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Cited by 63Hair Growth and DisordersDevelopmental Biology and Gene Regulationmelanin and skin pigmentation

Module‐based complexity formation: periodic patterning in feathers and hairs

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Chuong, Cheng‐Ming, Yeh, Chao‐Yuan, Ting‐Xin, Jiang, Widelitz, Randall·2013·WIREs Developmental Biology
DOI 10.1002/wdev.74PMC PMC3607644
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Abstract

Patterns describe order which emerges from homogeneity. Complex patterns on the integument are striking because of their visibility throughout an organism's lifespan. Periodic patterning is an effective design because the ensemble of hair or feather follicles (modules) allows the generation of complexity, including regional variations and cyclic regeneration, giving the skin appendages a new lease on life. Spatial patterns include the arrangements of feathers and hairs in specific number, size, and spacing. We explore how a field of equivalent progenitor cells can generate periodically arranged modules based on genetic information, physical–chemical rules and developmental timing. Reconstitution experiments suggest a competitive equilibrium regulated by activators/inhibitors involving Turing reaction‐diffusion. Temporal patterns result from oscillating stem cell activities within each module (microenvironment regulation), reflected as growth (anagen) and resting (telogen) phases during the cycling of feather and hair follicles. Stimulating modules with activators initiates the spread of regenerative hair waves, while global inhibitors outside each module (macroenvironment) prevent this. Different wave patterns can be simulated by cellular automata principles. Hormonal status and seasonal changes can modulate appendage phenotypes, leading to ‘organ metamorphosis’, with multiple ectodermal organ phenotypes generated from the same precursors. We discuss potential novel evolutionary steps using this module‐based complexity in several amniote integument organs, exemplified by the spectacular peacock feather pattern. We thus explore the application of the acquired knowledge of patterning in tissue engineering. New hair follicles can be generated after wounding. Hairs and feathers can be reconstituted through self‐organization of dissociated progenitor cells. WIREs Dev Biol 2013, 2:97–112. doi: 10.1002/wdev.74 This article is categorized under: Establishment of Spatial and Temporal Patterns > Repeating Patterns and Lateral Inhibition Establishment of Spatial and Temporal Patterns > Cell Sorting and Boundary Formation Establishment of Spatial and Temporal Patterns > Regulation of Size, Proportion, and Timing

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  • Organoid HFs are periodically spaced throughout the epidermis, suggesting that appendage patterning mechanisms are preserved in organoids.

    “Moreover, organoid HFs are periodically spaced throughout the epidermis suggesting that appendage patterning mechanisms are preserved in organoids18.”

    From Hair-bearing human skin generated entirely from pluripotent stem cells (2020) · cites this paper as [18]

    Section 4, “Engineering of the Periodic Patterning Process” (page unavailable), reports evenly spaced hairs in reconstituted skin grown on a matrix on a mouse. This supports periodic spacing as a feature of hair formation, but the paper does not report hair follicles in organoids or establish that appendage-patterning mechanisms are preserved in organoids. (LLM, conf=0.87)

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References 90 · Cited by 63

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Authors
Chuong, C., Yeh, C., Ting‐Xin, J., & Widelitz, R.
Affiliations
University of Southern California (US)
Corresponding author
Chuong, Cheng‐Ming
ORCID
Venue
WIREs Developmental Biology
Publisher
Wiley
Published
2012-05-25
Volume
2
Issue
1
Pages
97-112
ISSN
  • 1759-7684 (ISSN-L)
  • 1759-7692
DOI
10.1002/wdev.74
PMC
PMC3607644
OpenAlex
W2125454296
Cited by
63
References
90
Citations by year
2026: 3 · 2025: 9 · 2024: 2 · 2023: 4 · 2022: 2 · 2021: 3 · 2020: 4 · 2019: 4 · 2018: 8 · 2017: 7 · 2016: 7 · 2015: 4 · 2014: 5 · 2013: 1
FWCI
0.62
Type
journal article
Language
en
Open access
Licence
onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations
  • Wiley Interdisciplinary Reviews Developmental Biology (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
National Institute of Arthritis and Musculoskeletal and Skin Diseases (AR 42177, R01AR042177, R01AR060306, R01AR047364)
Topics
  • Health Sciences › Medicine › Urology › Hair Growth and Disorders
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › melanin and skin pigmentation
Keywords
feather follicle, hair follicle, integument, activator-inhibitor systems, cellular automata, tissue engineering
MeSH terms
Animals, Feathers, Hair, Stem Cells, Body Patterning, Tissue Engineering, Integumentary System

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