Therapeutic benefit derived from RNAi-mediated ablation of IMPDH1 transcripts in a murine model of autosomal dominant retinitis pigmentosa (RP10)

Human Molecular Genetics

Volumn 17, Issue 14, 2008, Pages 2084-2100

  Tam, Lawrence C S ^a   Kiang, Anna Sophia ^a   Kennan, Avril ^a   Kenna, Paul F ^a   Chadderton, Naomi ^a   Ader, Marius ^a   Palfi, Arpad ^a   Aherne, Aileen ^a   Ayuso, Carmen ^b   Campbell, Matthew ^a   Reynolds, Alison ^a   Mckee, Alex ^a   Humphries, Marian M ^a   Farrar, G Jane ^a   Humphries, Pete ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED DE ENFERMEDADES RARAS CIBERER   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; INOSINATE DEHYDROGENASE; MUTANT PROTEIN; PARVOVIRUS VECTOR; SHORT HAIRPIN RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOSOMAL DOMINANT DISORDER; CONTROLLED STUDY; DISEASE SEVERITY; DRUG EFFICACY; DRUG MECHANISM; DRUG TOLERABILITY; GENE DISRUPTION; GENE EXPRESSION; GENE REPRESSION; GENETIC MODEL; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; NONVIRAL GENE THERAPY; NUCLEOTIDE SEQUENCE; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN TARGETING; RETINITIS PIGMENTOSA; RNA INTERFERENCE; VIRAL GENE DELIVERY SYSTEM;

ANIMALS; BASE SEQUENCE; DEPENDOVIRUS; DOWN-REGULATION; GENE THERAPY; GENES, DOMINANT; GENETIC VECTORS; HELA CELLS; HUMANS; IMP DEHYDROGENASE; MICE; MICE, INBRED C57BL; MODELS, ANIMAL; MOLECULAR SEQUENCE DATA; MUTATION; RETINITIS PIGMENTOSA; RNA INTERFERENCE; RNA, SMALL INTERFERING; TRANSDUCTION, GENETIC;

MURINAE; MUS;

EID: 46249091156     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddn107     Document Type: Article

References (67)

1. Hartong, D.T., Berson, E.L. and Dryja, T. (2006) Retinitis Pigmentosa. Lancet, 368, 1795-1809.
2. Jordan, S.A., Farrar, G.J., Kenna, P.F., Humphries, M.M., Sheils, D.M., Kumar-Singh, R., Sharp, E.M., Ayuso, C., Benitez, J. and Humphries, P. (1993) Localization of an autosomal dominant retinitis pigmentosa gene to chromosome 7q. Nat. Genet., 4, 54-58.
3. Kennan, A., Aherne, A., Palfi, A., Humphries, M., McKee, A., Stitt, A., Simpson, D.A., Demtroder, K., Orntoft, T., Ayuso, C. et al. (2002) Identification of an IMPDH1 mutation in autosomal dominant retinitis pigmentosa (RP10) revealed following comparative microarray analysis of transcripts derived from retinas of wild-type and Rho-/- mice. Hum. Mol. Genet., 11, 547-557.
4. Bowne, S.J., Sullivan, L.S., Blanton, S.H., Cepko, C.L., Blackshaw, S., Birch, D.G., Hughbanks-Wheaton, D., Heckenlively, J.R. and Daiger, S.P. (2002) Mutations in the inosine monophosphate dehydrogenase 1 gene (IMPDH1) cause the RP10 form of autosomal dominant retinitis pigmentosa. Hum. Mol. Genet., 11, 559-568
5. Natsumeda, Y., Ohno, S., Kawaski, H., Konno, Y., Weber, G. and And Susuki, K. (1990) Two distinct cDNAs for human IMP dehydrogenase. J. Biol. Chem., 65, 5292-5295.
6. Carr S.F., Papp, E., Wu, J.C. and And Natsumeda, Y. (1993) Characterisation of human type 1 and type II IMP dehydrogenase. J Biol Chem. 268, 27286-27290.
7. Hager, P.W., Collart, F.R., Huberman, E. and Mitchell, B.S. (1995) Recombinant human inosine monophosphate dehydrogenase type I and type II proteins. Purification and characterization of inhibitor binding. Biochem. Pharmacol., 49, 1323-1329.
8. Collart, F. and Huberman, E. (1988) Cloning and sequence analysis of the human and Chinese Hamster Inosine-5′-monophosphate dehygrogenase cDNAs. J. Biol. Chem., 263, 15769-15772.
9. Nagai, M., Natsumeda, Y., Konno, Y., Hoffman, R., Irino, S. and Weber, G. (1991) Selective up-regulation of type II inosine 5′-monophosphate dehydrogenase messenger RNA expression in human leukemias. Cancer Res., 51, 3886-3890.
10. Collart, F.R., Chubb, C.B., Mirkin, B.L. and Huberman, E. (1992) Increased inosine-5′-phosphate dehydrogenase gene expression in solid tumor tissues and tumor cell lines. Cancer Res., 52, 5826-5828.
11. Nagai, M., Natsumeda, Y. and Weber, G. (1992) Proliferation-linked regulation of type II IMP dehydrogenase gene in human normal lymphocytes and HL-60 leukemic cells. Cancer Res., 52, 258-261.
12. Aherne, A., Kennan, A., Kenna, P.F., McNally, N., Lloyd, D.G., Alberts, I.L., Kiang, A.S., Humphries, M.M., Ayuso, C., Engel, P.C. et al. (2004) On the molecular pathology of neurodegeneration in IMPDH1-based retinitis pigmentosa. Hum. Mol. Genet., 13, 641-650.
13. McLean, J.E., Hamaguchi, N., Belenky, P., Mortimer, S.E., Stanton, M. and Hedstrom, L. (2004) Inosine 5́-monophosphate dehydrogenase binds nucleic acids in vitro and in vivo. J. Biochem., 379, 243-251.
14. Mortimer, S.E. and Hedstrom, L. (2005) Autosomal dominant retinitis pigmentosa mutations in inosine 5́-monophosphate dehydrogenase type 1 disrupt nucleic acid binding. J. Biochem., 390, 41-47.
15. Bowne, S.J., Liu, Q., Sullivan, L.S., Zhu, J., Spellicy, C.J., Rickman, C.B., Pierce, E.A, and Daiger, S.P. (2006) Why do mutations in the ubiquitously expressed housekeeping gene IMPDH1 cause retina-specific photoreceptor degeneration? Invest. Ophthalmol. Vis. Sci., 47 3754-3765.
16. Sohocki, M.M., Daiger, S.P., Bowne, S.J., Rodriquez, J.A., Northrup, H., Heckenlively, J.R., Birch, D.G., Mintz-Hittner, H., Ruiz, R.S., Lewis, R.A. et al. (2001) Prevalence of mutations causing retinitis pigmentosa and other inherited retinopathies. Hum Mutat., 17 42-51.
17. Reynolds, A., Leake, D., Boese, Q., Scaringe, S., Marshall, W.S. and Khovorova, A. (2004) Rational siRNA design for RNA interference. Nat. Biotechnol., 22, 326-330.
18. Elbashir, S.M., Harborth, J., Lendeckel, W., Yalcin, A., Weber, K. and Tuschl, T. (2001) Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalians cells. Nature, 411: 494-498
19. Myers, J.W., Jr, Chi, J-T., Gong, D., Schaner, M.E., O'Brown, P. and Ferrell, J.E., Jr (2006) Minimizing off-target effects by diced siRNAs for RNA interference. J. RNAi and Gene Silencing, 2. 181-194.
20. So, S., Nomura, Y., Adachi, N., Kobayashi, Y., Hori, T., Kurihara, Y. and Koyama, H. (2006) Enhanced gene targeting efficiency by siRNA that silences the expression of Bloom syndrome gene in human cells. Gene to Cells, 11. 363-371.
21. Kiang, A.S., Palfi, A., Ader, M., Kenna, P.F., Millington-Ward, S., Clark, G., Kennan, A., O'Reilly, M., Tam, L.C.S., Aherne, A. et al. (2005) Toward a Gene Therapy for Dominant Disease: Validation of an RNA Interference-Based Mutation-Independent Approach. Mol. Ther., 12, 555-561.
22. Palfi, A., Arder, M., Kiang, A.S., Millington-Ward, S., Clark, G., O'Reilly, M., McMahon, H.P., Kenna, P.F., Humphries, P. and Farrar, G.J. (2006) RNAi-based suppression and replacement of rds-peripherin in retinal organotypic culture. Hum. Mutat., 27, 260-268.
23. O'Reilly, M., Palfi, A., Chadderton, N., Millington-Ward, S., Ader, M., Cronin, T., Tuohy, T., Auricchio, A., Hildinger, M., Tivnan, A. et al. (2007) RNA interference-mediated suppression and replacement of human rhodopsin in vivo. Am. J. Hum. Genet., 81, 127-135.
24. Xiao, X., Li, J. and Samulski, R.J. (1998) Production of high-titer recombinant adeno-associated virus vectors in the absence of helper adenovirus. J. Virol., 72, 2224-2232.
25. Hildinger, M., Auricchio, A., Gao, G., Wang, L., Chirmule, N. and Wilson, J.M. (2001) Hybrid vectors based on adeno-associated virus serotypes 2 and 5 for muscle-directed gene transfer. J. Virol., 75, 6199-6203.
26. Auricchio, A., Kobinger, G., Anand, V., Hildinger, M., O'Connor, E., Maguire, A.M., Wilson, J.M. and Bennett, J. (2001) Exchange of surface proteins impacts on viral vector cellular specificity and transduction characteristics: The retina as a model. Hum. Mol. Genet., 10 3075-3081.
27. Tessitore, A., Parisi, F., Denti, M.A., Allocca, M., Di Vicino, U., Domenici, L., Bozzoni, I. and Auricchio, A. (2006) Preferential silencing of a common dominant rhodopsin mutation does not inhibit retinal degeneration in a transgenic model. Mol. Ther., 14, 692-699.
28. Gorbatyuk, M., Justilien, V., Liu, J., Hauswirth, W.W. and Lewin, A.S. (2007) Suppression of mouse rhodopsin expression in vivo by AAV mediated siRNA delivery. Vis. Res., 47, 1202-1208.
29. Humphries, M.M., Rancourt, D., Farrar, G.J., Kenna, P., Hazel, M., Bush, R.A., Sieving, P.A., Sheils, D.M., McNally, N., Creighton, P., Erven, A., Boros, A., Gulya, K., Capecchi, M.R. and Humphries, P. (1997) Retinopathy induced in mice by targeted disruption of the rhodopsin gene. Nat. Genet., 15: 216-219
30. Tan, E., Wang, Q., Quiambao, A.B., Xu, X., Qtaishat, N.M., Peachey, N.S., Lem, J., Fliesler, S.J., Pepperberg, D.R., Naash, M.I. and Al-Ubaidi, M.R. (2001) The relationship between opsin overexpression and photoreceptor degeneration, Invest. Ophthal. Vis. Sci., 42: 589-600
31. Cheng, T., Peachey, N.S., Li, S., Goto, Y., Cao, Y. and Naash, M.I. (1997) The effect of peripherin/rds haploinsufficiency on rod and cone photoreceptors. J. Neurosci., 17, 8118-8128
32. McNally, N., Kenna, P.F., Rancourt, D., Ahmed, T., Stitt, A., Colledge, W.H., Lloyd, D.G., Palfi, A., O'Neill, B., Humphries, M.M., Humphries, P. and Farrar, G.J. (2002) Murine model of autosomal dominant retinitis pigmentosa generated by targeted deletion at codon 307 of the rds-peripherin gene. Hum. Mol. Genet., 11: 1005-1016
33. Snyder, R.O., Miao, C., Meuse, L., Tubb, J., Donahue, B.A., Lin, H.F., Stafford, D.W., Patel, S., Thompson, A.R., Nichols, T. et al. (1999) Correction of hemophilia B in canine and murine models using recombinant adeno-associated viral vectors. Nat. Med., 5, 64-70.
34. Phillips, M.I., Tang, Y., Schmidt-Ott, K., Qian, K. and Kagiyama, S. (2002) Vigilant vector: Heart-specific promoter in an adeno-associated virus vector for cardioprotection. Hypertension, 39, 651-655.
35. Mount, J.D., Herzog, R.W., Tillson, D.M., Goodman, S.A., Robinson, N., McCleland, M.L., Bellinger, D., Nichols, T.C., Arruda, V.R., Lothrop, C.D., Jr. et al. (2002) Sustained phenotypic correction of hemophilia B dogs with a factor IX null mutation by liver-directed gene therapy. Blood, 99, 2670-2676.
36. Ali, R.R., Sarra, G.M., Stephens, C., Alwis, M.D., Bainbridge, J.W., Munro, P.M., Fauser, S., Reichel, M.B., Kinnon, C., Hunt, D.M. et al. (2000) Restoration of photoreceptor ultrastructure and function in retinal degeneration slow mice by gene therapy. Nat. Genet., 25 306-310.
37. Acland, G.M., Aguirre, G.D., Ray, J., Zhang, Q., Aleman, T.S., Cideciyan, A.V., Pearce-Kelling, S.E., Anand, V., Zeng, Y., Maguire, A.M. et al. (2001) Gene therapy restores vision in a canine model of childhood blindness. Nat. Genet., 28, 92-95.
38. Acland, G.M., Aguirre, G.D., Bennett, J., Aleman, T.S., Cideciyan, A.V., Bennicelli, J., Dejneka, N.S., Pearce-Kelling, S.E., Maguire, A.M., Palczewski, K. et al. (2005) Long-term restoration of rod and cone vision by single dose rAAV-mediated gene transfer to the retina in a canine model of childhood blindness. Mol. Ther., 12, 1072-1082.
39. Lotery, A.J., Yang, G.S., Mullins, R.F., Russell, S.R., Schmidt, M., Edwin, E.M., Lindbloom, J.D., Chiorini, J.A., Kotin, R.M. and Davidson, B.L. (2003) Adeno-associated virus type 5: Transduction efficiency and cell type specificity in the primate retina. Hum. Gene Ther., 14, 1663-1671.
40. Olsson, J.E., Gordon, J.W., Pawlyk, B.S., Roof, D., Hayes, A., Molday, R.S., Mukai, S., Cowley, G.S., Berson, E.L. and Dryja, T.P. (1992) Transgenic mice with rhodopsin mutation (Pro23His): A mouse model of autosomal dominant retinitis pigmentosa. Neuron, 9, 815-830.
41. Cashman, S.M., Bowman, L., Christofferson, J. and Kumar-Singh, R. (2006) Inhibition of choroidal neovascularization by adenovirus-mediated delivery of short hairpin RNAs targeting VEGF as a potential therapy for AMD. Invest. Ophthal. Vis. Sci., 47, 3496-3504.
42. Illing, M.E., Rajan, R.S., Bence, N.F. and Kopito, R.R. (2002) A rhodopsin mutant linked to autosomal dominant retinitis pigmentosa is prone to aggregate and interacts with the ubiquitin proteasome system. J. Biol. Chem., 277, 34150-34160.
43. Rebello, G., Ramesar, R., Vorster, A., Roberts, L., Ehrenreich, L., Oppon, E., Gama, D., Bardien, S., Greenberg, J., Bonpapace et al. (2004) Apoptosis inducing signal sequence mutation in carbonic anhydrase IV indentified in patients with the RP17 form of retinitis pigmentosa. Proc. Natl. Acad. Sci. USA, 101, 6617-6622.
44. Zoghbi, H.Y. and Orr, H.T. (2000). Glutamine repeats and neurodegeneration. Annu. Rev. Neurosci., 23, 217-247.
45. Nakamura, K., Jeong, S.Y., Uchihara, T., Anno, M., Nagashima, K., Nagashima, T., Ikeda, S., Tsuji, S. and Kanazawa, I. (2001) SCA17, a novel autosomal dominant cerebellar ataxia caused by an expanded polyglutamine in TATA-binding protein. Hum. Mol. Genet., 10, 1441-1448.
46. Xia, H., Mao, Q., Eliason, S.L., Harper, S.Q., Martins, I.H., Orr, H.T., Paulson, H.L., Yang, L., Kotin, R.M. and Davidson, B.L. (2004) RNAi suppresses polyglutamine-induced neurodegeneration in a model of spinocerebellar ataxia. Nat. Med., 10, 816-820.
47. Zimmermann, A.G., Spychala, J. and Mitchell, B.S. (1995) Characterization of the human inosine-5′-monophosphate dehydrogenase type II gene. J. Biol. Chem., 270, 6808-6814.
48. Gu, J.J., Spychala, J and Mitchell, B.S. (1997) Regulation of the Human Inosine Monophosphate Dehydrogenase Type I Gene. J. Biol Chem., 272, 4458-4466.
49. Semizarov, D., Kroeger, P. and Fesik, S. (2004) siRNA-mediated gene silencing: A global genome view. Nucleic Acids Res., 32, 3838-3845.
50. Persengiev, S.P., Zhu, X. and Green, M.R. (2004) Nonspecific, concentration-dependent stimulation and repression of mammalian gene expression by small interfering RNAs (siRNAs). RNA, 10, 12-18.
51. Sledz, C.A., Hoiko, M., de Veer, M.J, Silverman, R.H. and Williams, B.R. (2003) Activation of the interferon system by short interfering RNAs. Nature Cell Biol., 5, 834-839.
52. Scacheri, P.C., Rozenblatt-Rosen, O., Caplen, N.J., Wolfsberg, T.G., Umayam, L., Lee, J.C., Hughes, C.M., Shanmugam, K.S., Bhattacharjee, A., Meryerson, M. et al. (2004) Short interfering RNAs can induce unexpected and divergent changes in the levels of untargeted proteins in mammalian cells. Proc. Natl. Acad. Sci. USA, 101, 1892-1897.
53. Saxena, S., Jonsson, Z.O. and Dutta, A. (2003) Small RNAs with imperfect match to endogenous mRNA repress translation. Implications for off target activity of small inhibitory RNA in mammalian cells. J. Biol. Chem., 278, 44312-44319.
54. Zeng, Y., Yi, R. and Cullen, BR. (2003) MicroRNAs and small interfering RNAs can inhibit mRNA expression by similar mechanisms. Proc. Natl. Acad. Sci. USA, 100, 9779-9784.
55. Jackson, A.L., Bartz, S.R., Schelter, J., Kobayashi, S.V., Burebard, J., Mao, M., Li, B., Cavet, G. and Linsley, P.S. (2003) Expression profiling reveals off target gene regulation by RNAi. Nat. Biotechnol., 21, 635-637.
56. Reinhart, B.J., Slack, F.J., Basson, M., Pasquinelli, A.E., Bettinger, J.C., Rougvie, A.E., Horvitz, H.R. and Ruvkun, G. (2000) The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature, 403, 901-6.
57. Brennecke, J., Stark, A., Russell, R.B. and Cohen, S.M. (2005) Priniciples of microRNA-target recognition. PLoS. Biol., 3, 404-418.
58. Kawasaki, H. and Taira, K. (2003) Hes1 is a target of microRNA-23 during retinoic-acid-induced neuronal differentiation of NT2 cells. Nature 423, 838-842.
59. Du, Q., Thonberg, H., Wang, J., Wablestedt, C. and Liang, Z. (2005) A systematic analysis of the silencing effects of an active siRNA at all single-nucleotide mismatched target sites. Nucleic Acids Res., 33, 1671-1677.
60. Doench, J.G. and Sharp, P.A. (2004) Specificity of microRNA target selection translational repression. Genes Dev., 18, 504-511.
61. Lin, X., Ruan, X., Anderson, M.G., McDowell, J.A., Kroeger, P.E., Fesik, S.W. and.Shen Y. (2005) siRNA-mediated off target gene silencing triggered by a 7 nucleotide complementation. Nucleic Acids Res., 33, 4527-4535.
62. Rolling, F. (2004) Recombinant AAV-mediated gene transfer to the retina: gene therapy perspectives. Gene Ther., 11, 26-32.
63. Grimm, D., Streetz, K.L., Jopling, C.L., Storm, T.A., Pandey, K., Davies, C.R., Marion, P., Salazar, F. and Kay, M.A. (2006) Fatality in mice due to oversaturation of cellular microRNA/short hairpin RNA pathways Nature, 441, 537-541.
64. Silva, J.M., Li, M.Z., Chang, K., Ge, W., Golding, M.C., Rickles, R.J., Siolas, D., Hu, G., Paddison, P.J., Schlabach, M.R. et al. (2006). Second-generation shRNA libraries covering the mouse and human genomes. Nat. Genet., 37, 1281 -1284.
65. Castanotto, D., Sakurai, K., Lingeman, R., Li, H., Shively, L., Aagaard. L., Soifer, R., Gatignol, A., Riggs, A. and Rossi, J.J. (2007) Combinatorial delivery of small interfering RNAs reduces RNAi efficacy by selective incorporation into RISC. Nuclei Acids Res., 35, 5154-5164.
66. Brummelkamp, T.R., Bernards, R. and Agami, R. (2002) A system for stable expression of short interfering RNAs in mammalian cells. Science, 296, 550-553
67. Rohr, U.P., Wulf, M.A., Stahn, S., Steidl, U., Haas, R. and Kronenwett, R. (2002) Fast and reliable titration of recombinant adeno-associated virus type-2 using quantitative real-time PCR. J. Virol. Methods, 106, 81-88.