Lgr5 expression, cancer stem cells and pancreatic cancer: Results from biological and computational analyses

Future Oncology

Volumn 11, Issue 7, 2015, Pages 1037-1045

  Andrikou, Kalliopi ^a   Santoni, Matteo ^a   Piva, Francesco ^a   Bittoni, Alessandro ^a   Lanese, Andrea ^a   Pellei, Chiara ^a   Conti, Alessandro ^a   Loretelli, Cristian ^a   Mandolesi, Alessandra ^a   Giulietti, Matteo ^a   Scarpelli, Marina ^a   Principato, Giovanni ^a   Falconi, Massimo ^a   Cascinu, Stefano ^a  

^a UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

Author keywords

cancer stem cell; embryonic signaling pathways; Lgr5; overall survival; pancreatic ductal adenocarcinoma

Indexed keywords

CELL SURFACE RECEPTOR; CELL SURFACE RECEPTOR LGR5; UNCLASSIFIED DRUG; G PROTEIN COUPLED RECEPTOR; LGR5 PROTEIN, HUMAN; TUMOR MARKER;

ADULT; AGED; ARTICLE; BIOINFORMATICS; CANCER STEM CELL; CANCER SURVIVAL; FEMALE; GENE EXPRESSION; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; MULTIVARIATE ANALYSIS; PANCREAS ADENOCARCINOMA; PREDICTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UNIVARIATE ANALYSIS; ADENOCARCINOMA; GENETICS; METABOLISM; MIDDLE AGED; PANCREAS CARCINOMA; PANCREAS TUMOR; REAL TIME POLYMERASE CHAIN REACTION; VERY ELDERLY;

ADENOCARCINOMA; AGED; AGED, 80 AND OVER; BIOMARKERS, TUMOR; CARCINOMA, PANCREATIC DUCTAL; FEMALE; HUMANS; MALE; MIDDLE AGED; NEOPLASTIC STEM CELLS; PANCREATIC NEOPLASMS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, G-PROTEIN-COUPLED;

EID: 84925822533     PISSN: 14796694     EISSN: 17448301     Source Type: Journal    
DOI: 10.2217/fon.15.27     Document Type: Article

References (58)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics. CA Cancer J. Clin. 63(1), 11-30 (2013).
2. Hermann PC, Huber SL, Herrler T et al. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 1(3), 313-323 (2007).
3. Clarke MF, Fuller M. Stem cells and cancer: Two faces of eve. Cell 124(6), 1111-1115 (2006).
4. Takebe N, Ivy SP. Controversies in cancer stem cells: Targeting embryonic signaling pathways. Clin. Cancer Res. 16(12), 3106-3112 (2010).
5. Penchev VR, Rasheed ZA, Maitra A, Matsui W. Heterogeneity and targeting of pancreatic cancer stem cells. Clin. Cancer Res. 18(16), 4277-4284 (2012).
6. Hao HX, Xie Y, Zhang Y et al. ZNRF3 promotes Wnt receptor turnover in an R-spondin-sensitive manner. Nature 485(7397), 195-200 (2012).
7. Koo BK, Spit M, Jordens I et al. Tumour suppressor RNF43 is a stem-cell E3 ligase that induces endocytosis of Wnt receptors. Nature 488(7413), 665-669 (2012).
8. Carmon KS, Gong X, Lin Q, Thomas A, Liu Q. R-spondins function as ligands of the orphan receptors LGR4 and LGR5 to regulate Wnt/beta-catenin signaling. Proc. Natl Acad. Sci. USA 108(28), 11452-11457 (2011).
9. Clevers H, Nusse R. Wnt/ß-catenin signaling and disease. Cell 149(6), 1192-1205 (2012).
10. Wu XS, Xi HQ, Chen L. Lgr5 is a potential marker of colorectal carcinoma stem cells that correlates with patient survival. World J. Surg. Oncol. 10, 244 (2012).
11. Nakata S, Campos B, Bageritz J et al. LGR5 is a marker of poor prognosis in glioblastoma and is required for survival of brain cancer stem-like cells. Brain Pathol. 23(1), 60-72 (2013).
12. SABiosciences. www.SABiosciences.com
13. Fagerland MW, Hosmer DW, Bofin AM. Multinomial goodness-of-fit tests for logistic regression models. Stat. Med. 27(21), 4238-4253 (2008).
14. Mickey RM, Greenland S. The impact of confounder selection criteria on effect estimation. Am. J. Epidemiol. 129(1), 125-137 (1989).
15. Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30(1), 207-210 (2002).
16. NCBI. www.ncbi.nlm.nih.gov/geo/
17. Pei H, Li L, Fridley BL, Jenkins GD et al. FKBP51 affects cancer cell response to chemotherapy by negatively regulating Akt. Cancer Cell 16(3), 259-266 (2009).
18. Badea L, Herlea V, Dima SO, Dumitrascu T, Popescu I. Combined gene expression analysis of whole-tissue and microdissected pancreatic ductal adenocarcinoma identifies genes specifically overexpressed in tumor epithelia. Hepatogastroenterology 55(88), 2016-2027 (2008).
19. Su AI, Wiltshire T, Batalov S et al. A gene atlas of the mouse and human proteinencoding transcriptomes. Proc. Natl Acad. Sci. USA 101(16), 6062-6067 (2004).
20. Zhang G, Schetter A, He P et al. DPEP1 inhibits tumor cell invasiveness, enhances chemosensitivity and predicts clinical outcome in pancreatic ductal adenocarcinoma. PLoS ONE 7(2), e31507 (2012).
21. Laboratory for System Biology and Medicine. www.lsbm.org
22. Strausberg RL1, Buetow KH, Emmert-Buck MR, Klausner RD. The cancer genome anatomy project: building an annotated gene index. Trends Genet. 16(3), 103-106 (2000).
23. Uhlen M, Oksvold P, Fagerberg L et al. Towards a knowledge-based Human Protein Atlas. Nat. Biotechnol. 28, 1248-1250 (2010).
24. Protein Atlas. www.proteinatlas.org
25. Kandasamy K, Keerthikumar S, Goel R et al. Human Proteinpedia: A unified discovery resource for proteomics research. Nucleic Acids Res. 37, D773-D781 (2009).
26. Human Proteinpedia. www.humanproteinpedia.org
27. Peri S, Navarro JD, Amanchy R et al. Development of human protein reference database as an initial platform for approaching systems biology in humans. Genome Res. 13(10), 2363-2371 (2003).
28. Human Protein Reference Database. www.hprd.org
29. Frézal J. Genatlas database, genes and development defects. C. R. Acad. Sci. III 321(10), 805-817 (1998).
30. Gene Atlas. www.genatlas.org
31. Jackstadt R, Roh S, Neumann J et al. AP4 is a mediator of epithelial-mesenchymal transition and metastasis in colorectal cancer. J. Exp. Med. 210(7), 1331-1350 (2013).
32. Hahn S, Jackstadt R, Siemens H, Hunten S, Hermeking H. SNAIL and miR-34a feed-forward regulation of ZNF281/ZBP99 promotes epithelial-mesenchymal transition. EMBO J. 32(23), 3079-3095 (2013).
33. Kember K, Prasetyanti PR, De Lau W, Rodermond H, Clevers H, Medema JP. Monoclonal antibodies against Lgr5 identify human colorectal cancer stem cells. Stem Cells 30(11), 2378-2386 (2012).
34. Zheng ZX, Sun Y, Bu ZD et al. Intestinal stem cell marker LGR5 expression during gastric carcinogenesis. World J. Gastroenterol. 19(46), 8714-8721 (2013).
35. Fujishita T, Aoki K, Lane HA, Aoki M, Taketo MM. Inhibition of the mTORC1 pathway suppresses intestinal polyp formation and reduces mortality in Apc?716 mice. Proc. Natl Acad. Sci. USA 105(36), 13544-13549 (2008).
36. Ko SB, Azuma S, Yokoyama Y et al. Inflammation increases cells expressing ZSCAN4 and progenitor cell markers in the adult pancreas. Am. J Physiol. Gastrointest. Liver Physiol. 304(12), G1103-G1116 (2013).
37. Pasca di Magliano M, Biankin AV, Heiser PW et al. Common activation of canonical Wnt signaling in pancreatic adenocarcinoma. PLoS ONE 2(11), e1155 (2007).
38. Morris JP, Cano DA, Sekine S, Wang SC, Hebrok M. Beta-catenin blocks Krasdependent reprogramming of acini into pancreatic cancer precursor lesions in mice. J. Clin. Invest. 120(2), 508-520 (2010).
39. Simon E, Petke D, Boger C et al. The spatial distribution of LGR5+ cells correlates with gastric cancer progression. PLoS ONE 7(4), e35486 (2012).
40. Mizuno N, Yatabe Y, Hara K et al. Cytoplasmic expression of LGR5 in pancreatic adenocarcinoma. Front. Physiol. 4, 269 (2013).
41. Saigusa S, Inoue Y, Tanaka K et al. Significant correlation between LKB1 and LGR5 gene expression and the association with poor recurrence-free survival in rectal cancer after preoperative chemoradiotherapy. J. Cancer Res. Clin. Oncol. 139(1), 131-138 (2012).
42. Takahashi H, Ishii H, Nishida N et al. Significance of Lgr5 (+ve) cancer stem cells in the colon and rectum. Ann. Surg. Oncol. 18(4), 1166-1174 (2011).
43. Zheng ZX, Sun Y, Bu ZD et al. Intestinal stem cell marker LGR5 expression during gastric carcinogenesis. World J. Gastroenterol. 19(46), 8714-8721 (2013).
44. Becker L, Huang Q, Mashimo H. Lgr5, an intestinal stem cell marker, is abnormally expressed in Barrett's esophagus and esophageal adenocarcinoma. Dis. Esophagus. 23(2), 168-174 (2010).
45. Ryuge S, Sato Y, Jiang SX et al. The clinicopathological significance of Lgr5 expression in lung adenocarcinoma. Lung Cancer 82(1), 143-148 (2013).
46. Xi HQ, Cai AZ, Wu XS et al. Leucine-rich repeat-containing G-protein-coupled receptor is associated with invasion, metastasis, and could be a potential therapeutic target in human gastric cancer. Br. J. Cancer 110(8), 2011-2020 (2014).
47. Chen PH, Chen X, Lin Z, Fang D, He X. The structural basis of R-spondin recognition by LGR5 and RNF43. Genes Dev. 27(12), 1345-1350 (2013).
48. Rot S, Taubert H, Bache M et al. A novel splice variant of the stem cell marker LGR5/ GPR49 is correlated with the risk of tumor-related death in soft-tissue sarcoma patients. BMC Cancer 11, 429 (2011).
49. Wang P, Zhang J, Zhang L et al. MicroRNA 23b regulates autophagy associated with radioresistance of pancreatic cancer cells. Gastroenterology 145(5), 1133-1143 (2013).
50. Shen WW, Zeng Z, Zhu WX, Fu GH. MiR-142-3p functions as a tumor suppressor by targeting CD133, ABCG2, and Lgr5 in colon cancer cells. J. Mol. Med. (Berl). 91(8), 989-1000 (2013).
51. Endo K, Weng H, Kito N, Fukushima Y, Iwai N. MiR-216a and miR-216b as markers for acute phased pancreatic injury. Biomed. Res. 34(4), 179-188 (2013).
52. Szafranska AE, Davison TS, John J et al. MicroRNA expression alterations are linked to tumorigenesis and non-neoplastic processes in pancreatic ductal adenocarcinoma. Oncogene 26(30), 4442-4452 (2007).
53. Roldo C, Missiaglia E, Hagan JP et al. MicroRNA expression abnormalities in pancreatic endocrine and acinar tumors are associated with distinctive pathologic features and clinical behavior. J. Clin. Oncol. 24(29), 4677-4684 (2006).
54. Lee YS, Dutta A. MicroRNAs in cancer. Annu. Rev. Pathol. 4, 199-227 (2009).
55. Philip PA, Mooney M, Jaffe D et al. Consensus report of the national cancer institute clinical trials planning meeting on pancreas cancer treatment. J. Clin. Oncol. 27, 5660-5669 (2009).
56. Hong SP, Wen J, Bang S, Park S, Song SY. CD44-positive cells are responsible for gemcitabine resistance in pancreatic cancer cells. Int. J. Cancer 125(10), 2323-2331 (2009).
57. Jimeno A, Feldmann G, Suarez-Gauthier A et al. A direct pancreatic cancer xenograft model as a platform for cancer stem cell therapeutic development. Mol. Cancer Ther. 9, 2582-2592 (2009).
58. Mueller MT, Hermann PC, Witthauer J et al. Combined targeted treatment to eliminate tumorigenic cancer stem cells in human pancreatic cancer. Gastroenterology 137, 1102-1113 (2009).