Role of oxidative stress in stem, cancer, and cancer stem cells

Cancers

Volumn 2, Issue 2, 2010, Pages 859-884

  Abdal Dayem, Ahmed ^a   Choi, Hye Yeon ^a   Kim, Jung Hyun ^a   Cho, Ssang Goo ^a  

^a Konkuk University   (South Korea)

Author keywords

Apoptosis; Autophagy; Cancer stem cells; MAPKs; NF B; Oxidative stress; ROS

Indexed keywords

ANTINEOPLASTIC AGENT; ARTESUNATE; CD24 ANTIGEN; HERMES ANTIGEN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR;

APOPTOSIS; AUTOPHAGY; BREAST CANCER; CANCER CELL; CANCER CONTROL; CANCER GROWTH; CANCER RESISTANCE; CANCER STEM CELL; CARCINOGENESIS; CELL ACTIVATION; CELL ACTIVITY; CELL COUNT; CELL DIFFERENTIATION; CELL DIVISION; CELL FRACTIONATION; CELL HYPOXIA; CELL MATURATION; CELL PROLIFERATION; CELL RENEWAL; CELL STIMULATION; CELL STRESS; CELL SURVIVAL; CELL TRANSFORMATION; DRUG MECHANISM; EMBRYONIC STEM CELL; HEMATOPOIETIC STEM CELL; HUMAN; LEUKEMIA CELL; MALIGNANT NEOPLASTIC DISEASE; METASTASIS POTENTIAL; NEURAL STEM CELL; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PLURIPOTENT STEM CELL; PROSTATE CANCER; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; SOMATIC CELL; STEM CELL;

EID: 79952256467     PISSN: None     EISSN: 20726694     Source Type: Journal    
DOI: 10.3390/cancers2020859     Document Type: Review

References (169)

1. Vishal, R.T.; Sharma, S.; Mahajan, A.; Bardi, G.H. Oxidative Stress: A Novel Strategy in Cancer Treatment. JK Sci. 2005, 7, 1-3.
2. Chandra, J.; Samali, A.; Orrenius, S. Triggering and modulation of apoptosis by oxidative stress. Free Rad. Med. Biol. 2000, 29, 323-333.
3. Poli, G.; Biasi, F.; Chiarpotto, E. Oxidative stress and cell signaling. Curr. Med. Chem. 2004, 11, 1163-1182.
4. Pillai, C.K.; Pillai, K.S. Antioxidants in health. Int. J. Physiol. Pharmacol. 2002, 46, 1-5.
5. Sohal, R.S. Oxidative stress, caloric restriction, and aging. Science 1996, 273, 59-63.
6. Valko, M.; Rhodes, C.J.; Moncol, J.; Izakovic, M.; Mazur, M. Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem. Biol. Interact. 2006, 160, 1-40.
7. Inoue, M.; Nishikawa, M.; Park, A.M.; Kira, Y.; Imada, I.; Utsumi, K. Mitochondrial generation of reactive oxygen species and its role in aerobic life. Curr. Med. Chem. 2003, 10, 2495-2505.
8. Parke, D.V. Chemical toxicity and reactive oxygen species. Int. J. Occup. Med. Environ. Health 1996, 9, 331-340.
9. Waris, G.; Ahsan, H. Reactive oxygen species: Role in the development of cancer and various chronic conditions. J. Carcinog. 2006, 5, 1-8.
10. Ogasawara, M.A.; Zhang, H. Redox regulation and its emerging roles in stem cells and stem-like cancer cells. Antioxid. Redox Signal. 2009, 5, 1107-1122.
11. Nesti, C.; Pasquali, L.; Mancuso, M.; Siciliano, G. The Role of Mitochondria in StemCell Biology. In Stem Cell Biology and Regenerative Medicine Regulatory Networks in Stem Cells; Vinagolu, K.R., Mohan, C.V., Eds.; Memorial Sloan-Kettering Cancer Center: New York, NY, USA, 2009; pp. 135-143.
12. Thomson, J.A.; Odorico, J.S. Human embryonic stem cell and embryonic germ cell lines. Trends Biotechnol. 2000, 18, 53-57.
13. Serakinci, N; Keith, N.W. Therapeutic potential of adult stem cells. Eur. J. Cancer 2006, 42, 1243-1246.
14. Jacks, T.; Weinberg, R.A. Cell-cycle control and its watchman. Nature 1996, 381, 643-644
15. Sugimura, T. A new concept of co-mutagenicity from a phenomenon forgotten for the past two decades: Is it more important than previously expected? Environ. Health Perspect. 1998, 106, A522-A523.
16. Visvader, J.E.; Lindeman, G.J. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat. Rev. Cancer 2008, 8, 755-768.
17. Eyler, C.E; Rich, J.N. Survival of the fittest: cancer stem cells in therapeutic resistance and angiogenesis. J. Clin. Oncol. 2008, 26, 2839-2845.
18. Li, X.; Lewi, M.T.; Huang, J.; Gutierrez, C.; Osborne, C.K.; Wu, M.; Hilsenbeck, S.G.; Pavlick, A.; Xiaomei Zhang, X.; Chamness, G.C.; Wong, H.; Rosen, J.; Chang, J.C. Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. J. Natl. Cancer Inst. 2008, 100, 672-679.
19. Bao, S.; Wu, Q.; McLendon, R.E.; Hao, Y.; Shi, Q.; Hjelmeland, A.B.; Dewhirst, M.W.; Bigner, D.D.; Rich, J.N. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006, 444, 756-760.
20. Dalerba, P.; Cho, R.W.; Clarke, M.F. Cancer stem cells: models and concepts. Annu. Rev. Med.2007, 58, 267-284.
21. Wicha, M.S.; Liu, S.; Dontu, G. Cancer stem cells: an old idea-a paradigm shifts. Cancer Res.2006, 66, 1883-1890.
22. Al-Hajj, M.; Wicha, M.S.; Benito-Hernandez, A.; Morrison, S.J.; Clarke, M.F. Prospective identification of tumorigenic breast cancer cells. Proc. Natl. Acad. Sci. USA 2003, 100, 3983-3988.
23. Collins, A.T.; Berry, P.A.; Hyde, C.; Michael, J.; Stower; M.J.; Maitland, N.J. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res. 2005, 65, 10946-10951.
24. Soltysova, A.; Altanerova, V.; Altaner, C. Cancer stem cells. Neoplasma 2005, 52, 435-440.
25. Jones, R.J.; Matsui, W.H.; Smith, B.D. Cancer stem cells: are we missing the target? J. Natl. Cancer Inst. 2004, 96, 583-585.
26. Dontu, G.; Jackson, K.W.; McNicholas, E.; Kawamura, M.J.; Abdallah, W.M.; Wicha, M.S. Role of Notch signaling in cell-fate determination of human mammary stem/progenitor cells. Breast Cancer Res. 2004, 6, R605-R615.
27. Lowe, S.W.; Sherr, C.J. Tumor suppression by Ink4a-Arf: Progress and puzzles. Curr. Opin. Genet. Dev. 2003, 13, 77-83.
28. Hatsell, S.; Frost, A.R. Hedgehog signaling in mammary gland development and breast cancer. J. Mammary Gland Biol. Neoplasia 2007, 12, 163-173.
29. Lindvall, C.; Bu, W.; Williams, B.O. Wnt signaling, stem cells, and the cellular origin of breast cancer. Stem Cell Rev. 2007, 3, 157-168.
30. Zhou, J.; Wulfkuhle, J.; Zhang, H.; Gu, P.; Yang, Y.; Deng, J.; Margolick, J.B. Liotta, L.A.; Petricoin, E.; Zhang, Y. Activation of the PTEN/mTOR/STAT3 pathway in breast cancer stemlike cells is required for viability and maintenance. Proc. Natl. Acad. Sci. USA 2007, 104, 16158-16163.
31. Prince, M.E.; Sivanandan, R.; Kaczorowski, A.; Wolf, G.T.; Kaplan, M.J.; Dalerba, P.; Weissman, I.L.; Clarke, M.F.; Ailles, L.E. Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proc. Natl. Acad. Sci. USA 2007, 104, 973-978.
32. Shmelkov, S.V.; St Clair, R.; Lyden, D.; Rafii, S. AC133/CD133/Prominin-1. Int. J. Biochem. Cell Biol. 2005, 37, 715-719.
33. Mimeault, M.; Batra, S.K. Recent advances in cancer stem/progenitor cell research: therapeutic implications for overcoming resistance to the most aggressive cancers. J. Cell. Mol. Med. 2007, 11, 981-1011.
34. Kai, K.; Arima, Y.; Kamiya, T.; Saya, H. Breast cancer stem cells. Breast Cancer 2009, 17, 80-85.
35. Zhang, M.; Rosen, J.M. Stem cells in the etiology and treatment of cancer. Curr. Opin. Genet. Dev. 2006, 16, 60-64.
36. Sun, W.; Kang, K.S.; Morita, I.; Trosko, J.E.; Chang, C.C. High susceptibility of a human breast epithelial cell type with stem cell characteristics to telomerase activation and immortalization. Cancer Res. 1999, 59, 6118-6123.
37. -/low cells in breast cancer may not be associated with clinical outcome but may favor distant metastasis. Clin. Cancer Res. 2005, 11, 1154-1159.
38. Kritikou, E.A.; Sharkey, A.; Abell, K.; Came, P.J.; Anderson, E.; Clarkson, R.W.E.; Watson, C.J. A dual, non-redundant, role for LIF as a regulator of development and STAT3-mediated cell death in mammary gland. Development 2003, 130, 3459-3468.
39. Boulanger, C.A.; Wagner, K.U.; Smith, G.H. Parity-induced mouse mammary epithelial cells are pluripotent, self-renewing and sensitive to TGFb1 expression. Oncogene 2005, 24, 552-56.
40. Shipitsin, M.; Campbell, L.L.; Argani, P.; Weremowicz, S.; Bloushtain-Qimron, N.; Yao, J.; Nikolskaya, T.; Serebryiskaya, T.; Beroukhim, R.; Hu, M.; Halushka, M.K.; Saraswati, S.; Parker, L.M.; Anderson, K.S.; Lyndsay, N. Harris, L.N.; Garber, J.E.; Richardson, A.L.; Schnitt, S.J.; Nikolsky, Y.; Gelman, R.S.; Polyak, K. Molecular definition of breast tumor heterogeneity. Cancer Cell 2007, 11, 259-273.
41. Azad, N.; Rojanasakul, Y.; Vallyathan, V. Inflammation and lung cancer: Roles of reactive oxygen/nitrogen species. J. Toxicol. Environ. Health B 2008, 11, 1-15.
42. Vercauteren, S.M.; Sutherland, H.J. CD133 (AC133) expression on AML cells and progenitors. Cytotherapy 2001, 3, 449-45.
43. Kurata, S. Selective activation of p38 MAPK cascade and mitotic arrest caused by low level oxidative stress. J. Biol. Chem. 2000, 275, 23413-23416.
44. Marshall, H.E.; Hess, D.T.; Stamler, J.S. S-Nitrosylation: Physiological regulation of NF-kappaB. Proc. Natl. Acad. Sci. USA 2004, 101, 8841-8842.
45. Xia, Z.; Dickens, M.; Raingeaud, J.; Davis, R.J.; Greenberg, M.E. Opposing effects of ERK and JNK-p38MAPkinases on apoptosis. Science 1995, 270, 1326-1331.
46. Demicco, E.G.; Kavanagh, K.T.; Romieu-Mourez, R.; Xiaobo Wang, X.; Shin, S.R.; Esther Landesman-Bollag, E.; Seldin, D.C.; Sonenshein, G.E. RelB/p52 NF-kappaB complexes rescue an early delay in mammary gland development in transgenic mice with targeted superrepressor IkappaB-alpha expression and promote carcinogenesis of the mammary gland. Mol. Cell Biol.2005, 25, 10136-10147.
47. Cao, Y.; Luo, J.L.; Karin, M. IkappaB kinase alpha kinase activity is required for self-renewal of ErbB2/Her2-transformed mammary tumor-initiating cells. Proc. Natl. Acad. Sci. USA 2007, 104, 15852-15857.
48. Kasper, M.; Jaks, V.; Marie Fiaschi, M.; Rune Toftgård, R. Hedgehog signalling in breast cancer. Carcinogenesis 2009, 30, 903-911.
49. Lam, J.S.; Reiter, R.E. Stem cells in prostate and prostate cancer development. Urol. Oncol. 2006, 24, 131-140.
50. Tang, D.G.; Patrawala, L.; Calhoun, T.; Bhatia, B.; Schneider-Broussard, R.; Choy, G.; Jeter, C. Prostate cancer stem/progenitor cells: identification, characterization and implications. Mol. Carcinogen 2007, 46, 1-14.
51. Liu, A.Y.; True, L.D.; LaTray, L.; Nelson, P.S.; Ellis, W.J.; Vessella, R.L.; Lange, P.H.; Hood, L.; and Van Den Engh, G. Cell-cell interaction in prostate gene regulation and cytodifferentiation. Proc. Natl. Acad. Sci. USA 1997, 94, 10705-10710.
52. Patrawala, L.; Tang, D.G. CD44 as a functional cancer stem cell marker and therapeutic target. In Progress in Gene Therapy: Autologous and Cancer Stem Cell Gene Therapy; Bertolotti, R., Ozawka, K., Eds.; World Scientific: Hacxkensack, NJ, USA, 2008; Volume 3, pp. 317-334.
53. Ricci-Vitiani, L.; Lombardi, D.G.; Pilozzi, E.; Biffoni, M.; Todaro, M.; Peschle, C.; De Maria, R. Identification and expansion of human colon-cancer-initiating cells. Nature 2007, 445, 111-115.
54. Reynolds, B.A.; Weiss, S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992, 255, 1707-1710.
55. - phenotype is enriched in basal-like breast tumors Breast Cancer Res. 2008, 10, R53.
56. Bertucci, F.; Finetti, P.; Cervera, N.; Charafe-Jauffret, E.; Mamessier, E.; Adélaïde, J.; Debono, S.; Houvenaeghel, G.; Maraninchi, D.; Viens, P.; Charpin, C.; Jacquemier, J.; Birnbaum, D. Gene expression profiling of breast cell lines identifies potential new basal markers. Oncogene 2006, 6, 2273-2284.
57. Mark, A.; La Barge, M.A.; Bissell, M.J. Is CD133 a marker of metastatic colon cancer stem cells? J. Clin. Invest.2008, 118, 2021-2024.
58. Singh, S.K.; Clarke, I.D.; Hide, T.; Dirks, P.B. Cancer stem cells in nervous system tumors. Oncogene 2004, 23, 7267-7273.
59. Vercauteren, S.M.; Sutherland, H.J. CD133 (AC133) expression on AML cells and progenitors. Cytotherapy 2001, 3, 449-459.
60. Yin, S.; Li, J.; Hu, C.; Chen, X.; Yao, M.; Yan, M.; Jiang, G.; Ge, C.; Xie, H.; Wan, D.; Yang, S.; Zheng, S.; Gu, J. CD133 positive hepatocellular carcinoma cells possess high capacity for tumorigenicity. Int. J. Cancer 2007, 120, 1444-1450.
61. Wright, M.H.; Calcagno, A.M.; Salcido, C.D.; Carlson, M.D.; Ambudkar, S.V.; Varticovski, L. Brca1 breast tumors contain distinct CD44+/CD24- and CD133+ cells with cancer stem cell characteristics. Breast Cancer Res. 2008, 10, R10.
62. Brantley, D.M.; Chen, C.L.; Muraoka, R.S.; Bushdid, P.B.; Bradberry, J.L. Kittrell, F.; Medina; D.; Matrisian, L.M.; Kerr, L.D.; Yull, F.E. Nuclear factor-kappa B (NF-kappa B) regulates proliferation and branching in mouse mammary epithelium. Mol. Biol. Cell 2001, 12, 1445-1455.
63. Demicco, E.G.; Kavanagh, K.T.; Romieu-Mourez, R.; Wang, X.; Shin, S.R.; Landesman-Bollag, E.; Seldin, D.C.; Sonenshein, G.E. RelB/p52 NF-kappaB complexes rescue an early delay in mammary gland development in transgenic mice with targeted superrepressor IkappaB-alpha expression and promote carcinogenesis of the mammary gland. Mol. Cell Biol. 2005, 25, 10136-10147.
64. Cao, Y.; Luo, J.L.; Karin, M. IkappaB kinase alpha kinase activity is required for self-renewal of ErbB2/Her2-transformed mammary tumor-initiating cells. Proc. Natl. Acad. Sci. USA 2007, 104, 15852-15857.
65. Liu, R.; Wang, X.; Chen, G.Y.; Dalerba, P.; Gurney, A.; Hoey, T.; Sherlock, G.; Lewicki, J.; Shedden, K.; Clarke, M.F. The prognostic role of a gene signature from tumorigenic breastcancer cells. N. Engl. J. Med. 2007, 18, 217-226.
66. Lam, J.S.; Reiter, R.E. Stem cells in prostate and prostate cancer development. Urol. Oncol. 2006, 24, 131-140.
67. Klonisch, T.; Wiechec, E.; Hombach-Klonisch, S.; Ande, S.R.; Wesselborg, S.; Schulze-Osthoff, K.; Los, M. Cancer Stem cell markers in common cancers-therapeutic implications. Trends Mol. Med. 2008, 14, 450-460.
68. Takaishi, S.; Okumura, T.; Tu, S.; Wang, S.W.; Shibata, W.; Vigneshwaran, R.; Gordon, S.A.K.; Shimada, Y.; Wang, T.C. Identification of gastric cancer stem cells using the cell surface marker CD44. Stem Cells 2009, 27, 1006-1020.
69. Jang, Y.Y.; Sharkis, S.J. A low level of reactive oxygen species selects for primitive hematopoietic stem cells that may reside in the low-oxygenic niche. Blood 2007, 110, 3056-3063.
70. Ito, K.; Hirao, A.; Arai, F.; Matsuoka, S.; Takubo, K.; Hamaguchi, I.; Nomiyama, K.; Hosokawa, K.; Sakurada, K.; Nakagata, N.; Ikeda, Y.; Mak, T.W.; Suda, T. Regulation of oxidative stress by ATM is required for self-renewal of haematopoietic stem cells. Nature 2004, 431, 997-1002.
71. Diehn, M.; Cho, R.W.; Lobo, N.A.; Kalisky, T.; Dorie, M.J.; Kulp, A.N.; Qian, D.; Jessica S. Lam, J.S.; Ailles, L.E.; Wong, M.; Joshua, B.; Kaplan, M.J.; Wapnir, I.; Dirbas, F.M.; Somlo, G.; Garberoglio, C.; Paz, B.; Shen, J.;Lau, S.K.; Stephen R. Quake, S.R.; Brown, J.M.; Weissman, I.L.; Clarke, M.F. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 2009, 458, 780-783.
72. Szatrowski, T.P.; Nathan, C.F. Production of large amounts of hydrogen peroxide by human tumor cells. Cancer Res. 1991, 51, 794-798.
73. Kawanishi, S.; Hiraku, Y.; Pinlaor, S.; Ma, N. Oxidative and nitrative DNA damage in animals and patients with inflammatory diseases in relation to inflammation-related carcinogenesis. Biol. Chem. 2006, 387, 365-372.
74. Zhou, Y.; Hileman, E.O.; Plunkett, W.; Keating, M.J.; Huang, P. Free radical stress in chronic lymphocytic leukemia cells and its role in cellular sensitivity to ROS generating anticancer agents. Blood 2003, 101, 4098-4104.
75. Kamiguti, A.S; Serrander, L.; Lin, K.; Harris, R.J.; Cawley, J.C.; Allsup, D.J.; Slupsky, J.R.; Kraus, K.H.; Zuzel, M. Expression and activity of NOX5 in the circulating malignant B cells of hairy cell leukemia. J. Immunol. 2005, 175, 8424-8430.
76. Oberley, T.D.; Oberley, L.W. Antioxidant enzyme levels in cancer. Histol. Histopathol. 1997, 12, 525-535.
77. Hu, Y.; Rosen, D.G.; Zhou, Y.; Feng, L.; Yang, G.; Liu, J. L.; Huang, P. Mitochondrial manganese-superoxide dismutase expression in ovarian cancer: role in cell proliferation and response to oxidative stress. J. Biol. Chem. 2005, 280, 39485-39492.
78. Saydama, N.; Kirb, A.; Demirb, Ö.; Hazanc, E.; Otoc, Ö Saydama, O.; Güner, G. Determination of glutathione, glutathione reductase, glutathione peroxidase and glutathione S-transferase levels in human lung cancer tissues. Cancer 1997, 119, 13-19.
79. Townsend, D.M.; Tew, K.D. The role of glutathione-S-transferase in anti-cancer drug resistance. Oncogene 2003, 22, 7369-7375.
80. Yadav, S.; Zajac, E.; Singhal, S.S.; Awasthi, S. Linking stress-signaling, glutathione metabolism, signaling pathways and xenobiotic transporters. Cancer Metastasis Rev. 2007, 26, 59-69.
81. Trachootham, D.; Zhang, H.; Zhang, W.; Feng, L.; Du, M.; Zhou, Y.; Chen, Z.; Pelicano, H.; Plunkett, W.; Wierda, W.G.; Keating, M.J.; Huang, P. Effective elimination of fludarabineresistant CLL cells by PEITC through a redox-mediated mechanism. Blood 2008, 112, 1912-1922.
82. Zhang, H.; Trachootham, D.; Lu, W.; Carew, J.; Giles, F.J.; Keating, M.J.; Arlinghaus, R.B.; Huang, P. Effective killing of Gleevec-resistant CML cells with T315I mutation by a natural compound PEITC through redox-mediated mechanism. Leukemia 2008, 22, 1191-1199.
83. Naka, K.; Muraguchi, T.; Hoshii, T.; Hirao, A. Regulation of reactive oxygen species and genomic stability in hematopoietic stem cells. Antioxid. Redox Signal. 2008, 10, 1883-1894
84. Toyokuni, S. Novel aspects of oxidative stress associated carcinogenesis. Antioxid. Redox Signal.2006, 8, 1373-1377.
85. Ghaffari, S. Oxidative stress in the regulation of normal and neoplastic hematopoiesis. Antioxid. Redox Signal. 2008, 10, 1923-1940.
86. Lockshin, R.A.; Zakeri, Z. Apoptosis, autophagy, and more. Inter. J. Biochem. Cell Biol. 2004, 36, 2405-2419.
87. Schwartzman, R.A.; Cidlowski, L.A. Apoptosis: the biochemistry and molecular biology of programmed cell death. Endocrine Rev. 1993, 14, 133-151.
88. Ashkenazi, A.; Dixit, V.M. Death receptors: signaling and modulation. Science 1998, 281, 1305-1308.
89. Gorman, A.; McGowan, A.; Cotter, T.G. Role of peroxide and superoxide anion during tumour cell apoptosis. FEBS Lett. 1997, 404, 27-33.
90. 2 and antioxidants have opposite effects on activation of NF-kappa B and AP-1 in intact cells: AP-1 as secondary anti-oxidant responsive factor. EMBO J. 2005, 12, 2005-2015.
91. Gottlieb, E.; Vander Heiden, M.G.; Thompson, C.B. Bcl-x(L) prevents the initial decrease in mitochondrial membrane potential and subsequent reactive oxygen species production during tumor necrosis factor alpha-induced apoptosis. Mol. Cell Biol. 2000, 20, 5680-5689.
92. Price, R.; Vugt, M.V.; Nosten, F.; Luxemburger, C.; Brockman, A.; Phaipun, L.; Chongsuphajaisiddhi, T.; White, N. Artesunate versus artemether for the treatment of recrudescent multidrugresistant Plasmodium falciparum malaria. Am. J. Trop. Med. 1998, 59, 883-888.
93. Ribeiro, I.R.; Ollario, P. Safety of artemisinin and its derivatives. A review of published and unpublished clinical trials. Med. Trop. (Mars) 1998, 58, 50-53.
94. Adjuik, M.; Babiker, A.; Garner, P.; Olliato, P.; Taylor, W.; White, N. International Artemisinin Study Group. Artesunate combinations for treatment of malaria: meta-analysis. Lancet 2004, 363, 9-17.
95. Efferth, T. Molecular pharmacology and pharmacogenomics of artemisinin and its derivatives in cancer cells. Curr. Drug Targets 2006, 7, 407-421.
96. Schulze-Bergkamen, H.; Krar, P.H. Apoptosis in cancer-implications for therapy. Semin. Oncol.2004, 31, 90-119.
97. Debatin, K.M.; Krammer, P.H. Death receptors in chemotherapy and cancer. Oncogene 2004, 23, 2950-2966.
98. Gordi, T.; Lepist, E.I. Artemisinin derivatives: toxic for laboratory animals, safe for humans? Toxicol. Lett. 2004, 147, 539-545.
99. Dell'Eva, R.; Pfeffer, U.; Vene, R.; Anfosso, L.; Forlani, A.; Albini, A.; Efferth, T. Inhibition of angiogenesis in vivo and growth of Kaposi's sarcoma xenograft tumors by the anti-malarial artesunate. Biochem. Pharmacol. 2004, 68, 2359-2366.
100. Orrenius, S. Mitochondrial regulation of apoptotic cell death. Toxicol. Lett. 2004, 149, 19-23.
101. Muller, I.; Niethammer, D.; Bruchelt, G. Anthracycline-derived chemotherapeutics in apoptosis and free radical Cytotoxicity. Int. J. Mol. Med. 1998, 1, 491-494.
102. Efferth, T.; Giaisi, M.; Merling, A.; Krammer, P.H.; Li-Weber, M. Artesunate Induces ROS-Mediated Apoptosis in Doxorubicin-Resistant T Leukemia Cells. PLoS ONE 2007, 2, e693.
103. Eskelinen, E.L. New insights into the mechanisms of macroautophagy in Mammalian cells. Inter. Rev. Cell Mol. Biol. 2008, 266, 207-247.
104. Galluzzi, L.; Maiuri, M.C.; Vitale, I.; Zischka, H.; Castedo, M.; Zitvogel, L.; Kroemer, G. Cell death modalities: classification and pathophysiological implications. Cell Death Differ. 2007, 14, 1237-1243.
105. Kihara, A.; Noda, T.; Ishihara, N.; Ohsumi, Y. Two distinct vps34 phosphatidylinositol-3-kinase complexes function in autophagy and carboxypeptidase Y sorting in Saccharomyces cerevisiae. J. Cell Biol. 2001,152, 519-530.
106. Ohsumi, Y. Molecular dissection of autophagy: two ubiquitin-like systems. Nat. Rev. Mol. Cell Biol. 2001, 2, 211-216.
107. Shintani, T.; Klionsky, D.J. Autophagy in Health and Disease: A Double-Edged Sword. Science 2004, 306, 990-995.
108. Cuervo, A.M. Autophagy: In sickness and in health. Trends Cell Biol. 2004, 14, 70-77.
109. Levine, B. Eating Oneself and Uninvited Guests: Minireview Autophagy-Related Pathways in Cellular Defense. Cell 2005, 120, 159-162.
110. Tu, B.P.; Weissman, J.S. Oxidative protein folding in eukaryotes: mechanisms and consequences. J. Cell Biol. 2004, 164, 341-346.
111. Fariss, M.W.; Chan, C.B.; Patel, M.; Van Houten, B.; Orrenius, S. Role of mitochondria in toxic oxidative stress. Mol. Inter. 2005, 5, 94-111.
112. Wang, S.H.; Shih, Y.L.; Ko, W.C.; Wei, Y.H.; Shih, C.M. Cadmium-induced autophagy and apoptosis are mediated by a calcium signaling pathway. Cell. Mol. Life Sci. 2008, 65, 3640-3652.
113. Wang, S.H.; Shih, Y.L.; Kuo, T.C; Ko, W.C.; Shih, C.M. Cadmium Toxicity toward Autophagy through ROS-Activated GSK-3b in Mesangial Cells. Toxicol. Sci. 2009, 108, 124-131.
114. Gozuacik, D.; Kimchi, A. Autophagy as a cell death and tumor suppressor mechanism. Oncogene 2004, 23, 2891-2906.
115. Levine, B.; Yuan, J. Autophagy in cell death: an innocent convict? J. Clin. Invest. 2005, 115, 2679-2688.
116. Li, N.; Ragheb, K.; Lawler, G.; Sturgis, J.; Rajwa, B.; Melendez, J.A.; Robinson, J.P. Mitochondrial complex I inhibitor rotenone induces apoptosis through enhancing mitochondrial reactive oxygen species production. J. Biol. Chem. 2003, 278, 8516-8525.
117. Pelicano, H.; Carney, D.; Huang, P. ROS stress in cancer cells and therapeutic implications. Drug Resist. Updat.2004, 7, 97-110.
118. Scherz-Shouval, R.; Shvets, E.; Fass, E.; Shorer, H.; Gil, L.; Elazar, Z. Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J. 2007, 26, 1749-1760.
119. Yu, L.; Wan, F.; Dutta, S.; Welsh, S.; Liu, Z.; Freundt, E.; Baehrecke, E.H.; Lenardo, M. Autophagic programmed cell death by selective catalase degradation. Proc. Natl. Acad. Sci. USA 2006, 103, 4952-4957.
120. Reynolds, B.A.; Tetzlaff, W.; Weiss, S. A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes. J. Neurosci. 1992, 12, 4565-4574.
121. Jacks, T.; Weinberg, R.A. Cell-cycle control and its watchman. Nature 1996, 381, 643-644.
122. Sugimura, T. A new concept of co-mutagenicity from a phenomenon forgotten for the past two decades: Is it more important than previously expected? Environ. Health Perspect. 1998, 106, A522-A523.
123. Norman, J.; Cristina Cellurale, K.; Davis, R.J. A Radical Role for p38 MAPK in Tumor Initiation. Cancer Cell 2007, 11, 101-103.
124. Martindale, J.L.; Holbrook, N.J. Cellular response to oxidative stress: signaling for suicide and survival. J. Cell. Physiol. 2002, 192, 1-15.
125. Chatterjee, S.; Fisher, A.B. ROS to the rescue. Am. J. Physiol. Lung Cell Mol. Physiol. 2004, 287, L704-L705.
126. Kurata, S. Selective activation of p38 MAPK cascade and mitotic arrest caused by low level oxidative stress. J. Biol. Chem. 2000, 275, 23413-23416.
127. Marshall, H.E.; Hess, D.T.; Stamler, J.S. S-Nitrosylation: Physiological regulation of NF-kappaB. Proc. Natl. Acad. Sci. USA 2004, 101, 8841-8842.
128. Xia, Z.; Dickens, M.; Raingeaud, J.; Davis, R.J.; Greenberg, M.E. Opposing effects of ERK and JNK-p38MAPkinases on apoptosis. Science 1995, 270, 1326-1331.
129. Wang, D.; Kreutzer, D.A.; Esigmann, J.M. Mutagenicity and repair of oxidative DNA damage: insights from studies using defined lesions. Mutat. Res. 1998, 400, 99-115.
130. Bours, V.; Bentires-Alj, M.; Hellin, A-C.; Viatour, P.; Robe, P.; Delhalle, S.; Benoit, V.; Merville, M-P. Nuclear factor-κB, cancer, and apoptosis. Biochem. Pharmacol.1999, 60, 1085-1090.
131. Kennedy, N.J.; Davis, R.J. Role of JNK in tumor development. Cell Cycle 2003, 2, 199-201.
132. Bulavin, D.V.; Phillips, C.; Nannenga, B.; Timofeev, O.; Donehower, L.A.; Anderson, C.W.; Appella, E.; Fornace, A.J., Jr. Inactivation of the Wip1 phosphatase inhibits mammary tumorigenesis through p38 MAPK-mediated activation of the p16(Ink4a)-p19(Arf) pathway. Nat. Genet. 2004, 36, 343-350.
133. Ivanova, N.B.; Dimos, J.T.; Schaniel, C.; Hackney, J.A.; Moore, K.A.; Lemischka, I.R. A stem cell molecular signature. Science 2002, 298, 601-604.
134. Kunduzova, O.R.; Bianchi, P.; Pizzinat, N.; Escourrou, G.; Seguelas, M.H.; Parini, A.; Cambon, C. Regulation of JNK/ERK activation, cell apoptosis, and tissue regeneration by monoamine oxidases after renal ischemia-reperfusion. FASEB J. 2002, 16, 1129-1131.
135. Morel, A.P.; Marjory Lievre, M.; Thomas, C.; Hinkal, G.; Ansieau, S.; Alain Puisieux, A. Generation of Breast Cancer Stem Cells through Epithelial-Mesenchymal Transition. PLoS ONE 2008, 3, 1-7.
136. Das, B.; Tsuchida, R.; Baruchel, S.; Malkin, D.; Yeger, H. The role of VEGF/Flt1 signaling in the maintenance of neuroblastoma side-population celll "stemness" during hypoxia. In Advances in Neuroblastoma Research meeting, Los Angeles, CA, USA, 17-20 May 2006.
137. Das, B. The role of VEGF autocrine signaling in hypoxia and oxidative stress driven "stemness switch": implications in solid tumor progression and metastasis. PhD thesis, Institute of Medical Sciences, University of Toronto, Canada, 2007.
138. Tsuchida, R.; Das, B.; Yeger, H.; Koren, G.; Shibuya, M.; Thorner, P.S.; Baruchel, S.; Malkin, D. Cisplatin treatment increases survival and expansion of a highly tumorigenic side-population fraction by upregulating VEGF/Flt1 autocrine signaling. Oncogene 2008, 27, 3923-3934.
139. Kunath, T.; Saba-El-Leil, M.; Almousailleakh, M.; Wray, J.; Meloche, S.; Smith, A. FGF stimulation of the Erk1/2 signalling cascade triggers transition of pluripotent embryonic stem cells from self-renewal to lineage commitment. Development 2007, 134, 2895-2902.
140. Ito, K.; Hirao, A.; Arai, F.; Takubo, K.; Matsuoka, S.; Miyamoto, K.; Ohmura, M.; Naka, K.; Hosokawa, K.; Ikeda, Y.; Suda, T. Reactive oxygen species act through p38 MAPK to limit the lifespan of hematopoietic stem cells. Nat. Med. 2006, 12, 446-451.
141. Bonnet, D.; Dick, J.E. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat. Med. 1997, 3, 730-737.
142. Cook, J.A.; Giu, D.; Wink, D.A.; Krishna, M.C.; Russo, A.; Mitchell, J.B. Oxidative stress, redox, and the tumor microenvironment. Semin. Radiat. Oncol. 2004, 14, 259-266.
143. Azad, N.; Rojanasakul, Y.; Vallyathan, V. Inflammation and lung cancer: Roles of reactive oxygen/nitrogen species. J. Toxicol. Environ. Health B 2008 11, 1-15.
144. Dobrovolskaia, M.A.; Kozlov, S.V. Inflammation and cancer: when NF-kappaB amalgamates the perilous partnership. Curr. Cancer Drug Targets 2005, 5, 5325-5344.
145. Karin, M. Nuclear factor-κB in cancer development and progression. Nature 2006, 441, 431-436.
146. Drost, J.; Agami, R. Transformation Locked in a Loop. Cell 2009, 139, 654-656.
147. Klaunig, J.E.; Kamendulis, L.M. The Role of Oxidative Stress in Carcinogenesis. Ann. Rev. Pharmacol. Toxicol. 2004, 44,239-267.
148. Kaltschmidt, B.; Kaltschmidt, C. NF-kB in the nervous system. Nuclear Factor-κB. Regulation and Role in Disease; Beyaert, R., Ed.; Kluwer Academic Publishers: Norwell, MA, USA, 2003, pp. 375-394.
149. Denk, A.; Wirth, T.; Baumann, B. NF-kappaB transcription factors: critical regulators of hematopoiesis and neuronal survival. Cytokine Growth Factor Rev. 2000, 11, 303-320.
150. Qiu, P.; Pan, P.C.; Govind, S. A role for the Drosophila Toll/Cactus pathway in larval hematopoiesis. Development 1998, 125, 1909-1920.
151. Ghosh, S.; May, M.J.; Kopp, E.B. NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses. Annu. Rev. Immunol. 1998, 16, 225-260.
152. Liou, H.C.; Baltimore, D. Regulation of the NF-kappa B/rel transcription factor and I kappa B inhibitor system. Curr. Opin. Cell Biol. 1993, 5, 477-487.
153. Kang, H.B.; Kim, Y.E.; Kwon, H.J.; Sok, D.E.; Lee, Y. Enhancement of NF kappaB expression and activity upon differentiation of human embryonic stem cell line SNUhES3. Stem Cells Dev.2007, 16, 615-623.
154. Molofsky, A.V.; Pardal, R.; Iwashita, T.; Park, I.K.; Clarke, M.F.; Morrison, S. J.Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation. Nature 2003, 425, 962-967.
155. Lessard, J.; Sauvageau, G. Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature 2003a, 423, 255-260.
156. Park, I.K.; Qian, D.; Kiel, M.; Becker, M.W.; Pihalja, M.; Weissman, I.L.; Morrison, S.J.; Clarke, M.F. Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature 2003, 423,302-305.
157. Sawa, M.; Yamamoto, K.; Yokozawa, T.; Kiyoi, H.; Hishida, A.; Kajiguchi, T.; Seto, M.; Kohno, A.; Kitamura, K.; Itoh, Y.; Asou, N.; Hamajima, N.; Emi, N.; Naoe, T. BMI-1 is highly expressed in M0-subtype acute myeloid leukemia. Int. J. Hematol. 2005, 82, 42-47.
158. Androutsellis-Theotokis, A.; Leker, R.R.; Soldner, F.; Hoeppner, D.J.; Ravin, R.; Poser, S.W.; Rueger, M.A.; Bae, S.K.; Kittappa, R.; McKay, R.D.G. Notch signalling regulates stem cell numbers in vitro and in vivo. Nature 2006, 442, 823-826.
159. Lobo, N.A.; Shimono, Y.; Qian, D.; Clarke, M. F. The Biology of Cancer Stem Cells. Annu. Rev. Cell Dev. Biol. 2007, 23, 675-699.
160. Taipale, J.; Beachy, P.A. The Hedgehog and Wnt signaling pathways in cancer. Nature 2001, 411, 349-354.
161. Reya, T.; Duncan, A.W.; Ailles, L.; Domen, J.; Scherer, D.C.; Willert, K.; Hintz, L.; Nusse, R.; Weissman, I.L. A role for Wnt signaling in self-renewal of hematopoietic stem cells. Nature 2003, 423, 409-414.
162. Reguart, N.; He, B.; Taron, M.; You, L.; Jablons, D.M.; Rosell, R. The role of Wnt signaling in cancer and stem cells. Fut. Oncol. 2005, 1, 787-797.
163. Zhang, J.; Grindley, J.C.; Yin, T.; Jayasinghe, S.; He, X.C.; Ross, J.T.; Haug, J.S.; Rupp, D.; Porter-Westpfahl, K.S.; Wiedemann, L.M.; Wu, H.; Li, L. PTEN maintains haematopoietic stem cells and acts in lineage choice and leukaemia prevention. Nature 2006, 441, 518-522.
164. Chow, L.M.; Baker, S.J. PTEN function in normal and neoplastic growth. Cancer Lett. 2006, 241, 184-196.
165. Leung, C.; Lingbeek, M.; Shakhova, O.; Liu, J.; Tanger, E.; Saremaslani, P.; Van Lohuizen, M.; Marino, S. Bmi1 is essential for cerebellar development and is overexpressed in human medulloblastomas. Nature 2004, 428, 337-341.
166. Athar, M.; Tang, X.; Lee, J.L.; Kopelovich, L.; Kim, A.L. Hedgehog signalling in skin development and cancer. Exp. Dermatol. 2006, 15, 667-677.
167. Palma, V.; Lim, D.A.; Dahmane, N.; Sanchez, P.; Brionne, T.C.; Herzberg, C.D.; Gitton, Y.; Carleton, A.; Alvarez-Buylla, A.; Ruiz i Altaba, A. Sonic hedgehog controls stem cell behavior in the postnatal and adult brain. Development 2005, 132, 335-344.
168. Ruizi Altaba, A.; Sanchez, P.; Dahmane, N. Gli and hedgehog in cancer: tumours, embryos and stem cells. Nat. Rev. Cancer 2002, 2, 361-372.
169. Roche, J.; Zeng, C.; Barón, A; Gadgil, S.; Gemmill, R.M.; Tigaud, I.; Thomas X.; Drabkin, H.A. Hox expression in AML identifies a distinct subset of patients with intermediate cytogenetics. Leukemia 2004, 18, 1059-1063.