Aryl hydrocarbon receptor deletion in cerebellar granule neuron precursors impairs neurogenesis

Developmental Neurobiology

Volumn 76, Issue 5, 2016, Pages 533-550

  Dever, Daniel P ^a   Adham, Zachariah O ^a   Thompson, Bryan ^a   Genestine, Matthieu ^b   Cherry, Jonathan ^a   Olschowka, John A ^a   DiCicco Bloom, Emanuel ^b   Opanashuk, Lisa A ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^b RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

aryl hydrocarbon receptor; cerebellar granule cells; cerebellum development; neurogenesis

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; AROMATIC HYDROCARBON RECEPTOR; CELL DNA; CRE RECOMBINASE; DNA; HISTONE H3; THYMIDINE; 4 AMINOBUTYRIC ACID RECEPTOR ALPHA6; BROXURIDINE; UNCLASSIFIED DRUG; 4 AMINOBUTYRIC ACID A RECEPTOR; AHR PROTEIN, MOUSE; ATOH1 PROTEIN, MOUSE; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; GABRA6 PROTEIN, MOUSE;

ADULT; ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL CYCLE; CELL CYCLE S PHASE; CELL DIFFERENTIATION; CELL EXPANSION; CELL PROLIFERATION; CELL SURVIVAL; CEREBELLUM GRANULAR LAYER; CONTROLLED STUDY; DNA CONTENT; DNA SYNTHESIS; GENE; GENE DELETION; HISTONE PHOSPHORYLATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEURITE OUTGROWTH; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; CELL COUNT; DELETION MUTANT; EMBRYO; FEMALE; MALE; NEURAL STEM CELL; NOTE; ANIMAL; C57BL MOUSE; CELL CULTURE; CEREBELLUM; DEFICIENCY; GENETICS; GROWTH, DEVELOPMENT AND AGING; KNOCKOUT MOUSE; METABOLISM; NEURITE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL COUNT; CELL PROLIFERATION; CELLS, CULTURED; CEREBELLUM; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURAL STEM CELLS; NEURITES; NEUROGENESIS; NEURONS; RECEPTORS, ARYL HYDROCARBON; RECEPTORS, GABA-A;

EID: 85007543394     PISSN: 19328451     EISSN: 1932846X     Source Type: Journal    
DOI: 10.1002/dneu.22330     Document Type: Article

References (58)

1. Allen Institute for Brain Science. Allen Developing Mouse Brain Atlas. Available at: http://www.brain-map.org.
2. Aruga J, Inoue T, Hoshino J, Mikoshiba K. 2002. Zic2 controls cerebellar development in cooperation with Zic1. J Neurosci 22:218–225.
3. Ben-Arie N, McCall AE, Berkman S, Eichele G, Bellen HJ, Zoghbi HY. 1996. Evolutionary conservation of sequence and expression of the bHLH protein Atonal suggests a conserved role in neurogenesis. Hum Mol Genet 5:1207–1216.
4. Birnbaum LS, Tuomisto J. 2000. Non-carcinogenic effects of TCDD in animals. Food Addit Contam 17:275–288.
5. Cheng Y, Tao Y, Black IB, DiCicco-Bloom E. 2001. A single peripheral injection of basic fibroblast growth factor (bFGF) stimulates granule cell production and increases cerebellar growth in newborn rats. J Neurobiol 46:220–229.
6. Collins LL, Williamson MA, Thompson BD, Dever DP, Gasiewicz TA, Opanashuk LA. 2008. 2,3,7,8-Tetracholorodibenzo-p-dioxin exposure disrupts granule neuron precursor maturation in the developing mouse cerebellum. Toxicol Sci 103:125–136.
7. Corrales JD, Blaess S, Mahoney EM, Joyner AL. 2006. The level of sonic hedgehog signaling regulates the complexity of cerebellar foliation. Development 133:1811–1821.
8. Crews ST. 1998. Control of cell lineage-specific development and transcription by bHLH-PAS proteins. Genes Dev 12:607–620.
9. Crews ST, Fan CM. 1999. Remembrance of things PAS: Regulation of development by bHLH-PAS proteins. Curr Opin Genet Dev 9:580–587.
10. Denison MS, Nagy SR. 2003. Activation of the aryl hydrocarbon receptor by structurally diverse exogenous and endogenous chemicals. Annu Rev Pharmacol Toxicol 43:309–334.
11. Dever DP, Opanashuk LA. 2012. The aryl hydrocarbon receptor contributes to the proliferation of human medulloblastoma cells. Mol Pharmacol 81:669–678.
12. Duman-Scheel M, Weng L, Xin S, Du W. 2002. Hedgehog regulates cell growth and proliferation by inducing Cyclin D and Cyclin E. Nature 417:299–304.
13. Elizondo G, Fernandez-Salguero P, Sheikh MS, Kim GY, Fornace AJ, Lee KS, Gonzalez FJ. 2000. Altered cell cycle control at the G(2)/M phases in aryl hydrocarbon receptor-null embryo fibroblast. Mol Pharmacol 57:1056–1063.
14. Gasiewicz TA, Henry EC, Collins LL. 2008. Expression and activity of aryl hydrocarbon receptors in development and cancer. Crit Rev Eukaryot Gene Expr 18:279–321.
15. Hatten ME, Alder J, Zimmerman K, Heintz N. 1997. Genes involved in cerebellar cell specification and differentiation. Curr Opin Neurobiol 7:40–47.
16. Hatten ME, Heintz N. 1995. Mechanisms of neural patterning and specification in the developing cerebellum. Annu Rev Neurosci 18:385–408.
17. Huang X, Powell-Coffman JA, Jin Y. 2004. The AHR-1 aryl hydrocarbon receptor and its co-factor the AHA-1 aryl hydrocarbon receptor nuclear translocator specify GABAergic neuron cell fate in C. elegans. Development 131:819–828.
18. Ivnitski I, Elmaoued R, Walker MK. 2001. 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) inhibition of coronary development is preceded by a decrease in myocyte proliferation and an increase in cardiac apoptosis. Teratology 64:201–212.
19. Kajta M, Wojtowicz AK, Mackowiak M, Lason W. 2009. Aryl hydrocarbon receptor-mediated apoptosis of neuronal cells: A possible interaction with estrogen receptor signaling. Neuroscience 158:811–822.
20. Kakeyama M, Tohyama C. 2003. Developmental neurotoxicity of dioxin and its related compounds. Ind Health 41:215–230.
21. Kenney AM, Cole MD, Rowitch DH. 2003. Nmyc upregulation by sonic hedgehog signaling promotes proliferation in developing cerebellar granule neuron precursors. Development 130:15–28.
22. Kenney AM, Rowitch DH. 2000. Sonic hedgehog promotes G(1) cyclin expression and sustained cell cycle progression in mammalian neuronal precursors. Mol Cell Biol 20:9055–9067.
23. Kenney AM, Widlund HR, Rowitch DH. 2004. Hedgehog and PI-3 kinase signaling converge on Nmyc1 to promote cell cycle progression in cerebellar neuronal precursors. Development 131:217–228.
24. Kim MD, Jan LY, Jan YN. 2006. The bHLH-PAS protein Spineless is necessary for the diversification of dendrite morphology of Drosophila dendritic arborization neurons. Genes Dev 20:2806–2819.
25. Labarca C, Paigen K. 1980. A simple, rapid, and sensitive DNA assay procedure. Anal Biochem 102:344–352.
26. Lahvis GP, Pyzalski RW, Glover E, Pitot HC, McElwee MK, Bradfield CA. 2005. The aryl hydrocarbon receptor is required for developmental closure of the ductus venosus in the neonatal mouse. Mol Pharmacol 67:714–720.
27. Latchney SE, Hein AM, O'Banion MK, DiCicco-Bloom E, Opanashuk LA. 2013. Deletion or activation of the aryl hydrocarbon receptor alters adult hippocampal neurogenesis and contextual fear memory. J Neurochem 125:430–445.
28. Loukas CG, Wilson GD, Vojnovic B, Linney A. 2003. An image analysis-based approach for automated counting of cancer cell nuclei in tissue sections. Cytometry A 55:30–42.
29. Lund AK, Goens MB, Kanagy NL, Walker MK. 2003. Cardiac hypertrophy in aryl hydrocarbon receptor null mice is correlated with elevated angiotensin II, endothelin-1, and mean arterial blood pressure. Toxicol Appl Pharmacol 193:177–187.
30. Machold R, Fishell G. 2005. Math1 is expressed in temporally discrete pools of cerebellar rhombic-lip neural progenitors. Neuron 48:17–24.
31. Miyata T, Maeda T, Lee JE. 1999. NeuroD is required for differentiation of the granule cells in the cerebellum and hippocampus. Genes Dev 13:1647–1652.
32. Miyazawa K, Himi T, Garcia V, Yamagishi H, Sato S, Ishizaki Y. 2000. A role for p27/Kip1 in the control of cerebellar granule cell precursor proliferation. J Neurosci 20:5756–5763.
33. Mooney SM, Miller MW. 2000. Expression of bcl-2, bax, and caspase-3 in the brain of the developing rat. Brain Res Dev Brain Res 123:103–117.
34. Murata K, Hattori M, Hirai N, Shinozuka Y, Hirata H, Kageyama R, Sakai T, et al. 2005. Hes1 directly controls cell proliferation through the transcriptional repression of p27Kip1. Mol Cell Biol 25:4262–4271.
35. Muzumdar MD, Tasic B, Miyamichi K, Li L, Luo L. 2007. A global double-fluorescent Cre reporter mouse. Genesis 45:593–605.
36. Nicot A, DiCicco-Bloom E. 2001. Regulation of neuroblast mitosis is determined by PACAP receptor isoform expression. Proc Natl Acad Sci USA 98:4758–4763.
37. Pool M, Thiemann J, Bar-Or A, Fournier AE. 2008. NeuriteTracer: A novel ImageJ plugin for automated quantification of neurite outgrowth. J Neurosci Methods 168:134–139.
38. Przyborski SA, Cambray-Deakin MA. 1997. Profile of glutamylated tubulin expression during cerebellar granule cell development in vitro. Brain Res Dev Brain Res 100:133–138.
39. Qin H, Powell-Coffman JA. 2004. The Caenorhabditis elegans aryl hydrocarbon receptor, AHR-1, regulates neuronal development. Dev Biol 270:64–75.
40. Rossman IT, Lin L, Morgan KM, Digiovine M, Van Buskirk EK, Kamdar S, Millonig JH, et al. 2014. Engrailed2 modulates cerebellar granule neuron precursor proliferation, differentiation and insulin-like growth factor 1 signaling during postnatal development. Mol Autism 5:9
41. Roussel MF, Hatten ME. 2011. Cerebellum development and medulloblastoma. Curr Top Dev Biol 94:235–282.
42. Schantz SL. 1996. Developmental neurotoxicity of PCBs in humans: What do we know and where do we go from here? Neurotoxicol Teratol 18:217–227; discussion 229–276.
43. Schecter A, Cramer P, Boggess K, Stanley J, Papke O, Olson J, Silver A, et al. 2001. Intake of dioxins and related compounds from food in the U.S. population. J Toxicol Environ Health A 63:1–18.
44. Schmidt JV, Su GH, Reddy JK, Simon MC, Bradfield CA. 1996. Characterization of a murine Ahr null allele: Involvement of the Ah receptor in hepatic growth and development. Proc Natl Acad Sci USA 93:6731–6736.
45. Solecki DJ, Liu XL, Tomoda T, Fang Y, Hatten ME. 2001. Activated Notch2 signaling inhibits differentiation of cerebellar granule neuron precursors by maintaining proliferation. Neuron 31:557–568.
46. Thiel R, Koch E, Ulbrich B, Chahoud I. 1994. Peri- and postnatal exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin: Effects on physiological development, reflexes, locomotor activity and learning behaviour in Wistar rats. Arch Toxicol 69:79–86.
47. Thomsen JS, Kietz S, Strom A, Gustafsson JA. 2004. HES-1, a novel target gene for the aryl hydrocarbon receptor. Mol Pharmacol 65:165–171.
48. Tohkin M, Fukuhara M, Elizondo G, Tomita S, Gonzalez FJ. 2000. Aryl hydrocarbon receptor is required for p300-mediated induction of DNA synthesis by adenovirus E1A. Mol Pharmacol 58:845–851.
49. Walisser JA, Glover E, Pande K, Liss AL, Bradfield CA. 2005. Aryl hydrocarbon receptor-dependent liver development and hepatotoxicity are mediated by different cell types. Proc Natl Acad Sci USA 102:17858–17863.
50. Wang VY, Zoghbi HY. 2001. Genetic regulation of cerebellar development. Nat Rev Neurosci 2:484–491.
51. Wechsler-Reya R, Scott MP. 2001. The developmental biology of brain tumors. Annu Rev Neurosci 24:385–428.
52. Wechsler-Reya RJ, Scott MP. 1999. Control of neuronal precursor proliferation in the cerebellum by Sonic Hedgehog. Neuron 22:103–114.
53. White LD, Barone S Jr. 2001. Qualitative and quantitative estimates of apoptosis from birth to senescence in the rat brain. Cell Death Differ 8:345–356.
54. Williamson MA, Gasiewicz TA, Opanashuk LA. 2005. Aryl hydrocarbon receptor expression and activity in cerebellar granule neuroblasts: Implications for development and dioxin neurotoxicity. Toxicol Sci 83:340–348.
55. Yang H, Xie X, Deng M, Chen X, Gan L. 2010. Generation and characterization of Atoh1-Cre knock-in mouse line. Genesis 48:407–413.
56. Ye P, Xing Y, Dai Z, D'Ercole AJ. 1996. In vivo actions of insulin-like growth factor-I (IGF-I) on cerebellum development in transgenic mice: Evidence that IGF-I increases proliferation of granule cell progenitors. Brain Res Dev Brain Res 95:44–54.
57. Zheng C, Heintz N, Hatten ME. 1996. CNS gene encoding astrotactin, which supports neuronal migration along glial fibers. Science 272:417–419.
58. Zheng T, Santi MR, Bovolin P, Marlier LN, Grayson DR. 1993. Developmental expression of the alpha 6 GABAA receptor subunit mRNA occurs only after cerebellar granule cell migration. Brain Res Dev Brain Res 75:91–103.