Functional and genetic analysis of choroid plexus development in zebrafish

Frontiers in Neuroscience

Volumn 8, Issue OCT, 2014, Pages

  Henson, Hannah E ^a,b,d   Parupalli, Chaithanyarani ^a   Ju, Bensheng ^a   Taylor, Michael R ^a,c  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

^d UNIVERSITY OF KENTUCKY   (United States)

Author keywords

choroid plexus; Claudin 5; Fluorescein genetic mapping; Forward genetic screen; Transporters; Zebrafish

Indexed keywords

CLAUDIN 5; ENHANCED GREEN FLUORESCENT PROTEIN; ETHYLNITROSOUREA; GENOMIC DNA;

ADULT; ANIMAL CELL; ARTICLE; BLOOD CEREBROSPINAL FLUID BARRIER; BRAIN DEVELOPMENT; BRAIN FUNCTION; CARCINOGENESIS; CEREBROSPINAL FLUID; CHOROID PLEXUS; CHROMOSOME 13; CONFOCAL MICROSCOPY; DEGENERATIVE DISEASE; DNA ISOLATION; EMBRYO; ENHANCER REGION; ESSENTIAL GENE; GENE EXPRESSION; GENE MAPPING; GENE MUTATION; GENE SEQUENCE; GENETIC ANALYSIS; HYDROCEPHALUS; IMMUNOHISTOCHEMISTRY; NONHUMAN; PHENOTYPE; SOUTHERN BLOTTING; TIGHT JUNCTION; ZEBRA FISH;

EID: 84949117024     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2014.00364     Document Type: Article

References (61)

1. Alvira-Botero, X., and Carro, E.M. (2010). Clearance of amyloid-beta peptide across the choroid lexus in Alzheimer's disease. Curr Aging Sci 3, 219-229.
2. Bill, B.R., Balciunas, D., Mccarra, J.A., Young, E.D., Xiong, T., Spahn, A.M., Garcia-Lecea, M., Korzh, V., Ekker, S.C., and Schimmenti, LA. (2008). Development and Notch signaling requirements of the zebrafish choroid plexus. PLoS One 3, e3114.
3. Craig, M.P., Gilday, S.D., Dabiri, D., and Hove, J.R. (2012). An optimized method for delivering flow tracer particles to intravital fluid environments in the developing zebrafish. Zebrafish 9, 108-119.
4. Currle, D.S., Cheng, X., Hsu, CM., and Monuki, E.S. (2005). Direct and indirect roles of CNS dorsal midline cells in choroid plexus epithelia formation. Development 132, 3549-3559.
5. Daoud, R., Kast, C, Gros, P., and Georges, E. (2000). Rhodamine 123 binds to multiple sites in the multidrug resistance protein (MRP1). Biochemistry 39, 15344-15352.
6. Dohrmann, G.J. (1970). The choroid plexus: a historical review. Brain Res 18, 197-218.
7. Driever, W., Solnica-Krezel, L, Schier, A.F., Neuhauss, S.C., Malicki, J., Stemple, D.L., Stainier, D.Y., Zwartkruis, F., Abdelilah, S., Rangini, Z., Belak, J., and Boggs, C. (1996). A genetic screen for mutations affecting embryogenesis in zebrafish. Development 123, 37-46.
8. Dziegielewska, K.M., Ek, J., Habgood, M.D., and Saunders, N.R. (2001). Development of the choroid plexus. Microsc Res Tech 52, 5-20.
9. Folgueira, M., Bayley, P., Navratilova, P., Becker, T.S., Wilson, S.W., and Clarke, J.D. (2012). Morphogenesis underlying the development of the everted teleost telencephalon. Neural Dev 7, 32.
10. Garcia-Lecea, M., Kondrychyn, I., Fong, S.H., Ye, Z.R., and Korzh, V. (2008). In vivo analysis of choroid plexus morphogenesis in zebrafish. PLoS One 3, e3090.
11. Goldsmith, J.R., and Jobin, C. (2012). Think small: zebrafish as a model system of human pathology. J Biomed Biotechnol 2012, 817341.
12. Gonzalez, A.M., Podvin, S., Lin, S.Y., Miller, M.C., Botfield, H., Leadbeater, W.E., Roberton, A., Dang, X., Knowling, S.E., Cardenas-Galindo, E., Donahue, J.E., Stopa, E.G., Johanson, C.E., Coimbra, R., Eliceiri, B.P., and Baird, A. (2011). Ecrg4 expression and its product augurin in the choroid plexus: impact on fetal brain development, cerebrospinal fluid homeostasis and neuroprogenitor cell response to CNS injury. Fluids Barriers CNS 8, 6.
13. Gutzman, J.H., and Sive, H. (2009). Zebrafish brain ventricle injection. J Vis Exp
14. Horvitz, H.R. (1999). Genetic control of programmed cell death in the nematode Caenorhabditis elegans. Cancer Res 59, 1701s-1706s.
15. Huang, X., Ketova, T., Fleming, J.T., Wang, H., Dey, S.K., Litingtung, Y., and Chiang, C. (2009). Sonic hedgehog signaling regulates a novel epithelial progenitor domain of the hindbrain choroid plexus. Development 136, 2535-2543.
16. Irvin, D.K., Nakano, I., Paucar, A., and Kornblum, H.I. (2004). Patterns of Jagged1, Jagged2, Delta-like 1 and Delta-like 3 expression during late embryonic and postnatal brain development suggest multiple functional roles in progenitors and differentiated cells. J Neurosci Res 75, 330-343.
17. Jansen, W.F., De Weger, R.A., Woutersen, R.A., Van Loveren, H., and Van De Kamer, J.C. (1976). The saccus dorsalis of the rainbow trout, Salmo gairdneri Richardson: histological, cytochemical, electron microscopical and autoradiographical observations. Cell Tissue Res 167, 467-491.
18. Janssen, S.F., Van Der Spek, S.J., Ten Brink, J.B., Essing, A.H., Gorgels, T.G., Van Der Spek, P.J., Jansonius, N.M., and Bergen, A.A. (2013). Gene expression and functional annotation of the human and mouse choroid plexus epithelium. PLoS One 8, e83345.
19. Jiao, S., Dai, W., Lu, L, Liu, Y., Zhou, J., Li, Y., Korzh, V., and Duan, C. (2011). The conserved clusterin gene is expressed in the developing choroid plexus under the regulation of notch but not IGF signaling in zebrafish. Endocrinology 152, 1860-1871.
20. Johansson, P.A., Irmler, M., Acampora, D., Beckers, J., Simeone, A., and Gotz, M. (2013). The transcription factor Otx2 regulates choroid plexus development and function. Development 140, 1055-1066.
21. Keep, R.F., and Smith, D.E. (2011). Choroid plexus transport: gene deletion studies. Fluids Barriers CNS 8, 26
22. Kratzer, I., Liddelow, S.A., Saunders, N.R., Dziegielewska, K.M., Strazielle, N., and Ghersi-Egea, J.F. (2013). Developmental changes in the transcriptome of the rat choroid plexus in relation to neuroprotection. Fluids Barriers CNS 10, 25.
23. Kratzer, I., Vasiljevic, A., Rey, C, Fevre-Montange, M., Saunders, N., Strazielle, N., and Ghersi-Egea, J.F. (2012). Complexity and developmental changes in the expression pattern of claudins at the blood- CSF barrier. Histochem Cell Biol 138, 861-879.
24. Lagaraine, C, Skipor, J., Szczepkowska, A., Dufourny, L., and Thiery, J.C. (2011). Tight junction proteins vary in the choroid plexus of ewes according to photoperiod. Brain Res 1393, 44-51.
25. Liddelow, S.A., Dziegielewska, K.M., Mollgard, K., Whish, S.C., Noor, N.M., Wheaton, B.J., Gehwolf, R., Wagner, A., Traweger, A., Bauer, H., Bauer, H.C., and Saunders, N.R. (2014). Cellular Specificity of the Blood-CSF Barrier for Albumin Transfer across the Choroid Plexus Epithelium. PLoS One 9, e106592.
26. Liddelow, S.A., Dziegielewska, K.M., Vandeberg, J.L, and Saunders, N.R. (2010). Development of the lateral ventricular choroid plexus in a marsupial, Monodelphis domestica. Cerebrospinal Fluid Res 7, 16.
27. Liddelow, S.A., Temple, S., Mollgard, K., Gehwolf, R., Wagner, A., Bauer, H., Bauer, H.C., Phoenix, T.N., Dziegielewska, K.M., and Saunders, N.R. (2012). Molecular characterisation of transport mechanisms at the developing mouse blood-CSF interface: a transcriptome approach. PLoS One 7, e33554.
28. Lippoldt, A., Liebner, S., Andbjer, B., Kalbacher, H., Wolburg, H., Haller, H., and Fuxe, K. (2000). Organization of choroid plexus epithelial and endothelial cell tight junctions and regulation of claudin-1, -2 and -5 expression by protein kinase C. Neuroreport 11, 1427-1431.
29. Lowery, L.A., De Rienzo, G., Gutzman, J.H., and Sive, H. (2009). Characterization and classification of zebrafish brain morphology mutants. Anat Rec (Hoboken) 292, 94-106.
30. Lowery, L.A., Rubin, J., and Sive, H. (2007). Whitesnake/sfpq is required for cell survival and neuronal development in the zebrafish. Dev Dyn 236, 1347-1357.
31. Lowery, L.A., and Sive, H. (2005). Initial formation of zebrafish brain ventricles occurs independently of circulation and requires the nagie oko and snakehead/atp1a1a.1 gene products. Development 132, 2057-2067.
32. Meinke, D.W., and Sussex, I.M. (1979). Embryo-lethal mutants of Arabidopsis thaliana. A model system for genetic analysis of plant embryo development. Dev Biol 72, 50-61.
33. Monnot, A.D., and Zheng, W. (2013). Culture of choroid plexus epithelial cells and in vitro model of blood-CSF barrier. Methods Mol Biol 945, 13-29.
34. Muto, A., Orger, M.B., Wehman, A.M., Smear, M.C., Kay, J.N., Page-Mccaw, P.S., Gahtan, E., Xiao, T., Nevin, L.M., Gosse, N.J., Staub, W., Finger-Baier, K., and Baier, H. (2005). Forward genetic analysis of visual behavior in zebrafish. PLoS Genet 1, e66.
35. Nielsen, CM., and Dymecki, S.M. (2010). Sonic hedgehog is required for vascular outgrowth in the hindbrain choroid plexus. Dev Biol 340, 430-437.
36. Nolan, P.M., Peters, J., Strivens, M., Rogers, D., Hagan, J., Spurr, N., Gray, I.C., Vizor, L., Brooker, D., Whitehill, E., Washbourne, R., Hough, T., Greenaway, S., Hewitt, M., Liu, X., Mccormack, S., Pickford, K., Selley, R., Wells, C, Tymowska-Lalanne, Z., Roby, P., Glenister, P., Thornton, C, Thaung, C, Stevenson, J.A., Arkell, R., Mburu, P., Hardisty, R., Kiernan, A., Erven, A., Steel, K.P., Voegeling, S., Guenet, J.L., Nickols, C, Sadri, R., Nasse, M., Isaacs, A., Davies, K., Browne, M., Fisher, E.M., Martin, J., Rastan, S., Brown, S.D., and Hunter, J. (2000). A systematic, genome-wide, phenotype-driven mutagenesis programme for gene function studies in the mouse. Nat Genet 25, 440-443.
37. Nusslein-Volhard, C, and Wieschaus, E. (1980). Mutations affecting segment number and polarity in Drosophila. Nature 287, 795-801.
38. Omura, Y., Korf, H.W., and Oksche, A. (1985). Vascular permeability (problem of the blood-brain barrier) in the pineal organ of the rainbow trout, Salmo gairdneri. Cell Tissue Res 239, 599-610.
39. Saengkhae, C, Loetchutinat, C, and Garnier-Suillerot, A. (2003). Kinetic analysis of rhodamines efflux mediated by the multidrug resistance protein (MRP1). Biophys J 85, 2006-2014.
40. 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.
41. Schmidt, R., Strahle, U., and Scholpp, S. (2013). Neurogenesis in zebrafish-from embryo to adult. Neural Dev 8, 3.
42. Sehnert, A.J., Huq, A., Weinstein, B.M., Walker, C, Fishman, M., and Stainier, D.Y. (2002). Cardiac troponin T is essential in sarcomere assembly and cardiac contractility. Nat Genet 31, 106-110.
43. Shapiro, A.B., and Ling, V. (1998). Stoichiometry of coupling of rhodamine 123 transport to ATP hydrolysis by P-glycoprotein. Eur J Biochem 254, 189-193.
44. Sin, O., Michels, H., and Nollen, E.A. (2014). Genetic screens in Caenorhabditis elegans models for neurodegenerative diseases. Biochim Biophys Acta.
45. Skinner, D.C., and Malpaux, B. (1999). High melatonin concentrations in third ventricular cerebrospinal fluid are not due to Galen vein blood recirculating through the choroid plexus. Endocrinology 140, 4399-4405.
46. Stemple, D.L, Solnica-Krezel, L, Zwartkruis, F., Neuhauss, S.C., Schier, A.F., Malicki, J., Stainier, D.Y., Abdelilah, S., Rangini, Z., Mountcastle-Shah, E., and Driever, W. (1996). Mutations affecting development of the notochord in zebrafish. Development 123, 117-128.
47. Strazielle, N., and Ghersi-Egea, J.F. (2000). Choroid plexus in the central nervous system: biology and physiopathology. J Neuropathol Exp Neurol 59, 561-574.
48. Strazielle, N., and Preston, J.E. (2003). Transport across the choroid plexuses in vivo and in vitro. Methods Mol Med 89, 291-304.
49. Sykes, D., Sweet, D.H., Lowes, S., Nigam, S.K., Pritchard, J.B., and Miller, D.S. (2004). Organic anion transport in choroid plexus from wild-type and organic anion transporter 3 (Slc22a8)-null mice. Am J Physiol Renal Physiol 286, F972-978.
50. Thambisetty, M., Simmons, A., Velayudhan, L, Hye, A., Campbell, J., Zhang, Y., Wahlund, L.O., Westman, E., Kinsey, A., Guntert, A., Proitsi, P., Powell, J., Causevic, M., Killick, R., Lunnon, K., Lynham, S., Broadstock, M., Choudhry, F., Howlett, D.R., Williams, R.J., Sharp, S.I., Mitchelmore, C, Tunnard, C, Leung, R., Foy, C, O'brien, D., Breen, G., Furney, S.J., Ward, M., Kloszewska, I., Mecocci, P., Soininen, H., Tsolaki, M., Vellas, B., Hodges, A., Murphy, D.G., Parkins, S., Richardson, J.C., Resnick, S.M., Ferrucci, L., Wong, D.F., Zhou, Y., Muehlboeck, S., Evans, A., Francis, P.T., Spenger, C, and Lovestone, S. (2010). Association of plasma clusterin concentration with severity, pathology, and progression in Alzheimer disease. Arch Gen Psychiatry 67, 739-748.
51. Tsuneki, K. (1986). A survey of occurrence of about seventeen circumventricular organs in brains of various vertebrates with special reference to lower groups. J Hirnforsch 27, 441-470.
52. Umans, R.A., and Taylor, M.R. (2012). Zebrafish as a model to study drug transporters at the blood-brain barrier. Clin Pharmacol Ther 92, 567-570.
53. Vercellino, M., Votta, B., Condello, C, Piacentino, C, Romagnolo, A., Merola, A., Capello, E., Mancardi, G.L., Mutani, R., Giordana, M.T., and Cavalla, P. (2008). Involvement of the choroid plexus in multiple sclerosis autoimmune inflammation: a neuropathological study. J Neuroimmunol 199, 133-141.
54. Villalobos, A.R., Miller, D.S., and Renfro, J.L. (2002). Transepithelial organic anion transport by shark choroid plexus. Am J Physiol Regul Integr Comp Physiol 282, R1308-1316.
55. White, R.M., Sessa, A., Burke, C, Bowman, T., Leblanc, J., Ceol, C, Bourque, C, Dovey, M., Goessling, W., Burns, C.E., and Zon, L.I. (2008). Transparent adult zebrafish as a tool for in vivo transplantation analysis. Cell Stem Cell 2, 183-189.
56. Wijnholds, J., Delange, E.C., Scheffer, G.L., Van Den Berg, D.J., Mol, C.A., Van Der Valk, M., Schinkel, A.H., Scheper, R.J., Breimer, D.D., and Borst, P. (2000). Multidrug resistance protein 1 protects the choroid plexus epithelium and contributes to the blood-cerebrospinal fluid barrier. J Clin Invest 105, 279-285.
57. Winata, C.L., Korzh, S., Kondrychyn, I., Zheng, W., Korzh, V., and Gong, Z. (2009). Development of zebrafish swimbladder: The requirement of Hedgehog signaling in specification and organization of the three tissue layers. Dev Biol 331, 222-236.
58. Wodarczyk, C, Rowe, I., Chiaravalli, M., Pema, M., Qian, F., and Boletta, A. (2009). A novel mouse model reveals that polycystin-1 deficiency in ependyma and choroid plexus results in dysfunctional cilia and hydrocephalus. PLoS One 4, e7137.
59. Wolburg, H., and Paulus, W. (2010). Choroid plexus: biology and pathology. Acta Neuropathol 119, 75-88.
60. Xie, J., Farage, E., Sugimoto, M., and Anand-Apte, B. (2010). A novel transgenic zebrafish model for bloodbrain and blood-retinal barrier development. BMC Dev Biol 10, 76.
61. Zhang, J., Piontek, J., Wolburg, H., Piehl, C, Liss, M., Otten, C, Christ, A., Willnow, T.E., Blasig, I.E., and Abdelilah-Seyfried, S. (2010). Establishment of a neuroepithelial barrier by Claudin5a is essential for zebrafish brain ventricular lumen expansion. Proc Natl Acad Sci USA 107,1425-1430.