Maternal and neonatal plasma microrna biomarkers for fetal alcohol exposure in an ovine model

Alcoholism: Clinical and Experimental Research

Volumn 38, Issue 5, 2014, Pages 1390-1400

  Balaraman, Sridevi ^a   Lunde, E Raine ^b   Sawant, Onkar ^b   Cudd, Timothy A ^b   Washburn, Shannon E ^b   Miranda, Rajesh C ^a  

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

^b TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Fetal alcohol exposure; Maternal alcohol exposure; MiRNA; Passenger strand miRNA; Plasma miRNAs

Indexed keywords

ALCOHOL; BIOLOGICAL MARKER; MICRORNA; TRANSCRIPTOME;

ANIMAL; BLOOD; CHEMISTRY; DISEASE MODEL; DRUG EFFECTS; ERYTHROCYTE; FEMALE; FETAL ALCOHOL SPECTRUM DISORDERS; LEUKOCYTE; MALE; NEWBORN; PREGNANCY; SHEEP;

ANIMALS; ANIMALS, NEWBORN; BIOLOGICAL MARKERS; DISEASE MODELS, ANIMAL; ERYTHROCYTES; ETHANOL; FEMALE; FETAL ALCOHOL SPECTRUM DISORDERS; LEUKOCYTES; MALE; MICRORNAS; PREGNANCY; SHEEP; TRANSCRIPTOME;

EID: 84899444374     PISSN: 01456008     EISSN: 15300277     Source Type: Journal    
DOI: 10.1111/acer.12378     Document Type: Article

References (52)

1. Arroyo JD, Chevillet JR, Kroh EM, Ruf IK, Pritchard CC, Gibson DF, Mitchell PS, Bennett CF, Pogosova-Agadjanyan EL, Stirewalt DL, Tait JF, Tewari M (2011) Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci USA 108:5003-5008.
2. Bakhireva LN, Savich RD, Raisch DW, Cano S, Annett RD, Leeman L, Garg M, Goff C, Savage DD (2013) The feasibility and cost of neonatal screening for prenatal alcohol exposure by measuring phosphatidylethanol in dried blood spots. Alcohol Clin Exp Res 37:1008-1015.
3. Bala S, Petrasek J, Mundkur S, Catalano D, Levin I, Ward J, Alao H, Kodys K, Szabo G (2012) Circulating microRNAs in exosomes indicate hepatocyte injury and inflammation in alcoholic, drug-induced, and inflammatory liver diseases. Hepatology 56:1946-1957.
4. Balaraman S, Winzer-Serhan UH, Miranda RC (2012) Opposing actions of ethanol and nicotine on microRNAs are mediated by nicotinic acetylcholine receptors in fetal cerebral cortical-derived neural progenitor cells. Alcohol Clin Exp Res 36:1669-1677.
5. Ballard HS (1997) The hematological complications of alcoholism. Alcohol Health Res World 21:42-52.
6. Barry JS, Anthony RV (2008) The pregnant sheep as a model for human pregnancy. Theriogenology 69:55-67.
7. Caetano R, Ramisetty-Mikler S, Floyd LR, McGrath C (2006) The epidemiology of drinking among women of child-bearing age. Alcohol Clin Exp Res 30:1023-1030.
8. Centers for Disease Control and Prevention (CDC) (2012) Alcohol use and binge drinking among women of childbearing age-United States, 2006-2010. MMWR Morb Mortal Wkly Rep 61:534-538.
9. Chim SS, Shing TK, Hung EC, Leung TY, Lau TK, Chiu RW, Lo YM (2008) Detection and characterization of placental microRNAs in maternal plasma. Clin Chem 54:482-490.
10. Ebrahim SH, Diekman ST, Floyd RL, Decoufle P (1999) Comparison of binge drinking among pregnant and nonpregnant women, United States, 1991-1995. Am J Obstet Gynecol 180:1-7.
11. Gallo A, Tandon M, Alevizos I, Illei GG (2012) The majority of microRNAs detectable in serum and saliva is concentrated in exosomes. PLoS One 7:e30679.
12. Gladstone J, Nulman I, Koren G (1996) Reproductive risks of binge drinking during pregnancy. Reprod Toxicol 10:3-13.
13. Go AT, Visser A, van Dijk M, Mulders MA, Eijk P, Ylstra B, Blankenstein MA, van Vugt JM, Oudejans CB (2008) A novel method to identify syncytiotrophoblast-derived RNA products representative of trisomy 21 placental RNA in maternal plasma. Methods Mol Biol 444:291-302.
14. Gu H, Li H, Zhang L, Luan H, Huang T, Wang L, Fan Y, Zhang Y, Liu X, Wang W, Yuan Z (2012) Diagnostic role of microRNA expression profile in the serum of pregnant women with fetuses with neural tube defects. J Neurochem 122:641-649.
15. Habbick BF, Blakley PM, Houston CS, Snyder RE, Senthilselvan A, Nanson JL (1998) Bone age and growth in fetal alcohol syndrome. Alcohol Clin Exp Res 22:1312-1316.
16. Hellemans KG, Sliwowska JH, Verma P, Weinberg J (2010) Prenatal alcohol exposure: fetal programming and later life vulnerability to stress, depression and anxiety disorders. Neurosci Biobehav Rev 34:791-807.
17. Jones KL, Smith DW (1975) The fetal alcohol syndrome. Teratology 12:1-10.
18. Kagami M, Sekita Y, Nishimura G, Irie M, Kato F, Okada M, Yamamori S, Kishimoto H, Nakayama M, Tanaka Y, Matsuoka K, Takahashi T, Noguchi M, Tanaka Y, Masumoto K, Utsunomiya T, Kouzan H, Komatsu Y, Ohashi H, Kurosawa K, Kosaki K, Ferguson-Smith AC, Ishino F, Ogata T (2008) Deletions and epimutations affecting the human 14q32.2 imprinted region in individuals with paternal and maternal upd(14)-like phenotypes. Nat Genet 40:237-242.
19. Kirschner MB, Kao SC, Edelman JJ, Armstrong NJ, Vallely MP, van Zandwijk N, Reid G (2011) Haemolysis during sample preparation alters microRNA content of plasma. PLoS One 6:e24145.
20. Kvigne VL, Randall B, Simanton EG, Brenneman G, Welty TK (2012) Blood alcohol levels for American Indian mothers and newborns. Pediatrics 130:e1015-e1018.
21. Lai CY, Yu SL, Hsieh MH, Chen CH, Chen HY, Wen CC, Huang YH, Hsiao PC, Hsiao CK, Liu CM, Yang PC, Hwu HG, Chen WJ (2011) MicroRNA expression aberration as potential peripheral blood biomarkers for schizophrenia. PLoS One 6:e21635.
22. Leucht C, Stigloher C, Wizenmann A, Klafke R, Folchert A, Bally-Cuif L (2008) MicroRNA-9 directs late organizer activity of the midbrain-hindbrain boundary. Nat Neurosci 11:641-648.
23. Matlow JN, Aleksa K, Lubetsky A, Koren G (2012) The detection and quantification of ethyl glucuronide in placental tissue and placental perfusate by headspace solid-phase microextraction coupled with gas chromatography-mass spectrometry. J Popul Ther Clin Pharmacol 19:e473-e482.
24. Matranga C, Tomari Y, Shin C, Bartel DP, Zamore PD (2005) Passenger-strand cleavage facilitates assembly of siRNA into Ago2-containing RNAi enzyme complexes. Cell 123:607-620.
25. Mattson SN, Crocker N, Nguyen TT (2011) Fetal alcohol spectrum disorders: neuropsychological and behavioral features. Neuropsychol Rev 21:81-101.
26. May PA, Blankenship J, Marais AS, Gossage JP, Kalberg WO, Barnard R, De Vries M, Robinson LK, Adnams CM, Buckley D, Manning M, Jones KL, Parry C, Hoyme HE, Seedat S (2013) Approaching the prevalence of the full spectrum of fetal alcohol spectrum disorders in a South African population-based study. Alcohol Clin Exp Res 37:818-830.
27. May PA, Gossage JP, Kalberg WO, Robinson LK, Buckley D, Manning M, Hoyme HE (2009) Prevalence and epidemiologic characteristics of FASD from various research methods with an emphasis on recent in-school studies. Dev Disabil Res Rev 15:176-192.
28. Mayor-Lynn K, Toloubeydokhti T, Cruz AC, Chegini N (2011) Expression profile of microRNAs and mRNAs in human placentas from pregnancies complicated by preeclampsia and preterm labor. Reprod Sci 18:46-56.
29. Mitchell PS, Parkin RK, Kroh EM, Fritz BR, Wyman SK, Pogosova-Agadjanyan EL, Peterson A, Noteboom J, O'Briant KC, Allen A, Lin DW, Urban N, Drescher CW, Knudsen BS, Stirewalt DL, Gentleman R, Vessella RL, Nelson PS, Martin DB, Tewari M (2008) Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci USA 105:10513-10518.
30. Montecalvo A, Larregina AT, Shufesky WJ, Stolz DB, Sullivan ML, Karlsson JM, Baty CJ, Gibson GA, Erdos G, Wang Z, Milosevic J, Tkacheva OA, Divito SJ, Jordan R, Lyons-Weiler J, Watkins SC, Morelli AE (2012) Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes. Blood 119:756-766.
31. Pappalardo-Carter DL, Balaraman S, Sathyan P, Carter ES, Chen WJ, Miranda RC (2013) Suppression and epigenetic regulation of MiR-9 contributes to ethanol teratology: evidence from zebrafish and murine fetal neural stem cell models. Alcohol Clin Exp Res 37:1657-1667.
32. Perrotta S, Borriello A, Scaloni A, De Franceschi L, Brunati AM, Turrini F, Nigro V, del Giudice EM, Nobili B, Conte ML, Rossi F, Iolascon A, Donella-Deana A, Zappia V, Poggi V, Anong W, Low P, Mohandas N, Della Ragione F (2005) The N-terminal 11 amino acids of human erythrocyte band 3 are critical for aldolase binding and protein phosphorylation: implications for band 3 function. Blood 106:4359-4366.
33. Peterson J, Kirchner HL, Xue W, Minnes S, Singer LT, Bearer CF (2008) Fatty acid ethyl esters in meconium are associated with poorer neurodevelopmental outcomes to two years of age. J Pediatr 152:788-792.
34. Pietrzykowski AZ, Friesen RM, Martin GE, Puig SI, Nowak CL, Wynne PM, Siegelmann HT, Treistman SN (2008) Posttranscriptional regulation of BK channel splice variant stability by miR-9 underlies neuroadaptation to alcohol. Neuron 59:274-287.
35. Popova S, Lange S, Burd L, Rehm J (2012) Health care burden and cost associated with fetal alcohol syndrome: based on official Canadian data. PLoS One 7:e43024.
36. Pritchard CC, Kroh E, Wood B, Arroyo JD, Dougherty KJ, Miyaji MM, Tait JF, Tewari M (2012) Blood cell origin of circulating microRNAs: a cautionary note for cancer biomarker studies. Cancer Prev Res (Phila) 5:492-497.
37. Ramadoss J, Lunde ER, Pina KB, Chen WJ, Cudd TA (2007) All three trimester binge alcohol exposure causes fetal cerebellar purkinje cell loss in the presence of maternal hypercapnea, acidemia, and normoxemia: ovine model. Alcohol Clin Exp Res 31:1252-1258.
38. Redell JB, Moore AN, Ward NH 3rd, Hergenroeder GW, Dash PK (2010) Human traumatic brain injury alters plasma microRNA levels. J Neurotrauma 27:2147-2156.
39. Sathyan P, Golden HB, Miranda RC (2007) Competing interactions between micro-RNAs determine neural progenitor survival and proliferation after ethanol exposure: evidence from an ex vivo model of the fetal cerebral cortical neuroepithelium. J Neurosci 27:8546-8557.
40. Sawant OB, Ramadoss J, Hogan HA, Washburn SE (2013) The role of acidemia in maternal binge alcohol-induced alterations in fetal bone functional properties. Alcohol Clin Exp Res 37:1476-1482.
41. Shibata M, Nakao H, Kiyonari H, Abe T, Aizawa S (2011) MicroRNA-9 regulates neurogenesis in mouse telencephalon by targeting multiple transcription factors. J Neurosci 31:3407-3422.
42. Shukla PK, Sittig LJ, Ullmann TM, Redei EE (2011) Candidate placental biomarkers for intrauterine alcohol exposure. Alcohol Clin Exp Res 35:559-565.
43. Siegel SR, Mackenzie J, Chaplin G, Jablonski NG, Griffiths L (2012) Circulating microRNAs involved in multiple sclerosis. Mol Biol Rep 39:6219-6225.
44. Tal TL, Franzosa JA, Tilton SC, Philbrick KA, Iwaniec UT, Turner RT, Waters KM, Tanguay RL (2012) MicroRNAs control neurobehavioral development and function in zebrafish. FASEB J 26:1452-1461.
45. Vickers KC, Palmisano BT, Shoucri BM, Shamburek RD, Remaley AT (2011) MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat Cell Biol 13:423-433.
46. Wang LL, Zhang Z, Li Q, Yang R, Pei X, Xu Y, Wang J, Zhou SF, Li Y (2009) Ethanol exposure induces differential microRNA and target gene expression and teratogenic effects which can be suppressed by folic acid supplementation. Hum Reprod 24:562-579.
47. Wei J, Shi Y, Zheng L, Zhou B, Inose H, Wang J, Guo XE, Grosschedl R, Karsenty G (2012) miR-34s inhibit osteoblast proliferation and differentiation in the mouse by targeting SATB2. J Cell Biol 197:509-521.
48. Yang JS, Phillips MD, Betel D, Mu P, Ventura A, Siepel AC, Chen KC, Lai EC (2011) Widespread regulatory activity of vertebrate microRNA* species. RNA 17:312-326.
49. Zhang S, Zhao F, Wei C, Sheng X, Ren H, Xu L, Lu J, Liu J, Zhang L, Du L (2013) Identification and characterization of the miRNA transcriptome of Ovis aries. PLoS One 8:e58905.
50. Zhang Y, Liu D, Chen X, Li J, Li L, Bian Z, Sun F, Lu J, Yin Y, Cai X, Sun Q, Wang K, Ba Y, Wang Q, Wang D, Yang J, Liu P, Xu T, Yan Q, Zhang J, Zen K, Zhang CY (2010) Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol Cell 39:133-144.
51. Zheng H, Zeng Y, Zhang X, Chu J, Loh HH, Law PY (2010) mu-Opioid receptor agonists differentially regulate the expression of miR-190 and NeuroD. Mol Pharmacol 77:102-109.
52. Zijlstra WG, Buursma A (1997) Spectrophotometry of hemoglobin: absorption spectra of bovine oxyhemoglobin, deoxyhemoglobin, carboxyhemoglobin, and methemoglobin. Comp Biochem Physiol B: Biochem Mol Biol 118:743-749.