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Prospects for NMR imaging in the study of biological morphogenesis

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Summary

Small objects can be visualised with a spatial resolution that approaches microscopic dimensions using the technique of high resolution nuclear magnetic resonance (NMR) imaging. Some important features of the method are described and the prospects for using the technique to study morphogenesis are discussed. It is concluded that NMR imaging, in conjunction with the related method of localised spectroscopy, is capable of producing novel structural information.

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References

  1. Agris, P. F., and Campbell, I. D., Proton nuclear magnetic resonance of intact friend leukemia cells: phosphorylcholine increase during differentiation. Science216 (1982) 1325–1327.

    Article  CAS  PubMed  Google Scholar 

  2. Aguayo, J. B., Blackband, S. J., Schoeniger, J., Mattingly, M. A., and Hintermann, M., Nuclear magnetic resonance imaging of a single cell. Nature322 (1986) 190–191.

    Article  CAS  PubMed  Google Scholar 

  3. Aue, W. P., Localisation methods forin vivo nuclear magnetic resonance spectroscopy. Rev. magn. Reson. Med.1 (1986) 21–72.

    Google Scholar 

  4. Avison, M. J., Hetherington, H. P., and Shulman, R. G., Applications of NMR to studies of tissue metabolism. A. Rev. Biophys. Biophys. Chem.15 (1986) 377–402.

    Article  CAS  Google Scholar 

  5. Barton, J. K., Den Hollander, J. A., Hopfield, J. J., and Shulman, R. G.,13C nuclear magnetic resonance study of trehalose mobilisation in yeast spores. J. Bact.151 (1982) 177–185.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Baxter, R. L., Microbiological applications of NMR spectroscopy. Microbiol. Sci.2 (1985) 203–211; 340–345.

    CAS  PubMed  Google Scholar 

  7. Belton, P. S., Gordon, R. E., Jones, J. M., and Shaw, D., A31P topical magnetic resonance study of embryonic development in hens' eggs. Br. Poul. Sci.24 (1983) 429–433.

    Article  CAS  Google Scholar 

  8. Belton, P. S., and Ratcliffe, R. G., NMR and compartmentation in biological tissues. Prog. NMR Spec.17 (1985) 241–279.

    Article  CAS  Google Scholar 

  9. Budinger, T. F., Thresholds for physiological effects due to rf and magnetic fields used in NMR imaging. IEEE Trans. Nucl. Sci. NS-26 (1979) 2821–2825.

    Article  Google Scholar 

  10. Busa, W. B., and Crowe, J. H., Intracellular pH regulates transitions between dormancy and development of brine shrimp (Artemia salina) embryos. Science221 (1983) 366–368.

    Article  CAS  PubMed  Google Scholar 

  11. Busa, W. B., Crowe, J. H., and Matson, G. B., Intracellular pH and the metabolic status of dormant and developingArtemia embryos. Archs Biochem. Biophys.216 (1982) 711–718.

    Article  CAS  Google Scholar 

  12. Busa, W. B., and Nuccitelli, R., Metabolic regulation via intracellular pH. Am. J. Physiol.246 (1984) R409-R438.

    CAS  PubMed  Google Scholar 

  13. Cassone, A., Carpinelli, G., Angiolella, L., Maddaluno, G., and Podo, F.31P nuclear magnetic resonance study of growth and dimorphic transition inCandida albicans. J. gen. Microbiol.129 (1983) 1569–1575.

    CAS  PubMed  Google Scholar 

  14. Chen, S., Elofson, R. M., and MacTaggart, J. M., Carbon-13 nuclear magnetic resonance studies of lipids and starch digestion in intact seeds. J. Agric. Food Chem.27 (1979) 435–438.

    Article  CAS  Google Scholar 

  15. Colman, A., and Gadian, D. G.,31P nuclear magnetic resonance studies on the developing embryos ofXenopus laevis. Eur. J. Biochem.61 (1976) 387–396.

    Article  CAS  PubMed  Google Scholar 

  16. Colnago, L. A., and Seidl, P. R., Application of carbon-13 nuclear magnetic resonance to the germination of soybean seeds in vivo. J. Agric. Food Chem.31 (1983) 459–461.

    Article  CAS  Google Scholar 

  17. Connelly, A., Lohman, J. A. B., Loughman, B. C., Quiquampoix, H., and Ratcliffe, R. G., High resolution imaging of plant tissues by NMR. J. exp. Bot.38 (1987) 195.

    Article  Google Scholar 

  18. Cooke, P., and Morris, P. G., The effects of NMR exposure on living organisms. 2 A genetic study of human lymphocytes. Br. J. Radiol.54 (1981) 622–625.

    Article  CAS  PubMed  Google Scholar 

  19. Delfini, M., Angelini, R., Bruno, F., Conti, F., Di Cocco, E., Giuliani, A. M., and Manes, F., Phosphate metabolites in germinating lettuce seeds observed by31P NMR spectroscopy. Cell molec. Biol.31 (1985) 385–389.

    CAS  Google Scholar 

  20. Derome, A. E., Modern NMR techniques for chemistry research. Pergamon Press, Oxford 1987.

    Google Scholar 

  21. Deslauriers, R., Byrd, R. A., Jarrell, H. C., and Smith, I. C. P.,31P NMR studies of vegetative and encysted cells ofAcanthamoeba castellanii. Observation of phosphonic acids in live cells. Eur. J. Biochem.111 (1980) 369–375.

    Article  CAS  PubMed  Google Scholar 

  22. Deslauriers, R., Jarrell, H. C., Byrd, R. A., and Smith, I. C. P., Observation by13C NMR of metabolites in differentiating amoeba. Trehalose storage in encystedAcanthamoeba castellanii. FEBS Lett.118 (1980) 185–190.

    Article  CAS  PubMed  Google Scholar 

  23. Dickinson, J. R., Dawes, I. W., Boyd, A. S. F., and Baxter, R. L.,13C NMR studies of acetate metabolism during sporulation ofSaccharomyces cerevisiae. Proc. natl Acad. Sci. USA80 (1983) 5847–5851.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Drinkwater, L. E., and Crowe, J. H., Regulation of embryonic diapause inArtemia: environmental and physiological signals. J. exp. Zool.241 (1987) 297–307.

    Article  CAS  Google Scholar 

  25. Eccles, C. D., Callaghan, P. T., and Jenner, C. F., Biophys. J. (1987) submitted for publication.

  26. Gadian, D. G., Nuclear magnetic resonance and its applications to living systems. Clarendon Press, Oxford 1982.

    Google Scholar 

  27. Gassner, G., and Lohman, J. A. B., Combined proton NMR imaging and spectral analysis of locust embryonic development. Proc. natl Acad. Sci. USA84 (1987) 5297.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Gillies, R. J., Ugurbil, K., Den Hollander, J. A., and Shulman, R. G.,31P NMR studies of intracellular pH and phosphate metabolism during cell division cycle ofSaccharomyces cerevisiae. Proc. natl Acad. Sci. USA78 (1981) 2125–2129.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Gupta, R. K., Kostellow, A. B., and Morrill, G. A., NMR studies of intracellular sodium ions in amphibian oocytes, ovulated eggs and early embryos. J. biol. Chem.260 (1985) 9203–9208.

    Article  CAS  PubMed  Google Scholar 

  30. Hanstock, C. G., Rothman, D. L., Jue, T., and Shulman, R. G., J. magn. Reson. (1988) submitted for publication.

  31. Inoue, H., and Yoshioka, T., Measurement of intracellular pH in sea urchin eggs by31P NMR. J. cell. Physiol.105 (1980) 461–468.

    Article  CAS  PubMed  Google Scholar 

  32. Kay, R. R., Gadian, D. G., and Williams, S. R., Intracellular pH inDictyostelium: a31P nuclear magnetic resonance study of its regulation and possible role in controlling cell differentiation. J. Cell Sci.93 (1986) 165–179.

    Article  Google Scholar 

  33. Kean, D. M., and Smith, M. A., Magnetic resonance imaging. Principles and applications. William Heinemann Medical Books, London 1986.

    Google Scholar 

  34. Lohman, J. A. B., Ordidge, R. J., and Connelly, A., Spin echo imaging of multiple chemical shifts. Magn. Reson. Med.5 (1987) 83 (and references quoted therein).

    Article  CAS  PubMed  Google Scholar 

  35. Mathur-de Vre, R., The NMR studies of water in biological systems. Prog. Biophys. molec. Biol.35 (1979) 103–134.

    Article  CAS  Google Scholar 

  36. McCain, D. C.,31P NMR study of turnip seed germination and sprout growth inhibition by peroxydisulphate ion. Biochim. biophys. Acta763 (1983) 231–236.

    Article  CAS  Google Scholar 

  37. Morrill, G. A., Kostellow, A. B., Mahajan, S., and Gupta, R. K., Role of calcium in regulating intracellular pH following the stepwise release of the metabolic blocks at first meiotic prophase and second meiotic metaphase in amphibian oocytes. Biochim. biophys. Acta804 (1984) 107–117.

    Article  CAS  PubMed  Google Scholar 

  38. Morrill, G. A., Weinstein, S. P., Kostellow, A. B., and Gupta, R. K., Studies of insulin action on the amphibian oocyte plasma membrane using NMR, electrophysiological and ion flux techniques. Biochim. biophys. Acta844 (1985) 371–392.

    Google Scholar 

  39. Morris, P. G., Nuclear magnetic resonance imaging in medicine and biology. Clarendon Press, Oxford 1986.

    Google Scholar 

  40. Moore, G. R., Ratcliffe, R. G., and Williams, R. J. P., NMR and the biochemist. Essays Biochem.19 (1983) 142–195.

    CAS  PubMed  Google Scholar 

  41. Nuccitelli, R., and Heiple, J. M., Summary of the evidence and discussion concerning the involvement of pHi in the control of cellular functions, in intracellular pH: its measurement, regulation and utilisation in cellular functions, pp. 567–586. Eds. R. A. Nuccitelli and D. W. Deamer. A.R. Liss Inc., New York 1982.

    Google Scholar 

  42. Nuccitelli, R., Webb, D. J., Lagier, S. T., and Matson, G. B.,31P NMR reveals increased intracellular pH after fertilization inXenopus eggs. Proc. natl Acad. Sci. USA78 (1981) 4421–4425.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Ogawa, S., Lee, T. M., and Glyn, P., Energy metabolism in rat brainin vivo studied by31P nuclear magnetic resonance: changes during postnatal development. Archs Biochem. Biophys.248 (1986) 43–45.

    Article  CAS  Google Scholar 

  44. Ordidge, R. J., Connelly, A., and Lohman, J. A. B., Image-selectedin vivo spectroscopy (ISIS). A new technique for spatially selective NMR spectroscopy. J. magn. Reson.66 (1986) 283–294.

    CAS  Google Scholar 

  45. Overall, R., and Jaffe, L. F., Patterns of ionic current throughDrosophila follicles and eggs. Devl Biol.108 (1985) 102–119.

    Article  CAS  Google Scholar 

  46. Prasad, N., Wright D. A., and Forster, J. D., Effects of nuclear magnetic resonance on early stages of amphibian development. Magn. Reson. Imag.1 (1982) 35–37.

    Article  CAS  Google Scholar 

  47. Prato, F. S., Ossenkopp, K. P., Kavaliers, M., Sestine, E., and Teskey, G. C., Attenuation of morphine-induced analgesia in mice by exposure to magnetic resonance imaging: separate effects of the static, radiofrequency and time-varying magnetic fields. Magn. Reson. Imag.5 (1987) 9–14.

    Article  CAS  Google Scholar 

  48. Ratcliffe, R. G., Application of nuclear magnetic resonance methods to plant tissues. Meth. Enzymol.148 (1987) 683–700.

    Article  CAS  Google Scholar 

  49. Satre, M., Klein, G., and Martin, J. B., Intracellular pH control inDictyostelium discoideum: a31P NMR analysis. Biochimie68 (1986) 1253–1261.

    Article  CAS  PubMed  Google Scholar 

  50. Schaefer, J., Regeneration in alfalfa tissue culture. Characterisation of intracellular pH during somatic embryo production by solid state31P NMR. Plant Physiol.79 (1985) 584–589.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Skokut, T. A., Manchester, J., and Schaefer, J., Regeneration in alfalfa tissue culture. Stimulation of somatic embryo production by amino acids and N-15 NMR determination of nitrogen utilisation. Plant Physiol.79 (1985) 579–583.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Thevelein, J. M., Den Hollander, J. A., and Shulman, R. G., Changes in the activity and properties of trehalase during early germination of yeast asco spores. Correlation with trehalose breakdown as studied byin vivo 13C NMR. Proc. natl Acad. Sci. USA79 (1982) 3503–3507.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Thomas, A., and Morris, P. G., The effects of NMR exposure on living organisms. 1 A microbial assay. Br. J. Radiol.54 (1981) 615–621.

    Article  CAS  PubMed  Google Scholar 

  54. Van Laere, A., Francois, A., Overloop, K., Verbeke, M., and Van Gerven, L., Relation between germination, trehalose and the status of water inPhycomyces blakesleeanus spores as measured by proton NMR. J. gen. Microbiol.133 (1987) 239–245.

    Google Scholar 

  55. Wayne, R., Rice, D., and Hepler, P. K., Intracellular pH does not change during phytochrome-mediated spore germination inOnoclea. Devl Biol.113 (1986) 97–103.

    Article  CAS  Google Scholar 

  56. Williams, S. R., and Gadian, D. G., Tissue metabolism studied in vivo by nuclear magnetic resonance. J. exp. Physiol.71 (1986) 335–360.

    Article  CAS  Google Scholar 

  57. Winkler, M. M., Matson, G. B., Hershey, J. W. B., and Bradbury, E. M.,31P NMR study of the activation of the sea urchin egg. Exp. Cell Res.139 (1982) 217–222.

    Article  CAS  PubMed  Google Scholar 

  58. Wuethrich, K., NMR of proteins and nucleic acids. Wiley, New York 1986.

    Google Scholar 

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Author notes

  1. R. G. Ratcliffe

    Present address: MR Physics, Philips Medical Systems, P.O. Box 10 000, Best, The Netherlands

Authors and Affiliations

  1. Oxford Research Systems Limited, Nuffield Way, OX14 1RY, Abingdon, Oxon, England

    J. A. B. Lohman

  2. Department of Plant Sciences, University of Oxford, Agricultural Science Building, Parks Road, OX1 3PF, Oxford, England

    R. G. Ratcliffe

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Lohman, J.A.B., Ratcliffe, R.G. Prospects for NMR imaging in the study of biological morphogenesis. Experientia 44, 666–672 (1988). https://doi.org/10.1007/BF01941027

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