MiRNA expression profiling in a human stem cell-based model as a tool for developmental neurotoxicity testing

Cell Biology and Toxicology

Volumn 29, Issue 4, 2013, Pages 239-257

  Pallocca, Giorgia ^a   Fabbri, Marco ^a,b   Sacco, Maria Grazia ^a   Gribaldo, Laura ^a   Pamies, David ^a   Laurenza, Incoronata ^a   Bal Price, Anna ^a  

^a JOINT RESEARCH CENTRE   (Italy)

^b UNIVERSITY OF INSUBRIA   (Italy)

Author keywords

Developmental neurotoxicity; miRNA expression profiling; Pathways of toxicity

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; AMPA RECEPTOR; BETA TUBULIN; BIOLOGICAL MARKER; METHYLMERCURIC CHLORIDE; MICRORNA; MICRORNA 125B; MICRORNA 132; MICRORNA 141; MICRORNA 196B; MICRORNA 302B; MICRORNA 367; MICRORNA 372; MICRORNA LET 7; MICROTUBULE ASSOCIATED PROTEIN 2; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; RETINOIC ACID; SYNAPTOPHYSIN; TAU PROTEIN; TUBULIN BETA3; UNCLASSIFIED DRUG;

ARTICLE; CARCINOMA CELL; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; GLIA CELL; HUMAN; HUMAN CELL; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NEUROTOXICITY; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TOXICITY TESTING; TRANSCRIPTOMICS; UPREGULATION;

ANTINEOPLASTIC AGENTS; CELL DIFFERENTIATION; CELL LINE; GENE EXPRESSION PROFILING; GENETIC MARKERS; HUMANS; METHYLMERCURY COMPOUNDS; MICRORNAS; NEOPLASTIC STEM CELLS; NEUROGLIA; NEURONS; PLURIPOTENT STEM CELLS; TRETINOIN;

EID: 84883306186     PISSN: 07422091     EISSN: 15736822     Source Type: Journal    
DOI: 10.1007/s10565-013-9250-5     Document Type: Article

References (84)

1. Abbott AL, Alvarez-Saavedra E, Miska EA, Lau NC, Bartel DP, Horvitz HR, et al. The let-7 microRNA family members mir-48, mir-84, and mir-241 function together to regulate developmental timing in Caenorhabditis elegans. Dev Cell. 2005;9:403-14.
2. Amiel J, de Pontual L, Henrion-Caude A. miRNA, development and disease. Adv Genet. 2012;80:1-36.
3. Barco A, Alarcon JM, Kandel ER. Expression of constitutively active CREB protein facilitates the late phase of long-term potentiation by enhancing synaptic capture. Cell. 2002;108(5):689-703.
4. Barroso-del Jesus A, Romero-López C, Lucena-Aguilar G, Melen GJ, Sanchez L, Ligero G, et al. Embryonic stem cell-specific miR302-367 cluster: human gene structure and functional characterization of its core promoter. Mol Cell Biol. 2008;28(21):6609-19.
5. Braceen CP, Gregory PA, Kolesnikoff N, Bert AG, Wang J, Shannon MF, et al. A double-negative feedback loop between ZEB1-SIP1 and the microRNA-200 family regulates epithelial-mesenchymal transition. Cancer Res. 2008;68(19):7846-54.
6. Burbacher TM, Rodier PM, Weiss B. Methylmercury developmental neurotoxicity: a comparison of effects in humans and animals. Neurotoxicol. Teratol. 1990;12:191-202.
7. Buzanska L, Sypecka J, Nerini-Molteni S, Compagnoni A, Hogberg HT, del Torchio R, et al. A human stem cell-based model for identifying adverse effects of organic and inorganic chemicals on the developing nervous system. Stem Cells. 2009;27(10):2591-601.
8. Cao X, Pfaff SL, Gage FH. A functional study of miR-124 in the developing neural tube. Genes Dev. 2007;21(5):531-6.
9. Ceccatelli S, Daré E, Moors M. Methylmercury-induced neurotoxicity and apoptosis. Chem Biol Interact. 2010;188(2):301-8.
10. Chotard C, Leung W, Salecker I. Glial cells missing and gcm2 cell autonomously regulate both glial and neuronal development in the visual system of Drosophila. Neuron. 2005;48(2):237-51.
11. Christensen M, Schratt GM. microRNA involvement in developmental and functional aspects of the nervous system and in neurological diseases. Neurosci Lett. 2009;466(2):55-62.
12. Claudio L, Kwa WC, Russell AL, Wallinga D. Testing methods for developmental neurotoxicity of environmental chemicals. Toxicol Appl Pharmacol. 2000;164:1-14.
13. Cochella L, Hobert O. Embryonic priming of a miRNA locus predetermines postmitotic neuronal left/right asymmetry in C. elegans. Cell. 2012;151(6):1229-42.
14. De Pietri Tonelli D, Pulvers JN, Haffner C, Murchison EP, Hannon GJ, Huttner WB. 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. 2008;135(23):3911-21.
15. Dolbec J, Mergler D, Sousa Passos CJ, Sousa dM, Lebel J. Methylmercury exposure affects motor performance of a riverine population of the Tapajos River, Brazilian Amazon. Int Arch Occup Environ Health. 2000;73:195-203.
16. Dougan ST, Warga RM, Kane DA, Schier AF, Talbot WS. The role of the zebrafish nodal-related genes squint and cyclops in patterning of mesendoderm. Development. 2003;130(9):1837-51.
17. Dvinge H, Bertone P. HTqPCR: high-throughput analysis and visualization of quantitative real-time PCR data in R. Bioinformatics. 2009;25:3325-6.
18. Eriksson P. Developmental neurotoxicity of environmental agents in the neonate. Neurotoxicology. 1997;18:719-26.
19. Feng W, Feng Y. MicroRNAs in neural cell development and brain diseases. Sci China Life Sci. 2011;54(12):1103-12.
20. Fishwick KJ, Li RA, Halley P, Deng P, Storey KG. Initiation of neuronal differentiation requires PI3-kinase/TOR signalling in the vertebrate neural tube. Dev Biol. 2010;338(2):215-25.
21. Fox DA, Grandjean P, de Groot D, Paule MG. Developmental origins of adult diseases and neurotoxicity: epidemiological and experimental studies. Neurotoxicology. 2012;33(4):810-6.
22. Friedman Y, Naamati G, Linial M. MiRror: a combinatorial analysis web tool for ensembles of microRNAs and their targets. Bioinformatics. 2010;26(15):1920-1.
23. Gao FB. Context-dependent functions of specific microRNAs in neuronal development. Neural Dev. 2010;5:25. doi: 10.1186/1749-8104-5-25.
24. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 2004;5(10):R80.
25. Grandjean P, Landrigan PJ. Developmental neurotoxicity of industrial chemicals. Lancet. 2006;368(9553):2167-78.
26. Grandjean P, Weihe P, White RF, Debes F, Araki S, Yokoyama K, et al. Cognitive deficit in 7-year-old children with prenatal exposure to methylmercury. Neurotoxicol Teratol. 1997;19:417-28.
27. Harrill JA, Freudenrich TM, Robinette BL, Mundy WR. Comparative sensitivity of human and rat neural cultures to chemical-induced inhibition of neurite outgrowth. Toxicol Appl Pharmacol. 2011;256(3):268-80.
28. He X, Yan YL, Eberhart JK, Herpin A, Wagner TU, Schartl M, et al. miR-196 regulates axial patterning and pectoral appendage initiation. Dev Biol. 2011;357(2):463-77.
29. Hogberg HT, Kinsner-Ovaskainen A, Hartung T, Coecke S, Bal-Price AK. Gene expression as a sensitive endpoint to evaluate cell differentiation and maturation of the developing central nervous system in primary cultures of rat cerebellar granule cells (CGCs) exposed to pesticides. Toxicol Appl Pharmacol. 2009;235:268-86.
30. Hogberg HT, Kinsner-Ovaskainen A, Coecke S, Hartung T, Bal-Price AK. mRNA expression is a relevant tool to identify developmental neurotoxicants using an in vitro approach. Toxicol Sci. 2010;113:95-115.
31. Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4:44-57.
32. Kanehisa M, Goto S, Furumichi M, Tanabe M, Hirakawa M. KEGG for representation and analysis of molecular networks involving diseases and drugs. Nucleic Acids Res. 2010;38(Database issue):D355-60.
33. Kaur P, Armugam A, Jeyaseelan K. MicroRNAs in Neurotoxicity. J Toxicol. 2012; 870150
34. Kawahara H, Imai T, Okano H. MicroRNAs in neural stem cells and neurogenesis. Front Neurosci. 2012;6:30.
35. Kim J, Inoue K, Ishii J, Vanti WB, Voronov SV, Murchison E, et al. A microRNA feedback circuit in midbrain dopamine neurons. Science. 2007;317(5842):1220-4.
36. Konopka W, Schütz G, Kaczmarek L. The microRNA contribution to learning and memory. Neuroscientist. 2011;17(5):468-74.
37. Kosik KS. Neuroscience gears up for duel on the issue of brain versus deity. Nature. 2006;439(7073):138.
38. Krek A, Grün D, Poy MN, Wolf R, Rosenberg L, Epstein EJ, et al. Combinatorial microRNA target predictions. Nat Genet. 2005;37(5):495-500.
39. Krichevsky AM, King KS, Donahue CP, Khrapko K, Kosik KS. A microRNA array reveals extensive regulation of microRNAs during brain development. RNA. 2003;9(10):1274-81.
40. Krug AK, Balmer NV, Matt F, Schönenberger F, Merhof D, Leist M. Evaluation of a human neurite growth assay as specific screen for developmental neurotoxicants. Arch Toxicol. 2013; May 14.
41. Laurenza I, Pallocca G, Mennecozzi M, Scelfo B, Pamies D, Bal-Price A. A human pluripotent carcinoma stem cell-based model for in vitro developmental neurotoxicity testing: effects of methylmercury, lead and aluminum evaluated by gene expression studies. Int J Dev Neurosci. 2013;S0736-5748(13):00038-5.
42. Lebel J, Mergler D, Branches F, Lucotte M, Amorim M, Larribe F, et al. Neurotoxic effects of low-level methylmercury contamination in the Amazonian Basin. Environ Res. 1998;79:20-32.
43. Lei W, Hirose T, Zhang LX, Adachi H, Spinella MJ, Dmitrovsky E, et al. Cloning of the human orphan receptor germ cell nuclear factor/retinoid receptor-related testis-associated receptor and its differential regulation during embryonal carcinoma cell differentiation. J Mol Endocrinol. 1997;18(2):167-76.
44. Leucht C, Stigloher C, Wizenmann A, Klafke R, Folchert A, Bally-Cuif L. MicroRNA-9 directs late organizer activity of the midbrain-hindbrain boundary. Nat Neurosci. 2008;11(6):641-8.
45. Lim LP, Lau NC, Garrett-Engele P, Grimson A, Schelter JM, Castle J, et al. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature. 2005;433(7027):769-73.
46. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25:402-8.
47. Magenta A, Cencioni C, Fasanaro P, Zaccagnini G, Greco S, Sarra-Ferraris G, et al. miR-200c is upregulated by oxidative stress and induces endothelial cell apoptosis and senescence via ZEB1 inhibition. Cell Death Differ. 2011;18(10):1628-39.
48. Makeyev EV, Zhang J, Carrasco MA, Maniatis T. The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol Cell. 2007;27(3):435-48.
49. Maller Schulman BR, Liang X, Stahlhut C, DelConte C, Stefani G, Slack FJ. The let-7 microRNA target gene, Mlin41/Trim71 is required for mouse embryonic survival and neural tube closure. Cell Cycle. 2008;7(24):3935-42.
50. Mateescu B, Batista L, Cardon M, Gruosso T, de Feraudy Y, Mariani O, et al. miR-141 and miR-200a act on ovarian tumorigenesis by controlling oxidative stress response. Nat Med. 2011;17(12):1627-35.
51. Miska EA, Alvarez-Saavedra E, Townsend M, Yoshii A, Sestan N, Rakic P, et al. Microarray analysis of microRNA expression in the developing mammalian brain. Genome Biol. 2004;5(9):R68.
52. Nerini-Molteni S, Mennecozzi M, Fabbri M, Sacco MG, Vojnits K, Compagnoni A, et al. MicroRNA profiling as a tool for pathway analysis in a human in vitro model for neural development. Curr Med Chem. 2012;19(36):6214-23.
53. NRC. Toxicity testing in the 21st century: a vision and a strategy. Washington, D.C.: The National Academies Press; 2007.
54. O'Brien J, Wilson I, Orton T, Pognan F. Investigation of the Alamar Blue (resazurin) fluorescent dye for the assessment of mammalian cell cytotoxicity. Eur J Biochem. 2000;267:5421-6.
55. OECD (2007). Test Guideline 426. OECD Guideline for Testing of Chemicals. Developmental Neurotoxicity Study. Available: http://www.oecd.org/document/55/ 0,3343,en-2649-34377-2349687-1-1-1-1,00.html
56. Pan G, Thomson JA. Nanog and transcriptional networks in embryonic stem cell pluripotency. Cell Res. 2007;17(1):42-9.
57. Parsons XH. MicroRNA profiling reveals distinct mechanisms governing cardiac and neural lineage-specification of pluripotent human embryonic stem cells. J Stem Cell Res Ther. 2012;13:2(3).
58. Pasquinelli AE, Ruvkun G. Control of developmental timing by microRNAs and their targets. Annu Rev Cell Dev Biol. 2002;18:495-513.
59. Pleasure SJ, Page C, Lee VM. Pure, postmitotic, polarized human neurons derived from NTera 2 cells provide a system for expressing exogenous proteins in terminally differentiated neurons. J Neurosci. 1992;12:1802-15.
60. Radio NM, Mundy WR. Developmental neurotoxicity testing in vitro: models for assessing chemical effects on neurite outgrowth. Neurotoxicology. 2008;29(3):361-76.
61. Rand MD. Drosophotoxicology: the growing potential for Drosophila in neurotoxicology. Neurotoxicol Teratol. 2010;32(1):74-83.
62. Rodda S, Sharma S, Scherer M, Chapman G, Rathjen P. CRTR-1, a developmentally regulated transcriptional repressor related to the CP2 family of transcription factors. J Biol Chem. 2001;276(5):3324-32.
63. Rodier PM. Developing brain as a target of toxicity. Environ Health Perspect. 1995;103:73-6.
64. Roush S, Slack FJ. The let-7 family of microRNAs. Trends Cell Biol. 2008;18(10):505-16.
65. Rybak A, Fuchs H, Smirnova L, Brandt C, Pohl EE, Nitsch R, et al. A feedback loop comprising lin-28 and let-7 controls pre-let-7 maturation during neural stem-cell commitment. Nat Cell Biol. 2008;10(8):987-93.
66. Schaefer A, O'Carroll D, Tan CL, Hillman D, Sugimori M, Llinas R, et al. Cerebellar neurodegeneration in the absence of microRNAs. J Exp Med. 2007;204(7):1553-8.
67. Schratt GM, Tuebing F, Nigh EA, Kane CG, Sabatini ME, Kiebler M, et al. A brain-specific microRNA regulates dendritic spine development. Nature. 2006;439(7074):283-9.
68. Sempere LF, Freemantle S, Pitha-Rowe I, Moss E, Dmitrovsky E, Ambros V. Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation. Genome Biol. 2004;5(3):R13.
69. Smyth GK. Limma: linear models for microarray data. In: Bioinformatics and computational biology solutions using R and bioconductor. Springer: New York; 2005. p. 397-420.
70. Stallings RL, Foley NH, Bray IM, Das S, Buckley PG. MicroRNA and DNA methylation alterations mediating retinoic acid induced neuroblastoma cell differentiation. Semin Cancer Biol. 2011;21(4):283-90.
71. Stiegler NV, Krug AK, Matt F, Leist M. Assessment of chemical-induced impairment of human neurite outgrowth by multiparametric live cell imaging in high-density cultures. Toxicol Sci. 2011;121(1):73-87.
72. Stummann TC, Hareng L, Bremer S. Hazard assessment of methylmercury toxicity to neuronal induction in embryogenesis using human embryonic stem cells. Toxicology. 2009;257(3):117-26.
73. Suh MR, Lee Y, Kim JY, Kim SK, Moon SH, Lee JY, et al. Human embryonic stem cells express a unique set of microRNAs. Dev Biol. 2004;270(2):488-98.
74. Sutton MA, Schuman EM. Dendritic protein synthesis, synaptic plasticity, and memory. Cell. 2006;127(1):49-58.
75. Tilson HA. Neurotoxicology risk assessment guidelines: developmental neurotoxicology. Neurotoxicology. 2000;21:189-94.
76. U.S. EPA (U.S. Environmental Protection Agency), 1998. U.S. Environmental Protection Agency Health Effects Test Guidelines. OPPTS 870.6300. Developmental Neurotoxicity Study. U.S. EPA 712-C-98-239. Available: http://www.epa.gov/ opptsfrs/publications/OPPTS-Harmonized/870-Health-Effects-Test-Guidelines/ Series/870-6300.pdf
77. Visvanathan J, Lee S, Lee B, Lee JW, Lee SK. The microRNA miR-124 antagonizes the antineural REST/SCP1 pathway during embryonic CNS development. Genes Dev. 2007;21(7):744-9.
78. Vo N, Klein ME, Varlamova O, Keller DM, Yamamoto T, Goodman RH, et al. A cAMP-response element binding protein-induced microRNA regulates neuronal morphogenesis. Proc Natl Acad Sci U S A. 2005;102(45):16426-31.
79. Wanet A, Tacheny A, Arnould T, Renard P. miR-212/132 expression and functions: within and beyond the neuronal compartment. Nucleic Acids Res. 2012;40(11):4742-53.
80. Wang W, Kwon EJ, Tsai LH. MicroRNAs in learning, memory, and neurological diseases. Learn Mem. 2012;19(9):359-68.
81. Wayman GA, Davare M, Ando H, Fortin D, Varlamova O, Cheng HY, et al. An activity-regulated microRNA controls dendritic plasticity by down-regulating p250GAP. Proc Natl Acad Sci U S A. 2008;105(26):9093-8.
82. Wulczyn FG, Smirnova L, Rybak A, Brandt C, Kwidzinski E, Ninnemann O, et al. Post-transcriptional regulation of the let-7 microRNA during neural cell specification. FASEB J. 2007;21(2):415-26.
83. Yokoo EM, Valente JG, Grattan L, Schmidt SL, Platt I, Silbergeld EK. Low level methylmercury exposure affects neuropsychological function in adults. Environ Health. 2003;2(1):8.
84. Yu JY, Chung KH, Deo M, Thompson RC, Turner DL. MicroRNA miR-124 regulates neurite outgrowth during neuronal differentiation. Exp Cell Res. 2008;314(14):2618-33.