Complex Non-sinus-associated Pachymeningeal Lymphatic Structures: Interrelationship With Blood Microvasculature

Overview

Journal Front Physiol

Date 2019 Nov 19

PMID 31736785

Citations 6

Authors

Olga V Glinskii

Virginia H Huxley

Leike Xie

Filiz Bunyak

Kannappan Palaniappan

Vladislav V Glinsky

Affiliations

Soon will be listed here.

Abstract

The contribution of cranial dura mater vascular networks, as means for maintaining brain fluid movement and balance, and as the source of significant initiators and/or contributors to neurological disorders, has been overlooked. These networks consist of both blood and lymphatic vessels. The latter were discovered recently and described as sinus-associated structures thus changing the old paradigm that central nervous system lacks lymphatics. In this study, using markers specific to blood and lymphatic endothelia, we demonstrate the existence of the complex non-sinus-associated pachymeningeal lymphatic vasculature. We further show the interrelationship and possible connections between lymphatic vessels and the dural blood circulatory system. Our novel findings reveal the presence of lymphatic-like structures that exist on their own and/or in close proximity to microvessels. Of particular interest are sub-sets of vascular complexes with dual (lymphatic and blood) vessel identity representing a unique microenvironment within the cranial dura. The close association of the systemic blood circulation and meningeal lymphatics achieved in these complexes could facilitate fluid exchange between the two compartments and constitute an alternative route for CSF drainage.

Citing Articles

Dynamics of Endothelial Cell Diversity and Plasticity in Health and Disease.

Larionov A, Hammer C, Fiedler K, Filgueira L Cells. 2024; 13(15.

PMID: 39120307 PMC: 11312403. DOI: 10.3390/cells13151276.

Postnatal meningeal CSF transport is primarily mediated by the arachnoid and pia maters and is not altered after intraventricular hemorrhage-posthemorrhagic hydrocephalus.

Pan S, Koleske J, Koller G, Halupnik G, Alli A, Koneru S Fluids Barriers CNS. 2024; 21(1):4.

PMID: 38191402 PMC: 10773070. DOI: 10.1186/s12987-023-00503-7.

Corneal injury is associated with stromal and vascular alterations within cranial dura mater.

Glinskii O, Glinsky V, Xie L, Bunyak F, Glinskii V, Sinha S PLoS One. 2023; 18(4):e0284082.

PMID: 37079653 PMC: 10118146. DOI: 10.1371/journal.pone.0284082.

Ensemble of Deep Learning Cascades for Segmentation of Blood Vessels in Confocal Microscopy Images.

Wang Y, Glinskii O, Bunyak F, Palaniappan K IEEE Appl Imag Pattern Recognit Workshop. 2022; 2021.

PMID: 35506042 PMC: 9060211. DOI: 10.1109/aipr52630.2021.9762193.

Multi-focus Image Fusion for Confocal Microscopy Using U-Net Regression Map.

Shuvo M, Kassim Y, Bunyak F, Glinskii O, Xie L, Glinsky V Proc IAPR Int Conf Pattern Recogn. 2021; 2020:4317-4323.

PMID: 34651146 PMC: 8513773. DOI: 10.1109/icpr48806.2021.9412122.

References

Lim H, Lim S, Tan C, Thiam C, Goh C, Carbajo D . Hyaluronan Receptor LYVE-1-Expressing Macrophages Maintain Arterial Tone through Hyaluronan-Mediated Regulation of Smooth Muscle Cell Collagen. Immunity. 2018; 49(2):326-341.e7. DOI: 10.1016/j.immuni.2018.06.008. View

Baltsavias G, Parthasarathi V, Aydin E, Al Schameri R, Roth P, Valavanis A . Cranial dural arteriovenous shunts. Part 1. Anatomy and embryology of the bridging and emissary veins. Neurosurg Rev. 2014; 38(2):253-63. DOI: 10.1007/s10143-014-0590-2. View

Coles J, Myburgh E, Brewer J, McMenamin P . 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; 156:107-148. DOI: 10.1016/j.pneurobio.2017.05.002. View

Osaka K, Handa H, Matsumoto S, Yasuda M . Development of the cerebrospinal fluid pathway in the normal and abnormal human embryos. Childs Brain. 1980; 6(1):26-38. DOI: 10.1159/000119881. View

Roland J, Bernard C, Bracard S, Czorny A, Floquet J, Race J . Microvascularization of the intracranial dura mater. Surg Radiol Anat. 1987; 9(1):43-9. DOI: 10.1007/BF02116853. View

Schledzewski K, Falkowski M, Moldenhauer G, Metharom P, Kzhyshkowska J, Ganss R . Lymphatic endothelium-specific hyaluronan receptor LYVE-1 is expressed by stabilin-1+, F4/80+, CD11b+ macrophages in malignant tumours and wound healing tissue in vivo and in bone marrow cultures in vitro: implications for the assessment of.... J Pathol. 2006; 209(1):67-77. DOI: 10.1002/path.1942. View

Coles J, Stewart-Hutchinson P, Myburgh E, Brewer J . 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. PMC: 5595162. DOI: 10.1016/j.ymeth.2017.03.020. View

Maruyama K, Ii M, Cursiefen C, Jackson D, Keino H, Tomita M . Inflammation-induced lymphangiogenesis in the cornea arises from CD11b-positive macrophages. J Clin Invest. 2005; 115(9):2363-72. PMC: 1193872. DOI: 10.1172/JCI23874. View

Protasoni M, Sangiorgi S, Cividini A, Culuvaris G, Tomei G, Dellorbo C . The collagenic architecture of human dura mater. J Neurosurg. 2011; 114(6):1723-30. DOI: 10.3171/2010.12.JNS101732. View

10.

Iliff J, Wang M, Liao Y, Plogg B, Peng W, Gundersen G . A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid β. Sci Transl Med. 2012; 4(147):147ra111. PMC: 3551275. DOI: 10.1126/scitranslmed.3003748. View

11.

Bower N, Koltowska K, Pichol-Thievend C, Virshup I, Paterson S, Lagendijk A . Mural lymphatic endothelial cells regulate meningeal angiogenesis in the zebrafish. Nat Neurosci. 2017; 20(6):774-783. DOI: 10.1038/nn.4558. View

12.

Glinskii O, Huxley V, Glinskii V, Rubin L, Glinsky V . Pulsed estrogen therapy prevents post-OVX porcine dura mater microvascular network weakening via a PDGF-BB-dependent mechanism. PLoS One. 2013; 8(12):e82900. PMC: 3857298. DOI: 10.1371/journal.pone.0082900. View

13.

Baltsavias G, Kumar R, Avinash K, Valavanis A . Cranial dural arteriovenous shunts. Part 2. The shunts of the bridging veins and leptomeningeal venous drainage. Neurosurg Rev. 2014; 38(2):265-71. DOI: 10.1007/s10143-014-0594-y. View

14.

Bunyak F, Palaniappan K, Glinskii O, Glinskii V, Glinsky V, Huxley V . Epifluorescence-based quantitative microvasculature remodeling using geodesic level-sets and shape-based evolution. Annu Int Conf IEEE Eng Med Biol Soc. 2009; 2008:3134-7. PMC: 2630480. DOI: 10.1109/IEMBS.2008.4649868. View

15.

Glinskii O, Abraha T, Turk J, Rubin L, Huxley V, Glinsky V . Microvascular network remodeling in dura mater of ovariectomized pigs: role for angiopoietin-1 in estrogen-dependent control of vascular stability. Am J Physiol Heart Circ Physiol. 2007; 293(2):H1131-7. PMC: 3332330. DOI: 10.1152/ajpheart.01156.2006. View

16.

Kassim Y, Surya Prasath V, Glinskii O, Glinsky V, Huxley V, Palaniappan K . Confocal Vessel Structure Segmentation with Optimized Feature Bank and Random Forests. IEEE Appl Imag Pattern Recognit Workshop. 2017; 2016. PMC: 5690568. DOI: 10.1109/AIPR.2016.8010580. View

17.

Sandrone S, Moreno-Zambrano D, Kipnis J, van Gijn J . A (delayed) history of the brain lymphatic system. Nat Med. 2019; 25(4):538-540. DOI: 10.1038/s41591-019-0417-3. View

18.

Kipnis J, Gadani S, Derecki N . Pro-cognitive properties of T cells. Nat Rev Immunol. 2012; 12(9):663-9. PMC: 4032225. DOI: 10.1038/nri3280. View

19.

Kang J, Yoo J, Lee S, Tang W, Aguilar B, Ramu S . An exquisite cross-control mechanism among endothelial cell fate regulators directs the plasticity and heterogeneity of lymphatic endothelial cells. Blood. 2010; 116(1):140-50. PMC: 2904577. DOI: 10.1182/blood-2009-11-252270. View

20.

Kassim Y, Surya Prasath V, Pelapur R, Glinskii O, Maude R, Glinsky V . Random Forests for Dura Mater Microvasculature Segmentation Using Epifluorescence Images. Annu Int Conf IEEE Eng Med Biol Soc. 2017; 2016:2901-2904. PMC: 5324830. DOI: 10.1109/EMBC.2016.7591336. View