Lamin a rod domain mutants target heterochromatin protein 1α and β for proteasomal degradation by activation of F-box protein, FBXW10

PLoS ONE

Volumn 5, Issue 5, 2010, Pages

  Chaturvedi, Pankaj ^a   Parnaik, Veena K ^a  

^a CENTRE FOR CELLULAR AND MOLECULAR BIOLOGY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

EMERIN; F BOX PROTEIN; FBXW10 PROTEIN; HETEROCHROMATIN PROTEIN 1; HETEROCHROMATIN PROTEIN 1ALPHA; HETEROCHROMATIN PROTEIN 1BETA; ISOPROTEIN; LAMIN A; MUTANT PROTEIN; PROTEASOME; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; BENZYLOXYCARBONYLLEUCYL LEUCYL LEUCINE ALDEHYDE; BENZYLOXYCARBONYLLEUCYL-LEUCYL-LEUCINE ALDEHYDE; BIOLOGICAL MARKER; CDRT1 PROTEIN, HUMAN; HETEROCHROMATIN SPECIFIC NONHISTONE CHROMOSOMAL PROTEIN HP 1; HETEROCHROMATIN-SPECIFIC NONHISTONE CHROMOSOMAL PROTEIN HP-1; HISTONE; LEUPEPTIN; MEMBRANE PROTEIN; NONHISTONE PROTEIN; NUCLEAR PROTEIN; PROTEIN;

ARTICLE; CELL NUCLEUS; CELL NUCLEUS MEMBRANE; CELL TYPE; CONTROLLED STUDY; ENZYME ACTIVITY; HELA CELL; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; PROTEIN STABILITY; PROTEIN TARGETING; TURNOVER TIME; UBIQUITINATION; WILD TYPE; CHEMISTRY; DRUG ANTAGONISM; DRUG EFFECT; GENETIC TRANSFECTION; GENETICS; METABOLISM; METHYLATION; PROTEIN PROCESSING; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT; SOLUBILITY;

BIOLOGICAL MARKERS; CHROMOSOMAL PROTEINS, NON-HISTONE; HELA CELLS; HISTONES; HUMANS; LAMIN TYPE A; LEUPEPTINS; MEMBRANE PROTEINS; METHYLATION; MUTANT PROTEINS; NUCLEAR ENVELOPE; NUCLEAR PROTEINS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN ISOFORMS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; PROTEINS; SOLUBILITY; TRANSFECTION;

EID: 77956278711     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0010620     Document Type: Article

References (62)

1. Goldman RD, Gruenbaum Y, Moir RD, Shumaker DK, Spann TP (2002) Nuclear lamins: Building blocks of nuclear architecture. Genes Dev 16: 533-547.
2. Worman HJ, Courvalin J-C (2005) Nuclear envelope, nuclear lamina and inherited disease. Int Rev Cytol 246: 231-279.
3. Broers JL, Ramaekers FC, Bonne G, Yaou RB, Hutchison CJ (2006) Nuclear lamins: laminopathies and their role in premature ageing. Physiol Rev 86: 967-1008.
4. Capell BC, Collins FS (2006) Human laminopathies: nuclei gone genetically awry. Nat Rev Genet 7: 940-952.
5. Dechat T, Pfleghaar K, Sengupta K, Shimi T, Shumaker DK, et al. (2008) Nuclear lamins: major factors in the structural organization and function of the nucleus and chromatin. Genes Dev 22: 832-853.
6. Parnaik VK (2008) Role of nuclear lamins in nuclear organization, cellular signaling and inherited diseases. Int Rev Cell Mol Biol 266: 157-206.
7. Zastrow MS, Vlcek S, Wilson KL (2004) Proteins that bind A-type lamins: integrated isolated clues. J Cell Sci 117: 979-987.
8. Schirmer EC, Foisner R (2007) Proteins that associate with lamins: Many faces, many functions. Exp Cell Res 313: 2167-2179.
9. Eriksson M, Brown WT, Gordon LB, Glynn MW, Singer J, et al. (2003) Recurrent de novo point mutations in lamin A cause Hutchinson-Gilford progeria syndrome. Nature 423: 293-298.
10. De Sandre-Giovannoli A, Bernard R, Cau P, Navarro C, Amiel J, et al. (2003) Lamin A truncation in Hutchinson-Gilford progeria. Science 300: 2055.
11. Goldman RD, Shumaker DK, Erdos MR, Eriksson M, Goldman AE, et al. (2004) Accumulation of mutant lamin A causes progressive changes in nucleararchitecture in Hutchinson-Gilford progeria syndrome. Proc Natl Acad Sci USA 101: 8963-8968.
12. Columbaro M, Capanni C, Mattioli E, Novelli G, Parnaik VK, et al. (2005) Rescue of heterochromatin organization in Hutchinson-Gilford progeria by drug treatment. Cell Mol Life Sci 62: 2669-2678.
13. Scaffidi P, Misteli T (2005) Reversal of the cellular phenotype in the premature aging disease Hutchinson-Gilford progeria syndrome. Nat Med 11: 440-445.
14. Shumaker DK, Dechat T, Kohlmaier A, Adam SA, Bozovsky MR, et al. (2006) Mutant nuclear lamin A leads to progressive alterations of epigenetic control in premature aging. Proc Natl Acad Sci USA 103: 8703-8708.
15. Filesi I, Gullotta F, Lattanzi G, D'Apice MR, Capanni C, et al. (2005) Alterations of nuclear envelope and chromatin organization in mandibuloacral dysplasia, a rare form of laminopathy. Physiol Genomics 23: 150-158.
16. Favreau C, Dubosclard E, Östlund C, Vigouroux C, Capeau J, et al. (2003) Expression of lamin A mutated in the carboxyl-terminal tail generates an aberrant nuclear phenotype similar to that observed in cells from patients with Dunnigan-type partial lipodystrophy and Emery-Dreifuss muscular dystrophy. Exp Cell Res 282: 14-23.
17. Wang Y, Herron AJ, Worman HJ (2006) Pathology and nuclear abnormalities in hearts of transgenic mice expressing M371K lamin A encoded by an LMNA mutation causing Emery-Dreifuss muscular dystrophy. Hum Mol Genet 15: 2479-2489.
18. Meaburn KJ, Cabuy E, Bonne G, Levy N, Morris GE, et al. (2007) Primary laminopathy fibroblasts display altered genome organization and apoptosis. Aging Cell 6: 139-153.
19. Östlund C, Bonne G, Schwartz K, Worman HJ (2001) Properties of lamin A mutants found in Emery-Dreifuss muscular dystrophy, cardiomyopathy and Dunnigan-type partial lipodystrophy. J Cell Sci 114: 4435-4445.
20. Raharjo WH, Enarson P, Sullivan T, Stewart CL, Burke B (2001) Nuclear envelope defects associated with LMNA mutations cause dilated cardiomyopathy and Emery-Dreifuss muscular dystrophy. J Cell Sci 114: 4447-4457.
21. Vigouroux C, Auclair M, Dubosclard E, Pouchelet M, Capeau J, et al. (2001) Nuclear envelope disorganisation in fibroblasts from lipodystrophic patients with heterozygous R482Q/W mutations in the lamin A/C gene. J Cell Sci 114: 4459-4468.
22. Manju K, Muralikrishna Bh, Parnaik VK (2006) Expression of disease-causing lamin mutants impairs the formation of DNA repair foci. J Cell Sci 119: 2704-2714.
23. Herrmann H, Bar H, Kreplak L, Strelkov S V, Aebi U (2007) Intermediate filaments: from cell architecture to nanomechanics. Nat Rev Mol Cell Biol 8: 562-573.
24. Parnaik VK, Manju K (2006) Laminopathies: multiple disorders arising from defects in nuclear architecture. J Biosci 31: 405-421.
25. Hiragami K, Festenstein R (2005) Heterochromatin protein 1, a pervasive controlling influence. Cell Mol Life Sci 62: 2711-2726.
26. Hediger F, Gasser SM (2006) Heterochromatin protein 1, don't judge the book by its cover. Curr Opin Genet Develop 16: 143-150.
27. Sims RJ, 3rd, Nishioka K, Reinberg D (2003) Histone lysine methylation: a signature for chromatin function. Trends Genet 19: 629-639.
28. Schotta G, Lachner M, Sarma K, Ebert A, Sengupta R, et al. (2004) A silencing pathway to induce H3-K9 and H4-K20 trimethylation at constitutive heterochromatin. Genes Dev 18: 1251-1262.
29. Capell BC, Erdos MR, Madigan JP, Fiordalisi JJ, Varga R, et al. (2005) Inhibiting farnesylation of progerin prevents the characteristic nuclear blebbing of Hutchinson-Gilford progeria syndrome. Proc Natl Acad Sci USA 102: 12879-12884.
30. Glynn MW, Glover TW (2005) Incomplete processing of mutant lamin A in Hutchinson-Gilford progeria leads to nuclear abnormalities, which are reversed by farnesyltransferase inhibition. Hum Mol Genet 14: 2959-2969.
31. Mallampalli MP, Huyer G, Bendale P, Gelb MH, Michaelis S (2005) Inhibiting farnesylation reverses the nuclear morphology defect in a HeLa cell model for Hutchinson-Gilford progeria syndrome. Proc Natl Acad Sci USA 102: 14416-14421.
32. Yang SH, Bergo MO, Toth JI, Qiao X, Hu Y, et al. (2005) Blocking protein farnesyltransferase improves nuclear blebbing in mouse fibroblasts with a targeted Hutchinson-Gilford progeria syndrome mutation. Proc Natl Acad Sci USA 102: 10291-10296.
33. Kudlow BA, Jameson SA, Kennedy BK (2005) HIV protease inhibitors block adipocyte differentiation independently of lamin A/C. AIDS 19: 1565-1573.
34. Petroski MD, Deshais RJ (2005) Function and regulation of cullin-RING ubiquitin ligases. Nat Rev Mol Cell Biol 6: 9-20.
35. Jin J, Cardozo T, Lovering RC, Elledge SJ, Pagano M, et al. (2004) Systematic analysis and nomenclature of mammalian F-box proteins. Genes Dev 18: 2573-2580.
36. Jia S, Kobayashi R, Grewal SI (2005) Ubiquitin ligase component Cul4 associates with Cir4 histone methyltransferase to assemble heterochromatin. Nat Cell Biol 7: 1007-1013.
37. Dechat T, Korbei B, Vaughan OA, Vlcek S, Hutchison CJ, et al. (2000) Lamina-associated polypeptide 2a binds intranuclear A-type lamins. J Cell Sci 113: 3473-3484.
38. Markiewicz E, Dechat T, Foisner R, Quinlan RA, Hutchison CJ (2002) Lamin A/C binding protein LAP2a is required for nuclear anchorage of retinoblastoma protein. Mol Biol Cell 13: 4401-4413.
39. Nikolova V, Leimena C, McMahon AC, Tan JC, Chandar S, et al. (2004) Defects in nuclear structure and function promote dilated cardiomyopathy in lamin A/C-deficient mice. J Clin Invest 113: 357-69.
40. Liu J, Ben-Shahar TR, Riemer D, Treinin M, Spann P, et al. (2000) Essential roles for Caenorhabditis elegans lamin gene in nuclear organization, cell cycle progression, and spatial organization of nuclear pore complexes. Mol Biol Cell 11: 3937-3947.
41. Pickersgill H, Kalverda B, de Wit E, Talhout W, Fornerod M, et al. (2006) Characterization of the Drosophila melanogaster genome at the nuclear lamina. Nat Genet 38: 1005-1014.
42. Guelen L, Pagie L, Brasset E, Meuleman W, Faza MB, et al. (2008) Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 453: 948-951.
43. Misteli T (2007) Beyond the sequence: cellular organization of genome function. Cell 128: 787-800.
44. Lattanzi G, Columbaro M, Mattioli E, Cenni V, Camozzi D, et al. (2007) Prelamin A processing is linked to heterochromatin organization. J Cell Biochem 102: 1149-1159.
45. Mattioli E, Columbaro M, Capanni C, Santi S, Maraldi NM, et al. (2008) Drugs affecting prelamin A processing: Effects on heterochromatin organization. Exp Cell Res 314: 453-462.
46. Taimen P, Pfleghaar K, Shimi T, Moller D, Ben-Harush K, et al. (2009) A progeria mutation reveals functions for lamin A in nuclear assembly, architecture, and chromosome organization. Proc Natl Acad Sci USA 106: 20788-20793.
47. Broers JL, Machiels BM, van Eys GJ, Kuijpers HJ, Manders EM, et al. (1999) Dynamics of the nuclear lamina as monitored by GFP-tagged A-type lamins. J Cell Sci 112: 3463-3475.
48. Moir RD, Yoon M, Khuon S, Goldman RD (2000) Nuclear lamins A and B1: Different pathways of assembly during nuclear envelope formation in living cells. J Cell Biol 151: 1155-1168.
49. Gilchrist S, Gilbert N, Perry P, Östlund C, Worman HJ, et al. (2004) Altered protein dynamics of disease-associated lamin A mutants. BMC Cell Biol 5: 46.
50. Tripathi K, Muralikrishna Bh, Parnaik VK (2009) Differential dynamics and stability of lamin A rod domain mutants. Int J Integrative Biol 5: 1-8.
51. Sullivan T, Escalante-Alcade D, Bhatt H, Anver M, Bhat N, et al. (1999) Loss of A-type lamin expression compromises nuclear envelope integrity leading to muscular dystrophy. J Cell Biol 147: 913-920.
52. Vaughan A, Alvarez-Reyes M, Bridger JM, Broers JL, Ramaekers FC, et al. (2001) Both emerin and lamin C depend on lamin A for localization at the nuclear envelope. J Cell Sci 114: 2577-2590.
53. Ritou E, Bai M, Georgatos SD (2007) Variant-specific patterns and humoral regulation of HP1 proteins in human cells and tissues. J Cell Sci 120: 3425-3435.
54. Dialynas GK, Terjung S, Brown JP, Aucott RL, Baron-Luhr B, et al. (2007) Plasticity of HP1 proteins in mammalian cells. J Cell Sci 120: 3415-3424.
55. Mateos-Langerak J, Brink MC, Luijsterburg MS, van der Kraan I, van Driel R, et al. (2007) Pericentromeric heterochromatin domains are maintained without accumulation of HP1. Mol Biol Cell 18: 1464-1471.
56. Aucott R, Bullwinkle J, Yu Y, Shi W, Billur M, et al. (2008) HP1b is required for development of the cerebral neocortex and neuromuscular junctions. J Cell Biol 183: 597-606.
57. Ayoub N, Jeyasekharan AD, Bernal JA, Venkitaraman AR (2008) HP1b mobilization promotes chromatin changes that initiate the DNA damage response. Nature 453: 682-686.
58. Muchir A, Massart C, van Engelen BG, Lammens M, Bonne G, et al. (2006) Proteasome-mediated degradation of integral inner nuclear membrane protein emerin in fibroblasts lacking A-type lamins. Biochem Biophys Res Commun 351: 1011-1017.
59. Johnson BR, Nitta RT, Frock R L, Mounkes L, Barbie DA, et al. (2004) A-type lamins regulate retinoblastoma protein function by promoting sub-nuclear localization and preventing proteasomal degradation. Proc Natl Acad Sci USA 101: 9677-9682.
60. Mariappan I, Parnaik VK (2005) Sequestration of pRb by cyclin D3 causes intranuclear reorganization of lamin A/C during muscle cell differentiation. Mol Biol Cell 16: 1948-1960.
61. De Conto F, Pilotti E, Razin SV, Ferraglia F, Gérand G, et al. (2000) In mouse myoblasts nuclear prosomes are associated with the nuclear matrix and accumulate preferentially in the perinucleolar areas. J Cell Sci 113: 2399-2407.
62. Nickerson JA, Krockmalnic G, Wan KW, Turner CD, Penman S (1992) A normally masked nuclear antigen that appears at mitosis on cytoskeleton filaments adjoining chromosomes, centrioles and midbodies. J Cell Biol 116: 977-987.