Exome sequencing identifies SMAD3 mutations as a cause of familial thoracic aortic aneurysm and dissection with intracranial and other arterial aneurysms

Circulation Research

Volumn 109, Issue 6, 2011, Pages 680-686

  Regalado, Ellen S ^a   Guo, Dong Chuan ^a   Villamizar, Carlos ^a   Avidan, Nili ^a   Gilchrist, Dawna ^b   McGillivray, Barbara ^c   Clarke, Lorne ^c   Bernier, Francois ^d   Santos Cortez, Regie L ^e   Leal, Suzanne M ^e   Bertoli Avella, Aida M ^f   Shendure, Jay ^g   Rieder, Mark J ^g   Nickerson, Deborah A ^g   Milewicz, Dianna M ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF ALBERTA   (Canada)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^d UNIVERSITY OF CALGARY   (Canada)

^e BAYLOR COLLEGE OF MEDICINE   (United States)

^f ERASMUS MEDICAL CENTER   (Netherlands)

^g UNIVERSITY OF WASHINGTON   (United States)

Author keywords

arterial aneurysms; intracranial aneurysm; SMAD3; thoracic aortic aneurysm and dissection

Indexed keywords

SMAD3 PROTEIN;

ABDOMINAL AORTA ANEURYSM; ADULT; ALGORITHM; AORTA DISSECTION; ARTICLE; AUTOSOMAL DOMINANT INHERITANCE; BLOOD SAMPLING; CLINICAL FEATURE; CONTROLLED STUDY; EXOME; FEMALE; FRAMESHIFT MUTATION; GENE FREQUENCY; GENE IDENTIFICATION; GENE MAPPING; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC VARIABILITY; HUMAN; INTRACRANIAL ANEURYSM; MAJOR CLINICAL STUDY; MALE; MUTATIONAL ANALYSIS; NUCLEOTIDE SEQUENCE; OSTEOARTHRITIS; PEDIGREE ANALYSIS; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SALIVA ANALYSIS; SCORING SYSTEM; SEQUENCE ANALYSIS; SUBARACHNOID HEMORRHAGE; THORACIC AORTA ANEURYSM;

ANEURYSM, DISSECTING; AORTIC ANEURYSM, THORACIC; COHORT STUDIES; FEMALE; FRAMESHIFT MUTATION; GENES, DOMINANT; HUMANS; INTRACRANIAL ANEURYSM; MALE; PEDIGREE; SEQUENCE ANALYSIS, DNA; SMAD3 PROTEIN;

EID: 80052584397     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.111.248161     Document Type: Article

References (27)

1. Milewicz DM, Chen H, Park ES, Petty EM, Zaghi H, Shashidhar G, Willing M, Patel V. Reduced penetrance and variable expressivity of familial thoracic aortic aneurysms/dissections. Am J Cardiol. 1998;82: 474-479. (Pubitemid 28392280)
2. Zhu L, Vranckx R, Khau Van KP, Lalande A, Boisset N, Mathieu F, Wegman M, Glancy L, Gasc JM, Brunotte F, Bruneval P, Wolf JE, Michel JB, Jeunemaitre X. Mutations in myosin heavy chain 11 cause a syndrome associating thoracic aortic aneurysm/aortic dissection and patent ductus arteriosus. Nat Genet. 2006;38:343-349.
3. Loscalzo ML, Goh DL, Loeys B, Kent KC, Spevak PJ, Dietz HC. Familial thoracic aortic dilation and bicommissural aortic valve: a prospective analysis of natural history and inheritance. Am J Med Genet A. 2007;143:1960-1967.
4. Guo DC, Pannu H, Papke CL, Yu RK, Avidan N, Bourgeois S, Estrera AL, Safi HJ, Sparks E, Amor D, Ades L, McConnell V, Willoughby CE, Abuelo D, Willing M, Lewis RA, Kim DH, Scherer S, Tung PP, Ahn C, Buja LM, Raman CS, Shete S, Milewicz DM. Mutations in smooth muscle alpha-actin (ACTA2) lead to thoracic aortic aneurysms and dissections. Nat Genet. 2007;39:1488-1493. (Pubitemid 350191352)
5. Regalado E, Medrek S, Tran-Fadulu V, Guo D-C, Pannu H, Golabbakhsh H, Smart S, Chen JH, Shete S, Kim DH, Stern R, Braverman AC, Milewicz DM. Autosomal dominant inheritance of a predisposition to thoracic aortic aneurysms and dissections and intracranial saccular aneu-rysms. Am J Med Genet A. 2011. In press.
6. Collod-Beroud G, Le Bourdelles S, Ades L, Ala-Kokko L, Booms P, Boxer M, Child A, Comeglio P, De Paepe A, Hyland JC, Holman K, Kaitila I, Loeys B, Matyas G, Nuytinck L, Peltonen L, Rantamaki T, Robinson P, Steinmann B, Junien C, Beroud C, Boileau C. Update of the UMD-FBN1 mutation database and creation of an FBN1 polymorphism database. Hum Mutat. 2003;22:199-208. (Pubitemid 37071636)
7. Loeys BL, Schwarze U, Holm T, Callewaert BL, Thomas GH, Pannu H, De Backer JF, Oswald GL, Symoens S, Manouvrier S, Roberts AE, Faravelli F, Greco MA, Pyeritz RE, Milewicz DM, Coucke PJ, Cameron DE, Braverman AC, Byers PH, De Paepe AM, Dietz HC. Aneurysm syndromes caused by mutations in the TGF-beta receptor. N Engl J Med. 2006;355:788-798. (Pubitemid 44285584)
8. Pannu H, Fadulu V, Chang J, Lafont A, Hasham SN, Sparks E, Giampietro PF, Zaleski C, Estrera AL, Safi HJ, Shete S, Willing MC, Raman CS, Milewicz DM. Mutations in transforming growth factor-beta receptor type II cause familial thoracic aortic aneurysms and dissections. Circulation. 2005;112:513-520. (Pubitemid 41060791)
9. Tran-Fadulu V, Pannu H, Kim DH, Vick GW III, Lonsford CM, Lafont AL, Boccalandro C, Smart S, Peterson KL, Hain JZ, Willing MC, Coselli JS, LeMaire SA, Ahn C, Byers PH, Milewicz DM. Analysis of multi-generational families with thoracic aortic aneurysms and dissections due to TGFBR1 or TGFBR2 mutations. J Med Genet. 2009;46:607-613.
10. Milewicz DM, Michael K, Fisher N, Coselli JS, Markello T, Biddinger A. Fibrillin-1 (FBN1) mutations in patients with thoracic aortic aneurysms. Circulation. 1996;94:2708-2711. (Pubitemid 26411732)
11. Francke U, Berg MA, Tynan K, Brenn T, Liu WG, Aoyama T, Gasner C, Miller DC, Furthmayr H. A Gly1127Ser mutation in an Egf-like domain of the fibrillin-1 gene is a risk factor for ascending aortic-aneurysm and dissection. Am J Hum Genet. 1995;56:1287-1296.
12. van de Laar IM, Oldenburg RA, Pals G, Roos-Hesselink JW, de Graaf BM, Verhagen JM, Hoedemaekers YM, Willemsen R, Severijnen LA, Venselaar H, Vriend G, Pattynama PM, Collee M, Majoor-Krakauer D, Poldermans D, Frohn-Mulder IM, Micha D, Timmermans J, Hilhorst-Hofstee Y, Bierma-Zeinstra SM, Willems PJ, Kros JM, Oei EH, Oostra BA, Wessels MW, Bertoli-Avella AM. Mutations in SMAD3 cause a syndromic form of aortic aneurysms and dissections with early-onset osteoarthritis. Nat Genet. 2011;43:121-126.
13. O'Roak BJ, Deriziotis P, Lee C, Vives L, Schwartz JJ, Girirajan S, Karakoc E, MacKenzie AP, Ng SB, Baker C, Rieder MJ, Nickerson DA, Bernier R, Fisher SE, Shendure J, Eichler EE. Exome sequencing in sporadic autism spectrum disorders identifies severe de novo mutations. Nat Genet. 2011;43:585-589.
14. Li H, Durbin R. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics. 2010;26:589-595.
15. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. The sequence alignment/map format and SAMtools. Bioinformatics. 2009;25:2078-2079.
16. NHLBI Exome Sequencing Project (ESP). Exome Variant Server. http://snp.gs.washington.edu/popgenSNP/. Accessed May 2011.
17. Guo D, Hasham S, Kuang SQ, Vaughan CJ, Boerwinkle E, Chen H, Abuelo D, Dietz HC, Basson CT, Shete SS, Milewicz DM. Familial thoracic aortic aneurysms and dissections: genetic heterogeneity with a major locus mapping to 5q13-14. Circulation. 2001;103:2461-2468. (Pubitemid 32493372)
18. Cottingham RW Jr, Idury RM, Schaffer AA. Faster sequential genetic linkage computations. Am J Hum Genet. 1993;53:252-263. (Pubitemid 23313755)
19. Venselaar H, Te Beek TA, Kuipers RK, Hekkelman ML, Vriend G. Protein structure analysis of mutations causing inheritable diseases: an e-Science approach with life scientist friendly interfaces. BMC Bioinfor-matics. 2010;11:548.
20. Kurisaki A, Kurisaki K, Kowanetz M, Sugino H, Yoneda Y, Heldin CH, Moustakas A. The mechanism of nuclear export of Smad3 involves exportin 4 and Ran. Mol Cell Biol. 2006;26:1318-1332. (Pubitemid 43202559)
21. Hiratzka LF, Bakris GL, Beckman JA, Bersin RM, Carr VF, Casey DE Jr, Eagle KA, Hermann LK, Isselbacher EM, Kazerooni EA, Kouchoukos NT, Lytle BW, Milewicz DM, Reich DL, Sen S, Shinn JA, Svensson LG, Williams DM. 2010 ACCF/AHA/AATS/ACR/ASA/SCA/SCAI/SIR/STS/SVM guidelines for the diagnosis and management of patients with Thoracic Aortic Disease: a report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines, American Association for Thoracic Surgery, American College of Radiology, American Stroke Association, Society of Cardiovascular Anesthesiologists, Society for Cardiovascular Angiography and Interventions, Society of Interventional Radiology, Society of Thoracic Surgeons, and Society for Vascular Medicine. Circulation. 2010;121: e266-e369.
22. Hamamoto T, Beppu H, Okada H, Kawabata M, Kitamura T, Miyazono K, Kato M. Compound disruption of smad2 accelerates malignant progression of intestinal tumors in APC knockout mice. Cancer Res. 2002; 62:5955-5961. (Pubitemid 35204759)
23. Datto MB, Frederick JP, Pan L, Borton AJ, Zhuang Y, Wang XF. Targeted disruption of Smad3 reveals an essential role in transforming growth factor beta-mediated signal transduction. Mol Cell Biol. 1999;19: 2495-2504. (Pubitemid 29144493)
24. Uemura M, Swenson ES, Gaca MD, Giordano FJ, Reiss M, Wells RG. Smad2 and Smad3 play different roles in rat hepatic stellate cell function and alpha-smooth muscle actin organization. Mol Biol Cell. 2005;16: 4214-4224. (Pubitemid 41262890)
25. Gu L, Zhu YJ, Yang X, Guo ZJ, Xu WB, Tian XL. Effect of TGF-beta/Smad signaling pathway on lung myofibroblast differentiation. Acta Pharmacol Sin. 2007;28:382-391.
26. Dobaczewski M, Bujak M, Li N, Gonzalez-Quesada C, Mendoza LH, Wang XF, Frangogiannis NG. Smad3 signaling critically regulates fibroblast phenotype and function in healing myocardial infarction. Circ Res. 2010;107:418-428.
27. Inamoto S, Kwartler CS, Lafont AL, Liang YY, Fadulu VT, Duraisamy S, Willing M, Estrera A, Safi H, Hannibal MC, Carey J, Wiktorowicz J, Tan FK, Feng XH, Pannu H, Milewicz DM. TGFBR2 mutations alter smooth muscle cell phenotype and predispose to thoracic aortic aneu-rysms and dissections. Cardiovasc Res. 2010;88:520-529.