Knock-down of methyl CpG-binding protein 2 (MeCP2) causes alterations in cell proliferation and nuclear lamins expression in mammalian cells

BMC Cell Biology

Volumn 13, Issue , 2012, Pages

  Babbio, Federica ^a   Castiglioni, Ilaria ^a   Cassina, Chiara ^a   Gariboldi, Marzia B ^a   Pistore, Christian ^a   Magnani, Elena ^a   Badaracco, Gianfranco ^a   Monti, Elena ^a   Bonapace, Ian M ^a  

^a UNIVERSITY OF INSUBRIA   (Italy)

Author keywords

Cell proliferation; Methyl CpG binding protein 2 (MeCP2); Nuclear lamins

Indexed keywords

LAMIN A; LAMIN B; LAMIN B RECEPTOR; LAMIN C; MEMBRANE PROTEIN; METHYL CPG BINDING PROTEIN 2; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL AGING; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CELL NUCLEUS MEMBRANE; CELL PROLIFERATION; CELL VIABILITY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; GENE SILENCING; HETEROCHROMATIN; HUMAN; HUMAN CELL; MAMMAL CELL; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION;

ANIMALS; CELL CYCLE CHECKPOINTS; CELL LINE; CELL NUCLEUS; CELL PROLIFERATION; CELL SURVIVAL; HUMANS; LAMIN TYPE A; LAMIN TYPE B; METHYL-CPG-BINDING PROTEIN 2; MICE; NIH 3T3 CELLS; NUCLEAR ENVELOPE; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RNA INTERFERENCE; RNA, SMALL INTERFERING;

MAMMALIA; MURINAE;

EID: 84863585768     PISSN: None     EISSN: 14712121     Source Type: Journal    
DOI: 10.1186/1471-2121-13-19     Document Type: Article

References (57)

1. Gadalla KK, Bailey ME, Cobb SR. MeCP2 and Rett syndrome: reversibility and potential avenues for therapy. Biochem J 2011, 439(1):1-14. 10.1042/BJ20110648, 21916843.
2. Amir RE, Van den Veyver IB, Wan M, Tran CQ, Francke U, Zoghbi HY. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat Genet 1999, 23(2):185-188. 10.1038/13810, 10508514.
3. Mann J, Chu DC, Maxwell A, Oakley F, Zhu NL, Tsukamoto H, Mann DA. MeCP2 controls an epigenetic pathway that promotes myofibroblast transdifferentiation and fibrosis. Gastroenterology 2010, 138(2):705-714. 714 e701-704, 10.1053/j.gastro.2009.10.002, 2819585, 19843474.
4. Tao H, Huang C, Yang JJ, Ma TT, Bian EB, Zhang L, Lv XW, Jin Y, Li J. MeCP2 controls the expression of RASAL1 in the hepatic fibrosis in rats. Toxicology 2011, 290(2-3):327-333.
5. Joss-Moore LA, Wang Y, Ogata EM, Sainz AJ, Yu X, Callaway CW, McKnight RA, Albertine KH, Lane RH. IUGR differentially alters MeCP2 expression and H3K9Me3 of the PPARgamma gene in male and female rat lungs during alveolarization. Birth Defects Res A Clin Mol Teratol 2011, 91(8):672-681. 10.1002/bdra.20783, 3152656, 21425435.
6. Balmer D, Arredondo J, Samaco RC, LaSalle JM. MECP2 mutations in Rett syndrome adversely affect lymphocyte growth, but do not affect imprinted gene expression in blood or brain. Hum Genet 2002, 110(6):545-552. 10.1007/s00439-002-0724-4, 12107440.
7. Nagai K, Miyake K, Kubota T. A transcriptional repressor MeCP2 causing Rett syndrome is expressed in embryonic non-neuronal cells and controls their growth. Brain Res Dev Brain Res 2005, 157(1):103-106.
8. Squillaro T, Alessio N, Cipollaro M, Renieri A, Giordano A, Galderisi U. Partial silencing of methyl cytosine protein binding 2 (MECP2) in mesenchymal stem cells induces senescence with an increase in damaged DNA. FASEB J 2010, 24(5):1593-1603. 10.1096/fj.09-143057, 20065105.
9. Bernard D, Gil J, Dumont P, Rizzo S, Monte D, Quatannens B, Hudson D, Visakorpi T, Fuks F, de Launoit Y. The methyl-CpG-binding protein MECP2 is required for prostate cancer cell growth. Oncogene 2006, 25(9):1358-1366. 10.1038/sj.onc.1209179, 16331274.
10. Yaqinuddin A, Qureshi SA, Qazi R, Abbas F. Down-regulation of DNMT3b in PC3 cells effects locus-specific DNA methylation, and represses cellular growth and migration. Cancer Cell Int 2008, 8:13. 10.1186/1475-2867-8-13, 2564899, 18798999.
11. Clouaire T, Stancheva I. Methyl-CpG binding proteins: specialized transcriptional repressors or structural components of chromatin?. Cell Mol Life Sci 2008, 65(10):1509-1522. 10.1007/s00018-008-7324-y, 2873564, 18322651.
12. Georgel PT, Horowitz-Scherer RA, Adkins N, Woodcock CL, Wade PA, Hansen JC. Chromatin compaction by human MeCP2. Assembly of novel secondary chromatin structures in the absence of DNA methylation. J Biol Chem 2003, 278(34):32181-32188. 10.1074/jbc.M305308200, 12788925.
13. Brero A, Easwaran HP, Nowak D, Grunewald I, Cremer T, Leonhardt H, Cardoso MC. Methyl CpG-binding proteins induce large-scale chromatin reorganization during terminal differentiation. J Cell Biol 2005, 169(5):733-743. 10.1083/jcb.200502062, 2171616, 15939760.
14. Agarwal N, Hardt T, Brero A, Nowak D, Rothbauer U, Becker A, Leonhardt H, Cardoso MC. MeCP2 interacts with HP1 and modulates its heterochromatin association during myogenic differentiation. Nucleic Acids Res 2007, 35(16):5402-5408. 10.1093/nar/gkm599, 2018631, 17698499.
15. Furuta K, Chan EK, Kiyosawa K, Reimer G, Luderschmidt C, Tan EM. Heterochromatin protein HP1Hsbeta (p25beta) and its localization with centromeres in mitosis. Chromosoma 1997, 106(1):11-19. 10.1007/s004120050219, 9169582.
16. Lewis JD, Meehan RR, Henzel WJ, Maurer-Fogy I, Jeppesen P, Klein F, Bird A. Purification, sequence, and cellular localization of a novel chromosomal protein that binds to methylated DNA. Cell 1992, 69(6):905-914. 10.1016/0092-8674(92)90610-O, 1606614.
17. Polioudaki H, Kourmouli N, Drosou V, Bakou A, Theodoropoulos PA, Singh PB, Giannakouros T, Georgatos SD. Histones H3/H4 form a tight complex with the inner nuclear membrane protein LBR and heterochromatin protein 1. EMBO Rep 2001, 2(10):920-925. 10.1093/embo-reports/kve199, 1084077, 11571267.
18. Guarda A, Bolognese F, Bonapace IM, Badaracco G. Interaction between the inner nuclear membrane lamin B receptor and the heterochromatic methyl binding protein, MeCP2. Exp Cell Res 2009, 315(11):1895-1903. 10.1016/j.yexcr.2009.01.019, 19331822.
19. Liokatis S, Edlich C, Soupsana K, Giannios I, Panagiotidou P, Tripsianes K, Sattler M, Georgatos SD, Politou AS. Solution structure and molecular interactions of the lamin B receptor tudor domain. J Biol Chem 2012, 287(2):1032-1042. 10.1074/jbc.M111.281303, 22052904.
20. Moir RD, Spann TP, Goldman RD. The dynamic properties and possible functions of nuclear lamins. Int Rev Cytol 1995, 162B:141-182.
21. Stuurman N, Heins S, Aebi U. Nuclear lamins: their structure, assembly, and interactions. J Struct Biol 1998, 122(1-2):42-66.
22. Zuleger N, Robson MI, Schirmer EC. The nuclear envelope as a chromatin organizer. Nucleus 2011, 2(5):339-349. 10.4161/nucl.2.5.17846, 3322583, 21970986.
23. Guttinger S, Laurell E, Kutay U. Orchestrating nuclear envelope disassembly and reassembly during mitosis. Nat Rev Mol Cell Biol 2009, 10(3):178-191. 10.1038/nrm2641, 19234477.
24. Naetar N, Foisner R. Lamin complexes in the nuclear interior control progenitor cell proliferation and tissue homeostasis. Cell Cycle 2009, 8(10):1488-1493. 10.4161/cc.8.10.8499, 19377295.
25. Schirmer EC. The epigenetics of nuclear envelope organization and disease. Mutat Res 2008, 647(1-2):112-121.
26. Worman HJ. Nuclear lamins and laminopathies. J Pathol 2012, 226(2):316-325. 10.1002/path.2999, 21953297.
27. Lammerding J, Schulze PC, Takahashi T, Kozlov S, Sullivan T, Kamm RD, Stewart CL, Lee RT. Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction. J Clin Invest 2004, 113(3):370-378. 324542, 14755334.
28. Goldman RD, Shumaker DK, Erdos MR, Eriksson M, Goldman AE, Gordon LB, Gruenbaum Y, Khuon S, Mendez M, Varga R, et al. Accumulation of mutant lamin A causes progressive changes in nuclear architecture in Hutchinson-Gilford progeria syndrome. Proc Natl Acad Sci U S A 2004, 101(24):8963-8968. 10.1073/pnas.0402943101, 428455, 15184648.
29. Gruenbaum Y, Margalit A, Goldman RD, Shumaker DK, Wilson KL. The nuclear lamina comes of age. Nat Rev Mol Cell Biol 2005, 6(1):21-31. 10.1038/nrm1550, 15688064.
30. Vermeulen K, Van Bockstaele DR, Berneman ZN. Apoptosis: mechanisms and relevance in cancer. Ann Hematol 2005, 84(10):627-639. 10.1007/s00277-005-1065-x, 16041532.
31. Lu L, Osmond DG. Apoptosis during B lymphopoiesis in mouse bone marrow. J Immunol 1997, 158(11):5136-5145.
32. Dimri GP, Lee X, Basile G, Acosta M, Scott G, Roskelley C, Medrano EE, Linskens M, Rubelj I, Pereira-Smith O, et al. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci U S A 1995, 92(20):9363-9367. 10.1073/pnas.92.20.9363, 40985, 7568133.
33. Lleonart ME, Artero-Castro A, Kondoh H. Senescence induction; a possible cancer therapy. Mol Cancer 2009, 8:3. 10.1186/1476-4598-8-3, 2631463, 19133111.
34. Blagosklonny MV. Cell senescence: hypertrophic arrest beyond the restriction point. J Cell Physiol 2006, 209(3):592-597. 10.1002/jcp.20750, 17001692.
35. Lentini L, Barra V, Schillaci T, Di Leonardo A. MAD2 depletion triggers premature cellular senescence in human primary fibroblasts by activating a P53 pathway preventing aneuploid cells propagation. J Cell Physiol 2012, 227(9):3324-3332. 10.1002/jcp.24030, 22170163.
36. Oliver FJ, de la Rubia G, Rolli V, Ruiz-Ruiz MC, de Murcia G, Murcia JM. Importance of poly(ADP-ribose) polymerase and its cleavage in apoptosis. Lesson from an uncleavable mutant. J Biol Chem 1998, 273(50):33533-33539. 10.1074/jbc.273.50.33533, 9837934.
37. Narita M, Narita M, Krizhanovsky V, Nunez S, Chicas A, Hearn SA, Myers MP, Lowe SW. A novel role for high-mobility group a proteins in cellular senescence and heterochromatin formation. Cell 2006, 126(3):503-514. 10.1016/j.cell.2006.05.052, 16901784.
38. Lazebnik YA, Cole S, Cooke CA, Nelson WG, Earnshaw WC. Nuclear events of apoptosis in vitro in cell-free mitotic extracts: a model system for analysis of the active phase of apoptosis. J Cell Biol 1993, 123(1):7-22. 10.1083/jcb.123.1.7, 2119808, 8408207.
39. Gotzmann J, Vlcek S, Foisner R. Caspase-mediated cleavage of the chromosome-binding domain of lamina-associated polypeptide 2 alpha. J Cell Sci 2000, 113(Pt 21):3769-3780.
40. Cohen M, Lee KK, Wilson KL, Gruenbaum Y. Transcriptional repression, apoptosis, human disease and the functional evolution of the nuclear lamina. Trends Biochem Sci 2001, 26(1):41-47. 10.1016/S0968-0004(00)01727-8, 11165516.
41. Mounkes LC, Burke B, Stewart CL. The A-type lamins: nuclear structural proteins as a focus for muscular dystrophy and cardiovascular diseases. Trends Cardiovasc Med 2001, 11(7):280-285. 10.1016/S1050-1738(01)00126-8, 11709282.
42. Shumaker DK, Dechat T, Kohlmaier A, Adam SA, Bozovsky MR, Erdos MR, Eriksson M, Goldman AE, Khuon S, Collins FS, et al. Mutant nuclear lamin A leads to progressive alterations of epigenetic control in premature aging. Proc Natl Acad Sci U S A 2006, 103(23):8703-8708. 10.1073/pnas.0602569103, 1472659, 16738054.
43. Wang Y, Panteleyev AA, Owens DM, Djabali K, Stewart CL, Worman HJ. Epidermal expression of the truncated prelamin A causing Hutchinson-Gilford progeria syndrome: effects on keratinocytes, hair and skin. Hum Mol Genet 2008, 17(15):2357-2369. 10.1093/hmg/ddn136, 2733813, 18442998.
44. Dechat T, Shimi T, Adam SA, Rusinol AE, Andres DA, Spielmann HP, Sinensky MS, Goldman RD. Alterations in mitosis and cell cycle progression caused by a mutant lamin A known to accelerate human aging. Proc Natl Acad Sci U S A 2007, 104(12):4955-4960. 10.1073/pnas.0700854104, 1829246, 17360326.
45. Isaacs WB, Carter BS, Ewing CM. Wild-type p53 suppresses growth of human prostate cancer cells containing mutant p53 alleles. Cancer Res 1991, 51(17):4716-4720.
46. Herman JG, Merlo A, Mao L, Lapidus RG, Issa JP, Davidson NE, Sidransky D, Baylin SB. Inactivation of the CDKN2/p16/MTS1 gene is frequently associated with aberrant DNA methylation in all common human cancers. Cancer Res 1995, 55(20):4525-4530.
47. Balk SP, Knudsen KE. AR, the cell cycle, and prostate cancer. Nucl Recept Signal 2008, 6:e001. 2254330, 18301781.
48. Lanzi C, Cassinelli G, Cuccuru G, Supino R, Zuco V, Ferlini C, Scambia G, Zunino F. Cell cycle checkpoint efficiency and cellular response to paclitaxel in prostate cancer cells. Prostate 2001, 48(4):254-264. 10.1002/pros.1105, 11536305.
49. Burke B, Gerace L. A cell free system to study reassembly of the nuclear envelope at the end of mitosis. Cell 1986, 44(4):639-652. 10.1016/0092-8674(86)90273-4, 3948244.
50. Kutay U, Hetzer MW. Reorganization of the nuclear envelope during open mitosis. Curr Opin Cell Biol 2008, 20(6):669-677. 10.1016/j.ceb.2008.09.010, 2713602, 18938243.
51. Klose RJ, Bird AP. Genomic DNA methylation: the mark and its mediators. Trends Biochem Sci 2006, 31(2):89-97. 10.1016/j.tibs.2005.12.008, 16403636.
52. Chahrour M, Jung SY, Shaw C, Zhou X, Wong ST, Qin J, Zoghbi HY. MeCP2, a key contributor to neurological disease, activates and represses transcription. Science 2008, 320(5880):1224-1229. 10.1126/science.1153252, 2443785, 18511691.
53. Newport JW, Wilson KL, Dunphy WG. A lamin-independent pathway for nuclear envelope assembly. J Cell Biol 1990, 111(6 Pt 1):2247-2259. 2116431, 2277059.
54. Moir RD, Montag-Lowy M, Goldman RD. Dynamic properties of nuclear lamins: lamin B is associated with sites of DNA replication. J Cell Biol 1994, 125(6):1201-1212. 10.1083/jcb.125.6.1201, 2290916, 7911470.
55. Moir RD, Yoon M, Khuon S, Goldman RD. Nuclear lamins A and B1: different pathways of assembly during nuclear envelope formation in living cells. J Cell Biol 2000, 151(6):1155-1168. 10.1083/jcb.151.6.1155, 2190592, 11121432.
56. Makatsori D, Kourmouli N, Polioudaki H, Shultz LD, McLean K, Theodoropoulos PA, Singh PB, Georgatos SD. The inner nuclear membrane protein lamin B receptor forms distinct microdomains and links epigenetically marked chromatin to the nuclear envelope. J Biol Chem 2004, 279(24):25567-25573. 10.1074/jbc.M313606200, 15056654.
57. Wilson KL, Foisner R. Lamin-binding Proteins. Cold Spring Harb Perspect Biol 2010, 2(4):a000554. 10.1101/cshperspect.a000554, 2845209, 20452940.