Cellular transfer of macromolecules across the developing choroid plexus of Monodelphis domestica

European Journal of Neuroscience

Volumn 29, Issue 2, 2009, Pages 253-266

  Liddelow, Shane A ^a   Dziegielewska, Katarzyna M ^a   Ek, C Joakim ^a   Johansson, Pia A ^a   Potter, Ann M ^a   Saunders, Norman R ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Biotinylated dextran amine; Blood CSF barrier; Cerebrospinal fluid; Developing brain; Protein transfer

Indexed keywords

DEXTRAN DERIVATIVE; FETUIN; HEMOPEXIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL COUNT; CELL SPECIFICITY; CELL TRANSFER; CEREBROSPINAL FLUID; CHOROID PLEXUS; CONTROLLED STUDY; EPITHELIUM CELL; FEMALE; IMMUNOCYTOCHEMISTRY; MACROMOLECULE; MALE; MONODELPHIS DOMESTICA; NONHUMAN; OPOSSUM; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN TRANSPORT;

ANIMALS; BIOLOGICAL MARKERS; BIOLOGICAL TRANSPORT, ACTIVE; BLOOD-BRAIN BARRIER; BRAIN; CEREBROSPINAL FLUID; CHOROID PLEXUS; EPITHELIAL CELLS; FEMALE; LATERAL VENTRICLES; MALE; MODELS, ANIMAL; MOLECULAR PROBES; MONODELPHIS; NERVE TISSUE PROTEINS;

EID: 58449117390     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2008.06571.x     Document Type: Article

References (67)

1. Adam, E., Dziegielewska, K.M., Saunders, N.R. Schumacher, U. (1993) Neuraminic acid specific lectins as markers of early cortical plate neurons. Int. J. Dev. Neurosci., 11, 451 460.
2. Adinolfi, M. (1985) The development of the human blood-CSF-brain barrier. Dev. Med. Child Neurol., 27, 532 537.
3. Aleshire, S.J., Bradley, C.A., Richardson, L.D. Parl, F.F. (1983) Localization of human prealbumin in choroid plexus epithelium. J. Histochem. Cytochem., 31, 608 612.
4. Baehr, C.H., Fricker, G. Miller, D.S. (2006) Fluorescein-methotrexate transport in dogfish shark (Squalus acanthias) choroid plexus. Am. J. Physiol. Regul. Integr. Comp. Physiol., 291, R464 R472.
5. Balin, B.J. Broadwell, R.D. (1988) Transcytosis of protein through the mammalian cerebral epithelium and endothelium. I. Choroid plexus and the blood-cerebrospinal fluid barrier. J. Neurocytol., 17, 809 826.
6. Banks, W.A. Broadwell, R.D. (1994) Blood to brain and brain to blood passage of native horseradish peroxidase, wheat germ agglutinin and albumin: pharmacokinetic analysis and morphological assessments. J. Neurochem., 62, 2404 2419.
7. Balslev, Y., Dziegielewska, K.M., Møllgård, K. Saunders, N.R. (1997) Intercellular barriers to and transcellular transfer of protein albumin in the fetal sheep. Anat. Embryol., 195, 229 236.
8. 14C] inulin after intrathecal infusion. Brain Res., 52, 323 333.
9. Birge, W.J., Rose, A.D., Haywood, J.R. Doolin, P.F. (1974) Development of the blood-cerebrospinal fluid barrier to proteins and differentiation of cerebrospinal fluid in the chick embryo. Dev. Biol., 41, 245 254.
10. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 72, 248 254.
11. Brightman, M.W. Reese, T.S. (1969) Junctions between intimately apposed cell membranes in the vertebrate brain. J. Cell Biol., 40, 648 677.
12. Broadwell, R.D. Sofroniew, M.V. (1993) Serum proteins bypass the blood-brain fluid barriers for extracellular entry to the central nervous system. Exp. Neurol., 120, 245 263.
13. Broadwell, R.D., Balin, B.J., Salcman, M. Kaplan, R.S. (1983) Brain-blood barrier? Yes and no. Proc. Natl Acad. Sci. USA, 80, 7332 7356.
14. Cancilla, P.A., Zimmerman, H.M. Becker, N.H. (1966) A histochemical and fine structure study of the developing rat choroid plexus. Acta Neuropathol. (Berl), 6, 188 200.
15. Christie, D.L., Dziegielewska, K.M., Hill, R.M. Saunders, N.R. (1987) Fetuin: the bovine homologue of human alpha 2HS glycoprotein. FEBS Lett., 214, 45 49.
16. Clementi, F. (1970) Effect of horseradish peroxidase on mice lung capillaries' permeability. J. Histochem. Cytochem., 18, 887 892.
17. Davson, H. Segal, M.B. (1996) Physiology of the CSF and blood-brain barriers. CRC Press, Boca Raton, FL.
18. Donaldson, H.H. (1894) Preliminary observations on some changes caused in the nervous tissues by reagents commonly employed to harden them. J. Morphol., 9, 123 166.
19. Dziegielewska, K.M., Evans, C.A., Malinowska, D.H., Møllgå rd, K., Reynolds, M.L. Saunders, N.R. (1980) Blood-cerebrospinal fluid transfer of plasma proteins during fetal development in the sheep. J. Physiol., 300, 457 465.
20. Dziegielewska, K.M., Evans, C.A.N., Lai, P.C.W., Lorscheider, F.L., Malinowska, D.H., Møllgård, K. Saunders, N.R. (1981) Proteins in cerebrospinal fluid and plasma of fetal rats during development. Dev. Biol., 83, 193 200.
21. Dziegielewska, K.M., Møllgård, K., Reynolds, M.L. Saunders, N.R. (1987) A fetuin-related glycoprotein (alpha 2HS) in human embryonic and fetal development. Cell Tissue Res., 248, 33 41.
22. Dziegielewska, K.M., Habgood, M.D., Jones, H.C., Reader, M. Saunders, N.R. (1989) Proteins in cerebrospinal fluid and plasma of postnatal Monodelphis domestica (grey short-tailed opossum). Comp. Biochem. Physiol., 92B, 569 576.
23. Dziegielewska, K.M., Habgood, M.D., Møllgård, K., Stagaard, M. Saunders, N.R. (1991) Species-specific transfer of plasma albumin from blood into different cerebrospinal fluid compartments in the fetal sheep. J. Physiol., 439, 215 237.
24. Dziegielewska, K.M., Knott, G.W. Saunders, N.R. (2000) The nature and composition of the internal environment of the developing brain. Cell. Mol. Neurobiol., 20, 41 56.
25. Dziegielewska, K.M., Ek, J., Habgood, M.D. Saunders, N.R. (2001) Development of the choroid plexus. Microsc. Res. Tech., 52, 5 20.
26. Ek, C.J., Habgood, M.D., Dziegielewska, K.M., Potter, A. Saunders, N.R. (2001) Permeability and route of entry for lipid-insoluble molecules across brain barriers in developing Monodelphis domestica. J. Physiol., 536, 841 853.
27. Ek, C.J., Habgood, M.D., Dziegielewska, K.M. Saunders, N.R. (2003) Structural characteristics and barrier properties of the choroid plexuses in developing brain of the opossum (Monodelphis domestica). J. Comp. Neurol., 460, 451 464.
28. Ek, C.J., Dziegielewska, K.M. Saunders, N.R. (2005) Development of the blood-cerebrospinal fluid barrier. In Zheng, W. Chodobski, A. (Eds Blood-Cerebrospinal Fluid Barrier. CRC Press, Boca, Raton, pp. 3 23.
29. Ek, C.J., Dziegielewska, K.M., Stolp, H.B. Saunders, N.R. (2006) Functional effectiveness of the blood-barrier to small water-soluble molecules in developing and adult opossum (Monodelphis domestica). J. Comp. Neurol., 496, 13 26.
30. Evans, C.A., Reynolds, J.M., Reynolds, M.L., Saunders, N.R. Segal, M.B. (1974) The development of a blood-brain barrier mechanism in foetal sheep. J. Physiol., 238, 371 386.
31. Ferguson, R.K. Woodbury, D.M. (1969) Penetration of 14C-inulin and 14C-sucrose into brain, cerebrospinal fluid, and skeletal muscle of developing rats. Exp. Brain Res., 7, 181 194.
32. Guillery, R.W. (2002) On counting and counting errors. J. Comp. Neurol., 447, 1 7.
33. Guillery, R.W. Herrup, K. (1997) Quantification without pontification: choosing a method for counting objects in sectioned tissues. J. Comp. Neurol., 386, 2 7.
34. Habgood, M.D., Sedgwick, J.E., Dziegielewska, K.M. Saunders, N.R. (1992) A developmentally regulated blood-cerebrospinal fluid transfer mechanism for albumin in immature rats. J. Physiol., 456, 181 192.
35. Habgood, M.D., Knott, G.W., Dziegielewska, K.M. Saunders, N.R. (1993) The nature of the decrease in blood-cerebrospinal fluid barrier exchange during postnatal brain development in the rat. J. Physiol., 468, 73 83.
36. Ingvarsson, B.I., Carlsson, R.N. Karlsson, B.W. (1978) Synthesis of alpha-fetoprotein, albumin and total serum protein in neonatal pigs. Biol. Neonate, 34, 259 268.
37. Jacobsen, G.K., Jacobsen, M. Henriksen, O.B. (1981) An immunohistochemical study of a series of plasma proteins in the early human conceptus. Oncodev. Biol. Med., 2, 399 410.
38. Johansson, P.A., Dziegielewska, K.M., Ek, C.J., Habgood, M.D., Møllgård, K., Potter, A., Schuliga, M. Saunders, N.R. (2005) Aquaporin-1 in the choroid plexuses of developing mammalian brain. Cell Tissue Res., 322, 353 364.
39. Johansson, P.A., Dziegielewska, K.M., Ek, C.J., Habgood, M.D., Liddelow, S.A., Potter, A.M., Stolp, H.B. Saunders, N.R. (2006) Blood-CSF barrier function during choroid plexus development in the rat. Eur. J. Neurosci., 24, 65 76.
40. Johansson, P.A., Dziegielewska, K.M., Liddelow, S.A. Saunders, N.R. (2008) The blood-CSF barrier explained: when development is not immaturity. Bioessays, 30, 237 248.
41. Kniesel, U., Risau, W. Wolburg, H. (1996) Development of blood-brain barrier tight junctions in the rat cortex. Brain Res. Dev. Brain Res., 96, 229 240.
42. Knott, G.W., Dziegielewska, K.M., Habgood, M.D., Li, Z.S. Saunders, N.R. (1997) Albumin transfer across the choroid plexus of South American opossum (Monodelphis domestica). J. Physiol., 499, 179 194.
43. Kraus, D.B. Fadem, B.H. (1987) Reproduction, development and physiology of the gray short-tailed opossum (Monodelphis domestica). Lab. Anim. Sci., 37, 478 482.
44. Kusuhara, H. Sugiyama, Y. (2004) Efflux transport systems for organic anions and cations at the blood-CSF barrier. Adv. Drug Deliv. Rev., 56, 1741 1763.
45. Lai, P.C., Mears, G.J., van Petten, G.R., Hay, D.M. Lorscheider, F.L. (1978) Fetal-maternal distribution of ovine alpha-fetoprotein. Am. J. Physiol., 235, E27 E31.
46. Li, Z.S., Dziegielewska, K.M. Saunders, N.R. (1997) Transthyretin distribution in the developing choroid plexus of South America opossum, Monodelphis domestica. Cell Tissue Res., 287, 621 624.
47. Madsen, J.K. Møllgård, K. (1979) The tight epithelium of the Mongolian gerbil subcommissural organ as revealed by freeze-fracturing. J. Neurocytol., 8, 481 491.
48. Møllgård, K. Rostgaard, J. (1978) Morphological aspects of some sodium transporting epithelia suggesting a transcellular pathway via elements of endoplasmic reticulum. J. Membrane Biol., 40, 71 89.
49. Møllgård, K. Saunders, N.R. (1975) Complex tight junctions of epithelial and of endothelial cells in early foetal brain. J. Neurocytol., 4, 453 468.
50. Møllgård, K. Saunders, N.R. (1977) A possible transepithelial pathway via endoplasmic reticulum in foetal sheep choroid plexus. Proc. R. Soc. Lond. B Biol. Sci., 199, 321 326.
51. Møllgård, K., Lauritzen, B. Saunders, N.R. (1979) Double replica technique applied to choroid plexus from early foetal sheep: completeness and complexity of tight junctions. J. Neurocytol., 8, 139 149.
52. Normand, I.C.S., Oliver, R.E., Reynolds, E.O.R. Strang, L.B. (1971) Permeability of lung capillaries and alveoli to non-electrolytes in the foetal lamb. J. Physiol., 219, 303 330.
53. Parvas, M., Parada, C. Bueno, D. (2008) A blood-CSF barrier function controls embryonic CSF protein composition and homeostasis during early CNS development. Dev. Biol., 321, 51 63.
54. Petrov, T., Howarth, A.G., Krukoff, T.L. Stevenson, B.R. (1994) Distribution of the tight junction-associated protein ZO-1 in circumventricular organs of the CNS. Mol. Brain Res., 21, 235 246.
55. Pineiro, A., Calvo, M., Iguaz, F., Lampreave, F. Naval, J. (1982) Characterization, origin and evolution of alpha-fetoprotein and albumin in postnatal rat brain. Int. J. Biochem., 14, 817 823.
56. Saunders, N.R. (1992) Ontogenic development of brain barrier mechanisms. In Bradbury, M.W.B. (Ed. Handbook of Experimental Pharmacology. Physiology and Pharmacology of the Blood-Brain Barrier. Springer-Verlag, Berlin, Heiberlberg, New York, pp. 327 369.
57. Saunders, N.R., Adam, E., Reader, M. Møllgård, K. (1989) Monodelphis domestica (grey short-tailed opossum): an accessible model for studies of early neocortical development. Anat. Embryol. (Berl), 180, 227 236.
58. Saunders, N.R., Habgood, M.D. Dziegielewska, K.M. (1999) Barrier mechanisms in the brain, II. Immature brain. Clin. Exp. Pharmacol. Physiol., 26, 85 91.
59. Saunders, N.R., Knott, G.W. Dziegielewska, K.M. (2000) Barriers in the immature brain. Cell. Mol. Neurobiol., 20, 29 40.
60. Schreiber, G., Aldred, A.R., Jaworowski, A., Nilsson, C., Achen, M.G. Segal, M.B. (1990) Thyroxine transport from blood to brain via transthyretin synthesis in choroid plexus. Am. J. Physiol., 258, R338 R345.
61. Smith, K.M., Lai, P.C., Robertson, H.A., Church, R.B. Lorscheider, F.L. (1979) Distribution of alpha 1-fetoprotein in fetal plasma, allantoic fluid, amniotic fluid and maternal plasma of cows. J. Reprod. Fertil., 57, 235 238.
62. Smith, D.E., Johanson, C.E. Keep, R.F. (2004) Peptide and peptide analog transport systems at the blood-CSF barrier. Adv. Drug Deliv. Rev., 56, 1765 1791.
63. Speake, T., Whitwell, C., Kajita, H., Majid, A. Brown, P.D. (2001) Mechanisms of CSF secretion by the choroid plexus. Microsc. Res. Tech., 52, 49 59.
64. Strazielle, N. Ghersi-Egea, J.F. (1999) Demonstration of a coupled metabolism-efflux process at the choroid plexus as a mechanism of brain protection toward xenobiotics. J. Neurosci., 19, 6275 6289.
65. Tauc, M., Vignon, X. Bouchaud, C. (1984) Evidence for the effectiveness of the blood-CSF barrier in the fetal rat choroid plexus. A freeze-fracture and peroxidase diffusion study. Tissue Cell, 16, 65 74.
66. Towbin, H., Staehelin, T. Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl Acad. Sci. USA, 76, 4350 4354.
67. Zheng, W. Zhao, Q. (2002) Establishment and characterization of an immortalized Z310 choroidal epithelial cell line from murine choroid plexus. Brain Res., 958, 371 380.