Resveratrol enhances perforin expression and NK cell cytotoxicity through NKG2D-dependent pathways

Journal of Cellular Physiology

Volumn 223, Issue 2, 2010, Pages 343-351

  Lu, Chia Chen ^a   Chen, Jan Kan ^a  

^a CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 4 AMINO 5,6,7,8 TETRAHYDRO 7 HYDROXY 2 METHYLBENZO[B]THIENO[2,3 B]PYRIDINE 3 CARBOXYLIC ACID; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; INTERLEUKIN 2; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; MITOGEN ACTIVATED PROTEIN KINASE P38 INHIBITOR; PERFORIN; RESVERATROL; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL STRAIN HEPG2; CELL STRAIN K 562; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG POTENTIATION; HUMAN; HUMAN CELL; LYMPHOCYTE ACTIVATION; NATURAL KILLER CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANTIOXIDANTS; CELL LINE; CYTOTOXICITY, IMMUNOLOGIC; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SYNERGISM; ENZYME INHIBITORS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; IMMUNITY, INNATE; INTERLEUKIN-2; JNK MITOGEN-ACTIVATED PROTEIN KINASES; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; MAP KINASE SIGNALING SYSTEM; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY K; PERFORIN; RNA INTERFERENCE; STILBENES; UP-REGULATION;

RATTUS;

EID: 77950832747     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.22043     Document Type: Article

References (55)

1. Bauer S, Groh V, Wu J, Steinle A, Phillips JH, Lanier LL, Spies T. 1999. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 285:727-729.
2. Baur JA, Sinclair DA. 2006. Therapeutic potential of resveratrol: The in vivo evidence. Nat Rev Drug Discov 5:493-506.
3. Biron CA, Brossay L. 2001. NK cells and NKT cells in innate defense against viral infections. Curr Opin Immunol 13:458-464.
4. Borchers MT, Harris NL, Wesselkamper SC, Vitucci M, Cosman D. 2006. NKG2D ligands are expressed on stressed human airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 291:L222-L231.
5. Bruno AP, Lautier D, d'Orgeix AT, Laurent G, Quillet-Mary A. 2000. Acute myeloblastic leukemic cells acquire cellular cytotoxicity under genotoxic stress: Implication of granzyme B and perforin. Blood 96:1914-1920.
6. Castriconi R, Cantoni C, Della CM, Vitale M, Marcenaro E, Conte R, Biassoni R, Bottino C, Moretta L, Moretta A. 2003. Transforming growth factor beta 1 inhibits expression of NKp30 and NKG2D receptors: Consequences for the NK-mediated killing of dendritic cells. Proc Natl Acad Sci USA 100:4120-4125.
7. Chen X, Allan DS, Krzewski K, Ge B, Kopcow H, Strominger JL. 2006. CD28-stimulated ERK2 phosphorylation is required for polarization of the microtubule organizing center and granules in YTS NK cells. Proc Natl Acad Sci USA 103:10346-10351. (Pubitemid 44051169)
8. Chen X, Trivedi PP, Ge B, Krzewski K, Strominger JL. 2007. Many NK cell receptors activate ERK2 and JNK1 to trigger microtubule organizing center and granule polarization and cytotoxicity. Proc Natl Acad Sci USA 104:6329-6334. (Pubitemid 47186094)
9. Colucci F, Di Santo JP, Leibson PJ. 2002. Natural killer cell activation in mice and men: Different triggers for similar weapons? Nat Immunol 3:807-813.
10. Das DK, Maulik N. 2006. Resveratrol in cardioprotection: A therapeutic promise of alternative medicine. Mol Interv 6:36-47. (Pubitemid 43327521)
11. Diefenbach A, Jamieson AM, Liu SD, Shastri N, Raulet DH. 2000. Ligands for the murine NKG2D receptor: Expression by tumor cells and activation of NK cells and macrophages. Nat Immunol 1:119-126.
12. Docherty JJ, Smith JS, Fu MM, Stoner T, Booth T. 2004. Effect of topically applied resveratrol on cutaneous herpes simplex virus infections in hairless mice. Antiviral Res 61:19-26. (Pubitemid 37508526)
13. Docherty JJ, Fu MM, Hah JM, Sweet TJ, Faith SA, Booth T. 2005. Effect of resveratrol on herpes simplex virus vaginal infection in the mouse. Antiviral Res 67:155-162. (Pubitemid 41254199)
14. Donnelly LE, Newton R, Kennedy GE, Fenwick PS, Leung RH, Ito K, Russell RE, Barnes PJ. 2004. Anti-inflammatory effects of resveratrol in lung epithelial cells: Molecular mechanisms. Am J Physiol Lung Cell Mol Physiol 287:L774-L783.
15. Falchetti R, Fuggetta MP, Lanzilli G, Tricarico M, Ravagnan G. 2001. Effects of resveratrol on human immune cell function. Life Sci 70:81-96. (Pubitemid 33124357)
16. Fehniger TA, Cai SF, Cao X, Bredemeyer AJ, Presti RM, French AR, Ley TJ. 2007. Acquisition of murine NK cell cytotoxicity requires the translation of a pre-existing pool of granzyme B and perforin mRNAs. Immunity 26:798-811. (Pubitemid 46907665)
17. Feng YH, Zhou WL, Wu QL, Li XY, Zhao WM, Zou JP. 2002. Low dose of resveratrol enhanced immune response of mice. Acta Pharmacol Sin 23:893-897.
18. Ferry-Dumazet H, Garnier O, Mamani-Matsuda M, Vercauteren J, Belloc F, Billiard C, Dupouy M, Thiolat D, Kolb JP, Marit G, Reiffers J, Mossalayi MD. 2002. Resveratrol inhibits the growth and induces the apoptosis of both normal and leukemic hematopoietic cells. Carcinogenesis 23:1327-1333.
19. Grossman WJ, Revell PA, Lu ZH, Johnson H, Bredemeyer AJ, Ley TJ. 2003. The orphan granzymes of humans and mice. Curr Opin Immunol 15:544-552.
20. Henkart PA. 1985. Mechanism of lymphocyte-mediated cytotoxicity. Annu Rev Immunol 3:31-58.
21. Hernandez-Pigeon H, Jean C, Charruyer A, Haure MJ, Titeux M, Tonasso L, Quillet-Mary A, Baudouin C, Charveron M, Laurent G. 2006. Human keratinocytes acquire cellular cytotoxicity under UV-B irradiation. Implication of granzyme B and perforin. J Biol Chem 281:13525-13532.
22. Jamieson AM, Diefenbach A, McMahon CW, Xiong N, Carlyle JR, Raulet DH. 2002. The role of the NKG2D immunoreceptor in immune cell activation and natural killing. Immunity 17:19-29. (Pubitemid 34874615)
23. Janas ML, Groves P, Kienzle N, Kelso A. 2005. IL-2 regulates perforin and granzyme gene expression in CD8+ T cells independently of its effects on survival and proliferation. J Immunol 175:8003-8010. (Pubitemid 41798362)
24. Jang M, Cai L, Udeani GO, Slowing KV, Thomas CF, Beecher CW, Fong HH, Farnsworth NR, Kinghorn AD, Mehta RG, Moon RC, Pezzuto JM. 1997. Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science 275:218-220.
25. Jiang K, Zhong B, Gilvary DL, Corliss BC, Hong-Geller E, Wei S, Djeu JY. 2000. Pivotal role of phosphoinositide-3 kinase in regulation of cytotoxicity in natural killer cells. Nat Immunol 1:419-425.
26. Jurisic V. 2003. Estimation of cell membrane alteration after drug treatment by LDH release. Blood 101:2894.
27. Jurisic V, Spuzic I, Konjevic G. 1999. A comparison of the NK cell cytotoxicity with effects of TNF-alpha against K-562 cells, determined by LDH release assay. Cancer Lett 138: 67-72. (Pubitemid 29189186)
28. Kagi D, Vignaux F, Ledermann B, Burki K, Depraetere V, Nagata S, Hengartner H, Golstein P. 1994. Fas and perforin pathways as major mechanisms of T cell-mediated cytotoxicity. Science 265:528-530. (Pubitemid 24264998)
29. Konjevic G, Jurisic V, Spuzic I. 1997. Corrections to the original lactate dehydrogenase (LDH) release assay for the evaluation of NK cell cytotoxicity. J Immunol Methods 200:199-201. (Pubitemid 27035702)
30. Konjevic G, Mirjacic MK, Vuletic A, Jurisic V, Spuzic I. 2009. Distribution of several activating and inhibitory receptors on CD3-CD16+ NK cells and their correlation with NK cell function in healthy individuals. J Membr Biol 230:113-123.
31. Li C, Ge B, Nicotra M, Stern JN, Kopcow HD, Chen X, Strominger JL. 2008. JNK MAP kinase activation is required for MTOC and granule polarization in NKG2D-mediated NK cell cytotoxicity. Proc Natl Acad Sci USA 105:3017-3022. (Pubitemid 351723660)
32. Lieberman J. 2003. The ABCs of granule-mediated cytotoxicity: New weapons in the arsenal. Nat Rev Immunol 3:361-370. (Pubitemid 37323196)
33. Lin HY, Sun M, Tang HY, Simone TM, Wu YH, Grandis JR, Cao HJ, Davis PJ, Davis FB. 2008. Resveratrol causes COX-2- and p53-dependent apoptosis in head and neck squamous cell cancer cells. J Cell Biochem 104:2131-2142.
34. Lu CC, Lai HC, Hsieh SC, Chen JK. 2008. Resveratrol ameliorates Serratia marcescens-induced acute pneumonia in rats. J Leukoc Biol 83:1028-1037.
35. Moretta A, Bottino C, Vitale M, Pende D, Cantoni C, Mingari MC, Biassoni R, Moretta L. 2001. Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis. Annu Rev Immunol 19:197-223. (Pubitemid 32368034)
36. Nguyen TH, Mustafa FB, Pervaiz S, Ng FS, Lim LH. 2008. ERK1/2 activation is required for resveratrol-induced apoptosis in MDA-MB-231 cells. Int J Oncol 33:81-92.
37. Russell JH, Ley TJ. 2002. Lymphocyte-mediated cytotoxicity. Annu Rev Immunol 20:323-370.
38. Scarlatti F, Maffei R, Beau I, Codogno P, Ghidoni R. 2008. Role of non-canonical Beclin 1-independent autophagy in cell death induced by resveratrol in human breast cancer cells. Cell Death Differ 15:1318-1329. (Pubitemid 351984760)
39. Smyth MJ, Hayakawa Y, Takeda K, Yagita H. 2002. New aspects of natural-killer-cell surveillance and therapy of cancer. Nat Rev Cancer 2:850-861. (Pubitemid 37328903)
40. Smyth MJ, Swann J, Kelly JM, Cretney E, Yokoyama WM, Diefenbach A, Sayers TJ, Hayakawa Y. 2004. NKG2D recognition and perforin effector function mediate effective cytokine immunotherapy of cancer. J Exp Med 200:1325-1335. (Pubitemid 39552573)
41. Trapani JA, Smyth MJ. 2002. Functional significance of the perforin/granzyme cell death pathway. Nat Rev Immunol 2:735-747. (Pubitemid 37328714)
42. Tsai SH, Lin-Shiau SY, Lin JK. 1999. Suppression of nitric oxide synthase and the downregulation of the activation of NFkappa B in macrophages by resveratrol. Br J Pharmacol 126:673-680. (Pubitemid 29087846)
43. van Dommelen SL, Sumaria N, Schreiber RD, Scalzo AA, Smyth MJ, Gli-Esposti MA. 2006. Perforin and granzymes have distinct roles in defensive immunity and immunopathology. Immunity 25:835-848. (Pubitemid 46107286)
44. van Ginkel PR, Sareen D, Subramanian L, Walker Q, Darjatmoko SR, Lindstrom MJ, Kulkarni A, Albert DM, Polans AS. 2007. Resveratrol inhibits tumor growth of human neuroblastoma and mediates apoptosis by directly targeting mitochondria. Clin Cancer Res 13:5162-5169.
45. Verneris MR, Karami M, Baker J, Jayaswal A, Negrin RS. 2004. Role of NKG2D signaling in the cytotoxicity of activated and expanded CD8+ T cells. Blood 103:3065-3072. (Pubitemid 38451682)
46. Vivier E, Nunes JA, Vely F. 2004. Natural killer cell signaling pathways. Science 306:1517-1519. (Pubitemid 39564941)
47. Vyas YM, Maniar H, Dupont B. 2002. Visualization of signaling pathways and cortical cytoskeleton in cytolytic and noncytolytic natural killer cell immune synapses. Immunol Rev 189:161-178. (Pubitemid 35448951)
48. Wei S, Gamero AM, Liu JH, Daulton AA, Valkov NI, Trapani JA, Larner AC, Weber MJ, Djeu JY. 1998. Control of lytic function by mitogen-activated protein kinase/extracellular regulatory kinase 2 (ERK2) in a human natural killer cell line: Identification of perforin and granzyme B mobilization by functional ERK2. J Exp Med 187:1753-1765.
49. Wu SL, Pan CE, Yu L, Meng KW. 2005. Immunosuppression by combined use of cyclosporine and resveratrol in a rat liver transplantation model. Transpl Proc 37:2354-2359.
50. Yang Y, Paik JH, Cho D, Cho JA, Kim CW. 2008. Resveratrol induces the suppression of tumor-derived CD4+CD25+ regulatory T cells. Int Immunopharmacol 8:542-547.
51. Yokoyama WM, Kim S, French AR. 2004. The dynamic life of natural killer cells. Annu Rev Immunol 22:405-429.
52. Yu TK, Caudell EG, Smid C, Grimm EA. 2000. IL-2 activation of NK cells: Involvement of MKK1/2/ERK but not p38 kinase pathway. J Immunol 164:6244-6251.
53. Zhang C, Zhang J, Niu J, Zhang J, Tian Z. 2008. Interleukin-15 improves cytotoxicity of natural killer cells via up-regulating NKG2D and cytotoxic effector molecule expression as well as STAT1 and ERK1/2 phosphorylation. Cytokine 42:128-136.
54. Zhou J, Zhang J, Lichtenheld MG, Meadows GG. 2002. A role for NF-kappa B activation in perforin expression of NK cells upon IL-2 receptor signaling. J Immunol 169:1319-1325.
55. Zompi S, Hamerman JA, Ogasawara K, Schweighoffer E, Tybulewicz VL, Di Santo JP, Lanier LL, Colucci F. 2003. NKG2D triggers cytotoxicity in mouse NK cells lacking DAP12 or Syk family kinases. Nat Immunol 4:565-572.