Abstract
Chronic Myeloid Leukemia (CML) represents 15-20% of all new cases of leukemia and is characterized by an uncontrolled proliferation of abnormal myeloid cells. Currently, the first-line of treatment involves Tyrosine Kinase Inhibitors (TKIs), which specifically inhibits the activity of the fusion protein BCR-ABL. However, resistance, mainly due to mutations, can occur. In the attempt to find more effective and less toxic therapies, several approaches are taken into consideration such as research of new anti-leukemic drugs and “combination chemotherapy” where different drugs that act by different mechanisms are used. Here, we reviewed the molecular mechanisms of CML, the main mechanisms of drug resistance and current strategies to enhance the therapeutic effect of TKIs in CML. Despite major advances in CML treatment, new, more potent anticancer drugs and with fewer side effects are needed. Marine organisms, and particularly seaweed, have a high diversity of bioactive compounds with some of them having anticancer activity in several in vitro and in vivo models. The state-of-art suggests that their use during cancer treatment may improve the outcome. We reviewed here the yet few data supporting anti-leukemic activity of some carotenoids and phlorotannins in some leukemia models. Also, strategies to overcome drug resistance are discussed, particularly the combination of conventional drugs with natural compounds.
Keywords: Carotenoids, imatinib, leukemia, seaweed, phlorotannins, Acute Myeloid Leukemia (AML).
Graphical Abstract
[1]
Gibson, J.; Iland, H.J.; Larsen, S.R.; Brown, C.M.; Joshua, D.E. Leukaemias into the 21st century. Part 2: The chronic leukaemias. Intern. Med. J., 2013, 43(5), 484-494.
[2]
Torre, L.A.; Bray, F.; Siegel, R.L.; Ferlay, J.; Lortet-Tieulent, J.; Jemal, A. Global cancer statistics, 2012. CA Cancer J. Clin., 2015, 65(2), 87-108.
[3]
Vardiman, J.W.; Thiele, J.; Arber, D.A.; Brunning, R.D.; Borowitz, M.J.; Porwit, A.; Harris, N.L.; Le Beau, M.M.; Hellstrom-Lindberg, E.; Tefferi, A.; Bloomfield, C.D. The 2008 revision of the World Health Organization (WHO) classification of myeloid neoplasms and acute leukemia: Rationale and important changes. Blood, 2009, 114(5), 937-951.
[4]
Freireich, E.J.; Wiernik, P.H.; Steensma, D.P. The leukemias: A half-century of discovery. J. Clin. Oncol., 2014, 32(31), 3463-3469.
[5]
Rowley, J.D. Letter: A new consistent chromosomal abnormality in chronic myelogenous leukaemia identified by quinacrine fluorescence and Giemsa staining. Nature, 1973, 243(5405), 290-293.
[6]
Ilander, M.; Olsson-Stromberg, U.; Schlums, H.; Guilhot, J.; Bruck, O.; Lahteenmaki, H.; Kasanen, T.; Koskenvesa, P.; Soderlund, S.; Hoglund, M.; Markevarn, B.; Sjalander, A.; Lotfi, K.; Dreimane, A.; Lubking, A.; Holm, E.; Bjoreman, M.; Lehmann, S.; Stenke, L.; Ohm, L.; Gedde-Dahl, T.; Majeed, W.; Ehrencrona, H. Increased proportion of mature NK cells is associated with successful imatinib discontinuation in chronic myeloid leukemia. Leukemia, 2017, 31(5), 1108-1116.
[7]
Zhou, H.; Xu, R. Leukemia stem cells: The root of chronic myeloid leukemia. Protein Cell, 2015, 6(6), 403-412.
[8]
Carter, B.Z.; Mak, P.Y.; Mu, H.; Zhou, H.; Mak, D.H.; Schober, W.; Leverson, J.D.; Zhang, B.; Bhatia, R.; Huang, X.; Cortes, J.; Kantarjian, H.; Konopleva, M.; Andreeff, M. Combined targeting of BCL-2 and BCR-ABL tyrosine kinase eradicates chronic myeloid leukemia stem cells. Sci. Transl. Med., 2016, 8(355)355ra117
[9]
Hamed, I.; Özogul, F.; Özogul, Y.; Regenstein, J.M. Marine bioactive compounds and their health benefits: A review. Compr. Rev. Food Sci. Food Saf., 2015, 14(4), 446-465.
[10]
Liu, L.; Heinrich, M.; Myers, S.; Dworjanyn, S.A. Towards a better understanding of medicinal uses of the brown seaweed Sargassum in Traditional Chinese Medicine: A phytochemical and pharma-cological review. J. Ethnopharmacol., 2012, 142(3), 591-619.
[11]
Golub, T.R.; Slonim, D.K.; Tamayo, P.; Huard, C.; Gaasenbeek, M.; Mesirov, J.P.; Coller, H.; Loh, M.L.; Downing, J.R.; Caligiuri, M.A.; Bloomfield, C.D.; Lander, E.S. Molecular classification of cancer: class discovery and class prediction by gene expression monitoring. Science, 1999, 286(5439), 531-537.
[12]
Xiong, X.B.; Ma, Z.; Lai, R.; Lavasanifar, A. The therapeutic response to multifunctional polymeric nano-conjugates in the targeted cellular and subcellular delivery of doxorubicin. Biomaterials, 2010, 31(4), 757-768.
[13]
Ghosh, D.; Dey, S.K.; Saha, C. Protective effect of black tea extract during chemotherapeutic drug induced oxidative damage on normal lymphocytes in comparison with cancerous K562 cells. Int. J. Sci. Eng. Res., 2014, 5(2), 437-447.
[14]
Greuber, E.K.; Smith-Pearson, P.; Wang, J.; Pendergast, A.M. Role of ABL family kinases in cancer: From leukaemia to solid tumours. Nat. Rev. Cancer, 2013, 13(8), 559-571.
[15]
Deininger, M.W.; Goldman, J.M.; Melo, J.V. The molecular biology of chronic myeloid leukemia. Blood, 2000, 96(10), 3343-3356.
[16]
O’Brien, S.; Abboud, C.N.; Akhtari, M.; Altman, J.; Berman, E.; DeAngelo, D.J.; Devine, S.; Fathi, A.T.; Gotlib, J.; Jagasia, M.; Moore, J.O.; Pinilla-Ibarz, J.; Radich, J.P.; Reddy, V.V.; Shah, N.P.; Shami, P.J.; Smith, B.D.; Snyder, D.S.; Wetzler, M.; Yunus, F. Chronic myelogenous leukemia. J. Natl. Compr. Canc. Netw., 2012, 10, 64-110.
[17]
Sinclair, A.; Latif, A.L.; Holyoake, T.L. Targeting survival pathways in chronic myeloid leukaemia stem cells. Br. J. Pharmacol., 2013, 169(8), 1693-1707.
[18]
Collis, S.J.; Tighe, A.; Scott, S.D.; Roberts, S.A.; Hendry, J.H.; Margison, G.P. Ribozyme minigene-mediated RAD51 down-regulation increases radiosensitivity of human prostate cancer cells. Nucleic Acids Res., 2001, 29(7), 1534-1538.
[19]
Bedi, A.; Barber, J.P.; Bedi, G.C.; el-Deiry, W.S.; Sidransky, D.; Vala, M.S.; Akhtar, A.J.; Hilton, J.; Jones, R.J. BCR-ABL-mediated inhibition of apoptosis with delay of G2/M transition after DNA damage: A mechanism of resistance to multiple anticancer agents. Blood, 1995, 86(3), 1148-1158.
[20]
Skorski, T. BCR/ABL regulates response to DNA damage: The role in resistance to genotoxic treatment and in genomic instability. Oncogene, 2002, 21(56), 8591-8604.
[21]
Cook, G.J.; Pardee, T.S. Animal models of leukemia: Any closer to the real thing? Cancer Metastasis Rev., 2013, 32(1-2), 63-76.
[22]
Shet, A.S.; Jahagirdar, B.N.; Verfaillie, C.M. Chronic myelogenous leukemia: Mechanisms underlying disease progression. Leukemia, 2002, 16(8), 1402-1411.
[23]
Mahon, F.X.; Deininger, M.W.; Schultheis, B.; Chabrol, J.; Reiffers, J.; Goldman, J.M.; Melo, J.V. Selection and characterization of BCR-ABL positive cell lines with differential sensitivity to the tyrosine kinase inhibitor STI571: Diverse mechanisms of resistance. Blood, 2000, 96(3), 1070-1079.
[24]
Druker, B.J.; Tamura, S.; Buchdunger, E.; Ohno, S.; Segal, G.M.; Fanning, S.; Zimmermann, J.; Lydon, N.B. Effects of a selective inhibitor of the Abl tyrosine kinase on the growth of Bcr-Abl positive cells. Nat. Med., 1996, 2(5), 561-566.
[25]
Druker, B.J.; Guilhot, F.; O’Brien, S.G.; Gathmann, I.; Kantarjian, H.; Gattermann, N.; Deininger, M.W.; Silver, R.T.; Goldman, J.M.; Stone, R.M.; Cervantes, F.; Hochhaus, A.; Powell, B.L.; Gabrilove, J.L.; Rousselot, P.; Reiffers, J.; Cornelissen, J.J.; Hughes, T.; Agis, H.; Fischer, T.; Verhoef, G.; Shepherd, J.; Saglio, G.; Gratwohl, A.; Nielsen, J.L.; Radich, J.P.; Simonsson, B.; Taylor, K.; Baccarani, M.; So, C.; Letvak, L.; Larson, R.A. Five-year follow-up of patients receiving imatinib for chronic myeloid leukemia. N. Engl. J. Med., 2006, 355(23), 2408-2417.
[26]
Bhamidipati, P.K.; Kantarjian, H.; Cortes, J.; Cornelison, A.M.; Jabbour, E. Management of imatinib-resistant patients with chronic myeloid leukemia. Ther. Adv. Hematol., 2013, 4(2), 103-117.
[27]
Thomas, J.; Wang, L.; Clark, R.E.; Pirmohamed, M. Active transport of imatinib into and out of cells: Implications for drug resistance. Blood, 2004, 104(12), 3739-3745.
[28]
Gambacorti-Passerini, C.; Barni, R.; le Coutre, P.; Zucchetti, M.; Cabrita, G.; Cleris, L.; Rossi, F.; Gianazza, E.; Brueggen, J.; Cozens, R.; Pioltelli, P.; Pogliani, E.; Corneo, G.; Formelli, F.; D’Incalci, M. Role of alpha1 acid glycoprotein in the in vivo resistance of human BCR-ABL(+) leukemic cells to the abl inhibitor STI571. J. Natl. Cancer Inst., 2000, 92(20), 1641-1650.
[29]
Villuendas, R.; Steegmann, J.L.; Pollan, M.; Tracey, L.; Granda, A.; Fernandez-Ruiz, E.; Casado, L.F.; Martinez, J.; Martinez, P.; Lombardia, L.; Villalon, L.; Odriozola, J.; Piris, M.A. Identification of genes involved in imatinib resistance in CML: A gene-expression profiling approach. Leukemia, 2006, 20(6), 1047-1054.
[30]
Mughal, A.; Aslam, H.M.; Khan, A.M.; Saleem, S.; Umah, R.; Saleem, M. Bcr-Abl tyrosine kinase inhibitors- current status. Infect. Agent. Cancer, 2013, 8, 23.
[31]
Miller, G.D.; Bruno, B.J.; Lim, C.S. Resistant mutations in CML and Ph(+)ALL - role of ponatinib. Biologics, 2014, 8, 243-254.
[32]
Hu, Z.; Pan, X.F.; Wu, F.Q.; Ma, L.Y.; Liu, D.P.; Liu, Y.; Feng, T.T.; Meng, F.Y.; Liu, X.L.; Jiang, Q.L.; Chen, X.Q.; Liu, J.L.; Liu, P.; Chen, Z.; Chen, S.J.; Zhou, G.B. Synergy between proteasome inhibitors and imatinib mesylate in chronic myeloid leukemia. PLoS One, 2009, 4(7)e6257
[33]
FDA, U.S. Food and Drug Administration
https://www.accessdata. fda.gov/scripts/cder/daf/index.cfm?event=overview.process&applno=203469 (accessed November 2, 2017).
[34]
Tolomeo, M.; Grimaudo, S.; Di Cristina, A.; Roberti, M.; Pizzirani, D.; Meli, M.; Dusonchet, L.; Gebbia, N.; Abbadessa, V.; Crosta, L.; Barucchello, R.; Grisolia, G.; Invidiata, F.; Simoni, D. Pterostilbene and 3′-hydroxypterostilbene are effective apoptosis-inducing agents in MDR and BCR-ABL-expressing leukemia cells. Int. J. Biochem. Cell Biol., 2005, 37(8), 1709-1726.
[35]
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(6), 1191-1199.
[36]
Eucker, J.; Zang, C.; Zhou, Y.; Li, X.; Habbel, P.; Neumann, C.; Scholz, C.; Liu, H. The multi-tyrosine kinase inhibitor TKI258, alone or in combination with RAD001, is effective for treatment of human leukemia with BCR-ABL translocation in vitro. Anticancer Res., 2014, 34(9), 4909-4914.
[37]
Yardley, D.A. Drug resistance and the role of combination chemotherapy in improving patient outcomes. Int. J. Breast Cancer, 2013, 2013 137414
[38]
Mokhtari, R.B.; Homayouni, T.S.; Baluch, N.; Morgatskaya, E.; Kumar, S.; Das, B.; Yeger, H. Combination therapy in combating cancer. Oncotarget, 2017, 8(23), 38022-38043.
[39]
Nimmanapalli, R.; Fuino, L.; Stobaugh, C.; Richon, V.; Bhalla, K. Cotreatment with the histone deacetylase inhibitor Suberoylanilide Hydroxamic Acid (SAHA) enhances imatinib-induced apoptosis of Bcr-Abl-positive human acute leukemia cells. Blood, 2003, 101(8), 3236-3239.
[40]
Bu, Q.; Cui, L.; Li, J.; Du, X.; Zou, W.; Ding, K.; Pan, J. SAHA and S116836, a novel tyrosine kinase inhibitor, synergistically induce apoptosis in imatinib-resistant chronic myelogenous leukemia cells. Cancer Biol. Ther., 2014, 15(7), 951-962.
[41]
Lin, T.Y.; Chen, K.C.; Liu, H.J.; Liu, A.J.; Wang, K.L.; Shih, C.M. MicroRNA-1301-Mediated RanGAP1 downregulation induces bcr-abl nuclear entrapment to enhance imatinib efficacy in chronic myeloid leukemia cells. PLoS One, 2016, 11(5) e0156260
[42]
Wei, Y.; To, K.K.; Au-Yeung, S.C. Synergistic cytotoxicity from combination of imatinib and platinum-based anticancer drugs specifically in Bcr-Abl positive leukemia cells. J. Pharmacol. Sci., 2015, 129(4), 210-215.
[43]
Zhang, M.; Luo, Z.; Liu, H.; Croce, C.M.; Burke, T.R., Jr; Bottaro, D.P. Synergistic anti-leukemic activity of imatinib in combination with a small molecule Grb2 SH2 domain binding antagonist. Leukemia, 2014, 28(4), 948-951.
[44]
Tipping, A.J.; Mahon, F.X.; Zafirides, G.; Lagarde, V.; Goldman, J.M.; Melo, J.V. Drug responses of imatinib mesylate-resistant cells: Synergism of imatinib with other chemotherapeutic drugs. Leukemia, 2002, 16(12), 2349-2357.
[45]
Crawford, L.J.; Chan, E.T.; Aujay, M.; Holyoake, T.L.; Melo, J.V.; Jorgensen, H.G.; Suresh, S.; Walker, B.; Irvine, A.E. Synergistic effects of proteasome inhibitor carfilzomib in combination with tyrosine kinase inhibitors in imatinib-sensitive and -resistant chronic myeloid leukemia models. Oncogenesis, 2014, 3 e90
[46]
Gallipoli, P.; Cook, A.; Rhodes, S.; Hopcroft, L.; Wheadon, H.; Whetton, A.D.; Jorgensen, H.G.; Bhatia, R.; Holyoake, T.L. JAK2/STAT5 inhibition by nilotinib with ruxolitinib contributes to the elimination of CML CD34+ cells in vitro and in vivo. Blood, 2014, 124(9), 1492-1501.
[47]
Sithranga Boopathy, N.; Kathiresan, K. Anticancer drugs from marine flora: an overview. J. Oncol., 2010, 2010 214186
[48]
Kolanjinathan, K.; Ganesh, P.; Saranraj, P. Pharmacological importance of seaweeds: A review. World J. Fish Marine Sci., 2014, 6, 1-15.
[49]
Cornish, M.L.; Garbary, D.J. Antioxidants from macroalgae: Potential applications in human health and nutrition. Algae, 2010, 25(4), 155-171.
[50]
Hafting, J.T.; Craigie, J.S.; Stengel, D.B.; Loureiro, R.R.; Buschmann, A.H.; Yarish, C.; Edwards, M.D.; Critchley, A.T. Prospects and challenges for industrial production of seaweed bioactives. J. Phycol., 2015, 51(5), 821-837.
[51]
Stengel, D.B.; Connan, S. Marine algae: A source of biomass for biotechnological applications. Methods Mol. Biol., 2015, 1308, 1-37.
[52]
Heo, S-J.; Ko, S-C.; Kang, S-M.; Kang, H-S.; Kim, J-P.; Kim, S-H.; Lee, K-W.; Cho, M-G.; Jeon, Y-J. Cytoprotective effect of fucoxanthin isolated from brown algae Sargassum siliquastrum against H2O2-induced cell damage. Eur. Food Res. Technol., 2008, 228, 145-151.
[54]
Sharif, N.; Munir, N.; Saleem, F.; Aslam, F.; Naz, S. Prolific anticancer bioactivity of algal extracts. Cell, 2014, 3(4), 8.
[55]
Chojnacka, K.; Saeid, A.; Witkowska, Z.; Tuhy, L. In Biologically active compounds in seaweed extracts—the prospects for the application. Open Conf. Proc. J., 2012, M4.
[56]
Dembitsky, V.M.; Maoka, T. Allenic and cumulenic lipids. Prog. Lipid Res., 2007, 46(6), 328-375.
[58]
Takaichi, S. Carotenoids in algae: Distributions, biosyntheses and functions. Mar. Drugs, 2011, 9(6), 1101-1118.
[59]
Barros, M.P.; Poppe, S.C.; Bondan, E.F. Neuroprotective properties of the marine carotenoid astaxanthin and omega-3 fatty acids, and perspectives for the natural combination of both in krill oil. Nutrients, 2014, 6(3), 1293-1317.
[60]
Saini, R.K.; Nile, S.H.; Park, S.W. Carotenoids from fruits and vegetables: Chemistry, analysis, occurrence, bioavailability and biological activities. Food Res. Int., 2015, 76(Pt 3), 735-750.
[61]
Fernández-García, E.; Carvajal-Lérida, I.; Jarén-Galán, M.; Garrido-Fernández, J.; Pérez-Gálvez, A.; Hornero-Méndez, D. Carotenoids bioavailability from foods: From plant pigments to efficient biological activities. Food Res. Int., 2012, 46(2), 438-450.
[62]
Ishikawa, C.; Tafuku, S.; Kadekaru, T.; Sawada, S.; Tomita, M.; Okudaira, T.; Nakazato, T.; Toda, T.; Uchihara, J.N.; Taira, N.; Ohshiro, K.; Yasumoto, T.; Ohta, T.; Mori, N. Anti-adult T-cell leukemia effects of brown algae fucoxanthin and its deacetylated product, fucoxanthinol. Int. J. Cancer, 2008, 123(11), 2702-2712.
[63]
Tanaka, T.; Shnimizu, M.; Moriwaki, H. Cancer chemoprevention by carotenoids. Molecules, 2012, 17(3), 3202-3242.
[64]
Sachindra, N.M.; Sato, E.; Maeda, H.; Hosokawa, M.; Niwano, Y.; Kohno, M.; Miyashita, K. Radical scavenging and singlet oxygen quenching activity of marine carotenoid fucoxanthin and its metabolites. J. Agric. Food Chem., 2007, 55(21), 8516-8522.
[65]
Rengarajan, T.; Rajendran, P.; Nandakumar, N.; Balasubramanian, M.P.; Nishigaki, I. Cancer preventive efficacy of marine carotenoid fucoxanthin: Cell cycle arrest and apoptosis. Nutrients, 2013, 5(12), 4978-4989.
[66]
Peng, J.; Yuan, J-P.; Wu, C-F.; Wang, J-H. Fucoxanthin, a marine carotenoid present in brown seaweeds and diatoms: Metabolism and bioactivities relevant to human health. Mar. Drugs, 2011, 9(10), 1806-1828.
[67]
Anand, P.; Kunnumakkara, A.B.; Sundaram, C.; Harikumar, K.B.; Tharakan, S.T.; Lai, O.S.; Sung, B.; Aggarwal, B.B. Cancer is a preventable disease that requires major lifestyle changes. Pharm. Res., 2008, 25(9), 2097-2116.
[68]
Wang, J.; Chen, S.; Xu, S.; Yu, X.; Ma, D.; Hu, X.; Cao, X. In vivo induction of apoptosis by fucoxanthin, a marine carotenoid, associated with down-regulating STAT3/EGFR signaling in sarcoma 180 (S180) xenografts-bearing mice. Mar. Drugs, 2012, 10(9), 2055-2068.
[69]
Almeida, T.P.; Ferreira, J.; Vettorazzi, A.; Azqueta, A.; Rocha, E.; Ramos, A.A. Cytotoxic activity of fucoxanthin, alone and in combination with the cancer drugs imatinib and doxorubicin, in CML cell lines. Environ. Toxicol. Pharmacol., 2018, 59, 24-33.
[70]
Carter, B.Z.; Mak, D.H.; Schober, W.D.; Cabreira-Hansen, M.; Beran, M.; McQueen, T.; Chen, W.; Andreeff, M. Regulation of survivin expression through Bcr-Abl/MAPK cascade: Targeting survivin overcomes imatinib resistance and increases imatinib sensitivity in imatinib-responsive CML cells. Blood, 2006, 107(4), 1555-1563.
[71]
Baldwin, A.S. Control of oncogenesis and cancer therapy resistance by the transcription factor NF-kappaB. J. Clin. Invest., 2001, 107(3), 241-246.
[72]
Carrà, G.; Torti, D.; Crivellaro, S.; Panuzzo, C.; Taulli, R.; Cilloni, D.; Guerrasio, A.; Saglio, G.; Morotti, A. The BCR-ABL/NF-κB signal transduction network: A long lasting relationship in Philadelphia positive Leukemias. Oncotarget, 2016, 7(40), 66287-66298.
[73]
Konishi, I.; Hosokawa, M.; Sashima, T.; Kobayashi, H.; Miyashita, K. Halocynthiaxanthin and fucoxanthinol isolated from Halocynthia roretzi induce apoptosis in human leukemia, breast and colon cancer cells. Comp. Biochem. Physiol. C Toxicol. Pharmacol., 2006, 142(1-2), 53-59.
[74]
Hosokawa, M.; Wanezaki, S.; Miyauchi, K.; Kurihara, H.; Kohno, H.; Kawabata, J.; Odashima, S.; Takahashi, K. Apoptosis-inducing effect of fucoxanthin on human leukemia cell line HL-60. Food Sci. Technol. Res., 1999, 5(3), 243-246.
[75]
Nakazawa, Y.; Sashima, T.; Hosokawa, M.; Miyashita, K. Comparative evaluation of growth inhibitory effect of stereoisomers of fucoxanthin in human cancer cell lines. J. Funct. Foods, 2009, 1(1), 88-97.
[76]
Kim, K-N.; Heo, S-J.; Kang, S-M.; Ahn, G.; Jeon, Y-J. Fucoxanthin induces apoptosis in human leukemia HL-60 cells through a ROS-mediated Bcl-xL pathway. Toxicol. In Vitro, 2010, 24(6), 1648-1654.
[77]
Kotake-Nara, E.; Terasaki, M.; Nagao, A. Characterization of apoptosis induced by fucoxanthin in human promyelocytic leukemia cells. Biosci. Biotechnol. Biochem., 2005, 69(1), 224-227.
[78]
Ganesan, P.; Noda, K.; Manabe, Y.; Ohkubo, T.; Tanaka, Y.; Maoka, T.; Sugawara, T.; Hirata, T. Siphonaxanthin, a marine carotenoid from green algae, effectively induces apoptosis in human leukemia (HL-60) cells. Biochim. Biophys. Acta, 2011, 1810(5), 497-503.
[79]
Sugawara, T.; Matsubara, K.; Akagi, R.; Mori, M.; Hirata, T. Antiangiogenic activity of brown algae fucoxanthin and its deacetylated product, fucoxanthinol. J. Agric. Food Chem., 2006, 54(26), 9805-9810.
[80]
Ganesan, P.; Matsubara, K.; Ohkubo, T.; Tanaka, Y.; Noda, K.; Sugawara, T.; Hirata, T. Anti-angiogenic effect of siphonaxanthin from green alga, Codium fragile. Phytomedicine, 2010, 17(14), 1140-1144.
[81]
Vicente-Dueñas, C.; Barajas-Diego, M.; Romero-Camarero, I.; González-Herrero, I.; Flores, T.; Sánchez-García, I. Essential role for telomerase in chronic myeloid leukemia induced by BCR-ABL in mice. Oncotarget, 2012, 3(3), 261-266.
[82]
Wang, L.; Xiao, H.; Zhang, X.; Wang, C.; Huang, H. The role of telomeres and telomerase in hematologic malignancies and hematopoietic stem cell transplantation. J. Hematol. Oncol., 2014, 7(1), 61.
[83]
Gharib, A.; Faezizadeh, Z. In vitro anti-telomerase activity of novel lycopene-loaded nanospheres in the human leukemia cell line K562. Pharmacogn. Mag., 2014, 10(Suppl. 1), S157-S163.
[84]
Faezizadeh, Z.; Gharib, A.; Godarzi, M. The effect of β-ionone on telomerase activity in the human leukemia cell line K562. J. Kermanshah Uni. Med. Sci., 2015, 19(3), 118-127.
[85]
Gharib, A.; Faezizadeh, Z.; Godarzee, M. Preparation and characterization of nanoliposomal beta-cryptoxanthin and its effect on proliferation and apoptosis in human leukemia cell line K562. Trop. J. Pharm. Res., 2015, 14(2), 187-194.
[86]
Zhang, X.; Zhao, W.E.; Hu, L.; Zhao, L.; Huang, J. Carotenoids inhibit proliferation and regulate expression of peroxisome proliferators-activated receptor gamma (PPARgamma) in K562 cancer cells. Arch. Biochem. Biophys., 2011, 512(1), 96-106.
[87]
Wang, J.; Lu, L.; Kok, C.H.; Saunders, V.A.; Goyne, J.M.; Dang, P.; Leclercq, T.M.; Hughes, T.P.; White, D.L. Increased peroxisome proliferator-activated receptor γ activity reduces imatinib uptake and efficacy in chronic myeloid leukemia mononuclear cells. Haematologica, 2017, 102(5), 843-853.
[88]
Prost, S.; Relouzat, F.; Spentchian, M.; Ouzegdouh, Y.; Saliba, J.; Massonnet, G.; Beressi, J.P.; Verhoeyen, E.; Raggueneau, V.; Maneglier, B.; Castaigne, S.; Chomienne, C.; Chretien, S.; Rousselot, P.; Leboulch, P. Erosion of the chronic myeloid leukaemia stem cell pool by PPARgamma agonists. Nature, 2015, 525(7569), 380-383.
[89]
Das, S.K.; Hashimoto, T.; Shimizu, K.; Yoshida, T.; Sakai, T.; Sowa, Y.; Komoto, A.; Kanazawa, K. Fucoxanthin induces cell cycle arrest at G 0/G 1 phase in human colon carcinoma cells through up-regulation of p21 WAF1/Cip1. Biochim. Biophys. Acta, 2005, 1726(3), 328-335.
[90]
Lian, F.; Hu, K.Q.; Russell, R.M.; Wang, X.D. β-Cryptoxanthin suppresses the growth of immortalized human bronchial epithelial cells and non-small-cell lung cancer cells and up-regulates retinoic acid receptor β expression. Int. J. Cancer, 2006, 119(9), 2084-2089.
[91]
Stivala, L.A.; Savio, M.; Quarta, S.; Scotti, C.; Cazzalini, O.; Rossi, L.; Scovassi, I.A.; Pizzala, R.; Melli, R.; Bianchi, L. The antiproliferative effect of β-carotene requires p21waf1/cip1 in normal human fibroblasts. FEBS J., 2000, 267(8), 2290-2296.
[92]
Liu, J-H.; Yen, C-C.; Lin, Y-C.; Gau, J-P.; Yang, M-H.; Chao, T-C.; Hsiao, L-T.; Wang, W-S.; Tsai, Y-C.; Chen, P-M. Overexpression of cyclin D1 in accelerated-phase chronic myeloid leukemia. Leuk. Lymphoma, 2004, 45(12), 2419-2425.
[93]
Santos, G.; Almeida, M.; Antunes, L.; Bianchi, M. Effect of bixin on DNA damage and cell death induced by doxorubicin in HL60 cell line. Hum. Exp. Toxicol., 2016, 35(12), 1319-1327.
[94]
Palozza, P.; Serini, S.; Torsello, A.; Di Nicuolo, F.; Piccioni, E.; Ubaldi, V.; Pioli, C.; Wolf, F.I.; Calviello, G. Beta-carotene regulates NF-kappaB DNA-binding activity by a redox mechanism in human leukemia and colon adenocarcinoma cells. J. Nutr., 2003, 133(2), 381-388.
[95]
Sacha, T.; Zawada, M.; Hartwich, J.; Lach, Z.; Polus, A.; Szostek, M.; Zdzi Owska, E.; Libura, M.; Bodzioch, M.; Dembinska-Kiec, A.; Skotnicki, A.B.; Goralczyk, R.; Wertz, K.; Riss, G.; Moele, C.; Langmann, T.; Schmitz, G. The effect of beta-carotene and its derivatives on cytotoxicity, differentiation, proliferative potential and apoptosis on the three human acute leukemia cell lines: U-937, HL-60 and TF-1. Biochim. Biophys. Acta, 2005, 1740(2), 206-214.
[96]
Upadhyaya, K.R.; Radha, K.S.; Madhyastha, H.K. Cell cycle regulation and induction of apoptosis by beta-carotene in U937 and HL-60 leukemia cells. J. Biochem. Mol. Biol., 2007, 40(6), 1009-1015.
[97]
Yang, H.; Zeng, M.; Dong, S.; Liu, Z.; Li, R. Anti-proliferative activity of phlorotannin extracts from brown algae Laminaria japonica Aresch. Chin. J. Oceanology Limnol., 2010, 28(1), 122-130.
[98]
Liu, J.Y.; Liu, Z.; Wang, D.M.; Li, M.M.; Wang, S.X.; Wang, R.; Chen, J.P.; Wang, Y.F.; Yang, D.P. Induction of apoptosis in K562 cells by dicyclohexylammonium salt of hyperforin through a mitochondrial-related pathway. Chem. Biol. Interact., 2011, 190(2-3), 91-101.
[99]
Merhi, F.; Tang, R.; Piedfer, M.; Mathieu, J.; Bombarda, I.; Zaher, M.; Kolb, J-P.; Billard, C.; Bauvois, B. Hyperforin inhibits Akt1 kinase activity and promotes caspase-mediated apoptosis involving Bad and Noxa activation in human myeloid tumor cells. PLoS One, 2011, 6(10)e25963
[100]
Quiney, C.; Billard, C.; Faussat, A.M.; Salanoubat, C.; Ensaf, A.; Nait-Si, Y.; Fourneron, J.D.; Kolb, J.P. Pro-apoptotic properties of hyperforin in leukemic cells from patients with B-cell chronic lymphocytic leukemia. Leukemia, 2006, 20(3), 491-497.
[101]
Quiney, C.; Billard, C.; Mirshahi, P.; Fourneron, J.; Kolb, J. Hyperforin inhibits MMP-9 secretion by B-CLL cells and microtubule formation by endothelial cells. Leukemia, 2006, 20(4), 583.
[102]
Wiechmann, K.; Müller, H.; Fischer, D.; Jauch, J.; Werz, O. The acylphloroglucinols hyperforin and myrtucommulone A cause mitochondrial dysfunctions in leukemic cells by direct interference with mitochondria. Apoptosis, 2015, 20(11), 1508-1517.
[103]
Barbosa, M.; Valentão, P.; Andrade, P.B. Bioactive compounds from macroalgae in the new millennium: Implications for neurodegenerative diseases. Mar. Drugs, 2014, 12(9), 4934-4972.
[104]
Catarino, M.D.; Silva, A.M.S.; Cardoso, S.M. Fucaceae: A source of bioactive phlorotannins. Int. J. Mol. Sci., 2017, 18(6), 1327.
[105]
Thomas, N.V.; Kim, S-K. Potential pharmacological applications of polyphenolic derivatives from marine brown algae. Environ. Toxicol. Pharmacol., 2011, 32(3), 325-335.
[106]
Corona, G.; Ji, Y.; Anegboonlap, P.; Hotchkiss, S.; Gill, C.; Yaqoob, P.; Spencer, J.P.; Rowland, I. Gastrointestinal modifications and bioavailability of brown seaweed phlorotannins and effects on inflammatory markers. Br. J. Nutr., 2016, 115(7), 1240-1253.
[107]
Pádua, D.; Rocha, E.; Gargiulo, D.; Ramos, A. Bioactive compounds from brown seaweeds: Phloroglucinol, fucoxanthin and fucoidan as promising therapeutic agents against breast cancer. Phytochem. Lett., 2015, 14, 91-98.
[108]
Ha, D.; Bing, S.J.; Cho, J.; Ahn, G.; Kim, D.S.; Al-Amin, M.; Park, S.J.; Jee, Y. Phloroglucinol protects small intestines of mice from ionizing radiation by regulating apoptosis-related molecules: A comparative immunohistochemical study. J. Histochem. Cytochem., 2013, 61(1), 63-74.
[109]
Kang, K.A.; Zhang, R.; Chae, S.; Lee, S.J.; Kim, J.; Kim, J.; Jeong, J.; Lee, J.; Shin, T.; Lee, N.H. Phloroglucinol (1, 3, 5-trihydroxybenzene) protects against ionizing radiation-induced cell damage through inhibition of oxidative stress in vitro and in vivo. Chem. Biol. Interact., 2010, 185(3), 215-226.
[110]
Moon, C.; Kim, S.H.; Kim, J.C.; Hyun, J.W.; Lee, N.H.; Park, J.W.; Shin, T. Protective effect of phlorotannin components phloroglucinol and eckol on radiation-induced intestinal injury in mice. Phytother. Res., 2008, 22(2), 238-242.
[111]
Kang, H.S.; Chung, H.Y.; Kim, J.Y.; Son, B.W.; Jung, H.A.; Choi, J.S. Inhibitory phlorotannins from the edible brown alga Ecklonia stolonifera on total reactive oxygen species (ROS) generation. Arch. Pharm. Res., 2004, 27(2), 194-198.
[112]
Zou, Y.; Qian, Z-J.; Li, Y.; Kim, M-M.; Lee, S-H.; Kim, S-K. Antioxidant effects of phlorotannins isolated from Ishige okamurae in free radical mediated oxidative systems. J. Agric. Food Chem., 2008, 56(16), 7001-7009.
[113]
Nwosu, F.; Morris, J.; Lund, V.A.; Stewart, D.; Ross, H.A.; McDougall, G.J. Anti-proliferative and potential anti-diabetic effects of phenolic-rich extracts from edible marine algae. Food Chem., 2011, 126(3), 1006-1012.
[114]
Yoon, J.S.; Kasin Yadunandam, A.; Kim, S.J.; Woo, H.C.; Kim, H.R.; Kim, G.D. Dieckol, isolated from Ecklonia stolonifera, induces apoptosis in human hepatocellular carcinoma Hep3B cells. J. Nat. Med., 2013, 67(3), 519-527.
[115]
Ahn, J.H.; Yang, Y.I.; Lee, K.T.; Choi, J.H. Dieckol, isolated from the edible brown algae Ecklonia cava, induces apoptosis of ovarian cancer cells and inhibits tumor xenograft growth. J. Cancer Res. Clin. Oncol., 2015, 141(2), 255-268.
[116]
Hostanska, K.; Reichling, J.; Bommer, S.; Weber, M.; Saller, R. Hyperforin a constituent of St John’s wort (Hypericum perforatum L.) extract induces apoptosis by triggering activation of caspases and with hypericin synergistically exerts cytotoxicity towards human malignant cell lines. Eur. J. Pharm. Biopharm., 2003, 56(1), 121-132.
[117]
Zaher, M.; Tang, R.; Bombarda, I.; Merhi, F.; Bauvois, B.; Billard, C. Hyperforin induces apoptosis of chronic lymphocytic leukemia cells through upregulation of the BH3-only protein Noxa. Int. J. Oncol., 2012, 40(1), 269-276.
[118]
Yamamoto, K.; Ishikawa, C.; Katano, H.; Yasumoto, T.; Mori, N. Fucoxanthin and its deacetylated product, fucoxanthinol, induce apoptosis of primary effusion lymphomas. Cancer Lett., 2011, 300(2), 225-234.
[119]
Quiney, C.; Billard, C.; Faussat, A-M.; Salanoubat, C.; Kolb, J-P. Hyperforin inhibits P-gp and BCRP activities in chronic lymphocytic leukaemia cells and myeloid cells. Leuk. Lymphoma, 2007, 48(8), 1587-1599.
[120]
Liu, C.L.; Lim, Y.P.; Hu, M.L. Fucoxanthin attenuates rifampin-induced cytochrome P450 3A4 (CYP3A4) and multiple drug resistance 1 (MDR1) gene expression through pregnane X receptor (PXR)-mediated pathways in human hepatoma HepG2 and colon adenocarcinoma LS174T cells. Mar. Drugs, 2012, 10(1), 242-257.
[121]
Eid, S.Y.; El-Readi, M.Z.; Wink, M. Carotenoids reverse multidrug resistance in cancer cells by interfering with ABC-transporters. Phytomedicine, 2012, 19(11), 977-987.
[122]
Lardo, M.; Castro, M.; Moiraghi, B.; Rojas, F.; Borda, N.; Rey, J.A.; Lazarowski, A. MDR1/ABCB1 gene polymorphisms in patients with chronic myeloid leukemia. Blood Res., 2015, 50(3), 154-159.
[123]
Lin, L.C.; Yeh, C.T.; Kuo, C.C.; Lee, C.M.; Yen, G.C.; Wang, L.S.; Wu, C.H.; Yang, W.C.; Wu, A.T. Sulforaphane potentiates the efficacy of imatinib against chronic leukemia cancer stem cells through enhanced abrogation of Wnt/beta-catenin function. J. Agric. Food Chem., 2012, 60(28), 7031-7039.
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