Abstract
Centromeric and pericentric regions have long been regarded as transcriptionally inert portions of chromosomes. A number of studies in the past 10 years disproved this dogma and provided convincing evidence that centromeric and pericentric sequences are transcriptionally active in several biological contexts.
In this chapter, we provide a comprehensive picture of the various contexts (cell growth and differentiation, stress, effect of chromatin organization) in which these sequences are expressed in mouse and human cells and discuss the possible functional implications of centromeric and pericentric sequences activation and/or of the resulting noncoding RNAs. Moreover, we provide an overview of the molecular mechanisms underlying the activation of centromeric and pericentromeric sequences as well as the structural features of encoded RNAs.
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References
Alastalo TP, Hellesuo M, Sandqvist A, Hietakangas V, Kallio M, Sistonen L (2003) Formation of nuclear stress granules involves HSF2 and coincides with the nucleolar localization of Hsp70. J Cell Sci 116:3557–3570
Allshire RC, Karpen GH (2008) Epigenetic regulation of centromeric chromatin: old dogs, new tricks? Nat Rev Genet 9:923–937
Biamonti G (2004) Nuclear stress bodies: a heterochromatin affair? Nat Rev Mol Cell Biol 5:493–498
Biamonti G, Vourc’h C (2010) Nuclear Stress Bodies Cold Spring Harb Perspect Biol. 2:a000695
Bouzinba-Segard H, Guais A, Francastel C (2006) Accumulation of small murine minor satellite transcripts leads to impaired centromeric architecture and function. Proc Natl Acad Sci USA 103:8709–8714
Chen ES, Zhang K, Nicolas E, Cam HP, Zofall M, Grewal SI (2008) Cell cycle control of centromeric repeat transcription and heterochromatin assembly. Nature 451:734–737
Chiodi I, Corioni M, Giordano M, Valgardsdottir R, Ghigna C, Cobianchi F, Xu RM, Riva S, Biamonti G (2004) RNA recognition motif 2 directs the recruitment of SF2/ASF to nuclear stress bodies. Nucleic Acids Res 32:4127–4136
Denegri M, Chiodi I, Corioni M, Cobianchi F, Riva S, Biamonti G (2001) Stress-induced nuclear bodies are sites of accumulation of pre-mRNA processing factors. Mol Biol Cell 12:3502–3514
Du Y, Topp CN, Dawe RK (2010) DNA binding of centromere protein C (CENPC) is stabilized by single-stranded RNA. PLoS Genet 6:e1000835
Ehrlich M (2003) The ICF syndrome, a DNA methyltransferase 3B deficiency and immunodeficiency disease. Clin Immunol 109:17–28
Enukashvily NI, Donev R, Waisertreiger IS, Podgornaya OI (2007) Human chromosome 1 satellite 3 DNA is decondensed, demethylated and transcribed in senescent cells and in A431 epithelial carcinoma cells. Cytogenet Genome Res 118:42–54
Eymery A, Callanan M, Vourc’h C (2009a) The secret message of heterochromatin: new insights into the mechanisms and function of centromeric and pericentric repeat sequence transcription. Int J Dev Biol 53:259–268
Eymery A, Horard B, El Atifi-Borel M, Fourel G, Berger F, Vitte AL, Van den Broeck A, Brambilla E, Fournier A, Callanan M, Gazzeri S, Khochbin S, Rousseaux S, Gilson E, Vourc’h C (2009b) A transcriptomic analysis of human centromeric and pericentric sequences in normal and tumor cells. Nucleic Acids Res 19:6340–6354
Eymery A, Souchier C, Vourc’h C, Jolly C (2010) Heat shock factor 1 binds to and transcribes satellite II and III sequences at several pericentromeric regions in heat-shocked cells. Exp Cell Res 316:1845–1855
Fernandes M, Xiao H, Lis JT (1994) Fine structure analyses of the Drosophila and Saccharomyces heat shock factor-heat shock element interactions. Nucleic Acids Res 22:167–173
Ferri F, Bouzinba-Segard H, Velasco G, Hubé F, Francastel C (2009) Non-coding murine centromeric transcripts associate with and potentiate Aurora B kinase. Nucleic Acids Res 37:5071–5080
Fisher AG, Merkenschlager M (2002) Gene silencing, cell fate and nuclear organisation. Curr Opin Genet Dev 12:193–197
Fournier A, McLeer-Florin A, Lefebvre C, Duley S, Barki L, Ribeyron J, Alboukadel K, Hamaidia S, Granjon A, Gressin R, Lajmanovich A, Bonnefoix T, Chauvelier S, Debernardi A, Rousseaux S, de Fraipont F, Figeac M, Kerckaert JP, De Vos J, Usson Y, Delaval K, Grichine A, Vourc’h C, Khochbin S, Feil R, Leroux D, Callanan MB (2010) 1q12 chromosome translocations form aberrant heterochromatic foci associated with changes in nuclear architecture and gene expression in B cell lymphoma. EMBO Mol Med 2:159–171
Frescas D, Guardavaccaro D, Kuchay SM, Kato H, Poleshko A, Basrur V, Elenitoba-Johnson KS, Katz RA, Pagano M (2008) KDM2A represses transcription of centromeric satellite repeats and maintains the heterochromatic state. Cell Cycle 7:3539–3547
Frommer M, Prosser J, Tkachuk D, Reisner AH, Vincent PC (1982) Simple repeated sequences in human satellite DNA. Nucleic Acids Res 10:547–563
Frommer M, Paul C, Vincent PC (1988) Localisation of satellite DNA sequences on human metaphase chromosomes using bromodeoxyuridine. Chromosoma 97:11
Fukagawa T, Nogami M, Yoshikawa M, Ikeno M, Okazaki T, Takami Y, Nakayama T, Oshimura M (2004) Dicer is essential for formation of the heterochromatin structure in vertebrate cells. Nat Cell Biol 6:784–791
Fuks F, Hurd PJ, Wolf D, Nan X, Bird AP, Kouzarides T (2003) The methyl-CpG-binding protein MeCP2 links DNA methylation to histone methylation. J Biol Chem 278:4035–4040
Gaubatz JW, Cutler RG (1990) Mouse satellite DNA is transcribed in senescent cardiac muscle. J Biol Chem 265:17753–17758
Goldman RD, Shumaker DK, Erdos MR, Eriksson M, Goldman AE, Gordon LB, Gruenbaum Y, Khuon S, Mendez M, Varga R, Collins FS (2004) Accumulation of mutant lamin A causes progressive changes in nuclear architecture in Hutchinson-Gilford progeria syndrome. Proc Natl Acad Sci USA 101:8963–8968
Grewal SI, Elgin SC (2007) Transcription and RNA interference in the formation of heterochromatin. Nature 447:399–406
Jehan Z, Vallinayagam S, Tiwari S, Pradhan S, Singh L, Suresh A, Reddy HM, Ahuja YR, Jesudasan RA (2007) Novel noncoding RNA from human Y distal heterochromatic block (Yq12) generates testis-specific chimeric CDC2L2. Genome Res 17:433–440
Jolly C, Lakhotia SC (2006) Human sat III and Drosophila hsr omega transcripts: a common paradigm for regulation of nuclear RNA processing in stressed cells. Nucleic Acids Res 34:5508–5514
Jolly C, Konecny L, Grady DL, Kutskova YA, Cotto JJ, Morimoto RI, Vourc’h C (2002) In vivo binding of active heat shock transcription factor 1 to human chromosome 9 heterochromatin during stress. J Cell Biol 156:775–781
Jolly C, Metz A, Govin J, Vigneron M, Turner BM, Khochbin S, Vourc’h C (2004) Stress-induced transcription of satellite III repeats. J Cell Biol 164:25–33
Jones KW, Purdom IF, Prosser J, Corneo G (1974) The chromosomal localisation of human satellite DNA I. Chromosoma 49:161–171
Kanellopoulou C, Muljo SA, Kung AL, Ganesan S, Drapkin R, Jenuwein T, Livingston DM, Rajewsky K (2005) Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes Dev 19:489–501
Lehnertz B, Ueda Y, Derijck AA, Braunschweig U, Perez-Burgos L, Kubicek S, Chen T, Li E, Jenuwein T, Peters AH (2003) Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin. Curr Biol 13:1192–1200
Lu J, Gilbert DM (2007) Proliferation-dependent and cell cycle regulated transcription of mouse pericentric heterochromatin. J Cell Biol 179:411–21
Lu J, Gilbert DM (2008) Cell cycle regulated transcription of heterochromatin in mammals vs. fission yeast: functional conservation or coincidence? Cell Cycle 7:1907–1910
Maison C, Bailly D, Peters AH, Quivy JP, Roche D, Taddei A, Lachner M, Jenuwein T, Almouzni G (2002) Higher-order structure in pericentric heterochromatin involves a distinct pattern of histone modification and an RNA component. Nat Genet 30:329–334
Manuelidis L (1982) Nucleotide sequence definition of a major human repeated DNA, the Hind III 1.9 kb family. Nucleic Acids Res 10(10):3211–3219
Martens JH, O’Sullivan RJ, Braunschweig U, Opravil S, Radolf M, Steinlein P, Jenuwein T (2005) The profile of repeat-associated histone lysine methylation states in the mouse epigenome. EMBO J 24:800–801
Massé J, Laurent A, Nicol B, Guerrier D, Pellerin I, Deschamps S (2010) Involvement of ZFPIP/Zfp462 in chromatin integrity and survival of P19 pluripotent cells. Exp Cell Res 316:1190–1201
Masui O, Heard E (2006) RNA and protein actors in X-chromosome inactivation. Cold Spring Harb Symp Quant Biol 71:419–428
Metz A, Soret J, Vourc’h C, Tazi J, Jolly C (2004) A key role for stress-induced satellite III transcripts in the relocalization of splicing factors into nuclear stress granules. J Cell Sci 117:4551–4558
Meyne J, Goodwin EH, Moyzis RK (1994) Chromosome localization and orientation of the simple sequence repeat of human satellite I DNA. Chromosoma 103:99
Misteli T, Scaffidi P (2005) Genome instability in progeria: when repair gets old. Nat Med 7:718–719
Mitchell AR, Beauchamp RS, Bostock CJ (1979) A study of sequence homologies in four satellite DNAs of man. J Mol Biol 135:127–149
Morimoto RI (1998) Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev 12:3788–3796
Muchardt C, Guilleme M, Seeler JS, Trouche D, Dejean A, Yaniv M (2002) Coordinated methyl and RNA binding is required for heterochromatin localization of mammalian HP1alpha. EMBO Rep 3:975–981
Nan X, Ng HH, Johnson CA, Laherty CD, Turner BM, Eisenman RN, Bird A (1998a) Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393:386–389
Nan X, Cross S, Bird A (1998b) Gene silencing by methyl-CpG-binding proteins. Novartis Found Symp 214:6–16
Papait R, Pistore C, Negri D, Pecoraro D, Cantarini L, Bonapace IM (2007) Np95 is implicated in pericentromeric heterochromatin replication and in major satellite silencing. Mol Biol Cell 18:1098–1106
Prosser J, Frommer M, Paul C, Vincent PC (1986) Sequence relationships of three human satellite DNAs. J Mol Biol 187:145–155
Rizzi N, Denegri M, Chiodi I, Corioni M, Valgardsdottir R, Cobianchi F, Riva S, Biamonti G (2004) Transcriptional activation of a constitutive heterochromatic domain of the human genome in response to heat shock. Mol Biol Cell 15:543–551
Rudert F, Gronemeyer H (1993) Retinoic acid-response elements with a highly repetitive structure isolated by immuno-selection from genomic DNA. J Steroid Biochem Mol Biol 46:121–133
Rudert F, Bronner S, Garnier JM, Dolle P (1995) Transcripts from opposite strands of gamma satellite DNA are differentially expressed during mouse development. Mamm Genome 6:76–83
Sandqvist A, Björk JK, Akerfelt M, Chitikova Z, Grichine A, Vourc’h C, Jolly C, Salminen TA, Nymalm Y, Sistonen L (2009) Heterotrimerization of heat-shock factors 1 and 2 provides a transcriptional switch in response to distinct stimuli. Mol Biol Cell 5:1340–1347
Sengupta S, Parihar R, Ganesh S (2009) Satellite III non-coding RNAs show distinct and stress-specific patterns of induction. Biochem Biophys Res Commun 382:102–107
Shumaker DK, Dechat T, Kohlmaier A, Adam SA, Bozovsky MR, Erdos MR, Eriksson M, Goldman AE, Khuon S, Collins FS, Jenuwein T, Goldman RD (2006) Mutant nuclear lamin A leads to progressive alterations of epigenetic control in premature aging. Proc Natl Acad Sci USA 103:8703–8708
Tagarro I, Wiegant J, Raap AK, González-Aguilera JJ, Fernández-Peralta AM (1994) Assignment of human satellite 1 DNA as revealed by fluorescent in situ hybridization with oligonucleotides. Hum Genet 93:125–128
Talbert PB, Henikoff S (2006) Spreading of silent chromatin: inaction at a distance. Nat Rev Genet 7:793–803
Terranova R, Sauer S, Merkenschlager M, Fisher AG (2005) The reorganisation of constitutive heterochromatin in differentiating muscle requires HDAC activity. Exp Cell Res 310:344–356
Ugarković Đ (2009) Centromere-competent DNA: structure and evolution. Prog Mol Subcell Biol 48:53–76
Valgardsdottir R, Chiodi I, Giordano M, Rossi A, Bazzini S, Ghigna C, Riva S, Biamonti G (2007) Transcription of Satellite III non-coding RNAs is a general stress response in human cells. Nucleic Acids Res 36:423–434
Verdel A, Vavasseur A, Le Gorrec M, Touat-Todeschini L (2009) Common themes in siRNA-mediated epigenetic silencing pathways. Int J Dev Biol 53:245–257
Vissel JB, Choo KH (1987) Human alpha satellite DNA – consensus sequence and conserved regions. Nucleic Acids Res 15:6751–6752
Weighardt F, Cobianchi F, Cartegni L, Chiodi I, Villa A, Riva S, Biamonti G (1999) A novel hnRNP protein (HAP/SAF-B) enters a subset of hnRNP complexes and relocates in nuclear granules in response to heat shock. J Cell Sci 112:1465–1476
Wong AK, Rattner JB (1988) Sequence organization and cytological localization of the minor satellite of mouse. Nucleic Acids Res 16:11645–11661
Wong LH, Brettingham-Moore KH, Chan L, Quach JM, Anderson MA, Northrop EL, Hannan R, Saffery R, Shaw ML, Williams E, Choo KH (2007) Centromere RNA is a key component for the assembly of nucleoproteins at the nucleolus and centromere. Genome Res 17:1146–1160
Acknowledgments
Work in the team of Claire Vourc’h is supported by grants from by ARC (#5113) and by ANR (PCV08_324703). G. Biamonti is supported by grants from AIRC, Cariplo Foundation, and from European Union (EURASNET) Network of Excellence on Alternative Splicing (EURASNET).
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Vourc’h, C., Biamonti, G. (2011). Transcription of Satellite DNAs in Mammals. In: Ugarkovic, D. (eds) Long Non-Coding RNAs. Progress in Molecular and Subcellular Biology(), vol 51. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-16502-3_5
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DOI: https://doi.org/10.1007/978-3-642-16502-3_5
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