An internal promoter underlies the difference in disease severity between N-and C-terminal truncation mutations of titin in zebrafish

eLife

Volumn 4, Issue OCTOBER2015, 2015, Pages

  Zou, Jun ^a   Tran, Diana ^a   Baalbaki, Mai ^a   Tang, Ling Fung ^a   Poon, Annie ^a   Pelonero, Angelo ^a   Titus, Erron W ^a   Yuan, Christiana ^a   Shi, Chenxu ^a   Patchava, Shruthi ^a   Halper, Elizabeth ^a   Garg, Jasmine ^a   Movsesyan, Irina ^a   Yin, Chaoying ^b   Wu, Roland ^a,c   Wilsbacher, Lisa D ^a,c,g   Liu, Jiandong ^b   Hager, Ronald L ^d   Coughlin, Shaun R ^a,c   Jinek, Martin ^e   Pullinger, Clive R ^a   Kane, John P ^a,c   Hart, Daniel O ^a,c   Kwok, Pui Yan ^a   Deo, Rahul C ^a,c,f   more..

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d BRIGHAM YOUNG UNIVERSITY   (United States)

^e UNIVERSITY OF ZURICH   (Switzerland)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAS9 IN PROTEIN; CONNECTIN; DEOXYRIBONUCLEASE; HISTONE H3; MORPHOLINO OLIGONUCLEOTIDE; PROTEIN; UNCLASSIFIED DRUG; MUTANT PROTEIN;

ADULT; AGED; AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONFOCAL MICROSCOPY; CONGESTIVE CARDIOMYOPATHY; CONTROLLED STUDY; CRISPR CAS SYSTEM; DISEASE SEVERITY; EMBRYO; EXON; FEMALE; GENE MUTATION; GENE SILENCING; GENETIC TRANSCRIPTION; GENOTYPING TECHNIQUE; HUMAN; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; IN VITRO STUDY; MALE; MOLECULAR CLONING; MOUSE; MYOPATHY; NONHUMAN; NONSENSE MEDIATED MRNA DECAY; PROMOTER REGION; PROTEIN ELECTROPHORESIS; PROTEIN EXPRESSION; RAPID AMPLIFICATION OF 5' COMPLEMENTARY DNA ENDS; REAL TIME POLYMERASE CHAIN REACTION; RNA ANALYSIS; RNA SEQUENCE; SARCOMERE; SKELETAL MYOPATHY; STATISTICAL BIAS; ZEBRA FISH; ANIMAL; DISEASE MODEL; GENE DELETION; GENETICS; METABOLISM; MUSCLE DISEASE; PATHOLOGY;

ANIMALS; CARDIOMYOPATHY, DILATED; CONNECTIN; DISEASE MODELS, ANIMAL; HUMANS; MUSCULAR DISEASES; MUTANT PROTEINS; PROMOTER REGIONS, GENETIC; SEQUENCE DELETION; ZEBRAFISH;

EID: 84949883742     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.09406     Document Type: Article

References (54)

1. Bang M-L, Centner T, Fornoff F, Geach AJ, Gotthardt M, Mcnabb M, Witt CC, Labeit D, Gregorio CC, Granzier H, Labeit S. 2001. The complete gene sequence of titin, expression of an unusual 700-kDa titin isoform, and its interaction with obscurin identify a novel z-line to i-band linking system. Circulation Research 89:1065-1072. doi: 10.1161/hh2301.100981
2. Bullard B, Linke WA, Leonard K. 2002. Varieties of elastic protein in invertebrate muscles. Journal of Muscle Research and Cell Motility 23:435-447. doi: 10.1023/A:1023454305437
3. Carmignac V, Salih MA, Quijano-Roy S, Marchand S, Al Rayess MM, Mukhtar MM, Urtizberea JA, Labeit S, Guicheney P, Leturcq F, Gautel M, Fardeau M, Campbell KP, Richard I, Estournet B, Ferreiro A. 2007. C-terminal titin deletions cause a novel early-onset myopathy with fatal cardiomyopathy. Annals of Neurology 61: 340-351. doi: 10.1002/ana.21089
4. Ceyhan-Birsoy O, Agrawal PB, Hidalgo C, Schmitz-Abe K, DeChene ET, Swanson LC, Soemedi R, Vasli N, Iannaccone ST, Shieh PB, Shur N, Dennison JM, Lawlor MW, Laporte J, Markianos K, Fairbrother WG, Granzier H, Beggs AH. 2013. Recessive truncating titin gene, TTN, mutations presenting as centronuclear myopathy. Neurology 81:1205-1214. doi: 10.1212/WNL.0b013e3182a6ca62
5. Chauveau C, Rowell J, Ferreiro A. 2014. A rising titan: TTN review and mutation update. Human Mutation 35: 1046-1059. doi: 10.1002/humu.22611
6. Codd MB, Sugrue DD, Gersh BJ, Melton LJ. 1989. Epidemiology of idiopathic dilated and hypertrophic cardiomyopathy. a population-based study in olmsted county, minnesota, 1975-1984. Circulation 80:564-572. doi: 10.1161/01.CIR.80.3.564
7. Dahme T, Katus HA, Rottbauer W. 2009. Fishing for the genetic basis of cardiovascular disease. Disease Models & Mechanisms 2:18-22. doi: 10.1242/dmm.000687
8. Deo RC, Musso G, Tasan M, Tang P, Poon A, Yuan C, Felix JF, Vasan RS, Beroukhim R, De Marco T, Kwok P-Y, MacRae CA, Roth FP. 2014. Prioritizing causal disease genes using unbiased genomic features. Genome Biology 15:534 doi: 10.1186/s13059-014-0534-8
9. Furst DO, Osborn M, Nave R, Weber K. 1988. The organization of titin filaments in the half-sarcomere revealed by monoclonal antibodies in immunoelectron microscopy: a map of ten nonrepetitive epitopes starting at the z line extends close to the m line. The Journal of Cell Biology 106:1563-1572. doi: 10.1083/jcb.106.5.1563
10. Gaudet M, Fara A-G, Sabatti M, Kuzminsky E, Mugnozza GS. 2007. Single-reaction for SNP genotyping on agarose gel by allele-specific PCR in black poplar (populus nigra l.). Plant Molecular Biology Reporter 25:1-9. doi: 10.1007/s11105-007-0003-6
11. Geoffrey Burns C, Macrae C. 2006. Purification of hearts from zebrafish embryos. BioTechniques 40:278-282. doi: 10.2144/000112135
12. Gramlich M, Michely B, Krohne C, Heuser A, Erdmann B, Klaassen S, Hudson B, Magarin M, Kirchner F, Todiras M, Granzier H, Labeit S, Thierfelder L, Gerull B. 2009. Stress-induced dilated cardiomyopathy in a knock-in mouse model mimicking human titin-based disease. Journal of Molecular and Cellular Cardiology 47:352-358. doi: 10.1016/j.yjmcc.2009.04.014
13. Gramlich M, Pane LS, Zhou Q, Chen Z, Murgia M, Schötterl S, Goedel A, Metzger K, Brade T, Parrotta E, Schaller M, Gerull B, Thierfelder L, Aartsma-Rus A, Labeit S, Atherton JJ, Mcgaughran J, Harvey RP, Sinnecker D, Mann M, Laugwitz KL, Gawaz MP, Moretti A. 2015. Antisense-mediated exon skipping: a therapeutic strategy for titin-based dilated cardiomyopathy. EMBO Molecular Medicine 7:562-576. doi: 10.15252/emmm.201505047
14. Granzier HL, Labeit S. 2004. The giant protein titin: a major player in myocardial mechanics, signaling, and disease. Circulation Research 94:284-295. doi: 10.1161/01.RES.0000117769.88862.F8
15. Hazebroek MR, Moors S, Dennert R, van den Wijngaard A, Krapels I, Hoos M, Verdonschot J, Merken JJ, de Vries B, Wolffs PF, Crijns HJGM, Brunner-La Rocca H-P, Heymans S, et al. 2015. Prognostic relevance of gene-environment interactions in patients with dilated cardiomyopathy. Journal of the American College of Cardiology 66:1313-1323. doi: 10.1016/j.jacc.2015.07.023
16. Heredia JE, Mukundan L, Chen FM, Mueller AA, Deo RC, Locksley RM, Rando TA, Chawla A, Mueller AA, Deo RC, Locksley RM. 2013. Type 2 innate signals stimulate fibro/adipogenic progenitors to facilitate muscle regeneration. Cell 153:376-388. doi: 10.1016/j.cell.2013.02.053
17. Herman DS, Lam L, Taylor MR, Wang L, Teekakirikul P, Christodoulou D, Conner L, Depalma SR, Mcdonough B, Sparks E, Teodorescu DL, Cirino AL, Banner NR, Pennell DJ, Graw S, Merlo M, di Lenarda A, Sinagra G, Bos JM, Ackerman MJ, Mitchell RN, Murry CE, Lakdawala NK, Ho CY, Barton PJ, Cook SA, Mestroni L, Seidman JG, Seidman CE. 2012. Truncations of titin causing dilated cardiomyopathy. The New England Journal of Medicine 366:619-628. doi: 10.1056/NEJMoa1110186
18. Hinson JT, Chopra A, Nafissi N, Polacheck WJ, Benson CC, Swist S, Gorham J, Yang L, Schafer S, Sheng CC, Haghighi A, Homsy J, Hubner N, Church G, Cook SA, Linke WA, Chen CS, Seidman JG, Seidman CE. 2015. HEART DISEASE. titin mutations in iPS cells define sarcomere insufficiency as a cause of dilated cardiomyopathy. Science 349:982-986. doi: 10.1126/science.aaa5458
19. Hwang WY, Fu Y, Reyon D, Maeder ML, Tsai SQ, Sander JD, Peterson RT, Yeh JR, Joung JK. 2013. Efficient genome editing in zebrafish using a CRISPR-cas system. Nature Biotechnology 31:227-229. doi: 10.1038/nbt.2501
20. Itoh-Satoh M, Hayashi T, Nishi H, Koga Y, Arimura T, Koyanagi T, Takahashi M, Hohda S, Ueda K, Nouchi T, Hiroe M, Marumo F, Imaizumi T, Yasunami M, Kimura A. 2002. Titin mutations as the molecular basis for dilated cardiomyopathy. Biochemical and Biophysical Research Communications 291:385-393. doi: 10.1006/bbrc.2002.6448
21. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. 2012. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337:816-821. doi: 10.1126/science.1225829
22. Kakaradov B, Xiong H, Lee LJ, Jojic N, Frey BJ. 2012. Challenges in estimating percent inclusion of alternatively spliced junctions from RNA-seq data. BMC Bioinformatics 13:S11 doi: 10.1093/bioinformatics/btp120
23. Lahmers S, Wu Y, Call DR, Labeit S, Granzier H. 2004. Developmental control of titin isoform expression and passive stiffness in fetal and neonatal myocardium. Circulation Research 94:505-513. doi: 10.1161/01.RES.0000115522.52554.86
24. Lewinter MM, Granzier HL. 2013. Titin is a major human disease gene. Circulation 127:938-944. doi: 10.1161/CIRCULATIONAHA.112.139717
25. Li H, Durbin R. 2009. Fast and accurate short read alignment with burrows-wheeler transform. Bioinformatics 25: 1754-1760. doi: 10.1093/bioinformatics/btp324
26. Liversage AD, Holmes D, Knight PJ, Tskhovrebova L, Trinick J. 2001. Titin and the sarcomere symmetry paradox. Journal of Molecular Biology 305:401-409. doi: 10.1006/jmbi.2000.4279
27. Matz M, Shagin D, Bogdanova E, Britanova O, Lukyanov S, Diatchenko L, et al. 1999. Amplification of cDNA ends based on template-switching effect and step-out PCR. Nucleic Acids Research 27:1558-1560. doi: 10.1093/nar/27.6.1558
28. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo MA. 2010. The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Research 20:1297-1303. doi: 10.1101/gr.107524.110
29. Myhre JL, Hills JA, Prill K, Wohlgemuth SL, Pilgrim DB. 2014. The titin a-band rod domain is dispensable for initial thick filament assembly in zebrafish. Developmental Biology 387:93-108. doi: 10.1016/j.ydbio.2013.12.020
30. Neph S, Vierstra J, Stergachis AB, Reynolds AP, Haugen E, Vernot B,. 2013. An expansive human regulatory lexicon encoded in transcription factor footprints. Nature 488:83-90.
31. Norton N, Li D, Rampersaud E, Morales A, Martin ER, Zuchner S, Guo S, Gonzalez M, Hedges DJ, Robertson PD, Krumm N, Nickerson DA, Hershberger RE. National Heart, Lung, and Blood Institute GO Exome Sequencing Project and the Exome Sequencing Project Family Studies Project TeamNational Heart, Lung, and Blood Institute GO Exome Sequencing Project and the Exome Sequencing Project Family Studies Project Team. 2013. Exome sequencing and genome-wide linkage analysis in 17 families illustrate the complex contribution of TTN truncating variants to dilated cardiomyopathy. Circulation. Cardiovascular Genetics 6:144-153. doi: 10.1161/CIRCGENETICS.111.000062
32. Oleykowski CA, Bronson Mullins CR, Godwin AK, Yeung AT. 1998. Mutation detection using a novel plant endonuclease. Nucleic Acids Research 26:4597-4602. doi: 10.1093/nar/26.20.4597
33. Opitz CA, Leake MC, Makarenko I, Benes V, Linke WA. 2004. Developmentally regulated switching of titin size alters myofibrillar stiffness in the perinatal heart. Circulation Research 94:967-975. doi: 10.1161/01.RES.0000124301.48193.E1
34. Pervouchine DD, Knowles DG, Guigo R. 2013. Intron-centric estimation of alternative splicing from RNA-seq data. Bioinformatics. Oxford University Press 29:273-274. doi: 10.1093/bioinformatics/bts678
35. Picelli S, Faridani OR, Askbo R, Winberg GOS, Sagasser S, Sandberg R. 2014. Full-length RNA-seq from single cells using smart-seq2. Nature Publishing Group 9:171-181.
36. Pringle JW. 1968. Mechano-chemical transformation in striated muscle. Symposia of the Society for Experimental Biology 22:67-86.
37. Radke MH, Peng J, Wu Y, Mcnabb M, Nelson OL, Granzier H, Gotthardt M. 2007. Targeted deletion of titin N2B region leads to diastolic dysfunction and cardiac atrophy. Proceedings of the National Academy of Sciences of the USA of America 104:3444-3449. doi: 10.1073/pnas.0608543104
38. Richards S, Aziz N, Bale S, Bick D, Das S, Gastier-Foster J, Grody WW, Hegde M, Lyon E, Spector E, Voelkerding K, Rehm HL, Gastier-Foster J. 2015. Standards and guidelines for the interpretation of sequence variants: a joint consensus recommendation of the american college of medical genetics and genomics and the association for molecular pathology. Genetics in Medicine 17:405-423. doi: 10.1038/gim.2015.30
39. Roberts AM, Ware JS, Herman DS, Schafer S, Baksi J, Bick AG, Buchan RJ, Walsh R, John S, Wilkinson S, Mazzarotto F, Felkin LE, Gong S, Macarthur JA, Cunningham F, Flannick J, Gabriel SB, Altshuler DM, Macdonald PS, Heinig M, Keogh AM, Hayward CS, Banner NR, Pennell DJ, O’Regan DP, San TR, de Marvao A, Dawes TJ, Gulati A, Birks EJ, Yacoub MH, Radke M, Gotthardt M, Wilson JG, O’Donnell CJ, Prasad SK, Barton PJ, Fatkin D, Hubner N, Seidman JG, Seidman CE, Cook SA. 2015. Integrated allelic, transcriptional, and phenomic dissection of the cardiac effects of titin truncations in health and disease. Science Translational Medicine 7:270ra6. doi: 10.1126/scitranslmed.3010134
40. Robinson MD, Mccarthy DJ, Smyth GK. 2010. EdgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics (Oxford, England) 26:139-140. doi: 10.1093/bioinformatics/btp616
41. Robu ME, Larson JD, Nasevicius A, Beiraghi S, Brenner C, Farber SA, Ekker SC. 2007. P53 activation by knockdown technologies. PLoS Genetics 3:e78-e78. doi: 10.1371/journal.pgen.0030078
42. Seeley M, Huang W, Chen Z, Wolff WO, Lin X, Xu X. 2007. Depletion of zebrafish titin reduces cardiac contractility by disrupting the assembly of z-discs and a-bands. Circulation Research 100:238-245. doi: 10.1161/01.RES.0000255758.69821.b5
43. Steffen LS, Guyon JR, Vogel ED, Howell MH, Zhou Y, Weber GJ, Zon LI, Kunkel LM. 2007. The zebrafish runzel muscular dystrophy is linked to the titin gene. Developmental Biology 309:180-192. doi: 10.1016/j.ydbio.2007.06.015
44. Thisse C, Thisse B. 2008. High-resolution in situ hybridization to whole-mount zebrafish embryos. Nature Protocols 3:59-69. doi: 10.1038/nprot.2007.514
45. Traeger L, Mackenzie JM, Epstein HF, Goldstein MA. 1983. Transition in the thin-filament arrangement in rat skeletal muscle. Journal of Muscle Research and Cell Motility 4:353-366.
46. Trapnell C, Pachter L, Salzberg SL. 2009. TopHat: discovering splice junctions with RNA-seq. Bioinformatics 25: 1105-1111. doi: 10.1093/bioinformatics/btp120
47. van der Ven PF, Bartsch JW, Gautel M, Jockusch H, Fürst DO. 2000. A functional knock-out of titin results in defective myofibril assembly. Journal of Cell Science 113:1405-1414.
48. van Spaendonck-Zwarts KY, Posafalvi A, van den Berg MP, Hilfiker-Kleiner D, Bollen IA, Sliwa K, Alders M, Almomani R, van Langen IM, van der Meer P, Sinke RJ, van der Velden J, van Veldhuisen DJ, van Tintelen JP, Jongbloed JD. 2014. Titin gene mutations are common in families with both peripartum cardiomyopathy and dilated cardiomyopathy. European Heart Journal 35:2165-2173. doi: 10.1093/eurheartj/ehu050
49. Warren CM, Krzesinski PR, Greaser ML. 2003. Vertical agarose gel electrophoresis and electroblotting of high-molecular-weight proteins. Electrophoresis 24:1695-1702. doi: 10.1002/elps.200305392
50. Westerfield M. 1993. The zebrafish book: a guide for the laboratory use of zebrafish (brachydanio rerio).
51. Wickham H. 2009. Ggplot2. New York: NY: Springer Science & Business Media
52. Xu X, Meiler SE, Zhong TP, Mohideen M, Crossley DA, Burggren WW, Fishman MC. 2002. Cardiomyopathy in zebrafish due to mutation in an alternatively spliced exon of titin. Nature Genetics 30:205-209. doi: 10.1038/ng816
53. Zetoune AB, Fontaniére S, Magnin D, Anczuków O, Buisson M, Zhang CX, Mazoyer S, et al. 2008. Comparison of nonsense-mediated mRNA decay efficiency in various murine tissues. BMC Genetics 9:83-11. doi: 10.1186/1471-2156-9-83
54. Zhou VW, Goren A, Bernstein BE. 2011. Charting histone modifications and the functional organization of mammalian genomes. Nature Reviews Genetics 12:7-18. doi: 10.1038/nrg2905