Cardiac phenotyping in ex vivo murine embryos using μMRI

NMR in Biomedicine

Volumn 22, Issue 8, 2009, Pages 857-866

  Cleary, Jon O ^a,b   Price, Anthony N ^a   Thomas, David L ^b   Scambler, Peter J ^a   Kyriakopoulou, Vanessa ^a   McCue, Karen ^a   Schneider, Jürgen E ^c   Ordidge, Roger J ^b   Lythgoe, Mark F ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

CHARGE; Chd7; Contrast optimisation; Embryo; Magnetic resonance imaging; Mouse; MR microscopy; Phenotyping

Indexed keywords

DEFECTS; GADOLINIUM; HEART; MAGNETIC RESONANCE IMAGING; MAMMALS; SIGNAL TO NOISE RATIO; TISSUE;

CHARGE; CHD7; EMBRYO; MOUSE; MR MICROSCOPY; OPTIMISATIONS; PHENOTYPING;

BIOMEDICAL SIGNAL PROCESSING;

AGAROSE; CHROMODOMAIN HELICASE DNA BINDING PROTEIN 7; DNA BINDING PROTEIN; GADOLINIUM CHELATE; GADOLINIUM PENTETATE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; COMPUTER SIMULATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; EMBRYO; EX VIVO STUDY; HEART DEVELOPMENT; HEART VENTRICLE SEPTUM DEFECT; HETEROZYGOTE; IMAGE ANALYSIS; IMAGE DISPLAY; IMAGE PROCESSING; IMAGE QUALITY; MICROSCOPIC NUCLEAR MAGNETIC RESONANCE IMAGING; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PHENOTYPE; PRIORITY JOURNAL; PROCESS OPTIMIZATION; SIGNAL NOISE RATIO; SYNDROME CHARGE; THREE DIMENSIONAL ECHOCARDIOGRAPHY; TISSUE FIXATION;

MURINAE; MUS MUSCULUS;

ANIMALS; CONTRAST MEDIA; DNA-BINDING PROTEINS; EMBRYO, MAMMALIAN; FEMALE; GADOLINIUM DTPA; HEART; HEART DEFECTS, CONGENITAL; HUMANS; IMAGE ENHANCEMENT; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MICE; MICE, TRANSGENIC; PHENOTYPE; PREGNANCY;

EID: 70649099219     PISSN: 09523480     EISSN: 10991492     Source Type: Journal    
DOI: 10.1002/nbm.1400     Document Type: Article

References (37)

1. Mouse Genome Sequencing Consortium. Initial sequencing and comparative analysis of the mouse genome. Nature 2002; 420: 520-562.
2. Capecchi MR. Generating mice with targeted mutations. Nat. Med. 2001; 7: 1086-1090.
3. Balling R. ENU mutagenesis: analyzing gene function in mice. Annu. Rev. Genomics Hum. Genet. 2001; 2: 463-492.
4. The International Mouse Knockout Consortium. A mouse for all reasons. Cell 2007; 128: 9-13.
5. Hoffman JI, Kaplan S. The incidence of congenital heart disease. J. Am. Coll. Cardiol. 2002; 39: 1890-1900.
6. Bentham J, Bhattacharya S. Genetic mechanisms controlling cardiovascular development. Ann. N. Y. Acad. Sci. 2008; 1123: 10-19.
7. Kaufman MH. The Atlas of Mouse Development. Academic Press: London, 1992.
8. Weninger WJ, Geyer SH, Mohun TJ, Rasskin-Gutman D, Matsui T, Ribeiro I, Costa Lda F, Izúpisa-Belmonte JC, Müller GB. High-resolution episcopic microscopy: a rapid technique for high detailed 3D analysis of gene activity in the context of tissue architecture and morphology. Anat. Embryol. 2006; 211: 213-221.
9. Weninger WJ, Mohun TJ. Phenotyping transgenic embryos: a rapid 3-D screening method based on episcopic fluorescence image capturing. Nat. Genet. 2002; 30: 59-65.
10. Nolan PM, Peters J, Strivens M, Rogers D, Hagan J, Spurr N, Gray IC, Vizor L, Brooker D, Whitehill E, Washbourne R, Hough T, Greenaway S, Hewitt M, Liu X, McCormack S, Pickford K, Selley R, Wells C, Tymowska-Lalanne Z, Roby P, Glenister P, Thornton C, Thaung C, Stevenson JA, Arkell R, Mburu P, Hardisty R, Kiernan A, Erven A, Steel KP, Voegeling S, Guenet JL, Nickols C, Sadri R, Nasse M, Isaacs A, Davies K, Browne M, Fisher EM, Martin J, Rastan S, Brown SD, Hunter J. A systematic, genome-wide, phenotype-driven mutagenesis programme for gene function studies in the mouse. Nat. Genet. 2000; 25: 440-443.
11. Schneider JE, Bhattacharya S. Making the mouse embryo transparent: identifying developmental malformations using magnetic resonance imaging. Birth Defects Res. C Embryo Today 2004; 72: 241-249. (Pubitemid 39564151)
12. Kim S, Pickup S, Hsu O, Poptani H. Enhanced delineation of white matter structures of the fixed mouse brain using Gd-DTPA in microscopic MRI. NMR Biomed. 2009; 22: 303-309.
13. Petiet AE, Kaufman MH, Goddeeris MM, Brandenburg J, Elmore SA, Johnson GA. High-resolution magnetic resonance histology of the embryonic and neonatal mouse: a 4D atlas and morphologic database. Proc. Natl Acad. Sci. U.S.A. 2008; 105: 12331-12336.
14. Goddeeris MM, Rho S, Petiet A, Davenport CL, Johnson GA, Meyers EN, Klingensmith J. Intracardiac septation requires hedgehog-dependent cellular contributions from outside the heart. Development 2008; 135: 1887-1895.
15. Schneider JE, Bamforth SD, Grieve SM, Clarke K, Bhattacharya S, Neubauer S. High-resolution, high-throughput magnetic paragraph sign resonance imaging of mouse embryonic paragraph sign anatomy using a fast gradient-echo sequence. Magma 2003; 16: 43-51. (Pubitemid 38325347)
16. Schneider JE, Bose J, Bamforth SD, Gruber AD, Broadbent C, Clarke K, Neubauer S, Lengeling A, Bhattacharya S. Identification of cardiac malformations in mice lacking Ptdsr using a novel high-throughput magnetic resonance imaging technique. BMC Dev. Biol. 2004; 4: 16.
17. Holdsworth DW, Thornton MM. Micro-CT in small animal and specimen imaging. Trends Biotechnol. 2002; 20: S34-S39. (Pubitemid 34804433)
18. Johnson JT, Hansen MS, Wu I, Healy LJ, Johnson CR, Jones GM, Capecchi MR, Keller C. Virtual histology of transgenic mouse embryos for high-throughput phenotyping. PLoS Genet. 2006; 2: e61.
19. Sharpe J, Ahlgren U, Perry P, Hill B, Ross A, Hecksher-Sorensen J, Baldock R, Davidson D. Optical projection tomography as a tool for 3D microscopy and gene expression studies. Science 2002; 296: 541-545. (Pubitemid 34408675)
20. Takeda T, Momose A, Hirano K, Haraoka S, Watanabe T, Itai Y. Human carcinoma: early experience with phase-contrast x-ray ct with synchrotron radiation-comparative specimen study with optical microscopy1. Radiology 2000; 214: 298-301. (Pubitemid 30019908)
21. Schneider JE, Bamforth SD, Farthing CR, Clarke K, Neubauer S, Bhattacharya S. Rapid identification and 3D reconstruction of complex cardiac malformations in transgenic mouse embryos using fast gradient echo sequence magnetic resonance imaging. J. Mol. Cell. Cardiol. 2003; 35: 217-222.
22. Petiet AE, Hedlund L, Johnson GA. Staining methods for magnetic resonance microscopy of the rat fetus. J. Magn. Reson. Imaging 2007; 25: 1192-1198.
23. Bosman EA, Penn AC, Ambrose JC, Kettleborough R, Stemple DL, Steel KP. Multiple mutations in mouse Chd7 provide models for CHARGE syndrome. Hum. Mol. Genet. 2005; 14: 3463-3476.
24. Blake KD, Prasad C. CHARGE syndrome. Orphanet J. Rare Dis. 2006; 1: 34.
25. Callaghan PT, Forde LC, Rofe CJ. Correlated susceptibility and diffusion effects in NMR microscopy using both phase-frequency encoding and phase-phase encoding. J. Magn. Reson. B 1994; 104: 34-52.
26. Stanisz GJ, Henkelman RM. Gd-DTPA relaxivity depends on macromolecular content. Magn. Reson. Med. 2000; 44: 665-667.
27. Pelc NJ. Optimization of flip angle for T1 dependent contrast in MRI. Magn. Reson. Med. 1993; 29: 695-699.
28. Tweedle MF. The ProHance story: the making of a novel MRI contrast agent. Eur. Radiol. 1997; 7: S225-S230.
29. Bellin MF. MR contrast agents, the old and the new. Eur. J. Radiol. 2006; 60: 314-323.
30. Hardman MJ, Sisi P, Banbury DN, Byrne C. Patterned acquisition of skin barrier function during development. Development 1998; 125: 1541-1552. (Pubitemid 28239364)
31. Johnson GA, Cofer GP, Gewalt SL, Hedlund LW. Morphologic phenotyping with MR microscopy: the visible mouse. Radiology 2002; 222: 789-793.
32. Kingsley PB. Product operators, coherence pathways, and phase cycling. Part III: phase cycling. Concepts Magn. Reson. 1995; 7: 167-192.
33. Choi S, Tang XW, Cory DG. Constant time imaging approaches to NMR microscopy. Int. J. Imaging Syst. Technol. 1997; 8: 263-276.
34. Bottomley PA, Foster TH, Argersinger RE, Pfeifer LM. A review of normal tissue hydrogen NMR relaxation times and relaxation mechanisms from 1-100 MHz: dependence on tissue type, NMR frequency, temperature, species, excision, and age. Med. Phys. 1984; 11: 425-448.
35. de Graaf RA, Brown PB, McIntyre S, Nixon TW, Behar KL, Rothman DL. High magnetic field water and metabolite proton T1 and T2 relaxation in rat brain in vivo. Magn. Reson. Med. 2006; 56: 386-394.
36. Donahue KM, Burstein D, Manning WJ, Gray ML. Studies of Gd-DTPA relaxivity and proton exchange rates in tissue. Magn. Reson. Med. 1994; 32: 66-76.
37. Smith BR, Johnson GA, Groman EV, Linney E. Magnetic resonance microscopy of mouse embryos. Proc. Natl Acad. Sci. U.S.A. 1994; 91: 3530-3533.