A novel feed-forward loop between ARIH2 E3-ligase and PABPN1 regulates aging-associated muscle degeneration

American Journal of Pathology

Volumn 184, Issue 4, 2014, Pages 1119-1131

  Raz, Vered ^a   Buijze, Hellen ^a   Raz, Yotam ^a   Verwey, Nisha ^a   Anvar, Seyed Yahya ^a   Aartsma Rus, Annemieke ^a   Van Der Maarel, Silvère M ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; ARIH2 E3 LIGASE; LIGASE; MESSENGER RNA; NUCLEAR PROTEIN; POLY(A) BINDING PROTEIN NUCLEAR 1; UNCLASSIFIED DRUG; ARIH2 PROTEIN, HUMAN; PABPN1 PROTEIN, HUMAN; POLYADENYLIC ACID BINDING PROTEIN; UBIQUITIN PROTEIN LIGASE;

3' UNTRANSLATED REGION; AGING; ANIMAL CELL; ARTICLE; CELL CULTURE; CELL NUCLEUS INCLUSION BODY; CONTROLLED STUDY; DOWN REGULATION; FEMALE; HUMAN; HUMAN CELL; IN VIVO STUDY; MASKING; MOLECULAR PATHOLOGY; MOUSE; MUSCLE ATROPHY; MUSCLE DEVELOPMENT; MYOBLAST; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYADENYLATION; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN PROTEIN INTERACTION; VASTUS LATERALIS MUSCLE; ANIMAL; CELL LINE; DNA MICROARRAY; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; METABOLISM; OCULOPHARYNGEAL MUSCULAR DYSTROPHY; PATHOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKELETAL MUSCLE; WESTERN BLOTTING;

AGING; ANIMALS; BLOTTING, WESTERN; CELL LINE; GENE EXPRESSION REGULATION; HUMANS; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, OCULOPHARYNGEAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLY(A)-BINDING PROTEIN I; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSFECTION; UBIQUITIN-PROTEIN LIGASES;

EID: 84897840951     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2013.12.011     Document Type: Article

References (48)

1. S.H. Lecker, A.L. Goldberg, and W.E. Mitch Protein degradation by the ubiquitin-proteasome pathway in normal and disease states J Am Soc Nephrol 17 2006 1807 1819
2. M. Sandri Signaling in muscle atrophy and hypertrophy Physiology (Bethesda) 23 2008 160 170
3. A.B. Lindner, and A. Demarez Protein aggregation as a paradigm of aging Biochim Biophys Acta 1790 2009 980 996
4. D.C. David, N. Ollikainen, J.C. Trinidad, M.P. Cary, A.L. Burlingame, and C. Kenyon Widespread protein aggregation as an inherent part of aging in C. elegans PLoS Biol 8 2010 e1000450
5. B. Bingol, and M. Sheng Deconstruction for reconstruction: the role of proteolysis in neural plasticity and disease Neuron 69 2011 22 32
6. B. Brais Oculopharyngeal muscular dystrophy: a polyalanine myopathy Curr Neurol Neurosci Rep 9 2009 76 82
7. B. Brais, J.P. Bouchard, Y.G. Xie, D.L. Rochefort, N. Chretien, F.M. Tome, R.G. Lafreniere, J.M. Rommens, E. Uyama, O. Nohira, S. Blumen, A.D. Korczyn, P. Heutink, J. Mathieu, A. Duranceau, F. Codere, M. Fardeau, and G.A. Rouleau Short GCG expansions in the PABP2 gene cause oculopharyngeal muscular dystrophy Nat Genet 18 1998 164 167
8. F.M. Tome, and M. Fardeau Nuclear inclusions in oculopharyngeal dystrophy Acta Neuropathol 49 1980 85 87
9. V. Raz, G. Butler-Browne, B. van Engelen, and B. Brais 191st ENMC International Workshop: recent advances in oculopharyngeal muscular dystrophy research: from bench to bedside 8-10 June 2012, Naarden, The Netherlands Neuromuscul Disord 23 2013 516 523
10. M.T. Berciano, N.T. Villagra, J.L. Ojeda, J. Navascues, A. Gomes, M. Lafarga, and M. Carmo-Fonseca Oculopharyngeal muscular dystrophy-like nuclear inclusions are present in normal magnocellular neurosecretory neurons of the hypothalamus Hum Mol Genet 13 2004 829 838
11. S.Y. Anvar, Y. Raz, N. Verway, B. van der Sluijs, A. Venema, J.J. Goeman, J. Vissing, S.M. van der Maarel, P.A. t Hoen, B.G. van Engelen, and V. Raz A decline in PABPN1 induces progressive muscle weakness in oculopharyngeal muscle dystrophy and in muscle aging Aging (Albany NY) 5 2013 412 426
12. M. Simonelig PABPN1 shuts down alternative poly(A) sites Cell Res 22 2012 1419 1421
13. B. Benoit, G. Mitou, A. Chartier, C. Temme, S. Zaessinger, E. Wahle, I. Busseau, and M. Simonelig An essential cytoplasmic function for the nuclear poly(A) binding protein, PABP2, in poly(A) tail length control and early development in Drosophila Dev Cell 9 2005 511 522
14. M. Jenal, R. Elkon, F. Loayza-Puch, G. van Haaften, U. Kühn, F.M. Menzies, J.A.F.O. Vrielink, A.J. Bos, J. Drost, K. Rooijers, D.C. Rubinsztein, and R. Agami The poly(A)-binding protein nuclear 1 suppresses alternative cleavage and polyadenylation sites Cell 149 2012 538 553
15. E. de Klerk, A. Venema, S.Y. Anvar, J.J. Goeman, O. Hu, J.T. den Dunnen, S.M. van der Maarel, V. Raz, and P.A.C. Äòt Hoen Poly(A) binding protein nuclear 1 levels affect alternative polyadenylation Nucleic Acids Res 40 2012 9089 9101
16. Y.B. Beaulieu, C.L. Kleinman, A.M. Landry-Voyer, J. Majewski, and F. Bachand Polyadenylation-dependent control of long noncoding RNA expression by the poly(A)-binding protein nuclear 1 PLoS Genet 8 2012 15
17. V. Raz, S. Routledge, A. Venema, H. Buijze, E. van der Wal, S. Anvar, K.R. Straasheijm, R. Klooster, M. Antoniou, and S.M. van der Maarel Modeling oculopharyngeal muscular dystrophy in myotube cultures reveals reduced accumulation of soluble mutant PABPN1 protein Am J Pathol 179 2011 1988 2000
18. S.Y. Anvar, P.A. t Hoen, A. Venema, B. van der Sluijs, B. van Engelen, M. Snoeck, J. Vissing, C. Trollet, G. Dickson, A. Chartier, M. Simonelig, G.J. van Ommen, S.M. van der Maarel, and V. Raz Deregulation of the ubiquitin-proteasome system is the predominant molecular pathology in OPMD animal models and patients Skelet Muscle 1 2011 15
19. V. Raz, E. Sterrenburg, S. Routledge, A. Venema, B.M. van der Sluijs, C. Trollet, G. Dickson, B.G. van Engelen, S.M. van der Maarel, and M.N. Antoniou Nuclear entrapment and extracellular depletion of PCOLCE is associated with muscle degeneration in oculopharyngeal muscular dystrophy BMC Neurol 13 2013 1471 2377
20. C. Trollet, S.Y. Anvar, A. Venema, I.P. Hargreaves, K. Foster, A. Vignaud, A. Ferry, E. Negroni, C. Hourde, M.A. Baraibar, P.A. t Hoen, J.E. Davies, D.C. Rubinsztein, S.J. Heales, V. Mouly, S.M. van der Maarel, G. Butler-Browne, V. Raz, and G. Dickson Molecular and phenotypic characterization of a mouse model of oculopharyngeal muscular dystrophy reveals severe muscular atrophy restricted to fast glycolytic fibres Hum Mol Genet 19 2010 2191 2207
21. C.H. Zhu, V. Mouly, R.N. Cooper, K. Mamchaoui, A. Bigot, J.W. Shay, J.P. Di Santo, G.S. Butler-Browne, and W.E. Wright Cellular senescence in human myoblasts is overcome by human telomerase reverse transcriptase and cyclin-dependent kinase 4: consequences in aging muscle and therapeutic strategies for muscular dystrophies Aging Cell 6 2007 515 523
22. V. Raz, T. Abraham, E.W. van Zwet, R.W. Dirks, H.J. Tanke, and S.M. van der Maarel Reversible aggregation of PABPN1 pre-inclusion structures Nucleus 2 2011 208 218
23. V. Raz, F. Carlotti, B.J. Vermolen, E. van der Poel, W.C. Sloos, S. Knaan-Shanzer, A.A. de Vries, R.C. Hoeben, I.T. Young, H.J. Tanke, Y. Garini, and R.W. Dirks Changes in lamina structure are followed by spatial reorganization of heterochromatic regions in caspase-8-activated human mesenchymal stem cells J Cell Sci 119 2006 4247 4256
24. A. Aartsma-Rus, L. van Vliet, M. Hirschi, A.A. Janson, H. Heemskerk, C.L. de Winter, S. de Kimpe, J.C. van Deutekom, P.A. t Hoen, and G.J. van Ommen Guidelines for antisense oligonucleotide design and insight into splice-modulating mechanisms Mol Ther 17 2009 548 553
25. A. Aartsma-Rus Overview on DMD exon skipping Methods Mol Biol 867 2012 97 116
26. A. Aartsma-Rus, W.E. Kaman, M. Bremmer-Bout, A.A. Janson, J.T. den Dunnen, G.J. van Ommen, and J.C. van Deutekom Comparative analysis of antisense oligonucleotide analogs for targeted DMD exon 46 skipping in muscle cells Gene Ther 11 2004 1391 1398
27. T. Lu, Y. Pan, S.Y. Kao, C. Li, I. Kohane, J. Chan, and B.A. Yankner Gene regulation and DNA damage in the ageing human brain Nature 429 2004 883 891
28. J.M. Zahn, R. Sonu, H. Vogel, E. Crane, K. Mazan-Mamczarz, R. Rabkin, R.W. Davis, K.G. Becker, A.B. Owen, and S.K. Kim Transcriptional profiling of aging in human muscle reveals a common aging signature PLoS Genet 2 2006 e115
29. W.M. Passtoors, J.M. Boer, J.J. Goeman, E.B. Akker, J. Deelen, B.J. Zwaan, A. Scarborough, R. Breggen, R.H. Vossen, J.J. Houwing-Duistermaat, G.J. Ommen, R.G. Westendorp, D. Heemst, A.J. Craen, A.J. White, D.A. Gunn, M. Beekman, and P.E. Slagboom Transcriptional profiling of human familial longevity indicates a role for ASF1A and IL7R PLoS One 7 2012 e27759
30. G.E. Rodwell, R. Sonu, J.M. Zahn, J. Lund, J. Wilhelmy, L. Wang, W. Xiao, M. Mindrinos, E. Crane, E. Segal, B.D. Myers, J.D. Brooks, R.W. Davis, J. Higgins, A.B. Owen, and S.K. Kim A transcriptional profile of aging in the human kidney PLoS Biol 2 2004 e427
31. P. Verheesen, A. de Kluijver, S. van Koningsbruggen, M. de Brij, H.J. de Haard, G.J.B. van Ommen, S.M. van der Maarel, and C.T. Verrips Prevention of oculopharyngeal muscular dystrophy-associated aggregation of nuclear poly(A)-binding protein with a single-domain intracellular antibody Hum Mol Genet 15 2006 105 111
32. B. Marzani, G. Felzani, R.G. Bellomo, J. Vecchiet, and F. Marzatico Human muscle aging: ROS-mediated alterations in rectus abdominis and vastus lateralis muscles Exp Gerontol 40 2005 959 965
33. A. Abu-Baker, C. Messaed, J. Laganiere, C. Gaspar, B. Brais, and G.A. Rouleau Involvement of the ubiquitin-proteasome pathway and molecular chaperones in oculopharyngeal muscular dystrophy Hum Mol Genet 12 2003 2609 2623
34. S. Périé, K. Mamchaoui, V. Mouly, S. Blot, B. Bouazza, L.E. Thornell, J.L. St Guily, and G. Butler-Browne Premature proliferative arrest of cricopharyngeal myoblasts in oculo-pharyngeal muscular dystrophy: therapeutic perspectives of autologous myoblast transplantation Neuromuscul Disord 16 2006 770 781
35. M. Zhan, H. Yamaza, Y. Sun, J. Sinclair, H. Li, and S. Zou Temporal and spatial transcriptional profiles of aging in Drosophila melanogaster Genome Res 17 2007 1236 1243
36. R. Mazzulli Joseph, Y.H. Xu, Y. Sun, L. Knight Adam, J. McLean Pamela, A. Caldwell Guy, E. Sidransky, A. Grabowski Gregory, and D. Krainc Gaucher disease glucocerebrosidase and α-synuclein form a bidirectional pathogenic loop in synucleinopathies Cell 146 2011 37 52
37. J.L. George, S. Mok, D. Moses, S. Wilkins, A.I. Bush, R.A. Cherny, and D.I. Finkelstein Targeting the progression of Parkinson's disease Curr Neuropharmacol 7 2009 9 36
38. A. Calado, F.M. Tome, B. Brais, G.A. Rouleau, U. Kuhn, E. Wahle, and M. Carmo-Fonseca Nuclear inclusions in oculopharyngeal muscular dystrophy consist of poly(A) binding protein 2 aggregates which sequester poly(A) RNA Hum Mol Genet 9 2000 2321 2328
39. A. Ciechanover, and P. Brundin The ubiquitin proteasome system in neurodegenerative diseases: sometimes the chicken, sometimes the egg Neuron 40 2003 427 446
40. E.J. Bennett, N.F. Bence, R. Jayakumar, and R.R. Kopito Global impairment of the ubiquitin-proteasome system by nuclear or cytoplasmic protein aggregates precedes inclusion body formation Mol Cell 17 2005 351 365
41. N.F. Bence, R.M. Sampat, and R.R. Kopito Impairment of the ubiquitin-proteasome system by protein aggregation Science 292 2001 1552 1555
42. D.A. Ferrington, A.D. Husom, and L.V. Thompson Altered proteasome structure, function, and oxidation in aged muscle FASEB J 19 2005 644 646
43. M. Sandri, C. Sandri, A. Gilbert, C. Skurk, E. Calabria, A. Picard, K. Walsh, S. Schiaffino, S.H. Lecker, and A.L. Goldberg Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy Cell 117 2004 399 412
44. E. Edstrom, M. Altun, M. Hagglund, and B. Ulfhake Atrogin-1/MAFbx and MuRF1 are downregulated in aging-related loss of skeletal muscle J Gerontol A Biol Sci Med Sci 61 2006 663 674
45. B. Eisenhaber, N. Chumak, F. Eisenhaber, and M.-T. Hauser The ring between ring fingers (RBR) protein family Genome Biol 8 2007 209
46. C.F. Bennett, and E.E. Swayze RNA targeting therapeutics: molecular mechanisms of antisense oligonucleotides as a therapeutic platform Annu Rev Pharmacol Toxicol 50 2010 259 293
47. N.M. Goemans, M. Tulinius, J.T. van den Akker, B.E. Burm, P.F. Ekhart, N. Heuvelmans, T. Holling, A.A. Janson, G.J. Platenburg, J.A. Sipkens, J.M.A. Sitsen, A. Aartsma-Rus, G.-J.B. van Ommen, G. Buyse, N. Darin, J.J. Verschuuren, G.V. Campion, S.J. de Kimpe, and J.C. van Deutekom Systemic administration of PRO051 in Duchenne's muscular dystrophy N Engl J Med 364 2011 1513 1522
48. T.A. Vickers, J.R. Wyatt, T. Burckin, C.F. Bennett, and S.M. Freier Fully modified 2′ MOE oligonucleotides redirect polyadenylation Nucleic Acids Res 29 2001 1293 1299