In vitro neurogenesis from neural progenitor cells isolated from the hippocampus region of the brain of adult rats exposed to ethanol during early development through their alcohol-drinking mothers

Alcohol and Alcoholism

Volumn 44, Issue 2, 2009, Pages 185-198

  Singh, Ashok K ^a   Gupta, Shveta ^a   Jiang, Yin ^a   Younus, Mohammed ^a   Ramzan, Mohammed ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; ALCOHOL; BETA CATENIN; CALCIUM ION; CORTICOTROPIN RELEASING FACTOR; GLUTAMIC ACID; MANNOSE; WNT PROTEIN;

ALCOHOL CONSUMPTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING KINETICS; BRAIN REGION; BREAST FEEDING; CELL CULTURE; CELL DIFFERENTIATION; CELL ISOLATION; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; CULTURE MEDIUM; ENCEPHALE ISOLE; FEMALE; FLUID INTAKE; HIPPOCAMPUS; IN VITRO STUDY; MATERNAL BEHAVIOR; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROTOXICITY; NONHUMAN; PREGNANCY; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SYNAPTOGENESIS; WEANING;

ACETALDEHYDE; ANIMALS; ANTIMETABOLITES; BROMODEOXYURIDINE; CALCIUM SIGNALING; CELL COUNT; CELL DIFFERENTIATION; CELL PROLIFERATION; CENTRAL NERVOUS SYSTEM DEPRESSANTS; CORTICOTROPIN-RELEASING HORMONE; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ETHANOL; FEMALE; FETAL ALCOHOL SYNDROME; HIPPOCAMPUS; NEURONS; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA; STEM CELLS; SYNAPSES; SYNAPSINS; TRANSFECTION;

RATTUS; RODENTIA;

EID: 61449103645     PISSN: 07350414     EISSN: 14643502     Source Type: Journal    
DOI: 10.1093/alcalc/agn109     Document Type: Article

References (101)

1. Andres RH, Ducray AD, Huber AW et al. (2005) Effects of creatine treatment on survival and differentiation of GABA-ergic neurons in cultured striatal tissue. J Neurochem 95:33-45.
2. Bani-Yaghoub M, Tremblay RG, Lei JX et al. (2006) Role of Sox2 in the development of the mouse neocortex. Dev Biol 295:52-66.
3. Baron W, Metz B, Bansal R et al. (2000) PDGF and FGF-2 signaling in oligodendrocyte progenitor cells: Regulation of proliferation and differentiation by multiple intracellular signaling pathways. Mol Neurosci 15:314-29.
4. Behar TN, Li YX, Tran HT et al. (1996) GABA stimulates chemotaxis and chemokinesis of embryonic cortical neurons via calcium-dependent mechanisms. J Neurosci 16:1808-188.
5. Behar TN, Schaffner AE, Scott CA et al. (1998) Differential response of cortical plate and ventricular zone cells to GABA as a migration stimulus. J Neurosci 18:6378-87.
6. Behar TN, Smith SV, Kennedy RT et al. (2001) GABA(B) receptors mediate motility signals for migrating embryonic cortical cells. Cerebral Cortex 11:744-53.
7. Ben-Ari Y, Gaiarsa JL, Tyzio R et al. (2007) GABA: A pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol Rev 87:1215-84.
8. Ben-Ari Y, Khalilov I, Represa A et al. (2004) Interneurons set the tune of developing networks. Trends Neurosci 27:422-7.
9. Berridge MJ. (2007) Inositol trisphosphate and calcium oscillations. Biochem Soc Symp 74:1-7.
10. Berridge M, Lipp P, Bootman M. (1999) Calcium signaling. Curr Biol 9:R157-9.
11. Bhanot P, Fish M, Jemison JA et al. (1999) Frizzled and dfrizzled-2 function as redundant receptors for Wingless during Drosophila embryonic development. Development 126:4175-86.
12. Bonnert TP, Bilsland JB, Guest PC et al. (2006) Molecular characterization of adult mouse subventricular zone progenitor cells during the onset of differentiation. Eur J Neurosci 24 661-75.
13. Bookstein FL, Streissguth AP, Connor PD et al. (2006) Damage to the human cerebellum from prenatal alcohol exposure: The anatomy of a simple biometrical explanation. Anat Record: New Anat 289 195-209.
14. Brunner E, Peter O, Schweizer L et al. (1997) Pangolin encodes a Lef-1 homologue that acts downstream of armadillo to transduce the wingless signal in Drosophila. Nature 385:829-33.
15. Bryja V, Cajanek L, Grahn A et al. (2007) Inhibition of endocytosis blocks Wnt signalling to beta-catenin by promoting dishevelled degradation. Acta Physiol 190:55-61.
16. Cameron HA, McKay RD. (2001) Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 435 406-17.
17. Carpenter MK, Cui X, Hu ZY et al. (1999) In vitro expansion of a multipotent population of human neural progenitor cells. Exp Neurol 158:265-78.
18. Castelo-Branco G, Sousa KM, Bryja V et al. (2006) Ventral mid-brain glia express region-specific transcription factors and regulate dopaminergic neurogenesis through Wnt-5a secretion. Mol Cell Neurosci 31:251-62.
19. Charness ME, Querimit LA, Henteleff M. (1988) Ethanol differentially regulates G proteins in neural cells. Biochem Biophys Res Commun 155:138-43.
20. Chen Y-H, Yang CK, Xia M et al. (2007) Role of GAC63 in transcriptional activation mediated by β-catenin. Nucl Acids Res 35:2084-92.
21. Chou YH, Khuon S, Herrmann H et al. (2003) Nestin promotes the phosphorylation-dependent disassembly of vimentin intermediate filaments during mitosis. Mol Biol Cell 14:1468-78.
22. Christie BR, Cameron HA. (2006) Neurogenesis in the adult hippocampus. Hippocampus 16:199-207.
23. Ciani L, Salinas PC. (2005) WNTs in the vertebrate nervous system: From patterning to neuronal connectivity. Nat Rev Neurosci 6 351-62.
24. Ciapa B, Pesando D, Wilding M et al. (1994) Cell-cycle calcium transients driven by cyclic changes in inositol trisphosphate levels. Nature 368:875-8.
25. Crandall JE, McCarthy DM, Araki KY et al. (2007) Dopamine receptor activation modulates GABA neuron migration from the basal forebrain to the cerebral cortex. J Neurosci 27:3813-22.
26. Crews FT, Mdzinarishvili A, Kim D et al. (2006) Neurogenesis in adolescent brain is potently inhibited by ethanol. Neuroscience 137:437-45.
27. Daniels DL, Weis WI. (2005) Beta-catenin directly displaces Groucho/TLE repressors from Tcf/Lef in Wnt-mediated transcription activation. Nat Str Mol Biol 12:364-71.
28. Dietrichs E. (2007) Brain plasticity after stroke-implications for post-stroke rehabilitation. Tidsskrift Den Norske Laegeforening 127:1228-31.
29. Duchrow M, Schluter C, Key G et al. (1995) Cell proliferation-associated nuclear antigen defined by antibody Ki-67: A new kind of cell cycle-maintaining proteins. Immunol Ther Exp 43:117-21.
30. Elvsashagen T, Malt UF. (2008) Structural plasticity in the adult central nervous system. Tidsskrift Den Norske Laegeforening 128 298-302.
31. Fagotto F, Jho E, Zeng L et al. (1999) Domains of axin involved in protein-protein interactions, Wnt pathway inhibition, and intracellular localization. J Cell Biol 145:741-56.
32. Faure AV, Grunwald D, Moutin MJ et al. (2001) Developmental expression of the calcium release channels during early neurogenesis of the mouse cerebral cortex. Eur J Neurosci 14:1613-22.
33. Flaherty MP, Abdel-Latif A, Li Q et al. (2008) Noncanonical Wnt11 signaling is sufficient to induce cardiomyogenic differentiation in unfractionated bone marrow mononuclear cells Circulation 117 2241-52.
34. Fradkin LG, Garriga G, Salinas PC et al. (2005) Wnt signaling in neural circuit development. J Neurosci 25:10376-8.
35. Galvan V, Bredesen DE. (2007) Neurogenesis in the adult brain: implications for Alzheimer's disease. CNS Neurol Disord Drug Targets 6:303-10.
36. Ge S, Pradhan DA, Ming GL et al. (2007) GABA sets the tempo for activity-dependent adult neurogenesis. Trends Neurosci 30 1-8.
37. Gordon MD, Nusse R. (2006) Wnt signaling: Multiple pathways, multiple receptors, and multiple transcription factors. J Biol Chem 281 22429-33.
38. Haegele L, Ingold B, Naumann H et al. (2003) Wnt signaling inhibits neural differentiation of embryonic stem cells by controlling bone morphogenetic protein expression. Mol Cell Neurosci 24 696-708.
39. Halim ND, Weickert CS, McClintock BW et al. (2003) Presynaptic proteins in the prefrontal cortex of patients with schizophrenia and rats with abnormal prefrontal development. Mol Psychiatry 8 797-810.
40. Hardy KM, Garriock RJ, Yatskievych A et al. (2008) Non-canonical Wnt signaling through Wnt5a/b and a novel Wnt11 gene, Wnt11b, regulates cell migration during avian gastrulation. Dev Biol 320 391-401.
41. Hattiangady B, Shuai B, Cai J et al. (2007) Increased dentate neurogenesis after grafting of glial restricted progenitors or neural stem cells in the aging hippocampus. Stem Cells 25:2104-17.
42. He J, Nixon K, Shetty AK et al. (2005) Chronic alcohol exposure reduces hippocampal neurogenesis and dendritic growth of newborn neurons. Eur J Neurosci 21:2711-20.
43. Hirsch C, Campano LM, Wohrle S et al. (2007) Canonical Wnt signaling transiently stimulates proliferation and enhances neurogenesis in neonatal neural progenitor cultures. Exp Cell Res 313 572-87.
44. Hu, M., Kurobe, M., Jeong, Y.J. et al. (2007) Wnt/beta-catenin signaling in murine hepatic transit amplifying progenitor cells. Gastroenterology 133:1579-91.
45. Huang EJ, Reichardt LF. (2001) Neurotrophins: Roles in neuronal development and function. Annu Rev Neurosci 24:677-736.
46. Huelsken J, Behrens J. (2002) The Wnt signalling pathway. J Cell Sci 115:3977-8.
47. Huelsken J, Birchmeier W. (2001) New aspects of Wnt signaling pathways in higher vertebrates. Curr Opin Genet Dev 11:547-53.
48. Ieraci A, Herrera DG. (2007) Single alcohol exposure in early life damages hippocampal stem/progenitor cells and reduces adult neurogenesis. Neurobiol Dis 26:597-605.
49. Janak PH, Wolf FW, Heberlein U et al. (2006) BIG news in alcohol addiction: New findings on growth factor pathways BDNF, insulin, and GDNF. Alcohol Clin Exp Res 30:214-21.
50. Jessberger S, Kempermann G. (2003) Adult-born hippocampal neurons mature into activity-dependent responsiveness. Eur J Neurosci 18 2707-12.
51. Joe KH, Kim YK, Kim TS et al. (2007) Decreased plasma brain-derived neurotrophic factor levels in patients with alcohol dependence. Alcohol Clin Exp Res 31:1833-8.
52. Kaneko Y, Sakakibara S, Imai T et al. (2000) Musashi1: An evolutionally conserved marker for CNS progenitor cells including neural stem cells. Dev Neurosci 22:139-53.
53. Kao H-T, Li P, Chao HM et al. (2008) Early involvement of synapsin III in neural progenitor cell development in the adult hippocampus. J Comp Neurol 507:1860-70.
54. Katoh M, Katoh M. (2006) Cross-talk of WNT and FGF signaling pathways at GSK3beta to regulate beta-catenin and SNAIL signaling cascades. Cancer Biol Ther 5:1059-64.
55. Kempermann G, Gage FH. (1998) Closer to neurogenesis in adult humans. Nat Med 4:555-7.
56. Kempermann G, Gast D, Kronenberg G et al. (2003) Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development 130:391-9.
57. Kempermann G, Kuhn HG, Gage FH. (1997) Genetic influence on neurogenesis in the dentate gyrus of adult mice. Proc Natl Acad Sci USA 94 10409-14.
58. Kempermann G, Wiskott L, Gage FH. (2004) Functional significance of adult neurogenesis. Curr Opin Neurobiol 14:186-91.
59. Kim W-K, Hawthorn M, Rabin R. (1993) Differential effects of chronic ethanol exposure on ATP- and bradykinin-induced increases in intracellular calcium levels in PC12 cells. Mol Pharmacol 44 405-11.
60. Klempin F, Kempermann G. (2007) Adult hippocampal neurogenesis and aging. Eur Arch Psychiatry Clin Neurosci 257:271-80.
61. Klintsova AY, Helfer JL, Calizo LH et al. (2007) Persistent impairment of hippocampal neurogenesis in young adult rats following early postnatal alcohol exposure. Alcohol Clin Exp Res 31 2073-82.
62. Komuro H, Rakic P. (1996) Selective role of N-type calcium channels in neuronal migration. Science 257:806-8.
63. Korinek V, Barker N, Willert K et al. (1998) Two members of the Tcf family implicated in Wnt/beta-catenin signaling during embryogenesis in the mouse. Mol Cell Biol 18:1248-56.
64. Koyanagi M, Haendeler J, Badorff C et al. (2005) Non-canonical Wnt signaling enhances differentiation of human circulating progenitor cells. J Biol Chem 280:16838-42.
65. Kriegstein AR, Owens DF. (2001) GABA may act as a self-limiting trophic factor at developing synapses. Sci STKE 95:PE1.
66. Kuhn HG, Cooper-Kuhn CM, Boekhoorn A et al. (2007) Changes in neurogenesis in dementia and Alzheimer mouse models: Are they functionally relevant? Eur Arch Psych Clin Neurosci 257: 281-9.
67. Kurtz A, Zimmer A, Schnutgen F et al. (1994) The expression pattern of a novel gene encoding brain-fatty acid binding protein correlates with neuronal and glial cell development. Development 120:2637-49.
68. Leclerc C, Neant I, Webb SE et al. (2006) Calcium transients and calcium signalling during early neurogenesis in the amphibian embryo Xenopus laevis. Biochim Biophys Acta 1763:1184-91.
69. Lee JE, Wu SF, Goering LM et al. (2006) Canonical Wnt signaling through Lef1 is required for hypothalamic neurogenesis. Development 133:4451-61.
70. Levine GH, Maglio JJ, Horwitz J. (2000) Differential effects of ethanol on signal transduction. Alcohol Clin Exp Res 24:93-101.
71. Maccioni RB, Munoz JP, Barbeito L. (2001) The molecular bases of Alzheimer's disease and other neurodegenerative disorders. Arch Med Res 32:367-81.
72. Machon O, Backman M, Machonova O et al. (2007) A dynamic gradient of Wnt signaling controls initiation of neurogenesis in the mammalian cortex and cellular specification in the hippocampus. Dev Biol 311:223-37.
73. Malaterre J, Ramsay RG, Mantamadiotis T. (2007) Wnt-Frizzled signalling and the many paths to neural development and adult brain homeostasis. Front Biosci 12:492-506.
74. Marzesco AM, Janich P, Wilsch-Brauninger M et al. (2005) Release of extracellular membrane particles carrying the stem cell marker prominin-1 (CD133) from neural progenitors and other epithelial cells. J Cell Sci 118:2849-58.
75. Nakayama T, Momoki-Soga T, Inoue N. (2003) Astrocyte-derived factors instruct differentiation of embryonic stem cells into neurons. Neurosci Res 46:241-9.
76. Nixon K. (2006) Alcohol and adult neurogenesis: Roles in neurodegeneration and recovery in chronic alcoholism. Hippocampus 16:287-95.
77. Ostenfeld T, Svendsen CN. (2004) Requirement for neurogenesis to proceed through the division of neuronal progenitors following differentiation of epidermal growth factor and fibroblast growth factor-2 - responsive human neural stem cells. Stem Cell 22:798-811.
78. Ouko L, Ziegler TR, Gu LH et al. (2004) Wnt11 signaling promotes proliferation, transformation, and migration of IEC6 intestinal epithelial cells. J Biol Chem 279:26707-15.
79. Owens DF, Kriegstein AR. (2002) Is there more to GABA than synaptic inhibition? Nat Rev Neurosci 3:715-27.
80. Park CH, Kang JS, Kim JS et al. (2006a) Differential actions of the proneural genes encoding Mash1 and neurogenins in Nurr1-induced dopamine neuron differentiation. J Cell Sci 119:2310-20.
81. Park CH, Kang JS, Shin YH et al. (2006b) Acquisition of in vitro and in vivo functionality of Nurr1-induced dopamine neurons. FASEB J 20:2553-5.
82. Pittenger C, Duman RS. (2008) Stress, depression, and neuroplasticity: A convergence of mechanisms. Neuropsychopharmacology 33:88-109.
83. Roivainen R, Hundle B, Messing RO. (1994) Protein kinase C and adaptation to ethanol. EXS 71:29-38.
84. Roivainen R, Hundle B, Messing RO. (1995) Ethanol enhances growth factor activation of MAP kinases by a protein kinase C-dependent mechanism. Proc Natl Acad Sci USA 92:1891-5.
85. Sakurada K, Ohshima-Sakurada M, Palmer TD et al. (1999) Nurr1, an orphan nuclear receptor, is a transcriptional activator of endogenous tyrosine hydroxylase in neural progenitor cells derived from the adult brain. Development 126:4017-26.
86. Sheng M, Hoogenraad CC. (2007) The postsynaptic architecture of excitatory synapses: A more quantitative view. Annu Rev Biochem 76:823-47.
87. Sheng M, Kim MJ. (2002) Postsynaptic signaling and plasticity mechanisms. Science 298:776-80
88. Shim JW, Park CH, Bae YC et al. (2007) Generation of functional dopamine neurons from neural precursor cells isolated from the subventricular zone and white matter of the adult rat brain using Nurr1 overexpression. Stem Cells 25:1252-62.
89. Silberman Y, Shi L, Brunso-Bechtold D et al. (2008) Distinct mechanisms of ethanol potentiation of local and paracapsular GABAergic synapses in the rat basolateral amygdala. J Pharma Exp Ther 324 251-60
90. Silberman Y, Ariwodola OJ, Rawley M et al. (2005) Intracellular chloride may influence ethanol potentiation of GABAergic synapses in the rat hippocampus. Alcohol Clin Exp Res 29:56A.
91. Singh AK. (2002) Acute effects of acephate and methamidophos and interleukin-1 on corticotropin-releasing factor (CRF) synthesis in and release from the hypothalamus in vitro. Comp Biochem Physiol Toxicol Pharmacol 132:9-24.
92. Singh AK, Jiang Y. (2004) Lipopolysaccharide (LPS) induced activation of the immune system in control rats and rats chronically exposed to a low-level of the organophosphate insecticide, acephate. Toxicol Intustr Health 19:93-108.
93. Singh AK, Jiang Y, Benlhabib E et al. (2007) Herbal mixtures consisting of puerarin and either polyenylphosphatidylcholine or curcumin provide comprehensive protection against alcohol-related disorders in P rats receiving free choice water and 15% ethanol in pure water. J Med Food 10:526-42.
94. Toni N, Teng EM, Bushong EA et al. (2007) Synapse formation on neurons born in the adult hippocampus. Nat Neurosci 10 727-34.
95. Uchida N, Buck DW, He D et al. (2000) Direct isolation of human central nervous system stem cells. Proc Natl Acad Sci USA 97 14720-5.
96. van Praag H, Schinder AF, Christie BR et al. (2002) Functional neurogenesis in the adult hippocampus. Nature 415:1030-4.
97. 2+, and cyclic GMP: visualizing Frizzled functions. Science 300:1529-30.
98. Wang TW, Stromberg GP, Whitney JT. et al. (2006) Sox3 expression identifies neural progenitors in persistent neonatal and adult mouse forebrain germinative zones. J Comp Neurol 497:88-100.
99. Weissman TA, Riquelme PA, Ivic L et al. (2004) Calcium waves propagate through radial glial cells and modulate proliferation in the developing neocortex. Neuron 43:647-61.
100. Zhang Q, Major MB, Takanashi S et al. (2007) Small-molecule synergist of the Wnt/beta-catenin signaling pathway. Proc Natl Acad Sci U S A 104:7444-8. Erratum: Proc Natl Acad Sci U S A 2007; 104:12581.
101. Zhu PJ, Lovinger DM. (2006) Ethanol potentiates GABAergic synaptic transmission in a postsynaptic neuron/synaptic bouton preparation from basolateral amygdala. J Neurophysiol 96:433-41.