Whole exome sequencing implicates an INO80D mutation in a syndrome of aortic hypoplasia, premature atherosclerosis, and arterial stiffness

Circulation: Cardiovascular Genetics

Volumn 7, Issue 5, 2014, Pages 607-614

  Shameer, Khader ^a   Klee, Eric W ^b   Dalenberg, Angela K ^a   Kullo, Iftikhar J ^a  

^a MAYO CLINIC   (United States)

^b Laboratory Medicine and Pathology   (United States)

Author keywords

Aortic hypoplasia; Arterial stiffness; Atherosclerosis; Chromatin assembly and disassembly; Genetics; INO80D protein human

Indexed keywords

ADENOSINE TRIPHOSPHATE; MULTIPROTEIN COMPLEX; CHROMATIN; DNA HELICASE; INO80 PROTEIN, HUMAN;

ADOLESCENT; ADULT; AGED; AGING; AORTA DISEASE; AORTIC HYPOPLASIA; ARTERIAL STIFFNESS; ARTICLE; ATHEROSCLEROSIS; BASE PAIRING; CATARACT; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOME 2; CHROMOSOME STRUCTURE; CLINICAL ARTICLE; DISULFIDE BOND; DNA BINDING; EXOME; FEMALE; GENE FREQUENCY; GENE MAPPING; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC VARIABILITY; GENOME; GENOTYPE; HIGH THROUGHPUT SEQUENCING; HOMOZYGOSITY; HUMAN; MALE; MISSENSE MUTATION; NEXT GENERATION SEQUENCING; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; QUALITY CONTROL; SIBLING; SYSTOLIC HYPERTENSION; VASCULAR DISEASE; WHOLE EXOME SEQUENCING; FAMILY HEALTH; GENETICS; HOMOZYGOTE; HYPERTENSION; MUTATION; PHENOTYPE; SINGLE NUCLEOTIDE POLYMORPHISM; SYNDROME;

ADULT; AGED; AGING; AORTIC DISEASES; ATHEROSCLEROSIS; CATARACT; CHROMATIN; DNA HELICASES; EXOME; FAMILY HEALTH; FEMALE; GENOTYPE; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HOMOZYGOTE; HUMANS; HYPERTENSION; MALE; MUTATION; MUTATION, MISSENSE; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE; SYNDROME; VASCULAR STIFFNESS;

EID: 84920525015     PISSN: 1942325X     EISSN: 19423268     Source Type: Journal    
DOI: 10.1161/CIRCGENETICS.113.000233     Document Type: Article

References (55)

1. Nielsen R, Paul JS, Albrechtsen A, Song YS. Genotype and SNP calling from next-generation sequencing data. Nat Rev Genet. 2011;12:443-451
2. Ng SB, Buckingham KJ, Lee C, Bigham AW, Tabor HK, Dent KM, et al. Exome sequencing identifies the cause of a mendelian disorder. Nat Genet. 2010;42:30-35
3. Tennessen JA, Bigham AW, O'Connor TD, Fu W, Kenny EE, Gravel S, et al; Broad GO; Seattle GO; NHLBI Exome Sequencing Project. Evolution and functional impact of rare coding variation from deep sequencing of human exomes. Science. 2012;337:64-69
4. Gilissen C, Hoischen A, Brunner HG, Veltman JA. Unlocking Mendelian disease using exome sequencing. Genome Biol. 2011;12:228
5. Lander ES, Botstein D. Homozygosity mapping: A way to map human recessive traits with the DNA of inbred children. Science. 1987;236:1567-1570
6. Clark AG. The size distribution of homozygous segments in the human genome. Am J Hum Genet. 1999;65:1489-1492
7. Szpiech ZA, Xu J, Pemberton TJ, Peng W, Zöllner S, Rosenberg NA, et al. Long runs of homozygosity are enriched for deleterious variation. Am J Hum Genet. 2013;93:90-102
8. Takata A, Kato M, Nakamura M, Yoshikawa T, Kanba S, Sano A, et al. Exome sequencing identifies a novel missense variant in RRM2B associated with autosomal recessive progressive external ophthalmoplegia. Genome Biol. 2011;12:R92
9. Chahrour MH, Yu TW, Lim ET, Ataman B, Coulter ME, Hill RS, et al; ARRA Autism Sequencing Collaboration. Whole-exome sequencing and homozygosity analysis implicate depolarization-regulated neuronal genes in autism. PLoS Genet. 2012;8:e1002635
10. Shamseldin HE, Elfaki M, Alkuraya FS. Exome sequencing reveals a novel Fanconi group defined by XRCC2 mutation. J Med Genet. 2012;49:184-186
11. Walsh T, Shahin H, Elkan-Miller T, Lee MK, Thornton AM, Roeb W, et al. Whole exome sequencing and homozygosity mapping identify mutation in the cell polarity protein GPSM2 as the cause of nonsyndromic hearing loss DFNB82. Am J Hum Genet. 2010;87:90-94
12. Erlich Y, Edvardson S, Hodges E, Zenvirt S, Thekkat P, Shaag A, et al. Exome sequencing and disease-network analysis of a single family implicate a mutation in KIF1A in hereditary spastic paraparesis. Genome Res. 2011;21:658-664
13. Abu-Safieh L, Alrashed M, Anazi S, Alkuraya H, Khan AO, Al-Owain M, et al. Autozygome-guided exome sequencing in retinal dystrophy patients reveals pathogenetic mutations and novel candidate disease genes. Genome Res. 2013;23:236-247
14. Kullo IJ, Fan J, Pathak J, Savova GK, Ali Z, Chute CG. Leveraging informatics for genetic studies: use of the electronic medical record to enable a genome-wide association study of peripheral arterial disease. J Am Med Inform Assoc. 2010;17:568-574
15. Jouni H, Shameer K, Asmann YW, Hazin R, de Andrade M, Kullo IJ. Clinical correlates of autosomal chromosomal abnormalities in an electronic medical record-linked Genome-wide association study: A case series. Journal of Investigative Medicine: The Official Publication of the American Federation for Clinical Research. 2013;1
16. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, et al. PLINK: A tool set for whole-genome association and populationbased linkage analyses. Am J Hum Genet. 2007;81:559-575
17. Thorvaldsdottir H, Robinson JT, Mesirov JP. Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Briefings in Bioinformatics. 2013;14:178-92
18. Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, Bork P, et al. A method and server for predicting damaging missense mutations. Nat Methods. 2010;7:248-249
19. Han P, Hang CT, Yang J, Chang CP. Chromatin remodeling in cardiovascular development and physiology. Circ Res. 2011;108:378-96
20. Chen L, Cai Y, Jin J, Florens L, Swanson SK, Washburn MP, et al. Subunit organization of the human INO80 chromatin remodeling complex: An evolutionarily conserved core complex catalyzes ATP-dependent nucleosome remodeling. J Biol Chem. 2011;286:11283-11289
21. Jin J, Cai Y, Yao T, Gottschalk AJ, Florens L, Swanson SK, et al. A mammalian chromatin remodeling complex with similarities to the yeast INO80 complex. J Biol Chem. 2005;280:41207-41212
22. Morrison AJ, Shen X. Chromatin remodelling beyond transcription: The INO80 and SWR1 complexes. Nat Rev Mol Cell Biol. 2009;10:373-384
23. Bao Y, Shen X. INO80 subfamily of chromatin remodeling complexes. Mutat Res. 2007;618:18-29
24. Conaway RC, Conaway JW. The INO80 chromatin remodeling complex in transcription, replication and repair. Trends Biochem Sci. 2009;34:71-77
25. Ferrè F, Clote P. DiANNA: A web server for disulfide connectivity prediction. Nucleic Acids Res. 2005;33(Web Server issue):W230-W232
26. Wedemeyer WJ, Welker E, Narayan M, Scheraga HA. Disulfide bonds and protein folding. Biochemistry. 2000;39:4207-4216
27. Shen X. Preparation and analysis of the INO80 complex. Methods Enzymol. 2004;377:401-412
28. Fass D. Disulfide bonding in protein biophysics. Annu Rev Biophys. 2012;41:63-79
29. Hur SK, Park EJ, Han JE, Kim YA, Kim JD, Kang D, et al. Roles of human INO80 chromatin remodeling enzyme in DNA replication and chromosome segregation suppress genome instability. Cell Mol Life Sci. 2010;67:2283-2296
30. Park EJ, Hur SK, Kwon J. Human INO80 chromatin-remodelling complex contributes to DNA double-strand break repair via the expression of Rad54B and XRCC3 genes. Biochem J. 2010;431:179-187
31. Watanabe S, Peterson CL. The INO80 family of chromatin-remodeling enzymes: Regulators of histone variant dynamics. Cold Spring Harb Symp Quant Biol. 2010;75:35-42
32. Han P, Hang CT, Yang J, Chang CP. Chromatin remodeling in cardiovascular development and physiology. Circ Res. 2011;108:378-396
33. Chambers AL, Downs JA. The RSC and INO80 chromatin-remodeling complexes in DNA double-strand break repair. Prog Mol Biol Transl Sci. 2012;110:229-261
34. Chambers AL, Ormerod G, Durley SC, Sing TL, Brown GW, Kent NA, et al. The INO80 chromatin remodeling complex prevents polyploidy and maintains normal chromatin structure at centromeres. Genes Dev. 2012;26:2590-2603
35. Chang CP, Bruneau BG. Epigenetics and cardiovascular development. Annu Rev Physiol. 2012;74:41-68
36. Kozomara A, Griffiths-Jones S. miRBase: Integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res. 2011;39(Database issue):D152-D157
37. Lu M, Zhang Q, Deng M, Miao J, Guo Y, Gao W, et al. An analysis of human microRNA and disease associations. PLoS One. 2008;3:e3420
38. Rottbauer W, Saurin AJ, Lickert H, Shen X, Burns CG, Wo ZG, et al. Reptin and pontin antagonistically regulate heart growth in zebrafish embryos. Cell. 2002;111:661-672
39. Bhatia S, Pawar H, Dasari V, Mishra RK, Chandrashekaran S, Brahmachari V. Chromatin remodeling protein INO80 has a role in regulation of homeotic gene expression in Drosophila. Genes Cells. 2010;15:725-735
40. Clapier CR, Cairns BR. The biology of chromatin remodeling complexes. Annu Rev Biochem. 2009;78:273-304
41. Bakshi R, Mehta AK, Sharma R, Maiti S, Pasha S, Brahmachari V. Characterization of a human SWI2/SNF2 like protein hINO80: demonstration of catalytic and DNA binding activity. Biochem Biophys Res Commun. 2006;339:313-320
42. Cai Y, Jin J, Yao T, Gottschalk AJ, Swanson SK, Wu S, et al. YY1 functions with INO80 to activate transcription. Nat Struct Mol Biol. 2007;14:872-874
43. Falbo KB, Shen X. Function of the INO80 chromatin remodeling complex in DNA replication. Front Biosci. 2012;17:970-975
44. Cairns BR. Around the world of DNA damage INO80 days. Cell. 2004;119:733-735
45. Kawashima S, Ogiwara H, Tada S, Harata M, Wintersberger U, Enomoto T, et al. The INO80 complex is required for damage-induced recombination. Biochem Biophys Res Commun. 2007;355:835-841
46. Morrison AJ, Kim JA, Person MD, Highland J, Xiao J, Wehr TS, et al. Mec1/Tel1 phosphorylation of the INO80 chromatin remodeling complex influences DNA damage checkpoint responses. Cell. 2007;130:499-511
47. Czaja W, Bespalov VA, Hinz JM, Smerdon MJ. Proficient repair in chromatin remodeling defective ino80 mutants of Saccharomyces cerevisiae highlights replication defects as the main contributor to DNA damage sensitivity. DNA Repair (Amst). 2010;9:976-984
48. Kashiwaba S, Kitahashi K, Watanabe T, Onoda F, Ohtsu M, Murakami Y. The mammalian INO80 complex is recruited to DNA damage sites in an ARP8 dependent manner. Biochem Biophys Res Commun. 2010;402:619-625
49. Sarkar S, Kiely R, McHugh PJ. The Ino80 chromatin-remodeling complex restores chromatin structure during UV DNA damage repair. J Cell Biol. 2010;191:1061-1068
50. Kato D, Waki M, Umezawa M, Aoki Y, Utsugi T, Ohtsu M, et al. Phosphorylation of human INO80 is involved in DNA damage tolerance. Biochem Biophys Res Commun. 2012;417:433-438
51. Yu EY, Steinberg-Neifach O, Dandjinou AT, Kang F, Morrison AJ, Shen X, et al. Regulation of telomere structure and functions by subunits of the INO80 chromatin remodeling complex. Mol Cell Biol. 2007;27:5639-5649
52. Saravanan M, Wuerges J, Bose D, McCormack EA, Cook NJ, Zhang X, et al. Interactions between the nucleosome histone core and Arp8 in the INO80 chromatin remodeling complex. Proc Natl Acad Sci U S A. 2012;109:20883-20888
53. Charles GM, Chen C, Shih SC, Collins SR, Beltrao P, Zhang X, et al. Site-specific acetylation mark on an essential chromatin-remodeling complex promotes resistance to replication stress. Proc Natl Acad Sci U S A. 2011;108:10620-10625
54. van Attikum H, Fritsch O, Gasser SM. Distinct roles for SWR1 and INO80 chromatin remodeling complexes at chromosomal double-strand breaks. EMBO J. 2007;26:4113-4125
55. Dreesen O, Stewart CL. Accelerated aging syndromes, are they relevant to normal human aging? Aging. 2011;3:889-895.