Senescent fibroblasts promote neoplastic transformation of partially transformed ovarian epithelial cells in a three-dimensional model of early stage ovarian cancer

Neoplasia

Volumn 12, Issue 4, 2010, Pages 317-325

  Lawrenson, Kate ^a   Grun, Barbara ^a   Benjamin, Elizabeth ^b   Jacobs, Ian J ^a   Dafou, Dimitra ^a   Gayther, Simon A ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKERATIN 18; KI 67 ANTIGEN;

ARTICLE; CANCER MODEL; CANCER STAGING; CARCINOGENESIS; CELL AGING; CELL GROWTH; CELL IMMORTALIZATION; CELL INTERACTION; CELL MIGRATION; CELL PROLIFERATION; CELL TRANSFORMATION; COCULTURE; CONTROLLED STUDY; CULTURE MEDIUM; EPITHELIUM CELL; FEMALE; FIBROBLAST; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MALIGNANT TRANSFORMATION; ONCOGENE; OVARY CANCER; PRIORITY JOURNAL;

EID: 77951687669     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1593/neo.91948     Document Type: Article

References (32)

1. Yancik R (1993). Ovarian cancer. Age contrasts in incidence, histology, disease stage at diagnosis, and mortality. Cancer 71(2 suppl), 517-523.
2. Smith ER and Xu XX (2008). Ovarian ageing, follicle depletion, and cancer: a hypothesis for the aetiology of epithelial ovarian cancer involving follicle depletion. Lancet Oncol 9(11), 1108-1111.
3. Purdie DM, Bain CJ, Siskind V, Webb PM, and Green AC (2003). Ovulation and risk of epithelial ovarian cancer. Int J Cancer 104(2), 228-232.
4. Pike MC, Pearce CL, Peters R, Cozen W, Wan P, and Wu AH (2004). Hormonal factors and the risk of invasive ovarian cancer: a population-based case-control study. Fertil Steril 82(1), 186-195.
5. Herbig U, Ferreira M, Condel L, Carey D, and Sedivy JM (2006). Cellular senescence in aging primates. Science 311(5765), 1257.
6. Jeyapalan JC, Ferreira M, Sedivy JM, and Herbig U (2007). Accumulation of senescent cells in mitotic tissue of aging primates. Mech Ageing Dev 128(1), 36-44.
7. Olumi AF, Grossfeld GD, Hayward SW, Carroll PR, Tlsty TD, and Cunha GR (1999). Carcinoma-associated fibroblasts direct tumor progression of initiated human prostatic epithelium. Cancer Res 59(19), 5002-5011.
8. Parrinello S, Coppe JP, Krtolica A, and Campisi J (2005). Stromal-epithelial interactions in aging and cancer: senescent fibroblasts alter epithelial cell differentiation. J Cell Sci 118(Pt 3), 485-496.
9. Studebaker AW, Storci G, Werbeck JL, Sansone P, Sasser AK, Tavolari S, Huang T, Chan MW, Marini FC, Rosol TJ, et al. (2008). Fibroblasts isolated from common sites of breast cancer metastasis enhance cancer cell growth rates and invasiveness in an interleukin-6-dependent manner. Cancer Res 68(21), 9087-9095.
10. Krtolica A, Parrinello S, Lockett S, Desprez PY, and Campisi J (2001). Senescent fibroblasts promote epithelial cell growth and tumorigenesis: a link between cancer and aging. Proc Natl Acad Sci USA 98(21), 12072-12077.
11. Begley L, Monteleon C, Shah RB, Macdonald JW, and Macoska JA (2005). CXCL12 overexpression and secretion by aging fibroblasts enhance human prostate epithelial proliferation in vitro. Aging Cell 4(6), 291-298.
12. Bavik C, Coleman I, Dean JP, Knudsen B, Plymate S, and Nelson PS (2006). The gene expression program of prostate fibroblast senescence modulates neoplastic epithelial cell proliferation through paracrine mechanisms. Cancer Res 66(2), 794-802.
13. Pazolli E, Luo X, Brehm S, Carbery K, Chung JJ, Prior JL, Doherty J, Demehri S, Salavaggione L, Piwnica-Worms D, et al. (2009). Senescent stromal- derived osteopontin promotes preneoplastic cell growth. Cancer Res 69(3), 1230-1239.
14. Coppé JP, Patil CK, Rodier F, Sun Y, Muñoz DP, Goldstein J, Nelson PS, Desprez PY, and Campisi J (2008). Senescence-associated secretory phenotypes reveal cell-nonautonomous functions of oncogenic RAS and the p53 tumor suppressor. PLoS Biol 6(12), 2853-2868.
15. Coppé JP, Kauser K, Campisi J, and Beauséjour CM (2006). Secretion of vascular endothelial growth factor by primary human fibroblasts at senescence. J Biol Chem 281(40),29568-29574.
16. Liu D and Hornsby PJ (2007). Senescent human fibroblasts increase the early growth of xenograft tumors via matrix metalloproteinase secretion. Cancer Res 67(7),3117-3126.
17. Lawrenson K, Benjamin E, Turmaine M, Jacobs IJ, Gayther SA, and Dafou D (2009). In vitro three-dimensional modelling of human ovarian surface epithelial cells. Cell Prolif 42(3), 385-393.
18. Dimri GP, Lee X, Basile G, Acosta M, Scott G, Roskelley C, Medrano EE, Linskens M, Rubelj I, Pereira-Smith O, et al. (1995). A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci USA 92(20),9363-9367.
19. Iyer VR, Eisen MB, Ross DT, Schuler G, Moore T, Lee JC, Trent JM, Staudt LM, Hudson J Jr, Boguski MS, et al. (1999). The transcriptional program in the response of human fibroblasts to serum. Science 283, 83-87.
20. Chang HY, Sneddon JB, Alizadeh AA, Sood R, West RB, Montgomery K, Chi JT, van de Rijn M, Botstein D, and Brown PO (2004). Gene expression signature of fibroblast serum response predicts human cancer progression: similarities between tumors and wounds. PLoS Biol 2(2), e7.
21. Herbert BS, Wright WE, and Shay JW (2002). p16(INK4a) inactivation is not required to immortalize human mammary epithelial cells. Oncogene 21(51), 7897-7900.
22. Darbro BW, Lee KM, Nguyen NK, Domann FE, and Klingelhutz AJ (2006). Methylation of the p16(INK4a) promoter region in telomerase immortalized human keratinocytes co-cultured with feeder cells. Oncogene 25(56), 7421-7433.
23. Milyavsky M, Shats I, Erez N, Tang X, Senderovich S, Meerson A, Tabach Y, Goldfinger N, Ginsberg D, Harris CC, et al. (2003). Prolonged culture of telomerase-immortalized human fibroblasts leads to a premalignant phenotype. Cancer Res 63(21), 7147-7157.
24. Li NF, Broad S, Lu YJ, Yang JS, Watson R, Hagemann T, Wilbanks G, Jacobs I, Balkwill F, Dafou D, et al. (2007). Human ovarian surface epithelial cells immortalized with hTERT maintain functional pRb and p53 expression. CellProlif 40(5),780-794.
25. INK4a downregulation is involved in immortalization of primary human prostate epithelial cells induced by telomerase. Mol Carcinog 47(10), 775-783.
26. Fathalla MF (1971). Incessant ovulation-a factor in ovarian neoplasia? Lancet 2(7716),163.
27. Couzinet B, Meduri G, Lecce MG, Young J, Brailly S, Loosfelt H, Milgrom E, and Schaison G (2001). The postmenopausal ovary is not a major androgenproducing gland. J Clin Endocrinol Metab 86(10), 5060-5066.
28. Cai KQ, Klein-Szanto A, Karthik D, Edelson M, Daly MB, Ozols RF, Lynch HT, Godwin AK, and Xu XX (2006). Age-dependent morphological alterations of human ovaries from populations with and without BRCA mutations. Gynecol Oncol 103(2), 719-728.
29. Brustmann H (2005). Immunohistochemical detection of human telomerase reverse transcriptase (hTERT) and c-kit in serous ovarian carcinoma: a clinicopathologic study. Gynecol Oncol 98(3), 396-402.
30. Dimova I, Raitcheva S, Dimitrov R, Doganov N, and Toncheva D (2006). Correlations between c-myc gene copy-number and clinicopathological parameters of ovarian tumours. Eur J Cancer 42(5), 674-679.
31. Bladier C, Wolvetang EJ, Hutchinson P, de Haan JB, and Kola I (1997). Response of a primary human fibroblast cell line to H2O2: senescence-like growth arrest or apoptosis? Cell Growth Differ 8(5), 589-598.
32. Yang G, Rosen DG, Zhang Z, Bast RC Jr, Mills GB, Colacino JA, Mercado-Uribe I, and Liu J (2006). The chemokine growth-regulated oncogene 1 (Gro-1) links RAS signaling to the senescence of stromal fibroblasts and ovarian tumorigenesis. Proc Natl Acad Sci USA 103(44), 16472-16477.