Imbalance of desmoplastic stromal cell numbers drives aggressive cancer processes

Journal of Pathology

Volumn 230, Issue 1, 2013, Pages 107-117

  Kadaba, Raghu ^a,b   Birke, Hanna ^a   Wang, Jun ^a   Hooper, Steven ^c   Andl, Claudia D ^d   Di Maggio, Francesco ^a   Soylu, Erdinc ^a   Ghallab, Mohammed ^a   Bor, Daniel ^a   Froeling, Fieke E M ^a   Bhattacharya, Satyajit ^b   Rustgi, Anil K ^e   Sahai, Erik ^c   Chelala, Claude ^a   Sasieni, Peter ^a   Kocher, Hemant M ^a,b  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b ROYAL LONDON HOSPITAL   (United Kingdom)

^c IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^d VANDERBILT UNIVERSITY   (United States)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

apoptosis; gene expression microarray; invasion; organotypic model; proliferation

Indexed keywords

BETA CATENIN; UVOMORULIN;

APOPTOSIS; ARTICLE; CANCER INVASION; CELL ADHESION; CELL COUNT; CELL CULTURE; CELL DEATH; CELL INTERACTION; CELL MOTION; CELL POPULATION; CELL PROLIFERATION; CONTROLLED STUDY; DESMOPLASTIC STROMA; EPITHELIUM CELL; ESOPHAGUS CANCER; FIBROSIS; HUMAN; HUMAN CELL; HUMAN TISSUE; INFLAMMATION; MICROARRAY ANALYSIS; MYOFIBROBLAST; NUCLEOTIDE SEQUENCE; PANCREAS CANCER; PANCREATIC STELLATE CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SKIN CANCER; STROMA; STROMA CELL; TISSUE MICROARRAY;

APOPTOSIS; CELL LINE, TUMOR; CELL SURVIVAL; DISEASE PROGRESSION; EPITHELIAL CELLS; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MYOFIBROBLASTS; NEOPLASM INVASIVENESS; ORGAN CULTURE TECHNIQUES; PANCREAS; PANCREATIC NEOPLASMS; PANCREATIC STELLATE CELLS; SIGNAL TRANSDUCTION; STROMAL CELLS; TISSUE ARRAY ANALYSIS; TRANSCRIPTOME;

EID: 84876153722     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4172     Document Type: Article

References (46)

1. Erkan M, Michalski CW, Rieder S, et al., The activated stroma index is a novel and independent prognostic marker in pancreatic ductal adenocarcinoma. Clin Gastroenterol Hepatol 2008; 6: 1155-1161.
2. Fujita H, Ohuchida K, Mizumoto K, et al., α-Smooth muscle actin expressing stroma promotes an aggressive tumor biology in pancreatic ductal adenocarcinoma. Pancreas 2010; 39: 1254-1262.
3. Wang K, Ma W, Wang J, et al., Tumor:stroma ratio is an independent predictor for survival in esophageal squamous cell carcinoma. J Thorac Oncol 2012; 7: 1457-1461.
4. Woenne EC, Lederle W, Zwick S, et al., MMP inhibition blocks fibroblast-dependent skin cancer invasion, reduces vascularization and alters VEGF-A and PDGF-BB expression. Anticancer Res 2012; 30: 703-711.
5. Hanahan D, Weinberg RA,. Hallmarks of cancer: the next generation. Cell 2011; 144: 646-674.
6. De Wever O, Demetter P, Mareel M, et al., Stromal myofibroblasts are drivers of invasive cancer growth. Int J Cancer 2008; 123: 2229-2238.
7. Cukierman E, Bassi DE,. Physico-mechanical aspects of extracellular matrix influences on tumorigenic behaviors. Semin Cancer Biol 2010; 20: 139-145.
8. Erkan M, Adler G, Apte MV, et al., StellaTUM: current consensus and discussion on pancreatic stellate cell research. Gut 2012; 61: 172-178.
9. Hwang RF, Moore T, Arumugam T, et al., Cancer-associated stromal fibroblasts promote pancreatic tumor progression. Cancer Res 2008; 68: 918-926.
10. Froeling FE, Feig C, Chelala C, et al., Retinoic acid-induced pancreatic stellate cell quiescence reduces paracrine Wnt-β-catenin signaling to slow tumor progression. Gastroenterology 2011; 141: 1486-1497.
11. Olive KP, Jacobetz MA, Davidson CJ, et al., Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer. Science 2009; 324: 1457-1461.
12. Von Hoff DD, Ramanathan RK, Borad MJ, et al., Gemcitabine plus nab-paclitaxel is an active regimen in patients with advanced pancreatic cancer: a phase I/II trial. J Clin Oncol 2011; 29: 4548-4554.
13. Froeling FE, Mirza TA, Feakins RM, et al., Organotypic culture model of pancreatic cancer demonstrates that stromal cells modulate E-cadherin, β-catenin, and Ezrin expression in tumor cells. Am J Pathol 2009; 175: 636-648.
14. Froeling FE, Marshall JF, Kocher HM,. Pancreatic cancer organotypic cultures. J Biotechnol 2010; 148: 16-23.
15. Gaggioli C, Hooper S, Hidalgo-Carcedo C, et al., Fibroblast-led collective invasion of carcinoma cells with differing roles for RhoGTPases in leading and following cells. Nat Cell Biol 2007; 9: 1392-1400.
16. Oyama K, Okawa T, Nakagawa H, et al., AKT induces senescence in primary esophageal epithelial cells but is permissive for differentiation as revealed in organotypic culture. Oncogene 2007; 26: 2353-2364.
17. Li NF, Kocher HM, Salako MA, et al., A novel function of colony-stimulating factor 1 receptor in hTERT immortalization of human epithelial cells. Oncogene 2009; 28: 773-780.
18. Bachem MG, Schneider E, Gross H, et al., Identification, culture, and characterization of pancreatic stellate cells in rats and humans. Gastroenterology 1998; 115: 421-432.
19. Gentleman RC, Carey VJ, Bates DM, et al., Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 2004; 5: R80.
20. The R project of statistical computing: www.r-project.org.
21. Smyth GK,. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004; 3: Article 3.
22. Benjamini Y, Hochberg Y,. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Statist Soc 1995; 57: 289-300.
23. Girke T,. Intersect and Venn diagram functions: http://faculty.ucr. edu/∼tgirke/Documents/R-BioCond/My-R-Scripts/overLapper.R.
24. Gene Expression Omnibus: http://www.ncbi.nlm.nih.gov/geo/.
25. Primer Blast: http://www.ncbi.nlm.nih.gov/tools/primer-blast/.
26. -ΔΔC t method. Methods 2001; 25: 402-408.
27. Schneider CA, Rasband WS, Eliceiri KW., " NIH Image to ImageJ: 25 years of image analysis ". Nature Methods 2012; 9: 671-675.
28. Royston P, Altman DG,. Regression using fractional polynomials of continuous covariates: Parsimonious parametric modelling. Appl Statist 1994; 43: 429-467.
29. Cuzick J., A Wilcoxon-type test for trend. Statist Med 1985; 4: 87-90.
30. Kalabis J, Wong GS, Vega ME, et al., Isolation and characterization of mouse and human esophageal epithelial cells in 3D organotypic culture. Nat Protoc 2012; 7: 235-246.
31. Provenzano PP, Cuevas C, Chang AE, et al., Enzymatic targeting of the stroma ablates physical barriers to treatment of pancreatic ductal adenocarcinoma. Cancer Cell 2012; 21: 418-429.
32. Giampieri S, Manning C, Hooper S, et al., Localized and reversible TGFβ signalling switches breast cancer cells from cohesive to single cell motility. Nat Cell Biol 2009; 11: 1287-1296.
33. Heuberger J, Birchmeier W,. Interplay of cadherin-mediated cell adhesion and canonical Wnt signaling. Cold Spring Harb Perspect Biol 2010; 2: a002915.
34. Ai J, Tang Q, Wu Y, et al., The role of polymeric immunoglobulin receptor in inflammation-induced tumor metastasis of human hepatocellular carcinoma. J Natl Cancer Inst 2012; 103: 1696-1712.
35. Andl CD, McCowan KM, Allison GL, et al., Cathepsin B is the driving force of esophageal cell invasion in a fibroblast-dependent manner. Neoplasia 2011; 12: 485-498.
36. Andl CD, Fargnoli BB, Okawa T, et al., Coordinated functions of E-cadherin and transforming growth factor-β receptor II in vitro and in vivo. Cancer Res 2006; 66: 9878-9885.
37. Koenig A, Mueller C, Hasel C, et al., Collagen type I induces disruption of E-cadherin-mediated cell-cell contacts and promotes proliferation of pancreatic carcinoma cells. Cancer Res 2006; 66: 4662-4671.
38. Vermeulen L, De Sousa EMF, van der Heijden M, et al., Wnt activity defines colon cancer stem cells and is regulated by the microenvironment. Nat Cell Biol 2010; 12: 468-476.
39. Goentoro L, Kirschner MW,. Evidence that fold-change, and not absolute level, of β-catenin dictates Wnt signaling. Mol Cell 2009; 36: 872-884.
40. Sphyris N, Mani SA,. pIgR: frenemy of inflammation, EMT, and HCC progression. J Natl Cancer Inst 2012; 103: 1644-1645.
41. Kong B, Michalski CW, Hong X, et al., AZGP1 is a tumor suppressor in pancreatic cancer inducing mesenchymal-to-epithelial transdifferentiation by inhibiting TGFβ-mediated ERK signaling. Oncogene 2010; 29: 5146-5158.
42. Dumartin L, Whiteman HJ, Weeks ME, et al., AGR2 is a novel surface antigen that promotes the dissemination of pancreatic cancer cells through regulation of cathepsins B and D. Cancer Res 2011; 71: 7091-7102.
43. Sheikh AA, Vimalachandran D, Thompson CC, et al., The expression of S100A8 in pancreatic cancer-associated monocytes is associated with the Smad4 status of pancreatic cancer cells. Proteomics 2007; 7: 1929-1940.
44. Hummerich L, Muller R, Hess J, et al., Identification of novel tumour-associated genes differentially expressed in the process of squamous cell cancer development. Oncogene 2006; 25: 111-121.
45. Stairs DB, Bayne LJ, Rhoades B, et al., Deletion of p120-catenin results in a tumor microenvironment with inflammation and cancer that establishes it as a tumor suppressor gene. Cancer Cell 2012; 19: 470-483.
46. Yu M, Ting DT, Stott SL, et al., RNA sequencing of pancreatic circulating tumor cells implicates WNT signaling in metastasis. Nature 2012; 487: 510-513.This reference is cited only in the Supplementary material.