Expression atlas of the multivalent epigenetic regulator Brpf1 and its requirement for survival of mouse embryos

Epigenetics

Volumn 9, Issue 6, 2014, Pages 860-872

  You, Linya ^a,b   Chen, Lulu ^c   Penney, Janice ^a   Miao, Dengshun ^c   Yang, Xiang Jiao ^a,b,d  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c NANJING MEDICAL UNIVERSITY   (China)

^d MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

Author keywords

BRPF1; Epigenetic reader; Histone acetyltransferase; KAT6A; KAT6B; KAT7

Indexed keywords

ACYLTRANSFERASE; BROMODOMAIN AND PHD FINGER CONTAINING PROTEIN 1; PEPTIDES AND PROTEINS; UNCLASSIFIED DRUG; BRPF1 PROTEIN, MOUSE; CARRIER PROTEIN; HBO1 PROTEIN, MOUSE; HISTONE ACETYLTRANSFERASE; MOZ PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; GENE; GENE EXPRESSION; GENE INACTIVATION; GENOTYPING TECHNIQUE; HBO1 GENE; HIPPOCAMPUS; MALE; MOLECULAR INTERACTION; MORF GENE; MOUSE; MOZ GENE; NONHUMAN; POSTNATAL DEVELOPMENT; PROTEIN EXPRESSION; PROTEIN INTERACTION; REAL TIME POLYMERASE CHAIN REACTION; SPINAL GANGLION; SUBICULUM; ANIMAL; ANTIBODY SPECIFICITY; C57BL MOUSE; EMBRYO DEATH; FETUS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; KNOCKOUT MOUSE; MAMMALIAN EMBRYO; METABOLISM;

ANIMALS; CARRIER PROTEINS; EMBRYO LOSS; EMBRYO, MAMMALIAN; EPIGENESIS, GENETIC; FEMALE; FETUS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HISTONE ACETYLTRANSFERASES; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; ORGAN SPECIFICITY;

EID: 84901812775     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.28530     Document Type: Article

References (56)

1. Taverna SD, Li H, Ruthenburg AJ, Allis CD, Patel DJ. How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers. Nat Struct Mol Biol 2007; 14:1025-40; PMID:17984965; http://dx.doi.org/10.1038/ nsmb1338
2. Latham JA, Dent SY. Cross-regulation of histone modifications. Nat Struct Mol Biol 2007; 14:1017-24; PMID:17984964; http://dx.doi.org/10.1038/ nsmb1307
3. Musselman CA, Lalonde ME, Côté J, Kutateladze TG. Perceiving the epigenetic landscape through histone readers. Nat Struct Mol Biol 2012; 19:1218-27; PMID:23211769; http://dx.doi.org/10.1038/ nsmb.2436
4. Yang XJ, Ullah M. MOZ and MORF, two large MYSTic HATs in normal and cancer stem cells. Oncogene 2007; 26:5408-19; PMID:17694082; http://dx.doi.org/10.1038/sj.onc.1210609
5. Klein BJ, Lalonde ME, Côté J, Yang XJ, Kutateladze TG. Crosstalk between epigenetic readers regulates the MOZ/MORF HAT complexes. Epigenetics 2014; 9:186-93; PMID:24169304; http://dx.doi. org/10.4161/epi.26792
6. Thompson KA, Wang B, Argraves WS, Giancotti FG, Schranck DP, Ruoslahti E. BR140, a novel zinc-finger protein with homology to the TAF250 subunit of TFIID. Biochem Biophys Res Commun 1994; 198:1143-52; PMID:7906940; http://dx.doi. org/10.1006/bbrc.1994.1162
7. Chaplin T, Bernard O, Beverloo HB, Saha V, Hagemeijer A, Berger R, Young BD. The t(10;11) translocation in acute myeloid leukemia (M5) consistently fuses the leucine zipper motif of AF10 onto the HRX gene. Blood 1995; 86:2073-6; PMID:7662954
8. Prasad R, Leshkowitz D, Gu Y, Alder H, Nakamura T, Saito H, Huebner K, Berger R, Croce CM, Canaani E. Leucine-zipper dimerization motif encoded by the AF17 gene fused to ALL-1 (MLL) in acute leukemia. Proc Natl Acad Sci U S A 1994; 91:8107-11; PMID:8058765; http://dx.doi.org/10.1073/ pnas.91.17.8107
9. Saha V, Chaplin T, Gregorini A, Ayton P, Young BD. The leukemia-associated-protein (LAP) domain, a cysteine-rich motif, is present in a wide range of proteins, including MLL, AF10, and MLLT6 proteins. Proc Natl Acad Sci U S A 1995; 92:9737-41; PMID:7568208; http://dx.doi.org/10.1073/ pnas.92.21.9737
10. Perry J. The Epc-N domain: a predicted protein-protein interaction domain found in select chromatin associated proteins. BMC Genomics 2006; 7:6; PMID:16412250; http://dx.doi. org/10.1186/1471-2164-7-6
11. McCullagh P, Chaplin T, Meerabux J, Grenzelias D, Lillington D, Poulsom R, Gregorini A, Saha V, Young BD. The cloning, mapping and expression of a novel gene, BRL, related to the AF10 leukaemia gene. Oncogene 1999; 18:7442-52; PMID:10602503; http://dx.doi.org/10.1038/sj.onc.1203117
12. Qin S, Jin L, Zhang J, Liu L, Ji P, Wu M, Wu J, Shi Y. Recognition of unmodified histone H3 by the first PHD finger of bromodomain-PHD finger protein 2 provides insights into the regulation of histone acetyltransferases monocytic leukemic zinc-finger protein (MOZ) and MOZ-related factor (MORF). J Biol Chem 2011; 286:36944-55; PMID:21880731; http://dx.doi.org/10.1074/jbc.M111.244400
13. Lalonde ME, Avvakumov N, Glass KC, Joncas FH, Saksouk N, Holliday M, Paquet E, Yan K, Tong Q, Klein BJ, et al. Exchange of associated factors directs a switch in HBO1 acetyltransferase histone tail specificity. Genes Dev 2013; 27:2009-24; PMID:24065767; http://dx.doi.org/10.1101/gad.223396.113
14. Liu L, Qin S, Zhang J, Ji P, Shi Y, Wu J. Solution structure of an atypical PHD finger in BRPF2 and its interaction with DNA. J Struct Biol 2012; 180:165-73; PMID:22820306; http://dx.doi.org/10.1016/j. jsb.2012.06.014
15. Poplawski A, Hu K, Lee W, Natesan S, Peng D, Carlson S, Shi X, Balaz S, Markley JL, Glass KC. Molecular Insights into the Recognition of N-Terminal Histone Modifications by the BRPF1 Bromodomain. J Mol Biol 2014; (forthcoming); PMID:24333487
16. Vezzoli A, Bonadies N, Allen MD, Freund SM, Santiveri CM, Kvinlaug BT, Huntly BJ, Göttgens B, Bycroft M. Molecular basis of histone H3K36me3 recognition by the PWWP domain of Brpf1. Nat Struct Mol Biol 2010; 17:617-9; PMID:20400950; http://dx.doi.org/10.1038/nsmb.1797
17. Wu H, Zeng H, Lam R, Tempel W, Amaya MF, Xu C, Dombrovski L, Qiu W, Wang Y, Min J. Structural and histone binding ability characterizations of human PWWP domains. PLoS One 2011; 6:e18919; PMID:21720545; http://dx.doi.org/10.1371/journal. pone.0018919
18. Doyon Y, Cayrou C, Ullah M, Landry AJ, Côté V, Selleck W, Lane WS, Tan S, Yang XJ, Côté J. ING tumor suppressor proteins are critical regulators of chromatin acetylation required for genome expression and perpetuation. Mol Cell 2006; 21:51-64; PMID:16387653; http://dx.doi.org/10.1016/j. molcel.2005.12.007
19. Ullah M, Pelletier N, Xiao L, Zhao SP, Wang K, Degerny C, Tahmasebi S, Cayrou C, Doyon Y, Goh SL, et al. Molecular architecture of quartet MOZ/ MORF histone acetyltransferase complexes. Mol Cell Biol 2008; 28:6828-43; PMID:18794358; http:// dx.doi.org/10.1128/MCB.01297-08
20. Saksouk N, Avvakumov N, Champagne KS, Hung T, Doyon Y, Cayrou C, Paquet E, Ullah M, Landry AJ, Côté V, et al. HBO1 HAT complexes target chromatin throughout gene coding regions via multiple PHD finger interactions with histone H3 tail. Mol Cell 2009; 33:257-65; PMID:19187766; http://dx.doi. org/10.1016/j.molcel.2009.01.007
21. Mishima Y, Miyagi S, Saraya A, Negishi M, Endoh M, Endo TA, Toyoda T, Shinga J, Katsumoto T, Chiba T, et al. The Hbo1-Brd1/Brpf2 complex is responsible for global acetylation of H3K14 and required for fetal liver erythropoiesis. Blood 2011; 118:2443-53; PMID:21753189; http://dx.doi. org/10.1182/blood-2011-01-331892
22. Lafon A, Chang CS, Scott EM, Jacobson SJ, Pillus L. MYST opportunities for growth control: yeast genes illuminate human cancer gene functions. Oncogene 2007; 26:5373-84; PMID:17694079; http://dx.doi. org/10.1038/sj.onc.1210606
23. Butler JS, Dent SY. The role of chromatin modifiers in normal and malignant hematopoiesis. Blood 2013; 121:3076-84; PMID:23287864; http://dx.doi. org/10.1182/blood-2012-10-451237
24. Kraft M, Cirstea IC, Voss AK, Thomas T, Goehring I, Sheikh BN, Gordon L, Scott H, Smyth GK, Ahmadian MR, et al. Disruption of the histone acetyltransferase MYST4 leads to a Noonan syndromelike phenotype and hyperactivated MAPK signaling in humans and mice. J Clin Invest 2011; 121:3479-91; PMID:21804188; http://dx.doi.org/10.1172/ JCI43428
25. Clayton-Smith J, O'Sullivan J, Daly S, Bhaskar S, Day R, Anderson B, Voss AK, Thomas T, Biesecker LG, Smith P, et al. Whole-exome-sequencing identifies mutations in histone acetyltransferase gene KAT6B in individuals with the Say-Barber-Biesecker variant of Ohdo syndrome. Am J Hum Genet 2011; 89:675-81; PMID:22077973; http://dx.doi. org/10.1016/j.ajhg.2011.10.008
26. Simpson MA, Deshpande C, Dafou D, Vissers LE, Woollard WJ, Holder SE, Gillessen-Kaesbach G, Derks R, White SM, Cohen-Snuijf R, et al. De novo mutations of the gene encoding the histone acetyltransferase KAT6B cause Genitopatellar syndrome. Am J Hum Genet 2012; 90:290-4; PMID:22265017; http://dx.doi.org/10.1016/j.ajhg.2011.11.024
27. Campeau PM, Kim JC, Lu JT, Schwartzentruber JA, Abdul-Rahman OA, Schlaubitz S, Murdock DM, Jiang MM, Lammer EJ, Enns GM, et al. Mutations in KAT6B, encoding a histone acetyltransferase, cause Genitopatellar syndrome. Am J Hum Genet 2012; 90:282-9; PMID:22265014; http://dx.doi. org/10.1016/j.ajhg.2011.11.023
28. Skarnes WC, Rosen B, West AP, Koutsourakis M, Bushell W, Iyer V, Mujica AO, Thomas M, Harrow J, Cox T, et al. A conditional knockout resource for the genome-wide study of mouse gene function. Nature 2011; 474:337-42; PMID:21677750; http://dx.doi. org/10.1038/nature10163
29. Testa G, Schaft J, van der Hoeven F, Glaser S, Anastassiadis K, Zhang Y, Hermann T, Stremmel W, Stewart AF. A reliable lacZ expression reporter cassette for multipurpose, knockout-first alleles. Genesis 2004; 38:151-8; PMID:15048813; http://dx.doi. org/10.1002/gene.20012
30. Pettitt SJ, Liang Q, Rairdan XY, Moran JL, Prosser HM, Beier DR, Lloyd KC, Bradley A, Skarnes WC. Agouti C57BL/6N embryonic stem cells for mouse genetic resources. Nat Methods 2009; 6:493-5; PMID:19525957; http://dx.doi.org/10.1038/ nmeth.1342
31. Katsumoto T, Aikawa Y, Iwama A, Ueda S, Ichikawa H, Ochiya T, Kitabayashi I. MOZ is essential for maintenance of hematopoietic stem cells. Genes Dev 2006; 20:1321-30; PMID:16702405; http://dx.doi. org/10.1101/gad.1393106
32. Thomas T, Corcoran LM, Gugasyan R, Dixon MP, Brodnicki T, Nutt SL, Metcalf D, Voss AK. Monocytic leukemia zinc finger protein is essential for the development of long-term reconstituting hematopoietic stem cells. Genes Dev 2006; 20:1175-86; PMID:16651658; http://dx.doi.org/10.1101/ gad.1382606
33. Deng W, Aimone JB, Gage FH. New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nat Rev Neurosci 2010; 11:339-50; PMID:20354534; http:// dx.doi.org/10.1038/nrn2822
34. Apps R, Garwicz M. Anatomical and physiological foundations of cerebellar information processing. Nat Rev Neurosci 2005; 6:297-311; PMID:15803161; http://dx.doi.org/10.1038/nrn1646
35. Sillitoe RV, Joyner AL. Morphology, molecular codes, and circuitry produce the three-dimensional complexity of the cerebellum. Annu Rev Cell Dev Biol 2007; 23:549-77; PMID:17506688; http://dx.doi. org/10.1146/annurev.cellbio.23.090506.123237
36. Lakso M, Pichel JG, Gorman JR, Sauer B, Okamoto Y, Lee E, Alt FW, Westphal H. Efficient in vivo manipulation of mouse genomic sequences at the zygote stage. Proc Natl Acad Sci U S A 1996; 93:5860-5; PMID:8650183; http://dx.doi.org/10.1073/ pnas.93.12.5860
37. Kranz A, Fu J, Duerschke K, Weidlich S, Naumann R, Stewart AF, Anastassiadis K. An improved Flp deleter mouse in C57Bl/6 based on Flpo recombinase. Genesis 2010; 48:512-20; PMID:20506501; http:// dx.doi.org/10.1002/dvg.20641
38. Perez-Campo FM, Borrow J, Kouskoff V, Lacaud G. The histone acetyl transferase activity of monocytic leukemia zinc finger is critical for the proliferation of hematopoietic precursors. Blood 2009; 113:4866-74; PMID:19264921; http://dx.doi.org/10.1182/ blood-2008-04-152017
39. Chamberlin HM, Thomas JH. The bromodomain protein LIN-49 and trithorax-related protein LIN-59 affect development and gene expression in Caenorhabditis elegans. Development 2000; 127:713-23; PMID:10648230
40. Chang S, Johnston RJ Jr., Hobert O. A transcriptional regulatory cascade that controls left/right asymmetry in chemosensory neurons of C. elegans. Genes Dev 2003; 17:2123-37; PMID:12952888; http://dx.doi. org/10.1101/gad.1117903
41. O'Meara MM, Zhang F, Hobert O. Maintenance of neuronal laterality in Caenorhabditis elegans through MYST histone acetyltransferase complex components LSY-12, LSY-13 and LIN-49. Genetics 2010; 186:1497-502; PMID:20923973; http://dx.doi. org/10.1534/genetics.110.123661
42. Laue K, Daujat S, Crump JG, Plaster N, Roehl HH, Kimmel CB, Schneider R, Hammerschmidt M; Tübingen 2000 Screen Consortium. The multidomain protein Brpf1 binds histones and is required for Hox gene expression and segmental identity. Development 2008; 135:1935-46; PMID:18469222; http://dx.doi.org/10.1242/dev.017160
43. Hibiya K, Katsumoto T, Kondo T, Kitabayashi I, Kudo A. Brpf1, a subunit of the MOZ histone acetyl transferase complex, maintains expression of anterior and posterior Hox genes for proper patterning of craniofacial and caudal skeletons. Dev Biol 2009; 329:176-90; PMID:19254709; http://dx.doi. org/10.1016/j.ydbio.2009.02.021
44. Deguchi K, Ayton PM, Carapeti M, Kutok JL, Snyder CS, Williams IR, Cross NC, Glass CK, Cleary ML, Gilliland DG. MOZ-TIF2-induced acute myeloid leukemia requires the MOZ nucleosome binding motif and TIF2-mediated recruitment of CBP. Cancer Cell 2003; 3:259-71; PMID:12676584; http://dx.doi.org/10.1016/S1535-6108(03)00051-5
45. Voss AK, Vanyai HK, Collin C, Dixon MP, McLennan TJ, Sheikh BN, Scambler P, Thomas T. MOZ regulates the Tbx1 locus, and Moz mutation partially phenocopies DiGeorge syndrome. Dev Cell 2012; 23:652-63; PMID:22921202; http://dx.doi. org/10.1016/j.devcel.2012.07.010
46. Miller CT, Maves L, Kimmel CB. moz regulates Hox expression and pharyngeal segmental identity in zebrafish. Development 2004; 131:2443-61; PMID:15128673; http://dx.doi.org/10.1242/ dev.01134
47. Crump JG, Swartz ME, Eberhart JK, Kimmel CB. Moz-dependent Hox expression controls segmentspecific fate maps of skeletal precursors in the face. Development 2006; 133:2661-9; PMID:16774997; http://dx.doi.org/10.1242/dev.02435
48. Thomas T, Voss AK, Chowdhury K, Gruss P. Querkopf, a MYST family histone acetyltransferase, is required for normal cerebral cortex development. Development 2000; 127:2537-48; PMID:10821753
49. Kueh AJ, Dixon MP, Voss AK, Thomas T. HBO1 is required for H3K14 acetylation and normal transcriptional activity during embryonic development. Mol Cell Biol 2011; 31:845-60; PMID:21149574; http://dx.doi.org/10.1128/MCB.00159-10
50. Nagy A, Gertsenstein M, Vintersten K, Behringer R. Staining Whole Mouse Embryos for beta-Galactosidase (lacZ) Activity. CSH Protoc 2007; 2007:t4725; PMID:21357067
51. Kim GW, Li L, Gorbani M, You L, Yang XJ. Mice lacking α-tubulin acetyltransferase 1 are viable but display α-tubulin acetylation deficiency and dentate gyrus distortion. J Biol Chem 2013; 288:20334-50; PMID:23720746; http://dx.doi.org/10.1074/jbc. M113.464792
52. Theiler K. (1989) The House Mouse-Atlas of Embryonic Development, Springer-Verlag, New York.
53. Kaufmann MH. (1994) The atlas of mouse development, Revised 1994 ed., Elsevier, Acadmic Press, Amsterdam, Boston, Heidelberg, London, Singapore, Tokyo.
54. Dong HW. (2008) Allen Reference Altas, a digital brain atlas of the C57BL/6J male mouse, John Wiley & Sons, Inc, Hoboken, New Jersey.
55. Paxinos G, Franklin KBJ. (2008) The Mouse Brain in Stereotaxic Coordinates, 3rd ed., Academic Press.
56. Paxinos G, Halliday GM, Watson C, Koutcherov Y, Wang H. (2006) Atlas of the Developing Mouse Brain at E17.5, P0 and P6, 1st Edition, Elsevier, Academic Press, Amsteram, Boston, Heidelberg, London, New York.