Reactive oxygen species in BCR-ABL1-expressing cells - relevance to chronic myeloid leukemia

• Authors: Joanna Antoszewska-Smith , Elzbieta Pawlowska , Janusz Blasiak
• Languages of publication: EN

Abstracts

EN

Chronic myeloid leukemia (CML) results from the t(9;22) reciprocal chromosomal translocation producing the BCR-ABL1 gene, conferring growth and proliferation advantages in the CML cells. CML progresses from chronic, often syndrome-free, to blast phase, fatal if not treated. Although the involvement of BCR-ABL1 in some signaling pathways is considered as the cause of CML, the mechanisms resulting in its progression are not completely known. However, BCR-ABL1 stimulates the production of reactive oxygen species (ROS), which levels increase with CML progression and induce BCR-ABL1 self-mutagenesis. Introducing imatinib and other tyrosine kinase inhibitors (TKIs) to CML therapy radically improved its outcome, but TKIs-resistance became an emerging problem. TKI resistance can be associated with even higher ROS production than in TKI-sensitive cells. Therefore, ROS-induced self-mutagenesis of BCR-ABL1 can be crucial for CML progression and TKI resistance and in this way should be taken into account in therapeutic strategies. As a continuous production of ROS by BCR-ABL1 would lead to its self-destruction and death of CML cells, there must be mechanisms controlling this phenomenon. These can be dependent on DNA repair, which is modulated by BCR-ABL1 and can be different in CML stem and progenitor cells. Altogether, the mechanisms of the involvement of BCR-ABL1 in ROS signaling can be engaged in CML progression and TKI-resistance and warrant further study.

Keywords

EN

chronic myeloid leukemia; reactive oxygen species; DNA damage; DNA repair; cancer stem cells; imatinib resistance

• Publisher: Polish Biochemical Society
• Journal: Acta Biochimica Polonica
• Year: 2017
• Volume: 64
• Issue: 1
• Pages: 1-10

Dates

published

2017

received

2016-07-18

revised

2016-09-20

accepted

2016-10-26

(unknown)

2016-12-01

Contributors

author

Joanna Antoszewska-Smith

• Department of Maxillofacial Orthopedics and Orthodontics, Medical University of Wroclaw, Wrocław, Poland

author

Elzbieta Pawlowska

• Department of Orthodontics, Medical University of Lodz, Łódź, Poland

author

Janusz Blasiak

• Department of Molecular Genetics, University of Lodz, Łódź, Poland

References

• Abraham SA, Hopcroft LE, Carrick E, Drotar ME, Dunn K, Williamson AJ, Korfi K, Baquero P, Park LE, Scott MT, Pellicano F, Pierce A, Copland M, Nourse C, Grimmond SM, Vetrie D, Whetton AD, Holyoake TL (2016) Dual targeting of p53 and c-MYC selectively eliminates leukaemic stem cells. Nature 534: 341-346. doi: 10.1038/nature18288.
• Alam MS, Gaida MM, Ogawa Y, Kolios AG, Lasitschka F, Ashwell JD (2014) Counter-regulation of T cell effector function by differentially activated p38. J Exp Med 211: 1257-1270. doi: 10.1084/jem.20131917.
• Aspland SE, Bendall HH, Murre C (2001) The role of E2A-PBX1 in leukemogenesis. Oncogene 20: 5708-5717.
• Bellacosa A, Drohat AC (2015) Role of base excision repair in maintaining the genetic and epigenetic integrity of CpG sites. DNA Repair 32: 33-42. doi: 10.1016/j.dnarep.2015.04.011.
• Becker MW, Jordan CT (2011) Leukemia stemness signatures step toward the clinic. Cell Stem Cell 9: 185-186. doi: 10.1016/j.stem.2011.08.006.
• Blanpain C, Mohrin M, Sotiropoulou PA, Passegue E (2011) DNA-damage response in tissue-specific and cancer stem cells. Cell Stem Cell 8: 16-29. doi: 10.1016/j.stem.2010.12.012.
• Blasiak J, Hoser G, Bialkowska-Warzecha J, Pawlowska E, Skorski T (2016) Mitochondrial mutagenesis in BCR-ABL1-expressing cells sensitive and resistant to imatinib. Acta Biochim Pol 63: 365-370. doi: 10.18388/abp.2015_1189.
• Bolton-Gillespie E, Schemionek M, Klein HU, Flis S, Hoser G, Lange T, Nieborowska-Skorska M, Maier J, Kerstiens L, Koptyra M, Muller MC, Modi H, Stoklosa T, Seferynska I, Bhatia R, Holyoake TL, Koschmieder S, Skorski T (2013) Genomic instability may originate from imatinib-refractory chronic myeloid leukemia cells. Blood 121: 4175-4183. doi: 10.1182/blood-2012-11-466938.
• Bondar T, Medzhitov R (2010) p53-mediated hematopoietic stem and progenitor cell competition. Cell Stem Cell 6: 309-322. doi: 10.1016/j.stem.2010.03.002.
• Bourgeais J, Gouilleux-Gruart V, Gouilleux F (2013) Oxidative metabolism in cancer. A STAT affair? JAKSTAT 2: e25764. doi: 10.4161/jkst.25764.
• Brady N, Gaymes TJ, Cheung M, Mufti GJ, Rassool FV (2003) Increased error-prone NHEJ activity in myeloid leukemias is associated with DNA damage at sites that recruit key nonhomologous end-joining proteins. Cancer Res 63: 1798-1805.
• Brain JM, Saksena A, Laneuville P (2001) The kinase inhibitor STI571 reverses the Bcr/Abl induced point mutation frequencies observed in pre-leukemic P190Bcr/Abl transgenic mice. Leukemia Res 26: 1011-1016
• Burke BA, Carroll M (2010) BCR-ABL: a multi-faceted promoter of DNA mutation in chronic myelogeneous leukemia. Leukemia 24: 1105-1112. doi: 10.1038/leu.2010.67.
• Canitrot Y, Lautier D, Laurent G, Fréchet M, Ahmed A, Turhan AG, Salles B, Cazaux C, Hoffmann JS (1999) Mutator phenotype of BCR-ABL transfected Ba/F3 cell lines and its association with enhanced expression of DNA polymerase beta. Oncogene 18: 2676-2680.
• Cooke MS, Evans MD, Dizdaroglu M, Lunec J (2003) Oxidative DNA damage: mechanisms, mutation, and disease. FASEB J 17: 1195-1214.
• Dumont E, Grüber R, Bignon E, Morell C, Aranda J, Ravanat JL, Tuñón I (2016) Singlet oxygen attack on guanine: reactivity and structural signature within the B-DNA helix. Chemistry 22: 12358-12362. doi: 10.1002/chem.201601287.
• Dasmahapatra G, Patel H, Nguyen T, Attkisson E, Grant S (2013) PLK1 inhibitors synergistically potentiate HDAC inhibitor lethality in imatinib mesylate-sensitive or -resistant BCR/ABL+leukemia cells in vitro and in vivo. Clin Cancer Res 19: 404-414. doi: 10.1158/1078-0432.CCR-12-2799.
• Deininger MW, Goldman JM, Melo JV (2000) The molecular biology of chronic myeloid leukemia. Blood 96: 3343-3356.
• Druker BJ (2008) Translation of the Philadelphia chromosome into therapy for CML. Blood 112: 4808-4817. doi: 10.1182/blood-2008-07-077958.
• Du J, Yang YC (2013) Cited2 in hematopoietic stem cell function. Curr Opin Hematol 20: 301-307. doi: 10.1097/MOH.0b013e3283606022.
• Eppert K1, Takenaka K, Lechman ER, Waldron L, Nilsson B, van Galen P, Metzeler KH, Poeppl A, Ling V, Beyene J, Canty AJ, Danska JS, Bohlander SK, Buske C, Minden MD, Golub TR, Jurisica I, Ebert BL, Dick JE (2011) Stem cell gene expression programs influence clinical outcome in human leukemia. Nat Med 17: 1086-1093. doi: 10.1038/nm.2415.
• Hanawalt PC (2001) Revisiting the rodent repairadox. Environ Mol Mutagen 38: 89-96.
• Harrison JS, Rameshwar P, Chang V, Bandari P (2002) Oxygen saturation in the bone marrow of healthy volunteers. Blood 99: 394.
• He Q, Swindle CS, Wan C, Flynn RJ, Oster RA, Chen D, Zhang F, Shu Y, Klug CA (2016) Enhanced hematopoietic stem cell self-renewal-promoting ability of clonal primary MSC versus their osteogenic progeny. Stem Cells Aug 2016. doi: 10.1002/stem.2481.
• Ilaria RL (2002) Bcr/Abl, leukemogenesis, and genomic instability: a complex partnership. Leuk Res 26: 971-973.
• Ito K, Hirao A, Arai F, Takubo T, Matsuoka S, Miyamoto K, Ohmura M, Naka K, Hosokawa Y, Ikeda M, Suda T (2006) Reactive oxygen species act through p38 MAPK to limit the lifespan of hematopoietic stem cells. Nat Med 12: 446-451.
• Iwama A, Oguro H, Negishi M, Kato W, Morita Y, Tsukui H, Ema H, Kamijo T, Katoh-Fukui Y, Koseki H, van Lohuizen M, Nakauchi H (2004) Enhanced self-renewal of hematopoietic stem cells mediated by the polycomb gene product Bmi-1. Immunity 21: 843-851.
• Jang YY, Sharkis SJ (2007) 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.
• Kawagoe H, Humphries RK, Blair A, Sutherland HJ, Hogge DE (1999) Expression of HOX genes, HOX cofactors, and MLL in phenotypically and functionally defined subpopulations of leukemic and normal human hematopoietic cells. Leukemia 13: 687-698.
• Kiel MJ, Morrison SJ (2008) Uncertainty in the niches that maintain haematopoietic stem cells. Nat Rev Immunol 8: 290-301. doi: 10.1038/nri2279.
• Kiel MJ, Yilmaz OH, Iwashita T, Terhorst C, Morrison SJ (2005) SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 121: 1109-1121.
• Kim JH, Chu SC, Gramlich JL, Pride YB, Babendreier E, Chauhan D, Salgia R, Podar K, Griffin JD, Sattler M (2005) Activation of the PI3K/mTOR pathway by BCR-ABL contributes to increased production of reactive oxygen species. Blood 105: 1717-1723.
• Kim YJ, Wilson DM (2012) Overview of base excision repair biochemistry. Curr Mol Pharmacol 5: 3-13.
• Kocabas F, Xie L, Xie J, Yu Z, DeBerardinis RJ, Kimura W, Thet S, Elshamy AF, Abouellail H, Muralidhar S, Liu X, Chen C, Sadek HA, Zhang CC, Zheng J (2015) Hypoxic metabolism in human hematopoietic stem cells. Cell Biosci 5: 39. doi: 10.1186/s13578-015-0020-3.
• Koptyra M, Falinski R, Nowicki MO, Stoklosa T, Majsterek I, Nieborowska-Skorska M, Blasiak J, Skorski T (2006) BCR/ABL kinase induces self-mutagenesis via reactive oxygen species to encode imatinib resistance. Blood 108: 319-327.
• Leber B (2011) CML biology for the clinican in 2011: six impossible things to believe before breakfast on the way to cure. Curr Oncol 18: e185-e190.
• Lessard J, Sauvageau G (2003) Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature 423: 255-260.
• Li J, Sipple J, Maynard S, Mehta PA, Rose SR, Davies SM, Pang Q (2012) Fanconi anemia links reactive oxygen species to insulin resistance and obesity. Antioxid Redox Signal 17: 1083-1098. doi: 10.1089/ars.2011.4417.
• Liu L, Chen R, Huang S, Wu Y, Li G, Liu Q, Yin D, Liang Y (2011) Knockdown of SOD1 sensitizes the CD34+CML cells to imatinib therapy. Med Oncol 28: 835-839. doi: 10.1007/s12032-010-9529-9.
• Livneh Z, Cohen IS, Paz-Elizur T, Davidovsky D, Carmi D, Swain U, Mirlas-Neisberg N (2016) How do DNA polymerases switch during translesion DNA synthesis? DNA Repair 44: 59-67
• Ma Y, Wang H (2012) PI3K/Akt/FoxO: a novel participant in signal transduction in bone cells under mechanical stimulation. Cell Biol Int 36: 923-926. doi: 10.1042/CBI20120078.
• Matt S, Hofmann TG (2016) The DNA damage-induced cell death response: a roadmap to kill cancer cells. Cell Mol Life Sci 73: 2829-2850.
• Maryanovich M, Oberkovitz G, Niv H, Vorobiyov L, Zaltsman Y, Brenner O, Lapidot T, Jung S, Gross A (2012) The ATM-BID pathway regulates quiescence and survival of haematopoietic stem cells. Nat Cell Biol 14: 535-541.
• Miharada K, Karlsson G, Rehn M, Rörby E, Siva K, Cammenga J, Karlsson S (2012) Hematopoietic stem cells are regulated by Cripto, as an intermediary of HIF-1 in the hypoxic bone marrow niche. Ann N Y Acad Sci 1266: 55-62. doi: 10.1111/j.1749-6632.2012.06564.x.
• Milyavsky M, Gan OI, Trottier M, Komosa M, Tabach O, Notta F, Lechman E, Hermans KG, Eppert K, Konovalova Z, Ornatsky O, Domany E, Meyn MS, Dick JE (2010) A distinctive DNA damage response in human hematopoietic stem cells reveals an apoptosis-independent role for p53 in self-renewal. Cell Stem Cell 7: 186-197. doi: 10.1016/j.stem.2010.05.016.
• 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, Hirao A (2007) Foxo3a is essential for maintenance of the hematopoietic stem cell pool. Cell Stem Cell 1: 101-112. doi: 10.1016/j.stem.2007.02.001.
• Mohrin M, Bourke E, Alexander D, Warr MR, Barry-Holson K, Le Beau MM, Morrison CG, Passegué E (2010) Hematopoietic stem cell quiescence promotes error-prone DNA repair and mutagenesis. Cell Stem Cell 7: 174-185. doi: 10.1016/j.stem.2010.06.014.
• Muvarak N, Kelley S, Robert C, Baer MR, Perrotti D, Gambacorti-Passerini C, Civin C, Scheibner K, Rassool FV (2015) c-myc generates repair errors via increased transcription of alternative-NHEJ factors, Lig3 and PARP1, in tyrosine kinase-activated leukemias. Mol Cancer Res 13: 699-712. doi: 10.1158/1541-7786.MCR-14-0422.
• Naka K, Muraguchi T, Hoshii T, Hirao A (2008) Regulation of reactive oxygen species and genomic stability in hematopoietic stem cells. Antioxid Redox Signal 10: 1883-1894. doi: 10.1089/ars.2008.2114.
• Nakamura T, Yamazaki Y, Hatano Y, Miura I (1999) NUP98 is fused to PMX1 homeobox gene in human acute myelogenous leukemia with chromosome translocation t(1;11)(q23;p15). Blood 94: 741-747.
• Nemmar A, Beegam S, Yuvaraju P, Yasin J, Tariq S, Attoub S, Ali BH (2016) Ultrasmall superparamagnetic iron oxide nanoparticles acutely promote thrombosis and cardiac oxidative stress and DNA damage in mice. Part Fibre Toxicol 13: 22. doi: 10.1186/s12989-016-0132-x.
• Nguyen T, Dai Y, Attkisson E, Kramer L, Jordan N, Nguyen N, Kolluri N, Muschen M, Grant S (2011) HDAC inhibitors potentiate the activity of the BCR/ABL kinase inhibitor KW-2449 in imatinib-sensitive or -resistant BCR/ABL+leukemia cells in vitro and in vivo. Clin Cancer Res 17: 3219-3232. doi: 10.1158/1078-0432.CCR-11-0234.
• Nieborowska-Skorska M, Flis S, Skorski T (2014) AKT-induced reactive oxygen species generate imatinib-resistant clones emerging from chronic myeloid leukemia progenitor cells. Leukemia 28: 2416-2418. doi: 10.1038/leu.2014.249.
• Nieborowska-Skorska M, Hoser G, Hochhaus A, Stoklosa T, Skorski T (2013) Anti-oxidant vitamin E prevents accumulation of imatinib-resistant BCR-ABL1 kinase mutations in CML-CP xenografts in NSG mice. Leukemia 27: 2253-2254. doi: 10.1038/leu.2013.123.
• Nieborowska-Skorska M, Kopinski PK, Ray R, Hoser G, Ngaba D, Flis S, Cramer K, Reddy MM, Koptyra M, Penserga T, Glodkowska-Mrowka E, Bolton E, Holyoake TL, Eaves CJ, Cerny-Reiterer S, Valent P, Hochhaus A, Hughes TP, van der Kuip H, Sattler M, Wiktor-Jedrzejczak W, Richardson C, Dorrance A, Stoklosa T, Williams DA, Skorski T (2012) Rac2-MRC-cIII-generated ROS cause genomic instability in chronic myeloid leukemia stem cells and primitive progenitors. Blood 119: 4253-4263. doi: 10.1182/blood-2011-10-385658.
• Nieborowska-Skorska M, Stoklosa T, Datta M, Czechowska A, Rink L, Słupianek A, Koptyra M, Seferynska I, Krszyna K, Blasiak J, Skorski T (2006) ATR-Chk1 axis protects BCR/ABL leukemia cells from the lethal effect of DNA double-strand breaks. Cell Cycle 5: 994-1000.
• Nijnik A, Woodbine L, Marchetti C, Dawson S, Lambe T, Liu C, Rodrigues NP, Crockford TL, Cabuy E, Vindigni A, Enver T, Bell JI, Slijepcevic P, Goodnow CC, Jeggo PA, Cornall RJ (2007) DNA repair is limiting for haematopoietic stem cells during ageing. Nature 447: 686-690.
• Park IK, Qian D, Kiel M, Becker MW, Pihalja M, Weissman IL, Morrison SJ, Clarke MF (2003) Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature 423: 302-305.
• Pawlowska E, Blasiak J (2015) DNA repair - a double-edged sword in the genomic stability of cancer cells – the case of chronic myeloid leukemia. Int J Mol Sci 16: 27535–27549. doi: 10.3390/ijms161126049.
• Perrotti D, Jamieson C, Goldman J, Skorski T (2010) Chronic myeloid leukemia: mechanism of blastic transformation. J Clin Invest 120: 2254-2264. doi: 10.1172/JCI41246.
• Prost S, Relouzat F, Spentchian M, Ouzegdouh Y, Saliba J, Massonnet G, Beressi JP, Verhoeyen E, Raggueneau V, Maneglier B, Castaigne S, Chomienne C, Chrétien S, Rousselot P, Leboulch P (2015) Erosion of the chronic myeloid leukaemia stem cell pool by PPARγ agonists. Nature 525: 380-383. doi: 10.1038/nature15248.
• Quintas-Cardama A, Cortes J (2009) Molecular biology of bcr-abl1-positive chronic myeloid leukemia. Blood 113: 1619-1630.
• Rakshit S, Bagchi J, Mandal L, Paul K, Ganguly D, Bhattacharjee S, Ghosh M, Biswas N, Chaudhuri U, Bandyopadhyay S (2009) N-acetyl cysteine enhances imatinib-induced apoptosis of Bcr-Abl+cells by endothelial nitric oxide synthase-mediated production of nitric oxide. Apoptosis 14: 298-308. doi: 10.1007/s10495-008-0305-7.
• Ray PD, Huang BW, Tsuji Y (2012) Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal 24: 981-990. doi: 10.1016/j.cellsig.2012.01.008.
• Rossi DJ, Bryder D, Seita J, Nussenzweig A, Hoeijmakers J, Weissman IL (2007) Deficiencies in DNA damage repair limit the function of haematopoietic stem cells with age. Nature 447: 725-729.
• Rossi DJ, Jamieson CH, Weissman IL (2008) Stems cells and the pathways to aging and cancer. Cell 132: 681-696. doi: 10.1016/j.cell.2008.01.036.
• Ryu JM, Lee HJ, Jung YH, Lee KH, Kim DI, Kim JY, Ko SH, Choi GE, Chai II, Song EJ, Oh JY, Lee SJ, Han HJ (2015) Regulation of stem cell fate by ROS-mediated alteration of metabolism. Int J Stem Cells 8: 24-35. doi: 10.15283/ijsc.2015.8.1.24.
• Sattler M, Verma S, Shrikhande G, Byrne CH, Pride YB, Winkler T, Greenfield EA, Salgia R, Griffin JD (2000) The BCR/ABL tyrosine kinase induces production of reactive oxygen species in hematopoietic cells. J Biol Chem 275: 24273-24278.
• Schultz MB, Sinclair DA (2016) When stem cells grow old: phenotypes and mechanisms of stem cell aging. Development 143: 3-14. doi: 10.1242/dev.130633.
• Semenza GL (2009) Regulation of cancer cell metabolism by hypoxia-inducible factor 1. Semin Cancer Biol 19: 12-16. doi: 10.1016/j.semcancer.2008.11.009.
• Shi X, Zhang Y, Zheng J, Pan J (2012) Reactive oxygen species in cancer stem cells. Antioxid Redox Signal 16: 1215-1228. doi: 10.1089/ars.2012.4529.
• Shima H, Takubo K, Tago N, Iwasaki H, Arai F, Takahashi T, Suda T (2010) Acquisition of G₀ state by CD34-positive cord blood cells after bone marrow transplantation. Exp Hematol 38: 1231-1240. doi: 10.1016/j.exphem.2010.08.004.
• Shimura T, Noma N, Oikawa T, Ochia Y, Kakuda S, Kuwahara Y, Takai Y, Takahashi A, Fukumoto M (2012) Activation of the AKT/cyclin D1/Cdk4 survival signaling pathway in radioresistant cancer stem cells. Oncogenesis 1: e12. doi: 10.1038/oncsis.2012.12.
• Simsek T, Kocabas F, Zheng J, Deberardinis RJ, Mahmoud AI, Olson EN, Schneider JW, Zhang CC, Sadek HA (2010) The distinct metabolic profile of hematopoietic stem cells reflects their location in a hypoxic niche. Cell Stem Cell 7: 380-390. doi: 10.1016/j.stem.2010.07.011.
• Slupianek A, Falinski R, Znojek P, Stoklosa T, Flis S, Doneddu V, Pytel D, Synowiec E, Blasiak J, Bellacosa A, Skorski T (2013) BCR-ABL1 kinase inhibits uracil DNA glycosylase UNG2 to enhance oxidative DNA damage and stimulate genomic instability. Leukemia 27: 629-634. doi: 10.1038/leu.2012.294.
• Somsedikova A, Markova E, Kolenova A, Puskacova J, Kubes M, Belyaev I (2014) Constitutive 53BP1/γH2AX foci are increased in cells of ALL patients dependent on BCR-ABL and TEL-AML1 preleukemic gene fusions. Neoplasma 61: 617-625.
• Suda T, Takubo K, Semenza GL (2011) Metabolic regulation of hematopoietic stem cells in the hypoxic niche. Cell Stem Cell 9: 298-310. doi: 10.1016/j.stem.2011.09.010.
• Synowiec E, Hoser G, Bialkowska-Warzecha J, Pawlowska E, Skorski T, Blasiak J (2015) Doxorubicin differentially induces apoptosis, expression of mitochondrial apoptosis-related genes, and mitochondrial potential in BCR-ABL1-expressing cells sensitive and resistant to imatinib. Biomed Res Int 2015: 673512. doi: 10.1155/2015/673512.
• Takagi M, Sato M, Piao J, Miyamoto S, Isoda T, Kitagawa M, Honda H, Mizutani S (2013) ATM-dependent DNA damage-response pathway as a determinant in chronic myelogenous leukemia. DNA Repair 12: 500-507. doi: 10.1016/j.dnarep.2013.04.022.
• Testa U, Labbaye C, Castelli G, Pelosi E (2016) Oxidative stress and hypoxia in normal and leukemic stem cells. Exp Hematol 44: 540-560. doi: 10.1016/j.exphem.2016.04.012.
• Tothova Z, Kollipara R, Huntly BJ, Lee BH, Castrillon DH, Cullen DE, McDowell EP, Lazo-Kallanian S, Williams IR, Sears C, Armstrong SA, Passegue ER, DePinho A, Gilliland DJ (2007) FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell 128: 325-339.
• Truong T, Sun G, Doorly M, Wang JY, Schwartz MA (2003) Modulation of DNA damage-induced apoptosis by cell adhesion is independently mediated by p53 and c-Abl. Proc Natl Acad Sci U S A 100: 10281-10286.
• Wanet A, Arnould T, Najimi M, Renard P (2015) Connecting mitochondria, metabolism, and stem cell fate. Stem Cells Dev 24: 1957-1971. doi: 10.1089/scd.2015.0117.
• Wang Z, Liu Z, Wu X, Chu S, Wang J, Yuan H, Roth M, Yuan YC, Bhatia R, Chen W (2014) ATRA-induced cellular differentiation and CD38 expression inhibits acquisition of BCR-ABL mutations for CML acquired resistance. PLoS Genet 10: e1004414. doi: 10.1371/journal.pgen.1004414.
• Wierenga AT, Vellenga E, Schuringa JJ (2014) Convergence of hypoxia and TGFβ pathways on cell cycle regulation in human hematopoietic stem/progenitor cells. PLoS One 9: e93494. doi: 10.1371/journal.pone.0093494. eCollection 2014.
• Wu L, Chen X, Huang L, Tian J, Ke F, Xu J, Chen Y, Zheng M (2015) A novobiocin derivative, XN4, inhibits the proliferation of chronic myeloid leukemia cells by inducing oxidative DNA damage. PLoS One 10: e0123314. doi: 10.1371/journal.pone.0123314.
• Yamazaki S, Iwama A, Takayanagi S, Morita Y, Eto K, Ema H, Nakauchi H (2006) Cytokine signals modulated via lipid rafts mimic niche signals and induce hibernation in hematopoietic stem cells. EMBO J 25: 3515-3523.
• Yuan TL, Cantley LC (2008) PI3K pathway alterations in cancer: vari-ations on a theme. Oncogene 27: 5497-5510. doi: 10.1038/onc.2008.245.
• Zhang CC, Sadek HA (2014) Hypoxia and metabolic properties of hematopoietic stem cells. Antioxid Redox Signal 20: 1891-1901. doi: 10.1089/ars.2012.5019.
• Zhang J, Dai Q, Park D, Deng X (2016) Targeting DNA replication stress for cancer therapy. Genes 7: E51. doi: 10.3390/genes7080051.
• Zhang X, Sejas DP, Qiu Y, Williams DA, Pang Q (2007) Inflammatory ROS promote and cooperate with the Fanconi anemia mutation for hematopoietic senescence. J Cell Sci 120: 1572-1583.
• Zhou BB, Elledge SJ (2000) The DNA damage response: putting checkpoints in perspective. Nature 408: 433-439. doi: 10.1038/35044005.
• Zhou H, Xu R (2015) Leukemia stem cells: the root of chronic myeloid leukemia. Protein Cell 6: 403-412. doi: 10.1007/s13238-015-0143-7.
• Zhu Q, Xia SL, Mills GB, Lowell CA, Touw IP, Corey SJ (2006) G-CSF induced reactive oxygen species involves Lyn-PI3-kinase-Akt and contributes to myeloid cell growth. Blood 107: 1847-1856.

Identifiers

DOI

10.18388/abp.2016_1396