STAT3 expression, activity and functional consequences of STAT3 inhibition in esophageal squamous cell carcinomas and Barrett's adenocarcinomas

Oncogene

Volumn 33, Issue 25, 2014, Pages 3256-3266

  Timme, S ^a   Ihde, S ^a   Fichter, C D ^a,b   Waehle, V ^a   Bogatyreva, L ^b   Atanasov, K ^a   Kohler, I ^a   Schopflin A ^a   Geddert, H ^c   Faller, G ^c   Klimstra, D ^d   Tang, L ^d   Reinheckel, T ^a,b   Hauschke, D ^b   Busch, H ^b,e   Boerries, M ^b,e   Werner, M ^a,e   Lassmann, S ^a,b,e  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c St Vincentius Kliniken   (Germany)

^d MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^e GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

cell migration; cell proliferation; esophageal cancer; inhibition; STAT3

Indexed keywords

EPIDERMAL GROWTH FACTOR; STAT1 PROTEIN; STAT3 PROTEIN; STAT5 PROTEIN; TRANSCRIPTOME; TYROSINE;

ARTICLE; BARRETT ESOPHAGUS; CANCER CELL; CELL FUNCTION; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CTHRC1 GENE; DOWN REGULATION; ESOPHAGEAL ADENOCARCINOMA; ESOPHAGEAL SQUAMOUS CELL CARCINOMA; GENE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SHROOM2 GENE; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; UPREGULATION;

ADENOCARCINOMA; BARRETT ESOPHAGUS; CARCINOMA, SQUAMOUS CELL; CELL CYCLE; CELL GROWTH PROCESSES; CELL LINE, TUMOR; CELL MOVEMENT; DOWN-REGULATION; ESOPHAGEAL NEOPLASMS; GENE KNOCKDOWN TECHNIQUES; HUMANS; PHOSPHORYLATION; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; UP-REGULATION;

EID: 84903318074     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.298     Document Type: Article

References (52)

1. Jove R. Preface: STAT signaling. Oncogene 2000; 19: 2466-2467.
2. Bromberg J. Stat proteins and oncogenesis. J Clin Invest 2002; 109: 1139-1142.
3. Vinkemeier U. Getting the message across, STAT! design principles of a molecular signaling circuit. J Cell Biol 2004; 167: 197-201.
4. Yu H, Pardoll D, Jove R. STATs in cancer inflammation and immunity: a leading role for STAT3. Nat Rev Cancer 2009; 9: 798-809.
5. Aggarwal BB, Kunnumakkara AB, Harikumar KB, Gupta SR, Tharakan ST, Koca C et al. Signal transducer and activator of transcription-3, inflammation, and cancer: how intimate is the relationship? Ann NY Acad Sci 2009; 1171: 59-76.
6. Sansone P, Bromberg J. Targeting the interleukin-6/Jak/stat pathway in human malignancies. J Clin Oncol 2012; 30: 1005-1014.
7. Haura EB, Zheng Z, Song L, Cantor A, Bepler G. Activated epidermal growth factor receptor-Stat-3 signaling promotes tumor survival in vivo in non-small cell lung cancer. Clin Cancer Res 2005; 11: 8288-8294.
8. Jiang R, Jin Z, Liu Z, Sun L, Wang L, Li K. Correlation of activated STAT3 expression with clinicopathologic features in lung adenocarcinoma and squamous cell carcinoma. Mol Diagn Ther 2011; 15: 347-352.
9. Seethala RR, Gooding WE, Handler PN, Collins B, Zhang Q, Siegfried JM, Grandis JR. Immunohistochemical analysis of phosphotyrosine signal transducer and activator of transcription 3 and epidermal growth factor receptor autocrine signaling pathways in head and neck cancers and metastatic lymph nodes. Clin Cancer Res 2008; 14: 1303-1309.
10. Gong W, Wang L, Yao JC, Ajani JA, Wei D, Aldape KD et al. Expression of activated signal transducer and activator of transcription 3 predicts expression of vascular endothelial growth factor in and angiogenic phenotype of human gastric cancer. Clin Cancer Res 2005; 11: 1386-1393.
11. Lee J, Kang WK, Park JO, Park SH, Park YS, Lim HY et al. Expression of activated signal transducer and activator of transcription 3 predicts poor clinical outcome in gastric adenocarcinoma. APMIS 2009; 117: 598-606.
12. Lassmann S, Schuster I, Walch A, Gö bel H, Jü tting U, Makowiec F et al. STAT3 mRNA and protein expression in colorectal cancer: effects on STAT3-inducible targets linked to cell survival and proliferation. J Clin Pathol 2007; 60: 173-179.
13. Morikawa T, Baba Y, Yamauchi M, Kuchiba A, Nosho K, Shima K et al. STAT3 expression, molecular features, inflammation patterns, and prognosis in a database of 724 colorectal cancers. Clin Cancer Res 2011; 17: 1452-1462.
14. Zhao W, Jaganathan S, Turkson J. A cell-permeable Stat3 SH2 domain mimetic inhibits Stat3 activation and induces antitumor cell effects in vitro. J Biol Chem 2010; 285: 35855-35865.
15. Leong PL, Andrews GA, Johnson DE, Dyer KF, Xi S, Mai JC et al. Targeted inhibition of Stat3 with a decoy oligonucleotide abrogates head and neck cancer cell growth. Proc Natl Acad Sci USA 2003; 100: 4138-4143.
16. Souissi I, Najjar I, Ah-Koon L, Schischmanoff PO, Lesage D, Le Coquil S et al. A STAT3-decoy oligonucleotide induces cell death in a human colorectal carcinoma cell line by blocking nuclear transfer of STAT3 and STAT3-bound NF-kB. BMC Cell Biol 2011; 12: 14.
17. Boehm AL, Sen M, Seethala R, Gooding WE, Freilino M, Wong SM et al. Combined targeting of epidermal growth factor receptor, signal transducer and activator of transcription-3, and Bcl-X(L) enhances antitumor effects in squamous cell carcinoma of the head and neck. Mol Pharmacol 2008; 73: 1632-1642.
18. Bonner JA, Yang ES, Trummell HQ, Nowsheen S, Willey CD, Raisch KP. Inhibition of STAT-3 results in greater cetuximab sensitivity in head and neck squamous cell carcinoma. Radiother Oncol 2011; 99: 339-343.
19. Jaganathan S, Yue P, Turkson J. Enhanced sensitivity of pancreatic cancer cells to concurrent inhibition of aberrant signal transducer and activator of transcription 3 and epidermal growth factor receptor or Src. J Pharmacol Exp Ther 2010; 333: 373-381.
20. Nagaraj NS, Washington MK, Merchant NB. Combined blockade of Src kinase and epidermal growth factor receptor with gemcitabine overcomes STAT3-mediated resistance of inhibition of pancreatic tumor growth. Clin Cancer Res 2011; 17: 483-493.
21. Gabbert HE, Nakamura Y, Shimoda T, Field YK, Hainaut P, Inoue H. Esophageal squamous cell carcinomas. In: Bosman FT, Carneiro F, Hruban RH, Theise ND (eds.) WHO Classification of Tumours. Volume 3. (IARC Press, Lyon, France).
22. Werner M, Lambert R, Flejou JF, Keller G, Hainaut P, Stein HJ, Hö fler H. Adenocarcinoma of the esophagus. In: Bosman FT, Carneiro F, Hruban RH, Theise ND (eds.) WHO Classification of Tumours. Volume 3. (IARC Press, Lyon, France).
23. Pennathur A, Gibson MK, Jobe BA, Luketich JD. Oesophageal carcinoma. Lancet 2013; 381: 400-412.
24. Andl CD, Mizushima T, Oyama K, Bowser M, Nakagawa H, Rustgi AK. EGFR-induced cell migration is mediated predominantly by the JAK-STAT pathway in primary esophageal keratinocytes. Am J Physiol Gastrointest Liver Physiol 2004; 287: G1227-G1237.
25. Dvorak K, Chavarria M, Payne CM, Ramsey L, Crowley-Weber C, Dvorakova B et al. Activation of the interleukin-6/STAT3 antiapoptotic pathway in esophageal cells by bile acids and low pH: relevance to barrett's esophagus. Clin Cancer Res 2007; 13: 5305-5313.
26. Zhang HY, Zhang Q, Zhang X, Yu C, Huo X, Cheng E et al. Cancer-related inflammation and Barrett's carcinogenesis: interleukin-6 and STAT3 mediate apoptotic resistance in transformed Barrett's cells. Am J Physiol Gastrointest Liver Physiol 2011; 300: G454-G460.
27. Zhang Y, Du XL, Wang CJ, Lin DC, Ruan X, Feng YB et al. Reciprocal activation between plk1 and stat3 contributes to survival and proliferation of esophageal cancer cells. Gastroenterology 2011; 142: 521-530.
28. Yan S, Zhou C, Zhang W, Zhang G, Zhao X, Yang S et al. beta-Catenin/TCF pathway upregulates STAT3 expression in human esophageal squamous cell carcinoma. Cancer Lett 2008; 271: 85-97.
29. Reiser J, Adair B, Reinheckel T. Specialized roles for cysteine cathepsins in health and disease. J Clin Invest 2010; 120: 3421-3431.
30. Kreuzaler PA, Staniszewska AD, Li W, Omidvar N, Kedjouar B, Turkson J et al. Stat3 controls lysosomal-mediated cell death in vivo. Nat Cell Biol 2011; 13: 303-309.
31. Boonstra JJ, van Marion R, Beer DG, Lin L, Chaves P, Ribeiro C et al. Verification and unmasking of widely used human esophageal adenocarcinoma cell lines. J Natl Cancer Inst 2010; 102: 271-274.
32. Fichter CD, Herz C, Münch C, Opitz OG, Werner M, Lassmann S. Occurrence of multipolar mitoses and association with Aurora-A/-B kinases and p53 mutations in aneuploid esophageal carcinoma cells. BMC Cell Biol 2011; 12: 13.
33. Herz C, Schlü rmann F, Batarello D, Fichter CD, Schö pflin A, Münch C et al. Occurrence of Aurora A positive multipolar mitoses in distinct molecular classes of colorectal carcinomas and effect of Aurora A inhibition. Mol Carcinog 2012; 51: 696-710.
34. Luo W, Friedman MS, Shedden K, Hankenson KD, Woolf PJ. GAGE: generally applicable gene set enrichment for pathway analysis. BMC Bioinformatics 2009; 27(10): 161.
35. Park EH, Kim S, Jo JY, Kim SJ, Hwang Y, Kim JM et al. Collagen triple helix repeat containing-1 promotes pancreatic cancer progression by regulating migration and adhesion of tumor cells. Carcinogenesis 2013; 34: 694-702.
36. Etournay R, Zwaenepoel I, Perfettini I, Legrain P, Petit C, El-Amraoui A. Shroom2, a myosin-VIIa-and actin-binding protein, directly interacts with ZO-1 at tight junctions. J Cell Sci 2007; 120: 2838-2850.
37. Farber MJ, Rizaldy R, Hildebrand JD. Shroom2 regulates contractility to control endothelial morphogenesis. Mol Biol Cell 2011; 22: 795-805.
38. Hanawa M, Suzuki S, Dobashi Y, Yamane T, Kono K, Enomoto N, Ooi A. EGFR protein overexpression and gene amplification in squamous cell carcinomas of the esophagus. Int J Cancer 2006; 118: 1173-1180.
39. Yu WW, Guo YM, Zhu M, Cai XW, Zhu ZF, Zhao WX, Fu XL. Clinicopathological and prognostic significance of EGFR over-expression in esophageal squamous cell carcinoma: a meta-analysis. Hepatogastroenterology 2011; 58: 426-431.
40. Rauser S, Weis R, Braselmann H, Feith M, Stein HJ, Langer R et al. Significance of HER2 low-level copy gain in Barrett's cancer: implications for fluorescence in situ hybridization testing in tissues. Clin Cancer Res 2007; 13: 5115-5123.
41. Yoon HH, Shi Q, Sukov WR, Wiktor AE, Khan M, Sattler CA et al. Association of HER2/ErbB2 expression and gene amplification with pathologic features and prognosis in esophageal adenocarcinomas. Clin Cancer Res 2012; 18: 546-554.
42. Reipschlaeger S, Kubatzky K, Taromi S, Burger M, Orth J, Aktories K, Schmidt G. Toxin-induced RhoA activity mediates CCL1-triggered STAT signaling. J Biol Chem 2012; 287: 11183-11194.
43. Tischoff I, Hengge UR, Vieth M, Ell C, Stolte M, Weber A, Schmidt WE, Tannapfel A. Methylation of SOCS-3 and SOCS-1 in the carcinogenesis of Barrett's adenocarcinoma. Gut 2007; 56: 1047-1053.
44. Sobin LH, Gospodarowicz MK, Wittekind C (eds) TNM Classification of Malignant Tumours. 7th Edn (Wiley-Blackwell, UICC, Geneva, Switzerland, 2009).
45. Khoury JD, Medeiros LJ, Rassidakis GZ, Yared MA, Tsioli P, Leventaki V et al. Differential expression and clinical significance of tyrosine- phosphorylated STAT3 in ALK\+ and ALK-anaplastic large cell lymphoma. Clin Cancer Res 2003; 9: 3692-3699.
46. Nasr MR, Laver JH, Chang M, Hutchison RE. Expression of anaplastic lymphoma kinase, tyrosine-phosphorylated STAT3, and associated factors in pediatric anaplastic large cell lymphoma: A report from the children's oncology group. Am J Clin Pathol 2007; 127: 770-778.
47. Gerlach U, Kayser G, Walch A, Hopt U, Schulte-Mö nting J, Werner M, Lassmann S. Centrosome-, chromosomal-passenger-and cell-cycle-associated mRNAs are differentially regulated in the development of sporadic colorectal cancer. J Pathol 2006; 208: 462-472.
48. Lassmann S, Danciu M, Mü ller M, Weis R, Makowiec F, Schulte-Mö nting J et al. Aurora A is differentially expressed and regulated in chromosomal and microsatellite instable sporadic colorectal cancers. Mod Pathol 2009; 22: 1385-1397.
49. Lassmann S, Kreutz C, Schoepflin A, Hopt U, Timmer J, Werner M. A novel approach for reliable microarray analysis of microdissected tumor cells from formalin-fixed and paraffin-embedded colorectal cancer resection specimens. J Mol Med 2009; 87: 211-224.
50. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001; 25: 402-408.
51. Kamburov A, Stelzl U, Lehrach H, Herwig R. The ConsensusPathDB interaction database: 2013 update. Nucleic Acids Res 2013; 41: D793-D800.
52. Boerries M, Grahammer F, Eiselein S, Buck M, Meyer C, Goedel M et al. Molecular fingerprinting of the podocyte reveals novel gene and protein regulatory networks. Kidney Int 2013; 83: 1052-1064.