Scientific Papers

Proteomic interrogation of the meninges reveals the molecular identities of structural components and regional distinctions along the CNS axis | Fluids and Barriers of the CNS


  • Abbritti RV, Polito F, Cucinotta M, Lo Giudice C, Caffo M, Tomasello C, Germano A, Aguennouz M. Meningiomas and proteomics: focus on new potential biomarkers and molecular pathways. Cancer Genomics Proteomics. 2016;13(5):369–79.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Achtstatter T, Fouquet B, Rungger-Brandle E, Franke WW. Cytokeratin filaments and desmosomes in the epithelioid cells of the perineurial and arachnoidal sheaths of some vertebrate species. Differentiation. 1989;40(2):129–49. https://doi.org/10.1111/j.1432-0436.1989.tb00822.x.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Aguilan JT, Kulej K, Sidoli S. Guide for protein fold change and p-value calculation for non-experts in proteomics. Mol Omics. 2020;16(6):573–82. https://doi.org/10.1039/d0mo00087f.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Alcolado R, Weller RO, Parrish EP, Garrod D. The cranial arachnoid and pia mater in man: anatomical and ultrastructural observations. Neuropathol Appl Neurobiol. 1988;14(1):1–17. https://doi.org/10.1111/j.1365-2990.1988.tb00862.x.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Alers JC, Krijtenburg PJ, Vissers KJ, van Dekken H. Effect of bone decalcification procedures on DNA in situ hybridization and comparative genomic hybridization. EDTA is highly preferable to a routinely used acid decalcifier. J Histochem Cytochem. 1999;47(5):703–10. https://doi.org/10.1177/002215549904700512.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Alves de Lima K, Rustenhoven J, Kipnis J. Meningeal immunity and its function in maintenance of the central nervous system in health and disease. Annu Rev Immunol. 2020;38:597–620. https://doi.org/10.1146/annurev-immunol-102319-103410.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Anderson DR. ltrastructure of meningeal sheaths. Normal human and monkey optic nerves. Arch Ophthalmol. 1969;82(5):659–74. https://doi.org/10.1001/archopht.1969.00990020653015.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Anlar B, Gunel-Ozcan A. Tenascin-R: role in the central nervous system. Int J Biochem Cell Biol. 2012;44(9):1385–9. https://doi.org/10.1016/j.biocel.2012.05.009.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Arseni L, Lombardi A, Orioli D. From structure to phenotype: impact of collagen alterations on human health. Int J Mol Sci. 2018. https://doi.org/10.3390/ijms19051407.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G. Gene ontology: tool for the unification of biology. The gene ontology consortium. Nat Genet. 2000;25(1):25–9. https://doi.org/10.1038/75556.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Aszodi A, Chan D, Hunziker E, Bateman JF, Fassler R. Collagen II is essential for the removal of the notochord and the formation of intervertebral discs. J Cell Biol. 1998;143(5):1399–412. https://doi.org/10.1083/jcb.143.5.1399.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Benko N, Luke E, Alsanea Y, Coats B. Spatial distribution of human arachnoid trabeculae. J Anat. 2020;237(2):275–84. https://doi.org/10.1111/joa.13186.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bifari F, Berton V, Pino A, Kusalo M, Malpeli G, Di Chio M, Bersan E, Amato E, Scarpa A, Krampera M, Fumagalli G, Decimo I. Meninges harbor cells expressing neural precursor markers during development and adulthood. Front Cell Neurosci. 2015;9:383. https://doi.org/10.3389/fncel.2015.00383.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bolte AC, Shapiro DA, Dutta AB, Ma WF, Bruch KR, Kovacs MA, Royo Marco A, Ennerfelt HE, Lukens JR. The meningeal transcriptional response to traumatic brain injury and aging. Elife. 2023. https://doi.org/10.7554/eLife.81154.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bonifasi-Lista C, Lake SP, Small MS, Weiss JA. Viscoelastic properties of the human medial collateral ligament under longitudinal, transverse and shear loading. J Orthop Res. 2005;23(1):67–76. https://doi.org/10.1016/j.orthres.2004.06.002.

    Article 
    PubMed 

    Google Scholar
     

  • Brioschi S, Wang WL, Peng V, Wang M, Shchukina I, Greenberg ZJ, Bando JK, Jaeger N, Czepielewski RS, Swain A, Mogilenko DA, Beatty WL, Bayguinov P, Fitzpatrick JAJ, Schuettpelz LG, Fronick CC, Smirnov I, Kipnis J, Shapiro VS, Wu GF, Gilfillan S, Cella M, Artyomov MN, Kleinstein SH, Colonna M. Heterogeneity of meningeal B cells reveals a lymphopoietic niche at the CNS borders. Science. 2021. https://doi.org/10.1126/science.abf9277.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Brown DA, Sawchenko PE. Time course and distribution of inflammatory and neurodegenerative events suggest structural bases for the pathogenesis of experimental autoimmune encephalomyelitis. J Comp Neurol. 2007;502(2):236–60. https://doi.org/10.1002/cne.21307.

    Article 
    PubMed 

    Google Scholar
     

  • Cha JH, Wee HJ, Seo JH, Ahn BJ, Park JH, Yang JM, Lee SW, Lee OH, Lee HJ, Gelman IH, Arai K, Lo EH, Kim KW. Prompt meningeal reconstruction mediated by oxygen-sensitive AKAP12 scaffolding protein after central nervous system injury. Nat Commun. 2014;5:4952. https://doi.org/10.1038/ncomms5952.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Chait BT. Chemistry. Mass spectrometry: bottom-up or top-down? Science. 2006;314(5796):65–6. https://doi.org/10.1126/science.1133987.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Charrier EE, Janmey PA. Mechanical properties of intermediate filament proteins. Methods Enzymol. 2016;568:35–57. https://doi.org/10.1016/bs.mie.2015.09.009.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Chen Y, Yang S, Lovisa S, Ambrose CG, McAndrews KM, Sugimoto H, Kalluri R. Type-I collagen produced by distinct fibroblast lineages reveals specific function during embryogenesis and Osteogenesis Imperfecta. Nat Commun. 2021;12(1):7199. https://doi.org/10.1038/s41467-021-27563-3.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Coles JA, Myburgh E, Brewer JM, McMenamin PG. Where are we? The anatomy of the murine cortical meninges revisited for intravital imaging, immunology, and clearance of waste from the brain. Prog Neurobiol. 2017;156:107–48. https://doi.org/10.1016/j.pneurobio.2017.05.002.

    Article 
    PubMed 

    Google Scholar
     

  • Coles JA, Stewart-Hutchinson PJ, Myburgh E, Brewer JM. The mouse cortical meninges are the site of immune responses to many different pathogens, and are accessible to intravital imaging. Methods. 2017;127:53–61. https://doi.org/10.1016/j.ymeth.2017.03.020.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Conley Natividad G, Theodossiou SK, Schiele NR, Murdoch GK, Tsamis A, Tanner B, Potirniche G, Mortazavi M, Vorp DA, Martin BA. Ex-vivo quantification of ovine pia arachnoid complex biomechanical properties under uniaxial tension. Fluids Barriers CNS. 2020;17(1):68. https://doi.org/10.1186/s12987-020-00229-w.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Cox J, Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol. 2008;26(12):1367–72. https://doi.org/10.1038/nbt.1511.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Cragg BG. Ultrastructural features of human cerebral cortex. J Anat. 1976;121(2):331–62.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Cugurra A, Mamuladze T, Rustenhoven J, Dykstra T, Beroshvili G, Greenberg ZJ, Baker W, Papadopoulos Z, Drieu A, Blackburn S, Kanamori M, Brioschi S, Herz J, Schuettpelz LG, Colonna M, Smirnov I, Kipnis J. Skull and vertebral bone marrow are myeloid cell reservoirs for the meninges and CNS parenchyma. Science. 2021. https://doi.org/10.1126/science.abf7844.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Damjanov I. Antibodies to intermediate filaments and histogenesis. Lab Invest. 1982;47(3):215–7.

    CAS 
    PubMed 

    Google Scholar
     

  • Dasgupta K, Jeong J. Developmental biology of the meninges. Genesis. 2019;57(5):e23288. https://doi.org/10.1002/dvg.23288.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Decimo I, Fumagalli G, Berton V, Krampera M, Bifari F. Meninges: from protective membrane to stem cell niche. Am J Stem Cells. 2012;1(2):92–105.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Derk J, Jones HE, Como C, Pawlikowski B, Siegenthaler JA. Living on the edge of the CNS: meninges cell diversity in health and disease. Front Cell Neurosci. 2021;15:703944. https://doi.org/10.3389/fncel.2021.703944.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • DeSisto J, O’Rourke R, Jones HE, Pawlikowski B, Malek AD, Bonney S, Guimiot F, Jones KL, Siegenthaler JA. Single-Cell transcriptomic analyses of the developing meninges reveal meningeal fibroblast diversity and function. Dev Cell. 2020;54(1):43–59. https://doi.org/10.1016/j.devcel.2020.06.009.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Di Marco BR, Fitzpatrick Z, Clatworthy MR. The gut-meningeal immune axis: priming brain defense against the most likely invaders. J Exp Med. 2022. https://doi.org/10.1084/jem.20211520.

    Article 

    Google Scholar
     

  • DiTommaso T, Cottle DL, Pearson HB, Schluter H, Kaur P, Humbert PO, Smyth IM. Keratin 76 is required for tight junction function and maintenance of the skin barrier. PLoS Genet. 2014;10(10):e1004706. https://doi.org/10.1371/journal.pgen.1004706.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • El Ayachi I, Fernandez C, Baeza N, De Paula AM, Pesheva P, Figarella-Branger D. Spatiotemporal distribution of tenascin-R in the developing human cerebral cortex parallels neuronal migration. J Comp Neurol. 2011;519(12):2379–89. https://doi.org/10.1002/cne.22632.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Fan B, Bordigari G, Flammer J, Killer HE, Meyer P, Neutzner A. Meningothelial cells participate in immunological processes in the cerebrospinal fluid. J Neuroimmunol. 2012;244(1):45–50. https://doi.org/10.1016/j.jneuroim.2011.12.027.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Fuchs E, Weber K. Intermediate filaments: structure, dynamics, function, and disease. Annu Rev Biochem. 1994;63:345–82. https://doi.org/10.1146/annurev.bi.63.070194.002021.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Fujiyoshi T, Cheng KC, Krug MS, Yoo TJ. Molecular basis of type II collagen autoimmune disease: observations of arthritis, auricular chondritis and tympanitis in mice. ORL J Otorhinolaryngol Relat Spec. 1997;59(4):215–29. https://doi.org/10.1159/000276942.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Galambos JT, Hollingsworth MA Jr, Falek A, Warren WD, McCain JR. The rate of synthesis of glycosaminoglycans and collagen by fibroblasts cultured from adult human liver biopsies. J Clin Invest. 1977;60(1):107–14. https://doi.org/10.1172/JCI108746.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gregorio I, Braghetta P, Bonaldo P, Cescon M. Collagen VI in healthy and diseased nervous system. Dis Model Mech. 2018. https://doi.org/10.1242/dmm.032946.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Haines DE. On the question of a subdural space. Anat Rec. 1991;230(1):3–21. https://doi.org/10.1002/ar.1092300103.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Hayashi M, Ninomiya Y, Hayashi K, Linsenmayer TF, Olsen BR, Trelstad RL. Secretion of collagen types I and II by epithelial and endothelial cells in the developing chick cornea demonstrated by in situ hybridization and immunohistochemistry. Development. 1988;103(1):27–36. https://doi.org/10.1242/dev.103.1.27.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Herisson F, Frodermann V, Courties G, Rohde D, Sun Y, Vandoorne K, Wojtkiewicz GR, Masson GS, Vinegoni C, Kim J, Kim DE, Weissleder R, Swirski FK, Moskowitz MA, Nahrendorf M. Direct vascular channels connect skull bone marrow and the brain surface enabling myeloid cell migration. Nat Neurosci. 2018;21(9):1209–17. https://doi.org/10.1038/s41593-018-0213-2.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Humphries HE, Triantafilou M, Makepeace BL, Heckels JE, Triantafilou K, Christodoulides M. Activation of human meningeal cells is modulated by lipopolysaccharide (LPS) and non-LPS components of Neisseria meningitidis and is independent of Toll-like receptor (TLR)4 and TLR2 signalling. Cell Microbiol. 2005;7(3):415–30. https://doi.org/10.1111/j.1462-5822.2004.00471.x.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Jacob JT, Coulombe PA, Kwan R, Omary MB. Types I and II Keratin Intermediate Filaments. Cold Spring Harb Perspect Biol. 2018. https://doi.org/10.1101/cshperspect.a018275.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kaldjian EP, Gretz JE, Anderson AO, Shi Y, Shaw S. Spatial and molecular organization of lymph node T cell cortex: a labyrinthine cavity bounded by an epithelium-like monolayer of fibroblastic reticular cells anchored to basement membrane-like extracellular matrix. Int Immunol. 2001;13(10):1243–53. https://doi.org/10.1093/intimm/13.10.1243.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Karantza V. Keratins in health and cancer: more than mere epithelial cell markers. Oncogene. 2011;30(2):127–38. https://doi.org/10.1038/onc.2010.456.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kasper M, Perry G, Stosiek P. Cytokeratin expression in human spinal meninges and ependymal cells. J Hirnforsch. 1991;32(1):19–25.

    CAS 
    PubMed 

    Google Scholar
     

  • Katagata Y, Takeda H, Ishizawa T, Hozumi Y, Kondo S. Occurrence and comparison of the expressed keratins in cultured human fibroblasts, endothelial cells and their sarcomas. J Dermatol Sci. 2002;30(1):1–9. https://doi.org/10.1016/s0923-1811(02)00039-7.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kee R, Naughton M, McDonnell GV, Howell OW, Fitzgerald DC. A review of compartmentalised inflammation and tertiary lymphoid structures in the pathophysiology of multiple sclerosis. Biomedicines. 2022. https://doi.org/10.3390/biomedicines10102604.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kelly KK, MacPherson AM, Grewal H, Strnad F, Jones JW, Yu J, Pierzchalski K, Kane MA, Herson PS, Siegenthaler JA. Col1a1+ perivascular cells in the brain are a source of retinoic acid following stroke. BMC Neurosci. 2016;17(1):49. https://doi.org/10.1186/s12868-016-0284-5.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kendall RT, Feghali-Bostwick CA. Fibroblasts in fibrosis: novel roles and mediators. Front Pharmacol. 2014;5:123. https://doi.org/10.3389/fphar.2014.00123.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Khetarpal U, Robertson NG, Yoo TJ, Morton CC. Expression and localization of COL2A1 mRNA and type II collagen in human fetal cochlea. Hear Res. 1994;79:59–73. https://doi.org/10.1016/0378-5955(94)90127-9.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Killer HE, Laeng HR, Flammer J, Groscurth P. Architecture of arachnoid trabeculae, pillars, and septa in the subarachnoid space of the human optic nerve: anatomy and clinical considerations. Br J Ophthalmol. 2003;87(6):777–81. https://doi.org/10.1136/bjo.87.6.777.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kinaci A, Bergmann W, Bleys RL, van der Zwan A, van Doormaal TP. Histologic comparison of the dura mater among species. Comp Med. 2020;70(2):170–5. https://doi.org/10.30802/AALAS-CM-19-000022.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Knupp C, Squire JM. Molecular packing in network-forming collagens. Adv Protein Chem. 2005;70:375–403. https://doi.org/10.1016/S0065-3233(05)70011-5.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Korin B, Ben-Shaanan TL, Schiller M, Dubovik T, Azulay-Debby H, Boshnak NT, Koren T, Rolls A. High-dimensional, single-cell characterization of the brain’s immune compartment. Nat Neurosci. 2017;20(9):1300–9. https://doi.org/10.1038/nn.4610.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kramer RH, Rosen SD, McDonald KA. Basement-membrane components associated with the extracellular matrix of the lymph node. Cell Tissue Res. 1988;252(2):367–75. https://doi.org/10.1007/BF00214379.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kuznetsova I, Lugmayr A, Siira SJ, Rackham O, Filipovska A. CirGO: an alternative circular way of visualising gene ontology terms. BMC Bioinform. 2019;20(1):84. https://doi.org/10.1186/s12859-019-2671-2.

    Article 

    Google Scholar
     

  • Kypriotou M, Fossard-Demoor M, Chadjichristos C, Ghayor C, de Crombrugghe B, Pujol JP, Galera P. SOX9 exerts a bifunctional effect on type II collagen gene (COL2A1) expression in chondrocytes depending on the differentiation state. DNA Cell Biol. 2003;22(2):119–29. https://doi.org/10.1089/104454903321515922.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Lassmann H. Targets of therapy in progressive MS. Mult Scler. 2017;23(12):1593–9. https://doi.org/10.1177/1352458517729455.

    Article 
    PubMed 

    Google Scholar
     

  • Lavallee-Adam M, Rauniyar N, McClatchy DB, Yates JR 3rd. PSEA-Quant: a protein set enrichment analysis on label-free and label-based protein quantification data. J Proteome Res. 2014;13(12):5496–509. https://doi.org/10.1021/pr500473n.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Liu H, Zhu R, Liu C, Ma R, Wang L, Chen B, Li L, Niu J, Zhao D, Mo F, Fu M, Bromme D, Zhang D, Gao S. Evaluation of decalcification techniques for rat femurs using HE and immunohistochemical staining. Biomed Res Int. 2017;2017:9050754. https://doi.org/10.1155/2017/9050754.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lui VC, Ng LJ, Nicholls J, Tam PP, Cheah KS. Tissue-specific and differential expression of alternatively spliced alpha 1(II) collagen mRNAs in early human embryos. Dev Dyn. 1995;203(2):198–211. https://doi.org/10.1002/aja.1002030208.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Luo Y, Sinkeviciute D, He Y, Karsdal M, Henrotin Y, Mobasheri A, Onnerfjord P, Bay-Jensen A. The minor collagens in articular cartilage. Protein Cell. 2017;8(8):560–72. https://doi.org/10.1007/s13238-017-0377-7.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ma T, Wang F, Xu S, Huang JH. Meningeal immunity: Structure, function and a potential therapeutic target of neurodegenerative diseases. Brain Behav Immun. 2021;93:264–76. https://doi.org/10.1016/j.bbi.2021.01.028.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • MacManus DB, Pierrat B, Murphy JG, Gilchrist MD. Protection of cortex by overlying meninges tissue during dynamic indentation of the adolescent brain. Acta Biomater. 2017;57:384–94. https://doi.org/10.1016/j.actbio.2017.05.022.

    Article 
    PubMed 

    Google Scholar
     

  • Magliozzi R, Columba-Cabezas S, Serafini B, Aloisi F. Intracerebral expression of CXCL13 and BAFF is accompanied by formation of lymphoid follicle-like structures in the meninges of mice with relapsing experimental autoimmune encephalomyelitis. J Neuroimmunol. 2004;148(1–2):11–23. https://doi.org/10.1016/j.jneuroim.2003.10.056.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Miettinen M, Paetau A. Mapping of the keratin polypeptides in meningiomas of different types: an immunohistochemical analysis of 463 cases. Hum Pathol. 2002;33(6):590–8. https://doi.org/10.1053/hupa.2002.124912.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Mitsdoerffer M, Di Liberto G, Dotsch S, Sie C, Wagner I, Pfaller M, Kreutzfeldt M, Frassle S, Aly L, Knier B, Busch DH, Merkler D, Korn T. Formation and immunomodulatory function of meningeal B cell aggregates in progressive CNS autoimmunity. Brain. 2021;144(6):1697–710. https://doi.org/10.1093/brain/awab093.

    Article 
    PubMed 

    Google Scholar
     

  • Mitsdoerffer M, Peters A. Tertiary lymphoid organs in central nervous system autoimmunity. Front Immunol. 2016;7:451. https://doi.org/10.3389/fimmu.2016.00451.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Moll R, Divo M, Langbein L. The human keratins: biology and pathology. Histochem Cell Biol. 2008;129(6):705–33. https://doi.org/10.1007/s00418-008-0435-6.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Monaco S, Nicholas R, Reynolds R, Magliozzi R. Intrathecal inflammation in progressive multiple sclerosis. Int J Mol Sci. 2020. https://doi.org/10.3390/ijms21218217.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Montagnani S, Castaldo C, Di Meglio F, Sciorio S, Giordano-Lanza G. Extra cellular matrix features in human meninges. Ital J Anat Embryol. 2000;105(3):167–77.

    CAS 
    PubMed 

    Google Scholar
     

  • Mortazavi MM, Quadri SA, Khan MA, Gustin A, Suriya SS, Hassanzadeh T, Fahimdanesh KM, Adl FH, Fard SA, Taqi MA, Armstrong I, Martin BA, Tubbs RS. Subarachnoid trabeculae: a comprehensive review of their embryology, histology, morphology, and surgical significance. World Neurosurg. 2018;111:279–90. https://doi.org/10.1016/j.wneu.2017.12.041.

    Article 
    PubMed 

    Google Scholar
     

  • Nauta HJ, Dolan E, Yasargil MG. Microsurgical anatomy of spinal subarachnoid space. Surg Neurol. 1983;19(5):431–7. https://doi.org/10.1016/0090-3019(83)90141-6.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Nicholas DS, Weller RO. The fine anatomy of the human spinal meninges. A light and scanning electron microscopy study. J Neurosurg. 1988;69(2):276–82. https://doi.org/10.3171/jns.1988.69.2.0276.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Oda Y, Nakanishi I. Ultrastructure of the mouse leptomeninx. J Comp Neurol. 1984;225(3):448–57. https://doi.org/10.1002/cne.902250310.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ohnishi Y, Iwatsuki K, Morii E, Kobayashi M, Hori Y, Moriwaki T, Ishihara M, Yoshimura K, Umegaki M, Yoshimine T. Histopathological study of spinal meningioma originating from the arachnoid villi. Brain Tumor Pathol. 2011;28(1):77–81. https://doi.org/10.1007/s10014-010-0003-3.

    Article 
    PubMed 

    Google Scholar
     

  • Ortolani F, Giordano M, Marchini M. A model for type II collagen fibrils: distinctive D-band patterns in native and reconstituted fibrils compared with sequence data for helix and telopeptide domains. Biopolymers. 2000;54(6):448–63.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ortolani F, Marchini M. Cartilage type II collagen fibrils show distinctive negative-staining band patterns differences between type II and type I unfixed or glutaraldehyde-fixed collagen fibrils. J Electron Microsc. 1995;44(5):365–75.

    CAS 

    Google Scholar
     

  • Papaioannou MD, Djuric U, Kao J, Karimi S, Zadeh G, Aldape K, Diamandis P. Proteomic analysis of meningiomas reveals clinically distinct molecular patterns. Neuro Oncol. 2019;21(8):1028–38. https://doi.org/10.1093/neuonc/noz084.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Parkinson D. Human spinal arachnoid septa, trabeculae, and “rogue strands.” Am J Anat. 1991;192(4):498–509. https://doi.org/10.1002/aja.1001920414.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Patel N, Kirmi O. Anatomy and imaging of the normal meninges. Semin Ultrasound CT MR. 2009;30(6):559–64. https://doi.org/10.1053/j.sult.2009.08.006.

    Article 
    PubMed 

    Google Scholar
     

  • Paul D, Cowan AE, Ge S, Pachter JS. Novel 3D analysis of Claudin-5 reveals significant endothelial heterogeneity among CNS microvessels. Microvasc Res. 2013;86:1–10. https://doi.org/10.1016/j.mvr.2012.12.001.PubMedPMID:23261753;PMCID:3570614.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Pease DC, Schultz RL. Electron microscopy of rat cranial meninges. Am J Anat. 1958;102(2):301–21. https://doi.org/10.1002/aja.1001020207.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Pikor NB, Astarita JL, Summers-Deluca L, Galicia G, Qu J, Ward LA, Armstrong S, Dominguez CX, Malhotra D, Heiden B, Kay R, Castanov V, Touil H, Boon L, O’Connor P, Bar-Or A, Prat A, Ramaglia V, Ludwin S, Turley SJ, Gommerman JL. Integration of Th17- and lymphotoxin-derived signals initiates meningeal-resident stromal cell remodeling to propagate neuroinflammation. Immunity. 2015;43(6):1160–73. https://doi.org/10.1016/j.immuni.2015.11.010.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Pikor NB, Cupovic J, Onder L, Gommerman JL, Ludewig B. Stromal cell niches in the inflamed central nervous system. J Immunol. 2017;198(5):1775–81. https://doi.org/10.4049/jimmunol.1601566.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Pikor NB, Prat A, Bar-Or A, Gommerman JL. Meningeal tertiary lymphoid tissues and multiple sclerosis: a gathering place for diverse types of immune cells during CNS autoimmunity. Front Immunol. 2015;6:657. https://doi.org/10.3389/fimmu.2015.00657.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ramaglia V, Florescu A, Zuo M, Sheikh-Mohamed S, Gommerman JL. Stromal cell-mediated coordination of immune cell recruitment, retention, and function in brain-adjacent regions. J Immunol. 2021;206(2):282–91. https://doi.org/10.4049/jimmunol.2000833.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ramo NL, Troyer KL, Puttlitz CM. Viscoelasticity of spinal cord and meningeal tissues. Acta Biomater. 2018;75:253–62. https://doi.org/10.1016/j.actbio.2018.05.045.

    Article 
    PubMed 

    Google Scholar
     

  • Reboldi A, Coisne C, Baumjohann D, Benvenuto F, Bottinelli D, Lira S, Uccelli A, Lanzavecchia A, Engelhardt B, Sallusto F. C-C chemokine receptor 6-regulated entry of TH-17 cells into the CNS through the choroid plexus is required for the initiation of EAE. Nat Immunol. 2009;10(5):514–23. https://doi.org/10.1038/ni.1716.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Rhodes JM, Simons M. The extracellular matrix and blood vessel formation: not just a scaffold. J Cell Mol Med. 2007;11(2):176–205. https://doi.org/10.1111/j.1582-4934.2007.00031.x.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Royer PJ, Rogers AJ, Wooldridge KG, Tighe P, Mahdavi J, Rittig MG, Ala’Aldeen D. Deciphering the contribution of human meningothelial cells to the inflammatory and antimicrobial response at the meninges. Infect Immun. 2013;81(11):4299–310. https://doi.org/10.1128/IAI.00477-13.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Rua R, McGavern DB. Advances in Meningeal Immunity. Trends Mol Med. 2018;24(6):542–59. https://doi.org/10.1016/j.molmed.2018.04.003.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Russi AE, Brown MA. The meninges: new therapeutic targets for multiple sclerosis. Transl Res. 2015;165(2):255–69. https://doi.org/10.1016/j.trsl.2014.08.005.

    Article 
    PubMed 

    Google Scholar
     

  • Rustenhoven J, Drieu A, Mamuladze T, de Lima KA, Dykstra T, Wall M, Papadopoulos Z, Kanamori M, Salvador AF, Baker W, Lemieux M, Da Mesquita S, Cugurra A, Fitzpatrick J, Sviben S, Kossina R, Bayguinov P, Townsend RR, Zhang Q, Erdmann-Gilmore P, Smirnov I, Lopes MB, Herz J, Kipnis J. Functional characterization of the dural sinuses as a neuroimmune interface. Cell. 2021;184(4):1000–16. https://doi.org/10.1016/j.cell.2020.12.040.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Saboori P. Subarachnoid space trabeculae architecture. Clin Anat. 2021;34(1):40–50. https://doi.org/10.1002/ca.23635.

    Article 
    PubMed 

    Google Scholar
     

  • Saboori P, Sadegh A. Histology and morphology of the brain subarachnoid trabeculae. Anat Res Int. 2015;2015:279814. https://doi.org/10.1155/2015/279814.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sandberg MM, Hirvonen HE, Elima KJ, Vuorio EI. Co-expression of collagens II and XI and alternative splicing of exon 2 of collagen II in several developing human tissues. Biochem J. 1993;294(2):595–602. https://doi.org/10.1042/bj2940595.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Schafflick D, Wolbert J, Heming M, Thomas C, Hartlehnert M, Borsch AL, Ricci A, Martin-Salamanca S, Li X, Lu IN, Pawlak M, Minnerup J, Strecker JK, Seidenbecher T, Meuth SG, Hidalgo A, Liesz A, Wiendl H, Zu Horste GM. Single-cell profiling of CNS border compartment leukocytes reveals that B cells and their progenitors reside in non-diseased meninges. Nat Neurosci. 2021;24(9):1225–34. https://doi.org/10.1038/s41593-021-00880-y.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Scheyltjens I, Van Hove H, De Vlaminck K, Kancheva D, Bastos J, Vara-Perez M, Pombo Antunes AR, Martens L, Scott CL, Van Ginderachter JA, Saeys Y, Guilliams M, Vandamme N, Movahedi K. Single-cell RNA and protein profiling of immune cells from the mouse brain and its border tissues. Nat Protoc. 2022;17(10):2354–88. https://doi.org/10.1038/s41596-022-00716-4.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Schulte S, Unger C, Mo JA, Wendler O, Bauer E, Frischholz S, von der Mark K, Kalden JR, Holmdahl R, Burkhardt H. Arthritis-related B cell epitopes in collagen II are conformation-dependent and sterically privileged in accessible sites of cartilage collagen fibrils. J Biol Chem. 1998;273(3):1551–61. https://doi.org/10.1074/jbc.273.3.1551.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Schweizer J, Bowden PE, Coulombe PA, Langbein L, Lane EB, Magin TM, Maltais L, Omary MB, Parry DA, Rogers MA, Wright MW. New consensus nomenclature for mammalian keratins. J Cell Biol. 2006;174(2):169–74. https://doi.org/10.1083/jcb.200603161.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Schmitt C, Strazielle N, Ghersi-Egea JF. Brain leukocyte infiltration initiated by peripheral inflammation or experimental autoimmune encephalomyelitis occurs through pathways connected to the CSF-filled compartments of the forebrain and midbrain. J Neuroinflammation. 2012;9:187. https://doi.org/10.1186/1742-2094-9-187.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Schnell L, Fearn S, Klassen H, Schwab ME, Perry VH. Acute inflammatory responses to mechanical lesions in the CNS: differences between brain and spinal cord. Eur J Neurosci. 1999;11(10):3648–58. https://doi.org/10.1046/j.1460-9568.1999.00792.x.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Serafini B, Rosicarelli B, Magliozzi R, Stigliano E, Aloisi F. Detection of ectopic B-cell follicles with germinal centers in the meninges of patients with secondary progressive multiple sclerosis. Brain Pathol. 2004;14(2):164–74. https://doi.org/10.1111/j.1750-3639.2004.tb00049.x.

    Article 
    PubMed 

    Google Scholar
     

  • Sequeira I, Neves JF, Carrero D, Peng Q, Palasz N, Liakath-Ali K, Lord GM, Morgan PR, Lombardi G, Watt FM. Immunomodulatory role of Keratin 76 in oral and gastric cancer. Nat Commun. 2018;9(1):3437. https://doi.org/10.1038/s41467-018-05872-4.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Shaykhiev R, Bals R. Interactions between epithelial cells and leukocytes in immunity and tissue homeostasis. J Leukoc Biol. 2007;82(1):1–15. https://doi.org/10.1189/jlb.0207096.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Shrestha B, Jiang X, Ge S, Paul D, Chianchiano P, Pachter JS. Spatiotemporal resolution of spinal meningeal and parenchymal inflammation during experimental autoimmune encephalomyelitis. Neurobiol Dis. 2017;108:159–72. https://doi.org/10.1016/j.nbd.2017.08.010.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Shrestha B, Paul D, Pachter JS. Alterations in tight jiunction and IgG permeability accompany leukocyte extravasation across the choroid plexus during neuroinflammation. J Neuropathol Exp Neurol. 2014;73(11):1047–61. https://doi.org/10.1097/NEN.0000000000000127.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Silva JM, Wippel HH, Santos MDM, Verissimo DCA, Santos RM, Nogueira FCS, Passos GAR, Sprengel SL, Borba LAB, Carvalho PC, Fischer J. Proteomics pinpoints alterations in grade I meningiomas of male versus female patients. Sci Rep. 2020;10(1):10335. https://doi.org/10.1038/s41598-020-67113-3.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Stadnyk AW. Cytokine production by epithelial cells. FASEB J. 1994;8(13):1041–7. https://doi.org/10.1096/fasebj.8.13.7926369.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Sudres P, Evin M, Wagnac E, Bailly N, Diotalevi L, Melot A, Arnoux PJ, Petit Y. Tensile mechanical properties of the cervical, thoracic and lumbar porcine spinal meninges. J Mech Behav Biomed Mater. 2021;115:104280. https://doi.org/10.1016/j.jmbbm.2020.104280.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Supek F, Bosnjak M, Skunca N, Smuc T. REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS ONE. 2011;6(7):e21800. https://doi.org/10.1371/journal.pone.0021800.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Traweek ST, Liu J, Battifora H. Keratin gene expression in non-epithelial tissues. Detection with polymerase chain reaction. Am J Pathol. 1993;142(4):1111–8.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Vandenabeele F, Creemers J, Lambrichts I. Ultrastructure of the human spinal arachnoid mater and dura mater. J Anat. 1996;189(2):417–30.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Van Hove H, Martens L, Scheyltjens I, De Vlaminck K, Pombo Antunes AR, De Prijck S, Vandamme N, De Schepper S, Van Isterdael G, Scott CL, Aerts J, Berx G, Boeckxstaens GE, Vandenbroucke RE, Vereecke L, Moechars D, Guilliams M, Van Ginderachter JA, Saeys Y, Movahedi K. A single-cell atlas of mouse brain macrophages reveals unique transcriptional identities shaped by ontogeny and tissue environment. Nat Neurosci. 2019;22(6):1021–35. https://doi.org/10.1038/s41593-019-0393-4.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Van Linthout S, Miteva K, Tschope C. Crosstalk between fibroblasts and inflammatory cells. Cardiovasc Res. 2014;102(2):258–69. https://doi.org/10.1093/cvr/cvu062.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Walsh DR, Ross AM, Malijauskaite S, Flanagan BD, Newport DT, McGourty KD, Mulvihill JJE. Regional mechanical and biochemical properties of the porcine cortical meninges. Acta Biomater. 2018;80:237–46. https://doi.org/10.1016/j.actbio.2018.09.004.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Weis MA, Hudson DM, Kim L, Scott M, Wu JJ, Eyre DR. Location of 3-hydroxyproline residues in collagen types I, II, III, and V/XI implies a role in fibril supramolecular assembly. J Biol Chem. 2010;285(4):2580–90. https://doi.org/10.1074/jbc.M109.068726.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Werner S, Keller L, Pantel K. Epithelial keratins: biology and implications as diagnostic markers for liquid biopsies. Mol Aspects Med. 2020;72:100817. https://doi.org/10.1016/j.mam.2019.09.001.

    Article 
    PubMed 

    Google Scholar
     

  • Wieseler-Frank J, Jekich BM, Mahoney JH, Bland ST, Maier SF, Watkins LR. A novel immune-to-CNS communication pathway: cells of the meninges surrounding the spinal cord CSF space produce proinflammatory cytokines in response to an inflammatory stimulus. Brain Behav Immun. 2007;21(5):711–8. https://doi.org/10.1016/j.bbi.2006.07.004.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wisniewski JR, Zougman A, Nagaraj N, Mann M. Universal sample preparation method for proteome analysis. Nat Methods. 2009;6(5):359–62. https://doi.org/10.1038/nmeth.1322.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wu JJ, Weis MA, Kim LS, Eyre DR. Type III collagen, a fibril network modifier in articular cartilage. J Biol Chem. 2010;285(24):18537–44. https://doi.org/10.1074/jbc.M110.112904.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Xin X, Fan B, Flammer J, Miller NR, Jaggi GP, Killer HE, Meyer P, Neutzner A. Meningothelial cells react to elevated pressure and oxidative stress. PLoS ONE. 2011;6(5):e20142. https://doi.org/10.1371/journal.pone.0020142.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Xu J, Shi GP. Vascular wall extracellular matrix proteins and vascular diseases. Biochim Biophys Acta. 2014;1842(11):2106–19. https://doi.org/10.1016/j.bbadis.2014.07.008.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Xu L, Yao Y. Central nervous system fibroblast-like cells in stroke and other neurological disorders. Stroke. 2021;52(7):2456–64. https://doi.org/10.1161/STROKEAHA.120.033431.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhan J, Kipp M, Han W, Kaddatz H. Ectopic lymphoid follicles in progressive multiple sclerosis: from patients to animal models. Immunology. 2021;164(3):450–66. https://doi.org/10.1111/imm.13395.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhang B, Gensel JC. Is neuroinflammation in the injured spinal cord different than in the brain? Examining intrinsic differences between the brain and spinal cord. Exp Neurol. 2014;258:112–20. https://doi.org/10.1016/j.expneurol.2014.04.007.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Zhu Y, Oganesian A, Keene DR, Sandell LJ. Type IIA procollagen containing the cysteine-rich amino propeptide is deposited in the extracellular matrix of prechondrogenic tissue and binds to TGF-beta1 and BMP-2. J Cell Biol. 1999;144(5):1069–80. https://doi.org/10.1083/jcb.144.5.1069.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     



  • Source link