Convergent mutations and kinase fusions lead to oncogenic STAT3 activation in anaplastic large cell lymphoma

Cancer Cell

Volumn 27, Issue 4, 2015, Pages 516-532

  Crescenzo, Ramona ^a,b   Abate, Francesco ^a,c,d   Lasorsa, Elena ^a   Tabbo', Fabrizio ^a,b   Gaudiano, Marcello ^a,b   Chiesa, Nicoletta ^a   Di Giacomo, Filomena ^a   Spaccarotella, Elisa ^a   Barbarossa, Luigi ^a   Ercole, Elisabetta ^a   Todaro, Maria ^a,b   Boi, Michela ^a,b   Acquaviva, Andrea ^c   Ficarra, Elisa ^c   Novero, Domenico ^e   Rinaldi, Andrea ^f   Tousseyn, Thomas ^g   Rosenwald, Andreas ^h   Kenner, Lukas ⁱ   Cerroni, Lorenzo ^j   Tzankov, Alexander ^k   Ponzoni, Maurilio ^l   Paulli, Marco ^m   Weisenburger, Dennis ⁿ   Chan, Wing C ⁿ   Iqbal, Javeed ^o   Piris, Miguel A ^p   Zamo', Alberto ^q   Ciardullo, Carmela ^r   Rossi, Davide ^r   Gaidano, Gianluca ^r   Pileri, Stefano ^s,t   Tiacci, Enrico ^u   Falini, Brunangelo ^u   Shultz, Leonard D ^v   Mevellec, Laurence ^w   Vialard, Jorge E ^w   Piva, Roberto ^a,x   Bertoni, Francesco ^f,y   Rabadan, Raul ^d   Inghirami, Giorgio ^a,b,e   more..

^a UNIVERSITY OF TURIN   (Italy)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c POLITECNICO DI TORINO   (Italy)

^d Och Spine at New York Presbyterian Hospitals   (United States)

^e MOLINETTE HOSPITAL   (Italy)

^f INSTITUTE OF ONCOLOGY RESEARCH   (Switzerland)

^g UNIVERSITY OF LEUVEN   (Belgium)

^h UNIVERSITY OF WÜRZBURG   (Germany)

ⁱ MEDICAL UNIVERSITY OF VIENNA   (Austria)

^j MEDICAL UNIVERSITY OF GRAZ   (Austria)

^k UNIVERSITY HOSPITAL BASEL   (Switzerland)

^l SAN RAFFAELE HOSPITAL   (Italy)

^m UNIVERSITY OF PAVIA   (Italy)

ⁿ CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^o UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^p HOSPITAL UNIVERSITARIO MARQUÉS DE VALDECILLA   (Spain)

^q UNIVERSITY OF VERONA   (Italy)

^r UNIVERSITY OF EASTERN PIEDMONT   (Italy)

^s EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

^t UNIVERSITY OF BOLOGNA   (Italy)

^u UNIVERSITY OF PERUGIA   (Italy)

^v JACKSON LABORATORY   (United States)

^w JANSSEN RESEARCH AND DEVELOPMENT   (Belgium)

^x NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^y ONCOLOGY INSTITUTE OF SOUTHERN SWITZERLAND   (Switzerland)

more..

Author keywords

[No Author keywords available]

Indexed keywords

5 CHLORO 4 [[2 (ISOPROPYLSULFONYL)PHENYL]AMINO] 2 [[2 METHOXY 4 [4 (4 METHYL 1 PIPERAZINYL) 1 PIPERIDINYL]PHENYL]AMINO]PYRIMIDINE; ANAPLASTIC LYMPHOMA KINASE; CRIZOTINIB; JANUS KINASE 1; PROTEIN TYROSINE KINASE; RUXOLITINIB; STAT3 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NCOR2; TRANSCRIPTION FACTOR NFKB2; UNCLASSIFIED DRUG; ACTIVATING TRANSCRIPTION FACTOR 3; ATF3 PROTEIN, MOUSE; CHIMERIC PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; JAK1 PROTEIN, MOUSE; ONCOPROTEIN; PROTEIN KINASE TYK2; ROS1 PROTEIN, MOUSE; STAT3 PROTEIN, MOUSE; TYK2 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL GROWTH; CHIMERA; CONTROLLED STUDY; COPY NUMBER VARIATION; DRUG EFFECT; DRUG TARGETING; GENE; GENE FUSION; GENE MUTATION; GENE SEQUENCE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; JAK1 GENE; LARGE CELL LYMPHOMA; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; ROS1 GENE; SIGNAL TRANSDUCTION; SOMATIC MUTATION; STAT3 GENE; TYK2 GENE; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; METABOLISM; PHOSPHORYLATION; TUMOR CELL LINE;

ACTIVATING TRANSCRIPTION FACTOR 3; ANIMALS; CELL LINE, TUMOR; GENE EXPRESSION REGULATION, NEOPLASTIC; HEK293 CELLS; HUMANS; JANUS KINASE 1; LYMPHOMA, LARGE-CELL, ANAPLASTIC; MICE; MUTANT CHIMERIC PROTEINS; NF-KAPPA B; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS; RECEPTOR PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TYK2 KINASE;

EID: 84928015700     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccell.2015.03.006     Document Type: Article

References (36)

1. Abate F., Todaro M., van der Krogt J., Boi M., Landra I., Machiorlatti R., Tabbo F., Messana K., Barreca A., Novero D., et al. A novel patient derived tumorgraft model with TRAF1-ALK anaplastic large cell lymphoma translocation. Leukemia 2014, Published online December 23, 2014. 10.1038/leu.2014.347.
2. Abate F., Zairis S., Ficarra E., Acquaviva A., Wiggins C.H., Frattini V., Lasorella A., Iavarone A., Inghirami G., Rabadan R. Pegasus: a comprehensive annotation and prediction tool for detection of driver gene fusions in cancer. BMC Syst. Biol. 2014, 8:97.
3. Anderson K.C. Targeted therapy of multiple myeloma based upon tumor-microenvironmental interactions. Exp. Hematol. 2007, 35(4, Suppl. 1):155-162.
4. Bellanger D., Jacquemin V., Chopin M., Pierron G., Bernard O.A., Ghysdael J., Stern M.H. Recurrent JAK1 and JAK3 somatic mutations in T-cell prolymphocytic leukemia. Leukemia 2014, 28:417-419.
5. Boi M., Rinaldi A., Kwee I., Bonetti P., Todaro M., Tabbò F., Piva R., Rancoita P.M., Matolcsy A., Timar B., et al. PRDM1/BLIMP1 is commonly inactivated in anaplastic large T-cell lymphoma. Blood 2013, 122:2683-2693.
6. Bournazou E., Bromberg J. Targeting the tumor microenvironment: JAK-STAT3 signaling. JAK-STAT 2013, 2:e23828.
7. Chiarle R., Simmons W.J., Cai H., Dhall G., Zamo A., Raz R., Karras J.G., Levy D.E., Inghirami G. Stat3 is required for ALK-mediated lymphomagenesis and provides a possible therapeutic target. Nat. Med. 2005, 11:623-629.
8. Chrencik J.E., Patny A., Leung I.K., Korniski B., Emmons T.L., Hall T., Weinberg R.A., Gormley J.A., Williams J.M., Day J.E., et al. Structural and thermodynamic characterization of the TYK2 and JAK3 kinase domains in complex with CP-690550 and CMP-6. J.Mol. Biol. 2010, 400:413-433.
9. Grewal J.S., Smith L.B., Winegarden J.D., Krauss J.C., Tworek J.A., Schnitzer B. Highly aggressive ALK-positive anaplastic large cell lymphoma with a leukemic phase and multi-organ involvement: a report of three cases and a review of the literature. Ann. Hematol. 2007, 86:499-508.
10. Jerez A., Clemente M.J., Makishima H., Rajala H., Gómez-Seguí I., Olson T., McGraw K., Przychodzen B., Kulasekararaj A., Afable M., et al. STAT3 mutations indicate the presence of subclinical T-cell clones in a subset of aplastic anemia and myelodysplastic syndrome patients. Blood 2013, 122:2453-2459.
11. Johnston P.A., Grandis J.R. STAT3 signaling: anticancer strategies and challenges. Mol. Interv. 2011, 11:18-26.
12. Kiel M.J., Velusamy T., Rolland D., Sahasrabuddhe A.A., Chung F., Bailey N.G., Schrader A., Li B., Li J.Z., Ozel A.B., et al. Integrated genomic sequencing reveals mutational landscape of T-cell prolymphocytic leukemia. Blood 2014, 124:1460-1472.
13. Koskela H.L., Eldfors S., Ellonen P., van Adrichem A.J., Kuusanmäki H., Andersson E.I., Lagström S., Clemente M.J., Olson T., Jalkanen S.E., et al. Somatic STAT3 mutations in large granular lymphocytic leukemia. N.Engl. J. Med. 2012, 366:1905-1913.
14. Li R., You S., Hu Z., Chen Z.G., Sica G.L., Khuri F.R., Curran W.J., Shin D.M., Deng X. Inhibition of STAT3 by niclosamide synergizes with erlotinib against head and neck cancer. PLoS ONE 2013, 8:e74670.
15. Lupardus P.J., Ultsch M., Wallweber H., Bir Kohli P., Johnson A.R., Eigenbrot C. Structure of the pseudokinase-kinase domains from protein kinase TYK2 reveals a mechanism for Janus kinase (JAK) autoinhibition. Proc. Natl. Acad. Sci. U S A 2014, 111:8025-8030.
16. Neri A., Chang C.C., Lombardi L., Salina M., Corradini P., Maiolo A.T., Chaganti R.S., Dalla-Favera R. B cell lymphoma-associated chromosomal translocation involves candidate oncogene lyt-10, homologous to NF-kappa B p50. Cell 1991, 67:1075-1087.
17. Ngo V.N., Young R.M., Schmitz R., Jhavar S., Xiao W., Lim K.H., Kohlhammer H., Xu W., Yang Y., Zhao H., et al. Oncogenically active MYD88 mutations in human lymphoma. Nature 2011, 470:115-119.
18. Odejide O., Weigert O., Lane A.A., Toscano D., Lunning M.A., Kopp N., Kim S., van Bodegom D., Bolla S., Schatz J.H., et al. A targeted mutational landscape of angioimmunoblastic T-cell lymphoma. Blood 2014, 123:1293-1296.
19. + T-cell lymphomas and T-cell large granular lymphocytic leukemia. Leukemia 2013, 27:2244-2247.
20. Palomero T., Couronné L., Khiabanian H., Kim M.Y., Ambesi-Impiombato A., Perez-Garcia A., Carpenter Z., Abate F., Allegretta M., Haydu J.E., et al. Recurrent mutations in epigenetic regulators, RHOA and FYN kinase in peripheral Tcell lymphomas. Nat. Genet. 2014, 46:166-170.
21. Parilla Castellar E.R., Jaffe E.S., Said J.W., Swerdlow S.H., Ketterling R.P., Knudson R.A., Sidhu J.S., Hsi E.D., Karikehalli S., Jiang L., et al. ALK-negative anaplastic large cell lymphoma is a genetically heterogeneous disease with widely disparate clinical outcomes. Blood 2014, 124:1473-1480.
22. Pilati C., Amessou M., Bihl M.P., Balabaud C., Nhieu J.T., Paradis V., Nault J.C., Izard T., Bioulac-Sage P., Couchy G., et al. Somatic mutations activating STAT3 in human inflammatory hepatocellular adenomas. J.Exp. Med. 2011, 208:1359-1366.
23. Piva R., Agnelli L., Pellegrino E., Todoerti K., Grosso V., Tamagno I., Fornari A., Martinoglio B., Medico E., Zamò A., et al. Gene expression profiling uncovers molecular classifiers for the recognition of anaplastic large-cell lymphoma within peripheral T-cell neoplasms. J.Clin. Oncol. 2010, 28:1583-1590.
24. Privalsky M.L. The role of corepressors in transcriptional regulation by nuclear hormone receptors. Annu. Rev. Physiol. 2004, 66:315-360.
25. Rebouissou S., Amessou M., Couchy G., Poussin K., Imbeaud S., Pilati C., Izard T., Balabaud C., Bioulac-Sage P., Zucman-Rossi J. Frequent in-frame somatic deletions activate gp130 in inflammatory hepatocellular tumours. Nature 2009, 457:200-204.
26. Sanda T., Tyner J.W., Gutierrez A., Ngo V.N., Glover J., Chang B.H., Yost A., Ma W., Fleischman A.G., Zhou W., et al. TYK2-STAT1-BCL2 pathway dependence in T-cell acute lymphoblastic leukemia. Cancer Discov. 2013, 3:564-577.
27. + ALCL and peripheral T-cell lymphoma, not otherwise specified: report from the International Peripheral T-Cell Lymphoma Project. Blood 2008, 111:5496-5504. International Peripheral T-Cell Lymphoma Project.
28. Shaw A.T., Hsu P.P., Awad M.M., Engelman J.A. Tyrosine kinase gene rearrangements in epithelial malignancies. Nat. Rev. Cancer 2013, 13:772-787.
29. Shern J.F., Chen L., Chmielecki J., Wei J.S., Patidar R., Rosenberg M., Ambrogio L., Auclair D., Wang J., Song Y.K., et al. Comprehensive genomic analysis of rhabdomyosarcoma reveals a landscape of alterations affecting a common genetic axis in fusion-positive and fusion-negative tumors. Cancer Discov 2014, 4:216-231.
30. Sonbol M.B., Firwana B., Zarzour A., Morad M., Rana V., Tiu R.V. Comprehensive review of JAK inhibitors in myeloproliferative neoplasms. Ther. Adv. Hematol. 2013, 4:15-35.
31. Swerdlow S.H., Campo E., Haris N.L., Jaffe E.S., Pileri S.A., Stein H., Thiele J., Vardiman J.W. WHO Classification of Tumors of Haemotolopoietic and Lymphoid Tissues 2008, Stylus Publishing, Sterling. Fourth Edition.
32. Velusamy T., Kiel M.J., Sahasrabuddhe A.A., Rolland D., Dixon C.A., Bailey N.G., Betz B.L., Brown N.A., Hristov A.C., Wilcox R.A., et al. A novel recurrent NPM1-TYK2 gene fusion in cutaneous CD30-positive lymphoproliferative disorders. Blood 2014, 124:3768-3771.
33. + lung adenocarcinoma via EGR1. Oncogenesis 2013, 2:e43.
34. Vose J., Armitage J., Weisenburger D. International peripheral T-cell and natural killer/T-cell lymphoma study: pathology findings and clinical outcomes. J.Clin. Oncol. 2008, 26:4124-4130. International T-Cell Lymphoma Project.
35. Yin X., Dewille J.W., Hai T. A potential dichotomous role of ATF3, an adaptive-response gene, in cancer development. Oncogene 2008, 27:2118-2127.
36. Zhang L., Yang J., Qian J., Li H., Romaguera J.E., Kwak L.W., Wang M., Yi Q. Role of the microenvironment in mantle cell lymphoma: IL-6 is an important survival factor for the tumor cells. Blood 2012, 120:3783-3792.