Prostaglandin E2 Promotes Colorectal Cancer Stem Cell Expansion and Metastasis in Mice

Gastroenterology

Volumn 149, Issue 7, 2015, Pages 1884-1895.e4

  Wang, Dingzhi ^a   Fu, Lingchen ^a   Sun, Haiyan ^a   Guo, Lixia ^a   Dubois, Raymond N ^a,b  

^a ARIZONA STATE UNIVERSITY   (United States)

^b MAYO CLINIC   (United States)

Author keywords

Colon Cancer; Cyclooxygenase; NSAIDs; Tumorigenesis

Indexed keywords

ANTINEOPLASTIC AGENT; APC PROTEIN; CD133 ANTIGEN; CELECOXIB; HERMES ANTIGEN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LENTIVIRUS VECTOR; MITOGEN ACTIVATED PROTEIN KINASE 3; ONO AE 3208; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE P85ALPHA; PROSTAGLANDIN E RECEPTOR 4; PROSTAGLANDIN E2; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; AUTACOID; CYCLOOXYGENASE 2 INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE; PTGER4 PROTEIN, HUMAN; TUMOR MARKER;

ANIMAL CELL; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER PATIENT; CANCER STEM CELL; CANCER TISSUE; CECUM; CECUM TUMOR; CELL SELECTION; COLORECTAL CANCER; COLORECTAL CANCER CELL LINE; COLORECTAL CARCINOMA; COLORECTAL POLYP; CONTROLLED STUDY; FLOW CYTOMETRY; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; INJECTION; LIVER METASTASIS; MALE; MASS SPECTROMETRY; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; STEM CELL EXPANSION; TUMOR VOLUME; TUMOR XENOGRAFT; ANIMAL; CARCINOMA; CELL MOTION; CELL PROLIFERATION; COLORECTAL NEOPLASMS; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; LIVER NEOPLASMS; METABOLISM; NONOBESE DIABETIC MOUSE; PATHOLOGY; RNA INTERFERENCE; SCID MOUSE; SECONDARY; TRANSGENIC MOUSE; TUMOR CELL CULTURE; TUMOR CELL LINE; TUMOR SUPPRESSOR GENE; XENOGRAFT;

ANIMALS; BIOMARKERS, TUMOR; CARCINOMA; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; COLORECTAL NEOPLASMS; CYCLOOXYGENASE 2 INHIBITORS; DINOPROSTONE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, APC; HETEROGRAFTS; HUMANS; INFLAMMATION MEDIATORS; LIVER NEOPLASMS; MALE; MICE, INBRED NOD; MICE, SCID; MICE, TRANSGENIC; MITOGEN-ACTIVATED PROTEIN KINASES; NEOPLASTIC STEM CELLS; NF-KAPPA B; PHOSPHATIDYLINOSITOL 3-KINASE; RECEPTORS, PROSTAGLANDIN E, EP4 SUBTYPE; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSFECTION; TUMOR BURDEN; TUMOR CELLS, CULTURED;

EID: 84952975799     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2015.07.064     Document Type: Article

References (46)

1. P.A. Newcomb, J. Baron, M. Cotterchio, and et al. Colon Cancer Family Registry: an international resource for studies of the genetic epidemiology of colon cancer Cancer Epidemiol Biomarkers Prev 16 2007 2331 2343
2. S. Ogino, G.J. Kirkner, K. Nosho, and et al. Cyclooxygenase-2 expression is an independent predictor of poor prognosis in colon cancer Clin Cancer Res 14 2008 8221 8227
3. D.J. de Groot, E.G. de Vries, H.J. Groen, and et al. Non-steroidal anti-inflammatory drugs to potentiate chemotherapy effects: from lab to clinic Crit Rev Oncol Hematol 61 2007 52 69
4. D. Wang, and R.N. DuBois The role of COX-2 in intestinal inflammation and colorectal cancer Oncogene 29 2010 781 788
5. J. Cuzick, F. Otto, J.A. Baron, and et al. Aspirin and non-steroidal anti-inflammatory drugs for cancer prevention: an international consensus statement Lancet Oncol 10 2009 501 507
6. B. Rigas, I.S. Goldman, and L. Levine Altered eicosanoid levels in human colon cancer J Lab Clin Med 122 1993 518 523
7. D. Wang, and R.N. Dubois Cyclooxygenase-2: a potential target in breast cancer Semin Oncol 31 2004 64 73
8. T.L. McLemore, W.C. Hubbard, C.L. Litterst, and et al. Profiles of prostaglandin biosynthesis in normal lung and tumor tissue from lung cancer patients Cancer Res 48 1988 3140 3147
9. M. Hambek, M. Baghi, J. Wagenblast, and et al. Inverse correlation between serum PGE2 and T classification in head and neck cancer Head Neck 29 2007 244 248
10. Q. Cai, Y.T. Gao, W.H. Chow, and et al. Prospective study of urinary prostaglandin E2 metabolite and colorectal cancer risk J Clin Oncol 24 2006 5010 5016
11. M.J. Shrubsole, Q. Cai, W. Wen, and et al. Urinary prostaglandin E2 metabolite and risk for colorectal adenoma Cancer Prev Res (Phila) 5 2012 336 342
12. J.C. Johnson, C.R. Schmidt, M.J. Shrubsole, and et al. Urine PGE-M: a metabolite of prostaglandin E2 as a potential biomarker of advanced colorectal neoplasia Clin Gastroenterol Hepatol 4 2006 1358 1365
13. L.M. Dong, X.O. Shu, Y.T. Gao, and et al. Urinary prostaglandin E2 metabolite and gastric cancer risk in the Shanghai women's health study Cancer Epidemiol Biomarkers Prev 18 2009 3075 3078
14. S. Kim, J.A. Taylor, G. Milne, and et al. Association between urinary prostaglandin E2 metabolite and breast cancer risk: a prospective, case-cohort study of postmenopausal women Cancer Prev Res (Phila) 6 2013 511 518
15. P.G. Morris, X.K. Zhou, G.L. Milne, and et al. Increased levels of urinary PGE-M, a biomarker of inflammation, occur in association with obesity, aging, and lung metastases in patients with breast cancer Cancer Prev Res (Phila) 6 2013 428 436
16. V.D. Kekatpure, J.O. Boyle, X.K. Zhou, and et al. Elevated levels of urinary prostaglandin e metabolite indicate a poor prognosis in ever smoker head and neck squamous cell carcinoma patients Cancer Prev Res (Phila) 2 2009 957 965
17. D. Wang, and R.N. DuBois Eicosanoids and cancer Nat Rev Cancer 10 2010 181 193
18. S.K. Singh, I.D. Clarke, M. Terasaki, and et al. Identification of a cancer stem cell in human brain tumors Cancer Res 63 2003 5821 5828
19. L. Ricci-Vitiani, D.G. Lombardi, E. Pilozzi, and et al. Identification and expansion of human colon-cancer-initiating cells Nature 445 2007 111 115
20. P. Dalerba, S.J. Dylla, I.K. Park, and et al. Phenotypic characterization of human colorectal cancer stem cells Proc Natl Acad Sci USA 104 2007 10158 10163
21. T. Tanno, and W. Matsui Development and maintenance of cancer stem cells under chronic inflammation J Nihon Med Sch 78 2011 138 145
22. C. Zhou, J. Liu, Y. Tang, and et al. Inflammation linking EMT and cancer stem cells Oral Oncol 48 2012 1068 1075
23. W. Qiu, X. Wang, B. Leibowitz, and et al. Chemoprevention by nonsteroidal anti-inflammatory drugs eliminates oncogenic intestinal stem cells via SMAC-dependent apoptosis Proc Natl Acad Sci USA 107 2010 20027 20032
24. C.M. Moon, J.H. Kwon, J.S. Kim, and et al. Nonsteroidal anti-inflammatory drugs suppress cancer stem cells via inhibiting PTGS2 (cyclooxygenase 2) and NOTCH/HES1 and activating PPARG in colorectal cancer Int J Cancer 134 2014 519 529
25. D. Wang, H. Wang, Q. Shi, and et al. Prostaglandin E(2) promotes colorectal adenoma growth via transactivation of the nuclear peroxisome proliferator-activated receptor delta Cancer Cell 6 2004 285 295
26. C.A. O'Brien, A. Pollett, S. Gallinger, and et al. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice Nature 445 2007 106 110
27. M. Todaro, M. Gaggianesi, V. Catalano, and et al. CD44v6 is a marker of constitutive and reprogrammed cancer stem cells driving colon cancer metastasis Cell Stem Cell 14 2014 342 356
28. B.B. Patel, Y. Yu, J. Du, and et al. Age-related increase in colorectal cancer stem cells in macroscopically normal mucosa of patients with adenomas: a risk factor for colon cancer Biochem Biophys Res Commun 378 2009 344 347
29. R.R. Joseph, E. Yazer, Y. Hanakawa, and et al. Prostaglandins and activation of AC/cAMP prevents anoikis in IEC-18 Apoptosis 10 2005 1221 1233
30. M.D. Castellone, H. Teramoto, B.O. Williams, and et al. Prostaglandin E2 promotes colon cancer cell growth through a Gs-axin-beta-catenin signaling axis Science 310 2005 1504 1510
31. M.M. Chaturvedi, B. Sung, V.R. Yadav, and et al. NF-kappaB addiction and its role in cancer: 'one size does not fit all' Oncogene 30 2011 1615 1630
32. S. Schwitalla, A.A. Fingerle, P. Cammareri, and et al. Intestinal tumorigenesis initiated by dedifferentiation and acquisition of stem-cell-like properties Cell 152 2013 25 38
33. M. Dean, T. Fojo, and S. Bates Tumour stem cells and drug resistance Nat Rev Cancer 5 2005 275 284
34. Y. Li, L. Wang, L. Pappan, and et al. IL-1beta promotes stemness and invasiveness of colon cancer cells through Zeb1 activation Mol Cancer 11 2012 87
35. E. Charafe-Jauffret, C. Ginestier, F. Iovino, and et al. Breast cancer cell lines contain functional cancer stem cells with metastatic capacity and a distinct molecular signature Cancer Res 69 2009 1302 1313
36. H.J. Li, F. Reinhardt, H.R. Herschman, and et al. Cancer-stimulated mesenchymal stem cells create a carcinoma stem cell niche via prostaglandin E2 signaling Cancer Discov 2 2012 840 855
37. D. Wang, and R.N. Dubois Prostaglandins and cancer Gut 55 2006 115 122
38. Y. Shoji, M. Takahashi, T. Kitamura, and et al. Downregulation of prostaglandin E receptor subtype EP3 during colon cancer development Gut 53 2004 1151 1158
39. M. Majumder, X. Xin, L. Liu, and et al. Prostaglandin E2 receptor EP4 as the common target on cancer cells and macrophages to abolish angiogenesis, lymphangiogenesis, metastasis, and stem-like cell functions Cancer Sci 105 2014 1142 1151
40. X.C. He, T. Yin, J.C. Grindley, and et al. PTEN-deficient intestinal stem cells initiate intestinal polyposis Nat Genet 39 2007 189 198
41. A. Ragab, T. Buechling, V. Gesellchen, and et al. Drosophila Ras/MAPK signalling regulates innate immune responses in immune and intestinal stem cells EMBO J 30 2011 1123 1136
42. H. Jiang, M.O. Grenley, M.J. Bravo, and et al. EGFR/Ras/MAPK signaling mediates adult midgut epithelial homeostasis and regeneration in Drosophila Cell Stem Cell 8 2011 84 95
43. J.Y. Liou, D.P. Ellent, S. Lee, and et al. Cyclooxygenase-2-derived prostaglandin e2 protects mouse embryonic stem cells from apoptosis Stem Cells 25 2007 1096 1103
44. T.E. North, W. Goessling, C.R. Walkley, and et al. Prostaglandin E2 regulates vertebrate haematopoietic stem cell homeostasis Nature 447 2007 1007 1011
45. W. Goessling, T.E. North, S. Loewer, and et al. Genetic interaction of PGE2 and Wnt signaling regulates developmental specification of stem cells and regeneration Cell 136 2009 1136 1147
46. Y.Y. Fan, L.A. Davidson, E.S. Callaway, and et al. Differential effects of 2- and 3-series E-prostaglandins on in vitro expansion of Lgr5+ colonic stem cells Carcinogenesis 35 2014 606 612