Silencing human genetic diseases with oligonucleotide-based therapies

Human Genetics

Volumn 132, Issue 5, 2013, Pages 481-493

  Martínez, Tamara ^a   Wright, Natalia ^a   López Fraga, Marta ^a   Jiménez, Ana Isabel ^a   Pañeda, Covadonga ^a  

^a Sylentis   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ALN AT 3; ALN HPC; ALN PCS; ALN TMP; ALN TTR 01; ALN TTR 02; ALN TTRSC; ANTISENSE OLIGONUCLEOTIDE; BMS 844421; DNA ENZYME; DRISAPERSEN; EPITHELIAL SODIUM CHANNEL; ETEPLIRSEN; FOMIVIRSEN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; ISIS 33361; ISIS AATRX; ISIS SMNRX; ISIS TTRRX; MIPOMERSEN; OLIGONUCLEOTIDE; PRO 044; PRO 135; PRO 289; RIBOZYME; SHORT HAIRPIN RNA 2.1; SMALL INTERFERING RNA; SPC 4955; SPC 5001; TD 101; UNCLASSIFIED DRUG;

ALPHA 1 ANTITRYPSIN DEFICIENCY; AMYLOIDOSIS; AMYOTROPHIC LATERAL SCLEROSIS; BETA THALASSEMIA; CARCINOGENICITY; CLINICAL TRIAL; CONGENITAL PACHYONYCHIA; CYSTIC FIBROSIS; CYTOMEGALOVIRUS RETINITIS; DRUG DOSE ESCALATION; DRUG EFFICACY; DRUG MECHANISM; DRUG SAFETY; DUCHENNE MUSCULAR DYSTROPHY; FAMILIAL HYPERCHOLESTEROLEMIA; GENE EXPRESSION; GENE SEQUENCE; GENE SILENCING; GENETIC DISORDER; HEMOGLOBINOPATHY; HEMOPHILIA; HUMAN; HUNTINGTON CHOREA; IMMUNOPATHOLOGY; INFLAMMATION; INJECTION SITE REACTION; KENNEDY DISEASE; LIVER DISEASE; LIVER TOXICITY; LIVER TRANSPLANTATION; MYOTONIC DYSTROPHY; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; REVIEW; RNA INTERFERENCE; SICKLE CELL ANEMIA; SIDE EFFECT; SPINAL MUSCULAR ATROPHY; SPINOCEREBELLAR DEGENERATION; TRANSTHYRETIN MEDIATED AMYLOIDOSIS;

ANTISENSE ELEMENTS (GENETICS); GENETIC DISEASES, INBORN; HUMANS; OLIGONUCLEOTIDES; RNA INTERFERENCE; RNA, SMALL INTERFERING;

EUKARYOTA;

EID: 84876500198     PISSN: 03406717     EISSN: 14321203     Source Type: Journal    
DOI: 10.1007/s00439-013-1288-1     Document Type: Review

References (88)

1. Aagaard L, Rossi JJ (2007) RNAi therapeutics: principles, prospects and challenges. Adv Drug Deliv Rev 59:75-86
2. Aartsma-Rus A, Janson AA, Kaman WE, Bremmer-Bout M, den Dunnen JT, Baas F, van Ommen GJ, van Deutekom JC (2003) Therapeutic antisense-induced exon skipping in cultured muscle cells from six different DMD patients. Hum Mol Genet 12:907-914
3. Abifadel M, Rabes JP, Devillers M, Munnich A, Erlich D, Junien C, Varret M, Boileau C (2009) Mutations and polymorphisms in the proprotein convertase subtilisin kexin 9 (PCSK9) gene in cholesterol metabolism and disease. Hum Mutat 30:520-529
4. Ackermann EJ, Guo S, Booten S, Alvarado L, Benson M, Hughes S, Monia BP (2012) Clinical development of an antisense therapy for the treatment of transthyretin-associated polyneuropathy. Amyloid 19(Suppl 1):43-44
5. Ando Y, Ueda M (2012) Diagnosis and therapeutic approaches to transthyretin amyloidosis. Curr Med Chem 19:2312-2323
6. Andrade C (1952) A peculiar form of peripheral neuropathy: familiar atypical generalized amyloidosis with special involvement of the peripheral nerves. Brain 75:408-427
7. Arechavala-Gomeza V, Kinali M, Feng L, Guglieri M, Edge G, Main M, Hunt D, Lehovsky J, Straub V, Bushby K, Sewry CA, Morgan JE, Muntoni F (2010) Revertant fibres and dystrophin traces in Duchenne muscular dystrophy: implication for clinical trials. Neuromuscul Disord 20:295-301
8. Berntorp E, Gomperts E, Hoots K, Wong WY (2006) The next generation of hemophilia treatment specialists. Semin Thromb Hemost 32(Suppl 2):39-42
9. Boyle MP (2007) Adult cystic fibrosis. JAMA 298:1787-1793
10. Brautbar A, Ballantyne CM (2011) Pharmacological strategies for lowering LDL cholesterol: statins and beyond. Nat Rev Cardiol 8:253-265
11. Brouwer JR, Willemsen R, Oostra BA (2009) Microsatellite repeat instability and neurological disease. BioEssays 31:71-83
12. Burnett JC, Rossi JJ (2012) RNA-based therapeutics: current progress and future prospects. Chem Biol 19:60-71
13. Chambers LA, Rollins BM, Tarran R (2007) Liquid movement across the surface epithelium of large airways. Respir Physiol Neurobiol 159:256-270
14. Charlton-Menys V, Durrington PN (2008) Human cholesterol metabolism and therapeutic molecules. Exp Physiol 93:27-42
15. Chekulaeva M, Filipowicz W (2009) Mechanisms of miRNA-mediated post-transcriptional regulation in animal cells. Curr Opin Cell Biol 21:452-460
16. Cohen JC, Boerwinkle E, Mosley TH Jr, Hobbs HH (2006) Sequence variations in PCSK9, low LDL, and protection against coronary heart disease. N Engl J Med 354:1264-1272
17. Collawn JF, Lazrak A, Bebok Z, Matalon S (2012) The CFTR and ENaC debate: how important is ENaC in CF lung disease? Am J Physiol Lung Cell Mol Physiol 302:L1141-L1146
18. Cooper TA, Wan L, Dreyfuss G (2009) RNA and disease. Cell 136:777-793
19. Crooke ST (2004) Progress in antisense technology. Annu Rev Med 55:61-95
20. Davidson BL, McCray PB Jr (2011) Current prospects for RNA interference-based therapies. Nat Rev Genet 12:329-340
21. Day JW, Ranum LP (2005) Genetics and molecular pathogenesis of the myotonic dystrophies. Curr Neurol Neurosci Rep 5:55-59
22. Dedoussis GV (2007) Apolipoprotein polymorphisms and familial hypercholesterolemia. Pharmacogenomics 8:1179-1189
23. DiFiglia M, Sena-Esteves M, Chase K, Sapp E, Pfister E, Sass M, Yoder J, Reeves P, Pandey RK, Rajeev KG, Manoharan M, Sah DW, Zamore PD, Aronin N (2007) Therapeutic silencing of mutant huntingtin with siRNA attenuates striatal and cortical neuropathology and behavioral deficits. Proc Natl Acad Sci USA 104:17204-17209
24. Dunckley MG, Manoharan M, Villiet P, Eperon IC, Dickson G (1998) Modification of splicing in the dystrophin gene in cultured Mdx muscle cells by antisense oligoribonucleotides. Hum Mol Genet 7:1083-1090
25. Dykxhoorn DM, Schlehuber LD, London IM, Lieberman J (2006) Determinants of specific RNA interference-mediated silencing of human beta-globin alleles differing by a single nucleotide polymorphism. Proc Natl Acad Sci USA 103:5953-5958
26. Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T (2001a) Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411:494-498
27. Elbashir SM, Lendeckel W, Tuschl T (2001b) RNA interference is mediated by 21- and 22-nucleotide RNAs. Genes Dev 15:188-200
28. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806-811
29. Gagnon KT (2010) HD therapeutics - CHDI fifth annual conference. IDrugs 13:219-223
30. Goyenvalle A, Seto JT, Davies KE, Chamberlain J (2011) Therapeutic approaches to muscular dystrophy. Hum Mol Genet 20:R69-R78
31. Haddley K (2011) Mipomersen sodium: a new option for the treatment of familial hypercholesterolemia. Drugs Today (Barc) 47:891-901
32. Harper SQ (2009) Progress and challenges in RNA interference therapy for Huntington disease. Arch Neurol 66:933-938
33. Harper SQ, Staber PD, He X, Eliason SL, Martins IH, Mao Q, Yang L, Kotin RM, Paulson HL, Davidson BL (2005) RNA interference improves motor and neuropathological abnormalities in a Huntington's disease mouse model. Proc Natl Acad Sci USA 102:5820-5825
34. Hickerson RP, Smith FJ, McLean WH, Landthaler M, Leube RE, Kaspar RL (2006) SiRNA-mediated selective inhibition of mutant keratin mRNAs responsible for the skin disorder pachyonychia congenita. Ann NY Acad Sci 1082:56-61
35. Hickerson RP, Flores MA, Leake D, Lara MF, Contag CH, Leachman SA, Kaspar RL (2011) Use of self-delivery siRNAs to inhibit gene expression in an organotypic pachyonychia congenita model. J Invest Dermatol 131:1037-1044
36. Hoffman EP, Brown RH Jr, Kunkel LM (1987) Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 51:919-928
37. Hofmann Y, Lorson CL, Stamm S, Androphy EJ, Wirth B (2000) Htra2-beta 1 stimulates an exonic splicing enhancer and can restore full-length SMN expression to survival motor neuron 2 (SMN2). Proc Natl Acad Sci USA 97:9618-9623
38. Horton JD, Cohen JC, Hobbs HH (2007) Molecular biology of PCSK9: its role in LDL metabolism. Trends Biochem Sci 32:71-77
39. Hua Y, Vickers TA, Okunola HL, Bennett CF, Krainer AR (2008) Antisense masking of an hnRNP A1/A2 intronic splicing silencer corrects SMN2 splicing in transgenic mice. Am J Hum Genet 82:834-848
40. Imarisio S, Carmichael J, Korolchuk V, Chen CW, Saiki S, Rose C, Krishna G, Davies JE, Ttofi E, Underwood BR, Rubinsztein DC (2008) Huntington's disease: from pathology and genetics to potential therapies. Biochem J 412:191-209
41. Innerarity TL, Mahley RW, Weisgraber KH, Bersot TP, Krauss RM, Vega GL, Grundy SM, Friedl W, Davignon J, McCarthy BJ (1990) Familial defective apolipoprotein B-100: a mutation of apolipoprotein B that causes hypercholesterolemia. J Lipid Res 31:1337-1349
42. Jabs DA, Griffiths PD (2002) Fomivirsen for the treatment of cytomegalovirus retinitis. Am J Ophthalmol 133:552-556
43. Kaspar RL (2005) Challenges in developing therapies for rare diseases including pachyonychia congenita. J Investig Dermatol Symp Proc 10:62-66
44. Kinali M, Arechavala-Gomeza V, Feng L, Cirak S, Hunt D, Adkin C, Guglieri M, Ashton E, Abbs S, Nihoyannopoulos P, Garralda ME, Rutherford M, McCulley C, Popplewell L, Graham IR, Dickson G, Wood MJ, Wells DJ, Wilton SD, Kole R, Straub V, Bushby K, Sewry C, Morgan JE, Muntoni F (2009) Local restoration of dystrophin expression with the morpholino oligomer AVI-4658 in Duchenne muscular dystrophy: a single-blind, placebo-controlled, dose-escalation, proof-of-concept study. Lancet Neurol 8:918-928
45. Koenig M, Beggs AH, Moyer M, Scherpf S, Heindrich K, Bettecken T, Meng G, Muller CR, Lindlof M, Kaariainen H et al (1989) The molecular basis for Duchenne versus Becker muscular dystrophy: correlation of severity with type of deletion. Am J Hum Genet 45:498-506
46. Kubodera T, Yamada H, Anzai M, Ohira S, Yokota S, Hirai Y, Mochizuki H, Shimada T, Mitani T, Mizusawa H, Yokota T (2010) In vivo application of an RNAi strategy for the selective suppression of a mutant allele. Hum Gene Ther 22:27-34
47. Lara MF, Gonzalez-Gonzalez E, Speaker TJ, Hickerson RP, Leake D, Milstone LM, Contag CH, Kaspar RL (2012) Inhibition of CD44 gene expression in human skin models, using self-delivery short interfering RNA administered by dissolvable microneedle arrays. Hum Gene Ther 23:816-823
48. Leachman SA, Hickerson RP, Hull PR, Smith FJ, Milstone LM, Lane EB, Bale SJ, Roop DR, McLean WH, Kaspar RL (2008) Therapeutic siRNAs for dominant genetic skin disorders including pachyonychia congenita. J Dermatol Sci 51:151-157
49. Leachman SA, Hickerson RP, Schwartz ME, Bullough EE, Hutcherson SL, Boucher KM, Hansen CD, Eliason MJ, Srivatsa GS, Kornbrust DJ, Smith FJ, McLean WI, Milstone LM, Kaspar RL (2010) First-in-human mutation-targeted siRNA phase Ib trial of an inherited skin disorder. Mol Ther 18:442-446
50. Lopez-Fraga M, Martinez T, Jimenez A (2009) RNA interference technologies and therapeutics: from basic research to products. BioDrugs 23:305-332
51. Martinez T, Wright N, Pañeda C, Jimenez A, Lopez-Fraga M (2011) RNA interference-based therapeutics: harnessing the powers of nature In: Rundfeldt C (ed) Drug development: a case study based insight into modern strategies. InTech, pp 265-312
52. Maxwell MM, Pasinelli P, Kazantsev AG, Brown RH Jr (2004) RNA interference-mediated silencing of mutant superoxide dismutase rescues cyclosporin A-induced death in cultured neuroblastoma cells. Proc Natl Acad Sci USA 101:3178-3183
53. McGowan MP, Tardif JC, Ceska R, Burgess LJ, Soran H, Gouni-Berthold I, Wagener G, Chasan-Taber S (2012) Randomized, placebo-controlled trial of mipomersen in patients with severe hypercholesterolemia receiving maximally tolerated lipid-lowering therapy. PLoS ONE 7:e49006
54. Mulders SA, van Engelen BG, Wieringa B, Wansink DG (2010) Molecular therapy in myotonic dystrophy: focus on RNA gain-of-function. Hum Mol Genet 19:R90-R97
55. Nguyen J, Szoka FC (2012) Nucleic acid delivery: the missing pieces of the puzzle? Acc Chem Res 45:1153-1162
56. Pañeda C, Martinez T, Wright N, Jimenez A (2012) Recent advances in ocular nucleic-based therapies: the silent era. In: Adio A (ed) Ocular diseases. InTech, pp 157-185
57. Pecot CV, Calin GA, Coleman RL, Lopez-Berestein G, Sood AK (2011) RNA interference in the clinic: challenges and future directions. Nat Rev Cancer 11:59-67
58. Perkel JMPD (2012) RNAi therapeutics: the teenage years. Biotechniques 52:355-357
59. Persidis A (1999) Antisense therapeutics. Nat Biotechnol 17:403-404
60. Phillips MI (2005) Antisense therapeutics: a promise waiting to be fulfilled. Methods Mol Med 106:3-10
61. Phillips W, Shannon KM, Barker RA (2008) The current clinical management of Huntington's disease. Mov Disord 23:1491-1504
62. Raoul C, Abbas-Terki T, Bensadoun JC, Guillot S, Haase G, Szulc J, Henderson CE, Aebischer P (2005) Lentiviral-mediated silencing of SOD1 through RNA interference retards disease onset and progression in a mouse model of ALS. Nat Med 11:423-428
63. Rettig GR, Behlke MA (2011) Progress toward in vivo use of siRNAs-II. Mol Ther 20:483-512
64. Rigo F, Hua Y, Krainer AR, Bennett CF (2012) Antisense-based therapy for the treatment of spinal muscular atrophy. J Cell Biol 199:21-25
65. Rowland LP, Shneider NA (2001) Amyotrophic lateral sclerosis. N Engl J Med 344:1688-1700
66. Samakoglu S, Lisowski L, Budak-Alpdogan T, Usachenko Y, Acuto S, Di Marzo R, Maggio A, Zhu P, Tisdale JF, Riviere I, Sadelain M (2006) A genetic strategy to treat sickle cell anemia by coregulating globin transgene expression and RNA interference. Nat Biotechnol 24:89-94
67. Schlosser K, Li Y (2009) Biologically inspired synthetic enzymes made from DNA. Chem Biol 16:311-322
68. Schubert S, Kurreck J (2004) Ribozyme- and deoxyribozyme-strategies for medical applications. Curr Drug Targets 5:667-681
69. Seidah NG, Mayer G, Zaid A, Rousselet E, Nassoury N, Poirier S, Essalmani R, Prat A (2008) The activation and physiological functions of the proprotein convertases. Int J Biochem Cell Biol 40:1111-1125
70. Shen TJ, Rogers H, Yu X, Lin F, Noguchi CT, Ho C (2007) Modification of globin gene expression by RNA targeting strategies. Exp Hematol 35:1209-1218
71. Singh NN, Shishimorova M, Cao LC, Gangwani L, Singh RN (2009) A short antisense oligonucleotide masking a unique intronic motif prevents skipping of a critical exon in spinal muscular atrophy. RNA Biol 6:341-350
72. Sjouke B, Kusters DM, Kastelein JJ, Hovingh GK (2011) Familial hypercholesterolemia: present and future management. Curr Cardiol Rep 13:527-536
73. Smith FJ, Liao H, Cassidy AJ, Stewart A, Hamill KJ, Wood P, Joval I, van Steensel MA, Bjorck E, Callif-Daley F, Pals G, Collins P, Leachman SA, Munro CS, McLean WH (2005) The genetic basis of pachyonychia congenita. J Investig Dermatol Symp Proc 10:21-30
74. Solis AS, Shariat N, Patton JG (2008) Splicing fidelity, enhancers, and disease. Front Biosci 13:1926-1942
75. Stein EA, Dufour R, Gagne C, Gaudet D, East C, Donovan JM, Chin W, Tribble DL, McGowan M (2012) Apolipoprotein B synthesis inhibition with mipomersen in heterozygous familial hypercholesterolemia: results of a randomized, double-blind, placebo-controlled trial to assess efficacy and safety as add-on therapy in patients with coronary artery disease. Circulation 126:2283-2292
76. Stoller JK, Aboussouan LS (2012) A review of alpha1-antitrypsin deficiency. Am J Respir Crit Care Med 185:246-259
77. Sumner CJ (2006) Therapeutics development for spinal muscular atrophy. NeuroRx 3:235-245
78. Tomita N, Morishita R, Tomita T, Ogihara T (2002) Potential therapeutic applications of decoy oligonucleotides. Curr Opin Mol Ther 4:166-170
79. Tuschl T, Zamore PD, Lehmann R, Bartel DP, Sharp PA (1999) Targeted mRNA degradation by double-stranded RNA in vitro. Genes Dev 13:3191-3197
80. van Deutekom JC, Janson AA, Ginjaar IB, Frankhuizen WS, Aartsma-Rus A, Bremmer-Bout M, den Dunnen JT, Koop K, van der Kooi AJ, Goemans NM, de Kimpe SJ, Ekhart PF, Venneker EH, Platenburg GJ, Verschuuren JJ, van Ommen GJ (2007) Local dystrophin restoration with antisense oligonucleotide PRO051. N Engl J Med 357:2677-2686
81. Venter JC, Adams MD, Myers EW, Li PW, Mural RJ, Sutton GG, Smith HO, Yandell M, Evans CA, Holt RA, Gocayne JD, Amanatides P, Ballew RM, Huson DH, Wortman JR, Zhang Q, Kodira CD, Zheng XH, Chen L, Skupski M, Subramanian G, Thomas PD, Zhang J, Gabor Miklos GL, Nelson C, Broder S, Clark AG, Nadeau J, McKusick VA, Zinder N, Levine AJ, Roberts RJ, Simon M, Slayman C, Hunkapiller M, Bolanos R, Delcher A, Dew I, Fasulo D, Flanigan M, Florea L, Halpern A, Hannenhalli S, Kravitz S, Levy S, Mobarry C, Reinert K, Remington K, Abu-Threideh J, Beasley E, Biddick K, Bonazzi V, Brandon R, Cargill M, Chandramouliswaran I, Charlab R, Chaturvedi K, Deng Z, Di Francesco V, Dunn P, Eilbeck K, Evangelista C, Gabrielian AE, Gan W, Ge W, Gong F, Gu Z, Guan P, Heiman TJ, Higgins ME, Ji RR, Ke Z, Ketchum KA, Lai Z, Lei Y, Li Z, Li J, Liang Y, Lin X, Lu F, Merkulov GV, Milshina N, Moore HM, Naik AK, Narayan VA, Neelam B, Nusskern D, Rusch DB, Salzberg S, Shao W, Shue B, Sun J, Wang Z, Wang A, Wang X, Wang J, Wei M, Wides R, Xiao C, Yan C et al (2001) The sequence of the human genome. Science 291:1304-1351
82. Verhaart IE, Aartsma-Rus A (2012) Gene therapy for Duchenne muscular dystrophy. Curr Opin Neurol 25:588-596
83. Visser ME, Kastelein JJ, Stroes ES (2010) Apolipoprotein B synthesis inhibition: results from clinical trials. Curr Opin Lipidol 21:319-323
84. Visser ME, Witztum JL, Stroes ES, Kastelein JJ (2012) Antisense oligonucleotides for the treatment of dyslipidaemia. Eur Heart J 33:1451-1458
85. Xia X, Zhou H, Huang Y, Xu Z (2006) Allele-specific RNAi selectively silences mutant SOD1 and achieves significant therapeutic benefit in vivo. Neurobiol Dis 23:578-586
86. Yueksekdag G, Drechsel M, Rossner M, Schmidt C, Kormann M, Illenyi MC, Rudolph C, Rosenecker J (2010) Repeated siRNA application is a precondition for successful mRNA gammaENaC knockdown in the murine airways. Eur J Pharm Biopharm 75:305-310
87. Zamore PD, Tuschl T, Sharp PA, Bartel DP (2000) RNAi: double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21 to 23 nucleotide intervals. Cell 101:25-33
88. Zhao Z, Tuakli-Wosornu Y, Lagace TA, Kinch L, Grishin NV, Horton JD, Cohen JC, Hobbs HH (2006) Molecular characterization of loss-of-function mutations in PCSK9 and identification of a compound heterozygote. Am J Hum Genet 79:514-523