Myotonic dystrophy expanded CUG repeats disturb the expression and phosphorylation of τ in PC12 cells

Journal of Neuroscience Research

Volumn 84, Issue 4, 2006, Pages 841-851

  Hernández Hernández, Oscar ^a   Bermúdez De León, Mario ^a   Gómez, Pablo ^a   Velázquez Bernardino, Prisiliana ^a   García Sierra, Francisco ^a   Cisneros, Bulmaro ^a,b  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

^b NONE   (Mexico)

Author keywords

phosphorylation; Akt GSK3 pathway; DM1 expanded CUG repeats; Neuronal differentiation; PC12 cells

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3BETA; MESSENGER RNA; MICROTUBULE ASSOCIATED PROTEIN; PROTEIN KINASE B;

3' UNTRANSLATED REGION; ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; CELL DIFFERENTIATION; CONTROLLED STUDY; MUTATIONAL ANALYSIS; MYOTONIC DYSTROPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT;

ANIMALS; BLOTTING, WESTERN; EXONS; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; GLYCOGEN SYNTHASE KINASE 3; MYOTONIC DYSTROPHY; NERVE GROWTH FACTOR; PC12 CELLS; PHOSPHORYLATION; PROTEIN ISOFORMS; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SERINE; TAU PROTEINS; TRINUCLEOTIDE REPEAT EXPANSION;

EID: 33748530018     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.20989     Document Type: Article

References (53)

1. Aizawa H, Kawasaki H, Murofushi H, Kotani S, Suzuki K, Sakai H. 1988. Microtubule-binding domain of tau proteins. J Biol Chem 263:7703-7707.
2. Amack JD, Mahadevan MS. 2001. The myotonic dystrophy expanded CUG repeat tract is necessary but not sufficient to disrupt C2C12 myoblast differentiation. Hum Mol Genet 10:1879-1887.
3. Ashizawa T. 1998. Myotonic dystrophy as a brain disorder. Arch Neurol 55:291-293.
4. Brook JD, McCurrach ME, Harley HG, Buckler AJ, Church D, Aburatani H, Hunter K, Stanton VP, Thirion JP, Hudson T, et al. 1992. Molecular basis of myotonic dystrophy: expansion of a trinucleotide (CTG) repeat at the 3′ end of a transcript encoding a protein kinase family member. Cell 68:799-808.
5. Brugg B, Matus A. 1988. PC12 cells express juvenile microtubule- associated proteins during nerve growth factor-induced neurite outgrowth. J Cell Biol 107:643-650.
6. Buee-Scherrer V, Condamines O, Mourton-Gilles C, Jakes R, Goedert M, Pau B, Delacourte A. 1996. AD2, a phosphorylation-dependent monoclonal antibody directed against tau proteins found in Alzheimer's disease. Brain Res Mol Brain Res 39:79-88.
7. Buj-Bello A, Furling D, Tronchere H, Laporte J, Lerouge T, Butler-Browne GS, Mandel JL. 2002. Muscle-specific alternative splicing of myotubularin-related 1 gene is impaired in DM1 muscle cells. Hum Mol Genet 11:2297-2307.
8. Buxton J, Shelbourne P, Davies J, Jones C, Van Tongeren T, Aslanidis C, de Jong P, Jansen G, Anvret M, Riley B, et al. 1992. Detection of an unstable fragment of DNA specific to individuals with myotonic dystrophy. Nature 355:547-548.
9. Cross DA, Alessi DR, Cohen P, Andjelkovich M, Hemmings BA. 1995. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378:785-789.
10. Charlet BN, Savkur RS, Singh G, Philips AV, Grice EA, Cooper TA. 2002. Loss of the muscle-specific chloride channel in type 1 myotonic dystrophy due to misregulated alternative splicing. Mol Cell 10:45-53.
11. Cho JH, Johnson GV. 2003. Glycogen synthase kinase 3beta phosphorylates tau at both primed and unprimed sites. Differential impact on microtubule binding. J Biol Chem 278:187-193.
12. D'Souza I, Poorkaj P, Hong M, Nochlin D, Lee VM, Bird TD, Schellenberg GD. 1999. Missense and silent tau gene mutations cause fronto-temporal dementia with parkinsonism-chromosome 17 type, by affecting multiple alternative RNA splicing regulatory elements. Proc Natl Acad Sci U S A 96:5598-5603.
13. Dajani R, Fraser E, Roe SM, Young N, Good V, Dale TC, Pearl LH. 2001. Crystal structure of glycogen synthase kinase 3 beta: structural basis for phosphate-primed substrate specificity and auto inhibition. Cell 105:721-732.
14. Davis BM, McCurrach ME, Taneja KL, Singer RH, Housman DE. 1997. Expansion of a CUG trinucleotide repeat in the 3′ untranslated region of myotonic dystrophy protein kinase transcripts results in nuclear retention of transcripts. Proc Natl Acad Sci U S A 94:7388-7393.
15. Davis PK, Johnson GV. 1999. The microtubule binding of tau and high molecular weight tau in apoptotic PC12 cells is impaired because of altered phosphorylation. J Biol Chem 274:35686-35692.
16. Fu YH, Pizzuti A, Fenwick RG Jr, King J, Rajnarayan S, Dunne PW, Dubel J, Nasser GA, Ashizawa T, de Jong P, et al. 1992. An unstable triplet repeat in a gene related to myotonic muscular dystrophy. Science 255:1256-1258.
17. Goedert M, Jakes R. 1990. Expression of separate isoforms of human tau protein: correlation with the tau pattern in brain and effects on tubulin polymerization. EMBO J 9:4225-4230.
18. Harper PS. 2001. Myotonic dystrophy. London: W.B. Saunders.
19. Hughes K, Nikolakaki E, Plyte SE, Totty NF, Woodgett JR. 1993. Modulation of the glycogen synthase kinase-3 family by tyrosine phosphorylation. EMBO J 12:803-808.
20. Hunter A, Tsilfidis C, Mettler G, Jacob P, Mahadevan M, Surh L, Korneluk R. 1992. The correlation of age of onset with CTG trinucleotide repeat amplification in myotonic dystrophy. J Med Genet 29:774-779.
21. Hutton M, Lendon CL, Rizzu P, Baker M, Froelich S, Houlden H, Pickering-Brown S, Chakraverty S, Isaacs A, Grover A, Hackett J, Adamson J, Lincoln S, Dickson D, Davies P, Petersen RC, Stevens M, de Graaff E, Wauters E, van Baren J, Hillebrand M, Joosse M, Kwon JM, Nowotny P, Che LK, Norton J, Morris JC, Reed LA, Trojanowski J, Basun H, Lannfelt L, Neystat M, Fahn S, Dark F, Tannenberg T, Dodd PR, Hayward N, Kwok JB, Schofield PR, Andreadis A, Snowden J, Craufurd D, Neary D, Owen F, Oostra BA, Hardy J, Goate A, van Swieten J, Mann D, Lynch T, Heutink P. 1998. Association of missense and 5′-splice-site mutations in tau with the inherited dementia FTDP-17. Nature 393:702-705.
22. Jiang H, Mankodi A, Swanson MS, Moxley RT, Thornton CA. 2004. Myotonic dystrophy type 1 is associated with nuclear foci of mutant RNA, sequestration of muscle blind proteins and deregulated alternative splicing in neurons. Hum Mol Genet 13:3079-3088.
23. Kim Y, Seger R, Suresh Babu CV, Hwang SY, Yoo YS. 2004. A positive role of the PI3-K/Akt signaling pathway in PC12 cell differentiation. Mol Cells 18:353-359.
24. Kiuchi A, Otsuka N, Namba Y, Nakano I, Tomonaga M. 1991. Presenile appearance of abundant Alzheimer's neurofibrillary tangles without senile plaques in the brain in myotonic dystrophy. Acta Neuropathol (Berl) 82:1-5.
25. Klesert TR, Otten AD, Bird TD, Tapscott SJ. 1997. Trinucleotide repeat expansion at the myotonic dystrophy locus reduces expression of DMAHP. Nat Genet 16:402-406.
26. Lovestone S, Reynolds CH, Latimer D, Davis DR, Anderton BH, Gallo JM, Hanger D, Mulot S, Marquardt B, Stabel S, et al. 1994. Alzheimer's disease-like phosphorylation of the microtubule-associated protein tau by glycogen synthase kinase-3 in transfected mammalian cells. Curr Biol 4:1077-1086.
27. Lu M, Kosik KS. 2001. Competition for microtubule-binding with dual expression of tau missense and splice isoforms. Mol Biol Cell 12:171-184.
28. Lucas JJ, Hernandez F, Gomez-Ramos P, Moran MA, Hen R, Avila J. 2001. Decreased nuclear beta-catenin, tau hyperphosphorylation and neurodegeneration in GSK-3beta conditional transgenic mice. EMBO J 20:27-39.
29. Mahadevan M, Tsilfidis C, Sabourin L, Shutler G, Amemiya C, Jansen G, Neville C, Narang M, Barcelo J, O'Hoy K, et al. 1992. Myotonic dystrophy mutation: an unstable CTG repeat in the 3′ untranslated region of the gene. Science 255:1253-1255.
30. Mankodi A, Takahashi MP, Jiang H, Beck CL, Bowers WJ, Moxley RT, Cannon SC, Thornton CA. 2002. Expanded CUG repeats trigger aberrant splicing of ClC-1 chloride channel pre-mRNA and hyperexcitability of skeletal muscle in myotonic dystrophy. Mol Cell 10:35-44.
31. Otten AD, Tapscott SJ. 1995. Triplet repeat expansion in myotonic dystrophy alters the adjacent chromatin structure. Proc Natl Acad Sci U S A 92:5465-5469.
32. Pap M, Cooper GM. 1998. Role of glycogen synthase kinase-3 in the phosphatidylinositol 3-Kinase/Akt cell survival pathway. J Biol Chem 273:19929-19932.
33. Papasozomenos SC. 1996. Heat shock induces rapid dephosphorylation of tau in both female and male rats followed by hyperphosphorylation only in female rats: implications for Alzheimer's disease. J Neurochem 66:1140-1149.
34. Philips AV, Timchenko LT, Cooper TA. 1998. Disruption of splicing regulated by a CUG-binding protein in myotonic dystrophy. Science 280:737-741.
35. Quintero-Mora ML, Depardon F, Waring J, Robert GK, Cisneros B. 2002. Expanded CTG repeats inhibit neuronal differentiation of the PC12 cell line. Biochem Biophys Res Commun 295:289-294.
36. Ranum LP, Day JW. 2004. Myotonic dystrophy: RNA pathogenesis comes into focus. Am J Hum Genet 74:793-804.
37. Redman JB, Fenwick RG Jr, Fu YH, Pizzuti A, Caskey CT. 1993. Relationship between parental trinucleotide GCT repeat length and severity of myotonic dystrophy in offspring. JAMA 269:1960-1965.
38. Sadot E, Barg J, Rasouly D, Lazarovici P, Ginzburg I. 1995. Short- and long-term mechanisms of tau regulation in PC12 cells. J Cell Sci 108:2857-2864.
39. Savkur RS, Philips AV, Cooper TA. 2001. Aberrant regulation of insulin receptor alternative splicing is associated with insulin resistance in myotonic dystrophy. Nat Genet 29:40-47.
40. Sergeant N, Sablonniere B, Schraen-Maschke S, Ghestem A, Maurage CA, Wattez A, Vermersch P, Delacourte A. 2001. Dysregulation of human brain microtubule-associated tau mRNA maturation in myotonic dystrophy type 1. Hum Mol Genet 10:2143-2155.
41. Seznec H, Agbulut O, Sergeant N, Savouret C, Ghestem A, Tabti N, Willer JC, Ourth L, Duros C, Brisson E, Fouquet C, Butler-Browne G, Delacourte A, Junien C, Gourdon G. 2001. Mice transgenic for the human myotonic dystrophy region with expanded CTG repeats display muscular and brain abnormalities. Hum Mol Genet 10:2717-2726.
42. Spillantini MG, Murrell JR, Goedert M, Farlow MR, Klug A, Ghetti B. 1998. Mutation in the tau gene in familial multiple system tauopathy with presenile dementia. Proc Natl Acad Sci U S A 95:7737-7741.
43. Stambolic V, Woodgett JR. 1994. Mitogen inactivation of glycogen synthase kinase-3 beta in intact cells via serine 9 phosphorylation. Biochem J 303:701-704.
44. Taneja KL, McCurrach M, Schalling M, Housman D, Singer RH. 1995. Foci of trinucleotide repeat transcripts in nuclei of myotonic dystrophy cells and tissues. J Cell Biol 128:995-1002.
45. Thornton CA, Wymer JP, Simmons Z, McClain C, Moxley RT 3rd. 1997. Expansion of the myotonic dystrophy CTG repeat reduces expression of the flanking DMAHP gene. Nat Genet 16:407-409.
46. Thurston VC, Zinkowski RP, Binder LI. 1996. Tau as a nucleolar protein in human non neural cells in vitro and in vivo. Chromosoma 105:20-30.
47. Timchenko NA, Patel R, Iakova P, Cai ZJ, Quan L, Timchenko LT. 2004. Overexpression of CUG triplet repeat-binding protein, CUGBP1, in mice inhibits myogenesis. J Biol Chem 279:13129-13139.
48. Tsilfidis C, MacKenzie AE, Mettler G, Barcelo J, Korneluk RG. 1992. Correlation between CTG trinucleotide repeat length and frequency of severe congenital myotonic dystrophy. Nat Genet 1:192-195.
49. Vermersch P, Sergeant N, Ruchoux MM, Hofmann-Radvanyi H, Wattez A, Petit H, Dwailly P, Delacourte A. 1996. Specific tau variants in the brains of patients with myotonic dystrophy. Neurology 47:711-717.
50. Vojtek AB, Taylor J, DeRuiter SL, Yu JY, Figueroa C, Kwok RP, Turner DL. 2003. Akt regulates basic helix-loop-helix transcription factor-coactivator complex formation and activity during neuronal differentiation. Mol Cell Biol 23:4417-4427.
51. Wagner U, Utton M, Gallo JM, Miller CC. 1996. Cellular phosphorylation of tau by GSK-3 beta influences tau binding to microtubules and microtubule organization. J Cell Sci 109:1537-1543.
52. Wansink DG, van Herpen RE, Coerwinkel-Driessen MM, Groenen PJ, Hemmings BA, Wieringa B. 2003. Alternative splicing controls myotonic dystrophy protein kinase structure, enzymatic activity, and subcellular localization. Mol Cell Biol 23:5489-5501.
53. Zhang J, Johnson GV. 2000. Tau protein is hyperphosphorylated in a site-specific manner in apoptotic neuronal PC12 cells. J Neurochem 75:2346-2357.