Development of a reactive stroma associated with prostatic intraepithelial neoplasia in EAF2 deficient mice

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Pascal, Laura E ^a   Ai, Junkui ^a   Masoodi, Khalid Z ^a   Wang, Yujuan ^a   Wang, Dan ^a   Eisermann, Kurtis ^a   Rigatti, Lora H ^a   O'Malley, Katherine J ^a   Ma, Hei M ^a   Wang, Xinhui ^b   Dar, Javid A ^a   Parwani, Anil V ^a   Simons, Brian W ^c   Ittman, Michael M ^d   Li, Luyuan ^e   Davies, Benjamin J ^a   Wang, Zhou ^a,f  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

^e NANKAI UNIVERSITY   (China)

^f UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; CELL LINE, TUMOR; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LASER CAPTURE MICRODISSECTION; MICE; MICE, KNOCKOUT; MICE, MUTANT STRAINS; NUCLEAR PROTEINS; PROSTATIC INTRAEPITHELIAL NEOPLASIA; TRANS-ACTIVATORS;

EID: 84894160455     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0079542     Document Type: Article

References (50)

1. Cunha GR, Ricke W, Thomson A, Marker PC, Risbridger G, et al. (2004) Hormonal, cellular, and molecular regulation of normal and neoplastic prostatic development. J Steroid Biochem Mol Biol 92: 221-236. (Pubitemid 40136583)
2. Tuxhorn JA, Ayala GE, Rowley DR (2001) Reactive stroma in prostate cancer progression. J Urol 166: 2472-2483. (Pubitemid 33065339)
3. Tuxhorn JA, Ayala GE, Smith MJ, Smith VC, Dang TD, et al. (2002) Reactive stroma in human prostate cancer: induction of myofibroblast phenotype and extracellular matrix remodeling. Clin Cancer Res 8: 2912-2923. (Pubitemid 35025739)
4. Xue Y, Smedts F, Latijnhouwers MA, Ruijter ET, Aalders TW, et al. (1998) Tenascin-C expression in prostatic intraepithelial neoplasia (PIN): a marker of progression? Anticancer Res 18: 2679-2684. (Pubitemid 28386566)
5. Wang Z, Tufts R, Haleem R, Cai X (1997) Genes regulated by androgen in the rat ventral prostate. Proc Natl Acad Sci U S A 94: 12999-13004. (Pubitemid 27518465)
6. Xiao W, Zhang Q, Jiang F, Pins M, Kozlowski JM, et al. (2003) Suppression of prostate tumor growth by U19, a novel testosterone-regulated apoptosis inducer. Cancer Res 63: 4698-4704. (Pubitemid 36951050)
7. Fu JD, Li J, Tweedie D, Yu HM, Chen L, et al. (2006) Crucial role of the sarcoplasmic reticulum in the developmental regulation of Ca2+ transients and contraction in cardiomyocytes derived from embryonic stem cells. FASEB J 20: 181-183. (Pubitemid 43100507)
8. Xiao W, Zhang Q, Habermacher G, Yang X, Zhang AY, et al. (2008) U19/ Eaf2 knockout causes lung adenocarcinoma, B-cell lymphoma, hepatocellular carcinoma and prostatic intraepithelial neoplasia. Oncogene 27: 1536-1544. (Pubitemid 351347870)
9. Pascal LE, Ai J, Rigatti LH, Lipton AK, Xiao W, et al. (2011) EAF2 loss enhances angiogenic effects of Von Hippel-Lindau heterozygosity on the murine liver and prostate. Angiogenesis 14: 331-343.
10. Su F, Pascal LE, Xiao W, Wang Z (2010) Tumor suppressor U19/EAF2 regulates thrombospondin-1 expression via p53. Oncogene 29: 421-431.
11. Lawler J, Detmar M (2004) Tumor progression: the effects of thrombospondin-1 and -2. Int J Biochem Cell Biol 36: 1038-1045. (Pubitemid 38501556)
12. Doll JA, Reiher FK, Crawford SE, Pins MR, Campbell SC, et al. (2001) Thrombospondin-1, vascular endothelial growth factor and fibroblast growth factor-2 are key functional regulators of angiogenesis in the prostate. Prostate 49: 293-305. (Pubitemid 33117005)
13. Colombel M, Filleur S, Fournier P, Merle C, Guglielmi J, et al. (2005) Androgens repress the expression of the angiogenesis inhibitor thrombospondin-1 in normal and neoplastic prostate. Cancer Res 65: 300-308. (Pubitemid 40070822)
14. Kwak C, Jin RJ, Lee C, Park MS, Lee SE (2002) Thrombospondin-1, vascular endothelial growth factor expression and their relationship with p53 status in prostate cancer and benign prostatic hyperplasia. BJU Int 89: 303-309. (Pubitemid 34158467)
15. Mehta R, Kyshtoobayeva A, Kurosaki T, Small EJ, Kim H, et al. (2001) Independent association of angiogenesis index with outcome in prostate cancer. Clin Cancer Res 7: 81-88. (Pubitemid 32110208)
16. Wu HC, Hsieh JT, Gleave ME, Brown NM, Pathak S, et al. (1994) Derivation of androgen-independent human LNCaP prostatic cancer cell sublines: role of bone stromal cells. Int J Cancer 57: 406-412. (Pubitemid 24168617)
17. Cyriac J, Haleem R, Cai X, Wang Z (2002) Androgen regulation of spermidine synthase expression in the rat prostate. Prostate 50: 252-261. (Pubitemid 34184665)
18. Furlow JD, Berry DL, Wang Z, Brown DD (1997) A set of novel tadpole specific genes expressed only in the epidermis are down-regulated by thyroid hormone during Xenopus laevis metamorphosis. Dev Biol 182: 284-298. (Pubitemid 27145480)
19. Kohler G, Milstein C (1975) Continuous cultures of fused cells secreting antibody of predefined specificity. Nature 256: 495-497.
20. Wang X, Campoli M, Cho HS, Ogino T, Bandoh N, et al. (2005) A method to generate antigen-specific mAb capable of staining formalin-fixed, paraffin-embedded tissue sections. J Immunol Methods 299: 139-151. (Pubitemid 40725931)
21. Temponi M, Kageshita T, Perosa F, Ono R, Okada H, et al. (1989) Purification of murine IgG monoclonal antibodies by precipitation with caprylic acid: comparison with other methods of purification. Hybridoma 8: 85-95. (Pubitemid 19082761)
22. Malik G, Knowles LM, Dhir R, Xu S, Yang S, et al. (2010) Plasma fibronectin promotes lung metastasis by contributions to fibrin clots and tumor cell invasion. Cancer Res 70: 4327-4334.
23. Kajdacsy-Balla A, Geynisman JM, Macias V, Setty S, Nanaji NM, et al. (2007) Practical aspects of planning, building, and interpreting tissue microarrays: the Cooperative Prostate Cancer Tissue Resource experience. J Mol Histol 38: 113-121. (Pubitemid 46659332)
24. Chen S, Sanford CA, Sun J, Choi V, Van Dyke T, et al. (2010) VHL and PTEN loss coordinate to promote mouse liver vascular lesions. Angiogenesis 13: 59-69.
25. O'Malley KJ, Dhir R, Nelson JB, Bost J, Lin Y, et al. (2009) The expression of androgen-responsive genes is up-regulated in the epithelia of benign prostatic hyperplasia. Prostate 69: 1716-1723.
26. Spandidos A, Wang X, Wang H, Seed B (2010) PrimerBank: a resource of human and mouse PCR primer pairs for gene expression detection and quantification. Nucleic Acids Res 38: D792-799.
27. Barron DA, Strand DW, Ressler SJ, Dang TD, Hayward SW, et al. (2010) TGF-beta1 induces an age-dependent inflammation of nerve ganglia and fibroplasia in the prostate gland stroma of a novel transgenic mouse. PLoS One 5: e13751.
28. Buttyan R, Ghafar MA, Shabsigh A (2000) The effects of androgen deprivation on the prostate gland: cell death mediated by vascular regression. Curr Opin Urol 10: 415-420.
29. Stewart RJ, Panigrahy D, Flynn E, Folkman J (2001) Vascular endothelial growth factor expression and tumor angiogenesis are regulated by androgens in hormone responsive human prostate carcinoma: evidence for androgen dependent destabilization of vascular endothelial growth factor transcripts. J Urol 165: 688-693. (Pubitemid 32060501)
30. Godoy A, Montecinos VP, Gray DR, Sotomayor P, Yau JM, et al. (2011) Androgen deprivation induces rapid involution and recovery of human prostate vasculature. Am J Physiol Endocrinol Metab 300: E263-275.
31. Li M, Wu X, Zhuang F, Jiang S, Jiang M, et al. (2003) Expression of murine ELL-associated factor 2 (Eaf2) is developmentally regulated. Dev Dyn 228: 273-280. (Pubitemid 37193640)
32. Olumi AF, Grossfeld GD, Hayward SW, Carroll PR, Tlsty TD, et al. (1999) Carcinoma-associated fibroblasts direct tumor progression of initiated human prostatic epithelium. Cancer Res 59: 5002-5011. (Pubitemid 29472907)
33. Jennbacken K, Gustavsson H, Tesan T, Horn M, Vallbo C, et al. (2009) The prostatic environment suppresses growth of androgen-independent prostate cancer xenografts: an effect influenced by testosterone. Prostate 69: 1164-1175.
34. Pascal LE, Ai J, Vencio RZ, Vencio EF, Zhou Y, et al. (2011) Differential Inductive Signaling of CD90 Prostate Cancer-Associated Fibroblasts Compared to Normal Tissue Stromal Mesenchyme Cells. Cancer Microenviron 4: 51-59.
35. Su F, Correa BR, Luo J, Vencio RZ, Pascal LE, et al. (2013) Gene Expression Profiling Reveals Regulation of ERK Phosphorylation by Androgen-Induced Tumor Suppressor U19/EAF2 in the Mouse Prostate. Cancer Microenviron.
36. Whang YE, Wu X, Suzuki H, Reiter RE, Tran C, et al. (1998) Inactivation of the tumor suppressor PTEN/MMAC1 in advanced human prostate cancer through loss of expression. Proc Natl Acad Sci U S A 95: 5246-5250. (Pubitemid 28208583)
37. Suzuki H, Freije D, Nusskern DR, Okami K, Cairns P, et al. (1998) Interfocal heterogeneity of PTEN/MMAC1 gene alterations in multiple metastatic prostate cancer tissues. Cancer Res 58: 204-209. (Pubitemid 28047054)
38. Hermans KG, van Alewijk DC, Veltman JA, van Weerden W, van Kessel AG, et al. (2004) Loss of a small region around the PTEN locus is a major chromosome 10 alteration in prostate cancer xenografts and cell lines. Genes Chromosomes Cancer 39: 171-184. (Pubitemid 38209578)
39. Gustavsson H, Wang W, Jennbacken K, Welen K, Damber JE (2009) ADAMTS1, a putative anti-angiogenic factor, is decreased in human prostate cancer. BJU Int 104: 1786-1790.
40. Freeman KW, Welm BE, Gangula RD, Rosen JM, Ittmann M, et al. (2003) Inducible prostate intraepithelial neoplasia with reversible hyperplasia in conditional FGFR1-expressing mice. Cancer Res 63: 8256-8263. (Pubitemid 37549476)
41. Bianchi-Frias D, Vakar-Lopez F, Coleman IM, Plymate SR, Reed MJ, et al. (2010) The effects of aging on the molecular and cellular composition of the prostate microenvironment. PLoS One 5.
42. Ayala G, Tuxhorn JA, Wheeler TM, Frolov A, Scardino PT, et al. (2003) Reactive stroma as a predictor of biochemical-free recurrence in prostate cancer. Clin Cancer Res 9: 4792-4801. (Pubitemid 37323282)
43. Ayala GE, Muezzinoglu B, Hammerich KH, Frolov A, Liu H, et al. (2011) Determining prostate cancer-specific death through quantification of stromogenic carcinoma area in prostatectomy specimens. Am J Pathol 178: 79-87.
44. Xiao W, Ai J, Habermacher G, Volpert O, Yang X, et al. (2009) U19/Eaf2 binds to and stabilizes von hippel-lindau protein. Cancer Res 69: 2599-2606.
45. Tuxhorn JA, McAlhany SJ, Yang F, Dang TD, Rowley DR (2002) Inhibition of transforming growth factor-beta activity decreases angiogenesis in a human prostate cancer-reactive stroma xenograft model. Cancer Res 62: 6021-6025. (Pubitemid 35244446)
46. Chen Z, Trotman LC, Shaffer D, Lin HK, Dotan ZA, et al. (2005) Crucial role of p53-dependent cellular senescence in suppression of Pten-deficient tumorigenesis. Nature 436: 725-730. (Pubitemid 41117277)
47. Bastia E, Xu YH, Scibelli AC, Day YJ, Linden J, et al. (2005) A crucial role for forebrain adenosine A(2A) receptors in amphetamine sensitization. Neuropsychopharmacology 30: 891-900. (Pubitemid 40570905)
48. Eng C (2003) PTEN: one gene, many syndromes. Hum Mutat 22: 183-198.
49. Untergasser G, Gander R, Lilg C, Lepperdinger G, Plas E, et al. (2005) Profiling molecular targets of TGF-beta1 in prostate fibroblast-to-myofibroblast transdifferentiation. Mech Ageing Dev 126: 59-69. (Pubitemid 40018478)
50. True LD, Zhang H, Ye M, Huang CY, Nelson PS, et al. (2010) CD90/THY1 is overexpressed in prostate cancer-associated fibroblasts and could serve as a cancer biomarker. Mod Pathol 23: 1346-1356.