Regulation of protocadherin gene expression by multiple neuron-restrictive silencer elements scattered in the gene cluster

Nucleic Acids Research

Volumn 38, Issue 15, 2010, Pages 4985-4997

  Tan, Yuen Peng ^a   Li, Shaobing ^a   Jiang, Xiao Juan ^a,b   Loh, Wailin ^a   Foo, Yik Khon ^c   Loh, Chay Boon ^c   Xu, Qiurong ^c   Yuen, Wai Hong ^d   Jones, Michael ^d   Fu, Jianlin ^c   Venkatesh, Byrappa ^c   Yu, Wei Ping ^a  

^a National Neuroscience Institute   (Singapore)

^b SHANDONG UNIVERSITY   (China)

^c INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^d INSTITUTE OF MEDICAL BIOLOGY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

5' UNTRANSLATED REGION; ANIMAL CELL; ARTICLE; CELL SPECIFICITY; CONTROLLED STUDY; EMBRYO; GENE; GENE CLUSTER; GENE EXPRESSION REGULATION; GENE STRUCTURE; HUMAN; HUMAN CELL; MOUSE; NERVE CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTOCADHERIN GENE; PUFFER FISH; SILENCER ELEMENT; VERTEBRATE; XENOPUS; ANIMAL; CELL LINE; GENE SILENCING; GENETICS; METABOLISM; MULTIGENE FAMILY; XENOPUS LAEVIS; ZEBRA FISH;

CHONDRICHTHYES; COELACANTHIDAE; DANIO RERIO; SQUAMATA; TAKIFUGU; VERTEBRATA;

CADHERIN;

ANIMALS; CADHERINS; CELL LINE; GENE SILENCING; HUMANS; MICE; MULTIGENE FAMILY; NEURONS; PROMOTER REGIONS, GENETIC; SILENCER ELEMENTS, TRANSCRIPTIONAL; TAKIFUGU; XENOPUS LAEVIS; ZEBRAFISH;

EID: 77956132704     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkq246     Document Type: Article

References (63)

1. Shapiro,L. and Colman,D.R. (1999) The diversity of cadherins and implications for a synaptic adhesive code in the CNS. Neuron, 23, 427-430.
2. Takeichi,M. (2007) The cadherin superfamily in neuronal connections and interactions. Nat. Rev. Neurosci., 8, 11-20.
3. Yagi,T. and Takeichi,M. (2000) Cadherin superfamily genes: functions, genomic organization, and neurologic diversity. Genes Dev., 14, 1169-1180.
4. Halbleib,J.M. and Nelson,W.J. (2006) Cadherins in development: cell adhesion, sorting, and tissue morphogenesis. Genes Dev., 20, 3199-3214.
5. Kohmura,N., Senzaki,K., Hamada,S., Kai,N., Yasuda,R., Watanabe,M., Ishii,H., Yasuda,M., Mishina,M. and Yagi,T. (1998) Diversity revealed by a novel family of cadherins expressed in neurons at a synaptic complex. Neuron, 20, 1137-1151.
6. Wu,Q. (2005) Comparative genomics and diversifying selection of the clustered vertebrate protocadherin genes. Genetics, 169, 2179-2188.
7. Wu,Q., Zhang,T., Cheng,J.F., Kim,Y., Grimwood,J., Schmutz,J., Dickson,M., Noonan,J.P., Zhang,M.Q., Myers,R.M. et al. (2001) Comparative DNA sequence analysis of mouse and human protocadherin gene clusters. Genome Res., 11, 389-404.
8. Wu,Q. and Maniatis,T. (1999) A striking organization of a large family of human neural cadherin-like cell adhesion genes. Cell, 97, 779-790.
9. Zou,C., Huang,W., Ying,G. and Wu,Q. (2007) Sequence analysis and expression mapping of the rat clustered protocadherin gene repertoires. Neuroscience, 144, 579-603.
10. Sugino,H., Hamada,S., Yasuda,R., Tuji,A., Matsuda,Y., Fujita,M. and Yagi,T. (2000) Genomic organization of the family of CNR cadherin genes in mice and humans. Genomics, 63, 75-87.
11. Vanhalst,K., Kools,P., Vanden,E.E. and van,R.F. (2001) The human and murine protocadherin-beta one-exon gene families show high evolutionary conservation, despite the difference in gene number. FEBS Lett., 495, 120-125.
12. Wang,X., Weiner,J.A., Levi,S., Craig,A.M., Bradley,A. and Sanes,J.R. (2002) Gamma protocadherins are required for survival of spinal interneurons. Neuron, 36, 843-854.
13. Phillips,G.R., Tanaka,H., Frank,M., Elste,A., Fidler,L., Benson,D.L. and Colman,D.R. (2003) Gamma-protocadherins are targeted to subsets of synapses and intracellular organelles in neurons. J. Neurosci., 23, 5096-5104.
14. Blank,M., Triana-Baltzer,G.B., Richards,C.S. and Berg,D.K. (2004) Alpha-protocadherins are presynaptic and axonal in nicotinic pathways. Mol. Cell Neurosci., 26, 530-543.
15. Hasegawa,S., Hamada,S., Kumode,Y., Esumi,S., Katori,S., Fukuda,E., Uchiyama,Y., Hirabayashi,T., Mombaerts,P. and Yagi,T. (2008) The protocadherin-alpha family is involved in axonal coalescence of olfactory sensory neurons into glomeruli of the olfactory bulb in mouse. Mol. Cell Neurosci., 38, 66-79.
16. Katori,S., Hamada,S., Noguchi,Y., Fukuda,E., Yamamoto,T., Yamamoto,H., Hasegawa,S. and Yagi,T. (2009) Protocadherinalpha family is required for serotonergic projections to appropriately innervate target brain areas. J. Neurosci., 29, 9137-9147.
17. Weiner,J.A., Wang,X., Tapia,J.C. and Sanes,J.R. (2005) Gamma protocadherins are required for synaptic development in the spinal cord. Proc. Natl Acad. Sci. USA, 102, 8-14.
18. Wang,X., Su,H. and Bradley,A. (2002) Molecular mechanisms governing Pcdh-gamma gene expression: evidence for a multiple promoter and cis-alternative splicing model. Genes Dev., 16, 1890-1905.
19. Esumi,S., Kakazu,N., Taguchi,Y., Hirayama,T., Sasaki,A., Hirabayashi,T., Koide,T., Kitsukawa,T., Hamada,S. and Yagi,T. (2005) Monoallelic yet combinatorial expression of variable exons of the protocadherin-alpha gene cluster in single neurons. Nat. Genet., 37, 171-176.
20. Kaneko,R., Kato,H., Kawamura,Y., Esumi,S., Hirayama,T., Hirabayashi,T. and Yagi,T. (2006) Allelic gene regulation of Pcdh-alpha and Pcdh-gamma clusters involving both monoallelic and biallelic expression in single Purkinje cells. J. Biol. Chem., 281, 30551-30560.
21. Ribich,S., Tasic,B. and Maniatis,T. (2006) Identification of longrange regulatory elements in the protocadherin-alpha gene cluster. Proc. Natl Acad. Sci. USA, 103, 19719-19724.
22. Aparicio,S., Chapman,J., Stupka,E., Putnam,N., Chia,J.M., Dehal,P., Christoffels,A., Rash,S., Hoon,S., Smit,A. et al. (2002) Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes. Science, 297, 1301-1310.
23. Yu,W.P., Yew,K., Rajasegaran,V. and Venkatesh,B. (2007) Sequencing and comparative analysis of fugu protocadherin clusters reveal diversity of protocadherin genes among teleosts. BMC Evol. Biol., 7, 49.
24. Bailey,T.L. and Elkan,C. (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc. Int. Conf. Intell. Syst. Mol. Biol., 2, 28-36.
25. Schug,J. (2003) Using TESS to predict transcription factor binding sites in DNA sequence. In Baxevanis,A.D. (ed.), Current Protocols in Bioinformatics. John Wiley and Sons.
26. Muyrers,J.P., Zhang,Y., Testa,G. and Stewart,A.F. (1999) Rapid modification of bacterial artificial chromosomes by ET-recombination. Nucleic Acids Res., 27, 1555-1557.
27. Smith,S.J., Fairclough,L., Latinkic,B.V., Sparrow,D.B. and Mohun,T.J. (2006) Xenopus laevis transgenesis by sperm nuclear injection. Nat. Protoc., 1, 2195-2203.
28. Sparrow,D.B., Latinkic,B. and Mohun,T.J. (2000) A simplified method of generating transgenic Xenopus. Nucleic Acids Res., 28, E12.
29. Simonis,M., Kooren,J. and de,L.W. (2007) An evaluation of 3C-based methods to capture DNA interactions. Nat. Methods, 4, 895-901.
30. Splinter,E., Grosveld,F. and de,L.W. (2004) 3C technology: analyzing the spatial organization of genomic loci in vivo. Methods Enzymol., 375, 493-507.
31. Yu,W.P., Rajasegaran,V., Yew,K., Loh,W.L., Tay,B.H., Amemiya,C.T., Brenner,S. and Venkatesh,B. (2008) Elephant shark sequence reveals unique insights into the evolutionary history of vertebrate genes: a comparative analysis of the protocadherin cluster. Proc. Natl Acad. Sci. USA, 105, 3819-3824.
32. Tasic,B., Nabholz,C.E., Baldwin,K.K., Kim,Y., Rueckert,E.H., Ribich,S.A., Cramer,P., Wu,Q., Axel,R. and Maniatis,T. (2002) Promoter choice determines splice site selection in protocadherin alpha and gamma pre-mRNA splicing. Mol. Cell, 10, 21-33.
33. Mori,N., Schoenherr,C., Vandenbergh,D.J. and Anderson,D.J. (1992) A common silencer element in the SCG10 and type II Na+ channel genes binds a factor present in nonneuronal cells but not in neuronal cells. Neuron, 9, 45-54.
34. Kraner,S.D., Chong,J.A., Tsay,H.J. and Mandel,G. (1992) Silencing the type II sodium channel gene: a model for neuralspecific gene regulation. Neuron, 9, 37-44.
35. Chong,J.A., Tapia-Ramirez,J., Kim,S., Toledo-Aral,J.J., Zheng,Y., Boutros,M.C., Altshuller,Y.M., Frohman,M.A., Kraner,S.D. and Mandel,G. (1995) REST: a mammalian silencer protein that restricts sodium channel gene expression to neurons. Cell, 80, 949-957.
36. Schoenherr,C.J. and Anderson,D.J. (1995) The neuron-restrictive silencer factor (NRSF): a coordinate repressor of multiple neuron-specific genes. Science, 267, 1360-1363.
37. Johnson,D.S., Mortazavi,A., Myers,R.M. and Wold,B. (2007) Genome-wide mapping of in vivo protein-DNA interactions. Science, 316, 1497-1502.
38. Otto,S.J., McCorkle,S.R., Hover,J., Conaco,C., Han,J.J., Impey,S., Yochum,G.S., Dunn,J.J., Goodman,R.H. and Mandel,G. (2007) A new binding motif for the transcriptional repressor REST uncovers large gene networks devoted to neuronal functions. J. Neurosci., 27, 6729-6739.
39. Patel,P.D., Bochar,D.A., Turner,D.L., Meng,F., Mueller,H.M. and Pontrello,C.G. (2007) Regulation of tryptophan hydroxylase-2 gene expression by a bipartite RE-1 silencer of transcription/neuron restrictive silencing factor (REST/NRSF) binding motif. J. Biol. Chem., 282, 26717-26724.
40. Bruce,A.W., Donaldson,I.J., Wood,I.C., Yerbury,S.A., Sadowski,M.I., Chapman,M., Gottgens,B. and Buckley,N.J. (2004) Genome-wide analysis of repressor element 1 silencing transcription factor/neuron-restrictive silencing factor (REST/NRSF) target genes. Proc. Natl Acad. Sci. USA, 101, 10458-10463.
41. Mortazavi,A., Leeper Thompson,E.C., Garcia,S.T., Myers,R.M. and Wold,B. (2006) Comparative genomics modeling of the NRSF/REST repressor network: from single conserved sites to genome-wide repertoire. Genome Res., 16, 1208-1221.
42. Kemp,D.M., Lin,J.C. and Habener,J.F. (2003) Regulation of Pax4 paired homeodomain gene by neuron-restrictive silencer factor. J. Biol. Chem., 278, 35057-35062.
43. Kemp,D.M., Lin,J.C., Ubeda,M. and Habener,J.F. (2002) NRSF/REST confers transcriptional repression of the GPR10 gene via a putative NRSE/RE-1 located in the 5' promoter region. FEBS Lett., 531, 193-198.
44. Huang,Y., Myers,S.J. and Dingledine,R. (1999) Transcriptional repression by REST: recruitment of Sin3A and histone deacetylase to neuronal genes. Nat. Neurosci., 2, 867-872.
45. Naruse,Y., Aoki,T., Kojima,T. and Mori,N. (1999) Neural restrictive silencer factor recruits mSin3 and histone deacetylase complex to repress neuron-specific target genes. Proc. Natl Acad. Sci. USA, 96, 13691-13696.
46. Roopra,A., Sharling,L., Wood,I.C., Briggs,T., Bachfischer,U., Paquette,A.J. and Buckley,N.J. (2000) Transcriptional repression by neuron-restrictive silencer factor is mediated via the Sin3-histone deacetylase complex. Mol. Cell Biol., 20, 2147-2157.
47. Andres,M.E., Burger,C., Peral-Rubio,M.J., Battaglioli,E., Anderson,M.E., Grimes,J., Dallman,J., Ballas,N. and Mandel,G. (1999) CoREST: a functional corepressor required for regulation of neural-specific gene expression. Proc. Natl Acad. Sci. USA, 96, 9873-9878.
48. De,G.S., Houhou,L., Oda,Y., Corbex,M., Pajak,F., Thevenot,E., Vodjdani,G., Mallet,J. and Berrard,S. (2000) Is RE1/NRSE a common cis-regulatory sequence for ChAT and VAChT genes? J. Biol. Chem., 275, 36683-36690.
49. Uvarov,P., Pruunsild,P., Timmusk,T. and Airaksinen,M.S. (2005) Neuronal K+/Cl- co-transporter (KCC2) transgenes lacking neurone restrictive silencer element recapitulate CNS neurone-specific expression and developmental up-regulation of endogenous KCC2 gene. J. Neurochem., 95, 1144-1155.
50. Frank,M., Ebert,M., Shan,W., Phillips,G.R., Arndt,K., Colman,D.R. and Kemler,R. (2005) Differential expression of individual gamma-protocadherins during mouse brain development. Mol. Cell Neurosci., 29, 603-616.
51. Morishita,H., Murata,Y., Esumi,S., Hamada,S. and Yagi,T. (2004) CNR/Pcdhalpha family in subplate neurons, and developing cortical connectivity. Neuroreport, 15, 2595-2599.
52. Stapleton,T., Luchman,A., Johnston,J., Browder,L., Brenner,S., Venkatesh,B. and Jirik,F.R. (2004) Compact intergenic regions of the pufferfish genome facilitate isolation of gene promoters: characterization of Fugu 3'-phosphoadenosine 5'-phosphosulfate synthase 2 (fPapss2) gene promoter function in transgenic Xenopus. FEBS Lett., 556, 59-63.
53. Zhang,T., Tan,Y.H., Fu,J., Lui,D., Ning,Y., Jirik,F.R., Brenner,S. and Venkatesh,B. (2003) The regulation of retina specific expression of rhodopsin gene in vertebrates. Gene, 313, 189-200.
54. Dekker,J., Rippe,K., Dekker,M. and Kleckner,N. (2002) Capturing chromosome conformation. Science, 295, 1306-1311.
55. Tada,M.N., Senzaki,K., Tai,Y., Morishita,H., Tanaka,Y.Z., Murata,Y., Ishii,Y., Asakawa,S., Shimizu,N., Sugino,H. et al. (2004) Genomic organization and transcripts of the zebrafish Protocadherin genes. Gene, 340, 197-211.
56. Noonan,J.P., Grimwood,J., Danke,J., Schmutz,J., Dickson,M., Amemiya,C.T. and Myers,R.M. (2004) Coelacanth genome sequence reveals the evolutionary history of vertebrate genes. Genome Res., 14, 2397-2405.
57. Noonan,J.P., Grimwood,J., Schmutz,J., Dickson,M. and Myers,R.M. (2004) Gene conversion and the evolution of protocadherin gene cluster diversity. Genome Res., 14, 354-366.
58. Jiang,X.J., Li,S., Ravi,V., Venkatesh,B. and Yu,W.P. (2009) Identification and comparative analysis of the protocadherin cluster in a reptile, the green anole lizard. PLoS ONE, 4, e7614.
59. Kallunki,P., Edelman,G.M. and Jones,F.S. (1997) Tissue-specific expression of the L1 cell adhesion molecule is modulated by the neural restrictive silencer element. J. Cell Biol., 138, 1343-1354.
60. Mu,W. and Burt,D.R. (1999) Transcriptional regulation of GABAA receptor gamma2 subunit gene. Brain Res. Mol. Brain Res., 67, 137-147.
61. Mahajan,M.C., Karmakar,S. and Weissman,S.M. (2007) Control of beta globin genes. J. Cell Biochem., 102, 801-810.
62. Spitz,F., Gonzalez,F. and Duboule,D. (2003) A global control region defines a chromosomal regulatory landscape containing the HoxD cluster. Cell, 113, 405-417.
63. Nguyen,M.Q., Zhou,Z., Marks,C.A., Ryba,N.J. and Belluscio,L. (2007) Prominent roles for odorant receptor coding sequences in allelic exclusion. Cell, 131, 1009-1017.