MiR-125b protects against ethanol-induced apoptosis in neural crest cells and mouse embryos by targeting Bak 1 and PUMA

Experimental Neurology

Volumn 271, Issue , 2015, Pages 104-111

  Chen, Xiaopan ^a,b   Liu, Jie ^a,b   Feng, Wen ke ^a,b   Wu, Xiaoyang ^c   Chen, Shao yu ^a,b  

^a University of Louisville School of Medicine   (United States)

^b UNIVERSITY OF LOUISVILLE   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

Apoptosis; Bak1; Fetal alcohol spectrum disorders; MiR 125b; Neural crest cells; P53

Indexed keywords

ALCOHOL; BAK1 PROTEIN; CASPASE 3; MICRORNA 125B; PROTEIN BAK; PUMA PROTEIN; UNCLASSIFIED DRUG; APOPTOSIS REGULATORY PROTEIN; BAK1 PROTEIN, MOUSE; CENTRAL DEPRESSANT AGENT; MICRORNA; MIRN125 MICRORNA, MOUSE; PUMA PROTEIN, MOUSE; TUMOR SUPPRESSOR PROTEIN;

ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYOTOXICITY; GROWTH RETARDATION; MOUSE; MOUSE EMBRYO; NEURAL CREST CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION; ANIMAL; ANIMAL EMBRYO; C57BL MOUSE; CELL CULTURE; CELL SURVIVAL; CHEMICALLY INDUCED; DOSE RESPONSE; DRUG EFFECTS; FEMALE; GENETICS; METABOLISM; NEURAL CREST; ORGAN CULTURE TECHNIQUE; PREGNANCY; PRENATAL EXPOSURE;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BCL-2 HOMOLOGOUS ANTAGONIST-KILLER PROTEIN; CASPASE 3; CELL SURVIVAL; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM DEPRESSANTS; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYO, MAMMALIAN; ETHANOL; FEMALE; MICE; MICE, INBRED C57BL; MICRORNAS; NEURAL CREST; ORGAN CULTURE TECHNIQUES; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; TUMOR SUPPRESSOR PROTEINS; UP-REGULATION;

EID: 84930212592     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2015.04.026     Document Type: Article

References (48)

1. Augustine K. Antisense approaches for investigating mechanisms of abnormal development. Mutat. Res. 1997, 396:175-193. 10.1016/S0027-5107(97)00183-8.
2. Augustine K., Liu E.T., Sadler T.W. Antisense attenuation of Wnt-1 and Wnt-3a expression in whole embryo culture reveals roles for these genes in craniofacial, spinal cord, and cardiac morphogenesis. Dev. Genet. 1993, 14:500-520. 10.1002/dvg.1020140611.
3. Baek D., Villen J., Shin C., Camargo F.D., Gygi S.P., Bartel D.P. The impact of microRNAs on protein output. Nature 2008, 455:64-71. 10.1038/nature07242.
4. Bak M., Silahtaroglu A., Moller M., Christensen M., Rath M.F., Skryabin B., Tommerup N., Kauppinen S. MicroRNA expression in the adult mouse central nervous system. RNA 2008, 14:432-444. 10.1261/rna.783108.
5. Bartel D.P. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233.
6. Bavik C., Ward S.J., Chambon P. Developmental abnormalities in cultured mouse embryos deprived of retinoic by inhibition of yolk-sac retinol binding protein synthesis. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:3110-3114. 10.1073/pnas.93.7.3110.
7. Burd L. Fetal alcohol syndrome. Am. J. Med. Genet. C: Semin. Med. Genet. 2004, 127C:1-2. 10.1002/ajmg.c.30009.
8. Calegari F., Haubensak W., Yang D., Huttner W.B., Buchholz F. Tissue-specific RNA interference in postimplantation mouse embryos with endoribonuclease-prepared short interfering RNA. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:14236-14240. 10.1073/pnas.192559699.
9. Cartwright M.M., Smith S.M. 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, 19:378-386. 10.1111/j.1530-0277.1995.tb01519.x.
10. Chan J.A., Krichevsky A.M., Kosik K.S. MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res. 2005, 65:6029-6033. 10.1158/0008-5472.CAN-05-0137.
11. Chen S.Y., Sulik K.K. Free radicals and ethanol-induced cytotoxicity in neural crest cells. Alcohol. Clin. Exp. Res. 1996, 20:1071-1076. 10.1111/j.1530-0277.
12. Chen S.Y., Wilkemeyer M.F., Sulik K.K., Charness M.E. Octanol antagonism of ethanol teratogenesis. FASEB J. 2001, 15:1649-1651. 10.1096/fj.00-0862fje.
13. Chen X., Liu J., Chen S.Y. Sulforaphane protects against ethanol-induced oxidative stress and apoptosis in neural crest cells by the induction of Nrf2-mediated antioxidant response. Br. J. Pharmacol. 2013, 169:437-448. 10.1111/bph.12133.
14. Dong J., Sulik K.K., Chen S.Y. Nrf2-mediated transcriptional induction of antioxidant response in mouse embryos exposed to ethanol in vivo: implications for the prevention of fetal alcohol spectrum disorders. Antioxid. Redox Signal. 2008, 10:2023-2033. 10.1089/ars.2007.2019.
15. Dong J., Yan D., Chen S.Y. Stabilization of Nrf2 protein by D3T provides protection against ethanol-induced apoptosis in PC12 cells. PLoS One 2011, 6:e16845. 10.1371/journal.pone.0016845.
16. Dunty W.C., Chen S.Y., Zucker R.M., Dehart D.B., Sulik K.K. Selective vulnerability of embryonic cell populations to ethanol-induced apoptosis: implications for alcohol-related birth defects and neurodevelopmental disorder. Alcohol. Clin. Exp. Res. 2001, 25:1523-1535. 10.1111/j.1530-0277.2001.tb02156.x.
17. Flynt A.S., Lai E.C. Biological principles of microRNA-mediated regulation: shared themes amid diversity. Nat. Rev. Genet. 2008, 9:831-842. 10.1038/nrg2455.
18. Fujinaga M., Mazze R.I., Baden J.M., Fantel A.G., Shepard T.H. Rat whole embryo culture: an in vitro model for testing nitrous oxide teratogenicity. Anesthesiology 1988, 69:401-404. (doi: 0000542-198809000-00019).
19. Gundogan F., Elwood G., Mark P., Feijoo A., Longato L., Tong M., de la Monte S.M. Ethanol-induced oxidative stress and mitochondrial dysfunction in rat placenta: relevance to pregnancy loss. Alcohol. Clin. Exp. Res. 2010, 34:415-423. 10.1111/j.1530-0277.2009.01106.x.
20. Hall B.K. The neural crest and neural crest cells: discovery and significance for theories of embryonic organization. J. Biosci. 2008, 33:781-793. 10.1007/s12038-008-0098-4.
21. Hartig P.C., Hunter E.S. Gene delivery to the neurulating embryo during culture. Teratology 1998, 58:103-112. 10.1002/(SICI)1096-9926(199809/10)58:3/4<103::AID-TERA6>3.0.CO;2-O.
22. Ikonomidou C., Bittigau P., Ishimaru M.J., Wozniak D.F., Koch C., Genz K., Price M.T., Stefovska V., Horster F., Tenkova T., Dikranian K., Olney J.W. Ethanol-induced apoptotic neurodegeneration and fetal alcohol syndrome. Science 2000, 287:1056-1060. 10.1126/science.287.5455.1056.
23. Kim H., Rafiuddin-Shah M., Tu H.C., Jeffers J.R., Zambetti G.P., Hsieh J.J., Cheng E.H. Hierarchical regulation of mitochondrion-dependent apoptosis by BCL-2 subfamilies. Nat. Cell Biol. 2006, 8:1348-1358. 10.1038/ncb1499.
24. Kotch L.E., Sulik K.K. Patterns of ethanol-induced cell death in the developing nervous system of mice; neural fold states through the time of anterior neural tube closure. Int. J. Dev. Neurosci. 1992, 10:273-279. 10.1016/0736-5748(92)90016-S.
25. Kotch L.E., Chen S.Y., Sulik K.K. Ethanol-induced teratogenesis: free radical damage as a possible mechanism. Teratology 1995, 52:128-136. 10.1002/tera.1420520304.
26. Kuwana T., Bouchier-Hayes L., Chipuk J.E., Bonzon C., Sullivan B.A., Green D.R., Newmeyer D.D. BH3 domains of BH3-only proteins differentially regulate Bax-mediated mitochondrial membrane permeabilization both directly and indirectly. Mol. Cell 2005, 17:525-535. 10.1016/j.molcel.2005.02.003.
27. Lagos-Quintana M., Rauhut R., Yalcin A., Meyer J., Lendeckel W., Tuschl T. Identification of tissue-specific microRNAs from mouse. Curr. Biol. 2002, 12:735-739. 10.1016/S0960-9822(02)00809-6.
28. Le M.T., Teh C., Shyh-Chang N., Xie H., Zhou B., Korzh V., Lodish H.F., Lim B. MicroRNA-125b is a novel negative regulator of p53. Genes Dev. 2009, 23:862-876. 10.1101/gad.1767609.
29. Le M.T., Shyh-Chang N., Khaw S.L., Chin L., Teh C., Tay J., O'Day E., Korzh V., Yang H., Lal A., Lieberman J., Lodish H.F., Lim B. Conserved regulation of p53 network dosage by microRNA-125b occurs through evolving miRNA-target gene pairs. PLoS Genet. 2011, 7:e1002242. 10.1371/journal.pgen.1002242.
30. Lee Y.S., Kim H.K., Chung S., Kim K.S., Dutta A. Depletion of human micro-RNA miR-125b reveals that it is critical for the proliferation of differentiated cells but not for the down-regulation of putative targets during differentiation. J. Biol. Chem. 2005, 280:16635-16641. 10.1074/jbc.M412247200.
31. Lin K.Y., Zhang X.J., Feng D.D., Zhang H., Zeng C.W., Han B.W., Zhou A.D., Qu L.H., Xu L., Chen Y.Q. miR-125b, a target of CDX2, regulates cell differentiation through repression of the core binding factor in hematopoietic malignancies. J. Biol. Chem. 2011, 286:38253-38263. 10.1074/jbc.M111.269670.
32. Nelson P.T., Baldwin D.A., Kloosterman W.P., Kauppinen S., Plasterk R.H., Mourelatos Z. RAKE and LNA-ISH reveal microRNA expression and localization in archival human brain. RNA 2006, 12:187-191.
33. Osumi N., Inoue T. Gene transfer into cultured mammalian embryos by electroporation. Methods 2001, 24:35-42. 10.1007/978-1-4939-2459-2_11.
34. Pietrzykowski A.Z., Friesen R.M., Martin G.E., Puig S.I., Nowak C.L., Wynne P.M., Siegelmann H.T., Treistman S.N. Posttranscriptional regulation of BK channel splice variant stability by miR-9 underlies neuroadaptation to alcohol. Neuron 2008, 59:274-287. 10.1016/j.neuron.2008.05.032.
35. Qi Y., Zhang M., Li H., Frank J.A., Dai L., Liu H., Chen G. MicroRNA-29b regulates ethanol-induced neuronal apoptosis in the developing cerebellum through SP1/RAX/PKR cascade. J. Biol. Chem. 2014, 289:10201-10210. 10.1074/jbc.M113.535195.
36. Raver-Shapira N., Marciano E., Meiri E., Spector Y., Rosenfeld N., Moskovits N., Bentwich Z., Oren M. Transcriptional activation of miR-34a contributes to p53-mediated apoptosis. Mol. Cell 2007, 26:731-743. 10.1016/j.molcel.2007.05.017.
37. Sadler T.W., Horton W.E., Warner C.W. Whole embryo culture: a screening technique for teratogens?. Teratog. Carcinog. Mutagen. 1982, 2:243-253. 10.1002/1520-6866(1990)2:3/4<243::AID-TCM1770020306>3.0.CO;2-U.
38. Sathyan P., Golden H.B., Miranda R.C. 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. 2007, 27:8546-8557. 10.1523/JNEUROSCI.1269-07.2007.
39. Schulman B.R., Esquela-Kerscher A., Slack F.J. Reciprocal expression of lin-41 and the microRNAs let-7 and mir-125 during mouse embryogenesis. Dev. Dyn. 2005, 234:1046-1054. 10.1002/dvdy.20599.
40. Sulik K.K., Johnston M.C., Webb M.A. Fetal alcohol syndrome: embryogenesis in a mouse model. Science 1981, 214:936-938. 10.1126/science.6795717.
41. Swarbrick A., Woods S.L., Shaw A., Balakrishnan A., Phua Y., Nguyen A., Chanthery Y., Lim L., Ashton L.J., Judson R.L., Huskey N., Blelloch R., Haber M., Norris M.D., Lengyel P., Hackett C.S., Preiss T., Chetcuti A., Sullivan C.S., Marcusson E.G., Weiss W., L'Etoile N., Goga A. miR-380-5p represses p53 to control cellular survival and is associated with poor outcome in MYCN-amplified neuroblastoma. Nat. Med. 2010, 16:1134-1140. 10.1038/nm.2227.
42. Tsang W.P., Kwok T.T. Let-7a microRNA suppresses therapeutics-induced cancer cell death by targeting caspase-3. Apoptosis 2008, 13:1215-1222. 10.1007/s10495-008-0256-z.
43. Walker J.C., Harland R.M. microRNA-24a is required to repress apoptosis in the developing neural retina. Genes Dev. 2009, 23:1046-1051. 10.1101/gad.1777709.
44. Wei M.C., Zong W.X., Cheng E.H., Lindsten T., Panoutsakopoulou V., Ross A.J., Roth K.A., MacGregor G.R., Thompson C.B., Korsmeyer S.J. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 2001, 292:727-730. 10.1126/science.1059108.
45. Xia H.F., He T.Z., Liu C.M., Cui Y., Song P.P., Jin X.H., Ma X. MiR-125b expression affects the proliferation and apoptosis of human glioma cells by targeting Bmf. Cell. Physiol. Biochem. 2009, 23:347-358. 10.1159/000218181.
46. Yadav S., Pandey A., Shukla A., Talwelkar S.S., Kumar A., Pant A.B., Parmar D. miR-497 and miR-302b regulate ethanol-induced neuronal cell death through BCL2 protein and cyclin D2. J. Biol. Chem. 2011, 286:37347-37357. 10.1074/jbc.M111.235531.
47. Yamakuchi M., Ferlito M., Lowenstein C.J. miR-34a repression of SIRT1 regulates apoptosis. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:13421-13426. 10.1073/pnas.0801613105.
48. Zhao J.J., Sun D.G., Wang J., Liu S.R., Zhang C.Y., Zhu M.X., Ma X. Retinoic acid downregulates microRNAs to induce abnormal development of spinal cord in spina bifida rat model. Childs Nerv. Syst. 2008, 24:485-492. 10.1007/s00381-007-0520-5.