Phosphatidylinositol-3′-kinase/AKT signaling is essential in synovial sarcoma

International Journal of Cancer

Volumn 129, Issue 7, 2011, Pages 1564-1575

  Friedrichs, Nicolaus ^a   Trautmann, Marcel ^a   Endl, Elmar ^a   Sievers, Elisabeth ^a   Kindler, Dagmar ^a   Wurst, Peter ^a   Czerwitzki, Jacqueline ^a   Steiner, Susanne ^a   Renner, Marcus ^b   Penzel, Roland ^b   Koch, Arend ^c   Larsson, Olle ^d   Tanaka, Shinya ^e   Kawai, Akira ^f   Schirmacher, Peter ^b   Mechtersheimer, Gunhild ^b   Wardelmann, Eva ^a   Buettner, Reinhard ^a   Hartmann, Wolfgang ^a  

^a UNIVERSITY HOSPITAL BONN   (Germany)

^b UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^d KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^e HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^f NATIONAL CANCER CENTER HOSPITAL   (Japan)

Author keywords

AKT; GSK 3 ; p27; PI3K; synovial sarcoma

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; CYCLIN D1; CYCLIN DEPENDENT KINASE INHIBITOR 1B; DACTINOMYCIN; DOXORUBICIN; GLYCOGEN SYNTHASE KINASE 3BETA; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SERINE; VINCRISTINE; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; NUCLEAR PROTEIN; PI3KCA PROTEIN, HUMAN; TARGET OF RAPAMYCIN KINASE; TRANSCRIPTION FACTOR;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL GROWTH; CELL PROLIFERATION; CLINICAL ARTICLE; CONTROLLED STUDY; DRUG POTENTIATION; DRUG TARGETING; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GENE; GENE MUTATION; GENETIC SCREENING; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; PIK3CA GENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SARCOMA CELL; SIGNAL TRANSDUCTION; SYNOVIAL SARCOMA; CONNECTIVE TISSUE TUMOR; DRUG EFFECT; GENETICS; METABOLISM; PHOSPHORYLATION; TUMOR CELL LINE;

APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; GLYCOGEN SYNTHASE KINASE 3; HUMANS; NUCLEAR PROTEINS; PHOSPHATIDYLINOSITOL 3-KINASE; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; SARCOMA, SYNOVIAL; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; TRANSCRIPTION FACTORS;

EID: 79960911022     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.25829     Document Type: Article

References (50)

1. Ladanyi M,. Fusions of the SYT and SSX genes in synovial sarcoma. Oncogene 2001; 20: 5755-62. (Pubitemid 32928113)
2. dos Santos NR, de Bruijn DR, van Kessel AG,. Molecular mechanisms underlying human synovial sarcoma development. Genes Chromosomes Cancer 2001; 30: 1-14.
3. Sun Y, Gao D, Liu Y, Huang J, Lessnick S, Tanaka S,. IGF2 is critical for tumorigenesis by synovial sarcoma oncoprotein SYT-SSX1. Oncogene 2006; 25: 1042-52. (Pubitemid 43277012)
4. de Bruijn DR, Allander SV, van Dijk AH, Willemse MP, Thijssen J, van Groningen JJ, Meltzer PS, Geurts van Kessel A,. The synovial sarcoma-associated SS18-SSX2 fusion protein induces epigenetic gene (de)regulation. Cancer Res 2006; 66: 9474-82. (Pubitemid 44623645)
5. Fisher C, de Bruijn DRH, Geurts van Kessel A,. Synovial sarcoma. In:, Fletcher CMD, Unni KK, Mertens F, eds. Pathology and genetics of tumours of soft tissue and bone (WHO classification of tumors). Lyon: IARC, 2002. 200-4.
6. Nielsen TO, Hsu FD, O'Connell JX, Gilks CB, Sorensen PH, Linn S, West RB, Liu CL, Botstein D, Brown PO, van de Rijn M,. Tissue microarray validation of epidermal growth factor receptor and SALL2 in synovial sarcoma with comparison to tumors of similar histology. Am J Pathol 2003; 163: 1449-56. (Pubitemid 37175092)
7. Nuciforo PG, Pellegrini C, Fasani R, Maggioni M, Coggi G, Parafioriti A, Bosari S,. Molecular and immunohistochemical analysis of HER2/neu oncogene in synovial sarcoma. Hum Pathol 2003; 34: 639-45. (Pubitemid 36875508)
8. Tamborini E, Bonadiman L, Greco A, Gronchi A, Riva C, Bertulli R, Casali PG, Pierotti MA, Pilotti S,. Expression of ligand-activated KIT and platelet-derived growth factor receptor beta tyrosine kinase receptors in synovial sarcoma. Clin Cancer Res 2004; 10: 938-43. (Pubitemid 38198893)
9. Oda Y, Sakamoto A, Saito T, Kinukawa N, Iwamoto Y, Tsuneyoshi M,. Expression of hepatocyte growth factor (HGF)/scatter factor and its receptor c-MET correlates with poor prognosis in synovial sarcoma. Hum Pathol 2000; 31: 185-92. (Pubitemid 30090647)
10. Ishibe T, Nakayama T, Okamoto T, Aoyama T, Nishijo K, Shibata KR, Shima Y, Nagayama S, Katagiri T, Nakamura Y, Nakamura T, Toguchida J,. Disruption of fibroblast growth factor signal pathway inhibits the growth of synovial sarcomas: potential application of signal inhibitors to molecular target therapy. Clin Cancer Res 2005; 11: 2702-12. (Pubitemid 40569472)
11. Xie Y, Skytting B, Nilsson G, Brodin B, Larsson O,. Expression of insulin-like growth factor-1 receptor in synovial sarcoma: association with an aggressive phenotype. Cancer Res 1999; 59: 3588-91. (Pubitemid 29381857)
12. Friedrichs N, Kuchler J, Endl E, Koch A, Czerwitzki J, Wurst P, Metzger D, Schulte JH, Holst MI, Heukamp LC, Larsson O, Tanaka S, et al. Insulin-like growth factor-1 receptor acts as a growth regulator in synovial sarcoma. J Pathol 2008; 216: 428-39.
13. Terry J, Lubieniecka JM, Kwan W, Liu S, Nielsen TO,. Hsp90 inhibitor 17-allylamino-17-demethoxygeldanamycin prevents synovial sarcoma proliferation via apoptosis in in vitro models. Clin Cancer Res 2005; 11: 5631-8. (Pubitemid 41060842)
14. Diehl JA, Cheng M, Roussel MF, Sherr CJ,. Glycogen synthase kinase-3beta regulates cyclin D1 proteolysis and subcellular localization. Genes Dev 1998; 12: 3499-511. (Pubitemid 28553242)
15. Osaki M, Oshimura M, Ito H,. PI3K-Akt pathway: its functions and alterations in human cancer. Apoptosis 2004; 9: 667-76. (Pubitemid 40941196)
16. Vivanco I, Sawyers CL,. The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat Rev Cancer 2002; 2: 489-501. (Pubitemid 37328931)
17. Bjornsti MA, Houghton PJ,. The TOR pathway: a target for cancer therapy. Nat Rev Cancer 2004; 4: 335-48. (Pubitemid 38579480)
18. Liang J, Slingerland JM,. Multiple roles of the PI3K/PKB (Akt) pathway in cell cycle progression. Cell Cycle 2003; 2: 339-45.
19. Sherr CJ,. Cancer cell cycles. Science 1996; 274: 1672-7.
20. Samuels Y, Wang Z, Bardelli A, Silliman N, Ptak J, Szabo S, Yan H, Gazdar A, Powell SM, Riggins GJ, Willson JK, Markowitz S, et al. High frequency of mutations of the PIK3CA gene in human cancers. Science 2004; 304: 554. (Pubitemid 38541907)
21. Broderick DK, Di C, Parrett TJ, Samuels YR, Cummins JM, McLendon RE, Fults DW, Velculescu VE, Bigner DD, Yan H,. Mutations of PIK3CA in anaplastic oligodendrogliomas, high-grade astrocytomas, and medulloblastomas. Cancer Res 2004; 64: 5048-50. (Pubitemid 39006515)
22. Friedrichs N, Kriegl L, Poremba C, Schaefer KL, Gabbert HE, Shimomura A, Paggen E, Merkelbach-Bruse S, Buettner R,. Pitfalls in the detection of t(11;22) translocation by fluorescence in situ hybridization and RT-PCR: a single-blinded study. Diagn Mol Pathol 2006; 15: 83-9. (Pubitemid 44350484)
23. Xie Y, Skytting B, Nilsson G, Gasbarri A, Haslam K, Bartolazzi A, Brodin B, Mandahl N, Larsson O,. SYT-SSX is critical for cyclin D1 expression in synovial sarcoma cells: a gain of function of the t(X;18)(p11.2;q11.2) translocation. Cancer Res 2002; 62: 3861-7. (Pubitemid 34728873)
24. Xie Y, Tornkvist M, Aalto Y, Nilsson G, Girnita L, Nagy B, Knuutila S, Larsson O,. Gene expression profile by blocking the SYT-SSX fusion gene in synovial sarcoma cells. Identification of XRCC4 as a putative SYT-SSX target gene. Oncogene 2003; 22: 7628-31. (Pubitemid 37464096)
25. Watanabe T, Tsuda M, Makino Y, Ichihara S, Sawa H, Minami A, Mochizuki N, Nagashima K, Tanaka S,. Adaptor molecule Crk is required for sustained phosphorylation of Grb2-associated binder 1 and hepatocyte growth factor-induced cell motility of human synovial sarcoma cell lines. Mol Cancer Res 2006; 4: 499-510. (Pubitemid 44197045)
26. Kawai A, Naito N, Yoshida A, Morimoto Y, Ouchida M, Shimizu K, Beppu Y,. Establishment and characterization of a biphasic synovial sarcoma cell line, SYO-1. Cancer Lett 2004; 204: 105-13. (Pubitemid 38117199)
27. Hartmann W, Kuchler J, Koch A, Friedrichs N, Waha A, Endl E, Czerwitzki J, Metzger D, Steiner S, Wurst P, Leuschner I, von Schweinitz D, et al. Activation of phosphatidylinositol-3′-kinase/AKT signaling is essential in hepatoblastoma survival. Clin Cancer Res 2009; 15: 4538-45.
28. Webb JL,. Effects of more than one inhibitor. In:, Webb JL, ed. Enzyme and metabolic inhibitors: general principles of inhibition, Vol. 1. New York: Academic Press, 1963. 487-512.
29. Hartmann W, Koch A, Brune H, Waha A, Schuller U, Dani I, Denkhaus D, Langmann W, Bode U, Wiestler OD, Schilling K, Pietsch T,. Insulin-like growth factor II is involved in the proliferation control of medulloblastoma and its cerebellar precursor cells. Am J Pathol 2005; 166: 1153-62. (Pubitemid 40524439)
30. Toral-Barza L, Zhang WG, Lamison C, Larocque J, Gibbons J, Yu K,. Characterization of the cloned full-length and a truncated human target of rapamycin: activity, specificity, and enzyme inhibition as studied by a high capacity assay. Biochem Biophys Res Commun 2005; 332: 304-10. (Pubitemid 40719487)
31. Scotlandi K, Manara MC, Nicoletti G, Lollini PL, Lukas S, Benini S, Croci S, Perdichizzi S, Zambelli D, Serra M, Garcia-Echeverria C, Hofmann F, et al. Antitumor activity of the insulin-like growth factor-I receptor kinase inhibitor NVP-AEW541 in musculoskeletal tumors. Cancer Res 2005; 65: 3868-76. (Pubitemid 40616368)
32. Manara MC, Nicoletti G, Zambelli D, Ventura S, Guerzoni C, Landuzzi L, Lollini PL, Maira SM, Garcia-Echeverria C, Mercuri M, Picci P, Scotlandi K,. NVP-BEZ235 as a new therapeutic option for sarcomas. Clin Cancer Res 2010; 16: 530-40.
33. Cao L, Yu Y, Darko I, Currier D, Mayeenuddin LH, Wan X, Khanna C, Helman LJ,. Addiction to elevated insulin-like growth factor I receptor and initial modulation of the AKT pathway define the responsiveness of rhabdomyosarcoma to the targeting antibody. Cancer Res 2008; 68: 8039-48.
34. Khan J, Bittner ML, Saal LH, Teichmann U, Azorsa DO, Gooden GC, Pavan WJ, Trent JM, Meltzer PS,. cDNA microarrays detect activation of a myogenic transcription program by the PAX3-FKHR fusion oncogene. Proc Natl Acad Sci USA 1999; 96: 13264-9.
35. Riggi N, Suva ML, Suva D, Cironi L, Provero P, Tercier S, Joseph JM, Stehle JC, Baumer K, Kindler V, Stamenkovic I,. EWS-FLI-1 expression triggers a Ewing's sarcoma initiation program in primary human mesenchymal stem cells. Cancer Res 2008; 68: 2176-85. (Pubitemid 351521790)
36. Cironi L, Riggi N, Provero P, Wolf N, Suva ML, Suva D, Kindler V, Stamenkovic I,. IGF1 is a common target gene of Ewing's sarcoma fusion proteins in mesenchymal progenitor cells. PLoS One 2008; 3: e2634.
37. Manara MC, Landuzzi L, Nanni P, Nicoletti G, Zambelli D, Lollini PL, Nanni C, Hofmann F, Garcia-Echeverria C, Picci P, Scotlandi K,. Preclinical in vivo study of new insulin-like growth factor-I receptor-specific inhibitor in Ewing's sarcoma. Clin Cancer Res 2007; 13: 1322-30. (Pubitemid 46424074)
38. Scotlandi K, Picci P,. Targeting insulin-like growth factor 1 receptor in sarcomas. Curr Opin Oncol 2008; 20: 419-27.
39. Kim SY, Toretsky JA, Scher D, Helman LJ,. The role of IGF-1R in pediatric malignancies. Oncologist 2009; 14: 83-91.
40. Hashemolhosseini S, Nagamine Y, Morley SJ, Desrivieres S, Mercep L, Ferrari S,. Rapamycin inhibition of the G1 to S transition is mediated by effects on cyclin D1 mRNA and protein stability. J Biol Chem 1998; 273: 14424-9. (Pubitemid 28319162)
41. Bozzi F, Ferrari A, Negri T, Conca E, Luca da R, Losa M, Casieri P, Orsenigo M, Lampis A, Meazza C, Casanova M, Pierotti MA, et al. Molecular characterization of synovial sarcoma in children and adolescents: evidence of akt activation. Transl Oncol 2008; 1: 95-101.
42. Dobashi Y, Suzuki S, Sato E, Hamada Y, Yanagawa T, Ooi A,. EGFR-dependent and independent activation of Akt/mTOR cascade in bone and soft tissue tumors. Mod Pathol 2009; 22: 1328-40.
43. Kawauchi S, Goto Y, Ihara K, Furuya T, Oga A, Tsuneyoshi M, Kawai S, Sasaki K,. Survival analysis with p27 expression and apoptosis appears to estimate the prognosis of patients with synovial sarcoma more accurately. Cancer 2002; 94: 2712-8. (Pubitemid 34478088)
44. Barretina J, Taylor BS, Banerji S, Ramos AH, Lagos-Quintana M, Decarolis PL, Shah K, Socci ND, Weir BA, Ho A, Chiang DY, Reva B, et al. Subtype-specific genomic alterations define new targets for soft-tissue sarcoma therapy. Nat Genet 2010; 42: 715-21.
45. Saito T, Oda Y, Kawaguchi K, Takahira T, Yamamoto H, Tanaka K, Matsuda S, Sakamoto A, Iwamoto Y, Tsuneyoshi M,. PTEN and other tumor suppressor gene mutations as secondary genetic alterations in synovial sarcoma. Oncol Rep 2004; 11: 1011-5.
46. Francis P, Namlos HM, Muller C, Eden P, Fernebro J, Berner JM, Bjerkehagen B, Akerman M, Bendahl PO, Isinger A, Rydholm A, Myklebost O, et al. Diagnostic and prognostic gene expression signatures in 177 soft tissue sarcomas: hypoxia-induced transcription profile signifies metastatic potential. BMC Genomics 2007; 8: 73.
47. Horvai AE, Kramer MJ, O'Donnell R,. Beta-catenin nuclear expression correlates with cyclin D1 expression in primary and metastatic synovial sarcoma: a tissue microarray study. Arch Pathol Lab Med 2006; 130: 792-8. (Pubitemid 43886997)
48. Baryawno N, Sveinbjornsson B, Eksborg S, Chen CS, Kogner P, Johnsen JI,. Small-molecule inhibitors of phosphatidylinositol 3-kinase/Akt signaling inhibit Wnt/beta-catenin pathway cross-talk and suppress medulloblastoma growth. Cancer Res 2010; 70: 266-76.
49. Datta SR, Dudek H, Tao X, Masters S, Fu H, Gotoh Y, Greenberg ME,. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 1997; 91: 231-41. (Pubitemid 27456390)
50. Krskova L, Kalinova M, Brizova H, Mrhalova M, Sumerauer D, Kodet R,. Molecular and immunohistochemical analyses of BCL2, KI-67, and cyclin D1 expression in synovial sarcoma. Cancer Genet Cytogenet 2009; 193: 1-8.