Mechanisms for Nonrecurrent Genomic Rearrangements Associated with CMT1A or HNPP: Rare CNVs as a Cause for Missing Heritability

American Journal of Human Genetics

Volumn 86, Issue 6, 2010, Pages 892-903

  Zhang, Feng ^a,b   Seeman, Pavel ^c   Liu, Pengfei ^a   Weterman, Marian A J ^d   Gonzaga Jauregui, Claudia ^a   Towne, Charles F ^e   Batish, Sat Dev ^e   De Vriendt, Els ^f   De Jonghe, Peter ^f   Rautenstrauss, Bernd ^g,h   Krause, Klaus Henning ^h   Khajavi, Mehrdad ^a   Posadka, Jan ^c   Vandenberghe, Antoon ⁱ   Palau, Francesc ^j   Van Maldergem, Lionel ^k   Baas, Frank ^d   Timmerman, Vincent ^f   Lupski, James R ^a,l  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b FUDAN UNIVERSITY   (China)

^c CHARLES UNIVERSITY   (Czech Republic)

^d ACADEMIC MEDICAL CENTER   (Netherlands)

^e ATHENA DIAGNOSTICS INC   (United States)

^f UNIVERSITY OF ANTWERP   (Belgium)

^g Medical Genetic Center   (Germany)

^h LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

ⁱ Biomnis Inc   (France)

^j INSTITUTO DE BIOMEDICINA DE VALENCIA   (Spain)

^k UNIVERSITY OF LIÈGE   (Belgium)

^l TEXAS CHILDREN S HOSPITAL   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

OLIGONUCLEOTIDE; PERIPHERAL MYELIN PROTEIN 22;

ALU SEQUENCE; ARTICLE; CHARCOT MARIE TOOTH DISEASE TYPE 1A; CHROMOSOME 17P; CHROMOSOME BREAKAGE; CLINICAL ARTICLE; COMPARATIVE GENOMIC HYBRIDIZATION; COPY NUMBER VARIATION; DISEASE ASSOCIATION; EXON; FEMALE; GENE DELETION; GENE DUPLICATION; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCATION; GENE REARRANGEMENT; GENE REPLICATION; GENE SEQUENCE; GENE STRUCTURE; GENETIC ANALYSIS; GENOME SIZE; HEREDITARY MOTOR SENSORY NEUROPATHY; HEREDITARY NEUROPATHY WITH LIABILITY TO PRESSURE PALSIES; HERITABILITY; HOMOLOGOUS RECOMBINATION; HUMAN; MOLECULAR MECHANICS; NEUROPATHY; PHENOTYPE; PRIORITY JOURNAL;

CHARCOT-MARIE-TOOTH DISEASE; CHROMOSOMES, HUMAN, PAIR 17; COMPARATIVE GENOMIC HYBRIDIZATION; DNA COPY NUMBER VARIATIONS; GENE DELETION; GENE DUPLICATION; HEREDITARY SENSORY AND MOTOR NEUROPATHY; HUMANS; MYELIN PROTEINS; PARALYSIS; TRANSLOCATION, GENETIC;

EID: 77953232121     PISSN: 00029297     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ajhg.2010.05.001     Document Type: Article

References (54)

1. Lupski J.R. Genomic disorders: Structural features of the genome can lead to DNA rearrangements and human disease traits. Trends Genet. 14 (1998) 417-422
2. Stankiewicz P., and Lupski J.R. Genome architecture, rearrangements and genomic disorders. Trends Genet. 18 (2002) 74-82
3. Lupski J.R. Genomic disorders ten years on. Genome Med. 1 (2009) 42
4. Lupski J.R., de Oca-Luna R.M., Slaugenhaupt S., Pentao L., Guzzetta V., Trask B.J., Saucedo-Cardenas O., Barker D.F., Killian J.M., Garcia C.A., et al. DNA duplication associated with Charcot-Marie-Tooth disease type 1A. Cell 66 (1991) 219-232
5. Chance P.F., Alderson M.K., Leppig K.A., Lensch M.W., Matsunami N., Smith B., Swanson P.D., Odelberg S.J., Disteche C.M., and Bird T.D. DNA deletion associated with hereditary neuropathy with liability to pressure palsies. Cell 72 (1993) 143-151
6. Raeymaekers P., Timmerman V., Nelis E., De Jonghe P., Hoogendijk J.E., Baas F., Barker D.F., Martin J.J., De Visser M., Bolhuis P.A., et al. Duplication in chromosome 17p11.2 in Charcot-Marie-Tooth neuropathy type 1a (CMT 1a). Neuromuscul. Disord. 1 (1991) 93-97
7. Lupski J.R., and Chance P.F. Hereditary motor and sensory neuropathies involving altered dosage or mutation of PMP22: The CMT1A duplication and HNPP deletion. In: Dyck P.J., and Thomas P.K. (Eds). Peripheral Neuropathy (2005), Elsevier Science, Philadelphia 1659-1680
8. Lupski J.R., Wise C.A., Kuwano A., Pentao L., Parke J.T., Glaze D.G., Ledbetter D.H., Greenberg F., and Patel P.I. Gene dosage is a mechanism for Charcot-Marie-Tooth disease type 1A. Nat. Genet. 1 (1992) 29-33
9. Gu W., Zhang F., and Lupski J.R. Mechanisms for human genomic rearrangements. PathoGenetics 1 (2008) 4
10. Turner D.J., Miretti M., Rajan D., Fiegler H., Carter N.P., Blayney M.L., Beck S., and Hurles M.E. Germline rates of de novo meiotic deletions and duplications causing several genomic disorders. Nat. Genet. 40 (2008) 90-95
11. Bailey J.A., Gu Z., Clark R.A., Reinert K., Samonte R.V., Schwartz S., Adams M.D., Myers E.W., Li P.W., and Eichler E.E. Recent segmental duplications in the human genome. Science 297 (2002) 1003-1007
12. Pentao L., Wise C.A., Chinault A.C., Patel P.I., and Lupski J.R. Charcot-Marie-Tooth type 1A duplication appears to arise from recombination at repeat sequences flanking the 1.5 Mb monomer unit. Nat. Genet. 2 (1992) 292-300
13. Reiter L.T., Murakami T., Koeuth T., Gibbs R.A., and Lupski J.R. The human COX10 gene is disrupted during homologous recombination between the 24 kb proximal and distal CMT1A-REPs. Hum. Mol. Genet. 6 (1997) 1595-1603
14. Reiter L.T., Hastings P.J., Nelis E., De Jonghe P., Van Broeckhoven C., and Lupski J.R. 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
15. Valentijn L.J., Baas F., Wolterman R.A., Hoogendijk J.E., van den Bosch N.H., Zorn I., Gabreels-Festen A.W., de Visser M., and Bolhuis P.A. Identical point mutations of PMP-22 in Trembler-J mouse and Charcot-Marie-Tooth disease type 1A. Nat. Genet. 2 (1992) 288-291
16. Patel P.I., Roa B.B., Welcher A.A., Schoener-Scott R., Trask B.J., Pentao L., Snipes G.J., Garcia C.A., Francke U., Shooter E.M., et al. The gene for the peripheral myelin protein PMP-22 is a candidate for Charcot-Marie-Tooth disease type 1A. Nat. Genet. 1 (1992) 159-165
17. Timmerman V., Nelis E., Van Hul W., Nieuwenhuijsen B.W., Chen K.L., Wang S., Ben Othman K., Cullen B., Leach R.J., Hanemann C.O., et al. The peripheral myelin protein gene PMP-22 is contained within the Charcot-Marie-Tooth disease type 1A duplication. Nat. Genet. 1 (1992) 171-175
18. Valentijn L.J., Bolhuis P.A., Zorn I., Hoogendijk J.E., van den Bosch N., Hensels G.W., Stanton Jr. V.P., Housman D.E., Fischbeck K.H., Ross D.A., et al. The peripheral myelin gene PMP-22/GAS-3 is duplicated in Charcot-Marie-Tooth disease type 1A. Nat. Genet. 1 (1992) 166-170
19. Roa B.B., Garcia C.A., Suter U., Kulpa D.A., Wise C.A., Mueller J., Welcher A.A., Snipes G.J., Shooter E.M., Patel P.I., et al. Charcot-Marie-Tooth disease type 1A. Association with a spontaneous point mutation in the PMP22 gene. N. Engl. J. Med. 329 (1993) 96-101
20. Zhang F., Khajavi M., Connolly A.M., Towne C.F., Batish S.D., and Lupski J.R. The DNA replication FoSTeS/MMBIR mechanism can generate human genomic, genic, and exonic complex rearrangements. Nat. Genet. 41 (2009) 849-853
21. Palau F., Lofgren A., De Jonghe P., Bort S., Nelis E., Sevilla T., Martin J.J., Vilchez J., Prieto F., and Van Broeckhoven C. Origin of the de novo duplication in Charcot-Marie-Tooth disease type 1A: Unequal nonsister chromatid exchange during spermatogenesis. Hum. Mol. Genet. 2 (1993) 2031-2035
22. Timmerman V., Rautenstrauss B., Reiter L.T., Koeuth T., Lofgren A., Liehr T., Nelis E., Bathke K.D., De Jonghe P., Grehl H., et al. Detection of the CMT1A/HNPP recombination hotspot in unrelated patients of European descent. J. Med. Genet. 34 (1997) 43-49
23. Seeman P., Mazanec R., Zidar J., Hrusakova S., Ctvrteckova M., and Rautenstrauss B. Charcot-Marie-Tooth disease type 1A (CMT1A) and hereditary neuropathy with liability to pressure palsies (HNPP): reliable detection of the CMT1A duplication and HNPP deletion using 8 microsatellite markers in 2 multiplex PCRs. Int. J. Mol. Med. 6 (2000) 421-426
24. Weterman M.A., van Ruissen F., de Wissel M., Bordewijk L., Samijn J.P., van der Pol W.L., Meggouh F., and Baas F. Copy number variation upstream of PMP22 in Charcot-Marie-Tooth disease. Eur. J. Hum. Genet. 18 (2010) 421-428
25. Lee J.A., Carvalho C.M., and Lupski J.R. A DNA replication mechanism for generating nonrecurrent rearrangements associated with genomic disorders. Cell 131 (2007) 1235-1247
26. Bi W., Sapir T., Shchelochkov O.A., Zhang F., Withers M.A., Hunter J.V., Levy T., Shinder V., Peiffer D.A., Gunderson K.L., et al. Increased LIS1 expression affects human and mouse brain development. Nat. Genet. 41 (2009) 168-177
27. Stankiewicz P., Shaw C.J., Dapper J.D., Wakui K., Shaffer L.G., Withers M., Elizondo L., Park S.S., and Lupski J.R. Genome architecture catalyzes nonrecurrent chromosomal rearrangements. Am. J. Hum. Genet. 72 (2003) 1101-1116
28. Chen J.M., Chuzhanova N., Stenson P.D., Ferec C., and Cooper D.N. Meta-analysis of gross insertions causing human genetic disease: Novel mutational mechanisms and the role of replication slippage. Hum. Mutat. 25 (2005) 207-221
29. Chen J.M., Chuzhanova N., Stenson P.D., Ferec C., and Cooper D.N. Complex gene rearrangements caused by serial replication slippage. Hum. Mutat. 26 (2005) 125-134
30. Lieber M.R. The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu. Rev. Biochem. (2010) 10.1146/annurev.biochem.052308.093131
31. Kidd J.M., Cooper G.M., Donahue W.F., Hayden H.S., Sampas N., Graves T., Hansen N., Teague B., Alkan C., Antonacci F., et al. Mapping and sequencing of structural variation from eight human genomes. Nature 453 (2008) 56-64
32. Kang S.H., Shaw C., Ou Z., Eng P.A., Cooper M.L., Pursley A.N., Sahoo T., Bacino C.A., Chinault A.C., Stankiewicz P., et al. Insertional translocation detected using FISH confirmation of array-comparative genomic hybridization (aCGH) results. Am. J. Med. Genet. A. 152A (2010) 1111-1126
33. Stankiewicz P., Pursley A.N., and Cheung S.W. Challenges in clinical interpretation of microduplications detected by array CGH analysis. Am. J. Med. Genet. A. 152A (2010) 1089-1100
34. Roy A., Yan W., Burns K.H., and Matzuk M.M. Tektin3 encodes an evolutionarily conserved putative testicular microtubules-related protein expressed preferentially in male germ cells. Mol. Reprod. Dev. 67 (2004) 295-302
35. Lee J.A., Madrid R.E., Sperle K., Ritterson C.M., Hobson G.M., Garbern J., Lupski J.R., and Inoue K. Spastic paraplegia type 2 associated with axonal neuropathy and apparent PLP1 position effect. Ann. Neurol. 59 (2006) 398-403
36. Kleinjan D.A., and van Heyningen V. Long-range control of gene expression: emerging mechanisms and disruption in disease. Am. J. Hum. Genet. 76 (2005) 8-32
37. Carvalho C.M., Zhang F., Liu P., Patel P., Sahoo T., Bacino C.A., Shaw C., Peacock S., Pursley A., Tavyev Y.J., et al. Complex rearrangements in patients with duplications of MECP2 can occur by fork stalling and template switching. Hum. Mol. Genet. 18 (2009) 2188-2203
38. Lieber M.R. The mechanism of human nonhomologous DNA end joining. J. Biol. Chem. 283 (2008) 1-5
39. Hastings P.J., Ira G., and Lupski J.R. A microhomology-mediated break-induced replication model for the origin of human copy number variation. PLoS Genet. 5 (2009) e1000327
40. Payen C., Koszul R., Dujon B., and Fischer G. Segmental duplications arise from Pol32-dependent repair of broken forks through two alternative replication-based mechanisms. PLoS Genet. 4 (2008) e1000175
41. Zhang F., Carvalho C.M., and Lupski J.R. Complex human chromosomal and genomic rearrangements. Trends Genet. 25 (2009) 298-307
42. Hastings P.J., Lupski J.R., Rosenberg S.M., and Ira G. Mechanisms of change in gene copy number. Nat. Rev. Genet. 10 (2009) 551-564
43. Bailey J.A., Liu G., and Eichler E.E. An Alu transposition model for the origin and expansion of human segmental duplications. Am. J. Hum. Genet. 73 (2003) 823-834
44. Sen S.K., Han K., Wang J., Lee J., Wang H., Callinan P.A., Dyer M., Cordaux R., Liang P., and Batzer M.A. Human genomic deletions mediated by recombination between Alu elements. Am. J. Hum. Genet. 79 (2006) 41-53
45. Gajecka M., Gentles A.J., Tsai A., Chitayat D., Mackay K.L., Glotzbach C.D., Lieber M.R., and Shaffer L.G. Unexpected complexity at breakpoint junctions in phenotypically normal individuals and mechanisms involved in generating balanced translocations t(1;22)(p36;q13). Genome Res. 18 (2008) 1733-1742
46. Elliott B., Richardson C., and Jasin M. Chromosomal translocation mechanisms at intronic alu elements in mammalian cells. Mol. Cell 17 (2005) 885-894
47. Vissers L.E., Bhatt S.S., Janssen I.M., Xia Z., Lalani S.R., Pfundt R., Derwinska K., de Vries B.B., Gilissen C., Hoischen A., et al. Rare pathogenic microdeletions and tandem duplications are microhomology-mediated and stimulated by local genomic architecture. Hum. Mol. Genet. 18 (2009) 3579-3593
48. Lander E.S., Linton L.M., Birren B., Nusbaum C., Zody M.C., Baldwin J., Devon K., Dewar K., Doyle M., FitzHugh W., et al. Initial sequencing and analysis of the human genome. Nature 409 (2001) 860-921
49. Inoue K., Dewar K., Katsanis N., Reiter L.T., Lander E.S., Devon K.L., Wyman D.W., Lupski J.R., and Birren B. The 1.4-Mb CMT1A duplication/HNPP deletion genomic region reveals unique genome architectural features and provides insights into the recent evolution of new genes. Genome Res. 11 (2001) 1018-1033
50. Stankiewicz P., Shaw C.J., Withers M., Inoue K., and Lupski J.R. Serial segmental duplications during primate evolution result in complex human genome architecture. Genome Res. 14 (2004) 2209-2220
51. Wells R.D. Non-B DNA conformations, mutagenesis and disease. Trends Biochem. Sci. 32 (2007) 271-278
52. Argueso J.L., Westmoreland J., Mieczkowski P.A., Gawel M., Petes T.D., and Resnick M.A. Double-strand breaks associated with repetitive DNA can reshape the genome. Proc. Natl. Acad. Sci. USA 105 (2008) 11845-11850
53. Voineagu I., Narayanan V., Lobachev K.S., and Mirkin S.M. Replication stalling at unstable inverted repeats: Interplay between DNA hairpins and fork stabilizing proteins. Proc. Natl. Acad. Sci. USA 105 (2008) 9936-9941
54. Manolio T.A., Collins F.S., Cox N.J., Goldstein D.B., Hindorff L.A., Hunter D.J., McCarthy M.I., Ramos E.M., Cardon L.R., Chakravarti A., et al. Finding the missing heritability of complex diseases. Nature 461 (2009) 747-753