Correct mRNA processing at a mutant TT splice donor in FANCC ameliorates the clinical phenotype in patients and is enhanced by delivery of suppressor U1 snRNAs

American Journal of Human Genetics

Volumn 87, Issue 4, 2010, Pages 480-493

  Hartmann, Linda ^a   Neveling, Kornelia ^b   Borkens, Stephanie ^a   Schneider, Hildegard ^a   Freund, Marcel ^a   Grassman, Elke ^c   Theiss, Stephan ^d   Wawer, Angela ^e   Burdach, Stefan ^e   Auerbach, Arleen D ^f   Schindler, Detlev ^b   Hanenberg, Helmut ^a,g   Schaal, Heiner ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^d Result GmbH   (Germany)

^e TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^f ROCKEFELLER UNIVERSITY   (United States)

^g INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FANCONI ANEMIA GROUP A PROTEIN; FANCONI ANEMIA GROUP C PROTEIN; FANCONI ANEMIA GROUP D2 PROTEIN; FANCONI ANEMIA GROUP E PROTEIN; FANCONI ANEMIA GROUP F PROTEIN; FANCONI ANEMIA GROUP G PROTEIN; LENTIVIRUS VECTOR; MESSENGER RNA; SMALL NUCLEAR RNA; FANCC PROTEIN, HUMAN; RNA SPLICING; U1 SMALL NUCLEAR RNA;

ARTICLE; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CELL STRAIN HEK293; CLINICAL ARTICLE; FANCONI ANEMIA; FEMALE; FIBROBLAST; HELA CELL; HUMAN; IMMUNOBLOTTING; MALE; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SPLICING; SITE DIRECTED MUTAGENESIS; VIRAL GENE THERAPY; GENE THERAPY; GENE VECTOR; GENETICS; LENTIVIRINAE; METABOLISM; MUTATION; PATHOLOGY; PEDIGREE; PHYSIOLOGY; PROCEDURES; RNA PROCESSING;

FANCONI ANEMIA; FANCONI ANEMIA COMPLEMENTATION GROUP C PROTEIN; G2 PHASE; GENE THERAPY; GENETIC VECTORS; HUMANS; LENTIVIRUS; MUTATION; PEDIGREE; PHENOTYPE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA SPLICE SITES; RNA, MESSENGER; RNA, SMALL NUCLEAR; GENETIC THERAPY;

EID: 77957749244     PISSN: 00029297     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ajhg.2010.08.016     Document Type: Article

References (80)

1. W. Wang Emergence of a DNA-damage response network consisting of Fanconi anaemia and BRCA proteins Nat. Rev. Genet. 8 2007 735 748
2. J.P. de Winter, and H. Joenje The genetic and molecular basis of Fanconi anemia Mutat. Res. 668 2009 11 19
3. G.L. Moldovan, and A.D. D'Andrea How the fanconi anemia pathway guards the genome Annu. Rev. Genet. 43 2009 223 249
4. D.I. Kutler, B. Singh, J. Satagopan, S.D. Batish, M. Berwick, P.F. Giampietro, H. Hanenberg, and A.D. Auerbach A 20-year perspective on the International Fanconi Anemia Registry (IFAR) Blood 101 2003 1249 1256
5. A.M. Green, and G.M. Kupfer Fanconi anemia Hematol. Oncol. Clin. North Am. 23 2009 193 214
6. K. Neveling, D. Endt, H. Hoehn, and D. Schindler Genotype-phenotype correlations in Fanconi anemia Mutat. Res. 668 2009 73 91
7. F.O. Pinto, T. Leblanc, D. Chamousset, G. Le Roux, B. Brethon, B. Cassinat, J. Larghero, J.P. de Villartay, D. Stoppa-Lyonnet, and A. Baruchel Diagnosis of Fanconi anemia in patients with bone marrow failure Haematologica 94 2009 487 495
8. A.D. Auerbach Fanconi anemia and its diagnosis Mutat. Res. 668 2009 4 10
9. A.D. Auerbach Fanconi anemia diagnosis and the diepoxybutane (DEB) test Exp. Hematol. 21 1993 731 733
10. H. Seyschab, R. Friedl, Y. Sun, D. Schindler, H. Hoehn, S. Hentze, and T. Schroeder-Kurth Comparative evaluation of diepoxybutane sensitivity and cell cycle blockage in the diagnosis of Fanconi anemia Blood 85 1995 2233 2237
11. D. Schindler, R. Friedl, I. Gavvovidis, R. Kalb, K. Neveling, Y. Linka, H. Hanenberg, M. Kubbies, and H. Hoehn Application of cell cycle testing in Fanconi anemia D. Schindler, H. Hoehn, Fanconi Anemia: A Paradigmatic Disease for the Understanding of Cancer and Aging 2007 Karger Basel 110 130
12. A.F. Alpi, and K.J. Patel Monoubiquitylation in the Fanconi anemia DNA damage response pathway DNA Repair (Amst.) 8 2009 430 435
13. M. Ishiai, H. Kitao, A. Smogorzewska, J. Tomida, A. Kinomura, E. Uchida, A. Saberi, E. Kinoshita, E. Kinoshita-Kikuta, and T. Koike FANCI phosphorylation functions as a molecular switch to turn on the Fanconi anemia pathway Nat. Struct. Mol. Biol. 15 2008 1138 1146
14. P. Knipscheer, M. Räschle, A. Smogorzewska, M. Enoiu, T.V. Ho, O.D. Schärer, S.J. Elledge, and J.C. Walter The Fanconi anemia pathway promotes replication-dependent DNA interstrand cross-link repair Science 326 2009 1698 1701
15. A.E. Sims, E. Spiteri, R.J. Sims 3rd, A.G. Arita, F.P. Lach, T. Landers, M. Wurm, M. Freund, K. Neveling, and H. Hanenberg FANCI is a second monoubiquitinated member of the Fanconi anemia pathway Nat. Struct. Mol. Biol. 14 2007 564 567
16. J.C. Dorsman, M. Levitus, D. Rockx, M.A. Rooimans, A.B. Oostra, A. Haitjema, S.T. Bakker, J. Steltenpool, D. Schuler, and S. Mohan Identification of the Fanconi anemia complementation group I gene, FANCI Cell. Oncol. 29 2007 211 218
17. A. Smogorzewska, S. Matsuoka, P. Vinciguerra, E.R. McDonald 3rd, K.E. Hurov, J. Luo, B.A. Ballif, S.P. Gygi, K. Hofmann, A.D. D'Andrea, and S.J. Elledge Identification of the FANCI protein, a monoubiquitinated FANCD2 paralog required for DNA repair Cell 129 2007 289 301
18. F. Yuan, J. El Hokayem, W. Zhou, and Y. Zhang FANCI protein binds to DNA and interacts with FANCD2 to recognize branched structures J. Biol. Chem. 284 2009 24443 24452
19. R. Kalb, K. Neveling, H. Hoehn, H. Schneider, Y. Linka, S.D. Batish, C. Hunt, M. Berwick, E. Callen, and J. Surralles Hypomorphic mutations in the gene encoding a key Fanconi anemia protein, FANCD2, sustain a significant group of FA-D2 patients with severe phenotype Am. J. Hum. Genet. 80 2007 895 910
20. N.G. Howlett, T. Taniguchi, S. Olson, B. Cox, Q. Waisfisz, C. De Die-Smulders, N. Persky, M. Grompe, H. Joenje, and G. Pals Biallelic inactivation of BRCA2 in Fanconi anemia Science 297 2002 606 609
21. S. Reid, D. Schindler, H. Hanenberg, K. Barker, S. Hanks, R. Kalb, K. Neveling, P. Kelly, S. Seal, and M. Freund Biallelic mutations in PALB2 cause Fanconi anemia subtype FA-N and predispose to childhood cancer Nat. Genet. 39 2007 162 164
22. O. Levran, C. Attwooll, R.T. Henry, K.L. Milton, K. Neveling, P. Rio, S.D. Batish, R. Kalb, E. Velleuer, and S. Barral The BRCA1-interacting helicase BRIP1 is deficient in Fanconi anemia Nat. Genet. 37 2005 931 933
23. T.R. Singh, S.T. Bakker, S. Agarwal, M. Jansen, E. Grassman, B.C. Godthelp, A.M. Ali, C.H. Du, M.A. Rooimans, and Q. Fan Impaired FANCD2 monoubiquitination and hypersensitivity to camptothecin uniquely characterize Fanconi anemia complementation group M Blood 114 2009 174 180
24. K. Offit, O. Levran, B. Mullaney, K. Mah, K. Nafa, S.D. Batish, R. Diotti, H. Schneider, A. Deffenbaugh, and T. Scholl Shared genetic susceptibility to breast cancer, brain tumors, and Fanconi anemia J. Natl. Cancer Inst. 95 2003 1548 1551
25. J.E. Wagner, J. Tolar, O. Levran, T. Scholl, A. Deffenbaugh, J. Satagopan, L. Ben-Porat, K. Mah, S.D. Batish, and D.I. Kutler Germline mutations in BRCA2: Shared genetic susceptibility to breast cancer, early onset leukemia, and Fanconi anemia Blood 103 2004 3226 3229
26. F. Vaz, H. Hanenberg, B. Schuster, K. Barker, C. Wiek, V. Erven, K. Neveling, D. Endt, I. Kesterton, and F. Autore Mutation of the RAD51C gene in a Fanconi anemia-like disorder Nat. Genet. 42 2010 406 409
27. A.P. Gillio, P.C. Verlander, S.D. Batish, P.F. Giampietro, and A.D. Auerbach Phenotypic consequences of mutations in the Fanconi anemia FAC gene: An International Fanconi Anemia Registry study Blood 90 1997 105 110
28. T. Yamashita, N. Wu, G. Kupfer, C. Corless, H. Joenje, M. Grompe, and A.D. D'Andrea Clinical variability of Fanconi anemia (type C) results from expression of an amino terminal truncated Fanconi anemia complementation group C polypeptide with partial activity Blood 87 1996 4424 4432
29. M. Futaki, T. Yamashita, H. Yagasaki, T. Toda, M. Yabe, S. Kato, S. Asano, and T. Nakahata The IVS4 + 4 A to T mutation of the fanconi anemia gene FANCC is not associated with a severe phenotype in Japanese patients Blood 95 2000 1493 1498
30. A. Tachibana, T. Kato, Y. Ejima, T. Yamada, T. Shimizu, L. Yang, Y. Tsunematsu, and M.S. Sasaki The FANCA gene in Japanese Fanconi anemia: Reports of eight novel mutations and analysis of sequence variability Hum. Mutat. 13 1999 237 244
31. I. Demuth, M. Wlodarski, A.J. Tipping, N.V. Morgan, J.P. de Winter, M. Thiel, S. Gräsl, D. Schindler, A.D. D'Andrea, and C. Altay Spectrum of mutations in the Fanconi anaemia group G gene, FANCG/XRCC9 Eur. J. Hum. Genet. 8 2000 861 868
32. T. Yamada, A. Tachibana, T. Shimizu, H. Mugishima, M. Okubo, and M.S. Sasaki Novel mutations of the FANCG gene causing alternative splicing in Japanese Fanconi anemia J. Hum. Genet. 45 2000 159 166
33. O. Levran, R. Diotti, K. Pujara, S.D. Batish, H. Hanenberg, and A.D. Auerbach Spectrum of sequence variations in the FANCA gene: An International Fanconi Anemia Registry (IFAR) study Hum. Mutat. 25 2005 142 149
34. L. Faivre, P. Guardiola, C. Lewis, I. Dokal, W. Ebell, A. Zatterale, C. Altay, J. Poole, D. Stones, M.L. Kwee European Fanconi Anemia Research Group Association of complementation group and mutation type with clinical outcome in fanconi anemia Blood 96 2000 4064 4070
35. K. Huck, H. Hanenberg, S. Gudowius, R. Fenk, R. Kalb, K. Neveling, B. Betz, D. Niederacher, R. Haas, and U. Göbel Delayed diagnosis and complications of Fanconi anaemia at advanced age - A paradigm Br. J. Haematol. 133 2006 188 197
36. R.C. Cumming, J. Lightfoot, K. Beard, H. Youssoufian, P.J. O'Brien, and M. Buchwald Fanconi anemia group C protein prevents apoptosis in hematopoietic cells through redox regulation of GSTP1 Nat. Med. 7 2001 814 820
37. S.M. Davies, G.A. Radloff, T.E. DeFor, O. Levran, S.D. Batish, H. Hanenberg, and A.D. Auerbach GST genotype may modify clinical phenotype in patients with Fanconi anaemia Br. J. Haematol. 131 2005 118 122
38. M. Burset, I.A. Seledtsov, and V.V. Solovyev Analysis of canonical and non-canonical splice sites in mammalian genomes Nucleic Acids Res. 28 2000 4364 4375
39. M. Burset, I.A. Seledtsov, and V.V. Solovyev SpliceDB: Database of canonical and non-canonical mammalian splice sites Nucleic Acids Res. 29 2001 255 259
40. M.C. Wahl, C.L. Will, and R. Lührmann The spliceosome: Design principles of a dynamic RNP machine Cell 136 2009 701 718
41. S.L. Hall, and R.A. Padgett Requirement of U12 snRNA for in vivo splicing of a minor class of eukaryotic nuclear pre-mRNA introns Science 271 1996 1716 1718
42. W.Y. Tarn, and J.A. Steitz Highly diverged U4 and U6 small nuclear RNAs required for splicing rare AT-AC introns Science 273 1996 1824 1832
43. W.Y. Tarn, and J.A. Steitz A novel spliceosome containing U11, U12, and U5 snRNPs excises a minor class (AT-AC) intron in vitro Cell 84 1996 801 811
44. M. Krawczak, N.S. Thomas, B. Hundrieser, M. Mort, M. Wittig, J. Hampe, and D.N. Cooper Single base-pair substitutions in exon-intron junctions of human genes: Nature, distribution, and consequences for mRNA splicing Hum. Mutat. 28 2007 150 158
45. X. Roca, A.J. Olson, A.R. Rao, E. Enerly, V.N. Kristensen, A.L. Børresen-Dale, B.S. Andresen, A.R. Krainer, and R. Sachidanandam Features of 5′-splice-site efficiency derived from disease-causing mutations and comparative genomics Genome Res. 18 2008 77 87
46. S. Kammler, C. Leurs, M. Freund, J. Krummheuer, K. Seidel, T.O. Tange, M.K. Lund, J. Kjems, A. Scheid, and H. Schaal The sequence complementarity between HIV-1 5′ splice site SD4 and U1 snRNA determines the steady-state level of an unstable env pre-mRNA RNA 7 2001 421 434
47. M. Freund, C. Asang, S. Kammler, C. Konermann, J. Krummheuer, M. Hipp, I. Meyer, W. Gierling, S. Theiss, and T. Preuss A novel approach to describe a U1 snRNA binding site Nucleic Acids Res. 31 2003 6963 6975
48. Y. Zhuang, and A.M. Weiner A compensatory base change in U1 snRNA suppresses a 5′ splice site mutation Cell 46 1986 827 835
49. M. Pinotti, L. Rizzotto, D. Balestra, M.A. Lewandowska, N. Cavallari, G. Marchetti, F. Bernardi, and F. Pagani U1-snRNA-mediated rescue of mRNA processing in severe factor VII deficiency Blood 111 2008 2681 2684
50. M. Pinotti, D. Balestra, L. Rizzotto, I. Maestri, F. Pagani, and F. Bernardi Rescue of coagulation factor VII function by the U1+5A snRNA Blood 113 2009 6461 6464
51. G. Tanner, E. Glaus, D. Barthelmes, M. Ader, J. Fleischhauer, F. Pagani, W. Berger, and J. Neidhardt Therapeutic strategy to rescue mutation-induced exon skipping in rhodopsin by adaptation of U1 snRNA Hum. Mutat. 30 2009 255 263
52. D.B. Kohn, and F. Candotti Gene therapy fulfilling its promise N. Engl. J. Med. 360 2009 518 521
53. G. Vassilopoulos, and A. Rethwilm The usefulness of a perfect parasite Gene Ther. 15 2008 1299 1301
54. D.A. Williams Foamy virus vectors come of age Mol. Ther. 16 2008 635 636
55. H. Hanenberg, X.L. Xiao, D. Dilloo, K. Hashino, I. Kato, and D.A. Williams Colocalization of retrovirus and target cells on specific fibronectin fragments increases genetic transduction of mammalian cells Nat. Med. 2 1996 876 882
56. H. Hanenberg, K. Hashino, H. Konishi, R.A. Hock, I. Kato, and D.A. Williams Optimization of fibronectin-assisted retroviral gene transfer into human CD34+ hematopoietic cells Hum. Gene Ther. 8 1997 2193 2206
57. H. Hanenberg, S.D. Batish, K.E. Pollok, L. Vieten, P.C. Verlander, C. Leurs, R.J. Cooper, K. Göttsche, L. Haneline, and D.W. Clapp Phenotypic correction of primary Fanconi anemia T cells with retroviral vectors as a diagnostic tool Exp. Hematol. 30 2002 410 420
58. S. Chandra, O. Levran, I. Jurickova, C. Maas, R. Kapur, D. Schindler, R. Henry, K. Milton, S.D. Batish, and J.A. Cancelas A rapid method for retrovirus-mediated identification of complementation groups in Fanconi anemia patients Mol. Ther. 12 2005 976 984
59. P.C. Verlander, J.D. Lin, M.U. Udono, Q. Zhang, R.A. Gibson, C.G. Mathew, and A.D. Auerbach Mutation analysis of the Fanconi anemia gene FACC Am. J. Hum. Genet. 54 1994 595 601
60. B. Betz, S. Theiss, M. Aktas, C. Konermann, T.O. Goecke, G. Moslein, H. Schaal, and B. Royer-Pokora Comparative in silico analyses and experimental validation of novel splice site and missense mutations in the genes MLH1 and MSH2 J. Cancer Res. Clin. Oncol. 136 2010 123 134
61. S. Kammler, M. Otte, I. Hauber, J. Kjems, J. Hauber, and H. Schaal The strength of the HIV-1 3′ splice sites affects Rev function Retrovirology 3 2006 89
62. H. Schaal, M. Klein, P. Gehrmann, O. Adams, and A. Scheid Requirement of N-terminal amino acid residues of gp41 for human immunodeficiency virus type 1-mediated cell fusion J. Virol. 69 1995 3308 3314
63. P.J. Maddon, A.G. Dalgleish, J.S. McDougal, P.R. Clapham, R.A. Weiss, and R. Axel The T4 gene encodes the AIDS virus receptor and is expressed in the immune system and the brain Cell 47 1986 333 348
64. R.F. Selden, K.B. Howie, M.E. Rowe, H.M. Goodman, and D.D. Moore Human growth hormone as a reporter gene in regulation studies employing transient gene expression Mol. Cell. Biol. 6 1986 3173 3179
65. D. Schindler, and H. Hoehn Fanconi anemia mutation causes cellular susceptibility to ambient oxygen Am. J. Hum. Genet. 43 1988 429 435
66. H. Mochizuki, J.P. Schwartz, K. Tanaka, R.O. Brady, and J. Reiser High-titer human immunodeficiency virus type 1-based vector systems for gene delivery into nondividing cells J. Virol. 72 1998 8873 8883
67. T. Pietschmann, M. Heinkelein, M. Heldmann, H. Zentgraf, A. Rethwilm, and D. Lindemann Foamy virus capsids require the cognate envelope protein for particle export J. Virol. 73 1999 2613 2621
68. L. Hartmann, S. Theiss, D. Niederacher, and H. Schaal Diagnostics of pathogenic splicing mutations: Does bioinformatics cover all bases? Front. Biosci. 13 2008 3252 3272
69. I. Garcia-Higuera, T. Taniguchi, S. Ganesan, M.S. Meyn, C. Timmers, J. Hejna, M. Grompe, and A.D. D'Andrea Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway Mol. Cell 7 2001 249 262
70. X. Roca, and A.R. Krainer Recognition of atypical 5′ splice sites by shifted base-pairing to U1 snRNA Nat. Struct. Mol. Biol. 16 2009 176 182
71. M. Aebi, H. Hornig, and C. Weissmann 5′ cleavage site in eukaryotic pre-mRNA splicing is determined by the overall 5′ splice region, not by the conserved 5′ GU Cell 50 1987 237 246
72. C. Kyriakopoulou, P. Larsson, L. Liu, J. Schuster, F. Söderbom, L.A. Kirsebom, and A. Virtanen U1-like snRNAs lacking complementarity to canonical 5′ splice sites RNA 12 2006 1603 1611
73. H. Popp, R. Kalb, A. Fischer, S. Lobitz, I. Kokemohr, H. Hanenberg, and D. Schindler Screening Fanconi anemia lymphoid cell lines of non-A, C, D2, E, F, G subtypes for defects in BRCA2/FANCD1 Cytogenet. Genome Res. 103 2003 54 57
74. K. Meyer, J. Marquis, J. Trüb, R. Nlend Nlend, S. Verp, M.D. Ruepp, H. Imboden, I. Barde, D. Trono, and D. Schümperli Rescue of a severe mouse model for spinal muscular atrophy by U7 snRNA-mediated splicing modulation Hum. Mol. Genet. 18 2009 546 555
75. J.W. Bainbridge, A.J. Smith, S.S. Barker, S. Robbie, R. Henderson, K. Balaggan, A. Viswanathan, G.E. Holder, A. Stockman, and N. Tyler Effect of gene therapy on visual function in Leber's congenital amaurosis N. Engl. J. Med. 358 2008 2231 2239
76. A. Aiuti, and M.G. Roncarolo Ten years of gene therapy for primary immune deficiencies Hematology Am. Soc. Hematol. Educ. Program 2009 2009 682 689
77. J. Marquis, K. Meyer, L. Angehrn, S.S. Kämpfer, B. Rothen-Rutishauser, and D. Schümperli Spinal muscular atrophy: SMN2 pre-mRNA splicing corrected by a U7 snRNA derivative carrying a splicing enhancer sequence Mol. Ther. 15 2007 1479 1486
78. C. Timmers, T. Taniguchi, J. Hejna, C. Reifsteck, L. Lucas, D. Bruun, M. Thayer, B. Cox, S. Olson, and A.D. D'Andrea Positional cloning of a novel Fanconi anemia gene, FANCD2 Mol. Cell 7 2001 241 248
79. N. Sandoval, M. Platzer, A. Rosenthal, T. Dörk, R. Bendix, B. Skawran, M. Stuhrmann, R.D. Wegner, K. Sperling, and S. Banin Characterization of ATM gene mutations in 66 ataxia telangiectasia families Hum. Mol. Genet. 8 1999 69 79
80. K. Wimmer, X. Roca, H. Beiglböck, T. Callens, J. Etzler, A.R. Rao, A.R. Krainer, C. Fonatsch, and L. Messiaen Extensive in silico analysis of NF1 splicing defects uncovers determinants for splicing outcome upon 5′ splice-site disruption Hum. Mutat. 28 2007 599 612