Phospholipase C beta1 (PI-PLCbeta1)/Cyclin D3/protein kinase C (PKC) alpha signaling modulation during iron-induced oxidative stress in myelodysplastic syndromes (MDS).
Aged
Blood Transfusion
/ statistics & numerical data
Cyclin D3
/ genetics
Deferasirox
/ pharmacology
Female
Gene Expression Regulation
Humans
Iron
/ adverse effects
Iron Chelating Agents
/ pharmacology
Iron Overload
/ complications
Male
Middle Aged
Myelodysplastic Syndromes
/ pathology
Oxidative Stress
/ drug effects
Phospholipase C beta
/ genetics
Phosphorylation
Protein Kinase C-alpha
/ genetics
Signal Transduction
deferasirox
inositides
reactive oxygen species
Journal
FASEB journal : official publication of the Federation of American Societies for Experimental Biology
ISSN: 1530-6860
Titre abrégé: FASEB J
Pays: United States
ID NLM: 8804484
Informations de publication
Date de publication:
11 2020
11 2020
Historique:
received:
22
04
2020
revised:
31
08
2020
accepted:
09
09
2020
pubmed:
23
9
2020
medline:
28
4
2021
entrez:
22
9
2020
Statut:
ppublish
Résumé
MDS are characterized by anemia and transfusion requirements. Transfused patients frequently show iron overload that negatively affects hematopoiesis. Iron chelation therapy can be effective in these MDS cases, but the molecular consequences of this treatment need to be further investigated. That is why we studied the molecular features of iron effect and Deferasirox therapy on PI-PLCbeta1 inositide signaling, using hematopoietic cells and MDS samples. At baseline, MDS patients showing a positive response after iron chelation therapy displayed higher levels of PI-PLCbeta1/Cyclin D3/PKCalpha expression. During treatment, these responder patients, as well as hematopoietic cells treated with FeCl
Identifiants
pubmed: 32959428
doi: 10.1096/fj.202000933RR
doi:
Substances chimiques
CCND3 protein, human
0
Cyclin D3
0
Iron Chelating Agents
0
Iron
E1UOL152H7
PRKCA protein, human
EC 2.7.11.13
Protein Kinase C-alpha
EC 2.7.11.13
PLCB1 protein, human
EC 3.1.4.11
Phospholipase C beta
EC 3.1.4.11
Deferasirox
V8G4MOF2V9
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
15400-15416Informations de copyright
© 2020 The Authors. The FASEB Journal published by Wiley Periodicals LLC on behalf of Federation of American Societies for Experimental Biology.
Références
Manzoli L, Billi AM, Gilmour RS, et al. Phosphoinositide signaling in nuclei of Friend cells: tiazofurin down-regulates phospholipase C beta 1. Cancer Res. 1995;55:2978-2980.
Ratti S, Ramazzotti G, Faenza I, et al. Nuclear inositide signaling and cell cycle. Adv Biol Regul. 2018;67:1-6.
Faenza I, Bavelloni A, Fiume R, et al. Up-regulation of nuclear PLCbeta1 in myogenic differentiation. J Cell Physiol. 2003;195:446-452.
Faenza I, Billi AM, Follo MY, et al. Nuclear phospholipase C signaling through type 1 IGF receptor and its involvement in cell growth and differentiation. Anticancer Res. 2005;25:2039-2041.
Follo MY, Mongiorgi S, Finelli C, et al. Nuclear inositide signaling in myelodysplastic syndromes. J Cell Biochem. 2010;109:1065-1071.
Ramazzotti G, Faenza I, Fiume R, et al. The physiology and pathology of inositide signaling in the nucleus. J Cell Physiol. 2011;226:14-20.
Poli A, Fiume R, Baldanzi G, et al. Nuclear localization of diacylglycerol kinase alpha in K562 cells is involved in cell cycle progression. J Cell Physiol. 2017;232:2550-2557.
Poli A, Mongiorgi S, Cocco L, Follo MY. Protein kinase C involvement in cell cycle modulation. Biochem Soc Trans. 2014;42:1471-1476.
Ratti S, Mongiorgi S, Ramazzotti G, et al. Nuclear inositide signaling via phospholipase C. J Cell Biochem. 2017;118:1969-1978.
Ratti S, Follo MY, Ramazzotti G, et al. Nuclear phospholipase C isoenzyme imbalance leads to pathologies in brain, hematologic, neuromuscular, and fertility disorders. J Lipid Res. 2019;60:312-317.
Lo Vasco VR, Calabrese G, Manzoli L, et al. Inositide-specific phospholipase c beta1 gene deletion in the progression of myelodysplastic syndrome to acute myeloid leukemia. Leukemia. 2004;18:1122-1126.
Ratti S, Mongiorgi S, Rusciano I, Manzoli L, Follo MY. Glycogen Synthase Kinase-3 and phospholipase C-beta signalling: roles and possible interactions in myelodysplastic syndromes and acute myeloid leukemia. Biochim Biophys Acta Mol Cell Res. 2020;1867:118649.
Xian J, Owusu Obeng E, Ratti S, et al. Nuclear inositides and inositide-dependent signaling pathways in myelodysplastic syndromes. Cells. 2020;9:697.
Follo MY, Russo D, Finelli C, et al. Epigenetic regulation of nuclear PI-PLCbeta1 signaling pathway in low-risk MDS patients during azacitidine treatment. Leukemia. 2012;26:943-950.
Follo MY, Mongiorgi S, Clissa C, et al. Activation of nuclear inositide signalling pathways during erythropoietin therapy in low-risk MDS patients. Leukemia. 2012;26:2474-2482.
Follo MY, Finelli C, Mongiorgi S, et al. Synergistic induction of PI-PLCbeta1 signaling by azacitidine and valproic acid in high-risk myelodysplastic syndromes. Leukemia. 2011;25:271-280.
Poli A, Ratti S, Finelli C, et al. Nuclear translocation of PKC-alpha is associated with cell cycle arrest and erythroid differentiation in myelodysplastic syndromes (MDSs). FASEB J. 2018;32:681-692.
Forciniti S, Greco L, Grizzi F, Malesci A, Laghi L. Iron metabolism in cancer progression. Int J Mol Sci. 2020;21:2257.
Guida M, Maraldi T, Beretti F, Follo MY, Manzoli L, De Pol A. Nuclear Nox4-derived reactive oxygen species in myelodysplastic syndromes. Biomed Res Int. 2014;2014:456937.
Keune WJ, Jones DR, Divecha N. PtdIns5P and Pin1 in oxidative stress signaling. Adv Biol Regul. 2013;53:179-189.
Poli A, Zaurito AE, Abdul-Hamid S, Fiume R, Faenza I, Divecha N. Phosphatidylinositol 5 Phosphate (PI5P): from behind the scenes to the front (nuclear) stage. Int J Mol Sci. 2019;20:2080.
Suire S, Baltanas FC, Segonds-Pichon A, et al. Frontline science: TNF-alpha and GM-CSF1 priming augments the role of SOS1/2 in driving activation of Ras, PI3K-gamma, and neutrophil proinflammatory responses. J Leukoc Biol. 2019;106:815-822.
Leslie NR, Bennett D, Lindsay YE, Stewart H, Gray A, Downes CP. Redox regulation of PI 3-kinase signalling via inactivation of PTEN. EMBO J. 2003;22:5501-5510.
Casciaro F, Beretti F, Zavatti M, et al. Nuclear Nox4 interaction with prelamin A is associated with nuclear redox control of stem cell aging. Aging (Albany NY). 2018;10:2911-2934.
Zeitz MJ, Malyavantham KS, Seifert B, Berezney R. Matrin 3: chromosomal distribution and protein interactions. J Cell Biochem. 2009;108:125-133.
Jayavelu AK, Moloney JN, Böhmer FD, Cotter TG. NOX-driven ROS formation in cell transformation of FLT3-ITD-positive AML. Exp Hematol. 2016;44:1113-1122.
Song MG, Ryoo IG, Choi HY, et al. NRF2 signaling negatively regulates phorbol-12-myristate-13-acetate (PMA)-induced differentiation of human monocytic U937 cells into pro-inflammatory macrophages. PLoS One. 2015;10:e0134235.
Leitch HA, Gattermann N. Hematologic improvement with iron chelation therapy in myelodysplastic syndromes: Clinical data, potential mechanisms, and outstanding questions. Crit Rev Oncol Hematol. 2019;141:54-72.
Zuo Y, Xiang B, Yang J, et al. Oxidative modification of caspase-9 facilitates its activation via disulfide-mediated interaction with Apaf-1. Cell Res. 2009;19:449-457.
Hartmann J, Braulke F, Sinzig U, et al. Iron overload impairs proliferation of erythroid progenitors cells (BFU-E) from patients with myelodysplastic syndromes. Leuk Res. 2013;37:327-332.
Bowen D, Wang L, Frew M, Kerr R, Groves M. Antioxidant enzyme expression in myelodysplastic and acute myeloid leukemia bone marrow: further evidence of a pathogenetic role for oxidative stress? Haematologica. 2003;88:1070-1072.
Novotna B, Bagryantseva Y, Siskova M, Neuwirtova R. Oxidative DNA damage in bone marrow cells of patients with low-risk myelodysplastic syndrome. Leuk Res. 2009;33:340-343.
Ghoti H, Fibach E, Merkel D, Perez-Avraham G, Grisariu S, Rachmilewitz EA. Changes in parameters of oxidative stress and free iron biomarkers during treatment with deferasirox in iron-overloaded patients with myelodysplastic syndromes. Haematologica. 2010;95:1433-1434.
Angelucci E, Santini V, Di Tucci AA, et al. Deferasirox for transfusion-dependent patients with myelodysplastic syndromes: safety, efficacy, and beyond (GIMEMA MDS0306 Trial). Eur J Haematol. 2014;92:527-536.
Nolte F, Hochsmann B, Giagounidis A, et al. Results from a 1-year, open-label, single arm, multi-center trial evaluating the efficacy and safety of oral Deferasirox in patients diagnosed with low and int-1 risk myelodysplastic syndrome (MDS) and transfusion-dependent iron overload. Ann Hematol. 2013;92:191-198.
Gattermann N, Finelli C, Della Porta M, et al. Hematologic responses to deferasirox therapy in transfusion-dependent patients with myelodysplastic syndromes. Haematologica. 2012;97:1364-1371.
Messa E, Carturan S, Maffe C, et al. Deferasirox is a powerful NF-kappaB inhibitor in myelodysplastic cells and in leukemia cell lines acting independently from cell iron deprivation by chelation and reactive oxygen species scavenging. Haematologica. 2010;95:1308-1316.
Manzoli L, Mongiorgi S, Clissa C, et al. Strategic role of nuclear inositide signalling in myelodysplastic syndromes therapy. Mini Rev Med Chem. 2014;14:873-883.
Cermak J, Jonasova A, Vondrakova J, Cervinek L, Belohlavkova P, Neuwirtova R. A comparative study of deferasirox and deferiprone in the treatment of iron overload in patients with myelodysplastic syndromes. Leuk Res. 2013;37:1612-1615.
Harmening D, Baldwin AJ, Sohmer PR. Modern Blood Banking & Transfusion Practices. Philadelphia, PA: F.A. Davis; 1983.
Cappellini MD. Exjade(R) (deferasirox, ICL670) in the treatment of chronic iron overload associated with blood transfusion. Ther Clin Risk Manag. 2007;3:291-299.
Vardiman JW, Thiele J, Arber DA, et al. The 2008 revision of the World Health Organization (WHO) classification of myeloid neoplasms and acute leukemia: rationale and important changes. Blood. 2009;114:937-951.
Greenberg P, Cox C, LeBeau MM, et al. International scoring system for evaluating prognosis in myelodysplastic syndromes. Blood. 1997;89:2079-2088.
Cheson BD, Greenberg PL, Bennett JM, et al. Clinical application and proposal for modification of the International Working Group (IWG) response criteria in myelodysplasia. Blood. 2006;108:419-425.
Pellagatti A, Roy S, Di Genua C, et al. Targeted resequencing analysis of 31 genes commonly mutated in myeloid disorders in serial samples from myelodysplastic syndrome patients showing disease progression. Leukemia. 2016;30:247-250.
Follo MY, Pellagatti A, Armstrong RN, et al. Response of high-risk MDS to azacitidine and lenalidomide is impacted by baseline and acquired mutations in a cluster of three inositide-specific genes. Leukemia. 2019;33:2276-2290.
Cocco L, Finelli C, Mongiorgi S, et al. An increased expression of PI-PLCbeta1 is associated with myeloid differentiation and a longer response to azacitidine in myelodysplastic syndromes. J Leukoc Biol. 2015;98:769-780.
Chan S, Chan GC, Ye J, Lian Q, Chen J, Yang M. Thrombopoietin protects cardiomyocytes from iron-overload induced oxidative stress and mitochondrial injury. Cell Physiol Biochem. 2015;36:2063-2071.
Fabiani E, Calabrese C, Niscola P, et al. Mutational profile and haematological response to iron chelation in myelodysplastic syndromes (MDS). Br J Haematol. 2019;185:954-957.
Mongiorgi S, Finelli C, Yang YR, et al. Inositide-dependent signaling pathways as new therapeutic targets in myelodysplastic syndromes. Expert Opin Ther Targets. 2016;20:677-687.
Mongiorgi S, Follo MY, Yang YR, et al. Selective activation of nuclear PI-PLCbeta1 during normal and therapy-related differentiation. Curr Pharm Des. 2016;22:2345-2348.
Follo MY, Marmiroli S, Faenza I, et al. Nuclear phospholipase C beta1 signaling, epigenetics and treatments in MDS. Adv Biol Regul. 2013;53:2-7.
Tataranni T, Mazzoccoli C, Agriesti F, et al. Deferasirox drives ROS-mediated differentiation and induces interferon-stimulated gene expression in human healthy haematopoietic stem/progenitor cells and in leukemia cells. Stem Cell Res Ther. 2019;10:171.
Chen YL, Kan WM. Down-regulation of superoxide dismutase 1 by PMA is involved in cell fate determination and mediated via protein kinase D2 in myeloid leukemia cells. Biochim Biophys Acta. 2015;1853:2662-2675.
Nocka KH, Pelus LM. Cell cycle specific effects of deferoxamine on human and murine hematopoietic progenitor cells. Cancer Res. 1988;48:3571-3575.
Jiménez-Solas T, López-Cadenas F, Aires-Mejía I, et al. Deferasirox reduces oxidative DNA damage in bone marrow cells from myelodysplastic patients and improves their differentiation capacity. Br J Haematol. 2019;187:93-104.
Saigo K, Kono M, Takagi Y, et al. Deferasirox reduces oxidative stress in patients with transfusion dependency. J Clin Med Res. 2013;5:57-60.
Silva A, Gírio A, Cebola I, Santos CI, Antunes F, Barata JT. Intracellular reactive oxygen species are essential for PI3K/Akt/mTOR-dependent IL-7-mediated viability of T-cell acute lymphoblastic leukemia cells. Leukemia. 2011;25:960-967.
Garlanda C, Mantovani A. Ligands and receptors of the interleukin-1 family in immunity and disease. Front Immunol. 2013;4:396.
Gozali MV, Yi F, Zhang JA, et al. Photodynamic therapy inhibit fibroblast growth factor-10 induced keratinocyte differentiation and proliferation through ROS in fibroblast growth factor receptor-2b pathway. Sci Rep. 2016;6:27402.
Zhu G, Liu X, Fang Y, et al. Increased mTOR cancels out the effect of reduced Xbp-1 on antibody secretion in IL-1α-deficient B cells. Cell Immunol. 2018;328:9-17.
Kelly E, Won A, Refaeli Y, Van Parijs L. IL-2 and related cytokines can promote T cell survival by activating AKT. J Immunol. 2002;168:597-603.
Bae J, Park D, Lee YS, Jeoung D. Interleukin-2 promotes angiogenesis by activation of Akt and increase of ROS. J Microbiol Biotechnol. 2008;18:377-382.
Zhang J, Wang X, Vikash V, et al. ROS and ROS-mediated cellular signaling. Oxid Med Cell Longev. 2016;2016:4350965.