Subcellular localization of Matrin 3 containing mutations associated with ALS and distal myopathy

PLoS ONE

Volumn 10, Issue 11, 2015, Pages

  Gallego Iradi, M Carolina ^a,b   Clare, Alexis M ^a   Brown, Hilda H ^a,b   Janus, Christopher ^a   Lewis, Jada ^a   Borchelt, David R ^a,b  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARSENITE SODIUM; MATRILYSIN; MATRIN 3; UNCLASSIFIED DRUG; MATR3 PROTEIN, HUMAN; NUCLEAR MATRIX PROTEIN; RNA BINDING PROTEIN;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ARTICLE; CELL INCLUSION; CELL NUCLEUS; CELL STRESS; CELLULAR DISTRIBUTION; CHO CELL LINE; CONTROLLED STUDY; CYTOPLASM; DISTAL MYOPATHY; FEMALE; FLUORESCENCE ANALYSIS; GENE FUNCTION; GENE OVEREXPRESSION; GENETIC ASSOCIATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOREACTIVITY; MATR3 GENE; MOLECULAR DYNAMICS; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; PROTEIN EXPRESSION; WILD TYPE; ANIMAL; CRICETULUS; GENETICS; METABOLISM; MUTATION; PROTEIN TRANSPORT;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; CHO CELLS; CRICETULUS; CYTOPLASM; DISTAL MYOPATHIES; HUMANS; INCLUSION BODIES; MUTATION; NUCLEAR MATRIX-ASSOCIATED PROTEINS; PROTEIN TRANSPORT; RNA-BINDING PROTEINS;

EID: 84951011589     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0142144     Document Type: Article

References (37)

1. Ravits JM, La Spada AR. ALS motor phenotype heterogeneity, focality, and spread: deconstructing motor neuron degeneration. Neurology. 2009; 73: 805-811. doi: 10.1212/WNL.0b013e3181b6bbbd PMID: 19738176
2. Lomen-Hoerth C, Murphy J, Langmore S, Kramer JH, Olney RK, Miller B. Are amyotrophic lateral sclerosis patients cognitively normal? Neurology. 2003; 60: 1094-1097. PMID: 12682312
3. Johnson JO, Pioro EP, Boehringer A, Chia R, Feit H, Renton AE, et al. Mutations in the Matrin 3 gene cause familial amyotrophic lateral sclerosis. Nat Neurosci. 2014; 17: 664-666. doi: 10.1038/nn.3688 PMID: 24686783
4. Muller TJ, Kraya T, Stoltenburg-Didinger G, Hanisch F, Kornhuber M, Stoevesandt D, et al. Phenotype of matrin-3-related distal myopathy in 16 German patients. Ann Neurol. 2014; 76: 669-680. doi: 10.1002/ana.24255 PMID: 25154462
5. Senderek J, Garvey SM, Krieger M, Guergueltcheva V, Urtizberea A, Roos A, et al. Autosomal-dominant distal myopathy associated with a recurrent missense mutation in the gene encoding the nuclear matrix protein, matrin 3. Am J Hum Genet. 2009; 84: 511-518. doi: 10.1016/j.ajhg.2009.03.006 PMID: 19344878
6. Feit H, Silbergleit A, Schneider LB, Gutierrez JA, Fitoussi RP, Reyes C, et al. Vocal cord and pharyngeal weakness with autosomal dominant distal myopathy: clinical description and gene localization to 5q31. Am J Hum Genet. 1998; 63: 1732-1742. S0002-9297(07)61618-8 [pii]. PMID: 9837826
7. Millecamps S, De Septenville A, Teyssou E, Daniau M, Camuzat A, Albert M, et al. Genetic analysis of matrin 3 gene in French amyotrophic lateral sclerosis patients and frontotemporal lobar degeneration with amyotrophic lateral sclerosis patients. Neurobiol Aging. 2014; 35: 2882.e13-2882.e15. doi: 10.1016/j.neurobiolaging.2014.07.016
8. Belgrader P, Dey R, Berezney R. Molecular cloning of matrin 3. A 125-kilodalton protein of the nuclear matrix contains an extensive acidic domain. J Biol Chem. 1991; 266: 9893-9899. PMID: 2033075
9. Neumann M, Sampathu DM, Kwong LK, Truax AC, Micsenyi MC, Chou TT, et al. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science. 2006; 314: 130-133. PMID: 17023659
10. Da Cruz S, Cleveland DW. Understanding the role of TDP-43 and FUS/TLS in ALS and beyond. Curr Opin Neurobiol. 2011; 21: 904-919. doi: 10.1016/j.conb.2011.05.029 PMID: 21813273
11. Arimoto K, Fukuda H, Imajoh-Ohmi S, Saito H, Takekawa M. Formation of stress granules inhibits apoptosis by suppressing stress-responsive MAPK pathways. Nat Cell Biol. 2008; 10: 1324-1332. doi: 10.1038/ncb1791 PMID: 18836437
12. Buchan JR, Parker R. Eukaryotic stress granules: the ins and outs of translation. Mol Cell. 2009; 36: 932-941. doi: 10.1016/j.molcel.2009.11.020 PMID: 20064460
13. Parker SJ, Meyerowitz J, James JL, Liddell JR, Crouch PJ, Kanninen KM, et al. Endogenous TDP-43 localized to stress granules can subsequently form protein aggregates. Neurochem Int. 2012; 60: 415-424. doi: 10.1016/j.neuint.2012.01.019 PMID: 22306778
14. Colombrita C, Zennaro E, Fallini C, Weber M, Sommacal A, Buratti E, et al. TDP-43 is recruited to stress granules in conditions of oxidative insult. J Neurochem. 2009; 111: 1051-1061. doi: 10.1111/j.1471-4159.2009.06383.x PMID: 19765185
15. Irvine K, Stirling R, Hume D, Kennedy D. Rasputin, more promiscuous than ever: a review of G3BP. Int J Dev Biol. 2004; 48: 1065-1077. 041893ki [pii]. PMID: 15602692
16. Figley MD, Bieri G, Kolaitis RM, Taylor JP, Gitler AD. Profilin 1 associates with stress granules and ALS-linked mutations alter stress granule dynamics. J Neurosci. 2014; 34: 8083-8097. doi: 10.1523/JNEUROSCI.0543-14.2014 PMID: 24920614
17. Aulas A, Caron G, Gkogkas CG, Mohamed NV, Destroismaisons L, Sonenberg N, et al. G3BP1 promotes stress-induced RNA granule interactions to preserve polyadenylated mRNA. J Cell Biol. 2015; 209: 73-84. doi: 10.1083/jcb.201408092 PMID: 25847539
18. Reineke LC, Kedersha N, Langereis MA, van Kuppeveld FJ, Lloyd RE. Stress granules regulate double-stranded RNA-dependent protein kinase activation through a complex containing G3BP1 and Caprin1. MBio. 2015; 6: e02486-14. doi: 10.1128/mBio.02486-14 PMID: 25784705
19. Mizushima S, Nagata S. pEF-BOS, a powerful mammalian expression vector. Nucleic Acids Res. 1990; 18: 5322. PMID: 1698283
20. Borchelt DR, Lee MK, Slunt HS, Guarnieri M, Xu ZS, Wong PC, et al. Superoxide dismutase 1 with mutations linked to familial amyotrophic lateral sclerosis possesses significant activity. Proc Natl Acad Sci U S A. 1994; 91: 8292-8296. PMID: 8058797
21. Gilks N, Kedersha N, Ayodele M, Shen L, Stoecklin G, Dember LM, et al. Stress granule assembly is mediated by prion-like aggregation of TIA-1. Mol Biol Cell. 2004; 15: 5383-5398. doi: 10.1091/mbc.E04-08-0715 PMID: 15371533
22. Kim SH, Dong WK, Weiler IJ, Greenough WT. Fragile X mental retardation protein shifts between polyribosomes and stress granules after neuronal injury by arsenite stress or in vivo hippocampal electrode insertion. J Neurosci. 2006; 26: 2413-2418. 26/9/2413 [pii]. PMID: 16510718
23. Tanaka T, Ohashi S, Kobayashi S. Roles of YB-1 under arsenite-induced stress: translational activation of HSP70 mRNA and control of the number of stress granules. Biochim Biophys Acta. 2014; 1840: 985-992. doi: 10.1016/j.bbagen.2013.11.002 PMID: 24231679
24. Erazo A, Yee MB, Banfield BW, Kinchington PR. The alphaherpesvirus US3/ORF66 protein kinases direct phosphorylation of the nuclear matrix protein matrin 3. J Virol. 2011; 85: 568-581. doi: 10.1128/JVI.01611-10 PMID: 20962082
25. Matsuki H, Takahashi M, Higuchi M, Makokha GN, Oie M, Fujii M. Both G3BP1 and G3BP2 contribute to stress granule formation. Genes Cells. 2013; 18: 135-146. doi: 10.1111/gtc.12023 PMID: 23279204
26. Long RM, McNally MT. mRNA decay: x (XRN1) marks the spot. Mol Cell. 2003; 11: 1126-1128. S1097276503001989 [pii]. PMID: 12769838
27. Liu J, Rivas FV, Wohlschlegel J, Yates JR III, Parker R, Hannon GJ. A role for the P-body component GW182 in microRNA function. Nat Cell Biol. 2005; 7: 1261-1266. ncb1333 [pii]. PMID: 16284623
28. Martelli AM, Riccio M, Bareggi R, Manfioletti G, Tabellini G, Baldini G, et al. Intranuclear distribution of HMGI/Y proteins. An immunocytochemical study. J Histochem Cytochem. 1998; 46: 863-864. PMID: 9632746
29. Zhang Z, Carmichael GG. The fate of dsRNA in the nucleus: a p54(nrb)-containing complex mediates the nuclear retention of promiscuously A-to-I edited RNAs. Cell. 2001; 106: 465-475. S0092-8674(01)00466-4 [pii]. PMID: 11525732
30. Coelho MB, Attig J, Bellora N, Konig J, Hallegger M, Kayikci M, et al. Nuclear matrix protein Matrin3 regulates alternative splicing and forms overlapping regulatory networks with PTB. EMBO J. 2015; 34: 653-668. doi: 10.15252/embj.201489852 PMID: 25599992
31. Cronshaw JM, Krutchinsky AN, Zhang W, Chait BT, Matunis MJ. Proteomic analysis of the mammalian nuclear pore complex. J Cell Biol. 2002; 158: 915-927. doi: 10.1083/jcb.200206106 PMID: 12196509
32. Yedavalli VS, Jeang KT. Matrin 3 is a co-factor for HIV-1 Rev in regulating post-transcriptional viral gene expression. Retrovirology. 2011; 8: 61-4690-8-61. doi: 10.1186/1742-4690-8-61 PMID: 21771347
33. Salton M, Lerenthal Y, Wang SY, Chen DJ, Shiloh Y. Involvement of Matrin 3 and SFPQ/NONO in the DNA damage response. Cell Cycle. 2010; 9: 1568-1576. 11298 [pii]. PMID: 20421735
34. Giordano G, Sanchez-Perez AM, Montoliu C, Berezney R, Malyavantham K, Costa LG, et al. Activation of NMDA receptors induces protein kinase A-mediated phosphorylation and degradation of matrin 3. Blocking these effects prevents NMDA-induced neuronal death. J Neurochem. 2005; 94: 808-818. JNC3235 [pii]. PMID: 16000164
35. Depreux FF, Puckelwartz MJ, Augustynowicz A, Wolfgeher D, Labno CM, Pierre-Louis D, et al. Disruption of the lamin A and matrin-3 interaction by myopathic LMNA mutations. Hum Mol Genet. 2015; 24: 4284-4295. doi: 10.1093/hmg/ddv160 PMID: 25948554
36. Bertrand AT, Chikhaoui K, Yaou RB, Bonne G. Clinical and genetic heterogeneity in laminopathies. Biochem Soc Trans. 2011; 39: 1687-1692. doi: 10.1042/BST20110670 PMID: 22103508
37. Palmio J, Evila A, Bashir A, Norwood F, Viitaniemi K, Vihola A, et al. Re-evaluation of the phenotype caused by the common MATR3 p.Ser85Cys mutation in a new family. J Neurol Neurosurg Psychiatry. 2015. jnnp-2014-309349 [pii].