1932

Abstract

The p-arms of the five human acrocentric chromosomes bear nucleolar organizer regions (NORs) comprising ribosomal gene (rDNA) repeats that are organized in a homogeneous tandem array and transcribed in a telomere-to-centromere direction. Precursor ribosomal RNA transcripts are processed and assembled into ribosomal subunits, the nucleolus being the physical manifestation of this process. I review current understanding of nucleolar chromosome biology and describe current exploration into a role for the NOR chromosomal context. Full DNA sequences for acrocentric p-arms are now emerging, aided by the current revolution in long-read sequencing and genome assembly. Acrocentric p-arms vary from 10.1 to 16.7 Mb, accounting for ∼2.2% of the genome. Bordering rDNA arrays, distal junctions, and proximal junctions are shared among the p-arms, with distal junctions showing evidence of functionality. The remaining p-arm sequences comprise multiple satellite DNA classes and segmental duplications that facilitate recombination between heterologous chromosomes, which is likely also involved in Robertsonian translocations.

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2023-08-25
2024-04-14
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Literature Cited

  1. 1.
    Agrawal S, Ganley ARD. 2018. The conservation landscape of the human ribosomal RNA gene repeats. PLOS ONE 13:e0207531
    [Google Scholar]
  2. 2.
    Akamatsu Y, Kobayashi T. 2015. The human RNA polymerase I transcription terminator complex acts as a replication fork barrier that coordinates the progress of replication with rRNA transcription activity. Mol. Cell. Biol. 35:1871–81
    [Google Scholar]
  3. 3.
    Altemose N. 2022. A classical revival: human satellite DNAs enter the genomics era. Semin. Cell Dev. Biol. 128:2–14
    [Google Scholar]
  4. 4.
    Altemose N, Logsdon GA, Bzikadze AV, Sidhwani P, Langley SA et al. 2022. Complete genomic and epigenetic maps of human centromeres. Science 376:eabl4178
    [Google Scholar]
  5. 5.
    Antonarakis SE. 2022. Short arms of human acrocentric chromosomes and the completion of the human genome sequence. Genome Res. 32:599–607
    [Google Scholar]
  6. 6.
    Bandyopadhyay R, Heller A, Knox-DuBois C, McCaskill C, Berend SA et al. 2002. Parental origin and timing of de novo Robertsonian translocation formation. Am. J. Hum. Genet. 71:1456–62
    [Google Scholar]
  7. 7.
    Barr ML, Bertram EG. 1949. A morphological distinction between neurones of the male and female, and the behaviour of the nucleolar satellite during accelerated nucleoprotein synthesis. Nature 163:676–77
    [Google Scholar]
  8. 8.
    Bartsch I, Schoneberg C, Grummt I. 1988. Purification and characterization of TTFI, a factor that mediates termination of mouse ribosomal DNA transcription. Mol. Cell. Biol. 8:3891–97
    [Google Scholar]
  9. 9.
    Bassett AR, Akhtar A, Barlow DP, Bird AP, Brockdorff N et al. 2014. Considerations when investigating lncRNA function in vivo. eLife 3:e03058
    [Google Scholar]
  10. 10.
    Bizhanova A, Kaufman PD. 2021. Close to the edge: heterochromatin at the nucleolar and nuclear peripheries. Biochim. Biophys. Acta Gene Regul. Mech. 1864:194666
    [Google Scholar]
  11. 11.
    Bolcun-Filas E, Handel MA. 2018. Meiosis: the chromosomal foundation of reproduction. Biol. Reprod. 99:112–26
    [Google Scholar]
  12. 12.
    Borsos M, Torres-Padilla ME. 2016. Building up the nucleus: nuclear organization in the establishment of totipotency and pluripotency during mammalian development. Genes Dev. 30:611–21
    [Google Scholar]
  13. 13.
    Brangwynne CP, Mitchison TJ, Hyman AA. 2011. Active liquid-like behavior of nucleoli determines their size and shape in Xenopus laevis oocytes. PNAS 108:4334–39
    [Google Scholar]
  14. 14.
    Caburet S, Conti C, Schurra C, Lebofsky R, Edelstein SJ, Bensimon A. 2005. Human ribosomal RNA gene arrays display a broad range of palindromic structures. Genome Res. 15:1079–85
    [Google Scholar]
  15. 15.
    Choo KH, Vissel B, Brown R, Filby RG, Earle E 1988. Homologous alpha satellite sequences on human acrocentric chromosomes with selectivity for chromosomes 13, 14 and 21: implications for recombination between nonhomologues and Robertsonian translocations. Nucleic Acids Res. 16:1273–84
    [Google Scholar]
  16. 16.
    Cremer T, Cremer M. 2010. Chromosome territories. Cold Spring Harb. Perspect. Biol. 2:a003889
    [Google Scholar]
  17. 17.
    Cuthbert AP, Trott DA, Ekong RM, Jezzard S, England NL et al. 1995. Construction and characterization of a highly stable human: rodent monochromosomal hybrid panel for genetic complementation and genome mapping studies. Cytogenet. Cell Genet. 71:68–76
    [Google Scholar]
  18. 18.
    de Wit E, Vos ES, Holwerda SJ, Valdes-Quezada C, Verstegen MJ et al. 2015. CTCF binding polarity determines chromatin looping. Mol. Cell 60:676–84
    [Google Scholar]
  19. 19.
    Denton TE, Howell WM, Barrett JV. 1976. Human nucleolar organizer chromosomes: satellite associations. Chromosoma 55:81–84
    [Google Scholar]
  20. 20.
    Epstein ND, Karlsson S, O'Brien S, Modi W, Moulton A, Nienhuis AW 1987. A new moderately repetitive DNA sequence family of novel organization. Nucleic Acids Res. 15:2327–41
    [Google Scholar]
  21. 21.
    Ernst J, Kheradpour P, Mikkelsen TS, Shoresh N, Ward LD et al. 2011. Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 473:43–49
    [Google Scholar]
  22. 22.
    Essletzbichler P, Konopka T, Santoro F, Chen D, Gapp BV et al. 2014. Megabase-scale deletion using CRISPR/Cas9 to generate a fully haploid human cell line. Genome Res. 24:2059–65
    [Google Scholar]
  23. 23.
    Falahati H, Pelham-Webb B, Blythe S, Wieschaus E 2016. Nucleation by rRNA dictates the precision of nucleolus assembly. Curr. Biol. 26:277–85
    [Google Scholar]
  24. 24.
    Falahati H, Wieschaus E. 2017. Independent active and thermodynamic processes govern the nucleolus assembly in vivo. PNAS 114:1335–40
    [Google Scholar]
  25. 25.
    Floutsakou I, Agrawal S, Nguyen TT, Seoighe C, Ganley AR, McStay B. 2013. The shared genomic architecture of human nucleolar organizer regions. Genome Res. 23:2003–12
    [Google Scholar]
  26. 26.
    Fudenberg G, Imakaev M, Lu C, Goloborodko A, Abdennur N, Mirny LA. 2016. Formation of chromosomal domains by loop extrusion. Cell Rep. 15:2038–49
    [Google Scholar]
  27. 27.
    Fulka H, Rychtarova J, Loi P. 2020. The nucleolus-like and precursor bodies of mammalian oocytes and embryos and their possible role in post-fertilization centromere remodelling. Biochem. Soc. Trans. 48:581–93
    [Google Scholar]
  28. 28.
    Garagna S, Page J, Fernandez-Donoso R, Zuccotti M, Searle JB. 2014. The Robertsonian phenomenon in the house mouse: mutation, meiosis and speciation. Chromosoma 123:529–44
    [Google Scholar]
  29. 29.
    Gonzalez IL, Sylvester JE. 1995. Complete sequence of the 43-kb human ribosomal DNA repeat: analysis of the intergenic spacer. Genomics 27:320–28
    [Google Scholar]
  30. 30.
    Gonzalez IL, Sylvester JE. 1997. Beyond ribosomal DNA: on towards the telomere. Chromosoma 105:431–37
    [Google Scholar]
  31. 31.
    Goodfellow SJ, Zomerdijk JC. 2013. Basic mechanisms in RNA polymerase I transcription of the ribosomal RNA genes. Subcell. Biochem. 61:211–36
    [Google Scholar]
  32. 32.
    Goodpasture C, Bloom SE. 1975. Visualization of nucleolar organizer regions in mammalian chromosomes using silver staining. Chromosoma 53:37–50
    [Google Scholar]
  33. 33.
    Grob A, Colleran C, McStay B. 2014. Construction of synthetic nucleoli in human cells reveals how a major functional nuclear domain is formed and propagated through cell division. Genes Dev. 28:220–30
    [Google Scholar]
  34. 34.
    Guarracino A, Buonaiuto S, Gomes de Lima L, Potapova T, Rhie A et al. 2023. Recombination between heterologous human acrocentric chromosomes. Nature 617335–43
  35. 35.
    Guo Y, Xu Q, Canzio D, Shou J, Li J et al. 2015. CRISPR inversion of CTCF sites alters genome topology and enhancer/promoter function. Cell 162:900–10
    [Google Scholar]
  36. 36.
    Haltiner MM, Smale ST, Tjian R. 1986. Two distinct promoter elements in the human rRNA gene identified by linker scanning mutagenesis. Mol. Cell. Biol. 6:227–35
    [Google Scholar]
  37. 37.
    Hamerton JL, Canning N, Ray M, Smith S 1975. A cytogenetic survey of 14,069 newborn infants. I. Incidence of chromosome abnormalities. Clin. Genet. 8:223–43
    [Google Scholar]
  38. 38.
    Heitz E. 1931. Die Ursache der gesetzmässigen Zahl, Lage, Form und Grösse pflanzlicher Nukleolen. Planta 12:775–844
    [Google Scholar]
  39. 39.
    Heliot L, Kaplan H, Lucas L, Klein C, Beorchia A et al. 1997. Electron tomography of metaphase nucleolar organizer regions: evidence for a twisted-loop organization. Mol. Biol. Cell 8:2199–216
    [Google Scholar]
  40. 40.
    Henderson AS, Warburton D, Atwood KC. 1972. Location of ribosomal DNA in the human chromosome complement. PNAS 69:3394–98
    [Google Scholar]
  41. 41.
    Henras AK, Plisson-Chastang C, O'Donohue MF, Chakraborty A, Gleizes PE 2015. An overview of pre-ribosomal RNA processing in eukaryotes. Wiley Interdiscip. Rev. RNA 6:225–42
    [Google Scholar]
  42. 42.
    Hernandez-Verdun D. 2011. Assembly and disassembly of the nucleolus during the cell cycle. Nucleus 2:189–94
    [Google Scholar]
  43. 43.
    Holm PB, Rasmussen SW. 1977. Human meiosis I. The human pachytene karyotype analyzed by three dimensional reconstruction of the synaptonemal complex. Carlsberg Res. Commun. 42:283–323
    [Google Scholar]
  44. 44.
    Hori Y, Shimamoto A, Kobayashi T. 2021. The human ribosomal DNA array is composed of highly homogenized tandem clusters. Genome Res. 31:1971–82
    [Google Scholar]
  45. 45.
    Huddleston J, Chaisson MJP, Steinberg KM, Warren W, Hoekzema K et al. 2017. Discovery and genotyping of structural variation from long-read haploid genome sequence data. Genome Res. 27:677–85
    [Google Scholar]
  46. 46.
    Hyman AA, Weber CA, Julicher F. 2014. Liquid-liquid phase separation in biology. Annu. Rev. Cell Dev. Biol. 30:39–58
    [Google Scholar]
  47. 47.
    Jacobs PA, Wilson CM, Sprenkle JA, Rosenshein NB, Migeon BR. 1980. Mechanism of origin of complete hydatidiform moles. Nature 286:714–16
    [Google Scholar]
  48. 48.
    Jones MH, Learned RM, Tjian R. 1988. Analysis of clustered point mutations in the human ribosomal RNA gene promoter by transient expression in vivo. PNAS 85:669–73
    [Google Scholar]
  49. 49.
    Jordan P, Mannervik M, Tora L, Carmo-Fonseca M. 1996. In vivo evidence that TATA-binding protein/SL1 colocalizes with UBF and RNA polymerase I when rRNA synthesis is either active or inactive. J. Cell Biol. 133:225–34
    [Google Scholar]
  50. 50.
    Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J. 2005. Repbase Update, a database of eukaryotic repetitive elements. Cytogenet. Genome Res. 110:462–67
    [Google Scholar]
  51. 51.
    Kim JH, Dilthey AT, Nagaraja R, Lee HS, Koren S et al. 2018. Variation in human chromosome 21 ribosomal RNA genes characterized by TAR cloning and long-read sequencing. Nucleic Acids Res. 46:6712–25
    [Google Scholar]
  52. 52.
    Kim JH, Noskov VN, Ogurtsov AY, Nagaraja R, Petrov N et al. 2021. The genomic structure of a human chromosome 22 nucleolar organizer region determined by TAR cloning. Sci. Rep. 11:2997
    [Google Scholar]
  53. 53.
    Korsholm LM, Gal Z, Nieto B, Quevedo O, Boukoura S et al. 2020. Recent advances in the nucleolar responses to DNA double-strand breaks. Nucleic Acids Res. 48:9449–61
    [Google Scholar]
  54. 54.
    Krystal M, D'Eustachio P, Ruddle FH, Arnheim N 1981. Human nucleolus organizers on nonhomologous chromosomes can share the same ribosomal gene variants. PNAS 78:5744–48
    [Google Scholar]
  55. 55.
    Lafontaine DLJ, Riback JA, Bascetin R, Brangwynne CP. 2020. The nucleolus as a multiphase liquid condensate. Nat. Rev. Mol. Cell Biol. 22:165–82
    [Google Scholar]
  56. 56.
    Larson AG, Elnatan D, Keenen MM, Trnka MJ, Johnston JB et al. 2017. Liquid droplet formation by HP1α suggests a role for phase separation in heterochromatin. Nature 547:236–40
    [Google Scholar]
  57. 57.
    Lee C, Critcher R, Zhang JG, Mills W, Farr CJ. 2000. Distribution of gamma satellite DNA on the human X and Y chromosomes suggests that it is not required for mitotic centromere function. Chromosoma 109:381–89
    [Google Scholar]
  58. 58.
    Levan A, Fredga K, Sandberg AA. 1964. Nomenclature for centromeric position on chromosomes. Heriditas 52:201–20
    [Google Scholar]
  59. 59.
    Liao W-W, Asri M, Ebler J, Doerr D, Haukness M et al. 2023. A draft human pangenome reference. Nature 617312–24
  60. 60.
    Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T et al. 2009. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326:289–93
    [Google Scholar]
  61. 61.
    Lin CC, Sasi R, Lee C, Fan YS, Court D. 1993. Isolation and identification of a novel tandemly repeated DNA sequence in the centromeric region of human chromosome 8. Chromosoma 102:333–39
    [Google Scholar]
  62. 62.
    Lyle R, Prandini P, Osoegawa K, ten Hallers B, Humphray S et al. 2007. Islands of euchromatin-like sequence and expressed polymorphic sequences within the short arm of human chromosome 21. Genome Res. 17:1690–96
    [Google Scholar]
  63. 63.
    Mack H, Swisshelm K 2013. Robertsonian translocations. Brenner's Encyclopedia of Genetics S Maloy, K Hughes 301–5. San Diego, CA: Academic. , 2nd ed..
    [Google Scholar]
  64. 64.
    Mais C, Wright JE, Prieto JL, Raggett SL, McStay B. 2005. UBF-binding site arrays form pseudo-NORs and sequester the RNA polymerase I transcription machinery. Genes Dev. 19:50–64
    [Google Scholar]
  65. 65.
    Mangan H, Gailin MO, McStay B. 2017. Integrating the genomic architecture of human nucleolar organizer regions with the biophysical properties of nucleoli. FEBS J. 284:3977–85
    [Google Scholar]
  66. 66.
    Mangan H, McStay B. 2021. Human nucleoli comprise multiple constrained territories, tethered to individual chromosomes. Genes Dev. 35:483–88
    [Google Scholar]
  67. 67.
    Mc Cartney AM, Shafin K, Alonge M, Bzikadze AV, Formenti G et al. 2022. Chasing perfection: validation and polishing strategies for telomere-to-telomere genome assemblies. Nat. Methods 19:687–95
    [Google Scholar]
  68. 68.
    McClintock B. 1934. The relationship of a particular chromosomal element to the development of the nucleoli in Zea mays. Z. Zellforsch. Mikrosk. Anat. 21:294–328
    [Google Scholar]
  69. 69.
    McStay B. 2016. Nucleolar organizer regions: genomic ‘dark matter’ requiring illumination. Genes Dev. 30:1598–610
    [Google Scholar]
  70. 70.
    McStay B, Grummt I. 2008. The epigenetics of rRNA genes: from molecular to chromosome biology. Annu. Rev. Cell Dev. Biol. 24:131–57
    [Google Scholar]
  71. 71.
    Metzdorf R, Gottert E, Blin N. 1988. A novel centromeric repetitive DNA from human chromosome 22. Chromosoma 97:154–58
    [Google Scholar]
  72. 72.
    Misteli T. 2020. The self-organizing genome: principles of genome architecture and function. Cell 183:28–45
    [Google Scholar]
  73. 73.
    Moss T, Mars JC, Tremblay MG, Sabourin-Felix M. 2019. The chromatin landscape of the ribosomal RNA genes in mouse and human. Chromosome Res. 27:31–40
    [Google Scholar]
  74. 74.
    Nemeth A, Langst G. 2011. Genome organization in and around the nucleolus. Trends Genet. 27:149–56
    [Google Scholar]
  75. 75.
    Nielsen J, Wohlert M. 1991. Chromosome abnormalities found among 34,910 newborn children: results from a 13-year incidence study in Arhus, Denmark. Hum. Genet. 87:81–83
    [Google Scholar]
  76. 76.
    Nora EP, Goloborodko A, Valton AL, Gibcus JH, Uebersohn A et al. 2017. Targeted degradation of CTCF decouples local insulation of chromosome domains from genomic compartmentalization. Cell 169:930–44.e22
    [Google Scholar]
  77. 77.
    Nurk S, Koren S, Rhie A, Rautiainen M, Bzikadze AV et al. 2022. The complete sequence of a human genome. Science 376:44–53
    [Google Scholar]
  78. 78.
    O'Sullivan AC, Sullivan GJ, McStay B. 2002. UBF binding in vivo is not restricted to regulatory sequences within the vertebrate ribosomal DNA repeat. Mol. Cell. Biol. 22:657–68
    [Google Scholar]
  79. 79.
    Page SL, Shaffer LG. 1997. Nonhomologous Robertsonian translocations form predominantly during female meiosis. Nat. Genet. 15:231–32
    [Google Scholar]
  80. 80.
    Patau K, Smith DW, Therman E, Inhorn SL, Wagner HP. 1960. Multiple congenital anomaly caused by an extra autosome. Lancet 275:790–93
    [Google Scholar]
  81. 81.
    Pederson T. 2010. The nucleolus. Cold Spring Harb. Perspect. Biol. 3:a000638
    [Google Scholar]
  82. 82.
    Ponting CP, Haerty W. 2022. Genome-wide analysis of human long noncoding RNAs: a provocative review. Annu. Rev. Genom. Hum. Genet. 23:153–72
    [Google Scholar]
  83. 83.
    Poot M, Hochstenbach R. 2021. Prevalence and phenotypic impact of Robertsonian translocations. Mol. Syndromol. 12:1–11
    [Google Scholar]
  84. 84.
    Potapova TA, Unruh JR, Yu Z, Rancati G, Li H et al. 2019. Superresolution microscopy reveals linkages between ribosomal DNA on heterologous chromosomes. J. Cell Biol. 218:2492–513
    [Google Scholar]
  85. 85.
    Rao SSP, Huang SC, St Hilaire BG, Engreitz JM, Perez EM et al. 2017. Cohesin loss eliminates all loop domains. Cell 171:305–20.e24
    [Google Scholar]
  86. 86.
    Raska I, Shaw PJ, Cmarko D. 2006. Structure and function of the nucleolus in the spotlight. Curr. Opin. Cell Biol. 18:325–34
    [Google Scholar]
  87. 87.
    Robertson WRB. 1916. Chromosome studies. I. Taxonomic relationships shown in the chromosomes of Tettigidae and Acrididae: V-shaped chromosomes and their significance in Acrididae, Locustidae, and Gryllidae: chromosomes and variation. J. Morphol. 27:179–331
    [Google Scholar]
  88. 88.
    Roussel P, Andre C, Masson C, Geraud G, Hernandez VD. 1993. Localization of the RNA polymerase I transcription factor hUBF during the cell cycle. J. Cell Sci. 104:327–37
    [Google Scholar]
  89. 89.
    Sakai K, Ohta T, Minoshima S, Kudoh J, Wang Y et al. 1995. Human ribosomal RNA gene cluster: identification of the proximal end containing a novel tandem repeat sequence. Genomics 26:521–26
    [Google Scholar]
  90. 90.
    Sanborn AL, Rao SS, Huang SC, Durand NC, Huntley MH et al. 2015. Chromatin extrusion explains key features of loop and domain formation in wild-type and engineered genomes. PNAS 112:E6456–65
    [Google Scholar]
  91. 91.
    Sanulli S, Trnka MJ, Dharmarajan V, Tibble RW, Pascal BD et al. 2019. HP1 reshapes nucleosome core to promote phase separation of heterochromatin. Nature 575:390–94
    [Google Scholar]
  92. 92.
    Stahl A, Luciani JM, Hartung M, Devictor M, Berge-Lefranc JL, Guichaoua M. 1983. Structural basis for Robertsonian translocations in man: association of ribosomal genes in the nucleolar fibrillar center in meiotic spermatocytes and oocytes. PNAS 80:5946–50
    [Google Scholar]
  93. 93.
    Strom AR, Emelyanov AV, Mir M, Fyodorov DV, Darzacq X, Karpen GH. 2017. Phase separation drives heterochromatin domain formation. Nature 547:241–45
    [Google Scholar]
  94. 94.
    Stults DM, Killen MW, Pierce HH, Pierce AJ. 2008. Genomic architecture and inheritance of human ribosomal RNA gene clusters. Genome Res. 18:13–18
    [Google Scholar]
  95. 95.
    Stults DM, Killen MW, Williamson EP, Hourigan JS, Vargas HD et al. 2009. Human rRNA gene clusters are recombinational hotspots in cancer. Cancer Res. 69:9096–104
    [Google Scholar]
  96. 96.
    Sullivan BA, Wolff DJ, Schwartz S. 1994. Analysis of centromeric activity in Robertsonian translocations: implications for a functional acrocentric hierarchy. Chromosoma 103:459–67
    [Google Scholar]
  97. 97.
    Sullivan GJ, Bridger JM, Cuthbert AP, Newbold RF, Bickmore WA, McStay B. 2001. Human acrocentric chromosomes with transcriptionally silent nucleolar organizer regions associate with nucleoli. EMBO J. 20:2867–74
    [Google Scholar]
  98. 98.
    Tartakoff A, DiMario P, Hurt E, McStay B, Panse VG, Tollervey D. 2022. The dual nature of the nucleolus. Genes Dev. 36:765–69
    [Google Scholar]
  99. 99.
    Therman E, Susman B, Denniston C. 1989. The nonrandom participation of human acrocentric chromosomes in Robertsonian translocations. Ann. Hum. Genet. 53:49–65
    [Google Scholar]
  100. 100.
    van Sluis M, Gailin MO, McCarter JGW, Mangan H, Grob A, McStay B. 2019. Human NORs, comprising rDNA arrays and functionally conserved distal elements, are located within dynamic chromosomal regions. Genes Dev. 33:1688–701
    [Google Scholar]
  101. 101.
    van Sluis M, McStay B. 2015. A localized nucleolar DNA damage response facilitates recruitment of the homology-directed repair machinery independent of cell cycle stage. Genes Dev. 29:1151–63
    [Google Scholar]
  102. 102.
    van Sluis M, McStay B. 2019. Nucleolar DNA double-strand break responses underpinning rDNA genomic stability. Trends Genet. 35:743–53
    [Google Scholar]
  103. 103.
    van Sluis M, van Vuuren C, Mangan H, McStay B. 2020. NORs on human acrocentric chromosome p-arms are active by default and can associate with nucleoli independently of rDNA. PNAS 117:10368–77
    [Google Scholar]
  104. 104.
    van Sluis M, van Vuuren C, McStay B. 2016. The relationship between human nucleolar organizer regions and nucleoli, probed by 3D-immunoFISH. Methods Mol. Biol. 1455:3–14
    [Google Scholar]
  105. 105.
    Wang T, Antonacci-Fulton L, Howe K, Lawson HA, Lucas JK et al. 2022. The Human Pangenome Project: a global resource to map genomic diversity. Nature 604:437–46
    [Google Scholar]
  106. 106.
    Warburton PE, Hasson D, Guillem F, Lescale C, Jin X, Abrusan G. 2008. Analysis of the largest tandemly repeated DNA families in the human genome. BMC Genom. 9:533
    [Google Scholar]
  107. 107.
    Waye JS, Willard HF. 1989. Concerted evolution of alpha satellite DNA: evidence for species specificity and a general lack of sequence conservation among alphoid sequences of higher primates. Chromosoma 98:273–79
    [Google Scholar]
  108. 108.
    Yao RW, Xu G, Wang Y, Shan L, Luan PF et al. 2019. Nascent pre-rRNA sorting via phase separation drives the assembly of dense fibrillar components in the human nucleolus. Mol. Cell 76:767–83.e11
    [Google Scholar]
  109. 109.
    Zhang LF, Huynh KD, Lee JT. 2007. Perinucleolar targeting of the inactive X during S phase: evidence for a role in the maintenance of silencing. Cell 129:693–706
    [Google Scholar]
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