Skip to main content
Top
Published in: Molecular Brain 1/2014

Open Access 01-12-2014 | Research

5-mehtyltetrahydrofolate rescues alcohol-induced neural crest cell migration abnormalities

Authors: Yu Shi, Jiejing Li, Chunjiang Chen, Manzi Gong, Yuan Chen, Youxue Liu, Jie Chen, Tingyu Li, Weihong Song

Published in: Molecular Brain | Issue 1/2014

Login to get access

Abstract

Background

Alcohol is detrimental to early development. Fetal alcohol spectrum disorders (FASD) due to maternal alcohol abuse results in a series of developmental abnormalities including cranial facial dysmorphology, ocular anomalies, congenital heart defects, microcephaly and intellectual disabilities. Previous studies have been shown that ethanol exposure causes neural crest (NC) apoptosis and perturbation of neural crest migration. However, the underlying mechanism remains elusive. In this report we investigated the fetal effect of alcohol on the process of neural crest development in the Xenopus leavis.

Results

Pre-gastrulation exposure of 2-4% alcohol induces apoptosis in Xenopus embryo whereas 1% alcohol specifically impairs neural crest migration without observing discernible apoptosis. Additionally, 1% alcohol treatment considerably increased the phenotype of small head (43.4%± 4.4%, total embryo n = 234), and 1.5% and 2.0% dramatically augment the deformation to 81.2% ± 6.5% (n = 205) and 91.6% ±3.0% (n = 235), respectively (P < 0.05). Significant accumulation of Homocysteine was caused by alcohol treatment in embryos and 5-mehtyltetrahydrofolate restores neural crest migration and alleviates homocysteine accumulation, resulting in inhibition of the alcohol-induced neurocristopathies.

Conclusions

Our study demonstrates that prenatal alcohol exposure causes neural crest cell migration abnormality and 5-mehtyltetrahydrofolate could be beneficial for treating FASD.
Appendix
Available only for authorised users
Literature
1.
go back to reference Khalil A, O'Brien P: Alcohol and pregnancy. Obstet Gynaecol Reprod Med. 2010, 20 (10): 311-313. 10.1016/j.ogrm.2010.06.001.CrossRef Khalil A, O'Brien P: Alcohol and pregnancy. Obstet Gynaecol Reprod Med. 2010, 20 (10): 311-313. 10.1016/j.ogrm.2010.06.001.CrossRef
2.
go back to reference Wang G, Bieberich E: Prenatal alcohol exposure triggers ceramide-induced apoptosis in neural crest-derived tissues concurrent with defective cranial development. Cell Death Dis. 2010, 1 (5): e46-10.1038/cddis.2010.22.PubMedPubMedCentralCrossRef Wang G, Bieberich E: Prenatal alcohol exposure triggers ceramide-induced apoptosis in neural crest-derived tissues concurrent with defective cranial development. Cell Death Dis. 2010, 1 (5): e46-10.1038/cddis.2010.22.PubMedPubMedCentralCrossRef
3.
go back to reference Cartwright MM, Smith SM: Increased Cell Death and Reduced Neural Crest Cell Numbers in Ethanol-Exposed Embryos: Partial Basis for the Fetal Alcohol Syndrome Phenotype. Alcohol Clin Exp Res. 1995, 19 (2): 378-386. 10.1111/j.1530-0277.1995.tb01519.x.PubMedCrossRef Cartwright MM, Smith SM: Increased Cell Death and Reduced Neural Crest Cell Numbers in Ethanol-Exposed Embryos: Partial Basis for the Fetal Alcohol Syndrome Phenotype. Alcohol Clin Exp Res. 1995, 19 (2): 378-386. 10.1111/j.1530-0277.1995.tb01519.x.PubMedCrossRef
4.
go back to reference Debelak KA, Smith SM: Avian genetic background modulates the neural crest apoptosis induced by ethanol exposure. Alcohol Clin Exp Res. 2000, 24 (3): 307-314. 10.1111/j.1530-0277.2000.tb04612.x.PubMedCrossRef Debelak KA, Smith SM: Avian genetic background modulates the neural crest apoptosis induced by ethanol exposure. Alcohol Clin Exp Res. 2000, 24 (3): 307-314. 10.1111/j.1530-0277.2000.tb04612.x.PubMedCrossRef
5.
go back to reference Minoux M, Rijli FM: Molecular mechanisms of cranial neural crest cell migration and patterning in craniofacial development. Development. 2010, 137 (16): 2605-2621. 10.1242/dev.040048.PubMedCrossRef Minoux M, Rijli FM: Molecular mechanisms of cranial neural crest cell migration and patterning in craniofacial development. Development. 2010, 137 (16): 2605-2621. 10.1242/dev.040048.PubMedCrossRef
6.
go back to reference Fröb F, Bremer M, Finzsch M, Kichko T, Reeh P, Tamm ER, Charnay P, Wegner M: Establishment of myelinating schwann cells and barrier integrity between central and peripheral nervous systems depend on Sox10. Glia. 2012, 60 (5): 806-819. 10.1002/glia.22310.PubMedCrossRef Fröb F, Bremer M, Finzsch M, Kichko T, Reeh P, Tamm ER, Charnay P, Wegner M: Establishment of myelinating schwann cells and barrier integrity between central and peripheral nervous systems depend on Sox10. Glia. 2012, 60 (5): 806-819. 10.1002/glia.22310.PubMedCrossRef
7.
go back to reference Jain R, Engleka KA, Rentschler SL, Manderfield LJ, Li L, Yuan L, Epstein JA: Cardiac neural crest orchestrates remodeling and functional maturation of mouse semilunar valves. J Clin Invest. 2011, 121 (1): 422-430. 10.1172/JCI44244.PubMedPubMedCentralCrossRef Jain R, Engleka KA, Rentschler SL, Manderfield LJ, Li L, Yuan L, Epstein JA: Cardiac neural crest orchestrates remodeling and functional maturation of mouse semilunar valves. J Clin Invest. 2011, 121 (1): 422-430. 10.1172/JCI44244.PubMedPubMedCentralCrossRef
8.
go back to reference Betancur P, Bronner-Fraser M, Sauka-Spengler T: Assembling neural crest regulatory circuits into a gene regulatory network. Annu Rev Cell Dev Biol. 2010, 26: 581-603. 10.1146/annurev.cellbio.042308.113245.PubMedPubMedCentralCrossRef Betancur P, Bronner-Fraser M, Sauka-Spengler T: Assembling neural crest regulatory circuits into a gene regulatory network. Annu Rev Cell Dev Biol. 2010, 26: 581-603. 10.1146/annurev.cellbio.042308.113245.PubMedPubMedCentralCrossRef
9.
go back to reference Milet C, Monsoro-Burq AH: Neural crest induction at the neural plate border in vertebrates. Dev Biol. 2012, 366 (1): 22-33. 10.1016/j.ydbio.2012.01.013.PubMedCrossRef Milet C, Monsoro-Burq AH: Neural crest induction at the neural plate border in vertebrates. Dev Biol. 2012, 366 (1): 22-33. 10.1016/j.ydbio.2012.01.013.PubMedCrossRef
10.
go back to reference Pegoraro C, Monsoro-Burq AH: Signaling and transcriptional regulation in neural crest specification and migration: lessons from xenopus embryos. Wiley Interdiscip Rev Dev Biol. 2013, 2 (2): 247-259. 10.1002/wdev.76.PubMedCrossRef Pegoraro C, Monsoro-Burq AH: Signaling and transcriptional regulation in neural crest specification and migration: lessons from xenopus embryos. Wiley Interdiscip Rev Dev Biol. 2013, 2 (2): 247-259. 10.1002/wdev.76.PubMedCrossRef
11.
go back to reference Li J, Shi Y, Sun J, Zhang Y, Mao B: Xenopus reduced folate carrier regulates neural crest development epigenetically. PLoS ONE. 2011, 6 (11): e27198-10.1371/journal.pone.0027198.PubMedPubMedCentralCrossRef Li J, Shi Y, Sun J, Zhang Y, Mao B: Xenopus reduced folate carrier regulates neural crest development epigenetically. PLoS ONE. 2011, 6 (11): e27198-10.1371/journal.pone.0027198.PubMedPubMedCentralCrossRef
12.
go back to reference McCarthy N, Wetherill L, Lovely CB, Swartz ME, Foroud TM, Eberhart JK: Pdgfra protects against ethanol-induced craniofacial defects in a zebrafish model of FASD. Development. 2013, 140 (15): 3254-3265. 10.1242/dev.094938.PubMedPubMedCentralCrossRef McCarthy N, Wetherill L, Lovely CB, Swartz ME, Foroud TM, Eberhart JK: Pdgfra protects against ethanol-induced craniofacial defects in a zebrafish model of FASD. Development. 2013, 140 (15): 3254-3265. 10.1242/dev.094938.PubMedPubMedCentralCrossRef
13.
go back to reference Etchevers H, Amiel J, Lyonnet S: Molecular bases of human neurocristopathies. Neural Crest Induction Differ. 2006, 589: 213-234. 10.1007/978-0-387-46954-6_14.CrossRef Etchevers H, Amiel J, Lyonnet S: Molecular bases of human neurocristopathies. Neural Crest Induction Differ. 2006, 589: 213-234. 10.1007/978-0-387-46954-6_14.CrossRef
14.
go back to reference Finnell RH, Greer KA, Barber RC, Piedrahita JA, Shaw GM, Lammer EJ: Neural tube and craniofacial defects with special emphasis on folate pathway genes. Crit Rev Oral Biol Med. 1998, 9 (1): 38-53. 10.1177/10454411980090010201.PubMedCrossRef Finnell RH, Greer KA, Barber RC, Piedrahita JA, Shaw GM, Lammer EJ: Neural tube and craniofacial defects with special emphasis on folate pathway genes. Crit Rev Oral Biol Med. 1998, 9 (1): 38-53. 10.1177/10454411980090010201.PubMedCrossRef
15.
go back to reference Prescott NJ, Malcolm S: Folate and the face: Evaluating the evidence for the influence of folate genes on craniofacial development. Cleft Palate-Craniofacial J. 2002, 39 (3): 327-331. 10.1597/1545-1569(2002), 39(3):327-331CrossRef Prescott NJ, Malcolm S: Folate and the face: Evaluating the evidence for the influence of folate genes on craniofacial development. Cleft Palate-Craniofacial J. 2002, 39 (3): 327-331. 10.1597/1545-1569(2002), 39(3):327-331CrossRef
16.
go back to reference Goldmuntz E, Woyciechowski S, Renstrom D, Lupo PJ, Mitchell LE: Variants of folate metabolism genes and the risk of conotruncal cardiac defects. Circulation Cardiovascular Genetics. 2008, 1 (2): 126-132. 10.1161/CIRCGENETICS.108.796342.PubMedPubMedCentralCrossRef Goldmuntz E, Woyciechowski S, Renstrom D, Lupo PJ, Mitchell LE: Variants of folate metabolism genes and the risk of conotruncal cardiac defects. Circulation Cardiovascular Genetics. 2008, 1 (2): 126-132. 10.1161/CIRCGENETICS.108.796342.PubMedPubMedCentralCrossRef
17.
go back to reference Wang LL, Zhang Z, Li Q, Yang R, Pei X, Xu Y, Wang J, Zhou SF, Li Y: Ethanol exposure induces differential microRNA and target gene expression and teratogenic effects which can be suppressed by folic acid supplementation. Hum Reprod. 2009, 24 (3): 562-579. 10.1093/humrep/den439.PubMedCrossRef Wang LL, Zhang Z, Li Q, Yang R, Pei X, Xu Y, Wang J, Zhou SF, Li Y: Ethanol exposure induces differential microRNA and target gene expression and teratogenic effects which can be suppressed by folic acid supplementation. Hum Reprod. 2009, 24 (3): 562-579. 10.1093/humrep/den439.PubMedCrossRef
18.
go back to reference Xu Y, Tang Y, Li Y: Effect of folic acid on prenatal alcohol-induced modification of brain proteome in mice. Br J Nutr. 2008, 99 (3): 455-461. 10.1017/S0007114507812074.PubMedCrossRef Xu Y, Tang Y, Li Y: Effect of folic acid on prenatal alcohol-induced modification of brain proteome in mice. Br J Nutr. 2008, 99 (3): 455-461. 10.1017/S0007114507812074.PubMedCrossRef
19.
go back to reference Brauer PR, Rosenquist TH: Effect of elevated homocysteine on cardiac neural crest migration in vitro. Dev Dyn. 2002, 224 (2): 222-230. 10.1002/dvdy.10105.PubMedCrossRef Brauer PR, Rosenquist TH: Effect of elevated homocysteine on cardiac neural crest migration in vitro. Dev Dyn. 2002, 224 (2): 222-230. 10.1002/dvdy.10105.PubMedCrossRef
20.
go back to reference Swartz ME, Wells MB, Griffin M, McCarthy N, Lovely CB, McGurk P, Rozacky J, Eberhart JK: A screen of zebrafish mutants identifies ethanol-sensitive genetic loci. Alcohol Clin Exp Res. 2013, 38 (3): 694-703. 10.1111/acer.12286.PubMedPubMedCentralCrossRef Swartz ME, Wells MB, Griffin M, McCarthy N, Lovely CB, McGurk P, Rozacky J, Eberhart JK: A screen of zebrafish mutants identifies ethanol-sensitive genetic loci. Alcohol Clin Exp Res. 2013, 38 (3): 694-703. 10.1111/acer.12286.PubMedPubMedCentralCrossRef
21.
go back to reference Boric K, Orio P, Viéville T, Whitlock K: Quantitative analysis of cell migration using optical flow. PLoS ONE. 2013, 8 (7): e69574-10.1371/journal.pone.0069574.PubMedPubMedCentralCrossRef Boric K, Orio P, Viéville T, Whitlock K: Quantitative analysis of cell migration using optical flow. PLoS ONE. 2013, 8 (7): e69574-10.1371/journal.pone.0069574.PubMedPubMedCentralCrossRef
22.
go back to reference Oyedele OO, Kramer B: Nuanced but significant: How ethanol perturbs avian cranial neural crest cell actin cytoskeleton, migration and proliferation. Alcohol. 2013, 47 (5): 417-426. 10.1016/j.alcohol.2013.04.001.PubMedCrossRef Oyedele OO, Kramer B: Nuanced but significant: How ethanol perturbs avian cranial neural crest cell actin cytoskeleton, migration and proliferation. Alcohol. 2013, 47 (5): 417-426. 10.1016/j.alcohol.2013.04.001.PubMedCrossRef
23.
go back to reference Said HM, Mee L, Sekar VT, Ashokkumar B, Pandol SJ: Mechanism and regulation of folate uptake by pancreatic acinar cells: effect of chronic alcohol consumption. Am J Physiol Gastrointest Liver Physiol. 2010, 298 (6): G985-G993. 10.1152/ajpgi.00068.2010.PubMedPubMedCentralCrossRef Said HM, Mee L, Sekar VT, Ashokkumar B, Pandol SJ: Mechanism and regulation of folate uptake by pancreatic acinar cells: effect of chronic alcohol consumption. Am J Physiol Gastrointest Liver Physiol. 2010, 298 (6): G985-G993. 10.1152/ajpgi.00068.2010.PubMedPubMedCentralCrossRef
24.
go back to reference Bleich S, Degner D, Wiltfang J, Maler J, Niedmann P, Cohrs S, Mangholz A, Porzig J, Sprung R, Rüther E: Elevated homocysteine levels in alcohol withdrawal. Alcohol Alcohol. 2000, 35 (4): 351-354. 10.1093/alcalc/35.4.351.PubMedCrossRef Bleich S, Degner D, Wiltfang J, Maler J, Niedmann P, Cohrs S, Mangholz A, Porzig J, Sprung R, Rüther E: Elevated homocysteine levels in alcohol withdrawal. Alcohol Alcohol. 2000, 35 (4): 351-354. 10.1093/alcalc/35.4.351.PubMedCrossRef
25.
go back to reference Stickel F, Choi SW, Kim YI, Bagley PJ, Seitz HK, Russell RM, Selhub J, Mason JB: Effect of chronic alcohol consumption on total plasma homocysteine level in rats. Alcohol Clin Exp Res. 2000, 24 (3): 259-264. 10.1111/j.1530-0277.2000.tb04606.x.PubMedCrossRef Stickel F, Choi SW, Kim YI, Bagley PJ, Seitz HK, Russell RM, Selhub J, Mason JB: Effect of chronic alcohol consumption on total plasma homocysteine level in rats. Alcohol Clin Exp Res. 2000, 24 (3): 259-264. 10.1111/j.1530-0277.2000.tb04606.x.PubMedCrossRef
26.
go back to reference Lahiri DK, Maloney B, Zawia NH: The LEARn model: an epigenetic explanation for idiopathic neurobiological diseases. Mol Psychiatry. 2009, 14 (11): 992-1003. 10.1038/mp.2009.82.PubMedCrossRef Lahiri DK, Maloney B, Zawia NH: The LEARn model: an epigenetic explanation for idiopathic neurobiological diseases. Mol Psychiatry. 2009, 14 (11): 992-1003. 10.1038/mp.2009.82.PubMedCrossRef
27.
go back to reference Lahiri DK, Maloney B: The "LEARn" (Latent Early-life Associated Regulation) model integrates environmental risk factors and the developmental basis of Alzheimer's disease, and proposes remedial steps. Exp Gerontol. 2010, 45 (4): 291-296. 10.1016/j.exger.2010.01.001.PubMedPubMedCentralCrossRef Lahiri DK, Maloney B: The "LEARn" (Latent Early-life Associated Regulation) model integrates environmental risk factors and the developmental basis of Alzheimer's disease, and proposes remedial steps. Exp Gerontol. 2010, 45 (4): 291-296. 10.1016/j.exger.2010.01.001.PubMedPubMedCentralCrossRef
28.
go back to reference Beaudin AE, Stover PJ: Folate-mediated one-carbon metabolism and neural tube defects: Balancing genome synthesis and gene expression. Birth Defects Research Part C Embryo Today Reviews. 2007, 81 (3): 183-203. 10.1002/bdrc.20100.CrossRef Beaudin AE, Stover PJ: Folate-mediated one-carbon metabolism and neural tube defects: Balancing genome synthesis and gene expression. Birth Defects Research Part C Embryo Today Reviews. 2007, 81 (3): 183-203. 10.1002/bdrc.20100.CrossRef
29.
go back to reference Bajpai R, Chen DA, Rada-Iglesias A, Zhang J, Xiong Y, Helms J, Chang CP, Zhao Y, Swigut T, Wysocka J: CHD7 cooperates with PBAF to control multipotent neural crest formation. Nature. 2010, 463 (7283): 958-962. 10.1038/nature08733.PubMedPubMedCentralCrossRef Bajpai R, Chen DA, Rada-Iglesias A, Zhang J, Xiong Y, Helms J, Chang CP, Zhao Y, Swigut T, Wysocka J: CHD7 cooperates with PBAF to control multipotent neural crest formation. Nature. 2010, 463 (7283): 958-962. 10.1038/nature08733.PubMedPubMedCentralCrossRef
30.
go back to reference Huang RFS, Hsu YC, Lin HL, Yang FL: Folate depletion and elevated plasma homocysteine promote oxidative stress in rat livers. J Nutr Health. 2001, 131 (1): 33-38. Huang RFS, Hsu YC, Lin HL, Yang FL: Folate depletion and elevated plasma homocysteine promote oxidative stress in rat livers. J Nutr Health. 2001, 131 (1): 33-38.
31.
go back to reference van der Dijs FPL, Schnog JJB, Brouwer D, Velvis HJR, van den Berg GA, Bakker AJ, Duits AJ, Muskiet FD, Muskiet FAJ: Elevated homocysteine levels indicate suboptimal folate status in pediatric sickle cell patients. Am J Hematol 1998, 59(3):192-198. 10.1002/(SICI)1096-8652(199811)PubMedCrossRef van der Dijs FPL, Schnog JJB, Brouwer D, Velvis HJR, van den Berg GA, Bakker AJ, Duits AJ, Muskiet FD, Muskiet FAJ: Elevated homocysteine levels indicate suboptimal folate status in pediatric sickle cell patients. Am J Hematol 1998, 59(3):192-198. 10.1002/(SICI)1096-8652(199811)PubMedCrossRef
32.
go back to reference Jacques PF, Selhub J, Bostom AG, Wilson PWF, Rosenberg IH: The effect of folic acid fortification on plasma folate and total homocysteine concentrations. N Engl J Med. 1999, 340 (19): 1449-1454. 10.1056/NEJM199905133401901.PubMedCrossRef Jacques PF, Selhub J, Bostom AG, Wilson PWF, Rosenberg IH: The effect of folic acid fortification on plasma folate and total homocysteine concentrations. N Engl J Med. 1999, 340 (19): 1449-1454. 10.1056/NEJM199905133401901.PubMedCrossRef
33.
go back to reference Brauer P, Tierney B: Consequences of elevated homocysteine during embryonic development and possible modes of action. Curr Pharm Des. 2004, 10 (22): 2719-2732. 10.2174/1381612043383692.PubMedCrossRef Brauer P, Tierney B: Consequences of elevated homocysteine during embryonic development and possible modes of action. Curr Pharm Des. 2004, 10 (22): 2719-2732. 10.2174/1381612043383692.PubMedCrossRef
34.
go back to reference Steegers-Theunissen RPM, Boers GHJ, Trijbels FJM, Finkelstein JD, Blom HJ, Thomas CMG, Borm GF, Wouters MGAJ, Eskes TKAB: Maternal hyperhomocysteinemia: a risk factor for neural-tube defects?. Metabolism. 1994, 43 (12): 1475-1480. 10.1016/0026-0495(94)90004-3.PubMedCrossRef Steegers-Theunissen RPM, Boers GHJ, Trijbels FJM, Finkelstein JD, Blom HJ, Thomas CMG, Borm GF, Wouters MGAJ, Eskes TKAB: Maternal hyperhomocysteinemia: a risk factor for neural-tube defects?. Metabolism. 1994, 43 (12): 1475-1480. 10.1016/0026-0495(94)90004-3.PubMedCrossRef
35.
go back to reference Kapusta L, Haagmans MLM, Steegers EAP, Cuypers MHM, Blom HJ, Eskes TKAB: Congenital heart defects and maternal derangement of homocysteine metabolism. J Pediatr. 1999, 135 (6): 773-774. 10.1016/S0022-3476(99)70102-2.PubMedCrossRef Kapusta L, Haagmans MLM, Steegers EAP, Cuypers MHM, Blom HJ, Eskes TKAB: Congenital heart defects and maternal derangement of homocysteine metabolism. J Pediatr. 1999, 135 (6): 773-774. 10.1016/S0022-3476(99)70102-2.PubMedCrossRef
36.
go back to reference Verkleij-Hagoort A, Bliek J, Sayed-Tabatabaei F, Ursem N, Steegers E, Steegers-Theunissen R: Hyperhomocysteinemia and MTHFR polymorphisms in association with orofacial clefts and congenital heart defects: A meta-analysis. Am J Med Genet A. 2007, 143 (9): 952-960. 10.1002/ajmg.a.31684.CrossRef Verkleij-Hagoort A, Bliek J, Sayed-Tabatabaei F, Ursem N, Steegers E, Steegers-Theunissen R: Hyperhomocysteinemia and MTHFR polymorphisms in association with orofacial clefts and congenital heart defects: A meta-analysis. Am J Med Genet A. 2007, 143 (9): 952-960. 10.1002/ajmg.a.31684.CrossRef
37.
go back to reference Da Lee R, An SM, Kim SS, Rhee GS, Kwack SJ, Seok JH, Chae SY, Park CH, Choi YW, Kim HS: Neurotoxic effects of alcohol and acetaldehyde during embryonic development. J Toxic Environ Health A. 2005, 68 (23-24): 2147-2162. 10.1080/15287390500177255.CrossRef Da Lee R, An SM, Kim SS, Rhee GS, Kwack SJ, Seok JH, Chae SY, Park CH, Choi YW, Kim HS: Neurotoxic effects of alcohol and acetaldehyde during embryonic development. J Toxic Environ Health A. 2005, 68 (23-24): 2147-2162. 10.1080/15287390500177255.CrossRef
38.
go back to reference Bilotta J, Barnett JA, Hancock L, Saszik S: Ethanol exposure alters zebrafish development: a novel model of fetal alcohol syndrome. Neurotoxicol Teratol. 2004, 26 (6): 737-743. 10.1016/j.ntt.2004.06.011.PubMedCrossRef Bilotta J, Barnett JA, Hancock L, Saszik S: Ethanol exposure alters zebrafish development: a novel model of fetal alcohol syndrome. Neurotoxicol Teratol. 2004, 26 (6): 737-743. 10.1016/j.ntt.2004.06.011.PubMedCrossRef
39.
go back to reference Minana R, Climent E, Barettino D, Segui J, Renau-Piqueras J, Guerri C: Alcohol exposure alters the expression pattern of neural cell adhesion molecules during brain development. J Neurochem. 2000, 75 (3): 954-964. 10.1046/j.1471-4159.2000.0750954.x.PubMedCrossRef Minana R, Climent E, Barettino D, Segui J, Renau-Piqueras J, Guerri C: Alcohol exposure alters the expression pattern of neural cell adhesion molecules during brain development. J Neurochem. 2000, 75 (3): 954-964. 10.1046/j.1471-4159.2000.0750954.x.PubMedCrossRef
40.
go back to reference Zhou F, Sari Y, Zhang J, Goodlett C, Li TK: Prenatal alcohol exposure retards the migration and development of serotonin neurons in fetal C57BL mice. Dev Brain Res. 2001, 126 (2): 147-155. 10.1016/S0165-3806(00)00144-9.CrossRef Zhou F, Sari Y, Zhang J, Goodlett C, Li TK: Prenatal alcohol exposure retards the migration and development of serotonin neurons in fetal C57BL mice. Dev Brain Res. 2001, 126 (2): 147-155. 10.1016/S0165-3806(00)00144-9.CrossRef
41.
go back to reference Li YX, Yang HT, Zdanowicz M, Sicklick JK, Qi Y, Camp TJ, Diehl AM: Fetal alcohol exposure impairs Hedgehog cholesterol modification and signaling. Lab Investig. 2007, 87 (3): 231-240. 10.1038/labinvest.3700516.PubMedCrossRef Li YX, Yang HT, Zdanowicz M, Sicklick JK, Qi Y, Camp TJ, Diehl AM: Fetal alcohol exposure impairs Hedgehog cholesterol modification and signaling. Lab Investig. 2007, 87 (3): 231-240. 10.1038/labinvest.3700516.PubMedCrossRef
42.
go back to reference Shi Y, Zhao S, Li J, Mao B: Islet-1 is required for ventral neuron survival in Xenopus. Biochem Biophys Res Commun. 2009, 388 (3): 506-510. 10.1016/j.bbrc.2009.08.017.PubMedCrossRef Shi Y, Zhao S, Li J, Mao B: Islet-1 is required for ventral neuron survival in Xenopus. Biochem Biophys Res Commun. 2009, 388 (3): 506-510. 10.1016/j.bbrc.2009.08.017.PubMedCrossRef
43.
go back to reference Kashef J, Köhler A, Kuriyama S, Alfandari D, Mayor R, Wedlich D: Cadherin-11 regulates protrusive activity in Xenopus cranial neural crest cells upstream of Trio and the small GTPases. Genes Dev. 2009, 23 (12): 1393-1398. 10.1101/gad.519409.PubMedPubMedCentralCrossRef Kashef J, Köhler A, Kuriyama S, Alfandari D, Mayor R, Wedlich D: Cadherin-11 regulates protrusive activity in Xenopus cranial neural crest cells upstream of Trio and the small GTPases. Genes Dev. 2009, 23 (12): 1393-1398. 10.1101/gad.519409.PubMedPubMedCentralCrossRef
44.
go back to reference Aybar MJ, Nieto MA, Mayor R: Snail precedes slug in the genetic cascade required for the specification and migration of the Xenopus neural crest. Development. 2003, 130 (3): 483-494. 10.1242/dev.00238.PubMedCrossRef Aybar MJ, Nieto MA, Mayor R: Snail precedes slug in the genetic cascade required for the specification and migration of the Xenopus neural crest. Development. 2003, 130 (3): 483-494. 10.1242/dev.00238.PubMedCrossRef
Metadata
Title
5-mehtyltetrahydrofolate rescues alcohol-induced neural crest cell migration abnormalities
Authors
Yu Shi
Jiejing Li
Chunjiang Chen
Manzi Gong
Yuan Chen
Youxue Liu
Jie Chen
Tingyu Li
Weihong Song
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Molecular Brain / Issue 1/2014
Electronic ISSN: 1756-6606
DOI
https://doi.org/10.1186/s13041-014-0067-9

Other articles of this Issue 1/2014

Molecular Brain 1/2014 Go to the issue