Emodin as an effective agent in targeting cancer stem-like side population cells of gallbladder carcinoma

Stem Cells and Development

Volumn 22, Issue 4, 2013, Pages 554-566

  Li, Xin Xing ^a   Dong, Ying ^a   Wang, Wei ^a   Wang, Hao Lu ^a   Chen, Yu Ying ^b   Shi, Gui Ying ^b   Yi, Jing ^b   Wang, Jian ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BREAST CANCER RESISTANCE PROTEIN; CISPLATIN; DOXORUBICIN; EMODIN; MESSENGER RNA; MULTIDRUG RESISTANCE PROTEIN 1; REACTIVE OXYGEN METABOLITE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL; CANCER RESISTANCE; CANCER STEM CELL; CELL ADHESION; CELL STRUCTURE; CELL VIABILITY; CONTROLLED STUDY; DOSE RESPONSE; DOWN REGULATION; DRUG POTENTIATION; DRUG TARGETING; GALLBLADDER CARCINOMA; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIDE POPULATION CELL; TUMOR GROWTH; TUMOR VOLUME;

ANIMALS; ANTINEOPLASTIC AGENTS; ATP-BINDING CASSETTE TRANSPORTERS; CARCINOMA; CELL LINE, TUMOR; CISPLATIN; DRUG DELIVERY SYSTEMS; EMODIN; GALLBLADDER NEOPLASMS; HUMANS; MICE; MICE, INBRED BALB C; MICE, NUDE; NEOPLASM PROTEINS; NEOPLASTIC STEM CELLS; P-GLYCOPROTEIN; PROTEIN KINASE INHIBITORS; REACTIVE OXYGEN SPECIES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84873362126     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2011.0709     Document Type: Article

References (52)

1. Spillane JB and MA Henderson. (2007). Cancer stem cells: a review. ANZ J Surg 77:464-468 (Pubitemid 46733809)
2. Dalerba P, RW Cho and MF Clarke. (2007). Cancer stem cells: models and concepts. Annu Rev Med 58:267-284 (Pubitemid 46706514)
3. Dean M, T Fojo and S Bates. (2005). Tumour stem cells and drug resistance. Nat Rev Cancer 5:275-284 (Pubitemid 40488633)
4. Reya T, SJ Morrison,MF Clarke and IL Weissman. (2001). Stem cells, cancer, and cancer stem cells. Nature 414:105-111 (Pubitemid 33041634)
5. Biswas PK. (2010). Carcinoma gallbladder. Mymensingh Med J 19:477-481
6. Abahssain H, P Afchain, N Melas, N Ismaili, R Rahali, HM Rabti and H Errihani. (2010). [Chemotherapy in gallbladder carcinoma]. Presse Med 39:1238-1245
7. Fong D, A Yeh, R Naftalovich, TH Choi and MM Chan. (2010). Curcumin inhibits the side population (SP) phenotype of the rat C6 glioma cell line: towards targeting of cancer stem cells with phytochemicals. Cancer Lett 293:65-72
8. Mathew G, EA Timm Jr., P Sotomayor, A Godoy, VP Montecinos, GJ Smith and WJ Huss. (2009). ABCG2- mediated DyeCycle Violet efflux defined side population in benign and malignant prostate. Cell Cycle 8:1053-1061
9. Goodell MA, K Brose, G Paradis, AS Conner and RC Mulligan. (1996). Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med 183:1797-806 (Pubitemid 26134320)
10. Ailles LE and IL Weissman. (2007). Cancer stem cells in solid tumors. Curr Opin Biotechnol 18:460-466 (Pubitemid 350116595)
11. Oka M, C Toyoda, Y Kaneko, Y Nakazawa, E Aizu-Yokota and M Takehana. (2010). Characterization and localization of side population cells in the lens. Mol Vis 16:945-953
12. Sung JM, HJ Cho, H Yi, CH Lee, HS Kim, DK Kim, AM Abd El-Aty, JS Kim, CP Landowski, MA Hediger and HC Shin. (2008). Characterization of a stem cell population in lung cancer A549 cells. Biochem Biophys Res Commun 371: 163-167
13. Tabor MH, MR Clay, JH Owen, CR Bradford, TE Carey, GT Wolf and ME Prince. (2011). Head and neck cancer stem cells: the side population. Laryngoscope 121:527-533
14. Wan G, L Zhou, M Xie, H Chen and J Tian. (2010). Characterization of side population cells from laryngeal cancer cell lines. Head Neck 32:1302-1309
15. Wang B, H Yang, YZ Huang, RH Yan, FJ Liu and JN Zhang. (2010). Biologic characteristics of the side population of human small cell lung cancer cell line H446. Chin J Cancer 29:254-260
16. Wu C and BA Alman. (2008). Side population cells in human cancers. Cancer Lett 268:1-9
17. Cai J, X Niu, Y Chen, Q Hu, G Shi, H Wu, J Wang and J Yi. (2008). Emodin-induced generation of reactive oxygen species inhibits RhoA activation to sensitize gastric carcinoma cells to anoikis. Neoplasia 10:41-51 (Pubitemid 351170711)
18. Yang J, H Li, YY Chen, XJ Wang, GY Shi, QS Hu, XL Kang, Y Lu, XM Tang, QS Guo and J Yi. (2004). Anthraquinones sensitize tumor cells to arsenic cytotoxicity in vitro and in vivo via reactive oxygen species-mediated dual regulation of apoptosis. Free Radic Biol Med 37:2027-2041 (Pubitemid 39491322)
19. Yi J, J Yang, R He, F Gao, H Sang, X Tang and RD Ye. (2004). Emodin enhances arsenic trioxide-induced apoptosis via generation of reactive oxygen species and inhibition of survival signaling. Cancer Res 64:108-116 (Pubitemid 38114088)
20. Huang XZ, J Wang, C Huang, YY Chen, GY Shi, QS Hu and J Yi. (2008). Emodin enhances cytotoxicity of chemotherapeutic drugs in prostate cancer cells: the mechanisms involve ROS-mediated suppression of multidrug resistance and hypoxia inducible factor-1. Cancer Biol Ther 7:468-475 (Pubitemid 351847069)
21. Wang W, YP Sun, XZ Huang, M He, YY Chen, GY Shi, H Li, J Yi and J Wang. (2010). Emodin enhances sensitivity of gallbladder cancer cells to platinum drugs via glutathion depletion and MRP1 downregulation. Biochem Pharmacol 79:1134-1140
22. Cha TL, L Qiu, CT Chen, Y Wen and MC Hung. (2005). Emodin down-regulates androgen receptor and inhibits prostate cancer cell growth. Cancer Res 65:2287-2295 (Pubitemid 40490138)
23. Huang D, Q Gao, L Guo, C Zhang, W Jiang, H Li, J Wang, X Han, Y Shi and SH Lu. (2009). Isolation and identification of cancer stem-like cells in esophageal carcinoma cell lines. Stem Cells Dev 18:465-473
24. Singh SK, ID Clarke, M Terasaki, VE Bonn, C Hawkins, J Squire and PB Dirks. (2003). Identification of a cancer stem cell in human brain tumors. Cancer Res 63:5821-5828 (Pubitemid 37187480)
25. Reynolds BA and S Weiss. (1992). Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255:1707-1710
26. Clarke MF, M Diehn, RW Cho, NA Lobo, T Kalisky, MJ Dorie, AN Kulp, DL Qian, JS Lam, et al. (2009). Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 458:780-783
27. Yin L, P Castagnino and RK Assoian. (2008). ABCG2 expression and side population abundance regulated by a transforming growth factor beta-directed epithelialmesenchymal transition. Cancer Res 68:800-807 (Pubitemid 351206757)
28. Ding XW, JH Wu and CP Jiang. (2010). ABCG2: a potential marker of stem cells and novel target in stem cell and cancer therapy. Life Sci 86:631-637
29. Lopez JP, J Wang-Rodriguez, C Chang, JS Chen, FS Pardo, J Aguilera and WM Ongkeko. (2007). Gefitinib inhibition of drug resistance to doxorubicin by inactivating ABCG2 in thyroid cancer cell lines. Arch Otolaryngol Head Neck Surg 133:1022-1027 (Pubitemid 47607585)
30. Dai CL, AK Tiwari, CP Wu, XD Su, SR Wang, DG Liu, CR Ashby Jr., Y Huang, RW Robey, et al. (2008). Lapatinib (Tykerb, GW572016) reverses multidrug resistance in cancer cells by inhibiting the activity of ATP-binding cassette subfamily B member 1 and G member 2. Cancer Res 68:7905-7914
31. Robey RW, KK To, O Polgar, M Dohse, P Fetsch, M Dean and SE Bates. (2009). ABCG2: a perspective. Adv Drug Deliv Rev 61:3-13
32. Donnenberg VS and AD Donnenberg. (2005). Multiple drug resistance in cancer revisited: the cancer stem cell hypothesis. J Clin Pharmacol 45:872-877 (Pubitemid 41060226)
33. Shi C, R Tian, M Wang, X Wang, J Jiang, Z Zhang, X Li, Z He, W Gong and R Qin. (2010). CD44 + CD133 + population exhibits cancer stem cell-like characteristics in human gallbladder carcinoma. Cancer Biol Ther 10:1182-1190
34. Shi CJ, J Gao, M Wang, X Wang, R Tian, F Zhu, M Shen and RY Qin. (2011). CD133( + ) gallbladder carcinoma cells exhibit self-renewal ability and tumorigenicity. World J Gastroenterol 17:2965-2971
35. Yin BB, SJ Wu, HJ Zong, BJ Ma and D Cai. (2011). Preliminary screening and identification of stem cell-like sphere clones in a gallbladder cancer cell line GBC-SD. J Zhejiang Univ Sci B 12:256-263
36. Zhou S, JJ Morris, Y Barnes, L Lan, JD Schuetz and BP Sorrentino. (2002). Bcrp1 gene expression is required for normal numbers of side population stem cells in mice, and confers relative protection to mitoxantrone in hematopoietic cells in vivo. Proc Natl Acad Sci U S A 99:12339-12344
37. Li XX, J Wang, HL Wang, W Wang, XB Yin, QW Li, YY Chen and J Yi. (2012). Characterization of cancer stem-like cells derived from a side population of a human gallbladder carcinoma cell line, SGC-996. Biochem Biophys Res Commun 419:728-734
38. Zhang Z, F Zhu, L Xiao, M Wang, R Tian, C Shi and R Qin. (2011). Side population cells in human gallbladder cancer cell line GBC-SD regulated by TGF-beta-induced epithelialmesenchymal transition. J Huazhong Univ Sci Technolog Med Sci 31:749-755
39. Huang Q, HM Shen, G Shui, MR Wenk and CN Ong. (2006). Emodin inhibits tumor cell adhesion through disruption of the membrane lipid Raft-associated integrin signaling pathway. Cancer Res 66:5807-5815 (Pubitemid 43927135)
40. Su YT, HL Chang, SK Shyue and SL Hsu. (2005). Emodin induces apoptosis in human lung adenocarcinoma cells through a reactive oxygen species-dependent mitochondrial signaling pathway. Biochem Pharmacol 70:229-241
41. Velamakanni S, SL Wei, T Janvilisri and HW van Veen. (2007). ABCG transporters: structure, substrate specificities and physiological roles: a brief overview. J Bioenerg Biomembr 39:465-471
42. Wang H, JD Unadkat and Q Mao. (2008). Hormonal regulation of BCRP expression in human placental BeWo cells. Pharm Res 25:444-452 (Pubitemid 351257980)
43. Wang H, EW Lee, L Zhou, PC Leung, DD Ross, JD Unadkat and Q Mao. (2008). Progesterone receptor (PR) isoforms PRA and PRB differentially regulate expression of the breast cancer resistance protein in human placental choriocarcinoma BeWo cells. Mol Pharmacol 73:845-854 (Pubitemid 351397889)
44. Ifergan I, A Shafran, G Jansen, JH Hooijberg, GL Scheffer and YG Assaraf. (2004). Folate deprivation results in the loss of breast cancer resistance protein (BCRP/ABCG2) expression. A role for BCRP in cellular folate homeostasis. J Biol Chem 279:25527-25534 (Pubitemid 38756812)
45. Katayama R, S Koike, S Sato, Y Sugimoto, T Tsuruo and N Fujita. (2009). Dofequidar fumarate sensitizes cancer stemlike side population cells to chemotherapeutic drugs by inhibiting ABCG2/BCRP-mediated drug export. Cancer Sci 100:2060-2068
46. Gilliland DG, Z Tothova, R Kollipara, BJ Huntly, BH Lee, DH Castrillon, DE Cullen, EP McDowell, S Lazo-Kallanian, et al. (2007). FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell 128:325-339 (Pubitemid 46137992)
47. Noble M, J Smith, E Ladi and M Mayer-Proschel. (2000). Redox state is a central modulator of the balance between self-renewal and differentiation in a dividing glial precursor cell. Proc Natl Acad Sci U S A 97:10032-10037
48. Ito K, A Hirao, F Arai, S Matsuoka, TW Mak and T Suda. (2004). Regulation of oxidative stress by ATM is required for the self-renewal of haematopoietic stem cells. Blood 104:109a
49. Das B, R Tsuchida, D Malkin, G Koren, S Baruchel and H Yeger. (2008). Hypoxia enhances tumor stemness by increasing the invasive and tumorigenic side population fraction. Stem Cells 26:1818-1830
50. Robey RW, Y Honjo, K Morisaki, TA Nadjem, S Runge, M Risbood, MS Poruchynsky and SE Bates. (2003). Mutations at amino-acid 482 in the ABCG2 gene affect substrate and antagonist specificity. Br J Cancer 89:1971-1978 (Pubitemid 37533279)
51. Martin CM, A Ferdous, T Gallardo, C Humphries, H Sadek, A Caprioli, JA Garcia, LI Szweda, MG Garry and DJ Garry. (2008). Hypoxia-inducible factor-2alpha transactivates Abcg2 and promotes cytoprotection in cardiac side population cells. Circ Res 102:1075-1081 (Pubitemid 351667861)
52. Schuetz JD, P Krishnamurthy, DD Ross, T Nakanishi, K Bailey-Dell, S Zhou, KE Mercer, B Sarkadi and BP Sorrentino. (2004). The stem cell marker Bcrp/ABCG2 enhances hypoxic cell survival through interactions with heme. J Biol Chem 279:24218-24225. (Pubitemid 38725283)