Outer brain barriers in rat and human development

Frontiers in Neuroscience

Volumn 9, Issue FEB, 2015, Pages

  Brochner C B ^a   Holst, C B ^b   Mollgard K ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b Mental Health Services CPH   (Denmark)

Author keywords

Arachnoid blood CSF barrier; development; outer CSF brain barrier; pial microvessel blood CSF barrier; SSEA 4; subarachnoid space; YKL 40

Indexed keywords

ANTIBODY; BRAIN LIPID BINDING PROTEIN; CLAUDIN 11; COLLAGEN ANTIBODY; COLLAGEN TYPE 1; EXCITATORY AMINO ACID TRANSPORTER 1; INTERLEUKIN 13 ANTIBODY; INTERLEUKIN 13 RECEPTOR ALPHA2; LIPID BINDING PROTEIN; MICROTUBULE ASSOCIATED PROTEIN 2; PROTEIN; STAGE SPECIFIC EMBRYO ANTIGEN 4; UNCLASSIFIED DRUG; YKL40 PROTEIN;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARACHNOID; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; BLOOD CEREBROSPINAL FLUID BARRIER; BRAIN DEVELOPMENT; CONCEPTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; FETUS; FETUS (ANATOMY); FETUS DEVELOPMENT; FOREBRAIN; GLIA; HUMAN; HUMAN CELL; HUMAN DEVELOPMENT; HUMAN EMBRYO; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MENINX; MICROVASCULATURE; MORPHOLOGICAL TRAIT; NONHUMAN; OUTER BRAIN BARRIER; RAT; SUBARACHNOID SPACE;

EID: 84924364334     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2015.00075     Document Type: Article

References (63)

1. Abbott, N. J., Patabendige, A. A., Dolman, D. E., Yusof, S. R., and Begley, D. J. (2010). Structure and function of the blood-brain barrier. Neurobiol. Dis. 37, 13-25.
2. Adewumi, O., Aflatoonian, B., Ahrlund-Richter, L., Amit, M., Andrews, P. W., Beighton, G., Bello, P. A., Benvenisty, N., Berry, L. S., Bevan, S., Blum, B., Brooking, J., Chen, K. G., Choo, A. B., Churchill, G. A., Corbel, M., Damjanov, I., Draper, J. S., Dvorak, P., Emanuelsson, K., Fleck, R. A., Ford, A., Gertow, K., Gertsenstein, M., Gokhale, P. J., Hamilton, R. S., Hampl, A., Healy, L. E., Hovatta, O., Hyllner, J., Imreh, M. P., Itskovitz-Eldor, J., Jackson, J., Johnson, J. L., Jones, M., Kee, K., King, B. L., Knowles, B. B., Lako, M., Lebrin, F., Mallon, B. S., Manning, D., Mayshar, Y., McKay, R. D., Michalska, A. E., Mikkola, M., Mileikovsky, M., Minger, S. L., Moore, H. D., Mummery, C. L., Nagy, A., Nakatsuji, N., O'Brien, C. M., Oh, S. K., Olsson, C., Otonkoski, T., Park, K. Y., Passier, R., Patel, H., Patel, M., Pedersen, R., Pera, M. F., Piekarczyk, M. S., Pera, R. A., Reubinoff, B. E., Robins, A. J., Rossant, J., Rugg-Gunn, P., Schulz, T. C., Semb, H., Sherrer, E. S., Siemen, H., Stacey, G. N., Stojkovic, M., Suemori, H., Szatkiewicz, J., Turetsky, T., Tuuri, T., van den Brink, S., Vintersten, K., Vuoristo, S., Ward, D., Weaver, T. A., Young, L. A., and Zhang, W. (2007). Characterization of human embryonic stem cell lines by the International Stem Cell Initiative. Nat. Biotechnol. 25, 803-816.
3. Agrawal, S., Anderson, P., Durbeej, M., van, R. N., Ivars, F., Opdenakker, G., and Sorokin, L. M. (2006). Dystroglycan is selectively cleaved at the parenchymal basement membrane at sites of leukocyte extravasation in experimental autoimmune encephalomyelitis. J. Exp. Med. 203, 1007-1019.
4. Allt, G., and Lawrenson, J. G. (1997). Is the pial microvessel a good model for blood-brain barrier studies? Brain Res. Brain Res. Rev. 24(1), 67-76.
5. Arion, D., Unger, T., Lewis, D. A., Levitt, P., and Mirnics, K. (2007). Molecular evidence for increased expression of genes related to immune and chaperone function in the prefrontal cortex in schizophrenia. Biol. Psychiatry 62, 711-721.
6. Balslev, Y., Saunders, N. R., and Møllgård, K. (1997). Ontogenetic development of diffusional restriction to protein at the pial surface of the rat brain: an electron microscopical study. J. Neurocytol. 26, 133-148.
7. Barraud, P., Stott, S., Møllgård, K., Parmar, M., and Björklund, A. (2007). In vitro characterization of a human neural progenitor cell coexpressing SSEA4 and CD133. J. Neurosci. Res. 85, 250-259.
8. Bartholomaus, I., Kawakami, N., Odoardi, F., Schlager, C., Miljkovic, D., Ellwart, J. W., Klinkert, W. E., Flugel-Koch, C., Issekutz, T. B., Wekerle, H., and Flugel, A. (2009). Effector T cell interactions with meningeal vascular structures in nascent autoimmune CNS lesions. Nature 462, 94-98.
9. Bjørnbak, C., Brøchner, C. B., Larsen, L. A., Johansen, J. S., and Møllgård, K. (2014). Brain barriers and a subpopulation of astroglial progenitors of developing human forebrain are immunostained for the glycoprotein YKL-40. J. Histochem. Cytochem. 62, 369-388.
10. Bonneh-Barkay, D., Wang, G., Starkey, A., Hamilton, R. L., and Wiley, C. A. (2010). In vivo CHI3L1 (YKL-40) expression in astrocytes in acute and chronic neurological diseases. J. Neuroinflammation. 7, 34.
11. Brinker, T., Stopa, E., Morrison, J., and Klinge, P. (2014). A new look at cerebrospinal fluid circulation. Fluids Barriers. CNS. 11, 10.
12. Brocklehurst, G. (1969). The development of the human cerebrospinal fluid pathway with particular reference to the roof of the fourth ventricle. J. Anat. 105, 467-475.
13. Broman, T. (1949). The permeability of cerebrospinal vessels in normal and pathological conditions. Ejnar Munksgaard. Copenhagen. 92 pp.
14. Brøchner, C. B., Johansen, J. S., Larsen, L. A., Bak, M., Mikkelsen, H. B., Byskov, A. G., Andersen, C. Y., and Møllgård, K. (2012). YKL-40 is differentially expressed in human embryonic stem cells and in cell progeny of the three germ layers. J. Histochem. Cytochem. 60, 188-204.
15. Chung, C., Tallerico, T., and Seeman, P. (2003). Schizophrenia hippocampus has elevated expression of chondrex glycoprotein gene. Synapse 50, 29-34.
16. Clancy, B., Darlington, R. B., and Finlay, B. L. (2001). Translating developmental time across mammalian species. Neuroscience 105, 7-17.
17. Colin, C., Baeza, N., Bartoli, C., Fina, F., Eudes, N., Nanni, I., Martin, P. M., Ouafik, L., and Figarella- Branger, D. (2006). Identification of genes differentially expressed in glioblastoma versus pilocytic astrocytoma using Suppression Subtractive Hybridization. Oncogene 25, 2818-2826.
18. Colton, C. A., Mott, R. T., Sharpe, H., Xu, Q., Van Nostrand, W. E., and Vitek, M. P. (2006). Expression profiles for macrophage alternative activation genes in AD and in mouse models of AD. J. Neuroinflammation. 3, 27.
19. Decimo, I., Fumagalli, G., Berton, V., Krampera, M., and Bifari, F. (2012). Meninges: from protective membrane to stem cell niche. Am. J. Stem Cells 1, 92-105.
20. Engelhardt, B., and Coisne, C. (2011). Fluids and barriers of the CNS establish immune privilege by confining immune surveillance to a two-walled castle moat surrounding the CNS castle. Fluids Barriers. CNS. 8, 4.
21. Feig, S. L., and Haberly, L. B. (2011). Surface-associated astrocytes, not endfeet, form the glia limitans in posterior piriform cortex and have a spatially distributed, not a domain, organization. J. Comp Neurol. 519, 1952-1969.
22. Feng, L., Hatten, M. E., and Heintz, N. (1994). Brain lipid-binding protein (BLBP): a novel signaling system in the developing mammalian CNS. Neuron 12, 895-908.
23. Garbett, K., Ebert, P. J., Mitchell, A., Lintas, C., Manzi, B., Mirnics, K., and Persico, A. M. (2008). Immune transcriptome alterations in the temporal cortex of subjects with autism. Neurobiol. Dis. 30, 303-311.
24. Giachino, C., Basak, O., Lugert, S., Knuckles, P., Obernier, K., Fiorelli, R., Frank, S., Raineteau, O., Alvarez-Buylla, A., and Taylor, V. (2014). Molecular diversity subdivides the adult forebrain neural stem cell population. Stem Cells 32, 70-84.
25. He, C. H., Lee, C. G., Dela Cruz, C. S., Lee, C. M., Zhou, Y., Ahangari, F., Ma, B., Herzog, E. L., Rosenberg, S. A., Li, Y., Nour, A. M., Parikh, C. R., Schmidt, I., Modis, Y., Cantley, L., and Elias, J. A. (2013). Chitinase 3-like 1 regulates cellular and tissue responses via IL-13 receptor alpha2. Cell Rep. 4, 830-841.
26. Howard, B., Chen, Y., and Zecevic, N. (2006). Cortical progenitor cells in the developing human telencephalon. Glia 53, 57-66.
27. Ichikawa, H., and Itoh, K. (2011). Blood-arachnoid barrier disruption in experimental rat meningitis detected using gadolinium-enhancement ratio imaging. Brain Res. 1390, 142-149.
28. Johannson, P. A., Dziegielewska, K. M., Liddelow, S. A, and Saunders, N. R. (2008). The blood-CSF barrier explained: when development is not immaturity. Bioessays. 30(3), 237-248.
29. Johansen, J. S., Høyer, P. E., Larsen, L. A., Price, P. A., and Møllgård, K. (2007). YKL-40 protein expression in the early developing human musculoskeletal system. J. Histochem. Cytochem. 55(12), 1213-1228.
30. Kadhim, H. J., Gadisseux, J. F., and Evrard, P. (1988). Topographical and cytological evolution of the glial phase during prenatal development of the human brain: histochemical and electron microscopic study. J. Neuropathol. Exp. Neurol. 47, 166-188.
31. Kipp, M., Gingele, S., Pott, F., Clarner, T., van der Valk, P., Denecke, B., Gan, L., Siffrin, V., Zipp, F., Dreher, W., Baumgartner, W., Pfeifenbring, S., Godbout, R., Amor, S., and Beyer, C. (2011). BLBP expression in astrocytes during experimental demyelination and in human multiple sclerosis lesions. Brain Behav. Immun. 25, 1554-1568.
32. Ku, B. M., Lee, Y. K., Ryu, J., Jeong, J. Y., Choi, J., Eun, K. M., Shin, H. Y., Kim, D. G., Hwang, E. M., Yoo, J. C., Park, J. Y., Roh, G. S., Kim, H. J., Cho, G. J., Choi, W. S., Paek, S. H., and Kang, S. S. (2011). CHI3L1 (YKL-40) is expressed in human gliomas and regulates the invasion, growth and survival of glioma cells. Int. J. Cancer 128, 1316-1326.
33. Lal, A., Lash, A. E., Altschul, S. F., Velculescu, V., Zhang, L., McLendon, R. E., Marra, M. A., Prange, C., Morin, P. J., Polyak, K., Papadopoulos, N., Vogelstein, B., Kinzler, K. W., Strausberg, R. L., and Riggins, G. J. (1999). A public database for gene expression in human cancers. Cancer Res. 59, 5403-5407.
34. Lou, Y. W., Wang, P. Y., Yeh, S. C., Chuang, P. K., Li, S. T., Wu, C. Y., Khoo, K. H., Hsiao, M., Hsu, T. L., and Wong, C. H. (2014). Stage-specific embryonic antigen-4 as a potential therapeutic target in glioblastoma multiforme and other cancers. Proc. Natl. Acad. Sci. U. S. A 111, 2482-2487.
35. Malecki, M., Anderson, M., Beauchaine, M., Seo, S., Tombokan, X., and Malecki, R. (2012). TRA-1-60, SSEA-4, Oct4A, Nanog Clones of Pluripotent Stem Cells in the Embryonal Carcinomas of the Ovaries. J. Stem Cell Res. Ther. 2(5), pii:130.
36. Michelsen, A. E., Rathcke, C. N., Skjelland, M., Holm, S., Ranheim, T., Krohg-Sorensen, K., Klingvall, M. F., Brosstad, F., Oie, E., Vestergaard, H., Aukrust, P., and Halvorsen, B. (2010). Increased YKL-40 expression in patients with carotid atherosclerosis. Atherosclerosis 211, 589-595.
37. Møllgård, K., and Jacobsen, M. (1984). Immunohistochemical identification of some plasma proteins in human embryonic and fetal forebrain with particular reference to the development of the neocortex. Brain Res. 315(1), 49-63.
38. Møllgård, K., Balslev, Y., Lauritzen, B., and Saunders, N. R. (1987). Cell junctions and membrane specializations in the ventricular zone (germinal matrix) of the developing sheep brain: a CSF-brain barrier. J Neurocytol. 16, 433-444.
39. Morita, K., Sasaki, H., Fujimoto, K., Furuse, M., and Tsukita, S. (1999). Claudin-11/OSP-based tight junctions of myelin sheaths in brain and Sertoli cells in testis. J. Cell Biol. 145(3), 579-588.
40. Morrow, C. M., Mruk, D., Cheng, C. Y., and Hess, R. A. (2010). Claudin and occludin expression and function in the seminiferous epithelium. Philos. Trans. R. Soc. Lond B Biol. Sci. 365, 1679-1696.
41. Muldoon, L. L., Alvarez, J. I., Begley, D. J., Boado, R. J., Del Zoppo, G. J., Doolittle, N. D., Engelhardt, B., Hallenbeck, J. M., Lonser, R. R., Ohlfest, J. R., Prat, A., Scarpa, M., Smeyne, R. J., Drewes, L. R., and Neuwelt, E. A. (2013). Immunologic privilege in the central nervous system and the blood-brain barrier. J. Cereb. Blood Flow Metab 33, 13-21.
42. Nabeshima, S., Reese, T. S., Landis, D. M., and Brightman, M. W. (1975). Junctions in the meninges and marginal glia. J. Comp Neurol. 164, 127-169.
43. Nigro, J. M., Misra, A., Zhang, L., Smirnov, I., Colman, H., Griffin, C., Ozburn, N., Chen, M., Pan, E., Koul, D., Yung, W. K., Feuerstein, B. G., and Aldape, K. D. (2005). Integrated array-comparative genomic hybridization and expression array profiles identify clinically relevant molecular subtypes of glioblastoma. Cancer Res. 65, 1678-1686.
44. Noisa, P., Ramasamy, T. S., Lamont, F. R., Yu, J. S., Sheldon, M. J., Russell, A., Jin, X., and Cui, W. (2012). Identification and characterisation of the early differentiating cells in neural differentiation of human embryonic stem cells. PLoS. One. 7, e37129.
45. Noto, Z., Yoshida, T., Okabe, M., Koike, C., Fathy, M., Tsuno, H., Tomihara, K., Arai, N., Noguchi, M., and Nikaido, T. (2013). CD44 and SSEA-4 positive cells in an oral cancer cell line HSC-4 possess cancer stem like cell characteristics. Oral Oncol. 49, 787-795.
46. O'Rahilly, R., and Muller, F. (1986). The meninges in human development. J. Neuropathol. Exp. Neurol. 45, 588-608.
47. O'Rahilly, R., and Muller, F. (2010). Developmental stages in human embryos: revised and new measurements. Cells Tissues. Organs 192, 73-84.
48. Ransohoff, R. M., Kivisakk, P., and Kidd, G. (2003). Three or more routes for leukocyte migration into the central nervous system. Nat. Rev. Immunol. 3, 569-581.
49. Rascher, G., and Wolburg, H. (1997). The tight junctions of the leptomeningeal blood-cerebrospinal fluid barrier during development. J. Hirnforsch. 38, 525-540.
50. Saunders, N. R., Daneman, R., Dziegielewska, K. M., and Liddelow, S. A. (2013). Transporters of the blood brain and blood-CSF interfaces in development and in the adult. Mol. Aspects Med. 34, 742-752.
51. Saunders, N. R., Dreifuss, J-F., Dziegielewska, K. M., Johansson, P. A., Habgood, M. D., Møllgård. K., and Bauer, H-C. (2015) The rights and wrongs of blood-brain barrier permeability studies: a walk through 100 years of history. Frontiers in Neuroscience, in press/Saunders, N. R., Ek, C. J., Habgood, M. D., and Dziegielewska, K. M. (2008). Barriers in the brain: a renaissance? Trends Neurosci. 31, 279-286.
52. Saunders, N. R., Liddelow, S. A., and Dziegielewska, K. M. (2012). Barrier mechanisms in the developing brain. Front Pharmacol. 3, 46.
53. Schmechel, D. E., and Rakic, P. (1979) A Golgi study of radial glial cells in developing monkey telencephalon: morphogenesis and transformation into astrocytes. Anat. Embryol. (Berl.) 156(2), 115-152.
54. Schwartz, M., Kipnis, J., Rivest, S., and Prat, A. (2013). How do immune cells support and shape the brain in health, disease, and aging? J. Neurosci. 33, 17587-17596.
55. Siegenthaler, J. A., Ashque A. M., Zarbalis K., Patterson K. P., Hecth J. H., Kane M. A. et al. (2009). Retinoic acid from the meninges regulates cortical neuron generation. Cell 139, 597-609.
56. Siegenthaler, J. A., and Pleasure, S. J. (2011). We have got you 'covered': how the meninges control brain development. Curr. Opin. Genet. Dev. 21, 249-255.
57. Stolp, H. B., Dziegielewska, K. M., Ek, C. J., Habgood, M. D., Lane, M. A., Potter, A. M., and Saunders, N. R. (2005). Breakdown of the blood-brain barrier to proteins in white matter of the developing brain following systemic inflammation. Cell Tissue Res. 320, 369-378.
58. Stolp, H. B., Liddelow, S. A., Sa-Pereira, I., Dziegielewska, K. M., and Saunders, N. R. (2013). Immune responses at brain barriers and implications for brain development and neurological function in later life. Front Integr. Neurosci. 7, 61.
59. Verney, C., Monier, A., Fallet-Bianco, C., and Gressens, P. (2010). Early microglial colonization of the human forebrain and possible involvement in periventricular white-matter injury of preterm infants. J. Anat. 217, 436-448.
60. Voigt, T. (1989). Development of glial cells in the cerebral wall of ferrets: direct tracing of their transformation from radial glia into astrocytes. J. Comp. Neurol. 289(1), 74-88.
61. Whish, S., Dziegielewska, K. M., Møllgård, K., Noor, N. M., Liddelow, S. A., Habgood, M. D., Richardson S. J., and Saunders, N. R. (2015). The inner CSF-brain barrier: developmentally controlled access to the brain. Frontiers in Neurosceince, in press.
62. Xu, L. Z., Sánchez, R., Sali, A., and Heintz, N. (1996). Ligand specificity of brain lipid-binding protein. J. Biol. Chem. 271(40), 24711-24719.
63. Yasuda, K., Cline, C., Vogel, P., Onciu, M., Fatima, S., Sorrentino, B. P., Thirumaran, R. K., Ekins, S., Urade, Y., Fujimori, K., and Schuetz, E. G. (2013). Drug transporters on arachnoid barrier cells contribute to the blood-cerebrospinal fluid barrier. Drug Metab Dispos. 41, 923-931.