Cross talk of signals between EGFR and IL-6R through JAK2/STAT3 mediate epithelial-mesenchymal transition in ovarian carcinomas

British Journal of Cancer

Volumn 100, Issue 1, 2009, Pages 134-144

  Colomiere, M ^a,b   Ward, A C ^b   Riley, C ^a   Trenerry, M K ^b   Cameron Smith, D ^b   Findlay, J ^a,c   Ackland, L ^b   Ahmed, N ^a,d  

^a ROYAL WOMEN'S HOSPITAL   (Australia)

^b DEAKIN UNIVERSITY   (Australia)

^c HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

^d UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Epithelial; Janus kinase 2; Mesenchymal transition; Migration; Ovarian carcinoma; Signal transducer and activator of transcription 3

Indexed keywords

BETA CATENIN; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; INTERLEUKIN 6; INTERLEUKIN 6 ANTIBODY; INTERLEUKIN 6 RECEPTOR; JANUS KINASE 2; LEUKEMIA INHIBITORY FACTOR; N BENZYL 2 CYANO 3 (3,4 DIHYDROXYPHENYL)ACRYLAMIDE; NERVE CELL ADHESION MOLECULE; STAT3 PROTEIN; VIMENTIN;

ARTICLE; BENIGN TUMOR; CANCER CELL; CANCER GRADING; CELL MOTILITY; CELL STRUCTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MESENCHYMOMA; METASTASIS; OVARY; OVARY CARCINOMA; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TRANSITIONAL CELL CARCINOMA;

ANTIGENS, CD; BETA CATENIN; CADHERINS; CELL LINE, TUMOR; EPIDERMAL GROWTH FACTOR; EPITHELIAL CELLS; FEMALE; HUMANS; INTERLEUKIN-6; JANUS KINASE 2; LEUKEMIA INHIBITORY FACTOR; MESODERM; OVARIAN NEOPLASMS; RECEPTOR CROSS-TALK; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, INTERLEUKIN-6; STAT3 TRANSCRIPTION FACTOR; VIMENTIN;

EID: 58149218143     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/sj.bjc.6604794     Document Type: Article

References (46)

1. Ahmed N, Maines-Bandiera S, Quinn MA, Unger WG, Dedhar S, Auersperg N (2006) Molecular pathways regulating EGF-induced epithelio-mesenchymal transition in human ovarian surface epithelium. Am J Physiol Cell Physiol 290: C1532-C1542
2. Ahmed N, Pansino F, Clyde R, Murthi P, Quinn MA, Rice GE, Agrez MV, Mok S, Baker MS (2002b) Overexpression of alpha(v)beta6 integrin in serous epithelial ovarian cancer regulates extracellular matrix degradation via the plasminogen activation cascade. Carcinogenesis 23: 237-244
3. Ahmed N, Riley C, Oliva K, Rice G, Quinn M (2005) Ascites induces modulation of alpha6beta1 integrin and urokinase plasminogen activator receptor expression and associated functions in ovarian carcinoma. Br J Cancer 92: 1475-1485
4. Ahmed N, Riley C, Oliva K, Stutt E, Rice G, Quinn M (2003) Integrin-linked kinase expression increases with ovarian tumour grade and is sustained by peritoneal tumour fluid. J Pathol 201: 229-237
5. Ahmed N, Riley C, Rice GE, Quinn MA, Baker MS (2002a) Alpha(v)beta(6) integrin-A marker for the malignant potential of epithelial ovarian cancer. J Histochem Cytochem 50: 1371-1380
6. Ahmed N, Thompson EA, Quinn MA (2007) Epithelial-mesenchymal interconversions in normal ovarian epithelium and ovarian carcinomas: an exception to the norm. J of Cell Physiol 213/3: 501-508
7. Badache A, Hynes N (2001) Interleukin 6 inhibits proliferation and, in cooperation with an epidermal growth factor receptor autocrine loop, increases migration of T47D breast cancer cells. Cancer Res 61: 383-391
8. Bagnato A, Rosanò L (2007) Epithelial-mesenchymal transition in ovarian cancer progression: a crucial role for the endothelin axis. Cells Tissues Organs 185: 1-3
9. Blank SV, Chang R, Muggia F (2005) Epidermal growth factor receptor inhibitors for the treatment of epithelial ovarian cancer. Oncology 19/4: 553-559
10. Carbia-Nagashima A, Arzt E (2004) Intracellular proteins and mechanisms involved in the control of gp130/JAK/STAT cytokine signaling. IUBMB Life 56/2: 83-88
11. Chan KS, Carbajal S, Kiguchi K, Clifford J, Sano S, DiGiovanni J (2004) Epidermal growth factor receptor-mediated activation of Stat3 during multistage skin carcinogenesis. Cancer Res 64: 2382-2389
12. Chen CL, Loy A, Cen L, Chan C, Hsieh FC, Cheng G, Wu B, Qualman SJ, Kunisada K, Yamauchi-Takihara K, Lin J (2007) Signal transducer and activator of transcription 3 is involved in cell growth and survival of human rhabdomyosarcoma and osteosarcoma cells. BMC Cancer 7: 111
13. Colomiere M, Findlay J, Ackland L, Ahmed N (2008) Epidermal growth factor induced ovarian carcinoma cell migration is associated with JAK2/STAT3 signals and changes in the expression and abundance of alpha6beta1 integrin. Inter J Biochem Cell Biol 27 September 2008 [E-pub ahead of print]
14. Demir AY, Groothius P, Nap AW, Punyadeera C, de Goeij AF, Evers JL, Dunselman GA (2004) Menstrual effluent induces epithelial-mesenchymal transitions in mesothelial cells. Hum Reprod 19: 21-29
15. Ferrand A, Kowalski-Chauvel A, Bertrand C, Pradayrol L, Fourmy D, Dufresne M, Seva C (2004) Involvement of JAK2 upstream of the PI 3-kinase in cell-cell adhesion regulation by gastrin. Exp Cell Res 301: 128-138
16. Gao SP, Mark KG, Leslie K, Pao W, Motoi N, Gerald WL, Travis WD, Bornmann W, Veach D, Clarkson B, Bromberg JF (2007) Mutations in the EGFR kinase domain mediate STAT3 activation via IL-6 production in human lung adenocarcinomas. J Clin Invest 117: 3846-3856
17. Garcia R, Bowman TL, Niu G, Yu H, Minton S, Muro-Cacho CA, Cox CE, Falcone R, Fairclough R, Parsons S, Laudano A, Gazit A, Levitzki A, Kraker A, Jove R (2001) Constitutive activation of Stat3 by the Src and JAK tyrosine kinases participates in growth regulation of human breast carcinoma cells. Oncogene 20: 2499-2513
18. Hay ED, Zuk A (1995) Transformations between epithelium and mesenchyme: normal, pathological, and experimentally induced. Am J Kidney Dis 26: 678-690
19. Lebret SC, Newgreen D, Thompson EW, Ackland ML (2007) Induction of epithelial to mesenchymal transition in PMC42-LA human breast carcinoma cells by carcinoma-associated fibroblast secreted factors. Breast Cancer Res 9: R19
20. Levy DE, Darnell JE (2002) Stats: transcriptional control and biological impact. Nat Rev Mol Cell Biol 3: 651-662
21. Lim R, Ahmed N, Borregaard N, Riley C, Wafai R, Thompson EW, Quinn MA, Rice GE (2007) Neutrophil gelatinase-associated lipocalin (NGAL) an early-screening biomarker for ovarian cancer: NGAL is associated with epidermal growth factor-induced epithelio-mesenchymal transition. Int J Cancer 120: 2426-2434
22. Lo HW, Hsu SC, Xia W, Cao X, Shih JY, Wei Y, Abbruzzese JL, Hortobagyi GN, Hung MC (2007) Epidermal growth factor receptor cooperates with signal transducer and activator of transcription 3 to induce epithelial-mesenchymal transition in cancer cells via up-regulation of TWIST gene expression. Cancer Res 67: 9066-9076
23. Montell DJ (2003) Border cell migration: the race is on. Nat Rev Mol Cell Biol 4: 13-24
24. Nightingale J, Patel S, Suzuki N, Buxton R, Takagi KI, Suzuki J, Sumi Y, Imaizumi A, Mason RM, Zhang Z (2004) Oncostatin M, a cytokine released by activated mononuclear cells, induces epithelial cell-myofibroblast transdifferentiation via Jak/Stat pathway activation. J Am Soc Nephrol 15: 21-32
25. Polette M, Mestdagt M, Bindels S, Nawrocki-Raby B, Hunziker W, Foidart JM, Birembaut P, Gilles C (2007) Beta-catenin and ZO-1: shuttle molecules involved in tumor invasion-associated epithelial-mesenchymal transition processes. Cells Tissues Organs 185: 61-65
26. Psyrri AK, Kassar M, Yu Z, Bamias A, Weinberger PM, Markakis S, Kowalski D, Camp RL, Rimm DL, Dimopoulos MA (2005) Effect of epidermal growth factor receptor expression level on survival in patients with epithelial ovarian cancer. Clin Cancer Res 15/11: 8637-8643
27. Puiffe ME, Le Page C, Mouhim AF, Ziestarska M, Quellet V, Tonin PN, Chevrette M, Provencher DM, Mes-Masson AM (2007) Characterization of ovarian cancer ascites on cell invasion, proliferation, spheroid formation, and gene expression in an in vitro model of epithelial ovarian cancer. Neoplasia 9/10: 820-829
28. Rosanò L, Di Castro V, Spinella F, Tortora G, Nicotra MR, Natali PG, Bagnato A (2007) Combined targeting of endothelin A receptor and epidermal growth factor receptor in ovarian cancer shows enhanced antitumor activity. Cancer Res 67/13: 6351-6359
29. Rosen DG, Mercado-Uribe I, Yang G, Bast Jr RC, Amin HM, Lai R, Liu J (2006) The role of constitutively active signal transducer and activator of transcription 3 in ovarian tumorigenesis and prognosis. Cancer 107: 2730-2740
30. Sano S, Itami S, Takeda K, Tarutani M, Yamaguchi Y, Miura H, Yoshikawa K, Akira S, Takeda J (1999) Keratinocyte-specific ablation of Stat3 exhibits impaired skin remodeling, but does not affect skin morphogenesis. EMBO J 18: 4657-4668
31. Silver DL, Montell DJ (2001) Paracrine signaling through the JAK/STAT pathway activates invasive behavior of ovarian epithelial cells in Drosophila. Cell 107: 831-841
32. Silver DL, Naora H, Liu J, Cheng W, Montell DJ (2004) Activated signal transducer and activator of transcription (STAT) 3: localization in focal adhesions and function in ovarian cancer cell motility. Cancer Res 64: 3550-3556
33. Silverberg SG (2000) Histopathologic grading of ovarian carcinoma: a review and proposal. Int J Gynecol Pathol 19: 7-15
34. Sriuranpong V, Park JI, Amornphimoltham P, Patel V, Nelkin BD, Gutkind JS (2003) Epidermal growth factor receptor-independent constitutive activation of STAT3 in head and neck squamous cell carcinoma is mediated by the autocrine/paracrine stimulation of the interleukin 6/gp130 cytokine system. Cancer Res 63: 2948-2956
35. Takeda K, Noguchi K, Shi W, Tanaka T, Matsumoto M, Yoshida N, Kishimoto T, Akira S (1997) Targeted disruption of the mouse Stat3 gene leads to early embryonic lethality. Proc Natl Acad Sci USA 94: 3801-3804
36. Tanaka T, Saika S, Ohnishi Y, Ooshima A, McAvoy JW, Liu CY, Azhar M, Doetschman T, Kao WW (2004) Fibroblast growth factor 2: roles of regulation of lens cell proliferation and epithelial-mesenchymal transition in response to injury. Mol Vis 15: 462-467
37. Taylor KM, Hiscox S, Nicholson RI (2004) Zinc transporter LIV-1: a link between cellular development and cancer progression. Trends Endocrinol Metab 15: 461-463
38. Teng CB, Diao HL, Ma XH, Xu LB, Yang ZM (2004) Differential expression and activation of Stat3 during mouse embryo implantation and decidualization. Mol Reprod Dev 69/1: 1-10
39. Theriault BL, Shepherd TG, Mujoomdar ML, Nachtigal MW (2007) BMP4 induces EMT and Rho GTPase activation in human ovarian cancer cells. Carcinogenesis 28: 1153-1162
40. Thomas SM, Grandis JR, Wentzel AL, Gooding WE, Lui VW, Siegfried JM (2005) Gastrin-releasing peptide receptor. Neoplasia 7: 426-431
41. Todd MS, Campbell CL, McQuain C, Mitchell K, Guardiani R, Quesenberry P, Nelson B (2002) Coexpression of oncostatin M and its receptors and evidence for STAT3 activation in human ovarian carcinomas. Cytokine 17/6: 324-334
42. Trenerry MK, Carey KA, Ward AC, Cameron-Smith D (2007) STAT3 signaling is activated in human skeletal muscle following acute resistance exercise. J Appl Physiol 102: 1483-1489
43. Wang FQ, So J, Reierstad S, Fishman DA (2006) Vascular endothelial growth factor-regulated ovarian cancer invasion and migration involves expression and activation of matrix metalloproteinases. Int J Cancer 118: 879-888
44. Yamashita S, Miyagi C, Carmany-Rampey A, Shimizu T, Fujii R, Schier AF, Hirano T (2002) Stat3 controls cell movements during zebrafish gastrulation. Dev Cell 2: 363-375
45. Yarden Y, Shilo BZ (2007) SnapShot: EGFR signaling pathway Cell 131(5): 1018
46. Yip SC, El-Sibai M, Coniglio SJ, Mouneimne G, Eddy RJ, Drees BE, Neilsen PO, Goswami S, Symons M, Condeelis JS, Backer JM (2007) The distinct roles of Ras and Rac in PI3-kinase-dependent protrusion during EGF-stimulated cell migration. J Cell Sci 120: 3138-3146