STIM2 is involved in the regulation of apoptosis and the cell cycle in normal and malignant monocytic cells.

SOCE apoptosis calcium genomic stress leukemia monocytic cells

Journal

Molecular oncology
ISSN: 1878-0261
Titre abrégé: Mol Oncol
Pays: United States
ID NLM: 101308230

Informations de publication

Date de publication:
17 Jan 2024
Historique:
revised: 28 11 2023
received: 27 09 2023
accepted: 02 01 2024
medline: 18 1 2024
pubmed: 18 1 2024
entrez: 18 1 2024
Statut: aheadofprint

Résumé

Calcium is a ubiquitous messenger that regulates a wide range of cellular functions, but its involvement in the pathophysiology of acute myeloid leukemia (AML) is not widely investigated. Here, we identified, from an analysis of The Cancer Genome Atlas and genotype-tissue expression databases, stromal interaction molecule 2 (STIM2) as being highly expressed in AML with monocytic differentiation and negatively correlated with overall survival. This was confirmed on a validation cohort of 407 AML patients. We then investigated the role of STIM2 in cell proliferation, differentiation, and survival in two leukemic cell lines with monocytic potential and in normal hematopoietic stem cells. STIM2 expression increased at the RNA and protein levels upon monocyte differentiation. Phenotypically, STIM2 knockdown drastically inhibited cell proliferation and induced genomic stress with DNA double-strand breaks, as shown by increased levels of phosphorylate histone H2AXγ (p-H2AXγ), followed by activation of the cellular tumor antigen p53 pathway, decreased expression of cell cycle regulators such as cyclin-dependent kinase 1 (CDK1)-cyclin B1 and M-phase inducer phosphatase 3 (CDC25c), and a decreased apoptosis threshold with a low antiapoptotic/proapoptotic protein ratio. Our study reports STIM2 as a new actor regulating genomic stability and p53 response in terms of cell cycle and apoptosis of human normal and malignant monocytic cells.

Identifiants

pubmed: 38234211
doi: 10.1002/1878-0261.13584
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Cent pour Sang la Vie Journée contre la Leucémie
Organisme : Journée contre la Leucémie
Organisme : La Ligue contre le Cancer Comité Septentrion

Informations de copyright

© 2024 The Authors. Molecular Oncology published by John Wiley & Sons Ltd on behalf of Federation of European Biochemical Societies.

Références

Acute myeloid leukemia treatment - NCI. 2023 [cited 2023 Jul 17]. Available from: https://www.cancer.gov/types/leukemia/patient/adult-aml-treatment-pdq
Ding L, Ley TJ, Larson DE, Miller CA, Koboldt DC, Welch JS, et al. Clonal evolution in relapsed acute myeloid leukaemia revealed by whole-genome sequencing. Nature. 2012;481(7382):506-510.
Li S, Mason C, Melnick A. Genetic and epigenetic heterogeneity in acute myeloid leukemia. Curr Opin Genet Dev. 2016;36:100-106.
Kantarjian HM, Kadia TM, DiNardo CD, Welch MA, Ravandi F. Acute myeloid leukemia: treatment and research outlook for 2021 and the MD Anderson approach. Cancer. 2021;127(8):1186-1207.
Humeau J, Bravo-San Pedro JM, Vitale I, Nuñez L, Villalobos C, Kroemer G, et al. Calcium signaling and cell cycle: progression or death. Cell Calcium. 2018;70:3-15.
Giorgio V, Guo L, Bassot C, Petronilli V, Bernardi P. Calcium and regulation of the mitochondrial permeability transition. Cell Calcium. 2018;70:56-63.
Pitts MW, Hoffmann PR. Endoplasmic reticulum-resident selenoproteins as regulators of calcium signaling and homeostasis. Cell Calcium. 2018;70:76-86.
Hennings H, Michael D, Cheng C, Steinert P, Holbrook K, Yuspa SH. Calcium regulation of growth and differentiation of mouse epidermal cells in culture. Cell. 1980;19(1):245-254.
Berridge MJ, Bootman MD, Roderick HL. Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol. 2003;4(7):517-529.
Bagur R, Hajnóczky G. Intracellular Ca2+ sensing: role in calcium homeostasis and signaling. Mol Cell. 2017;66(6):780-788.
Prakriya M, Lewis RS. Store-operated calcium channels. Physiol Rev. 2015;95(4):1383-1436.
Shen W-W, Frieden M, Demaurex N. Remodelling of the endoplasmic reticulum during store-operated calcium entry. Biol Cell. 2011;103(8):365-380.
Liou J, Kim ML, Heo WD, Jones JT, Myers JW, Ferrell JE, et al. STIM is a Ca2+ sensor essential for Ca2+−store-depletion-triggered Ca2+ influx. Curr Biol. 2005;15(13):1235-1241.
Roos J, DiGregorio PJ, Yeromin AV, Ohlsen K, Lioudyno M, Zhang S, et al. STIM1, an essential and conserved component of store-operated Ca2+ channel function. J Cell Biol. 2005;169(3):435-445.
Cahalan MD. STIMulating store-operated Ca(2+) entry. Nat Cell Biol. 2009;11(6):669-677.
Derler I, Jardin I, Romanin C. Molecular mechanisms of STIM/Orai communication. Am J Physiol Cell Physiol. 2016;310(8):C643-C662.
Yang S, Zhang JJ, Huang X-Y. Orai1 and STIM1 are critical for breast tumor cell migration and metastasis. Cancer Cell. 2009;15(2):124-134.
Schmidt S, Liu G, Liu G, Yang W, Honisch S, Pantelakos S, et al. Enhanced Orai1 and STIM1 expression as well as store operated Ca2+ entry in therapy resistant ovary carcinoma cells. Oncotarget. 2014;5(13):4799-4810.
Zhu H, Zhang H, Jin F, Fang M, Huang M, Yang CS, et al. Elevated Orai1 expression mediates tumor-promoting intracellular Ca2+ oscillations in human esophageal squamous cell carcinoma. Oncotarget. 2014;5(11):3455-3471.
Kim J-H, Lkhagvadorj S, Lee M-R, Hwang K-H, Chung HC, Jung JH, et al. Orai1 and STIM1 are critical for cell migration and proliferation of clear cell renal cell carcinoma. Biochem Biophys Res Commun. 2014;448(1):76-82.
Liu H, Jia X, Luo Z, Guan H, Jiang H, Li X, et al. Inhibition of store-operated Ca(2+) channels prevent ethanol-induced intracellular Ca(2+) increase and cell injury in a human hepatoma cell line. Toxicol Lett. 2012;208(3):254-261.
Zhang J, Wei J, Kanada M, Yan L, Zhang Z, Watanabe H, et al. Inhibition of store-operated Ca2+ entry suppresses EGF-induced migration and eliminates extravasation from vasculature in nasopharyngeal carcinoma cell. Cancer Lett. 2013;336(2):390-397.
Faouzi M, Kischel P, Hague F, Ahidouch A, Benzerdjeb N, Sevestre H, et al. ORAI3 silencing alters cell proliferation and cell cycle progression via c-myc pathway in breast cancer cells. Biochim Biophys Acta. 2013;1833(3):752-760.
Faouzi M, Hague F, Potier M, Ahidouch A, Sevestre H, Ouadid-Ahidouch H. Down-regulation of Orai3 arrests cell-cycle progression and induces apoptosis in breast cancer cells but not in normal breast epithelial cells. J Cell Physiol. 2011;226(2):542-551.
Dubois C, Vanden Abeele F, Lehen'kyi V, Gkika D, Guarmit B, Lepage G, et al. Remodeling of channel-forming ORAI proteins determines an oncogenic switch in prostate cancer. Cancer Cell. 2014;26(1):19-32.
Guitart AV, Finch AJ, Kranc KR. Ca2+tapulting HSCs into action. J Exp Med. 2018;215(8):1971-1973.
Paredes-Gamero EJ, Leon CMMP, Borojevic R, Oshiro MEM, Ferreira AT. Changes in intracellular Ca2+ levels induced by cytokines and P2 agonists differentially modulate proliferation or commitment with macrophage differentiation in murine hematopoietic cells. J Biol Chem. 2008;283(46):31909-31919.
Yen A, Freeman L, Powers V, Van Sant R, Fishbaugh J. Cell cycle dependence of calmodulin levels during HL-60 proliferation and myeloid differentiation. No changes during pre-commitment. Exp Cell Res. 1986;165(1):139-151.
Schuler AD, Si J, Mueller L, Simon JA, Collins SJ. KN-62 analogues as potent differentiating agents of HL-60 cells. Leuk Res. 2007;31(5):683-689.
Chen S, Bao L, Keefer K, Shanmughapriya S, Chen L, Lee J, et al. Transient receptor potential ion channel TRPM2 promotes AML proliferation and survival through modulation of mitochondrial function, ROS, and autophagy. Cell Death Dis. 2020;11(4):247.
Shi J, Fu L, Wang W. High expression of inositol 1,4,5-trisphosphate receptor, type 2 (ITPR2) as a novel biomarker for worse prognosis in cytogenetically normal acute myeloid leukemia. Oncotarget. 2015;6(7):5299-5309.
Diez-Bello R, Jardin I, Salido GM, Rosado JA. Orai1 and Orai2 mediate store-operated calcium entry that regulates HL60 cell migration and FAK phosphorylation. Biochim Biophys Acta Mol Cell Res. 2017;1864(6):1064-1070.
Lewuillon C, Guillemette A, Titah S, Shaik FA, Jouy N, Labiad O, et al. Involvement of ORAI1/SOCE in human AML cell lines and primary cells according to ABCB1 activity, LSC compartment and potential resistance to Ara-C exposure. Int J Mol Sci. 2022;23(10):5555.
Deng M, Zhang Q, Wu Z, Ma T, He A, Zhang T, et al. Mossy cell synaptic dysfunction causes memory imprecision via miR-128 inhibition of STIM2 in Alzheimer's disease mouse model. Aging Cell. 2020;19(5):e13144.
Vigont VA, Grekhnev DA, Lebedeva OS, Gusev KO, Volovikov EA, Skopin AY, et al. STIM2 mediates excessive store-operated calcium entry in patient-specific iPSC-derived neurons modeling a juvenile form of Huntington's disease. Front Cell Dev Biol. 2021;9:625231.
Saint Fleur-Lominy S, Maus M, Vaeth M, Lange I, Zee I, Suh D, et al. STIM1 and STIM2 mediate cancer-induced inflammation in T cell acute lymphoblastic leukemia. Cell Rep. 2018;24(11):3045-3060.e5.
Berna-Erro A, Braun A, Kraft R, Kleinschnitz C, Schuhmann MK, Stegner D, et al. STIM2 regulates capacitive Ca2+ entry in neurons and plays a key role in hypoxic neuronal cell death. Sci Signal. 2009;2(93):ra67.
Chanaday NL, Nosyreva E, Shin O-H, Zhang H, Aklan I, Atasoy D, et al. Presynaptic store-operated Ca2+ entry drives excitatory spontaneous neurotransmission and augments endoplasmic reticulum stress. Neuron. 2021;109(8):1314-1332.e5.
Clemens RA, Chong J, Grimes D, Hu Y, Lowell CA. STIM1 and STIM2 cooperatively regulate mouse neutrophil store-operated calcium entry and cytokine production. Blood. 2017;130(13):1565-1577.
Carralot J-P, Kim T-K, Lenseigne B, Boese AS, Sommer P, Genovesio A, et al. Automated high-throughput siRNA transfection in raw 264.7 macrophages: a case study for optimization procedure. SLAS Discov. 2009;14(2):151-160.
Döhner H, Estey E, Grimwade D, Amadori S, Appelbaum FR, Büchner T, et al. Diagnosis and management of AML in adults: 2017 ELN recommendations from an international expert panel. Blood. 2017;129(4):424-447.
Fenwarth L, Thomas X, de Botton S, Duployez N, Bourhis J-H, Lesieur A, et al. A personalized approach to guide allogeneic stem cell transplantation in younger adults with acute myeloid leukemia. Blood. 2021;137(4):524-532.
Kaplan EL, Meier P. Nonparametric estimation from incomplete observations. J Am Stat Assoc. 1958;53(282):457-481.
Grambsch PM, Therneau TM. Proportional hazards tests and diagnostics based on weighted residuals. Biometrika. 1994;81(3):515-526.
Fine JP, Gray RJ. A proportional hazards model for the subdistribution of a competing risk. J Am Stat Assoc. 1999;94(446):496-509.
Tang Z, Kang B, Li C, Chen T, Zhang Z. GEPIA2: an enhanced web server for large-scale expression profiling and interactive analysis. Nucleic Acids Res. 2019;47(W1):W556-W560.
Thomas X, de Botton S, Chevret S, Caillot D, Raffoux E, Lemasle E, et al. Randomized phase II study of clofarabine-based consolidation for younger adults with acute myeloid leukemia in first remission. J Clin Oncol. 2017;35(11):1223-1230.
Liu K, Zheng M, Lu R, Du J, Zhao Q, Li Z, et al. The role of CDC25C in cell cycle regulation and clinical cancer therapy: a systematic review. Cancer Cell Int. 2020;20(1):213.
St Clair S, Giono L, Varmeh-Ziaie S, Resnick-Silverman L, Liu W-J, Padi A, et al. DNA damage-induced downregulation of Cdc25C is mediated by p53 via two independent mechanisms: one involves direct binding to the cdc25C promoter. Mol Cell. 2004;16(5):725-736.
Ruano Y, Mollejo M, Ribalta T, Fiaño C, Camacho FI, Gómez E, et al. Identification of novel candidate target genes in amplicons of glioblastoma multiforme tumors detected by expression and CGH microarray profiling. Mol Cancer. 2006;5:39.
Aytes A, Molleví DG, Martinez-Iniesta M, Nadal M, Vidal A, Morales A, et al. Stromal interaction molecule 2 (STIM2) is frequently overexpressed in colorectal tumors and confers a tumor cell growth suppressor phenotype. Mol Carcinog. 2012;51(9):746-753.
Chen F-Q, Zheng H, Gu T, Hu Y-H, Yang L, Huang Z-P, et al. Modification of STIM2 by m 6 A RNA methylation inhibits metastasis of cholangiocarcinoma. Ann Transl Med. 2022;10(2):40.
Déliot N, Constantin B. Plasma membrane calcium channels in cancer: alterations and consequences for cell proliferation and migration. Biochim Biophys Acta. 2015;1848(10 Pt B):2512-2522.
Xie J, Pan H, Yao J, Zhou Y, Han W. SOCE and cancer: recent progress and new perspectives. Int J Cancer. 2016;138(9):2067-2077.
Li G, Zhang Z, Wang R, Ma W, Yang Y, Wei J, et al. Suppression of STIM1 inhibits human glioblastoma cell proliferation and induces G0/G1 phase arrest. J Exp Clin Cancer Res. 2013;32(1):20.
Zhan Z-Y, Zhong L-X, Feng M, Wang J-F, Liu D-B, Xiong J-P. Over-expression of Orai1 mediates cell proliferation and associates with poor prognosis in human non-small cell lung carcinoma. Int J Clin Exp Pathol. 2015;8(5):5080-5088.
Sun Y, Ye C, Tian W, Ye W, Gao Y-Y, Feng Y-D, et al. TRPC1 promotes the genesis and progression of colorectal cancer via activating CaM-mediated PI3K/AKT signaling axis. Oncogenesis. 2021;10(10):1-13.
Song MY, Makino A, Yuan JX-J. STIM2 contributes to enhanced store-operated Ca2+ entry in pulmonary artery smooth muscle cells from patients with idiopathic pulmonary arterial hypertension. Pulm Circ. 2011;1(1):84-94.
Abdullaev IF, Bisaillon JM, Potier M, Gonzalez JC, Motiani RK, Trebak M. Stim1 and Orai1 mediate CRAC currents and store-operated calcium entry important for endothelial cell proliferation. Circ Res. 2008;103(11):1289-1299.
Fisher D, Krasinska L, Coudreuse D, Novák B. Phosphorylation network dynamics in the control of cell cycle transitions. J Cell Sci. 2012;125(Pt 20):4703-4711.
Sur S, Agrawal DK. Phosphatases and kinases regulating CDC25 activity in the cell cycle: clinical implications of CDC25 overexpression and potential treatment strategies. Mol Cell Biochem. 2016;416(1-2):33-46.
Jeffy BD, Chen EJ, Gudas JM, Romagnolo DF. Disruption of cell cycle kinetics by benzo[a]pyrene: inverse expression patterns of BRCA-1 and p53 in MCF-7 cells arrested in S and G2. Neoplasia. 2000;2(5):460-470.
Fragkos M, Jurvansuu J, Beard P. H2AX is required for cell cycle arrest via the p53/p21 pathway. Mol Cell Biol. 2009;29(10):2828-2840.
Hsu J-W, Huang H-C, Chen S-T, Wong C-H, Juan H-F. Ganoderma lucidum polysaccharides induce macrophage-like differentiation in human leukemia THP-1 cells via caspase and p53 activation. Evid Based Complement Alternat Med. 2011;2011:358717.
Feng Z, Chen Q, Ren M, Tian Z, Gong Y. CD40L inhibits cell growth of THP-1 cells by suppressing the PI3K/Akt pathway. Onco Targets Ther. 2019;12:3011-3017.
Maugeri A, Russo C, Musumeci L, Lombardo GE, De Sarro G, Barreca D, et al. The anticancer effect of a flavonoid-rich extract of bergamot juice in THP-1 cells engages the SIRT2/AKT/p53 pathway. Pharmaceutics. 2022;14(10):2168.
Lu C, Zhu F, Cho Y-Y, Tang F, Zykova T, Ma W, et al. Cell apoptosis: requirement of H2AX in DNA ladder formation but not for the activation of Caspase-3. Mol Cell. 2006;23(1):121-132.
Kracikova M, Akiri G, George A, Sachidanandam R, Aaronson SA. A threshold mechanism mediates p53 cell fate decision between growth arrest and apoptosis. Cell Death Differ. 2013;20(4):576-588.
Kruiswijk F, Labuschagne CF, Vousden KH. p53 in survival, death and metabolic health: a lifeguard with a licence to kill. Nat Rev Mol Cell Biol. 2015;16(7):393-405.
Chen X, Ko LJ, Jayaraman L, Prives C. p53 levels, functional domains, and DNA damage determine the extent of the apoptotic response of tumor cells. Genes Dev. 1996;10(19):2438-2451.
Pan R, Ruvolo VR, Wei J, Konopleva M, Reed JC, Pellecchia M, et al. Inhibition of Mcl-1 with the pan-Bcl-2 family inhibitor (−)BI97D6 overcomes ABT-737 resistance in acute myeloid leukemia. Blood. 2015;126(3):363-372.
Lopez JJ, Albarran L, Gómez LJ, Smani T, Salido GM, Rosado JA. Molecular modulators of store-operated calcium entry. Biochim Biophys Acta. 2016;1863(8):2037-2043.
Shalygin A, Skopin A, Kalinina V, Zimina O, Glushankova L, Mozhayeva GN, et al. STIM1 and STIM2 proteins differently regulate endogenous store-operated channels in HEK293 cells. J Biol Chem. 2015;290(8):4717-4727.
Darbellay B, Arnaudeau S, Ceroni D, Bader CR, Konig S, Bernheim L. Human muscle economy myoblast differentiation and excitation-contraction coupling use the same molecular partners, STIM1 and STIM2. J Biol Chem. 2010;285(29):22437-22447.
Soboloff J, Spassova MA, Tang XD, Hewavitharana T, Xu W, Gill DL. Orai1 and STIM reconstitute store-operated calcium channel function. J Biol Chem. 2006;281(30):20661-20665.
Miederer A-M, Alansary D, Schwär G, Lee P-H, Jung M, Helms V, et al. A STIM2 splice variant negatively regulates store-operated calcium entry. Nat Commun. 2015;6:6899.
Rana A, Yen M, Sadaghiani AM, Malmersjö S, Park CY, Dolmetsch RE, et al. Alternative splicing converts STIM2 from an activator to an inhibitor of store-operated calcium channels. J Cell Biol. 2015;209(5):653-669.
Weidinger C, Shaw PJ, Feske S. STIM1 and STIM2-mediated Ca2+ influx regulates antitumour immunity by CD8+ T cells. EMBO Mol Med. 2013;5(9):1311-1321.
Shaw PJ, Weidinger C, Vaeth M, Luethy K, Kaech SM, Feske S. CD4+ and CD8+ T cell-dependent antiviral immunity requires STIM1 and STIM2. J Clin Invest. 2014;124(10):4549-4563.
Sogkas G, Stegner D, Syed SN, Vögtle T, Rau E, Gewecke B, et al. Cooperative and alternate functions for STIM1 and STIM2 in macrophage activation and in the context of inflammation. Immun Inflamm Dis. 2015;3(3):154-170.
Vaeth M, Zee I, Concepcion AR, Maus M, Shaw P, Portal-Celhay C, et al. Ca2+ signaling but not store-operated Ca2+ entry is required for the function of macrophages and dendritic cells. J Immunol. 2015;195(3):1202-1217.
Floto RA, Mahaut-Smith MP, Allen JM, Somasundaram B. Differentiation of the human monocytic cell line U937 results in an upregulation of the calcium release-activated current, ICRAC. J Physiol. 1996;495(Pt 2):331-338.
Saul S, Gibhardt CS, Schmidt B, Lis A, Pasieka B, Conrad D, et al. A calcium-redox feedback loop controls human monocyte immune responses: the role of ORAI Ca2+ channels. Sci Signal. 2016;9(418):ra26.
Liang S-J, Zeng D-Y, Mai X-Y, Shang J-Y, Wu Q-Q, Yuan J-N, et al. Inhibition of Orai1 store-operated calcium channel prevents foam cell formation and atherosclerosis. Arterioscler Thromb Vasc Biol. 2016;36(4):618-628.

Auteurs

Stefan Djordjevic (S)

HEMATIM UR4666, Université Picardie Jules Verne, Amiens, France.

Raphaël Itzykson (R)

Département Hématologie et Immunologie, Hôpital Saint-Louis, Assistance Publique-Hôpitaux de Paris, France.
Génomes, Biologie Cellulaire et Thérapeutique U944, INSERM, CNRS, Université Paris Cité, France.

Frédéric Hague (F)

Laboratoire de Physiologie Cellulaire et Moléculaire UR4667, Université Picardie Jules Verne, Amiens, France.

Delphine Lebon (D)

HEMATIM UR4666, Université Picardie Jules Verne, Amiens, France.
Service d'Hématologie Clinique et de Thérapie Cellulaire, CHU Amiens-Picardie, France.

Julien Legrand (J)

HEMATIM UR4666, Université Picardie Jules Verne, Amiens, France.

Hakim Ouled-Haddou (H)

HEMATIM UR4666, Université Picardie Jules Verne, Amiens, France.

Guillaume Jedraszak (G)

HEMATIM UR4666, Université Picardie Jules Verne, Amiens, France.
Laboratoire de Génétique Constitutionnelle, CHU Amiens-Picardie, France.

Juliette Harbonnier (J)

HEMATIM UR4666, Université Picardie Jules Verne, Amiens, France.

Louison Collet (L)

HEMATIM UR4666, Université Picardie Jules Verne, Amiens, France.

Etienne Paubelle (E)

HEMATIM UR4666, Université Picardie Jules Verne, Amiens, France.
Service d'Hématologie Clinique et de Thérapie Cellulaire, CHU Amiens-Picardie, France.

Jean-Pierre Marolleau (JP)

HEMATIM UR4666, Université Picardie Jules Verne, Amiens, France.
Service d'Hématologie Clinique et de Thérapie Cellulaire, CHU Amiens-Picardie, France.

Loïc Garçon (L)

HEMATIM UR4666, Université Picardie Jules Verne, Amiens, France.
Service d'Hématologie Biologique, CHU Amiens-Picardie, France.

Thomas Boyer (T)

HEMATIM UR4666, Université Picardie Jules Verne, Amiens, France.
Service d'Hématologie Biologique, CHU Amiens-Picardie, France.

Classifications MeSH