MicroRNAs control neurobehavioral development and function in zebrafish

FASEB Journal

Volumn 26, Issue 4, 2012, Pages 1452-1461

  Tal, Tamara L ^a,c   Franzosa, Jill A ^a   Tilton, Susan C ^b   Philbrick, Kenneth A ^a   Iwaniec, Urszula T ^a   Turner, Russell T ^a   Waters, Katrina M ^b   Tanguay, Robert L ^a  

^a OREGON STATE UNIVERSITY   (United States)

^b PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

^c U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

Author keywords

miR 153; miR 9; Skeletal development

Indexed keywords

ALCOHOL; MESSENGER RNA; MICRORNA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL SURVIVAL; CONTROLLED STUDY; CRANIOFACIAL DEVELOPMENT; EMBRYO; GENE EXPRESSION PROFILING; GENE REPRESSION; HUMAN; IN VIVO STUDY; JUVENILE; LARVA; MORPHOGENESIS; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SWIMMING; VERTEBRATE; ZEBRA FISH;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN; EMBRYO, NONMAMMALIAN; ETHANOL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCKDOWN TECHNIQUES; HUMANS; LARVA; LIGHT; MICRORNAS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ORGANOGENESIS; RNA, MESSENGER; ZEBRAFISH;

DANIO RERIO; VERTEBRATA;

EID: 84860895221     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-194464     Document Type: Article

References (57)

1. Kim, V. N., Han, J., and Siomi, M. C. (2009) Biogenesis of small RNAs in animals. Nat. Rev. Mol. Cell Biol. 10, 126-139
2. Kapsimali, M., Kloosterman, W. P., de Bruijn, E., Rosa, F., Plasterk, R. H., and Wilson, S. W. (2007) MicroRNAs show a wide diversity of expression profiles in the developing and mature central nervous system. Genome Biol. 8, R173
3. Krichevsky, A. M., King, K. S., Donahue, C. P., Khrapko, K., and Kosik, K. S. (2003) A microRNA array reveals extensive regulation of microRNAs during brain development. RNA 9, 1274-1281 (Pubitemid 37151681)
4. Ling, K. H., Brautigan, P. J., Hahn, C. N., Daish, T., Rayner, J. R., Cheah, P. S., Raison, J. M., Piltz, S., Mann, J. R., Mattiske, D. M., Thomas, P. Q., Adelson, D. L., and Scott, H. S. (2011) Deep sequencing analysis of the developing mouse brain reveals a novel microRNA. BMC Genomics 12, 176
5. De Pietri Tonelli, D., Pulvers, J. N., Haffner, C., Murchison, E. P., Hannon, G. J., and Huttner, W. B. (2008) miRNAs are essential for survival and differentiation of newborn neurons but not for expansion of neural progenitors during early neurogenesis in the mouse embryonic neocortex. Development 135, 3911-3921
6. Giraldez, A. J., Cinalli, R. M., Glasner, M. E., Enright, A. J., Thomson, J. M., Baskerville, S., Hammond, S. M., Bartel, D. P., and Schier, A. F. (2005) MicroRNAs regulate brain morphogenesis in zebrafish. Science 308, 833-838 (Pubitemid 40629259)
7. Huang, T., Liu, Y., Huang, M., Zhao, X., and Cheng, L. (2010) Wnt1-cre-mediated conditional loss of Dicer results in malformation of the midbrain and cerebellum and failure of neural crest and dopaminergic differentiation in mice. J. Mol. Cell Biol. 2, 152-163
8. Schaefer, A., O'Carroll, D., Tan, C. L., Hillman, D., Sugimori, M., Llinas, R., and Greengard, P. (2007) Cerebellar neurodegeneration in the absence of microRNAs. J. Exp. Med. 204, 1553-1558 (Pubitemid 47048023)
9. Zehir, A., Hua, L. L., Maska, E. L., Morikawa, Y., and Cserjesi, P. Dicer is required for survival of differentiating neural crest cells. Dev. Biol. 340, 459-467
10. Davis, T. H., Cuellar, T. L., Koch, S. M., Barker, A. J., Harfe, B. D., McManus, M. T., and Ullian, E. M. (2008) Conditional loss of Dicer disrupts cellular and tissue morphogenesis in the cortex and hippocampus. J. Neurosci. 28, 4322-4330
11. Pinter, R., and Hindges, R. (2010) Perturbations of microRNA function in mouse dicer mutants produce retinal defects and lead to aberrant axon pathfinding at the optic chiasm. PLoS One 5, e10021
12. Kimmel, C. B. (1993) Patterning the brain of the zebrafish embryo. Annu. Rev. Neurosci. 16, 707-732
13. Reimers, M. J., Flockton, A. R., and Tanguay, R. L. (2004) Ethanol- and acetaldehyde-mediated developmental toxicity in zebrafish. Neurotoxicol. Teratol. 26, 769-781 (Pubitemid 39296761)
14. Reimers, M. J., La Du, J. K., Periera, C. B., Giovanini, J., and Tanguay, R. L. (2006) Ethanol-dependent toxicity in zebrafish is partially attenuated by antioxidants. Neurotoxicol. Teratol. 28, 497-508 (Pubitemid 44332879)
15. Kocerha, J., Faghihi, M. A., Lopez-Toledano, M. A., Huang, J., Ramsey, A. J., Caron, M. G., Sales, N., Willoughby, D., Elmen, J., Hansen, H. F., Orum, H., Kauppinen, S., Kenny, P. J., and Wahlestedt, C. (2009) MicroRNA-219 modulates NMDA receptor-mediated neurobehavioral dysfunction. Proc. Natl. Acad. Sci. U. S. A. 106, 3507-3512
16. Westerfield, M. (2000) The Zebrafish Book, 4th ed. University of Oregon Press, Eugene, OR, USA
17. Emran, F., Rihel, J., and Dowling, J. E. (2008) A behavioral assay to measure responsiveness of zebrafish to changes in light intensities. J. Vis. Exp. 20, 923
18. MacPhail, R. C., Brooks, J., Hunter, D. L., Padnos, B., Irons, T. D., and Padilla, S. (2009) Locomotion in larval zebrafish: Influence of time of day, lighting and ethanol. Neurotoxicology 30, 52-58
19. Bolstad, B. M., Irizarry, R. A., Astrand, M., and Speed, T. P. (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19, 185-193 (Pubitemid 36181903)
20. Kerr, M. K., Martin, M., and Churchill, G. A. (2000) Analysis of variance for gene expression microarray data. J. Comput. Biol. 7, 819-837
21. Benjamini, Y. a. H., Y (1995) Controlling the false discovery ratea practical and powerful approach to multiple testing. J. R. Stat. Soc. B Met. 57, 289-300
22. Gao, X., Gulari, E., and Zhou, X. (2004) In situ synthesis of oligonucleotide microarrays. Biopolymers 73, 579-596 (Pubitemid 38480705)
23. Edgar, R., Domrachev, M., and Lash, A. E. (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30, 207-210 (Pubitemid 34679544)
24. Saeed, A. I., Sharov, V., White, J., Li, J., Liang, W., Bhagabati, N., Braisted, J., Klapa, M., Currier, T., Thiagarajan, M., Sturn, A., Snuffin, M., Rezantsev, A., Popov, D., Ryltsov, A., Kostukovich, E., Borisovsky, I., Liu, Z., Vinsavich, A., Trush, V., and Quackenbush, J. (2003) TM4: a free, open-source system for microarray data management and analysis. BioTechniques 34, 374-378 (Pubitemid 36184095)
25. Wienholds, E., and Plasterk, R. H. (2005) MicroRNA function in animal development. FEBS Lett. 579, 5911-5922 (Pubitemid 41487106)
26. Delaloy, C., Liu, L., Lee, J. A., Su, H., Shen, F., Yang, G. Y., Young, W. L., Ivey, K. N., and Gao, F. B. (2010) MicroRNA-9 coordinates proliferation and migration of human embryonic stem cell-derived neural progenitors. Cell Stem Cell 6, 323-335
27. Leucht, C., Stigloher, C., Wizenmann, A., Klafke, R., Folchert, A., and Bally-Cuif, L. (2008) MicroRNA-9 directs late organizer activity of the midbrain-hindbrain boundary. Nat. Neurosci. 11, 641-648 (Pubitemid 351748112)
28. Burgess, H. A., and Granato, M. (2007) Modulation of locomotor activity in larval zebrafish during light adaptation. J. Exp. Biol. 210, 2526-2539 (Pubitemid 47235044)
29. Aschoff, J. (1960) Exogenous and endogenous components in circadian rhythms. Cold Spring Harb. Symp. Quant. Biol. 25, 11-28
30. Hagins, W. A., Penn, R. D., and Yoshikami, S. (1970) Dark current and photocurrent in retinal rods. Biophys. J. 10, 380-412
31. Staddon, J. E., MacPhail, R. C., and Padilla, S. (2010) The dynamics of successive induction in larval zebrafish. J. Exp. Anal. Behav. 94, 261-266
32. Rihel, J., Prober, D. A., Arvanites, A., Lam, K., Zimmerman, S., Jang, S., Haggarty, S. J., Kokel, D., Rubin, L. L., Peterson, R. T., and Schier, A. F. (2010) Zebrafish behavioral profiling links drugs to biological targets and rest/wake regulation. Science 327, 348-351
33. Wolman, M., and Granato, M. (2011) Behavioral genetics in larval zebrafish-learning from the young. [E-pub ahead of print] Dev. Neurobiol. doi: 10.1002/dneu.20872
34. Echevarria, D. J., Toms, C. N., and Jouandot, D. J. (2011) Alcohol-induced behavior change in zebrafish models. Rev. Neurosci. 22, 85-93
35. Irons, T. D., MacPhail, R. C., Hunter, D. L., and Padilla, S. (2009) Acute neuroactive drug exposures alter locomotor activity in larval zebrafish. Neurotoxicol. Teratol. 32, 84-90
36. Ali, S., Champagne, D. L., Alia, A., and Richardson, M. K. (2011) Large-scale analysis of acute ethanol exposure in zebrafish development: a critical time window and resilience. PLoS One 6, e20037
37. Fernandes, Y., and Gerlai, R. (2009) Long-term behavioral changes in response to early developmental exposure to ethanol in zebrafish. Alcohol Clin. Exp. Res. 33, 601-609
38. Blaser, R. E., Koid, A., and Poliner, R. M. Context-dependent sensitization to ethanol in zebrafish (Danio rerio). Pharmacol. Biochem. Behav. 95, 278-284
39. Sathyan, P., Golden, H. B., and Miranda, R. C. (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 (Pubitemid 47254255)
40. Pietrzykowski, A. Z., Friesen, R. M., Martin, G. E., Puig, S. I., Nowak, C. L., Wynne, P. M., Siegelmann, H. T., and Treistman, S. N. (2008) Posttranscriptional regulation of BK channel splice variant stability by miR-9 underlies neuroadaptation to alcohol. Neuron 59, 274-287 (Pubitemid 352033687)
41. Treistman, S. N., and Martin, G. E. (2009) BK channels: mediators and models for alcohol tolerance. Trends Neurosci. 32, 629-637
42. Cowmeadow, R. B., Krishnan, H. R., and Atkinson, N. S. (2005) The slowpoke gene is necessary for rapid ethanol tolerance in Drosophila. Alcohol Clin. Exp. Res. 29, 1777-1786 (Pubitemid 41579127)
43. Davies, A. G., Pierce-Shimomura, J. T., Kim, H., VanHoven, M. K., Thiele, T. R., Bonci, A., Bargmann, C. I., and McIntire, S. L. (2003) A central role of the BK potassium channel in behavioral responses to ethanol in C. elegans. Cell 115, 655-666 (Pubitemid 38030295)
44. Gao, F. B. (2010) Context-dependent functions of specific microRNAs in neuronal development. Neural. Dev. 5, 25
45. Lagos-Quintana, M., Rauhut, R., Yalcin, A., Meyer, J., Lendeckel, W., and Tuschl, T. (2002) Identification of tissue-specific microRNAs from mouse. Curr. Biol. 12, 735-739 (Pubitemid 34455427)
46. Packer, A. N., Xing, Y., Harper, S. Q., Jones, L., and Davidson, B. L. (2008) The bifunctional microRNA miR-9/miR-9*regulates REST and CoREST and is downregulated in Huntington's disease. J. Neurosci. 28, 14341-14346
47. Cogswell, J. P., Ward, J., Taylor, I. A., Waters, M., Shi, Y., Cannon, B., Kelnar, K., Kemppainen, J., Brown, D., Chen, C., Prinjha, R. K., Richardson, J. C., Saunders, A. M., Roses, A. D., and Richards, C. A. (2008) Identification of miRNA changes in Alzheimer's disease brain and CSF yields putative biomarkers and insights into disease pathways. J. Alzheimers Dis. 14, 27-41 (Pubitemid 352039013)
48. Haramati, S., Chapnik, E., Sztainberg, Y., Eilam, R., Zwang, R., Gershoni, N., McGlinn, E., Heiser, P. W., Wills, A. M., Wirguin, I., Rubin, L. L., Misawa, H., Tabin, C. J., Brown, R., Jr., Chen, A., and Hornstein, E. (2010) miRNA malfunction causes spinal motor neuron disease. Proc. Natl. Acad. Sci. U. S. A. 107, 13111-13116
49. Bilotta, J., Barnett, J. A., Hancock, L., and Saszik, S. (2004) Ethanol exposure alters zebrafish development: a novel model of fetal alcohol syndrome. Neurotoxicol. Teratol. 26, 737-743 (Pubitemid 39296758)
50. Carvan, M. J., 3rd, Loucks, E., Weber, D. N., and Williams, F. E. (2004) Ethanol effects on the developing zebrafish: neurobehavior and skeletal morphogenesis. Neurotoxicol. Teratol. 26, 757-768 (Pubitemid 39296760)
51. Marrs, J. A., Clendenon, S. G., Ratcliffe, D. R., Fielding, S. M., Liu, Q., and Bosron, W. F. (2010) Zebrafish fetal alcohol syndrome model: effects of ethanol are rescued by retinoic acid supplement. Alcohol 44, 707-715
52. U.S. Centers for Disease Control and Prevention (2009) Alcohol use among pregnant and nonpregnant women of childbearing age - United States, 1991-2005. MMWR 58, 529-532
53. Hoyme, H. E., May, P. A., Kalberg, W. O., Kodituwakku, P., Gossage, J. P., Trujillo, P. M., Buckley, D. G., Miller, J. H., Aragon, A. S., Khaole, N., Viljoen, D. L., Jones, K. L., and Robinson, L. K. (2005) A practical clinical approach to diagnosis of fetal alcohol spectrum disorders: clarification of the 1996 institute of medicine criteria. Pediatrics 115, 39-47 (Pubitemid 43046280)
54. Hassan, M. Q., Gordon, J. A., Beloti, M. M., Croce, C. M., van Wijnen, A. J., Stein, J. L., Stein, G. S., and Lian, J. B. (2010) A network connecting Runx2, SATB2, and the miR-23a∼27a∼24-2 cluster regulates the osteoblast differentiation program. Proc. Natl. Acad. Sci. U. S. A. 107, 19879-19884
55. Inose, H., Ochi, H., Kimura, A., Fujita, K., Xu, R., Sato, S., Iwasaki, M., Sunamura, S., Takeuchi, Y., Fukumoto, S., Saito, K., Nakamura, T., Siomi, H., Ito, H., Arai, Y., Shinomiya, K., and Takeda, S. (2009) A microRNA regulatory mechanism of osteoblast differentiation. Proc. Natl. Acad. Sci. U. S. A. 106, 20794-20799
56. Li, Z., Hassan, M. Q., Volinia, S., van Wijnen, A. J., Stein, J. L., Croce, C. M., Lian, J. B., and Stein, G. S. (2008) A microRNA signature for a BMP2-induced osteoblast lineage commitment program. Proc. Natl. Acad. Sci. U. S. A. 105, 13906-13911
57. Maurel, D. B., Boisseau, N., Benhamou, C. L., and Jaffre, C. (2012) Alcohol and bone: review of dose effects and mechanisms. Osteoporos. Int. 23, 1-16