Drug-sensitized zebrafish screen identifies multiple genes, including GINS3, as regulators of myocardial repolarization

Circulation

Volumn 120, Issue 7, 2009, Pages 553-559

  Milan, David J ^a   Kim, Albert M ^a   Winterfield, Jeffrey R ^a   Jones, Ian L ^a   Pfeufer, Arne ^b,c,d   Sanna, Serena ^d   Arking, Dan E ^d,e   Amsterdam, Adam H ^f   Sabeh, Khaled M ^a   Mably, John D ^g   Rosenbaum, David S ^h   Peterson, Randall T ^a   Chakravarti, Aravinda ^d,e   Kääb, Stefan ^d,i   Roden, Dan M ^j   MacRae, Calum A ^a  

^a Cardiovascular Research Center   (United States)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^d CNR   (Italy)

^e JOHNS HOPKINS UNIVERSITY   (United States)

^f MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^g BOSTON CHILDREN S HOSPITAL   (United States)

^h CASE WESTERN RESERVE UNIVERSITY   (United States)

ⁱ LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^j VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

more..

Author keywords

Electrophysiology; Genes; Ion channels; Myocardial repolarization

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE PREDISPOSITION; DRUG SENSITIZATION; EXPERIMENTAL ANIMAL; GENE IDENTIFICATION; GENE SEQUENCE; GENETIC SCREENING; GENOME; GINS3 GENE; HEART REPOLARIZATION; MEMBRANE POTENTIAL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; QT INTERVAL; REGULATOR GENE; SUDDEN DEATH; ZEBRA FISH;

ANIMALS; DEATH, SUDDEN, CARDIAC; GENE EXPRESSION PROFILING; GENES, REGULATOR; HEART; HEART CONDUCTION SYSTEM; HUMANS; LONG QT SYNDROME; MEMBRANE POTENTIALS; MODELS, ANIMAL; MYOCYTES, CARDIAC; PHENOTYPE; RISK FACTORS; ZEBRAFISH;

EID: 69549124105     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.108.821082     Document Type: Article

References (38)

1. Priori SG, Napolitano C, Schwartz PJ, Grillo M, Bloise R, Ronchetti E, Moncalvo C, Tulipani C, Veia A, Bottelli G, Nastoli J. Association of long QT syndrome loci and cardiac events among patients treated with beta-blockers. JAMA. 2004;292:1341-1344.
2. Siscovick DS, Raghunathan TE, Rautaharju P, Psaty BM, Cobb LA, Wagner EH. Clinically silent electrocardiographic abnormalities and risk of primary cardiac arrest among hypertensive patients. Circulation. 1996; 94:1329-1333. (Pubitemid 26307261)
3. Brooksby P, Batin PD, Nolan J, Lindsay SJ, Andrews R, Mullen M, Baig W, Flapan AD, Prescott RJ, Neilson JM, Cowley AJ, Fox KA. The relationship between QT intervals and mortality in ambulant patients with chronic heart failure: the United Kingdom Heart Failure Evaluation and Assessment of Risk Trial (UK-HEART). Eur Heart J. 1999;20: 1335-1341.
4. Roden DM. Drug-induced prolongation of the QT interval. N Engl J Med. 2004;350:1013-1022.
5. Wilke RA, Lin DW, Roden DM, Watkins PB, Flockhart D, Zineh I, Giacomini KM, Krauss RM. Identifying genetic risk factors for serious adverse drug reactions: current progress and challenges. Nat Rev Drug Discov. 2007;6:904-916.
6. Keating MT, Sanguinetti MC. Molecular and cellular mechanisms of cardiac arrhythmias. Cell. 2001;104:569-580.
7. Nerbonne JM, Kass RS. Molecular physiology of cardiac repolarization. Physiol Rev. 2005;85:1205-1253.
8. Vincent GM. Hypothesis for the molecular physiology of the Romano-Ward long QT syndrome. J Am Coll Cardiol. 1992;20:500-503.
9. Mohler PJ, Schott JJ, Gramolini AO, Dilly KW, Guatimosim S, duBell WH, Song LS, Haurogne K, Kyndt F, Ali ME, Rogers TB, Lederer WJ, Escande D, Le Marec H, Bennett V. Ankyrin-B mutation causes type 4 long-QT cardiac arrhythmia and sudden cardiac death. Nature. 2003;421: 634-639.
10. Vatta M, Ackerman MJ, Ye B, Makielski JC, Ughanze EE, Taylor EW, Tester DJ, Balijepalli RC, Foell JD, Li Z, Kamp TJ, Towbin JA. Mutant caveolin-3 induces persistent late sodium current and is associated with long-QT syndrome. Circulation. 2006;114:2104-2112.
11. Chen JN, Haffter P, Odenthal J, Vogelsang E, Brand M, van Eeden FJ, Furutani-Seiki M, Granato M, Hammerschmidt M, Heisenberg CP, Jiang YJ, Kane DA, Kelsh RN, Mullins MC, Nusslein-Volhard C. Mutations affecting the cardiovascular system and other internal organs in zebrafish. Development. 1996;123:293-302.
12. Briggs JP. The zebrafish: a new model organism for integrative physiology. Am J Physiol Regul Integr Comp Physiol. 2002;282:R3-R9.
13. Burns CG, Milan DJ, Grande EJ, Rottbauer W, MacRae CA, Fishman MC. High-throughput assay for small molecules that modulate zebrafish embryonic heart rate. Nat Chem Biol. 2005;1:263-264.
14. Boisen AM, Amstrup J, Novak I, Grosell M. Sodium and chloride transport in soft water and hard water acclimated zebrafish (Danio rerio). Biochim Biophys Acta. 2003;1618:207-218.
15. Arnaout R, Ferrer T, Huisken J, Spitzer K, Stainier DY, Tristani-Firouzi M, Chi NC. Zebrafish model for human long QT syndrome. Proc Natl Acad Sci U S A. 2007;104:11316-11321.
16. Sedmera D, Reckova M, deAlmeida A, Sedmerova M, Biermann M, Volejnik J, Sarre A, Raddatz E, McCarthy RA, Gourdie RG, Thompson RP. Functional and morphological evidence for a ventricular conduction system in zebrafish and Xenopus hearts. Am J Physiol Heart Circ Physiol. 2003;284:H1152-H1160.
17. Amsterdam A, Nissen RM, Sun Z, Swindell EC, Farrington S, Hopkins N. Identification of 315 genes essential for early zebrafish development. Proc Natl Acad Sci U S A. 2004;101:12792-12797.
18. Milan DJ, Peterson TA, Ruskin JN, Peterson RT, MacRae CA. Drugs that induce repolarization abnormalities cause bradycardia in zebrafish. Circulation. 2003;107:1355-1358.
19. Hassel D, Scholz EP, Trano N, Friedrich O, Just S, Meder B, Weiss DL, Zitron E, Marquart S, Vogel B, Karle CA, Seemann G, Fishman MC, Katus HA, Rottbauer W. Deficient zebrafish ether-a-go-go-related gene channel gating causes short-QT syndrome in zebrafish reggae mutants. Circulation. 2008;117:866-875.
20. Langheinrich U, Vacun G, Wagner T. Zebrafish embryos express an orthologue of HERG and are sensitive toward a range of QT-prolonging drugs inducing severe arrhythmia. Toxicol Appl Pharmacol. 2003;193: 370-382.
21. Bezzina CR, Verkerk AO, Busjahn A, Jeron A, Erdmann J, Koopmann TT, Bhuiyan ZA, Wilders R, Mannens MM, Tan HL, Luft FC, Schunkert H, Wilde AA. A common polymorphism in KCNH2 (HERG) hastens cardiac repolarization. Cardiovasc Res. 2003;59:27-36.
22. Pfeufer A, Jalilzadeh S, Perz S, Mueller JC, Hinterseer M, Illig T, Akyol M, Huth C, Schopfer-Wendels A, Kuch B, Steinbeck G, Holle R, Nabauer M, Wichmann HE, Meitinger T, Kaab S. Common variants in myocardial ion channel genes modify the QT interval in the general population: results from the KORA study. Circ Res. 2005;96:693-701.
23. Newton-Cheh C, Guo CY, Larson MG, Musone SL, Surti A, Camargo AL, Drake JA, Benjamin EJ, Levy D, D'Agostino RB Sr, Hirschhorn JN, O'Donnell CJ. Common genetic variation in KCNH2 is associated with QT interval duration: the Framingham Heart Study. Circulation. 2007; 116:1128-1136.
24. Catterall WA, Beress L. Sea anemone toxin and scorpion toxin share a common receptor site associated with the action potential sodium ionophore. J Biol Chem. 1978;253:7393-7396.
25. Arking DE, Pfeufer A, Post W, Kao WH, Newton-Cheh C, Ikeda M, West K, Kashuk C, Akyol M, Perz S, Jalilzadeh S, Illig T, Gieger C, Guo CY, Larson MG, Wichmann HE, Marban E, O'Donnell CJ, Hirschhorn JN, Kaab S, Spooner PM, Meitinger T, Chakravarti A. A common genetic variant in the NOS1 regulator NOS1AP modulates cardiac repolarization. Nat Genet. 2006;38:644-651.
26. Lupoglazoff JM, Denjoy I, Villain E, Fressart V, Simon F, Bozio A, Berthet M, Benammar N, Hainque B, Guicheney P. Long QT syndrome in neonates: conduction disorders associated with HERG mutations and sinus bradycardia with KCNQ1 mutations. J Am Coll Cardiol. 2004;43: 826-830.
27. Trippel DL, Parsons MK, Gillette PC. Infants with long-QT syndrome and 2:1 atrioventricular block. Am Heart J. 1995;130:1130-1134.
28. Scott WA, Dick M II. Two:one atrioventricular block in infants with congenital long QT syndrome. Am J Cardiol. 1987;60:1409-1410.
29. Mably JD, Chuang LP, Serluca FC, Mohideen MA, Chen JN, Fishman MC. Santa and valentine pattern concentric growth of cardiac myocardi-um in the zebrafish. Development. 2006;133:3139-3146.
30. Mably JD, Mohideen MA, Burns CG, Chen JN, Fishman MC. Heart of glass regulates the concentric growth of the heart in zebrafish. Curr Biol. 2003;13:2138-2147.
31. Newton-Cheh C, Eijgelsheim M, Rice KM, de Bakker PI, Yin X, Estrada K, Bis JC, Marciante K, Rivadeneira F, Noseworthy PA, Sotoodehnia N, Smith NL, Rotter JI, Kors JA, Witteman JC, Hofman A, Heckbert SR, O'Donnell CJ, Uitterlinden AG, Psaty BM, Lumley T, Larson MG, Stricker BH. Common variants at ten loci influence QT interval duration in the QTGEN Study. Nat Genet. 2009;41:399-406.
32. Pfeufer A, Sanna S, Arking DE, Muller M, Gateva V, Fuchsberger C, Ehret GB, Orru M, Pattaro C, Kottgen A, Perz S, Usala G, Barbalic M, Li M, Putz B, Scuteri A, Prineas RJ, Sinner MF, Gieger C, Najjar SS, Kao WH, Muhleisen TW, Dei M, Happle C, Mohlenkamp S, Crisponi L, Erbel R, Jockel KH, Naitza S, Steinbeck G, Marroni F, Hicks AA, Lakatta E, Muller-Myhsok B, Pramstaller PP, Wichmann HE, Schlessinger D, Boer-winkle E, Meitinger T, Uda M, Coresh J, Kaab S, Abecasis GR, Chakravarti A. Common variants at ten loci modulate the QT interval duration in the QTSCD Study. Nat Genet. 2009;41:407-414.
33. Chang KC, Barth AS, Sasano T, Kizana E, Kashiwakura Y, Zhang Y, Foster DB, Marban E. CAPON modulates cardiac repolarization via neuronal nitric oxide synthase signaling in the heart. Proc Natl Acad Sci U S A. 2008;105:4477-4482.
34. Mullins MC, Hammerschmidt M, Haffter P, Nusslein-Volhard C. Large-scale mutagenesis in the zebrafish: in search of genes controlling development in a vertebrate. Curr Biol. 1994;4:189-202.
35. Martin AB, Garson A Jr, Perry JC. Prolonged QT interval in hypertrophic and dilated cardiomyopathy in children. Am Heart J. 1994;127:64-70.
36. Milan DJ, Giokas AC, Serluca FC, Peterson RT, MacRae CA. Notch1b and neuregulin are required for specification of central cardiac conduction tissue. Development. 2006;133:1125-1132.
37. Chen Y, Zhu J, Lum PY, Yang X, Pinto S, MacNeil DJ, Zhang C, Lamb J, Edwards S, Sieberts SK, Leonardson A, Castellini LW, Wang S, Champy MF, Zhang B, Emilsson V, Doss S, Ghazalpour A, Horvath S, Drake TA, Lusis AJ, Schadt EE. Variations in DNA elucidate molecular networks that cause disease. Nature. 2008;452:429-435.
38. Qu X, Jia H, Garrity DM, Tompkins K, Batts L, Appel B, Zhong TP, Baldwin HS. Ndrg4 is required for normal myocyte proliferation during early cardiac development in zebrafish. Dev Biol. 2008;317:486-496.