SVCT2 vitamin C transporter expression in progenitor cells of the postnatal neurogenic niche

Frontiers in Cellular Neuroscience

Volumn , Issue JUL, 2013, Pages

  Pastor, Patricia ^a   Cisternas, Pedro ^a   Salazar, Katterine ^a   Silva Alvarez, Carmen ^a   Oyarce, Karina ^a   Jara, Nery ^a   Espinoza, Francisca ^a   Martínez, Agustín D ^b   Nualart, Francisco ^a  

^a UNIVERSITY OF CONCEPCIÓN   (Chile)

^b UNIVERSIDAD DE VALPARAÍSO   (Chile)

Author keywords

Brain; Ependymal cells; Niche; Progenitor; Stem cells; SVCT2; Vitamin C

Indexed keywords

ASCORBIC ACID; BETA 3 TUBULIN; BETA TUBULIN; BROXURIDINE; GLIAL FIBRILLARY ACIDIC PROTEIN; MESSENGER RNA; SODIUM ASCORBIC ACID COTRANSPORTER; SODIUM ASCORBIC ACID COTRANSPORTER 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYONAL CARCINOMA STEM CELL; GENE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; POSTNATAL DEVELOPMENT; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; ROSTRAL MIGRATORY STREAM; SODIUM ASCORBIC ACID COTRANSPORTER 2 GENE; STEM CELL NICHE; SUBVENTRICULAR ZONE; UPREGULATION;

EID: 84880053515     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2013.00119     Document Type: Article

References (77)

1. Alvarez-Buylla, A., and Garcia-Verdugo, J.M. (2002). Neurogenesis in adult subventricular zone. J Neurosci 22, 629-634.
2. Alvarez-Buylla, A., and Lim, D.A. (2004). For the long run: maintaining germinal niches in the adult brain. Neuron 41, 683-686.
3. Astuya, A., Caprile, T., Castro, M., Salazar, K., Garcia Mde, L., Reinicke, K., Rodriguez, F., Vera, J.C., Millan, C., Ulloa, V., Low, M., Martinez, F., and Nualart, F. (2005). Vitamin C uptake and recycling among normal and tumor cells from the central nervous system. J Neurosci Res 79, 146-156.
4. Beier, D., Hau, P., Proescholdt, M., Lohmeier, A., Wischhusen, J., Oefner, P.J., Aigner, L., Brawanski, A., Bogdahn, U., and Beier, C.P. (2007). CD133(+) and CD133(-) glioblastoma-derived cancer stem cells show differential growth characteristics and molecular profiles. Cancer Res 67, 4010-4015.
5. Bergmann, O., Liebl, J., Bernard, S., Alkass, K., Yeung, M.S., Steier, P., Kutschera, W., Johnson, L., Landén, M., Druid, H., Spalding, K.L., Frisén, J. (2012). The age of olfactory bulb neurons in humans. Neuron 74, 634-639.
6. Bowie, A.G., and O'neill, L.A. (2000). Vitamin C inhibits NF-kappa B activation by TNF via the activation of p38 mitogen-activated protein kinase. J Immunol 165, 7180-7188.
7. Caprile, T., Salazar, K., Astuya, A., Cisternas, P., Silva-Alvarez, C., Montecinos, H., Millan, C., García, M., and Nualart, F. (2009). The Na+-dependent L-ascorbic acid transporter SVCT2 expressed in brainstem cells, neurons, and neuroblastoma cells is inhibited by flavonoids. J Neurochem 108, 563-577.
8. Carcamo, J.M., Pedraza, A., Borquez-Ojeda, O., and Golde, D.W. (2002). Vitamin C suppresses TNF alpha-induced NF kappa B activation by inhibiting I kappa B alpha phosphorylation. Biochemistry 41, 12995-13002.
9. Castro, M., Caprile, T., Astuya, A., Millan, C., Reinicke, K., Vera, J.C., Vasquez, O., Aguayo, L.G., and Nualart, F. (2001). High-affinity sodium-vitamin C co-transporters (SVCT) expression in embryonic mouse neurons. J Neurochem 78, 815-823.
10. Chojnacki, A.K., Mak, G.K., and Weiss, S. (2009). Identity crisis for adult periventricular neural stem cells: subventricular zone astrocytes, ependymal cells or both? Nat Rev Neurosci 10, 153-163.
11. Conover, J.C., and Notti, R.Q. (2008). The neural stem cell niche. Cell Tissue Res 331, 211-224.
12. Daruwala, R., Song, J., Koh, W.S., Rumsey, S.C., and Levine, M. (1999). Cloning and functional characterization of the human sodium-dependent vitamin C transporters hSVCT1 and hSVCT2. FEBS Lett 460, 480-484.
13. Dhara, S.K., and Stice, S.L. (2008). Neural differentiation of human embryonic stem cells. J Cell Biochem 105, 633-640.
14. Doetsch, F., and Alvarez-Buylla, A. (1996). Network of tangential pathways for neuronal migration in adult mammalian brain. Proc Natl Acad Sci U S A 93, 14895-14900.
15. Doetsch, F., Caille, I., Lim, D.A., Garcia-Verdugo, J.M., and Alvarez-Buylla, A. (1999). Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97, 703-716.
16. Doetsch, F., Garcia-Verdugo, J.M., and Alvarez-Buylla, A. (1997). Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci 17, 5046-5061.
17. Eisch, A.J., and Mandyam, C.D. (2007). Adult neurogenesis: can analysis of cell cycle proteins move us "Beyond BrdU"? Curr Pharm Biotechnol 8, 147-165.
18. Esteban, M.A., Wang, T., Qin, B., Yang, J., Qin, D., Cai, J., Li, W., Weng, Z., Chen, J., Ni, S., Chen, K., Li, Y., Liu, X., Xu, J., Zhang, S., Li, F., He, W., Labuda, K., Song, Y., Peterbauer, A., Wolbank, S., Redl, H., Zhong, M., Cai, D., Zeng, L., and Pei, D. (2010). Vitamin C enhances the generation of mouse and human induced pluripotent stem cells. Cell Stem Cell 6, 71-79.
19. Frebel, K., and Wiese, S. (2006). Signalling molecules essential for neuronal survival and differentiation. Biochem Soc Trans 34, 1287-1290.
20. García, M., Salazar, K., Millán, C., Rodríguez, F., Montecinos, H., Caprile, T., Silva, C., Córtes, C., Reinicke, K., Vera, J.C., Aguayo, L.G., Olate, J., Molina, B., and Nualart, F. (2005). Sodium vitamin C cotransporter SVCT2 is expressed in hypothalamic glial cells. Glia 50, 32-47.
21. Gibbons, H.M., and Dragunow, M. (2010). Adult human brain cell culture for neuroscience research. Int J Biochem Cell Biol 42, 844-856.
22. Harrison, F.E., and May, J.M. (2009). Vitamin C function in the brain: vital role of the ascorbate transporter SVCT2. Free Radic Biol Med 46, 719-730.
23. Hartfuss, E., Galli, R., Heins, N., and Gotz, M. (2001). Characterization of CNS precursor subtypes and radial glia. Dev Biol 229, 15-30.
24. Hediger, M.A. (2002). New view at C. Nat Med 8, 445-446.
25. Hemmati, H.D., Nakano, I., Lazareff, J.A., Masterman-Smith, M., Geschwind, D.H., Bronner-Fraser, M., and Kornblum, H.I. (2003). Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci U S A 100, 15178-15183.
26. Horning, M.G., Nowlin, J., Butler, C.M., Lertratanangkoon, K., Sommer, K., and Hill, R.M. (1975). Clinical applications of gas chromatograph/mass spectrometer/computer systems. Clin Chem 21, 1282-1287.
27. Ihrie, R.A., and Alvarez-Buylla, A. (2008). Cells in the astroglial lineage are neural stem cells. Cell Tissue Res 331, 179-191.
28. Johansson, C.B., Svensson, M., Wallstedt, L., Janson, A.M., and Frisen, J. (1999). Neural stem cells in the adult human brain. Exp Cell Res 253, 733-736.
29. Kee, N., Sivalingam, S., Boonstra, R., and Wojtowicz, J.M. (2002). The utility of Ki-67 and BrdU as proliferative markers of adult neurogenesis. J Neurosci Methods 115, 97-105.
30. Kratzing, C.C., Kelly, J.D., and Kratzing, J.E. (1985). Ascorbic acid in fetal rat brain. J Neurochem 44, 1623-1624.
31. Kratzing, C.C., Kelly, J.D., and Oelrichs, B.A. (1982). Ascorbic acid in neural tissues. J Neurochem 39, 625-627.
32. Kriegstein, A., and Alvarez-Buylla, A. (2009). The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci 32, 149-184.
33. Lee, J.Y., Chang, M.Y., Park, C.H., Kim, H.Y., Kim, J.H., Son, H., Lee, Y.S., and Lee, S.H. (2003). Ascorbate-induced differentiation of embryonic cortical precursors into neurons and astrocytes. J Neurosci Res 73, 156-165.
34. Lee, S.H., Lumelsky, N., Studer, L., Auerbach, J.M., and Mckay, R.D. (2000). Efficient generation of midbrain and hindbrain neurons from mouse embryonic stem cells. Nat Biotechnol 18, 675-679.
35. Leprince, P., and Chanas-Sacre, G. (2001). Regulation of radial glia phenotype. Prog Brain Res 132, 13-22.
36. Lim, D.A., Tramontin, A.D., Trevejo, J.M., Herrera, D.G., Garcia-Verdugo, J.M., and Alvarez-Buylla, A. (2000). Noggin antagonizes BMP signaling to create a niche for adult neurogenesis. Neuron 28, 713-726.
37. Lledo, P.M., Merkle, F.T., and Alvarez-Buylla, A. (2008). Origin and function of olfactory bulb interneuron diversity. Trends Neurosci 31, 392-400.
38. Lois, C., and Alvarez-Buylla, A. (1993). Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc Natl Acad Sci U S A 90, 2074-2077.
39. Lois, C., Garcia-Verdugo, J.M., and Alvarez-Buylla, A. (1996). Chain migration of neuronal precursors. Science 271, 978-981.
40. Ma, D.K., Bonaguidi, M.A., Ming, G.L., and Song, H. (2009). Adult neural stem cells in the mammalian central nervous system. Cell Res 19, 672-682.
41. Ma, D.K., Ming, G.L., and Song, H. (2005). Glial influences on neural stem cell development: cellular niches for adult neurogenesis. Curr Opin Neurobiol 15, 514-520.
42. Mcburney, M.W. (1993). P19 embryonal carcinoma cells. Int J Dev Biol 37, 135-140.
43. Merkle, F.T., Mirzadeh, Z., and Alvarez-Buylla, A. (2007). Mosaic organization of neural stem cells in the adult brain. Science 317, 381-384.
44. Milby, K., Oke, A., and Adams, R.N. (1982). Detailed mapping of ascorbate distribution in rat brain. Neurosci Lett 28, 169-174.
45. Mimori, K., Komaki, M., Iwasaki, K., and Ishikawa, I. (2007). Extracellular signal-regulated kinase 1/2 is involved in ascorbic acid-induced osteoblastic differentiation in periodontal ligament cells. J Periodontol 78, 328-334.
46. Mirzadeh, Z., Merkle, F.T., Soriano-Navarro, M., Garcia-Verdugo, J.M., and Alvarez-Buylla, A. (2008). Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. Cell Stem Cell 3, 265-278.
47. Mun, G.H., Kim, M.J., Lee, J.H., Kim, H.J., Chung, Y.H., Chung, Y.B., Kang, J.S., Hwang, Y.I., Oh, S.H., Kim, J.G., Hwang, D.H., Shin, D.H., and Lee, W.J. (2006). Immunohistochemical study of the distribution of sodium-dependent vitamin C transporters in adult rat brain. J Neurosci Res 83, 919-928.
48. Noctor, S.C., Flint, A.C., Weissman, T.A., Wong, W.S., Clinton, B.K., and Kriegstein, A.R. (2002). Dividing precursor cells of the embryonic cortical ventricular zone have morphological and molecular characteristics of radial glia. J Neurosci 22, 3161-3173.
49. Nualart, F., Salazar, K., Oyarce, K., Cisternas, P., Jara, N., Silva-Álvarez, C., Pastor, P., Martínez, F., García, A., García-Robles, M., Tapia, J.C. (2012). Typical and atypical stem cells in the brain, vitamin C effect and neuropathology. Biol Res 45, 243-256.
50. Nunes, M.C., Roy, N.S., Keyoung, H.M., Goodman, R.R., Mckhann, G., 2nd, Jiang, L., Kang, J., Nedergaard, M., and Goldman, S.A. (2003). Identification and isolation of multipotential neural progenitor cells from the subcortical white matter of the adult human brain. Nat Med 9, 439-447.
51. Park, S., Park, C.H., Hahm, E.R., Kim, K., Kimler, B.F., Lee, S.J., Park, H.K., Lee, S.H., Kim, W.S., Jung, C.W., Park, K., Riordan, H.D., and Lee, J.H. (2005). Activation of Raf1 and the ERK pathway in response to l-ascorbic acid in acute myeloid leukemia cells. Cell Signal 17, 111-119.
52. Qiu, S., Li, L., Weeber, E.J., and May, J.M. (2007). Ascorbate transport by primary cultured neurons and its role in neuronal function and protection against excitotoxicity. J Neurosci Res 85, 1046-1056.
53. Quinones-Hinojosa, A., Sanai, N., Soriano-Navarro, M., Gonzalez-Perez, O., Mirzadeh, Z., Gil-Perotin, S., Romero-Rodriguez, R., Berger, M.S., Garcia-Verdugo, J.M., and Alvarez-Buylla, A. (2006). Cellular composition and cytoarchitecture of the adult human subventricular zone: a niche of neural stem cells. J Comp Neurol 494, 415-434.
54. Rajan, D.P., Huang, W., Dutta, B., Devoe, L.D., Leibach, F.H., Ganapathy, V., and Prasad, P.D. (1999). Human placental sodium-dependent vitamin C transporter (SVCT2): molecular cloning and transport function. Biochem Biophys Res Commun 262, 762-768.
55. Reynolds, B.A., and Weiss, S. (1992). Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255, 1707-1710.
56. Reynolds, B.A., and Weiss, S. (1996). Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev Biol 175, 1-13.
57. Roy, N.S., Benraiss, A., Wang, S., Fraser, R.A., Goodman, R., Couldwell, W.T., Nedergaard, M., Kawaguchi, A., Okano, H., and Goldman, S.A. (2000). Promoter-targeted selection and isolation of neural progenitor cells from the adult human ventricular zone. J Neurosci Res 59, 321-331.
58. Sabo, J.K., Kilpatrick, T.J., and Cate, H.S. (2009). Effects of bone morphogenic proteins on neural precursor cells and regulation during central nervous system injury. Neurosignals 17, 255-264.
59. Sanai, N., Tramontin, A.D., Quinones-Hinojosa, A., Barbaro, N.M., Gupta, N., Kunwar, S., Lawton, M.T., Mcdermott, M.W., Parsa, A.T., Manuel-Garcia Verdugo, J., Berger, M.S., and Alvarez-Buylla, A. (2004). Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427, 740-744.
60. Sanai, N., Nguyen, T., Ihrie, R.A., Mirzadeh, Z., Tsai, H.H., Wong, M., Gupta, N., Berger, M.S., Huang, E., Garcia-Verdugo, J.M., Rowitch, D.H., Alvarez-Buylla, A. (2011). Corridors of migrating neurons in the human brain and their decline during infancy. Nature 478, 382-386.
61. Shen, Q., Goderie, S.K., Jin, L., Karanth, N., Sun, Y., Abramova, N., Vincent, P., Pumiglia, K., and Temple, S. (2004). Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 304, 1338-1340.
62. Shen, Q., Wang, Y., Kokovay, E., Lin, G., Chuang, S.M., Goderie, S.K., Roysam, B., and Temple, S. (2008). Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions. Cell Stem Cell 3, 289-300.
63. Shin, D.M., Ahn, J.I., Lee, K.H., and Lee, Y.S. (2004). Ascorbic acid responsive genes during neuronal differentiation of embryonic stem cells. Neuroreport 15, 1959-1963.
64. Silva-Alvarez, C., Carrasco, M., Balmaceda-Aguilera, C., Pastor, P., Garcia Mde, L., Reinicke, K., Aguayo, L., Molina, B., Cifuentes, M., Medina, R., and Nualart, F. (2005). Ependymal cell differentiation and GLUT1 expression is a synchronous process in the ventricular wall. Neurochem Res 30, 1227-1236.
65. Sotiriou, S., Gispert, S., Cheng, J., Wang, Y., Chen, A., Hoogstraten-Miller, S., Miller, G.F., Kwon, O., Levine, M., Guttentag, S.H., and Nussbaum, R.L. (2002). Ascorbic-acid transporter Slc23a1 is essential for vitamin C transport into the brain and for perinatal survival. Nat Med 8, 514-517.
66. Spassky, N., Merkle, F.T., Flames, N., Tramontin, A.D., Garcia-Verdugo, J.M., and Alvarez-Buylla, A. (2005). Adult ependymal cells are postmitotic and are derived from radial glial cells during embryogenesis. J Neurosci 25, 10-18.
67. Spector, R., and Lorenzo, A.V. (1974). Specificity of ascorbic acid transport system of the central nervous system. Am J Physiol 226, 1468-1473.
68. Tavazoie, M., Van Der Veken, L., Silva-Vargas, V., Louissaint, M., Colonna, L., Zaidi, B., Garcia-Verdugo, J.M., and Doetsch, F. (2008). A specialized vascular niche for adult neural stem cells. Cell Stem Cell 3, 279-288.
69. Tramontin, A.D., Garcia-Verdugo, J.M., Lim, D.A., and Alvarez-Buylla, A. (2003). Postnatal development of radial glia and the ventricular zone (VZ): a continuum of the neural stem cell compartment. Cereb Cortex 13, 580-587.
70. Tsukaguchi, H., Tokui, T., Mackenzie, B., Berger, U.V., Chen, X.Z., Wang, Y., Brubaker, R.F., and Hediger, M.A. (1999). A family of mammalian Na+-dependent L-ascorbic acid transporters. Nature 399, 70-75.
71. 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, 74-88.
72. Wang, H., Dutta, B., Huang, W., Devoe, L.D., Leibach, F.H., Ganapathy, V., and Prasad, P.D. (1999). Human Na(+)-dependent vitamin C transporter 1 (hSVCT1): primary structure, functional characteristics and evidence for a non-functional splice variant. Biochim Biophys Acta 1461, 1-9.
73. Wang, T., Chen, K., Zeng, X., Yang, J., Wu, Y., Shi, X., Qin, B., Zeng, L., Esteban, M.A., Pan, G., and Pei, D. (2011). The histone demethylases Jhdm1a/1b enhance somatic cell reprogramming in a vitamin-C-dependent manner. Cell Stem Cell 9, 575-587.
74. Wang, Y., Mackenzie, B., Tsukaguchi, H., Weremowicz, S., Morton, C.C., and Hediger, M.A. (2000). Human vitamin C (L-ascorbic acid) transporter SVCT1. Biochem Biophys Res Commun 267, 488-494.
75. Wu, X., Zeng, L.H., Taniguchi, T., and Xie, Q.M. (2007). Activation of PKA and phosphorylation of sodium-dependent vitamin C transporter 2 by prostaglandin E2 promote osteoblast-like differentiation in MC3T3-E1 cells. Cell Death Differ 14, 1792-1801.
76. Yan, J., Studer, L., and Mckay, R.D. (2001). Ascorbic acid increases the yield of dopaminergic neurons derived from basic fibroblast growth factor expanded mesencephalic precursors. J Neurochem 76, 307-311.
77. Yu, D.H., Lee, K.H., Lee, J.Y., Kim, S., Shin, D.M., Kim, J.H., Lee, Y.S., Oh, S.K., Moon, S.Y., and Lee, S.H. (2004). Changes of gene expression profiles during neuronal differentiation of central nervous system precursors treated with ascorbic acid. J Neurosci Res 78, 29-37.