Skip to main content
SpringerLink
Log in

Oxygen Transport Parameter in Plasma Membrane of Eye Lens Fiber Cells by Saturation Recovery EPR

  • Original Paper
  • Published:
Applied Magnetic Resonance Aims and scope Submit manuscript

Abstract

A probability distribution of rate constants contained within an exponential-like saturation recovery (SR) electron paramagnetic resonance signal can be constructed using stretched exponential function fitting parameters. Previously (Stein et al. Appl. Magn. Reson. 2019.), application of this method was limited to the case where only one relaxation process, namely spin–lattice relaxations due to the rotational diffusion of the spin labels in the intact eye-lens membranes, contributed to an exponential-like SR signal. These conditions were achieved for thoroughly deoxygenated samples. Here, the case is described where the second relaxation process, namely Heisenberg exchange between the spin label and molecular oxygen that occurs during bimolecular collisions, contributes to the decay of SR signals. We have further developed the theory for application of stretched exponential function to analyze SR signals involving these two processes. This new approach allows separation of stretched exponential parameters, namely characteristic stretched rates and heterogeneity parameters for both processes. Knowing these parameters allowed us to separately construct the probability distributions of spin–lattice relaxation rates determined by the rotational diffusion of spin labels and the distribution of relaxations induced strictly by collisions with molecular oxygen. The later distribution is determined by the distribution of oxygen diffusion concentration products within the membrane, which forms a sensitive new way to describe membrane fluidity and heterogeneity. This method was validated in silico and by fitting SR signals from spin-labeled intact nuclear fiber cell plasma membranes extracted from porcine eye lenses equilibrated with different fractions of air.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  1. W.K. Subczynski, J.S. Hyde, A. Kusumi, Biochemistry 30, 8578 (1991)

    Google Scholar 

  2. R.J. Pace, S.I. Chan, J. Chem. Phys. 76, 4217 (1982)

    ADS  Google Scholar 

  3. C. Altenbach, D.A. Greenhalgh, H.G. Khorana, W.L. Hubbell, Proc. Natl. Acad. Sci. USA 91, 1667 (1994)

    ADS  Google Scholar 

  4. A. Kusumi, W.K. Subczynski, J.S. Hyde, Proc. Natl. Acad. Sci. USA 79, 1854 (1982)

    ADS  Google Scholar 

  5. W.K. Subczynski, J.S. Hyde, A. Kusumi, Proc. Natl. Acad. Sci. USA 86, 4474 (1989)

    ADS  Google Scholar 

  6. J. Widomska, M. Raguz, W.K. Subczynski, Biochim. Biophys. Acta Biomembr. 1768, 2635 (2007)

    Google Scholar 

  7. W.K. Subczynski, J.S. Hyde, Adv. Exp. Med. Biol. 454, 399–408 (1998)

    Google Scholar 

  8. W.K. Subczynski, L.E. Hopwood, J.S. Hyde, J. Gen. Physiol. 100, 69 (1992)

    Google Scholar 

  9. M. Raguz, L. Mainali, W.J. O’Brien, W.K. Subczynski, Exp. Eye Res. 132, 78 (2015)

    Google Scholar 

  10. W.K. Subczynski, H.M. Swartz, Biol. Magn. Reson. 23, 229–282 (2005)

    Google Scholar 

  11. W.K. Subczynski, J. Widomska, L. Mainali, Adv. Exp. Med. Biol. 977, 27–34 (2017)

    Google Scholar 

  12. I. Ashikawa, J.J. Yin, W.K. Subczynski, J.S. Hyde, T. Kouyama, A. Kusumi, Biochemistry 33, 4947 (1994)

    Google Scholar 

  13. K. Kawasaki, J.J. Yin, W.K. Subczynski, J.S. Hyde, A. Kusumi, Biophys. J. 80, 738 (2001)

    Google Scholar 

  14. M. Raguz, L. Mainali, W.J. O’Brien, W.K. Subczynski, Exp. Eye Res. 120, 138 (2014)

    Google Scholar 

  15. W.K. Subczynski, A. Wisniewska, J.S. Hyde, A. Kusumi, Biophys. J. 92, 1573 (2007)

    ADS  Google Scholar 

  16. M. Raguz, L. Mainali, J. Widomska, W.K. Subczynski, Biochim. Biophys. Acta Biomembr. 1808, 1072 (2011)

    Google Scholar 

  17. W.K. Subczynski, M. Raguz, J. Widomska, Methods Mol. Biol. 606, 247 (2010)

    Google Scholar 

  18. M. Raguz, L. Mainali, J. Widomska, W.K. Subczynski, Chem. Phys. Lipids 164, 819 (2011)

    Google Scholar 

  19. L. Mainali, M. Raguz, W.K. Subczynski, J. Phys. Chem. B 117, 8994 (2013)

    Google Scholar 

  20. W.K. Subczynski, M. Raguz, J. Widomska, L. Mainali, A. Konovalov, J. Membr. Biol. 245, 51 (2012)

    Google Scholar 

  21. L. Mainali, M. Pasenkiewicz-Gierula, W.K. Subczynski, Curr. Eye Res. 45, 162 (2020)

    Google Scholar 

  22. J. Widomska, W.K. Subczynski, L. Mainali, M. Raguz, Cell Biochem. Biophys. 75, 387 (2017)

    Google Scholar 

  23. C. Mailer, R.D. Nielsen, B.H. Robinson, J. Phys. Chem. A 109, 4049 (2005)

    Google Scholar 

  24. D. Marsh, J. Magn. Reson. 290, 38 (2018)

    ADS  Google Scholar 

  25. L. Mainali, J.B. Feix, J.S. Hyde, W.K. Subczynski, J. Magn. Reson. 212, 418 (2011)

    ADS  Google Scholar 

  26. L. Mainali, J.S. Hyde, W.K. Subczynski, J. Magn. Reson. 226, 35 (2013)

    ADS  Google Scholar 

  27. B.H. Robinson, D.A. Haas, C. Mailer, Science 263, 490 (1994)

    ADS  Google Scholar 

  28. W.K. Subczynski, J.S. Hyde, BBA Biomembr. 643, 283 (1981)

    Google Scholar 

  29. L. Huang, V. Grami, Y. Marrero, D. Tang, M.C. Yappert, V. Rasi, D. Borchman, Investig. Ophthalmol. Vis. Sci. 46, 1682 (2005)

    Google Scholar 

  30. C.A. Paterson, J. Zeng, Z. Husseini, D. Borchman, N.A. Delamere, D. Garland, J. Jimenez-Asensio, Curr. Eye Res. 16, 333 (1997)

    Google Scholar 

  31. S. Bassnett, Y. Shi, G.F.J.M. Vrensen, Philos. Trans. R. Soc. B Biol. Sci. 366, 1250 (2011)

    Google Scholar 

  32. T. Gonen, Y. Cheng, J. Kistler, T. Walz, J. Mol. Biol. 342, 1337 (2004)

    Google Scholar 

  33. J. Kistler, S. Bullivant, FEBS Lett. 111, 73 (1980)

    Google Scholar 

  34. V. Vidová, J. Pól, M. Volný, P. Novák, V. Havlícek, S.K. Wiedmer, J.M. Holopainen, J. Lipid Res. 51, 2295 (2010)

    Google Scholar 

  35. R.J.W. Truscott, Ophthalmic Res. 32, 185 (2000)

    Google Scholar 

  36. M.C. Yappert, M. Rujoi, D. Borchman, I. Vorobyov, R. Estrada, Exp. Eye Res. 76, 725 (2003)

    Google Scholar 

  37. D. Borchman, W.C. Byrdwell, M.C. Yappert, Investig. Ophthalmol. Vis. Sci. 35, 3938 (1994)

    Google Scholar 

  38. J.M. Deeley, T.W. Mitchell, X. Wei, J. Korth, J.R. Nealon, S.J. Blanksby, R.J.W. Truscott, Biochim. Biophys. Acta Mol. Cell Biol. Lipids 1781, 288 (2008)

    Google Scholar 

  39. M. Rujoi, R. Estrada, M.C. Yappert, Anal. Chem. 76, 1657 (2004)

    Google Scholar 

  40. M. Raguz, J. Widomska, J. Dillon, E.R. Gaillard, W.K. Subczynski, Biochim. Biophys. Acta Biomembr. 1788, 2380 (2009)

    Google Scholar 

  41. M. Rujoi, J. Jin, D. Borchman, D. Tang, M.C. Yappert, Investig. Ophthalmol. Vis. Sci. 44, 1634 (2003)

    Google Scholar 

  42. P.S. Zelenka, Curr. Eye Res. 3, 1337 (1984)

    Google Scholar 

  43. N. Stein, L. Mainali, J.S. Hyde, W.K. Subczynski, Appl. Magn. Reson. 50, 903 (2019)

    Google Scholar 

  44. D.C. Johnston, Phys. Rev. B Condens. Matter Mater. Phys. 74, 184430 (2006)

    ADS  Google Scholar 

  45. L. Mainali, M. Raguz, W.J. O’Brien, W.K. Subczynski, Exp. Eye Res. 97, 117 (2012)

    Google Scholar 

  46. R. Estrada, M.C. Yappert, J. Mass Spectrom. 39, 1531 (2004)

    ADS  Google Scholar 

  47. R.J. Cenedella, C.R. Fleschner, Curr. Eye Res. 11, 801 (1992)

    Google Scholar 

  48. G. Chandrasekher, R.J. Cenedella, Exp. Eye Res. 60, 707 (1995)

    Google Scholar 

  49. J. Lim, Y.C. Lam, J. Kistler, P.J. Donaldson, Investig. Ophthalmol. Vis. Sci. 46, 2869 (2005)

    Google Scholar 

  50. H. Bloemendal, A. Zweers, F. Vermorken, I. Dunia, E.L. Benedetti, Cell Differ. 1, 91 (1972)

    Google Scholar 

  51. J. Folch, M. Lees, G.H. Sloane Stanley, J. Biol. Chem. 226, 497 (1957)

    Google Scholar 

  52. W.K. Subczynski, C.C. Felix, C.S. Klug, J.S. Hyde, J. Magn. Reson. 176, 244 (2005)

    ADS  Google Scholar 

  53. J.T. Buboltz, Rev. Sci. Instrum. 80, 124301 (2009)

    ADS  Google Scholar 

  54. J. Huang, J.T. Buboltz, G.W. Feigenson, Biochim. Biophys. Acta Biomembr. 1417, 89 (1999)

    Google Scholar 

  55. L. Mainali, M. Raguz, W.J. O’Brien, W.K. Subczynski, Biochim. Biophys. Acta Biomembr. 1828, 1432 (2013)

    Google Scholar 

  56. L. Mainali, T.G. Camenisch, J.S. Hyde, W.K. Subczynski, Appl. Magn. Reson. 48, 1355 (2017)

    Google Scholar 

  57. F.A. Heberle, G.W. Feigenson, Cold Spring Harb. Perspect. Biol. 3, 1 (2011)

    Google Scholar 

  58. K. Simons, W.L.C. Vaz, Annu. Rev. Biophys. Biomol. Struct. 33, 269 (2004)

    Google Scholar 

  59. S. Arumugam, E.P. Petrov, P. Schwille, Biophys. J. 108, 1104 (2015)

    ADS  Google Scholar 

  60. V. Corradi, B.I. Sejdiu, H. Mesa-Galloso, H. Abdizadeh, S.Y. Noskov, S.J. Marrink, D.P. Tieleman, Chem. Rev. 119, 5775 (2019)

    Google Scholar 

  61. T. Fujimoto, I. Parmryd, Front. Cell Dev. Biol. 4, 155 (2017)

    Google Scholar 

  62. D.B. Thibault, C.J. Gillam, A.C. Grey, J. Han, K.L. Schey, J. Am. Soc. Mass Spectrom. 19, 814 (2008)

    Google Scholar 

  63. R.A. Strangeway, J.S. Hyde, T.G. Camenisch, J.W. Sidabras, R.R. Mett, J.R. Anderson, J.J. Ratke, W.K. Subczynski, Cell Biochem. Biophys. 75, 259 (2017)

    Google Scholar 

  64. L. Mainali, J.W. Sidabras, T.G. Camenisch, J.J. Ratke, M. Raguz, J.S. Hyde, W.K. Subczynski, Appl. Magn. Reson. 45, 1343 (2014)

    Google Scholar 

  65. R.R. Mett, J.W. Sidabras, J.R. Anderson, C.S. Klug, J.S. Hyde, J. Magn. Reson. 307, 106585 (2019)

    Google Scholar 

Download references

Acknowledgements

Research reported in this publication was supported by the National Eye Institute of the National Institutes of Health under award number R01 EY015526. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. The authors thank Professor James S. Hyde for all the helpful discussions.

Author information

Authors and Affiliations

  1. Department of Biophysics, Medical College of Wisconsin, 8701 Watertown Plank Road, Milwaukee, WI, 53226, USA

    N. Stein & W. K. Subczynski

Authors
  1. N. Stein
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. W. K. Subczynski
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization, NS, WKS; performed research, NS; data analysis, NS; writing–original draft preparation, NS; review and editing, WKS; visualization, NS; project administration, WKS; funding acquisition, WKS.

Corresponding authors

Correspondence to N. Stein or W. K. Subczynski.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Stein, N., Subczynski, W.K. Oxygen Transport Parameter in Plasma Membrane of Eye Lens Fiber Cells by Saturation Recovery EPR. Appl Magn Reson 52, 61–80 (2021). https://doi.org/10.1007/s00723-020-01237-7

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00723-020-01237-7

Search

Navigation