Sensitivity of human granulosa cell tumor cells to epidermal growth factor receptor inhibition

Journal of Molecular Endocrinology

Volumn 52, Issue 2, 2014, Pages 223-234

  Andersson, Noora ^a   Anttonen, Mikko ^a,b   Färkkilä, Anniina ^a,b   Pihlajoki, Marjut ^a   Butzow, Ralf ^b   Unkila Kallio, Leila ^b   Heikinheimo, Markku ^a,c  

^a UNIVERSITY OF HELSINKI AND HELSINKI UNIVERSITY HOSPITAL   (Finland)

^b HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^c ST LOUIS CHILDREN S HOSPITAL   (United States)

Author keywords

Apoptosis; Cell viability; Epidermal growth factor receptor (EGFR) inhibition; Granulosa cell tumor (GCT); Ovary

Indexed keywords

ACTIN; CASPASE 3; CASPASE 7; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; ERLOTINIB; GEFITINIB; LAPATINIB; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN KINASE B;

APOPTOSIS ASSAY; ARTICLE; CELL PROLIFERATION; CELL VIABILITY; COPY NUMBER VARIATION; ENZYME ACTIVATION; FEMALE; GENE DOSAGE; GENE EXPRESSION; GRANULOSA CELL TUMOR; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; TISSUE MICROARRAY; WESTERN BLOTTING;

APOPTOSIS; CELL VIABILITY; EPIDERMAL GROWTH FACTOR RECEPTOR (EGFR) INHIBITION; GRANULOSA CELL TUMOR (GCT); OVARY;

ADULT; APOPTOSIS; CASPASE 3; CASPASE 7; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SCREENING ASSAYS, ANTITUMOR; ENZYME ACTIVATION; GENE DOSAGE; GENE EXPRESSION REGULATION, NEOPLASTIC; GRANULOSA CELL TUMOR; HUMANS; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RNA, MESSENGER;

EID: 84897894034     PISSN: 09525041     EISSN: 14796813     Source Type: Journal    
DOI: 10.1530/JME-13-0286     Document Type: Article

References (57)

1. Al-Agha OM, Huwait HF, Chow C, Yang W, Senz J, Kalloger SE, Huntsman DG, Young RH & Gilks CB 2011 FOXL2 is a sensitive and specific marker for sex cord-stromal tumors of the ovary. American Journal of Surgical Pathology 35 484-494. (doi:10.1159/ 000334649)
2. Algars A, Lintunen M, Carpen O, Ristamaki R & Sundstrom J 2011 EGFR gene copy number assessment from areas with highest EGFR expression predicts response to anti-EGFR therapy in colorectal cancer. British Journal of Cancer 105 255-262. (doi:10.1016/j.cyto. 2009.01.001)
3. Anttonen M, Unkila-Kallio L, Leminen A, Butzow R & Heikinheimo M 2005 High GATA-4 expression associates with aggressive behavior, whereas low anti-Müllerian hormone expression associates with growth potential of ovarian granulosa cell tumors. Journal of Clinical Endocrinology and Metabolism 90 6529-6535. (doi:10.1159/ 000318292)
4. Benayoun BA, Anttonen M, L'Hote D, Bailly-Bechet M, Andersson N, Heikinheimo M & Veitia RA 2012 Adult ovarian granulosa cell tumor transcriptomics: prevalence of FOXL2 target genes misregula-tion gives insights into the pathogenic mechanism of the p.Cys134Trp somatic mutation. Oncogene 32 2739-2746. (doi:10.1681/ASN. 2004090742)
5. Biswas DK, Cruz AP, Gansberger E & Pardee AB 2000 Epidermal growth factor-induced nuclear factor kB activation: a major pathway of cell-cycle progression in estrogen-receptor negative breast cancer cells. PNAS 97 8542-8547. (doi:10.1007/s10735-008-9198-6)
6. Bittinger S, Alexiadis M & Fuller PJ 2009 Expression status and mutational analysis of the PTEN and P13K subunit genes in ovarian granulosa cell tumors. International Journal of Gynecological Cancer 19 339-342. (doi:10.1002/jcp.22726)
7. Campiglio M, Locatelli A, Olgiati C, Normanno N, Somenzi G, Vigano L, Fumagalli M, Menard S & Gianni L 2004 Inhibition of proliferation and induction of apoptosis in breast cancer cells by the epidermal growth factor receptor (EGFR) tyrosine kinase inhibitor ZD1839 ('iressa') is independent of EGFR expression level. Journal of Cellular Physiology 198 259-268. (doi:10.1002/jcp.10411)
8. Chong CR & Janne PA 2013 The quest to overcome resistance to EGFR-targeted therapies in cancer. Nature Medicine 19 1389-1400. (doi:10.14310/horm.2002.1345)
9. Chu S, Nishi Y, Yanase T, Nawata H & Fuller PJ 2004 Transrepression of estrogen receptor b signaling by nuclear factor-kb in ovarian granulosa cells. Molecular Endocrinology 18 1919-1928. (doi:10.1007/s00125-004-1597-y)
10. Dietel M, Ellis IO, Hofler H, Kreipe H, Moch H, Dankof A, Kolble K & Kristiansen G 2007 Comparison of automated silver enhanced in situ hybridisation (SISH) and fluorescence ISH (FISH) for the validation of HER2 gene status in breast carcinoma according to the guidelines of the American Society of Clinical Oncology and the College of American Pathologists. Virchows Archiv 451 19-25. (doi:10.2337/diabetes.55.02.06. db05-1064)
11. Dutta PR & Maity A 2007 Cellular responses to EGFR inhibitors and their relevance to cancer therapy. Cancer Letters 254 165-177. (doi:10.2337/ db09-0204)
12. Farkkila A, Anttonen M, Pociuviene J, Leminen A, Butzow R, Heikinheimo M & Unkila-Kallio L 2011 Vascular endothelial growth factor (VEGF) and its receptor VEGFR-2 are highly expressed in ovarian granulosa cell tumors. European Journal of Endocrinology 164 115-122. (doi:10.1152/ajprenal.00137.2012)
13. Farkkilä A, Andersson N, Butzow R, Leminen A, Heikinheimo M, Anttonen M & Unkila-Kallio L 2014 HER2 and GATA4 are New Prognostic Factors for Early-Stage Ovarian Granulosa Cell Tumor A Long-term Follow-up study. Cancer Medicine [in press].
14. Fuller PJ, Chu S, Fikret S & Burger HG 2002 Molecular pathogenesis of granulosa cell tumours. Molecular and Cellular Endocrinology 191 89-96. (doi:10.1007/s00125-005-1850-z)
15. Furger C, Fiddes RJ, Quinn DI, Bova RJ, Daly RJ & Sutherland RL 1998 Granulosa cell tumors express erbB4 and are sensitive to the cytotoxic action of heregulin-b2/PE40. Cancer Research 58 1773-1778. (doi:10.1507/endocrj.K06-016)
16. Gershon R, Aviel-Ronen S, Korach J, Daniel-Carmi V, Avivi C, Bar-Ilan D, Barshack I, Meirow D, Ben-Baruch G & Cohen Y 2011 FOXL2 C402G mutation detection using MALDI-TOF-MS in DNA extracted from Israeli granulosa cell tumors. Gynecologic Oncology 122 580-584. (doi:10.1161/01.HYP.0000078490.59735.6E)
17. Glaysher S, Bolton LM, Johnson P, Atkey N, Dyson M, Torrance C & Cree IA 2013 Targeting EGFR and PI3K pathways in ovarian cancer. British Journal of Cancer 109 1786-1794. (doi:10.1097/00004872-200410000-00021)
18. Gullick WJ 1991 Prevalence of aberrant expression of the epidermal growth factor receptor in human cancers. British Medical Bulletin 47 87-98.
19. Henson ES & Gibson SB 2006 Surviving cell death through epidermal growth factor (EGF) signal transduction pathways: implications for cancer therapy. Cellular Signalling 18 2089-2097. (doi:10.2337/ db08-1750)
20. Jamieson S & Fuller PJ 2012 Molecular pathogenesis of granulosa cell tumors of the ovary. Endocrine Reviews 33 109-144. (doi:10.1111/ j.1440-1797.2008.01047.x)
21. Jamieson S, Alexiadis M & Fuller PJ 2004 Expression status and mutational analysis of the ras and B-raf genes in ovarian granulosa cell and epithelial tumors. Gynecologic Oncology 95 603-609. (doi:10.1161/ 01.ATV.20.6.1595)
22. Jamieson S, Butzow R, Andersson N, Alexiadis M, Unkila-Kallio L, Heikinheimo M, Fuller PJ & Anttonen M 2010 The FOXL2 C134W mutation is characteristic of adult granulosa cell tumors of the ovary. Modern Pathology 23 1477-1485. (doi:10.1530/eje.1.01930)
23. Janne PA 2003 The role of epidermal growth factor receptor in advanced non-small cell lung carcinoma. Annals of Medicine 35 450-457. (doi:10.1016/j.ejphar.2013.03.024)
24. Jost M, Kari C & Rodeck U 2000 The EGF receptor - an essential regulator of multiple epidermal functions. European Journal of Dermatology 10 505-510. (doi:10.1038/ki.2012.408)
25. Kim MS, Hur SY, Yoo NJ & Lee SH 2010a Mutational analysis of FOXL2 codon 134 in granulosa cell tumour of ovary and other human cancers. Journal of Pathology 221 147-152. (doi:10.1681/ASN. 2006010097)
26. Kim T, Sung CO, Song SY, Bae DS & Choi YL 2010b FOXL2 mutation in granulosa-cell tumours of the ovary. Histopathology 56 408-410. (doi:10.1038/ki.2008.201)
27. King LA, Okagaki T, Gallup DG, Twiggs LB, Messing MJ & Carson LF 1996 Mitotic count, nuclear atypia, and immunohistochemical determination of ki-67, c-myc, p21-ras, c-erbB2, and p53 expression in granulosa cell tumors of the ovary: mitotic count and ki-67 are indicators of poor prognosis. Gynecologic Oncology 61 227-232. (doi:10.1016/j.jdiacomp. 2013.06.008)
28. Kyronlahti A, Kauppinen M, Lind E, Unkila-Kallio L, Butzow R, Klefstrom J, Wilson DB, Anttonen M & Heikinheimo M 2010 GATA4 protects granulosa cell tumors from TRAIL-induced apoptosis. Endocrine-Related Cancer 17 709-717. (doi:10.3109/00365513.2012.668928)
29. Lassus H, Leminen A, Vayrynen A, Cheng G, Gustafsson JA, Isola J & Butzow R 2004 ERBB2 amplification is superior to protein expression status in predicting patient outcome in serous ovarian carcinoma. Gynecologic Oncology 92 31-39. (doi:10.1007/s11255-011-0118-4)
30. Leibl S, Bodo K, Gogg-Kammerer M, Hrzenjak A, Petru E, Winter R, Denk H & Moinfar F 2006 Ovarian granulosa cell tumors frequently express EGFR (her-1), her-3, and her-4: an immunohistochemical study. Gynecologic Oncology 101 18-23. (doi:10.5935/0101-2800. 20120007)
31. Lo HW, Xia W, Wei Y, Ali-Seyed M, Huang SF & Hung MC 2005 Novel prognostic value of nuclear epidermal growth factor receptor in breast cancer. Cancer Research 65 338-348. (doi:10.1016/S0140-6736 (05)67667-2)
32. McCubrey JA, Steelman LS, Chappell WH, Abrams SL, Wong EW, Chang F, Lehmann B, Terrian DM, Milella M, Tafuri A et al. 2007 Roles of the raf/MEK/ERK pathway in cell growth, malignant transformation and drug resistance. Biochimica et Biophysica Acta 1773 1263-1284. (doi:10.1159/000345919)
33. Merras-Salmio L, Vettenranta K, Mottonen M & Heikinheimo M 2002 Ovarian granulosa cell tumors in childhood. Pediatric Hematology and Oncology 19 145-156. (doi:10.1159/000096870)
34. Miller K & McCluggage WG 2008 Prognostic factors in ovarian adult granulosa cell tumour. Journal of Clinical Pathology 61 881-884. (doi:10.1093/cvr/cvp415)
35. Nishi Y, Yanase T, Mu Y, Oba K, Ichino I, Saito M, Nomura M, Mukasa C, Okabe T, Goto K et al. 2001 Establishment and characterization of a steroidogenic human granulosa-like tumor cell line, KGN, that expresses functional follicle-stimulating hormone receptor. Endocrinology 142 437-445. (doi:10.1016/j.bbrc.2004.02.032)
36. Nofech-Mozes S, Ismiil N, Dube V, Saad RS, Khalifa MA, Moshkin O & Ghorab Z 2012 Immunohistochemical characterization of primary and recurrent adult granulosa cell tumors. International Journal of Gynecological Pathology 31 80-90. (doi:10.1152/ajprenal. 00278.2006)
37. Normanno N, Bianco C, Strizzi L, Mancino M, Maiello MR, De Luca A, Caponigro F & Salomon DS 2005 The ErbB receptors and their ligands in cancer: an overview. Current Drug Targets 6 243-257. (doi:10.1210/ jc.2003-031916)
38. Noro R, Gemma A, Kosaihira S, Kokubo Y, Chen M, Seike M, Kataoka K, Matsuda K, Okano T, Minegishi Y et al. 2006 Gefitinib (IRESSA) sensitive lung cancer cell lines show phosphorylation of akt without ligand stimulation. BMC Cancer 6 277. (doi:10.1038/ki.2012.421)
39. Nosov V, Silva I, Tavassoli F, Adamyan L, Farias-Eisner R & Schwartz PE 2009 Predictors of recurrence of ovarian granulosa cell tumors. International Journal of Gynecological Cancer 19 628-633. (doi:10.1681/ ASN.2006040331)
40. Palayekar MJ & Herzog TJ 2008 The emerging role of epidermal growth factor receptor inhibitors in ovarian cancer. International Journal of Gynecological Cancer 18 879-890. (doi:10.1038/sj.ki.5002516)
41. Park JY, Su YQ, Ariga M, Law E, Jin SL & Conti M 2004 EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 303 682-684. (doi:10.1258/ebm.2011.010218)
42. Pectasides D, Pectasides E & Psyrri A 2008 Granulosa cell tumor of the ovary. Cancer Treatment Reviews 34 1-12. (doi:10.2337/dc10-0739)
43. Prigent SA, Lemoine NR, Hughes CM, Plowman GD, Selden C & Gullick WJ 1992 Expression of the c-erbB-3 protein in normal human adult and fetal tissues. Oncogene 7 1273-1278. (doi:10.1111/cen.12041)
44. Qu J, Nisolle M & Donnez J 2000 Expression of transforming growth factor-a, epidermal growth factor, and epidermal growth factor receptor in follicles of human ovarian tissue before and after cryopreservation. Fertility and Sterility 74 113-121. (doi:10.1161/ ATVBAHA.107.147645)
45. Schrader KA, Gorbatcheva B, Senz J, Heravi-Moussavi A, Melnyk N, Salamanca C, Maines-Bandiera S, Cooke SL, Leung P, Brenton JD et al. 2009 The specificity of the FOXL2 c.402COG somatic mutation: a survey of solid tumors. PLoS ONE 4 e7988. (doi:10.2169/internal-medicine.47.0614)
46. Schumer ST & Cannistra SA 2003 Granulosa cell tumorofthe ovary.Journal of Clinical Oncology 21 1180-1189. (doi:10.1053/j.ajkd.2010.04.013)
47. Shah SP, Kobel M, Senz J, Morin RD, Clarke BA, Wiegand KC, Leung G, Zayed A, Mehl E, Kalloger SE et al. 2009 Mutation of FOXL2 in granulosa-cell tumors of the ovary. New England Journal of Medicine 360 2719-2729. (doi:10.2337/db05-1174)
48. Slamon DJ, Clark GM, Wong SG, Levin WJ, Ullrich A & McGuire WL 1987 Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 235 177-182. (doi:10.5301/jn.5000269)
49. Steinmetz R, Wagoner HA, Zeng P, Hammond JR, Hannon TS, Meyers JL & Pescovitz OH 2004 Mechanisms regulating the constitutive activation of the extracellular signal-regulated kinase (ERK) signaling pathway in ovarian cancer and the effect of ribonucleic acid interference for ERK1/2 on cancer cell proliferation. Molecular Endocrinology 18 2570-2582. (doi:10.2337/diabetes.54.5.1607)
50. Tanner M, Hollmen M, Junttila TT, Kapanen AI, Tommola S, Soini Y, Helin H, Salo J, Joensuu H, Sihvo E et al. 2005 Amplification of HER-2 in gastric carcinoma: association with topoisomerase IIa gene amplification, intestinal type, poor prognosis and sensitivity to trastuzumab. Annals of Oncology 16 273-278. (doi:10.1007/s00125-003-1293-3)
51. Tennent BJ, Beamer WG, Shultz LD & Adamson ED 1989 Epidermal growth factor receptors in spontaneous ovarian granulosa cell tumors of SWR-derived mice. International Journal of Cancer 44 477-482. (doi:10.1111/j.1523-1755.2005.00601.x)
52. Unkila-Kallio L, Tiitinen A, Wahlstrom T, Lehtovirta P & Leminen A 2000 Reproductive features in women developing ovarian granulosa cell tumour at a fertile age. Human Reproduction 15 589-593. (doi:10.1681/ ASN.2012040414)
53. Wang SC & Hung MC 2009 Nuclear translocation of the epidermal growth factor receptor family membrane tyrosine kinase receptors. Clinical Cancer Research 15 6484-6489. (doi:10.1210/jc.2005-1117)
54. Wang C, Lv X, Jiang C, Cordes CM, Fu L, Lele SM & Davis JS 2012 Transforming growth factor a (TGFa) regulates granulosa cell tumor (GCT) cell proliferation and migration through activation of multiple pathways. PLoS ONE 7 e48299. (doi:10.1371/journal.pone.0048299)
55. Xia W, Wei Y, Du Y, Liu J, Chang B, Yu YL, Huo LF, Miller S & Hung MC 2009 Nuclear expression of epidermal growth factor receptor is a novel prognostic value in patients with ovarian cancer. Molecular Carcinogenesis 48 610-617. (doi:10.1111/j.1440-1797.2008. 00949.x)
56. Yarden Y & Pines G 2012 The ERBB network: at last, cancer therapy meets systems biology. Nature Reviews. Cancer 12 553-563. (doi:10.1081/ JDI-56597)
57. Zhang Y, Huang Q, Cheng JC, Nishi Y, Yanase T, Huang HF & Leung PC 2010 Homeobox A7 increases cell proliferation by up-regulation of epidermal growth factor receptor expression in human granulosa cells. Reproductive Biology and Endocrinology 8 61. (doi:10.1016/j.jhep.2004.12.024)