Treatment of type 1 Myotonic dystrophy by engineering site-specific RNA endonucleases that target (CUG) n repeats

Molecular Therapy

Volumn 22, Issue 2, 2014, Pages 312-320

  Zhang, Wenjing ^a,b   Wang, Yang ^b   Dong, Shuyun ^b,c   Choudhury, Rajarshi ^b   Jin, Yongfeng ^a   Wang, Zefeng ^b,d  

^a ZHEJIANG UNIVERSITY   (China)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF UTAH   (United States)

^d Macro Science Solutions LLP   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTIFICIAL SITE SPECIFIC RNA ENDONUCLEASE; ENDONUCLEASE; MESSENGER RNA; MYOTONIC DYSTROPHY PROTEIN KINASE; UNCLASSIFIED DRUG; PROTEIN BINDING; RIBONUCLEASE;

ALLELE; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; MYOTONIC DYSTROPHY; PROTEIN EXPRESSION; RNA BINDING; RNA CLEAVAGE; RNA DEGRADATION; RNA STRUCTURE; WILD TYPE; ALTERNATIVE RNA SPLICING; ANIMAL; CELL LINE; CHEMISTRY; ENZYME ACTIVE SITE; ENZYMOLOGY; GENE EXPRESSION; GENETICS; HYDROLYSIS; METABOLISM; TRINUCLEOTIDE REPEAT;

ALTERNATIVE SPLICING; ANIMALS; CATALYTIC DOMAIN; CELL LINE; ENDORIBONUCLEASES; GENE EXPRESSION; HUMANS; HYDROLYSIS; MYOTONIC DYSTROPHY; PROTEIN BINDING; TRINUCLEOTIDE REPEATS;

EID: 84895904922     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2013.251     Document Type: Article

References (47)

1. Turner, C and Hilton-Jones, D (2010). The myotonic dystrophies: diagnosis and management. J Neurol Neurosurg Psychiatr 81: 358-367.
2. Brook, JD, McCurrach, ME, Harley, HG, Buckler, AJ, Church, D, Aburatani, H 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.
3. Mahadevan, M, Tsilfidis, C, Sabourin, L, Shutler, G, Amemiya, C, Jansen, G et al. (1992). Myotonic dystrophy mutation: an unstable CTG repeat in the 3′ untranslated region of the gene. Science 255: 1253-1255.
4. Wheeler, TM and Thornton, CA (2007). Myotonic dystrophy: RNA-mediated muscle disease. Curr Opin Neurol 20: 572-576.
5. Lee, JE and Cooper, TA (2009). Pathogenic mechanisms of myotonic dystrophy. Biochem Soc Trans 37(Pt 6): 1281-1286.
6. Miller, JW, Urbinati, CR, Teng-Umnuay, P, Stenberg, MG, Byrne, BJ, Thornton, CA et al. (2000). Recruitment of human muscleblind proteins to (CUG)(n) expansions associated with myotonic dystrophy. EMBO J 19: 4439-4448.
7. Fardaei, M, Rogers, MT, Thorpe, HM, Larkin, K, Hamshere, MG, Harper, PS et al. (2002). Three proteins, MBNL, MBLL and MBXL, co-localize in vivo with nuclear foci of expanded-repeat transcripts in DM1 and DM2 cells. Hum Mol Genet 11: 805-814.
8. Jiang, H, Mankodi, A, Swanson, MS, Moxley, RT and Thornton, CA (2004). Myotonic dystrophy type 1 is associated with nuclear foci of mutant RNA, sequestration of muscleblind proteins and deregulated alternative splicing in neurons. Hum Mol Genet 13: 3079-3088.
9. Philips, AV, Timchenko, LT and Cooper, TA (1998). Disruption of splicing regulated by a CUG-binding protein in myotonic dystrophy. Science 280: 737-741.
10. Kuyumcu-Martinez, NM, Wang, GS and Cooper, TA (2007). Increased steadystate levels of CUGBP1 in myotonic dystrophy 1 are due to PKC-mediated hyperphosphorylation. Mol Cell 28: 68-78.
11. Ravel-Chapuis, A, Bélanger, G, Yadava, RS, Mahadevan, MS, DesGroseillers, L, Côté, J et al. (2012). The RNA-binding protein Staufen1 is increased in DM1 skeletal muscle and promotes alternative pre-mRNA splicing. J Cell Biol 196: 699-712.
12. Du, H, Cline, MS, Osborne, RJ, Tuttle, DL, Clark, TA, Donohue, JP et al. (2010). Aberrant alternative splicing and extracellular matrix gene expression in mouse models of myotonic dystrophy. Nat Struct Mol Biol 17: 187-193.
13. Savkur, RS, Philips, AV and Cooper, TA (2001). Aberrant regulation of insulin receptor alternative splicing is associated with insulin resistance in myotonic dystrophy. Nat Genet 29: 40-47.
14. Ho, TH, Charlet-B, N, Poulos, MG, Singh, G, Swanson, MS and Cooper, TA (2004). Muscleblind proteins regulate alternative splicing. EMBO J 23: 3103-3112.
15. Fugier, C, Klein, AF, Hammer, C, Vassilopoulos, S, Ivarsson, Y, Toussaint, A et al. (2011). Misregulated alternative splicing of BIN1 is associated with T tubule alterations and muscle weakness in myotonic dystrophy. Nat Med 17: 720-725.
16. Kimura, T, Nakamori, M, Lueck, JD, Pouliquin, P, Aoike, F, Fujimura, H et al. (2005). Altered mRNA splicing of the skeletal muscle ryanodine receptor and sarcoplasmic/ endoplasmic reticulum Ca2+-ATPase in myotonic dystrophy type 1. Hum Mol Genet 14: 2189-2200.
17. Hino, S, Kondo, S, Sekiya, H, Saito, A, Kanemoto, S, Murakami, T et al. (2007). Molecular mechanisms responsible for aberrant splicing of SERCA1 in myotonic dystrophy type 1. Hum Mol Genet 16: 2834-2843.
18. Kalsotra, A, Xiao, X, Ward, AJ, Castle, JC, Johnson, JM, Burge, CB et al. (2008). A postnatal switch of CELF and MBNL proteins reprograms alternative splicing in the developing heart. Proc Natl Acad Sci USA 105: 20333-20338.
19. Kanadia, RN, Shin, J, Yuan, Y, Beattie, SG, Wheeler, TM, Thornton, CA et al. (2006). Reversal of RNA missplicing and myotonia after muscleblind overexpression in a mouse poly(CUG) model for myotonic dystrophy. Proc Natl Acad Sci USA 103: 11748-11753.
20. Langlois, MA, Lee, NS, Rossi, JJ and Puymirat, J (2003). Hammerhead ribozymemediated destruction of nuclear foci in myotonic dystrophy myoblasts. Mol Ther 7(5 Pt 1): 670-680.
21. Lee, JE, Bennett, CF and Cooper, TA (2012). RNase H-mediated degradation of toxic RNA in myotonic dystrophy type 1. Proc Natl Acad Sci USA 109: 4221-4226.
22. Mulders, SA, van den Broek, WJ, Wheeler, TM, Croes, HJ, van Kuik-Romeijn, P, de Kimpe, SJ et al. (2009). Triplet-repeat oligonucleotide-mediated reversal of RNA toxicity in myotonic dystrophy. Proc Natl Acad Sci USA 106: 13915-13920.
23. Wheeler, TM, Sobczak, K, Lueck, JD, Osborne, RJ, Lin, X, Dirksen, RT et al. (2009). Reversal of RNA dominance by displacement of protein sequestered on triplet repeat RNA. Science 325: 336-339.
24. Wheeler, TM, Leger, AJ, Pandey, SK, MacLeod, AR, Nakamori, M, Cheng, SH et al. (2012). Targeting nuclear RNA for in vivo correction of myotonic dystrophy. Nature 488: 111-115.
25. Gareiss, PC, Sobczak, K, McNaughton, BR, Palde, PB, Thornton, CA and Miller, BL (2008). Dynamic combinatorial selection of molecules capable of inhibiting the (CUG) repeat RNA-MBNL1 interaction in vitro: discovery of lead compounds targeting myotonic dystrophy (DM1). J Am Chem Soc 130: 16254-16261.
26. Arambula, JF, Ramisetty, SR, Baranger, AM and Zimmerman, SC (2009). A simple ligand that selectively targets CUG trinucleotide repeats and inhibits MBNL protein binding. Proc Natl Acad Sci USA 106: 16068-16073.
27. Warf, MB, Nakamori, M, Matthys, CM, Thornton, CA and Berglund, JA (2009). Pentamidine reverses the splicing defects associated with myotonic dystrophy. Proc Natl Acad Sci USA 106: 18551-18556.
28. Childs-Disney, JL, Parkesh, R, Nakamori, M, Thornton, CA and Disney, MD (2012). Rational design of bioactive, modularly assembled aminoglycosides targeting the RNA that causes myotonic dystrophy type 1. ACS Chem Biol 7: 1984-1993.
29. Choudhury, R, Tsai, YS, Dominguez, D, Wang, Y and Wang, Z (2012). Engineering RNA endonucleases with customized sequence specificities. Nat Commun 3: 1147.
30. Cheong, CG and Hall, TM (2006). Engineering RNA sequence specificity of Pumilio repeats. Proc Natl Acad Sci USA 103: 13635-13639.
31. Wang, X, McLachlan, J, Zamore, PD and Hall, TM (2002). Modular recognition of RNA by a human pumilio-homology domain. Cell 110: 501-512.
32. Dong, S, Wang, Y, Cassidy-Amstutz, C, Lu, G, Bigler, R, Jezyk, MR et al. (2011). Specific and modular binding code for cytosine recognition in Pumilio/FBF (PUF) RNAbinding domains. J Biol Chem 286: 26732-26742.
33. Filipovska, A, Razif, MF, Nygård, KK and Rackham, O (2011). A universal code for RNA recognition by PUF proteins. Nat Chem Biol 7: 425-427.
34. Mooers, BH, Logue, JS and Berglund, JA (2005). The structural basis of myotonic dystrophy from the crystal structure of CUG repeats. Proc Natl Acad Sci USA 102: 16626-16631.
35. Michalowski, S, Miller, JW, Urbinati, CR, Paliouras, M, Swanson, MS and Griffith, J (1999). Visualization of double-stranded RNAs from the myotonic dystrophy protein kinase gene and interactions with CUG-binding protein. Nucleic Acids Res 27: 3534-3542.
36. Stumpf, CR, Opperman, L and Wickens, M (2008). Chapter 14. Analysis of RNA-protein interactions using a yeast three-hybrid system. Meth Enzymol 449: 295-315.
37. Glavan, F, Behm-Ansmant, I, Izaurralde, E and Conti, E (2006). Structures of the PIN domains of SMG6 and SMG5 reveal a nuclease within the mRNA surveillance complex. EMBO J 25: 5117-5125.
38. Takeshita, D, Zenno, S, Lee, WC, Saigo, K and Tanokura, M (2007). Crystal structure of the PIN domain of human telomerase-associated protein EST1A. Proteins 68: 980-989.
39. Davis, RL, Weintraub, H and Lassar, AB (1987). Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell 51: 987-1000.
40. Santoro, M, Masciullo, M, Bonvissuto, D, Bianchi, ML, Michetti, F and Silvestri, G (2013). Alternative splicing of human insulin receptor gene (INSR) in type I and type II skeletal muscle fibers of patients with myotonic dystrophy type 1 and type 2. Mol Cell Biochem 380: 259-265.
41. Gottlieb, PD, Pierce, SA, Sims, RJ, Yamagishi, H, Weihe, EK, Harriss, JV et al. (2002). Bop encodes a muscle-restricted protein containing MYND and SET domains and is essential for cardiac differentiation and morphogenesis. Nat Genet 31: 25-32.
42. Brandl, CJ, Green, NM, Korczak, B and MacLennan, DH (1986). Two Ca2+ ATPase genes: homologies and mechanistic implications of deduced amino acid sequences. Cell 44: 597-607.
43. MacLennan, DH, Rice, WJ and Green, NM (1997). The mechanism of Ca2+ transport by sarco(endo)plasmic reticulum Ca2+-ATPases. J Biol Chem 272: 28815- 28818.
44. Krzyzosiak, WJ, Sobczak, K, Wojciechowska, M, Fiszer, A, Mykowska, A and Kozlowski, P (2012). Triplet repeat RNA structure and its role as pathogenic agent and therapeutic target. Nucleic Acids Res 40: 11-26.
45. Tang, Y, Cummins, J, Huard, J and Wang, B (2010). AAV-directed muscular dystrophy gene therapy. Expert Opin Biol Ther 10: 395-408.
46. Terzi, D and Zachariou, V (2008). Adeno-associated virus-mediated gene delivery approaches for the treatment of CNS disorders. Biotechnol J 3: 1555-1563.
47. Wang, Y, Xiao, X, Zhang, J, Choudhury, R, Robertson, A, Li, K et al. (2013). A complex network of factors with overlapping affinities represses splicing through intronic elements. Nat Struct Mol Biol 20: 36-45.