In Vivo Imaging of the Adult Drosophila melanogaster Heart With Real-Time Optical Coherence Tomography
2006; Lippincott Williams & Wilkins; Volume: 114; Issue: 2 Linguagem: Inglês
10.1161/circulationaha.105.593541
ISSN1524-4539
AutoresMichael A. Choma, Susan Izatt, Robert Wessells, Rolf Bodmer, Joseph A. Izatt,
Tópico(s)Insect behavior and control techniques
ResumoHomeCirculationVol. 114, No. 2In Vivo Imaging of the Adult Drosophila melanogaster Heart With Real-Time Optical Coherence Tomography Free AccessReview ArticlePDF/EPUBAboutView PDFView EPUBSections ToolsAdd to favoritesDownload citationsTrack citationsPermissionsDownload Articles + Supplements ShareShare onFacebookTwitterLinked InMendeleyReddit Jump toSupplemental MaterialFree AccessReview ArticlePDF/EPUBIn Vivo Imaging of the Adult Drosophila melanogaster Heart With Real-Time Optical Coherence Tomography Michael A. Choma, Susan D. Izatt, Robert J. Wessells, Rolf Bodmer and Joseph A. Izatt Michael A. ChomaMichael A. Choma From the Departments of Biomedical Engineering (M.A.C., J.A.I.) and Pediatrics (S.D.I.), Duke University, Durham, NC, and The Burnham Institute (R.J.W., R.B.), La Jolla, Calif. , Susan D. IzattSusan D. Izatt From the Departments of Biomedical Engineering (M.A.C., J.A.I.) and Pediatrics (S.D.I.), Duke University, Durham, NC, and The Burnham Institute (R.J.W., R.B.), La Jolla, Calif. , Robert J. WessellsRobert J. Wessells From the Departments of Biomedical Engineering (M.A.C., J.A.I.) and Pediatrics (S.D.I.), Duke University, Durham, NC, and The Burnham Institute (R.J.W., R.B.), La Jolla, Calif. , Rolf BodmerRolf Bodmer From the Departments of Biomedical Engineering (M.A.C., J.A.I.) and Pediatrics (S.D.I.), Duke University, Durham, NC, and The Burnham Institute (R.J.W., R.B.), La Jolla, Calif. and Joseph A. IzattJoseph A. Izatt From the Departments of Biomedical Engineering (M.A.C., J.A.I.) and Pediatrics (S.D.I.), Duke University, Durham, NC, and The Burnham Institute (R.J.W., R.B.), La Jolla, Calif. Originally published11 Jul 2006https://doi.org/10.1161/CIRCULATIONAHA.105.593541Circulation. 2006;114:e35–e36Over the past century, research involving the fruit fly Drosophila melanogaster has consistently yielded fundamental insights into the nature of complex organisms. The cardiovascular sciences have benefited from these discoveries. Examples include the discovery of the human ether-a-go-go inward rectifying potassium channel, a fly homologue of HERG that is implicated in inherited long-QT syndrome, and the tinman protein, a fly homologue of NKX2.5 that is responsible for certain congential atrial septal defects and conduction abnormalities. More recent results, such as those involving the insulin regulation of heart function in aging fruit flies, suggest that D melanogaster is an emerging model organism in cardiac disease. To date, functional studies of the adult D melanogaster heart have been difficult, and in vivo cross-sectional imaging has been essentially impossible. Here, we present real-time in vivo B- and M-mode optical coherence tomography (OCT) images of wild-type (OreR) D melanogaster heat tubes. Our OCT system has axial and lateral resolution of 10 μm and 23 μm, respectively, a B-mode frame rate of 8 to 20 per second, and an M-mode line rate of 4000 per second. Flies were anesthetized with FlyNap (Carolina Biological, Burlington, NC) for examination. Numbered figures represent different flies. Figure 1 and Movies I and II show transverse and sagittal B-scans of the heat tube during systole and diastole. M-mode images were taken at the landmark indicated by the line in Figure 1C. Figure 2 shows a 1-second M-scan. From the M-scan, the heart rate is determined to be 360 beats per minute (beat-to-beat interval of 167 milliseconds), and the shortening fraction to be 67%. Figure 3 and Movie III show intermittent arrhythmia and asystole occasionally noted immediately after induction of anesthesia. These images suggest that D melanogaster can be readily used as a model organism in genetic and genomic studies of cardiovascular disease including heart failure and arrhythmia. Download figureDownload PowerPointFigure 1. Transverse (A, B) and sagittal (C, D) real-time OCT images of D melanogaster dorsal heart tube of the anterior abdomen in diastole (A, C) and systole (B, D). The solid arrow points to the conical chamber in the anterior portion of the abdomen, wheras the dashed arrow points to distal portions of the heart tube. The vertical line marked by m indicates the location of M-mode image acquisition. The inset in B shows the heart tube at 2× image magnification. Scale bars=100 μm.Download figureDownload PowerPointFigure 2. A, M-mode image of dorsal heart tube taken over 1 second. This image is composed of 4000 A lines. The heart completes 6 cardiac cycles over the course of this second (heart rate=360 bpm). B and C are 68-ms segments of A when the heart tube is in diastole and systole, respectively. These scans indicate that the diameter of the tube changes by a factor of 3 when contracting. This corresponds to a shortening fraction of 67% at the position indicated in Figure 1C.Download figureDownload PowerPointFigure 3. Arrhythmia in D melanogaster observed with M-mode imaging. A, Heart tube is in asystole for the first 400 ms, after which regular rhythm is resumed. B, Irregular rate present at 0 ms and 750 ms.The online-only Data Supplement, which contains 3 movies, can be found at http://circ.ahajournals.org/cgi/content/full/114/2/e35/DC1.Sources of FundingThis work was supported by National Institutes of Health grant R24-EB00243, "Partnership for Research in Optical Coherence Tomography."DisclosuresDr J. Izatt is a cofounder, officer, and major stockholder in Bioptigen, Inc, which has commercialized an advanced version of the instrument used in this study. Duke University has licensed intellectual property to and holds equity in Bioptigen, Inc.FootnotesCorrespondence to Michael A. Choma, PhD, Department of Biomedical Engineering, Duke University, 136 Hudson Hall, PO Box 90281, Durham, NC 27708–0281. Email [email protected]. eLetters(0)eLetters should relate to an article recently published in the journal and are not a forum for providing unpublished data. Comments are reviewed for appropriate use of tone and language. Comments are not peer-reviewed. Acceptable comments are posted to the journal website only. Comments are not published in an issue and are not indexed in PubMed. Comments should be no longer than 500 words and will only be posted online. References are limited to 10. Authors of the article cited in the comment will be invited to reply, as appropriate.Comments and feedback on AHA/ASA Scientific Statements and Guidelines should be directed to the AHA/ASA Manuscript Oversight Committee via its Correspondence page.Sign In to Submit a Response to This Article Previous Back to top Next FiguresReferencesRelatedDetailsCited By Chakraborty A, Peterson N, King J, Gross R, Pla M, Thennavan A, Zhou K, DeLuca S, Bursac N, Bowles D, Wolf M and Fox D (2023) Conserved chamber-specific polyploidy maintains heart function in Drosophila , Development, 10.1242/dev.201896, 150:16, Online publication date: 15-Aug-2023. Zhu J, Liu C, Huang X, van de Leemput J, Lee H and Han Z (2023) H3K36 Di-Methylation Marks, Mediated by Ash1 in Complex with Caf1-55 and MRG15, Are Required during Drosophila Heart Development, Journal of Cardiovascular Development and Disease, 10.3390/jcdd10070307, 10:7, (307) Shukla A, Scott A and Giniger E (2022) Invertebrate model organisms for aging research Anti-Aging Drug Discovery on the Basis of Hallmarks of Aging, 10.1016/B978-0-323-90235-9.00004-5, (353-382), . Vavakou A, Scherberich J, Nowotny M and van der Heijden M (2021) Tuned vibration modes in a miniature hearing organ: Insights from the bushcricket, Proceedings of the National Academy of Sciences, 10.1073/pnas.2105234118, 118:39, Online publication date: 28-Sep-2021. Göttler C, Amador G, van de Kamp T, Zuber M, Böhler L, Siegwart R and Sitti M (2021) Fluid mechanics and rheology of the jumping spider body fluid, Soft Matter, 10.1039/D1SM00338K, 17:22, (5532-5539) Purevjav E (2020) Animal Models of Cardiomyopathies Animal Models in Medicine and Biology, 10.5772/intechopen.89033 Su Y, Wei L, Tan H, Li J, Li W, Fu L, Wang T, Kang L and Yao X (2019) Optical coherence tomography as a noninvasive 3D real time imaging tool for the rapid evaluation of phenotypic variations in insect embryonic development, Journal of Biophotonics, 10.1002/jbio.201960047, 13:2, Online publication date: 1-Feb-2020. Lee C, Wang H, Jhang J and Cho I (2019) Automated drosophila heartbeat counting based on image segmentation technique on optical coherence tomography, Scientific Reports, 10.1038/s41598-019-41720-1, 9:1, Online publication date: 1-Dec-2019. Tan H, Su Y, Wei L, Yao X, Mai T, Li X, Luo Q, Li X, Tang Y, Gu Y and Zhu D (2019) Non-invasive 3D real time observation of physiological traits during the embryonic development of insects Optics in Health Care and Biomedical Optics IX, 10.1117/12.2537479, 9781510630970, (88) Duan L, Qin X, He Y, Sang X, Pan J, Xu T, Men J, Tanzi R, Li A, Ma Y and Zhou C (2018) Segmentation of Drosophila heart in optical coherence microscopy images using convolutional neural networks , Journal of Biophotonics, 10.1002/jbio.201800146, 11:12, Online publication date: 1-Dec-2018. Joos J, Saadatmand A, Schnabel C, Viktorinová I, Brand T, Kramer M, Nattel S, Dobrev D, Tomancak P, Backs J, Kleinbongard P, Heusch G, Lorenz K, Koch E, Weber S and El-Armouche A (2018) Ectopic expression of S28A-mutated Histone H3 modulates longevity, stress resistance and cardiac function in Drosophila, Scientific Reports, 10.1038/s41598-018-21372-3, 8:1 Kim A, Nekimken A, Fechner S, O'Brien L and Pruitt B (2018) Microfluidics for mechanobiology of model organisms Microfluidics in Cell Biology Part A: Microfluidics for Multicellular Systems, 10.1016/bs.mcb.2018.05.010, (217-259), . Klassen M, Peters C, Zhou S, Williams H, Jan L and Jan Y (2017) Age-dependent diastolic heart failure in an in vivo Drosophila model, eLife, 10.7554/eLife.20851, 6 Peterson L, Gu S, Karunamuni G, Jenkins M, Watanabe M and Rollins A (2017) Embryonic aortic arch hemodynamics are a functional biomarker for ethanol-induced congenital heart defects [Invited], Biomedical Optics Express, 10.1364/BOE.8.001823, 8:3, (1823), Online publication date: 1-Mar-2017. Deniz E, Jonas S, Hooper M, N. Griffin J, Choma M and Khokha M (2017) Analysis of Craniocardiac Malformations in Xenopus using Optical Coherence Tomography, Scientific Reports, 10.1038/srep42506, 7:1 Fercher A and Andersen P (2017) Optical Coherence Tomography Encyclopedia of Analytical Chemistry, 10.1002/9780470027318.a0114.pub3, (1-38) Men J, Huang Y, Solanki J, Zeng X, Alex A, Jerwick J, Zhang Z, Tanzi R, Li A and Zhou C Optical Coherence Tomography for Brain Imaging and Developmental Biology, IEEE Journal of Selected Topics in Quantum Electronics, 10.1109/JSTQE.2015.2513667, 22:4, (1-13) Xue P and Zheng J (2016) Chapter 20 Investigation of Spindle Structure and Embryo Development for Preimplantation Genetic Diagnosis by Subcellular Live Imaging with FF-OCT Handbook of Full-Field Optical Coherence Microscopy, 10.1201/9781315364889-21, (689-726), Online publication date: 8-Jun-2016. Rollins A, Fraser S, Choma M, Wang S, Singh M, Lopez A, Wu C, Raghunathan R, Schill A, Li J, Larin K and Larina I (2016) Live dynamic OCT imaging of cardiac structure and function in mouse embryos with 43 Hz direct volumetric data acquisition SPIE BiOS, 10.1117/12.2210751, , (971603), Online publication date: 9-Mar-2016. Andersen J, MacMillan H and Overgaard J (2015) Temperate Drosophila preserve cardiac function at low temperature, Journal of Insect Physiology, 10.1016/j.jinsphys.2015.03.016, 77, (26-32), Online publication date: 1-Jun-2015. Duncker D, Bakkers J, Brundel B, Robbins J, Tardiff J and Carrier L (2015) Animal and in silico models for the study of sarcomeric cardiomyopathies, Cardiovascular Research, 10.1093/cvr/cvv006, 105:4, (439-448), Online publication date: 1-Apr-2015. Jenkins M and Rollins A (2015) 4-D OCT in Developmental Cardiology Optical Coherence Tomography, 10.1007/978-3-319-06419-2_67, (2003-2023), . Garcia M, Lopez A, Larin K and Larina I (2015) Imaging of Cardiovascular Development in Mammalian Embryos Using Optical Coherence Tomography Vascular Morphogenesis, 10.1007/978-1-4939-1462-3_8, (151-161), . Brown K and Harvey M (2014) Optical coherence tomography: Age estimation of Calliphora vicina pupae in vivo ?, Forensic Science International, 10.1016/j.forsciint.2014.07.001, 242, (157-161), Online publication date: 1-Sep-2014. Li A, Ahsen O, Liu J, Du C, McKee M, Yang Y, Wasco W, Newton-Cheh C, O'Donnell C, Fujimoto J, Zhou C and Tanzi R (2013) Silencing of the Drosophila ortholog of SOX5 in heart leads to cardiac dysfunction as detected by optical coherence tomography, Human Molecular Genetics, 10.1093/hmg/ddt230, 22:18, (3798-3806), Online publication date: 15-Sep-2013. Xie H, Cammarato A, Rajasekaran N, Zhang H, Suggs J, Lin H, Bernstein S, Benjamin I, Golic K and Lu B (2013) The NADPH Metabolic Network Regulates Human αB-crystallin Cardiomyopathy and Reductive Stress in Drosophila melanogaster, PLoS Genetics, 10.1371/journal.pgen.1003544, 9:6, (e1003544) Dorn G (2013) Mitochondrial dynamics in heart disease, Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, 10.1016/j.bbamcr.2012.03.008, 1833:1, (233-241), Online publication date: 1-Jan-2013. Monnier V, Iché-Torres M, Rera M, Contremoulins V, Guichard C, Lalevée N, Tricoire H, Perrin L and Kim S (2012) dJun and Vri/dNFIL3 Are Major Regulators of Cardiac Aging in Drosophila, PLoS Genetics, 10.1371/journal.pgen.1003081, 8:11, (e1003081) Larina I, Garcia M, Vadakkan T, Larin K and Dickinson M (2012) Imaging Mouse Embryonic Cardiovascular Development, Cold Spring Harbor Protocols, 10.1101/pdb.top071498, 2012:10, (pdb.top071498), Online publication date: 1-Oct-2012. Lehmacher C, Abeln B and Paululat A (2012) The ultrastructure of Drosophila heart cells, Arthropod Structure & Development, 10.1016/j.asd.2012.02.002, 41:5, (459-474), Online publication date: 1-Sep-2012. Xiao J, Wang B, Lu G, Zhu Z and Huang Y (2012) Imaging of oocyte development using ultrahigh-resolution full-field optical coherence tomography, Applied Optics, 10.1364/AO.51.003650, 51:16, (3650), Online publication date: 1-Jun-2012. Jenkins M, Watanabe M and Rollins A Longitudinal Imaging of Heart Development With Optical Coherence Tomography, IEEE Journal of Selected Topics in Quantum Electronics, 10.1109/JSTQE.2011.2166060, 18:3, (1166-1175) Hoage T, Ding Y and Xu X (2012) Quantifying Cardiac Functions in Embryonic and Adult Zebrafish Cardiovascular Development, 10.1007/978-1-61779-523-7_2, (11-20), . Larina I, Larin K, Justice M and Dickinson M (2011) Optical Coherence Tomography for live imaging of mammalian development, Current Opinion in Genetics & Development, 10.1016/j.gde.2011.09.004, 21:5, (579-584), Online publication date: 1-Oct-2011. Pandey U, Nichols C and Barker E (2011) Human Disease Models in Drosophila melanogaster and the Role of the Fly in Therapeutic Drug Discovery , Pharmacological Reviews, 10.1124/pr.110.003293, 63:2, (411-436), Online publication date: 1-Jun-2011. Tsai M, Chang F, Lee C, Chi T, Yang K, Lin L, Wu J and Yang C (2011) Observations of cardiac beating behaviors of wild-type and mutant Drosophilae with optical coherence tomography, Journal of Biophotonics, 10.1002/jbio.201100009, (n/a-n/a), Online publication date: 3-May-2011. Choma M, Suter M, Vakoc B, Bouma B and Tearney G (2011) Physiological homology between Drosophila melanogaster and vertebrate cardiovascular systems , Disease Models & Mechanisms, 10.1242/dmm.005231, 4:3, (411-420), Online publication date: 1-May-2011. Gu S, Jenkins M, Watanabe M and Rollins A (2011) High-Speed Optical Coherence Tomography Imaging of the Beating Avian Embryonic Heart, Cold Spring Harbor Protocols, 10.1101/pdb.top98, 2011:2, (pdb.top98), Online publication date: 1-Feb-2011. Ma L, Bradu A, Podoleanu A, Bloor J and Egles C (2010) Arrhythmia Caused by a Drosophila Tropomyosin Mutation Is Revealed Using a Novel Optical Coherence Tomography Instrument, PLoS ONE, 10.1371/journal.pone.0014348, 5:12, (e14348) Choma M, Suter M, Vakoc B, Bouma B and Tearney G Heart wall velocimetry and exogenous contrast-based cardiac flow imaging in Drosophila melanogaster using Doppler optical coherence tomography, Journal of Biomedical Optics, 10.1117/1.3503418, 15:05, (1) Kühnlein R (2010) Drosophila as a lipotoxicity model organism — more than a promise?, Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, 10.1016/j.bbalip.2009.09.006, 1801:3, (215-221), Online publication date: 1-Mar-2010. Fercher A, Sander B, Jørgensen T and Andersen P (2009) Optical Coherence Tomography Encyclopedia of Analytical Chemistry, 10.1002/9780470027318.a0114.pub2 Bradu A, Ma L, Bloor J and Podoleanu A (2009) Dual optical coherence tomography/fluorescence microscopy for monitoring of Drosophila melanogaster larval heart , Journal of Biophotonics, 10.1002/jbio.200910021, 2:6-7, (380-388), Online publication date: 1-Jul-2009. Gargesha M, Jenkins M, Wilson D and Rollins A (2009) High temporal resolution OCT using image-based retrospective gating, Optics Express, 10.1364/OE.17.010786, 17:13, (10786), Online publication date: 22-Jun-2009. Larina I, Ivers S, Syed S, Dickinson M and Larin K (2009) Hemodynamic measurements from individual blood cells in early mammalian embryos with Doppler swept source OCT, Optics Letters, 10.1364/OL.34.000986, 34:7, (986), Online publication date: 1-Apr-2009. Thrane L (2009) Field programmable gate-array-based real-time optical Doppler tomography system for in vivo imaging of cardiac dynamics in the chick embryo, Optical Engineering, 10.1117/1.3081062, 48:2, (023201), Online publication date: 1-Feb-2009. Thomsen J, Sander B, Mogensen M, Thrane L, Jørgensen T, Jemec G and Andersen P Optical Coherence Tomography: Technique and Applications Advanced Imaging in Biology and Medicine, 10.1007/978-3-540-68993-5_5, (103-129) Männer J, Thrane L, Norozi K and Yelbuz T (2008) High‐resolution in vivo imaging of the cross‐sectional deformations of contracting embryonic heart loops using optical coherence tomography, Developmental Dynamics, 10.1002/dvdy.21483, 237:4, (953-961), Online publication date: 1-Apr-2008. Feala J, Omens J, Paternostro G and McCulloch A (2008) Discovering Regulators of the Drosophila Cardiac Hypoxia Response Using Automated Phenotyping Technology , Annals of the New York Academy of Sciences, 10.1196/annals.1420.019, 1123:1, (169-177), Online publication date: 1-Mar-2008. Larina I, Sudheendran N, Ghosn M, Jiang J, Cable A, Larin K and Dickinson M (2008) Live imaging of blood flow in mammalian embryos using Doppler swept-source optical coherence tomography, Journal of Biomedical Optics, 10.1117/1.3046716, 13:6, (060506), . Feala J, Coquin L, Paternostro G and McCulloch A (2008) Integrating metabolomics and phenomics with systems models of cardiac hypoxia, Progress in Biophysics and Molecular Biology, 10.1016/j.pbiomolbio.2007.07.014, 96:1-3, (209-225), Online publication date: 1-Jan-2008. Mariampillai A, Standish B, Munce N, Randall C, Liu G, Jiang J, Cable A, Vitkin I and Yang V (2007) Doppler optical cardiogram gated 2D color flow imaging at 1000 fps and 4D in vivo visualization of embryonic heart at 45 fps on a swept source OCT system, Optics Express, 10.1364/OE.15.001627, 15:4, (1627), Online publication date: 19-Feb-2007. Spöler F, Först M, Kurz H, Frentz M and Schrage N (2007) Dynamic analysis of chemical eye burns using high-resolution optical coherence tomography, Journal of Biomedical Optics, 10.1117/1.2768018, 12:4, (041203), . July 11, 2006Vol 114, Issue 2 Advertisement Article InformationMetrics https://doi.org/10.1161/CIRCULATIONAHA.105.593541PMID: 16831991 Originally publishedJuly 11, 2006 PDF download Advertisement SubjectsAnimal Models of Human DiseaseArrhythmiasContractile FunctionImaging
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