Energy transfer along Müller cell intermediate filaments isolated from porcine retina: I. Excitons produced by ADH1A dimers upon simultaneous hydrolysis of two ATP molecules

Spectrochim Acta A Mol Biomol Spectrosc. 2021 Apr 5:250:119361. doi: 10.1016/j.saa.2020.119361. Epub 2021 Jan 6.

Abstract

IR exciton propagation was explored in Müller cell (MC) intermediate filaments (IFs) filling a capillary matrix. These IFs have been isolated from porcine retina using different methods, while their properties were almost identical. Therefore, IFs isolated from the whole retinas were used presently. IR excitons were generated by IR radiation at 2 μm wavelength, or by enzymatic ATP hydrolysis, with the energy transferred to IFs. Excitons produced by ATP hydrolysis required simultaneous energy contribution of two ATP molecules, indicating simultaneous hydrolysis of two ATP molecules in the naturally dimeric human alcohol dehydrogenase enzyme (ADH1A). ATP hydrolysis was thus catalyzed by ADH1A…NAD+ enzymatic complexes absorbed at the IF extremities protruding out of the capillary matrix. The IR emission spectra of excitons were dependent on the exciton generation method. We believe this resulted from the exciton energy distribution varying in function of the generation method used. The latter seems reasonable, given the very long excited-state lifetimes, implying low nonradiative relaxation rates. The energy liberated by ATP hydrolysis has been measured directly in these experiments, for the first time. The results demonstrate that contrary to the predictions of equilibrium thermodynamics, the liberated energy is independent on the ATP/ADP concentration ratio, indicating that non-equilibrium reactions take place. Time-resolved experiments with excitons produced by pulsed IR radiation evaluated characteristic exciton propagation and emission times. For the first time, biexcitonic processes were observed in biological objects, whereby simultaneous hydrolysis of two ATP molecules bound to the same dimeric ADH1A molecule generated excitons carrying twice the energy liberated by hydrolysis of a single ATP molecule. The results reported indicate that ATP-liberated energy may be transmitted along natural polypeptide nanofibers in vivo, within and between live cells. These ideas could promote new understanding of the biophysics of life.

Keywords: ADH1A enzyme; ATP; Energy transfer; Excitons; Glial Müller cells; Intermediate filament.

MeSH terms

  • Adenosine Triphosphate
  • Animals
  • Energy Transfer
  • Ependymoglial Cells*
  • Humans
  • Hydrolysis
  • Intermediate Filaments*
  • Retina
  • Swine

Substances

  • Adenosine Triphosphate