Spatial genome organization and its emerging role as a potential diagnosis tool

Frontiers in Genetics

Volumn 7, Issue JUL, 2016, Pages

  Meaburn, Karen J ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Cancer; Diagnosis; Disease; Gene positioning; Genome organization; Nuclear architecture; Spatial positioning

Indexed keywords

TRASTUZUMAB; TUMOR MARKER;

BREAST CANCER; CANCER DIAGNOSIS; CANCER GROWTH; CANCER MORTALITY; CANCER PROGNOSIS; CELL CYCLE REGULATION; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOME POSITIONING; CHRONIC MYELOID LEUKEMIA; CYTOGENETICS; FLUORESCENCE IN SITU HYBRIDIZATION; FUNCTIONAL GENOMICS; GENE EXPRESSION PROFILING; GENE LOCUS; HISTOLOGY; HUMAN; NONHUMAN; PROSTATE CANCER; REVIEW; SPATIAL ANALYSIS; TRANSCRIPTION REGULATION;

EID: 84983320530     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2016.00134     Document Type: Review

References (206)

1. Ahmad, A. S., Ormiston-Smith, N., and Sasieni, P. D. (2015). Trends in the lifetime risk of developing cancer in Great Britain: comparison of risk for those born from 1930 to 1960. Br. J. Cancer 112, 943-947. doi: 10.1038/bjc.2014.606
2. Ahmed, S., Brickner, D. G., Light, W. H., Cajigas, I., McDonough, M., Froyshteter, A. B., et al. (2010). DNA zip codes control an ancient mechanism for gene targeting to the nuclear periphery. Nat. Cell Biol. 12, 111-118. doi: 10.1038/ncb2011
3. Arican-Goktas, H. D., Ittiprasert, W., Bridger, J. M., and Knight, M. (2014). Differential spatial repositioning of activated genes in Biomphalaria glabrata snails infected with Schistosoma mansoni. PLoS Negl. Trop. Dis. 8:e3013. doi: 10.1371/journal.pntd.0003013
4. Belt, E. J., Fijneman, R. J., van den Berg, E. G., Bril, H., Delis-van Diemen, P. M., Tijssen, M., et al. (2011). Loss of lamin A/C expression in stage II and III colon cancer is associated with disease recurrence. Eur. J. Cancer 47, 1837-1845. doi: 10.1016/j.ejca.2011.04.025
5. Berger, A. B., Cabal, G. G., Fabre, E., Duong, T., Buc, H., Nehrbass, U., et al. (2008). High-resolution statistical mapping reveals gene territories in live yeast. Nat. Methods 5, 1031-1037. doi: 10.1038/nmeth.1266
6. Bian, Q., Khanna, N., Alvikas, J., and Belmont, A. S. (2013). Beta-Globin cis-elements determine differential nuclear targeting through epigenetic modifications. J. Cell Biol. 203, 767-783. doi: 10.1083/jcb.201305027
7. Bickmore, W. A., and van Steensel, B. (2013). Genome architecture: domain organization of interphase chromosomes. Cell 152, 1270-1284. doi: 10.1016/j.cell.2013.02.001
8. Bleyer, A., and Welch, H. G. (2012). Effect of three decades of screening mammography on breast-cancer incidence. N. Engl. J. Med. 367, 1998-2005. doi: 10.1056/NEJMoa1206809
9. Bolzer, A., Kreth, G., Solovei, I., Koehler, D., Saracoglu, K., Fauth, C., et al. (2005). Three-dimensional maps of all chromosomes in human male fibroblast nuclei and prometaphase rosettes. PLoS Biol. 3:e157. doi: 10.1371/journal.pbio.0030157
10. Borden, J., and Manuelidis, L. (1988). Movement of the X chromosome in epilepsy. Science 242, 1687-1691. doi: 10.1126/science.3201257
11. Boutanaev, A. M., Mikhaylova, L. M., and Nurminsky, D. I. (2005). The pattern of chromosome folding in interphase is outlined by the linear gene density profile. Mol. Cell. Biol. 25, 8379-8386. doi: 10.1128/MCB.25.18.8379-8386.2005
12. Boyle, S., Gilchrist, S., Bridger, J. M., Mahy, N. L., Ellis, J. A., and Bickmore, W. A. (2001). The spatial organization of human chromosomes within the nuclei of normal and emerin-mutant cells. Hum. Mol. Genet. 10, 211-219. doi: 10.1093/hmg/10.3.211
13. Boyle, S., Rodesch, M. J., Halvensleben, H. A., Jeddeloh, J. A., and Bickmore, W. A. (2011). Fluorescence in situ hybridization with high-complexity repeat-free oligonucleotide probes generated by massively parallel synthesis. Chromosome Res. 19, 901-909. doi: 10.1007/s10577-011-9245-0
14. Brickner, D. G., Cajigas, I., Fondufe-Mittendorf, Y., Ahmed, S., Lee, P. C., Widom, J., et al. (2007). H2A.Z-mediated localization of genes at the nuclear periphery confers epigenetic memory of previous transcriptional state. PLoS Biol 5:e81. doi: 10.1371/journal.pbio.0050081
15. Brickner, J. H., and Walter, P. (2004). Gene recruitment of the activated INO1 locus to the nuclear membrane. PLoS Biol. 2:e342. doi: 10.1371/journal.pbio.0020342
16. Bridger, J. M., Arican-Gotkas, H. D., Foster, H. A., Godwin, L. S., Harvey, A., Kill, I. R., et al. (2014). The non-random repositioning of whole chromosomes and individual gene loci in interphase nuclei and its relevance in disease, infection, aging, and cancer. Adv. Exp. Med. Biol. 773, 263-279. doi: 10.1007/978-1-4899-8032-8_12
17. Bridger, J. M., Boyle, S., Kill, I. R., and Bickmore, W. A. (2000). Re-modelling of nuclear architecture in quiescent and senescent human fibroblasts. Curr. Biol. 10, 149-152. doi: 10.1016/S0960-9822(00)00312-2
18. Broers, J. L., and Ramaekers, F. C. (2014). The role of the nuclear lamina in cancer and apoptosis. Adv. Exp. Med. Biol. 773, 27-48. doi: 10.1007/978-1-4899-8032-8_2
19. Broers, J. L., Raymond, Y., Rot, M. K., Kuijpers, H., Wagenaar, S. S., and Ramaekers, F. C. (1993). Nuclear A-type lamins are differentially expressed in human lung cancer subtypes. Am. J. Pathol. 143, 211-220.
20. Brown, J. M., Leach, J., Reittie, J. E., Atzberger, A., Lee-Prudhoe, J., Wood, W. G., et al. (2006). Coregulated human globin genes are frequently in spatial proximity when active. J. Cell Biol. 172, 177-187. doi: 10.1083/jcb.200507073
21. Brown, K. E., Baxter, J., Graf, D., Merkenschlager, M., and Fisher, A. G. (1999). Dynamic repositioning of genes in the nucleus of lymphocytes preparing for cell division. Mol. Cell 3, 207-217. doi: 10.1016/S1097-2765(00)80311-1
22. Brown, K. E., Guest, S. S., Smale, S. T., Hahm, K., Merkenschlager, M., and Fisher, A. G. (1997). Association of transcriptionally silent genes with Ikaros complexes at centromeric heterochromatin. Cell 91, 845-854. doi: 10.1016/S0092-8674(00)80472-9
23. Bustin, M., and Misteli, T. (2016). Nongenetic functions of the genome. Science 352:aad6933. doi: 10.1126/science.aad6933
24. Capo-Chichi, C. D., Aguida, B., Chabi, N. W., Cai, Q. K., Offrin, G., Agossou, V. K., et al. (2016). Lamin A/C deficiency is an independent risk factor for cervical cancer. Cell. Oncol. 39, 59-68. doi: 10.1007/s13402-015-0252-6
25. Chambeyron, S., and Bickmore, W. A. (2004). Chromatin decondensation and nuclear reorganization of the HoxB locus upon induction of transcription. Genes Dev. 18, 1119-1130. doi: 10.1101/gad.292104
26. Chandra, T., Ewels, P. A., Schoenfelder, S., Furlan-Magaril, M., Wingett, S. W., Kirschner, K., et al. (2015). Global reorganization of the nuclear landscape in senescent cells. Cell Rep. 10, 471-483. doi: 10.1016/j.celrep.2014.12.055
27. Chang, A. J., Autio, K. A., Roach, M. III, and Scher, H. I. (2014). High-risk prostate cancer-classification and therapy. Nat. Rev. Clin. Oncol. 11, 308-323. doi: 10.1038/nrclinonc.2014.68
28. Chiarle, R., Zhang, Y., Frock, R. L., Lewis, S. M., Molinie, B., Ho, Y. J., et al. (2011). Genome-wide translocation sequencing reveals mechanisms of chromosome breaks and rearrangements in B cells. Cell 147, 107-119. doi: 10.1016/j.cell.2011.07.049
29. Chuang, C. H., Carpenter, A. E., Fuchsova, B., Johnson, T., de Lanerolle, P., and Belmont, A. S. (2006). Long-range directional movement of an interphase chromosome site. Curr. Biol. 16, 825-831. doi: 10.1016/j.cub.2006.03.059
30. Chuang, T. C., Moshir, S., Garini, Y., Chuang, A. Y., Young, I. T., Vermolen, B., et al. (2004). The three-dimensional organization of telomeres in the nucleus of mammalian cells. BMC Biol. 2:12. doi: 10.1186/1741-7007-2-12
31. Clemson, C. M., Hall, L. L., Byron, M., McNeil, J., and Lawrence, J. B. (2006). The X chromosome is organized into a gene-rich outer rim and an internal core containing silenced nongenic sequences. Proc. Natl. Acad. Sci. U.S.A. 103, 7688-7693. doi: 10.1073/pnas.0601069103
32. Clowney, E. J., LeGros, M. A., Mosley, C. P., Clowney, F. G., Markenskoff-Papadimitriou, E. C., Myllys, M., et al. (2012). Nuclear aggregation of olfactory receptor genes governs their monogenic expression. Cell 151, 724-737. doi: 10.1016/j.cell.2012.09.043
33. Cooperberg, M. R., Broering, J. M., and Carroll, P. R. (2009). Risk assessment for prostate cancer metastasis and mortality at the time of diagnosis. J. Natl. Cancer Inst. 101, 878-887. doi: 10.1093/jnci/djp122
34. Cooperberg, M. R., Broering, J. M., and Carroll, P. R. (2010). Time trends and local variation in primary treatment of localized prostate cancer. J. Clin. Oncol. 28, 1117-1123. doi: 10.1200/JCO.2009.26.0133
35. Cournac, A., Koszul, R., and Mozziconacci, J. (2016). The 3D folding of metazoan genomes correlates with the association of similar repetitive elements. Nucleic Acids Res. 44, 245-255. doi: 10.1093/nar/gkv1292
36. Cremer, M., Kupper, K., Wagler, B., Wizelman, L., von Hase, J., Weiland, Y., et al. (2003). Inheritance of gene density-related higher order chromatin arrangements in normal and tumor cell nuclei. J. Cell Biol. 162, 809-820. doi: 10.1083/jcb.200304096
37. Cremer, T., and Cremer, C. (2001). Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat. Rev. Genet. 2, 292-301. doi: 10.1038/35066075
38. Croft, J. A., Bridger, J. M., Boyle, S., Perry, P., Teague, P., and Bickmore, W. A. (1999). Differences in the localization and morphology of chromosomes in the human nucleus. J. Cell Biol. 145, 1119-1131. doi: 10.1083/jcb.145.6.1119
39. Dai, X., Li, T., Bai, Z., Yang, Y., Liu, X., Zhan, J., et al. (2015). Breast cancer intrinsic subtype classification, clinical use and future trends. Am. J. Cancer Res. 5, 2929-2943.
40. D'Amico, A. V., Whittington, R., Malkowicz, S. B., Schultz, D., Blank, K., Broderick, G. A., et al. (1998). Biochemical outcome after radical prostatectomy, external beam radiation therapy, or interstitial radiation therapy for clinically localized prostate cancer. JAMA 280, 969-974. doi: 10.1001/jama.280.11.969
41. Davidson, P. M., Denais, C., Bakshi, M. C., and Lammerding, J. (2014). Nuclear deformability constitutes a rate-limiting step during cell migration in 3-D environments. Cell. Mol. Bioeng. 7, 293-306. doi: 10.1007/s12195-014-0342-y
42. de Azambuja, E., Cardoso, F., de Castro, G. Jr., Colozza, M., Mano, M. S., Durbecq, V., et al. (2007). Ki-67 as prognostic marker in early breast cancer: a meta-analysis of published studies involving 12,155 patients. Br. J. Cancer 96, 1504-1513. doi: 10.1038/sj.bjc.6603756
43. Dekker, J., and Misteli, T. (2015). Long-Range Genome Interactions. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
44. Demmerle, J., Koch, A. J., and Holaska, J. M. (2013). Emerin and histone deacetylase 3 (HDAC3) cooperatively regulate expression and nuclear positions of MyoD, Myf5, and Pax7 genes during myogenesis. Chromosome Res. 21, 765-779. doi: 10.1007/s10577-013-9381-9
45. Dittmer, T. A., and Misteli, T. (2011). The lamin protein family. Genome Biol. 12, 222. doi: 10.1186/gb-2011-12-5-222
46. Dixon, J. R., Selvaraj, S., Yue, F., Kim, A., Li, Y., Shen, Y., et al. (2012). Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485, 376-380. doi: 10.1038/nature11082
47. Draisma, G., Etzioni, R., Tsodikov, A., Mariotto, A., Wever, E., Gulati, R., et al. (2009). Lead time and overdiagnosis in prostate-specific antigen screening: importance of methods and context. J. Natl. Cancer Inst. 101, 374-383. doi: 10.1093/jnci/djp001
48. Dultz, E., Tjong, H., Weider, E., Herzog, M., Young, B., Brune, C., et al. (2016). Global reorganization of budding yeast chromosome conformation in different physiological conditions. J. Cell Biol. 212, 321-334. doi: 10.1083/jcb.201507069
49. Dundr, M., Ospina, J. K., Sung, M. H., John, S., Upender, M., Ried, T., et al. (2007). Actin-dependent intranuclear repositioning of an active gene locus in vivo. J. Cell Biol. 179, 1095-1103. doi: 10.1083/jcb.200710058
50. Dupont, C., Guimiot, F., Perrin, L., Marey, I., Smiljkovski, D., Le Tessier, D., et al. (2012). 3D position of pericentromeric heterochromatin within the nucleus of a patient with ICF syndrome. Clin. Genet. 82, 187-192. doi: 10.1111/j.1399-0004.2011.01697.x
51. Egeblad, M., and Werb, Z. (2002). New functions for the matrix metalloproteinases in cancer progression. Nat. Rev. Cancer 2, 161-174. doi: 10.1038/nrc745
52. Egecioglu, D., and Brickner, J. H. (2011). Gene positioning and expression. Curr. Opin. Cell Biol. 23, 338-345. doi: 10.1016/j.ceb.2011.01.001
53. Epstein, J. I., Egevad, L., Amin, M. B., Delahunt, B., Srigley, J. R., Humphrey, P. A., et al. (2016). The 2014 international society of urological pathology (isup) consensus conference on gleason grading of prostatic carcinoma: definition of grading patterns and proposal for a new grading system. Am. J. Surg. Pathol. 40, 244-252. doi: 10.1097/PAS.0000000000000530
54. Ferrai, C., de Castro, I. J., Lavitas, L., Chotalia, M., and Pombo, A. (2010). Gene positioning. Cold Spring Harb. Perspect. Biol. 2, a000588. doi: 10.1101/cshperspect.a000588
55. Ferte, C., Andre, F., and Soria, J. C. (2010). Molecular circuits of solid tumors: prognostic and predictive tools for bedside use. Nat. Rev. Clin. Oncol. 7, 367-380. doi: 10.1038/nrclinonc.2010.84
56. Finlan, L. E., Sproul, D., Thomson, I., Boyle, S., Kerr, E., Perry, P., et al. (2008). Recruitment to the nuclear periphery can alter expression of genes in human cells. PLoS Genet 4:e1000039. doi: 10.1371/journal.pgen.1000039
57. Foster, H. A., Griffin, D. K., and Bridger, J. M. (2012). Interphase chromosome positioning in in vitro porcine cells and ex vivo porcine tissues. BMC Cell Biol. 13:30. doi: 10.1186/1471-2121-13-30
58. Francastel, C., Walters, M. C., Groudine, M., and Martin, D. I. (1999). A functional enhancer suppresses silencing of a transgene and prevents its localization close to centrometric heterochromatin. Cell 99, 259-269. doi: 10.1016/S0092-8674(00)81657-8
59. Fraser, P., and Bickmore, W. (2007). Nuclear organization of the genome and the potential for gene regulation. Nature 447, 413-417. doi: 10.1038/nature05916
60. Gadji, M., Fortin, D., Tsanaclis, A. M., Garini, Y., Katzir, N., Wienburg, Y., et al. (2010). Three-dimensional nuclear telomere architecture is associated with differential time to progression and overall survival in glioblastoma patients. Neoplasia 12, 183-191. doi: 10.1593/neo.91752
61. Goetze, S., Mateos-Langerak, J., and van Driel, R. (2007). Three-dimensional genome organization in interphase and its relation to genome function. Semin. Cell Dev. Biol. 18, 707-714. doi: 10.1016/j.semcdb.2007.08.007
62. Grand, R. S., Pichugina, T., Gehlen, L. R., Jones, M. B., Tsai, P., Allison, J. R., et al. (2014). Chromosome conformation maps in fission yeast reveal cell cycle dependent sub nuclear structure. Nucleic Acids Res. 42, 12585-12599. doi: 10.1093/nar/gku965
63. Guelen, L., Pagie, L., Brasset, E., Meuleman, W., Faza, M. B., Talhout, W., et al. (2008). Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 453, 948-951. doi: 10.1038/nature06947
64. Hacisuleyman, E., Goff, L. A., Trapnell, C., Williams, A., Henao-Mejia, J., Sun, L., et al. (2014). Topological organization of multichromosomal regions by the long intergenic noncoding RNA Firre. Nat. Struct. Mol. Biol. 21, 198-206. doi: 10.1038/nsmb.2764
65. Hakim, O., Resch, W., Yamane, A., Klein, I., Kieffer-Kwon, K. R., Jankovic, M., et al. (2012). DNA damage defines sites of recurrent chromosomal translocations in B lymphocytes. Nature 484, 69-74. doi: 10.1038/nature10909
66. Hakim, O., Sung, M. H., Nakayamada, S., Voss, T. C., Baek, S., and Hager, G. L. (2013). Spatial congregation of STAT binding directs selective nuclear architecture during T-cell functional differentiation. Genome Res. 23, 462-472. doi: 10.1101/gr.147652.112
67. Hakim, O., Sung, M. H., Voss, T. C., Splinter, E., John, S., Sabo, P. J., et al. (2011). Diverse gene reprogramming events occur in the same spatial clusters of distal regulatory elements. Genome Res. 21, 697-706. doi: 10.1101/gr.111153.110
68. Hanahan, D., and Weinberg, R. A. (2011). Hallmarks of cancer: the next generation. Cell 144, 646-674. doi: 10.1016/j.cell.2011.02.013
69. Harewood, L., Schutz, F., Boyle, S., Perry, P., Delorenzi, M., Bickmore, W. A., et al. (2010). The effect of translocation-induced nuclear reorganization on gene expression. Genome Res. 20, 554-564. doi: 10.1101/gr.103622.109
70. Harr, J. C., Gonzalez-Sandoval, A., and Gasser, S. M. (2016). Histones and histone modifications in perinuclear chromatin anchoring: from yeast to man. EMBO Rep 17, 139-155. doi: 10.15252/embr.201541809
71. Harr, J. C., Luperchio, T. R., Wong, X., Cohen, E., Wheelan, S. J., and Reddy, K. L. (2015). Directed targeting of chromatin to the nuclear lamina is mediated by chromatin state and A-type lamins. J. Cell Biol. 208, 33-52. doi: 10.1083/jcb.201405110
72. Hastings, R. (2010). Quality control in FISH as part of a laboratory's quality management system. Methods Mol. Biol. 659, 249-259. doi: 10.1007/978-1-60761-789-1_18
73. Hehlmann, R., Hochhaus, A., Baccarani, M., and European, L. (2007). Chronic myeloid leukaemia. Lancet 370, 342-350. doi: 10.1016/S0140-6736(07)61165-9
74. Hiratani, I., Ryba, T., Itoh, M., Yokochi, T., Schwaiger, M., Chang, C. W., et al. (2008). Global reorganization of replication domains during embryonic stem cell differentiation. PLoS Biol. 6:e245. doi: 10.1371/journal.pbio.0060245
75. Hnisz, D., Weintraub, A. S., Day, D. S., Valton, A. L., Bak, R. O., Li, C. H., et al. (2016). Activation of proto-oncogenes by disruption of chromosome neighborhoods. Science 351, 1454-1458. doi: 10.1126/science.aad9024
76. Hogan, M. S., Parfitt, D. E., Zepeda-Mendoza, C. J., Shen, M. M., and Spector, D. L. (2015). Transient pairing of homologous Oct4 alleles accompanies the onset of embryonic stem cell differentiation. Cell Stem Cell 16, 275-288. doi: 10.1016/j.stem.2015.02.001
77. Hveem, T. S., Kleppe, A., Vlatkovic, L., Ersvaer, E., Waehre, H., Nielsen, B., et al. (2016). Chromatin changes predict recurrence after radical prostatectomy. Br. J. Cancer 114, 1243-1250. doi: 10.1038/bjc.2016.96
78. Ioannou, D., Kandukuri, L., Quadri, A., Becerra, V., Simpson, J. L., and Tempest, H. G. (2015). Spatial positioning of all 24 chromosomes in the lymphocytes of six subjects: evidence of reproducible positioning and spatial repositioning following DNA damage with hydrogen peroxide and ultraviolet B. PLoS ONE 10:e0118886. doi: 10.1371/journal.pone.0118886
79. Jefferson, A., Colella, S., Moralli, D., Wilson, N., Yusuf, M., Gimelli, G., et al. (2010). Altered intra-nuclear organisation of heterochromatin and genes in ICF syndrome. PLoS ONE 5:e11364. doi: 10.1371/journal.pone.0011364
80. Jonat, W., and Arnold, N. (2011). Is the Ki-67 labelling index ready for clinical use? Ann. Oncol. 22, 500-502. doi: 10.1093/annonc/mdq732
81. Khanna, N., Hu, Y., and Belmont, A. S. (2014). HSP70 transgene directed motion to nuclear speckles facilitates heat shock activation. Curr. Biol. 24, 1138-1144. doi: 10.1016/j.cub.2014.03.053
82. Kind, J., Pagie, L., de Vries, S. S., Nahidiazar, L., Dey, S. S., Bienko, M., et al. (2015). Genome-wide maps of nuclear lamina interactions in single human cells. Cell 163, 134-147. doi: 10.1016/j.cell.2015.08.040
83. Kind, J., Pagie, L., Ortabozkoyun, H., Boyle, S., de Vries, S. S., Janssen, H., et al. (2013). Single-cell dynamics of genome-nuclear lamina interactions. Cell 153, 178-192. doi: 10.1016/j.cell.2013.02.028
84. Klein, I. A., Resch, W., Jankovic, M., Oliveira, T., Yamane, A., Nakahashi, H., et al. (2011). Translocation-capture sequencing reveals the extent and nature of chromosomal rearrangements in B lymphocytes. Cell 147, 95-106. doi: 10.1016/j.cell.2011.07.048
85. Knight, M., Ittiprasert, W., Odoemelam, E. C., Adema, C. M., Miller, A., Raghavan, N., et al. (2011). Non-random organization of the Biomphalaria glabrata genome in interphase Bge cells and the spatial repositioning of activated genes in cells co-cultured with Schistosoma mansoni. Int. J. Parasitol. 41, 61-70. doi: 10.1016/j.ijpara.2010.07.015
86. Kong, L., Schafer, G., Bu, H., Zhang, Y., Zhang, Y., and Klocker, H. (2012). Lamin A/C protein is overexpressed in tissue-invading prostate cancer and promotes prostate cancer cell growth, migration and invasion through the PI3K/AKT/PTEN pathway. Carcinogenesis 33, 751-759. doi: 10.1093/carcin/bgs022
87. Kosak, S. T., Skok, J. A., Medina, K. L., Riblet, R., Le Beau, M. M., Fisher, A. G., et al. (2002). Subnuclear compartmentalization of immunoglobulin loci during lymphocyte development. Science 296, 158-162. doi: 10.1126/science.1068768
88. Kozubek, S., Lukasova, E., Jirsova, P., Koutna, I., Kozubek, M., Ganova, A., et al. (2002). 3D Structure of the human genome: order in randomness. Chromosoma 111, 321-331. doi: 10.1007/s00412-002-0210-8
89. Kruhlak, M. J., Celeste, A., Dellaire, G., Fernandez-Capetillo, O., Muller, W. G., McNally, J. G., et al. (2006). Changes in chromatin structure and mobility in living cells at sites of DNA double-strand breaks. J. Cell Biol. 172, 823-834. doi: 10.1083/jcb.200510015
90. Kubben, N., Adriaens, M., Meuleman, W., Voncken, J. W., van Steensel, B., and Misteli, T. (2012). Mapping of lamin A-and progerin-interacting genome regions. Chromosoma 121, 447-464. doi: 10.1007/s00412-012-0376-7
91. Kumaran, R. I., and Spector, D. L. (2008). A genetic locus targeted to the nuclear periphery in living cells maintains its transcriptional competence. J. Cell Biol. 180, 51-65. doi: 10.1083/jcb.200706060
92. Lambros, M. B., Natrajan, R., and Reis-Filho, J. S. (2007). Chromogenic and fluorescent in situ hybridization in breast cancer. Hum. Pathol. 38, 1105-1122. doi: 10.1016/j.humpath.2007.04.011
93. Lelek, M., Casartelli, N., Pellin, D., Rizzi, E., Souque, P., Severgnini, M., et al. (2015). Chromatin organization at the nuclear pore favours HIV replication. Nat. Commun. 6, 6483. doi: 10.1038/ncomms7483
94. Leshner, M., Devine, M., Roloff, G. W., True, L. D., Misteli, T., and Meaburn, K. J. (2016). Locus-specific gene repositioning in prostate cancer. Mol. Biol. Cell 27, 236-246. doi: 10.1091/mbc.E15-05-0280
95. Li, C., Shi, Z., Zhang, L., Huang, Y., Liu, A., Jin, Y., et al. (2010). Dynamic changes of territories 17 and 18 during EBV-infection of human lymphocytes. Mol. Biol. Rep. 37, 2347-2354. doi: 10.1007/s11033-009-9740-y
96. Liang, Y., and Hetzer, M. W. (2011). Functional interactions between nucleoporins and chromatin. Curr. Opin. Cell Biol. 23, 65-70. doi: 10.1016/j.ceb.2010.09.008
97. Lieberman-Aiden, E., van Berkum, N. L., Williams, L., Imakaev, M., Ragoczy, T., Telling, A., et al. (2009). Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326, 289-293. doi: 10.1126/science.1181369
98. Lin, C., Yang, L., Tanasa, B., Hutt, K., Ju, B. G., Ohgi, K., et al. (2009). Nuclear receptor-induced chromosomal proximity and DNA breaks underlie specific translocations in cancer. Cell 139, 1069-1083. doi: 10.1016/j.cell.2009.11.030
99. Lukasova, E., Kozubek, S., Kozubek, M., Kjeronska, J., Ryznar, L., Horakova, J., et al. (1997). Localisation and distance between ABL and BCR genes in interphase nuclei of bone marrow cells of control donors and patients with chronic myeloid leukaemia. Hum. Genet. 100, 525-535. doi: 10.1007/s004390050547
100. Lupianez, D. G., Kraft, K., Heinrich, V., Krawitz, P., Brancati, F., Klopocki, E., et al. (2015). Disruptions of topological chromatin domains cause pathogenic rewiring of gene-enhancer interactions. Cell 161, 1012-1025. doi: 10.1016/j.cell.2015.04.004
101. MacDonald, W. A., Sachani, S. S., White, C. R., and Mann, M. R. (2016). A role for chromatin topology in imprinted domain regulation. Biochem. Cell Biol. 94, 43-55. doi: 10.1139/bcb-2015-0032
102. Malhas, A., Lee, C. F., Sanders, R., Saunders, N. J., and Vaux, D. J. (2007). Defects in lamin B1 expression or processing affect interphase chromosome position and gene expression. J. Cell Biol. 176, 593-603. doi: 10.1083/jcb.200607054
103. Mani, R. S., Tomlins, S. A., Callahan, K., Ghosh, A., Nyati, M. K., Varambally, S., et al. (2009). Induced chromosomal proximity and gene fusions in prostate cancer. Science 326, 1230. doi: 10.1126/science.1178124
104. Marini, B., Kertesz-Farkas, A., Ali, H., Lucic, B., Lisek, K., Manganaro, L., et al. (2015). Nuclear architecture dictates HIV-1 integration site selection. Nature 521, 227-231. doi: 10.1038/nature14226
105. Matarazzo, M. R., Boyle, S., D'Esposito, M., and Bickmore, W. A. (2007). Chromosome territory reorganization in a human disease with altered DNA methylation. Proc. Natl. Acad. Sci. U.S.A. 104, 16546-16551. doi: 10.1073/pnas.0702924104
106. Mathas, S., Kreher, S., Meaburn, K. J., Johrens, K., Lamprecht, B., Assaf, C., et al. (2009). Gene deregulation and spatial genome reorganization near breakpoints prior to formation of translocations in anaplastic large cell lymphoma. Proc. Natl. Acad. Sci. U.S.A. 106, 5831-5836. doi: 10.1073/pnas.0900912106
107. Mathur, S., Glogowska, A., McAvoy, E., Righolt, C., Rutherford, J., Willing, C., et al. (2014). Three-dimensional quantitative imaging of telomeres in buccal cells identifies mild, moderate, and severe Alzheimer's disease patients. J. Alzheimers. Dis. 39, 35-48. doi: 10.3233/JAD-130866
108. Mattout, A., Pike, B. L., Towbin, B. D., Bank, E. M., Gonzalez-Sandoval, A., Stadler, M. B., et al. (2011). An EDMD mutation in C. elegans lamin blocks muscle-specific gene relocation and compromises muscle integrity. Curr. Biol. 21, 1603-1614. doi: 10.1016/j.cub.2011.08.030
109. McCord, R. P., Nazario-Toole, A., Zhang, H., Chines, P. S., Zhan, Y., Erdos, M. R., et al. (2013). Correlated alterations in genome organization, histone methylation, and DNA-lamin A/C interactions in Hutchinson-Gilford progeria syndrome. Genome Res. 23, 260-269. doi: 10.1101/gr.138032.112
110. McGregor, M., Hanley, J. A., Boivin, J. F., and McLean, R. G. (1998). Screening for prostate cancer: estimating the magnitude of overdetection. CMAJ 159, 1368-1372.
111. Meaburn, K., Burman, B., and Misteli, T. (2016). "Spatial genome organization and disease," in The Functional Nucleus, eds G. Dellaire and D. Bazett-Jones (New York, NY: Springer).
112. Meaburn, K. J., Agunloye, O., Devine, M., Leshner, M., Roloff, G. W., True, L. D., et al. (2016). Tissue-of-origin-specific gene repositioning in breast and prostate cancer. Histochem. Cell Biol. 145, 433-446. doi: 10.1007/s00418-015-1401-8
113. Meaburn, K. J., Cabuy, E., Bonne, G., Levy, N., Morris, G. E., Novelli, G., et al. (2007). Primary laminopathy fibroblasts display altered genome organization and apoptosis. Aging Cell 6, 139-153. doi: 10.1111/j.1474-9726.2007.00270.x
114. Meaburn, K. J., Gudla, P. R., Khan, S., Lockett, S. J., and Misteli, T. (2009). Disease-specific gene repositioning in breast cancer. J. Cell Biol. 187, 801-812. doi: 10.1083/jcb.200909127
115. Meaburn, K. J., Levy, N., Toniolo, D., and Bridger, J. M. (2005). Chromosome positioning is largely unaffected in lymphoblastoid cell lines containing emerin or A-type lamin mutations. Biochem. Soc. Trans. 33, 1438-1440. doi: 10.1042/BST20051438
116. Meaburn, K. J., and Misteli, T. (2008). Locus-specific and activity-independent gene repositioning during early tumorigenesis. J. Cell Biol. 180, 39-50. doi: 10.1083/jcb.200708204
117. Meaburn, K. J., Newbold, R. F., and Bridger, J. M. (2008). Positioning of human chromosomes in murine cell hybrids according to synteny. Chromosoma 117, 579-591. doi: 10.1007/s00412-008-0175-3
118. Mehta, I. S., Amira, M., Harvey, A. J., and Bridger, J. M. (2010). Rapid chromosome territory relocation by nuclear motor activity in response to serum removal in primary human fibroblasts. Genome Biol. 11, R5. doi: 10.1186/gb-2010-11-1-r5
119. Mehta, I. S., Eskiw, C. H., Arican, H. D., Kill, I. R., and Bridger, J. M. (2011). Farnesyltransferase inhibitor treatment restores chromosome territory positions and active chromosome dynamics in Hutchinson-Gilford progeria syndrome cells. Genome Biol. 12, R74. doi: 10.1186/gb-2011-12-8-r74
120. Mehta, I. S., Kulashreshtha, M., Chakraborty, S., Kolthur-Seetharam, U., and Rao, B. J. (2013). Chromosome territories reposition during DNA damage-repair response. Genome Biol. 14, R135. doi: 10.1186/gb-2013-14-12-r135
121. Mewborn, S. K., Puckelwartz, M. J., Abuisneineh, F., Fahrenbach, J. P., Zhang, Y., MacLeod, H., et al. (2010). Altered chromosomal positioning, compaction, and gene expression with a lamin A/C gene mutation. PLoS ONE 5:e14342. doi: 10.1371/journal.pone.0014342
122. Mikelsaar, R., Paves, H., Org, K., and Mikelsaar, A. V. (2014). Chromosome variant 1qh-and its influence on the 3D organization of chromosome 1 heterochromatin in interphase nucleus of patients with endometriosis. J. Genet. 93, 219-223. doi: 10.1007/s12041-014-0340-9
123. Miller, A. B., Wall, C., Baines, C. J., Sun, P., To, T., and Narod, S. A. (2014). Twenty five year follow-up for breast cancer incidence and mortality of the Canadian National Breast Screening Study: randomised screening trial. BMJ 348, g366. doi: 10.1136/bmj.g366
124. Mitelman, F., Johansson, B., and Mertens, F. (2007). The impact of translocations and gene fusions on cancer causation. Nat. Rev. Cancer 7, 233-245. doi: 10.1038/nrc2091
125. Moen, P. T. Jr., Johnson, C. V., Byron, M., Shopland, L. S., de la Serna, I. L., Imbalzano, A. N., et al. (2004). Repositioning of muscle-specific genes relative to the periphery of SC-35 domains during skeletal myogenesis. Mol. Biol. Cell 15, 197-206. doi: 10.1091/mbc.E03-06-0388
126. Montironi, R., Mazzuccheli, R., Scarpelli, M., Lopez-Beltran, A., Fellegara, G., and Algaba, F. (2005). Gleason grading of prostate cancer in needle biopsies or radical prostatectomy specimens: contemporary approach, current clinical significance and sources of pathology discrepancies. BJU Int. 95, 1146-1152. doi: 10.1111/j.1464-410X.2005.05540.x
127. Morey, C., Kress, C., and Bickmore, W. A. (2009). Lack of bystander activation shows that localization exterior to chromosome territories is not sufficient to up-regulate gene expression. Genome Res. 19, 1184-1194. doi: 10.1101/gr.089045.108
128. Moss, S. F., Krivosheyev, V., de Souza, A., Chin, K., Gaetz, H. P., Chaudhary, N., et al. (1999). Decreased and aberrant nuclear lamin expression in gastrointestinal tract neoplasms. Gut 45, 723-729. doi: 10.1136/gut.45.5.723
129. Muhlmann, M. (2002). Molecular cytogenetics in metaphase and interphase cells for cancer and genetic research, diagnosis and prognosis. Application in tissue sections and cell suspensions. Genet. Mol. Res. 1, 117-127.
130. Murata, S., Nakazawa, T., Ohno, N., Terada, N., Iwashina, M., Mochizuki, K., et al. (2007). Conservation and alteration of chromosome territory arrangements in thyroid carcinoma cell nuclei. Thyroid 17, 489-496. doi: 10.1089/thy.2006.0328
131. Narendra, V., Rocha, P. P., An, D., Raviram, R., Skok, J. A., Mazzoni, E. O., et al. (2015). CTCF establishes discrete functional chromatin domains at the Hox clusters during differentiation. Science 347, 1017-1021. doi: 10.1126/science.1262088
132. Neems, D. S., Garza-Gongora, A. G., Smith, E. D., and Kosak, S. T. (2016). Topologically associated domains enriched for lineage-specific genes reveal expression-dependent nuclear topologies during myogenesis. Proc. Natl. Acad. Sci. U.S.A. 113, E1691-E1700. doi: 10.1073/pnas.1521826113
133. Nemeth, A., Conesa, A., Santoyo-Lopez, J., Medina, I., Montaner, D., Peterfia, B., et al. (2010). Initial genomics of the human nucleolus. PLoS Genet. 6:e1000889. doi: 10.1371/journal.pgen.1000889
134. Neves, H., Ramos, C., da Silva, M. G., Parreira, A., and Parreira, L. (1999). The nuclear topography of ABL, BCR, PML, and RARalpha genes: evidence for gene proximity in specific phases of the cell cycle and stages of hematopoietic differentiation. Blood 93, 1197-1207.
135. Nielsen, B., Albregtsen, F., and Danielsen, H. E. (2008). Statistical nuclear texture analysis in cancer research: a review of methods and applications. Crit. Rev. Oncog. 14, 89-164. doi: 10.1615/CritRevOncog.v14.i2-3.10
136. Nora, E. P., Lajoie, B. R., Schulz, E. G., Giorgetti, L., Okamoto, I., Servant, N., et al. (2012). Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 485, 381-385. doi: 10.1038/nature11049
137. Palstra, R. J., Simonis, M., Klous, P., Brasset, E., Eijkelkamp, B., and de Laat, W. (2008). Maintenance of long-range DNA interactions after inhibition of ongoing RNA polymerase II transcription. PLoS ONE 3:e1661. doi: 10.1371/journal.pone.0001661
138. Parada, L., McQueen, P., and Misteli, T. (2004). Tissue-specific spatial organization of genomes. Genome Biol. 5, R44. doi: 10.1186/gb-2004-5-7-r44
139. Parada, L. A., McQueen, P. G., Munson, P. J., and Misteli, T. (2002). Conservation of relative chromosome positioning in normal and cancer cells. Curr. Biol. 12, 1692-1697. doi: 10.1016/S0960-9822(02)01166-1
140. Parada, L. A., Roix, J. J., and Misteli, T. (2003). An uncertainty principle in chromosome positioning. Trends Cell Biol, 13, 393-396. doi: 10.1016/S0962-8924(03)00149-1
141. Paz, N., Felipe-Blanco, I., Royo, F., Zabala, A., Guerra-Merino, I., Garcia-Orad, A., et al. (2015). Expression of the DYRK1A gene correlates with its 3D positioning in the interphase nucleus of down syndrome cells. Chromosome Res. 23, 285-298. doi: 10.1007/s10577-015-9467-7
142. Paz, N., Zabala, A., Royo, F., Garcia-Orad, A., Zugaza, J. L., and Parada, L. A. (2013). Combined fluorescent-chromogenic in situ hybridization for identification and laser microdissection of interphase chromosomes. PLoS ONE 8:e60238. doi: 10.1371/journal.pone.0060238
143. Peric-Hupkes, D., Meuleman, W., Pagie, L., Bruggeman, S. W., Solovei, I., Brugman, W., et al. (2010). Molecular maps of the reorganization of genome-nuclear lamina interactions during differentiation. Mol. Cell. 38, 603-613. doi: 10.1016/j.molcel.2010.03.016
144. Pichugina, T., Sugawara, T., Kaykov, A., Schierding, W., Masuda, K., Uewaki, J., et al. (2016). A diffusion model for the coordination of DNA replication in Schizosaccharomyces pombe. Sci. Rep. 6, 18757. doi: 10.1038/srep18757
145. Pickersgill, H., Kalverda, B., de Wit, E., Talhout, W., Fornerod, M., and van Steensel, B. (2006). Characterization of the Drosophila melanogaster genome at the nuclear lamina. Nat. Genet. 38, 1005-1014. doi: 10.1038/ng1852
146. Ragoczy, T., Bender, M. A., Telling, A., Byron, R., and Groudine, M. (2006). The locus control region is required for association of the murine beta-globin locus with engaged transcription factories during erythroid maturation. Genes Dev. 20, 1447-1457. doi: 10.1101/gad.1419506
147. Ragoczy, T., Telling, A., Sawado, T., Groudine, M., and Kosak, S. T. (2003). A genetic analysis of chromosome territory looping: diverse roles for distal regulatory elements. Chromosome Res. 11, 513-525. doi: 10.1023/A:1024939130361
148. Ranade, D., Koul, S., Thompson, J., Prasad, K. B., and Sengupta, K. (2016). Chromosomal aneuploidies induced upon Lamin B2 depletion are mislocalized in the interphase nucleus. Chromosoma doi: 10.1007/s00412-016-0580-y [Epub ahead of print].
149. Randise-Hinchliff, C., Coukos, R., Sood, V., Sumner, M. C., Zdraljevic, S., Meldi Sholl, L., et al. (2016). Strategies to regulate transcription factor-mediated gene positioning and interchromosomal clustering at the nuclear periphery. J. Cell Biol. 212, 633-646. doi: 10.1083/jcb.201508068
150. Rao, S. S., Huntley, M. H., Durand, N. C., Stamenova, E. K., Bochkov, I. D., Robinson, J. T., et al. (2014). A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159, 1665-1680. doi: 10.1016/j.cell.2014.11.021
151. Reddy, K. L., Zullo, J. M., Bertolino, E., and Singh, H. (2008). Transcriptional repression mediated by repositioning of genes to the nuclear lamina. Nature 452, 243-247. doi: 10.1038/nature06727
152. Rodley, C. D., Bertels, F., Jones, B., and O'Sullivan, J. M. (2009). Global identification of yeast chromosome interactions using Genome conformation capture. Fungal Genet. Biol. 46, 879-886. doi: 10.1016/j.fgb.2009.07.006
153. Roix, J. J., McQueen, P. G., Munson, P. J., Parada, L. A., and Misteli, T. (2003). Spatial proximity of translocation-prone gene loci in human lymphomas. Nat. Genet. 34, 287-291. doi: 10.1038/ng1177
154. Roukos, V., Voss, T. C., Schmidt, C. K., Lee, S., Wangsa, D., and Misteli, T. (2013). Spatial dynamics of chromosome translocations in living cells. Science 341, 660-664. doi: 10.1126/science.1237150
155. Saarinen, I., Mirtti, T., Seikkula, H., Bostrom, P. J., and Taimen, P. (2015). Differential predictive roles of A-and B-Type nuclear lamins in prostate cancer progression. PLoS ONE 10:e0140671. doi: 10.1371/journal.pone.0140671
156. Sandhu, G. S., and Andriole, G. L. (2012). Overdiagnosis of prostate cancer. J. Natl. Cancer Inst. Monogr. 2012, 146-151. doi: 10.1093/jncimonographs/lgs031
157. Scaffidi, P., and Misteli, T. (2005). Reversal of the cellular phenotype in the premature aging disease Hutchinson-Gilford progeria syndrome. Nat. Med. 11, 440-445. doi: 10.1038/nm1204
158. Scheuermann, M. O., Tajbakhsh, J., Kurz, A., Saracoglu, K., Eils, R., and Lichter, P. (2004). Topology of genes and nontranscribed sequences in human interphase nuclei. Exp. Cell Res. 301, 266-279. doi: 10.1016/j.yexcr.2004.08.031
159. Schnitt, S. J. (2010). Classification and prognosis of invasive breast cancer: from morphology to molecular taxonomy. Mod. Pathol. 23(Suppl. 2), S60-S64. doi: 10.1038/modpathol.2010.33
160. Schoenfelder, S., Sexton, T., Chakalova, L., Cope, N. F., Horton, A., Andrews, S., et al. (2010). Preferential associations between co-regulated genes reveal a transcriptional interactome in erythroid cells. Nat. Genet. 42, 53-61. doi: 10.1038/ng.496
161. Sexton, T., Yaffe, E., Kenigsberg, E., Bantignies, F., Leblanc, B., Hoichman, M., et al. (2012). Three-dimensional folding and functional organization principles of the Drosophila genome. Cell 148, 458-472. doi: 10.1016/j.cell.2012.01.010
162. Shachar, S., Voss, T. C., Pegoraro, G., Sciascia, N., and Misteli, T. (2015). Identification of gene positioning factors using high-throughput imaging mapping. Cell 162, 911-923. doi: 10.1016/j.cell.2015.07.035
163. Shopland, L. S., Lynch, C. R., Peterson, K. A., Thornton, K., Kepper, N., Hase, J., et al. (2006). Folding and organization of a contiguous chromosome region according to the gene distribution pattern in primary genomic sequence. J. Cell Biol. 174, 27-38. doi: 10.1083/jcb.200603083
164. Siegel, R. L., Miller, K. D., and Jemal, A. (2016). Cancer statistics, 2016. CA Cancer J. Clin. 66, 7-30. doi: 10.3322/caac.21332
165. Simonis, M., Klous, P., Splinter, E., Moshkin, Y., Willemsen, R., de Wit, E., et al. (2006). Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation capture-on-chip (4C). Nat. Genet. 38, 1348-1354. doi: 10.1038/ng1896
166. Smemo, S., Tena, J. J., Kim, K. H., Gamazon, E. R., Sakabe, N. J., Gomez-Marin, C., et al. (2014). Obesity-associated variants within FTO form long-range functional connections with IRX3. Nature 507, 371-375. doi: 10.1038/nature13138
167. Solovei, I., Kreysing, M., Lanctot, C., Kosem, S., Peichl, L., Cremer, T., et al. (2009). Nuclear architecture of rod photoreceptor cells adapts to vision in mammalian evolution. Cell 137, 356-368. doi: 10.1016/j.cell.2009.01.052
168. Solovei, I., Schermelleh, L., During, K., Engelhardt, A., Stein, S., Cremer, C., et al. (2004). Differences in centromere positioning of cycling and postmitotic human cell types. Chromosoma 112, 410-423. doi: 10.1007/s00412-004-0287-3
169. Solovei, I., Thanisch, K., and Feodorova, Y. (2016). How to rule the nucleus: divide et impera. Curr. Opin. Cell Biol. 40, 47-59. doi: 10.1016/j.ceb.2016.02.014
170. Solovei, I., Wang, A. S., Thanisch, K., Schmidt, C. S., Krebs, S., Zwerger, M., et al. (2013). LBR and lamin A/C sequentially tether peripheral heterochromatin and inversely regulate differentiation. Cell 152, 584-598. doi: 10.1016/j.cell.2013.01.009
171. Sorlie, T., Perou, C. M., Tibshirani, R., Aas, T., Geisler, S., Johnsen, H., et al. (2001). Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc. Natl. Acad. Sci. U.S.A. 98, 10869-10874. doi: 10.1073/pnas.191367098
172. Soutoglou, E., Dorn, J. F., Sengupta, K., Jasin, M., Nussenzweig, A., Ried, T., et al. (2007). Positional stability of single double-strand breaks in mammalian cells. Nat. Cell Biol. 9, 675-682. doi: 10.1038/ncb1591
173. Taddei, A., Van Houwe, G., Hediger, F., Kalck, V., Cubizolles, F., Schober, H., et al. (2006). Nuclear pore association confers optimal expression levels for an inducible yeast gene. Nature 441, 774-778. doi: 10.1038/nature04845
174. Taimen, P., Pfleghaar, K., Shimi, T., Moller, D., Ben-Harush, K., Erdos, M. R., et al. (2009). A progeria mutation reveals functions for lamin A in nuclear assembly, architecture, and chromosome organization. Proc. Natl. Acad. Sci. U.S.A. 106, 20788-20793. doi: 10.1073/pnas.0911895106
175. Takizawa, T., Gudla, P. R., Guo, L., Lockett, S., and Misteli, T. (2008a). Allele-specific nuclear positioning of the monoallelically expressed astrocyte marker GFAP. Genes Dev. 22, 489-498. doi: 10.1101/gad.1634608
176. Takizawa, T., Meaburn, K. J., and Misteli, T. (2008b). The meaning of gene positioning. Cell 135, 9-13. doi: 10.1016/j.cell.2008.09.026
177. Tan-Wong, S. M., Wijayatilake, H. D., and Proudfoot, N. J. (2009). Gene loops function to maintain transcriptional memory through interaction with the nuclear pore complex. Genes Dev. 23, 2610-2624. doi: 10.1101/gad.1823209
178. Therizols, P., Illingworth, R. S., Courilleau, C., Boyle, S., Wood, A. J., and Bickmore, W. A. (2014). Chromatin decondensation is sufficient to alter nuclear organization in embryonic stem cells. Science 346, 1238-1242. doi: 10.1126/science.1259587
179. Thompson, I., Thrasher, J. B., Aus, G., Burnett, A. L., Canby-Hagino, E. D., Cookson, M. S., et al. (2007). Guideline for the management of clinically localized prostate cancer: 2007 update. J. Urol. 177, 2106-2131. doi: 10.1016/j.juro.2007.03.003
180. Thompson, M., Haeusler, R. A., Good, P. D., and Engelke, D. R. (2003). Nucleolar clustering of dispersed tRNA genes. Science 302, 1399-1401. doi: 10.1126/science.1089814
181. Timme, S., Schmitt, E., Stein, S., Schwarz-Finsterle, J., Wagner, J., Walch, A., et al. (2011). Nuclear position and shape deformation of chromosome 8 territories in pancreatic ductal adenocarcinoma. Anal. Cell. Pathol. (Amst). 34, 21-33. doi: 10.3233/ACP-2011-0004
182. Tjong, H., Gong, K., Chen, L., and Alber, F. (2012). Physical tethering and volume exclusion determine higher-order genome organization in budding yeast. Genome Res. 22, 1295-1305. doi: 10.1101/gr.129437.111
183. Torre, L. A., Bray, F., Siegel, R. L., Ferlay, J., Lortet-Tieulent, J., and Jemal, A. (2015). Global cancer statistics, 2012. CA Cancer J. Clin. 65, 87-108. doi: 10.3322/caac.21262
184. Towbin, B. D., Gonzalez-Aguilera, C., Sack, R., Gaidatzis, D., Kalck, V., Meister, P., et al. (2012). Step-wise methylation of histone H3K9 positions heterochromatin at the nuclear periphery. Cell 150, 934-947. doi: 10.1016/j.cell.2012.06.051
185. Van der Kwast, T. H. (2014). Prognostic prostate tissue biomarkers of potential clinical use. Virchows Arch. 464, 293-300. doi: 10.1007/s00428-014-1540-7
186. van Koningsbruggen, S., Gierlinski, M., Schofield, P., Martin, D., Barton, G. J., Ariyurek, Y., et al. (2010). High-resolution whole-genome sequencing reveals that specific chromatin domains from most human chromosomes associate with nucleoli. Mol. Biol. Cell 21, 3735-3748. doi: 10.1091/mbc.E10-06-0508
187. van Steensel, B., and Dekker, J. (2010). Genomics tools for unraveling chromosome architecture. Nat. Biotechnol. 28, 1089-1095. doi: 10.1038/nbt.1680
188. Veltri, R. W., and Christudass, C. S. (2014). Nuclear morphometry, epigenetic changes, and clinical relevance in prostate cancer. Adv. Exp. Med. Biol. 773, 77-99. doi: 10.1007/978-1-4899-8032-8_4
189. Venables, R. S., McLean, S., Luny, D., Moteleb, E., Morley, S., Quinlan, R. A., et al. (2001). Expression of individual lamins in basal cell carcinomas of the skin. Br. J. Cancer 84, 512-519. doi: 10.1054/bjoc.2000.1632
190. Volpi, E. V., Chevret, E., Jones, T., Vatcheva, R., Williamson, J., Beck, S., et al. (2000). Large-scale chromatin organization of the major histocompatibility complex and other regions of human chromosome 6 and its response to interferon in interphase nuclei. J. Cell Sci. 113 (Pt 9), 1565-1576.
191. Wang, Q., Sawyer, I. A., Sung, M. H., Sturgill, D., Shevtsov, S. P., Pegoraro, G., et al. (2016). Cajal bodies are linked to genome conformation. Nat. Commun. 7, 10966. doi: 10.1038/ncomms10966
192. Wansink, D. G., Schul, W., van der Kraan, I., van Steensel, B., van Driel, R., and de Jong, L. (1993). Fluorescent labelling of nascent RNA reveals transcription by RNA polymerase II in domains scattered throughout the nucleus. J. Cell Biol. 122, 282-293. doi: 10.1083/jcb.122.2.283
193. Wazir, U., Ahmed, M. H., Bridger, J. M., Harvey, A., Jiang, W. G., Sharma, A. K., et al. (2013). The clinicopathological significance of lamin A/C, lamin B1 and lamin B receptor mRNA expression in human breast cancer. Cell. Mol. Biol. Lett. 18, 595-611. doi: 10.2478/s11658-013-0109-9
194. Welch, H. G., and Black, W. C. (2010). Overdiagnosis in cancer. J. Natl. Cancer Inst. 102, 605-613. doi: 10.1093/jnci/djq099
195. Wiech, T., Stein, S., Lachenmaier, V., Schmitt, E., Schwarz-Finsterle, J., Wiech, E., et al. (2009). Spatial allelic imbalance of BCL2 genes and chromosome 18 territories in nonneoplastic and neoplastic cervical squamous epithelium. Eur. Biophys. J. 38, 793-806. doi: 10.1007/s00249-009-0474-5
196. Wiech, T., Timme, S., Riede, F., Stein, S., Schuricke, M., Cremer, C., et al. (2005). Human archival tissues provide a valuable source for the analysis of spatial genome organization. Histochem. Cell Biol. 123, 229-238. doi: 10.1007/s00418-005-0768-3
197. Wijchers, P. J., Geeven, G., Eyres, M., Bergsma, A. J., Janssen, M., Verstegen, M., et al. (2015). Characterization and dynamics of pericentromere-associated domains in mice. Genome Res. 25, 958-969. doi: 10.1101/gr.186643.114
198. Wijchers, P. J., Krijger, P. H., Geeven, G., Zhu, Y., Denker, A., Verstegen, M. J., et al. (2016). Cause and consequence of tethering a subTAD to different nuclear compartments. Mol. Cell 61, 461-473. doi: 10.1016/j.molcel.2016.01.001
199. Williams, R. R., Azuara, V., Perry, P., Sauer, S., Dvorkina, M., Jorgensen, H., et al. (2006). Neural induction promotes large-scale chromatin reorganisation of the Mash1 locus. J. Cell Sci. 119, 132-140. doi: 10.1242/jcs.02727
200. Williams, R. R., Broad, S., Sheer, D., and Ragoussis, J. (2002). Subchromosomal positioning of the epidermal differentiation complex (EDC) in keratinocyte and lymphoblast interphase nuclei. Exp. Cell Res. 272, 163-175. doi: 10.1006/excr.2001.5400
201. Willis, N. D., Cox, T. R., Rahman-Casans, S. F., Smits, K., Przyborski, S. A., van den Brandt, P., et al. (2008). Lamin A/C is a risk biomarker in colorectal cancer. PLoS ONE 3:e2988. doi: 10.1371/journal.pone.0002988
202. Zeitz, M. J., Ay, F., Heidmann, J. D., Lerner, P. L., Noble, W. S., Steelman, B. N., et al. (2013). Genomic interaction profiles in breast cancer reveal altered chromatin architecture. PLoS ONE 8:e73974. doi: 10.1371/journal.pone.0073974
203. Zink, D., Amaral, M. D., Englmann, A., Land, S., Clarke, L. A., Rudolph, C., et al. (2004a). Transcription-dependent spatial arrangement of CFTR and adjacent genes in human cell nuclei. J. Cell Biol. 166, 815-825. doi: 10.1083/jcb.200404107
204. Zink, D., Fische, A. H., and Nickerson, J. A. (2004b). Nuclear structure in cancer cells. Nat. Rev. Cancer 4, 677-687. doi: 10.1038/nrc1430
205. Zuleger, N., Boyle, S., Kelly, D. A., de Las Heras, J. I., Lazou, V., Korfali, N., et al. (2013). Specific nuclear envelope transmembrane proteins can promote the location of chromosomes to and from the nuclear periphery. Genome Biol. 14, R14. doi: 10.1186/gb-2013-14-2-r14
206. Zullo, J. M., Demarco, I. A., Pique-Regi, R., Gaffney, D. J., Epstein, C. B., Spooner, C. J., et al. (2012). DNA sequence-dependent compartmentalization and silencing of chromatin at the nuclear lamina. Cell 149, 1474-1487. doi: 10.1016/j.cell.2012.04.035