Activation of Wnt signalling in stroma from pancreatic cancer identified by gene expression profiling

Journal of Cellular and Molecular Medicine

Volumn 12, Issue 6B, 2008, Pages 2823-2835

  Pilarsky, Christian ^a   Ammerpohl, Ole ^b   Sipos, Bence ^b   Dahl, Edgar ^c   Hartmann, Arndt ^d   Wellmann, Axel ^c   Braunschweig, Till ^c   Löhr, Matthias ^e   Jesnowski, Ralf ^f   Friess, Helmut ^e   Wente, Moritz Nicolas ^e   Kristiansen, Glen ^g   Jahnke, Beatrix ^a   Denz, Axel ^a   Rückert, Felix ^a   Schackert, Hans K ^a   Klöppel, Günter ^b   Kalthoff, Holger ^b   Saeger, Hans Detlev ^a   Grützmann, Robert ^a  

^a UNIVERSITY HOSPITAL CARL GUSTAV CARUS   (Germany)

^b UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^c UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^d UNIVERSITY OF REGENSBURG   (Germany)

^e UNIVERSITY OF HEIDELBERG   (Germany)

^f GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^g CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Chronic pancreatitis; Expression profiling; Microarray; Microdissection; Pancreatic ductal adenocarcinoma; Stroma; WNT5a

Indexed keywords

WNT PROTEIN;

ARTICLE; CLUSTER ANALYSIS; COCULTURE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HUMAN; IMMUNOHISTOCHEMISTRY; METABOLISM; PANCREAS TUMOR; PATHOLOGY; REPRODUCIBILITY; SIGNAL TRANSDUCTION; STROMA CELL; TUMOR CELL LINE; TUMOR GENE;

CELL LINE, TUMOR; CLUSTER ANALYSIS; COCULTURE TECHNIQUES; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, NEOPLASM; HUMANS; IMMUNOHISTOCHEMISTRY; PANCREATIC NEOPLASMS; REPRODUCIBILITY OF RESULTS; SIGNAL TRANSDUCTION; STROMAL CELLS; WNT PROTEINS;

EID: 55249103738     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2008.00289.x     Document Type: Article

References (49)

1. Jemal A, Siegel R, Ward E, Murray T, Xu J, Smigal C, Thun MJ. Cancer statistics, 2006. CA Cancer J Clin. 2006 56 : 106 30.
2. Lohr M. Is it possible to survive pancreatic cancer? Nat Clin Pract Gastroenterol Hepatol. 2006 3 : 236 7.
3. Moore PS, Beghelli S, Zamboni G, Scarpa A. Genetic abnormalities in pancreatic cancer. Mol Cancer. 2003 2 : 7.
4. Chu GC, Kimmelman AC, Hezel AF, Depinho RA. Stromal biology of pancreatic cancer. J Cell Biochem. 2007 101 : 887 907.
5. Kenny PA, Bissell MJ. Tumor reversion: correction of malignant behavior by microenvironmental cues. Int J Cancer. 2003 107 : 688 95.
6. Tlsty TD. Stromal cells can contribute oncogenic signals. Semin Cancer Biol. 2001 11 : 97 104.
7. Fukino K, Shen L, Matsumoto S, Morrison CD, Mutter GL, Eng C. Combined total genome loss of heterozygosity scan of breast cancer stroma and epithelium reveals multiplicity of stromal targets. Cancer Res. 2004 64 : 7231 6.
8. Ohuchida K, Mizumoto K, Murakami M, Qian LW, Sato N, Nagai E, Matsumoto K, Nakamura T, Tanaka M. Radiation to stromal fibroblasts increases invasiveness of pancreatic cancer cells through tumorstromal interactions. Cancer Res. 2004 64 : 3215 22.
9. Skrzydlewska E, Sulkowska M, Koda M, Sulkowski S. Proteolytic- antiproteolytic balance and its regulation in carcinogenesis. World J Gastroenterol. 2005 11 : 1251 66.
10. Micke P, Ostman A. Tumour-stroma interaction: cancer-associated fibroblasts as novel targets in anti-cancer therapy? Lung cancer. 2004 45 Suppl 2 : S163 75.
11. Lohr M, Schmidt C, Ringel J, Kluth M, Muller P, Nizze H, Jesnowski R. Transforming growth factor-beta1 induces desmoplasia in an experimental model of human pancreatic carcinoma. Cancer Res. 2001 61 : 550 5.
12. Katoh M, Katoh M. STAT3-induced WNT5A signaling loop in embryonic stem cells, adult normal tissues, chronic persistent inflammation, rheumatoid arthritis and cancer. Int J Mol Med. 2007 19 : 273 8.
13. Wong SC, Lo ES, Lee KC, Chan JK, Hsiao WL. Prognostic and diagnostic significance of beta-catenin nuclear immunos-taining in colorectal cancer. Clin Cancer Res. 2004 10 : 1401 8.
14. Watanabe I, Hasebe T, Sasaki S, Konishi M, Inoue K, Nakagohri T, Oda T, Mukai K, Kinoshita T. Advanced pancreatic ductal cancer: fibrotic focus and beta-catenin expression correlate with outcome. Pancreas. 2003 26 : 326 33.
15. Grutzmann R, Boriss H, Ammerpohl O, Luttges J, Kalthoff H, Schackert H, Kloppel G, Saeger H, Pilarsky C. Meta-analysis of microarray data on pancreatic cancer defines a set of commonly dysregulated genes. Oncogene. 2005 24 : 5079 88.
16. Brandt R, Grutzmann R, Bauer A, Jesnowski R, Ringel J, Lohr M, Pilarsky C, Hoheisel JD. DNA microarray analysis of pancreatic malignancies. Pancreatology. 2004 4 : 587 97.
17. Nakamura T, Fidler IJ, Coombes KR. Gene expression profile of metastatic human pancreatic cancer cells depends on the organ microenvironment. Cancer Res. 2007 67 : 139 48.
18. Nakamura T, Furukawa Y, Nakagawa H, Tsunoda T, Ohigashi H, Murata K, Ishikawa O, Ohgaki K, Kashimura N, Miyamoto M, Hirano S, Kondo S, Katoh H, Nakamura Y, Katagiri T. Genome-wide cDNA microarray analysis of gene expression profiles in pancreatic cancers using populations of tumor cells and normal ductal epithelial cells selected for purity by laser microdissection. Oncogene. 2004 23 : 2385 400.
19. Buchholz M, Braun M, Heidenblut A, Kestler HA, Kloppel G, Schmiegel W, Hahn SA, Luttges J, Gress TM. Transcriptome analysis of microdissected pancreatic intraepithelial neoplastic lesions. Oncogene. 2005 24 : 6626 36.
20. Missiaglia E, Blaveri E, Terris B, Wang YH, Costello E, Neoptolemos JP, Crnogorac-Jurcevic T, Lemoine NR. Analysis of gene expression in cancer cell lines identifies candidate markers for pancreatic tumorigenesis and metastasis. Int J Cancer. 2004 112 : 100 12.
21. Grutzmann R, Pilarsky C, Ammerpohl O, Luttges J, Bohme A, Sipos B, Foerder M, Alldinger I, Jahnke B, Schackert HK, Kalthoff H, Kremer B, Kloppel G, Saeger HD. Gene expression profiling of microdissected pancreatic ductal carcinomas using high-density DNA microarrays. Neoplasia. 2004 6 : 611 22.
22. Kloppel G. Chronic pancreatitis of alcoholic and nonalcoholic origin. Semin Diagn Pathol. 2004 21 : 227 36.
23. Kapischke M, Prinz K, Tepel J, Tensfeldt J, Schulz T. Precoating of alloplastic materials with living human fibroblasts-a feasibility study. Surg Endosc. 2005 19 : 791 7.
24. Jesnowski R, Furst D, Ringel J, Chen Y, Schrodel A, Kleeff J, Kolb A, Schareck WD, Lohr M. Immortalization of pancreatic stellate cells as an in vitro model of pancreatic fibrosis: deactivation is induced by matrigel and N-acetylcysteine. Lab Invest. 2005 85 : 1276 91.
25. Li C, Wong WH. Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc Natl Acad Sci USA. 2001 98 : 31 6.
26. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA. 2001 98 : 5116 21.
27. Fink L, Seeger W, Ermert L, Hanze J, Stahl U, Grimminger F, Kummer W, Bohle RM. Real-time quantitative RT-PCR after laser-assisted cell picking. Nat Med. 1998 4 : 1329 33.
28. Stoehr R, Wissmann C, Suzuki H, Knuechel R, Krieg RC, Klopocki E, Dahl E, Wild P, Blaszyk H, Sauter G, Simon R, Schmitt R, Zaak D, Hofstaedter F, Rosenthal A, Baylin SB, Pilarsky C, Hartmann A. Deletions of chromosome 8p and loss of sFRP1 expression are progression markers of papillary bladder cancer. Lab Invest. 2004 84 : 465 78.
29. Klopocki E, Kristiansen G, Wild PJ, Klaman I, Castanos-Velez E, Singer G, Stohr R, Simon R, Sauter G, Leibiger H, Essers L, Weber B, Hermann K, Rosenthal A, Hartmann A, Dahl E. Loss of SFRP1 is associated with breast cancer progression and poor prognosis in early stage tumors. Int J Oncol. 2004 25 : 641 9.
30. Al-Shahrour F, Minguez P, Vaquerizas JM, Conde L, Dopazo J. BABELOMICS: a suite of web tools for functional annotation and analysis of groups of genes in high-throughput experiments. Nucleic Acids Res. 2005 33 : W460 4.
31. Ripka S, Konig A, Buchholz M, Wagner M, Sipos B, Kloppel G, Downward J, Gress T, Michl P. WNT5A - target of CUTL1 and potent modulator of tumor cell migration and invasion in pancreatic cancer. Carcinogenesis. 2007 28 : 1178 87.
32. Kim JB, Stein R, O'Hare MJ. Tumourstromal interactions in breast cancer: the role of stroma in tumourigenesis. Tumour Biol. 2005 26 : 173 85.
33. Bilalovic N, Vranic S, Serdarevic F, Foco F. The role of the stroma in carcinogenesis. Bosn J Basic Med Sci. 2006 6 : 33 8.
34. Chung LW, Baseman A, Assikis V, Zhau HE. Molecular insights into prostate cancer progression: the missing link of tumor microenvironment. J Urol. 2005 173 : 10 20.
35. Basset P, Bellocq JP, Lefebvre O, Noel A, Chenard MP, Wolf C, Anglard P, Rio MC. Stromelysin-3: a paradigm for stromaderived factors implicated in carcinoma progression. Crit Rev Oncol Hematol. 1997 26 : 43 53.
36. Ricci F, Kern SE, Hruban RH, Iacobuzio-Donahue CA. Stromal responses to carcinomas of the pancreas: juxtatumoral gene expression conforms to the infiltrating pattern and not the biologic subtype. Cancer Biol Ther. 2005 4 : 302 7.
37. Allinen M, Beroukhim R, Cai L, Brennan C, Lahti-Domenici J, Huang H, Porter D, Hu M, Chin L, Richardson A, Schnitt S, Sellers WR, Polyak K. Molecular characterization of the tumor microenvironment in breast cancer. Cancer Cell. 2004 6 : 17 32.
38. Binkley CE, Zhang L, Greenson JK, Giordano TJ, Kuick R, Misek D, Hanash S, Logsdon CD, Simeone DM. The molecular basis of pancreatic fibrosis: common stromal gene expression in chronic pan-creatitis and pancreatic adenocarcinoma. Pancreas. 2004 29 : 254 63.
39. Veeck J, Niederacher D, An H, Klopocki E, Wiesmann F, Betz B, Galm O, Camara O, Durst M, Kristiansen G, Huszka C, Knuchel R, Dahl E. Aberrant methylation of the Wnt antagonist SFRP1 in breast cancer is associated with unfavourable prognosis. Oncogene. 2006 25 : 3479 88.
40. Sato N, Fukushima N, Maitra A, Matsubayashi H, Yeo CJ, Cameron JL, Hruban RH, Goggins M. Discovery of novel targets for aberrant methylation in pancreatic carcinoma using high-throughput microarrays. Cancer Res. 2003 63 : 3735 42.
41. Rodriguez J, Esteve P, Weinl C, Ruiz JM, Fermin Y, Trousse F, Dwivedy A, Holt C, Bovolenta P. SFRP1 regulates the growth of retinal ganglion cell axons through the Fz2 receptor. Nat Neurosci. 2005 8 : 1301 9.
42. Mikels AJ, Nusse R. Purified Wnt5a protein activates or inhibits beta-catenin-TCF signaling depending on receptor context. PLoS Biol. 2006 4 : 570 82.
43. Pukrop T, Klemm F, Hagemann T, Gradl D, Schulz M, Siemes S, Trumper L, Binder C. Wnt5a signaling is critical for macrophage-induced invasion of breast cancer cell lines. Proc Natl Acad Sci USA. 2006 103 : 5454 9.
44. Kayed H, Kleeff J, Osman T, Keleg S, Buchler MW, Friess H. Hedgehog signaling in the normal and diseased pancreas. Pancreas. 2006 32 : 119 29.
45. Reddy S, Andl T, Bagasra A, Lu MM, Epstein DJ, Morrisey EE, Millar SE. Characterization of Wnt gene expression in developing and postnatal hair follicles and identification of Wnt5a as a target of Sonic hedgehog in hair follicle morphogenesis. Mech Dev. 2001 107 : 69 82.
46. Yang Y, Topol L, Lee H, Wu J. Wnt5a and Wnt5b exhibit distinct activities in coordinating chondrocyte proliferation and differentiation. Development. 2003 130 : 1003 15.
47. Zheng Q, Zhou G, Morello R, Chen Y, Garcia-Rojas X, Lee B. Type X collagen gene regulation by Runx2 contributes directly to its hypertrophic chondrocyte-specific expression in vivo. J Cell Biol. 2003 162 : 833 42.
48. Fischer H, Stenling R, Rubio C, Lindblom A. Colorectal carcinogenesis is associated with stromal expression of COL11A1 and COL5A2. Carcinogenesis. 2001 22 : 875 8.
49. Kristiansen G, Jacob J, Buckendahl AC, Grutzmann R, Alldinger I, Sipos B, Kloppel G, Bahra M, Langrehr JM, Neuhaus P, Dietel M, Pilarsky C. Peroxisome proliferator-activated receptor gamma is highly expressed in pancreatic cancer and is associated with shorter overall survival times. Clin Cancer Res. 2006 12 : 6444 51.