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大肠杆菌K1与血脑屏障细胞致病机制研究进展
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Abstract:
细菌性脑膜炎是严重危害人类健康的公共健康卫生问题,尤其在儿童甚至是新生儿发病较多,且容易引发神经系统后遗症。大肠杆菌作为细菌性脑膜炎的主要致病病原体,其引起细菌性脑膜炎的发病机制仍未完全明确,病原体与宿主相互作用机制仍有许多学者研究探讨。血脑屏障作为大脑的保护屏障,其通透性改变进而引起血脑屏障结构破坏,大肠杆菌继续定植在脑膜甚至脑实质繁殖引发一系列免疫炎症反应,以此来致病。血脑屏障组成细胞种类较多,并且细胞间也会存在信号分子的交流作用,因此,大肠杆菌细菌性脑膜炎的发病机制极其复杂,理清分子生物水平的作用水平,并提出针对性的预防及治疗手段有非常深远的意义。
Bacterial meningitis is a public health problem that seriously endangers human health, especially in children and even neonates, and is prone to cause neurological sequelae. As the main pathogen of bacterial meningitis, the pathogenesis of Escherichia coli is still not fully understood, and the pathogen-host interaction mechanism is still being studied by many scholars. As a protective barrier of the brain, the permeability of the blood-brain barrier changes and then causes the destruction of the blood-brain barrier structure, and Escherichia coli continues to colonize the meninges and even the brain parenchyma to multiply, triggering a series of immune and inflammatory responses, so as to cause disease. Therefore, the pathogenesis of bacterial meningitis of E. coli is extremely complex, and it is of far-reaching significance to clarify the level of action at the molecular biological level and propose targeted prevention and treatment methods.
[1] | Bundy, L.M., Rajnik, M. and Noor, A. (2013) Neonatal Meningitis. StatPearls, Treasure Island. |
[2] | Baud, O. and Aujard, Y. (2013) Neonatal Bacterial Meningitis. Handbook of Clinical Neurology, 112, 1109-1113. https://doi.org/10.1016/B978-0-444-52910-7.00030-1 |
[3] | Ouchenir, L., Renaud, C., Khan, S., et al. (2017) The Epidemiology, Management, and Outcomes of Bacterial Meningitis in Infants. Pediatrics, 140, e20170476. https://doi.org/10.1542/peds.2017-0476 |
[4] | 廖镇宇, 常淑婷, 肖勇, 等. 早产儿细菌性脑膜炎临床分析[J]. 中国感染控制杂志, 2022, 21(10): 1006-1014. |
[5] | Zhai, Q., Li, S., Zhang, L., et al. (2022) Changes in Pathogens of Neonatal Bacterial Meningitis over the Past 12 Years: A Single-Center Retrospective Study. Translational Pediatrics, 11, 1595-1603. https://doi.org/10.21037/tp-22-103 |
[6] | Ueno, M., Chiba, Y., Murakami, R., et al. (2016) Blood-Brain Barrier and Blood-Cerebrospinal Fluid Barrier in Normal and Pathological Conditions. Brain Tumor Pathology, 33, 89-96. https://doi.org/10.1007/s10014-016-0255-7 |
[7] | Gawdi, R., Shumway, K.R. and Emmady, P.D. (2023) Physiology, Blood Brain Barrier. StatPearls, Treasure Island. |
[8] | Kim, B.J., Hancock, B.M., Bermudez, A., et al. (2015) Bacterial Induction of Snail1 Contributes to Blood-Brain Barrier Disruption. Journal of Clinical Investigation, 125, 2473-83. https://doi.org/10.1172/JCI74159 |
[9] | Deshayes De Cambronne, R., Fouet, A., Picart, A., et al. (2021) CC17 Group B Streptococcus Exploits Integrins for Neonatal Meningitis Development. Journal of Clinical Investigation, 131, e136737. https://doi.org/10.1172/JCI136737 |
[10] | Zhu, N., Liu, W., Prakash, A., et al. (2020) Targeting E. coli Invasion of the Blood-Brain Barrier for Investigating the Pathogenesis and Therapeutic Development of E. coli Meningitis. Cellular Microbiology, 22, e13231. https://doi.org/10.1111/cmi.13231 |
[11] | Doran, K.S., Fulde, M., Gratz, N., et al. (2016) Host-Pathogen Interactions in Bacterial Meningitis. Acta Neuropathologica, 131, 185-209. https://doi.org/10.1007/s00401-015-1531-z |
[12] | Gong, Z., Gao, X., Li, Y., et al. (2022) α7 Nicotinic Acetylcholine Receptor Antagonists Prevent Meningitic Escherichia coli-Induced Blood-Brain Barrier Disruptions by Targeting the CISH/JAK2/STAT5b Axis. Biomedicines, 10, Article 2358. https://doi.org/10.3390/biomedicines10102358 |
[13] | He, X., Wang, L., Liu, L., et al. (2021) Endogenous α7 NAChR Agonist SLURP1 Facilitates Escherichia coli K1 Crossing the Blood-Brain Barrier. Frontiers in Immunology, 12, Article 745854. https://doi.org/10.3389/fimmu.2021.745854 |
[14] | Liu, R., Wu, C., Li, L., et al. (2019) CD48 and α7 Nicotinic Acetylcholine Receptor Synergistically Regulate FimH-Mediated Escherichia coli K1 Penetration and Neutrophil Transmigration across Human Brain Microvascular Endothelial Cells. The Journal of Infectious Diseases, 219, 470-479. https://doi.org/10.1093/infdis/jiy531 |
[15] | Fan, Y., Sun, H., Yang, W., et al. (2022) YbdO Promotes the Pathogenicity of Escherichia coli K1 by Regulating Capsule Synthesis. International Journal of Molecular Sciences, 23, Article 5543. https://doi.org/10.3390/ijms23105543 |
[16] | Fan, Y., Bai, J., Xi, D. and Yang, B. (2022) RpoE Facilitates Stress-Resistance, Invasion, and Pathogenicity of Escherichia coli K1. Microorganisms, 10, Article 879. https://doi.org/10.3390/microorganisms10050879 |
[17] | Loh, L.N., McCarthy, E.M.C., Narang, P., et al. (2017) Escherichia coli K1 Utilizes Host Macropinocytic Pathways for Invasion of Brain Microvascular Endothelial Cells. Traffic, 18, 733-746. https://doi.org/10.1111/tra.12508 |
[18] | Chambers, C.A., Dadelahi, A.S., Moley, C.R., et al. (2022) Nucleotide Receptors Mediate Protection against Neonatal Sepsis and Meningitis Caused by α-Hemolysin Expressing Escherichia coli K1. The FASEB Journal, 36, e22197. https://doi.org/10.1096/fj.202101485R |
[19] | Huang, S.H., Chi, F., Peng, L., et al. (2016) Vimentin, a Novel NF-κB Regulator, Is Required for Meningitic Escherichia coli K1-Induced Pathogen Invasion and PMN Transmigration across the Blood-Brain Barrier. PLOS ONE, 11, e0162641. https://doi.org/10.1371/journal.pone.0162641 |
[20] | Krishnan, S., Chang, A.C., Stoltz, B.M. and Prasadarao, N.V. (2016) Escherichia coli K1 Modulates Peroxisome Proliferator-Activated Receptor γ and Glucose Transporter 1 at the Blood-Brain Barrier in Neonatal Meningitis. The Journal of Infectious Diseases, 214, 1092-1104. https://doi.org/10.1093/infdis/jiw306 |
[21] | Wu, C., Yang, M., Liu, R., et al. (2020) Nicotine Reduces Human Brain Microvascular Endothelial Cell Response to Escherichia coli K1 Infection by Inhibiting Autophagy. Frontiers in Cellular and Infection Microbiology, 10, Article 484. https://doi.org/10.3389/fcimb.2020.00484 |
[22] | Liu, P., Wang, X., Yang, Q., et al. (2022) Collaborative Action of Microglia and Astrocytes Mediates Neutrophil Recruitment to the CNS to Defend Against Escherichia coli K1 Infection. International Journal of Molecular Sciences, 23, Article 6540. https://doi.org/10.3390/ijms23126540 |
[23] | Jha, M.K., Jo, M., Kim, J.H., et al. (2019) Microglia-Astrocyte Crosstalk: An Intimate Molecular Conversation. Neuroscientist, 25, 227-240. https://doi.org/10.1177/1073858418783959 |
[24] | Michael, B.D., Bricio-Moreno, L., Sorensen, E.W., et al. (2020) Astrocyte-and Neuron-Derived CXCL1 Drives Neutrophil Transmigration and Blood-Brain Barrier Permeability in Viral Encephalitis. Cell Reports, 32, Article ID: 108150. https://doi.org/10.1016/j.celrep.2020.108150 |
[25] | Thorsdottir, S., Henriques-Normark, B. and Iovino, F. (2019) The Role of Microglia in Bacterial Meningitis: Inflammatory Response, Experimental Models and New Neuroprotective Therapeutic Strategies. Frontiers in Microbiology, 10, Article 576. https://doi.org/10.3389/fmicb.2019.00576 |
[26] | Diesselberg, C., Ribes, S., Seele, J., Kaufmann, A., et al. (2018) Activin a Increases Phagocytosis of Escherichia coli K1 by Primary Murine Microglial Cells Activated by Toll-Like Receptor Agonists. Journal of Neuroinflammation, 15, Article No. 175. https://doi.org/10.1186/s12974-018-1209-2 |
[27] | Liddelow, S.A., Guttenplan, K.A., Clarke, L.E., et al. (2017) Neurotoxic Reactive Astrocytes Are Induced by Activated Microglia. Nature, 541, 481-487. https://doi.org/10.1038/nature21029 |
[28] | Jo, M., Kim, J.H., Song, G.J., et al. (2017) Astrocytic Orosomucoid-2 Modulates Microglial Activation and Neuroinflammation. Journal of Neuroscience, 37, 2878-2894. https://doi.org/10.1523/JNEUROSCI.2534-16.2017 |
[29] | Molino, Y., Jabès, F., Lacassagne, E., et al. (2014) Setting-Up an in Vitro Model of Rat Blood-Brain Barrier (BBB): A Focus on BBB Impermeability and Receptor-Mediated Transport. Journal of Visualized Experiments, 88, e51278. https://doi.org/10.3791/51278 |
[30] | Bohannon, D.G., Long, D. and Kim, W.K. (2021) Understanding the Heterogeneity of Human Pericyte Subsets in Blood-Brain Barrier Homeostasis and Neurological Diseases. Cells, 10, Article 890. https://doi.org/10.3390/cells10040890 |
[31] | Heymans, M., Figueiredo, R., Dehouck, L., et al. (2020) Contribution of Brain Pericytes in Blood-Brain Barrier Formation and Maintenance: A Transcriptomic Study of Cocultured Human Endothelial Cells Derived from Hematopoietic Stem Cells. Fluids and Barriers of the CNS, 17, Article No. 48. https://doi.org/10.1186/s12987-020-00208-1 |
[32] | Kim, J., Lee, K.T., Lee, J.S., et al. (2021) Fungal Brain Infection Modelled in a Human-Neurovascular-Unit-on-a-Chip with a Functional Blood-Brain Barrier. Nature Biomedical Engineering, 5, 830-846. https://doi.org/10.1038/s41551-021-00743-8 |
[33] | Abbott, N.J., Dolman, D.E., Drndarski, S., et al. (2012) An Improved in Vitro Blood-Brain Barrier Model: Rat Brain Endothelial Cells Co-Cultured with Astrocytes. Methods in Molecular Biology, 814, 415-430. https://doi.org/10.1007/978-1-61779-452-0_28 |
[34] | Gil, E., Venturini, C., Stirling, D., et al. (2022) Pericyte Derived Chemokines Amplify Neutrophil Recruitment across the Cerebrovascular Endothelial Barrier. Methods in Molecular Biology, 13, Article 935798. https://doi.org/10.3389/fimmu.2022.935798 |
[35] | Jansson, D., Rustenhoven, J., Feng, S., et al. (2014) A Role for Human Brain Pericytes in Neuroinflammation. Journal of Neuroinflammation, 11, Article No. 104. https://doi.org/10.1186/1742-2094-11-104 |
[36] | Armulik, A., Genové, G., M?e, M., et al. (2010) Pericytes Regulate the Blood-Brain Barrier. Nature, 468, 557-561. https://doi.org/10.1038/nature09522 |
[37] | Salmeri, M., Motta, C., Anfuso, C.D., et al. (2013) VEGF Receptor-1 Involvement in Pericyte Loss Induced by Escherichia coli in an in Vitro Model of Blood Brain Barrier. Cellular Microbiology, 15, 1367-1384. https://doi.org/10.1111/cmi.12121 |
[38] | Caporarello, N., Olivieri, M., Cristaldi, M., et al. (2018) Blood-Brain Barrier in a Haemophilus influenzae Type A in Vitro Infection: Role of Adenosine Receptors A2A and A2B. Molecular Neurobiology, 55, 5321-5336. https://doi.org/10.1007/s12035-017-0769-y |
[39] | Kim, J., Alejandro, B., Hetman, M., et al. (2020) Zika Virus Infects Pericytes in the Choroid Plexus and Enters the Central Nervous System through the Blood-Cerebrospinal Fluid Barrier. PLOS Pathogens, 16, e1008204. https://doi.org/10.1371/journal.ppat.1008204 |
[40] | Kurlansky, P.A., Sadeghi, A.M., Michler, R.E., et al. (1986) Role of the Carrier Solution in Cyclosporine Pharmacokinetics in the Baboon. The Journal of Heart and Lung Transplantation, 5, 312-316. |
[41] | Zhang, X.W., An, M.X., Huang, Z.K., et al. (2023) Lpp of Escherichia coli K1 Inhibits Host ROS Production to Counteract Neutrophil-Mediated Elimination. Redox Biology, 59, Article ID: 102588. https://doi.org/10.1016/j.redox.2022.102588 |
[42] | Zhang, K., Shi, M.J., Niu, Z., et al. (2019) Activation of Brain Endothelium by Escherichia coli K1 Virulence Factor CglD Promotes Polymorphonuclear Leukocyte Transendothelial Migration. Medical Microbiology and Immunology, 208, 59-68. https://doi.org/10.1007/s00430-018-0560-3 |
[43] | Yang, J., Ma, W., Wu, Y., et al. (2021) O-Acetylation of Capsular Polysialic Acid Enables Escherichia coli K1 Escaping from Siglec-Mediated Innate Immunity and Lysosomal Degradation of E. coli-Containing Vacuoles in Macrophage-Like Cells. Microbiology Spectrum, 9, e0039921. https://doi.org/10.1128/spectrum.00399-21 |
[44] | Chambers, C.A., Lacey, C.A., Brown, D.C., et al. (2021) Nitric Oxide Inhibits Interleukin-1-Mediated Protection against Escherichia coli K1-Induced Sepsis and Meningitis in a Neonatal Murine Model. Immunology & Cell Biology, 99, 596-610. https://doi.org/10.1111/imcb.12445 |
[45] | Chang, A.C., Krishnan, S. and Prasadarao, N.V. (2016) The Effects of Cytotoxic Necrotizing Factor 1 Expression in the Uptake of Escherichia coli K1 by Macrophages and the Onset of Meningitis in Newborn Mice. Virulence, 7, 806-818. https://doi.org/10.1080/21505594.2016.1192730 |
[46] | Shanmuganathan, M.V., Krishnan, S., Fu, X. and Prasadarao, N.V. (2014) Escherichia coli K1 Induces Pterin Production for Enhanced Expression of Fcγ Receptor I to Invade RAW 264.7 Macrophages. Microbes and Infection, 16, 134-141. https://doi.org/10.1016/j.micinf.2013.10.013 |
[47] | Krishnan, S., Liu, F., Abrol, R., et al. (2014) The Interaction of N-Glycans in Fcγ Receptor I α-Chain with Escherichia coli K1 Outer Membrane Protein A for Entry into Macrophages: Experimental and Computational Analysis. Journal of Biological Chemistry, 289, 30937-30949. https://doi.org/10.1074/jbc.M114.599407 |
[48] | Lu, J., Ding, J., Chu, B., et al. (2023) Inactive Trojan Bacteria as Safe Drug Delivery Vehicles Crossing the Blood-Brain Barrier. Nano Letters, 23, 4326-4333. https://doi.org/10.1021/acs.nanolett.3c00563 |
[49] | Chen, H., Zhou, M., Zeng, Y., et al. (2022) Biomimetic Lipopolysaccharide-Free Bacterial Outer Membrane-Functionalized Nanoparticles for Brain-Targeted Drug Delivery. Advanced Science, 9, e2105854. https://doi.org/10.1002/advs.202105854 |
[50] | Zhang, J., Sun, H., Gao, C., et al. (2021) Development of a Chitosan-Modified PLGA Nanoparticle Vaccine for Protection against Escherichia coli K1 Caused Meningitis in Mice. Journal of Nanobiotechnology, 19, Article No. 69. https://doi.org/10.1186/s12951-021-00812-9 |
[51] | Masri, A., Khan, N.A., Zoqratt, M.Z.H.M., et al. (2021) Transcriptome Analysis of Escherichia coli K1 after Therapy with Hesperidin Conjugated with Silver Nanoparticles. BMC Microbiology, 21, Article No. 51. https://doi.org/10.1186/s12866-021-02097-2 |
[52] | Gu, H., Liao, Y., Zhang, J., et al. (2018) Rational Design and Evaluation of an Artificial Escherichia coli K1 Protein Vaccine Candidate Based on the Structure of OmpA. Frontiers in Cellular and Infection Microbiology, 8, Article 172. https://doi.org/10.3389/fcimb.2018.00172 |
[53] | Pons, S., Frapy, E., Sereme, Y., et al. (2023) A High-Throughput Sequencing Approach Identifies Immunotherapeutic Targets for Bacterial Meningitis in Neonates. eBioMedicine, 88, Article ID: 104439. https://doi.org/10.1016/j.ebiom.2023.104439 |
[54] | Xu, X., Zhang, L., Cai, Y., et al. (2020) Inhibitor Discovery for the E. coli Meningitis Virulence Factor IbeA from Homology Modeling and Virtual Screening. Journal of Computer-Aided Molecular Design, 34, 11-25. https://doi.org/10.1007/s10822-019-00250-8 |
[55] | Zeng, Q., He, X.L., Xiao, H.S., et al. (2017) Lactobacillus rhamnosus GG Conditioned Medium Prevents E. coli Meningitis by Inhibiting Nuclear Factor-κB Pathway. Journal of Southern Medical University, 37, 24-29. |
[56] | Yu, J.Y., Zhang, B., Peng, L., et al. (2015) Repositioning of Memantine as a Potential Novel Therapeutic Agent against Meningitic E. coli-Induced Pathogenicities through Disease-Associated α7 Cholinergic Pathway and RNA Sequencing-Based Transcriptome Analysis of Host Inflammatory Responses. PLOS ONE, 10, e0121911. https://doi.org/10.1371/journal.pone.0121911 |
[57] | Krishnan, S., Shanmuganathan, M.V., Behenna, D., et al. (2014) Angiotensin II Receptor Type 1—A Novel Target for Preventing Neonatal Meningitis in Mice by Escherichia coli K1. The Journal of Infectious Diseases, 209, 409-419. https://doi.org/10.1093/infdis/jit499 |