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Development of the Blood–Brain Barrier in Ducks

Published online by Cambridge University Press:  02 March 2022

Sheng Yang ,
Jingxian Wu ,
Yonghong Shi ,
Yufei Huang Open the ORCID record for Yufei Huang [Opens in a new window] ,
Yafei Zhang  and
Qiusheng Chen Open the ORCID record for Qiusheng Chen [Opens in a new window]
Sheng Yang
Affiliation:
MOE Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, Jiangsu Province 210095, China
Jingxian Wu
Affiliation:
MOE Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, Jiangsu Province 210095, China
Yonghong Shi
Affiliation:
MOE Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, Jiangsu Province 210095, China Chinese Academy of Agricultural Sciences, Shanghai Veterinary Research Institute, Shanghai 200241, China
Yufei Huang
Affiliation:
MOE Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, Jiangsu Province 210095, China
Yafei Zhang
Affiliation:
MOE Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, Jiangsu Province 210095, China
Qiusheng Chen*
Affiliation:
MOE Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, Jiangsu Province 210095, China
*
*Corresponding author: Qiusheng Chen, E-mail: [email protected]
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Abstract

The blood-brain barrier (BBB) is an important internal barrier. Herein, the electron microscope examination of duck BBB was performed during the brain development. Meanwhile, the genes/proteins of tight junctions (TJs) including zonula occludens-1, occludin, and claudin-5 in the duck brain were detected by Q-PCR and immunohistochemistry. The results showed the density of capillaries in the brain gradually increased during the embryonic period. The generation of the BBB and the specialization of its components occurred mainly in the embryonic stage. During this period, the endothelial cells (ECs) became thinner and pinocytic vesicles decreased; the TJs between EC membranes became longer and more electron-dense; the basement membrane surrounding ECs and pericytes gradually thickened; and the astrocyte foot processes appeared to wrap around the vessels. By the day of hatching (P1), the whole set of duck BBB structures was completely assembled and gradually improved in the subsequent growth process. Interestingly, compared with the cerebrum and cerebellum, the maturity level of the midbrain BBB was earlier seen during the embryonic stage. The expression of TJs increased during the embryonic period and remained stable by post-hatching. The study systematically investigated the histochemical and ultrastructural features of duck BBB during development and explored the corresponding relationship between structure and function.

Keywords

basement membraneblood–brain barrierclaudin-5duckendothelial cellsoccludinzonula occludens-1
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 28 , Issue 2 , April 2022 , pp. 504 - 514
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Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press on behalf of the Microscopy Society of America

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References

Abbott, NJ, Patabendige, AAK, Dolman, DEM, Yusof, SR & Begley, DJ (2010). Structure and function of the blood-brain barrier. Neurobiol Dis 37(1), 13–25.CrossRefGoogle ScholarPubMed
Alvarez, JI, Dodelet-Devillers, A, Kebir, H, Ifergan, I, Fabre, PJ, Terouz, S, Sabbagh, M, Wosik, K, Bourbonnière, L, Bernard, M, van Horssen, J, de Vries, HE, Charron, F & Prat, A (2011). The hedgehog pathway promotes blood-brain barrier integrity and CNS immune quiescence. Science 334(6063), 1727–1731.CrossRefGoogle ScholarPubMed
Amtorp, O & Sørensen, SC (1974). The ontogenetic development of concentration differences for protein and ions between plasma and cerebrospinal fluid in rabbits and rats. J Physiol 243(2), 387–400.CrossRefGoogle ScholarPubMed
Ballabh, P, Braun, A & Nedergaard, M (2004). The blood-brain barrier: An overview: Structure, regulation, and clinical implications. Neurobiol Dis 16(1), 1–13.CrossRefGoogle ScholarPubMed
Begley, DJ & Brightman, MW (2003). Structural and functional aspects of the blood-brain barrier. Prog Drug Res 61, 39–78.Google ScholarPubMed
Bell, RD, Winkler, EA, Sagare, AP, Singh, I, LaRue, B, Deane, R & Zlokovic, BV (2010). Pericytes control key neurovascular functions and neuronal phenotype in the adult brain and during brain aging. Neuron 68(3), 409–427.CrossRefGoogle ScholarPubMed
Birge, WJ, Rose, AD, Haywood, JR & Doolin, PF (1974). Development of the blood-cerebrospinal fluid barrier to proteins and differentiation of cerebrospinal fluid in the chick embryo. Dev Biol 41(2), 245–254.CrossRefGoogle ScholarPubMed
Butt, AM (1995). Effect of inflammatory agents on electrical resistance across the blood-brain barrier in pial microvessels of anaesthetized rats. Brain Res 696(1), 145–150.CrossRefGoogle ScholarPubMed
Butt, AM, Jones, HC & Abbott, NJ (1990). Electrical resistance across the blood-brain barrier in anaesthetized rats: A developmental study. J Physiol 429(1), 47–62.CrossRefGoogle ScholarPubMed
Caroline, B, Erik, OÅ, Henrik, U, Karin, B, Désirée, SJ & Dolores, G-W (2012). Characterization of encephalitis in wild birds naturally infected by highly pathogenic avian influenza H5N1. Avian Dis 56, 144–152.Google Scholar
Chaudhuri, JD (2000). Blood brain barrier and infection. Med Sci Monitor 6(6), 1213–1222.Google ScholarPubMed
Chaves, AJ, Vergara-Alert, J, Busquets, N, Valle, R, Rivas, R, Ramis, A, Darji, A & Majó, N (2014). Neuroinvasion of the highly pathogenic influenza virus H7N1 is caused by disruption of the blood brain barrier in an avian model. PLoS ONE 9(12), e115138.CrossRefGoogle Scholar
Chow, BW & Gu, C (2017). Gradual suppression of transcytosis governs functional blood-retinal barrier formation. Neuron 93(6), 1325–1333.CrossRefGoogle ScholarPubMed
Coomber, BL & Stewart, PA (1985). Morphometric analysis of CNS microvascular endothelium. Microvasc Res 30(1), 99–115.CrossRefGoogle ScholarPubMed
Daneman, R, Zhou, L, Kebede, AA & Barres, BA (2010). Pericytes are required for blood–brain barrier integrity during embryogenesis. Nature 468(7323), 562–566.CrossRefGoogle ScholarPubMed
Delaney, C & Campbell, M (2017). The blood brain barrier: Insights from development and ageing. Tissue Barriers 5(4), e1373897.CrossRefGoogle ScholarPubMed
Ehrlich, P & Frerichs, T (1885). Das sauerstoff-Bedürfnis des organismus: eine farbanalytische studie. Berlin: Hirschwald.Google Scholar
Engelhardt, B (2003). Development of the blood-brain barrier. Cell Tissue Res 314(1), 119–129.CrossRefGoogle ScholarPubMed
Hellström, M, Kalén, M, Lindahl, P, Abramsson, A & Betsholtz, C (1999). Role of PDGF-B and PDGFR-beta in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development 126(14), 3047–3055.CrossRefGoogle ScholarPubMed
Hunt, SP & Brecha, N (1984). Avian Optic tectum: A Synthesis of Morphology and Biochemistry. New York: Pleum Press.Google Scholar
Iadecola, C (2017). The neurovascular unit coming of age: A journey through neurovascular coupling in health and disease. Neuron 96(1), 17–42.CrossRefGoogle ScholarPubMed
Karten, HJ, Cox, K & Mpodozis, J (1997). Two distinct populations of tectal neurons have unique connections within the retinotectorotundal pathway of the pigeon (Columba livia). J Comp Neurol 387(3), 449–465.3.0.CO;2-G>CrossRefGoogle Scholar
Koyuncu, OO, Hogue, IB & Enquist, LW (2013). Virus infections in the nervous system. Cell Host Microbe 13(4), 379–393.CrossRefGoogle ScholarPubMed
Langen, UH, Ayloo, S & Gu, C (2019). Development and cell biology of the blood-brain barrier. Annu Rev Cell Dev Bio 35(1), 591–613.CrossRefGoogle ScholarPubMed
Li, S, Gong, X, Chen, Q, Zheng, F, Ji, G & Liu, Y (2018). Threshold level of Riemerella anatipestifer crossing blood-brain barrier and expression profiles of immune-related proteins in blood and brain tissue from infected ducks. Vet Immunol Immunop 200, 26–31.CrossRefGoogle ScholarPubMed
Liu, T, Yang, P, Chen, H, Huang, Y, Liu, Y, Waqas, Y, Ahmed, N, Chu, X & Chen, Q (2016). Global analysis of differential gene expression related to long-term sperm storage in oviduct of Chinese Soft-Shelled Turtle Pelodiscus sinensis. Sci Rep 6(1), 33296.CrossRefGoogle ScholarPubMed
Møllgård, K & Saunders, NR (1986). The development of the human blood-brain and blood-CSF barriers. Neuropathol Appl Neurobiol 12(4), 337–358.CrossRefGoogle ScholarPubMed
Morita, K, Sasaki, H, Furuse, M & Tsukita, S (1999). Endothelial claudin: Claudin-5/TMVCF constitutes tight junction strands in endothelial cells. J Cell Biol 147(1), 185–194.CrossRefGoogle ScholarPubMed
Niu, Y, Ma, H, Ding, Y, Li, Z, Sun, Y, Li, M & Shi, Y (2019). The pathogenicity of duck hepatitis A virus types 1 and 3 on ducklings. Poult Sci 98(12), 6333–6339.CrossRefGoogle ScholarPubMed
Oldendorf, WH, Cornford, ME & Brown, WJ (1977). The large apparent work capability of the blood-brain barrier: A study of the mitochondrial content of capillary endothelial cells in brain and other tissues of the rat. Ann Neurol 1(5), 409–417.CrossRefGoogle ScholarPubMed
Paolinelli, R, Corada, M, Orsenigo, F & Dejana, E (2011). The molecular basis of the blood brain barrier differentiation and maintenance. Is it still a mystery? Pharmacol Res 63(3), 165–171.CrossRefGoogle Scholar
Pettmann, B, Louis, JC & Sensenbrenner, M (1979). Morphological and biochemical maturation of neurones cultured in the absence of glial cells. Nature 281(5730), 378–380.CrossRefGoogle ScholarPubMed
Ribatti, D, Nico, B & Bertossi, M (1993). The development of the blood-brain barrier in the chick. Studies with Evans blue and horseradish peroxidase. Ann Anat 175(1), 85–88.CrossRefGoogle ScholarPubMed
Risau, W (1991). Induction of blood-brain barrier endothelial cell differentiation. Ann N Y Acad Sci 633(1), 405–419.CrossRefGoogle ScholarPubMed
Saunders, NR, Knott, GW & Dziegielewska, KM (2000). Barriers in the immature brain. Cell Mol Neurobiol 20(1), 29–40.CrossRefGoogle ScholarPubMed
Sauvageot, CM & Stiles, CD (2002). Molecular mechanisms controlling cortical gliogenesis. Curr Opin Neurobiol 12(3), 244–249.CrossRefGoogle ScholarPubMed
Schmidley, JW & Wissig, SL (1986). Basement membrane of central nervous system capillaries lacks ruthenium red-staining sites. Microvasc Res 32(3), 300–314.CrossRefGoogle ScholarPubMed
Sorokin, L (2010). The impact of the extracellular matrix on inflammation. Nat Rev Immunol 10(10), 712–723.CrossRefGoogle ScholarPubMed
Stewart, PA, Magliocco, M, Hayakawa, K, Farrell, CL, Del Maestro, RF, Girvin, J, Kaufmann, JCE, Vinters, HV & Gilbert, J (1987). A quantitative analysis of blood-brain barrier ultrastructure in the aging human. Microvas Res 33(2), 270–282.CrossRefGoogle ScholarPubMed
Stewart, PA & Wiley, MJ (1981). Structural and histochemical features of the avian blood-brain barrier. J Comp Neurol 202(2), 157–167.CrossRefGoogle ScholarPubMed
Sun, XY, Diao, YX, Wang, J, Liu, X, Lu, AL, Zhang, L, Ge, PP & Hao, DM (2014). Tembusu virus infection in Cherry Valley ducks: The effect of age at infection. Vet Microbiol 168(1), 16–24.CrossRefGoogle ScholarPubMed
Swayne, DE, Fletcher, OJ & Schierman, LW (1988). Marek's disease virus-induced transient paralysis in chickens: Alterations in brain density. Acta Neuropathol 76(3), 287–291.CrossRefGoogle ScholarPubMed
Tannock, GA & Shafren, DR (1994). Avian encephalomyelitis: A review. Avian Pathol 23(4), 603–620.CrossRefGoogle ScholarPubMed
Tien, AC, Tsai, HH, Molofsky, AV, McMahon, M, Foo, LC, Kaul, A, Dougherty, JD, Heintz, N, Gutmann, DH, Barres, BA & Rowitch, DH (2012). Regulated temporal-spatial astrocyte precursor cell proliferation involves BRAF signalling in mammalian spinal cord. Development 139(14), 2477–2487.CrossRefGoogle ScholarPubMed
Wakai, S & Hirokawa, N (1978). Development of the blood-brain barrier to horseradish peroxidase in the chick embryo. Cell Tissue Res 28(2), 195–203.Google Scholar
Wolburg, H, Noell, S, Mack, A, Wolburg-Buchholz, K & Fallier-Becker, P (2009). Brain endothelial cells and the glio-vascular complex. Cell Tissue Res 335(1), 75–96.CrossRefGoogle ScholarPubMed
Yang, S, Huang, Y, Shi, Y, Bai, X, Yang, P & Chen, Q (2021). Tembusu virus entering the central nervous system caused nonsuppurative encephalitis without disrupting the blood-brain barrier. J Virol 95(7), e02191-20.CrossRefGoogle Scholar
Yang, Y, Higashimori, H & Morel, L (2013). Developmental maturation of astrocytes and pathogenesis of neurodevelopmental disorders. J Neurodeve Disord 5(1), 22.CrossRefGoogle ScholarPubMed
Yao, Y, Chen, ZL, Norris, EH & Strickland, S (2014). Astrocytic laminin regulates pericyte differentiation and maintains blood brain barrier integrity. Nat Commun 5(1), 3413.CrossRefGoogle ScholarPubMed
Zhao, Z, Nelson, AR, Betsholtz, C & Zllokovic, BV (2015). Establishment and dysfunction of the blood-brain barrier. Cell 163(5), 1064–1078.CrossRefGoogle ScholarPubMed
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