Quantitative three-dimensional imaging of live avian embryonic morphogenesis via micro-computed tomography

Developmental Dynamics

Volumn 240, Issue 8, 2011, Pages 1949-1957

  Henning, Alyssa L ^a   Jiang, Michael X ^a   Yalcin, Huseyin C ^b   Butcher, Jonathan T ^a  

^a Cornell University   (United States)

^b DOGUS UNIVERSITY   (Turkey)

Author keywords

Allantois; Biodistribution; Brain; Clearance; Contrast agent; Defect; Development; Dosage; Heart; Iodine; Radiation; Teratogen; Toxicity

Indexed keywords

IODIXANOL; OSMIUM TETRAOXIDE;

ANIMAL EXPERIMENT; ARTICLE; CHICK EMBRYO; CONTROLLED STUDY; EMBRYO; FETUS MEMBRANE; FOWL; MICRO-COMPUTED TOMOGRAPHY; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RADIATION DOSE; TERATOGENESIS; THREE DIMENSIONAL IMAGING; X RAY;

ANIMALS; CHICK EMBRYO; CONTRAST MEDIA; HUMANS; IMAGING, THREE-DIMENSIONAL; MORPHOGENESIS; TIME FACTORS; TOMOGRAPHY, X-RAY COMPUTED;

AVES;

EID: 79960363228     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.22694     Document Type: Article

References (52)

1. Ahrens ET, Srinivas M, Capuano S, Simhan HN, Schatten GP. 2006. Magnetic resonance imaging of embryonic and fetal development in model systems. Methods Mol Med 124: 87-101.
2. Almajdub M, Magnier L, Juillard L, Janier M. 2008. Kidney volume quantification using contrast-enhanced in vivo X-ray micro-CT in mice. Contrast Media Mol Imag 3: 120-126.
3. Aristizabal O, Ketterling JA, Turnbull DH. 2006. 40-MHz annular array imaging of mouse embryos. Ultrasound Med Biol 32: 1631-1637.
4. Badea C, Hedlund LW, Johnson GA. 2004. Micro-CT with respiratory and cardiac gating. Med Phys 31: 3324-3329.
5. 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: R319-350.
6. 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. Journal of magnetic resonance imaging. JMRI 26: 198-201.
7. Bellairs R, Osmond M. 2005. Atlas of chick development. New York: Elsevier Academic Press. 476p.
8. Bentley MD, Jorgensen SM, Lerman LO, Ritman EL, Romero JC. 2007. Visualization of three-dimensional nephron structure with microcomputed tomography. Anat Rec (Hoboken) 290: 277-283.
9. Butcher JT, Sedmera D, Guldberg RE, Markwald RR. 2007. Quantitative volumetric analysis of cardiac morphogenesis assessed through micro-computed tomography. Dev Dyn 236: 802-809.
10. Clark NB, Feng JQ, Murphy MJ. 1993. Renal clearance measurements of electrolytes in embryonic chickens. J Exp Zool 265: 107-111.
11. De la Cruz MV, Campillo-Sainz C, Munoz-Armas S. 1966. Congenital heart defects in chick embryos subjected to temperature variations. Circul Res 18: 257-262.
12. Duce S, Morrison F, Welten M, Baggott G, Tickle C. 2011. Micro-magnetic resonance imaging study of live quail embryos during embryonic development. Magn Reson Imag 29: 132-139.
13. Gargesha M, Jenkins MW, Wilson DL, Rollins AM. 2009. High temporal resolution OCT using image-based retrospective gating. Opt Express 17: 10786-10799.
14. Gilbert S, editor. 2006. Developmental biology. Sunderland, MA: Sinauer Associates, Inc. 785 p.
15. Graves JS, Dunn BE, Brown SC. 1986. Embryonic chick allantois: functional isolation and development of sodium transport. Am J Physiol 251: C787-794.
16. Groenendijk BC, Stekelenburg-de Vos S, Vennemann P, Wladimiroff JW, Nieuwstadt FT, Lindken R, Westerweel J, Hierck BP, Ursem NT, Poelmann RE. 2008. The endothelin-1 pathway and the development of cardiovascular defects in the haemodynamically challenged chicken embryo. J Vasc Res 45: 54-68.
17. Hainfeld JF, Slatkin DN, Focella TM, Smilowitz HM. 2006. Gold nanoparticles: a new X-ray contrast agent. Br J Radiol 79: 248-253.
18. Heidrich A, Wurbach L, Opfermann T, Saluz HP. 2011. Motion-artifact-free in vivo imaging utilizing narcotized avian embryos in ovo. Mol Imag Biol 13: 208-214.
19. Hogers B, van der Weerd L, Olofsen H, van der Graaf LM, DeRuiter MC, Groot ACGD, 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. 2008. Images in cardiovascular medicine. Noninvasive self-gated magnetic resonance cardiac imaging of developing chick embryos in ovo. Circulation 117: e346-347.
21. Hornberger LK, Need L, Benacerraf BR. 1996. Development of significant left and right ventricular hypoplasia in the second and third trimester fetus. J Ultrasound Med 15: 655-659.
22. Jenkins MW, Chughtai OQ, Basavanhally AN, Watanabe M, Rollins AM. 2007. In vivo gated 4D imaging of the embryonic heart using optical coherence tomography. J Biomed Opt 12: 030505.
23. 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: 471-477.
24. Jones EA, Baron MH, Fraser SE, Dickinson ME. 2005. Dynamic in vivo imaging of mammalian hematovascular development using whole embryo culture. Methods Mol Med 105: 381-394.
25. Kim JS, Min J, Recknagel AK, Riccio M, Butcher JT. 2011. Quantitative three-dimensional analysis of embryonic chick morphogenesis via microcomputed tomography. Anat Rec (Hoboken) 294: 1-10.
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. Lloyd-Jones D, Adams RJ, Brown TM, Carnethon M, Dai S, De Simone G, Ferguson TB, Ford E, Furie K, Gillespie C, Go A, Greenlund K, Haase N, Hailpern S, Ho PM, Howard V, Kissela B, Kittner S, Lackland D, Lisabeth L, Marelli A, McDermott MM, Meigs J, Mozaffarian D, Mussolino M, Nichol G, Roger VL, Rosamond W, Sacco R, Sorlie P, Thom T, Wasserthiel-Smoller S, Wong ND, Wylie-Rosett J. 2010. Heart disease and stroke statistics: 2010 update: a report from the American Heart Association. Circulation 121: e46-e215.
28. McQuinn TC, Bratoeva M, Dealmeida A, Remond M, Thompson RP, Sedmera D. 2007. High-frequency ultrasonographic imaging of avian cardiovascular development. Dev Dyn 236: 3503-3513.
29. Metscher BD. 2009a. MicroCT for comparative morphology: simple staining methods allow high-contrast 3D imaging of diverse non-mineralized animal tissues. BMC Physiol 9: 11.
30. Metscher BD. 2009b. MicroCT for developmental biology: a versatile tool for high-contrast 3D imaging at histological resolutions. Dev Dyn 238: 632-640.
31. Moran CM, Pye SD, Ellis W, Janeczko A, Morris KD, McNeilly AS, Fraser HM. 2011. A comparison of the imaging performance of high resolution ultrasound scanners for preclinical imaging. Ultrasound Med Biol 37: 493-501.
32. Mukundan S, Jr., Ghaghada KB, Badea CT, Kao CY, Hedlund LW, Provenzale JM, Johnson GA, Chen E, Bellamkonda RV, Annapragada A. 2006. A liposomal nanoscale contrast agent for preclinical CT in mice. AJR Am J Roentgenol 186: 300-307.
33. Murphy MJ, Brown PS, Brown SC. 1983. Hydromineral balance during avian embryonic-development: effects of prolactin and growth-hormone. Am Zool 23: 898-898.
34. Nakamura H, Funahashi J. 2001. Introduction of DNA into chick embryos by in ovo electroporation. Methods 24: 43-48.
35. Narbaitz R, Kapal VK. 1986. Scanning electron microscopical observations on the differentiating mesonephros of the chick embryo. Acta Anat (Basel) 125: 183-190.
36. Navarro M, DeRuiter MC, Carretero A, Ruberte J. 2003. Microvascular assembly and cell invasion in chick mesonephros grafted onto chorioallantoic membrane. J Anat 202: 213-225.
37. Nieman BJ, Turnbull DH. 2010. Ultrasound and magnetic resonance microimaging of mouse development. Methods Enzymol 476: 379-400.
38. Pallares P, Fernandez-Valle ME, Gonzalez-Bulnes A. 2009. In vivo virtual histology of mouse embryogenesis by ultrasound biomicroscopy and magnetic resonance imaging. Reprod Fertil Dev 21: 283-292.
39. Paulus MJ, Gleason SS, Kennel SJ, Hunsicker PR, Johnson DK. 2000. High resolution X-ray computed tomography: an emerging tool for small animal cancer research. Neoplasia 2: 62-70.
40. Prajapati SI, Keller C. 2011. Contrast enhanced vessel imaging using microCT. J Vis Exp [DOI: 10.3791/2377].
41. 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.
42. Romanoff A. 1952. Membrane growth and function. Ann NY Acad Sci 55: 288-301.
43. Romanoff A. 1967. Biochemistry of the avian embryo: a quantitative analysis of prenatal development. New York: John Wiley and Sons.
44. Rychter Z, Kopecky M, Lemez L. 1955. Micromethod for determination of the circulating blood volume in chick embryos. Nature 175: 1126-1127.
45. Starck J, Ricklefs R. 1998. Avian growth and development: evolution within the altricial-precocial spectrum. New York: Oxford University Press. 456p.
46. van Soest G, Goderie T, Regar E, Koljenovic S, van Leenders GL, Gonzalo N, van Noorden S, Okamura T, Bouma BE, Tearney GJ, Oosterhuis JW, Serruys PW, van der Steen AF. 2010. Atherosclerotic tissue characterization in vivo by optical coherence tomography attenuation imaging. J Biomed Optics 15: 011105.
47. Winkelmann CT, Wise LD. 2009. High-throughput micro-computed tomography imaging as a method to evaluate rat and rabbit fetal skeletal abnormalities for developmental toxicity studies. J Pharmacol Toxicol Methods 59: 156-165.
48. Yalcin HC, Shekhar A, Nishimura N, Rane AA, Schaffer CB, Butcher JT. 2010a. Two-photon microscopy-guided femtosecond-laser photoablation of avian cardiogenesis: noninvasive creation of localized heart defects. Am J Physiol Heart Circ Physiol 299: H1728-1735.
49. Yalcin HC, Shekhar A, Rane AA, Butcher JT. 2010b. An ex-ovo chicken embryo culture system suitable for imaging and microsurgery applications. J Vis Exp [DOI: 10.3791/2154].
50. Yalcin HC, Shekhar A, McQuinn TC, Butcher JT. 2011. Hemodynamic patterning of the avian atrioventricular valve. Dev Dyn 240: 23-35.
51. Zamir EA, Czirok A, Cui C, Little CD, Rongish BJ. 2006. Mesodermal cell displacements during avian gastrulation are due to both individual cell-autonomous and convective tissue movements. Proc Natl Acad Sci USA 103: 19806-19811.
52. Zhang W, Chen Y, Swift MR, Tassi E, Stylianou DC, Gibby KA, Riegel AT, Wellstein A. 2008. Effect of FGF-binding protein 3 on vascular permeability. J Biol Chem 283: 28329-28337.