N-methyl-D-aspartate receptor regulates the circadian clock in megakaryocytic cells and impacts cell proliferation through BMAL1

References

• Ebling FJ. The role of glutamate in the photic regulation of the suprachiasmatic nucleus. Prog Neurobiol. 1996;50(2–3):109–14. doi:10.1016/S0301-0082(96)00032-9.
   PubMed Web of Science ®Google Scholar
• Ohi K, Takashima M, Nishikawa T, Takahashi K. N-Methyl-D-Aspartate receptor participates in neuronal transmission of photic information through the retinohypothalamic tract. Neuroendocrinology. 1991;53(4):344–8. doi:10.1159/000125740.
   PubMed Web of Science ®Google Scholar
• Brown SA. Circadian clock-mediated control of stem cell division and differentiation: beyond night and day. Development. 2014;141(16):3105–11. doi:10.1242/dev.104851.
   PubMed Web of Science ®Google Scholar
• Hartley PS, John Sheward W, French K, Horn JM, Holmes MC, Harmar AJ. Food-entrained rhythmic expression of PER2 and BMAL1 in murine megakaryocytes does not correlate with circadian rhythms in megakaryopoiesis. J Thromb Haemost. 2008;6(7):1144–52. doi:10.1111/j.1538-7836.2008.02978.x.
   PubMed Web of Science ®Google Scholar
• Hartley PS. The diurnal tick-tockery of platelet biology. Platelets. 2012;23(2):157–60. doi:10.3109/09537104.2011.600791.
   PubMed Web of Science ®Google Scholar
• Richards J, Gumz ML. Advances in understanding the peripheral circadian clocks. FASEB J. 2012;26(9):3602–13. doi:10.1096/fj.12-203554.
   PubMed Web of Science ®Google Scholar
• Hastings MH, Maywood ES, Reddy AB. Two decades of circadian time. J Neuroendocrinol. 2008;20(6):812–9. doi:10.1111/j.1365-2826.2008.01715.x.
   PubMed Web of Science ®Google Scholar
• Albrecht U. Timing to perfection: the biology of central and peripheral circadian clocks. Neuron. 2012;74(2):246–60. doi:10.1016/j.neuron.2012.04.006.
   PubMed Web of Science ®Google Scholar
• Cai YD, Chiu JC. Timeless in animal circadian clocks and beyond. FEBS J. 2022;289(21):6559–75. doi:10.1111/febs.16253.
   PubMed Web of Science ®Google Scholar
• Kurien P, Hsu PK, Leon J, Wu D, McMahon T, Shi G, Xu Y, Lipzen A, Pennacchio LA, Jones CR, et al. TIMELESS mutation alters phase responsiveness and causes advanced sleep phase. Proc Natl Acad Sci USA. 2019;116(24):12045–53. doi:10.1073/pnas.1819110116.
   PubMed Web of Science ®Google Scholar
• Boucher H, Vanneaux V, Domet T, Parouchev A, Larghero J, Shiels PG. Circadian clock genes modulate human bone marrow mesenchymal stem cell differentiation, migration and cell cycle. PLoS One. 2016;11(1):e0146674. doi:10.1371/journal.pone.0146674.
   PubMed Web of Science ®Google Scholar
• Chakrabarti S, Michor F. Circadian clock effects on cellular proliferation: insights from theory and experiments. Curr Opin Cell Biol. 2020;67:17–26. doi:10.1016/j.ceb.2020.07.003.
   PubMed Web of Science ®Google Scholar
• Kalev-Zylinska ML, Hearn JI, Rong J, Zhu M, Munro J, Cornish J, Dalbeth N, Poulsen RC. Altered N-methyl D-aspartate receptor subunit expression causes changes to the circadian clock and cell phenotype in osteoarthritic chondrocytes. Osteoarthritis Cartilage. 2018;26(11):1518–30. doi:10.1016/j.joca.2018.06.015.
   PubMed Web of Science ®Google Scholar
• Alhilali M, Hearn JI, Rong J, Jain L, Bolam SM, Monk AP, Munro JT, Dalbeth N, Poulsen RC. IL-1beta induces changes in expression of core circadian clock components PER2 and BMAL1 in primary human chondrocytes through the NMDA receptor/CREB and NF-kappaB signalling pathways. Cell Signal. 2021;87:110143. doi:10.1016/j.cellsig.2021.110143.
   PubMed Web of Science ®Google Scholar
• Hansen KB, Yi F, Perszyk RE, Furukawa H, Wollmuth LP, Gibb AJ, Traynelis SF. Structure, function, and allosteric modulation of NMDA receptors. J Gen Physiol. 2018;150(8):1081–105. doi:10.1085/jgp.201812032.
   PubMed Web of Science ®Google Scholar
• Hitchcock IS, Skerry TM, Howard MR, Genever PG. NMDA receptor-mediated regulation of human megakaryocytopoiesis. Blood. 2003;102(4):1254–9. doi:10.1182/blood-2002-11-3553.
   PubMed Web of Science ®Google Scholar
• Hearn JI, Green TN, Hisey CL, Bender M, Josefsson EC, Knowlton N, Baumann J, Poulsen RC, Bohlander SK, Kalev-Zylinska ML. Deletion of Grin1 in mouse megakaryocytes reveals NMDA receptor role in platelet function and proplatelet formation. Blood. 2022;139(17):2673–90. doi:10.1182/blood.2021014000.
   PubMed Web of Science ®Google Scholar
• Kalev-Zylinska ML, Hearn JI, Makhro A, Bogdanova A. N-Methyl-D-Aspartate receptors in hematopoietic cells: what have we learned? Front Physiol. 2020;11:577. doi:10.3389/fphys.2020.00577.
   PubMed Web of Science ®Google Scholar
• Kalev-Zylinska ML, Morel-Kopp M-C, Ward CM, Hearn JI, Hamilton JR, Bogdanova AY. Ionotropic glutamate receptors in platelets: opposing effects and a unifying hypothesis. Platelets. 2020;32(8):1–11. doi:10.1080/09537104.2020.1852542.
   PubMed Web of Science ®Google Scholar
• Genever PG, Wilkinson DJ, Patton AJ, Peet NM, Hong Y, Mathur A, Erusalimsky JD, Skerry TM. Expression of a functional N-methyl-D-aspartate-type glutamate receptor by bone marrow megakaryocytes. Blood. 1999;93(9):2876–83. doi:10.1182/blood.V93.9.2876.409k31_2876_2883.
   PubMed Web of Science ®Google Scholar
• Kamal T, Green TN, Hearn JI, Josefsson EC, Morel-Kopp MC, Ward CM, During MJ, Kalev-Zylinska ML. N-methyl-d-aspartate receptor mediated calcium influx supports in vitro differentiation of normal mouse megakaryocytes but proliferation of leukemic cell lines. Res Pract Thromb Haemost. 2018;2(1):125–38. doi:10.1002/rth2.12068.
   PubMed Web of Science ®Google Scholar
• Kamal T, Green TN, Morel-Kopp MC, Ward CM, McGregor AL, McGlashan SR, Bohlander SK, Browett PJ, Teague L, During MJ, et al. 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.
   PubMed Web of Science ®Google Scholar
• Hearn JI, Green TN, Chopra M, Nursalim YNS, Ladvanszky L, Knowlton N, Blenkiron C, Poulsen RC, Singleton DC, Bohlander SK, et al. N-Methyl-D-Aspartate receptor hypofunction in Meg-01 cells reveals a role for intracellular calcium homeostasis in balancing megakaryocytic-erythroid differentiation. Thromb Haemost. 2020;120(4):671–86. doi:10.1055/s-0040-1708483.
   PubMed Web of Science ®Google Scholar
• Pritchett D, Reddy AB. Circadian clocks in the hematologic system. J Biol Rhythms. 2015;30(5):374–88. doi:10.1177/0748730415592729.
   PubMed Web of Science ®Google Scholar
• Ogura M, Morishima Y, Ohno R, Kato Y, Hirabayashi N, Nagura H, Saito H. Establishment of a novel human megakaryoblastic leukemia cell line, MEG-01, with positive Philadelphia chromosome. Blood. 1985;66(6):1384–92. doi:10.1182/blood.V66.6.1384.1384.
   PubMed Web of Science ®Google Scholar
• Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 2003;31(4):e15. doi:10.1093/nar/gng015.
   PubMed Web of Science ®Google Scholar
• Smyth GK. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol. 2004;3(1):Article3. doi:10.2202/1544-6115.1027.
   PubMedGoogle Scholar
• Luo W, Pant G, Bhavnasi YK, Blanchard SG Jr., Brouwer C. Pathview web: user friendly pathway visualization and data integration. Nucleic Acids Res. 2017;45(W1):W501–w508. doi:10.1093/nar/gkx372.
   PubMed Web of Science ®Google Scholar
• Balsalobre A, Damiola F, Schibler U. A serum shock induces circadian gene expression in mammalian tissue culture cells. Cell. 1998;93(6):929–37. doi:10.1016/S0092-8674(00)81199-X.
   PubMed Web of Science ®Google Scholar
• Born J, Lange T, Hansen K, Molle M, Fehm HL. Effects of sleep and circadian rhythm on human circulating immune cells. J Immunol. 1997;158(9):4454–64. doi:10.4049/jimmunol.158.9.4454.
   PubMed Web of Science ®Google Scholar
• Kanabrocki EL, Sothern RB, Messmore HL, Roitman-Johnson B, McCormick JB, Dawson S, Bremner FW, Third JL, Nemchausky BA, Shirazi P, et al. Circadian interrelationships among levels of plasma fibrinogen, blood platelets, and serum interleukin-6. Clin Appl Thromb Hemost. 1999;5(1):37–42. doi:10.1177/107602969900500108.
   PubMed Web of Science ®Google Scholar
• Bremner WF, Sothern RB, Kanabrocki EL, Ryan M, McCormick JB, Dawson S, Connors ES, Rothschild R, Third JL, Vahed S, et al. Relation between circadian patterns in levels of circulating lipoprotein(a), fibrinogen, platelets, and related lipid variables in men. Am Heart J. 2000;139(1):164–73. doi:10.1016/S0002-8703(00)90324-7.
   PubMed Web of Science ®Google Scholar
• Haus E, Cusulos M, Sackett-Lundeen L, Swoyer J. Circadian variations in blood coagulation parameters, alpha-antitrypsin antigen and platelet aggregation and retention in clinically healthy subjects. Chronobiol Int. 1990;7(3):203–16. doi:10.3109/07420529009056976.
   PubMed Web of Science ®Google Scholar
• Undar L, Turkay C, Korkmaz L. Circadian variation in circulating platelet aggregates. Ann Med. 1989;21(6):429–33. doi:10.3109/07853898909149234.
   PubMed Web of Science ®Google Scholar
• Jafri SM, VanRollins M, Ozawa T, Mammen EF, Goldberg AD, Goldstein S. Circadian variation in platelet function in healthy volunteers. Am J Cardiol. 1992;69(9):951–4. doi:10.1016/0002-9149(92)90799-5.
   PubMed Web of Science ®Google Scholar
• Andrews NP, Gralnick HR, Merryman P, Vail M, Quyyumi AA. Mechanisms underlying the morning increase in platelet aggregation: a flow cytometry study. J Am Coll Cardiol. 1996;28(7):1789–95. doi:10.1016/S0735-1097(96)00398-1.
   PubMed Web of Science ®Google Scholar
• Tofler GH, Brezinski D, Schafer AI, Czeisler CA, Rutherford JD, Willich SN, Gleason RE, Williams GH, Muller JE. Concurrent morning increase in platelet aggregability and the risk of myocardial infarction and sudden cardiac death. N Engl J Med. 1987;316(24):1514–18. doi:10.1056/NEJM198706113162405.
   PubMed Web of Science ®Google Scholar
• Scheer FA, Michelson AD, Frelinger AL, Evoniuk H, Kelly EE, McCarthy M, Doamekpor LA, Barnard MR, Shea SA. The human endogenous circadian system causes greatest platelet activation during the biological morning independent of behaviors. PLoS One. 2011;6(9):e24549. doi:10.1371/journal.pone.0024549.
   PubMed Web of Science ®Google Scholar
• Hartley PS, Sheward J, Scholefield E, French K, Horn JM, Holmes MC, Harmar AJ. Timed feeding of mice modulates light-entrained circadian rhythms of reticulated platelet abundance and plasma thrombopoietin and affects gene expression in megakaryocytes. Br J Haematol. 2009;146(2):185–92. doi:10.1111/j.1365-2141.2009.07722.x.
   PubMed Web of Science ®Google Scholar
• Hartley PS. Mice housed in groups of 4-6 exhibit a diurnal surge in their platelet count. Platelets. 2013;24(5):412–4. doi:10.3109/09537104.2012.706728.
   PubMed Web of Science ®Google Scholar
• Tracey CJ, Pan X, Catterson JH, Harmar AJ, Hussain MM, Hartley PS. Diurnal expression of the thrombopoietin gene is regulated by CLOCK. J Thromb Haemost. 2012;10(4):662–9. doi:10.1111/j.1538-7836.2012.04643.x.
   PubMed Web of Science ®Google Scholar
• Zhao Y, Zhang Y, Wang S, Hua Z, Zhang J. The clock gene Per2 is required for normal platelet formation and function. Thromb Res. 2011;127(2):122–30. doi:10.1016/j.thromres.2010.11.025.
   PubMed Web of Science ®Google Scholar
• Ohkura N, Oishi K, Sudo T, Hayashi H, Shikata K, Ishida N, Matsuda J, Horie S. CLOCK regulates circadian platelet activity. Thromb Res. 2009;123(3):523–7. doi:10.1016/j.thromres.2008.03.009.
   PubMed Web of Science ®Google Scholar
• Damiola F, Le Minh N, Preitner N, Kornmann B, Fleury-Olela F, Schibler U. Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Gen Devel. 2000;14(23):2950–61. doi:10.1101/gad.183500.
   PubMed Web of Science ®Google Scholar
• Harvey JRM, Plante AE, Meredith AL. Ion channels controlling circadian rhythms in suprachiasmatic nucleus excitability. Physiol Rev. 2020;100(4):1415–54. doi:10.1152/physrev.00027.2019.
   PubMed Web of Science ®Google Scholar
• Yang MY, Chang JG, Lin PM, Tang KP, Chen YH, Lin HY, Liu TC, Hsiao HH, Liu YC, Lin SF. Downregulation of circadian clock genes in chronic myeloid leukemia: alternative methylation pattern of hPER3. Cancer Sci. 2006;97(12):1298–307. doi:10.1111/j.1349-7006.2006.00331.x.
   PubMed Web of Science ®Google Scholar
• Yang MY, Yang WC, Lin PM, Hsu JF, Hsiao HH, Liu YC, Tsai HJ, Chang CS, Lin SF. Altered expression of circadian clock genes in human chronic myeloid leukemia. J Biol Rhythms. 2011;26(2):136–48. doi:10.1177/0748730410395527.
   PubMed Web of Science ®Google Scholar
• Yang MY, Lin PM, Hsiao HH, Hsu JF, Lin HY, Hsu CM, Chen IY, Su SW, Liu YC, Lin SF. Up-regulation of PER3 expression is correlated with better clinical outcome in acute leukemia. Anticancer Res. 2015;35:6615–22.
   PubMed Web of Science ®Google Scholar
• Thompson A, Zhang Y, Kamen D, Jackson CW, Cardiff RD, Ravid K. Deregulated expression of c-myc in megakaryocytes of transgenic mice increases megakaryopoiesis and decreases polyploidization. J Biol Chem. 1996;271(38):22976–82. doi:10.1074/jbc.271.38.22976.
   PubMed Web of Science ®Google Scholar
• Guo Y, Niu C, Breslin P, Tang M, Zhang S, Wei W, Kini AR, Paner GP, Alkan S, Morris SW, et al. C-Myc-mediated control of cell fate in megakaryocyte-erythrocyte progenitors. Blood. 2009;114(10):2097–106. doi:10.1182/blood-2009-01-197947.
   PubMed Web of Science ®Google Scholar
• Kellogg DR. Wee1-dependent mechanisms required for coordination of cell growth and cell division. J Cell Sci. 2003;116(24):4883–90. doi:10.1242/jcs.00908.
   PubMed Web of Science ®Google Scholar
• Khapre RV, Kondratova AA, Patel S, Dubrovsky Y, Wrobel M, Antoch MP, Kondratov RV. BMAL1-dependent regulation of the mTOR signaling pathway delays aging. Aging (Albany NY). 2014;6(1):48–57. doi:10.18632/aging.100633.
   PubMedGoogle Scholar
• Lipton JO, Yuan ED, Boyle LM, Ebrahimi-Fakhari D, Kwiatkowski E, Nathan A, Guttler T, Davis F, Asara JM, Sahin M. The circadian protein BMAL1 regulates translation in response to S6K1-mediated phosphorylation. Cell. 2015;161(5):1138–51. doi:10.1016/j.cell.2015.04.002.
   PubMed Web of Science ®Google Scholar
• Lipton JO, Boyle LM, Yuan ED, Hochstrasser KJ, Chifamba FF, Nathan A, Tsai PT, Davis F, Sahin M. Aberrant proteostasis of BMAL1 underlies circadian abnormalities in a paradigmatic Mtor-opathy. Cell Rep. 2017;20(4):868–80. doi:10.1016/j.celrep.2017.07.008.
   PubMed Web of Science ®Google Scholar
• Snelling SJ, Forster A, Mukherjee S, Price AJ, Poulsen RC. The chondrocyte-intrinsic circadian clock is disrupted in human osteoarthritis. Chronobiol Int. 2016;33(5):574–9. doi:10.3109/07420528.2016.1158183.
   PubMed Web of Science ®Google Scholar
• Yang W, Kang X, Liu J, Li H, Ma Z, Jin X, Qian Z, Xie T, Qin N, Feng D, et al. Clock gene Bmal1 modulates human cartilage gene expression by crosstalk with sirt1. Endocrinology. 2016;157(8):3096–107. doi:10.1210/en.2015-2042.
   PubMed Web of Science ®Google Scholar
• Wang J, Li S, Li X, Li B, Li Y, Xia K, Yang Y, Aman S, Wang M, Wu H. Circadian protein BMAL1 promotes breast cancer cell invasion and metastasis by up-regulating matrix metalloproteinase9 expression. Cancer Cell Int. 2019;19(1):182. doi:10.1186/s12935-019-0902-2.
   PubMedGoogle Scholar
• Korkmaz T, Aygenli F, Emisoglu H, Ozcelik G, Canturk A, Yilmaz S, Ozturk N. Opposite carcinogenic effects of circadian clock gene BMAL1. Sci Rep. 2018;8(1):16023. doi:10.1038/s41598-018-34433-4.
   PubMedGoogle Scholar
• Zhang Y, Devocelle A, Souza L, Foudi A, Tenreira Bento S, Desterke C, Sherrard R, Ballesta A, Adam R, Giron-Michel J, et al. BMAL1 knockdown triggers different colon carcinoma cell fates by altering the delicate equilibrium between AKT/mTOR and P53/P21 pathways. Aging. 2020;12(9):8067–83. doi:10.18632/aging.103124.
   PubMedGoogle Scholar
• Ding H, Zhao J, Liu H, Wang J, Lu W. BMAL1 knockdown promoted apoptosis and reduced testosterone secretion in TM3 Leydig cell line. Gene. 2020;747:144672. doi:10.1016/j.gene.2020.144672.
   PubMed Web of Science ®Google Scholar
• Sun Y, Wang P, Li H, Dai J. BMAL1 and CLOCK proteins in regulating UVB-induced apoptosis and DNA damage responses in human keratinocytes. J Cell Physiol. 2018;233(12):9563–74. doi:10.1002/jcp.26859.
   PubMed Web of Science ®Google Scholar
• Puram RV, Kowalczyk MS, de Boer CG, Schneider RK, Miller PG, McConkey M, Tothova Z, Tejero H, Heckl D, Järås M, et al. Core circadian clock genes regulate leukemia stem cells in AML. Cell. 2016;165(2):303–16. doi:10.1016/j.cell.2016.03.015.
   PubMed Web of Science ®Google Scholar
• Hemmeryckx B, Van Hove CE, Fransen P, Emmerechts J, Kauskot A, Bult H, Lijnen HR, Hoylaerts MF. Progression of the prothrombotic state in aging Bmal1-deficient mice. Arterioscler Thromb Vasc Biol. 2011;31(11):2552–9. doi:10.1161/ATVBAHA.111.229062.
   PubMed Web of Science ®Google Scholar
• Somanath PR, Podrez EA, Chen J, Ma Y, Marchant K, Antoch M, Byzova TV. Deficiency in core circadian protein Bmal1 is associated with a prothrombotic and vascular phenotype. J Cell Physiol. 2011;226(1):132–40. doi:10.1002/jcp.22314.
   PubMed Web of Science ®Google Scholar
• Taniguchi H, Fernandez AF, Setien F, Ropero S, Ballestar E, Villanueva A, Yamamoto H, Imai K, Shinomura Y, Esteller M. Epigenetic inactivation of the circadian clock gene BMAL1 in hematologic malignancies. Cancer Res. 2009;69(21):8447–54. doi:10.1158/0008-5472.CAN-09-0551.
   PubMed Web of Science ®Google Scholar
• Rahman S, Al-Hallaj AS, Nedhi A, Gmati G, Ahmed K, Jama HA, Trivilegio T, Mashour A, Askar AA, Boudjelal M. Differential expression of circadian genes in leukemia and a possible role for Sirt1 in restoring the circadian clock in chronic myeloid leukemia. J Circadian Rhythms. 2017;15(1):3. doi:10.5334/jcr.147.
   PubMedGoogle Scholar
• Gery S, Gombart AF, Yi WS, Koeffler C, Hofmann WK, Koeffler HP. Transcription profiling of C/EBP targets identifies Per2 as a gene implicated in myeloid leukemia. Blood. 2005;106(8):2827–36. doi:10.1182/blood-2005-01-0358.
   PubMed Web of Science ®Google Scholar
• Gery S, Koeffler HP. Per2 is a C/EBP target gene implicated in myeloid leukemia. Integr Cancer Ther. 2009;8(4):317–20. doi:10.1177/1534735409352084.
   PubMed Web of Science ®Google Scholar
• Jiang H, Yang X, Mi M, Wei X, Wu H, Xin Y, Sun C. PER2: a potential molecular marker for hematological malignancies. Mol Biol Rep. 2021;48(11):7587–95. doi:10.1007/s11033-021-06751-w.
   PubMed Web of Science ®Google Scholar
• Marler JR, Price TR, Clark GL, Muller JE, Robertson T, Mohr JP, Hier DB, Wolf PA, Caplan LR, Foulkes MA. Morning increase in onset of ischemic stroke. Stroke. 1989;20(4):473–6. doi:10.1161/01.STR.20.4.473.
   PubMed Web of Science ®Google Scholar
• Muller JE, Stone PH, Turi ZG, Rutherford JD, Czeisler CA, Parker C, Poole WK, Passamani E, Roberts R, Robertson T, et al. Circadian variation in the frequency of onset of acute myocardial infarction. N Engl J Med. 1985;313(21):1315–22. doi:10.1056/NEJM198511213132103.
   PubMed Web of Science ®Google Scholar
• Sanford ABA, da Cunha LS, Machado CB, de Pinho Pessoa FMC, Silva A, Ribeiro RM, Moreira FC, de Moraes Filho MO, de Moraes MEA, de Souza LEB, et al. Circadian rhythm dysregulation and leukemia development: the role of clock genes as promising biomarkers. Int J Mol Sci. 2022;23(15):8212. doi:10.3390/ijms23158212.
   PubMed Web of Science ®Google Scholar
• Ince LM, Barnoud C, Lutes LK, Pick R, Wang C, Sinturel F, Chen CS, de Juan A, Weber J, Holtkamp SJ, et al. Influence of circadian clocks on adaptive immunity and vaccination responses. Nat Commun. 2023;14(1):476. doi:10.1038/s41467-023-35979-2.
   PubMed Web of Science ®Google Scholar
• Cervantes-Silva MP, Carroll RG, Wilk MM, Moreira D, Payet CA, O’Siorain JR, Cox SL, Fagan LE, Klavina PA, He Y, et al. The circadian clock influences T cell responses to vaccination by regulating dendritic cell antigen processing. Nat Commun. 2022;13(1):7217. doi:10.1038/s41467-022-34897-z.
   PubMed Web of Science ®Google Scholar
• Wang C, Lutes LK, Barnoud C, Scheiermann C. The circadian immune system. Sci Immunol. 2022;7(72):eabm2465. doi:10.1126/sciimmunol.abm2465.
   PubMed Web of Science ®Google Scholar
• Hong H, Cheung YM, Cao X, Wu Y, Li C, Tian XY. REV-ERBalpha agonist SR9009 suppresses IL-1beta production in macrophages through BMAL1-dependent inhibition of inflammasome. Biochem Pharmacol. 2021;192:114701. doi:10.1016/j.bcp.2021.114701.
   PubMed Web of Science ®Google Scholar
• Deng W, Zhu S, Zeng L, Liu J, Kang R, Yang M, Cao L, Wang H, Billiar TR, Jiang J, et al. The circadian clock controls immune checkpoint pathway in sepsis. Cell Rep. 2018;24(2):366–78. doi:10.1016/j.celrep.2018.06.026.
   PubMed Web of Science ®Google Scholar
• Cunin P, Nigrovic PA. Megakaryocytes as immune cells. J Leukoc Biol. 2019;105(6):1111–21. doi:10.1002/JLB.MR0718-261RR.
   PubMed Web of Science ®Google Scholar
• Tilburg J, Becker IC, Italiano JE. Don’t you forget about me(gakaryocytes). Blood. 2022;139(22):3245–54. doi:10.1182/blood.2020009302.
   PubMed Web of Science ®Google Scholar
• Koupenova M, Livada AC, Morrell CN. Platelet and megakaryocyte roles in innate and adaptive immunity. Circ Res. 2022;130(2):288–308. doi:10.1161/CIRCRESAHA.121.319821.
   PubMed Web of Science ®Google Scholar
• Bernardes JP, Mishra N, Tran F, Bahmer T, Best L, Blase JI, Bordoni D, Franzenburg J, Geisen U, Josephs-Spaulding J, et al. Longitudinal multi-omics analyses identify responses of megakaryocytes, erythroid cells, and plasmablasts as hallmarks of severe COVID-19. Immunity. 2020;53(6):1296–314 e1299. doi:10.1016/j.immuni.2020.11.017.
   PubMed Web of Science ®Google Scholar
• Campbell RA, Schwertz H, Hottz ED, Rowley JW, Manne BK, Washington AV, Hunter-Mellado R, Tolley ND, Christensen M, Eustes AS, et al. Human megakaryocytes possess intrinsic antiviral immunity through regulated induction of IFITM3. Blood. 2019;133(19):2013–26. doi:10.1182/blood-2018-09-873984.
   PubMed Web of Science ®Google Scholar
• Wang J, Xie J, Wang D, Han X, Chen M, Shi G, Jiang L, Zhao M. Cxcr4(high) megakaryocytes regulate host-defense immunity against bacterial pathogens. Elife. 2022;11:11. doi:10.7554/eLife.78662.
   Web of Science ®Google Scholar
• Wunderlich F, Delic D, Gerovska D, Arauzo-Bravo MJ. Vaccination accelerates liver-intrinsic expression of megakaryocyte-related genes in response to blood-stage malaria. Vaccines (Basel). 2022;10(2):287. doi:10.3390/vaccines10020287.
   PubMed Web of Science ®Google Scholar
• Liu Y, Zuo X, Chen P, Hu X, Sheng Z, Liu A, Liu Q, Leng S, Zhang X, Li X, et al. Deciphering transcriptome alterations in bone marrow hematopoiesis at single-cell resolution in immune thrombocytopenia. Signal Transduct Target Ther. 2022;7(1):347. doi:10.1038/s41392-022-01167-9.
   PubMed Web of Science ®Google Scholar
• Boilard E, Nigrovic PA, Larabee K, Watts GF, Coblyn JS, Weinblatt ME, Massarotti EM, Remold-O’Donnell E, Farndale RW, Ware J, et al. Platelets amplify inflammation in arthritis via collagen-dependent microparticle production. Science. 2010;327(5965):580–3. doi:10.1126/science.1181928.
   PubMed Web of Science ®Google Scholar
• Khatib-Massalha E, Mendez-Ferrer S. Megakaryocyte diversity in ontogeny, functions and cell-cell interactions. Front Oncol. 2022;12:840044. doi:10.3389/fonc.2022.840044.
   PubMed Web of Science ®Google Scholar
• Oyama Y, Walker LA, Eckle T. Targeting circadian PER2 as therapy in myocardial ischemia and reperfusion injury. Chronobiol Int. 2021;38(9):1262–73. doi:10.1080/07420528.2021.1928160.
   PubMed Web of Science ®Google Scholar
• Penaloza-Martinez E, Moreno G, Aroca-Crevillen A, Huertas S, Vicent L, Rosillo N, Hidalgo A, Bueno H. Circadian rhythms in thrombosis and atherothrombotic events. Front Biosci (Landmark Ed). 2022;27(2):51. doi:10.31083/j.fbl2702051.
   Web of Science ®Google Scholar
• Battaglin F, Chan P, Pan Y, Soni S, Qu M, Spiller ER, Castanon S, Roussos Torres ET, Mumenthaler SM, Kay SA, et al. Clocking cancer: the circadian clock as a target in cancer therapy. Oncogene. 2021;40(18):3187–200. doi:10.1038/s41388-021-01778-6.
   PubMed Web of Science ®Google Scholar
• Ruan W, Yuan X, Eltzschig HK. Circadian rhythm as a therapeutic target. Nat Rev Drug Discov. 2021;20(4):287–307. doi:10.1038/s41573-020-00109-w.
   PubMed Web of Science ®Google Scholar
• Poole J, Ray D. The role of circadian clock genes in critical illness: the potential role of translational clock gene therapies for targeting inflammation, mitochondrial function, and muscle mass in intensive care. J Biol Rhythms. 2022;37(4):385–402. doi:10.1177/07487304221092727.
   PubMed Web of Science ®Google Scholar
• Xia Y, Ding X, Wang S, Ren W. Circadian orchestration of host and gut microbiota in infection. Biol Rev Camb Philos Soc. 2023;98(1):115–31. doi:10.1111/brv.12898.
   PubMed Web of Science ®Google Scholar