Mutations in SQSTM1 encoding p62 in amyotrophic lateral sclerosis: genetics and neuropathology (original) (raw)

References

  1. Al-Sarraj S, King A, Troakes C, Smith B, Maekawa S, Bodi I, Rogelj B, Al-Chalabi A, Hortobagyi T, Shaw CE (2011) p62 positive, TDP-43 negative, neuronal cytoplasmic and intranuclear inclusions in the cerebellum and hippocampus define the pathology of C9orf72-linked FTLD and MND/ALS. Acta Neuropathol 122:691–702
    Article PubMed CAS Google Scholar
  2. Albagha OM, Visconti MR, Alonso N, Langston AL, Cundy T, Dargie R, Dunlop MG, Fraser WD, Hooper MJ, Isaia G, Nicholson GC, del Pino Montes J, Gonzalez-Sarmiento R, di Stefano M, Tenesa A, Walsh JP, Ralston SH (2010) Genome-wide association study identifies variants at CSF1, OPTN and TNFRSF11A as genetic risk factors for Paget’s disease of bone. Nat Genet 42:520–524
    Google Scholar
  3. Brady OA, Meng P, Zheng Y, Mao Y, Hu F (2011) Regulation of TDP-43 aggregation by phosphorylation and p62/SQSTM1. J Neurochem 116:248–259
    Article PubMed CAS Google Scholar
  4. Brettschneider J, Libon DJ, Toledo JB, Xie SX, McCluskey L, Elman L, Geser F, Lee VM, Grossman M, Trojanowski JQ (2012) Microglial activation and TDP-43 pathology correlate with executive dysfunction in amyotrophic lateral sclerosis. Acta Neuropathol 123:395–407
    Article PubMed CAS Google Scholar
  5. Brettschneider J, Van Deerlin VM, Robinson JL, Kwong L, Lee EB, Ali YO, Safren N, Monteiro MJ, Toledo JB, Elman L, McCluskey L, Irwin DJ, Grossman M, Molina-Porcel L, Lee VM, Trojanowski JQ (2012) Pattern of ubiquilin pathology in ALS and FTLD indicates presence of C9ORF72 hexanucleotide expansion. Acta Neuropathol 123:825–839
    Article PubMed Google Scholar
  6. Brooks BR, Miller RG, Swash M, Munsat TL (2000) El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord 1:293–299
    Article PubMed CAS Google Scholar
  7. Cavey JR, Ralston SH, Sheppard PW, Ciani B, Gallagher TR, Long JE, Searle MS, Layfield R (2006) Loss of ubiquitin binding is a unifying mechanism by which mutations of SQSTM1 cause Paget’s disease of bone. Calcif Tissue Int 78:271–277
    Article PubMed CAS Google Scholar
  8. Collet C, Michou L, Audran M, Chasseigneaux S, Hilliquin P, Bardin T, Lemaire I, Cornelis F, Launay JM, Orcel P, Laplanche JL (2007) Paget’s disease of bone in the French population: novel SQSTM1 mutations, functional analysis, and genotype-phenotype correlations. J Bone Miner Res 22:310–317
    Article PubMed CAS Google Scholar
  9. Cooper C, Schafheutle K, Dennison E, Kellingray S, Guyer P, Barker D (1999) The epidemiology of Paget’s disease in Britain: is the prevalence decreasing? J Bone Miner Res 14:192–197
    Article PubMed CAS Google Scholar
  10. Dai RM, Li CC (2001) Valosin-containing protein is a multi-ubiquitin chain-targeting factor required in ubiquitin-proteasome degradation. Nat Cell Biol 3:740–744
    Article PubMed CAS Google Scholar
  11. Daroszewska A, van ‘t Hof RJ, Rojas JA, Layfield R, Landao-Basonga E, Rose L, Rose K, Ralston SH (2011) A point mutation in the ubiquitin-associated domain of SQSMT1 is sufficient to cause a Paget’s disease-like disorder in mice. Hum Mol Genet 20:2734–2744
    Google Scholar
  12. Dejesus-Hernandez M, Mackenzie IR, Boeve BF, Boxer AL, Baker M, Rutherford NJ, Nicholson AM, Finch NA, Flynn H, Adamson J, Kouri N, Wojtas A, Sengdy P, Hsiung GY, Karydas A, Seeley WW, Josephs KA, Coppola G, Geschwind DH, Wszolek ZK, Feldman H, Knopman DS, Petersen RC, Miller BL, Dickson DW, Boylan KB, Graff-Radford NR, Rademakers R (2011) Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS. Neuron 72:245–256
    Article PubMed CAS Google Scholar
  13. Falchetti A, Di Stefano M, Marini F, Ortolani S, Ulivieri MF, Bergui S, Masi L, Cepollaro C, Benucci M, Di Munno O, Rossini M, Adami S, Del Puente A, Isaia G, Torricelli F, Brandi ML (2009) Genetic epidemiology of Paget’s disease of bone in Italy: sequestosome1/p62 gene mutational test and haplotype analysis at 5q35 in a large representative series of sporadic and familial Italian cases of Paget’s disease of bone. Calcif Tissue Int 84:20–37
    Article PubMed CAS Google Scholar
  14. Fecto F, Yan J, Vemula SP, Liu E, Yang Y, Chen W, Zheng JG, Shi Y, Siddique N, Arrat H, Donkervoort S, Ajroud-Driss S, Sufit RL, Heller SL, Deng HX, Siddique T (2011) SQSTM1 mutations in familial and sporadic amyotrophic lateral sclerosis. Arch Neurol 68:1440–1446
    Article PubMed Google Scholar
  15. Geetha T, Vishwaprakash N, Sycheva M, Babu JR (2012) Sequestosome 1/p62: across diseases. Biomarkers 17:99–103
    Article PubMed CAS Google Scholar
  16. Geser F, Robinson JL, Malunda JA, Xie SX, Clark CM, Kwong LK, Moberg PJ, Moore EM, Van Deerlin VM, Lee VM, Arnold SE, Trojanowski JQ (2010) Pathological 43-kDa transactivation response DNA-binding protein in older adults with and without severe mental illness. Arch Neurol 67:1238–1250
    Article PubMed Google Scholar
  17. Geser F, Stein B, Partain M, Elman LB, McCluskey LF, Xie SX, Van Deerlin VM, Kwong LK, Lee VM, Trojanowski JQ (2011) Motor neuron disease clinically limited to the lower motor neuron is a diffuse TDP-43 proteinopathy. Acta Neuropathol 121:509–517
    Article PubMed Google Scholar
  18. Gleason CE, Ordureau A, Gourlay R, Arthur JS, Cohen P (2011) Polyubiquitin binding to optineurin is required for optimal activation of TANK-binding kinase 1 and production of interferon beta. J Biol Chem 286:35663–35674
    Article PubMed CAS Google Scholar
  19. Goode A, Layfield R (2010) Recent advances in understanding the molecular basis of Paget disease of bone. J Clin Pathol 63:199–203
    Article PubMed CAS Google Scholar
  20. Hamdy RC (1995) Clinical features and pharmacologic treatment of Paget’s disease. Endocrinol Metab Clin North Am 24:421–436
    PubMed CAS Google Scholar
  21. Hart MP, Brettschneider J, Lee VM, Trojanowski JQ, Gitler AD (2012) Distinct TDP-43 pathology in ALS patients with ataxin 2 intermediate-length polyQ expansions. Acta Neuropathol 124:221–230
    Article PubMed CAS Google Scholar
  22. Hernandez Lain A, Millecamps S, Dubourg O, Salachas F, Bruneteau G, Lacomblez L, LeGuern E, Seilhean D, Duyckaerts C, Meininger V, Mallet J, Pradat PF (2011) Abnormal TDP-43 and FUS proteins in muscles of sporadic IBM: similarities in a TARDBP-linked ALS patient. J Neurol Neurosurg Psychiatry 82:1414–1416
    Article PubMed Google Scholar
  23. Hirano M, Nakamura Y, Saigoh K, Sakamoto H, Ueno S, Isono C, Miyamoto K, Akamatsu M, Mitsui Y, Kusunoki S (2013) Mutations in the gene encoding p62 in Japanese patients with amyotrophic lateral sclerosis. Neurology 80:458–463
    Article PubMed CAS Google Scholar
  24. Hocking LJ, Lucas GJ, Daroszewska A, Mangion J, Olavesen M, Cundy T, Nicholson GC, Ward L, Bennett ST, Wuyts W, Van Hul W, Ralston SH (2002) Domain-specific mutations in sequestosome 1 (SQSTM1) cause familial and sporadic Paget’s disease. Hum Mol Genet 11:2735–2739
    Article PubMed CAS Google Scholar
  25. Johnson JO, Mandrioli J, Benatar M, Abramzon Y, Van Deerlin VM, Trojanowski JQ, Gibbs JR, Brunetti M, Gronka S, Wuu J, Ding J, McCluskey L, Martinez-Lage M, Falcone D, Hernandez DG, Arepalli S, Chong S, Schymick JC, Rothstein J, Landi F, Wang YD, Calvo A, Mora G, Sabatelli M, Monsurro MR, Battistini S, Salvi F, Spataro R, Sola P, Borghero G, Galassi G, Scholz SW, Taylor JP, Restagno G, Chio A, Traynor BJ (2010) Exome sequencing reveals VCP mutations as a cause of familial ALS. Neuron 68:857–864
    Article PubMed CAS Google Scholar
  26. Kuusisto E, Salminen A, Alafuzoff I (2001) Ubiquitin-binding protein p62 is present in neuronal and glial inclusions in human tauopathies and synucleinopathies. NeuroReport 12:2085–2090
    Article PubMed CAS Google Scholar
  27. Laurin N, Brown JP, Morissette J, Raymond V (2002) Recurrent mutation of the gene encoding sequestosome 1 (SQSTM1/p62) in Paget disease of bone. Am J Hum Genet 70:1582–1588
    Article PubMed CAS Google Scholar
  28. Mackenzie IR, Bigio EH, Ince PG, Geser F, Neumann M, Cairns NJ, Kwong LK, Forman MS, Ravits J, Stewart H, Eisen A, McClusky L, Kretzschmar HA, Monoranu CM, Highley JR, Kirby J, Siddique T, Shaw PJ, Lee VM, Trojanowski JQ (2007) Pathological TDP-43 distinguishes sporadic amyotrophic lateral sclerosis from amyotrophic lateral sclerosis with SOD1 mutations. Ann Neurol 61:427–434
    Article PubMed CAS Google Scholar
  29. Mackenzie IR, Neumann M, Baborie A, Sampathu DM, Du Plessis D, Jaros E, Perry RH, Trojanowski JQ, Mann DM, Lee VM (2011) A harmonized classification system for FTLD-TDP pathology. Acta Neuropathol 122:111–113
    Article PubMed Google Scholar
  30. Maruyama H, Morino H, Ito H, Izumi Y, Kato H, Watanabe Y, Kinoshita Y, Kamada M, Nodera H, Suzuki H, Komure O, Matsuura S, Kobatake K, Morimoto N, Abe K, Suzuki N, Aoki M, Kawata A, Hirai T, Kato T, Ogasawara K, Hirano A, Takumi T, Kusaka H, Hagiwara K, Kaji R, Kawakami H (2010) Mutations of optineurin in amyotrophic lateral sclerosis. Nature 465:223–226
    Article PubMed CAS Google Scholar
  31. Michou L, Collet C, Laplanche JL, Orcel P, Cornelis F (2006) Genetics of Paget’s disease of bone. Joint Bone Spine 73:243–248
    Article PubMed CAS Google Scholar
  32. Michou L, Collet C, Morissette J, Audran M, Thomas T, Gagnon E, Launay JM, Laplanche JL, Brown JP, Orcel P (2012) Epidemiogenetic study of French families with Paget’s disease of bone. Joint Bone Spine 79:393–398
    Article PubMed Google Scholar
  33. Millecamps S, Boillee S, Chabrol E, Camu W, Cazeneuve C, Salachas F, Pradat PF, Danel-Brunaud V, Vandenberghe N, Corcia P, Le Forestier N, Lacomblez L, Bruneteau G, Seilhean D, Brice A, Feingold J, Meininger V, LeGuern E (2011) Screening of OPTN in French familial amyotrophic lateral sclerosis. Neurobiol Aging 32:557 e511–e553
    Google Scholar
  34. Millecamps S, Boillee S, Le Ber I, Seilhean D, Teyssou E, Giraudeau M, Moigneu C, Vandenberghe N, Danel-Brunaud V, Corcia P, Pradat PF, Le Forestier N, Lacomblez L, Bruneteau G, Camu W, Brice A, Cazeneuve C, Leguern E, Meininger V, Salachas F (2012) Phenotype difference between ALS patients with expanded repeats in C9ORF72 and patients with mutations in other ALS-related genes. J Med Genet 49:258–263
    Article PubMed CAS Google Scholar
  35. Millecamps S, Corcia P, Cazeneuve C, Boillee S, Seilhean D, Danel-Brunaud V, Vandenberghe N, Pradat PF, Le Forestier N, Lacomblez L, Bruneteau G, Camu W, Brice A, Meininger V, LeGuern E, Salachas F (2012) Mutations in UBQLN2 are rare in French amyotrophic lateral sclerosis. Neurobiol Aging 33:839 e831–e833
    Google Scholar
  36. Millecamps S, Da Barroca S, Cazeneuve C, Salachas F, Pradat PF, Danel-Brunaud V, Vandenberghe N, Lacomblez L, Le Forestier N, Bruneteau G, Camu W, Brice A, Meininger V, LeGuern E (2010) Questioning on the role of D amino acid oxidase in familial amyotrophic lateral sclerosis. Proc Natl Acad Sci USA 107:E107 (author reply E108)
  37. Millecamps S, Salachas F, Cazeneuve C, Gordon P, Bricka B, Camuzat A, Guillot-Noel L, Russaouen O, Bruneteau G, Pradat PF, Le Forestier N, Vandenberghe N, Danel-Brunaud V, Guy N, Thauvin-Robinet C, Lacomblez L, Couratier P, Hannequin D, Seilhean D, Le Ber I, Corcia P, Camu W, Brice A, Rouleau G, Leguern E, Meininger V (2010) SOD1, ANG, VAPB, TARDBP, and FUS mutations in familial amyotrophic lateral sclerosis: genotype–phenotype correlations. J Med Genet 47:554–560
    Article PubMed CAS Google Scholar
  38. Mizuno Y, Amari M, Takatama M, Aizawa H, Mihara B, Okamoto K (2006) Immunoreactivities of p62, an ubiqutin-binding protein, in the spinal anterior horn cells of patients with amyotrophic lateral sclerosis. J Neurol Sci 249:13–18
    Article PubMed CAS Google Scholar
  39. Neumann M, Sampathu DM, Kwong LK, Truax AC, Micsenyi MC, Chou TT, Bruce J, Schuck T, Grossman M, Clark CM, McCluskey LF, Miller BL, Masliah E, Mackenzie IR, Feldman H, Feiden W, Kretzschmar HA, Trojanowski JQ, Lee VM (2006) Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 314:130–133
    Article PubMed CAS Google Scholar
  40. Okamoto K, Hirai S, Amari M, Watanabe M, Sakurai A (1993) Bunina bodies in amyotrophic lateral sclerosis immunostained with rabbit anti-cystatin C serum. Neurosci Lett 162:125–128
    Article PubMed CAS Google Scholar
  41. Pikkarainen M, Hartikainen P, Alafuzoff I (2008) Neuropathologic features of frontotemporal lobar degeneration with ubiquitin-positive inclusions visualized with ubiquitin-binding protein p62 immunohistochemistry. J Neuropathol Exp Neurol 67:280–298
    Article PubMed Google Scholar
  42. Ramesh Babu J, Lamar Seibenhener M, Peng J, Strom AL, Kemppainen R, Cox N, Zhu H, Wooten MC, Diaz-Meco MT, Moscat J, Wooten MW (2008) Genetic inactivation of p62 leads to accumulation of hyperphosphorylated tau and neurodegeneration. J Neurochem 106:107–120
    Article PubMed CAS Google Scholar
  43. Renton AE, Majounie E, Waite A, Simon-Sanchez J, Rollinson S, Gibbs JR, Schymick JC, Laaksovirta H, van Swieten JC, Myllykangas L, Kalimo H, Paetau A, Abramzon Y, Remes AM, Kaganovich A, Scholz SW, Duckworth J, Ding J, Harmer DW, Hernandez DG, Johnson JO, Mok K, Ryten M, Trabzuni D, Guerreiro RJ, Orrell RW, Neal J, Murray A, Pearson J, Jansen IE, Sondervan D, Seelaar H, Blake D, Young K, Halliwell N, Callister JB, Toulson G, Richardson A, Gerhard A, Snowden J, Mann D, Neary D, Nalls MA, Peuralinna T, Jansson L, Isoviita VM, Kaivorinne AL, Holtta-Vuori M, Ikonen E, Sulkava R, Benatar M, Wuu J, Chio A, Restagno G, Borghero G, Sabatelli M, Heckerman D, Rogaeva E, Zinman L, Rothstein JD, Sendtner M, Drepper C, Eichler EE, Alkan C, Abdullaev Z, Pack SD, Dutra A, Pak E, Hardy J, Singleton A, Williams NM, Heutink P, Pickering-Brown S, Morris HR, Tienari PJ, Traynor BJ (2011) A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD. Neuron 72:257–268
    Article PubMed CAS Google Scholar
  44. Rubino E, Rainero I, Chio A, Rogaeva E, Galimberti D, Fenoglio P, Grinberg Y, Isaia G, Calvo A, Gentile S, Bruni AC, St George-Hyslop PH, Scarpini E, Gallone S, Pinessi L (2012) SQSTM1 mutations in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Neurology 79:1556–1562
  45. Tanji K, Zhang HX, Mori F, Kakita A, Takahashi H, Wakabayashi K (2012) p62/sequestosome 1 binds to TDP-43 in brains with frontotemporal lobar degeneration with TDP-43 inclusions. J Neurosci Res 90:2034–2042
    Article PubMed CAS Google Scholar
  46. Vadlamudi RK, Joung I, Strominger JL, Shin J (1996) p62, a phosphotyrosine-independent ligand of the SH2 domain of p56lck, belongs to a new class of ubiquitin-binding proteins. J Biol Chem 271:20235–20237
    Article PubMed CAS Google Scholar
  47. Watts GD, Wymer J, Kovach MJ, Mehta SG, Mumm S, Darvish D, Pestronk A, Whyte MP, Kimonis VE (2004) Inclusion body myopathy associated with Paget disease of bone and frontotemporal dementia is caused by mutant valosin-containing protein. Nat Genet 36:377–381
    Article PubMed CAS Google Scholar

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