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A circadian clock regulates efflux by the blood-brain barrier in mice and human cells

Efflux from mouse brain is highest when mice are active
Circadian clocks in mouse brain endothelium and cultured human endothelial cell culture found to drive TRPM7, a magnesium channel.
Oscillation TRPM7 levels result in fluctuations of intracellular free magnesium levels in brain endothelial cells, driving rhythms in efflux

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A Circadian Clock in the Blood-Brain Barrier Regulates Xenobiotic Efflux

The Drosophila BBB displays a circadian rhythm of permeability
Cyclic efflux driven by a clock in the BBB underlies the permeability rhythm
Circadian control is non-cell-autonomous via gap junction regulation of intracellular magnesium
An anti-seizure drug is more effective when administered at night

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All publications

Yang Z, Kim M, Montgomery M, Lewandowski A, Ho A, Buchwald ZS, Zhang SL. Pharmacological Modulation of Circadian Rhythms in Brain Microvasculature. Journal of Cerebral Blood Flow and Metabolism. 2025 Dec 7:0271678X251399116

Parker RE, McSwain L, Zhou W, Marcus AI, Fu H, Ramalingam SS, Zhang S, Gilbert-Ross M.J Cancer Res Clin Oncol. High PER1 expression is associated with STK11 mutation and clinical biomarkers of immunotherapy resistance in lung adenocarcinoma. 2025 Jul 26;151(7):223. doi: 10.1007/s00432-025-06269-9.PMID: 40715535

Shen Y, Connolly E, Aiello M, Zhou C, Chappa P, Song H, Tippitak P, Clark R, Cardenas M, Prokhnevska N, Mariniello A, De Bruyker I, Pagadala MS, Dhere VR, Rafiq S, Kesarwala AH, Orthwein A, Thomas SN, Zhang SL, Khan MK, Dixon JB, Lesinski G, Lowe MC, Kissick H, Yu DS, Paulos CM, Schmitt NC, Buchwald ZS. “Combination radiation and αPD-L1 enhance tumor control via stimulation of a CD8+ PD-1+ TCF-1+ T cell population in the tumor-draining lymph node.” Nature Communications. 2025 Apr 14.

Adebambo TH, Medina-Flores F, Zhang SL, Lerit DA. Arsenic impairs Drosophila neural stem cell mitotic progression and sleep behavior in a tauopathy model. G3 (Bethesda). 2025 Apr 7:jkaf049. PMID: 40192438

Avila A, Lewandowski AS, Li Y, Gui J, Lee KA, Kim M, Yang Z, Sehgal A, Chandler JD, and Zhang SL. Carnitine transporter at the blood-brain barrier modulates sleep in Drosophila through regulation of brain fatty acid oxidation. PNAS. 2025 Jan 28;122(4):e2421178122. PMID: 39847335

Li Y, Chouhan NS, Zhang S, Moore RS, Noya SB, Shon J, Yue Z, Sehgal A. Sleep and memory consolidation are linked by RNA processing genes in the Drosophila mushroom body. Elife 2024 Dec 6:12:RP89023. PMID: 39642051

Schwarz JE, Mrčela A, Lahens NF, Li Y, Hsu CT, Grant G, Skarke C, Zhang SL#, and Sehgal A#. Evidence for a role of human blood-borne factors in mediating age-associated changes in molecular circadian rhythms. ELife. 2024 Nov 1:12:RP88322. Oct 2024 PMID: 39485282

Iascone DM, Zhang X, Bafford P, Mesaros C, Sela Y, Zhang SL, Cook K, Pivarshev P, Stanger B, Anderson S, Dang C, Sehgal A. Hypermetabolic state is associated with circadian rhythm disruption in mouse and human cancer cells. PNAS. 2024 Jul 23;121(30):e2319782121. PMID: 39008664

Byrns C, Perlegos A, Carranza F, Manchanda P, Beveridge C, Randolph C, Chaluvadi V, Srinivasan A, Zhang SL, Frederick B, Sehgal A, Chopra G, and Bonini NM. Senescent glia link neuronal mitochondrial dysfunction and lipid accumulation with age. Nature. 2024 Jun;630(8016):475-483. PMID: 38839958

Schwarz JE, Sengupta A, Camilo G, Barber A, Hsu C, Zhang SL, Weljie A, Seghal A. Age-regulated cycling metabolites are relevant for behavior. Aging Cell. 2024 Apr;23(4):e14082. PMID: 38204362.

Li Y, Haynes P, Zhang SL, Yue Z, Sehgal A. Ecdysone acts through cortex glia to regulate sleep in Drosophila. eLife. 2023 12:e81723. https://doi.org/10.7554/eLife.81723

Lee Y, Fong SY, Shon J, Zhang SL, Brooks R, Lahens NF, Chen D, Dang CV, Field JM, Sehgal A. Time-of-day specificity of anticancer drugs may be mediated by circadian regulation of the cell cycle. Sci Adv. 2021 Feb;7(7). doi: 10.1126/sciadv.abd2645. Print 2021 Feb. PubMed PMID: 33579708; PubMed Central PMCID: PMC7880601.

Zhang SL, Lahens NF, Yue Z, Arnold DM, Pakstis PP, Schwarz JE, Sehgal A. A circadian clock regulates efflux by the blood-brain barrier in mice and human cells. Nat Commun. 2021 Jan 27;12(1):617. doi: 10.1038/s41467-020-20795-9. PubMed PMID: 33504784; PubMed Central PMCID: PMC7841146.

Sengupta S, Tang SY, Devine JC, Anderson ST, Nayak S, Zhang SL, Valenzuela A, Fisher DG, Grant GR, López CB, FitzGerald GA. Circadian control of lung inflammation in influenza infection. Nat Commun. 2019 Sep 11;10(1):4107. doi: 10.1038/s41467-019-11400-9. PubMed PMID: 31511530; PubMed Central PMCID: PMC6739310.

Cuddapah VA, Zhang SL, Sehgal A. Regulation of the Blood-Brain Barrier by Circadian Rhythms and Sleep. Trends Neurosci. 2019 Jul;42(7):500-510. doi: 10.1016/j.tins.2019.05.001. Review. PubMed PMID: 31253251; PubMed Central PMCID: PMC6602072.

Lee Y, Lahens NF, Zhang S, Bedont J, Field JM, Sehgal A. G1/S cell cycle regulators mediate effects of circadian dysregulation on tumor growth and provide targets for timed anticancer treatment. PLoS Biol. 2019 Apr;17(4):e3000228. doi: 10.1371/journal.pbio.3000228. eCollection 2019 Apr. PubMed PMID: 31039152; PubMed Central PMCID: PMC6490878.

Artiushin G, Zhang SL, Tricoire H, Sehgal A. Endocytosis at the Drosophila blood-brain barrier as a function for sleep. Elife. 2018 Nov 26;7. doi: 10.7554/eLife.43326. PubMed PMID: 30475209; PubMed Central PMCID: PMC6255390.

Rhoades SD, Nayak K, Zhang SL, Sehgal A, Weljie AM. Circadian- and Light-driven Metabolic Rhythms in Drosophila melanogaster. J Biol Rhythms. 2018 Apr;33(2):126-136. doi: 10.1177/0748730417753003. Epub 2018 Jan 21. PubMed PMID: 29355066; PubMed Central PMCID: PMC6692290.

Zhang SL, Yue Z, Arnold DM, Artiushin G, Sehgal A. A Circadian Clock in the Blood-Brain Barrier Regulates Xenobiotic Efflux. Cell. 2018 Mar 22;173(1):130-139.e10. doi: 10.1016/j.cell.2018.02.017. Epub 2018 Mar 8. PubMed PMID: 29526461; PubMed Central PMCID: PMC5866247.

Zhang SL, Bai L, Goel N, Bailey A, Jang CJ, Bushman FD, Meerlo P, Dinges DF, Sehgal A. Human and rat gut microbiome composition is maintained following sleep restriction. Proc Natl Acad Sci U S A. 2017 Feb 21;114(8):E1564-E1571. doi: 10.1073/pnas.1620673114. Epub 2017 Feb 8. PubMed PMID: 28179566; PubMed Central PMCID: PMC5338418.

Yang E, Zou T, Leichner TM, Zhang SL, Kambayashi T. Both retention and recirculation contribute to long-lived regulatory T-cell accumulation in the thymus. Eur J Immunol. 2014 Sep;44(9):2712-20. doi: 10.1002/eji.201444529. Epub 2014 Jul 1. PubMed PMID: 24894919; PubMed Central PMCID: PMC4177035.

Zhang SL, Wang X, Manna S, Zlotoff DA, Bryson JL, Blazar BR, Bhandoola A. Chemokine treatment rescues profound T-lineage progenitor homing defect after bone marrow transplant conditioning in mice. Blood. 2014 Jul 10;124(2):296-304. doi: 10.1182/blood-2014-01-552794. Epub 2014 May 29. PubMed PMID: 24876562; PubMed Central PMCID: PMC4093685.

Zhang SL, Bhandoola A. Trafficking to the thymus. Curr Top Microbiol Immunol. 2014;373:87-111. doi: 10.1007/82_2013_324. Review. PubMed PMID: 23624945.

Sultana DA, Zhang SL, Todd SP, Bhandoola A. Expression of functional P-selectin glycoprotein ligand 1 on hematopoietic progenitors is developmentally regulated. J Immunol. 2012 May 1;188(9):4385-93. doi: 10.4049/jimmunol.1101116. Epub 2012 Mar 28. PubMed PMID: 22461691; PubMed Central PMCID: PMC3331963.

Gus-Brautbar Y, Johnson D, Zhang L, Sun H, Wang P, Zhang S, Zhang L, Chen YH. The anti-inflammatory TIPE2 is an inhibitor of the oncogenic Ras. Mol Cell. 2012 Mar 9;45(5):610-8. doi: 10.1016/j.molcel.2012.01.006. Epub 2012 Feb 8. PubMed PMID: 22326055; PubMed Central PMCID: PMC3299909.

Zhang SL, Bhandoola A. Losing TREC with age. Immunity. 2012 Feb 24;36(2):163-5. doi: 10.1016/j.immuni.2012.02.005. PubMed PMID: 22365662; PubMed Central PMCID: PMC4026262.

Zlotoff DA, Zhang SL, De Obaldia ME, Hess PR, Todd SP, Logan TD, Bhandoola A. Delivery of progenitors to the thymus limits T-lineage reconstitution after bone marrow transplantation. Blood. 2011 Aug 18;118(7):1962-70. doi: 10.1182/blood-2010-12-324954. Epub 2011 Jun 9. PubMed PMID: 21659540; PubMed Central PMCID: PMC3158723.

Hettiarachchi K, Zhang S, Feingold S, Lee AP, Dayton PA. Controllable microfluidic synthesis of multiphase drug-carrying lipospheres for site-targeted therapy. Biotechnol Prog. 2009 Jul-Aug;25(4):938-45. doi: 10.1002/btpr.214. PubMed PMID: 19455647; PubMed Central PMCID: PMC2782552.

Wondrak GT, Cabello CM, Villeneuve NF, Zhang S, Ley S, Li Y, Sun Z, Zhang DD. Cinnamoyl-based Nrf2-activators targeting human skin cell photo-oxidative stress. Free Radic Biol Med. 2008 Aug 15;45(4):385-95. doi: 10.1016/j.freeradbiomed.2008.04.023. Epub 2008 Apr 26. PubMed PMID: 18482591; PubMed Central PMCID: PMC3710742.

Wang XJ, Sun Z, Villeneuve NF, Zhang S, Zhao F, Li Y, Chen W, Yi X, Zheng W, Wondrak GT, Wong PK, Zhang DD. Nrf2 enhances resistance of cancer cells to chemotherapeutic drugs, the dark side of Nrf2. Carcinogenesis. 2008 Jun;29(6):1235-43. doi: 10.1093/carcin/bgn095. Epub 2008 Apr 15. PubMed PMID: 18413364; PubMed Central PMCID: PMC3312612.

Sun Z, Zhang S, Chan JY, Zhang DD. Keap1 controls postinduction repression of the Nrf2-mediated antioxidant response by escorting nuclear export of Nrf2. Mol Cell Biol. 2007 Sep;27(18):6334-49. doi: 10.1128/MCB.00630-07. Epub 2007 Jul 16. PubMed PMID: 17636022; PubMed Central PMCID: PMC2099624.