Stromal activation associated with development of prostate cancer in prostate-targeted fibroblast growth factor 8b transgenic mice

Neoplasia

Volumn 12, Issue 11, 2010, Pages 915-927

  Elo, Teresa D ^a   Valve, Eeva M ^a   Seppänen, Jani A ^a,b   Vuorikoski, Heikki J ^a,b   Mäkelä, Sari I ^a   Poutanen, Matti ^a   Kujala, Paula M ^c   Härkönen, Pirkko L ^a,d  

^a UNIVERSITY OF TURKU   (Finland)

^b Pharmatest Services Ltd   (Finland)

^c TAMPERE UNIVERSITY HOSPITAL   (Finland)

^d LUND UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTOR; CONNECTIVE TISSUE GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 8; FIBROBLAST GROWTH FACTOR 8B; OSTEOPONTIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CONTROLLED STUDY; FIBROBLAST; HISTOPATHOLOGY; INFLAMMATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTATE ADENOCARCINOMA; PROSTATE CANCER; PROSTATE EPITHELIUM; PROSTATIC INTRAEPITHELIAL NEOPLASIA; PROTEIN EXPRESSION; SARCOMA; SIGNAL TRANSDUCTION; STROMA; TRANSGENIC MOUSE; TUMOR GROWTH; TUMOR VASCULARIZATION; UPREGULATION; WILD TYPE;

EID: 78449263437     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1593/neo.10776     Document Type: Article

References (55)

1. Beenken A and Mohammadi M (2009). The FGF family: biology, pathophysiology and therapy. Nat Rev Drug Discov 8, 235-253.
2. Kwabi-Addo B, Ozen M, and Ittmann M (2004). The role of fibroblast growth factors and their receptors in prostate cancer. Endocr Relat Cancer 11, 709-724.
3. Li ZG, Mathew P, Yang J, Starbuck MW, Zurita AJ, Liu J, Sikes C, Multani AS, Efstathiou E, Lopez A, et al. (2008). Androgen receptor-negative human prostate cancer cells induce osteogenesis in mice through FGF9-mediated mechanisms. J Clin Invest 118, 2697-2710.
4. Song Z, Wu X, Powell WC, Cardiff RD, Cohen MB, Tin RT, Matusik RJ, Miller GJ, and Roy-Burman P (2002). Fibroblast growth factor 8 isoform B overexpression in prostate epithelium: a new mouse model for prostatic intraepithelial neoplasia. Cancer Res 62, 5096-5105.
5. Chua SS, Ma ZQ, Gong L, Lin SH, DeMayo FJ, and Tsai SY (2002). Ectopic expression of FGF-3 results in abnormal prostate and wolffian duct development. Oncogene 21, 1899-1908.
6. Freeman KW, Welm BE, Gangula RD, Rosen JM, Ittmann M, Greenberg NM, and Spencer DM (2003). Inducible prostate intraepithelial neoplasia with reversible hyperplasia in conditional FGFR1-expressing mice. Cancer Res 63, 8256-8263.
7. Wang F, McKeehan K, Yu C, Ittmann M, and McKeehan WL (2004). Chronic activity of ectopic type 1 fibroblast growth factor receptor tyrosine kinase in prostate epithelium results in hyperplasia accompanied by intraepithelial neoplasia. Prostate 58, 1-12.
8. Acevedo VD, Gangula RD, Freeman KW, Li R, Zhang Y, Wang F, Ayala GE, Peterson LE, Ittmann M, and Spencer DM (2007). Inducible FGFR-1 activation leads to irreversible prostate adenocarcinoma and an epithelial-to-mesenchymal transition. Cancer Cell 12, 559-571.
9. Tanaka A, Furuya A, Yamasaki M, Hanai N, Kuriki K, Kamiakito T, Kobayashi Y, Yoshida H, Koike M, and Fukayama M (1998). High frequency of fibroblast growth factor (FGF) 8 expression in clinical prostate cancers and breast tissues, immunohistochemically demonstrated by a newly established neutralizing monoclonal antibody against FGF 8. Cancer Res 58, 2053-2056.
10. Leung HY, Dickson C, Robson CN, and Neal DE (1996). Over-expression of fibroblast growth factor-8 in human prostate cancer. Oncogene 12, 1833-1835.
11. Valve EM, Nevalainen MT, Nurmi MJ, Laato MK, Martikainen PM, and Harkonen PL (2001). Increased expression of FGF-8 isoforms and FGF receptors in human premalignant prostatic intraepithelial neoplasia lesions and prostate cancer. Lab Invest 81, 815-826.
12. Gnanapragasam VJ, Robinson MC, Marsh C, Robson CN, Hamdy FC, and Leung HY (2003). FGF8 isoform b expression in human prostate cancer. Br J Cancer 88, 1432-1438.
13. Marsh SK, Bansal GS, Zammit C, Barnard R, Coope R, Roberts-Clarke D, Gomm JJ, Coombes RC, and Johnston CL (1999). Increased expression of fibroblast growth factor 8 in human breast cancer. Oncogene 18, 1053-1060.
14. Valve E, Martikainen P, Seppanen J, Oksjoki S, Hinkka S, Anttila L, Grenman S, Klemi P, and Harkonen P (2000). Expression of fibroblast growth factor (FGF)-8 isoforms and FGF receptors in human ovarian tumors. Int J Cancer 88, 718-725.
15. Ohuchi H, Yoshioka H, Tanaka A, Kawakami Y, Nohno T, and Noji S (1994). Involvement of androgen-induced growth factor (FGF-8) gene in mouse embryogenesis and morphogenesis. Biochem Biophys Res Commun 204, 882-888.
16. MacArthur CA, Lawshe A, Xu J, Santos-Ocampo S, Heikinheimo M, Chellaiah AT, and Ornitz DM (1995). FGF-8 isoforms activate receptor splice forms that are expressed in mesenchymal regions of mouse development. Development 121, 3603-3613.
17. Zhang X, Ibrahimi OA, Olsen SK, Umemori H, Mohammadi M, and Ornitz DM (2006). Receptor specificity of the fibroblast growth factor family. The complete mammalian FGF family. J Biol Chem 281, 15694-15700.
18. Gemel J, Gorry M, Ehrlich GD, and MacArthur CA (1996). Structure and sequence of human FGF8. Genomics 35, 253-257.
19. MacArthur CA, Lawshe A, Shankar DB, Heikinheimo M, and Shackleford GM (1995). FGF-8 isoforms differ in NIH3T3 cell transforming potential. Cell Growth Differ 6, 817-825.
20. Murphy T, Darby S, Mathers ME, and Gnanapragasam VJ (2010). Evidence for distinct alterations in the FGF axis in prostate cancer progression to an aggressive clinical phenotype. J Pathol 4, 452-460.
21. Dorkin TJ, Robinson MC, Marsh C, Bjartell A, Neal DE, and Leung HY (1999). FGF8 over-expression in prostate cancer is associated with decreased patient survival and persists in androgen independent disease. Oncogene 18, 2755-2761.
22. Mattila MM, Ruohola JK, Valve EM, Tasanen MJ, Seppanen JA, and Harkonen PL (2001). FGF-8b increases angiogenic capacity and tumor growth of androgenregulated S115 breast cancer cells. Oncogene 20, 2791-2804.
23. Ruohola JK, Viitanen TP, Valve EM, Seppanen JA, Loponen NT, Keskitalo JJ, Lakkakorpi PT, and Harkonen PL (2001). Enhanced invasion and tumor growth of fibroblast growth factor 8b-overexpressing MCF-7 human breast cancer cells. Cancer Res 61, 4229-4237.
24. Valta MP, Tuomela J, Bjartell A, Valve E, Vaananen HK, and Harkonen P (2008). FGF-8 is involved in bone metastasis of prostate cancer. Int J Cancer 123, 22-31.
25. Valta MP, Tuomela J, Vuorikoski H, Loponen N, Vaananen RM, Pettersson K, Vaananen HK, and Harkonen PL (2009). FGF-8b induces growth and rich vascularization in an orthotopic PC-3 model of prostate cancer. J Cell Biochem 107, 769-784.
26. Zhang J, Thomas TZ, Kasper S, and Matusik RJ (2000). A small composite probasin promoter confers high levels of prostate-specific gene expression through regulation by androgens and glucocorticoids in vitro and in vivo. Endocrinology 141, 4698-4710.
27. Kallio A, Guo T, Lamminen E, Seppanen J, Kangas L, Vaananen HK, and Harkonen P (2008). Estrogen and the selective estrogen receptor modulator (SERM) protection against cell death in estrogen receptor alpha and beta expressing U2OS cells. Mol Cell Endocrinol 289, 38-48.
28. Livak KJ and Schmittgen TD (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402-408.
29. Jiborn T, Abrahamson M, Wallin H, Malm J, Lundwall A, Gadaleanu V, Abrahamsson PA, and Bjartell A (2004). Cystatin C is highly expressed in the human male reproductive system. J Androl 25, 564-572.
30. Shappell SB, Thomas GV, Roberts RL, Herbert R, Ittmann MM, Rubin MA, Humphrey PA, Sundberg JP, Rozengurt N, Barrios R, et al. (2004). Prostate pathology of genetically engineered mice: definitions and classification. The consensus report from the Bar Harbor Meeting of the Mouse Models of Human Cancer Consortium Prostate Pathology Committee. Cancer Res 64, 2270-2305.
31. Tuxhorn JA, Ayala GE, Smith MJ, Smith VC, Dang TD, and Rowley DR (2002). Reactive stroma in human prostate cancer: induction of myofibroblast phenotype and extracellular matrix remodeling. Clin Cancer Res 8, 2912-2923.
32. Tuxhorn JA, McAlhany SJ, Dang TD, Ayala GE, and Rowley DR (2002). Stromal cells promote angiogenesis and growth of human prostate tumors in a differential reactive stroma (DRS) xenograft model. Cancer Res 62, 3298-3307.
33. Ayala G, Tuxhorn JA, Wheeler TM, Frolov A, Scardino PT, Ohori M, Wheeler M, Spitler J, and Rowley DR (2003). Reactive stroma as a predictor of biochemicalfree recurrence in prostate cancer. Clin Cancer Res 9, 4792-4801.
34. Wang KX and Denhardt DT (2008). Osteopontin: role in immune regulation and stress responses. Cytokine Growth Factor Rev 19, 333-345.
35. Yang F, Tuxhorn JA, Ressler SJ, McAlhany SJ, Dang TD, and Rowley DR (2005). Stromal expression of connective tissue growth factor promotes angiogenesis and prostate cancer tumorigenesis. Cancer Res 65, 8887-8895.
36. Castellano G, Malaponte G, Mazzarino MC, Figini M, Marchese F, Gangemi P, Travali S, Stivala F, Canevari S, and Libra M (2008). Activation of the osteopontin/matrix metalloproteinase-9 pathway correlates with prostate cancer progression. Clin Cancer Res 14, 7470-7480.
37. Ramankulov A, Lein M, Kristiansen G, Loening SA, and Jung K (2007). Plasma osteopontin in comparison with bone markers as indicator of bone metastasis and survival outcome in patients with prostate cancer. Prostate 67, 330-340.
38. Khodavirdi AC, Song Z, Yang S, Zhong C, Wang S, Wu H, Pritchard C, Nelson PS, and Roy-Burman P (2006). Increased expression of osteopontin contributes to the progression of prostate cancer. Cancer Res 66, 883-888.
39. Freeman KW, Gangula RD, Welm BE, Ozen M, Foster BA, Rosen JM, Ittmann M, Greenberg NM, and Spencer DM (2003). Conditional activation of fibroblast growth factor receptor (FGFR) 1, but not FGFR2, in prostate cancer cells leads to increased osteopontin induction, extracellular signal-regulated kinase activation, and in vivo proliferation. Cancer Res 63, 6237-6243.
40. 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, 1230-1239.
41. Jin D, El-Tanani M, and Campbell FC (2006). Identification of apolipoprotein D as a novel inhibitor of osteopontin-induced neoplastic transformation. Int J Oncol 29, 1591-1599.
42. Hall RE, Horsfall DJ, Stahl J, Vivekanandan S, Ricciardelli C, Stapleton AM, Scardino PT, Neufing P, and Tilley WD (2004). Apolipoprotein-D: a novel cellular marker for HGPIN and prostate cancer. Prostate 58, 103-108.
43. Yan G, Fukabori Y, McBride G, Nikolaropolous S, and McKeehan WL (1993). Exon switching and activation of stromal and embryonic fibroblast growth factor (FGF)-FGF receptor genes in prostate epithelial cells accompany stromal independence and malignancy. Mol Cell Biol 13, 4513-4522.
44. Sahadevan K, Darby S, Leung HY, Mathers ME, Robson CN, and Gnanapragasam VJ (2007). Selective over-expression of fibroblast growth factor receptors 1 and 4 in clinical prostate cancer. J Pathol 213, 82-90.
45. Jin C, McKeehan K, Guo W, Jauma S, Ittmann MM, Foster B, Greenberg NM, McKeehan WL, and Wang F (2003). Cooperation between ectopic FGFR1 and depression of FGFR2 in induction of prostatic intraepithelial neoplasia in the mouse prostate. Cancer Res 63, 8784-8790.
46. Gowardhan B, Douglas DA, Mathers ME, McKie AB, McCracken SR, Robson CN, and Leung HY (2005). Evaluation of the fibroblast growth factor system as a potential target for therapy in human prostate cancer. Br J Cancer 92, 320-327.
47. Wang J, Stockton DW, and Ittmann M (2004). The fibroblast growth factor receptor-4 Arg388 allele is associated with prostate cancer initiation and progression. Clin Cancer Res 10, 6169-6178.
48. Thiery JP (2002). Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2, 442-454.
49. Prins GS, Birch L, and Greene GL (1991). Androgen receptor localization in different cell types of the adult rat prostate. Endocrinology 129, 3187-3199.
50. Cunha GR, Hayward SW, Wang YZ, and Ricke WA (2003). Role of the stromal microenvironment in carcinogenesis of the prostate. Int J Cancer 107, 1-10.
51. Wikstrom P, Marusic J, Stattin P, and Bergh A (2009). Low stroma androgen receptor level in normal and tumor prostate tissue is related to poor outcome in prostate cancer patients. Prostate 69, 799-809.
52. Hansel DE, Herawi M, Montgomery E, and Epstein JI (2007). Spindle cell lesions of the adult prostate. Mod Pathol 20, 148-158.
53. Wang X, Jones TD, Zhang S, Eble JN, Bostwick DG, Qian J, Lopez-Beltran A, Montironi R, Harris JJ, and Cheng L (2007). Amplifications of EGFR gene and protein expression of EGFR, her-2/neu, c-kit, and androgen receptor in phyllodes tumor of the prostate. Mod Pathol 20, 175-182.
54. Zhu ML and Kyprianou N (2008). Androgen receptor and growth factor signaling cross-talk in prostate cancer cells. Endocr Relat Cancer 15, 841-849.
55. Memarzadeh S, Xin L, Mulholland DJ, Mansukhani A, Wu H, Teitell MA, and Witte ON (2007). Enhanced paracrine FGF10 expression promotes formation of multifocal prostate adenocarcinoma and an increase in epithelial androgen receptor. Cancer Cell 12, 572-585.