Arsenic-specific stem cell selection during malignant transformation

Journal of the National Cancer Institute

Volumn 102, Issue 9, 2010, Pages 638-649

  Tokar, Erik J ^a   Qu, Wei ^a   Liu, Jie ^a   Liu, Wei ^b   Webber, Mukta M ^c   Phang, James M ^b   Waalkes, Michael P ^a  

^a National Cancer Institute   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARSENIC; BIOLOGICAL MARKER; CADMIUM; GLUTATHIONE; METHYLNITROSOUREA; PROTEIN BCL 2;

APOPTOSIS; ARTICLE; CELL SELECTION; CELL STRESS; CELL SURVIVAL; CONTROLLED STUDY; EXPOSURE; HUMAN; HUMAN CELL; MALE; MALIGNANT TRANSFORMATION; PHENOTYPE; PRIORITY JOURNAL; PROSTATE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEM CELL; WESTERN BLOTTING;

APOPTOSIS; ARSENITES; BLOTTING, WESTERN; CADMIUM COMPOUNDS; CARCINOGENS; CELL LINE; CELL SURVIVAL; CELL TRANSFORMATION, NEOPLASTIC; GLUTATHIONE; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; METHYLNITROSOUREA; MICROSCOPY, CONFOCAL; PROSTATE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STEM CELLS; TUMOR STEM CELL ASSAY;

EID: 77952074045     PISSN: 00278874     EISSN: 14602105     Source Type: Journal    
DOI: 10.1093/jnci/djq093     Document Type: Article

References (59)

1. International Agency for Research on Cancer. Arsenic in Drinking Water. International Agency for Research on Cancer Monographs on the Evaluation of Carcinogenic Risk to Humans. Some Drinking Water Disinfectants and Contaminants, Including Arsenic. Vol.84. Lyon, France: IARC Press; 2004. 269-477.
2. Kitchin KT. Recent advances in arsenic carcinogenesis: modes of action, animal model systems, and methylated arsenic metabolites. Toxicol Appl Pharmacol. 2001;172(3):249-261.
3. Benbrahim-Tallaa L, Waalkes MP. Inorganic arsenic and human prostate cancer. Environ Health Perspect. 2008;116(2):158-164.
4. Achanzar WE, Brambila EM, Diwan BA, et al. Inorganic arsenite induced malignant transformation of human prostate epithelial cells. J Natl Cancer Inst. 2002;94(24):1888-1891.
5. Waalkes MP, Liu J, Diwan BA. Transplacental arsenic carcinogenesis in mice. Toxicol Appl Pharmacol. 2007;222(3):271-280.
6. Smith AH, Marshall G, Yuan Y, et al. Increased mortality from lung cancer and bronchiectasis in young adults after exposure to arsenic in utero and in early childhood. Environ Health Perspect. 2006;114(8):1293-1296.
7. Anderson LM, Diwan B, Fear N, et al. Critical windows of exposure for children's health: cancer in human epidemiological studies and neoplasms in experimental animal models. Environ Health Perspect. 2000;108 (Suppl 3):573-594.
8. Pardal R, Clarke MF, Morrison SJ. Applying the principles of stem-cell biology to cancer. Nat Rev Cancer. 2003;3(12):895-902.
9. Patterson TJ, Rice RH. Arsenite and insulin exhibit opposing effects on epidermal growth factor receptor and keratinocyte proliferative potential. Toxicol Appl Pharmacol. 2007;221(1):119-128.
10. Waalkes MP, Liu J, Germolec D, et al. Arsenic exposure in utero exacerbates skin cancer response in adulthood with contemporaneous distortion of rumor stem cell dynamics. Cancer Res. 2008;68(20):8278-8285.
11. Johnstone RW, Ruefi AA, Lowe SW. Apoptosis: a link between cancer genetics and chemotherapy. Cell. 2002;108(2):153-164.
12. Waalkes MP, Fox DA, States JC, et al. Metals and disorders of cell accumulation: modulation of apoptosis and cell proliferation. Toxicol Sci. 2000; 56(2):255-261.
13. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell. 2000;100(1): 57-70.
14. McKenzie S, Kyprianou N. Apoptosis evasion: the role of survival pathways in prostate cancer progression and therapeutic resistance. J Cell Biochem. 2006;97(1):18-32.
15. Zhivotovsky B, Orrenius S. Carcinogenesis and apoptosis: paradigms and paradoxes. Carcinogenesis. 2006;27(10):1939-1945.
16. Liu J, Chen H, Miller DS, et al. Overexpression of glutathione S-transferase II and multidrug resistant transport proteins is associated with acquired arsenic tolerance to inorganic arsenic. Mol Pharmacol. 2001;60(2):302-309.
17. Gottesman MM, Fojo T, Bates SE. Multidrug resistance in cancer: role of ATP dependent transporters. Nat Rev Cancer. 2002;2(1):48-58.
18. Brambila EM, Achanzar WE, Qu W, et al. Chronic arsenic exposed human prostate epithelial cells exhibit stable arsenic tolerance: mechanistic implications of altered cellular glutathione and glutathione S-transferase. Toxicol Appl Pharmacol. 2002;183(2):99-107.
19. Zhao CQ, Young MR, Diwan BA, et al. Association of arsenic-induced malignant transformation with DNA hypomethylation and aberrant gene expression. Proc Natl Acad Sci USA. 1997;94(20):10907-10912.
20. Donnenberg VS, Luketich JD, Landreneau RJ, et al. Tumorigenic epithelial stem cells and their normal counterparts. Ernst Schering Found Symp Proc. 2006;5(9):245-263.
21. Donnenberg VS, Landreneau RJ, Donnenberg AD. Tumorigenic stem and progenitor cells: implications for the therapeutic index of anti-cancer agents. J Control Release. 2007;122(3):385-391.
22. Li X, Lewis MT, Huang J, et al. Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. J Natl Cancer Inst. 2008;100(9):672-679.
23. Shafee N, Smith CR, Wei S, et al. Cancer stem cells contribute to cisplatin resistance in Brca1/p53-meditated mouse mammary tumors. Cancer Res. 2008;68(9):3243-3250.
24. Iannolo G, Conticello C, Memeo L, De Maria R. Apoptosis in normal and cancer stem cells. Crit Rev Oncol Hematol. 2008;66(1):42-51.
25. Matsui W, Wang Q, Barber JP, et al. Clonogenic multiple myeloma progenitors, stem cell properties, and drug resistance. Cancer Res. 2008; 68(1):190-197.
26. Tokar EJ, Ancrile BB, Cunha GR, Webber MM. Stem/progenitor and intermediate cells and the origin of human prostate cancer. Differentiation. 2005;73(9-10):463-473.
27. Bello D, Webber MM, Kleinman HK, et al. Androgen responsive adult human prostatic epithelial cell lines immortalized by human papilloma-virus 18. Carcinogenesis. 1997;18(6):1215-1223.
28. Tokar EJ, Diwan BA, Waalkes MP. Arsenic transforms human epithelial stem/progenitor cells into a cancer stem-like phenotype. Environ Health Perspect. 2010;118(1):108-115.
29. Stingl J, Eirew P, Ricketson I, et al. Purifcation and unique properties of mammary epithelial stem cells. Nature. 2006;439(7079):993-997.
30. Ghods AJ, Irvin D, Liu G, et al. Spheres isolated from 9L gliosarcoma rat cell line possess chemoresistant and aggressive cancer stem-like cells. Stem Cells. 2007;25(7):1645-1653.
31. Webber MM, Quader STA, Kleinman HK, et al. Human cell lines as an in vitro/in vivo model for prostate carcinogenesis and progression. Prostate. 2001;47(1):1-13.
32. Achanzar WE, Diwan BA, Liu J, Quader ST, Webber MM, Waalkes MP. Cadmium-induced malignant transformation of human prostate epithelial cells. Cancer Res. 2001;61(2):455-458.
33. Pi J, Yamauchi H, Kumagai Y, et al. Evidence for induction of oxidative stress caused by chronic exposure of Chinese residents to arsenic contained in drinking water. Environ Health Perspect. 2002;110(4):331-336.
34. Coppin JF, Qu W, Waalkes MP. Interplay between cellular methyl metabolism and adaptive effux during oncogenic transformation from chronic arsenic exposure in human cells. J Biol Chem. 2008;283(28):19342-19350.
35. Rasband WS. ImageJ. Bethesda, MD: U.S. National Institutes of Health; 1997-2005. http://rsb.info.nih.gov/ij/. Accessed January 15, 2009.
36. Hamburger AW, Salmon SE. Primary bioassay of human tumor stem cells. Science. 1977;197(4302):461-463.
37. Zhang L, Yu J, Park BH, et al. Role of bax in the apoptotic response to anticancer agents. Science. 2000;290(5493):989-992.
38. Shimoda R, Achanzar WE, Qu W, et al. Metallothionein is a potential negative regulator of apoptosis. Toxicol Sci. 2003;73(2):294-300.
39. Liu J, Cheng ML, Yang Q, et al. Blood metallothionein transcript as a biomarker for metal sensitivity: low blood metallothionein transcripts in arsenicosis patients from Guizhou, China. Environ Health Perspect. 2007;115(7):1101-1106.
40. Leslie EM, Haimeur A, Waalkes MP. Arsenic transport by the human multidrug resistance protein (MRP1/ABCC1): evidence that a tri-glutathione conjugate is required. J Biol Chem. 2004;279(31):32700-32708.
41. Kala SV, Neely MW, Kala G, et al. The MRP2/cMOAT transporter and arsenic-glutathione complex formation are required for biliary excretion of arsenic. J Biol Chem. 2000;275(43):33404-33408.
42. Pandhare J, Cooper SK, Donald SP, Phang JM. Regulation and function of proline oxidase under nutrient stress. J Cell Biochem. 2009;107(4): 759-768.
43. Dubrovska A, Kim S, Salamone RJ, et al. The role of PTEN/Akt/PI3K signaling in the maintenance and viability of prostate cancer stem-like cell populations. Proc Natl Acad Sci USA. 2009;106(1):268-273.
44. Blanpain C, Lowry WE, Geoghegan A, Polak L, Fuchs E. Self-renewal, multipotency, and the existence of two cell populations within an epithelial stem cell niche. Cell. 2004;118(5):635-648.
45. Li H, Chen X, Calhoun-Davis T, Claypool K, Tang DG. PC3 human prostate carcinoma cell holoclones contain self-renewing tumor-initiating cells. Cancer Res. 2008;68(6):1820-1825.
46. Qu W, Bortner CD, Sakurai T, et al. Acquisition of apoptotic resistance in arsenic-induced malignant transformation: role of the JNK signal trans-duction pathway. Carcinogenesis. 2002;23(1):151-159.
47. Hengartner MO. The biochemistry of apoptosis. Nature. 2000;407(6805): 770-776.
48. Domen J, Cheshier SH, Weissman IL. The role of apoptosis in the regulation of hematopoietic stem cells: overexpression of Bcl-2 increases both their number and repopulation potential. J Exp Med. 2000;191(2):253-264.
49. Liu J, Liu Y, Goyer RA, et al. Metallothionein-I/II null mice are more sensitive than wild-type mice to the hepatotoxic and nephrotoxic effects of chronic oral or injected inorganic arsenic. Toxicol Sci. 2000;55(2):460-467.
50. Qu W, Fuquay R, Sakurai T, et al. Acquisition of apoptotic resistance in cadmium-induced malignant transformation: specifc perturbation of JNK signal transduction pathway and associated metallothionein overexpres-sion. Mol Carcinog. 2006;45(8):561-571.
51. Ghibelli L, Fanelli C, Rotilio G, et al. Rescue of cell from apoptosis by inhibition of active GSH extrusion. FASEB J. 1998;12(6):479-486.
52. Borst P, Evers R, Kool M, et al. A family of drug transporters: the multidrug resistance-associated proteins. J Natl Cancer Inst. 2000;92(16):1295-1302.
53. Kamat CD, Green DE, Curilla S, et al. Role of HIF signaling on tumori-genesis in response to chronic low-dose arsenic administration. Toxicol Sci. 2005;86(2):248-257.
54. Ramos-Gomez M, Kwak MK, Dolan PM, et al. Sensitivity to carcinogen-esis is increased and chemoprotective effcacy of enzyme inducers lost in Nrf2 transcription factor-defcient mice. Proc Natl Acad Sci USA. 2001; 98(6):3410-3415.
55. Lee JM, Calkins MJ, Chan K, et al. Identifcation of the NF-E2-related factor-2-dependent genes conferring protection against oxidative stress in primary cortical astrocytes using oligonucleotide microarray analysis. J Biol Chem. 2003;278(14):12029-12038.
56. Romach EH, Zhao CQ, Del Razo LM, et al. Studies on the mechanisms of arsenic-induced self tolerance developed in liver epithelial cells through continuous low-level arsenite exposure. Toxicol Sci. 2000;54(2): 500-508.
57. Pi J, He Y, Bortner C, et al. Low level, long-term inorganic arsenite exposure causes generalized resistance to apoptosis in cultured human keratinocytes: potential role in skin-carcinogenesis. Int J Cancer. 2005;116(1):20-26.
58. Tang DG, Patrawala L, Calhoun T, et al. Prostate cancer stem/progenitor cells: identifcation, characterization, and implications. Mol Carcinog. 2007;46(1):1-14.
59. Rosen JM, Jordan CT. The increasing complexity of the cancer stem cells paradigm. Science. 2009;324(5935):1670-1673.