Messages diffuse faster than messengers

doi:10.1073/pnas.0509576103

Messages diffuse faster than messengers

*Department of Physics, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, MA 02139;
^‡Departamento de Física, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Pabellón 1, 1428 Buenos Aires, Argentina;
^§Department of Physiology, University of Pennsylvania, B400 Richards Buildings, 3700 Hamilton Walk, Philadelphia, PA 19104-6085; and
^¶Theoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, NM 87545

Edited by Joseph Schlessinger, Yale University School of Medicine, New Haven, CT, and approved January 24, 2006 (received for review November 3, 2005)

Abstract

In many cell-signaling pathways, information is transmitted by the diffusion of messenger molecules. Diffusion coefficients characterize the messenger's spatial range and the characteristic times of signal propagation. Inside cells, particles usually diffuse in the presence of immobile binding sites (or traps). It is well known that binding to traps results in an effective diffusion coefficient that is smaller than the free coefficient in media free of traps. To measure effective diffusion coefficients in cells, “tagged” particles are often used. Radioactive calcium was used in a giant squid axon and in cytosolic extracts of Xenopus laevis oocytes. Fluorescence recovery after photobleaching yields diffusion coefficients from observations of the distribution of fluorescently labeled proteins. In the absence of traps, free diffusion coefficients give both the rate at which single-particle mean square displacements increase and the rate at which information in the form of inhomogeneities in particle concentration spread out with time. We show here that, in the presence of traps, information diffuses faster than single particles. Thus, messages diffuse faster than messengers. Tagged-particle experiments give the single-particle diffusion coefficients and, thus, can underestimate the rate of diffusive signal propagation.

Footnotes

^‖To whom correspondence should be addressed. E-mail: pearson{at}lanl.gov
Author contributions: B.P., S.P.D., and J.E.P. designed research; B.P., S.P.D., and J.E.P. performed research; and B.P., S.P.D., D.-O.D.M., and J.E.P. wrote the paper.
Conflict of interest statement: No conflicts declared.
This paper was submitted directly (Track II) to the PNAS office.
Abbreviations:

Abbreviations:

MP,

measurement point;

IP,

point at which the bolus is added;

FRAP,

fluorescence recovery after photobleaching.
Freely available online through the PNAS open access option.