Multiexponential proton relaxation in model cellular systems

Water proton relaxation measurements obtained from model cellular systems composed of red blood cell (RBC) ghosts are presented. The purpose of the investigation was to evaluate hypotheses concerning the possible sources of multiple exponential components in similar relaxation measurements made on tissue. Both laboratory frame transverse and longitudinal relaxation rates, as well as rotating frame relaxation rates, were measured in preparations of RBC ghosts and “extracellular fluid” that were, (a) uniformly mixed or (b) compartmentalized by layering, as the concentration of serum albumin was varied in the “extracellular fluid.” The data show that although transmembrane exchange is too fast to give rise to multiexponential relaxation, multiple components can result from compartmentalization at the level of the cellular organization and do not necessarily require different tissue types. In addition, the data clearly demonstrate the importance of protein adsorption to cellular membranes as a determinant of the concentration of freely mobile solute protein molecules in tissue fluids. © 1991 Academic Press, Inc.

[1]  Alex L. MacKay,et al.  Quantitative interpretation of NMR relaxation data , 1989 .

[2]  D. Chang,et al.  Nuclear magnetic resonance study of squid giant axon. , 1980, Biochimica et biophysica acta.

[3]  H. Eisendrath,et al.  Analysis by the Carr–Purcell–Meiboom–Gill sequence of the influence of P388 leukemia and of cis‐diamminedichloroplatinum(II) nephrotoxicity on water compartmentalization in kidneys and spleens of mice , 1988, Magnetic resonance in medicine.

[4]  S. H. Koenig,et al.  Determinants of Proton Relaxation Rates in Tissue , 1984, Magnetic resonance in medicine.

[5]  W. Brittin,et al.  Nuclear Magnetic Resonance Studies in Multiple Phase Systems: Lifetime of a Water Molecule in an Adsorbing Phase on Silica Gel , 1957 .

[6]  A. K. Solomon,et al.  Role of membrane proteins and lipids in water diffusion across red cell membranes. , 1984, Biochimica et biophysica acta.

[7]  R. Knispel,et al.  Dispersion of proton spin-lattice relaxation in tissues☆ , 1974 .

[8]  T. J. Swift,et al.  A proton spin-echo study of the state of water in frog nerves. , 1969, Biophysical journal.

[9]  J. Brahm Diffusional water permeability of human erythrocytes and their ghosts , 1982, The Journal of general physiology.

[10]  Daniel Canet,et al.  Frequency dependence of water proton longitudinal nuclear magnetic relaxation times in mouse tissues at 20°C , 1982 .

[11]  Seymour H. Koenig,et al.  The Dynamics of Water-Protein Interactions: Results from Measurements of Nuclear Magnetic Relaxation Dispersion , 1980 .

[12]  D. Marquardt An Algorithm for Least-Squares Estimation of Nonlinear Parameters , 1963 .

[13]  S. Conti Proton magnetic relaxation dispersion in aqueous biopolymer systems. I: Fibrinogen solutions , 1986 .

[14]  R. Freeman,et al.  Fourier Transform Study of NMR Spin–Spin Relaxation , 1971 .

[15]  E. Finch,et al.  Proton nuclear magnetic resonance relaxation measurements in frog muscle. , 1974, Biophysical journal.

[16]  I. Kuntz,et al.  The properties of water in biological systems. , 1974, Annual review of biophysics and bioengineering.

[17]  M. E. Clark,et al.  Water in barnacle muscle. III. NMR studies of fresh fibers and membrane-damaged fibers equilibrated with selected solutes. , 1981, Biophysical journal.

[18]  R. Outhred,et al.  The temperature dependence of erythrocyte water diffusion permeability. , 1978, Biochimica et biophysica acta.

[19]  M. Pintar,et al.  Origin of the nonexponentiality of the water proton spin relaxations in tissues. , 1975, Biophysical journal.

[20]  S. Law,et al.  The adsorption of bovine serum albumin by liposomes , 1986 .

[21]  G. Raaphorst,et al.  Nuclear magnetic resonance study of mammalian cell water influence of water content and ionic environment. , 1975, Biophysical journal.

[22]  J L Potter,et al.  NMR relaxation of protons in tissues and other macromolecular water solutions. , 1982, Magnetic resonance imaging.

[23]  E. Purcell,et al.  Effects of Diffusion on Free Precession in Nuclear Magnetic Resonance Experiments , 1954 .

[24]  R. Vré The NMR studies of water in biological systems. , 1980 .

[25]  F. Noack,et al.  NMR relaxation investigation of water mobility in aqueous bovine serum albumin solutions. , 1976, Biochimica et biophysica acta.

[26]  B. Fung,et al.  The state of water in muscle as studied by pulsed NMR. , 1974, Biochimica et biophysica acta.

[27]  P. Allen,et al.  Application of continuous relaxation time distributions to the fitting of data from model systmes and excised tissue , 1991, Magnetic resonance in medicine.

[28]  C. Hazlewood,et al.  Spin Echo Studies on Cellular Water , 1972, Nature.

[29]  S. Meiboom,et al.  Modified Spin‐Echo Method for Measuring Nuclear Relaxation Times , 1958 .

[30]  S. Conti Proton magnetic relaxation dispersion in aqueous biopolymer systems , 1986 .

[31]  K. J. Packer,et al.  Pulsed NMR studies of water in striated muscle non-freezing factor of water II. Spin-lattice relaxation times and the dynamics of the non-freezing fraction of water , 1973 .

[32]  J. Vriend,et al.  Multi-exponential water proton spin-lattice relaxation in biological tissues and its implications for quantitative NMR imaging. , 1984, Physics in medicine and biology.

[33]  J. Oakes,et al.  Protein hydration. Nuclear magnetic resonance relaxation studies of the state of water in native bovine serum albumin solutions , 1976 .

[34]  A proton NMR relaxation evaluation of a model of brain oedema fluid. , 1986, Physics in medicine and biology.

[35]  P. Belton,et al.  NMR and compartmentation in biological tissues , 1985 .

[36]  E. George,et al.  Water and ions in muscles and model systems. , 1973, Biophysical journal.

[37]  Modeling of proton spin relaxation in muscle tissue using nuclear magnetic resonance spin grouping and exchange analysis. , 1986, Biophysical journal.

[38]  B. Nichols,et al.  Evidence for the Existence of a Minimum of Two Phases of Ordered Water in Skeletal Muscle , 1969, Nature.

[39]  P. Allen,et al.  Solvent proton relaxation of aqueous solutions of the serum proteins alpha 2-macroglobulin, fibrinogen, and albumin. , 1990, Biophysical journal.

[40]  E. Hahn,et al.  Nuclear Double Resonance in the Rotating Frame , 1962 .