Tyrosine kinase pathways modulate tumor susceptibility to natural killer cells

Journal of Clinical Investigation

Volumn 122, Issue 7, 2012, Pages 2369-2383

  Bellucci, Roberto ^a,b,c   Nguyen, Hong Nam ^a   Martin, Allison ^a   Heinrichs, Stefan ^c,d   Schinzel, Anna C ^a,d   Hahn, William C ^a,b,c,d   Ritz, Jerome ^a,b,c,d  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d DFCI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; JANUS KINASE 1; JANUS KINASE 2; MITOGEN ACTIVATED PROTEIN KINASE 1; PROTEIN TYROSINE KINASE; SHORT HAIRPIN RNA; TRANSFORMING GROWTH FACTOR BETA;

ACUTE GRANULOCYTIC LEUKEMIA; ACUTE LYMPHOCYTIC LEUKEMIA; APOPTOSIS; ARTICLE; CELL INTERACTION; CELL MEDIATED CYTOTOXICITY; CELL TYPE; CONTROLLED STUDY; CYTOKINE RELEASE; DISEASE PREDISPOSITION; DOWN REGULATION; EFFECTOR CELL; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENE TARGETING; GENETIC SCREENING; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; IMMUNOMODULATION; INHIBITION KINETICS; LENTIVIRINAE; LEUKEMIA CELL; MOLECULAR DYNAMICS; MOLECULAR LIBRARY; MULTIPLE MYELOMA; MYELOMA CELL; NATURAL KILLER CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN TARGETING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; WESTERN BLOTTING;

APOPTOSIS; CELL LINE, TUMOR; COCULTURE TECHNIQUES; GENE EXPRESSION PROFILING; GENE KNOCKDOWN TECHNIQUES; HUMANS; INTERFERON-GAMMA; JANUS KINASE 1; JANUS KINASE 2; JANUS KINASE 3; KILLER CELLS, NATURAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RECEPTOR, IGF TYPE 1; RECEPTOR, INSULIN; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TUMOR ESCAPE; TYK2 KINASE; TYRPHOSTINS;

EID: 84863551532     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI58457     Document Type: Article

References (46)

1. Caligiuri MA. Human natural killer cells. Blood. 2008;112(3):461-469.
2. Vivier E, et al. Innate or adaptive immunity? The example of natural killer cells. Science. 2011; 331(6013):44-49.
3. Lanier LL. Up on the tightrope: natural killer cell activation and inhibition. Nat Immunol. 2008;9(5):495-502. (Pubitemid 351560518)
4. Moretta L, Biassoni R, Bottino C, Mingari MC, Moretta A. Human NK-cell receptors. Immunol Today. 2000;21(9):420-422.
5. Berns K, et al. A large-scale RNAi screen in human cells identifies new components of the p53 pathway. Nature. 2004;428(6981):431-437. (Pubitemid 38419689)
6. Root DE, Hacohen N, Hahn WC, Lander ES, Sabatini DM. Genome-scale loss-of-function screening with a lentiviral RNAi library. Nat Methods. 2006;3(9):715-719. (Pubitemid 44275739)
7. Silva JM, et al. Second-generation shRNA libraries covering the mouse and human genomes. Nat Genet. 2005;37(11):1281-1288. (Pubitemid 41568714)
8. Firestein R, et al. CDK8 is a colorectal cancer oncogene that regulates beta-catenin activity. Nature. 2008;455(7212):547-551.
9. Tiedemann RE, et al. Kinome-wide RNAi studies in human multiple myeloma identify vulnerable kinase targets, including a lymphoid-restricted kinase, GRK6. Blood. 2010;115(8):1594-1604.
10. Robertson MJ, Cochran KJ, Cameron C, Le JM, Tantravahi R, Ritz J. Characterization of a cell line, NKL, derived from an aggressive human natural killer cell leukemia. Exp Hematol. 1996;24(3):406-415. (Pubitemid 26098857)
11. Moffat J, et al. A lentiviral RNAi library for human and mouse genes applied to an arrayed viral high-content screen. Cell. 2006;124(6):1283-1298.
12. Chang L, Karin M. Mammalian MAP kinase signalling cascades. Nature. 2001;410(6824):37-40. (Pubitemid 32225829)
13. Schaeffer HJ, Weber MJ. Mitogen-activated protein kinases: specific messages from ubiquitous messengers. Mol Cell Biol. 1999;19(4):2435-2444. (Pubitemid 29144487)
14. Brideau C, Gunter B, Pikounis B, Liaw A. Improved statistical methods for hit selection in high-throughput screening. J Biomol Screen. 2003; 8(6):634-647.
15. Jackson AL, Linsley PS. Noise amidst the silence: off-target effects of siRNAs? Trends Genet. 2004; 20(11):521-524. (Pubitemid 39314555)
16. Sharma S, Rao A. RNAi screening: tips and techniques. Nat Immunol. 2009;10(8):799-804.
17. McCubrey JA, et al. Roles of the Raf/MEK/ERK pathway in cell growth, malignant transformation and drug resistance. Biochim Biophys Acta. 2007;1773(8):1263-1284. (Pubitemid 47125967)
18. Nair PN, De Armond DT, Adamo ML, Strodel WE, Freeman JW. Aberrant expression and activation of insulin-like growth factor-1 receptor (IGF-1R) are mediated by an induction of IGF-1R promoter activity and stabilization of IGF-1R mRNA and contributes to growth factor independence and increased survival of the pancreatic cancer cell line MIA PaCa-2. Oncogene. 2001;20(57):8203-8214. (Pubitemid 34038209)
19. Gong JH, Maki G, Klingemann HG. Characterization of a human cell line (NK-92) with phenotypical and functional characteristics of activated natural killer cells. Leukemia. 1994;8(4):652-658. (Pubitemid 24133034)
20. Baserga R. The insulin-like growth factor-I receptor as a target for cancer therapy. Expert Opin Ther Targets. 2005;9(4):753-768. (Pubitemid 41131677)
21. Shaw RJ, Cantley LC. Ras, PI(3)K and mTOR signalling controls tumour cell growth. Nature. 2006;441(7092):424-430. (Pubitemid 44050136)
22. Johnstone RW, Frew AJ, Smyth MJ. The TRAIL apoptotic pathway in cancer onset, progression and therapy. Nat Rev Cancer. 2008;8(10):782-798.
23. Shimizu K, Asakura M, Fujii S. Prolonged antitumor NK cell reactivity elicited by CXCL10-expressing dendritic cells licensed by CD40L+ CD4+ memory T cells. J Immunol. 2011;186(10):5927-5937.
24. Taub DD, Sayers TJ, Carter CR, Ortaldo JR. Alpha and beta chemokines induce NK cell migration and enhance NK-mediated cytolysis. J Immunol. 1995;155(8):3877-3888.
25. Lanier LL. NK cell recognition. Annu Rev Immunol. 2005;23:225-274. (Pubitemid 40563170)
26. Dunn GP, Bruce AT, Ikeda H, Old LJ, Schreiber RD. Cancer immunoediting: from immunosurveillance to tumor escape. Nat Immunol. 2002;3(11):991-998. (Pubitemid 35363648)
27. Orr MT, Lanier LL. Natural killer cell education and tolerance. Cell. 2010;142(6):847-856.
28. Smyth MJ, Dunn GP, Schreiber RD. Cancer immunosurveillance and immunoediting: the roles of immunity in suppressing tumor development and shaping tumor immunogenicity. Adv Immunol. 2006;90:1-50. (Pubitemid 43765795)
29. Manning G, Whyte DB, Martinez R, Hunter T, Sudarsanam S. The protein kinase complement of the human genome. Science. 2002;298(5600):1912-1934. (Pubitemid 35425239)
30. Jiang K, et al. Pivotal role of phosphoinositide-3 kinase in regulation of cytotoxicity in natural killer cells. Nat Immunol. 2000;1(5):419-425.
31. Wei S, et al. Direct tumor lysis by NK cells uses a Ras-independent mitogen-activated protein kinase signal pathway. J Immunol. 2000;165(7):3811- 3819. (Pubitemid 32057288)
32. Bellido T, Borba VZ, Roberson P, Manolagas SC. Activation of the Janus kinase/STAT (signal transducer and activator of transcription) signal transduction pathway by interleukin-6-type cytokines promotes osteoblast differentiation. Endocrinology. 1997;138(9):3666-3676. (Pubitemid 27351915)
33. Nicholson SE, Oates AC, Harpur AG, Ziemiecki A, Wilks AF, Layton JE. Tyrosine kinase JAK1 is associated with the granulocyte-colony-stimulating factor receptor and both become tyrosine-phosphorylated after receptor activation. Proc Natl Acad Sci U S A. 1994;91(8):2985-2988.
34. Jelinek J, et al. JAK2 mutation 1849G>T is rare in acute leukemias but can be found in CMML, Philadelphia chromosome-negative CML, and megakaryocytic leukemia. Blood. 2005;106(10):3370-3373. (Pubitemid 41609167)
35. Lacronique V, et al. A TEL-JAK2 fusion protein with constitutive kinase activity in human leukemia. Science. 1997;278(5341):1309-1312. (Pubitemid 27495745)
36. Conklyn M, Andresen C, Changelian P, Kudlacz E. The JAK3 inhibitor CP-690550 selectively reduces NK and CD8+ cell numbers in cynomolgus monkey blood following chronic oral dosing. J Leukoc Biol. 2004;76(6):1248-1255. (Pubitemid 39602962)
37. Hedvat M, et al. The JAK2 inhibitor AZD1480 potently blocks Stat3 signaling and oncogenesis in solid tumors. Cancer Cell. 2009;16(6):487-497.
38. Ferrajoli A, et al. WP1066 disrupts Janus kinase-2 and induces caspase-dependent apoptosis in acute myelogenous leukemia cells. Cancer Res. 2007;67(23):11291-11299. (Pubitemid 350248555)
39. Blake SJ, Bruce Lyons A, Fraser CK, Hayball JD, Hughes TP. Dasatinib suppresses in vitro natural killer cell cytotoxicity. Blood. 2008;111(8):4415-4416.
40. Schade AE, et al. Dasatinib, a small-molecule protein tyrosine kinase inhibitor, inhibits T-cell activation and proliferation. Blood. 2008;111(3):1366-1377. (Pubitemid 351213423)
41. Escudier B, et al. Sorafenib in advanced clear-cell renal-cell carcinoma. N Engl J Med. 2007; 356(2):125-134. (Pubitemid 46089673)
42. Goodman VL, et al. Approval summary: sunitinib for the treatment of imatinib refractory or intolerant gastrointestinal stromal tumors and advanced renal cell carcinoma. Clin Cancer Res. 2007;13(5):1367-1373. (Pubitemid 46450424)
43. Hipp MM, et al. Sorafenib, but not sunitinib, affects function of dendritic cells and induction of primary immune responses. Blood. 2008;111(12):5610-5620.
44. Krusch M, et al. The kinase inhibitors sunitinib and sorafenib differentially affect NK cell antitumor reactivity in vitro. J Immunol. 2009;183(12):8286-8294.
45. Ozao-Choy J, et al. The novel role of tyrosine kinase inhibitor in the reversal of immune suppression and modulation of tumor microenvironment for immune-based cancer therapies. Cancer Res. 2009;69(6):2514-2522.
46. Reich M, Liefeld T, Gould J, Lerner J, Tamayo P, Mesirov JP. GenePattern 2.0. Nat Genet. 2006; 38(5):500-501.