High-throughput transcriptome sequencing identifies candidate genetic modifiers of vulnerability to fetal alcohol spectrum disorders

Alcoholism: Clinical and Experimental Research

Volumn 38, Issue 7, 2014, Pages 1874-1882

  Garic, Ana ^a   Berres, Mark E ^a   Smith, Susan M ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Apoptosis; Diamond Blackfan anemia; Fetal alcohol spectrum disorders; Gallus gallus; Neural crest; Oxidative phosphorylation; Ribosome biogenesis; Transcriptome profiling

Indexed keywords

ALCOHOL; BETA CATENIN; CALCIUM; CALMODULIN; PROTEIN P53; RIBOSOME PROTEIN; RNA; TRANSCRIPTOME; WNT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BIOGENESIS; CALCIUM CELL LEVEL; CALCIUM MOBILIZATION; CALCIUM SIGNALING; CONTROLLED STUDY; CRANIOFACIAL MALFORMATION; DNA POLYMORPHISM; EMBRYO; ENDOPLASMIC RETICULUM; ENERGY METABOLISM; FETAL ALCOHOL SYNDROME; GALLUS GALLUS; GENE CLUSTER; GENE EXPRESSION; GENETIC RESOURCE; GENETIC TRANSCRIPTION; HEREDITY; HIGH THROUGHPUT SEQUENCING; METABOLISM; MOUSE; NEURAL CREST; NEUROTOXICITY; NONHUMAN; ONTOGENY; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN PROCESSING; RNA SEQUENCE; SIGNAL TRANSDUCTION; SPLICEOSOME; ANIMAL; CELL DEATH; CHICKEN; CYTOLOGY; DOSE RESPONSE; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION; GENETIC PREDISPOSITION; GENETICS; NEURAL STEM CELL;

ANIMALS; APOPTOSIS; CELL DEATH; CHICKENS; DOSE-RESPONSE RELATIONSHIP, DRUG; ETHANOL; FETAL ALCOHOL SPECTRUM DISORDERS; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION STUDIES; GENETIC PREDISPOSITION TO DISEASE; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; NEURAL CREST; NEURAL STEM CELLS; SIGNAL TRANSDUCTION;

EID: 84904341459     PISSN: 01456008     EISSN: 15300277     Source Type: Journal    
DOI: 10.1111/acer.12457     Document Type: Article

References (46)

1. Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106.
2. Boehm SL II, Lundahl KR, Caldwell J, Gilliam DM (1997) Ethanol teratogenesis in the C57BL/6J, DBA/2J, and A/J inbred mouse strains. Alcohol 14:389-395.
3. Bolnick JM, Karana R, Chiang PJ, Kilburn BA, Romero R, Diamond MP, Smith SM, Armant DR (2014) Apoptosis of alcohol-exposed human placental cytotrophoblast cells is downstream of intracellular calcium signaling. Alcohol Clin Exp Res 2014; doi: 10.1111/acer.12417
4. Bugner V, Tecza A, Gessert S, Kühl M (2011) Peter Pan functions independently of its role in ribosome biogenesis during early eye and craniofacial cartilage development in Xenopus laevis. Development 138:2369-2378.
5. Carter RC, Jacobson SW, Molteno CD, Jacobson JL (2007) Fetal alcohol exposure, iron-deficiency anemia, and infant growth. Pediatrics 120:559-567.
6. Cartwright MM, Smith SM (1995) Stage dependent effects of ethanol on cranial neural crest cell development: partial basis for the phenotypic variations observed in fetal alcohol syndrome. Alcohol Clin Exp Res 19:1454-1462.
7. Cartwright MM, Tessmer LA, Smith SM (1998) Ethanol-induced neural crest apoptosis is coincident with their endogenous death but is mechanistically distinct. Alcohol Clin Exp Res 22:142-149.
8. Chen SY, Periasamy A, Yang B, Herman B, Jacobson K, Sulik KK (2000) Differential sensitivity of mouse neural crest cells to ethanol-induced toxicity. Alcohol 20:75-81.
9. Das UG, Cronk CE, Martier SS, Simpson PM, McCarver DG (2004) Alcohol dehydrogenase 2*3 affects alterations in offspring facial morphology associated with maternal ethanol intake in pregnancy. Alcohol Clin Exp Res 28:1598-1606.
10. Debelak KA, Smith SM (2000) Avian genetic background modulates the neural crest apoptosis induced by ethanol exposure. Alcohol Clin Exp Res 24:307-314.
11. Debelak-Kragtorp KA, Armant DR, Smith SM (2003) Ethanol-induced cephalic apoptosis requires phospholipase C-dependent intracellular calcium signaling. Alcohol Clin Exp Res 27:515-523.
12. Dillies MA, Rau A, Aubert J, Hennequet-Antier C, Jeanmougin M, Servant N, Keime C, Marot G, Castel D, Estelle J, Guernec G, Jagla B, Jouneau L, Laloë D, Le Gall C, Schaëffer B, Le Crom S, Guedj M, Jaffrézic F; French StatOmique Consortium (2013) A comprehensive evaluation of normalization methods for Illumina high-throughput RNA sequencing data analysis. Brief Bioinform 14:671-683.
13. Downing C, Balderrama-Durbin C, Kimball A, Biers J, Wright H, Gilliam D, Johnson TE (2012) Quantitative trait locus mapping for ethanol teratogenesis in BXD recombinant inbred mice. Alcohol Clin Exp Res 36:1340-1354.
14. Dunty WC Jr, Chen SY, Zucker RM, Dehart DB, Sulik KK (2001) Selective vulnerability of embryonic cell populations to ethanol-induced apoptosis: implications for alcohol-related birth defects and neurodevelopmental disorder. Alcohol Clin Exp Res 36:1340-1354.
15. Flentke GR, Garic A, Amberger E, Hernandez M, Smith SM (2011) Calcium-mediated repression of β-catenin and its transcriptional signaling mediates neural crest cell death in an avian model of fetal alcohol syndrome. Birth Defects Res A Clin Mol Teratol 91:591-602.
16. Flentke GR, Garic A, Hernandez M, Smith SM (2014a) CaMKII represses transcriptionally-active β-catenin to mediate acute ethanol neurodegeneration and can phosphorylate β-catenin. J Neurochem 128:523-535.
17. Flentke GR, Klingler RH, Tanguay RL, Carvan MJ III, Smith SM (2014b) An evolutionarily-conserved mechanism of calcium-dependent neurotoxicity in a zebrafish model of FASD. Alcohol Clin Exp Res 38:1255-1265.
18. Fumagalli S, Thomas G (2011) The role of p53 in ribosomopathies. Semin Hematol 48:97-105.
19. Garic A, Flentke GR, Amberger E, Hernandez M, Smith SM (2011) CaMKII activation is a novel effector of alcohol's neurotoxicity in neural crest stem/progenitor cells. J Neurochem 118:646-657.
20. 2+ transient. Alcohol Clin Exp Res 29:1237-1246.
21. Gilliam DM, Kotch LE (1996) Dose-related growth deficits in LS but not SS mice prenatally exposed to alcohol. Alcohol 13:47-51.
22. Goodlett CR, Gillam DM, Nichols JM, West JR (1989) Genetic influences on brain growth restriction induced by developmental exposure to alcohol. Neurotoxicity 10:321-334.
23. Green ML, Singh AV, Zhang Y, Nemeth KA, Sulik KK, Knudsen TB (2007) Reprogramming of genetic networks during initiation of the Fetal Alcohol Syndrome. Dev Dyn 236:613-631.
24. Gutala R, Wang J, Kadapakkam S, Hwang Y, Ticku M, Li MD (2004) Microarray analysis of ethanol-treated cortical neurons reveals disruption of genes related to the ubiquitin-proteasome pathway and protein synthesis. Alcohol Clin Exp Res 28:1779-1788.
25. Huang DW, Sherman BT, Lempicki RA (2009a) Systematic and integrative analysis of large gene lists using DAVID Bioinformatics Resources. Nat Protoc 4:44-57.
26. Huang DW, Sherman BT, Lempicki RA (2009b) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37:1-13.
27. Kanehisa M, Goto S (2000) KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28:27-30.
28. Kilburn BA, Chiang PJ, Wang J, Flentke GR, Smith SM, Armant DR (2006) Rapid induction of apoptosis in gastrulating mouse embryos by ethanol and its prevention by HB-EGF. Alcohol Clin Exp Res 30:127-134.
29. Kouzoukas DE, Li G, Takapoo M, Moninger T, Bhalla RC, Pantazis NJ (2013) Intracellular calcium plays a critical role in the alcohol-mediated death of cerebellar granule neurons. J Neurochem 124:323-335.
30. Kruse JP, Gu W (2009) Modes of p53 regulation. Cell 137:3907-3920.
31. Leonardson GR, Loudenburg R (2003) Risk factors for alcohol use during pregnancy in a multistate area. Neurotoxicol Teratol 25:651-658.
32. Mattson SN, Roesch SC, Glass L, Deweese BN, Coles CD, Kable JA, May PA, Kalberg WO, Sowell ER, Adnams CM, Jones KL, Riley EP; CIFASD (2013) Further development of a neurobehavioral profile of fetal alcohol spectrum disorders. Alcohol Clin Exp Res 37:517-528.
33. May PA, Tabachnick BG, Gossage JP, Kalberg WO, Marais AS, Robinson LK, Manning M, Buckley D, Hoyme HE (2011) Maternal risk factors predicting child physical characteristics and dysmorphology in fetal alcohol syndrome and partial fetal alcohol syndrome. Drug Alcohol Depend 119:18-27.
34. McCarver DG, Thomasson HR, Martier SS, Sokol RJ, Li T (1997) Alcohol dehydrogenase-2*3 allele protects against alcohol-related birth defects among African Americans. J Pharmacol Exp Ther 283:1095-1101.
35. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621-628.
36. Narla A, Ebert BL (2010) Ribosomopathies: human disorders of ribosome dysfunction. Blood 115:3196-3205.
37. Oshlack A, Wakefield MJ (2009) Transcript length bias in RNA-seq data confounds systems biology. Biol Direct 4:14.
38. Rahman S, Miles MF (2001) Identification of novel ethanol-sensitive genes by expression profiling. Pharmacol Ther 92:123-134.
39. Streissguth AP, Dehaene P (1993) Fetal alcohol syndrome in twins of alcoholic mothers: concordance of diagnosis and IQ. Am J Med Genet 47:857-861.
40. Su B, Debelak KA, Tessmer LL, Cartwright MM, Smith SM (2001) Genetic influences on craniofacial outcome in an avian model of prenatal alcohol exposure. Alcohol Clin Exp Res 25:60-69.
41. Swartz ME, Wells MB, Griffin M, McCarthy N, Lovely CB, McGurk P, Rozacky J, Eberhart JK (2014) A screen of zebrafish mutants identifies ethanol-sensitive genetic loci. Alcohol Clin Exp Res 38:694-703.
42. Teng T, Thomas G, Mercer CA (2013) Growth control and ribosomopathies. Curr Opin Genet Dev 23:63-71.
43. Trainor PA (2010) Craniofacial birth defects: the role of neural crest cells in the etiology and pathogenesis of Treacher Collins syndrome and the potential for prevention. Am J Med Genet A 152A:2984-2994.
44. Viljoen DL, Carr LG, Foroud TM, Brooke L, Ramsay M, Li TK (2001) Alcohol dehydrogenase-2*2 allele is associated with decreased prevalence of fetal alcohol syndrome in the mixed-ancestry population of the Western Cape Province, South Africa. Alcohol Clin Exp Res 25:1719-1722.
45. Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10:57-63.
46. Warren KR, Li TK (2005) Genetic polymorphisms: impact on the risk of fetal alcohol spectrum disorders. Birth Defects Res A Clin Mol Teratol 73:195-203.