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Anti-Cancer Agents in Medicinal Chemistry

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

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Review Article

Effects of Berberine on Leukemia with a Focus on Its Molecular Targets

Author(s): Mohammad Reza Mazandaranian, Parisa Maleki Dana, Zatollah Asemi, Jamal Hallajzadeh*, Mohammad Ali Mansournia and Bahman Yousefi

Volume 22, Issue 15, 2022

Published on: 12 May, 2022

Page: [2766 - 2774] Pages: 9

DOI: 10.2174/1871520622666220324092302

Price: $65

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Abstract

Leukemia is common among both women and men worldwide. Besides the fact that finding new treatment methods may enhance the life quality of patients, there are several problems that we face today in treating leukemia patients, such as drugs’ side effects and acquired resistance to chemotherapeutic drugs. Berberine is a bioactive alkaloid found in herbal plants (e.g., Rhizoma coptidis and Cortex phellodendri) and exerts several beneficial functions, including anti-tumor activities. Furthermore, berberine exerts antiproliferative and anti-inflammatory effects. Up to now, some studies have investigated the roles of berberine in different types of leukemia, including acute myeloid leukemia and chronic lymphocytic leukemia. In this review, a detailed description of the roles of berberine in leukemia is provided. We discuss how berberine involves different molecular targets (e.g., interleukins and cyclins) and signaling pathways (e.g., mTOR and PI3K) to exert its anti-tumor functions and how berberine is effective in leukemia treatment when combined with other therapeutic drugs.

Keywords: Berberine, leukemia, apoptosis, proliferation, autophagy, inflammation.

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[1]
Lin, C.C.; Ng, L.T.; Hsu, F.F.; Shieh, D.E.; Chiang, L.C. Cytotoxic effects of Coptis chinensis and Epimedium sagittatum extracts and their major constituents (berberine, coptisine and icariin) on hepatoma and leukaemia cell growth. Clin. Exp. Pharmacol. Physiol., 2004, 31(1-2), 65-69.
[http://dx.doi.org/10.1111/j.1440-1681.2004.03951.x] [PMID: 14756686]
[2]
Zheng, Y.; Feng, W.; Wang, Y.J.; Sun, Y.; Shi, G.; Yu, Q. Galectins as potential emerging key targets in different types of leukemia. Eur. J. Pharmacol., 2019, 844, 73-78.
[http://dx.doi.org/10.1016/j.ejphar.2018.11.019] [PMID: 30452910]
[3]
Panagal, M. S R, S.K.; P, S.; M, B.; M, K.; Gopinathe, V.; Sivakumare, P.; Sekar, D. MicroRNA21 and the various types of myeloid leu-kemia. Cancer Gene Ther., 2018, 25(7-8), 161-166.
[http://dx.doi.org/10.1038/s41417-018-0025-2] [PMID: 29795410]
[4]
Aladag, E.; Haznedaroğlu, İ.C. Current perspectives for the treatment of chronic myeloid leukemia. 2019, 49(1), 1-10.
[http://dx.doi.org/10.3906/sag-1810-81] [PMID: 30761815]
[5]
Bazargan, A.; Tam, C.S.; Keating, M.J. Predicting survival in chronic lymphocytic leukemia. Expert Rev. Anticancer Ther., 2012, 12(3), 393-403.
[http://dx.doi.org/10.1586/era.12.2] [PMID: 22369330]
[6]
Ilhan, G.; Karakus, S.; Andic, N. Risk factors and primary prevention of acute leukemia. Asian Pac. J. Cancer Prev., 2006, 7(4), 515-517.
[PMID: 17250419]
[7]
Heck, J.E.; Park, A.S.; Qiu, J.; Cockburn, M.; Ritz, B. Risk of leukemia in relation to exposure to ambient air toxics in pregnancy and early childhood. Int. J. Hyg. Environ. Health, 2014, 217(6), 662-668.
[http://dx.doi.org/10.1016/j.ijheh.2013.12.003] [PMID: 24472648]
[8]
Bispo, J.A.B.; Pinheiro, P.S.; Kobetz, E.K. Epidemiology and etiology of leukemia and Lymphoma. Cold Spring Harb. Perspect. Med., 2020, 10(6), a034819.
[http://dx.doi.org/10.1101/cshperspect.a034819] [PMID: 31727680]
[9]
Rautenberg, C.; Germing, U.; Haas, R.; Kobbe, G.; Schroeder, T. Relapse of acute myeloid leukemia after allogeneic stem cell transplanta-tion: Prevention, detection, and treatment. Int. J. Mol. Sci., 2019, 20(1), 228.
[http://dx.doi.org/10.3390/ijms20010228] [PMID: 30626126]
[10]
Ayati, S.H.; Fazeli, B.; Momtazi-Borojeni, A.A.; Cicero, A.F.G.; Pirro, M.; Sahebkar, A. Regulatory effects of berberine on microRNome in cancer and other conditions. Crit. Rev. Oncol. Hematol., 2017, 116, 147-158.
[http://dx.doi.org/10.1016/j.critrevonc.2017.05.008] [PMID: 28693796]
[11]
Sun, Y.; Xun, K.; Wang, Y.; Chen, X. A systematic review of the anticancer properties of berberine, a natural product from Chinese herbs. Anticancer Drugs, 2009, 20(9), 757-769.
[http://dx.doi.org/10.1097/CAD.0b013e328330d95b] [PMID: 19704371]
[12]
Zhao, Y.; Wang, Y.; Ma, S. Racial differences in four leukemia subtypes: Comprehensive descriptive epidemiology. Sci. Rep., 2018, 8(1), 548.
[http://dx.doi.org/10.1038/s41598-017-19081-4] [PMID: 29323237]
[13]
Chen, L.S.; Balakrishnan, K.; Gandhi, V. Inflammation and survival pathways: Chronic lymphocytic leukemia as a model system. Biochem. Pharmacol., 2010, 80(12), 1936-1945.
[http://dx.doi.org/10.1016/j.bcp.2010.07.039] [PMID: 20696142]
[14]
Jabbour, E.; O’Brien, S.; Konopleva, M.; Kantarjian, H. New insights into the pathophysiology and therapy of adult acute lymphoblastic leukemia. Cancer, 2015, 121(15), 2517-2528.
[http://dx.doi.org/10.1002/cncr.29383] [PMID: 25891003]
[15]
De Kouchkovsky, I.; Abdul-Hay, M. Acute myeloid leukemia: A comprehensive review and 2016 update. Blood Cancer J., 2016, 6(7), e441-e441.
[http://dx.doi.org/10.1038/bcj.2016.50] [PMID: 27367478]
[16]
Talati, C.; Sweet, K. Recently approved therapies in acute myeloid leukemia: A complex treatment landscape. Leuk. Res., 2018, 73, 58-66.
[http://dx.doi.org/10.1016/j.leukres.2018.09.001] [PMID: 30223250]
[17]
Finn, L.; Dalovisio, A.; Foran, J. Older patients with acute myeloid leukemia: Treatment challenges and future directions. Ochsner J., 2017, 17(4), 398-404.
[PMID: 29230125]
[18]
Mendoza-Nunez, V.M.; Garcia-Martinez, B.I. The effect of 600 mg alpha-lipoic acid supplementation on oxidative stress, inflammation, and RAGE in older adults with type 2 diabetes mellitus. 2019, 2019, 3276958.
[http://dx.doi.org/10.1155/2019/3276958]
[19]
Hole, P.S.; Darley, R.L.; Tonks, A. Do reactive oxygen species play a role in myeloid leukemias? Blood, 2011, 117(22), 5816-5826.
[http://dx.doi.org/10.1182/blood-2011-01-326025] [PMID: 21398578]
[20]
Rani, V.; Deep, G.; Singh, R.K.; Palle, K.; Yadav, U.C. Oxidative stress and metabolic disorders: Pathogenesis and therapeutic strategies. Life Sci., 2016, 148, 183-193.
[http://dx.doi.org/10.1016/j.lfs.2016.02.002] [PMID: 26851532]
[21]
Samimi, A.; Kalantari, H.; Lorestani, M.Z.; Shirzad, R.; Saki, N. Oxidative stress in normal hematopoietic stem cells and leukemia. APMIS, 2018, 126(4), 284-294.
[http://dx.doi.org/10.1111/apm.12822] [PMID: 29575200]
[22]
Martindale, J.L.; Holbrook, N.J. Cellular response to oxidative stress: Signaling for suicide and survival. J. Cell. Physiol., 2002, 192(1), 1-15.
[http://dx.doi.org/10.1002/jcp.10119] [PMID: 12115731]
[23]
Ariffin, H.; Azanan, M.S.; Abd Ghafar, S.S.; Oh, L.; Lau, K.H.; Thirunavakarasu, T.; Sedan, A.; Ibrahim, K.; Chan, A.; Chin, T.F.; Liew, F.F.; Jeyamogan, S.; Rosli, E.S.; Baharudin, R.; Yap, T.Y.; Skinner, R.; Lum, S.H.; Hainaut, P. Young adult survivors of childhood acute lymphoblastic leukemia show evidence of chronic inflammation and cellular aging. Cancer, 2017, 123(21), 4207-4214.
[http://dx.doi.org/10.1002/cncr.30857] [PMID: 28654149]
[24]
Binder, S.; Luciano, M.; Horejs-Hoeck, J. The cytokine network in acute myeloid leukemia (AML): A focus on pro- and anti-inflammatory mediators. Cytokine Growth Factor Rev., 2018, 43, 8-15.
[http://dx.doi.org/10.1016/j.cytogfr.2018.08.004] [PMID: 30181021]
[25]
Hu, S.; Chen, C.W.; Chen, S.T.; Tsui, K.H.; Tang, T.K.; Cheng, H.T.; Hwang, G.S.; Yu, J.W.; Li, Y.C.; Wang, P.S.; Wang, S.W. Inhibitory effect of berberine on interleukin-2 secretion from PHA-treated lymphocytic Jurkat cells. Int. Immunopharmacol., 2019, 66, 267-273.
[http://dx.doi.org/10.1016/j.intimp.2018.11.020] [PMID: 30502647]
[26]
Milata, V.; Svedova, A.; Barbierikova, Z.; Holubkova, E.; Cipakova, I.; Cholujova, D.; Jakubikova, J.; Panik, M.; Jantova, S.; Brezova, V.; Cipak, L. Synthesis and anticancer activity of novel 9-O-substituted berberine derivatives. Int. J. Mol. Sci., 2019, 20(9), E2169.
[http://dx.doi.org/10.3390/ijms20092169] [PMID: 31052469]
[27]
Liu, D.; Meng, X.; Wu, D.; Qiu, Z.; Luo, H. A natural isoquinoline alkaloid with antitumor activity: Studies of the biological activities of berberine. Front. Pharmacol., 2019, 10, 9.
[http://dx.doi.org/10.3389/fphar.2019.00009] [PMID: 30837865]
[28]
Cicero, A.F.; Baggioni, A. Berberine and its role in chronic disease. Adv. Exp. Med. Biol., 2016, 928, 27-45.
[http://dx.doi.org/10.1007/978-3-319-41334-1_2] [PMID: 27671811]
[29]
Iizuka, N.; Miyamoto, K.; Okita, K.; Tangoku, A.; Hayashi, H.; Yosino, S.; Abe, T.; Morioka, T.; Hazama, S.; Oka, M. Inhibitory effect of Coptidis Rhizoma and berberine on the proliferation of human esophageal cancer cell lines. Cancer Lett., 2000, 148(1), 19-25.
[http://dx.doi.org/10.1016/S0304-3835(99)00264-5] [PMID: 10680588]
[30]
Kong, W.; Wei, J.; Abidi, P.; Lin, M.; Inaba, S.; Li, C.; Wang, Y.; Wang, Z.; Si, S.; Pan, H.; Wang, S.; Wu, J.; Wang, Y.; Li, Z.; Liu, J.; Jiang, J.D. Berberine is a novel cholesterol-lowering drug working through a unique mechanism distinct from statins. Nat. Med., 2004, 10(12), 1344-1351.
[http://dx.doi.org/10.1038/nm1135] [PMID: 15531889]
[31]
Xue, M.; Yang, M.X.; Zhang, W.; Li, X.M.; Gao, D.H.; Ou, Z.M.; Li, Z.P.; Liu, S.H.; Li, X.J.; Yang, S.Y. Characterization, pharmacokinet-ics, and hypoglycemic effect of berberine loaded solid lipid nanoparticles. Int. J. Nanomedicine, 2013, 8, 4677-4687.
[http://dx.doi.org/10.2147/IJN.S51262] [PMID: 24353417]
[32]
Mirhadi, E.; Rezaee, M.; Malaekeh-Nikouei, B. Nano strategies for berberine delivery, a natural alkaloid of Berberis. Biomed. Pharmacother., 2018, 104, 465-473.
[http://dx.doi.org/10.1016/j.biopha.2018.05.067] [PMID: 29793179]
[33]
Kumar, A. Ekavali; Chopra, K.; Mukherjee, M.; Pottabathini, R.; Dhull, D.K. Current knowledge and pharmacological profile of berber-ine: An update. Eur. J. Pharmacol., 2015, 761, 288-297.
[http://dx.doi.org/10.1016/j.ejphar.2015.05.068] [PMID: 26092760]
[34]
Hu, X.; Zhang, Y.; Xue, Y.; Zhang, Z.; Wang, J. Berberine is a potential therapeutic agent for metabolic syndrome via brown adipose tissue activation and metabolism regulation. Am. J. Transl. Res., 2018, 10(11), 3322-3329.
[PMID: 30662589]
[35]
Feng, X.; Sureda, A.; Jafari, S.; Memariani, Z.; Tewari, D.; Annunziata, G.; Barrea, L.; Hassan, S.T.S.; Šmejkal, K.; Malaník, M.; Sychrová, A.; Barreca, D.; Ziberna, L.; Mahomoodally, M.F.; Zengin, G.; Xu, S.; Nabavi, S.M.; Shen, A.Z. Berberine in cardiovascular and metabolic diseases: From mechanisms to therapeutics. Theranostics, 2019, 9(7), 1923-1951.
[http://dx.doi.org/10.7150/thno.30787] [PMID: 31037148]
[36]
Imenshahidi, M.; Hosseinzadeh, H. Berberine and barberry (Berberis vulgaris): A clinical review. Phytother. Res., 2019, 33(3), 504-523.
[http://dx.doi.org/10.1002/ptr.6252] [PMID: 30637820]
[37]
Zou, K.; Li, Z.; Zhang, Y.; Zhang, H.Y.; Li, B.; Zhu, W.L.; Shi, J.Y.; Jia, Q.; Li, Y.M. Advances in the study of berberine and its deriva-tives: A focus on anti-inflammatory and anti-tumor effects in the digestive system. Acta Pharmacol. Sin., 2017, 38(2), 157-167.
[http://dx.doi.org/10.1038/aps.2016.125] [PMID: 27917872]
[38]
Li, N.; Gu, L.; Qu, L.; Gong, J.; Li, Q.; Zhu, W.; Li, J. Berberine attenuates pro-inflammatory cytokine-induced tight junction disruption in an in vitro model of intestinal epithelial cells. Eur. J. Pharm. Sci., 2010, 40(1), 1-8.
[http://dx.doi.org/10.1016/j.ejps.2010.02.001] [PMID: 20149867]
[39]
Gu, L.; Li, N.; Gong, J.; Li, Q.; Zhu, W.; Li, J. Berberine ameliorates intestinal epithelial tight-junction damage and down-regulates myosin light chain kinase pathways in a mouse model of endotoxinemia. J. Infect. Dis., 2011, 203(11), 1602-1612.
[http://dx.doi.org/10.1093/infdis/jir147] [PMID: 21592990]
[40]
Tew, X.N.; Xin Lau, N.J.; Chellappan, D.K.; Madheswaran, T.; Zeeshan, F.; Tambuwala, M.M.; Aljabali, A.A.; Balusamy, S.R.; Perumal-samy, H.; Gupta, G.; Oliver, B.G.; Hsu, A.; Wark, P.; Reddy, K.; Wadhwa, R.; Hansbro, P.M.; Dua, K. Immunological axis of berberine in managing inflammation underlying chronic respiratory inflammatory diseases. Chem. Biol. Interact., 2020, 317, 108947.
[http://dx.doi.org/10.1016/j.cbi.2020.108947] [PMID: 31968208]
[41]
Lu, Z.; He, B.; Chen, Z.; Yan, M.; Wu, L. Anti-inflammatory activity of berberine in non-alcoholic fatty liver disease via the Angptl2 pathway. BMC Immunol., 2020, 21(1), 28.
[http://dx.doi.org/10.1186/s12865-020-00358-9] [PMID: 32429849]
[42]
Eissa, L.A.; Kenawy, H.I.; El-Karef, A.; Elsherbiny, N.M.; El-Mihi, K.A. Antioxidant and anti-inflammatory activities of berberine attenu-ate hepatic fibrosis induced by thioacetamide injection in rats. Chem. Biol. Interact., 2018, 294, 91-100.
[http://dx.doi.org/10.1016/j.cbi.2018.08.016] [PMID: 30138605]
[43]
Li, Z.; Jiang, T.; Lu, Q.; Xu, K.; He, J.; Xie, L.; Chen, Z.; Zheng, Z.; Ye, L.; Xu, K.; Zhang, H.; Hu, A. Berberine attenuated the cytotoxicity induced by t-BHP via inhibiting oxidative stress and mitochondria dysfunction in PC-12 cells. Cell. Mol. Neurobiol., 2020, 40(4), 587-602.
[http://dx.doi.org/10.1007/s10571-019-00756-7] [PMID: 31828466]
[44]
Dkhil, M.A.; Metwaly, M.S.; Al-Quraishy, S. Berberine improves the intestinal antioxidant status of laboratory mice, Mus musculus. Saudi J. Biol. Sci., 2017, 24(7), 1567-1573.
[http://dx.doi.org/10.1016/j.sjbs.2015.10.012] [PMID: 30294226]
[45]
Zhuang, W.; Li, T.; Wang, C.; Shi, X.; Li, Y.; Zhang, S.; Zhao, Z.; Dong, H.; Qiao, Y. Berberine exerts antioxidant effects via protection of spiral ganglion cells against cytomegalovirus-induced apoptosis. Free Radic. Biol. Med., 2018, 121, 127-135.
[http://dx.doi.org/10.1016/j.freeradbiomed.2018.04.575] [PMID: 29715550]
[46]
Zhang, C.; Sheng, J.; Li, G.; Zhao, L.; Wang, Y.; Yang, W.; Yao, X.; Sun, L.; Zhang, Z.; Cui, R. Effects of berberine and its derivatives on cancer: A systems pharmacology review. Front. Pharmacol., 2020, 10, 1461-1461.
[http://dx.doi.org/10.3389/fphar.2019.01461] [PMID: 32009943]
[47]
Muller, P.A.; Vousden, K.H. p53 mutations in cancer. Nat. Cell Biol., 2013, 15(1), 2-8.
[http://dx.doi.org/10.1038/ncb2641] [PMID: 23263379]
[48]
Bieging, K.T.; Mello, S.S.; Attardi, L.D. Unravelling mechanisms of p53-mediated tumour suppression. Nat. Rev. Cancer, 2014, 14(5), 359-370.
[http://dx.doi.org/10.1038/nrc3711] [PMID: 24739573]
[49]
Prokocimer, M.; Molchadsky, A.; Rotter, V. Dysfunctional diversity of p53 proteins in adult acute myeloid leukemia: Projections on diag-nostic workup and therapy. Blood, 2017, 130(6), 699-712.
[http://dx.doi.org/10.1182/blood-2017-02-763086] [PMID: 28607134]
[50]
Eischen, C.M.; Lozano, G. p53 and MDM2: Antagonists or partners in crime? Cancer Cell, 2009, 15(3), 161-162.
[http://dx.doi.org/10.1016/j.ccr.2009.02.004] [PMID: 19249672]
[51]
Van Maerken, T.; Rihani, A.; Van Goethem, A.; De Paepe, A.; Speleman, F.; Vandesompele, J. Pharmacologic activation of wild-type p53 by nutlin therapy in childhood cancer. Cancer Lett., 2014, 344(2), 157-165.
[http://dx.doi.org/10.1016/j.canlet.2013.11.002] [PMID: 24262662]
[52]
Trino, S.; De Luca, L.; Laurenzana, I.; Caivano, A.; Del Vecchio, L.; Martinelli, G.; Musto, P. P53-MDM2 pathway: Evidences for a new targeted therapeutic approach in B-acute lymphoblastic leukemia. Front. Pharmacol., 2016, 7, 491.
[http://dx.doi.org/10.3389/fphar.2016.00491] [PMID: 28018226]
[53]
Liu, J.; Zhu, Z.; Liu, Y.; Wei, L.; Li, B.; Mao, F.; Zhang, J.; Wang, Y.; Liu, Y. MDM2 inhibition-mediated autophagy contributes to the pro-apoptotic effect of berberine in p53-null leukemic cells. Life Sci., 2020, 242, 117228.
[http://dx.doi.org/10.1016/j.lfs.2019.117228] [PMID: 31881227]
[54]
Liu, J.; Zhang, X.; Liu, A.; Liu, S.; Zhang, L.; Wu, B.; Hu, Q. Berberine induces apoptosis in p53-null leukemia cells by down-regulating XIAP at the post-transcriptional level. Cell. Physiol. Biochem., 2013, 32(5), 1213-1224.
[http://dx.doi.org/10.1159/000354520] [PMID: 24335171]
[55]
Zhang, X.; Gu, L.; Li, J.; Shah, N.; He, J.; Yang, L.; Hu, Q.; Zhou, M. Degradation of MDM2 by the interaction between berberine and DAXX leads to potent apoptosis in MDM2-overexpressing cancer cells. Cancer Res., 2010, 70(23), 9895-9904.
[http://dx.doi.org/10.1158/0008-5472.CAN-10-1546] [PMID: 20935220]
[56]
Kapelko-Słowik, K.; Urbaniak-Kujda, D.; Wołowiec, D.; Jaźwiec, B.; Dybko, J.; Jakubaszko, J.; Słowik, M.; Kuliczkowski, K. Expression of PIM-2 and NF-κB genes is increased in patients with acute myeloid leukemia (AML) and acute lymphoblastic leukemia (ALL) and is associated with complete remission rate and overall survival. Postepy Hig. Med. Dosw., 2013, 67, 553-559.
[http://dx.doi.org/10.5604/17322693.1052449] [PMID: 23752607]
[57]
Fox, C.J.; Hammerman, P.S.; Cinalli, R.M.; Master, S.R.; Chodosh, L.A.; Thompson, C.B. The serine/threonine kinase Pim-2 is a tran-scriptionally regulated apoptotic inhibitor. Genes Dev., 2003, 17(15), 1841-1854.
[http://dx.doi.org/10.1101/gad.1105003] [PMID: 12869584]
[58]
Liu, Z.; Liu, H.; Yuan, X.; Wang, Y.; Li, L.; Wang, G.; Song, J.; Shao, Z.; Fu, R. Downregulation of Pim-2 induces cell cycle arrest in the G0/G1 phase via the p53-non-dependent p21 signaling pathway. Oncol. Lett., 2018, 15(4), 4079-4086.
[http://dx.doi.org/10.3892/ol.2018.7865] [PMID: 29541172]
[59]
Wang, Y.; Liu, Y.; Du, X.; Ma, H.; Yao, J. The anti-cancer mechanisms of berberine: A review. Cancer Manag. Res., 2020, 12, 695-702.
[http://dx.doi.org/10.2147/CMAR.S242329] [PMID: 32099466]
[60]
Stagno, F.; Stella, S.; Spitaleri, A.; Pennisi, M.S.; Di Raimondo, F.; Vigneri, P. Imatinib mesylate in chronic myeloid leukemia: Frontline treatment and long-term outcomes. Expert Rev. Anticancer Ther., 2016, 16(3), 273-278.
[http://dx.doi.org/10.1586/14737140.2016.1151356] [PMID: 26852913]
[61]
Valent, P. Imatinib-resistant chronic myeloid leukemia (CML): Current concepts on pathogenesis and new emerging pharmacologic ap-proaches. Biologics, 2007, 1(4), 433-448.
[PMID: 19707313]
[62]
Yin, Z.; Huang, G.; Gu, C.; Liu, Y.; Yang, J.; Fei, J. Discovery of berberine that targetedly induce autophagic degradation of both BCR-ABL and BCR-ABL T315I through recruiting LRSAM1 for overcoming imatinib-resistance. Clin. Cancer Res., 2020, 26(15), 4040-4053.
[http://dx.doi.org/10.1158/1078-0432.CCR-19-2460]
[63]
Ly, M.; Rentas, S.; Vujovic, A.; Wong, N.; Moreira, S.; Xu, J.; Holzapfel, N.; Bhatia, S.; Tran, D.; Minden, M.D.; Draper, J.S.; Hope, K.J. Diminished AHR signaling drives human acute myeloid leukemia stem cell maintenance. Cancer Res., 2019, 79(22), 5799-5811.
[http://dx.doi.org/10.1158/0008-5472.CAN-19-0274] [PMID: 31519687]
[64]
Gentil, M.; Hugues, P.; Desterke, C.; Telliam, G.; Sloma, I.; Souza, L.E.B.; Baykal, S.; Artus, J.; Griscelli, F.; Guerci, A.; Johnson-Ansah, H.; Foudi, A.; Bennaceur-Griscelli, A.; Turhan, A.G. Aryl hydrocarbon receptor (AHR) is a novel druggable pathway controlling malignant progenitor proliferation in chronic myeloid leukemia (CML). PLoS One, 2018, 13(8), e0200923.
[http://dx.doi.org/10.1371/journal.pone.0200923] [PMID: 30091999]
[65]
Mohammadi, S.; Seyedhoseini, F.S.; Asadi, J.; Yazdani, Y. Effects of berberine on the secretion of cytokines and expression of genes involved in cell cycle regulation in THP-1 monocytic cell line. Iran. J. Basic Med. Sci., 2017, 20(5), 530-537.
[PMID: 28656088]
[66]
Wang, L.; Chen, B.; Lin, M.; Cao, Y.; Chen, Y.; Chen, X.; Liu, T.; Hu, J. Decreased expression of nucleophosmin/B23 increases drug sensitivity of adriamycin-resistant Molt-4 leukemia cells through mdr-1 regulation and Akt/mTOR signaling. Immunobiology, 2015, 220(3), 331-340.
[http://dx.doi.org/10.1016/j.imbio.2014.10.015] [PMID: 25457413]
[67]
Zhang, M.J.; Ding, Y.L.; Xu, C.W.; Yang, Y.; Lian, W.X.; Zhan, Y.Q.; Li, W.; Xu, W.X.; Yu, M.; Ge, C.H.; Ning, H.M.; Li, C.Y.; Yang, X.M. Erythroid differentiation-associated gene interacts with NPM1 (nucleophosmin/B23) and increases its protein stability, resisting cell apoptosis. FEBS J., 2012, 279(16), 2848-2862.
[http://dx.doi.org/10.1111/j.1742-4658.2012.08663.x] [PMID: 22712502]
[68]
Wu, H.L.; Hsu, C.Y.; Liu, W.H.; Yung, B.Y. Berberine-induced apoptosis of human leukemia HL-60 cells is associated with down-regulation of nucleophosmin/B23 and telomerase activity. Int. J. Cancer, 1999, 81(6), 923-929.
[http://dx.doi.org/10.1002/(SICI)1097-0215(19990611)81:6<923:AID-IJC14>3.0.CO;2-D] [PMID: 10362140]
[69]
Fu, S.; Ni, S.; Wang, D.; Fu, M.; Hong, T. Berberine suppresses mast cell-mediated allergic responses via regulating FcɛRI-mediated and MAPK signaling. Int. Immunopharmacol., 2019, 71, 1-6.
[http://dx.doi.org/10.1016/j.intimp.2019.02.041] [PMID: 30861392]
[70]
Lin, C.C.; Lin, S.Y.; Chung, J.G.; Lin, J.P.; Chen, G.W.; Kao, S.T. Down-regulation of cyclin B1 and up-regulation of wee1 by berberine promotes entry of leukemia cells into the G2/M-phase of the cell cycle. Anticancer Res., 2006, 26(2A), 1097-1104.
[PMID: 16619512]
[71]
He, Z.W.; Zhao, X.Y.; Xu, R.Z.; Wu, D. Effects of berbamine on growth of leukemia cell line NB4 and its mechanism. Zhejiang Da Xue Xue Bao Yi Xue Ban, 2006, 35(2), 209-214.
[PMID: 16610091]
[72]
Diab, S.; Fidanzi, C.; Léger, D.Y.; Ghezali, L.; Millot, M.; Martin, F.; Azar, R.; Esseily, F.; Saab, A.; Sol, V.; Diab-Assaf, M.; Liagre, B. Berberis libanotica extract targets NF-κB/COX-2, PI3K/Akt and mitochondrial/caspase signalling to induce human erythroleukemia cell apoptosis. Int. J. Oncol., 2015, 47(1), 220-230.
[http://dx.doi.org/10.3892/ijo.2015.3012] [PMID: 25997834]
[73]
Okubo, S.; Uto, T.; Goto, A.; Tanaka, H.; Nishioku, T.; Yamada, K.; Shoyama, Y. Berberine induces apoptotic cell death via activation of caspase-3 and -8 in HL-60 human leukemia cells: Nuclear localization and structure-activity relationships. Am. J. Chin. Med., 2017, 45(7), 1497-1511.
[http://dx.doi.org/10.1142/S0192415X17500811] [PMID: 29025293]
[74]
Li, H.; Guo, L.; Jie, S.; Liu, W.; Zhu, J.; Du, W.; Fan, L.; Wang, X.; Fu, B.; Huang, S. Berberine inhibits SDF-1-induced AML cells and leukemic stem cells migration via regulation of SDF-1 level in bone marrow stromal cells. Biomed. Pharmacother., 2008, 62(9), 573-578.
[http://dx.doi.org/10.1016/j.biopha.2008.08.003] [PMID: 18805669]
[75]
Lin, C.C.; Kao, S.T.; Chen, G.W.; Ho, H.C.; Chung, J.G. Apoptosis of human leukemia HL-60 cells and murine leukemia WEHI-3 cells induced by berberine through the activation of caspase-3. Anticancer Res., 2006, 26(1A), 227-242.
[PMID: 16475703]
[76]
Chung, J.G.; Chen, G.W.; Hung, C.F.; Lee, J.H.; Ho, C.C.; Ho, H.C.; Chang, H.L.; Lin, W.C.; Lin, J.G. Effects of berberine on arylamine N-acetyltransferase activity and 2-aminofluorene-DNA adduct formation in human leukemia cells. Am. J. Chin. Med., 2000, 28(2), 227-238.
[http://dx.doi.org/10.1142/S0192415X00000271] [PMID: 10999441]
[77]
Lin, S.S.; Chung, J.G.; Lin, J.P.; Chuang, J.Y.; Chang, W.C.; Wu, J.Y.; Tyan, Y.S. Berberine inhibits arylamine N-acetyltransferase activity and gene expression in mouse leukemia L 1210 cells. Phytomedicine, 2005, 12(5), 351-358.
[http://dx.doi.org/10.1016/j.phymed.2003.11.008] [PMID: 15957369]
[78]
Lin, C.C.; Kao, S.T.; Chen, G.W.; Chung, J.G. Berberine decreased N-acetylation of 2-aminofluorene through inhibition of N-acetyltransferase gene expression in human leukemia HL-60 cells. Anticancer Res., 2005, 25(6B), 4149-4155.
[PMID: 16309210]
[79]
Lu, Y-C.; Lin, Q.; Luo, G-S.; Dai, Y-Y. Solubility of berberine chloride in various solvents. J. Chem. Eng. Data, 2006, 51(2), 642-644.
[http://dx.doi.org/10.1021/je0504360]
[80]
Ge, L.; Bao, A.; Yang, K. Determination and correlation of the solubility for berberine chloride in pure imidazolium-based ionic liquids. J. Chem. Eng. Data, 2016, 61(5), 1829-1835.
[http://dx.doi.org/10.1021/acs.jced.5b01017]
[81]
Zhu, X.; Sun, Y.; Zhang, C.; Liu, H. Effects of berberine on a rat model of chronic stress and depression via gastrointestinal tract patholo-gy and gastrointestinal flora profile assays. Mol. Med. Rep., 2017, 15(5), 3161-3171.
[http://dx.doi.org/10.3892/mmr.2017.6353] [PMID: 28339024]
[82]
Xiao, D.; Liu, Z.; Zhang, S.; Zhou, M.; He, F.; Zou, M.; Peng, J.; Xie, X.; Liu, Y.; Peng, D. Berberine derivatives with different pharmaco-logical activities via structural modifications. Mini Rev. Med. Chem., 2018, 18(17), 1424-1441.
[http://dx.doi.org/10.2174/1389557517666170321103139] [PMID: 28325147]
[83]
Sagar, B. In-vitro production of berberine in cultures of Berberis aristataand pharmacological investigation for anti-hepatotoxic activity: 145. J. Pharm. Pharmacol., 2006, 58.
[84]
Guamán Ortiz, L.M.; Tillhon, M.; Parks, M.; Dutto, I.; Prosperi, E.; Savio, M.; Arcamone, A.G.; Buzzetti, F.; Lombardi, P.; Scovassi, A.I. Multiple effects of berberine derivatives on colon cancer cells. BioMed Res. Int., 2014, 2014, 924585.
[http://dx.doi.org/10.1155/2014/924585] [PMID: 25045712]
[85]
Park, K.D.; Lee, J.H.; Kim, S.H.; Kang, T.H.; Moon, J.S.; Kim, S.U. Synthesis of 13-(substituted benzyl) berberine and berberrubine de-rivatives as antifungal agents. Bioorg. Med. Chem. Lett., 2006, 16(15), 3913-3916.
[http://dx.doi.org/10.1016/j.bmcl.2006.05.033] [PMID: 16730982]
[86]
Huang, L.; Luo, Z.; He, F.; Shi, A.; Qin, F.; Li, X. Berberine derivatives, with substituted amino groups linked at the 9-position, as inhibi-tors of acetylcholinesterase/butyrylcholinesterase. Bioorg. Med. Chem. Lett., 2010, 20(22), 6649-6652.
[http://dx.doi.org/10.1016/j.bmcl.2010.09.013] [PMID: 20880702]
[87]
Cui, J.S.; Xu, F.; Pang, J.Y.; Chen, W.H.; Jiang, Z.H. Synthesis and DNA-binding affinities of protoberberine-based multivalent agents. Chem. Biodivers., 2010, 7(12), 2908-2916.
[http://dx.doi.org/10.1002/cbdv.200900386] [PMID: 21162004]
[88]
Pang, J.Y.; Long, Y.H.; Chen, W.H.; Jiang, Z.H. Amplification of DNA-binding affinities of protoberberine alkaloids by appended polyam-ines. Bioorg. Med. Chem. Lett., 2007, 17(4), 1018-1021.
[http://dx.doi.org/10.1016/j.bmcl.2006.11.037] [PMID: 17127054]
[89]
Pang, J.Y.; Qin, Y.; Chen, W.H.; Luo, G.A.; Jiang, Z.H. Synthesis and DNA-binding affinities of monomodified berberines. Bioorg. Med. Chem., 2005, 13(20), 5835-5840.
[http://dx.doi.org/10.1016/j.bmc.2005.05.048] [PMID: 15993616]
[90]
Krishnan, P.; Bastow, K.F. The 9-position in berberine analogs is an important determinant of DNA topoisomerase II inhibition. Anticancer Drug Des., 2000, 15(4), 255-264.
[PMID: 11200501]
[91]
Iwasa, K.; Kamigauchi, M.; Ueki, M.; Taniguchi, M. Antibacterial activity and structure-activity relationships of berberine analogs. Eur. J. Med. Chem., 1996, 31(6), 469-478.
[http://dx.doi.org/10.1016/0223-5234(96)85167-1]
[92]
Inoue, K.; Kulsum, U.; Chowdhury, S.A.; Fujisawa, S.; Ishihara, M.; Yokoe, I.; Sakagami, H. Tumor-specific cytotoxicity and apoptosis-inducing activity of berberines. Anticancer Res., 2005, 25(6B), 4053-4059.
[PMID: 16309199]
[93]
Tang, P.; Cheng, W.; He, X.; Zhang, Q.; Zhong, J.; Lu, X.; Liu, S.; Zhong, L. Raman spectrum spectral imaging revealing the molecular mechanism of berberine-induced Jurkat cell apoptosis and the receptor-mediated berberine delivery system. Biomed. Opt. Express, 2019, 10(4), 1581-1600.
[http://dx.doi.org/10.1364/BOE.10.001581] [PMID: 31061758]
[94]
Jin, L.; Liao, H.J.; Zhang, M.Y.; Liu, Q.Y.; Wang, Y.F. Effect of berberine on the differentiation and apoptosis of K562 cell line. Zhong Yao Cai, 2009, 32(3), 384-388.
[PMID: 19565717]
[95]
Pazhang, Y.; Ahmadian, S.; Mahmoudian, M.; Shafiezadeh, M. Berberine-induced apoptosis via decreasing the survivin protein in K562 cell line. Med. Oncol., 2011, 28(4), 1577-1583.
[http://dx.doi.org/10.1007/s12032-010-9586-0] [PMID: 20517657]
[96]
Ma, Y.; Ou, T.M.; Tan, J.H.; Hou, J.Q.; Huang, S.L.; Gu, L.Q.; Huang, Z.S. Quinolino-benzo-[5, 6]-dihydroisoquindolium compounds derived from berberine: A new class of highly selective ligands for G-quadruplex DNA in c-myc oncogene. Eur. J. Med. Chem., 2011, 46(5), 1906-1913.
[http://dx.doi.org/10.1016/j.ejmech.2011.02.020] [PMID: 21392861]
[97]
Jantová, S.; Cipák, L.; Cernáková, M.; Kost’álová, D. Effect of berberine on proliferation, cell cycle and apoptosis in HeLa and L1210 cells. J. Pharm. Pharmacol., 2003, 55(8), 1143-1149.
[http://dx.doi.org/10.1211/002235703322277186] [PMID: 12956905]
[98]
Yu, F.S.; Yang, J.S.; Lin, H.J.; Yu, C.S.; Tan, T.W.; Lin, Y.T.; Lin, C.C.; Lu, H.F.; Chung, J.G. Berberine inhibits WEHI-3 leukemia cells in vivo. In Vivo, 2007, 21(2), 407-412.
[PMID: 17436595]
[99]
Kuo, C.L.; Chou, C.C.; Yung, B.Y. Berberine complexes with DNA in the berberine-induced apoptosis in human leukemic HL-60 cells. Cancer Lett., 1995, 93(2), 193-200.
[http://dx.doi.org/10.1016/0304-3835(95)03809-B] [PMID: 7621428]
[100]
Kettmann, V.; Kosfálová, D.; Jantová, S.; Cernáková, M.; Drímal, J. In vitro cytotoxicity of berberine against HeLa and L1210 cancer cell lines. Pharmazie, 2004, 59(7), 548-551.
[PMID: 15296093]
[101]
Liu, J.; Liu, P.; Xu, T.; Chen, Z.; Kong, H.; Chu, W.; Wang, Y.; Liu, Y. Berberine induces autophagic cell death in acute lymphoblastic leukemia by inactivating AKT/mTORC1 signaling. Drug Des. Devel. Ther., 2020, 14, 1813-1823.
[http://dx.doi.org/10.2147/DDDT.S239247] [PMID: 32494123]
[102]
Yin, Z.; Huang, G.; Gu, C.; Liu, Y.; Yang, J.; Fei, J. Discovery of berberine that targetedly induces autophagic degradation of both BCR-ABL and BCR-ABL T315I through recruiting LRSAM1 for overcoming imatinib resistance. Clin. Cancer Res., 2020, 26(15), 4040-4053.
[http://dx.doi.org/10.1158/1078-0432.CCR-19-2460] [PMID: 32098768]

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