Minnelide effectively eliminates CD133+ side population in pancreatic cancer

Molecular Cancer

Volumn 14, Issue 1, 2015, Pages

  Nomura, Alice ^a   McGinn, Olivia ^a   Dudeja, Vikas ^a   Sangwan, Veena ^a   Saluja, Ashok K ^a,b   Banerjee, Sulagna ^a,b  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; BREAST CANCER RESISTANCE PROTEIN; CD133 ANTIGEN; MINNELIDE; TRIPTOLIDE; UNCLASSIFIED DRUG; 14-O-PHOSPHONOOXYMETHYLTRIPTOLIDE; DITERPENE; EPOXIDE; GLYCOPROTEIN; LEUKOCYTE ANTIGEN; ORGANOPHOSPHATE; PEPTIDE; PHENANTHRENE DERIVATIVE; PROM1 PROTEIN, HUMAN; PROM1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANTIGEN EXPRESSION; ANTIGEN SPECIFICITY; ARTICLE; CANCER PROGNOSIS; CANCER STEM CELL; CANCER SURVIVAL; CELL INVASION; CONTROLLED STUDY; DRUG EFFICACY; FEMALE; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; PANCREAS ADENOCARCINOMA; PANCREAS CANCER; T LYMPHOCYTE; TREATMENT FAILURE; TUMOR RECURRENCE; TUMOR REGRESSION; TUMOR VOLUME; CARCINOMA, PANCREATIC DUCTAL; CELL SURVIVAL; DRUG EFFECTS; DRUG RESISTANCE; DRUG SCREENING; METABOLISM; PANCREATIC NEOPLASMS; PATHOLOGY; PHYSIOLOGY; SIDE POPULATION CELL; TUMOR CELL LINE;

AC133 ANTIGEN; ANTIGENS, CD; ANTINEOPLASTIC AGENTS; CARCINOMA, PANCREATIC DUCTAL; CELL LINE, TUMOR; CELL SURVIVAL; DITERPENES; DRUG RESISTANCE, NEOPLASM; DRUG SCREENING ASSAYS, ANTITUMOR; EPOXY COMPOUNDS; GLYCOPROTEINS; HUMANS; NEOPLASTIC STEM CELLS; ORGANOPHOSPHATES; PANCREATIC NEOPLASMS; PEPTIDES; PHENANTHRENES; SIDE-POPULATION CELLS;

EID: 84947712555     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/s12943-015-0470-6     Document Type: Article

References (49)

1. Jemal A, Center MM, DeSantis C, Ward EM. Global patterns of cancer incidence and mortality rates and trends. Cancer Epidemiol Biomarkers Prev. 2010;19:1893-907.
2. Griffin JF, Smalley SR, Jewell W, Paradelo JC, Reymond RD, Hassanein RE, et al. Patterns of failure after curative resection of pancreatic carcinoma. Cancer. 1990;66:56-61.
3. Cameron JL, Crist DW, Sitzmann JV, Hruban RH, Boitnott JK, Seidler AJ, et al. Factors influencing survival after pancreaticoduodenectomy for pancreatic cancer. Am J Surg. 1991;161:120-4. discussion 124-125.
4. Al-Hajj M, Clarke MF. Self-renewal and solid tumor stem cells. Oncogene. 2004;23:7274-82.
5. Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med. 1997;3:730-7.
6. Li C, Heidt DG, Dalerba P, Burant CF, Zhang L, Adsay V, et al. Identification of pancreatic cancer stem cells. Cancer Res. 2007;67:1030-7.
7. Hermann PC, Huber SL, Herrler T, Aicher A, Ellwart JW, Guba M, et al. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell. 2007;1:313-23.
8. Immervoll H, Hoem D, Sakariassen PO, Steffensen OJ, Molven A. Expression of the "stem cell marker" CD133 in pancreas and pancreatic ductal adenocarcinomas. BMC Cancer. 2008;8:48.
9. Qu D, Johnson J, Chandrakesan P, Weygant N, May R, Aiello N, et al. Doublecortin-like kinase 1 is elevated serologically in pancreatic ductal adenocarcinoma and widely expressed on circulating tumor cells. PLoS One. 2015;10(2):e0118933. doi: 10.1371/journal.pone.0118933. eCollection 2015.
10. Olempska M, Eisenach PA, Ammerpohl O, Ungefroren H, Fandrich F, Kalthoff H. Detection of tumor stem cell markers in pancreatic carcinoma cell lines. Hepatobiliary Pancreat Dis Int. 2007;6:92-7.
11. Shah AN, Summy JM, Zhang J, Park SI, Parikh NU, Gallick GE. Development and characterization of gemcitabine-resistant pancreatic tumor cells. Ann Surg Oncol. 2007;14:3629-37.
12. Du Z, Qin R, Wei C, Wang M, Shi C, Tian R, et al. Pancreatic cancer cells resistant to chemoradiotherapy rich in "stem-cell-like" tumor cells. Dig Dis Sci. 2011;56:741-50.
13. Angelastro JM, Lame MW. Overexpression of CD133 promotes drug resistance in C6 glioma cells. Mol Cancer Res. 2010;8:1105-15.
14. Nomura A, Banerjee S, Chugh R, Dudeja V, Yamamoto M, Vickers SM, et al. CD133 initiates tumors, induces epithelial-mesenchymal transition and increases metastasis in pancreatic cancer. Oncotarget. 2015;6(10):8313-22.
15. Yao J, Cai HH, Wei JS, An Y, Ji ZL, Lu ZP, et al. Side population in the pancreatic cancer cell lines SW1990 and CFPAC-1 is enriched with cancer stem-like cells. Oncol Rep. 2010;23:1375-82.
16. Wang D, Zhu H, Zhu Y, Liu Y, Shen H, Yin R, et al. CD133(+)/CD44(+)/Oct4(+)/Nestin(+) stem-like cells isolated from Panc-1 cell line may contribute to multi-resistance and metastasis of pancreatic cancer. Acta Histochem. 2013;115:349-56.
17. Goodell MA, Brose K, Paradis G, Conner AS, Mulligan RC. Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med. 1996;183:1797-806.
18. Golebiewska A, Bougnaud S, Stieber D, Brons NH, Vallar L, Hertel F, et al. Side population in human glioblastoma is non-tumorigenic and characterizes brain endothelial cells. Brain. 2013;136:1462-75.
19. Golebiewska A, Brons NH, Bjerkvig R, Niclou SP. Critical appraisal of the side population assay in stem cell and cancer stem cell research. Cell Stem Cell. 2011;8:136-47.
20. Kabashima A, Higuchi H, Takaishi H, Matsuzaki Y, Suzuki S, Izumiya M, et al. Side population of pancreatic cancer cells predominates in TGF-beta-mediated epithelial to mesenchymal transition and invasion. Int J Cancer. 2009;124:2771-9.
21. Dou J, Wen P, Hu W, Li Y, Wu Y, Liu C, et al. Identifying tumor stem-like cells in mouse melanoma cell lines by analyzing the characteristics of side population cells. Cell Biol Int. 2009;33:807-15.
22. Abbott BL. ABCG2 (BCRP) expression in normal and malignant hematopoietic cells. Hematol Oncol. 2003;21:115-30.
23. Feuring-Buske M, Hogge DE. Hoechst 33342 efflux identifies a subpopulation of cytogenetically normal CD34(+)CD38(-) progenitor cells from patients with acute myeloid leukemia. Blood. 2001;97:3882-9.
24. Guo D, Xu BL, Zhang XH, Dong MM. Cancer stem-like side population cells in the human nasopharyngeal carcinoma cell line cne-2 possess epithelial mesenchymal transition properties in association with metastasis. Oncol Rep. 2012;28:241-7.
25. Chen S, Song X, Chen Z, Li X, Li M, Liu H, et al. CD133 expression and the prognosis of colorectal cancer: a systematic review and meta-analysis. PLoS One. 2013;8:e56380.
26. Sasaki A, Kamiyama T, Yokoo H, Nakanishi K, Kubota K, Haga H, et al. Cytoplasmic expression of CD133 is an important risk factor for overall survival in hepatocellular carcinoma. Oncol Rep. 2010;24:537-46.
27. Li C, Wu JJ, Hynes M, Dosch J, Sarkar B, Welling TH, et al. c-Met is a marker of pancreatic cancer stem cells and therapeutic target. Gastroenterology. 2011;141:2218-2227.e2215.
28. Jiang R, Li Y, Xu Y, Zhou Y, Pang Y, Shen L, et al. EMT and CSC-like properties mediated by the IKKbeta/IkappaBalpha/RelA signal pathway via the transcriptional regulator, Snail, are involved in the arsenite-induced neoplastic transformation of human keratinocytes. Arch Toxicol. 2012;87(6):991-1000.
29. Mirantes C, Espinosa I, Ferrer I, Dolcet X, Prat J, Matias-Guiu X. Epithelial-to-mesenchymal transition and stem cells in endometrial cancer. Hum Pathol. 2013;44(10):1973-81.
30. Aghdassi A, Phillips P, Dudeja V, Dhaulakhandi D, Sharif R, Dawra R, et al. Heat shock protein 70 increases tumorigenicity and inhibits apoptosis in pancreatic adenocarcinoma. Cancer Res. 2007;67:616-25.
31. Banerjee S, Thayanithy V, Sangwan V, Mackenzie TN, Saluja AK, Subramanian S. Minnelide reduces tumor burden in preclinical models of osteosarcoma. Cancer Lett. 2013;335:412-20.
32. Chugh R, Sangwan V, Patil SP, Dudeja V, Dawra RK, Banerjee S, et al. A preclinical evaluation of Minnelide as a therapeutic agent against pancreatic cancer. Sci Transl Med. 2012;4:156ra139.
33. Banerjee S, Nomura A, Sangwan V, Chugh R, Dudeja V, Vickers SM, et al. CD133+ tumor initiating cells in a syngenic murine model of pancreatic cancer respond to Minnelide. Clin Cancer Res. 2014;20:2388-99.
34. Cho RW, Clarke MF. Recent advances in cancer stem cells. Curr Opin Genet Dev. 2008;18:48-53.
35. Clevers H. The cancer stem cell: premises, promises and challenges. Nat Med. 2011;17:313-9.
36. Monzani E, Facchetti F, Galmozzi E, Corsini E, Benetti A, Cavazzin C, et al. Melanoma contains CD133 and ABCG2 positive cells with enhanced tumourigenic potential. Eur J Cancer. 2007;43:935-46.
37. Adhikari AS, Agarwal N, Iwakuma T. Metastatic potential of tumor-initiating cells in solid tumors. Front Biosci (Landmark Ed). 2011;16:1927-38.
38. Hirschmann-Jax C, Foster AE, Wulf GG, Goodell MA, Brenner MK. A distinct "side population" of cells in human tumor cells: implications for tumor biology and therapy. Cell Cycle. 2005;4:203-5.
39. Hu X, Ghisolfi L, Keates AC, Zhang J, Xiang S, Lee DK, et al. Induction of cancer cell stemness by chemotherapy. Cell Cycle. 2012;11:2691-8.
40. Zhou J, Wang CY, Liu T, Wu B, Zhou F, Xiong JX, et al. Persistence of side population cells with high drug efflux capacity in pancreatic cancer. World J Gastroenterol. 2008;14:925-30.
41. Yin T, Wei H, Gou S, Shi P, Yang Z, Zhao G, et al. Cancer stem-like cells enriched in panc-1 spheres possess increased migration ability and resistance to gemcitabine. Int J Mol Sci. 2011;12:1595-604.
42. Hu G, Li F, Ouyang K, Xie F, Tang X, Wang K, et al. Intrinsic gemcitabine resistance in a novel pancreatic cancer cell line is associated with cancer stem cell-like phenotype. Int J Oncol. 2012;40:798-806.
43. Hueng DY, Sytwu HK, Huang SM, Chang C, Ma HI. Isolation and characterization of tumor stem-like cells from human meningiomas. J Neurooncol. 2011;104:45-53.
44. Warrier S, Pavanram P, Raina D, Arvind M. Study of chemoresistant CD133+ cancer stem cells from human glioblastoma cell line U138MG using multiple assays. Cell Biol Int. 2012;36:1137-43.
45. Alt R, Wilhelm F, Pelz-Ackermann O, Egger D, Niederwieser D, Cross M. ABCG2 expression is correlated neither to side population nor to hematopoietic progenitor function in human umbilical cord blood. Exp Hematol. 2009;37:294-301.
46. Saxena M, Stephens MA, Pathak H, Rangarajan A. Transcription factors that mediate epithelial-mesenchymal transition lead to multidrug resistance by upregulating ABC transporters. Cell Death Dis. 2011;2:e179.
47. Zhang GN, Liang Y, Zhou LJ, Chen SP, Chen G, Zhang TP, et al. Combination of salinomycin and gemcitabine eliminates pancreatic cancer cells. Cancer Lett. 2011;313:137-44.
48. Pirozzi G, Tirino V, Camerlingo R, La Rocca A, Martucci N, Scognamiglio G, et al. Prognostic value of cancer stem cells, epithelial-mesenchymal transition and circulating tumor cells in lung cancer. Oncol Rep. 2013;29:1763-8.
49. Goodell MA, McKinney-Freeman S, Camargo FD. Isolation and characterization of side population cells. Methods Mol Biol. 2005;290:343-52.