Advanced echocardiography in adult zebrafish reveals delayed recovery of heart function after myocardial cryoinjury

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Hein, Selina J ^a,b   Lehmann, Lorenz H ^a,b   Kossack, Mandy ^a,b   Juergensen, Lonny ^a,b   Fuchs, Dieter ^c   Katus, Hugo A ^a,b   Hassel, David ^a,b  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^b DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

^c Sonics Inc   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ATENOLOL; GREEN FLUORESCENT PROTEIN; ISOPRENALINE;

ACUTE HEART FAILURE; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIAC IMAGING; CARDIAC REGENERATION; COLD INJURY; CONTROLLED STUDY; DISEASE MODEL; ECHOCARDIOGRAPH; ECHOCARDIOGRAPHY; HEART EJECTION FRACTION; HEART FUNCTION; HEART MUSCLE; HEART MUSCLE INJURY; HEART OUTPUT; HEART PERFORMANCE; HEART RATE; HEART STROKE VOLUME; HEART VENTRICLE CONTRACTILITY; HEART VENTRICLE SIZE; HEART VENTRICLE WALL MOTION; HISTOLOGY; IMAGE ANALYSIS; IMAGING SOFTWARE; NONHUMAN; OPTICAL RESOLUTION; SPECKLE TRACKING ANALYSIS; TISSUE REGENERATION; ZEBRA FISH; ANIMAL; CARDIOVASCULAR FUNCTION; GROWTH, DEVELOPMENT AND AGING; HEART; HEART VENTRICLE; HUMAN; MYOCARDIAL INFARCTION; PATHOPHYSIOLOGY; PHYSIOLOGY; REGENERATION;

DANIO RERIO;

ANIMALS; CARDIOVASCULAR PHYSIOLOGICAL PHENOMENA; DISEASE MODELS, ANIMAL; ECHOCARDIOGRAPHY; HEART; HEART VENTRICLES; HUMANS; MYOCARDIAL INFARCTION; REGENERATION; ZEBRAFISH;

EID: 84928963683     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0122665     Document Type: Article

References (59)

1. Bakkers J. Zebrafish as a model to study cardiac development and human cardiac disease. Cardiovascular research. 2011; 91(2):279-88. doi: 10.1093/cvr/cvr098 PMID: 21602174; PubMed Central PMCID: PMC3125074.
2. Staudt D, Stainier D. Uncovering the molecular and cellular mechanisms of heart development using the zebrafish. Annual review of genetics. 2012; 46:397-418. doi: 10.1146/annurev-genet-110711-155646 PMID: 22974299.
3. Santoriello C, Zon LI. Hooked! Modeling human disease in zebrafish. The Journal of clinical investigation. 2012; 122(7):2337-43. doi: 10.1172/JCI60434 PMID: 22751109; PubMed Central PMCID: PMC3386812.
4. Hassel D, Dahme T, Erdmann J, Meder B, Huge A, Stoll M, et al. Nexilin mutations destabilize cardiac Z-disks and lead to dilated cardiomyopathy. Nature medicine. 2009; 15(11):1281-8. doi: 10.1038/nm.2037 PMID: 19881492.
5. Stainier DY, Fouquet B, Chen JN, Warren KS, Weinstein BM, Meiler SE, et al. Mutations affecting the formation and function of the cardiovascular system in the zebrafish embryo. Development. 1996; 123:285-92. PMID: 9007248.
6. Jao LE, Wente SR, Chen W. Efficient multiplex biallelic zebrafish genome editing using a CRISPR nuclease system. Proceedings of the National Academy of Sciences of the United States of America. 2013; 110(34):13904-9. doi: 10.1073/pnas.1308335110 PMID: 23918387; PubMed Central PMCID: PMC3752207.
7. Hwang WY, Fu Y, Reyon D, Maeder ML, Tsai SQ, Sander JD, et al. Efficient genome editing in zebrafish using a CRISPR-Cas system. Nature biotechnology. 2013; 31(3):227- 9. doi: 10.1038/nbt.2501 PMID: 23360964; PubMed Central PMCID: PMC3686313.
8. Cade L, Reyon D, Hwang WY, Tsai SQ, Patel S, Khayter C, et al. Highly efficient generation of heritable zebrafish gene mutations using homo- and heterodimeric TALENs. Nucleic acids research. 2012; 40(16):8001-10. doi: 10.1093/nar/gks518 PMID: 22684503; PubMed Central PMCID: PMC3439908.
9. Ding Y, Sun X, Xu X. TOR-autophagy signaling in adult zebrafish models of cardiomyopathy. Autophagy. 2012; 8(1):142-3. doi: 10.4161/auto.8.1.18536 PMID: 22186229; PubMed Central PMCID: PMC3335998.
10. Sun X, Hoage T, Bai P, Ding Y, Chen Z, Zhang R, et al. Cardiac hypertrophy involves both myocyte hypertrophy and hyperplasia in anemic zebrafish. PloS one. 2009; 4(8):e6596. doi: 10.1371/journal.pone.0006596 PMID: 19672293; PubMed Central PMCID: PMC2719798.
11. Kalogirou S, Malissovas N, Moro E, Argenton F, Stainier DY, Beis D. Intracardiac Flow Dynamics Regulate Atrioventricular Valve Morphogenesis. Cardiovascular research. 2014. doi: 10.1093/cvr/cvu186 PMID: 25100766.
12. Xiong JW, Chang NN. Recent advances in heart regeneration. Birth defects research Part C, Embryo today: reviews. 2013; 99(3):160-9. doi: 10.1002/bdrc.21039 PMID: 24078494.
13. Fang Y, Gupta V, Karra R, Holdway JE, Kikuchi K, Poss KD. Translational profiling of cardiomyocytes identifies an early Jak1/Stat3 injury response required for zebrafish heart regeneration. Proceedings ofthe National Academy of Sciences of the United States of America. 2013; 110(33):13416-21. doi: 10. 1073/pnas.1309810110 PMID: 23901114; PubMed Central PMCID: PMC3746860.
14. Yin VP, Lepilina A, Smith A, Poss KD. Regulation of zebrafish heart regeneration by miR-133. Developmental biology. 2012; 365(2):319-27. doi: 10.1016/j.ydbio.2012.02.018 PMID: 22374218; PubMed Central PMCID: PMC3342384.
15. Kikuchi K, Holdway JE, Werdich AA, Anderson RM, Fang Y, Egnaczyk GF, et al. Primary contribution to zebrafish heart regeneration by gata4(+) cardiomyocytes. Nature. 2010; 464(7288):601-5. doi: 10. 1038/nature08804 PMID: 20336144; PubMed Central PMCID: PMC3040215.
16. Jopling C, Sleep E, Raya M, Marti M, Raya A, Izpisua Belmonte JC. Zebrafish heart regeneration occurs by cardiomyocyte dedifferentiation and proliferation. Nature. 2010; 464(7288):606-9. doi: 10. 1038/nature08899 PMID: 20336145; PubMed Central PMCID: PMC2846535.
17. Poss KD. Getting to the heart of regeneration in zebrafish. Seminars in cell & developmental biology. 2007; 18(1):36-45. doi: 10.1016/j.semcdb.2006.11.009 PMID: 17178459.
18. Poss KD, Wilson LG, Keating MT. Heart regeneration in zebrafish. Science. 2002; 298(5601):2188-90.doi: 10.1126/science.1077857 PMID: 12481136.
19. Hoage T, Ding Y, Xu X. Quantifying cardiac functions in embryonic and adult zebrafish. Methods in molecular biology. 2012; 843:11-20. doi: 10.1007/978-1-61779-523-7-2 PMID: 22222517; PubMed Central PMCID: PMC3762588.
20. Rao KD, Alex A, Verma Y, Thampi S, Gupta PK. Real-time in vivo imaging of adult zebrafish brain using optical coherence tomography. Journal of biophotonics. 2009; 2(5):288-91. doi: 10.1002/jbio.200910032 PMID: 19434615.
21. Sun L, Lien CL, Xu X, Shung KK. In vivo cardiac imaging of adult zebrafish using high frequency ultrasound (45-75 MHz). Ultrasound in medicine & biology. 2008; 34(1):31-9. doi: 10.1016/j.ultrasmedbio. 2007.07.002 PMID: 17825980; PubMed Central PMCID: PMC2292109.
22. Kabli S, Alia A, Spaink HP, Verbeek FJ, De Groot HJ. Magnetic resonance microscopy of the adult zebrafish. Zebrafish. 2006; 3(4):431-9. doi: 10.1089/zeb.2006.3.431 PMID: 18377223.
23. Zhou X, Sun L, Yu Y, Qiu W, Lien CL, Shung KK, et al. Ultrasound bio-microscopic image segmentation for evaluation of zebrafish cardiac function. IEEE transactions on ultrasonics, ferroelectrics, and frequency control. 2013; 60(4):718-26. doi: 10.1109/TUFFC.2013.2620 PMID: 23549532; PubMed Central PMCID: PMC3750995.
24. Parente V, Balasso S, Pompilio G, Verduci L, Colombo GI, Milano G, et al. Hypoxia/reoxygenation cardiac injury and regeneration in zebrafish adult heart. PloS one. 2013; 8(1):e53748. doi: 10.1371/ journal.pone.0053748 PMID: 23341992; PubMed Central PMCID: PMC3547061.
25. Wang J, Panakova D, Kikuchi K, Holdway JE, Gemberling M, Burris JS, et al. The regenerative capacity of zebrafish reverses cardiac failure caused by genetic cardiomyocyte depletion. Development. 2011; 138(16):3421-30. doi: 10.1242/dev.068601 PMID: 21752928; PubMed Central PMCID: PMC3143562.
26. Sun L, Lien C- L, Wu Q, Chang JH, Shung KK. Longitudinal study of adult zebrafish heart regeneration using high frequency echocardiography. 2008 IEEE Ultrasonics Symposium (IUS); Aug 26: IEEE;2008. p. 1738-41.
27. Ho YL, Shau YW, Tsai HJ, Lin LC, Huang PJ, Hsieh FJ. Assessment of zebrafish cardiac performance using Doppler echocardiography and power angiography. Ultrasound in medicine & biology. 2002; 28 (9):1137-43. PMID: 12401383.
28. Schnabel K, Wu CC, Kurth T, Weidinger G. Regeneration of cryoinjury induced necrotic heart lesions in zebrafish is associated with epicardial activation and cardiomyocyte proliferation. PloS one. 2011; 6(4): e18503. doi: 10.1371/journal.pone.0018503 PMID: 21533269; PubMed Central PMCID: PMC3075262.
29. Gonzalez-Rosa JM, Martin V, Peralta M, Torres M, Mercader N. Extensive scar formation and regression during heart regeneration after cryoinjury in zebrafish. Development. 2011; 138(9):1663-74. doi: 10.1242/dev.060897 PMID: 21429987.
30. Chablais F, Veit J, Rainer G, Jazwinska A. The zebrafish heart regenerates after cryoinjury-induced myocardial infarction. BMC developmental biology. 2011; 11:21. doi: 10.1186/1471-213X-11-21 PMID: 21473762; PubMed Central PMCID: PMC3078894.
31. Bauer M, Cheng S, Jain M, Ngoy S, Theodoropoulos C, Trujillo A, et al. Echocardiographic speckletracking based strain imaging for rapid cardiovascular phenotyping in mice. Circulation research. 2011; 108(8):908-16. doi: 10.1161/CIRCRESAHA.110.239574 PMID: 21372284; PubMed Central PMCID: PMC3376717.
32. Lee SC, Lee J, Jin DK, Kim JS, Jeon ES, Kwun YH, et al. Improvement of cardiac function by shortterm enzyme replacement therapy in a murine model of cardiomyopathy associated with Hunter syndrome evaluated by serial echocardiography with speckle tracking 2-D strain analysis. Molecular genetics and metabolism. 2014. doi: 10.1016/j.ymgme.2014.04.005 PMID: 24836711.
33. Dragulescu A, Friedberg MK, Grosse-Wortmann L, Redington A, Mertens L. Effect of Chronic Right Ventricular Volume Overload on Ventricular Interaction in Patients after Tetralogy of Fallot Repair. Journal of the American Society of Echocardiography: official publication of the American Society of Echocardiography.2014. doi: 10.1016/j.echo.2014.04.012 PMID: 24846007.
34. Blessberger H, Binder T. NON-invasive imaging: Two dimensional speckle tracking echocardiography: basic principles. Heart. 2010; 96(9):716-22. doi: 10.1136/hrt.2007.141002 PMID: 20424157.
35. Nanna M, Nanna G. Recent developments in echocardiographic imaging. Current opinion in cardiology.2014. doi: 10.1097/HCO.0000000000000095 PMID: 25046004.
36. Geyer H, Caracciolo G, Abe H, Wilansky S, Carerj S, Gentile F, et al. Assessment of myocardial mechanics using speckle tracking echocardiography: fundamentals and clinical applications. Journal of the American Society of Echocardiography: official publication of the American Society of Echocardiography. 2010; 23(4):351-69; quiz 453-5. doi: 10.1016/j.echo.2010.02.015 PMID: 20362924.
37. Westerfield M. The Zebrafish Book. A Guide for the Laboratory Use of Zebrafish (Danio rerio), 3rd Edition. Eugene, OR, University of Oregon Press, 385 (Book). 1995.
38. Burns CG, Milan DJ, Grande EJ, RottbauerW, MacRae CA, Fishman MC. High-throughput assay for small molecules that modulate zebrafish embryonic heart rate. Nature chemical biology. 2005; 1(5): 263-4. doi: 10.1038/nchembio732 PMID: 16408054.
39. Huang WC, Hsieh YS, Chen IH, Wang CH, Chang HW, Yang CC, et al. Combined use of MS-222 (tricaine) and isoflurane extends anesthesia time and minimizes cardiac rhythm side effects in adult zebrafish. Zebrafish. 2010; 7(3):297-304. doi: 10.1089/zeb.2010.0653 PMID: 20807039.
40. Sonics V. VisualSonics Vevo2100 Imaging System-Operator Manual. http://teststruct.uib.no:8080/ filearchive/vevo2100-manual.pdf].
41. Dandel M, Lehmkuhl H, Knosalla C, Suramelashvili N, Hetzer R. Strain and strain rate imaging by echocardiography-basic concepts and clinical applicability. Current cardiology reviews. 2009; 5(2): 133-48. doi: 10.2174/157340309788166642 PMID: 20436854; PubMed Central PMCID: PMC2805816.
42. D'Hooge J, Heimdal A, Jamal F, Kukulski T, Bijnens B, Rademakers F, et al. Regional strain and strain rate measurements by cardiac ultrasound: principles, implementation and limitations. European journal of echocardiography: the journal of the Working Group on Echocardiography of the European Society of Cardiology. 2000; 1(3):154-70. doi: 10.1053/euje.2000.0031 PMID: 11916589.
43. Hu N, Yost HJ, Clark EB. Cardiac morphology and blood pressure in the adult zebrafish. The Anatomical record. 2001; 264(1):1-12. PMID: 11505366.
44. Hu N, Sedmera D, Yost HJ, Clark EB. Structure and function of the developing zebrafish heart. The Anatomical record. 2000; 260(2):148-57. PMID: 10993952.
45. Mahmoud AM, Sandoval C, Teng B, Schnermann JB, Martin KH, Mustafa SJ, et al. High-resolution vascular tissue characterization in mice using 55MHz ultrasound hybrid imaging. Ultrasonics. 2013; 53(3): 727-38. doi: 10.1016/j.ultras.2012.10.017 PMID: 23218908; PubMed Central PMCID: PMC3639478.
46. Foster FS, Mehi J, Lukacs M, Hirson D, White C, Chaggares C, et al. A new 15-50 MHz array-based micro-ultrasound scanner for preclinical imaging. Ultrasound in medicine & biology. 2009; 35(10): 1700-8. doi: 10.1016/j.ultrasmedbio.2009.04.012 PMID: 19647922.
47. Swillens A, Segers P, Torp H, Lovstakken L. Two-dimensional blood velocity estimation with ultrasound: speckle tracking versus crossed-beam vector Doppler based on flow simulations in a carotid bifurcation model. IEEE transactions on ultrasonics, ferroelectrics, and frequency control. 2010; 57(2): 327-39. doi: 10.1109/TUFFC.2010.1413 PMID: 20178899.
48. Goertz DE, Christopher DA, Yu JL, Kerbel RS, Burns PN, Foster FS. High-frequency color flow imaging of the microcirculation. Ultrasound in medicine & biology. 2000; 26(1):63-71. PMID: 10687794.
49. Teske AJ, De Boeck BW, Melman PG, Sieswerda GT, Doevendans PA, Cramer MJ. Echocardiographic quantification of myocardial function using tissue deformation imaging, a guide to image acquisition and analysis using tissue Doppler and speckle tracking. Cardiovascular ultrasound. 2007; 5:27. doi: 10. 1186/1476-7120-5-27 PMID: 17760964; PubMed Central PMCID: PMC2000459.
50. Zhang KW, French B, May Khan A, Plappert T, Fang JC, Sweitzer NK, et al. Strain improves risk prediction beyond ejection fraction in chronic systolic heart failure. J Am Heart Assoc. 3(1):e000550. Epub 2014/01/15. jah3397 [pii]. PMID: 24419736. doi: 10.1161/JAHA.113.000550
51. Liu J, Stainier DY. Zebrafish in the study of early cardiac development. Circulation research. 2012; 110(6):870-4. doi: 10.1161/CIRCRESAHA.111.246504 PMID: 22427324; PubMed Central PMCID: PMC3329892.
52. Huttner IG, Trivedi G, Jacoby A, Mann SA, Vandenberg JI, Fatkin D. A transgenic zebrafish model of a human cardiac sodium channel mutation exhibits bradycardia, conduction-system abnormalities andearly death. Journal of molecular and cellular cardiology. 2013; 61:123-32. doi: 10.1016/j.yjmcc.2013. 06.005 PMID: 23791817.
53. Volkers M, Dolatabadi N, Gude N, Most P, Sussman MA, Hassel D. Orai1 deficiency leads to heart failure and skeletal myopathy in zebrafish. Journal of cell science. 2012; 125(Pt 2):287-94. doi: 10.1242/ jcs.090464 PMID: 22302996; PubMed Central PMCID: PMC3283868.
54. Mercer SE, Odelberg SJ, Simon HG. A dynamic spatiotemporal extracellular matrix facilitates epicardialmediated vertebrate heart regeneration. Developmental biology. 2013; 382(2):457-69. doi: 10.1016/j. ydbio.2013.08.002 PMID: 23939298; PubMed Central PMCID: PMC3957425.
55. Blessberger H, Binder T. Two dimensional speckle tracking echocardiography: clinical applications. Heart. 2010; 96(24):2032-40. doi: 10.1136/hrt.2010.199885 PMID: 21088126.
56. Chi NC, Bussen M, Brand-Arzamendi K, Ding C, Olgin JE, Shaw RM, et al. Cardiac conduction is required to preserve cardiac chamber morphology. Proceedings of the National Academy of Sciences of the United States of America. 2010; 107(33):14662-7. doi: 10.1073/pnas.0909432107 PMID: 20675583; PubMed Central PMCID: PMC2930423.
57. Auman HJ, Coleman H, Riley HE, Olale F, Tsai HJ, Yelon D. Functional modulation of cardiac form through regionally confined cell shape changes. PLoS biology. 2007; 5(3):e53. doi: 10.1371/journal. pbio.0050053 PMID: 17311471; PubMed Central PMCID: PMC1802756.
58. Thorstensen A, Dalen H, Amundsen BH, Stoylen A. Peak systolic velocity indices are more sensitive than end-systolic indices in detecting contraction changes assessed by echocardiography in young healthy humans. European journal of echocardiography: the journal of the Working Group on Echocardiography of the European Society of Cardiology. 2011; 12(12):924-30. doi: 10.1093/ejechocard/ jer178 PMID: 21940728.
59. Lepilina A, Coon AN, Kikuchi K, Holdway JE, Roberts RW, Burns CG, et al. A dynamic epicardial injury response supports progenitor cell activity during zebrafish heart regeneration. Cell. 2006; 127(3): 607-19. doi: 10.1016/j.cell.2006.08.052 PMID: 17081981.