Reactive oxygen species in cancer stem cells

Antioxidants and Redox Signaling

Volumn 16, Issue 11, 2012, Pages 1215-1228

  Shi, Xiaoke ^a,b   Zhang, Yan ^b   Zheng, Junheng ^b   Pan, Jingxuan ^a,b  

^a SUN YAT SEN UNIVERSITY   (China)

^b SUN YAT SEN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PR DOMAIN CONTAINING 16; PROTEIN; PROTEIN P53; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR FKHRL1; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; XENOBIOTIC AGENT;

ATAXIA TELANGIECTASIA; CANCER CELL; CANCER STEM CELL; CELL RENEWAL; HEMATOPOIETIC STEM CELL; HUMAN; HYPOXIA; MEDICAL RESEARCH; METASTASIS; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVIEW; TUMOR GROWTH; TUMOR MICROENVIRONMENT;

HUMANS; NEOPLASTIC STEM CELLS; REACTIVE OXYGEN SPECIES;

EID: 84859829553     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2012.4529     Document Type: Review

References (134)

1. Abbas HA, Maccio DR, Coskun S, Jackson JG, Hazen AL, Sills TM, You MJ, Hirschi KK, and Lozano G. Mdm2 is required for survival of hematopoietic stem cells/progenitors via dampening of ROS-induced p53 activity. Cell Stem Cell 7: 606-617, 2010.
2. Abbott A. Stem cells: the cell division. Nature 480: 310-312, 2011.
3. Abdel-Wahab O and Levine RL. Metabolism and the leukemic stem cell. J Exp Med 207: 677-680, 2010.
4. Achanta G, Sasaki R, Feng L, Carew JS, Lu W, Pelicano H, Keating MJ, and Huang P. Novel role of p53 in maintaining mitochondrial genetic stability through interaction with DNA Pol gamma. EMBO J 24: 3482-3492, 2005. (Pubitemid 41486785)
5. Adhikari AS, Agarwal N, Wood BM, Porretta C, Ruiz B, Pochampally RR, and Iwakuma T. CD117 and Stro-1 identify osteosarcoma tumor-initiating cells associated with metastasis and drug resistance. Cancer Res 70: 4602-4612, 2010.
6. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, and Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 100: 3983-3988, 2003. (Pubitemid 36418143)
7. Alvero AB, Fu HH, Holmberg J, Visintin I, Mor L, Marquina CC, Oidtman J, Silasi DA, and Mor G. Stem-like ovarian cancer cells can serve as tumor vascular progenitors. Stem Cells 27: 2405-2413, 2009.
8. Arai F, Hirao A, Ohmura M, Sato H, Matsuoka S, Takubo K, Ito K, Koh GY, and Suda T. Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell 118: 149-161, 2004. (Pubitemid 38962572)
9. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD, and Rich JN. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444: 756-760, 2006. (Pubitemid 44949604)
10. Barker N, Ridgway RA, van Es JH, van de Wetering M, Begthel H, van den Born M, Danenberg E, Clarke AR, Sansom OJ, and Clevers H. Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 457: 608-611, 2009.
11. Bell EL, Klimova TA, Eisenbart J, Moraes CT, Murphy MP, Budinger GR, and Chandel NS. The Qo site of the mitochondrial complex III is required for the transduction of hypoxic signaling via reactive oxygen species production. J Cell Biol 177: 1029-1036, 2007. (Pubitemid 46955707)
12. Bilbao PS, Santillan G, and Boland R. ATP stimulates the proliferation of MCF-7 cells through the PI3K/Akt signaling pathway. Arch Biochem Biophys 499: 40-48, 2010.
13. Boiko AD, Razorenova OV, van de Rijn M, Swetter SM, Johnson DL, Ly DP, Butler PD, Yang GP, Joshua B, Kaplan MJ, Longaker MT, and Weissman IL. Human melanomainitiating cells express neural crest nerve growth factor receptor CD271. Nature 466: 133-137, 2010.
14. Bonnet D and Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 3: 730-737, 1997. (Pubitemid 27298715)
15. Brandon M, Baldi P, and Wallace DC. Mitochondrial mutations in cancer. Oncogene 25: 4647-4662, 2006. (Pubitemid 44187615)
16. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J, and Greenberg ME. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96: 857-868, 1999. (Pubitemid 29165088)
17. Carew JS, Zhou Y, Albitar M, Carew JD, Keating MJ, and Huang P. Mitochondrial DNA mutations in primary leukemia cells after chemotherapy: clinical significance and therapeutic implications. Leukemia 17: 1437-1447, 2003. (Pubitemid 36986944)
18. Chan K and Kan YW. Nrf2 is essential for protection against acute pulmonary injury in mice. Proc Natl Acad Sci USA 96: 12731-12736, 1999. (Pubitemid 29513571)
19. Chan KS, Espinosa I, Chao M, Wong D, Ailles L, Diehn M, Gill H, Presti J Jr., Chang HY, van de Rijn M, Shortliffe L, and Weissman IL. Identification, molecular characterization, clinical prognosis, and therapeutic targeting of human bladder tumor-initiating cells. Proc Natl Acad Sci USA 106: 14016-14021, 2009.
20. Chandel NS, Maltepe E, Goldwasser E, Mathieu CE, Simon MC, and Schumacker PT. Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc Natl Acad Sci USA 95: 11715-11720, 1998. (Pubitemid 28460480)
21. Chen C, Liu Y, Liu R, Ikenoue T, Guan KL, Liu Y, and Zheng P. TSC-mTOR maintains quiescence and function of hematopoietic stem cells by repressing mitochondrial biogenesis and reactive oxygen species. J Exp Med 205: 2397-2408, 2008.
22. Chen W, Druhan LJ, Chen CA, Hemann C, Chen YR, Berka V, Tsai AL, and Zweier JL. Peroxynitrite induces destruction of the tetrahydrobiopterin and heme in endothelial nitric oxide synthase: transition from reversible to irreversible enzyme inhibition. Biochemistry 49: 3129-3137, 2010.
23. Chen YC, Chen YW, Hsu HS, Tseng LM, Huang PI, Lu KH, Chen DT, Tai LK, Yung MC, Chang SC, Ku HH, Chiou SH, and Lo WL. Aldehyde dehydrogenase 1 is a putative marker for cancer stem cells in head and neck squamous cancer. Biochem Biophys Res Commun 385: 307-313, 2009.
24. Chuikov S, Levi BP, Smith ML, and Morrison SJ. Prdm16 promotes stem cell maintenance in multiple tissues, partly by regulating oxidative stress. Nat Cell Biol 12: 999-1006, 2010.
25. Cicalese A, Bonizzi G, Pasi CE, Faretta M, Ronzoni S, Giulini B, Brisken C, Minucci S, Di Fiore PP, and Pelicci PG. The tumor suppressor p53 regulates polarity of self-renewing divisions in mammary stem cells. Cell 138: 1083-1095, 2009.
26. Cipolleschi MG, Rovida E, Ivanovic Z, Praloran V, Olivotto M, and Dello Sbarba P. The expansion of murine bone marrow cells preincubated in hypoxia as an in vitro indicator of their marrow-repopulating ability. Leukemia 14: 735-739, 2000. (Pubitemid 30195468)
27. Clement V, Marino D, Cudalbu C, Hamou MF, Mlynarik V, de Tribolet N, Dietrich PY, Gruetter R, Hegi ME, and Radovanovic I. Marker-independent identification of gliomainitiating cells. Nat Methods 7: 224-228, 2010.
28. Collins AT, Berry PA, Hyde C, Stower MJ, and Maitland NJ. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res 65: 10946-10951, 2005. (Pubitemid 41713363)
29. Cosentino C, Grieco D, and Costanzo V. ATM activates the pentose phosphate pathway promoting anti-oxidant defence and DNA repair. EMBO J 30: 546-555, 2011.
30. Cox CV, Evely RS, Oakhill A, Pamphilon DH, Goulden NJ, and Blair A. Characterization of acute lymphoblastic leukemia progenitor cells. Blood 104: 2919-2925, 2004. (Pubitemid 39434980)
31. Curley MD, Therrien VA, Cummings CL, Sergent PA, Koulouris CR, Friel AM, Roberts DJ, Seiden MV, Scadden DT, Rueda BR, and Foster R. CD133 expression defines a tumor initiating cell population in primary human ovarian cancer. Stem Cells 27: 2875-2883, 2009.
32. Dalerba P, Dylla SJ, Park IK, Liu R, Wang X, Cho RW, Hoey T, Gurney A, Huang EH, Simeone DM, Shelton AA, Parmiani G, Castelli C, and Clarke MF. Phenotypic characterization of human colorectal cancer stem cells. Proc Natl Acad Sci USA 104: 10158-10163, 2007. (Pubitemid 47175279)
33. Dey-Guha I, Wolfer A, Yeh AC, J GA, Darp R, Leon E, Wulfkuhle J, Petricoin EF 3rd, Wittner BS, and Ramaswamy S. Asymmetric cancer cell division regulated by AKT. Proc Natl Acad Sci USA 108: 12845-12850, 2011.
34. Diehn M, Cho RW, Lobo NA, Kalisky T, Dorie MJ, Kulp AN, Qian D, Lam JS, Ailles LE, Wong M, Joshua B, Kaplan MJ, Wapnir I, Dirbas FM, Somlo G, Garberoglio C, Paz B, Shen J, Lau SK, Quake SR, Brown JM, Weissman IL, and Clarke MF. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 458: 780-783, 2009.
35. Donald SP, Sun XY, Hu CA, Yu J, Mei JM, Valle D, and Phang JM. Proline oxidase, encoded by p53-induced gene-6, catalyzes the generation of proline-dependent reactive oxygen species. Cancer Res 61: 1810-1815, 2001. (Pubitemid 32691989)
36. Eramo A, Lotti F, Sette G, Pilozzi E, Biffoni M, Di Virgilio A, Conticello C, Ruco L, Peschle C, and De Maria R. Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ 15: 504-514, 2008. (Pubitemid 351267301)
37. Fang D, Nguyen TK, Leishear K, Finko R, Kulp AN, Hotz S, Van Belle PA, Xu X, Elder DE, and Herlyn M. A tumorigenic subpopulation with stem cell properties in melanomas. Cancer Res 65: 9328-9337, 2005. (Pubitemid 41508000)
38. Fuchs E. The tortoise and the hair: slow-cycling cells in the stem cell race. Cell 137: 811-819, 2009.
39. Fujisaki J, Wu J, Carlson AL, Silberstein L, Putheti P, Larocca R, Gao W, Saito TI, Lo Celso C, Tsuyuzaki H, Sato T, Cote D, Sykes M, Strom TB, Scadden DT, and Lin CP. In vivo imaging of Treg cells providing immune privilege to the haematopoietic stem-cell niche. Nature 474: 216-219, 2011.
40. Gibbs CP, Kukekov VG, Reith JD, Tchigrinova O, Suslov ON, Scott EW, Ghivizzani SC, Ignatova TN, and Steindler DA. Stem-like cells in bone sarcomas: implications for tumorigenesis. Neoplasia 7: 967-976, 2005.
41. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, Jacquemier J, Viens P, Kleer CG, Liu S, Schott A, Hayes D, Birnbaum D, Wicha MS, and Dontu G. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 1: 555-567, 2007. (Pubitemid 350056407)
42. Gupta PB, Chaffer CL, and Weinberg RA. Cancer stem cells: mirage or reality? Nat Med 15: 1010-1012, 2009.
43. Gupta SC, Hevia D, Patchva S, Park B, Koh W, and Aggarwal BB. Upsides and downsides of reactive oxygen species for cancer: the roles of reactive oxygen species in tumorigenesis, prevention, and therapy. Antioxid Redox Signal 16: 1295-1322, 2012.
44. Guzman ML, Rossi RM, Karnischky L, Li X, Peterson DR, Howard DS, and Jordan CT. The sesquiterpene lactone parthenolide induces apoptosis of human acute myelogenous leukemia stem and progenitor cells. Blood 105: 4163-4169, 2005. (Pubitemid 40720758)
45. Haghdoost S, Czene S, Naslund I, Skog S, and Harms-Ringdahl M. Extracellular 8-oxo-dG as a sensitive parameter for oxidative stress in vivo and in vitro. Free Radic Res 39: 153-162, 2005. (Pubitemid 40425737)
46. Haraguchi N, Ishii H, Mimori K, Tanaka F, Ohkuma M, Kim HM, Akita H, Takiuchi D, Hatano H, Nagano H, Barnard GF, Doki Y, and Mori M. CD13 is a therapeutic target in human liver cancer stem cells. J Clin Invest 120: 3326-3339, 2010.
47. Hermann PC, Huber SL, Herrler T, Aicher A, Ellwart JW, Guba M, Bruns CJ, and Heeschen C. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 1: 313-323, 2007. (Pubitemid 47355323)
48. Hills M, Lucke K, Chavez EA, Eaves CJ, and Lansdorp PM. Probing the mitotic history and developmental stage of hematopoietic cells using single telomere length analysis (STELA). Blood 113: 5765-5775, 2009.
49. Huang EH, Hynes MJ, Zhang T, Ginestier C, Dontu G, Appelman H, Fields JZ, Wicha MS, and Boman BM. Aldehyde dehydrogenase 1 is a marker for normal and malignant human colonic stem cells (SC) and tracks SC overpopulation during colon tumorigenesis. Cancer Res 69: 3382-3389, 2009.
50. Huang J, Yang J, Maity B, Mayuzumi D, and Fisher RA. Regulator of G protein signaling 6 mediates doxorubicininduced ATM and p53 activation by a reactive oxygen species-dependent mechanism. Cancer Res 71: 6310-6319, 2011.
51. Huang P, Feng L, Oldham EA, Keating MJ, and Plunkett W. Superoxide dismutase as a target for the selective killing of cancer cells. Nature 407: 390-395, 2000.
52. Indo HP, Davidson M, Yen HC, Suenaga S, Tomita K, Nishii T, Higuchi M, Koga Y, Ozawa T, and Majima HJ. Evidence of ROS generation by mitochondria in cells with impaired electron transport chain and mitochondrial DNA damage. Mitochondrion 7: 106-118, 2007. (Pubitemid 46351959)
53. Inui M, Martello G, and Piccolo S. MicroRNA control of signal transduction. Nat Rev Mol Cell Biol 11: 252-263, 2010.
54. Irani K, Xia Y, Zweier JL, Sollott SJ, Der CJ, Fearon ER, Sundaresan M, Finkel T, and Goldschmidt-Clermont PJ. Mitogenic signaling mediated by oxidants in Ras-transformed fibroblasts. Science 275: 1649-1652, 1997. (Pubitemid 27120541)
55. Ishikawa K, Koshikawa N, Takenaga K, Nakada K, and Hayashi J. Reversible regulation of metastasis by ROSgenerating mtDNA mutations. Mitochondrion 8: 339-344, 2008.
56. Ishimoto T, Nagano O, Yae T, Tamada M, Motohara T, Oshima H, Oshima M, Ikeda T, Asaba R, Yagi H, Masuko T, Shimizu T, Ishikawa T, Kai K, Takahashi E, Imamura Y, Baba Y, Ohmura M, Suematsu M, Baba H, and Saya H. CD44 variant regulates redox status in cancer cells by stabilizing the xCT subunit of system xc(-) and thereby promotes tumor growth. Cancer Cell 19: 387-400, 2011.
57. Ito K, Bernardi R, Morotti A, Matsuoka S, Saglio G, Ikeda Y, Rosenblatt J, Avigan DE, Teruya-Feldstein J, and Pandolfi PP. PML targeting eradicates quiescent leukaemiainitiating cells. Nature 453: 1072-1078, 2008. (Pubitemid 351871736)
58. Ito K, Hirao A, Arai F, Matsuoka S, Takubo K, Hamaguchi I, Nomiyama K, Hosokawa K, Sakurada K, Nakagata N, Ikeda Y, Mak TW, and Suda T. Regulation of oxidative stress by ATM is required for self-renewal of haematopoietic stem cells. Nature 431: 997-1002, 2004. (Pubitemid 39434422)
59. Ito K, Hirao A, Arai F, Takubo K, Matsuoka S, Miyamoto K, Ohmura M, Naka K, Hosokawa K, Ikeda Y, and Suda T. Reactive oxygen species act through p38 MAPK to limit the lifespan of hematopoietic stem cells. Nat Med 12: 446-451, 2006.
60. Jang YY and Sharkis SJ. A low level of reactive oxygen species selects for primitive hematopoietic stem cells that may reside in the low-oxygenic niche. Blood 110: 3056-3063, 2007. (Pubitemid 350006961)
61. Jin L, Hope KJ, Zhai Q, Smadja-Joffe F, and Dick JE. Targeting of CD44 eradicates human acute myeloid leukemic stem cells. Nat Med 12: 1167-1174, 2006. (Pubitemid 44527352)
62. Jin L, Lee EM, Ramshaw HS, Busfield SJ, Peoppl AG, Wilkinson L, Guthridge MA, Thomas D, Barry EF, Boyd A, Gearing DP, Vairo G, Lopez AF, Dick JE, and Lock RB. Monoclonal antibody-mediated targeting of CD123, IL-3 receptor alpha chain, eliminates human acute myeloid leukemic stem cells. Cell Stem Cell 5: 31-42, 2009.
63. Jin Y, Lu Z, Ding K, Li J, Du X, Chen C, Sun X, Wu Y, Zhou J, and Pan J. Antineoplastic mechanisms of niclosamide in acute myelogenous leukemia stem cells: inactivation of the NF-kappaB pathway and generation of reactive oxygen species. Cancer Res 70: 2516-2527, 2010.
64. Jordan CT, Upchurch D, Szilvassy SJ, Guzman ML, Howard DS, Pettigrew AL, Meyerrose T, Rossi R, Grimes B, Rizzieri DA, Luger SM, and Phillips GL. The interleukin-3 receptor alpha chain is a unique marker for human acute myelogenous leukemia stem cells. Leukemia 14: 1777-1784, 2000.
65. Juntilla MM, Patil VD, Calamito M, Joshi RP, Birnbaum MJ, and Koretzky GA. AKT1 and AKT2 maintain hematopoietic stem cell function by regulating reactive oxygen species. Blood 115: 4030-4038, 2010.
66. Kensler TW, Wakabayashi N, and Biswal S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol 47: 89-116, 2007.
67. Kim CF, Jackson EL, Woolfenden AE, Lawrence S, Babar I, Vogel S, Crowley D, Bronson RT, and Jacks T. Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell 121: 823-835, 2005. (Pubitemid 40806415)
68. Kim HM, Haraguchi N, Ishii H, Ohkuma M, Okano M, Mimori K, Eguchi H, Yamamoto H, Nagano H, Sekimoto M, Doki Y, and Mori M. Increased CD13 expression reduces reactive oxygen species, promoting survival of liver cancer stem cells via an epithelial-mesenchymal transitionlike phenomenon. Ann Surg Oncol 2011; [Epub ahead of print]; DOI: 10.1245/s10434-011-2040-5.
69. Kim J and Wong PK. Loss of ATM impairs proliferation of neural stem cells through oxidative stress-mediated p38 MAPK signaling. Stem Cells 27: 1987-1998, 2009.
70. Kim JH, Chu SC, Gramlich JL, Pride YB, Babendreier E, Chauhan D, Salgia R, Podar K, Griffin JD, and Sattler M. Activation of the PI3K/mTOR pathway by BCR-ABL contributes to increased production of reactive oxygen species. Blood 105: 1717-1723, 2005. (Pubitemid 40223695)
71. Kopnin PB, Agapova LS, Kopnin BP, and Chumakov PM. Repression of sestrin family genes contributes to oncogenic Ras-induced reactive oxygen species up-regulation and genetic instability. Cancer Res 67: 4671-4678, 2007. (Pubitemid 46910172)
72. Kwon C, Cheng P, King IN, Andersen P, Shenje L, Nigam V, and Srivastava D. Notch post-translationally regulates beta-catenin protein in stem and progenitor cells. Nat Cell Biol 13: 1244-1251, 2011.
73. Kyo S, Maida Y, and Inoue M. Stem cells in endometrium and endometrial cancer: accumulating evidence and unresolved questions. Cancer Lett 308: 123-133, 2011.
74. Lapidot T, Sirard C, Vormoor J, Murdoch B, Hoang T, Caceres-Cortes J, Minden M, Paterson B, Caligiuri MA, and Dick JE. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 367: 645-648, 1994. (Pubitemid 24067706)
75. Le Belle JE, Orozco NM, Paucar AA, Saxe JP, Mottahedeh J, Pyle AD, Wu H, and Kornblum HI. Proliferative neural stem cells have high endogenous ROS levels that regulate self-renewal and neurogenesis in a PI3K/Akt-dependant manner. Cell Stem Cell 8: 59-71, 2011.
76. Lee JY, Nakada D, Yilmaz OH, Tothova Z, Joseph NM, Lim MS, Gilliland DG, and Morrison SJ. mTOR activation induces tumor suppressors that inhibit leukemogenesis and deplete hematopoietic stem cells after Pten deletion. Cell Stem Cell 7: 593-605, 2010.
77. Lee TK, Castilho A, Cheung VC, Tang KH, Ma S, and Ng IO. CD24( + ) liver tumor-initiating cells drive self-renewal and tumor initiation through STAT3-mediated NANOG regulation. Cell Stem Cell 9: 50-63, 2011.
78. MacKenzie ED, Selak MA, Tennant DA, Payne LJ, Crosby S, Frederiksen CM, Watson DG, and Gottlieb E. Cell-permeating alpha-ketoglutarate derivatives alleviate pseudohypoxia in succinate dehydrogenase-deficient cells. Mol Cell Biol 27: 3282-3289, 2007. (Pubitemid 46685207)
79. Majeti R, Chao MP, Alizadeh AA, Pang WW, Jaiswal S, Gibbs KD Jr., van Rooijen N, and Weissman IL. CD47 is an adverse prognostic factor and therapeutic antibody target on human acute myeloid leukemia stem cells. Cell 138: 286-299, 2009.
80. Malanchi I, Peinado H, Kassen D, Hussenet T, Metzger D, Chambon P, Huber M, Hohl D, Cano A, Birchmeier W, and Huelsken J. Cutaneous cancer stem cell maintenance is dependent on beta-catenin signalling. Nature 452: 650-653, 2008. (Pubitemid 351483363)
81. Merchant AA, Singh A, Matsui W, and Biswal S. The redox-sensitive transcription factor, Nrf2, regulates murine hematopoietic stem cell survival independent of ROS levels. Blood 118: 6572-6579, 2011.
82. Miyamoto K, Araki KY, Naka K, Arai F, Takubo K, Yamazaki S, Matsuoka S, Miyamoto T, Ito K, Ohmura M, Chen C, Hosokawa K, Nakauchi H, Nakayama K, Nakayama KI, Harada M, Motoyama N, Suda T, and Hirao A. Foxo3a is essential for maintenance of the hematopoietic stem cell pool. Cell Stem Cell 1: 101-112, 2007. (Pubitemid 46865800)
83. Morrison SJ and Spradling AC. Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell 132: 598-611, 2008. (Pubitemid 351253690)
84. Nguyen LV, Vanner R, Dirks P, and Eaves CJ. Cancer stem cells: an evolving concept. Nat Rev Cancer 12: 133-143, 2012.
85. O'Brien CA, Pollett A, Gallinger S, and Dick JE. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 445: 106-110, 2007. (Pubitemid 46067310)
86. Pan J, She M, Xu ZX, Sun L, and Yeung SC. Farnesyltransferase inhibitors induce DNA damage via reactive oxygen species in human cancer cells. Cancer Res 65: 3671-3681, 2005. (Pubitemid 40616344)
87. Park BS, Kim WS, Choi JS, Kim HK, Won JH, Ohkubo F, and Fukuoka H. Hair growth stimulated by conditioned medium of adipose-derived stem cells is enhanced by hypoxia: evidence of increased growth factor secretion. Biomed Res 31: 27-34, 2010.
88. Pece S, Tosoni D, Confalonieri S, Mazzarol G, Vecchi M, Ronzoni S, Bernard L, Viale G, Pelicci PG, and Di Fiore PP. Biological and molecular heterogeneity of breast cancers correlates with their cancer stem cell content. Cell 140: 62-73, 2010.
89. Pervaiz S, Taneja R, and Ghaffari S. Oxidative stress regulation of stem and progenitor cells. Antioxid Redox Signal 11: 2777-2789, 2009.
90. Phillips TM, McBride WH, and Pajonk F. The response of CD24(-/low)/CD44 + breast cancer-initiating cells to radiation. J Natl Cancer Inst 98: 1777-1785, 2006. (Pubitemid 46017929)
91. Ping YF and Bian XW. Consice review: Contribution of cancer stem cells to neovascularization. Stem Cells 29: 888-894, 2011.
92. Prince ME, Sivanandan R, Kaczorowski A, Wolf GT, Kaplan MJ, Dalerba P, Weissman IL, Clarke MF, and Ailles LE. Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proc Natl Acad Sci USA 104: 973-978, 2007. (Pubitemid 46154721)
93. Quintana E, Shackleton M, Foster HR, Fullen DR, Sabel MS, Johnson TM, and Morrison SJ. Phenotypic heterogeneity among tumorigenic melanoma cells from patients that is reversible and not hierarchically organized. Cancer Cell 18: 510-523, 2010.
94. Raj L, Ide T, Gurkar AU, Foley M, Schenone M, Li X, Tolliday NJ, Golub TR, Carr SA, Shamji AF, Stern AM, Mandinova A, Schreiber SL, and Lee SW. Selective killing of cancer cells by a small molecule targeting the stress response to ROS. Nature 475: 231-234, 2011.
95. Rehn M, Olsson A, Reckzeh K, Diffner E, Carmeliet P, Landberg G, and Cammenga J. Hypoxic induction of vascular endothelial growth factor regulates murine hematopoietic stem cell function in the low-oxygenic niche. Blood 118: 1534-1543, 2011.
96. Reya T, Duncan AW, Ailles L, Domen J, Scherer DC, Willert K, Hintz L, Nusse R, and Weissman IL. A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature 423: 409-414, 2003. (Pubitemid 36626987)
97. Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, Peschle C, and De Maria R. Identification and expansion of human colon-cancer-initiating cells. Nature 445: 111-115, 2007. (Pubitemid 46067311)
98. Ricci-Vitiani L, Pallini R, Biffoni M, Todaro M, Invernici G, Cenci T, Maira G, Parati EA, Stassi G, Larocca LM, and De Maria R. Tumour vascularization via endothelial differentiation of glioblastoma stem-like cells. Nature 468: 824-828, 2010.
99. Roesch A, Fukunaga-Kalabis M, Schmidt EC, Zabierowski SE, Brafford PA, Vultur A, Basu D, Gimotty P, Vogt T, and Herlyn M. A temporarily distinct subpopulation of slowcycling melanoma cells is required for continuous tumor growth. Cell 141: 583-594, 2010.
100. Sattler M, Verma S, Shrikhande G, Byrne CH, Pride YB, Winkler T, Greenfield EA, Salgia R, and Griffin JD. The BCR/ABL tyrosine kinase induces production of reactive oxygen species in hematopoietic cells. J Biol Chem 275: 24273-24278, 2000. (Pubitemid 30626515)
101. Schatton T, Murphy GF, Frank NY, Yamaura K, Waaga-Gasser AM, Gasser M, Zhan Q, Jordan S, Duncan LM, Weishaupt C, Fuhlbrigge RC, Kupper TS, Sayegh MH, and Frank MH. Identification of cells initiating human melanomas. Nature 451: 345-349, 2008.
102. Schepers H, van Gosliga D, Wierenga AT, Eggen BJ, Schuringa JJ, and Vellenga E. STAT5 is required for longterm maintenance of normal and leukemic human stem/progenitor cells. Blood 110: 2880-2888, 2007. (Pubitemid 350006941)
103. Schober M and Fuchs E. Tumor-initiating stem cells of squamous cell carcinomas and their control by TGF-beta and integrin/focal adhesion kinase (FAK) signaling. Proc Natl Acad Sci USA 108: 10544-10549, 2011.
104. She M, Yang H, Sun L, and Yeung SC. Redox control of manumycin A-induced apoptosis in anaplastic thyroid cancer cells: involvement of the xenobiotic apoptotic pathway. Cancer Biol Ther 5: 275-280, 2006.
105. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, and Dirks PB. Identification of human brain tumour initiating cells. Nature 432: 396-401, 2004. (Pubitemid 39551674)
106. Son MJ, Woolard K, Nam DH, Lee J, and Fine HA. SSEA-1 is an enrichment marker for tumor-initiating cells in human glioblastoma. Cell Stem Cell 4: 440-452, 2009.
107. Stingl J, Eirew P, Ricketson I, Shackleton M, Vaillant F, Choi D, Li HI, and Eaves CJ. Purification and unique properties of mammary epithelial stem cells. Nature 439: 993-997, 2006. (Pubitemid 43292419)
108. Suetsugu A, Nagaki M, Aoki H, Motohashi T, Kunisada T, and Moriwaki H. Characterization of CD133 + hepatocellular carcinoma cells as cancer stem/progenitor cells. Biochem Biophys Res Commun 351: 820-824, 2006. (Pubitemid 44715858)
109. Szatrowski TP and Nathan CF. Production of large amounts of hydrogen peroxide by human tumor cells. Cancer Res 51: 794-798, 1991.
110. Takubo K, Goda N, Yamada W, Iriuchishima H, Ikeda E, Kubota Y, Shima H, Johnson RS, Hirao A, Suematsu M, and Suda T. Regulation of the HIF-1alpha level is essential for hematopoietic stem cells. Cell Stem Cell 7: 391-402, 2010.
111. Thimmulappa RK, Mai KH, Srisuma S, Kensler TW, Yamamoto M, and Biswal S. Identification of Nrf2-regulated genes induced by the chemopreventive agent sulforaphane by oligonucleotide microarray. Cancer Res 62: 5196-5203, 2002. (Pubitemid 35033454)
112. Tothova Z, Kollipara R, Huntly BJ, Lee BH, Castrillon DH, Cullen DE, McDowell EP, Lazo-Kallanian S, Williams IR, Sears C, Armstrong SA, Passegue E, DePinho RA, and Gilliland DG. FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell 128: 325-339, 2007. (Pubitemid 46137992)
113. Trachootham D, Alexandre J, and Huang P. Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach? Nat Rev Drug Discov 8: 579-591, 2009.
114. Trachootham D, Zhang H, Zhang W, Feng L, Du M, Zhou Y, Chen Z, Pelicano H, Plunkett W, Wierda WG, Keating MJ, and Huang P. Effective elimination of fludarabine-resistant CLL cells by PEITC through a redox-mediated mechanism. Blood 112: 1912-1922, 2008.
115. Vafa O, Wade M, Kern S, Beeche M, Pandita TK, Hampton GM, and Wahl GM. c-Myc can induce DNA damage, increase reactive oxygen species, and mitigate p53 function: a mechanism for oncogene-induced genetic instability. Mol Cell 9: 1031-1044, 2002. (Pubitemid 34626672)
116. Venkataraman S, Alimova I, Fan R, Harris P, Foreman N, and Vibhakar R. MicroRNA 128a increases intracellular ROS level by targeting Bmi-1 and inhibits medulloblastoma cancer cell growth by promoting senescence. PLoS One 5: e10748, 2010.
117. Visvader JE and Lindeman GJ. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer 8: 755-768, 2008.
118. Vollrath V, Wielandt AM, Iruretagoyena M, and Chianale J. Role of Nrf2 in the regulation of the Mrp2 (ABCC2) gene. Biochem J 395: 599-609, 2006.
119. Ward PS, Patel J, Wise DR, Abdel-Wahab O, Bennett BD, Coller HA, Cross JR, Fantin VR, Hedvat CV, Perl AE, Rabinowitz JD, Carroll M, Su SM, Sharp KA, Levine RL, and Thompson CB. The common feature of leukemia-associated IDH1 and IDH2 mutations is a neomorphic enzyme activity converting alpha-ketoglutarate to 2-hydroxyglutarate. Cancer Cell 17: 225-234, 2010.
120. West AP, Brodsky IE, Rahner C, Woo DK, Erdjument-Bromage H, Tempst P, Walsh MC, Choi Y, Shadel GS, and Ghosh S. TLR signalling augments macrophage bactericidal activity through mitochondrial ROS. Nature 472: 476-480, 2011.
121. Wiseman RL, Chin KT, Haynes CM, Stanhill A, Xu CF, Roguev A, Krogan NJ, Neubert TA, and Ron D. Thioredoxin-related Protein 32 is an arsenite-regulated Thiol Reductase of the proteasome 19 S particle. J Biol Chem 284: 15233-15245, 2009.
122. Wu XJ, Kassie F, and Mersch-Sundermann V. The role of reactive oxygen species (ROS) production on diallyl disulfide (DADS) induced apoptosis and cell cycle arrest in human A549 lung carcinoma cells. Mutat Res 579: 115-124, 2005. (Pubitemid 41540136)
123. Yan H, Parsons DW, Jin G, McLendon R, Rasheed BA, Yuan W, Kos I, Batinic-Haberle I, Jones S, Riggins GJ, Friedman H, Friedman A, Reardon D, Herndon J, Kinzler KW, Velculescu VE, Vogelstein B, and Bigner DD. IDH1 and IDH2 mutations in gliomas. N Engl J Med 360: 765-773, 2009.
124. Yang ZF, Ho DW, Ng MN, Lau CK, Yu WC, Ngai P, Chu PW, Lam CT, Poon RT, and Fan ST. Significance of CD90 + cancer stem cells in human liver cancer. Cancer Cell 13: 153-166, 2008. (Pubitemid 351163165)
125. Ye XQ, Li Q, Wang GH, Sun FF, Huang GJ, Bian XW, Yu SC, and Qian GS. Mitochondrial and energy metabolismrelated properties as novel indicators of lung cancer stem cells. Int J Cancer 129: 820-831, 2011.
126. Yeung SJ, Pan J, and Lee MH. Roles of p53, MYC and HIF-1 in regulating glycolysis-the seventh hallmark of cancer. Cell Mol Life Sci 65: 3981-3999, 2008.
127. Yeung TM, Gandhi SC, Wilding JL, Muschel R, and Bodmer WF. Cancer stem cells from colorectal cancer-derived cell lines. Proc Natl Acad Sci USA 107: 3722-3727, 2010.
128. Yilmaz OH, Valdez R, Theisen BK, Guo W, Ferguson DO, Wu H, and Morrison SJ. Pten dependence distinguishes haematopoietic stem cells from leukaemia-initiating cells. Nature 441: 475-482, 2006. (Pubitemid 44050144)
129. Yin T and Li L. The stem cell niches in bone. J Clin Invest 116: 1195-1201, 2006.
130. Yoshihara H, Arai F, Hosokawa K, Hagiwara T, Takubo K, Nakamura Y, Gomei Y, Iwasaki H, Matsuoka S, Miyamoto K, Miyazaki H, Takahashi T, and Suda T. Thrombopoietin/MPL signaling regulates hematopoietic stem cell quiescence and interaction with the osteoblastic niche. Cell Stem Cell 1: 685-697, 2007. (Pubitemid 350215333)
131. Zhang J, Niu C, Ye L, Huang H, He X, Tong WG, Ross J, Haug J, Johnson T, Feng JQ, Harris S, Wiedemann LM, Mishina Y, and Li L. Identification of the haematopoietic stem cell niche and control of the niche size. Nature 425: 836-841, 2003. (Pubitemid 37351467)
132. Zhang S, Balch C, Chan MW, Lai HC, Matei D, Schilder JM, Yan PS, Huang TH, and Nephew KP. Identification and characterization of ovarian cancer-initiating cells from primary human tumors. Cancer Res 68: 4311-4320, 2008.
133. Zhao S, Lin Y, Xu W, Jiang W, Zha Z, Wang P, Yu W, Li Z, Gong L, Peng Y, Ding J, Lei Q, Guan KL, and Xiong Y. Glioma-derived mutations in IDH1 dominantly inhibit IDH1 catalytic activity and induce HIF-1alpha. Science 324: 261-265, 2009.
134. Zhou Y, Hileman EO, Plunkett W, Keating MJ, and Huang P. Free radical stress in chronic lymphocytic leukemia cells and its role in cellular sensitivity to ROS-generating anticancer agents. Blood 101: 4098-4104, 2003. (Pubitemid 36857891)