Quantitative Three-Dimensional Analysis of Embryonic Chick Morphogenesis Via Microcomputed Tomography

Anatomical Record

Volumn 294, Issue 1, 2011, Pages 1-10

  Kim, Jun Sup ^a   Min, Jouha ^a   Recknagel, Andrew K ^a   Riccio, Mark ^a   Butcher, Jonathan T ^a  

^a Cornell University   (United States)

Author keywords

Chick; Embryo; Histology quantification; MicroCT based virtual histology; Morphology; Quantitative imaging

Indexed keywords

OSMIUM TETRAOXIDE;

ARTICLE; CHICK EMBRYO; EMBRYO; EMBRYO DEVELOPMENT; HEART MUSCLE CELL; HISTOLOGY; MICRO-COMPUTED TOMOGRAPHY; MORPHOGENESIS; NONHUMAN; ORGAN GROWTH; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; THREE DIMENSIONAL IMAGING; VOLUMETRY;

ANIMALS; BRAIN; CHICK EMBRYO; EMBRYOLOGY; EXTREMITIES; EYE; HEART; IMAGING, THREE-DIMENSIONAL; MODELS, ANIMAL; ORGANOGENESIS; TIME FACTORS; X-RAY MICROTOMOGRAPHY;

EID: 78650118279     PISSN: 19328486     EISSN: 19328494     Source Type: Journal    
DOI: 10.1002/ar.21276     Document Type: Article

References (46)

1. Alter J, Sennoga CA, Lopes DM, Eckersley RJ, Wells DJ. 2009. Microbubble stability is a major determinant of the efficiency of ultrasound and microbubble mediated in vivo gene transfer. Ultrasound Med Biol 35: 976-984.
2. Badea CT, Drangova M, Holdsworth DW, Johnson GA. 2008. In vivo small-animal imaging using micro-CT and digital subtraction angiography. Phys Med Biol 53: R319-R350.
3. Bain MM, Fagan AJ, Mullin JM, McNaught I, McLean J, Condon B. 2007. Noninvasive monitoring of chick development in ovo using a 7T MRI system from day 12 of incubation through to hatching. J Magn Reson Imaging 26: 198-201.
4. Bellairs R, Osmond M. 2005. The atlas of chick development. 2nd ed. New York, USA: Academic Press.
5. Borue X, Noden DM. 2004. Normal and aberrant craniofacial myogenesis by grafted trunk somitic and segmental plate mesoderm. Development 131: 3967-3980.
6. Broekhuizen ML, Hogers B, DeRuiter MC, Poelmann RE, Gittenberger-de Groot AC, Wladimiroff JW. 1999. Altered hemodynamics in chick embryos after extraembryonic venous obstruction. Ultrasound Obstet Gynecol 13: 437-445.
7. Butcher JT, McQuinn TC, Sedmera D, Turner D, Markwald RR. 2007a. Transitions in early embryonic atrioventricular valvular function correspond with changes in cushion biomechanics that are predictable by tissue composition. Circ Res 100: 1503-1511.
8. Butcher JT, Sedmera D, Guldberg RE, Markwald RR. 2007b. Quantitative volumetric analysis of cardiac morphogenesis assessed through micro-computed tomography. Dev Dyn 236: 802-809.
9. Camenisch TD, Schroeder JA, Bradley J, Klewer SE, McDonald JA. 2002. Heart-valve mesenchyme formation is dependent on hyaluronan-augmented activation of ErbB2-ErbB3 receptors. Nat Med 8: 850-855.
10. Carney EW, Tornesi B, Keller C, Findlay HA, Nowland WS, Marshall VA, Ozolins TR. 2007. Refinement of a morphological scoring system for postimplantation rabbit conceptuses. Birth Defects Res B Dev Reprod Toxicol 80: 213-222.
11. Clark KL, Yutzey KE, Benson DW. 2006. Transcription factors and congenital heart defects. Annu Rev Physiol 68: 97-121.
12. Davis AM, Rothenberg FG, Shepherd N, Izatt JA. 2008. In vivo spectral domain optical coherence tomography volumetric imaging and spectral Doppler velocimetry of early stage embryonic chicken heart development. J Opt Soc Am A Opt Image Sci Vis 25: 3134-3143.
13. Degenhardt K, Wright AC, Horng D, Padmanabhan A, Epstein JA. 2010. Rapid 3D phenotyping of cardiovascular development in mouse embryos by micro-CT with iodine staining. Circ Cardiovasc Imaging 3: 314-322.
14. Dhenain M, Ruffins SW, Jacobs RE. 2001. Three-dimensional digital mouse atlas using high-resolution MRI. Dev Biol 232: 458-470.
15. Goedbloed JF. 1972. The embryonic and postnatal growth of rat and mouse. I. The embryonic and early postnatal growth of the whole embryo. A model with exponential growth and sudden changes in growth rate. Acta Anat (Basel) 82: 305-306.
16. Goedbloed JF. 1980. Embryonic and postnatal growth of the rat and mouse. VI. Prenatal growth of organs and tissues: individual organs; final remarks on parts I-VI, phase transitions. Acta Anat (Basel) 106: 108-128.
17. Goodall N, Kisiswa L, Prashar A, Faulkner S, Tokarczuk P, Singh K, Erichsen JT, Guggenheim J, Halfter W, Wride MA. 2009. 3-Dimensional modelling of chick embryo eye development and growth using high resolution magnetic resonance imaging. Exp Eye Res 89: 511-521.
18. Hogers B, DeRuiter MC, Gittenberger-de Groot AC, Poelmann RE. 1999. Extraembryonic venous obstructions lead to cardiovascular malformations and can be embryolethal. Cardiovasc Res 41: 87-99.
19. Hogers B, van der Weerd L, Olofsen H, van der Graaf LM, DeRuiter MC, Gittenberger-de Groot AC, Poelmann RE. 2009. Non-invasive tracking of avian development in vivo by MRI. NMR Biomed 22: 365-373.
20. Holmes WM, McCabe C, Mullin JM, Condon B, Bain MM. 2009. In ovo non-invasive quantification of the myocardial function and mass of chick embryos using magnetic resonance imaging. NMR Biomed 22: 745-752.
21. Hu N, Christensen DA, Agrawal AK, Beaumont C, Clark EB, Hawkins JA. 2009. Dependence of aortic arch morphogenesis on intracardiac blood flow in the left atrial ligated chick embryo. Anat Rec (Hoboken) 292: 652-660.
22. Hu N, Clark EB. 1989. Hemodynamics of the stage 12 to stage 29 chick embryo. Circ Res 65: 1665-1670.
23. Hurle JM, Ganan Y. 1987. Formation of extra-digits induced by surgical removal of the apical ectodermal ridge of the chick embryo leg bud in the stages previous to the onset of interdigital cell death. Anat Embryol (Berl) 176: 393-399.
24. Johnson JT, Hansen MS, Wu I, Healy LJ, Johnson CR, Jones GM, Capecchi MR, Keller C. 2006. Virtual histology of transgenic mouse embryos for high-throughput phenotyping. PLoS Genet 2: e61.
25. Li X, Liu J, Davey M, Duce S, Jaberi N, Liu G, Davidson G, Tenent S, Mahood R, Brown P, Cunningham C, Bain A, Beattie K, McDonald L, Schmidt K, Towers M, Tickle C, Chudek S. 2007. Micro-magnetic resonance imaging of avian embryos. J Anat 211: 798-809.
26. Liebling M, Forouhar AS, Gharib M, Fraser SE, Dickinson ME. 2005. Four-dimensional cardiac imaging in living embryos via postacquisition synchronization of nongated slice sequences. J Biomed Opt 10: 054001.
27. Maciaczyk J, Singec I, Maciaczyk D, Klein A, Nikkhah G. 2009. Restricted spontaneous in vitro differentiation and region-specific migration of long-term expanded fetal human neural precursor cells after transplantation into the adult rat brain. Stem Cells Dev 18: 1043-1058.
28. Martinez HG, Prajapati SI, Estrada CA, Jimenez F, Quinones MP, Wu I, Bahadur A, Sanderson A, Johnson CR, Shim M, Keller C, Ahuja SS. 2009. Images in cardiovascular medicine: microscopic computed tomography-based virtual histology for visualization and morphometry of atherosclerosis in diabetic apolipoprotein e mutant mice. Circulation 120: 821-822.
29. McBride KL, Pignatelli R, Lewin M, Ho T, Fernbach S, Menesses A, Lam W, Leal SM, Kaplan N, Schliekelman P, Towbin JA, Belmont JW. 2005. Inheritance analysis of congenital left ventricular outflow tract obstruction malformations: segregation, multiplex relative risk, and heritability. Am J Med Genet A 134: 180-186.
30. Metscher BD. 2009. MicroCT for comparative morphology: simple staining methods allow high-contrast 3D imaging of diverse non-mineralized animal tissues. BMC Physiol 9: 11.
31. Mjaatvedt CH, Nakaoka T, Moreno-Rodriguez R, Norris RA, Kern MJ, Eisenberg CA, Turner D, Markwald RR. 2001. The outflow tract of the heart is recruited from a novel heart-forming field. Dev Biol 238: 97-109.
32. Munoz-Sanjuan I, Simandl BK, Fallon JF, Nathans J. 1999. Expression of chicken fibroblast growth factor homologous factor (FHF)-1 and of differentially spliced isoforms of FHF-2 during development and involvement of FHF-2 in chicken limb development. Development 126: 409-421.
33. Niswander L. 2002. Interplay between the molecular signals that control vertebrate limb development. Int J Dev Biol 46: 877-881.
34. Olson EN. 2004. A decade of discoveries in cardiac biology. Nat Med 10: 467-474.
35. Phoon CK. 2001. Circulatory physiology in the developing embryo. Curr Opin Pediatr 13: 456-464.
36. Rabin O, Manuel Perez J, Grimm J, Wojtkiewicz G, Weissleder R. 2006. An X-ray computed tomography imaging agent based on long-circulating bismuth sulphide nanoparticles. Nat Mater 5: 118-122.
37. Ruffins SW, Martin M, Keough L, Truong S, Fraser SE, Jacobs RE, Lansford R. 2007. Digital three-dimensional atlas of quail development using high-resolution MRI. Sci World J 7: 592-604.
38. Smith BR, Linney E, Huff DS, Johnson GA. 1996. Magnetic resonance microscopy of embryos. Comput Med Imaging Graph 20: 483-490.
39. Snider P, Hinton RB, Moreno-Rodriguez RA, Wang J, Rogers R, Lindsley A, Li F, Ingram DA, Menick D, Field L, Firulli AB, Molkentin JD, Markwald R, Conway SJ. 2008. Periostin is required for maturation and extracellular matrix stabilization of noncardiomyocyte lineages of the heart. Circ Res 102: 752-760.
40. Wagner GP. 2005. The developmental evolution of avian digit homology: an update. Theor Biosci 124: 165-183.
41. Wang Y, Dur O, Patrick MJ, Tinney JP, Tobita K, Keller BB, Pekkan K. 2009. Aortic arch morphogenesis and flow modeling in the chick embryo. Ann Biomed Eng 37: 1069-1081.
42. Wenink AC. 1992. Quantitative morphology of the embryonic heart: an approach to development of the atrioventricular valves. Anat Rec 234: 129-135.
43. Wessels A, Perez-Pomares JM. 2004. The epicardium and epicardially derived cells (EPDCs) as cardiac stem cells. Anat Rec A Discov Mol Cell Evol Biol 276: 43-57.
44. Williams BS, Doyle MD. 1996. An Internet atlas of mouse development. Comput Med Imaging Graph 20: 433-447.
45. Yelbuz TM, Waldo KL, Zhang X, Zdanowicz M, Parker J, Creazzo TL, Johnson GA, Kirby ML. 2003. Myocardial volume and organization are changed by failure of addition of secondary heart field myocardium to the cardiac outflow tract. Dev Dyn 228: 152-160.
46. Zhang X, Yelbuz TM, Cofer GP, Choma MA, Kirby ML, Johnson GA. 2003. Improved preparation of chick embryonic samples for magnetic resonance microscopy. Magn Reson Med 49: 1192-1195.