Publication Cover
Nutritional Neuroscience
An International Journal on Nutrition, Diet and Nervous System
Volume 26, 2023 - Issue 8
694
Views
0
CrossRef citations to date
0
Altmetric
Research Article

Obesity induces extracellular vesicle release from the endothelium as a contributor to brain damage after cerebral ischemia in rats

ORCID Icon, , ORCID Icon & ORCID Icon

References

  • Farooqui AA. High Calorie Diet and the Human Brain: Metabolic Consequences of Long-Term Consumption.; 2015. doi:10.1007/978-3-319-15254-7
  • Anstey KJ, Cherbuin N, Budge M, Young J. Body mass index in midlife and late-life as a risk factor for dementia: a metaanalysis of prospective studies. Obes Rev. 2011 May;12(5):e426–37. doi:10.1111/j.1467-789X.2010.00825.x
  • Pedditzi E, Peters R, Beckett N. The risk of overweight/obesity in mid-life and late life for the development of dementia: a systematic review and meta-analysis of longitudinal studies. Age Ageing. 2016 Jan;45(1):14-21. doi: 10.1093/ageing/afv151. Erratum in: Age Ageing. 2016 Sep;45(5):740.
  • Heuschmann PU, Kircher J, Nowe T, Dittrich R, Reiner Z, Cifkova R, et al. Control of main risk factors after ischaemic stroke across Europe: data from the stroke-specific module of the EUROASPIRE III survey. 2015 Oct;22(10):1354–62. doi:10.1177/2047487314546825
  • Haley MJ, Lawrence CB. Obesity and stroke: Can we translate from rodents to patients? J Cereb Blood Flow Metab. 2016 Dec;36(12):2007–21. doi: 10.1177/0271678X16670411
  • Osmond JM, Mintz JD, Dalton B, Stepp DW. Obesity increases blood pressure, cerebral vascular remodeling, and severity of stroke in the Zucker rat. 2009 Feb; 53(2):381–6. doi:10.1161/HYPERTENSIONAHA.108.124149
  • Deutsch C, Portik-Dobos V, Smith AD, Ergul A, Dorrance AM. Diet-induced obesity causes cerebral vessel remodeling and increases the damage caused by ischemic stroke. Microvasc Res. 2009;78(1):100–106. doi:10.1016/j.mvr.2009.04.004
  • Terao S, Yilmaz G, Stokes KY, Ishikawa M, Kawase T, Neil Granger D. Inflammatory and injury responses to ischemic stroke in obese mice Stroke. 2008;39:943–50. doi:10.1161/STROKEAHA.107.494542
  • Chan AML, Ng AMH, Mohd Yunus MH, et al. Recent developments in rodent models of high-fructose diet-induced metabolic syndrome: a systematic review. Nutrients. 2021;13(8):1–21. doi:10.3390/nu13082497
  • Ogundele OM, Ajonijebu DC, Adeniyi PA, Alade OI, Balogun WG, Cobham AE, et al. Cerebrovascular changes in the rat brain in two models of ischemia. Pathophysiology. 2014 Sep;21(3):199–209. doi:10.1016/j.pathophys.2014.08.002
  • Engelhardt B, Sorokin L. The blood-brain and the blood-cerebrospinal fluid barriers: function and dysfunction. Semin Immunopathol. 2009;31(4):497–511. doi:10.1007/s00281-009-0177-0
  • Arraud N, Linares R, Tan S, Gounou C, Pasquet JM, Mornet S, et al. Extracellular vesicles from blood plasma: determination of their morphology, size, phenotype and concentration. J Thromb Haemost. 2014 May;12(5):614–27. doi:10.1111/jth.12554
  • Ramirez SH, Andrews AM, Paul D, Pachter JS. Extracellular vesicles: mediators and biomarkers of pathology along CNS barriers. Fluids Barriers CNS. 2018 Jul 1;15(1):19. doi:10.1186/s12987-018-0104-7
  • van Niel G, D'Angelo G, Raposo G. Shedding light on the cell biology of extracellular vesicles. Nat Rev Mol Cell Biol. 2018 Apr;19(4):213–28. doi:10.1038/nrm.2017.125
  • Bond ST, Calkin AC, Drew BG. Adipose-derived extracellular vesicles: systemic messengers and metabolic regulators in health and disease. Front Physiol. 2022 Feb 23;13:837001. doi:10.3389/fphys.2022.837001
  • Pérez-Corredor PA, Gutiérrez-Vargas JA, Ciro-Ramírez L, Balcazar N, Cardona-Gómez GP. High fructose diet-induced obesity worsens post-ischemic brain injury in the hippocampus of female rats. Nutr Neurosci. 2022 Jan;25(1):122–36. doi:10.1080/1028415X.2020.1724453
  • Lehmann JS, Zhao A, Sun B, Jiang W, Ji S. Multiplex cytokine profiling of stimulated mouse splenocytes using a cytometric bead-based immunoassay platform. J Vis Exp. 2017 Nov 9;(129):56440. doi:10.3791/56440
  • Vemmos K, Ntaios G, Spengos K, et al. Association between obesity and mortality after acute first-ever stroke: The obesity-stroke paradox. Stroke. 2011;42(1):30–36. doi:10.1161/STROKEAHA.110.593434
  • Skolarus LE, Sanchez BN, Levine DA, Baek J, Kerber KA, Morgenstern LB, et al. Association of body mass index and mortality after acute ischemic stroke. Circ Cardiovasc Qual Outcomes. 2014 Jan;7(1):64–9. doi:10.1161/CIRCOUTCOMES.113.000129
  • Weimar C, Mieck T, Buchthal J, Ehrenfeld CE, Schmid E, Diener HC. German stroke study collaboration. Neurologic worsening during the acute phase of ischemic stroke. Arch Neurol. 2005 Mar;62(3):393–7. doi:10.1001/archneur.62.3.393
  • Young JA, Tolentino M. Stroke evaluation and treatment. Top Stroke Rehabil. 2009 Nov–Dec;16(6):389–410. doi:10.1310/tsr1606-389
  • Bleyenheuft Y, Gordon AM. Precision grip in congenital and acquired hemiparesis: similarities in impairments and implications for neurorehabilitatio. Front Hum Neurosci. 2014 Jun 30;8:459. doi:10.3389/fnhum.2014.00459
  • Hatem SM, Saussez G, Della Faille M, Prist V, Zhang X, Dispa D, et al. Rehabilitation of motor function after stroke: a multiple systematic review focused on techniques to stimulate upper extremity recovery. Front Hum Neurosci. 2016 Sep 13;10:442. doi:10.3389/fnhum.2016.00442
  • Slyper AH, Rosenberg H, Kabra A, Weiss MJ, Blech B, Gensler S, et al. Early atherogenesis and visceral fat in obese adolescents. Int J Obes (Lond). 2014 Jul;38(7):954–8. doi:10.1038/ijo.2014.11
  • Vazzana N, Ranalli P, Cuccurullo C, Davì G. Diabetes mellitus and thrombosis. Thromb Res. 2012 Mar;129(3):371–7. doi:10.1016/j.thromres.2011.11.052
  • Patience Ojo O, Perez-Corredor PA, Gutierrez-Vargas JA, Busayo Akinola O, Cardona-Gómez GP. Lasting metabolic effect of a high-fructose diet on global cerebral ischemia. Nutr Neurosci. 2022 Jun;25(6):1159–72. doi:10.1080/1028415X.2020.1841482
  • Gutiérrez-Vargas JA, Múnera A, Cardona-Gómez GP. CDK5 knockdown prevents hippocampal degeneration and cognitive dysfunction produced by cerebral ischemia. J Cereb Blood Flow Metab. 2015;35(12):1937–49. doi:10.1038/jcbfm.2015.150
  • Salter MW, Stevens B. Microglia emerge as central players in brain disease. Nat Med. 2017 Sep 8;23(9):1018–27. doi:10.1038/nm.4397
  • Park JH, Cho JH, Ahn JH, Choi SY, Lee TK, Lee JC, et al. Neuronal loss and gliosis in the rat striatum subjected to 15 and 30 minutes of middle cerebral artery occlusion. Metab Brain Dis. 2018 Jun;33(3):775–84. doi:10.1007/s11011-018-0192-8
  • Lee TK, Kim H, Song M, Lee JC, Park JH, Ahn JH, et al. Time-course pattern of neuronal loss and gliosis in gerbil hippocampi following mild, severe, or lethal transient global cerebral ischemia. Neural Regen Res. 2019 Aug;14(8):1394–1403. doi:10.4103/1673-5374.253524
  • Grivas I, Michaloudi H, Batzios C, et al. Vascular network of the rat hippocampus is not homogeneous along the septotemporal axis. Brain Res. 2003;971(2):245–9. doi:10.1016/S0006-8993(03)02475-2
  • Han HS, Qiao Y, Karabiyikoglu M, Giffard RG, Yenari MA. Influence of mild hypothermia on inducible nitric oxide synthase expression and reactive nitrogen production in experimental stroke and inflammation. J Neurosci. 2002 May 15;22(10):3921–8. doi:10.1523/jneurosci.22-10-03921.2002
  • Kato H, Kogure K, Liu XH, Araki T, Itoyama Y. Progressive expression of immunomolecules on activated microglia and invading leukocytes following focal cerebral ischemia in the rat. Brain Res. 1996 Sep 23;734(1-2):203–12. doi:10.1016/0006-8993(96)00636-1
  • Yan BC, Park JH, Ahn JH, Kim IH, Lee JC, Yoo KY, et al. Effects of high-fat diet on neuronal damage, gliosis, inflammatory process and oxidative stress in the hippocampus induced by transient cerebral ischemia. Neurochem Res. 2014 Dec;39(12):2465–78. doi:10.1007/s11064-014-1450-8
  • Liddelow SA, Guttenplan KA, Clarke LE, Bennett FC, Bohlen CJ, Schirmer L, et al. Neurotoxic reactive astrocytes are induced by activated microglia. Nature. 2017 Jan 26;541(7638):481–7. doi:10.1038/nature21029
  • Sofroniew MV, Vinters HV. Astrocytes: biology and pathology. Acta Neuropathol. 2010 Jan;119(1):7–35. doi:10.1007/s00401-009-0619-8
  • Zamanian JL, Xu L, Foo LC, Nouri N, Zhou L, Giffard RG, et al. Genomic analysis of reactive astrogliosis. J Neurosci. 2012 May 2;32(18):6391–410. doi:10.1523/JNEUROSCI.6221-11.2012
  • Brambilla R, Bracchi-Ricard V, Hu WH, Frydel B, Bramwell A, Karmally S, et al. Inhibition of astroglial nuclear factor kappaB reduces inflammation and improves functional recovery after spinal cord injury. J Exp Med. 2005 Jul 4;202(1):145–56. doi:10.1084/jem.20041918
  • Douglass JD, Dorfman MD, Fasnacht R, Shaffer LD, Thaler JP. Astrocyte IKKβ/NF-κB signaling is required for diet-induced obesity and hypothalamic inflammation. Mol Metab. 2017 Jan 28;6(4):366–73. doi:10.1016/j.molmet.2017.01.010
  • Robb JL, Hammad NA, Weightman Potter PG, Chilton JK, Beall C, Ellacott KLJ. The metabolic response to inflammation in astrocytes is regulated by nuclear factor-kappa B signaling. Glia. 2020 Nov;68(11):2246–63.
  • Li K, Li J, Zheng J, Qin S. Reactive astrocytes in neurodegenerative diseases. Aging Dis. 2019 Jun 1;10(3):664–75. doi:10.14336/AD.2018.0720
  • Takano T, Oberheim NA, Cotrina ML, Nedergaard M. Astrocytes and ischemic injury. Stroke. 2009 Mar;40(3 Suppl):S8–12. doi:10.1161/STROKEAHA.108.533166
  • Gao L, Jiang T, Guo J, Liu Y, Cui G, Gu L, et al. Inhibition of autophagy contributes to ischemic postconditioning-induced neuroprotection against focal cerebral ischemia in rats. PLoS One. 2012;7(9):e46092. doi:10.1371/journal.pone.0046092
  • Haley MJ, Lawrence CB. The blood-brain barrier after stroke: structural studies and the role of transcytotic vesicles. J Cereb Blood Flow Metab. 2017 Feb;37(2):456–70. doi:10.1177/0271678X16629976
  • Pircher A, Treps L, Bodrug N, Carmeliet P. Endothelial cell metabolism: A novel player in atherosclerosis? Basic principles and therapeutic opportunities. Atherosclerosis. 2016 Oct;253:247–57. doi:10.1016/j.atherosclerosis.2016.08.011
  • Medina-Leyte DJ, Zepeda-García O, Domínguez-Pérez M, González-Garrido A, Villarreal-Molina T, Jacobo-Albavera L. Endothelial dysfunction, inflammation and coronary artery disease: potential biomarkers and promising therapeutical approaches. Int J Mol Sci. 2021 Apr 8;22(8):3850. doi:10.3390/ijms22083850
  • Nafisa A, Gray SG, Cao Y, Wang T, Xu S, Wattoo FH, et al. Endothelial function and dysfunction: Impact of metformin. Pharmacol Ther. 2018 Dec;192:150–62. doi:10.1016/j.pharmthera.2018.07.007
  • Silva IVG, de Figueiredo RC, Rios DRA. Effect of different classes of antihypertensive drugs on endothelial function and inflammation. Int J Mol Sci. 2019 Jul 14;20(14):3458. doi:10.3390/ijms20143458
  • Garcia-Martinez I, Alen R, Rada P, Valverde AM. Insights into extracellular vesicles as biomarker of NAFLD pathogenesis. Front Med (Lausanne). 2020 Aug 11;7395. doi:10.3389/fmed.2020.00395
  • Robbins PD, Morelli AE. Regulation of immune responses by extracellular vesicles. Nat Rev Immunol. 2014 Mar;14(3):195–208. doi:10.1038/nri3622
  • Eguchi A, Lazic M, Armando AM, Phillips SA, Katebian R, Maraka S, et al. Circulating adipocyte-derived extracellular vesicles are novel markers of metabolic stress. J Mol Med (Berl). 2016 Nov;94(11):1241–53. doi:10.1007/s00109-016-1446-8
  • Murakami T, Horigome H, Tanaka K, Nakata Y, Ohkawara K, Katayama Y, et al. Impact of weight reduction on production of platelet-derived microparticles and fibrinolytic parameters in obesity. Thromb Res. 2007;119(1):45–53. doi:10.1016/j.thromres.2005.12.013
  • Stepanian A, Bourguignat L, Hennou S, Coupaye M, Hajage D, Salomon L, et al. Microparticle increase in severe obesity: not related to metabolic syndrome and unchanged after massive weight loss. Obesity (Silver Spring). 2013 Nov;21(11):2236–43. doi:10.1002/oby.20365
  • Pardo F, Villalobos-Labra R, Sobrevia B, Toledo F, Sobrevia L. Extracellular vesicles in obesity and diabetes mellitus. Mol Aspects Med. 2018 Apr;60:81–91. doi:10.1016/j.mam.2017.11.010
  • Qu Y, Franchi L, Nunez G, Dubyak GR. Nonclassical IL-1 beta secretion stimulated by P2X7 receptors is dependent on inflammasome activation and correlated with exosome release in murine macrophages. J Immunol. 2007 Aug 1;179(3):1913–25. doi:10.4049/jimmunol.179.3.1913