Shared long-range regulatory elements coordinate expression of a gene cluster encoding nicotinic receptor heteromeric subtypes

Molecular and Cellular Biology

Volumn 26, Issue 15, 2006, Pages 5636-5649

  Xu, Xiaohong ^a   Scott, Michael M ^a   Deneris, Evan S ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; ALPHA3 INTEGRIN; ALPHA5 INTEGRIN; BETA GALACTOSIDASE; BETA4 INTEGRIN; NICOTINIC RECEPTOR; RECEPTOR SUBTYPE; RECEPTOR SUBUNIT;

3' UNTRANSLATED REGION; ADRENAL GLAND; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ARTIFICIAL CHROMOSOME; AUTONOMIC GANGLION; BINDING SITE; BRAIN; CELL POPULATION; CENTRAL NERVOUS SYSTEM; CHOLINERGIC SYNAPSE; CONSERVED NONCODING REGION; CONTROLLED STUDY; DNA FLANKING REGION; DNA SEQUENCE; ENHANCER REGION; EXON; GENE CLUSTER; GENE DELETION; GENE EXPRESSION; GENE EXPRESSION REGULATION; HUMAN; MOUSE; NERVE CELL; NICOTINIC RECEPTOR ALPHA3 GENE; NICOTINIC RECEPTOR ALPHA5 GENE; NICOTINIC RECEPTOR BETA4 GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PINEAL BODY; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RAT; RECEPTOR BINDING; RECEPTOR GENE; REGULATORY SEQUENCE; SUPERIOR CERVICAL GANGLION; SYNAPTIC TRANSMISSION; TRANSCRIPTION REGULATION; TRANSGENE; TRANSGENICS; UNTRANSLATED REGION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BASE SEQUENCE; CHROMOSOMES, ARTIFICIAL, MAMMALIAN; EXONS; GENES, REPORTER; HUMANS; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; NEURONS; PINEAL GLAND; PROTEIN ISOFORMS; RATS; RECEPTORS, NICOTINIC; REGULATORY SEQUENCES, NUCLEIC ACID; SEQUENCE ALIGNMENT; SUPERIOR CERVICAL GANGLION; TISSUE DISTRIBUTION; TRANSGENES;

EID: 33746512547     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00456-06     Document Type: Article

References (69)

1. Antoch, M. P., E. J. Song, A. M. Chang, M. H. Vitaterna, Y. Zhao, L. D. Wilsbacher, A. M. Sangoram, D. P. King, L. H. Pinto, and J. S. Takahashi. 1997. Functional identification of the mouse circadian Clock gene by transgenic BAC rescue. Cell 89:655-667.
2. Bauchwitz, R., and F. Costantini. 2000. Developmentally distinct effects on human epsilon-, gamma- and delta-globin levels caused by the absence or altered position of the human beta-globin gene in YAC transgenic mice. Hum. Mol. Genet. 9:561-574.
3. Bender, M. A., M. Bulger, J. Close, and M. Groudine. 2000. Beta-globin gene switching and DNase I sensitivity of the endogenous beta-globin locus in mice do not require the locus control region. Mol. Cell 5:387-393.
4. Bender, M. A., J. N. Roach, J. Halow, J. Close, R. Alami, E. E. Bouhassira, M. Groudine, and S. N. Fiering. 2001. Targeted deletion of 5′HS1 and 5′HS4 of the beta-globin locus control region reveals additive activity of the DNaseI hypersensitive sites. Blood 98:2022-2027.
5. Bigger, C., E. A. Casanova, and P. D. Gardner. 1996. Transcriptional regulation of neuronal nicotinic acetylcholine receptor genes. Functional interactions between Sp1 and the rat beta4 subunit gene promoter. J. Biol. Chem. 271:32842-32848.
6. Bigger, C. B., I. N. Melnikova, and P. D. Gardner. 1997. Sp1 and Sp3 regulate expression of the neuronal nicotinic acetylcholine receptor subunit gene. J. Biol. Chem. 272:25976-25982.
7. Boulter, J., A. O'Shea-Greenfield, R. M. Duvoisin, J. G. Connolly, E. Wada, A. Jensen, P. D. Gardner, M. Ballivet, E. S. Deneris, D. McKinnon, S. Heinemann, and J. Patrick. 1990. α3, α5, and β4: three members of the rat neuronal nicotinic acetylcholine receptor-related gene family form a gene cluster. J. Biol. Chem. 265:4472-4482.
8. Boutanaev, A. M., A. I. Kalmykova, Y. Y. Shevelyov, and D. I. Nurminsky. 2002. Large clusters of co-expressed genes in the Drosophila genome. Nature 420:666-669.
9. Boyd, R. T. 1996. Transcriptional regulation and cell specificity determinants of the rat nicotinic acetylcholine receptor α3 gene. Neurosci. Lett. 208:73-76.
10. Campos-Caro, A., C. Carrasco-Serrano, L. M. Valor, S. Viniegra, J. J. Ballesta, and M. Criado. 1999. Multiple functional Sp1 domains in the minimal promoter region of the neuronal nicotinic receptor alpha5 subunit gene. J. Biol. Chem. 274:4693-4701.
11. Cordero-Erausquin, M., L. M. Marubio, R. Klink, and J. P. Changeux. 2000. Nicotinic receptor function: new perspectives from knockout mice. Trends Pharmacol. Sci. 21:211-217.
12. Corriveau, R. A., and D. K. Berg. 1993. Coexpression of multiple acetylcholine receptor genes in neurons: quantification of transcripts during development. J. Neurosci. 13:2662-2671.
13. Couturier, S., L. Erkman, S. Valera, D. Rungger, S. Bertrand, J. Boulter, M. Ballivet, and D. Bertrand. 1990. α5, α3, and non-α3: three clustered avian genes encoding neuronal nicotinic acetylcholine receptor-related subunits. J. Biol. Chem. 265:17560-17567.
14. Deneris, E. S., N. Francis, J. McDonough, D. Fyodorov, T. Miller, and X. Yang. 2000. Transcriptional control of the neuronal nicotinic acetylcholine receptor gene cluster by the beta43′ enhancer, Sp1, SCIP and ETS transcription factors. Eur. J. Pharmacol. 393:69-74.
15. de Souza, F. S., A. M. Santangelo, V. Bumaschny, M. E. Avale, J. L. Smart, M. J. Low, and M. Rubinstein. 2005. Identification of neuronal enhancers of the proopiomelanocortin gene by transgenic mouse analysis and phylogenetic footprinting. Mol. Cell. Biol. 25:3076-3086.
16. Di Angelantonio, S., C. Matteoni, E. Fabbretti, and A. Nistri. 2003. Molecular biology and electrophysiology of neuronal nicotinic receptors of rat chromaffin cells. Eur. J. Neurosci. 17:2313-2322.
17. Farrell, C. M., A. G. West, and G. Felsenfeld. 2002. Conserved CTCF insulator elements flank the mouse and human β-globin loci. Mol. Cell. Biol. 22:3820-3831.
18. Francis, N., and E. S. Deneris. 2002. Retinal neuron activity of ETS domain-binding sites in a nicotinic acetylcholine receptor gene cluster enhancer. J. Biol. Chem. 277:6511-6519.
19. Frank, M., and R. Kemler. 2002. Protocadherins. Curr. Opin. Cell Biol. 14:557-562.
20. Fyodorov, D., and E. Deneris. 1996. The POU domain of SCIP/Tst-1/Oct-6 is sufficient for activation of an acetylcholine receptor promoter. Mol. Cell. Biol. 16:5004-5014.
21. Gahring, L. C., K. Persiyanov, and S. W. Rogers. 2004. Neuronal and astrocyte expression of nicotinic receptor subunit beta4 in the adult mouse brain. J. Comp. Neurol. 468:322-333.
22. Gotti, C., and F. Clementi. 2004. Neuronal nicotinic receptors: from structure to pathology. Prog. Neurobiol. 74:363-396.
23. Helms, A. W., A. L. Abney, N. Ben-Arie, H. Y. Zoghbi, and J. E. Johnson. 2000. Autoregulation and multiple enhancers control Math1 expression in the developing nervous system. Development 127:1185-1196.
24. Hernandez, S. C., S. Vicini, Y. Xiao, M. I. Davila-Garcia, R. P. Yasuda, B. B. Wolfe, and K. J. Kellar. 2004. The nicotinic receptor in the rat pineal gland is an alpha3beta4 subtype. Mol. Pharmacol. 66:978-987.
25. Huang, M. M., N. Arnheim, and M. F. Goodman. 1992. Extension of base mispairs by Taq DNA polymerase: implications for single nucleotide discrimination in PCR. Nucleic Acids Res. 20:4567-4573.
26. Hurst, L. D., C. Pal, and M. J. Lercher. 2004. The evolutionary dynamics of eukaryotic gene order. Nat. Rev. Genet. 5:299-310.
27. Kaufman, R. M., C. T. Pham, and T. J. Ley. 1999. Transgenic analysis of a 100-kb human beta-globin cluster-containing DNA fragment propagated as a bacterial artificial chromosome. Blood 94:3178-3184.
28. Khandekar, M., N. Suzuki, J. Lewton, M. Yamamoto, and J. D. Engel. 2004. Multiple, distant Gata2 enhancers specify temporally and tissue-specific patterning in the developing urogenital system. Mol. Cell. Biol. 24:10263-10276.
29. Kleinjan, D. A., and V. van Heyningen. 2005. Long-range control of gene expression: emerging mechanisms and disruption in disease. Am. J. Hum. Genet. 76:8-32.
30. Lee, E. C., D. Yu, J. Martinez de Velasco, L. Tessarollo, D. A. Swing, D. L. Court, N. A. Jenkins, and N. G. Copeland. 2001. A highly efficient Escherichia coli-based chromosome engineering system adapted for recombinogenic targeting and subcloning of BAC DNA. Genomics 73:56-65.
31. Levey, M. S., C. L. Brumwell, S. E. Dryer, and M. H. Jacob. 1995. Innervation and target tissue interactions differentially regulate acetylcholine receptor subunit mRNA levels in developing neurons in situ. Neuron 14:153-162.
32. Levey, M. S., and M. H. Jacob. 1996. Changes in the regulatory effects of cell-cell interactions on neuronal AChR subunit transcript levels after synapse formation. J. Neurosci. 16:6878-6885.
33. Levings, P. P., and J. Bungert. 2002. The human beta-globin locus control region, Eur. J. Biochem. 269:1589-1599.
34. Li, Q., K. R. Peterson, X. Fang, and G. Stamatoyannopoulos. 2002. Locus control regions. Blood 100:3077-3086.
35. Liu, Q., I. N. Melnikova, M. Hu, and P. D. Gardner. 1999. Cell type-specific activation of neuronal nicotinic acetylcholine receptor subunit genes by Sox10. J. Neurosci. 19:9747-9755.
36. Loots, G. G., R. M. Locksley, C. M. Blankespoor, Z. E. Wang, W. Miller, E. M. Rubin, and K. A. Frazer. 2000. Identification of a coordinate regulator of interleukins 4, 13, and 5 by cross-species sequence comparisons. Science 288:136-140.
37. Mandelzys, A., B. Pié, E. S. Deneris, and E. Cooper. 1994. The developmental increase in ACh current densities on rat sympathetic neurons correlates with changes in nicotinic ACh receptor a-subunit gene expression and occurs independently of innervation. J. Neurosci. 14:2357-2364.
38. McDonough, J., and E. Deneris. 1997. β43′: an enhancer displaying neural-restricted activity is located in the 3′-untranslated exon of the rat nicotinic acetylcholine receptor β4 gene. J. Neurosci. 17:2273-2283.
39. McDonough, J., N. Francis, T. Miller, and E. S. Deneris. 2000. Regulation of transcription in the neuronal nicotinic receptor subunit gene cluster by a neuron-selective enhancer and ETS domain factors. J. Biol. Chem. 275:28962-28970.
40. Moretti, M., S. Vailati, M. Zoli, G. Lippi, L. Riganti, R. Longhi, A. Viegi, F. Clementi, and C. Gotti. 2004. Nicotinic acetylcholine receptor subtypes expression during rat retina development and their regulation by visual experience. Mol. Pharmacol. 66:85-96.
41. Navas, P. A., K. R. Peterson, Q. Li, E. Skarpidi, A. Rohde, S. E. Shaw, C. H. Clegg, H. Asano, and G. Stamatoyannopoulos. 1998. Developmental specificity of the interaction between the locus control region and embryonic or fetal globin genes in transgenic mice with an HS3 core deletion. Mol. Cell. Biol. 18:4188-4196.
42. Nobrega, M. A., I. Ovcharenko, V. Afzal, and E. M. Rubin. 2003. Scanning human gene deserts for long-range enhancers. Science 302:413.
43. Ovcharenko, I., M. A. Nobrega, G. G. Loots, and L. Stubbs. 2004. ECR Browser: a tool for visualizing and accessing data from comparisons of multiple vertebrate genomes. Nucleic Acids Res. 32:W280-W286.
44. Perry, D. C., Y. Xiao, H. N. Nguyen, J. L. Musachio, M. I. Davila-Garcia, and K. J. Kellar. 2002. Measuring nicotinic receptors with characteristics of alpha4beta2, alpha3beta2 and alpha3beta4 subtypes in rat tissues by autoradiography. J. Neurochem. 82:468-481.
45. Pfaffl, M. W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45.
46. Pfaffl, M. W., G. W. Horgan, and L. Dempfle. 2002. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30:e36.
47. Rosenberg, M. M., R. C. Blitzblau, D. P. Olsen, and M. H. Jacob. 2002. Regulatory mechanisms that govern nicotinic synapse formation in neurons. J. Neurobiol. 53:542-555.
48. Saitoh, N., A. C. Bell, F. Recillas-Targa, A. G. West, M. Simpson, M. Pikaart, and G. Felsenfeld. 2000. Structural and functional conservation at the boundaries of the chicken b-globin domain. EMBO J. 19:2315-2322.
49. Scott, M. M., K. C. Krueger, and E. S. Deneris. 2005. A differentially autoregulated Pet-1 enhancer region is a critical target of the transcriptional cascade that governs serotonin neuron development. J. Neurosci. 25:2628-2636.
50. Sheffield, E. B., M. W. Quick, and R. A. Lester. 2000. Nicotinic acetylcholine receptor subunit mRNA expression and channel function in medial habenula neurons. Neuropharmacology 39:2591-2603.
51. Simon, J., H. Wakimoto, N. Fujita, M. Lalande, and E. A. Barnard. 2004. Analysis of the set of GABA(A) receptor genes in the human genome. J. Biol. Chem. 279:41422-41435.
52. Spitz, F., C. Herkenne, M. A. Morris, and D. Duboule. 2005. Inversion-induced disruption of the Hoxd cluster leads to the partition of regulatory landscapes. Nat. Genet. 37:889-893.
53. Tanimoto, K., Q. Liu, J. Bungert, and J. D. Engel. 1999. Effects of altered gene order or orientation of the locus control region on human beta-globin gene expression in mice. Nature 398:344-348.
54. Valor, L. M., A. Campos-Caro, C. Carrasco-Serrano, J. A. Ortiz, J. J. Ballesta, and M. Criado. 2002. Transcription factors NF-Y and Sp1 are important determinants of the promoter activity of the bovine and human neuronal nicotinic receptor beta 4 subunit genes. J. Biol. Chem. 277:8866-8876.
55. Wada, E., D. McKinnon, S. Heinemann, J. Patrick, and L. W. Swanson. 1990. The distribution of RNA encoded by a new member of the neuronal nicotinic acetylcholine receptor gene family (a5) in the rat central nervous system. Brain Res. 526:45-53.
56. Wada, E., K. Wada, J. Boulter, E. Deneris, S. Heinemann, J. Patrick, and L. W. Swanson. 1989. Distribution of alpha 2, alpha 3, alpha 4, and beta 2 neuronal nicotinic receptor subunit mRNAs in the central nervous system: a hybridization histochemical study in the rat. J. Comp. Neurol. 284:314-335.
57. Wang, N., A. Orr-Urtreger, and A. D. Korczyn. 2002. The role of neuronal nicotinic acetylcholine receptor subunits in autonomic ganglia: lessons from knockout mice. Prog. Neurobiol. 68:341-360.
58. Winzer-Serhan, U. H., and F. M. Leslie. 1997. Codistribution of nicotinic acetylcholine receptor subunit α3 and β4 mRNAs during rat brain development. J. Comp. Neurol. 386:540-554.
59. Woolfe, A., M. Goodson, D. K. Goode, P. Snell, G. K. McEwen, T. Vavouri, S. F. Smith, P. North, H. Callaway, K. Kelly, K. Walter, I. Abnizova, W. Gilks, Y. J. Edwards, J. E. Cooke, and G. Elgar. 2005. Highly conserved non-coding sequences are associated with vertebrate development. PLoS Biol. 3:e7. [Epub ahead of print.]
60. Woon, P. Y., K. Osoegawa, P. J. Kaisaki, B. Zhao, J. J. Catanese, D. Gauguier, R. Cox, E. R. Levy, G. M. Lathrop, A. P. Monaco, and P. J. de Jong. 1998. Construction and characterization of a 10-fold genome equivalent rat P1-derived artificial chromosome library. Genomics 50:306-316.
61. Yang, X., D. Fyodorov, and E. S. Deneris. 1995. Transcriptional analysis of acetylcholine receptor alpha 3 gene promoter motifs that bind Sp1 and AP2. J. Biol. Chem. 270:8514-8520.
62. Yang, X., Y. Kuo, P. Devay, C. Yu, and L. Role. 1998. A eystein-rich isoform of neuregulin controls the level of expression of neuronal nicotinic receptor channels during synaptogenesis. Neuron 20:255-270.
63. Yang, X., J. McDonough, D. Fyodorov, M. Morris, F. Wang, and E. S. Deneris. 1994. Characterization of an acetylcholine receptor alpha 3 gene promoter and its activation by the POU domain factor SC1P/Tst-1. J. Biol. Chem. 269:10252-10264.
64. Yang, X., P. Model, and N. Heintz. 1997. Homologous recombination based modification in Escherichia coli and germline transmission in transgenic mice of a bacterial artificial chromosome. Nat. Biotech. 15:859-865.
65. Yang, X., F. Yang, D. Fyodorov, F. Wang, J. McDonough, K. Herrup, and E. Deneris. 1997. Elements between the protein-coding regions of the adjacent β4 and α3 acetylcholine receptor genes directs neuron-specific expression in the central nervous system. J. Neurobiol. 32:311-324.
66. Yee, S. P., and P. W. Rigby. 1993. The regulation of myogenin gene expression during the embryonic development of the mouse. Genes Dev. 7:1277-1289.
67. Zhang, X., and S. Firestein. 2002. The olfactory receptor gene superfamily of the mouse. Nat. Neurosci. 5:124-133.
68. Zhou, Y., E. Deneris, and R. E. Zigmond. 1998. Differential regulation of levels of nicotinic receptor subunit transcripts in adult sympathetic neurons after axotomy. J. Neurobiol. 34:164-178.
69. Zoli, M., N. L. Novére, J. A. Hill, and J.-P. Changeux. 1995. Developmental regulation of nicotinic ACh receptor subunit mRNAs in the rat central and peripheral nervous systems. J. Neurosci. 15:1912-1939.