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Immunological Investigations
A Journal of Molecular and Cellular Immunology
Volume 52, 2023 - Issue 4
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Research Article

Promoted Generation of T Helper 1-Like Regulatory T Cells After Transient Middle Cerebral Artery Occlusion in Type-2 Diabetic Mice

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Pages 482-498 | Received 04 Oct 2022, Accepted 09 Jan 2023, Published online: 19 Apr 2023

References

  • Akamatsu Y, Nishijima Y, Lee CC, Yang SY, Shi L, An L, Wang RK, Tominaga T, Liu J. 2015. Impaired leptomeningeal collateral flow contributes to the poor outcome following experimental stroke in the type 2 diabetic mice. J Neurosci. 35:3851–64.
  • Ali AJ, Makings J, Ley K. 2020. Regulatory T cell stability and plasticity in atherosclerosis. Cells. 9:2665.
  • Boddaert J, Bielen K, S Jongers B, Manocha E, Yperzeele L, Cras P, Pirici D, Kumar-Singh S. 2018. CD8 signaling in microglia/macrophage M1 polarization in a rat model of cerebral ischemia. PLoS One. 13:e0186937.
  • Butcher MJ, Filipowicz AR, Waseem TC, McGary CM, Crow KJ, Magilnick N, Boldin M, Lundberg PS, Galkina EV. 2016. Atherosclerosis-driven treg plasticity results in formation of a dysfunctional subset of plastic IFNγ + Th1/Tregs. Circ Res. 119:1190–203.
  • Chen S, Wu H, Klebe D, Hong Y, Zhang J, Tang J. 2013. Regulatory T cell in stroke: a new paradigm for immune regulation. Clin Dev Immunol. 2013:689827.
  • De Rosa V, Procaccini C, Cali G, Pirozzi G, Fontana S, Zappacosta S, La Cava A, Matarese G. 2007. A key role of leptin in the control of regulatory T cell proliferation. Immunity. 26:241–55.
  • Di Giovangiulio M, Rizzo A, Franze E, Caprioli F, Facciotti F, Onali S, Favale A, Stolfi C, Fehling HJ, Monteleone G, et al. 2019. Tbet expression in regulatory T cells is required to initiate Th1-mediated colitis. Front Immunol. 10:2158.
  • Jayaraj RL, Azimullah S, Beiram R, Jalal FY, Rosenberg GA. 2019. Neuroinflammation: friend and foe for ischemic stroke. J Neuroinflammation. 16:142.
  • Kitz A, Dominguez-Villar M. 2017. Molecular mechanisms underlying Th1-like Treg generation and function. Cell Mol Life Sci. 74:4059–75.
  • Kitz A, Singer E, Hafler D. 2018. Regulatory T cells: from discovery to autoimmunity. Cold Spring Harb Perspect Med. 8:a029041.
  • Kleinschnitz C, Kraft P, Dreykluft A, Hagedorn I, Göbel K, Schuhmann MK, Langhauser F, Helluy X, Schwarz T, Bittner S, et al. 2013. Regulatory T cells are strong promoters of acute ischemic stroke in mice by inducing dysfunction of the cerebral microvasculature. Blood. 121:679–91.
  • Lee GR. 2018. IRF8: identity-keeper for suppressive Th1-like Treg cells. Cell Mol Immunol. 15:1080–81.
  • Liesz A, Zhou W, Na SY, Hämmerling GJ, Garbi N, Karcher S, Mracsko E, Backs J, Rivest S, Veltkamp R. 2013. Boosting regulatory T cells limits neuroinflammation in permanent cortical stroke. J Neurosci. 33:17350–62.
  • Mao JH, Xu Y, Li BW, Yang YL, Peng Y, Zhi F. 2021. Microglia polarization in ischemic stroke: complex mechanisms and therapeutic interventions. Chin Med J (Engl). 134:2415–17.
  • Matarese G, Procaccini C, De Rosa V, Horvath TL, La Cava A. 2010. Regulatory T cells in obesity: the leptin connection. Trends Mol Med. 16:247–56.
  • Moraes-Vieira PM, Larocca RA, Bassi EJ, Peron JPS, Andrade-Oliveira V, Wasinski F, Araujo R, Thornley T, Quintana FJ, Basso AS, et al. 2014. Leptin deficiency impairs maturation of dendritic cells and enhances induction of regulatory T and Th17 cells. Eur J Immunol. 44:794–806.
  • Piconese S, Walker LSK, Dominguez-Villar M. 2020. Editorial: control of regulatory T cell stability, plasticity, and function in health and disease. Front Immunol. 11:611591.
  • Pluta R, Januszewski S, Czuczwar SJ. 2021. Neuroinflammation in post-ischemic neurodegeneration of the brain: friend, foe, or both? Int J Mol Sci. 22(9):4405.
  • Qiu R, Zhou L, Ma Y, Zhou L, Liang T, Shi L, Long J, Yuan D. 2020. Regulatory T cell plasticity and stability and autoimmune diseases. Clin Rev Allergy Immunol. 58:52–70.
  • Rom S, Zuluaga-Ramirez V, Gajghate S, Seliga A, Winfield M, Heldt NA, Kolpakov MA, Bashkirova YV, Sabri AK, Persidsky Y. 2019. Hyperglycemia-driven neuroinflammation compromises BBB leading to memory loss in both Diabetes Mellitus (DM) type 1 and type 2 mouse models. Mol Neurobiol. 56:1883–96.
  • Santamaria-Cadavid M, Rodriguez-Castro E, Rodriguez-Yanez M, Arias-Rivas S, López-Dequidt I, Pérez-Mato M, Rodríguez-Pérez M, López-Loureiro I, Hervella P, Campos F, et al. 2020. Regulatory T cells participate in the recovery of ischemic stroke patients. BMC Neurol. 20:68.
  • Schuhmann MK, Kraft P, Stoll G, Lorenz K, Meuth SG, Wiendl H, Nieswandt B, Sparwasser T, Beyersdorf N, Kerkau T, et al. 2015. CD28 superagonist-mediated boost of regulatory T cells increases thrombo-inflammation and ischemic neurodegeneration during the acute phase of experimental stroke. J Cereb Blood Flow Metab. 35:6–10.
  • Selvaraj UM, Stowe AM. 2017. Long-term T cell responses in the brain after an ischemic stroke. Discov Med. 24:323–33.
  • Shi L, Sun Z, Su W, Xu F, Xie D, Zhang Q, Dai X, Iyer K, Hitchens TK, Foley LM, et al. 2021. Treg cell-derived osteopontin promotes microglia-mediated white matter repair after ischemic stroke. Immunity. 54:1527–42 e1528. doi:10.1016/j.immuni.2021.04.022.
  • Shu L, Xu CQ, Yan ZY, Yan Y, Jiang SZ, Wang YR. 2019. Post-stroke microglia induce sirtuin2 expression to suppress the anti-inflammatory function of infiltrating regulatory T cells. Inflammation. 42:1968–79.
  • Shukla V, Shakya AK, Perez-Pinzon MA, Dave KR. 2017. Cerebral ischemic damage in diabetes: an inflammatory perspective. J Neuroinflammation. 14:21.
  • Stubbe T, Ebner F, Richter D, Engel OR, Klehmet J, Royl G, Meisel A, Nitsch R, Meisel C, Brandt C. 2013. Regulatory T cells accumulate and proliferate in the ischemic hemisphere for up to 30 days after MCAO. J Cereb Blood Flow Metab. 33:37–47.
  • Taleb S, Herbin O, Ait-Oufella H, Verreth W, Gourdy P, Barateau V, Merval R, Esposito B, Clément K, Holvoet P, et al. 2007. Defective leptin/leptin receptor signaling improves regulatory T cell immune response and protects mice from atherosclerosis. Arterioscler Thromb Vasc Biol. 27:2691–98.
  • Tureyen K, Bowen K, Liang J, Dempsey RJ, Vemuganti R. 2011. Exacerbated brain damage, edema and inflammation in type-2 diabetic mice subjected to focal ischemia. J Neurochem. 116:499–507.
  • Vannucci SJ, Willing LB, Goto S, Alkayed NJ, Brucklacher RM, Wood TL, Towfighi J, Hurn PD, Simpson IA. 2001. Experimental stroke in the female diabetic, db/db, mouse. J Cereb Blood Flow Metab. 21:52–60.
  • Wang H, Wang Z, Wu Q, Yuan Y, Cao W, Zhang X. 2021. Regulatory T cells in ischemic stroke. CNS Neurosci Ther. 27:643–51.
  • Xia Y, Cai W, Thomson AW, Hu X. 2016. Regulatory T cell therapy for ischemic stroke: how far from clinical translation? Transl Stroke Res. 7:415–19.
  • Xie L, Choudhury GR, Winters A, Yang SH, Jin K. 2015. Cerebral regulatory T cells restrain microglia/macrophage-mediated inflammatory responses via IL-10. Eur J Immunol. 45:180–91.
  • Xie L, Sun F, Wang J, Mao X, Xie L, Yang S-H, Su D-M, Simpkins JW, Greenberg DA, Jin K. 2014. mTOR signaling inhibition modulates macrophage/microglia-mediated neuroinflammation and secondary injury via regulatory T cells after focal ischemia. J Immunol. 192:6009–19.
  • Yang C, Gong S, Chen X, Wang M, Zhang L, Zhang L, Hu C. 2021. Analgecine regulates microglia polarization in ischemic stroke by inhibiting NF-κB through the TLR4 MyD88 pathway. Int Immunopharmacol. 99:107930.
  • Zhang D, Ren J, Luo Y, He Q, Zhao R, Chang J, Yang Y, Guo ZN. 2021. T Cell Response in Ischemic Stroke: from Mechanisms to Translational Insights. Front Immunol. 12:707972.
  • Zhang F, Zhao Q, Jiang Y, Liu N, Liu Q, Shi FD, Hao J, Xu Y, Lo EH, Wang X. 2019. Augmented brain infiltration and activation of leukocytes after cerebral ischemia in type 2 diabetic mice. Front Immunol. 10:2392.

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