Enhancer interaction networks as a means for singular olfactory receptor expression

Cell

Volumn 159, Issue 3, 2014, Pages 543-557

  Markenscoff Papadimitriou, Eirene ^a   Allen, William E ^b   Colquitt, Bradley M ^a   Goh, Tracie ^c   Murphy, Karl K ^a   Monahan, Kevin ^c   Mosley, Colleen P ^c   Ahituv, Nadav ^a   Lomvardas, Stavros ^a,c,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BROMO AND PHD FINGER TRANSCRIPTION FACTOR; CIS ACTING ELEMENT; DEOXYRIBONUCLEASE I; LAMIN B; NEUROGENIN 1; SPACER DNA; TRANS ACTING FACTOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; VESICULAR GLUTAMATE TRANSPORTER 2; CELL NUCLEUS ANTIGEN; FETAL ALZHEIMER ANTIGEN; NERVE PROTEIN; NUCLEOPROTEIN; OLFACTORY RECEPTOR;

ANIMAL CELL; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOME 16; CHROMOSOME 2; CHROMOSOME 3; CHROMOSOME 7; CONSENSUS SEQUENCE; DNA FLANKING REGION; DNA SEQUENCE; EMBRYO; ENHANCER REGION; EPIGENETICS; GENE ACTIVATION; GENE CLUSTER; GENE INTERACTION; GENETIC MANIPULATION; HISTONE MODIFICATION; HOMOLOGOUS RECOMBINATION; IMMUNOFLUORESCENCE; IN SITU HYBRIDIZATION; INTERCHROMOSOMAL INTERACTION; INVERSE POLYMERASE CHAIN REACTION; MOLECULAR INTERACTION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OLFACTORY BULB; OLFACTORY EPITHELIUM; OLFACTORY RECEPTOR; OOCYTE; PROMOTER REGION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; TRANSGENIC ZEBRAFISH; WILD TYPE; ANIMAL; EMBRYOLOGY; GENETICS; METABOLISM; TRANSCRIPTION INITIATION; TRANSGENIC ANIMAL; ZEBRA FISH;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANTIGENS, NUCLEAR; ENHANCER ELEMENTS, GENETIC; MICE; NERVE TISSUE PROTEINS; NUCLEOPROTEINS; OLFACTORY RECEPTOR NEURONS; RECEPTORS, ODORANT; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION; ZEBRAFISH;

EID: 84908306696     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.09.033     Document Type: Article

References (67)

1. G. Andrey, and D. Duboule SnapShot: Hox gene regulation Cell 156 2014 856
2. E. Apostolou, and D. Thanos Virus infection induces NF-kappaB-dependent interchromosomal associations mediating monoallelic IFN-beta gene expression Cell 134 2008 85 96
3. A. Ariza-Cosano, A. Visel, L.A. Pennacchio, H.B. Fraser, J.L. Gómez-Skarmeta, M. Irimia, and J. Bessa Differences in enhancer activity in mouse and zebrafish reporter assays are often associated with changes in gene expression BMC Genomics 13 2012 713
4. L.M. Armelin-Correa, L.M. Gutiyama, D.Y. Brandt, and B. Malnic Nuclear compartmentalization of odorant receptor genes Proc. Natl. Acad. Sci. USA 111 2014 2782 2787
5. T.L. Bailey, and C. Elkan Fitting a mixture model by expectation maximization to discover motifs in biopolymers Proc. Int. Conf. Intell. Syst. Mol. Biol. 2 1994 28 36
6. C.I. Bargmann Comparative chemosensation from receptors to ecology Nature 444 2006 295 301
7. G. Barnea, S. O'Donnell, F. Mancia, X. Sun, A. Nemes, M. Mendelsohn, and R. Axel Odorant receptors on axon termini in the brain Science 304 2004 1468
8. A. Barski, S. Cuddapah, K. Cui, T.Y. Roh, D.E. Schones, Z. Wang, G. Wei, I. Chepelev, and K. Zhao High-resolution profiling of histone methylations in the human genome Cell 129 2007 823 837
9. S. Bonn, R.P. Zinzen, C. Girardot, E.H. Gustafson, A. Perez-Gonzalez, N. Delhomme, Y. Ghavi-Helm, B. Wilczyński, A. Riddell, and E.E. Furlong Tissue-specific analysis of chromatin state identifies temporal signatures of enhancer activity during embryonic development Nat. Genet. 44 2012 148 156
10. B.M. Booker, K.K. Murphy, and N. Ahituv Functional analysis of limb enhancers in the developing fin Dev. Genes Evol. 223 2013 395 399
11. L. Buck, and R. Axel A novel multigene family may encode odorant receptors: a molecular basis for odor recognition Cell 65 1991 175 187
12. C. Bushdid, M.O. Magnasco, L.B. Vosshall, and A. Keller Humans can discriminate more than 1 trillion olfactory stimuli Science 343 2014 1370 1372
13. A. Chess, I. Simon, H. Cedar, and R. Axel Allelic inactivation regulates olfactory receptor gene expression Cell 78 1994 823 834
14. E.J. Clowney, A. Magklara, B.M. Colquitt, N. Pathak, R.P. Lane, and S. Lomvardas High-throughput mapping of the promoters of the mouse olfactory receptor genes reveals a new type of mammalian promoter and provides insight into olfactory receptor gene regulation Genome Res. 21 2011 1249 1259
15. E.J. Clowney, M.A. LeGros, C.P. Mosley, F.G. Clowney, E.C. Markenskoff-Papadimitriou, M. Myllys, G. Barnea, C.A. Larabell, and S. Lomvardas Nuclear aggregation of olfactory receptor genes governs their monogenic expression Cell 151 2012 724 737
16. R.P. Dalton, D.B. Lyons, and S. Lomvardas Co-opting the unfolded protein response to elicit olfactory receptor feedback Cell 155 2013 321 332
17. S. Delpretti, T. Montavon, M. Leleu, E. Joye, A. Tzika, M. Milinkovitch, and D. Duboule Multiple enhancers regulate Hoxd genes and the Hotdog LncRNA during cecum budding Cell Rep. 5 2013 137 150
18. J. Ernst, P. Kheradpour, T.S. Mikkelsen, N. Shoresh, L.D. Ward, C.B. Epstein, X. Zhang, L. Wang, R. Issner, and M. Coyne Mapping and analysis of chromatin state dynamics in nine human cell types Nature 473 2011 43 49
19. T. Ferreira, S.R. Wilson, Y.G. Choi, D. Risso, S. Dudoit, T.P. Speed, and J. Ngai Silencing of odorant receptor genes by G protein βγ signaling ensures the expression of one odorant receptor per olfactory sensory neuron Neuron 81 2014 847 859
20. Y. Guo, K. Monahan, H. Wu, J. Gertz, K.E. Varley, W. Li, R.M. Myers, T. Maniatis, and Q. Wu CTCF/cohesin-mediated DNA looping is required for protocadherin α promoter choice Proc. Natl. Acad. Sci. USA 109 2012 21081 21086
21. J.M. Hébert, and S.K. McConnell Targeting of cre to the Foxg1 (BF-1) locus mediates loxP recombination in the telencephalon and other developing head structures Dev. Biol. 222 2000 296 306
22. J. Hirota, and P. Mombaerts The LIM-homeodomain protein Lhx2 is required for complete development of mouse olfactory sensory neurons Proc. Natl. Acad. Sci. USA 101 2004 8751 8755
23. J.R. Hughes, N. Roberts, S. McGowan, D. Hay, E. Giannoulatou, M. Lynch, M. De Gobbi, S. Taylor, R. Gibbons, and D.R. Higgs Analysis of hundreds of cis-regulatory landscapes at high resolution in a single, high-throughput experiment Nat. Genet. 46 2014 205 212
24. R.J. Johnston Jr., and C. Desplan Interchromosomal communication coordinates intrinsically stochastic expression between alleles Science 343 2014 661 665
25. K.L. Jordan-Sciutto, J.M. Dragich, J.L. Rhodes, and R. Bowser Fetal Alz-50 clone 1, a novel zinc finger protein, binds a specific DNA sequence and acts as a transcriptional regulator J. Biol. Chem. 274 1999 35262 35268
26. M. Khan, E. Vaes, and P. Mombaerts Regulation of the probability of mouse odorant receptor gene choice Cell 147 2011 907 921
27. R. Kothary, S. Clapoff, A. Brown, R. Campbell, A. Peterson, and J. Rossant A transgene containing lacZ inserted into the dystonia locus is expressed in neural tube Nature 335 1988 435 437
28. M. Krzywinski, J. Schein, I. Birol, J. Connors, R. Gascoyne, D. Horsman, S.J. Jones, and M.A. Marra Circos: an information aesthetic for comparative genomics Genome Res. 19 2009 1639 1645
29. J.W. Landry, S. Banerjee, B. Taylor, P.D. Aplan, A. Singer, and C. Wu Chromatin remodeling complex NURF regulates thymocyte maturation Genes Dev. 25 2011 275 286
30. J.W. Lewcock, and R.R. Reed A feedback mechanism regulates monoallelic odorant receptor expression Proc. Natl. Acad. Sci. USA 101 2004 1069 1074
31. Q. Li, D. Ritter, N. Yang, Z. Dong, H. Li, J.H. Chuang, and S. Guo A systematic approach to identify functional motifs within vertebrate developmental enhancers Dev. Biol. 337 2010 484 495
32. S. Lomvardas, G. Barnea, D.J. Pisapia, M. Mendelsohn, J. Kirkland, and R. Axel Interchromosomal interactions and olfactory receptor choice Cell 126 2006 403 413
33. D.B. Lyons, W.E. Allen, T. Goh, L. Tsai, G. Barnea, and S. Lomvardas An epigenetic trap stabilizes singular olfactory receptor expression Cell 154 2013 325 336
34. A. Magklara, A. Yen, B.M. Colquitt, E.J. Clowney, W. Allen, E. Markenscoff-Papadimitriou, Z.A. Evans, P. Kheradpour, G. Mountoufaris, and C. Carey An epigenetic signature for monoallelic olfactory receptor expression Cell 145 2011 555 570
35. D.M. McGaughey, R.M. Vinton, J. Huynh, A. Al-Saif, M.A. Beer, and A.S. McCallion Metrics of sequence constraint overlook regulatory sequences in an exhaustive analysis at phox2b Genome Res. 18 2008 252 260
36. T. Montavon, N. Soshnikova, B. Mascrez, E. Joye, L. Thevenet, E. Splinter, W. de Laat, F. Spitz, and D. Duboule A regulatory archipelago controls Hox genes transcription in digits Cell 147 2011 1132 1145
37. M. Navarro, and K. Gull A pol I transcriptional body associated with VSG mono-allelic expression in Trypanosoma brucei Nature 414 2001 759 763
38. S. Neph, A.B. Stergachis, A. Reynolds, R. Sandstrom, E. Borenstein, and J.A. Stamatoyannopoulos Circuitry and dynamics of human transcription factor regulatory networks Cell 150 2012 1274 1286
39. S. Neph, J. Vierstra, A.B. Stergachis, A.P. Reynolds, E. Haugen, B. Vernot, R.E. Thurman, S. John, R. Sandstrom, and A.K. Johnson An expansive human regulatory lexicon encoded in transcription factor footprints Nature 489 2012 83 90
40. H. Nishizumi, K. Kumasaka, N. Inoue, A. Nakashima, and H. Sakano Deletion of the core-H region in mice abolishes the expression of three proximal odorant receptor genes in cis Proc. Natl. Acad. Sci. USA 104 2007 20067 20072
41. I.K. Nolis, D.J. McKay, E. Mantouvalou, S. Lomvardas, M. Merika, and D. Thanos Transcription factors mediate long-range enhancer-promoter interactions Proc. Natl. Acad. Sci. USA 106 2009 20222 20227
42. D. Noordermeer, M. Leleu, P. Schorderet, E. Joye, F. Chabaud, and D. Duboule Temporal dynamics and developmental memory of 3D chromatin architecture at Hox gene loci eLife 3 2014 e02557
43. S. Ribich, B. Tasic, and T. Maniatis Identification of long-range regulatory elements in the protocadherin-alpha gene cluster Proc. Natl. Acad. Sci. USA 103 2006 19719 19724
44. A. Rothman, P. Feinstein, J. Hirota, and P. Mombaerts The promoter of the mouse odorant receptor gene M71 Mol. Cell. Neurosci. 28 2005 535 546
45. A.J. Ruthenburg, H. Li, T.A. Milne, S. Dewell, R.K. McGinty, M. Yuen, B. Ueberheide, Y. Dou, T.W. Muir, D.J. Patel, and C.D. Allis Recognition of a mononucleosomal histone modification pattern by BPTF via multivalent interactions Cell 145 2011 692 706
46. S. Serizawa, K. Miyamichi, H. Nakatani, M. Suzuki, M. Saito, Y. Yoshihara, and H. Sakano Negative feedback regulation ensures the one receptor-one olfactory neuron rule in mouse Science 302 2003 2088 2094
47. B.M. Shykind, S.C. Rohani, S. O'Donnell, A. Nemes, M. Mendelsohn, Y. Sun, R. Axel, and G. Barnea Gene switching and the stability of odorant receptor gene choice Cell 117 2004 801 815
48. R.P. Smith, S.J. Riesenfeld, A.K. Holloway, Q. Li, K.K. Murphy, N.M. Feliciano, L. Orecchia, N. Oksenberg, K.S. Pollard, and N. Ahituv A compact, in vivo screen of all 6-mers reveals drivers of tissue-specific expression and guides synthetic regulatory element design Genome Biol. 14 2013 R72
49. A.B. Stergachis, E. Haugen, A. Shafer, W. Fu, B. Vernot, A. Reynolds, A. Raubitschek, S. Ziegler, E.M. LeProust, and J.M. Akey Exonic transcription factor binding directs codon choice and affects protein evolution Science 342 2013 1367 1372
50. S.L. Sullivan, M.C. Adamson, K.J. Ressler, C.A. Kozak, and L.B. Buck The chromosomal distribution of mouse odorant receptor genes Proc. Natl. Acad. Sci. USA 93 1996 884 888
51. R.E. Thurman, E. Rynes, R. Humbert, J. Vierstra, M.T. Maurano, E. Haugen, N.C. Sheffield, A.B. Stergachis, H. Wang, and B. Vernot The accessible chromatin landscape of the human genome Nature 489 2012 75 82
52. A. Vassalli, P. Feinstein, and P. Mombaerts Homeodomain binding motifs modulate the probability of odorant receptor gene choice in transgenic mice Mol. Cell. Neurosci. 46 2011 381 396
53. F. Wang, A. Nemes, M. Mendelsohn, and R. Axel Odorant receptors govern the formation of a precise topographic map Cell 93 1998 47 60
54. A. Williams, C.G. Spilianakis, and R.A. Flavell Interchromosomal association and gene regulation in trans Trends Genet. 26 2010 188 197
55. J. Wysocka, T. Swigut, H. Xiao, T.A. Milne, S.Y. Kwon, J. Landry, M. Kauer, A.J. Tackett, B.T. Chait, and P. Badenhorst A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling Nature 442 2006 86 90
56. C. Zang, D.E. Schones, C. Zeng, K. Cui, K. Zhao, and W. Peng A clustering approach for identification of enriched domains from histone modification ChIP-Seq data Bioinformatics 25 2009 1952 1958
57. X. Zhang, I. Rodriguez, P. Mombaerts, and S. Firestein Odorant and vomeronasal receptor genes in two mouse genome assemblies Genomics 83 2004 802 811
58. Z. Zhou, and L. Belluscio Coding odorant concentration through activation timing between the medial and lateral olfactory bulb Cell Rep. 2 2012 1143 1150
59. T.L. Bailey, M. Boden, F.A. Buske, M. Frith, C.E. Grant, L. Clementi, J. Ren, W.W. Li, and W.S. Noble MEME SUITE: tools for motif discovery and searching Nucleic Acids Res. 37 2009 W202 W208
60. L. Buck, and R. Axel A novel multigene family may encode odorant receptors: a molecular basis for odor recognition Cell 65 1991 175 187
61. G.E. Crooks, G. Hon, J. Chandonia, and S.E. Brenner WebLogo: a sequence logo generator Genome Res. 14 2004 1188 1190
62. S. Gupta, J.A. Stamatoyannopoulos, T.L. Bailey, and W.S. Noble Quantifying similarity between motifs Genome Biol. 8 2007 R24 10.1186/gb-2007-8-2-r24
63. M. Imakaev, G. Fudenberg, R.P. Mccord, N. Naumova, A. Goloborodko, B.R. Lajoie, J. Dekker, and L.A. Mirny Iterative correction of Hi-C data reveals hallmarks of chromosome organization Nat. Methods 9 2012 999 1003
64. B. Langmead, and S.L. Salzberg Fast gapped-read alignment with Bowtie 2 Nat. Methods 9 2012 357 359 10.1038/nmeth.1923
65. B. Malnic, J. Hirono, T. Sato, and L.B. Buck Combinatorial receptor codes for odors Cell 96 1999 713 723 http://www.ncbi.nlm.nih.gov/pubmed/10089886
66. V. Matys, O.V. Kel-Margoulis, E. Fricke, I. Liebich, S. Land, A. Barre-Dirrie, I. Reuter, D. Chekmenev, M. Krull, and K. Hornischer TRANSFAC and its module TRANSCompel: transcriptional gene regulation in eukaryotes Nucleic Acids Res. 34 Database issue 2006 D108 D110
67. B.M. Shykind, S.C. Rohani, S. O'Donnell, A. Nemes, M. Mendelsohn, Y. Sun, R. Axel, and G. Barnea Gene switching and the stability of odorant receptor gene choice Cell 117 2004 801 815