Human Pancreatic Cancer Contains a Side Population Expressing Cancer Stem Cell-Associated and Prognostic Genes

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Van den broeck, Anke ^a,b   Vankelecom, Hugo ^b   Van Delm, Wouter ^b   Gremeaux, Lies ^b   Wouters, Jasper ^b   Allemeersch, Joke ^b   Govaere, Olivier ^a   Roskams, Tania ^a   Topal, Baki ^a  

^a UNIVERSITY HOSPITALS LEUVEN   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

CD31 ANTIGEN; CD45 ANTIGEN; CHEMOKINE RECEPTOR CXCR4; MULTIDRUG RESISTANCE PROTEIN 1;

ABCB1 GENE; ARTICLE; CANCER PROGNOSIS; CANCER STEM CELL; CELL TYPE; CXCR4 GENE; DISEASE FREE SURVIVAL; DOWN REGULATION; DRUG RESISTANCE; ENDOTHELIUM CELL; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCOMPETENT CELL; MAIN POPULATION CELL; OVERALL SURVIVAL; PANCREAS ADENOCARCINOMA; SIDE POPULATION CELL; TUMOR CELL; UPREGULATION;

ADULT; AGED; AGED, 80 AND OVER; CARCINOMA, PANCREATIC DUCTAL; CASE-CONTROL STUDIES; FEMALE; GENE EXPRESSION PROFILING; HUMANS; IMMUNOPHENOTYPING; MALE; MIDDLE AGED; NEOPLASTIC STEM CELLS; P-GLYCOPROTEIN; PANCREATIC NEOPLASMS; PROGNOSIS; RECEPTORS, CXCR4; SIDE-POPULATION CELLS;

EID: 84884237412     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0073968     Document Type: Article

References (38)

1. Jemal A, Bray F, (2011) Center MM, Ferlay J, Ward E, et al (2011) Global cancer statistics. CA Cancer J Clin 61: 69-90.
2. Hirschmann-Jax C, Foster AE, Wulf GG, Nuchtern JG, Jax TW, et al. (2004) A distinct "side population" of cells with high drug efflux capacity in human tumor cells. Proc Natl Acad Sci U S A 101: 14228-33.
3. Chen J, Hersmus N, Van Duppen V, Caesens P, Denef C, et al. (2005) The adult pituitary contains a cell population displaying stem/progenitor cell and early embryonic characteristics. Endocrinology 146: 3985-98.
4. Sergeant G, Vankelecom H, Gremeaux L, Topal B, (2009) Cancer stem cells in pancreatic ductal adenocarcinoma. Nat Rev Clin Oncol 6: 580-586.
5. Li C, Heidt DG, Dalerba P, Burant CF, Zhang L, et al. (2007) Identification of pancreatic cancer stem cells. Cancer Res 67: 1030-7.
6. Hermann PC, Huber SL, Herrler T, Aicher A, Ellwart JW, et al. (2007) Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell stem cell 1: 313-23.
7. Wu C, Alman BA, (2008) Side population cells in human cancers. Cancer Lett 268: 1-9.
8. Zhou J, Wang CY, Liu T, Wu B, Zhou F, et al. (2008) Persistence of side population cells with high drug efflux capacity in pancreatic cancer. World J Gastroenterol 14: 925-30.
9. Yao J, Cai HH, Wei JS, An Y, Ji ZL, et al. (2010) Side population in the pancreatic cancer cell lines SW1990 and CFPAC-1 is enriched with cancer stem-like cells. Oncol Rep 23: 1375-82.
10. Zhang SN, Huang FT, Huang YJ, Zhong W, Yu Z, (2010) Characterization of a cancer stem cell-like side population derived from human pancreatic adenocarcinoma cells. Tumori 96: 985-92.
11. Wang YH, Li F, Luo B, Wang XH, Sun HC, et al. (2009) A side population of cells from a human pancreatic carcinoma cell line harbors cancer stem cell characteristics. Neoplasma 56: 371-8.
12. Van den broeck A, Gremeaux L, Topal B, Vankelecom H, (2012) Human pancreatic adenocarcinoma contains a side population resistant to gemcitabine. BMC Cancer 12: 354.
13. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, et al. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-64.
14. Smyth GK, (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Gen Mol Biol 3: 1-29.
15. Shi L, Reid LH, Jones WD, Shippy R, Warrington JA, et al. (2006) The MicroArray Quality Control (MAQC) project shows inter- and intraplatform reproducibility of gene expression measurements. Nat Biotechnol 24: 1151-61.
16. Saeys Y, Inza I, Larranaga P, (2007) A review of feature selection techniques in bioinformatics. Bioinformatics 23: 2507-17.
17. Wessels LF, Reinders MJ, Hart AA, Veenman CJ, Dai H, et al. (2005) A protocol for building and evaluating predictors of disease state based on microarray data. Bioinformatics 21: 3755-62.
18. Nitsch D, Tranchevent LC, Goncalves JP, Vogt JK, Madeira SC, et al. (2011) PINTA: a web server for network-based gene prioritization from expression data. Nucleic Acids Res 39: W334-8.
19. Kulkarni MM, (2011) Digital multiplexed gene expression analysis using the NanoString nCounter system. Curr Protoc Mol Biol 94: 25B.10.1-25B.10.17.
20. Chen J, Gremeaux L, Fu Q, Liekens D, Van Laere S, et al. (2009) Pituitary progenitor cells tracked down by side population dissection. Stem Cells 27: 1182-95.
21. Kabashima A, Higuchi H, Takaishi H, Matsuzaki Y, Suzuki S, et al. (2009) Side population of pancreatic cancer cells predominates in TGF-beta-mediated epithelial to mesenchymal transition and invasion. Int J Cancer 124: 2771-9.
22. Bleau AM, Hambardzumyan D, Ozawa T, Fomchenko EI, Huse JT, et al. (2009) PTEN/PI3K/Akt pathway regulates the side population phenotype and ABCG2 activity in glioma tumor stem-like cells. Cell Stem Cell 4: 226-35.
23. Carmon KS, Gong X, Lin Q, Thomas A, Liu Q, (2011) R-spondins function as ligands of the orphan receptors LGR4 and LGR5 to regulate Wnt/beta-catenin signaling. Proc Natl Acad Sci U S A 108: 11452-7.
24. Seymour PA, Freude KK, Tran MN, Mayes EE, Jensen J, et al. (2007) SOX9 is required for maintenance of the pancreatic progenitor cell pool. Proc Natl Acad Sci U S A 104: 1865-70.
25. Parisi S, Passaro F, Aloia L, Manabe I, Nagai R, et al. (2008) Klf5 is involved in self-renewal of mouse embryonic stem cells. J Cell Sci 121: 2629-34.
26. Li C, Wu JJ, Hynes M, Dosch J, Sarkar B, et al. (2011) c-Met is a marker of pancreatic cancer stem cells and therapeutic target. Gastroenterology 141: 2218-27 e5.
27. Hermann PC, Huber SL, Heeschen C, (2008) Metastatic cancer stem cells: a new target for anti-cancer therapy? Cell Cycle 7: 188-93.
28. Duxbury MS, Ito H, Zinner MJ, Ashley SW, Whang EE, (2004) EphA2: a determinant of malignant cellular behavior and a potential therapeutic target in pancreatic adenocarcinoma. Oncogene 23: 1448-56.
29. Iiizumi M, Hosokawa M, Takehara A, Chung S, Nakamura T, et al. (2006) EphA4 receptor, overexpressed in pancreatic ductal adenocarcinoma, promotes cancer cell growth. Cancer Sci 97: 1211-6.
30. Friess H, Yamanaka Y, Kobrin MS, Do DA, Buchler MW, et al. (1995) Enhanced erbB-3 expression in human pancreatic cancer correlates with tumor progression. Clin Cancer Res 1: 1413-20.
31. Liles JS, Arnoletti JP, Kossenkov AV, Mikhaylina A, Frost AR, et al. (2011) Targeting ErbB3-mediated stromal-epithelial interactions in pancreatic ductal adenocarcinoma. Br J Cancer 105: 523-33.
32. Ohta T, Elnemr A, Kitagawa H, Kayahara M, Takamura H, et al. (2004) Fas ligand expression in human pancreatic cancer. Oncol Rep 12: 749-54.
33. Khanna A, Mahalingam K, Chakrabarti D, Periyasamy G, (2011) Ets-1 expression and gemcitabine chemoresistance in pancreatic cancer cells. Cell Mol Biol Lett 16: 101-13.
34. Marechal R, Demetter P, Nagy N, Berton A, Decaestecker C, et al. (2009) High expression of CXCR4 may predict poor survival in resected pancreatic adenocarcinoma. Br J Cancer 100: 1444-51.
35. Lu Z, Kleeff J, Shrikhande S, Zimmermann T, Korc M, et al. (2000) Expression of the multidrug-resistance 1 (MDR1) gene and prognosis in human pancreatic cancer. Pancreas 21: 240-7.
36. Zhang H, Wang J, Cai K, Jiang L, Zhou D, et al. (2012) Downregulation of gene MDR1 by shRNA to reverse multidrug-resistance of ovarian cancer A2780 cells. J cancer Res Ther 8: 226-31.
37. Tong XZ, Wang F, Liang S, Zhang X, He JH, et al. (2012) Apatinib (YN968D1) enhances the efficacy of conventional chemotherapeutical drugs in side population cells and ABCB1-overexpressing leukemia cells. Biochem Pharmacol 83: 586-97.
38. Mohelnikova-Duchonova B, Brynchova V, Oliverius M, Honsova E, Kala Z, et al. (2013) Differences in transcript levels of ABC transporters between pancreatic adenocarcinoma and nonneoplastic tissues. Pancreas 42: 707-16.