Constitutive activation of STAT3 in Sézary syndrome is independent of SHP-1

Leukemia

Volumn 26, Issue 2, 2012, Pages 323-331

  McKenzie, R C T ^a   Jones, C L ^a   Tosi, I ^a   Caesar, J A ^a   Whittaker, S J ^a   Mitchell, T J ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

cutaneous T cell lymphoma; JAK; S zary syndrome; SHP 1; STAT3

Indexed keywords

JANUS KINASE 1; JANUS KINASE 2; JANUS KINASE INHIBITOR; PROTEIN TYROSINE PHOSPHATASE SHP 1; PYRIDONE 6; SMALL INTERFERING RNA; STAT3 PROTEIN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CD4+ T LYMPHOCYTE; CELL POPULATION; CONTROLLED STUDY; CPG ISLAND; EX VIVO STUDY; GENE EXPRESSION; GENE MUTATION; GENE TARGETING; HISTOPATHOLOGY; HUMAN; HUMAN CELL; MAJOR CLINICAL STUDY; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN METHYLATION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; SEZARY CELL; SEZARY SYNDROME; TRANSCRIPTION INITIATION; TUMOR CELL;

BASE SEQUENCE; CASE-CONTROL STUDIES; CELL LINE; DNA METHYLATION; DNA PRIMERS; FLOW CYTOMETRY; GENE SILENCING; HUMANS; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 6; REAL-TIME POLYMERASE CHAIN REACTION; SEZARY SYNDROME; STAT3 TRANSCRIPTION FACTOR;

EID: 84856699177     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2011.198     Document Type: Article

References (56)

1. Agar NS, Wedgeworth E, Crichton S, Mitchell TJ, Cox M, Ferreira S et al. Survival outcomes and prognostic factors in mycosis fungoides/Sezary syndrome: validation of the revised International Society for Cutaneous Lymphomas/European Organisation for Research and Treatment of Cancer staging proposal. J Clin Oncol 2010; 28: 4730-4739.
2. Campbell JJ, Clark RA, Watanabe R, Kupper TS. Sezary syndrome and mycosis fungoides arise from distinct T-cell subsets: a biologic rationale for their distinct clinical behaviors. Blood 2010; 116: 767-771.
3. Contassot E, Kerl K, Roques S, Shane R, Gaide O, Dupuis M et al. Resistance to FasL and tumor necrosis factor-related apoptosisinducing ligand-mediated apoptosis in Sezary syndrome T-cells associated with impaired death receptor and FLICE-inhibitory protein expression. Blood 2008; 111: 4780-4787.
4. Levy DE, Darnell Jr JE. Stats: transcriptional control and biological impact. Nat Rev Mol Cell Biol 2002; 3: 651-662. (Pubitemid 34987786)
5. Lim CP, Cao X. Structure, function, and regulation of STAT proteins. Mol Biosyst 2006; 2: 536-550. (Pubitemid 44583902)
6. Yang J, Liao X, Agarwal MK, Barnes L, Auron PE, Stark GR. Unphosphorylated STAT3 accumulates in response to IL-6 and activates transcription by binding to NFkappaB. Genes Dev 2007; 21: 1396-1408. (Pubitemid 46871042)
7. Yang J, Stark GR. Roles of unphosphorylated STATs in signaling. Cell Res 2008; 18: 443-451. (Pubitemid 351498851)
8. Bromberg JF, Horvath CM, Besser D, Lathem WW, Darnell Jr JE. Stat3 activation is required for cellular transformation by v-src. Mol Cell Biol 1998; 18: 2553-2558. (Pubitemid 28183425)
9. Al Zaid Siddiquee K, Turkson J. STAT3 as a target for inducing apoptosis in solid and hematological tumors. Cell Res 2008; 18: 254-267. (Pubitemid 351206162)
10. Zhang Q, Nowak I, Vonderheid EC, Rook AH, Kadin ME, Nowell PC et al. Activation of Jak/STAT proteins involved in signal transduction pathway mediated by receptor for interleukin 2 in malignant T lymphocytes derived from cutaneous anaplastic large T-cell lymphoma and Sezary syndrome. Proc Natl Acad Sci USA 1996; 93: 9148-9153.
11. Sommer VH, Clemmensen OJ, Nielsen O, Wasik M, Lovato P, Brender C et al. In vivo activation of STAT3 in cutaneous T-cell lymphoma. Evidence for an antiapoptotic function of STAT3. Leukemia 2004; 18: 1288-1295. (Pubitemid 39023140)
12. Verma NK, Davies AM, Long A, Kelleher D, Volkov Y. STAT3 knockdown by siRNA induces apoptosis in human cutaneous T-cell lymphoma line Hut78 via downregulation of Bcl-xL. Cell Mol Biol Lett 2010; 15: 342-355.
13. Eriksen KW, Kaltoft K, Mikkelsen G, Nielsen M, Zhang Q, Geisler C et al. Constitutive STAT3-activation in Sezary syndrome: tyrphostin AG490 inhibits STAT3-activation, interleukin-2 receptor expression and growth of leukemic Sezary cells. Leukemia 2001; 15: 787-793. (Pubitemid 32492702)
14. Nielsen M, Nissen MH, Gerwien J, Zocca MB, Rasmussen HM, Nakajima K et al. Spontaneous interleukin-5 production in cutaneous T-cell lymphoma lines is mediated by constitutively activated Stat3. Blood 2002; 99: 973-977. (Pubitemid 34525560)
15. Shao W, Growney JD, Feng Y, O'Connor G, Pu M, Zhu W et al. Activity of deacetylase inhibitor panobinostat (LBH589) in cutaneous T-cell lymphoma models: Defining molecular mechanisms of resistance. Int J Cancer 2010; 127: 2199-2208.
16. Zhang C, Li B, Gaikwad AS, Haridas V, Xu Z, Gutterman JU et al. Avicin D selectively induces apoptosis and downregulates p-STAT-3, bcl-2, and survivin in cutaneous T-cell lymphoma cells. J Invest Dermatol 2008; 128: 2728-2735.
17. van Kester MS, Out-Luiting JJ, von dem Borne PA, Willemze R, Tensen CP, Vermeer MH. Cucurbitacin I inhibits Stat3 and induces apoptosis in Sezary cells. J Invest Dermatol 2008; 128: 1691-1695. (Pubitemid 351847375)
18. Zhang C, Li B, Zhang X, Hazarika P, Aggarwal BB, Duvic M. Curcumin selectively induces apoptosis in cutaneous T-cell lymphoma cell lines and patients0 PBMCs: potential role for STAT-3 and NF-kappaB signaling. J Invest Dermatol 2010; 130: 2110-2119.
19. Brender C, Nielsen M, Kaltoft K, Mikkelsen G, Zhang Q, Wasik M et al. STAT3-mediated constitutive expression of SOCS-3 in cutaneous T-cell lymphoma. Blood 2001; 97: 1056-1062. (Pubitemid 32154293)
20. Yu H, Jove R. The STATs of cancer-new molecular targets come of age. Nat Rev Cancer 2004; 4: 97-105. (Pubitemid 38198738)
21. Levine RL, Gilliland DG. JAK-2 mutations and their relevance to myeloproliferative disease. Curr Opin Hematol 2007; 14: 43-47. (Pubitemid 44885611)
22. Chiarle R, Voena C, Ambrogio C, Piva R, Inghirami G. The anaplastic lymphoma kinase in the pathogenesis of cancer. Nat Rev Cancer 2008; 8: 11-23.
23. Hagemeijer A, Graux C. ABL1 rearrangements in T-cell acute lymphoblastic leukemia. Genes Chromosomes Cancer 2010; 49: 299-308.
24. Kameda T, Shide K, Shimoda HK, Hidaka T, Kubuki Y, Katayose K et al. Absence of gain-of-function JAK1 and JAK3 mutations in adult T cell leukemia/lymphoma. Int J Hematol 2010; 92: 320-325.
25. Cornejo MG, Kharas MG, Werneck MB, Le Bras S, Moore SA, Ball B et al. Constitutive JAK3 activation induces lymphoproliferative syndromes in murine bone marrow transplantation models. Blood 2009; 113: 2746-2754.
26. Chim CS, Fung TK, Cheung WC, Liang R, Kwong YL. SOCS1 and SHP1 hypermethylation in multiple myeloma: implications for epigenetic activation of the Jak/STAT pathway. Blood 2004; 103: 4630-4635. (Pubitemid 38745995)
27. Sato H, Oka T, Shinnou Y, Kondo T, Washio K, Takano M et al. Multi-step aberrant CpG island hyper-methylation is associated with the progression of adult T-cell leukemia/lymphoma. Am J Pathol 2010; 176: 402-415.
28. Zhang Q, Raghunath PN, Vonderheid E, Odum N, Wasik MA. Lack of phosphotyrosine phosphatase SHP-1 expression in malignant T-cell lymphoma cells results from methylation of the SHP-1 promoter. Am J Pathol 2000; 157: 1137-1146.
29. Zhang Q, Wang HY, Marzec M, Raghunath PN, Nagasawa T, Wasik MA. STAT3-and DNA methyltransferase 1-mediated epigenetic silencing of SHP-1 tyrosine phosphatase tumor suppressor gene in malignant T lymphocytes. Proc Natl Acad Sci USA 2005; 102: 6948-6953. (Pubitemid 40675422)
30. Witkiewicz A, Raghunath P, Wasik A, Junkins-Hopkins JM, Jones D, Zhang Q et al. Loss of SHP-1 tyrosine phosphatase expression correlates with the advanced stages of cutaneous T-cell lymphoma. Hum Pathol 2007; 38: 462-467. (Pubitemid 46227537)
31. van Dongen JJ, Langerak AW, Bruggemann M, Evans PA, Hummel M, Lavender FL et al. Design and standardization of PCR primers and protocols for detection of clonal immunoglobulin and T-cell receptor gene recombinations in suspect lymphoproliferations: report of the BIOMED-2 Concerted Action BMH4-CT98-3936. Leukemia 2003; 17: 2257-2317. (Pubitemid 38072572)
32. Tiemessen MM, Mitchell TJ, Hendry L, Whittaker SJ, Taams LS, John S. Lack of suppressive CD4+CD25+FOXP3+ T cells in advanced stages of primary cutaneous T-cell lymphoma. J Invest Dermatol 2006; 126: 2217-2223. (Pubitemid 44413168)
33. Jones CL, Wain EM, Chu CC, Tosi I, Foster R, McKenzie RC et al. Downregulation of Fas gene expression in Sezary syndrome is associated with promoter hypermethylation. J Invest Dermatol 2010; 130: 1116-1125.
34. Oka T, Ouchida M, Koyama M, Ogama Y, Takada S, Nakatani Y et al. Gene silencing of the tyrosine phosphatase SHP1 gene by aberrant methylation in leukemias/lymphomas. Cancer Res 2002; 62: 6390-6394. (Pubitemid 35364092)
35. Leon F, Cespon C, Franco A, Lombardia M, Roldan E, Escribano L et al. SHP-1 expression in peripheral T cells from patients with Sezary syndrome and in the T cell line HUT-78: implications in JAK3-mediated signaling. Leukemia 2002; 16: 1470-1477.
36. Scarisbrick JJ, Woolford AJ, Russell-Jones R, Whittaker SJ. Loss of heterozygosity on 10q and microsatellite instability in advanced stages of primary cutaneous T-cell lymphoma and possible association with homozygous deletion of PTEN. Blood 2000; 95: 2937-2942. (Pubitemid 30235906)
37. Pedranzini L, Dechow T, Berishaj M, Comenzo R, Zhou P, Azare J et al. Pyridone 6, a pan-Janus-activated kinase inhibitor, induces growth inhibition of multiple myeloma cells. Cancer Res 2006; 66: 9714-9721. (Pubitemid 44623672)
38. Berishaj M, Gao SP, Ahmed S, Leslie K, Al-Ahmadie H, Gerald WL et al. Stat3 is tyrosine-phosphorylated through the interleukin-6/ glycoprotein 130/Janus kinase pathway in breast cancer. Breast Cancer Res 2007; 9: R32.
39. Ghoreschi K, Laurence A, Shea JJ. Janus kinases in immune cell signaling. Immunol Rev 2009; 228: 273-287.
40. Yu H, Pardoll D, Jove R. STATs in cancer inflammation and immunity: a leading role for STAT3. Nat Rev Cancer 2009; 9: 798-809.
41. Klingmuller U, Lorenz U, Cantley LC, Neel BG, Lodish HF. Specific recruitment of SH-PTP1 to the erythropoietin receptor causes inactivation of JAK2 and termination of proliferative signals. Cell 1995; 80: 729-738.
42. David M, Chen HE, Goelz S, Larner AC, Neel BG. Differential regulation of the alpha/beta interferon-stimulated Jak/Stat pathway by the SH2 domain-containing tyrosine phosphatase SHPTP1. Mol Cell Biol 1995; 15: 7050-7058. (Pubitemid 3004334)
43. Jones PA, Wolkowicz MJ, Rideout III WM, Gonzales FA, Marziasz CM, Coetzee GA et al. De novo methylation of the MyoD1 CpG island during the establishment of immortal cell lines. Proc Natl Acad Sci USA 1990; 87: 6117-6121.
44. Brender C, Lovato P, Sommer VH, Woetmann A, Mathiesen AM, Geisler C et al. Constitutive SOCS-3 expression protects T-cell lymphoma against growth inhibition by IFNalpha. Leukemia 2005; 19: 209-213. (Pubitemid 40220583)
45. Krejsgaard T, Vetter-Kauczok CS, Woetmann A, Lovato P, Labuda T, Eriksen KW et al. Jak3-and JNK-dependent vascular endothelial growth factor expression in cutaneous T-cell lymphoma. Leukemia 2006; 20: 1759-1766. (Pubitemid 44574987)
46. Flex E, Petrangeli V, Stella L, Chiaretti S, Hornakova T, Knoops L et al. Somatically acquired JAK1 mutations in adult acute lymphoblastic leukemia. J Exp Med 2008; 205: 751-758. (Pubitemid 351549874)
47. Mullighan CG, Zhang J, Harvey RC, Collins-Underwood JR, Schulman BA, Phillips LA et al. JAK mutations in high-risk childhood acute lymphoblastic leukemia. Proc Natl Acad Sci USA 2009; 106: 9414-9418.
48. Cornejo MG, Boggon TJ, Mercher T. JAK3: a two-faced player in hematological disorders. Int J Biochem Cell Biol 2009; 41: 2376-2379.
49. Lee JW, Soung YH, Kim SY, Nam SW, Park WS, Lee JY et al. JAK2 V617F mutation is uncommon in non-Hodgkin lymphomas. Leuk Lymphoma 2006; 47: 313-314. (Pubitemid 43084572)
50. Constantinescu SN, Girardot M, Pecquet C. Mining for JAK-STAT mutations in cancer. Trends Biochem Sci 2008; 33: 122-131.
51. Berger CL, Tigelaar R, Cohen J, Mariwalla K, Trinh J, Wang N et al. Cutaneous T-cell lymphoma: malignant proliferation of T-regulatory cells. Blood 2005; 105: 1640-1647. (Pubitemid 40223685)
52. Chong BF, Wilson AJ, Gibson HM, Hafner MS, Luo Y, Hedgcock CJ et al. Immune function abnormalities in peripheral blood mononuclear cell cytokine expression differentiates stages of cutaneous T-cell lymphoma/mycosis fungoides. Clin Cancer Res 2008; 14: 646-653. (Pubitemid 351231143)
53. Schoof N, von Bonin F, Trumper L, Kube D. HSP90 is essential for Jak-STAT signaling in classical Hodgkin lymphoma cells. Cell Commun Signal 2009; 7: 17.
54. Lai KO, Chen Y, Po HM, Lok KC, Gong K, Ip NY. Identification of the Jak/Stat proteins as novel downstream targets of EphA4 signaling in muscle: implications in the regulation of acetylcholinesterase expression. J Biol Chem 2004; 279: 13383-13392. (Pubitemid 38468861)
55. van Doorn R, Dijkman R, Vermeer MH, Out-Luiting JJ, van der Raaij-Helmer EM, Willemze R et al. Aberrant expression of the tyrosine kinase receptor EphA4 and the transcription factor twist in Sezary syndrome identified by gene expression analysis. Cancer Res 2004; 64: 5578-5586. (Pubitemid 39095552)
56. Youle RJ, Strasser A. The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol 2008; 9: 47-59.