A rohitukine derivative IIIM-290 induces p53 dependent mitochondrial apoptosis in acute lymphoblastic leukemia cells.

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Abstrakt

Tytuł:: A rohitukine derivative IIIM-290 induces p53 dependent mitochondrial apoptosis in acute lymphoblastic leukemia cells.
Autorzy:: Mintoo M; Cancer Pharmacology Division, CSIR-Indian Institute of Integrative Medicine, Jammu, India.; Academy of Scientific and Innovative Research (AcSIR), Ghaziabad, India.
Khan S; Cancer Pharmacology Division, CSIR-Indian Institute of Integrative Medicine, Jammu, India.; Academy of Scientific and Innovative Research (AcSIR), Ghaziabad, India.
Wani A; Cancer Pharmacology Division, CSIR-Indian Institute of Integrative Medicine, Jammu, India.; Academy of Scientific and Innovative Research (AcSIR), Ghaziabad, India.
Malik S; Cancer Pharmacology Division, CSIR-Indian Institute of Integrative Medicine, Jammu, India.; Academy of Scientific and Innovative Research (AcSIR), Ghaziabad, India.
Bhurta D; Medicinal Chemistry Division, CSIR-Indian Institute of Integrative Medicine, Jammu, India.; Academy of Scientific and Innovative Research (AcSIR), Ghaziabad, India.
Bharate S; Medicinal Chemistry Division, CSIR-Indian Institute of Integrative Medicine, Jammu, India.; Academy of Scientific and Innovative Research (AcSIR), Ghaziabad, India.
Malik F; Cancer Pharmacology Division, CSIR-Indian Institute of Integrative Medicine, Jammu, India.; Academy of Scientific and Innovative Research (AcSIR), Ghaziabad, India.
Mondhe D; Cancer Pharmacology Division, CSIR-Indian Institute of Integrative Medicine, Jammu, India.; Academy of Scientific and Innovative Research (AcSIR), Ghaziabad, India.
Źródło:: Molecular carcinogenesis [Mol Carcinog] 2021 Oct; Vol. 60 (10), pp. 671-683. Date of Electronic Publication: 2021 Jul 29.
Typ publikacji:: Journal Article; Research Support, Non-U.S. Gov't
Język:: English
Imprint Name(s):: Publication: <2005- > : [Hoboken, N.J.] : Wiley-Liss
Original Publication: New York : Alan R. Liss, Inc., c1988-
MeSH Terms:: Antineoplastic Agents, Phytogenic/*pharmacology
Apoptosis/*drug effects
Chromones/*pharmacology
Mitochondria/*drug effects
Mitochondria/*metabolism
Piperidines/*pharmacology
Precursor Cell Lymphoblastic Leukemia-Lymphoma/*metabolism
Animals ; Apoptosis Regulatory Proteins/genetics ; Apoptosis Regulatory Proteins/metabolism ; Cell Line, Tumor ; Chromones/chemistry ; Disease Models, Animal ; Gene Expression Regulation, Neoplastic ; Humans ; Mice ; Piperidines/chemistry ; Precursor Cell Lymphoblastic Leukemia-Lymphoma/genetics ; Tumor Suppressor Protein p53/metabolism ; Xenograft Model Antitumor Assays
References:: Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68(6):394-424.
Bhojwani D, Yang JJ, Pui C-H. Biology of childhood acute lymphoblastic leukemia. Pediatric Clinics. 2015;62(1):47-60.
Li Y, Zhu R, Mi L, Cao Y, Yao D. Segmentation of white blood cell from acute lymphoblastic leukemia images using dual-threshold method. Comput Math Methods Med. 2016;2016:2016.
Groves F, Linet M, Devesa S. Patterns of occurrence of the leukaemias. Eur J Cancer. 1995;31(6):941-949.
Wartenberg D, Groves FD, Adelman AS. Acute lymphoblastic leukemia: epidemiology and etiology. Acute Leukemias. Springer. 2008;77-93.
Malumbres M, Barbacid M. Milestones in cell division: to cycle or not to cycle: a critical decision in cancer. Nat Rev Cancer. 2001;1(3):222-231.
Shapiro GI. Cyclin-dependent kinase pathways as targets for cancer treatment. J Clin Oncol. 2006;24(11):1770-1783.
Toogood PL, Harvey PJ, Repine JT, et al. Discovery of a potent and selective inhibitor of cyclin-dependent kinase 4/6. J Med Chem. 2005;48(7):2388-2406.
McClue SJ, Blake D, Clarke R, et al. In vitro and in vivo antitumor properties of the cyclin dependent kinase inhibitor CYC202 (R-roscovitine). Int J Cancer. 2002;102(5):463-468.
Besson A, Dowdy SF, Roberts JM. CDK inhibitors: cell cycle regulators and beyond. Dev Cell. 2008;14(2):159-169.
Burki TK. Palbociclib improves survival in advanced breast cancer. Lancet Oncol. 2017;18(1):e1.
Zerdes I, Ziogas DE, Lykoudis EG, Roukos DH. Palbociclib: an approval at last for HER2-negative breast cancer. Future Med. 2016;12:1097-1100.
Sledge GW Jr., Toi M, Neven P, et al. MONARCH 2: abemaciclib in combination with fulvestrant in women with HR+/HER2-advanced breast cancer who had progressed while receiving endocrine therapy. J Clin Oncol. 2017;35(25):2875-2884.
Torres-Guzmán R, Calsina B, Hermoso A, et al. Preclinical characterization of abemaciclib in hormone receptor positive breast cancer. Oncotarget. 2017;8(41):69493-69507.
Moharram SA, Shah K, Khanum F, Marhäll A, Gazi M, Kazi JU. Efficacy of the CDK inhibitor dinaciclib in vitro and in vivo in T-cell acute lymphoblastic leukemia. Cancer Lett. 2017;405:73-78.
Pikman Y, Alexe G, Roti G, et al. Synergistic drug combinations with a CDK4/6 inhibitor in t-cell acute lymphoblastic leukemia. Clin Cancer Res. 2017;23(4):1012-1024.
Rivlin N, Brosh R, Oren M, Rotter V. Mutations in the p53 tumor suppressor gene: important milestones at the various steps of tumorigenesis. Genes Cancer. 2011;2(4):466-474.
Lanza C, Gaidano G, Cimino G, et al. p53 gene inactivation in acute lymphoblastic leukemia of B cell lineage associates with chromosomal breakpoints at 11q23 and 8q24. Leukemia. 1995;9(6):955-959.
Marks DI, Kurz BW, Link MP, et al. High incidence of potential p53 inactivation in poor outcome childhood acute lymphoblastic leukemia at diagnosis. Blood. 1996;87(3):1155-1161.
Wu J, Liang Y, Tan Y, et al. CDK9 inhibitors reactivate p53 by downregulating iASPP. Cell Signall. 2020;67:109508.
Štětková M, Growková K, Fojtík P, et al. CDK9 activity is critical for maintaining MDM4 overexpression in tumor cells. Cell Death Dis. 2020;11(9):754.
Demidenko ZN, Blagosklonny MV. Flavopiridol induces p53 via initial inhibition of Mdm2 and p21 and, independently of p53, sensitizes apoptosis-reluctant cells to tumor necrosis factor. Cancer Res. 2004;64(10):3653-3660.
Bharate SB, Kumar V, Jain SK, et al. Discovery and preclinical development of IIIM-290, an orally active potent cyclin-dependent kinase inhibitor. J Med Chem. 2018;61(4):1664-1687.
Mahajan V, Sharma N, Kumar S, et al. Production of rohitukine in leaves and seeds of Dysoxylum binectariferum: an alternate renewable resource. Pharm Biol. 2015;53(3):446-450.
Hussain A, Qazi AK, Mupparapu N, et al. A novel PI3K axis selective molecule exhibits potent tumor inhibition in colorectal carcinogenesis. Mol Carcinog. 2016;55(12):2135-2155.
Kumar A, Singh B, Mahajan G, et al. A novel colchicine-based microtubule inhibitor exhibits potent antitumor activity by inducing mitochondrial mediated apoptosis in MIA PaCa-2 pancreatic cancer cells. Tumor Biol. 2016;37(10):13121-13136.
Wani A, Gupta M, Ahmad M, et al. Alborixin clears amyloid-β by inducing autophagy through PTEN-mediated inhibition of the AKT pathway. Autophagy. 2019;15:1-19.
Yu Z, Li W. Induction of apoptosis by puerarin in colon cancer HT-29 cells. Cancer Lett. 2006;238(1):53-60.
Kumar A, Singh B, Sharma PR, Bharate SB, Saxena AK, Mondhe D. A novel microtubule depolymerizing colchicine analogue triggers apoptosis and autophagy in HCT-116 colon cancer cells. Cell Biochem Funct. 2016;34(2):69-81.
Majeed R, Hamid A, Sangwan PL, et al. Inhibition of phosphotidylinositol-3 kinase pathway by a novel naphthol derivative of betulinic acid induces cell cycle arrest and apoptosis in cancer cells of different origin. Cell Death Dis. 2014;5(10):e1459.
Bhushan S, Kumar A, Malik F, et al. A triterpenediol from Boswellia serrata induces apoptosis through both the intrinsic and extrinsic apoptotic pathways in human leukemia HL-60 cells. Apoptosis. 2007;12(10):1911-1926.
Shankar S, Faheem MM, Nayak D, et al. Cyclodipeptide c(Orn-Pro) conjugate with 4-ethylpiperic acid abrogates cancer cell metastasis through modulating MDM2. Bioconjug Chem. 2018;29(1):164-175.
Orrenius S, Zhivotovsky B, Nicotera P. Regulation of cell death: the calcium-apoptosis link. Nat Rev Mol Cell Biol. 2003;4(7):552-565.
Tummers B, Green DR. Caspase-8: regulating life and death. Immunol Rev. 2017;277(1):76-89.
Andreyev AY, Kushnareva YE, Starkov A. Mitochondrial metabolism of reactive oxygen species. Biochemistry. 2005;70(2):200-214.
Zhao R-Z, Jiang S, Zhang L, Yu Z-B. Mitochondrial electron transport chain, ROS generation and uncoupling (Review). Int J Mol Med. 2019;44(1):3-15.
Lustgarten MS, Bhattacharya A, Muller FL, et al. Complex I generated, mitochondrial matrix-directed superoxide is released from the mitochondria through voltage dependent anion channels. Biochem Biophys Res Commun. 2012;422(3):515-521.
Muller FL, Liu Y, VanRemmen, H. Complex III releases superoxide to both sides of the inner mitochondrial membrane. J Biol Chem. 2004;279(47):49064-49073.
Mnatsakanyan N, Beutner G, Porter GA, Alavian KN, Jonas EA. Physiological roles of the mitochondrial permeability transition pore. J Bioenerg Biomembr. 2017;49(1):13-25.
Zorov DB, Juhaszova M, Sollott SJ. Mitochondrial reactive oxygen species (ROS) and ROS-induced ROS release. Physiol Rev. 2014;94(3):909-950.
Toufektchan E, Toledo F. The guardian of the genome revisited: p53 downregulates genes required for telomere maintenance, DNA repair, and centromere structure. Cancers. 2018;10(5):135.
Harris SL, Levine AJ. The p53 pathway: positive and negative feedback loops. Oncogene. 2005;24(17):2899-2908.
Cortes JE, Kantarjian HM. Acute lymphoblastic leukemia a comprehensive review with emphasis on biology and therapy. Cancer. 1995;76(12):2393-2417.
Mohseni M, Uludag H, Brandwein JM. Advances in biology of acute lymphoblastic leukemia (ALL) and therapeutic implications. Am J Blood Res. 2018;8(4):29-56.
Rowe JM, Buck G, Burnett AK, et al. Induction therapy for adults with acute lymphoblastic leukemia: results of more than 1500 patients from the international ALL trial: MRC UKALL XII/ECOG E2993. Blood. 2005;106(12):3760-3767.
Sive JI, Buck G, Fielding A, et al. Outcomes in older adults with acute lymphoblastic leukaemia (ALL): results from the international MRC UKALL XII/ECOG 2993 trial. Br J Haematol. 2012;157(4):463-471.
Thomas DA, O'Brien S, Faderl S, et al. Chemoimmunotherapy with a modified Hyper-CVAD and Rituximab regimen improves outcome in de novo Philadelphia chromosome-negative precursor B-lineage acute lymphoblastic leukemia. J Clin Oncol. 2010;28(24):3880-3889.
Szatrowski TP, Nathan CF. Production of large amounts of hydrogen peroxide by human tumor cells. Cancer Res. 1991;51(3):794-798.
Gorrini C, Harris IS, Mak TW. Modulation of oxidative stress as an anticancer strategy. Nat Rev Drug Discovery. 2013;12(12):931-947.
Trachootham D, Alexandre J, Huang P. Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach? Nat Rev Drug Discovery. 2009;8(7):579-591.
Kruman I, Guo Q, Mattson MP. Calcium and reactive oxygen species mediate staurosporine-induced mitochondrial dysfunction and apoptosis in PC12 cells. J Neurosci Res. 1998;51(3):293-308.
Lynch K, Fernandez G, Pappalardo A, Peluso J. Basic fibroblast growth factor inhibits apoptosis of spontaneously immortalized granulosa cells by regulating intracellular free calcium levels through a protein kinase Cδ-dependent pathway. Endocrinology. 2000;141(11):4209-4217.
Tombal B, Denmeade S, Isaacs J. Assessment and validation of a microinjection method for kinetic analysis of [Ca2+] i in individual cells undergoing apoptosis. Cell Calcium. 1999;25(1):19-28.
Brooks CL, Gu W. p53 ubiquitination: Mdm2 and beyond. Mol Cell. 2006;21(3):307-315.
Contributed Indexing:: Keywords: CDK-9; L1210; MOLT-4; P388; apoptosis
Substance Nomenclature:: 0 (5,7-dihydroxy-2-methyl-8-(4-(3-hydroxy-1-methyl)-piperidinyl)-4H-1-benzopyran-4-one)
0 (Antineoplastic Agents, Phytogenic)
0 (Apoptosis Regulatory Proteins)
0 (Chromones)
0 (Piperidines)
0 (Tumor Suppressor Protein p53)
Entry Date(s):: Date Created: 20210729 Date Completed: 20210927 Latest Revision: 20210927
Update Code:: 20240105
DOI:: 10.1002/mc.23332
PMID:: 34324743
: Czasopismo naukowe

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Rohitukine, a chromone alkaloid extracted from Dysoxylum binectariferum, has a propitious anticancer activity. Our previous study shows that a new Rohitukine derivative IIIM-290 restricts the growth of pancreatic cancer in vivo and in vitro. In the present findings, we report the mechanism of cell death induced by IIIM-290 in MOLT-4 cells (acute lymphoblastic leukemia) and its anticancer potential against various murine leukemic tumor models in vivo. We found that IIIM-290 induced apoptosis through upregulation of different apoptotic proteins like PUMA, BAX, cytochrome c, cleaved (active) caspase-3, and cleaved PARP in MOLT-4 cells. Moreover, IIIM-290 abated mitochondrial membrane potential, elevated calcium levels, reactive oxygen species, and arrested growth of MOLT-4 cells in the synthesis (S) phase of the cell cycle. Interestingly, the elevation in proapoptotic markers was p53 dependent-the silencing of p53 abrogated apoptosis (programmed cell death) triggered by IIIM-290 in MOLT-4 cells. Furthermore, IIIM-290 significantly enhanced the survival of animals with P388 and L1210 leukemia. Thus, our results put IIIM-290 as a potential candidate for the anticancer lead.
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