Stroma regulates increased epithelial lateral cell adhesion in 3D culture: A role for actin/cadherin dynamics

PLoS ONE

Volumn 6, Issue 4, 2011, Pages

  Chambers, Karen F ^a   Pearson, Joanna F ^a   Aziz, Naveed ^a   O'Toole, Peter ^a   Garrod, David ^b,c   Lang, Shona H ^a  

^a UNIVERSITY OF YORK   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c KING SAUD UNIVERSITY   (Saudi Arabia)

Author keywords

[No Author keywords available]

Indexed keywords

F ACTIN; FIBROBLAST GROWTH FACTOR 10; RNA; STROMAL CELL DERIVED FACTOR 1; TRANSFORMING GROWTH FACTOR BETA2; UVOMORULIN; ACTIN; CADHERIN; CXCL12 PROTEIN, HUMAN; FGF10 PROTEIN, HUMAN; TGFB2 PROTEIN, HUMAN;

ARTICLE; BASOLATERAL MEMBRANE; CELL ADHESION; CELL GROWTH; CELL MEMBRANE PERMEABILITY; CELL STRAIN; CELL STRAIN BPH 1; CONTROLLED STUDY; CULTURE TECHNIQUE; DESMOSOME; ELECTRON MICROSCOPY; EPITHELIUM CELL; GENE EXPRESSION; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; STROMA; THREE DIMENSIONAL CULTURE; UPREGULATION; CELL LINE; COCULTURE; CYTOLOGY; EXTRACELLULAR MATRIX; MALE; METABOLISM; PROSTATE; STROMA CELL; ULTRASTRUCTURE;

ACTINS; CADHERINS; CELL ADHESION; CELL LINE; CHEMOKINE CXCL12; COCULTURE TECHNIQUES; EPITHELIAL CELLS; EXTRACELLULAR MATRIX; FIBROBLAST GROWTH FACTOR 10; HUMANS; MALE; MICROSCOPY, ELECTRON; PROSTATE; SIGNAL TRANSDUCTION; STROMAL CELLS; TRANSFORMING GROWTH FACTOR BETA2;

EID: 79955139282     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0018796     Document Type: Article

References (60)

1. Lecuit T, Lenne PF, (2007) Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis. Nat Rev Mol Cell Biol 8: 633-44.
2. Mailleux AA, Overholtzer M, Schmelzle T, Bouillet P, Strasser A, et al. (2007) BIM regulates apoptosis during mammary ductal morphogenesis, and its absence reveals alternative cell death mechanisms. Dev Cell 12: 221-34.
3. Martin-Belmonte F, Yu W, Rodriguez-Fraticelli AE, Ewald AJ, Werb Z, et al. (2008) Cell-polarity dynamics controls the mechanism of lumen formation in epithelial morphogenesis. Curr Biol 18: 507-13.
4. Lang SH, Stark M, Collins A, Paul, AB, Stower M J, et al. (2001) Experimental Prostate Epithelial Morphogenesis in Response to Stroma and Three-Dimensional Matrigel Culture. Cell Growth Differ 12: 631-640.
5. Lang SH, Stower M, Maitland NJ, (2000) In vitro modelling of epithelial and stromal interactions in non-malignant and malignant prostates. Br J Cancer 82: 990-7.
6. Green KJ, Simpson CL, (2007) Desmosomes: new perspectives on a classic. J Invest Dermatol 127: 2499-515.
7. Halbleib JM, Nelson WJ, (2006) Cadherins in development: cell adhesion, sorting, and tissue morphogenesis. Genes Dev 20: 3199-214.
8. De Vries WN, Evsikov AV, Haac BE, Fancher KS, Holbrook AE, et al. (2004) Maternal β-catenin and E-cadherin in mouse development. Development 131: 4435-4445.
9. Gates J, Peifer M, (2005) Can 1000 reviews be wrong? Actin, alpha-Catenin, and adherens junctions. Cell 123: 769-72.
10. Garrod D, Chidgey M, (2008) Desmosome structure, composition and function. Biochim Biophys Acta 1778: 572-87.
11. Cowell HE, Garrod DR, (1999) Activation of protein kinase C modulates cell-cell and cell-substratum adhesion of a human colorectal carcinoma cell line and restores 'normal' epithelial morphology. Int J Cancer 80: 455-64.
12. Vasioukhin V, Bowers E, Bauer C, Degenstein L, Fuchs E, (2001) Desmoplakin is essential in epidermal sheet formation. Nat Cell Biol 3: 1076-85.
13. Berry PA, Maitland NJ, Collins AT, (2008) Androgen receptor signalling in prostate: effects of stromal factors on normal and cancer stem cells. Mol. Cell. Endocrinology 288: 30-37.
14. Hayward SW, Del Buono R, Deshpande N, Hall PA, (1992) A functional model of adult human prostate epithelium. The role of androgens and stroma in architectural organisation and the maintenance of differentiated secretory function. J Cell Sci 102: 361-72.
15. Lang SH, Clarke NW, George NJ, Testa NG, (1999) Scatter factor influences the formation of prostate epithelial cell colonies on bone marrow stroma in vitro. Clin Exp Metastasis 17: 333-40.
16. Donjacour AA, Thomson AA, Cunha GR, (2003) FGF-10 plays an essential role in the growth of the fetal prostate. Dev Biol 261: 39-54.
17. Sugimura Y, Foster BA, Hom YK, Lipschutz JH, Rubin JS, et al. (1996) Keratinocyte growth factor (KGF) can replace testosterone in the ductal branching morphogenesis of the rat ventral prostate. Int J Dev Biol 40: 941-51.
18. Bhowmick NA, Chyti A, Plieth D, Gorska AE, Dumont N, et al. (2004) TGF-beta signaling in fibroblasts modulates the oncogenic potential of adjacent epithelia. Science 303: 848-51.
19. Danielpour D, (2005) Functions and regulation of transforming growth factor-beta (TGF-beta) in the prostate. Eur J Cancer 41: 846-57.
20. Placencio VR, Sharif-Afshar AR, Li X, Huang H, Uwamariya C, et al. (2008) Stromal transforming growth factor-beta signaling mediates prostatic response to androgen ablation by paracrine Wnt activity. Cancer Res 68: 4709-18.
21. Ao M, Franco OE, Park D, Raman D, Williams K, et al. (2007) Cross-talk between paracrine-acting cytokine and chemokine pathways promotes malignancy in benign human prostatic epithelium. Cancer Res 67: 4244-53.
22. Pearson J, Hughes S Chambers K, Lang SH, (2009) Polarized fluid movement and not cell death, creates luminal spaces in adult prostate epithelium. Cell Death Differ 16: 475-82.
23. Yap AS, Brieher WM, Pruschy M, Gumbiner BM, (1997) Lateral clustering of the adhesive ectodomain: a fundamental determinant of cadherin function. Curr Biol 7: 308-15.
24. Cavey M, Rauzi M, Lenne PF, Lecuit T, (2008) A two-tiered mechanism for stabilization and immobilization of E-cadherin. Nature 453: 751-6.
25. Lang S H, Clarke NW, George N J, Allen TD, Testa NG, (1998) Interaction of prostate epithelial cells from benign and malignant tumor tissue with bone-marrow stroma. Prostate 34: 203-213.
26. Prins GS, Putz O, (2008) Molecular signaling pathways that regulate prostate gland development. Differentiation 76: 641-59.
27. Blanchere M, Mestayer C, Saunier E, Broshuis M, Mowszowicz I, (2001) Transforming growth factor beta in the human prostate: its role in stromal-epithelial interactions in non-cancerous cell culture. Prostate 46: 311-8.
28. Zhang, J, Foudi A, Geay JF, Berthebaud M, Buet DJ, et al. (2004) Intracellular localization and constitutive endocytosis of CXCR4 in human CD34+ hematopoietic progenitor cells. Stem Cells 22: 1015-29.
29. Scotton CJ, Wilson JL, Scott K, Stamp G, Wilbanks GD, et al. (2002) Multiple actions of the chemokine CXCL12 on epithelial tumor cells in human ovarian cancer. Cancer Res 62: 5930-5938.
30. Koziczak M, Holbro T, Hynes NE, (2004) Blocking of FGFR signaling inhibits breast cancer cell proliferation through downregulation of D-type cyclins. Oncogene 23: 3501-8.
31. Xia L, H Wang, Munk S, Kwan J, Goldberg HJ, et al. (2008) High glucose activates PKC-zeta and NADPH oxidase through autocrine TGF-beta1 signaling in mesangial cells. Am J Physiol Renal Physiol 295: F1705-14.
32. Matter K, Balda MS, (2003) Functional analysis of tight junctions. Methods 30: 228-34.
33. Schmelz M, Moll R, Hesse U, Prasad AR, Gandolfi JA, et al. (2005) Identification of a stem cell candidate in the normal human prostate gland. Eur J Cell Biol 84: 341-54.
34. Derynck R, Zhang YE, (2003) Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature 425: 577-84.
35. Angres B, Barth A, Nelson WJ, (1996) Mechanism for transition from initial to stable cell-cell adhesion: kinetic analysis of E-cadherin-mediated adhesion using a quantitative adhesion assay. J Cell Biol 134: 549-57.
36. Chu YS, Thomas WA, Eder O, Pincet F, Perez E, et al. (2004) Force measurements in E-cadherin-mediated cell doublets reveal rapid adhesion strengthened by actin cytoskeleton remodeling through Rac and Cdc42. J Cell Biol 167: 1183-94.
37. Cook BD, Ferrari G, Pintucci G, Mignatti P, (2008) TGF-beta1 induces rearrangement of FLK-1-VE-cadherin-beta-catenin complex at the adherens junction through VEGF-mediated signaling. J Cell Biochem 105: 1367-73.
38. Howe KL, Reardon C, Wang A, Nazli A, McKay DM, (2005) Transforming growth factor-beta regulation of epithelial tight junction proteins enhances barrier function and blocks enterohemorrhagic Escherichia coli O157:H7-induced increased permeability. Am J Pathol 167: 587-97.
39. Ogata S, Morokuma J, Hayata T, Kolle G, Niehrs C, et al. (2007) TGF-beta signaling-mediated morphogenesis: modulation of cell adhesion via cadherin endocytosis. Genes Dev 21: 1817-31.
40. Shiou SR, Singh AB, Moorthy K, Datta PK, Washington MK, et al. (2007) Smad4 regulates claudin-1 expression in a transforming growth factor-beta-independent manner in colon cancer cells. Cancer Res 67: 1571-9.
41. Dzamba DJ, Jakab KR, Marsden M, Schwartz MA, DeSimone DW, (2009) Cadherin adhesion, tissue tension, and noncanonical wnt signaling regulate fibronectin matrix organization. Developmental Cell 16: 421-432.
42. Vasioukhin V, Bauer C, Yin M, Fuchs E, (2000) Directed actin polymerization is the driving force for epithelial cell-cell adhesion. Cell 100: 209-219.
43. Lee JM, Dedhar S, Kalluri R, Thompson EW, (2006) The epithelial-mesenchymal transition: new insights in signaling, development, and disease. J Cell Biol 172: 973-81.
44. Tate A, Isotani S, Bradley MJ, Sikes RA, Davis R, et al. (2006) Met-Independent Hepatocyte Growth Factor-mediated regulation of cell adhesion in human prostate cancer cells. BMC Cancer 6: 197.
45. Montesano R, Matsumoto K, Nakamura T, Orci L, (1991) Identification of a fibroblast-derived epithelial morphogen as hepatocyte growth factor. Cell 67: 901-8.
46. O'Brien LE, Tang K, Kats ES, Schutz-Geschwender A, Lipschutz JH, et al. (2004) ERK and MMPs sequentially regulate distinct stages of epithelial tubule development. Dev Cell 7: 21-32.
47. Krause S, Maffini MV, Soto AM, Sonnenschein C, (2008) A novel 3D in vitro culture model to study stromal-epithelial interactions in the mammary gland. Tissue Eng Part C Methods. 14: 261-71.
48. Swamydas M, Eddy JM, Burg KJ, Dréau D, (2010) Matrix compositions and the development of breast acini and ducts in 3D cultures. 46:673-84. In Vitro Cell Dev Biol Anim 46: 673-84. Epub 2010 Jun 29.
49. Sai X, Ladher RK, (2008) FGF signalling regulates cytoskeletal remodelling during epithelial morphogenesis. Curr Biol 18: 976-81.
50. Komarova Y, Malik AB, (2008) FGF signalling preserves the integrity of endothelial adherens junctions. Dev. Cell 15: 335-336.
51. Jamora C, Fuchs E, (2002) Intercellular adhesion, signaling and the cytoskeleton. Nature Cell Biology 4: 101-108.
52. Grammont M, (2007) Adherens junction remodeling by the Notch pathway in Drosophila melanogaster oogenesis. J Cell Biol 177: 139-150.
53. Lang SH, Hyde C, Reid IN, Hitchcock IS, Hart CA, et al. (2002) Enhanced expression of vimentin in motile prostate cell lines and in poorly differentiated and metastatic prostate carcinoma. Prostate 52: 253-63.
54. Manders EMM, Verbeek FJ, Aten JA, (1993) Measurement of co-localization of objects in dual-colour confocal images. J Microscopy 169: 375-382.
55. Abramoff MD, Magelhaes PJ, Ram SJ, (2004) Image Processing with Image J. Biophotonics International 11: 36-42.
56. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-8.
57. Li C, Hung Wong W, (2001) Model-based analysis of oligonucleotide arrays: model validation, design issues and standard error application. Genome Biol 2 RESEARCH0032.
58. Chambers KF, Bacon JR, Kemsley EK, Mills RD, Ball RY, et al. (2009) Gene expression profile of primary prostate epithelial and stromal cells in response to sulforaphane or iberin exposure. Prostate 69: 1411-21.
59. Draghici S, Khatri P, Tarca AL, Amin K, et al. (2007) A systems biology approach for pathway level analysis. Genome Res 17: 1537-45.
60. Xia L, Wang H, Munk S, Kwan J, Goldberg HJ, et al. (2008) High glucose activates PKC-zeta and NADPH oxidase through autocrine TGF-beta1 signaling in mesangial cells. Am J Physiol Renal Physiol 295: F1705-14.