Extracellular matrix secreted by reactive stroma is a main inducer of pro-tumorigenic features on LNCaP prostate cancer cells

Cancer Letters

Volumn 321, Issue 1, 2012, Pages 55-64

  Palumbo, Antonio ^a   Ferreira, Luciana Bueno ^b   Reis de Souza, Pedro A V ^a   Oliveira, Felipe Leite de ^a   Pontes, Bruno ^a   Viana, Nathan B ^a   Machado, Daniel Escorsim ^c   Palmero, Celia Yelimar ^a   Alves, Leandro M ^a   Gimba, Etel R P ^b,d   Nasciutti, Luiz E ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b INSTITUTO NACIONAL DE CÂNCER   (Brazil)

^c STATE UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^d FLUMINENSE FEDERAL UNIVERSITY   (Brazil)

Author keywords

Extracellular matrix; LNCaP cells; Prostate cancer; Reactive stroma

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CHONDROITIN SULFATE; COLLAGEN TYPE 1; COLLAGEN TYPE 3; COLLAGEN TYPE 4; CYTOKERATIN 18; DESMIN; FIBRONECTIN; GELATINASE A; GELATINASE B; LAMININ; NERVE CELL ADHESION MOLECULE; UVOMORULIN; VIMENTIN;

APOPTOSIS; ARTICLE; BAX GENE; BCL 2 GENE; CANCER CELL CULTURE; CARCINOGENICITY; CDK1 GENE; CDK2 GENE; CELL CONTACT; CELL INTERACTION; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; CELL STRUCTURE; CK18 GENE; CK8 GENE; COCULTURE; CONTROLLED STUDY; E CADHERIN GENE; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; METASTASIS; MMP 2 GENE; MMP 9 GENE; N CADHERIN GENE; ONCOGENE; PRIORITY JOURNAL; PROSTATE CANCER; PROSTATE HYPERTROPHY; REACTIVE STROMAL CELL; STROMA CELL; TUMOR GROWTH; TUMOR MICROENVIRONMENT; VIMENTIN GENE;

ANIMALS; CELL COMMUNICATION; CELL LINE, TUMOR; CELL SURVIVAL; DISEASE PROGRESSION; EXTRACELLULAR MATRIX; GENE EXPRESSION PROFILING; HUMANS; MALE; MICE; MICE, NUDE; PROSTATIC HYPERPLASIA; PROSTATIC NEOPLASMS; STROMAL CELLS; TUMOR MICROENVIRONMENT;

EID: 84860352064     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2012.02.026     Document Type: Article

References (50)

1. Damber J.E., Aus G. Prostate cancer. Lancet. 2008, 371:1710-1721.
2. Guise T. Examining the metastatic niche: targeting the microenvironment. Semin. Oncol. 2010, 37(Suppl):S2-S14.
3. Gregory C.D., Pound J.D. Cell death in the neighborhood direct microenvironmental effects of apoptosis in normal and neoplastic tissues. J. Pathol. 2011, 223:177-194.
4. Ayala G., Tuxhorn J.A., Wheeler T.M., Frolov A., Scardino P.T., Ohori M., Wheeler M., Spitler J., Rowley D.R. Reactive stroma as a predictor of biochemical-free recurrence in prostate cancer. Can. Res. 2003, 9:4792-4801.
5. Condon M.S. The role of the stromal microenvironment in prostate cancer. Semin. Can. Biol. 2005, 15:132-137.
6. Taylor R.A., Risbridger G.P. Prostatic tumor stroma: a key player in cancer progression. Curr. Can. Drugs Targets 2008, 8:490-497.
7. Olumi A.F., Dazin P., Tisty T.D. A novel coculture technique demonstrates that normal human prostatic fibroblasts contribute to tumor formation of LNCaP cells by retarding cell death. Can. Res. 1998, 58:4525-4530.
8. Olumi A.F., Grossfeld G.D., Hayward S.W., Carroll P.R., Tisty T.D., Cunha G.R. Carcinoma associated fibroblasts tumor progression of initiated human prostatic epithelium. Can. Res. 1999, 59:5002-5011.
9. Singh H., Dang T.D., Ayala G.E., Rowley D.R. Transforming growth factor-ß1 induced myofibroblasts regulates LNCaP cell death. J. Urol. 2004, 172:2421-2425.
10. Tuxhorn J.A., Ayala G.E., Rowley D.R. Reactive stroma in prostate cancer progression. J. Urol. 2001, 166:2472-2483.
11. Yang F., Strand D.W., Rowley D.R. Fibroblast growth factor-2 mediates transforming growth factor-β action in prostate cancer reactive stroma. Oncogene. 2008, 27:450-459.
12. Yang F., Tuxhorn J.A., Ressler S.J., McAlhany S.J., Dang T.D., Rowley D.R. Stromal expression of connective tissue growth factor promotes angiogenesis and prostate cancer tumorigenesis. Can. Res. 2005, 65:8887-8895.
13. San Francisco I.F., Dewolf W.C., Peehl D.M., Olumi A.F. Expression of transforming growth factor-beta 1 and growth in soft agar differentiate prostate carcinoma-associated fibroblasts from normal prostate fibroblasts. Int. J. Can. 2004, 112:213-218.
14. Tuxhorn J.A., Ayala G.E., Smith M.J., Smith V.C., Dang T.D., Rowley D.R. Reactive stroma in human prostate cancer: induction of myofibroblast phenotype and extracellular matrix remodeling. Clin. Can Res. 2002, 8:2912-2923.
15. Untergasser G., Gander R., Lilg C., Lepperdinger G., Plas E., Berger P. Profiling molecular targets of TGF-ß1 in Prostate Fibroblast to myofibroblast transdifferentiation. Mech. Age. Dev. 2005, 126:59-69.
16. Xue Y., Smedts F., Latijnhouwers M.A., Ruijter E.T., Aalders T.W., Rosette J.J., Debruyne F.M., Schalken J.A. Tenascin-c expression in prostatic intraepithelial neoplasia (pin): a marker of progression?. Anticancer. Res. 1998, 18:2679-2684.
17. Ricciardelli C., Mayne K., Sykes J.P., Raymond W.A., McCaul K., Marshall V.R., Horsfall D.J. Elevated levels of versican but not decorin predict disease progression in early -stage prostate cancer. Clin. Can. Res. 1998, 4:963-971.
18. Wilson M.J., Sellers R.G., Wiehr C., Maraud O., Peehl D. Expression of matrix metalloproteinase-2 and -9 and their inhibitors, tissue inhibitor of metalloproteinase-1 and -2, in primary cultures of prostatic stromal and epithelial cells. J. Cell. Phys. 2002, 191:208-216.
19. P.C. Walsh, A.B. Retik, E.D. A.J. Vaughan, L.R. Wein, Kavoussi, A.C. Novick, A.W. Partin, C.A. Peters, Campbell's Urology, eighth ed., Elsevier, Oxford, 2003.
20. Bushman W. Etiology, epidemiology and natural history of prostate enlargement. Urol. Clin. North America 2009, 36:403-415.
21. Theyer G., Kramer G., Assman I. Phenotypic characterization of infiltrating leukocytes in benign prostatic hyperplasia. Lab. Inv. 1992, 66:96-107.
22. Schauer I.G., Ressler S.J., Tuxhorn J.A., Dang T.D. D.R. Rowley, Elevated epithelial expression of interleukin-8 correlates with myofibroblast reactive stroma in benign prostatic hyperplasia. J. Urol. 2008, 72:205-213.
23. Tuxhorn J.A., McAlhany S.J., Yang F., Dang T.D., Rowley D.R. Inhibition of transforming growth factor- β activity decreases angiogenesis in a human prostate cancer reactive stroma xenograft model. Can. Res. 2002, 62:6021-6025.
24. Bair E.L., Massey C.P., Tran N.L., Borchers A.H., Heimark R.L., Cress A.E., Bowden G.T. Integrin and cadherin mediated induction of the matrix metalloprotease matrilysin in cocultures of malignant oral squamous cell carcinoma cells and dermal fibroblasts. Exp. Cell. Res. 2001, 270:259-267.
25. Mingfang A.O., Franco O.E., Park D., Raman D., Williams K., Hayward S.W. Cross-talk between paracrine acting cytokine and chemokine pathways promotes malignancy in benign human prostatic epithelium. Can. Res. 2007, 67:4244-4253.
26. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell. 2011, 144:646-674.
27. Arnolds J.T., Isaacs J.T. Mechanisms involved in the progression of androgen-independent prostate cancers: it is not only the cancer cell's fault. Endoc. Related. Cancer. 2002, 9:61-73.
28. Radisky D.C., Levy D.D., Littlepage L.E., Liu H., Nelson C.M., Fata J.E., Leak D., Godden E.L., Albertson D.G., Nieto M.A., Werb Z., Bissel M.J. Rac1b and reactive oxygen species mediate MMP-3 induced EMT and genomic instability. Nature 2005, 436:123-127.
29. Gehler S., Baldassare M., Lad Y., Leight J., Wozniak M., Riching K., Eliceiri K., Weaver V., Calderwood D., Keely P. Filamin A-beta-1 integrin complex tunes epithelial cell response to matrix tension. Mol. Biol. Cell. 2009, 20:3224-3238.
30. Levental K.R., Yu H., Kass L., Lakins J.N., Egeblad M., Erler J.T., T Fong S.F., Csiszar K., Giaccia A., Weninger W., Yamauchi M., Gasser D.L., Weaver V.M. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 2009, 139:891-906.
31. Coulson-Thomas V.J., Gesteira T.F., Coulson-Thomas Y.M., Vicente C.M., S Tersariol I.L., Nader H.B., Toma L. Fibroblast and prostate tumor cell cross-talk: fibroblast differentiation, TGF-β, and extracellular matrix down regulation. Exp. Cell. Res. 2010, 19:3207-3226.
32. Nagle R.B. Role of the extracellular matrix in prostate carcinogenesis. J. Cell. Biochem. 2004, 91:36-40.
33. Calaluce R., Kunkel M.W., Watts G.S., Schmelz M., Hao J., Barrera J., Guzman M.G., Isett R., Fitchmun M., Bowden G.T., Cress A.E., Futscher B.W., Nagle R.B. Laminin-5 mediated gene expression in human prostate carcinoma cells. Mol. Carcinogen. 2001, 30:119-129.
34. Udayakumar T.S., Chen M.L., Bair E.L., Von Bredow D.C., Cress A.E., Nagle R.B., Bowden G.T. Membrane type-1-matrix metalloproteinase expressed by prostate carcinoma cells cleaves human laminin-5 β3 chain and induces cell migration. Can. Res. 2003, 63:2292-2299.
35. DeOcampo D.B., Kleinman H.K., DeOcampo N.D., Webber M.M. Laminin-1 and α6β1 integrin regulate acinar morphogenesis of normal and malignant human prostate epithelial cells. The Prostate. 2001, 46:142-153.
36. Yu L., Wang C.Y., Shi J., Miao L., Du X., Mayer D., Zhang J. Estrogens promote invasion of prostate cancer cells in a paracrine manner through up-regulation of matrix metalloproteinase 2 in prostatic stromal cells. Endocrinology 2011, 152:773-781.
37. Kundu J.K., Surh Y.J. Inflammation: gearing the journey to cancer. Mutat Res. 2008, 659:15-30.
38. Jakowlew S.B. Transforming growth factor-beta in cancer and metastasis. CancerMetast Rev. 2006, 25:435-457.
39. E Giannoni, M Parri, P Chiarugi, EMT and Oxidative Stress: A BidirectionalInterplay Affecting Tumor Malignancy. Antioxid Redox Signal, 2011 November, Epubahead of print.
40. Chen P.S., Shih Y.W., Huang H.C., Cheng H.W. Diosgenin, a steroidal saponin, inhibits migration and invasion of human prostate cancer PC-3 cells by reducing matrix metalloproteinases expression. PLoS One. 2011, 6(5):20164.
41. Armstrong A.J., Marengo M.S., Oltean S., Kemeny G., Bitting R.L., Turnbull J.D., Herold C.I., Marcom P.K., George D.J., Garcia-Blanco M.A. Circulating tumor cells from patients with advanced prostate and breast cancer display both epithelial and mesenchymal markers. Mol Cancer Res. 2011, 9(8):997-1007.
42. Gravdal K., Halvorsen O.J., Haukaas S.A., Akslen L.A. A switch from E-cadherin toN-cadherin expression indicates epithelial to mesenchymal transition and is of strong and independent importance for the progress of prostate cancer. Clin. Cancer Res. 2007, 23:7003-7011.
43. Putzke A.P., Ventura A.P., Bailey A.M., Akture C., Opoku-Ansah J., Celiktaş M., Hwang M.S., Darling D.S., Coleman I.M., Nelson P.S., Nguyen H.M., Corey E., Tewari M., Morrissey C., Vessella R.L., Knudsen B.S. Metastatic progression of prostate cancer and e-cadherin regulation by zeb1 and SRC family kinases. Am. J. Pathol. 2011, 179:400-410.
44. Yin H., Lowery M., Glass J. In prostate cancer C/EBP alpha promotes cell growth by the loss of interactions with CDK2, CDK4, and E2F and by activation of AKT. Prostate. 2009, 69(9):1001-1016.
45. R.A. Weinberg, The Cancer Biology, first ed., Garland Science, 2007.
46. Yamaguchi H., Condeelis J. Regulation of the actin cytoskeleton in cancer cell migration and invasion. Biochim. Biophy. Acta. 2007, 1773:642-652.
47. Gleave M., Hsieh J.T., Gao C., Eschenbach A.C., Chung L.W.K. Acceleration of human prostate cancer growth in vivo by factors produced by prostate and bone fibroblasts. Can. Res. 1991, 51:3753-3761.
48. Giri D., Ropiquet F., Ittmann M. Alterations in expression of basic fibroblast growth factor (FGF) 2 and its receptor FGFR-1 in human prostate cancer. Clin. Can. Res. 1999, 5:1063-1071.
49. Degeorges A., Tatoud R., Lafeve F.F., Podgorniak M.P., Millot G., Cremoux P., Calvo F. Stromal cells from human benign prostatic hyperplasia produce a growth-inhibitory factor for LNCaP prostate cancer cells identified as interleukin-6. Int. J. Can. 1996, 68:207-214.
50. Tamm I., Cardinalie I., Murphyj S. Decreased adherence of interleukin 6-treated breast carcinoma cells can lead to separation from neighbors after mitosis. Proc. Nat; Acad. Sci. 1991, 88:4414-4418.