Ethanol exposure during neurogenesis induces persistent effects on neural maturation: Evidence from an ex vivo model of fetal cerebral cortical neuroepithelial progenitor maturation

Gene Expression

Volumn 14, Issue 3, 2007, Pages 159-171

  Camarillo, Cynthia ^a   Miranda, Rajesh C ^a,b  

^a TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

Author keywords

CDC42; Dynein light chain; Fetal alcohol syndrome; Gap43; LC8 type 1 (DYNLL1); Migration; Neural stem cells; Paxillin; RhoA

Indexed keywords

ALCOHOL; DYNEIN ADENOSINE TRIPHOSPHATASE; DYNEIN LIGHT CHAIN; LC8 PROTEIN 1; MESSENGER RNA; NEUROMODULIN; PAXILLIN; PROTEIN CDC42; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN MATURATION; CELL MATURATION; CELL PROLIFERATION; EX VIVO STUDY; FETAL ALCOHOL SYNDROME; FETUS; INCIDENCE; MOUSE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEUROEPITHELIUM; NONHUMAN; NUCLEOTIDE SEQUENCE; PRENATAL EXPOSURE;

ANIMALS; CELL DIFFERENTIATION; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM DEPRESSANTS; CEREBRAL CORTEX; ETHANOL; FEMALE; FETAL ALCOHOL SYNDROME; FETUS; GENE EXPRESSION REGULATION; HUMANS; MICE; NEUROEPITHELIAL CELLS; PREGNANCY; RANDOM ALLOCATION; STEM CELLS; TERATOGENS;

EID: 46949107358     PISSN: 10522166     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (50)

1. Anthony, T. E.; Klein, C.; Fishell, G.; Heintz, N. Radial glia serve as neuronal progenitors in all regions of the central nervous system. Neuron 41:881-890; 2004.
2. Azuma, K.; Tanaka, M.; Uekita, T.; Inoue, S.; Yokota, J.; Ouchi, Y.; Sakai, R. Tyrosine phosphorylation of paxillin affects the metastatic potential of human osteosarcoma. Oncogene 24:4754-4764; 2005.
3. Bonthius, D. J.; McKim, R. A.; Koele, L.; Harb, H.; Kehrberg, A. H.; Mahoney, J.; Karacay, B.; Pantazis, N. J. Severe alcohol-induced neuronal deficits in the hippocampus and neocortex of neonatal mice genetically deficient for neuronal nitric oxide synthase (nNOS). J. Comp. Neurol. 499:290-305; 2006.
4. Bonthius, D. J.; Tzouras, G.; Karacay, B.; Mahoney, J.; Hutton, A.; McKim, R.; Pantazis, N. J. Deficiency of neuronal nitric oxide synthase (nNOS) worsens alcohol-induced microencephaly and neuronal loss in developing mice. Brain Res. Dev. Brain Res. 138:45-59; 2002.
5. Bonthius, D. J.; West, J. R. Alcohol-induced neuronal loss in developing rats: Increased brain damage with binge exposure. Alcohol Clin. Exp. Res. 14:107-118; 1990.
6. Camarillo, C.; Kumar, L. S.; Bake, S.; Sohrabji, F.; Miranda, R. C. Ethanol regulates angiogenic cytokines during neural development: Evidence from an in vitro model of mitogen-withdrawal-induced cerebral cortical neuroepithelial differentiation. Alcohol Clin. Exp. Res. 31:324-335; 2007.
7. Caviness, Jr., V. S. Neocortical histogenesis in normal and reeler mice: A developmental study based upon [3H]thymidine autoradiography. Brain Res. 256:293-302; 1982.
8. Cheema, Z. F.; West, J. R.; Miranda, R. C. Ethanol induces Fas/Apo (apoptosis)-l mRNA and cell suicide in the developing cerebral cortex. Alcohol Clin. Exp. Res. 24:535-543; 2000.
9. Clarren, S. K. Neuropathology in fetal alcohol syndrome. In: West, J. R. (Ed.), Alcohol and brain development. New York: Oxford University Press; 1986: 158-166.
10. Dohrman, D. P.; West, J. R.; Pantazis, N. J. Ethanol reduces expression of the nerve growth factor receptor, but not nerve growth factor protein levels in the neonatal rat cerebellum. Alcohol Clin. Exp. Res. 21:882-893; 1997.
11. Ever, L.; Gaiano, N. Radial 'glial' progenitors: Neurogenesis and signaling. Curr. Opin. Neurobiol. 15:29-33; 2005.
12. Gary, D. S.; Mattson, M. P. Integrin signaling via the PI3-kinase-Akt pathway increases neuronal resistance to glutamate-induced apoptosis. J. Neurochem. 76: 1485-1496; 2001.
13. Goodlett, C. R.; Marcussen, B. L.; West, J. R. A single day of alcohol exposure during the brain growth spurt induces brain weight restriction and cerebellar Purkinje cell loss. Alcohol 7:107-114; 1990.
14. Hamre, K. M.; West, J. R. The effects of the timing of ethanol exposure during the brain growth spurt on the number of cerebellar Purkinje and granule cell nuclear profiles. Alcohol Clin. Exp. Res. 17:610-622; 1993.
15. Huang, C.; Borchers, C. H.; Schaller, M. D.; Jacobson, K. Phosphorylation of paxillin by p38MAPK is involved in the neurite extension of PC-12 cells. J. Cell Biol. 164:593-602; 2004.
16. Huang, C.; Jacobson, K.; Schaller, M. D. A role for JNK-paxillin signaling in cell migration. Cell Cycle 3: 4-6; 2004.
17. Jaffrey, S. R.; Snyder, S. H. PIN: An associated protein inhibitor of neuronal nitric oxide synthase. Science 274:774-777; 1996.
18. Lindsley, T. A.; Kerlin, A. M.; Rising, L. J. Time-lapse analysis of ethanol's effects on axon growth in vitro. Brain Res. Dev. Brain Res. 147:191-199; 2003.
19. Livy, D.; Miller, K.; Maier, S. E.; West, J. Fetal alcohol exposure and temporal vulnerability: Effects of binge-like alcohol exposure on the developing rat hippocampus. Neurotoxicol. Teratol. 25:447-458; 2003.
20. Loock, C.; Conry, J.; Cook, J. L.; Chudley, A. E.; Rosales, T. Identifying fetal alcohol spectrum disorder in primary care. CMAJ 172:628-630; 2005.
21. Luo, J.; Miller, M. W. Growth factor-mediated neural proliferation: Target of ethanol toxicity. Brain Res. Rev. 27:157-167; 1998.
22. Luo, J.; West, J. R.; Pantazis, N. J. Ethanol exposure reduces the density of the low-affinity nerve growth factor receptor (p75) on pheochromocytoma (PC12) cells. Brain Res. 737:34-44; 1996.
23. Maier, S. E.; Cramer, J. A.; West, J. R.; Sohrabji, F. Alcohol exposure during the first two trimesters equivalent alters granule cell number and neurotrophin expression in the developing rat olfactory bulb. J. Neurobiol. 41:414-423; 1999.
24. Mani, S.; Shen, Y.; Schaefer, J.; Meiri, K. F. Failure to express GAP-43 during neurogenesis affects cell cycle regulation and differentiation of neural precursors and stimulates apoptosis of neurons. Mol. Cell. Neurosci. 17:54-66; 2001.
25. McAlhaney, R. E. J.; Miranda, R. C.; Finnell, R. H.; West, J. R. Ethanol decreases glial-derived neurotrophic factor (GDNF) protein release but not mRNA expression and increases GDNF-stimulated She phosphorylation in the developing cerebellum. Alcohol Clin. Exp. Res. 23:1691-1697; 1999.
26. McAlhany, R. E. J.; West, J. R.; Miranda, R. C. Glial-derived neurotrophic factor (GDNF) prevents ethanol-induced apoptosis and JUN kinase phosphorylation. Dev. Brain Res. 119:209-216; 2000.
27. Miller, M.; Jacobs, J.; Yokoyama, R. Neg, a nerve growth factor-stimulated gene expressed by fetal neocortical neurons that is downregulated by ethanol. J. Comp. Neurol. 460:212-222; 2003.
28. Miller, M. W. Migration of cortical neurons is altered by gestational exposure to ethanol. Alcohol Clin. Exp. Res. 17:304-314; 1993.
29. Mooney, S. M.; Miller, M. W. Effects of prenatal exposure to ethanol on the expression of bcl-2, bax and caspase 3 in the developing rat cerebral cortex and thalamus. Brain Res. 911:71-81; 2001.
30. Mooney, S. M.; Miller, M. W. Ethanol-induced neuronal death in organotypic cultures of rat cerebral cortex. Brain Res. Dev. Brain Res. 147:135-141; 2003.
31. Noctor, S. C.; Martinez-Cerdeno, V.; Ivic, L.; Kriegstein, A. R. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat. Neurosci. 7:136-144; 2004.
32. Pantazis, N. J.; West, J. R.; Dai, D. The nitric oxide-cyclic GMP pathway plays an essential role in both promoting cell survival of cerebellar granule cells in culture and protecting the cells against ethanol neurotoxicity. J. Neurochem. 70:1826-1838; 1998.
33. Pfaffl, M. W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45; 2001.
34. Polikandriotis, J. A.; Rupnow, H. L.; Hart, C. M. Chronic ethanol exposure stimulates endothelial cell nitric oxide production through PI-3 kinase-and hsp90-dependent mechanisms. Alcohol Clin. Exp. Res. 29: 1932-1938; 2005.
35. Prock, T. L.; Miranda, R. C. Embryonic cerebral cortical progenitors are resistant to apoptosis, but increase expression of suicide receptor DISC-complex genes and suppress autophagy following ethanol exposure. Alcohol Clin. Exp. Res. 31:694-703; 2007.
36. Qiang, M.; Wang, M. W.; Elberger, A. J. Second trimester prenatal alcohol exposure alters development of rat corpus callosum. Neurotoxicol. Teratol. 24:719-732; 2002.
37. Ridley, A. J.; Schwartz, M. A.; Burridge, K.; Firtel, R. A.; Ginsberg, M. H.; Borisy, G.; Parsons, J. T.; Horwitz, A. R. Cell migration: Integrating signals from front to back. Science 302:1704-1709; 2003.
38. Riley, E. P.; McGee, C. L. Fetal alcohol spectrum disorders: An overview with emphasis on changes in brain and behavior. Exp. Biol. Med. (Maywood) 230: 357-365; 2005.
39. Santillano, D. R.; Kumar, L. S.; Prock, T. L.; Camarillo, C.; Tingling, J. D.; Miranda, R. C. Ethanol induces cell-cycle activity and reduces stem cell diversity to alter both regenerative capacity and differentiation potential of cerebral cortical neuroepithelial precursors. BMC Neurosci. 6:59; 2005.
40. Sathyan, P.; Golden, H. B.; Miranda, R. C. Competing interactions between microRNAs determine neural progenitor survival and proliferation following ethanol exposure: Evidence from an ex vivo model of the fetal cerebral cortical neuroepithelium. J. Neurosci. 27: 8546-8557; 2007.
41. Shen, Y.; Mani, S.; Meiri, K. F. Failure to express GAP-43 leads to disruption of a multipotent precursor and inhibits astrocyte differentiation. Mol. Cell. Neurosci. 26:390-405; 2004.
42. Smit, M.; Leng, J.; Klemke, R. L. Assay for neurite outgrowth quantification. Biotechniques 35:254-256; 2003.
43. Sokol, R. J.; Delaney-Black, V.; Nordstrom, B. Fetal alcohol spectrum disorder. JAMA 290:2996-2999; 2003.
44. Takahisi, T.; Goto, T.; Miyama, S.; Nowakowski, R. S.; Caviness, Jr., V. S. Sequence of neuron origin and neocortical laminar fate: Relation to cell cycle of origin in the developing murine cerebral wall. J. Neurosci. 19: 10357-10371; 1999.
45. Tang, N.; He, M.; O'Riordan, M. A.; Farkas, C.; Buck, K.; Lemmon, V.; Bearer, C. F. Ethanol inhibits L1 cell adhesion molecule activation of mitogen-activated protein kinases. J. Neurochem. 96:1480-1490; 2006.
46. Tsai, J.; Floyd, R. Alcohol consumption among women who are pregnant or who might become pregnant -United States, 2002. MMWR 53:1178-1181; 2004.
47. Wade, S.; Oommen, P.; Conner, W.; Earnest, D.; Miranda, R. Overlapping and divergent actions of estrogen and the neurogrophins on cell fate and p-53 dependent signal transduction in conditionally immortalized cerebral cortical neuroblasts. J. Neurosci. 15: 6994-7006; 1999.
48. West, J. R.; Hamre, K. M. Effects of alcohol exposure during different periods of development: Changes in hippocampal mossy fibers. Brain Res. 349:280-284; 1985.
49. West, J. R.; Hamre, K. M.; Cassell, M. D. Effects of ethanol exposure during the third trimester equivalent on neuron number in rat hippocampus and dentate gyrus. Alcohol Clin. Exp. Res. 10:190-197; 1986.
50. Wu, P.; Tarasenko, Y. I.; Gu, Y.; Huang, L. Y.; Coggeshall, R. E.; Yu, Y. Region-specific generation of cholinergic neurons from fetal human neural stem cells grafted in adult rat. Nat. Neurosci. 5:1271-1278; 2002.