Emerging Principles of Gene Expression Programs and Their Regulation

Molecular Cell

Volumn 71, Issue 3, 2018, Pages 389-397

  Pope, Scott D ^a   Medzhitov, Ruslan ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; GENETIC TRANSCRIPTION; ANIMAL; ANTIBODY SPECIFICITY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

TRANSCRIPTION FACTOR; TRANSCRIPTOME;

ANIMALS; GENE EXPRESSION REGULATION; HUMANS; ORGAN SPECIFICITY; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSCRIPTOME;

EID: 85050291252     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2018.07.017     Document Type: Review

References (69)

1. Adelman, K., Lis, J.T., Promoter-proximal pausing of RNA polymerase II: emerging roles in metazoans. Nat. Rev. Genet. 13 (2012), 720–731.
2. Amit, I., Regev, A., Hacohen, N., Strategies to discover regulatory circuits of the mammalian immune system. Nat. Rev. Immunol. 11 (2011), 873–880.
3. Andersson, R., Sandelin, A., Danko, C.G., A unified architecture of transcriptional regulatory elements. Trends Genet. 31 (2015), 426–433.
4. Arendt, D., Musser, J.M., Baker, C.V.H., Bergman, A., Cepko, C., Erwin, D.H., Pavlicev, M., Schlosser, G., Widder, S., Laubichler, M.D., Wagner, G.P., The origin and evolution of cell types. Nat. Rev. Genet. 17 (2016), 744–757.
5. Arnold, H.H., Braun, T., Targeted inactivation of myogenic factor genes reveals their role during mouse myogenesis: a review. Int. J. Dev. Biol. 40 (1996), 345–353.
6. Blum, R., Vethantham, V., Bowman, C., Rudnicki, M., Dynlacht, B.D., Genome-wide identification of enhancers in skeletal muscle: the role of MyoD1. Genes Dev. 26 (2012), 2763–2779.
7. Buenrostro, J.D., Giresi, P.G., Zaba, L.C., Chang, H.Y., Greenleaf, W.J., Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat. Methods 10 (2013), 1213–1218.
8. Cairns, B.R., The logic of chromatin architecture and remodelling at promoters. Nature 461 (2009), 193–198.
9. Cipolletta, D., Feuerer, M., Li, A., Kamei, N., Lee, J., Shoelson, S.E., Benoist, C., Mathis, D., PPAR-γ is a major driver of the accumulation and phenotype of adipose tissue Treg cells. Nature 486 (2012), 549–553.
10. Curina, A., Termanini, A., Barozzi, I., Prosperini, E., Simonatto, M., Polletti, S., Silvola, A., Soldi, M., Austenaa, L., Bonaldi, T., et al. High constitutive activity of a broad panel of housekeeping and tissue-specific cis-regulatory elements depends on a subset of ETS proteins. Genes Dev. 31 (2017), 399–412.
11. Davies, L.C., Jenkins, S.J., Allen, J.E., Taylor, P.R., Tissue-resident macrophages. Nat. Immunol. 14 (2013), 986–995.
12. Deaton, A.M., Bird, A., CpG islands and the regulation of transcription. Genes Dev. 25 (2011), 1010–1022.
13. Fan, X., Rudensky, A.Y., Hallmarks of Tissue-Resident Lymphocytes. Cell 164 (2016), 1198–1211.
14. Foster, S.L., Hargreaves, D.C., Medzhitov, R., Gene-specific control of inflammation by TLR-induced chromatin modifications. Nature 447 (2007), 972–978.
15. Fowler, T., Sen, R., Roy, A.L., Regulation of primary response genes. Mol. Cell 44 (2011), 348–360.
16. Fullwood, M.J., Liu, M.H., Pan, Y.F., Liu, J., Xu, H., Mohamed, Y.B., Orlov, Y.L., Velkov, S., Ho, A., Mei, P.H., et al. An oestrogen-receptor-alpha-bound human chromatin interactome. Nature 462 (2009), 58–64.
17. Ghisletti, S., Barozzi, I., Mietton, F., Polletti, S., De Santa, F., Venturini, E., Gregory, L., Lonie, L., Chew, A., Wei, C.L., et al. Identification and characterization of enhancers controlling the inflammatory gene expression program in macrophages. Immunity 32 (2010), 317–328.
18. Glass, C.K., Natoli, G., Molecular control of activation and priming in macrophages. Nat. Immunol. 17 (2016), 26–33.
19. Gordon, S., Akopyan, G., Garban, H., Bonavida, B., Transcription factor YY1: structure, function, and therapeutic implications in cancer biology. Oncogene 25 (2006), 1125–1142.
20. Graf, T., Enver, T., Forcing cells to change lineages. Nature 462 (2009), 587–594.
21. Hargreaves, D.C., Horng, T., Medzhitov, R., Control of inducible gene expression by signal-dependent transcriptional elongation. Cell 138 (2009), 129–145.
22. Heinz, S., Romanoski, C.E., Benner, C., Glass, C.K., The selection and function of cell type-specific enhancers. Nat. Rev. Mol. Cell Biol. 16 (2015), 144–154.
23. Holmberg, J., Perlmann, T., Maintaining differentiated cellular identity. Nat. Rev. Genet. 13 (2012), 429–439.
24. Joseph, S.B., Castrillo, A., Laffitte, B.A., Mangelsdorf, D.J., Tontonoz, P., Reciprocal regulation of inflammation and lipid metabolism by liver X receptors. Nat. Med. 9 (2003), 213–219.
25. Kaczynski, J., Cook, T., Urrutia, R., Sp1- and Krüppel-like transcription factors. Genome Biol., 4, 2003, 206.
26. Kim, H.D., Shay, T., O'Shea, E.K., Regev, A., Transcriptional regulatory circuits: predicting numbers from alphabets. Science 325 (2009), 429–432.
27. Kohyama, M., Ise, W., Edelson, B.T., Wilker, P.R., Hildner, K., Mejia, C., Frazier, W.A., Murphy, T.L., Murphy, K.M., Role for Spi-C in the development of red pulp macrophages and splenic iron homeostasis. Nature 457 (2009), 318–321.
28. Levchenko, A., Nemenman, I., Cellular noise and information transmission. Curr. Opin. Biotechnol. 28 (2014), 156–164.
29. Liao, X., Sharma, N., Kapadia, F., Zhou, G., Lu, Y., Hong, H., Paruchuri, K., Mahabeleshwar, G.H., Dalmas, E., Venteclef, N., et al. Krüppel-like factor 4 regulates macrophage polarization. J. Clin. Invest. 121 (2011), 2736–2749.
30. Lieberman-Aiden, E., van Berkum, N.L., Williams, L., Imakaev, M., Ragoczy, T., Telling, A., Amit, I., Lajoie, B.R., Sabo, P.J., Dorschner, M.O., et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326 (2009), 289–293.
31. Lin, C.Y., Lovén, J., Rahl, P.B., Paranal, R.M., Burge, C.B., Bradner, J.E., Lee, T.I., Young, R.A., Transcriptional amplification in tumor cells with elevated c-Myc. Cell 151 (2012), 56–67.
32. Link, V.M., Gosselin, D., Glass, C.K., Mechanisms Underlying the Selection and Function of Macrophage-Specific Enhancers. Cold Spring Harb. Symp. Quant. Biol. 80 (2015), 213–221.
33. Litvak, V., Ramsey, S.A., Rust, A.G., Zak, D.E., Kennedy, K.A., Lampano, A.E., Nykter, M., Shmulevich, I., Aderem, A., Function of C/EBPdelta in a regulatory circuit that discriminates between transient and persistent TLR4-induced signals. Nat. Immunol. 10 (2009), 437–443.
34. Macosko, E.Z., Basu, A., Satija, R., Nemesh, J., Shekhar, K., Goldman, M., Tirosh, I., Bialas, A.R., Kamitaki, N., Martersteck, E.M., et al. Highly Parallel Genome-wide Expression Profiling of Individual Cells Using Nanoliter Droplets. Cell 161 (2015), 1202–1214.
35. Mottis, A., Mouchiroud, L., Auwerx, J., Emerging roles of the corepressors NCoR1 and SMRT in homeostasis. Genes Dev. 27 (2013), 819–835.
36. Mumbach, M.R., Rubin, A.J., Flynn, R.A., Dai, C., Khavari, P.A., Greenleaf, W.J., Chang, H.Y., HiChIP: efficient and sensitive analysis of protein-directed genome architecture. Nat. Methods 13 (2016), 919–922.
37. Naik, S., Larsen, S.B., Gomez, N.C., Alaverdyan, K., Sendoel, A., Yuan, S., Polak, L., Kulukian, A., Chai, S., Fuchs, E., Inflammatory memory sensitizes skin epithelial stem cells to tissue damage. Nature 550 (2017), 475–480.
38. Natoli, G., Ghisletti, S., Barozzi, I., The genomic landscapes of inflammation. Genes Dev. 25 (2011), 101–106.
39. Netea, M.G., Joosten, L.A., Latz, E., Mills, K.H., Natoli, G., Stunnenberg, H.G., O'Neill, L.A., Xavier, R.J., Trained immunity: A program of innate immune memory in health and disease. Science, 352, 2016, aaf1098.
40. Nie, Z., Hu, G., Wei, G., Cui, K., Yamane, A., Resch, W., Wang, R., Green, D.R., Tessarollo, L., Casellas, R., et al. c-Myc is a universal amplifier of expressed genes in lymphocytes and embryonic stem cells. Cell 151 (2012), 68–79.
41. Nish, S.A., Lin, W.W., Reiner, S.L., Lymphocyte Fate and Metabolism: A Clonal Balancing Act. Trends Cell Biol. 27 (2017), 946–954.
42. Okabe, Y., Medzhitov, R., Tissue-specific signals control reversible program of localization and functional polarization of macrophages. Cell 157 (2014), 832–844.
43. Okabe, Y., Medzhitov, R., Tissue biology perspective on macrophages. Nat. Immunol. 17 (2016), 9–17.
44. Picelli, S., Faridani, O.R., Björklund, A.K., Winberg, G., Sagasser, S., Sandberg, R., Full-length RNA-seq from single cells using Smart-seq2. Nat. Protoc. 9 (2014), 171–181.
45. Pombo, A., Dillon, N., Three-dimensional genome architecture: players and mechanisms. Nat. Rev. Mol. Cell Biol. 16 (2015), 245–257.
46. Ramirez-Carrozzi, V.R., Nazarian, A.A., Li, C.C., Gore, S.L., Sridharan, R., Imbalzano, A.N., Smale, S.T., Selective and antagonistic functions of SWI/SNF and Mi-2beta nucleosome remodeling complexes during an inflammatory response. Genes Dev. 20 (2006), 282–296.
47. Ramirez-Carrozzi, V.R., Braas, D., Bhatt, D.M., Cheng, C.S., Hong, C., Doty, K.R., Black, J.C., Hoffmann, A., Carey, M., Smale, S.T., A unifying model for the selective regulation of inducible transcription by CpG islands and nucleosome remodeling. Cell 138 (2009), 114–128.
48. Ramsey, S.A., Klemm, S.L., Zak, D.E., Kennedy, K.A., Thorsson, V., Li, B., Gilchrist, M., Gold, E.S., Johnson, C.D., Litvak, V., et al. Uncovering a macrophage transcriptional program by integrating evidence from motif scanning and expression dynamics. PLoS Comput. Biol., 4, 2008, e1000021.
49. Raser, J.M., O'Shea, E.K., Noise in gene expression: origins, consequences, and control. Science 309 (2005), 2010–2013.
50. Ricote, M., Li, A.C., Willson, T.M., Kelly, C.J., Glass, C.K., The peroxisome proliferator-activated receptor-gamma is a negative regulator of macrophage activation. Nature 391 (1998), 79–82.
51. Rosenfeld, M.G., Lunyak, V.V., Glass, C.K., Sensors and signals: a coactivator/corepressor/epigenetic code for integrating signal-dependent programs of transcriptional response. Genes Dev. 20 (2006), 1405–1428.
52. Satoh, T., Takeuchi, O., Vandenbon, A., Yasuda, K., Tanaka, Y., Kumagai, Y., Miyake, T., Matsushita, K., Okazaki, T., Saitoh, T., et al. The Jmjd3-Irf4 axis regulates M2 macrophage polarization and host responses against helminth infection. Nat. Immunol. 11 (2010), 936–944.
53. Scarpulla, R.C., Transcriptional activators and coactivators in the nuclear control of mitochondrial function in mammalian cells. Gene 286 (2002), 81–89.
54. Shalek, A.K., Satija, R., Shuga, J., Trombetta, J.J., Gennert, D., Lu, D., Chen, P., Gertner, R.S., Gaublomme, J.T., Yosef, N., et al. Single-cell RNA-seq reveals dynamic paracrine control of cellular variation. Nature 510 (2014), 363–369.
55. Smale, S.T., Natoli, G., Transcriptional control of inflammatory responses. Cold Spring Harb. Perspect. Biol., 6, 2014, a016261.
56. Smale, S.T., Plevy, S.E., Weinmann, A.S., Zhou, L., Ramirez-Carrozzi, V.R., Pope, S.D., Bhatt, D.M., Tong, A.J., Toward an understanding of the gene-specific and global logic of inducible gene transcription. Cold Spring Harb. Symp. Quant. Biol. 78 (2013), 61–68.
57. Smale, S.T., Tarakhovsky, A., Natoli, G., Chromatin contributions to the regulation of innate immunity. Annu. Rev. Immunol. 32 (2014), 489–511.
58. Smyth, G.K., Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol., 3, 2004, e3.
59. Soshnev, A.A., Josefowicz, S.Z., Allis, C.D., Greater Than the Sum of Parts: Complexity of the Dynamic Epigenome. Mol. Cell 62 (2016), 681–694.
60. Spiegelman, B.M., Heinrich, R., Biological control through regulated transcriptional coactivators. Cell 119 (2004), 157–167.
61. Thompson, D., Regev, A., Roy, S., Comparative analysis of gene regulatory networks: from network reconstruction to evolution. Annu. Rev. Cell Dev. Biol. 31 (2015), 399–428.
62. Tong, A.J., Liu, X., Thomas, B.J., Lissner, M.M., Baker, M.R., Senagolage, M.D., Allred, A.L., Barish, G.D., Smale, S.T., A Stringent Systems Approach Uncovers Gene-Specific Mechanisms Regulating Inflammation. Cell 165 (2016), 165–179.
63. Urbánek, P., Wang, Z.Q., Fetka, I., Wagner, E.F., Busslinger, M., Complete block of early B cell differentiation and altered patterning of the posterior midbrain in mice lacking Pax5/BSAP. Cell 79 (1994), 901–912.
64. Weake, V.M., Workman, J.L., Inducible gene expression: diverse regulatory mechanisms. Nat. Rev. Genet. 11 (2010), 426–437.
65. Wynn, T.A., Chawla, A., Pollard, J.W., Macrophage biology in development, homeostasis and disease. Nature 496 (2013), 445–455.
66. Ying, Q.L., Nichols, J., Chambers, I., Smith, A., BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3. Cell 115 (2003), 281–292.
67. Yosef, N., Regev, A., Impulse control: temporal dynamics in gene transcription. Cell 144 (2011), 886–896.
68. Yosef, N., Regev, A., Writ large: Genomic dissection of the effect of cellular environment on immune response. Science 354 (2016), 64–68.
69. Yosef, N., Shalek, A.K., Gaublomme, J.T., Jin, H., Lee, Y., Awasthi, A., Wu, C., Karwacz, K., Xiao, S., Jorgolli, M., et al. Dynamic regulatory network controlling TH17 cell differentiation. Nature 496 (2013), 461–468.