Influx mechanisms in the embryonic and adult rat choroid plexus: A transcriptome study

Frontiers in Neuroscience

Volumn 9, Issue MAR, 2015, Pages

  Saunders, Norman R ^a   Dziegielewska, Katarzyna M ^a   Møllgård, Kjeld ^c   Habgood, Mark D ^a   Wakefield, Matthew J ^d   Lindsay, Helen ^e   Stratzielle, Nathalie ^f   Ghersi Egea, Jean Francois ^f   Liddelow, Shane A ^a,b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b STANFORD UNIVERSITY   (United States)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^e UNIVERSITY OF ZURICH   (Switzerland)

^f UNIVERSITÉ LYON 1   (France)

Author keywords

Amino acid transfer; Brain barriers; Brain development; Cerebrospinal fluid; Choroid plexus; Protein transfer

Indexed keywords

AMINO ACID; AMINO ACID TRANSPORTER; CARRIER PROTEIN; COMPLEMENTARY DNA; GLUCOSE TRANSPORTER; MESSENGER RNA; MONOCARBOXYLATE TRANSPORTER; THYROID HORMONE; TRANSCRIPTOME;

ADULT; AMINO ACID TRANSPORT; ARTICLE; BRAIN DEVELOPMENT; CELLULAR DISTRIBUTION; CEREBROSPINAL FLUID; CHOROID PLEXUS; DNA LIBRARY; EMBRYO; GENE PRODUCT; GLUCOSE TRANSPORT; IMMUNOHISTOCHEMISTRY; MICROARRAY ANALYSIS; NEXT GENERATION SEQUENCING; NONHUMAN; RAT; RNA SEQUENCE;

EID: 84928168469     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2015.00123     Document Type: Article

References (86)

1. Abbott, N.J., and Friedman, A. (2012). Overview and introduction: the blood-brain barrier in health and disease. Epilepsia, 53, Suppl. 6, 1-6. doi: 10.1111/j.1528-1167.2012.03696.x.
2. Abbott, N.J., Patabendige, A.A., Dolman, D.E., Yusof, S.R., Begley, D.J. (2010). Structure and function of the blood-brain barrier. Neurobiol. Dis. 37(1), 13-25. doi: 0.1016/j.nbd.2009.07.030.
3. Al-Sarraf, H. (2002) Transport of 14C-gamma-aminobutyric acid into brain, cerebrospinal fluid and choroid plexus in neonatal and adult rats. Brain Res. Dev. Brain Res. 139, 121-129.
4. Al-Sarraf, H., Preston, J.E., and Segal, M.B. (1995). The entry of acidic amino acids into brain and CSF during development, using in situ perfusion in the rat. Dev Brain Res. 90, 151-158.
5. Al-Sarraf, H., Preston, J.E., and Segal, M.B. (1997) Changes in the kinetics of the acidic amino acid brain and CSF uptake during development in the rat. Dev. Brain Res. 102, 127-134.
6. Anders, S. (2010). HTSeq 0.4.7p4. http://www-huber.embl.de/users/anders/HTSeq/.
7. Baños, G., Daniel, P.M., and Pratt, O.E. (1978). The effect of age upon the entry of some amino acids into the brain, and their incorporation into cerebral protein. Dev Med Child Neurol. 20, 335-346.
8. Baud, O., Fayol, L., Gressens, P., Pellerin, L., Magistretti, P., et al. (2003). Perinatal and early postnatal changes in the expression of monocarboxylate transporters MCT1 and MCT2 in the rat forebrain. J. Comp. Neurol. 465(3), 445-454.
9. Bauer H (1998). Glucose transporters in mammalian brain development. In Introduction to the Blood-Brain Barrier, Ed WM Pardridge, Cambridge University press, Cambridge. P175-187.
10. Benrabh, H., and Lefauconnier, J.M. (1996). Blood-endothelial cell and blood-brain transport of L-proline, alpha-aminoisobutyric acid, and L-alanine. Neurochem. Res. 21(10), 1227-1235.
11. Beschorner, R., Pantazis, G., Jeibmann, A,. Boy, J., Meyermann, R., Mittelbronn, M., and Schittenhelm, J. (2009). Expression of EAAT-1 distinguishes choroid plexus tumors from normal and reactive choroid plexus epithelium. Acta Neuropath. 117(6), 667-675.
12. Braun, L.D., Cornford, E.M., and Oldendorf, W.H. (1980). Newborn rabbit blood-brain barrier is selectively permeable and differs substantially from the adult. J. Neurochem. 34, 147-152.
13. Brown, P.D., Davies, S.L, Speake, T., and Millar, I.D. (2004) Molecular mechanisms of cerebrospinal fluid production. Neuroscience, 129(4), 957-970.
14. Chen, B., Jiang, Y., Zeng, S., Yan, J., Li, X., et al. (2010) Endocytic sorting and recycling require membrane phosphatidylserine asymmetry maintained by TAT-1/CHAT-1. PLoS Genet 6: e1011235.
15. Chowanadisai, W., Kelleher, S.L., and Lönnerdal, B. (2005). Zinc deficiency is associated with increased brain zinc import and LIV-1 expression and decrease ZnT-1 expression in neonatal rats. J. Nutr.135: 1002-1007.
16. Chowanadisai, W., Graham, D,M, Keen, C.L., Rucker, R.B., and Messerli, M.A. (2013a). Neurulation and neurite extension require the zinc transporter ZIP12 (slc39a12). Proc. Natl. Acad. Sci. U S A. 2110(24), 9903-9908. doi:10.1073/pnas.1222142110.
17. Chowanadisai, W., Graham, D.M., Keen, C.L., Rucker, R.B., and Messerli, M.A. (2013b). A zinc transporter gene required for development of the nervous system. Commun. Integr. Biol. 6(6):e26207. doi: 10.4161/cib.26207. Epub 2013 Aug 21.
18. Cornford, E.M., and Cornford, M.E. (1986). Nutrient transport and the blood-brain barrier in developing animals. Fed. Proc. 45(7), 2065-2072.
19. Cornford, E.M., Braun, L.D., and Oldendorf, W.H. (1982). Developmental modulations of blood-brain barrier permeability as an indicator of changing nutritional requirements in the brain. Pediatr. Res.16, 324-328.
20. Cremer, J.E. (1982). Substrate utilization and brain development. J. Cereb. Blood Flow Metab. 2, 394-407, 1982.
21. Cubelos, B., González-González, I.M., Giménez, C., Zafra, F. (2005). Amino acid transporter SNAT5 localizes to glial cells in the rat brain. Glia, 49(2), 230-244.
22. Damkier, H.H., Nielsen, S., and Praetorius, J. (2007). Molecular expression of SLC4-derived Na+-dependent anion transporters in selected human tissues. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293, R2136-2146.
23. Damkier, H.H., Brown, P.D., and Praetorius, J. (2013). Cerebrospinal fluid secretion by the choroid plexus. Physiol. Rev. 93(4), 1847-1892. doi:10.1152/physrev.00004.2013
24. Davson, H. and Segal, M.B. (1996) Physiology of the CSF and Blood-Brain Barriers. CRC Press.
25. Ek, C.J., Nathanielsz, P., Li, C., and Mallard, C. (2015). Transciptomal changes and functional annotation of the developing non human primate choroid plexus. Front. Neurosci. in press.
26. Evans, C.A., Harbuz, M.S., Ostenfeld, T., Norrish, A., and Blackwell, J.M. (2001). Nramp1 is expressed in neurons and is associated with behavioural and immune responses to stress. Neurogenetics, 3(2), 69-78.
27. Gentleman, R.C., Carey, V.J., Bates, D.M., Bolstad, B., Dettling, M., et al. (2004). Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5, R80.
28. Grabrucker, S., Jannetti, L., Eckert, M., Gaub, S., Chhabra, R., et al. (2014). Zinc deficiency dysregulates the synaptic ProSAP/Shank scaffold and might contribute to autism spectrum disorders. Brain, 137(Pt 1):137-152. doi: 10.1093/brain/awt303.
29. Gray, S., Feinberg, M.W., Hull, S., Kuo, C.T., Watanabe, M., et al. (2002). The Krüppel-like factor KLF15 regulates the insulin-sensitive glucose transporter GLUT4. J. Biol. Chem. 277(37), 34322-34328.
30. Gunter, T.E., Gerstner, B., Gunter, K.K., Malecki, J., Gelein, R. et al. (2013). Manganese transport via the transferrin mechanism. Neurotoxicology. 34, 118-127. doi: 10.1016/j.neuro.2012.10.018.
31. Gybina, A.A., and Prohaska, J.R. (2006). Variable response of selected cuproproteins in rat choroid plexus and cerebellum following perinatal copper deficiency. Genes Nutr. 1(1), 51- 59. doi: 10.1007/BF02829936.
32. Hamdani, el H., Gudbrandsen, M., Bjørkmo, M., and Chaudhry, F.A. (2012). The system N transporter SN2 doubles as a transmitter precursor furnisher and a potential regulator of NMDA receptors. Glia, 60(11), 1671-1683.
33. Hediger, M.A. (2013). The ABCs of membrane transporters in health and disease (SLC series). Mol.Aspects Med. 34 (2-3), 95-752.
34. Hubbard, T.J., Aken, B.L., Ayling, S., Ballester, B., Beal, K., et al. (2009) Ensembl 2009. Nucleic Acids Res. 37(Database issue): D690-697.
35. Janssen, S.F., van der Spek, S.J., Ten Brink, J.B., Essing, A.H., Gorgels, T.G., van der Spek, P.J. et al (2013). Gene expression and functional annotation of the human and mouse choroid plexus epithelium. PLoS One. 8(12):e83345. doi: 10.1371/journal.pone.0083345. eCollection 2013.
36. Johansson, P.A., Dziegielewska, K.M., Ek, C.J., Habgood, M.D., Møllgård, K., Potter, A., et al., (2005). Aquaporin-1 in the choroid plexuses of developing mammalian brain. Cell Tissue Res. 322(3), 353-364.
37. Johansson, 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, 237-248.
38. Keep, R.F., and Jones, H.C. (1990). A morphometric study on the development of the lateral ventricular choroid plexus, choroid plexus capillaries and ventricular ependyma in the rat. Dev. Brain Res. 56, 47-53.
39. Keep, R.F., and Smith, D.E. (2011). Choroid plexus transport: gene deletion studies. Fluids Barriers CNS. 8(1):26. doi: 10.1186/2045-8118-8-26.
40. Kinne, A., Schülein, R., and Krause, G. (2011) Primary and secondary thyroid hormone ransporters. Thyroid Res. 4, S7.
41. Koehler-Stec, E.M., Simpson, I.A., Vannucci, S.J., Landschulz, K.T., and Landschulz, W.H. (1998). Monocarboxylate transporter expression in mouse brain. Am. J. Physiol. 275(3 Pt 1), E516-524.
42. Kohle, S.J., and Vannucci, R.C. (1977). Glycogen metabolism in fetal and postnatal rat brain: influence of birth. J Neurochem. 28(2), 441-443.
43. Kratzer, I., Liddelow, S.A., Saunders, N.R., Strazielle, N., Ghersi-Egea, J.F. (2013). Developmental changes in the transcriptome of the rat choroid plexus in relation to neuroprotection Fluids and Barriers of the CNS, http://www.fluidsbarrierscns.com/content/10/1/25.
44. Kuo, Y.M., Zhou, B., Cosco, D., and Gitschier, J. (2001). The copper transporter CTR1 provides an essential function in mammalian embryonic development. Proc. Natl. Acad. Sci. U S A. 98(12), 6836-6841.
45. Langmead. B., Trapnell, C., Pop, M., and Salzberg, S.L. (2009) Ultrafast and memory efficient alignment of short DNA sequences to the human genome. Genome Biol. 10(3), R25.
46. Lefauconnier, J-M., and Trouvé, R., (1983). Developmental changes in the pattern of amino acid transport at the blood-brain barrier in rats. Brain Res. 283, 175-182.
47. Leino, R.L., Gerhart, D.Z., and Drewes, L.R. (1999). Monocarboxylate transporter (MCT1) abundance in brains of suckling and adult rats: a quantitative electron microscopic immunogold study. Brain Res Dev Brain Res. 113(1-2), 47-54.
48. Leitner, D.F., and Connor, J.R. (2012). Functional roles of transferrin in the brain. Biochim. Biophys. Acta. 1820(3), 393-402. doi: 10.1016/j.bbagen.2011.10.016.
49. 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. doi: 10.1186/1743-8454-7-16.
50. Liddelow, S.A., Temple, S., Møllgård, K., Gehwold, R., Wagner, A., Bauer, H., et al. (2012). Molecular characterisation of transport mechanisms at the developing mouse blood-CSF interface: a transcriptome approach. PloS ONE. 2012;7(3):e33554. doi: 10.1371/journal.pone.0033554.
51. Liddelow, S.A, Dziegielewska, K.M., Ek, C.J., Habgood, M.D., Bauer, H., Bauer, H-C., et al. (2013) Mechanisms that determine the internal environment of the developing brain: a transcriptomic, functional and ultrastructural approach. PLoS ONE, 8(7):e65629. doi: 10.1371/journal.pone.0065629.
52. Marger, L., Schubert, C.R., and Bertrand, D. (2014). Zinc: An underappreciated modulatory actor of brain function. Biochem. Pharmacol. 91(4),426-435. doi: 10.1016/j.bcp.2014.08.002.
53. Marques, F., Sousa, J.C., Coppola, G., Gao, F., Puga, R., Brentani, H. et al. (2011). Transcriptome signature of the adult mouse choroid plexus. Fluids Barriers CNS. 18;8(1):10. doi: 10.1186/2045-8118-8-10.
54. Mckenzie, J.M., Fosmire, G.J., and Sandstead, H.H. (1975). Zinc deficiency during the latter third of pregnancy: Effects on fetal rat brain, liver, and placenta. J. Nutr. 105, 1466-1475.
55. Moos, T., and Morgan, E.H. (1998) Evidence for low molecular weight, non-transferrin-bound iron in rat brain and cerebrospinal fluid. J. Neurosci. Res. 54(4), 486-494.
56. Moos, T., and Morgan, E.H. (2000). Transferrin and transferrin receptor function in brain barrier systems. Cell. Mol. Neurobiol. 20(1), 77-95.
57. Morgan, E.H., and Moos, T. (2002) Mechanism and developmental changes in iron transport across the blood-brain barrier. Dev. Neurosci. 24(2), 106-113.
58. Nehlig, A. (1997). Cerebral energy metabolism, glucose transport and blood flow: changes with maturation and adaptation to hypoglycaemia. Diabetes Metab 23, 18-29.
59. Netsky, M.G., and Shuangshoti, S. (1975). The choroid plexus in health and disease. Bristol: Wright.
60. Porterfield, S.P., and Hendrick, C.E. (1992). Tissue iodothyronine levels in fetuses of control and hypothyroid rats at 13 and 16 days gestation. Endocrinology, 131, 195-200.
61. Rivas, M., and Naranjo, J.R. (2007). Thyroid hormones, learning and memory. Genes Brain Behav. Suppl 1, 40-44.
62. Robinson, M.D., McCarthy, D.J. and Smyth, D.K. (2010). edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26(1), 139- 140.
63. Rouault, T, A., Zhang, De-L., and Jeong, S.Y. (2009). Brain iron homeostasis, the choroid plexus, and localization of iron transport proteins. Metab. Brain Dis. 24, 673-684.
64. Sandstead, H.H. (1985). W.O. Atwater memorial lecture. Zinc: essentiality for brain development and function. Nutr. Rev. 43(5), 129-137.
65. Sandstead, H.H., Fosmire, G.J., McKenzie, J.M., and Halas, E.S. (1975). Zinc deficiency and brain development in the rat. Fed. Proc. 34(1), 86-88.
66. Santamaria, A.B., and Sulsky, S. (2010). Risk assessment of an essential element: manganese. J. Toxicol. Environ. Health A. 73(2), 128-55. doi: 10.1080/15287390903337118.
67. Saunders, N.R., Liddelow, S.A., and Dziegielewska, K.M. (2012). Barrier mechanisms in the developing brain. Front. Pharmacol. 3, 46, 1-18, doi: 10.3389/fphar.2012.00046.
68. 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.
69. Schmitt, C., Strazielle, N., Richaud P., Bouron A., and Ghersi- Egea, J-F. (2011). Active transport at the blood-CSF barrier contributes to manganese influx into the brain. J. Neurochem. 117(4), 747-756
70. Schachenmayr, W.Z (1967). On the development of ependyma and plexus choriodeus of the rat. Zellforsch. Mikrosk. Anat. 77(1), 25-63.
71. Scheiber, I.F., Mercer, J.F., and Dringen, R. (2014). Metabolism and functions of copper in brain. Prog. Neurobiol. 116, 33-57. doi: 10.1016/j.pneurobio.2014.01.002.
72. Segal, M.B. (2001). Transport of nutrients across the choroid plexus. Microsc. Res. Tech. 52(1), 38-48.
73. Sershen, H., and Lajtha, A. (1976). Capillary transport of amino acids in the developing brain. Exp Neurol. 53(2), 465-474.
74. Siddappa, A.J., Rao, R.B., Wobken, J.D., Casperson, K. Leibold, E.A., et al. (2003). Iron deficiency alters iron regulatory protein and iron transport protein expression in the perinatal rat brain. Pediatr. Res. 53(5), 800-807.
75. Singh, N., Haldar, S., Tripathi, A.K., Horback, K., Wong, J., et al. (2014). Brain iron homeostasis: from molecular mechanisms to clinical significance and therapeutic opportunities. Antioxid. Redox. Signal. 20(8),1324-1363. doi: 10.1089/ars.2012.4931.
76. Skeaff, SA (2011) Iodine Deficiency in Pregnancy: The Effect on Neurodevelopment in the Child. Nutrients, 3, 265-273.
77. Tyszka-Czochara, M., Grzywacz, A., Gdula-Argasinska, J., Librowski, T., Wilinski,B., and Opoka, W. (2014). The role of zinc in the pathogenesis and treatment of central nervous system (CNS) diseases. Implications of zinc homeostasis for proper CNS function. Acta Pol. Pharm. 71(3), 369-377.
78. Uriu-Adams, J.Y., Scherr, R.E., Lanoue, L., and Keen, C.L. (2010). Influence of copper on early development: prenatal and postnatal considerations. Biofactors. 36(2), 136-152. doi: 10.1002/biof.85.
79. Vannucci, S.J. (1994). Developmental expression of GLUT1 and GLUT3 glucose transporters in rat brain. J. Neurochem. 62(1), 240-246.
80. Vannucci, R.C., and Vannucci, S.J. (2000). Glucose metabolism in the developing brain. Semin Perinatol. 24(2), 107-115.
81. Vannucci, S.J., Rutherford, T., Wilkie, M.B., Simpson, I.A., and Lauder, J.M. (2000). Prenatal expression of the GLUT4 glucose transporter in the mouse. Dev. Neurosci. 22(4), 274-282.
82. Vannucci, S.J. and Simpson, I.A. (2003). Developmental switch in brain nutrient transporter expression in the rat. Am. J Physiol. Endocrinol. Metab. 285, E1127-E1134.
83. Wang, X., Miller, D.S., Zheng, W. (2008). Intracellular localization and subsequent redistribution of metal transporters in a rat choroid plexus model following exposure to manganese or iron. Toxicol. Appl. Pharmacol. 230(2):167-174. doi: 10.1016/j.taap.2008.02.024.
84. Wright, E.M. (2013). Glucose transport families SLC5 and SLC50. Mol. Aspects. Med. 34(2-3), 183-196. doi: 10.1016/j.mam.2012.11.002.
85. Yon, J.M., Baek, I.J., Lee, S.R., Kim, M.R., Lee, B.J., Yun, Y.W. et al. (2008). Immunohistochemical identification and quantitative analysis of cytoplasmic Cu/Zn superoxide dismutase in mouse organogenesis. J. Vet. Sci. 9(3), 233-240.
86. Yon, J.M., Baek, I.J., Lee, B.J., Yun, Y.W., and Nam, S.Y. (2011). Dynamic expression of manganese superoxide dismutase during mouse embryonic organogenesis. Int. J. Dev. Biol. 55(3), 327-334. doi: 10.1387/ijdb.103270jy.