Astrocytic Endfeet Re-cover Blood Vessels After Removal by Laser Ablation

Overview

Journal Sci Rep

Specialty Science

Date 2019 Feb 6

PMID 30718555

Citations 57

Authors

Hideaki Kubotera

Hiroko Ikeshima-Kataoka

Yoshiki Hatashita

Anna Letizia Allegra Mascaro

Francesco Saverio Pavone

Takafumi Inoue

Affiliations

Soon will be listed here.

Abstract

The astrocyte, one of the glial cells, plays many functional roles. These include provision of nutrients from blood vessels to neurons, supply of neurotransmitters and support of blood-brain barrier (BBB) integrity. Astrocytes are known to support the integrity of BBB through maintenance of the tight junction between endothelial cells of blood vessels. However, evidence of its direct contribution to BBB is lacking owing to technical limitations. In this study, astrocytic endfeet covering blood vessels were removed by the laser ablation method with two photon laser scanning microscopy in in vivo mouse brain, and the re-covering of blood vessels with the astrocytic endfeet was observed in about half of the cases. Blood vessels kept their integrity without astrocytic endfoot covers: leakage of plasma marker dyes, Evans Blue or dextran-conjugated fluorescein, was not observed from stripped blood vessels, while ablation of vascular walls induced extravasation of Evans Blue. These results suggest that the astrocytic endfeet covering blood vessels do not contribute to the immediate BBB barrier.

Citing Articles

Immune cell infiltration and modulation of the blood-brain barrier in a guinea pig model of tuberculosis: Observations without evidence of bacterial dissemination to the brain.

Latham A, Geer C, Ackart D, Weninger K, Gross C, Podell B PLoS One. 2024; 19(12):e0307577.

PMID: 39739680 PMC: 11687776. DOI: 10.1371/journal.pone.0307577.

The Involvement of Glial Cells in Blood-Brain Barrier Damage in Neuroimmune Diseases.

Nagata S, Yamasaki R Int J Mol Sci. 2024; 25(22).

PMID: 39596390 PMC: 11594741. DOI: 10.3390/ijms252212323.

Inflammaging and Brain Aging.

Jurcau M, Jurcau A, Cristian A, Hogea V, Diaconu R, Nunkoo V Int J Mol Sci. 2024; 25(19).

PMID: 39408862 PMC: 11476611. DOI: 10.3390/ijms251910535.

Astrocyte-Neuron Interactions in Substance Use Disorders.

Harder E, Franklin J, VanRyzin J, Reissner K Adv Neurobiol. 2024; 39():165-191.

PMID: 39190075 DOI: 10.1007/978-3-031-64839-7_7.

Satellite glial cell manipulation prior to axotomy enhances developing dorsal root ganglion central branch regrowth into the spinal cord.

Brown R, Barber H, Kucenas S Glia. 2024; 72(10):1766-1784.

PMID: 39141572 PMC: 11325082. DOI: 10.1002/glia.24581.

References

Manley G, Fujimura M, Ma T, Noshita N, Filiz F, Bollen A . Aquaporin-4 deletion in mice reduces brain edema after acute water intoxication and ischemic stroke. Nat Med. 2000; 6(2):159-63. DOI: 10.1038/72256. View

Voutsinos-Porche B, Bonvento G, Tanaka K, Steiner P, Welker E, Chatton J . Glial glutamate transporters mediate a functional metabolic crosstalk between neurons and astrocytes in the mouse developing cortex. Neuron. 2003; 37(2):275-86. DOI: 10.1016/s0896-6273(02)01170-4. View

Nitta T, Hata M, Gotoh S, Seo Y, Sasaki H, Hashimoto N . Size-selective loosening of the blood-brain barrier in claudin-5-deficient mice. J Cell Biol. 2003; 161(3):653-60. PMC: 2172943. DOI: 10.1083/jcb.200302070. View

Lee S, Kim W, Choi Y, Song H, Son M, Gelman I . SSeCKS regulates angiogenesis and tight junction formation in blood-brain barrier. Nat Med. 2003; 9(7):900-6. DOI: 10.1038/nm889. View

Kuzmanovic M, Dudley V, Sarthy V . GFAP promoter drives Müller cell-specific expression in transgenic mice. Invest Ophthalmol Vis Sci. 2003; 44(8):3606-13. DOI: 10.1167/iovs.02-1265. View

Davalos D, Grutzendler J, Yang G, Kim J, Zuo Y, Jung S . ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci. 2005; 8(6):752-8. DOI: 10.1038/nn1472. View

Takano T, Tian G, Peng W, Lou N, Libionka W, Han X . Astrocyte-mediated control of cerebral blood flow. Nat Neurosci. 2006; 9(2):260-7. DOI: 10.1038/nn1623. View

Nishimura N, Schaffer C, Friedman B, Tsai P, Lyden P, Kleinfeld D . Targeted insult to subsurface cortical blood vessels using ultrashort laser pulses: three models of stroke. Nat Methods. 2006; 3(2):99-108. DOI: 10.1038/nmeth844. View

Myer D, Gurkoff G, Lee S, Hovda D, Sofroniew M . Essential protective roles of reactive astrocytes in traumatic brain injury. Brain. 2006; 129(Pt 10):2761-72. DOI: 10.1093/brain/awl165. View

10.

Iadecola C, Nedergaard M . Glial regulation of the cerebral microvasculature. Nat Neurosci. 2007; 10(11):1369-76. DOI: 10.1038/nn2003. View

11.

Sacconi L, OConnor R, Jasaitis A, Masi A, Buffelli M, Pavone F . In vivo multiphoton nanosurgery on cortical neurons. J Biomed Opt. 2007; 12(5):050502. DOI: 10.1117/1.2798723. View

12.

Cahoy J, Emery B, Kaushal A, Foo L, Zamanian J, Christopherson K . A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J Neurosci. 2008; 28(1):264-78. PMC: 6671143. DOI: 10.1523/JNEUROSCI.4178-07.2008. View

13.

Ikeshima-Kataoka H, Shen J, Eto Y, Saito S, Yuasa S . Alteration of inflammatory cytokine production in the injured central nervous system of tenascin-deficient mice. In Vivo. 2008; 22(4):409-13. View

14.

Koehler R, Roman R, Harder D . Astrocytes and the regulation of cerebral blood flow. Trends Neurosci. 2009; 32(3):160-9. DOI: 10.1016/j.tins.2008.11.005. View

15.

Holtmaat A, Bonhoeffer T, Chow D, Chuckowree J, de Paola V, Hofer S . Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window. Nat Protoc. 2009; 4(8):1128-44. PMC: 3072839. DOI: 10.1038/nprot.2009.89. View

16.

Mathiisen T, Lehre K, Danbolt N, Ottersen O . The perivascular astroglial sheath provides a complete covering of the brain microvessels: an electron microscopic 3D reconstruction. Glia. 2010; 58(9):1094-103. DOI: 10.1002/glia.20990. View

17.

Allegra Mascaro A, Sacconi L, Pavone F . Multi-photon nanosurgery in live brain. Front Neuroenergetics. 2010; 2. PMC: 2922942. DOI: 10.3389/fnene.2010.00021. View

18.

Kimelberg H, Nedergaard M . Functions of astrocytes and their potential as therapeutic targets. Neurotherapeutics. 2010; 7(4):338-53. PMC: 2982258. DOI: 10.1016/j.nurt.2010.07.006. View

19.

Armulik A, Genove G, Mae M, Nisancioglu M, Wallgard E, Niaudet C . Pericytes regulate the blood-brain barrier. Nature. 2010; 468(7323):557-61. DOI: 10.1038/nature09522. View

20.

Kuga N, Sasaki T, Takahara Y, Matsuki N, Ikegaya Y . Large-scale calcium waves traveling through astrocytic networks in vivo. J Neurosci. 2011; 31(7):2607-14. PMC: 6623677. DOI: 10.1523/JNEUROSCI.5319-10.2011. View