1158/1078-0432.CCR-07-1750.
13. Gullett NP, Ruhul Amin AR, Bayraktar S, Pezzuto JM, Shin DM, Khuri FR, et al. Cancer prevention with natural compounds. Semin Oncol 2010; 37:258-81; PMID:20709209; http://dx.doi.org/10.1053/j.seminoncol. 2010.06.014.
14. Provinciali M, Re F, Donnini A, Orlando F, Bartozzi B, Di Stasio G, et al. Effect of resveratrol on the development of spontaneous mammary tumors in HER-2/neu transgenic mice. Int J Cancer 2005; 115:36-45; PMID:15688416; http://dx.doi.org/10.1002/ijc.20874.
15. Falchetti R, Fuggetta MP, Lanzilli G, Tricarico M, Ravagnan G. Effects of resveratrol on human immune cell function. Life Sci 2001; 70:81-96; PMID:11764009; http://dx.doi.org/10.1016/S0024-3205(01)01367-4.
16. Zunino SJ, Storms DH. Resveratrol alters proliferative responses and apoptosis in human activated B lymphocytes in vitro. J Nutr 2009; 139:1603-8; PMID:19549761; http://dx.doi.org/10.3945/jn.109.105064.
17. Lu CC, Chen JK. Resveratrol enhances perforin expression and NK cell cytotoxicity through NKG2Ddependent pathways. J Cell Physiol 2010; 223:343-51; PMID:20082299.
18. Soto BL, Hank JA, Darjatmoko SR, Polans AS, Yanke EM, Rakhmilevich AL, et al. Anti-tumor and immunomodulatory activity of resveratrol in vitro and its potential for combining with cancer immunotherapy. Int Immunopharmacol 2011; 11:1877-86; PMID:21854876; http://dx.doi.org/10.1016/j. intimp.2011.07.019.
19. She M, Niu X, Chen X, Li J, Zhou M, He Y, et al. Resistance of leukemic stem-like cells in AML cell line KG-1a to natural killer cell-mediated cytotoxicity. Cancer Lett 2011; PMID:22198207; http://dx.doi. org/10.1016/j.canlet.2011.12.017.
20. Tang Z, Liu XY, Zou P. Resveratrol inhibits the secretion of vascular endothelial growth factor and subsequent proliferation in human leukemia U937 cells. J Huazhong Univ Sci Technolog Med Sci 2007; 27:508-12; PMID:18060622; http://dx.doi.org/10.1007/s11596-007-0508-0.
21. Reis-Sobreiro M, Gajate C, Mollinedo F. Involvement of mitochondria and recruitment of Fas/CD95 signaling in lipid rafts in resveratrol-mediated antimyeloma and antileukemia actions. Oncogene 2009; 28:3221-34; PMID:19561642; http://dx.doi.org/10.1038/onc.2009.183.
22. Cakir Z, Saydam G, Sahin F, Baran Y. The roles of bioactive sphingolipids in resveratrol-induced apoptosis in HL60: acute myeloid leukemia cells. J Cancer Res Clin Oncol 2011; 137:279-86; PMID:20401667; http:// dx.doi.org/10.1007/s00432-010-0884-x.
23. Kartal M, Saydam G, Sahin F, Baran Y. Resveratrol triggers apoptosis through regulating ceramide metabolizing genes in human K562 chronic myeloid leukemia cells. Nutr Cancer 2011; 63:637-44; PMID:21500096; http://dx.doi.org/ 10.1080/01635581.2011.538485.
24. Shankar S, Nall D, Tang SN, Meeker D, Passarini J, Sharma J, et al. Resveratrol inhibits pancreatic cancer stem cell characteristics in human and KrasG12D transgenic mice by inhibiting pluripotency maintaining factors and epithelial-mesenchymal transition. PLoS One 2011; 6:16530; PMID:21304978; http://dx.doi. org/10.1371/journal.pone.0016530.
25. Pandey PR, Okuda H, Watabe M, Pai SK, Liu W, Kobayashi A, et al. Resveratrol suppresses growth of cancer stem-like cells by inhibiting fatty acid synthase. Breast Cancer Res Treat 2011; 130:387-98; PMID:21188630; http://dx.doi.org/10.1007/s10549-010-1300-6.
26. Li T, Wang W, Chen H, Li T, Ye L. Evaluation of anti-leukemia effect of resveratrol by modulating STAT3 signaling. Int Immuno pharmacol 2010; 10:18-25; PMID:19796711; http://dx.doi.org/10.1016/j. intimp.2009.09.009.
27. Luzi C, Brisdelli F, Cinque B, Cifone G, Bozzi A. Differential sensitivity to resveratrol-induced apoptosis of human chronic myeloid (K562) and acute lymphoblastic (HSB-2) leukemia cells. Biochem Pharmacol 2004; 68:2019-30; PMID:15476673; http://dx.doi. org/10.1016/j.bcp.2004.07.002.
28. Feng YH, Zhou WL, Wu QL, Li XY, Zhao WM, Zou JP. Low dose of resveratrol enhanced immune response of mice. Acta Pharmacol Sin 2002; 23:893-7; PMID:12370094.
29. Buddingh EP, Schilham MW, Ruslan SE, Berghuis D, Szuhai K, Suurmond J, et al. Chemotherapy-resistant osteosarcoma is highly susceptible to IL-15-activated allogeneic and autologous NK cells. Cancer Immunol Immunother 2011; 60:575-86; PMID:21240486; http://dx.doi.org/10.1007/s00262-010-0965-3.
30. Correia MP, Costa AV, Uhrberg M, Cardoso EM, Arosa FA. IL-15 induces CD8+ T cells to acquire functional NK receptors capable of modulating cytotoxicity and cytokine secretion. Immunobiology 2011; 216:604-12; PMID:20956026; http://dx.doi.org/10.1016/j. imbio.2010.09.012.
31. Bae JH, Kim JY, Kim MJ, Chang SH, Park YS, Son CH, et al. Quercetin enhances susceptibility to NK cell-mediated lysis of tumor cells through induction of NKG2D ligands and suppression of HSP70. J Immunother 2010; 33:391-401; PMID:20386467; http://dx.doi.org/10.1097/CJI.0b013e3181d32f22.
32. González S, López-Soto A, Suarez-Alvarez B, López- Vázquez A, López-Larrea C. NKG2D ligands: key targets of the immune response. Trends Immunol 2008; 29:397-403; PMID:18602338; http://dx.doi. org/10.1016/j.it.2008.04.007.
33. Ogbomo H, Michaelis M, Klassert D, Doerr HW, Cinatl J Jr. Resistance to cytarabine induces the upregulation of NKG2D ligands and enhances natural killer cell lysis of leukemic cells. Neoplasia 2008; 10:1402-10; PMID:19048119.
34. Waldhauer I, Steinle A. NK cells and cancer immunosurveillance. Oncogene 2008; 27:5932-43; PMID:18836474; http://dx.doi.org/10.1038/onc.2008.267.
35. Zhang C, Wang Y, Zhou Z, Zhang J, Tian Z. Sodium butyrate upregulates expression of NKG2D ligand MICA/B in HeLa and HepG2 cell lines and increases their susceptibility to NK lysis. Cancer Immunol Immunother 2009; 58:1275-85; PMID:19139882; http://dx.doi.org/10.1007/s00262-008-0645-8.
36. Armeanu S, Krusch M, Baltz KM, Weiss TS, Smirnow I, Steinle A, et al. Direct and natural killer cell-mediated antitumor effects of low-dose bortezomib in hepatocellular carcinoma. Clin Cancer Res 2008; 14:3520-8; PMID:18519785; http://dx.doi.org/10.1158/1078-0432.CCR-07-4744.
37. Tang KF, Ren H, Cao J, Zeng GL, Xie J, Chen M, et al. Decreased Dicer expression elicits DNA damage and upregulation of MICA and MICB. J Cell Biol 2008; 182:233-9; PMID:18644891; http://dx.doi. org/10.1083/jcb.200801169.
38. Qiao Y, Liu B, Li Z. Activation of NK cells by extra-cellular heat shock protein 70 through induction of NKG2D ligands on dendritic cells. Cancer Immun 2008; 8:12; PMID:18613644.
39. Molinero LL, Fuertes MB, Girart MV, Fainboim L, Rabinovich GA, Costas MA, et al. NFkappaB regulates expression of the MHC class I-related chain A gene in activated T lymphocytes. J Immunol 2004; 173:5583-90; PMID:15494508.
40. Tokuyama M, Lorin C, Delebecque F, Jung H, Raulet DH, Coscoy L. Expression of the RAE-1 family of stimulatory NK-cell ligands requires activation of the PI3K pathway during viral infection and transformation. PLoS Pathog 2011; 7:1002265; PMID:21966273; http://dx.doi.org/10.1371/journal.ppat. 1002265.
41. Zauli G, Bosco R, Secchiero P. Molecular targets for selective killing of TRAIL-resistant leukemic cells. Expert Opin Ther Targets 2011; 15:931-42; PMID:21548717; http://dx.doi.org/10.1517/1472822 2.2011.580278.
42. Smyth MJ, Cretney E, Kelly JM, Westwood JA, Street SE, Yagita H, et al. Activation of NK cell cytotoxicity. Mol Immunol 2005; 42:501-10; PMID:15607806; http://dx.doi.org/10.1016/j.molimm.2004.07.034.
43. Sayers TJ. Targeting the extrinsic apoptosis signaling pathway for cancer therapy. Cancer Immunol Immunother 2011; 60:1173-80; PMID:21626033; http://dx.doi.org/10.1007/s00262-011-1008-4.
44. Shankar S, Chen Q, Siddiqui I, Sarva K, Srivastava RK. Sensitization of TRAIL-resistant LNCaP cells by resveratrol (3,4',5-tri-hydroxystilbene): molecular mechanisms and therapeutic potential. J Mol Signal 2007; 2:7; PMID:17718901; http://dx.doi. org/10.1186/1750-2187-2-7.
45. Rushworth SA, Micheau O. Molecular crosstalk between TRAIL and natural antioxidants in the treatment of cancer. Br J Pharmacol 2009; 157:1186-8; PMID:19664138; http://dx.doi.org/10.1111/j.1476-5381.2009.00266.x.
46. Jacquemin G, Shirley S, Micheau O. Combining naturally occurring polyphenols with TNF-related apoptosis-inducing ligand: a promising approach to kill resistant cancer cells? Cell Mol Life Sci 2010; 67:3115-30; PMID:20508968; http://dx.doi.org/10.1007/s00018-010-0407-6.
47. Naka K, Hoshii T, Tadokoro Y, Hirao A. Molecular pathology of tumor-initiating cells: lessons from Philadelphia chromosome-positive leukemia. Pathol Int 2011; 61:501-8; PMID:21884299; http://dx.doi. org/10.1111/j.1440-827. 2011.02688.x.
48. Li Y, Wicha MS, Schwartz SJ, Sun D. Implications of cancer stem cell theory for cancer chemoprevention by natural dietary compounds. J Nutr Biochem 2011; 22:799-806; PMID:21295962; http://dx.doi. org/10.1016/j.jnutbio.2010.11. 001.
49. Buss EC, Ho AD. Leukemia stem cells. Int J Cancer 2011; 129:2328-36; PMID:21796620; http://dx.doi. org/10.1002/ijc.26318.