SpringerProtocols: Abstract: 3. Magnetic Resonance Imaging of Embryonic and Fetal Development in Model Systems

3. Magnetic Resonance Imaging of Embryonic and Fetal Development in Model Systems

By: Eric T. Ahrens², Mangala Srinivas³, Saverio Capuano⁴, Hyagriv N. Simhan⁵, Gerald P. Schatten⁶

Abstract

Full Text

Download PDF (651K)

We give an overview of the applications and methods of high-resolution anatomical magnetic resonance imaging (MRI) in the study of embryonic and fetal development in animal models. Challenges associated with performing in utero studies are described. Recent in utero images in mouse and in nonhuman primates are presented. Results using magnetic resonance microscopy in fixed mouse embryos and in amphibian embryos in vivo are reviewed. We discuss how studies of pregnancy in animal models aid in the translation of innovative new MRI techniques to clinical applications.

Affiliation(s): (2) Department of Biological Sciences and the Pittsburgh NMR Center for Biomedical Research, Carnegie Mellon University, Pittsburgh, PA
(3) Department of Biological Sciences and the Pittsburgh NMR Center for Biomedical Research, Carnegie Mellon University, Pittsburgh, PA
(4) Pittsburgh Development Center, Magee-Womenrrses Research Institute, Pittsburgh, PA
(5) Pittsburgh Development Center, Magee-Womenrrses Research Institute, Pittsburgh, PA
(6) Pittsburgh Development Center, Magee-Womenrrses Research Institute, Pittsburgh, PA

Book Title: Magnetic Resonance Imaging: Methods and Biologic Applications

Series: Methods in Molecular Medicine | Volume: 124 | Pub. Date: Nov-01-2005 | Page Range: 87-101 | DOI: 10.1385/1-59745-010-3:87

Subject: Imaging/Radiology

Key Words: In utero MRI - embryo - fetus - primate - developmental biology

References

Download References

1.	Smith B. R., Johnson G. A., Groman E. V., and Linney E. (1994) Magneticresonance microscopy of mouse embryos. Proc. Natl. Acad. Sci. USA 91, 3530–3533.

2.	Smith B. R. (1999) Magnetic resonance microscopy for developmental biology. Dev. Biol. 210, 222–222.

3.	Jacobs R. E., Ahrens E. T., Meade T. J., and Fraser S. E. (1999) Looking deeper into vertebrate development. Trends Cell Biol. 9, 73–76.

4.	Jacobs R. E., Ahrens E. T., Dickinson M. E., and Laidlaw D. (1999) Towards a microMRI atlas of mouse development. Comput. Med. Imaging Graph. 23, 15–24.

5.	Ahrens E. T., Blumenthal J., Jacobs R. E., and Giedd J. N. (2000) Imaging brain development, in: Brain Mapping: The Systems (Toga A. W. and Mazziotta J. C., eds.), Academic, San Diego, CA, pp. 561–589.

6.	Dhenain M., Ruffins S. W., and Jacobs R. E. (2001) Three-dimensional digital mouse atlas using high-resolution MRI. Dev. Biol. 232, 458–470.

7.	Benveniste H., Fowler J. S., Rooney W. D., et al. (2003) Maternal-fetal in vivo imaging: a combined PET and MRI study. J. Nucl. Med. 44, 1522–1530.

8.	Schatten G., Hewitson L., Simerly C., Sutovsky P., and Huszar G. (1998) Cell and molecular biological challenges of ICSI: ART before science? Law Med. Ethics 26, 29–37.

9.	Chan A. W. S., Chong K. Y., Martinovich C., Simerly C., and Schatten G. (2001) Transgenic monkeys produced by retroviral gene transfer into mature oocytes. Science 291, 309–312.

10.	Wilmut I., Schnieke A. E., McWhir J., Kind A. J., and Campbell K. H. S. (1997) Viable offspring derived from fetal and adult mammalian cells. Nature 385, 810–813.

11.	Campbell K. H. S., McWhir J., Ritchie W. A., and Wilmut I. (1996) Sheep cloned by nuclear transfer from a cultured cell line. Nature 380, 64–66.

12.	Stark D. D. and Bradley Jr. W. G., eds. (1992) Magnetic Resonance Imaging. 2nd ed., vols. 1 and 2, Mosby-Year Book, St. Louis, MO.

13.	Liang Z. P. and Lauterbur P. C. (2000) Principles of Magnetic Resonance Imaging: A Signal Processing Perspective. IEEE, Piscataway, NJ.

14.	Cassidy P. J., Schneider J. E., Grieve S. M., Lygate C., Neubauer S., and Clarke K. (2004) Assessment of motion gating strategies for mouse magnetic resonance at high magnetic fields. J. Magn. Reson. Imaging 19, 229–237.

15.	Wiesmann F., Szimtenings M., Frydrychowicz A., et al. (2003) High-resolution MRI with cardiac and respiratory gating allows for accurate in vivo atherosclerotic plaque visualization in the murine aortic arch. Magn. Reson. Med. 50, 69–74.

16.	Hofman M. B. M., Paschal C. B., Li D. B., Haacke E. M., Vanrossum A. C., and Sprenger M. (1995) MRI of coronary arteries-2D breath-hold vs 3D respiratory-gated acquisition. J. Comput. Assist. Tomogr. 19, 56–62.

17.	Lenz G. W., Haacke E. M., and White R. D. (1989) Retrospective cardiac gating-a review of technical aspects and future-directions. Magn. Reson. Imaging 7, 445–455.

18.	Korin H. W., Felmlee J. P., Riederer S. J., and Ehman R. L. (1995) Spatialfrequency-tuned markers and adaptive correction for rotational motion. Magn. Reson. Med. 33, 663–669.

19.	Wood M. L., Shivji M. J., and Stanchev P. L. (1995) Planar-motion correction with use of k-space data acquired in Fourier MR-imaging. J. Magn. Reson. Imaging 5, 57–64.

20.	Hedley M. and Yan H. (1992) Motion artifact suppression-a review of postprocessing techniques. Magn. Reson. Imaging 10, 627–635.

21.	Ehman R. L. and Felmlee J. P. (1989) Adaptive technique for high-definition MR imaging of moving structures. Radiology 173, 255–263.

22.	Callaghan P. T. (1991) Principles of Nuclear Magnetic Resonance Microscopy, Oxford University Press, New York, NY.

23.	Ahrens E. T. and Dubowitz D. J. (2001) Peripheral somatosensory fMRI in mouse at 11.7 T. NMR Biomed. 14, 318–324.

24.	Dwyer R., Fee J. P., and Moore J. (1995) Uptake of halothane and isoflurane by mother and baby during caesarean section. Br. J. Anaesth. 74, 379–383.

25.	Muir W., Hubbell J., and Skarda, R. (1989) Handbook of Veterinary Anesthesia. Mosby, St. Louis, MO, pp. 95–107.

26.	Ramanathan S., Gandhi S., Arismendy J., Chalon J., and Turndorf H. (1982) Oxygen transfer from mother to fetus during cesarean section under epidural anesthesia. Anesth. Analg. 61, 576–581.

27.	Heynick L. and Merritt J. (2003) Radiofrequency fields and teratogenesis. Bioelectromagnetics Suppl 6, S174–S186.

28.	Espinar A., Piera V., Carmona A., and Guerrero J. (1997) Histological changes during development of the cerebellum in the chick embryo exposed to a static magnetic field. Bioelectromagnetics 18, 36–46.

29.	Denegre J., Valles J., Lin K., Jordan W., and Mowry K. (1998) Cleavage planes in frog eggs are altered by strong magnetic fields. Proc. Natl. Acad. Sci. USA 95, 14,729–14,732.

30.	Narra V. R., Howell R. W., Goddu S. M., Rao D. V. (1996) Effects of a 1.5-Tesla static magnetic field on spermatogenesis and embryogenesis in mice. Invest. Radiol. 31, 586–590.

31.	Canedo L., Cantu R., and Hernandez J. (2003) Magnetic field exposure during gestation: pineal and cerebral cortex serotonin in the rat. Int. J. Dev. Neurosci. 52, 263.

32.	Allahyar K. and Robitaille P. (2000) Biological effects and health implications in magnetic resonance imaging. Concepts Magnetic Res. 15, 321–359.

33.	Iwasaka M., Ueno S, and Tsuda H. (1994) Effects of magnetic fields on fibrinolysis. J. Appl. Phys. 75, 7162–7164.

34.	Lary J. M., Conover D. L., Johnson P. H., and Hornung R. W. (1986) Doseresponse relationship between body-temperature and birth defects in radio frequency-irradiated rats. Bioelectromagnetics 7, 141–149.

35.	Levine D., Zuo C., Faro C., and Chen Q. (2001) Potential heating effect in the gravid uterus during MR HASTE imaging. J. Magn. Reson. Imaging 13, 856–861.

36.	Johnson G. A., Benveniste H., Black R. D., Hedlund L. W., Maronpot R. R., and Smith B. R. (1993) Histology by magnetic resonance microscopy. Magn. Reson. Q. 9, 1–30.

37.	Johnson G. A., Cofer G. P., Gewalt S. L., and Hedlund L. W. (2002) Morphologic phenotyping with MR microscopy: the visible mouse. Radiology 222, 789–793.

38.	Smith B. R., Linney E., Huff D. S., and Johnson G. A. (1996) Magnetic resonance microscopy of embryos. Comput. Med. Imaging Graph. 20, 483–490.

39.	Schneider J. E., Bamforth S. D., Grieve S. M., Clarke K., Bhattacharya S., and Neubauer S. (2003) High-resolution, high-throughput magnetic resonance imaging of mouse embryonic anatomy using a fast gradient-echo sequence. MAGMA 16, 43–51.

40.	Chapon C., Franconi F., Roux J., Marescaux L., Le Jeune J. J., and Lemaire L. (2002) In utero time-course assessment of mouse embryo development using high resolution magnetic resonance imaging. Anat. Embryol. 206, 131–137.

41.	Kornguth S., Bersu E., Anderson M., and Markley J. (1992) Correlation of increased levels of class-I MHC H-2K(k) in the placenta of murine trisomy-16 conceptuses with structural abnormalities revealed by magnetic resonance microscopy. Teratology 45, 383–391.

42.	Basser P. J. and Pierpaoli C. (1996) Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J. Magn. Reson. B 111, 209–219.

43.	Ahrens E. T., Narasimhan P. T., Nakada T., and Jacobs R. E. (2002) Small animal neuroimaging using magnetic resonance microscopy. Prog. Nucl. Mag. Res. 40, 275–306.

44.	Zhang J. Y., Richards L. J., Yarowsky P., Huang H., van Zijl P. C. M., and Mori S. (2003) Three-dimensional anatomical characterization of the developing mouse brain by diffusion tensor microimaging. Neuroimage 20, 1639–1648

45.	Glastonbury C. M. and Kennedy A. M. (2002) Ultrafast MRI of the fetus Australas. Radiol. 46, 22–32.

46.	Levine D. (2001) Ultrasound versus magnetic resonance imaging in fetal evaluation. Top. Magn. Reson. Imaging 12, 25–38.

47.	Aguayo J. B., Blackband S. J., Schoeniger J., Mattingly M. A., and Hintermann M. (1986) NMR imaging of a single cell. Nature 322, 190–191.

48.	Jacobs R. E. and Fraser S. E. (1994) Magnetic resonance microscopy of embryonic cell lineages and movement. Science 263, 681–684.

49.	Louie A. Y., Huber M. M., Ahrens E. T., et al. (2000) In vivo visualization of gene expression using magnetic resonance imaging. Nat. Biotechnol. 18, 321–325.

50.	Ahrens E. T., Rothbacher U., Jacobs R. E., and Fraser S. E. (1998) A model for MRI contrast enhancement using T1 agents. Proc. Natl. Acad. Sci. USA 95, 8443–8448.

51.	Huber M. M., Staubli A. B., Kustedjo K., et al. (1998) Fluorescently detectable magnetic resonance imaging agents. Bioconjugate Chem. 9, 242–249.

52.	Pauser S., Keller K., Zschunke A., and Mugge C. (1993) Study of the membrane premeability of a paramagnetic metal complex on single cells by NMR microscopy. Magn. Reson. Imaging 11, 419–424.

53.	Sehy J. V., Ackerman J. J. H., and Neil J. J. (2002) Apparent diffusion of water, ions, and small molecules in the Xenopus oocyte is consistent with Brownian displacement. Magn. Reson. Med. 48, 42–51.

54.	Sehy J. V., Ackerman J. J. H., and Neil J. J. (2001) Water and lipid MRI of the Xenopus oocyte. Magn. Reson. Med. 46, 900–906.

55.	Pascolo L., Cupelli F., Anelli P. L., et al. (1999) Molecular mechanisms for the hepatic uptake of magnetic resonance imaging contrast agents. Biochem. Biophys. Res. Commun. 257, 746–752.

56.	Wald L. L., Carvajal L., Moyher S. E., et al. (1995) Phased-array detectors and an automated intensity-correction algorithm for high-resolution MR-imaging of the human brain. Magn. Reson. Med. 34, 433–439.

57.	Fenyes D. A. and Narayana P. A. (1998) In vivo echo-planar imaging of rat spinal cord. Magn. Reson. Imaging 16, 1249–1255.

58.	Arnder L. L., Shattuck M. D., and Black R. D. (1996) Signal-to-noise ratio comparison between surface coils and implanted coils. Magn. Reson. Med. 35, 727–733.

59.	Ahrens E. T., Feili-Hariri M., Xu H., Genove G., and Morel P. A. (2003) Receptor-mediated endocytosis of iron-oxide particles provides efficient labeling of dendritic cells for in vivo MR imaging. Magn. Reson. Med. 49, 1006–1013.

60.	Weissleder R., Cheng H. C., Bogdanova A., and Bogdanov A. (1997) Magnetically labeled cells can be detected by MR imaging. J. Magn. Reson. Imaging 7, 258–263.

61.	Contag C. H. and Bachmann M. H. (2002) Advances in vivo bioluminescence imaging of gene expression. Annu. Rev. Biomed. Eng. 4, 235–260.

62.	Costa G. L., Sandora M. R., Nakajima A., et al. (2001) Adoptive immunotherapy of experimental autoimmune encephalomyelitis via T cell delivery of the IL-12 p40 subunit. J. Immunol. 167, 2379–2387.

63.	Gambhir S. S., Barrio J. R., Phelps M. E., et al. (1999) Imaging adenoviraldirected reporter gene expression in living animals with positron emission tomography. Proc. Natl. Acad. Sci. USA 96, 2333–2338.

Comments (Loading...)

Post comment/View all comments