Comparative ultrastructure of CRM1-nucleolar bodies (CNoBs), intranucleolar bodies (INBs) and hybrid PML/p62 bodies uncovers new facets of nuclear body dynamic and diversity

Nucleus

Volumn 6, Issue 4, 2015, Pages 326-338

  Souquere, Sylvie ^a   Weil, Dominique ^b   Pierron, Gérard ^a  

^a Institut Gustave Roussy   (France)

^b SORBONNE UNIVERSITÉ   (France)

Author keywords

CNoB; Immunoelectron microscopy; INB; Nuclear bodies; Nuclear organization; Nucleolus; P62 SQSTM1; PML bodies; SUMO; Ubiquitin

Indexed keywords

EXPORTIN 1; LEPTOMYCIN B; PROMYELOCYTIC LEUKEMIA PROTEIN; PROTEIN P62; SUMO 1 PROTEIN; SUMO 2 PROTEIN; SUMO 3 PROTEIN; UBIQUITIN; CELL RECEPTOR; CHROMATIN; EXPORTIN 1 PROTEIN; KARYOPHERIN; SUMO1 PROTEIN, HUMAN; UNSATURATED FATTY ACID;

ARTICLE; CELL NUCLEUS INCLUSION BODY; CELL ULTRASTRUCTURE; COMPARATIVE STUDY; CONTROLLED STUDY; HELA CELL LINE; HETEROCHROMATIN; HUMAN; HUMAN CELL; IMMUNOELECTRON MICROSCOPY; IMMUNOFLUORESCENCE MICROSCOPY; IN SITU HYBRIDIZATION; INTRANUCLEOLAR BODY; NUCLEOLUS; VITREOUS BODY; ACTIVE TRANSPORT; CHEMISTRY; CHROMATIN; GENETICS; METABOLISM; ULTRASTRUCTURE;

ACTIVE TRANSPORT, CELL NUCLEUS; CELL NUCLEOLUS; CHROMATIN; FATTY ACIDS, UNSATURATED; HELA CELLS; HUMANS; INTRANUCLEAR INCLUSION BODIES; KARYOPHERINS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SUMO-1 PROTEIN;

EID: 84954567696     PISSN: 19491034     EISSN: 19491042     Source Type: Journal    
DOI: 10.1080/19491034.2015.1082695     Document Type: Article

References (66)

1. Lallemand-Breitenbach V, de The H. PML nuclear bodies. Cold Spring Harb Perspect Biol 2010; 2: a000661; PMID:20452955; http://dx.doi.org/10.1101/cshperspect.a000661
2. Mao YS, Zhang B, Spector DL. Biogenesis and function of nuclear bodies. Trends Genet 2011; 27:295-306; PMID:21680045; http://dx.doi.org/10.1016/j. tig.2011.05.006
3. Matera AG, Izaguire-Sierra M, Praveen K, Rajendra TK. Nuclear bodies: random aggregates of sticky proteins or crucibles of macromolecular assembly? Dev Cell 2009; 17:639-47; PMID:19922869; http://dx.doi.org/10.1016/j.devcel.2009.10.017
4. Koken MH, Puvion-Dutilleul F, Guillemin MC, Viron A, Linares-Cruz G, Stuurman N, de Jong L, Szostecki C, Calvo F, Chomienne C, et al. The t (15;17) translocation alters a nuclear body in a retinoic acid-reversible fashion. Embo J 1994; 13:1073-83; PMID:8131741
5. Monneron A, Bernhard W. Fine structural organization of the interphase nucleus in some mammalian cells. J Ultrastruct Res 1969; 27:266-88; PMID:5813971; http://dx.doi.org/10.1016/S0022-5320(69)80017-1
6. Navascues J, Berciano MT, Tucker KE, Lafarga M, Matera AG. Targeting SMN to Cajal bodies and nuclear gems during neuritogenesis. Chromosoma 2004; 112:398-409; PMID:15164213; http://dx.doi. org/10.1007/s00412-004-0285-5
7. Raska I, Andrade LE, Ochs RL, Chan EK, Chang CM, Roos G, Tan EM. Immunological and ultrastructural studies of the nuclear coiled body with autoimmune antibodies. Exp Cell Res 1991; 195:27-37; PMID:2055273; http://dx.doi.org/10.1016/0014-4827(91)90496-H
8. Raska I, Ochs RL, Andrade LE, Chan EK, Burlingame R, Peebles C, Gruol D, Tan EM. Association between the nucleolus and the coiled body. J Struct Biol 1990; 104:120-7; PMID:2088441; http://dx.doi.org/10.1016/1047-8477(90)90066-L
9. Souquere S, Beauclair G, Harper F, Fox A, Pierron G. Highly ordered spatial organization of the structural long noncoding NEAT1 RNAs within paraspeckle nuclear bodies. Mol Biol Cell 2010; 21:4020-7; PMID:20881053; http://dx.doi.org/10.1091/mbc. E10-08-0690
10. Visa N, Puvion-Dutilleul F, Bachellerie JP, Puvion E. Intranuclear distribution of U1 and U2 snRNAs visualized by high resolution in situ hybridization: revelation of a novel compartment containing U1 but not U2 snRNA in HeLa cells. Eur J Cell Biol 1993; 60:308-21; PMID:8330629
11. Weis K, Rambaud S, Lavau C, Jansen J, Carvalho T, n Carmo-Fonseca M, Lamond A, Dejean A. Retinoic acid regulates aberrant nuclear localization of PML-RAR alpha in acute promyelocytic leukemia cells. Cell 1994; 76:345-56; PMID:8293468; http://dx.doi.org/ 10.1016/0092-8674(94)90341-7
12. Fong KW, Li Y, Wang W, Ma W, Li K, Qi RZ, Liu D, Songyang Z, Chen J. Whole-genome screening identifies proteins localized to distinct nuclear bodies. J Cell Biol 2013; 203:149-64; PMID:24127217; http://dx.doi.org/10.1083/jcb.201303145 www.tandfonline.com
13. Chen T, Boisvert FM, Bazett-Jones DP, Richard S. A role for the GSG domain in localizing Sam68 to novel nuclear structures in cancer cell lines. Mol Biol Cell 1999; 10:3015-33; PMID:10473643; http://dx.doi. org/10.1091/mbc.10.9.3015
14. Griffis ER, Altan N, Lippincott-Schwartz J, Powers MA. Nup98 is a mobile nucleoporin with transcription-dependent dynamics. Mol Biol Cell 2002; 13:1282-97; PMID:11950939; http://dx.doi.org/10.1091/mbc.01-11-0538
15. Ernoult-Lange M, Wilczynska A, Harper M, Aigueperse C, Dautry F, Kress M, Weil D. Nucleocytoplasmic traffic of CPEB1 and accumulation in Crm1 nucleolar bodies. Mol Biol Cell 2009; 20:176-87; PMID:18923137; http://dx.doi.org/10.1091/mbc.E08-09-0904
16. Hutten S, Prescott A, James J, Riesenberg S, Boulon S, Lam YW, Lamond AI. An intranucleolar body associated with rDNA. Chromosoma 2011; 120:481-99; PMID:21698343; http://dx.doi.org/10.1007/s00412- 011-0327-8
17. Marnef A, Weil D, Standart N. RNA-related nuclear functions of human Pat1b, the P-body mRNA decay factor. Mol Biol Cell 2012; 23:213-24; PMID:22090346; http://dx.doi.org/10.1091/mbc.E11-05-0415
18. Ghule PN, Dominski Z, Yang XC, Marzluff WF, Becker KA, Harper JW, Lian JB, Stein JL, van Wijnen AJ, Stein GS. Staged assembly of histone gene expression machinery at subnuclear foci in the abbreviated cell cycle of human embryonic stem cells. Proc Natl Acad Sci USA 2008; 105:16964-9; PMID:18957539; http://dx.doi.org/10.1073/pnas.0809273105
19. Hadjolov AA. The nucleolus and Ribosome biogenesis. 1985
20. Boisvert FM, van Koningsbruggen S, Navascues J, Lamond AI. The multifunctional nucleolus. Nat Rev Mol Cell Biol 2007; 8:574-85; PMID:17519961; http://dx.doi.org/10.1038/nrm2184
21. Politz JC, Polena I, Trask I, Bazett-Jones DP, Pederson T. A nonribosomal landscape in the nucleolus revealed by the stem cell protein nucleostemin. Mol Biol Cell 2005; 16:3401-10; PMID:15857956; http://dx.doi. org/10.1091/mbc.E05-02-0106
22. Andersen JS, Lyon CE, Fox AH, Leung AK, Lam YW, Steen H, Mann M, Lamond AI. Directed proteomic analysis of the human nucleolus. Curr Biol 2002; 12:11; PMID:11790298; http://dx.doi.org/10.1016/ S0960-9822(01)00650-9
23. Scherl A, Coute Y, Deon C, Calle A, Kindbeiter K, Sanchez JC, Greco A, Hochstrasser D, Diaz JJ. Functional proteomic analysis of human nucleolus. Mol Biol Cell 2002; 13:4100-9; PMID:12429849; http:// dx.doi.org/10.1091/mbc.E02-05-0271
24. Boulon S, Westman BJ, Hutten S, Boisvert FM, Lamond AI. The nucleolus under stress. Mol Cell 2010; 40:216-27; PMID:20965417; http://dx.doi.org/10.1016/j.molcel.2010.09.024
25. Pankiv S, Lamark T, Bruun JA, Overvatn A, Bjorkoy G, Johansen T. Nucleocytoplasmic shuttling of p62/ SQSTM1 and its role in recruitment of nuclear polyubiquitinated proteins to promyelocytic leukemia bodies. J Biol Chem 2010; 285:5941-53; PMID:20018885; http://dx.doi.org/10.1074/jbc.M109.039925 Nucleus
26. Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, Outzen H, Overvatn A, Bjorkoy G, Johansen T. p62/ SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem 2007; 282:24131-45; PMID:17580304; http://dx.doi.org/10.1074/jbc.M702824200
27. Bjorkoy G, Lamark T, Brech A, Outzen H, Perander M, Overvatn A, Stenmark H, Johansen T. p62/ SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtininduced cell death. J Cell Biol 2005; 171:603-14; PMID:16286508; http://dx.doi.org/10.1083/jcb.200507002
28. Clausen TH, Lamark T, Isakson P, Finley K, Larsen KB, Brech A, Overvatn A, Stenmark H, Bjorkoy G, Simonsen A, et al. p62/SQSTM1 and ALFY interact to facilitate the formation of p62 bodies/ALIS and their degradation by autophagy. Autophagy 2010; 6:330-44; PMID:20168092; http://dx.doi.org/10.4161/ auto.6.3.11226
29. Hirose T, Virnicchi G, Tanigawa A, Naganuma T, Li R, Kimura H, Yokoi T, Nakagawa S, Benard M, Fox AH, et al. NEAT1 long noncoding RNA regulates transcription via protein sequestration within subnuclear bodies. Mol Biol Cell 2014; 25(1):169-83; PMID:24173718
30. Boulon S, Verheggen C, Jady BE, Girard C, Pescia C, Paul C, Ospina JK, Kiss T, Matera AG, Bordonne R, et al. PHAX and CRM1 are required sequentially to transport U3 snoRNA to nucleoli. Mol Cell 2004; 16:777-87; PMID:15574332; http://dx.doi.org/10.1016/j.molcel.2004.11.013
31. Sleeman J. A regulatory role for CRM1 in the multidirectional trafficking of splicing snRNPs in the mammalian nucleus. J Cell Sci 2007; 120:1540-50; PMID:17405816; http://dx.doi.org/10.1242/ jcs.001529
32. Andrade LE, Chan EK, Raska I, Peebles CL, Roos G, Tan EM. Human autoantibody to a novel protein of the nuclear coiled body: immunological characterization and cDNA cloning of p80-coilin. J Exp Med 1991; 173:1407-19; PMID:2033369; http://dx.doi.org/10.1084/jem.173.6.1407
33. Ochs RL, Stein TW, Jr., Tan EM. Coiled bodies in the nucleolus of breast cancer cells. J Cell Sci 1994; 107(Pt 2):385-99; PMID:8207070
34. Tapia O, Bengoechea R, Berciano MT, Lafarga M. Nucleolar targeting of coilin is regulated by its hypomethylation state. Chromosoma 2010; 119:527-40; PMID:20449600; http://dx.doi.org/10.1007/s00412-010-0276-7
35. Sleeman J, Lyon CE, Platani M, Kreivi JP, Lamond AI. Dynamic interactions between splicing snRNPs, coiled bodies and nucleoli revealed using snRNP protein fusions to the green fluorescent protein. Exp Cell Res 1998; 243:290-304; PMID:9743589; http://dx.doi.org/10.1006/excr.1998.4135
36. Pederson T, Tsai RY. In search of nonribosomal nucleolar protein function and regulation. J Cell Biol 2009; 184:771-6; PMID:19289796; http://dx.doi.org/10.1083/jcb.200812014
37. Desterro JM, Keegan LP, Jaffray E, Hay RT, O’Connell MA, Carmo-Fonseca M. SUMO-1 modification alters ADAR1 editing activity. Mol Biol Cell2005; 16:5115-26; PMID:16120648; http://dx.doi. org/10.1091/mbc.E05-06-0536
38. Pfander B, Moldovan GL, Sacher M, Hoege C, Jentsch S. SUMO-modified PCNA recruits Srs2 to prevent recombination during S phase. Nature 2005; 436:428-33; PMID:15931174
39. Hang LE, Lopez CR, Liu X, Williams JM, Chung I, Wei L, Bertuch AA, Zhao X. Regulation of Ku-DNA association by Yku70 C-terminal tail and SUMO modification. J Biol Chem 2014; 289:10308-17; PMID:24567323; http://dx.doi.org/10.1074/jbc.M113.526178
40. Wu Y, Wang L, Zhou P, Wang G, Zeng Y, Wang Y, Liu J, Zhang B, Liu S, Luo H, et al. Regulation of REGgamma cellular distribution and function by SUMO modification. Cell Res 2011; 21:807-16; PMID:21445096; http://dx.doi.org/10.1038/cr.2011.57
41. Goodarzi AA, Kurka T, Jeggo PA. KAP-1 phosphorylation regulates CHD3 nucleosome remodeling during the DNA double-strand break response. Nat Struct Mol Biol 2011; 18:831-9; PMID:21642969; http://dx.doi.org/10.1038/nsmb.2077
42. Zhao Q, Xie Y, Zheng Y, Jiang S, Liu W, Mu W, Liu Z, Zhao Y, Xue Y, Ren J. GPS-SUMO: a tool for the prediction of sumoylation sites and SUMO-interaction motifs. Nucleic Acids Res 2014; 42:W325-30; PMID:24880689; http://dx.doi.org/10.1093/nar/gku383
43. Pelisch F, Gerez J, Druker J, Schor IE, Munoz MJ, Risso G, Petrillo E, Westman BJ, Lamond AI, Arzt E, et al. The serine/arginine-rich protein SF2/ASF regu-lates protein sumoylation. Proc Natl Acad Sci U S A 2010; 107:16119-24; PMID:20805487; http://dx.doi.org/10.1073/pnas.1004653107
44. Scheer U, Weisenberger D. The nucleolus. Curr Opin Cell Biol 1994; 6:354-9; PMID:7917325; http://dx.doi.org/10.1016/0955-0674(94)90026-4
45. Neville M, Stutz F, Lee L, Davis LI, Rosbash M. The importin-beta family member Crm1p bridges the interaction between Rev and the nuclear pore complex during nuclear export. Curr Biol 1997; 7:767-75; PMID:9368759; http://dx.doi.org/10.1016/S0960-9822(06)00335-6
46. Xu S, Powers MA. Nup98-homeodomain fusions interact with endogenous Nup98 during interphase and localize to kinetochores and chromosome arms during mitosis. Mol Biol Cell 2010; 21:1585-96; PMID:20237156; http://dx.doi.org/10.1091/mbc.E09-07-0561
47. Carvalho T, Almeida F, Calapez A, Lafarga M, Berciano MT, Carmo-Fonseca M. The spinal muscular atrophy disease gene product, SMN: A link between snRNP biogenesis and the Cajal (coiled) body. J Cell Biol 1999; 147:715-28; PMID:10562276; http://dx.doi.org/10.1083/jcb.147.4.715
48. Thakar K, Karaca S, Port SA, Urlaub H, Kehlenbach RH. Identification of CRM1-dependent Nuclear Export Cargos Using Quantitative Mass Spectrometry. Mol Cell Proteomics 2013; 12:664-78; PMID:23242554; http://dx.doi.org/10.1074/mcp.M112.024877
49. Vernier M, Bourdeau V, Gaumont-Leclerc MF, Moiseeva O, Begin V, Saad F, Mes-Masson AM, Ferbeyre G. Regulation of E2Fs and senescence by PML nuclear bodies. Genes Dev 2013; 25:41-50; http://dx.doi.org/ 10.1101/gad.1975111
50. Lain S, Xirodimas D, Lane DP. Accumulating active p53 in the nucleus by inhibition of nuclear export: a novel strategy to promote the p53 tumor suppressor function. Exp Cell Res 1999; 253:315-24; PMID:10585254; http://dx.doi.org/10.1006/excr.1999.4672
51. Ruthardt M, Orleth A, Tomassoni L, Puccetti E, Riganelli D, Alcalay M, Mannucci R, Nicoletti I, Grignani F, Fagioli M, et al. The acute promyelocytic leukaemia specific PML and PLZF proteins localize to adjacent and functionally distinct nuclear bodies. Oncogene 1998; 16:1945-53; PMID:9591778; http://dx.doi.org/10.1038/sj.onc.1201722
52. Tashiro S, Muto A, Tanimoto K, Tsuchiya H, Suzuki H, Hoshino H, Yoshida M, Walter J, Igarashi K. Repression of PML nuclear body-associated transcription by oxidative stress-activated Bach2. Mol Cell Biol 2004; 24:3473-84; PMID:15060166; http://dx.doi.org/10.1128/MCB.24.8.3473-3484.2004
53. Buchberger E, El Harchi M, Payrhuber D, Zommer A, Schauer D, Simonitsch-Klupp I, Bilban M, Brostjan C. Overexpression of the transcriptional repressor complex BCL¡6/BCoR leads to nuclear aggregates distinct from classical aggresomes. PLoS One 2013; 8:e76845; PMID:24146931; http://dx.doi.org/10.1371/journal.pone.0076845
54. Briers S, Crawford C, Bickmore WA, Sutherland HG. KRAB zinc-finger proteins localise to novel KAP1-containing foci that are adjacent to PML nuclear bodies. J Cell Sci 2009; 122:937-46; PMID:19258395; http:// dx.doi.org/10.1242/jcs.034793
55. Tsukamoto T, Hashiguchi N, Janicki SM, Tumbar T, Belmont AS, Spector DL. Visualization of gene activity in living cells. Nat Cell Biol 2000; 2:871-8; PMID:11146650; http://dx.doi.org/10.1038/35046510
56. Kaiser TE, Intine RV, Dundr M. De novo formation of a subnuclear body. Science 2008; 322:1713-7; PMID:18948503; http://dx.doi.org/10.1126/ science.1165216
57. Sahin U, Ferhi O, Jeanne M, Benhenda S, Berthier C, Jollivet F, Niwa-Kawakita M, Faklaris O, Setterblad N, de The H, et al. Oxidative stress-induced assembly of PML nuclear bodies controls sumoylation of partner proteins. J Cell Biol 2014; 204:931-45; PMID:24637324; http://dx.doi.org/10.1083/jcb.201305148
58. Brangwynne CP. Phase transitions and size scaling of membrane-less organelles. J Cell Biol 2013; 203:875-81; PMID:24368804; http://dx.doi.org/10.1083/jcb.201308087
59. Brangwynne CP, Mitchison TJ, Hyman AA. Active liquid-like behavior of nucleoli determines their size and shape in Xenopus laevis oocytes. Proc Natl Acad Sci U S A 2011; 108:4334-9; PMID:21368180; http://dx. doi.org/10.1073/pnas.1017150108
60. Hubstenberger A, Noble SL, Cameron C, Evans TC. Translation repressors, an RNA helicase, and developmental cues control RNP phase transitions during early development. Dev Cell 2013; 27:161-73; PMID:24176641; http://dx.doi.org/10.1016/j.devcel.2013.09.024
61. Lafarga M, Berciano MT, Pena E, Mayo I, Castano JG, Bohmann D, Rodrigues JP, Tavanez JP, Carmo-Fonseca M. Clastosome: a subtype of nuclear body enriched in 19S and 20S proteasomes, ubiquitin, and protein substrates of proteasome. Mol Biol Cell 2002; 13:2771-82; PMID:12181345; http://dx.doi.org/ 10.1091/mbc.E02-03-0122
62. Guo L, Giasson BI, Glavis-Bloom A, Brewer MD, Shorter J, Gitler AD, Yang X. A cellular system that degrades misfolded proteins and protects against neurodegeneration. Mol Cell 2014; 55:15-30; PMID:24882209; http://dx.doi.org/10.1016/j.molcel.2014.04.030
63. Janer A, Martin E, Muriel MP, Latouche M, Fujigasaki H, Ruberg M, Brice A, Trottier Y, Sittler A. PML clastosomes prevent nuclear accumulation of mutant ataxin-7 and other polyglutamine proteins. J Cell Biol 2006; 174:65-76; PMID:16818720; http://dx.doi.org/10.1083/jcb.200511045
64. Daniel MT, Koken M, Romagne O, Barbey S, Bazarbachi A, Stadler M, Guillemin MC, Degos L, Chomienne C, de The H. PML protein expression in hematopoietic and acute promyelocytic leukemia cells. Blood 1993; 82:1858-67; PMID:8400236
65. Souquere S, Mollet S, Kress M, Dautry F, Pierron G, Weil D. Unravelling the ultrastructure of stress granules and associated P-bodies in human cells. J Cell Sci 2009; 122:3619-26; PMID:19812307; http://dx.doi.org/10.1242/jcs.054437
66. Souquere S, Pierron G. Ultrastructural analysis of nuclear bodies using electron microscopy. Methods Mol Biol 2015; 1262:105-18; PMID:25555578; http://dx.doi.org/10.1007/978-1-4939-2253-6_7