Order from disorder: Self-organization in mammalian hair patterning

doi:10.1073/pnas.0609712104

Order from disorder: Self-organization in mammalian hair patterning

Departments of *Molecular Biology and Genetics,
^‡Neuroscience, and
^§Ophthalmology, and
^†Howard Hughes Medical Institute, Johns Hopkins University School of Medicine, Baltimore, MD 21205

Contributed by Jeremy Nathans, November 3, 2006 (received for review October 16, 2006)

Abstract

Hairs, feathers, and scales normally exhibit precise orientations with respect to the body axes. In Frizzled6 (Fz6)^−/− mice, the global orientation of hair follicles is disrupted, leading to waves, whorls, and tufts, each comprising many hundreds of hairs. By analyzing the orientation of developing hair follicles, we observed that the nearly parallel arrangement of wild-type (WT) hairs arises from fields of imperfectly aligned follicles, and that the Fz6 ^−/− hair patterns arise from fields of grossly misoriented or randomly oriented follicles. Despite their large size, both mutant and WT hair follicles display a remarkable and unexpected plasticity, reorienting on a time scale of days in what seems to be a self-organized refinement process. The essential features of this process can be studied with a simple cellular automata model in which a local consensus “rule” acts iteratively to bias each hair's orientation in favor of the average orientation of its neighbors. These experiments define two systems for hair orientation: a global orienting system that acts early in development and is Fz6-dependent, and a local self-organizing system that acts later and is Fz6 independent.

Footnotes

^¶To whom correspondence should be addressed at:
805 Preclinical Teaching Building, 725 North Wolfe Street, Johns Hopkins University School of Medicine, Baltimore, MD 21205.
E-mail: jnathans{at}jhmi.edu
Author contributions: Y.W. and T.B. contributed equally to this work; Y.W., T.B., and J.N. designed research; Y.W. performed research; T.B. and J.N. contributed analytic tools; T.B. analyzed data; J.N. wrote the paper; and J.N. imaged the presented data.
The authors declare no conflict of interest.
This article contains supporting information online at www.pnas.org/cgi/content/full/0609712104/DC1.
↵ ‖ Manneville P, Boccara N, Vichniac GY, Bidaux R (1989) Cellular Automata and Modeling of Complex Physical Systems: Proceedings of the Winter School, February 21–March 2, 1989, Les Houches, France.
Abbreviations:

PCP,

planar cell polarity;

K17,

keratin-17;

Pn,

postnatal day n.