Nuclear Shape Changes Are Induced by Knockdown of the SWI/SNF ATPase BRG1 and Are Independent of Cytoskeletal Connections

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Imbalzano, Karen M ^a   Cohet, Nathalie ^a   Wu, Qiong ^a   Underwood, Jean M ^a   Imbalzano, Anthony N ^a   Nickerson, Jeffrey A ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRG1 PROTEIN;

ARTICLE; BREAST EPITHELIUM; BREAST METASTASIS; CANCER CELL CULTURE; CELL NUCLEUS; CELL ULTRASTRUCTURE; CONTROLLED STUDY; CYTOLOGY; CYTOSKELETON; ENZYME ACTIVITY; ENZYME ASSAY; EPITHELIUM CELL; HETEROCHROMATIN; MICROTUBULE; NUCLEAR LAMINA; PROTEIN EXPRESSION;

BLOTTING, WESTERN; BREAST; BREAST NEOPLASMS; CELL NUCLEUS; CELLS, CULTURED; CHROMATIN ASSEMBLY AND DISASSEMBLY; CYTOPLASM; CYTOSKELETON; DNA HELICASES; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; NUCLEAR PROTEINS; RNA, SMALL INTERFERING; TRANSCRIPTION FACTORS;

EID: 84873548412     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0055628     Document Type: Article

References (78)

1. Imbalzano AN, Kwon H, Green MR, Kingston RE, (1994) Facilitated binding of TATA-binding protein to nucleosomal DNA. Nature 370: 481-485.
2. Kwon H, Imbalzano AN, Khavari PA, Kingston RE, Green MR, (1994) Nucleosome disruption and enhancement of activator binding by a human SW1/SNF complex. Nature 370: 477-481.
3. Clapier CR, Cairns BR, (2009) The biology of chromatin remodeling complexes. Annu Rev Biochem 78: 273-304.
4. Liu R, Jiang B, Yu H, Chaput JC, (2011) Generating DNA synbodies from previously discovered peptides. Chembiochem 12: 1813-1817.
5. Khavari PA, Peterson CL, Tamkun JW, Mendel DB, Crabtree GR, (1993) BRG1 contains a conserved domain of the SWI2/SNF2 family necessary for normal mitotic growth and transcription. Nature 366: 170-174.
6. Muchardt C, Yaniv M, (1993) A human homologue of Saccharomyces cerevisiae SNF2/SWI2 and Drosophila brm genes potentiates transcriptional activation by the glucocorticoid receptor. Embo J 12: 4279-4290.
7. Wang W, Xue Y, Zhou S, Kuo A, Cairns BR, et al. (1996) Diversity and specialization of mammalian SWI/SNF complexes. Genes Dev 10: 2117-2130.
8. Cohet N, Stewart KM, Mudhasani R, Asirvatham AJ, Mallappa C, et al. (2010) SWI/SNF chromatin remodeling enzyme ATPases promote cell proliferation in normal mammary epithelial cells. J Cell Physiol 223: 667-678.
9. Bultman SJ, Herschkowitz JI, Godfrey V, Gebuhr TC, Yaniv M, et al. (2008) Characterization of mammary tumors from Brg1 heterozygous mice. Oncogene 27: 460-468.
10. Serber DW, Rogala A, Makarem M, Rosson GB, Simin K, et al. (2012) The BRG1 chromatin remodeler protects against ovarian cysts, uterine tumors, and mammary tumors in a lineage-specific manner. PLoS One 7: e31346.
11. Bultman S, Gebuhr T, Yee D, La Mantia C, Nicholson J, et al. (2000) A Brg1 null mutation in the mouse reveals functional differences among mammalian SWI/SNF complexes. Mol Cell 6: 1287-1295.
12. Zink D, Fischer AH, Nickerson JA, (2004) Nuclear structure in cancer cells. Nat Rev Cancer 4: 677-687.
13. Haroske G, Dimmer V, Friedrich K, Meyer W, Thieme B, et al. (1996) Nuclear image analysis of immunohistochemically stained cells in breast carcinomas. Histochem Cell Biol 105: 479-485.
14. Giardina C, Renzulli G, Serio G, Caniglia DM, Lettini T, et al. (1996) Nuclear morphometry in node-negative breast carcinoma. Anal Quant Cytol Histol 18: 374-382.
15. Capell BC, Collins FS, (2006) Human laminopathies: nuclei gone genetically awry. Nat Rev Genet 7: 940-952.
16. Worman HJ, (2012) Nuclear lamins and laminopathies. J Pathol 226: 316-325.
17. Bank EM, Gruenbaum Y, (2011) The nuclear lamina and heterochromatin: a complex relationship. Biochem Soc Trans 39: 1705-1709.
18. Maniotis AJ, Chen CS, Ingber DE, (1997) Demonstration of mechanical connections between integrins, cytoskeletal filaments, and nucleoplasm that stabilize nuclear structure. Proc Natl Acad Sci U S A 94: 849-854.
19. Wang N, Tytell JD, Ingber DE, (2009) Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat Rev Mol Cell Biol 10: 75-82.
20. Mazumder A, Roopa T, Kumar A, Iyer KV, Ramdas NM, et al. (2010) Prestressed nuclear organization in living cells. Methods Cell Biol 98: 221-239.
21. Franke WW, (1971) Relationship of nuclear membranes with filaments and microtubules. Protoplasma 73: 263-292.
22. Capco DG, Wan KM, Penman S, (1982) The nuclear matrix: three-dimensional architecture and protein composition. Cell 29: 847-858.
23. Jones JC, Goldman AE, Steinert PM, Yuspa S, Goldman RD, (1982) Dynamic aspects of the supramolecular organization of intermediate filament networks in cultured epidermal cells. Cell Motil 2: 197-213.
24. Fey EG, Capco DG, Krochmalnic G, Penman S, (1984) Epithelial structure revealed by chemical dissection and unembedded electron microscopy. J Cell Biol 99: 203s-208s.
25. Vikstrom KL, Borisy GG, Goldman RD, (1989) Dynamic aspects of intermediate filament networks in BHK-21 cells. Proc Natl Acad Sci U S A 86: 549-553.
26. Djabali K, Portier MM, Gros F, Blobel G, Georgatos SD, (1991) Network antibodies identify nuclear lamin B as a physiological attachment site for peripherin intermediate filaments. Cell 64: 109-121.
27. Carmo-Fonseca M, Cidadao AJ, David-Ferreira JF, (1988) Filamentous cross-bridges link intermediate filaments to the nuclear pore complexes. Eur J Cell Biol 45: 282-290.
28. Crisp M, Liu Q, Roux K, Rattner JB, Shanahan C, et al. (2006) Coupling of the nucleus and cytoplasm: role of the LINC complex. J Cell Bio 172: 41-53.
29. Starr DA, Fridolfsson HN, (2010) Interactions between nuclei and the cytoskeleton are mediated by SUN-KASH nuclear-envelope bridges. Annu Rev Cell Dev Biol 26: 421-444.
30. Padmakumar VC, Abraham S, Braune S, Noegel AA, Tunggal B, et al. (2004) Enaptin, a giant actin-binding protein, is an element of the nuclear membrane and the actin cytoskeleton. Exp Cell Res 295: 330-339.
31. Zhen YY, Libotte T, Munck M, Noegel AA, Korenbaum E, (2002) NUANCE, a giant protein connecting the nucleus and actin cytoskeleton. J Cell Sci 115: 3207-3222.
32. Ketema M, Wilhelmsen K, Kuikman I, Janssen H, Hodzic D, et al. (2007) Requirements for the localization of nesprin-3 at the nuclear envelope and its interaction with plectin. J Cell Sci 120: 3384-3394.
33. Wilhelmsen K, Litjens SH, Kuikman I, Tshimbalanga N, Janssen H, et al. (2005) Nesprin-3, a novel outer nuclear membrane protein, associates with the cytoskeletal linker protein plectin. J Cell Biol 171: 799-810.
34. Roux KJ, Crisp ML, Liu Q, Kim D, Kozlov S, et al. (2009) Nesprin 4 is an outer nuclear membrane protein that can induce kinesin-mediated cell polarization. Proc Natl Acad Sci U S A 106: 2194-2199.
35. Lombardi ML, Jaalouk DE, Shanahan CM, Burke B, Roux KJ, et al. (2011) The interaction between nesprins and sun proteins at the nuclear envelope is critical for force transmission between the nucleus and cytoskeleton. J Biol Chem 286: 26743-26753.
36. Debnath J, Muthuswamy SK, Brugge JS, (2003) Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 30: 256-268.
37. Javed A, Barnes GL, Pratap J, Antkowiak T, Gerstenfeld LC, et al. (2005) Impaired intranuclear trafficking of Runx2 (AML3/CBFA1) transcription factors in breast cancer cells inhibits osteolysis in vivo. Proc Natl Acad Sci U S A 102: 1454-1459.
38. Cailleau R, Olive M, Cruciger QV, (1978) Long-term human breast carcinoma cell lines of metastatic origin: preliminary characterization. In Vitro 14: 911-915.
39. Marshall PN, (1983) Papanicolaou staining-a review. Microsc Acta 87: 233-243.
40. Wagner S, Chiosea S, Nickerson JA, (2003) The spatial targeting and nuclear matrix binding domains of SRm160. Proc Natl Acad Sci U S A 100: 3269-3274.
41. Underwood JM, Imbalzano KM, Weaver VM, Fischer AH, Imbalzano AN, et al. (2006) The ultrastructure of MCF-10A acini. J Cell Physiol 208: 141-148.
42. Feoli F, Paesmans M, Van Eeckhout P, (2008) Fine needle aspiration cytology of the breast: impact of experience on accuracy, using standardized cytologic criteria. Acta Cytol 52: 145-151.
43. Paesmans M, (2008) [Stage IV NSCLC. Prognostic factors]. Rev Mal Respir 25: 3S99-106.
44. Shimi T, Butin-Israeli V, Adam SA, Goldman RD, (2010) Nuclear lamins in cell regulation and disease. Cold Spring Harb Symp Quant Biol 75: 525-531.
45. Dittmer TA, Misteli T, (2011) The lamin protein family. Genome Biol 12: 222.
46. Goulbourne CN, Malhas AN, Vaux DJ, (2011) The induction of a nucleoplasmic reticulum by prelamin A accumulation requires CTP:phosphocholine cytidylyltransferase-alpha. J Cell Sci 124: 4253-4266.
47. Fricker M, Hollinshead M, White N, Vaux D, (1997) Interphase nuclei of many mammalian cell types contain deep, dynamic, tubular membrane-bound invaginations of the nuclear envelope. J Cell Bio 136: 531-544.
48. Spector I, Shochet NR, Kashman Y, Groweiss A, (1983) Latrunculins: novel marine toxins that disrupt microfilament organization in cultured cells. Science 219: 493-495.
49. Spector I, Shochet NR, Blasberger D, Kashman Y, (1989) Latrunculins-novel marine macrolides that disrupt microfilament organization and affect cell growth: I. Comparison with cytochalasin D. Cell Motil Cytoskeleton. 13: 127-144.
50. Yarmola EG, Somasundaram T, Boring TA, Spector I, Bubb MR, (2000) Actin-latrunculin A structure and function. Differential modulation of actin-binding protein function by latrunculin A. J Biol Chem 275: 28120-28127.
51. Martin SS, Leder P, (2001) Human MCF10A mammary epithelial cells undergo apoptosis following actin depolymerization that is independent of attachment and rescued by Bcl-2. Mol Cell Biol 21: 6529-6536.
52. Enomoto T, (1996) Microtubule disruption induces the formation of actin stress fibers and focal adhesions in cultured cells: possible involvement of the rho signal cascade. Cell Struct Funct 21: 317-326.
53. Vasiliev JM, Gelfand IM, Domnina LV, Ivanova OY, Komm SG, et al. (1970) Effect of colcemid on the locomotory behaviour of fibroblasts. J Embryol Exp Morphol 24: 625-640.
54. Gordon JA, (1991) Use of vanadate as protein-phosphotyrosine phosphatase inhibitor. Methods Enzymol 201: 477-482.
55. Strnad P, Windoffer R, Leube RE, (2002) Induction of rapid and reversible cytokeratin filament network remodeling by inhibition of tyrosine phosphatases. J Cell Sci 115: 4133-4148.
56. Wang W, Cote J, Xue Y, Zhou S, Khavari PA, et al. (1996) Purification and biochemical heterogeneity of the mammalian SWI-SNF complex. Embo J 15: 5370-5382.
57. Mazumder A, Shivashankar GV, (2010) Emergence of a prestressed eukaryotic nucleus during cellular differentiation and development. J R Soc Interface 7Suppl 3: S321-330.
58. Dunaief JL, Strober BE, Guha S, Khavari PA, Alin K, et al. (1994) The retinoblastoma protein and BRG1 form a complex and cooperate to induce cell cycle arrest. Cell 79: 119-130.
59. Strober BE, Dunaief JL, Guha, Goff SP, (1996) Functional interactions between the hBRM/hBRG1 transcriptional activators and the pRB family of proteins. Mol Cell Biol 16: 1576-1583.
60. Asp P, Wihlborg M, Karlen M, Farrants AK, (2002) Expression of BRG1, a human SWI/SNF component, affects the organisation of actin filaments through the RhoA signalling pathway. J Cell Sci 115: 2735-2746.
61. Shanahan F, Seghezzi W, Parry D, Mahony D, Lees E, (1999) Cyclin E associates with BAF155 and BRG1, components of the mammalian SWI-SNF complex, and alters the ability of BRG1 to induce growth arrest. Mol Cell Biol 19: 1460-1469.
62. Hill DA, Chiosea S, Jamaluddin S, Roy K, Fischer AH, et al. (2004) Inducible changes in cell size and attachment area due to expression of a mutant SWI/SNF chromatin remodeling enzyme. J Cell Sci 117: 5847-5854.
63. Bannister AJ, Kouzarides T, (2011) Regulation of chromatin by histone modifications. Cell Res 21: 381-395.
64. Kim SI, Bresnick EH, Bultman SJ, (2009) BRG1 directly regulates nucleosome structure and chromatin looping of the alpha globin locus to activate transcription. Nucleic Acids Res 37: 6019-6027.
65. Kim SI, Bultman SJ, Kiefer CM, Dean A, Bresnick EH, (2009) BRG1 requirement for long-range interaction of a locus control region with a downstream promoter. Proc Natl Acad Sci U S A 106: 2259-2264.
66. Hu Q, Kwon YS, Nunez E, Cardamone MD, Hutt KR, et al. (2008) Enhancing nuclear receptor-induced transcription requires nuclear motor and LSD1-dependent gene networking in interchromatin granules. Proc Natl Acad Sci U S A 105: 19199-19204.
67. Cai S, Lee CC, Kohwi-Shigematsu T, (2006) SATB1 packages densely looped, transcriptionally active chromatin for coordinated expression of cytokine genes. Nat Genet 38: 1278-1288.
68. Beale LS, (1860) Examination of sputum from a case of cancer of the pharynx and the adjacent parts. Archives of Medicine, London 2: 44.
69. Wu JI, (2012) Diverse functions of ATP-dependent chromatin remodeling complexes in development and cancer. Acta Biochim Biophys Sin (Shanghai) 44: 54-69.
70. Wilson BG, Roberts CW, (2011) SWI/SNF nucleosome remodellers and cancer. Nat Rev Cancer 11: 481-492.
71. Lin H, Wong RP, Martinka M, Li G, (2010) BRG1 expression is increased in human cutaneous melanoma. Br J Dermatol 163: 502-510.
72. Sun A, Tawfik O, Gayed B, Thrasher JB, Hoestje S, et al. (2007) Aberrant expression of SWI/SNF catalytic subunits BRG1/BRM is associated with tumor development and increased invasiveness in prostate cancers. Prostate 67: 203-213.
73. Heeboll S, Borre M, Ottosen PD, Andersen CL, Mansilla F, et al. (2008) SMARCC1 expression is upregulated in prostate cancer and positively correlated with tumour recurrence and dedifferentiation. Histol Histopathol 23: 1069-1076.
74. Sentani K, Oue N, Kondo H, Kuraoka K, Motoshita J, et al. (2001) Increased expression but not genetic alteration of BRG1, a component of the SWI/SNF complex, is associated with the advanced stage of human gastric carcinomas. Pathobiology 69: 315-320.
75. Watanabe T, Semba S, Yokozaki H, (2011) Regulation of PTEN expression by the SWI/SNF chromatin-remodelling protein BRG1 in human colorectal carcinoma cells. Br J Cancer 104: 146-154.
76. Saladi SV, Keenen B, Marathe HG, Qi H, Chin KV, et al. (2010) Modulation of extracellular matrix/adhesion molecule expression by BRG1 is associated with increased melanoma invasiveness. Mol Cancer 9: 280.
77. Bourgo RJ, Siddiqui H, Fox S, Solomon D, Sansam CG, et al. (2009) SWI/SNF deficiency results in aberrant chromatin organization, mitotic failure, and diminished proliferative capacity. Mol Biol Cell 20: 3192-3199.
78. Webster M, Witkin KL, Cohen-Fix O, (2009) Sizing up the nucleus: nuclear shape, size and nuclear-envelope assembly. J Cell Sci 122: 1477-1486.