The downregulation of Wnt/β-catenin signaling pathway is associated with zinc deficiency-induced proliferative deficit of C17.2 neural stem cells

Brain Research

Volumn 1615, Issue , 2015, Pages 61-70

  Zhao, Jianya ^a   Han, Jingling ^a   Jiang, Junkang ^a   Shi, Shangshi ^a   Ma, Xia ^a   Liu, Xinhang ^a   Wang, Cheng ^a   Nie, Xiaoke ^a   He, Yunhua ^b   Jiang, Shengyang ^a   Wan, Chunhua ^a  

^a NANTONG UNIVERSITY   (China)

^b NANTONG MEDICAL COLLEGE   (China)

Author keywords

C17.2 cells; Neural stem cell proliferation; Wnt catenin signaling; Zinc deficiency

Indexed keywords

BETA CATENIN; CELL CYCLE PROTEIN; CYCLIN D1; WNT PROTEIN; ETHYLENEDIAMINE DERIVATIVE; N,N,N',N'-TETRAKIS(2-PYRIDYLMETHYL)ETHYLENEDIAMINE; ZINC;

APOPTOSIS; ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE PROGRESSION; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; FLOW CYTOMETRY; NEURAL STEM CELL; ONCOGENE C MYC; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; WNT SIGNALING PATHWAY; ZINC DEFICIENCY; ANIMAL; CELL CULTURE; CELL SURVIVAL; DEFICIENCY; DRUG EFFECTS; METABOLISM; MOUSE; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; BETA CATENIN; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; DOWN-REGULATION; ETHYLENEDIAMINES; MICE; NEURAL STEM CELLS; SIGNAL TRANSDUCTION; WNT SIGNALING PATHWAY; ZINC;

EID: 84928911124     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2015.04.028     Document Type: Article

References (56)

1. K. Adachi, Z. Mirzadeh, M. Sakaguchi, T. Yamashita, T. Nikolcheva, Y. Gotoh, G. Peltz, L. Gong, T. Kawase, A. Alvarez-Buylla, H. Okano, and K. Sawamoto Beta-catenin signaling promotes proliferation of progenitor cells in the adult mouse subventricular zone Stem Cells 25 2007 2827 2836
2. S. Akhondzadeh, M.R. Mohammadi, and M. Khademi Zinc sulfate as an adjunct to methylphenidate for the treatment of attention deficit hyperactivity disorder in children: a double blind and randomized trial [ISRCTN64132371] BMC Psychiatry 4 2004 9
3. M. Almeida, L. Han, M. Martin-Millan, C.A. O'Brien, and S.C. Manolagas Oxidative stress antagonizes Wnt signaling in osteoblast precursors by diverting beta-catenin from T cell factor- to forkhead box O-mediated transcription J. Biol. Chem. 282 2007 27298 27305
4. G. Ambrosini, C. Adida, and D.C. Altieri A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma Nat. Med. 3 1997 917 921
5. D. Beyersmann, and H. Haase Functions of zinc in signaling, proliferation and differentiation of mammalian cells Biometals 14 2001 331 341
6. S. Boku, S. Nakagawa, T. Masuda, H. Nishikawa, A. Kato, Y. Kitaichi, T. Inoue, and T. Koyama Glucocorticoids and lithium reciprocally regulate the proliferation of adult dentate gyrus-derived neural precursor cells through GSK-3beta and beta-catenin/TCF pathway Neuropsychopharmacology 34 2009 805 815
7. D.F. Caldwell, D. Oberleas, J.J. Clancy, and A.S. Prasad Behavioral impairment in adult rats following acute zinc deficiency Proc. Soc. Exp. Biol. Med. 133 1970 1417 1421
8. B.Y. Chen, X. Wang, Z.Y. Wang, Y.Z. Wang, L.W. Chen, and Z.J. Luo Brain-derived neurotrophic factor stimulates proliferation and differentiation of neural stem cells, possibly by triggering the Wnt/beta-catenin signaling pathway J. Neurosci. Res. 91 2013 30 41
9. A. Chenn, and C.A. Walsh Regulation of cerebral cortical size by control of cell cycle exit in neural precursors Science 297 2002 365 369
10. W. Chowanadisai, S.L. Kelleher, and B. Lonnerdal Maternal zinc deficiency reduces NMDA receptor expression in neonatal rat brain, which persists into early adulthood J. Neurochem. 94 2005 510 519
11. H. Clevers Wnt/beta-catenin signaling in development and disease Cell 127 2006 469 480
12. H. Clevers, and R. Nusse Wnt/beta-catenin signaling and disease Cell 149 2012 1192 1205
13. R.S. Corniola, N.M. Tassabehji, J. Hare, G. Sharma, and C.W. Levenson Zinc deficiency impairs neuronal precursor cell proliferation and induces apoptosis via p53-mediated mechanisms Brain Res. 1237 2008 52 61
14. W. Deng, J.B. Aimone, and F.H. Gage New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nat. Rev. Neurosci. 11 2010 339 350
15. M.A. Essers, L.M. de Vries-Smits, N. Barker, P.E. Polderman, B.M. Burgering, and H.C. Korswagen Functional interaction between beta-catenin and FOXO in oxidative stress signaling Science 308 2005 1181 1184
16. S. Frame, and P. Cohen GSK3 takes centre stage more than 20 years after its discovery Biochem. J. 359 2001 1 16
17. C.J. Frederickson, and D.W. Moncrieff Zinc-containing neurons Biol. Signals 3 1994 127 139
18. C.J. Frederickson, J.Y. Koh, and A.I. Bush The neurobiology of zinc in health and disease Nat. Rev. Neurosci. 6 2005 449 462
19. H.L. Gao, H. Xu, N. Xin, W. Zheng, Z.H. Chi, and Z.Y. Wang Disruption of the CaMKII/CREB signaling is associated with zinc deficiency-induced learning and memory impairments Neurotox. Res. 19 2011 584 591
20. S. Gogia, and H.S. Sachdev Zinc supplementation for mental and motor development in children Cochrane Database Syst. Rev. 12 2012 CD007991
21. M.S. Golub, C.L. Keen, M.E. Gershwin, and A.G. Hendrickx Developmental zinc deficiency and behavior J. Nutr. 125 1995 2263S 2271S
22. S.D. Gower-Winter, R.S. Corniola, T.J. Morgan Jr., and C.W. Levenson Zinc deficiency regulates hippocampal gene expression and impairs neuronal differentiation Nutr. Neurosci. 16 2013 174 182
23. E.S. Halas, M.J. Eberhardt, M.A. Diers, and H.H. Sandstead Learning and memory impairment in adult rats due to severe zinc deficiency during lactation Physiol. Behav. 30 1983 371 381
24. E.S. Halas, C.D. Hunt, and M.J. Eberhardt Learning and memory disabilities in young adult rats from mildly zinc deficient dams Physiol. Behav. 37 1986 451 458
25. M. Hambidge Human zinc deficiency J. Nutr. 130 2000 1344S 1349SS
26. E. Ho, C. Courtemanche, and B.N. Ames Zinc deficiency induces oxidative DNA damage and increases p53 expression in human lung fibroblasts J. Nutr. 133 2003 2543 2548
27. N.C. Inestrosa, and E. Arenas Emerging roles of Wnts in the adult nervous system Nat. Rev. Neurosci. 11 2010 77 86
28. N. Israsena, M. Hu, W. Fu, L. Kan, and J.A. Kessler The presence of FGF2 signaling determines whether beta-catenin exerts effects on proliferation or neuronal differentiation of neural stem cells Dev. Biol. 268 2004 220 231
29. M.D. Kaytor, and H.T. Orr The GSK3 beta signaling cascade and neurodegenerative disease Curr. Opin. Neurobiol. 12 2002 275 278
30. N. Lehwald, G.Z. Tao, K.Y. Jang, I. Papandreou, B. Liu, M.A. Pysz, J.K. Willmann, W.T. Knoefel, N.C. Denko, and K.G. Sylvester Beta-catenin regulates hepatic mitochondrial function and energy balance in mice Gastroenterology 143 2012 754 764
31. D.C. Lie, S.A. Colamarino, H.J. Song, L. Desire, H. Mira, A. Consiglio, E.S. Lein, S. Jessberger, H. Lansford, A.R. Dearie, and F.H. Gage Wnt signalling regulates adult hippocampal neurogenesis Nature 437 2005 1370 1375
32. M.C. Limon-Mortes, M. Mora-Santos, A. Espina, J.A. Pintor-Toro, A. Lopez-Roman, M. Tortolero, and F. Romero UV-induced degradation of securin is mediated by SKP1-CUL1-beta TrCP E3 ubiquitin ligase J. Cell Sci. 121 2008 1825 1831
33. C.L. Lin, J.Y. Wang, Y.T. Huang, Y.H. Kuo, K. Surendran, and F.S. Wang Wnt/beta-catenin signaling modulates survival of high glucose-stressed mesangial cells J. Am. Soc. Nephrol. 17 2006 2812 2820
34. B.T. MacDonald, K. Tamai, and X. He Wnt/beta-catenin signaling: components, mechanisms, and diseases Dev. Cell. 17 2009 9 26
35. R.T. Moon, A.D. Kohn, G.V. De Ferrari, and A. Kaykas WNT and beta-catenin signalling: diseases and therapies Nat. Rev. Genet. 5 2004 691 701
36. Y. Pei, S.N. Brun, S.L. Markant, W. Lento, P. Gibson, M.M. Taketo, M. Giovannini, R.J. Gilbertson, and R.J. Wechsler-Reya WNT signaling increases proliferation and impairs differentiation of stem cells in the developing cerebellum Development 139 2012 1724 1733
37. A.S. Prasad Zinc deficiency in women, infants and children J. Am. Coll. Nutr. 15 1996 113 120
38. A.S. Prasad Recognition of zinc-deficiency syndrome Nutrition 17 2001 67 69
39. Q. Qu, G. Sun, W. Li, S. Yang, P. Ye, C. Zhao, R.T. Yu, F.H. Gage, R.M. Evans, and Y. Shi Orphan nuclear receptor TLX activates Wnt/beta-catenin signalling to stimulate neural stem cell proliferation and self-renewal Nat. Cell Biol. 12 31-40 2010 1 9 Suppl
40. H. Schonheyder, S. Hoffmann, H.E. Jensen, B.F. Hansen, and M.B. Franzmann Aspergillus fumigatus fungaemia and myocarditis in a patient with acquired immunodeficiency syndrome 100 1992 605 608 APMIS 100 1992 605 608
41. D.R. Seib, N.S. Corsini, K. Ellwanger, C. Plaas, A. Mateos, C. Pitzer, C. Niehrs, T. Celikel, and A. Martin-Villalba Loss of Dickkopf-1 restores neurogenesis in old age and counteracts cognitive decline Cell Stem Cell 12 2013 204 214
42. Y. Shi, G. Sun, C. Zhao, and R. Stewart Neural stem cell self-renewal Crit. Rev. Oncol. Hematol. 65 2008 43 53
43. T. Shimizu, T. Kagawa, T. Inoue, A. Nonaka, S. Takada, H. Aburatani, and T. Taga Stabilized beta-catenin functions through TCF/LEF proteins and the Notch/RBP-Jkappa complex to promote proliferation and suppress differentiation of neural precursor cells Mol. Cell Biol. 28 2008 7427 7441
44. S.Y. Shin, C.G. Kim, E.H. Jho, M.S. Rho, Y.S. Kim, Y.H. Kim, and Y.H. Lee Hydrogen peroxide negatively modulates Wnt signaling through downregulation of beta-catenin Cancer Lett. 212 2004 225 231
45. Y. Song, S.W. Leonard, M.G. Traber, and E. Ho Zinc deficiency affects DNA damage, oxidative stress, antioxidant defenses, and DNA repair in rats J. Nutr. 139 2009 1626 1631
46. S.W. Suh, S.J. Won, A.M. Hamby, B.H. Yoo, Y. Fan, C.T. Sheline, H. Tamano, A. Takeda, and J. Liu Decreased brain zinc availability reduces hippocampal neurogenesis in mice and rats J. Cereb. Blood Flow Metab. 29 2009 1579 1588
47. A. Swain, V. Soutter, R. Loblay, and A.S. Truswell Salicylates, oligoantigenic diets, and behaviour Lancet 2 1985 41 42
48. A. Takeda, K. Yamada, A. Minami, T. Nagano, and N. Oku Enhanced excitability of hippocampal mossy fibers and CA3 neurons under dietary zinc deficiency Epilepsy Res. 63 2005 77 84
49. P. Toren, S. Eldar, B.A. Sela, L. Wolmer, R. Weitz, D. Inbar, S. Koren, A. Reiss, R. Weizman, and N. Laor Zinc deficiency in attention-deficit hyperactivity disorder Biol. Psychiatry 40 1996 1308 1310
50. H.L. Wang, J. Wang, S.Y. Xiao, R. Haydon, D. Stoiber, T.C. He, M. Bissonnette, and J. Hart Elevated protein expression of cyclin D1 and Fra-1 but decreased expression of c-Myc in human colorectal adenocarcinomas overexpressing beta-catenin Int. J. Cancer 101 2002 301 310
51. K. Willert, and K.A. Jones Wnt signaling: is the party in the nucleus? Genes Dev. 20 2006 1394 1404
52. G.J. Woodhead, C.A. Mutch, E.C. Olson, and A. Chenn Cell-autonomous beta-catenin signaling regulates cortical precursor proliferation J. Neurosci. 26 2006 12620 12630
53. M.V. Wu, and R. Hen The young and the restless: regulation of adult neurogenesis by Wnt signaling Cell Stem Cell 12 2013 139 140
54. D.Y. Zhang, H.J. Wang, and Y.Z. Tan Wnt/beta-catenin signaling induces the aging of mesenchymal stem cells through the DNA damage response and the p53/p21 pathway PLoS One 6 2011 e21397
55. D.Y. Zhang, Y. Pan, C. Zhang, B.X. Yan, S.S. Yu, D.L. Wu, M.M. Shi, K. Shi, X.X. Cai, S.S. Zhou, J.B. Wang, J.P. Pan, and L.H. Zhang Wnt/beta-catenin signaling induces the aging of mesenchymal stem cells through promoting the ROS production Mol. Cell Biochem. 374 2013 13 20
56. F. Zhang, C.J. Phiel, L. Spece, N. Gurvich, and P.S. Klein Inhibitory phosphorylation of glycogen synthase kinase-3 (GSK-3) in response to lithium. Evidence for autoregulation of GSK-3 J. Biol. Chem. 278 2003 33067 33077