The alu-rich genomic architecture of SPAST predisposes to diverse and functionally distinct disease-associated CNV alleles

American Journal of Human Genetics

Volumn 95, Issue 2, 2014, Pages 143-161

  Boone, Philip M ^a   Yuan, Bo ^a   Campbell, Ian M ^a   Scull, Jennifer C ^a   Withers, Marjorie A ^a   Baggett, Brett C ^a   Beck, Christine R ^a   Shaw, Christine J ^a   Stankiewicz, Pawel ^a   Moretti, Paolo ^a,b   Goodwin, Wendy E ^c   Hein, Nichole ^d   Fink, John K ^d,e,f   Seong, Moon Woo ^g   Seo, Soo Hyun ^g   Park, Sung Sup ^g   Karbassi, Izabela D ^h   Batish, Sat Dev ^h   Ordóñez Ugalde, Andrés ⁱ   Quintáns, Beatriz ⁱ   Sobrido, María Jesús ⁱ   Stemmler, Susanne ^j   Lupski, James R ^a,k   more..

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b MICHAEL E DEBAKEY VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c CHILDREN S MEDICAL CENTER   (United States)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^e Geriatric Research Education and Clinical Center   (United States)

^f VETERANS AFFAIRS MEDICAL CENTER   (United States)

^g Seoul National University Hospital   (South Korea)

^h QUEST DIAGNOSTICS NICHOLS INSTITUTE   (United States)

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

^j RUHR UNIVERSITY BOCHUM   (Germany)

^k TEXAS CHILDREN S HOSPITAL   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASES; ALU ELEMENTS; BASE SEQUENCE; CATION TRANSPORT PROTEINS; CELL LINE, TRANSFORMED; DNA COPY NUMBER VARIATIONS; GENOTYPE; HUMANS; PROTEIN ISOFORMS; RECOMBINANT FUSION PROTEINS; SEQUENCE ANALYSIS, DNA; SEQUENCE DELETION; SPASTIC PARAPLEGIA, HEREDITARY;

EID: 84905900217     PISSN: 00029297     EISSN: 15376605     Source Type: Journal    
DOI: 10.1016/j.ajhg.2014.06.014     Document Type: Article

References (68)

1. W. Wiszniewski, J.V. Hunter, N.A. Hanchard, J.R. Willer, C. Shaw, Q. Tian, A. Illner, X. Wang, S.W. Cheung, and A. Patel et al. TM4SF20 ancestral deletion and susceptibility to a pediatric disorder of early language delay and cerebral white matter hyperintensities Am. J. Hum. Genet. 93 2013 197 210
2. Y. Okamoto, M.T. Goksungur, D. Pehlivan, C.R. Beck, C. Gonzaga-Jauregui, D.M. Muzny, M.M. Atik, C.M.B. Carvalho, Z. Matur, and S. Bayraktar et al. Exonic duplication CNV of NDRG1 associated with autosomal-recessive HMSN-Lom/CMT4D Genet. Med. 16 2014 386 394
3. S. Benito-Sanz, J.L. Royo, E. Barroso, B. Paumard-Hernández, A.C. Barreda-Bonis, P. Liu, R. Gracía, J.R. Lupski, Á. Campos-Barros, J.L. Gómez-Skarmeta, and K.E. Heath Identification of the first recurrent PAR1 deletion in Léri-Weill dyschondrosteosis and idiopathic short stature reveals the presence of a novel SHOX enhancer J. Med. Genet. 49 2012 442 450
4. R. Hjeij, A. Lindstrand, R. Francis, M.A. Zariwala, X. Liu, Y. Li, R. Damerla, G.W. Dougherty, M. Abouhamed, and H. Olbrich et al. ARMC4 mutations cause primary ciliary dyskinesia with randomization of left/right body asymmetry Am. J. Hum. Genet. 93 2013 357 367
5. J.L. Loureiro, E. Brandão, L. Ruano, A.F. Brandão, A.M. Lopes, C. Thieleke-Matos, L. Miller-Fleming, V.T. Cruz, M. Barbosa, and I. Silveira et al. Autosomal dominant spastic paraplegias: a review of 89 families resulting from a portuguese survey JAMA Neurol. 70 2013 481 487
6. C. Depienne, E. Fedirko, S. Forlani, C. Cazeneuve, P. Ribaï, I. Feki, C. Tallaksen, K. Nguyen, B. Stankoff, and M. Ruberg et al. Exon deletions of SPG4 are a frequent cause of hereditary spastic paraplegia J. Med. Genet. 44 2007 281 284
7. H. Vandebona, N.P. Kerr, C. Liang, and C.M. Sue SPAST mutations in Australian patients with hereditary spastic paraplegia Intern. Med. J. 42 2012 1342 1347
8. C.J. McDermott, C.E. Burness, J. Kirby, L.E. Cox, D.G. Rao, C. Hewamadduma, B. Sharrack, M. Hadjivassiliou, P.F. Chinnery, A. Dalton, P.J. Shaw UK and Irish HSP Consortium Clinical features of hereditary spastic paraplegia due to spastin mutation Neurology 67 2006 45 51
9. V. Álvarez, E. Sánchez-Ferrero, C. Beetz, M. Díaz, B. Alonso, A.I. Corao, J. Gámez, J. Esteban, J.F. Gonzalo, S.I. Pascual-Pascual Group for the Study of the Genetics of Spastic Paraplegia Mutational spectrum of the SPG4 (SPAST) and SPG3A (ATL1) genes in Spanish patients with hereditary spastic paraplegia BMC Neurol. 10 2010 89
10. S. Sauter, B. Miterski, S. Klimpe, D. Bönsch, L. Schöls, A. Visbeck, T. Papke, H.C. Hopf, W. Engel, and T. Deufel et al. Mutation analysis of the spastin gene (SPG4) in patients in Germany with autosomal dominant hereditary spastic paraplegia Hum. Mutat. 20 2002 127 132
11. M. Mitne-Neto, F. Kok, C. Beetz, A. Pessoa, C. Bueno, Z. Graciani, M. Martyn, C.B.M. Monteiro, G. Mitne, and P. Hubert et al. A multi-exonic SPG4 duplication underlies sex-dependent penetrance of hereditary spastic paraplegia in a large Brazilian pedigree Eur. J. Hum. Genet. 15 2007 1276 1279
12. F. Zhang, W. Gu, M.E. Hurles, and J.R. Lupski Copy number variation in human health, disease, and evolution Annu. Rev. Genomics Hum. Genet. 10 2009 451 481
13. W. Gu, F. Zhang, and J.R. Lupski Mechanisms for human genomic rearrangements Pathogenetics 1 2008 4
14. P.M. Boone, P. Liu, F. Zhang, C.M.B. Carvalho, C.F. Towne, S.D. Batish, and J.R. Lupski Alu-specific microhomology-mediated deletion of the final exon of SPAST in three unrelated subjects with hereditary spastic paraplegia Genet. Med. 13 2011 582 592
15. P. Deininger Alu elements: know the SINEs Genome Biol. 12 2011 236
16. G. Franke, B. Bausch, M.M. Hoffmann, M. Cybulla, C. Wilhelm, J. Kohlhase, G. Scherer, and H.P.H. Neumann Alu-Alu recombination underlies the vast majority of large VHL germline deletions: Molecular characterization and genotype-phenotype correlations in VHL patients Hum. Mutat. 30 2009 776 786
17. M.A. Lehrman, W.J. Schneider, T.C. Südhof, M.S. Brown, J.L. Goldstein, and D.W. Russell Mutation in LDL receptor: Alu-Alu recombination deletes exons encoding transmembrane and cytoplasmic domains Science 227 1985 140 146
18. A.J. de Smith, R.G. Walters, L.J.M. Coin, I. Steinfeld, Z. Yakhini, R. Sladek, P. Froguel, and A.I.F. Blakemore Small deletion variants have stable breakpoints commonly associated with alu elements PLoS ONE 3 2008 e3104
19. D. Mei, R. Lewis, E. Parrini, L.P. Lazarou, C. Marini, D.T. Pilz, and R. Guerrini High frequency of genomic deletions - and a duplication - in the LIS1 gene in lissencephaly: implications for molecular diagnosis J. Med. Genet. 45 2008 355 361
20. P.L. Deininger, and M.A. Batzer Alu repeats and human disease Mol. Genet. Metab. 67 1999 183 193
21. M.P. Strout, G. Marcucci, C.D. Bloomfield, and M.A. Caligiuri The partial tandem duplication of ALL1 (MLL) is consistently generated by Alu-mediated homologous recombination in acute myeloid leukemia Proc. Natl. Acad. Sci. USA 95 1998 2390 2395
22. S.K. Sen, K. Han, J. Wang, J. Lee, H. Wang, P.A. Callinan, M. Dyer, R. Cordaux, P. Liang, and M.A. Batzer Human genomic deletions mediated by recombination between Alu elements Am. J. Hum. Genet. 79 2006 41 53
23. M. Babcock, A. Pavlicek, E. Spiteri, C.D. Kashork, I. Ioshikhes, L.G. Shaffer, J. Jurka, and B.E. Morrow Shuffling of genes within low-copy repeats on 22q11 (LCR22) by Alu-mediated recombination events during evolution Genome Res. 13 2003 2519 2532
24. Z. Szabó, S.A. Levi-Minzi, A.M. Christiano, C. Struminger, M. Stoneking, M.A. Batzer, and C.D. Boyd Sequential loss of two neighboring exons of the tropoelastin gene during primate evolution J. Mol. Evol. 49 1999 664 671
25. M.A. Batzer, and P.L. Deininger Alu repeats and human genomic diversity Nat. Rev. Genet. 3 2002 370 379
26. P.M. Boone, Z.T. Soens, I.M. Campbell, P. Stankiewicz, S.W. Cheung, A. Patel, A.L. Beaudet, S.E. Plon, C.A. Shaw, A.L. McGuire, and J.R. Lupski Incidental copy-number variants identified by routine genome testing in a clinical population Genet. Med. 15 2013 45 54
27. J. de Ligt, P.M. Boone, R. Pfundt, L.E.L.M. Vissers, T. Richmond, J. Geoghegan, K. O'Moore, N. de Leeuw, C. Shaw, and H.G. Brunner et al. Detection of clinically relevant copy number variants with whole-exome sequencing Hum. Mutat. 34 2013 1439 1448
28. H. Iwanaga, A. Tsujino, S. Shirabe, H. Eguchi, N. Fukushima, N. Niikawa, K. Yoshiura, and K. Eguchi Large deletion involving the 5′-UTR in the spastin gene caused mild phenotype of autosomal dominant hereditary spastic paraplegia Am. J. Med. Genet. A. 133A 2005 13 17
29. S. Salinas, C. Proukakis, A. Crosby, and T.T. Warner Hereditary spastic paraplegia: clinical features and pathogenetic mechanisms Lancet Neurol. 7 2008 1127 1138
30. J.E. Nielsen, B. Johnsen, P. Koefoed, K.H. Scheuer, M. Grønbech-Jensen, I. Law, K. Krabbe, A. Nørremølle, H. Eiberg, and H. Søndergård et al. Hereditary spastic paraplegia with cerebellar ataxia: a complex phenotype associated with a new SPG4 gene mutation Eur. J. Neurol. 11 2004 817 824
31. S. Murphy, G. Gorman, C. Beetz, P. Byrne, M. Dytko, P. McMonagle, K. Kinsella, M. Farrell, and M. Hutchinson Dementia in SPG4 hereditary spastic paraplegia: clinical, genetic, and neuropathologic evidence Neurology 73 2009 378 384
32. P. Ribaï, C. Depienne, E. Fedirko, A.-C. Jothy, C. Viveweger, V. Hahn-Barma, A. Brice, and A. Durr Mental deficiency in three families with SPG4 spastic paraplegia Eur. J. Hum. Genet. 16 2008 97 104
33. A.K. Erichsen, E. Inderhaug, M. Mattingsdal, K. Eiklid, and C.M.E. Tallaksen Seven novel mutations and four exon deletions in a collection of Norwegian patients with SPG4 hereditary spastic paraplegia Eur. J. Neurol. 14 2007 809 814
34. J.L. Smith, S. Xiong, W.R. Markesbery, and M.A. Lovell Altered expression of zinc transporters-4 and -6 in mild cognitive impairment, early and late Alzheimer's disease brain Neuroscience 140 2006 879 888
35. M.A. Lovell, J.L. Smith, and W.R. Markesbery Elevated zinc transporter-6 in mild cognitive impairment, Alzheimer disease, and pick disease J. Neuropathol. Exp. Neurol. 65 2006 489 498
36. K.D. White, P.G. Ince, M. Lusher, J. Lindsey, M. Cookson, R. Bashir, P.J. Shaw, and K.M. Bushby Clinical and pathologic findings in hereditary spastic paraparesis with spastin mutation Neurology 55 2000 89 94
37. C. Gonzaga-Jauregui, F. Zhang, C.F. Towne, S.D. Batish, and J.R. Lupski GJB1/Connexin 32 whole gene deletions in patients with X-linked Charcot-Marie-Tooth disease Neurogenetics 11 2010 465 470
38. P.M. Boone, C.A. Bacino, C.A. Shaw, P.A. Eng, P.M. Hixson, A.N. Pursley, S.-H.L. Kang, Y. Yang, J. Wiszniewska, and B.A. Nowakowska et al. Detection of clinically relevant exonic copy-number changes by array CGH Hum. Mutat. 31 2010 1326 1342
39. G.R. Abecasis, A. Auton, L.D. Brooks, M.A. DePristo, R.M. Durbin, R.E. Handsaker, H.M. Kang, G.T. Marth, G.A. McVean 1000 Genomes Project Consortium An integrated map of genetic variation from 1,092 human genomes Nature 491 2012 56 65
40. S. Miura, H. Shibata, H. Kida, K. Noda, T. Toyama, N. Iwasaki, A. Iwaki, M. Ayabe, H. Aizawa, T. Taniwaki, and Y. Fukumaki Partial SPAST and DPY30 deletions in a Japanese spastic paraplegia type 4 family Neurogenetics 12 2011 25 31
41. A. Sulek, E. Elert, M. Rajkiewicz, E. Zdzienicka, I. Stepniak, W. Krysa, and J. Zaremba Screening for the hereditary spastic paraplaegias SPG4 and SPG3A with the multiplex ligation-dependent probe amplification technique in a large population of affected individuals Neurol. Sci. 34 2013 239 242
42. S. Myers, C. Freeman, A. Auton, P. Donnelly, and G. McVean A common sequence motif associated with recombination hot spots and genome instability in humans Nat. Genet. 40 2008 1124 1129
43. M. Sasaki, J. Lange, and S. Keeney Genome destabilization by homologous recombination in the germ line Nat. Rev. Mol. Cell Biol. 11 2010 182 195
44. F. Baudat, J. Buard, C. Grey, A. Fledel-Alon, C. Ober, M. Przeworski, G. Coop, and B. de Massy PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice Science 327 2010 836 840
45. P. Liu, A. Erez, S.C.S. Nagamani, S.U. Dhar, K.E. Kołodziejska, A.V. Dharmadhikari, M.L. Cooper, J. Wiszniewska, F. Zhang, and M.A. Withers et al. Chromosome catastrophes involve replication mechanisms generating complex genomic rearrangements Cell 146 2011 889 903
46. M.J.L. Ligtenberg, R.P. Kuiper, T.L. Chan, M. Goossens, K.M. Hebeda, M. Voorendt, T.Y.H. Lee, D. Bodmer, E. Hoenselaar, and S.J.B. Hendriks-Cornelissen et al. Heritable somatic methylation and inactivation of MSH2 in families with Lynch syndrome due to deletion of the 3′ exons of TACSTD1 Nat. Genet. 41 2009 112 117
47. M. Shoukier, J. Neesen, S.M. Sauter, L. Argyriou, N. Doerwald, D.V.K. Pantakani, and A.U. Mannan Expansion of mutation spectrum, determination of mutation cluster regions and predictive structural classification of SPAST mutations in hereditary spastic paraplegia Eur. J. Hum. Genet. 17 2009 187 194
48. A. Aartsma-Rus Overview on DMD exon skipping Methods Mol. Biol. 867 2012 97 116
49. D.A. Wheeler, M. Srinivasan, M. Egholm, Y. Shen, L. Chen, A. McGuire, W. He, Y.-J. Chen, V. Makhijani, and G.T. Roth et al. The complete genome of an individual by massively parallel DNA sequencing Nature 452 2008 872 876
50. M.A. Lehrman, D.W. Russell, J.L. Goldstein, and M.S. Brown Alu-Alu recombination deletes splice acceptor sites and produces secreted low density lipoprotein receptor in a subject with familial hypercholesterolemia J. Biol. Chem. 262 1987 3354 3361
51. L.T. Reiter, P.J. Hastings, E. Nelis, P. De Jonghe, C. Van Broeckhoven, and J.R. Lupski Human meiotic recombination products revealed by sequencing a hotspot for homologous strand exchange in multiple HNPP deletion patients Am. J. Hum. Genet. 62 1998 1023 1033
52. A.B. Metzenberg, G. Wurzer, T.H.J. Huisman, and O. Smithies Homology requirements for unequal crossing over in humans Genetics 128 1991 143 161
53. D. Ottaviani, M. LeCain, and D. Sheer The role of microhomology in genomic structural variation Trends Genet. 30 2014 85 94
54. J.E. Haber Transpositions and translocations induced by site-specific double-strand breaks in budding yeast DNA Repair (Amst.) 5 2006 998 1009
55. F. Pâques, and J.E. Haber Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae Microbiol. Mol. Biol. Rev. 63 1999 349 404
56. B. Elliott, C. Richardson, and M. Jasin Chromosomal translocation mechanisms at intronic alu elements in mammalian cells Mol. Cell 17 2005 885 894
57. N. Sugawara, T. Goldfarb, B. Studamire, E. Alani, and J.E. Haber Heteroduplex rejection during single-strand annealing requires Sgs1 helicase and mismatch repair proteins Msh2 and Msh6 but not Pms1 Proc. Natl. Acad. Sci. USA 101 2004 9315 9320
58. C. Mézard, D. Pompon, and A. Nicolas Recombination between similar but not identical DNA sequences during yeast transformation occurs within short stretches of identity Cell 70 1992 659 670
59. D. Yang, and A.S. Waldman Fine-resolution analysis of products of intrachromosomal homeologous recombination in mammalian cells Mol. Cell. Biol. 17 1997 3614 3628
60. A.M. Bailis, and R. Rothstein A defect in mismatch repair in Saccharomyces cerevisiae stimulates ectopic recombination between homeologous genes by an excision repair dependent process Genetics 126 1990 535 547
61. L.C. Rossetti, A. Goodeve, I.B. Larripa, and C.D. De Brasi Homeologous recombination between AluSx-sequences as a cause of hemophilia Hum. Mutat. 24 2004 440
62. P. Dittwald, T. Gambin, P. Szafranski, J. Li, S. Amato, M.Y. Divon, L.X. Rodríguez Rojas, L.E. Elton, D.A. Scott, and C.P. Schaaf et al. NAHR-mediated copy-number variants in a clinical population: mechanistic insights into both genomic disorders and Mendelizing traits Genome Res. 23 2013 1395 1409
63. A.S. Waldman, and R.M. Liskay Differential effects of base-pair mismatch on intrachromosomal versus extrachromosomal recombination in mouse cells Proc. Natl. Acad. Sci. USA 84 1987 5340 5344
64. E. Lieberman-Aiden, N.L. van Berkum, L. Williams, M. Imakaev, T. Ragoczy, A. Telling, I. Amit, B.R. Lajoie, P.J. Sabo, and M.O. Dorschner et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome Science 326 2009 289 293
65. G. Fudenberg, G. Getz, M. Meyerson, and L.A. Mirny High order chromatin architecture shapes the landscape of chromosomal alterations in cancer Nat. Biotechnol. 29 2011 1109 1113
66. N. Naumova, M. Imakaev, G. Fudenberg, Y. Zhan, B.R. Lajoie, L.A. Mirny, and J. Dekker Organization of the mitotic chromosome Science 342 2013 948 953
67. A.I. Bush The metal theory of Alzheimer's disease J. Alzheimers Dis. 33 Suppl 1 2013 S277 S281
68. R.P. Kuiper, L.E.L.M. Vissers, R. Venkatachalam, D. Bodmer, E. Hoenselaar, M. Goossens, A. Haufe, E. Kamping, R.C. Niessen, and F.B.L. Hogervorst et al. Recurrence and variability of germline EPCAM deletions in Lynch syndrome Hum. Mutat. 32 2011 407 414