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Published in: Fluids and Barriers of the CNS 1/2006

Open Access 01-12-2006 | Research

Cerebrospinal fluid supports viability and proliferation of cortical cells in vitro, mirroring in vivo development

Authors: Jaleel A Miyan, Mahjiub Zendah, Farhad Mashayekhi, P Jane Owen-Lynch

Published in: Fluids and Barriers of the CNS | Issue 1/2006

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Abstract

Background

The central nervous system develops around a fluid filled compartment. Recently, attention has turned to the potential role of the fluid (cerebrospinal fluid, CSF) in the developmental process. In particular, the cerebral cortex develops from the germinal epithelium adjacent to the CSF with regulation of cell proliferation and differentiation provided by cells adjacent to the fluid-filled subarachnoid space.

Methods

Histological analysis of fetal rat cortical sections was used to follow the extent of in vivo cortical development. A quantitative analysis of proliferation and migration of cortical cells at E17 – E21 was obtained through immunocytochemical staining of bromodeoxyuridine (BrdU) -labelled cells. In vitro studies were performed on primary cortical cells at days E17-E20, maintained in either Neurobasal media or 100% fetal rat CSF for 72 h before analysis of proliferation.

Results

The proliferation potential of primary cortical cells varied depending on the age of extraction. E17 and E20 cells showed little proliferation while E18 and E19 cell showed the maximum. The CSF from fetuses of all ages tested, except E21, was able to maintain primary cortical cells from the developing fetus in vitro and to stimulate and support their proliferation in the absence of any additions. E17 cells showed little proliferation in any media while E19 cells showed maximum proliferation in E19 and E20 CSF.

Conclusion

CSF composition most probably changes with age, as does the proliferation potential of cells in the developing cerebral cortex. CSF alone supports viability as well as proliferation of cortical cells. CSF must therefore be regarded as an important environmental influence in brain development and can be used in vitro to maintain both the viability of cortical progenitor cells and their age-related proliferative potential.
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Literature
1.
2.
go back to reference Ostenfeld T, Svendsen CN: Recent advances in stem cell neurobiology. Adv Tech Stand Neurosurg. 2003, 28: 3-89.PubMed Ostenfeld T, Svendsen CN: Recent advances in stem cell neurobiology. Adv Tech Stand Neurosurg. 2003, 28: 3-89.PubMed
3.
go back to reference Bottai D: Neural stem cells: plasticity and therapeutic potential. J Neurochem. 2003, 85 Suppl 2: 13-10.1046/j.1471-4159.85.s2.13_2.x.CrossRef Bottai D: Neural stem cells: plasticity and therapeutic potential. J Neurochem. 2003, 85 Suppl 2: 13-10.1046/j.1471-4159.85.s2.13_2.x.CrossRef
4.
go back to reference McKay R: Stem cells and the cellular organization of the brain. J Neurosci Res. 2000, UNITED STATES , 59 (3): 298-300. 10.1002/(SICI)1097-4547(20000201)59:3<298::AID-JNR2>3.0.CO;2-U. McKay R: Stem cells and the cellular organization of the brain. J Neurosci Res. 2000, UNITED STATES , 59 (3): 298-300. 10.1002/(SICI)1097-4547(20000201)59:3<298::AID-JNR2>3.0.CO;2-U.
5.
go back to reference Gage FH: Mammalian neural stem cells. Science. 2000, 287 (5457): 1433-1438. 10.1126/science.287.5457.1433.CrossRefPubMed Gage FH: Mammalian neural stem cells. Science. 2000, 287 (5457): 1433-1438. 10.1126/science.287.5457.1433.CrossRefPubMed
6.
go back to reference Parmar M, Skogh C, Bjorklund A, Campbell K: Regional specification of neurosphere cultures derived from subregions of the embryonic telencephalon. Mol Cell Neurosci. 2002, 21 (4): 645-656. 10.1006/mcne.2002.1204.CrossRefPubMed Parmar M, Skogh C, Bjorklund A, Campbell K: Regional specification of neurosphere cultures derived from subregions of the embryonic telencephalon. Mol Cell Neurosci. 2002, 21 (4): 645-656. 10.1006/mcne.2002.1204.CrossRefPubMed
7.
go back to reference Kornblum HI, Yanni DS, Easterday MC, Seroogy KB: Expression of the EGF receptor family members ErbB2, ErbB3, and ErbB4 in germinal zones of the developing brain and in neurosphere cultures containing CNS stem cells. Dev Neurosci. 2000, SWITZERLAND , 22 (1-2): 16-24. 10.1159/000017423. Kornblum HI, Yanni DS, Easterday MC, Seroogy KB: Expression of the EGF receptor family members ErbB2, ErbB3, and ErbB4 in germinal zones of the developing brain and in neurosphere cultures containing CNS stem cells. Dev Neurosci. 2000, SWITZERLAND , 22 (1-2): 16-24. 10.1159/000017423.
8.
go back to reference Dono R: Fibroblast growth factors as regulators of central nervous system development and function. Am J Physiol Regul Integr Comp Physiol. 2003, 284 (4): R867-81.CrossRefPubMed Dono R: Fibroblast growth factors as regulators of central nervous system development and function. Am J Physiol Regul Integr Comp Physiol. 2003, 284 (4): R867-81.CrossRefPubMed
9.
go back to reference Palmer TD, Markakis EA, Willhoite AR, Safar F, Gage FH: Fibroblast growth factor-2 activates a latent neurogenic program in neural stem cells from diverse regions of the adult CNS. J Neurosci. 1999, UNITED STATES , 19 (19): 8487-8497. Palmer TD, Markakis EA, Willhoite AR, Safar F, Gage FH: Fibroblast growth factor-2 activates a latent neurogenic program in neural stem cells from diverse regions of the adult CNS. J Neurosci. 1999, UNITED STATES , 19 (19): 8487-8497.
10.
go back to reference Krieglstein K, Strelau J, Schober A, Sullivan A, Unsicker K: TGF-ß and the regulation of neuron survival and death. Journal of Physiology-Paris. 2002, 96 (1-2): 25-30. 10.1016/S0928-4257(01)00077-8.CrossRef Krieglstein K, Strelau J, Schober A, Sullivan A, Unsicker K: TGF-ß and the regulation of neuron survival and death. Journal of Physiology-Paris. 2002, 96 (1-2): 25-30. 10.1016/S0928-4257(01)00077-8.CrossRef
11.
go back to reference Miyan JA, Nabiyouni M, Zendah M: Development of the brain: a vital role for cerebrospinal fluid. Can J Physiol Pharmacol. 2003, 81 (4): 317-328. 10.1139/y03-027.CrossRefPubMed Miyan JA, Nabiyouni M, Zendah M: Development of the brain: a vital role for cerebrospinal fluid. Can J Physiol Pharmacol. 2003, 81 (4): 317-328. 10.1139/y03-027.CrossRefPubMed
12.
go back to reference Gato A, Martin P, Alonso MI, Martin C, Pulgar MA, Moro JA: Analysis of cerebro-spinal fluid protein composition in early developmental stages in chick embryos. J Exp Zoolog A Comp Exp Biol. 2004, 301 (4): 280-289. 10.1002/jez.a.20035.CrossRef Gato A, Martin P, Alonso MI, Martin C, Pulgar MA, Moro JA: Analysis of cerebro-spinal fluid protein composition in early developmental stages in chick embryos. J Exp Zoolog A Comp Exp Biol. 2004, 301 (4): 280-289. 10.1002/jez.a.20035.CrossRef
13.
go back to reference Owen-Lynch PJ, Draper CE, Mashayekhi F, Bannister CM, Miyan JA: Defective cell cycle control underlies abnormal cortical development in the hydrocephalic Texas rat. BRAIN. 2003, 126 (3): Owen-Lynch PJ, Draper CE, Mashayekhi F, Bannister CM, Miyan JA: Defective cell cycle control underlies abnormal cortical development in the hydrocephalic Texas rat. BRAIN. 2003, 126 (3):
14.
go back to reference Mashayekhi F, Draper CE, Pourghasem M, Bannister CM, Owen-Lynch PJ, Miyan JA: Deficient cortical development in the hydrocephalic Texas (H-Tx) rat: a role for cerebrospinal fluid. BRAIN. 2002, 125 (8): 1859-1874. 10.1093/brain/awf182.CrossRefPubMed Mashayekhi F, Draper CE, Pourghasem M, Bannister CM, Owen-Lynch PJ, Miyan JA: Deficient cortical development in the hydrocephalic Texas (H-Tx) rat: a role for cerebrospinal fluid. BRAIN. 2002, 125 (8): 1859-1874. 10.1093/brain/awf182.CrossRefPubMed
15.
go back to reference Miyan JA, Mashayekhi F, Bannister CM: Developmental abnormalities in early-onset hydrocephalus: clues to signalling. Symp Soc Exp Biol. 2001, England , 91-106. Miyan JA, Mashayekhi F, Bannister CM: Developmental abnormalities in early-onset hydrocephalus: clues to signalling. Symp Soc Exp Biol. 2001, England , 91-106.
16.
go back to reference Dziegielewska KM, Ek J, Habgood MD, Saunders NR: Development of the choroid plexus. Microsc Res Tech. 2001, 52 (1): 5-20. 10.1002/1097-0029(20010101)52:1<5::AID-JEMT3>3.0.CO;2-J.CrossRefPubMed Dziegielewska KM, Ek J, Habgood MD, Saunders NR: Development of the choroid plexus. Microsc Res Tech. 2001, 52 (1): 5-20. 10.1002/1097-0029(20010101)52:1<5::AID-JEMT3>3.0.CO;2-J.CrossRefPubMed
17.
go back to reference Chodobski A, Szmydynger-Chodobska J: Choroid plexus: target for polypeptides and site of their synthesis. Microsc Res Tech. 2001, 52 (1): 65-82. 10.1002/1097-0029(20010101)52:1<65::AID-JEMT9>3.0.CO;2-4.CrossRefPubMed Chodobski A, Szmydynger-Chodobska J: Choroid plexus: target for polypeptides and site of their synthesis. Microsc Res Tech. 2001, 52 (1): 65-82. 10.1002/1097-0029(20010101)52:1<65::AID-JEMT9>3.0.CO;2-4.CrossRefPubMed
18.
go back to reference Stopa EG, Berzin TM, Kim S, Song P, Kuo-LeBlanc V, Rodriguez-Wolf M, Baird A, Johanson CE: Human choroid plexus growth factors: What are the implications for CSF dynamics in Alzheimer's disease?. Exp Neurol. 2001, 167 (1): 40-47. 10.1006/exnr.2000.7545.CrossRefPubMed Stopa EG, Berzin TM, Kim S, Song P, Kuo-LeBlanc V, Rodriguez-Wolf M, Baird A, Johanson CE: Human choroid plexus growth factors: What are the implications for CSF dynamics in Alzheimer's disease?. Exp Neurol. 2001, 167 (1): 40-47. 10.1006/exnr.2000.7545.CrossRefPubMed
19.
go back to reference Desmond ME, Jacobson AG: Embryonic brain enlargement requires cerebrospinal fluid pressure. Dev Biol. 1977, 57 (1): 188-198. 10.1016/0012-1606(77)90364-5.CrossRefPubMed Desmond ME, Jacobson AG: Embryonic brain enlargement requires cerebrospinal fluid pressure. Dev Biol. 1977, 57 (1): 188-198. 10.1016/0012-1606(77)90364-5.CrossRefPubMed
20.
go back to reference Pexieder T, Jelinek R: Pressure of the CSF and the morphogenesis of the CNS. II. Pressure necessary for normal development of brain vesicles. Folia Morphol (Praha). 1970, 18 (2): 181-192. Pexieder T, Jelinek R: Pressure of the CSF and the morphogenesis of the CNS. II. Pressure necessary for normal development of brain vesicles. Folia Morphol (Praha). 1970, 18 (2): 181-192.
21.
go back to reference Armstrong RJ, Svendsen CN: Neural stem cells: from cell biology to cell replacement. Cell Transplant. 2000, UNITED STATES , 9 (2): 139-152. Armstrong RJ, Svendsen CN: Neural stem cells: from cell biology to cell replacement. Cell Transplant. 2000, UNITED STATES , 9 (2): 139-152.
22.
go back to reference Korzhevskii DE: [Structural organization of choroid plexus primordium in human telencephalon]. Morfologiia. 2002, 121 (1): 63-67.PubMed Korzhevskii DE: [Structural organization of choroid plexus primordium in human telencephalon]. Morfologiia. 2002, 121 (1): 63-67.PubMed
23.
go back to reference Gato A, Moro JA, Alonso MI, Bueno D, De la Mano A, Martin C: Embryonic cerebrospinal fluid regulates neuroepithelial survival, proliferation, and neurogenesis in chick embryos. Anatomical Record Part A-Discoveries In Molecular Cellular And Evolutionary Biology. 2005, 284A (1): 475-484. 10.1002/ar.a.20185.CrossRef Gato A, Moro JA, Alonso MI, Bueno D, De la Mano A, Martin C: Embryonic cerebrospinal fluid regulates neuroepithelial survival, proliferation, and neurogenesis in chick embryos. Anatomical Record Part A-Discoveries In Molecular Cellular And Evolutionary Biology. 2005, 284A (1): 475-484. 10.1002/ar.a.20185.CrossRef
24.
go back to reference Ohmiya M, Shudai T, Nitta A, Nomoto H, Furukawa Y, Furukawa S: Brain-derived neurotrophic factor alters cell migration of particular progenitors in the developing mouse cerebral cortex. Neuroscience Letters. 2002, 317 (1): 21-24. 10.1016/S0304-3940(01)02412-0.CrossRefPubMed Ohmiya M, Shudai T, Nitta A, Nomoto H, Furukawa Y, Furukawa S: Brain-derived neurotrophic factor alters cell migration of particular progenitors in the developing mouse cerebral cortex. Neuroscience Letters. 2002, 317 (1): 21-24. 10.1016/S0304-3940(01)02412-0.CrossRefPubMed
25.
go back to reference Ringstedt T, Linnarsson S, Wagner J, Lendahl U, Kokaia Z, Arenas E, Ernfors P, Ibanez CF: BDNF regulates reelin expression and Cajal-Retzius cell development in the cerebral cortex. Neuron. 1998, UNITED STATES , 21 (2): 305-315. 10.1016/S0896-6273(00)80540-1. Ringstedt T, Linnarsson S, Wagner J, Lendahl U, Kokaia Z, Arenas E, Ernfors P, Ibanez CF: BDNF regulates reelin expression and Cajal-Retzius cell development in the cerebral cortex. Neuron. 1998, UNITED STATES , 21 (2): 305-315. 10.1016/S0896-6273(00)80540-1.
26.
go back to reference Saunders NR, Habgood MD, Dziegielewska KM: Barrier mechanisms in the brain, I. Adult brain. Clin Exp Pharmacol Physiol. 1999, 26 (1): 11-19. 10.1046/j.1440-1681.1999.02986.x.CrossRefPubMed Saunders NR, Habgood MD, Dziegielewska KM: Barrier mechanisms in the brain, I. Adult brain. Clin Exp Pharmacol Physiol. 1999, 26 (1): 11-19. 10.1046/j.1440-1681.1999.02986.x.CrossRefPubMed
27.
go back to reference Saunders NR, Habgood MD, Dziegielewska KM: Barrier mechanisms in the brain, II. Immature brain. Clin Exp Pharmacol Physiol. 1999, 26 (2): 85-91. 10.1046/j.1440-1681.1999.02987.x.CrossRefPubMed Saunders NR, Habgood MD, Dziegielewska KM: Barrier mechanisms in the brain, II. Immature brain. Clin Exp Pharmacol Physiol. 1999, 26 (2): 85-91. 10.1046/j.1440-1681.1999.02987.x.CrossRefPubMed
28.
go back to reference Dziegielewska KM, Knott GW, Saunders NR: The nature and composition of the internal environment of the developing brain. Cell Mol Neurobiol. 2000, 20 (1): 41-56. 10.1023/A:1006943926765.CrossRefPubMed Dziegielewska KM, Knott GW, Saunders NR: The nature and composition of the internal environment of the developing brain. Cell Mol Neurobiol. 2000, 20 (1): 41-56. 10.1023/A:1006943926765.CrossRefPubMed
29.
go back to reference Super H, Del Rio JA, Martinez A, Perez-Sust P, Soriano E: Disruption of neuronal migration and radial glia in the developing cerebral cortex following ablation of Cajal-Retzius cells. Cereb Cortex. 2000, UNITED STATES , 10 (6): 602-613. 10.1093/cercor/10.6.602. Super H, Del Rio JA, Martinez A, Perez-Sust P, Soriano E: Disruption of neuronal migration and radial glia in the developing cerebral cortex following ablation of Cajal-Retzius cells. Cereb Cortex. 2000, UNITED STATES , 10 (6): 602-613. 10.1093/cercor/10.6.602.
30.
go back to reference Gilmore EC, Herrup K: Cortical development: receiving reelin. Curr Biol. 2000, ENGLAND , 10 (4): R162-6. 10.1016/S0960-9822(00)00332-8. Gilmore EC, Herrup K: Cortical development: receiving reelin. Curr Biol. 2000, ENGLAND , 10 (4): R162-6. 10.1016/S0960-9822(00)00332-8.
31.
go back to reference Bar I, Lambert de Rouvroit C, Goffinet AM: The Reelin-signaling pathway and mouse cortical development. Results Probl Cell Differ. 2000, GERMANY , 30: 255-276. Bar I, Lambert de Rouvroit C, Goffinet AM: The Reelin-signaling pathway and mouse cortical development. Results Probl Cell Differ. 2000, GERMANY , 30: 255-276.
32.
go back to reference Frotscher M: Cajal-Retzius cells, Reelin, and the formation of layers. Curr Opin Neurobiol. 1998, ENGLAND , 8 (5): 570-575. 10.1016/S0959-4388(98)80082-2. Frotscher M: Cajal-Retzius cells, Reelin, and the formation of layers. Curr Opin Neurobiol. 1998, ENGLAND , 8 (5): 570-575. 10.1016/S0959-4388(98)80082-2.
33.
go back to reference D'Arcangelo G, Curran T: Reeler: new tales on an old mutant mouse. Bioessays. 1998, ENGLAND , 20 (3): 235-244. 10.1002/(SICI)1521-1878(199803)20:3<235::AID-BIES7>3.0.CO;2-Q. D'Arcangelo G, Curran T: Reeler: new tales on an old mutant mouse. Bioessays. 1998, ENGLAND , 20 (3): 235-244. 10.1002/(SICI)1521-1878(199803)20:3<235::AID-BIES7>3.0.CO;2-Q.
34.
go back to reference Curran T, D'Arcangelo G: Role of reelin in the control of brain development. Brain Res Brain Res Rev. 1998, NETHERLANDS , 26 (2-3): 285-294. 10.1016/S0165-0173(97)00035-0. Curran T, D'Arcangelo G: Role of reelin in the control of brain development. Brain Res Brain Res Rev. 1998, NETHERLANDS , 26 (2-3): 285-294. 10.1016/S0165-0173(97)00035-0.
Metadata
Title
Cerebrospinal fluid supports viability and proliferation of cortical cells in vitro, mirroring in vivo development
Authors
Jaleel A Miyan
Mahjiub Zendah
Farhad Mashayekhi
P Jane Owen-Lynch
Publication date
01-12-2006
Publisher
BioMed Central
Published in
Fluids and Barriers of the CNS / Issue 1/2006
Electronic ISSN: 2045-8118
DOI
https://doi.org/10.1186/1743-8454-3-2

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