Role of endothelial glycocalyx in central nervous system diseases and evaluation of the targeted therapeutic strategies for its protection: a review of clinical and experimental data

References

Abassi, Z., Armaly, Z., and Heyman, S.N. (2020). Glycocalyx degradation in ischemia-reperfusion injury. Am. J. Pathol. 190: 752–767, https://doi.org/10.1016/j.ajpath.2019.08.019.Search in Google Scholar PubMed

Albert, V., Subramanian, A., Agrawal, D., Pati, H.P., Gupta, S.D., and Mukhopadhyay, A.K. (2018). Acute traumatic endotheliopathy in isolated severe brain injury and its impact on clinical outcome. Med. Sci. 6: 5, https://doi.org/10.3390/medsci6010005.Search in Google Scholar PubMed PubMed Central

Alexopoulou, A.N., Multhaupt, H.A., and Couchman, J.R. (2007). Syndecans in wound healing, inflammation and vascular biology. Int. J. Biochem. Cell Biol. 39: 505–528, https://doi.org/10.1016/j.biocel.2006.10.014.Search in Google Scholar PubMed

Ali, M.M., Mahmoud, A.M., Master, E.L., Levitan, I., and Phillips, S.A. (2019). Role of matrix metalloproteinases and histone deacetylase in oxidative stress-induced degradation of the endothelial glycocalyx. Am. J. Physiol.: Heart Circ. Physiol. 316: H647–H663, https://doi.org/10.1152/ajpheart.00090.2018.Search in Google Scholar PubMed PubMed Central

Anderson, T.N., Hinson, H.E., Dewey, E.N., Rick, E.A., Schreiber, M.A., and Rowell, S.E. (2020). Early tranexamic acid administration after traumatic brain injury is associated with reduced syndecan-1 and angiopoietin-2 in patients with traumatic intracranial hemorrhage. J. Head Trauma Rehabil. 35: 317–323, https://doi.org/10.1097/htr.0000000000000619.Search in Google Scholar

Arafa, E.A., Elgendy, N.O., Elhemely, M.A., Abdelaleem, E.A., and Mohamed, W.R. (2023). Diosmin mitigates dexamethasone-induced osteoporosis in vivo: role of Runx2, RANKL/OPG, and oxidative stress. Biomed. Pharmacother. 161: 114461, https://doi.org/10.1016/j.biopha.2023.114461.Search in Google Scholar PubMed

Balistreri, C.R. (2022). Promising strategies for preserving adult endothelium health and reversing its dysfunction: from liquid biopsy to new omics technologies and noninvasive circulating biomarkers. Int. J. Mol. Sci. 23: 7548, https://doi.org/10.3390/ijms23147548.Search in Google Scholar PubMed PubMed Central

Bell, J.D., Rhind, S.G., Battista, A.P. Di, Macdonald, R.L., and Baker, A.J. (2017). Biomarkers of glycocalyx injury are associated with delayed cerebral ischemia following aneurysmal subarachnoid hemorrhage: a case series supporting a new hypothesis. Neurocrit. Care 26: 339–347, https://doi.org/10.1007/s12028-016-0357-4.Search in Google Scholar PubMed

Britten, M.W., Lümers, L., Tominaga, K., Peters, J., and Dirkmann, D. (2021). Glycocalyx components affect platelet function, whole blood coagulation, and fibrinolysis: an in vitro study suggesting a link to trauma-induced coagulopathy. BMC Anesthesiol. 21: 83, https://doi.org/10.1186/s12871-021-01300-1.Search in Google Scholar PubMed PubMed Central

Changyaleket, B., Chong, Z.Z., Dull, R.O., Nanegrungsunk, D., and Xu, H. (2017). Heparanase promotes neuroinflammatory response during subarachnoid hemorrhage in rats. J. Neuroinflammation 14: 137, https://doi.org/10.1186/s12974-017-0912-8.Search in Google Scholar PubMed PubMed Central

Cheng, Z., Kang, C., Che, S., Su, J., Sun, Q., Ge, T., Guo, Y., Lv, J., Sun, Z., Yang, W., et al.. (2022). Berberine: a promising treatment for neurodegenerative diseases. Front. Pharmacol. 13: 845591, https://doi.org/10.3389/fphar.2022.845591.Search in Google Scholar PubMed PubMed Central

Chico-Fernández, M., Barea-Mendoza, J.A., Pérez-Bárcena, J., García-Sáez, I., Quintana-Díaz, M.M., Mayor-García, D.M., Serviá-Goixart, L., Jiménez-Moragas, J.M., Lompart-Pou, J.A., and Llompart-Pou, J.A. (2021). Concomitant traumatic brain injury and hemorrhagic shock: outcomes using the Spanish trauma ICU registry (RETRAUCI). Am. Surg. 87: 370–375, https://doi.org/10.1177/0003134820949990.Search in Google Scholar PubMed

Chiu, K.M., Hung, Y.L., Wang, S.J., Tsai, Y.J., Wu, N.L., Liang, C.W., Chang, D.C., and Hung, C.F. (2021). Anti-allergic and anti-inflammatory effects of neferine on RBL-2H3 cells. Int. J. Mol. Sci. 22: 10994, https://doi.org/10.3390/ijms222010994.Search in Google Scholar PubMed PubMed Central

Csecsei, P., Olah, C., Varnai, R., Simon, D., Erdo-Bonyar, S., Berki, T., Czabajszki, M., Zavori, L., Schwarcz, A., and Molnar, T. (2023). Different kinetics of serum ADAMTS13, GDF-15, and neutrophil gelatinase-associated lipocalin in the early phase of aneurysmal subarachnoid hemorrhage. Int. J. Mol. Sci. 24: 11005, https://doi.org/10.3390/ijms241311005.Search in Google Scholar PubMed PubMed Central

Czeiter, E., Amrein, K., Gravesteijn, B.Y., Lecky, F., Menon, D.K., Mondello, S., Newcombe, V.F.J., Richter, S., Steyerberg, E.W., Vyvere, T.V., et al.. (2020). Blood biomarkers on admission in acute traumatic brain injury: relations to severity, CT findings and care path in the CENTER-TBI study. EBioMedicine 56: 102785, https://doi.org/10.1016/j.ebiom.2020.102785.Search in Google Scholar PubMed PubMed Central

Daglas, M., Galle, A., Draxler, D.F., Ho, H., Liu, Z., Sashindranath, M., and Medcalf, R.L. (2020). Sex-dependent effects of tranexamic acid on blood-brain barrier permeability and the immune response following traumatic brain injury in mice. J. Thromb. Haemostasis 18: 2658–2671, https://doi.org/10.1111/jth.15015.Search in Google Scholar PubMed

Deen, W.M., Lazzara, M.J., and Myers, B.D. (2001). Structural determinants of glomerular permeability. Am. J. Physiol. Renal Physiol. 281: F579–F596, https://doi.org/10.1152/ajprenal.2001.281.4.f579.Search in Google Scholar PubMed

Delgadillo, L.F., Lomakina, E.B., Kuebel, J., and Waugh, R.E. (2021). Changes in endothelial glycocalyx layer protective ability after inflammatory stimulus. Am. J. Physiol. Cell Physiol. 320: C216–C224, https://doi.org/10.1152/ajpcell.00259.2020.Search in Google Scholar PubMed PubMed Central

Delgadillo, L.F., Marsh, G.A., and Waugh, R.E. (2020). Endothelial glycocalyx layer properties and its ability to limit leukocyte adhesion. Biophys. J. 118: 1564–1575, https://doi.org/10.1016/j.bpj.2020.02.010.Search in Google Scholar PubMed PubMed Central

DellaValle, B., Hasseldam, H., Johansen, F.F., Iversen, H.K., Rungby, J., and Hempel, C. (2019). Multiple soluble components of the glycocalyx are increased in patient plasma after ischemic stroke. Stroke 50: 2948–2951, https://doi.org/10.1161/strokeaha.119.025953.Search in Google Scholar

DellaValle, B., Manresa-Arraut, A., Hasseldam, H., Stensballe, A., Rungby, J., Larsen, A., and Hempel, C. (2018). Detection of glycan shedding in the blood: new class of multiple sclerosis biomarkers? Front. Immunol. 9: 1254, https://doi.org/10.3389/fimmu.2018.01254.Search in Google Scholar PubMed PubMed Central

Drew, P.J. (2022). Neurovascular coupling: motive unknown. Trends Neurosci. 45: 809–819, https://doi.org/10.1016/j.tins.2022.08.004.Search in Google Scholar PubMed PubMed Central

Druzak, S., Iffrig, E., Roberts, B.R., Zhang, T., Fibben, K.S., Sakurai, Y., Verkerke, H.P., Rostad, C.A., Chahroudi, A., Schneider, F., et al.. (2023). Multiplatform analyses reveal distinct drivers of systemic pathogenesis in adult versus pediatric severe acute COVID-19. Nat. Commun. 14: 1638, https://doi.org/10.1038/s41467-023-37269-3.Search in Google Scholar PubMed PubMed Central

Ebong, E.E., Lopez-Quintero, S.V., Rizzo, V., Spray, D.C., and Tarbell, J.M. (2014). Shear-induced endothelial NOS activation and remodeling via heparan sulfate, glypican-1, and syndecan-1. Integr. Biol. 6: 338–347, https://doi.org/10.1039/c3ib40199e.Search in Google Scholar PubMed PubMed Central

Endo, S. and Shimazaki, R. (2018). An open-label, randomized, phase 3 study of the efficacy and safety of antithrombin gamma in patients with sepsis-induced disseminated intravascular coagulation syndrome. J. Intensive Care 6: 75, https://doi.org/10.1186/s40560-018-0339-z.Search in Google Scholar PubMed PubMed Central

Fan, J., Sun, Y., Xia, Y., Tarbell, M., and Fu, B.M. (2019). Endothelial surface glycocalyx (ESG) components and ultra-structure revealed by stochastic optical reconstruction microscopy (STORM). Biorheology 56: 77–88, https://doi.org/10.3233/bir-180204.Search in Google Scholar PubMed

Fu, B.M. and Tarbell, J.M. (2013). Mechano-sensing and transduction by endothelial surface glycocalyx: composition, structure, and function. Wiley Interdiscip. Rev.: Syst. Biol. Med. 5: 381–390, https://doi.org/10.1002/wsbm.1211.Search in Google Scholar PubMed PubMed Central

Geraghty, J.R. and Testai, F.D. (2017). Delayed cerebral ischemia after subarachnoid hemorrhage: beyond vasospasm and towards a multifactorial pathophysiology. Curr. Atheroscler. Rep. 19: 50, https://doi.org/10.1007/s11883-017-0690-x.Search in Google Scholar PubMed

Ghanemi, A., Melouane, A., Yoshioka, M., and St-Amand, J. (2022). Secreted protein acidic and rich in Cysteine (Sparc) KO leads to an accelerated ageing phenotype which is improved by exercise whereas SPARC overexpression mimics exercise effects in mice. Metabolites 12: 125, https://doi.org/10.3390/metabo12020125.Search in Google Scholar PubMed PubMed Central

Gonzalez, R.E., Cardenas, J.C., Cox, C.S., Kitagawa, R.S., Stensballe, J., Holcomb, J.B., Johansson, P.I., and Wade, C.E. (2018). Traumatic brain injury is associated with increased syndecan-1 shedding in severely injured patients. Scand J. Trauma Resusc. Emerg. Med. 26: 102, https://doi.org/10.1186/s13049-018-0565-3.Search in Google Scholar PubMed PubMed Central

Gonzalez, R.E., Ostrowski, S.R., Cardenas, J.C., Baer, L.A., Tomasek, J.S., Henriksen, H.H., Stensballe, J., Cotton, B.A., Holcomb, J.B., Johansson, P.I., et al.. (2017). Syndecan-1: a quantitative marker for the endotheliopathy of trauma. J. Am. Coll. Surg. 225: 419–427, https://doi.org/10.1016/j.jamcollsurg.2017.05.012.Search in Google Scholar PubMed

Harding, I.C., Mitra, R., Mensah, S.A., Herman, I.M., and Ebong, E.E. (2018). Pro-atherosclerotic disturbed flow disrupts caveolin-1 expression, localization, and function via glycocalyx degradation. J. Transl. Med. 16: 364, https://doi.org/10.1186/s12967-018-1721-2.Search in Google Scholar PubMed PubMed Central

He, Q., Fang, Y., Ma, C., Deng, Z., Wang, F., Qu, Y., Yin, M., Zhao, R., Zhang, D., Guo, F., et al.. (2023). Remote ischemic conditioning attenuates blood-brain barrier disruption after recombinant tissue plasminogen activator treatment via reducing PDGF-CC. Pharmacol. Res. 187: 106641, https://doi.org/10.1016/j.phrs.2022.106641.Search in Google Scholar PubMed

Henriksen, H.H., Marín de Mas, I., Nielsen, L.K., Krocker, J., Stensballe, J., Karvelsson, S.T., Secher, N.H., Rolfsson, Ó., Wade, C.E., and Johansson, P.I. (2023). Endothelial cell phenotypes demonstrate different metabolic patterns and predict mortality in trauma patients. Int. J. Mol. Sci. 24: 2257, https://doi.org/10.3390/ijms24032257.Search in Google Scholar PubMed PubMed Central

Heula, A.L., Sajanti, J., and Majamaa, K. (2015). Glycosaminoglycans in subdural fluid and CSF after meningeal injury. Acta Neurochir. 157: 2105–2110; discussion 2110, https://doi.org/10.1007/s00701-015-2591-5.Search in Google Scholar PubMed

Huang, X.W., Hussain, B., and Chang, J.L. (2021). Peripheral inflammation and blood-brain barrier disruption: effects and mechanisms. CNS Neurosci. Ther. 27: 36–47, https://doi.org/10.1111/cns.13569.Search in Google Scholar PubMed PubMed Central

Iba, T. and Levy, J.H. (2019). Derangement of the endothelial glycocalyx in sepsis. J. Thromb. Haemost. 17: 283–294, https://doi.org/10.1111/jth.14371.Search in Google Scholar PubMed

Iba, T., Levy, J.H., Aihara, K., Kadota, K., Tanaka, H., Sato, K., and Nagaoka, I. (2020). Newly developed recombinant antithrombin protects the pndothelial glycocalyx in an endotoxin-induced rat model of sepsis. Int. J. Mol. Sci. 22: 176, https://doi.org/10.3390/ijms22010176.Search in Google Scholar PubMed PubMed Central

Inagawa, R., Okada, H., Takemura, G., Suzuki, K., Takada, C., Yano, H., Ando, Y., Usui, T., Hotta, Y., Miyazaki, N., et al.. (2018). Ultrastructural alteration of pulmonary capillary endothelial glycocalyx during Endotoxemia. Chest 154: 317–325, https://doi.org/10.1016/j.chest.2018.03.003.Search in Google Scholar PubMed

Jasiak-Zatońska, M., Pietrzak, A., Wyciszkiewicz, A., Więsik-Szewczyk, E., Pawlak-Buś, K., Leszczyński, P., Kozubski, W., Michalak, S., and Kalinowska-Łyszczarz, A. (2022). Different blood-brain-barrier disruption profiles in multiple sclerosis, neuromyelitis optica spectrum disorders, and neuropsychiatric systemic lupus erythematosus. Neurol. Neurochir. Pol. 56: 246–255, https://doi.org/10.5603/pjnns.a2022.0013.Search in Google Scholar

Jin, J., Fang, F., Gao, W., Chen, H., Wen, J., Wen, X., and Chen, J. (2021). The structure and function of the glycocalyx and its connection with blood-brain barrier. Front. Cell Neurosci. 15: 739699, https://doi.org/10.3389/fncel.2021.739699.Search in Google Scholar PubMed PubMed Central

Kaplan, L., Chow, B.W., and Gu, C.H. (2020). Neuronal regulation of the blood-brain barrier and neurovascular coupling. Nat. Rev. Neurosci. 21: 416–432, https://doi.org/10.1038/s41583-020-0322-2.Search in Google Scholar PubMed PubMed Central

Karimi, A., Halabian, M., Razaghi, R., Downs, J.C., Kelley, M.J., and Acott, T.S. (2022). Modeling the endothelial glycocalyx layer in the human conventional aqueous outflow pathway. Cells 11: 3925, https://doi.org/10.3390/cells11233925.Search in Google Scholar PubMed PubMed Central

Kastenholz, N., Megjhani, M., Conzen-Dilger, C., Albanna, W., Veldeman, M., Nametz, D., Kwon, S.B., Schulze-Steinen, H., Ridwan, H., Clusmann, H., et al.. (2023). The oxygen reactivity index indicates disturbed local perfusion regulation after aneurysmal subarachnoid hemorrhage: an observational cohort study. Crit. Care 27: 235, https://doi.org/10.1186/s13054-023-04452-3.Search in Google Scholar PubMed PubMed Central

Kim, H.B., Soh, S., Kwak, Y.L., Bae, J.C., Kang, S.H., and Song, J.W. (2020). High preoperative serum syndecan-1, a marker of endothelial glycocalyx degradation, and severe acute kidney Injury after valvular heart surgery. J. Clin. Med. 9: 1803, https://doi.org/10.3390/jcm9061803.Search in Google Scholar PubMed PubMed Central

Ko, K., Suzuki, T., Ishikawa, R., Hattori, N., Ito, R., Umehara, K., Furihata, T., Dohmae, N., Linhardt, R.J., Igarashi, K., et al.. (2020). Ischemic stroke disrupts the endothelial glycocalyx through activation of proHPSE via acrolein exposure. J. Biol. Chem. 295: 18614–18624, https://doi.org/10.1074/jbc.ra120.015105.Search in Google Scholar PubMed PubMed Central

Kolářová, H., Víteček, J., Černá, A., Černík, M., Přibyl, J., Skládal, P., Potěšil, D., Ihnatová, I., Zdráhal, Z., Hampl, A., et al.. (2021). Myeloperoxidase mediated alteration of endothelial function is dependent on its cationic charge. Free Radic. Biol. Med. 162: 14–26, https://doi.org/10.1016/j.freeradbiomed.2020.11.008.Search in Google Scholar PubMed

Krüger-Genge, A., Blocki, A., Franke, R.P., and Jung, F. (2019). Vascular endothelial cell biology: an update. Int. J. Mol. Sci. 20: 4411, https://doi.org/10.3390/ijms20184411.Search in Google Scholar PubMed PubMed Central

Kutuzov, N., Flyvbjerg, H., and Lauritzen, M. (2018). Contributions of the glycocalyx, endothelium, and extravascular compartment to the blood-brain barrier. Proc. Natl. Acad. Sci. U. S. A. 115: E9429–E9438, https://doi.org/10.1073/pnas.1802155115.Search in Google Scholar PubMed PubMed Central

Lei, J., Xiang, P., Zeng, S., Chen, L., Zhang, L., Yuan, Z., Zhang, J., Wang, T., Yu, R., Zhang, W., et al.. (2021). Tetramethylpyrazine alleviates endothelial glycocalyx degradation and promotes glycocalyx restoration via TLR4/NF-κB/HPSE1 signaling pathway during inflammation. Front. Pharmacol. 12: 791841, https://doi.org/10.3389/fphar.2021.791841.Search in Google Scholar PubMed PubMed Central

Li, H., Hao, Y., Yang, L.L., Wang, X.Y., Li, X.Y., Bhandari, S., Han, J., Liu, Y.J., Gong, Y.Q., Scott, A., et al.. (2020). MCTR1 alleviates lipopolysaccharide-induced acute lung injury by protecting lung endothelial glycocalyx. J. Cell. Physiol. 235: 7283–7294, https://doi.org/10.1002/jcp.29628.Search in Google Scholar PubMed

Li, J., Kim, K., Barazia, A., Tseng, A., and Cho, J. (2015). Platelet-neutrophil interactions under thromboinflammatory conditions. Cell. Mol. Life Sci. 72: 2627–2643, https://doi.org/10.1007/s00018-015-1845-y.Search in Google Scholar PubMed PubMed Central

Litkowski, E.M., Logue, M.W., Zhang, R., Charest, B.R., Lange, E.M., Hokanson, J.E., Lynch, J.A., Vujkovic, M., Phillips, L.S., Hauger, R.L., et al.. (2023). Mendelian randomization study of diabetes and dementia in the Million Veteran Program. Alzheimers Dement 19: 4367–4376, https://doi.org/10.1002/alz.13373.Search in Google Scholar PubMed PubMed Central

Liu, H.Q., Li, J., Xuan, C.L., and Ma, H.C. (2020). A review on the physiological and pathophysiological role of endothelial glycocalyx. J. Biochem. Mol. Toxicol. 34: e22571, https://doi.org/10.1002/jbt.22571.Search in Google Scholar PubMed

Liu, J.X., Yan, Z.P., Zhang, Y.Y., Wu, J., Liu, X.H., and Zeng, Y. (2016). Hemodynamic shear stress regulates the transcriptional expression of heparan sulfate proteoglycans in human umbilical vein endothelial cell. Cell Mol. Biol. 62: 28–34.Search in Google Scholar

Liu, X.Y., Xu, H.X., Li, J.K., Zhang, D., Ma, X.H., Huang, L.N., Lü, J.H., and Wang, X.Z. (2018). Neferine protects endothelial glycocalyx via mitochondrial ROS in lipopolysaccharide-induced acute respiratory distress syndrome. Front. Physiol. 9: 102, https://doi.org/10.3389/fphys.2018.00102.Search in Google Scholar PubMed PubMed Central

Livingston, G., Huntley, J., Sommerlad, A., Ames, D., Ballard, C., Banerjee, S., Brayne, C., Burns, A., Cohen-Mansfield, J., Cooper, C., et al.. (2020). Dementia prevention, intervention, and care: 2020 report of the Lancet Commission. Lancet 396: 413–446, https://doi.org/10.1016/s0140-6736(20)30367-6.Search in Google Scholar PubMed PubMed Central

Lopez, A., Panisello-Rosello, A., Castro-Benitez, C., and Adam, R. (2018). Glycocalyx preservation and NO production in fatty livers-the protective role of high molecular polyethylene glycol in cold ischemia injury. Int. J. Mol. Sci. 19: 2375, https://doi.org/10.3390/ijms19082375.Search in Google Scholar PubMed PubMed Central

Luft, J.H. (1966). Fine structures of capillary and endocapillary layer as revealed by ruthenium red. Fed. Proc. 25: 1773–1783.Search in Google Scholar

Ma, Y., Lu, Z., Jia, B., Shi, Y., Dong, J., Jiang, S., and Li, Z. (2022). DNA origami as a nanomedicine for targeted rheumatoid arthritis therapy through reactive oxygen species and nitric oxide scavenging. ACS Nano 16: 12520–12531, https://doi.org/10.1021/acsnano.2c03991.Search in Google Scholar PubMed

Ma, Y., Sannino, D., Linden, J.R., Haigh, S., Zhao, B., Grigg, J.B., Zumbo, P., Dündar, F., Butler, D., Profaci, C.P., et al.. (2023). Epsilon toxin-producing clostridium perfringens colonize the multiple sclerosis gut microbiome overcoming CNS immune privilege. J. Clin. Invest. 133: e163239, https://doi.org/10.1172/jci163239.Search in Google Scholar

Machin, D.R., Bloom, S.I., Campbell, R.A., Phuong, T.T.T., Gates, P.E., Lesniewski, L.A., Rondina, M.T., and Donato, A.J. (2018). Advanced age results in a diminished endothelial glycocalyx. Am. J. Physiol. Heart Circ. Physiol. 315: H531–h539, https://doi.org/10.1152/ajpheart.00104.2018.Search in Google Scholar PubMed PubMed Central

Mahmoud, M., Mayer, M., CancelL, M., Bartosch, A.M., Mathews, R., and Tarbell, J.M. (2021). The glycocalyx core protein Glypican 1 protects vessel wall endothelial cells from stiffness-mediated dysfunction and disease. Cardiovasc. Res. 117: 1592–1605, https://doi.org/10.1093/cvr/cvaa201.Search in Google Scholar PubMed PubMed Central

Mayer, S.A., Aldrich, E.F., Bruder, N., Hmissi, A., Macdonald, R.L., Viarasilpa, T., Marr, A., Roux, S., and Higashida, R.T. (2019). Thick and diffuse subarachnoid Blood as a treatment effect modifier of clazosentan after subarachnoid hemorrhage. Stroke 50: 2738–2744, https://doi.org/10.1161/strokeaha.119.025682.Search in Google Scholar PubMed

McCarthy, K.J. (2020). Syndecan-4: major player or innocent bystander of the endothelial glycocalyx? Kidney Int. 97: 858–860, https://doi.org/10.1016/j.kint.2020.01.040.Search in Google Scholar PubMed PubMed Central

McConnell, E.D., Wei, H.S., Reitz, K.M., Kang, H., Takano, T., Vates, G.E., and Nedergaard, M. (2016). Cerebral microcirculatory failure after subarachnoid hemorrhage is reversed by hyaluronidase. J. Cereb. Blood Flow Metab. 36: 1537–1552, https://doi.org/10.1177/0271678x15608389.Search in Google Scholar PubMed PubMed Central

Mitra, R., Nersesyan, A., Pentland, K., Melin, M.M., Levy, R.M., and Ebong, E.E. (2022). Diosmin and its glycocalyx restorative and anti-inflammatory effects on injured blood vessels. Faseb J. 36: e22630, https://doi.org/10.1096/fj.202200053rr.Search in Google Scholar PubMed

Morsing, S.K.H., Rademakers, T., Brouns, S.L.N., Stalborch, A.D.V., Donners, M., and van Buul, J.D. (2021). ADAM10-mediated cleavage of ICAM-1 is involved in neutrophil transendothelial migration. Cells 10: 232, https://doi.org/10.3390/cells10020232.Search in Google Scholar PubMed PubMed Central

Nägga, K., Hansson, O., van Westen, D., Minthon, L., and Wennström, M. (2014). Increased levels of hyaluronic acid in cerebrospinal fluid in patients with vascular dementia. J. Alzheimers Dis. 42: 1435–1441, https://doi.org/10.3233/jad-141200.Search in Google Scholar

Nukala, S.B., Jousma, J., Yan, G., Han, Z., Kwon, Y., Cho, Y., Liu, C., Gagnon, K., Pinho, S., Rehman, J., et al.. (2023). Modulation of lncRNA links endothelial glycocalyx to vascular dysfunction of tyrosine kinase inhibitor. Cardiovasc. Res. 119: 1997–2013, https://doi.org/10.1093/cvr/cvad087.Search in Google Scholar PubMed PubMed Central

O’Neil, M., Demeulenaere, S.K., DeChristopher, P.J., Holthaus, E., Jeske, W., Glynn, L., Husain, A., and Muraskas, J. (2024). Syndecan-1 level, a marker of endothelial glycocalyx degradation, is associated with fetal exposure to chorioamnionitis and is a potential biomarker for early-onset neonatal sepsis. Pediatr. Dev. Pathol. 14: 10935266241235504, https://doi.org/10.1177/10935266241235504.Search in Google Scholar PubMed

Ostrowski, S.R. and Johansson, P.I. (2012). Endothelial glycocalyx degradation induces endogenous heparinization in patients with severe injury and early traumatic coagulopathy. J. Trauma Acute Care Surg. 73: 60–66, https://doi.org/10.1097/ta.0b013e31825b5c10.Search in Google Scholar

Parton, R.G. and Simons, K. (2007). The multiple faces of caveolae. Nat. Rev. Mol. Cell Biol. 8: 185–194, https://doi.org/10.1038/nrm2122.Search in Google Scholar PubMed

Pei, S., Zheng, D., Wang, Z., Hu, X., Pan, S., and Wang, H. (2018). Elevated soluble syndecan-1 levels in neuromyelitis optica are associated with disease severity. Cytokine 111: 140–145, https://doi.org/10.1016/j.cyto.2018.08.017.Search in Google Scholar PubMed

Peng, N., Geng, Y., Ouyang, J., Liu, S., Yuan, F., Wan, Y., Chen, W., Yu, B., Tang, Y., Su, L., et al.. (2023). Endothelial glycocalyx injury is involved in heatstroke-associated coagulopathy and protected by N-acetylcysteine. Front. Immunol. 14: 1159195, https://doi.org/10.3389/fimmu.2023.1159195.Search in Google Scholar PubMed PubMed Central

Piotti, A., Novelli, D., Meessen, J., Ferlicca, D., Coppolecchia, S., Marino, A., Salati, G., Savioli, M., Grasselli, G., Bellani, G., et al.. (2021). Endothelial damage in septic shock patients as evidenced by circulating syndecan-1, sphingosine-1-phosphate and soluble VE-cadherin: a substudy of ALBIOS. Crit. Care 25: 113, https://doi.org/10.1186/s13054-021-03545-1.Search in Google Scholar PubMed PubMed Central

Pries, A.R., Secomb, T.W., and Gaehtgens, P. (2000). The endothelial surface layers. Pflugers Arch. 440: 653–666, https://doi.org/10.1007/s004240000307.Search in Google Scholar PubMed

Rapraeger, A., Jalkanen, M., Endo, E., Koda, J., and Bernfield, M. (1985). The cell surface proteoglycan from mouse mammary epithelial cells bears chondroitin sulfate and heparan sulfate glycosaminoglycans. J. Biol. Chem. 260: 11046–11052, https://doi.org/10.1016/s0021-9258(17)39146-9.Search in Google Scholar

Reitsma, S., Slaaf, D.W., Vink, H., van Zandvoort, M.A., and oude Egbrink, M.G. (2007). The endothelial glycocalyx: composition, functions, and visualization. Pflugers Arch. 454: 345–359, https://doi.org/10.1007/s00424-007-0212-8.Search in Google Scholar PubMed PubMed Central

Rienks, M., Carai, P., van Teeffelen, J., Eskens, B., Verhesen, W., Hemmeryckx, B., Johnson, D.M., van Leeuwen, R., Jones, E.A., Heymans, S., et al.. (2018). SPARC preserves endothelial glycocalyx integrity, and protects against adverse cardiac inflammation and injury during viral myocarditis. Matrix Biol. 74: 21–34, https://doi.org/10.1016/j.matbio.2018.04.015.Search in Google Scholar PubMed

Rosenberg, R.D., Shworak, N.W., Liu, J., Schwartz, J.J., and Zhang, L. (1997). Heparan sulfate proteoglycans of the cardiovascular system. Specific structures emerge but how is synthesis regulated? J. Clin. Invest. 99: 2062–2070, https://doi.org/10.1172/jci119377.Search in Google Scholar

Santa-Maria, A.R., Walter, F.R., Figueiredo, R., Kincses, A., Vigh, J.P., Heymans, M., Culot, P., Winter, M., Gosselet, F., Dér, A., et al.. (2021). Flow induces barrier and glycocalyx-related genes and negative surface charge in a lab-on-a-chip human blood-brain barrier model. J. Cereb. Blood Flow Metab. 41: 2201–2215, https://doi.org/10.1177/0271678x21992638.Search in Google Scholar PubMed PubMed Central

Schaeffer, S. and Iadecola, C. (2021). Revisiting the neurovascular unit. Nat. Neurosci. 24: 1198–1209, https://doi.org/10.1038/s41593-021-00904-7.Search in Google Scholar PubMed PubMed Central

Schenck, H., Netti, E., Teernstra, O., De Ridder, I., Dings, J., Niemelä, M., Temel, Y., Hoogland, G., and Haeren, R. (2021). The role of the glycocalyx in the pathophysiology of subarachnoid hemorrhage-induced delayed cerebral ischemia. Front. Cell Dev. Biol. 9: 731641, https://doi.org/10.3389/fcell.2021.731641.Search in Google Scholar PubMed PubMed Central

Schick, V.C., Neumann, T., Illerhaus, A., Timmer, M., Fuchs, A., Grau, S., and Annecke, T. (2023). Release of hyaluronan in aneurysmal subarachnoid hemorrhage and cerebral vasospasm: a pilot study indicating a shedding of the endothelial glycocalyx. J. Neurosurg. Anesthesiol. 35: 232–237, https://doi.org/10.1097/ana.0000000000000814.Search in Google Scholar

Stoddart, P., Satchell, S.C., and Ramnath, R. (2022). Cerebral microvascular endothelial glycocalyx damage, its implications on the blood-brain barrier and a possible contributor to cognitive impairment. Brain Res. 1780: 147804, https://doi.org/10.1016/j.brainres.2022.147804.Search in Google Scholar PubMed

Sun, L., Wang, L., Ye, K.X., Wang, S., Zhang, R., Juan, Z., Feng, L., and Min, S. (2023). Endothelial glycocalyx in aging and age-related diseases. Aging Dis. 14: 1606–1617, https://doi.org/10.14336/ad.2023.0131.Search in Google Scholar PubMed PubMed Central

Tomizawa, Y., Yokoyama, K., Saiki, S., Takahashi, T., Matsuoka, J., and Hattori, N. (2012). Blood-brain barrier disruption is more severe in neuromyelitis optica than in multiple sclerosis and correlates with clinical disability. J. Int. Med. Res. 40: 1483–1491, https://doi.org/10.1177/147323001204000427.Search in Google Scholar PubMed

Tsao, C.W., Aday, A.W., Almarzooq, Z.I., Anderson, C.A.M., Arora, P., Avery, C.L., Baker-Smith, C.M., Beaton, A.Z., Boehme, A.K., Buxton, A.E., et al.. (2023). Heart disease and stroke statistics-2023 update: a report from the american heart association. Circulation 147: E93–E621, https://doi.org/10.1161/cir.0000000000001123.Search in Google Scholar

Vahldieck, C., Cianflone, E., Fels, B., Löning, S., Depelmann, P., Sabatino, J., Salerno, N., Karsten, C.M., Kusche-Vihrog, K., Sun, D., et al.. (2023). Endothelial glycocalyx and cardiomyocyte damage is prevented by recombinant syndecan-1 in acute myocardial infarction. Am. J. Pathol. 193: 474–492, https://doi.org/10.1016/j.ajpath.2022.12.009.Search in Google Scholar PubMed PubMed Central

van Steen, A.C.I., Grönloh, M.L.B., Joosten, S., van Alphen, F., van den Biggelaar, M., Nolte, M.A., Spaargaren, M., van Buul, J.D., and Schoppmeyer, R. (2023). Endothelial ICAM-1 adhesome recruits CD44 for optimal transcellular migration of human CTLs. J. Immunol. 211: 377–388, https://doi.org/10.4049/jimmunol.2200761.Search in Google Scholar PubMed

Vink, H. and Duling, B.R. (1996). Identification of distinct luminal domains for macromolecules, erythrocytes, and leukocytes within mammalian capillaries. Circ. Res. 79: 581–589, https://doi.org/10.1161/01.res.79.3.581.Search in Google Scholar PubMed

Wang, G., Tiemeier, G.L., van den Berg, B.M., and Rabelink, T.J. (2020). Endothelial glycocalyx hyaluronan: regulation and role in prevention of diabetic complications. Am. J. Pathol. 190: 781–790, https://doi.org/10.1016/j.ajpath.2019.07.022.Search in Google Scholar PubMed

Wang, G., Zhang, H., Liu, D., and Wang, X. (2022). Resuscitation fluids as drugs: targeting the endothelial glycocalyx. Chin Med. J. 135: 137–144, https://doi.org/10.1097/cm9.0000000000001869.Search in Google Scholar PubMed PubMed Central

Wang, L., Wang, J., Ren, G., Sun, S., Nishikawa, K., Yu, J., and Zhang, C. (2023). Ameliorative effects of the Coptis inflorescence extract against lung injury in diabetic mice by regulating AMPK/NEU1 signaling. Phytomedicine 118: 154963, https://doi.org/10.1016/j.phymed.2023.154963.Search in Google Scholar PubMed

Yang, H., Zhu, L., Gu, Y., Kong, X., Yan, L., Chen, M., Xie, X., Luo, J., and Chen, S. (2019). Berberine inhibits low shear stress-induced glycocalyx degradation via modulating AMPK and p47(phox)/Hyal2 signal pathway. Eur. J. Pharmacol. 856: 172413, https://doi.org/10.1016/j.ejphar.2019.172413.Search in Google Scholar PubMed

Yang, R., Chen, M., Zheng, J., Li, X., and Zhang, X. (2021). The Role of heparin and glycocalyx in blood-brain barrier dysfunction. Front. Immunol. 12: 754141, https://doi.org/10.3389/fimmu.2021.754141.Search in Google Scholar PubMed PubMed Central

Yao, L., He, F., Zhao, Q., Li, D., Fu, S., Zhang, M., Zhang, X., Zhou, B., and Wang, L. (2023). Spatial Multiplexed protein profiling of cardiac ischemia-reperfusion injury. Circ. Res. 133: 86–103, https://doi.org/10.1161/circresaha.123.322620.Search in Google Scholar

Yavarpour-Bali, H., Ghasemi-Kasman, M., and Pirzadeh, M. (2019). Curcumin-loaded nanoparticles: a novel therapeutic strategy in treatment of central nervous system disorders. Int. J. Nanomed. 14: 4449–4460, https://doi.org/10.2147/ijn.s208332.Search in Google Scholar PubMed PubMed Central

Yin, T., Hao, J., Jiang, Q., Xu, X., Xu, B., Lv, H., Liu, W., Xiao, Y., Jiao, L., Wang, J., et al.. (2022). Dynamics of intracranial and peripheral plasma syndecan-1 after ischemic stroke with large vessel occlusion. CNS Neurosci. Ther. 28: 1648–1650, https://doi.org/10.1111/cns.13898.Search in Google Scholar PubMed PubMed Central

Yoon, J.H., Shin, P., Joo, J., Kim, G.S., Oh, W.Y., and Jeong, Y. (2022). Increased capillary stalling is associated with endothelial glycocalyx loss in subcortical vascular dementia. J. Cereb. Blood Flow Metab. 42: 1383–1397, https://doi.org/10.1177/0271678x221076568.Search in Google Scholar

Yu, W.Q., Zhang, S.Y., Fu, S.Q., Fu, Q.H., Lu, W.N., Zhang, J., Liang, Z.Y., Zhang, Y., and Liang, T.B. (2019). Dexamethasone protects the glycocalyx on the kidney microvascular endothelium during severe acute pancreatitis. J. Zhejiang Univ., Sci., B 20: 355–362, https://doi.org/10.1631/jzus.b1900006.Search in Google Scholar

Zhang, D., Li, L., Chen, Y., Ma, J., Yang, Y., Aodeng, S., Cui, Q., Wen, K., Xiao, M., Xie, J., et al.. (2021a). Syndecan-1, an indicator of endothelial glycocalyx degradation, predicts outcome of patients admitted to an ICU with COVID-19. Mol. Med. 27: 151, https://doi.org/10.1186/s10020-021-00412-1.Search in Google Scholar PubMed PubMed Central

Zhang, Q., Pei, S., Zhou, Z., Wang, Z., Peng, Y., Chen, J., and Wang, H. (2021b). High level of serum and cerebrospinal fluid of heparan sulfate and hyaluronic acid might be a biomarker ofseverity of neuromyelitis optica. Front. Immunol. 12: 705536, https://doi.org/10.3389/fimmu.2021.705536.Search in Google Scholar PubMed PubMed Central

Zhang, D., Qi, B.Y., Zhu, W.W., Huang, X., and Wang, X.Z. (2020a). Crocin alleviates lipopolysaccharide-induced acute respiratory distress syndrome by protecting against glycocalyx damage and suppressing inflammatory signaling pathways. Inflamm. Res. 69: 267–278, https://doi.org/10.1007/s00011-019-01314-z.Search in Google Scholar PubMed PubMed Central

Zhang, H., Tang, W., Wang, S., Zhang, J., and Fan, X. (2020b). Tetramethylpyrazine inhibits platelet adhesion and inflammatory response in vascular endothelial cells by inhibiting P38 MAPK and NF-κB signaling pathways. Inflammation 43: 286–297, https://doi.org/10.1007/s10753-019-01119-6.Search in Google Scholar PubMed

Zhang, Y.N., Wu, Q., Zhang, N.N., and Chen, H.S. (2023). Ischemic preconditioning alleviates cerebral ischemia-reperfusion injury by interfering with glycocalyx. Transl. Stroke Res. 14: 929–940, https://doi.org/10.1007/s12975-022-01081-w.Search in Google Scholar PubMed

Zhao, F., Wang, R., Huang, Y., Li, L., Zhong, L., Hu, Y., Han, Z., Fan, J., Liu, P., Zheng, Y., et al.. (2022). Elevated plasma syndecan-1 as glycocalyx injury marker predicts unfavorable outcomes after rt-PA intravenous thrombolysis in acute ischemic stroke. Front. Pharmacol. 13: 949290, https://doi.org/10.3389/fphar.2022.949290.Search in Google Scholar PubMed PubMed Central

Zhao, F., Zhong, L., and Luo, Y. (2021). Endothelial glycocalyx as an important factor in composition of blood-brain barrier. CNS Neurosci. Ther. 27: 26–35, https://doi.org/10.1111/cns.13560.Search in Google Scholar PubMed PubMed Central

Zhu, J., Li, Z., Ji, Z., Wu, Y., He, Y., Liu, K., Chang, Y., Peng, Y., Lin, Z., Wang, S., et al.. (2022). Glycocalyx is critical for blood-brain barrier integrity by suppressing caveolin1-dependent endothelial transcytosis following ischemic stroke. Brain Pathol. 32: e13006, https://doi.org/10.1111/bpa.13006.Search in Google Scholar PubMed PubMed Central

Zou, Z., Li, L., Li, Q., Zhao, P., Zhang, K., Liu, C., Cai, D., Maegele, M., Gu, Z., and Huang, Q. (2022). The role of S100B/RAGE-enhanced ADAM17 activation in endothelial glycocalyx shedding after traumatic brain injury. J. Neuroinflammation 19: 46, https://doi.org/10.1186/s12974-022-02412-2.Search in Google Scholar PubMed PubMed Central

Zou, Z., Li, L., Schäfer, N., Huang, Q., Maegele, M., and Gu, Z. (2021). Endothelial glycocalyx in traumatic brain injury associated coagulopathy: potential mechanisms and impact. J. Neuroinflammation 18: 134, https://doi.org/10.1186/s12974-021-02192-1.Search in Google Scholar PubMed PubMed Central