Generic placeholder image

Anti-Cancer Agents in Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 1871-5206
ISSN (Online): 1875-5992

Mini-Review Article

The Emerging Roles of Aldehyde Dehydrogenase in Acute Myeloid Leukemia and Its Therapeutic Potential

Author(s): Atefe Rahmati, Sajad Goudarzi, Maryam Sheikhi, Payam Siyadat, Gordon A Ferns and Hossein Ayatollahi*

Volume 23, Issue 3, 2023

Published on: 20 August, 2022

Page: [246 - 255] Pages: 10

DOI: 10.2174/1871520622666220610154043

Price: $65

Abstract

Acute myeloid leukemia (AML) is a malignant disorder characterized by myeloid differentiation arrest and uncontrolled clonal expansion of abnormal myeloid progenitor cells. AML is the most common malignant bone marrow (BM) disease in adults and accounts for approximately 80% of adult leukemia cases. There has been little improvement in the treatment of patients with AML over the past decade. Cytogenetic and morphologic heterogeneity of AML and the difficulty in distinguishing leukemic stem cells (LSCs) from normal hematopoietic stem cells (HSCs) continue to be the major challenges in treating this malignancy. In recent years, intensive efforts have been made to explore novel potential markers for the efficient identification and characterization of leukemic stem cells. Aldehyde dehydrogenase (ALDH) is a potential target molecule that plays crucial roles in leukemic stem cell survival and multidrug resistance, mainly through its involvement in the detoxification of many endogenous and exogenous aldehydes. The selection and isolation of cancer stem cells based on high ALDH activity seem to be a useful approach in many human malignancies, especially leukemia. Moreover, it is worth mentioning that several previous studies have indicated that a high ALDH activity (classified as ALDHbr cells in flow cytometry) can act as an independent prognostic factor in several types of cancer. In the present review, we update and critically discuss the available data regarding the importance of ALDH activity in normal and leukemic stem cells and its potential diagnostic and therapeutic implications.

Keywords: Aldehyde dehydrogenase, acute myeloid leukemia, hematopoietic stem cell, leukemic stem cell, targeted therapy, therapeutic potential.

Graphical Abstract

[1]
Jemal, A.; Siegel, R.; Xu, J.; Ward, E. Cancer statistics, 2010. CA Cancer J. Clin., 2010, 60(5), 277-300.
[http://dx.doi.org/10.3322/caac.20073] [PMID: 20610543]
[2]
Jemal, A.; Clegg, L.X.; Ward, E.; Ries, L.A.G.; Wu, X.; Jamison, P.M.; Wingo, P.A.; Howe, H.L.; Anderson, R.N.; Edwards, B.K. Annual report to the nation on the status of cancer, 1975-2001, with a special feature regarding survival. Cancer, 2004, 101(1), 3-27.
[http://dx.doi.org/10.1002/cncr.20288] [PMID: 15221985]
[3]
Döhner, H.; Estey, E.H.; Amadori, S.; Appelbaum, F.R.; Büchner, T.; Burnett, A.K.; Dombret, H.; Fenaux, P.; Grimwade, D.; Larson, R.A.; Lo-Coco, F.; Naoe, T.; Niederwieser, D.; Ossenkoppele, G.J.; Sanz, M.A.; Sierra, J.; Tallman, M.S.; Löwenberg, B.; Bloomfield, C.D. Diagnosis and management of acute myeloid leukemia in adults: Recommendations from an international expert panel, on behalf of the European LeukemiaNet. Blood, 2010, 115(3), 453-474.
[http://dx.doi.org/10.1182/blood-2009-07-235358] [PMID: 19880497]
[4]
Cheson, B.D.; Bennett, J.M.; Kopecky, K.J.; Büchner, T.; Willman, C.L.; Estey, E.H.; Schiffer, C.A.; Doehner, H.; Tallman, M.S.; Lister, T.A.; Lo-Coco, F.; Willemze, R.; Biondi, A.; Hiddemann, W.; Larson, R.A.; Löwenberg, B.; Sanz, M.A.; Head, D.R.; Ohno, R.; Bloomfield, C.D. Revised recommendations of the international working group for diagnosis, standardization of response criteria, treatment outcomes, and reporting standards for therapeutic trials in acute myeloid leukemia. J. Clin. Oncol., 2003, 21(24), 4642-4649.
[http://dx.doi.org/10.1200/JCO.2003.04.036] [PMID: 14673054]
[5]
Ding, L.; Ley, T.J.; Larson, D.E.; Miller, C.A.; Koboldt, D.C.; Welch, J.S.; Ritchey, J.K.; Young, M.A.; Lamprecht, T.; McLellan, M.D.; McMichael, J.F.; Wallis, J.W.; Lu, C.; Shen, D.; Harris, C.C.; Dooling, D.J.; Fulton, R.S.; Fulton, L.L.; Chen, K.; Schmidt, H.; Kalicki-Veizer, J.; Magrini, V.J.; Cook, L.; McGrath, S.D.; Vickery, T.L.; Wendl, M.C.; Heath, S.; Watson, M.A.; Link, D.C.; Tomasson, M.H.; Shannon, W.D.; Payton, J.E.; Kulkarni, S.; Westervelt, P.; Walter, M.J.; Graubert, T.A.; Mardis, E.R.; Wilson, R.K.; DiPersio, J.F. Clonal evolution in relapsed acute myeloid leukaemia revealed by whole-genome sequencing. Nature, 2012, 481(7382), 506-510.
[http://dx.doi.org/10.1038/nature10738] [PMID: 22237025]
[6]
Yanada, M.; Mori, J.; Aoki, J.; Harada, K.; Mizuno, S.; Uchida, N.; Kurosawa, S.; Toya, T.; Kanamori, H.; Ozawa, Y.; Ogawa, H.; Henzan, H.; Iwato, K.; Sakura, T.; Ota, S.; Fukuda, T.; Ichinohe, T.; Atsuta, Y.; Yano, S. Effect of cytogenetic risk status on outcomes for patients with acute myeloid leukemia undergoing various types of allogeneic hematopoietic cell transplantation: an analysis of 7812 patients. Leuk. Lymphoma, 2018, 59(3), 601-609.
[http://dx.doi.org/10.1080/10428194.2017.1357173] [PMID: 28750566]
[7]
Hassan, C.; Afshinnekoo, E.; Li, S.; Wu, S.; Mason, C.E. Genetic and epigenetic heterogeneity and the impact on cancer relapse. Exp. Hematol., 2017, 54, 26-30.
[http://dx.doi.org/10.1016/j.exphem.2017.07.002] [PMID: 28705639]
[8]
Medeiros, B. C.; Othus, M.; Fang, M.; Appelbaum, F. R.; Erba, H.P. Cytogenetic heterogeneity negatively impacts outcomes in patients with acute myeloid leukemia. Haematologica, 2015, 100(3), 331-335.
[9]
Döhner, H.; Weisdorf, D.J.; Bloomfield, C.D. Acute myeloid leukemia. N. Engl. J. Med., 2015, 373(12), 1136-1152.
[http://dx.doi.org/10.1056/NEJMra1406184] [PMID: 26376137]
[10]
Maynadié, M.; De Angelis, R.; Marcos-Gragera, R.; Visser, O.; Allemani, C.; Tereanu, C.; Capocaccia, R.; Giacomin, A.; Lutz, J.-M.; Martos, C. Survival of European patients diagnosed with myeloid malignancies: A HAEMACARE study. Haematologica, 2013, 98(2), 230-238.
[11]
Löwenberg, B.; Downing, J.R.; Burnett, A. Acute myeloid leukemia. N. Engl. J. Med., 1999, 341(14), 1051-1062.
[http://dx.doi.org/10.1056/NEJM199909303411407] [PMID: 10502596]
[12]
Grimwade, D.; Walker, H.; Oliver, F.; Wheatley, K.; Harrison, C.; Harrison, G.; Rees, J.; Hann, I.; Stevens, R.; Burnett, A.; Goldstone, A. The importance of diagnostic cytogenetics on outcome in AML: Analysis of 1,612 patients entered into the MRC AML 10 trial. Blood, 1998, 92(7), 2322-2333.
[http://dx.doi.org/10.1182/blood.V92.7.2322] [PMID: 9746770]
[13]
Blume, R.; Rempel, E.; Manta, L.; Saeed, B.R.; Wang, W.; Raffel, S.; Ermakova, O.; Eckstein, V.; Benes, V.; Trumpp, A.; Ho, A.D.; Lutz, C. The molecular signature of AML with increased ALDH activity suggests a stem cell origin. Leuk. Lymphoma, 2018, 59(9), 2201-2210.
[http://dx.doi.org/10.1080/10428194.2017.1422862] [PMID: 29334844]
[14]
Sykes, S.M.; Kokkaliaris, K.D.; Milsom, M.D.; Levine, R.L.; Majeti, R. Clonal evolution of preleukemic hematopoietic stem cells in acute myeloid leukemia. Exp. Hematol., 2015, 43(12), 989-992.
[http://dx.doi.org/10.1016/j.exphem.2015.08.012] [PMID: 26455528]
[15]
Passegué, E.; Weisman, I.L. Leukemic stem cells: Where do they come from? Stem Cell Rev., 2005, 1(3), 181-188.
[http://dx.doi.org/10.1385/SCR:1:3:181] [PMID: 17142854]
[16]
Chopra, M.; Bohlander, S.K. The cell of origin and the leukemia stem cell in acute myeloid leukemia. Genes Chromosomes Cancer, 2019, 58(12), 850-858.
[http://dx.doi.org/10.1002/gcc.22805] [PMID: 31471945]
[17]
Hanekamp, D.; Cloos, J.; Schuurhuis, G.J. Leukemic stem cells: Identification and clinical application. Int. J. Hematol., 2017, 105(5), 549-557.
[http://dx.doi.org/10.1007/s12185-017-2221-5] [PMID: 28357569]
[18]
Hope, K.J.; Jin, L.; Dick, J.E. Acute myeloid leukemia originates from a hierarchy of leukemic stem cell classes that differ in self-renewal capacity. Nat. Immunol., 2004, 5(7), 738-743.
[http://dx.doi.org/10.1038/ni1080] [PMID: 15170211]
[19]
Misaghian, N.; Ligresti, G.; Steelman, L.S.; Bertrand, F.E.; Bäsecke, J.; Libra, M.; Nicoletti, F.; Stivala, F.; Milella, M.; Tafuri, A.; Cervello, M.; Martelli, A.M.; McCubrey, J.A. Targeting the leukemic stem cell: The Holy Grail of leukemia therapy. Leukemia, 2009, 23(1), 25-42.
[http://dx.doi.org/10.1038/leu.2008.246] [PMID: 18800146]
[20]
Al-Mawali, A.; Gillis, D.; Lewis, I. Immunoprofiling of leukemic stem cells CD34+/CD38−/CD123+ delineate FLT3/ITD-positive clones. J. Hematol. Oncol., 2016, 9(1), 61.
[http://dx.doi.org/10.1186/s13045-016-0292-z] [PMID: 27465508]
[21]
Iwasaki, M.; Liedtke, M.; Gentles, A.J.; Cleary, M.L. CD93 marks a non-quiescent human leukemia stem cell population and is required for development of MLL-rearranged acute myeloid leukemia. Cell Stem Cell, 2015, 17(4), 412-421.
[http://dx.doi.org/10.1016/j.stem.2015.08.008] [PMID: 26387756]
[22]
Kersten, B.; Valkering, M.; Wouters, R.; van Amerongen, R.; Hanekamp, D.; Kwidama, Z.; Valk, P.; Ossenkoppele, G.; Zeijlemaker, W.; Kaspers, G.; Cloos, J.; Schuurhuis, G.J. CD45RA, a specific marker for leukaemia stem cell sub-populations in acute myeloid leukaemia. Br. J. Haematol., 2016, 173(2), 219-235.
[http://dx.doi.org/10.1111/bjh.13941] [PMID: 26814163]
[23]
Quek, L.; Otto, G.W.; Garnett, C.; Lhermitte, L.; Karamitros, D.; Stoilova, B.; Lau, I.J.; Doondeea, J.; Usukhbayar, B.; Kennedy, A.; Metzner, M.; Goardon, N.; Ivey, A.; Allen, C.; Gale, R.; Davies, B.; Sternberg, A.; Killick, S.; Hunter, H.; Cahalin, P.; Price, A.; Carr, A.; Griffiths, M.; Virgo, P.; Mackinnon, S.; Grimwade, D.; Freeman, S.; Russell, N.; Craddock, C.; Mead, A.; Peniket, A.; Porcher, C.; Vyas, P. Genetically distinct leukemic stem cells in human CD34− acute myeloid leukemia are arrested at a hemopoietic precursor-like stage. J. Exp. Med., 2016, 213(8), 1513-1535.
[http://dx.doi.org/10.1084/jem.20151775] [PMID: 27377587]
[24]
Vasiliou, V.; Thompson, D.C.; Smith, C.; Fujita, M.; Chen, Y. Aldehyde dehydrogenases: From eye crystallins to metabolic disease and cancer stem cells. Chem. Biol. Interact., 2013, 202(1-3), 2-10.
[http://dx.doi.org/10.1016/j.cbi.2012.10.026] [PMID: 23159885]
[25]
Jackson, B.; Brocker, C.; Thompson, D.C.; Black, W.; Vasiliou, K.; Nebert, D.W.; Vasiliou, V. Update on the aldehyde dehydrogenase gene (ALDH) superfamily. Hum. Genomics, 2011, 5(4), 283-303.
[http://dx.doi.org/10.1186/1479-7364-5-4-283] [PMID: 21712190]
[26]
Januchowski, R.; Wojtowicz, K.; Zabel, M. The role of aldehyde dehydrogenase (ALDH) in cancer drug resistance. Biomed. Pharmacother., 2013, 67(7), 669-680.
[http://dx.doi.org/10.1016/j.biopha.2013.04.005] [PMID: 23721823]
[27]
Huang, C.P.; Tsai, M.F.; Chang, T.H.; Tang, W.C.; Chen, S.Y.; Lai, H.H.; Lin, T.Y.; Yang, J.C.H.; Yang, P.C.; Shih, J.Y.; Lin, S.B. ALDH-positive lung cancer stem cells confer resistance to epidermal growth factor receptor tyrosine kinase inhibitors. Cancer Lett., 2013, 328(1), 144-151.
[http://dx.doi.org/10.1016/j.canlet.2012.08.021] [PMID: 22935675]
[28]
Laskar, A.A.; Younus, H. Aldehyde toxicity and metabolism: The role of aldehyde dehydrogenases in detoxification, drug resistance and carcinogenesis. Drug Metab. Rev., 2019, 51(1), 42-64.
[http://dx.doi.org/10.1080/03602532.2018.1555587] [PMID: 30514131]
[29]
Yanagawa, Y.; Chen, J.C.; Hsu, L.C.; Yoshida, A. The transcriptional regulation of human aldehyde dehydrogenase I gene. The structural and functional analysis of the promoter. J. Biol. Chem., 1995, 270(29), 17521-17527.
[http://dx.doi.org/10.1074/jbc.270.29.17521] [PMID: 7615557]
[30]
Elizondo, G.; Corchero, J.; Sterneck, E.; Gonzalez, F.J. Feedback inhibition of the retinaldehyde dehydrogenase gene ALDH1 by retinoic acid through retinoic acid receptor α and CCAAT/enhancer-binding protein β. J. Biol. Chem., 2000, 275(50), 39747-39753.
[http://dx.doi.org/10.1074/jbc.M004987200] [PMID: 10995752]
[31]
Chute, J.P.; Muramoto, G.G.; Whitesides, J.; Colvin, M.; Safi, R.; Chao, N.J.; McDonnell, D.P. Inhibition of aldehyde dehydrogenase and retinoid signaling induces the expansion of human hematopoietic stem cells. Proc. Natl. Acad. Sci. USA, 2006, 103(31), 11707-11712.
[http://dx.doi.org/10.1073/pnas.0603806103] [PMID: 16857736]
[32]
Pearce, D.J.; Taussig, D.; Simpson, C.; Allen, K.; Rohatiner, A.Z.; Lister, T.A.; Bonnet, D. Characterization of cells with a high aldehyde dehydrogenase activity from cord blood and acute myeloid leukemia samples. Stem Cells, 2005, 23(6), 752-760.
[http://dx.doi.org/10.1634/stemcells.2004-0292] [PMID: 15917471]
[33]
Vassalli, G. Aldehyde dehydrogenases: Not just markers, but functional regulators of stem cells. Stem Cells Int., 2019, 2019, 1-15.
[http://dx.doi.org/10.1155/2019/3904645] [PMID: 30733805]
[34]
Yang, Y.; Zhou, W.; Xia, J.; Gu, Z.; Wendlandt, E.; Zhan, X.; Janz, S.; Tricot, G.; Zhan, F. NEK2 mediates ALDH1A1-dependent drug resistance in multiple myeloma. Oncotarget, 2014, 5(23), 11986-11997.
[http://dx.doi.org/10.18632/oncotarget.2388] [PMID: 25230277]
[35]
Ma, I.; Allan, A.L. The role of human aldehyde dehydrogenase in normal and cancer stem cells. Stem Cell Rev., 2011, 7(2), 292-306.
[http://dx.doi.org/10.1007/s12015-010-9208-4] [PMID: 21103958]
[36]
Vasiliou, V.; Pappa, A.; Petersen, D.R. Role of aldehyde dehydrogenases in endogenous and xenobiotic metabolism. Chem. Biol. Interact., 2000, 129(1-2), 1-19.
[http://dx.doi.org/10.1016/S0009-2797(00)00211-8] [PMID: 11154732]
[37]
Gasparetto, M.; Smith, C.A. ALDHs in normal and malignant hematopoietic cells: Potential new avenues for treatment of AML and other blood cancers. Chem. Biol. Interact., 2017, 276, 46-51.
[http://dx.doi.org/10.1016/j.cbi.2017.06.020] [PMID: 28645468]
[38]
Hira, A.; Yabe, H.; Yoshida, K.; Okuno, Y.; Shiraishi, Y.; Chiba, K.; Tanaka, H.; Miyano, S.; Nakamura, J.; Kojima, S.; Ogawa, S.; Matsuo, K.; Takata, M.; Yabe, M. Variant ALDH2 is associated with accelerated progression of bone marrow failure in Japanese Fanconi anemia patients. Blood, 2013, 122(18), 3206-3209.
[http://dx.doi.org/10.1182/blood-2013-06-507962] [PMID: 24037726]
[39]
Feron, V.J.; Til, H.P.; de Vrijer, F.; Woutersen, R.A.; Cassee, F.R.; van Bladeren, P.J. Aldehydes: occurrence, carcinogenic potential, mechanism of action and risk assessment. Mutat. Res. Genet. Toxicol. Test., 1991, 259(3-4), 363-385.
[http://dx.doi.org/10.1016/0165-1218(91)90128-9] [PMID: 2017217]
[40]
Mele, L.; Liccardo, D.; Tirino, V. Evaluation and isolation of cancer stem cells using ALDH activity assay. Eds. Methods in Molecular Biology Cancer Stem Cells Springer: NY, 2018; 1692, pp. 43-48.
[41]
Moreb, J.S.; Ucar, D.; Han, S.; Amory, J.K.; Goldstein, A.S.; Ostmark, B.; Chang, L.J. The enzymatic activity of human aldehyde dehydrogenases 1A2 and 2 (ALDH1A2 and ALDH2) is detected by Aldefluor, inhibited by diethylaminobenzaldehyde and has significant effects on cell proliferation and drug resistance. Chem. Biol. Interact., 2012, 195(1), 52-60.
[http://dx.doi.org/10.1016/j.cbi.2011.10.007] [PMID: 22079344]
[42]
Zhou, L.; Sheng, D.; Wang, D.; Ma, W.; Deng, Q.; Deng, L.; Liu, S. Identification of cancer-type specific expression patterns for active aldehyde dehydrogenase (ALDH) isoforms in ALDEFLUOR assay. Cell Biol. Toxicol., 2019, 35(2), 161-177.
[http://dx.doi.org/10.1007/s10565-018-9444-y] [PMID: 30220009]
[43]
Hoang, V.T.; Buss, E.C.; Wang, W.; Hoffmann, I.; Raffel, S.; Zepeda-Moreno, A.; Baran, N.; Wuchter, P.; Eckstein, V.; Trumpp, A.; Jauch, A.; Ho, A.D.; Lutz, C. The rarity of ALDH+ cells is the key to separation of normal versus leukemia stem cells by ALDH activity in AML patients. Int. J. Cancer, 2015, 137(3), 525-536.
[http://dx.doi.org/10.1002/ijc.29410] [PMID: 25545165]
[44]
Brooks, P.J.; Theruvathu, J.A. DNA adducts from acetaldehyde: implications for alcohol-related carcinogenesis. Alcohol, 2005, 35(3), 187-193.
[http://dx.doi.org/10.1016/j.alcohol.2005.03.009] [PMID: 16054980]
[45]
Rice, K.L.; Izon, D.J.; Ford, J.; Boodhoo, A.; Kees, U.R.; Greene, W.K. Overexpression of stem cell associated ALDH1A1, a target of the leukemogenic transcription factor TLX1/HOX11, inhibits lymphopoiesis and promotes myelopoiesis in murine hematopoietic progenitors. Leuk. Res., 2008, 32(6), 873-883.
[http://dx.doi.org/10.1016/j.leukres.2007.11.001] [PMID: 18082256]
[46]
Auerbach, A.D. Fanconi anemia and its diagnosis. Mutat. Res., 2009, 668(1-2), 4-10.
[http://dx.doi.org/10.1016/j.mrfmmm.2009.01.013] [PMID: 19622403]
[47]
Hou, H.; Li, D.; Gao, J.; Gao, L.; Lu, Q.; Hu, Y.; Wu, S.; Chu, X.; Yao, Y.; Wan, L.; Ling, J.; Pan, J.; Xu, G.; Hu, S. Proteomic profiling and bioinformatics analysis identify key regulators during the process from fanconi anemia to acute myeloid leukemia. Am. J. Transl. Res., 2020, 12(4), 1415-1427.
[PMID: 32355551]
[48]
Yabe, M.; Koike, T.; Ohtsubo, K.; Imai, E.; Morimoto, T.; Takakura, H.; Koh, K.; Yoshida, K.; Ogawa, S.; Ito, E.; Okuno, Y.; Muramatsu, H.; Kojima, S.; Matsuo, K.; Mori, M.; Hira, A.; Takata, M.; Yabe, H. Associations of complementation group, ALDH2 genotype, and clonal abnormalities with hematological outcome in Japanese patients with Fanconi anemia. Ann. Hematol., 2019, 98(2), 271-280.
[http://dx.doi.org/10.1007/s00277-018-3517-0] [PMID: 30368588]
[49]
Langevin, F.; Crossan, G.P.; Rosado, I.V.; Arends, M.J.; Patel, K.J. Fancd2 counteracts the toxic effects of naturally produced aldehydes in mice. Nature, 2011, 475(7354), 53-58.
[http://dx.doi.org/10.1038/nature10192] [PMID: 21734703]
[50]
Yang, Z.; Wu, X.S.; Wei, Y.; Polyanskaya, S.A.; Iyer, S.V.; Jung, M.; Lach, F.P.; Adelman, E.R.; Klingbeil, O.; Milazzo, J.P.; Kramer, M.; Demerdash, O.E.; Chang, K.; Goodwin, S.; Hodges, E.; McCombie, W.R.; Figueroa, M.E.; Smogorzewska, A.; Vakoc, C.R. Transcriptional silencing of ALDH2 confers a dependency on fanconi anemia proteins in acute myeloid leukemia. Cancer Discov., 2021, 11(9), 2300-2315.
[http://dx.doi.org/10.1158/2159-8290.CD-20-1542] [PMID: 33893150]
[51]
Dick, J.E. Stem cell concepts renew cancer research. Blood, 2008, 112(13), 4793-4807.
[http://dx.doi.org/10.1182/blood-2008-08-077941] [PMID: 19064739]
[52]
Hess, D.A.; Wirthlin, L.; Craft, T.P.; Herrbrich, P.E.; Hohm, S.A.; Lahey, R.; Eades, W.C.; Creer, M.H.; Nolta, J.A. Selection based on CD133 and high aldehyde dehydrogenase activity isolates long-term reconstituting human hematopoietic stem cells. Blood, 2006, 107(5), 2162-2169.
[http://dx.doi.org/10.1182/blood-2005-06-2284] [PMID: 16269619]
[53]
Armstrong, L.; Stojkovic, M.; Dimmick, I.; Ahmad, S.; Stojkovic, P.; Hole, N.; Lako, M. Phenotypic characterization of murine primitive hematopoietic progenitor cells isolated on basis of aldehyde dehydrogenase activity. Stem Cells, 2004, 22(7), 1142-1151.
[http://dx.doi.org/10.1634/stemcells.2004-0170] [PMID: 15579635]
[54]
Christ, O.; Lucke, K.; Imren, S.; Leung, K.; Hamilton, M.; Eaves, A.; Smith, C.; Eaves, C. Improved purification of hematopoietic stem cells based on their elevated aldehyde dehydrogenase activity. Haematologica, 2007, 92(9), 1165-1172.
[55]
Tomita, H.; Tanaka, K.; Tanaka, T.; Hara, A. Aldehyde dehydrogenase 1A1 in stem cells and cancer. Oncotarget, 2016, 7(10), 11018-11032.
[http://dx.doi.org/10.18632/oncotarget.6920] [PMID: 26783961]
[56]
Toledo-Guzmán, M.E.; Hernández, M.I.; Gómez-Gallegos, Á.A.; Ortiz-Sánchez, E. ALDH as a stem cell marker in solid tumors. Curr. Stem Cell Res. Ther., 2019, 14(5), 375-388.
[http://dx.doi.org/10.2174/1574888X13666180810120012] [PMID: 30095061]
[57]
Schuurhuis, G.J.; Meel, M.H.; Wouters, F.; Min, L.A.; Terwijn, M.; de Jonge, N.A.; Kelder, A.; Snel, A.N.; Zweegman, S.; Ossenkoppele, G.J.; Smit, L. Normal hematopoietic stem cells within the AML bone marrow have a distinct and higher ALDH activity level than co-existing leukemic stem cells. PLoS One, 2013, 8(11), e78897.
[http://dx.doi.org/10.1371/journal.pone.0078897] [PMID: 24244383]
[58]
Long, N.A.; Golla, U.; Sharma, A.; Claxton, D.F. Acute myeloid Leukemia stem cells: Origin, characteristics, and clinical implications. Stem Cell Rev. Rep., 2022, 18(4), 1211-1226.
[http://dx.doi.org/10.1007/s12015-021-10308-6] [PMID: 35050458]
[59]
Ran, D.; Schubert, M.; Pietsch, L.; Taubert, I.; Wuchter, P.; Eckstein, V.; Bruckner, T.; Zoeller, M.; Ho, A.D. Aldehyde dehydrogenase activity among primary leukemia cells is associated with stem cell features and correlates with adverse clinical outcomes. Exp. Hematol., 2009, 37(12), 1423-1434.
[http://dx.doi.org/10.1016/j.exphem.2009.10.001] [PMID: 19819294]
[60]
Gerber, J.M.; Smith, B.D.; Ngwang, B.; Zhang, H.; Vala, M.S.; Morsberger, L.; Galkin, S.; Collector, M.I.; Perkins, B.; Levis, M.J.; Griffin, C.A.; Sharkis, S.J.; Borowitz, M.J.; Karp, J.E.; Jones, R.J. A clinically relevant population of leukemic CD34+CD38− cells in acute myeloid leukemia. Blood, 2012, 119(15), 3571-3577.
[http://dx.doi.org/10.1182/blood-2011-06-364182] [PMID: 22262762]
[61]
Liersch, R.; Müller-Tidow, C.; Berdel, W.E.; Krug, U. Prognostic factors for acute myeloid leukaemia in adults - biological significance and clinical use. Br. J. Haematol., 2014, 165(1), 17-38.
[http://dx.doi.org/10.1111/bjh.12750] [PMID: 24484469]
[62]
Li, T.; Su, Y.; Mei, Y.; Leng, Q.; Leng, B.; Liu, Z.; Stass, S.A.; Jiang, F. ALDH1A1 is a marker for malignant prostate stem cells and predictor of prostate cancer patients’ outcome. Lab. Invest., 2010, 90(2), 234-244.
[http://dx.doi.org/10.1038/labinvest.2009.127] [PMID: 20010854]
[63]
Cheung, A.M.S.; Wan, T.S.K.; Leung, J.C.K.; Chan, L.Y.Y.; Huang, H.; Kwong, Y.L.; Liang, R.; Leung, A.Y.H. Aldehyde dehydrogenase activity in leukemic blasts defines a subgroup of acute myeloid leukemia with adverse prognosis and superior NOD/SCID engrafting potential. Leukemia, 2007, 21(7), 1423-1430.
[http://dx.doi.org/10.1038/sj.leu.2404721] [PMID: 17476279]
[64]
Schubert, M.; Herbert, N.; Taubert, I.; Ran, D.; Singh, R.; Eckstein, V.; Vitacolonna, M.; Ho, A. D.; Zöller, M. Differential survival of AML subpopulations in NOD/SCID mice. Exp. Hematol., 2011, 39(2), 250-254.
[65]
Yang, W.; Xie, J.; Hou, R.; Chen, X.; Xu, Z.; Tan, Y.; Ren, F.; Zhang, Y.; Xu, J.; Chang, J.; Wang, H. Disulfiram/cytarabine eradicates a subset of acute myeloid leukemia stem cells with high aldehyde dehydrogenase expression. Leuk. Res., 2020, 92, 106351.
[http://dx.doi.org/10.1016/j.leukres.2020.106351] [PMID: 32224355]
[66]
Yang, L.; Chen, W.M.; Dao, F.T.; Zhang, Y.H.; Wang, Y.Z.; Chang, Y.; Liu, Y.R.; Jiang, Q.; Zhang, X.H.; Liu, K.Y.; Huang, X.J.; Qin, Y.Z. High aldehyde dehydrogenase activity at diagnosis predicts relapse in patients with t(8;21) acute myeloid leukemia. Cancer Med., 2019, 8(12), 5459-5467.
[http://dx.doi.org/10.1002/cam4.2422] [PMID: 31364309]
[67]
Wang, W.; Stiehl, T.; Raffel, S.; Hoang, V. T.; Hoffmann, I.; Poisa-Beiro, L.; Saeed, B. R.; Blume, R.; Manta, L.; Eckstein, V. Reduced hematopoietic stem cell frequency predicts outcome in acute myeloid leukemia. Haematologica, 2017, 102(9), 1567.
[68]
Dancik, G.M.; Voutsas, I.F.; Vlahopoulos, S. Lower RNA expression of ALDH1A1 distinguishes the favorable risk group in acute myeloid leukemia. Mol. Biol. Rep., 2022, 49(4), 3321-3331.
[http://dx.doi.org/10.1007/s11033-021-07073-7] [PMID: 35028852]
[69]
Yanagisawa, B.; Ghiaur, G.; Smith, B.D.; Jones, R.J. Translating leukemia stem cells into the clinical setting: Harmonizing the heterogeneity. Exp. Hematol., 2016, 44(12), 1130-1137.
[http://dx.doi.org/10.1016/j.exphem.2016.08.010] [PMID: 27693555]
[70]
Gerber, J.M.; Zeidner, J.F.; Morse, S.; Blackford, A.L.; Perkins, B.; Yanagisawa, B.; Zhang, H.; Morsberger, L.; Karp, J.; Ning, Y.; Gocke, C.D.; Rosner, G.L.; Smith, B.D.; Jones, R.J. Association of acute myeloid leukemia's most immature phenotype with risk groups and outcomes. Haematologica, 2016, 101(5), 607-616.
[71]
Karantanos, T.; Jones, R.J. Acute myeloid Leukemia stem cell heterogeneity and its clinical relevance. Adv. Exp. Med. Biol., 2019, 1139, 153-169.
[http://dx.doi.org/10.1007/978-3-030-14366-4_9] [PMID: 31134500]
[72]
Plesa, A.; Dumontet, C.; Mattei, E.; Tagoug, I.; Hayette, S.; Sujobert, P.; Tigaud, I.; Pages, M.P.; Chelghoum, Y.; Baracco, F.; Labussierre, H.; Ducastelle, S.; Paubelle, E.; Nicolini, F.E.; Elhamri, M.; Campos, L.; Plesa, C.; Morisset, S.; Salles, G.; Bertrand, Y.; Michallet, M.; Thomas, X. High frequency of CD34+CD38-/low immature leukemia cells is correlated with unfavorable prognosis in acute myeloid leukemia. World J. Stem Cells, 2017, 9(12), 227-234.
[http://dx.doi.org/10.4252/wjsc.v9.i12.227] [PMID: 29321824]
[73]
van Rhenen, A.; Feller, N.; Kelder, A.; Westra, A.H.; Rombouts, E.; Zweegman, S.; van der Pol, M.A.; Waisfisz, Q.; Ossenkoppele, G.J.; Schuurhuis, G.J. High stem cell frequency in acute myeloid leukemia at diagnosis predicts high minimal residual disease and poor survival. Clin. Cancer Res., 2005, 11(18), 6520-6527.
[http://dx.doi.org/10.1158/1078-0432.CCR-05-0468] [PMID: 16166428]
[74]
Hernandez-Valladares, M.; Aasebø, E.; Berven, F.; Selheim, F.; Bruserud, Ø. Biological characteristics of aging in human acute myeloid leukemia cells: The possible importance of aldehyde dehydrogenase, the cytoskeleton and altered transcriptional regulation. Aging (Albany NY), 2020, 12(24), 24734-24777.
[http://dx.doi.org/10.18632/aging.202361] [PMID: 33349623]
[75]
Yuan, B.; El Dana, F.; Ly, S.; Yan, Y.; Ruvolo, V.; Shpall, E.J.; Konopleva, M.; Andreeff, M.; Battula, V.L. Bone marrow stromal cells induce an ALDH+ stem cell-like phenotype and enhance therapy resistance in AML through a TGF-β-p38-ALDH2 pathway. PLoS One, 2020, 15(11), e0242809.
[http://dx.doi.org/10.1371/journal.pone.0242809] [PMID: 33253299]
[76]
Kawasoe, M.; Yamamoto, Y.; Okawa, K.; Funato, T.; Takeda, M.; Hara, T.; Tsurumi, H.; Moriwaki, H.; Arioka, Y.; Takemura, M. Acquired resistance of leukemic cells to AraC is associated with the upregulation of aldehyde dehydrogenase 1 family member A2. Exp. Hematol., 2013, 41(7), 597-603.
[http://dx.doi.org/10.1016/j.exphem.2013.03.004]
[77]
Yusuf, R.Z.; Saez, B.; Sharda, A.; van Gastel, N.; Yu, V.W.C.; Baryawno, N.; Scadden, E.W.; Acharya, S.; Chattophadhyay, S.; Huang, C.; Viswanathan, V.; S’aulis, D.; Cobert, J.; Sykes, D.B.; Keibler, M.A.; Das, S.; Hutchinson, J.N.; Churchill, M.; Mukherjee, S.; Lee, D.; Mercier, F.; Doench, J.; Bullinger, L.; Logan, D.J.; Schreiber, S.; Stephanopoulos, G.; Rizzo, W.B.; Scadden, D.T. Aldehyde dehydrogenase 3a2 protects AML cells from oxidative death and the synthetic lethality of ferroptosis inducers. Blood, 2020, 136(11), 1303-1316.
[http://dx.doi.org/10.1182/blood.2019001808] [PMID: 32458004]
[78]
Morgan, C.A.; Parajuli, B.; Buchman, C.D.; Dria, K.; Hurley, T.D. N,N-diethylaminobenzaldehyde (DEAB) as a substrate and mechanism-based inhibitor for human ALDH isoenzymes. Chem. Biol. Interact., 2015, 234, 18-28.
[http://dx.doi.org/10.1016/j.cbi.2014.12.008] [PMID: 25512087]
[79]
Xu, B.; Wang, S.; Li, R.; Chen, K.; He, L.; Deng, M.; Kannappan, V.; Zha, J.; Dong, H.; Wang, W. Disulfiram/copper selectively eradicates AML leukemia stem cells in vitro and in vivo by simultaneous induction of ROS-JNK and inhibition of NF-κB and Nrf2. Cell Death Dis., 2017, 8(5), e2797.
[http://dx.doi.org/10.1038/cddis.2017.176] [PMID: 28518151]
[80]
Bista, R.; Lee, D.W.; Pepper, O.B.; Azorsa, D.O.; Arceci, R.J.; Aleem, E. Disulfiram overcomes bortezomib and cytarabine resistance in Down-syndrome-associated acute myeloid leukemia cells. J. Exp. Clin. Cancer Res., 2017, 36(1), 22.
[http://dx.doi.org/10.1186/s13046-017-0493-5] [PMID: 28143565]
[81]
Skrott, Z.; Majera, D.; Gursky, J.; Buchtova, T.; Hajduch, M.; Mistrik, M.; Bartek, J. Disulfiram’s anti-cancer activity reflects targeting NPL4, not inhibition of aldehyde dehydrogenase. Oncogene, 2019, 38(40), 6711-6722.
[http://dx.doi.org/10.1038/s41388-019-0915-2] [PMID: 31391554]
[82]
Venton, G.; Pérez-Alea, M.; Baier, C.; Fournet, G.; Quash, G.; Labiad, Y.; Martin, G.; Sanderson, F.; Poullin, P.; Suchon, P.; Farnault, L.; Nguyen, C.; Brunet, C.; Ceylan, I.; Costello, R.T. Aldehyde dehydrogenases inhibition eradicates leukemia stem cells while sparing normal progenitors. Blood Cancer J., 2016, 6(9), e469.
[http://dx.doi.org/10.1038/bcj.2016.78] [PMID: 27611922]
[83]
Annageldiyev, C.; Gowda, K.; Patel, T.; Bhattacharya, P.; Tan, S.-F.; Iyer, S.; Desai, D.; Dovat, S.; Feith, D.J.; Loughran, T.P., Jr The novel Isatin analog KS99 targets stemness markers in acute myeloid leukemia. Haematologica, 2020, 105, 3-687.
[84]
Elcheva, I.A.; Wood, T.; Chiarolanzio, K.; Chim, B.; Wong, M.; Singh, V.; Gowda, C.P.; Lu, Q.; Hafner, M.; Dovat, S.; Liu, Z.; Muljo, S.A.; Spiegelman, V.S. RNA-binding protein IGF2BP1 maintains leukemia stem cell properties by regulating HOXB4, MYB, and ALDH1A1. Leukemia, 2020, 34(5), 1354-1363.
[http://dx.doi.org/10.1038/s41375-019-0656-9] [PMID: 31768017]
[85]
Smith, C.; Gasparetto, M.; Humphries, K.; Pollyea, D.A.; Vasiliou, V.; Jordan, C.T. Aldehyde dehydrogenases in acute myeloid leukemia. Ann. N. Y. Acad. Sci., 2014, 1310(1), 58-68.
[http://dx.doi.org/10.1111/nyas.12414] [PMID: 24641679]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy