Phenotypic Characterization of Prostate Cancer LNCaP Cells Cultured within a Bioengineered Microenvironment

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Sieh, Shirly ^a   Taubenberger, Anna V ^a   Rizzi, Simone C ^a   Sadowski, Martin ^a   Lehman, Melanie L ^a,b   Rockstroh, Anja ^a   An, Jiyuan ^a   Clements, Judith A ^a   Nelson, Colleen C ^a,b   Hutmacher, Dietmar W ^a  

^a QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN; ANDROGEN RECEPTOR; ARGININE; ASPARTIC ACID; GLYCINE; MACROGOL; MATRIX METALLOPROTEINASE; METRIBOLONE; SCLEROPROTEIN;

APOPTOSIS; ARTICLE; BIOENGINEERING; CANCER CELL CULTURE; CARCINOGENESIS; CELL CULTURE; CELL GROWTH; CELL HYPOXIA; CELL INTERACTION; CELL KINETICS; CELL STRAIN LNCAP; CELL STRUCTURE; CONTROLLED STUDY; DIFFUSION; EARLY CANCER; GENE EXPRESSION; HORMONE ACTION; HYDROGEL; INTERMETHOD COMPARISON; NUCLEOTIDE SEQUENCE; PROSTATE CANCER; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN SYNTHESIS; RIGIDITY; THREE DIMENSIONAL CULTURE SYSTEM; THREE DIMENSIONAL IMAGING; TUMOR MICROENVIRONMENT; TWO DIMENSIONAL CULTURE SYSTEM;

ACTIVE TRANSPORT, CELL NUCLEUS; AMINO ACID MOTIFS; ANOXIA; APOPTOSIS; BIOMIMETICS; BIOPHYSICS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL LINE, TUMOR; COLLAGEN; DIFFUSION; DRUG COMBINATIONS; EXTRACELLULAR MATRIX; HUMANS; HYDROGEL; HYDROGELS; KINETICS; LAMININ; MALE; PHENOTYPE; PROSTATIC NEOPLASMS; PROTEOGLYCANS; RECEPTORS, ANDROGEN; STRESS, MECHANICAL; TIME FACTORS;

EID: 84866039025     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0040217     Document Type: Article

References (92)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, et al. (2008) Cancer Statistics, 2008. 58: 71-96.
2. PCFA (2012) Prostate Cancer Statistics. Available: http://www.prostate.org.au/articleLive/pages/Prostate-Cancer-Statistics.html. Accessed: 10 January 2012.
3. Cukierman E, Pankov R, Yamada KM, (2002) Cell interactions with three-dimensional matrices. Current Opinion in Cell Biology 14: 633-640.
4. Vogel V, Sheetz M, (2006) Local force and geometry sensing regulate cell functions. Nat Rev Mol Cell Biol 7: 265-275.
5. Paszek MJ, Zahir N, Johnson KR, Lakins JN, Rozenberg GI, et al. (2005) Tensional homeostasis and the malignant phenotype. Cancer Cell 8: 241-254.
6. Krouskop TA, Wheeler TM, Kallel F, Garra BS, Hall T, (1998) Elastic moduli of breast and prostate tissues under compression. Ultrasonic Imaging 20: 260-274.
7. Hoyt K, Castaneda B, Zhang M, Nigwekar P, di Sant'Agnese PA, et al. (2008) Tissue elasticity properties as biomarkers for prostate cancer. Cancer Biomarkers 4: 213-225.
8. Levental KR, Yu H, Kass L, Lakins JN, Egeblad M, et al. (2009) Matrix Crosslinking Forces Tumor Progression by Enhancing Integrin Signaling. Cell 139: 891-906.
9. Kostic A, Lynch CD, Sheetz MP, (2009) Differential Matrix Rigidity Response in Breast Cancer Cell Lines Correlates with the Tissue Tropism. PLoS ONE 4: 1-11.
10. Tilghman RW, Cowan CR, Mih JD, Koryakina Y, Gioeli D, et al. (2010) Matrix Rigidity Regulates Cancer Cell Growth and Cellular Phenotype. PLoS ONE 5: 1-13.
11. Indra I, Beningo KA, (2011) An in vitro correlation of metastatic capacity, substrate rigidity, and ECM composition. Journal of Cellular Biochemistry 112: 3151-3158.
12. Yamada KM, Cukierman E, (2007) Modeling Tissue Morphogenesis and Cancer in 3D. Cell 130: 601-610.
13. Schwartz MP, Fairbanks BD, Rogers RE, Rangarajan R, Zaman MH, et al. (2010) A synthetic strategy for mimicking the extracellular matrix provides new insight about tumor cell migration. Integrative Biology 2: 32-40.
14. Harunaga JS, Yamada KM, (2011) Cell-matrix adhesions in 3D. Matrix Biology 30: 363-368.
15. Pathak A, Kumar S, (2010) Biophysical regulation of tumor cell invasion: moving beyond matrix stiffness. Integrative Biology 3: 267-278.
16. Ohmori T, Yang J-L, Price JO, Arteaga CL, (1998) Blockade of Tumor Cell Transforming Growth Factor-[beta]s Enhances Cell Cycle Progression and Sensitizes Human Breast Carcinoma Cells to Cytotoxic Chemotherapy. Experimental Cell Research 245: 350-359.
17. Fischbach C, Chen R, Matsumoto T, Schmelzle T, Brugge JS, et al. (2007) Engineering tumors with 3D scaffolds. Nat Meth 4: 855-860.
18. Friedrich J, Ebner R, Kunz-Schughart LA, (2007) Experimental anti-tumor therapy in 3-D: spheroids-old hat or new challenge? Int J Radiat Biol 83: 849-871.
19. Chu JH, Yu S, Hayward SW, Chan FL, (2008) Development of a three-dimensional culture model of prostatic epithelial cells and its use for the study of epithelial-mesenchymal transition and inhibition of PI3K pathway in prostate cancer. The Prostate 69: 428-442.
20. Yeung TM, Gandhi SC, Wilding JL, Muschel R, Bodmer WF, (2010) Cancer stem cells from colorectal cancer-derived cell lines. Proceedings of the National Academy of Sciences 107: 3722-3727.
21. Weaver VM, Petersen OW, Wang F, Larabell CA, Briand P, et al. (1997) Reversion of the Malignant Phenotype of Human Breast Cells in Three-Dimensional Culture and In Vivo by Integrin Blocking Antibodies. The Journal of Cell Biology 137: 231-245.
22. Lee GY, Kenny PA, Lee EH, Bissell MJ, (2007) Three-dimensional culture models of normal and malignant breast epithelial cells. Nat Meth 4: 359-365.
23. Doillon CJ, Gagnon E, Paradis RE, Koutsilieris M, (2004) Three-dimensional Culture System as a Model for Studying Cancer Cell Invasion Capacity and Anticancer Drug Sensitivity. Anticancer Research 24: 2169-2178.
24. Hutmacher DW, Loessner D, Rizzi S, Kaplan DL, Mooney DJ, et al. (2010) Can tissue engineering concepts advance tumor biology research? Trends in Biotechnology 28: 125-133.
25. Shu XZ, Liu Y, Palumbo F, Prestwich GD, (2003) Disulfide-crosslinked hyaluronan-gelatin hydrogel films: a covalent mimic of the extracellular matrix for in vitro cell growth. Biomaterials 24: 3825-3834.
26. Liu Y, Shu XZ, Prestwich GD, (2007) Tumor Engineering: Orthotopic Cancer Models in Mice Using Cell-Loaded, Injectable, Cross-Linked Hyaluronan-Derived Hydrogels. Tissue Engineering 13: 1091-1101.
27. Fischbach C, Kong HJ, Hsiong SX, Evangelista MB, Yuen W, et al. (2009) Cancer cell angiogenic capability is regulated by 3D culture and integrin engagement. Proceedings of the National Academy of Sciences 106: 399-404.
28. Lutolf MP, Hubbell JA, (2005) Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat Biotech 23: 47-55.
29. Ehrbar M, Rizzi SC, Schoenmakers RG, San Miguel B, Hubbell JA, et al. (2007) Biomolecular Hydrogels Formed and Degraded via Site-Specific Enzymatic Reactions. Biomacromolecules 8: 3000-3007.
30. Bott K, Upton Z, Schrobback K, Ehrbar M, Hubbell JA, et al. (2010) The effect of matrix characteristics on fibroblast proliferation in 3D gels. Biomaterials 31: 8454-8464.
31. Loessner D, Stok KS, Lutolf MP, Hutmacher DW, Clements JA, et al. (2010) Bioengineered 3D platform to explore cell-ECM interactions and drug resistance of epithelial ovarian cancer cells. Biomaterials 31: 8494-8506.
32. Lutolf MP, Lauer-Fields JL, Schmoekel HG, Metters AT, Weber FE, et al. (2003) Synthetic matrix metalloproteinase-sensitive hydrogels for the conduction of tissue regeneration: Engineering cell-invasion characteristics. Proceedings of the National Academy of Sciences 100: 5413-5418.
33. Herrala A, Kurkela R, Vihinen M, Kalkkinen N, Vihko P, (1998) Androgen-sensitive human prostate cancer cells, LNCaP, produce both N-terminally mature and truncated prostate-specific antigen isoforms. European Journal of Biochemistry 255: 329-335.
34. Pandini G, Mineo R, Frasca F, Roberts CT, Marcelli M, et al. (2005) Androgens Up-regulate the Insulin-like Growth Factor-I Receptor in Prostate Cancer Cells. Cancer Research 65: 1849-1857.
35. Schwartz MA, (2010) Integrins and Extracellular Matrix in Mechanotransduction. Cold Spring Harbor Perspectives in Biology 2: a005066.
36. Lutolf MP, Hubbell JA, (2003) Synthesis and Physicochemical Characterization of End-Linked Poly(ethylene glycol)-co-peptide Hydrogels Formed by Michael-Type Addition. Biomacromolecules 4: 713-722.
37. Ramanujan S, Pluen A, McKee TD, Brown EB, Boucher Y, et al. (2002) Diffusion and Convection in Collagen Gels: Implications for Transport in the Tumor Interstitium. Biophysical Journal 83: 1650-1660.
38. Erikson A, Andersen HN, Naess SN, Sikorski P, Davies CdL, (2008) Physical and chemical modifications of collagen gels: Impact on diffusion. Biopolymers 89: 135-143.
39. Helmlinger G, Netti PA, Lichtenbeld HC, Melder RJ, Jain RK, (1997) Solid stress inhibits the growth of multicellular tumor spheroids. Nat Biotech 15: 778-783.
40. Koike C, McKee TD, Pluen A, Ramanujan S, Burton K, et al. (2002) Solid stress facilitates spheroid formation: potential involvement of hyaluronan. Br J Cancer 86: 947-953.
41. Ballangrud AM, Yang W-H, Dnistrian A, Lampen NM, Sgouros G, (1999) Growth and Characterization of LNCaP Prostate Cancer Cell Spheroids. Clinical Cancer Research 5: 3171s-3176s.
42. Takagi A, Watanabe M, Ishii Y, Morita J, Hirokawa Y, et al. (2007) Three-dimensional Cellular Spheroid Formation Provides Human Prostate Tumor Cells with Tissue-like Features. Anticancer Research 27: 45-53.
43. Tuxhorn JA, McAlhany SJ, Dang TD, Ayala GE, Rowley DR, (2002) Stromal Cells Promote Angiogenesis and Growth of Human Prostate Tumors in a Differential Reactive Stroma (DRS) Xenograft Model. Cancer Research 62: 3298-3307.
44. Denmeade SR, Jakobsen CM, Janssen S, Khan SR, Garrett ES, et al. (2003) Prostate-Specific Antigen-Activated Thapsigargin Prodrug as Targeted Therapy for Prostate Cancer. Journal of the National Cancer Institute 95: 990-1000.
45. Hensley HH, Hannoun-Levi J-M, Hachem P, Mu Z, Stoyanova R, et al. (2011) PKA knockdown enhances cell killing in response to radiation and androgen deprivation. International Journal of Cancer 128: 962-973.
46. Li Y, Ligr M, McCarron JP, Daniels G, Zhang D, et al. (2011) Natura-Alpha Targets Forkhead Box M1 and Inhibits Androgen-Dependent and-Independent Prostate Cancer Growth and Invasion. Clinical Cancer Research 17: 4414-4424.
47. Discher DE, Janmey P, Wang Y-l, (2005) Tissue Cells Feel and Respond to the Stiffness of Their Substrate. Science 310: 1139-1143.
48. Zhang XP, Fournier MV, Ware JL, Bissell MJ, Yacoub A, et al. (2009) Inhibition of vimentin or beta(1) integrin revert morphology of prostate tumor cells grown in laminin-rich extracellular matrix gels and reduces tumor growth in vivo. Molecular Cancer Therapeutics 8: 499-508.
49. Härmä V, Virtanen J, Mäkelä{currency sign} R, Happonen A, Mpindi J-P, et al. (2010) A Comprehensive Panel of Three-Dimensional Models for Studies of Prostate Cancer Growth, Invasion and Drug Responses. PLoS ONE 5: 1-17.
50. Raleigh JA, Miller GG, Franko AJ, Koch CJ, Fuciarelli AF, et al. (1987) Fluorescence immunohistochemical detection of hypoxic cells in spheroids and tumours. Br J Cancer 56: 395-400.
51. Zhao D, Constantinescu A, Hahn EW, Mason RP, (2001) Tumor Oxygen Dynamics with Respect to Growth and Respiratory Challenge: Investigation of the Dunning Prostate R3327-HI Tumor. Radiation Research 156: 510-520.
52. Franovic A, Gunaratnam L, Smith K, Robert I, Patten D, et al. (2007) Translational up-regulation of the EGFR by tumor hypoxia provides a nonmutational explanation for its overexpression in human cancer. Proceedings of the National Academy of Sciences 104: 13092-13097.
53. Jankovic B, Aquino-Parsons C, Raleigh JA, Stanbridge EJ, Durand RE, et al. (2006) Comparison between pimonidazole binding, oxygen electrode measurements, and expression of endogenous hypoxia markers in cancer of the uterine cervix. Cytometry Part B: Clinical Cytometry 70B: 45-55.
54. Li X-F, O'Donoghue JA, (2008) Hypoxia in microscopic tumors. Cancer Letters 264: 172-180.
55. Kunz-Schughart LA, Freyer JP, Hofstaedter F, Ebner R, (2004) The Use of 3-D Cultures for High-Throughput Screening: The Multicellular Spheroid Model. Journal of Biomolecular Screening 9: 273-285.
56. Taplin M-E, Balk SP, (2004) Androgen receptor: A key molecule in the progression of prostate cancer to hormone independence. Journal of Cellular Biochemistry 91: 483-190.
57. Heinlein CA, Chang C, (2004) Androgen Receptor in Prostate Cancer. Endocrine Reviews 25: 276-308.
58. Tindall D, Lonergan P, (2011) Androgen receptor signaling in prostate cancer development and progression. Journal of Carcinogenesis 10: 20-20.
59. Syms AJ, Norris JS, Panko WB, Smith RG, (1985) Mechanism of androgen-receptor augmentation. Analysis of receptor synthesis and degradation by the density-shift technique. The Journal of Biological Chemistry 260: 455-461.
60. Yeap BB, Krueger RG, Leedman PJ, (1999) Differential Posttranscriptional Regulation of Androgen Receptor Gene Expression by Androgen in Prostate and Breast Cancer Cells. Endocrinology 140: 3282-3291.
61. Locke JA, Guns ES, Lubik AA, Adomat HH, Hendy SC, et al. (2008) Androgen Levels Increase by Intratumoral De novo Steroidogenesis during Progression of Castration-Resistant Prostate Cancer. Cancer Res 68: 6407-6415.
62. Lubik AA, Gunter JH, Hendy SC, Locke JA, Adomat HH, et al. (2011) Insulin Increases De Novo Steroidogenesis in Prostate Cancer Cells. Cancer Research 71: 5754-5764.
63. Horning JL, Sahoo SK, Vijayaraghavalu S, Dimitrijevic S, Vasir JK, et al. (2008) 3-D Tumor Model for In Vitro Evaluation of Anticancer Drugs. Molecular Pharmaceutics 5: 849-862.
64. Hakkinen KM, Harunaga JS, Doyle AD, Yamada KM, (2010) Direct Comparisons of the Morphology, Migration, Cell Adhesions, and Actin Cytoskeleton of Fibroblasts in Four Different Three-dimensional Extracellular Matrices. Tissue Eng Part A 17: 713-724.
65. Li S, Lao J, Chen BPC, Li Y-S, Zhao Y, et al. (2003) Genomic analysis of smooth muscle cells in 3-dimensional collagen matrix. The FASEB Journal 17: 97-99.
66. Wells RG, (2008) The role of matrix stiffness in regulating cell behavior. Hepatology 47: 1394-1400.
67. Lin R-Z, Chang H-Y, (2008) Recent advances in three-dimensional multicellular spheroid culture for biomedical research. Biotechnology Journal 3: 1172-1184.
68. Hirschhaeuser F, Menne H, Dittfeld C, West J, Mueller-Klieser W, et al. (2010) Multicellular tumor spheroids: An underestimated tool is catching up again. Journal of Biotechnology 148: 3-15.
69. Cheng G, Tse J, Jain RK, Munn LL, (2009) Micro-environmental mechanical stress controls tumor spheroid size and morphology by suppressing proliferation and inducing apoptosis in cancer cells. PLoS One 4: e4632.
70. Sutherland R, (1988) Cell and environment interactions in tumor microregions: the multicell spheroid model. Science 240: 177-184.
71. Butterworth KT, McCarthy HO, Devlin A, Ming L, Robson T, et al. (2008) Hypoxia selects for androgen independent LNCaP cells with a more malignant geno- and phenotype. International Journal of Cancer 123: 760-768.
72. Rehfeldt F, Engler AJ, Eckhardt A, Ahmed F, Discher DE, (2007) Cell responses to the mechanochemical microenvironment-Implications for regenerative medicine and drug delivery. Advanced Drug Delivery Reviews 59: 1329-1339.
73. Chou SC, Azuma Y, Varia MA, Raleigh JA, (2004) Evidence that involucrin, a marker for differentiation, is oxygen regulated in human squamous cell carcinomas. Br J Cancer 90: 728-735.
74. Tupper J, Greco O, Tozer GM, Dachs GU, (2004) Analysis of the horseradish peroxidase//indole-3-acetic acid combination in a three-dimensional tumor model. Cancer Gene Ther 11: 508-513.
75. Schafer ZT, Grassian AR, Song L, Jiang Z, Gerhart-Hines Z, et al. (2009) Antioxidant and oncogene rescue of metabolic defects caused by loss of matrix attachment. Nature 461: 109-113.
76. Movsas B, Chapman JD, Hanlon AL, Horwitz EM, Pinover WH, et al. (2001) Hypoxia in human prostate carcinoma- An Eppendorf Po-2 study. American Journal of Clinical Oncology-Cancer Clinical Trials 24: 458-461.
77. Parker C, Milosevic M, Toi A, Sweet J, Panzarella T, et al. (2004) Polarographic electrode study of tumor oxygenation in clinically localized prostate cancer. International Journal of Radiation Oncology*Biology*Physics 58: 750-757.
78. Vaupel P, Mayer A, (2007) Hypoxia in cancer: significance and impact on clinical outcome. Cancer and Metastasis Reviews 26: 225-239.
79. Anderson ARA, Weaver AM, Cummings PT, Quaranta V, (2006) Tumor Morphology and Phenotypic Evolution Driven by Selective Pressure from the Microenvironment. Cell 127: 905-915.
80. Rorth P, (2009) Collective Cell Migration. Annual Review of Cell and Development 25: 407-429.
81. Friedl P, Gilmour D, (2009) Collective cell migration in morphogenesis, regeneration and cancer. Nat Rev Mol Cell Biol 10: 445-457.
82. Quaranta V, Rejniak KA, Gerlee P, Anderson ARA, (2008) Invasion emerges from cancer cell adaptation to competitive microenvironments: Quantitative predictions from multiscale mathematical models. Seminars in Cancer Biology 18: 338-348.
83. Kesler CT, Gioeli D, Conaway MR, Weber MJ, Paschal BM, (2007) Subcellular Localization Modulates Activation Function 1 Domain Phosphorylation in the Androgen Receptor. Molecular Endocrinology 21: 2071-2084.
84. Zhang J, Xiang J-Q, Zhang Y-W, Chen Y-Y, Zhou X-Y, et al. (2007) Cell Adhesion Regulates Expression of the Androgen Receptor and Coregulators in Different Prostate Cancer Cells. International Journal of Molecular Sciences 8: 156-165.
85. Park S-Y, Kim Y-J, Gao AC, Mohler JL, Onate SA, et al. (2006) Hypoxia Increases Androgen Receptor Activity in Prostate Cancer Cells. Cancer Research 66: 5121-5129.
86. Mitani T, Yamaji R, Higashimura Y, Harada N, Nakano Y, et al. (2011) Hypoxia enhances transcriptional activity of androgen receptor through hypoxia-inducible factor-1α in a low androgen environment. Journal of Steroid Biochemistry and Molecular Biology 123: 58-64.
87. Lamb LE, Zarif JC, Miranti CK, (2011) The Androgen Receptor Induces Integrin α6β1 to Promote Prostate Tumor Cell Survival via NF-κB and Bcl-xL Independently of PI3K Signaling. Cancer Research 71: 2739-2749.
88. Khandrika L, Lieberman R, Koul S, Kumar B, Maroni P, et al. (2009) Hypoxia-associated p38 mitogen-activated protein kinase-mediated androgen receptor activation and increased HIF-1[alpha] levels contribute to emergence of an aggressive phenotype in prostate cancer. Oncogene 28: 1248-1260.
89. Sayeed A, Alam N, Trerotola M, Languino LR, (2012) Insulin-like growth factor 1 stimulation of androgen receptor activity requires β1A integrins. Journal of Cellular Physiology 227: 751-758.
90. Ehrbar M, Rizzi SC, Hlushchuk R, Djonov V, Zisch AH, et al. (2007) Enzymatic formation of modular cell-instructive fibrin analogs for tissue engineering. Biomaterials 28: 3856-3866.
91. Quent VMC, Loessner D, Friis T, Reichert JC, Hutmacher DW, (2010) Discrepancies between metabolic activity and DNA content as tool to assess cell proliferation in cancer research. Journal of Cellular and Molecular Medicine 14: 1003-1013.
92. Sieh S, Lubik AA, Clements JA, Nelson CC, Hutmacher DW, (2010) Interactions between human osteoblasts and prostate cancer cells in a novel 3D in vitro model. Organogenesis 6: 181-188.