Pathophysiological Significance of Store-Operated Calcium Entry in Megakaryocyte Function: Opening New Paths for Understanding the Role of Calcium in Thrombopoiesis

Overview

Journal Int J Mol Sci

Publisher MDPI

Specialties Biochemistry
Chemistry
Molecular Biology

Date 2016 Dec 13

PMID 27941645

Citations 6

Authors

Christian A Di Buduo

Alessandra Balduini

Francesco Moccia

Affiliations

Soon will be listed here.

Abstract

Store-Operated Calcium Entry (SOCE) is a universal calcium (Ca) influx mechanism expressed by several different cell types. It is now known that Stromal Interaction Molecule (STIM), the Ca sensor of the intracellular compartments, together with Orai and Transient Receptor Potential Canonical (TRPC), the subunits of Ca permeable channels on the plasma membrane, cooperate in regulating multiple cellular functions as diverse as proliferation, differentiation, migration, gene expression, and many others, depending on the cell type. In particular, a growing body of evidences suggests that a tight control of SOCE expression and function is achieved by megakaryocytes along their route from hematopoietic stem cells to platelet production. This review attempts to provide an overview about the SOCE dynamics in megakaryocyte development, with a focus on most recent findings related to its involvement in physiological and pathological thrombopoiesis.

Citing Articles

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N-Methyl-D-Aspartate Receptor Hypofunction in Meg-01 Cells Reveals a Role for Intracellular Calcium Homeostasis in Balancing Megakaryocytic-Erythroid Differentiation.

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References

Liu X, Cheng K, Bandyopadhyay B, Pani B, Dietrich A, Paria B . Attenuation of store-operated Ca2+ current impairs salivary gland fluid secretion in TRPC1(-/-) mice. Proc Natl Acad Sci U S A. 2007; 104(44):17542-7. PMC: 2077292. DOI: 10.1073/pnas.0701254104. View

Sundivakkam P, Freichel M, Singh V, Yuan J, Vogel S, Flockerzi V . The Ca(2+) sensor stromal interaction molecule 1 (STIM1) is necessary and sufficient for the store-operated Ca(2+) entry function of transient receptor potential canonical (TRPC) 1 and 4 channels in endothelial cells. Mol Pharmacol. 2012; 81(4):510-26. PMC: 3310414. DOI: 10.1124/mol.111.074658. View

Zeng W, Yuan J, Kim M, Choi Y, Huang G, Worley P . STIM1 gates TRPC channels, but not Orai1, by electrostatic interaction. Mol Cell. 2008; 32(3):439-48. PMC: 2586614. DOI: 10.1016/j.molcel.2008.09.020. View

Roos J, Digregorio P, Yeromin A, Ohlsen K, Lioudyno M, Zhang S . STIM1, an essential and conserved component of store-operated Ca2+ channel function. J Cell Biol. 2005; 169(3):435-45. PMC: 2171946. DOI: 10.1083/jcb.200502019. View

Heise N, Palme D, Misovic M, Koka S, Rudner J, Lang F . Non-selective cation channel-mediated Ca2+-entry and activation of Ca2+/calmodulin-dependent kinase II contribute to G2/M cell cycle arrest and survival of irradiated leukemia cells. Cell Physiol Biochem. 2010; 26(4-5):597-608. DOI: 10.1159/000322327. View

Wedel B, Vazquez G, McKay R, Bird G, Putney Jr J . A calmodulin/inositol 1,4,5-trisphosphate (IP3) receptor-binding region targets TRPC3 to the plasma membrane in a calmodulin/IP3 receptor-independent process. J Biol Chem. 2003; 278(28):25758-65. DOI: 10.1074/jbc.M303890200. View

Borst O, Schmidt E, Munzer P, Schonberger T, Towhid S, Elvers M . The serum- and glucocorticoid-inducible kinase 1 (SGK1) influences platelet calcium signaling and function by regulation of Orai1 expression in megakaryocytes. Blood. 2011; 119(1):251-61. DOI: 10.1182/blood-2011-06-359976. View

Moccia F, Zuccolo E, Soda T, Tanzi F, Guerra G, Mapelli L . Stim and Orai proteins in neuronal Ca(2+) signaling and excitability. Front Cell Neurosci. 2015; 9:153. PMC: 4408853. DOI: 10.3389/fncel.2015.00153. View

Berra-Romani R, Mazzocco-Spezzia A, Pulina M, Golovina V . Ca2+ handling is altered when arterial myocytes progress from a contractile to a proliferative phenotype in culture. Am J Physiol Cell Physiol. 2008; 295(3):C779-90. PMC: 2544451. DOI: 10.1152/ajpcell.00173.2008. View

10.

Abbonante V, Di Buduo C, Gruppi C, Malara A, Gianelli U, Celesti G . Thrombopoietin/TGF-β1 Loop Regulates Megakaryocyte Extracellular Matrix Component Synthesis. Stem Cells. 2016; 34(4):1123-33. DOI: 10.1002/stem.2285. View

11.

Klampfl T, Gisslinger H, Harutyunyan A, Nivarthi H, Rumi E, Milosevic J . Somatic mutations of calreticulin in myeloproliferative neoplasms. N Engl J Med. 2013; 369(25):2379-90. DOI: 10.1056/NEJMoa1311347. View

12.

Lopez E, Berna-Erro A, Salido G, Rosado J, Redondo P . FKBP52 is involved in the regulation of SOCE channels in the human platelets and MEG 01 cells. Biochim Biophys Acta. 2012; 1833(3):652-62. DOI: 10.1016/j.bbamcr.2012.11.029. View

13.

Zheng L, Stathopulos P, Li G, Ikura M . Biophysical characterization of the EF-hand and SAM domain containing Ca2+ sensory region of STIM1 and STIM2. Biochem Biophys Res Commun. 2008; 369(1):240-6. DOI: 10.1016/j.bbrc.2007.12.129. View

14.

Lockwich T, Singh B, Liu X, Ambudkar I . Stabilization of cortical actin induces internalization of transient receptor potential 3 (Trp3)-associated caveolar Ca2+ signaling complex and loss of Ca2+ influx without disruption of Trp3-inositol trisphosphate receptor association. J Biol Chem. 2001; 276(45):42401-8. DOI: 10.1074/jbc.M106956200. View

15.

Kaushansky K . Thrombopoiesis. Semin Hematol. 2015; 52(1):4-11. DOI: 10.1053/j.seminhematol.2014.10.003. View

16.

Pietra D, Rumi E, Ferretti V, Di Buduo C, Milanesi C, Cavalloni C . Differential clinical effects of different mutation subtypes in CALR-mutant myeloproliferative neoplasms. Leukemia. 2015; 30(2):431-8. PMC: 4740452. DOI: 10.1038/leu.2015.277. View

17.

Frischauf I, Muik M, Derler I, Bergsmann J, Fahrner M, Schindl R . Molecular determinants of the coupling between STIM1 and Orai channels: differential activation of Orai1-3 channels by a STIM1 coiled-coil mutant. J Biol Chem. 2009; 284(32):21696-706. PMC: 2755892. DOI: 10.1074/jbc.M109.018408. View

18.

Potier M, Gonzalez J, Motiani R, Abdullaev I, Bisaillon J, Singer H . Evidence for STIM1- and Orai1-dependent store-operated calcium influx through ICRAC in vascular smooth muscle cells: role in proliferation and migration. FASEB J. 2009; 23(8):2425-37. PMC: 2717784. DOI: 10.1096/fj.09-131128. View

19.

Kamal T, Green T, Morel-Kopp M, Ward C, McGregor A, McGlashan S . Inhibition of glutamate regulated calcium entry into leukemic megakaryoblasts reduces cell proliferation and supports differentiation. Cell Signal. 2015; 27(9):1860-72. DOI: 10.1016/j.cellsig.2015.05.004. View

20.

Locke E, Bonilla M, Liang L, Takita Y, Cunningham K . A homolog of voltage-gated Ca(2+) channels stimulated by depletion of secretory Ca(2+) in yeast. Mol Cell Biol. 2000; 20(18):6686-94. PMC: 86178. DOI: 10.1128/MCB.20.18.6686-6694.2000. View